Pleiotropic molecules in axon regeneration and neuroinflammation

Experimental Neurology

Volumn 258, Issue , 2014, Pages 17-23

  Lang, Bradley T ^b   Wang, Jian ^a   Filous, Angela R ^b   Au, Ngan Pan Bennett ^c   Ma, Chi Him Eddie ^c   Shen, Yingjie ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c CITY UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Axon regeneration; Myelin associated inhibitors and receptors; Neuroinflammation; Proteoglycans

Indexed keywords

GROWTH INHIBITOR; MYELIN; MYELIN ASSOCIATED GLYCOPROTEIN; OLIGODENDROCYTE MYELIN GLYCOPROTEIN; PAIRED IMMUNOGLOBULIN LIKE RECEPTOR B; PROTEIN NOGO A; PROTEOCHONDROITIN SULFATE; PROTEOHEPARAN SULFATE; RECEPTOR; UNCLASSIFIED DRUG;

CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; GLIA; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; INFLAMMATION; INNATE IMMUNITY; MEDIATOR RELEASE; NERVE FIBER REGENERATION; NERVE REGENERATION; NERVOUS SYSTEM INFLAMMATION; NERVOUS SYSTEM INJURY; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; REVIEW; SCAR FORMATION; SIGNAL TRANSDUCTION; TISSUE INJURY;

AXON REGENERATION; MYELIN-ASSOCIATED INHIBITORS AND RECEPTORS; NEUROINFLAMMATION; PROTEOGLYCANS;

ANIMALS; AXONS; GENETIC PLEIOTROPY; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; NERVE REGENERATION; NEURONS;

EID: 84904723515     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.04.031     Document Type: Review

References (120)

