A multi-gene signature predicts outcome in patients with pancreatic ductal adenocarcinoma

Genome Medicine

Volumn 6, Issue 12, 2014, Pages

  Haider, Syed ^a   Wang, Jun ^a   Nagano, Ai ^a   Desai, Ami ^a   Arumugam, Prabhu ^a   Dumartin, Laurent ^a   Fitzgibbon, Jude ^a   Hagemann, Thorsten ^a   Marshall, John F ^a   Kocher, Hemant M ^a   Crnogorac Jurcevic, Tatjana ^a   Scarpa, Aldo ^b   Lemoine, Nicholas R ^a   Chelala, Claude ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b University and Hospital Trust of Verona   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ARTICLE; CANCER GENETICS; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; COMPUTER MODEL; DIAGNOSTIC TEST ACCURACY STUDY; GENE EXPRESSION; GENETIC TRAIT; HUMAN; INFORMATION RETRIEVAL; MAJOR CLINICAL STUDY; MULTIGENE FAMILY; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROGNOSTIC ASSESSMENT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 84927916016     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/s13073-014-0105-3     Document Type: Article

References (50)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010, 60:277-300. 10.3322/caac.20073, 20610543.
2. Hidalgo M. Pancreatic cancer. N Engl J Med 2010, 362:1605-1617. 10.1056/NEJMra0901557, 20427809.
3. Stratford JK, Bentrem DJ, Anderson JM, Fan C, Volmar KA, Marron JS, Routh ED, Caskey LS, Samuel JC, Der CJ, Thorne LB, Calvo BF, Kim HJ, Talamonti MS, Iacobuzio-Donahue CA, Hollingsworth MA, Perou CM, Yeh JJ. A six-gene signature predicts survival of patients with localized pancreatic ductal adenocarcinoma. PLoS Med 2010, 7:e1000307. 10.1371/journal.pmed.1000307, 20644708.
4. Stathis A, Moore MJ. Advanced pancreatic carcinoma: current treatment and future challenges. Nat Rev Clin Oncol 2010, 7:163-172. 10.1038/nrclinonc.2009.236, 20101258.
5. Plentz RR, Manns MP, Greten TF. Molecular therapy of pancreatic cancer. Minerva Endocrinol 2010, 35:27-33. 20386525.
6. Biankin AV, Waddell N, Kassahn KS, Gingras MC, Muthuswamy LB, Johns AL, Miller DK, Wilson PJ, Patch AM, Wu J, Chang DK, Cowley MJ, Gardiner BB, Song S, Harliwong I, Idrisoglu S, Nourse C, Nourbakhsh E, Manning S, Wani S, Gongora M, Pajic M, Scarlett CJ, Gill AJ, Pinho AV, Rooman I, Anderson M, Holmes O, Leonard C, Taylor D, et al. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 2012, 491:399-405. 10.1038/nature11547, 23103869.
7. Coupland VH, Kocher HM, Berry DP, Allum W, Linklater KM, Konfortion J, Moller H, Davies EA. Incidence and survival for hepatic, pancreatic and biliary cancers in England between 1998 and 2007. Cancer Epidemiol 2012, 36:e207-e214. 10.1016/j.canep.2012.03.010, 22534487.
8. Al-Hawary MM, Francis IR, Chari ST, Fishman EK, Hough DM, Lu DS, Macari M, Megibow AJ, Miller FH, Mortele KJ, Merchant NB, Minter RM, Tamm EP, Sahani DV, Simeone DM. Pancreatic ductal adenocarcinoma radiology reporting template: consensus statement of the society of abdominal radiology and the American pancreatic association. Gastroenterology 2014, 146:291-304. e291, 10.1053/j.gastro.2013.11.004, 24355035.
9. Tempero MA, Arnoletti JP, Behrman SW, Ben-Josef E, Benson AB, Casper ES, Cohen SJ, Czito B, Ellenhorn JD, Hawkins WG, Herman J, Hoffman JP, Ko A, Komanduri S, Koong A, Ma WW, Malafa MP, Merchant NB, Mulvihill SJ, Muscarella P, Nakakura EK, Obando J, Pitman MB, Sasson AR, Tally A, Thayer SP, Whiting S, Wolff RA, Wolpin BM, Freedman-Cass DA, et al. Pancreatic adenocarcinoma, version 2.2012: featured updates to the NCCN Guidelines. J Natl Compr Canc Netw 2012, 10:703-713. 22679115.
