The role of the miR‐17–92 cluster in neurogenesis and angiogenesis in the central nervous system of adults

It is well known that neurogenesis is not the only concern for the fully functional recovery after brain or spinal cord injury, as it has been shed light on the critical role of angiogenesis in improving neurological functional recovery. Angiogenesis and neurogenesis coordinately interact with each other in the developing and adult brain, during which they may respond to similar mediators and receptors, in which they share a common posttranscriptional regulator: the miR‐17–92 cluster. The miR‐17–92 cluster was initially described as an oncogene and was later demonstrated to drive key physiological and pathological responses during development and diseases respectively. It has been reported that the miR‐17–92 cluster regulates both neurogenesis and angiogenesis. The miR‐17–92 cluster modulates neural progenitor cells proliferation not only during development but also during neurological disorders such as stroke. It has also been shown that the endothelial miR‐17–92 cluster regulates angiogenesis during embryonic stage and adulthood. In this review, we have discussed the actions of the miR‐17–92 cluster in neuronal and vascular plasticity, and its potential as a novel therapeutic strategy for CNS injury. © 2016 Wiley Periodicals, Inc.

[1]  Susu Mao,et al.  miR-17-92 facilitates neuronal differentiation of transplanted neural stem/precursor cells under neuroinflammatory conditions , 2016, Journal of Neuroinflammation.

[2]  T. Sun,et al.  miR-17-92 Cluster Regulates Adult Hippocampal Neurogenesis, Anxiety, and Depression. , 2016, Cell reports.

[3]  F. Micciulla,et al.  Regulation of angiogenesis through the efficient delivery of microRNAs into endothelial cells using polyamine-coated carbon nanotubes , 2016, Nanomedicine : nanotechnology, biology, and medicine.

[4]  J. Qu,et al.  MicroRNA-17-92 regulates myoblast proliferation and differentiation by targeting the ENH1/Id1 signaling axis , 2016, Cell Death and Differentiation.

[5]  Clotilde Théry,et al.  Communication by Extracellular Vesicles: Where We Are and Where We Need to Go , 2016, Cell.

[6]  Y. Suárez,et al.  VEGF-Induced Expression of miR-17–92 Cluster in Endothelial Cells Is Mediated by ERK/ELK1 Activation and Regulates Angiogenesis , 2016, Circulation research.

[7]  Preeti Raghavan,et al.  The Effect of Body Weight Support Treadmill Training on Gait Recovery, Proximal Lower Limb Motor Pattern, and Balance in Patients with Subacute Stroke , 2015, BioMed research international.

[8]  Yan-li Zhou,et al.  Non-coding RNAs in cardiac regeneration , 2015, Oncotarget.

[9]  R. Gregory,et al.  A Biogenesis Step Upstream of Microprocessor Controls miR-17∼92 Expression , 2015, Cell.

[10]  Wei Chen,et al.  General hallmarks of microRNAs in brain evolution and development , 2015, RNA biology.

[11]  Lina Mao,et al.  Skin-Derived Precursor Cells Promote Angiogenesis and Stimulate Proliferation of Endogenous Neural Stem Cells after Cerebral Infarction , 2015, BioMed research international.

[12]  Sha Li,et al.  Exosome and Exosomal MicroRNA: Trafficking, Sorting, and Function , 2015, Genom. Proteom. Bioinform..

[13]  D. De Pietri Tonelli,et al.  Convergent microRNA actions coordinate neocortical development , 2014, Cellular and Molecular Life Sciences.

[14]  K. Zen,et al.  miR‐17 regulates the proliferation and differentiation of the neural precursor cells during mouse corticogenesis , 2014, The FEBS journal.

[15]  L. Di Marcotullio,et al.  microRNA-17-92 cluster is a direct Nanog target and controls neural stem cell through Trp53inp1 , 2013, The EMBO journal.

[16]  M. Chopp,et al.  MicroRNAs in cerebral ischemia-induced neurogenesis. , 2013, Journal of neuropathology and experimental neurology.

