Cooperative interaction of trp melastatin channel transient receptor potential (TRPM2) with its splice variant TRPM2 short variant is essential for Endothelial cell Apoptosis

Circulation Research

Volumn 114, Issue 3, 2014, Pages 469-479

  Hecquet, Claudie M ^a   Zhang, Min ^a   Mittal, Manish ^a   Vogel, Stephen M ^a   Di, Anke ^a   Gao, Xiaopei ^a   Bonini, Marcelo G ^a,b   Malik, Asrar B ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

apoptosis; capillary permeability; endothelium; inflammation

Indexed keywords

APOPTOSIS; CAPILLARY PERMEABILITY; ENDOTHELIUM; INFLAMMATION;

ANIMALS; APOPTOSIS; CALCIUM SIGNALING; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; GENETIC VARIATION; HUMANS; MICE; MICE, KNOCKOUT; MULTIGENE FAMILY; PROTEIN BINDING; PROTEIN ISOFORMS; RNA SPLICING; TRPM CATION CHANNELS;

EID: 84894044010     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.114.302414     Document Type: Article

References (44)

1. Aarts MM, Tymianski M. TRPMs and neuronal cell death. Pflugers Arch. 2005;451:243-249.
2. Naz?ro?lu M. TRPM2 cation channels, oxidative stress and neurological diseases: where are we now? Neurochem Res. 2011;36:355-366.
3. Nagamine K, Kudoh J, Minoshima S, Kawasaki K, Asakawa S, Ito F, Shimizu N. Molecular cloning of a novel putative Ca2+ channel protein (TRPC7) highly expressed in brain. Genomics. 1998;54:124-131.
4. Kraft R, Grimm C, Grosse K, Hoffmann A, Sauerbruch S, Kettenmann H, Schultz G, Harteneck C. Hydrogen peroxide and ADP-ribose induce TRPM2-mediated calcium influx and cation currents in microglia. Am J Physiol Cell Physiol. 2004;286:C129-C137.
5. Hecquet CM, Ahmmed GU, Vogel SM, Malik AB. Role of TRPM2 channel in mediating H2O2-induced Ca2+ entry and endothelial hyperpermeability. Circ Res. 2008;102:347-355.
6. Hara Y, Wakamori M, Ishii M, Maeno E, Nishida M, Yoshida T, Yamada H, Shimizu S, Mori E, Kudoh J, Shimizu N, Kurose H, Okada Y, Imoto K, Mori Y. LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol Cell. 2002;9:163-173.
7. Uchida K, Dezaki K, Damdindorj B, Inada H, Shiuchi T, Mori Y, Yada T, Minokoshi Y, Tominaga M. Lack of TRPM2 impaired insulin secretion and glucose metabolisms in mice. Diabetes. 2011;60:119-126.
8. Togashi K, Hara Y, Tominaga T, Higashi T, Konishi Y, Mori Y, Tominaga M. TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J. 2006;25:1804-1815.
9. Ishii M, Shimizu S, Hara Y, Hagiwara T, Miyazaki A, Mori Y, Kiuchi Y. Intracellular-produced hydroxyl radical mediates H2O2-induced Ca2+ influx and cell death in rat beta-cell line RIN-5F. Cell Calcium. 2006;39:487-494.
10. Kühn FJ, Heiner I, Lückhoff A. TRPM2: a calcium influx pathway regulated by oxidative stress and the novel second messenger ADP-ribose. Pflugers Arch. 2005;451:212-219.
11. Yamamoto S, Shimizu S, Kiyonaka S, et al. TRPM2-mediated Ca2+ influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat Med. 2008;14:738-747.
12. Miller BA. The role of TRP channels in oxidative stress-induced cell death. J Membr Biol. 2006;209:31-41.
13. McNulty S, Fonfria E. The role of TRPM channels in cell death. Pflugers Arch. 2005;451:235-242.
14. Zhang W, Hirschler-Laszkiewicz I, Tong Q, Conrad K, Sun SC, Penn L, Barber DL, Stahl R, Carey DJ, Cheung JY, Miller BA. TRPM2 is an ion channel that modulates hematopoietic cell death through activation of caspases and PARP cleavage. Am J Physiol Cell Physiol. 2006;290:C1146-C1159.
15. Walsh K, Isner JM. Apoptosis in inflammatory-fibroproliferative disorders of the vessel wall. Cardiovasc Res. 2000;45:756-765.
16. Hashimoto S, Kobayashi A, Kooguchi K, Kitamura Y, Onodera H, Nakajima H. Upregulation of two death pathways of perforin/granzyme and FasL/Fas in septic acute respiratory distress syndrome. Am J Respir Crit Care Med. 2000;161:237-243.
17. Hotchkiss RS, Tinsley KW, Swanson PE, Karl IE. Endothelial cell apoptosis in sepsis. Crit Care Med. 2002;30:S225-S228.
18. Kwan HY, Huang Y, Yao X. TRP channels in endothelial function and dysfunction. Biochim Biophys Acta. 2007;1772:907-914.
19. Dietrich A, Gudermann T. Another TRP to endothelial dysfunction. Circ Res. 2008;102:275-277.
20. Hecquet CM, Ahmmed GU, Malik AB. TRPM2 channel regulates endothelial barrier function. Adv Exp Med Biol. 2010;661:155-167.
21. Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, Schmitz C, Stokes AJ, Zhu Q, Bessman MJ, Penner R, Kinet JP, Scharenberg AM. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature. 2001;411:595-599.
