Homophilic adhesion of human CEACAM1 involves N-terminal domain interactions: Structural analysis of the binding site

Blood

Volumn 98, Issue 5, 2001, Pages 1469-1479

  Watt, Suzanne M ^{a,b,c,d,e,f,g,h}   Teixeira, Ana M ^{a,b,c,d,e,f,g}   Zhou, Guang Qian ^{a,b,c,d,e,f,g}   Doyonnas, Regis ^{a,b,c,d,e,f,g}   Zhang, Youyi ^{a,b,c,d,e,f,g}   Grunert, Fritz ^{a,b,c,d,e,f,g}   Blumberg, Richard S ^{a,b,c,d,e,f,g}   Kuroki, Motomu ^{a,b,c,d,e,f,g}   Skubitz, Keith M ^{a,b,c,d,e,f,g}   Bates, Paul A ^{a,b,c,d,e,f,g}  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c Genovac GmbH   (Germany)

^d HARVARD MEDICAL SCHOOL   (United States)

^e FUKUOKA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^g IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^h JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARCINOEMBRYONIC ANTIGEN; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; GENE PRODUCT; MUTANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; CORONAVIRUS; EPITHELIUM CELL; FEMALE; GENE CONTROL; GENE MUTATION; HAEMOPHILUS INFLUENZAE; HYDROPHOBICITY; IMMUNOGLOBULIN VARIABLE REGION; LEUKOCYTE; MOUSE; MULTIGENE FAMILY; MUTAGENESIS; MUTATIONAL ANALYSIS; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT;

EID: 0035469860     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.V98.5.1469     Document Type: Article

References (71)

