NCAM stimulates the Ras-MAPK pathway and CREB phosphorylation in neuronal cells

Journal of Neurobiology

Volumn 38, Issue 4, 1999, Pages 542-558

  Schmid, Ralf Steffen ^a   Graft, Ronald D ^a   Schaller, Michael D ^a   Chen, Suzhen ^b   Schachner, Melitta ^c   Hemperly, John J ^d   Maness, Patricia F ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b Institute of Neuroinformatics Zurich   (Switzerland)

^c UNIVERSITY OF HAMBURG   (Germany)

^d BD Technologies   (United States)

Author keywords

CREB; MAP kinase; Neural cell adhesion molecules; Neurite outgrowth; Synaptic plasticity

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NERVE CELL ADHESION MOLECULE; RAS PROTEIN; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE EXPRESSION REGULATION; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; JNK MITOGEN-ACTIVATED PROTEIN KINASES; L CELLS (CELL LINE); MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; NEURAL CELL ADHESION MOLECULES; NEURITES; NEUROBLASTOMA; NEURONS; PHOSPHORYLATION; RAS PROTEINS; RATS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0033029727     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199903)38:4<542::AID-NEU9>3.0.CO;2-1     Document Type: Article

References (74)

1. Arami S, Jucker M, Schachner M, Welzl H. 1996. The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behav Brain Res 81:81-87.
2. Atashi JR, Klinz SG, Ingraham CA, Matten WT, Schachner M, Maness PF. 1992. Neural cell adhesion molecules modulate tyrosine phosphorylation of tubulin in nerve growth cone membranes. Neuron 8:1-20.
3. Bartsch D, Ghirardi M, Skehel PA, Karl KA, Herder SP, Chen M, Bailey CH, Kandel ER. 1995. Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 83:979-992.
4. Bebbington CR. 1991. Expression of antibody genes in non-lymphoid mammalian cells. Methods (Orlando) 2:136-145.
5. fyn. J Biol Chem 272:8310-8319.
6. Beggs HE, Soriano P, Maness PF. 1994. NCAM-dependent neurite outgrowth is inhibited in neurons from fyn-minus mice. J Cell Biol 127:825-833.
7. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. 1994. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59-68.
8. Braun U, Habermann B, Just I, Aktories K, Vandekerckhove J. 1989. Purification of the 22 kDa protein substrate of botulinum ADP-ribosyltransferase C3 from porcine brain cytosol and its characterization as a GTP-binding protein highly homologous to the rho gene product. FEBS Lett 243:70-76.
9. Burridge K, Chrzanowska-Wodnicka M. 1996. Focal adhesions, contractility, and signaling. Ann Rev Cell Dev Biol 12:463-518.
10. Chen H-C, Appeddu PA, Isoda H, Guan J-L. 1996. Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase. J Biol Chem 271:26329-26334.
11. Chen Q, Kinch MS, Lin TH, Burridge K, Juliano RL. 1994. Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J Biol Chem 269:26602-26605.
12. Chrzanowska-Wodnicka M, Burridge K. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 133:1403-1415.
13. Cleghon V, Morrison DK. 1994. Raf-1 interacts with Fyn and Src in a non-phosphotyrosine-dependent manner. J Biol Chem 269:17749-17755.
14. Covault J, Sanes JR. 1985. Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles. Proc Natl Acad Sci USA 82:4544-4548.
15. Cremer H, Chazal G, Goridis C, Represa A. 1997. NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 8:323-335.
16. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Barthels D, Rajewsky K, Wille W. 1994. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
17. Crews CM, Alessandrini A, Erikson RL. 1992. The primary structure of MEK, a protein kinase that phosphorylates the ERK gene product. Science 258:478-480.
18. Cunningham BA, Hemperly JJ, Murray BA, Prediger EA, Brackenbury R, Edelman GA. 1987. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236:799-806.
19. Deng T, Karin M. 1994. c-Fos transcriptional activity stimulated by H-Ras-activated protein kinase distinct from JNK and ERK. Nature 371:171-175.
20. English JD, Sweatt JD. 1997. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106.
21. Fuller SJ, Davies EL, Gillespie-Brown JHS, Tonks NK. 1997. Mitogen-activated protein kinase phosphatase 1 inhibits the stimulation of gene expression by hypertrophic agonists in cardiac myocytes. Biochem J 323:313-319.
