Relative over-reactivity of human versus chimpanzee lymphocytes: Implications for the human diseases associated with immune activation

Journal of Immunology

Volumn 184, Issue 8, 2010, Pages 4185-4195

  Soto, Paula C ^a,b   Stein, Lance L ^a,b   Hurtado Ziola, Nancy ^a,b   Hedrick, Stephen M ^c   Varki, Ajit ^d  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d University of California San Diego   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LECTIN; SIALIC ACID RECOGNIZING IG SUPERFAMILY LECTIN 5; UNCLASSIFIED DRUG; URIDINE; CELL SURFACE RECEPTOR; DIFFERENTIATION ANTIGEN; GROWTH INHIBITOR; LEUKOCYTE ANTIGEN; SIGLEC14 PROTEIN, HUMAN; SIGLEC5 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL STIMULATION; CHIMPANZEE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; LYMPHOCYTE PROLIFERATION; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; SPECIES COMPARISON; T LYMPHOCYTE ACTIVATION; ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADAPTIVE IMMUNITY; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL PROLIFERATION; COMPARATIVE STUDY; DOWN REGULATION; GENETICS; HEPATITIS C; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PAN TROGLODYTES; PATHOLOGY; PHYSIOLOGY; T LYMPHOCYTE; UPREGULATION; VIROLOGY;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; B-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; DOWN-REGULATION; GROWTH INHIBITORS; HEPATITIS C; HIV INFECTIONS; HUMANS; LECTINS; LYMPHOCYTE ACTIVATION; PAN TROGLODYTES; RECEPTORS, CELL SURFACE; T-LYMPHOCYTES; UP-REGULATION;

EID: 77952760339     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903420     Document Type: Article

References (80)

1. Chimpanzee Sequencing and Analysis Consortium. 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437: 69-87.
2. Varki, A. 2000. A chimpanzee genome project is a biomedical imperative. Genome Res. 10: 1065-1070.
3. Varki, A., and T. K. Altheide. 2005. Comparing the human and chimpanzee genomes: searching for needles in a haystack. Genome Res. 15: 1746-1758.
4. Finch, C. E. 2009. The evolution of the human lifespan and diseases of aging: roles of infection, inflammation, and nutrition. Proc. Natl. Acad. Sci. U S A [Epub ahead of print]
5. Alter, H. J., J. W. Eichberg, H. Masur, W. C. Saxinger, R. Gallo, A. M. Macher, H. C. Lane, and A. S. Fauci. 1984. Transmission of HTLV-III infection fromhuman plasma to chimpanzees: an animal model for AIDS. Science 226: 549-552.
6. Novembre, F. J., M. Saucier, D. C. Anderson, S. A. Klumpp, S. P. O'Neil, C. R. I. Brown, 2nd, 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: 4086-4091.
7. Sharp, P. M., G. M. Shaw, and B. H. Hahn. 2005. Simian immunodeficiency virus infection of chimpanzees. J. Virol. 79: 3891-3902.
8. 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.
9. Bassett, S. E., K. M. Brasky, and R. E. Lanford. 1998. Analysis of hepatitis C virus-inoculated chimpanzees reveals unexpected clinical profiles. J. Virol. 72: 2589-2599.
10. Walker, C. M. 1997. Comparative features of hepatitis C virus infection in humans and chimpanzees. Springer Semin. Immunopathol. 19: 85-98.
11. Gagneux, P., and E. A. Muchmore. 2004. The chimpanzee model: contributions and considerations for studies of hepatitis B virus. Methods Mol. Med. 96: 289-318.
12. Akari, H., Y. Iwasaki, T. Yoshida, and S. Iijima. 2009. Non-human primate surrogate model of hepatitis C virus infection. Microbiol. Immunol. 53: 53-57.
13. Bukh, J., X. Forns, S. U. Emerson, and R. H. Purcell. 2001. Studies of hepatitis C virus in chimpanzees and their importance for vaccine development. Intervirology 44: 132-142.
