Oxidative CaMKII as a potential target for inflammatory disease (Review)
- Authors:
- Jingjing Qu
- Quanhui Mei
- Ruichao Niu
-
Affiliations: Department of Lung Cancer and Gastroenterology, Hunan Cancer Hospital, Affiliated Tumor Hospital of Xiangya Medical School of Central South University, Changsha, Hunan 410008, P.R. China, Department of Intensive Care Unit, The First People's Hospital of Changde City, Changde, Hunan 410005, P.R. China, Department of Respiratory Medicine, Xiangya Hospital, Central South University, Changsha, Hunan 410008, P.R. China - Published online on: May 29, 2019 https://doi.org/10.3892/mmr.2019.10309
- Pages: 863-870
This article is mentioned in:
Abstract
 |
|
Hudmon A and Schulman H: Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J. 364:593–611. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Rosenberg OS, Deindl S, Sung RJ, Nairn AC and Kuriyan J: Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme. Cell. 123:849–860. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Erickson JR, He BJ, Grumbach IM and Anderson ME: CaMKII in the cardiovascular system: Sensing redox states. Physiol Rev. 91:889–915. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Stratton M, Lee IH, Bhattacharyya M, Christensen SM, Chao LH, Schulman H, Groves JT and Kuriyan J: Activation-triggered subunit exchange between CaMKII holoenzymes facilitates the spread of kinase activity. Elife. 3:e016102013. View Article : Google Scholar | |
|
Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O'Donnell SE, Aykin-Burns N, et al: A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell. 133:462–474. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Brookes PS, Yoon Y, Robotham JL, Anders MW and Sheu SS: Calcium, ATP, and ROS: A mitochondrial love-hate triangle. Am J Physiol Cell Physiol. 287:C817–C833. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Nickel AG, Kohlhaas M, Bertero E, Wilhelm D, Wagner M, Sequeira V, Kreusser MM, Dewenter M, Kappl R, Hoth M, et al: CaMKII does not control mitochondrial Ca2+ uptake in cardiac myocytes. J Physiol. Feb 16–2019.(Epub ahead of print). doi: 10.1113/JP276766. View Article : Google Scholar : PubMed/NCBI | |
|
Luo M, Guan X, Luczak ED, Lang D, Kutschke W, Gao Z, Yang J, Glynn P, Sossalla S, Swaminathan PD, et al: Diabetes increases mortality after myocardial infarction by oxidizing CaMKII. J Clin Invest. 123:1262–1274. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Sanders PN, Koval OM, Jaffer OA, Prasad AM, Businga TR, Scott JA, Hayden PJ, Luczak ED, Dickey DD, Allamargot C, et al: CaMKII is essential for the proasthmatic effects of oxidation. Sci Transl Med. 5:195ra972013. View Article : Google Scholar : PubMed/NCBI | |
|
Viatchenko-Karpinski S Kornyeyev D, El-Bizri N, Budas G, Fan P, Jiang Z, Yang J, Anderson ME, Shryock JC, Chang CP, et al: Intracellular Na+ overload causes oxidation of CaMKII and leads to Ca2+ mishandling in isolated ventricular myocytes. J Mol Cell Cardiol. 76:247–256. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Ho HT, Liu B, Snyder JS, Lou Q, Brundage EA, Velez-Cortes F, Wang H, Ziolo MT, Anderson ME, Sen CK, et al: Ryanodine receptor phosphorylation by oxidized CaMKII contributes to the cardiotoxic effects of cardiac glycosides. Cardiovasc Res. 101:165–174. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Singh MV, Swaminathan PD, Luczak ED, Kutschke W, Weiss RM and Anderson ME: MyD88 mediated inflammatory signaling leads to CaMKII oxidation, cardiac hypertrophy and death after myocardial infarction. J Mol Cell Cardiol. 52:1135–1144. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Swaminathan PD, Purohit A, Soni S, Voigt N, Singh MV, Glukhov AV, Gao Z, He BJ, Luczak ED, Joiner ML, et al: Oxidized CaMKII causes cardiac sinus node dysfunction in mice. J Clin Invest. 121:3277–3288. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
He BJ, Joiner ML, Singh MV, Luczak ED, Swaminathan PD, Koval OM, Kutschke W, Allamargot C, Yang J, Guan X, et al: Oxidation of CaMKII determines the cardiotoxic effects of aldosterone. Nat Med. 17:1610–1618. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Erickson JR, Pereira L, Wang L, Han G, Ferguson A, Dao K, Copeland RJ, Despa F, Hart GW, Ripplinger CM and Bers DM: Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature. 502:372–376. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Gutierrez DA, Fernandez-Tenorio M, Ogrodnik J and Niggli E: NO-dependent CaMKII activation during β-adrenergic stimulation of cardiac muscle. Cardiovasc Res. 100(392-401): 12013 | |
