Tobacco smoking effect on HIV-1 pathogenesis: Role of cytochrome P450 isozymes

Expert Opinion on Drug Metabolism and Toxicology

Volumn 9, Issue 11, 2013, Pages 1453-1464

  Ande, Anusha ^a   McArthur, Carole ^a   Kumar, Anil ^a   Kumar, Santosh ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

Cytochrome p450; HIV 1; Nicotine; Oxidative stress; Smoking tobacco

Indexed keywords

CYTOCHROME P450 ISOENZYME;

ASTROCYTE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOCYTE; MACROPHAGE; MONOCYTE; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; REVIEW; SMOKING; TOBACCO; VIRUS REPLICATION;

ANTI-RETROVIRAL AGENTS; ASTROCYTES; CYTOCHROME P-450 ENZYME SYSTEM; DRUG INTERACTIONS; HIV INFECTIONS; HIV-1; HUMANS; LYMPHOCYTES; MACROPHAGES; MONOCYTES; NEURONS; NF-E2-RELATED FACTOR 2; NICOTINE; OXIDATIVE STRESS; PROTEIN KINASE C; SIGNAL TRANSDUCTION; SMOKING; TOBACCO; VIRUS REPLICATION;

EID: 84886043288     PISSN: 17425255     EISSN: 17447607     Source Type: Journal    
DOI: 10.1517/17425255.2013.816285     Document Type: Review

References (100)

