Depleted skeletal muscle mitochondrial DNA, hyperlactatemia, and decreased oxidative capacity in HIV-infected patients on highly active antiretroviral therapy

Journal of Medical Virology

Volumn 77, Issue 1, 2005, Pages 29-38

  Haugaard, Steen B ^a   Andersen, Ove ^a   Pedersen, Steen B ^b,c   Dela, Flemming ^d   Richelsen, Bjørn ^b,c   Nielsen, Jens Ole ^a   Madsbad, Sten ^a   Iversen, Johan ^a  

^a HVIDOVRE HOSPITAL   (Denmark)

^b Aarhus Amtsygehus ^*  (Denmark)

^c AARHUS UNIVERSITY HOSPITAL   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Glucose oxidation; Mitochondrial DNA; Nucleoside reverse transcriptase inhibitor; Skeletal muscle; Toxicity

Indexed keywords

DIDANOSINE; DNA DIRECTED DNA POLYMERASE GAMMA; EFAVIRENZ; INDINAVIR; LACTIC ACID; LAMIVUDINE; MITOCHONDRIAL DNA; NELFINAVIR; RITONAVIR; RNA DIRECTED DNA POLYMERASE INHIBITOR; SAQUINAVIR; STAVUDINE; ZIDOVUDINE;

ADULT; AEROBIC CAPACITY; ARTICLE; CALORIMETRY; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; GLUCOSE OXIDATION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HIV ASSOCIATED LIPODYSTROPHY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; HYPERLACTATEMIA; INFLAMMATION; MITOCHONDRIAL RESPIRATION; SKELETAL MUSCLE;

ADULT; ANTI-HIV AGENTS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; DNA, MITOCHONDRIAL; GENE DELETION; HIV INFECTIONS; HUMANS; LACTIC ACID; MIDDLE AGED; MITOCHONDRIAL DISEASES; MUSCLE, SKELETAL; OXIDATION-REDUCTION;

EID: 23044453130     PISSN: 01466615     EISSN: None     Source Type: Journal    
DOI: 10.1002/jmv.20410     Document Type: Article

References (57)

