Macaque species susceptibility to simian immunodeficiency virus: increased incidence of SIV central nervous system disease in pigtailed macaques versus rhesus macaques

Journal of NeuroVirology

Volumn 21, Issue 2, 2015, Pages 148-158

  Beck, Sarah E ^a   Kelly, Kathleen M ^a,c   Queen, Suzanne E ^a   Adams, Robert J ^a   Zink, M Christine ^a   Tarwater, Patrick M ^b   Mankowski, Joseph L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Paul L Foster School of Medicine   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

CNS disease; Macaque; MHC class I; SIV

Indexed keywords

HLA ANTIGEN CLASS 1;

ANIMAL; DISEASE COURSE; DISEASE PREDISPOSITION; HIV ASSOCIATED DEMENTIA; IMMUNOLOGY; MACACA NEMESTRINA; RHESUS MONKEY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIROLOGY;

AIDS DEMENTIA COMPLEX; ANIMALS; DISEASE PROGRESSION; DISEASE SUSCEPTIBILITY; HISTOCOMPATIBILITY ANTIGENS CLASS I; MACACA MULATTA; MACACA NEMESTRINA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84937758110     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-015-0313-7     Document Type: Article

References (46)

1. Andrade MC, Leite JP, Cabello PH (2009) Frequency of the major histocompatibility complex Mamu-A*01 allele in a closed breeding colony of rhesus monkey (Macaca mulatta) from Brazil. J Med Primatol 38:39–41
2. Batten CJ, De Rose R, Wilson KM, Agy MB, Chea S, Stratov I, Montefiori DC, Kent SJ (2006) Comparative evaluation of simian, simian-human, and human immunodeficiency virus infections in the pigtail macaque (Macaca nemestrina) model. AIDS Res Hum Retroviruses 22:580–8
3. Benveniste RE, Morton WR, Clark EA, Tsai CC, Ochs HD, Ward JM, Kuller L, Knott WB, Hill RW, Gale MJ et al (1988) Inoculation of baboons and macaques with simian immunodeficiency virus/Mne, a primate lentivirus closely related to human immunodeficiency virus type 2. J Virol 62:2091–101
4. Blankson JN (2010) Control of HIV-1 replication in elite suppressors. Discov Med 9:261–6
5. Buch SJ, Villinger F, Pinson D, Hou Y, Adany I, Li Z, Dalal R, Raghavan R, Kumar A, Narayan O (2002) Innate differences between simian-human immunodeficiency virus (SHIV)(KU-2)-infected rhesus and pig-tailed macaques in development of neurological disease. Virology 295:54–62
6. 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 186:905–13
7. Clements JE, Mankowski JL, Gama L, Zink MC (2008) The accelerated simian immunodeficiency virus macaque model of human immunodeficiency virus-associated neurological disease: from mechanism to treatment. J Neurovirol 14:309–17
8. Cohen J (2000) AIDS research. Vaccine studies stymied by shortage of animals. Science 287:959–60
9. Czub S, Muller JG, Czub M, Muller-Hermelink HK (1996) Impact of various simian immunodeficiency virus variants on induction and nature of neuropathology in macaques. Res Virol 147:165–70
10. Goulder PJ, Watkins DI (2008) Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat Rev Immunol 8:619–30
11. Goulder PJ, Bunce M, Krausa P, McIntyre K, Crowley S, Morgan B, Edwards A, Giangrande P, Phillips RE, McMichael AJ (1996) Novel, cross-restricted, conserved, and immunodominant cytotoxic T lymphocyte epitopes in slow progressors in HIV type 1 infection. AIDS Res Hum Retroviruses 12:1691–8
