MHC class I chain-related protein A shedding in chronic HIV-1 infection is associated with profound NK cell dysfunction

Virology

Volumn 406, Issue 1, 2010, Pages 12-20

  Nolting, Anne ^a,b,c   Dugast, Anne Sophie ^a,b   Rihn, Suzannah ^a,b   Luteijn, Rutger ^a,b   Carrington, Mary F ^a,b   Kane, Katherine ^a,b   Jost, Stephanie ^a,b   Toth, Ildiko ^a,b   Nagami, Ellen ^a,b   Faetkenheuer, Gerd ^c   Hartmann, Pia ^c   Altfeld, Marcus ^a,b   Alter, Galit ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

Escape; HIV; Innate immunity; NK cells

Indexed keywords

ANTIRETROVIRUS AGENT; BINDING PROTEIN; CD4 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1 CHAIN RELATED PROTEIN A; NATURAL KILLER CELL RECEPTOR NKG2D; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; KLRK1 PROTEIN, HUMAN; LIGAND; MATRIX METALLOPROTEINASE; MHC CLASS I-RELATED CHAIN A; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; PRIMER DNA;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; MAJOR CLINICAL STUDY; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; BLOOD; CASE CONTROL STUDY; CELL LINE; DOWN REGULATION; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; K562 CELL LINE; METABOLISM; NUCLEOTIDE SEQUENCE; SOLUBILITY; UPREGULATION; VIROLOGY;

BASE SEQUENCE; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; DNA PRIMERS; DOWN-REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV INFECTIONS; HIV-1; HUMANS; IMMUNE TOLERANCE; K562 CELLS; KILLER CELLS, NATURAL; LIGANDS; MATRIX METALLOPROTEINASES; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; SOLUBILITY; TRANSCRIPTION, GENETIC; UP-REGULATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77956174618     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.05.014     Document Type: Article

References (46)

