Publications by authors named "Robert A Hill"

69 Publications

Intravital Imaging of Neocortical Heterotopia Reveals Aberrant Axonal Pathfinding and Myelination around Ectopic Neurons.

Cereb Cortex 2021 Apr 20. Epub 2021 Apr 20.

Interdepartmental Neuroscience Program, Yale School of Medicine, New Haven, CT 06510, USA.

Neocortical heterotopia consist of ectopic neuronal clusters that are frequently found in individuals with cognitive disability and epilepsy. However, their pathogenesis remains poorly understood due in part to a lack of tractable animal models. We have developed an inducible model of focal cortical heterotopia that enables their precise spatiotemporal control and high-resolution optical imaging in live mice. Here, we report that heterotopia are associated with striking patterns of circumferentially projecting axons and increased myelination around neuronal clusters. Despite their aberrant axonal patterns, in vivo calcium imaging revealed that heterotopic neurons remain functionally connected to other brain regions, highlighting their potential to influence global neural networks. These aberrant patterns only form when heterotopia are induced during a critical embryonic temporal window, but not in early postnatal development. Our model provides a new way to investigate heterotopia formation in vivo and reveals features suggesting the existence of developmentally modulated, neuron-derived axon guidance and myelination factors.
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http://dx.doi.org/10.1093/cercor/bhab090DOI Listing
April 2021

Imaging and optogenetic modulation of vascular mural cells in the live brain.

Nat Protoc 2021 01 9;16(1):472-496. Epub 2020 Dec 9.

Department of Neurology, Yale School of Medicine, New Haven, CT, USA.

Mural cells (smooth muscle cells and pericytes) are integral components of brain blood vessels that play important roles in vascular formation, blood-brain barrier maintenance, and regulation of regional cerebral blood flow (rCBF). These cells are implicated in conditions ranging from developmental vascular disorders to age-related neurodegenerative diseases. Here we present complementary tools for cell labeling with transgenic mice and organic dyes that allow high-resolution intravital imaging of the different mural cell subtypes. We also provide detailed methodologies for imaging of spontaneous and neural activity-evoked calcium transients in mural cells. In addition, we describe strategies for single- and two-photon optogenetics that allow manipulation of the activity of individual and small clusters of mural cells. Together with measurements of diameter and flow in individual brain microvessels, calcium imaging and optogenetics allow the investigation of pericyte and smooth muscle cell physiology and their role in regulating rCBF. We also demonstrate the utility of these tools to investigate mural cells in the context of Alzheimer's disease and cerebral ischemia mouse models. Thus, these methods can be used to reveal the functional and structural heterogeneity of mural cells in vivo, and allow detailed cellular studies of the normal function and pathophysiology of mural cells in a variety of disease models. The implementation of this protocol can take from several hours to days depending on the intended applications.
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http://dx.doi.org/10.1038/s41596-020-00425-wDOI Listing
January 2021

The potassium channel subunit Kβ1 serves as a major control point for synaptic facilitation.

Proc Natl Acad Sci U S A 2020 11 9;117(47):29937-29947. Epub 2020 Nov 9.

Department of Biology, Dartmouth College, Hanover, NH 03755;

Analysis of the presynaptic action potential's (AP) role in synaptic facilitation in hippocampal pyramidal neurons has been difficult due to size limitations of axons. We overcame these size barriers by combining high-resolution optical recordings of membrane potential, exocytosis, and Ca in cultured hippocampal neurons. These recordings revealed a critical and selective role for K1 channel inactivation in synaptic facilitation of excitatory hippocampal neurons. Presynaptic K1 channel inactivation was mediated by the Kβ1 subunit and had a surprisingly rapid onset that was readily apparent even in brief physiological stimulation paradigms including paired-pulse stimulation. Genetic depletion of Kβ1 blocked all broadening of the AP during high-frequency stimulation and eliminated synaptic facilitation without altering the initial probability of vesicle release. Thus, using all quantitative optical measurements of presynaptic physiology, we reveal a critical role for presynaptic K channels in synaptic facilitation at presynaptic terminals of the hippocampus upstream of the exocytic machinery.
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http://dx.doi.org/10.1073/pnas.2000790117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7703594PMC
November 2020

Astrocytes and microglia play orchestrated roles and respect phagocytic territories during neuronal corpse removal in vivo.

