A kernel-based integration of genome-wide data for clinical decision support
Tóm tắt
Although microarray technology allows the investigation of the transcriptomic make-up of a tumor in one experiment, the transcriptome does not completely reflect the underlying biology due to alternative splicing, post-translational modifications, as well as the influence of pathological conditions (for example, cancer) on transcription and translation. This increases the importance of fusing more than one source of genome-wide data, such as the genome, transcriptome, proteome, and epigenome. The current increase in the amount of available omics data emphasizes the need for a methodological integration framework. We propose a kernel-based approach for clinical decision support in which many genome-wide data sources are combined. Integration occurs within the patient domain at the level of kernel matrices before building the classifier. As supervised classification algorithm, a weighted least squares support vector machine is used. We apply this framework to two cancer cases, namely, a rectal cancer data set containing microarray and proteomics data and a prostate cancer data set containing microarray and genomics data. For both cases, multiple outcomes are predicted. For the rectal cancer outcomes, the highest leave-one-out (LOO) areas under the receiver operating characteristic curves (AUC) were obtained when combining microarray and proteomics data gathered during therapy and ranged from 0.927 to 0.987. For prostate cancer, all four outcomes had a better LOO AUC when combining microarray and genomics data, ranging from 0.786 for recurrence to 0.987 for metastasis. For both cancer sites the prediction of all outcomes improved when more than one genome-wide data set was considered. This suggests that integrating multiple genome-wide data sources increases the predictive performance of clinical decision support models. This emphasizes the need for comprehensive multi-modal data. We acknowledge that, in a first phase, this will substantially increase costs; however, this is a necessary investment to ultimately obtain cost-efficient models usable in patient tailored therapy.
Tài liệu tham khảo
Shawe-Taylor J, Cristianini N: Kernel Methods for Pattern Analysis. 2004, Cambridge: Cambridge University Press
Bhaskar H, Hoyle DC, Singh S: Machine learning in bioinformatics: a brief survey and recommendations for practitioners. Comput Biol Med. 2006, 36: 1104-1125. 10.1016/j.compbiomed.2005.09.002.
Suykens JAK, Vandewalle J: Least squares support vector machine classifiers. Neural Processing Lett. 1999, 9: 293-300. 10.1023/A:1018628609742.
Suykens JAK, Van Gestel T, De Brabanter J, De Moor B, Vandewalle J: Least Squares Support Vector Machines. 2002, Singapore: World Scientific
Cawley GC: Leave-one-out cross-validation based model selection criteria for weighted LS-SVMs. Proc Int Joint Conf on Neural Networks. 2006, 1661-1668. full_text.
Alon A, Barkai N, Notterman DA, Gish K, Ybarra S, Mack D, Levine AJ: Broad patterns of gene expression revealed by clustering analysis of tumor and normal colon tissues probed by oligonucleotide arrays. Proc Natl Acad Sci USA. 1999, 96: 6745-6750. 10.1073/pnas.96.12.6745.
Golub TR, Slonim DK, Tamayo P, Huard C, Gaasenbeek M, Mesirov JP, Coller H, Loh ML, Downing JR, Caligiuri MA, Bloomfield CD, Lander ES: Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science. 1999, 286: 531-537. 10.1126/science.286.5439.531.
Cardoso F, van't Veer L, Rutgers E, Loi S, Mook S, Piccart-Gebhart MJ: Clinical application of the 70-gene profile: the MINDACT trial. J Clin Oncol. 2008, 26: 729-735. 10.1200/JCO.2007.14.3222.
Sparano JA: TAILORx: trial assigning individualized options for treatment (Rx). Clin Breast Cancer. 2006, 7: 347-350. 10.3816/CBC.2006.n.051.
Sparano JA, Paik S: Development of the 21-gene assay and its application in clinical practice and clinical trials. J Clin Oncol. 2008, 26: 721-728. 10.1200/JCO.2007.15.1068.
Pinkel D, Albertson DG: Array comparative genomic hybridization and its applications in cancer. Nat Genet. 2005, 37: S11-S17. 10.1038/ng1569.
Esteller M: Epigenetics in cancer. N Engl J Med. 2008, 358: 1148-1159. 10.1056/NEJMra072067.
Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, Fiegler H, Shapero MH, Carson AR, Chen W, Cho EK, Dallaire S, Freeman JL, González JR, Gratacòs M, Huang J, Kalaitzopoulos D, Komura D, MacDonald JR, Marshall CR, Mei R, Montgomery L, Nishimura K, Okamura K, Shen F, Somerville MJ, Tchinda J, Valsesia A, Woodwark C, Yang F, et al: Global variation in copy number in the human genome. Nature. 2006, 444: 444-454. 10.1038/nature05329.
