Pivotal Advance: CEACAM1 is a negative coreceptor for the B cell receptor and promotes CD19-mediated adhesion of B cells in a PI3K-dependent manner

Journal of Leukocyte Biology

Volumn 86, Issue 2, 2009, Pages 205-218

  Lobo, Elizabeth O ^a   Zhang, Zhifang ^a   Shively, John E ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Apoptosis activation induced cell death; Cell aggregation; SHP 1

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; B LYMPHOCYTE RECEPTOR; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; CD19 ANTIGEN; IMMUNOGLOBULIN M ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE PHOSPHATASE SHP 1; TYROSINE; AUTOANTIBODY; CD66 ANTIGENS; CELL ADHESION MOLECULE; ENZYME INHIBITOR; LEUKOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; PTPN6 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL ADHESION; CELL AGGREGATION; CELL FUNCTION; CELL GROWTH; CLONE; CONTROLLED STUDY; DAUDI CELL; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; WILD TYPE; CELL CULTURE; CHEMISTRY; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVE SITE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANTIGENS, CD; ANTIGENS, CD19; APOPTOSIS; AUTOANTIBODIES; B-LYMPHOCYTES; CATALYTIC DOMAIN; CELL ADHESION; CELL ADHESION MOLECULES; CELL LINE, TUMOR; CELLS, CULTURED; DOWN-REGULATION; ENZYME INHIBITORS; HUMANS; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION;

EID: 69449100854     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0109037     Document Type: Article

References (72)

1. Beauchemin, N., Draber, P., Dveksler, G., Gold, P., Gray-Owen, S., Grunert, F., Hammarstrom, S., Holmes, K. V., Karlsson, A., Kuroki, M., Lin, S. H., Lucka, L., Najjar, S. M., Neumaier, M., Obrink, B., Shively, J. E., Skubitz, K. M., Stanners, C. P., Thomas, P., Thompson, J. A., Virji, M., von Kleist, S., Wagener, C., Watt, S., Zimmermann, W. (1999) Redefined nomenclature for members of the carcinoembryonic antigen family. Exp. Cell Res. 252, 243-249. (Pubitemid 29530255)
2. Barnett, T. R., Drake, L., Pickle II, W. (1993) Human biliary glycoprotein gene: characterization of a family of novel alternatively spliced RNAs and their expressed proteins. Mol. Cell. Biol. 13, 1273-1282.
3. Barnett, T., Zimmermann, W. (1990) Workshop report: proposed nomenclature for the carcinoembryonic antigen (CEA) gene family. Tumour Biol. 11, 59-63. (Pubitemid 20099947)
4. Chen, T., Zimmermann, W., Parker, J., Chen, I., Maeda, A., Bolland, S. (2001) Biliary glycoprotein (BGPa, CD66a, CEACAM1) mediates inhibitory signals. J. Leukoc. Biol. 70, 335-340. (Pubitemid 32751527)
5. Gray-Owen, S. D., Blumberg, R. S. (2006) CEACAM1: contact-dependent control of immunity. Nat. Rev. Immunol. 6, 433-446.
6. Nagaishi, T., Pao, L., Lin, S. H., Iijima, H., Kaser, A., Qiao, S. W., Chen, Z., Glickman, J., Najjar, S. M., Nakajima, A., Neel, B. G., Blumberg, R. S. (2006) SHP1 phosphatase-dependent T cell inhibition by CEACAM1 adhesion molecule isoforms. Immunity 25, 769-781. (Pubitemid 46107284)
7. Markel, G., Lieberman, N., Katz, G., Arnon, T. I., Lotem, M., Drize, O., Blumberg, R. S., Bar-Haim, E., Mader, R., Eisenbach, L., Mandelboim, O. (2002) CD66a interactions between human melanoma and NK cells: a novel class I MHC-independent inhibitory mechanism of cytotoxicity. J. Immunol. 168, 2803-2810. (Pubitemid 34211659)
8. Beauchemin, N., Kunath, T., Roitaille, J., Chow, B., Turbide, C., Daniels, E., Veillette, A. (1997) Association of biliary glycoprotein with protein tyrosine phosphatase SHP-1 in malignant colon epithelial cells. Oncogene 14, 783-790. (Pubitemid 27100022)
9. Chen, C. J., Shively, J. E. (2004) The cell-cell adhesion molecule carcinoembryonic antigen-related cellular adhesion molecule 1 inhibits IL-2 production and proliferation in human T cells by association with Src homology protein-1 and down-regulates IL-2 receptor. J. Immunol. 172, 3544-3552.
