Publications by authors named "Yizhi Liu"

287 Publications

A Peer-to-Peer Live-Streaming Intervention for Children During COVID-19 Homeschooling to Promote Physical Activity and Reduce Anxiety and Eye Strain: Cluster Randomized Controlled Trial.

J Med Internet Res 2021 04 30;23(4):e24316. Epub 2021 Apr 30.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.

Background: The COVID-19 pandemic has led to worldwide school closures, with millions of children confined to online learning at home. As a result, children may be susceptible to anxiety and digital eye strain, highlighting a need for population interventions.

Objective: The objective of our study was to investigate whether a digital behavior change intervention aimed at promoting physical activity could reduce children's anxiety and digital eye strain while undergoing prolonged homeschooling during the COVID-19 pandemic.

Methods: In this cluster randomized controlled trial, homeschooled grade 7 students at 12 middle schools in southern China were recruited through local schools and randomly assigned by the school to receive (1:1 allocation): (1) health education information promoting exercise and ocular relaxation, and access to a digital behavior change intervention, with live streaming and peer sharing of promoted activities (intervention), or (2) health education information only (control). The primary outcome was change in self-reported anxiety score. Secondary outcomes included change in self-reported eye strain and sleep quality.

Results: On March 16, 2020, 1009 children were evaluated, and 954 (94.5%) eligible children of consenting families were included in the intention-to-treat analysis. Children in the intervention (n=485, 6 schools) and control (n=469, 6 schools) groups were aged 13.5 (SD 0.5) years, and 52.3% (n=499) were male. The assigned interventions were completed by 896 children (intervention: n=467, 96.3%; control: n=429, 91.5%). The 2-week change in square-root-transformed self-reported anxiety scores was greater in the intervention (-0.23, 95% CI -0.27 to -0.20) vs control group (0.12, 95% CI 0.09-0.16; unadjusted difference -0.36, 95% CI -0.63 to -0.08; P=.02). There was a significant reduction in square-root-transformed eye strain in the intervention group (-0.08, 95% CI -0.10 to 0.06) compared to controls (0.07, 95% CI 0.05-0.09; difference -0.15, 95% CI -0.26 to -0.03; P=.02). Change in sleep quality was similar between the two groups.

Conclusions: This digital behavior change intervention reduced children's anxiety and eye strain during COVID-19-associated online schooling.

Trial Registration: ClinicalTrials.gov NCT04309097; http://clinicaltrials.gov/ct2/show/NCT04309097.
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http://dx.doi.org/10.2196/24316DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8092026PMC
April 2021

A specific RIP3 subpopulation of microglia promotes retinopathy through a hypoxia-triggered necroptotic mechanism.

Proc Natl Acad Sci U S A 2021 Mar;118(11)

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-Sen University, Guangzhou 510060, China;

Retinal neovascularization is a leading cause of severe visual loss in humans, and molecular mechanisms of microglial activation-driven angiogenesis remain unknown. Using single-cell RNA sequencing, we identified a subpopulation of microglia named sMG2, which highly expressed necroptosis-related genes Rip3 and Mlkl. Genetic and pharmacological loss of function demonstrated that hypoxia-induced microglial activation committed to necroptosis through the RIP1/RIP3-mediated pathway. Specific deletion of Rip3 gene in microglia markedly decreased retinal neovascularization. Furthermore, hypoxia induced explosive release of abundant FGF2 in microglia through RIP3-mediated necroptosis. Importantly, blocking signaling components of the microglia necropotosis-FGF2 axis largely ablated retinal angiogenesis and combination therapy with simultaneously blocking VEGF produced synergistic antiangiogenic effects. Together, our data demonstrate that targeting the microglia necroptosis axis is an antiangiogenesis therapy for retinal neovascular diseases.
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http://dx.doi.org/10.1073/pnas.2023290118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7980367PMC
March 2021

Glass polyamorphism in gallium: Two amorphous solid states and their transformation on the potential energy landscape.

J Chem Phys 2021 Apr;154(13):134503

International Center for Quantum Materials, School of Physics, Peking University, Beijing 100871, China.

Using the potential energy landscape (PEL) formalism and molecular dynamics simulations, we investigate a phase transformation between two amorphous solid states of gallium, namely, a low-density amorphous solid (LDA) and a high-density amorphous solid (HDA), and compare with its equilibrium counterpart, the liquid-liquid phase transition (LLPT). It is found that on the PEL, the signatures of the out-of-equilibrium LDA-HDA transition are reminiscent of those of the equilibrium LLPT in terms of pressure, inherent structure pressure, inherent structure energy, and shape function, indicating that the LDA-HDA transformation is a first-order-like transition. However, differences are also found between the out-of-equilibrium phase transition and the equilibrium one, for example, the path from LDA to HDA on the PEL cannot be accessed by the path from LDL to HDL. Our results also suggest that the signatures of the out-of-equilibrium transition in gallium are rather general features of systems with an accessible LLPT-not only systems with pairwise interactions but also those with many-body interactions. This finding is of crucial importance for obtaining a deeper understanding of the nature of transitions in the polyamorphic family.
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http://dx.doi.org/10.1063/5.0038058DOI Listing
April 2021

Generation of a homozygous CRISPR/Cas9-mediated knockout H9 hESC subline for the MERTK locus.

Stem Cell Res 2021 Mar 24;53:102310. Epub 2021 Mar 24.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-Sen University, Guangzhou, Guangdong, PR China. Electronic address:

MERTK mutations are associate with rod-cone dystrophies. To enable investigations into the mechanism of this disease, we generated a cell line resource of H9 human embryonic stem cells harboring large fragment deletion mutation in a homozygous state in exon 19 of the MERTK gene. This subline expressed pluripotent stem cell markers, presented a normal karyotype, and preserved the ability to differentiate into endodermal, mesodermal, and ectodermal lineages.
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http://dx.doi.org/10.1016/j.scr.2021.102310DOI Listing
March 2021

The MSP-RON pathway regulates liver fibrosis through transforming growth factor beta-dependent epithelial-mesenchymal transition.

