Protein-based identification of quantitative trait loci associated with malignant transformation in two HER2+ cellular models of breast cancer

Proteome Science

Volumn 10, Issue 1, 2012, Pages

  Kulkarni, Yogesh M ^a   Klinke II, David J ^a,b  

^a West Virginia University   (United States)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Breast cancer; Ingenuity pathway analysis; MALDI TOF MS; Malignant transformation; Proteomics; Two dimensional gel electrophoresis

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; ALPHA ACTININ 4; CYCLIN DEPENDENT KINASE INHIBITOR 2A; EPIDERMAL GROWTH FACTOR RECEPTOR 2; G PROTEIN COUPLED RECEPTOR KINASE 4; GLUTATHIONE TRANSFERASE P1; INTERLEUKIN 12P35; PEROXIREDOXIN 2; PEROXIREDOXIN 6; PROTEIN BID; PROTEIN KINASE B BETA; PROTEIN KINASE LYN; SOMATOMEDIN; TRANSCRIPTION FACTOR;

AMINO ACID METABOLISM; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CAPNOCYTOPHAGA; CELL MOTILITY; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE TRAIT LOCUS; SIGNAL TRANSDUCTION; TUMOR CELL LINE; UBIQUITINATION;

EID: 84857207921     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-10-11     Document Type: Article