1. Obrink B. CEA adhesion molecules: multifunctional proteins with signal-regulatory properties. Curr Opin Cell Biol. 1997;9:616-626.
2. Beauchemin N, Draber P, Dveksler G, et al. Redefined nomenclature for members of the carcinoembryonic antigen family. Exp Cell Res. 1999;252:243-249.
3. Watt SM, Sala-Newby G, Hoang T, et al. CD66 identifies a neutrophil-specific epitope within the hematopoietic system that is expressed by members of the carcinoembryonic antigen family of adhesion molecules. Blood. 1991;78:63-74.
4. Morales V, Crist A, Watt SM, et al. Regulation of human intestinal intraepithelial lymphocyte cytolytic function by biliary glycoprotein (CD66a). J Immunol. 1999;163:1363-1370.
5. Watt SM, Fawcett J, Murdoch SJ, et al. CD66 identifies the biliary glycoprotein (BGP) adhesion molecule: cloning, expression and adhesion functions of the BGPc splice variant. Blood. 1994;84:200-210.
6. ++ dependent intercellular adhesion molecule. Cell Growth Differ. 1990;1:527-533.
7. Teixeira AM, Fawcett J, Simmons DL, Watt SM. The N-domain of the biliary glycoprotein (BGP) adhesion molecule mediates homotypic binding: domain interactions and epitope analysis of BGPc. Blood. 1994;84:211-219.
8. Skubitz KM, Campbell KD, Skubitz APN. CD66a, CD66b, CD66c and CD66d each independently stimulate neutrophils. J Leukoc Biol. 1996;60:106-117.
9. Ergun S, Kilik N, Ziegeler G, et al. CEA-related cell adhesion molecule 1: a potent angiogenic factor and a major effector of vascular endothelial growth factor. Mol Cell. 2000;5:311-320.
10. Holmes KV, Dveksler G, Gagneten S, et al. Coronavirus receptor specificity. Adv Exp Med Biol. 1993;342:261-266.
11. Stocks SC, Kerr MA, Haslett C, Dransfield I. CD66-dependent neutrophil activation: a possible mechanism for vascular selectin-mediated regulation of neutrophil adhesion. J Leukoc Biol. 1995;58:40-48.
12. Kuijpers TW, Hoogerwerf M, van der Laan LJW, et al. CD66 non-specific cross-reacting antigens are involved in neutrophil adherence to cytokine activated endothelial cells. J Cell. Biol. 1992;118:457-466.
13. Virji M, Makepeace K, Ferguson DJP, Watt SM. Carcinoembryonic antigens (CD66) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic neisseriae. Mol Microbiol. 1996;22:941-950.
14. Virji M, Watt SM, Barker S, Makepeace K, Doyonnas R. The N-domain of the human CD66a adhesion molecule is a target for Opa proteins of Neisseria meningitidis and Neisseria gonorrhoeae. Mol Microbiol. 1996;22:929-939.
15. Bos MP, Grunert F, Belland RJ. Differential recognition of members of the carcinoembryonic antigen family by Opa variants of Neisseria gonorrhoeae. Infect Immun. 1997;65:2353-2361.
16. Chen T, Grunert F, Medina-Marino A, Gotschlich EC. Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J Exp Med. 1997;185:1557-1564.
17. Gray-Owen SD, Dehio C, Gaude A, Grunert F, Meyer TF. CD66 carcinoembryonic antigens mediate interactions between Opa-expressing Neisseria gonorrhoeae and human polymorphonuclear phagocytes. EMBO J. 1997;16:3435-3445.
18. Virji M, Evans D, Griffith J, et al. Carcinoembryonic antigens are targeted by diverse strains of typable and non-typable Haemophilus influenzae. Mol Microbiol. 2000;36:784-759.
19. Sippel CJ, Shen T, Perlmutter DH. Site-directed mutagenesis within an ectroplasmic ATPase consensus sequence abrogates the cell aggregating properties of the rat liver canalicular bile acid transporter/Ecto-ATPase/cell CAM 105 and carcinoembryonic antigen. J Biol Chem. 1996;271:33095-33104.
20. Wikstrom K, Kjellstrom G, Obrink B. Homophilic intercellular adhesion mediated by C-CAM is due to a domain 1-domain 1 reciprocal binding. Exp Cell Res. 1996;227:360-366.
21. Cheung PH, Luo W, Qiu Y, et al. Structure and function of C-CAM1. J Biol Chem. 1993;268:24303-24310.
22. Rojas M, DeMarte L, Screaton RA, Stanners CP. Radical differences in functions of closely related members of the human carcinoembryonic antigen gene family. Cell Growth Differ. 1996;7:655-662.
23. Zhou H, Fuks A, Alcaraz G, Bolling TJ, Stanners CP. Homophilic adhesion between Ig superfamily carcinoembryonic antigen molecules involves double reciprocal bonds. J Cell Biol. 1993;122:951-960.
24. Jones EY, Davis SJ, Williams AF, Harlos K. Stuart DI. Crystal structure at 2.8: a resolution of a soluble form of the cell adhesion molecule CD2. Nature. 1992;360:232-239.
25. Wang J-H, Smolyar A, Tan K, et al. Structure of a heterophilic adhesion complex between the human CD2 and CD58 (LFA-3) counterreceptors. Cell. 1999;97:791-803.
