The Calpain/Calpastatin System Has Opposing Roles in Growth and Metastatic Dissemination of Melanoma

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Raimbourg, Quentin ^a   Perez, Joëlle ^a   Vandermeersch, Sophie ^a   Prignon, Aurélie ^b   Hanouna, Guillaume ^a   Haymann, Jean Philippe ^c   Baud, Laurent ^c   Letavernier, Emmanuel ^c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c Urgences Néphrologiques et Transplantation Rénale Hôpital Tenon 4   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CALPASTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER INVASION; CELL INFILTRATION; CELL MIGRATION; CONTROLLED STUDY; IMMUNOCOMPETENT CELL; LYMPH NODE METASTASIS; MALE; MELANOMA; MELANOMA CELL; METASTASIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR ESCAPE; TUMOR IMMUNITY; TUMOR VASCULARIZATION;

ANIMALS; CALCIUM-BINDING PROTEINS; CALPAIN; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; MALE; MELANOMA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC;

EID: 84875648563     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060469     Document Type: Article

References (51)

1. Goll DE, Thompson VF, Li H, Wei W, Cong J, (2003) The calpain system. Physiol Rev 83: 731-801.
2. Glading A, Uberall F, Keyse SM, Lauffenburger DA, Wells A, (2001) Membrane proximal ERK signaling is required for M-calpain activation downstream of epidermal growth factor receptor signaling. J Biol Chem 276: 23341-8.
3. Su Y, Cui Z, Li Z, Block ER, (2006) Calpain-2 regulation of VEGF-mediated angiogenesis. FASEB J 20: 1443-51.
4. Franco SJ, Huttenlocher A, (2005) Regulating cell migration: calpains make the cut. J Cell Sci 118: 3829-38.
5. Dewitt S, Hallett M, (2007) Leukocyte membrane "expansion": a central mechanism for leukocyte extravasation. J Leukoc Biol 81: 1160-4.
6. Beckerle MC, Burridge K, DeMartino GN, Croall DE, (1987) Colocalization of calcium-dependent protease II and one of its substrates at sites of cell adhesion. Cell 51: 569-77.
7. Han Y, Weinman S, Boldogh I, Walker RK, Brasier AR, (1999) Tumor necrosis factor-alpha-inducible IkappaBalpha proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-kappab activation. J Biol Chem 274: 787-94.
8. Youn JY, Wang T, Cai H, (2009) An ezrin/calpain/PI3K/AMPK/eNOSs1179 signaling cascade mediating VEGF-dependent endothelial nitric oxide production. Circ Res 104: 50-9.
9. Letavernier B, Zafrani L, Nassar D, Perez J, Levi C, et al. (2012) Calpains contribute to vascular repair in rapidly progressive form of glomerulonephritis: potential role of their externalization. Arterioscler Thromb Vasc Biol 32: 335-42.
10. Lu T, Xu Y, Mericle MT, Mellgren RL, (2002) Participation of the conventional calpains in apoptosis. Biochim Biophys Acta 1590: 16-26.
11. Squier MK, Sehnert AJ, Sellins KS, Malkinson AM, Takano E, et al. (1999) Calpain and calpastatin regulate neutrophil apoptosis. J Cell Physiol 178: 311-9.
12. Arthur JS, Elce JS, Hegadorn C, Williams K, Greer PA, (2000) Disruption of the murine calpain small subunit gene, Capn4: calpain is essential for embryonic development but not for cell growth and division. Mol Cell Biol 20: 4474-81.
13. Azam M, Andrabi SS, Sahr KE, Kamath L, Kuliopulos A, et al. (2001) Disruption of the mouse mu-calpain gene reveals an essential role in platelet function. Mol Cell Biol 21: 2213-20.
