Canonical Wnt signaling is required for pancreatic carcinogenesis

Cancer Research

Volumn 73, Issue 15, 2013, Pages 4909-4922

  Zhang, Yaqing ^a   Morris IV, John P ^b   Yan, Wei ^a   Schofield, Heather K ^a   Gurney, Austin ^c   Simeone, Diane M ^a   Millar, Sarah E ^d   Hoey, Timothy ^c   Hebrok, Matthias ^b   Di Magliano, Marina Pasca ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OncoMed Pharmaceuticals   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DICKKOPF 1 PROTEIN; VANTICTUMAB; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CONTROLLED STUDY; DRUG TARGETING; HUMAN; HUMAN CELL; METAPLASIA; MOUSE; NONHUMAN; NULL CELL; PANCREAS ADENOMA; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BETA CATENIN; BLOTTING, WESTERN; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MICE; PANCREATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; WNT SIGNALING PATHWAY;

EID: 84881473798     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-4384     Document Type: Article

References (62)

1. Katz MH, Wang H, Fleming JB, Sun CC, Hwang RF, Wolff RA, et al. Long-term survival after multidisciplinary management of resected pancreatic adenocarcinoma. Ann Surg Oncol 2009;16: 836-47.
2. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer 2011;11:761-74.
3. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008;321:1801-6.
4. Morris JP, Wang SC, Hebrok M. KRAS, Hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma. Nat Rev Cancer 2010;10:683-95.
5. Angers S, Moon RT. Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 2009;10:468-77.
6. Gordon MD, Nusse R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 2006;281: 22429-33.
7. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003;4:437-50.
8. Olive KP, Tuveson DA. The use of targeted mouse models for preclinical testing of novel cancer therapeutics. Clin Cancer Res 2006;12: 5277-87.
9. Pasca di Magliano M, Biankin AV, Heiser PW, Cano DA, Gutierrez PJ, Deramaudt T, et al. Common activation of canonical Wnt signaling in pancreatic adenocarcinoma. PLoS ONE 2007;2:e1155.
10. Morris JP, Cano DA, Sekine S, Wang SC, Hebrok M. Beta-catenin blocks Kras-dependent reprogramming of acini into pancreatic cancer precursor lesions in mice. J Clin Invest 2010;120:508-20.
11. Al-Aynati MM, Radulovich N, Riddell RH, Tsao MS. Epithelial-cadherin and beta-catenin expression changes in pancreatic intraepithelial neoplasia. Clin Cancer Res 2004;10:1235-40.
12. Zeng G, Germinaro M, Micsenyi A, Monga NK, Bell A, Sood A, et al. Aberrant Wnt/beta-catenin signaling in pancreatic adenocarcinoma. Neoplasia 2006;8:279-89.
13. Wang L, Heidt DG, Lee CJ, Yang H, Logsdon CD, Zhang L, et al. Oncogenic function of ATDC in pancreatic cancer through Wnt pathway activation and beta-catenin stabilization. Cancer Cell 2009;15: 207-19.
14. Chu EY, Hens J, Andl T, Kairo A, Yamaguchi TP, Brisken C, et al. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development 2004;131:4819-29.
15. Yang SH, Andl T, Grachtchouk V, Wang A, Liu J, Syu LJ, et al. Pathological responses to oncogenic Hedgehog signaling in skin are dependent on canonical Wnt/beta3-catenin signaling. Nat Genet 2008;40:1130-5.
16. Gurney A, Axelrod F, Bond CJ, Cain J, Chartier C, Donigan L, et al. Wnt pathway inhibition via the targeting of Frizzled receptors results in decreased growth and tumorigenicity of human tumors. Proc Natl Acad Sci U S A 2012;109:11717-22.
17. Collins MA, Brisset JC, Zhang Y, Bednar F, Pierre J, Heist KA, et al. Metastatic pancreatic cancer is dependent on oncogenic Kras in mice. PLoS ONE 2012;7:e49707.
18. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res 2007;67: 1030-7.
19. Miyamoto Y, Maitra A, Ghosh B, Zechner U, Argani P, Iacobuzio- Donahue CA, et al. Notch mediates TGF alpha-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell 2003;3:565-76.
