Reduced genetic diversity in lymphoid and central nervous system tissues and selection-induced tissue-specific compartmentalization of neuropathogenic SIVsmmFGb during acute infection

AIDS Research and Human Retroviruses

Volumn 25, Issue 6, 2009, Pages 583-601

  Reeve, Aaron B ^a   Patel, Kalpana ^a   Pearce, Nicholas C ^a   Augustus, Katherine V ^a   Domingues, Heber G ^c   O'Neil, Shawn P ^c   Novembre, Francis J ^a,b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRASE; NEF PROTEIN; NEF PROTEIN, SIV; SIV ENVELOPE GLYCOPROTEIN GP160; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXILLARY LYMPH NODE; BASAL GANGLION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; FRONTAL CORTEX; GENE SEQUENCE; GENETIC SELECTION; GENETIC VARIABILITY; HIPPOCAMPUS; LENTIVIRINAE; LYMPH NODE; LYMPHATIC SYSTEM; LYMPHOID TISSUE; MESENTERIC LYMPHADENITIS; NERVOUS SYSTEM; NEUROPATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; TISSUE SPECIFICITY; VIRUS ENVELOPE; VIRUS GENE; ANIMAL; CLASSIFICATION; DNA SEQUENCE; GENETIC POLYMORPHISM; GENETICS; ISOLATION AND PURIFICATION; MACACA; MOLECULAR GENETICS; MONKEY DISEASE; VIROLOGY;

ANIMALS; CENTRAL NERVOUS SYSTEM; GENE PRODUCTS, ENV; GENETIC VARIATION; INTEGRASES; LYMPH NODES; MACACA; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; SEQUENCE ANALYSIS, DNA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL PROTEINS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 67651172918     PISSN: 08892229     EISSN: None     Source Type: Journal    
DOI: 10.1089/aid.2008.0240     Document Type: Article

References (74)

1. Glenn AA, and Novembre FJ: A single amino acid change in gp41 is linked to the macrophage-only replication pheno-type of a molecular clone of simian immunodeficiency virus derived from the brain of a macaque with neuropathogenic infection. Virology 2004;325:297-307.
2. Hahn BH, Shaw GM, deCock KM, and Sharp PM: AIDS as a zoonosis: Scientific and public health implications. Science 2000;287:607-614.
3. Luo W, and Peterlin BM: Activation of the T-cell receptor signalling pathway by Nef from an aggressive strain of simian immunodeficiency virus. J Virol 1997;71:9531-9537.
4. Novembre FJ, De Rosayro J, O'Neil SP, Anderson DC, Klumpp SA, and McClure HM: Isolation and characterization of a neuropathogenic simian immunodeficiency virus derived from a sooty mangabey. J Virol 1998;72:8841-8851.
5. O'Neil SP, Suwyn C, Anderson DC, Niedziela G, Bradley J, Novembre FJ, Herndon JG, and McClure HM: Correlation of acute humoral response with brain virus burden and survival time in pigtailed macaques infected with the neuro-virulent simian immunodeficiency virus SIVsmmFGb. Am J Pathol 2004;164:1157-1172.
6. Skinner LM, Lamers SL, Sanders JC, Eyster ME, Goodenow MM, and Klatzman M: Analysis of a large collection of natural HIV-1 integrase sequences, including those from long-term nonprogressors. J Acquir Immune Defic Syndr Hum Retrovirol 1998;19:99-110.
7. Luciano CA, Pardo CA, and McArthur JC: Recent developments in the HIV neuropathies. Curr Opin Neurol 2003;16: 403-409.
8. Price RW: AIDS dementia complex. HIV InSite Knowledge Base Chapter, 1998. Available at http://hivinsite.ucsf.edu/ InSite?page/kb-04-01-03 (accessed May 2009).
9. Sharpless N, Gilbert D, Vandercam B, Zhou JM, Verdin E, Ronnett G, Friedman E, and Dubois-Dalcq M: The restricted nature of HIV-1 tropism for cultured neural cells. Virology 1992;191:813-825.
