Human spermatozoa as a model for detecting missing proteins in the context of the chromosome-centric human proteome project

Journal of Proteome Research

Volumn 14, Issue 9, 2015, Pages 3606-3620

  Jumeau, Fanny ^a,f   Com, Emmanuelle ^b,c   Lane, Lydie ^d,e   Duek, Paula ^e   Lagarrigue, Mélanie ^b,c   Lavigne, Régis ^b,c   Guillot, Laëtitia ^b,c   Rondel, Karine ^b,c   Gateau, Alain ^e   Melaine, Nathalie ^b,c   Guével, Blandine ^b,c   Sergeant, Nicolas ^f   Mitchell, Valérie ^a   Pineau, Charles ^b,c  

^a Rouen Normandy University Hospital   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c Faculté de Médecine   (France)

^d UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^e SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^f UNIV LILLE   (France)

Author keywords

chromosome 14; chromosome 2; human proteome project; mass spectrometry proteomics; missing proteins; spermatozoon

Indexed keywords

ADULT; AMINO ACID SEQUENCE; ARTICLE; CELL MOTILITY; CHROMOSOME; CHROMOSOME 14; CHROMOSOME 2; GENE REPRESSION; GERM CELL; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SPERMATOGENESIS; SPERMATOZOON; TESTIS FUNCTION; BIOLOGICAL MODEL; CHEMISTRY; CHROMOSOMAL MAPPING; GENETICS; LIQUID CHROMATOGRAPHY; TANDEM MASS SPECTROMETRY; VALIDATION STUDY;

PROTEIN; PROTEOME;

CHROMATOGRAPHY, LIQUID; CHROMOSOME MAPPING; HUMANS; MALE; MODELS, BIOLOGICAL; PROTEINS; PROTEOME; SPERMATOZOA; TANDEM MASS SPECTROMETRY;

EID: 84941041199     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00170     Document Type: Article

References (45)

