Identification of rare alternative splicing events in MS/MS data reveals a significant fraction of alternative translation initiation sites

PeerJ

Volumn 2014, Issue 1, 2014, Pages

  Kroll, José E ^a,b   de Souza, Sandro J ^b   de Souza, Gustavo A ^a,c  

^a Institute of Bioinformatics and Biotechnology   (Brazil)

^b Brain Institute   (Brazil)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Alternative splicing events; Mass spectrometry; Peptide identification; Proteomics; Translation initiation sites

Indexed keywords

MESSENGER RNA; PROTEIN VARIANT; TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ARTICLE; HUMAN; INFORMATION PROCESSING; MASS SPECTROMETRY; OPEN READING FRAME; PEPTIDE ANALYSIS; PROTEIN ANALYSIS; PROTEIN DATABASE; PROTEIN STRUCTURE; PROTEOMICS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; TRANSLATION INITIATION;

EID: 84911396120     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.673     Document Type: Article

References (34)

1. Au KF, Sebastiano V, Afshar PT, Durruthy JD, Lee L, Williams BA, Van Bakel H, Schadt EE, Reijo-Pera RA, Underwood JG, Wong WH. 2013. Characterization of the human ESC transcriptome by hybrid sequencing. Proceedings of the National Academy of Sciences of the United States of America 110:E4821-E4830 DOI 10.1073/pnas.1320101110.
2. Beck M, Schmidt A, MalmstroemJ, Claassen M, Ori A, Szymborska A, Herzog F, Rinner O, Ellenberg J, Aebersold R. 2011. The quantitative proteome of a human cell line. Molecular Systems Biology 7:1-6 Article 549.
3. Blakeley P, Siepen JA, Lawless C, Hubbard SJ. 2010. Investigating protein isoforms via proteomics: a feasibility study. Proteomics 10:1127-1140 DOI 10.1002/pmic.200900445.
4. Brosch M, Saunders GI, Frankish A, Collins MO, Yu L, Wright J, Verstraten R, Adams DJ, Harrow J, Choudhary JS, Hubbard T. 2011. Shotgun proteomics aids discovery of novel protein-coding genes, alternative splicing, and "resurrected" pseudogenes in the mouse genome. Genome Research 21:756-767 DOI 10.1101/gr.114272.110.
5. Cork DMW, Lennard TWJ, Tyson-Capper AJ. 2012. Progesterone receptor (PR) variants exist in breast cancer cells characterised as PR negative. Tumour Biology 33:2329-2340 DOI 10.1007/s13277-012-0495-z.
6. Cox J, Mann M. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology 26:1367-1372 DOI 10.1038/nbt.1511.
7. Desiere F, Deutsch EW, King NL, Nesvizhskii AI, Mallick P, Eng J, Chen S, Eddes J, Loevenich SN, Aebersold R. 2006. The PeptideAtlas project. Nucleic Acids Research 34:D655-D658 DOI 10.1093/nar/gkj040.
8. Geiger T, Wehner A, Schaab C, Cox J, Mann M. 2012. Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Molecular & Cellular Proteomics 11:M111 014050 DOI 10.1074/mcp. M111.014050.
9. Griss J, Martin M, O'Donovan C, Apweiler R, Hermjakob H, Vizcaino JA. 2011. Consequences of the discontinuation of the International Protein Index (IPI) database and its substitution by the UniProtKB "complete proteome" sets. Proteomics 11:4434-4438 DOI 10.1002/pmic.201100363.
