Global analysis of protein folding thermodynamics for disease state characterization

Journal of Proteome Research

Volumn 14, Issue 5, 2015, Pages 2287-2297

  Adhikari, Jagat ^a   West, Graham M ^b,d   Fitzgerald, Michael C ^a,c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c DUKE UNIVERSITY   (United States)

^d PFIZER INC   (United States)

Author keywords

breast cancer; chemical denaturation; mass spectrometry; MCF 10A; MCF 7; MDA MB 231; protein folding; proteomics; SILAC

Indexed keywords

AMINO ACID; ESTROGEN RECEPTOR; STABLE ISOTOPE; PROTEOME; TUMOR MARKER; TUMOR PROTEIN;

ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; LARGE SCALE PRODUCTION; MCF 7 CELL LINE; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STABILITY; THERMODYNAMICS; BREAST NEOPLASMS; CHEMISTRY; GENE EXPRESSION; GENETICS; ISOLATION AND PURIFICATION; ISOTOPE LABELING; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PATHOLOGY; PROCEDURES; PROTEOMICS; TUMOR CELL LINE;

AMINO ACIDS; BIOMARKERS, TUMOR; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION; HUMANS; ISOTOPE LABELING; MOLECULAR SEQUENCE ANNOTATION; NEOPLASM PROTEINS; OXIDATION-REDUCTION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEOME; PROTEOMICS; THERMODYNAMICS;

EID: 84929657455     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00057     Document Type: Article

References (58)

