Traffic lights for axon growth: Proteoglycans and their neuronal receptors

Neural Regeneration Research

Volumn 9, Issue 4, 2014, Pages 356-361

  Shen, Yingjie ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Axonal regeneration; Chondroitin sulfate and heparan sulfate proteoglycans

Indexed keywords

DERMATAN SULFATE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; GLYPICAN; HEPARIN LYASE; KERATAN SULFATE; LEUKOCYTE ANTIGEN; NEURITE PROMOTING FACTOR; NOGO 66 RECEPTOR; PROTEIN TYROSINE PHOSPHATASE; PROTEOCHONDROITIN SULFATE; PROTEOGLYCAN; PROTEOHEPARAN SULFATE; SEMAPHORIN;

ARTICLE; BRAIN ISCHEMIA; CELL MIGRATION; HUMAN; MIGRATING MYOELECTRIC COMPLEX; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE INJURY; PROTEIN EXPRESSION; SCIATIC NERVE INJURY; SIGNAL TRANSDUCTION; SPATIOTEMPORAL ANALYSIS;

EID: 84897068293     PISSN: 16735374     EISSN: 18767958     Source Type: Journal    
DOI: 10.4103/1673-5374.128236     Document Type: Article

References (77)

1. Alilain W. J, Horn KP, Hu H, Dick TE, Silver J (2011) Functional regeneration of respiratory pathways after spinal cord injury. Nature 475:196-200.
2. Aricescu A. R, McKinnell IW, Halfter W, Stoker AW (2002) Heparan sulfate proteoglycans are ligands for receptor protein tyrosine phosphatase sigma. Mol Cell Biol 22:1881-1892.
3. Asher R. A, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, Levine JM, Margolis RU, Rogers JH, Fawcett JW (2000) Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20:2427-2438.
4. B. T. Lang, M. A. Depaul, A. R. Filous, T. A. Evans, Y. L. Weng, A. Y. Huang, S. Li, J. Silver. (2012) Peptide inhibitors of LAR family phosphatases release CSPG mediated entrapment of axons and promote robust behavioral recovery following contusive spinal cord injury.
5. Bandtlow C. E, Zimmermann DR (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80:1267-1290.
6. Bartus K., James ND, Bosch KD, Bradbury EJ (2012) Chondroitin sulphate proteoglycans: key modulators of spinal cord and brain plasticity. Exp Neurol 235:5-17.
7. Bilwes A. M, den Hertog J, Hunter T, Noel JP (1996) Structural basis for inhibition of receptor protein-tyrosine phosphatase-alpha by dimerization. Nature 382:555-559.
8. Bloechlinger S., Karchewski LA, Woolf CJ (2004) Dynamic changes in glypican-1 expression in dorsal root ganglion neurons after peripheral and central axonal injury. Eur J Neurosci 19:1119-1132.
9. Bovolenta P., Fernaud-Espinosa I (2000) Nervous system proteoglycans as modulators of neurite outgrowth. Prog Neurobiol 61:113-132.
10. Bradbury E. J, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640.
11. Brittis P. A, Canning DR, Silver J (1992) Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science 255:733-736.
12. Busch S. A, Horn KP, Cuascut FX, Hawthorne AL, Bai L, Miller RH, Silver J (2010) Adult NG2+ cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage-induced axonal dieback after spinal cord injury. J Neurosci 30:255-265.
13. Busch S. A, Silver J (2007) The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 17:120-127.
14. Cafferty W. B, Strittmatter SM (2006) The Nogo-Nogo receptor pathway limits a spectrum of adult CNS axonal growth. J Neurosci 26:12242-12250.
15. Chagnon M. J, Uetani N, Tremblay ML (2004) Functional significance of the LAR receptor protein tyrosine phosphatase family in development and diseases. Biochem Cell Biol 82:664-675.
16. Coles C. H, Shen Y, Tenney AP, Siebold C, Sutton GC, Lu W, Gallagher JT, Jones EY, Flanagan JG, Aricescu AR (2011) Proteoglycan-specific molecular switch for RPTPsigma clustering and neuronal extension. Science 332:484-488.
17. Davies S. J, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-683.
18. Dickendesher T. L, Baldwin KT, Mironova YA, Koriyama Y, Raiker SJ, Askew K. L, Wood A, Geoffroy CG, Zheng B, Liepmann CD, Katagiri Y, Benowitz L. I, Geller HM, Giger RJ (2012) NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci 15:703-712.
