Identification of HPV integration and gene mutation in HeLa cell line by integrated analysis of RNA-Seq and MS/MS data

Journal of Proteome Research

Volumn 14, Issue 4, 2015, Pages 1678-1686

  Sun, Han ^a,b   Chen, Chen ^c   Lian, Baofeng ^a   Zhang, Menghuan ^a   Wang, Xiaojing ^d   Zhang, Bing ^d   Li, Yixue ^a,b   Yang, Pengyuan ^c   Xie, Lu ^a  

^a SHANGHAI CENTER FOR BIOINFORMATION TECHNOLOGY   (China)

^b Chinese Academy of Sciences   (China)

^c FUDAN UNIVERSITY   (China)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

HeLa; HPV; MRM; MS MS; proteogenomics; RNA Seq

Indexed keywords

RNA;

ARTICLE; GENE MUTATION; GENETIC VARIABILITY; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 18; INDEL MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; RNA SEQUENCE; TANDEM MASS SPECTROMETRY; VIRUS DNA CELL DNA INTERACTION; VIRUS GENOME; VIRUS INFECTION; WART VIRUS; GENETIC VARIATION; GENETICS; MOLECULAR GENETICS; MUTATION; PAPILLOMAVIRIDAE; PHYSIOLOGY; PROCEDURES; SEQUENCE ANALYSIS;

HUMAN PAPILLOMAVIRUS;

GENETIC VARIATION; HELA CELLS; HUMANS; MOLECULAR SEQUENCE ANNOTATION; MUTATION; PAPILLOMAVIRIDAE; PROTEOMICS; SEQUENCE ANALYSIS, RNA; TANDEM MASS SPECTROMETRY; VIRUS INTEGRATION;

EID: 84926429701     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500944c     Document Type: Article

References (46)