10. Pantelic, M., Kim, Y. J., Bolland, S., Chen, I., Shively, J., Chen, T. (2005) Neisseria gonorrhoeae kills carcinoembryonic antigen-related cellular adhesion molecule 1 (CD66a)-expressing human B cells and inhibits antibody production. Infect. Immun. 73, 4171-4179. (Pubitemid 40923159)
11. Chen, D., Iijima, H., Nagaishi, T., Nakajima, A., Russell, S., Raychowdhury, R., Morales, V., Rudd, C. E., Utku, N., Blumberg, R. S. (2004) Carcinoembryonic antigen-related cellular adhesion molecule 1 isoforms alternatively inhibit and costimulate human T cell function. J. Immunol. 172, 3535-3543. (Pubitemid 38337934)
12. Greicius, G., Severinson, E., Beauchemin, N., Obrink, B., Singer, B. B. (2003) CEACAM1 is a potent regulator of B cell receptor complex-induced activation. J. Leukoc. Biol. 74, 126-134. (Pubitemid 38040445)
13. Racila, E., Hsueh, R., Marches, R., Tucker, T. F., Krammer, P. H., Scheuermann, R. H., Uhr, J. W. (1996) Tumor dormancy and cell signaling: anti-μ-induced apoptosis in human B-lymphoma cells is not caused by an APO-1-APO-1 ligand interaction. Proc. Natl. Acad. Sci. USA 93, 2165-2168. (Pubitemid 26079899)
14. Marches, R., Racila, E., Tucker, T. F., Picker, L., Mongini, P., Hsueh, R., Vitetta, E. S., Scheuermann, R. H., Uhr, J. W. (1995) Tumor dormancy and cell signaling-III: role of hypercrosslinking of IgM and CD40 on the induction of cell cycle arrest and apoptosis in B lymphoma cells. Ther. Immunol. 2, 125-136. (Pubitemid 26298044)
15. Pani, G., Kozlowski, M., Cambier, J. C., Mills, G. B., Siminovitch, K. A. (1995) Identification of the tyrosine phosphatase PTP1C as a B cell antigen receptor-associated protein involved in the regulation of B cell signaling. J. Exp. Med. 181, 2077-2084.
16. Adachi, T., Wienands, J., Wakabayashi, C., Yakura, H., Reth, M., Tsubata, T. (2001) SHP-1 requires inhibitory co-receptors to down-modulate B cell antigen receptor-mediated phosphorylation of cellular substrates. J. Biol. Chem. 276, 26648-26655. (Pubitemid 37412888)
17. Kelm, S., Gerlach, J., Brossmer, R., Danzer, C. P., Nitschke, L. (2002) The ligand-binding domain of CD22 is needed for inhibition of the B cell receptor signal, as demonstrated by a novel human CD22-specific inhibitor compound. J. Exp. Med. 195, 1207-1213. (Pubitemid 34517147)
18. D'Ambrosio, D., Hippen, K. L., Minskoff, S. A., Mellman, I., Pani, G., Siminovitch, K. A., Cambier, J. C. (1995) Recruitment and activation of PTP1C in negative regulation of antigen receptor signaling by Fc γ RIIB1. Science 268, 293-297.
19. Li, D. H., Tung, J. W., Tarner, I. H., Snow, A. L., Yukinari, T., Ngernmaneepothong, R., Martinez, O. M., Parnes, J. R. (2006) CD72 downmodulates BCR-induced signal transduction and diminishes survival in primary mature B lymphocytes. J. Immunol. 176, 5321-5328.