Liver Int 2021 Mar 31. Epub 2021 Mar 31.

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China.

Background: Liver fibrosis is pathologically important in the liver cirrhosis progression. The epithelial-mesenchymal transition (EMT) is crucial for organ fibrosis. Macrophage-stimulating protein (MSP) and its receptor tyrosine kinase, RON, promote cellular EMT. However, their role in liver fibrosis is unclear. Here, we clarify the biological profile, potential mechanisms and therapeutic targets of the MSP-RON pathway in liver fibrosis.

Materials And Methods: Macrophage-stimulating protein expression and its correlation with clinicopathological characteristics of cirrhosis were evaluated in 57 clinical cases and a control group. The effect of MSP-RON pathway in liver fibrosis was determined in vitro and in vivo. The therapeutic effects of MSP or RON inhibition on liver fibrosis were evaluated in a mouse liver fibrosis model.

Results: Macrophage-stimulating protein is upregulated in liver cirrhosis, which was associated with poor patient prognosis. The MSP-RON pathway promoted hepatocytes EMT. MSP-RON-induced EMT depends on the transforming growth factor beta (TGF-β) pathway and is regulated by TGF-β inhibitors. In animal models, an MSP blocking antibody and a small molecule inhibitor of RON, BMS-777607, both inhibited liver fibrosis progression.

Conclusion: Our study revealed that MSP is an important biomarker in liver cirrhosis progression and can be used to prognose patients. The MSP-RON pathway promotes the EMT of hepatocytes and the progress of fibrosis via a TGF-β related pathway. Consequently, we identified a new treatment strategy for liver cirrhosis through targeted inhibition of MSP/RON. This research increases the understanding of EMT-modulated liver fibrosis and provides new insights into biomarkers and therapeutic targets of liver fibrosis.
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http://dx.doi.org/10.1111/liv.14892DOI Listing
March 2021

The distributions of crystalline lens tilt and decentration and associated factors in age related-cataract.

J Cataract Refract Surg 2021 Mar 5. Epub 2021 Mar 5.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, Guangdong, China.

Purpose: To investigate the characteristics and factors associated with crystalline lens tilt and decentration measured by Casia2 anterior segment optical coherence tomography (AS-OCT).

Setting: Zhongshan Ophthalmic Centre, Sun Yat-sen University, Guangzhou, China.

Design: This is a cross-sectional study.

Methods: One thousand and ninety-seven eyes of 1097 patients who plan to undergo cataract surgery were enrolled. All patients underwent a general ophthalmologic examination. Lens thickness (LT), front curvature radius (FCR), back curvature radius (BCR), lens equator diameter (LED), tilt, and decentration of preoperative crystalline lenses were measured by Casia2. Univariate and multivariate regression analyses were performed to evaluate the relationships between the tilt and decentration of crystalline lens with related factors.

Results: The natural crystalline lenses showed an average tilt of 5.16 degrees towards the inferotemporal direction and an average decentration of 0.22 mm towards the temporal direction. One hundred and nineteen eyes (10.85%) had a tilt greater than 7 degrees, and 89 eyes (8.11%) had a decentration more than 0.4 mm. Multivariate regression analysis showed larger decentration, thicker LT, shorter AL and FCR were associated with greater lens tilt (P<0.001, P=0.007, P=0.006 and P=0.003). Additionally, greater tilt, older and thinner LT were correlated with larger decentration (all P<0.001).

Conclusions And Relevance: Preoperative crystalline lens has a certain degree of tilt and decentration in age related-cataract. Greater tilt the crystalline lens is, larger decentration it is. Additionally, AL, FCR, LT and age also correlate to tilt and decentration.
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http://dx.doi.org/10.1097/j.jcrs.0000000000000631DOI Listing
March 2021

Identification of an intraocular microbiota.

Cell Discov 2021 Mar 9;7(1):13. Epub 2021 Mar 9.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, Guangdong, 510060, China.

The current dogma in ophthalmology and vision research presumes the intraocular environment to be sterile. However, recent evidence of intestinal bacterial translocation into the bloodstream and many other internal organs including the eyes, found in healthy and diseased animal models, suggests that the intraocular cavity may also be inhabited by a microbial community. Here, we tested intraocular samples from over 1000 human eyes. Using quantitative PCR, negative staining transmission electron microscopy, direct culture, and high-throughput sequencing technologies, we demonstrated the presence of intraocular bacteria. The possibility that the microbiome from these low-biomass communities could be a contamination from other tissues and reagents was carefully evaluated and excluded. We also provide preliminary evidence that a disease-specific microbial signature characterized the intraocular environment of patients with age-related macular degeneration and glaucoma, suggesting that either spontaneous or pathogenic bacterial translocation may be associated with these common sight-threatening conditions. Furthermore, we revealed the presence of an intraocular microbiome in normal eyes from non-human mammals and demonstrated that this varied across species (rat, rabbit, pig, and macaque) and was established after birth. These findings represent the first-ever evidence of intraocular microbiota in humans.
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http://dx.doi.org/10.1038/s41421-021-00245-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7943566PMC
March 2021

Microinvasive pars plana vitrectomy versus panretinal photocoagulation in the treatment of severe non-proliferative diabetic retinopathy (the VIP study): study protocol for a randomised controlled trial.

