T-cell reconstitution during murine acquired immunodeficiency syndrome (MAIDS) produces neuroinflammation and mortality in animals harboring opportunistic viral brain infection

Journal of Neuroinflammation

Volumn 10, Issue , 2013, Pages

  Mutnal, Manohar B ^a   Schachtele, Scott J ^a   Hu, Shuxian ^a   Lokensgard, James R ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROGRAMMED DEATH 1 RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM RELATED IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; FEMALE; FLOW CYTOMETRY; HERPES SIMPLEX ENCEPHALITIS; HERPES SIMPLEX VIRUS 1; IMMUNE DEFICIENCY; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; IMMUNOPATHOGENESIS; IMMUNOREGULATION; INFECTION RESISTANCE; INFECTION SENSITIVITY; LYMPHOCYTIC INFILTRATION; LYMPHOCYTOPENIA; MICROGLIA; MORTALITY; MOUSE; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OPPORTUNISTIC INFECTION; PROCEDURES CONCERNING CELLS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE STUDY; T CELL DEPLETION; T CELL RECONSTITUTION; TH1 CELL;

EID: 84880862179     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-10-98     Document Type: Article

References (40)

1. Palella FJ, Delaney KM, Moorman AC, Loveless MO, Fuhrer J, Satten GA, Aschman DJ, Holmberg SD. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl J Med 1998, 338:853-860. 10.1056/NEJM199803263381301, 9516219.
2. Barber DL, Andrade BB, Sereti I, Sher A. Immune reconstitution inflammatory syndrome: the trouble with immunity when you had none. Nat Rev Microbiol 2012, 10:150-156. 3507517, 22230950.
3. French MA, Lenzo N, John M, Mallal SA, McKinnon EJ, James IR, Price P, Flexman JP, Tay-Kearney ML. Immune restoration disease after the treatment of immunodeficient HIV-infected patients with highly active antiretroviral therapy. HIV Med 2000, 1:107-115. 10.1046/j.1468-1293.2000.00012.x, 11737333.
4. French MA, Mallal SA, Dawkins RL. Zidovudine-induced restoration of cell-mediated immunity to mycobacteria in immunodeficient HIV-infected patients. AIDS 1992, 6:1293-1297. 10.1097/00002030-199211000-00009, 1472334.
5. Shelburne SA, Hamill RJ, Rodriguez-Barradas MC, Greenberg SB, Atmar RL, Musher DW, Gathe JC, Visnegarwala F, Trautner BW. Immune reconstitution inflammatory syndrome: emergence of a unique syndrome during highly active antiretroviral therapy. Medicine (Baltimore) 2002, 81:213-227.
6. Shelburne SA, Darcourt J, White AC, Greenberg SB, Hamill RJ, Atmar RL, Visnegarwala F. The role of immune reconstitution inflammatory syndrome in AIDS-related Cryptococcus neoformans disease in the era of highly active antiretroviral therapy. Clin Infect Dis 2005, 40:1049-1052. 10.1086/428618, 15825000.
7. McCombe JA, Auer RN, Maingat FG, Houston S, Gill MJ, Power C. Neurologic immune reconstitution inflammatory syndrome in HIV/AIDS: outcome and epidemiology. Neurol 2009, 72:835-841.
8. Asselman V, Thienemann F, Pepper DJ, Boulle A, Wilkinson RJ, Meintjes G, Marais S. Central nervous system disorders after starting antiretroviral therapy in South Africa. AIDS 2010, 24:2871-2876. 10.1097/QAD.0b013e328340fe76, 3077551, 21045634.
9. Sharma SK, Soneja M. HIV & immune reconstitution inflammatory syndrome (IRIS). Indian J Med Res 2011, 134:866-877. 10.4103/0971-5916.92632, 3284095, 22310819.
10. Riedel DJ, Pardo CA, McArthur J, Nath A. Therapy insight: CNS manifestations of HIV-associated immune reconstitution inflammatory syndrome. Nat Clin Pract Neurol 2006, 2:557-565. 10.1038/ncpneuro0303, 16990829.
