Compartmentalization and clonal amplification of HIV-1 variants in the cerebrospinal fluid during primary infection

Journal of Virology

Volumn 84, Issue 5, 2010, Pages 2395-2407

  Schnell, Gretja ^a   Price, Richard W ^b   Swanstrom, Ronald ^a   Spudich, Serena ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

ARTICLE; BLOOD ANALYSIS; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CEREBROSPINAL FLUID ANALYSIS; CLINICAL ARTICLE; ENVELOPE GENE; EVOLUTIONARY ADAPTATION; GENE AMPLIFICATION; GENE SEQUENCE; GENE TARGETING; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOTYPE; HETERODUPLEX ANALYSIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIMARY INFECTION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE; VIRUS REPLICATION; VIRUS TRANSMISSION;

AIDS DEMENTIA COMPLEX; AMINO ACID SEQUENCE; BASE SEQUENCE; CENTRAL NERVOUS SYSTEM; GENE AMPLIFICATION; GENES, ENV; GENETIC VARIATION; HIV INFECTIONS; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77649195668     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01863-09     Document Type: Article

References (64)

1. Blennow, K., P. Fredman, A. Wallin, C. G. Gottfries, I. Karlsson, G. Langstrom, I. Skoog, L. Svennerholm, and C. Wikkelso. 1993. Protein analysis in cerebrospinal fluid. II. Reference values derived from healthy individuals 18-88 years of age. Eur. Neurol. 33:129-133.
2. Boisse, L., M. J. Gill, and C. Power. 2008. HIV infection of the central nervous system: clinical features and neuropathogenesis. Neurol. Clin. 26:799-819.
3. Brew, B. J., R. B. Bhalla, M. Paul, H. Gallardo, J. C. McArthur, M. K. Schwartz, and R. W. Price. 1990. Cerebrospinal fluid neopterin in human immunodeficiency virus type 1 infection. Ann. Neurol. 28:556-560.
4. Chenna, R., H. Sugawara, T. Koike, R. Lopez, T. J. Gibson, D. G. Higgins, and J. D. Thompson. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-3500.
5. Cinque, P., A. Bestetti, R. Marenzi, S. Sala, M. Gisslen, L. Hagberg, and R. W. Price. 2005. Cerebrospinal fluid interferon-gamma-inducible protein 10 (IP-10, CXCL10) in HIV-1 infection. J. Neuroimmunol. 168:154-163.
6. Cinque, P., L. Vago, M. Mengozzi, V. Torri, D. Ceresa, E. Vicenzi, P. Transidico, A. Vagani, S. Sozzani, A. Mantovani, A. Lazzarin, and G. Poli. 1998. Elevated cerebrospinal fluid levels of monocyte chemotactic protein-1 correlate with HIV-1 encephalitis and local viral replication. AIDS 12:1327-1332.
7. Cosenza, M. A., M. L. Zhao, Q. Si, and S. C. Lee. 2002. Human brain parenchymal microglia express CD14 and CD45 and are productively infected by HIV-1 in HIV-1 encephalitis. Brain Pathol. 12:442-455.
8. Daar, E. S., S. Little, J. Pitt, J. Santangelo, P. Ho, N. Harawa, P. Kerndt, J. V. Glorgi, J. Bai, P. Gaut, D. D. Richman, S. Mandel, and S. Nichols. 2001. Diagnosis of primary HIV-1 infection. Los Angeles County Primary HIV Infection Recruitment Network. Ann. Intern. Med. 134:25-29.
9. Delwart, E. L., and C. J. Gordon. 1997. Tracking changes in HIV-1 envelope quasispecies using DNA heteroduplex analysis. Methods 12:348-354.
10. Delwart, E. L., J. I. Mullins, P. Gupta, G. H. Learn, Jr., M. Holodniy, D. Katzenstein, B. D. Walker, and M. K. Singh. 1998. Human immunodeficiency virus type 1 populations in blood and semen. J. Virol. 72:617-623.
