Elevated natural killer cell activity despite altered functional and phenotypic profile in Ugandans with HIV-1 clade A or clade D infection

Journal of Acquired Immune Deficiency Syndromes

Volumn 51, Issue 4, 2009, Pages 380-389

  Eller, Michael A ^a,b,c   Eller, Leigh Anne ^b,c   Ouma, Benson J ^b   Thelian, Doris ^c   Gonzalez, Veronica D ^a   Guwatudde, David ^b,d   McCutchan, Francine E ^c   Marovich, Mary A ^c   Michael, Nelson L ^c   De Souza, Mark S ^e   Wabwire Mangen, Fred ^b,d   Robb, Merlin L ^c   Currier, Jeffrey R ^c   Sandberg, Johan K ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b Makerere University   (Uganda)

^c US Military HIV Research Program   (United States)

^d MAKERERE UNIVERSITY   (Uganda)

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

Author keywords

CD4; HIV 1; NK cells; Viral infections

Indexed keywords

CD161 ANTIGEN; CD56 ANTIGEN; GAMMA INTERFERON; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2A; PROTEIN NKP30; PROTEIN NKP44; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CD4 LYMPHOCYTE COUNT; CELL FUNCTION; CELLULAR IMMUNITY; CLADISTICS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGRANULATION; DISEASE COURSE; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INNATE IMMUNITY; MAJOR CLINICAL STUDY; MALE; NATURAL KILLER CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UGANDA; VIRUS LOAD;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ADULT; ANTIGENS, CD56; CD4 LYMPHOCYTE COUNT; FEMALE; HIV-1; HUMANS; IMMUNOPHENOTYPING; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MALE; MIDDLE AGED; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; RECEPTORS, KIR2DL1; UGANDA;

EID: 68049121908     PISSN: 15254135     EISSN: None     Source Type: Journal    
DOI: 10.1097/QAI.0b013e3181aa256e     Document Type: Article

References (47)

