Insights into the lysine acetylproteome of human sperm

Journal of Proteomics

Volumn 109, Issue , 2014, Pages 199-211

  Sun, Guohai ^a   Jiang, Min ^a   Zhou, Tao ^a   Guo, Yueshuai ^a   Cui, Yiqiang ^a   Guo, Xuejiang ^a   Sha, Jiahao ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Acetylproteome; Capacitation; Human sperm; Lysine acetylation; Proteomics

Indexed keywords

HISTONE DEACETYLASE; LYSINE; NICOTINAMIDE; PROTEOME; TRICHOSTATIN A; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; ACYLTRANSFERASE INHIBITOR; ANTIBODY;

ACETYLATION; ACROSOME REACTION; ADULT; ANIMAL CELL; ARTICLE; BIOINFORMATICS; CARBOHYDRATE METABOLISM; CELL INTERACTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME INHIBITION; FERTILIZATION; FERTILIZATION IN VITRO; HUMAN; HUMAN CELL; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MALE; MALE FERTILITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEOMICS; SPERM; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY; TANDEM MASS SPECTROMETRY; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SPERMATOZOON; ANIMAL EXPERIMENT; INHIBITION KINETICS; OOCYTE; PROTEIN ACETYLATION; REGULATORY MECHANISM;

ACETYLATION; ACROSOME REACTION; ADULT; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; LYSINE; MALE; PROTEOME; SPERM MOTILITY; SPERMATOZOA;

EID: 84904898620     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.07.002     Document Type: Article

References (72)

