Crystal Structure of Myeloid Cell Activating Receptor Leukocyte Ig-like Receptor A2 (LILRA2/ILT1/LIR-7) Domain Swapped Dimer: Molecular Basis for Its Non-binding to MHC Complexes

Journal of Molecular Biology

Volumn 386, Issue 3, 2009, Pages 841-853

  Chen, Yong ^a,b   Gao, Feng ^a,c   Chu, Fuliang ^a   Peng, Hao ^a   Zong, Lili ^a,d   Liu, Yiwei ^a   Tien, Po ^a   Gao, George F ^a,b  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^d SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

crystal structure; domain swapping dimer; ILT1; LILRA2; MHC non binding

Indexed keywords

HLA G ANTIGEN; IMMUNOGLOBULIN RECEPTOR; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR A1; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR A2; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR A3; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR B1; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR B2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BONE MARROW CELL; CRYSTAL STRUCTURE; DIMERIZATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT;

EID: 59649124978     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.01.006     Document Type: Article

References (42)

1. Colonna M., Navarro F., Bellon T., Llano M., Garcia P., Samaridis J., et al. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med. 186 (1997) 1809-1818
2. Cosman D., Fanger N., Borges L., Kubin M., Chin W., Peterson L., and Hsu M.L. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7 (1997) 273-282
3. Saverino D., Fabbi M., Ghiotto F., Merlo A., Bruno S., Zarcone D., et al. The CD85/LIR-1/ILT2 inhibitory receptor is expressed by all human T lymphocytes and down-regulates their functions. J. Immunol. 165 (2000) 3742-3755
4. Willcox B.E., Thomas L.M., and Bjorkman P.J. Crystal structure of HLA-A2 bound to LIR-1, a host and viral major histocompatibility complex receptor. Nature Immunol. 4 (2003) 913-919
5. Willcox B.E., Thomas L.M., Chapman T.L., Heikema A.P., West Jr. A.P., and Bjorkman P.J. Crystal structure of LIR-2 (ILT4) at 1.8 Å: differences from LIR-1 (ILT2) in regions implicated in the binding of the human cytomegalovirus class I MHC homolog UL18. BMC Struct. Biol. 2 (2002) 6-15
6. Chapman T.L., Heikema A.P., West Jr. A.P., and Bjorkman P.J. Crystal structure and ligand binding properties of the D1D2 region of the inhibitory receptor LIR-1 (ILT2). Immunity 13 (2000) 727-736
7. Shiroishi M., Tsumoto K., Amano K., Shirakihara Y., Colonna M., Braud V.M., 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 100 (2003) 8856-8861
8. Young N.T., Waller E.C., Patel R., Roghanian A., Austyn J.M., and Trowsdale J. The inhibitory receptor LILRB1 modulates the differentiation and regulatory potential of human dendritic cells. Blood 111 (2008) 3090-3096
9. Lichterfeld M., Kavanagh D.G., Williams K.L., Moza B., Mui S.K., Miura T., et al. A viral CTL escape mutation leading to immunoglobulin-like transcript 4-mediated functional inhibition of myelomonocytic cells. J. Exp. Med. 204 (2007) 2813-2824
10. Shiroishi M., Kuroki K., Rasubala L., Tsumoto K., Kumagai I., Kurimoto E., et al. Structural basis for recognition of the nonclassical MHC molecule HLA-G by the leukocyte Ig-like receptor B2 (LILRB2/LIR2/ILT4/CD85d). Proc. Natl Acad. Sci. USA 103 (2006) 16412-16417
11. Yang Z., and Bjorkman P.J. Structure of UL18, a peptide-binding viral MHC mimic, bound to a host inhibitory receptor. Proc. Natl Acad. Sci. USA 105 (2008) 10095-10100
12. Shiroishi M., Kajikawa M., Kuroki K., Ose T., Kohda D., and Maenaka K. Crystal structure of the human monocyte-activating receptor, "Group 2" leukocyte Ig-like receptor A5 (LILRA5/LIR9/ILT11). J. Biol. Chem. 281 (2006) 19536-19544
13. Garner L.I., Salim M., Mohammed F., and Willcox B.E. Expression, purification, and refolding of the myeloid inhibitory receptor leukocyte immunoglobulin-like receptor-5 for structural and ligand identification studies. Protein Expr. Purif. 47 (2006) 490-497
14. Chen Y., Chu F., Gao F., Zhou B., and Gao G.F. Stability engineering, biophysical, and biological characterization of the myeloid activating receptor immunoglobulin-like transcript 1 (ILT1/LIR-7/LILRA2). Protein Expr. Purif. 56 (2007) 253-260
15. Nakajima H., Samaridis J., Angman L., and Colonna M. Human myeloid cells express an activating ILT receptor (ILT1) that associates with Fc receptor gamma-chain. J. Immunol. 162 (1999) 5-8