14. Porter, B. F., S. D. Goens, K. M. Brasky, and G. B. Hubbard. 2004. A case report of hepatocellular carcinoma and focal nodular hyperplasia with a myelolipoma in two chimpanzees and a review of spontaneous hepatobiliary tumors in nonhuman primates. J. Med. Primatol. 33: 38-47.
15. Bettauer, R. H. 2010. Chimpanzees in hepatitis C virus research: 1998-2007. J. Med. Primatol. 39: 9-23.
16. Gougeon, M. L., H. Lecoeur, F. Boudet, E. Ledru, S. Marzabal, S. Boullier, R. Roué, S. Nagata, and J. 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.
17. Baenziger, S., M. Heikenwalder, P. Johansen, E. Schlaepfer, U. Hofer, R. C. Miller, S. Diemand, K. Honda, T. M. Kundig, A. Aguzzi, and R. F. Speck. 2009. Triggering TLR7 in mice induces immune activation and lymphoid system disruption, resembling HIV-mediated pathology. Blood 113: 377-388.
18. Franco, A., L. G. Guidotti, M. V. Hobbs, V. Pasquetto, and F. V. Chisari. 1997. Pathogenetic effector function of CD4-positive T helper 1 cells in hepatitis B virus transgenic mice. J. Immunol. 159: 2001-2008.
19. Schott, E., H. Witt, K. Neumann, S. Taube, D. Y. Oh, E. Schreier, S. Vierich, G. Puhl, A. Bergk, J. Halangk, et al. 2007. A Toll-like receptor 7 single nucleotide polymorphism protects from advanced inflammation and fibrosis in male patients with chronic HCV-infection. J. Hepatol. 47: 203-211.
20. Guidotti, L. G., and F. V. Chisari. 2006. Immunobiology and pathogenesis of viral hepatitis. Annu. Rev. Pathol. 1: 23-61.
21. Cohen, J. I., T. Moskal, M. Shapiro, and R. H. Purcell. 1996. Varicella in Chimpanzees. J. Med. Virol. 50: 289-292.
22. Crocker, P. R., J. C. Paulson, and A. Varki. 2007. Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7: 255-266.
23. Zhang, M., T. Angata, J. Y. Cho, M. Miller, D. H. Broide, and A. Varki. 2007. Defining the in vivo function of Siglec-F, a CD33-related Siglec expressed on mouse eosinophils. Blood 109: 4280-4287.
24. Hoffmann, A., S. Kerr, J. Jellusova, J. Zhang, F. Weisel, U. Wellmann, T. H. Winkler, B. Kneitz, P. R. Crocker, and L. Nitschke. 2007. Siglec-G is a B1 cell-inhibitory receptor that controls expansion and calcium signaling of the B1 cell population. Nat. Immunol. 8: 695-704.
25. Carlin, A. F., S. Uchiyama, Y. C. Chang, A. L. Lewis, V. Nizet, and A. Varki. 2009. Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil Siglec-9 and dampen the innate immune response. Blood 113: 3333-3336.
26. Chen, G. Y., J. Tang, P. Zheng, and Y. Liu. 2009. CD24 and Siglec-10 selectively repress tissue damage-induced immune responses. Science 323: 1722-1725.
27. Bochner, B. S. 2009. Siglec-8 on human eosinophils and mast cells, and Siglec-F on murine eosinophils, are functionally related inhibitory receptors. Clin. Exp. Allergy 39: 317-324.
28. Cornish, A. L., S. Freeman, G. Forbes, J. Ni, M. Zhang, M. Cepeda, R. Gentz, M. Augustus, K. C. Carter, and P. R. Crocker. 1998. Characterization of siglec-5, a novel glycoprotein expressed on myeloid cells related to CD33. Blood 92: 2123-2132.
29. Avril, T., S. D. Freeman, H. Attrill, R. G. Clarke, and P. R. Crocker. 2005. Siglec-5 (CD170) can mediate inhibitory signaling in the absence of immunoreceptor tyrosine-based inhibitory motif phosphorylation. J. Biol. Chem. 280: 19843-19851.
