Critical role of calpain in inflammation (Review)

Saez ME, Ramirez-Lorca R, Moron FJ and Ruiz A: The therapeutic potential of the calpain family: New aspects. Drug Discov Today. 11:917–923. 2006. View Article : Google Scholar : PubMed/NCBI

Perrin BJ and Huttenlocher A: Calpain. Int J Biochem Cell Biol. 34:722–725. 2002. View Article : Google Scholar : PubMed/NCBI

Goll DE, Thompson VF, Li H, Wei W and Cong J: The calpain system. Physiol Rev. 83:731–801. 2003. View Article : Google Scholar : PubMed/NCBI

Medzhitov R: Inflammation 2010: New adventures of an old flame. Cell. 140:771–776. 2010. View Article : Google Scholar : PubMed/NCBI

Cuzzocrea S, McDonald MC, Mazzon E, Siriwardena D, Serraino I, Dugo L, Britti D, Mazzullo G, Caputi AP and Thiemermann C: Calpain inhibitor I reduces the development of acute and chronic inflammation. Am J Pathol. 157:2065–2079. 2000. View Article : Google Scholar : PubMed/NCBI

Ruetten H and Thiemermann C: Effect of calpain inhibitor I, an inhibitor of the proteolysis of I kappa B, on the circulatory failure and multiple organ dysfunction caused by endotoxin in the rat. Br J Pharmacol. 121:695–704. 1997. View Article : Google Scholar : PubMed/NCBI

Shumway SD, Maki M and Miyamoto S: The PEST domain of IkappaBalpha is necessary and sufficient for in vitro degradation by mu-calpain. J Biol Chem. 274:30874–30881. 1999. View Article : Google Scholar : PubMed/NCBI

Sun Z and Andersson R: NF-kappaB activation and inhibition: A review. Shock. 18:99–106. 2002. View Article : Google Scholar : PubMed/NCBI

Huang Z, Hoffmann FW, Norton RL, Hashimoto AC and Hoffmann PR: Selenoprotein K is a novel target of m-calpain, and cleavage is regulated by Toll-like receptor-induced calpastatin in macrophages. J Biol Chem. 286:34830–34838. 2011. View Article : Google Scholar : PubMed/NCBI

Fettucciari K, Quotadamo F, Noce R, Palumbo C, Modesti A, Rosati E, Mannucci R, Bartoli A and Marconi P: Group B Streptococcus (GBS) disrupts by calpain activation the actin and microtubule cytoskeleton of macrophages. Cell Microbiol. 13:859–884. 2011. View Article : Google Scholar : PubMed/NCBI

Fettucciari K, Fetriconi I, Mannucci R, Nicoletti I, Bartoli A, Coaccioli S and Marconi P: Group B Streptococcus induces macrophage apoptosis by calpain activation. J Immunol. 176:7542–7556. 2006. View Article : Google Scholar : PubMed/NCBI

Goldmann O, Sastalla I, Wos-Oxley M, Rohde M and Medina E: Streptococcus pyogenes induces oncosis in macrophages through the activation of an inflammatory programmed cell death pathway. Cell Microbiol. 11:138–155. 2009. View Article : Google Scholar : PubMed/NCBI

Lim YJ, Choi HH, Choi JA, Jeong JA, Cho SN, Lee JH, Park JB, Kim HJ and Song CH: Mycobacterium kansasii-induced death of murine macrophages involves endoplasmic reticulum stress responses mediated by reactive oxygen species generation or calpain activation. Apoptosis. 18:150–159. 2013. View Article : Google Scholar : PubMed/NCBI

Rana T, Misra S, Mittal MK, Farrow AL, Wilson KT, Linton MF, Fazio S, Willis IM and Chaudhuri G: Mechanism of down-regulation of RNA polymerase III-transcribed non-coding RNA genes in macrophages by Leishmania. J Biol Chem. 286:6614–6626. 2011. View Article : Google Scholar : PubMed/NCBI

Lokuta MA, Nuzzi PA and Huttenlocher A: Calpain regulates neutrophil chemotaxis. Proc Natl Acad Sci USA. 100:4006–4011. 2003. View Article : Google Scholar : PubMed/NCBI

Katsube M, Kato T, Kitagawa M, Noma H, Fujita H and Kitagawa S: Calpain-mediated regulation of the distinct signaling pathways and cell migration in human neutrophils. J Leukoc Biol. 84:255–263. 2008. View Article : Google Scholar : PubMed/NCBI