11. Delwart, E. L., H. W. Sheppard, B. D. Walker, J. Goudsmit, and J. I. Mullins. 1994. Human immunodeficiency virus type 1 evolution in vivo tracked by DNA heteroduplex mobility assays. J. Virol. 68:6672-6683.
12. Delwart, E. L., E. G. Shpaer, J. Louwagie, F. E. McCutchan, M. Grez, H. Rubsamen-Waigmann, and J. I. Mullins. 1993. Genetic relationships determined by a DNA heteroduplex mobility assay: analysis of HIV-1 env genes. Science 262:1257-1261.
13. Dunfee, R. L., E. R. Thomas, P. R. Gorry, J. Wang, J. Taylor, K. Kunstman, S. M. Wolinsky, and D. Gabuzda. 2006. The HIV Env variant N283 enhances macrophage tropism and is associated with brain infection and dementia. Proc. Natl. Acad. Sci. U. S. A. 103:15160-15165.
14. Dunfee, R. L., E. R. Thomas, J. Wang, K. Kunstman, S. M. Wolinsky, and D. Gabuzda. 2007. Loss of the N-linked glycosylation site at position 386 in the HIV envelope V4 region enhances macrophage tropism and is associated with dementia. Virology 367:222-234.
15. Edmonson, P. F., and J. I. Mullins. 1992. Efficient amplification of HIV half-genomes from tissue DNA. Nucleic Acids Res. 20:4933.
16. Fishman, R. A.1992. Cerebrospinal fluid in diseases of the nervous system, 2nd ed. W. B. Saunders Company, Philadelphia, PA.
17. Gisslen, M., L. Hagberg, L. Rosengren, B. J. Brew, P. Cinque, S. Spudich, and R. W. Price. 2007. Defining and evaluating HIV-related neurodegenerative disease and its treatment targets: a combinatorial approach to use of cerebrospinal fluid molecular biomarkers. J. Neuroimmune Pharmacol. 2:112-119.
18. Gonzalez-Scarano, F., and J. Martin-Garcia. 2005. The neuropathogenesis of AIDS. Nat. Rev. Immunol. 5:69-81.
19. Gorry, P. R., G. Bristol, J. A. Zack, K. Ritola, R. Swanstrom, C. J. Birch, J. E. Bell, N. Bannert, K. Crawford, H. Wang, D. Schols, E. De Clercq, K. Kunstman, S. M. Wolinsky, and D. Gabuzda. 2001. Macrophage tropism of human immunodeficiency virus type 1 isolates from brain and lymphoid tissues predicts neurotropism independent of coreceptor specificity. J. Virol. 75:10073-10089.
20. Gorry, P. R., J. Taylor, G. H. Holm, A. Mehle, T. Morgan, M. Cayabyab, M. Farzan, H. Wang, J. E. Bell, K. Kunstman, J. P. Moore, S. M. Wolinsky, and D. Gabuzda. 2002. Increased CCR5 affinity and reduced CCR5/CD4 dependence of a neurovirulent primary human immunodeficiency virus type 1 isolate. J. Virol. 76:6277-6292.
21. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
22. Guindon, S., F. Lethiec, P. Duroux, and O. Gascuel. 2005. PHYML Online - a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33:W557-W559.
23. Harrington, P. R., M. J. Connell, R. B. Meeker, P. R. Johnson, and R. Swanstrom. 2007. Dynamics of simian immunodeficiency virus populations in blood and cerebrospinal fluid over the full course of infection. J. Infect. Dis. 196:1058-1067.
24. Harrington, P. R., D. W. Haas, K. Ritola, and R. Swanstrom. 2005. Compartmentalized human immunodeficiency virus type 1 present in cerebrospinal fluid is produced by short-lived cells. J. Virol. 79:7959-7966.
25. Harrington, P. R., J. A. Nelson, K. M. Kitrinos, and R. Swanstrom. 2007. Independent evolution of human immunodeficiency virus type 1 env V1/V2 and V4/V5 hypervariable regions during chronic infection. J. Virol. 81:5413-5417.