|
Coultrap SJ and Bayer KU: Nitric oxide induces Ca2+-independent activity of the Ca2+/calmodulin-dependent protein kinase II (CaMKII). J Biol Chem. 289:19458–19465. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Curran J, Tang L, Roof SR, Velmurugan S, Millard A, Shonts S, Wang H, Santiago D, Ahmad U, Perryman M, et al: Nitric oxide-dependent activation of CaMKII increases diastolic sarcoplasmic reticulum calcium release in cardiac myocytes in response to adrenergic stimulation. PLoS One. 9:e874952014. View Article : Google Scholar : PubMed/NCBI | |
|
Erickson JR, Nichols CB, Uchinoumi H, Stein ML, Bossuyt J and Bers DM: S-Nitrosylation induces both autonomous activation and inhibition of Calcium/Calmodulin-dependent protein kinase II δ. J Biol Chem. 290:25646–25656. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Yilmaz M, Gangopadhyay SS, Leavis P, Grabarek Z and Morgan KG: Phosphorylation at Ser26 in the ATP-binding site of Ca2+/calmodulin-dependent kinase II as a mechanism for switching off the kinase activity. Biosci Rep. 33:e000242013. View Article : Google Scholar : PubMed/NCBI | |
|
Tobimatsu T and Fujisawa H: Tissue-specific expression of four types of rat calmodulin-dependent protein kinase II mRNAs. J Biol Chem. 264:17907–17912. 1989.PubMed/NCBI | |
|
Tombes RM and Krystal GW: Identification of novel human tumor cell-specific CaMK-II variants. Biochim Biophys Acta. 1355:281–292. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Takaishi T, Saito N and Tanaka C: Evidence for distinct neuronal localization of gamma and delta subunits of Ca2+/calmodulin-dependent protein kinase II in the rat brain. J Neurochem. 58:1971–1974. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Bayer KU, Löhler J, Schulman H and Harbers K: Developmental expression of the CaM kinase II isoforms: Ubiquitous gamma- and delta-CaM kinase II are the early isoforms and most abundant in the developing nervous system. Brain Res Mol Brain Res. 70:147–154. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Kim I, Je HD, Gallant C, Zhan Q, Riper DV, Badwey JA, Singer HA and Morgan KG: Ca2+-calmodulin-dependent protein kinase II-dependent activation of contractility in ferret aorta. J Physiol. 526:367–374. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Gangopadhyay SS, Barber AL, Gallant C, Grabarek Z, Smith JL and Morgan KG: Differential functional properties of calmodulin-dependent protein kinase IIgamma variants isolated from smooth muscle. Biochem J. 372:347–357. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Marganski WA, Gangopadhyay SS, Je HD, Gallant C and Morgan KG: Targeting of a novel Ca+2/calmodulin-dependent protein kinase II is essential for extracellular signal-regulated kinase-mediated signaling in differentiated smooth muscle cells. Circ Res. 97:541–549. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Guo T, Zhang T, Ginsburg KS, Mishra S, Brown JH and Bers DM: CaMKIIδC slows Ca]i decline in cardiac myocytes by promoting Ca sparks. Biophys J. 102:2461–2470. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Mishra S, Ling H, Grimm M, Zhang T, Bers DM and Brown JH: Cardiac hypertrophy and heart failure development through Gq and CaM kinase II signaling. J Cardiovasc Pharmacol. 56:598–603. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Singh MV, Kapoun A, Higgins L, Kutschke W, Thurman JM, Zhang R, Singh M, Yang J, Guan X, Lowe JS, et al: Ca2+/calmodulin-dependent kinase II triggers cell membrane injury by inducing complement factor B gene expression in the mouse heart. J Clin Invest. 119:986–996. 2009.PubMed/NCBI | |
|
Crack PJ, Taylor JM, Ali U, Mansell A and Hertzog PJ: Potential contribution of NF-kappaB in neuronal cell death in the glutathione peroxidase-1 knockout mouse in response to ischemia-reperfusion injury. Stroke. 37:1533–1538. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Gu SX, Blokhin IO, Wilson KM, Dhanesha N, Doddapattar P, Grumbach IM, Chauhan AK and Lentz SR: Protein methionine oxidation augments reperfusion injury in acute ischemic stroke. JCI Insight. 1(pii): e864602016.PubMed/NCBI | |
|
