CD82 blocks cMet activation and overcomes hepatocyte growth factor effects on oligodendrocyte precursor differentiation

Journal of Neuroscience

Volumn 33, Issue 18, 2013, Pages 7952-7960

  Mela, Angeliki ^a   Goldman, James E ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD82 ANTIGEN; MYELIN; PROTEIN CDC42; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SCATTER FACTOR RECEPTOR; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRECURSOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; WHITE MATTER;

ADULT; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD82; BRAIN; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HEPATOCYTE GROWTH FACTOR; HUMANS; OLIGODENDROGLIA; PROTO-ONCOGENE PROTEINS C-MET; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; STEM CELLS;

EID: 84877115771     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5836-12.2013     Document Type: Article

References (50)

1. Achim CL, Katyal S, Wiley CA, Shiratori M, Wang G, Oshika E, Petersen BE, Li JM, Michalopoulos GK (1997) Expression of HGF and c Met in the developing and adult brain. Brain Res Dev Brain Res 102:299-303. CrossRef Medline
2. Assanah M, Lochhead R, Ogden A, Bruce J, Goldman J, Canoll P (2006) Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. J Neurosci 26:6781-6790. CrossRef Medline
3. Assanah MC, Bruce JN, Suzuki SO, Chen A, Goldman JE, Canoll P (2009) PDGF stimulates the massive expansion of glial progenitors in the neonatal forebrain. Glia 57:1835-1847. CrossRef Medline
4. Bai L, Lennon DP, Caplan AI, De Chant A, Hecker J, Kranso J, Zaremba A, Miller RH. (2012) Hepatocyte growth factor mediates mesenchymal stem cell-induced recovery in multiple sclerosis models. Nat Neurosci 15:862-870. CrossRef Medline
5. Baron W, Decker L, Colognato H, ffrench-Constant C (2003) Regulation of integrin growth factor interactions in oligodendrocytes by lipid raft microdomains. Curr Biol 13:151-155. CrossRef Medline
6. Barros CS, Nguyen T, Spencer KS, Nishiyama A, Colognato H, Müller U (2009) Beta1 integrins are required for normal CNS myelination and promote AKT-dependent myelin outgrowth. Development 136:2717-2724. CrossRef Medline
7. Decker L, ffrench-Constant C (2004) Lipid rafts and integrin activation regulate oligodendrocyte survival. J Neurosci 24:3816-3825. CrossRef Medline
8. Decker L, Baron W, ffrench-Constant C (2004) Lipid rafts: microenvironments for integrin-growth factor interactions in neural development. Biochem Soc Trans 32:426-430. CrossRef Medline
9. Delaguillaumie A, Harriague J, Kohanna S, Bismuth G, Rubinstein E, Seigneuret M, Conjeaud H (2004) Tetraspanin CD82 controls the association of cholesterol-dependent microdomains with the actin cytoskeleton in T lymphocytes: relevance to co-stimulation. J Cell Sci 117:5269-5282. CrossRef Medline
10. Dong JT, Lamb PW, Rinker-Schaeffer CW, Vukanovic J, Ichikawa T, Isaacs JT, Barrett JC (1995) KAI1, a metastasis suppressor gene for prostate cancer on human chromosome 11p11.2. Science 268:884-886. CrossRef Medline
11. Feltri ML, Suter U, Relvas JB (2008) The function of Rho GTPases in axon ensheathment and myelination. Glia 56:1508-1517. CrossRef Medline
12. Honda S, Kagoshima M, Wanaka A, Tohyama M, Matsumoto K, Nakamura T (1995) Localization and functional coupling of HGF and c-Met/HGF receptor in rat brain: implication as neurotrophic factor. Brain Res Mol Brain Res 32:197-210. CrossRef Medline
13. Jackson P, Marreiros A, Russell PJ (2005) KAI1 tetraspanin and metastasis suppressor. Int J Biochem Cell Biol 37:530-534. CrossRef Medline
14. Judson MC, Bergman MY, Campbell DB, Eagleson KL, Levitt P (2009) Dynamic gene and protein expression patterns of the autism-associated met receptor tyrosine kinase in the developing mouse forebrain. J Comp Neurol 513:511-531. CrossRef Medline
