Human pancreatic cancer-associated stellate cells remain activated after in vivo chemoradiation

Frontiers in Oncology

Volumn 4 MAY, Issue , 2014, Pages

  Cabrera, M Carla ^a,b   Tilahun, Estifanos ^b   Nakles, Rebecca ^b   Diaz Cruz, Edgar S ^b,c   Charabaty, Aline ^d   Suy, Simeng ^b,e   Jackson, Patrick ^e   Ley, Lisa ^b   Slack, Rebecca ^f   Jha, Reena ^e   Collins, Sean P ^b,e   Haddad, Nadim ^d   Kallakury, Bhaskar V S ^b,e   Schroeder, Timm ^g,h   Pishvaian, Michael J ^b,d,e   Furth, Priscilla A ^b,e  

^a NATIONAL CANCER INSTITUTE   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c BELMONT UNIVERSITY   (United States)

^d GEORGETOWN UNIVERSITY   (United States)

^e GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF TEXAS   (United States)

^g INSTITUTE OF EPIDEMIOLOGY   (Germany)

^h ETH ZURICH   (Switzerland)

Author keywords

Chemotherapy; Gemcitabine; Pancreatic cancer; PDAC; Radiation; Stellate cells

Indexed keywords

GEMCITABINE; GLIAL FIBRILLARY ACIDIC PROTEIN; VIMENTIN;

ARTICLE; CELL ACTIVATION; CELL INVASION; CELL MEMBRANE; CELL MOTION; CELL PROLIFERATION; CELL TRACKING; CELLULAR PARAMETERS; CHEMORADIOTHERAPY; CLINICAL TRIAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FINE NEEDLE ASPIRATION BIOPSY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MULTIPLE CYCLE TREATMENT; PANCREAS ADENOCARCINOMA; PANCREATIC STELLATE CELL; STEREOTACTIC RADIOSURGERY; TUMOR MICROENVIRONMENT;

EID: 84904649320     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00102     Document Type: Article