11. Mosier DE, Yetter RA, Morse HC. Retroviral induction of acute lymphoproliferative disease and profound immunosuppression in adult C57BL/6 mice. J Exp Med 1985, 161:766-784. 10.1084/jem.161.4.766, 2189053, 2984305.
12. Yetter RA, Buller RM, Lee JS, Elkins KL, Mosier DE, Fredrickson TN, Morse HC. CD4+ T cells are required for development of a murine retrovirus-induced immunodeficiency syndrome (MAIDS). J Exp Med 1988, 168:623-635. 10.1084/jem.168.2.623, 2189016, 2842430.
13. Sei Y, Basile AS. A murine model of retroviral encephalopathy. Curr Protoc Neurosci 2002, Chapter 9:Unit9 8.
14. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J Immunol 1995, 154:4309-4321.
15. Marten NW, Stohlman SA, Bergmann CC. Role of viral persistence in retaining CD8(+) T cells within the central nervous system. J Virol 2000, 74:7903-7910. 10.1128/JVI.74.17.7903-7910.2000, 112321, 10933698.
16. Sharpe AH, Wherry EJ, Ahmed R, Freeman GJ. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat Immunol 2007, 8:239-245. 10.1038/ni1443, 17304234.
17. Elrefaei M, Baker CA, Jones NG, Bangsberg DR, Cao H. Presence of suppressor HIV-specific CD8+ T cells is associated with increased PD-1 expression on effector CD8+ T cells. J Immunol 2008, 180:7757-7763. 3591725, 18490780.
18. Gazzinelli RT, Hartley JW, Fredrickson TN, Chattopadhyay SK, Sher A, Morse HC. Opportunistic infections and retrovirus-induced immunodeficiency: studies of acute and chronic infections with Toxoplasma gondii in mice infected with LP-BM5 murine leukemia viruses. Infect Immun 1992, 60:4394-4401. 257477, 1328058.
19. Barral-Netto M, da Silva JS, Barral A, Reed S. Up-regulation of T helper 2 and down-regulation of T helper 1 cytokines during murine retrovirus-induced immunodeficiency syndrome enhances susceptibility of a resistant mouse strain to Leishmania amazonensis. Am J Pathol 1995, 146:635-642. 1869162, 7887446.
20. Cole GT, Saha K, Seshan KR, Lynn KT, Franco M, Wong PK. Retrovirus-induced immunodeficiency in mice exacerbates gastrointestinal candidiasis. Infect Immun 1992, 60:4168-4178. 257449, 1398927.
21. Darban H, Enriquez J, Sterling CR, Lopez MC, Chen G, Abbaszadegan M, Watson RR. Cryptosporidiosis facilitated by murine retroviral infection with LP-BM5. J Infect Dis 1991, 164:741-745. 10.1093/infdis/164.4.741, 1654357.
22. Lundberg P, Welander P, Openshaw H, Nalbandian C, Edwards C, Moldawer L, Cantin E. A locus on mouse chromosome 6 that determines resistance to herpes simplex virus also influences reactivation, while an unlinked locus augments resistance of female mice. J Virol 2003, 77:11661-11673. 10.1128/JVI.77.21.11661-11673.2003, 229335, 14557652.
23. Zloza A, Schenkel JM, Tenorio AR, Martinson JA, Jeziorczak PM, Al-Harthi L. Potent HIV-specific responses are enriched in a unique subset of CD8+ T cells that coexpresses CD4 on its surface. Blood 2009, 114:3841-3853. 10.1182/blood-2009-02-202481, 19700667.
24. Marques CP, Cheeran MC, Palmquist JM, Hu S, Urban SL, Lokensgard JR. Prolonged microglial cell activation and lymphocyte infiltration following experimental herpes encephalitis. J Immunol 2008, 181:6417-6426. 2614272, 18941232.
25. Mutnal MB, Hu S, Little MR, Lokensgard JR. Memory T cells persisting in the brain following MCMV infection induce long-term microglial activation via interferon-gamma. J Neurovirol 2011, 17:424-437. 10.1007/s13365-011-0042-5, 3204167, 21800103.
26. Letendre SL, Zheng JC, Kaul M, Yiannoutsos CT, Ellis RJ, Taylor MJ, Marquie-Beck J, Navia B. Chemokines in cerebrospinal fluid correlate with cerebral metabolite patterns in HIV-infected individuals. J Neurovirol 2011, 17:63-69. 10.1007/s13365-010-0013-2, 3032187, 21246320.
