Optimal functional levels of activation-induced deaminase specifically require the Hsp40 DnaJa1

EMBO Journal

Volumn 31, Issue 3, 2012, Pages 679-691

  Orthwein, Alexandre ^a,b   Zahn, Astrid ^a   Methot, Stephen P ^a,e   Godin, David ^a   Conticello, Silvestro G ^c   Terada, Kazutoyo ^d   Di Noia, Javier M ^a,b,e  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c ISTITUTO TOSCANO TUMORI   (Italy)

^d KUMAMOTO UNIVERSITY   (Japan)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

activation induced deaminase; antibody diversification; DnaJa1; farnesylation; Hsp40

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; HEAT SHOCK PROTEIN 40; PROTEIN DNAJA1; PROTEIN DNAJA2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STABILITY;

ANIMALS; CELL LINE, TUMOR; CYTIDINE DEAMINASE; FEMALE; HSP40 HEAT-SHOCK PROTEINS; HUMANS; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL;

MUS;

EID: 84856472936     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.417     Document Type: Article

References (78)

1. Aoufouchi S, Faili A, Zober C, D'Orlando O, Weller S, Weill J-C, Reynaud C-A (2008) Proteasomal degradation restricts the nuclear lifespan of AID. J Exp Med 205: 1357-1368 (Pubitemid 351831492)
2. Arakawa H, Hauschild J, Buerstedde J-M (2002) Requirement of the activation-induced deaminase (AID) gene for immunoglobulin gene conversion. Science 295: 1301-1306 (Pubitemid 34157623)
3. Bardwell JC, Tilly K, Craig E, King J, Zylicz M, Georgopoulos C (1986) The nucleotide sequence of the Escherichia coli K12 dnaJ+ gene. A gene that encodes a heat shock protein. J Biol Chem 261: 1782-1785 (Pubitemid 17205014)
4. Bhangoo MK, Tzankov S, Fan ACY, Dejgaard K, Thomas DY, Young JC (2007) Multiple 40-kDa heat-shock protein chaperones function in Tom70-dependent mitochondrial import. Mol Biol Cell 18: 3414-3428 (Pubitemid 47378681)
5. Brar SS, Watson M, Diaz M (2004) Activation-induced cytosine deaminase (AID) is actively exported out of the nucleus but retained by the induction of DNA breaks. J Biol Chem 279: 26395-26401 (Pubitemid 38798791)
6. Caplan AJ, Langley E, Wilson EM, Vidal J (1995) Hormone-dependent transactivation by the human androgen receptor is regulated by a dnaJ protein. J Biol Chem 270: 5251-5257
7. Caplan AJ, Tsai J, Casey PJ, Douglas MG (1992) Farnesylation of YDJ1p is required for function at elevated growth temperatures in Saccharomyces cerevisiae. J Biol Chem 267: 18890-18895
8. Cintron NS, Toft DO (2006) Defining the requirements for Hsp40 and Hsp70 in the Hsp90 chaperone pathway. J Biol Chem 281: 26235-26244 (Pubitemid 44401831)
9. Conticello SG, Ganesh K, Xue K, Lu M, Rada C, Neuberger MS (2008) Interaction between antibody-diversification enzyme AID and spliceosome- associated factor CTNNBL1. Mol Cell 31: 474-484
10. Di Noia JM, Neuberger MS (2007) Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem 76: 1-22
11. Dittmar KD, Banach M, Galigniana MD, Pratt WB (1998) The role of DnaJ-like proteins in glucocorticoid receptor.hsp90 heterocomplex assembly by the reconstituted hsp90.p60.hsp70 foldosome complex. J Biol Chem 273: 7358-7366 (Pubitemid 28152756)
12. Ficker E, Dennis AT,Wang L, Brown AM (2003) Role of the cytosolic chaperones Hsp70 and Hsp90 in maturation of the cardiac potassium channel HERG. Circ Res 92: e87-e100
13. Flom GA, Lemieszek M, Fortunato EA, Johnson JL (2008) Farnesylation of Ydj1 is required for in vivo interaction with Hsp90 client proteins. Mol Biol Cell 19: 5249-5258
14. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425: 737-741 (Pubitemid 37314318)
15. Gur E, Katz C, Ron EZ (2005) All three J-domain proteins of the Escherichia coli DnaK chaperone machinery are DNA binding proteins. FEBS Lett 579: 1935-1939 (Pubitemid 40404034)
16. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475: 324-332
