Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma

Cancer Cell

Volumn 25, Issue 6, 2014, Pages 735-747

  Rhim, Andrew D ^a,b   Oberstein, Paul E ^c   Thomas, Dafydd H ^c   Mirek, Emily T ^b   Palermo, Carmine F ^c   Sastra, Stephen A ^c   Dekleva, Erin N ^b   Saunders, Tyler ^d   Becerra, Claudia P ^c   Tattersall, Ian W ^c   Westphalen, C Benedikt ^c   Kitajewski, Jan ^c   Fernandez Barrena, Maite G ^e   Fernandez Zapico, Martin E ^e   Iacobuzio Donahue, Christine ^d   Olive, Kenneth P ^c   Stanger, Ben Z ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c NewYork Presbyterian Hospital   (United States)

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

^e MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOCKING ANTIBODY; SONIC HEDGEHOG PROTEIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; HISTOPATHOLOGY; MOUSE; MOUSE MODEL; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VASCULARIZATION;

ERINACEIDAE; MUS;

ANIMALS; ANTIBODIES, MONOCLONAL; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GENE KNOCKDOWN TECHNIQUES; HEDGEHOG PROTEINS; HUMANS; IMMUNOGLOBULIN G; MICE; MICE, TRANSGENIC; PANCREATIC NEOPLASMS; RANDOM ALLOCATION; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SIGNAL TRANSDUCTION; STROMAL CELLS;

EID: 84902435628     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2014.04.021     Document Type: Article

References (41)

