The vitamin D analog, MART-10, represses metastasis potential via downregulation of epithelial-mesenchymal transition in pancreatic cancer cells

Cancer Letters

Volumn 354, Issue 2, 2014, Pages 235-244

  Chiang, Kun Chun ^a   Yeh, Chun Nan ^a   Hsu, Jun Te ^a   Jan, Yi Yin ^a   Chen, Li Wei ^a   Kuo, Sheng Fong ^a   Takano, Masashi ^b   Kittaka, Atsushi ^b   Chen, Tai C ^c   Chen, Wen Tsung ^d   Pang, Jong Hwei S ^e   Yeh, Ta Sen ^a   Juang, Horng Heng ^e  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^b TEIKYO UNIVERSITY   (Japan)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL KAOHSIUNG UNIVERSITY OF HOSPITALITY AND TOURISM   (Taiwan)

^e CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

BxPC 3; EMT; MART 10; Metastasis; Pancreatic cancer; Vitamin D analog

Indexed keywords

19 NOR 2ALPHA (3 HYDROXYPROPYL) 1ALPHA,25(OH)2D3; 1ALPHA,25(OH)2D3; CADHERIN; F ACTIN; GELATINASE A; GELATINASE B; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; VIMENTIN; VITAMIN D DERIVATIVE; 19-NOR-2-(3-HYDROXYPROPYL)-1,25-DIHYDROXYVITAMIN D3; ANTINEOPLASTIC AGENT; CDH2 PROTEIN, HUMAN; COLECALCIFEROL; COLLAGENASE 3; LEUKOCYTE ANTIGEN; MMP13 PROTEIN, HUMAN; MMP2 PROTEIN, HUMAN; MMP9 PROTEIN, HUMAN;

ARTICLE; BXPC 3 CELL; CANCER CELL; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; DRUG POTENCY; ENZYME RELEASE; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; METASTASIS INHIBITION; PANC CELL; PANCREAS CANCER; PANCREATIC CANCER CELL LINE; PHARMACOLOGICAL BLOCKING; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; WESTERN BLOTTING; ZYMOGRAPHY; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; CELL MOTION; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; METASTASIS; PANCREATIC NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

ANTIGENS, CD; ANTINEOPLASTIC AGENTS; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; CHOLECALCIFEROL; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; NEOPLASM METASTASIS; PANCREATIC NEOPLASMS;

EID: 84907985408     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.08.019     Document Type: Article

References (56)

1. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J. Clin 2013, 63:11-30.
2. Pour P.M. The silent killer. Int. J. Pancreatol 1991, 10:103-104.
3. Jemal A., Siegel R., Ward E., Murray T., Xu J., Thun M.J. Cancer statistics, 2007. CA Cancer J. Clin 2007, 57:43-66.
4. Haller D.G. New perspectives in the management of pancreas cancer. Semin. Oncol 2003, 30:3-10.
5. Trede M., Schwall G., Saeger H.D. Survival after pancreatoduodenectomy. 118 consecutive resections without an operative mortality. Ann. Surg 1990, 211:447-458.
6. Yeo C.J., Cameron J.L., Sohn T.A., Lillemoe K.D., Pitt H.A., Talamini M.A., et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Ann. Surg 1997, 226:248-257. discussion 257-260.
7. Nitecki S.S., Sarr M.G., Colby T.V., van Heerden J.A. Long-term survival after resection for ductal adenocarcinoma of the pancreas. Is it really improving?. Ann. Surg 1995, 221:59-66.
8. Chiang K.C., Yeh C.N., Hsu J.T., Yeh T.S., Jan Y.Y., Wu C.T., et al. Evaluation of the potential therapeutic role of a new generation of vitamin D analog, MART-10, in human pancreatic cancer cells in vitro and in vivo. Cell Cycle 2013, 12:1316-1325.
9. Krishnan A.V., Feldman D. Mechanisms of the anti-cancer and anti-inflammatory actions of vitamin D. Annu. Rev. Pharmacol. Toxicol 2011, 51:311-336.
10. Flanagan J.N., Zheng S., Chiang K.C., Kittaka A., Sakaki T., Nakabayashi S., et al. Evaluation of 19-nor-2alpha-(3-hydroxypropyl)-1alpha,25-dihydroxyvitamin D3 as a therapeutic agent for androgen-dependent prostate cancer. Anticancer Res 2009, 29:3547-3553.
11. Iglesias-Gato D., Zheng S., Flanagan J.N., Jiang L., Kittaka A., Sakaki T., et al. Substitution at carbon 2 of 19-nor-1alpha,25-dihydroxyvitamin D3 with 3-hydroxypropyl group generates an analogue with enhanced chemotherapeutic potency in PC-3 prostate cancer cells. J. Steroid Biochem. Mol. Biol 2011, 127:269-275.
12. Chiang K.C., Yeh C.N., Chen H.Y., Lee J.M., Juang H.H., Chen M.F., et al. 19-Nor-2alpha-(3-hydroxypropyl)-1alpha,25-dihydroxyvitamin D3 (MART-10) is a potent cell growth regulator with enhanced chemotherapeutic potency in liver cancer cells. Steroids 2011, 76:1513-1519.
13. Chiang K.C., Yeh C.N., Hsu J.T., Chen L.W., Kuo S.F., Sun C.C., et al. MART-10, a novel vitamin D analog, inhibits head and neck squamous carcinoma cells growth through cell cycle arrest at G0/G1 with upregulation of p21 and p27 and downregulation of telomerase. J. Steroid Biochem. Mol. Biol 2013, 138:427-434.
14. Chiang K.C., Yeh C.N., Chen S.C., Shen S.C., Hsu J.T., Yeh T.S., et al. MART-10, a new generation of vitamin D analog, is more potent than 1alpha,25-dihydroxyvitamin D(3) in inhibiting cell proliferation and inducing apoptosis in ER+ MCF-7 breast cancer cells. Evid. Based Complement. Altern. Med. eCAM 2012, 2012:310872.
15. Chiang K.C., Chen S.C., Yeh C.N., Pang J.H., Shen S.C., Hsu J.T., et al. MART-10, a less calcemic vitamin D analog, is more potent than 1alpha,25-dihydroxyvitamin D3 in inhibiting the metastatic potential of MCF-7 breast cancer cells in vitro. J. Steroid Biochem. Mol. Biol 2014, 139:54-60.
16. Bouillon R., Verstuyf A., Verlinden L., Allewaert K., Branisteanu D., Mathieu C., et al. Non-hypercalcemic pharmacological aspects of vitamin D analogs. Biochem. Pharmacol 1995, 50:577-583.
17. Guyton K.Z., Kensler T.W., Posner G.H. Cancer chemoprevention using natural vitamin D and synthetic analogs. Annu. Rev. Pharmacol. Toxicol 2001, 41:421-442.
18. Kittaka A., Yoshida A., Chiang K.C., Takano M., Sawada D., Sakaki T., et al. Potent 19-norvitamin D analogs for prostate and liver cancer therapy. Future Med. Chem 2012, 4:2049-2065.
19. Zugmaier G., Jager R., Grage B., Gottardis M.M., Havemann K., Knabbe C. Growth-inhibitory effects of vitamin D analogues and retinoids on human pancreatic cancer cells. Br. J. Cancer 1996, 73:1341-1346.
20. Kawa S., Nikaido T., Aoki Y., Zhai Y., Kumagai T., Furihata K., et al. Vitamin D analogues up-regulate p21 and p27 during growth inhibition of pancreatic cancer cell lines. Br. J. Cancer 1997, 76:884-889.
21. Kawa S., Yoshizawa K., Tokoo M., Imai H., Oguchi H., Kiyosawa K., et al. Inhibitory effect of 220-oxa-1,25-dihydroxyvitamin D3 on the proliferation of pancreatic cancer cell lines. Gastroenterology 1996, 110:1605-1613.
22. Pettersson F., Colston K.W., Dalgleish A.G. Differential and antagonistic effects of 9-cis-retinoic acid and vitamin D analogues on pancreatic cancer cells in vitro. Br. J. Cancer 2000, 83:239-245.
23. Colston K.W., James S.Y., Ofori-Kuragu E.A., Binderup L., Grant A.G. Vitamin D receptors and anti-proliferative effects of vitamin D derivatives in human pancreatic carcinoma cells in vivo and in vitro. Br. J. Cancer 1997, 76:1017-1020.
24. Schwartz G.G., Eads D., Naczki C., Northrup S., Chen T., Koumenis C. 19-nor-1 alpha,25-dihydroxyvitamin D2 (paricalcitol) inhibits the proliferation of human pancreatic cancer cells in vitro and in vivo. Cancer Biol. Ther 2008, 7:430-436.
25. Evans T.R., Colston K.W., Lofts F.J., Cunningham D., Anthoney D.A., Gogas H., et al. A phase II trial of the vitamin D analogue seocalcitol (EB1089) in patients with inoperable pancreatic cancer. Br. J. Cancer 2002, 86:680-685.
