Central nervous system inflammation and infection during early, nonaccelerated simian-human immunodeficiency virus infection in rhesus macaques

Journal of Virology

Volumn 92, Issue 11, 2018, Pages

  Hsu, Denise C ^a,b   Sunyakumthorn, Piyanate ^a   Wegner, Matthew ^a   Schuetz, Alexandra ^a,b   Silsorn, Decha ^a   Estes, Jacob D ^c,k,l   Deleage, Claire ^c   Tomusange, Khamis ^d   Lakhashe, Samir K ^d   Ruprecht, Ruth M ^d,e   Lombardini, Eric ^a   Im Erbsin, Rawiwan ^a   Kuncharin, Yanin ^a   Phuang Ngern, Yuwadee ^a   Inthawong, Dutsadee ^a   Chuenarom, Weerawan ^a   Burke, Robin ^a,m   Robb, Merlin L ^b,f   Ndhlovu, Lishomwa C ^g   Ananworanich, Jintanat ^b,f,h   Valcour, Victor ⁱ   O'Connell, Robert J ^a   Spudich, Serena ^j   Michael, Nelson L ^f   Vasan, Sandhya ^a,b   more..

^a ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

^b HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^d SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^e SOUTHWEST NATIONAL PRIMATE RESEARCH CENTER   (United States)

^f WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^g UNIVERSITY OF HAWAII   (United States)

^h UNIVERSITY OF AMSTERDAM   (Netherlands)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j YALE UNIVERSITY   (United States)

^k OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^l DEFENSE THREAT REDUCTION AGENCY   (United States)

^m Virginia Office of the Surgeon General   (United States)

more..

Author keywords

Early infection; HIV; Neuropathology; SHIV

Indexed keywords

CD163 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD68 ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MONOCYTE CHEMOTACTIC PROTEIN 1; VIRUS RNA; CD68 ANTIGEN, HUMAN; CELL SURFACE RECEPTOR; DIFFERENTIATION ANTIGEN; LEUKOCYTE ANTIGEN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM INFECTION; CENTRAL NERVOUS SYSTEM INFLAMMATION; CONTROLLED STUDY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MACROPHAGE; MALE; MENINX; MICROGLIA; MONOCYTE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PARENCHYMA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN CEREBROSPINAL FLUID LEVEL; RHESUS MONKEY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIRUS ENVELOPE; ANIMAL; BLOOD; BRAIN; CD4 LYMPHOCYTE COUNT; CELL CULTURE; CEREBROSPINAL FLUID; DISEASE MODEL; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; PATHOGENICITY; PATHOLOGY; SIMIAN IMMUNODEFICIENCY VIRUS; VIROLOGY; VIRUS LOAD;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BRAIN; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HIV-1; HUMANS; MACACA MULATTA; MACROPHAGES; MENINGES; MICROGLIA; MONOCYTES; PARENCHYMAL TISSUE; RECEPTORS, CELL SURFACE; RNA, VIRAL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD;

EID: 85046890057     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00222-18     Document Type: Article

References (44)