1. Global HIV/AIDS Response, Epidemic update and health sector progress towards Universal Access; Progress Report 2011
2. Okeudo C, Ezem BU, Ojiyi EC. Human immuno-deficiency virus antibody seroprevalence among pregnant women at booking at a university teaching hospital in South-Eastern Nigeria. Niger J Med 2012(2):227-30
3. Bork K, Cames C, Cournil A, et al. Infant feeding modes and determinants among HIV-1-infected African Women in the Kesho Bora Study. J Acquir Immune defic syndr 2013;62(1):109-18
4. Rempel H, Sun B, Calosing C, et al. Monocyte Activation in HIV/HCV Coinfection Correlates with Cognitive Impairment. PLoS ONE 2013;8(2):e55776
5. Gray JM, Cohn DL. Tuberculosis and HIV Coinfection. Semin Respir Crit Care Med 2013;34(1):32-43
6. Burgoyne RW, Tan DH. Prolongation and quality of life for HIV-infected adults treated with highly active antiretroviral therapy (HAART): a balancing act. J Antimicrob Chemother 2008;61(3):469-73 (Pubitemid 351321116)
7. Xia C, Luo D, Yu X, et al. HIV-associated dementia in the era of highly active antiretroviral therapy (HAART). Microbes and infection/Institut Pasteur 2011;13(5):419-25
8. Mothobi NZ, Brew BJ. Neurocognitive dysfunction in the highly active antiretroviral therapy era. Curr Opin Infect Dis 2012;25(1):4-9
9. Vivithanaporn P, Gill MJ, Power C. Impact of current antiretroviral therapies on neuroAIDS. Expert Rev Anti Infect Ther 2011;9(4):371-4
10. Purohit V, Rapaka R, Shurtleff D. Drugs of abuse, dopamine, and HIV-associated neurocognitive disorders/HIV-associated dementia. Mol Neurobiol 2011;44(1):102-10
11. Unique interactions between tobacco use and HIV/AIDS (R03) PA-08-254. In: (NIDA) NIoDA, editor. Bethesda; Maryland 20892: 2009. Available from: http://grants.nih.gov/grants/guide/pa-files/PA-08-254.html
12. Messner B, Frotschnig S, Steinacher-Nigisch A, et al. Apoptosis and necrosis: two different outcomes of cigarette smoke condensate-induced endothelial cell death. Cell death disease 2012;3:e424
13. Murray CJ, Lopez AD. Alternative projections of mortality and disability by cause 1990-2020: global Burden of Disease Study. Lancet 1997;349(9064):1498- 504 (Pubitemid 27216360)
14. Burkhalter JE, Springer CM, Chhabra R, et al. Tobacco use and readiness to quit smoking in low-income HIV-infected persons. Nicotine Tob Res 2005;7(4):511-22 (Pubitemid 41600909)
15. Cigarette Smoking Among Adults-United States, 2004: CDC; 2005
16. Feldman JG, Minkoff H, Schneider MF, et al. Association of cigarette smoking with HIV prognosis among women in the HAART era: a report from the women's interagency HIV study. Am J Public Health 2006;96(6):1060-5 (Pubitemid 43825275)
17. Kalra R, Singh SP, Pena-Philippides JC, et al. Immunosuppressive and anti-inflammatory effects of nicotine administered by patch in an animal model. Clin Diagn Lab Immunol 2004;11(3):563-8 (Pubitemid 38661424)
18. Sopori M. Effects of cigarette smoke on the immune system. Nature Rev Immunol 2002;2(5):372-7 (Pubitemid 37328760)
19. Singh SP, Kalra R, Puttfarcken P, et al. Acute and chronic nicotine exposures modulate the immune system through different pathways. Toxicol Appl Pharmacol 2000;164(1):65-72 (Pubitemid 30198545)
20. Hodge-Bell KC, Lee KM, Renne RA, et al. Pulmonary inflammation in mice exposed to mainstream cigarette smoke. Inhal Toxicol 2007;19(4):361-76 (Pubitemid 46294849)
21. Razani-Boroujerdi S, Singh SP, Knall C, et al. Chronic nicotine inhibits inflammation and promotes influenza infection. Cell Immunol 2004;230(1):1-9 (Pubitemid 39482356)
22. McMaster SK, Paul-Clark MJ, Walters M, et al. Cigarette smoke inhibits macrophage sensing of Gram-negative bacteria and lipopolysaccharide: relative roles of nicotine and oxidant stress. Br J Pharmacol 2008;153(3):536-43 (Pubitemid 351199021)
