Ancient phylogenetic beginnings of immunoglobulin hypermutation

Journal of Molecular Evolution

Volumn 63, Issue 5, 2006, Pages 691-706

  Kubrycht, Jaroslav ^a   Sigler, Karel ^b   Růžička, Michal ^c   Souček, Pavel ^a   Borecký, Jiří ^d   Ježek, Petr ^c  

^a NATIONAL INSTITUTE OF PUBLIC HEALTH   (Czech Republic)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^c INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^d UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

BLAST; CDR1; Domain similarity; Geodia cydonium; Hypermutation; Immunoglobulin; Primordial building block; Protein kinase substrate; Template

Indexed keywords

CELL ADHESION MOLECULE; ENZYME; IMMUNOGLOBULIN; LYMPHOCYTE ANTIGEN RECEPTOR; SPONGE ADHESION MOLECULE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM; CARBOXY TERMINAL SEQUENCE; COELOMATA; COMPLEMENTARITY DETERMINING REGION; COMPLEMENTARITY DETERMINING REGION 1; GENE MUTATION; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC CONSERVATION; GEODIA; IMMUNOGLOBULIN GENE; IMMUNOGLOBULIN HYPERMUTATION; IMMUNOGLOBULIN STRUCTURE; IMMUNOGLOBULIN VARIABLE REGION; METAZOON; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMORDIAL BUILDING BLOCK; PROTEIN DOMAIN; PROTEOBACTERIA; SEQUENCE HOMOLOGY; SPECIES COMPARISON; SPONGE (PORIFERA); STRUCTURE ANALYSIS; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; COMPUTATIONAL BIOLOGY; DNA MUTATIONAL ANALYSIS; EVOLUTION, MOLECULAR; GENES, IMMUNOGLOBULIN; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; SEQUENCE ALIGNMENT;

ANIMALIA; COELOMATA; GEODIA CYDONIUM; MAMMALIA; METAZOA; VERTEBRATA;

EID: 33751508841     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-006-0051-9     Document Type: Article

References (108)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402
2. Azumi K, De Santis R, De Tomaso A , Rigoutsos I, Yoshizaki F, Pinto MR, Marino R, Shida K, Ikeda M, Ikeda M, Arai M, Inoue Y, Shimizu T, Satoh N, Rokhsar DS, Du Pasquier L, Kasahara M, Satake M, Nonaka M (2003) Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: "Waiting for Godot." Immunogenetics 55:570-581
3. Banerjee M, Mehr R, Belelovsky A, Spencer J, Dunn-Walters DK (2002) Age- and tissue-specific differences in human germinal center B cell selection revealed by analysis of IgVH gene hypermutation and lineage trees. Eur J Immunol 32:1947-1957
4. Beale RCL, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS (2004) Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J Mol Biol 337:585-596
5. Bernstein RM, Schluter SF, Bernstein H, Marchalonis JJ (1996a) Primordial emergence of the recombination activating gene 1 (RAG1): sequence of the complete shark gene indicates homology to microbial integrases. Proc Natl Acad Sci USA 93:9454-9459
6. Bernstein RM, Schluter SF, Shen S, Marchalonis JJ (1996b) A new high molecular weight immunoglobulin class from the carcharhine shark: implications for the properties of the primordial immunoglobulin. Proc Natl Acad Sci USA 93:3289-3293
7. Bjedov I, Lecointre G, Tenaillon O, Vaury C, Radman M, Taddei F, Denamur E, Matic I (2003) Polymorphism of genes encoding SOS polymerases in natural populations of Escherichia coli. DNA Repair 2:417-426
8. Blumbach B, Diehl-Seifert B, Seack J, Steffen R, Muller IM, Muller WEG (1999) Cloning and expression of new receptors belonging to the immunoglobulin superfamily from the marine sponge Geodia cydonium. Immunogenetics 49:751-763
9. Boursier L, Su W, Spencer J (2004) Analysis of strand biased 'G'.C hypermutation in human immunoglobulin V(lambda) gene segments suggests that both DNA strands are targets for deamination by activation-induced cytidine deaminase. Mol Immunol 40:1273-1278
