Microarray analysis of HIV resistant female sex workers reveal a gene expression signature pattern reminiscent of a lowered immune activation state

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Songok, Elijah M ^a,b   Luo, Ma ^b,d   Liang, Ben ^d   Mclaren, Paul ^b   Kaefer, Nadine ^b   Apidi, Winnie ^b   Boucher, Genevieve ^c   Kimani, Joshua ^b,e   Wachihi, Charles ^e   Sekaly, Rafick ^c   Fowke, Keith ^b   Ball, Blake T ^b,d   Plummer, Francis A ^b,d  

^a KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^b UNIVERSITY OF MANITOBA   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^e UNIVERSITY OF NAIROBI   (Kenya)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; PENTOSE PHOSPHATE; PHOSPHATIDYLINOSITOL; RIBOSOME PROTEIN; RNA; T LYMPHOCYTE RECEPTOR;

ADULT; ARTICLE; BLOOD SAMPLING; CLUSTER ANALYSIS; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC DATABASE; GLUCONEOGENESIS; GLYCOLYSIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION RESISTANCE; MICROARRAY ANALYSIS; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PROSTITUTION; PROTEIN SYNTHESIS; RNA EXTRACTION; RNA HYBRIDIZATION; SERODIAGNOSIS; SIGNAL TRANSDUCTION; TIGHT JUNCTION; UPREGULATION; COHORT ANALYSIS; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; INNATE IMMUNITY; KENYA; LYMPHOCYTE ACTIVATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VALIDATION STUDY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CLUSTER ANALYSIS; COHORT STUDIES; DOWN-REGULATION; FEMALE; GENE EXPRESSION PROFILING; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, INNATE; KENYA; LYMPHOCYTE ACTIVATION; MICROARRAY ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEX WORKERS; VALIDATION STUDIES AS TOPIC;

EID: 84856255109     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030048     Document Type: Article

References (73)

1. Joint United Nations Programme on HIV/AIDS, UNAIDS (2008) Report on the Global AIDS Epidemic. http://www.unaids.org.
2. Kallings LO, (2008) The first postmordern epidemic: 25 years of HIV/AIDS. J internal Med 263: 218-243.
3. Stover J, Fidzani B, Molomo BC, Moeti T, Musuka G, (2008) Estimated HIV trends and program effects in Botswana. PLos ONE 3: e3729.
4. Wainberg M, Kuan-TeJeang, (2008) 25 years of HIV research-progress and perspectives. BMC Medicine 6: 31.
5. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, et al. (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361: 2209-20.
6. Saez-Cirion A, Versmisse P, Truong LX, Chakrabarti L, Carpentier W, et al. (2006) Persistent resistance to HIV-1 infection in CD4 T cells from exposed uninfected Vietnamese individuals is mediated by entry and post entry blocks. Retrovirology 3: 81.
7. Rowland- Jones SL, Nixon DF, Aldhous MC, Gotch F, Ariyoshi K, et al. (1993) HIV specific cytotoxic T-cell activity in a HIV-exposed but uninfected infant. Lancet 341: 860-861.
8. Clerici M, Sison AV, Berzofsky JA, Rakusan TA, Brandt CD, et al. (1993) Cellular immune factors associated with mother-to-infant tansmission of HIV. AIDS 7: 1427-1433.
9. Begaud E, Chartier L, Marechal V, Ipero J, Leal J, et al. (2006) Reduced CD4 T- cell activation and in vitro susceptibility to HIV-1 infection in exposed uninfected Central Africans. Retrovirology 3: 35.
10. Kelker HC, Seidlin M, Vogler M, Valentine FT, (1992) Lymphocytes from some long term seronegative heterosexual partners of HIV infected individuals proliferate in response to HIV antigens. AIDS Res Hum Retroviruses 8: 1355-9.
11. Fowke KR, Nagelkerke NJ, Kimani J, Simonsen N, Anzala AO, et al. (1996) Resistance to HIV-1 infection among persistently seronegative prostitutes in Nairobi, Kenya. Lancet 348: 1347-1351.
12. Rowland-Jones SJ, Sutton J, Ariyoshi K, Dong T, Gotch F, et al. (1995) HIV specific cytotoxic T-cells in HIV exposed but uninfected Gambian Women. Nat Med 1: 59-64.
13. Beyrer C, Artenstein AW, Rugpao S, Stephens H, VanCott TC, et al. (1999) Epidemiologic and biologic characterization of a cohort of human immunodeficiency virus type 1 highly exposed persistently seronegative female sex workers in Northen Thailand. J Infect Dis 179: 59-67.
14. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, et al. (1996) Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply exposed individuals in HIV-1 infection. Cell 86: 367-377.
15. Lama J, Planelles V, (2007) Host factors influencing susceptibility to HIV infection and AIDS Progression. Retrovirology 4: 52.
16. MacDonald KS, Fowke KR, Kimani J, Dunand VA, Nalgerke NJ, et al. (2000) Influence of HLA supertypes on susceptibility and resistance to human immunodeficiency virus type 1 infection. J Inf Dis 181: 1581-1589.
17. Carthagena L, Parise MC, Ringeard M, Chelbi-Alix MK, Hazan U, et al. (2008) Implications of TRIM alpha and TRIMCyp in interferon induced antiretroviral restriction activities. Retrovirology 5: 59.
18. Boyton RJ, Altmann DM, (2007) Natural Killer cells, killer immunoglobulin-like receptors and human leucocyte antigen Class I in disease. Clin Exp Immunol 149: 1-8.
19. Valcke HS, Bernard NF, Bruneau J, Alary M, Tsoukas CM, et al. (2006) APOBEC3G genetic variants and their association with risk of HIV infection in highly exposed Caucasians. AIDS 20: 1984-1986.
20. Plummer FA, Ball TB, Kimani J, Fowke KR, (1999) Resistance to HIV-1 Infection among highly exposed sex workers in Nairobi: what mediates protection and why does it develop? Immunol Lett 66: 27-34.
21. Ball TB, Hezhao J, Kimani J, Mclaren P, Marlin C, et al. (2007) Polymorphisms in IRF-1 associated with resistance to HIV-1 infection in highly exposed uninfected Kenyan sex workers. AIDS 21: 1091-1101.
22. Kaul R, Plummer F, Clerici M, Bomsel M, Lopalco L, et al. (2001) Mucosal IgA in exposed uninfected subjects: evidence for a role in protection against HIV infection. AIDS 2001 15: 431-2.
23. Burgener A, Boutilier J, Wachihi C, Kimani J, Carpenter M, et al. (2008) Identification of differentially expressed proteins in the cervical mucosa of HIV-1 resistant sex workers. Proteome Res 10: 4446-54.
24. Rits AM, Van Dort KA, Kootsra NA, (2008) Polymorphisms in the regulatory region of the cyclophilin A gene influence the susceptibility for HIV-1 Infection. PLOS One 3: e3975.
25. Havre PA, Abe M, Urasaki Y, Ohnuma K, Morimoto C, et al. (2008) The role of CD26/dipeptidyl peptidase IV in cancer. Frontiers in Bioscience 13: 1634-45.
26. Boonacker E, Van Noordern CJ, (2003) The multifunctional or moonlighting protein CD26/DPPIV. European Journal of Cell Biology 82: 53-73.
27. Hildebrandt M, Rose M, Ruter J, Salama A, Monnikes A, et al. (2001) Dipetidylpeptidase IV activity in patients in patients with inflammatory bowel bowel disease. Scand J Gastroenterology 36: 1067-1072.
28. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, et al. (1996) Identification of a major co-receptor for primary isolates of HIV-1. Nature 381: 661-6.
29. Proost P, Meester I, Schols D, Struyf S, Lambeir A, et al. (1998) Amino-terminal truncation of chemokines by CD26/dipeptidyl-peptidase IV- conversion of RANTES into a potent inhibitor of monocyte chemotaxis and HIV infection. J Biol Chem 273: 7222-7.
30. Morimoto C, Lord CI, Zhang C, Duke-Chohan J, Letvin N, et al. (1994) Role of CD26/dipeptidyl peptidase IV in human immunodeficiency virus type 1 infection and apotosis. Proc Natl Acad Sci USA 91: 9960-4.
31. Blazquez M, Madueno J, Gonzalez R, Jurado R, Bachovchin W, et al. (1992) Selective decrease of CD26 expression in T-cells from HIV infected individuals. J Immunol 149: 3073-7.
32. Vanham G, Kestens L, Van Hoof J, Peene C, Colebunders R, et al. (1993) Decreased expression of memory marker CD26 on both CD4+ and CD8+ T lymphocytes of HIV infected subjects. J Acquired Immune Defic Syndr 6: 749-57.
