Calpain activity is essential in skin wound healing and contributes to scar formation

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Nassar, Dany ^a,b   Letavernier, Emmanuel ^a,c,d   Baud, Laurent ^a,c,d   Aractingi, Selim ^a,b,d   Khosrotehrani, Kiarash ^a,b,e  

^a SORBONNE UNIVERSITÉ   (France)

^b CENTRE DE RECHERCHE SAINT ANTOINE   (France)

^c INSERM   (France)

^d HÔPITAL TENON   (France)

^e UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALPAIN; CALPASTATIN; CALPEPTIN; TRANSFORMING GROWTH FACTOR BETA;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; CELL PROLIFERATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EPIDERMIS; EPITHELIZATION; FEMALE; GENE OVEREXPRESSION; GRANULATION TISSUE; HOMOZYGOSITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MORPHOLOGY; MOUSE; MYOFIBROBLAST; NONHUMAN; PROTEIN DEGRADATION; SCAR FORMATION; SKIN INJURY; TRANSGENIC MOUSE; WOUND HEALING;

ACTINS; ANIMALS; ANTIGENS, CD31; BLOOD VESSELS; CALCIUM-BINDING PROTEINS; CALPAIN; CELL ADHESION; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; CICATRIX; COLLAGEN; FEMALE; FIBROBLASTS; FIBROSIS; GRANULATION TISSUE; HUMANS; INFLAMMATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOFIBROBLASTS; SKIN; WOUND HEALING;

MUS; MUS MUSCULUS;

EID: 84861204362     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037084     Document Type: Article

References (56)