19. Dunah A. W, Hueske E, Wyszynski M, Hoogenraad CC, Jaworski J, Pak DT, Simonetta A, Liu G, Sheng M (2005) LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci 8:458-467.
20. Fisher D., Xing B, Dill J, Li H, Hoang HH, Zhao Z, Yang XL, Bachoo R, Cannon S, Longo FM, Sheng M, Silver J, Li S (2011) Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J Neurosci 31:14051-14066.
21. Fox A. N, Zinn K (2005) The heparan sulfate proteoglycan syndecan is an in vivo ligand for the Drosophila LAR receptor tyrosine phosphatase. Curr Biol 15:1701-1711.
22. Fry E. J, Chagnon MJ, Lopez-Vales R, Tremblay ML, David S (2010) Corticospinal tract regeneration after spinal cord injury in receptor protein tyrosine phosphatase sigma deficient mice. Glia 58:423-433.
23. Garcia de Yebenes E, Ho A, Damani T, Fillit H, Blum M (1999) Regulation of the heparan sulfate proteoglycan, perlecan, by injury and interleukin-1alpha. J Neurochem 73:812-820.
24. Garcia-Alias G., Barkhuysen S, Buckle M, Fawcett JW (2009) Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 12:1145-1151.
25. Garcia-Alias G., Fawcett JW (2012) Training and anti-CSPG combination therapy for spinal cord injury. Exp Neurol 235:26-32.
26. Gardner R. T, Habecker BA (2013) Infarct-derived chondroitin sulfate proteoglycans prevent sympathetic reinnervation after cardiac ischemia-reperfusion injury. J Neurosci 33:7175-7183.
27. Garrity P. A, Lee CH, Salecker I, Robertson HC, Desai CJ, Zinn K, Zipursky SL (1999) Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase. Neuron 22:707-717.
28. Haworth K., Shu KK, Stokes A, Morris R, Stoker A (1998) The expression of receptor tyrosine phosphatases is responsive to sciatic nerve crush. Mol Cell Neurosci 12:93-104.
29. Hendriks W. J, Elson A, Harroch S, Pulido R, Stoker A, den Hertog J (2013) Protein tyrosine phosphatases in health and disease. FEBS J 280:708-730.
30. Hill J. J, Jin K, Mao XO, Xie L, Greenberg DA (2012) Intracerebral chondroitinase ABC and heparan sulfate proteoglycan glypican improve outcome from chronic stroke in rats. Proc Natl Acad Sci U S A 109: 9155-9160.
31. Horn K. E, Xu B, Gobert D, Hamam BN, Thompson KM, Wu CL, Bouchard J. F, Uetani N, Racine RJ, Tremblay ML, Ruthazer ES, Chapman CA, Kennedy TE (2012) Receptor protein tyrosine phosphatase sigma regulates synapse structure, function and plasticity. J Neurochem 122:147-161.
32. Hsueh Y. P, Sheng M (1999) Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development. J Neurosci 19:7415-7425.
33. Iseki K., Hagino S, Mori T, Zhang Y, Yokoya S, Takaki H, Tase C, Murakawa M., Wanaka A (2002) Increased syndecan expression by pleiotrophin and FGF receptor-expressing astrocytes in injured brain tissue. Glia 39:1-9.
34. Ivins J. K, Litwack ED, Kumbasar A, Stipp CS, Lander AD (1997) Cerebroglycan, a developmentally regulated cell-surface heparan sulfate proteoglycan, is expressed on developing axons and growth cones. Dev Biol 184:320-332.
35. Johnson K. G, Holt CE (2000) Expression of CRYP-alpha, LAR, PTP-delta, and PTP-rho in the developing Xenopus visual system. Mech Dev 92:291-294.
36. Johnson K. G, Tenney AP, Ghose A, Duckworth AM, Higashi ME, Parfitt K, Marcu O, Heslip TR, Marsh JL, Schwarz TL, Flanagan JG, Van Vactor D (2006) The HSPGs Syndecan and Dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron 49:517-531.
37. Jones L. L, Margolis RU, Tuszynski MH (2003) The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol 182:399-411.
38. Kantor D. B, Chivatakarn O, Peer KL, Oster SF, Inatani M, Hansen MJ, Flanagan J. G, Yamaguchi Y, Sretavan DW, Giger RJ, Kolodkin AL (2004) Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44:961-975.
39. Kim J. E, Liu BP, Park JH, Strittmatter SM (2004) Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron 44:439-451.