[17]  G. Wang,et al.  mir-17–92 Cluster Is Required for and Sufficient to Induce Cardiomyocyte Proliferation in Postnatal and Adult Hearts , 2013, Circulation research.

[18]  T. Sun,et al.  MicroRNA cluster miR-17-92 regulates neural stem cell expansion and transition to intermediate progenitors in the developing mouse neocortex. , 2013, Cell reports.

[19]  M. Chopp,et al.  MicroRNA-17-92 Cluster Mediates the Proliferation and Survival of Neural Progenitor Cells after Stroke* , 2013, The Journal of Biological Chemistry.

[20]  Jianwei Jiao,et al.  The role of microRNAs in neural stem cells and neurogenesis. , 2013, Journal of genetics and genomics = Yi chuan xue bao.

[21]  Graça Raposo,et al.  Extracellular vesicles: Exosomes, microvesicles, and friends , 2013, The Journal of cell biology.

[22]  S. Pfeffer,et al.  The miR-17 ∼ 92 Cluster: A Key Player in the Control of Inflammation during Rheumatoid Arthritis , 2013, Front. Immunol..

[23]  Nnenna A. Finn,et al.  Intracellular and Extracellular miRNAs in Regulation of Angiogenesis Signaling. , 2012, Current angiogenesis.

[24]  A. Ergul,et al.  Angiogenesis: A Harmonized Target for Recovery After Stroke , 2012, Stroke.

[25]  X. Chen,et al.  Secreted microRNAs: a new form of intercellular communication. , 2012, Trends in cell biology.

[26]  M. Chopp,et al.  MicroRNA Profiling in Subventricular Zone after Stroke: MiR-124a Regulates Proliferation of Neural Progenitor Cells through Notch Signaling Pathway , 2011, PloS one.

[27]  G. Fan,et al.  Extracellular/circulating microRNAs and their potential role in cardiovascular disease. , 2011, American journal of cardiovascular disease.

[28]  P. Carmeliet,et al.  Molecular mechanisms and clinical applications of angiogenesis , 2011, Nature.

[29]  S. Whittemore,et al.  Targeting Microvasculature for Neuroprotection after SCI , 2011, Neurotherapeutics.

[30]  R. Adams,et al.  Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice , 2010, Nature Protocols.

[31]  Jessica A. Weber,et al.  Export of microRNAs and microRNA-protective protein by mammalian cells , 2010, Nucleic acids research.

[32]  L. Opitz,et al.  Control of oligodendroglial cell number by the miR-17-92 cluster , 2010, Development.

[33]  P. Jin,et al.  Roles of small regulatory RNAs in determining neuronal identity , 2010, Nature Reviews Neuroscience.

[34]  Y. Matsuki,et al.  Secretory Mechanisms and Intercellular Transfer of MicroRNAs in Living Cells*♦ , 2010, The Journal of Biological Chemistry.

[35]  M. Moskowitz,et al.  Sonic Hedgehog Regulates Ischemia/Hypoxia-Induced Neural Progenitor Proliferation , 2009, Stroke.

[36]  O. Wagner,et al.  The VEGF-induced transcriptional response comprises gene clusters at the crossroad of angiogenesis and inflammation , 2009, Thrombosis and Haemostasis.

[37]  G. Rougon,et al.  Quantitative analysis by in vivo imaging of the dynamics of vascular and axonal networks in injured mouse spinal cord , 2009, Proceedings of the National Academy of Sciences.

[38]  J. E. Lee,et al.  Ex Vivo VEGF Delivery by Neural Stem Cells Enhances Proliferation of Glial Progenitors, Angiogenesis, and Tissue Sparing after Spinal Cord Injury , 2009, PloS one.

[39]  Y. Suárez,et al.  MicroRNAs as novel regulators of angiogenesis. , 2009, Circulation research.

[40]  Fedor V. Karginov,et al.  The miR-17∼92 cluster collaborates with the Sonic Hedgehog pathway in medulloblastoma , 2009, Proceedings of the National Academy of Sciences.

