Tumor proteomics by multivariate analysis on individual pathway data for characterization of vulvar cancer phenotypes

Molecular and Cellular Proteomics

Volumn 11, Issue 7, 2012, Pages

  Sandberg, AnnSofi ^a   Lindell, Gunnel ^b   Källström, Brita Nordström ^b   Branca, Rui Mamede ^a   Danielsson, Kristina Gemzell ^b   Dahlberg, Mats ^a   Larson, Barbro ^b   Forshed, Jenny ^a   Lehtiö, Janne ^a  

^a SCIENCE FOR LIFE LABORATORY   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; CYSTEINE PROTEINASE; GUANINE NUCLEOTIDE BINDING PROTEIN; LEGUMAIN; MYXOVIRUS RESISTANCE PROTEINS; PROTEASOME; STAT1 PROTEIN; TUMOR MARKER; TUMOR PROTEIN;

ADULT; AGED; ARTICLE; CANCER PATIENT; CLINICAL ARTICLE; DISEASE CLASSIFICATION; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; PAPILLOMAVIRUS INFECTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; RELAPSE; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TANDEM MASS SPECTROMETRY; VULVA CARCINOMA; VULVAR SQUAMOUS CELL CARCINOMA; WART VIRUS; GENE EXPRESSION REGULATION; GENETICS; ISOELECTRIC FOCUSING; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; PAPILLOMA VIRUS; PHYSIOLOGY; RECURRENT DISEASE; STAINING; VULVA TUMOR;

HUMAN PAPILLOMAVIRUS; ORTHOMYXOVIRIDAE;

AGED; AGED, 80 AND OVER; CARCINOMA, SQUAMOUS CELL; CHROMATOGRAPHY, LIQUID; CYSTEINE ENDOPEPTIDASES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GTP-BINDING PROTEINS; HUMANS; ISOELECTRIC FOCUSING; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM PROTEINS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOMICS; RECURRENCE; STAINING AND LABELING; STAT1 TRANSCRIPTION FACTOR; TANDEM MASS SPECTROMETRY; TUMOR MARKERS, BIOLOGICAL; VULVAR NEOPLASMS;

EID: 84863799495     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.016998     Document Type: Article

References (71)

