Nitric oxide, mitochondrial hyperpolarization, and T cell activation

Free Radical Biology and Medicine

Volumn 42, Issue 11, 2007, Pages 1625-1631

  Nagy, Gyorgy ^a,b   Koncz, Agnes ^a   Fernandez, David ^a   Perl, Andras ^a  

^a Department of Medicine   (United States)

^b SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Apoptosis; Calcium; Free radicals; Mitochondrial biogenesis; Mitochondrial hyperpolarization; Nitric oxide

Indexed keywords

CALCIUM; CYCLIC GMP; GUANYLATE CYCLASE; NITRIC OXIDE;

APOPTOSIS; AUTOIMMUNITY; BIOGENESIS; CALCIUM SIGNALING; CELL MEMBRANE POTENTIAL; ENZYME ACTIVATION; HUMAN; HYPERPOLARIZATION; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION;

AUTOIMMUNITY; CALCIUM SIGNALING; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MEMBRANE POTENTIAL, MITOCHONDRIAL; NITRIC OXIDE; OXIDATIVE STRESS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 34247360451     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.02.026     Document Type: Review

References (70)

1. Duchen M.R. Mitochondria in health and disease: perspectives on a new mitochondrial biology. Mol. Aspects Med. 25 (2004) 365-451
2. Nagy G., Koncz A., and Perl A. T- and B-cell abnormalities in systemic lupus erythematosus. Crit. Rev. Immunol. 25 (2005) 123-140
3. Skulachev V.P. Mitochondrial physiology and pathology: concepts of programmed death of organelles, cells and organisms. Mol. Aspects Med. 20 (1999) 139-140
4. Constantini P., Chernyak B.V., Petronilli B., and Bernardi P. Modulation of themitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol. Chem. 271 (1996) 6746-6751
5. Perl A., Gergely Jr. P., Puskas F., and Banki K. Metabolic switches of T-cell activation and apoptosis. Antioxid. Redox Signaling 4 (2002) 427-443
6. Banki K., Hutter E., Gonchoroff N., and Perl A. Elevation of mitochondrial transmembrane potential and reactive oxygen intermediate levels are early events and occur independently from activation of caspases in Fas signaling. J. Immunol. 162 (1999) 1466-1479
7. Banki K., Hutter E., Colombo E., Gonchoroff N.J., and Perl A. Glutathione levels and sensitivity to apoptosis are regulated by changes in transaldolase expression. J. Biol. Chem. 271 (1996) 32994-33001
8. Puskas F., Gergely P., Banki K., and Perl A. Stimulation of the pentose phosphate pathway and glutathione levels by dehydroascorbate, the oxidized form of vitamin C. FASEB J. 14 (2000) 1352-1361
9. Li P.-F., Dietz R., and von Harsdorf R. p53 regulates mitochondrial membrane potential through reactive oxygen species and induces cytochrome c-independent apoptosis blocked by bcl-2. EMBO J. 18 (1999) 6027-6036
10. Gottlieb E., Vander Heiden M.G., and Thompson C.B. Bcl-XL prevents the initial decrease in mitochondrial membrane potential and subsequent reactive oxygen species production during tumor necrosis factor alpha-induced apoptosis. Mol. Cell. Biol. 20 (2000) 5680-5689
11. Scarlett J.L., Sheard P.W., Hughes G., Ledgerwood E.C., Ku H.-H., and Murphy M.P. Changes in mitochondrial membrane potential during staurosporin-induced apoptosis in Jurkat cells. FEBS Lett. 475 (2000) 267-272
12. Sanchez-Alcazar J.A., Ault J.G., Khodjakov A., and Schneider E. Increased mitochondrial cytochrome c levels and mitochondrial hyperpolarization precede camptothecin-induced apoptosis in Jurkat cells. Cell Death Differ. 7 (2000) 1090-1100