Kimura W, Muralidhar S, Canseco DC, Puente B, Zhang CC, Xiao F, Abderrahman YH and Sadek HA: Redox signaling in cardiac renewal. Antioxid Redox Signal. 21:1660–1673. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Fraccarollo D, Galuppo P, Neuser J, Bauersachs J and Widder JD: Pentaerythritol tetranitrate targeting myocardial reactive oxygen species production improves left ventricular remodeling and function in rats with ischemic heart failure. Hypertension. 66:978–987. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Frantz S, Brandes RP, Hu K, Rammelt K, Wolf J, Scheuermann H, Ertl G and Bauersachs J: Left ventricular remodeling after myocardial infarction in mice with targeted deletion of the NADPH oxidase subunit gp91PHOX. Basic Res Cardiol. 101:127–132. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Murdoch CE, Zhang M, Cave AC and Shah AM: NADPH oxidase-dependent redox signalling in cardiac hypertrophy, remodelling and failure. Cardiovasc Res. 71:208–215. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Purohit A, Rokita AG, Guan X, Chen B, Koval OM, Voigt N, Neef S, Sowa T, Gao Z, Luczak ED, et al: Oxidized Ca(2+)/calmodulin-dependent protein kinase II triggers atrial fibrillation. Circulation. 128:1748–1757. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Wagner S, Ruff HM, Weber SL, Bellmann S, Sowa T, Schulte T, Anderson ME, Grandi E, Bers DM, Backs J, et al: Reactive oxygen species-activated Ca/calmodulin kinase IIδ is required for late I(Na) augmentation leading to cellular Na and Ca overload. Circ Res. 108:555–565. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Zhu LJ, Klutho PJ, Scott JA, Xie L, Luczak ED, Dibbern ME, Prasad AM, Jaffer OA, Venema AN, Nguyen EK, et al: Oxidative activation of the Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) regulates vascular smooth muscle migration and apoptosis. Vascul Pharmacol. 60:75–83. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Scott JA, Xie L, Li H, Li W, He JB, Sanders PN, Carter AB, Backs J, Anderson ME and Grumbach IM: The multifunctional Ca2+/calmodulin-dependent kinase II regulates vascular smooth muscle migration through matrix metalloproteinase 9. Am J Physiol Heart Circ Physiol. 302:H1953–H1964. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Rajtik T, Carnicka S, Szobi A, Giricz Z, O-Uchi J, Hassova V, Svec P, Ferdinandy P, Ravingerova T and Adameova A: Oxidative activation of CaMKIIδ in acute myocardial ischemia/reperfusion injury: A role of angiotensin AT1 receptor-NOX2 signaling axis. Eur J Pharmacol. 771:114–122. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA and Nathan DM: Reduction in the incidence of type 2 diabetes with lifestyle intervention or met-formin. N Engl J Med. 346:393–403. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Donahoe SM, Stewart GC, McCabe CH, Mohanavelu S, Murphy SA, Cannon CP and Antman EM: Diabetes and mortality following acute coronary syndromes. JAMA. 298:765–775. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Chai S, Qian Y, Tang J, Liang Z, Zhang M, Si J, Li X, Huang W, Xu R and Wang K: Retracted: Ca(2+)/calmodulin-dependent protein kinase IIγ, a critical mediator of the NF-κB network, is a novel therapeutic target in non-small cell lung cancer. Cancer Lett. 344:119–128. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Britschgi A, Bill A, Brinkhaus H, Rothwell C, Clay I, Duss S, Rebhan M, Raman P, Guy CT, Wetzel K, et al: Calcium-activated chloride channel ANO1 promotes breast cancer progression by activating EGFR and CAMK signaling. Proc Natl Acad Sci USA. 110:E1026–E1034. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Kim JH, Kim TW and Kim SJ: Downregulation of ARFGEF1 and CAMK2B by promoter hypermethylation in breast cancer cells. BMB Rep. 44:523–528. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Wang T, Guo S, Liu Z, Wu L, Li M, Yang J, Chen R, Liu X, Xu H, Cai S, et al: CAMK2N1 inhibits prostate cancer progression through androgen receptor-dependent signaling. Oncotarget. 5:10293–10306. 2014.PubMed/NCBI | |
|
Wang C, Li N, Liu X, Zheng Y and Cao X: A novel endogenous human CaMKII inhibitory protein suppresses tumor growth by inducing cell cycle arrest via p27 stabilization. J Biol Chem. 283:11565–11574. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Jing Z, Sui X, Yao J, Xie J, Jiang L, Zhou Y, Pan H and Han W: SKF-96365 activates cytoprotective autophagy to delay apoptosis in colorectal cancer cells through inhibition of the calcium/CaMKIIγ/AKT-mediated pathway. Cancer Lett. 372:226–238. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Bhat PJ, Darunte L, Kareenhalli V, Dandekar J and Kumar A: Can metabolic plasticity be a cause for cancer? Warburg-Waddington legacy revisited. Clin Epigenetics. 2:113–122. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Hart PC, Mao M, de Abreu AL, Ansenberger-Fricano K, Ekoue DN, Ganini D, Kajdacsy-Balla A, Diamond AM, Minshall RD, Consolaro ME, et al: MnSOD upregulation sustains the Warburg effect via mitochondrial ROS and AMPK-dependent signalling in cancer. Nat Commun. 6:60532015. View Article : Google Scholar : PubMed/NCBI | |