1. McCluggage, W. G. (2009) Recent developments in vulvovaginal pathology. Histopathology 54, 156-173
2. Brandenberger, A. W., Rüdlinger, R., Hänggi, W., Bersinger, N. A., and Dreher, E. (1992) Detection of human papillomavirus in vulvar carcinoma. A study by in situ hybridisation. Arch. Gynecol. Obstet. 252, 31-35
3. Iwasawa, A., Nieminen, P., Lehtinen, M., and Paavonen, J. (1997) Human papillomavirus in squamous cell carcinoma of the vulva by polymerase chain reaction. Obstet. Gyneco.l 89, 81-84 (Pubitemid 27024472)
4. Lerma, E., Matias-Guiu, X., Lee, S. J., and Prat, J. (1999) Squamous cell carcinoma of the vulva: study of ploidy, HPV, p53, and pRb. Int. J. Gynecol. Pathol. 18, 191-197 (Pubitemid 29306973)
5. Pinto, A. P., Schlecht, N. F., Pintos, J., Kaiano, J., Franco, E. L., Crum, C. P., and Villa, L. L. (2004) Prognostic significance of lymph node variables and human papillomavirus DNA in invasive vulvar carcinoma. Gynecol. Oncol. 92, 856-865 (Pubitemid 38251389)
6. Skapa, P., Zamecnik, J., Hamsikova, E., Salakova, M., Smahelova, J., Jandova, K., Robova, H., Rob, L., and Tachezy, R. (2007) Human papillomavirus (HPV) profiles of vulvar lesions: possible implications for the classification of vulvar squamous cell carcinoma precursors and for the efficacy of prophylactic HPV vaccination. Am. J. Surg. Pathol. 31, 1834-1843 (Pubitemid 350175810)
7. Knopp, S., Nesland, J. M., Tropé, C., and Holm, R. (2006) p14ARF, a prognostic predictor in HPV-negative vulvar carcinoma. Am. J. Clin. Pathol. 126, 266-276 (Pubitemid 44162574)
8. Madsen, B. S., Jensen, H. L., van den Brule, A. J., Wohlfahrt, J., and Frisch, M. (2008) Risk factors for invasive squamous cell carcinoma of the vulva and vagina-population-based case-control study in Denmark. Int. J. Cancer 122, 2827-2834 (Pubitemid 351631386)
9. Sutton, B. C., Allen, R. A., Moore, W. E., and Dunn, S. T. (2008) Distribution of human papillomavirus genotypes in invasive squamous carcinoma of the vulva. Mod. Pathol. 21, 345-354 (Pubitemid 351304289)
10. Lindell, G., Nasman, A., Jonsson, C., Ehrsson, R. J., Jacobsson, H., Danielsson, K. G., Dalianis, T., Kallström, B. N., and Larson, B. (2010) Presence of human papillomavirus (HPV) in vulvar squamous cell carcinoma (VSCC) and sentinel node. Gynecol. Oncol. 117, 312-316
11. van de Nieuwenhof, H. P., van Kempen, L. C., de Hullu, J. A., Bekkers, R. L., Bulten, J., Melchers, W. J., and Massuger, L. F. (2009) The etiologic role of HPV in vulvar squamous cell carcinoma fine tuned. Cancer Epidemiol. Biomarkers Prev. 18, 2061-2067
12. van der Avoort, I. A., Shirango, H., Hoevenaars, B. M., Grefte, J. M., de Hullu, J. A., de Wilde, P. C., Bulten, J., Melchers, W. J., and Massuger, L. F. (2006) Vulvar squamous cell carcinoma is a multifactorial disease following two separate and independent pathways. Int. J. Gynecol. Pathol. 25, 22-29 (Pubitemid 44638331)
13. Hoevenaars, B. M., van der Avoort, I. A., de Wilde, P. C., Massuger, L. F., Melchers, W. J., de Hullu, J. A., and Bulten, J. (2008) A panel of p16(INK4A), MIB1 and p53 proteins can distinguish between the 2 pathways leading to vulvar squamous cell carcinoma. Int. J. Cancer 123, 2767-2773
14. Alonso, I., Fusté, V., del Pino, M., Castillo, P., Torné, A., Fusté, P., Rios, J., Pahisa, J., Balasch, J., and Ordi, J. (2011) Does human papillomavirus infection imply a different prognosis in vulvar squamous cell carcinoma? Gynecol Oncol 122, 509-514
15. Flowers, L. C., Wistuba, II, Scurry, J., Muller, C. Y., Ashfaq, R., Miller, D. S., Minna, J. D., and Gazdar, A. F. (1999) Genetic changes during the multistage pathogenesis of human papillomavirus positive and negative vulvar carcinomas. J. Soc. Gynecol. Investig. 6, 213-221 (Pubitemid 29408666)
16. Pinto, A. P., Miron, A., Yassin, Y., Monte, N., Woo, T. Y., Mehra, K. K., Medeiros, F., and Crum, C. P. (2010) Differentiated vulvar intraepithelial neoplasia contains Tp53 mutations and is genetically linked to vulvar squamous cell carcinoma. Mod. Pathol. 23, 404-412
17. Hording, U., Daugaard, S., Junge, J., and Lundvall, F. (1996) Human papillomaviruses and multifocal genital neoplasia. Int. J. Gynecol. Pathol. 15, 230-234 (Pubitemid 26227281)
