Tissue-based proteogenomics reveals that human testis endows plentiful missing proteins

Journal of Proteome Research

Volumn 14, Issue 9, 2015, Pages 3583-3594

  Zhang, Yao ^a,d,e   Li, Qidan ^b,c,e   Wu, Feilin ^a,f   Zhou, Ruo ^c   Qi, Yingzi ^a   Su, Na ^a   Chen, Lingsheng ^a,h   Xu, Shaohang ^c   Jiang, Tao ^c   Zhang, Chengpu ^a   Cheng, Gang ^c   Chen, Xinguo ⁱ   Kong, Degang ^j   Wang, Yujia ^c   Zhang, Tao ^a   Zi, Jin ^c   Wei, Wei ^a   Gao, Yuan ^a   Zhen, Bei ^a   Xiong, Zhi ^f   Wu, Songfeng ^a   Yang, Pengyuan ^k   Wang, Quanhui ^b,c,e   Wen, Bo ^c   He, Fuchu ^a   Xu, Ping ^a,g   Liu, Siqi ^b,c,e   more..

^a BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^b Chinese Academy of Sciences   (China)

^c BGI SHENZHEN   (China)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^e UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^f SOUTHWEST FORESTRY UNIVERSITY   (China)

^g WUHAN UNIVERSITY   (China)

^h GUANGXI UNIVERSITY   (China)

ⁱ GENERAL HOSPITAL OF CHINESE PEOPLE'S ARMED POLICE FORCES   (China)

^j CAPITAL MEDICAL UNIVERSITY   (China)

^k FUDAN UNIVERSITY   (China)

more..

Author keywords

Chromosome Centric Human Proteome Project; individual; missing proteins; proteome; testis; transcriptome

Indexed keywords

GLYCINE; PROTEIN; TRANSCRIPTOME;

ARTICLE; BIOINFORMATICS; GENE EXPRESSION; GENOMICS; HUMAN; HUMAN TISSUE; MALE; MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOGENOMICS; PROTEOMICS; REPRODUCTION; SPERMATOGENESIS; TESTIS; TRANSCRIPTOMICS; ISOLATION AND PURIFICATION; LIQUID CHROMATOGRAPHY; METABOLISM; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY;

CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENOMICS; HUMANS; MALE; PROTEINS; PROTEOMICS; SEQUENCE ANALYSIS, RNA; TANDEM MASS SPECTROMETRY; TESTIS; TRANSCRIPTOME;

EID: 84941039788     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00435     Document Type: Article

References (44)

