Epithelial Notch signaling is a limiting step for pancreatic carcinogenesis

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Thomas, Marsha M ^a   Zhang, Yaqing ^a   Mathew, Esha ^b   Kane, Kevin T ^a   Maillard, Ivan ^b   Di Magliano, Marina Pasca ^a,b,c  

^a Department of Surgery ^*  (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

DNMAML; Epithelium; Genetically engineered mouse model; Mastermind like; Notch; Pancreatic cancer

Indexed keywords

MASTERMIND LIKE 1 PROTEIN; NOTCH RECEPTOR; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CONTROLLED STUDY; MASTERMIND LIKE 1 GENE; MOUSE; NONHUMAN; PANCREAS CANCER; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; TUMOR PROMOTION;

EID: 84928722688     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-862     Document Type: Article

References (45)

1. Hariharan D, Saied A, Kocher HM: Analysis of mortality rates for pancreatic cancer across the world. HPB (Oxford) 2008, 10:58-62.
2. Siegel R, Naishadham D, Jemal A: Cancer statistics, 2013. CA Cancer J Clin 2013, 63:11-30.
3. Hruban RH, Goggins M, Parsons J, Kern SE: Progression model for pancreatic cancer. Clin Cancer Res 2000, 6:2969-2972.
4. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, Ross S, Conrads TP, Veenstra TD, Hitt BA, Kawaguchi Y, Johann D, Liotta LA, Crawford HC, Putt ME, Jacks T, Wright CV, Hruban RH, Lowy AM, Tuveson DA: Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003, 4:437-450.
5. Di Magliano MP, Sekine S, Ermilov A, Ferris J, Dlugosz AA, Hebrok M: Hedgehog/Ras interactions regulate early stages of pancreatic cancer. Genes Dev 2006, 20:3161-3173.
6. Collins MA, Bednar F, Zhang YQ, Brisset JC, Galban S, Galban CJ, Rakshit S, Flannagan KS, Adsay NV, Di Magliano MP: Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice. J Clin Invest 2012, 122:639-653.
7. Bardeesy N, DePinho RA: Pancreatic cancer biology and genetics. Nat Rev Cancer 2002, 2:897-909.
8. Di Magliano MP, Biankin AV, Heiser PW, Cano DA, Gutierrez PJA, Deramaudt T, Segara D, Dawson AC, Kench JG, Henshall SM, Sutherland RL, Dlugosz A, Rustgi AK, Hebrok M: Common activation of canonical wnt signaling in pancreatic adenocarcinoma. Plos One 2007, 2:e1155.
9. Miyamoto Y, Maitra A, Ghosh B, Zechner U, Argani P, Iacobuzio-Donahue CA, Sriuranpong V, Iso T, Meszoely IM, Wolfe MS, Hruban RH, Ball DW, Schmid RM, Leach SD: Notch mediates TGF alpha-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell 2003, 3:565-576.
10. Plentz R, Park JS, Rhim AD, Abravanel D, Hezel AF, Sharma SV, Gurumurthy S, Deshpande V, Kenific C, Settleman J, Majumder PK, Stanger BZ, Bardeesy N: Inhibition of gamma-secretase activity inhibits tumor progression in a mouse model of pancreatic ductal adenocarcinoma. Gastroenterology 2009, 136:1741-1749.
11. Wang Z, Li Y, Kong D, Banerjee S, Ahmad A, Azmi AS, Ali S, Abbruzzese JL, Gallick GE, Sarkar FH: Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res 2009, 69:2400-2407.
12. Mullendore ME, Koorstra JB, Li YM, Offerhaus GJ, Fan X, Henderson CM, Matsui W, Eberhart CG, Maitra A, Feldmann G: Ligand-dependent notch signaling is involved in tumor initiation and tumor maintenance in pancreatic cancer. Clin Cancer Res 2009, 15:2291-2301.