27. Antonelli LR, Mahnke Y, Hodge JN, Porter BO, Barber DL, DerSimonian R, Greenwald JH, Roby G, Mican J, Sher A, Roederer M, Sereti I. Elevated frequencies of highly activated CD4+ T cells in HIV + patients developing immune reconstitution inflammatory syndrome. Blood 2010, 116:3818-3827. 10.1182/blood-2010-05-285080, 2981537, 20660788.
28. D'Souza M, Fontenot AP, Mack DG, Lozupone C, Dillon S, Meditz A, Wilson CC, Connick E, Palmer BE. Programmed death 1 expression on HIV-specific CD4+ T cells is driven by viral replication and associated with T cell dysfunction. J Immunol 2007, 179:1979-1987.
29. Dyavar Shetty R, Velu V, Titanji K, Bosinger SE, Freeman GJ, Silvestri G, Amara RR. PD-1 blockade during chronic SIV infection reduces hyperimmune activation and microbial translocation in rhesus macaques. J Clin Invest 2012, 122:1712-1716. 10.1172/JCI60612, 3336983, 22523065.
30. Palmer BE, Neff CP, Lecureux J, Ehler A, Dsouza M, Remling-Mulder L, Korman AJ, Fontenot AP, Akkina R. In vivo blockade of the PD-1 receptor suppresses HIV-1 viral loads and improves CD4+ T cell levels in humanized mice. J Immunol 2013, 190:211-219. 10.4049/jimmunol.1201108, 23209326.
31. Kastrukoff LF, Lau AS, Takei F, Smyth MJ, Jones CM, Clarke SR, Carbone FR. Redundancy in the immune system restricts the spread of HSV-1 in the central nervous system (CNS) of C57BL/6 mice. Virol 2010, 400:248-258.
32. Buller RM, Yetter RA, Fredrickson TN, Morse HC. Abrogation of resistance to severe mousepox in C57BL/6 mice infected with LP-BM5 murine leukemia viruses. J Virol 1987, 61:383-387. 253960, 3027368.
33. Chau F, Levacher-Clergeot M, Desforges B, Ricatte L, Sinet M. Prognostic value of phenotypic alterations in blood lymphocyte subsets in a murine retrovirus-induced immunodeficiency syndrome (MAIDS). Clin Exp Immunol 1993, 91:467-472. 1554708, 8095194.
34. Day CL, Kaufmann DE, Kiepiela P, Brown JA, Moodley ES, Reddy S, Mackey EW, Miller JD, Leslie AJ, DePierres C, Mncube Z, Duraiswamy J, Zhu B, Eichbaum Q, Altfeld M, Wherry EJ, Coovadia HM, Goulder PJ, Klenerman P, Ahmed R, Freeman GJ, Walker BD. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nat 2006, 443:350-354.
35. Trautmann L, Janbazian L, Chomont N, Said EA, Gimmig S, Bessette B, Boulassel MR, Delwart E, Sepulveda H, Balderas RS, Routy JP, Haddad EK, Sekaly RP. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat Med 2006, 12:1198-1202. 10.1038/nm1482, 16917489.
36. Velu V, Titanji K, Zhu B, Husain S, Pladevega A, Lai L, Vanderford TH, Chennareddi L, Silvestri G, Freeman GJ, Ahmed R, Amara RR. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nat 2009, 458:206-210.
37. Li W, Green WR. Immunotherapy of murine retrovirus-induced acquired immunodeficiency by CD4 T regulatory cell depletion and PD-1 blockade. J Virol 2011, 85:13342-13353. 10.1128/JVI.00120-11, 3233148, 21917983.
38. Roths JB, Sidman CL. Both immunity and hyperresponsiveness to Pneumocystis carinii result from transfer of CD4+ but not CD8+ T cells into severe combined immunodeficiency mice. J Clin Invest 1992, 90:673-678. 10.1172/JCI115910, 443150, 1353767.
39. Barber DL, Mayer-Barber KD, Antonelli LR, Wilson MS, White S, Caspar P, Hieny S, Sereti I, Sher A. Th1-driven immune reconstitution disease in Mycobacterium avium-infected mice. Blood 2010, 116:3485-3493. 10.1182/blood-2010-05-286336, 2981475, 20656932.
40. Wiesner DL, Boulware DR. Cryptococcus-related immune reconstitution inflammatory syndrome (IRIS): pathogenesis and its clinical implications. Curr Fungal Infect Rep 2011, 5:252-261. 10.1007/s12281-011-0064-8, 3289516, 22389746.