NogoR1 and PirB signaling stimulates neural stem cell survival and proliferation

Stem Cells

Volumn 32, Issue 6, 2014, Pages 1636-1648

  Ramasamy, Srinivas ^a   Yu, Fenggang ^b   Hong Yu, Yuan ^a   Srivats, Hariharan ^a   Stewart Dawe, Gavin ^c   Ahmed, Sohail ^a,b  

^a INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cell signaling; Neural stem cell; Progenitor cells; Proliferation

Indexed keywords

PROTEIN DERIVATIVE; PROTEIN NOGO; PROTEIN PIRB; UNCLASSIFIED DRUG; APOLIPOPROTEIN E; CELL SURFACE RECEPTOR; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; IMMUNOGLOBULIN RECEPTOR; MYELIN PROTEIN; PIRB PROTEIN, MOUSE; PROTEOCHONDROITIN SULFATE; RTN4R PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; MOUSE; NEOCORTEX; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR AFFINITY; SIGNAL TRANSDUCTION; ANIMAL EMBRYO; AUTOCRINE EFFECT; CELL COUNT; CELL SIZE; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; EMBRYOLOGY; FEMALE; FOREBRAIN; HEK293 CELL LINE; HUMAN; METABOLISM; MULTICELLULAR SPHEROID; PARACRINE SIGNALING; TUMOR CELL LINE;

APOLIPOPROTEINS E; AUTOCRINE COMMUNICATION; CELL COUNT; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CHONDROITIN SULFATE PROTEOGLYCANS; EMBRYO, MAMMALIAN; FEMALE; GPI-LINKED PROTEINS; HEK293 CELLS; HUMANS; MYELIN PROTEINS; NEURAL STEM CELLS; PARACRINE COMMUNICATION; PROSENCEPHALON; RECEPTORS, CELL SURFACE; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR;

EID: 84901436889     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1645     Document Type: Article

References (83)