20. Adachi, T., Flaswinkel, H., Yakura, H., Reth, M., Tsubata, T. (1998) The B cell surface protein CD72 recruits the tyrosine phosphatase SHP-1 upon tyrosine phosphorylation. J. Immunol. 160, 4662-4665. (Pubitemid 28215297)
21. Eeva, J., Pelkonen, J. (2004) Mechanisms of B cell receptor induced apoptosis. Apoptosis 9, 525-531. (Pubitemid 39158628)
22. Booth, J. W., Telio, D., Liao, E. H., McCaw, S. E., Matsuo, T., Grinstein, S., Gray-Owen, S. D. (2003) Phosphatidylinositol 3-kinases in carcinoembryonic antigen-related cellular adhesion molecule-mediated internalization of Neisseria gonorrhoeae. J. Biol. Chem. 278, 14037-14045. (Pubitemid 36799948)
23. Yu, Q., Chow, E. M., Wong, H., Gu, J., Mandelboim, O., Gray-Owen, S. D., Ostrowski, M. A. (2006) CEACAM1 (CD66a) promotes human monocyte survival via a phosphatidylinositol 3-kinase- and AKT-dependent pathway. J. Biol. Chem. 281, 39179-39193. (Pubitemid 46041878)
24. Mizuno, K., Tagawa, Y., Mitomo, K., Arimura, Y., Hatano, N., Katagiri, T., Ogimoto, M., Yakura, H. (2000) Src homology region 2 (SH2) domain-containing phosphatase-1 dephosphorylates B cell linker protein/SH2 domain leukocyte protein of 65 kDa and selectively regulates c-Jun NH2-terminal kinase activation in B cells. J. Immunol. 165, 1344-1351. (Pubitemid 30604564)
25. Mizuno, K., Tagawa, Y., Mitomo, K., Watanabe, N., Katagiri, T., Ogimoto, M., Yakura, H. (2002) Src homology region 2 domain-containing phosphatase 1 positively regulates B cell receptor-induced apoptosis by modulating association of B cell linker protein with Nck and activation of c-Jun NH2-terminal kinase. J. Immunol. 169, 778-786. (Pubitemid 34753433)
26. Cuevas, B., Lu, Y., Watt, S., Kumar, R., Zhang, J., Siminovitch, K. A., Mills, G. B. (1999) SHP-1 regulates Lck-induced phosphatidylinositol 3-kinase phosphorylation and activity. J. Biol. Chem. 274, 27583-27589. (Pubitemid 129527805)
27. Cuevas, B. D., Lu, Y., Mao, M., Zhang, J., LaPushin, R., Siminovitch, K., Mills, G. B. (2001) Tyrosine phosphorylation of p85 relieves its inhibitory activity on phosphatidylinositol 3-kinase. J. Biol. Chem. 276, 27455-27461. (Pubitemid 37410663)
28. Smith, S. H., Rigley, K. P., Callard, R. E. (1991) Activation of human B cells through the CD19 surface antigen results in homotypic adhesion by LFA-1-dependent and -independent mechanisms. Immunology 73, 293-297.
