Roles of TRPM7 in Renal Ischemia-Reperfusion Injury

Author(s): Aifen Liu , Bin Yang* .

Journal Name: Current Protein & Peptide Science

Volume 20 , Issue 8 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Ischemia-reperfusion injury (IRI) is a major cause of acute kidney injury (AKI) that is a global health concern associated with high morbidity and mortality. So far, no specific interventions limit injury or improve recovery and survival. Transient receptor potential melastatin 7 (TRPM7), a bifunctional membrane protein, plays key roles in inflammation and cell death. However, the precise role and underlying mechanism of TRPM7 in IR-induced AKI have not been well defined. Herein, we reviewed the structure and function of TRPM7 as a non-selective ion channel, but Ca2+ and Mg2+-conducting, that mediated the elevation of cytosolic Ca2+ and Mg2+. We then comprehensively reviewed the mechanism of TRPM7 involved in the pathophysiology of renal IRI, including inflammatory response, apoptosis and necroptosis, renal microvasculature, as well as maladaptive fibrogenesis leading to chronic kidney disease (CKD). Our previous study has shown that the dynamic change and underlying mechanism of TRPM7 involving in inflammation and apoptosis in in vitro hypoxia/reoxygenation and in vivo renal IRI models. The association between TRPM7, inflammatory response and apoptosis, as well as related caspase-3, HMGB1 and Bax/Bcl-2 ratio, was also discussed. Disclosing the involvement of TRPM7 in renal IRI might provide new mechanistic insights for a potential biomarker as diagnostic and therapeutic target of AKI.

Keywords: TRPM7, ischemia-reperfusion injury, kidney, inflammation, apoptosis, necroptosis, fibrosis.

[1]
Yang, L.; Xing, G.; Wang, L.; Wu, Y.; Li, S.; Xu, G.; He, Q.; Chen, J.; Chen, M.; Liu, X.; Zhu, Z.; Yang, L.; Lian, X.; Ding, F.; Li, Y.; Wang, H.; Wang, J.; Wang, R.; Mei, C.; Xu, J.; Li, R.; Cao, J.; Zhang, L.; Wang, Y.; Xu, J.; Bao, B.; Liu, B.; Chen, H.; Li, S.; Zha, Y.; Luo, Q.; Chen, D.; Shen, Y.; Liao, Y.; Zhang, Z.; Wang, X.; Zhang, K.; Liu, L.; Maeleto, P.; Guo, C.; Li, J.; Wang, Z.; Bai, S.; Shi, S.; Wang, Y.; Wang, J.; Liu, Z.; Wang, F.; Huang, D.; Wang, S.; Ge, S.; Shen, Q.; Zhang, P.; Wu, L.; Pan, M.; Zou, X.; Zhu, P.; Zhao, J.; Zhou, M.; Yang, L.; Hu, W.; Wang, J.; Liu, B.; Zhang, T.; Han, J.; Wen, T.; Zhao, M.; Wang, H. ISN AKF 0by25 China Consortiums. Acute kidney injury in China: A cross-sectional survey. Lancet, 2015, 386(10002), 1465-1471.
[2]
Zuk, A.; Bonventre, J.V. Acute kidney injury. Annu. Rev. Med., 2016, 67, 293-307.
[3]
Remuzzi, G.; Horton, R. Acute renal failure: An unacceptable death sentence globally. Lancet, 2013, 382(9910), 2041-2042.
[4]
Bonventre, J.V. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J. Am. Soc. Nephrol., 2003, 14(Suppl. 1), S55-S61.
[5]
Jones, M. Recognising acute kidney injury. Clin. Med. (Lond.), 2012, 12(3), 287-289.
[6]
Sharfuddin, A.A.; Molitoris, B.A. Pathophysiology of ischemic acute kidney injury. Nat. Rev. Nephrol., 2011, 7(4), 189-200.
[7]
Barasch, J.; Zager, R.; Bonventre, J.V. Acute kidney injury: A problem of definition. Lancet, 2017, 389(10071), 779-781.
[8]
Bonventre, J.V.; Yang, L. Cellular pathophysiology of ischemic acute kidney injury. J. Clin. Invest., 2011, 121(11), 4210-4221.
[9]
Liu, B.C.; Tang, T.T.; Lv, L.L.; Lan, H.Y. Renal tubule injury: A driving force toward chronic kidney disease. Kidney Int., 2018, 93(3), 568-579.