1. Chocu, S.; Calvel, P.; Rolland, A. D.; Pineau, C. Spermatogenesis in mammals: proteomic insights Syst. Biol. Reprod. Med. 2012, 58 (4) 179-90 10.3109/19396368.2012.691943
2. Macleod, G.; Varmuza, S. The application of proteomic approaches to the study of mammalian spermatogenesis and sperm function FEBS J. 2013, 280 (22) 5635-51 10.1111/febs.12461
3. Dacheux, J. L.; Belleannee, C.; Guyonnet, B.; Labas, V.; Teixeira-Gomes, A. P.; Ecroyd, H.; Druart, X.; Gatti, J. L.; Dacheux, F. The contribution of proteomics to understanding epididymal maturation of mammalian spermatozoa Syst. Biol. Reprod. Med. 2012, 58 (4) 197-210 10.3109/19396368.2012.663233
4. Nowicka-Bauer, K.; Kurpisz, M. Current knowledge of the human sperm proteome Expert Rev. Proteomics 2013, 10 (6) 591-605 10.1586/14789450.2013.846221
5. Rousseaux, S.; Khochbin, S. Combined proteomic and in silico approaches to decipher post-meiotic male genome reprogramming in mice Syst. Biol. Reprod. Med. 2012, 58 (4) 191-6 10.3109/19396368.2012.663055
6. Aitken, R. J.; Nixon, B.; Lin, M.; Koppers, A. J.; Lee, Y. H.; Baker, M. A. Proteomic changes in mammalian spermatozoa during epididymal maturation Asian J. Androl. 2007, 9 (4) 554-64 10.1111/j.1745-7262.2007.00280.x
7. Baker, M. A.; Nixon, B.; Naumovski, N.; Aitken, R. J. Proteomic insights into the maturation and capacitation of mammalian spermatozoa Syst. Biol. Reprod. Med. 2012, 58 (4) 211-7 10.3109/19396368.2011.639844
8. Rolland, A. D.; Jegou, B.; Pineau, C. Testicular development and spermatogenesis: harvesting the postgenomics bounty Advances in experimental medicine and biology 2009, 636, 16-41 10.1007/978-0-387-09597-4-2
9. Paik, Y. K.; Jeong, S. K.; Omenn, G. S.; Uhlen, M.; Hanash, S.; Cho, S. Y.; Lee, H. J.; Na, K.; Choi, E. Y.; Yan, F.; Zhang, F.; Zhang, Y.; Snyder, M.; Cheng, Y.; Chen, R.; Marko-Varga, G.; Deutsch, E. W.; Kim, H.; Kwon, J. Y.; Aebersold, R.; Bairoch, A.; Taylor, A. D.; Kim, K. Y.; Lee, E. Y.; Hochstrasser, D.; Legrain, P.; Hancock, W. S. The Chromosome-Centric Human Proteome Project for cataloging proteins encoded in the genome Nat. Biotechnol. 2012, 30 (3) 221-3 10.1038/nbt.2152
10. Gaudet, P.; Argoud-Puy, G.; Cusin, I.; Duek, P.; Evalet, O.; Gateau, A.; Gleizes, A.; Pereira, M.; Zahn-Zabal, M.; Zwahlen, C.; Bairoch, A.; Lane, L. neXtProt: organizing protein knowledge in the context of human proteome projects J. Proteome Res. 2013, 12 (1) 293-8 10.1021/pr300830v
11. Kim, M. S.; Pinto, S. M.; Getnet, D.; Nirujogi, R. S.; Manda, S. S.; Chaerkady, R.; Madugundu, A. K.; Kelkar, D. S.; Isserlin, R.; Jain, S.; Thomas, J. K.; Muthusamy, B.; Leal-Rojas, P.; Kumar, P.; Sahasrabuddhe, N. A.; Balakrishnan, L.; Advani, J.; George, B.; Renuse, S.; Selvan, L. D.; Patil, A. H.; Nanjappa, V.; Radhakrishnan, A.; Prasad, S.; Subbannayya, T.; Raju, R.; Kumar, M.; Sreenivasamurthy, S. K.; Marimuthu, A.; Sathe, G. J.; Chavan, S.; Datta, K. K.; Subbannayya, Y.; Sahu, A.; Yelamanchi, S. D.; Jayaram, S.; Rajagopalan, P.; Sharma, J.; Murthy, K. R.; Syed, N.; Goel, R.; Khan, A. A.; Ahmad, S.; Dey, G.; Mudgal, K.; Chatterjee, A.; Huang, T. C.; Zhong, J.; Wu, X.; Shaw, P. G.; Freed, D.; Zahari, M. S.; Mukherjee, K. K.; Shankar, S.; Mahadevan, A.; Lam, H.; Mitchell, C. J.; Shankar, S. K.; Satishchandra, P.; Schroeder, J. T.; Sirdeshmukh, R.; Maitra, A.; Leach, S. D.; Drake, C. G.; Halushka, M. K.; Prasad, T. S.; Hruban, R. H.; Kerr, C. L.; Bader, G. D.; Iacobuzio-Donahue, C. A.; Gowda, H.; Pandey, A. A draft map of the human proteome Nature 2014, 509 (7502) 575-81 10.1038/nature13302