References (63)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674. 10.1016/j.cell.2011.02.013, 21376230.
2. Morange M. The field of cancer research: an indicator of present transformations in biology. Oncogene 2007, 26:7607-7610. 10.1038/sj.onc.1210583, 17653097.
3. Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA. Creation of human tumour cells with defined genetic elements. Nature 1999, 400:464-468. 10.1038/22780, 10440377.
4. Stephens PJ, McBride DJ, Lin ML, Varela I, Pleasance ED, Simpson JT, Stebbings LA, Leroy C, Edkins S, Mudie LJ, Greenman CD, Jia M, Latimer C, Teague JW, Lau KW, Burton J, Quail MA, Swerdlow H, Churcher C, Natrajan R, Sieuwerts AM, Martens JW, Silver DP, Langerod A, Russnes HE, Foekens JA, Reis-Filho JS, van V, Richardson AL, Borresen-Dale AL, Campbell PJ, Futreal PA, Stratton MR. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 2009, 462:1005-1010. 10.1038/nature08645, 20033038.
5. Greenman C, Stephens P, Smith R, Dalgliesh GL, Hunter C, Bignell G, Davies H, Teague J, Butler A, Stevens C, Edkins S, O'Meara S, Vastrik I, Schmidt EE, Avis T, Barthorpe S, Bhamra G, Buck G, Choudhury B, Clements J, Cole J, Dicks E, Forbes S, Gray K, Halliday K, Harrison R, Hills K, Hinton J, Jenkinson A, Jones D, Menzies A, Mironenko T, Perry J, Raine K, Richardson D, Shepherd R, Small A, Tofts C, Varian J, Webb T, West S, Widaa S, Yates A, Cahill DP, Louis DN, Goldstraw P, Nicholson AG, Brasseur F, Looijenga L, Weber BL, Chiew YE, DeFazio A, Greaves MF, Green AR, Campbell P, Birney E, Easton DF, Chenevix-Trench G, Tan MH, Khoo SK, Teh BT, Yuen ST, Leung SY, Wooster R, Futreal PA, Stratton MR. Patterns of somatic mutation in human cancer genomes. Nature 2007, 446:153-158. 10.1038/nature05610, 2712719, 17344846.
6. Bild AH, Yao G, Chang JT, Wang Q, Potti A, Chasse D, Joshi MB, Harpole D, Lancaster JM, Berchuck A, Olson JA, Marks JR, Dressman HK, West M, Nevins JR. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 2006, 439:353-357. 10.1038/nature04296, 16273092.
7. Greaves M, Maley CC. Clonal evolution in cancer. Nature 2012, 481:306-313. 10.1038/nature10762, 22258609.
8. Gygi SP, Rochon Y, Franza BR, Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 1999, 19:1720-1730. 83965, 10022859.
9. Kholodenko BN. Cell-signalling dynamics in time and space. Nat Rev Mol Cell Biol 2006, 7:165-176. 10.1038/nrm1838, 1679905, 16482094.
10. Cox J, Mann M. Is proteomics the new genomics?. Cell 2007, 130:395-398. 10.1016/j.cell.2007.07.032, 17693247.
11. Miles CM, Wayne M. Quantitative Trait Locus (QTL) analysis. Nature Education 2008, 1(1)., http://www.nature.com/scitable/topicpage/quantitative-trait-locus-qtl-analysis-53904
12. Patwardhan AJ, Strittmatter EF, Camp DG, Smith RD, Pallavicini MG. Quantitative proteome analysis of breast cancer cell lines using 18O-labeling and an accurate mass and time tag strategy. Proteomics 2006, 6:2903-2915. 10.1002/pmic.200500582, 16596714.
13. Alexopoulos LG, Saez-Rodriguez J, Cosgrove BD, Lauffenburger DA, Sorger PK. Networks inferred from biochemical data reveal profound differences in toll-like receptor and inflammatory signaling between normal and transformed hepatocytes. Mol Cell Proteomics 2010, 9:1849-1865. 10.1074/mcp.M110.000406, 2938121, 20460255.
14. Perou CM, Sorlie T, Eisen MB, van de RM, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, et al. Molecular portraits of human breast tumours. Nature 2000, 406:747-752. 10.1038/35021093, 10963602.
15. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de RM, Jeffrey SS, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001, 98:10869-10874. 10.1073/pnas.191367098, 58566, 11553815.
16. Sorlie T, Wang Y, Xiao C, Johnsen H, Naume B, Samaha RR, Borresen-Dale AL. Distinct molecular mechanisms underlying clinically relevant subtypes of breast cancer: gene expression analyses across three different platforms. BMC Genomics 2006, 7:127. 10.1186/1471-2164-7-127, 1489944, 16729877.
17. Sihto H, Lundin J, Lehtimaki T, Sarlomo-Rikala M, Butzow R, Holli K, Sailas L, Kataja V, Lundin M, Turpeenniemi-Hujanen T, et al. Molecular subtypes of breast cancers detected in mammography screening and outside of screening. Clin Cancer Res 2008, 14:4103-4110. 10.1158/1078-0432.CCR-07-5003, 18593987.
18. Onitilo AA, Engel JM, Greenlee RT, Mukesh BN. Breast cancer subtypes based on ER/PR and Her2 expression: comparison of clinicopathologic features and survival. Clin Med Res 2009, 7:4-13. 10.3121/cmr.2009.825, 2705275, 19574486.