[41]  D. Bartel MicroRNAs: Target Recognition and Regulatory Functions , 2009, Cell.

[42]  Karl H. Plate,et al.  Angiogenesis after cerebral ischemia , 2009, Acta Neuropathologica.

[43]  C. Burge,et al.  Most mammalian mRNAs are conserved targets of microRNAs. , 2008, Genome research.

[44]  K. Barami Relationship of neural stem cells with their vascular niche: Implications in the malignant progression of gliomas , 2008, Journal of Clinical Neuroscience.

[45]  R. Simpson,et al.  Proteomic profiling of exosomes: Current perspectives , 2008, Proteomics.

[46]  Scott A Gerber,et al.  Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis , 2008, Proceedings of the National Academy of Sciences.

[47]  J. Mendell miRiad Roles for the miR-17-92 Cluster in Development and Disease , 2008, Cell.

[48]  R V Davuluri,et al.  A microRNA component of the hypoxic response , 2008, Cell Death and Differentiation.

[49]  Jing Wang,et al.  Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes , 2008, Nature Immunology.

[50]  Rudolf Jaenisch,et al.  Targeted Deletion Reveals Essential and Overlapping Functions of the miR-17∼92 Family of miRNA Clusters , 2008, Cell.

[51]  Chieh-Hsi Wu,et al.  Hypoxia-induced compensatory effect as related to Shh and HIF-1α in ischemia embryo rat heart , 2008, Molecular and Cellular Biochemistry.

[52]  Jordan S. Pober,et al.  Evolving functions of endothelial cells in inflammation , 2007, Nature Reviews Immunology.

[53]  S. Carmichael,et al.  A Neurovascular Niche for Neurogenesis after Stroke , 2006, The Journal of Neuroscience.

[54]  E. Lavik,et al.  Modeling the neurovascular niche: VEGF‐ and BDNF‐mediated cross‐talk between neural stem cells and endothelial cells: An in vitro study , 2006, Journal of neuroscience research.

[55]  H. Okano,et al.  Subventricular Zone-Derived Neuroblasts Migrate and Differentiate into Mature Neurons in the Post-Stroke Adult Striatum , 2006, The Journal of Neuroscience.

[56]  J. LaManna,et al.  The neurovascular unit and its growth factors: coordinated response in the vascular and nervous systems , 2004, Neurological research.

[57]  Sally Temple,et al.  Endothelial Cells Stimulate Self-Renewal and Expand Neurogenesis of Neural Stem Cells , 2004, Science.

[58]  E. Fuchs,et al.  Socializing with the Neighbors Stem Cells and Their Niche , 2004, Cell.

[59]  G. I. Hatton,et al.  Anatomy of the brain neurogenic zones revisited: Fractones and the fibroblast/macrophage network , 2002, The Journal of comparative neurology.

[60]  O. Lindvall,et al.  Neuronal replacement from endogenous precursors in the adult brain after stroke , 2002, Nature Medicine.

[61]  Steven A. Goldman,et al.  Coordinated Interaction of Neurogenesis and Angiogenesis in the Adult Songbird Brain , 2002, Neuron.

[62]  T. Palmer,et al.  Vascular niche for adult hippocampal neurogenesis , 2000, The Journal of comparative neurology.

[63]  M. Vidal,et al.  Aggregation reroutes molecules from a recycling to a vesicle-mediated secretion pathway during reticulocyte maturation. , 1997, Journal of cell science.

[64]  W. Risau,et al.  Mechanisms of angiogenesis , 1997, Nature.

[65]  Y Alsafadi,et al.  Observer detection performance in radiology using a retransmission-free network communication protocol. , 1994, Academic radiology.

[66]  M. Simona,et al.  CD157-extracellular matrix proteins interactions enhance integrin-mediated signalling cascade in monocytes , 2013 .

[67]  Y. Suárez,et al.  MicroRNAs As Novel Regulators of Angiogenesis Role of MicroRNAs in Cardiac Development , 2009 .