1. Walther, T. C.; Mann, M. Mass spectrometry-based proteomics in cell biology J. Cell Biol. 2010, 190 (4) 491-500
2. Oppermann, F. S.; Gnad, F.; Olsen, J. V.; Hornberger, R.; Greff, Z.; Keri, G.; Mann, M.; Daub, H. Large-scale Proteomics Analysis of the Human Kinome Mol. Cell. Proteomics 2009, 8 (7) 1751-1764
3. Alizadeh, A. A.; Eisen, M. B.; Davis, R. E.; Ma, C.; Lossos, I. S.; Rosenwald, A.; Boldrick, J. G.; Sabet, H.; Tran, T.; Yu, X.; Powell, J. I.; Yang, L. M.; Marti, G. E.; Moore, T.; Hudson, J.; Lu, L. S.; Lewis, D. B.; Tibshirani, R.; Sherlock, G.; Chan, W. C.; Greiner, T. C.; Weisenburger, D. D.; Armitage, J. O.; Warnke, R.; Levy, R.; Wilson, W.; Grever, M. R.; Byrd, J. C.; Botstein, D.; Brown, P. O.; Staudt, L. M. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling Nature 2000, 403 (6769) 503-511
4. Golub, T. R.; Slonim, D. K.; Tamayo, P.; Huard, C.; Gaasenbeek, M.; Mesirov, J. P.; Coller, H.; Loh, M. L.; Downing, J. R.; Caligiuri, M. A.; Bloomfield, C. D.; Lander, E. S. Molecular classification of cancer: Class discovery and class prediction by gene expression monitoring Science 1999, 286 (5439) 531-537
5. Lu, J.; Getz, G.; Miska, E. A.; Alvarez-Saavedra, E.; Lamb, J.; Peck, D.; Sweet-Cordero, A.; Ebet, B. L.; Mak, R. H.; Ferrando, A. A.; Downing, J. R.; Jacks, T.; Horvitz, H. R.; Golub, T. R. MicroRNA expression profiles classify human cancers Nature 2005, 435 (7043) 834-838
6. Perou, C. M.; Sorlie, T.; Eisen, M. B.; van de Rijn, M.; Jeffrey, S. S.; Rees, C. A.; Pollack, J. R.; Ross, D. T.; Johnsen, H.; Akslen, L. A.; Fluge, O.; Pergamenschikov, A.; Williams, C.; Zhu, S. X.; Lonning, P. E.; Borresen-Dale, A. L.; Brown, P. O.; Botstein, D. Molecular portraits of human breast tumours Nature 2000, 406 (6797) 747-752
7. Sorlie, T.; Perou, C. M.; Tibshirani, R.; Aas, T.; Geisler, S.; Johnsen, H.; Hastie, T.; Eisen, M. B.; van de Rijn, M.; Jeffrey, S. S.; Thorsen, T.; Quist, H.; Matese, J. C.; Brown, P. O.; Botstein, D.; Lonning, P. E.; Borresen-Dale, A. L. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (19) 10869-10874
8. Sorlie, T.; Tibshirani, R.; Parker, J.; Hastie, T.; Marron, J. S.; Nobel, A.; Deng, S.; Johnsen, H.; Pesich, R.; Geisler, S.; Demeter, J.; Perou, C. M.; Lonning, P. E.; Brown, P. O.; Borresen-Dale, A. L.; Botstein, D. Repeated observation of breast tumor subtypes in independent gene expression data sets Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (14) 8418-8423
9. van't Veer, L. J.; Dai, H. Y.; van de Vijver, M. J.; He, Y. D. D.; Hart, A. A. M.; Mao, M.; Peterse, H. L.; van der Kooy, K.; Marton, M. J.; Witteveen, A. T.; Schreiber, G. J.; Kerkhoven, R. M.; Roberts, C.; Linsley, P. S.; Bernards, R.; Friend, S. H. Gene expression profiling predicts clinical outcome of breast cancer Nature 2002, 415 (6871) 530-536
10. Volinia, S.; Calin, G. A.; Liu, C. G.; Ambs, S.; Cimmino, A.; Petrocca, F.; Visone, R.; Iorio, M.; Roldo, C.; Ferracin, M.; Prueitt, R. L.; Yanaihara, N.; Lanza, G.; Scarpa, A.; Vecchione, A.; Negrini, M.; Harris, C. C.; Croce, C. M. A microRNA expression signature of human solid tumors defines cancer gene targets Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (7) 2257-2261
11. Adam, B. L.; Qu, Y. S.; Davis, J. W.; Ward, M. D.; Clements, M. A.; Cazares, L. H.; Semmes, O. J.; Schellhammer, P. F.; Yasui, Y.; Feng, Z. D.; Wright, G. L. Serum protein fingerprinting coupled with a pattern-matching algorithm distinguishes prostate cancer from benign prostate hyperplasia and healthy men Cancer Res. 2002, 62 (13) 3609-3614