1. Price RW, Brew B, Sidtis J, Rosenblum M, Scheck AC, Cleary P. 1988. The brain in AIDS: central nervous system HIV-1 infection and AIDS dementia complex. Science 239:586-592. https://doi.org/10.1126/science.3277272
2. 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. https://doi.org/10.1126/science.3016903
3. Murray EA, Rausch DM, Lendvay J, Sharer LR, Eiden LE. 1992. Cognitive and motor impairments associated with SIV infection in rhesus monkeys. Science 255:1246-1249. https://doi.org/10.1126/science.1546323
4. Lackner AA, Smith MO, Munn RJ, Martfeld DJ, Gardner MB, Marx PA, Dandekar S. 1991. Localization of simian immunodeficiency virus in the central nervous system of rhesus monkeys. Am J Pathol 139:609-621
5. Chakrabarti L, Hurtrel M, Maire MA, Vazeux R, Dormont D, Montagnier L, Hurtrel B. 1991. Early viral replication in the brain of SIV-infected rhesus monkeys. Am J Pathol 139:1273-1280
6. 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. https://doi.org/10.3109/13550289609146909
7. Nowlin BT, Burdo TH, Midkiff CC, Salemi M, Alvarez X, Williams KC. 2015. SIV encephalitis lesions are composed of CD163(+) macrophages present in the central nervous system during early SIV infection and SIVpositive macrophages recruited terminally with AIDS. Am J Pathol 185: 1649-1665. https://doi.org/10.1016/j.ajpath.2015.01.033
8. Soulas C, Conerly C, Kim WK, Burdo TH, Alvarez X, Lackner AA, Williams KC. 2011. Recently infiltrating MAC387(+) monocytes/macrophages a third macrophage population involved in SIV and HIV encephalitic lesion formation. Am J Pathol 178:2121-2135. https://doi.org/10.1016/j.ajpath.2011.01.023
9. Clements JE, Babas T, Mankowski JL, Suryanarayana K, Piatak M, Jr, Tarwater PM, Lifson JD, Zink MC. 2002. The central nervous system as a reservoir for simian immunodeficiency virus (SIV): steady-state levels of SIV DNA in brain from acute through asymptomatic infection. J Infect Dis 186:905-913. https://doi.org/10.1086/343768
10. Zink MC, Brice AK, Kelly KM, Queen SE, Gama L, Li M, Adams RJ, Bartizal C, Varrone J, Rabi SA, Graham DR, Tarwater PM, Mankowski JL, Clements JE. 2010. Simian immunodeficiency virus-infected macaques treated with highly active antiretroviral therapy have reduced central nervous system viral replication and inflammation but persistence of viral DNA. J Infect Dis 202:161-170. https://doi.org/10.1086/653213
11. Graham DR, Gama L, Queen SE, Li M, Brice AK, Kelly KM, Mankowski JL, Clements JE, Zink MC. 2011. Initiation of HAART during acute simian immunodeficiency virus infection rapidly controls virus replication in the CNS by enhancing immune activity and preserving protective immune responses. J Neurovirol 17:120-130. https://doi.org/10.1007/s13365-010-0005-2
12. Witwer KW, Gama L, Li M, Bartizal CM, Queen SE, Varrone JJ, Brice AK, Graham DR, Tarwater PM, Mankowski JL, Zink MC, Clements JE. 2009. Coordinated regulation of SIV replication and immune responses in the CNS. PLoS One 4:e8129. https://doi.org/10.1371/journal.pone.0008129
13. Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL, Leblanc S, Corkran SH, Duarte NA, Clifford DB, Woods SP, Collier AC, Marra CM, Morgello S, Mindt MR, Taylor MJ, Marcotte TD, Atkinson JH, Wolfson T, Gelman BB, McArthur JC, Simpson DM, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I, Charter Group, HNRC Group. 2011. HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol 17:3-16. https://doi.org/10.1007/s13365-010-0006-1
14. Evering TH, Applebaum A, La Mar M, Garmon D, Dorfman D, Markowitz M. 2016. Rates of non-confounded HIV-associated neurocognitive disorders in men initiating combination antiretroviral therapy during primary infection. AIDS 30:203-210. https://doi.org/10.1097/QAD.0000000000000892
15. Ghate M, Mehendale S, Meyer R, Umlauf A, Deutsch R, Kamat R, Thakar M, Risbud A, Kulkarni S, Sakamoto M, Alexander T, Franklin D, Letendre S, Heaton RK, Grant I, Marcotte TD. 2015. The effects of antiretroviral treatment initiation on cognition in HIV-infected individuals with advanced disease in Pune, India. J Neurovirol 21:391-398. https://doi.org/10.1007/s13365-015-0329-z