26. Harrington, P. R., G. Schnell, S. L. Letendre, K. Ritola, K. Robertson, C. Hall, C. L. Burch, C. B. Jabara, D. T. Moore, R. J. Ellis, R. W. Price, and R. Swanstrom. 2009. Cross-sectional characterization of HIV-1 env compartmentalization in cerebrospinal fluid over the full disease course. AIDS 23:907-915.
27. Henderson, G. J., N. G. Hoffman, L. H. Ping, S. A. Fiscus, I. F. Hoffman, K. M. Kitrinos, T. Banda, F. E. Martinson, P. N. Kazembe, D. A. Chilongozi, M. S. Cohen, and R. Swanstrom. 2004. HIV-1 populations in blood and breast milk are similar. Virology 330:295-303.
28. Katoh, K., and H. Toh. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 9:286-298.
29. Keele, B. F., E. E. Giorgi, J. F. Salazar-Gonzalez, J. M. Decker, K. T. Pham, M. G. Salazar, C. Sun, T. Grayson, S. Wang, H. Li, X. Wei, C. Jiang, J. L. Kirchherr, F. Gao, J. A. Anderson, L. H. Ping, R. Swanstrom, G. D. Tomaras, W. A. Blattner, P. A. Goepfert, J. M. Kilby, M. S. Saag, E. L. Delwart, M. P. Busch, M. S. Cohen, D. C. Montefiori, B. F. Haynes, B. Gaschen, G. S. Athreya, H. Y. Lee, N. Wood, C. Seoighe, A. S. Perelson, T. Bhattacharya, B. T. Korber, B. H. Hahn, and G. M. Shaw. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 105:7552-7557.
30. Kelder, W., J. C. McArthur, T. Nance-Sproson, D. McClernon, and D. E. Griffin. 1998. Beta-chemokines MCP-1 and RANTES are selectively increased in cerebrospinal fluid of patients with human immunodeficiency virus-associated dementia. Ann. Neurol. 44:831-835.
31. Kitrinos, K. M., N. G. Hoffman, J. A. Nelson, and R. Swanstrom. 2003. Turnover of env variable region 1 and 2 genotypes in subjects with late-stage human immunodeficiency virus type 1 infection. J. Virol. 77:6811-6822.
32. Koenig, S., H. E. Gendelman, J. M. Orenstein, M. C. Dal Canto, G. H. Pezeshkpour, M. Yungbluth, F. Janotta, A. Aksamit, M. A. Martin, and A. S. Fauci. 1986. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233:1089-1093.
33. Lane, J. H., V. G. Sasseville, M. O. Smith, P. Vogel, D. R. Pauley, M. P. Heyes, and A. A. Lackner. 1996. Neuroinvasion by simian immunodeficiency virus coincides with increased numbers of perivascular macrophages/microglia and intrathecal immune activation. J. Neurovirol. 2:423-432.
34. Lindback, S., A. C. Karlsson, J. Mittler, A. Blaxhult, M. Carlsson, G. Briheim, A. Sonnerborg, and H. Gaines. 2000. Viral dynamics in primary HIV-1 infection. Karolinska Institutet Primary HIV Infection Study Group. AIDS 14:2283-2291.
35. Lindback, S., R. Thorstensson, A. C. Karlsson, M. von Sydow, L. Flamholc, A. Blaxhult, A. Sonnerborg, G. Biberfeld, and H. Gaines. 2000. Diagnosis of primary HIV-1 infection and duration of follow-up after HIV exposure. Karolinska Institute Primary HIV Infection Study Group. AIDS 14:2333-2339.
36. Little, S. J., S. D. Frost, J. K. Wong, D. M. Smith, S. L. Pond, C. C. Ignacio, N. T. Parkin, C. J. Petropoulos, and D. D. Richman. 2008. Persistence of transmitted drug resistance among subjects with primary human immunodeficiency virus infection. J. Virol. 82:5510-5518.
