Key role of pancreatic stellate cells in pancreatic cancer

Cancer Letters

Volumn 381, Issue 1, 2016, Pages 194-200

  Pothula, Srinivasa P ^a,b   Xu, Zhihong ^a,b   Goldstein, David ^a   Pirola, Romano C ^a,b   Wilson, Jeremy S ^a,b   Apte, Minoti V ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b INGHAM INSTITUTE FOR APPLIED MEDICAL RESEARCH   (Australia)

Author keywords

Desmoplastic reaction; Pancreatic cancer; Pancreatic stellate cells; Stromal tumour interactions; Tumour microenvironment

Indexed keywords

ANTINEOPLASTIC AGENT; AZD 8542; CALCIPOTRIOL; ELLAGIC ACID; EMBELIN; FLUOROURACIL; FOLINIC ACID; GANCICLOVIR; GEMCITABINE; IRINOTECAN; LOSARTAN; OLMESARTAN; OXALIPLATIN; PACLITAXEL; PATIDEGIB; PIRFENIDONE; RECOMBINANT HYALURONIDASE; RETINOIC ACID; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; CANCER CELL; CANCER GROWTH; CANCER PROGNOSIS; CARCINOGENESIS; CELL INTERACTION; CELL PROLIFERATION; DRUG EFFICACY; DRUG RESISTANCE; DRUG TARGETING; ENDOTHELIUM CELL; HUMAN; IMMUNOCOMPETENT CELL; MYOFIBROBLAST; NERVE CELL; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PANCREATIC STELLATE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTON THERAPY; RADIOSENSITIVITY; SHORT SURVEY; STROMA; TUMOR MICROENVIRONMENT; ANIMAL; CELL COMMUNICATION; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; PANCREATIC NEOPLASMS; PATHOLOGY; SIGNAL TRANSDUCTION; STROMA CELL;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL COMMUNICATION; HUMANS; MOLECULAR TARGETED THERAPY; PANCREATIC NEOPLASMS; PANCREATIC STELLATE CELLS; SIGNAL TRANSDUCTION; STROMAL CELLS; TUMOR MICROENVIRONMENT;

EID: 84948799840     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.10.035     Document Type: Review

References (72)