1. Alter G., Teigen N., Davis B.T., Addo M.M., Suscovich T.J., Waring M.T., Streeck H., Johnston M.N., Staller K.D., Zaman M.T., Yu X.G., Lichterfeld M., Basgoz N., Rosenberg E.S., Altfeld M. Sequential deregulation of NK cell subset distribution and function starting in acute HIV-1 infection. Blood 2005.
2. Arase H., Mocarski E.S., Campbell A.E., Hill A.B., Lanier L.L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 2002, 296(5571):1323-1326.
3. Bauer S., Groh V., Wu J., Steinle A., Phillips J.H., Lanier L.L., Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999, 285(5428):727-729.
4. Biron C.A., Byron K.S., Sullivan J.L. Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J. Med. 1989, 320(26):1731-1735.
5. Brown P.D. Ongoing trials with matrix metalloproteinase inhibitors. Expert Opin. Investig. Drugs 2000, 9(9):2167-2177.
6. Cao W., Xi X., Wang Z., Dong L., Hao Z., Cui L., Ma C., He W. Four novel ULBP splice variants are ligands for human NKG2D. Int. Immunol. 2008, 20(8):981-991.
7. Cerboni C., Neri F., Casartelli N., Zingoni A., Cosman D., Rossi P., Santoni A., Doria M. Human immunodeficiency virus 1 Nef protein downmodulates the ligands of the activating receptor NKG2D and inhibits natural killer cell-mediated cytotoxicity. J. Gen. Virol. 2007, 88(Pt 1):242-250.
8. Dezube B.J., Sullivan R., Koon H.B. Emerging targets and novel strategies in the treatment of AIDS-related Kaposi's sarcoma: bidirectional translational science. J. Cell. Physiol. 2006, 209(3):659-662.
9. Diefenbach A., Jensen E.R., Jamieson A.M., Raulet D.H. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001, 413(6852):165-171.
10. Etzioni A., Eidenschenk C., Katz R., Beck R., Casanova J.L., Pollack S. Fatal varicella associated with selective natural killer cell deficiency. J. Pediatr. 2005, 146(3):423-425.
11. Fang M., Lanier L.L., Sigal L.J. A role for NKG2D in NK cell-mediated resistance to poxvirus disease. PLoS Pathog. 2008, 4(2):e30.
12. Fdez-Morera J.L., Tunon A., Rodriguez-Rodero S., Rodrigo L., Martinez-Borra J., Gonzalez S., Lopez-Vazquez A., Lahoz C.H., Lopez-Larrea C. Clinical behavior of multiple sclerosis is modulated by the MHC class I-chain-related gene A. Tissue Antigens 2006, 67(5):409-414.
13. Gambelunghe G., Brozzetti A., Ghaderi M., Candeloro P., Tortoioli C., Falorni A. MICA gene polymorphism in the pathogenesis of type 1 diabetes. Ann. N. Y. Acad. Sci. 2007, 1110:92-98.
14. Groh V., Bahram S., Bauer S., Herman A., Beauchamp M., Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc. Natl. Acad. Sci. U. S. A. 1996, 93(22):12445-12450.
15. Groh V., Rhinehart R., Randolph-Habecker J., Topp M.S., Riddell S.R., Spies T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2001, 2(3):255-260.
16. Groh V., Wu J., Yee C., Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002, 419(6908):734-738.
17. Hijova E. Matrix metalloproteinases: their biological functions and clinical implications. Bratisl. Lek. Listy 2005, 106(3):127-132.
18. Huard B., Karlsson L. KIR expression on self-reactive CD8+ T cells is controlled by T-cell receptor engagement. Nature 2000, 403(6767):325-328.
19. Jinushi M., Vanneman M., Munshi N.C., Tai Y.T., Prabhala R.H., Ritz J., Neuberg D., Anderson K.C., Carrasco D.R., Dranoff G. MHC class I chain-related protein A antibodies and shedding are associated with the progression of multiple myeloma. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(4):1285-1290.
20. Kaiser B.K., Yim D., Chow I.T., Gonzalez S., Dai Z., Mann H.H., Strong R.K., Groh V., Spies T. Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature 2007, 447(7143):482-486.
21. Kiessling R., Klein E., Wigzell H. "Natural" killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur. J. Immunol. 1975, 5(2):112-117.
22. Lanier L.L. A renaissance for the tumor immunosurveillance hypothesis. Nat. Med. 2001, 7(11):1178-1180.
23. Lanier L.L. NK cell recognition. Annu. Rev. Immunol. 2005, 23:225-274.
24. Li K., Mandai M., Hamanishi J., Matsumura N., Suzuki A., Yagi H., Yamaguchi K., Baba T., Fujii S., Konishi I. Clinical significance of the NKG2D ligands, MICA/B and ULBP2 in ovarian cancer: high expression of ULBP2 is an indicator of poor prognosis. Cancer Immunol. Immunother. 2009, 58(5):641-652.