Frohling S, Dohner H: Chromosomal abnormalities in cancer. N Engl J Med. 2008, 359: 722-734. 10.1056/NEJMra0803109.
Kolch W, Mischak H, Pitt AR: The molecular make-up of a tumor: proteomics in cancer research. Clin Sci. 2005, 108: 369-383. 10.1042/CS20050006.
Aebersold R, Mann M: Mass spectrometry-based proteomics. Nature. 2003, 422: 198-207. 10.1038/nature01511.
MacBeatch G, Schreiber SL: Printing proteins as microarrays for high-throughput function determination. Science. 2000, 289: 1760-1763.
Cooper GM, Zerr T, Kidd JM, Eichler EE, Nickerson DA: Systematic assessment of copy number variant detection via genome-wide SNP genotyping. Nat Genet. 2008, 40: 1199-1203. 10.1038/ng.236.
Tibshirani RJ, Efron B: Pre-validation and inference in microarrays. Stat Appl Genet Mol Biol. 2002, 1: Article 1-
Nevins JR, Huang ES, Dressman H, Pittman J, Huang AT, West M: Towards integrated clinico-genomic models for personalized medicine: combining gene expression signatures and clinical factors in breast cancer outcomes prediction. Hum Mol Genet. 2003, 12: R153-R157. 10.1093/hmg/ddg287.
Wang SM, Ooi LL, Hui KM: Identification and validation of a novel gene signature associated with the recurrence of human hepatocellular carcinoma. Clin Cancer Res. 2007, 13: 6275-6283. 10.1158/1078-0432.CCR-06-2236.
Mathew JP, Taylor BS, Bader GD, Pyarajan S, Antoniotti M, Chinnaiyan AM, Sander C, Burakoff SJ, Mishra B: From bytes to bedside: data integration and computational biology for translational cancer research. PLoS Comput Biol. 2007, 3: e12-10.1371/journal.pcbi.0030012.
Fridlyand J, Snijders AM, Ylstra B, Li H, Olshen A, Segraves R, Dairkee S, Tokuyasu T, Ljung BM, Jain AN, McLennan J, Ziegler J, Chin K, Devries S, Feiler H, Gray JW, Waldman F, Pinkel D, Albertson DG: Breast tumor copy number aberration phenotypes and genomic instability. BMC Cancer. 2006, 6: 96-10.1186/1471-2407-6-96.
Tomioka N, Oba S, Ohira M, Misra A, Fridlyand J, Ishii S, Nakamura Y, Isogai E, Hirata T, Yoshida Y, Todo S, Kanedo Y, Albertson DG, Pinkel D, Feuerstein BG, Nakagawara A: Novel risk stratification of patients with neuroblastoma by genomic signature, which is independent of molecular signature. Oncogene. 2008, 27: 441-449. 10.1038/sj.onc.1210661.
Waters KM, Pounds JG, Thrall BD: Data merging for integrated microarray and proteomic analysis. Brief Funct Genomic Proteomic. 2006, 5: 261-272. 10.1093/bfgp/ell019.
Goble C, Stevens R: State of the nation in data integration for bioinformatics. J Biomed Inform. 2008, 41: 687-693. 10.1016/j.jbi.2008.01.008.
Bitton DA, Okoniewski MJ, Connolly Y, Miller CJ: Exon level integration of proteomics and microarray data. BMC Bioinformatics. 2008, 9: 118-10.1186/1471-2105-9-118.
Lanckriet GRG, De Bie T, Cristianini N, Jordan MI, Noble WS: A statistical framework for genomic data fusion. Bioinformatics. 2004, 20: 2626-2635. 10.1093/bioinformatics/bth294.
Daemen A, Gevaert O, Moor BD: Integration of clinical and microarray data with kernel methods. Conf Proc IEEE Eng Med Biol Soc. 2007, 5411-5415.
Lapointe J, Li C, Higgins JP, Rijn van de M, Bair E, Montgomery K, Ferrari M, Egevad L, Rayford W, Bergerheim U, Ekman P, DeMarzo AM, Tibshirani R, Botstein D, Brown PO, Brooks JD, Pollack JR: Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc Natl Acad Sci USA. 2004, 101: 811-816. 10.1073/pnas.0304146101.