20. Hruban RH, Adsay NV, Albores-Saavedra J, Anver MR, Biankin AV, Boivin GP, et al. Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations. Cancer Res 2006;66:95-106.
21. Collins MA, Bednar F, Zhang Y, Brisset JC, Galban S, Galban CJ, et al. Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice. J Clin Invest 2012;122:639-53.
22. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, et al. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001;128:1253-64.
23. Murtaugh LC, Law AC, Dor Y, Melton DA. Beta-catenin is essential for pancreatic acinar but not islet development. Development 2005;132: 4663-74.
24. Dessimoz J, Bonnard C, Huelsken J, Grapin-Botton A. Pancreasspecific deletion of beta-catenin reveals Wnt-dependent and Wntindependent functions during development. Curr Biol 2005;15: 1677-83.
25. Papadopoulou S, Edlund H. Attenuated wnt signaling perturbs pancreatic growth but not pancreatic function. Diabetes 2005;54: 2844-51.
26. Habbe N, Shi G, Meguid RA, Fendrich V, Esni F, Chen H, et al. Spontaneous induction of murine pancreatic intraepithelial neoplasia (mPanIN) by acinar cell targeting of oncogenic Kras in adult mice. Proc Natl Acad Sci U S A 2008;105:18913-8.
27. Valenta T, Hausmann G, Basler K. The many faces and functions of beta-catenin. EMBO J 2012;31:2714-36.
28. Mao B,Wu W, Davidson G, Marhold J, Li M, Mechler BM, et al. Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature 2002;417:664-7.
29. Belteki G, Haigh J, Kabacs N, Haigh K, Sison K, Costantini F, et al. Conditional and inducible transgene expression in mice through the combinatorial use of Cre-mediated recombination and tetracycline induction. Nucleic Acids Res 2005;33:e51.
30. Aguirre AJ, Bardeesy N, Sinha M, Lopez L, Tuveson DA, Horner J, et al. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev 2003;17: 3112-26.
31. Van Mater D, Kolligs FT, Dlugosz AA, Fearon ER. Transient activation of beta -catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. Genes Dev 2003;17:1219-24.
32. Grumolato L, Liu G, Mong P, Mudbhary R, Biswas R, Arroyave R, et al. Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev 2010;24: 2517-30.
33. Montcouquiol M, Rachel RA, Lanford PJ, Copeland NG, Jenkins NA, Kelley MW. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 2003;423:173-7.
34. Axelrod JD, Miller JR, Shulman JM, Moon RT, Perrimon N. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev 1998;12: 2610-22.
35. Collisson EA, Trejo CL, Silva JM, Gu S, Korkola JE, Heiser LM, et al. A central role for RAF!MEK!ERK signaling in the genesis of pancreatic ductal adenocarcinoma. Cancer Discov 2012;2:685-93.
36. Qu C, DiRenzo D, Konieczny SF. Identifying molecular signatures for the earliest KRAS-induced transformation events in pancreatic adenocarcinoma development. Pancreas 2011;40:1349.
37. Ardito CM, Gruner BM, Takeuchi KK, Lubeseder-Martellato C, Teichmann N, Mazur PK, et al. EGF receptor is required for KRAS-induced pancreatic tumorigenesis. Cancer Cell 2012;22:304-17.
38. Daniluk J, Liu Y, Deng D, Chu J, Huang H, Gaiser S, et al. An NFkappaB pathway-mediated positive feedback loop amplifies Ras activity to pathological levels in mice. J Clin Invest 2012;122: 1519-28.
39. Guerra C, Collado M, Navas C, Schuhmacher AJ, Hernandez-Porras I, Canamero M, et al. Pancreatitis-induced inflammation contributes to pancreatic cancer by inhibiting oncogene-induced senescence. Cancer Cell 2011;19:728-39.
40. Guerra C, Schuhmacher AJ, Canamero M, Grippo PJ, Verdaguer L, Perez-Gallego L, et al. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell 2007;11:291-302.
41. Navas C, Hernandez-Porras I, Schuhmacher AJ, Sibilia M, Guerra C, Barbacid M. EGF receptor signaling is essential for k-ras oncogenedriven pancreatic ductal adenocarcinoma. Cancer Cell 2012;22: 318-30.