23. Yamaguchi Y, Nasu F, Harada A, Kunitomo M. Oxidants in the gas phase of cigarette smoke pass through the lung alveolar wall and raise systemic oxidative stress. J Pharmacol Sci 2007;103(3):275-82 (Pubitemid 46465770)
24. Abbud RA, Finegan CK, Guay LA, Rich EA. Enhanced production of human immunodeficiency virus type 1 by in vitro-infected alveolar macrophages from otherwise healthy cigarette smokers. J Infect Dis 1995;172(3):859-63
25. Rock RB, Gekker G, Aravalli RN, et al. Potentiation of HIV-1 expression in microglial cells by nicotine: involvement of transforming growth factor-beta J Neuroimmune Pharmacol 2008;3(3):143-9
26. Zhao L, Li F, Zhang Y, et al. Mechanisms and genes involved in enhancement of HIV infectivity by tobacco smoke. Toxicology 2010;278(2):242-8
27. Boelaert JR, Piette J, Weinberg GA, et al. Iron and oxidative stress as a mechanism for the enhanced production of human immunodeficiency virus by alveolar macrophages from otherwise healthy cigarette smokers. J Infect Dis 1996;173(4):1045-7
28. Ghosh D, Mishra MK, Das S, et al. Tobacco carcinogen induces microglial activation and subsequent neuronal damage. J Neurochem 2009;110(3):1070-81
29. Bao Z, He XY, Ding X, et al. Metabolism of nicotine and cotinine by human cytochrome P450 2A13. Drug metab Dispos 2005;33(2):258-61 (Pubitemid 40216593)
30. Smith TJ, Liao AM, Liu Y, et al. Enzymes involved in the bioactivation of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in patas monkey lung and liver microsomes. Carcinogenesis 1997;18(8):1577-84 (Pubitemid 28134782)
31. Helleberg M, Afzal S, Kronborg G, et al. Mortality attributable to smoking among HIV-1-infected individuals: a nationwide, population-based cohort study. Clin Infect Dis 2013;56(5):727-34
32. Minkoff H, Feldman JG, Strickler HD, et al. Relationship between smoking and human papillomavirus infections in HIV-infected and-uninfected women. J Infect Dis 2004;189(10):1821-8 (Pubitemid 38657218)
33. Kaner RJ, Santiago F, Crystal RG. Up-regulation of alveolar macrophage matrix metalloproteinases in HIV1(+) smokers with early emphysema. J Leukoc Biol 2009;86(4):913-22
34. Marshall MM, McCormack MC, Kirk GD. Effect of cigarette smoking on HIV acquisition, progression, and mortality. AIDS Educ Prev 2009;21(3 Suppl):28-39
35. Chuang CH, Hu ML. Synergistic DNA damage and lipid peroxidation in cultured human white blood cells exposed to 4-(methyl-nitrosamino)-1-(3-pyridyl) -1-butanone and ultraviolet A. Environ Mol Mutagen 2006;47(2):73-81
36. Wojna V, Robles L, Skolasky RL, et al. Associations of cigarette smoking with viral immune and cognitive function in human immunodeficiency virus-seropositive women. J Neurovirol 2007;13(6):561-8
37. Manda VK, Mittapalli RK, Geldenhuys WJ, Lockman PR. Chronic exposure to nicotine and saquinavir decreases endothelial Notch-4 expression and disrupts blood-brain barrier integrity. J Neurochem 2010;115(2):515-25
38. Benowitz NL. Pharmacology of nicotine: addiction, smoking-induced disease, and therapeutics. Annu Rev Pharmacol Toxicol 2009;49:57-71
39. Benowitz NL, Hukkanen J, Jacob P III. Nicotine chemistry, metabolism, kinetics and biomarkers. Handb Exp Pharmacol 2009;192:29-60
40. Hernando-Rodriguez M, Rey-Barja N, Marichalar-Mendia X, et al. Role of cytochrome P-450 genetic polymorphisms in oral carcinogenesis. J Oral Pathol Med 2012;41(1):1-8
41. Kulbacka J, Saczko J, Chwilkowska A. Oxidative stress in cells damage processes. Pol Merkur Lekarski 2009;27(157):44-7
42. Murphy SE, Raulinaitis V, Brown KM. Nicotine 5'-oxidation and methyl oxidation by P450 2A enzymes. Drug Metab Dispos 2005;33(8):1166-73 (Pubitemid 41043760)
43. Hukkanen J, Jacob P III, Benowitz NL. Metabolism and disposition kinetics of nicotine. Pharmacol Rev 2005;57(1):79-115 (Pubitemid 40283970)