37. Liu, Y., X. P. Tang, J. C. McArthur, J. Scott, and S. Gartner. 2000. Analysis of human immunodeficiency virus type 1 gp160 sequences from a patient with HIV dementia: evidence for monocyte trafficking into brain. J. Neurovirol. 6(Suppl 1):S70-S81.
38. Marra, C. M., C. L. Maxwell, A. C. Collier, K. R. Robertson, and A. Imrie. 2007. Interpreting cerebrospinal fluid pleocytosis in HIV in the era of potent antiretroviral therapy. BMC Infect. Dis. 7:37.
39. Martin, C., J. Albert, P. Hansson, P. Pehrsson, H. Link, and A. Sonnerborg. 1998. Cerebrospinal fluid mononuclear cell counts influence CSF HIV-1 RNA levels. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 17:214-219.
40. Murphy, G., A. Charlett, L. F. Jordan, N. Osner, O. N. Gill, and J. V. Parry. 2004. HIV incidence appears constant in men who have sex with men despite widespread use of effective antiretroviral therapy. AIDS 18:265-272.
41. Nelson, J. A., S. A. Fiscus, and R. Swanstrom. 1997. Evolutionary variants of the human immunodeficiency virus type 1 V3 region characterized by using a heteroduplex tracking assay. J. Virol. 71:8750-8758.
42. Nottet, H. S., Y. Persidsky, V. G. Sasseville, A. N. Nukuna, P. Bock, Q. H. Zhai, L. R. Sharer, R. D. McComb, S. Swindells, C. Soderland, and H. E. Gendelman. 1996. Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. J. Immunol. 156:1284-1295.
43. Ohagen, A., A. Devitt, K. J. Kunstman, P. R. Gorry, P. P. Rose, B. Korber, J. Taylor, R. Levy, R. L. Murphy, S. M. Wolinsky, and D. Gabuzda. 2003. 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. 77:12336-12345.
44. Palmer, S., M. Kearney, F. Maldarelli, E. K. Halvas, C. J. Bixby, H. Bazmi, D. Rock, J. Falloon, R. T. Davey, Jr., R. L. Dewar, J. A. Metcalf, S. Hammer, J. W. Mellors, and J. M. Coffin. 2005. Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J. Clin. Microbiol. 43:406-413.
45. Peters, P. J., J. Bhattacharya, S. Hibbitts, M. T. Dittmar, G. Simmons, J. Bell, P. Simmonds, and P. R. Clapham. 2004. Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J. Virol. 78:6915-6926.
46. Pillai, S. K., S. L. Pond, Y. Liu, B. M. Good, M. C. Strain, R. J. Ellis, S. Letendre, D. M. Smith, H. F. Gunthard, I. Grant, T. D. Marcotte, J. A. McCutchan, D. D. Richman, and J. K. Wong. 2006. Genetic attributes of cerebrospinal fluid-derived HIV-1 env. Brain 129:1872-1883.
47. Pond, S. L., S. D. Frost, and S. V. Muse. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679.
48. Power, C., J. C. McArthur, R. T. Johnson, D. E. Griffin, J. D. Glass, S. Perryman, and B. Chesebro. 1994. Demented and nondemented patients with AIDS differ in brain-derived human immunodeficiency virus type 1 envelope sequences. J. Virol. 68:4643-4649.
49. Riddle, T. M., N. J. Shire, M. S. Sherman, K. F. Franco, H. W. Sheppard, and J. A. Nelson. 2006. Sequential turnover of human immunodeficiency virus type 1 env throughout the course of infection. J. Virol. 80:10591-10599.
50. Ritola, K., C. D. Pilcher, S. A. Fiscus, N. G. Hoffman, J. A. Nelson, K. M. Kitrinos, C. B. Hicks, J. J. Eron, Jr., and R. Swanstrom. 2004. Multiple V1/V2 env variants are frequently present during primary infection with human immunodeficiency virus type 1. J. Virol. 78:11208-11218.
51. Ritola, K., K. Robertson, S. A. Fiscus, C. Hall, and R. Swanstrom. 2005. Increased human immunodeficiency virus type 1 (HIV-1) env compartmentalization in the presence of HIV-1-associated dementia. J. Virol. 79:10830-10834.