1. Bailey J.M., Swanson B.J., Hamada T., Eggers J.P., Singh P.K., Caffery T., Ouellette M.M., Hollingsworth M.A. Sonic hedgehog promotes desmoplasia in pancreatic cancer. Clin. Cancer Res. 2008, 14:5995-6004.
2. Brownell I., Guevara E., Bai C.B., Loomis C.A., Joyner A.L. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 2011, 8:552-565.
3. Chu G.C., Kimmelman A.C., Hezel A.F., DePinho R.A. Stromal biology of pancreatic cancer. J.Cell. Biochem. 2007, 101:887-907.
4. El-Zaatari M., Kao J.Y., Tessier A., Bai L., Hayes M.M., Fontaine C., Eaton K.A., Merchant J.L. Gli1 deletion prevents Helicobacter-induced gastric metaplasia and expansion of myeloid cell subsets. PLoS ONE 2013, 8:e58935.
5. Engels B., Rowley D.A., Schreiber H. Targeting stroma to treat cancers. Semin. Cancer Biol. 2012, 22:41-49.
6. Feldmann G., Fendrich V., McGovern K., Bedja D., Bisht S., Alvarez H., Koorstra J.B., Habbe N., Karikari C., Mullendore M., et al. An orally bioavailable small-molecule inhibitor of Hedgehog signaling inhibits tumor initiation and metastasis in pancreatic cancer. Mol. Cancer Ther. 2008, 7:2725-2735.
7. Feldmann G., Habbe N., Dhara S., Bisht S., Alvarez H., Fendrich V., Beaty R., Mullendore M., Karikari C., Bardeesy N., et al. Hedgehog inhibition prolongs survival in a genetically engineered mouse model of pancreatic cancer. Gut 2008, 57:1420-1430.
8. Han S.S., Jang J.Y., Kim S.W., Kim W.H., Lee K.U., Park Y.H. Analysis of long-term survivors after surgical resection for pancreatic cancer. Pancreas 2006, 32:271-275.
9. Hanahan D., Weinberg R.A. Hallmarks of cancer: The next generation. Cell 2011, 144:646-674.
10. Hingorani S.R., Wang L., Multani A.S., Combs C., Deramaudt T.B., Hruban R.H., Rustgi A.K., Chang S., Tuveson D.A. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005, 7:469-483.
11. Hwang R.F., Moore T., Arumugam T., Ramachandran V., Amos K.D., Rivera A., Ji B., Evans D.B., Logsdon C.D. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 2008, 68:918-926.
12. Iacobuzio-Donahue C.A., Fu B., Yachida S., Luo M., Abe H., Henderson C.M., Vilardell F., Wang Z., Keller J.W., Banerjee P., et al. DPC4 gene status of the primary carcinoma correlates with patterns of failure in patients with pancreatic cancer. J.Clin. Oncol. 2009, 27:1806-1813.
13. Ikenaga N., Ohuchida K., Mizumoto K., Cui L., Kayashima T., Morimatsu K., Moriyama T., Nakata K., Fujita H., Tanaka M. CD10+ pancreatic stellate cells enhance the progression of pancreatic cancer. Gastroenterology 2010, 139:1041-1051.
14. Jacobetz M.A., Chan D.S., Neesse A., Bapiro T.E., Cook N., Frese K.K., Feig C., Nakagawa T., Caldwell M.E., Zecchini H.I., et al. Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer. Gut 2013, 62:112-120.
15. Jimeno A., Weiss G.J., Miller W.H., Gettinger S., Eigl B.J., Chang A.L., Dunbar J., Devens S., Faia K., Skliris G., et al. Phase I study of the hedgehog pathway inhibitor IPI-926 in adult patients with solid tumors. Clin. Cancer Res. 2013, 19:2766-2774.
16. Kindler H.L., Niedzwiecki D., Hollis D., Sutherland S., Schrag D., Hurwitz H., Innocenti F., Mulcahy M.F., O'Reilly E., Wozniak T.F., et al. Gemcitabine plus bevacizumab compared with gemcitabine plus placebo in patients with advanced pancreatic cancer: Phase III trial of the Cancer and Leukemia Group B (CALGB 80303). J.Clin. Oncol. 2010, 28:3617-3622.
17. Klein G. Evolutionary aspects of cancer resistance. Semin. Cancer Biol. 2014, 25C:10-14.
18. Kondo Y., Kanzawa T., Sawaya R., Kondo S. The role of autophagy in cancer development and response to therapy. Nat. Rev. Cancer 2005, 5:726-734.
19. Lonardo E., Frias-Aldeguer J., Hermann P.C., Heeschen C. Pancreatic stellate cells form a niche for cancer stem cells and promote their self-renewal and invasiveness. Cell Cycle 2012, 11:1282-1290.
20. Mao J., Ligon K.L., Rakhlin E.Y., Thayer S.P., Bronson R.T., Rowitch D., McMahon A.P. A novel somatic mouse model to survey tumorigenic potential applied to the Hedgehog pathway. Cancer Res. 2006, 66:10171-10178.
21. Mills L.D., Zhang Y., Marler R.J., Herreros-Villanueva M., Zhang L., Almada L.L., Couch F., Wetmore C., Pasca di Magliano M., Fernandez-Zapico M.E. 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.