10. Kocher HM, Alrawashdeh W: Pancreatic cancer. Clin Evid 2010, ISSN: 05:409..
11. Campbell PJ, Yachida S, Mudie LJ, Stephens PJ, Pleasance ED, Stebbings LA, Morsberger LA, Latimer C, McLaren S, Lin ML, McBride DJ, Varela I, Nik-Zainal SA, Leroy C, Jia M, Menzies A, Butler AP, Teague JW, Griffin CA, Burton J, Swerdlow H, Quail MA, Stratton MR, Iacobuzio-Donahue C, Futreal PA. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010, 467:1109-1113. 10.1038/nature09460, 20981101.
12. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, Hong SM, Fu B, Lin MT, Calhoun ES, Kamiyama M, Walter K, Nikolskaya T, Nikolsky Y, Hartigan J, Smith DR, Hidalgo M, Leach SD, Klein AP, Jaffee EM, Goggins M, Maitra A, Iacobuzio-Donahue C, Eshleman JR, Kern SE, Hruban RH, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321:1801-1806. 10.1126/science.1164368, 18772397.
13. Collisson EA, Sadanandam A, Olson P, Gibb WJ, Truitt M, Gu S, Cooc J, Weinkle J, Kim GE, Jakkula L, Feiler HS, Ko AH, Olshen AB, Danenberg KL, Tempero MA, Spellman PT, Hanahan D, Gray JW. Subtypes of pancreatic ductal adenocarcinoma and their differing responses to therapy. Nat Med 2011, 17:500-503. 10.1038/nm.2344, 21460848.
14. Donahue TR, Tran LM, Hill R, Li Y, Kovochich A, Hargan Calvopina J, Patel SG, Wu N, Hindoyan A, Farrell JJ, Li X, Dawson DW, Wu H. Integrative survival-based molecular profiling of human pancreatic cancer. Clin Cancer Res 2012, 18:1352-1363. 10.1158/1078-0432.CCR-11-1539, 22261810.
15. Grutzmann R, Pilarsky C, Ammerpohl O, Luttges J, Bohme A, Sipos B, Foerder M, Alldinger I, Jahnke B, Schackert HK, Kalthoff H, Kremer B, Kloppel G, Saeger HD. Gene expression profiling of microdissected pancreatic ductal carcinomas using high-density DNA microarrays. Neoplasia 2004, 6:611-622. 10.1593/neo.04295, 15548371.
16. Winter C, Kristiansen G, Kersting S, Roy J, Aust D, Knosel T, Rummele P, Jahnke B, Hentrich V, Ruckert F, Niedergethmann M, Weichert W, Bahra M, Schlitt HJ, Settmacher U, Friess H, Buchler M, Saeger HD, Schroeder M, Pilarsky C, Grutzmann R. Google goes cancer: improving outcome prediction for cancer patients by network-based ranking of marker genes. PLoS Comput Biol 2012, 8:e1002511. 10.1371/journal.pcbi.1002511, 22615549.
17. Zhang G, Schetter A, He P, Funamizu N, Gaedcke J, Ghadimi BM, Ried T, Hassan R, Yfantis HG, Lee DH, Lacy C, Maitra A, Hanna N, Alexander HR, Hussain SP. DPEP1 inhibits tumor cell invasiveness, enhances chemosensitivity and predicts clinical outcome in pancreatic ductal adenocarcinoma. PLoS One 2012, 7:e31507. 10.1371/journal.pone.0031507, 22363658.
18. Yoshihara K, Tsunoda T, Shigemizu D, Fujiwara H, Hatae M, Masuzaki H, Katabuchi H, Kawakami Y, Okamoto A, Nogawa T, Matsumura N, Udagawa Y, Saito T, Itamochi H, Takano M, Miyagi E, Sudo T, Ushijima K, Iwase H, Seki H, Terao Y, Enomoto T, Mikami M, Akazawa K, Tsuda H, Moriya T, Tajima A, Inoue I, Tanaka K. High-risk ovarian cancer based on 126-gene expression signature is uniquely characterized by downregulation of antigen presentation pathway. Clin Cancer Res 2012, 18:1374-1385. 10.1158/1078-0432.CCR-11-2725, 22241791.
19. Buffa FM, Harris AL, West CM, Miller CJ. Large meta-analysis of multiple cancers reveals a common, compact and highly prognostic hypoxia metagene. Br J Cancer 2010, 102:428-435. 10.1038/sj.bjc.6605450, 20087356.