29. Fujimoto, M., Poe, J. C., Hasegawa, M., Tedder, T. F. (2000) CD19 regulates intrinsic B lymphocyte signal transduction and activation through a novel mechanism of processive amplification. Immunol. Res. 22, 281-298. (Pubitemid 32382241)
30. Gold, M. R., Ingham, R. J., McLeod, S. J., Christian, S. L., Scheid, M. P., Duronio, V., Santos, L., Matsuuchi, L. (2000) Targets of B-cell antigen receptor signaling: the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase-3 signaling pathway and the Rap1 GTPase. Immunol. Rev. 176, 47-68. (Pubitemid 30703319)
31. Carter, R. H., Wang, Y., Brooks, S. (2002) Role of CD19 signal transduction in B cell biology. Immunol. Res. 26, 45-54. (Pubitemid 35177483)
32. Sato, S., Steeber, D. A., Jansen, P. J., Tedder, T. F. (1997) CD19 expression levels regulate B lymphocyte development: human CD19 restores normal function in mice lacking endogenous CD19. J. Immunol. 158, 4662-4669. (Pubitemid 127483784)
33. Maloney, M. D., Lingwood, C. A. (1994) CD19 has a potential CD77 (globotriaosyl ceramide)-binding site with sequence similarity to verotoxin B-subunits: implications of molecular mimicry for B cell adhesion and enterohemorrhagic Escherichia coli pathogenesis. J. Exp. Med. 180, 191-201. (Pubitemid 24181068)
34. Kansas, G. S., Tedder, T. F. (1991) Transmembrane signals generated through MHC class II, CD19, CD20, CD39, and CD40 antigens induce LFA-1-dependent and independent adhesion in human B cells through a tyrosine kinase-dependent pathway. J. Immunol. 147, 4094-4102.
35. Rojas, M., Fuks, A., Stanners, C. P. (1990) Biliary glycoprotein, a member of the immunoglobulin supergene family, functions in vitro as a Ca2(+)-dependent intercellular adhesion molecule. Cell Growth Differ. 1, 527-533.
36. Oikawa, S., Kuroki, M., Matsuoka, Y., Kosaki, G., Nakazato, H. (1992) Homotypic and heterotypic Ca(++)-independent cell adhesion activities of biliary glycoprotein, a member of carcinoembryonic antigen family, expressed on CHO cell surface. Biochem. Biophys. Res. Commun. 186, 881-887.
37. Teixeira, A. M., Fawcett, J., Simmons, D. L., Watt, S. M. (1994) The N-domain of the biliary glycoprotein (BGP) adhesion molecule mediates homotypic binding: domain interactions and epitope analysis of BGPc. Blood 84, 211-219. (Pubitemid 24193823)
38. Kaptein, J. S., Lin, C. K., Wang, C. L., Nguyen, T. T., Kalunta, C. I., Park, E., Chen, F. S., Lad, P. M. (1996) Anti-IgM-mediated regulation of c-myc and its possible relationship to apoptosis. J. Biol. Chem. 271, 18875-18884. (Pubitemid 26322760)
39. Marches, R., Hsueh, R., Uhr, J. W. (1999) Cancer dormancy and cell signaling: induction of p21(waf1) initiated by membrane IgM engagement increases survival of B lymphoma cells. Proc. Natl. Acad. Sci. USA 96, 8711-8715. (Pubitemid 29354856)
40. Carey, G. B., Scott, D. W. (2001) Role of phosphatidylinositol 3-kinase in anti-IgM- and anti-IgD-induced apoptosis in B cell lymphomas. J. Immunol. 166, 1618-1626. (Pubitemid 32114642)
41. Padmore, L., Radda, G. K., Knox, K. A. (1996) Wortmannin-mediated inhibition of phosphatidylinositol 3-kinase activity triggers apoptosis in normal and neoplastic B lymphocytes which are in cell cycle. Int. Immunol. 8, 585-594. (Pubitemid 26115874)
42. Curnock, A. P., Knox, K. A. (1998) LY294002-mediated inhibition of phosphatidylinositol 3-kinase activity triggers growth inhibition and apoptosis in CD40-triggered Ramos-Burkitt lymphoma B cells. Cell. Immunol. 187, 77-87.