1. Akbik F., Cafferty W.B., Strittmatter S.M. Myelin associated inhibitors: a link between injury-induced and experience-dependent plasticity. Exp. Neurol. 2012, 235:43-52.
2. Alilain W.J., Horn K.P., Hu H., Dick T.E., Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature 2011, 475:196-200.
3. Andersson M., Yu M., Soderstrom M., Weerth S., Baig S., Solders G., Link H. Multiple MAG peptides are recognized by circulating T and B lymphocytes in polyneuropathy and multiple sclerosis. Eur. J. Neurol. 2002, 9:243-251.
4. Ang B.T., Xu G., Xiao Z.C. Therapeutic vaccination for central nervous system repair. Clin. Exp. Pharmacol. Physiol. 2006, 33:541-545.
5. Ankeny D.P., Popovich P.G. B cells and autoantibodies: complex roles in CNS injury. Trends Immunol. 2010, 31:332-338.
6. Asher R.A., Morgenstern D.A., Fidler P.S., Adcock K.H., Oohira A., Braistead J.E., Levine J.M., Margolis R.U., Rogers J.H., Fawcett J.W. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J. Neurosci. 2000, 20:2427-2438.
7. Atwal J.K., Pinkston-Gosse J., Syken J., Stawicki S., Wu Y., Shatz C., Tessier-Lavigne M. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008, 322:967-970.
8. Bandtlow C.E., Zimmermann D.R. Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev. 2000, 80:1267-1290.
9. Barnett M.H., Sutton I. The pathology of multiple sclerosis: a paradigm shift. Curr. Opin. Neurol. 2006, 19:242-247.
10. Bartsch U., Bandtlow C.E., Schnell L., Bartsch S., Spillmann A.A., Rubin B.P., Hillenbrand R., Montag D., Schwab M.E., Schachner M. Lack of evidence that myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS. Neuron 1995, 15:1375-1381.
11. Bartus K., James N.D., Bosch K.D., Bradbury E.J. Chondroitin sulphate proteoglycans: key modulators of spinal cord and brain plasticity. Exp. Neurol. 2012, 235:5-17.
12. Bloechlinger S., Karchewski L.A., Woolf C.J. Dynamic changes in glypican-1 expression in dorsal root ganglion neurons after peripheral and central axonal injury. Eur. J. Neurosci. 2004, 19:1119-1132.
13. Borrie S.C., Baeumer B.E., Bandtlow C.E. The Nogo-66 receptor family in the intact and diseased CNS. Cell Tissue Res. 2012, 349:105-117.
14. Bovolenta P., Fernaud-Espinosa I. Nervous system proteoglycans as modulators of neurite outgrowth. Prog. Neurobiol. 2000, 61:113-132.
15. Brittis P.A., Canning D.R., Silver J. Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science 1992, 255:733-736.
16. Busch S.A., Silver J. The role of extracellular matrix in CNS regeneration. Curr. Opin. Neurobiol. 2007, 17:120-127.
17. Cafferty W.B., Duffy P., Huebner E., Strittmatter S.M. MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J. Neurosci. 2010, 30:6825-6837.
18. Cafferty W.B., Strittmatter S.M. The Nogo-Nogo receptor pathway limits a spectrum of adult CNS axonal growth. J. Neurosci. 2006, 26:12242-12250.
19. Cai D., Shen Y., De Bellard M., Tang S., Filbin M.T. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 1999, 22:89-101.
20. Cao Z., Gao Y., Deng K., Williams G., Doherty P., Walsh F.S. Receptors for myelin inhibitors: structures and therapeutic opportunities. Mol. Cell. Neurosci. 2010, 43:1-14.
21. Caroni P., Schwab M.E. Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1988, 1:85-96.
22. Chen M.S., Huber A.B., van der Haar M.E., Frank M., Schnell L., Spillmann A.A., Christ F., Schwab M.E. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 2000, 403:434-439.
23. Coles C.H., Shen Y., Tenney A.P., Siebold C., Sutton G.C., Lu W., Gallagher J.T., Jones E.Y., Flanagan J.G., Aricescu A.R. Proteoglycan-specific molecular switch for RPTP sigma clustering and neuronal extension. Science 2011, 332:484-488.
24. David S., Braun P.E., Jackson D.L., Kottis V., McKerracher L. Laminin overrides the inhibitory effects of peripheral nervous system and central nervous system myelin-derived inhibitors of neurite growth. J. Neurosci. Res. 1995, 42:594-602.
25. David S., Fry E.J., Lopez-Vales R. Novel roles for Nogo receptor in inflammation and disease. Trends Neurosci. 2008, 31:221-226.
26. Davies S.J., Fitch M.T., Memberg S.P., Hall A.K., Raisman G., Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 1997, 390:680-683.
27. Dickendesher T.L., Baldwin K.T., Mironova Y.A., Koriyama Y., Raiker S.J., Askew K.L., Wood A., Geoffroy C.G., Zheng B., Liepmann C.D., et al. NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat. Neurosci. 2012, 15:703-712.