10. Kim MS, Pinto SM, Getnet D, Nirujogi RS, Manda SS, Chaerkady R, Madugundu AK, Kelkar DS, Isserlin R, Jain S, Thomas JK, Muthusamy B, Leal-Rojas P, Kumar P, Sahasrabuddhe NA, Balakrishnan L, Advani J, George B, Renuse S, Selvan LD, Patil AH, Nanjappa V, Radhakrishnan A, Prasad S, Subbannayya T, Raju R, Kumar M, Sreenivasamurthy SK, Marimuthu A, Sathe GJ, Chavan S, Datta KK, Subbannayya Y, Sahu A, Yelamanchi SD, Jayaram S, Rajagopalan P, Sharma J, Murthy KR, Syed N, Goel R, Khan AA, Ahmad S, Dey G, Mudgal K, Chatterjee A, Huang TC, Zhong J, Wu X, Shaw PG, Freed D, Zahari MS, Mukherjee KK, Shankar S, Mahadevan A, Lam H, Mitchell CJ, Shankar SK, Satishchandra P, Schroeder JT, Sirdeshmukh R, Maitra A, Leach SD, Drake CG, Halushka MK, Prasad TS, Hruban RH, Kerr CL, Bader GD, Iacobuzio-Donahue CA, Gowda H, Pandey A. 2014. A draft map of the human proteome. Nature 509:575-581 DOI 10.1038/nature13302.
11. Kroll JE, Galante PA, Ohara DT, Navarro FC, Ohno-Machado L, de Souza SJ. 2012. SPLOOCE: a new portal for the analysis of human splicing variants. RNA Biology 9:1339-1343 DOI 10.4161/rna.22182.
12. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, Stange-Thomann N, Stojanovic N, Subramanian A, Wyman D, Rogers J, Sulston J, Ainscough R, Beck S, Bentley D, Burton J, Clee C, Carter N, Coulson A, Deadman R, Deloukas P, Dunham A, Dunham I, Durbin R, French L, Grafham D, Gregory S, Hubbard T, Humphray S, Hunt A, Jones M, Lloyd C, McMurray A, Matthews L, Mercer S, Milne S, Mullikin JC, Mungall A, Plumb R, Ross M, Shownkeen R, Sims S, Waterston RH, Wilson RK, Hillier LW, McPherson JD, Marra MA, Mardis ER, Fulton LA, Chinwalla AT, Pepin KH, Gish WR, Chissoe SL, Wendl MC, Delehaunty KD, Miner TL, Delehaunty A, Kramer JB, Cook LL, Fulton RS, Johnson DL, Minx PJ, Clifton SW, Hawkins T, Branscomb E, Predki P, Richardson P, Wenning S, Slezak T, Doggett N, Cheng JF, Olsen A, Lucas S, Elkin C, Uberbacher E, Frazier M, Gibbs RA, Muzny DM, Scherer SE, Bouck JB, Sodergren EJ, Worley KC, Rives CM, Gorrell JH, Metzker ML, Naylor SL, Kucherlapati RS, Nelson DL, Weinstock GM, Sakaki Y, Fujiyama A, Hattori M, Yada T, Toyoda A, Itoh T, Kawagoe C, Watanabe H, Totoki Y, Taylor T, Weissenbach J, Heilig R, Saurin W, Artiguenave F, Brottier P, Bruls T, Pelletier E, Robert C, Wincker P, Smith DR, Doucette-Stamm L, Rubenfield M, Weinstock K, Lee HM, Dubois J, Rosenthal A, Platzer M, Nyakatura G, Taudien S, Rump A, Yang H, Yu J, Wang J, Huang G, Gu J, Hood L, Rowen L, Madan A, Qin S, Davis RW, Federspiel NA, Abola AP, Proctor MJ, Myers RM, Schmutz J, Dickson M, Grimwood J, Cox DR, Olson MV, Kaul R, Raymond C, Shimizu N, Kawasaki K, Minoshima S, Evans GA, Athanasiou M, Schultz R, Roe BA, Chen F, Pan H, Ramser J, Lehrach H, Reinhardt R, McCombie WR, de la Bastide M, Dedhia N, Blocker H, Hornischer K, Nordsiek G, Agarwala R, Aravind L, Bailey JA, Bateman A, Batzoglou S, Birney E, Bork P, Brown DG, Burge CB, Cerutti L, Chen HC, Church