Effect of morphine on the neuropathogenesis of SIVmac infection in Indian rhesus macaques

Journal of NeuroImmune Pharmacology

Volumn 3, Issue 1, 2008, Pages 12-25

  Marcario, Joanne K ^a   Riazi, Mariam ^a   Adany, Istvan ^a   Kenjale, Himanshu ^a   Fleming, Kandace ^c   Marquis, Janet ^c   Nemon, Olga ^b   Mayo, Matthew S ^b   Yankee, Thomas ^a   Narayan, Opendra ^a   Cheney, Paul D ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^c Schiefelbusch Institute for Life Span Studies   (United States)

Author keywords

AIDS; Cell mediated immune responses (CMI); Morphine; RT PCR; SIV; Viral titers

Indexed keywords

MESSENGER RNA; MORPHINE; NARCOTIC AGENT; VIRUS RNA;

ANIMAL; ARTICLE; BRAIN; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COUNT; CELLULAR IMMUNITY; DRUG EFFECT; FLOW CYTOMETRY; IMMUNOLOGY; MACACA; MALE; MONKEY DISEASE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIMIAN IMMUNODEFICIENCY VIRUS; VIREMIA; VIROLOGY; VIRUS LOAD;

ANIMALS; BRAIN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL COUNT; FLOW CYTOMETRY; IMMUNITY, CELLULAR; MACACA MULATTA; MALE; MORPHINE; NARCOTICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, VIRAL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD; VIREMIA;

EID: 38949092489     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-007-9085-z     Document Type: Article

References (53)