20. Boutros PC, Lau SK, Pintilie M, Liu N, Shepherd FA, Der SD, Tsao MS, Penn LZ, Jurisica I. Prognostic gene signatures for non-small-cell lung cancer. Proc Natl Acad Sci USA 2009, 106:2824-2828. 10.1073/pnas.0809444106, 19196983.
21. Zhu CQ, Ding K, Strumpf D, Weir BA, Meyerson M, Pennell N, Thomas RK, Naoki K, Ladd-Acosta C, Liu N, Pintilie M, Der S, Seymour L, Jurisica I, Shepherd FA, Tsao MS. Prognostic and predictive gene signature for adjuvant chemotherapy in resected non-small-cell lung cancer. J Clin Oncol 2010, 28:4417-4424. 10.1200/JCO.2009.26.4325, 20823422.
22. Grutzmann R, Boriss H, Ammerpohl O, Luttges J, Kalthoff H, Schackert HK, Kloppel G, Saeger HD, Pilarsky C. Meta-analysis of microarray data on pancreatic cancer defines a set of commonly dysregulated genes. Oncogene 2005, 24:5079-5088. 10.1038/sj.onc.1208696, 15897887.
23. Datasets in the Pancreatic Expression Database. [www.pancreasexpression.org/cgi-bin/pancexp/DataSets.pl].
24. Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Holko M, Yefanov A, Lee H, Zhang N, Robertson CL, Serova N, Davis S, Soboleva A. NCBI GEO: archive for functional genomics data sets - update. Nucleic Acids Res 2013, 41:D991-D995. 10.1093/nar/gks1193, 23193258.
25. Badea L, Herlea V, Dima SO, Dumitrascu T, Popescu I. Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia. Hepatogastroenterology 2008, 55:2016-2027. 19260470.
26. Pei H, Li L, Fridley BL, Jenkins GD, Kalari KR, Lingle W, Petersen G, Lou Z, Wang L. FKBP51 affects cancer cell response to chemotherapy by negatively regulating Akt. Cancer Cell 2009, 16:259-266. 10.1016/j.ccr.2009.07.016, 19732725.
27. Huang H, Lu X, Liu Y, Haaland P, Marron JS. R/DWD: distance-weighted discrimination for classification, visualization and batch adjustment. Bioinformatics 2012, 28:1182-1183. 10.1093/bioinformatics/bts096, 22368246.
28. Wasif N, Ko CY, Farrell J, Wainberg Z, Hines OJ, Reber H, Tomlinson JS. Impact of tumor grade on prognosis in pancreatic cancer: should we include grade in AJCC staging?. Ann Surg Oncol 2010, 17:2312-2320. 10.1245/s10434-010-1071-7, 20422460.
29. Brennan MF, Kattan MW, Klimstra D, Conlon K. Prognostic nomogram for patients undergoing resection for adenocarcinoma of the pancreas. Ann Surg 2004, 240:293-298. 10.1097/01.sla.0000133125.85489.07, 15273554.
30. Mosley JD, Keri RA. Intrinsic bias in breast cancer gene expression data sets. BMC Cancer 2009, 9:214. 10.1186/1471-2407-9-214, 19563679.
31. Cancer Genome Atlas N: Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70..
32. Network CGA. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012, 487:330-337. 10.1038/nature11252.
33. Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615. 10.1038/nature10166.
34. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, Speed D, Lynch AG, Samarajiwa S, Yuan Y, Graf S, Ha G, Haffari G, Bashashati A, Russell R, McKinney S, Langerod A, Green A, Provenzano E, Wishart G, Pinder S, Watson P, Markowetz F, Murphy L, Ellis I, Purushotham A, Borresen-Dale AL, Brenton JD, Tavare S, Caldas C, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486:346-352. 22522925.
35. Wong HH, Lemoine NR. Pancreatic cancer: molecular pathogenesis and new therapeutic targets. Nat Rev Gastroenterol Hepatol 2009, 6:412-422. 10.1038/nrgastro.2009.89, 19506583.
36. Febbo PG, Kantoff PW. Noise and bias in microarray analysis of tumor specimens. J Clin Oncol 2006, 24:3719-3721. 10.1200/JCO.2006.06.7942, 16822841.
