Quantitative proteomics profiling of primary lung adenocarcinoma tumors reveals functional perturbations in tumor metabolism

Journal of Proteome Research

Volumn 12, Issue 9, 2013, Pages 3934-3943

  Pernemalm, Maria ^a   De Petris, Luigi ^b   Branca, Rui M ^a   Forshed, Jenny ^a   Kanter, Lena ^b   Soria, Jean Charles ^c,g   Girard, Philippe ^d   Validire, Pierre ^d   Pawitan, Yudi ^a   Van Den Oord, Joost ^e   Lazar, Vladimir ^c   Paìšhlman, Sven ^f   Lewensohn, Rolf ^b   Lehtiö, Janne ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c INSTITUT GUSTAVE ROUSSY   (France)

^d INSTITUT MUTUALISTE MONTSOURIS   (France)

^e DEPARTMENT OF IMAGING AND PATHOLOGY   (Belgium)

^f LUND UNIVERSITY   (Sweden)

^g UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

adenocarcinoma; CTSD; ENO1; glycolysis; HIF1; hypoxia; NSCLC; peptide isoelectric focusing; prognosis; relapse; VDAC1; Warburg

Indexed keywords

ALPHA ENOLASE; CATHEPSIN D; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; VOLTAGE DEPENDENT ANION CHANNEL 1;

ADULT; AGED; ARTICLE; BIOINFORMATICS; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SURGERY; CELL ENERGY; FEMALE; FUNCTIONAL PROTEOMICS; GLYCOLYSIS; HUMAN; LUNG ADENOCARCINOMA; MALE; MASS SPECTROMETRY; METABOLISM; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; UPREGULATION;

ADENOCARCINOMA; AGED; CATHEPSIN D; CLUSTER ANALYSIS; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KERATIN-5; LUNG NEOPLASMS; MALE; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; PHOSPHOPYRUVATE HYDRATASE; PRINCIPAL COMPONENT ANALYSIS; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; PROTEOME; PROTEOMICS; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 84883766689     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr4002096     Document Type: Article

References (45)

