Hedgehog inhibition prolongs survival in a genetically engineered mouse model of pancreatic cancer

Gut

Volumn 57, Issue 10, 2008, Pages 1420-1430

  Feldmann, G ^a   Habbe, N ^a   Dhara, S ^a   Bisht, S ^a   Alvarez, H ^a   Fendrich, V ^a,b   Beaty, R ^a,c   Mullendore, M ^a   Karikari, C ^a   Bardeesy, N ^d   Ouellette, M M ^e   Yu, W ^a   Maitra, A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; CRE RECOMBINASE; CYCLOPAMINE; NEURONAL APOPTOSIS INHIBITORY PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR PDX 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER GROWTH; CANCER SURVIVAL; CONTROLLED STUDY; EXPERIMENTAL MODEL; GENE EXPRESSION; GENE TARGETING; GENETIC ANALYSIS; GENETIC ENGINEERING; IN VITRO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE K RAS; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE; UNINDEXED SEQUENCE;

ANIMALS; CARCINOMA, PANCREATIC DUCTAL; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HEDGEHOG PROTEINS; HUMANS; MICE; MICE, TRANSGENIC; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PANCREATIC NEOPLASMS; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TUMOR CELLS, CULTURED; UP-REGULATION; VERATRUM ALKALOIDS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 52649169761     PISSN: 00175749     EISSN: None     Source Type: Journal    
DOI: 10.1136/gut.2007.148189     Document Type: Article

References (56)