[10]
Dusmez, D.; Cengiz, B.; Yumrutas, O.; Demir, T.; Oztuzcu, S.; Demiryurek, S.; Tutar, E.; Bayraktar, R.; Bulut, A.; Simsek, H.; Dagli, S.N.; Kilic, T.; Bagci, C. Effect of verapamil and lidocaine on TRPM and NaV1.9 gene expressions in renal ischemia-reperfusion. Transplant. Proc., 2014, 46(1), 33-39.
[11]
Nadler, M.J.; Hermosura, M.C.; Inabe, K.; Perraud, A.L.; Zhu, Q.; Stokes, A.J.; Kurosaki, T.; Kinet, J.P.; Penner, R.; Scharenberg, A.M.; Fleig, A. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature, 2001, 411(6837), 590-595.
[12]
Asrar, S.; Aarts, M. TRPM7, the cytoskeleton and neuronal death. Channels (Austin), 2013, 7(1), 6-16.
[13]
Runnels, L.W.; Yue, L.; Clapham, D.E. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science, 2001, 291(5506), 1043-1047.
[14]
Cahalan, M.D. Cell biology. Channels as enzymes. Nature, 2001, 411(6837), 542-543.
[15]
Matsushita, M.; Kozak, J.A.; Shimizu, Y.; McLachlin, D.T.; Yamaguchi, H.; Wei, F.Y.; Tomizawa, K.; Matsui, H.; Chait, B.T.; Cahalan, M.D.; Nairn, A.C. Channel function is dissociated from the intrinsic kinase activity and autophosphorylation of TRPM7/ChaK1. J. Biol. Chem., 2005, 280(21), 20793-20803.
[16]
Fleig, A.; Chubanov, V. Trpm7. Handb. Exp. Pharmacol., 2014, 222, 521-546.
[17]
Schmitz, C.; Perraud, A.L.; Johnson, C.O.; Inabe, K.; Smith, M.K.; Penner, R.; Kurosaki, T.; Fleig, A.; Scharenberg, A.M. Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell, 2003, 114(2), 191-200.
[18]
Aarts, M.; Iihara, K.; Wei, W.L.; Xiong, Z.G.; Arundine, M.; Cerwinski, W.; MacDonald, J.F.; Tymianski, M. A key role for TRPM7 channels in anoxic neuronal death. Cell, 2003, 115(7), 863-877.
[19]
Nicotera, P.; Bano, D. The enemy at the gates. Ca2+ entry through TRPM7 channels and anoxic neuronal death. Cell, 2003, 115(7), 768-770.
[20]
Sun, H.S.; Jackson, M.F.; Martin, L.J.; Jansen, K.; Teves, L.; Cui, H.; Kiyonaka, S.; Mori, Y.; Jones, M.; Forder, J.P.; Golde, T.E.; Orser, B.A.; Macdonald, J.F.; Tymianski, M. Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia. Nat. Neurosci., 2009, 12(10), 1300-1307.
[21]
Demir, T.; Yumrutas, O.; Cengiz, B.; Demiryurek, S.; Unverdi, H.; Kaplan, D.S.; Bayraktar, R.; Ozkul, N.; Bagci, C. Evaluation of TRPM (transient receptor potential melastatin) genes expressions in myocardial ischemia and reperfusion. Mol. Biol. Rep., 2014, 41(5), 2845-2849.
[22]
Liu, A.; Wu, J.; Yang, C.; Wu, Y.; Zhang, Y.; Zhao, F.; Wang, H.; Yuan, L.; Song, L.; Zhu, T.; Fan, Y.; Yang, B. TRPM7 in CHBP-induced renoprotection upon ischemia reperfusion-related injury. Sci. Rep., 2018, 8(1), 5510.
[23]
Meng, Z.; Wang, X.; Yang, Z.; Xiang, F. Expression of transient receptor potential melastatin 7 up-regulated in the early stage of renal ischemia-reperfusion. Transplant. Proc., 2012, 44(5), 1206-1210.
[24]
Meng, Z.; Cao, R.; Wang, Y.; Cao, H.; Liu, T.; Yang, Z.; Wang, X. Suppression of renal TRPM7 may alleviate kidney injury in the renal transplantation. World J. Urol., 2014, 32(5), 1303-1311.