1. Andersen O, Haugaard SB, Andersen UB, Friis-Moller N, Storgaard H, Volund A, Nielsen JO, Iversen J, Madsbad S. 2003. Lipodystrophy in human immunodeficiency virus patients impairs insulin action and induces defects in beta-cell function. Metabolism 52:1343-1353.
2. Arnaudo E, Dalakas M, Shanske S, Moraes CT, Dimauro S, Schon EA. 1991. Depletion of muscle mitochondrial DNA in AIDS patients with zidovudine-induced myopathy. Lancet 337:508-510.
3. Bernasconi E, Boubaker K, Junghans C, Flepp M, Furrer HJ, Haensel A, Hirschel B, Boggian K, Chave JP, Opravil M, Weber R, Rickenbach M, Telenti A. 2002. Abnormalities of body fat distribution in HIV-infected persons treated with antiretroviral drugs: The Swiss HIV Cohort Study. J Acquir Immune Defic Syndr 31:50-55.
4. Boubaker K, Flepp M, Sudre P, Furrer H, Haensel A, Hirschel B, Boggian K, Chave JP, Bernasconi E, Egger M, Opravil M, Rickenbach M, Francioli P, Telenti A. 2001. Hyperlactatemia and antiretroviral therapy: The Swiss HIV Cohort Study. Clin Infect Dis 33:1931-1937.
5. Brinkman K. 2001. Evidence for mitochondrial toxicity: Lactic acidosis as proof of concept. J HIV Ther 6:13-16.
6. Brinkman K, ter Hofstede HJ, Burger DM, Smeitink JA, Koopmans PP. 1998. Adverse effects of reverse transcriptase inhibitors: Mitochondrial toxicity as common pathway. AIDS 12:1735-1744.
7. Brinkman K, Smeitink JA, Romijn JA, Reiss P. 1999. Mitochondrial toxicity induced by nucleoside-analog reverse-transcriptase inhibitors is a key factor in the pathogenesis of antiretroviral-therapy-related lipodystrophy. Lancet 354:1112-1115.
8. Carr A, Emery S, Law M, Puls R, Lundgren JD, Powderly WG. 2003. An objective case definition of lipodystrophy in HIV-infected adults: A case-control study. Lancet 361:726-735.
9. Chen CH, Vazquez-Padua M, Cheng YC. 1991. Effect of anti-human immunodeficiency virus nucleoside analogs on mitochondrial DNA and its implication for delayed toxicity. Mol Pharmacol 39:625-628.
10. Chen D, Misra A, Garg A. 2002. Clinical review 153: Lipodystrophy in human immunodeficiency virus-infected patients. J Clin Endocrinol Metab 87:4845-4856.
11. Collins ML, Sondel N, Cesar D, Hellerstein MK. 2004. Effect of nucleoside reverse transcriptase inhibitors on mitochondrial DNA synthesis in rats and humans. J Acquir Immune Defic Syndr 37: 1132-1139.
12. Cossarizza A, Mussini C, Mongiardo N, Borghi V, Sabbatini A, De Rienzo B, Franceschi C. 1997. Mitochondria alterations and dramatic tendency to undergo apoptosis in peripheral blood lymphocytes during acute HIV syndrome. AIDS 11:19-26.
13. Cossarizza A, Mussini C, Vigano A. 2001. Mitochondria in the pathogenesis of lipodystrophy induced by anti-HIV antiretroviral drugs: Actors or bystanders? Bioessays 23:1070-1080.
14. Cossarizza A, Pinti M, Moretti L, Bricalli D, Bianchi R, Troiano L, Fernandez MG, Balli F, Brambilla P, Mussini C, Vigano A. 2002. Mitochondrial functionality and mitochondrial DNA content in lymphocytes of vertically infected human immunodeficiency virus-positive children with highly active antiretroviral therapy-related lipodystrophy. J Infect Dis 185:299-305.
15. Cote HC, Brumme ZL, Craib KJ, Alexander CS, Wynhoven B, Ting L, Wong H, Harris M, Harrigan PR, O'Shaughnessy MV, Montaner JS. 2002. Changes in mitochondrial DNA as a marker of nucleoside toxicity in HIV-infected patients. N Engl J Med 346:811-820.
16. Cui L, Locatelli L, Xie MY, Sommadossi JP. 1997. Effect of nucleoside analogs on neurite regeneration and mitochondrial DNA synthesis in PC-12 cells. J Pharmacol Exp Ther 280:1228-1234.
17. DeFronzo RA, Tobin JD, Andres R. 1979. Glucose clamp technique: A method for quantifying insulin secretion and resistance. Am J Physiol 237:E214-E223.
18. Ferri KF, Jacotot E, Blanco J, Este JA, Kroemer G. 2000. Mitochondrial control of cell death induced by HIV-1-encoded proteins. Ann N Y Acad Sci 926:149-164.
