Sequence diversity at the proximal 14q32.1 SERPIN subcluster: Evidence for natural selection favoring the pseudogenization of SERPINA2

Molecular Biology and Evolution

Volumn 24, Issue 2, 2007, Pages 587-598

  Seixas, Susana ^a,b   Suriano, Gianpaolo ^a,c   Carvalho, Filipa ^c   Seruca, Raquel ^a,c   Rocha, Jorge ^a   Di Rienzo, Anna ^b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF CHICAGO   (United States)

^c University of Porto   (Portugal)

Author keywords

Natural selection; Pseudogenization; SERPIN

Indexed keywords

SERINE PROTEASE INHIBITOR A2; SERINE PROTEASE INHIBITOR A6; SERINE PROTEINASE INHIBITOR; TRANSCORTIN; UNCLASSIFIED DRUG;

AFRICA; APE; ARTICLE; CHIMPANZEE; COMPARATIVE GENE MAPPING; CONTROLLED STUDY; EUROPE; FREQUENCY ANALYSIS; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HOMOZYGOSITY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; MULTIGENE FAMILY; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIMATE; PROTEIN FAMILY; PSEUDOGENE; SAMPLE; SEQUENCE HOMOLOGY;

AFRICA; ALPHA 1-ANTITRYPSIN; ANIMALS; CHROMOSOMES, HUMAN, PAIR 14; EUROPE; HAPLOTYPES; HOMINIDAE; HUMANS; MULTIGENE FAMILY; PAN TROGLODYTES; PROTEIN CONFORMATION; PSEUDOGENES; SELECTION (GENETICS); SERPINS;

HOMINIDAE; PAN; PRIMATES;

EID: 33846805804     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msl187     Document Type: Article

References (76)