10. Ghafouri M, Amini S, Khalili K, and Sawaya BE: HIV-1 associated dementia: Symptoms and causes. Retrovirology 2006;3:28-38.
11. Whetter LE, Ojukwu IC, Novembre FJ, and Dewhurst S: Pathogenesis of simian immunodeficiency virus infection. J Gen Virol 1999;80:1557-1568.
12. Wiley CA, Soontonniyomkij V, Radhakrishnan L, Masliah E, Mellors J, Hermann SA, Dailey P, and Achim CL: Distribution of brain HIV load in AIDS. Brain Pathol. 1998;8:277-284.
13. Acheampong EA, Parveen Z, Muthoga LW, Kalayeh M, Mukhtar M, and Pomerantz RJ: Human immunodeficiency virus type 1 Nef potently induces apoptosis in primary human brain microvascular endothelial cells via the activation of caspases. J Virol 2005;79:4257-4269.
14. Dore GJ, McDonald A, Li Y, Kaldor JM, and Brew BJ: Marked improvement in survival following AIDS dementia complex in the era of highly active antiretroviral therapy. AIDS 2003;17:1539-1545.
15. Enting RH, Prins JM, Jurriaans S, Brinkman K, Portegies P, and Lange JMA: Concentrations of human immunodeficiency virus type 1 RNA in cerebrospinal fluid after anti-retroviral treatment initiated during primary HIV-1 infection. Clin Infect Dis 2001;32:1095-1099.
16. Gisolf EH, Enting RH, Jurriaans S, de Wolf F, van der Ende ME, Hoetelmans RMW, Portegies P, and Danner SA: Cere-brospinal fluid HIV-1 RNA during treatment with ritonavir/ saquinavir or ritonavir/saquinavir/stavudine. AIDS 2000;14: 1583-1589.
17. Sacktor N: The epidemiology of human immunodeficiency virus-associated neurological disease in the era of highly active antiretroviral therapy. J Neurovirol 2002;8:115-121.
18. Groothius DR, and Levy RM: The entry of antiviral and antiretroviral drugs into the central nervous system. J Neu-rovirol 1997;3:387-400.
19. Nath A, and Sacktor N: Influence of highly active anti-retroviral therapy on persistence of HIV in the central nervous system. Curr Opin Neurol 2006;19:358-361.
20. McArthur JC, Haughey N, Gartner S, Conant K, Pardo C, Nath A, and Sacktor N: Human immunodeficiency virus-associated dementia: An evolving disease. J Neurovirol 2003; 9:205-221.
21. Desrosiers RC: The simian immunodeficiency viruses. Annu Rev Immunol 1990;8:557-578.
22. McClure HM, Anderson DC, Fultz PN, Ansari AA, Lock-wood E, and Brodie A: Spectrum of disease in macaque monkeys chronically infected with SIV/SMM. Vet Immunol Immunopathol 1989;21:13-24.
23. Rausch DM, Murray EA, and Eiden LE: The SIV-infected rhesus monkey model for HIV-associated dementia and implication for neurological disease. J Leukoc Biol 1999;65: 466-474.
24. Sopper S, Koutsilieri E, Scheller C, Czub S, Riederer P, and ter Meulen V: Macaque animal model for HIV-induced neurological disease. J Neural Transm 2002;109:747-766.
25. Clemens JE, Babas T, Mankowski JL, Suryanarayana K, Piatak Jr M, Tarwater PM, Lifson JD, and Zink MC: 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 2002;186:905-913.
26. Lackner AA, Smith MO, Munn RJ, Martfeld DJ, Gardner MB, Marx PA, and Dandekar S: Localization of simian immunodeficiency virus in the central nervous system of rhesus macaques. Am J Pathol 1991;139:609-621.
27. Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, deBakker C, Alvarez X, and Lackner AA: 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 2001;193:905-915.