13. Bao B, Wang Z, Ali S, Kong D, Li Y, Ahmad A, Banerjee S, Azmi AS, Miele L, Sarkar FH: Notch-1 induces epithelial-mesenchymal transition consistent with cancer stem cell phenotype in pancreatic cancer cells. Cancer Lett 2011, 307:26-36.
14. Hemming ML, Elias JE, Gygi SP, Selkoe DJ: Proteomic profiling of gamma-secretase substrates and mapping of substrate requirements. PLoS Biol 2008, 6:e257.
15. Hanlon L, Avila JL, Demarest RM, Troutman S, Allen M, Ratti F, Rustgi AK, Stanger BZ, Radtke F, Adsay V, Long F, Capobianco AJ, Kissil JL: Notch1 functions as a tumor suppressor in a model of K-ras-induced pancreatic ductal adenocarcinoma. Cancer Res 2010, 70:4280-4286.
16. Mazur PK, Einwachter H, Lee M, Sipos B, Nakhai H, Rad R, Zimber-Strobl U, Strobl LJ, Radtke F, Kloppel G, Schmid RM, Siveke JT: Notch2 is required for progression of pancreatic intraepithelial neoplasia and development of pancreatic ductal adenocarcinoma. Proc Natl Acad Sci U S A 2010, 107:13438-13443.
17. Nakhai H, Siveke JT, Klein B, Mendoza-Torres L, Mazur PK, Algul H, Radtke F, Strobl L, Zimber-Strobl U, Schmid RM: Conditional ablation of Notch signaling in pancreatic development. Development 2008, 135:2757-2765.
18. Wu L, Sun T, Kobayashi K, Gao P, Griffin JD: Identification of a family of mastermind-like transcriptional coactivators for mammalian notch receptors. Mol Cell Biol 2002, 22:7688-7700.
19. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, Wright CV: The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 2002, 32:128-134.
20. Tuveson DA, Shaw AT, Willis NA, Silver DP, Jackson EL, Chang S, Mercer KL, Grochow R, Hock H, Crowley D, Hingorani SR, Zaks T, King C, Jacobetz MA, Wang L, Bronson RT, Orkin SH, DePinho RA, Jacks T: Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 2004, 5:375-387.
21. Maillard I, Koch U, Dumortier A, Shestova O, Xu L, Sai H, Pross SE, Aster JC, Bhandoola A, Radtke F, Pear WS: Canonical notch signaling is dispensable for the maintenance of adult hematopoietic stem cells. Cell Stem Cell 2008, 2:356-366.
22. Maillard I, Tu L, Sambandam A, Yashiro-Ohtani Y, Millholland J, Keeshan K, Shestova O, Xu L, Bhandoola A, Pear WS: The requirement for Notch signaling at the beta-selection checkpoint in vivo is absolute and independent of the pre-T cell receptor. J Exp Med 2006, 203:2239-2245.
23. Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, Warman ML: Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 2000, 29:52-54.
24. 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, 120:508-520.
25. Kojima K, Vickers SM, Adsay NV, Jhala NC, Kim HG, Schoeb TR, Grizzle WE, Klug CA: Inactivation of Smad4 accelerates Kras(G12D)-mediated pancreatic neoplasia. Cancer Res 2007, 67:8121-8130.
26. Hruban RH, Rustgi AK, Brentnall TA, Tempero MA, Wright CV, Tuveson DA: Pancreatic cancer in mice and man: the penn workshop 2004. Cancer Res 2006, 66:14-17.
27. Mumm JS, Kopan R: Notch signaling: from the outside in. Dev Biol 2000, 228:151-165.
28. Jouve C, Palmeirim I, Henrique D, Beckers J, Gossler A, Ish-Horowicz D, Pourquie O: Notch signalling is required for cyclic expression of the hairy-like gene HES1 in the presomitic mesoderm. Development 2000, 127:1421-1429.
29. Steidl C, Leimeister C, Klamt B, Maier M, Nanda I, Dixon M, Clarke R, Schmid M, Gessler M: Characterization of the human and mouse HEY1, HEY2, and HEYL genes: cloning, mapping, and mutation screening of a new bHLH gene family. Genomics 2000, 66:195-203.