Dewitt S, Francis RJ and Hallett MB: Ca²⁺ and calpain control membrane expansion during the rapid cell spreading of neutrophils. J. Cell Sci. 126:4627–4635. 2013. View Article : Google Scholar : PubMed/NCBI

Dewitt S and Hallett M: Leukocyte membrane ‘expansion’: A central mechanism for leukocyte extravasation. J Leukoc Biol. 81:1160–1164. 2007. View Article : Google Scholar : PubMed/NCBI

Squier MK, Sehnert AJ, Sellins KS, Malkinson AM, Takano E and Cohen JJ: Calpain and calpastatin regulate neutrophil apoptosis. J Cell Physiol. 178:311–319. 1999. View Article : Google Scholar : PubMed/NCBI

Francis RJ, Kotecha S and Hallett MB: Ca²⁺ activation of cytosolic calpain induces the transition from apoptosis to necrosis in neutrophils with externalized phosphatidylserine. J Leukoc Biol. 93:95–100. 2013. View Article : Google Scholar : PubMed/NCBI

Deshpande RV, Goust JM, Chakrabarti AK, Barbosa E, Hogan EL and Banik NL: Calpain expression in lymphoid cells. Increased mRNA and protein levels after cell activation. J Biol Chem. 270:2497–2505. 1995. View Article : Google Scholar : PubMed/NCBI

Smith AW, Doonan BP, Tyor WR, Abou-Fayssal N, Haque A and Banik NL: Regulation of Th1/Th17 cytokines and IDO gene expression by inhibition of calpain in PBMCs from MS patients. J Neuroimmunol. 232:179–185. 2011. View Article : Google Scholar : PubMed/NCBI

Iguchi-Hashimoto M, Usui T, Yoshifuji H, Shimizu M, Kobayashi S, Ito Y, Murakami K, Shiomi A, Yukawa N, Kawabata D, et al: Overexpression of a minimal domain of calpastatin suppresses IL-6 production and Th17 development via reduced NF-κB and increased STAT5 signals. PLoS One. 6:e270202011. View Article : Google Scholar : PubMed/NCBI

Stewart MP, McDowall A and Hogg N: LFA-1-mediated adhesion is regulated by cytoskeletal restraint and by a Ca²⁺-dependent protease, calpain. J Cell Biol. 140:699–707. 1998. View Article : Google Scholar : PubMed/NCBI

Svensson L, McDowall A, Giles KM, Stanley P, Feske S and Hogg N: Calpain 2 controls turnover of LFA-1 adhesions on migrating T lymphocytes. PLoS One. 5:e150902010. View Article : Google Scholar : PubMed/NCBI

Hussain AM, Zhang QX and Murray AG: Endothelial cell calpain activity facilitates lymphocyte diapedesis. Am J Transplant. 5:2640–2648. 2005. View Article : Google Scholar : PubMed/NCBI

Mikosik A, Foerster J, Jasiulewicz A, Frąckowiak J, Colonna-Romano G, Bulati M, Buffa S, Martorana A, Caruso C, Bryl E, et al: Expression of calpain-calpastatin system (CCS) member proteins in human lymphocytes of young and elderly individuals; pilot baseline data for the CALPACENT project. Immun Ageing. 10:272013. View Article : Google Scholar : PubMed/NCBI

Kobayashi Y, Yamamoto K, Saido T, Kawasaki H, Oppenheim JJ and Matsushima K: Identification of calcium-activated neutral protease as a processing enzyme of human interleukin 1 alpha. Proc Natl Acad Sci USA. 87:5548–5552. 1990. View Article : Google Scholar : PubMed/NCBI

Zheng Y, Humphry M, Maguire JJ, Bennett MR and Clarke MCH: Intracellular interleukin-1 receptor 2 binding prevents cleavage and activity of interleukin-1α, controlling necrosis-induced sterile inflammation. Immunity. 38:285–295. 2013. View Article : Google Scholar : PubMed/NCBI

McCarthy DA, Ranganathan A, Subbaram S, Flaherty NL, Patel N, Trebak M, Hempel N and Melendez JA: Redox-control of the alarmin, Interleukin-1α. Redox Biol. 1:218–225. 2013. View Article : Google Scholar : PubMed/NCBI