1. Omenn, G. S.; Lane, L.; Lundberg, E. K.; Beavis, R. C.; Nesvizhskii, A. I.; Deutsch, E. W. Metrics for the Human Proteome Project 2015: Progress on the Human Proteome and Guidelines for High-Confidence Protein Identification J. Proteome Res. 2015, 10.1021/acs.jproteome.5b00499
2. Shiromizu, T.; Adachi, J.; Watanabe, S.; Murakami, T.; Kuga, T.; Muraoka, S.; Tomonaga, T. Identification of missing proteins in the neXtProt database and unregistered phosphopeptides in the PhosphoSitePlus database as part of the Chromosome-centric Human Proteome Project J. Proteome Res. 2013, 12 (6) 2414-21 10.1021/pr300825v
3. Zhang, C.; Li, N.; Zhai, L.; Xu, S.; Liu, X.; Cui, Y.; Ma, J.; Han, M.; Jiang, J.; Yang, C.; Fan, F.; Li, L.; Qin, P.; Yu, Q.; Chang, C.; Su, N.; Zheng, J.; Zhang, T.; Wen, B.; Zhou, R.; Lin, L.; Lin, Z.; Zhou, B.; Zhang, Y.; Yan, G.; Liu, Y.; Yang, P.; Guo, K.; Gu, W.; Chen, Y.; Zhang, G.; He, Q. Y.; Wu, S.; Wang, T.; Shen, H.; Wang, Q.; Zhu, Y.; He, F.; Xu, P. Systematic analysis of missing proteins provides clues to help define all of the protein-coding genes on human chromosome 1 J. Proteome Res. 2014, 13 (1) 114-25 10.1021/pr400900j
4. Kwon, K. H.; Kim, J. Y.; Kim, S. Y.; Min, H. K.; Lee, H. J.; Ji, I. J.; Kang, T.; Park, G. W.; An, H. J.; Lee, B.; Ravid, R.; Ferrer, I.; Chung, C. K.; Paik, Y. K.; Hancock, W. S.; Park, Y. M.; Yoo, J. S. Chromosome 11-centric human proteome analysis of human brain hippocampus tissue J. Proteome Res. 2013, 12 (1) 97-105 10.1021/pr3008368
5. Martins-de-Souza, D.; Carvalho, P. C.; Schmitt, A.; Junqueira, M.; Nogueira, F. C.; Turck, C. W.; Domont, G. B. Deciphering the human brain proteome: characterization of the anterior temporal lobe and corpus callosum as part of the Chromosome 15-centric Human Proteome Project J. Proteome Res. 2014, 13 (1) 147-57 10.1021/pr4009157
6. Lee, H. J.; Jeong, S. K.; Na, K.; Lee, M. J.; Lee, S. H.; Lim, J. S.; Cha, H. J.; Cho, J. Y.; Kwon, J. Y.; Kim, H.; Song, S. Y.; Yoo, J. S.; Park, Y. M.; Kim, H.; Hancock, W. S.; Paik, Y. K. Comprehensive genome-wide proteomic analysis of human placental tissue for the Chromosome-Centric Human Proteome Project J. Proteome Res. 2013, 12 (6) 2458-66 10.1021/pr301040g
7. 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
8. 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
9. 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
10. 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
11. Fagerberg, L.; Hallström, B. M.; Oksvold, P.; Kampf, C.; Djureinovic, D.; Odeberg, J.; Habuka, M.; Tahmasebpoor, S.; Danielsson, A.; Edlund, K. Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics Mol. Cell. Proteomics 2014, 13 (2) 397-406 10.1074/mcp.M113.035600
12. 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
13. 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
14. 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
15. Simpson, A. J.; Caballero, O. L.; Jungbluth, A.; Chen, Y. T.; Old, L. J. Cancer/testis antigens, gametogenesis and cancer Nat. Rev. Cancer 2005, 5 (8) 615-25 10.1038/nrc1669
16. Wang, J.; Xia, Y.; Wang, G.; Zhou, T.; Guo, Y.; Zhang, C.; An, X.; Sun, Y.; Guo, X.; Zhou, Z.; Sha, J. In-depth proteomic analysis of whole testis tissue from the adult rhesus macaque Proteomics 2014, 14 (11) 1393-402 10.1002/pmic.201300149