30. Carlin, A. F., Y. C. Chang, T. Areschoug, G. Lindahl, N. Hurtado-Ziola, C. C. King, A. Varki, and V. Nizet. 2009. Group B Streptococcus suppression of phagocyte functions by protein-mediated engagement of human Siglec-5. J. Exp. Med. 206: 1691-1699.
31. Song, D. J., J. Y. Cho, S. Y. Lee, M. Miller, P. Rosenthal, P. Soroosh, M. Croft, M. Zhang, A. Varki, and D. H. Broide. 2009. Anti-Siglec-F antibody reduces allergen-induced eosinophilic inflammation and airway remodeling. J. Immunol. 183: 5333-5341.
32. Hudson, S. A., N. V. Bovin, R. L. Schnaar, P. R. Crocker, and B. S. Bochner. 2009. Eosinophil-selective binding and proapoptotic effect in vitro of a synthetic Siglec-8 ligand, polymeric 6′-sulfated sialyl Lewis x. J. Pharmacol. Exp. Ther. 330: 608-612.
33. Boyd, C. R., S. J. Orr, S. Spence, J. F. Burrows, J. Elliott, H. P. Carroll, K. Brennan, J. Ní Gabhann, W. A. Coulter, J. A. Johnston, and C. A. Jefferies. 2009. Siglec-E is up-regulated and phosphorylated following lipopolysaccharide stimulation in order to limit TLR-driven cytokine production. J. Immunol. 183: 7703-7709.
34. Blasius, A. L., M. Cella, J. Maldonado, T. Takai, and M. Colonna. 2006. Siglec-H is an IPC-specific receptor that modulates type I IFN secretion through DAP12. Blood 107: 2474-2476.
35. Salomon, B., and J. A. Bluestone. 2001. Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annu. Rev. Immunol. 19: 225-252.
36. Schwartz, R. H. 2003. T cell anergy. Annu. Rev. Immunol. 21: 305-334.
37. Sharpe, A. H., and A. K. Abbas. 2006. T-cell costimulation - biology, therapeutic potential, and challenges. N. Engl. J. Med. 355: 973-975.
38. Zang, X., and J. P. Allison. 2007. The B7 family and cancer therapy: costimulation and coinhibition. Clin. Cancer Res. 13: 5271-5279.
39. Nguyen, D. H., N. Hurtado-Ziola, P. Gagneux, and A. Varki. 2006. Loss of Siglec expression on T lymphocytes during human evolution. Proc. Natl. Acad. Sci. USA 103: 7765-7770.
40. Ikehara, Y., S. K. Ikehara, and J. C. Paulson. 2004. Negative regulation of T cell receptor signaling by Siglec-7 (p70/AIRM) and Siglec-9. J. Biol. Chem. 279: 43117-43125.
41. Angata, T., T. Hayakawa, M. Yamanaka, A. Varki, and M. Nakamura. 2006. Discovery of Siglec-14, a novel sialic acid receptor undergoing concerted evolution with Siglec-5 in primates. FASEB J. 20: 1964-1973.
42. Varki, A., and T. Angata. 2006. Siglecs - the major subfamily of I-type lectins. Glycobiology 16: 1R-27R.
43. Lanier, L. L., and A. B. Bakker. 2000. The ITAM-bearing transmembrane adaptor DAP12 in lymphoid and myeloid cell function. Immunol. Today 21: 611-614.
44. Yamanaka, M., Y. Kato, T. Angata, and H. Narimatsu. 2009. Deletion polymorphism of SIGLEC14 and its functional implications. Glycobiology 19: 841-846.
45. Tacke, M., G. Hanke, T. Hanke, and T. Hünig. 1997. CD28-mediated induction of proliferation in resting T cells in vitro and in vivo without engagement of the T cell receptor: evidence for functionally distinct forms of CD28. Eur. J. Immunol. 27: 239-247.
46. Bischof, A., T. Hara, C. H. Lin, A. D. Beyers, and T. Hünig. 2000. Autonomous induction of proliferation, JNK and NF-alphaB activation in primary resting T cells by mobilized CD28. Eur. J. Immunol. 30: 876-882.