1. ACS. Cancer facts and figures 2007. American Cancer Society, 2007.
2. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2006. CA Cancer J Clin 2006;56:106-30.
3. Berman DM, Karhadkar SS, Maitra A, et al. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 2003;425:846-51.
4. Thayer SP, di Magliano MP, Heiser PW, et al. Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 2003;425:851-6.
5. Karhadkar SS, Bova GS, Abdallah N, et al. Hedgehog signalling in prostate regeneration, neoplasia and metastasis. Nature 2004;431:707-12.
6. Feldmann G, Ohara S, Fendrich V, et al. Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res 2007;67:2187-96.
7. Kelland LR. Of mice and men: values and liabilities of the athymic nude mouse model in anticancer drug development. Eur J Cancer 2004;40:827-36.
8. Bibby NIC. Orthotopic models of cancer for preclinical drug evaluation: advantages and disadvantages. Eur J Cancer 2004;40:852-7.
9. Aguirre AJ, Bardeesy N, Sinha M, et al. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev 2003;17:3112-26.
10. Lee KM, Yasuda H, Hollingsworth MA, et al. Notch 2-positive progenitors with the intrinsic ability to give rise to pancreatic ductal cells. Lab Invest 2005;85:1003-12.
11. Fendrich V, Waldmann J, Esni F, et al. Snail and Sonic Hedgehog activation in neuroendocrine tumors of the ileum. Endocr Relat Cancer 2007;14:865-74.
12. Wang X, Seed B. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 2003;31:e154.
13. Feldmann G, Nattermann J, Nischalke HD, et al. Detection of human aspartyl (asparaginyl) beta-hydroxylase and homeobox B7 mRNA in brush cytology specimens from patients with bile duct cancer. Endoscopy 2006;38:604-9.
14. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402-8.
15. Hingorani SR, Petricoin EF, Maitra A, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003;4:437-50.
16. Hruban RH, Adsay NV, Albores-Saavedra J, et al. Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations. Cancer Res 2006;66:95-106.
17. Hughes TR, Marton MJ, Jones AR, et al. Functional discovery via a compendium of expression profiles. Cell 2000;102:109-26.
18. lacobuzio-Donahue CA, Maitra A, Olsen M, et al. Exploration of global gene expression patterns in pancreatic adenocarcinoma using cDNA microarrays. Am J Pathol 2003;162:1151-62.
19. lacobuzio-Donahue CA, Maitra A, Shen-Ong GL, et al. Discovery of novel tumor markers of pancreatic cancer using global gene expression technology. Am J Pathol 2002;160:1239-49.
20. lacobuzio-Donahue CA, Ashfaq R, Maitra A, et al. Highly expressed genes in pancreatic ductal adenocarcinomas: a comprehensive characterization and comparison of the transcription profiles obtained from three major technologies. Cancer Res 2003;63:8614-22.
21. Cao D, Hustinx SR, Sui G, et al. Identification of novel highly expressed genes in pancreatic ductal adenocarcinomas through a bioinformatics analysis of expressed sequence tags. Cancer Biol Ther 2004;3:1081-9; discussion 90-1.
22. Hustinx SR, Cao D, Maitra A, et al. Differentially expressed genes in pancreatic ductal adenocarcinomas identified through serial analysis of gene expression. Cancer Biol Ther 2004;3:1254-61.
23. Missiaglia E, Blaveri E, Terris B, et al. Analysis of gene expression in cancer cell lines identifies candidate markers for pancreatic tumorigenesis and metastasis. Int J Cancer 2004;112:100-12.
24. Chen R, Yi EC, Donohoe S, et al. Pancreatic cancer proteome: the proteins that underlie invasion, metastasis, and immunologic escape. Gastroenterology 2005;129:1187-97.
25. Cmogorac-Jurcevic T, Missiaglia E, Blaveri E, et al. Molecular alterations in pancreatic carcinoma: expression profiling shows that dysregulated expression of S100 genes is highly prevalent. J Pathol 2003;201:63-74.
26. Crnogorac-Jurcevic T, Gangeswaran R, Bhakta V, et al. Proteomic analysis of chronic pancreatitis and pancreatic adenocarcinoma. Gastroenterology 2005;129:1454-63.
27. Grutzmann R, Pilarsky C, Ammerpohl O, et al. Gene expression profiling of microdissected pancreatic ductal carcinomas using high-density DNA microarrays. Neoplasia 2004;6:611-22.
28. Friess H, Ding J, Kleeff J, et al. Microarray-based identification of differentially expressed growth- and metastasis-associated genes in pancreatic cancer. Cell Mol Life Sci 2003;60:1180-99.
29. Tan ZJ, Hu XG, Cao GS, et al. Analysis of gene expression profile of pancreatic carcinoma using cDNA microarray. World J Gastroenterol 2003;9:818-23.
30. Nakamura T, Furukawa Y, Nakagawa H, et al. Genome-wide cDNA microarray analysis of gene expression profiles in pancreatic cancers using populations of tumor cells and normal ductal epithelial cells selected for purity by laser microdissection. Oncogene 2004;23:2385-400.
