Publications by authors named "Luis Antonio Justulin"

27 Publications

  • Page 1 of 1

Exposure to Bacteriophages T4 and M13 Increases Integrin Gene Expression and Impairs Migration of Human PC-3 Prostate Cancer Cells.

Antibiotics (Basel) 2021 Oct 3;10(10). Epub 2021 Oct 3.

Laboratory of Extracellular Matrix Biology, Department of Structural and Functional Biology, Institute of Biosciences of Botucatu, Sao Paulo State University (UNESP), Botucatu 18618-689, SP, Brazil.

The interaction between bacteriophages and integrins has been reported in different cancer cell lines, and efforts have been undertaken to understand these interactions in tumor cells along with their possible role in gene alterations, with the aim to develop new cancer therapies. Here, we report that the non-specific interaction of T4 and M13 bacteriophages with human PC-3 cells results in differential migration and varied expression of different integrins. PC-3 tumor cells (at 70% confluence) were exposed to 1 × 10 pfu/mL of either lytic T4 bacteriophage or filamentous M13 bacteriophage. After 24 h of exposure, cells were processed for a histochemical analysis, wound-healing migration assay, and gene expression profile using quantitative real-time PCR (qPCR). qPCR was performed to analyze the expression profiles of integrins , , , , and . Our findings revealed that PC-3 cells interacted with T4 and M13 bacteriophages, with significant upregulation of , , , genes after phage exposure. PC-3 cells also exhibited reduced migration activity when exposed to either T4 or M13 phages. These results suggest that wildtype bacteriophages interact non-specifically with PC-3 cells, thereby modulating the expression of integrin genes and affecting cell migration. Therefore, bacteriophages have future potential applications in anticancer therapies.
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http://dx.doi.org/10.3390/antibiotics10101202DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8532711PMC
October 2021

Syndecan Family Gene and Protein Expression and Their Prognostic Values for Prostate Cancer.

Int J Mol Sci 2021 Aug 12;22(16). Epub 2021 Aug 12.

Department of Structural and Functional BIology, Institute of Bioscience of Botucatu (IBB), São Paulo State University, Botucatu 18618-689, SP, Brazil.

Prostate cancer (PCa) is the leading cause of cancer-associated mortality in men, and new biomarkers are still needed. The expression pattern and protein tissue localization of proteoglycans of the syndecan family (SDC 1-4) and syntenin-1 (SDCBP) were determined in normal and prostatic tumor tissue from two genetically engineered mouse models and human prostate tumors. Studies were validated using SDC 1-4 and SDCBP mRNA levels and patient survival data from The Cancer Genome Atlas and CamCAP databases. RNAseq showed increased expression of in mouse Pca and upregulation of expression and downregulation of and when compared to the normal prostatic tissue in mouse tumors. These changes were confirmed by immunohistochemistry. In human PCa, SDC 1-4 and SDCBP immunostaining showed variable localization. Furthermore, Kaplan-Meier analysis showed that patients expressing SDC3 had shorter prostate-specific survival than those without SDC3 expression (log-rank test, = 0.0047). Analysis of the MSKCC-derived expression showed that and overexpression is predictive of decreased biochemical recurrence-free survival ( = 0.0099 and = 0.045, respectively), and overexpression is predictive of increased biochemical recurrence-free survival ( = 0.035). SDC4 overexpression was associated with a better prognosis, while SDC1 and SDC3 were associated with more aggressive tumors and a worse prognosis.
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http://dx.doi.org/10.3390/ijms22168669DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8395474PMC
August 2021

Maternal protein restriction changes structural and metabolic gene expression in the skeletal muscle of aging offspring rats.

Histol Histopathol 2021 Apr 12:18337. Epub 2021 Apr 12.

Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil.

Maternal protein restriction affects postnatal skeletal muscle physiology with impacts that last through senility. To investigate the morphological and molecular characteristics of skeletal muscle in aging rats subjected to maternal protein restriction, we used aged male rats (540 days old) born of dams fed a protein restricted diet (6% protein) during pregnancy and lactation. Using morphological, immunohistochemical and molecular analyses, we evaluated the soleus (SOL) and extensor digitorum longus (EDL) muscles, muscle fiber cross-sectional area (CSA) (n=8), muscle fiber frequency (n=5) and the gene expression (n=8) of the oxidative markers (succinate dehydrogenase-Sdha and citrate synthase-CS) and the glycolytic marker (lactate dehydrogenase-Ldha). Global transcriptome analysis (n=3) was also performed to identify differentially regulated genes, followed by gene expression validation (n=8). The oxidative SOL muscle displayed a decrease in muscle fiber CSA (*p<0.05) and in the expression of oxidative metabolism marker Sdha (***p<0.001), upregulation of the anabolic Igf-1 (**p<0.01), structural Chad (**p<0.01), and Fmod (*p<0.05) genes, and downregulation of the Hspb7 (**p<0.01) gene. The glycolytic EDL muscle exhibited decreased IIA (*p<0.05) and increased IIB (*p<0.05) fiber frequency, and no changes in muscle fiber CSA or in the expression of oxidative metabolism genes. In contrast, the gene expression of Chad (**p<0.01) was upregulated and the Myog (**p<0.01) gene was downregulated. Collectively, our morphological, immunohistochemical and molecular analyses showed that maternal protein restriction induced changes in the expression of metabolic, anabolic, myogenic, and structural genes, mainly in the oxidative SOL muscle, in aged offspring rats.
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http://dx.doi.org/10.14670/HH-18-337DOI Listing
April 2021

The essential oil from Baccharis trimera (Less.) DC improves gastric ulcer healing in rats through modulation of VEGF and MMP-2 activity.

J Ethnopharmacol 2021 May 15;271:113832. Epub 2021 Jan 15.

Department of Structural and Functional Biology (Physiology), Biosciences Institute, UNESP-São Paulo State University, CEP, 18618-689, Botucatu, São Paulo, Brazil. Electronic address:

Ethnopharmacological Relevance: Baccharis trimera (Less.) DC known as "carqueja" in Brazil has been acknowledged as a medicinal plant in folk medicine for the treatment of stomach aches and gastrointestinal disorders.