BMJ Open 2021 02 22;11(2):e043371. Epub 2021 Feb 22.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China

Introduction: Diabetic retinopathy (DR) is the main cause of adult visual impairment worldwide. Severe non-proliferative DR (sNPDR) is an important clinical intervention stage. Currently, panretinal photocoagulation (PRP) is the standard treatment for sNPDR. However, PRP alone cannot completely prevent NPDR progression. One explanation might be that PRP does not remove the detrimental vitreous that plays an important role in DR progression. Microinvasive pars plana vitrectomy (PPV) was shown to be a safe and effective method to treat late-stage proliferative DR (PDR) by completely removing the pathological vitreous. However, whether PPV is effective in controlling sNPDR remains unknown. In this trial, we aim to compare the effectiveness of microinvasive PPV with that of PRP for sNPDR progression control.

Methods And Analysis: This single centre, parallel group, randomised controlled trial aims to evaluate the clinical efficacy of microinvasive PPV in preventing the progression of sNPDR compared with PRP. A total of 272 adults diagnosed with sNPDR will be randomised 1:1 to the microinvasive PPV and PRP groups. The primary outcome is the disease progression rate, calculated as the rate of sNPDR progressed to PDR from baseline to 12 months after treatment. The secondary outcomes include the change in best-corrected visual acuity, re-treatment rate, diabetic macular oedema occurrence, change in central retinal thickness, change in the visual field, cataract occurrence and change in the quality of life.

Ethics And Dissemination: The Ethics Committee of Zhongshan Ophthalmic Center approved this study (2019KYPJ108). The results will be presented at scientific meetings and submitted for publication to peer-reviewed journals.

Trial Registration Number: NCT04103671.
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http://dx.doi.org/10.1136/bmjopen-2020-043371DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7903093PMC
February 2021

Core transcription regulatory circuitry orchestrates corneal epithelial homeostasis.

Nat Commun 2021 01 18;12(1):420. Epub 2021 Jan 18.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, 510060, Guangzhou, China.

Adult stem cell identity, plasticity, and homeostasis are precisely orchestrated by lineage-restricted epigenetic and transcriptional regulatory networks. Here, by integrating super-enhancer and chromatin accessibility landscapes, we delineate core transcription regulatory circuitries (CRCs) of limbal stem/progenitor cells (LSCs) and find that RUNX1 and SMAD3 are required for maintenance of corneal epithelial identity and homeostasis. RUNX1 or SMAD3 depletion inhibits PAX6 and induces LSCs to differentiate into epidermal-like epithelial cells. RUNX1, PAX6, and SMAD3 (RPS) interact with each other and synergistically establish a CRC to govern the lineage-specific cis-regulatory atlas. Moreover, RUNX1 shapes LSC chromatin architecture via modulating H3K27ac deposition. Disturbance of RPS cooperation results in cell identity switching and dysfunction of the corneal epithelium, which is strongly linked to various human corneal diseases. Our work highlights CRC TF cooperativity for establishment of stem cell identity and lineage commitment, and provides comprehensive regulatory principles for human stratified epithelial homeostasis and pathogenesis.
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http://dx.doi.org/10.1038/s41467-020-20713-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7814021PMC
January 2021

Single-cell analysis of nonhuman primate preimplantation development in comparison to humans and mice.

Dev Dyn 2021 Jan 15. Epub 2021 Jan 15.

Department of Human Genetics, David Geffen School of Medicine, UCLA, Los Angeles, California, USA.

Background: Genetic programs underlying preimplantation development and early lineage segregation are highly conserved across mammals. It has been suggested that nonhuman primates would be better model organisms for human embryogenesis, but a limited number of studies have investigated the monkey preimplantation development. In this study, we collect single cells from cynomolgus monkey preimplantation embryos for transcriptome profiling and compare with single-cell RNA-seq data derived from human and mouse embryos.

Results: By weighted gene-coexpression network analysis, we found that cynomolgus gene networks have greater conservation with human embryos including a greater number of conserved hub genes than that of mouse embryos. Consistently, we found that early ICM/TE lineage-segregating genes in monkeys exhibit greater similarity with human when compared to mouse, so are the genes in signaling pathways such as LRP1 and TCF7 involving in WNT pathway. Last, we tested the role of one conserved pre-EGA hub gene, SIN3A, using a morpholino knockdown of maternal RNA transcripts in monkey embryos followed by single-cell RNA-seq. We found that SIN3A knockdown disrupts the gene-silencing program during the embryonic genome activation transition and results in developmental delay of cynomolgus embryos.

Conclusion: Taken together, our study provided new insight into evolutionarily conserved and divergent transcriptome dynamics during mammalian preimplantation development.
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http://dx.doi.org/10.1002/dvdy.295DOI Listing
January 2021

Objective quantification of lens nuclear opacities using swept-source anterior segment optical coherence tomography.

Br J Ophthalmol 2021 Jan 13. Epub 2021 Jan 13.

Zhongshan Ophthalmic Center (ZIP: 510623), Sun Yat-Sen University, Guangzhou, China.

Background/aims: The primary objective is to quantify the lens nuclear opacity using swept-source anterior segment optical coherence tomography (SS-ASOCT) and to evaluate its correlations with Lens Opacities Classification System III (LOCS-III) system and surgical parameters. The secondary objective is to assess the diagnostic performance for hard nuclear cataract.

Methods: This cross-sectional study included 1222 patients eligible for cataract surgery (1222 eyes). The latest SS-ASOCT (CASIA-2) was used to obtain high-resolution lens images, and the average nuclear density (AND) and maximum nuclear density (MND) were measured by a custom ImageJ software. Spearman's correlations analysis was used to assess associations of AND/MND with LOCS-III nuclear scores, visual acuity and surgical parameters. The subjects were then split randomly (9:1) into the training dataset and validating dataset. Receiver operating characteristic curves and calibration curves were constructed for the classification on hard nuclear cataract.

Results: The AND and MND from SS-ASOCT images were significantly correlated with nuclear colour scores (AND: r=0.716; MND: r=0.660; p<0.001) and nuclear opalescence scores (AND: r=0.712; MND: r=0.655; p<0.001). The AND by SS-ASOCT images had the highest values of Spearman's r for preoperative corrected distance visual acuity (r=0.3131), total ultrasonic time (r=0.3481) and cumulative dissipated energy (r=0.4265). The nuclear density had good performance in classifying hard nuclear cataract, with area under the curves of 0.859 (0.831-0.886) for AND and 0.796 (0.768-0.823) for MND.

