c-Rel plays a key role in deficient activation of B cells from a non-X-linked hyper-IgM patient

Blood

Volumn 108, Issue 12, 2006, Pages 3769-3776

  Lu, Kristina T ^b   Sinquett, Frank L ^b   Dryer, Rebecca L ^b   Song, Charles ^b   Covey, Lori R ^a  

^a RUTGERS UNIVERSITY   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CD23 ANTIGEN; MESSENGER RNA; TETRACYCLINE; TRANSCRIPTION FACTOR REL;

ARTICLE; B LYMPHOCYTE ACTIVATION; CLINICAL ARTICLE; FEMALE; GENE MUTATION; HUMAN; HUMAN CELL; HYPERIMMUNOGLOBULINEMIA M; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; X CHROMOSOME LINKED DISORDER;

EID: 33845251141     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-03-008839     Document Type: Article

References (72)

1. Harnett MM. CD40: a growing cytoplasmic tale. Sci STKE. 2004;2004:pe25.
2. Kawabe T, Naka T, Yishida K, et al. The immune response in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity. 1994;1:167-178.
3. Xu J, Foy TM, Laman JD, et al. Mice deficient for the CD40 ligand. Immunity. 1994;1:423-431.
4. Allen RC, Armitage RJ, Conley ME, et al. CD40 ligand gene defects responsible for X-linked hyper-IgM syndrome. Science. 1993;259:990-993.
5. Aruffo A, Farrington M, Hollenbaugh D, et al. The CD40 ligand, gp39, is defective in activated T cells from patients with X-linked immunodeficiency with hyper-IgM. Cell. 1993;72:291-300.
6. DiSanto JP, Bonnefoy JY, Gauchat JF, Fischer A, de SaintBasile G. CD40 ligand mutations in X-linked immunodeficiency with hyper-IgM. Nature. 1993;361:539-541.
7. Ferrari S, Giliani S, Insalaco A, et al. Mutations of CD40 gene cause an autosomal recessive form of immunodeficiency with hyper IgM. Proc Natl Acad Sci U S A. 2001;98:12614-12619.
8. Fuleihan R, Ramesh N, Loh R, et al. Defective expression of the CD40 ligand in X-chromosome-linked immunoglobulin deficiency with normal or elevated IgM. Proc Natl Acad Sci U S A. 1993;90:2170-2173.
9. Korthauer U, Graf D, Mages HW, et al. Defective expression of T-cell CD40 ligand causes X-linked immunodeficiency with hyper-IgM. Nature. 1993;361:539-541.
10. Etzioni A, Ochs HD. The hyper IgM syndrome: an evolving story. Pediatr Res. 2004;56:519-525.
11. Revy P, Muto T, Levy Y, et al. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the hyper-IgM syndrome (HIGM2). Cell. 2000;102:565-575.
12. Muramatsu M, Sankaranand VS, Anant S, et al. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J Biol Chem. 1999;274:18470-18476.
13. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 2000;102:553-563.
14. Zonana J, Elder ME, Schneider LC, et al. A novel X-linked disorder of immune deficiency and hypohidrotic ectodermal dysplasia is allelic to incontinentia pigmenti and due to mutations in IKK-gamma (NEMO). Am J Hum Genet. 2000;67:1555-1562.
15. Doffinger R, Smahi A, Bessia C, et al. X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-kappaB signaling. Nat Genet. 2001;27:277-285.
16. Jain A, Ma CA, Liu S, Brown M, Cohen J, Strober W. Specific missense mutations in NEMO result in hyper-IgM syndrome with hypohydrotic ectodermal dysplasia. Nat Immunol. 2001;2:223-228.
17. Bhushan A, Barnhart B, Shone S, Song C, Covey LR. A transcriptional defect underlies B lymphocyte dysfunction in a patient diagnosed with non-X-linked hyper-IgM syndrome. J Immunol. 2000;164:2871-2880.
18. Lu KT, Dryer RL, Song C, Covey LR. Maintenance of the CD40-related immunodeficient response in hyper-IgM B cells immortalized with a LMP1-regulated mini-EBV. J Leukoc Biol. 2005;78:620-629.