1. Caligiuri MA. Human natural killer cells. Blood. 2008;112:461-469.
2. Vivier E, Tomasello E, Baratin M, et al. Functions of natural killer cells. Nat Immunol. 2008;9:503-510.
3. Alter G, Altfeld M. NK cell function in HIV-1 infection. Curr Mol Med. 2006;6:621-629.
4. Biassoni R, Cantoni C, Pende D, et al. Human natural killer cell receptors and co-receptors. Immunol Rev. 2001;181:203-214. (Pubitemid 32703408)
5. Fauci AS, Mavilio D, Kottilil S. NK cells in HIV infection: paradigm for protection or targets for ambush. Nat Rev Immunol. 2005;5:835-843. (Pubitemid 41581665)
6. Kärre K. Natural killer cell recognition of missing self. Nat Immunol. 2008;9:477-480. (Pubitemid 351560515)
7. Cooper MA, Fehniger TA, Turner SC, et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood. 2001;97:3146-3151.
8. Alter G, Teigen N, Ahern R, et al. Evolution of innate and adaptive effector cell functions during acute HIV-1 infection. J Infect Dis. 2007;195:1452-1460. (Pubitemid 46717463)
9. Hu PF, Hultin LE, Hultin P, et al. Natural killer cell immunodeficiency in HIV disease is manifest by profoundly decreased numbers of CD16+CD56+ cells and expansion of a population of CD16dimCD56-cells with low lytic activity. J Acquir Immune Defic Syndr Hum Retrovirol. 1995;10:331-340.
10. Azzoni L, Papasavvas E, Chehimi J, et al. Sustained impairment of IFN-gamma secretion in suppressed HIV-infected patients despite mature NK cell recovery: evidence for a defective reconstitution of innate immunity. J Immunol. 2002;168:5764-5770. (Pubitemid 34556161)
11. De Maria A, Fogli M, Costa P, et al. The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur J Immunol. 2003;33:2410-2418. (Pubitemid 37138973)
12. Alter G, Teigen N, Davis BT, et al. Sequential deregulation of NK cell subset distribution and function starting in acute HIV-1 infection. Blood. 2005;106:3366-3369. (Pubitemid 41609166)
13. Gonzalez VD, Falconer K, Michaëlsson J, et al. Expansion of CD56- NK cells in chronic HCV/HIV-1 co-infection: reversion by antiviral treatment with pegylated IFNalpha and ribavirin. Clin Immunol. 2008;128:46-56.
14. Mavilio D, Lombardo G, Benjamin J, et al. Characterization of CD56-/CD16+ natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc Natl Acad Sci U S A. 2005;102:2886-2891. (Pubitemid 40299886)
15. Mela CM, Burton CT, Imami N, et al. Switch from inhibitory to activating NKG2 receptor expression in HIV-1 infection: lack of reversion with highly active antiretroviral therapy. AIDS. 2005;19:1761-1769. (Pubitemid 41546594)
16. Bandyopadhyay S, Ziegner U, Campbell DE, et al. Natural killer cell-mediated lysis of T cell lines chronically infected with HIV-1. Clin Exp Immunol. 1990;79:430-435. (Pubitemid 20082272)
17. Bonaparte MI, Barker E. Killing of human immunodeficiency virus-infected primary T-cell blasts by autologous natural killer cells is dependent on the ability of the virus to alter the expression of major histocompatibility complex class I molecules. Blood. 2004;104:2087-2094. (Pubitemid 39297862)
18. Fehniger TA, Herbein G, Yu H, et al. Natural killer cells from HIV-1+ patients produce C-C chemokines and inhibit HIV-1 infection. J Immunol. 1998;161:6433-6438. (Pubitemid 28536022)
19. Oliva A, Kinter AL, Vaccarezza M, et al. Natural killer cells from human immunodeficiency virus (HIV)-infected individuals are an important source of CC-chemokines and suppress HIV-1 entry and replication in vitro. J Clin Invest. 1998;102:223-231. (Pubitemid 28323849)
20. Kottilil S, Chun TW, Moir S, et al. Innate immunity in human immunodeficiency virus infection: effect of viremia on natural killer cell function. J Infect Dis. 2003;187:1038-1045. (Pubitemid 36399345)
21. Martin MP, Gao X, Lee JH, et al. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet. 2002;31:429-434. (Pubitemid 35154456)
22. Long BR, Ndhlovu LC, Oksenberg JR, et al. Conferral of enhanced natural killer cell function by KIR3DS1 in early human immunodeficiency virus type 1 infection. J Virol. 2008;82:4785-4792.
23. Alter G, Martin MP, Teigen N, et al. Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exp Med. 2007;204:3027-3036. (Pubitemid 350179568)
24. BallanWM, Vu BN, Long BR, et al. Natural killer cells in perinatally HIV-1-infected children exhibit less degranulation compared to HIV-1-exposed uninfected children and their expression of KIR2DL3, NKG2C, and NKp46 correlates with disease severity. J Immunol. 2007;179:3362-3370.