1. Tulsiani D.R., Abou-Haila A. Molecular events that regulate mammalian fertilization. Minerva Ginecol 2011, 63:103-118.
2. Wykes S.M., Visscher D.W., Krawetz S.A. Haploid transcripts persist in mature human spermatozoa. Mol Hum Reprod 1997, 3:15-19.
3. Kota V., Dhople V.M., Shivaji S. Tyrosine phosphoproteome of hamster spermatozoa: role of glycerol-3-phosphate dehydrogenase 2 in sperm capacitation. Proteomics 2009, 9:1809-1826.
4. Wang G., Wu Y., Zhou T., Guo Y., Zheng B., Wang J., et al. Mapping of the N-linked glycoproteome of human spermatozoa. J Proteome Res 2013, 12:5750-5759.
5. Norris K.L., Lee J.Y., Yao T.P. Acetylation goes global: the emergence of acetylation biology. Sci Signal 2009, 2:pe76.
6. Close P., Creppe C., Gillard M., Ladang A., Chapelle J.P., Nguyen L., et al. The emerging role of lysine acetylation of non-nuclear proteins. Cell Mol Life Sci 2010, 67:1255-1264.
7. Lundby A., Lage K., Weinert B.T., Bekker-Jensen D.B., Secher A., Skovgaard T., et al. Proteomic analysis of lysine acetylation sites in rat tissues reveals organ specificity and subcellular patterns. Cell Rep 2012, 2:419-431.
8. Henriksen P., Wagner S.A., Weinert B.T., Sharma S., Bacinskaja G., Rehman M., et al. Proteome-wide analysis of lysine acetylation suggests its broad regulatory scope in Saccharomyces cerevisiae. Mol Cell Proteomics 2012, 11:1510-1522.
9. Wang G., Guo Y., Zhou T., Shi X., Yu J., Yang Y., et al. In-depth proteomic analysis of the human sperm reveals complex protein compositions. J Proteomics 2013, 79:114-122.
10. Hubbert C., Guardiola A., Shao R., Kawaguchi Y., Ito A., Nixon A., et al. HDAC6 is a microtubule-associated deacetylase. Nature 2002, 417:455-458.
11. +-dependent tubulin deacetylase. Mol Cell 2003, 11:437-444.
12. Schwer B., North B.J., Frye R.A., Ott M., Verdin E. The human silent information regulator (Sir)2 homologue hSIRT3 is a mitochondrial nicotinamide adenine dinucleotide-dependent deacetylase. J Cell Biol 2002, 158:647-657.
13. Ruiz-Pesini E., Diez-Sanchez C., Lopez-Perez M.J., Enriquez J.A. The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process?. Curr Top Dev Biol 2007, 77:3-19.
14. World Health Organization WHO laboratory manual for the examination and processing of human semen 2010, World Health Organization, Geneva. 5th ed.
15. Wang L., Chen W., Zhao C., Huo R., Guo X.J., Lin M., et al. The role of ezrin-associated protein network in human sperm capacitation. Asian J Androl 2010, 12:667-676.
16. Villen J., Gygi S.P. The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat Protoc 2008, 3:1630-1638.
17. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008, 26:1367-1372.
18. Magrane M., Consortium U. UniProt Knowledgebase: a hub of integrated protein data. Database (Oxford) 2011, 2011:bar009.
19. Colaert N., Helsens K., Martens L., Vandekerckhove J., Gevaert K. Improved visualization of protein consensus sequences by iceLogo. Nat Methods 2009, 6:786-787.
20. Zhou T., Zhou Z.M., Guo X.J. Bioinformatics for spermatogenesis: annotation of male reproduction based on proteomics. Asian J Androl 2013, 15:594-602.
21. Chen J., Bardes E.E., Aronow B.J., Jegga A.G. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res 2009, 37:W305-W311.
22. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13:2498-2504.
23. Wang J., Duncan D., Shi Z., Zhang B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res 2013, 41:77-83.
24. Jensen L.J., Kuhn M., Stark M., Chaffron S., Creevey C., Muller J., et al. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 2009, 37:D412-D416.
25. Letunic I., Doerks T., Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 2012, 40:D302-D305.
26. Yin L., Chung C.M., Huo R., Liu H., Zhou C., Xu W., et al. A sperm GPI-anchored protein elicits sperm-cumulus cross-talk leading to the acrosome reaction. Cell Mol Life Sci 2009, 66:900-908.
27. Lu C.T., Huang K.Y., Su M.G., Lee T.Y., Bretana N.A., Chang W.C., et al. DbPTM 3.0: an informative resource for investigating substrate site specificity and functional association of protein post-translational modifications. Nucleic Acids Res 2013, 41:D295-D305.