19. Ling NR, Hardie D, Lowe J, Johnson GD, Khan M, MacLennan IC. A phenotypic study of cells from Burkitt lymphoma and EBV-B-lymphoblastoid lines and their relationship to cells in normal lymphoid tissues. Int J Cancer. 1989;43:112-118.
20. Kikutani H, Suemura M, Owaki H, et al. Fc epsilon receptor, a specific differentiation marker transiently expressed on mature B cells before isotype switching. J Exp Med. 1986;164:1455-1469.
21. Defrance T, Aubry JP, Rousset F, et al. Human recombinant interleukin 4 induces Fc epsilon receptors (CD23) on normal human B lymphocytes. J Exp Med. 1987;165:1459-1467.
22. Thorley-Lawson DA, Nadler LM, Bhan AK, Schooley RT. BLAST-2 [EBVCS], an early cell surface marker of human B cell activation, is superinduced by Epstein Barr virus. J Immunol. 1985;134:3007-3012.
23. Yokota A, Yukawa K, Yamamoto A, et al. Two forms of the low-affinity Fc receptor for IgE differentially mediate endocytosis and phagocytosis: identification of the critical cytoplasmic domains. Proc Natl Acad Sci U S A. 1992;89:5030-5034.
24. Bevilacqua C, Montagnac G, Benmerah A, et al. Food allergens are protected from degradation during CD23-mediated transepithelial transport. Int Arch Allergy Immunol. 2004;135:108-116.
25. Yu LC, Montagnac G, Yang PC, Conrad DH, Benmerah A, Perdue MH. Intestinal epithelial CD23 mediates enhanced antigen transport in allergy: evidence for novel splice forms. Am J Physiol Gastrointest Liver Physiol. 2003;285:G223-G234.
26. Kintner C, Sugden B. Identification of antigenic determinants unique to the surfaces of cells transformed by Epstein-Barr virus. Nature. 1981;294:458-460.
27. Thorley-Lawson DA, Swendeman SL, Edson CM. Biochemical analysis suggests distinct functional roles for the BLAST-1 and BLAST-2 antigens. J Immunol. 1986;136:1745-1751.
28. Calender A, Billaud M, Aubry JP, Banchereau J, Vuillaume M, Lenoir GM. Epstein-Barr virus (EBV) induces expression of B-cell activation markers on in vitro infection of EBV-negative B-lymphoma cells. Proc Natl Acad Sci U S A. 1987;84:8060-8064.
29. Kikutani H, Nakamura H, Sato R, et al. Delineation and characterization of human B cell subpopulations at various stages of activation by using a B cell-specific monoclonal antibody. J Immunol. 1986;136:4027-4034.
30. Cordier M, Calender A, Billaud M, et al. Stable transfection of Epstein-Barr virus (EBV) nuclear antigen 2 in lymphoma cells containing the EBV P3HR1 genome induces expression of B-cell activation molecules CD21 and CD23. J Virol. 1990;64:1002-1013.
31. Tinnell SB, Jacobs-Helber SM, Sterneck E, Sawyer ST, Conrad DH. STAT6, NF-kappaB and C/EBP in CD23 expression and IgE production. Int Immunol. 1998;10:1529-1538.
32. Ewart MA, Ozanne BW, Cushley W. The CD23a and CD23b proximal promoters display different sensitivities to exogenous stimuli in B lymphocytes. Genes Immun. 2002;3:158-164.
33. Xiao C, Ghosh S. NF-kappaB, an evolutionarily conserved mediator of immune and inflammatory responses. Adv Exp Med Biol. 2005;560:41-45.
34. Tumang JR, Owyang A, Andjelic S, et al. c-Rel is essential for B lymphocyte survival and cell cycle progression. Eur J Immunol. 1998;28:4299-4312.
35. Ghosh S, May MJ, Kopp EB. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol. 1998;16:225-260.
36. Gerondakis S, Grossmann M, Nakamura Y, Pohl T, Grumont R. Genetic approaches in mice to understand Rel/NF-kappaB and IkappaB function: transgenics and knockouts. Oncogene. 1999;18:6888-6895.