16. Hellmuth J, Fletcher JL, Valcour V, Kroon E, Ananworanich J, Intasan J, Lerdlum S, Narvid J, Pothisri M, Allen I, Krebs SJ, Slike B, Prueksakaew P, Jagodzinski LL, Puttamaswin S, Phanuphak N, Spudich S, SEARCH 010/RV254 Study Group. 2016. Neurologic signs and symptoms frequently manifest in acute HIV infection. Neurology 87:148-154. https://doi.org/10.1212/WNL.0000000000002837
17. Schnell G, Price RW, Swanstrom R, Spudich S. 2010. Compartmentalization and clonal amplification of HIV-1 variants in the cerebrospinal fluid during primary infection. J Virol 84:2395-2407. https://doi.org/10.1128/JVI.01863-09
18. Sturdevant CB, Joseph SB, Schnell G, Price RW, Swanstrom R, Spudich S. 2015. Compartmentalized replication of R5 T cell-tropic HIV-1 in the central nervous system early in the course of infection. PLoS Pathog 11:e1004720. https://doi.org/10.1371/journal.ppat.1004720
19. Valcour V, Chalermchai T, Sailasuta N, Marovich M, Lerdlum S, Suttichom D, Suwanwela NC, Jagodzinski L, Michael N, Spudich S, van Griensven F, de Souza M, Kim J, Ananworanich J, RV254/Search 010 Study Group. 2012. Central nervous system viral invasion and inflammation during acute HIV infection. J Infect Dis 206:275-282. https://doi.org/10.1093/infdis/jis326
20. Lentz MR, Kim WK, Lee V, Bazner S, Halpern EF, Venna N, Williams K, Rosenberg ES, Gonzalez RG. 2009. Changes in MRS neuronal markers and T cell phenotypes observed during early HIV infection. Neurology 72:1465-1472. https://doi.org/10.1212/WNL.0b013e3181a2e90a
21. Harbison C, Zhuang K, Gettie A, Blanchard J, Knight H, Didier P, Cheng-Mayer C, Westmoreland S. 2014. Giant cell encephalitis and microglial infection with mucosally transmitted simian-human immunodeficiency virus SHIVSF162P3N in rhesus macaques. J Neurovirol 20:62-72. https://doi.org/10.1007/s13365-013-0229-z
22. Song RJ, Chenine AL, Rasmussen RA, Ruprecht CR, Mirshahidi S, Grisson RD, Xu W, Whitney JB, Goins LM, Ong H, Li PL, Shai-Kobiler E, Wang T, McCann CM, Zhang H, Wood C, Kankasa C, Secor WE, McClure HM, Strobert E, Else JG, Ruprecht RM. 2006. Molecularly cloned SHIV-1157ipd3N4: a highly replication-competent, mucosally transmissible R5 simian-human immunodeficiency virus encoding HIV clade C Env. J Virol 80:8729-8738. https://doi.org/10.1128/JVI.00558-06
23. Horn TF, Huitron-Resendiz S, Weed MR, Henriksen SJ, Fox HS. 1998. Early physiological abnormalities after simian immunodeficiency virus infection. Proc Natl Acad Sci U S A 95:15072-15077. https://doi.org/10.1073/pnas.95.25.15072
24. Wikoff WR, Pendyala G, Siuzdak G, Fox HS. 2008. Metabolomic analysis of the cerebrospinal fluid reveals changes in phospholipase expression in the CNS of SIV-infected macaques. J Clin Investig 118:2661-2669. https://doi.org/10.1172/JCI34138
25. Deleage C, Wietgrefe SW, Del Prete G, Morcock DR, Hao XP, Piatak M, Jr, Bess J, Anderson JL, Perkey KE, Reilly C, McCune JM, Haase AT, Lifson JD, Schacker TW, Estes JD. 2016. Defining HIV and SIV reservoirs in lymphoid tissues. Pathog Immun 1:68-106. https://doi.org/10.20411/pai.v1i1.100
26. Gendelman HE, Narayan O, Molineaux S, Clements JE, Ghotbi Z. 1985. Slow, persistent replication of lentiviruses: role of tissue macrophages and macrophage precursors in bone marrow. Proc Natl Acad Sci U S A 82:7086-7090. https://doi.org/10.1073/pnas.82.20.7086
27. Persidsky Y, Gendelman HE. 2003. Mononuclear phagocyte immunity and the neuropathogenesis of HIV-1 infection. J Leukoc Biol 74:691-701. https://doi.org/10.1189/jlb.0503205
28. Le Grand R, Nadal M, Cheret A, Roques P, Vaslin B, Matheux F, Theodoro F, Gras G, Gauthier L, Aubertin AM, et al. 1995. Infection of macaques after vaginal exposure to a primary isolate of SIVmac251. AIDS 9:308-309. https://doi.org/10.1097/00002030-199509030-00020