31. Sipos B, Moser S, Kalthoff H, et al. A comprehensive characterization of pancreatic ductal carcinoma cell lines: towards the establishment of an in vitro research platform. Virchows Arch 2003;442:444-52.
32. Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res 2007;67:1030-7.
33. Hingorani SR, Wang L, Multani AS, et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005;7:469-83.
34. Bardeesy N, Cheng KH, Berger JH, et al. Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer. Genes Dev 2006;20:3130-46.
35. Izeradjene K, Combs C, Best M, et al. Kras(G12D) and Smad4/Dpc4 haploinsufficiency cooperate to induce mucinous cystic neoplasms and invasive adenocarcinoma of the pancreas. Cancer Cell 2007;11:229- 43.
36. Ijichi H, Chytil A, Gorska AE, et al. Aggressive pancreatic ductal adenocarcinoma in mice caused by pancreas-specific blockade of transforming growth factor-beta signaling in cooperation with active Kras expression. Genes Dev 2006;20:3147-60.
37. Rakhlin EY, Rosow D, Hezel A, et al. Sonic hedgehog pathway- potential target for pancreatic adenocarcinoma treatment. J Am Coll Surg 2006;203:S46-7.
38. Ji Z, Mei FC, Xie J, et al. Oncogenic KRAS activates hedgehog signaling pathway in pancreatic cancer cells. J Biol Chem 2007;282:14048-55.
39. Morton JP, Mongeau ME, Klimstra DS, et al. Sonic hedgehog acts at multiple stages during pancreatic tumorigenesis. Proc Natl Acad Sci USA 2007;104:5103-8.
40. Han JJ, Fernandez-Zapico ME. Crosstalk between KRAS and hedgehog pathways in the regulation of GLI function in pancreatic cancer cells [abstract]. Pancreas 2006;33:466.
41. Pennica D, Swanson TA, Welsh JW, et al. WISP genes are members of the connective tissue growth factor family that are up-regulated in wnt-1-transformed cells and aberrantly expressed in human colon tumors. Proc Natl Acad Sci USA 1998;95:14717-22.
42. Pasca di Magliano M, Biankin AV, Heiser PW, et al. Common activation of canonical wnt signaling in pancreatic adenocarcinoma. PLoS ONE 2007;2:e1155.
43. Esposito I, Kleeff J, Abiatari I, et al. Overexpression of cellular inhibitor of apoptosis protein 2 is an early event in the progression of pancreatic cancer. J Clin Pathol 2007;60:885-95.
44. Liu Z, Li H, Derouet M, et al. ras Oncogene triggers up-regulation of clAP2 and XIAP in intestinal epithelial cells: epidermal growth factor receptor-dependent and -independent mechanisms of ras-induced transformation. J Biol Chem 2005;280:37383-92.
45. Nakagawa Y, Abe S, Kurata M, et al. IAP family protein expression correlates with poor outcome of multiple myeloma patients in association with chemotherapy-induced overexpression of multidrug resistance genes. Am J Hematol 2006;81:824-31.
46. Ricci MS, Kim SH, Ogi K, et al. Reduction of TRAIL-induced Mcl-1 and clAP2 by c-Myc or sorafenib sensitizes resistant human cancer cells to TRAIL-induced death. Cancer Cell 2007;12:66-80.
47. Bashyam MD, Bair R, Kim YH, et al. Array-based comparative genomic hybridization identifies localized DNA amplifications and homozygous deletions in pancreatic cancer. Neoplasia 2005;7:556-62.
48. Mann AP, Verma A, Sethi G, et al. Overexpression of tissue transglutaminase leads to constitutive activation of nuclear factor-kappaB in cancer cells: delineation of a novel pathway. Cancer Res 2006;66:8788-95.
49. Verma A, Mehta K. Transglutaminase-mediated activation of nuclear transcription factor-kappaB in cancer cells: a new therapeutic opportunity. Curr Cancer Drug Targets 2007;7:559-65.
50. Cantero D, Friess H, Deflorin J, et al. Enhanced expression of urokinase plasminogen activator and its receptor in pancreatic carcinoma. Br J Cancer 1997;75:388-95.
51. Wang W, Abbruzzese JL, Evans DB, et al. Overexpression of urokinase-type plasminogen activator in pancreatic adenocarcinoma is regulated by constitutively activated RelA. Oncogene 1999;18:4554-63.
52. Pulukuri SM, Rao JS. Small interfering RNA directed reversal of urokinase plasminogen activator demethylation inhibits prostate tumor growth and metastasis. Cancer Res 2007;67:6637-46.
53. Kleeff J, Maruyama H, Ishiwata T, et al. Bone morphogenetic protein 2 exerts diverse effects on cell growth in vitro and is expressed in human pancreatic cancer in vivo. Gastroenterology 1999;116:1202- 16.
54. Clement JH, Raida M, Sanger J, et al. Bone morphogenetic protein 2 (BMP-2] induces in vitro invasion and in vivo hormone independent growth of breast carcinoma cells. Int J Oncol 2005;27:401-7.
55. Feeley BT, Krenek L, Liu N, et al. Overexpression of noggin inhibits BMP-mediated growth of osteolytic prostate cancer lesions. Bone 2006;38:154-66.
56. Ma L, Lu MF, Schwartz RJ, et al. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 2005;132:5601-11.