Roles for KRAS in pancreatic tumor development and progression

Gastroenterology

Volumn 144, Issue 6, 2013, Pages 1220-1229

  Di Magliano, Marina Pasca ^a,b   Logsdon, Craig D ^c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

Inflammation; Kras; Mouse Model; Pancreatic Cancer

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; INTERLEUKIN 6; K RAS PROTEIN; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; PICTILISIB; PROSTAGLANDIN E RECEPTOR 4; SELUMETINIB; SONIC HEDGEHOG PROTEIN; STAT3 PROTEIN;

ACUTE PANCREATITIS; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER GENETICS; CANCER GROWTH; CARCINOGENESIS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; ENVIRONMENTAL FACTOR; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; LIVER CELL CARCINOMA; LUNG ADENOCARCINOMA; MELANOMA; METASTASIS; NEOPLASM; NONHUMAN; ONCOGENE K RAS; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TUMOR MICROENVIRONMENT; TUMOR SUPPRESSOR GENE;

EID: 84876802642     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2013.01.071     Document Type: Article

References (82)

1. V.T. Smit, A.J. Boot, A.M. Smits KRAS codon 12 mutations occur very frequently in pancreatic adenocarcinomas Nucleic Acids Res 16 1988 7773 7782
2. C. Almoguera, D. Shibata, K. Forrester Most human carcinomas of the exocrine pancreas contain mutant c-K-ras genes Cell 53 1988 549 554
3. M. Spaargaren, J.R. Bischoff, F. McCormick Signal transduction by Ras-like GTPases: a potential target for anticancer drugs Gene Expr 4 1995 345 356
4. K. Scheffzek, M.R. Ahmadian, W. Kabsch The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants Science 277 1997 333 338
5. A. Fernandez-Medarde, E. Santos Ras in cancer and developmental diseases Genes Cancer 2 2011 344 358
6. A.V. Biankin, N. Waddell, K.S. Kassahn Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes Nature 491 2012 399 405
7. S. Jones, X. Zhang, Parsons Core signaling pathways in human pancreatic cancers revealed by global genomic analyses Science 321 2008 1801 1806
8. H.P. Koeffler, F. McCormick, C. Denny Molecular mechanisms of cancer West J Med 155 1991 505 514
9. Y. Pylayeva-Gupta, E. Grabocka, D. Bar-Sagi RAS oncogenes: weaving a tumorigenic web Nat Rev Cancer 11 2011 761 774
10. A.E. Karnoub, R.A. Weinberg Ras oncogenes: split personalities Nat Rev Mol Cell Biol 9 2008 517 531
11. P.M. Campbell, A. Singh, F.J. Williams Genetic and pharmacologic dissection of Ras effector utilization in oncogenesis Methods Enzymol 407 2006 195 217
12. S.L. Campbell, R. Khosravi-Far, K.L. Rossman Increasing complexity of Ras signaling Oncogene 17 1998 1395 1413
13. J. Daniluk, Y. Liu, D. Deng An NF-κB pathway-mediated positive feedback loop amplifies Ras activity to pathological levels in mice J Clin Invest 122 2012 1519 1528
14. J.D. Haojie Huang, Yan Liu, Jun Chu Oncogenic K-Ras requires activation for enhanced activity Oncogene 2013 Jan 21 [Epub ahead of print]
15. L. Yan, C. McFaul, N. Howes Molecular analysis to detect pancreatic ductal adenocarcinoma in high-risk groups Gastroenterology 128 2005 2124 2130
16. X. Lu, T. Xu, J. Qian Detecting K-ras and p53 gene mutation from stool and pancreatic juice for diagnosis of early pancreatic cancer Chin Med J (Engl) 115 2002 1632 1636
17. B.L. Parsons, F. Meng K-RAS mutation in the screening, prognosis and treatment of cancer Biomark Med 3 2009 757 769
18. M.S. Yakubovskaya, V. Spiegelman, F.C. Luo High frequency of K-ras mutations in normal appearing lung tissues and sputum of patients with lung cancer Int J Cancer 63 1995 810 814
19. D.A. Tuveson, A.T. Shaw, N.A. Willis Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects Cancer Cell 5 2004 375 387
20. C. Guerra, N. Mijimolle, A. Dhawahir Tumor induction by an endogenous K-ras oncogene is highly dependent on cellular context Cancer Cell 4 2003 111 120
21. C. Carriere, A.L. Young, J.R. Gunn Acute pancreatitis markedly accelerates pancreatic cancer progression in mice expressing oncogenic Kras Biochem Biophys Res Commun 382 2009 561 565
22. C.M. Ardito, B.M. Gruner, K.K. Takeuchi EGF receptor is required for KRAS-induced pancreatic tumorigenesis Cancer Cell 22 2012 304 317
23. C. Navas, I. Hernandez-Porras, A.J. Schuhmacher EGF receptor signaling is essential for k-ras oncogene-driven pancreatic ductal adenocarcinoma Cancer Cell 22 2012 318 330