14. Dutt P, Croall DE, Arthur JS, Veyra TD, Williams K, et al. (2006) m-Calpain is required for preimplantation embryonic development in mice. BMC Dev Biol 24 6: 3.
15. Storr SJ, Carragher NO, Frame MC, Parr T, Martin SG, (2011) The calpain system and cancer. Nat Rev Cancer 11: 364-74.
16. Shiba E, Kambayashi JI, Sakon M, Kawasaki T, Kobayashi T, et al. (1996) Ca2+-Dependent Neutral Protease (Calpain) Activity in Breast Cancer Tissue and Estrogen Receptor Status. Breast Cancer 3: 13-17.
17. Kimura Y, Koga H, Araki N, Mugita N, Fujita N, et al. (1998) The involvement of calpain-dependent proteolysis of the tumor suppressor NF2 (merlin) in schwannomas and meningiomas. Nat Med 4: 915-22.
18. Lakshmikuttyamma A, Selvakumar P, Kanthan R, Kanthan SC, Sharma RK, (2004) Overexpression of m-calpain in human colorectal adenocarcinomas. Cancer Epidemiol Biomarkers Prev 13: 1604-9.
19. Braun C, Engel M, Seifert M, Theisinger B, Seitz G, et al. (1999) Expression of calpain I messenger RNA in human renal cell carcinoma: correlation with lymph node metastasis and histological type. Int J Cancer 84: 6-9.
20. Bai DS, Dai Z, Zhou J, Liu YK, Qiu SJ, et al. (2009) Capn4 overexpression underlies tumor invasion and metastasis after liver transplantation for hepatocellular carcinoma. Hepatology 49: 460-70.
21. Salehin D, Fromberg I, Haugk C, Dohmen B, Georg T, et al. (2010) Immunhistochemical analysis for expression of calpain 1, calpain 2 and calpastatin in endometrial cancer. Anticancer Res 30: 2837-43.
22. Yoshikawa Y, Mukai H, Hino F, Asada K, Kato I, (2000) Isolation of two novel genes, down-regulated in gastric cancer. Jpn J Cancer Res 91: 459-63.
23. Moreno-Luna R, Abrante A, Esteban F, González-Moles MA, Delgado-Rodríguez M, et al. (2011) Calpain 10 gene and laryngeal cancer: a survival analysis. Head Neck 33: 72-6.
24. Frances CP, Conde MC, Saez ME, Diez SF, Rey CM, et al. (2007) Identification of a protective haplogenotype within CAPN10 gene influencing colorectal cancer susceptibility. J Gastroenterol Hepatol 22: 2298-302.
25. Moretti D, Del Bello B, Cosci E, Biagioli M, Miracco C, et al. (2009) Novel variants of muscle calpain 3 identified in human melanoma cells: cisplatin-induced changes in vitro and differential expression in melanocytic lesions. Carcinogenesis 30: 960-7.
26. Kubbutat MH, Vousden KH, (1997) Proteolytic cleavage of human p53 by calpain: a potential regulator of protein stability. Mol Cell Biol 17: 460-8.
27. Potter DA, Tirnauer JS, Janssen R, Croall DE, Hughes CN, et al. (1998) Calpain regulates actin remodeling during cell spreading. J Cell Biol 141: 647-62.
28. Benetti R, Copetti T, Dell'Orso S, Melloni E, Brancolini C, et al. (2005) The calpain system is involved in the constitutive regulation of beta-catenin signaling functions. Biol Chem 280: 22070-80.
29. Gafni J, Cong X, Chen SF, Gibson BW, Ellerby LM, (2009) Calpain-1 cleaves and activates caspase-7. J Biol Chem 284: 25441-9.
30. Gao G, Dou QP, (2000) N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome C release and apoptotic cell death. J Cell Biochem 80: 53-72.
31. Hirai S, Kawasaki H, Yaniv M, Suzuki K, (1991) Degradation of transcription factors, c-Jun and c-Fos, by calpain. FEBS Lett 287: 57-61.
32. Kim MJ, Jo DG, Hong GS, Kim BJ, Lai M, et al. (2002) Calpain-dependent cleavage of cain/cabin1 activates calcineurin to mediate calcium-triggered cell death. Proc Natl Acad Sci U S A 99: 9870-5.