12. Hanash, S. Disease proteomics Nature 2003, 422 (6928) 226-232
13. Li, J. N.; Zhang, Z.; Rosenzweig, J.; Wang, Y. Y.; Chan, D. W. Proteomics and bioinformatics approaches for identification of serum biomarkers to detect breast cancer Clin. Chem. 2002, 48 (8) 1296-1304
14. Rikova, K.; Guo, A.; Zeng, Q.; Possemato, A.; Yu, J.; Haack, H.; Nardone, J.; Lee, K.; Reeves, C.; Li, Y.; Hu, Y.; Tan, Z. P.; Stokes, M.; Sullivan, L.; Mitchell, J.; Wetzel, R.; MacNeill, J.; Ren, J. M.; Yuan, J.; Bakalarski, C. E.; Villen, J.; Kornhauser, J. M.; Smith, B.; Li, D.; Zhou, X.; Gygi, S. P.; Gu, T. L.; Polakiewicz, R. D.; Rush, J.; Comb, M. J. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer Cell 2007, 131 (6) 1190-1203
15. Yanagisawa, K.; Shyr, Y.; Xu, B. G. J.; Massion, P. P.; Larsen, P. H.; White, B. C.; Roberts, J. R.; Edgerton, M.; Gonzalez, A.; Nadaf, S.; Moore, J. H.; Caprioli, R. M.; Carbone, D. P. Proteomic patterns of tumour subsets in non-small-cell lung cancer Lancet 2003, 362 (9382) 433-439
16. Jessani, N.; Liu, Y. S.; Humphrey, M.; Cravatt, B. F. Enzyme activity profiles of the secreted and membrane proteome that depict cancer cell invasiveness Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (16) 10335-10340
17. Apetri, A. C.; Surewicz, K.; Surewicz, W. K. The effect of disease-associated mutations on the folding pathway of human prion protein J. Biol. Chem. 2004, 279 (17) 18008-18014
18. Chiti, F.; Taddei, N.; Bucciantini, M.; White, P.; Ramponi, G.; Dobson, C. M. Mutational analysis of the propensity for amyloid formation by a globular protein EMBO J. 2000, 19 (7) 1441-1449
19. Liemann, S.; Glockshuber, R. Influence of amino acid substitutions related to inherited human prion diseases on the thermodynamic stability of the cellular prion protein Biochemistry 1999, 38 (11) 3258-3267
20. Ma, J. Y.; Wollmann, R.; Lindquist, S. Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol Science 2002, 298 (5599) 1781-1785
21. Qu, B. H.; Thomas, P. J. Alteration of the cystic fibrosis transmembrane conductance regulator folding pathway-Effects of the Delta F508 mutation on the thermodynamic stability and folding yield of NBD1 J. Biol. Chem. 1996, 271 (13) 7261-7264
22. Varani, L.; Hasegawa, M.; Spillantini, M. G.; Smith, M. J.; Murrell, J. R.; Ghetti, B.; Klug, A.; Goedert, M.; Varani, G. Structure of tau exon 10 splicing regulatory element RNA and destabilization by mutations of frontotemporal dementia and parkinsonism linked to chromosome 17 Proc. Natl. Acad. Sci. U.S.A. 1999, 96 (14) 8229-8234
23. Proctor, E. A.; Ding, F.; Dokholyan, N. V. Structural and thermodynamic effects of post-translational modifications in mutant and wild type Cu, Zn superoxide dismutase J. Mol. Biol. 2011, 408 (3) 555-67
24. Bullock, A. N.; Henckel, J.; DeDecker, B. S.; Johnson, C. M.; Nikolova, P. V.; Proctor, M. R.; Lane, D. P.; Fersht, A. R. Thermodynamic stability of wild-type and mutant p53 core domain Proc. Natl. Acad. Sci. U.S.A. 1997, 94 (26) 14338-42
25. Mayer, S.; Rudiger, S.; Ang, H. C.; Joerger, A. C.; Fersht, A. R. Correlation of levels of folded recombinant p53 in escherichia coli with thermodynamic stability in vitro J. Mol. Biol. 2007, 372 (1) 268-76
26. Gyorgy, B.; Toth, E.; Tarcsa, E.; Falus, A.; Buzas, E. I. Citrullination: a posttranslational modification in health and disease Int. J. Biochem. Cell Biol. 2006, 38 (10) 1662-77