1. Williams BP, Price J,. Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron 1995; 14: 1181-1188.
2. Temple S,. The development of neural stem cells. Nature 2001; 414: 112-117.
3. Takahashi T, Goto T, Miyama S, et al. Sequence of neuron origin and neocortical laminar fate: Relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 1999; 19: 10357-10371.
4. Takahashi T, Nowakowski RS, Caviness VS, Jr,. Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosci 1995; 15: 6058-6068.
5. Ramasamy S, Narayanan G, Sankaran S, et al. Neural stem cell survival factors. Arch Biochem Biophys 2013; 534: 71-87.
6. Chang M, Park C, Lee S,. Embryonic cortical stem cells secrete diffusible factors to enhance their survival. Neuroreport 2003; 14: 1191-1195.
7. Taupin P, Ray J, Fischer W, et al. FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 2000; 28: 385-397.
8. Kalani M, Cheshier S, Cord B, et al. Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci USA 2008; 105: 16970-16975.
9. Sousa VH, Fishell G,. Sonic hedgehog functions through dynamic changes in temporal competence in the developing forebrain. Curr Opin Genet Dev 2010; 20: 391-399.
10. Lillien L, Raphael H,. BMP and FGF regulate the development of EGF-responsive neural progenitor cells. Development 2000; 127: 4993-5005.
11. Theus MH, Ricard J, Bethea JR, et al. EphB3 limits the expansion of neural progenitor cells in the subventricular zone by regulating p53 during homeostasis and following traumatic brain injury. Stem Cells 2010; 28: 1231-1242.
12. Chen HL, Panchision DM,. Concise review: Bone morphogenetic protein pleiotropism in neural stem cells and their derivatives-Alternative pathways, convergent signals. Stem Cells 2007; 25: 63-68.
13. Sakaguchi DS, Van Hoffelen SJ, Theusch E, et al. Transplantation of neural progenitor cells into the developing retina of the Brazilian opossum: An in vivo system for studying stem/progenitor cell plasticity. Dev Neurosci 2004; 26: 336-345.
14. del Valle K, Theus MH, Bethea JR, et al. Neural progenitors proliferation is inhibited by EphB3 in the developing subventricular zone. Int J Dev Neurosci 2011; 29: 9-14.
15. Reynolds BA, Weiss S,. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255: 1707-1710.
16. Tham M, Ramasamy S, Gan HT, et al. CSPG is a secreted factor that stimulates neural stem cell survival possibly by enhanced EGFR signaling. Plos One 2010; 5: e15341.
17. Gan HT, Tham M, Hariharan S, et al. Identification of ApoE as an autocrine/paracrine factor that stimulates neural stem cell survival via MAPK/ERK signaling pathway. J Neurochem 2011; 117: 565-578.
18. Mingorance A, Soriano-Garcia E, del Rio JA,. Nogo-A functions during the development of the central nervous system and in the adult. Rev Neurol 2004; 39: 440-446.
19. Mingorance-Le Meur A, Zheng B, Soriano E, et al. Involvement of the myelin-associated inhibitor Nogo-A in early cortical development and neuronal maturation. Cereb Cortex 2007; 17: 2375-2386.
20. Mathis C, Schroter A, Thallmair M, et al. Nogo-a regulates neural precursor migration in the embryonic mouse cortex. Cereb Cortex 2010; 20: 2380-2390.
21. Gil V, Bichler Z, Lee JK, et al. Developmental expression of the oligodendrocyte myelin glycoprotein in the mouse telencephalon. Cereb Cortex 2010; 20: 1769-1779.
22. Mathis C, Schroter A, Thallmair M, et al. Nogo-a regulates neural precursor migration in the embryonic mouse cortex. Cereb Cortex 2010; 20: 2380-2390.
23. Schwab ME,. Functions of Nogo proteins and their receptors in the nervous system. Nat Rev Neurosci 2010; 11: 799-811.
24. Fournier AE, GrandPre T, Strittmatter SM,. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001; 409: 341-346.
25. Fournier AE, Strittmatter SM,. Repulsive factors and axon regeneration in the CNS. Curr Opin Neurobiol 2001; 11: 89-94.
26. Atwal JK, Pinkston-Gosse J, Syken J, et al. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008; 322: 967-970.
27. Fournier AE, Gould GC, Liu BP, et al. Truncated soluble Nogo receptor binds Nogo-66 and blocks inhibition of axon growth by myelin. J Neurosci 2002; 22: 8876-8883.
28. Fournier AE, GrandPre T, Gould G, et al. Nogo and the Nogo-66 receptor. Prog Brain Res 2002; 137: 361-369.
