FOXO1 transcription factor: A critical effector of the PI3K-AKT axis in B-Cell development

International Reviews of Immunology

Volumn 33, Issue 2, 2014, Pages 146-157

  Szydłowski, Maciej ^a   Jabłońska, Ewa ^a   Juszczyński, Przemysław ^a  

^a INSTITUTE OF HEMATOLOGY AND TRANSFUSION MEDICINE   (Poland)

Author keywords

B cell development; FOXO1; PI3K AKT signaling

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHR;

B LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; HUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; SYSTEMATIC REVIEW;

ANIMALS; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; FORKHEAD TRANSCRIPTION FACTORS; GENE REGULATORY NETWORKS; HOMEOSTASIS; HUMANS; IMMUNE TOLERANCE; ONCOGENE PROTEIN V-AKT; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, INTERLEUKIN-7; SIGNAL TRANSDUCTION;

EID: 84896139490     PISSN: 08830185     EISSN: 15635244     Source Type: Journal    
DOI: 10.3109/08830185.2014.885022     Document Type: Review

References (72)

1. Rowland SL, Tuttle K, Torres RM, Pelanda R. Antigen and cytokine receptor signals guide the development of the naivemature B cell repertoire. Immunol Res 2013;55:231-240.
2. Okkenhaug K, Vanhaesebroeck B. PI3K in lymphocyte development, differentiation and activation. Nat Rev Immunol 2003;3:317-330. (Pubitemid 37328684)
3. Yamanashi Y, Kakiuchi T,Mizuguchi J, et al. Association of B cell antigen receptor with protein tyrosine kinase Lyn. Science 1991;251:192-194. (Pubitemid 21916867)
4. Aiba Y, Kameyama M, Yamazaki T, et al. Regulation of B-cell development by BCAP and CD19 through their binding to phosphoinositide 3-kinase. Blood 2008;111:1497-1503. (Pubitemid 351213438)
5. Hollander MC, Blumenthal GM, Dennis PA. PTEN loss in the continuum of common cancers, rare syndromes and mousemodels. Nat Rev Cancer 2011;11:289-301.
6. Miletic AV, Anzelon-Mills AN,Mills DM, et al. Coordinate suppression of B cell lymphoma by PTEN and SHIP phosphatases. J ExpMed 2010;207:2407-2420.
7. Ong CJ,Ming-Lum A, NodwellM, et al. Small-molecule agonists of SHIP1 inhibit the phosphoinositide 3-kinase pathway in hematopoietic cells. Blood 2007;110:1942-1949. (Pubitemid 47443908)
8. Kennah M, Yau TY, Nodwell M, et al. Activation of SHIP via a small molecule agonist kills multiple myeloma cells. Exp Hematol 2009;37:1274-1283.
9. Brazil DP, Hemmings BA. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem Sci 2001;26:657-664. (Pubitemid 33042488)
10. Alessi DR, James SR, Downes CP, et al. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol 1997;7:261-269. (Pubitemid 27176852)
11. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005;307:1098-1101. (Pubitemid 40262113)
12. Paradis S, Ruvkun G. Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev 1998;12:2488-2498. (Pubitemid 28406952)
13. Brunet A, Bonni A, ZigmondMJ, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999;96:857-868. (Pubitemid 29165088)
14. Kousteni S. FoxO1: amolecule for all seasons. J BoneMiner Res 2011;26:912-917.
15. Dejean AS,Hedrick SM, Kerdiles YM.Highly specialized role of Forkhead boxOtranscription factors in the immune system. Antioxid Redox Signal 2011;14:663-674.
16. Dijkers PF, Medema RH, Lammers JW, et al. Expression of the pro-apoptotic Bcl-2 family member Bimis regulated by the forkhead transcription factor FKHR-L1. Curr Biol 2000;10:1201-1204.
17. Dijkers PF, Medema RH, Pals C, et al. Forkhead transcription factor FKHR-L1 modulates cytokinedependent transcriptional regulation of p27(KIP1).Mol Cell Biol 2000;20:9138-9148. (Pubitemid 32246103)
18. Hurtz C, Hatzi K, Cerchietti L, et al. BCL6-mediated repression of p53 is critical for leukemia stem cell survival in chronicmyeloid leukemia. J ExpMed 2011;208:2163-2174.
19. Schmidt M, Fernandez de Mattos S, van der Horst A, et al. Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D.Mol Cell Biol 2002;22:7842-7852. (Pubitemid 35217295)
20. Tran H, Brunet A, Grenier JM, et al. DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 2002;296:530-534. (Pubitemid 34408672)
21. Yusuf I, Zhu X, Kharas MG, et al. Optimal B-cell proliferation requires phosphoinositide 3-kinasedependent inactivation of FOXO transcription factors. Blood 2004;104:784-787. (Pubitemid 38970574)