27. West, G. M.; Tucker, C. L.; Xu, T.; Park, S. K.; Han, X. M.; Yates, J. R.; Fitzgerald, M. C. Quantitative proteomics approach for identifying protein-drug interactions in complex mixtures using protein stability measurements Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (20) 9078-9082
28. Strickland, E. C.; Geer, M. A.; Tran, D. T.; Adhikari, J.; West, G. M.; DeArmond, P. D.; Xu, Y.; Fitzgerald, M. C. Thermodynamic analysis of protein-ligand binding interactions in complex biological mixtures using the stability of proteins from rates of oxidation Nat. Protoc. 2013, 8 (1) 148-161
29. Dearmond, P. D.; Xu, Y.; Strickland, E. C.; Daniels, K. G.; Fitzgerald, M. C. Thermodynamic analysis of protein-ligand interactions in complex biological mixtures using a shotgun proteomics approach J. Proteome Res. 2011, 10 (11) 4948-58
30. Tran, D. T.; Adhikari, J.; Fitzgerald, M. C. SILAC-Based Strategy for Proteome-Wide Thermodynamic Analysis of Protein-Ligand Binding Interactions Mol. Cell. Proteomics 2014, 13, 1800-1813
31. Adhikari, J.; Fitzgerald, M. C. SILAC-pulse proteolysis: A mass spectrometry-based method for discovery and cross-validation in proteome-wide studies of ligand binding J. Am. Soc. Mass Spectrom. 2014, 25 (12) 2073-83
32. Feng, Y. H.; De Franceschi, G.; Kahraman, A.; Soste, M.; Melnik, A.; Boersema, P. J.; de Laureto, P. P.; Nikolaev, Y.; Oliveira, A. P.; Picotti, P. Global analysis of protein structural changes in complex proteomes Nat. Biotechnol. 2014, 32 (10) 1036-1044
33. Savitski, M. M.; Reinhard, F. B. M.; Franken, H.; Werner, T.; Savitski, M. F.; Eberhard, D.; Molina, D. M.; Jafari, R.; Dovega, R. B.; Klaeger, S.; Kuster, B.; Nordlund, P.; Bantscheff, M.; Drewes, G. Tracking cancer drugs in living cells by thermal profiling of the proteome Science 2014, 346 (6205) 1255784
34. Liu, P. F.; Kihara, D.; Park, C. Energetics-based discovery of protein-ligand interactions on a proteomic scale J. Mol. Biol. 2011, 408 (1) 147-62
35. Chang, Y.; Schlebach, J. P.; VerHeul, R. A.; Park, C. Simplified proteomics approach to discover protein-ligand interactions Protein Sci. 2012, 21 (9) 1280-1287
36. Lomenick, B.; Hao, R.; Jonai, N.; Chin, R. M.; Aghajan, M.; Warburton, S.; Wang, J. N.; Wu, R. P.; Gomez, F.; Loo, J. A.; Wohlschlegel, J. A.; Vondriska, T. M.; Pelletier, J.; Herschman, H. R.; Clardy, J.; Clarke, C. F.; Huang, J. Target identification using drug affinity responsive target stability (DARTS) Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (51) 21984-21989
37. Jafari, R.; Almqvist, H.; Axelsson, H.; Ignatushchenko, M.; Lundback, T.; Nordlund, P.; Molina, D. M. The cellular thermal shift assay for evaluating drug target interactions in cells Nat. Protoc. 2014, 9 (9) 2100-2122
38. West, G. M.; Tang, L.; Fitzgerald, M. C. Thermodynamic analysis of protein stability and ligand binding using a chemical modification- and mass spectrometry-based strategy Anal. Chem. 2008, 80 (11) 4175-85
39. Ong, S. E.; Mann, M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC) Nat. Protoc 2006, 1 (6) 2650-2660
40. Geiger, T.; Madden, S. F.; Gallagher, W. M.; Cox, J.; Mann, M. Proteomic portrait of human breast cancer progression identifies novel prognostic markers Cancer Res. 2012, 72 (9) 2428-39
41. Bendall, S. C.; Hughes, C.; Stewart, M. H.; Doble, B.; Bhatia, M.; Lajoie, G. A. Prevention of amino acid conversion in SILAC experiments with embryonic stem cells Mol. Cell. Proteomics 2008, 7 (9) 1587-1597
42. Cox, J.; Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 2008, 26 (12) 1367-1372
