p66SHC promotes T cell apoptosis by inducing mitochondrial dysfunction and impaired Ca2+ homeostasis

Cell Death and Differentiation

Volumn 14, Issue 2, 2007, Pages 338-347

  Pellegrini, M ^a   Finetti, F ^a   Petronilli, V ^b   Ulivieri, C ^a   Giusti, F ^a   Lupetti, P ^a   Giorgio, M ^c   Pelicci, P G ^c   Bernardi, P ^b   Baldari, C T ^a  

^a UNIVERSITY OF SIENA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CALCIMYCIN; CALCIUM ION; CYTOCHROME C; OXIDOREDUCTASE; PROTEIN P66SHC; SERINE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CELL FRACTIONATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; ELECTRON MICROSCOPY; ENZYME RELEASE; FLOW CYTOMETRY; GENETIC TRANSFECTION; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS; CALCIMYCIN; CALCIUM; DOWN-REGULATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HOMEOSTASIS; HUMANS; JURKAT CELLS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PHOSPHOSERINE; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; T-LYMPHOCYTES;

EID: 33846240368     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401997     Document Type: Article

References (39)

1. Ravichandran KS. Signaling via Shc family adapter proteins. Oncogene 2001; 20: 6322-6330.
2. Migliaccio E, Mele S, Salcini AE, Pelicci G, Lai KM, Superti-Furga G et al. Opposite effects of the p52shc/p46shc and p66shc splicing isoforms on the EGF receptor-MAP kinase-fos signalling pathway. EMBO J 1997; 16: 706-716.
3. Okada S, Kao AW, Ceresa BP, Blaikie P, Margolis B, Pessin JE. The 66-kDa Shc isoform is a negative regulator of the epidermal growth factor-stimulated mitogen-activated protein kinase pathway. J Biol Chem 1997; 272: 28042-28049.
4. Pacini S, Pellegrini M, Migliaccio E, Patrussi L, Ulivieri C, Ventura A et al. p66SHC promotes apoptosis and antagonizes mitogenic signaling in T cells. Mol Cell Biol 2004; 24: 1747-1757.
5. Pellegrini M, Pacini S, Baldari CT. p66SHC: The apoptotic side of Shc proteins. Apoptosis 2005; 10: 13-18.
6. Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP et al. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 1999; 402: 309-313.
7. Smith WW, Norton DD, Gorospe M, Jiang H, Nemoto S, Holbrook NJ et al. Phosphorylation of p66Shc and forkhead proteins mediates Aβ toxicity. J Cell Biol 2005; 169: 331-339.
8. Yang CP, Horwitz SB. Taxol mediates serine phosphorylation of the 66-kDa Shc isoform. Cancer Res 2000; 60: 5171-5178.
9. Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 2002; 295: 2450-2452.
10. Trinei M, Giorgio M, Cicalese A, Barozzi S, Ventura A, Migliaccio E et al. A p53-p66Shc signalling pathway controls intracellular redox status, levels of oxidation-damaged DNA and oxidative stress-induced apoptosis. Oncogene 2002; 21: 3872-3878.
11. Napoli C, Martin-Padura I, de Nigris F, Giorgio M, Mansueto G, Somma P et al. Deletion of the p66Shc longevity gene reduces systemic and tissue oxidative stress, vascular cell apoptosis, and early atherogenesis in mice fed a high-fat diet. Proc Natl Acad Sci USA 2003; 100: 2112-2116.
12. Zaccagnini G, Martelli F, Fasanaro P, Magenta A, Gaetano C, Di Carlo A et al. p66ShcA modulates tissue response to hindlimb ischemia. Circulation 2004; 109: 2917-2923.
13. Orsini F, Migliaccio E, Moroni M, Contursi C, Raker VA, Piccini D et al. The life span determinant p66Shc localizes to mitochondria where it associates with mitochondrial heat shock protein 70 and regulates trans-membrane potential. J Biol Chem 2004; 279: 25689-25695.
14. Bernardi P, Krauskopf A, Basso E, Petronilli V, Blalchy-Dyson E, Di Lisa F et al. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J 2006; 273: 2077-2099.
15. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C et al. Electron transfer between cytochrome c and p66(Shc) generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 2005; 122: 221-223.