22. Morton J.P., Mongeau M.E., Klimstra D.S., Morris J.P., Lee Y.C., Kawaguchi Y., Wright C.V., Hebrok M., Lewis B.C. Sonic hedgehog acts at multiple stages during pancreatic tumorigenesis. Proc. Natl. Acad. Sci. USA 2007, 104:5103-5108.
23. Nolan-Stevaux O., Lau J., Truitt M.L., Chu G.C., Hebrok M., Fernández-Zapico M.E., Hanahan D. GLI1 is regulated through Smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation. Genes Dev. 2009, 23:24-36.
24. Olive K.P., Jacobetz M.A., Davidson C.J., Gopinathan A., McIntyre D., Honess D., Madhu B., Goldgraben M.A., Caldwell M.E., Allard D., et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009, 324:1457-1461.
25. Pasca di Magliano M., Sekine S., Ermilov A., Ferris J., Dlugosz A.A., Hebrok M. Hedgehog/Ras interactions regulate early stages of pancreatic cancer. Genes Dev. 2006, 20:3161-3173.
26. Provenzano P.P., Cuevas C., Chang A.E., Goel V.K., Von Hoff D.D., Hingorani S.R. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 2012, 21:418-429.
27. Rhim A.D., Mirek E.T., Aiello N.M., Maitra A., Bailey J.M., McAllister F., Reichert M., Beatty G.L., Rustgi A.K., Vonderheide R.H., et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012, 148:349-361.
28. Roberts D.J., Smith D.M., Goff D.J., Tabin C.J. Epithelial-mesenchymal signaling during the regionalization of the chick gut. Development 1998, 125:2791-2801.
29. Sastra S.A., Olive K.P. Quantification of murine pancreatic tumors by high-resolution ultrasound. Methods Mol. Biol. 2013, 980:249-266.
30. Singh A., Greninger P., Rhodes D., Koopman L., Violette S., Bardeesy N., Settleman J. A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell 2009, 15:489-500.
31. Singh M., Lima A., Molina R., Hamilton P., Clermont A.C., Devasthali V., Thompson J.D., Cheng J.H., Bou Reslan H., Ho C.C., et al. Assessing therapeutic responses in Kras mutant cancers using genetically engineered mouse models. Nat. Biotechnol. 2010, 28:585-593.
32. Stoker M.G., Shearer M., O'Neill C. Growth inhibition of polyoma-transformed cells by contact with static normal fibroblasts. J.Cell Sci. 1966, 1:297-310.
33. Sukegawa A., Narita T., Kameda T., Saitoh K., Nohno T., Iba H., Yasugi S., Fukuda K. The concentric structure of the developing gut is regulated by Sonic hedgehog derived from endodermal epithelium. Development 2000, 127:1971-1980.
34. Thayer S.P., di Magliano M.P., Heiser P.W., Nielsen C.M., Roberts D.J., Lauwers G.Y., Qi Y.P., Gysin S., Fernández-del Castillo C., Yajnik V., et al. Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 2003, 425:851-856.
35. Theunissen J.W., de Sauvage F.J. Paracrine Hedgehog signaling in cancer. Cancer Res. 2009, 69:6007-6010.
36. Tian H., Callahan C.A., DuPree K.J., Darbonne W.C., Ahn C.P., Scales S.J., de Sauvage F.J. Hedgehog signaling is restricted to the stromal compartment during pancreatic carcinogenesis. Proc. Natl. Acad. Sci. USA 2009, 106:4254-4259.
37. Vonlaufen A., Phillips P.A., Xu Z., Goldstein D., Pirola R.C., Wilson J.S., Apte M.V. Pancreatic stellate cells and pancreatic cancer cells: An unholy alliance. Cancer Res. 2008, 68:7707-7710.
38. Walter K., Omura N., Hong S.M., Griffith M., Vincent A., Borges M., Goggins M. Overexpression of Smoothened activates the sonic hedgehog signaling pathway in pancreatic cancer-associated fibroblasts. Clin. Cancer Res. 2010, 16:1781-1789.
39. Watanabe S., Ueda Y., Akaboshi S., Hino Y., Sekita Y., Nakao M. HMGA2 maintains oncogenic RAS-induced epithelial-mesenchymal transition in human pancreatic cancer cells. Am. J. Pathol. 2009, 174:854-868.
40. Xu Z., Vonlaufen A., Phillips P.A., Fiala-Beer E., Zhang X., Yang L., Biankin A.V., Goldstein D., Pirola R.C., Wilson J.S., Apte M.V. Role of pancreatic stellate cells in pancreatic cancer metastasis. Am. J. Pathol. 2010, 177:2585-2596.
41. Yonemasu H., Takashima M., Nishiyama K.I., Ueki T., Yao T., Tanaka M., Tsuneyoshi M. Phenotypical characteristics of undifferentiated carcinoma of the pancreas: A comparison with pancreatic ductal adenocarcinoma and relevance of E-cadherin, alpha catenin and beta catenin expression. Oncol. Rep. 2001, 8:745-752.