29. Wong ST, Henley JR, Kanning KC, et al. A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat Neurosci 2002; 5: 1302-1308.
30. Oertle T, van der Haar ME, Bandtlow CE, et al. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J Neurosci 2003; 23: 5393-5406.
31. Li M, Li Y, Liao X, et al. Rational design, solution conformation and identification of functional residues of the soluble and structured Nogo-54, which mimics Nogo-66 in inhibiting the CNS neurite outgrowth. Biochem Biophys Res Commun 2008; 373: 498-503.
32. Wang KC, Kim JA, Sivasankaran R, et al. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 2002; 420: 74-78.
33. Josephson A, Widenfalk J, Widmer HW, et al. NOGO mRNA expression in adult and fetal human and rat nervous tissue and in weight drop injury. Exp Neurol 2001; 169: 319-328.
34. Huber AB, Weinmann O, Brosamle C, et al. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J Neurosci 2002; 22: 3553-3567.
35. Tozaki H, Kawasaki T, Takagi Y, et al. Expression of Nogo protein by growing axons in the developing nervous system. Brain Res Mol Brain Res 2002; 104: 111-119.
36. Petrinovic MM, Duncan CS, Bourikas D, et al. Neuronal Nogo-A regulates neurite fasciculation, branching and extension in the developing nervous system. Development 2010; 137: 2539-2550.
37. Wang X, Baughman KW, Basso DM, et al. Delayed Nogo receptor therapy improves recovery from spinal cord contusion. Ann Neurol 2006; 60: 540-549.
38. Dickendesher TL, Baldwin KT, Mironova YA, et al. NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci 2012; 15: 703-712.
39. Rolando C, Parolisi R, Boda E, et al. Distinct roles of Nogo-a and Nogo receptor 1 in the homeostatic regulation of adult neural stem cell function and neuroblast migration. J Neurosci 2012; 32: 17788-17799.
40. Wang B, Xiao Z, Chen B, et al. Nogo-66 promotes the differentiation of neural progenitors into astroglial lineage cells through mTOR-STAT3 pathway. PLoS ONE 2008; 3: e1856.
41. Gao Y, Wang B, Xiao Z, et al. Nogo-66 regulates nanog expression through stat3 pathway in murine embryonic stem cells. Stem Cells Dev 2010; 19: 53-60.
42. Gao Y, Xiao Z, Chen B, et al. Effect of different regions of Nogo-A on the differentiation of neural progenitors. Neurosci Lett 2009; 458: 132-135.
43. Govind S, Kozma R, Monfries C, et al. Cdc42Hs facilitates cytoskeletal reorganization and neurite outgrowth by localizing the 58-kD insulin receptor substrate to filamentous actin. J Cell Biol 2001; 152: 579-594.
44. Ramasamy S, Wang H, Quach HN, et al. Zebrafish Staufen1 and Staufen2 are required for the survival and migration of primordial germ cells. Dev Biol 2006; 292: 393-406.
45. Shen Y, Tenney AP, Busch SA, et al. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009; 326: 592-596.
46. Syken J, Grandpre T, Kanold PO, et al. PirB restricts ocular-dominance plasticity in visual cortex. Science 2006; 313: 1795-1800.
47. Wood JN, Bevan SJ, Coote PR, et al. Novel cell lines display properties of nociceptive sensory neurons. Proc Biol Sci 1990; 241: 187-194.
48. Ujike A, Takeda K, Nakamura A, et al. Impaired dendritic cell maturation and increased T(H)2 responses in PIR-B(-/-) mice. Nat Immunol 2002; 3: 542-548.
49. Zheng B, Atwal J, Ho C, et al. Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proc Natl Acad Sci USA 2005; 102: 1205-1210.
50. Coles-Takabe BL, Brain I, Purpura KA, et al. Don't look: Growing clonal versus nonclonal neural stem cell colonies. Stem Cells 2008; 26: 2938-2944.
51. Wang H, Liu Z, Li D, et al. Injectable biodegradable hydrogels for embryonic stem cell transplantation: Improved cardiac remodelling and function of myocardial infarction. J Cell Mol Med 2012; 16: 1310-1320.
52. Li M, Liu J, Song J,. Nogo goes in the pure water: Solution structure of Nogo-60 and design of the structured and buffer-soluble Nogo-54 for enhancing CNS regeneration. Protein Sci 2006; 15: 1835-1841.
53. He XL, Bazan JF, McDermott G, et al. Structure of the Nogo receptor ectodomain: A recognition module implicated in myelin inhibition. Neuron 2003; 38: 177-185.
54. Llorens F, Gil V, del Rio JA,. Emerging functions of myelin-associated proteins during development, neuronal plasticity, and neurodegeneration. FASEB J 2011; 25: 463-475.
