Emergence of the PI3-kinase pathway as a central modulator of normal and aberrant B cell differentiation

Current Opinion in Immunology

Volumn 23, Issue 2, 2011, Pages 178-183

  Baracho, G V ^a   Miletic, A V ^a   Omori, S A ^a   Cato, M H ^a   Rickert, R C ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD19 ANTIGEN; CELL PROTEIN; INTERLEUKIN 7 RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BCAP; PROTEIN KINASE B; PROTEIN PRECURSOR; PROTEIN TC21; PROTEIN TYROSINE PHOSPHATASE SHP; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG;

B LYMPHOCYTE DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HOMEOSTASIS; LYMPHOCYTE FUNCTION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; HOMEOSTASIS; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION;

EID: 79953112441     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2011.01.001     Document Type: Review

References (50)

1. Denley A., Kang S., Karst U., Vogt P.K. Oncogenic signaling of class I PI3K isoforms. Oncogene 2007, 27:2561-2574.
2. Kang S., Denley A., Vanhaesebroeck B., Vogt P.K. Oncogenic transformation induced by the p110beta-gamma, and -delta isoforms of class I phosphoinositide 3-kinase. Proc Natl Acad Sci U S A 2006, 103:1289-1294.
3. Carracedo A., Pandolfi P.P. The PTEN-PI3K pathway: of feedbacks and cross-talks. Oncogene 2008, 27:5527-5541.
4. Leslie N.R., Downes C.P. PTEN: the down side of PI 3-kinase signalling. Cell Signal 2002, 14:285-295.
5. Salmena L., Carracedo A., Pandolfi P.P. Tenets of PTEN tumor suppression. Cell 2008, 133:403-414.
6. Currie R.A., Walker K.S., Gray A., Deak M., Casamayor A., Downes C.P., Cohen P., Alessi D.R., Lucocq J. Role of phosphatidylinositol 3,4,5-trisphosphate in regulating the activity and localization of 3-phosphoinositide-dependent protein kinase-1. Biochem J 1999, 337(Pt 3):575-583.
7. Ramadani F., Bolland D.J., Garcon F., Emery J.L., Vanhaesebroeck B., Corcoran A.E., Okkenhaug K The PI3K isoforms p110{alpha} and p110{delta} are essential for pre-B cell receptor signaling and B cell development. Sci Signal 2010, 3:ra60.
8. Beer-Hammer S., Zebedin E., von Holleben M., Alferink J., Reis B., Dresing P., Degrandi D., Scheu S., Hirsch E., Sexl V., et al. The catalytic PI3K isoforms p110{gamma} and p110{delta} contribute to B cell development and maintenance, transformation, and proliferation. J Leukoc Biol 2010, 87:1083-1095.
9. Alcazar I., Marques M., Kumar A., Hirsch E., Wymann M., Carrera A.C., Barber D.F. Phosphoinositide 3 kinase {gamma} participates in T cell receptor induced T cell activation. J Exp Med 2007, 204:2977-2987.
10. Webb L.M.C., Vigorito E., Wymann M.P., Hirsch E., Turner M. Cutting edge: T cell development requires the combined activities of the p110{gamma} and p110{delta} catalytic isoforms of phosphatidylinositol 3-kinase. J Immunol 2005, 175:2783-2787.
11. Corcoran A.E., Smart F.M., Cowling R.J., Crompton T., Owen M.J., Venkitaraman A.R. The interleukin-7 receptor alpha chain transmits distinct signals for proliferation and differentiation during B lymphopoiesis. EMBO J 1996, 15:1924-1932.
12. Dengler H.S., Baracho G.V., Omori S.A., Bruckner S., Arden K.C., Castrillon D.H., DePinho R.A., Rickert R.C. Distinct functions for the transcription factor Foxo1 at various stages of B cell differentiation. Nat Immunol 2008, 9:1388-1398.
13. Ramaswamy S., Nakamura N., Sansal I., Bergeron L., Sellers W.R. A novel mechanism of gene regulation and tumor suppression by the transcription factor FKHR. Cancer Cell 2002, 2:81-91.
14. Schmidt M., Fernandez de Mattos S., van der Horst A., Klompmaker R., Kops G.J.P.L., Lam E.W.-F., Burgering B.M.T., Medema R.H. Cell cycle inhibition by Foxo forkhead transcription factors involves downregulation of cyclin D. Mol Cell Biol 2002, 22:7842-7852.