18. Moody, C. A., and Laimins, L. A. (2010) Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 10, 550-560
19. Walboomers, J. M., Jacobs, M. V., Manos, M. M., Bosch, F. X., Kummer, J. A., Shah, K. V., Snijders, P. J., Peto, J., Meijer, C. J., and Muñoz, N. (1999) Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189, 12-19 (Pubitemid 29406813)
20. zur Hausen, H. (2009) Papillomaviruses in the causation of human cancers - a brief historical account. Virology 384, 260-265
21. Gray, H. J. (2010) Advances in vulvar and vaginal cancer treatment. Gynecol. Oncol. 118, 3-5
22. Monk, B. J., Burger, R. A., Lin, F., Parham, G., Vasilev, S. A., and Wilczynski, S. P. (1995) Prognostic significance of human papillomavirus DNA in vulvar carcinoma. Obstet. Gynecol. 85, 709-715
23. Ansink, A. C., Sie-Go, D. M., van der Velden, J., Sijmons, E. A., de Barros Lopes, A., Monaghan, J. M., Kenter, G. G., Murdoch, J. B., ten Kate, F. J., and Heintz, A. P. (1999) Identification of sentinel lymph nodes in vulvar carcinoma patients with the aid of a patent blue V injection: a multicenter study. Cancer 86, 652-656 (Pubitemid 29379411)
24. Eriksson, H., Lengqvist, J., Hedlund, J., Uhlen, K., Orre, L. M., Bjellqvist, B., Persson, B., Lehtiö, J., and Jakobsson, P. J. (2008) Quantitative membrane proteomics applying narrow range peptide isoelectric focusing for studies of small cell lung cancer resistance mechanisms. Proteomics 8, 3008-3018
25. Lengqvist, J., Uhlén, K., and Lehtiö, J. (2007) iTRAQ compatibility of peptide immobilized pH gradient isoelectric focusing. Proteomics 7, 1746-1752 (Pubitemid 46910994)
26. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (Pubitemid 30007252)
27. Reiter, L., Claassen, M., Schrimpf, S. P., Jovanovic, M., Schmidt, A., Buhmann, J. M., Hengartner, M. O., and Aebersold, R. (2009) Protein identification false discovery rates for very large proteomics data sets generated by tandem mass spectrometry. Mol. Cell. Proteomics 8, 2405-2417
28. Forshed, J., Johansson, H. J., Pernemalm, M., Branca, R. M., Sandberg, A., and Lehtio, J. (2011) Enhanced information output from shotgun proteomics data by protein quantification and peptide quality control (PQPQ). Mol. Cell. Proteomics 10, M111.010264
29. Uhlén, M., Björling, E., Agaton, C., Szigyarto, C. A., Amini, B., Andersen, E., Andersson, A. C., Angelidou, P., Asplund, A., Asplund, C., Berglund, L., Bergström, K., Brumer, H., Cerjan, D., Ekstrom, M., Elobeid, A., Eriksson, C., Fagerberg, L., Falk, R., Fall, J., Forsberg, M., Björklund, M. G., Gumbel, K., Halimi, A., Hallin, I., Hamsten, C., Hansson, M., Hedhammar, M., Hercules, G., Kampf, C., Larsson, K., Lindskog, M., Lodewyckx, W., Lund, J., Lundeberg, J., Magnusson, K., Malm, E., Nilsson, P., Odling, J., Oksvold, P., Olsson, I., Oster, E., Ottosson, J., Paavilainen, L., Persson, A., Rimini, R., Rockberg, J., Runeson, M., Sivertsson, A., Sköllermo, A., Steen, J., Stenvall, M., Sterky, F., Stromberg, S., Sundberg, M., Tegel, H., Tourle, S., Wahlund, E., Walden, A., Wan, J., Wernerus, H., Westberg, J., Wester, K., Wrethagen, U., Xu, L. L., Hober, S., and Ponten, F. (2005) A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol. Cell. Proteomics 4, 1920-1932 (Pubitemid 41830186)
30. Tusher, V. G., Tibshirani, R., and Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A. 98, 5116-5121 (Pubitemid 32397092)
31. Roxas, B. A. P., and Li, Q. B. (2008) Significance analysis of microarray for relative quantitation of LC/MS data in proteomics. Bmc Bioinformatics 9, 187
32. Sturn, A., Quackenbush, J., and Trajanoski, Z. (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18, 207-208 (Pubitemid 34145055)
33. Eriksson, L., Antti, H., Gottfries, J., Holmes, E., Johansson, E., Lindgren, F., Long, I., Lundstedt, T., Trygg, J., and Wold, S. (2004) Using chemometrics for navigating in the large data sets of genomics, proteomics, and metabonomics (gpm). Anal. Bioanal. Chem. 380, 419-429
34. Geladi, P., and Esbensen, K. (1991) Regression on Multivariate Images - Principal Component Regression for Modeling, Prediction and Visual Diagnostic-Tools. J. Chemometr. 5, 97-111
35. Wold, S., Jonsson, J., Sjostrom, M., Sandberg, M., and Rannar, S. (1993) DNA and Peptide Sequences and Chemical Processes Multivariately Modeled by Principal Component Analysis and Partial Least-Squares Projections to Latent Structures. Anal. Chim. Acta 277, 239-253 (Pubitemid 23158002)
