Impaired B cell development in the absence of Krüppel-like factor 3

Journal of Immunology

Volumn 187, Issue 10, 2011, Pages 5032-5042

  Vu, Thi Thanh ^a   Gatto, Dominique ^b   Turner, Vivian ^b   Funnell, Alister P W ^a,c   Mak, Ka Sin ^c   Norton, Laura J ^c   Kaplan, Warren ^b   Cowley, Mark J ^b   Agenès, Fabien ^d   Kirberg, Jörg ^e   Brink, Robert ^a,c   Pearson, Richard C M ^a,c   Crossley, Merlin ^a,c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

^e PAUL EHRLICH INSTITUT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; BONE MARROW; CELL MATURATION; CONTROLLED STUDY; FETUS; GENE; GENE EXPRESSION; GENE REGULATORY NETWORK; IMMUNOHISTOLOGY; KRUPPEL LIKE FACTOR GENE; LYMPHOPOIESIS; MOUSE; NONHUMAN; PERITONEAL CAVITY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPLEEN;

ANIMALS; B-LYMPHOCYTE SUBSETS; BONE MARROW CELLS; CELL DIFFERENTIATION; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LYMPHOPOIESIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PERITONEUM; RADIATION CHIMERA; SPLEEN;

EID: 81455131847     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101450     Document Type: Article

References (59)

