Critical role for Kalirin in nerve growth factor signaling through TrkA

Molecular and Cellular Biology

Volumn 25, Issue 12, 2005, Pages 5106-5118

  Chakrabarti, Kausik ^a   Lin, Kong ^a   Schiller, Noraisha I ^a   Wang, Yanping ^a   Koubi, David ^b   Fan, Ying Xin ^c   Rudkin, Brian B ^b   Johnson, Gibbes R ^c   Schiller, Martin R ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITÉ DE LYON   (France)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; KALIRIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN; PLECKSTRIN; PROTEIN TYROSINE KINASE A; RAC PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CELL STRAIN; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; MORPHOLOGY; NERVE FIBER GROWTH; NERVOUS SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENZYME ACTIVATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MAP KINASE KINASE 1; MICE; NERVE GROWTH FACTOR; NEURONS; PC12 CELLS; PROTEIN BINDING; PROTEIN ISOFORMS; RAC GTP-BINDING PROTEINS; RATS; RECEPTOR, TRKA; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 20344371219     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.12.5106-5118.2005     Document Type: Article

References (59)

1. Ahmed, Z., and T. S. Pillay. 2001. Functional effects of APS and SH2-B on insulin receptor signalling. Biochem. Soc. Trans. 29:529-534.
2. Ahmed, Z., and T. S. Pillay. 2003. Adapter protein with a pleckstrin homology (PH) and an Src homology 2 (SH2) domain (APS) and SH2-B enhance insulin-receptor autophosphorylation, extracellular-signal-regulated kinase and phosphoinositide 3-kinase-dependent signalling. Biochem. J. 371:405-412.
3. Bagrodia, S., S. J. Taylor, C. L. Creasy, J. Chernoff, and R. A. Cerione. 1995. Identification of a mouse p21Cdc42/Rac activated kinase. J. Biol. Chem. 270:22731-22737.
4. Barbacid, M. 1994. The Trk family of neurotrophin receptors. J. Neurobiol. 25:1386-1403.
5. Barker-Gibb, A. L., K. D. Dougherty, S. Einheber, C. T. Drake, and T. A. Milner. 2001. Hippocampal tyrosine kinase A receptors are restricted primarily to presynaptic vesicle clusters. J. Comp. Neurol. 430:182-199.
6. Barone, S. J., H. Hasegawa, D. K. F. Parran, and H. A. Tilson. 1998. Gestational exposure to methylmercury alters the developmental pattern of trk-like immunoreactivity in the rat brain and results in cortical dysmorphology. Brain Res. Dev. Brain Res. 109:13-31.
7. Bishop, A. L., and A. Hall. 2000. Rho GTPases and their effector proteins. Biochem. J. 348:241-255.
8. Boglari, G., and J. Szeberenyi. 2002. Nuclear translocation of p90Rsk and phosphorylation of CREB is induced by ionomycin in a Ras-independent manner in PC12 cells. Acta Biol. Hung. 53:325-334.
9. Boss, V., J. D. Roback, A. N. Young, L. J. Roback, D. M. V. Weisenhorn, R. Medina-Flores, and B. H. Wainer. 2001. Nerve growth factor, but not epidermal' growth factor, increases Fra-2 expression and alters Fra-2/JunD binding to AP-1 and CREB binding elements in pheochromocytoma (PC12) cells. J. Neurosci. 21:18-26.
10. Di Luca, M., F. Gardoni, A. Finardi, S. Pagliardini, F. Cattabeni, G. Battaglia, and C. Missale. 2001. NMDA receptor subunits are phosphorylated by activation of neurotrophin receptors in PSD of rat spinal cord. Neuroreport 12:1301-1305.
11. Drago, J., M. Murphy, K. A. Bailey, and P. F. Bartlett. 1991. A method for the isolation of purified murine neuroepithelial cells from the developing mouse brain. J. Neurosci. Methods 37:251-256.