33. Mentlein R, Gallwitz B, Schmidt W, (1993) Dipeptidyl peptidase IV hydrolyses gastric inhibitory polypeptide, glucagon like peptide 1 (7-36) amide peptide histidine methionine and is responsible for their degradation in human serum. Eur J Biochem 214: 829-835.
34. Drucker D, Shi Q, Crivici A, Sumner-Smith M, Tavares W, et al. (1997) Regulation of the biological activity of glucagons-like peptide 2 in vivo by dipeptidyl peptidase IV. Nat Biotechnology 15: 673-677.
35. Pratley RE, Salsali A, (2007) Inhibition of DPP-4: A new therapeutic approach for treatment of type 2 diabetes. Curr Med Res Opin 4: 919-31.
36. Songok EM, Osero B, Mackinnon L, Rono MK, Apidi W, et al. (2010) CD26/DPPIV is highly expressed in peripheral blood of HIV resistant female commercial sex workers. Virol J 7: 343.
37. Isotani S, Hara K, Takunaga C, Inoue H, Avruch J, et al. (1999) Immunopurified mammalian target of rapamycin phophorylates and activates p70 S6 kinase alpha in vitro. J Biol Chem 274: 34493-8.
38. Uenio M, Carvalheira JB, Tambascia RC, Bezerra RM, Amaral ME, et al. (2005) Regulation of insulin signalling by hyperinsulinemia: role of IRS-1/2 serine phosphorylation and the Mtor/p70 S6K pathway. Diabetologia 48: 506-18.
39. Francois F, Klotman ME, (2003) Phosphatidylinositol 3-Kinase regulates human immunodeficiency virus type 1 replication following viral entry in primary CD4+ T-lymphocytes and macrophages. J Virol 77: 2539-2549.
40. Brown BK, Karasavvas N, Beck Z, Matyas GR, Birx DL, et al. (2007) Monoclonal antibodies to phoshatidylinositol phosphate neutralize human immunodeficiency virus type 1: Role of phosphate-binding subsites. Virol 81: 2087-2091.
41. Chugh P, Bradel-Tretheway B, Monteiro-Filho CMR, Planelles V, Maggirwar SB, et al. (2008) AKt inhibitors as an HIV-1 infected macrophage-specific antiviral therapy. Retrovirology 5: 11.
42. Mclaren PJ, Ball TB, Wachihi C, Jaoko W, Kelvin DJ, et al. (2010) HIV-exposed seronegative commercial sex workers show a quiescent phenotype in the CD4+ T cell compartment and reduced expression of HIV-dependent host factors. J Infect Dis Suppl 3: S339-44.
43. Bentwich Z, Kalinkovich A, Weisman Z, (1995) Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunology Today 16: 187-191.
44. Koblavi-Deme S, Maran M, Kabran N, Borget MY, Kalou M, et al. (2003) Changes in levels of immune activation and reconstitution markers among HIV-1 infected Africans receiving antiretroviral therapy. AIDS 17: (suppl 3): S17-22.
45. Begaud E, Chartier L, Marechal V, Ipero J, Leal J, et al. (2006) Reduced CD4 T- cell activation and in vitro susceptibility to HIV-1 infection in exposed uninfected Central Africans. Retrovirology 3: 35.
46. Jennes W, Evertse D, Borget MY, Vuylsteke B, Maurice C, et al. (2006) Supressed cellular alloimune responses in HIV exposed seronegative female sex workers. Clin Exp Immunol 143: 435-444.
47. Biasin M, Caputo SL, Speciale L, Colombo F, Racioppi L, et al. (2000) Mucosal and systemic immune activation is present in human immunodeficiency virus exponed seronegative women. J infect Dis 182: 1365-1374.
48. Tran HK, Chartier L, Troung LX, Nguyen NN, Fontanet A, et al. (2006) Systemic immune activation in HIV-1 exposed uninfected Vietnamese intravascular drug users. AIDS Res Human Retroviruses 22: 255-261.
49. Suy A, Castro P, Nomdedeu M, Garcia F, Lopez A, et al. (2007) Immunological profile of heterosexual highly HIV exposed uinfected individuals: predominant role of CD4 and CD8 T-cell activation. J Infect Dis 196: 1191-1201.
50. Roos D, Loos JA, (1973) Changes in carbohydrate metabolism of mitogenically stimulated human peripheral lymphocytes II. Relative importance of glycolysis and oxidative phosphorylation on phytohaemagglutinin stimulation. Exp Cell Res 77: 127-135.