1. Adams AM, Hudson RR. 2004. Maximum-likelihood estimation of demographicparametersusingthe frequencyspectrumofunlinked single-nucleotide polymorphisms. Genetics. 168:1699-1712.
2. Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, Nickerson DA, Kruglyak L. 2004. Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol. 2:e286.
3. Asch HL, Dresden MH. 1977. Schistosoma mansoni: inhibition of cercarial "penetration" proteases by components of mammalian blood. Comp Biochem Physiol B. 58:89-95.
4. Atchley WR, Lokot T, Wollenberg K, Dress A, Ragg H. 2001. Phylogenetic analyses of amino acid variation in the serpin proteins. Mol Biol Evol. 18:1502-1511.
5. Bao JJ, Reed-Fourquet L, Sifers RN, Kidd VJ, Woo SL. 1988. Molecular structure and sequence homology of a gene related to alpha 1-antitrypsin in the human genome. Genomics. 2:165-173.
6. Carrell RW, Lomas DA. 2002. Alpha1-antitrypsin deficiency - a model for conformational diseases. N Engl J Med. 346:45-53.
7. Clark NL, Swanson WJ. 2005. Pervasive adaptive evolution in primate seminal proteins. PLoS Genet. 1:e35.
8. Conrad DF, Andrews TD, Carter NP, Hurles ME, Pritchard JK. 2006. A high-resolution survey of deletion polymorphism in the human genome. Nat Genet. 38:75-81.
9. Cox DW. 1995. α1-antitrypsin deficiency. In: Sriver CR, Beaudet AL, Sly WL, Valle D, editors. The metabolic and molecular bases of inherited disease. New York: McGraw-Hill. p. 4125-4158.
10. Crawford DC, Akey DT, Nickerson DA. 2005. The patterns of natural variation in human genes. Annu Rev Genomics Hum Genet. 6:287-312.
11. Creighton TE, Darby NJ. 1989. Functional evolutionary divergence of proteolytic enzymes and their inhibitors. Trends Biochem Sci. 14:319-324.
12. Currat M, Trabuchet G, Rees D, Perrin P, Harding RM, Clegg JB, Langaney A, Excoffier L. 2002. Molecular analysis of the beta-globin gene cluster in the Niokholo Mandenka population reveals a recent origin of the beta(S) Senegal mutation. Am J Hum Genet. 70:207-223.
13. Feuk L, Carson AR, Scherer SW. 2006. Structural variation in the human genome. Nat Rev Genet. 7:85-97.
14. Forney JR, Yang S, Healey MC. 1996. Protease activity associated with excystation of Cryptosporidium parvum oocysts. J Parasitol. 82:889-892.
15. Forney JR, Yang S, Healey MC. 1997. Synergistic anticryptosporidial potential of the combination alpha-1-antitrypsin and paromomycin. Antimicrob Agents Chemother. 41:2006-2008.
16. Freudenstein-Dan A, Gold D, Fishelson Z. 2003. Killing of schistosomes by elastase and hydrogen peroxide: implications for leukocyte-mediated schistosome killing. J Parasitol. 89:1129-1135.
17. Frisse L, Hudson RR, Bartoszewicz A, Wall JD, Donfack J, Di Rienzo A. 2001. Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am J Hum Genet. 69:831-843.
18. Gaillard MC, Zwi S, Nogueira CM, Ludewick H, Feldman C, Frankel A, Tsilimigras C, Kilroe-Smith TA. 1994. Ethnic differences in the occurrence of the M1(ala213) haplotype of alpha-1-antitrypsin in asthmatic and non-asthmatic black and white South Africans. Clin Genet. 45:122-127.
19. Gaubin M, Autiero M, Basmaciogullari S, Metivier D, Misëhal Z, Culerrier R, Oudin A, Guardiola J, Piatier-Tonneau D. 1999. Potent inhibition of CD4/TCR-mediated T cell apoptosis by a CD4-binding glycoprotein secreted from breast tumor and seminal vesicle cells. J Immunol. 162:2631-2638.
20. Goodwin RL, Baumann H, Berger FG. 1996. Patterns of divergence during evolution of alpha 1-proteinase inhibitors in mammals. Mol Biol Evol. 13:346-358.
21. Hamblin MT, Di Rienzo A. 2000. Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am J Hum Genet. 66:1669-1679.
22. Hayakawa T, Aki I, Varki A, Satta Y, Takahata N. 2006. Fixation of the human-specific CMP-N-acetylneuraminic acid hydroxylase pseudogene and implications of haplotype diversity for human evolution. Genetics. 172:1139-1146.
23. Hayes VM, Gardiner-Garden M. 2003. Are polymorphic markers within the alpha-1-antitrypsin gene associated with risk of human immunodeficiency virus disease? J Infect Dis. 188:1205-1208.