17. Heldens L, Dirks RP, Hensen SMM, Onnekink C, van Genesen ST, Rustenburg F, Lubsen NH (2010) Co-chaperones are limiting in a depleted chaperone network. Cell Mol Life Sci 67: 4035-4048
18. Hernández MP, Chadli A, Toft DO (2002) HSP40 binding is the first step in the HSP90 chaperoning pathway for the progesterone receptor. J Biol Chem 277: 11873-11881 (Pubitemid 34952744)
19. Ito S, Nagaoka H, Shinkura R, Begum NA, Muramatsu M, Nakata M, Honjo T (2004) Activation-induced cytidine deaminase shuttles between nucleus and cytoplasm like apolipoprotein B mRNA editing catalytic polypeptide 1. Proc Natl Acad Sci USA 101: 1975-1980 (Pubitemid 38229000)
20. Johnson JL, Craig EA (2001) An essential role for the substratebinding region of Hsp40s in Saccharomyces cerevisiae. J Cell Biol 152: 851-856 (Pubitemid 34280169)
21. Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11: 579-592
22. Kanazawa M, Terada K, Kato S, Mori M (1997) HSDJ, a human homolog of DnaJ, is farnesylated and is involved in protein import into mitochondria. J Biochem 121: 890-895 (Pubitemid 27236907)
23. Kimura Y, Yahara I, Lindquist S (1995) Role of the protein chaperone YDJ1 in establishing Hsp90-mediated signal transduction pathways. Science 268: 1362-1365
24. Kosano H, Stensgard B, Charlesworth MC, McMahon N, Toft D (1998) The assembly of progesterone receptor-hsp90 complexes using purified proteins. J Biol Chem 273: 32973-32979 (Pubitemid 28557691)
25. Kuraoka M, Holl TM, Liao D, Womble M, Cain DW, Reynolds AE, Kelsoe G (2011) Activation-induced cytidine deaminase mediates central tolerance in B cells. Proc Natl Acad Sci USA 108: 11560-11565
26. Langer T, Lu C, Echols H, Flanagan J, Hayer MK, Hartl FU (1992) Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356: 683-689
27. Li J, Qian X, Sha B (2003) The crystal structure of the yeast Hsp40 Ydj1 complexed with its peptide substrate. Structure 11: 1475-1483 (Pubitemid 37510348)
28. Liu M, Duke JL, Richter DJ, Vinuesa CG, Goodnow CC, Kleinstein SH, Schatz DG (2008) Two levels of protection for the B cell genome during somatic hypermutation. Nature 451: 841-845 (Pubitemid 351253166)
29. Lu Z, Cyr DM (1998) Protein folding activity of Hsp70 is modified differentially by the hsp40 co-chaperones Sis1 and Ydj1. J Biol Chem 273: 27824-27830 (Pubitemid 28496069)
30. Macduff D, Demorest Z, Harris R (2009) AID can restrict L1 retrotransposition suggesting a dual role in innate and adaptive immunity. Nucleic Acids Res 37: 1854-1867
31. Marshall CJ (1993) Protein prenylation: a mediator of proteinprotein interactions. Science 259: 1865-1866 (Pubitemid 23124458)
32. Matsumoto Y, Marusawa H, Kinoshita K, Endo Y, Kou T, Morisawa T, Azuma T, Okazaki IM, Honjo T, Chiba T (2007) Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium. Nat Med 13: 470-476 (Pubitemid 46559833)
33. McBride KM, Barreto V, Ramiro AR, Stavropoulos P, Nussenzweig MC (2004) Somatic hypermutation is limited by CRM1-dependent nuclear export of activation-induced deaminase. J Exp Med 199: 1235-1244 (Pubitemid 38620260)
34. Minami Y, Höhfeld J, Ohtsuka K, Hartl FU (1996) Regulation of the heat-shock protein 70 reaction cycle by the mammalian DnaJ homolog, Hsp40. J Biol Chem 271: 19617-19624 (Pubitemid 26271642)
35. Morgan HD, Dean W, Coker HA, Reik W, Petersen-Mahrt SK (2004) Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J Biol Chem 279: 52353-52360 (Pubitemid 39656611)
36. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102: 553-563
37. Muramatsu M, Sankaranand VS, Anant S, Sugai M, Kinoshita K, Davidson NO, Honjo T (1999) Specific expression of activationinduced cytidine deaminase (AID), a novel member of the RNAediting deaminase family in germinal center B cells. J Biol Chem 274: 18470-18476
38. Nakamura M, Kondo S, Sugai M, Nazarea M, Imamura S, Honjo T (1996) High frequency class switching of an IgM+ B lymphoma clone CH12F3 to IgA+ cells. Int Immunol 8: 193-201 (Pubitemid 26049771)