19. Fogh-Andersen N, D'Orazio P. 1998. Proposal for standardizing direct-reading biosensors for blood glucose. Clin Chem 44:655-659.
20. Foli A, Benvenuto F, Piccinini G, Bareggi A, Cossarizza A, Lisziewicz J, Lori F. 2001. Direct analysis of mitochondrial toxicity of antiretroviral drugs. AIDS 15:1687-1694.
21. Frayn KN. 1983. Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol 55:628-634.
22. Gallant JE, Staszewski S, Pozniak AL, DeJesus E, Suleiman JM, Miller MD, Coakley DF, Lu B, Toole JJ, Cheng AK. 2004. Efficacy and safety of tenofovir DF versus stavudine in combination therapy in antiretroviral-naive patients: A 3-year randomized trial. JAMA 292:191-201.
23. + subjects. Immunol Invest 30:267-287.
24. Haugaard SB, Andersen O, Storgaard H, Dela F, Holst JJ, Iversen J, Nielsen JO, Madsbad S. 2004. Insulin secretion in lipodystrophic HIV-infected patients is associated with high levels of nonglucose secretagogs and insulin resistance of beta-cells. Am J Physiol Endocrinol Metab 287:E677-E685.
25. Heitmann BL. 1990. Prediction of body water and fat in adult Danes from measurement of electrical impedance. A validation study. Int J Obes 14:789-802.
26. Holloszy JO, Booth FW. 1976. Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol 38:273-291.
27. Hruz PW, Murata H, Qiu H, Mueckler M. 2002. Indinavir induces acute and reversible peripheral insulin resistance in rats. Diabetes 51:937-942.
28. Jensen CB, Storgaard H, Dela F, Holst JJ, Madsbad S, Vaag AA. 2002. Early differential defects of insulin secretion and action in 19-year-old caucasian men who had low birth weight. Diabetes 51:1271-1280.
29. John M, Moore CB, James IR, Nolan D, Upton RP, McKinnon EJ, Mallal SA. 2001. Chronic hyperlactatemia in HIV-infected patients taking antiretroviral therapy. AIDS 15:717-723.
30. Juel C, Holten MK, Dela F. 2004. Effects of strength training on muscle lactate release and MCT1 and MCT4 content in healthy and type 2 diabetic humans. J Physiol 556:297-304.
31. Lee H, Hanes J, Johnson KA. 2003. Toxicity of nucleoside analogs used to treat AIDS and the selectivity of the mitochondrial DNA polymerase. Biochemistry 42:14711-14719.
32. Lonergan JT, Barber RE, Mathews WC. 2003. Safety and efficacy of switching to alternative nucleoside analogs following symptomatic hyperlactatemia and lactic acidosis. AIDS 17:2495-2499.
33. Lonergan JT, McComsey GA, Fisher RL, Shalit P, File TM, Ward DJ, Williams VC, Hessenthaler SM, Lindsey L, Hernandez JE. 2004. Lack of recurrence of hyperlactatemia in HIV-infected patients switched from Stavudine to Abacavir or Zidovudine. J Acquir Immune Defic Syndr 36:935-942.
34. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. 1985. Homeostasis model assessment: Insulin resistance and beta-cell function from fastingplasma glucose and insulin concentrations in man. Diabetologia 28:412-419.
35. McComsey G, Lonergan JT. 2004. Mitochondrial dysfunction: Patient monitoring and toxicity management. J Acquir Immune Defic Syndr 37:S30-S35.
36. McComsey G, Tan DJ, Lederman M, Wilson E, Wong LJ. 2002. Analysis of the mitochondrial DNA genome in the peripheral blood leukocytes of HIV-infected patients with or without lipoatrophy. AIDS 16:513-518.
37. McComsey GA, Ward DJ, Hessenthaler SM, Sension MG, Shalit P, Lonergan JT, Fisher RL, Williams VC, Hernandez JE. 2004. Improvement in lipoatrophy associated with highly active antiretroviral therapy in human immunodeficiency virus-infected patients switched from stavudine to abacavir or zidovudine: The results of the TARHEEL study. Clin Infect Dis 38:263-270.
38. McComsey GA, Paulsen DM, Lonergan JT, Hessenthaler SM, Hoppel CL, Williams VC, Fisher RL, Cherry CL, White-Owen C, Thompson KA, Ross ST, Hernandez JE, Ross LL. 2005. Improvements in lipoatrophy, mitochondrial DNA levels and fat apoptosis after replacing stavudine with abacavir or zidovudine. AIDS 19:15-23.