[25]
Du, J.; Xie, J.; Zhang, Z.; Tsujikawa, H.; Fusco, D.; Silverman, D.; Liang, B.; Yue, L. TRPM7-mediated Ca2+ signals confer fibrogenesis in human atrial fibrillation. Circ. Res., 2010, 106(5), 992-1003.
[26]
Fang, L.; Huang, C.; Meng, X.; Wu, B.; Ma, T.; Liu, X.; Zhu, Q.; Zhan, S.; Li, J. TGF-beta1-elevated TRPM7 channel regulates collagen expression in hepatic stellate cells via TGF-beta1/Smad pathway. Toxicol. Appl. Pharmacol., 2014, 280(2), 335-344.
[27]
Clapham, D.E.; Runnels, L.W.; Strubing, C. The TRP ion channel family. Nat. Rev. Neurosci., 2001, 2(6), 387-396.
[28]
Fonfria, E.; Murdock, P.R.; Cusdin, F.S.; Benham, C.D.; Kelsell, R.E.; McNulty, S. Tissue distribution profiles of the human TRPM cation channel family. J. Recept. Signal Transduct. Res., 2006, 26(3), 159-178.
[29]
Kunert-Keil, C.; Bisping, F.; Kruger, J.; Brinkmeier, H. Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics, 2006, 7, 159.
[30]
Dokuyucu, R.; Gogebakan, B.; Yumrutas, O.; Bozgeyik, I.; Gokce, H.; Demir, T. Expressions of TRPM6 and TRPM7 and histopathological evaluation of tissues in ischemia reperfusion performed rats. Ren. Fail., 2014, 36(6), 932-936.
[31]
Jang, Y.; Lee, Y.; Kim, S.M.; Yang, Y.D.; Jung, J.; Oh, U. Quantitative analysis of TRP channel genes in mouse organs. Arch. Pharm. Res., 2012, 35(10), 1823-1830.
[32]
Wang, M.; Weiss, M.; Simonovic, M.; Haertinger, G.; Schrimpf, S.P.; Hengartner, M.O.; von Mering, C. PaxDb, a database of protein abundance averages across all three domains of life. Mol. Cell. Proteomics, 2012, 11(8), 492-500.
[33]
Nikonorova, I.A.; Kornakov, N.V.; Dmitriev, S.E.; Vassilenko, K.S.; Ryazanov, A.G. Identification of a Mg2+-sensitive ORF in the 5′-leader of TRPM7 magnesium channel mRNA. Nucleic Acids Res., 2014, 42(20), 12779-12788.
[34]
Levitan, I.B.; Cibulsky, S.M. Biochemistry. TRP ion channels--two proteins in one. Science, 2001, 293(5533), 1270-1271.
[35]
Miller, B.A.; Zhang, W. TRP channels as mediators of oxidative stress. Adv. Exp. Med. Biol., 2011, 704, 531-544.
[36]
Dorovkov, M.V.; Ryazanov, A.G. Phosphorylation of annexin I by TRPM7 channel-kinase. J. Biol. Chem., 2004, 279(49), 50643-50646.
[37]
Dorovkov, M.V.; Kostyukova, A.S.; Ryazanov, A.G. Phosphorylation of annexin A1 by TRPM7 kinase: A switch regulating the induction of an alpha-helix. Biochemistry, 2011, 50(12), 2187-2193.
[38]
Clark, K.; Middelbeek, J.; Lasonder, E.; Dulyaninova, N.G.; Morrice, N.A.; Ryazanov, A.G.; Bresnick, A.R.; Figdor, C.G.; van Leeuwen, F.N. TRPM7 regulates myosin IIA filament stability and protein localization by heavy chain phosphorylation. J. Mol. Biol., 2008, 378(4), 790-803.
[39]
Perraud, A.L.; Zhao, X.; Ryazanov, A.G.; Schmitz, C. The channel-kinase TRPM7 regulates phosphorylation of the translational factor eEF2 via eEF2-k. Cell. Signal., 2011, 23(3), 586-593.
[40]
Ryazanova, L.V.; Dorovkov, M.V.; Ansari, A.; Ryazanov, A.G. Characterization of the protein kinase activity of TRPM7/ChaK1, a protein kinase fused to the transient receptor potential ion channel. J. Biol. Chem., 2004, 279(5), 3708-3716.