55. Caltharp SA, Pira CU, Mishima N, et al. NOGO-A induction and localization during chick brain development indicate a role disparate from neurite outgrowth inhibition. BMC Dev Biol 2007; 7: 32.
56. Buss A, Sellhaus B, Wolmsley A, et al. Expression pattern of NOGO-A protein in the human nervous system. Acta Neuropathol 2005; 110: 113-119.
57. Al Halabiah H, Delezoide AL, Cardona A, et al. Expression pattern of NOGO and NgR genes during human development. Gene Expr Patterns 2005; 5: 561-568.
58. Conover JC, Notti RQ,. The neural stem cell niche. Cell Tissue Res 2008; 331: 211-224.
59. Kazanis I, ffrench-Constant C,. Extracellular matrix and the neural stem cell niche. Dev Neurobiol 2011; 71: 1006-1017.
60. Sirko S, Akita K, Von Holst A, et al. Structural and functional analysis of chondroitin sulfate proteoglycans in the neural stem cell niche. Methods Enzymol 2010; 479: 37-71.
61. Sirko S, von Holst A, Wizenmann A, et al. Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 2007; 134: 2727-2738.
62. Garcion E, Halilagic A, Faissner A, et al. Generation of an environmental niche for neural stem cell development by the extracellular matrix molecule tenascin C. Development 2004; 131: 3423-3432.
63. von Holst A, Egbers U, Prochiantz A, et al. Neural stem/progenitor cells express 20 tenascin C isoforms that are differentially regulated by Pax6. J Biol Chem 2007; 282: 9172-9181.
64. von Holst A, Sirko S, Faissner A,. The unique 473HD-Chondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J Neurosci 2006; 26: 4082-4094.
65. Barton WA, Liu BP, Tzvetkova D, et al. Structure and axon outgrowth inhibitor binding of the Nogo-66 receptor and related proteins. EMBO J 2003; 22: 3291-3302.
66. Reynolds B, Tetzlaff W, Weiss S,. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 1992; 12: 4565-4574.
67. Vescovi A, Reynolds B, Fraser D, et al. bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 1993; 11: 951-966.
68. Maric D, Fiorio Pla A, Chang YH, et al. Self-renewing and differentiating properties of cortical neural stem cells are selectively regulated by basic fibroblast growth factor (FGF) signaling via specific FGF receptors. J Neurosci 2007; 27: 1836-1852.
69. Komada M, Saitsu H, Kinboshi M, et al. Hedgehog signaling is involved in development of the neocortex. Development 2008; 135: 2717-2727.
70. Hitoshi S, Alexson T, Tropepe V, et al. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 2002; 16: 846-858.
71. Mizutani K, Yoon K, Dang L, et al. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 2007; 449: 351-355.
72. Hitoshi S, Seaberg RM, Koscik C, et al. Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signaling. Genes Dev 2004; 18: 1806-1811.
73. Androutsellis-Theotokis A, Leker RR, Soldner F, et al. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 2006; 442: 823-826.
74. Kalani MYS, Cheshier SH, Cord BJ, et al. Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci 2008; 105: 16970-16975.
75. Sivasankaran R, Pei J, Wang KC, et al. PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci 2004; 7: 261-268.
76. Yamashita T, Tohyama M,. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat Neurosci 2003; 6: 461-467.
77. Maeda A, Kurosaki M, Ono M, et al. Requirement of SH2-containing protein tyrosine phosphatases SHP-1 and SHP-2 for paired immunoglobulin-like receptor B (PIR-B)-mediated inhibitory signal. J Exp Med 1998; 187: 1355-1360.
78. Takai T,. Paired immunoglobulin-like receptors and their MHC class I recognition. Immunology 2005; 115: 433-440.
79. Takai T, Ono M,. Activating and inhibitory nature of the murine paired immunoglobulin-like receptor family. Immunol Rev 2001; 181: 215-222.
80. Jung TY, Jung S, Lee KH, et al. Nogo-A expression in oligodendroglial tumors. Neuropathology 2011; 31: 11-19.
81. Marucci G, Di Oto E, Farnedi A, et al. Nogo-A: A useful marker for the diagnosis of oligodendroglioma and for identifying 1p19q codeletion. Hum Pathol 2012; 43: 374-380.
82. Hsu R, Woodroffe A, Lai WS, et al. Nogo Receptor 1 (RTN4R) as a candidate gene for schizophrenia: Analysis using human and mouse genetic approaches. PLoS ONE 2007; 2: e1234.
83. Gregorio SP, Mury FB, Ojopi EB, et al. Nogo CAA 3'UTR Insertion polymorphism is not associated with Schizophrenia nor with bipolar disorder. Schizophr Res 2005; 75: 5-9.