15. Medema R.H., Kops G.J., Bos J.L., Burgering B.M. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 2000, 404:782-787.
16. Amin R.H., Schlissel M.S. Foxo1 directly regulates the transcription of recombination-activating genes during B cell development. Nat Immunol 2008, 9:613-622.
17. Herzog S., Hug E., Meixlsperger S., Paik J.H., DePinho R.A., Reth M., Jumaa H. SLP-65 regulates immunoglobulin light chain gene recombination through the PI(3)K-PKB-Foxo pathway. Nat Immunol 2008, 9:623-631.
18. Hayashi K., Yamamoto M., Nojima T., Goitsuka R., Kitamura D. Distinct signaling requirements for Dmu selection, IgH allelic exclusion, pre-B cell transition, and tumor suppression in B cell progenitors. Immunity 2003, 18:825-836.
19. Aiba Y., Kameyama M., Yamazaki T., Tedder T.F., Kurosaki T. Regulation of B-cell development by BCAP and CD19 through their binding to phosphoinositide 3-kinase. Blood 2008, 111:1497-1503.
20. Okada T., Maeda A., Iwamatsu A., Gotoh K., Kurosaki T. BCAP: the tyrosine kinase substrate that connects B cell receptor to phosphoinositide 3-kinase activation. Immunity 2000, 13:817-827.
21. Lazorchak A.S., Liu D., Facchinetti V., Di Lorenzo A., Sessa W.C., Schatz D.G., Su B. Sin1-mTORC2 suppresses rag and il7r gene expression through Akt2 in B cells. Mol Cell 2010, 39:433-443.
22. Sparks C.A., Guertin D.A. Targeting mTOR: prospects for mTOR complex 2 inhibitors in cancer therapy. Oncogene 2010, 29:3733-3744.
23. Sarbassov D.D., Guertin D.A., Ali S.M., Sabatini D.M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307:1098-1101.
24. Cheng S., Hsia C.Y., Feng B., Liou M.-L., Fang X., Pandolfi P.P., Liou H.-C. BCR-mediated apoptosis associated with negative selection of immature B cells is selectively dependent on Pten. Cell Res 2009, 19:196-207.
25. Browne C.D., Del Nagro C.J., Cato M.H., Dengler H.S., Rickert R.C. Suppression of phosphatidylinositol 3,4,5-trisphosphate production is a key determinant of B cell anergy. Immunity 2009, 31:749-760.
26. Oak J.S., Chen J., Peralta R.Q., Deane J.A., Fruman D.A. The p85beta regulatory subunit of phosphoinositide 3-kinase has unique and redundant functions in B cells. Autoimmunity 2009, 42:447-458.
27. Rickert R.C., Rajewsky K., Roes J. Impairment of T-cell-dependent B-cell responses and B-1 cell development in CD19-deficient mice. Nature 1995, 376:352-355.
28. Engel P., Zhou L.J., Ord D.C., Sato S., Koller B., Tedder T.F. Abnormal B lymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity 1995, 3:39-50.
29. Okkenhaug K., Bilancio A., Farjot G., Priddle H., Sancho S., Peskett E., Pearce W., Meek S.E., Salpekar A., Waterfield M.D., et al. Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science 2002, 297:1031-1034.
30. Clayton E., Bardi G., Bell S.E., Chantry D., Downes C.P., Gray A., Humphries L.A., Rawlings D., Reynolds H., Vigorito E., et al. A crucial role for the p110{delta} subunit of phosphatidylinositol 3-kinase in B cell development and activation. J Exp Med 2002, 196:753-763.
31. Yamazaki T., Takeda K., Gotoh K., Takeshima H., Akira S., Kurosaki T. Essential immunoregulatory role for BCAP in B cell development and function. J Exp Med 2002, 195:535-545.
32. Delgado P., Cubelos B., Calleja E., Martinez-Martin N., Cipres A., Merida I., Bellas C., Bustelo X.R., Alarcon B. Essential function for the GTPase TC21 in homeostatic antigen receptor signaling. Nat Immunol 2009, 10:880-888.
33. Srinivasan L., Sasaki Y., Calado D.P., Zhang B., Paik J.H., DePinho R.A., Kutok J.L., Kearney J.F., Otipoby K.L., Rajewsky K. PI3 kinase signals BCR-dependent mature B cell survival. Cell 2009, 139:573-586.