12. Hatziioannou T, Del Prete GQ, Keele BF, Estes JD, McNatt MW, Bitzegeio J, Raymond A, Rodriguez A, Schmidt F, Mac Trubey C, Smedley J, Piatak M Jr, KewalRamani VN, Lifson JD, Bieniasz PD (2014) HIV-1-induced AIDS in monkeys. Science 344:1401–5
13. Kaizu M, Borchardt GJ, Glidden CE, Fisk DL, Loffredo JT, Watkins DI, Rehrauer WM (2007) Molecular typing of major histocompatibility complex class I alleles in the Indian rhesus macaque which restrict SIV CD8+ T cell epitopes. Immunogenetics 59:693–703
14. Kanthaswamy S, Kou A, Satkoski J, Penedo MC, Ward T, Ng J, Gill L, Lerche NW, Erickson BJ, Smith DG (2010) Genetic characterization of specific pathogen-free rhesus macaque (Macaca mulatta) populations at the California National Primate Research Center (CNPRC). Am J Primatol 72:587–99
15. Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, Goedert JJ, Winkler C, O’Brien SJ, Rinaldo C, Detels R, Blattner W, Phair J, Erlich H, Mann DL (1996) Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med 2:405–11
16. Klatt NR, Canary LA, Vanderford TH, Vinton CL, Engram JC, Dunham RM, Cronise HE, Swerczek JM, Lafont BA, Picker LJ, Silvestri G, Brenchley JM (2012) Dynamics of simian immunodeficiency virus SIVmac239 infection in pigtail macaques. J Virol 86:1203–13
17. Kneitz C, Kerkau T, Muller J, Coulibaly C, Stahl-Hennig C, Hunsmann G, Hunig T, Schimpl A (1993) Early phenotypic and functional alterations in lymphocytes from simian immunodeficiency virus infected macaques. Vet Immunol Immunopathol 36:239–55
18. Kyes RC, Jones-Engel L, Chalise MK, Engel G, Heidrich J, Grant R, Bajimaya SS, McDonough J, Smith DG, Ferguson B (2006) Genetic characterization of rhesus macaques (Macaca mulatta) in Nepal. Am J Primatol 68:445–55
19. Laast VA, Pardo CA, Tarwater PM, Queen SE, Reinhart TA, Ghosh M, Adams RJ, Zink MC, Mankowski JL (2007) Pathogenesis of simian immunodeficiency virus-induced alterations in macaque trigeminal ganglia. J Neuropathol Exp Neurol 66:26–34
20. Laast VA, Shim B, Johanek LM, Dorsey JL, Hauer PE, Tarwater PM, Adams RJ, Pardo CA, McArthur JC, Ringkamp M, Mankowski JL (2011) Macrophage-mediated dorsal root ganglion damage precedes altered nerve conduction in SIV-infected macaques. Am J Pathol 179:2337–45
21. Letvin NL, King NW (1990) Immunologic and pathologic manifestations of the infection of rhesus monkeys with simian immunodeficiency virus of macaques. J Acquir Immune Defic Syndr 3:1023–40
22. Lim SY, Chan T, Gelman RS, Whitney JB, O’Brien KL, Barouch DH, Goldstein DB, Haynes BF, Letvin NL (2010) Contributions of Mamu-A*01 status and TRIM5 allele expression, but not CCL3L copy number variation, to the control of SIVmac251 replication in Indian-origin rhesus monkeys. PLoS Genet 6:e1000997
23. Limou S, Zagury JF (2013) Immunogenetics: genome-wide association of Non-progressive HIV and viral load control: HLA genes and beyond. Front Immunol 4:118
24. Mankowski JL, Flaherty MT, Spelman JP, Hauer DA, Didier PJ, Amedee AM, Murphey-Corb M, Kirstein LM, Munoz A, Clements JE, Zink MC (1997) Pathogenesis of simian immunodeficiency virus encephalitis: viral determinants of neurovirulence. J Virol 71:6055–60
25. Mankowski JL, Queen SE, Clements JE, Zink MC (2004) Cerebrospinal fluid markers that predict SIV CNS disease. J Neuroimmunol 157:66–70