37. Kilger E, Kieser A, Baumann M, Hammerschmidt W. Epstein-Barr virus-mediated B-cell proliferation is dependent upon latent membrane protein 1, which simulates an activated CD40 receptor. EMBO J. 1998;17:1700-1709.
38. Fan Y, Rayet B, Gelinas C. Divergent C-terminal transactivation domains of Rel/NF-kappa B proteins are critical determinants of their oncogenic potential in lymphocytes. Oncogene. 2004;23:1030-1042.
39. Dryer RL, Covey LR. A novel NF-kappa B-regulated site within the human I gamma 1 promoter requires p300 for optimal transcriptional activity. J Immunol. 2005;175:4499-4507.
40. Richards ML, Katz DH. Analysis of the promoter elements necessary for IL-4 and anti-CD40 antibody induction of murine FcεRII (CD23). J Immunol. 1997;158:263-272.
41. Suter U, Bastos R, Hofstetter H. Molecular structure of the gene and the 5′-flanking region of the human lymphocyte immunoglobulin E receptor. Nuc Acids Res. 1987;15:7295-7308.
42. Ling PD, Hsieh JJ, Ruf IK, Rawlins DR, Hayward SD. EBNA-2 upregulation of Epstein-Barr virus latency promoters and the cellular CD23 promoter utilizes a common targeting intermediate, CBF1. J Virol. 1994;68:5375-5383.
43. Visan I, Goller M, Berberich I, Kneitz C, Tony HP. Pax-5 is a key regulator of the B cell-restricted expression of the CD23a isoform. Eur J Immunol. 2003;33:1163-1173.
44. Gupta S, Jiang M, Anthony A, Pernis AB. Lineage-specific modulation of interleukin 4 signaling by interferon regulatory factor 4. J Exp Med. 1999;190:1837-1848.
45. Kneitz C, Goller M, Tony H, et al. The CD23b promoter is a target for NF-AT transcription factors in B-CLL cells. Biochim Biophys Acta. 2002;1588:41-47.
46. Gilmore TD, Kalaitzidis D, Liang MC, Starczynowski DT. The c-Rel transcription factor and B-cell proliferation: a deal with the devil. Oncogene. 2004;23:2275-2286.
47. Kontgen F, Grumont RJ, Strasser A, et al. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 1995;9:1965-1977.
48. Hsia CY, Cheng S, Owyang AM, Dowdy SF, Liou HC. c-Rel regulation of the cell cycle in primary mouse B lymphocytes. Int Immunol. 2002;14:905-916.
49. Cheng S, Hsia CY, Leone G, Liou HC. Cyclin E and Bcl-xL cooperatively induce cell cycle progression in c-Rel-/- B cells. Oncogene. 2003;22:8472-8486.
50. Andjelic S, Hsia C, Suzuki H, Kadowaki T, Koyasu S, Liou HC. Phosphatidylinositol 3-kinase and NF-kappa B/Rel are at the divergence of CD40-mediated proliferation and survival pathways. J Immunol. 2000;165:3860-3867.
51. Lee HH, Dadgostar H, Cheng Q, Shu J, Cheng G. NF-kappa B-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc Natl Acad Sci U S A. 1999;96:9136-9141.
52. Owyang AM, Tumang JR, Schram BR, et al. c-Rel is required for the protection of B cells from antigen receptor-mediated, but not Fas-mediated, apoptosis. J Immunol. 2001;167:4948-4956.
53. Zong WX, Edelstein LC, Chen C, Bash J, Gelinas C. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev. 1999;13:382-387.
54. Tumang JR, Hsia CY, Tian W, Bromberg JF, Liou HC. IL-6 rescues the hyporesponsiveness of c-Rel deficient B cells independent of Bcl-xL, Mcl-1, and Bcl-2. Cell Immunol. 2002;217:47-57.
55. Chen E, Hrdlickova R, Nehyba J, Longo DL, Bose HR Jr, Li CC. Degradation of proto-oncoprotein c-Rel by the ubiquitin-proteasome pathway. J Biol Chem. 1998;273:35201-35207.
56. Barkett M, Dooher JE, Lemonnier L, et al. Three mutations in v-Rel render it resistant to cleavage by cell-death protease caspase-3. Biochim Biophys Acta. 2001;1526:25-36.