Conclusion: Objective and quantitative evaluation of the lens nuclear density using SS-ASOCT images enable accurate diagnosis of hard nuclear cataract.
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http://dx.doi.org/10.1136/bjophthalmol-2020-318334DOI Listing
January 2021

Melatonin protects inner retinal neurons of newborn mice after hypoxia-ischemia.

J Pineal Res 2021 Jan 11:e12716. Epub 2021 Jan 11.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.

Retinopathy of prematurity is a vision-threatening disease associated with retinal hypoxia-ischemia, leading to the death of retinal neurons and chronic neuronal degeneration. During this study, we used the oxygen-induced retinopathy mice model to mimic retinal hypoxia-ischemia phenotypes to investigate further the neuroprotective effect of melatonin on neonatal retinal neurons. Melatonin helped maintain relatively normal inner retinal architecture and thickness and preserve inner retinal neuron populations in avascular areas by rescuing retinal ganglion and bipolar cells, and horizontal and amacrine neurons, from apoptosis. Meanwhile, melatonin recovered visual dysfunction, as reflected by the improved amplitudes and implicit times of a-wave, b-wave, and oscillatory potentials. Additionally, elevated cleaved caspase-3 and Bax protein levels and reduced Bcl-2 protein levels in response to hypoxia-ischemia were diminished after melatonin treatment. Moreover, melatonin increased BDNF and downstream phospho-TrkB/Akt/ERK/CREB levels. ANA-12, a TrkB receptor antagonist, antagonized these melatonin actions and reduced melatonin-induced neuroprotection. Furthermore, melatonin rescued the reduction in melatonin receptor expression. This study suggests that melatonin exerted anti-apoptotic and neuroprotective effects in inner retinal neurons after hypoxia-ischemia, at least partly due to modulation of the BDNF-TrkB pathway.
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http://dx.doi.org/10.1111/jpi.12716DOI Listing
January 2021

Express Medicine-Potential for Home-Based Medical Care.

JAMA Ophthalmol 2021 Mar;139(3):269-270

Department of Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, Maryland.

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http://dx.doi.org/10.1001/jamaophthalmol.2020.5981DOI Listing
March 2021

Lens regeneration in humans: using regenerative potential for tissue repairing.

Ann Transl Med 2020 Nov;8(22):1544

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.

The crystalline lens is an important optic element in human eyes. It is transparent and biconvex, refracting light and accommodating to form a clear retinal image. The lens originates from the embryonic ectoderm. The epithelial cells at the lens equator proliferate, elongate and differentiate into highly aligned lens fiber cells, which are the structural basis for maintaining the transparency of the lens. Cataract refers to the opacity of the lens. Currently, the treatment of cataract is to remove the opaque lens and implant an intraocular lens (IOL). This strategy is inappropriate for children younger than 2 years, because a developing eyeball is prone to have severe complications such as inflammatory proliferation and secondary glaucoma. On the other hand, the absence of the crystalline lens greatly affects visual function rehabilitation. The researchers found that mammalian lenses possess regenerative potential. We identified lens stem cells through linear tracking experiments and designed a minimally invasive lens-content removal surgery (MILS) to remove the opaque lens material while preserving the lens capsule, stem cells and microenvironment. In infants with congenital cataract, functional lens regeneration in situ can be observed after MILS, and the prognosis of visual function is better than that of traditional surgery. Because of insufficient regenerative ability in humans, the morphology and volume of the regenerated lens cannot reach the level of a normal lens. The activation, proliferation and differentiation of lens stem cells and the alignment of lens fibers are regulated by epigenetic factors, growth factors, transcription factors, immune system and other signals and their interactions. The construction of appropriate microenvironment can accelerate lens regeneration and improve its morphology. The therapeutic concept of MILS combined with microenvironment manipulation to activate endogenous stem cells for functional regeneration of organs in situ can be extended to other tissues and organs with strong self-renewal and repair ability.
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http://dx.doi.org/10.21037/atm-2019-rcs-03DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7729322PMC
November 2020

Developmental characteristics of the cytokine profile in aqueous humor and its relationship with the inflammatory response in children.

Ann Transl Med 2020 Nov;8(22):1542

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.

Background: Although influencing the severity of postoperative intraocular inflammation of congenital cataract, the developmental characteristics of cytokine profile in the aqueous humor during childhood had not been described. And its relationship with the inflammatory response after intraocular surgery remained unsolved.

Methods: Preoperative aqueous humor samples were collected from 65 eyes of congenital cataract patients (CC group) and 13 eyes of age-related cataract patients (ARC group) from January 2015 to May 2017. The concentrations of 22 cytokines were measured. Differences in concentrations between the CC and ARC groups were described. Correlation analysis, least absolute shrinkage and selection operator (LASSO) and multivariate linear regression were then used to investigate the dynamic changes in the cytokine profile with age and their relationships with the postoperative inflammatory response.

Results: The concentrations of granulocyte colony stimulating factor (G-CSF), interferon (IFN)-α2, interleukin (IL)-1α and IL-7 were higher in the CC group than in the ARC group, while the concentrations of epidermal growth factor (EGF), granulocyte-macrophage colony stimulating factor (GM-CSF), IL-10, IL-12p70, IL-2, IL-3, IL-4, IL-5, IL-6, IL-8, and tumor necrosis factor (TNF)-α were more abundant in the ARC group (P<0.05). Within the CC group, the concentrations of EGF and IL-3 were positively correlated with age, while negative correlations were observed for monocyte chemotactic protein-1 (MCP-1) and IL-8 (P<0.05). Further multivariate analysis revealed that age was an independent associated factor of MCP-1 (β=-0.337, P<0.001). IL-3 (β=-0.490, P=0.006) and EGF (β=-0.415, P=0.044) were significantly correlated with the postoperative inflammatory response [evaluation of posterior capsule opacification (EPCO)] at 3 and 12 months after surgery, respectively.