39. Okazaki IM, Hiai H, Kakazu N, Yamada S, Muramatsu M, Kinoshita K, Honjo T (2003) Constitutive expression of AID leads to tumorigenesis. J Exp Med 197: 1173-1181 (Pubitemid 36570072)
40. Okazaki IM, Okawa K, Kobayashi M, Yoshikawa K, Kawamoto S, Nagaoka H, Shinkura R, Kitawaki Y, Taniguchi H, Natsume T, Iemura S-I, Honjo T (2011) Histone chaperone Spt6 is required for class switch recombination but not somatic hypermutation. Proc Natl Acad Sci USA 108: 7920-7925
41. Orthwein A, Patenaude A-M, Affar EB, Lamarre A, Young JC, Di Noia JM (2010) Regulation of activation-induced deaminase stability and antibody gene diversification by Hsp90. J Exp Med 207: 2751-2765
42. Pasqualucci L, Bhagat G, Jankovic M, Compagno M, Smith P, Muramatsu M, Honjo T, Morse III HC, Nussenzweig MC, Dalla-Favera R (2008) AID is required for germinal center-derived lymphomagenesis. Nat Genet 40: 108-112
43. Pasqualucci L, Guglielmino R, Houldsworth J, Mohr J, Aoufouchi S, Polakiewicz R, Chaganti RS, Dalla-Favera R (2004) Expression of the AID protein in normal and neoplastic B cells. Blood 104: 3318-3325 (Pubitemid 39507152)
44. Pasqualucci L, Neumeister P, Goossens T, Nanjangud G, Chaganti RS, Kuppers R, Dalla-Favera R (2001) Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 412: 341-346 (Pubitemid 32691848)
45. Patenaude AM, Di Noia JM (2010) The mechanisms regulating the subcellular localization of AID. Nucleus 1: 325-331
46. Patenaude AM, Orthwein A, Hu Y, Campo VA, Kavli B, Buschiazzo A, Di Noia JM (2009) Active nuclear import and cytoplasmic retention of activation-induced deaminase. Nat Struct Mol Biol 16: 517-527
47. Pauklin S, Sernández I, Bachmann G, Ramiro AR, Petersen-Mahrt SK (2009) Estrogen directly activates AID transcription and function. J Exp Med 206: 99-111
48. Peled JU, Kuang FL, Iglesias-Ussel MD, Roa S, Kalis SL, Goodman MF, Scharff MD (2008) The biochemistry of somatic hypermutation. Annu Rev Immunol 26: 481-511 (Pubitemid 351600383)
49. Picard D (2006) Chaperoning steroid hormone action. Trends Endocrinol Metab 17: 229-235 (Pubitemid 44164280)
50. Qiu X-B, Shao Y-M, Miao S, Wang L (2006) The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol Life Sci 63: 2560-2570 (Pubitemid 44800711)
51. Rada C, Di Noia JM, Neuberger MS (2004) Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation. Mol Cell 16: 163-171 (Pubitemid 39388832)
52. Ramiro AR, Jankovic M, Eisenreich T, Difilippantonio S, Chen-Kiang S, Muramatsu M, Honjo T, Nussenzweig A, Nussenzweig MC (2004) AID is required for c-myc/IgH chromosome translocations in vivo. Cell 118: 431-438 (Pubitemid 39485663)
53. Ramos PS, Williams AH, Ziegler JT, Comeau ME, Guy RT, Lessard CJ, Li H, Edberg JC, Zidovetzki R, Criswell LA, Gaffney PM, Graham DC, Graham RR, Kelly JA, Kaufman KM, Brown EE, Alarcón GS, Petri MA, Reveille JD, Mcgwin G et al (2011) Genetic analyses of interferon pathway-related genes reveal multiple new loci associated with systemic lupus erythematosus. Arthritis Rheum 63: 2049-2057
54. Revy P, Muto T, Levy Y, Geissmann F, Plebani A, Sanal O, Catalan N, Forveille M, Dufourcq-Labelouse R, Gennery A, Tezcan I, Ersoy F, Kayserili H, Ugazio AG, Brousse N, Muramatsu M, Notarangelo LD, Kinoshita K, Honjo T, Fischer A et al (2000) Activationinduced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 102: 565-575
55. Robbiani DF, Bothmer A, Callen E, Reina-San-Martin B, Dorsett Y, Difilippantonio S, Bolland DJ, Chen HT, Corcoran AE, Nussenzweig A, Nussenzweig MC (2008) AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell 135: 1028-1038
56. Robbiani DF, Bunting S, Feldhahn N, Bothmer A, Camps J, Deroubaix S, McBride KM, Klein IA, Stone G, Eisenreich TR, Ried T, Nussenzweig A, Nussenzweig MC (2009) AID produces DNA double-strand breaks in non-Ig genes and mature B cell lymphomas with reciprocal chromosome translocations. Mol Cell 36: 631-641