24. Hill RE, Hastie ND. 1987. Accelerated evolution in the reactive centre regions of serine protease inhibitors. Nature. 326:96-99.
25. Hinds DA, Kloek AP, Jen M, Chen X, Frazer KA. 2006. Common deletions and SNPs are in linkage disequilibrium in the human genome. Nat Genet. 38:82-85.
26. Hinds DA, Stuve LL, Nilsen GB, Halperin E, Eskin E, Ballinger DG, Frazer KA, Cox DR. 2005. Whole-genome patterns of common DNA variation in three human populations. Science. 307:1072-1079.
27. Hofker MH, Nelen M, Klasen EC, Nukiwa T, Curiel D, Crystal RG, Frants RR. 1988. Cloning and characterization of an alpha 1-antitrypsin like gene 12 KB downstream of the genuine alpha 1-antitrypsin gene. Biochem Biophys Res Commun. 155:634-642.
28. Hudson RR. 2001. Two-locus sampling distributions and their application. Genetics. 159:1805-1817.
29. Hudson RR. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics. 18:337-338.
30. Hudson RR, Bailey K, Skarecky D, Kwiatowski J, Ayala FJ. 1994. Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics. 136:1329-1340.
31. Irving JA, Pike RN, Lesk AM, Whisstock JC. 2000. Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res. 10:1845-1864.
32. Irving JA, Steenbakkers PJ, Lesk AM, Op den Camp HJ, Pike RN, Whisstock JC. 2002. Serpins in prokaryotes. Mol Biol Evol. 19:1881-1890.
33. Kelsey GD, Parkar M, Povey S. 1988. The human alpha-1-antitrypsin-related sequence gene: isolation and investigation of its expression. Ann Hum Genet. 52:151-160.
34. Kong A, Gudbjartsson DF, Sainz J, et al. (16 co-authors). 2002. A high-resolution recombination map of the human genome. Nat Genet. 31:241-247.
35. Lomas DA, Carrell RW. 2002. Serpinopathies and the conformational dementias. Nat Rev Genet. 3:759-768.
36. Marsden MD, Fournier RE. 2005. Organization and expression of the human serpin gene cluster at 14q32.1. Front Biosci. 10:1768-1778.
37. McCarroll SA, Hadnott TN, Perry GH, et al. (11 co-authors). 2006. Common deletion polymorphisms in the human genome. Nat Genet. 38:86-92.
38. Namciu SJ, Friedman RD, Marsden MD, Sarausad LM, Jasoni CL, Fournier RE. 2004. Sequence organization and matrix attachment regions of the human serine protease inhibitor gene cluster at 14q32.1. Mamm Genome. 15:162-178.
39. Needham M, Stockley RA. 2004. Alpha 1-antitrypsin deficiency. 3: clinical manifestations and natural history. Thorax. 59:441-445.
40. Nickerson DA, Tobe VO, Taylor SL. 1997. PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing. Nucleic Acids Res. 25:2745-2751.
41. Nukiwa T, Brantly M, Ogushi F, Fells G, Satoh K, Stier L, Courtney M, Crystal RG. 1987. Characterization of the M1(Ala213) type of alpha 1-antitrypsin, a newly recognized, common "normal" alpha 1-antitrypsin haplotype. Biochemistry. 26:5259-5267.
42. Nukiwa T, Seyama K, Kira S. 1996. The prevalence of a1AT deficiency outside the United States and Europe. In: Crystal RG, editor. Alpha-1-antitrypsin deficiency. Biology, pathogenesis, clinical manifestations, therapy. New York: Marcel Dekker Inc. p. 293-300.
43. Olson MV. 1999. When less is more: gene loss as an engine of evolutionary change. Am J Hum Genet. 64:18-23.
44. Puente XS, Gutierrez-Fernandez A, Ordonez GR, Hillier LW, Lopez-Otin C. 2005. Comparative genomic analysis of human and chimpanzee proteases. Genomics. 86:638-647.
45. Puente XS, Lopez-Otin C. 2004. A genomic analysis of rat proteases and protease inhibitors. Genome Res. 14:609-622.
46. Puente XS, Sanchez LM, Gutierrez-Fernandez A, Velasco G, Lopez-Otin C. 2005. A genomic view of the complexity of mammalian proteolytic systems. Biochem Soc Trans. 33:331-334.
47. Ramensky V, Bork P, Sunyaev S. 2002. Human non-synonymous SNPs: server and survey. Nucleic Acids Res. 30:3894-3900.
48. Rompler H, Schulz A, Pitra C, Coop G, Przeworski M, Paabo S, Schoneberg T. 2005. The rise and fall of the chemoattractant receptor GPR33. J Biol Chem. 280:31068-31075.
49. Rozas J, Rozas R. 1997. DnaSP version 2.0: a novel software package for extensive molecular population genetics analysis. Comput Appl Biosci. 13:307-311.