Conclusions: This study demonstrated the dynamic change in the cytokine profile of the aqueous humor in children and its relationship with the postoperative inflammatory response. These findings can serve as the foundation for further investigation into the mechanisms that underlie the early development of intraocular immunology.
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http://dx.doi.org/10.21037/atm-19-2377DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7729307PMC
November 2020

Modified organized ophthalmology pre-internship in China.

Ann Transl Med 2020 Nov;8(21):1426

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.

Background: Medical pre-internship plays a crucial role in medical education promoting early involvement of students in clinical setting and helping them explore potential interest of specialty. However, there is currently no specifically designed pre-internship curriculum in China. Using ophthalmology as a pilot field, we have set up a modified organized pre-internship curriculum and evaluated its effectiveness and students' feedback in this study.

Methods: In this prospective noncomparative study, 42 junior undergraduate medical students were enrolled in the organized ophthalmology pre-internship. The effects of organized pre-internship on student performance were evaluated by difference of post- to pre-lecture scores by paired -test. The effects of baseline knowledge level and gender on performance improvement were analyzed by independent -test. Student satisfaction comparing organized pre-internship with traditional pre-internship was measured by questionnaire.

Results: The difference of post- to pre-lecture scores of all participants was 6.21±2.02 (P<0.0001). The improvement in post- to pre-lecture scores of students with low knowledge level (7.08±1.85) was significantly higher than that of students with high knowledge level (4.81±1.42) (P<0.0001). Gender did not influence student performance. The responses to the questionnaire showed that most of students were more satisfied with the organized pre-internship than traditional pre-internship.

Conclusions: The organized pre-internship significantly improved student performance and satisfaction. Performance improvement in students with low knowledge level was more obvious. Compared to traditional pre-internship, the organized pre-internship showed advantages in improving student performance as well as promoting learning enthusiasm. Instructors played an essential role in the organized pre-internship teaching system.
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http://dx.doi.org/10.21037/atm-20-1651DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7723654PMC
November 2020

Exploring the growth patterns of medical demand for eye care: a longitudinal hospital-level study over 10 years in China.

Ann Transl Med 2020 Nov;8(21):1374

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.

Background: The increasing demand for eye care inflicts a heavy burden on the eye care system. The uneven distribution of demand dynamically exacerbates the supply-demand imbalance. Systematic explorations of the growth patterns of the demand for eye care are needed to detect potential influences on the safety and quality of medical services.

Methods: This is an observational longitudinal study at the hospital level. We exported 8 million outpatient visit records over 10 years from the electronic health record (EHR) system of Zhongshan Ophthalmic Center (ZOC). The total visits to all levels of medical institutions in China were collected from the websites of the China National Statistics Bureau. The target 10-year period was from Jan 1, 2008, to Dec 31, 2017. Revisit intervals were analysed to assess the stickiness of patient demand. The proportions of non-local patients (from cities other than Guangzhou in Guangdong Province, or provinces other than Guangdong Province in China) were analysed to assess flowing demand liquidity.

Results: Visits to medical institutions continuously increased over the examined period (2008-2017) in China. Increasing patient visits and corresponding supplementation of doctors broke the supply-demand balance at ZOC. In terms of the temporal aspect, uneven distributions over cycles of weeks and years, referred to as Monday peaks and vacation peaks, became more evident during the examined period. With respect to geography, the coverage of demand sources expanded to the whole nation, and the flowing demand accounted for higher proportions at both the city and province levels. Subdepartments of ophthalmology had diverse growth speeds and proportions of flowing demand. Patients presented higher stickiness with shorter revisit intervals, and non-locals had higher stickiness than local patients.

Conclusions: The growth patterns of demand for eye care indicate potential challenges for ophthalmologists at the hospital level, including regular workload peaks, a wider range of patients with diverse cultural backgrounds, and higher stickiness of patients.
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http://dx.doi.org/10.21037/atm-20-2939DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7723615PMC
November 2020

Real-Time Imaging of Incision-Related Descemet Membrane Detachment During Cataract Surgery.

JAMA Ophthalmol 2021 02;139(2):150-155

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, Guangdong, China.

Importance: Incision-related Descemet membrane detachment (DMD) is a common complication of cataract surgery. Most postoperative severe DMD that leads to corneal decompensation originates from intraoperative incision-related DMD. It is important to determine the incidence, extent, and associated risk factors of intraoperative DMD at each step of surgery to help in formulating precise and effective prevention strategies.

Objectives: To investigate the intraoperative development of incision-site DMD associated with a 2.2-mm clear corneal incision during cataract surgery and to analyze its associated factors.

Design, Setting, And Participants: In this case series, consecutive, prospectively enrolled 133 patients with cataract 50 to 90 years of age (133 eyes) undergoing coaxial 2.2-mm clear corneal microincision phacoemulsification with intraocular lens (IOL) implantation between January 1 and March 31, 2019, at Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China, were studied.

Exposures: Coaxial 2.2-mm clear corneal microincision phacoemulsification with IOL implantation.

Main Outcomes And Measures: Real-time incidence and extent of intraoperative incision-related DMD at each step of surgery.