44. Wong HL, Zhang X, Zhang QY, et al. Metabolic activation of the tobacco carcinogen 4-(methylnitrosamino)-(3-pyridyl)-1-butanone by cytochrome P450 2A13 in human fetal nasal microsomes. Chem Res Toxicol 2005;18(6):913-18 (Pubitemid 40880879)
45. Guo L, Zhang C, Shi S, Guo X. Correlation between smoking and the polymorphisms of cytochrome P450 1A1-Msp I and glutathione S-transferase T1 genes and oral cancer. Hua Xi Kou Qiang Yi Xue Za Zhi 2012;30(2):187-91
46. Chi AC, Appleton K, Henriod JB, et al. Differential induction of CYP1A1 and CYP1B1 by benzo[a]pyrene in oral squamous cell carcinoma cell lines and by tobacco smoking in oral mucosa. Oral Oncol 2009;45(11):980-5
47. Igarashi T, Brown CR, Endo Y, et al. Macrophage are the principal reservoir and sustain high virus loads in rhesus macaques after the depletion of CD4+ T cells by a highly pathogenic simian immunodeficiency virus/HIV type 1 chimera (SHIV): implications for HIV-1 infections of humans. Proc Natl Acad Sci USA 2001;98(2):658-63 (Pubitemid 32105099)
48. Montaner LJ, Crowe SM, Aquaro S, et al. Advances in macrophage and dendritic cell biology in HIV-1 infection stress key understudied areas in infection, pathogenesis, and analysis of viral reservoirs. J Leukoc Biol 2006;80(5):961-4 (Pubitemid 44646301)
49. Kedzierska K, Crowe SM. The role of monocytes and macrophages in the pathogenesis of HIV-1 infection. Curr Med Chem 2002;9(21):1893-903 (Pubitemid 35230257)
50. Aquaro S, Ronga L, Pollicita M, et al. Human immunodeficiency virus infection and acquired immunodeficiency syndrome dementia complex: role of cells of monocyte-macrophage lineage. J Neurovirol 2005;11(Suppl 3):58-66
51. Kim WK, Avarez X, Williams K. The role of monocytes and perivascular macrophages in HIV and SIV neuropathogenesis: information from non-human primate models. Neurotox Res 2005;8(1-2):107-15
52. Nottet HS. Interactions between macrophages and brain microvascular endothelial cells: role in pathogenesis of HIV-1 infection and blood-brain barrier function. J Neurovirol 1999;5(6):659-69 (Pubitemid 30032091)
53. Persidsky Y, Gendelman HE. Mononuclear phagocyte immunity and the neuropathogenesis of HIV-1 infection. J Leukoc Biol 2003;74(5):691-701 (Pubitemid 38040345)
54. Persidsky Y, Ghorpade A, Rasmussen J, et al. Microglial and astrocyte chemokines regulate monocyte migration through the blood-brain barrier in human immunodeficiency virus-1 encephalitis. Am J Pathol 1999;155(5):1599-611
55. Jin M, Kumar A, Kumar S. Ethanol-mediated regulation of cytochrome P450 2A6 expression in monocytes: role of oxidative stress-mediated PKC/MEK/Nrf2 pathway. PLoS One 2012;7(4):e35505
56. Jin M, Arya P, Patel K, et al. Effect of alcohol on drug efflux protein and drug metabolic enzymes in U937 macrophages. Alcohol Clin Exp Res 2011;35(1):132-9
57. Nagai F, Hiyoshi Y, Sugimachi K, Tamura HO. Cytochrome P450 (CYP) expression in human myeloblastic and lymphoid cell lines. Biol Pharm Bull 2002;25(3):383-5 (Pubitemid 39663295)
58. Hodges VM, Molloy GY, Wickramasinghe SN. Demonstration of mRNA for five species of cytochrome P450 in human bone marrow, bone marrow-derived macrophages and human haemopoietic cell lines. Br J Haematol 2000;108(1):151-6 (Pubitemid 30089947)
59. Kumar S, Jin M, Ande A, et al. Alcohol consumption effect on antiretroviral therapy and HIV-1 pathogenesis: role of cytochrome P450 isozymes. Expert Opin Drug Metab Toxicol 2012;8(11):1363-75
60. Jin M, Earla R, Shah A, et al. A LC-MS/MS method for concurrent determination of nicotine metabolites and role of CYP2A6 in nicotine metabolism in U937 macrophages: implications in oxidative stress in HIV + smokers. J Neuroimmune Pharmacol 2012;7(1):289-99
61. Aquaro S, Muscoli C, Ranazzi A, et al. The contribution of peroxynitrite generation in HIV replication in human primary macrophages. Retrovirology 2007;4:76