28. Dimou L., Schnell L., Montani L., Duncan C., Simonen M., Schneider R., Liebscher T., Gullo M., Schwab M.E. Nogo-A-deficient mice reveal strain-dependent differences in axonal regeneration. J. Neurosci. 2006, 26:5591-5603.
29. Domeniconi M., Cao Z., Spencer T., Sivasankaran R., Wang K., Nikulina E., Kimura N., Cai H., Deng K., Gao Y., et al. Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 2002, 35:283-290.
30. Fawcett J.W., Asher R.A. The glial scar and central nervous system repair. Brain Res. Bull. 1999, 49:377-391.
31. Felts P.A., Woolston A.M., Fernando H.B., Asquith S., Gregson N.A., Mizzi O.J., Smith K.J. Inflammation and primary demyelination induced by the intraspinal injection of lipopolysaccharide. Brain 2005, 128:1649-1666.
32. Filbin M.T. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 2003, 4:703-713.
33. Fisher D., Xing B., Dill J., Li H., Hoang H.H., Zhao Z., Yang X.L., Bachoo R., Cannon S., Longo F.M., et al. Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J. Neurosci. 2011, 31:14051-14066.
34. Fournier A.E., GrandPre T., Strittmatter S.M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001, 409:341-346.
35. Fry E.J., Ho C., David S. A role for Nogo receptor in macrophage clearance from injured peripheral nerve. Neuron 2007, 53:649-662.
36. Fujita Y., Endo S., Takai T., Yamashita T. Myelin suppresses axon regeneration by PIR-B/SHP-mediated inhibition of Trk activity. EMBO J. 2011, 30:1389-1401.
37. Fujita Y., Takashima R., Endo S., Takai T., Yamashita T. The p75 receptor mediates axon growth inhibition through an association with PIR-B. Cell Death Dis. 2011, 2:e198.
38. Garcia-Alias G., Fawcett J.W. Training and anti-CSPG combination therapy for spinal cord injury. Exp. Neurol. 2012, 235:26-32.
39. Gaudet A.D., Popovich P.G., Ramer M.S. Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury. J. Neuroinflammation 2011, 8:110.
40. Gaudet A.D., Popovich P.G. Extracellular matrix regulation of inflammation in the healthy and injured spinal cordy. Exp. Neurol. 2014, 258:24-34. (in this issue).
41. Gou X., Zhang Q., Xu N., Deng B., Wang H., Xu L., Wang Q. Spatio-temporal expression of paired immunoglobulin-like receptor-B in the adult mouse brain after focal cerebral ischaemia. Brain Inj. 2013, 27:1311-1315.
42. Griffin R.S., Costigan M., Brenner G.J., Ma C.H., Scholz J., Moss A., Allchorne A.J., Stahl G.L., Woolf C.J. Complement induction in spinal cord microglia results in anaphylatoxin C5a-mediated pain hypersensitivity. J. Neurosci. 2007, 27:8699-8708.
43. Gris D., Marsh D.R., Oatway M.A., Chen Y., Hamilton E.F., Dekaban G.A., Weaver L.C. Transient blockade of the CD11d/CD18 integrin reduces secondary damage after spinal cord injury, improving sensory, autonomic, and motor function. J. Neurosci. 2004, 24:4043-4051.
44. Hayes K.C., Hull T.C., Delaney G.A., Potter P.J., Sequeira K.A., Campbell K., Popovich P.G. Elevated serum titers of proinflammatory cytokines and CNS autoantibodies in patients with chronic spinal cord injury. J. Neurotrauma 2002, 19:753-761.
45. Hill J.J., Jin K., Mao X.O., Xie L., Greenberg D.A. Intracerebral chondroitinase ABC and heparan sulfate proteoglycan glypican improve outcome from chronic stroke in rats. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:9155-9160.
46. Hirata K., Kawabuchi M. Myelin phagocytosis by macrophages and nonmacrophages during Wallerian degeneration. Microsc. Res. Tech. 2002, 57:541-547.
47. Horn K.P., Busch S.A., Hawthorne A.L., van Rooijen N., Silver J. Another barrier to regeneration in the CNS: activated macrophages induce extensive retraction of dystrophic axons through direct physical interactions. J. Neurosci. 2008, 28:9330-9341.
48. Hsueh Y.P., Sheng M. Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development. J. Neurosci. 1999, 19:7415-7425.
49. Huang D.W., McKerracher L., Braun P.E., David S. A therapeutic vaccine approach to stimulate axon regeneration in the adult mammalian spinal cord. Neuron 1999, 24:639-647.
50. Johnson D., Hafler D.A., Fallis R.J., Lees M.B., Brady R.O., Quarles R.H., Weiner H.L. Cell-mediated immunity to myelin-associated glycoprotein, proteolipid protein, and myelin basic protein in multiple sclerosis. J. Neuroimmunol. 1986, 13:99-108.