Results: Among 133 patients with cataracts (mean [SD] age, 72.3 [8.1] years; 77 [57.9%] female), DMD was encountered in 125 eyes (94.0%), occurring at the following steps: capsulorrhexis (2 [1.6%]), hydrodissection (7 [5.6%]), phacoemulsification (69 [55.2%]), irrigation-aspiration (44 [35.2%]), and IOL implantation (3 [2.4%]). The extent of DMD increased during the operation (mean [SD] difference between final and initial relative DMD length, 22.8% [1.4%]; 95% CI, 20.0-25.6; P < .001). Associations for the extent of DMD found in multivariate stepwise analyses included time of ultrasonography (β = 0.34; 95% CI, 0.17-0.50; P < .001), equivalent mean ultrasonic power (β = 87.8; 95% CI, 19.1-156.4; P = .01), and the presence of DMD at the anterior and posterior wound margins (coefficient = 16.7; 95% CI, 6.4-26.9; P = .002).

Conclusions And Relevance: The results of this case series suggest that friction of surgical instruments has the greatest association with incisional DMD. Decreasing ultrasonic energy and phacoemulsification time may reduce the severity of incisional DMD.
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http://dx.doi.org/10.1001/jamaophthalmol.2020.5396DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7729572PMC
February 2021

Accuracy of new-generation intraocular lens calculation formulas in eyes undergoing combined silicone oil removal and cataract surgery.

J Cataract Refract Surg 2021 May;47(5):593-598

From the State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, Guangdong, China.

Purpose: To compare the performance of new-generation and traditional intraocular lens (IOL) calculation formulas in eyes undergoing combined silicone oil (SO) removal and cataract surgery and to evaluate the prediction accuracy of Wang-Koch (WK) adjustment in SO-filled long eyes.

Setting: Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.

Design: Retrospective consecutive case-series study.

Methods: New-generation formulas (Barrett Universal II, Emmetropia Verifying Optical, Kane, and Ladas Super formulas) and traditional formulas (Haigis, Hoffer Q, Holladay 1, and SRK/T formulas) were compared. The performance of WK adjustment was assessed in eyes with axial length more than 26 mm. The median absolute error (MedAE) was the main parameter to evaluate the accuracy of formulas.

Results: A total of 211 participants (211 eyes) who underwent combined SO removal and phacoemulsification with IOL implantation were included. Four new-generation formulas displayed statistically significant lower MedAE (0.32 to 0.35 diopter [D]) and higher percentage of eyes within ±1.00 D of prediction error (85.31% to 87.20%) compared with those of the traditional formulas (MedAE: 0.39 to 0.50 D; ±1.00 D: 81.04% to 81.99%, P < .05). For SO-filled long eyes, all traditional formulas showed hyperopic bias (0.36 to 0.65 D, P < .05), except for Haigis formula (0.28 D, P = .083), and this bias could be corrected by WK adjustment (P > .05). EVO formula displayed the lowest MedAE both in total (0.32 D) and in long eyes (0.33 D).

Conclusions: New-generation formulas and traditional formulas with WK adjustment showed satisfactory prediction accuracy in eyes undergoing combined SO removal and cataract surgery. EVO formula displayed the highest accuracy.
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http://dx.doi.org/10.1097/j.jcrs.0000000000000509DOI Listing
May 2021

A decision aid to facilitate informed choices among cataract patients: A randomized controlled trial.

Patient Educ Couns 2020 Nov 9. Epub 2020 Nov 9.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China. Electronic address:

Objective: To assess the effect of a patient decision aid on the quality of decision-making for patients with age-related cataracts.

Methods: 773 patients with cataracts aged 50-80 years were randomly assigned to receive either the intervention decision aid (including standard information, quantitative information on the possible outcomes of cataract surgery and a value clarification exercise) or the control booklet (including standard information). The primary outcome was informed choice (defined as adequate knowledge and congruency between attitudes and surgical intentions), which was assessed at 2 weeks after intervention via a telephone interview.

Results: The decision aid increased the proportion of participants making an informed choice, from 5.68 % in the control group to 27.7 % in the intervention group (P < 0.001). Compared with controls, more participants in the intervention group had adequate overall knowledge about cataract surgery (36.8 % vs. 8.79 % in controls; P < 0.001), and fewer participants intended to undergo surgery (22.5 % vs. 34.1 % in controls; P < 0.001).

Conclusion: Use of the patient decision aid may increase the proportion of patients making informed choices. Importantly, it might also reduce the acceptance of operations.

Practice Implications: Patient decision aids represent a simple and low-cost tool to facilitate informed choice among patients with cataracts.
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http://dx.doi.org/10.1016/j.pec.2020.10.036DOI Listing
November 2020

Autophagy inhibition attenuates TGF-β2-induced epithelial-mesenchymal transition in lens epithelial cells.

Life Sci 2021 Jan 10;265:118741. Epub 2020 Nov 10.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China.

Aims: Autophagy has been reported to play an essential role in fibrotic disorders. Known as fibrotic cataract, posterior capsular opacification (PCO) result from pathological epithelial-mesenchymal transition (EMT) of lens epithelial cells (LECs). This study aims to identify the role and potential mechanism of autophagy in TGF-β2-induced EMT in LECs.

Main Methods: Primary rabbit LECs were treated with TGF-β2 to induce EMT as a model of fibrotic cataract in vitro. 3-methyladenine, chloroquine, bafilomycin A1, and gene silencing of autophagy-related protein 7 (ATG7) were treated in LECs for autophagy inhibition, while rapamycin was utilized for autophagy activation. The expression levels of EMT/autophagy-associated markers were analyzed by qRT-PCR, western blotting, immunofluorescence and transmission electron microscopy. We additionally examined cell migration ability with transwell migration assay and wound healing assay.

Key Findings: TGF-β2 promoted autophagy flux during EMT progression of LECs in a time-dependent manner. Autophagy activation by rapamycin enhanced TGF-β2-triggered fibrogenic responses and cell migration in LECs, whereas pharmacological inhibition of autophagy alleviated TGF-β2-induced increases of EMT markers and cell migration of LECs. In addition, the phosphorylation of Smad2/3 induced by TGF-β2 was suppressed through autophagy inhibition, while it was promoted upon autophagy activation, indicating that TGF-β2/Smad signaling was involved in the modulation of autophagy on EMT in LECs. Furthermore, ATG7-silenced LECs exerted anti-fibrosis effect induced by TGF-β2 through downregulation of autophagy.