17. Almeida, L. G.; Sakabe, N. J.; deOliveira, A. R.; Silva, M. C.; Mundstein, A. S.; Cohen, T.; Chen, Y. T.; Chua, R.; Gurung, S.; Gnjatic, S.; Jungbluth, A. A.; Caballero, O. L.; Bairoch, A.; Kiesler, E.; White, S. L.; Simpson, A. J.; Old, L. J.; Camargo, A. A.; Vasconcelos, A. T. CTdatabase: a knowledge-base of high-throughput and curated data on cancer-testis antigens Nucleic Acids Res. 2009, 37 (Database issue) D816-9 10.1093/nar/gkn673
18. Xu, P.; Duong, D. M.; Peng, J. Systematical optimization of reverse-phase chromatography for shotgun proteomics J. Proteome Res. 2009, 8 (8) 3944-3950 10.1021/pr900251d
19. Mann, K.; Mann, M. In-depth analysis of the chicken egg white proteome using an LTQ Orbitrap Velos Proteome Sci. 2011, 9 (1) 7 10.1186/1477-5956-9-7
20. Lander, E. S.; Linton, L. M.; Birren, B.; Nusbaum, C.; Zody, M. C.; Baldwin, J.; Devon, K.; Dewar, K.; Doyle, M.; FitzHugh, W. Initial sequencing and analysis of the human genome Nature 2001, 409 (6822) 860-921 10.1038/35057062
21. The Uniprot Consortium UniProt: a hub for protein information Nucleic Acids Res. 2015, 43 (Database issue) D204-12
22. Cunningham, F.; Amode, M. R.; Barrell, D.; Beal, K.; Billis, K.; Brent, S.; Carvalho-Silva, D.; Clapham, P.; Coates, G.; Fitzgerald, S.; Gil, L.; Giron, C. G.; Gordon, L.; Hourlier, T.; Hunt, S. E.; Janacek, S. H.; Johnson, N.; Juettemann, T.; Kahari, A. K.; Keenan, S.; Martin, F. J.; Maurel, T.; McLaren, W.; Murphy, D. N.; Nag, R.; Overduin, B.; Parker, A.; Patricio, M.; Perry, E.; Pignatelli, M.; Riat, H. S.; Sheppard, D.; Taylor, K.; Thormann, A.; Vullo, A.; Wilder, S. P.; Zadissa, A.; Aken, B. L.; Birney, E.; Harrow, J.; Kinsella, R.; Muffato, M.; Ruffier, M.; Searle, S. M.; Spudich, G.; Trevanion, S. J.; Yates, A.; Zerbino, D. R.; Flicek, P. Ensembl 2015 Nucleic Acids Res. 2015, 43 (Database issue) D662-9 10.1093/nar/gku1010
23. Wen, B.; Du, C.; Li, G.; Ghali, F.; Jones, A. R.; Käll, L.; Xu, S.; Zhou, R.; Ren, Z.; Feng, Q. IPeak: An open source tool to combine results from multiple MS/MS search engines Proteomics 2015, n/a 10.1002/pmic.201400208
24. Wen, B.; Li, G.; Wright, J. C.; Du, C.; Feng, Q.; Xu, X.; Choudhary, J. S.; Wang, J. The OMSSAPercolator: an automated tool to validate OMSSA results Proteomics 2014, 14 (9) 1011-4 10.1002/pmic.201300393
25. Savitski, M. M.; Wilhelm, M.; Hahne, H.; Kuster, B.; Bantscheff, M. A scalable approach for protein false discovery rate estimation in large proteomic data sets Mol. Cell. Proteomics 2015, mcp.M114.046995 10.1074/mcp.M114.046995
26. Deutsch, E. W.; Sun, Z.; Campbell, D.; Kusebauch, U.; Chu, C. S.; Mendoza, L.; Shteynberg, D.; Omenn, G. S.; Moritz, R. L. State of the Human Proteome in 2014/2015 As Viewed through PeptideAtlas: Enhancing Accuracy and Coverage through the AtlasProphet J. Proteome Res. 2015, 150724142438005 10.1021/acs.jproteome.5b00500
27. Zhang, C.; Li, N.; Zhai, L.; Xu, S.; Liu, X.; Cui, Y.; Ma, J.; Han, M.; Jiang, J.; Yang, C. Systematic analysis of missing proteins provides clues to help define all of the protein-coding genes on human chromosome 1 J. Proteome Res. 2013, 13 (1) 114-125 10.1021/pr400900j
28. Köhrer, K.; Domdey, H. [27] Preparation of high molecular weight RNA Methods Enzymol. 1991, 194, 398-405 10.1016/0076-6879(91)94030-G