47. Rodríguez-Palmero, M., T. Hara, A. Thumbs, and T. Hünig. 1999. Triggering of T cell proliferation through CD28 induces GATA-3 and promotes T helper type 2 differentiation in vitro and in vivo. Eur. J. Immunol. 29: 3914-3924.
48. Hünig, T., and K. Dennehy. 2005. CD28 superagonists: mode of action and therapeutic potential. Immunol. Lett. 100: 21-28.
49. Beyersdorf, N., T. Hanke, T. Kerkau, and T. Hünig. 2005. Superagonistic anti-CD28 antibodies: potent activators of regulatory T cells for the therapy of autoimmune diseases. Ann. Rheum. Dis. 64(Suppl 4): iv91-iv95.
50. Schmidt, J., K. Elflein, M. Stienekemeier, M. Rodriguez-Palmero, C. Schneider, K. V. Toyka, R. Gold, and T. Hünig. 2003. Treatment and prevention of experimental autoimmune neuritis with superagonistic CD28-specific monoclonal antibodies. J. Neuroimmunol. 140: 143-152.
51. Lin, C. H., and T. Hünig. 2003. Efficient expansion of regulatory T cells in vitro and in vivo with a CD28 superagonist. Eur. J. Immunol. 33: 626-638.
52. Suntharalingam, G., M. R. Perry, S. Ward, S. J. Brett, A. Castello-Cortes, M. D. Brunner, and N. Panoskaltsis. 2006. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N. Engl. J. Med. 355: 1018-1028.
53. Schneider, C. K., U. Kalinke, and J. Löwer. 2006. TGN1412 - a regulator's perspective. Nat. Biotechnol. 24: 493-496.
54. Schraven, B., and U. Kalinke. 2008. CD28 superagonists: what makes the difference in humans? Immunity 28: 591-595.
55. Muul, L. M., C. Silvin, S. P. James, and F. Candotti. 2008. Measurement of proliferative responses of cultured lymphocytes. Curr Protoc Immunol Chapter 7: Unit 7.10.1-7.10.24.
56. Bibollet-Ruche, F., B. A. McKinney, A. Duverger, F. H. Wagner, A. A. Ansari, and O. Kutsch. 2008. The quality of chimpanzee T-cell activation and simian immunodeficiency virus/human immunodeficiency virus susceptibility achieved via antibody-mediated T-cell receptor/CD3 stimulation is a function of the anti-CD3 antibody isotype. J. Virol. 82: 10271-10278.
57. Moretta, A., A. Poggi, D. Olive, C. Bottino, C. Fortis, G. Pantaleo, and L. Moretta. 1987. Selection and characterization of T-cell variants lacking molecules involved in T-cell activation (T3 T-cell receptor, T44, and T11): analysis of the functional relationship among different pathways of activation. Proc. Natl. Acad. Sci. USA 84: 1654-1658.
58. Cummings, R. D., and S. Kornfeld. 1982. Characterization of the structural determinants required for the high affinity interaction of asparagine-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J. Biol. Chem. 257: 11230-11234.
59. Waibler, Z., L. Y. Sender, C. Merten, R. Hartig, S. Kliche, M. Gunzer, P. Reichardt, U. Kalinke, and B. Schraven. 2008. Signaling signatures and functional properties of anti-human CD28 superagonistic antibodies. PLoS ONE 3: e1708.
60. Bavari, S., R. E. Hunt, and R. G. Ulrich. 1995. Divergence of human and nonhuman primate lymphocyte responses to bacterial superantigens. Clin. Immunol. Immunopathol. 76: 248-254.
61. Cottrez, F., C. Auriault, A. Capron, and H. Groux. 1994. Analysis of the V beta specificity of superantigen activation with a rapid and sensitive method using RT PCR and an automatic DNA analyser. J. Immunol. Methods 172: 85-94.
62. Komanduri, K. V., M. D. Salha, R. P. Sékaly, and J. M. McCune. 1997. Superantigen-mediated deletion of specific T cell receptor V beta subsets in the SCID-hu Thy/Liv mouse is induced by staphylococcal enterotoxin B, but not HIV-1. J. Immunol. 158: 544-549.