22. Galcheva-Gargova Z, Derijard B, Wu IH, Davis RJ. 1994. An osmosensing signal transduction pathway in mammalian cells. Science 265:806-808.
23. Gilmore AP, Burridge K. 1996. Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate. Nature 381:532-535.
24. Hotchin NA, Hall A. 1996. Regulation of the actin cytoskeleton, integrins and cell growth by the Rho family of small GTPases. Cancer Surv 27:311-322.
25. Ihara S, Nakajima K, Fukada T, Hibi M, Ngata S, Hirano T, Fukui Y. 1997. Dual control of neunte outgrowth by STAT3 and MAP kinase in PC12 cells stimulated by interleukin-6. EMBO J 16:5345-5352.
26. Impey S, Mark M, Villacres EC, Poser S, Chavkin C, Storm DR. 1996. Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16:973-982.
27. Khosravi-Far R, Campbell S, Rossman KL, Der CJ. 1998. Increasing complexity of Ras signal transduction: involvement of Rho family proteins. Adv Cancer Res 72:57-107.
28. Klinz SG, Schachner M, Maness PF. 1995. L1 and NCAM antibodies trigger protein phosphatase activity in growth cone-enriched membranes. J Neurochem 65:84-95.
29. Klippel A, Reinhard C, Kavanaugh WM, Apell G, Escobedo MA, Williams LT. 1996. Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol Cell Biol 16:4117-4127.
30. Kogan JH, Frankland PW, Blendy JA, Coblentz J, Marowitz Z, Schutz G, Silva AJ. 1997. Spaced training induces normal long-term memory in CREB mutant mice. Curr Biol 7:1-11.
31. Kranenburg O, Verlaan I, Hordijk PL, Moolenaar WH. 1997. Gi-mediated activation of the Ras/MAP kinase pathway involves a 100 kDa tyrosine-phosphorylated Grb2 SH3 binding protein, but not Src nor Shc. EMBO J 16:3097-3105.
32. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, Ahmad MF, Avruch J, Woodgett JR. 1994. The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369:156-160.
33. + +-induced regulation of ion channel and MAP kinase functions. Nature 376:737-745.
34. Li N, Batzer A, Daly R, Yajnik V, Skolnik E, Chardin P, Bar-Sagi D, Margolis B, Schlessinger J. 1993. Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 363:85-88.
35. Lin RH, Aplin AE, Shen Y, Chen Q, Schaller M, Romer L, Aukhil I, Juliano RL. 1997. Integrin-mediated activation of MAP kinase is independent of FAK: evidence for dual integrin signaling pathways in fibroblasts. J Cell Biol 136:1385-1395.
36. Liu L, Haines S, Shew R, Akeson RA. 1993. Axon growth is enhanced by NCAM lacking the VASE exon when expressed in either the growth substrate of the growing axon. J Neurosci Res 35:327-345.
37. Lüthi A, Laurent JP, Figurov A, Muller D, MS. 1994. Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372:777-779.
38. Madhani HD, Styles CA, Fink GR. 1997. MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation.Cell 91:673-684.
39. Marais R, Marshall CJ. 1996. Control of the ERK MAP kinase cascade by Ras and Raf. Cancer Surv 27:101-125.
40. c-src modulate axonal guidance in the developing mouse olfactory pathway. J Neurobiol 36:53-63.
41. Murray BA, Hemperly JJ, Pridiger EA, Edelman GM, Cunningham BA. 1986. Alternatively spliced mRNAs code for different polypeptide chains of the chicken neural cell adhesion molecule (N-CAM). J Cell Biol 102:189-193.
42. Payne DM, Rossomando AJ, Martine P, Erickson AK, Her JH, Shabanowitz J, Hunt DF, Weber MJ, Sturgill TW. 1991. Identification of the regulatory phosphorylation sites in pp42/mitogen-activated protein kinase (MAP kinase). EMBO J 10:885-892.
43. Pende M, Fisher TL, Simpson PB, Russell JT, Blenis J, Gallo V. 1997. Neurotransmitter- and growth factor-induced cAMP response element binding protein phosphorylation in glial cell progenitors: role of calcium ions, protein kinase C, and mitogen-activated protein kinase/ ribosomal S6 kinase pathway. J Neurosci 17:1291-1301.
44. Persohn E, Pollerberg GW, Schachner M. 1989. Immunoelectron-microscopic localization of the 180kDa component of the neural cell adhesion molecule N-CAM in postsynaptic membranes. J Comp Neurol 288:92-100.
45. Pollerberg GE, Schachner M, Davoust J. 1986. Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule. Nature 324:462-465.
46. Quilliam LA, Kato K, Rabun KM, Hisaka MM, Huff SY, Campbell-Burk S, Der CJ. 1994. Identification of residues critical for Ras(17N) growth-inhibitory phenotype and for Ras interaction with guanine nucleotide exchange factors. Mol Cell Biol 14:1113-1121.