29. Mortazavi, A.; Williams, B. A.; McCue, K.; Schaeffer, L.; Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq Nat. Methods 2008, 5 (7) 621-8 10.1038/nmeth.1226
30. Fu, Y.; Yang, Q.; Sun, R.; Li, D.; Zeng, R.; Ling, C. X.; Gao, W. Exploiting the kernel trick to correlate fragment ions for peptide identification via tandem mass spectrometry Bioinformatics 2004, 20 (12) 1948-1954 10.1093/bioinformatics/bth186
31. Li, D.; Fu, Y.; Sun, R.; Ling, C. X.; Wei, Y.; Zhou, H.; Zeng, R.; Yang, Q.; He, S.; Gao, W. pFind: a novel database-searching software system for automated peptide and protein identification via tandem mass spectrometry Bioinformatics 2005, 21 (13) 3049-3050 10.1093/bioinformatics/bti439
32. Wang, L. h.; Li, D. Q.; Fu, Y.; Wang, H. P.; Zhang, J. F.; Yuan, Z. F.; Sun, R. X.; Zeng, R.; He, S. M.; Gao, W. pFind 2.0: a software package for peptide and protein identification via tandem mass spectrometry Rapid Commun. Mass Spectrom. 2007, 21 (18) 2985-2991 10.1002/rcm.3173
33. 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
34. Krämer, A.; Green, J.; Pollard, J.; Tugendreich, S. Causal Analysis Approaches in Ingenuity Pathway Analysis (IPA) Bioinformatics 2014, 30, 523-530 10.1093/bioinformatics/btt703
35. Schagger, H. Tricine-SDS-PAGE Nat. Protoc. 2006, 1 (1) 16-22 10.1038/nprot.2006.4
36. Chen, L.; Zhai, L.; Li, Y.; Li, N.; Zhang, C.; Ping, L.; Chang, L.; Wu, J.; Li, X.; Shi, D.; Xu, P. Development of gel-filter method for high enrichment of low-molecular weight proteins from serum PLoS One 2015, 10 (2) e0115862 10.1371/journal.pone.0115862
37. Stiles, G. Adenosine receptors J. Biol. Chem. 1992, 267 (10) 6451-6454
38. Jenner, T. L.; Rose'meyer, R. B. Adenosine A(3) receptor mediated coronary vasodilation in the rat heart: changes that occur with maturation Mech. Ageing Dev. 2006, 127 (3) 264-73 10.1016/j.mad.2005.10.005
39. Peculis, R.; Latkovskis, G.; Tarasova, L.; Pirags, V.; Erglis, A.; Klovins, J. A nonsynonymous variant I248L of the adenosine A3 receptor is associated with coronary heart disease in a Latvian population DNA Cell Biol. 2011, 30 (11) 907-11 10.1089/dna.2011.1230
40. Huang, C.; Jia, Y.; Yang, S.; Chen, B.; Sun, H.; Shen, F.; Wang, Y. Characterization of ZNF23, a KRAB-containing protein that is downregulated in human cancers and inhibits cell cycle progression Exp. Cell Res. 2007, 313 (2) 254-63 10.1016/j.yexcr.2006.10.009
41. Huang, C.; Yang, S.; Ge, R.; Sun, H.; Shen, F.; Wang, Y. ZNF23 induces apoptosis in human ovarian cancer cells Cancer Lett. 2008, 266 (2) 135-43 10.1016/j.canlet.2008.02.059
42. Shi, Y.; Zheng, L.; Luo, G.; Wei, J.; Zhang, J.; Yu, Y.; Feng, Y.; Li, M.; Xu, N. Expression of zinc finger 23 gene in human hepatocellular carcinoma Anticancer Res. 2011, 31 (10) 3595-3599
43. Khakoo, S. I.; Thio, C. L.; Martin, M. P.; Brooks, C. R.; Gao, X.; Astemborski, J.; Cheng, J.; Goedert, J. J.; Vlahov, D.; Hilgartner, M. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection Science 2004, 305 (5685) 872-874 10.1126/science.1097670
44. Yen, J.-H.; Moore, B. E.; Nakajima, T.; Scholl, D.; Schaid, D. J.; Weyand, C. M.; Goronzy, J. J. Major histocompatibility complex class I-recognizing receptors are disease risk genes in rheumatoid arthritis J. Exp. Med. 2001, 193 (10) 1159-1168 10.1084/jem.193.10.1159