12. Wilhelm, M.; Schlegl, J.; Hahne, H.; Gholami, A. M.; Lieberenz, M.; Savitski, M. M.; Ziegler, E.; Butzmann, L.; Gessulat, S.; Marx, H.; Mathieson, T.; Lemeer, S.; Schnatbaum, K.; Reimer, U.; Wenschuh, H.; Mollenhauer, M.; Slotta-Huspenina, J.; Boese, J. H.; Bantscheff, M.; Gerstmair, A.; Faerber, F.; Kuster, B. Mass-spectrometry-based draft of the human proteome Nature 2014, 509 (7502) 582-7 10.1038/nature13319
13. Lane, L.; Bairoch, A.; Beavis, R. C.; Deutsch, E. W.; Gaudet, P.; Lundberg, E.; Omenn, G. S. Metrics for the Human Proteome Project 2013-2014 and strategies for finding missing proteins J. Proteome Res. 2014, 13 (1) 15-20 10.1021/pr401144x
14. Uhlen, M.; Fagerberg, L.; Hallstrom, B. M.; Lindskog, C.; Oksvold, P.; Mardinoglu, A.; Sivertsson, A.; Kampf, C.; Sjostedt, E.; Asplund, A.; Olsson, I.; Edlund, K.; Lundberg, E.; Navani, S.; Szigyarto, C. A.; Odeberg, J.; Djureinovic, D.; Takanen, J. O.; Hober, S.; Alm, T.; Edqvist, P. H.; Berling, H.; Tegel, H.; Mulder, J.; Rockberg, J.; Nilsson, P.; Schwenk, J. M.; Hamsten, M.; von Feilitzen, K.; Forsberg, M.; Persson, L.; Johansson, F.; Zwahlen, M.; von Heijne, G.; Nielsen, J.; Ponten, F. Proteomics. Tissue-based map of the human proteome Science 2015, 347 (6220) 1260419 10.1126/science.1260419
15. Ramskold, D.; Wang, E. T.; Burge, C. B.; Sandberg, R. An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data PLoS Comput. Biol. 2009, 5 (12) e1000598 10.1371/journal.pcbi.1000598
16. Soumillon, M.; Necsulea, A.; Weier, M.; Brawand, D.; Zhang, X.; Gu, H.; Barthes, P.; Kokkinaki, M.; Nef, S.; Gnirke, A.; Dym, M.; de Massy, B.; Mikkelsen, T. S.; Kaessmann, H. Cellular source and mechanisms of high transcriptome complexity in the mammalian testis Cell Rep. 2013, 3 (6) 2179-90 10.1016/j.celrep.2013.05.031
17. Djureinovic, D.; Fagerberg, L.; Hallstrom, B.; Danielsson, A.; Lindskog, C.; Uhlen, M.; Ponten, F. The human testis-specific proteome defined by transcriptomics and antibody-based profiling Mol. Hum. Reprod. 2014, 20 (6) 476-88 10.1093/molehr/gau018
18. Lavigne, R.; Becker, E.; Liu, Y.; Evrard, B.; Lardenois, A.; Primig, M.; Pineau, C. Direct iterative protein profiling (DIPP)-an innovative method for large-scale protein detection applied to budding yeast mitosis Mol. Cell. Proteomics 2012, 11 (2) M111.012682 10.1074/mcp.M111.012682
19. Vizcaino, J. A.; Deutsch, E. W.; Wang, R.; Csordas, A.; Reisinger, F.; Rios, D.; Dianes, J. A.; Sun, Z.; Farrah, T.; Bandeira, N.; Binz, P. A.; Xenarios, I.; Eisenacher, M.; Mayer, G.; Gatto, L.; Campos, A.; Chalkley, R. J.; Kraus, H. J.; Albar, J. P.; Martinez-Bartolome, S.; Apweiler, R.; Omenn, G. S.; Martens, L.; Jones, A. R.; Hermjakob, H. ProteomeXchange provides globally coordinated proteomics data submission and dissemination Nat. Biotechnol. 2014, 32 (3) 223-6 10.1038/nbt.2839
