Leukocyte-associated Ig-like receptor-1 - Deficient mice have an altered immune cell phenotype

Journal of Immunology

Volumn 188, Issue 2, 2012, Pages 548-558

  Tang, Xiaobin ^a,d   Tian, Linjie ^a   Esteso, Gloria ^a   Choi, Seung Chul ^a   Barrow, Alexander D ^b,e   Colonna, Marco ^b   Borrego, Francisco ^c   Coligan, John E ^a  

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

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CELL PROTEIN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; LEUKOCYTE ASSOCIATED IMMUNOGLOBULIN LIKE RECEPTOR 1; OVALBUMIN; TRINITROPHENYL; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE ACTIVATION; CELL MIGRATION; CELLULAR IMMUNITY; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE EXACERBATION; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNIZATION; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY T LYMPHOCYTE; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; WILD TYPE;

ANIMALS; B-LYMPHOCYTE SUBSETS; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; IMMUNOPHENOTYPING; LEUKOCYTES; LONGEVITY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, IMMUNOLOGIC; SPLEEN; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 84862927540     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102044     Document Type: Article

References (58)

1. Long, E. O. 2008. Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol. Rev. 224: 70-84.
2. Hoek, R. M., S. R. Ruuls, C. A. Murphy, G. J. Wright, R. Goddard, S. M. Zurawski, B. Blom, M. E. Homola, W. J. Streit, M. H. Brown, et al. 2000. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 290: 1768-1771. (Pubitemid 32004808)
3. Nishimura, H., M. Nose, H. Hiai, N. Minato, and T. Honjo. 1999. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11: 141-151. (Pubitemid 29428807)
4. Oya, Y., N. Watanabe, T. Owada, M. Oki, K. Hirose, A. Suto, S. Kagami, H. Nakajima, T. Kishimoto, I. Iwamoto, et al. 2008. Development of autoimmune hepatitis-like disease and production of autoantibodies to nuclear antigens in mice lacking B and T lymphocyte attenuator. Arthritis Rheum. 58: 2498-2510.
5. Bolland, S., and J. V. Ravetch. 2000. Spontaneous autoimmune disease in Fc (gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity 13: 277-285.
6. Lebbink, R. J., T. de Ruiter, A. Verbrugge, W. S. Bril, and L. Meyaard. 2004. The mouse homologue of the leukocyte-associated Ig-like receptor-1 is an inhibitory receptor that recruits Src homology region 2-containing protein tyrosine phosphatase (SHP)-2, but not SHP-1. J. Immunol. 172: 5535-5543. (Pubitemid 38542055)
7. Verbrugge, A., E. S. Rijkers, T. de Ruiter, and L. Meyaard. 2006. Leukocyte-associated Ig-like receptor-1 has SH2 domain-containing phosphatase-independent function and recruits C-terminal Src kinase. Eur. J. Immunol. 36: 190-198. (Pubitemid 43116405)
8. Verbrugge, A., T. Ruiter Td, H. Clevers, and L. Meyaard. 2003. Differential contribution of the immunoreceptor tyrosine-based inhibitory motifs of human leukocyte-associated Ig-like receptor-1 to inhibitory function and phosphatase recruitment. Int. Immunol. 15: 1349-1358. (Pubitemid 37369328)
9. Lebbink, R. J., T. de Ruiter, G. J. Kaptijn, D. G. Bihan, C. A. Jansen, P. J. Lenting, and L. Meyaard. 2007. Mouse leukocyte-associated Ig-like receptor-1 (mLAIR-1) functions as an inhibitory collagen-binding receptor on immune cells. Int. Immunol. 19: 1011-1019. (Pubitemid 47386926)
10. Maasho, K., M. Masilamani, R. Valas, S. Basu, J. E. Coligan, and F. Borrego. 2005. The inhibitory leukocyte-associated Ig-like receptor-1 (LAIR-1) is expressed at high levels by human naive T cells and inhibits TCR mediated activation. Mol. Immunol. 42: 1521-1530. (Pubitemid 40798939)