28. Weinert B.T., Wagner S.A., Horn H., Henriksen P., Liu W.R., Olsen J.V., et al. Proteome-wide mapping of the Drosophila acetylome demonstrates a high degree of conservation of lysine acetylation. Sci Signal 2011, 4:ra48.
29. Sylvestersen K.B., Young C., Nielsen M.L. Advances in characterizing ubiquitylation sites by mass spectrometry. Curr Opin Chem Biol 2013, 17:49-58.
30. Lin P., Sherman F. The unique hetero-oligomeric nature of the subunits in the catalytic cooperativity of the yeast Cct chaperonin complex. Proc Natl Acad Sci U S A 1997, 94:10780-10785.
31. Kouzarides T. Acetylation: a regulatory modification to rival phosphorylation?. EMBO J 2000, 19:1176-1179.
32. Yang X.J., Seto E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol Cell 2008, 31:449-461.
33. Beltrao P., Albanese V., Kenner L.R., Swaney D.L., Burlingame A., Villen J., et al. Systematic functional prioritization of protein posttranslational modifications. Cell 2012, 150:413-425.
34. Urner F., Sakkas D. Protein phosphorylation in mammalian spermatozoa. Reproduction 2003, 125:17-26.
35. Weinert B.T., Iesmantavicius V., Moustafa T., Scholz C., Wagner S.A., Magnes C., et al. Acetylation dynamics and stoichiometry in Saccharomyces cerevisiae. Mol Syst Biol 2014, 10:716.
36. Guan K.L., Xiong Y. Regulation of intermediary metabolism by protein acetylation. Trends Biochem Sci 2011, 36:108-116.
37. Newman J.C., He W., Verdin E. Mitochondrial protein acylation and intermediary metabolism: regulation by sirtuins and implications for metabolic disease. J Biol Chem 2012, 287:42436-42443.
38. Moellering R.E., Cravatt B.F. Functional lysine modification by an intrinsically reactive primary glycolytic metabolite. Science 2013, 341:549-553.
39. Wagner G.R., Payne R.M. Widespread and enzyme-independent Nepsilon-acetylation and Nepsilon-succinylation of proteins in the chemical conditions of the mitochondrial matrix. J Biol Chem 2013, 288:29036-29045.
40. Weinert B.T., Scholz C., Wagner S.A., Iesmantavicius V., Su D., Daniel J.A., et al. Lysine succinylation is a frequently occurring modification in prokaryotes and eukaryotes and extensively overlaps with acetylation. Cell Rep 2013, 4:842-851.
41. Palazzo A., Ackerman B., Gundersen G.G. Cell biology: tubulin acetylation and cell motility. Nature 2003, 421:230.
42. Janke C., Bulinski J.C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat Rev Mol Cell Biol 2011, 12:773-786.
43. Piperno G., Fuller M.T. Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J Cell Biol 1985, 101:2085-2094.
44. LeDizet M., Piperno G. Cytoplasmic microtubules containing acetylated alpha-tubulin in Chlamydomonas reinhardtii: spatial arrangement and properties. J Cell Biol 1986, 103:13-22.
45. Salmon N.A., Reijo Pera R.A., Xu E.Y. A gene trap knockout of the abundant sperm tail protein, outer dense fiber 2, results in preimplantation lethality. Genesis 2006, 44:515-522.
46. Roy A., Lin Y.N., Agno J.E., DeMayo F.J., Matzuk M.M. Absence of tektin 4 causes asthenozoospermia and subfertility in male mice. FASEB J 2007, 21:1013-1025.
47. Roy A., Lin Y.N., Agno J.E., DeMayo F.J., Matzuk M.M. Tektin 3 is required for progressive sperm motility in mice. Mol Reprod Dev 2009, 76:453-459.
48. Iida H., Honda Y., Matsuyama T., Shibata Y., Inai T. Tektin 4 is located on outer dense fibers, not associated with axonemal tubulins of flagella in rodent spermatozoa. Mol Reprod Dev 2006, 73:929-936.
49. Bunch D.O., Welch J.E., Magyar P.L., Eddy E.M., O'Brien D.A. Glyceraldehyde 3-phosphate dehydrogenase-S protein distribution during mouse spermatogenesis. Biol Reprod 1998, 58:834-841.
50. Welch J.E., Brown P.L., O'Brien D.A., Magyar P.L., Bunch D.O., Mori C., et al. Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells. J Androl 2000, 21:328-338.
51. Miki K., Qu W., Goulding E.H., Willis W.D., Bunch D.O., Strader L.F., et al. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci U S A 2004, 101:16501-16506.