62. McCartney EM, Semendric L, Helbig KJ, et al. Alcohol metabolism increases the replication of hepatitis C virus and attenuates the antiviral action of interferon. J Infect Dis 2008;198(12):1766-75
63. Osna NA, White RL, Krutik VM, et al. Proteasome activation by hepatitis C core protein is reversed by ethanol-induced oxidative stress. Gastroenterology 2008;134(7):2144-52 (Pubitemid 351783253)
64. Ghosh C, Marchi N, Desai NK, et al. Cellular localization and functional significance of CYP3A4 in the human epileptic brain. Epilepsia 2011;52(3):562-71
65. Crothers K, Goulet JL, Rodriguez-Barradas MC, et al. Impact of cigarette smoking on mortality in HIV-positive and HIV-negative veterans. AIDS Edu Prev 2009;21(3 Suppl):40-53
66. Das S, Neogy S, Gautam N, Roy S. In vitro nicotine induced superoxide mediated DNA fragmentation in lymphocytes: protective role of Andrographis paniculata Nees. Toxicol In Vitro 2009;23(1):90-8
67. Kleinsasser NH, Sassen AW, Semmler MP, et al. The tobacco alkaloid nicotine demonstrates genotoxicity in human tonsillar tissue and lymphocytes. Toxicol Sci 2005;86(2):309-17 (Pubitemid 41418644)
68. Vanden Heuvel JP, Clark GC, Thompson CL, et al. CYP1A1 mRNA levels as a human exposure biomarker: use of quantitative polymerase chain reaction to measure CYP1A1 expression in human peripheral blood lymphocytes. Carcinogenesis 1993;14(10):2003-6 (Pubitemid 23311423)
69. Lambert N, Chambers SJ, Plumb GW, Williamson G. Human cytochrome P450's are pro-oxidants in iron/ascorbate-initiated microsomal lipid peroxidation. Free Radic Res 1996;24(3):177-85
70. Sharma A, Dinesh K, Yadav S, et al. Cytochrome P450 2A isoenzymes in freshly prepared blood lymphocytes isolated from rats and validation as a biomarker for clinical studies in humans. Xenobiotica 2013;43(4):311-19
71. Kranick SM, Nath A. Neurologic complications of HIV-1 infection and its treatment in the era of antiretroviral therapy. Continuum 2012;18(6 Infectious Disease):1319-37
72. Li J, Bentsman G, Potash MJ, Volsky DJ. Human immunodeficiency virus type 1 efficiently binds to human fetal astrocytes and induces neuroinflammatory responses independent of infection. BMC Neurosci 2007;8:31
73. Wang T, Gong N, Liu J, et al. HIV-1-infected astrocytes and the microglial proteome. J Neuroimmune Pharmacol 2008;3(3):173-86
74. Shah A, Singh DP, Buch S, Kumar A. HIV-1 envelope protein gp120 up regulates CCL5 production in astrocytes which can be circumvented by inhibitors of NF-kappaB pathway. Biochem Biophys Res Commun 2011;414(1):112-17
75. Shah A, Verma AS, Patel KH, et al. HIV-1 gp120 induces expression of IL-6 through a nuclear factor-kappa B-dependent mechanism: suppression by gp120 specific small interfering RNA. PLoS One 2011;6(6):e21261
76. Shah A, Kumar A. HIV-1 gp120-mediated increases in IL-8 production in astrocytes are mediated through the NF-kappaB pathway and can be silenced by gp120-specific siRNA. J Neuroinflammation 2010;7:96
77. Hawkins BT, Abbruscato TJ, Egleton RD, et al. Nicotine increases in vivo blood-brain barrier permeability and alters cerebral microvascular tight junction protein distribution. Brain Res 2004;1027(1-2):48-58 (Pubitemid 39370994)
78. Lockman PR, Van der Schyf CJ, Abbruscato TJ, Allen DD. Chronic nicotine exposure alters blood-brain barrier permeability and diminishes brain uptake of methyllycaconitine. J Neurochem 2005;94(1):37-44 (Pubitemid 40911390)
79. Ande A, Earla R, Jin M, et al. An LCMS/MS method for concurrent determination of nicotine metabolites and the role of CYP2A6 in nicotine metabolite-mediated oxidative stress in SVGA astrocytes. Drug Alcohol Depend 2012;125(1-2):49-59
80. Midde NM, Gomez AM, Harrod SB, Zhu J. Genetically expressed HIV-1 viral proteins attenuate nicotine-induced behavioral sensitization and alter mesocorticolimbic ERK and CREB signaling in rats. Pharmacol Biochem Behav 2011;98(4):587-97