39. Medina DJ, Tsai CH, Hsiung GD, Cheng YC. 1994. Comparison of mitochondrial morphology, mitochondrial DNA content, and cell viability in cultured cells treated with three anti-human immunodeficiency virus dideoxynucleosides. Antimicrob Agents Chemother 38:1824-1828.
40. Miro O, Lopez S, Martinez E, Pedrol E, Milinkovic A, Deig E, Garrabou G, Casademont J, Gatell JM, Cardellach F. 2004. Mitochondrial effects of HIV infection on the peripheral blood mononuclear cells of HIV-infected patients who were never treated with antiretrovirals. Clin Infect Dis 39:710-716.
41. Miura T, Goto M, Hosoya N, Odawara T, Kitamura Y, Nakamura T, Iwamoto A. 2003. Depletion of mitochondrial DNA in HIV-1-infected patients and its amelioration by antiretroviral therapy. J Med Virol 70:497-505.
42. Moyle GJ, Sadler M. 1998. Peripheral neuropathy with nucleoside antiretrovirals: Risk factors, incidence and management. Drug Saf 19:481-494.
43. Nolan D, Hammond E, Martin A, Taylor L, Herrmann S, McKinnon E, Metcalf C, Latham B, Mallal S. 2003. Mitochondrial DNA depletion and morphologic changes in adipocytes associated with nucleoside reverse transcriptase inhibitor therapy. AIDS 17:1329-1338.
44. Pesce V, Cormio A, Fracasso F, Vecchiet J, Felzani G, Lezza AM, Cantatore P, Gadaleta MN. 2001. Age-related mitochondrial genotypic and phenotypic alterations in human skeletal muscle. Free Radic Biol Med 30:1223-1233.
45. Polo R, Martinez S, Madrigal P, Gonzalez-Munoz M. 2003. Factors associated with mitochondrial dysfunction in circulating peripheral blood lymphocytes from HIV-infected people. J Acquir Immune Defic Syndr 34:32-36.
46. Rodriguez-Santiago B, Casademont J, Nunes V. 2001. Is mitochondrial DNA depletion involved in Alzheimer's disease? Eur J Hum Genet 9:279-285.
47. Rossignol R, Malgat M, Mazat JP, Letellier T. 1999. Threshold effect and tissue specificity. Implication for mitochondrial cytopathies. J Biol Chem 274:33426-33432.
48. Saag MS, Cahn P, Raffi F, Wolff M, Pearce D, Molina JM, Powderly W, Shaw AL, Mondou E, Hinkle J, Borroto-Esoda K, Quinn JB, Barry DW, Rousseau F. 2004. Efficacy and safety of emtricitabine versus stavudine in combination therapy in antiretroviral-naive patients: A randomized trial. JAMA 292:180-189.
49. Sande MA, Ronald A. 2004. Treatment of HIV/AIDS: Do the dilemmas only increase? JAMA 292:266-268.
50. Stacpoole PW. 1997. Lactic acidosis and other mitochondrial disorders. Metabolism 46:306-321.
51. Vaag A, Lehtovirta M, Thye-Ronn P, Groop L. 2001. Metabolic impact of a family history of Type 2 diabetes. Results from a European multicentre study (EGIR). Diabet Med 18:533-540.
52. Velsor LW, Kovacevic M, Goldstein M, Leitner HM, Lewis W, Day BJ. 2004. Mitochondrial oxidative stress in human hepatoma cells exposed to stavudine. Toxicol Appl Pharmacol 199:10-19.
53. Vittecoq D, Jardel C, Barthelemy C, Escaut L, Cheminot N, Chapin S, Sternberg D, Maisonobe T, Lombes A. 2002. Mitochondrial damage associated with long-term antiretroviral treatment: Associated alteration or causal disorder? J Acquir Immune Defic Syndr 31:299-308.
54. Walker UA. 2001. Clinical manifestations of mitochondrial toxicity. J HIV Ther 6:17-21.
55. Walker UA, Bickel M, Lutke Volksbeck SI, Ketelsen UP, Schofer H, Setzer B, Venhoff N, Rickerts V, Staszewski S. 2002. Evidence of nucleoside analog reverse transcriptase inhibitor-associated genetic and structural defects of mitochondria in adipose tissue of HIV-infected patients. J Acquir Immune Defic Syndr 29:117-121.
56. White AJ. 2001. Mitochondrial toxicity and HIV therapy. Sex Transm Infect 77:158-173.
57. Zaera MG, Miro O, Pedrol E, Soler A, Picon M, Cardellach F, Casademont J, Nunes V. 2001. Mitochondrial involvement in antiretroviral therapy-related lipodystrophy. AIDS 15:1643-1651.