Expansion and functional diversification of a leucyl aminopeptidase family that encodes the major protein constituents of Drosophila sperm

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Dorus, Steve ^a   Wilkin, Elaine C ^a   Karr, Timothy L ^b  

^a University of Bath   (United Kingdom)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

spermproteomicsgene duplicationgene familyproteasespermatogenesis; testis

Indexed keywords

AMINOPEPTIDASE; CELL EXTRACT; CYTOSOL AMINOPEPTIDASE; DROSOPHILA PROTEIN;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; GENE; GENE DUPLICATION; GENE FUNCTION; GENETIC VARIABILITY; INSECT GENOME; MASS SPECTROMETRY; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NONHUMAN; PHYLOGENY; SPERM; SPERM LEUCYLAMINOPEPTIDASE GENE; TESTIS; TWO DIMENSIONAL GEL ELECTROPHORESIS; DROSOPHILA MELANOGASTER; LIMIT OF QUANTITATION; MALE; PROTEIN EXPRESSION; PROTEIN FUNCTION; TESTICULAR SPERM EXTRACTION; ANIMAL; COMPARATIVE GENOMIC HYBRIDIZATION; ENZYMOLOGY; GENE DOSAGE; GENETIC SELECTION; GENETICS; GENOME; METABOLISM; SPERMATOZOON;

HEXAPODA; MEROPS;

ANIMALS; COMPARATIVE GENOMIC HYBRIDIZATION; DROSOPHILA; DROSOPHILA PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EVOLUTION, MOLECULAR; GENE DOSAGE; GENOME, INSECT; LEUCYL AMINOPEPTIDASE; MALE; MASS SPECTROMETRY; MULTIGENE FAMILY; PHYLOGENY; SELECTION, GENETIC; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPERMATOZOA;

EID: 79953277607     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-171     Document Type: Article

References (59)