Aim Of The Study: The present study aimed to evaluate the gastroprotective and healing effects of essential oil from B. trimera (EOBT) against gastric ulcer lesions caused by absolute ethanol and acetic acid, respectively, and to identify the mechanism of action of this essential oil in male Wistar rats.

Materials And Methods: The plant material used to obtain EOBT was collected in the southern region of Brazil and was analyzed by chromatography-mass spectrometry (GCMS) demonstrate its characteristic chemical composition, with carquejyl acetate as its main component. Different doses of EOBT (50, 100, and 200 mg/kg) were administered orally in male Wistar rats as an acute treatment against absolute ethanol-induced gastric lesions. The gastric healing effect of EOBT (100 mg/kg) was evaluated once a day after 7, 10, and 14 days of treatment. After treatment, the stomachs of rats from all groups were collected to measure the lesion area (mm), the activity of myeloperoxidase (MPO), and the relative expression of caspases -3, -8, -9, cyclooxygenase-1 (COX-1), cyclooxygenase-2 (COX-2), vascular endothelial growth factor (VEGF), and epidermal growth factor (EGF). The zymography method was used to elucidate the activity of matrix metalloproteinase-2 (MMP-2) and -9 (MMP-9) in the healing action of EOBT. We also analyzed toxicological parameters (body weight evolution and biochemical parameters) that could result after treatment with this essential oil for 14 days.

Results: Pretreatment with EOBT (100 and 200 mg/kg) significantly decreased the severity of gastric damage induced by absolute ethanol and decreased MPO activity in gastric tissue. After 10 and 14 days of treatment with EOBT (100 mg/kg) once a day, the lesion area was significantly reduced by 61% and 65.5%, respectively, compared to the negative control group. The gastric healing effect of EOBT was followed by a decrease in the expression of COX-1 compared to that in the negative control group. Notably, treatment with EOBT for 14 days increased the expression of VEGF compared to that using an anti-ulcer drug (lansoprazole). Additionally, analyses of MMP-2 and MMP-9 activities in the gastric mucosa confirmed the accelerated gastric healing effect of EOBT, with a significant decrease in the activity of pro-MMP-2. No sign of toxicity was observed after treatment with EOBT for 14 consecutive days.

Conclusion: These findings indicated that EOBT was effective in preventing and accelerating ulcer healing by decreasing MPO activity, increasing VEGF expression, and decreasing MMP-2 activity. These actions collectively contribute to the rapid recovery of gastric mucosa following treatment with EOBT, without any observed toxicity.
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http://dx.doi.org/10.1016/j.jep.2021.113832DOI Listing
May 2021

Maternal protein restriction impairs nutrition and ovarian histomorphometry without changing p38MAPK and PI3K-AKT-mTOR signaling in adult rat ovaries.

Life Sci 2021 Jan 29;264:118693. Epub 2020 Oct 29.

Department of Structural and Functional Biology, Institute of Biosciences (IBB), São Paulo State University-UNESP, 18618-689, Botucatu, SP, Brazil. Electronic address:

Aims: Because an adequate protein supply is detrimental for the maintenance of folliculogenesis and ovulation, we evaluated the impact of maternal low protein diet on nutritional parameters, estrous cycle, ovarian histomorphometry, and on the expression of metabolic and survival signaling molecules in different follicular stages.

Main Methods: Twenty Wistar pregnant rats were divided into two groups: the normoprotein (NP) group, composed of animals that received 17% protein, and a low-protein (LP) group, composed of animals that received 6% protein during gestation and lactation period. After weaning, female rats were fed with standard diet until the 120-days-old.

Key Findings: LP animals showed reduced body mass index, total body weight, energy intake, feed efficiency, and visceral fat. The ovarian tissue presented vascular congestion and fat accumulation in the medulla, followed by a significant reduction in the amount of primordial and primary follicles. In addition, the number of atretic follicles was higher in LP than in NP animals. Maternal undernutrition also resulted in increased levels of estradiol (E2) and progesterone (P4) while testosterone (T) was unchanged in the offspring. Although discrete changes in p38MAPK and in PI3K-AKT-mTOR immunostaining were observed in the ovarian follicles and corpus luteum in LP, no differences were found at their protein levels.

Significance: Maternal protein restriction alters estrous cycle and histomorphometry of the offspring's ovary without changing the levels of intracellular regulatory molecules in adulthood. These morphofunctional changes may alter reproductive performance in female offspring, highlighting maternal dietary conditions as an important factor for offspring reproductive health.
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http://dx.doi.org/10.1016/j.lfs.2020.118693DOI Listing
January 2021

Identification of potential molecular pathways involved in prostate carcinogenesis in offspring exposed to maternal malnutrition.

Aging (Albany NY) 2020 10 13;12(20):19954-19978. Epub 2020 Oct 13.

Department of Structural and Functional Biology, Institute of Biosciences, Sao Paulo State University (UNESP), Botucatu 18618-689, São Paulo, Brazil.

The developmental origins of health and disease concept links adult diseases with early-life exposure to inappropriate environmental conditions. Intrauterine and postnatal malnutrition may lead to an increased incidence of type 2 diabetes, obesity, and cardiovascular diseases. Maternal malnutrition (MM) has also been associated with prostate carcinogenesis. However, the molecular mechanisms associated with this condition remain poorly understood. Using a proteomic analysis, we demonstrated that MM changed the levels of proteins associated with growth factors, estrogen signaling, detoxification, and energy metabolism in the prostate of both young and old rats. These animals also showed increased levels of molecular markers of endoplasmic reticulum function and histones. We further performed an analysis that identified commonly deregulated proteins in the ventral prostate of old rats submitted to MM with a mouse model and patients with prostate cancer. In conclusion, our results demonstrated that estrogenic signaling pathways, endoplasmic reticulum functions, energy metabolism, and molecular sensors of protein folding and Ca2+ homeostasis, besides histone, and RAS-GTPase family appear to be involved in this process. Knowledge of these factors may raise discussions regarding the role of maternal dietary intervention as a public policy for the lifelong prevention of chronic diseases.
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http://dx.doi.org/10.18632/aging.104093DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7655221PMC
October 2020

A meta-analysis of microRNA networks regulated by melatonin in cancer: Portrait of potential candidates for breast cancer treatment.