11. van der Vuurst de Vries, A. R., H. Clevers, T. Logtenberg, and L. Meyaard. 1999. Leukocyte-associated immunoglobulin-like receptor-1 (LAIR-1) is differentially expressed during human B cell differentiation and inhibits B cell receptor-mediated signaling. Eur. J. Immunol. 29: 3160-3167.
12. Verbrugge, A., T. de Ruiter, C. Geest, P. J. Coffer, and L. Meyaard. 2006. Differential expression of leukocyte-associated Ig-like receptor-1 during neutrophil differentiation and activation. J. Leukoc. Biol. 79: 828-836. (Pubitemid 44835615)
13. Poggi, A., S. Catellani, A. Bruzzone, F. Caligaris-Cappio, M. Gobbi, and M. R. Zocchi. 2008. Lack of the leukocyte-associated Ig-like receptor-1 expression in high-risk chronic lymphocytic leukaemia results in the absence of a negative signal regulating kinase activation and cell division. Leukemia 22: 980-988. (Pubitemid 351689880)
14. Lebbink, R. J., T. de Ruiter, J. Adelmeijer, A. B. Brenkman, J. M. van Helvoort, M. Koch, R. W. Farndale, T. Lisman, A. Sonnenberg, P. J. Lenting, and L. Meyaard. 2006. Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1. J. Exp. Med. 203: 1419-1425. (Pubitemid 43877604)
15. Jansen, C. A., C. W. Cruijsen, T. de Ruiter, N. Nanlohy, N. Willems, P. L. Janssens-Korpela, and L. Meyaard. 2007. Regulated expression of the inhibitory receptor LAIR-1 on human peripheral T cells during T cell activation and differentiation. Eur. J. Immunol. 37: 914-924. (Pubitemid 46925329)
16. Meyaard, L., J. Hurenkamp, H. Clevers, L. L. Lanier, and J. H. Phillips. 1999. Leukocyte-associated Ig-like receptor-1 functions as an inhibitory receptor on cytotoxic T cells. J. Immunol. 162: 5800-5804. (Pubitemid 29314931)
17. Lebbink, R. J., M. C. van den Berg, T. de Ruiter, N. Raynal, J. A. van Roon, P. J. Lenting, B. Jin, and L. Meyaard. 2008. The soluble leukocyte-associated Iglike receptor (LAIR)-2 antagonizes the collagen/LAIR-1 inhibitory immune interaction. J. Immunol. 180: 1662-1669.
18. Tang, X., S. Narayanan, G. Peruzzi, A. Apara, K. Natarajan, D. H. Margulies, J. E. Coligan, and F. Borrego. 2009. A single residue, arginine 65, is critical for the functional interaction of leukocyte-associated inhibitory receptor-1 with collagens. J. Immunol. 182: 5446-5452.
19. Leitinger, B., and E. Hohenester. 2007. Mammalian collagen receptors. Matrix Biol. 26: 146-155. (Pubitemid 46401227)
20. Myllyharju, J., and K. I. Kivirikko. 2004. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20: 33-43. (Pubitemid 38032818)
21. Yoshimura, T., W. Matsuyama, and H. Kamohara. 2005. Discoidin domain receptor 1: a new class of receptor regulating leukocyte-collagen interaction. Immunol. Res. 31: 219-230.
22. Matsuyama, W., L. Wang, W. L. Farrar, M. Faure, and T. Yoshimura. 2004. Activation of discoidin domain receptor 1 isoform b with collagen up-regulates chemokine production in human macrophages: role of p38 mitogen-activated protein kinase and NF-kappa B. J. Immunol. 172: 2332-2340. (Pubitemid 38182381)
23. Nieswandt, B., and S. P. Watson. 2003. Platelet-collagen interaction: is GPVI the central receptor? Blood 102: 449-461. (Pubitemid 36841960)
24. Ruggeri, Z. M. 2002. Platelets in atherothrombosis. Nat. Med. 8: 1227-1234. (Pubitemid 35373553)
25. de Fougerolles, A. R., A. G. Sprague, C. L. Nickerson-Nutter, G. Chi-Rosso, P. D. Rennert, H. Gardner, P. J. Gotwals, R. R. Lobb, and V. E. Koteliansky. 2000. Regulation of inflammation by collagen-binding integrins alpha1beta1 and alpha2beta1 inmodels of hypersensitivity and arthritis. J. Clin. Invest. 105: 721-729. (Pubitemid 30164110)