1. Corden, S. A.; Sant-Cassia, L. J.; Easton, A. J.; Morris, A. G. The integration of HPV-18 DNA in cervical carcinoma Mol. Pathol. 1999, 52 (5) 275-282
2. Peter, M.; Stransky, N.; Couturier, J.; Hupe, P.; Barillot, E.; de Cremoux, P.; Cottu, P.; Radvanyi, F.; Sastre-Garau, X. Frequent genomic structural alterations at HPV insertion sites in cervical carcinoma J. Pathol. 2010, 221 (3) 320-330
3. Goodwin, E. C.; DiMaio, D. Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways Proc. Natl. Acad. Sci. U. S. A. 2000, 97 (23) 12513-1258
4. Adey, A.; Burton, J. N.; Kitzman, J. O.; Hiatt, J. B.; Lewis, A. P.; Martin, B. K.; Qiu, R.; Lee, C.; Shendure, J. The haplotype-resolved genome and epigenome of the aneuploid HeLa cancer cell line Nature 2013, 500 (7461) 207-211
5. Schmitz, M.; Driesch, C.; Jansen, L.; Runnebaum, I. B.; Durst, M. Non-random integration of the HPV genome in cervical cancer PLoS One 2012, 7 (6) e39632
6. Papachristou, E. K.; Roumeliotis, T. I.; Chrysagi, A.; Trigoni, C.; Charvalos, E.; Townsend, P. A.; Pavlakis, K.; Garbis, S. D. The shotgun proteomic study of the human ThinPrep cervical smear using iTRAQ mass-tagging and 2D LC-FT-Orbitrap-MS: the detection of the human papillomavirus at the protein level J. Proteome Res. 2013, 12 (5) 2078-2089
7. Landry, J. J.; Pyl, P. T.; Rausch, T.; Zichner, T.; Tekkedil, M. M.; Stutz, A. M.; Jauch, A.; Aiyar, R. S.; Pau, G.; Delhomme, N.; Gagneur, J.; Korbel, J. O.; Huber, W.; Steinmetz, L. M. The genomic and transcriptomic landscape of a HeLa cell line G3: Genes, Genomes, Genet. 2013, 3 (8) 1213-1224
8. Thiede, B.; Koehler, C. J.; Strozynski, M.; Treumann, A.; Stein, R.; Zimny-Arndt, U.; Schmid, M.; Jungblut, P. R. High Resolution Quantitative Proteomics of HeLa Cells Protein Species Using Stable Isotope Labeling with Amino Acids in Cell Culture(SILAC), Two-Dimensional Gel Electrophoresis(2DE) and Nano-Liquid Chromatograpohy Coupled to an LTQ-OrbitrapMass Spectrometer Mol. Cell. Proteomics 2013, 12 (2) 529-538
9. Nagaraj, N.; Wisniewski, J. R.; Geiger, T.; Cox, J.; Kircher, M.; Kelso, J.; Paabo, S.; Mann, M. Deep proteome and transcriptome mapping of a human cancer cell line Mol. Syst. Biol. 2011, 7, 548
10. Castellana, N.; Bafna, V. Proteogenomics to discover the full coding content of genomes: a computational perspective J. Proteomics 2010, 73 (11) 2124-2135
11. Xing, X. B.; Li, Q. R.; Sun, H.; Fu, X.; Zhan, F.; Huang, X.; Li, J.; Chen, C. L.; Shyr, Y.; Zeng, R.; Li, Y. X.; Xie, L. The discovery of novel protein-coding features in mouse genome based on mass spectrometry data Genomics 2011, 98 (5) 343-351
12. Zhang, B.; Wang, J.; Wang, X.; Zhu, J.; Liu, Q.; Shi, Z.; Chambers, M. C.; Zimmerman, L. J.; Shaddox, K. F.; Kim, S.; Davies, S. R.; Wang, S.; Wang, P.; Kinsinger, C. R.; Rivers, R. C.; Rodriguez, H.; Townsend, R. R.; Ellis, M. J.; Carr, S. A.; Tabb, D. L.; Coffey, R. J.; Slebos, R. J.; Liebler, D. C.; NCI CPTAc Proteogenomic characterization of human colon and rectal cancer Nature 2014, 513, 382-387
13. Li, J.; Su, Z.; Ma, Z. Q.; Slebos, R. J.; Halvey, P.; Tabb, D. L.; Liebler, D. C.; Pao, W.; Zhang, B. A bioinformatics workflow for variant peptide detection in shotgun proteomics Mol. Cell. Proteomics 2011, 10 (5) M110 006536
14. Wang, X. J.; Slebos, R. J. C.; Wang, D.; Halvey, P. J.; Tabb, D. L.; Liebler, D. C.; Zhang, B. Protein Identification Using Customized Protein Sequence Databases Derived from RNA-Seq Data J. Proteome Res. 2012, 11 (2) 1009-1017
15. Sheynkman, G. M.; Shortreed, M. R.; Frey, B. L.; Smith, L. M. Discovery and mass spectrometric analysis of novel splice-junction peptides using RNA-Seq Mol. Cell. Proteomics 2013, 12 (8) 2341-2353
16. Banfai, B.; Jia, H.; Khatun, J.; Wood, E.; Risk, B.; Gundling, W. E., Jr.; Kundaje, A.; Gunawardena, H. P.; Yu, Y.; Xie, L.; Krajewski, K.; Strahl, B. D.; Chen, X.; Bickel, P.; Giddings, M. C.; Brown, J. B.; Lipovich, L. Long noncoding RNAs are rarely translated in two human cell lines Genome Res. 2012, 22 (9) 1646-1657
17. Hernandez, C.; Waridel, P.; Quadroni, M. Database construction and peptide identification strategies for proteogenomic studies on sequenced genomes Curr. Top. Med. Chem. 2014, 14 (3) 425-434
