An Infectious Murine Model for Studying the Systemic Effects of Opioids on Early HIV Pathogenesis in the Gut

Journal of Neuroimmune Pharmacology

Volumn 10, Issue 1, 2015, Pages 74-87

  Sindberg, Gregory M ^a   Sharma, Umakant ^b   Banerjee, Santanu ^b   Anand, Vidhu ^b   Dutta, Raini ^b   Gu, Chao Jiang ^c   Volsky, David J ^c   Roy, Sabita ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Early HIV pathogenesis; EcoHIV; Gastrointestinal (GI); HIV model; Microbial translocation; Morphine; Opioids

Indexed keywords

CYTOKINE; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MORPHINE; OCCLUDIN; PLACEBO; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR ALPHA; NARCOTIC ANALGESIC AGENT; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; CONTROLLED STUDY; DISORIENTATION; DRUG EFFECT; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INTESTINE; INTESTINE FLORA; LIVER; MALE; MOUSE; MURINE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS PATHOGENESIS; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; COMPLICATION; DRUG EFFECTS; GASTROINTESTINAL DISEASES; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHAGOCYTOSIS;

ANALGESICS, OPIOID; ANIMALS; BACTERIAL TRANSLOCATION; FEMALE; GASTROINTESTINAL DISEASES; HIV INFECTIONS; HIV-1; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; LIVER; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OCCLUDIN; PHAGOCYTOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84925460927     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-014-9574-9     Document Type: Article

References (44)