J Pineal Res 2020 Nov 19;69(4):e12693. Epub 2020 Sep 19.

Department of Cell Systems and Anatomy, UT Health, San Antonio, TX, USA.

Melatonin is a ubiquitous molecule with a broad spectrum of functions including widespread anti-cancer activities. Identifying how melatonin intervenes in complex molecular signaling at the gene level is essential to guide proper therapies. Using meta-analysis approach, herein we examined the role of melatonin in regulating the expression of 46 microRNAs (miRNAs) and their target genes in breast, oral, gastric, colorectal, and prostate cancers, and glioblastoma. The deregulated miRNA-associated target genes revealed their involvement in the regulation of cellular proliferation, differentiation, apoptosis, senescence, and autophagy. Melatonin changes the expression of miRNA-associated genes in breast, gastric, and oral cancers. These genes are associated with cellular senescence, the hedgehog signaling pathway, cell proliferation, p53 signaling, and the hippo signaling pathway. Conversely, colorectal and prostate cancers as well as glioblastoma and oral carcinoma present a clear pattern of less pronounced changes in the expression of miRNA-associated genes. Most notably, colorectal cancer displayed a unique molecular change in response to melatonin. Considering breast cancer network complexity, we compared the genes found during the meta-analysis with RNA-Seq data from breast cancer-bearing mice treated with melatonin. Mechanistically, melatonin upregulated genes associated with immune responses and apoptotic processes, whereas it downregulated genes involved in cellular aggressiveness/metastasis (eg, mitosis, telomerase activity, and angiogenesis). We further characterized the expression profile of our gene subsets with human breast cancer and found eight upregulated genes and 16 downregulated genes that were appositively correlated with melatonin. Our results pose a multi-dimension network of tumor-associated genes regulated by miRNAs potentially targeted by melatonin.
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http://dx.doi.org/10.1111/jpi.12693DOI Listing
November 2020

Panax ginseng metabolite (GIM-1) modulates the effects of monobutyl phthalate (MBP) on the GPR30/GPER1 canonical pathway in human Sertoli cells.

Reprod Toxicol 2020 Jul 16;96:209-215. Epub 2020 Jul 16.

São Paulo State University (UNESP), Institute of Biosciences, Department of Structural and Functional Biology, Botucatu, SP, 18618-689, Brazil. Electronic address:

This study was performed to evaluate the effect of monobutyl phthalate (MBP) on GPR30-activated pathways in Sertoli cells. Additionally, we tested if GIM-1 (Panax ginseng metabolite) modulates MBP action. Human Sertoli cells (HSeC lineage) were exposed to MBP and/or GIM-1 for 30 min, 1, 12, and 48 h. Four experimental treatments were performed: control (DEMEM/F12 medium), MBP, GIM-1, and MBP + GIM-1. The results indicate that MBP activates GPR30, PKA, Src, EGFR, and the ERK1/2 proteins, while GIM-1 inhibits PKA, Src, ERK1/2, and the AKT pathway. MBP also enhances Cofilin expression, decreasing F-actin intensity on the cell surface in a short time. The combined exposure demonstrated a functional antagonism between compounds. Collectively, these data show that MBP activates GPR30 in Sertoli cells, and GIM-1 modulates this response, playing a protective role in Sertoli cells exposed to MBP.
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http://dx.doi.org/10.1016/j.reprotox.2020.07.004DOI Listing
July 2020

Highly effective fibrin biopolymer scaffold for stem cells upgrading bone regeneration.

Materials (Basel) 2020 Jun 17;13(12). Epub 2020 Jun 17.

Center for the Study of Venoms and Venomous Animals (CEVAP), UNESP-São Paulo State University, Botucatu 18610-307, Brazil.

Fibrin scaffold fits as a provisional platform promoting cell migration and proliferation, angiogenesis, connective tissue formation and growth factors stimulation. We evaluated a unique heterologous fibrin biopolymer as scaffold to mesenchymal stem cells (MSCs) to treat a critical-size bone defect. Femurs of 27 rats were treated with fibrin biopolymer (FBP); FBP + MSCs; and FBP + MSC differentiated in bone lineage (MSC-D). Bone repair was evaluated 03, 21 and 42 days later by radiographic, histological and scanning electron microscopy (SEM) imaging. The FBP + MSC-D association was the most effective treatment, since newly formed Bone was more abundant and early matured in just 21 days. We concluded that FBP is an excellent scaffold for MSCs and also use of differentiated cells should be encouraged in regenerative therapy researches. The FBP ability to maintain viable MSCs at Bone defect site has modified inflammatory environment and accelerating their regeneration.
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http://dx.doi.org/10.3390/ma13122747DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7344939PMC
June 2020

Terminalia catappa L. infusion accelerates the healing process of gastric ischemia-reperfusion injury in rats.

J Ethnopharmacol 2020 Jun 30;256:112793. Epub 2020 Mar 30.

Department of Physiology, Biosciences Institute, UNESP-São Paulo State University, CEP 18618-689, Botucatu, São Paulo, Brazil. Electronic address:

Ethnopharmacological Relevance: Terminalia catappa L. (Combretaceae), known as "amendoeira da praia" in Brazil, has been recognized as a medicinal plant in folk medicine for the treatment of gastrointestinal disorders and other inflammatory conditions. The present study aimed to investigate the preventive and healing effects of the infusion of leaves of T. catappa (ILTC) against gastric lesions caused by ischemia and reperfusion (I/R) injury and characterize its mechanism of action in the gastric mucosa of rats.

Materials And Methods: Different doses (30, 100, and 300 mg/kg) of ILTC were orally administered as acute and subacute treatments against I/R-induced gastric lesion in rats. After treatment, the stomach of rats was collected to measure the lesion area, redox parameters malondialdehyde (MDA), superoxide dismutase (SOD), catalase (CAT), and reduced glutathione (GSH) and inflammatory parameters myeloperoxidase activity (MPO), interleukin 1β (IL-1β) and tumor necrosis factor α (TNF-α). The activities of matrix metalloproteinases 2 and 9 (MMPs 2 and 9) were assessed by zymography method to clarify the mechanisms of the healing acceleration promoted by ILTC.