26. Napoli J.L., Sommerfeld J.L., Pramanik B.C., Gardner R., Sherry A.D., Partridge J.J., et al. 19-nor-10-ketovitamin D derivatives: unique metabolites of vitamin D3, vitamin D2, and 25-hydroxyvitamin D3. Biochemistry 1983, 22:3636-3640.
27. Perlman K.L., Sicinski R.R., Schnoes H.K., DeLuca H.F. 1a,25-dihydroxy-19-norvitamin D3, a novel vitamin D-related compound with potential therapeutic activity. Tetra. Lett 1990, 31:1823-1824.
28. Kittaka A., Saito N., Honzawa S., Takenouchi K., Ishizuka S., Chen T.C., et al. Creative synthesis of novel vitamin D analogs for health and disease. J. Steroid Biochem. Mol. Biol 2007, 103:269-276.
29. Ono K., Yoshida A., Saito N., Fujishima T., Honzawa S., Suhara Y., et al. Efficient synthesis of 2-modified 1alpha,25-dihydroxy-19-norvitamin D3 with Julia olefination: high potency in induction of differentiation on HL-60 cells. J. Org. Chem 2003, 68:7407-7415.
30. Chen T.C., Persons K.S., Zheng S., Mathieu J., Holick M.F., Lee Y.F., et al. Evaluation of C-2-substituted 19-nor-1alpha,25-dihydroxyvitamin D3 analogs as therapeutic agents for prostate cancer. J. Steroid Biochem. Mol. Biol 2007, 103:717-720.
31. Tsai M.J., O'Malley B.W. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem 1994, 63:451-486.
32. Ramagopalan S.V., Heger A., Berlanga A.J., Maugeri N.J., Lincoln M.R., Burrell A., et al. A ChIP-seq defined genome-wide map of vitamin D receptor binding: associations with disease and evolution. Genome Res 2010, 20:1352-1360.
33. Cross H.S., Kallay E. Regulation of the colonic vitamin D system for prevention of tumor progression: an update. Future Oncol 2009, 5:493-507.
34. Welsh J. Cellular and molecular effects of vitamin D on carcinogenesis. Arch. Biochem. Biophys 2012, 523:107-114.
35. Deeb K.K., Trump D.L., Johnson C.S. Vitamin D signalling pathways in cancer: potential for anticancer therapeutics. Nat. Rev. Cancer 2007, 7:684-700.
36. Hourai S., Fujishima T., Kittaka A., Suhara Y., Takayama H., Rochel N., et al. Probing a water channel near the A-ring of receptor-bound 1 alpha,25-dihydroxyvitamin D3 with selected 2 alpha-substituted analogues. J. Med. Chem 2006, 49:5199-5205.
37. Suhara Y., Nihei K.I., Kurihara M., Kittaka A., Yamaguchi K., Fujishima T., et al. Efficient and versatile synthesis of novel 2alpha-substituted 1alpha,25-dihydroxyvitamin D(3) analogues and their docking to vitamin D receptors. J. Org. Chem 2001, 66:8760-8771.
38. Koli K., Keski-Oja J. 1alpha,25-dihydroxyvitamin D3 and its analogues down-regulate cell invasion-associated proteases in cultured malignant cells. Cell Growth Differ 2000, 11:221-229.
39. Baker A., Wood C.L., Wood A.M., Timms P., Allsopp A.J. Changes in vitamin D and matrix metalloproteinase-9 in submariners during a submerged patrol. Occup. Environ. Med 2014, 71:104-108.
40. Timms P.M., Mannan N., Hitman G.A., Noonan K., Mills P.G., Syndercombe-Court D., et al. Circulating MMP9, vitamin D and variation in the TIMP-1 response with VDR genotype: mechanisms for inflammatory damage in chronic disorders?. QJM 2002, 95:787-796.
41. Kim J.B., Islam S., Kim Y.J., Prudoff R.S., Sass K.M., Wheelock M.J., et al. N-cadherin extracellular repeat 4 mediates epithelial to mesenchymal transition and increased motility. J. Cell Biol 2000, 151:1193-1206.
42. Birchmeier W., Hulsken J., Behrens J. Adherens junction proteins in tumour progression. Cancer Surv 1995, 24:129-140.
43. Tsanou E., Peschos D., Batistatou A., Charalabopoulos A., Charalabopoulos K. The E-cadherin adhesion molecule and colorectal cancer. A global literature approach. Anticancer Res 2008, 28:3815-3826.
44. Joo Y.E., Rew J.S., Park C.S., Kim S.J. Expression of E-cadherin, alpha- and beta-catenins in patients with pancreatic adenocarcinoma. Pancreatology 2002, 2:129-137.
45. Derycke L.D., Bracke M.E. N-cadherin in the spotlight of cell-cell adhesion, differentiation, embryogenesis, invasion and signalling. Int. J. Dev. Biol 2004, 48:463-476.
46. Hazan R.B., Phillips G.R., Qiao R.F., Norton L., Aaronson S.A. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J. Cell Biol 2000, 148:779-790.
47. Nakajima S., Doi R., Toyoda E., Tsuji S., Wada M., Koizumi M., et al. N-cadherin expression and epithelial-mesenchymal transition in pancreatic carcinoma. Clin. Cancer Res 2004, 10:4125-4133.
48. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol 2006, 7:131-142.
49. Christiansen J.J., Rajasekaran A.K. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 2006, 66:8319-8326.
50. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
51. Scheel C., Eaton E.N., Li S.H., Chaffer C.L., Reinhardt F., Kah K.J., et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011, 145:926-940.
52. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
53. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
54. Peinado H., Olmeda D., Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat. Rev. Cancer 2007, 7:415-428.
55. Nishioka R., Itoh S., Gui T., Gai Z., Oikawa K., Kawai M., et al. SNAIL induces epithelial-to-mesenchymal transition in a human pancreatic cancer cell line (BxPC3) and promotes distant metastasis and invasiveness in vivo. Exp. Mol. Pathol 2010, 89:149-157.
56. Akhshi T.K., Wernike D., Piekny A. Microtubules and actin crosstalk in cell migration and division. Cytoskeleton 2014, 71:1-23.