Lapointe J, Li C, Giacomini CP, Salari K, Huang S, Wang P, Ferrari M, Hernandez-Boussard T, Brooks JD, Pollack JR: Genomic profiling reveals alternative genetic pathways of prostate tumorigenesis. Cancer Res. 2007, 67: 8504-8510. 10.1158/0008-5472.CAN-07-0673.
Machiels JP, Sempoux C, Scalliet P, Coche JC, Humblet Y, Van Cutsem E, Kerger J, Canon JL, Peeters M, Aydin S, Laurent S, Kartheuser A, Coster B, Roels S, Daisne JF, Honhon B, Duck L, Kirkove C, Bonny MA, Haustermans K: Phase I/II study of preoperative cetuximab, capecitabine, and external beam radiotherapy in patients with rectal cancer. Ann Oncol. 2007, 18: 738-744. 10.1093/annonc/mdl460.
Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003, 4: 249-264. 10.1093/biostatistics/4.2.249.
Wheeler JMD, Warren BF, Mortensen NJ, Ekanyaka N, Kulacoglu H, Jones AC, George BD, Kettlewell MGW: Quantification of histologic regression of rectal cancer after irradiation. Dis Colon Rectum. 2002, 45: 1051-1056. 10.1007/s10350-004-6359-x.
Machiels JP, Aydin S, Bonny MA, Hammouch F, Sempoux C: What is the best to predict disease-free survival after preoperative radiochemotherapy for rectal cancer patients: tumor regression grading, nodal status or circumferential resection margin invasion?. J Clin Oncol. 2006, 24: 1319-1321. 10.1200/JCO.2005.05.0963.
Adam IJ, Mohamdee MO, Martin IG, Scott N, Finan PJ, Johnston D, Dixon MF, Quirke P: Role of circumferential margin involvement in the local recurrence of rectal cancer. Lancet. 1994, 344: 707-711. 10.1016/S0140-6736(94)92206-3.
Quirke P, Durdey P, Dixon MF, Williams NS: Local recurrence of rectal adenocarcinoma due to inadequate surgical resection: histopathological study of lateral tumor spread and surgical excision. Lancet. 1986, 2: 996-999. 10.1016/S0140-6736(86)92612-7.
Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, Tibshirani R, Botstein D, Altman RB: Missing value estimation methods for DNA microarrays. Bioinformatics. 2001, 17: 520-525. 10.1093/bioinformatics/17.6.520.
Gleason DF: Classification of prostatic carcinomas. Cancer Chemother Rep. 1966, 50: 125-128.
Scholkopf B, Tsuda K, Vert JP: Kernel Methods in Computational Biology. 2004, Cambridge, MA: MIT Press
Vapnik V: Statistical Learning Theory. 1998, New York: Wiley
Pochet N, De Smet F, Suykens J, Moor BD: Systematic benchmarking of microarray data classification: assessing the role of nonlinearity and dimensionality reduction. Bioinformatics. 2004, 20: 3185-3195. 10.1093/bioinformatics/bth383.
Lai C, Reinders MJT, van't Veer LJ, Wessels LFA: A comparison of univariate and multivariate gene selection techniques for classification of cancer datasets. Bioinformatics. 2006, 7: 235-244. 10.1186/1471-2105-7-235.
Yang YH, Xiao Y, Segal MR: Identifying differentially expressed genes from microarray experiments via statistic synthesis. Bioinformatics. 2005, 21: 1084-1093. 10.1093/bioinformatics/bti108.
Li W, Yang Y: How many genes are needed for a discriminant microarray data analysis. Methods of Microarray Data Analysis. Edited by: Lin SM, Johnson KF. 2002, Kluwer Academic, 137-150.
Hanley JA, McNeil BJ: A method of comparing the areas under receiver operating characteristics curves derived from the same cases. Radiology. 1983, 148: 839-843.
Pavlidis P, Weston J, Cai J, Grundy WN: Gene functional classification from heterogeneous data. Proceedings of the Fifth Annual International Conference on Computational Biology: April 22-25, 2001; Montreal, Quebec, Canada. 2001, New York, NY: ACM, 242-252.
Zien A, Ong CS: Multiclass multiple kernel learning. Proceedings of the 24th International Conference on Machine Learning: June 20-24, 2007; Corvalis, Oregon. 2007, New York, NY: ACM, 1191-1198.
