Notch mediates TGFα-induced changes in epithelial differentiation during pancreatic tumorigenesis

Cancer Cell

Volumn 3, Issue 6, 2003, Pages 565-576

  Miyamoto, Yoshiharu ^a   Maitra, Anirban ^a   Ghosh, Bidyut ^a   Zechner, Ulrich ^b   Argani, Pedram ^a   Iacobuzio Donahue, Christine A ^a   Sriuranpong, Virote ^a   Iso, Tatsuya ^c   Meszoely, Ingrid M ^d   Wolfe, Michael S ^e   Hruban, Ralph H ^a   Ball, Douglas W ^a   Schmid, Roland M ^b   Leach, Steven D ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b UNIVERSITY OF ULM   (Germany)

^c GUNMA UNIVERSITY   (Japan)

^d FOX CHASE CANCER CENTER   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; NESTIN; NOTCH RECEPTOR; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIUM; EPITHELIUM CELL; GENE TARGETING; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; PANCREAS; PANCREAS TUMOR; PRECURSOR; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 10744223624     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1535-6108(03)00140-5     Document Type: Article

References (65)

1. Apelqvist A., Li H., Sommer L., Beatus P., Anderson D.J., Honjo T., Hrabe de Angelis M., Lendahl U., Edlund H. Notch signalling controls pancreatic cell differentiation. Nature. 400:1999;877-881.
2. Arlt A., Vorndamm J., Breitenbroich M., Folsch U.R., Kalthoff H., Schmidt W.E., Schafer H. Inhibition of NF-kappaB sensitizes human pancreatic carcinoma cells to apoptosis induced by etoposide (VP16) or doxorubicin. Oncogene. 20:2001;859-868.
3. Artavanis-Tsakonas S., Rand M.D., Lake R.J. Notch signaling. cell fate control and signal integration in development Science. 284:1999;770-776.
4. Bellavia D., Campese A.F., Alesse E., Vacca A., Felli M.P., Balestri A., Stoppacciaro A., Tiveron C., Tatangelo L., Giovarelli M.et al. Constitutive activation of NF-kappaB and T-cell leukemia/lymphoma in Notch3 transgenic mice. EMBO J. 19:2000;3337-3348.
5. Berezovska O., Jack C., McLean P., Aster J.C., Hicks C., Xia W., Wolfe M.S., Kimberly W.T., Weinmaster G., Selkoe D.J., Hyman B.T. Aspartate mutations in presenilin and gamma-secretase inhibitors both impair notch1 proteolysis and nuclear translocation with relative preservation of notch1 signaling. J. Neurochem. 75:2000;583-593.
6. Berset T., Hoier E.F., Battu G., Canevascini S., Hajnal A. Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science. 291:2001;1055-1058.
7. Capobianco A.J., Zagouras P., Blaumueller C.M., Artavanis-Tsakonas S., Bishop J.M. Neoplastic transformation by truncated alleles of human NOTCH1/TAN1 and NOTCH2. Mol. Cell. Biol. 17:1997;6265-6273.
8. Carmena A., Buff E., Halfon M.S., Gisselbrecht S., Jimenez F., Baylies M.K., Michelson A.M. Reciprocal regulatory interactions between the Notch and Ras signaling pathways in the Drosophila embryonic mesoderm. Dev. Biol. 244:2002;226-242.
9. Chen H., Thiagalingam A., Chopra H., Borges M.W., Feder J.N., Nelkin B.D., Baylin S.B., Ball D.W. Conservation of the Drosophila lateral inhibition pathway in human lung cancer. a hairy-related protein (HES-1) directly represses achaete-scute homolog-1 expression Proc. Natl. Acad. Sci. USA. 94:1997;5355-5360.
10. Cheng P., Zlobin A., Volgina V., Gottipati S., Osborne B., Simel E.J., Miele L., Gabrilovich D.I. Notch-1 regulates NF-kappaB activity in hemopoietic progenitor cells. J. Immunol. 167:2001;4458-4467.
11. Culi J., Martin-Blanco E., Modolell J. The EGF receptor and N signalling pathways act antagonistically in Drosophila mesothorax bristle patterning. Development. 128:2001;299-308.