Sci Adv 2020 Jun 26;6(26):eaba3239. Epub 2020 Jun 26.

Department of Neurology, Yale School of Medicine, New Haven, CT, USA.

Cell death is prevalent throughout life; however, the coordinated interactions and roles of phagocytes during corpse removal in the live brain are poorly understood. We developed photochemical and viral methodologies to induce death in single cells and combined this with intravital optical imaging. This approach allowed us to track multicellular phagocytic interactions with precise spatiotemporal resolution. Astrocytes and microglia engaged with dying neurons in an orchestrated and synchronized fashion. Each glial cell played specialized roles: Astrocyte processes rapidly polarized and engulfed numerous small dendritic apoptotic bodies, while microglia migrated and engulfed the soma and apical dendrites. The relative involvement and phagocytic specialization of each glial cell was plastic and controlled by the receptor tyrosine kinase . In aging, there was a marked delay in apoptotic cell removal. Thus, a precisely orchestrated response and cross-talk between glial cells during corpse removal may be critical for maintaining brain homeostasis.
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http://dx.doi.org/10.1126/sciadv.aba3239DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7319765PMC
June 2020

Triterpenoids.

Nat Prod Rep 2020 07 14;37(7):962-998. Epub 2020 Feb 14.

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

Covering 2015. Previous review: Nat. Prod. Rep., 2018, 35, 1294-1329This review covers the isolation and structure determination of triterpenoids reported during 2015 including squalene derivatives, lanostanes, holostanes, cycloartanes, cucurbitanes, dammaranes, euphanes, tirucallanes, tetranortriterpenoids, quassinoids, lupanes, oleananes, friedelanes, ursanes, hopanes, serratanes, isomalabaricanes and saponins; 320 references are cited.
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http://dx.doi.org/10.1039/c9np00067dDOI Listing
July 2020

Myelin plasticity in adulthood and aging.

Neurosci Lett 2020 01 22;715:134645. Epub 2019 Nov 22.

Department of Biological Sciences, Dartmouth College, Hanover, NH, USA. Electronic address:

The central nervous system maintains the potential for molecular and cellular plasticity throughout life. This flexibility underlies fundamental features of neural circuitry including the brain's ability to sense, store, and properly adapt to everchanging external stimuli on time scales from seconds to years. Evidence for most forms of plasticity are centered around changes in neuronal structure and synaptic strength, however recent data suggests that myelinating oligodendrocytes exhibit certain forms of plasticity in the adult. This plasticity ranges from the generation of entirely new myelinating cells to more subtle changes in myelin sheath length, thickness, and distribution along axons. The extent to which these changes dynamically modify axonal function and neural circuitry and whether they are directly related to mechanisms of learning and memory remains an open question. Here we describe different forms of myelin plasticity, highlight some recent evidence for changes in myelination throughout life, and discuss how defects in these forms of plasticity could be associated with cognitive decline in aging.
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http://dx.doi.org/10.1016/j.neulet.2019.134645DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6981290PMC
January 2020

Uncovering the biology of myelin with optical imaging of the live brain.

Glia 2019 11 29;67(11):2008-2019. Epub 2019 Apr 29.

Departments of Neurology and Neuroscience, Yale School of Medicine, New Haven, Connecticut.

Myelin has traditionally been considered a static structure that is produced and assembled during early developmental stages. While this characterization is accurate in some contexts, recent studies have revealed that oligodendrocyte generation and patterns of myelination are dynamic and potentially modifiable throughout life. Unique structural and biochemical properties of the myelin sheath provide opportunities for the development and implementation of multimodal label-free and fluorescence optical imaging approaches. When combined with genetically encoded fluorescent tags targeted to distinct cells and subcellular structures, these techniques offer a powerful methodological toolbox for uncovering mechanisms of myelin generation and plasticity in the live brain. Here, we discuss recent advances in these approaches that have allowed the discovery of several forms of myelin plasticity in developing and adult nervous systems. Using these techniques, long-standing questions related to myelin generation, remodeling, and degeneration can now be addressed.
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http://dx.doi.org/10.1002/glia.23635DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6744352PMC
November 2019

Hot off the press.