Results: Pretreatment with ILTC (100 mg/kg) was effective in preventing the aggravation of lesions in the acute model by reducing MPO activity by 38% relative to control group, despite the lack of clarity of this action at the macroscopical level at the lesion area (p < 0.05). After three days of treatment with ILTC (30 and 100 mg/kg), this infusion significantly reduced the lesion area by 95% and 89%, respectively, compared the control (p < 0.05). The gastric healing effect of all doses of ILTC was followed by a reduction in MPO activity (decrease by 70-78%). Compared to the negative control, an improvement in gastric healing owing to treatment with ILTC was observed and this was followed by an increase in MMP-2 (20-47%) (p < 0.05).

Conclusion: Three days of treatment with ILTC could accelerate the healing process in I/R-induced lesions in rats. By decreasing MPO levels, ILTC enabled the action of MMP-2, which led to tissue recovery in the gastric mucosa.
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http://dx.doi.org/10.1016/j.jep.2020.112793DOI Listing
June 2020

Fibrin biopolymer as scaffold candidate to treat bone defects in rats.

J Venom Anim Toxins Incl Trop Dis 2019 4;25:e20190027. Epub 2019 Nov 4.

Center for the Study of Venoms and Venomous Animals (CEVAP), São Paulo State University (UNESP), Botucatu, SP, Brazil.

Background: Bone tissue repair remains a challenge in tissue engineering. Currently, new materials are being applied and often integrated with live cells and biological scaffolds. The fibrin biopolymer (FBP) proposed in this study has hemostatic, sealant, adhesive, scaffolding and drug-delivery properties. The regenerative potential of an association of FBP, biphasic calcium phosphate (BCP) and mesenchymal stem cells (MSCs) was evaluated in defects of rat femurs.

Methods: Adult male Wistar rats were submitted to a 5-mm defect in the femur. This was filled with the following materials and/or associations: BPC; FBP and BCP; FBP and MSCs; and BCP, FBP and MSCs. Bone defect without filling was defined as the control group. Thirty and sixty days after the procedure, animals were euthanatized and subjected to computed tomography, scanning electron microscopy and qualitative and quantitative histological analysis.

Results: It was shown that FBP is a suitable scaffold for bone defects due to the formation of a stable clot that facilitates the handling and optimizes the surgical procedures, allowing also cell adhesion and proliferation. The association between the materials was biocompatible. Progressive deposition of bone matrix was higher in the group treated with FBP and MSCs. Differentiation of mesenchymal stem cells into osteogenic lineage was not necessary to stimulate bone formation.

Conclusions: FBP proved to be an excellent scaffold candidate for bone repair therapies due to application ease and biocompatibility with synthetic calcium-based materials. The satisfactory results obtained by the association of FBP with MSCs may provide a more effective and less costly new approach for bone tissue engineering.
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http://dx.doi.org/10.1590/1678-9199-JVATITD-2019-0027DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6830407PMC
November 2019

Panax ginseng methabolit (GIM-1) prevents oxidative stress and apoptosis in human Sertoli cells exposed to Monobutyl-phthalate (MBP).

Reprod Toxicol 2019 06 6;86:68-75. Epub 2019 Apr 6.

São Paulo State University (UNESP), Institute of Biosciences, Department of Morphology, Botucatu, SP, 18618-689, Brazil. Electronic address:

This study evaluated oxidative stress markers in Human Sertoli cells cultivated on Geltrex® and exposed to Monobutyl Phthalate (MBP), and the potential cytoprotective role of GIM-1 on the antioxidant response. Exposure was performed at 30 min, 1, 12 and 48 h into 4 groups: control, MBP (10μM), GIM-1 (0,05μM) and MBP + GIM-1. Morphology was evaluated. Antioxidant enzymes were analyzed by colorimetric method; NRF-2, SIRT-1, 8- OHdG and Cleaved Caspase-3 by Western Blot. Larger spaces between cells were shown in MBP treatment; GIM-1 was similar to Control and MBP + GIM-1 showed an intermediate aspect. MBP reduced enzymatic activity of all enzymes and NRF-2 expression, increasing cleaved Caspase-3 expression; while GIM-1 increased antioxidants markers alone and attenuated MPB effects in MBP + GIM-1. MBP induced deleterious effects on Sertoli cells, increasing the oxidative stress, apoptosis and modifying their distribution in culture; however, GIM-1 acted as an important cytoprotective agent reversing our attenuating MBP effects.
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http://dx.doi.org/10.1016/j.reprotox.2019.02.008DOI Listing
June 2019

Raloxifene decreases cell viability and migratory potential in prostate cancer cells (LNCaP) with GPR30/GPER1 involvement.

J Pharm Pharmacol 2019 Jul 28;71(7):1065-1071. Epub 2019 Mar 28.

Department of Morphology, Institute of Biosciences, São Paulo State University, UNESP, Botucatu, SP, Brazil.

Objectives: This study evaluated raloxifene (ral) effects on LNCaP prostate tumour cells modulating the activity of GPER1/GPR30 receptors.

Methods: LNCaP cells were submitted for 40/120 min and 12 h to the following treatments: C: RPMI + DMSO; R: RPMI + Ral; G: RPMI + Ral + G15 (GPER1 antagonist). Trypan blue staining measured cell viability. Migratory potential (12 h) was measured by transwell migration test in translucent inserts, which were then stained with DAPI and analysed under a fluorescence microscope for quantification. Cells from 40- and 120-min treatments were subjected to protein extraction to the study of AKT, pAKT, ERK, pERK, ERβ and SIRT1.

Key Findings: There is a reduction in cellular viability in R compared to C at all evaluated times, and an increased cell viability in G when compared to R; cell viability was similar in C and G in all times studied. The migration assay demonstrated a significant decrease in migration potential of tumour cells in R compared to C and G. Ral treatment reduced pERK expression and increased pAKT in the treated groups after 40 min, pointing out to an antiproliferative and apoptotic effect in the GPER1-controlled rapid-effect pathways.