22. Sano Y, Inamura K, Miyake A, Mochizuki S, Yokoi H, Matsushime H, Furuichi K. Immunocyte Ca2+ influx system mediated by LTRPC2. Science. 2001;293:1327-1330.
23. Perraud AL, Takanishi CL, Shen B, Kang S, Smith MK, Schmitz C, Knowles HM, Ferraris D, Li W, Zhang J, Stoddard BL, Scharenberg AM. Accumulation of free ADP-ribose from mitochondria mediates oxidative stress-induced gating of TRPM2 cation channels. J Biol Chem. 2005;280:6138-6148.
24. Fonfria E, Marshall IC, Benham CD, Boyfield I, Brown JD, Hill K, Hughes JP, Skaper SD, McNulty S. TRPM2 channel opening in response to oxidative stress is dependent on activation of poly(ADP-ribose) polymerase. Br J Pharmacol. 2004;143:186-192.
25. Miller BA. Inhibition of TRPM2 function by PARP inhibitors protects cells from oxidative stress-induced death. Br J Pharmacol. 2004;143:515-516.
26. Wehage E, Eisfeld J, Heiner I, Jüngling E, Zitt C, Lückhoff A. Activation of the cation channel long transient receptor potential channel 2 (LTRPC2) by hydrogen peroxide. A splice variant reveals a mode of activation independent of ADP-ribose. J Biol Chem. 2002;277:23150-23156.
27. Hecquet CM, Malik AB. Role of H(2)O(2)-activated TRPM2 calcium channel in oxidant-induced endothelial injury. Thromb Haemost. 2009;101:619-625.
28. Zhang W, Chu X, Tong Q, Cheung JY, Conrad K, Masker K, Miller BA. A novel TRPM2 isoform inhibits calcium influx and susceptibility to cell death. J Biol Chem. 2003;278:16222-16229.
29. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature. 1994;371:346-347.
30. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, Yuan J. Human ICE/CED-3 protease nomenclature. Cell. 1996;87:171.
31. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, Hug H, Marmé D, Schächtele C. Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976. J Biol Chem. 1993;268:9194-9197.
32. Robaye B, Mosselmans R, Fiers W, Dumont JE, Galand P. Tumor necrosis factor induces apoptosis (programmed cell death) in normal endothelial cells in vitro. Am J Pathol. 1991;138:447-453.
33. Bornancin F, Parker PJ. Phosphorylation of protein kinase C-alpha on serine 657 controls the accumulation of active enzyme and contributes to its phosphatase-resistant state. J Biol Chem. 1997;272:3544-3549.
34. Barnard ML, Matalon S. Mechanisms of extracellular reactive oxygen species injury to the pulmonary microvasculature. J Appl Physiol (1985). 1992;72:1724-1729.
35. Lum H, Roebuck KA. Oxidant stress and endothelial cell dysfunction. Am J Physiol Cell Physiol. 2001;280:C719-C741.
36. Di A, Gao X-P, Qian F, et al. The redox-sensitive cation channel TRPM2 modulates phagocyte ROS production and inflammation. Nat Immunol. 2012;13:29-34.
37. Inamura K, Sano Y, Mochizuki S, Yokoi H, Miyake A, Nozawa K, Kitada C, Matsushime H, Furuichi K. Response to ADP-ribose by activation of TRPM2 in the CRI-G1 insulinoma cell line. J Membr Biol. 2003;191:201-207.
38. Sergeev IN. Calcium signaling in cancer and vitamin D. J Steroid Biochem Mol Biol. 2005;97:145-151.
39. Xu XZ, Moebius F, Gill DL, Montell C. Regulation of melastatin, a TRP-related protein, through interaction with a cytoplasmic isoform. Proc Natl Acad Sci USA. 2001;98:10692-10697.
40. Gasser A, Glassmeier G, Fliegert R, Langhorst MF, Meinke S, Hein D, Krüger S, Weber K, Heiner I, Oppenheimer N, Schwarz JR, Guse AH. Activation of T cell calcium influx by the second messenger ADP-ribose. J Biol Chem. 2006;281:2489-2496.
41. Vandenbroucke St Amant E, Tauseef M, Vogel SM, Gao X-P, Mehta D, Komarova YA, Malik AB. PKCα activation of p120-catenin serine 879 phospho-switch disassembles VE-cadherin junctions and disrupts vascular integrity. Circ Res. 2012;111:739-749.
42. Denning TL, Takaishi H, Crowe SE, Boldogh I, Jevnikar A, Ernst PB. Oxidative stress induces the expression of Fas and Fas ligand and apoptosis in murine intestinal epithelial cells. Free Radic Biol Med. 2002;33:1641-1650.
43. Ma S, Ochi H, Cui L, Zhang J, He W. Hydrogen peroxide induced down-regulation of CD28 expression of Jurkat cells is associated with a change of site alpha-specific nuclear factor binding activity and the activation of caspase-3. Exp Gerontol. 2003;38:1109-1118.
44. Wiseman H, Halliwell B. Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem J. 1996;313(Pt 1):17-29.