[41]
Runnels, L.W.; Yue, L.; Clapham, D.E. The TRPM7 channel is inactivated by PIP(2) hydrolysis. Nat. Cell Biol., 2002, 4(5), 329-336.
[42]
Chubanov, V.; Waldegger, S.; Mederos y Schnitzler, M.; Vitzthum, H.; Sassen, M.C.; Seyberth, H.W.; Konrad, M.; Gudermann, T. Disruption of TRPM6/TRPM7 complex formation by a mutation in the TRPM6 gene causes hypomagnesemia with secondary hypocalcemia. Proc. Natl. Acad. Sci. USA, 2004, 101(9), 2894-2899.
[43]
Chubanov, V.; Mittermeier, L.; Gudermann, T. Role of kinase-coupled TRP channels in mineral homeostasis. Pharmacol. Ther., 2018, 184, 159-176.
[44]
Schlingmann, K.P.; Weber, S.; Peters, M.; Niemann Nejsum, L.; Vitzthum, H.; Klingel, K.; Kratz, M.; Haddad, E.; Ristoff, E.; Dinour, D.; Syrrou, M.; Nielsen, S.; Sassen, M.; Waldegger, S.; Seyberth, H.W.; Konrad, M. Hypomagnesemia with secondary hypocalcemia is caused by mutations in TRPM6, a new member of the TRPM gene family. Nat. Genet., 2002, 31(2), 166-170.
[45]
Arjona, F.J.; de Baaij, J.H.; Schlingmann, K.P.; Lameris, A.L.; van Wijk, E.; Flik, G.; Regele, S.; Korenke, G.C.; Neophytou, B.; Rust, S.; Reintjes, N.; Konrad, M.; Bindels, R.J.; Hoenderop, J.G. CNNM2 mutations cause impaired brain development and seizures in patients with hypomagnesemia. PLoS Genet., 2014, 10(4), e1004267.
[46]
Zhang, Z.; Yu, H.; Huang, J.; Faouzi, M.; Schmitz, C.; Penner, R.; Fleig, A. The TRPM6 kinase domain determines the Mg. ATP sensitivity of TRPM7/M6 heteromeric ion channels. J. Biol. Chem., 2014, 289(8), 5217-5227.
[47]
Bessac, B.F.; Fleig, A. TRPM7 channel is sensitive to osmotic gradients in human kidney cells. J. Physiol., 2007, 582(Pt 3), 1073-1086.
[48]
Sontia, B.; Montezano, A.C.; Paravicini, T.; Tabet, F.; Touyz, R.M. Downregulation of renal TRPM7 and increased inflammation and fibrosis in aldosterone-infused mice: Effects of magnesium. Hypertension, 2008, 51(4), 915-921.
[49]
Yogi, A.; Callera, G.E.; O’Connor, S.E.; He, Y.; Correa, J.W.; Tostes, R.C.; Mazur, A.; Touyz, R.M. Dysregulation of renal transient receptor potential melastatin 6/7 but not paracellin-1 in aldosterone-induced hypertension and kidney damage in a model of hereditary hypomagnesemia. J. Hypertens., 2011, 29(7), 1400-1410.
[50]
Elizondo, M.R.; Arduini, B.L.; Paulsen, J.; MacDonald, E.L.; Sabel, J.L.; Henion, P.D.; Cornell, R.A.; Parichy, D.M. Defective skeletogenesis with kidney stone formation in dwarf zebrafish mutant for trpm7. Curr. Biol., 2005, 15(7), 667-671.
[51]
Yogi, A.; Callera, G.E.; Antunes, T.T.; Tostes, R.C.; Touyz, R.M. Transient receptor potential melastatin 7 (TRPM7) cation channels, magnesium and the vascular system in hypertension. Circ. J., 2011, 75(2), 237-245.
[52]
Schappe, M.S.; Szteyn, K.; Stremska, M.E.; Mendu, S.K.; Downs, T.K.; Seegren, P.V.; Mahoney, M.A.; Dixit, S.; Krupa, J.K.; Stipes, E.J.; Rogers, J.S.; Adamson, S.E.; Leitinger, N.; Desai, B.N. Chanzyme TRPM7 mediates the Ca2+ Influx essential for lipopolysaccharide-induced Toll-Like receptor 4 endocytosis and macrophage activation. Immunity, 2018, 48(1), 59-74.e55.
[53]
Granucci, F. The family of LPS signal transducers increases: The arrival of Chanzymes. Immunity, 2018, 48(1), 4-6.