30. Maier MM, Gessler M: Comparative analysis of the human and mouse hey1 promoter: hey genes are new Notch target genes. Biochem Biophys Res Commun 2000, 275:652-660.
31. Scholzen T, Gerdes J: The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000, 182:311-322.
32. Berman DM, Karhadkar SS, Maitra A, Montes De Oca R, Gerstenblith MR, Briggs K, Parker AR, Shimada Y, Eshleman JR, Watkins DN, Beachy PA: Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 2003, 425:846-851.
33. Yauch RL, Gould SE, Scales SJ, Tang T, Tian H, Ahn CP, Marshall D, Fu L, Januario T, Kallop D, Nannini-Pepe M, Kotkow K, Marsters JC, Rubin LL, de Sauvage FJ: A paracrine requirement for hedgehog signalling in cancer. Nature 2008, 455:406-410.
34. Lucero OM, Dawson DW, Moon RT, Chien AJ: A re-evaluation of the "oncogenic" nature of Wnt/beta-catenin signaling in melanoma and other cancers. Curr Oncol Rep 2010, 12:314-318.
35. Zhang Y, Morris JP, Yan W, Schofield HK, Gurney A, Simeone DM, Millar SE, Hoey T, Hebrok M, Pasca Di Magliano M: Canonical wnt signaling is required for pancreatic carcinogenesis. Cancer Res 2013, 73:4909-4922.
36. Mills LD, Zhang Y, Marler RJ, Herreros-Villanueva M, Zhang L, Almada LL, Couch F, Wetmore C, Pasca Di Magliano M, Fernandez-Zapico ME: Loss of the transcription factor GLI1 identifies a signaling network in the tumor microenvironment mediating KRAS oncogene-induced transformation. J Biol Chem 2013, 288:11786-11794.
37. Guerra C, Collado M, Navas C, Schuhmacher AJ, Hernandez-Porras I, Canamero M, Rodriguez-Justo M, Serrano M, Barbacid M: Pancreatitisinduced inflammation contributes to pancreatic cancer by inhibiting oncogene-induced senescence. Cancer Cell 2011, 19:728-739.
38. Guerra C, Schuhmacher AJ, Canamero M, Grippo PJ, Verdaguer L, Perez-Gallego L, Dubus P, Sandgren EP, Barbacid M: Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell 2007, 11:291-302.
39. 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.
40. Murtaugh LC, Stanger BZ, Kwan KM, Melton DA: Notch signaling controls multiple steps of pancreatic differentiation. Proc Natl Acad Sci U S A 2003, 100:14920-14925.
41. Rooman I, De Medts N, Baeyens L, Lardon J, De Breuck S, Heimberg H, Bouwens L: Expression of the Notch signaling pathway and effect on exocrine cell proliferation in adult rat pancreas. Am J Pathol 2006, 169:1206-1214.
42. Siveke JT, Lubeseder-Martellato C, Lee M, Mazur PK, Nakhai H, Radtke F, Schmid RM: Notch signaling is required for exocrine regeneration after acute pancreatitis. Gastroenterology 2008, 134:544-555.
43. Kitamoto T, Takahashi K, Takimoto H, Tomizuka K, Hayasaka M, Tabira T, Hanaoka K: Functional redundancy of the Notch gene family during mouse embryogenesis: analysis of Notch gene expression in Notch3-deficient mice. Biochem Biophys Res Commun 2005, 331:1154-1162.
44. Afelik S, Qu X, Hasrouni E, Bukys MA, Deering T, Nieuwoudt S, Rogers W, Macdonald RJ, Jensen J: Notch-mediated patterning and cell fate allocation of pancreatic progenitor cells. Development 2012, 139:1744-1753.
45. Horn S, Kobberup S, Jorgensen MC, Kalisz M, Klein T, Kageyama R, Gegg M, Lickert H, Lindner J, Magnuson MA, Kong YY, Serup P, Ahnfelt-Rønne J, Jensen JN: Mind bomb 1 is required for pancreatic beta-cell formation. Proc Natl Acad Sci U S A 2012, 109:7356-7361.