1. Fathke C, Wilson L, Hutter J, Kapoor V, Smith A, et al. (2004) Contribution of bone marrow-derived cells to skin: collagen deposition and wound repair. Stem cells 22: 812-822.
2. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, et al. (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circulation research 85: 221-228.
3. Morris LM, Klanke CA, Lang SA, Pokall S, Maldonado AR, et al. (2010) Characterization of endothelial progenitor cells mobilization following cutaneous wounding. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society 18: 383-390.
4. Kim MH, Liu W, Borjesson DL, Curry FR, Miller LS, et al. (2008) Dynamics of neutrophil infiltration during cutaneous wound healing and infection using fluorescence imaging. The Journal of investigative dermatology 128: 1812-1820.
5. Lucas T, Waisman A, Ranjan R, Roes J, Krieg T, et al. (2010) Differential roles of macrophages in diverse phases of skin repair. Journal of immunology 184: 3964-3977.
6. Bellini A, Mattoli S, (2007) The role of the fibrocyte, a bone marrow-derived mesenchymal progenitor, in reactive and reparative fibroses. Laboratory investigation; a journal of technical methods and pathology 87: 858-870.
7. Blumbach K, Zweers MC, Brunner G, Peters AS, Schmitz M, et al. (2010) Defective granulation tissue formation in mice with specific ablation of integrin-linked kinase in fibroblasts- role of TGFbeta1 levels and RhoA activity. Journal of cell science 123: 3872-3883.
8. Gurtner GC, Werner S, Barrandon Y, Longaker MT, (2008) Wound repair and regeneration. Nature 453: 314-321.
9. Larson BJ, Longaker MT, Lorenz HP, (2010) Scarless fetal wound healing: a basic science review. Plastic and reconstructive surgery 126: 1172-1180.
10. Satish L, Blair HC, Glading A, Wells A, (2005) Interferon-inducible protein 9 (CXCL11)-induced cell motility in keratinocytes requires calcium flux-dependent activation of mu-calpain. Molecular and cellular biology 25: 1922-1941.
11. Franco SJ, Huttenlocher A, (2005) Regulating cell migration: calpains make the cut. Journal of cell science 118: 3829-3838.
12. Miyachi Y, Yoshimura N, Suzuki S, Hamakubo T, Kannagi R, et al. (1986) Biochemical demonstration and immunohistochemical localization of calpain in human skin. The Journal of investigative dermatology 86: 346-349.
13. Goll DE, Thompson VF, Li H, Wei W, Cong J, (2003) The calpain system. Physiological reviews 83: 731-801.
14. Undyala VV, Dembo M, Cembrola K, Perrin BJ, Huttenlocher A, et al. (2008) The calpain small subunit regulates cell-substrate mechanical interactions during fibroblast migration. Journal of cell science 121: 3581-3588.
15. Cuevas BD, Abell AN, Witowsky JA, Yujiri T, Johnson NL, et al. (2003) MEKK1 regulates calpain-dependent proteolysis of focal adhesion proteins for rear-end detachment of migrating fibroblasts. The EMBO journal 22: 3346-3355.
16. Chan KT, Bennin DA, Huttenlocher A, (2010) Regulation of adhesion dynamics by calpain-mediated proteolysis of focal adhesion kinase (FAK). The Journal of biological chemistry 285: 11418-11426.
17. Franco SJ, Rodgers MA, Perrin BJ, Han J, Bennin DA, et al. (2004) Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nature cell biology 6: 977-983.
18. Perrin BJ, Amann KJ, Huttenlocher A, (2006) Proteolysis of cortactin by calpain regulates membrane protrusion during cell migration. Molecular biology of the cell 17: 239-250.
19. Lebart MC, Benyamin Y, (2006) Calpain involvement in the remodeling of cytoskeletal anchorage complexes. The FEBS journal 273: 3415-3426.
20. Shumway SD, Maki M, Miyamoto S, (1999) The PEST domain of IkappaBalpha is necessary and sufficient for in vitro degradation by mu-calpain. The Journal of biological chemistry 274: 30874-30881.
21. Lokuta MA, Nuzzi PA, Huttenlocher A, (2003) Calpain regulates neutrophil chemotaxis. Proceedings of the National Academy of Sciences of the United States of America 100: 4006-4011.
22. Wiemer AJ, Lokuta MA, Surfus JC, Wernimont SA, Huttenlocher A, (2010) Calpain inhibition impairs TNF-alpha-mediated neutrophil adhesion, arrest and oxidative burst. Molecular immunology 47: 894-902.
23. Su Y, Cui Z, Li Z, Block ER, (2006) Calpain-2 regulation of VEGF-mediated angiogenesis. The FASEB journal: official publication of the Federation of American Societies for Experimental Biology 20: 1443-1451.
24. Youn JY, Wang T, Cai H, (2009) An ezrin/calpain/PI3K/AMPK/eNOSs1179 signaling cascade mediating VEGF-dependent endothelial nitric oxide production. Circulation research 104: 50-59.
25. Bodnar RJ, Yates CC, Wells A, (2006) IP-10 blocks vascular endothelial growth factor-induced endothelial cell motility and tube formation via inhibition of calpain. Circulation research 98: 617-625.
26. Glading A, Chang P, Lauffenburger DA, Wells A, (2000) Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway. The Journal of biological chemistry 275: 2390-2398.
27. Storr SJ, Carragher NO, Frame MC, Parr T, Martin SG, (2011) The calpain system and cancer. Nature reviews Cancer 11: 364-374.
28. Cuzzocrea S, McDonald MC, Mazzon E, Siriwardena D, Serraino I, et al. (2000) Calpain inhibitor I reduces the development of acute and chronic inflammation. The American journal of pathology 157: 2065-2079.
