Dclk1 facilitates intestinal tumor growth via enhancing pluripotency and epithelial mesenchymal transition

Oncotarget

Volumn 5, Issue 19, 2014, Pages 9269-9280

  Chandrakesan, Parthasarathy ^a,b   Weygant, Nathaniel ^a   May, Randal ^a,c   Qu, Dongfeng ^a,b   Chinthalapally, Harisha R ^a   Sureban, Sripathi M ^a,c   Ali, Naushad ^a   Lightfoot, Stan A ^a   Umar, Shahid ^d   Houchen, Courtney W ^a,b,c  

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

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Dclk1; EMT; MiRNAs; Pluripotency; Self renewal; Tumorigenesis

Indexed keywords

DOUBLECORTIN LIKE KINASE 1; MICRORNA; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; APC PROTEIN; DCAMKL1 PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APC GENE; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CELL PLURIPOTENCY; CELL RENEWAL; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; INTESTINAL ADENOCARCINOMA; INTESTINAL ADENOMA; INTESTINE CANCER; INTESTINE EPITHELIUM; LOSS OF FUNCTION MUTATION; MALE; MOUSE; NONHUMAN; ONCOGENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ADENOCARCINOMA; ADENOMA; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CANCER STEM CELL; CELL TRANSFORMATION; CYTOLOGY; EPITHELIUM CELL; GENETICS; INTESTINE; INTESTINE MUCOSA; INTESTINE TUMOR; METABOLISM; MULTICELLULAR SPHEROID; PATHOLOGY; RNA INTERFERENCE; TRANSGENIC MOUSE; TUMOR CELL CULTURE;

ADENOCARCINOMA; ADENOMA; ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; INTESTINAL MUCOSA; INTESTINAL NEOPLASMS; INTESTINES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; NEOPLASTIC STEM CELLS; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 84910046833     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2393     Document Type: Article

References (33)

1. Fearnhead NS, Britton MP and Bodmer WF. The ABC of APC. Hum Mol Genet. 2001; 10(7):721-733.
2. Rustgi AK. The genetics of hereditary colon cancer. Genes Dev. 2007; 21(20):2525-2538.
3. Lewis A, Segditsas S, Deheragoda M, Pollard P, Jeffery R, Nye E, Lockstone H, Davis H, Clark S, Stamp G, Poulsom R, Wright N and Tomlinson I. Severe polyposis in Apc(1322T) mice is associated with submaximal Wnt signalling and increased expression of the stem cell marker Lgr5. Gut. 2010; 59(12):1680-1686.
4. Medema JP and Vermeulen L. Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature. 2011; 474(7351):318-326.
5. Garraway LA and Lander ES. Lessons from the cancer genome. Cell. 2013; 153(1):17-37.
6. Wasan HS, Novelli M, Bee J and Bodmer WF. Dietary fat influences on polyp phenotype in multiple intestinal neoplasia mice. Proceedings of the National Academy of Sciences of the United States of America. 1997; 94(7):3308-3313.
7. Ritland SR and Gendler SJ. Chemoprevention of intestinal adenomas in the ApcMin mouse by piroxicam: kinetics, strain effects and resistance to chemosuppression. Carcinogenesis. 1999; 20(1):51-58.
8. Tomita H, Yamada Y, Oyama T, Hata K, Hirose Y, Hara A, Kunisada T, Sugiyama Y, Adachi Y, Linhart H and Mori H. Development of gastric tumors in Apc(Min/+) mice by the activation of the beta-catenin/Tcf signaling pathway. Cancer research. 2007; 67(9):4079-4087.
9. Halberg RB, Waggoner J, Rasmussen K, White A, ClipsonL, Prunuske AJ, Bacher JW, Sullivan R, Washington MK, Pitot HC, Petrini JH, Albertson DG and Dove WF. Long-lived Min mice develop advanced intestinal cancers through a genetically conservative pathway. Cancer research. 2009; 69(14):5768-5775.
10. Luu C, Arrington AK, Schoellhammer HF, Singh G and Kim J. Targeted therapies in colorectal cancer: surgical considerations. Journal of gastrointestinal oncology. 2013; 4(3):328-336.
11. May R, Riehl TE, Hunt C, Sureban SM, Anant S and Houchen CW. Identification of a novel putative gastrointestinal stem cell and adenoma stem cell marker, doublecortin and CaM kinase-like-1, following radiation injury and in adenomatous polyposis coli/multiple intestinal neoplasia mice. Stem cells. 2008; 26(3):630-637.
12. Sureban SM, May R, Lightfoot SA, Hoskins AB, Lerner M, Brackett DJ, Postier RG, Ramanujam R, Mohammed A, Rao CV, Wyche JH, Anant S and Houchen CW. DCAMKL-1 regulates epithelial-mesenchymal transition in human pancreatic cells through a miR-200a-dependent mechanism. Cancer research. 2011; 71(6):2328-2338.
13. Ali N, Allam H, Bader T, May R, Basalingappa KM, BerryWL, Chandrakesan P, Qu D, Weygant N, BronzeMS, Umar S, Janknecht R, Sureban SM, Huycke M and HouchenCW. Fluvastatin interferes with hepatitis C virus replication via microtubule bundling and a doublecortin-like kinase-mediated mechanism. PloS one. 2013; 8(11):e80304.
14. Vega KJ, May R, Sureban SM, Lightfoot SA, Qu D, ReedA, Weygant N, Ramanujam R, Souza R, MadhounM, Whorton J, Anant S, Meltzer SJ and Houchen CW. Identification of the putative intestinal stem cell marker doublecortin and CaM kinase-like-1 in Barrett's esophagus and esophageal adenocarcinoma. J Gastroenterol Hepatol. 2012; 27(4):773-780.
15. Nakanishi Y, Seno H, Fukuoka A, