Trk is a calmodulin-binding protein: Implications for receptor processing

Journal of Neurochemistry

Volumn 88, Issue 2, 2004, Pages 422-433

  Llovera, Marta ^a   De Pablo, Yolanda ^a   Egea, Joaquim ^a,f   Encinas, Mario ^a,g   Peiró, Sandra ^b   Martín Zanca, Dionisio ^c   Rocamora, Nativitat ^d   Comella, Joan X ^a,e  

^a Universitat de Lleida Facultat de Medicina Sabadell   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF SALAMANCA   (Spain)

^d CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^e UNIVERSITY OF LLEIDA   (Spain)

^f MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calmodulin binding protein; p41 fragment; PC12 cells; Rat cortical neurones; Receptor cleavage; Trk receptor

Indexed keywords

CALMODULIN; CALMODULIN BINDING PROTEIN; NEUROTROPHIN; PROTEIN TRK; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; BINDING KINETICS; BINDING SITE; CALCIUM CELL LEVEL; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL POPULATION; CELL SURVIVAL; CONTROLLED STUDY; FETUS; IMMUNOPRECIPITATION; INHIBITION KINETICS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0347087301     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.02178.x     Document Type: Article

References (45)

1. Alexander K. A., Cimler B. M., Meier K. E. and Storm D. R. (1987) Regulation of calmodulin binding to P-57: a neurospecific calmodulin binding protein. J. Biol. Chem. 262, 6108-6113.
2. Arevalo J. C., Conde B., Hempstead B. L., Chao M. V., Martin-Zanca D. and Perez P. (2000) TrkA immunoglobulin-like ligand binding domains inhibit spontaneous activation of the receptor. Mol. Cell. Biol. 20, 5908-5916.
3. Arevalo J. C., Conde B., Hempstead B. I., Chao M. V., Martin-Zanca D. and Perez P. (2001) A novel mutation within the extracellular domain of TrkA causes constitutive receptor activation. Oncogene 20, 1229-1234.
4. Barbacid M. (1995) Neurotrophic factors and their receptors. Curr. Opin. Cell Biol. 7, 148-155.
5. Cabrera N., Diaz-Rodriguez E., Becker E., Martin-Zanca D. and Pandiella A. (1996) TrkA receptor ectodomain cleavage generates a tyrosine-phosphorylated cell-associated fragment. J. Cell. Biol. 132, 427-436.
6. Clary D. O., Weskamp. G., Austin. L. R. and Reichardt L. F. (1994) TrkA cross-linking mimics neuronal responses to nerve growth factor. Mol. Biol. Cell 5, 549-563.
7. Crivici A. and Ikura M. (1995) Molecular and structural basis of target recognition by calmodulin. Annu. Rev. Biophys. Biomol. Struct. 24, 85-116.
8. Crowley C., Spencer S. D., Nishimura M. C., Chen K. S., Pitts-Meek S., Armanini M. P., Ling L. H., MacMahon S. B., Shelton D. L., Levinson A. D. et al. (1994) Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76, 1001-1011.
9. Davies A. M. (1994) The role of neurotrophins in the developing nervous system. J. Neurobiol. 25, 1334-1348.
10. Delcroix J. D., Valletta J. S., Wu C., Hunt S. J., Kowal A. S. and Mobley W. C. (2003) NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron 39, 69-84.
11. Diaz-Rodriguez E., Cabrera N., Esparis-Ogando A., Montero J. C. and Pandiella A. (1999) Cleavage of the TrkA neurotrophin receptor by multiple metalloproteases generates signalling-competent truncated forms. Eur. J. Neurosci. 11, 1421-1430.
12. Diaz-Rodriguez E., Esparis-Ogando A., Montero J. C., Yuste L. and Pandiella A. (2000) Stimulation of cleavage of membrane proteins by calmodulin inhibitors. Biochem. J. 346, 359-367.
13. Egea J., Espinet C. and Comella J. X. (1999) Calcium influx activates extracellular-regulated kinase/mitogen-activated protein kinase pathway through a calmodulin-sensitive mechanism in PC12 cells. J. Biol. Chem. 274, 75-85.
14. Egea J., Espinet C., Soler R. M., Peiro S., Rocamora N. and Comella J. X. (2000) Nerve growth factor activation of the extracellular signal-regulated kinase pathway is modulated by Ca(2+) and calmodulin. Mol. Cell. Biol. 20, 1931-1946.
15. Egea J., Espinet C., Soler R. M., Dolcet X., Yuste V. J., Encinas M., Iglesias M., Rocamora N. and Comella J. X. (2001) Neuronal survival induced by neurotrophins requires calmodulin. J. Cell. Biol. 154, 585-597.
16. Fukumitsu H., Furukawa Y., Tsusaka M., Kinukawa H., Nitta A., Nomoto H., Mima T. and Furukawa S. (1998) Simultaneous expression of brain-derived neurotrophic factor and neurotrophin-3 in Cajal-Retzius, subplate and ventricular progenitor cells during early development stages of the rat cerebral cortex. Neuroscience 84, 115-127.
17. Gnegy M. E. (1995) Calmodulin: effects of cell stimuli and drugs on cellular activation. Prog. Drug Res. 45, 33-65.
18. Graves C. B., Goewert R. R. and McDonald J. M. (1985) The insulin receptor contains a calmodulin-binding domain. Science 230, 827-829.
