Proteomic analysis identifies prohibitin down-regulation as a crucial event in the mitochondrial damage observed in HIV-infected patients

Antiviral Therapy

Volumn 15, Issue 3, 2010, Pages 377-390

  Ciccosanti, Fabiola ^a   Corazzari, Marco ^a   Soldani, Fabio ^a,b   Matarrese, Paola ^c   Pagliarini, Vittoria ^a   Iadevaia, Valentina ^a   Tinari, Antonella ^c   Zaccarelli, Mauro ^a   Perfettini, Jean Luc ^d,e,f   Malorni, Walter ^c   Kroemer, Guido ^d,e,f   Antinori, Andrea ^a   Fimia, Gian Maria ^a   Piacentini, Mauro ^a,g  

^a NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d Institut Gustave Roussy   (France)

^e INSTITUT GUSTAVE ROUSSY   (France)

^f UNIVERSITÉ PARIS SACLAY   (France)

^g UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE ISOENZYME 2; ANTIRETROVIRUS AGENT; CALPHOBINDIN II; CHAPERONE; DIDANOSINE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 60; LAMIVUDINE; MITOCHONDRIAL ENZYME; PROHIBITIN; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RAB PROTEIN; STAVUDINE; ZIDOVUDINE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; REPRESSOR PROTEIN; RNA DIRECTED DNA POLYMERASE INHIBITOR;

ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; ENERGY YIELD; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; LIPODYSTROPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRIAL TOXICITY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEOMICS; RISK ASSESSMENT; TIME OF FLIGHT MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS; VALIDATION PROCESS; DRUG EFFECTS; ENZYMOLOGY; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS 1; MASS SPECTROMETRY; METABOLISM; MITOCHONDRION; PATHOLOGY; PATHOPHYSIOLOGY;

ANTI-HIV AGENTS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; DOWN-REGULATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HIV INFECTIONS; HIV-1; HUMANS; MITOCHONDRIA; PROTEOMICS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE INHIBITORS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STAVUDINE; ZIDOVUDINE;

EID: 77952919203     PISSN: 13596535     EISSN: None     Source Type: Journal    
DOI: 10.3851/IMP1530     Document Type: Article

References (50)