1. van Vliet, J., L. A. Crofts, K. G. Quinlan, R. Czolij, A. C. Perkins, and M. Crossley. 2006. Human KLF17 is a new member of the Sp/KLF family of transcription factors. Genomics 87: 474-482.
2. Pearson, R., J. Fleetwood, S. Eaton, M. Crossley, and S. Bao. 2008. Krüppel-like transcription factors: a functional family. Int. J. Biochem. Cell Biol. 40: 1996-2001. (Pubitemid 352004270)
3. Cao, Z., X. Sun, B. Icli, A. K. Wara, and M. W. Feinberg. 2010. Role of Kruppellike factors in leukocyte development, function, and disease. Blood 116: 4404-4414.
4. Perkins, A. C., A. H. Sharpe, and S. H. Orkin. 1995. Lethal beta-thalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature 375: 318-322.
5. Carlson, C. M., B. T. Endrizzi, J. Wu, X. Ding, M. A. Weinreich, E. R. Walsh, M. A. Wani, J. B. Lingrel, K. A. Hogquist, and S. C. Jameson. 2006. Kruppellike factor 2 regulates thymocyte and T-cell migration. Nature 442: 299-302. (Pubitemid 44114904)
6. Hoek, K. L., L. E. Gordy, P. L. Collins, V. V. Parekh, T. M. Aune, S. Joyce, J. W. Thomas, L. Van Kaer, and E. Sebzda. 2010. Follicular B cell trafficking within the spleen actively restricts humoral immune responses. Immunity 33: 254-265.
7. Hart, G. T., X. Wang, K. A. Hogquist, and S. C. Jameson. 2011. Krüppel-like factor 2 (KLF2) regulates B-cell reactivity, subset differentiation, and trafficking molecule expression. Proc. Natl. Acad. Sci. USA 108: 716-721.
8. Winkelmann, R., L. Sandrock, M. Porstner, E. Roth, M. Mathews, E. Hobeika, M. Reth, M. L. Kahn, W. Schuh, and H. M. Jäck. 2011. B cell homeostasis and plasma cell homing controlled by Krüppel-like factor 2. Proc. Natl. Acad. Sci. USA 108: 710-715.
9. Feinberg, M. W., A. K. Wara, Z. Cao, M. A. Lebedeva, F. Rosenbauer, H. Iwasaki, H. Hirai, J. P. Katz, R. L. Haspel, S. Gray, et al. 2007. The Kruppellike factor KLF4 is a critical regulator of monocyte differentiation. EMBO J. 26: 4138-4148. (Pubitemid 47462091)
10. Good, K. L., and S. G. Tangye. 2007. Decreased expression of Kruppel-like factors in memory B cells induces the rapid response typical of secondary antibody responses. Proc. Natl. Acad. Sci. USA 104: 13420-13425. (Pubitemid 47293960)
11. Cao, Z., X. Sun, B. Icli, A. K. Wara, and M. W. Feinberg. 2010. Role of Kruppellike factors in leukocyte development, function, and disease. Blood 116: 4404-4414.
12. Sankaran, V. G., J. Xu, and S. H. Orkin. 2010. Advances in the understanding of haemoglobin switching. Br. J. Haematol. 149: 181-194.
13. Crossley, M., E. Whitelaw, A. Perkins, G. Williams, Y. Fujiwara, and S. H. Orkin. 1996. Isolation and characterization of the cDNA encoding BKLF/TEF-2, a major CACCC-box-binding protein in erythroid cells and selected other cells. Mol. Cell. Biol. 16: 1695-1705. (Pubitemid 26095642)
14. Turner, J., and M. Crossley. 1998. Cloning and characterization of mCtBP2, a co-repressor that associates with basic Krüppel-like factor and other mammalian transcriptional regulators. EMBO J. 17: 5129-5140. (Pubitemid 28408479)
15. Himeda, C. L., J. A. Ranish, R. C. Pearson, M. Crossley, and S. D. Hauschka. 2010. KLF3 regulates muscle-specific gene expression and synergizes with serum response factor on KLF binding sites. Mol. Cell. Biol. 30: 3430-3443.
16. Perdomo, J., A. Verger, J. Turner, and M. Crossley. 2005. Role for SUMO modification in facilitating transcriptional repression by BKLF. Mol. Cell. Biol. 25: 1549-1559. (Pubitemid 40204929)
17. Funnell, A. P., C. A. Maloney, L. J. Thompson, J. Keys, M. Tallack, A. C. Perkins, and M. Crossley. 2007. Erythroid Krüppel-like factor directly activates the basic Krüppel-like factor gene in erythroid cells. Mol. Cell. Biol. 27: 2777-2790. (Pubitemid 46581365)
18. Sue, N., B. H. Jack, S. A. Eaton, R. C. Pearson, A. P. Funnell, J. Turner, R. Czolij, G. Denyer, S. Bao, J. C. Molero-Navajas, et al. 2008. Targeted disruption of the basic Krüppel-like factor gene (Klf3) reveals a role in adipogenesis. Mol. Cell. Biol. 28: 3967-3978. (Pubitemid 351812983)
19. Pearson, R. C., A. P. Funnell, and M. Crossley. 2011. The mammalian zinc finger transcription factor Krüppel-like factor 3 (KLF3/BKLF). IUBMB Life 63: 86-93.
20. Kirberg, J., C. Gschwendner, J. P. Dangy, F. Rückerl, F. Frommer, and J. Bachl. 2005. Proviral integration of an Abelson-murine leukemia virus deregulates BKLF-expression in the hypermutating pre-B cell line 18-81. Mol. Immunol. 42: 1235-1242.