18. Woo, S.; Cha, S. W.; Merrihew, G.; He, Y.; Castellana, N.; Guest, C.; MacCoss, M.; Bafna, V. Proteogenomic database construction driven from large scale RNA-seq data J. Proteome Res. 2014, 13 (1) 21-28
19. Jagtap, P.; Goslinga, J.; Kooren, J. A.; McGowan, T.; Wroblewski, M. S.; Seymour, S. L.; Griffin, T. J. A two-step database search method improves sensitivity in peptide sequence matches for metaproteomics and proteogenomics studies Proteomics 2013, 13 (8) 1352-1357
20. Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 2009, 25 (14) 1754-1760
21. Rudin, C. M.; Durinck, S.; Stawiski, E. W.; Poirier, J. T.; Modrusan, Z.; Shames, D. S.; Bergbower, E. A.; Guan, Y.; Shin, J.; Guillory, J.; Rivers, C. S.; Foo, C. K.; Bhatt, D.; Stinson, J.; Gnad, F.; Haverty, P. M.; Gentleman, R.; Chaudhuri, S.; Janakiraman, V.; Jaiswal, B. S.; Parikh, C.; Yuan, W.; Zhang, Z.; Koeppen, H.; Wu, T. D.; Stern, H. M.; Yauch, R. L.; Huffman, K. E.; Paskulin, D. D.; Illei, P. B.; Varella-Garcia, M.; Gazdar, A. F.; de Sauvage, F. J.; Bourgon, R.; Minna, J. D.; Brock, M. V.; Seshagiri, S. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer Nat. Genet. 2012, 44 (10) 1111-1116
22. Cancer Genome Atlas, N. Comprehensive molecular characterization of human colon and rectal cancer Nature 2012, 487 (7407) 330-337
23. Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R.; Proc, G. P. D. The Sequence Alignment/Map format and SAMtools Bioinformatics 2009, 25 (16) 2078-2079
24. Koboldt, D. C.; Zhang, Q.; Larson, D. E.; Shen, D.; McLellan, M. D.; Lin, L.; Miller, C. A.; Mardis, E. R.; Ding, L.; Wilson, R. K. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing Genome Res. 2012, 22 (3) 568-576
25. Wang, K.; Li, M. Y.; Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data Nucleic Acids Res. 2010, 38 (16) e164
26. Ye, K.; Schulz, M. H.; Long, Q.; Apweiler, R.; Ning, Z. M. Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads Bioinformatics 2009, 25 (21) 2865-2871
27. Kim, D.; Salzberg, S. L. TopHat-Fusion: an algorithm for discovery of novel fusion transcripts Genome Biol. 2011, 12 (8) R72
28. Bao, Y. M.; Federhen, S.; Leipe, D.; Pham, V.; Resenchuk, S.; Rozanov, M.; Tatusov, R.; Tatusova, T. National Center for Biotechnology Information Viral Genomes Project J. Virol. 2004, 78 (14) 7291-7298
29. Chen, C.; Liu, X.; Zheng, W.; Zhang, L.; Yao, J.; Yang, P. Screening of Missing Proteins in the Human Liver Proteome by Improved MRM-Approach-Based Targeted Proteomics J. Proteome Res. 2014, 13 (4) 1969-1978
30. Prensner, J. R.; Iyer, M. K.; Balbin, O. A.; Dhanasekaran, S. M.; Cao, Q.; Brenner, J. C.; Laxman, B.; Asangani, I. A.; Grasso, C. S.; Kominsky, H. D.; Cao, X.; Jing, X.; Wang, X.; Siddiqui, J.; Wei, J. T.; Robinson, D.; Iyer, H. K.; Palanisamy, N.; Maher, C. A.; Chinnaiyan, A. M. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression Nat. Biotechnol. 2011, 29 (8) 742-749
31. Ge, X.; Chen, Y.; Liao, X.; Liu, D.; Li, F.; Ruan, H.; Jia, W. Overexpression of long noncoding RNA PCAT-1 is a novel biomarker of poor prognosis in patients with colorectal cancer Med. Oncol. 2013, 30 (2) 588
32. Prensner, J. R.; Chen, W.; Iyer, M. K.; Cao, Q.; Ma, T.; Han, S.; Sahu, A.; Malik, R.; Wilder-Romans, K.; Navone, N.; Logothetis, C. J.; Araujo, J. C.; Pisters, L. L.; Tewari, A. K.; Canman, C. E.; Knudsen, K. E.; Kitabayashi, N.; Rubin, M. A.; Demichelis, F.; Lawrence, T. S.; Chinnaiyan, A. M.; Feng, F. Y. PCAT-1, a long noncoding RNA, regulates BRCA2 and controls homologous recombination in cancer Cancer Res. 2014, 74 (6) 1651-1660
33. Nissan, A.; Stojadinovic, A.; Mitrani-Rosenbaum, S.; Halle, D.; Grinbaum, R.; Roistacher, M.; Bochem, A.; Dayanc, B. E.; Ritter, G.; Gomceli, I.; Bostanci, E. B.; Akoglu, M.; Chen, Y. T.; Old, L. J.; Gure, A. O. Colon cancer associated transcript-1: a novel RNA expressed in malignant and pre-malignant human tissues Int. J. Cancer 2012, 130 (7) 1598-1606
