Cloning of rhesus monkey LILRs*
Corresponding Author
I.I. Slukvin
Department of Pathology and Laboratory Medicine, University of Wisconsin, Madison, WI, USA
Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
*Dr Igor I. Slukvin, MD, PhD Department of Pathology and Laboratory Medicine Wisconsin National Primate Research Center University of Wisconsin 1220 Capitol Court Madison, WI 53715 USA Tel: 1 608 263 0058 Fax:1 608 265 8984 e-mail: [email protected]Search for more papers by this authorR.L. Grendell
Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
Search for more papers by this authorD.S. Rao
Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
Search for more papers by this authorA.L. Hughes
Department of Biological Sciences, University of South Carolina, Columbia, SC, USA
Search for more papers by this authorT.G. Golos
Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
Department of Obstetrics and Gynecology, University of Wisconsin, Madison, WI, USA
Search for more papers by this authorCorresponding Author
I.I. Slukvin
Department of Pathology and Laboratory Medicine, University of Wisconsin, Madison, WI, USA
Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
*Dr Igor I. Slukvin, MD, PhD Department of Pathology and Laboratory Medicine Wisconsin National Primate Research Center University of Wisconsin 1220 Capitol Court Madison, WI 53715 USA Tel: 1 608 263 0058 Fax:1 608 265 8984 e-mail: [email protected]Search for more papers by this authorR.L. Grendell
Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
Search for more papers by this authorD.S. Rao
Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
Search for more papers by this authorA.L. Hughes
Department of Biological Sciences, University of South Carolina, Columbia, SC, USA
Search for more papers by this authorT.G. Golos
Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA
Department of Obstetrics and Gynecology, University of Wisconsin, Madison, WI, USA
Search for more papers by this authorSupported by NIH grants HD44067, HD37120, HD34215 and RR00167.
Abstract
Leukocyte Ig-like receptors (LILRs) are a family of receptors that have inhibitory and activating functions and widely expressed by lymphoid and myeloid cells. Here we report the identification of the rhesus monkey LILRs by screening of rhesus spleen and decidua cDNA libraries and RT-PCR cloning. We obtained eight different full-length clones with structural and functional diversity similar to human LILRs, including LILRs with immunoreceptor tyrosine-based inhibitory motifs, LILRs with truncated cytoplasmic tails containing positively charged arginine residues in the transmembrane domain, and putative soluble receptors lacking transmembrane or cytoplasmic domains. Characterization of rhesus LILRs will facilitate use of this non-human primate model for the study of the functional role(s) of LILRs, including immune regulation through interaction with non-classical MHC class I molecules.
References
- 1 Arm JP, Nwankwo C, Austen KF. Molecular identification of a novel family of human Ig superfamily members that possess immunoreceptor tyrosine-based inhibition motifs and homology to the mouse gp49B1 inhibitory receptor. J Immunol 1997: 159: 2342–9.
- 2 Brown D, Trowsdale J, Allen R. The LILR family: modulators of innate and adaptive immune pathways in health and disease. Tissue Antigens 2004: 64: 215–25.
- 3 Fanger NA, Borges L, Cosman D. The leukocyte immunoglobulin-like receptors (LIRs): a new family of immune regulators. J Leukoc Biol 1999: 66: 231–6.
- 4 Canavez F, Young NT, Guethlein LA et al. Comparison of chimpanzee and human leukocyte Ig-like receptor genes reveals framework and rapidly evolving genes. J Immunol 2001: 167: 5786–94.
- 5 Cella M, Dohring C, Samaridis J et al. A novel inhibitory receptor (ILT3) expressed on monocytes, macrophages, and dendritic cells involved in antigen processing. J Exp Med 1997: 185: 1743–51.
- 6 Cosman D, Fanger N, Borges L et al. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 1997: 7: 273–82.
- 7 Samaridis J, Colonna M. Cloning of novel immunoglobulin superfamily receptors expressed on human myeloid and lymphoid cells – structural evidence for new stimulatory and inhibitory pathways. Eur J Immunol 1997: 27: 660–5.
- 8 Nakajima H, Samaridis J, Angman L et al. Human myeloid cells express an activating ILT receptor (ILT1) that associates with Fc receptor gamma-chain. J Immunol 1999: 162: 5–8.
- 9 Borges L, Kubin M, Kuhlman T. LIR9, an immunoglobulin-superfamily-activating receptor, is expressed as a transmembrane and as a secreted molecule. Blood 2003: 101: 1484–6. E-pub 2002 September 26.
- 10 Shiroishi M, Tsumoto K, Amano K et al. Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc Natl Acad Sci USA 2003: 100: 8856–61. E-pub 2003 July 9.
- 11 Allan DSJ, Colonna M, Lanier LL et al. Tetrameric complex of human histocompatibility leukocyte antigen (HLA) -G bind to peripheral blood myelomonocytic cells. J Exp Med 1999: 189: 1149–56.
- 12 Colonna M, Navarro F, Bellon T et al. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J Exp Med 1997: 186: 1809–18.
- 13 Bouteiller PL, Commentary. Major breakthrough in the HLA-G debate: occurrence of pregnancy in human depends on the HLA-G status of preimplantation embryos. Eur J Immunol 2002: 32: 309–10.
- 14 Fuzzi B, Rizzo R, Criscuoli L et al. HLA-G expression in early embryos is a fundamental prerequisite for the obtainment of pregnancy. Eur J Immunol 2002: 32: 311–5.
- 15 Golos TG. Nonhuman primate placental MHC expression: a model for exploring mechanisms of human maternal-fetal immune tolerance. Hum Immunol 2003: 64: 1102–9.
- 16 Ponte M, Cantoni C, Biassoni R et al. Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor. Proc Natl Acad Sci U S A 1999: 96: 5674–9.
- 17 Ristich V, Liang S, Zhang W et al. Tolerization of dendritic cells HLA-G. Eur J Immunol 2005: 35: 1133–42.
- 18 LeMaoult J, Zafaranloo K, Le Danff C et al. HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells. FASEB J 2005: 19: 662–4. E-pub 2005 January 24.
- 19 Slukvin II, Breburda EE, Golos TG. Dynamic changes in primate endometrial leukocyte populations: differential distribution of macrophages and natural killer cells at the rhesus monkey implantation site and in early pregnancy. Placenta 2004: 25: 297–307.
- 20 Chang CC, Ciubotariu R, Manavalan JS et al. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 2002: 3: 237–43. E-pub 2002 January 28.
- 21 Manavalan JS, Rossi PC, Vlad G et al. High expression of ILT3 and ILT4 is a general feature of tolerogenic dendritic cells Transpl Immunol 2003: 11: 245–58.
- 22 Penna G, Roncari A, Amuchastegui S et al. Expression of the inhibitory receptor ILT3 on dendritic cells is dispensable for induction of CD4+Foxp3+ regulatory T cells by 1,25-dihydroxyvitamin D3. Blood 2005: 106: 3490–7. E-pub 2005 July 19.
- 23 Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987: 4: 406–25.
- 24 Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986: 3: 418–26.
- 25 Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985: 39: 783–91.