Zhang W, Park DJ, Lu B, Yang DY, Gordon M, Groshen S, Yun J, Press OA, Vallbohmer D, Rhodes K, Lenz HJ: Epidermal growth factor receptor gene polymorphisms predict pelvic recurrence in patients with rectal cancer treated with chemoradiation. Clin Cancer Res. 2005, 11: 600-605.
Maihofner C, Charalambous MP, Bhambra U, Lightfoot T, Geisslinger G, Gooderham NJ, The Colorectal Cancer Group: Expression of cyclooxygenase-2 parallels expression of interleukin-1beta, interleukin-6 and NF-kappaB in human colorectal cancer. Carcinogenesis. 2003, 24: 665-671. 10.1093/carcin/bgg006.
Sawhney RS, Sharma B, Humphrey LE, Brattain MG: Integrin α2 and extracellular signal-regulated kinase are functionally linked in highly malignant autocrine transforming growth factor-α-driven colon cancer cells. J Biol Chem. 2003, 278: 19861-19869. 10.1074/jbc.M213162200.
Rubie C, Frick VO, Pfeil S, Wagner M, Kollmar O, Kopp B, Graber S, Rau BM, Schilling MK: Correlation of IL-8 with induction, progression and metastatic potential of colorectal cancer. World J Gastroenterol. 2007, 13: 4996-5002.
Louhimo J, Carpelan-Holmstrom M, Alfthan H, Stenman UH, Jarvinen HJ, Haglund C: Serum HCG beta, CA 72-4 and CEA are independent prognostic factors in colorectal cancer. Int J Cancer. 2002, 101: 545-548. 10.1002/ijc.90009.
Bhatia B, Maldonado CJ, Tang S, Chandra D, Klein RD, Chopra D, Shappell SB, Yang P, Newman RA, Tang DG: Subcellular localization and tumor-suppressive functions of 15-lipoxygenase 2 (15-LOX2) and its splice variants. J Biol Chem. 2003, 278: 25091-25100. 10.1074/jbc.M301920200.
Horvath LG, Lelliott JE, Kench JG, Lee CS, Williams ED, Saunders DN, Grvgiel JJ, Sutherland RL, Henshall SM: Secreted frizzled-related protein 4 inhibits proliferation and metastatic potential in prostate cancer. Prostate. 2007, 67: 1081-1090. 10.1002/pros.20607.
Schwarze SR, Luo J, Isaacs WB, Jarrard DF: Modulation of CXCL14 (BRAK) expression in prostate cancer. Prostate. 2005, 64: 67-74. 10.1002/pros.20215.
Furusato B, Gao CL, Ravindranath L, Chen Y, Cullen J, McLeod DG, Dobi A, Srivastava S, Petrovics G, Sesterhenn IA: Mapping of TMPRSS2-ERG fusions in the context of multi-focal prostate cancer. Mod Pathol. 2008, 21: 67-75. 10.1038/sj.modpathol.3801030.
Nam RK, Sugar L, Yang W, Srivastava S, Klotz LH, Yang LY, Stanimirovic A, Encioiu E, Neill M, Loblaw DA, Trachtenberg J, Narod SA, Seth A: Expression of the TMPRSS2:ERG fusion gene predicts cancer recurrence after surgery for localised prostate cancer. Br J Cancer. 2007, 97: 1690-1695. 10.1038/sj.bjc.6604054.
Dong Z, Liu Y, Lu S, Wang A, Lee K, Wang LH, Revelo M, Lu S: Vav3 oncogene is overexpressed and regulates cell growth and androgen receptor activity in human prostate cancer. Mol Endocrinol. 2006, 20: 2315-2325. 10.1210/me.2006-0048.
Engers R, Mueller M, Walter A, Collard JG, Willers R, Gabbert HE: Prognostic relevance of Tiam1 protein expression in prostate carcinomas. Br J Cancer. 2006, 95: 1081-1086. 10.1038/sj.bjc.6603385.
Santagata S, Demichelis F, Riva A, Varambally S, Hofer MD, Kutok JL, Kim R, Tang J, Montie JE, Chinnaiyan AM, Rubin MA, Aster JC: JAGGED1 expression is associated with prostate cancer metastasis and recurrence. Cancer Res. 2004, 64: 6854-6857. 10.1158/0008-5472.CAN-04-2500.
Silverman RH: Implications for RNase L in prostate cancer biology. Biochemistry. 2003, 42: 1805-1812. 10.1021/bi027147i.