Significance: Intervention/inhibition of autophagy could attenuate TGF-β2-induced EMT in LECs, which provides autophagy-related insights on preventing and treating the fibrotic cataract or other fibrotic diseases.
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http://dx.doi.org/10.1016/j.lfs.2020.118741DOI Listing
January 2021

Impact of cataract screening integrated into establishment of resident health record on surgical output in a rural area of south China.

Ann Transl Med 2020 Oct;8(19):1222

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.

Background: Strategy establishment for improving the efficiency and sustainability of cataract surgical output is important for eye health program. The aim of this study is to assess the three-year output of a novel cataract screening model integrated into establishment of resident health record in a rural area of south China.

Methods: A novel cataract screening model which combined private hospital screening and annual health examinations for establishing resident health record from January 2015 to December 2017 was implemented in an eye hospital in Zhaoqing, Guangdong, China. Demographic information and cataract surgery rate were recorded. A subgroup of patients who underwent cataract surgery were surveyed by customized questionnaire to determine the accessibility to eye-care services and barriers to cataract surgery.

Results: A total of 172,814 people aged ≥50 years in Zhaoqing were screened and 56,292 (32.57%) people were diagnosed with age-related cataract, among whom 18,422 (10.66%) with a best corrected visual acuity (BCVA) less than 20/63 were recommended for cataract surgery. Surgery was performed on 11,105 (60.28%) recommended patients. After the introduction of this screening model, the cataract surgical rate (CSR) in this area dramatically increased to 2,739/million/y (by 1.8 folds) in 2015 and 3,678/million/y (by 2.4 folds) in 2017, compared with that in 2014 (1,520/million/y). Accessibility to eye-care service was improved, and the main reason for not receiving cataract surgery changed from misconception of cataract to having good vision in the fellow eye after 3 years of screening.

Conclusions: This study documented the benefit of a novel cataract screening model integrated into establishment of resident health record in rural China, which may serve as a cost-effective, practicable, and sustainable strategy to disseminate cataract knowledge and eliminate cataract blindness.
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http://dx.doi.org/10.21037/atm-20-396DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7607123PMC
October 2020

High-dimensional single-cell analysis reveals the immune characteristics of COVID-19.

Am J Physiol Lung Cell Mol Physiol 2021 01 4;320(1):L84-L98. Epub 2020 Nov 4.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, People's Republic of China.

Coronavirus disease 2019 (COVID-19), driven by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), was declared a global pandemic in March 2020. Pathogenic T cells and inflammatory monocytes are regarded as the central drivers of the cytokine storm associated with the severity of COVID-19. In this study, we explored the characteristic peripheral cellular profiles of patients with COVID-19 in both acute and convalescent phases by single-cell mass cytometry (CyTOF). Using a combination of algorithm-guided data analyses, we identified peripheral immune cell subsets in COVID-19 and revealed CD4 T-cell depletion, T-cell differentiation, plasma cell expansion, and the reduced antigen presentation capacity of innate immunity. Notably, COVID-19 induces a dysregulation in the balance of monocyte populations by the expansion of the monocyte subsets. Collectively, our results represent a high-dimensional, single-cell profile of the peripheral immune response to SARS-CoV-2 infection.
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http://dx.doi.org/10.1152/ajplung.00355.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7869955PMC
January 2021

Ontogenesis of the tear drainage system requires Prickle1-driven polarized basement membrane deposition.

Development 2020 11 30;147(22). Epub 2020 Nov 30.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China

In terrestrial animals, the lacrimal drainage apparatus evolved to serve as conduits for tear flow; however, little is known about the ontogenesis of this system. Here, we define the anatomy of the fully formed tear duct in mice, characterize crucial morphogenetic events for the development of tear duct components and identify the site for primordial tear duct (PTD) initiation. We report that the PTD originates from the orbital lacrimal lamina, a junction formed by the epithelia of the maxillary and lateral nasal processes. We demonstrate that , a key component of planar cell polarity signaling, is expressed in progenitors of the PTD and throughout tear duct morphogenesis. Disruption of stalls tear duct elongation; in particular, the loss of basement membrane deposition and aberrant cytoplasmic accumulation of laminin are salient. Altered cell adhesion, cytoskeletal transport systems, vesicular transport systems and cell axis orientation in mutants support the role of in planar cell polarity. Taken together, our results highlight a crucial role of Prickle1-mediated polarized basement membrane secretion and deposition in PTD elongation.
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http://dx.doi.org/10.1242/dev.191726DOI Listing
November 2020

Malformation of Tear Ducts Underlies the Epiphora and Precocious Eyelid Opening in Prickle 1 Mutant Mice: Genetic Implications for Tear Duct Genesis.

Invest Ophthalmol Vis Sci 2020 11;61(13)

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou City, China.

Purpose: Obstruction of the tear drainage causes a range of ocular surface disorders. Hitherto, the genetics of tear duct development and obstruction has been scarcely explored, and related animal models are lacking. This study aims to study the potential role of the Wnt/PCP pathway mediated by Prickle 1 in tear duct development and diseases.

Methods: A severe hypomorphic Prickle 1 mutant was generated. Histology and immunohistochemistry were performed to compare wild type, Prickle 1 hypomorphic, and null mutant tear ducts. In situ hybridization was conducted to identify the signaling components in the developing tear ducts. Three-dimensional (3D) reconstruction was used to detect the human embryonic tear duct.