12. Davis R.L., Turner D.L. Vertebrate hairy and Enhancer of split related proteins. transcriptional repressors regulating cellular differentiation and embryonic patterning Oncogene. 20:2001;8342-8357.
13. De Strooper B., Annaert W., Cupers P., Saftig P., Craessaerts K., Mumm J.S., Schroeter E.H., Schrijvers V., Wolfe M.S., Ray W.J.et al. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature. 398:1999;518-522.
14. Deftos M.L., Bevan M.J. Notch signaling in T cell development. Curr. Opin. Immunol. 12:2000;166-172.
15. Donoviel D.B., Donoviel M.S., Fan E., Hadjantonakis A., Bernstein A. Cloning and characterization of Sel-1l, a murine homolog of the C. elegans sel-1 gene. Mech. Dev. 78:1998;203-207.
16. Dovey H.F., John V., Anderson J.P., Chen L.Z., de Saint Andrieu P., Fang L.Y., Freedman S.B., Folmer B., Goldbach E., Holsztynska E.J.et al. Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain. J. Neurochem. 76:2001;173-181.
17. Esler W.P., Kimberly W.T., Ostaszewski B.L., Ye W., Diehl T.S., Selkoe D.J., Wolfe M.S. Activity-dependent isolation of the presenilin-gamma-secretase complex reveals nicastrin and a gamma substrate. Proc. Natl. Acad. Sci. USA. 99:2002;2720-2725.
18. Finch P.W., He X., Kelley M.J., Uren A., Schaudies R.P., Popescu N.C., Rudikoff S., Aaronson S.A., Varmus H.E., Rubin J.S. Purification and molecular cloning of a secreted, Frizzled-related antagonist of Wnt action. Proc. Natl. Acad. Sci. USA. 94:1997;6770-6775.
19. Fitzgerald K., Harrington A., Leder P. Ras pathway signals are required for notch-mediated oncogenesis. Oncogene. 19:2000;4191-4198.
20. Gansauge S., Gansauge F., Ramadani M., Stobbe H., Rau B., Harada N., Beger H.G. Overexpression of cyclin D1 in human pancreatic carcinoma is associated with poor prognosis. Cancer Res. 57:1997;1634-1637.
21. Gasslander T., Ihse I., Smeds S. The importance of the centroacinar region in cerulein-induced mouse pancreatic growth. Scand. J. Gastroenterol. 27:1992;564-570.
22. Grant B., Greenwald I. Structure, function, and expression of SEL-1, a negative regulator of LIN-12 and GLP-1 in C. elegans. Development. 124:1997;637-644.
23. Harada Y., Ozaki K., Suzuki M., Fujiwara T., Takahashi E., Nakamura Y., Tanigami A. Complete cDNA sequence and genomic organization of a human pancreas-specific gene homologous to Caenorhabditis elegans sel-1. J. Hum. Genet. 44:1999;330-336.
24. Hayashi K., Takahashi T., Kakita A., Yamashina S. Regional differences in the cellular proliferation activity of the regenerating rat pancreas after partial pancreatectomy. Arch. Histol. Cytol. 62:1999;337-346.
25. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA. 95:1998;2509-2514.
26. Hruban R.H., Wilentz R.E., Goggins M., Offerhaus G.J., Yeo C.J., Kern S.E. Pathology of incipient pancreatic cancer. Ann. Oncol. 10(Suppl. 4):1999;9-11.
27. Hu Y.X., Watanabe H., Ohtsubo K., Yamaguchi Y., Ha A., Motoo Y., Okai T., Sawabu N. Bcl-2 expression related to altered p53 protein and its impact on the progression of human pancreatic carcinoma. Br. J. Cancer. 80:1999;1075-1079.
28. Hunziker E., Stein M. Nestin-expressing cells in the pancreatic islets of Langerhans. Biochem. Biophys. Res. Commun. 271:2000;116-119.
29. Iacobuzio-Donahue C.A., Maitra A., Shen-Ong G.L., van Heek T., Ashfaq R., Meyer R., Walter K., Berg K., Hollingsworth M.A., Cameron J.L.et al. Discovery of novel tumor markers of pancreatic cancer using global gene expression technology. Am. J. Pathol. 160:2002;1239-1249. a.
30. Iacobuzio-Donahue C.A., Ryu B., Hruban R.H., Kern S.E. Exploring the host desmoplastic response to pancreatic carcinoma. gene expression of stromal and neoplastic cells at the site of primary invasion Am. J. Pathol. 160:2002;91-99. b.