1. [1] Jemal, A., et al. Global cancer statistics. CA Cancer J. Clin 61:2 (2011), 69–90.
2. [2] Siegel, R., et al. Cancer statistics, 2014. CA Cancer J. Clin 64:1 (2014), 9–29.
3. [3] Rahib, L., et al. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res 74:11 (2014), 2913–2921.
4. [4] Apte, M.V., et al. Pancreatic cancer: the microenvironment needs attention too!. Pancreatology 15:Suppl. 4 (2015), S32–S38.
5. [5] Apte, M.V., et al. Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas 29:3 (2004), 179–187.
6. [6] Apte, M.V., et al. A starring role for stellate cells in the pancreatic cancer microenvironment. Gastroenterology 144:6 (2013), 1210–1219.
7. [7] Gore, J., Korc, M., Pancreatic cancer stroma: friend or foe?. Cancer Cell 25:6 (2014), 711–712.
8. [8] Erkan, M., et al. The activated stroma index is a novel and independent prognostic marker in pancreatic ductal adenocarcinoma. Clin. Gastroenterol. Hepatol 6:10 (2008), 1155–1161.
9. [9] Mantoni, T.S., et al. Stromal SPARC expression and patient survival after chemoradiation for non-resectable pancreatic adenocarcinoma. Cancer Biol. Ther 7:11 (2008), 1806–1815.
10. [10] Erkan, M., et al. Periostin creates a tumor-supportive microenvironment in the pancreas by sustaining fibrogenic stellate cell activity. Gastroenterology 132:4 (2007), 1447–1464.
11. [11] Bever, K.M., et al. The prognostic value of stroma in pancreatic cancer in patients receiving adjuvant therapy. HPB (Oxford) 17:4 (2015), 292–298.
12. [12] Ozdemir, B.C., et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 25:6 (2014), 719–734.
13. [13] Binkley, C.E., et al. The molecular basis of pancreatic fibrosis: common stromal gene expression in chronic pancreatitis and pancreatic adenocarcinoma. Pancreas 29:4 (2004), 254–263.
14. [14] Fukushima, N., et al. Periostin deposition in the stroma of invasive and intraductal neoplasms of the pancreas. Mod. Pathol 21:8 (2008), 1044–1053.
15. [15] Apte, M.V., Pirola, R.C., Wilson, J.S., Pancreatic stellate cells: a starring role in normal and diseased pancreas. Front. Physiol, 3, 2012, 344.
16. [16] Jaster, R., et al. Extracellular signal regulated kinases are key mediators of mitogenic signals in rat pancreatic stellate cells. Gut 51:4 (2002), 579–584.
17. [17] Masamune, A., Kume, K., Shimosegawa, T., [Pancreatitis-associated genes and development of pancreatic cancer]. Nihon Shokakibyo Gakkai Zasshi 106:8 (2009), 1147–1155.
18. [18] McCarroll, J.A., et al. Pancreatic stellate cell migration: role of the phosphatidylinositol 3-kinase(PI3-kinase) pathway. Biochem. Pharmacol 67:6 (2004), 1215–1225.
19. [19] Shinozaki, S., et al. Indian hedgehog promotes the migration of rat activated pancreatic stellate cells by increasing membrane type-1 matrix metalloproteinase on the plasma membrane. J. Cell. Physiol 216:1 (2008), 38–46.
20. [20] Ohnishi, H., et al. Distinct roles of Smad2-, Smad3-, and ERK-dependent pathways in transforming growth factor-beta1 regulation of pancreatic stellate cellular functions. J. Biol. Chem 279:10 (2004), 8873–8878 Epub 2003 Dec 18.
21. [21] Gukovskaya, A.S., et al. Ethanol metabolism and transcription factor activation in pancreatic acinar cells in rats. Gastroenterology 122:1 (2002), 106–118.
22. [22] McCarroll, J.A., et al. Pancreatic stellate cell activation by ethanol and acetaldehyde: is it mediated by the mitogen-activated protein kinase signaling pathway?. Pancreas 27:2 (2003), 150–160.
23. [23] Masamune, A., et al. Pancreatic stellate cells express Toll-like receptors. J. Gastroenterol 43:5 (2008), 352–362.
24. [24] Masamune, A., et al. Rho kinase inhibitors block activation of pancreatic stellate cells. Br. J. Pharmacol 140:7 (2003), 1292–1302.
25. [25] Hennigs, J.K., et al. Molecular basis of P2-receptor-mediated calcium signaling in activated pancreatic stellate cells. Pancreas 40:5 (2011), 740–746.
