Comparative genomic analysis of a mammalian β-defensin gene cluster

Physiological Genomics

Volumn 30, Issue 3, 2007, Pages 213-222

  Radhakrishnan, Yashwanth ^a   Fares, Mario A ^b   French, Frank S ^a   Hall, Susan H ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Antimicrobial; Evolution; Gene duplication; Gene expression; Immunity; Positive selection; Reproduction

Indexed keywords

BETA DEFENSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMOSOME; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENE LOCUS; GENETIC SELECTION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; GENOMICS; HOST RESISTANCE; MALE; MAMMAL; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPRODUCTION; RHESUS MONKEY; RODENT; SPECIES COMPARISON; UROGENITAL SYSTEM;

AMINO ACID SEQUENCE; ANIMALS; BETA-DEFENSINS; FEMALE; GENOMICS; HUMANS; ISOELECTRIC POINT; MALE; MAMMALS; MICE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TISSUE DISTRIBUTION;

MAMMALIA; PRIMATES; RATTUS; RODENTIA;

EID: 34548057323     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00263.2006     Document Type: Article

References (87)

1. Akashi H. Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination. Genetics 151: 221-238, 1999.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 215: 403-410, 1990.
3. Antcheva N, Boniotto M, Zelezetsky I, Pacor S, Verga Falzacappa MV, Crovella S, Tossi A. Effects of positively selected sequence variations in human and Macaca fascicularis beta-defensins 2 on antimicrobial activity. Antimicrob Agents Chemother 48: 685-688, 2004.
4. Boniotto M, Antcheva N, Zelezetsky I, Tossi A, Palumbo V, Verga Falzacappa MV, Sgubin S, Braida L, Amoroso A, Crovella S. A study of host defence peptide beta-defensin 3 in primates. Biochem J 374: 707-714, 2003.
5. Boniotto M, Tossi A, DelPero M, Sgubin S, Antcheva N, Santon D, Masters J, Crovella S. Evolution of the beta defensin 2 gene in primates. Genes Immun 4: 251-257, 2003.
6. Bourque G, Pevzner PA, Tesler G. Reconstructing the genomic architecture of ancestral mammals: lessons from human, mouse, and rat genomes. Genome Res 14: 507-516, 2004.
7. Brinkmann H, Philippe H. Archaea sister group of Bacteria? Indications from tree reconstruction artifacts in ancient phylogenies. Mol Biol Evol 16: 817-825, 1999.
8. Chen CI, Schaller-Bals S, Paul KP, Wahn U, Bals R. Beta-defensins and LL-37 in bronchoalveolar lavage fluid of patients with cystic fibrosis. J Cyst Fibros 3: 45-50, 2004.
9. Com E, Bourgeon F, Evrard B, Ganz T, Colleu D, Jegou B, Pineau C. Expression of antimicrobial defensins in the male reproductive tract of rats, mice, and humans. Biol Reprod 68: 95-104, 2003.
10. Crandall KA, Kelsey CR, Imamichi H, Lane HC, Salzman NP. Parallel evolution of drug resistance in HIV: failure of nonsynonymous/synonymous substitution rate ratio to detect selection. Mol Biol Evol 16: 372-382, 1999.
11. Del Pero M, Boniotto M, Zuccon D, Cervella P, Spano A, Amoroso A, Crovella S. Beta-defensin 1 gene variability among non-human primates. Immunogenetics 53: 907-913, 2002.
12. Eichler EE, Sankoff D. Structural dynamics of eukaryotic chromosome evolution. Science 301: 793-797, 2003.
13. Fares MA. SWAPSC: sliding window analysis procedure to detect selective constraints. Bioinformatics 20: 2867-2868, 2004.
14. Fares MA, Elena SF, Ortiz J, Moya A, Barrio E. A sliding window-based method to detect selective constraints in protein-coding genes and its application to RNA viruses. J Mol Evol 55: 509-521, 2002.
15. Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3: 710-720, 2003.
16. Gilad Y, Oshlack A, Smyth GK, Speed TP, White KP. Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440: 242-245, 2006.