52. Rossi, F., B. Querido, M. Nimmagadda, S. Cocklin, S. Navas-Martin, and J. Martin-Garcia. 2008. The V1-V3 region of a brain-derived HIV-1 envelope glycoprotein determines macrophage tropism, low CD4 dependence, increased fusogenicity and altered sensitivity to entry inhibitors. Retrovirology. 5:89.
53. Salazar-Gonzalez, J. F., E. Bailes, K. T. Pham, M. G. Salazar, M. B. Guffey, B. F. Keele, C. A. Derdeyn, P. Farmer, E. Hunter, S. Allen, O. Manigart, J. Mulenga, J. A. Anderson, R. Swanstrom, B. F. Haynes, G. S. Athreya, B. T. Korber, P. M. Sharp, G. M. Shaw, and B. H. Hahn. 2008. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J. Virol. 82:3952-3970.
54. Schnell, G., S. Spudich, P. Harrington, R. W. Price, and R. Swanstrom. 2009. Compartmentalized human immunodeficiency virus type 1 originates from long-lived cells in some subjects with HIV-1-associated dementia. PLoS Pathog. 5:e1000395.
55. Sevigny, J. J., S. M. Albert, M. P. McDermott, J. C. McArthur, N. Sacktor, K. Conant, G. Schifitto, O. A. Selnes, Y. Stern, D. R. McClernon, D. Palumbo, K. Kieburtz, G. Riggs, B. Cohen, L. G. Epstein, and K. Marder. 2004. Evaluation of HIV RNA and markers of immune activation as predictors of HIV-associated dementia. Neurology 63:2084-2090.
56. Simmonds, P., P. Balfe, C. A. Ludlam, J. O. Bishop, and A. J. Brown. 1990. Analysis of sequence diversity in hypervariable regions of the external glycoprotein of human immunodeficiency virus type 1. J. Virol. 64:5840-5850.
57. Slatkin, M., and W. P. Maddison. 1989. A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics 123:603-613.
58. Spudich, S. S., A. C. Nilsson, N. D. Lollo, T. J. Liegler, C. J. Petropoulos, S. G. Deeks, E. E. Paxinos, and R. W. Price. 2005. Cerebrospinal fluid HIV infection and pleocytosis: relation to systemic infection and antiretroviral treatment. BMC Infect. Dis. 5:98.
59. Strain, M. C., S. Letendre, S. K. Pillai, T. Russell, C. C. Ignacio, H. F. Gunthard, B. Good, D. M. Smith, S. M. Wolinsky, M. Furtado, J. Marquie-Beck, J. Durelle, I. Grant, D. D. Richman, T. Marcotte, J. A. McCutchan, R. J. Ellis, and J. K. Wong. 2005. Genetic composition of human immunodeficiency virus type 1 in cerebrospinal fluid and blood without treatment and during failing antiretroviral therapy. J. Virol. 79:1772-1788.
60. Takahashi, K., S. L. Wesselingh, D. E. Griffin, J. C. McArthur, R. T. Johnson, and J. D. Glass. 1996. Localization of HIV-1 in human brain using polymerase chain reaction/in situ hybridization and immunocytochemistry. Ann. Neurol. 39:705-711.
61. Thomas, E. R., R. L. Dunfee, J. Stanton, D. Bogdan, J. Taylor, K. Kunstman, J. E. Bell, S. M. Wolinsky, and D. Gabuzda. 2007. Macrophage entry mediated by HIV Envs from brain and lymphoid tissues is determined by the capacity to use low CD4 levels and overall efficiency of fusion. Virology 360:105-119.
62. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
63. Wiley, C. A., R. D. Schrier, J. A. Nelson, P. W. Lampert, and M. B. Oldstone. 1986. Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc. Natl. Acad. Sci. U. S. A. 83:7089-7093.
64. Zetola, N. M., and C. D. Pilcher. 2007. Diagnosis and management of acute HIV infection. Infect. Dis. Clin. North Am. 21:19-48, vii.