29. Robb ML, Eller LA, Kibuuka H, Rono K, Maganga L, Nitayaphan S, Kroon E, Sawe FK, Sinei S, Sriplienchan S, Jagodzinski LL, Malia J, Manak M, de Souza MS, Tovanabutra S, Sanders-Buell E, Rolland M, Dorsey-Spitz J, Eller MA, Milazzo M, Li Q, Lewandowski A, Wu H, Swann E, O'Connell RJ, Peel S, Dawson P, Kim JH, Michael NL, RV 217 Study Team. 2016. Prospective study of acute HIV-1 infection in adults in East Africa and Thailand. N Engl J Med 374:2120-2130. https://doi.org/10.1056/NEJMoa1508952
30. Perelson AS, Essunger P, Ho DD. 1997. Dynamics of HIV-1 and CD4+ lymphocytes in vivo. AIDS 11(Suppl A):S17-S24
31. Clayton F, Reka S, Cronin WJ, Torlakovic E, Sigal SH, Kotler DP. 1992. Rectal mucosal pathology varies with human immunodeficiency virus antigen content and disease stage. Gastroenterology 103:919-933. https://doi.org/10.1016/0016-5085(92)90026-U
32. Lim SG, Condez A, Lee CA, Johnson MA, Elia C, Poulter LW. 1993. Loss of mucosal CD4 lymphocytes is an early feature of HIV infection. Clin Exp Immunol 92:448-454. https://doi.org/10.1111/j.1365-2249.1993.tb03419.x
33. Schuetz A, Deleage C, Sereti I, Rerknimitr R, Phanuphak N, Phuang-Ngern Y, Estes JD, Sandler NG, Sukhumvittaya S, Marovich M, Jongrakthaitae S, Akapirat S, Fletscher JL, Kroon E, Dewar R, Trichavaroj R, Chomchey N, Douek DC, O'Connell RJ, Ngauy V, Robb ML, Phanuphak P, Michael NL, Excler JL, Kim JH, de Souza MS, Ananworanich J, Rv254/Search 010 Study Group. 2014. Initiation of ART during early acute HIV infection preserves mucosal Th17 function and reverses HIV-related immune activation. PLoS Pathog 10:e1004543. https://doi.org/10.1371/journal.ppat.1004543
34. Estes JD, Kityo C, Ssali F, Swainson L, Makamdop KN, Del Prete GQ, Deeks SG, Luciw PA, Chipman JG, Beilman GJ, Hoskuldsson T, Khoruts A, Anderson J, Deleage C, Jasurda J, Schmidt TE, Hafertepe M, Callisto SP, Pearson H, Reimann T, Schuster J, Schoephoerster J, Southern P, Perkey K, Shang L, Wietgrefe SW, Fletcher CV, Lifson JD, Douek DC, McCune JM, Haase AT, Schacker TW. 2017. Defining total-body AIDS-virus burden with implications for curative strategies. Nat Med 23:1271-1276
35. Marcondes MC, Burudi EM, Huitron-Resendiz S, Sanchez-Alavez M, Watry D, Zandonatti M, Henriksen SJ, Fox HS. 2001. Highly activated CD8(+) T cells in the brain correlate with early central nervous system dysfunction in simian immunodeficiency virus infection. J Immunol 167:5429-5438. https://doi.org/10.4049/jimmunol.167.9.5429
36. Aspelund A, Antila S, Proulx ST, Karlsen TV, Karaman S, Detmar M, Wiig H, Alitalo K. 2015. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med 212:991-999. https://doi.org/10.1084/jem.20142290
37. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J. 2015. Structural and functional features of central nervous system lymphatic vessels. Nature 523:337-341. https://doi.org/10.1038/nature14432
38. Absinta M, Ha SK, Nair G, Sati P, Luciano NJ, Palisoc M, Louveau A, Zaghloul KA, Pittaluga S, Kipnis J, Reich DS. 2017. Human and nonhuman primate meninges harbor lymphatic vessels that can be visualized noninvasively by MRI. Elife 6:e29738. https://doi.org/10.7554/eLife.29738
39. Lamers SL, Rose R, Ndhlovu LC, Nolan DJ, Salemi M, Maidji E, Stoddart CA, McGrath MS. 2016. The meningeal lymphatic system: a route for HIV brain migration? J Neurovirol 22:275-281. https://doi.org/10.1007/s13365-015-0399-y
40. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC
41. AVMA Panel On Euthanasia. 2013. Guidelines for the euthanasia of animals. American Veterinary Medical Association, Schaumburg, IL
42. Seaman MS, Santra S, Newberg MH, Philippon V, Manson K, Xu L, Gelman RS, Panicali D, Mascola JR, Nabel GJ, Letvin NL. 2005. Vaccineelicited memory cytotoxic T lymphocytes contribute to Mamu-A*01-associated control of simian/human immunodeficiency virus 89.6P replication in rhesus monkeys. J Virol 79:4580-4588. https://doi.org/10.1128/JVI.79.8.4580-4588.2005
43. Cline AN, Bess JW, Piatak M, Jr, Lifson JD. 2005. Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J Med Primatol 34:303-312. https://doi.org/10.1111/j.1600-0684.2005.00128.x
44. Gorantla S, Che M, Gendelman HE. 2005. Isolation, propagation, and HIV-1 infection of monocyte-derived macrophages and recovery of virus from brain and cerebrospinal fluid. Methods Mol Biol 304: 35-48