Nat Prod Rep 2019 02;36(2):258-262

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as vlasoulamine A from Vladimiria souliei.
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http://dx.doi.org/10.1039/c9np90001bDOI Listing
February 2019

Hot off the press.

Nat Prod Rep 2018 12;35(12):1236-1240

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as kadsuraol A from Kadsura longipedunculata.
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http://dx.doi.org/10.1039/c8np90046aDOI Listing
December 2018

Hot off the Press.

Nat Prod Rep 2018 10;35(10):1024-1028

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as huperphlegmine A from Huperzia phlegmaria.
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http://dx.doi.org/10.1039/c8np90032aDOI Listing
October 2018

Hot off the Press.

Nat Prod Rep 2018 08;35(8):702-706

School of Chemistry, Glasgow University, Glasgow, UKG12 8QQ.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as pepluanol C from Euphorbia peplus.
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http://dx.doi.org/10.1039/c8np90024hDOI Listing
August 2018

Organotypic Slice Cultures to Study Oligodendrocyte Proliferation, Fate, and Myelination.

Methods Mol Biol 2018 ;1791:145-156

Department of Physiology and Neurobiology, University of Connecticut, Storrs, CT, USA.

Oligodendrocyte development and myelination are processes in the central nervous system that are regulated by cell intrinsic and extrinsic mechanisms. Organotypic slice cultures provide a simple method for studying factors that affect oligodendrocyte proliferation, differentiation, and myelination in the context of the local cellular environment. Here we show that major glial cell types and neurons are preserved in slice cultures from postnatal mouse forebrain, and their morphological characteristics are retained. We further demonstrate that cellular processes requiring interactions with neighboring cells such as myelination can proceed in slice culture.
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http://dx.doi.org/10.1007/978-1-4939-7862-5_11DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6372239PMC
February 2019

Triterpenoids.

Nat Prod Rep 2018 12;35(12):1294-1329

School of Chemistry, Glasgow University, Glasgow, UK G12 8QQ.

Covering 2014. Previous review: Nat. Prod. Rep., 2017, 34, 90-122 This review covers the isolation and structure determination of triterpenoids reported during 2014 including squalene derivatives, lanostanes, holostanes, cycloartanes, cucurbitanes, dammaranes, euphanes, tirucallanes, tetranortriterpenoids, quassinoids, lupanes, oleananes, friedelanes, ursanes, hopanes, serratanes, isomalabaricanes and saponins; 374 references are cited.
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http://dx.doi.org/10.1039/c8np00029hDOI Listing
December 2018

Hot off the Press.

Nat Prod Rep 2018 06;35(6):496-500

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as mollebenzylanol A from Rhododendron molle.
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http://dx.doi.org/10.1039/c8np90015aDOI Listing
June 2018

Lifelong cortical myelin plasticity and age-related degeneration in the live mammalian brain.

Nat Neurosci 2018 05 19;21(5):683-695. Epub 2018 Mar 19.

Department of Neurology, Yale School of Medicine, New Haven, CT, USA.

Axonal myelin increases neural processing speed and efficiency. It is unknown whether patterns of myelin distribution are fixed or whether myelinating oligodendrocytes are continually generated in adulthood and maintain the capacity for structural remodeling. Using high-resolution, intravital label-free and fluorescence optical imaging in mouse cortex, we demonstrate lifelong oligodendrocyte generation occurring in parallel with structural plasticity of individual myelin internodes. Continuous internode formation occurred on both partially myelinated and unmyelinated axons, and the total myelin coverage along individual axons progressed up to two years of age. After peak myelination, gradual oligodendrocyte death and myelin degeneration in aging were associated with pronounced internode loss and myelin debris accumulation within microglia. Thus, cortical myelin remodeling is protracted throughout life, potentially playing critical roles in neuronal network homeostasis. The gradual loss of internodes and myelin degeneration in aging could contribute significantly to brain pathogenesis.
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http://dx.doi.org/10.1038/s41593-018-0120-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5920745PMC
May 2018

Hot off the press.

Nat Prod Rep 2018 04;35(4):298-302

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as tundrenone from Methylobacter tundripaludum.
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http://dx.doi.org/10.1039/c8np90008fDOI Listing
April 2018

Age-Dependent Decline in Fate Switch from NG2 Cells to Astrocytes After Olig2 Deletion.