D, Clamp M, Copley RR, Doerks T, Eddy SR, Eichler EE, Furey TS, Galagan J, Gilbert JG, Harmon C, Hayashizaki Y, Haussler D, Hermjakob H, Hokamp K, Jang W, Johnson LS, Jones TA, Kasif S, Kaspryzk A, Kennedy S, Kent WJ, Kitts P, Koonin EV, Korf I, Kulp D, Lancet D, Lowe TM, McLysaght A, Mikkelsen T, Moran JV, Mulder N, Pollara VJ, Ponting CP, Schuler G, Schultz J, Slater G, Smit AF, Stupka E, Szustakowski J, Thierry-Mieg D, Thierry-Mieg J, Wagner L, Wallis J, Wheeler R, Williams A, Wolf YI, Wolfe KH, Yang SP, Yeh RF, Collins F, Guyer MS, Peterson J, Felsenfeld A, Wetterstrand KA, Patrinos A, Morgan MJ, de Jong P, Catanese JJ, Osoegawa K, Shizuya H, Choi S, Chen YJ, International Human Genome Sequencing C. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921 DOI 10.1038/35057062.
13. Lee S, Liu B, Lee S, Huang SX, Shen B, Qian SB. 2012. Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution. Proceedings of the National Academy of Sciences of the United States of America 109:E2424-2432 DOI 10.1073/pnas.1207846109.
14. Ma B, Zhang K, Hendrie C, Liang C, Li M, Doherty-Kirby A, Lajoie G. 2003. PEAKS: powerful software for peptide de novo sequencing by tandem mass spectrometry. Rapid Communications in Mass Spectrometry 17:2337-2342 DOI 10.1002/rcm.1196.
15. Magrane M, UniProt Consortium. 2011. UniProt Knowledgebase: a hub of integrated protein data. Database 2011:bar009 DOI 10.1093/database/bar009.
16. Nagaraj N, Wisniewski JR, Geiger T, Cox J, Kircher M, Kelso J, Paabo S, Mann M. 2011. Deep proteome and transcriptome mapping of a human cancer cell line. Molecular Systems Biology 7:1-8 Article 548.
17. Peng Z, Cheng Y, Tan BC-M, Kang L, Tian Z, Zhu Y, Zhang W, Liang Y, Hu X, Tan X, Guo J, Dong Z, Liang Y, Bao L, Wang J. 2012. Comprehensive analysis of RNA-Seq data reveals extensive RNA editing in a human transcriptome. Nature Biotechnology 30:253-260 DOI 10.1038/nbt.2122.
18. Perez-Riverol Y, Alpi E., Wang R, Hermjakob H, Vizcaino JA. 2014. Making proteomics data accessible and reusable: current state of proteomics databases and repositories. Proteomics In press DOI 10.1002/pmic.201400302.
19. Perez-Riverol Y, Sanchez A, Ramos Y, Schmidt A, Muller M, Betancourt L, Gonzalez LJ, Vera R, Padron G, Besada V. 2011. In silico analysis of accurate proteomics, complemented by selective isolation of peptides. Journal of Proteomics 74:2071-2082 DOI 10.1016/j.jprot.2011.05.034.
20. Pruitt KD, Brown GR, Hiatt SM, Thibaud-Nissen F, Astashyn A, Ermolaeva O, Farrell CM, Hart J, Landrum MJ, McGarvey KM, Murphy MR, O'Leary NA, Pujar S, Rajput B, Rangwala SH, Riddick LD, Shkeda A, Sun H, Tamez P, Tully RE, Wallin C, Webb D, Weber J, Wu W, DiCuccio M, Kitts P, Maglott DR, Murphy TD, Ostell JM. 2014. RefSeq: an update on mammalian reference sequences. Nucleic Acids Research 42:D756-D763 DOI 10.1093/nar/gkt1114.
21. Severing EI, Van Dijk AD, Van Ham RC. 2011. Assessing the contribution of alternative splicing to proteome diversity in Arabidopsis thaliana using proteomics data. BMC Plant Biology 11:82 DOI 10.1186/1471-2229-11-82.