10. Bradshaw PS, Condie A, Matutes E, Catovsky D, Yuille MR (2002) Breakpoints in the ataxia telangiectasia gene arise at the RGYW somatic hypermutation motif. Gene 21:483-487
11. Bray N, Pachter L (2004) MAVID: constrained ancestral alignment of multiple sequences. Genome Res 14:693-699
12. Brotcorne-Lannoye A, Maenhaut-Michel G (1986) Role of RecA protein in untargeted UV mutagenesis of bacteriophage lambda: evidence for the requirement for the dinB gene. Proc Natl Acad Sci USA 83:3904-3908
13. Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol 3:1200-1207
14. Cannon JP, Haire RN, Pancer Z, Mueller MG, Skapura D, Cooper MD, Litman GW (2005) Variable domains and a VpreB-like molecule are present in jawless vertebrate. Immunogenetics 56:924-929
15. Chiang SC, Ali V, Huang AL, Chu KY, Lee ST (2001) Molecular, cellular and functional characterization of a novel ICAM-like molecule of the immunoglobulin superfamily from Leishmania mexicana amazonensis. Mol Biochem Parasitol 112:263-275
16. Chiang SC, Chang SC, Lee ST (2002) ICAM-L gene is conserved only in Leishmania species in the family of kinetoplastida. Mol Biochem Parasitol 124:47-50
17. China B, Jacquemin E, Devrin A-C, Pirson V, Mainil J (1999) Heterogeneity of the eae genes in attaching/effacing Escherichia coli from cattle: comparison with human strains. Res Microbiol 150:323-332
18. Deppenmeier U, Johann A, Hartsch T, Merkl R, Schmitz RA, Martinez-Arias R, Henne A, Weizer A, Baumer S, Jakobi C, Bruggemann H, Lienard T, Christmann A, Bomeke M, Steckel S, Bhattacharya A, Lykidis A, Overbeek R, Klenk HP Gunsalus RP, Fritz HJ, Gottschalk G (2002) The genome of Methanosarcina mazei: evidence for lateral gene transfer between Bacteria and Archaea. J Mol Microbiol Biotechnol 4:453-461
19. Dersch P, Isberg RR (2000) An immunoglobulin superfamily-like domain unique to the Yersinia pseudotuberculosis invasin protein is required for stimulation of bacterial uptake via integrin receptors. Infect Immun 68:2930-2938
20. Diaz M, Flajnik MF (1998) Evolution of somatic hypermutation and gene conversion in adaptive immunity. Immunol Rev 162:13-24
21. Diaz M, Velez J, Singh M, Cerny J, Flajnik MF (1999) Mutational pattern of the nurse shark antigen receptor gene (NAR) is similar to that of mammalian Ig genes and to spontaneous mutations in evolution: the translesion synthesis model of somatic hypermutation. Internat Immunol 11:825-833
22. Diaz M, Watson NB, Turkington G, Verkoczy LK, Klinman NR, McGregor WG (2003) Decreased frequency and highly aberrant spectrum of ultraviolet-induced mutations in the hprt gene of mouse fibroblast expressing antisense RNA to DNA polymerase zeta. Mol Cancer Res 1:836-847
23. Di Noia JM, Neuberger MS (2004) Immunoglobulin gene conversion in chicken DT40 cells largely proceeds through an abasic site intermediate generated by excision of the uracil produced by AID-mediated deoxycytidine deamination. Eur J Immunol 34:504-508
24. Dorner T, Brezinschek H-P, Brezinschek RI, Foster SJ, Domiati-Saad R, Lipsky PE (1997) Analysis of the frequency and pattern of somatic mutations within nonproductively rearranged human variable heavy chain genes. J Immunol 158:2779-2789
25. Dorner T, Foster SJ, Farner NL, Lipsky PE (1998a) Somatic hypermutation of human immunoglobulin heavy chain genes: targeting of RGYW motifs on both DNA strands. Eur J Immunol 28:3384-3396
26. Dorner T, Foster SJ, Brezinschek H-P, Lipsky PE (1998b) Analysis of the targeting of the hypermutational machinery and the impact of subsequent selection on the distribution of nucleotide changes in human VHDJH rearrangements. Immunol Rev 162:161-171
