Essential, nonredundant role for the phosphoinositide 3-kinase p110δ in signaling by the B-cell receptor complex

Molecular and Cellular Biology

Volumn 22, Issue 24, 2002, Pages 8580-8591

  Jou, Shiann Tarng ^a,c   Carpino, Nick ^a   Takahashi, Yutaka ^a   Piekorz, Roland ^a   Chao, Jyh Rong ^a   Carpino, Neena ^a   Wang, Demin ^a,d   Ihle, James N ^a,b  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; B LYMPHOCYTE RECEPTOR; IMMUNOGLOBULIN M; ISOENZYME; MITOGENIC AGENT; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CALCIUM TRANSPORT; CELL FUNCTION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME SUBUNIT; GERMINAL CENTER; HUMORAL IMMUNITY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, T-INDEPENDENT; B-LYMPHOCYTES; CALCIUM; CELLS, CULTURED; FLOW CYTOMETRY; GENE TARGETING; GERMINAL CENTER; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOGLOBULINS; MACROMOLECULAR SUBSTANCES; MICE; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; STEM CELLS; T-LYMPHOCYTES;

ANIMALIA;

EID: 0037695593     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.22.24.8580-8591.2002     Document Type: Article

References (39)

1. Bi, L., I. Okabe, D. J. Bernard, and R. L. Nussbaum. 2002. Early embryonic lethality in mice deficient in the p110beta catalytic subunit of PI 3-kinase. Mamm. Genome 13:169-172.
2. Bi, L., I. Okabe, D. J. Bernard, A. Wynshaw-Boris, and R. L. Nussbaum. 1999. Proliferative defect and embryonic lethality in mice homozygous for a deletion in the p110alpha subunit of phosphoinositide 3-kinase. J. Biol. Chem. 274:10963-10968.
3. Buhl, A. M., C. M. Pleiman, R. C. Rickert, and J. C. Cambier. 1997. Qualitative regulation of B cell antigen receptor signaling by CD19: Selective requirement for PI3-kinase activation, inositol-1,4,5-trisphosphate production and Ca2+ mobilization. J. Exp. Med. 186:1897-1910.
4. Chen, W. S., P. Z. Xu, K. Gottlob, M. L. Chen, K. Sokol, T. Shiyanova, I. Roninson, W. Weng, R. Suzuki, K. Tobe, T. Kadowaki, and N. Hay. 2001. Growth retardation and increased apoptosis in mice with homozygous disruption of the Aktl gene. Genes Dev. 15:2203-2208.
5. Cho, H., J. Mu, J. K. Kim, J. L. Thorvaldsen, Q. Chu, E. B. Crenshaw III, K. H. Kaestner, M. S. Bartolomei, G. I. Shulman, and M. J. Birnbaum. 2001. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292:1728-1731.
6. Di Cristofano, A., P. Kotsi, Y. F. Peng, C. Cordon-Cardo, K. B. Elkon, and P. P. Pandolfi. 1999. Impaired Fas response and autoimmunity in Pten+/mice. Science 285:2122-2125.
7. Engel, P., L. J. Zhou, D. C. Ord, S. Sato, B. Koller, and T. F. Tedder. 1995. Abnormal B lymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity 3:39-50.
8. + thymoctyes. Nature 374:474-477.
9. Fruman, D. A., and L. C. Cantley. 2002. Phosphoinositide 3-kinase in immunological systems. Semin. Immunol. 14:7-18.
10. Fruman, D. A., R. E. Meyers, and L. C. Cantley. 1998. Phosphoinositide kinases. Annu. Rev. Biochem. 67:481-507.
11. Fruman, D. A., S. B. Snapper, C. M. Yballe, L. Davidson, J. Y. Yu, F. W. Alt, and L. C. Cantley. 1999. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85alpha. Science 283:393-397.
12. Hirsch, E., V. L. Katanaev, C. Garlanda, O. Azzolino, L. Pirola, L. Silengo, S. Sozzani, A. Mantovani, F. Altruda, and M. P. Wymann. 2000. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 287:1049-1053.
13. Ihle, J. N. 1994. The Janus kinase family and signaling through members of the cytokine receptor superfamily. Proc. Soc. Exp. Biol. Med. 206:268-272.
14. Ihle, J. N. 1996. Janus kinases in cytokine signalling. Philos. Trans. R. Soc. London B 351:159-166.
15. Kerner, J. D., M. W. Appleby, R. N. Mohr, S. Chien, D. J. Rawlings, C. R. Maliszewski, O. N. Witte, and R. M. Perlmutter. 1995. Impaired expansion of mouse B cell progenitors lacking Btk. Immunity 3:301-312.
16. Khan, W. N., F. W. Alt, R. M. Gerstein, B. A. Malynn, I. Larsson, G. Rathbun, L. Davidson, S. Muller, A. B. Kantor, and L. A. Herzenberg. 1995. Defective B cell development and function in Btk-deficient mice. Immunity 3:283-299.
17. Leitges, M., C. Schmedt, R. Guinamard, J. Davoust, S. Schaal, S. Stabel, and A. Tarakhovsky. 1996. Immunodeficiency in protein kinase cbeta-deficient mice. Science 273:788-791.
18. Minegishi, Y., J. Rohrer, E. Coustan-Smith, H. M. Lederman, R. Pappu, D. Campana, A. C. Chan, and M. E. Conley. 1999. An essential role for BLNK in human B cell development. Science 286:1954-1957.
19. Moriggl, R., D. J. Topham, S. Teglund, V. Sexl, C. McKay, D. Wang, A. Hoffmeyer, J. van Deursen, M. Y. Sangster, K. D. Bunting, G. C. Grosveld, and J. N. Ihle. 1999. Stat5 is required for IL-2 induced cell cycle progression of peripheral T cells. Immunity 10:249-259.