28. Chakrabarti L, Hurtrel M, Maire M, Vazeux R, Dormont D, Montagnier L, and Hurtrel B: Early viral replication in the brain of SIV-infected rhesus monkeys. Am J Pathol 1991;139: 1273-1280.
29. Davis LE, Hjelle BL, Miller VE, Palmer DL, Llewellyn AL, Merlin TL, Young SA, Mills RG, WachsmanW, and Wiley CA: Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 1992;42:1736-1739.
30. Gouldsmit J, deWolf F, Paul DA, Epstein LG, Lange AJM, Krone WJA, Speelman H, Wolters EC, Van der Noordaa J, Oleske JM, Van der Helm HJ, and Coutinho RA: Expression of human immunodeficiency virus antigen (HIV-Ag) in serum and cerebrospinal fluid during acute and chronic infection. Lancet 1986;2:177-180.
31. Ho DD, Rota TR, Schooley RT, Kaplan JC, Allan JD, Groopman JE, Resnick L, Felsenstein D, Andrews CA, and Hirsch MS: Isolation of HTLV-III from cerebrospinal fluid and neural tissues of patients with neurologic syndromes related to the acquired immunodeficiency syndrome. N Engl J Med 1985;313:1493-1497.
32. Zink MC, Amedee AM, Mankowski JL, Craig L, Didier P, Carter DL, Munoz A, Murphey-Corb M, and Clements JE: Pathogenesis of SIV encephalitis. selection and replication of neurovirulent SIV. Am J Pathol 1997;151:793-803.
33. Flaherty MT, Hauer DA, Mankowski JL, Zink MC, and Clements JE: Molecular and biological characterization of a neurovirulent molecular clone of simian immunodeficiency virus. J Virol 1997;71:5790-5798.
34. Mankowski JL, Flaherty MT, Spelman JP, Hauer DA, Didier PJ, Amedee AM, Murphey-Corb M, Kirstein LM, Munoz A, Clements JE, and Zink MC: Pathogenesis of simian immunodeficiency virus encephalitis: Viral determinants of neu-rovirulence. J Virol 1997;71:6055-6060.
35. Cichutek K, Merget H, Norley S, Linde R, Kruez W, Gahr M, and Kurth R: Development of a quasispecies of human immunodeficiency virus type 1 in vivo. Proc Natl Acad Sci USA 1992;89:7365-7369.
36. Wain-Hobson S: Human immunodeficiency virus type 1 quasispecies in vivo and ex vivo. Curr Top Microbiol Immunol 1992;176:181-193.
37. Strizki JM, Albright AV, Sheng H, O'Connor M, Perrin L, and Gonzalez-Scarano F: Infection of primary human mi-croglia and monocyte-derived macrophages with human immunodeficiency virus type 1 isolates: Evidence of differential tropism. J Virol 1996;70:7654-7662.
38. Chen MF, Westmoreland S, Ryzhova EV, Martin-Garcia J, Soldan SS, Lackner A, and Gonzalez-Scarano F: Simian immunodeficiency virus envelope compartmentalizes in brains egions independent of neuropathology. J Neurovirol 2006; 12:73-89.
39. Poss M, Rodrigo AG, Gosink JJ, Learn GH, Panteleeff DDV, Martin Jr HL, Bwayo J, Kreiss JK, and Overbaugh J: Evolution of envelope sequences from the genital tract and peripheral blood of women infected with clade A human immunodeficiency virus type 1. J Virol 1998;72:8240-8251.
40. Ritola K, Robertson K, Fiscus SA, Hall C, and Swanstrom R: Increased human immunodeficiency virus type 1 (HIV-1) env compartmentalization in the presence of HIV-1-associated dementia. J Virol 2005;79:10830-10834.
41. Collins KR, Quinones-Mateu ME, Wu M, Luzze H, Johnson JL, Hirsch C, Toossi Z, and Arts EJ: Human immunodeficiency virus type 1 quasispecies at the sites of Mycobacterium tuberculosis infection contribute to systemic HIV-1 heterogeneity. J Virol 2002;76:1697-1706.