25. Limou S., Le Clerc S., Coulonges C., Carpentier W., Dina C., Delaneau O., Labib T., Taing L., Sladek R., Deveau C., Ratsimandresy R., Montes M., Spadoni J.L., Lelievre J.D., Levy Y., Therwath A., Schachter F., Matsuda F., Gut I., Froguel P., Delfraissy J.F., Hercberg S., Zagury J.F. Genomewide association study of an AIDS-nonprogression cohort emphasizes the role played by HLA genes (ANRS Genomewide Association Study 02). J. Infect. Dis. 2009, 199(3):419-426.
26. Linsley P.S., Bradshaw J., Urnes M., Grosmaire L., Ledbetter J.A. CD28 engagement by B7/BB-1 induces transient down-regulation of CD28 synthesis and prolonged unresponsiveness to CD28 signaling. J. Immunol. 1993, 150(8 Pt 1):3161-3169.
27. Liu Q., Sun Y., Rihn S., Nolting A., Tsoukas P.N., Jost S., Cohen K., Walker B., Alter G. Matrix metalloprotease inhibitors restore impaired NK cell-mediated antibody-dependent cellular cytotoxicity in human immunodeficiency virus type 1 infection. J. Virol. 2009, 83(17):8705-8712.
28. Lopez-Arbesu R., Ballina-Garcia F.J., Alperi-Lopez M., Lopez-Soto A., Rodriguez-Rodero S., Martinez-Borra J., Lopez-Vazquez A., Fernandez-Morera J.L., Riestra-Noriega J.L., Queiro-Silva R., Quinones-Lombrana A., Lopez-Larrea C., Gonzalez S. MHC class I chain-related gene B (MICB) is associated with rheumatoid arthritis susceptibility. Rheumatology (Oxford) 2007, 46(3):426-430.
29. Lozzio B.B., Lozzio C.B. Properties of the K562 cell line derived from a patient with chronic myeloid leukemia. Int. J. Cancer 1977, 19(1):136.
30. Mavilio D., Benjamin J., Daucher M., Lombardo G., Kottilil S., Planta M.A., Marcenaro E., Bottino C., Moretta L., Moretta A., Fauci A.S. 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(25):15011-15016.
31. Mavilio D., Lombardo G., Benjamin J., Kim D., Follman D., Marcenaro E., O'Shea M.A., Kinter A., Kovacs C., Moretta A., Fauci A.S. 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(8):2886-2891.
32. Ramankulov A., Lein M., Johannsen M., Schrader M., Miller K., Jung K. Plasma matrix metalloproteinase-7 as a metastatic marker and survival predictor in patients with renal cell carcinomas. Cancer Sci. 2008, 99(6):1188-1194.
33. Raulet D.H. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 2003, 3(10):781-790.
34. Salih H.R., Rammensee H.G., Steinle A. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J. Immunol. 2002, 169(8):4098-4102.
35. Salih H.R., Antropius H., Gieseke F., Lutz S.Z., Kanz L., Rammensee H.G., Steinle A. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 2003, 102(4):1389-1396.
36. Shimizu Y., DeMars R. Production of human cells expressing individual transferred HLA-A,-B,-C genes using an HLA-A,-B,-C null human cell line. J. Immunol. 1989, 142(9):3320-3328.
37. Shirts B.H., Kim J.J., Reich S., Dickerson F.B., Yolken R.H., Devlin B., Nimgaonkar V.L. Polymorphisms in MICB are associated with human herpes virus seropositivity and schizophrenia risk. Schizophr. Res. 2007, 94(1-3):342-353.
38. Smyth M.J., Swann J., Kelly J.M., Cretney E., Yokoyama W.M., Diefenbach A., Sayers T.J., Hayakawa Y. NKG2D recognition and perforin effector function mediate effective cytokine immunotherapy of cancer. J. Exp. Med. 2004, 200(10):1325-1335.
39. Trinchieri G. Biology of natural killer cells. Adv. Immunol. 1989, 47:187-376.
40. Valitutti S., Muller S., Salio M., Lanzavecchia A. Degradation of T cell receptor (TCR)-CD3-zeta complexes after antigenic stimulation. J. Exp. Med. 1997, 185(10):1859-1864.
41. Vetter C.S., Groh V., thor Straten P., Spies T., Brocker E.B., Becker J.C. Expression of stress-induced MHC class I related chain molecules on human melanoma. J. Invest. Dermatol. 2002, 118(4):600-605.
42. Waldhauer I., Goehlsdorf D., Gieseke F., Weinschenk T., Wittenbrink M., Ludwig A., Stevanovic S., Rammensee H.G., Steinle A. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008, 68(15):6368-6376.
43. Webster N.L., Crowe S.M. Matrix metalloproteinases, their production by monocytes and macrophages and their potential role in HIV-related diseases. J. Leukoc. Biol. 2006, 80(5):1052-1066.
44. Wiemann K., Mittrucker H.W., Feger U., Welte S.A., Yokoyama W.M., Spies T., Rammensee H.G., Steinle A. Systemic NKG2D down-regulation impairs NK and CD8 T cell responses in vivo. J. Immunol. 2005, 175(2):720-729.
45. Yokoyama Y., Grunebach F., Schmidt S.M., Heine A., Hantschel M., Stevanovic S., Rammensee H.G., Brossart P. Matrilysin (MMP-7) is a novel broadly expressed tumor antigen recognized by antigen-specific T cells. Clin. Cancer Res. 2008, 14(17):5503-5511.
46. Zaunders J., Carr A., McNally L., Penny R., Cooper D.A. Effects of primary HIV-1 infection on subsets of CD4+ and CD8+ T lymphocytes. AIDS 1995, 9(6):561-566.