Differential NKp30 inducibility in chimpanzee NK cells and conserved NK cell phenotype and function in long-term HIV-1-infected animals

Journal of Immunology

Volumn 178, Issue 3, 2007, Pages 1702-1712

  Rutjens, Erik ^a   Mazza, Stefania ^b,c   Biassoni, Roberto ^d   Koopman, Gerrit ^a   Radic, Luana ^d   Fogli, Manuela ^c,f   Costa, Paola ^b,d   Mingari, Maria Cristina ^c,e   Moretta, Lorenzo ^b,c,d   Heeney, Jonathan ^a   De Maria, Andrea ^b,c,e,g  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^b Centro di Eccellenza per la Ricerca Biomedica   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d G GASLINI INSTITUTE   (Italy)

^e CENTRO DI BIOTECNOLOGIE AVANZATE   (Italy)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^g UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; NATURAL KILLER CELL RECEPTOR NKP30; NATURAL KILLER CELL RECEPTOR NKP46; NATURAL KILLER CELL RECEPTOR NKP80; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADAPTIVE IMMUNITY; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL INTERACTION; CHIMPANZEE; DENDRITIC CELL; DISEASE COURSE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LENTIVIRINAE; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION;

EID: 33846526231     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.3.1702     Document Type: Article

References (60)