31. Irvin D.K., Zurcher S.D., Nguyen T., Weinmaster G., Kornblum H.I. Expression patterns of Notch1, Notch2, and Notch3 suggest multiple functional roles for the Notch-DSL signaling system during brain development. J. Comp. Neurol. 436:2001;167-181.
32. Iso T., Sartorelli V., Chung G., Shichinohe T., Kedes L., Hamamori Y. HERP, a new primary target of Notch regulated by ligand binding. Mol. Cell. Biol. 21:2001;6071-6079.
33. Iso T., Chung G., Hamamori Y., Kedes L. HERP1 is a cell type-specific primary target of Notch. J. Biol. Chem. 277:2002;6598-6607.
34. Jemal A., Thomas A., Murray T., Thun M. Cancer statistics, 2002. CA Cancer J. Clin. 52:2002;23-47.
35. Jensen J., Heller R.S., Funder-Nielsen T., Pedersen E.E., Lindsell C., Weinmaster G., Madsen O.D., Serup P. Independent development of pancreatic alpha- and beta-cells from neurogenin3-expressing precursors. a role for the notch pathway in repression of premature differentiation Diabetes. 49:2000;163-176. a.
36. Jensen J., Pedersen E.E., Galante P., Hald J., Heller R.S., Ishibashi M., Kageyama R., Guillemot F., Serup P., Madsen O.D. Control of endodermal endocrine development by Hes-1. Nat. Genet. 24:2000;36-44. b.
37. Jhappan C., Stahle C., Harkins R.N., Fausto N., Smith G.H., Merlino G.T. TGF alpha overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell. 61:1990;1137-1146.
38. Kao H.Y., Ordentlich P., Koyano-Nakagawa N., Tang Z., Downes M., Kintner C.R., Evans R.M., Kadesch T. A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev. 12:1998;2269-2277.
39. Kawaguchi A., Miyata T., Sawamoto K., Takashita N., Murayama A., Akamatsu W., Ogawa M., Okabe M., Tano Y., Goldman S.A., Okano H. Nestin-EGFP transgenic mice. visualization of the self-renewal and multipotency of CNS stem cells Mol. Cell. Neurosci. 17:2001;259-273.
40. Korc M. Role of growth factors in pancreatic cancer. Surg. Oncol. Clin. N. Am. 7:1998;25-41.
41. Lechner A., Leech C.A., Abraham E.J., Nolan A.L., Habener J.F. Nestin-positive progenitor cells derived from adult human pancreatic islets of Langerhans contain side population (SP) cells defined by expression of the ABCG2 (BCRP1) ATP-binding cassette transporter. Biochem. Biophys. Res. Commun. 293:2002;670-674.
42. Lutolf S., Radtke F., Aguet M., Suter U., Taylor V. Notch1 is required for neuronal and glial differentiation in the cerebellum. Development. 129:2002;373-385.
43. Mayr T., Deutsch U., Kuhl M., Drexler H.C., Lottspeich F., Deutzmann R., Wedlich D., Risau W. Fritz. a secreted frizzled-related protein that inhibits Wnt activity Mech. Dev. 63:1997;109-125.
44. Messam C.A., Hou J., Major E.O. Coexpression of nestin in neural and glial cells in the developing human CNS defined by a human-specific anti-nestin antibody. Exp. Neurol. 161:2000;585-596.
45. Moskaluk C.A., Hruban R.H., Kern S.E. p16 and K-ras gene mutations in the intraductal precursors of human pancreatic adenocarcinoma. Cancer Res. 57:1997;2140-2143.
46. Mumm J.S., Kopan R. Notch signaling. from the outside in Dev. Biol. 228:2000;151-165.
47. Nickoloff B.J., Qin J.Z., Chaturvedi V., Denning M.F., Bonish B., Miele L. Jagged-1 mediated activation of notch signaling induces complete maturation of human keratinocytes through NF-kappaB and PPARgamma. Cell Death Differ. 9:2002;842-855.
48. Oswald F., Liptay S., Adler G., Schmid R.M. NF-kappaB2 is a putative target gene of activated Notch-1 via RBP-Jkappa. Mol. Cell. Biol. 18:1998;2077-2088.
49. Parsa I., Longnecker D.S., Scarpelli D.G., Pour P., Reddy J.K., Lefkowitz M. Ductal metaplasia of human exocrine pancreas and its association with carcinoma. Cancer Res. 45:1985;1285-1290.