20. Carapito, C.; Lane, L.; Benama, M.; Opsomer, A.; Mouton-Barbosa, E.; Garrigues, L.; Gonzalez de Peredo, A.; Burel, A.; Bruley, C.; Gateau, A.; Bouyssié, D.; Jaquinod, M.; Cianférani, S.; Burlet-Schiltz, O.; Van Dorsselaer, A.; Garin, J.; Vandenbrouck, Y. Computational and mass spectrometry-based workflow for the discovery and validation of human missing proteins: Application to chromosomes 2 and 14. J. Proteome Res., submitted for publication. DOI: 10.1021/pr5010345.
21. Huang, D. W.; Sherman, B. T.; Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 2008, 4 (1) 44-57 10.1038/nprot.2008.211
22. Uhlen, M.; Oksvold, P.; Fagerberg, L.; Lundberg, E.; Jonasson, K.; Forsberg, M.; Zwahlen, M.; Kampf, C.; Wester, K.; Hober, S.; Wernerus, H.; Bjorling, L.; Ponten, F. Towards a knowledge-based Human Protein Atlas Nat. Biotechnol. 2010, 28 (12) 1248-50 10.1038/nbt1210-1248
23. Com, E.; Rolland, A. D.; Guerrois, M.; Aubry, F.; Jegou, B.; Vallet-Erdtmann, V.; Pineau, C. Identification, molecular cloning, and cellular distribution of the rat homolog of minichromosome maintenance protein 7 (MCM7) in the rat testis Mol. Reprod. Dev. 2006, 73 (7) 866-77 10.1002/mrd.20453
24. Chalmel, F.; Lardenois, A.; Evrard, B.; Mathieu, R.; Feig, C.; Demougin, P.; Gattiker, A.; Schulze, W.; Jegou, B.; Kirchhoff, C.; Primig, M. Global human tissue profiling and protein network analysis reveals distinct levels of transcriptional germline-specificity and identifies target genes for male infertility Hum. Reprod. 2012, 27 (11) 3233-48 10.1093/humrep/des301
25. Chalmel, F.; Rolland, A. D.; Niederhauser-Wiederkehr, C.; Chung, S. S.; Demougin, P.; Gattiker, A.; Moore, J.; Patard, J. J.; Wolgemuth, D. J.; Jegou, B.; Primig, M. The conserved transcriptome in human and rodent male gametogenesis Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (20) 8346-51 10.1073/pnas.0701883104
26. Johnsen, S. G. Testicular biopsy score count - a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males Horm. Res. 1970, 1 (1) 2-25 10.1159/000178170
27. Rolland, A. D.; Lavigne, R.; Dauly, C.; Calvel, P.; Kervarrec, C.; Freour, T.; Evrard, B.; Rioux-Leclercq, N.; Auger, J.; Pineau, C. Identification of genital tract markers in the human seminal plasma using an integrative genomics approach Hum. Reprod. 2013, 28 (1) 199-209 10.1093/humrep/des360
28. Chapelin, C.; Duriez, B.; Magnino, F.; Goossens, M.; Escudier, E.; Amselem, S. Isolation of several human axonemal dynein heavy chain genes: genomic structure of the catalytic site, phylogenetic analysis and chromosomal assignment FEBS Lett. 1997, 412 (2) 325-30 10.1016/S0014-5793(97)00800-4
29. Ben Khelifa, M.; Coutton, C.; Zouari, R.; Karaouzene, T.; Rendu, J.; Bidart, M.; Yassine, S.; Pierre, V.; Delaroche, J.; Hennebicq, S.; Grunwald, D.; Escalier, D.; Pernet-Gallay, K.; Jouk, P. S.; Thierry-Mieg, N.; Toure, A.; Arnoult, C.; Ray, P. F. Mutations in DNAH1, which encodes an inner arm heavy chain dynein, lead to male infertility from multiple morphological abnormalities of the sperm flagella Am. J. Hum. Genet. 2014, 94 (1) 95-104 10.1016/j.ajhg.2013.11.017
30. Jones, R. T.; Abedalthagafi, M. S.; Brahmandam, M.; Greenfield, E. A.; Hoang, M. P.; Louis, D. N.; Hornick, J. L.; Santagata, S. Cross-reactivity of the BRAF VE1 antibody with epitopes in axonemal dyneins leads to staining of cilia Mod. Pathol. 2015, 28, 596 10.1038/modpathol.2014.150