20. Okkenhaug, K., A. Bilancio, G. Farjot, H. Priddle, S. Sancho, E. Peskett, W. Pearce, S. E. Meek, A. Salpekar, M. D. Waterfield, A. J. Smith, and B. Vanhaesebroeck. 2002. Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science 297:1031-1034.
21. Pappu, R., A. M. Cheng, B. Li, Q. Gong, C. Chiu, N. Griffin, M. White, B. P. Sleckman, and A. C. Chan. 1999. Requirement for B cell linker protein (BLNK) in B cell development. Science 286:1949-1954.
22. Rawlings, D. J., D. C. Saffran, S. Tsukada, D. A. Largaespada, J. C. Grimaldi, L. Cohen, R. N. Mohr, J. F. Bazan, M. Howard, N. G. Copeland, N. A. Jenkins, and O. N. Witte. 1993. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science 261:358-361.
23. Rickert, R. C., K. Rajewsky, and J. Roes. 1995. Impairment of T-cell-dependent B-cell responses and B-1 cell development in CD19-deficient mice. Nature 376:352-355.
24. Schaeffer, E. M., J. Debnath, G. Yap, D. McVicar, X. C. Liao, D. R. Littman, A. Sher, H. E. Varmus, M. J. Lenardo, and P. L. Schwartzberg. 1999. Requirement for Tec kinases Rlk and Itk in T cell receptor signaling and immunity. Science 284:638-641.
25. Sun, Z., C. W. Arendt, W. Ellmeier, E. M. Schaeffer, M. J. Sunshine, L. Gandhi, J. Annes, D. Petrzilka, A. Kupfer, P. L. Schwartzberg, and D. R. Littman. 2000. PKC-theta is required for TCR-induced NF-kappaB activation in mature but not immature T lymphocytes. Nature 404:402-407.
26. Suzuki, H., Y. Terauchi, M. Fujiwara, S. Aizawa, Y. Yazaki, T. Kadowaki, and S. Koyasu. 1999. Xid-like immunodeficiency in mice with disruption of the p85alpha subunit of phosphoinositide 3-kinase. Science 283:390-392.
27. Tedford, K., L. Nitschke, I. Girkontaite, A. Charlesworth, G. Chan, V. Sakk, M. Barbacid, and K. D. Fischer. 2001. Compensation between Vav-1 and Vav-2 in B cell development and antigen receptor signaling. Nat. Immunol. 2:548-555.
28. Teglund, S., C. McKay, E. Schuetz, J. van Deursen, D. Stravopodis, D. Wang, M. Brown, S. Bodner, G. Grosveld, and J. N. Ihle. 1998. Stat5a and Stat5b proteins have essential and non-essential, or redundant, roles in cytokine responses. Cell 93:841-850.
29. Thomas, J. D., P. Sideras, C. I. Smith, I. Vorechovsky, V. Chapman, and W. E. Paul. 1993. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science 261:355-358.
30. Toker, A., and L. Cantley. 1997. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387:673-676.
31. Tsukada, S., D. C. Saffran, D. J. Rawlings, O. Parolini, R. C. Allen, I. Klisak, H. Kubagawa, T. Mohandas, S. Quan, J. W. Belmont, M. D. Cooper, M. E. Conley, and O. N. Witte. 1993. Deficient expression of a B-cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia. Cell 72:279-290.
32. Vanhaesebroeck, B., M. J. Welham, K. Kotani, R. Stein, P. H. Warne, M. J. Zvelebil, K. Higashi, S. Volinia, J. Downward, and M. D. Waterfield. 1997. P110delta, a novel phosphoinositide 3-kinase in leukocytes. Proc. Natl. Acad. Sci. USA 94:4330-4335.
33. Vetrie, D., I. Vorechovsky, P. Sideras, J. Holland, A. Davies, F. Flinter, L. Hammarstrom, C. Kinnon, R. Levinsky, M. Bobrow, C. I. E. Smith, and D. R. Bentley. 1993. The gene involved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases. Nature 361:226-233. (Erratum, 364:362.)
34. Wang, D., E. C. Boylin, Y. Minegishi, R. Wen, C. I. Smith, J. N. Ihle, and M. E. Conley. 2001. Variations in the human phospholipase Cgamma2 gene in patients with B-cell defects of unknown etiology. Immunogenetics 53:550-556.
35. Wang, D., J. Feng, R. Wen, J. C. Marine, M. Y. Sangster, E. Parganas, A. Hoffmeyer, C. W. Jackson, J. L. Cleveland, P. J. Murray, and J. N. Ihle. 2000. Phospholipase Cgamma2 is essential in the functions of B cell and several Fc receptors. Immunity 13:25-35.
36. Wang, D., D. Stravopodis, S. Teglund, J. Kitazawa, and J. N. Ihle. 1996. Naturally occurring dominant negative variants of Stat5. Mol. Cell. Biol. 16:6141-6148.
37. Yamazaki, T., K. Takeda, K. Gotoh, H. Takeshima, S. Akira, and T. Kurosaki. 2002. Essential immunoregulatory role for BCAP in B cell development and function. J. Exp. Med. 195:535-545.
38. Zang, H., K. Sato, H. Nakajima, C. McKay, P. A. Ney, and J. N. Ihle. 2001. The distal region and receptor tyrosines of the Epo receptor are non-essential for in vivo erythropoiesis. EMBO J. 20:3156-3166.
39. Zhang, R., F. W. Alt, L. Davidson, S. H. Orkin, and W. Swat. 1995. Defective signalling through the T- and B-cell antigen receptors in lymphoid cells lacking the vav proto-oncogene. Nature 374:470-473.