Conclusions: Raloxifene was able to modulate GPER1 in LNCaP prostate tumour cells, decreasing cell viability and their migratory potential.
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http://dx.doi.org/10.1111/jphp.13089DOI Listing
July 2019

"Prostate telocytes change their phenotype in response to castration or testosterone replacement".

Sci Rep 2019 03 6;9(1):3761. Epub 2019 Mar 6.

Sao Paulo State University - UNESP, Institute of Biosciences, Laboratory of Extracellular Matrix, Prof. Dr. Antônio Celso Wagner Zanin St., 250, Rubião Júnior District, Botucatu, São Paulo, 18618-689, Brazil.

Telocytes are CD34-positive cells with a fusiform cell body and long, thin cytoplasmic projections called telopodes. These cells were detected in the stroma of various organs, including the prostate. The prostate is a complex gland capable of undergoing involution due to low testosterone levels; and this condition can be reversed with testosterone replacement. Telocyte function in the mature prostate remains to be dermined, and it is not known whether telocytes can take place in tissue remodeling during prostate involution and regrowth. The present study employed structural, ultrastructural and immunohistochemical methods to investigate the telocyte's phenotypes in the ventral prostate (VP) from control (CT), castrated (CS) and testosterone replacement (TR) groups of adult male Wistar rats. Telocytes were found in the subepithelial, perimuscular and interstitical regions around glandular acini. Telocytes from CT animals have condensed chromatin and long and thin telopodes. In CS group, telocytes appeared quiescent and exhibited layers of folded up telopodes. After TR, telocytes presented loose chromatin, abundant rough endoplasmic reticulum and enlarged telopodes, closely associated with bundles of collagen fibrils. We called these cells "telocytes with a synthetic phenotype". As testosterone levels and glandular morphology returned toward to the CT group parameters, after 10 days of TR, these telocytes progressively switched to the normal phenotype. Our results demonstrate that telocytes exhibit phenotypic plasticity upon androgen manipulation and interact with fibroblast and smooth muscle cells to maintain glandular architecture in control animals and during tissue remodeling after hormonal manipulation.
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http://dx.doi.org/10.1038/s41598-019-40465-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6403354PMC
March 2019

Protective effect of resveratrol on urogenital sinus and prostate development in rats exposed in utero to TCDD (2,3,7,8-tetrachlorodibenzo-p-dioxin).

Reprod Toxicol 2019 01 20;83:82-92. Epub 2018 Jun 20.

Department of Morphology, São Paulo State University - UNESP, Institute of Biosciences, Brazil. Electronic address:

This study evaluated the protective effects of resveratrol on the prostate development of rats exposed to TCDD. Pregnant rats received TCDD (1 μg/kg) at GD15 and/or RES (20 mg/kg/day) from GD10 to PND21. Newborn and adult males from Control, TCDD, TCDD + RES and RES groups were euthanized and the prostate was excised. On PND1, there was a reduction in the number of prostatic buds, AR-positive mesenchymal cells and proliferation index in epithelial and mesenchymal cells in TCDD group, but restored by RES. AhR immunoreactivity was greater in TCDD group than the other groups. On PND90, there was higher frequency of functional hyperplasia in the distal area of the prostate acini in TCDD group, but restored by RES. AhRR expression was higher in the TCDD while NRF2 was higher in the TCDD + RES compared to the other groups. Resveratrol was able to reduce the adverse effects of TCDD on prostate development and its long-term repercussions.
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http://dx.doi.org/10.1016/j.reprotox.2018.06.012DOI Listing
January 2019

Combinatorial Effect of Abiraterone Acetate and NVP-BEZ235 on Prostate Tumor Progression in Rats.

Horm Cancer 2018 06 23;9(3):175-187. Epub 2018 Jan 23.

Department of Morphology, Institute of Biosciences, Sao Paulo State University (UNESP), Rua Professor Doutor Antonio Celso Wagner Zanin, 250, Botucatu, SP, 18618-689, Brazil.

Use of drug combinations that target different pathways involved in the development and progression of prostate cancer (PCa) has emerged as an alternative to overcome the resistance caused by drug monotherapies. The antiandrogen abiraterone acetate and the PI3K/Akt inhibitor NVP-BEZ235 (BEZ235) may be suitable options for the prevention of drug resistance and the inhibition of PCa progression. The aim of the present study was to evaluate whether abiraterone acetate and BEZ235 achieve superior therapeutic effects to either drug administered as monotherapy, in the early stages of PCa in an androgen-dependent system. Our study showed that each drug might impair tumor growth by reducing proliferation and increasing cell death when administered as monotherapy. However, tumor growth continued to progress with each drug monotherapy and some important side effects were related to BEZ. Conversely, when used in combination, the drugs impaired the inflammatory response, decreased hyperplastic lesions, and blocked tumor progression from premalignant to a malignant stage. Our data showed that the strategy to block the androgenic and PI3K/AKT/mTOR pathway is an effective therapeutic option and should be investigated including distinct PI3K pathway inhibitors.
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http://dx.doi.org/10.1007/s12672-018-0323-zDOI Listing
June 2018

Field-relevant doses of the systemic insecticide fipronil and fungicide pyraclostrobin impair mandibular and hypopharyngeal glands in nurse honeybees (Apis mellifera).

Sci Rep 2017 11 9;7(1):15217. Epub 2017 Nov 9.

Núcleo de Ensino, Ciência e Tecnologia em Apicultura Racional (NECTAR), São Paulo State University (UNESP), School of Veterinary Medicine and Animal Science, Department of Animal Production, Botucatu, SP, Brazil.