12. Estrach, S., S. Schmidt, S. Diriong, A. Penna, A. Blangy, P. Fort, and A. Debant. 2002. The human Rho-GEF trio and its target GTPase RhoG are involved in the NGF pathway, leading to neurite outgrowth. Curr. Biol. 12:307-312.
13. Fan, Y. X., L. Wong, T. B. Deb, and G. R. Johnson. 2004. Ligand regulates epidermal growth factor receptor kinase specificity: activation increases preference for GAB1 and SHC versus autophosphorylation sites. J. Biol. Chem. 279:38143-38150.
14. Fuentes, E. J., A. E. Karnoub, M. A. Booden, C. J. Der, and S. L. Campbell. 2003. Critical role of the pleckstrin homology domain in Dbs signaling and growth regulation. J. Biol. Chem. 278:21188-21196.
15. Hansel, D. E., M. E. Quinones, G. V. Ronnett, and B. A. Eipper. 2001. Kalirin, a GDP/GTP exchange factor of the Dbl family, is localized to nerve, muscle, and endocrine tissue during embryonic rat development. J. Histochem. Cytochem. 49:833-844.
16. Horikawa, I., T. Miwa, T. Ishimaru, M. Furukawa, T. Kato, and T. Moriizumi. 1999. TrkA expression in olfactory epithelium and bulb during development. Neuroreport 10:2205-2208.
17. Howe, C. L., J. S. Valletta, A. S. Rusnak, and W. C. Mobley. 2001. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 32:801-814.
18. Husten, E. J., and B. A. Eipper. 1994. Purification and characterization of PAM-1, an integral membrane protein involved in peptide processing. Arch. Biochem. Biophys. 312:487-492.
19. Inagaki, N., H. Thoenen, and D. Lindholm. 1995. TrkA tyrosine residues involved in NGF-induced neurite outgrowth of PC12 cells. Eur. J. Neurosci. 7:1125-1133.
20. Jackson, T. R., I. J. Blader, L. P. Hammonds-Odie, C. R. Burga, F. Cooke, P. T. Hawkins, A. G. Wolf, K. A. Heldman, and A. B. Theibert. 1996. Initiation and maintenance of NGF-stimulated neurite outgrowth requires activation of a phosphoinositide 3-kinase. J. Cell Sci. 109:289-300.
21. Jessen, U., V. Novitskaya, N. Pedersen, P. Serup, V. Berezin, and E. Bock. 2001. The transcription factors CREB and c-Fos play key roles in NCAM-mediated neuritogenesis in PC12-E2 cells. J. Neurochem. 79:1149-1160.
22. Johnson, R. C., P. Penzes, B. A. Eipper, and R. E. Mains. 2000. Isoforms of kalirin, a neuronal Dbl family member, generated through use of different 5′- and 3′-ends along with an internal translational initiation site. J. Biol. Chem. 275:19324-19333.
23. Kari, B., N. Lussenhop, R. Goertz, M. Wabuke-Bunoti, R. Radeke, and R. Gehrz. 1986. Characterization of monoclonal antibodies reactive to several biochemically distinct human cytomegalovirus glycoprotein complexes. J. Virol. 60:345-352.
24. Kwon, Y. K., H. J. Jang, S. Kole, H. J. He, and M. Bernier. 2003. Role of the pleckstrin homology domain of PLGγ1 in its interaction with the insulin receptor. J. Cell Biol. 163:375-384.
25. Leoni, C., and F. Valtorta. 2002. Constitutive TrkA activity in receptor-overexpressing PC12 clones. Biochem. Biophys. Res. Commun. 291:972-978.
26. Lou, X. J., H. Yano, F. Lee, M. V. Chao, and M. G. Farquhar. 2001. GIPC and GAIP form a complex with TrkA: a putative link between G protein and receptor tyrosine kinase pathways. Mol. Biol. Cell 12:615-627.
27. Ma, A. D., and C. S. Abrams. 1999. Pleckstrin homology domains and phospholipid-induced cytoskeletal reorganization. Thromb. Haemost. 82: 399-406.