42. Smith MS, Niu Y, Buch S, Li Z, Adany I, Pinson DM, Potula R, Novembre FJ, and Narayan O: Active simian immunodeficiency virus (strain smmPGm) infection in macaque central nervous system correlates with neurological disease. J Acquir Immune Defic Syndr 2005;38:518-530.
43. Reinke R, Steffen NR, and Robinson WE: Natural selection results in conservation of HIV-1 integrase activity despite sequence variability. AIDS 2001;15:823-830.
44. Chiu TK, and Davies DR: Structure and function of HIV-1 integrase. Curr Top Med Chem 2004;4:965-977.
45. Gorry PR, Howard JL, Churchill MJ, Anderson JL, Cunningham A, Adrian D, McPhee DA, and Purcell DFJ: Diminished production of human immunodeficiency virus type 1 in astrocytes results from inefficient translation of gag, env and nef mRNAs despite efficient expression of Tat and Rev. J Virol 1999;73:352-361.
46. Overholser ED, Coleman GD, Bennett JL, Casaday RJ, Zink MC, Barber SA, and Clements JE: Expression of simian immunodeficiency virus (SIV) Nef inastrocytes during acute and terminal infection and requirement of Nef for optimal replication of neurovirulent SIV in vitro. J Virol 2003;77:6855-6866.
47. van Marle G, Henry S, Todoruk T, Sullivan A, Silva C, Rourke SB, Holden J, McArthur JC, Gill MJ, and Power C: Human immunodeficiency virus type 1 Nef protein mediates neural cell death: A neurotoxic role for IP-10. Virology 2004;329:302-318.
48. Jurkiewicz E, Hunsmann G, Schaffner J, Nisslein T, Luke W, and Petry H: Identification of the V1 region as a linear neutralizing epitope of the simian immunodeficiency virus SIVmac envelope glycoprotein. J Virol 1997;71:9475-9481.
49. Kim S, Pang H, and Kay MS: Peptide mimic of the HIV envelope gp120-gp41 interface. J Mol Biol 2008;376:786-797.
50. Dreyer EB, Kaiser PK, Offermann JT, and Lipton SA: HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists. Science 1990;248:364-367.
51. Swingler S: Pathogenic mechanisms of neuronal damage in the AIDS dementia complex. J Clin Pathol Mol Pathol 1997;50:72-76.
52. Starcich BR, Hahn BH, Shaw GM, McNeely PD, Modrow S, Wolf H, Parks ES, Parks WP, Josephs SF, Gallo RC, and Wong-Staal F: Identification and characterization of conserved and variable regions in the envelope gene of HTLV-III/LAV, the retrovirus of AIDS. Cell 1986;45:637-648.
53. Petry H, Pekrun K, Hunsmann G, Jurkiewicz E, and Luke W: Naturally occurring V1-Env region variants mediate simian immunodeficiency virus SIVmac escape from a high-titer neutralizing antibodies induced by a protective subunit vaccine. J Virol 2000;74:11145-11152.
54. Burkala EJ, He J, West JT, Wood C, and Petito CK: Com-partmentalization of HIV-1 in the central nervous system: Role of the choroids plexus. AIDS 2005;19:675-684.
55. Zarate S, Pond KSL, Shapshak P, and Frost SDW: Comparative study of methods for detecting sequence compart-mentalization in human immunodeficiency virus type 1. J Virol 2007;81:6643-6651.
56. Renjifo B, Chung M, Gilbert P, Mwakagile D, Msamanga G, Fawzi W, and Essex M: In utero transmission of quasispecies among human immunodeficiency type 1 genotypes. Virology 2003;307:278-282.
57. Greenier JL, Miller CJ, Lu D, Dailey PJ, Lu FX, Kunstman KJ, Wolinsky SM, and Marthas ML: Route of simian immunodeficiency virus inoculation determines the complexity but not the identity of viral variant populations that infect rhesus macaques. J Virol 2001;75:3753-3765.