22. Sheynkman GM, Shortreed MR, Frey BL, Smith LM. 2013. Discovery and mass spectrometric analysis of novel splice-junction peptides using RNA-Seq. Molecular & Cellular Proteomics 12:2341-2353 DOI 10.1074/mcp. O113.028142.
23. The 1000 Genomes Project Consortium. 2012. An integrated map of genetic variation from 1,092 human genomes. Nature 491:56-65 DOI 10.1038/nature11632.
24. Tress ML, Bodenmiller B, Aebersold R, Valencia A. 2008. Proteomics studies confirm the presence of alternative protein isoforms on a large scale. Genome Biology 9:R162 DOI 10.1186/gb-2008-9-11-r162.
25. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, Gocayne JD, Amanatides P, Ballew RM, Huson DH, Wortman JR, Zhang Q, Kodira CD, Zheng XH, Chen L, Skupski M, Subramanian G, Thomas PD, Zhang J, GaborMiklos GL, Nelson C, Broder S, Clark AG, Nadeau J, McKusick VA, Zinder N, Levine AJ, Roberts RJ, Simon M, Slayman C, Hunkapiller M, Bolanos R, Delcher A, Dew I, Fasulo D, Flanigan M, Florea L, Halpern A, Hannenhalli S, Kravitz S, Levy S, Mobarry C, Reinert K, Remington K, Abu-Threideh J, Beasley E, Biddick K, Bonazzi V, Brandon R, Cargill M, Chandramouliswaran I, Charlab R, Chaturvedi K, Deng Z, Di Francesco V, Dunn P, Eilbeck K, Evangelista C, Gabrielian AE, Gan W, Ge W, Gong F, Gu Z, Guan P, Heiman TJ, Higgins ME, Ji RR, Ke Z, Ketchum KA, Lai Z, Lei Y, Li Z, Li J, Liang Y, Lin X, Lu F, Merkulov GV, Milshina N, Moore HM, Naik AK, Narayan VA, Neelam B, Nusskern D, Rusch DB, Salzberg S, Shao W, Shue B, Sun J, Wang Z, Wang A, Wang X, Wang J, Wei M, Wides R, Xiao C, Yan C, Yao A, Ye J, Zhan M, Zhang W, Zhang H, Zhao Q, Zheng L, Zhong F, Zhong W, Zhu S, Zhao S, Gilbert D, Baumhueter S, Spier G, Carter C, Cravchik A, Woodage T, Ali F, An H, Awe A, Baldwin D, Baden H, Barnstead M, Barrow I, Beeson K, Busam D, Carver A, Center A, Cheng ML, Curry L, Danaher S, Davenport L, Desilets R, Dietz S, Dodson K, Doup L, Ferriera S, Garg N, Gluecksmann A, Hart B, Haynes J, Haynes C, Heiner C, Hladun S, Hostin D, Houck J, Howland T, Ibegwam C, Johnson J, Kalush F, Kline L, Koduru S, Love A, Mann F, May D, McCawley S, McIntosh T, McMullen I, Moy M, Moy L, Murphy B, Nelson K, Pfannkoch C, Pratts E, Puri V, Qureshi H, Reardon M, Rodriguez R, Rogers YH, Romblad D, Ruhfel B, Scott R, Sitter C, Smallwood M, Stewart E, Strong R, Suh E, Thomas R, Tint NN, Tse S, Vech C, Wang G, Wetter J, Williams S, Williams M, Windsor S, Winn-Deen E, Wolfe K, Zaveri J, Zaveri K, Abril JF, Guigo R, Campbell MJ, Sjolander KV, Karlak B, Kejariwal A, Mi H, Lazareva B, Hatton T, Narechania A, Diemer K, Muruganujan A, Guo N, Sato S, Bafna V, Istrail S, Lippert R, Schwartz R, Walenz B, Yooseph S, Allen D, Basu A, Baxendale J, Blick L, Caminha M, Carnes-Stine J, Caulk P, Chiang YH, Coyne M, Dahlke C, Mays A, Dombroski M, Donnelly M, Ely D, Esparham S, Fosler C, Gire H, Glanowski S, Glasser K, Glodek A, Gorokhov M, Graham K, Gropman