DCLK1 Regulates Pluripotency and Angiogenic Factors via microRNA-Dependent Mechanisms in Pancreatic Cancer

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Sureban, Sripathi M ^a,b,c   May, Randal ^a,b   Qu, Dongfeng ^a,b   Weygant, Nathaniel ^a   Chandrakesan, Parthasarathy ^a   Ali, Naushad ^a,c   Lightfoot, Stan A ^a,b   Pantazis, Panayotis ^d   Rao, Chinthalapally V ^a,c   Postier, Russell G ^a   Houchen, Courtney W ^a,b,c  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Peggy and Charles Stephenson Oklahoma Cancer Center   (United States)

^d COARE Biotechnology Inc ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

K RAS PROTEIN; KRUPPEL LIKE FACTOR 4; LET 7A; MICRORNA; MICRORNA 145; MICRORNA 200; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR ZEB1; TUMOR MARKER; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; CONTROLLED STUDY; DCLK1 GENE; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; KLF4 GENE; LIN28B GENE; MOUSE; NANOG GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OCT4 GENE; ONCOGENE K RAS; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PLURIPOTENT STEM CELL; RREB1 GENE; SNAIL GENE; SOX2 GENE; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT; VEGFR1 GENE; VEGFR2 GENE; ZEB1 GENE; ZEB2 GENE;

ANIMALS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICRORNAS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; PANCREATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84883613491     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073940     Document Type: Article

References (60)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2009) Cancer statistics, 2009. CA Cancer J Clin 59: 225-249. doi:10.3322/caac.20006. PubMed: 19474385.
2. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, et al. (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323. doi:10.1016/j.stem.2007.06.002. PubMed: 18371365.
3. Jimeno A, Feldmann G, Suárez-Gauthier A, Rasheed Z, Solomon A, et al. (2009) A direct pancreatic cancer xenograft model as a platform for cancer stem cell therapeutic development. Mol Cancer Ther 8: 310-314. doi:10.1158/1535-7163.MCT-08-0924. PubMed: 19174553.
4. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, et al. (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037. doi:10.1158/0008-5472.CAN-06-2030. PubMed: 17283135.
5. Polyak K, (2011) Heterogeneity in breast cancer. J Clin Invest 121: 3786-3788. doi:10.1172/JCI60534. PubMed: 21965334.
6. Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, et al. (2005) Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 7: 469-483. doi:10.1016/j.ccr.2005.04.023. PubMed: 15894267.
7. Turley EA, Veiseh M, Radisky DC, Bissell MJ, (2008) Mechanisms of disease: epithelial-mesenchymal transition--does cellular plasticity fuel neoplastic progression? Nat Clin Pract Oncol 5: 280-290. doi:10.1038/ncpcardio1163. PubMed: 18349857.
8. Diehn M, Clarke MF, (2006) Cancer stem cells and radiotherapy: new insights into tumor radioresistance. J Natl Cancer Inst 98: 1755-1757. doi:10.1093/jnci/djj505. PubMed: 17179471.
9. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715. doi:10.1016/j.cell.2008.03.027. PubMed: 18485877.
10. Park SM, Gaur AB, Lengyel E, Peter ME, (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22: 894-907. doi:10.1101/gad.1640608. PubMed: 18381893.
11. Sureban SM, May R, Lightfoot SA, Hoskins AB, Lerner M, et al. (2011) DCAMKL-1 regulates epithelial-mesenchymal transition in human pancreatic cells through a miR-200a-dependent mechanism. Cancer Res 71: 2328-2338. doi:10.1158/0008-5472.CAN-10-2738. PubMed: 21285251.
12. Sureban SM, May R, Mondalek FG, Qu D, Ponnurangam S, et al. (2011) Nanoparticle-based delivery of siDCAMKL-1 increases microRNA-144 and inhibits colorectal cancer tumor growth via a Notch-1 dependent mechanism. J Nanobiotechnol 9: 40. doi:10.1186/1477-3155-9-40.
13. Cullen BR, (2004) Transcription and processing of human microRNA precursors. Mol Cell 16: 861-865. doi:10.1016/j.molcel.2004.12.002. PubMed: 15610730.