43. Nittka, S., Gunther, J., Ebisch, C., Erbersdobler, A., Neumaier, M. (2004) The human tumor suppressor CEACAM1 modulates apoptosis and is implicated in early colorectal tumorigenesis. Oncogene 23, 9306-9313. (Pubitemid 40069663)
44. Graves, J. D., Draves, K. E., Craxton, A., Saklatvala, J., Krebs, E. G., Clark, E. A. (1996) Involvement of stress-activated protein kinase and p38 mitogen-activated protein kinase in mIgM-induced apoptosis of human B lymphocytes. Proc. Natl. Acad. Sci. USA 93, 13814-13818. (Pubitemid 26424203)
45. Gururajan, M., Chui, R., Karuppannan, A. K., Ke, J., Jennings, C. D., Bondada, S. (2005) c-Jun N-terminal kinase (JNK) is required for survival and proliferation of B-lymphoma cells. Blood 106, 1382-1391. (Pubitemid 41129605)
46. Berard, M., Mondiere, P., Casamayor-Palleja, M., Hennino, A., Bella, C., Defrance, T. (1999) Mitochondria connects the antigen receptor to effector caspases during B cell receptor-induced apoptosis in normal human B cells. J. Immunol. 163, 4655-4662. (Pubitemid 29501225)
47. Bouchon, A., Krammer, P. H., Walczak, H. (2000) Critical role for mitochondria in B cell receptor-mediated apoptosis. Eur. J. Immunol. 30, 69-77. (Pubitemid 30011767)
48. Koncz, G., Bodor, C., Kovesdi, D., Gati, R., Sarmay, G. (2002) BCR mediated signal transduction in immature and mature B cells. Immunol. Lett. 82, 41-49. (Pubitemid 34468033)
49. Gauld, S. B., Blair, D., Moss, C. A., Reid, S. D., Harnett, M. M. (2002) Differential roles for extracellularly regulated kinase-mitogen-activated protein kinase in B cell antigen receptor-induced apoptosis and CD40-mediated rescue of WEHI-231 immature B cells. J. Immunol. 168, 3855-3864. (Pubitemid 34298387)
50. Lee, J. R., Koretzky, G. A. (1998) Extracellular signal-regulated kinase-2, but not c-Jun NH2-terminal kinase, activation correlates with surface IgM-mediated apoptosis in the WEHI 231 B cell line. J. Immunol. 161, 1637-1644.
51. Richards, J. D., Dave, S. H., Chou, C. H., Mamchak, A. A., DeFranco, A. L. (2001) Inhibition of the MEK/ERK signaling pathway blocks a subset of B cell responses to antigen. J. Immunol. 166, 3855-3864.
52. Kondo, E., Harashima, A., Takabatake, T., Takahashi, H., Matsuo, Y., Yoshino, T., Orita, K., Akagi, T. (2003) NF-ATc2 induces apoptosis in Burkitt's lymphoma cells through signaling via the B cell antigen receptor. Eur. J. Immunol. 33, 1-11. (Pubitemid 36157637)
53. Nitschke, L., Carsetti, R., Ocker, B., Kohler, G., Lamers, M. C. (1997) CD22 is a negative regulator of B-cell receptor signaling. Curr. Biol. 7, 133-143. (Pubitemid 27155622)
54. Huber, M., Izzi, L., Grondin, P., Houde, C., Kunath, T., Veillette, A., Beauchemin, N. (1999) The carboxyl-terminal region of biliary glycoprotein controls its tyrosine phosphorylation and association with proteintyrosine phosphatases SHP-1 and SHP-2 in epithelial cells. J. Biol. Chem. 274, 335-344. (Pubitemid 29035067)
55. Izzi, L., Turbide, C., Houde, C., Kunath, T., Beauchemin, N. (1999) cis-Determinants in the cytoplasmic domain of CEACAM1 responsible for its tumor inhibitory function. Oncogene 18, 5563-5572. (Pubitemid 29481503)
56. Chen, T., Zimmermann, W., Parker, J., Chen, I., Maeda, A., Bolland, S. (2001) Biliary glycoprotein (BGPa, CD66a, CEACAM1) mediates inhibitory signals. J. Leukoc. Biol. 70, 335-340. (Pubitemid 32751527)
57. Lub, M., van Kooyk, Y., van Vliet, S. J., Figdor, C. G. (1997) Dual role of the actin cytoskeleton in regulating cell adhesion mediated by the integrin lymphocyte function-associated molecule-1. Mol. Biol. Cell 8, 341-351. (Pubitemid 27097948)
58. Schumann, D., Chen, C. J., Kaplan, B., Shively, J. E. (2001) Carcinoembryonic antigen cell adhesion molecule 1 directly associates with cytoskeleton proteins actin and tropomyosin. J. Biol. Chem. 276, 47421-47433. (Pubitemid 37373124)