Global decreases in bee populations emphasize the importance of assessing how environmental stressors affect colony maintenance, especially considering the extreme task specialization observed in honeybee societies. Royal jelly, a protein secretion essential to colony nutrition, is produced by nurse honeybees, and development of bee mandibular glands, which comprise a reservoir surrounded by secretory cells and hypopharyngeal glands that are shaped by acini, is directly associated with production of this secretion. Here, we examined individual and combined effects of the systemic fungicide pyraclostrobin and insecticide fipronil in field-relevant doses (850 and 2.5 ppb, respectively) on mandibular and hypopharyngeal glands in nurse honeybees. Six days of pesticide treatment decreased secretory cell height in mandibular glands. When pyraclostrobin and fipronil were combined, the reservoir volume in mandibular glands also decreased. The total number of acini in hypopharyngeal glands was not affected, but pesticide treatment reduced the number of larger acini while increasing smaller acini. These morphological impairments appeared to reduce royal jelly secretion by nurse honeybees and consequently hampered colony maintenance. Overall, pesticide exposure in doses close to those experienced by bees in the field impaired brood-food glands in nurse honeybees, a change that could negatively influence development, survival, and colony maintenance.
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http://dx.doi.org/10.1038/s41598-017-15581-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5680249PMC
November 2017

Hyperglycemic condition during puberty increases collagen fibers deposition in the prostatic stroma and reduces MMP-2 activity.

Biochem Biophys Res Commun 2017 12 6;493(4):1581-1586. Epub 2017 Oct 6.

Department of Morphology, Institute of Biosciences, Sao Paulo State University (UNESP), Botucatu, Sao Paulo, Brazil. Electronic address:

Puberty is an important period for the growth and maturation of the male reproductive system, and is also a critical window for endocrine or environmental interference. The physiological levels of circulating insulin and hyperglycemic control are important factors for a normal prostate growth. Hyperglycemia during puberty is reported to retard the growth of the prostate gland, with remarkable effects on the epithelial compartment. Here, we investigated the impact of hyperglycemia along with a simultaneous or late insulin replacement on the ventral prostate growth in rats during puberty, paying special attention to the deposition of collagen fibers and activities of gelatinase, matrix metalloproteinase-2 (MMP-2), and -9 (MMP-9). Hyperglycemia was induced by streptozotocin (STZ) administration in 40-day-old male Wistar rats. A subset of hyperglycemic rats underwent an early insulin replacement (three days after the STZ administration), and another subset underwent a late insulin replacement (twenty days after the STZ administration). Animals were euthanized at 60 and/or 80 days of age. The ventral prostatic lobe was processed for picrosirius red staining, type I and III collagen immunohistochemistry, and gelatin zymography. Hyperglycemic animals showed an increased area of collagen fibers in the prostate, which was composed both types of collagens. MMP-2 activity was significantly reduced in the hyperglycemic animals, while MMP-9 activity was very low and showed no alteration. The simultaneous and late insulin administration restored collagen content and MMP-2 activity. In conclusion, puberty is a critical window for prostate maturation and type-1 diabetes-induced hyperglycemia affects the ratio of the prostatic parenchymal and stromal growth, leading to fibrotic tissues by also MMP-2 down regulation.
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http://dx.doi.org/10.1016/j.bbrc.2017.10.022DOI Listing
December 2017

A unique heterologous fibrin sealant (HFS) as a candidate biological scaffold for mesenchymal stem cells in osteoporotic rats.

Stem Cell Res Ther 2017 09 29;8(1):205. Epub 2017 Sep 29.

Center for the Study of Venoms and Venomous Animals (CEVAP), UNESP - Universidade Estadual Paulista, Botucatu, SP, Brazil.

Background: The injection of mesenchymal stem cells (MSCs) directly into the bone of osteoporotic (OP) patients for rapid recovery has been studied worldwide. Scaffolds associated with MSCs are used to maintain and avoid cell loss after application. A unique heterologous fibrin sealant (HFS) derived from snake venom was evaluated for the cytotoxicity of its main components and as a three-dimensional biological scaffold for MSCs to repair a critical femur defect in osteoporotic rats.

Methods: The cytotoxicity of HFS was assessed using a 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazoliumbromide (MTT) assay and transmission electron microscopy. The cells were cultured, characterized by flow cytometry and differentiated into the osteogenic lineage. Two-month-old rats underwent ovariectomy to induce OP. After 3 months, a 5 mm critical bone defect was made in the distal end of the rat femurs and filled with HFS; HFS + MSCs; and HFS + MSCs D (differentiated into the osteogenic lineage) to evaluate the effects. An injury control group (injury and no treatment) and blank control group (no injury and no treatment) were also included. The animals were observed at days 14 and 28 by microtomographic (micro-CT) analyses, histologic and biochemical analysis, as well as scanning electron microscopy.

Results: The results revealed that one of the compounds of HFS, the thrombin-like enzyme extracted from snake venom, had no cytotoxic effects on the MSCs. OP was successfully induced, as demonstrated by the significant differences in the levels of 17β-estradiol, Micro-CT analyses and alkaline phosphatase between the ovariectomized (OVX) and non-ovariectomized (NOVX) groups. The histological data revealed that at 14 days after surgery in both the OVX and NOVX animals, the HFS + CTMs and HFS + CTMsD showed a higher formation of bone cells at the site in relation to the control group (without treatment). Collagen formation was evidenced through bone neoformation in all treated and control groups. No morphological differences in the femurs of the NOVX and OVX animals were observed after the surgical procedure. Scanning electron microscopy (SEM) confirmed the histological analysis.

Conclusions: The new HFS composed of two non-toxic components for MSCs showed capacity to promote the recovery of the bone lesions in OVX and NOVX animals at 14 days after surgery. In addition, the HFS enabled the differentiation of MSCs into MSCs D in the group treated with HFS + MSCs. Using the MSCs and/or MSCs D together with this biopharmaceutical could potentially enable significant advances in the treatment of osteoporotic fractures. Future clinical trials will be necessary to confirm these results.
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http://dx.doi.org/10.1186/s13287-017-0654-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5622505PMC
September 2017

Comparison between two different experimental models of osteoarthritis in rabbits. Intra-articular collagenase injection and anterior cruciate ligament transection.

Acta Cir Bras 2016 Sep;31(9):602-607

PhD, Associate Professor, Institute of Biosciences, Department of Morphology, Extracellular Matrix Laboratory, UNESP, Botucatu-SP, Brazil. Histopathological examinations.

Purpose:: To compare two different experimental models of osteoarthritis in rabbits: intra-articular collagenase injection and anterior cruciate ligament transection.