36. Trygg, J., and Wold, S. (2002) Orthogonal projections to latent structures (O-PLS). J. Chemometr. 16, 119-128
37. Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., Varela, I., Phillimore, B., Begum, S., McDonald, N. Q., Butler, A., Jones, D., Raine, K., Latimer, C., Santos, C. R., Nohadani, M., Eklund, A. C., Spencer-Dene, B., Clark, G., Pickering, L., Stamp, G., Gore, M., Szallasi, Z., Downward, J., Futreal, P. A., and Swanton, C. (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883-892
38. Karp, N. A., Huber, W., Sadowski, P. G., Charles, P. D., Hester, S. V., and Lilley, K. S. (2010) Addressing accuracy and precision issues in iTRAQ quantitation. Mol. Cell. Proteomics 9, 1885-1897
39. Navon, A., and Ciechanover, A. (2009) The 26 S proteasome: from basic mechanisms to drug targeting. J. Biol. Chem. 284, 33713-33718
40. Crawford, L. J., Walker, B., and Irvine, A. E. (2011) Proteasome inhibitors in cancer therapy. J. Cell. Commun. Signal. 5, 101-110
41. Latonen, L., Moore, H. M., Bai, B., Jaamaa, S., and Laiho, M. (2010) Proteasome inhibitors induce nucleolar aggregation of proteasome target proteins and polyadenylated RNA by altering ubiquitin availability. Oncogene
42. Strome, S. E., Kawakami, K., Alejandro, D., Voss, S., Kasperbauer, J. L., Salomao, D., Chen, L., Maki, R. A., and Puri, R. K. (2002) Interleukin 4 receptor-directed cytotoxin therapy for human head and neck squamous cell carcinoma in animal models. Clin. Cancer Res. 8, 281-286 (Pubitemid 34101489)
43. Sijts, E. J., and Kloetzel, P. M. (2011) The role of the proteasome in the generation of MHC class I ligands and immune responses. Cell Mol. Life Sci. 68, 1491-1502
44. Chang, Y. E., and Laimins, L. A. (2000) Microarray analysis identifies interferon- inducible genes and Stat-1 as major transcriptional targets of human papillomavirus type 31. J. Virol. 74, 4174-4182 (Pubitemid 30214423)
45. Arany, I., Goel, A., and Tyring, S. K. (1995) Interferon response depends on viral transcription in human papillomavirus-containing lesions. Anticancer Res. 15, 2865-2869 (Pubitemid 26095114)
46. Holzinger, D., Jorns, C., Stertz, S., Boisson-Dupuis, S., Thimme, R., Weidmann, M., Casanova, J. L., Haller, O., and Kochs, G. (2007) Induction of MxA gene expression by influenza A virus requires type I or type III interferon signaling. J. Virol. 81, 7776-7785 (Pubitemid 47047864)
47. Dupuis, S., Jouanguy, E., Al-Hajjar, S., Fieschi, C., Al-Mohsen, I. Z., Al-Jumaah, S., Yang, K., Chapgier, A., Eidenschenk, C., Eid, P., Al Ghonaium, A., Tufenkeji, H., Frayha, H., Al-Gazlan, S., Al-Rayes, H., Schreiber, R. D., Gresser, I., and Casanova, J. L. (2003) Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat. Genet. 33, 388-391 (Pubitemid 36278855)
48. Kochs, G., and Haller, O. (1999) Interferon-induced human MxA GTPase blocks nuclear import of Thogoto virus nucleocapsids. Proc. Natl. Acad. Sci. U.S.A. 96, 2082-2086 (Pubitemid 29117871)
49. Reichelt, M., Stertz, S., Krijnse-Locker, J., Haller, O., and Kochs, G. (2004) Missorting of LaCrosse virus nucleocapsid protein by the interferoninduced MxA GTPase involves smooth ER membranes. Traffic 5, 772-784 (Pubitemid 39307261)
50. Jiang, L. J., Zhang, N. N., Ding, F., Li, X. Y., Chen, L., Zhang, H. X., Zhang, W., Chen, S. J., Wang, Z. G., Li, J. M., Chen, Z., and Zhu, J. (2011) RA-inducible gene-I induction augments STAT1 activation to inhibit leukemia cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 108, 1897-1902
51. Tsai, F. M., Shyu, R. Y., and Jiang, S. Y. (2007) RIG1 suppresses Ras activation and induces cellular apoptosis at the Golgi apparatus. Cell Signal. 19, 989-999
52. Kim, H. S., and Lee, M. S. (2007) STAT1 as a key modulator of cell death. Cell Signal. 19, 454-465 (Pubitemid 46107818)
53. Xu, X., Fu, X. Y., Plate, J., and Chong, A. S. (1998) IFN-gamma induces cell growth inhibition by Fas-mediated apoptosis: requirement of STAT1 protein for up-regulation of Fas and FasL expression. Cancer Res. 58, 2832-2837 (Pubitemid 28311915)