Pan HC, Yang CN, Hung YW, Lee WJ, Tien HR, Shen CC, Sheehan J, Chou CT and Sheu ML: Reciprocal modulation of C/EBP-α and C/EBP-β by IL-13 in activated microglia prevents neuronal death. Eur J Immunol. 43:2854–2865. 2013. View Article : Google Scholar : PubMed/NCBI

Han Y, Weinman S, Boldogh I, Walker RK and Brasier AR: 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. 274:787–794. 1999. View Article : Google Scholar : PubMed/NCBI

Averna M, Stifanese R, De Tullio R, Salamino F, Bertuccio M, Pontremoli S and Melloni E: Proteolytic degradation of nitric oxide synthase isoforms by calpain is modulated by the expression levels of HSP90. FEBS J. 274:6116–6127. 2007. View Article : Google Scholar : PubMed/NCBI

Bellocq A, Doublier S, Suberville S, Perez J, Escoubet B, Fouqueray B, Puyol DR and Baud L: Somatostatin increases glucocorticoid binding and signaling in macrophages by blocking the calpain-specific cleavage of Hsp 90. J Biol Chem. 274:36891–36896. 1999. View Article : Google Scholar : PubMed/NCBI

Li X, Luo R, Jiang R, Meng X, Wu X, Zhang S and Hua W: The role of the Hsp90/Akt pathway in myocardial calpain-induced caspase-3 activation and apoptosis during sepsis. BMC Cardiovasc Disord. 13:82013. View Article : Google Scholar : PubMed/NCBI

Stalker TJ, Gong Y and Scalia R: The calcium-dependent protease calpain causes endothelial dysfunction in type 2 diabetes. Diabetes. 54:1132–1140. 2005. View Article : Google Scholar : PubMed/NCBI

Letavernier E, Perez J, Bellocq A, Mesnard L, de Castro Keller A, Haymann JP and Baud L: Targeting the calpain/calpastatin system as a new strategy to prevent cardiovascular remodeling in angiotensin II-induced hypertension. Circ Res. 102:720–728. 2008. View Article : Google Scholar : PubMed/NCBI

Zhao Y, Malinin NL, Meller J, Ma Y, West XZ, Bledzka K, Qin J, Podrez EA and Byzova TV: Regulation of cell adhesion and migration by Kindlin-3 cleavage by calpain. J Biol Chem. 287:40012–40020. 2012. View Article : Google Scholar : PubMed/NCBI

Franco SJ and Huttenlocher A: Regulating cell migration: Calpains make the cut. J Cell Sci. 118:3829–3838. 2005. View Article : Google Scholar : PubMed/NCBI

Cortesio CL, Boateng LR, Piazza TM, Bennin DA and Huttenlocher A: Calpain-mediated proteolysis of paxillin negatively regulates focal adhesion dynamics and cell migration. J Biol Chem. 286:9998–10006. 2011. View Article : Google Scholar : PubMed/NCBI

Cui Z, Han Z, Li Z, Hu H, Patel JM, Antony V, Block ER and Su Y: Involvement of calpain-calpastatin in cigarette smoke-induced inhibition of lung endothelial nitric oxide synthase. Am J Respir Cell Mol Biol. 33:513–520. 2005. View Article : Google Scholar : PubMed/NCBI

Dong Y, Wu Y, Wu M, Wang S, Zhang J, Xie Z, Xu J, Song P, Wilson K, Zhao Z, et al: Activation of protease calpain by oxidized and glycated LDL increases the degradation of endothelial nitric oxide synthase. J Cell Mol Med 13 (no. 9A). 2899–2910. 2009. View Article : Google Scholar

Wang S, Peng Q, Zhang J and Liu L: Na⁺/H⁺ exchanger is required for hyperglycaemia-induced endothelial dysfunction via calcium-dependent calpain. Cardiovasc Res. 80:255–262. 2008. View Article : Google Scholar : PubMed/NCBI

Nathan C and Ding A: Nonresolving inflammation. Cell. 140:871–882. 2010. View Article : Google Scholar : PubMed/NCBI

Bergounioux J, Elisee R, Prunier A-L, Donnadieu F, Sperandio B, Sansonetti P and Arbibe L: Calpain activation by the Shigella flexneri effector VirA regulates key steps in the formation and life of the bacterium's epithelial niche. Cell Host Microbe. 11:240–252. 2012. View Article : Google Scholar : PubMed/NCBI