Results: Here, we report that a severe Prickle 1 hypomorph mouse line exhibited epiphora. This phenotype was due to the blockage of the tear drainage by incompletely formed nasolacrimal duct (NLD) and lacrimal canaliculi (LC), which also causes precocious eyelid opening. We observed a dose-dependent requirement of Prickle 1 for tear duct outgrowth. An investigation of the expression of Wnt/PCP core genes demonstrated a subset of PCP signaling components expressed in the developing tear duct. Furthermore, Prickle 1 is not required for the expression of Fgfr2/Fgf10 and p63 genes, which are associated with the NLD and LC hypoplasia in humans. Last, we showed that Prickle 1 expression in the developing tear drainage system is conserved between mice and humans.

Conclusions: The study suggests that malformed tear ducts caused by disruption of Prickle 1 underlies the epiphora and precocious eyelid opening.
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http://dx.doi.org/10.1167/iovs.61.13.6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7645213PMC
November 2020

Generation of a homozygous CRISPR/Cas9-mediated knockout H9 hESC subline for the CRB1 locus.

Stem Cell Res 2020 12 16;49:102057. Epub 2020 Oct 16.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-Sen University, Guangzhou, Guangdong, People's Republic of China. Electronic address:

Mutations in the CRB1 gene reportedly cause early-onset autosomal recessive retinitis pigmentosa (RP), which can result in severe loss of vision at an early age. To investigate the mechanism of CRB1-knockout (CRB1) induced RP, we generated a subline of H9 human embryonic stem cells harboring frame shift mutations in a homozygous state in exon 2 of the CRB1 gene. This subline expressed pluripotent stem cell markers, presented a normal karyotype, and preserved the ability to differentiate into endodermal, mesodermal, and ectodermal lineages.
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http://dx.doi.org/10.1016/j.scr.2020.102057DOI Listing
December 2020

Improved Design via Simulation of Micro-Modified PVDF and its Copolymer Energy Harvester with High Electrical Outputs.

Sensors (Basel) 2020 Oct 15;20(20). Epub 2020 Oct 15.

Harbin Institute of Technology, Department of Astronautic Science and Mechanics, Harbin 150001, China.

In this work, micro-modified polyvinylidene fluoride (PVDF) and its copolymer poly(vinylidene-trifluoroethylene) (P(VDF-TrFE)) with salient enhancement in current output are demonstrated. The influence of surface-modified structure characteristics on electrical properties of energy harvester is systematically analyzed based on the finite element method. For vertical load mode, eight structures consisting of banded and disjunctive groups are compared to evaluate the voltage performance. The cylinder is proved to be the best structure of 3.25 V, compared to the pristine structure of 0.99 V (P(VDF-TrFE)). The relevant experiment has been done to verify the simulation. The relationship between radius, height, force and distance to the voltage output of the cylinder allocation is discussed. For periodical changing load mode, the cylinder modified structure shows a conspicuous enhancement in current output. The suitable resistance, current-voltage and frequency, the relationship between loading speed and current, and the ductility of current loading are studied. For 30 kHz, the peak current is 20 times larger than the flat plate structure. Tip shape mode and fusiform shape mode are found, which show the different shapes of the peak current-frequency curves. Four electrical loading circuit properties are also discussed: the suitable resistance of the system, synchronism of current and voltage, time delay nature of energy harvester and current-loading relationship. The simulation results can provide some theoretical basis for designing the energy harvester and piezoelectric nanogenerator (PENG).
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http://dx.doi.org/10.3390/s20205834DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7602673PMC
October 2020

Single-cell RNA cap and tail sequencing (scRCAT-seq) reveals subtype-specific isoforms differing in transcript demarcation.

Nat Commun 2020 10 13;11(1):5148. Epub 2020 Oct 13.

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-Sen University, Guangzhou, China.

The differences in transcription start sites (TSS) and transcription end sites (TES) among gene isoforms can affect the stability, localization, and translation efficiency of mRNA. Gene isoforms allow a single gene diverse functions across different cell types, and isoform dynamics allow different functions over time. However, methods to efficiently identify and quantify RNA isoforms genome-wide in single cells are still lacking. Here, we introduce single cell RNA Cap And Tail sequencing (scRCAT-seq), a method to demarcate the boundaries of isoforms based on short-read sequencing, with higher efficiency and lower cost than existing long-read sequencing methods. In conjunction with machine learning algorithms, scRCAT-seq demarcates RNA transcripts with unprecedented accuracy. We identified hundreds of previously uncharacterized transcripts and thousands of alternative transcripts for known genes, revealed cell-type specific isoforms for various cell types across different species, and generated a cell atlas of isoform dynamics during the development of retinal cones.
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http://dx.doi.org/10.1038/s41467-020-18976-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7555861PMC
October 2020

The Structure of the Lens and Its Associations with the Visual Quality.

BMJ Open Ophthalmol 2020 18;5(1):e000459. Epub 2020 Sep 18.

State Key Laboratory of Ophthalmology, Sun Yat-Sen University Zhongshan Ophthalmic Center, Guangzhou, China.

In humans, the lens is the organ with the ability to change morphology and refractive power, designated as accommodation, to focus light from various distances and obtain clear retinal image. The accommodative ability of the lens depends on its structure and biological parameters. The lens grows throughout the life, forming specific lens sutures and a unique gradient refractive index, and possesses regenerative ability under certain circumstances. Minimally invasive lens surgery that preserves endogenous lens epithelial stem/progenitor cells (LECs) can achieve functional lens regeneration in humans. The lens is the main source of intraocular aberration, especially intraocular higher-order aberrations (IHOAs) which is found to be binocularly symmetrical in phakic eyes. There is a compensation mechanism between corneal aberrations and lens aberrations. Therefore, the structure and the biological parameters of the lens, the binocular relationship of the lens and the correlation between the lens and cornea affect visual quality. This paper summarises the above findings and their current and potential applications in refractive surgeries, providing a comprehensive understanding of the lens as a strong determinant of visual quality in the optical system.
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http://dx.doi.org/10.1136/bmjophth-2020-000459DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7511618PMC
September 2020