31. Grayson, P.; Civetta, A. Positive Selection and the Evolution of izumo Genes in Mammals Int. J. Evol. Biol. 2012, 2012, 1 10.1155/2012/958164
32. Bianchi, E.; Doe, B.; Goulding, D.; Wright, G. J. Juno is the egg Izumo receptor and is essential for mammalian fertilization Nature 2014, 508 (7497) 483-7 10.1038/nature13203
33. Inoue, N.; Ikawa, M.; Isotani, A.; Okabe, M. The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs Nature 2005, 434 (7030) 234-8 10.1038/nature03362
34. Zhang, L.; Shang, X. J.; Li, H. F.; Shi, Y. Q.; Li, W.; Teves, M. E.; Wang, Z. Q.; Jiang, G. F.; Song, S. Z.; Zhang, Z. B. Characterization of membrane occupation and recognition nexus repeat containing 3, meiosis expressed gene 1 binding partner, in mouse male germ cells Asian J. Androl. 2015, 17 (1) 86-93 10.4103/1008-682X.138186
35. Liu, J.; Xia, J.; Cho, K. H.; Clapham, D. E.; Ren, D. CatSperbeta, a novel transmembrane protein in the CatSper channel complex J. Biol. Chem. 2007, 282 (26) 18945-52 10.1074/jbc.M701083200
36. Singh, A. P.; Rajender, S. CatSper channel, sperm function and male fertility Reprod. BioMed. Online 2015, 30 (1) 28-38 10.1016/j.rbmo.2014.09.014
37. Nikpoor, P.; Mowla, S. J.; Movahedin, M.; Ziaee, S. A.; Tiraihi, T. CatSper gene expression in postnatal development of mouse testis and in subfertile men with deficient sperm motility Human reproduction 2004, 19 (1) 124-8 10.1093/humrep/deh043
38. Avidan, N.; Tamary, H.; Dgany, O.; Cattan, D.; Pariente, A.; Thulliez, M.; Borot, N.; Moati, L.; Barthelme, A.; Shalmon, L.; Krasnov, T.; Ben-Asher, E.; Olender, T.; Khen, M.; Yaniv, I.; Zaizov, R.; Shalev, H.; Delaunay, J.; Fellous, M.; Lancet, D.; Beckmann, J. S. CATSPER2, a human autosomal nonsyndromic male infertility gene Eur. J. Hum. Genet. 2003, 11 (7) 497-502 10.1038/sj.ejhg.5200991
39. Firat-Karalar, E. N.; Sante, J.; Elliott, S.; Stearns, T. Proteomic analysis of mammalian sperm cells identifies new components of the centrosome J. Cell Sci. 2014, 127 (19) 4128-33 10.1242/jcs.157008
40. Pazour, G. J.; Agrin, N.; Leszyk, J.; Witman, G. B. Proteomic analysis of a eukaryotic cilium J. Cell Biol. 2005, 170 (1) 103-13 10.1083/jcb.200504008
41. Imsland, F.; Feng, C.; Boije, H.; Bed'hom, B.; Fillon, V.; Dorshorst, B.; Rubin, C. J.; Liu, R.; Gao, Y.; Gu, X.; Wang, Y.; Gourichon, D.; Zody, M. C.; Zecchin, W.; Vieaud, A.; Tixier-Boichard, M.; Hu, X.; Hallbook, F.; Li, N.; Andersson, L. The Rose-comb mutation in chickens constitutes a structural rearrangement causing both altered comb morphology and defective sperm motility PLoS Genet. 2012, 8 (6) e1002775 10.1371/journal.pgen.1002775
42. Baker, M. A.; Hetherington, L.; Reeves, G. M.; Aitken, R. J. The mouse sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identification Proteomics 2008, 8 (8) 1720-30 10.1002/pmic.200701020
43. Baker, M. A.; Hetherington, L.; Reeves, G.; Muller, J.; Aitken, R. J. The rat sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identification Proteomics 2008, 8 (11) 2312-21 10.1002/pmic.200700876
44. Cao, W.; Gerton, G. L.; Moss, S. B. Proteomic profiling of accessory structures from the mouse sperm flagellum Mol. Cell. Proteomics 2006, 5 (5) 801-10 10.1074/mcp.M500322-MCP200
45. Clermont, Y. The cycle of the seminiferous epithelium in man Am. J. Anat. 1963, 112, 35-51 10.1002/aja.1001120103