51. Jones GR, Thomson BC, (2007) Revving the engine: Signal transduction fuels T-cell activation. Immunity 27: 173-178.
52. Krauss S, Brand MD, Buttgereit F, (2001) Signalling takes a breath-new quantitative perspectives on bioenergetics and signal transduction. Immunity 15: 497-502.
53. Kawata H, Yamada K, Shou Z, Mizutani T, Yazawa T, et al. (2003): Zinc finger and homeoboxes (ZXH)2, a novel member of the ZHX family function as a transcriptional repressor. Biochem J 373: 747-757.
54. Xie Z, Zhang H, Tsai W, Zhang Y, Du Y, et al. (2008) Zinc finger protein ZBTB20 is a key repressor of alfa-fetoprotein gene transcription in liver. Proc Natl Acad Sci USA 105: 10859-10864.
55. Modiano JF, Johnson L, Bellgrau D, (2008) Negative regulators in homeostasis of naïve peripheral T-cells. Immunol Res 41: 137-153.
56. Wutz A, Gribnau J, (2007) X inactivation Xplained. Current Opin Genet Dev 5: 387-93.
57. Arthos J, Cicala C, Martinelli E, Macleod K, Van Ryk D, et al. (2008) HIV-1 envelope protein binds to and signals through integrin alpha4beta7, the gut mucosal homing receptor for peripheral T cells. Nat Immunol 9: 301-9.
58. Schweneker M, Bachmann AS, Moelling K, (2004) The HIV-1 co-receptor CCR5 binds to alpha-catenin, a component of the cellular cytoskeleton. Biochem Biophys Commun 325: 751-7.
59. Alcami J, Lera DL, Folgueira L, Pedrazza MA, Jacque JM, et al. (1995) Absolute dependence on Kappa B responsive elements for initition and tat mediated amplification of HIV transcription in blood CD4 T-lymphocytes. EMBO 14: 1552-1560.
60. Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A, et al. (2008) Identification of host proteins required for HIV infection through a functional genomic screen. Science 319: 921-6.
61. Dudoit S, Gentleman RC, Ouackenbush J, (2003) Open source software for analysis of microarray data. Biotechniques pp. Suppl 45-51.
62. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protoc 4: 44-57.
63. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation Visualization, and Intergrated Discovery. Genome Biol 4: P3.
64. Lester RT, Yao XD, Ball TB, Mckinnon LR, Kaul R, et al. (2008) Toll-like receptor expression and responsiveness are increased in viraemic HIV-1 infection. AIDS 22: 685-94.
65. Gonzalez E, Kulkarni H, Bolivar H, Mangano A, Sanchez R, et al. (2005) The influence of CCL3L1 gene containing segmental duplications on HIV/AIDS suscpetibility. Science 174: 5655-64.
66. de witte L, Nabatov A, Pion M, Fluitsman D, de Jong MA, et al. (2007) Langerin is a natural barrier to HIV-1 transmission by Langerhan cells. Nat Med 13: 367-371.
67. Martin MP, Lederman MM, Hutchenson HB, Goedert JJ, Nelson GW, et al. (2004) Association of DC-SIGN promoter polymorphism with increased risk for parenteral, but not mucosal, acquisition of human immunodeficiency virus type 1 infection. J Virol 78: 14053-14056.
68. An P, Duggal P, Wang LH, OBrien SJ, Donfield S, et al. (2007) Polymorphism of CUL5 are associated with CD4+ T cell loss in HIV-1 infected individuals. PLoS Genet 3: e19.
69. Winkler C, Modi W, Smith MW, Nelson GW, Wu X, et al. (1998) Genetic restriction of AIDS pathogenesis by a SDF-1 chemokine variant. Science 279: 389-393.
70. Schuitmemaker H, (1994) IL4 and IL10 as potent inhibitors of HIV1 replication in macrophages in vitro: a role for cytokines in the in vivo virus host range? Res Immunol 145: 588-92.
71. Chang TL, Vargas J Jnr, DelPortillo A, Klotman ME, (2005) Dual Role of alpha-defensins-I in anti-HIV innate immunity. J Clin Invest 115: 765-773.
72. Jennes W, Verhevden S, Demanet C, Adie-Toure CA, Vuylsteke B, et al. (2006) Cutting edge: Resistance to HIV-1 infection among African female sex workers is associated with inhibitory KIR in absence of their HLA ligands. J Immunol 177: 6588-92.
73. Finberg RW, Wang JP, Kurt-Jones EA, (2007) Toll-like receptors and viruses. Rev Med Virol 17: 35-43.