59. Tsubata, T., Wienands, J. (2001) B cell signaling. Introduction. Int. Rev. Immunol. 20, 675-678.
60. Mueller, K. L., Daniels, M. A., Felthauser, A., Kao, C., Jameson, S. C., Shimizu, Y. (2004) Cutting edge: LFA-1 integrin-dependent T cell adhesion is regulated by both Ag specificity and sensitivity. J. Immunol. 173, 2222-2226. (Pubitemid 39063074)
61. Greicius, G., Tamosiunas, V., Severinson, E. (1998) Assessment of the role of leucocyte function-associated antigen-1 in homotypic adhesion of activated B lymphocytes. Scand. J. Immunol. 48, 642-650. (Pubitemid 28552988)
62. Dang, L. H., Rock, K. L. (1991) Stimulation of B lymphocytes through surface Ig receptors induces LFA-1 and ICAM-1-dependent adhesion. J. Immunol. 146, 3273-3279.
63. Otipoby, K. L., Draves, K. E., Clark, E. A. (2001) CD22 regulates B cell receptor-mediated signals via two domains that independently recruit Grb2 and SHP-1. J. Biol. Chem. 276, 44315-44322. (Pubitemid 37384006)
64. Poe, J. C., Haas, K. M., Uchida, J., Lee, Y., Fujimoto, M., Tedder, T. F. (2004) Severely impaired B lymphocyte proliferation, survival, and induction of the c-Myc:Cullin 1 ubiquitin ligase pathway resulting from CD22 deficiency on the C57BL/6 genetic background. J. Immunol. 172, 2100-2110. (Pubitemid 38182355)
65. Bokhoven, M., Stephen, S. L., Knight, S., Gevers, E. F., Robinson, I. C., Takeuchi, Y., Collins, M. K. (2009) Insertional gene activation by lentiviral and γ retroviral vectors. J. Virol. 83, 283-294.
66. Poy, M. N., Ruch, R. J., Fernstrom, M. A., Okabayashi, Y., Najjar, S. M. (2002) Shc and CEACAM1 interact to regulate the mitogenic action of insulin. J. Biol. Chem. 277, 1076-1084. (Pubitemid 34968853)
67. Obrink, B. (1997) CEA adhesion molecules: multifunctional proteins with signal-regulatory properties. Curr. Opin. Cell Biol. 9, 616-626.
68. Hauck, C. R., Gulbins, E., Lang, F., Meyer, T. F. (1999) Tyrosine phosphatase SHP-1 is involved in CD66-mediated phagocytosis of Opa52-expressing Neisseria gonorrhoeae. Infect. Immun. 67, 5490-5494. (Pubitemid 29455333)
69. Otero, D. C., Anzelon, A. N., Rickert, R. C. (2003) CD19 function in early and late B cell development: I. Maintenance of follicular and marginal zone B cells requires CD19-dependent survival signals. J. Immunol. 170, 73-83.
70. Jackson, T., Van Exel, C., Reagans, K., Verret, R., Maloney, M. (2001) Comparison of adhesion mechanisms and surface protein expression in CD77-positive and CD77-negative Burkitt's lymphoma cells. Cell. Mol. Biol. (Noisy-le-grand) 47, 1195-1200.
71. Alahari, S. K., Reddig, P. J., Juliano, R. L. (2002) Biological aspects of signal transduction by cell adhesion receptors. Int. Rev. Cytol. 220, 145-184. (Pubitemid 34988797)
72. Singer, B. B., Scheffrahn, I., Obrink, B. (2000) The tumor growth-inhibiting cell adhesion molecule CEACAM1 (C-CAM) is differently expressed in proliferating and quiescent epithelial cells and regulates cell proliferation. Cancer Res. 60, 1236-1244. (Pubitemid 30151990)