16. Tedla N., Bandeira-Melo C., Tassinari P., Sloane D.E., Samplaski M., Cosman D., et al. Activation of human eosinophils through leukocyte immunoglobulin-like receptor 7. Proc. Natl Acad. Sci. USA 100 (2003) 1174-1179
17. Sloane D.E., Tedla N., Awoniyi M., Macglashan Jr. D.W., Borges L., Austen K.F., and Arm J.P. Leukocyte immunoglobulin-like receptors: novel innate receptors for human basophil activation and inhibition. Blood 104 (2004) 2832-2839
18. Huynh O.A., Hampartzoumian T., Arm J.P., Hunt J., Borges L., Ahern M., et al. Down-regulation of leucocyte immunoglobulin-like receptor expression in the synovium of rheumatoid arthritis patients after treatment with disease-modifying anti-rheumatic drugs. Rheumatology (Oxford) 46 (2007) 742-751
19. Tedla N., Gibson K., McNeil H.P., Cosman D., Borges L., and Arm J.P. The co-expression of activating and inhibitory leukocyte immunoglobulin-like receptors in rheumatoid synovium. Am. J. Pathol. 160 (2002) 425-431
20. Allen R.L., Raine T., Haude A., Trowsdale J., and Wilson M.J. Leukocyte receptor complex-encoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J. Immunol. 167 (2001) 5543-5547
21. Liu Y., and Eisenberg D. 3D domain swapping: as domains continue to swap. Protein Sci. 11 (2002) 1285-1299
22. Bazan J.F. Structural design and molecular evolution of a cytokine receptor superfamily. Proc. Natl Acad. Sci. USA 87 (1990) 6934-6938
23. Foster C.E., Colonna M., and Sun P.D. Crystal structure of the human natural killer (NK) cell activating receptor NKp46 reveals structural relationship to other leukocyte receptor complex immunoreceptors. J. Biol. Chem. 278 (2003) 46081-46086
24. Rousseau F., Schymkowitz J.W., Wilkinson H.R., and Itzhaki L.S. Three-dimensional domain swapping in p13suc1 occurs in the unfolded state and is controlled by conserved proline residues. Proc. Natl Acad. Sci. USA 98 (2001) 5596-5601
25. Ding K., Louis J.M., and Gronenborn A.M. Insights into conformation and dynamics of protein GB1 during folding and unfolding by NMR. J. Mol. Biol. 335 (2004) 1299-1307
26. Borges L., Hsu M.L., Fanger N., Kubin M., and Cosman D. A family of human lymphoid and myeloid Ig-like receptors, some of which bind to MHC class I molecules. J. Immunol. 159 (1997) 5192-5196
27. Bennett M.J., Choe S., and Eisenberg D. Domain swapping: entangling alliances between proteins. Proc. Natl Acad. Sci. USA 91 (1994) 3127-3131
28. Bennett M.J., Schlunegger M.P., and Eisenberg D. 3D domain swapping: a mechanism for oligomer assembly. Protein Sci. 4 (1995) 2455-2468
29. Sanejouand Y.H. Domain swapping of CD4 upon dimerization. Proteins: Struct. Funct. Genet. 57 (2004) 205-212
30. Murray A.J., Lewis S.J., Barclay A.N., and Brady R.L. One sequence, two folds: a metastable structure of CD2. Proc. Natl Acad. Sci. USA 92 (1995) 7337-7341
31. Denisov A.Y., Sprules T., Fraser J., Kozlov G., and Gehring K. Heat-induced dimerization of BCL-xL through alpha-helix swapping. Biochemistry 46 (2007) 734-740
32. O'Neill J.W., Manion M.K., Maguire B., and Hockenbery D.M. BCL-XL dimerization by three-dimensional domain swapping. J. Mol. Biol. 356 (2006) 367-381
33. Srimathi T., Robbins S.L., Dubas R.L., Hasegawa M., Inohara N., and Park Y.C. Monomer/dimer transition of the caspase-recruitment domain of human Nod1. Biochemistry 47 (2008) 1319-1325
34. Chattopadhyay K., Ramagopal U.A., Brenowitz M., Nathenson S.G., and Almo S.C. Evolution of GITRL immune function: murine GITRL exhibits unique structural and biochemical properties within the TNF superfamily. Proc. Natl Acad. Sci. USA 105 (2008) 635-640
35. Nakajima H., Asai A., Okada A., Ping L., Hamajima F., Sata T., and Isobe K. Transcriptional regulation of ILT family receptors. J. Immunol. 171 (2003) 6611-6620
36. Janket M.L., DeRicco J.S., Borowski L., and Ayyavoo V. Human immunodeficiency virus (HIV-1) Vpr induced downregulation of NHE1 induces alteration in intracellular pH and loss of ERM complex in target cells. Virus Res. 126 (2007) 76-85
37. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
38. Navaza J. AMORE - an automated package for molecular replacement. Acta Crystallogr. A 50 (1994) 157-163
39. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60 (2004) 2126-2132
40. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54 (1998) 905-921
41. Collaborative Computing Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50 (1994) 760-763
42. Lovell S.C., Davis I.W., Arendall III W.B., de Bakker P.I., Word J.M., Prisant M.G., et al. Structure validation by Calpha geometry: phi,psi and Cbeta deviation. Proteins 50 (2003) 437-450