15. Jung W, Castren E, Odenthal M, Vande Woude GF, Ishii T, Dienes HP, Lindholm D, Schirmacher P (1994) Expression and functional interaction of hepatocyte growth factor-scatter factor and its receptor c-met in mammalian brain. J Cell Biol 126:485-494. CrossRef Medline
16. Kippert A, Trajkovic K, Rajendran L, Ries J, Simons M (2007) Rho regulates membrane transport in the endocytic pathway to control plasma membrane specialization in oligodendroglial cells. J Neurosci 27:3560-3570. CrossRef Medline
17. Kitamura K, Iwanami A, Nakamura M, Yamane J, Watanabe K, Suzuki Y, Miyazawa D, Shibata S, Funakoshi H, Miyatake S, Coffin RS, Nakamura T, Toyama Y, Okano H (2007) Hepatocyte growth factor promotes endogenous repair and functional recovery after spinal cord injury. J Neurosci Res 85:2332-2342. CrossRef Medline
18. Lagaudrière-Gesbert C, Lebel-Binay S, Hubeau C, Fradelizi D, Conjeaud H (1998) Signaling through the tetraspanin CD82 triggers its association with the cytoskeleton leading to sustained morphological changes and T cell activation. Eur J Immunol 28:4332-4344. CrossRef Medline
19. Lalive PH, Paglinawan R, Biollaz G, Kappos EA, Leone DP, Malipiero U, Relvas JB, Moransard M, Suter T, Fontana A (2005) TGF-beta-treated microglia induce oligodendrocyte precursor cell chemotaxis through the HGF-c-Met pathway. Eur J Immunol 35:727-737. CrossRef Medline
20. Laursen LS, Chan CW, ffrench-Constant C (2011) Translation of myelin basic protein m RNA in oligodendrocytes is regulated by integrin activation and hn RNP-K. J Cell Biol 192:797-811. CrossRef Medline
21. Liang X, Draghi NA, Resh MD (2004) Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J Neurosci 24:7140-7149. CrossRef Medline
22. Lin G, Mela A, Guilfoyle EM, Goldman JE (2009) Neonatal and adult O4(+) oligodendrocyte lineage cells display different growth factor responses and different gene expression patterns. J Neurosci Res 87:3390-3402. CrossRef Medline
23. Liu WM, Zhang XA (2006) KAI1/CD82, a tumor metastasis suppressor. Cancer lett 240:183-194. CrossRef Medline
24. Mannion BA, Berditchevski F, Kraeft SK, Chen LB, Hemler ME (1996) Transmembrane-4 superfamily proteins CD81 (TAPA-1), CD82, CD63, and CD53 specifically associated with integrin alpha 4 beta 1 (CD49d/ CD29). J Immunol 157:2039-2047. Medline
25. Mason JL, Goldman JE (2002) A2B5+and O4+Cycling progenitors in the adult forebrain white matter respond differentially to PDGF-AA, FGF-2, and IGF-1. Mol Cell Neurosci 20:30-42. CrossRef Medline
26. Mason JL, Toews A, Hostettler JD, Morell P, Suzuki K, Goldman JE, Matsushima GK (2004) Oligodendrocytes and progenitors become progressively depleted within chronically demyelinated lesions. Am J Pathol 164: 1673-1682. CrossRef Medline
27. Mela A, Goldman JE (2009) The tetraspanin KAI1/CD82 is expressed by late-lineage oligodendrocyte precursors and may function to restrict precursor migration and promote oligodendrocyte differentiation and myelination. J Neurosci 29:11172-11181. CrossRef Medline
28. Mi S, Miller RH, Lee X, Scott ML, Shulag-Morskaya S, Shao Z, Chang J, Thill G, Levesque M, Zhang M, Hession C, Sah D, Trapp B, He Z, Jung V, McCoy JM, Pepinsky RB (2005) LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 8:745-751. CrossRef Medline
29. Miranti CK (2009) Controlling cell surface dynamics and signaling: how CD82/KAI1 suppresses metastasis. Cell Signal 21:196-211. CrossRef Medline
30. Moransard M, Sawitzky M, Fontana A, Suter T (2010) Expression of the HGF receptor c-met by macrophages in experimental autoimmune encephalomyelitis. Glia 58:559-571. CrossRef Medline
31. Müller AM, Jun E, Conlon H, Sadiq SA (2012) Cerebrospinal hepatocyte growth factor levels correlate negatively with disease activity in multiple sclerosis. J Neuroimmunol 251:80-86. CrossRef Medline