26. [26] Masamune, A., et al. Alteration of the microRNA expression profile during the activation of pancreatic stellate cells. Scand. J. Gastroenterol 49:3 (2014), 323–331.
27. [27] Shen, J., et al. miR-15b and miR-16 induce the apoptosis of rat activated pancreatic stellate cells by targeting Bcl-2 in vitro. Pancreatology 12:2 (2012), 91–99.
28. [28] Shimizu, K., et al. Troglitazone inhibits the progression of chronic pancreatitis and the profibrogenic activity of pancreatic stellate cells via a PPARgamma-independent mechanism. Pancreas 29:1 (2004), 67–74.
29. [29] Hwang, R.F., et al. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 68:3 (2008), 918–926.
30. [30] Kikuta, K., et al. Pancreatic stellate cells promote epithelial-mesenchymal transition in pancreatic cancer cells. Biochem. Biophys. Res. Commun 403:3–4 (2010), 380–384.
31. [31] Mantoni, T.S., et al. Pancreatic stellate cells radioprotect pancreatic cancer cells through beta1-integrin signaling. Cancer Res 71:10 (2011), 3453–3458.
32. [32] Hamada, S., et al. Pancreatic stellate cells enhance stem cell-like phenotypes in pancreatic cancer cells. Biochem. Biophys. Res. Commun 421:2 (2012), 349–354.
33. [33] Pandol, S., et al. Epidemiology, risk factors, and the promotion of pancreatic cancer: role of the stellate cell. J. Gastroenterol. Hepatol 27:Suppl. 2 (2012), 127–134.
34. [34] Yoshida, S., et al. Pancreatic stellate cells (PSCs) express cyclooxygenase-2 (COX-2) and pancreatic cancer stimulates COX-2 in PSCs. Mol. Cancer, 4, 2005, 27.
35. [35] Kiss, K., et al. Chronic hyperglycemia induces trans-differentiation of human pancreatic stellate cells and enhances the malignant molecular communication with human pancreatic cancer cells. PLoS ONE, 10(5), 2015 e0128059.
36. [36] Ikenaga, N., et al. CD10+ pancreatic stellate cells enhance the progression of pancreatic cancer. Gastroenterology 139:3 (2010), 1041–1051 1051 e1-8.
37. [37] Hwang, R.F., et al. Inhibition of the hedgehog pathway targets the tumor-associated stroma in pancreatic cancer. Mol. Cancer Res 10:9 (2012), 1147–1157.
38. [38] Gao, Z., et al. Pancreatic stellate cells increase the invasion of human pancreatic cancer cells through the stromal cell-derived factor-1/CXCR4 axis. Pancreatology 10:2–3 (2010), 186–193.
39. [39] Masamune, A., et al. Hypoxia stimulates pancreatic stellate cells to induce fibrosis and angiogenesis in pancreatic cancer. Am. J. Physiol. Gastrointest. Liver Physiol 295:4 (2008), G709–G717.
40. [40] Xu, Z., et al. Role of pancreatic stellate cells in pancreatic cancer metastasis. Am. J. Pathol 177:5 (2010), 2585–2596.
41. [41] Brammer, R.D., Bramhall, S.R., Eggo, M.C., Endostatin expression in pancreatic tissue is modulated by elastase. Br. J. Cancer 92:1 (2005), 89–93.
42. [42] Patel, M.B., et al. The role of the hepatocyte growth factor/c-MET pathway in pancreatic stellate cell-endothelial cell interactions: antiangiogenic implications in pancreatic cancer. Carcinogenesis 35:8 (2014), 1891–1900.
43. [43] Ene-Obong, A., et al. Activated pancreatic stellate cells sequester CD8+ T-cells to reduce their infiltration of the juxtatumoral compartment of pancreatic ductal adenocarcinoma. Gastroenterology 145 (2013), 1121–1132.
44. [44] Mace, T.A., et al. Pancreatic cancer-associated stellate cells promote differentiation of myeloid-derived suppressor cells in a STAT3-dependent manner. Cancer Res 73:10 (2013), 3007–3018.
45. [45] Ma, Y., et al. Dynamic mast cell-stromal cell interactions promote growth of pancreatic cancer. Cancer Res 73:13 (2013), 3927–3937.
46. [46] Tang, D., et al. High expression of Galectin-1 in pancreatic stellate cells plays a role in the development and maintenance of an immunosuppressive microenvironment in pancreatic cancer. Int. J. Cancer 130:10 (2012), 2337–2348.
47. [47] Shi, C., et al. Fibrogenesis in pancreatic cancer is a dynamic process regulated by macrophage-stellate cell interaction. Lab. Invest 94:4 (2014), 409–421.