13. Almeida A., Almeida J., Bolanos J.P., and Moncada S. Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc. Natl. Acad. Sci. USA 98 (2001) 15294-15299
14. Norman J.P., Perry S.W., Kasischke K.A., Volsky D.J., and Gelbard H.A. HIV-1 trans activator of transcription protein elicits mitochondrial hyperpolarization and respiratory deficit, with dysregulation of complex IV and nicotinamide adenine dinucleotide homeostasis in cortical neurons. J. Immunol. 178 (2007) 869-876
15. Gergely P.J., Grossman C., Niland B., Puskas F., Neupane H., Allam F., Banki K., Phillips P.E., and Perl A. Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus. Arthritis Rheum. 46 (2002) 175-190
16. 2+- and redox-dependent production of nitric oxide. J. Immunol. 171 (2003) 5188-5197
17. Krishnan S., Kiang J.G., Fisher C.U., Nambiar M.P., Nguyen H.T., Kyttaris V.C., Chowdhury B., Rus V., and Tsokos G.C. Increased caspase-3 expression and activity contribute to reduced CD3{zeta} expression in systemic lupus erythematosus T cells. J. Immunol. 175 (2005) 3417-3423
18. Perl A., Gergely Jr. P., Nagy G., Koncz A., and Banki K. Mitochondrial hyperpolarization: a checkpoint of T cell life, death, and autoimmunity. Trends Immunol. 25 (2004) 360-367
19. Cohen J.J., Duke R.C., Fadok V.A., and Sellins K.A. Apoptosis and programmed cell death in immunity. Annu. Rev. Immunol. 10 (1992) 267-293
20. Sauter B., Albert M.L., Francisco L., Larsson M., Somersan S., and Bhardwaj N. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med. 191 (2000) 423-434
21. Eisner M.D., Amory J., Mullaney B., Tierney Jr. L., and Browner W.S. Necrotizing lymphadenitis associated with systemic lupus erythematosus. Semin. Arthritis Rheum. 26 (1996) 477-482
22. Ma L., Chan K.W., Trendell-Smith N.J., Wu A., Tian L., Lam A.C., Chan A.K., Lo C.K., Chik S., Ko K.H., To C.K., Kam S.K., Li X.S., Yang C.H., Leung S.Y., Ng M.H., Stott D.I., MacPherson G.G., and Huang F.P. Systemic autoimmune disease induced by dendritic cells that have captured necrotic but not apoptotic cells in susceptible mouse strains. Eur. J. Immunol. 35 (2005) 3364-3375
23. Lanzaveccia A., Lezzi G., and Viola A. From TcR engagement to T cell activation: a kinetic view of T cell behavior. Cell 96 (1999) 1-4
24. Germain R.N. The T cell receptor for antigen: signaling and ligand discrimination. J. Biol. Chem. 276 (2001) 35223-35226
25. Abraham N., Miceli M.C., Parnes J.R., and Veillette A. Enhancement of T-cell responsiveness by the lymphocyte-specific tyrosine protein kinase p56lck. Nature 350 (1991) 62-66
26. Samelson L.E., and Klauser R.D. Tyrosine kinases and tyrosine based activation motifs. J. Biol. Chem. 267 (1992) 24913-24916
27. 2+ mobilization. Biochem. J. 247 (1987) 695-700
28. Lewis R.S. Calcium signaling mechanism in T lymphocytes. Annu. Rev. Immunol. 19 (2001) 497-521
29. Premack B.A., and Gardner P. Signal transduction by T cell receptors: mobilization of Ca and regulation of Ca-dependent effector molecules. Am. J. Physiol. 263 (1992) 19-40
30. Chance B. The nature of electron transfer and energy coupling reactions. FEBS Lett. 23 (1972) 3-20
31. Rizzuto R., Bernardi P., and Pozzan T. Mitochondria as all-round players of the calcium game. J. Physiol. 15 (2000) 37-47
32. Duchen M.R. Mitochondria and calcium: from cell signalling to cell death. J. Physiol. 529 (2000) 57-68
33. 2+ oscillations in the mitochondria. Cell 82 (1995) 415-424