Smani Y, Docobo-Pérez F, McConnell MJ and Pachón J: Acinetobacter baumannii-induced lung cell death: Role of inflammation, oxidative stress and cytosolic calcium. Microb Pathog. 50:224–232. 2011. View Article : Google Scholar : PubMed/NCBI

Li M, Wang X, Yu Y, Yu Y, Xie Y, Zou Y, Ge J, Peng T and Chen R: Coxsackievirus B3-induced calpain activation facilitates the progeny virus replication via a likely mechanism related with both autophagy enhancement and apoptosis inhibition in the early phase of infection: An in vitro study in H9c2 cells. Virus Res. 179:177–186. 2014. View Article : Google Scholar : PubMed/NCBI

Liu D, Yan Z, Minshall RD, Schwartz DE, Chen Y and Hu G: Activation of calpains mediates early lung neutrophilic inflammation in ventilator-induced lung injury. Am J Physiol Lung Cell Mol Physiol. 302:L370–L379. 2012. View Article : Google Scholar : PubMed/NCBI

Celes MRN, Malvestio LM, Suadicani SO, Prado CM, Figueiredo MJ, Campos EC, Freitas ACS, Spray DC, Tanowitz HB, da Silva JS, et al: Disruption of calcium homeostasis in cardiomyocytes underlies cardiac structural and functional changes in severe sepsis. PLoS One. 8:e688092013. View Article : Google Scholar : PubMed/NCBI

Li X, Li Y, Shan L, Shen E, Chen R and Peng T: Over-expression of calpastatin inhibits calpain activation and attenuates myocardial dysfunction during endotoxaemia. Cardiovasc Res. 83:72–79. 2009. View Article : Google Scholar : PubMed/NCBI

Smith IJ, Lecker SH and Hasselgren P-O: Calpain activity and muscle wasting in sepsis. Am J Physiol Endocrinol Metab. 295:E762–E771. 2008. View Article : Google Scholar : PubMed/NCBI

Hu H, Li X, Li Y, Wang L, Mehta S, Feng Q, Chen R and Peng T: Calpain-1 induces apoptosis in pulmonary microvascular endothelial cells under septic conditions. Microvasc Res. 78:33–39. 2009. View Article : Google Scholar : PubMed/NCBI

Supinski GS, Wang W and Callahan LA: Caspase and calpain activation both contribute to sepsis-induced diaphragmatic weakness. J Appl Physiol. 107:1389–1396. 2009. View Article : Google Scholar : PubMed/NCBI

Wei W, Fareed MU, Evenson A, Menconi MJ, Yang H, Petkova V and Hasselgren PO: Sepsis stimulates calpain activity in skeletal muscle by decreasing calpastatin activity but does not activate caspase-3. Am J Physiol Regul Integr Comp Physiol. 288:R580–R590. 2005. View Article : Google Scholar : PubMed/NCBI

Kraemer BF, Campbell RA, Schwertz H, Franks ZG, de Abreu A Vieira, Grundler K, Kile BT, Dhakal BK, Rondina MT, Kahr WHA, et al: Bacteria differentially induce degradation of Bcl-xL, a survival protein, by human platelets. Blood. 120:5014–5020. 2012. View Article : Google Scholar : PubMed/NCBI

Zafrani L, Gerotziafas G, Byrnes C, Hu X, Perez J, Lévi C, Placier S, Letavernier E, Leelahavanichkul A, Haymann JP, et al: Calpastatin controls polymicrobial sepsis by limiting procoagulant microparticle release. Am J Respir Crit Care Med. 185:744–755. 2012. View Article : Google Scholar : PubMed/NCBI

Kumar V, Everingham S, Hall C, Greer PA and Craig AWB: Calpains promote neutrophil recruitment and bacterial clearance in an acute bacterial peritonitis model. Eur J Immunol. 44:831–841. 2014. View Article : Google Scholar : PubMed/NCBI

Samantaray S, Knaryan VH, Shields DC and Banik NL: Critical role of calpain in spinal cord degeneration in Parkinson's disease. J Neurochem. 127:880–890. 2013. View Article : Google Scholar : PubMed/NCBI