1. Chimpanzee Sequencing and Analysis Consortium. 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437: 69-87.
2. Heeney, J. L., A. G. Dalgleish, and R. A. Weiss. 2006. Origins of HIV and the evolution of resistance to AIDS. Science 313: 462-466.
3. Rutjens, E., S. Balla-Jhagjhoorsingh, E. Verschoor, W. Bogers, G. Koopman, and J. L. Heeney. 2003. Lentivirus infections and mechanisms of disease resistance in chimpanzees. Front. Biosci. 8: d1134-d1145.
4. ten Haaft, P., K. Murthy, M. Salas, H. McClure, R. Dubbes, W. Koornstra, H. Niphuis, D. Davis, G. van der Groen, and J. Heeney. 2001. Differences in early virus loads with different phenotypic variants of HIV-1 and SIV(cpz) in chimpanzees. AIDS 15: 2085-2092.
5. Novembre, F. J., M. Saucier, D. C. Anderson, S. A. Klumpp, S. P. O'Neil, C. R. Brown, II, C. E. Hart, P. C. Guenthner, R. B. Swenson, and H. M. McClure. 1997. Development of AIDS in a chimpanzee infected with human immunodeficiency virus type 1. J. Virol. 71: 4086-4084.
6. + cytotoxic T lymphocytes. AIDS Res. Hum. Retroviruses 15: 365-373.
7. Balla-Jhagjhoorsingh, S. S., E. J. Verschoor, N. de Groot, V. J. Teeuwsen, R. E. Bontrop, and J. L. Heeney. 2003. Specific nature of cellular immune responses elicited by chimpanzees against HIV-1. Hum. Immunol. 64: 681-688.
8. Balla-Jhagjhoorsingh, S. S., G. Koopman, P. Mooij, T. G. Haaksma, V. J. Teeuwsen, R. E. Bontrop, and J. L. Heeney. 1999. Conserved CTL epitopes shared between HIV-infected human long-term survivors and chimpanzees. J. Immunol. 162: 2308-2314.
9. Alpan, O., E. Bachelder, E. Isil, H. Arnheiter, and P. Matzinger. 2004. 'Educated' dendritic cells act as messengers from memory to naive T helper cells. Nat. Immunol. 5: 615-622.
10. Heeney, J. L., P. Beverley, A. McMichael, G. Shearer, J. Strominger, B. Wahren, J. Weber, and F. Gotch. 1999. Immune correlates of protection from HIV and AIDS - more answers but yet more questions. Immunol. Today 20: 247-251.
11. Ondoa, P., C. Vereecken, K. Fransen, R. Colebunders, G. van der Groen, J. L. Heeney, and L. Kestens. 2003. Human and simian immunodeficiency virus-infected chimpanzees do not have increased intracellular levels of β-chemokines in contrast to infected humans. J. Med. Virol. 69: 297-305.
12. Dalgleish, A. G., and K. J. O'Byrne. 2002. Chronic immune activation and inflammation in the pathogenesis of AIDS and cancer. Adv. Cancer Res. 84: 231-276.
13. Gougeon, M. L., H. Lecoeur, F. Boudet, E. Ledru, S. Marzabal, S. Boullier, R. Roue, S. Nagata, and J. L. Heeney. 1997. Lack of chronic immune activation in HIV-infected chimpanzees correlates with the resistance of T cells to Fas/Apo-1 (CD95)-induced apoptosis and preservation of a T helper 1 phenotype. J. Immunol. 158: 2964-2976.
14. + T-cell levels. AIDS 7: 1159-1166.
15. Pantaleo, G., S. Menzo, M. Vaccarezza, C. Graziosi, O. J. Cohen, J. F. Demarest, D. Montefiori, J. M. Orenstein, C. Fox, L. K. Schrager, and A. S. Fauci. 1995. Studies in subjects with long-term nonprogressive human immunodeficiency virus infection. N. Engl. J. Med. 332: 209-216.
16. Cao, Y., L. Qin, L. Zhang, J. Safrit, and D. D. Ho. 1995. Virologic and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N. Engl. J. Med. 332: 201-208.
17. Trabattoni, D., S. Piconi, M. Biasin, G. Rizzardini, M. Migliorino, E. Seminari, A. Boasso, L. Piacentini, M. L. Villa, R. Maserati, and M. Clerici. 2004. Granule-dependent mechanisms of lysis are defective in CD8 T cells of HIV-infected, antiretroviral therapy-treated individuals. AIDS 18: 859-854.
18. Rodes, B., C. Toro, E. Paxinos, E. Poveda, M. Martinez-Padial, J. M. Benito, V. Jimenez, T. Wrin, S. Bassani, and V. Soriano. 2004. Differences in disease progression in a cohort of long-term non-progressors after more than 16 years of HIV-1 infection. AIDS 18: 1109-1116.
19. + T-cell repertoire in long-term nonprogressors and its role in the control of viral load and disease activity. Hum. Immunol. 62: 561-576.
20. Migueles, S. A., M. S. Sabbaghian, W. L. Shupert, M. P. Bettinotti, F. M. Marincola, L. Martino, C. W. Hallahan, S. M. Selig, D. Schwartz, J. Sullivan, and M. Connors. 2000. HLA B*5701 is highly associated with restriction of virus replication in a subgroup of HIV-infected long term nonprogressors. Proc. Natl. Acad. Sci. USA 97: 2709-2714.