27. Du Pasquier L, Zucchetti I, De Santis R (2004) Immunoglobulin superfamily receptors in protochordates: before RAG time. Immunol Rev 198:233-248
28. Duquette ML, Pham P, Goodman MF, Maizels N (2005) AID binds to transcription-induced structures in c-MYC, that map to regions associated with translocation and hypermutation. Oncogene 24:5791-5798
29. Faili A, Aoufouchi S, Flatter E, Gueranger Q, Reynaud C-A, Weill JC (2002) Induction of somatic hypermutation in immunoglobulin genes is depedent on DNA polymerase iota. Nature 419:944-947
30. Faili A, Aoufouchi S, Weller S, Vuillier F, Stary A, Sarasin A, Reynaud C-A, Weill JC (2004) DNA polymerase eta is involved in hypermutation occurring during immunoglobulin class switch recombination. J Exp Med 199:265-270
31. Gordon MS, Kanegai CM, Doerr JR, Wall R (2003) Somatic hypermutation of the B cell receptor genes B29 (Igb, CD79b) and mb1(Iga, CD79a). Proc Natl Acad Sci USA 100:4126-4131
32. Halaby DM, Mornon JPE (1998) The immunoglobulin superfamily: an insight on its tissular, species, and functional diversity. J Mol Evol 46:389-400
33. Hoek RM, Smit AB, Frings H, Vink JM, de Jong-Brink M Geraerts WPM (1996) A new Ig-superfamily member, molluscan defence molecule (MDM) from Lymnaea stagnalis, is down-regulated during parasitosis. Eur J Immunol 26:939-944
34. Huang TW, Tien AC, Huang WS, Lee YC, Peng CL, Tseng CL, Kao CY, Huang CY (2004) POINT: a database for the prediction of protein-protein interactions based on the orthologous interactome. Bioinformatics 20:3273-3276
35. Ito T, Chiba T, Yoshida M (2001) Exploring the protein interactome using comprehensive two-hybrid projects. Trends Biotechnol 19:S23-S27
36. James LC, Roversi P, Tawfik DS (2003) Antibody multispecificity mediated by conformational diversity. Science 299:1362-1367
37. Jing H, Takagi J, Liu JH, Lindgren S, Zhang RG, Joachimiak A, Wang JH, Springer TA (2002) Archaeal surface layer proteins contain beta propeller, PKD, and beta helix domains and are related to metazoan cell surface proteins. Structure 10:1453-1464
38. Kabat EA, Wu TT, Perry HM, Gottesman KS, Foeller C (1991) Sequences of proteins of immunological interest. NIH publication No. 91-3242. NIH, Bethesda, MD
39. Kim WK, Bolser DM, Park JH (2004) Large scale co-evolution analysis of protein structural interlogues using the global protein structural interactome map (PSIMAP). Bioinformatics 20:1138-1150
40. Klasen M, Spillman FJX, Lorens JB, Wabl M (2005) Retroviral vectors to monitor somatic hypermutation. J Immunol Methods 300:47-62
41. Kubrycht J, Sigler K (1997) Animal membrane receptors and adhesive molecules. Crit Rev Biotechnol 17:123-147
42. Kubrycht J, Borecký J, Sigler K (2002) Sequence similarities of protein kinase peptide substrates. Comparison of their primary structures with immunoglobulin repeats. Folia Microbiol 47:319-358
43. Kubrycht J, Borecký J, Souček P, Ježek P (2004) Sequence similarities of protein kinase substrates and inhibitors with immunoglobulins and model immunoglobulin homologue: cell adhesion molecule from the living fossil sponge Geodia cydonium. Mapping of coherent database similarities and implications for evolution of CDR1 and hypermutation. Folia Microbiol 49:219-246
44. Lee SS, Tranchina D, Ohta Y, Flajnik MF, Hsu E (2002) Hypermutation in shark immunoglobulin light chain genes results contiguous substitutions. Immunity 16:571-582
45. Lepš J (1996) Biostatistics. University of Southern Bohemia, Ceske Budejovice, Czech Republic
46. Lindstrom-Dinnetz I, Sun SC, Faye I (1995) Structure and expression of hemolin, an insect member of the immunoglobulin gene superfamily. Eur J Biochem 230:920-925
