Ca2+/calmodulin and apo-calmodulin both bind to and enhance the tyrosine kinase activity of c-Src

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Stateva, Silviya R ^a   Salas, Valentina ^a,b   Anguita, Estefanía ^a   Benaim, Gustavo ^b,c   Villalobo, Antonio ^a  

^a CSIC   (Spain)

^b FACULTAD DE CIENCIAS   (Venezuela)

^c Fundacion Instituto de Estudios Avanzados IDEA   (Venezuela)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALMODULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; PROTEIN TYROSINE KINASE; PROTEIN BINDING;

AFFINITY CHROMATOGRAPHY; ARTICLE; AUTOPHOSPHORYLATION; BREAST ADENOCARCINOMA; CALCIUM CELL LEVEL; CANCER CELL LINE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME REGULATION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; IN VITRO STUDY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; SQUAMOUS CELL CARCINOMA; WESTERN BLOTTING; METABOLISM; TUMOR CELL LINE;

CALCIUM; CALMODULIN; CELL LINE, TUMOR; HUMANS; PROTEIN BINDING; SRC-FAMILY KINASES;

EID: 84936805391     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128783     Document Type: Article

References (49)

1. Chin D, Means AR (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10: 322-328. PMID: 10884684
2. Jurado LA, Chockalingam PS, Jarrett HW (1999) Apocalmodulin. Physiol Rev 79: 661-682. PMID: 10390515
3. Crivici A, Ikura M (1995) Molecular and structural basis of target recognition by calmodulin. Annu Rev Biophys Biomol Struct 24: 85-116. PMID: 7663132
4. Hoeflich KP, Ikura M (2002) Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108: 739-742. PMID: 11955428
5. Tidow H, Nissen P (2013) Structural diversity of calmodulin binding to its target sites. FEBS J 280: 5551-5565. doi: 10.1111/febs.12296 PMID: 23601118
6. Rhoads AR, Friedberg F (1997) Sequence motifs for calmodulin recognition. FASEB J 11: 331-340. PMID: 9141499
7. Ba¨hler M, Rhoads A (2002) Calmodulin signaling via the IQ motif. FEBS Lett 513: 107-113. PMID: 11911888
8. Mal TK, Skrynnikov NR, Yap KL, Kay LE, Ikura M (2002) Detecting protein kinase recognition modes of calmodulin by residual dipolar couplings in solution NMR. Biochemistry 41: 12899-12906. PMID: 12390014
9. Yamniuk AP, Vogel HJ (2004) Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol Biotechnol 27: 33-57. PMID: 15122046
10. 2+/calmodulin binding and autoinhibition. J Biol Chem 284: 15573-15588. doi: 10.1074/jbc.M809585200 PMID: 19305019
11. Berchtold MW, Villalobo A (2014) The many faces of calmodulin in cell proliferation, programmed cell death, autophagy, and cancer. Biochim Biophys Acta 1843: 398-435. doi: 10.1016/j.bbamcr.2013.10.021 PMID: 24188867
12. Martin-Nieto J, Villalobo A (1998) The human epidermal growth factor receptor contains a juxtamembrane calmodulin-binding site. Biochemistry 37: 227-236. PMID: 9425043
13. Li H, Ruano MJ, Villalobo A (2004) Endogenous calmodulin interacts with the epidermal growth factor receptor in living cells. FEBS Lett 559: 175-180. PMID: 14960328
14. Li H, Panina S, Kaur A, Ruano MJ, Sanchez-Gonzalez P, et al. (2012) Regulation of the ligand-dependent activation of the epidermal growth factor receptor by calmodulin. J Biol Chem 287: 3273-3281. doi: 10.1074/jbc.M111.317529 PMID: 22157759
15. McLaughlin S, Smith SO, Hayman MJ, Murray D (2005) An electrostatic engine model for autoinhibition and activation of the epidermal growth factor receptor (EGFR/ErbB) family. J Gen Physiol 126: 41-53. PMID: 15955874