57. Mosialos G, Hamer P, Capobianco AJ, Laursen RA, Gilmore TD. A protein kinase-A recognition sequence is structurally linked to transformation by p59v-rel and cytoplasmic retention of p68c-rel. Mol Cell Biol. 1991;11:5867-5877.
58. Bryan RG, Li Y, Totten RK, Van M, Tan TH, Rich RR. Long-term inositol phosphate release, but not tyrosine kinase activity, correlates with IL-2 secretion and NF-AT induction in anti-CD3-activated peripheral human T lymphocytes. Cell Immunol. 1994;157:158-169.
59. Neumann M, Tsapos K, Scheppler JA, Ross J, Franza BR Jr. Identification of complex formation between two intracellular tyrosine kinase substrates: human c-Rel and the p105 precursor of p50 NF-kappa B. Oncogene. 1992;7:2095-2104.
60. Brownell E, Mittereder N, Rice NR. A human rel proto-oncogene cDNA containing an Alu fragment as a potential coding exon. Oncogene. 1989;4:935-942.
61. Starczynowski DT, Reynolds JG, Gilmore TD. Mutations of tumor necrosis factor alpha-responsive serine residues within the C-terminal transactivation domain of human transcription factor REL enhance its in vitro transforming ability. Oncogene. 2005;24:7355-7368.
62. Martin AG, San-Antonio B, Fresno M. Regulation of nuclear factor kappa B transactivation: implication of phosphatidylinositol 3-kinase and protein kinase C zeta in c-Rel activation by tumor necrosis factor alpha. J Biol Chem. 2001;276:15840-15849.
63. Sanchez-Valdepenas C, Martin AG, Ramakrishnan P, Wallach D, Fresno M. NF-kappaB-inducing kinase is involved in the activation of the CD28 responsive element through phosphorylation of c-Rel and regulation of its transactivating activity. J Immunol. 2006;176:4666-4674.
64. Hu MC, Tang-Oxley Q, Qiu WR, et al. Protein phosphatase X interacts with c-Rel and stimulates c-Rel/nuclear factor kappaB activity. J Biol Chem. 1998;273:33561-33565.
65. Wang F, Kikutani H, Tsang SF, Kishimoto T, Kieff E. Epstein-Barr virus nuclear protein 2 transactivates a cis-acting CD23 DNA element. J Virol. 1991;65:4101-4106.
66. Chen FE, Ghosh G. Regulation of DNA binding by Rel/NF-kappaB transcription factors: structural views. Oncogene. 1999;18:6845-6852.
67. Kunsch C, Ruben SM, Rosen CA. Selection of optimal kappa B/Rel DNA-binding motifs: interaction of both subunits of NF-kappa B with DNA is required for transcriptional activation. Mol Cell Biol. 1992;12:4412-4421.
68. Sanjabi S, Williams KJ, Saccani S, et al. A c-Rel subdomain responsible for enhanced DNA-binding affinity and selective gene activation. Genes Dev. 2005;19:2138-2151.
69. Leung TH, Hoffmann A, Baltimore D. One nucleotide in a kappaB site can determine cofactor specificity for NF-kappaB dimers. Cell. 2004;118:453-464.
70. Pohl T, Gugasyan R, Grumont RJ, et al. The combined absence of NF-kappa B1 and c-Rel reveals that overlapping roles for these transcription factors in the B cell lineage are restricted to the activation and function of mature cells. Proc Natl Acad Sci U S A. 2002;99:4514-4519.
71. Zelazowski P, Carrasco D, Rosas FR, Moorman MA, Bravo R, Snapper CM. B cells genetically deficient in the c-Rel transactivation domain have selective defects in germline CH transcription and Ig class switching. J Immunol. 1997;159:3133-3139.
72. Jain A, Ma CA, Lopez-Granados E, et al. Specific NEMO mutations impair CD40-mediated c-Rel activation and B cell terminal differentiation. J Clin Invest. 2004;114:1593-1602.