[54]
Gluba, A.; Banach, M.; Hannam, S.; Mikhailidis, D.P.; Sakowicz, A.; Rysz, J. The role of Toll-like receptors in renal diseases. Nat. Rev. Nephrol., 2010, 6(4), 224-235.
[55]
Venereau, E.; Ceriotti, C.; Bianchi, M.E. DAMPs from cell death to new life. Front. Immunol., 2015, 6, 422.
[56]
Wu, H.; Ma, J.; Wang, P.; Corpuz, T.M.; Panchapakesan, U.; Wyburn, K.R.; Chadban, S.J. HMGB1 contributes to kidney ischemia reperfusion injury. J. Am. Soc. Nephrol., 2010, 21(11), 1878-1890.
[57]
Tang, T.T.; Lv, L.L.; Pan, M.M.; Wen, Y.; Wang, B.; Li, Z.L.; Wu, M.; Wang, F.M.; Crowley, S.D.; Liu, B.C. Hydroxychloroquine attenuates renal ischemia/reperfusion injury by inhibiting cathepsin mediated NLRP3 inflammasome activation. Cell Death Dis., 2018, 9(3), 351.
[58]
Zhou, R.; Tardivel, A.; Thorens, B.; Choi, I.; Tschopp, J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol., 2010, 11(2), 136-140.
[59]
Wang, J.; Wen, Y.; Lv, L.L.; Liu, H.; Tang, R.N.; Ma, K.L.; Liu, B.C. Involvement of endoplasmic reticulum stress in angiotensin II-induced NLRP3 inflammasome activation in human renal proximal tubular cells in vitro. Acta Pharmacol. Sin., 2015, 36(7), 821-830.
[60]
Wen, Y.; Liu, Y.R.; Tang, T.T.; Pan, M.M.; Xu, S.C.; Ma, K.L.; Lv, L.L.; Liu, H.; Liu, B.C. mROS-TXNIP axis activates NLRP3 inflammasome to mediate renal injury during ischemic AKI. Int. J. Biochem. Cell Biol., 2018, 98, 43-53.
[61]
Havasi, A.; Borkan, S.C. Apoptosis and acute kidney injury. Kidney Int., 2011, 80(1), 29-40.
[62]
Jiang, M.; Wei, Q.; Dong, G.; Komatsu, M.; Su, Y.; Dong, Z. Autophagy in proximal tubules protects against acute kidney injury. Kidney Int., 2012, 82(12), 1271-1283.
[63]
Padanilam, B.J. Cell death induced by acute renal injury: a perspective on the contributions of apoptosis and necrosis. Am. J. Physiol. Renal Physiol., 2003, 284(4), F608-F627.
[64]
Yang, B.; Johnson, T.S.; Thomas, G.L.; Watson, P.F.; Wagner, B.; Nahas, A.M. Apoptosis and caspase-3 in experimental anti-glomerular basement membrane nephritis. J. Am. Soc. Nephrol., 2001, 12(3), 485-495.
[65]
Yang, B.; El Nahas, A.M.; Thomas, G.L.; Haylor, J.L.; Watson, P.F.; Wagner, B.; Johnson, T.S. Caspase-3 and apoptosis in experimental chronic renal scarring. Kidney Int., 2001, 60(5), 1765-1776.
[66]
McArthur, K.; Whitehead, L.W.; Heddleston, J.M.; Li, L.; Padman, B.S.; Oorschot, V.; Geoghegan, N.D.; Chappaz, S.; Davidson, S.; San Chin, H.; Lane, R.M.; Dramicanin, M.; Saunders, T.L.; Sugiana, C.; Lessene, R.; Osellame, L.D.; Chew, T.L.; Dewson, G.; Lazarou, M.; Ramm, G.; Lessene, G.; Ryan, M.T.; Rogers, K.L.; van Delft, M.F.; Kile, B.T. BAK/BAX macropores facilitate mitochondrial herniation and mtDNA efflux during apoptosis. Science, 2018, 359(6378), pii: eaao6047.
[67]
Yang, B.; Johnson, T.S.; Thomas, G.L.; Watson, P.F.; Wagner, B.; Skill, N.J.; Haylor, J.L.; El Nahas, A.M. Expression of apoptosis-related genes and proteins in experimental chronic renal scarring. J. Am. Soc. Nephrol., 2001, 12(2), 275-288.