34. Perl A., Qian Y., Chohan K.R., Shirley C.R., Amidon W., Banerjee S., Middleton F.A., Conkrite K.L., Barcza M., Gonchoroff N., Suarez S.S., and Banki K. Transaldolase is essential for maintenance of the mitochondrial transmembrane potential and fertility of spermatozoa. Proc. Natl. Acad. Sci. USA 103 (2006) 14813-14818
35. 2+-dependent control of the permeability properties of the mitochondrial outer membrane and voltage-dependent anion-selective channel (VDAC). J. Biol. Chem. 281 (2006) 17347-17358
36. Bredt D.S. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic. Res. 31 (1999) 577-596
37. Song H., Xia S.L., Liao C., Li Y.L., Wang Y.F., Li T.P., and Zhao M.J. Genes encoding Pir51, Beclin 1, RbAp48 and aldolase b are up or down-regulated in human primary hepatocellular carcinoma. World J. Gastroenterol. 10 (2004) 509-513
38. 2+/calmodulin-dependent isoform in human B and T lymphocytes. Eur. J. Immunol. 3 (1996) 511-516
39. Ibiza S., Victor V.M., Bosca I., Ortega A., Urzainqui A., O'Connor J.E., Sanchez-Madrid F., Esplugues J.V., and Serrador J.M. Endothelial nitric oxide synthase regulates T cell receptor signaling at the immunological synapse. Immunity 24 (2006) 753-765
40. Beltran B., Mathur A., Duchen M.R., Erusalimsky J.D., and Moncada S. The effect of nitric oxide on cell respiration: a key to understanding its role in cell survival, or death. Proc. Natl. Acad. Sci. USA 26 (2000) 14602-14607
41. Nisoli E., and Carruba M.O. Nitric oxide and mitochondrial biogenesis. J. Cell Sci. 119 (2006) 2855-2862
42. Nisoli E., Clementi E., and Paolucci C. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299 (2003) 896-899
43. 2+ signaling profile of lupus T cells. J. Immunol. 173 (2004) 3576-3583
44. Grakoui A., Bromley S.K., Sumen C., Davis M.M., Shaw A.S., Allen P.M., and Dustin M.L. The immunological synapse: a molecular machine controlling T cell activation. Science 285 (1999) 221-227
45. Bates T.E., Loesch A., Burnstock G., and Clark J.B. Mitochondrial nitric oxide synthase: a ubiquitous regulator of oxidative phosphorylation?. Biochem. Biophys. Res. Commun. 218 (1996) 40-44
46. Valdez L.B., Zaobornyj T., and Boveris A. Mitochondrial metabolic states and membrane potential modulate mtNOS activity. Biochim. Biophys. Acta 1757 (2006) 166-172
47. Gao S., Chen J., Brodsky S.V., Huang H., Adler S., Lee J.H., Dhadwal N., Cohen-Gould L., Gross S.S., and Goligorsky M.S. Docking of endothelial nitric oxide synthase (eNOS) to the mitochondrial outer membrane: a pentabasic amino acid sequence in the autoinhibitory domain of eNOS targets a proteinase K-cleavable peptide on the cytoplasmic face of mitochondria. J. Biol. Chem. 279 (2004) 15968-15974
48. Moncada S., and Erusalimsky J.D. Does nitric oxide modulate mitochondrial energy generation and apoptosis?. Nat. Rev. Mol. Cell. Biol. 3 (2002) 214-220
49. Cemerski S., Cantagrel A., Van Meerwijk J.P., and Romagnoli P. Reactive oxygen species differentially affect T cell receptor-signaling pathways. J. Biol. Chem. 277 (2002) 19585-19593
50. Schreck R., Rieber P., and Baeuerle P.A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 10 (1991) 2247-2258
51. Williams M.S., and Kwon J. T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radic. Biol. Med. 37 (2004) 1144-1151
52. Hardwick J.S., and Sefton B.M. Activation of the Lck tyrosine protein kinaseby hydrogen peroxide requires the phosphorylation of Tyr-394. Proc. Natl. Acad. Sci. USA 92 (1995) 4527-42531