1. Ohno S. Evolution by gene duplication. 1970, Springer, Berlin, 1970.
2. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545. 1460548, 10101175.
3. Lynch M, Force A. The probability of duplicate gene preservation by subfunctionalization. Genetics 2000, 154:459-473. 1460895, 10629003.
4. Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science 2000, 290:1151-1155. 10.1126/science.290.5494.1151, 11073452.
5. Maston GA, Ruvolo M. Chorionic gonadotropin has a recent origin within primates and an evolutionary history of selection. Mol Biol Evol 2002, 19:320-335.
6. Brown CJ, Todd KM, Rosenzweig RF. Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol Biol Evol 1998, 15:931-942.
7. Dai HZ, Chen Y, Chen SD, Mao QY, Kennedy D, Landback P, Eyre-Walker A, Du W, Long MY. The evolution of courtship behaviors through the origination of a new gene in Drosophila. Proc Natl Acad Sci USA 2008, 105:7478-7483. 10.1073/pnas.0800693105, 2396706, 18508971.
8. Loppin B, Lepetit D, Dorus S, Couble P, Karr TL. Origin and neofunctionalization of a Drosophila paternal effect gene essential for zygote viability. Curr Biol 2005, 15:87-93. 10.1016/j.cub.2004.12.071, 15668163.
9. Kalamegham R, Sturgill D, Siegfried E, Oliver B. Drosophila mojoless, a retroposed GSK-3, has functionally diverged to acquire an essential role in male fertility. Mol Biol Evol 2007, 24:732-742. 10.1093/molbev/msl201, 2292417, 17179138.
10. Hahn MW, Han MV, Han SG. Gene family evolution across 12 Drosophila genomes. PLoS Genet 2007, 3:e197. 10.1371/journal.pgen.0030197, 2065885, 17997610.
11. Betran E, Thornton K, Long M. Retroposed new genes out of the X in Drosophila. Genome Res 2002, 12:1854-1859. 10.1101/gr.6049, 187566, 12466289.
12. Dorus S, Freeman ZN, Parker ER, Heath BD, Karr TL. Recent origins of sperm genes in Drosophila. Mol Biol Evol 2008, 25:2157-2166. 10.1093/molbev/msn162, 2727386, 18653731.
13. Emerson JJ, Kaessmann H, Betran E, Long M. Extensive gene traffic on the mammalian X chromosome. Science 2004, 303:537-540. 10.1126/science.1090042, 14739461.
14. Dorus S, Gilbert SL, Forster ML, Barndt RJ, Lahn BT. The CDY-related gene family: coordinated evolution in copy number, expression profile and protein sequence. Hum Mol Genet 2003, 12:1643-1650. 10.1093/hmg/ddg185, 12837688.
15. Marques AC, Dupanloup I, Vinckenbosch N, Reymond A, Kaessmann H. Emergence of young human genes after a burst of retroposition in primates. PLoS Biol 2005, 3:e357. 10.1371/journal.pbio.0030357, 1251493, 16201836.
16. Vinckenbosch N, Dupanloup I, Kaessmann H. Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci USA 2006, 103:3220-3225. 10.1073/pnas.0511307103, 1413932, 16492757.
17. Nurminsky DI, Nurminskaya MV, Benevolenskaya EV, Shevelyov YY, Hartl DL, Gvozdev VA. Cytoplasmic dynein intermediate-chain isoforms with different targeting properties created by tissue-specific alternative splicing. Mol Cell Biol 1998, 18:6816-6825. 109265, 9774695.
18. Dorus S, Busby SA, Gerike U, Shabanowitz J, Hunt DF, Karr TL. Genomic and functional evolution of the Drosophila melanogaster sperm proteome. Nat Genet 2006, 38:1440-1445. 10.1038/ng1915, 17099714.
19. Wigby S, Chapman T. Sex peptide causes mating costs in female Drosophila melanogaster. Curr Biol 2005, 15:316-321. 10.1016/j.cub.2005.01.051, 15723791.
20. Ravi Ram K, Sirot LK, Wolfner MF. Predicted seminal astacin-like protease is required for processing of reproductive proteins in Drosophila melanogaster. Proc Natl Acad Sci USA 2006, 103:18674-18679. 10.1073/pnas.0606228103, 1693721, 17116868.
21. Wong A, Albright SN, Giebel JD, Ram KR, Ji S, Fiumera AC, Wolfner MF. A role for Acp29AB, a predicted seminal fluid lectin, in female sperm storage in Drosophila melanogaster. Genetics 2008, 180:921-931. 10.1534/genetics.108.092106, 2567391, 18757944.
22. Dean MD, Clark NL, Findlay GD, Karn RC, Yi X, Swanson WJ, MacCoss MJ, Nachman MW. Proteomics and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus). Mol Biol Evol 2009, 26:1733-1743. 10.1093/molbev/msp094, 2734151, 19420050.
23. Wolfner MF. "S.P.E.R.M." (seminal proteins (are) essential reproductive modulators): the view from Drosophila. Soc Reprod Fertil 2007, 65:183-199.
24. Kelleher ES, Pennington JE. Protease gene duplication and proteolytic activity in Drosophila female reproductive tracts. Mol Biol Evol 2009, 26:2125-2134. 10.1093/molbev/msp121, 2734159, 19546158.
25. Dorus S, Evans PD, Wyckof GJ, Choi SS, Lahn BT. Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat Genet 2004, 36:1326-1329. 10.1038/ng1471, 15531881.
26. Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci USA 2001, 98:7375-7379. 10.1073/pnas.131568198, 34676, 11404480.
27. Parker GA. Selection on non-random fusion of gametes during the evolution of anisogamy. J Theor Biol 1978, 73:1-28. 10.1016/0022-5193(78)90177-7, 567721.
28. Rice WR. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 1996, 381:232-234. 10.1038/381232a0, 8622764.
29. Dorus S, Wasbrough ER, Busby J, Wilkin EC, Karr TL. Sperm proteomics reveals intensified selection on mouse sperm membrane and acrosome genes. Mol Biol Evol 2010, 27:1235-1246. 10.1093/molbev/msq007, 20080865.
30. Baker MA, Hetherington L, Reeves GM, Aitken RJ. The mouse sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identification. Proteomics 2008, 8:1720-1730. 10.1002/pmic.200701020, 18340633.