1. Goldstraw, P.; Crowley, J.; Chansky, K.; Giroux, D. J.; Groome, P. A.; Rami-Porta, R.; Postmus, P. E.; Rusch, V.; Sobin, L.; Committee, I. A. f. t. S. o. L. C. I. S.; Institutions, P. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours J. Thorac. Oncol. 2007, 2 (8) 706-714
2. Jemal, A.; Siegel, R.; Ward, E.; Hao, Y.; Xu, J.; Thun, M. J. Cancer statistics, 2009 Ca-Cancer J. Clin. 2009, 59 (4) 225-249
3. Djebali, S.; Davis, C. A.; Merkel, A.; Dobin, A.; Lassmann, T.; Mortazavi, A.; Tanzer, A.; Lagarde, J.; Lin, W.; Schlesinger, F.; Xue, C.; Marinov, G. K.; Khatun, J.; Williams, B. A.; Zaleski, C.; Rozowsky, J.; Röder, M.; Kokocinski, F.; Abdelhamid, R. F.; Alioto, T.; Antoshechkin, I.; Baer, M. T.; Bar, N. S.; Batut, P.; Bell, K.; Bell, I.; Chakrabortty, S.; Chen, X.; Chrast, J.; Curado, J.; Derrien, T.; Drenkow, J.; Dumais, E.; Dumais, J.; Duttagupta, R.; Falconnet, E.; Fastuca, M.; Fejes-Toth, K.; Ferreira, P.; Foissac, S.; Fullwood, M. J.; Gao, H.; Gonzalez, D.; Gordon, A.; Gunawardena, H.; Howald, C.; Jha, S.; Johnson, R.; Kapranov, P.; King, B.; Kingswood, C.; Luo, O. J.; Park, E.; Persaud, K.; Preall, J. B.; Ribeca, P.; Risk, B.; Robyr, D.; Sammeth, M.; Schaffer, L.; See, L. H.; Shahab, A.; Skancke, J.; Suzuki, A. M.; Takahashi, H.; Tilgner, H.; Trout, D.; Walters, N.; Wang, H.; Wrobel, J.; Yu, Y.; Ruan, X.; Hayashizaki, Y.; Harrow, J.; Gerstein, M.; Hubbard, T.; Reymond, A.; Antonarakis, S. E.; Hannon, G.; Giddings, M. C.; Ruan, Y.; Wold, B.; Carninci, P.; Guigó, R.; Gingeras, T. R. Landscape of transcription in human cells Nature 2012, 489 (7414) 101-108
4. Govindan, R.; Ding, L.; Griffith, M.; Subramanian, J.; Dees, N. D.; Kanchi, K. L.; Maher, C. A.; Fulton, R.; Fulton, L.; Wallis, J.; Chen, K.; Walker, J.; McDonald, S.; Bose, R.; Ornitz, D.; Xiong, D.; You, M.; Dooling, D. J.; Watson, M.; Mardis, E. R.; Wilson, R. K. Genomic landscape of non-small cell lung cancer in smokers and never-smokers Cell 2012, 150 (6) 1121-1134
5. Seo, J. S.; Ju, Y. S.; Lee, W. C.; Shin, J. Y.; Lee, J. K.; Bleazard, T.; Lee, J.; Jung, Y. J.; Kim, J. O.; Yu, S. B.; Kim, J.; Lee, E. R.; Kang, C. H.; Park, I. K.; Rhee, H.; Lee, S. H.; Kim, J. I.; Kang, J. H.; Kim, Y. T. The transcriptional landscape and mutational profile of lung adenocarcinoma Genome Res. 2012, 22, 2109-2119
6. Imielinski, M.; Berger, A. H.; Hlammerman, P. S.; Hernandez, B.; Pugh, T. J.; Hodis, E.; Cho, J.; Suh, J.; Capelletti, M.; Sivachenko, A.; Sougnez, C.; Auclair, D.; Lawrence, M. S.; Stojanov, P.; Cibulskis, K.; Choi, K.; de Waal, L.; Sharifnia, T.; Brooks, A.; Greulich, H.; Banerji, S.; Zander, T.; Seidel, D.; Leenders, F.; Ansén, S.; Ludwig, C.; Engel-Riedel, W.; Stoelben, E.; Wolf, J.; Goparju, C.; Thompson, K.; Winckler, W.; Kwiatkowski, D.; Johnson, B. E.; Jänne, P. A.; Miller, V. A.; Pao, W.; Travis, W. D.; Pass, H. I.; Gabriel, S. B.; Lander, E. S.; Thomas, R. K.; Garraway, L. A.; Getz, G.; Meyerson, M. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing Cell 2012, 150 (6) 1107-1120