34. Calamito M., Juntilla M.M., Thomas M., Northrup D.L., Rathmell J., Birnbaum M.J., Koretzky G., Allman D. Akt1 and Akt2 promote peripheral B-cell maturation and survival. Blood 2010, 115:4043-4050.
35. Patke A., Mecklenbrauker I., Erdjument-Bromage H., Tempst P., Tarakhovsky A. BAFF controls B cell metabolic fitness through a PKC{beta}- and Akt-dependent mechanism. J Exp Med 2006, 203:2551-2562.
36. Woodland R.T., Fox C.J., Schmidt M.R., Hammerman P.S., Opferman J.T., Korsmeyer S.J., Hilbert D.M., Thompson C.B. Multiple signaling pathways promote B lymphocyte stimulator dependent B-cell growth and survival. Blood 2008, 111:750-760.
37. Thomas J.D., Sideras P., Smith C.I., Vorechovsky I., Chapman V., Paul W.E. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science 1993, 261:355-358.
38. Rawlings D.J., Saffran D.C., Tsukada S., Largaespada D.A., Grimaldi J.C., Cohen L., Mohr R.N., Bazan J.F., Howard M., Copeland N.G., et al. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science 1993, 261:358-361.
39. Chen J., Limon J.J., Blanc C., Peng S.L., Fruman D.A. Foxo1 regulates marginal zone B-cell development. Eur J Immunol 2010, 40:1890-1896.
40. Suzuki A., Kaisho T., Ohishi M., Tsukio-Yamaguchi M., Tsubata T., Koni P.A., Sasaki T., Mak T.W., Nakano T. Critical roles of Pten in B cell homeostasis and immunoglobulin class switch recombination. J Exp Med 2003, 197:657-667.
41. Anzelon A.N., Wu H., Rickert R.C. Pten inactivation alters peripheral B lymphocyte fate and reconstitutes CD19 function. Nat Immunol 2003, 4:287-294.
42. Rolf J., Bell S.E., Kovesdi D., Janas M.L., Soond D.R., Webb L.M.C., Santinelli S., Saunders T., Hebeis B., Killeen N., et al. Phosphoinositide 3-kinase activity in T cells regulates the magnitude of the germinal center reaction. J Immunol 2010, 185:4042-4052.
43. Vigorito E., Bardi G., Glassford J., Lam E.W., Clayton E., Turner M. Vav-dependent and vav-independent phosphatidylinositol 3-kinase activation in murine B cells determined by the nature of the stimulus. J Immunol 2004, 173:3209-3214.
44. Omori S.A., Cato M.H., Anzelon-Mills A., Puri K.D., Shapiro-Shelef M., Calame K., Rickert R.C. Regulation of class-switch recombination and plasma cell differentiation by phosphatidylinositol 3-kinase signaling. Immunity 2006, 25:545-557.
45. Samuels Y., Wang Z., Bardelli A., Silliman N., Ptak J., Szabo S., Yan H., Gazdar A., Powell S.M., Riggins G.J., et al. High frequency of mutations of the PIK3CA gene in human cancers. Science 2004, 304. 554.
46. Miletic A.V., Anzelon-Mills A.N., Mills D.M., Omori S.A., Pedersen I.M., Shin D.-M., Ravetch J.V., Bolland S., Morse H.C., Rickert R.C. Coordinate suppression of B cell lymphoma by PTEN and SHIP phosphatases. J Exp Med 2010, 207:2407-2420.
47. Honigberg L.A., Smith A.M., Sirisawad M., Verner E., Loury D., Chang B., Li S., Pan Z., Thamm D.H., Miller R.A., et al. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci 2010, 107:13075-13080.
48. Lannutti B.J., Meadows S.A., Herman S.E.M., Kashishian A., Steiner B., Johnson A.J., Byrd J.C., Tyner J.W., Loriaux M.M., Deininger M., et al. CAL-101, a p110{delta} selective phosphatidylinositol-3-kinase inhibitor (PI3K) for the treatment of B cell malignancies inhibits PI3K signaling and cellular viability. Blood 2010, 117:591-594.
49. Doi T., Obayashi K., Kadowaki T., Fujii H., Koyasu S. PI3K is a negative regulator of IgE production. Int Immunol 2008, 20:499-508.
50. Zhang T.-t., Okkenhaug K., Nashed B.F., Puri K.D., Knight Z.A., Shokat K.M., Vanhaesebroeck B., Marshall A.J. Genetic or pharmaceutical blockade of p110[delta] phosphoinositide 3-kinase enhances IgE production. J Allergy Clin Immunol 2008, 122. 811-819, e812.