26. Sun Z-YJ, Dotsch V, Kim M, Li J, Reinherz EL, Wagner G. Functional glycan-free adhesion domain of human cell surface receptor CD58: design, production and NMR studies. EMBO J. 1999;18:2941-2949.
27. Ikemizu H, Sparks LM, Van der Merwe A, et al. Crystal structure of the CD2-binding domain of CD58 (lymphocyte function-associated antigen 3) at 1.8-A resolution. Proc Natl Acad Sci U S A. 1999;96:4289-4294.
28. Skubitz KM, Micklem K, van der Schoot E. CD66 and CD67 cluster workshop report. In: Schlossman SF, Boumsell L, Gilks W, et al, eds. Leucocyte Typing V. Oxford, United Kingdom: Oxford University Press; 1995:889-899.
29. Skubitz KM, Grunert F, Jantscheff P, Kuroki M, Skubitz APN. Summary of the CD66 cluster workshop. In: Kishimoto, ed. Leukocyte Typing VI. New York: Garland Publishing; 1997:992-1000.
30. -+ independent cell adhesion activities of biliary glycoprotein, a member of the carcinoembryonic antigen family, expressed on CHO cell surface. Biochem Biophys Res Commun. 1992;186:881-887.
31. Nagel G, Grunert F, Kuijpers TW, Watt SM, Thompson J, Zimmermann W. Genomic organisation, splice variants and expression of CGMI, a CD66-related member of the carcinoembryonic antigen gene family. Eur J Biochem. 1993;214:27-35.
32. Daniel S, Nagel G, Johnson JP, et al. Determination of the specificities of monoclonal antibodies recognizing members of the CEA family using a panel of transfectants. Int J Cancer. 1993;55:303-310.
33. Berling BF, Kolbinger F, Grunert F, et al. Cloning of a carinoembryonic antigen gene family member expressed by leukocytes of chronic-myeloid leukemia patients and bone marrow. Cancer Res. 1990;50:6534-6539.
34. + hematopoietic precursor cells with early myeloid and B-lymphoid cell phenotypes. Blood. 1993;82:2649-2663.
35. Higuchi R, Krummel B, Saiki RK. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and cDNA. Nucleic Acids Res. 1988;16:7351-7367.
36. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-410.
37. Wang J, Yan Y, Garrett TPJ, et al. Atomic structure of human CD4 containing two immunoglobulin-like domains. Nature. 1990;348:411-418.
38. Epp O, Lattman EE, Shiffer M, Huber R, Palm W. The molecular structure of a dimer composed of the variable portions of the Bence-Jones protein 1REI refined at 2.0 angstroms resolution. Biochemistry. 1975;353:4943-4952.
39. Driscoll PC, Cyster JG, Campbell ID, Williams AF. Structure of domain 1 of rat T lymphocyte CD2 antigen. Nature. 1991;353:762-765.
40. Wyss DF, Choi JS, Wagner G. Composition and sequence specific resonance assignments of the heterogeneous N-linked glycan in the 13.6 kDa adhesion domain of human CD2 as determined by NMR on the intact glycoprotein. Biochemistry. 1995;34:1622-1634.
41. Gerstein M, Levitt M. Using interactive dynamic programming to obtain accurate pairwise and multiple alignments of protein structure. Fourth International Conference on Intelligent Systems for Molecular Biology. Menlo Park, CA; 1996:59-67.
42. Bates PA, Sternberg MJE. Model building by comparison at CASP3: using expert knowledge and computer automation. Proteins. 1999;37 (suppl 3):47-54.
43. Lin S-H, Luo W, Earley K, Cheung P, Hixson DC. Structure and function of C-CAM1: effects of the cytoplasmic domain on cell aggregation. Biochem J. 1995;311:239-245.
44. Hunter I, Sawa H, Edlund M, Öbrink B. Evidence for regulated dimerization of cell-cell adhesion molecule (C-CAM) in epithelial cells. Biochem J. 1996;320:847-853.
45. Hunter I, Lindh M, Obrink B. Differential regulation of C-CAM isoforms in epithelial cells. J Cell Sci. 1994;107:1205-1216.
46. Oikawa S, Inusuka C, Kuroki M, Matsuoka Y, Kosaki G, Nakazato H. Cell adhesion of non-specific cross-reacting antigen (NCA) and carcinoembryonic antigen (CEA) expressed on CHO cell surface: homophilic and heterophilic adhesion. Biochem Biophys Res Commun. 1989;164:39-45.
47. Oikawa S, Inuzuka C, Kuroki M, et al. A specific heterotypic cell adhesion activity between members of the carcinoembryonic antigen family, W272 and NCA, is mediated by N-domains. J Biol Chem. 1991;266:7995-8001.
48. Oikawa S, Sugiyama M, Kuroki M, Kuroki M, Nakazato H. Extracellular N-domain alone can mediate specific heterophilic adhesion between members of the carcinoembryonic antigen family, CEACAM6 and CEACAM8. Biochim Biophys Res Commun. 2000;278:564-568.