51. Johnson P.W., Abramow-Newerly W., Seilheimer B., Sadoul R., Tropak M.B., Arquint M., Dunn R.J., Schachner M., Roder J.C. Recombinant myelin-associated glycoprotein confers neural adhesion and neurite outgrowth function. Neuron 1989, 3:377-385.
52. Jones L.L., Margolis R.U., Tuszynski M.H. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp. Neurol. 2003, 182:399-411.
53. Jones M.V., Nguyen T.T., Ewaleifoh O., Lebson L., Whartenby K.A., Griffin J.W., Calabresi P.A. Accelerated axon loss in MOG35-55 experimental autoimmune encephalomyelitis (EAE) in myelin-associated glycoprotein-deficient (MAGKO) mice. J. Neuroimmunol. 2013, 262:53-61.
54. Kantor D.B., Chivatakarn O., Peer K.L., Oster S.F., Inatani M., Hansen M.J., Flanagan J.G., Yamaguchi Y., Sretavan D.W., Giger R.J., et al. Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 2004, 44:961-975.
55. Karo-Atar D., Moshkovits I., Eickelberg O., Konigshoff M., Munitz A. Paired immunoglobulin-like receptor-B inhibits pulmonary fibrosis by suppressing profibrogenic properties of alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 2013, 48:456-464.
56. Katz H.R. Inhibition of inflammatory responses by leukocyte Ig-like receptors. Adv. Immunol. 2006, 91:251-272.
57. Kiefer R., Kieseier B.C., Stoll G., Hartung H.P. The role of macrophages in immune-mediated damage to the peripheral nervous system. Prog. Neurobiol. 2001, 64:109-127.
58. Kim J.E., Li S., GrandPre T., Qiu D., Strittmatter S.M. Axon regeneration in young adult mice lacking Nogo-A/B. Neuron 2003, 38:187-199.
59. Kim J.E., Liu B.P., Park J.H., Strittmatter S.M. Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron 2004, 44:439-451.
60. Kondo Y., Jadlowiec C.C., Muto A., Yi T., Protack C., Collins M.J., Tellides G., Sessa W.C., Dardik A. The Nogo-B-PirB axis controls macrophage-mediated vascular remodeling. PLoS One 2013, 8:e81019.
61. Lauren J., Airaksinen M.S., Saarma M., Timmusk T. Two novel mammalian Nogo receptor homologs differentially expressed in the central and peripheral nervous systems. Mol. Cell. Neurosci. 2003, 24:581-594.
62. Lauren J., Hu F., Chin J., Liao J., Airaksinen M.S., Strittmatter S.M. Characterization of myelin ligand complexes with neuronal Nogo-66 receptor family members. J. Biol. Chem. 2007, 282:5715-5725.
63. Lee J.K., Chow R., Xie F., Chow S.Y., Tolentino K.E., Zheng B. Combined genetic attenuation of myelin and semaphorin-mediated growth inhibition is insufficient to promote serotonergic axon regeneration. J. Neurosci. 2010, 30:10899-10904.
64. Lee J.K., Geoffroy C.G., Chan A.F., Tolentino K.E., Crawford M.J., Leal M.A., Kang B., Zheng B. Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron 2010, 66:663-670.
65. Li J., Li J.P., Zhang X., Lu Z., Yu S.P., Wei L. Expression of heparanase in vascular cells and astrocytes of the mouse brain after focal cerebral ischemia. Brain Res. 2012, 1433:137-144.
66. Li M., Shibata A., Li C., Braun P.E., McKerracher L., Roder J., Kater S.B., David S. Myelin-associated glycoprotein inhibits neurite/axon growth and causes growth cone collapse. J. Neurosci. Res. 1996, 46:404-414.
67. Liu B.P., Fournier A., GrandPre T., Strittmatter S.M. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 2002, 297:1190-1193.
68. Locatelli G., Wortge S., Buch T., Ingold B., Frommer F., Sobottka B., Kruger M., Karram K., Buhlmann C., Bechmann I., et al. Primary oligodendrocyte death does not elicit anti-CNS immunity. Nat. Neurosci. 2012, 15:543-550.
69. Maeda N., Ishii M., Nishimura K., Kamimura K. Functions of chondroitin sulfate and heparan sulfate in the developing brain. Neurochem. Res. 2011, 36:1228-1240.
70. Massey J.M., Hubscher C.H., Wagoner M.R., Decker J.A., Amps J., Silver J., Onifer S.M. Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J. Neurosci. 2006, 26:4406-4414.
71. Maurer M.A., Rakocevic G., Leung C.S., Quast I., Lukacisin M., Goebels N., Munz C., Wardemann H., Dalakas M., Lunemann J.D. Rituximab induces sustained reduction of pathogenic B cells in patients with peripheral nervous system autoimmunity. J. Clin. Invest. 2012, 122:1393-1402.
72. McDonald C.L., Steinbach K., Kern F., Schweigreiter R., Martin R., Bandtlow C.E., Reindl M. Nogo receptor is involved in the adhesion of dendritic cells to myelin. J. Neuroinflammation 2011, 8:113.
73. McGee A.W., Yang Y., Fischer Q.S., Daw N.W., Strittmatter S.M. Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 2005, 309:2222-2226.