33. Polster BM, Basañez G, Etxebarria A, Hardwick JM, Nicholls DG, (2005) Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J Biol Chem 280: 6447-54.
34. Demarchi F, Bertoli C, Copetti T, Tanida I, Brancolini C, et al. (2006) Calpain is required for macroautophagy in mammalian cells. J Cell Biol 175: 595-605.
35. Letavernier E, Dansou B, Lochner M, Perez J, Bellocq A, et al. (2011) Critical role of the calpain/calpastatin balance in acute allograft rejection. Eur J Immunol 41: 473-84.
36. Peltier J, Bellocq A, Perez J, Doublier S, Dubois YC, et al. (2006) Calpain activation and secretion promote glomerular injury in experimental glomerulonephritis: evidence from calpastatin-transgenic mice. J Am Soc Nephrol 17: 3415-23.
37. Letavernier E, Perez J, Bellocq A, Mesnard L, de Castro Keller A, et al. (2008) Targeting the calpain/calpastatin system as a new strategy to prevent cardiovascular remodeling in angiotensin II-induced hypertension. Circ Res 102: 720-8.
38. Nassar D, Letavernier E, Baud L, Aractingi S, Khosrotehrani K, (2012) Calpain activity is essential in skin wound healing and contributes to scar formation. PLoS One 7: e37084.
39. Storr SJ, Mohammed RA, Woolston CM, Green AR, Parr T, et al. (2011) Calpastatin is associated with lymphovascular invasion in breast cancer. Breast 20: 413-8.
40. Fenouille N, Grosso S, Yunchao S, Mary D, Pontier-Bres R, et al. (2012) Calpain 2-dependent IκBα degradation mediates CPT-11 secondary resistance in colorectal cancer xenografts. J Pathol 227: 118-29.
41. Ho WC, Pikor L, Gao Y, Elliott BE, Greer PA, (2012) Calpain 2 regulates Akt-FoxO-p27(Kip1) protein signaling pathway in mammary carcinoma. J Biol Chem 287: 15458-65.
42. Frangié C, Zhang W, Perez J, Dubois YC, Haymann JP, et al. (2006) Extracellular calpains increase tubular epithelial cell mobility. Implications for kidney repair after ischemia. J Biol Chem 281: 26624-32.
43. Lokuta MA, Nuzzi PA, Huttenlocher A, (2003) Calpain regulates neutrophil chemotaxis. Proc Natl Acad Sci U S A 100: 4006-11.
44. Cortesio CL, Boateng LR, Piazza TM, Bennin DA, Huttenlocher A, (2011) Calpain-mediated proteolysis of paxillin negatively regulates focal adhesion dynamics and cell migration. J Biol Chem 286: 9998-10006.
45. Bellocq A, Doublier S, Suberville S, Perez J, Escoubet B, et al. (1999) Somatostatin increases glucocorticoid binding and signaling in macrophages by blocking the calpain-specific cleavage of Hsp 90. J Biol Chem 274: 36891-6.
46. Wang X, Song X, Zhuo W, Fu Y, Shi H, et al. (2009) The regulatory mechanism of Hsp90alpha secretion and its function in tumor malignancy. Proc Natl Acad Sci U S A 106: 21288-93.
47. Martin-Orozco N, Muranski P, Chung Y, Yang XO, Yamazaki T, et al. (2009) T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 31: 787-98.
48. Loges S, Mazzone M, Hohensinner P, Carmeliet P, (2009) Silencing or fueling metastasis with VEGF inhibitors: antiangiogenesis revisited. Cancer Cell 15: 167-70.
49. Getz GS, (2012) Calpain inhibition as a potential treatment of Alzheimer's disease. Am J Pathol 181: 388-91.
50. Higuchi M, Iwata N, Matsuba Y, Takano J, Suemoto T, et al. (2012) Mechanistic involvement of the calpain-calpastatin system in Alzheimer neuropathology. FASEB J 26: 1204-17.
51. Leloup L, Wells A, (2011) Calpains as potential anti-cancer targets. Expert Opin Ther Targets 15: 309-23.