19. Graves C. B., Gale R. D., Laurino J. P. and McDonald J. M. (1986) The insulin receptor and calmodulin: calmodulin enhances insulin-mediated receptor kinase activity and insulin stimulates phosphorylation of calmodulin. J. Biol. Chem. 261, 10429-10438.
20. Hamburger V. and Levi-Montalcini R. (1949) Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. J. Exp. Zool. 111, 457-501.
21. Holgado-Madruga M., Moscatello D. K., Emlet D. R., Dieterich R. and Wong A. J. (1997) Grb2-associated binder-1 mediates phosphatidylinositol 3-kinase activation and the promotion of cell survival by nerve growth factor. Proc. Natl Acad. Sci. USA 94, 12419-12424.
22. Huang K. P., Huang F. L. and Chen H. C. (1993) Characterization of a 7.5-kDa protein kinase C substrate (RC3 protein, neurogranin) from rat brain. Arch. Biochem. Biophys. 305, 570-580.
23. Jiang H. and Guroff G. (1997) Actions of the neurotrophins on calcium uptake. J. Neurosci. Res. 50, 355-360.
24. Jullien J., Guili V., Reichardt L. F. and Rudkin B. B. (2002) Molecular kinetics of nerve growth factor receptor trafficking and activation. J. Biol. Chem. 277, 38700-38708.
25. Jullien J., Guili V., Derrington E. A., Darlix J. L., Reichardt L. F. and Rudkin B. B. (2003) Trafficking of TrkA-GFP chimera during NGF-induced differentiation. J. Biol. Chem. 278, 8706-8716.
26. Kahn J., Walcheck B., Migaki G. I., Jutila M. A. and Kishimoto T. K. (1998) Calmodulin regulates 1-selectin adhesion molecule expression and function through a protease-dependent mechanism. Cell 92, 809-818.
27. Kanning K. C., Hudson M., Amieux P. S., Wiley J. C., Bothwell M. and Schecterson L. C. (2003) Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability. J. Neurosci. 23, 5425-5436.
28. Klee C. B., Crouch T. H. and Richman P. G. (1980) Calmodulin. Annu. Rev. Biochem. 49, 489-515.
29. Levitan I. B. (1999) It is calmodulin after all! Mediator of the calcium modulation of multiple ion channels. Neuron 22, 645-648.
30. Lewin G. R. and Barde Y. A. (1996) Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
31. Li H. and Villalobo A. (2002) Evidence for the direct interaction between calmodulin and the human epidermal growth factor receptor. Biochem. J. 362, 499-505.
32. MacInnis B. L. and Campenot R. B. (2002) Retrograde support of neuronal survival without retrograde transport of nerve growth factor. Science 295, 1536-1539.
33. Martin-Nieto J. and Villalobo A. (1998) The human epidermal growth factor receptor contains a juxtamembrane calmodulin-binding site. Biochemistry 37, 227-236.
34. Martin-Zanca D., Oskam R., Mitra G., Copeland T. and Barbacid M. (1989) Molecular and biochemical characterization of the human trk proto-oncogene. Mol. Cell. Biol. 9, 24-33.
35. Mobley W. C., Schenker A. and Shooter E. M. (1976) Characterization and isolation of proteolytically modified nerve growth factor. Biochemistry 15, 5543-5552.
36. Pandiella-Alonso A., Malgaroli A., Vicentini L. M. and Meldolesi J. (1986) Early rise of cytosolic Ca2+ induced by NGF in PC12 and chromaffin cells. FEBS Lett. 208, 48-51.
37. Rodrigues G. A. and Park M. (1994) Oncogenic activation of tyrosine kinases. Curr Opin. Genet. Dev 4, 15-24.
38. Smeyne R. J., Klein R., Schnapp A., Long L. K., Bryant S., Lewin A., Lira S. A. and Barbacid M. (1994) Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368, 246-249.
39. Stephens R. M., Loeb D. M., Copeland T. D., Pawson T., Greene L. A. and Kaplan D. R. (1994) Trk receptors use redundant signal transduction pathways involving SHC and PLC-gamma 1 to mediate NGF responses. Neuron 12, 691-705.
40. Swanljung-Collins H. and Collins J. H. (1994) Brush border myosin I has a calmodulin/phosphatidylserine switch and tail actin-binding. Adv. Exp. Med. Biol. 358, 205-213.
41. Tapley P., Lamballe F. and Barbacid M. (1992) K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 7, 371-381.
42. Tebar F., Villalonga P., Sorkina T., Agell N., Sorkin A. and Enrich C. (2002) Calmodulin regulates intracellular trafficking of epidermal growth factor receptor and the MAPK signaling pathway. Mol. Biol. Cell 13, 2057-2068.
43. Vogel H. J. (1994) The Merck Frosst Award Lecture 1994. Calmodulin: a versatile calcium mediator protein. Biochem. Cell. Biol. 72, 357-376.
44. Yamada M., Ohnishi H., Sano S., Nakatani A., Ikeuchi T. and Hatanaka H. (1997) Insulin receptor substrate (IRS)-1 and IRS-2 are tyrosine-phosphorylated and associated with phosphatidylinositol 3-kinase in response to brain-derived neurotrophic factor in cultured cerebral cortical neurons. J. Biol. Chem. 272, 30334-30339.
45. Ye H., Kuruvilla R., Zweifel L. S. and Ginty D. D. (2003) Evidence in support of signaling endosome-based retrograde survival of sympathetic neurons. Neuron 39, 57-68.