47. Litman GW, Anderson MK, Rast JP (1999) Evolution of antigen receptors. Annu Rev Immunol 17:109-147
48. Lossos IS, Levy R, Alizadeh AA (2004) AID is expressed in germinal B-cell-like and activated B-cell-like diffuse large-cell lymphomas and is not correlated with intraclonal heterogeneity. Leukemia 18:1775-1779
49. Malpeli G, Barbi S, Moore PS, Scardoni M, Chilosi M, Scarpa A, Menestrina F (2004) Primary mediastinal B-cell lymphoma: hypermutation of the Bcl6 gene targets motifs different from those in diffuse large B-cell and follicular lymphomas. Haematologica 89:1091-1099
50. Marchalonis JJ, Schluter SF (1998) A stochastic model for the rapid emergence of specific vertebrate immunity incorporating horizontal transfer of systems enabling duplication and combinational diversification. J Theor Biol 193:429-444
51. Marchalonis JJ, Kaveri S, Lacroix-Desmazes S, Kazatchine MD (2002) Natural recognition repertoire and the evolutionary emergence of the combinatorial immune system. FASEB J 16:842-848
52. Marchler-Bauer A, Panchenko AR, Shoemaker BA, Thiessen PA, Geer LY, Bryant SH (2002) CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res 30:281-283
53. Morelli C, Karayianni E, Magnanini C, Mungall AJ, Thorland E, Negrini M, Smith DI, Barbanti-Brodano G (2002) Cloning and characterization of the common fragile site FRAF6F, harboring a replicative senescence gene and frequently deleted in human tumors. Oncogene 21:7266-7276
54. Muller WEG (1998) Origin of Metazoa: sponges as living fossils. Naturwissenschften 85:11-25
55. Muller WEG, Schroder HC, Skorokhod A, Bunz C, Muller IM, Grebenjuk VA (2001) Contribution of sponge genes to unravel the genome of the hypothetical ancestor of Metazoa (Urmetazoa). Gene 276:161-173
56. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Schinkai Y, Honjo T (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553-563
57. Notredame C (2003) Recent progress in multiple sequence alignments: a survey. Available at: http//:www.isrec.isb-sib.ch/~cschmid/DEA/Module5/lectures/ 4.2.msa_algorithms.pdf
58. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and nature of bacterial innovation. Nature 405:299-304
59. Ohno S, Matsunaga T, Wallace RB (1982) Identification of 48-base-long primordial building block sequence of mouse immunoglobulin variable region genes. Proc Natl Acad Sci USA 79:1999-2002
60. Okazaki I-M, 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
61. Oprea M, Kepler TB (1999) Genetic plasticity of V genes under somatic hypermutation: statistical analyses using a new resampling-based methodology. Genome Res 9:1294-1304
62. Oprea M, Cowell LG, Kepler TB (2001) The targeting of somatic hypermutation closely resembles that of meiotic mutation. J Immunol 166:892-899
63. Pancer Z, Mayer WS, Klein J, Cooper MD (2004) Prototypic T cell receptor and CD4-like coreceptor are expressed by lymphocytes in the agnathan sea lamprey. Proc Natl Acad Sci USA 101:13273-13278
64. Park D, Lee S, Bolser DM, Schroeder M, Lappe M, Oh D, Bhak J (2005) Comparative interactomics analysis of protein family interaction networks using PSIMAP (protein structural interactome map). Bioinformatics 21:3234-3240
65. Petersen-Mahrt SK, Harris RS, Neuberger MS (2002) AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418:99-103
66. Poltoratsky VP, Wilson SH, Kunkel TA, Pavlov YI (2004) Recombinogenic phenotype of human activation-induced cytosine deaminase. J Immunol 172:4308-4313
67. Potter M, Padlan E, Rudikoff S (1976) Localized deletion-insertion mutations: a major factor in the evolution of immunoglobulin structural variability. J Immunol 117:626-629