B, Harris M, Heil J, Henderson S, Hoover J, Jennings D, Jordan C, Jordan J, Kasha J, Kagan L, Kraft C, Levitsky A, Lewis M, Liu X, Lopez J, Ma D, Majoros W, McDaniel J, Murphy S, Newman M, Nguyen T, Nguyen N, Nodell M, Pan S, Peck J, Peterson M, Rowe W, Sanders R, Scott J, Simpson M, Smith T, Sprague A, Stockwell T, Turner R, Venter E, Wang M, Wen M, Wu D, Wu M, Xia A, Zandieh A, Zhu X. 2001. The sequence of the human genome. Science 291:1304-1351 DOI 10.1126/science.1058040.
26. Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, Foster JM, Griss J, Alpi E, Birim M, Contell J, O'Kelly G, Schoenegger A, Ovelleiro D, Perez-Riverol Y, Reisinger F, Rios D, Wang R, Hermjakob H. 2013. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Research 41:D1063-D1069 DOI 10.1093/nar/gks1262.
27. Vizcaino JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Rios D, Dianes JA, Sun Z, Farrah T, Bandeira N, Binz PA, Xenarios I, Eisenacher M, Mayer G, Gatto L, Campos A, Chalkley RJ, Kraus HJ, Albar JP, Martinez-Bartolome S, Apweiler R, Omenn GS, Martens L, Jones AR, Hermjakob H. 2014. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nature Biotechnology 32:223-226 DOI 10.1038/nbt.2839.
28. Wan J, Qian SB. 2014. TISdb: a database for alternative translation initiation in mammalian cells. Nucleic Acids Research 42:D845-D850 DOI 10.1093/nar/gkt1085.
29. Wang X, Slebos RJ, Wang D, Halvey PJ, Tabb DL, Liebler DC, Zhang B. 2012. Protein identification using customized protein sequence databases derived from RNA-Seq data. Journal of Proteome Research 11:1009-1017 DOI 10.1021/pr200766z.
30. Wilhelm M, Schlegl J, Hahne H, Moghaddas Gholami A, Lieberenz M, Savitski MM, Ziegler E, Butzmann L, Gessulat S, Marx H, Mathieson T, Lemeer S, Schnatbaum K, Reimer U, Wenschuh H, Mollenhauer M, Slotta-Huspenina J, Boese JH, BantscheffM, Gerstmair A, Faerber F, Kuster B. 2014. Mass-spectrometry-based draft of the human proteome. Nature 509:582-587 DOI 10.1038/nature13319.
31. Wilson LO, Spriggs A, Taylor JM, Fahrer AM. 2014. A novel splicing outcome reveals more than 2000 new mammalian protein isoforms. Bioinformatics 30:151-156 DOI 10.1093/bioinformatics/btt668.
32. Woo S, Cha SW, Merrihew G, He Y, Castellana N, Guest C, MacCoss M, Bafna V. 2014. Proteogenomic database construction driven from large scale RNA-seq data. Journal of Proteome Research 13:21-28 DOI 10.1021/pr400294c.
33. Xue J, Schmidt SV, Sander J, Draffehn A, Krebs W, Quester I, De Nardo D, Gohel TD, Emde M, Schmidleithner L, Ganesan H, Nino-Castro A, Mallmann MR, Labzin L, Theis H, Kraut M, Beyer M, Latz E, Freeman TC, Ulas T, Schultze JL. 2014. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 40:274-288 DOI 10.1016/j.immuni.2014.01.006.
34. Zhang C, Hastings ML, Krainer AR, Zhang MQ. 2007. Dual-specificity splice sites function alternatively as 5' and 3' splice sites. Proceedings of the National Academy of Sciences of the United States of America 104:15028-15033 DOI 10.1073/pnas.0703773104.