40. Kwon S. K, Woo J, Kim SY, Kim H, Kim E (2010) Trans-synaptic adhesions between netrin-G ligand-3 (NGL-3) and receptor tyrosine phosphatases LAR, protein-tyrosine phosphatase delta (PTPdelta), and PTPsigma via specific domains regulate excitatory synapse formation. J Biol Chem 285:13966-13978.
41. Lauren J., Airaksinen MS, Saarma M, Timmusk T (2003) Two novel mammalian Nogo receptor homologs differentially expressed in the central and peripheral nervous systems. Mol Cell Neurosci 24:581-594.
42. Lauren J., Hu F, Chin J, Liao J, Airaksinen MS, Strittmatter SM (2007) Characterization of myelin ligand complexes with neuronal Nogo-66 receptor family members. J Biol Chem 282:5715-5725.
43. Ledig M. M, Haj F, Bixby JL, Stoker AW, Mueller BK (1999) The receptor tyrosine phosphatase CRYPalpha promotes intraretinal axon growth. J Cell Biol 147:375-388.
44. Maeda N., Ishii M, Nishimura K, Kamimura K (2011) Functions of chondroitin sulfate and heparan sulfate in the developing brain. Neurochem Res 36:1228-1240.
45. Massey J. M, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, Onifer S. M (2006) Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci 26:4406-4414.
46. McGee A. W, Yang Y, Fischer QS, Daw NW, Strittmatter SM (2005) Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 309:2222-2226.
47. McKeon R. J, Schreiber RC, Rudge JS, Silver J (1991) Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398-3411.
48. McLean J., Batt J, Doering LC, Rotin D, Bain JR (2002) Enhanced rate of nerve regeneration and directional errors after sciatic nerve injury in receptor protein tyrosine phosphatase sigma knock-out mice. J Neurosci 22:5481-5491.
49. Milev P., Maurel P, Chiba A, Mevissen M, Popp S, Yamaguchi Y, Margolis RK, Margolis RU (1998) Differential regulation of expression of hyaluronan-binding proteoglycans in developing brain: aggrecan, versican, neurocan, and brevican. Biochem Biophys Res Commun 247:207-212.
50. Mueller B. K, Ledig MM, Wahl S (2000) The receptor tyrosine phosphatase CRYPalpha affects growth cone morphology. J Neurobiol 44:204-218.
51. Oohira A., Matsui F, Watanabe E, Kushima Y, Maeda N (1994) Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody IG2 in the rat cerebrum. Neuroscience 60:145-157.
52. Pindzola R. R, Doller C, Silver J (1993) Putative inhibitory extracellular matrix molecules at the dorsal root entry zone of the spinal cord during development and after root and sciatic nerve lesions. Dev Biol 156:34-48.
53. Properzi F., Lin R, Kwok J, Naidu M, van Kuppevelt TH, Ten Dam GB, Camargo L. M, Raha-Chowdhury R, Furukawa Y, Mikami T, Sugahara K, Fawcett JW (2008) Heparan sulphate proteoglycans in glia and in the normal and injured CNS: expression of sulphotransferases and changes in sulphation. Eur J Neurosci 27:593-604.
54. Pulido R., Serra-Pages C, Tang M, Streuli M (1995) The LAR/PTP delta/ PTPsigma subfamily of transmembrane protein-tyrosine-phosphatases: multiple human LAR, PTP delta, and PTPsigma isoforms are expressed in a tissue-specific manner and associate with the LAR-interacting protein LIP.1. Proc Natl Acad Sci U S A 92:11686-11690.
55. Sapieha P. S, Duplan L, Uetani N, Joly S, Tremblay ML, Kennedy TE, Di Polo A. (2005) Receptor protein tyrosine phosphatase sigma inhibits axon regrowth in the adult injured CNS. Mol Cell Neurosci 28:625-635.
56. Schaapveld R. Q, Schepens JT, Bachner D, Attema J, Wieringa B, Jap PH, Hendriks W. J (1998) Developmental expression of the cell adhesion molecule-like protein tyrosine phosphatases LAR, RPTPdelta and RPTPsigma in the mouse. Mech Dev 77:59-62.
57. Shen Y., Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, Flanagan J. G (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326:592-596.
58. Snow D. M, Lemmon V, Carrino DA, Caplan AI, Silver J (1990) Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109:111-130.