50. Price J.V., Savenye E.D., Lum D., Breitkreutz A. Dominant enhancers of Egfr in Drosophila melanogaster. genetic links between the Notch and Egfr signaling pathways Genetics. 147:1997;1139-1153.
51. Ronchini C., Capobianco A.J. Induction of cyclin D1 transcription and CDK2 activity by Notch(ic). implication for cell cycle disruption in transformation by Notch(ic) Mol. Cell. Biol. 21:2001;5925-5934.
52. Ruiz-Hidalgo M.J., Garces C., Laborda J. Notch-1 expression levels in 3T3-L1 cells influence ras signaling and transformation by oncogenic ras. Int. J. Oncol. 14:1999;777-783.
53. Sandgren E.P., Luetteke N.C., Palmiter R.D., Brinster R.L., Lee D.C. Overexpression of TGF alpha in transgenic mice. induction of epithelial hyperplasia, pancreatic metaplasia, and carcinoma of the breast Cell. 61:1990;1121-1135.
54. Selander L., Edlund H. Nestin is expressed in mesenchymal and not epithelial cells of the developing mouse pancreas. Mech. Dev. 113:2002;189-192.
55. Song S.Y., Gannon M., Washington M.K., Scoggins C.R., Meszoely I.M., Goldenring J.R., Marino C.R., Sandgren E.P., Coffey R.J. Jr., Wright C.V., Leach S.D. Expansion of Pdx1-expressing pancreatic epithelium and islet neogenesis in transgenic mice overexpressing transforming growth factor alpha. Gastroenterology. 117:1999;1416-1426.
56. Sriuranpong V., Borges M.W., Ravi R.K., Arnold D.R., Nelkin B.D., Baylin S.B., Ball D.W. Notch signaling induces cell cycle arrest in small cell lung cancer cells. Cancer Res. 61:2001;3200-3205.
57. Tomlinson A., Struhl G. Delta/Notch and Boss/Sevenless signals act combinatorially to specify the Drosophila R7 photoreceptor. Mol. Cell. 7:2001;487-495.
58. Wagner M., Luhrs H., Kloppel G., Adler G., Schmid R.M. Malignant transformation of duct-like cells originating from acini in transforming growth factor transgenic mice. Gastroenterology. 115:1998;1254-1262.
59. Wagner M., Greten F.R., Weber C.K., Koschnick S., Mattfeldt T., Deppert W., Kern H., Adler G., Schmid R.M. A murine tumor progression model for pancreatic cancer recapitulating the genetic alterations of the human disease. Genes Dev. 15:2001;286-293.
60. Wagner M., Weber C.K., Bressau F., Greten F.R., Stagge V., Ebert M., Leach S.D., Adler G., Schmid R.M. Transgenic overexpression of amphiregulin induces a mitogenic response selectively in pancreatic duct cells. Gastroenterology. 122:2002;1898-1912.
61. Weijzen S., Rizzo P., Braid M., Vaishnav R., Jonkheer S.M., Zlobin A., Osborne B.A., Gottipati S., Aster J.C., Hahn W.C.et al. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nat. Med. 8:2002;979-986.
62. Wilentz R.E., Iacobuzio-Donahue C.A., Argani P., McCarthy D.M., Parsons J.L., Yeo C.J., Kern S.E., Hruban R.H. Loss of expression of Dpc4 in pancreatic intraepithelial neoplasia. evidence that DPC4 inactivation occurs late in neoplastic progression Cancer Res. 60:2000;2002-2006.
63. Wolfe M.S., Xia W., Moore C.L., Leatherwood D.D., Ostaszewski B., Rahmati T., Donkor I.O., Selkoe D.J. Peptidomimetic probes and molecular modeling suggest that Alzheimer's gamma-secretase is an intramembrane-cleaving aspartyl protease. Biochemistry. 38:1999;4720-4727.
64. Zulewski H., Abraham E.J., Gerlach M.J., Daniel P.B., Moritz W., Muller B., Vallejo M., Thomas M.K., Habener J.F. Multipotential nestin-positive stem cells isolated from adult pancreatic islets differentiate ex vivo into pancreatic endocrine, exocrine, and hepatic phenotypes. Diabetes. 50:2001;521-533.
65. zur Lage P., Jarman A.P. Antagonism of EGFR and notch signalling in the reiterative recruitment of Drosophila adult chordotonal sense organ precursors. Development. 126:1999;3149-3157.