|
Kirkham P and Rahman I: Oxidative stress in asthma and COPD: Antioxidants as a therapeutic strategy. Pharmacol Ther. 111:476–494. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Jaffer OA, Carter AB, Sanders PN, Dibbern ME, Winters CJ, Murthy S, Ryan AJ, Rokita AG, Prasad AM, Zabner J, et al: Mitochondrial-targeted antioxidant therapy decreases transforming growth factor-β-mediated collagen production in a murine asthma model. Am J Respir Cell Mol Biol. 52:106–115. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Anandan C, Nurmatov U, van Schayck OC and Sheikh A: Is the prevalence of asthma declining? Systematic review of epidemiological studies. Allergy. 65:152–167. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Lambrecht BN and Hammad H: The immunology of asthma. Nat Immunol. 16:45–56. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Huang SK, Zhang Q, Qiu Z and Chung KF: Mechanistic impact of outdoor air pollution on asthma and allergic diseases. J Thorac Dis. 7:23–33. 2015.PubMed/NCBI | |
|
Casalino-Matsuda SM, Monzón ME and Forteza RM: Epidermal growth factor receptor activation by epidermal growth factor mediates oxidant-induced goblet cell metaplasia in human airway epithelium. Am J Respir Cell Mol Biol. 34:581–591. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Abdala-Valencia H, Earwood J, Bansal S, Jansen M, Babcock G, Garvy B, Wills-Karp M and Cook-Mills JM: Nonhematopoietic NADPH oxidase regulation of lung eosinophilia and airway hyperresponsiveness in experimentally induced asthma. Am J Physiol Lung Cell Mol Physiol. 292:L1111–L1125. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Spinelli AM, Liu Y, Sun LY, González-Cobos JC, Backs J, Trebak M and Singer HA: Smooth muscle CaMKIIδ promotes allergen-induced airway hyper-responsiveness and inflammation. Pflugers Arch. 467:2541–2554. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Li JM, Mullen AM, Yun S, Wientjes F, Brouns GY, Thrasher AJ and Shah AM: Essential role of the NADPH oxidase subunit p47(phox) in endothelial cell superoxide production in response to phorbol ester and tumor necrosis factor-alpha. Circ Res. 90:143–150. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Ikeda RK, Nayar J, Cho JY, Miller M, Rodriguez M, Raz E and Broide DH: Resolution of airway inflammation following ovalbumin inhalation: Comparison of ISS DNA and corticosteroids. Am J Respir Cell Mol Biol. 28:655–663. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Anderson ME: Oxidant stress promotes disease by activating CaMKII. J Mol Cell Cardiol. 89:160–167. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Fujisawa T, Velichko S, Thai P, Hung LY, Huang F and Wu R: Regulation of airway MUC5AC expression by IL-1beta and IL-17A; the NF-kappaB paradigm. J Immunol. 183:6236–6243. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Qu J, Do DC, Zhou Y, Luczak E, Mitzner W, Anderson ME and Gao P: Oxidized CaMKII promotes asthma through the activation of mast cells. JCI Insight. 2:e901392017. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou Y, Tung HY, Tsai YM, Hsu SC, Chang HW, Kawasaki H, Tseng HC, Plunkett B, Gao P, Hung CH, et al: Aryl hydrocarbon receptor controls murine mast cell homeostasis. Blood. 121:3195–3204. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Mahdavinia M, Suh LA, Carter RG, Stevens WW, Norton JE, Kato A, Tan BK, Kern RC, Conley DB, Chandra R, et al: Increased noneosinophilic nasal polyps in chronic rhinosinusitis in US second-generation Asians suggest genetic regulation of eosinophilia. J Allergy Clin Immunol. 135:576–579. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Totlandsdal AI, Cassee FR, Schwarze P, Refsnes M and Låg M: Diesel exhaust particles induce CYP1A1 and pro-inflammatory responses via differential pathways in human bronchial epithelial cells. Part Fibre Toxicol. 7:412010. View Article : Google Scholar : PubMed/NCBI | |
|
Manners S, Alam R, Schwartz DA and Gorska MM: A mouse model links asthma susceptibility to prenatal exposure to diesel exhaust. J Allergy Clin Immunol. 134:63–72. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Wang H, Do DC, Liu J, Wang B, Qu J, Ke X, Luo X, Tang HM, Tang HL, Hu C, et al: Functional role of kynurenine and aryl hydrocarbon receptor axis in chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol. 141:586–600.e6. 2018. View Article : Google Scholar : PubMed/NCBI |