57. Sale JE, Calandrini DM, Takata M, Takeda S, Neuberger MS (2001) Ablation of XRCC2/3 transforms immunoglobulin V gene conversion into somatic hypermutation. Nature 412: 921-926 (Pubitemid 32821738)
58. Sebti SM, Der CJ (2003) Opinion: searching for the elusive targets of farnesyltransferase inhibitors. Nat Rev Cancer 3: 945-951 (Pubitemid 37500179)
59. Sernández IV, De Yébenes VG, Dorsett Y, Ramiro AR (2008) Haploinsufficiency of activation-induced deaminase for antibody diversification and chromosome translocations both in vitro and in vivo. PLoS ONE 3: e3927
60. Sha B, Lee S, Cyr DM (2000) The crystal structure of the peptidebinding fragment from the yeast Hsp40 protein Sis1. Structure 8: 799-807
61. Stavnezer J (2011) Complex regulation and function of activationinduced cytidine deaminase. Trends Immunol 32: 194-201
62. Stavnezer J, Guikema JEJ, Schrader CE (2008) Mechanism and regulation of class switch recombination. Annu Rev Immunol 26: 261-292 (Pubitemid 351600377)
63. Storck S, Aoufouchi S, Weill J-C, Reynaud C-A (2011) AID and partners: for better and (not) for worse. Curr Opin Immunol 23: 337-344
64. Takizawa M, Tolarová H, Li Z, Dubois W, Lim S, Callen E, Franco S, Mosaico M, Feigenbaum L, Alt FW, Nussenzweig A, Potter M, Casellas R (2008) AID expression levels determine the extent of cMyc oncogenic translocations and the incidence of B cell tumor development. J Exp Med 205: 1949-1957
65. Teng G, Hakimpour P, Landgraf P, Rice A, Tuschl T, Casellas R, Papavasiliou FN (2008) MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 28: 621-629
66. Terada K, Mori M (2000) Human DnaJ homologs dj2 and dj3, and bag-1 are positive cochaperones of hsc70. J Biol Chem 275: 24728-24734 (Pubitemid 30626575)
67. Terada K, Oike Y (2010) Multiple molecules of Hsc70 and a dimer of DjA1 independently bind to an unfolded protein. J Biol Chem 285: 16789-16797
68. Terada K, Yomogida K, Imai T, Kiyonari H, Takeda N, Kadomatsu T, Yano M, Aizawa S, Mori M (2005) A type I DnaJ homolog, DjA1, regulates androgen receptor signaling and spermatogenesis. EMBO J 24: 611-622 (Pubitemid 40343262)
69. Tzankov S, Wong MJH, Shi K, Nassif C, Young JC (2008) Functional divergence between co-chaperones of Hsc70. J Biol Chem 283: 27100-27109
70. Uchiyama Y, Takeda N, Mori M, Terada K (2006) Heat shock protein 40/DjB1 is required for thermotolerance in early phase. J Biochem 140: 805-812 (Pubitemid 46941010)
71. Walker VE, Wong MJ, Atanasiu R, Hantouche C, Young JC, Shrier A (2010) Hsp40 chaperones promote degradation of the HERG potassium channel. J Biol Chem 285: 3319-3329
72. Walsh P, saæ D, Law YC, Cyr DM, Lithgow T (2004) The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep 5: 567-571 (Pubitemid 39136416)
73. Wegele H, Wandinger SK, Schmid AB, Reinstein J, Buchner J (2006) Substrate transfer from the chaperone Hsp70 to Hsp90. J Mol Biol 356: 802-811 (Pubitemid 43139339)
74. Wu Y, Li J, Jin Z, Fu Z, Sha B (2005) The crystal structure of the Cterminal fragment of yeast Hsp40 Ydj1 reveals novel dimerization motif for Hsp40. J Mol Biol 346: 1005-1011 (Pubitemid 40215525)
75. Yamane A, Resch W, Kuo N, Kuchen S, Li Z, Sun H-W, Robbiani DF, McBride K, Nussenzweig MC, Casellas R (2011) Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat Immunol 12: 62-69
76. Young JC, Agashe VR, Siegers K, Hartl FU (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5: 781-791 (Pubitemid 39336272)
77. Young P, Anderton E, Paschos K, White R, Allday MJ (2008) Epstein-Barr virus nuclear antigen (EBNA) 3A induces the expression of and interacts with a subset of chaperones and co-chaperones. J Gen Virol 89: 866-877
78. Zaheen A, Martin A (2011) Activation-induced cytidine deaminase and aberrant germinal center selection in the development of humoral autoimmunities. Am J Pathol 178: 462-471