43. Vizcaino, J. A.; Cote, R. G.; Csordas, A.; Dianes, J. A.; Fabregat, A.; Foster, J. M.; 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. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013 Nucleic Acids Res. 2013, 41 (Database issue) D1063-9
44. Myers, J. K.; Pace, C. N.; Scholtz, J. M. Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding Protein Sci. 1995, 4 (10) 2138-2148
45. Vora, H. H.; Patel, N. A.; Rajvik, K. N.; Mehta, S. V.; Brahmbhatt, B. V.; Shah, M. J.; Shukla, S. N.; Shah, P. M. Cytokeratin and vimentin expression in breast cancer Int. J. Biol. Markers 2009, 24 (1) 38-46
46. Cimpean, A. M.; Suciu, C.; Ceausu, R.; Tatucu, D.; Muresan, A. M.; Raica, M. Relevance of the immunohistochemical expression of cytokeratin 8/18 for the diagnosis and classification of breast cancer Rom. J. Morphol. Embryol. 2008, 49 (4) 479-483
47. Derycke, L.; Stove, C.; Vercoutter-Edouart, A. S.; De Wever, O.; Dolle, L.; Colpaert, N.; Depypere, H.; Michalski, J. C.; Bracke, M. The role of non-muscle myosin IIA in aggregation and invasion of human MCF-7 breast cancer cells Int. J. Dev. Biol. 2011, 55 (7-9) 835-840
48. Krasnov, G. S.; Dmitriev, A. A.; Snezhkina, A. V.; Kudryavtseva, A. V. Deregulation of glycolysis in cancer: glyceraldehyde-3-phosphate dehydrogenase as a therapeutic target Expert Opin. Ther. Targets 2013, 17 (6) 681-693
49. Dennison, J. B.; Molina, J. R.; Mitra, S.; Gonzalez-Angulo, A. M.; Balko, J. M.; Kuba, M. G.; Sanders, M. E.; Pinto, J. A.; Gomez, H. L.; Arteaga, C. L.; Brown, R. E.; Mills, G. B. Lactate Dehydrogenase B: A Metabolic Marker of Response to Neoadjuvant Chemotherapy in Breast Cancer Clin. Cancer Res. 2013, 19 (13) 3703-3713
50. Brown, N. J.; Higham, S. E.; Perunovic, B.; Arafa, M.; Balasubramanian, S.; Rehman, I. Lactate Dehydrogenase-B Is Silenced by Promoter Methylation in a High Frequency of Human Breast Cancers PLoS One 2013, 8 (2) e57697
51. Nagaraja, G. M.; Othman, M.; Fox, B. P.; Alsaber, R.; Pellegrino, C. M.; Zeng, Y.; Khanna, R.; Tamburini, P.; Swaroop, A.; Kandpal, R. P. Gene expression signatures and biomarkers of noninvasive and invasive breast cancer cells: comprehensive profiles by representational difference analysis, microarrays and proteomics Oncogene 2006, 25 (16) 2328-2338
52. Capello, M.; Ferri-Borgogno, S.; Cappello, P.; Novelli, F. alpha-Enolase: a promising therapeutic and diagnostic tumor target FEBS J. 2011, 278 (7) 1064-74
53. 2+-Dependent Neutral Protease (Calpain) Activity in Breast Cancer Tissue and Estrogen Receptor Status Breast Cancer 1996, 3 (1) 13-17
54. Dulyaninova, N. G.; House, R. P.; Betapudi, V.; Bresnick, A. R. Myosin-IIA heavy-chain phosphorylation regulates the motility of MDA-MB-231 carcinoma cells Mol. Biol. Cell 2007, 18 (8) 3144-3155
55. Glondu, M.; Coopman, P.; Laurent-Matha, V.; Garcia, M.; Rochefort, H.; Liaudet-Coopman, E. A mutated cathepsin-D devoid of its catalytic activity stimulates the growth of cancer cells Oncogene 2001, 20 (47) 6920-9
56. Mi, H. Y.; Muruganujan, A.; Casagrande, J. T.; Thomas, P. D. Large-scale gene function analysis with the PANTHER classification system Nat. Protoc. 2013, 8 (8) 1551-1566
57. Mi, H. Y.; Muruganujan, A.; Thomas, P. D. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees Nucleic Acids Res. 2013, 41 (D1) D377-D386
58. Lacroix, M.; Leclercq, G. Relevance of breast cancer cell lines as models for breast tumours: an update Breast Cancer Res. Treat. 2004, 83 (3) 249-89