32. Noble M, Murray K, Stroobant P, Waterfield MD, Riddle P (1988) Plateletderived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 333:560-562. CrossRef Medline
33. Odintsova E, Voortman J, Gilbert E, Berditchevski F (2003) Tetraspanin CD82 regulates compartmentalisation and ligand-induced dimerization of EGFR. J Cell Sci 116:4557-4566. CrossRef Medline
34. Ohya W, Funakoshi H, Kurosawa T, Nakamura T (2007) Hepatocyte growth factor (HGF) promotes oligodendrocyte progenitor cell proliferation and inhibits its differentiation during postnatal development in the rat. Brain Res 1147:51-65. CrossRef Medline
35. Ono M, Handa K, Withers DA, Hakomori S (1999) Motility inhibition and apoptosis are induced by metastasis-suppressing gene product CD82 and its analogue CD9, with concurrent glycosylation. Cancer Res 59:2335-2339. Medline
36. Pedraza L, Owens GC, Green LA, Salzer JL (1990) The myelin-associated glycoproteins: membrane disposition, evidence of a novel disulfide linkage between immunoglobulin-like domains, and posttranslational palmitylation. J Cell Biol 111:2651-2661. CrossRef Medline
37. Schmidt C, Bladt F, Goedecke S, Brinkmann V, Zschiesche W, Sharpe M, Gherardi E, Birchmeier C (1995) Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373:699-702. CrossRef Medline
38. Shibagaki N, Hanada K, Yamaguchi S, Yamashita H, Shimada S, Hamada H (1998) Functional analysis of CD82 in the early phase of T cell activation: roles in cell adhesion and signal transduction. Eur J Immunol 28:1125-1133. CrossRef Medline
39. Shibagaki N, Hanada KI, Yamashita H, Shimada S, Hamada H (1999) Overexpression of CD82 on human T cells enhances LFA-1/ICAM-1-mediated cell-cell adhesion: functional association between CD82 and LFA-1 in T cell activation. Eur J Immunol 29:4081-4091. CrossRef Medline
40. Symons M, Settleman J (2000) Rho family GTPases: more than simple switches. Trends Cell Biol 10:415-419. CrossRef Medline
41. Takahashi M, Sugiura T, Abe M, Ishii K, Shirasuna K (2007) Regulation of c-Met signaling by the tetraspanin KAI-1/CD82 affects cancer cell migration. Int J Cancer 121:1919-1929. CrossRef Medline
42. Terada N, Kidd GJ, Kinter M, Bjartmar C, Moran-Jones K, Trapp BD (2005) Beta IV tubulin is selectively expressed by oligodendrocytes in the central nervous system. Glia 50:212-222. CrossRef Medline
43. Thurnherr T, Benninger Y, Wu X, Chrostek A, Krause SM, Nave KA, Franklin RJ, Brakebusch C, Suter U, Relvas JB (2006) Cdc42 and Rac1 signaling are both required for and act synergistically in the correct formation of myelin sheaths in the CNS. J Neurosci 26:10110-10119. CrossRef Medline
44. Todeschini AR, Dos Santos JN, Handa K, Hakomori SI (2007) Ganglioside GM2-tetraspanin CD82 complex inhibits met and its cross-talk with integrins, providing a basis for control of cell motility through glycosynapse. J Biol Chem 282:8123-8133. CrossRef Medline
45. Tsuboi Y, Kakimoto K, Akatsu H, Daikuhara Y, Yamada T (2002) Hepatocyte growth factor in cerebrospinal fluid in neurologic disease. Acta Neurol Scand 106:99-103. CrossRef Medline
46. Uehara Y, Minowa O, Mori C, Shiota K, Kuno J, Noda T, Kitamura N (1995) Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373:702-705. CrossRef Medline van
47. van Heyningen P, Calver AR, Richardson WD (2001) Control of progenitor cell number by mitogen supply and demand. Curr Biol 11:232-241. CrossRef Medline
48. Wang L, Zheng Y (2007) Cell type-specific functions of Rho GTPases revealed by gene targeting in mice. Trends Cell Biol 17:58-64. CrossRef Medline
49. Yan H, Rivkees SA (2002) Hepatocyte growth factor stimulates the proliferation and migration of oligodendrocyte precursor cells. J Neurosci Res 69:597-606. CrossRef Medline
50. Yang X, Wei LL, Tang C, Slack R, Mueller S, Lippman ME (2001) Overexpression of KAI1 suppresses in vitro invasiveness and in vivo metastasis in breast cancer cells. Cancer Res 61:5284-5288. Medline