21. Glynne, R., G. Ghandour, J. Rayner, D. H. Mack, and C. C. Goodnow. 2000. Blymphocyte quiescence, tolerance and activation as viewed by global gene expression profiling on microarrays. Immunol. Rev. 176: 216-246.
22. Akagi, K., T. Suzuki, R. M. Stephens, N. A. Jenkins, and N. G. Copeland. 2004. RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res. 32(Database issue): D523-D527. (Pubitemid 38081713)
23. Turchinovich, G., T. T. Vu, F. Frommer, J. Kranich, S. Schmid, M. Alles, J. B. Loubert, J. P. Goulet, U. Zimber-Strobl, P. Schneider, et al. 2011. Programming of marginal zone B-cell fate by basic Kruppel-like factor (BKLF/KLF3). Blood 117: 3780-3792.
24. Hardy, R. R., C. E. Carmack, S. A. Shinton, J. D. Kemp, and K. Hayakawa. 1991. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173: 1213-1225.
25. Allende, M. L., G. Tuymetova, B. G. Lee, E. Bonifacino, Y. P. Wu, and R. L. Proia. 2010. S1P1 receptor directs the release of immature B cells from bone marrow into blood. J. Exp. Med. 207: 1113-1124.
26. Shiow, L. R., D. B. Rosen, N. Brdicková, Y. Xu, J. An, L. L. Lanier, J. G. Cyster, and M. Matloubian. 2006. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440: 540-544.
27. Kishimoto, T. K., M. A. Jutila, and E. C. Butcher. 1990. Identification of a human peripheral lymph node homing receptor: a rapidly down-regulated adhesion molecule. Proc. Natl. Acad. Sci. USA 87: 2244-2248.
28. Postigo, A. A., P. Sánchez-Mateos, A. I. Lazarovits, F. Sánchez-Madrid, and M. O. de Landázuri. 1993. Alpha 4 beta 7 integrin mediates B cell binding to fibronectin and vascular cell adhesion molecule-1. Expression and function of alpha 4 integrins on human B lymphocytes. J. Immunol. 151: 2471-2483. (Pubitemid 23264500)
29. Tumang, J. R., W. D. Hastings, C. Bai, and T. L. Rothstein. 2004. Peritoneal and splenic B-1 cells are separable by phenotypic, functional, and transcriptomic characteristics. Eur. J. Immunol. 34: 2158-2167. (Pubitemid 39256097)
30. Casola, S., K. L. Otipoby, M. Alimzhanov, S. Humme, N. Uyttersprot, J. L. Kutok, M. C. Carroll, and K. Rajewsky. 2004. B cell receptor signal strength determines B cell fate. Nat. Immunol. 5: 317-327. (Pubitemid 38332129)
31. Niiro, H., and E. A. Clark. 2002. Regulation of B-cell fate by antigen-receptor signals. Nat. Rev. Immunol. 2: 945-956. (Pubitemid 37323215)
32. Eaton, S. A., A. P. Funnell, N. Sue, H. Nicholas, R. C. Pearson, and M. Crossley. 2008. A network of Krüppel-like Factors (Klfs). Klf8 is repressed by Klf3 and activated by Klf1 in vivo. J. Biol. Chem. 283: 26937-26947.
33. van Vliet, J., J. Turner, and M. Crossley. 2000. Human Krüppel-like factor 8: a CACCC-box binding protein that associates with CtBP and represses transcription. Nucleic Acids Res. 28: 1955-1962. (Pubitemid 30229662)
34. Schuierer, M., K. Hilger-Eversheim, T. Dobner, A. K. Bosserhoff, M. Moser, J. Turner, M. Crossley, and R. Buettner. 2001. Induction of AP-2alpha expression by adenoviral infection involves inactivation of the AP-2rep transcriptional corepressor CtBP1. J. Biol. Chem. 276: 27944-27949.
35. Outram, S. V., A. R. Gordon, A. L. Hager-Theodorides, J. Metcalfe, T. Crompton, and P. Kemp. 2008. KLF13 influences multiple stages of both B and T cell development. Cell Cycle 7: 2047-2055. (Pubitemid 352030351)
36. Cariappa, A., M. Tang, C. Parng, E. Nebelitskiy, M. Carroll, K. Georgopoulos, and S. Pillai. 2001. The follicular versus marginal zone B lymphocyte cell fate decision is regulated by Aiolos, Btk, and CD21. Immunity 14: 603-615. (Pubitemid 32520871)
37. Wen, L., J. Brill-Dashoff, S. A. Shinton, M. Asano, R. R. Hardy, and K. Hayakawa. 2005. Evidence of marginal-zone B cell-positive selection in spleen. Immunity 23: 297-308. (Pubitemid 41317797)
38. Berland, R., and H. H. Wortis. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20: 253-300. (Pubitemid 34293426)
39. Cariappa, A., H. Takematsu, H. Liu, S. Diaz, K. Haider, C. Boboila, G. Kalloo, M. Connole, H. N. Shi, N. Varki, et al. 2009. B cell antigen receptor signal strength and peripheral B cell development are regulated by a 9-O-acetyl sialic acid esterase. J. Exp. Med. 206: 125-138.
40. Pillai, S., A. Cariappa, and S. T. Moran. 2005. Marginal zone B cells. Annu. Rev. Immunol. 23: 161-196. (Pubitemid 40563168)