42. Carriere C, Young AL, Gunn JR, Longnecker DS, Korc M. Acute pancreatitis accelerates initiation and progression to pancreatic cancer in mice expressing oncogenic Kras in the nestin cell lineage. PLoS ONE 2011;6:e27725.
43. Semenov MV, Habas R, Macdonald BT,He X. SnapShot: noncanonical Wnt signaling pathways. Cell 2007;131:1378.
44. Nolan-Stevaux O, Lau J, Truitt ML, Chu GC, Hebrok M, Fernandez- Zapico ME, et al. GLI1 is regulated through Smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation. Genes Dev 2009;23:24-36.
45. Heiser PW, Lau J, Taketo MM, Herrera PL, Hebrok M. Stabilization of beta-catenin impacts pancreas growth. Development 2006;133: 2023-32.
46. Wells JM, Esni F, Boivin GP, Aronow BJ, Stuart W, Combs C, et al. Wnt/ beta-catenin signaling is required for development of the exocrine pancreas. BMC Dev Biol 2007;7:4.
47. Keefe MD, Wang H, De La OJ, Khan A, Firpo MA, Murtaugh LC. b-Catenin is selectively required for the expansion and regeneration of mature pancreatic acinar cells in mice. Dis Model Mech 2012; 5:503-14.
48. Heiser PW, Cano DA, Landsman L, Kim GE, Kench JG, Klimstra DS, et al. Stabilization of beta-catenin induces pancreas tumor formation. Gastroenterology 2008;135:1288-300.
49. Arensman MD, Kovochich AN, Kulikauskas RM, Lay AR, Yang PT, Li X, et al. WNT7B mediates autocrine Wnt/beta-catenin signaling and anchorage-independent growth in pancreatic adenocarcinoma. Oncogene. 2013 Feb 18. [Epub ahead of print].
50. Nawroth R, van Zante A, Cervantes S, McManus M, Hebrok M, Rosen SD. Extracellular sulfatases, elements of the wnt signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells. PLoS ONE 2007;2:e392.
51. Mann KM, Ward JM, Yew CC, Kovochich A, Dawson DW, Black MA, et al. Sleeping Beauty mutagenesis reveals cooperating mutations and pathways in pancreatic adenocarcinoma. Proc Natl Acad Sci U S A 2012;109:5934-41.
52. Yu M, Ting DT, Stott SL, Wittner BS, Ozsolak F, Paul S, et al. RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis. Nature 2012;487:510-3.
53. Crnogorac-Jurcevic T, Efthimiou E, Capelli P, Blaveri E, Baron A, Terris B, et al. Gene expression profiles of pancreatic cancer and stromal desmoplasia. Oncogene 2001;20:7437-46.
54. Griesmann H, Ripka S, Pralle M, Ellenrieder V, Baumgart S, Buchholz M, et al. WNT5A-NFAT signaling mediates resistance to apoptosis in pancreatic cancer. Neoplasia 2013;15:11-22.
55. Pilarsky C, Ammerpohl O, Sipos B, Dahl E, Hartmann A, Wellmann A, et al. Activation of Wnt signalling in stroma from pancreatic cancer identified by gene expression profiling. J Cell Mol Med 2008;12:2823-35.
56. Ripka S, Konig A, Buchholz M, Wagner M, Sipos B, Kloppel G, et al. WNT5A-target of CUTL1 and potent modulator of tumor cell migration and invasion in pancreatic cancer. Carcinogenesis 2007;28:1178-87.
57. Pacheco-Pinedo EC, Durham AC, Stewart KM, Goss AM, Lu MM, Demayo FJ, et al. Wnt/beta-catenin signaling accelerates mouse lung tumorigenesis by imposing an embryonic distal progenitor phenotype on lung epithelium. J Clin Invest 2011;121:1935-45.
58. Janssen KP, Alberici P, Fsihi H, Gaspar C, Breukel C, Franken P, et al. APC and oncogenic KRAS are synergistic in enhancing Wnt signaling in intestinal tumor formation and progression. Gastroenterology 2006;131:1096-109.
59. Jeong WJ, Yoon J, Park JC, Lee SH, Kaduwal S, Kim H, et al. Ras stabilization through aberrant activation of Wnt/beta-catenin signaling promotes intestinal tumorigenesis. Sci Signal 2012;5:ra30.
60. Biechele TL, Kulikauskas RM, Toroni RA, Lucero OM, Swift RD, James RG, et al. Wnt/beta-catenin signaling and AXIN1 regulate apoptosis triggered by inhibition of the mutant kinase BRAFV600E in human melanoma. Sci Signal 2012;5:ra3.
61. Li H, Pamukcu R, Thompson WJ. beta-Catenin signaling: therapeutic strategies in oncology. Cancer Biol Ther 2002;1:621-5.
62. PolakisP.DruggingWnt signalling in cancer. EMBOJ 2012;31:2737-46.