53. Blokhina O., Virolainen E., and Fagerstedt K.V. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. (London) 91 (2003) 179-194
54. Kim Y.M., Bombeck C.A., and Billiar T.R. Nitric oxide as a bifunctional regulator of apoptosis. Circ. Res. 19 (1999) 253-256
55. Chung H.T., Pae H.O., Choi B.M., Billiar T.R., and Kim Y.M. Nitric oxide as a bioregulator of apoptosis. Biochem. Biophys. Res. Commun. 282 (2001) 1075-1079
56. Melino G., Catani M.V., Corazzari M., Guerrieri P., and Bernassola F. Nitric oxide can inhibit apoptosis or switch it into necrosis. Cell Mol. Life.Sci. 57 (2000) 612-622
57. Beltran B., Quintero M., Gracia-Zaragoza E., O'Connor E., Esplugues J.V., and Moncada S. Inhibition of mitochondrial respiration by endogenous nitric oxide: a critical step in Fas signalling. Proc. Natl. Acad. Sci. USA 13 (2002) 8892-8897
58. Brown C.G. Nitric oxide and mitochondrial respiration. Biochem. Biophys. Acta 1411 (1999) 351-369
59. Brookes P.S., Salinas E.P., Darley-Usmar K., Eiserich J.P., Freeman B.A., Darley-Usmar V.M., and Anderson P.G. Concentration dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome c release. J. Biol. Chem. 275 (2000) 20474-20479
60. Packer M.A., and Murphy M.P. Peroxynitrite causes calcium efflux from mitochondria which is prevented by cyclosporin A. FEBS Lett. 2-3 (1994) 237-240
61. Weinberg J.B., Granger D.L., and Pisetsky D.S. Alterations to glutathione andnicotinamide nucleotides during the mitochondrial permeability transition induced by peroxynitrite. Biochem. Pharmacol. 7 (1996) 1047-1055
62. Packer M.A., and Murphy M.P. Peroxynitrite formed by simultaneous nitric oxide and superoxide generation causes cyclosporin-A-sensitive mitochondrial calcium efflux and depolarisation. Eur. J. Biochem. 1 (1995) 231-239
63. Caricchio R., and Cohen P.L. Spontaneous and induced apoptosis in systemic lupus erythematosus: multiple assays fail to reveal consistent abnormalities. Cell. Immunol. 1 (1999) 54-60
64. Leist M., Single B., Castoldi A.F., Kuhnle S., and Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 185 (1997) 1481-1486
65. Amin A.R., Attur M., and Vyas P. Expression of nitric oxide synthase in human peripheral blood mononuclear cells and neutrophils. J. Inflammation 4 (1995) 190-205
66. Paglin S., Lee N.Y., Nakar C., Fitzgerald M., Plotkin J., Deuel B., Hackett N., McMahill M., Sphicas E., Lampen N., and Yahalom J. Rapamycin-sensitive pathway regulates mitochondrial membrane potential, autophagy, and survival in irradiated MCF-7 cells. Cancer Res. 65 (2005) 11061-11070
67. Warner L.M., Adams L.M., and Sehgal S.N. Rapamycin prolongs survival and arrests pathophysiologic changes in murine systemic lupus erythematosus. Arthritis Rheum. 37 (1994) 289-297
68. Fernandez D., Bonilla E., Mirza N., Niland B., and Perl A. Rapamycin reduces disease activity and normalizes T cell activation-induced calcium fluxing in patients with systemic lupus erythematosus. Arthritis Rheum. 54 (2006) 2983-2988
69. Ban H., Shigemitsu K., Yamatsuji T., Haisa M., Nakajo T., Takaoka M., Nobuhisa T., Gunduz M., Tanaka N., and Naomoto Y. Arginine and leucine regulate p70 S6 kinase and 4E-BP1 in intestinal epithelial cells. Int. J. Mol. Med. 13 (2004) 537-543
70. Desai B.N., Myers B.R., and Schreiber S.L. FKBP12-rapamycin-associated protein associates with mitochondria and senses osmotic stress via mitochondrial dysfunction. Proc. Natl. Acad. Sci. USA 99 (2002) 4319-4324