68. Rada C, Yelamos J, Dean W, Milstein C (1997) The 5′ hypermutation boundary of kappa chains is independent of local and neighbouring sequences and related to the distance from the initiation of transcription. Eur J Immunol 27:3115-3120
69. Ray JL, Nielsen KM (2005) Experimental methods for assaying natural transformation and inferring horizontal gene transfer. Methods Enzymol 395:491-520
70. Reuven NB, Arad G, Maor-Shoshani A, Livneh Z (1999) The mutagenesis protein UmuC is a DNA polymerase activated by UmuD, RecA, and SSB and is specialized for translesion replication. J Biol Chem 274:31763-31766
71. Riazuddin S, Khan SN, Ahmed ZM, Ghosh M, Caution K, Nazli S, Kabra M, Zafar AU, Chen K, Naz S, Antonellis A, Pavan WJ, Green ED, Wilcox ER, Friedman PL, Morrel RJ, Riazuddin S, Friedman TB (2006) Mutations in TRIOBP, which encodes a putative cytoskeletal-organizing protein, are associated with nonsyndromic recessive deafness. Am J Hum Genet 78:137-143
72. Rogozin IB, Diaz M (2004) Cutting Edge: DGYW/WRCH is a better predictor of mutability at G:C bases in Ig hypermutation than the widely accepted RGYW/WRCY motif and probably reflects a two-step activation-induced cytidine demainase-triggered process. J Immunol 172:3382-3384
73. Rogozin IB, Kolchanov NA (1992) Somatic hypermutagenesis in immunoglobulin genes II. Influence of neighbouring base sequences on mutagenesis. Biochim Biophys Acta 1171:11-18
74. Rossenu S, Dewitte D, Vandekerckhove J, Ampe C (1997) A phage display technique for a fast, sensitive and systematic investigation of protein-protein interactions. J Protein Chem 16:499-503
75. Rumfelt LL, Lohr RL, Dooley H, Flajnik MF (2004) Diversity and repertoire of IgW and IgM VH families in the newborn nurse shark. BMC Immunol 5:8
76. Sato A, Mayer WE, Klein J (2003) A molecule bearing an immunoglobulin-like V region of the CTX subfamily in amphioxus. Immunogenetics 55:423-427
77. Schaffer AA, Aravind L, Madden TL, Shavirin S, Spouge JL, Wolf YI, Koonin EV, Altschul SF (2001) Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and the other refinements. Nucleic Acids Res 29:2994-3005
78. Schatz DG (2004) Antigen receptor genes and the evolution of a recombinase. Semin Immunol 16:245-256
79. Schluter SF, Bernstein RM, Marchalonis JJ (1997) Molecular origins and evolution of immunoglobulin heavy-chain genes of jawed vertebrates. Immunol Today 18:543-549
80. Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097-6100
81. Schutze J, Skorokhod A, Muller IM, Muller WEG (2001) Molecular evolution of the metazoan extracellular matrix: cloning and expression of structural proteins from the demosponges Suberites domuncula and Geodia cydonium. J Mol Evol 53:402-415
82. Shapiro GS, Ellison MC, Wysocki LJ (2003) Sequence-specific targeting of two bases on both DNA strands by the somatic hypermutation mechanism. Mol Immunol 40:287-295
83. Shen HM, Peters A, Baron B, Zhu X, Storb U (1998) Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes. Science 280:1750-1752
84. Sheppard DC, Yeaman MR, Welch WH, Phan QT, Fu Y, Ibrahim AS, Filler SG, Zhang M, Waring AJ, Edwards JE Jr (2004) Functional and structural diversity in the Als protein family of Candida albicans. J Biol Chem 279:30480-30489
85. Simhadri S, Kramata P, Zajc B, Sayer JM, Jerina DM, Hinkle DC, Wei CS (2002) Benzo[a]pyrene diol epoxide-deoxyguanosine adducts are accurately bypassed by yeast DNA polymerase zeta in vitro. Mutat Res 508:137-145
86. Simossis VA, Kleinjung J, Heringa J (2005) Homology-extended sequence alignment. Nucleic Acids Res 33:816-824
87. Simpson LJ, Sale JE (2003) Rev1 is essential for DNA damage tolerance and non-templated immunoglobulin gene mutation in a vertebrate cell line. EMBO J 22:1654-1664