50. Sabeti PC, Reich DE, Higgins JM, et al. (17 co-authors). 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature. 419:832-837.
51. Schenkels LC, Walgreen-Weterings E, Oomen LC, Bolscher JG, Veerman EC, Nieuw Amerongen AV. 1997. In vivo binding of the salivary glycoprotein EP-GP (identical to GCDFP-15) to oral and non-oral bacteria detection and identification of EP-GP binding species. Biol Chem. 378:83-88.
52. Sebat J, Lakshmi B, Troge J, et al. (21 co-authors). 2004. Large-scale copy number polymorphism in the human genome. Science. 305:525-528.
53. Seixas S, Ferrand N, Rocha J. 2002. Microsatellite variation and evolution of the human Duffy blood group polymorphism. Mol Biol Evol. 19:1802-1806.
54. Seixas S, Garcia O, Trovoada MJ, Santos MT, Amorim A, Rocha J. 2001. Patterns of haplotype diversity within the serpin gene cluster at 14q32.1: insights into the natural history of the alpha1-antitrypsin polymorphism. Hum Genet. 108:20-30.
55. Serre D, Nadon R, Hudson TJ. 2005. Large-scale recombination rate patterns are conserved among human populations. Genome Res. 15:1547-1552.
56. Shapiro L, Pott GB, Ralston AH. 2001. Alpha-1-antitrypsin inhibits human immunodeficiency virus type 1. FASEB J. 15:115-122.
57. Sharp AJ, Locke DP, McGrath SD, et al. (14 co-authors). 2005. Segmental duplications and copy-number variation in the human genome. Am J Hum Genet. 77:78-88.
58. Smith CL, Power SG, Hammond GL. 1992. A Leu-His substitution at residue 93 in human corticosteroid binding globulin results in reduced affinity for cortisol. J Steroid Biochem Mol Biol. 42:671-676.
59. Stajich JE, Hahn MW. 2005. Disentangling the effects of demography and selection in human history. Mol Biol Evol. 22:63-73.
60. Stein PE, Carrell RW. 1995. What do dysfunctional serpins tell us about molecular mobility and disease? Nat Struct Biol. 2:96-113.
61. Stephens M, Donnelly P. 2003. A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet. 73:1162-1169.
62. Stephens M, Smith NJ, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 68:978-989.
63. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 123:585-595.
64. Teshima KM, Coop G, Przeworski M. 2006. How reliable are empirical genomic scans for selective sweeps? Genome Res. 16:702-712.
65. Tishkoff SA, Varkonyi R, Cahinhinan N, et al. (17 co-authors). 2001. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science. 293:455-462.
66. Tomas G, Seco L, Seixas S, Faustino P, Lavinha J, Rocha J. 2002. The peopling of Sao Tome (Gulf of Guinea): origins of slave settlers and admixture with the Portuguese. Hum Biol. 74:397-411.
67. Torpy DJ, Bachmann AW, Gartside M, Grice JE, Harris JM, Clifton P, Easteal S, Jackson RV, Whitworth JA. 2004. Association between chronic fatigue syndrome and the corticosteroid-binding globulin gene ALA SER224 polymorphism. Endocr Res. 30:417-429.
68. Tuzun E, Sharp AJ, Bailey JA, et al. (12 co-authors). 2005. Fine-scale structural variation of the human genome. Nat Genet. 37:727-732.
69. van Gent D, Sharp P, Morgan K, Kalsheker N. 2003. Serpins: structure, function and molecular evolution. Int J Biochem Cell Biol. 35:1536-1547.
70. Voight BF, Adams AM, Frisse LA, Qian Y, Hudson RR, Di Rienzo A. 2005. Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci. 102:18508-18513.
71. Voight BF, Kudaravalli S, Wen X, Pritchard JK. 2006. A map of recent positive selection in the human genome. PLoS Biol. 4:e72.
72. Wall JD, Przeworski M. 2000. When did the human population size start increasing? Genetics. 155:1865-1874.
73. Wang X, Grus WE, Zhang J. 2006. Gene losses during human origins. PLoS Biol. 4:e52.
74. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 7:256-276.
75. [WHO] World Health Organization. 1997. Alpha 1-antitrypsin deficiency: memorandum from a WHO meeting. Bull W H O. 75:397-415.
76. Xue Y, Daly A, Yngvadottir B, et al. (14 co-authors). 2006. Spread of an inactive form of caspase-12 in humans is due to recent positive selection. Am J Hum Genet. 78:659-670.