7. Peifer, M.; Fernández-Cuesta, L.; Sos, M. L.; George, J.; Seidel, D.; Kasper, L. H.; Plenker, D.; Leenders, F.; Sun, R.; Zander, T.; Menon, R.; Koker, M.; Dahmen, I.; Müller, C.; Di Cerbo, V.; Schildhaus, H. U.; Altmüller, J.; Baessmann, I.; Becker, C.; de Wilde, B.; Vandesompele, J.; Böhm, D.; Ansén, S.; Gabler, F.; Wilkening, I.; Heynck, S.; Heuckmann, J. M.; Lu, X.; Carter, S. L.; Cibulskis, K.; Banerji, S.; Getz, G.; Park, K. S.; Rauh, D.; Grütter, C.; Fischer, M.; Pasqualucci, L.; Wright, G.; Wainer, Z.; Russell, P.; Petersen, I.; Chen, Y.; Stoelben, E.; Ludwig, C.; Schnabel, P.; Hoffmann, H.; Muley, T.; Brockmann, M.; Engel-Riedel, W.; Muscarella, L. A.; Fazio, V. M.; Groen, H.; Timens, W.; Sietsma, H.; Thunnissen, E.; Smit, E.; Heideman, D. A.; Snijders, P. J.; Cappuzzo, F.; Ligorio, C.; Damiani, S.; Field, J.; Solberg, S.; Brustugun, O. T.; Lund-Iversen, M.; Sänger, J.; Clement, J. H.; Soltermann, A.; Moch, H.; Weder, W.; Solomon, B.; Soria, J. C.; Validire, P.; Besse, B.; Brambilla, E.; Brambilla, C.; Lantuejoul, S.; Lorimier, P.; Schneider, P. M.; Hallek, M.; Pao, W.; Meyerson, M.; Sage, J.; Shendure, J.; Schneider, R.; Büttner, R.; Wolf, J.; Nürnberg, P.; Perner, S.; Heukamp, L. C.; Burindle, P. K.; Haas, S.; Thomas, R. K. Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer Nat. Genet. 2012, 44 (10) 1104-1110
8. Kikuchi, T.; Hassanein, M.; Amann, J. M.; Liu, Q.; Slebos, R. J.; Rahman, S. M.; Kaufman, J. M.; Zhang, X.; Hoeksema, M. D.; Harris, B. K.; Li, M.; Shyr, Y.; Gonzalez, A. L.; Zimmerman, L. J.; Liebler, D. C.; Massion, P. P.; Carbone, D. P. In-depth Proteomic Analysis of Nonsmall Cell Lung Cancer to Discover Molecular Targets and Candidate Biomarkers Mol. Cell. Proteomics 2012, 11 (10) 916-932
9. Eriksson, H.; Lengqvist, J.; Hedlund, J.; Uhlen, K.; Orre, L. M.; Bjellqvist, B.; Persson, B.; Lehtio, J.; Jakobsson, P. J. Quantitative membrane proteomics applying narrow range peptide isoelectric focusing for studies of small cell lung cancer resistance mechanisms Proteomics 2008, 8 (15) 3008-3018
10. Käll, L.; Canterbury, J. D.; Weston, J.; Noble, W. S.; MacCoss, M. J. Semi-supervised learning for peptide identification from shotgun proteomics datasets Nat. Methods 2007, 4 (11) 923-925
11. Spivak, M.; Weston, J.; Bottou, L.; Käll, L.; Noble, W. S. Improvements to the percolator algorithm for Peptide identification from shotgun proteomics data sets J. Proteome Res. 2009, 8 (7) 3737-3745
12. Reiter, L.; Claassen, M.; Schrimpf, S. P.; Jovanovic, M.; Schmidt, A.; Buhmann, J. M.; Hengartner, M. O.; Aebersold, R. Protein identification false discovery rates for very large proteomics data sets generated by tandem mass spectrometry Mol. Cell. Proteomics 2009, 8 (11) 2405-2417
13. Eriksson, L.; Antti, H.; Gottfries, J.; Holmes, E.; Johansson, E.; Lindgren, F.; Long, I.; Lundstedt, T.; Trygg, J.; Wold, S. Using chemometrics for navigating in the large data sets of genomics, proteomics, and metabonomics (gpm) Anal. Bioanal. Chem. 2004, 380 (3) 419-429
14. Chong Performance of some variable selection methods when multicollinearity is present Chemom. Intell. Lab. Syst. 2005, 78 (1-2) 103-112
15. Huang, d. w.; Sherman, B. T.; Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 2009, 4 (1) 44-57