[68]
Yang, B.; Jain, S.; Pawluczyk, I.Z.; Imtiaz, S.; Bowley, L.; Ashra, S.Y.; Nicholson, M.L. Inflammation and caspase activation in long-term renal ischemia/reperfusion injury and immunosuppression in rats. Kidney Int., 2005, 68(5), 2050-2067.
[69]
Feldenberg, L.R.; Thevananther, S.; del Rio, M.; de Leon, M.; Devarajan, P. Partial ATP depletion induces Fas- and caspase-mediated apoptosis in MDCK cells. Am. J. Physiol., 1999, 276(6), F837-F846.
[70]
Desai, B.N.; Krapivinsky, G.; Navarro, B.; Krapivinsky, L.; Carter, B.C.; Febvay, S.; Delling, M.; Penumaka, A.; Ramsey, I.S.; Manasian, Y.; Clapham, D.E. Cleavage of TRPM7 releases the kinase domain from the ion channel and regulates its participation in Fas-induced apoptosis. Dev. Cell, 2012, 22(6), 1149-1162.
[71]
Oltvai, Z.N.; Milliman, C.L.; Korsmeyer, S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell, 1993, 74(4), 609-619.
[72]
Korsmeyer, S.J.; Shutter, J.R.; Veis, D.J.; Merry, D.E.; Oltvai, Z.N. Bcl-2/Bax: A rheostat that regulates an anti-oxidant pathway and cell death. Semin. Cancer Biol., 1993, 4(6), 327-332.
[73]
Yang, B.; Johnson, T.S.; Thomas, G.L.; Watson, P.F.; Wagner, B.; Furness, P.N.; El Nahas, A.M. A shift in the Bax/Bcl-2 balance may activate caspase-3 and modulate apoptosis in experimental glomerulonephritis. Kidney Int., 2002, 62(4), 1301-1313.
[74]
Czabotar, P.E.; Lessene, G.; Strasser, A.; Adams, J.M. Control of apoptosis by the BCL-2 protein family: Implications for physiology and therapy. Nat. Rev. Mol. Cell Biol., 2014, 15(1), 49-63.
[75]
Yang, B.; Jain, S.; Ashra, S.Y.; Furness, P.N.; Nicholson, M.L. Apoptosis and caspase-3 in long-term renal ischemia/reperfusion injury in rats and divergent effects of immunosuppressants. Transplantation, 2006, 81(10), 1442-1450.
[76]
Waller, H.L.; Harper, S.J.; Hosgood, S.A.; Bagul, A.; Kay, M.D.; Kaushik, M.; Yang, B.; Bicknell, G.R.; Nicholson, M.L. Differential expression of cytoprotective and apoptotic genes in an ischaemia-reperfusion isolated organ perfusion model of the transplanted kidney. Transpl. Int., 2007, 20(7), 625-631.
[77]
Wu, Y.; Zhang, J.; Liu, F.; Yang, C.; Zhang, Y.; Liu, A.; Shi, L.; Wu, Y.; Zhu, T.; Nicholson, M.L.; Fan, Y.; Yang, B. Protective effects of HBSP on ischemia reperfusion and cyclosporine a induced renal injury. Clin. Dev. Immunol., 2013, 2013, 758159.
[78]
Yang, C.; Hosgood, S.A.; Meeta, P.; Long, Y.; Zhu, T.; Nicholson, M.L.; Yang, B. Cyclic helix B peptide in preservation solution and autologous blood perfusate ameliorates ischemia-reperfusion injury in isolated porcine kidneys. Transplant. Direct, 2015, 1(2), e6.
[79]
Yang, B.; Harris, K.P.; Jain, S.; Nicholson, M.L. Caspase-7, Fas and FasL in long-term renal ischaemia/reperfusion and immunosuppressive injuries in rats. Am. J. Nephrol., 2007, 27(4), 397-408.
[80]
Chatterjee, P.K.; Todorovic, Z.; Sivarajah, A.; Mota-Filipe, H.; Brown, P.A.; Stewart, K.N.; Cuzzocrea, S.; Thiemermann, C. Differential effects of caspase inhibitors on the renal dysfunction and injury caused by ischemia-reperfusion of the rat kidney. Eur. J. Pharmacol., 2004, 503(1-3), 173-183.