58. Neildez O, Le Grand R, Caufour P, Vaslin B, Cheret A, Matheux F, Theodoro F, Roques P, and Dormont D: Selective quasispecies transmission after systemic or mucousal exposure of macaques to simian immunodeficiency virus. Virology 1998;243:12-20.
59. Brew BJ, Rosenblum M, Cronin K, and Price RW: AIDS dementia complex and HIV-1 brain infection: Clinical-virological correlations. Anna Neurol 1995;38:563-570.
60. Walter BL, Wehrly K, Swanstrom R, Platt E, Kabat D, and Chesebro B: Role of low CD4 Levels in the influence of human immunodeficiency virus type 1 envelope V1 and V2 regions on entry and spread in macrophages. J Virol 2005;79: 4828-4837.
61. Rybarcyzk B: Molecular evolution: The HIV envelope protein. Evol Educ Outreach 2008;1:179-183.
62. Kazazi F, Mathijs J, Foley P, and Cunningham AL: Variations in CD4 expression by human monocytes and macrophages and their relationship to infection with the human immunodeficiency virus. J Gen Virol 1989;70: 2661-2672.
63. Badley AD, Pilon AA, Landay A, and Lynch DH: Mechanisms of HIV-associated lymphocyte apoptosis. Blood 2000; 96:2951-2964.
64. Das SR, and Jameel S: Biology of the Nef protein. Indian J Med Res 2005;121:315-332.
65. Olivetta E, and Federico M: HIV-1 Nef protects human-monocyte-derived macrophages from HIV-1-induced apo-ptosis. Exp Cell Res 2006;312:890-900.
66. Babas T, Munoz D, Mankowski JL, Tarwater PM, Clements JE, and Zink MC: Role of microglial cells in selective replication of simian immunodeficiency virus genotypes in the brain. J Virol 2003;77:208-216.
67. Watkins BA, Dorn HH, Kelly WB, Armstrong RC, Potts BJ, Michaels F, Kufta CV, and Dubois-Dalcq M: Specific tropism of HIV-1 for microglial cells in primary human brain cultures. Science 1990;249:549-553.
68. Watry D, Lane TE, Streb M, and Fox HS: Transfer of neu-ropathogenic simian immunodeficiency virus with naturally infected microglia. Am J Pathol 1995;146:914-923.
69. Mankowski JL, Spelman JP, Ressetar HG, Strandberg JD, Laterra J, Carter DL, Clements JE, and Zink MC: Neuro-virulent simian immunodeficiency virus replicates productively in endothelial cells of the central nervous system in vivo and in vitro. J Virol 1994;68:8202-8208.
70. Maslin CLV, Kedzierska K, Webster NL, Muller WA, and Crowe SM: Transendothelial migration of monocytes: The underlying molecular mechanisms and consequences of HIV-1 infection. Curr HIV Res 2005;3:303-312.
71. Ohagen A, Devitt A, Kunstman KJ, Gorry PR, Rose PP, Korber B, Taylor J, Levy R, Murphy RL, Wolinsky SM, and Gabudza D: Genetic and functional analysis of full-length human immunodeficiency virus type 1 env genes derived from brain and blood of patients with AIDS. J Virol 2003;77: 12336-12345.
72. Korber BTM, Kunstman JK, Patterson BK, Furtado M, McEvilly MM, Levy R, and Wolinsky SM: Genetic differences between blood- and brain-derived viral sequences from human immunodeficiency virus type 1-infected patients: Evidence of conserved elements in theV3 region of the envelope protein of brain-derived sequences. J Virol 1994;68: 7467-7481.
73. Sharp P: In search of molecular Darwinism. Nature 1997; 385:111-112.
74. Piguet V, and D. Trono: A structure-function analysis of the Nef protein of primate lentiviruses. Hum Retroviruses AIDS 1999:448-459.