16. Herrero, J.; Valencia, A.; Dopazo, J. A hierarchical unsupervised growing neural network for clustering gene expression patterns Bioinformatics 2001, 17 (2) 126-136
17. Cuezva, J. M.; Krajewska, M.; de Heredia, M. L.; Krajewski, S.; Santamaria, G.; Kim, H.; Zapata, J. M.; Marusawa, H.; Chamorro, M.; Reed, J. C. The bioenergetic signature of cancer: A marker of tumor progression Cancer Res. 2002, 62 (22) 6674-6681
18. Hernlund, E.; Hjerpe, E.; Avall-Lundqvist, E.; Shoshan, M. Ovarian carcinoma cells with low levels of beta-F1-ATPase are sensitive to combined platinum and 2-deoxy- d -glucose treatment Mol. Cancer Ther. 2009, 8 (7) 1916-1923
19. De Petris, L.; Orre, L. M.; Kanter, L.; Pernemalm, M.; Koyi, H.; Lewensohn, R.; Lehtiö, J. Tumor expression of S100A6 correlates with survival of patients with stage I non-small-cell lung cancer Lung Cancer 2009, 63 (3) 410-417
20. Munksgaard Persson, M.; Johansson, M. E.; Monsef, N.; Planck, M.; Beckman, S.; Seckl, M. J.; Rönnstrand, L.; PaÌŠhlman, S.; Pettersson, H. M. HIF-2α expression is suppressed in SCLC cells, which survive in moderate and severe hypoxia when HIF-1α is repressed Am. J. Pathol. 2012, 180 (2) 494-504
21. Lopez-Rios, F.; Sanchez-Arago, M.; Garcia-Garcia, E.; Ortega, A. D.; Berrendero, J. R.; Pozo-Rodriguez, F.; Lopez-Encuentra, A.; Ballestin, C.; Cuezva, J. M. Loss of the mitochondrial bioenergetic capacity underlies the glucose avidity of carcinomas Cancer Res. 2007, 67 (19) 9013-9017
22. Denko, N. C. Hypoxia, HIF1 and glucose metabolism in the solid tumour Nat. Rev. Cancer 2008, 8 (9) 705-713
23. Wise, D. R.; DeBerardinis, R. J.; Mancuso, A.; Sayed, N.; Zhang, X. Y.; Pfeiffer, H. K.; Nissim, I.; Daikhin, E.; Yudkoff, M.; McMahon, S. B.; Thompson, C. B. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (48) 18782-18787
24. Cuezva, J. M.; Chen, G.; Alonso, A. M.; Isidoro, A.; Misek, D. E.; Hanash, S. M.; Beer, D. G. The bioenergetic signature of lung adenocarcinomas is a molecular marker of cancer diagnosis and prognosis Carcinogenesis 2004, 25 (7) 1157-1163
25. Keith, B.; Johnson, R. S.; Simon, M. C. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression Nat. Rev. Cancer 2012, 12 (1) 9-22
26. Hung, J. J.; Yang, M. H.; Hsu, H. S.; Hsu, W. H.; Liu, J. S.; Wu, K. J. Prognostic significance of hypoxia-inducible factor-1alpha, TWIST1 and Snail expression in resectable non-small cell lung cancer Thorax 2009, 64 (12) 1082-1089
27. Kim, S. J.; Rabbani, Z. N.; Dewhirst, M. W.; Vujaskovic, Z.; Vollmer, R. T.; Schreiber, E. G.; Oosterwijk, E.; Kelley, M. J. Expression of HIF-1α, CA IX, VEGF, and MMP-9 in surgically resected non-small cell lung cancer Lung Cancer 2005, 49 (3) 325-335
28. Giatromanolaki, A.; Koukourakis, M. I.; Sivridis, E.; Turley, H.; Talks, K.; Pezzella, F.; Gatter, K. C.; Harris, A. L. Relation of hypoxia inducible factor 1 alpha and 2 alpha in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival Br. J. Cancer 2001, 85 (6) 881-980
29. Cavailles, V.; Garcia, M.; Rochefort, H. Regulation of cathepsin-D and pS2 gene expression by growth factors in MCF7 human breast cancer cells Mol. Endocrinol. 1989, 3 (3) 552-558