1. Alcabes P, Friedland G (1995) Injection drug use and human immunodeficiency virus infection. Clin Infect Dis 20:1467-1479
2. Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE, Murphy PM, Berger EA (1996) CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272:1955-1958
3. Allen TM, Mothe BR, Sidney J, Jing P, Dzuris JL, Liebl ME, Vogel TU, O'Connor DH, Wang X, Wussow MC, Thomson JA, Altman JD, Watkins DI, Sette A (2001) CD8(+) lymphocytes from simian immunodeficiency virus-infected Rhesus Macaques recognize 14 different epitopes bound by the major histocompatibility complex class I molecule mamu-A*01: implications for vaccine design and testing. J Virol 75:738-749
4. Ancuta P, Kunstman KJ, Autissier P, Zaman T, Stone D, Wolinsky SM, Gabuzda D (2006) CD16+ monocytes exposed to HIV promote highly efficient viral replication upon differentiation into macrophages and interaction with T cells. Virology 344:267-276
5. Berman NE, Raymond LA, Warren KA, Raghavan R, Joag SV, Narayan O, Cheney PD (1998) Fractionator analysis shows loss of neurons in the lateral geniculate nucleus of macaques infected with neurovirulent simian immunodeficiency virus. Neuropathol Appl Neurobiol 24:44-52
6. Berman NE, Marcario JK, Yong C, Raghavan R, Raymond LA, Joag SV, Narayan O, Cheney PD (1999) Microglial activation and neurological symptoms in the SIV model of NeuroAIDS: association of MHC-II and MMP-9 expression with behavioral deficits and evoked potential changes. Neurobiol Dis 6:486-498
7. Bissel SJ, Wang G, Trichel AM, Murphey-Corb M, Wiley CA (2006) Longitudinal analysis of monocyte/macrophage infection in simian immunodeficiency virus-infected, CD8+ T-cell-depleted macaques that develop lentiviral encephalitis. Am J Pathol 168:1553-1569
8. Budka H (1986) Multinucleated giant cells in brain: a hallmark of the acquired immune deficiency syndrome (AIDS). Acta Neuropathol (Berl) 69:253-258
9. Budka H (1991) Neuropathology of human immunodeficiency virus infection. Brain Pathol 1:163-175
10. Carruth LM, Zink MC, Tarwater PM, Miller MD, Li M, Queen LA, Mankowski JL, Shen A, Siliciano RF, Clements JE (2005) SIV-specific T lymphocyte responses in PBMC and lymphoid tissues of SIV-infected pigtailed macaques during suppressive combination antiretroviral therapy. J Med Primatol 34:109-121
11. CDC (2002) Estimated numbers of diagnoses of HIV/AIDS, by year of diagnosis and selected characteristics of persons, 1999-2002. HIV/AIDS Surveill Rep 10
12. Chen Z, Zhou P, Ho DD, Landau NR, Marx PA (1997) Genetically divergent strains of simian immunodeficiency virus use CCR5 as a coreceptor for entry. J Virol 71:2705-2714
13. Chuang LF, Killam KF Jr, Chuang RY (1993) Opioid dependency and T-helper cell functions in Rhesus monkey. In Vivo 7:159-166
14. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, Di Marzio P, Marmon S, Sutton RE, Hill CM, Davis CB, Peiper SC, Schall TJ, Littman DR, Landau NR (1996) Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661-666
15. Dickson DW, Lee SC, Mattiace LA, Yen SH, Brosnan C (1993) Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia 7:75-83
16. Dickson DW, Lee SC, Hatch W, Mattiace LA, Brosnan CF, Lyman WD (1994) Macrophages and microglia in HIV-related CNS neuropathology. Res Publ Assoc Res Nerv Ment Dis 72:99-118
17. Donahoe RM (2004) Multiple ways that drug abuse might influence AIDS progression: clues from a monkey model. J Neuroimmunol 147:28-32
18. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, Cayanan C, Maddon PJ, Koup RA, Moore JP, Paxton WA (1996) HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667-673
19. Guo CJ, Li Y, Tian S, Wang X, Douglas SD, Ho WZ (2002) Morphine enhances HIV infection of human blood mononuclear phagocytes through modulation of beta-chemokines and CCR5 receptor. J Investig Med 50:435-442
20. Hatsukari I, Hitosugi N, Dinda A, Singhal PC (2006) Morphine modulates monocyte-macrophage conversion phase. Cell Immunol 239:41-48
21. Hofmann-Lehmann R, Swenerton RK, Liska V, Leutenegger CM, Lutz H, McClure HM, Ruprecht RM (2000) Sensitive and robust one-tube real-time reverse transcriptase-polymerase chain reaction to quantify SIV RNA load: comparison of one- versus two-enzyme systems. AIDS Res Hum Retrovir 16:1247-1257
22. Joag SV, Adany I, Li Z, Foresman L, Pinson DM, Wang C, Stephens EB, Raghavan R, Narayan O (1997) Animal model of mucosally transmitted human immunodeficiency virus type 1 disease: intravaginal and oral deposition of simian/human immunodeficiency virus in macaques results in systemic infection, elimination of CD4+ T cells, and AIDS. J Virol 71:4016-4023
23. Johnson JK, Warren KA, Berman NE, Narayan O, Stephens EB, Joag SV, Raghavan R, Marcario JK, Cheney PD (2004) Manifestations of SIV-induced ocular pathology in macaque monkeys. J NeuroAIDS 2:1-13
24. Kalams SA, Walker BD (1994) The cytotoxic T-lymphocyte response in HIV-1 infection. Clin Lab Med 14:271-299
25. Kirchhoff F, Pohlmann S, Hamacher M, Means RE, Kraus T, Uberla K, Di Marzio P (1997) Simian immunodeficiency virus variants with differential T-cell and macrophage tropism use CCR5 and an unidentified cofactor expressed in CEMx174 cells for efficient entry. J Virol 71:6509-6516
26. Koenig S, Gendelman HE, Orenstein JM, Dal Canto MC, Pezeshkpour GH, Yungbluth M, Janotta F, Aksamit A, Martin MA, Fauci AS (1986) Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233:1089-1093
27. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, Borkowsky W, Farthing C, Ho DD (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 68:4650-4655
28. Kumar R, Orsoni S, Norman L, Verma AS, Tirado G, Giavedoni LD, Staprans S, Miller GM, Buch SJ, Kumar A (2006) Chronic morphine exposure causes pronounced virus replication in cerebral compartment and accelerated onset of AIDS in SIV/SHIV-infected Indian Rhesus Macaques. Virology 354:192-206