14. Zhang L, Huang J, Yang N, Greshock J, Megraw MS, et al. (2006) microRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci U S A 103: 9136-9141. doi:10.1073/pnas.0508889103. PubMed: 16754881.
15. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, et al. (2005) A microRNA polycistron as a potential human oncogene. Nature 435: 828-833. doi:10.1038/nature03552. PubMed: 15944707.
16. Voorhoeve PM, le Sage C, Schrier M, Gillis AJ, Stoop H, et al. (2006) A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124: 1169-1181. doi:10.1016/j.cell.2006.02.037. PubMed: 16564011.
17. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, et al. (2002) Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 99: 15524-15529. doi:10.1073/pnas.242606799. PubMed: 12434020.
18. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, et al. (2005) RAS is regulated by the let-7 microRNA family. Cell 120: 635-647. doi:10.1016/j.cell.2005.01.014. PubMed: 15766527.
19. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, et al. (2006) Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9: 189-198. doi:10.1016/j.ccr.2006.01.025. PubMed: 16530703.
20. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, et al. (2004) Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 64: 3753-3756. doi:10.1158/0008-5472.CAN-04-0637. PubMed: 15172979.
21. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS, (2009) MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137: 647-658. doi:10.1016/j.cell.2009.02.038. PubMed: 19409607.
22. Shankar S, Nall D, Tang SN, Meeker D, Passarini J, et al. (2011) Resveratrol inhibits pancreatic cancer stem cell characteristics in human and KrasG12D transgenic mice by inhibiting pluripotency maintaining factors and epithelial-mesenchymal transition. PLOS ONE 6: e16530. doi:10.1371/journal.pone.0016530. PubMed: 21304978.
23. Chen YC, Hsu HS, Chen YW, Tsai TH, How CK, et al. (2008) Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLOS ONE 3: e2637. doi:10.1371/journal.pone.0002637. PubMed: 18612434.
24. Wen J, Park JY, Park KH, Chung HW, Bang S, et al. (2010) Oct4 and Nanog expression is associated with early stages of pancreatic carcinogenesis. Pancreas 39: 622-626. doi:10.1097/MPA.0b013e3181c75f5e. PubMed: 20173672.
25. Prasad NB, Biankin AV, Fukushima N, Maitra A, Dhara S, et al. (2005) Gene expression profiles in pancreatic intraepithelial neoplasia reflect the effects of Hedgehog signaling on pancreatic ductal epithelial cells. Cancer Res 65: 1619-1626. doi:10.1158/0008-5472.CAN-04-1413. PubMed: 15753353.
26. Wei D, Wang L, Kanai M, Jia Z, Le X, et al. (2010) KLF4α up-regulation promotes cell cycle progression and reduces survival time of patients with pancreatic cancer. Gastroenterology 139: 2135-2145. doi:10.1053/j.gastro.2010.08.022. PubMed: 20727893.
27. Peter ME, (2009) Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 8: 843-852. doi:10.4161/cc.8.6.7907. PubMed: 19221491.
28. Sureban SM, Johnson JJ, Houchen CW, (2012) Cancer Stem Cells and Pluripotency. Pancreatic Disorders and Therapy 02.
29. Kent OA, Chivukula RR, Mullendore M, Wentzel EA, Feldmann G, et al. (2010) Repression of the miR-143/145 cluster by oncogenic Ras initiates a tumor-promoting feed-forward pathway. Genes Dev 24: 2754-2759. doi:10.1101/gad.1950610. PubMed: 21159816.
30. Peng X, Guo W, Liu T, Wang X, Tu X, et al. (2011) Identification of miRs-143 and-145 that is associated with bone metastasis of prostate cancer and involved in the regulation of EMT. PLOS ONE 6: e20341. doi:10.1371/journal.pone.0020341. PubMed: 21647377.
31. Yao J, Wu X, Zhuang G, Kasman IM, Vogt T, et al. (2011) Expression of a functional VEGFR-1 in tumor cells is a major determinant of anti-PlGF antibodies efficacy. Proc Natl Acad Sci U S A 108: 11590-11595. doi:10.1073/pnas.1109029108. PubMed: 21709213.