17. Goldman MJ, Anderson GM, Stolzenberg ED, Kari UP, Zasloff M, Wilson JM. Human beta-defensin-1 is a salt-sensitive antibiotic in lung that is inactivated in cystic fibrosis. Cell 88: 553-560, 1997.
18. Hall SH, Hamil KG, French FS. Host defense proteins of the male reproductive tract. J Androl 23: 585-597, 2002.
19. Hamil KG, Liu Q, Sivashanmugam P, Anbalagan M, Yenugu S, Soundararajan R, Grossman G, Rao AJ, Birse CE, Ruben SM, Richardson RT, Zhang YL, O'Rand MG, Petrusz P, French FS, Hall SH. LCN6, a novel human epididymal lipocalin. Reprod Biol Endocrinol 1: 112, 2003.
20. Hancock RE, Chapple DS. Peptide antibiotics. Antimicrob Agents Chemother 43: 1317-1323, 1999.
21. Harder J, Schroder JM. Psoriatic scales: a promising source for the isolation of human skin-derived antimicrobial proteins. J Leukoc Biol 77: 476-486, 2005.
22. Hedges SB. The origin and evolution of model organisms. Nat Rev Genet 3: 838-849, 2002.
23. Huang H, Winter EE, Wang H, Weinstock KG, Xing H, Goodstadt L, Stenson PD, Cooper DN, Smith D, Alba MM, Ponting CP, Fechtel K. Evolutionary conservation and selection of human disease gene orthologs in the rat and mouse genomes. Genome Biol 5: R47, 2004.
24. Hughes AL. Gene duplication and the origin of novel proteins. Proc Natl Acad Sci USA 102: 8791-8792, 2005.
25. Hughes AL, Yeager M. Coordinated amino acid changes in the evolution of mammalian defensins. J Mol Evol 44: 675-682, 1997.
26. Huttner KM, Kozak CA, Bevins CL. The mouse genome encodes a single homolog of the antimicrobial peptide human beta-defensin 1. FEBS Lett 413: 45-49, 1997.
27. Jia HP, Mills JN, Barahmand-Pour F, Nishimura D, Mallampali RK, Wang G, Wiles K, Tack BF, Bevins CL, McCray PB Jr. Molecular cloning and characterization of rat genes encoding homologues of human beta-defensins. Infect Immun 67: 4827-4833, 1999.
28. Jia HP, Wowk SA, Schutte BC, Lee SK, Vivado A, Tack BF, Bevins CL, McCray PB Jr. A novel murine beta-defensin expressed in tongue, esophagus, and trachea. J Biol Chem 275: 33314-33320, 2000.
29. Kelley J, Walter L, Trowsdale J. Comparative genomics of major histocompatibility complexes. Immunogenetics 56: 683-695, 2005.
30. Kimura M. Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267: 275-276, 1977.
31. Koonin EV, Rogozin IB. Getting positive about selection. Genome Biol 4: 331, 2003.
32. Kopelman NM, Lancet D, Yanai I. Alternative splicing and gene duplication are inversely correlated evolutionary mechanisms. Nat Genet 37: 588-589, 2005.
33. Kumar S, Tamura K, Nei M. MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150-163, 2004.
34. Lehrer RI. Primate defensins. Nat Rev Microbiol 2: 727-738, 2004.
35. Li P, Chan HC, He B, So SC, Chung YW, Shang Q, Zhang YD, Zhang YL. An antimicrobial peptide gene found in the male reproductive system of rats. Science 291: 1783-1785, 2001.
36. Li WH. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36: 96-99, 1993.
37. Liu Q, Hamil KG, Sivashanmugam P, Grossman G, Soundararajan R, Rao AJ, Richardson RT, Zhang YL, O'Rand MG, Petrusz P, French FS, Hall SH. Primate epididymis-specific proteins: characterization of ESC42, a novel protein containing a trefoil-like motif in monkey and human. Endocrinology 142: 4529-4539, 2001.
38. Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155, 2000.
39. Lynn DJ, Lloyd AT, Fares MA, O'Farrelly C. Evidence of positively selected sites in mammalian alpha-defensins. Mol Biol Evol 21: 819-827, 2004.
40. Menke DB, Page DC. Sexually dimorphic gene expression in the developing mouse gonad. Gene Expr Patterns 2: 359-367, 2002.
41. Miller W, Makova KD, Nekrutenko A, Hardison RC. Comparative genomics. Annu Rev Genomics Hum Genet 5: 15-56, 2004.
42. Modrek B, Lee CJ. Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and/or loss. Nat Genet 34: 177-180, 2003.