47. Riccio A, Pierchala BA, Ciarallom CL, Ginty DD. 1997. An NGF-TrkA-mediated retrograde signal to transcription factor CREB in sympathetic neurons. Science 277:1097-1100.
48. Richardson A, Parsons T. 1996. A mechanism for regulation of the adhesion-associated protein tyrosine kinase ppl25FAK. Nature 380:538-540.
49. Saffell JL, Doherty P, Tiveron MC, Morris RJ, Walsh FS. 1995. NCAM requires a cytoplasmic domain to function as a neurite outgrowth-promoting neuronal receptor. Mol Cell Neurosci 6:521-531.
50. Saffell JL, Williams EJ, Mason IJ, Walsh FS, Doherty P. 1997. Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs. Neuron 18:231-242.
51. Schaller MD, Borgman CA, Parsons JT. 1993. Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK. Mol Cell Biol 13:785-791.
52. src. Mol Cell Biol 14:1680-1688.
53. Schaller MD, Parsons JT. 1993. Focal adhesion kinase: an integrin-linked protein tyrosine kinase. Trends Cell Biol 3:258-262.
54. Schlaepfer DD, Broome MA, Hunter T. 1997. Fibronectin-stimulated signaling from a focal adhesion kinase-c-Src complex: Involvement of the Grb2, p130cas and Nek adaptor proteins. Mol Cell Biol 17:1702-1713.
55. Schlaepfer DD, Hanks SK, Hunter T, van der Geer P. 1994. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 372:786-791.
56. Schnitzer, J. and Schachner, M. (1981). Characterization of isolated mouse cerebellar cell populations in vitro. J. Neuroimmunol. 1:457-470.
57. Scholey AB, Rose SP, Zamani MR, Bock E, Schachner M. 1993. A role for the neural cell adhesion molecule in a late, consolidating phase of glycoprotein synthesis six hours following passive avoidance training of the young chick. Neuroscience 55:499-509.
58. Schreyer DJ, Skene JHP. 1991. Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: delayed accumulation and correlation with regenerative potential. J Neurosci 11:378-3751.
59. Schubert D, Heinemann S, Carlisle W, Tarikas H, Kimes B, Patrick J, Steinback JH, Gulp W, Brandt BL. 1974. Clonal cell lines from the rat central nervous system. Nature 249:224-227.
60. Schuch U, Lohse MJ, Schachner M. 1989. Neural cell adhesion molecules influence second messenger systems. Neuron 3:13-20.
61. Schuster CM, Davis GW, Fetter RD, Goodman CS. 1996a. Genetic dissection of structural and functional components of synaptic plasticity I. Fasciclin II controls synaptic stabilization and growth. Neuron 17:641-654.
62. Schuster CM, Davis GW, Fetter RD, Goodman CS. 1996b. Genetic dissection of structural and functional components of synaptic plasticity II. Fasciclin II controls presynaptic structural plasticity. Neuron 17:655-667.
63. Segal RA, Greenberg ME. 1996. Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci 19:463-489.
64. Sheng M, Thompson MA, Greenberg ME. 1991. CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252:1427-1430.
65. Simmons DL. 1993. Cloning cell surface molecules by transient expression in mammalian cells. In: Hartley DA, editor. Cellular interactions in development: a practical approach. Oxford: IRL Press. p 93-127.
66. Stoeckli ET, Landmesser LT. 1995. Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commisural neurons. Neuron 14:1165-1179.
67. Stork O, Welzl H, Cremer H, Schachner M. 1997. Increased intermale aggression and neuroendocrine response in mice deficient for the neural cell adhesiuon molecules. Eur J Neurosci 9:424-434.
68. Thanos S, Bonhoeffer F, Rutishauser U. 1984. Fiber-fiber interaction and tectal cues influence the development of the chicken retinotectal projection. Proc Natl Acad Sci USA 81:1906-1910.
69. 2+ influx regulated BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709-726.
70. van der Geer P, Wiley S, Gish GD, Pawson T. 1996. The Shc adaptor protein is highly phosphorylated at conserved, twin tyrosine residues (Y239/240) that mediate protein-protein interactions. Curr Biol 6:1435-1444.
71. Williams EJ, Furness J, Walsh FS, Doherty P. 1994. Activation of the FGF receptor underlies neunte outgrowth stimulated by L1, NCAM, and N-cadherin. Neuron 13:583-594.
72. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
73. Xing J, Ginty DD, Greenberg ME. 1996. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273:959-963.
74. Yin JC, Wallach JS, Del Vecchio M, Wilder EL, Zhou H, Quinn WG, Tully T. 1994. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79:49-58.