Methods:: Ten adult rabbits were randomly divided in two groups: COLL (collagenase group) and ACLT (anterior cruciate ligament transection). The COLL group was treated with 0.5 ml collagenase solution (2mg collagenase/0.5 ml sterile PBS), and the ACTL group was subjected to anterior cruciate ligament. After six and twelve weeks, respectively, the animals in the COLL and ACTL groups were euthanized. The gross appearance and histological examinations conducted in the cartilage articular surface was blindly scored according to the criteria developed by Yoshimi et al. (1994) and Mankin et al. (1971), respectively.

Results:: The gross morphologic observation, macroscopic score and histological examinations have demonstrated that the ACTL group presented the highest scores, and lesions more severe than those in the COLL group.

Conclusions: : Both methods, anterior cruciate ligament transection and collagenase, applied to the stifle joint of the rabbits have effectively induced degenerative changes in the cartilage tissue, through statistically significant analysis (p≤0.05). The ACTL method has presented more severe lesions.
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http://dx.doi.org/10.1590/S0102-865020160090000005DOI Listing
September 2016

Ethanol modulates the synthesis and catabolism of retinoic acid in the rat prostate.

Reprod Toxicol 2015 Jun 25;53:1-9. Epub 2015 Feb 25.

Department of Anatomy, Institute of Biosciences, UNESP-Univ Estadual Paulista, Botucatu, SP, Brazil.

All-trans retinoic acid (atRA) maintains physiological stability of the prostate, and we reported that ethanol intake increases atRA in the rat prostate; however the mechanisms underlying these changes are unknown. We evaluated the impact of a low- and high-dose ethanol intake (UChA and UChB strains) on atRA metabolism in the dorsal and lateral prostate. Aldehyde dehydrogenase (ALDH) subtype 1A3 was increased in the dorsal prostate of UChA animals while ALDH1A1 and ALDH1A2 decreased in the lateral prostate. In UChB animals, ALDH1A1, ALDH1A2, and ALDH1A3 increased in the dorsal prostate, and ALDH1A3 decreased in the lateral prostate. atRA levels increased with the low activity of CYP2E1 and decreased with high CYP26 activity in the UChB dorsal prostate. Conversely, atRA was found to decrease when the activity of total CYP was increased in the UChA lateral prostate. Ethanol modulates the synthesis and catabolism of atRA in the prostate in a concentration-dependent manner.
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http://dx.doi.org/10.1016/j.reprotox.2015.02.010DOI Listing
June 2015

Lobe variation effects of experimental diabetes and insulin replacement on rat prostate.

Microsc Res Tech 2011 Nov 20;74(11):1040-8. Epub 2011 Apr 20.

Institute of Biology, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil.

We investigated the impact of diabetes with simultaneous and late insulin replacement on rat prostate growth during puberty, paying special attention to different prostatic lobes. Diabetes was induced by administration of streptozotocin (STZ) in 40-day-old male Wistar rats. A subset of diabetic rats underwent simultaneous insulin replacement (3 days after STZ administration), and another subset underwent a late insulin replacement (20 days after STZ administration). The ventral, dorsolateral, and anterior prostatic lobes were weighed and processed for histological, immunohistochemical, and morphometric analyses. Both diabetic and insulin-treated animals maintained low plasma testosterone (T) concentrations, whereas dihydrotestostenore (DHT) levels were normal. Diabetic animals had a decreased gain in absolute prostatic weight when compared to age-matched controls and insulin replacement animals. However, prostatic lobe weight in the diabetic animals was ∼100% higher, even at the beginning of the experiment. Among the lobes, the anterior lobe showed the highest weight gain in diabetic and insulin replacement conditions. Epithelial cell proliferation in all lobes was significantly reduced in diabetic animals and significantly increased in insulin replacement animals, although apoptosis was unaltered. In conclusion, diabetes diminishes, but does not abolish, prostate growth during puberty. Even late insulin administration reduces the adverse effects of this disease on the prostate. In a scenario with both low insulin and T levels, DHT and other factors may play an important role in pubertal prostate growth. The adverse effects of diabetes on the rat prostate show a variation in lobe response, suggesting that diabetes may affect human prostate zones differently.
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http://dx.doi.org/10.1002/jemt.20991DOI Listing
November 2011

Calcaneal tendon regions exhibit different MMP-2 activation after vertical jumping and treadmill running.

Anat Rec (Hoboken) 2009 Oct;292(10):1656-62

São Paulo State University (UNESP), School of Science and Technology, Department of Physical Education, Presidente Prudente, SP, Brazil.

Increased activity of matrix metalloproteinases (MMPs) -2 and -9 was found in calcaneal tendon after physical training. However, little attention has been given to the distinct biomechanical and tissue structure of the calcaneal tendon's proximal and distal regions. Herein, we evaluated the effect of two types of physical activities on tendon morphology and matrix metalloproteinase activities in the proximal and distal regions of rat calcaneal tendon, separately. Adult male Wistar rats from control, water-adapted, vertical-jumping, and treadmill-running groups were sacrificed after 1 or 4 days of physical exercise, 6 hr after the end of that day's exercise session. Tendons were processed for histology, morphometry, and gelatin zymography. Tendons from adapted and trained animals showed active secretory cells and increased thickness, cellularity, and blood vessel volume fraction of peritendinous sheath, but without inflammatory process. In the proximal region, both pro- and active MMP-2 were increased after vertical jumping, but only pro-MMP-2 was increased after treadmill running. In contrast, in the distal region, both exercise types increased the activity of pro- and active MMP-2, especially treadmill running, which increased the active MMP-2 by about 11- and eightfold, respectively, after 1 and 4 days of training. No activity of MMP-9 was observed in either tendon region in this study. In conclusion, distal and proximal regions of calcaneal tendon exhibit differential intensities of tissue remodeling after treadmill running or vertical jumping and MMP-2, in the absence of inflammation, plays a major role in this adaptive response.
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http://dx.doi.org/10.1002/ar.20953DOI Listing
October 2009

Differential MMP-2 and MMP-9 activity and collagen distribution in skeletal muscle from pacu (Piaractus mesopotamicus) during juvenile and adult growth phases.