16. Ventura A, Luzi L, Pacini S, Baldari CT, Pelicci PG. The p66Shc longevity gene is silenced through epigenetic modifications of an alternative promoter. J Biol Chem 2002; 277: 22370-22376.
17. Penzo D, Petronilli V, Angelin A, Cusa C, Colonna R, Scorrano L et al. Arachidonic acid released by phospholipase A(2) activation triggers Ca(2+)-dependent apoptosis through the mitochondrial pathway. J Biol Chem 2004; 279: 25219-25225.
18. Bernardi P. Mitochondrial transport of cations: Channels, exchangers and permeability transition. Physiol Rev 1999; 79: 1127-1155.
19. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: The calcium-apoptosis link. Nat Rev Mol Cell Biol 2003; 4: 552-565.
20. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T et al. BAX and BAK regulation of endoplasmic reticulum Ca2+: A control point for apoptosis. Science 2003; 300: 135-139.
21. Bautista DM, Hoth M, Lewis RS. Enhancement of calcium signalling dynamics and stability by delayed modulation of the plasma-membrane calcium-ATPase in human T cells. J Physiol 2002; 541: 877-894.
22. Chen J, McLean PA, Neel BG, Okunade G, Shull GE, Wortis HH. CD22 attenuates calcium signaling by potentiating plasma membrane calcium-ATPase activity. Nat Immunol 2004; 5: 651-657.
23. Fujimoto T. Calcium pump of the plasma membrane is localized in caveolae. J Cell Biol 1993; 120: 1147-1157.
24. Guerini D, Wang X, Li L, Genazzani A, Carafoli E. Calcineurin controls the expression of isoform 4CII of the plasma membrane Ca(2+) pump in neurons. J Biol Chem 2000; 275: 3706-3712.
25. Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 1997; 15: 707-747.
26. Eskes R, Desagher S, Antonsson B, Martinou JC. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 2000; 20: 929-935.
27. Gross A, Jockel J, Wei MC, Korsmeyer SJ. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 1998; 17: 3878-3885.
28. Cai J, Jones DP. Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J Biol Chem 1998; 273: 11401-11404.
29. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA et al. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2002; 2: 55-67.
30. Soriano ME, Nicolosi L, Bernardi P. Desensitization of the permeability transition pore by cyclosporin A prevents activation of the mitochondrial apoptotic pathway and liver damage by tumor necrosis factor-alpha. J Biol Chem 2004; 279: 36803-36808.
31. Chiara MD, Bedoya F, Sobrino F. Cyclosporin A inhibits phorbol ester-induced activation of superoxide production in resident mouse peritoneal macrophages. Biochem J 1989; 264: 21-26.
32. 2+ pump: Focus on calpain sensitivity. J Biol Chem 2003; 278: 38141-38148.
33. Schwab BL, Guerini D, Didszun C, Bano D, Ferrando-May E, Fava E et al. Cleavage of plasma membrane calcium pumps by caspases: A link between apoptosis and necrosis. Cell Death Differ 2002; 9: 818-831.
34. Heissmeyer V, Macian F, Im SH, Varma R, Feske S, Venuprasad K et al. Calcineurin imposes T cell unresponsiveness through targeted proteolysis of signaling proteins. Nat Immunol 2004; 5: 255-265.
35. Bigelow DJ, Squier TC. Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim Biophys Acta 2005; 1703: 121-123.
36. Zaidi A, Michaelis ML. Effects of reactive oxygen species on brain synaptic plasma membrane Ca(2+)-ATPase. Free Radic Biol Med 1999; 27: 810-821.
37. Plyte S, Boncristiano M, Fattori E, Galvagni F, Rossi Paccani S, Majolini MB et al. Identification and characterization of a novel nuclear factor of activated T-cells-1 isoform expressed in mouse brain. J Biol Chem 2001; 276: 14350-14358.
38. Ghittoni R, Patrussi L, Pirozzi K, Pellegrini M, Lazzerini PE, Capecchi PL et al. Simvastatin inhibits T-cell activation by selectively impairing the function of Ras superfamily GTPases. FASEB J 2005; 19: 605-607.
39. Liang Y, Yan C, Nylander KD, Schor NF. Early events in Bcl-2-enhanced apoptosis. Apoptosis 2003; 8: 609-611.