1. Palella FJ, Jr., Delaney KM, Moorman AC, et al. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl J Med 1998; 338:853-860.
2. Mocroft A, Ledergerber B, Katlama C, et al. Decline in the AIDS and death rates in the EuroSIDA study: an observational study. Lancet 2003; 362:22-29. (Pubitemid 36835816)
3. d'Armino Monforte A, Lepri AC, Rezza G, et al. Insights into the reasons for discontinuation of the first highly active antiretroviral therapy (HAART) regimen in a cohort of antiretroviral naive patients. AIDS 2000; 14:499-507.
4. Gerschenson M, Brinkman K. Mitochondrial dysfunction in AIDS and its treatment. Mitochondrion 2004; 4:763-777.
5. Brinkman K, Smeitink JA, Romijn JA, Reiss P. Mitochondrial toxicity induced by nucleoside-analogue reverse-transcriptase inhibitors is a key factor in the pathogenesis of antiretroviral-therapy-related lipodystrophy. Lancet 1999; 354:1112-1115. (Pubitemid 29452832)
6. McComsey GA, Walker UA. Role of mitochondria in HIV lipoatrophy: insight into pathogenesis and potential therapies. Mitochondrion 2004; 4:111-118.
7. Grinspoon S, Carr A. Cardiovascular risk and body-fat abnormalities in HIV-infected adults. N Engl J Med 2005; 352:48-62. (Pubitemid 40075680)
8. Petit F, Fromenty B, Owen A, Estaquier J. Mitochondria are sensors for HIV drugs. Trends Pharmacol Sci 2005; 26:258-264. (Pubitemid 40603074)
9. Lewis W, Day BJ, Copeland WC. Mitochondrial toxicity of NRTI antiviral drugs: an integrated cellular perspective. Nat Rev Drug Discov 2003; 2:812-822. (Pubitemid 37361813)
10. DiMauro S, Schon EA. Mitochondrial respiratory-chain diseases. N Engl J Med 2003; 348:2656-2668.
11. Brinkman K, ter Hofstede HJ, Burger DM, Smeitink JA, Koopmans PP. Adverse effects of reverse transcriptase inhibitors: mitochondrial toxicity as common pathway. AIDS 1998; 12:1735-1744.
12. Moyle G. Mechanisms of HIV and nucleoside reverse transcriptase inhibitor injury to mitochondria. Antivir Ther 2005; 10 Suppl 2:M47-M52.
13. Llibre JM, Domingo P, Palacios R, et al. Sustained improvement of dyslipidaemia in HAART-treated patients replacing stavudine with tenofovir. AIDS 2006; 20:1407-1414. (Pubitemid 43948247)
14. Gallant JE, DeJesus E, Arribas JR, et al. Tenofovir DF, emtricitabine, and efavirenz vs. zidovudine, lamivudine, and efavirenz for HIV. N Engl J Med 2006; 354:251-260.
15. Lewis W. Mitochondrial dysfunction and nucleoside reverse transcriptase inhibitor therapy: experimental clarifications and persistent clinical questions. Antiviral Res 2003; 58:189-197. (Pubitemid 36589009)
16. Cote HC, Brumme ZL, Craib KJ, et al. Changes in mitochondrial DNA as a marker of nucleoside toxicity in HIV-infected patients. N Engl J Med 2002; 346:811-820.
17. Cote HC. Possible ways nucleoside analogues can affect mitochondrial DNA content and gene expression during HIV therapy. Antivir Ther 2005; 10 Suppl 2:M3-M11.
18. Casula M, Weverling GJ, Wit FW, et al. Mitochondrial DNA and RNA increase in peripheral blood mononuclear cells from HIV-1-infected patients randomized to receive stavudine-containing or stavudine-sparing combination therapy. J Infect Dis 2005; 192:1794-1800. (Pubitemid 41587831)
19. Mallon PW, Unemori P, Sedwell R, et al. In vivo, nucleoside reverse-transcriptase inhibitors alter expression of both mitochondrial and lipid metabolism genes in the absence of depletion of mitochondrial DNA. J Infect Dis 2005; 191:1686-1696.
20. Gerschenson M, Shiramizu B, LiButti DE, Shikuma CM. Mitochondrial DNA levels of peripheral blood mononuclear cells and subcutaneous adipose tissue from thigh, fat and abdomen of HIV-1 seropositive and negative individuals. Antivir Ther 2005; 10 Suppl 2:M83-M89.
21. Cossarizza A, Riva A, Pinti M, et al. Increased mitochondrial DNA content in peripheral blood lymphocytes from HIV-infected patients with lipodystrophy. Antivir Ther 2003; 8:315-321. (Pubitemid 37101635)
22. Macho A, Castedo M, Marchetti P, et al. Mitochondrial dysfunctions in circulating T lymphocytes from human immunodeficiency virus-1 carriers. Blood 1995; 86:2481-2487.
23. Miro O, Lopez S, Martinez E, et al. Mitochondrial effects of HIV infection on the peripheral blood mononuclear cells of HIV-infected patients who were never treated with antiretrovirals. Clin Infect Dis 2004; 39:710-716. (Pubitemid 39180445)
24. Gougeon ML. Apoptosis as an HIV strategy to escape immune attack. Nat Rev Immunol 2003; 3:392-404.