16. Li H, Sanchez-Torres J, Del Carpio A, Salas V, Villalobo A (2004) The ErbB2/Neu/HER2 receptor is a new calmodulin-binding protein. Biochem J 381: 257-266. PMID: 15080792
17. Graves CB, Gale RD, Laurino JP, McDonald JM (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. PMID: 3525545
18. Llovera M, de Pablo Y, Egea J, Encinas M, Peiro S, et al. (2004) Trk is a calmodulin-binding protein: implications for receptor processing. J Neurochem 88: 422-433. PMID: 14690530
19. Parsons SJ, Parsons JT (2004) Src family kinases, key regulators of signal transduction. Oncogene 23: 7906-7909. PMID: 15489908
20. Benaim G, Villalobo A (2002) Phosphorylation of calmodulin. Functional implications. Eur J Biochem 269: 3619-3631. PMID: 12153558
21. Hayashi N, Nakagawa C, Ito Y, Takasaki A, Jinbo Y, et al. (2004) Myristoylation-regulated direct interaction between calcium-bound calmodulin and N-terminal region of pp60v-src . J Mol Biol 338: 169-180. PMID: 15050832
22. 2+/calmodulin-, Src- and PP2A-mediated pathway and promote melanoma tumor growth. Carcinogenesis 33: 740-750. doi: 10.1093/carcin/bgs021 PMID: 22287561
23. Yang W, Wang X, Duan C, Lu L, Yang H (2013) α-Synuclein overexpression increases phospho-protein phosphatase 2A levels via formation of calmodulin/Src complex. Neurochem Int 63: 180-194. doi: 10.1016/j.neuint.2013.06.010 PMID: 23796501
24. Yuan K, Jing G, Chen J, Liu H, Zhang K, et al. (2011) Calmodulin mediates Fas-induced FADD-independent survival signaling in pancreatic cancer cells via activation of Src-extracellular signal-regulated kinase (ERK). J Biol Chem 286: 24776-24784. doi: 10.1074/jbc.M110.202804 PMID: 21613217
25. Wu J, Masci PP, Chen C, Chen J, Lavin MF, et al. (2015) β-Adducin siRNA disruption of the spectrin-based cytoskeleton in differentiating keratinocytes prevented by calcium acting through calmodulin/epidermal growth factor receptor/cadherin pathway. Cell Signal 27: 15-25. doi: 10.1016/j.cellsig.2014.10.001 PMID: 25305142
26. Pérez Y, Maffei M, Igea A, Amata I, Gairi M, et al. (2013) Lipid binding by the Unique and SH3 domains of c-Src suggests a new regulatory mechanism. Sci Rep 3: 1295. doi: 10.1038/srep01295 PMID: 23416516
27. Salas V, Sanchez-Torres J, Cusido-Hita DM, Garcia-Marchan Y, Sojo F, et al. (2005) Characterisation of tyrosine-phosphorylation-defective calmodulin mutants. Protein Expr Purif 41: 384-392. PMID: 15866726
28. Stateva SR, Salas V, Benaim G, Menéndez M, Solís D, et al. (2015) Characterization of phospho-(tyrosine)-mimetic calmodulin mutants. PLoS One 10: e0120798. doi: 10.1371/journal.pone.0120798 PMID: 25830911
29. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685. PMID: 5432063
30. Parks EE, Ceresa BP (2014) Cell surface epidermal growth factor receptors increase Src and c-Cbl activity and receptor ubiquitylation. J Biol Chem 289: 25537-25545. doi: 10.1074/jbc.M114.579581 PMID: 25074934
31. Sato K, Ogawa K, Tokmakov AA, Iwasaki T, Fukami Y (2001) Hydrogen peroxide induces Src family tyrosine kinase-dependent activation of Xenopus eggs. Dev Growth Differ 43: 55-72. PMID: 11148452
32. Basuroy S, Dunagan M, Sheth P, Seth A, Rao RK (2010) Hydrogen peroxide activates focal adhesion kinase and c-Src by a phosphatidylinositol 3 kinase-dependent mechanism and promotes cell migration in Caco-2 cell monolayers. Am J Physiol Gastrointest Liver Physiol 299: G186-G195. doi: 10.1152/ajpgi.00368.2009 PMID: 20378826