26. Ray, S. J., S. N. Franki, R. H. Pierce, S. Dimitrova, V. Koteliansky, A. G. Sprague, P. C. Doherty, A. R. de Fougerolles, and D. J. Topham. 2004. The collagen binding alpha1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity 20: 167-179. (Pubitemid 38258393)
27. Halin, C., M. L. Scimone, R. Bonasio, J. M. Gauguet, T. R. Mempel, E. Quackenbush, R. L. Proia, S. Mandala, and U. H. von Andrian. 2005. The S1P-analog FTY720 differentially modulates T-cell homing via HEV: T-cell-expressed S1P1 amplifies integrin activation in peripheral lymph nodes but not in Peyer patches. Blood 106: 1314-1322. (Pubitemid 41129595)
28. Morrissey, P. J., K. Charrier, S. Braddy, D. Liggitt, and J. D. Watson. 1993. CD4+ T cells that express high levels of CD45RB induce wasting disease when transferred into congenic severe combined immunodeficient mice. Disease development is prevented by cotransfer of purified CD4+ T cells. J. Exp. Med. 178: 237-244. (Pubitemid 23173259)
29. Stromnes, I. M., and J. M. Goverman. 2006. Active induction of experimental allergic encephalomyelitis. Nat. Protoc. 1: 1810-1819. (Pubitemid 46773300)
30. Ivanov, I. I., B. S. McKenzie, L. Zhou, C. E. Tadokoro, A. Lepelley, J. J. Lafaille, D. J. Cua, and D. R. Littman. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133. (Pubitemid 44380299)
31. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R. M. Steinman. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176: 1693-1702.
32. Pillai, S., and A. Cariappa. 2009. The follicular versus marginal zone B lymphocyte cell fate decision. Nat. Rev. Immunol. 9: 767-777.
33. Martin, F., and J. F. Kearney. 2002. Marginal-zone B cells. Nat. Rev. Immunol. 2: 323-335. (Pubitemid 37328755)
34. Bonaccorsi, I., C. Cantoni, P. Carrega, D. Oliveri, G. Lui, R. Conte, M. Navarra, R. Cavaliere, E. Traggiai, M. Gattorno, et al. 2010. The immune inhibitory receptor LAIR-1 is highly expressed by plasmacytoid dendritic cells and acts complementary with NKp44 to control IFNa production. PLoS ONE 5: e15080.
35. Bolland, S., Y. S. Yim, K. Tus, E. K. Wakeland, and J. V. Ravetch. 2002. Genetic modifiers of systemic lupus erythematosus in FcgammaRIIB(-/-) mice. J. Exp. Med. 195: 1167-1174. (Pubitemid 34517142)
36. Fujikado, N., S. Saijo, T. Yonezawa, K. Shimamori, A. Ishii, S. Sugai, H. Kotaki, K. Sudo, M. Nose, and Y. Iwakura. 2008. Dcir deficiency causes development of autoimmune diseases in mice due to excess expansion of dendritic cells. Nat. Med. 14: 176-180. (Pubitemid 351214549)
37. Okazaki, T., I. M. Okazaki, J. Wang, D. Sugiura, F. Nakaki, T. Yoshida, Y. Kato, S. Fagarasan, M. Muramatsu, T. Eto, et al. 2011. PD-1 and LAG-3 inhibitory coreceptors act synergistically to prevent autoimmunity in mice. J. Exp. Med. 208: 395-407.
38. Pisitkun, P., J. A. Deane, M. J. Difilippantonio, T. Tarasenko, A. B. Satterthwaite, and S. Bolland. 2006. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 312: 1669-1672. (Pubitemid 43902669)
39. Powrie, F., J. Carlino, M. W. Leach, S. Mauze, and R. L. Coffman. 1996. A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J. Exp. Med. 183: 2669-2674.
40. Pillai, S., A. Cariappa, and S. T. Moran. 2005. Marginal zone B cells. Annu. Rev. Immunol. 23: 161-196. (Pubitemid 40563168)
41. Ehrenstein, M. R., and C. A. Notley. 2010. The importance of natural IgM: scavenger, protector and regulator. Nat. Rev. Immunol. 10: 778-786.
42. Poggi, A., E. Tomasello, E. Ferrero, M. R. Zocchi, and L. Moretta. 1998. p40/LAIR-1 regulates the differentiation of peripheral blood precursors to dendritic cells induced by granulocyte-monocyte colony-stimulating factor. Eur. J. Immunol. 28: 2086-2091. (Pubitemid 28321291)
