Evidence of amino acid diversity-enhancing selection within humans and among primates at the candidate sperm-receptor gene PKDREJ

American Journal of Human Genetics

Volumn 81, Issue 1, 2007, Pages 44-52

  Hamm, David ^a   Mautz, Brian S ^b   Wolfner, Mariana F ^c   Aquadro, Charles F ^c   Swanson, Willie J ^a,b,c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; EGG PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; FERTILITY; GENE; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC SELECTION; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; MAMMAL; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PKDREJ GENE; PRIMATE; PRIORITY JOURNAL; SPECIES COMPARISON; SPECIES DIFFERENCE; SPERM;

MAMMALIA; PRIMATES;

EID: 34347231337     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1086/518695     Document Type: Article

References (60)

1. GenBank, http://www.ncbi.nlm.nih.gov/Genbank/ (for PKDREJ [accession number NM_006071] and nonhuman primate PKDREJ sequences laccession numbers EF517278-EF517291])
2. Oxford Evolutionary Biology, http://evolve.zoo.ox.ac.uk/software .html?id=seal (for Se-Al sequence alignment editor)
3. SeattleSNPs, http://pga.gs.washington.edu/
4. Vacquier VD (1998) Evolution of gamete recognition proteins. Science 281:1995-1998
5. Swanson WJ, Vacquier VD (2002) Rapid evolution of reproductive proteins. Nat Rev Genet 3:137-144
6. Dean J (2004) Reassessing the molecular biology of sperm-egg recognition with mouse genetics. Bioessays 26:29-38
7. Wassarman PM (1999) Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell 96: 175-183
8. Kinloch RA, Sakai Y, Wassarman PM (1995) Mapping the mouse ZP3 combining site for sperm by exon swapping and site-directed mutagenesis. Proc Natl Acad Sci USA 92:263-267
9. Chen J, Litscher ES, Wassarman PM (1998) Inactivation of the mouse sperm receptor, mZP3, by site-directed mutagenesis of individual serine residues located at the combining site for sperm. Proc Natl Acad Sci USA 95:6193-6197
10. Rankin TL, Coleman JS, Epifano O, Hoodbhoy T, Turner SG, Castle PE, Lee E, Gore-Langton R, Dean J (2003) Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologs. Dev Cell 5: 33-43
11. Swanson WJ, Yang Z, Wolfner MF, Aquadro CF (2001) Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc Natl Acad Sci USA 98:2509-2514
12. Jansa SA, Lundrigan BL, Tucker PK (2003) Tests for positive-selection on immune and reproductive genes in closely related species of the murine genus Mus. J Mol Evol 56:294-307
13. Wassarman PM, Jovine L, Litscher ES (2001) A profile of fertilization in mammals. Nat Cell Biol 3:E59-E64
14. Wassarman PM, Jovine L, Litscher ES, Qi H, Williams Z (2004) Egg-sperm interactions at fertilization in mammals. Eur J Obstet Gynecol Reprod Biol Suppl 115:S57-S60
15. Galindo BE, Vacquier VD, Swanson WJ (2003) Positive selection in the egg receptor for abalone sperm lysin. Proc Natl Acad Sci USA 100:4639-4643
16. Hughes J, Ward CJ, Aspinwall R, Butler R, Harris PC (1999) Identification of a human homologue of the sea urchin receptor for egg jelly: a polycystic kidney disease-like protein. Hum Mol Genet 8:543-549
17. Gallagher AR, Hidaka S, Gretz N, Witzgall R (2002) Molecular basis of autosomal-dominant polycystic kidney disease. Cell Mol Life Sci 59:682-693
18. Hughes J, Ward CJ, Peral B, Aspinwall R, Clark K, San Millan JL, Gamble V, Harris PC (1995) The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat Genet 10:151-160
19. Moy GW, Mendoza LM, Schulz JR, Swanson WJ, Glabe CG, Vacquier VD (1996) The sea urchin sperm receptor for egg jelly is a modular protein with extensive homology to the human polycystic kidney disease protein, PKD1. J Cell Biol 133:809-817
20. Mengerink KJ, Moy GW, Vacquier VD (2002) suREJ3, a polycystin-1 protein, is cleaved at the GPS domain and localizes to the acrosomal region of sea urchin sperm. J Biol Chem 277:943-948
21. Butscheid Y, Chubanov V, Steger K, Meyer D, Dietrich A, Gudermann T (2006) Polycystic kidney disease and receptor for egg jelly is a plasma membrane protein of mouse sperm head. Mol Reprod Dev 73:350-360