19. Huang DW, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, Guo Y, Stephens R, Baseler MW, Lane HC, et al. DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res 2007, 35:W169-W175. 10.1093/nar/gkm415, 1933169, 17576678.
20. Lasfargues EY, Coutinho WG, Redfield ES. Isolation of two human tumor epithelial cell lines from solid breast carcinomas. J Natl Canc Inst 1978, 61:961-978.
21. Trempe GL. Human breast cancer in culture. Recent Results Cancer Res 1976, 57:33-41.
22. Bhaskaran N, Lin KW, Gautier A, Woksepp H, Hellman U, Souchelnytskyi S. Comparative proteome profiling of MCF10A and 184A1 human breast epithelial cells emphasized involvement of CDK4 and cyclin D3 in cell proliferation. Proteomics Clin Appl 2009, 3:68-77. 10.1002/prca.200800045, 21136936.
23. Weinberg RA. The Biology of Cancer 2007, New York, NY: Garland Science.
24. Kulkarni YM, Suarez V, Klinke DJ. Inferring predominant pathways in cellular models of breast cancer using limited sample proteomic profiling. BMC Cancer 2010, 10:291. 10.1186/1471-2407-10-291, 2896362, 20550684.
25. Morali OG, Delmas V, Moore R, Jeanney C, Thiery JP, Larue L. IGF-II induces rapid beta-catenin relocation to the nucleus during epithelium to mesenchyme transition. Oncogene 2001, 20:4942-4950. 10.1038/sj.onc.1204660, 11526479.
26. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715. 10.1016/j.cell.2008.03.027, 2728032, 18485877.
27. Voulgari A, Pintzas A. Epithelial-mesenchymal transition in cancer metastasis: mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim Biophys Acta 2009, 1796:75-90.
28. Belfiore A, Malaguarnera R. Insulin receptor and cancer. Endocr Relat Cancer 2011, 18:R125-R147. 10.1530/ERC-11-0074, 21606157.
29. Klinke DJ. Signal transduction networks in cancer: quantitative parameters influence network topology. Cancer Res 2010, 70:1773-1782. 10.1158/0008-5472.CAN-09-3234, 2831142, 20179207.
30. Kokai Y, Myers JN, Wada T, Brown VI, LeVea CM, Davis JG, Dobashi K, Greene MI. Synergistic interaction of p185c-neu and the EGF receptor leads to transformation of rodent fibroblasts. Cell 1989, 58:287-292. 10.1016/0092-8674(89)90843-X, 2568888.
31. Kawazoe Y, Nakai A, Tanabe M, Nagata K. Proteasome inhibition leads to the activation of all members of the heat-shock-factor family. Eur J Biochem 1998, 255:356-362. 10.1046/j.1432-1327.1998.2550356.x, 9716376.
32. Bush KT, Goldberg AL, Nigam SK. Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. J Biol Chem 1997, 272:9086-9092. 10.1074/jbc.272.14.9086, 9083035.
33. Williams K, Chubb C, Huberman E, Giometti CS. Analysis of differential protein expression in normal and neoplastic human breast epithelial cell lines. Electrophoresis 1998, 19:333-343. 10.1002/elps.1150190231, 9548300.
34. Franzen B, Linder S, Alaiya AA, Eriksson E, Fujioka K, Bergman AC, Jornvall H, Auer G. Analysis of polypeptide expression in benign and malignant human breast lesions. Electrophoresis 1997, 18:582-587. 10.1002/elps.1150180341, 9150945.
35. Fernandez PM, Tabbara SO, Jacobs LK, Manning FC, Tsangaris TN, Schwartz AM, Kennedy KA, Patierno SR. Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast Cancer Res Treat 2000, 59:15-26. 10.1023/A:1006332011207, 10752676.
36. Barazi HO, Zhou L, Templeton NS, Krutzsch HC, Roberts DD. Identification of heat shock protein 60 as a molecular mediator of alpha 3 beta 1 integrin activation. Cancer Res 2002, 62:1541-1548.
37. Li DQ, Wang L, Fei F, Hou YF, Luo JM, Zeng R, Wu J, Lu JS, Di GH, Ou ZL, Xia QC, Shen ZZ, Shao ZM. Identification of breast cancer metastasis-associated proteins in an isogenic tumor metastasis model using two-dimensional gel electrophoresis and liquid chromatography-ion trap-mass spectrometry. Proteomics 2006, 6:3352-3368. 10.1002/pmic.200500617, 16637015.
38. Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 2008, 8:782-798. 10.1038/nrc2465, 18813321.
39. Norbury CJ, Zhivotovsky B. DNA damage-induced apoptosis. Oncogene 2004, 23:2797-2808. 10.1038/sj.onc.1207532, 15077143.
40. Pucci B, Kasten M, Giordano A. Cell cycle and apoptosis. Neoplasia 2000, 2:291-299. 10.1038/sj.neo.7900101, 1550296, 11005563.
41. Huang DC, Strasser A. BH3-Only proteins-essential initiators of apoptotic cell death. Cell 2000, 103:839-842. 10.1016/S0092-8674(00)00187-2, 11136969.
42. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG, Colman PM, Day CL, Adams JM, Huang DC. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 2005, 17:393-403. 10.1016/j.molcel.2004.12.030, 15694340.
43. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, Bruncko M, Deckwerth TL, Dinges J, Hajduk PJ, Joseph MK, Kitada S, Korsmeyer SJ, Kunzer AR, Letai A, Li C, Mitten MJ, Nettesheim DG, Ng S, Nimmer PM, O'Connor JM, Oleksijew A, Petros AM, Reed JC, Shen W, Tahir SK, Thompson CB, Tomaselli KJ, Wang B, Wendt MD, Zhang H, Fesik SW, Rosenberg SH. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005, 435:677-681. 10.1038/nature03579, 15902208.
44. Walensky LD, Kung AL, Escher I, Malia TJ, Barbuto S, Wright RD, Wagner G, Verdine GL, Korsmeyer SJ. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 2004, 305:1466-1470. 10.1126/science.1099191, 1360987, 15353804.
45. Disson O, Haouzi D, Desagher S, Loesch K, Hahne M, Kremer EJ, Jacquet C, Lemon SM, Hibner U, Lerat H. Impaired clearance of virus-infected hepatocytes in transgenic mice expressing the hepatitis C virus polyprotein. Gastroenterology 2004, 126:859-872. 10.1053/j.gastro.2003.12.005, 14988840.
46. Amm HM, Zhou T, Steg AD, Kuo H, Li Y, Buchsbaum DJ. Mechanisms of drug sensitization to TRA-8, an agonistic death receptor 5 antibody, involve modulation of the intrinsic apoptotic pathway in human breast cancer cells. Mol Cancer Res 2011, 9:403-417. 10.1158/1541-7786.MCR-10-0133, 21357440.
47. Purcell JW, Davis J, Reddy M, Martin S, Samayoa K, Vo H, Thomsen K, Bean P, Kuo WL, Ziyad S, Billig J, Feiler HS, Gray JW, Wood KW, Cases S. Activity of the kinesin spindle protein inhibitor ispinesib (SB-715992) in models of breast cancer. Clin Cancer Res 2010, 16:566-576. 10.1158/1078-0432.CCR-09-1498, 2844774, 20068098.
48. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 2003, 83:731-801.
49. Chhabra A, Fernando H, Mansel RE, Jiang WG. Pattern of expression of calpain subunits (large and small) in human breast cancer and the prognostic significance. ASCO Annual Meeting Proceedings 2007, 25(18S):6-20.
50. Kubbutat MH, Vousden KH. Proteolytic cleavage of human p53 by calpain: a potential regulator of protein stability. Mol Cell Biol 1997, 17:460-468. 231771, 8972227.
51. Han Y, Weinman S, Boldogh I, Walker RK, Brasier AR. Tumor necrosis factor-alpha-inducible IkappaBalpha proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-kappab activation. J Biol Chem 1999, 274:787-794. 10.1074/jbc.274.2.787, 9873017.
52. Zhu H, Zhang L, Huang X, Davis JJ, Jacob DA, Teraishi F, Chiao P, Fang B. Overcoming acquired resistance to TRAIL by chemotherapeutic agents and calpain inhibitor I through distinct mechanisms. Mol Ther 2004, 9:666-673. 10.1016/j.ymthe.2004.02.007, 15120327.
53. Mlynarczuk-Bialy I, Roeckmann H, Kuckelkorn U, Schmidt B, Umbreen S, Golab J, Ludwig A, Montag C, Wiebusch L, Hagemeier C, Schadendorf D, Kloetzel PM, Seifert U. Combined effect of proteasome and calpain inhibition on cisplatin-resistant human melanoma cells. Cancer Res 2006, 66:7598-7605. 10.1158/0008-5472.CAN-05-2614, 16885359.
54. Kulkarni S, Reddy KB, Esteva FJ, Moore HC, Budd GT, Tubbs RR. Calpain regulates sensitivity to trastuzumab and survival in HER2-positive breast cancer. Oncogene 2010, 29:1339-1350. 10.1038/onc.2009.422, 19946330.
55. Simonin Y, Disson O, Lerat H, Antoine E, Biname F, Rosenberg AR, Desagher S, Lassus P, Bioulac-Sage P, Hibner U. Calpain activation by hepatitis C virus proteins inhibits the extrinsic apoptotic signaling pathway. Hepatology 2009, 50:1370-1379. 10.1002/hep.23169, 19711428.
56. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 1996, 274:787-789. 10.1126/science.274.5288.787, 8864120.
57. Sovak MA, Bellas RE, Kim DW, Zanieski GJ, Rogers AE, Traish AM, Sonenshein GE. Aberrant nuclear factor-kappaB/Rel expression and the pathogenesis of breast cancer. J Clin Invest 1997, 100:2952-2960. 10.1172/JCI119848, 508506, 9399940.
58. Wang CY, Cusack JC, Liu R, Baldwin AS. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-kappaB. Nat Med 1999, 5:412-417. 10.1038/7410, 10202930.
59. Garg A, Aggarwal BB. Nuclear transcription factor-kappaB as a target for cancer drug development. Leukemia 2002, 16:1053-1068. 10.1038/sj.leu.2402482, 12040437.
60. Bateman NW, Sun M, Hood BL, Flint MS, Conrads TP. Defining central themes in breast cancer biology by differential proteomics: conserved regulation of cell spreading and focal adhesion kinase. J Proteome Res 2010, 9:5311-5324. 10.1021/pr100580e, 20681588.
61. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J Royal Stat Soc Series B (Methodological) 1995, 57(1):289-300.
62. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
63. Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13. 10.1093/nar/gkn923, 2615629, 19033363.