41. Samardzic, T., D. Marinkovic, C. P. Danzer, J. Gerlach, L. Nitschke, and T. Wirth. 2002. Reduction of marginal zone B cells in CD22-deficient mice. Eur. J. Immunol. 32: 561-567. (Pubitemid 34173347)
42. O'Keefe, T. L., G. T. Williams, S. L. Davies, and M. S. Neuberger. 1996. Hyperresponsive B cells in CD22-deficient mice. Science 274: 798-801. (Pubitemid 26398264)
43. Seo, S., J. Buckler, and J. Erikson. 2001. Novel roles for Lyn in B cell migration and lipopolysaccharide responsiveness revealed using anti-double-stranded DNA Ig transgenic mice. J. Immunol. 166: 3710-3716. (Pubitemid 32224893)
44. Chan, V. W., F. Meng, P. Soriano, A. L. DeFranco, and C. A. Lowell. 1997. Characterization of the B lymphocyte populations in Lyn-deficient mice and the role of Lyn in signal initiation and down-regulation. Immunity 7: 69-81. (Pubitemid 27357266)
45. Khan, W. N., F. W. Alt, R. M. Gerstein, B. A. Malynn, I. Larsson, G. Rathbun, L. Davidson, S. Müller, A. B. Kantor, L. A. Herzenberg, et al. 1995. Defective B cell development and function in Btk-deficient mice. Immunity 3: 283-299.
46. 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.
47. Makowska, A., N. N. Faizunnessa, P. Anderson, T. Midtvedt, and S. Cardell. 1999. CD1high B cells: a population of mixed origin. Eur. J. Immunol. 29: 3285-3294. (Pubitemid 29484219)
48. Wang, J. H., N. Avitahl, A. Cariappa, C. Friedrich, T. Ikeda, A. Renold, K. Andrikopoulos, L. Liang, S. Pillai, B. A. Morgan, and K. Georgopoulos. 1998. Aiolos regulates B cell activation and maturation to effector state. Immunity 9: 543-553. (Pubitemid 28499205)
49. Schneider, P., H. Takatsuka, A. Wilson, F. Mackay, A. Tardivel, S. Lens, T. G. Cachero, D. Finke, F. Beermann, and J. Tschopp. 2001. Maturation of marginal zone and follicular B cells requires B cell activating factor of the tumor necrosis factor family and is independent of B cell maturation antigen. J. Exp. Med. 194: 1691-1697. (Pubitemid 33126819)
50. Allman, D., and S. Pillai. 2008. Peripheral B cell subsets. Curr. Opin. Immunol. 20: 149-157.
51. Ogata, H., I. Su, K. Miyake, Y. Nagai, S. Akashi, I. Mecklenbräuker, K. Rajewsky, M. Kimoto, and A. Tarakhovsky. 2000. The toll-like receptor protein RP105 regulates lipopolysaccharide signaling in B cells. J. Exp. Med. 192: 23-29. (Pubitemid 30470803)
52. Kimoto, M., K. Nagasawa, and K. Miyake. 2003. Role of TLR4/MD-2 and RP105/MD-1 in innate recognition of lipopolysaccharide. Scand. J. Infect. Dis. 35: 568-572. (Pubitemid 37336874)
53. Banks, T. A., B. T. Rouse, M. K. Kerley, P. J. Blair, V. L. Godfrey, N. A. Kuklin, D. M. Bouley, J. Thomas, S. Kanangat, and M. L. Mucenski. 1995. Lymphotoxin-alpha-deficient mice. Effects on secondary lymphoid organ development and humoral immune responsiveness. J. Immunol. 155: 1685-1693.
54. De Togni, P., J. Goellner, N. H. Ruddle, P. R. Streeter, A. Fick, S. Mariathasan, S. C. Smith, R. Carlson, L. P. Shornick, J. Strauss-Schoenberger, et al. 1994. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264: 703-707. (Pubitemid 24185880)
55. Arbonés, M. L., D. C. Ord, K. Ley, H. Ratech, C. Maynard-Curry, G. Otten, D. J. Capon, and T. F. Tedder. 1994. Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity 1: 247-260.
56. Kin, N.W., D. M. Crawford, J. Liu, T.W. Behrens, and J. F. Kearney. 2008. DNA microarray gene expression profile of marginal zone versus follicular B cells and idiotype positive marginal zone B cells before and after immunization with Streptococcus pneumoniae. J. Immunol. 180: 6663-6674.
57. Dang, D. T., W. Zhao, C. S. Mahatan, D. E. Geiman, and V. W. Yang. 2002. Opposing effects of Krüppel-like factor 4 (gut-enriched Krüppel-like factor) and Krüppel-like factor 5 (intestinal-enriched Krüppel-like factor) on the promoter of the Krüppel-like factor 4 gene. Nucleic Acids Res. 30: 2736-2741. (Pubitemid 34778131)
58. Patel, S., Z. F. Xi, E. Y. Seo, D. McGaughey, and J. A. Segre. 2006. Klf4 and corticosteroids activate an overlapping set of transcriptional targets to accelerate in utero epidermal barrier acquisition. Proc. Natl. Acad. Sci. USA 103: 18668-18673. (Pubitemid 44913468)
59. Yusuf, I., M. G. Kharas, J. Chen, R. Q. Peralta, A. Maruniak, P. Sareen, V. W. Yang, K. H. Kaestner, and D. A. Fruman. 2008. KLF4 is a FOXO target gene that suppresses B cell proliferation. Int. Immunol. 20: 671-681. (Pubitemid 351619235)