Raje D, Mukhtar H, Oshowo A, Clark CI: What proportion of patients referred to secondary care with iron deficiency anemia have colon cancer?. Dis Colon Rectum. 2007, 50: 1211-1214. 10.1007/s10350-007-0249-y.
Ciardiello F, Tortora G: Epidermal growth factor receptor (EGFR) as a target in cancer therapy: understanding the role of receptor expression and other molecular determinants that could influence the response to anti-EGFR drugs. Eur J Cancer. 2003, 39: 1348-1354. 10.1016/S0959-8049(03)00235-1.
Kim TD, Song KS, Li G, Choi H, Park HD, Lim K, Hwang BD, Yoon WH: Activity and expression of urokinase-type plasminogen activator and matrix metalloproteinases in human colorectal cancer. BMC Cancer. 2006, 6: 211-10.1186/1471-2407-6-211.
Uner A, Akcali Z, Unsal D: Serum levels of soluble E-selectin in colorectal cancer. Neoplasma. 2004, 51: 269-274.
Eksioglu EA, Mahmood SS, Chang M, Reddy V: GM-CSF promotes differentiation of human dendritic cells and T lymphocytes toward a predominantly type 1 proinflammatory response. Exp Hematol. 2007, 35: 1163-1171. 10.1016/j.exphem.2007.05.001.
Zinzindohoue F, Lecomte T, Ferraz JM, Houllier AM, Cugnenc PH, Berger A, Blons H, Laurent-Puig P: Prognostic significance of MMP-1 and MMP-3 functional promoter polymorphisms in colorectal cancer. Clin Cancer Res. 2005, 11: 594-599.
Zhang Y, Lai M, Lv B, Gu X, Wang H, Zhu Y, Zhu Y, Shao L, Wang G: Overexpression of Reg IV in colorectal adenoma. Cancer Lett. 2003, 200: 69-76. 10.1016/S0304-3835(03)00460-9.
Ahn DH, Crawley SC, Hokari R, Kato S, Yang SC, Li JD, Kim YS: TNF-alpha activates MUC2 transcription via NF-kappaB but inhibits via JNK activation. Cell Physiol Biochem. 2005, 15: 29-40. 10.1159/000083636.
Kummola L, Hala J, Kivelamainen JM, Kivela AJ, Saarnio J, Karttunen T, Parkkila S: Expression of a novel carbonic anhydrase, CA XIII, in normal and neoplastic colorectal mucosa. BMC Cancer. 2005, 5: 41-10.1186/1471-2407-5-41.
Gropcke S, Mannone J, Weber B, Staub E, Heinze M, Klaman I, Pilarsky C, Hermann K, Castanos-Velez E, Ropcke S, Mann B, Rosenthal A, Buhr HJ: Differential expression of genes encoding tight junction proteins in colorectal cancer: frequent dysregulation of claudin-1, -8 and -12. Int J Colorectal Dis. 2007, 22: 651-659. 10.1007/s00384-006-0197-3.
Viet HT, Wagsater D, Hugander A, Dimberg J: Interleukin-1 receptor antagonist gene polymorphism a gs in human colorectal cancer. Oncol Rep. 2005, 14: 915-918.
Kloor M, Michel S, Buckowitz B, Ruschoff J, Buttner R, Holinski-Feder E, Dippold W, Wagner R, Tariverdian M, Benner A, Schwitalle Y, Kuchenbuch B, von Knebel Doeberitz M: Beta2-microglobulin mutations in microsatellite unstable colorectal tumors. Int J Cancer. 2007, 121: 454-458. 10.1002/ijc.22691.
Youssef EM, Chen Xq, Higuchi E, Kondo Y, Garcia-Manero G, Lotan R, Issa JPJ: Hypermethylation and silencing of the putative tumor suppressor Tazarotene-induced gene 1 in human cancers. Cancer Res. 2004, 64: 2411-2417. 10.1158/0008-5472.CAN-03-0164.
Muc-Wierzgon M, Nowakowska-Zajdel E, Kokot T, Kozowicz A, Zubelewicz B, Klakla K, Mazurek U, Cholewa K, Wilczok T, Wierzgon J, Sosada K: Genetic disregulation of gene coding tumor necrosis factor alpha receptors (TNFalpha Rs) in colorectal cancer cells. J Exp Clin Cancer Res. 2004, 23: 651-660.
Maeda K, Kang SM, Sawada T, Nishiguchi Y, Yashiro M, Ogawa Y, Ohira M, Ishikawa T, Hirakawa YS, Chung K: Expression of intercellular adhesion molecule-1 and prognosis in colorectal cancer. Oncol Rep. 2002, 9: 511-514.