37. Muller MW, Giese NA, Swiercz JM, Ceyhan GO, Esposito I, Hinz U, Buchler P, Giese T, Buchler MW, Offermanns S, Friess H. Association of axon guidance factor semaphorin 3A with poor outcome in pancreatic cancer. Int J Cancer 2007, 121:2421-2433. 10.1002/ijc.22949, 17631638.
38. Li NF, Gemenetzidis E, Marshall FJ, Davies D, Yu Y, Frese K, Froeling FE, Woolf AK, Feakins RM, Naito Y, Iacobuzio-Donahue C, Tuveson DA, Hart IR, Kocher HM. RhoC interacts with integrin α5β1 and enhances its trafficking in migrating pancreatic carcinoma cells. PLoS One 2013, 8:e81575. 10.1371/journal.pone.0081575, 24312560.
39. Taniwaki M, Takano A, Ishikawa N, Yasui W, Inai K, Nishimura H, Tsuchiya E, Kohno N, Nakamura Y, Daigo Y. Activation of KIF4A as a prognostic biomarker and therapeutic target for lung cancer. Clin Cancer Res 2007, 13:6624-6631. 10.1158/1078-0432.CCR-07-1328, 18006763.
40. Tercero JA, Labib K, Diffley JF. DNA synthesis at individual replication forks requires the essential initiation factor Cdc45p. EMBO J 2000, 19:2082-2093. 10.1093/emboj/19.9.2082, 10790374.
41. Srinivasan SV, Dominguez-Sola D, Wang LC, Hyrien O, Gautier J. Cdc45 is a critical effector of myc-dependent DNA replication stress. Cell Rep 2013, 3:1629-1639. 10.1016/j.celrep.2013.04.002, 23643534.
42. Kovacevic I, Hu J, Siehoff-Icking A, Opitz N, Griffin A, Perkins AC, Munn AL, Muller-Esterl W, Popp R, Fleming I, Jungblut B, Hoffmeister M, Oess S. The F-BAR protein NOSTRIN participates in FGF signal transduction and vascular development. EMBO J 2012, 31:3309-3322. 10.1038/emboj.2012.176, 22751148.
43. Coleman SJ, Chioni AM, Ghallab M, Anderson RK, Lemoine NR, Kocher HM, Grose RP. Nuclear translocation of FGFR1 and FGF2 in pancreatic stellate cells facilitates pancreatic cancer cell invasion. EMBO Mol Med 2014, 6:467-481. 10.1002/emmm.201302698, 24503018.
44. Perez-Mancera PA, Tuveson DA. Physiological analysis of oncogenic K-ras. Methods Enzymol 2006, 407:676-690. 10.1016/S0076-6879(05)07053-9, 16757361.
45. Janouskova H, Maglott A, Leger DY, Bossert C, Noulet F, Guerin E, Guenot D, Pinel S, Chastagner P, Plenat F, Entz-Werle N, Lehmann-Che J, Godet J, Martin S, Teisinger J, Dontenwill M. Integrin α5β1 plays a critical role in resistance to temozolomide by interfering with the p53 pathway in high-grade glioma. Cancer Res 2012, 72:3463-3470. 10.1158/0008-5472.CAN-11-4199, 22593187.
46. Maione F, Capano S, Regano D, Zentilin L, Giacca M, Casanovas O, Bussolino F, Serini G, Giraudo E. Semaphorin 3A overcomes cancer hypoxia and metastatic dissemination induced by antiangiogenic treatment in mice. J Clin Invest 2012, 122:1832-1848. 10.1172/JCI58976, 22484816.
47. Cox D, Brennan M, Moran N. Integrins as therapeutic targets: lessons and opportunities. Nat Rev Drug Discov 2010, 9:804-820. 10.1038/nrd3266, 20885411.
48. Anderson NL, Polanski M, Pieper R, Gatlin T, Tirumalai RS, Conrads TP, Veenstra TD, Adkins JN, Pounds JG, Fagan R, Lobley A. The human plasma proteome: a nonredundant list developed by combination of four separate sources. Mol Cell Proteomics 2004, 3:311-326. 10.1074/mcp.M300127-MCP200, 14718574.
49. Adachi J, Kumar C, Zhang Y, Olsen JV, Mann M. The human urinary proteome contains more than 1500 proteins, including a large proportion of membrane proteins. Genome Biol 2006, 7:R80. 10.1186/gb-2006-7-9-r80, 16948836.
50. The Cancer Genome Atlas. [http://cancergenome.nih.gov/].