32. Bhattacharya R, Kang-Decker N, Hughes DA, Mukherjee P, Shah V, et al. (2005) Regulatory role of dynamin-2 in VEGFR-2/KDR-mediated endothelial signaling. FASEB J 19: 1692-1694. PubMed: 16049137.
33. Cao Y, (2009) Positive and negative modulation of angiogenesis by VEGFR1 ligands. Sci Signal 2re1 PubMed: 19244214.
34. Lee YJ, Karl DL, Maduekwe UN, Rothrock C, Ryeom S, et al. (2010) Differential effects of VEGFR-1 and VEGFR-2 inhibition on tumor metastases based on host organ environment. Cancer Res 70: 8357-8367. doi:10.1158/0008-5472.CAN-10-1138. PubMed: 20978198.
35. Hoshida T, Sunamura M, Duda DG, Egawa S, Miyazaki S, et al. (2002) Gene therapy for pancreatic cancer using an adenovirus vector encoding soluble flt-1 vascular endothelial growth factor receptor. Pancreas 25: 111-121. doi:10.1097/00006676-200208000-00001. PubMed: 12142732.
36. Ogawa T, Takayama K, Takakura N, Kitano S, Ueno H, (2002) Anti-tumor angiogenesis therapy using soluble receptors: enhanced inhibition of tumor growth when soluble fibroblast growth factor receptor-1 is used with soluble vascular endothelial growth factor receptor. Cancer Gene Ther 9: 633-640. doi:10.1038/sj.cgt.7700478. PubMed: 12136423.
37. Solorzano CC, Baker CH, Bruns CJ, Killion JJ, Ellis LM, et al. (2001) Inhibition of growth and metastasis of human pancreatic cancer growing in nude mice by PTK 787/ZK222584, an inhibitor of the vascular endothelial growth factor receptor tyrosine kinases. Cancer Biother Radiopharm 16: 359-370.
38. Korc M, (2003) Pathways for aberrant angiogenesis in pancreatic cancer. Mol Cancer 2: 8. doi:10.1186/1476-4598-2-8. PubMed: 12556241.
39. Gerbe F, van Es JH, Makrini L, Brulin B, Mellitzer G, et al. (2011) Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. J Cell Biol 192: 767-780. doi:10.1083/jcb.201010127. PubMed: 21383077.
40. Bjerknes M, Khandanpour C, Möröy T, Fujiyama T, Hoshino M, et al. (2012) Origin of the brush cell lineage in the mouse intestinal epithelium. Dev Biol 362: 194-218. doi:10.1016/j.ydbio.2011.12.009. PubMed: 22185794.
41. Sureban SM, May R, Ramalingam S, Subramaniam D, Natarajan G, et al. (2009) Selective blockade of DCAMKL-1 results in tumor growth arrest by a Let-7a MicroRNA-dependent mechanism. Gastroenterology 137: 649-659, e641-642 doi:10.1053/j.gastro.2009.05.004. PubMed: 19445940.
42. Ali N, Allam H, May R, Sureban SM, Bronze MS, et al. (2011) Hepatitis C virus-induced cancer stem cell-like signatures in cell culture and murine tumor xenografts. J Virol 85: 12292-12303. doi:10.1128/JVI.05920-11. PubMed: 21937640.
43. Nakanishi Y, Seno H, Fukuoka A, Ueo T, Yamaga Y, et al. (2013) Dclk1 distinguishes between tumor and normal stem cells in the intestine. Nat Genet 45: 98-103. PubMed: 23202126.
44. Mondalek FG, Ponnurangam S, Govind J, Houchen C, Anant S, et al. (2010) Inhibition of angiogenesis- and inflammation-inducing factors in human colon cancer cells in vitro and in ovo by free and nanoparticle-encapsulated redox dye, DCPIP. J Nanobiotechnology 8: 17. doi:10.1186/1477-3155-8-17. PubMed: 20633276.
45. de Fougerolles AR, (2008) Delivery vehicles for small interfering RNA in vivo. Hum Gene Ther 19: 125-132. doi:10.1089/hum.2008.928. PubMed: 18257677.