J Neurosci 2018 02 30;38(9):2359-2371. Epub 2018 Jan 30.

Department of Physiology and Neurobiology,

NG2 cells are a resident glial progenitor cell population that is uniformly distributed throughout the developing and mature mammalian CNS. Those in the postnatal CNS generate exclusively myelinating and non-myelinating oligodendrocytes and are thus equated with oligodendrocyte precursor cells. Prenatally, NG2 cells in the ventral gray matter of the forebrain generate protoplasmic astrocytes as well as oligodendrocytes. The fate conversion from NG2 cells into protoplasmic astrocytes is dependent on downregulation of the key oligodendrocyte transcription factor Olig2. We showed previously that constitutive deletion of Olig2 in NG2 cells converts NG2 cells in the neocortex into protoplasmic astrocytes at the expense of oligodendrocytes. In this study, we show that postnatal deletion of Olig2 caused NG2 cells in the neocortex but not in other gray matter regions to become protoplasmic astrocytes. However, NG2 cells in the neocortex became more resistant to astrocyte fate switch over the first 3 postnatal weeks. Fewer NG2 cells differentiated into astrocytes and did so with longer latency after Olig2 deletion at postnatal day 18 (P18) compared with deletion at P2. The high-mobility group transcription factor Sox10 was not downregulated for at least 1 month after Olig2 deletion at P18 despite an early transient upregulation of the astrocyte transcription factor NFIA. Furthermore, inhibiting cell proliferation in slice culture reduced astrocyte differentiation from Olig2-deleted perinatal NG2 cells, suggesting that cell division might facilitate nuclear reorganization needed for astrocyte transformation. NG2 cells are glial progenitor cells that retain a certain degree of lineage plasticity. In the normal postnatal neocortex, they generate mostly oligodendrocyte lineage cells. When the oligodendrocyte transcription factor Olig2 is deleted in NG2 cells in the neocortex, they switch their fate to protoplasmic astrocytes. However, the efficiency of the fate switch decreases with age over the first 3 postnatal weeks and is reduced when cell proliferation is inhibited. As the neocortex matures, sustained expression of the oligodendrocyte lineage-specific key transcription factor Sox10 becomes less dependent on Olig2. Together, our findings suggest a gradual stabilization of the oligodendrocyte lineage genes and loss of lineage plasticity during the first 3 weeks after birth, possibly due to nuclear reorganization.
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http://dx.doi.org/10.1523/JNEUROSCI.0712-17.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5830521PMC
February 2018

Hot off the press.

Nat Prod Rep 2018 02;35(2):132-136

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as illisimonin A from Illicium simonsii.
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http://dx.doi.org/10.1039/c7np90051aDOI Listing
February 2018

Hot off the press.

Nat Prod Rep 2017 Dec;34(12):1340-1344

School of Chemistry, Glasgow University, Glasgow, UKG12 8QQ.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as tryptorubin A isolated from a Streptomyces species.
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http://dx.doi.org/10.1039/c7np90044aDOI Listing
December 2017

Hot off the Press.

Nat Prod Rep 2017 Oct;34(10):1180-1184

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as caesalpinflavin A from Caesalpina enneaphylla.
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http://dx.doi.org/10.1039/c7np90040fDOI Listing
October 2017

Hot off the Press.

Nat Prod Rep 2017 08;34(8):940-944

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as svetamycin B from a Streptomyces species.
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http://dx.doi.org/10.1039/c7np90028gDOI Listing
August 2017

Targeted two-photon chemical apoptotic ablation of defined cell types in vivo.

Nat Commun 2017 06 16;8:15837. Epub 2017 Jun 16.

Department of Neurology, Yale School of Medicine, New Haven, Connecticut 06511, USA.