88. Sitnikova T, Su C (1998) Coevolution of immunoglobulin heavy- and light-chain variable-region gene families. Mol Biol Evol 15:617-625
89. Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228:1315-1317
90. Suzuki T, Shin-I T, Kohara Y, Kasahara M (2004) Transcriptome analysis of hagfish leukocytes: a framework for understanding the immune system of jawless fishes. Dev Comp Immunol 28:993-1003
91. Teichmann SA, Chothia C (2000) Immunoglobulin superfamily proteins in Caenorhabditis elegans. J Mol Biol 296:1367-1383
92. Tilson MD, Rzhetsky A (2000) A novel hypothesis regarding the evolutionary origins of the immunoglobulin fold. Curr Med Res Opin 16:88-93
93. van den Berg TK, Yoder JA, Litman GW (2004) On the origins of adaptive immunity: innate immune receptors join the tale. Trends Immunol 25:11-16
94. Vogel C, Teichmann SA, Chothia C (2003) The immunoglobulin superfamily in Drosophila melanogaster and Caenorhabditis elegans and the evolution of complexity. Development 130:6317-6328
95. Washington MT, Johnson RE, Prakash L, Prakash S (2003) The mechanism of nucleotide incorporation by human DNA polymerase eta differs from that of the yeast enzyme. Mol Cell Biol 23:8316-8322
96. Wedekind JE, Dance GSC, Sowden MP, Smith HC (2003) Messenger RNA editing in mammals: new members of the APOBEC family seeking roles in the family business. Trends Genet 19:207-216
97. Wiens M, Mangoni A, D'Esposito M, Fattorusso E, Korchagina N, Schroder HC, Grebenjuk VA, Krasko A, Batel R, Muller IM, Muller WEG (2003) The molecular basis for the evolution of the metazoan bodyplan: extracellular matrix-mediated morphogenesis in marine demosponges. J Mol Evol 57:S60-S75
98. Williams AF, Barclay AN (1988) The immunoglobulin superfamily-domains for cell surface recognition. Annu Rev Immunol 6:381-405
99. Wojciechowicz D, Lu CF, Kurjan J, Lipke PN (1993) Cell surface anchorage and ligand-binding domains of the Saccharomyces cerevisae cell adhesion protein alpha-agglutinin, a member of the immunoglobulin superfamily. Mol Cell Biol 13:2554-2563
100. Wright BE, Schmidt KH, Minnick MF (2004) Mechanism by which transcription can regulate somatic hypermutation. Genes Immun 5:176-182
101. Yang C, Carlow D, Wolfenden R, Short SA (1992) Cloning and nucleotide sequence of the Escherichia coli cytidine deaminase (ccd) gene. Biochemistry 31:4168-4174
102. Yang W (2005) Portraits of a Y-family DNA polymerase. FEBS Lett 579:868-872
103. Yu XQ, Kanost MR (2002) Binding of hemolin to bacterial lipopolysaccharide and lipoteichoic acid. An immunoglobulin superfamily member from insects as a pattern-recognition receptor. Eur J Biochem 269:1827-1834
104. Zarrin AA, Alt FW, Chaudhuri J, Stokes N, Kaushal D, Du Pasquier L, Tian M (2004) An evolutionarily conserved target for immunoglobulin class-switch recombination. Nat Immunol 5:1275-1281
105. Zeng X, Negrete GA, Kasmer C, Yang WW, Gearhart PJ (2004) Absence of DNA polymerase eta reveals targeting of C mutations on the nontranscribed strand in immunoglobulin switch regions. J Exp Med 199:917-924
106. Zhang WL, Kohler B, Oswald E, Beutin L, Karch H, Morabito S, Caprioli A, Sauerbaum S, Schmidt H (2002) Genetic diversity of intimin genes of attaching and effacing Escherichia coli strains. J Clin Microbiol 40:4486-4492
107. Zhang Z, Schaffer AA, Miller W, Madden TL, Lipman DJ, Koonin EV, Altschul SF (1998) Protein sequence similarity searches using pattern as seeds. Nucleic Acids Res 26:3986-3990
108. Zvárová J (2001) Biomedical statistics. I. The fundamentals of statistics for biomedical fields. Karolinum, Prague, Czech Republic