[81]
Yang, B.; Elias, J.E.; Bloxham, M.; Nicholson, M.L. Synthetic small interfering RNA down-regulates caspase-3 and affects apoptosis, IL-1 beta, and viability of porcine proximal tubular cells. J. Cell. Biochem., 2011, 112(5), 1337-1347.
[82]
Yang, B.; Hosgood, S.A.; Nicholson, M.L. Naked small interfering RNA of caspase-3 in preservation solution and autologous blood perfusate protects isolated ischemic porcine kidneys. Transplantation, 2011, 91(5), 501-507.
[83]
Yang, C.; Li, L.; Xue, Y.; Zhao, Z.; Zhao, T.; Jia, Y.; Rong, R.; Xu, M.; Nicholson, M.L.; Zhu, T.; Yang, B. Innate immunity activation involved in unprotected porcine auto-transplant kidneys preserved by naked caspase-3 siRNA. J. Transl. Med., 2013, 11, 210.
[84]
Yang, C.; Zhao, T.; Zhao, Z.; Jia, Y.; Li, L.; Zhang, Y.; Song, M.; Rong, R.; Xu, M.; Nicholson, M.L.; Zhu, T.; Yang, B. Serum-stabilized naked caspase-3 siRNA protects autotransplant kidneys in a porcine model. Mol. Ther., 2014, 22(10), 1817-1828.
[85]
Yang, B.; Lan, S.; Dieude, M.; Sabo-Vatasescu, J.P.; Karakeussian-Rimbaud, A.; Turgeon, J.; Qi, S.; Gunaratnam, L.; Patey, N.; Hebert, M.J. Caspase-3 is a pivotal regulator of microvascular rarefaction and renal fibrosis after ischemia-reperfusion injury. J. Am. Soc. Nephrol., 2018, 29(7), 1900-1916.
[86]
Lin, C.M.; Ma, J.M.; Zhang, L.; Hao, Z.Y.; Zhou, J.; Zhou, Z.Y.; Shi, H.Q.; Zhang, Y.F.; Shao, E.M.; Liang, C.Z. Inhibition of transient receptor potential melastain 7 enhances apoptosis induced by TRAIL in PC-3 cells. Asian Pac. J. Cancer Prev., 2015, 16(10), 4469-4475.
[87]
Li, X.; Wang, X.; Wang, Y.; Li, X.; Huang, C.; Li, J. Inhibition of transient receptor potential melastatin 7 (TRPM7) channel induces RA FLSs apoptosis through endoplasmic reticulum (ER) stress. Clin. Rheumatol., 2014, 33(11), 1565-1574.
[88]
Zong, W.X.; Thompson, C.B. Necrotic death as a cell fate. Genes Dev., 2006, 20(1), 1-15.
[89]
Cho, Y.S.; Challa, S.; Moquin, D.; Genga, R.; Ray, T.D.; Guildford, M.; Chan, F.K. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell, 2009, 137(6), 1112-1123.
[90]
He, S.; Wang, L.; Miao, L.; Wang, T.; Du, F.; Zhao, L.; Wang, X. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell, 2009, 137(6), 1100-1111.
[91]
Galluzzi, L.; Kepp, O.; Kroemer, G. MLKL regulates necrotic plasma membrane permeabilization. Cell Res., 2014, 24(2), 139-140.
[92]
Cai, Z.; Jitkaew, S.; Zhao, J.; Chiang, H.C.; Choksi, S.; Liu, J.; Ward, Y.; Wu, L.G.; Liu, Z.G. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat. Cell Biol., 2014, 16(1), 55-65.
[93]
Dannappel, M.; Vlantis, K.; Kumari, S.; Polykratis, A.; Kim, C.; Wachsmuth, L.; Eftychi, C.; Lin, J.; Corona, T.; Hermance, N.; Zelic, M.; Kirsch, P.; Basic, M.; Bleich, A.; Kelliher, M.; Pasparakis, M. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature, 2014, 513(7516), 90-94.
[94]
Liang, X.; Chen, Y.; Zhang, L.; Jiang, F.; Wang, W.; Ye, Z.; Liu, S.; Yu, C.; Shi, W. Necroptosis, a novel form of caspase-independent cell death, contributes to renal epithelial cell damage in an ATP-depleted renal ischemia model. Mol. Med. Rep., 2014, 10(2), 719-724.
