Anti-Thy-1 antibody-induced neurite outgrowth in cultured dorsal root ganglionic neurons is mediated by the c-Src-MEK signaling pathway

Journal of Cellular Biochemistry

Volumn 103, Issue 1, 2008, Pages 67-77

  Yang, Shih Hung ^a,b   Chen, Yi Jen ^a   Tung, Po Yuan ^a   Lai, Wei Ling ^a   Chen, Ying ^a   Jeng, Chung Jiuan ^c   Wang, Seu Mei ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Anti Thy 1 antibody; C Src kinase; CREB; DRG neuron; MEK; Neurite outgrowth

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; DIMETHYL SULFOXIDE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN ANTIBODY; THY 1 ANTIBODY; THY 1 ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; MALE; NERVE FIBER GROWTH; NEUROTROPISM; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; RAT; SIGNAL TRANSDUCTION; SPINAL GANGLION; UPREGULATION;

ANIMALS; ANTIBODIES; ANTIGENS, THY-1; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENZYME ACTIVATION; FEMALE; GANGLIA, SPINAL; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEURITES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RATS; RATS, WISTAR;

EID: 38149004162     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21387     Document Type: Article

References (52)

1. Akhand AA, Kato M, Suzuki H, Liu W, Du J, Hamaguchi M, Miyata T, Kurokawa K, Nakashima I. 1999. Carbonyl compounds cross-link cellular proteins and activate protein-tyrosine kinase p60c-Src. J Cell Biochem 72:1-7.
2. Avalos AM, Labra CV, Questa AFG, Leyton L. 2002. Signaling triggered by Thy-1 interaction with beta(3) integrin on astrocytes is an essential step towards unraveling neuronal Thy-1 function. Biological Research 35:231-238.
3. Avalos AM, Arthur WT, Schneider P, Quest AFG, Burridge K, Leyton L. 2004. Aggregation of integrins and RhoA activation are required for Thy-1-induced morphological changes in astrocytes. Journal of Biological Chemistry 279:39139-39145.
4. Barlow JZ, Huntley GW. 2000. Developmentally regulated expression of Thy-1 in structures of the mouse sensory-motor system. Journal of Comparative Neurology 421:215-233.
5. Barlow JZ, Kelley KA, Bozdagi O, Huntley GW. 2002. Testing the role of the cell-surface molecule Thy-1 in regeneration and plasticity of connectivity in the CNS. Neuroscience 111:837-852.
6. Beech JN, Morris RJ, Raisman G. 1983. Density of Thy-1 on axonal membrane of different rat nerves. J Neurochem 41:411-417.
7. Chen CH, Wang SM, Yang SH, Jeng CJ. 2005. Role of Thy-1 in in vivo and in vitro neural development and regeneration of dorsal root ganglionic neurons. J Cell Biochem 94:684-694.
8. Chen CH, Chen YJ, Jeng CJ, Yang SH, Tung PY, Wang SM. 2007. Role of PKA in the anti-Thy-1 Antibody-induced Neurite Outgrowth of Dorsal Root Ganglionic Neurons. J Cell Biochem online published in December 2006.
9. Deininger SO, Rajendran L, Lottspeich F, Przybylski M, Illges H, Stuermer CAO, Reuter A. 2003. Identification of teleost Thy-1 and association with the microdomain/lipid raft reggie proteins in regenerating CNS axons. Molecular and Cellular Neuroscience 22:544-554.
10. Doherty P, Singh A, Rimon G, Bolsover SR, Walsh FS. 1993. Thy-1 Antibody-Triggered Neurite Outgrowth Requires an Influx of Calcium into Neurons Via N-Type and L-Type Calcium Channels. Journal of Cell Biology 122:181-189.
11. Draberova L, Draber P. 1993. Thy-1 glycoprotein and src-like protein-tyrosine kinase p53/p56lyn are associated in large detergent-resistant complexes in rat basophilic leukemia cells. Proc Natl Acad Sci U S A 90:3611-3615.
12. Draberova L, Amoui M, Draber P. 1996. Thy-1-mediated activation of rat mast cells: the role of Thy-1 membrane microdomains. Immunology 87:141-148.