References (42)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin (2012) 62:10-29. doi:10.3322/caac.20138.
2. Brand RE, Tempero MA. Pancreatic cancer. Curr Opin Oncol (1998) 10:362-6. doi:10.1097/00001622-199807000-00014.
3. Hidalgo M. Pancreatic Cancer. N Engl J Med (2010) 362:1605-17. doi:10.1056/NEJMra0901557.
4. Pandol S, Edderkaoui M, Gukovsky I, Lugea A, Gukovskaya A. Desmoplasia of pancreatic ductal adenocarcinoma. Clin Gastroenterol Hepatol (2009) 7:S44-7. doi:10.1016/j.cgh.2009.07.039.
5. Guturu P, Shah V, Urrutia R. Interplay of tumor microenvironment cell types with parenchymal cells in pancreatic cancer development and therapeutic implications. J Gastrointest Cancer (2009) 40:1-9. doi:10.1007/s12029-009-9071-1.
6. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, et al. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res (2008) 68:918-26. doi:10.1158/0008-5472.CAN-07-5714.
7. Kikuta K, Masamune A, Watanabe T, Ariga H, Itoh H, Hamada S, et al. Pancreatic stellate cells promote epithelial-mesenchymal transition in pancreatic cancer cells. Biochem Biophys Res Commun (2010) 403:380-4. doi:10.1016/j.bbrc.2010.11.040.
8. Mantoni TS, Lunardi S, Al-Assar O, Masamune A, Brunner TB. Pancreatic stellate cells radioprotect pancreatic cancer cells through 1-integrin signaling. Cancer Res (2011) 71:3453-8. doi:10.1158/0008-5472.CAN-10-1633.
9. Bachem MG, Zhou S, Buck K, Schneiderhan W, Siech M. Pancreatic stellate cells-role in pancreas cancer. Langenbecks Arch Surg (2008) 393:891-900. doi:10.1007/s00423-008-0279-5.
10. Bachem MG, Schneider E, Gross H, Weidenbach H, Schmid RM, Menke A, et al. Identification, culture, and characterization of pancreatic stellate cells in rats and humans. Gastroenterology (1998) 115:421-32. doi:10.1016/S0016-5085(98)70209-4.
11. Apte MV, Haber PS, Darby SJ, Rodgers SC, McCaughan GW, Korsten MA, et al. Pancreatic stellate cells are activated by proinflammatory cytokines: implications for pancreatic fibrogenesis. Gut (1999) 44:534-41. doi:10.1136/gut.44.4.534.
12. Luttenberger T, Schmid-Kotsas A, Menke A, Siech M, Beger H, Adler G, et al. Platelet-derived growth factors stimulate proliferation and extracellular matrix synthesis of pancreatic stellate cells: implications in pathogenesis of pancreas fibrosis. Lab Invest (2000) 80:47-55. doi:10.1038/labinvest.3780007.
13. Schneider E, Schmid-Kotsas A, Zhao J, Weidenbach H, Schmid RM, Menke A, et al. Identification of mediators stimulating proliferation and matrix synthesis of rat pancreatic stellate cells. Am J Physiol Cell Physiol (2001) 281:C532-43.
14. Buniatian G, Hamprecht B, Gebhardt R. Glial fibrillary acidic protein as a marker of perisinusoidal stellate cells that can distinguish between the normal and myofibroblast-like phenotypes. Biol Cell (1996) 87:65-73. doi:10.1111/j.1768-322X.1996.tb00967.x.
15. Omary MB, Lugea A, Lowe AW, Pandol SJ. The pancreatic stellate cell: a star on the rise in pancreatic diseases. J Clin Investig (2007) 117:50-9. doi:10.1172/JCI30082.
16. Masamune A, Satoh M, Kikuta K, Suzuki N, Shimosegawa T. Endothelin-1 stimulates contraction and migration of rat pancreatic stellate cells. World J Gastroenterol (2005) 11:6144-51.
17. Phillips PA, Wu MJ, Kumar RK, Doherty E, McCarroll JA, Park S, et al. Cell migration: a novel aspect of pancreatic stellate cell biology. Gut (2003) 52:677-82. doi:10.1136/gut.52.5.677.
18. Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C. Defining the mode of tumour growth by clonal analysis. Nature (2012) 488:527-30. doi:10.1038/nature11344.
19. Chen J, Li Y, Yu T-S, McKay RM, Burns DK, Kernie SG, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature (2012) 488:522-6. doi:10.1038/nature11287.
20. Schepers AG, Snippert HJ, Stange DE, Born M, van den Es JH, van Wetering M, et al. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science (2012) 337:730-5. doi:10.1126/science.1224676.
21. Hamada S, Masamune A, Takikawa T, Suzuki N, Kikuta K, Hirota M, et al. Pancreatic stellate cells enhance stem cell-like phenotypes in pancreatic cancer cells. Biochem Biophys Res Commun (2012) 421:349-54. doi:10.1016/j.bbrc.2012.04.014.