52. Odet F., Duan C., Willis W.D., Goulding E.H., Kung A., Eddy E.M., et al. Expression of the gene for mouse lactate dehydrogenase C (Ldhc) is required for male fertility. Biol Reprod 2008, 79:26-34.
53. Danshina P.V., Geyer C.B., Dai Q., Goulding E.H., Willis W.D., Kitto G.B., et al. Phosphoglycerate kinase 2 (PGK2) is essential for sperm function and male fertility in mice. Biol Reprod 2010, 82:136-145.
54. Imai H., Suzuki K., Ishizaka K., Ichinose S., Oshima H., Okayasu I., et al. Failure of the expression of phospholipid hydroperoxide glutathione peroxidase in the spermatozoa of human infertile males. Biol Reprod 2001, 64:674-683.
55. Flohe L. Selenium in mammalian spermiogenesis. Biol Chem 2007, 388:987-995.
56. Ursini F., Heim S., Kiess M., Maiorino M., Roveri A., Wissing J., et al. Dual function of the selenoprotein PHGPx during sperm maturation. Science 1999, 285:1393-1396.
57. Naaby-Hansen S., Mandal A., Wolkowicz M.J., Sen B., Westbrook V.A., Shetty J., et al. CABYR, a novel calcium-binding tyrosine phosphorylation-regulated fibrous sheath protein involved in capacitation. Dev Biol 2002, 242:236-254.
58. Li Y.F., He W., Mandal A., Kim Y.H., Digilio L., Klotz K., et al. CABYR binds to AKAP3 and Ropporin in the human sperm fibrous sheath. Asian J Androl 2011, 13:266-274.
59. Li Y.F., He W., Kim Y.H., Mandal A., Digilio L., Klotz K., et al. CABYR isoforms expressed in late steps of spermiogenesis bind with AKAPs and ropporin in mouse sperm fibrous sheath. Reprod Biol Endocrinol 2010, 8:101.
60. Luconi M., Carloni V., Marra F., Ferruzzi P., Forti G., Baldi E. Increased phosphorylation of AKAP by inhibition of phosphatidylinositol 3-kinase enhances human sperm motility through tail recruitment of protein kinase A. J Cell Sci 2004, 117:1235-1246.
61. Hasegawa K., Ono T., Matsushita H., Shimono M., Noguchi Y., Mizutani Y., et al. A-kinase anchoring protein 3 messenger RNA expression in ovarian cancer and its implication on prognosis. Int J Cancer 2004, 108:86-90.
62. Jagan Mohanarao G., Atreja S.K. Identification of capacitation associated tyrosine phosphoproteins in buffalo (Bubalus bubalis) and cattle spermatozoa. Anim Reprod Sci 2011, 123:40-47.
63. Kong M., Diaz E.S., Morales P. Participation of the human sperm proteasome in the capacitation process and its regulation by protein kinase A and tyrosine kinase. Biol Reprod 2009, 80:1026-1035.
64. Foster J.A. Baby brother acrosin-binding protein (ACRBP) says, "look at me now!". Biol Reprod 2013, 88:106.
65. Foster J.A., Klotz K.L., Flickinger C.J., Thomas T.S., Wright R.M., Castillo J.R., et al. Human SP-10: acrosomal distribution, processing, and fate after the acrosome reaction. Biol Reprod 1994, 51:1222-1231.
66. Coonrod S.A., Herr J.C., Westhusin M.E. Inhibition of bovine fertilization in vitro by antibodies to SP-10. J Reprod Fertil 1996, 107:287-297.
67. Gincel D., Zaid H., Shoshan-Barmatz V. Calcium binding and translocation by the voltage-dependent anion channel: a possible regulatory mechanism in mitochondrial function. Biochem J 2001, 358:147-155.
68. Hinsch K.D., De Pinto V., Aires V.A., Schneider X., Messina A., Hinsch E. Voltage-dependent anion-selective channels VDAC2 and VDAC3 are abundant proteins in bovine outer dense fibers, a cytoskeletal component of the sperm flagellum. J Biol Chem 2004, 279:15281-15288.
69. Triphan X., Menzel V.A., Petrunkina A.M., Cassara M.C., Wemheuer W., Hinsch K.D., et al. Localisation and function of voltage-dependent anion channels (VDAC) in bovine spermatozoa. Pflugers Arch 2008, 455:677-686.
70. Zhang J., Wu J., Huo R., Mao Y., Lu Y., Guo X., et al. ERp57 is a potential biomarker for human fertilization capability. Mol Hum Reprod 2007, 13:633-639.
71. Hagaman J.R., Moyer J.S., Bachman E.S., Sibony M., Magyar P.L., Welch J.E., et al. Angiotensin-converting enzyme and male fertility. Proc Natl Acad Sci U S A 1998, 95:2552-2557.
72. Yu Y., Xu W., Yi Y.J., Sutovsky P., Oko R. The extracellular protein coat of the inner acrosomal membrane is involved in zona pellucida binding and penetration during fertilization: characterization of its most prominent polypeptide (IAM38). Dev Biol 2006, 290:32-43.