30. Krishnamachary, B.; Berg-Dixon, S.; Kelly, B.; Agani, F.; Feldser, D.; Ferreira, G.; Iyer, N.; LaRusch, J.; Pak, B.; Taghavi, P.; Semenza, G. L. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1 Cancer Res. 2003, 63 (5) 1138-1143
31. Zaidi, N.; Maurer, A.; Nieke, S.; Kalbacher, H. Cathepsin D: A cellular roadmap Biochem. Biophys. Res. Commun. 2008, 376 (1) 5-9
32. Koblinski, J. E.; Ahram, M.; Sloane, B. F. Unraveling the role of proteases in cancer Clin. Chim. Acta 2000, 291 (2) 113-135
33. Schwartz, M. K. Tissue cathepsins as tumor markers Clin. Chim. Acta 1995, 237 (1-2) 67-78
34. Ohri, S. S.; Vashishta, A.; Vetvickova, J.; Fusek, M.; Vetvicka, V. Procathepsin D expression correlates with invasive and metastatic phenotype of MDA-MB-231 derived cell lines Int. J. Biol. Macromol. 2007, 41 (2) 204-209
35. Sudhir, P. R.; Chen, C. H.; Pavana Kumari, M.; Wang, M. J.; Tsou, C. C.; Sung, T. Y.; Chen, J. Y. Label-free quantitative proteomics and N-glycoproteomics analysis of KRAS-activated human bronchial epithelial cells Mol. Cell. Proteomics 2012, 11 (10) 901-915
36. Mimae, T.; Tsuta, K.; Maeshima, A. M.; Okada, M.; Asamura, H.; Kondo, T.; Tsuda, H. Cathepsin D as a potential prognostic marker for lung adenocarcinoma Pathol., Res. Pract. 2012, 208 (9) 534-540
37. Semenza, G. L.; Jiang, B. H.; Leung, S. W.; Passantino, R.; Concordet, J. P.; Maire, P.; Giallongo, A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1 J. Biol. Chem. 1996, 271 (51) 32529-32537
38. Altenberg, B.; Greulich, K. O. Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes Genomics 2004, 84 (6) 1014-1020
39. Shoshan-Barmatz, V.; Keinan, N.; Zaid, H. Uncovering the role of VDAC in the regulation of cell life and death J. Bioenerg. Biomembr. 2008, 40 (3) 183-191
40. Brahimi-Horn, M. C.; Ben-Hail, D.; Ilie, M.; Gounon, P.; Rouleau, M.; Hofman, V.; Doyen, J.; Mari, B.; Shoshan-Barmatz, V.; Hofman, P.; Pouysségur, J.; Mazure, N. M. Expression of a Truncated Active Form of VDAC1 in Lung Cancer Associates with Hypoxic Cell Survival and Correlates with Progression to Chemotherapy Resistance Cancer Res. 2012, 72 (8) 2140-2150
41. Azoulay-Zohar, H.; Israelson, A.; Abu-Hamad, S.; Shoshan-Barmatz, V. In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death Biochem. J. 2004, 377 (Pt 2) 347-355
42. Shoshan-Barmatz, V.; Ben-Hail, D. VDAC, a multi-functional mitochondrial protein as a pharmacological target Mitochondrion 2012, 12 (1) 24-34
43. Memmott, R. M.; Mercado, J. R.; Maier, C. R.; Kawabata, S.; Fox, S. D.; Dennis, P. A. Metformin prevents tobacco carcinogen - induced lung tumorigenesis Cancer Prev. Res. 2010, 3 (9) 1066-1076
44. Lee, C.; Raffaghello, L.; Brandhorst, S.; Safdie, F. M.; Bianchi, G.; Martin-Montalvo, A.; Pistoia, V.; Wei, M.; Hwang, S.; Merlino, A.; Emionite, L.; de Cabo, R.; Longo, V. D. Fasting cycles retard growth of tumors and sensitize a range of cancer cell types to chemotherapy Sci. Transl. Med. 2012, 4 (124) 124ra27
45. Schulze, A.; Harris, A. L. How cancer metabolism is tuned for proliferation and vulnerable to disruption Nature 2012, 491 (7424) 364-373