22. Kops GJ, Dansen TB, Polderman PE, et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 2002;419:316-321.
23. Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 2002;295:2450-2452. (Pubitemid 34270258)
24. Xin L, Lawson DA, Witte ON. The Sca-1 cell surface marker enriches for a prostate-regenerating cell subpopulation that can initiate prostate tumorigenesis. Proc Natl Acad Sci USA 2005;102:6942-6947. (Pubitemid 40675421)
25. Murayama K, Kimura T, Tarutani M, et al. Akt activation induces epidermal hyperplasia and proliferation of epidermal progenitors. Oncogene 2007;26:4882-4888. (Pubitemid 47093171)
26. Zhang J, Grindley JC, Yin T, et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 2006;441:518-522. (Pubitemid 44050154)
27. Yilmaz OH, Valdez R,Theisen BK, et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 2006;441:475-482. (Pubitemid 44050144)
28. Tothova Z, Kollipara R,Huntly BJ, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007;128:325-339. (Pubitemid 46137992)
29. Lin YC, Jhunjhunwala S, Benner C, et al. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat Immunol 2010;11:635-643.
30. Nutt SL, Kee BL. The transcriptional regulation of B cell lineage commitment. Immunity 2007;26:715-725. (Pubitemid 46908962)
31. Amin RH, Schlissel MS. Foxo1 directly regulates the transcription of recombination-activating genes during B cell development. Nat Immunol 2008;9:613-622. (Pubitemid 351712632)
32. Mansson R, Welinder E, Ahsberg J, et al. Positive intergenic feedback circuitry, involving EBF1 and FOXO1, orchestrates B-cell fate. Proc Natl Acad Sci USA 2012;109:21028-21033.
33. Zandi S,Mansson R, Tsapogas P, et al. EBF1 is essential for B-lineage priming and establishment of a transcription factor network in common lymphoid progenitors. J Immunol 2008;181:3364-3372.
34. Lin H, Grosschedl R. Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 1995;376:263-267.
35. Chen J, Yusuf I, Andersen HM, Fruman DA. FOXO transcription factors cooperate with delta EF1 to activate growth suppressive genes in B lymphocytes. J Immunol 2006;176:2711-2721.
36. Cobb BS, Smale ST. Ikaros-family proteins: in search of molecular functions during lymphocyte development. Curr TopMicrobiol Immunol 2005;290:29-47. (Pubitemid 40299559)
37. ReynaudD,Demarco IA, Reddy KL, et al. Regulation of B cell fate commitment and immunoglobulin heavy-chain gene rearrangements by Ikaros. Nat Immunol 2008;9:927-936.
38. Dengler HS, Baracho GV, Omori SA, et al. Distinct functions for the transcription factor Foxo1 at various stages of B cell differentiation. Nat Immunol 2008;9:1388-1398.
39. Alkhatib A,Werner M, Hug E, et al. FoxO1 induces Ikaros splicing to promote immunoglobulin gene recombination. J ExpMed 2012;209:395-406.
40. Peschon JJ, Morrissey PJ, Grabstein KH, et al. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J ExpMed 1994;180:1955-1960.
41. von Freeden-Jeffry U, Vieira P, Lucian LA, et al. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J ExpMed 1995;181:1519-1526.
42. Chow KT, Timblin GA, McWhirter SM, Schlissel MS. MK5 activates Rag transcription via Foxo1 in developing B cells. J ExpMed 2013;210:1621-1634.
43. Rolink AG, Winkler T, Melchers F, Andersson J. Precursor B cell receptor-dependent B cell proliferation and differentiation does not require the bone marrow or fetal liver environment. J Exp Med 2000;191:23-32.
44. Ochiai K,Maienschein-Cline M,Mandal M, et al. A self-reinforcing regulatory network triggered by limiting IL-7 activates pre-BCR signaling and differentiation. Nat Immunol 2012;13:300-307.
45. Tze LE, SchramBR,LamKP, et al.Basal immunoglobulin signaling activelymaintains developmental stage in immature B cells. PLoS Biol 2005;3:0463-0475. (Pubitemid 40605295)
46. Cheng S, Hsia CY, Feng B, et al. BCR-mediated apoptosis associated with negative selection of immature B cells is selectively dependent on Pten. Cell Res 2009;19:196-207.
47. Browne CD, Del Nagro CJ, Cato MH, et al. Suppression of phosphatidylinositol 3,4,5-trisphosphate production is a key determinant of B cell anergy. Immunity 2009;31:749-760.