Anat Rec (Hoboken) 2009 Mar;292(3):387-95

Department of Morphology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil.

Here, we evaluated collagen distribution and matrix metalloproteinases (MMPs) MMP-2 and MMP-9 activities in skeletal muscle of pacu (Piaractus mesopotamicus) during juvenile and adult growth phases. Muscle samples from juvenile and adult fishes were processed by histochemistry for collagen system fibers and for gelatin-zymography for MMP-2 and MMP-9 activities analysis. Picrosirius staining revealed a myosept, endomysium, and perimysium-like structures in both growth phases and muscle types, with increased areas of collagen fibers in adults, mainly in red muscle. Reticulin staining showed that reticular fibers in the endomysium-like structure were thinner and discontinuous in the red muscle fibers. The zymography revealed clear bands of the pro- MMP-9, active- MMP-9, intermediate- MMP-2, and active- MMP-2 forms in red and white muscle in both growth phases. MMP-2 activity was more intense in juvenile than adult muscle fibers. Comparing the red and white muscle types, MMP-2 activity was significantly higher in red muscle in adult phase only. The activity of MMP-9 forms was similar in juvenile red and white muscles and in the adult red muscle, without any activity in adult white muscle. In conclusion, our results show that, in pacu, the higher activities of MMP-2 and -9 are associated with the rapid muscle growth in juvenile age and in adult fish, these activities are related with a different red and white muscle physiology. This study may contribute to the understanding muscle growth mechanisms and may also contribute to analyse red and the white muscle parameters of firmness and softness, respectively, of the commercial product.
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http://dx.doi.org/10.1002/ar.20863DOI Listing
March 2009

Metalloproteinases 2 and 9 activity during promotion and progression stages of rat liver carcinogenesis.

J Mol Histol 2009 Feb 4;40(1):1-11. Epub 2008 Dec 4.

School of Medicine, Department of Pathology, UNESP São Paulo State University, Botucatu, SP 18618-000, Brazil.

Activity of metalloproteinases 2 and 9 (MMP-2 and 9) during promotion and progression of rat liver carcinogenesis was investigated in a modified resistant hepatocyte model. Development of preneoplastic liver lesions positive for glutathione S-transferase 7-7-(GST-P 7-7-positive PNL) and tumors besides hepatocytes positive for proliferating cell nuclear antigen (PCNA) were quantified and compared to MMP-2 and-9 activity using gelatin zymography. Marked increases in GST-P 7-7-positive PNL development, PCNA labeling indices, MMP-2 (pro, intermediate and active forms) and pro-MMP-9 activity were observed after proliferative stimulus induced by 2-acetylaminofluorene (2-AAF) exposure cycles. After 2-AAF withdrawal, increase in MMP-2 activity was detected only in neoplastic mixed lesions, whereas active MMP-9 was increased in both PLN and neoplastic tissues. Our findings suggest that MMP-2 may be associated with proliferative events induced by 2-AAF rather than with selective growth of PNL and that MMP-9 could be associated with progression of PNL and neoplastic mixed lesions.
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http://dx.doi.org/10.1007/s10735-008-9206-xDOI Listing
February 2009

Immunolocalization of aquaporins 1, 2 and 7 in rete testis, efferent ducts, epididymis and vas deferens of adult dog.

Cell Tissue Res 2008 May 14;332(2):329-35. Epub 2008 Mar 14.

Department of Cell Biology, Institute of Biology, UNICAMP, Campinas, SP, Brazil.

The transepithelial movement of water into the male reproductive tract is an essential process for normal male fertility. Protein water channels, referred to as aquaporins (AQPs), are involved in increasing the osmotic permeability of membranes. This study has examined the expression of AQP1, AQP2, and AQP7 in epithelial cells in adult dog efferent ducts, epididymis, and vas deferens. Samples of dog male reproductive tract comprising fragments of the testis, initial segment, caput, corpus and cauda epididymidis, and vas deferens were investigated by immunohistochemistry and Western blotting procedures to show the localization and distribution of the AQPs. AQP1 was noted in rete testis, in efferent ducts, and in vessels in the intertubular space, suggesting that AQP1 participated in the absorption of the large amount of testicular fluid occurring characteristically in the efferent ducts. AQP2 expression was found in the rete testis, efferent ducts and epididymis, whereas AQP7 was expressed in the epithelium of the proximal regions of the epididymis and in the vas deferens. This is the first time that AQP2 and AQP7 have been observed in these regions of mammalian excurrent ducts, but their functional role in the dog male reproductive tract remains unknown. Investigations of AQP biology could be relevant for clinical studies of the male reproductive tract and to technologies for assisted procreation.
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http://dx.doi.org/10.1007/s00441-008-0592-xDOI Listing
May 2008

Aquaporin 9 (AQP9) localization in the adult dog testis excurrent ducts by immunohistochemistry.

Anat Rec (Hoboken) 2007 Dec;290(12):1519-25

Department of Cell Biology, Institute of Biology, UNICAMP, Campinas, SP, Brazil.

Aquaporins (AQPs) are small, intrinsic membrane proteins that are present in many cell types involved in fluid transport. AQP9 is a major apical water channel that is expressed throughout the efferent ducts, epididymis, and vas deferens, as well as in other regions of the human and rodent male reproductive tract. The target of this study was to examine the expression of AQP9 in epithelial cells in the adult dog efferent ducts, epididymis, and vas deferens. Samples of dog male reproductive tract comprising fragments of the testis; initial segment, caput, corpus, and cauda of the epididymis; and vas deferens were obtained from eight adult mongrel dogs. Immunohistochemistry and Western blotting procedures were used to show AQP9 localization and distribution. AQP9 expression was not detected either in dog seminiferous tubules or rete testis. However, apical labeling for AQP9 was detected in the different regions of epididymis and vas deferens, with the reaction being less intense in the caput epididymis. Thus, AQP9 is abundantly expressed in dog male reproductive tract, in which it is an important apical pathway for transmembrane flow of water and neutral solutes.
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http://dx.doi.org/10.1002/ar.20611DOI Listing
December 2007
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