[95]
Ryazanova, L.V.; Rondon, L.J.; Zierler, S.; Hu, Z.; Galli, J.; Yamaguchi, T.P.; Mazur, A.; Fleig, A.; Ryazanov, A.G. TRPM7 is essential for Mg(2+) homeostasis in mammals. Nat. Commun., 2010, 1, 109.
[96]
Su, L.T.; Agapito, M.A.; Li, M.; Simonson, W.T.; Huttenlocher, A.; Habas, R.; Yue, L.; Runnels, L.W. TRPM7 regulates cell adhesion by controlling the calcium-dependent protease calpain. J. Biol. Chem., 2006, 281(16), 11260-11270.
[97]
Jin, J.; Wu, L.J.; Jun, J.; Cheng, X.; Xu, H.; Andrews, N.C.; Clapham, D.E. The channel kinase, TRPM7, is required for early embryonic development. Proc. Natl. Acad. Sci. USA, 2012, 109(5), E225-E233.
[98]
Jin, J.; Desai, B.N.; Navarro, B.; Donovan, A.; Andrews, N.C.; Clapham, D.E. Deletion of Trpm7 disrupts embryonic development and thymopoiesis without altering Mg2+ homeostasis. Science, 2008, 322(5902), 756-760.
[99]
Dietrich, A.; Chubanov, V.; Kalwa, H.; Rost, B.R.; Gudermann, T. Cation channels of the transient receptor potential superfamily: their role in physiological and pathophysiological processes of smooth muscle cells. Pharmacol. Ther., 2006, 112(3), 744-760.
[100]
He, Y.; Yao, G.; Savoia, C.; Touyz, R.M. Transient receptor potential melastatin 7 ion channels regulate magnesium homeostasis in vascular smooth muscle cells: Role of angiotensin II. Circ. Res., 2005, 96(2), 207-215.
[101]
Oancea, E.; Wolfe, J.T.; Clapham, D.E. Functional TRPM7 channels accumulate at the plasma membrane in response to fluid flow. Circ. Res., 2006, 98(2), 245-253.
[102]
Gurney, A.M. Going with the flow: Smooth muscle TRPM7 channels and the vascular response to blood flow. Circ. Res., 2006, 98(2), 163-164.
[103]
Gunther, T. Concentration, compartmentation and metabolic function of intracellular free Mg2+. Magnes. Res., 2006, 19(4), 225-236.
[104]
Romani, A.M. Cellular magnesium homeostasis. Arch. Biochem. Biophys., 2011, 512(1), 1-23.
[105]
Ferre, S.; Hoenderop, J.G.; Bindels, R.J. Insight into renal Mg2+ transporters. Curr. Opin. Nephrol. Hypertens., 2011, 20(2), 169-176.
[106]
Walder, R.Y.; Landau, D.; Meyer, P.; Shalev, H.; Tsolia, M.; Borochowitz, Z.; Boettger, M.B.; Beck, G.E.; Englehardt, R.K.; Carmi, R.; Sheffield, V.C. Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat. Genet., 2002, 31(2), 171-174.
[107]
Zhang, Z.; Wang, M.; Fan, X.H.; Chen, J.H.; Guan, Y.Y.; Tang, Y.B. Upregulation of TRPM7 channels by angiotensin II triggers phenotypic switching of vascular smooth muscle cells of ascending aorta. Circ. Res., 2012, 111(9), 1137-1146.
[108]
Brooks, D.P. Role of endothelin in renal function and dysfunction. Clin. Exp. Pharmacol. Physiol., 1996, 23(4), 345-348.
[109]
Baldoli, E.; Castiglioni, S.; Maier, J.A. Regulation and function of TRPM7 in human endothelial cells: TRPM7 as a potential novel regulator of endothelial function. PLoS One, 2013, 8(3), e59891.
[110]
Inoue, K.; Xiong, Z.G. Silencing TRPM7 promotes growth/proliferation and nitric oxide production of vascular endothelial cells via the ERK pathway. Cardiovasc. Res., 2009, 83(3), 547-557.
[111]
MacDonald, J.F.; Xiong, Z.G.; Jackson, M.F. Paradox of Ca2+ signaling, cell death and stroke. Trends Neurosci., 2006, 29(2), 75-81.


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VOLUME: 20
ISSUE: 8
Year: 2019
Page: [777 - 788]
Pages: 12
DOI: 10.2174/1389203720666190507102948
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