43. Morrison GM, Semple CA, Kilanowski FM, Hill RE, Dorin JR. Signal sequence conservation and mature peptide divergence within subgroups of the murine beta-defensin gene family. Mol Biol Evol 20: 460-470, 2003.
44. Mouse Genome Sequencing Consortium. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562, 2002.
45. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426, 1986.
46. Nei M, Kumar S. Molecular Evolution and Phylogenetics. Oxford, UK: Oxford Univ. Press, 2000.
47. Nei M, Rooney AP. Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39: 121-152, 2005.
48. Nguyen TX, Cole AM, Lehrer RI. Evolution of primate theta-defensins: a serpentine path to a sweet tooth. Peptides 24: 1647-1654, 2003.
49. Nielsen H, Engelbrecht J, Brunak S, von Heijne G. A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int J Neural Syst 8: 581-599, 1997.
50. Nielsen R. Comparative genomics: difference of expression. Nature 440: 161, 2006.
51. Niyonsaba F, Ogawa H, Nagaoka I. Human beta-defensin-2 functions as a chemotactic agent for tumour necrosis factor-alpha-treated human neutrophils. Immunology 111: 273-281, 2004.
52. O'Brien SJ, Menotti-Raymond M, Murphy WJ, Nash WG, Wienberg J, Stanyon R, Copeland NG, Jenkins NA, Womack JE, Marshall Graves JA. The promise of comparative genomics in mammals. Science 286: 458-462, 479-481, 1999.
53. Patil AA, Cai Y, Sang Y, Blecha F, Zhang G. Cross-species analysis of the mammalian beta-defensin gene family: presence of syntenic gene clusters and preferential expression in the male reproductive tract. Physiol Genomics 23: 5-17, 2005.
54. Radhakrishnan Y, Hamil KG, Yenugu S, Young SL, French FS, Hall SH. Identification, characterization, and evolution of a primate beta-defensin gene cluster. Genes Immun 6: 203-210, 2005.
55. Rat Genome Sequencing Project Consortium. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428: 493-521, 2004.
56. Rodriguez-Jimenez FJ, Krause A, Schulz S, Forssmann WG, Conejo-Garcia JR, Schreeb R, Motzkus D. Distribution of new human beta-defensin genes clustered on chromosome 20 in functionally different segments of epididymis. Genomics 81: 175-183, 2003.
57. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425, 1987.
58. Schroder JM, Harder J. Human beta-defensin-2. Int J Biochem Cell Biol 31: 645-651, 1999.
59. Schutte BC, Mitros JP, Bartlett JA, Walters JD, Jia HP, Welsh MJ, Casavant TL, McCray PB Jr. Discovery of five conserved beta-defensin gene clusters using a computational search strategy. Proc Natl Acad Sci USA 99: 2129-2133, 2002.
60. Semple CA, Maxwell A, Gautier P, Kilanowski FM, Eastwood H, Barran PE, Dorin JR. The complexity of selection at the major primate beta-defensin locus. BMC Evol Biol 5: 32, 2005.
61. Semple CA, Rolfe M, Dorin JR. Duplication and selection in the evolution of primate beta-defensin genes. Genome Biol 4: R31, 2003.
62. Sharp PM. In search of molecular darwinism. Nature 385: 111-112, 1997.
63. Suzuki Y, Gojobori T. A method for detecting positive selection at single amino acid sites. Mol Biol Evol 16: 1315-1328, 1999.
64. Suzuki Y, Nei M. Simulation study of the reliability and robustness of the statistical methods for detecting positive selection at single amino acid sites. Mol Biol Evol 19: 1865-1869, 2002.
65. Swanson WJ, Nielsen R, Yang Q. Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20: 18-20, 2003.
66. Swanson WJ, Vacquier VD. The rapid evolution of reproductive proteins. Nat Rev Genet 3: 137-144, 2002.
67. Takahashi K, Nei M. Efficiencies of fast algorithms of phylogenetic inference under the criteria of maximum parsimony, minimum evolution, and maximum likelihood when a large number of sequences are used. Mol Biol Evol 17: 1251-1258, 2000.