74. McKeon R.J., Schreiber R.C., Rudge J.S., Silver J. 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. 1991, 11:3398-3411.
75. McKerracher L., David S., Jackson D.L., Kottis V., Dunn R.J., Braun P.E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 1994, 13:805-811.
76. Mi S., Lee X., Shao Z., Thill G., Ji B., Relton J., Levesque M., Allaire N., Perrin S., Sands B., et al. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 2004, 7:221-228.
77. Milev P., Maurel P., Chiba A., Mevissen M., Popp S., Yamaguchi Y., Margolis R.K., Margolis R.U. Differential regulation of expression of hyaluronan-binding proteoglycans in developing brain: aggrecan, versican, neurocan, and brevican. Biochem. Biophys. Res. Commun. 1998, 247:207-212.
78. Monaco S., Ferrari S., Bonetti B., Moretto G., Kirshfink M., Nardelli E., Nobile-Orazio E., Zanusso G., Rizzuto N., Tedesco F. Experimental induction of myelin changes by anti-MAG antibodies and terminal complement complex. J. Neuropathol. Exp. Neurol. 1995, 54:96-104.
79. Mukhopadhyay G., Doherty P., Walsh F.S., Crocker P.R., Filbin M.T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 1994, 13:757-767.
80. Munitz A., Cole E.T., Beichler A., Groschwitz K., Ahrens R., Steinbrecher K., Willson T., Han X., Denson L., Rothenberg M.E., et al. Paired immunoglobulin-like receptor B (PIR-B) negatively regulates macrophage activation in experimental colitis. Gastroenterology 2010, 139:530-541.
81. Nakamura Y., Fujita Y., Ueno M., Takai T., Yamashita T. Paired immunoglobulin-like receptor B knockout does not enhance axonal regeneration or locomotor recovery after spinal cord injury. J. Biol. Chem. 2011, 286:1876-1883.
82. Omoto S., Ueno M., Mochio S., Takai T., Yamashita T. Genetic deletion of paired immunoglobulin-like receptor B does not promote axonal plasticity or functional recovery after traumatic brain injury. J. Neurosci. 2010, 30:13045-13052.
83. Oohira A., Matsui F., Watanabe E., Kushima Y., Maeda N. Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody IG2 in the rat cerebrum. Neuroscience 1994, 60:145-157.
84. Park J.B., Yiu G., Kaneko S., Wang J., Chang J., He X.L., Garcia K.C., He Z. A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 2005, 45:345-351.
85. Pereira S., Zhang H., Takai T., Lowell C.A. The inhibitory receptor PIR-B negatively regulates neutrophil and macrophage integrin signaling. J. Immunol. 2004, 173:5757-5765.
86. Pindzola R.R., Doller C., Silver J. 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. 1993, 156:34-48.
87. Pool M., Niino M., Rambaldi I., Robson K., Bar-Or A., Fournier A.E. Myelin regulates immune cell adhesion and motility. Exp. Neurol. 2009, 217:371-377.
88. Popovich P.G., Guan Z., Wei P., Huitinga I., van Rooijen N., Stokes B.T. Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp. Neurol. 1999, 158:351-365.
89. Prineas J.W., McLeod J.G. Chronic relapsing polyneuritis. J. Neurol. Sci. 1976, 27:427-458.
90. Properzi F., Lin R., Kwok J., Naidu M., van Kuppevelt T.H., Ten Dam G.B., Camargo L.M., Raha-Chowdhury R., Furukawa Y., Mikami T., et al. Heparan sulphate proteoglycans in glia and in the normal and injured CNS: expression of sulphotransferases and changes in sulphation. Eur. J. Neurosci. 2008, 27:593-604.
91. Rolls A., Shechter R., London A., Segev Y., Jacob-Hirsch J., Amariglio N., Rechavi G., Schwartz M. Two faces of chondroitin sulfate proteoglycan in spinal cord repair: a role in microglia/macrophage activation. PLoS Med. 2008, 5:e171.
92. Salzer J.L., Holmes W.P., Colman D.R. The amino acid sequences of the myelin-associated glycoproteins: homology to the immunoglobulin gene superfamily. J. Cell Biol. 1987, 104:957-965.
93. Schwab J.M., Zhang Y., Kopp M.A., Brommer B., Popovich P.G. The paradox of chronic neuroinflammation, systemic immune suppression, autoimmunity after traumatic chronic spinal cord injury. Exp. Neurol. 2014, 258:121-129. (in this issue).
94. Selvan R.S., Ihrcke N.S., Platt J.L. Heparan sulfate in immune responses. Ann. N. Y. Acad. Sci. 1996, 797:127-139.
95. Sergott R.C., Brown M.J., Lisak R.P., Miller S.L. Antibody to myelin-associated glycoprotein produces central nervous system demyelination. Neurology 1988, 38:422-426.
96. Sharma K., Selzer M.E., Li S. Scar-mediated inhibition and CSPG receptors in the CNS. Exp. Neurol. 2012, 237:370-378.