33. Hidaka H, Sasaki Y, Tanaka T, Endo T, Ohno S, et al. (1981) N-(6-aminohexyl)-5-chloro-1-naphthalenesulfonamide, a calmodulin antagonist, inhibits cell proliferation. Proc Natl Acad Sci U S A 78: 4354-4357. PMID: 6945588
34. Hidaka H, Tanaka T (1983) Naphthalenesulfonamides as calmodulin antagonists. Methods Enzymol 102: 185-194. PMID: 6139736
35. Anderson D, Koch CA, Grey L, Ellis C, Moran MF, et al. (1990) Binding of SH2 domains of phospholipase Cγ1, GAP, and Src to activated growth factor receptors. Science 250: 979-982. PMID: 2173144
36. Lombardo CR, Consler TG, Kassel DB (1995) In vitro phosphorylation of the epidermal growth factor receptor autophosphorylation domain by c-Src: identification of phosphorylation sites and c-Src SH2 domain binding sites. Biochemistry 34: 16456-16466. PMID: 8845374
37. Sato K, Sato A, Aoto M, Fukami Y (1995) Site-specific association of c-Src with epidermal growth factor receptor in A431 cells. Biochem Biophys Res Commun 210: 844-851. PMID: 7539262
38. Biscardi JS, Belsches AP, Parsons SJ (1998) Characterization of human epidermal growth factor receptor and c-Src interactions in human breast tumor cells. Mol Carcinog 21: 261-272. PMID: 9585256
39. Gao Y, Tang S, Zhou S, Ware JA (2001) The thromboxane A2 receptor activates mitogen-activated protein kinase via protein kinase C-dependent Gi coupling and Src-dependent phosphorylation of the epidermal growth factor receptor. J Pharmacol Exp Ther 296: 426-433. PMID: 11160627
40. 2-induced transactivation of EGF receptor requires Src and mediates ERK1/2, but not Akt, activation in renal cells. Am J Physiol Renal Physiol 286: F858-865. PMID: 15075181
41. Osawa M, Swindells MB, Tanikawa J, Tanaka T, Mase T, et al. (1998) Solution structure of calmodulin-W-7 complex: the basis of diversity in molecular recognition. J Mol Biol 276: 165-176. PMID: 9514729
42. Bobe R, Yin X, Roussanne MC, Stepien O, Polidano E, et al. (2003) Evidence for ERK1/2 activation by thrombin that is independent of EGFR transactivation. Am J Physiol Heart Circ Physiol 285: H745-754. PMID: 12730054
43. Samak G, Narayanan D, Jaggar JH, Rao R (2011) CaV1.3 channels and intracellular calcium mediate osmotic stress-induced N-terminal c-Jun kinase activation and disruption of tight junctions in Caco-2 cell monolayers. J Biol Chem 286: 30232-30243. doi: 10.1074/jbc.M111.240358 PMID: 21737448
44. 2+ signaling in cardiac myocytes. J Mol Cell Cardiol 52: 312-316. doi: 10.1016/j.yjmcc.2011.06.005 PMID: 21708171
45. Sengupta P, Ruano MJ, Tebar F, Golebiewska U, Zaitseva I, et al. (2007) Membrane-permeable calmodulin inhibitors (e.g. W-7/W-13) bind to membranes, changing the electrostatic surface potential: dual effect of W-13 on epidermal growth factor receptor activation. J Biol Chem 282: 8474-8486. PMID: 17227773
46. Schatzman RC, Raynor RL, Kuo JF (1983) N-(6-Aminohexyl)-5-chloro-1-naphthalenesulfonamide(W-7), a calmodulin antagonist, also inhibits phospholipid-sensitive calcium-dependent protein kinase. Biochim Biophys Acta 755: 144-147. PMID: 6297609
47. c-src function. J Biol Chem 264: 20886-20893. PMID: 2480346
48. Cooper JA, Howell B (1993) The when and how of Src regulation. Cell 73: 1051-1054. PMID: 7685656
49. Irtegun S, Wood RJ, Ormsby AR, Mulhern TD, Hatters DM (2013) Tyrosine 416 is phosphorylated in the closed, repressed conformation of c-Src. PLoS One 8: e71035. doi: 10.1371/journal.pone.0071035 PMID: 23923048