21. Valdez, H., N. L. Carlson, A. B. Post, R. Asaad, P. S. Heeger, M. M. Lederman, P. V. Lehmann, and D. D. Anthony. 2002. HIV long-term non-progressors maintain brisk CD8 T cell responses to other viral antigens. AIDS 16: 1113-1118.
22. Koup, R. A., J. T. Safrit, Y. Cao, C. A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D. D. Ho. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68: 4650-4655.
23. + Th1 effector cells during primary HIV-1 infection. Blood 106: 1660-1667.
24. Zaunders, J. J., P. H. Cunningham, A. D. Kelleher, G. R. Kaufmann, A. B. Jaramillo, R. Wright, D. Smith, P. Grey, J. Vizzard, A. Carr, and D. A. Cooper. 1999. Potent antiretroviral therapy of primary human immunodeficiency virus type 1 (HIV-1) infection: partial normalization of T lymphocyte subsets and limited reduction of HIV-1 DNA despite clearance of plasma viremia. J. Infect. Dis. 180: 320-329.
25. Fleury, S., G. P. Rizzardi, A. Chapuis, G. Tambussi, C. Knabenhans, E. Simeoni, J. Y. Meuwly, J. M. Corpataux, A. Lazzarin, F. Miedema, and G. Pantaleo. 2000. Long-term kinetics of T cell production in HIV-infected subjects treated with highly active antiretroviral therapy. Proc. Natl. Acad. Sci. USA 97: 5393-5398.
26. + T lymphocytes of patients with AIDS maintain normal broad cytolytic function despite the loss of human immunodeficiency virus-specific cytotoxicity. Proc. Natl. Acad. Sci. USA 87: 4818-4822.
27. De Maria, A., A. Ferraris, M. Guastella, S. Pilia, C. Cantoni, L. Polero, M. C. Mingari, D. Bassetti, A. S. Fauci, and L. Moretta. 1997. Expression of HLA class I-specific inhibitory natural killer cell receptors in HIV-specific cytolytic T lymphocytes: impairment of specific cytolytic functions. Proc. Natl. Acad. Sci. USA 94: 10285-10288.
28. Trimble, L. A., P. Shankar, M. Patterson, J. P. Daily, and J. Lieberman. 2000. Human immunodeficiency virus-specific circulating CD8 T lymphocytes have down-modulated CD3ζ and CD28, key signaling molecules for T-cell activation. J. Virol. 74: 7320-7330.
29. Grassi, F., A. Hosmalin, D. McIlroy, V. Calvez, P. Debre, and B. Autran. 1999. Depletion in blood CD11c-positive dendritic cells from HIV-infected patients. AIDS 13: 759-766.
30. Moretta, A. 2005. The dialogue between human natural killer cells and dendritic cells. Curr. Opin. Immunol 17: 306-311.
31. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274.
32. Moretta, L., and A. Moretta. 2004. Killer immunoglobulin-like receptors. Curr. Opin. Immunol. 16: 626-633.
33. Bottino, C., R. Castriconi, L. Moretta, and A. Moretta. 2005. Cellular ligands of activating NK receptors. Trends Immunol. 26: 221-226.
34. Biassoni, R., and N. Dimasi. 2005. Human natural killer cell receptor functions and their implication in diseases. Expert Rev. Clin. Immunol. I: 405-417.
35. Moretta, L., C. Bottino, D. Pende, M. C. Mingari, R. Biassoni, and A. Moretta. 2002. Human natural killer cells: their origin, receptors and function. Eur. J. Immunol. 32: 1205-1211.
36. Ferlazzo, G., M. Pack, D. Thomas, C. Paludan, D. Schmid, T. Strowig, G. Bougras, W. A. Muller, L. Moretta, and C. Munz. 2004. Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc. Natl. Acad. Sci. USA 101: 16606-16611.
37. Vitale, M., M. Della Chiesa, S. Carlomagno, D. Pende, M. Arico, L. Moretta, and A. Moretta. 2005. NK-dependent DC maturation is mediated by TKFα and IFN-γ released upon engagement of the NKp30 triggering receptor. Blood 106: 566-571.
38. + T cell effector function in response to an intracellular pathogen. J. Immunol. 172: 130-137.
39. Vitale, C., L. Chiossone, G. Morreale, E. Lanino, F. Cottalasso, S. Moretti, G. Dini, L. Moretta, and M. C. Mingari. 2005. Human natural killer cells undergoing in vivo differentiation after allogeneic bone marrow transplantation: analysis of the surface expression and function of activating NK receptors. Mol. Immunol 42: 405-411.
40. Poli, G., P. Biswas, and A. S. Fauci. 1994. Interferons in the pathogenesis and treatment of human immunodeficiency virus infection. Antiviral Res. 24: 221-233.
41. Cai, Q., X. L. Huang, G. Rappocciolo, and C. R. Rinaldo, Jr. 1990. Natural killer cell responses in homosexual men with early HIV infection. J. Acquired Immune Defic. Syndr. 3: 669-664.
42. De Maria, A., M. Fogli, P. Costa, G. Murdaca, F. Puppo, D. Mavilio, A. Moretta, and L. Moretta. 2003. 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. 33: 2410-2418.