1. Ancuta P, Kamat A, Kunstman KJ et al (2008) Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS ONE 3:e2516. doi:10.1371/journal.pone.0002516
2. Banerjee S, Meng J, Das S et al (2013) Morphine induced exacerbation of sepsis is mediated by tempering endotoxin tolerance through modulation of miR-146a. Sci Rep 3:1977. doi:10.1038/srep01977
3. Beyrer C, Malinowska-Sempruch K, Kamarulzaman A et al (2010) Time to act: a call for comprehensive responses to HIV in people who use drugs. Lancet 376:551–563. doi:10.1016/S0140-6736(10)60928-2
4. Bokhari SM, Hegde R, Callen S et al (2011) Morphine potentiates neuropathogenesis of SIV infection in rhesus macaques. J Neuroimmune Pharmacol 1–14
5. Brenchley JM, Schacker TW, Ruff LE et al (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200:749–759. doi:10.1084/jem.20040874
6. Brenchley JM, Price DA, Schacker TW et al (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12:1365–1371. doi:10.1038/nm1511
7. Brenchley JM, Paiardini M, Knox KS et al (2008) Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112:2826–2835. doi:10.1182/blood-2008-05-159301
8. Casellas AM, Guardiola H, Renaud FL (1991) Inhibition by opioids of phagocytosis in peritoneal macrophages. Neuropeptides 18:35–40. doi:10.1016/0143-4179(91)90161-B
9. Clark JA, Coopersmith CM (2007) Intestinal crosstalk: a new paradigm for understanding the gut as the “motor” of critical illness. Shock 28:384–393. doi:10.1097/shk.0b013e31805569df
10. Denning TL, Wang Y, Patel SR et al (2007) Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 8:1086–1094. doi:10.1038/ni1511
11. Denton PW, Garcia JV (2009) Novel humanized murine models for HIV research. Curr HIV/AIDS Rep 6:13–19
12. Dighe SV, Madia PA, Sirohi S, Yoburn BC (2009) Continuous morphine produces more tolerance than intermittent or acute treatment. Pharmacol Biochem Behav 92:537–542. doi:10.1016/j.pbb.2009.02.004
13. Donahoe RM, Vlahov D (1998) Opiates as potential cofactors in progression of HIV-1 infections to AIDS. J Neuroimmunol 83:77–87
14. Edgett W (2004) Alcian Blue - H&E - Metanil Yellow Stain for diagnosing Barrett’s esophagus. HistoLogic 37
15. El-Hage N, Podhaizer EM, Sturgill J, Hauser KF (2011) Toll-like receptor expression and activation in astroglia: differential regulation by HIV-1 Tat, gp120, and morphine. Immunol Investig 40:498–522. doi:10.3109/08820139.2011.561904
16. Estes JD, Harris LD, Klatt NR et al (2010) Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog. doi:10.1371/journal.ppat.1001052
17. Gordon S, Klatt N, Bosinger S et al (2007) Severe depletion of mucosal CD4+ T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J Immunol
18. Gordon SN, Cervasi B, Odorizzi P et al (2010) Disruption of intestinal CD4+ T cell homeostasis is a key marker of systemic CD4+ T cell activation in HIV-infected individuals. J Immunol 185:5169–5179. doi:10.4049/jimmunol.1001801
19. Hauser KF, El-Hage N, Stiene-Martin A et al (2007) HIV-1 neuropathogenesis: glial mechanisms revealed through substance abuse. J Neurochem 100:567–586. doi:10.1111/j.1471-4159.2006.04227.x
20. He H, Sharer LR, Chao W et al (2014) Enhanced human immunodeficiency virus Type 1 expression and neuropathogenesis in knockout mice lacking type I interferon responses. J Neuropathol Exp Neurol 73:59–71. doi:10.1097/NEN.0000000000000026
21. Hilburger ME, Adler MW, Truant AL et al (1997) Morphine induces sepsis in mice. J Infect Dis 176:183–188
22. Hinkin CH, Hardy DJ, Mason KI et al (2004) Medication adherence in HIV-infected adults: effect of patient age, cognitive status, and substance abuse. AIDS 18(Suppl 1):S19–S25
23. Hollenbach R, Sagar D, Khan ZK et al (2014) Effect of morphine and SIV on dendritic cell trafficking into the central nervous system of rhesus macaques. J Neurovirol 20:175–183. doi:10.1007/s13365-013-0182-x
24. Kapadia F, Vlahov D, Donahoe RM, Friedland G (2005) The role of substance abuse in HIV disease progression: reconciling differences from laboratory and epidemiologic investigations. Clin Infect Dis 41:1027
25. Kedia S, Sell M, Relyea G (2007) Mono-versus polydrug abuse patterns among publicly funded clients. Subst Abuse Treat Prev Policy 9:1–9. doi:10.1186/1747-597X-2-Received
26. Kelschenbach JL, Saini M, Hadas E et al (2011) Mice chronically infected with chimeric HIV resist peripheral and brain superinfection: a model of protective immunity to HIV. J Neuroimmune Pharmacol. doi:10.1007/s11481-011-9316-1
27. Kwok YH, Hutchinson MR, Gentgall MG, Rolan PE (2012) Increased responsiveness of peripheral blood mononuclear cells to in vitro TLR 2, 4 and 7 ligand stimulation in chronic pain patients. PLoS ONE 7:e44232. doi:10.1371/journal.pone.0044232
28. Meng J, Yu H, Ma J et al (2013) Morphine induces bacterial translocation in mice by compromising intestinal barrier function in a TLR-dependent manner. PLoS ONE 8:e54040. doi:10.1371/journal.pone.0054040
29. Nazli A, Chan O, Dobson-Belaire WN et al (2010) Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 6:e1000852. doi:10.1371/journal.ppat.1000852
30. Ninković J, Roy S (2012) Morphine decreases bacterial phagocytosis by inhibiting actin polymerization through cAMP-, Rac-1-, and p38 MAPK-dependent mechanisms. Am J Pathol 180:1068–1079. doi:10.1016/j.ajpath.2011.11.034
31. Nowroozalizadeh S, Månsson F, da Silva Z et al (2010) Microbial translocation correlates with the severity of both HIV-1 and HIV-2 infections. J Infect Dis 201:1150–1154. doi:10.1086/651430
32. Pahar B, Lackner AA, Veazey RS (2006) Intestinal double-positive CD4+CD8+ T cells are highly activated memory cells with an increased capacity to produce cytokines. Eur J Immunol 36:583–592. doi:10.1002/eji.200535520
33. Pandrea IV, Gautam R, Ribeiro RM et al (2007) Acute loss of intestinal CD4+ T cells is not predictive of simian immunodeficiency virus virulence. J Immunol 179:3035–3046
34. Pandrea I, Sodora DL, Silvestri G, Apetrei C (2008) Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends Immunol 29:419–428. doi:10.1016/j.it.2008.05.004
35. Potash MJ, Chao W, Bentsman G et al (2005) A mouse model for study of systemic HIV-1 infection, antiviral immune responses, and neuroinvasiveness. Proc Natl Acad Sci U S A 102:3760–3765. doi:10.1073/pnas.0500649102
36. Rivera I, García Y, Gangwani MR et al (2013) Identification and molecular characterization of SIV Vpr R50G mutation associated with long term survival in SIV-infected morphine dependent and control macaques. Virology 446:144–151. doi:10.1016/j.virol.2013.07.027
37. Rivera-Amill V, Silverstein PS, Noel RJ et al (2010) Morphine and rapid disease progression in nonhuman primate model of AIDS: inverse correlation between disease progression and virus evolution. J Neuroimmune Pharmacol 5:122–132. doi:10.1007/s11481-009-9184-0
38. Rojavin M, Szabo I, Bussiere J, Rogers T (1993) Morphine treatment in vitro or in vivo decreases phagocytic functions of murine macrophages. Life Sci 53:997
39. Roy S, Ninkovic J, Banerjee S et al (2011) Opioid drug abuse and modulation of immune function: consequences in the susceptibility to opportunistic infections. J Neuroimmune Pharmacol. doi:10.1007/s11481-011-9292-5
40. Shultz LD, Brehm MA, Garcia-Martinez JV, Greiner DL (2012) Humanized mice for immune system investigation: progress, promise and challenges. Nat Rev Immunol 12:786–798. doi:10.1038/nri3311
41. Spikes L, Dalvi P, Tawfik O et al (2012) Enhanced pulmonary arteriopathy in simian immunodeficiency virus-infected macaques exposed to morphine. Am J Respir Crit Care Med 185:1235–1243. doi:10.1164/rccm.201110-1909OC
42. Tubaro E, Avico U, Santiangeli C (1985) Morphine and methadone impact on human phagocytic physiology. Int J Immunopharmacol 7:865–874
43. Wolfe D, Carrieri MP, Shepard D (2010) Treatment and care for injecting drug users with HIV infection: a review of barriers and ways forward. Lancet 376:355–366. doi:10.1016/S0140-6736(10)60832-X
44. Zhang L, Su L (2012) HIV-1 immunopathogenesis in humanized mouse models. Cell Mol Immunol 9:237–244. doi:10.1038/cmi.2012.7