28. Ma, X. M., J. P. Huang, Y. Wang, B. A. Eipper, and R. E. Mains. 2003. Kalirin, a multifunctional Rho GEF, is necessary for maintenance of hippocampal pyramidal neuron dendrites and dendritic spines. J. Neurosci. 23:10593-10603.
29. Mahajan, N. P., and H. S. Earp. 2003. An SH2 domain-dependent, phosphotyrosine-independent interaction between Vav1 and the Mer receptor tyrosine kinase: a mechanism for localizing guanine nucleotide-exchange factor action. J. Biol. Chem. 278:42596-42603.
30. Maliartchouk, S., T. Debeir, N. Beglova, A. C. Cuello, K. Gehring, and H. U. Saragovi. 2000. Genuine monovalent ligands of TrkA nerve growth factor receptors reveal a novel pharmacological mechanism of action. J. Biol. Chem. 275:9946-9956.
31. Maroun, C. R., M. Holgado-Madruga, I. Royal, M. A. Naujokas, T. M. Fournier, A. J. Wong, and M. Park 1999. The Gab1 PH domain is required for localization of Gab1 at sites of cell-cell contact and epithelial morphogenesis downstream from the Met receptor tyrosine kinase. Mol. Cell. Biol. 19:1784-1799.
32. May, V., M. R. Schiller, B. A. Eipper, and R. E. Mains. 2002. Kalirin Dbl-homology guanine nucleotide exchange factor 1 domain initiates new axon outgrowths via RhoG-mediated mechanisms. J. Neurosci. 22:6980-6990.
33. Moores, S. L., L. M. Selfors, J. Fredericks, T. Breit, K. Fujikawa, F. W. Alt, J. S. Brugge, and W. Swat. 2000. Vav family proteins couple to diverse cell surface receptors. Mol. Cell. Biol. 20:6364-6373.
34. Murray, S. S., P. Perez, R. Lee, B. L. Hempstead, and M. V. Chao. 2004. A novel p75 neurotrophin receptor-related protein, NRH2, regulates nerve growth factor binding to the TrkA receptor. J. Neurosci. 24:2742-2749.
35. Nishida, K., Y. Kaziro, and T. Satoh. 1999. Association of the proto-oncogene product dbl with G protein βγ subunits. FEBS Lett. 459:186-190.
36. Penzes, P., A. Beeser, J. Chernoff, M. R. Schiller, B. A. Eipper, R. E. Mains, and R. L. Huganir. 2003. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrin B-EphB receptor activation of the Rho-GEF kalirin. Neuron 37:263-274.
37. Penzes, P., R. C. Johnson, M. R. Alam, V. Kambampati, R. E. Mains, and B. A. Eipper. 2000. An isoform of kalirin, a brain-specific GDP/GTP exchange factor, is enriched in the postsynaptic density fraction. J. Biol. Chem. 275:6395-6403.
38. Penzes, P., R. C. Johnson, V. Kambampati, R. E. Mains, and B. A. Eipper. 2001. Distinct roles for the two Rho GDP/GTP exchange factor domains of kalirin in regulation of neurite growth and neuronal morphology. J. Neurosci. 21:8426-8434.
39. Penzes, P., R. C. Johnson, R. Sattler, X. Zhang, R. L. Huganir, V. Kambampati, R. E. Mains, and B. A. Eipper. 2001. The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 29:229-242.
40. Posern, G., R. Saffrich, W. Ansorge, and S. M. Feller. 2000. Rapid lamellipodia formation in nerve growth factor-stimulated PC12 cells is dependent on Rac and PI3K activity. J. Cell. Physiol. 183:416-424.
41. Qian, X., and D. D. Ginty. 2001. SH2-B and APS are multimeric adapters that augment TrkA signaling. Mol. Cell. Biol. 21:1613-1620.