81. Miksys S, Lerman C, Shields PG, et al. Smoking, alcoholism and genetic polymorphisms alter CYP2B6 levels in human brain. Neuropharmacology 2003;45(1):122-32 (Pubitemid 36700458)
82. Khokhar JY, Miksys SL, Tyndale RF. Rat brain CYP2B induction by nicotine is persistent and does not involve nicotinic acetylcholine receptors. Brain Res 2010;1348:1-9
83. Lee AM, Miksys S, Palmour R, Tyndale RF. CYP2B6 is expressed in African Green monkey brain and is induced by chronic nicotine treatment. Neuropharmacology 2006;50(4):441-50 (Pubitemid 43209040)
84. Dicke KE, Skrlin SM, Murphy SE. Nicotine and 4-(methylnitrosamino)-1-(3- pyridyl)-butanone metabolism by cytochrome P450 2B6. Drug Metab Dispos 2005;33(12):1760-4 (Pubitemid 41697258)
85. Guo X, Li W, Xin Q, et al. Vitamin C protective role for alcoholic liver disease in mice through regulating iron metabolism. Toxicol Ind Health 2011;27(4):341-8
86. Durazzo TC, Rothlind JC, Cardenas VA, et al. Chronic cigarette smoking and heavy drinking in human immunodeficiency virus: consequences for neurocognition and brain morphology. Alcohol 2007;41(7):489-501 (Pubitemid 350016708)
87. Jin M, Ande A, Kumar A, Kumar S. Regulation of cytochrome P450 2e1 expression by ethanol: role of oxidative stress-mediated pkc/jnk/sp1 pathway. Cell Death Dis 2013;4:e554
88. Corbett EL, Watt CJ, Walker N, et al. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 2003;163(9):1009-21 (Pubitemid 36548927)
89. Gadkowski LB, Hamilton CD, Allen M, et al. HIV-specific health care utilization and mortality among tuberculosis/HIV coinfected persons. AIDS Patient Care STDS 2009;23(10):845-51
90. Rabirad N, Mohammad Nejad E, Hadizadeh MR, et al. The prevalence of Tb in HIV patients and risk factor with frequent referral (Iran, 2009-10). Iran Red Crescent Med J 2013;15(1):58-61
91. Hsu O, Hill CJ, Kim M, et al. Decreased plasma efavirenz concentrations in a patient receiving rifabutin. Am J Health System Pharm 2010;67(19):1611-14
92. Breen RA, Swaden L, Ballinger J, Lipman MC. Tuberculosis and HIV coinfection: a practical therapeutic approach. Drugs 2006;66(18):2299-308 (Pubitemid 46072443)
93. Washio I, Maeda M, Sugiura C, et al. Cigarette smoke extract induces CYP2B6 through constitutive androstane receptor in hepatocytes. Drug Metab Dispos 2011;39(1):1-3
94. Wyen C, Hendra H, Siccardi M, et al. Cytochrome P450 2B6 (CYP2B6) and constitutive androstane receptor (CAR) polymorphisms are associated with early discontinuation of efavirenz-containing regimens. J Antimicrob Chemother 2011;66(9):2092-8
95. Worodria W, Menten J, Massinga-Loembe M, et al. Clinical spectrum, risk factors and outcome of immune reconstitution inflammatory syndrome in patients with tuberculosis-HIV coinfection. Antivir Ther 2012;17(5):841-8
96. Meintjes G, Lawn SD, Scano F, et al. Tuberculosis-associated immune reconstitution inflammatory syndrome: case definitions for use in resource-limited settings. Lancet Infect Dis 2008;8(8):516-23 (Pubitemid 352005824)
97. Kabue JP, de Swardt D, de Beer C, Glashoff RH. Short-term antiretroviral therapy fails to reduce the expanded activated ccr5-expressing CD4(+) T lymphocyte population or to restore the depleted naive population in chronically hiv-infected individuals with active pulmonary tuberculosis. AIDS Res Hum Retroviruses 2013;29(5):769-77
98. Bourgarit A, Carcelain G, Martinez V, et al. Explosion of tuberculin-specific Th1-responses induces immune restoration syndrome in tuberculosis and HIV co-infected patients. AIDS 2006;20(2):F1-7
99. Armstrong AW, Armstrong EJ, Fuller EN, et al. Smoking and pathogenesis of psoriasis: a review of oxidative, inflammatory and genetic mechanisms. Br J Dermatol 2011;165(6):1162-8
100. Williams JF. Cytochrome P450 isoforms. Regulation during infection, inflammation and by cytokines. J Fla Med Assoc 1991;78(8):517-19