22. Sutton KA, Jungnickel MK, Ward CJ, Harris PC, Florman HM (2006) Functional characterization of PKDREJ, a male germ cell-restricted polycystin. J Cell Physiol 209:493-500
23. Swanson WJ, Nielsen R, Yang Q (2003) Pervasive adaptive evolution in Mammalian fertilization proteins. Mol Biol Evol 20:18-20
24. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386
25. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150-163
26. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) release 3.6, Seattle
27. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818
28. Yang Z (2000) Phylogenetic Analysis by Maximum Likelihood (PAML). release 3.1, London
29. Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449
30. Yang Z, Wong WS, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107-1118
31. Dorus S, Evans PD, Wyckoff GJ, Choi SS, Lahn BT (2004) Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat Genet 36: 1326-1329
32. Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. 11. Error probabilities. Genome Res 8:186-194
33. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using Phred. 1. Accuracy assessment. Genome Res 8:175-185
34. Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195-202
35. 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
36. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978-989
37. Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175
38. Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857-5864
39. Ng PC, Henikoff S (2003) SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res 31:3812-3814
40. Ramensky V, Bork P, Sunyaev S (2002) Human non-synonymous SNPs: server and survey. Nucleic Acids Res 30:3894-3900
41. Goodman M (1999) The genomic record of humankind's evolutionary roots. Am J Hum Genet 64:31-39
42. Goodman M, Bailey WJ, Hayasaka K, Stanhope MJ, Slightom J, Czelusniak J (1994) Molecular evidence on primate phytogeny from DNA sequences. Am J Phys Anthropol 94:3-24
43. Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472-2479
44. Kingan SB, Tatar M, Rand DM (2003) Reduced polymorphism in the chimpanzee semen coagulating protein semenogelin 1. J Mol Evol 57:159-169
45. Przeworski M, Hudson RR, Di Rienzo A (2000) Adjusting the focus on human variation. Trends Genet 16:296-302
46. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654
47. Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197-218
48. McDonald JH (1996) Detecting non-neutral heterogeneity across a region of DNA sequence in the ratio of polymorphism to divergence. Mol Biol Evol 13:253-260
49. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595
50. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693-709
51. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405-1413
52. Kierszenbaum AL (2004) Polycystins: what polycystic kidney disease tells us about sperm. Mol Reprod Dev 67:385-388
53. Mengerink KJ, Moy GW, Vacquier VD (2000) suREJ proteins: new signalling molecules in sea urchin spermatozoa. Zygote Suppl 8:S28-S30
54. Frank SA (2000) Sperm competition and female avoidance of polyspermy mediated by sperm-egg biochemistry. Evol Ecol Res 2:613-625
55. Tsaur SC, Ting CT, Wu CI (2001) Sex in Drosophila mauritiana: a very high level of amino acid polymorphism in a male reproductive protein gene, Acp26Aa. Mol Biol Evol 18:22-26
56. Herndon LA, Wolfner MF (1995) A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating. Proc Natl Acad Sci USA 92:10114-10118
57. Aguade M, Miyashita N, Langley CH (1992) Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila. Genetics 132:755-770
58. Metz EC, Palumbi SR (1996) Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol Biol Evol 13:397-406
59. Vacquier VD, Moy GW (1977) Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs. Proc Natl Acad Sci USA 74:2456-2460
60. Gavrilets S, Waxman D (2002) Sympatric speciation by sexual conflict. Proc Natl Acad Sci USA 99:10533-10538