68. Tollner TL, Yudin AI, Treece CA, Overstreet JW, Cherr GN. Macaque sperm release ESP13.2 and PSP94 during capacitation: the absence of ESP132 is linked to sperm-zona recognition and binding. Mol Reprod Dev 69: 325-337, 2004.
69. Torgerson DG, Kulathinal RJ, Singh RS. Mammalian sperm proteins are rapidly evolving: evidence of positive selection in functionally diverse genes. Mol Biol Evol 19: 1973-1980, 2002.
70. Valen LV. A new evolutionary law. Evol Theory 1: 1-30, 1973.
71. Vallender EJ, Lahn BT. Positive selection on the human genome. Hum Mol Genet 13: R245-R254, 2004.
72. Wyckoff GJ, Wang W, Wu CI. Rapid evolution of male reproductive genes in the descent of man. Nature 403: 304-309, 2000.
73. Xiao Y, Hughes AL, Ando J, Matsuda Y, Cheng JF, Skinner-Noble D, Zhang G. A genome-wide screen identifies a single beta-defensin gene cluster in the chicken: implications for the origin and evolution of mammalian defensins. BMC Genomics 5: 56, 2004.
74. Yamaguchi Y, Nagase T, Makita R, Fukuhara S, Tomita T, Tominaga T, Kurihara H, Ouchi Y. Identification of multiple novel epididymis-specific beta-defensin isoforms in humans and mice. J Immunol 169: 2516-2523, 2002.
75. Yamamoto M, Matsui Y. Testis-specific expression of a novel mouse defensin-like gene, Tdl. Mech Dev 116: 217-221, 2002.
76. Yang D, Biragyn A, Hoover DM, Lubkowski J, Oppenheim JJ. Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol 22: 181-215, 2004.
77. Yang D, Chertov O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, Anderson M, Schroder JM, Wang JM, Howard OM, Oppenheim JJ. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286: 525-528, 1999.
78. Yang Z, Nielsen R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17: 32-43, 2000.
79. Yenugu S, Chintalgattu V, Wingard CJ, Radhakrishnan Y, French FS, Hall SH. Identification, cloning and functional characterization of novel beta-defensins in the rat (Rattus norvegicus). Reprod Biol Endocrinol 4: 7, 2006.
80. Yenugu S, Hamil KG, French FS, Hall SH. Antimicrobial actions of the human epididymis 2 (HE2) protein isoforms, HE2alpha, HE2beta1 and HE2beta2. Reprod Biol Endocrinol 2: 61, 2004.
81. Yenugu S, Hamil KG, Radhakrishnan Y, French FS, Hall SH. The androgen-regulated epididymal sperm-binding protein, human beta-defensin 118 (DEFB118) (formerly ESC42), is an antimicrobial beta-defensin. Endocrinology 145: 3165-3173, 2004.
82. Yeo GW, Van Nostrand E, Holste D, Poggio T, Burge CB. Identification and analysis of alternative splicing events conserved in human and mouse. Proc Natl Acad Sci USA 102: 2850-2855, 2005.
83. Yudin AI, Generao SE, Tollner TL, Treece CA, Overstreet JW, Cherr GN. Beta-defensin 126 on the cell surface protects sperm from immunorecognition and binding of anti-sperm antibodies. Biol Reprod 73: 1243-1252, 2005.
84. Yudin AI, Tollner TL, Li MW, Treece CA, Overstreet JW, Cherr GN. ESP13.2, a member of the beta-defensin family, is a macaque sperm surface-coating protein involved in the capacitation process. Biol Reprod 69: 1118-1128, 2003.
85. Zaballos A, Villares R, Albar JP, Martinez AC, Marquez G. Identification on mouse chromosome 8 of new beta-defensin genes with regionally specific expression in the male reproductive organ. J Biol Chem 279: 12421-12426, 2004.
86. Zhou CX, Zhang YL, Xiao L, Zheng M, Leung KM, Chan MY, Lo PS, Tsang LL, Wong HY, Ho LS, Chung YW, Chan HC. An epididymis-specific beta-defensin is important for the initiation of sperm maturation. Nat Cell Biol 6: 458-464, 2004.
87. Zhu L, Swergold GD, Seldin MF. Examination of sequence homology between human chromosome 20 and the mouse genome: intense conservation of many genomic elements. Hum Genet 113: 60-70, 2003.