26. Mankowski JL, Queen SE, Fernandez CS, Tarwater PM, Karper JM, Adams RJ, Kent SJ (2008) Natural host genetic resistance to lentiviral CNS disease: a neuroprotective MHC class I allele in SIV-infected macaques. PLoS One 3:e3603
27. McClure HM, Anderson DC, Fultz PN, Ansari AA, Lockwood E, Brodie A (1989) Spectrum of disease in macaque monkeys chronically infected with SIV/SMM. Vet Immunol Immunopathol 21:13–24
28. Migueles SA, Sabbaghian MS, Shupert WL, Bettinotti MP, Marincola FM, Martino L, Hallahan CW, Selig SM, Schwartz D, Sullivan J, Connors M (2000) HLA B*5701 is highly associated with restriction of virus replication in a subgroup of HIV-infected long term nonprogressors. Proc Natl Acad Sci U S A 97:2709–14
29. Mothe BR, Weinfurter J, Wang C, Rehrauer W, Wilson N, Allen TM, Allison DB, Watkins DI (2003) Expression of the major histocompatibility complex class I molecule Mamu-A*01 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 77:2736–40
30. Muhl T, Krawczak M, Ten Haaft P, Hunsmann G, Sauermann U (2002) MHC class I alleles influence set-point viral load and survival time in simian immunodeficiency virus-infected rhesus monkeys. J Immunol 169:3438–46
31. Nakamura M, Takahara Y, Ishii H, Sakawaki H, Horiike M, Miura T, Igarashi T, Naruse TK, Kimura A, Matano T, Matsuoka S (2011) Major histocompatibility complex class I-restricted cytotoxic T lymphocyte responses during primary simian immunodeficiency virus infection in Burmese rhesus macaques. Microbiol Immunol 55:768–73
32. O’Connor DH, Mothe BR, Weinfurter JT, Fuenger S, Rehrauer WM, Jing P, Rudersdorf RR, Liebl ME, Krebs K, Vasquez J, Dodds E, Loffredo J, Martin S, McDermott AB, Allen TM, Wang C, Doxiadis GG, Montefiori DC, Hughes A, Burton DR, Allison DB, Wolinsky SM, Bontrop R, Picker LJ, Watkins DI (2003) Major histocompatibility complex class I alleles associated with slow simian immunodeficiency virus disease progression bind epitopes recognized by dominant acute-phase cytotoxic-T-lymphocyte responses. J Virol 77:9029–40
33. Pal R, Venzon D, Letvin NL, Santra S, Montefiori DC, Miller NR, Tryniszewska E, Lewis MG, VanCott TC, Hirsch V, Woodward R, Gibson A, Grace M, Dobratz E, Markham PD, Hel Z, Nacsa J, Klein M, Tartaglia J, Franchini G (2002) ALVAC-SIV-gag-pol-env-based vaccination and macaque major histocompatibility complex class I (A*01) delay simian immunodeficiency virus SIVmac-induced immunodeficiency. J Virol 76:292–302
34. Pereyra F, Jia X, McLaren PJ, Telenti A, de Bakker PI, Walker BD, Ripke S, Brumme CJ, Pulit SL, Carrington M, Kadie CM, Carlson JM, Heckerman D, Graham RR, Plenge RM, Deeks SG, Gianniny L, Crawford G, Sullivan J, Gonzalez E, Davies L, Camargo A, Moore JM, Beattie N, Gupta S, Crenshaw A, Burtt NP, Guiducci C, Gupta N, Gao X, Qi Y, Yuki Y, Piechocka-Trocha A, Cutrell E, Rosenberg R, Moss KL, Lemay P, O’Leary J, Schaefer T, Verma P, Toth I, Block B, Baker B, Rothchild A, Lian J, Proudfoot J, Alvino DM, Vine S, Addo MM, Allen TM, Altfeld M, Henn MR, Le Gall S, Streeck H, Haas DW, Kuritzkes DR, Robbins GK, Shafer RW, Gulick RM, Shikuma CM, Haubrich R, Riddler S, Sax PE, Daar ES, Ribaudo HJ, Agan B, Agarwal S, Ahern RL, Allen BL, Altidor S, Altschuler EL, Ambardar S, Anastos K, Anderson B, Anderson V, Andrady U, Antoniskis D, Bangsberg D, Barbaro D, Barrie W, Bartczak J, Barton S, Basden P, Basgoz N, Bazner S, Bellos NC, Benson AM, Berger J, Bernard NF, Bernard AM, Birch C, Bodner SJ, Bolan RK, Boudreaux ET, Bradley M, Braun JF, Brndjar JE, Brown SJ, Brown K, Brown ST et al (2010) The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 330:1551–7