48. [48] Kraman, M., et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 330:6005 (2010), 827–830.
49. [49] Li, X., et al. Sonic hedgehog paracrine signaling activates stromal cells to promote perineural invasion in pancreatic cancer. Clin. Cancer Res 20:16 (2014), 4326–4338.
50. [50] Omary, M.B., et al. The pancreatic stellate cell: a star on the rise in pancreatic diseases. J. Clin. Invest 117:1 (2007), 50–59.
51. [51] Kikuta, K., et al. Pancreatic stellate cells reduce insulin expression and induce apoptosis in pancreatic beta-cells. Biochem. Biophys. Res. Commun 433:3 (2013), 292–297.
52. [52] Watanabe, I., et al. Advanced pancreatic ductal cancer: fibrotic focus and beta-catenin expression correlate with outcome. Pancreas 26:4 (2003), 326–333.
53. [53] Bachem, M.G., et al. Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. Gastroenterology 128:4 (2005), 907–921.
54. [54] Vonlaufen, A., et al. Pancreatic stellate cells: partners in crime with pancreatic cancer cells. Cancer Res 68:7 (2008), 2085–2093.
55. [55] Xu, Z., et al. Pancreatic cancer and its stroma: a conspiracy theory. World J. Gastroenterol 20:32 (2014), 11216–11229.
56. [56] Duda, D.G., et al. Malignant cells facilitate lung metastasis by bringing their own soil. Proc. Natl. Acad. Sci. U.S.A. 107:50 (2010), 21677–21682.
57. [57] Hingorani, S.R., et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 7:5 (2005), 469–483.
58. [58] Ijichi, H., et al. Inhibiting Cxcr2 disrupts tumor-stromal interactions and improves survival in a mouse model of pancreatic ductal adenocarcinoma. J. Clin. Invest 121:10 (2011), 4106–4117.
59. [59] Olive, K.P., et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324:5933 (2009), 1457–1461.
60. [60] Provenzano, P.P., et al. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 21:3 (2012), 418–429.
61. [61] Chang, D.Z., et al. Mast cells in tumor microenvironment promotes the in vivo growth of pancreatic ductal adenocarcinoma. Clin. Cancer Res 17:22 (2011), 7015–7023.
62. [62] Feldmann, G., et al. Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res 67:5 (2007), 2187–2196.
63. [63] Von Hoff, D.D., et al. Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. J. Clin. Oncol 29:34 (2011), 4548–4554.
64. [64] Masamune, A., et al. The angiotensin II type I receptor blocker olmesartan inhibits the growth of pancreatic cancer by targeting stellate cell activities in mice. Scand. J. Gastroenterol 48:5 (2013), 602–609.
65. [65] Chauhan, V.P., et al. Angiotensin inhibition enhances drug delivery and potentiates chemotherapy by decompressing tumour blood vessels. Nat. Commun, 4, 2013, 2516.
66. [66] Kozono, S., et al. Pirfenidone inhibits pancreatic cancer desmoplasia by regulating stellate cells. Cancer Res 73:7 (2013), 2345–2356.
67. [67] Froeling, F.E., et al. Retinoic acid-induced pancreatic stellate cell quiescence reduces paracrine Wnt-beta-catenin signaling to slow tumor progression. Gastroenterology 141:4 (2011), 1486–1497 1497 e1-14.
68. [68] Sherman, M.H., et al. Vitamin D receptor-mediated stromal reprogramming suppresses pancreatitis and enhances pancreatic cancer therapy. Cell 159:1 (2014), 80–93.
69. [69] Von Hoff, D.D., et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N. Engl. J. Med 369:18 (2013), 1691–1703.
70. [70] Beatty, G.L., et al. A phase I study of an agonist CD40 monoclonal antibody (CP-870,893) in combination with gemcitabine in patients with advanced pancreatic ductal adenocarcinoma. Clin. Cancer Res 19:22 (2013), 6286–6295.
71. [71] Rhim, A.D., et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 25:6 (2014), 735–747.
72. [72] Edderkaoui, M., et al. Ellagic acid and embelin affect key cellular components of pancreatic adenocarcinoma, cancer, and stellate cells. Nutr. Cancer 65:8 (2013), 1232–1244.