22. Lonardo E, Frias-Aldeguer J, Hermann PC, Heeschen C. Pancreatic stellate cells form a niche for cancer stem cells and promote their self-renewal and invasiveness. Cell Cycle (2012) 11:1282-90. doi:10.4161/cc.19679.
23. Lonardo E, Cioffi M, Sancho P, Sanchez-Ripoll Y, Trabulo SM, Dorado J, et al. Metformin targets the metabolic Achilles heel of human pancreatic cancer stem cells. PLoS One (2013) 8:e76518. doi:10.1371/journal.pone.0076518.
24. Farrow B, Rowley D, Dang T, Berger DH. Characterization of tumor-derived pancreatic stellate cells. J Surg Res (2009) 157:96-102. doi:10.1016/j.jss.2009.03.064.
25. Farrow B, Albo D, Berger DH. The role of the tumor microenvironment in the progression of pancreatic cancer. J Surg Res (2008) 149:319-28. doi:10.1016/j.jss.2007.12.757.
26. Von Hoff DD, Ramanathan RK, Borad MJ, Laheru DA, Smith LS, Wood TE, et al. Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. J Clin Oncol (2011) 29:4548-54. doi:10.1200/JCO.2011.36.5742.
27. Beljaars L, Meijer DKF, Poelstra K. Targeting hepatic stellate cells for cell-specific treatment of liver fibrosis. Front Biosci (2002) 7:e214-22. doi:10.2741/beljaars.
28. Grippo P, Munshi HG. Pancreatic Cancer and Tumor Microenvironment. Transworld Research Network (2012). Available at: http://www.ncbi.nlm.nih.gov/books/NBK98930/.
29. Gurka MK, Collins SP, Slack R, Tse G, Charabaty A, Ley L, et al. Stereotactic body radiation therapy with concurrent full-dose gemcitabine for locally advanced pancreatic cancer: a pilot trial demonstrating safety. Radiat Oncol (2013) 8:44. doi:10.1186/1748-717X-8-44.
30. Nakles RE, Millman SL, Cabrera MC, Johnson P, Mueller S, Hoppe PS, et al. Time-lapse imaging of primary preneoplastic mammary epithelial cells derived from genetically engineered mouse models of breast cancer. J Vis Exp (2013). 72;:e50198. doi:10.3791/50198.
31. Eilken HM, Nishikawa S-I, Schroeder T. Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature (2009) 457:896-900. doi:10.1038/nature07760.
32. Schroeder T. Long-term single-cell imaging of mammalian stem cells. Nat Methods (2011) 8:S30-5. doi:10.1038/nmeth.1577.
33. Erkan M, Kleeff J, Gorbachevski A, Reiser C, Mitkus T, Esposito I, et al. Periostin creates a tumor-supportive microenvironment in the pancreas by sustaining fibrogenic stellate cell activity. Gastroenterology (2007) 132:1447-64. doi:10.1053/j.gastro.2007.01.031.
34. Mollenhauer J, Roether I, Kern HF. Distribution of extracellular matrix proteins in pancreatic ductal adenocarcinoma and its influence on tumor cell proliferation in vitro. Pancreas (1987) 2:14-24. doi:10.1097/00006676-198701000-00003.
35. Xu Z, Vonlaufen A, Phillips PA, Fiala-Beer E, Zhang X, Yang L, et al. Role of pancreatic stellate cells in pancreatic cancer metastasis. Am J Pathol (2010) 177:2585-96. doi:10.2353/ajpath.2010.090899.
36. Bachem MG, Schünemann M, Ramadani M, Siech M, Beger H, Buck A, et al. Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. Gastroenterology (2005) 128:907-21. doi:10.1053/j.gastro.2004.12.036.
37. Vonlaufen A, Joshi S, Qu C, Phillips PA, Xu Z, Parker NR, et al. Pancreatic stellate cells: partners in crime with pancreatic cancer cells. Cancer Res (2008) 68:2085-93. doi:10.1158/0008-5472.CAN-07-2477.
38. Lowenfels AB, Maisonneuve P, Cavallini G, Ammann RW, Lankisch PG, Andersen JR, et al. Pancreatitis and the risk of pancreatic cancer. N Engl J Med (1993) 328:1433-7.
39. Apte MV, Pirola RC, Wilson JS. Pancreatic stellate cells: a starring role in normal and diseased pancreas. Front Physiol (2012) 3:344. doi:10.3389/fphys.2012.00344.
40. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science (2009) 324:1457-61. doi:10.1126/science.1171362.
41. Lauffenburger DA, Wells A. Quantitative parsing of cell multi-tasking in wound repair and tissue morphogenesis. Biophys J (2003) 84:3499-500. doi:10.1016/S0006-3495(03)75084-X.
42. Shreiber DI, Barocas VH, Tranquillo RT. Temporal variations in cell migration and traction during fibroblast-mediated gel compaction. Biophys J (2003) 84:4102-14. doi:10.1016/S0006-3495(03)75135-2.