35. Polacino P, Larsen K, Galmin L, Suschak J, Kraft Z, Stamatatos L, Anderson D, Barnett SW, Pal R, Bost K, Bandivdekar AH, Miller CJ, Hu SL (2008) Differential pathogenicity of SHIV infection in pig-tailed and rhesus macaques. J Med Primatol 37(Suppl 2):13–23
36. Pratt BF, O’Connor DH, Lafont BA, Mankowski JL, Fernandez CS, Triastuti R, Brooks AG, Kent SJ, Smith MZ (2006) MHC class I allele frequencies in pigtail macaques of diverse origin. Immunogenetics 58:995–1001
37. Queen SE, Mears BM, Kelly KM, Dorsey JL, Liao Z, Dinoso JB, Gama L, Adams RJ, Zink MC, Clements JE, Kent SJ, Mankowski JL (2011) Replication-competent simian immunodeficiency virus (SIV) Gag escape mutations archived in latent reservoirs during antiretroviral treatment of SIV-infected macaques. J Virol 85:9167–75
38. Reed JS, Sidney J, Piaskowski SM, Glidden CE, Leon EJ, Burwitz BJ, Kolar HL, Eernisse CM, Furlott JR, Maness NJ, Walsh AD, Rudersdorf RA, Bardet W, McMurtrey CP, O’Connor DH, Hildebrand WH, Sette A, Watkins DI, Wilson NA (2011) The role of MHC class I allele Mamu-A*07 during SIV(mac)239 infection. Immunogenetics 63:789–807
39. Schneidewind A, Brockman MA, Yang R, Adam RI, Li B, Le Gall S, Rinaldo CR, Craggs SL, Allgaier RL, Power KA, Kuntzen T, Tung CS, LaBute MX, Mueller SM, Harrer T, McMichael AJ, Goulder PJ, Aiken C, Brander C, Kelleher AD, Allen TM (2007) Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication. J Virol 81:12382–93
40. Smith MZ, Dale CJ, De Rose R, Stratov I, Fernandez CS, Brooks AG, Weinfurter J, Krebs K, Riek C, Watkins DI, O’Connor DH, Kent SJ (2005a) Analysis of pigtail macaque major histocompatibility complex class I molecules presenting immunodominant simian immunodeficiency virus epitopes. J Virol 79:684–95
41. Smith MZ, Fernandez CS, Chung A, Dale CJ, De Rose R, Lin J, Brooks AG, Krebs KC, Watkins DI, O’Connor DH, Davenport MP, Kent SJ (2005b) The pigtail macaque MHC class I allele Mane-A*10 presents an immundominant SIV Gag epitope: identification, tetramer development and implications of immune escape and reversion. J Med Primatol 34:282–93
42. Spudich S (2013) HIV and neurocognitive dysfunction. Curr HIV/AIDS Rep 10:235–43
43. Stephens EB, Galbreath D, Liu ZQ, Sahni M, Li Z, Lamb-Wharton R, Foresman L, Joag SV, Narayan O (1997) Significance of macrophage tropism of SIV in the macaque model of HIV disease. J Leukoc Biol 62:12–9
44. Wu Y, Gao F, Liu J, Qi J, Gostick E, Price DA, Gao GF (2011) Structural basis of diverse peptide accommodation by the rhesus macaque MHC class I molecule Mamu-B*17: insights into immune protection from simian immunodeficiency virus. J Immunol 187:6382–92
45. Zink MC, Amedee AM, Mankowski JL, Craig L, Didier P, Carter DL, Munoz A, Murphey-Corb M, Clements JE (1997) Pathogenesis of SIV encephalitis. Selection and replication of neurovirulent SIV. Am J Pathol 151:793–803
46. Zink MC, Suryanarayana K, Mankowski JL, Shen A, Piatak M Jr, Spelman JP, Carter DL, Adams RJ, Lifson JD, Clements JE (1999) High viral load in the cerebrospinal fluid and brain correlates with severity of simian immunodeficiency virus encephalitis. J Virol 73:10480–8