48. Gauld SB, Benschop RJ,MerrellKT,Cambier JC.Maintenance of B cell anergy requires constant antigen receptor occupancy and signaling. Nat Immunol 2005;6:1160-1167. (Pubitemid 41541794)
49. Halverson R, Torres RM, Pelanda R. Receptor editing is the main mechanism of B cell tolerance toward membrane antigens. Nat Immunol 2004;5:645-650. (Pubitemid 38811890)
50. Phan TG, AmesburyM,Gardam S, et al. B cell receptor-independent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J ExpMed 2003;197:845-860. (Pubitemid 36437862)
51. Verkoczy L, Duong B, Skog P, et al. Basal B cell receptor-directed phosphatidylinositol 3-kinase signaling turns off RAGs and promotes B cell-positive selection. J Immunol 2007;178:6332-6341. (Pubitemid 46717417)
52. Monroe JG. ITAM-mediated tonic signalling through pre-BCR andBCRcomplexes.Nat Rev Immunol 2006;6:283-294.
53. Lam KP, Kuhn R, Rajewsky K. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 1997;90:1073-1083. (Pubitemid 27408521)
54. Kraus M, Alimzhanov MB, Rajewsky N, Rajewsky K. Survival of resting mature B lymphocytes depends on BCR signaling via the Igalpha/beta heterodimer. Cell 2004;117:787-800. (Pubitemid 38748894)
55. Smith SH, Reth M. Perspectives on the nature of BCR-mediated survival signals. Mol Cell 2004;14:696-697. (Pubitemid 38780844)
56. Torres RM, Flaswinkel H, Reth M, Rajewsky K. Aberrant B cell development and immune response in mice with a compromised BCR complex. Science 1996;272:1804-1808. (Pubitemid 26256403)
57. Oak JS, Chen J, Peralta RQ, et al.The p85beta regulatory subunit of phosphoinositide 3-kinase has unique and redundant functions in B cells. Autoimmunity 2009;42:447-458.
58. Rickert RC, 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.
59. Engel P, Zhou LJ, OrdDC, et al.AbnormalBlymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transductionmolecule. Immunity 1995;3:39-50.
60. OkkenhaugK,BilancioA, FarjotG, et al.ImpairedBand T cell antigen receptor signaling in p110delta PI 3-kinasemutant mice. Science 2002;297:1031-1034. (Pubitemid 34856039)
61. Clayton E, Bardi G, Bell SE, et al. A crucial role for the p110delta subunit of phosphatidylinositol 3- kinase in B cell development and activation. J ExpMed 2002;196:753-763.
62. Yamazaki T, Takeda K, Gotoh K, et al. Essential immunoregulatory role for BCAP in B cell development and function. J ExpMed 2002;195:535-545. (Pubitemid 34461499)
63. Srinivasan L, Sasaki Y, Calado DP, et al. PI3 kinase signals BCR-dependent mature B cell survival. Cell 2009;139:573-586.
64. Chen J, Limon JJ, Blanc C, et al. Foxo1 regulates marginal zone B-cell development. Eur J Immunol 2010;40:1890-1896.
65. Donahue AC,Hess KL,Ng KL, Fruman DA. Altered splenic B cell subset development inmice lacking phosphoinositide 3-kinase p85alpha. Int Immunol 2004;16:1789-1798. (Pubitemid 40003867)
66. Calamito M, Juntilla MM,ThomasM, et al. Akt1 and Akt2 promote peripheral B-cellmaturation and survival. Blood 2010;115:4043-4050.
67. Suzuki A, Kaisho T, Ohishi M, et al. Critical roles of Pten in B cell homeostasis and immunoglobulin class switch recombination. J ExpMed 2003;197:657-667. (Pubitemid 36314660)
68. Pape KA, Kouskoff V, Nemazee D, et al. Visualization of the genesis and fate of isotype-switched B cells during a primary immune response. J ExpMed 2003;197:1677-1687. (Pubitemid 36745343)
69. Peakman MC,MaizelsN. Localization of splenic B cells activated for switch recombination by in situ hybridization with Igamma1 switch transcript and Rad51 probes. J Immunol 1998;161:4008-4015. (Pubitemid 28468978)
70. Omori SA, Cato MH, Anzelon-Mills A, et al. Regulation of class-switch recombination and plasma cell differentiation by phosphatidylinositol 3-kinase signaling. Immunity 2006;25:545-557. (Pubitemid 44550181)
71. Rolf J, Bell SE, Kovesdi D, et al. Phosphoinositide 3-kinase activity in T cells regulates themagnitude of the germinal center reaction. J Immunol 2010;185:4042-4052.
72. Kerdiles YM, Stone EL, Beisner DR, et al. Foxo transcription factors control regulatory T cell development and function. Immunity 2010;33:890-904.