13. Durbec P, Gennarini G, Goridis C, Rougon G. 1992. A soluble form of the F3 neuronal cell adhesion molecule promotes neurite outgrowth. J Cell Biol 117:877-887.
14. Durrheim GA, Garnett D, Dennehy KM, Beyers AD. 2001. Thy-1 associated PP 85-90 is a potential docking site for SH2 domain-containing signal transduction molecules. Cell Biol Int 25:33-42.
15. Fukuda M, Gotoh Y, Tachibana T, Dell K, Hattori S, Yoneda Y, Nishida E. 1995. Induction of neurite outgrowth by MAP kinase in PC12 cells. Oncogene 11:239-244.
16. Henke RC, Seeto GS, Jeffrey PL. 1997. Thy-1 and AvGp50 signal transduction complex in the avian nervous system: c-Fyn and G alpha i protein association and activation of signalling pathways. Journal of Neuroscience Research 49:655-670.
17. Impey S, Obrietan K, Wong ST, Poser S, Yano S, Wayman G, Deloulme JC, Chan G, Storm DR. 1998. Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
18. Jeng CJ, McCarroll SA, Martin TF, Floor E, Adams J, Krantz D, Butz S, Edwards R, Schweitzer ES. 1998. Thy1 is a component common to multiple populations of synaptic vesicles. J Cell Biol 140:685-698.
19. Johansson JU, Lilja L, Chen XL, Higashida H, Meister B, Noda M, Zhong ZG, Yokoyama S, Berggren PO, Bark C. 2005. Cyclin-dependent kinase 5 activators p35 and p39 facilitate formation of functional synapses. Brain Res Mol Brain Res 138:215-227.
20. Kawauchi T, Chihama K, Nabeshima Y, Hoshino M. 2006. Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat Cell Biol 8:17-26.
21. Kesavapany S, Li BS, Pant HC. 2003. Cyclin-dependent kinase 5 in neurofilament function and regulation. Neurosignals 12:252-264.
22. Kim B, Leventhal PS, Saltiel AR, Feldman EL. 1997. Insulin-like Growth Factor-I-mediated Neurite Outgrowth in Vitro Requires Mitogen-activated Protein Kinase Activation. J Biol Chem 272:21268-21273.
23. Lang DM, Lommel S, Jung M, Ankerhold R, Petrausch B, Laessing U, Wiechers MF, Plattner H, Stuermer CAO. 1998. Identification of reggie-1 and reggie-2 as plasma membrane-associated proteins which cocluster with activated GPI-anchored cell adhesion molecules in non-caveolar micropatches in neurons. Journal of Neurobiology 37:502-523.
24. Leifer D, Lipton SA, Barnstable CJ, Masland RH. 1984. Monoclonal antibody to Thy-1 enhances regeneration of processes by rat retinal ganglion cells in culture. Science 224:303-306.
25. Leifer D, Dreyer EB, Lipton SA. 1991. Immunofluorescent characterization of retinal ganglion cell neurites cultured on substrates coated with antibodies against Thy-1. Exp Neurol 113:386-390.
26. Leyton L, Schneider P, Labra CV, Ruegg C, Hetz CA, Quest AFG, Bron C. 2001. Thy-1 binds to integrin beta(3) on astrocytes and triggers formation of focal contact sites. Current Biology 11:1028-1038.
27. Lipton SA, Leifer D, Barnstable CJ. 1992. Selectivity of Thy-1 Monoclonal-Antibodies in Enhancing Neurite Outgrowth. Neuroscience Letters 137:75-77.
28. Lonze BE, Ginty DD. 2002. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605-623.
29. Lucero HA, Robbins PW. 2004. Lipid rafts-protein association and the regulation of protein activity. Archives of Biochemistry and Biophysics 426:208-224.
30. Mahanthappa NK, Patterson PH. 1992. Thy-1 Involvement in Neurite Outgrowth - Perturbation by Antibodies, Phospholipase-C, and Mutation. Developmental Biology 150:47-59.
31. Mayeux-Portas V, File SE, Stewart CL, Morris RJ. 2000. Mice lacking the cell adhesion molecule Thy-1 fail to use socially transmitted cues to direct their choice of food. Current Biology 10:68-75.
32. Morris R. 1985. Thy-1 in developing nervous tissue. Developmental Neuroscience 7:133-160.
33. Morris R. 1992. Thy-1, the enigmatic extrovert on the neuronal surface. Bioessays 14:715-722.
34. Morris R, Grosveld F. 1989. Expression of Thy-1 in the nervous system of the rat and mouse. Immunology Series 45:121-148.