34. Alaiyan, B.; Ilyayev, N.; Stojadinovic, A.; Izadjoo, M.; Roistacher, M.; Pavlov, V.; Tzivin, V.; Halle, D.; Pan, H.; Trink, B.; Gure, A. O.; Nissan, A. Differential expression of colon cancer associated transcript1 (CCAT1) along the colonic adenoma-carcinoma sequence BMC Cancer 2013, 13, 196
35. Yang, F.; Xue, X.; Bi, J.; Zheng, L.; Zhi, K.; Gu, Y.; Fang, G. Long noncoding RNA CCAT1, which could be activated by c-Myc, promotes the progression of gastric carcinoma J. Cancer Res. Clin. Oncol. 2013, 139 (3) 437-445
36. Strausberg, R. L.; Feingold, E. A.; Grouse, L. H.; Derge, J. G.; Klausner, R. D.; Collins, F. S.; Wagner, L.; Shenmen, C. M.; Schuler, G. D.; Altschul, S. F.; Zeeberg, B.; Buetow, K. H.; Schaefer, C. F.; Bhat, N. K.; Hopkins, R. F.; Jordan, H.; Moore, T.; Max, S. I.; Wang, J.; Hsieh, F.; Diatchenko, L.; Marusina, K.; Farmer, A. A.; Rubin, G. M.; Hong, L.; Stapleton, M.; Soares, M. B.; Bonaldo, M. F.; Casavant, T. L.; Scheetz, T. E.; Brownstein, M. J.; Usdin, T. B.; Toshiyuki, S.; Carninci, P.; Prange, C.; Raha, S. S.; Loquellano, N. A.; Peters, G. J.; Abramson, R. D.; Mullahy, S. J.; Bosak, S. A.; McEwan, P. J.; McKernan, K. J.; Malek, J. A.; Gunaratne, P. H.; Richards, S.; Worley, K. C.; Hale, S.; Garcia, A. M.; Gay, L. J.; Hulyk, S. W.; Villalon, D. K.; Muzny, D. M.; Sodergren, E. J.; Lu, X. H.; Gibbs, R. A.; Fahey, J.; Helton, E.; Ketteman, M.; Madan, A.; Rodrigues, S.; Sanchez, A.; Whiting, M.; Madan, A.; Young, A. C.; Shevchenko, Y.; Bouffard, G. G.; Blakesley, R. W.; Touchman, J. W.; Green, E. D.; Dickson, M. C.; Rodriguez, A. C.; Grimwood, J.; Schmutz, J.; Myers, R. M.; Butterfield, Y. S. N.; Kryzywinski, M. I.; Skalska, U.; Smailus, D. E.; Schnerch, A.; Schein, J. E.; Jones, S. J. M.; Marra, M. A.; Pro, M. G. C. M. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences Proc. Natl. Acad. Sci. U. S. A. 2002, 99 (26) 16899-16903
37. Ziegert, C.; Wentzensen, N.; Vinokurova, S.; Kisseljov, F.; Einenkel, J.; Hoeckel, M.; von Knebel Doeberitz, M. A comprehensive analysis of HPV integration loci in anogenital lesions combining transcript and genome-based amplification techniques Oncogene 2003, 22 (25) 3977-3984
38. Caceres, M.; National Institutes of Health Intramural Sequencing Center Comparative Sequencing, P.; Sullivan, R. T.; Thomas, J. W. A recurrent inversion on the eutherian X chromosome Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (47) 18571-18576
39. Sherry, S. T.; Ward, M. H.; Kholodov, M.; Baker, J.; Phan, L.; Smigielski, E. M.; Sirotkin, K. dbSNP: the NCBI database of genetic variation Nucleic Acids Res. 2001, 29 (1) 308-311
40. Jensen, L. J.; Kuhn, M.; Stark, M.; Chaffron, S.; Creevey, C.; Muller, J.; Doerks, T.; Julien, P.; Roth, A.; Simonovic, M.; Bork, P.; von Mering, C. STRING 8-A global view on proteins and their functional interactions in 630 organisms Nucleic Acids Res. 2009, 37, D412-D416
41. Eden, E.; Navon, R.; Steinfeld, I.; Lipson, D.; Yakhini, Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists BMC Bioinf. 2009, 10
42. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for mass spectrometry-based proteomics Methods Mol. Biol. 2010, 604, 55-71
43. 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
44. Sun, H.; Xing, X.; Li, J.; Zhou, F.; Chen, Y.; He, Y.; Li, W.; Wei, G.; Chang, X.; Jia, J.; Li, Y.; Xie, L. Identification of gene fusions from human lung cancer mass spectrometry data BMC Genomics 2013, 14 (Suppl 8) S5
45. Sun, H.; Chen, C.; Shi, M.; Wang, D.; Liu, M.; Li, D.; Yang, P.; Li, Y.; Xie, L. Integration of mass spectrometry and RNA-Seq data to confirm human ab initio predicted genes and lncRNAs Proteomics 2014, 14 (23-24) 2760-2768
46. Sung, W. K.; Zheng, H. C.; Li, S. Y.; Chen, R. H.; Liu, X.; Li, Y. R.; Lee, N. P.; Lee, W. H.; Ariyaratne, P. N.; Tennakoon, C.; Mulawadi, F. H.; Wong, K. F.; Liu, A. M.; Poon, R. T.; Fan, S. T.; Chan, K. L.; Gong, Z. L.; Hu, Y. J.; Lin, Z.; Wang, G.; Zhang, Q. H.; Barber, T. D.; Chou, W. C.; Aggarwal, A.; Hao, K.; Zhou, W.; Zhang, C. S.; Hardwick, J.; Buser, C.; Xu, J. C.; Kan, Z. Y.; Dai, H. Y.; Mao, M.; Reinhard, C.; Wang, J.; Luk, J. M. Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma Nat. Genet. 2012, 44 (7) 765-769