A major bottleneck limiting understanding of mechanisms and consequences of cell death in complex organisms is the inability to induce and visualize this process with spatial and temporal precision in living animals. Here we report a technique termed two-photon chemical apoptotic targeted ablation (2Phatal) that uses focal illumination with a femtosecond-pulsed laser to bleach a nucleic acid-binding dye causing dose-dependent apoptosis of individual cells without collateral damage. Using 2Phatal, we achieve precise ablation of distinct populations of neurons, glia and pericytes in the mouse brain and in zebrafish. When combined with organelle-targeted fluorescent proteins and biosensors, we uncover previously unrecognized cell-type differences in patterns of apoptosis and associated dynamics of ribosomal disassembly, calcium overload and mitochondrial fission. 2Phatal provides a powerful and rapidly adoptable platform to investigate in vivo functional consequences and neural plasticity following cell death as well as apoptosis, cell clearance and tissue remodelling in diverse organs and species.
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http://dx.doi.org/10.1038/ncomms15837DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5501159PMC
June 2017

A fluoro-Nissl dye identifies pericytes as distinct vascular mural cells during in vivo brain imaging.

Nat Neurosci 2017 Jul 15;20(7):1023-1032. Epub 2017 May 15.

Department of Neurology, Yale School of Medicine, New Haven, Connecticut, USA.

Pericytes and smooth muscle cells are integral components of the brain microvasculature. However, no techniques exist to unambiguously identify these cell types, greatly limiting their investigation in vivo. Here we show that the fluorescent Nissl dye NeuroTrace 500/525 labels brain pericytes with specificity, allowing high-resolution optical imaging in the live mouse. We demonstrate that capillary pericytes are a population of mural cells with distinct morphological, molecular and functional features that do not overlap with precapillary or arteriolar smooth muscle actin-expressing cells. The remarkable specificity for dye uptake suggests that pericytes have molecular transport mechanisms not present in other brain cells. We demonstrate feasibility of longitudinal pericyte imaging during microvascular development and aging and in models of brain ischemia and Alzheimer's disease. The ability to easily label pericytes in any mouse model opens the possibility of a broad range of investigations of mural cells in vascular development, neurovascular coupling and neuropathology.
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http://dx.doi.org/10.1038/nn.4564DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5550770PMC
July 2017

Hot off the press.

Nat Prod Rep 2017 06;34(6):566-570

School of Chemistry, Glasgow University, Glasgow, UKG12 8QQ.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as macrophilone A from Macrorhynchia philippina.
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http://dx.doi.org/10.1039/c7np90017aDOI Listing
June 2017

Hot off the press.

Nat Prod Rep 2017 Feb 12;34(2):130-134. Epub 2017 Jan 12.

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as hitorin A from Chloranthus japonicus.
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http://dx.doi.org/10.1039/c6np90051hDOI Listing
February 2017

Triterpenoids.

Nat Prod Rep 2017 Jan;34(1):90-122

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

Covering: 2013. Previous review: Nat. Prod. Rep., 2015, 29, 1028-1065This review covers the isolation and structure determination of triterpenoids reported during 2013 including squalene derivatives, lanostanes, holostanes, cycloartanes, cucurbitanes, dammaranes, euphanes, tirucallanes, tetranortriterpenoids, quassinoids, lupanes, oleananes, friedelanes, ursanes, hopanes, serratanes, isomalabaricanes and saponins; 350 references are cited.
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http://dx.doi.org/10.1039/c6np00094kDOI Listing
January 2017

Hot off the press.

Nat Prod Rep 2016 Nov;33(12):1352-1356

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as kanamienamide from the marine cyanobacterium Moorea bouillonii.
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http://dx.doi.org/10.1039/c6np90047jDOI Listing
November 2016

Correction: Hot off the press.

Nat Prod Rep 2016 09;33(10):1239

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

Correction for 'Hot off the press' by Robert A. Hill et al., Nat. Prod. Rep., 2016, DOI: 10.1039/c6np90039a.
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http://dx.doi.org/10.1039/c6np90040bDOI Listing
September 2016

Hot off the press.

Nat Prod Rep 2016 Sep;33(10):1126-1130

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 32 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products such as chrysamide A from a deep-sea fungus Penicillium chrysogenum.
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http://dx.doi.org/10.1039/c6np90039aDOI Listing
September 2016

Hot off the Press.

Nat Prod Rep 2016 Jun;33(6):742-6

School of Chemistry, Glasgow University, Glasgow, G12 8QQ, UK.

A personal selection of 33 recent papers is presented covering various aspects of current developments in bioorganic chemistry and novel natural products, such as epicochalasine A from Aspergillus flavipes.
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http://dx.doi.org/10.1039/c6np90022dDOI Listing
June 2016