54. Watts, C., Matthews, S. P., Mazzeo, D., Manoury, B., and Moss, C. X. (2005) Asparaginyl endopeptidase: case history of a class II MHC compartment protease. Immunol. Rev. 207, 218-228 (Pubitemid 41415020)
55. Manoury, B., Mazzeo, D., Li, D. N., Billson, J., Loak, K., Benaroch, P., and Watts, C. (2003) Asparagine endopeptidase can initiate the removal of the MHC class II invariant chain chaperone. Immunity 18, 489-498 (Pubitemid 36513631)
56. Liu, C., Sun, C., Huang, H., Janda, K., and Edgington, T. (2003) Overexpression of legumain in tumors is significant for invasion/metastasis and a candidate enzymatic target for prodrug therapy. Cancer Res. 63, 2957-2964 (Pubitemid 36667169)
57. Gawenda, J., Traub, F., Lück, H. J., Kreipe, H., and von Wasielewski, R. (2007) Legumain expression as a prognostic factor in breast cancer patients. Breast Cancer Res. Treat. 102, 1-6 (Pubitemid 46294961)
58. Wu, C. C., Hsu, C. W., Chen, C. D., Yu, C. J., Chang, K. P., Tai, D. I., Liu, H. P., Su, W. H., Chang, Y. S., and Yu, J. S. (2010) Candidate serological biomarkers for cancer identified from the secretomes of 23 cancer cell lines and the human protein atlas. Mol. Cell. Proteomics 9, 1100-1117
59. Miller, G., Matthews, S. P., Reinheckel, T., Fleming, S., and Watts, C. (2011) Asparagine endopeptidase is required for normal kidney physiology and homeostasis. FASEB J. 25, 1606-1617
60. Straight, S. W., Herman, B., and McCance, D. J. (1995) The E5 oncoprotein of human papillomavirus type 16 inhibits the acidification of endosomes in human keratinocytes. J. Virol. 69, 3185-3192
61. Schmeink, C. E., Melchers, W. J., Siebers, A. G., Quint, W. G., Massuger, L. F., and Bekkers, R. L. (2011) Human papillomavirus persistence in young unscreened women, a prospective cohort study. PLoS One 6, e27937
62. McCormack, S. J., Brazinski, S. E., Moore, J. L., Jr., Werness, B. A., and Goldstein, D. J. (1997) Activation of the focal adhesion kinase signal transduction pathway in cervical carcinoma cell lines and human genital epithelial cells immortalized with human papillomavirus type 18. Oncogene 15, 265-274 (Pubitemid 27370873)
63. Du, M., Fan, X., Hong, E., and Chen, J. J. (2002) Interaction of oncogenic papillomavirus E6 proteins with fibulin-1. Biochem. Biophys. Res. Commun. 296, 962-969
64. Hantschmann, P., Jeschke, U., and Friese, K. (2005) TGF-alpha, c-erbB-2 expression and neoangiogenesis in vulvar squamous cell carcinoma. Anticancer Res. 25, 1731-1737 (Pubitemid 40896795)
65. Gordinier, M. E., Steinhoff, M. M., Hogan, J. W., Peipert, J. F., Gajewski, W. H., Falkenberry, S. S., and Granai, C. O. (1997) S-Phase fraction, p53, and HER-2/neu status as predictors of nodal metastasis in early vulvar cancer. Gynecol. Oncol. 67, 200-202 (Pubitemid 27500420)
66. Johnson, G. A., Mannel, R., Khalifa, M., Walker, J. L., Wren, M., Min, K. W., and Benbrook, D. M. (1997) Epidermal growth factor receptor in vulvar malignancies and its relationship to metastasis and patient survival. Gynecol. Oncol. 65, 425-429 (Pubitemid 27255982)
67. Oonk, M. H., de Bock, G. H., van der Veen, D. J., Ten Hoor, K. A., de Hullu, J. A., Hollema, H., and van der Zee, A. G. (2007) EGFR expression is associated with groin node metastases in vulvar cancer, but does not improve their prediction. Gynecol. Oncol. 104, 109-113 (Pubitemid 46054130)
68. Hermeking, H., Lengauer, C., Polyak, K., He, T. C., Zhang, L., Thiagalingam, S., Kinzler, K. W., and Vogelstein, B. (1997) 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1, 3-11 (Pubitemid 127376388)
69. Wang, Z., Nesland, J. M., Suo, Z., Trope, C. G., and Holm, R. (2011) The prognostic value of 14-3-3 isoforms in vulvar squamous cell carcinoma cases: 14-3-3beta and epsilon are independent prognostic factors for these tumors. PLoS One 6, e24843
70. Ashrafi, G. H., Haghshenas, M., Marchetti, B., and Campo, M. S. (2006) E5 protein of human papillomavirus 16 downregulates HLA class I and interacts with the heavy chain via its first hydrophobic domain. Int. J. Cancer 119, 2105-2112 (Pubitemid 44423668)
71. Tomas, M. I., Kucic, N., Mahmutefendić, H., Blagojević, G., and Lucin, P. (2010) Murine cytomegalovirus perturbs endosomal trafficking of major histocompatibility complex class I molecules in the early phase of infection. J. Virol. 84, 11101-11112