25. Maagaard A, Holberg-Petersen M, Kvittingen EA, Sandvik L, Bruun JN. Depletion of mitochondrial DNA copies/cell in peripheral blood mononuclear cells in HIV-1-infected treatment-naive patients. HIV Med 2006; 7:53-58.
26. Cossarizza A, Moyle G. Antiretroviral nucleoside and nucleotide analogues and mitochondria. AIDS 2004; 18:137-151. (Pubitemid 38253435)
27. Nijtmans LG, Artal SM, Grivell LA, Coates PJ. The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell Mol Life Sci 2002; 59:143-155.
28. Steglich G, Neupert W, Langer T. prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol Cell Biol 1999; 19:3435-3442. (Pubitemid 29193803)
29. Merkwirth C, Dargazanli S, Tatsuta T, et al. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 2008; 22:476-488. (Pubitemid 351272755)
30. Mishra S, Murphy LC, Murphy LJ. The prohibitins: emerging roles in diverse functions. J Cell Mol Med 2006; 10:353-363. (Pubitemid 44870184)
31. Merkwirth C, Langer T. Prohibitin function within mitochondria: essential roles for cell proliferation and cristae morphogenesis. Biochim Biophys Acta 2009; 1793:27-32.
32. Theiss AL, Idell RD, Srinivasan S, et al. Prohibitin protects against oxidative stress in intestinal epithelial cells. FASEB J 2007; 21:197-206. (Pubitemid 46052557)
33. Ross JA, Nagy ZS, Kirken RA. The PHB1/2 phosphocomplex is required for mitochondrial homeostasis and survival of human T cells. J Biol Chem 2008; 283:4699-4713.
34. Kasashima K, Sumitani M, Satoh M, Endo H. Human prohibitin 1 maintains the organization and stability of the mitochondrial nucleoids. Exp Cell Res 2008; 314:988-996.
35. Agsteribbe E, Huckriede A, Veenhuis M, et al. A fatal, systemic mitochondrial disease with decreased mitochondrial enzyme activities, abnormal ultrastructure of the mitochondria and deficiency of heat shock protein 60. Biochem Biophys Res Commun 1993; 193:146-154. (Pubitemid 23199925)
36. MacKenzie JA, Payne RM. Mitochondrial protein import and human health and disease. Biochim Biophys Acta 2007; 1772:509-523. (Pubitemid 46589979)
37. Chan EY, Sutton JN, Jacobs JM, Bondarenko A, Smith RD, Katze MG. Dynamic host energetics and cytoskeletal proteomes in human immunodeficiency virus type 1-infected human primary CD4 cells: analysis by multiplexed labelfree mass spectrometry. J Virol 2009; 83:9283-9295.
38. Ringrose JH, Jeeninga RE, Berkhout B, Speijer D. Proteomic studies reveal coordinated changes in T-cell expression patterns upon infection with human immunodeficiency virus type 1. J Virol 2008; 82:4320-4330. (Pubitemid 351563669)
39. Chan EY, Qian WJ, Diamond DL, et al. Quantitative analysis of human immunodeficiency virus type 1-infected CD4+ cell proteome: dysregulated cell cycle progression and nuclear transport coincide with robust virus production. J Virol 2007; 81:7571-7583.
40. Frederick RL, Shaw JM. Moving mitochondria: establishing distribution of an essential organelle. Traffic 2007; 8:1668-1675.
41. Boldogh IR, Pon LA. Mitochondria on the move. Trends Cell Biol 2007; 17:502-510.
42. Anesti V, Scorrano L. The relationship between mitochondrial shape and function and the cytoskeleton. Biochim Biophys Acta 2006; 1757:692-699. (Pubitemid 43993860)
43. Bellomo G, Mirabelli F. Oxidative stress and cytoskeletal alterations. Ann N Y Acad Sci 1992; 663:97-109.
44. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001; 81:807-869. (Pubitemid 32267078)
45. Ouasti S, Matarrese P, Paddon R, et al. Death receptor ligation triggers membrane scrambling between Golgi and mitochondria. Cell Death Differ 2007; 14:453-461. (Pubitemid 46259953)
46. Strzelecka-Kiliszek A, Buszewska ME, Podszywalow-Bartnicka P, et al. Calcium- and pH-dependent localization of annexin A6 isoforms in Balb/3T3 fibroblasts reflecting their potential participation in vesicular transport. J Cell Biochem 2008; 104:418-434. (Pubitemid 351671632)
47. Sklan EH, Serrano RL, Einav S, Pfeffer SR, Lambright DG, Glenn JS. TBC1D20 is a Rab1 GTPase-activating protein that mediates hepatitis C virus replication. J Biol Chem 2007; 282:36354-36361.
48. Nguyen DH, Hildreth JE. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J Virol 2000; 74:3264-3272.
49. Fust G, Beck Z, Banhegyi D, Kocsis J, Biro A, Prohaszka Z. Antibodies against heat shock proteins and cholesterol in HIV infection. Mol Immunol 2005; 42:79-85. (Pubitemid 39360929)
50. The Strategies for Management of Antiretroviral Therapy (SMART) Study Group. Major clinical outcomes in antiretroviral therapy (ART)-naive participants and in those not receiving ART at baseline in the SMART study. J Infect Dis 2008; 197:1133-1144.