24. V.A. Appleman, L.G. Ahronian, J. Cai KRAS(G12D)- and BRAF(V600E)-induced transformation of murine pancreatic epithelial cells requires MEK/ERK-stimulated IGF1R signaling Mol Cancer Res 10 2012 1228 1239
25. C. Guerra, M. Collado, C. Navas Pancreatitis-induced inflammation contributes to pancreatic cancer by inhibiting oncogene-induced senescence Cancer Cell 19 2011 728 739
26. G.M. DeNicola, D.A. Tuveson RAS in cellular transformation and senescence Eur J Cancer 45 Suppl 1 2009 211 216
27. N. Bardeesy, A.J. Aguirre, G.C. Chu Both p16(Ink4a) and the p19(Arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse Proc Natl Acad Sci U S A 103 2006 5947 5952
28. K.E. Lee, D. Bar-Sagi Oncogenic KRas suppresses inflammation-associated senescence of pancreatic ductal cells Cancer Cell 18 2010 448 458
29. A.J. Aguirre, N. Bardeesy, M. Sinha Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma Genes Dev 17 2003 3112 3126
30. S.R. Hingorani, L. Wang, A.S. Multani Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice Cancer Cell 7 2005 469 483
31. C. Guerra, A.J. Schuhmacher, M. Canamero Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice Cancer Cell 11 2007 291 302
32. M. Kanda, H. Matthaei, J. Wu Presence of somatic mutations in most early-stage pancreatic intraepithelial neoplasia Gastroenterology 142 2012 730 733.e9
33. S.M. Hong, A. Vincent, M. Kanda Genome-wide somatic copy number alterations in low-grade PanINs and IPMNs from individuals with a family history of pancreatic cancer Clin Cancer Res 18 2012 4303 4312
34. S.R. Hingorani, E.F. Petricoin, A. Maitra Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse Cancer Cell 4 2003 437 450
35. K. Podsypanina, K. Politi, L.J. Beverly Oncogene cooperation in tumor maintenance and tumor recurrence in mouse mammary tumors induced by Myc and mutant Kras Proc Natl Acad Sci U S A 105 2008 5242 5247
36. G.H. Fisher, S.L. Wellen, D. Klimstra Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes Genes Dev 15 2001 3249 3262
37. L. Chin, A. Tam, J. Pomerantz Essential role for oncogenic Ras in tumour maintenance Nature 400 1999 468 472
38. M.A. Collins, F. Bednar, Y. Zhang Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice J Clin Invest 122 2012 639 653
39. H. Ying, A.C. Kimmelman, C.A. Lyssiotis Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism Cell 149 2012 656 670
40. J.P. Morris 4th, D.A. Cano, S. Sekine Beta-catenin blocks Kras-dependent reprogramming of acini into pancreatic cancer precursor lesions in mice J Clin Invest 120 2010 508 520
41. S. Yachida, S. Jones, I. Bozic Distant metastasis occurs late during the genetic evolution of pancreatic cancer Nature 467 2010 1114 1147
42. B. Ji, L. Tsou, H. Wang Ras activity levels control the development of pancreatic diseases Gastroenterology 137 2009 1072 1082
43. M.A. Collins, J.C. Brisset, Y. Zhang Metastatic pancreatic cancer is dependent on oncogenic Kras in mice PLoS One 7 2012 e49707
44. C.E. Clark, S.R. Hingorani, R. Mick Dynamics of the immune reaction to pancreatic cancer from inception to invasion Cancer Res 67 2007 9518 9527
45. J.H. Won, Y. Zhang, B. Ji Phenotypic changes in mouse pancreatic stellate cell Ca2+ signaling events following activation in culture and in a disease model of pancreatitis Mol Biol Cell 22 2011 421 436
46. Z. Xu, A. Vonlaufen, P.A. Phillips Role of pancreatic stellate cells in pancreatic cancer metastasis Am J Pathol 177 2010 2585 2596
47. M. Erkan, G. Adler, M.V. Apte StellaTUM: current consensus and discussion on pancreatic stellate cell research Gut 61 2012 172 178
48. M.A. Jacobetz, D.S. Chan, A. Neesse Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer Gut 62 2013 112 120
49. P.P. Provenzano, C. Cuevas, A.E. Chang Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma Cancer Cell 21 2012 418 429
50. C. Charo, R.F. Hwang, T. Arumugam PGE2 activation of the EP4 receptor regulates stellate cell activity in the pancreatic stromal microenvironment Pancreas 42 2013 467 474
51. S.P. Thayer, M.P. di Magliano, P.W. Heiser Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis Nature 425 2003 851 856
52. D.M. Berman, S.S. Karhadkar, A. Maitra Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours Nature 425 2003 846 851