31. Stein KK, Go JC, Lane WS, Primakoff P, Myles DG. Proteomic analysis of sperm regions that mediate sperm-egg interactions. Proteomics 2006, 6:3533-3543. 10.1002/pmic.200500845, 16758446.
32. Rawlings ND, Barrett AJ, Bateman A. MEROPS: the peptidase database. Nucleic Acids Res 2010, 38:D227-33. 10.1093/nar/gkp971, 2808883, 19892822.
33. Wasbrough R, Dorus S, Hester S, Howard-Murkin J, Lilley KS, Wilkin E, Polpitiya A, Petritis K, Karr TL. The Drosophila melanogaster sperm proteome-II (DmSP-II). J Proteomics 2010, 73:2171-2185. 10.1016/j.jprot.2010.09.002, 20833280.
34. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25-29. 10.1038/75556, 3037419, 10802651.
35. Chintapalli VR, Wang J, Dow JA. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 2007, 39:715-720. 10.1038/ng2049, 17534367.
36. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567. 10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2, 10612281.
37. Saifuku K, Sekine T, Namihisa T, Takahashi T, Kanaoka Y. A novel fluorometric ultramicro determination of serum leucine aminopeptidase using a coumarine derivative. Clin Chim Acta 1978, 84:85-91. 10.1016/0009-8981(78)90479-5, 639319.
38. Kim H, Burley SK, Lipscomb WN. Re-refinement of the X-ray crystal structure of bovine lens leucine aminopeptidase complexed with bestatin. J Mol Biol 1993, 230:722-724. 10.1006/jmbi.1993.1193, 8478928.
39. Maric S, Donnelly SM, Robinson MW, Skinner-Adams T, Trenholme KR, Maric S, Donnelly SM, Robinsin MW, Skinner-Adams T, Trenholme KR, Gardiner DL, Dalton JP, Stack CM, Lowther J. The M17 leucine aminopeptidase of the malaria parasite Plasmodium falciparum: importance of active site metal ions in the binding of substrates and inhibitors. Biochemistry 2009, 48:5435-5439. 10.1021/bi9003638, 19408962.
40. Strater N, Sun L, Kantrowitz ER, Lipscomb WN. A bicarbonate ion as a general base in the mechanism of peptide hydrolysis by dizinc leucine aminopeptidase. Proc Natl Acad Sci USA 1999, 96:11151-11155. 10.1073/pnas.96.20.11151, 18002, 10500145.
41. Strater N, Sherratt DJ, Colloms SD. X-ray structure of aminopeptidase A from Escherichia coli and a model for the nucleoprotein complex in Xer site-specific recombination. EMBO J 1999, 18:4513-4522. 10.1093/emboj/18.16.4513, 1171526, 10449417.
42. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, et al. Evolution of genes and genomes on the Drosophila phylogeny. Nature 2007, 450:203-218. 10.1038/nature06341, 17994087.
43. Wang W, Zhang J, Alvarez C, Llopart A, Long M. The origin of the Jingwei gene and the complex modular structure of its parental gene, yellow emperor, in Drosophila melanogaster. Mol Biol Evol 2000, 17:1294-1301.
44. Long M, Langley CH. Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science 1993, 260:91-95. 10.1126/science.7682012, 7682012.
45. Schurko AM, Mazur DJ, Logsdon JMJ. Inventory and phylogenomic distribution of meiotic genes in Nasonia vitripennis and among diverse arthropods. Insect Mol Biol 2010, 19(Suppl 1):165-180. 10.1111/j.1365-2583.2009.00948.x, 20167026.
46. Fernandez D, Valdivia A, Irazusta J, Ochoa C, Casis L. Peptidase activities in human semen. Peptides 2002, 23:461-468. 10.1016/S0196-9781(01)00622-2, 11835995.
47. Schaller J, Glander HJ. Flow cytometric analysis of enzymes in live spermatozoa before and after cryostorage. Andrologia 2000, 32:357-364. 10.1046/j.1439-0272.2000.00362.x, 11131845.
48. Yasuhara T, Yokosawa H, Ishii S. Purification and characterization of an aminopeptidase from sperm of the sea urchin, Strongylocentrotus intermedius. Ca2(+)-dependent substrate specificity as a novel feature of the enzyme. J Biochem (Tokyo) 1990, 107:273-279.
49. Togo T, Morisawa M. GPI-anchored aminopeptidase is involved in the acrosome reaction in sperm of the mussel Mytilus edulis. Mol Reprod Dev 2004, 67:465-471. 10.1002/mrd.20037, 14991738.
50. Vibranovski MD, Lopes HF, Karr TL, Long M. Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet 2009, 5:e1000731. 10.1371/journal.pgen.1000731, 2770318, 19936020.
51. Jao SC, Huang LF, Hwang SM, Li WS. Tyrosine 387 and arginine 404 are critical in the hydrolytic mechanism of Escherichia coli aminopeptidase P. Biochemistry 2006, 45:1547-1553. 10.1021/bi051786m, 16460001.
52. Strater N, Lipscomb WN. Transition state analogue L-leucinephosphonic acid bound to bovine lens leucine aminopeptidase: X-ray structure at 1.65 A resolution in a new crystal form. Biochemistry 1995, 34:9200-9210. 10.1021/bi00028a033, 7619821.
53. Piatigorsky J. Gene Sharing and Evolution. 2007, Cambridge: Harvard University.
54. Matsui M, Fowler JH, Walling LL. Leucine aminopeptidases: diversity in structure and function. Biol Chem 2006, 387:1535-1544. 10.1515/BC.2006.191, 17132098.
55. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599. 10.1093/molbev/msm092, 17488738.
56. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574. 10.1093/bioinformatics/btg180, 12912839.
57. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
58. Pond SL, Frost SD, Muse SV. HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005, 21:676-679. 10.1093/bioinformatics/bti079, 15509596.
59. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002, 74:5383-5392. 10.1021/ac025747h, 12403597.