29. Lane JH, Sasseville VG, Smith MO, Vogel P, Pauley DR, Heyes MP, Lackner AA (1996) Neuroinvasion by simian immunodeficiency virus coincides with increased numbers of perivascular macrophages/microglia and intrathecal immune activation. J Neurovirol 2:423-432
30. Loffredo JT, Sidney J, Wojewoda C, Dodds E, Reynolds MR, Napoe G, Mothe BR, O'Connor DH, Wilson NA, Watkins DI, Sette A (2004) Identification of seventeen new simian immunodeficiency virus-derived CD8+ T cell epitopes restricted by the high frequency molecule, Mamu-A02, and potential escape from CTL recognition. J Immunol 173:5064-5076
31. Mackay GA, Liu Z, Singh DK, Smith MS, Mukherjee S, Sheffer D, Jia F, Adany I, Sun KH, Dhillon S, Zhuge W, Narayan O (2004) Protection against late-onset AIDS in macaques prophylactically immunized with a live simian HIV vaccine was dependent on persistence of the vaccine virus. J Immunol 173:4100-4107
32. Mankowski JL, Clements JE, Zink MC (2002) Searching for clues: tracking the pathogenesis of human immunodeficiency virus central nervous system disease by use of an accelerated, consistent simian immunodeficiency virus macaque model. J Infect Dis 186(Suppl 2):S199-S208
33. Marcario JK, Raymond LA, McKiernan BJ, Foresman LL, Joag SV, Raghavan R, Narayan O, Cheney PD (1999a) Motor skill impairment in SIV-infected Rhesus Macaques with rapidly and slowly progressing disease. J Med Primatol 28:105-117
34. Marcario JK, Raymond LA, McKiernan BJ, Foresman LL, Joag SV, Raghavan R, Narayan O, Hershberger S, Cheney PD (1999b) Simple and choice reaction time performance in SIV-infected Rhesus Macaques. AIDS Res Hum Retrovir 15:571-583
35. Marcario JK, Manaye KF, SantaCruz KS, Mouton PR, Berman NE, Cheney PD (2004) Severe subcortical degeneration in macaques infected with neurovirulent simian immunodeficiency virus. J Neurovirol 10:387-399
36. Marx PA, Chen Z (1998) The function of simian chemokine receptors in the replication of SIV. Semin Immunol 10:215-223
37. Navia BA, Cho ES, Petito CK, Price RW (1986) The AIDS dementia complex: II. Neuropathology. Ann Neurol 19:525-535
38. Petito CK, Cho ES, Lemann W, Navia BA, Price RW (1986) Neuropathology of acquired immunodeficiency syndrome (AIDS): an autopsy review. J Neuropathol Exp Neurol 45:635-646
39. Raghavan R, Cheney PD, Raymond LA, Joag SV, Stephens EB, Adany I, Pinson DM, Li Z, Marcario JK, Jia F, Wang C, Foresman L, Berman NE, Narayan O (1999) Morphological correlates of neurological dysfunction in macaques infected with neurovirulent simian immunodeficiency virus. Neuropathol Appl Neurobiol 25:285-294
40. Raymond LA, Wallace D, Berman NE, Marcario J, Foresman L, Joag SV, Raghavan R, Narayan O, Cheney PD (1998) Auditory brainstem responses in a Rhesus Macaque model of neuro-AIDS. J Neurovirol 4:512-520
41. Raymond LA, Wallace D, Marcario JK, Raghavan R, Narayan O, Foresman LL, Berman NE, Cheney PD (1999) Motor evoked potentials in a Rhesus Macaque model of neuro-AIDS. J Neurovirol 5:217-231
42. Raymond LA, Wallace D, Raghavan R, Marcario JK, Johnson JK, Foresman LL, Joag SV, Narayan O, Berman NE, Cheney PD (2000) Sensory evoked potentials in SIV-infected monkeys with rapidly and slowly progressing disease. AIDS Res Hum Retrovir 16:1163-1173
43. Riviere Y (1994) Virus-specific cytotoxic T lymphocyte responses in patients infected with the human immunodeficiency virus, HIV-1. Cell Mol Biol (Noisy-le-grand) 40(Suppl 1):45-48
44. Roy S, Wang J, Charboneau R, Loh HH, Barke RA (2005) Morphine induces CD4+ T cell IL-4 expression through an adenylyl cyclase mechanism independent of the protein kinase A pathway. J Immunol 175:6361-6367
45. Selwyn PA, Alcabes P, Hartel D, Buono D, Schoenbaum EE, Klein RS, Davenny K, Friedland GH (1992) Clinical manifestations and predictors of disease progression in drug users with human immunodeficiency virus infection. N Engl J Med 327:1697-1703
46. Suzuki S, Carlos MP, Chuang LF, Torres JV, Doi RH, Chuang RY (2002) Methadone induces CCR5 and promotes AIDS virus infection. FEBS Lett 519:173-177
47. Thorpe LE, Frederick M, Pitt J, Cheng I, Watts DH, Buschur S, Green K, Zorrilla C, Landesman SH, Hershow RC (2004) Effect of hard-drug use on CD4 cell percentage, HIV RNA level, and progression to AIDS-defining class C events among HIV-infected women. J Acquir Immune Defic Syndr 37:1423-1430
48. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, Knight HL, Rosenzweig M, Johnson RP, Desrosiers RC, Lackner AA (1998) Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280:427-431
49. Veazey RS, Mansfield KG, Tham IC, Carville AC, Shvetz DE, Forand AE, Lackner AA (2000a) Dynamics of CCR5 expression by CD4(+) T cells in lymphoid tissues during simian immunodeficiency virus infection. J Virol 74:11001-11007
50. Veazey RS, Tham IC, Mansfield KG, DeMaria M, Forand AE, Shvetz DE, Chalifoux LV, Sehgal PK, Lackner AA (2000b) Identifying the target cell in primary simian immunodeficiency virus (SIV) infection: highly activated memory CD4(+) T cells are rapidly eliminated in early SIV infection in vivo. J Virol 74:57-64
51. Walker CM (1993) Non-cytolytic control of HIV replication by CD8+ T cells. Semin Immunol 5:195-201
52. Wang J, Barke RA, Charboneau R, Loh HH, Roy S (2003) Morphine negatively regulates interferon-gamma promoter activity in activated murine T cells through two distinct cyclic AMP-dependent pathways. J Biol Chem 278:37622-37631
53. Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, deBakker C, Alvarez X, Lackner AA (2001) Perivascular macrophages are the primary cell type productively infected by simian immunodeficiency virus in the brains of macaques: implications for the neuropathogenesis of AIDS. J Exp Med 193:905-915