35. Narisawa-Saito M, Yamanashi Y, Morioka T, Oite T, Shimizu F. 1996. Thy-1 molecule associates with protein tyrosine kinase(s) in rat mesangial cells. Clin Exp Immunol 106:86-90.
36. NostenBertrand M, Errington ML, Murphy K, Tokugawa Y, Barboni E, Kozlova E, Michalovich D, Morris RGM, Silver J, Stewart CL, Bliss TVP, Morris RJ. 1996. Normal spatial learning despite regional inhibition of LTP in mice lacking Thy-1. Nature 379:826-829.
37. Obata K, Yamanaka H, Dai Y, Mizushima T, Fukuoka T, Tokunaga A, Noguchi K. 2004. Differential activation of MAPK in injured and uninjured DRG neurons following chronic constriction injury of the sciatic nerve in rats. Eur J Neurosci 20:2881-2895.
38. Olsson A-K, Nanberg E. 2001. A Functional Role for ERK in Gene Induction, but Not in Neurite Outgrowth in Differentiating Neuroblastoma Cells. Experimental Cell Research 265:21-30.
39. Pesheva P, Gennarini G, Goridis C, Schachner M. 1993. The F3/11 cell adhesion molecule mediates the repulsion of neurons by the extracellular matrix glycoprotein J1-160/180. Neuron 10:69-82.
40. Rajendran L, Simons K. 2005. Lipid rafts and membrane dynamics. J Cell Sci 118:1099-1102.
41. Robinson MJ, Stippec SA, Goldsmith E, White MA, Cobb MH. 1998. A constitutively active and nuclear form of the MAP kinase ERK2 is sufficient for neurite outgrowth and cell transformation. Curr Biol 8:1141-1150.
42. Shenoyscaria AM, Gauen LKT, Kwong J, Shaw AS, Lublin DM. 1993. Palmitylation of an Amino-Terminal Cysteine Motif of Protein-Tyrosine Kinases P56lck and P59fyn Mediates Interaction with Glycosyl-Phosphatidylinositol- Anchored Proteins. Molecular and Cellular Biology 13:6385-6392.
43. Simon PD, McConnell J, Zurakowski D, Vorwerk CK, Naskar R, Grosskreutz CL, Dreyer EB. 1999. Thy-1 is critical for normal retinal development. Developmental Brain Research 117:219-223.
44. Song JH, Wang CX, Song DK, Wang P, Shuaib A, Hao C. 2005. Interferon gamma induces neurite outgrowth by up-regulation of p35 neuron-specific cyclin-dependent kinase 5 activator via activation of ERK1/2 pathway. J Biol Chem 280:12896-12901.
45. Stefanova I, Horejsi V, Ansotegui IJ, Knapp W, Stockinger H. 1991. GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science 254:1016-1019.
46. Stuermer CAO, Plattner H. 2005. The 'lipid raft' microdomain proteins reggie-1 and reggie-2 (flotillins) are scaffolds for protein interaction and signalling. In: Lipids, Rafts and Traffic p 109-118.
47. Stuermer CA, Lang DM, Kirsch F, Wiechers M, Deininger SO, Plattner H. 2001. Glycosylphosphatidyl inositol-anchored proteins and fyn kinase assemble in noncaveolar plasma membrane microdomains defined by reggie-1 and -2. Mol Biol Cell 12:3031-3045.
48. Thomas PM, Samelson LE. 1992. The glycophosphatidylinositol-anchored Thy-1 molecule interacts with the p60fyn protein tyrosine kinase in T cells. J Biol Chem 267:12317-12322.
49. Tiveron MC, Barboni E, Rivero FBP, Gormley AM, Seeley PJ, Grosveld F, Morris R. 1992. Selective-Inhibition of Neurite Outgrowth on Mature Astrocytes by Thy-1 Glycoprotein. Nature 355:745-748.
50. Tiveron MC, Nosten-Bertrand M, Jani H, Garnett D, Hirst EM, Grosveld F, Morris RJ. 1994. The mode of anchorage to the cell surface determines both the function and the membrane location of Thy-1 glycoprotein. Journal of Cell Science 107:1783-1796.
51. Tojima T, Kobayashi S, Ito E. 2003. Dual role of cyclic AMP-dependent protein kinase in neuritogenesis and synaptogenesis during neuronal differentiation. J Neurosci Res 74:829-837.
52. Xue GP, Rivero BP, Morris RJ. 1991. The surface glycoprotein Thy-1 is excluded from growing axons during development: a study of the expression of Thy-1 during axogenesis in hippocampus and hindbrain. Development 112:161-176.