43. Fogli, M., P. Costa, G. Murdaca, M. Setti, M. C. Mingari, L. Moretta, A. Moretta, and A. De Maria. 2004. Significant NK cell activation associated with decreased cytolytic function in peripheral blood of HIV-1-infected patients. Eur. J. Immunol 34: 2313-2321.
44. + natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc. Natl. Acad. Sci. USA 102: 2886-2884.
45. Mela, C. M., C. T. Burton, N. Imami, M. Nelson, A. Steel, B. G. Gazzard, F. M. Gotch, and M. R. Goodier. 2005. Switch from inhibitory to activating NKG2 receptor expression in HIV-1 infection: lack of reversion with highly active antiretroviral therapy. AIDS 19: 1761-1769.
46. Guma, M., C. Cabrera, I. Erkizia, M. Bofill, B. Clotet, L. Ruiz, and M. Lopez-Botet. 2006. Human cytomegalovirus infection is associated with increased proportions of NK cells that express the CD94/NKG2C receptor in aviremic HIV-1-positive patients. J. Infect. Dis. 194: 38-41.
47. De Maria, A., R. Biassoni, M. Fogli, M. Rizzi, C. Cantoni, P. Costa, R. Conte, D. Mavilio, B. Ensoli, A. Cafaro, et al. 2001. Identification, molecular cloning and functional characterization of NKp46 and NKp30 natural cytotoxicity receptors in Macaca fascicularis NK cells. Eur. J. Immunol. 31: 3546-3556.
48. Biassoni, R., M. Fogli, C. Cantoni, P. Costa, R. Conte, G. Koopman, A. Cafaro, B. Ensoli, A. Moretta, L. Moretta, and A. De Maria. 2005. Molecular and functional characterization of NKG2D, NKp80, and NKG2C triggering NK cell receptors in rhesus and cynomolgus macaques: monitoring of NK cell function during simian HIV infection. J. Immunol. 174: 5695-5705.
49. Ponassi, M., C. Cantoni, R. Biassoni, R. Conte, A. Spallarossa, A. Pesce, A. Moretta, L. Moretta, M. Bolognesi, and D. Bordo. 2003. Structure of the human NK cell triggering receptor NKp46 ectodomain. Biochem. Biophys. Res. Commun. 309: 317-323.
50. Vitale, M., M. Falco, R. Castriconi, S. Parolini, R. Zambello, G. Semenzato, R. Biassoni, C. Bottino, L. Moretta, and A. Moretta. 2001. Identification of NKp80, a novel triggering molecule expressed by human NK cells. Eur. J. Immunol. 31: 233-242.
51. Biassoni, R., S. Ferrini, I. Prigione, A. Moretta, and E. O. Long. 1988. CD3-negative lymphokine-activated cytotoxic cells express the CD3 epsilon gene. J. Immunol. 140: 1685-1689.
52. Lanier, L. L., C. Chang, H. Spits, and J. H. Phillips. 1992. Expression of cytoplasmic CD3 epsilon proteins in activated human adult natural killer (NK) cells and CD3 α, γ, ε complexes in fetal NK cells. Implications for the relationship of NK and T lymphocytes. J. Immunol. 149: 1876-1880.
53. Wang, J. G., M. Collinge, V. Ramgolam, O. Ayalon, X. C. Fan, R. Pardi, and J. R. Bender. 2006. LFA-1-dependent HuR nuclear export and cytokine mRNA stabilization in T cell activation. J. Immunol. 176: 2105-2113.
54. Meng, Z., P. H. King, L. B. Nabors, N. L. Jackson, C. Y. Chen, P. D. Emanuel, and S. W. Blume. 2005. The ELAV RNA-stability factor HuR binds the 5′-untranslated region of the human IGF-IR transcript and differentially represses cap-dependent and IRES-mediated translation. Nucleic Acids Res. 33: 2962-2979.
55. Ferlazzo, G., M. L. Tsang, L. Moretta, G. Melioli, R. M. Steinman, and C. Munz. 2002. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J. Exp. Med. 195: 343-351.
56. Pende, D., R. Castriconi, P. Romagnani, G. M. Spaggiari, S. Marcenaro, A. Dondero, E. Lazzeri, L. Lasagni, S. Martini, P. Rivera, A. Capobianco, et al. 2006. Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood 107: 2030-2036.
57. Khakoo, S. I., C. L. Thio, M. P. Martin, C. R. Brooks, X. Gao, J. Astemborski. J. Cheng, J. J. Goedert, D. Vlahov, M. Hilgartner, et al. 2004. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305: 872-874.
58. Carrington, M., S. Wang, M. P. Martin, X. Gao, M. Schiffman, J. Cheng, R. Herrero, A. C. Rodriguez, R. Kurman, R. Mortel, et al. 2005. Hierarchy of resistance to cervical neoplasia mediated by combinations of killer immunoglobulin-like receptor and human leukocyte antigen loci. J. Exp. Med. 201: 1069-1075.
59. Martin, M. P., X. Gao, J. H. Lee, G. W. Nelson, R. Detels, J. J. Goedert, S. Buchbinder, K. Hoots, D. Vlahov, J. Trowsdale, et al. 2002. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat. Genet. 31:429-434.
60. Nguyen, D. H., N. Hurtado-Zola, P. Gagneux, and A. Varki. 2006. Loss of Siglec expression on T lymphocytes during human evolution. Proc. Natl. Acad. Sci. USA 103: 7765-7770.