43. Mócsai, A., M. B. Humphrey, J. A. Van Ziffle, Y. Hu, A. Burghardt, S. C. Spusta, S. Majumdar, L. L. Lanier, C. A. Lowell, and M. C. Nakamura. 2004. The immunomodulatory adapter proteins DAP12 and Fc receptor gamma-chain (FcRgamma) regulate development of functional osteoclasts through the Syk tyrosine kinase. Proc. Natl. Acad. Sci. USA 101: 6158-6163. (Pubitemid 38520544)
44. Barrow, A. D., N. Raynal, T. L. Andersen, D. A. Slatter, D. Bihan, N. Pugh, M. Cella, T. Kim, J. Rho, T. Negishi-Koga, et al. 2011. OSCAR is a collagen receptor that costimulates osteoclastogenesis in DAP12-deficient humans and mice. J. Clin. Invest. 121: 3505-3516.
45. Barrow, A. D., and J. Trowsdale. 2008. The extended human leukocyte receptor complex: diverse ways of modulating immune responses. Immunol. Rev. 224: 98-123.
46. Daëron, M., S. Jaeger, L. Du Pasquier, and E. Vivier. 2008. Immunoreceptor tyrosine-based inhibition motifs: a quest in the past and future. Immunol. Rev. 224: 11-43.
47. Zocchi, M. R., F. Pellegatta, I. Pierri, M. Gobbi, and A. Poggi. 2001. Leukocyte-associated Ig-like receptor-1 prevents granulocyte-monocyte colony stimulating factor-dependent proliferation and Akt1/PKB alpha activation in primary acute myeloid leukemia cells. Eur. J. Immunol. 31: 3667-3675. (Pubitemid 34030980)
48. Castro, C., and M. Gourley. 2010. Diagnostic testing and interpretation of tests for autoimmunity. J. Allergy Clin. Immunol. 125(Suppl 2): S238-S247.
49. Simon, D., and H. U. Simon. 2007. Eosinophilic disorders. J. Allergy Clin. Immunol. 119: 1291-1300; quiz 1301-1292.
50. Xue, J., X. Zhang, H. Zhao, Q. Fu, Y. Cao, Y. Wang, X. Feng, and A. Fu. 2011. Leukocyte-associated immunoglobulin-like receptor-1 is expressed on human megakaryocytes and negatively regulates the maturation of primary megakaryocytic progenitors and cell line. Biochem. Biophys. Res. Commun. 405: 128-133.
51. Wu, C., F. Ivars, P. Anderson, R. Hallmann, D. Vestweber, P. Nilsson, H. Robenek, K. Tryggvason, J. Song, E. Korpos, et al. 2009. Endothelial basement membrane laminin alpha5 selectively inhibits T lymphocyte extravasation into the brain. Nat. Med. 15: 519-527.
52. Sixt, M., B. Engelhardt, F. Pausch, R. Hallmann, O. Wendler, and L. M. Sorokin. 2001. Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood-brain barrier in experimental autoimmune encephalomyelitis. J. Cell Biol. 153: 933-946.
53. Wu, Y., K. Tworkoski, M. Michaud, and J. A. Madri. 2009. Bone marrow monocyte PECAM-1 deficiency elicits increased osteoclastogenesis resulting in trabecular bone loss. J. Immunol. 182: 2672-2679.
54. Mori, Y., S. Tsuji, M. Inui, Y. Sakamoto, S. Endo, Y. Ito, S. Fujimura, T. Koga, A. Nakamura, H. Takayanagi, et al. 2008. Inhibitory immunoglobulin-like receptors LILRB and PIR-B negatively regulate osteoclast development. J. Immunol. 181: 4742-4751.
55. van Beek, E. M., T. J. de Vries, L. Mulder, T. Schoenmaker, K. A. Hoeben, T. Matozaki, G. E. Langenbach, G. Kraal, V. Everts, and T. K. van den Berg. 2009. Inhibitory regulation of osteoclast bone resorption by signal regulatory protein alpha. FASEB J. 23: 4081-4090.
56. Nguyen, T. V., Y. Ke, E. E. Zhang, and G. S. Feng. 2006. Conditional deletion of Shp2 tyrosine phosphatase in thymocytes suppresses both pre-TCR and TCR signals. J. Immunol. 177: 5990-5996. (Pubitemid 44628812)
57. Orr, M. T., J. Wu, M. Fang, L. J. Sigal, P. Spee, T. Egebjerg, E. Dissen, S. Fossum, J. H. Phillips, and L. L. Lanier. 2010. Development and function of CD94-deficient natural killer cells. PLoS ONE 5: e15184.
58. Fang, M., M. T. Orr, P. Spee, T. Egebjerg, L. L. Lanier, and L. J. Sigal. 2011. CD94 is essential for NK cell-mediated resistance to a lethal viral disease. Immunity 34: 579-589.