53. R.L. Yauch, S.E. Gould, S.J. Scales A paracrine requirement for hedgehog signalling in cancer Nature 455 2008 406 410
54. K.P. Olive, M.A. Jacobetz, C.J. Davidson Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer Science 324 2009 1457 1461
55. M. Lesina, M.U. Kurkowski, K. Ludes Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer Cancer Cell 19 2011 456 469
56. D.Z. Chang, Y. Ma, B. Ji Mast cells in tumor microenvironment promotes the in vivo growth of pancreatic ductal adenocarcinoma Clin Cancer Res 17 2011 7015 7023
57. Y. Pylayeva-Gupta, K.E. Lee, C.H. Hajdu Oncogenic Kras-induced GM-CSF production promotes the development of pancreatic neoplasia Cancer Cell 21 2012 836 847
58. L.J. Bayne, G.L. Beatty, N. Jhala Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer Cancer Cell 21 2012 822 835
59. M. Hidalgo, A. Maitra The hedgehog pathway and pancreatic cancer N Engl J Med 361 2009 2094 2096
60. N.V. Chaika, T. Gebregiworgis, M.E. Lewallen MUC1 mucin stabilizes and activates hypoxia-inducible factor 1 alpha to regulate metabolism in pancreatic cancer Proc Natl Acad Sci U S A 109 2012 13787 13792
61. D. Hanahan, R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
62. G.L. Semenza HIF-1: upstream and downstream of cancer metabolism Curr Opin Genet Dev 20 2010 51 56
63. J.R. Cantor, D.M. Sabatini Cancer cell metabolism: one hallmark, many faces Cancer Discov 2 2012 881 898
64. A. Neesse, P. Michl, K.K. Frese Stromal biology and therapy in pancreatic cancer Gut 60 2011 861 868
65. A. Singh, P. Greninger, D. Rhodes A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival Cancer Cell 15 2009 489 500
66. I. Hofmann, A. Weiss, G. Elain K-RAS mutant pancreatic tumors show higher sensitivity to MEK than to PI3K inhibition in vivo PLoS One 7 2012 e44146
67. E.A. Collisson, C.L. Trejo, J.M. Silva A central role for RAF→MEK→ERK signaling in the genesis of pancreatic ductal adenocarcinoma Cancer Discov 2 2012 685 693
68. A.D. Cox, C.J. Der Ras family signaling: therapeutic targeting Cancer Biol Ther 1 2002 599 606
69. T. Maurer, L.S. Garrenton, A. Oh Small-molecule ligands bind to a distinct pocket in Ras and inhibit SOS-mediated nucleotide exchange activity Proc Natl Acad Sci U S A 109 2012 5299 5304
70. A. Patgiri, K.K. Yadav, P.S. Arora An orthosteric inhibitor of the Ras-Sos interaction Nat Chem Biol 7 2011 585 587
71. J.S. Macdonald, S. McCoy, R.P. Whitehead A phase II study of farnesyl transferase inhibitor R115777 in pancreatic cancer: a Southwest oncology group (SWOG 9924) study Invest New Drugs 23 2005 485 487
72. L. Elghazi, A.J. Weiss, D.J. Barker Regulation of pancreas plasticity and malignant transformation by Akt signaling Gastroenterology 136 2009 1091 1103
73. S. Eser, N. Reiff, M. Messer Selective requirement of PI3K/PDK1 signaling for Kras oncogene-driven pancreatic cell plasticity and cancer Cancer Cell 2013 Feb 27 Epub ahead of print
74. D. Vigil, J. Cherfils, K.L. Rossman Ras superfamily GEFs and GAPs: validated and tractable targets for cancer therapy? Nat Rev Cancer 10 2010 842 857
75. N.F. Neel, T.D. Martin, J.K. Stratford The RalGEF-Ral effector signaling network: the road less traveled for anti-Ras drug discovery Genes Cancer 2 2011 275 287
76. K.H. Lim, K. O'Hayer, S.J. Adam Divergent roles for RalA and RalB in malignant growth of human pancreatic carcinoma cells Curr Biol 16 2006 2385 2394
77. G. Feldmann, A. Mishra, S.M. Hong Inhibiting the cyclin-dependent kinase CDK5 blocks pancreatic cancer formation and progression through the suppression of Ras-Ral signaling Cancer Res 70 2010 4460 4469
78. S. Etienne-Manneville, A. Hall Rho GTPases in cell biology Nature 420 2002 629 635
79. I. Heid, C. Lubeseder-Martellato, B. Sipos Early requirement of Rac1 in a mouse model of pancreatic cancer Gastroenterology 141 2011 719 730
80. A. Fukuda, S.C. Wang, J.P. Morris 4th Stat3 and MMP7 contribute to pancreatic ductal adenocarcinoma initiation and progression Cancer Cell 19 2011 441 455
81. H. Ebi, R.B. Corcoran, A. Singh Receptor tyrosine kinases exert dominant control over PI3K signaling in human KRAS mutant colorectal cancers J Clin Invest 121 2011 4311 4321
82. J.A. Engelman, L. Chen, X. Tan Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers Nat Med 14 2008 1351 1356