Ferroni P, Palmirotta R, Spila A, Martini F, Raparelli V, Fossile E, Mariotti S, Del Monte G, Buonomo O, Roselli M, Guadagni F: Prognostic significance of adiponectin levels in non-metastatic colorectal cancer. Anticancer Res. 2007, 27: 483-489.
Miyanaga K, Kato Y, Nakamura T, Matsumura M, Amaya H, Horiuchi T, Chiba Y, Tanaka K: Expression and role of thrombospondin-1 in colorectal cancer. Anticancer Res. 2002, 22: 3941-3948.
Wan Y, Wu N, Wang Z, Ju X, Zhu J, Liu Y, Tang J, Huang Y: Relationship between tissue factor expression and hepatic metastasis and prognosis in rectal cancer. Zhonghua Zhong Liu Za Zhi. 2002, 24: 378-380.
Bethke L, Webb E, Sellick G, Rudd M, Penegar S, Withey L, Qureshi M, Houlston R: Polymorphisms in the cytochrome P450 genes CYP1A2, CYP1B1, CYP3A4, CYP3A5, CYP11A1, CYP17A1, CYP19A1 and colorectal cancer risk. BMC Cancer. 2007, 7: 123-10.1186/1471-2407-7-123.
Cross NA, Chandrasekharan S, Jokonya N, Fowles A, Hamdy FC, Buttle DJ, Eaton CL: The expression and regulation of ADAMTS-1, -4, -5, -9, and -15, and TIMP-3 by TGFbeta1 in prostate cells: relevance to the accumulation of versican. Prostate. 2005, 63: 269-275. 10.1002/pros.20182.
Hudolin T, Juretic A, Spagnoli GC, Pasini J, Bandic D, Heberer M, Kosicek M, Cacic M: Immunohistochemical expression of tumor antigens MAGE-A1, MAGE-A3/4, and NY-ESO-1 in cancerous and benign prostatic tissue. Prostate. 2006, 66: 13-18. 10.1002/pros.20312.
Ishii K, Usui S, Sugimura Y, Yoshida S, Hioki T, Tatematsu M, Yamamoto H, Hirano K: Aminopeptidase N regulated by zinc in human prostate participates in tumor cell invasion. Int J Cancer. 2001, 92: 49-54. 10.1002/1097-0215(200102)9999:9999<::AID-IJC1161>3.0.CO;2-S.
Diss JK, Faulkes DJ, Walker MM, Patel A, Foster CS, Budhram-Mahadeo V, Djamgoz MB, Latchman DS: Brn-3a neuronal transcription factor functional expression in human prostate cancer. Prostate Cancer Prostatic Dis. 2006, 9: 83-91. 10.1038/sj.pcan.4500837.
Cross DS, Burmester JK: Functional characterization of the GDEP promoter and three enhancer elements in retinoblastoma and prostate cell lines. Med Oncol. 2008, 25: 40-49. 10.1007/s12032-007-0038-4.
Wolfgang CD, Essand M, Lee B, Pastan I: T-cell receptor gamma chain alternate reading frame protein (TARP) expression in prostate cancer cells leads to an increased growth rate and induction of caveolins and amphiregulin. Cancer Res. 2001, 61: 8122-8126.
Descazeaud A, de la Taille A, Allory Y, Faucon H, Salomon L, Bismar T, Kim R, Hofer MD, Chopin D, Abbou CC, Rubin MA: Characterization of ZAG protein expression in prostate cancer using a semi-automated microscope system. Prostate. 2006, 66: 1037-1043. 10.1002/pros.20405.
Sahni A, Simpson-Haidaris PJ, Sahni SK, Vaday GG, Francis CW: Fibrinogen synthesized by cancer cells augments the proliferative effect of fibroblast growth factor-2 (FGF-2). J Thromb Haemost. 2008, 6: 176-183.
Bandyopadhyay S, Wang Y, Zhan R, Pai SK, Watabe M, Iiizumi M, Furuta E, Mohinta S, Liu W, Hirota S, Hosobe S, Tsukada T, Miura K, Takano Y, Saito K, Commes T, Piquemal D, Hai T, Watabe K: The tumor metastasis suppressor gene Drg-1 down-regulates the expression of activating transcription factor 3 in prostate cancer. Cancer Res. 2006, 66: 11983-11990. 10.1158/0008-5472.CAN-06-0943.