97. Shen Y., Tenney A.P., Busch S.A., Horn K.P., Cuascut F.X., Liu K., He Z., Silver J., Flanagan J.G. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009, 326:592-596.
98. Shen Y.J., DeBellard M.E., Salzer J.L., Roder J., Filbin M.T. Myelin-associated glycoprotein in myelin and expressed by Schwann cells inhibits axonal regeneration and branching. Mol. Cell. Neurosci. 1998, 12:79-91.
99. Sicotte M., Tsatas O., Jeong S.Y., Cai C.Q., He Z., David S. Immunization with myelin or recombinant Nogo-66/MAG in alum promotes axon regeneration and sprouting after corticospinal tract lesions in the spinal cord. Mol. Cell. Neurosci. 2003, 23:251-263.
100. Simonen M., Pedersen V., Weinmann O., Schnell L., Buss A., Ledermann B., Christ F., Sansig G., van der Putten H., Schwab M.E. Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 2003, 38:201-211.
101. Snow D.M., Lemmon V., Carrino D.A., Caplan A.I., Silver J. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol. 1990, 109:111-130.
102. Snow D.M., Watanabe M., Letourneau P.C., Silver J. A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth. Development 1991, 113:1473-1485.
103. Steck A.J., Murray N., Meier C., Page N., Perruisseau G. Demyelinating neuropathy and monoclonal IgM antibody to myelin-associated glycoprotein. Neurology 1983, 33:19-23.
104. Steck A.J., Stalder A.K., Renaud S. Anti-myelin-associated glycoprotein neuropathy. Curr. Opin. Neurol. 2006, 19:458-463.
105. Stipp C.S., Litwack E.D., Lander A.D. Cerebroglycan: an integral membrane heparan sulfate proteoglycan that is unique to the developing nervous system and expressed specifically during neuronal differentiation. J. Cell Biol. 1994, 124:149-160.
106. Syken J., Grandpre T., Kanold P.O., Shatz C.J. PirB restricts ocular-dominance plasticity in visual cortex. Science 2006, 313:1795-1800.
107. Takai T. Paired immunoglobulin-like receptors and their MHC class I recognition. Immunology 2005, 115:433-440.
108. Turnley A.M., Bartlett P.F. MAG and MOG enhance neurite outgrowth of embryonic mouse spinal cord neurons. Neuroreport 1998, 9:1987-1990.
109. Venkatesh K., Chivatakarn O., Lee H., Joshi P.S., Kantor D.B., Newman B.A., Mage R., Rader C., Giger R.J. The Nogo-66 receptor homolog NgR2 is a sialic acid-dependent receptor selective for myelin-associated glycoprotein. J. Neurosci. 2005, 25:808-822.
110. Wang F., Wolfson S.N., Gharib A., Sagasti A. LAR receptor tyrosine phosphatases and HSPGs guide peripheral sensory axons to the skin. Curr. Biol. 2012, 22:373-382.
111. Wang K.C., Kim J.A., Sivasankaran R., Segal R., He Z. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 2002, 420:74-78.
112. Wang K.C., Koprivica V., Kim J.A., Sivasankaran R., Guo Y., Neve R.L., He Z. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002, 417:941-944.
113. Wang X., Duffy P., McGee A.W., Hasan O., Gould G., Tu N., Harel N.Y., Huang Y., Carson R.E., Weinzimmer D., et al. Recovery from chronic spinal cord contusion after Nogo receptor intervention. Ann. Neurol. 2011, 70:805-821.
114. Wilson M.T., Snow D.M. Chondroitin sulfate proteoglycan expression pattern in hippocampal development: potential regulation of axon tract formation. J. Comp. Neurol. 2000, 424:532-546.
115. Yan J., Zhou X., Guo J.J., Mao L., Wang Y.J., Sun J., Sun L.X., Zhang L.Y., Zhou X.F., Liao H. Nogo-66 inhibits adhesion and migration of microglia via GTPase Rho pathway in vitro. J. Neurochem. 2012, 120:721-731.
116. Yiu G., He Z. Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 2006, 7:617-627.
117. Zhang X., Wang B., O'Callaghan P., Hjertstrom E., Jia J., Gong F., Zcharia E., Nilsson L.N., Lannfelt L., Vlodavsky I., et al. Heparanase overexpression impairs inflammatory response and macrophage-mediated clearance of amyloid-beta in murine brain. Acta Neuropathol. 2012, 124:465-478.
118. Zhang Y., Yeung M.N., Liu J., Chau C.H., Chan Y.S., Shum D.K. Mapping heparanase expression in the spinal cord of adult rats. J. Comp. Neurol. 2006, 494:345-357.
119. Zheng B., Atwal J., Ho C., Case L., He X.L., Garcia K.C., Steward O., Tessier-Lavigne M. 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. 2005, 102:1205-1210.
120. Zheng B., Ho C., Li S., Keirstead H., Steward O., Tessier-Lavigne M. Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 2003, 38:213-224.