46. Yang X, Lin X, Zhong X, Kaur S, Li N, et al. (2010) Double-negative feedback loop between reprogramming factor LIN28 and microRNA let-7 regulates aldehyde dehydrogenase 1-positive cancer stem cells. Cancer Res 70: 9463-9472. doi:10.1158/0008-5472.CAN-10-2388. PubMed: 21045151.
47. Zhong X, Li N, Liang S, Huang Q, Coukos G, et al. (2010) Identification of microRNAs regulating reprogramming factor LIN28 in embryonic stem cells and cancer cells. J Biol Chem 285: 41961-41971. doi:10.1074/jbc.M110.169607. PubMed: 20947512.
48. Roybal JD, Zang Y, Ahn YH, Yang Y, Gibbons DL, et al. (2011) miR-200 Inhibits lung adenocarcinoma cell invasion and metastasis by targeting Flt1/VEGFR1. Mol Cancer Res 9: 25-35. doi:10.1158/1541-7786.MCR-10-0497. PubMed: 21115742.
49. Choi YC, Yoon S, Jeong Y, Yoon J, Baek K, (2011) Regulation of vascular endothelial growth factor signaling by miR-200b. Mol Cells 32: 77-82. doi:10.1007/s10059-011-1042-2. PubMed: 21544626.
50. Michael MZ, O' Connor SM, van Holst Pellekaan NG, Young GP, James RJ, (2003) Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 1: 882-891. PubMed: 14573789.
51. Akao Y, Nakagawa Y, Kitade Y, Kinoshita T, Naoe T, (2007) Downregulation of microRNAs-143 and-145 in B-cell malignancies. Cancer Sci 98: 1914-1920. doi:10.1111/j.1349-7006.2007.00618.x. PubMed: 17892514.
52. Pramanik D, Campbell NR, Karikari C, Chivukula R, Kent OA, et al. (2011) Restitution of tumor suppressor microRNAs using a systemic nanovector inhibits pancreatic cancer growth in mice. Mol Cancer Ther 10: 1470-1480. doi:10.1158/1535-7163.MCT-11-0152. PubMed: 21622730.
53. Perera RM, Bardeesy N, (2012) Ready, Set, Go: The EGF Receptor at the Pancreatic Cancer Starting Line. Cancer Cell 22: 281-282. doi:10.1016/j.ccr.2012.08.019. PubMed: 22975369.
54. Navas C, Hernández-Porras I, Schuhmacher AJ, Sibilia M, Guerra C, et al. (2012) EGF Receptor Signaling Is Essential for K-Ras Oncogene-Driven Pancreatic Ductal Adenocarcinoma. Cancer Cell 22: 318-330. doi:10.1016/j.ccr.2012.08.001. PubMed: 22975375.
55. Cho WC, Chow AS, Au JS, (2011) MiR-145 inhibits cell proliferation of human lung adenocarcinoma by targeting EGFR and NUDT1. RNA Biol 8: 125-131. doi:10.4161/rna.8.1.14259. PubMed: 21289483.
56. Zhu H, Dougherty U, Robinson V, Mustafi R, Pekow J, et al. (2011) EGFR signals downregulate tumor suppressors miR-143 and miR-145 in Western diet-promoted murine colon cancer: role of G1 regulators. Mol Cancer Res 9: 960-975. doi:10.1158/1541-7786.MCR-10-0531. PubMed: 21653642.
57. Tian H, Biehs B, Warming S, Leong KG, Rangell L, et al. (2011) A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478: 255-259. doi:10.1038/nature10408. PubMed: 21927002.
58. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, et al. (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40: 499-507. doi:10.1038/ng.127. PubMed: 18443585.
59. Bao B, Wang Z, Ali S, Kong D, Li Y, et al. (2011) Notch-1 induces epithelial-mesenchymal transition consistent with cancer stem cell phenotype in pancreatic cancer cells. Cancer Lett 307: 26-36. doi:10.1016/j.canlet.2011.03.012. PubMed: 21463919.
60. Brabletz S, Bajdak K, Meidhof S, Burk U, Niedermann G, et al. (2011) The ZEB1/miR-200 feedback loop controls Notch signalling in cancer cells. EMBO J 30: 770-782. doi:10.1038/emboj.2010.349. PubMed: 21224848.