59. Snow D. M, Watanabe M, Letourneau PC, Silver J (1991) A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth. Development 113:1473-1485.
60. Stipp C. S, Litwack ED, Lander AD (1994) Cerebroglycan: an integral membrane heparan sulfate proteoglycan that is unique to the developing nervous system and expressed specifically during neuronal differentiation. J Cell Biol 124:149-160.
61. Takahashi H., Craig AM (2013) Protein tyrosine phosphatases PTPdelta, PTPsigma, and LAR: presynaptic hubs for synapse organization. Trends Neurosci 36:522-534.
62. Takahashi H., Katayama K, Sohya K, Miyamoto H, Prasad T, Matsumoto Y, Ota M, Yasuda H, Tsumoto T, Aruga J, Craig AM (2012) Selective control of inhibitory synapse development by Slitrk3-PTPdelta trans-synaptic interaction. Nat Neurosci 15:389-398, S381-382.
63. Thompson K. (2003) Receptor protein tyrosine phosphatase sigma inhibits axonal regeneration and the rate of axon extension. Mol Cell Neurosci 23:681-692.
64. Van der Zee CE, Man TY, Van Lieshout EM, Van der Heijden I, Van Bree M, Hendriks WJ (2003) Delayed peripheral nerve regeneration and central nervous system collateral sprouting in leucocyte common antigen-related protein tyrosine phosphatase-deficient mice. Eur J Neurosci 17:991-1005.
65. Venkatesh K., Chivatakarn O, Lee H, Joshi PS, Kantor DB, Newman BA, Mage R., Rader C, Giger RJ (2005) The Nogo-66 receptor homolog NgR2 is a sialic acid-dependent receptor selective for myelin-associated glycoprotein. J Neurosci 25:808-822.
66. Wallace M. J, Fladd C, Batt J, Rotin D (1998) The second catalytic domain of protein tyrosine phosphatase delta (PTP delta) binds to and inhibits the first catalytic domain of PTPsigma. Mol Cell Biol 18:2608-2616.
67. Wang D., Fawcett J (2012) The perineuronal net and the control of CNS plasticity. Cell Tissue Res 349:147-160.
68. Wang F., Wolfson SN, Gharib A, Sagasti A (2012) LAR receptor tyrosine phosphatases and HSPGs guide peripheral sensory axons to the skin. Curr Biol 22:373-382.
69. Wang H., Yan H, Canoll PD, Silvennoinen O, Schlessinger J, Musacchio JM (1995) Expression of receptor protein tyrosine phosphatase-sigma (RPTP-sigma) in the nervous system of the developing and adult rat. J Neurosci Res 41:297-310.
70. Wang K. C, Kim JA, Sivasankaran R, Segal R, He Z (2002a) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420:74-78.
71. Wang X., Chun SJ, Treloar H, Vartanian T, Greer CA, Strittmatter SM (2002b) Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J Neurosci 22:5505-5515.
72. Wilson M. T, Snow DM (2000) Chondroitin sulfate proteoglycan expression pattern in hippocampal development: potential regulation of axon tract formation. J Comp Neurol 424:532-546.
73. Xie Y., Yeo TT, Zhang C, Yang T, Tisi MA, Massa SM, Longo FM (2001) The leukocyte common antigen-related protein tyrosine phosphatase receptor regulates regenerative neurite outgrowth in vivo. J Neurosci 21:5130-5138.
74. Yan H., Grossman A, Wang H, D'Eustachio P, Mossie K, Musacchio JM, Silvennoinen O, Schlessinger J (1993) A novel receptor tyrosine phosphatase-sigma that is highly expressed in the nervous system. J Biol Chem 268:24880-24886.
75. Yi J. H, Katagiri Y, Susarla B, Figge D, Symes AJ, Geller HM (2012) Alterations in sulfated chondroitin glycosaminoglycans following controlled cortical impact injury in mice. J Comp Neurol 520:3295-3313.
76. Zhang J. S, Honkaniemi J, Yang T, Yeo TT, Longo FM (1998) LAR tyrosine phosphatase receptor: A developmental isoform is present in neurites and growth cones and its expression is regional-and cell-specific. Mol Cell Neurosci 10:271-286.
77. Zheng B., Atwal J, Ho C, Case L, He XL, Garcia KC, Steward O, Tessier-Lavigne M. (2005) Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proc Natl Acad Sci U S A 102:1205-1210.