49. Bates PA, Luo J, Sternberg MJE. A predicted three-dimensional structure for the carcinoembryonic antigen (CEA). FEBS Lett. 1992;301:207-214.
50. Skubitz KM, Campbell KD, Skubitz APN. Synthetic peptides of CD66a stimulate neutrophil adhesion to endothelial cells. J Immunol. 2000;164:4257-4264.
51. Wessner DR, Shick PC, Lu J-H, et al. Mutational analysis of the virus and monoclonal antibody binding sites in MHVR, the cellular receptor of the murine coronavirus mouse hepatitis virus strain A59. J Virol. 1998;72:1941-1948.
52. Bos MP, Hogan D, Belland RJ. Homologue scanning mutagenesis reveals CD66 receptor residues required for neisserial opa protein binding. J Exp Med. 1999;190:331-340.
53. Virji M, Evans D, Hadfield A, Grunert F, Teixeira AM, Watt SM. Critical determinants of host receptor targeting by Neisseria meningiditis and Neisseria gonorrhoeae: identification of Opa adhesiotopes on the N-domain of CD66 molecules. Mol Microbiol. 1999;34:538-548.
54. Popp A, Dehio C, Grunert F, Meyer TF, Gray-Owen SD. Molecular analysis of neisserial Opa protein interactions with the CEA family of receptors: identification of determinants contributing to the differential specificities of binding. Cell Microbiol. 1999;1:169-181.
55. Bos MP, Kuroki M, Krop-Watorek A, Hogan D, Belland RJ. CD66 receptor specificity exhibited by neisserial Opa variants is controlled by protein determinants in CD66 N-domains. Proc Natl Acad Sci U S A. 1998;95:9584-9589.
56. Chen T, Gotschlich EC. CGM1 antigen of neutrophils, a receptor of gonococcal opacity proteins. Proc Natl Acad Sci U S A. 1996;93:14851-14856.
57. Wang J, Gray-Owen SD, Knorre A, Meyer TF, Dehio C. Opa binding to cellular CD66 receptors mediates the transcellular traversal of Neisseria gonorrhoeae across polarized T84 epithelial cell monolayers. Mol Biol. 1998;30:657-671.
58. Muenzer P, Dehio C, Fujiwara T, Achtman M, Meyer TF, Gray-Owen SD. Carcinoembryonic antigen family receptor specificity of Neisseria meningiditis Opa variants influences adherence to and invasion of proinflammatory cytokine-activated endothelial cells. Infect Immun. 2000;68:3601-3607.
59. Springer TA. The sensation and regulation of interactions with the extracellular environment: the cell biology of lymphocyle adhesion receptors. Annu Rev Cell Biol. 1990;6:359-402.
60. Davis SJ, Ikemizu S, Wild MK, Van der Merwe PA. CD2 and the nature of protein interactions mediating cell-cell recognition. Immunol Rev. 1998;163:217-236.
61. Wang J, Springer TA. Structural specializations of immunoglobulin superfamily members for adhesion to integrins and viruses. Immunol Rev. 1998;163:197-215.
62. Taheri M, Saragovi U, Fuks A, Makkerh J, Mort J, Stanners CP. Self-recognition in the Ig superfamily: identification of precise subdomains in carcinoembryonic antigen required for intercellular adhesion. J Biol Chem. 2000;35:25935-25948.
63. Shapiro L, Fannon AM, Kwong PD, et al. Structural basis of cell-cell adhesion by cadherins. Nature. 1995;374:327-337.
64. Stanners CP, Fuks A. Properties of adhesion mediated by the human CEA family. In Stanners CP, ed. Cell adhesion and communication mediated by the CEA family. Amsterdam, The Netherlands: Harwood Academic Publishers; 1998:57-71.
65. Turbide C, Kunath T, Daniels E, Beauchemin N. Optimal ratios of biliary glycoprotein isoforms required for inhibition of colonic tumor growth. Cancer Res. 1997;57:2781-2788.
66. Stanners CP, DeMarte L, Rogas M, Gold P, Fuks A. Opposite functions for two classes of genes of the human carcinoembryonic antigen family. Tumor Biol. 1995;16:23-31.
67. Olsson H, Wikstrom K, Kjellstrom G, Obrink B. Cell adhesion activity of the short cyloplasmic domain isoform of C-Cam (C-CAM2) in CHO cells. FEBS Lett. 1995;1:51-56.
68. Edlund M, Blikstad I, Obrink B. Calmodulin binds to specific sequences in the cytoplasmic domain of C-CAM and down-regulates C-CAM self-association. J Biol Chem. 1996;271:1393-1399.
69. Edlund M, Gaardsvoll H, Bock E, Obrink B. Different isoforms and stock-specific variants of the cell adhesion molecule C-CAM (cell-CAM 105) in rat liver. Eur J Biochem. 1993;213:1109-1116.
70. Hunter I, Sigmundsson K, Beauchemin N, Obrink B. The cell adhesion molecule C-CAM is a substrate for tissue transglutaminase. FEBS Lett. 1998;425:141-144.
71. Stocks SC, Kerr MA. Neutrophil NCA-160 (CD66) is the major protein carrier of selectin binding carbohydrate groups Lewis X and sialyl Lewis X. Biochem Biophys Res Commun. 1993;195:478-483.