25. JennesW, Verheyden S, Demanet C, et al. Cutting edge: resistance to HIV-1 infection among African female sex workers is associated with inhibitory KIR in the absence of their HLA ligands. J Immunol. 2006;177:6588-6592. (Pubitemid 44715020)
26. Wakabi W. New strategies sought in Uganda as HIV infections rise. Lancet Infect Dis. 2008;8:285.
27. HladikW, Musinguzi J, KirungiW, et al. The estimated burden of HIV/AIDS in Uganda, 2005-2010. AIDS. 2008;22:503-510.
28. Harris M, Serwada D, Sewankambo NK, et al. Among 46 near full-length HIV type 1 genome sequences from Rakai District, Uganda, subtype D and AD recombinants predominate. AIDS Res Hum Retroviruses. 2002;18:1281-1290. (Pubitemid 36042988)
29. Peeters M, Toure-Kane C, Nkengasong JN. Genetic diversity of HIV in Africa: impact on diagnosis, treatment, vaccine development and trials. AIDS. 2003;17:2547-2560. (Pubitemid 38402333)
30. Kiwanuka N, Laeyendecker O, Robb M, et al. Effect of human immunodeficiency virus type 1 (HIV-1) subtype on disease progression in persons from Rakai, Uganda, with incident HIV-1 infection. J Infect Dis. 2008;197:707-713.
31. Baker CA, McEvers K, Byaruhanga R, et al. HIV subtypes induce distinct profiles of HIV-specific CD8(+) T cell responses. AIDS Res Hum Retroviruses. 2008;24:283-287. (Pubitemid 351282106)
32. Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods. 2004;294:15-22. (Pubitemid 39626587)
33. Gonzalez VD, Bjorkström NK, Malmberg KJ, et al. Application of nine-color flow cytometry for detailed studies of the phenotypic complexity and functional heterogeneity of human lymphocyte subsets. J Immunol Methods. 2008;330:64-74.
34. Eller LA, Eller MA, Ouma BJ, et al. Large-scale human immunodefi- ciency virus rapid test evaluation in a low-prevalence Ugandan blood bank population. J Clin Microbiol. 2007;45:3281-3285.
35. Laeyendecker O, Henson C, Gray RH, et al. Performance of a commercial, type-specific enzyme-linked immunosorbent assay for detection of herpes simplex virus type 2-specific antibodies in Ugandans. J Clin Microbiol. 2004;42:1794-1796. (Pubitemid 38500844)
36. Arroyo MA, Sateren WB, Serwadda D, et al. Higher HIV-1 incidence and genetic complexity along main roads in Rakai District, Uganda. J Acquir Immune Defic Syndr. 2006;43:440-445. (Pubitemid 44737102)
37. Hoelscher M, Dowling WE, Sanders-Buell E, et al. Detection of HIV-1 subtypes, recombinants, and dual infections in East Africa by a multi-region hybridization assay. AIDS. 2002;16:2055-2064. (Pubitemid 35205270)
38. Mavilio D, Benjamin J, Daucher M, et al. Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc Natl Acad Sci U S A. 2003;100:15011- 15016. (Pubitemid 37518008)
39. Bryceson YT, Long EO. Line of attack: NK cell specificity and integration of signals. Curr Opin Immunol. 2008;20:344-352.
40. Fogli M, Costa P, Murdaca G, et al. Significant NK cell activation associated with decreased cytolytic function in peripheral blood of HIV-1-infected patients. Eur J Immunol. 2004;34:2313-2321. (Pubitemid 39256113)
41. Vieillard V, Habib RE, Brochard P, et al. CCR5 or CXCR4 use influences the relationship between CD4 cell depletion, NKp44L expression and NK cytotoxicity in SHIV-infected macaques. AIDS. 2008;22:185-192.
42. Vieillard V, Strominger JL, Debré P. NK cytotoxicity against CD4+ T cells during HIV-1 infection: a gp41 peptide induces the expression of an NKp44 ligand. Proc Natl Acad Sci U S A. 2005;102:10981-10986. (Pubitemid 41105979)
43. Vieillard V, Costagliola D, Simon A, et al; Group FAàLTAS. Specific adaptive humoral response against a gp41 motif inhibits CD4 T-cell sensitivity to NK lysis during HIV-1 infection. AIDS. 2006;20:1795-1804.
44. Fu GF, Hao S, Zhao JL, et al. Changes in NK cell counts and receptor expressions and emergence of CD3(dim)/CD56+ cells in HIV-1 infected patients in China. Viral Immunol. 2009;22:105-116.
45. Strowig T, Brilot F, Münz C. Noncytotoxic functions of NK cells: direct pathogen restriction and assistance to adaptive immunity. J Immunol. 2008;180:7785-7791.
46. Hunt PW, Brenchley J, Sinclair E, et al. Relationship between T cell activation and CD4+ T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis. 2008;197:126-133. (Pubitemid 351263476)
47. Jiang W, Lederman MM, Hunt P, et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis. 2009;199:1177-1185.