63. Crocker, P. R. 2005. Siglecs in innate immunity. Curr. Opin. Pharmacol. 5: 431-437.
64. Diebold, S. S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
65. Heil, F., H. Hemmi, H. Hochrein, F. Ampenberger, C. Kirschning, S. Akira, G. Lipford, H. Wagner, and S. Bauer. 2004. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303: 1526-1529.
66. Stone, G. A., B. K. Johnson, R. Druilhet, P. B. Garza, and C. J. Gibbs, Jr. 2000. Immunophenotyping of peripheral blood, ranges of serum chemistries and clinical hematology values of healthy chimpanzees (Pan troglodytes). J. Med. Primatol. 29: 324-329.
67. Manigold, T., E. C. Shin, E. Mizukoshi, K. Mihalik, K. K. Murthy, C. M. Rice, C. A. Piccirillo, and B. Rehermann. 2006. Foxp3+CD4+CD25+ T cells control virus-specific memory T cells in chimpanzees that recovered from hepatitis C. Blood 107: 4424-4432.
68. Gogishvili, T., D. Langenhorst, F. Lühder, F. Elias, K. Elflein, K. M. Dennehy, R. Gold, and T. Hünig. 2009. Rapid regulatory T-cell response prevents cytokine storm in CD28 superagonist treated mice. PLoS One 4: e4643.
69. Findlay, L., D. Eastwood, R. Stebbings, G. Sharp, Y. Mistry, C. Ball, J. Hood, R. Thorpe, and S. Poole. 2009. Improved in vitro methods to predict the in vivo toxicity in man of therapeutic monoclonal antibodies including TGN1412. J. Immunol. Methods [Epub ahead of print]:
70. Virgin, H. W., E. J. Wherry, and R. Ahmed. 2009. Redefining chronic viral infection. Cell 138: 30-50.
71. Mariani, R., D. Chen, B. Schröfelbauer, F. Navarro, R. König, B. Bollman, C. Münk, H. Nymark-McMahon, and N. R. Landau. 2003. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114: 21-31.
72. Song, B., H. Javanbakht, M. Perron, D. H. Park, M. Stremlau, and J. Sodroski. 2005. Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. J. Virol. 79: 3930-3937.
73. Schindler, M., J. Münch, O. Kutsch, H. Li, M. L. Santiago, F. Bibollet-Ruche, M. C. Müller-Trutwin, F. J. Novembre, M. Peeters, V. Courgnaud, et al. 2006. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125: 1055-1067.
74. Gagneux, P., C. Wills, U. Gerloff, D. Tautz, P. A. Morin, C. Boesch, B. Fruth, G. Hohmann, O. A. Ryder, and D. S. Woodruff. 1999. Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc. Natl. Acad. Sci. USA 96: 5077-5082.
75. Keele, B. F., F. Van Heuverswyn, Y. Li, E. Bailes, J. Takehisa, M. L. Santiago, F. Bibollet-Ruche, Y. Chen, L. V. Wain, F. Liegeois, et al. 2006. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313: 523-526.
76. Badley, A. D. 2006. Cell death during HIV infection. CRC/Taylor & Francis, Boca Raton.
77. Oyaizu, N., T. W. McCloskey, S. Than, R. Hu, V. S. Kalyanaraman, and S. Pahwa. 1994. Cross-linking of CD4 molecules upregulates Fas antigen expression in lymphocytes by inducing interferon-gamma and tumor necrosis factor-alpha secretion. Blood 84: 2622-2631.
78. Mandl, J. N., A. P. Barry, T. H. Vanderford, N. Kozyr, R. Chavan, S. Klucking, F. J. Barrat, R. L. Coffman, S. I. Staprans, and M. B. Feinberg. 2008. Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat. Med. 14: 1077-1087.
79. Hedrick, S. M. 2004. The acquired immune system: a vantage from beneath. Immunity 21: 607-615.
80. Hedrick, S. M. 2009. Immune system: not so superior. Science 325: 1623-1624.