42. Razzini, G., A. Ingrosso, A. Brancaccio, S. Sciacchitano, D. L. Esposito, and M. Falasca. 2000. Different subcellular localization and phosphoinositides binding of insulin receptor substrate protein pleckstrin homology domains. Mol. Endocrinol. 14:823-836.
43. Schiller, M. R., A. Blangy, J. P. Huang, R. E. Mains, and B. A. Eipper. The two GEFs of Kalirin: specificity and activity-independent actions. J. Cell Sci., in press.
44. Schiller, M. R., R. E. Mains, and B. A. Eipper. 1995. A neuroendocrine-specific protein localized to the endoplasmic reticulum by distal degradation. J. Biol. Chem. 270:26129-26138.
45. Shamah, S. M., M. Z. Lin, J. L. Goldberg, S. Estrach, M. Sahin, L. Hu, M. Bazalakova, R. L. Neve, G. Corfas, A. Debant, and M. E. Greenberg. 2001. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105:233-244.
46. Shaywitz, A. J., and M. E. Greenberg. 1999. CREB: a stimulus-induced transcription factor activated bv a diverse array of extracellular signals. Annu. Rev. Biochem. 68:821-861.
47. Shmueli, O., A. Gdalyahu, K. Sorokina, E. Nevo, A. Avivi, and O. Reiner. 2001. DCX in PC12 cells: CREB-mediated transcription and neurite outgrowth. Hum. Mol. Genet. 10:1061-1070.
48. Swiercz, J. M., R. Kuner, J. Behrens, and S. Offermanns. 2002. Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 35:51-63.
49. Tanaka, M., R. Ohashi, R. Nakamura, K. Shinmura, T. Kamo, R. Sakai, and H. Sugimura. 2004. Tiam1 mediates neurite outgrowth induced by ephrin-B1 and EphA2. EMBO J. 23:1075-1088.
50. Taya, S., N. Inagaki, H. Sengikui, H. Makino, A. Iwamatsu, I. Urakawa, K. Nagao, S. Kataoka, and K. Kaibuchi. 2001. Direct interaction of insulin-like growth factor-1 receptor with leukemia-associated RhoGEF. J. Cell Biol. 155:809-820.
51. Teramoto, H., P. Salem, K. C. Robbins, X. R. Bustelo, and J. S. Gutkind. 1997. Tyrosine phosphorylation of the vav proto-oncogene product links Fc epsilon RI to the Rac1-JNK pathway. J. Biol. Chem. 272:10751-10755.
52. Watson, F. L., M. A. Porcionatto, A. Bhattacharyya, C. D. Stiles, and R. A. Segal. 1999. TrkA glycosylation regulates receptor localization and activity. J. Neurobiol. 39:323-336.
53. Wu, G. Y., K. Deisseroth, and R. W. Tsien. 2001. Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat. Neurosci. 4:151-158.
54. Xing, J., J. M. Kernhauser, Z. Xia, E. A. Thiele, and M. E. Greenberg. 1998. Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol. Cell. Biol. 18:1946-1955.
55. Yano, H., F. Cong, R. B. Birge, S. P. Goff, and M. V. Chao. 2000. Association of the abl tyrosine kinase with the Trk nerve growth factor receptor. J. Neurosci. Res. 59:356-364.
56. Yasui, H., H. Katoh, Y. Yamaguchi, J. Aoki, H. Fujila, K. Mori, and M. Negishi. 2001. Differential responses to nerve growth factor and epidermal growth factor in neurite outgrowth of PC12 cells are determined by Rac1 activation systems. J. Biol. Chem. 276:15298-15305.
57. York, R. D., H. Yao, T. Dillon, C. L. Ellig, S. P. Eckert, E. W. McCleskey, and P. J. Stork. 1998. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392:622-626.
58. Zapf-Colby, A., and J. M. Olefsky. 1998. Nerve growth factor processing and trafficking events following TrkA-mediated endocytosis. Endocrinology 139: 3232-3240.
59. Zheng, Y. 2002. DBL family guanine nucleotide exchange factors. Trends Biochem. Sci. 25:724-732.