Smolock AR, Mishra G, Eguchi K, Eguchi S and Scalia R: Protein kinase C upregulates intercellular adhesion molecule-1 and leukocyte-endothelium interactions in hyperglycemia via activation of endothelial expressed calpain. Arterioscler Thromb Vasc Biol. 31:289–296. 2011. View Article : Google Scholar : PubMed/NCBI

Loot AE, Pierson I, Syzonenko T, Elgheznawy A, Randriamboavonjy V, Zivković A, Stark H and Fleming I: Ca²⁺-sensing receptor cleavage by calpain partially accounts for altered vascular reactivity in mice fed a high-fat diet. J Cardiovasc Pharmacol. 61:528–535. 2013. View Article : Google Scholar : PubMed/NCBI

Chen B, Zhao Q, Ni R, Tang F, Shan L, Cepinskas I, Cepinskas G, Wang W, Schiller PW and Peng T: Inhibition of calpain reduces oxidative stress and attenuates endothelial dysfunction in diabetes. Cardiovasc Diabetol. 13:882014. View Article : Google Scholar : PubMed/NCBI

Li Y, Arnold JMO, Pampillo M, Babwah AV and Peng T: Taurine prevents cardiomyocyte death by inhibiting NADPH oxidase-mediated calpain activation. Free Radic Biol Med. 46:51–61. 2009. View Article : Google Scholar : PubMed/NCBI

Shan L, Li J, Wei M, Ma J, Wan L, Zhu W, Li Y, Zhu H, Arnold JMO and Peng T: Disruption of Rac1 signaling reduces ischemia-reperfusion injury in the diabetic heart by inhibiting calpain. Free Radic Biol Med. 49:1804–1814. 2010. View Article : Google Scholar : PubMed/NCBI

Li Y, Li Y, Feng Q, Arnold M and Peng T: Calpain activation contributes to hyperglycaemia-induced apoptosis in cardiomyocytes. Cardiovasc Res. 84:100–110. 2009. View Article : Google Scholar : PubMed/NCBI

Scalia R, Gong Y, Berzins B, Freund B, Feather D, Landesberg G and Mishra G: A novel role for calpain in the endothelial dysfunction induced by activation of angiotensin II type 1 receptor signaling. Circ Res. 108:1102–1111. 2011. View Article : Google Scholar : PubMed/NCBI

Ma J, Wei M, Wang Q, Li J, Wang H, Liu W, Lacefield JC, Greer PA, Karmazyn M, Fan GC, et al: Deficiency of Capn4 gene inhibits nuclear factor-κB (NF-κB) protein signaling/inflammation and reduces remodeling after myocardial infarction. J Biol Chem. 287:27480–27489. 2012. View Article : Google Scholar : PubMed/NCBI

Li Y, Ma J, Zhu H, Singh M, Hill D, Greer PA, Arnold JM, Abel ED and Peng T: Targeted inhibition of calpain reduces myocardial hypertrophy and fibrosis in mouse models of type 1 diabetes. Diabetes. 60:2985–2994. 2011. View Article : Google Scholar : PubMed/NCBI

Aich J, Mabalirajan U, Ahmad T, Agrawal A and Ghosh B: Loss-of-function of inositol polyphosphate-4-phosphatase reversibly increases the severity of allergic airway inflammation. Nat Commun. 3:8772012. View Article : Google Scholar : PubMed/NCBI

Morita M, Banno Y, Dohjima T, Nozawa S, Fushimi K, Fan DG, Ohno T, Miyazawa K, Liu N and Shimizu K: Mu-calpain is involved in the regulation of TNF-alpha-induced matrix metalloproteinase-3 release in a rheumatoid synovial cell line. Biochem Biophys Res Commun. 343:937–942. 2006. View Article : Google Scholar : PubMed/NCBI

Chakrabarti S, Rizvi M, Morin K, Garg R and Freedman JE: The role of CD40L and VEGF in the modulation of angiogenesis and inflammation. Vascul Pharmacol. 53:130–137. 2010. View Article : Google Scholar : PubMed/NCBI

Wang Y, Zheng D, Wei M, Ma J, Yu Y, Chen R, Lacefield JC, Xu H and Peng T: Over-expression of calpastatin aggravates cardiotoxicity induced by doxorubicin. Cardiovasc Res. 98:381–390. 2013. View Article : Google Scholar : PubMed/NCBI