29. 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. Journal of the American Society of Nephrology: JASN 17: 3415-3423.
30. Liang B, Duan BY, Zhou XP, Gong JX, Luo ZG, (2010) Calpain activation promotes BACE1 expression, amyloid precursor protein processing, and amyloid plaque formation in a transgenic mouse model of Alzheimer disease. The Journal of biological chemistry 285: 27737-27744.
31. 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. Circulation research 102: 720-728.
32. Kamata Y, Taniguchi A, Yamamoto M, Nomura J, Ishihara K, et al. (2009) Neutral cysteine protease bleomycin hydrolase is essential for the breakdown of deiminated filaggrin into amino acids. The Journal of biological chemistry 284: 12829-12836.
33. Hsu CY, Henry J, Raymond AA, Mechin MC, Pendaries V, et al. (2011) Deimination of human filaggrin-2 promotes its proteolysis by calpain 1. The Journal of biological chemistry 286: 23222-23233.
34. Zhao R, Guan DW, Zhang W, Du Y, Xiong CY, et al. (2009) Increased expressions and activations of apoptosis-related factors in cell signaling during incised skin wound healing in mice: a preliminary study for forensic wound age estimation. Legal medicine 11 (Suppl 1): S155-160.
35. Khosrotehrani K, Nguyen Huu S, Prignon A, Avril MF, Boitier F, et al. (2011) Pregnancy promotes melanoma metastasis through enhanced lymphangiogenesis. The American journal of pathology 178: 1870-1880.
36. Arora PD, Narani N, McCulloch CA, (1999) The compliance of collagen gels regulates transforming growth factor-beta induction of alpha-smooth muscle actin in fibroblasts. The American journal of pathology 154: 871-882.
37. Lenga Y, Koh A, Perera AS, McCulloch CA, Sodek J, et al. (2008) Osteopontin expression is required for myofibroblast differentiation. Circulation research 102: 319-327.
38. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G, (1993) Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. The Journal of cell biology 122: 103-111.
39. Rolfe KJ, Irvine LM, Grobbelaar AO, Linge C, (2007) Differential gene expression in response to transforming growth factor-beta1 by fetal and postnatal dermal fibroblasts. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society 15: 897-906.
40. 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. Molecular and cellular biology 21: 2213-2220.
41. 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. The Journal of biological chemistry 274: 36891-36896.
42. Takano J, Tomioka M, Tsubuki S, Higuchi M, Iwata N, et al. (2005) Calpain mediates excitotoxic DNA fragmentation via mitochondrial pathways in adult brains: evidence from calpastatin mutant mice. The Journal of biological chemistry 280: 16175-16184.
43. Wilson L, Fathke C, Isik F, (2002) Tissue dispersion and flow cytometry for the cellular analysis of wound healing. BioTechniques 32: 548-551.
44. Badiavas EV, Abedi M, Butmarc J, Falanga V, Quesenberry P, (2003) Participation of bone marrow derived cells in cutaneous wound healing. Journal of cellular physiology 196: 245-250.
45. Noma H, Kato T, Fujita H, Kitagawa M, Yamano T, et al. (2009) Calpain inhibition induces activation of the distinct signalling pathways and cell migration in human monocytes. Immunology 128: e487-496.
46. Katsube M, Kato T, Kitagawa M, Noma H, Fujita H, et al. (2008) Calpain-mediated regulation of the distinct signaling pathways and cell migration in human neutrophils. Journal of leukocyte biology 84: 255-263.
47. Okuno Y, Nakamura-Ishizu A, Kishi K, Suda T, Kubota Y, (2011) Bone marrow-derived cells serve as pro-angiogenic macrophages but not endothelial cells in wound healing. Blood.
48. Hoang MV, Nagy JA, Fox JE, Senger DR, (2010) Moderation of calpain activity promotes neovascular integration and lumen formation during VEGF-induced pathological angiogenesis. PloS one 5: e13612.
49. Stramer BM, Mori R, Martin P, (2007) The inflammation-fibrosis link? A Jekyll and Hyde role for blood cells during wound repair. The Journal of investigative dermatology 127: 1009-1017.
50. Kuwahara F, Kai H, Tokuda K, Takeya M, Takeshita A, et al. (2004) Hypertensive myocardial fibrosis and diastolic dysfunction: another model of inflammation? Hypertension 43: 739-745.
51. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M, (2008) Growth factors and cytokines in wound healing. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society 16: 585-601.
52. Rodero MP, Khosrotehrani K, (2010) Skin wound healing modulation by macrophages. International journal of clinical and experimental pathology 3: 643-653.
53. Darby IA, Hewitson TD, (2007) Fibroblast differentiation in wound healing and fibrosis. International review of cytology 257: 143-179.
54. Farahani RM, Kloth LC, (2008) The hypothesis of 'biophysical matrix contraction': wound contraction revisited. International wound journal 5: 477-482.
55. Tabata C, Tabata R, Nakano T, (2010) The calpain inhibitor calpeptin prevents bleomycin-induced pulmonary fibrosis in mice. Clinical and experimental immunology 162: 560-567.
56. Burkard N, Becher J, Heindl C, Neyses L, Schuh K, et al. (2005) Targeted proteolysis sustains calcineurin activation. Circulation 111: 1045-1053.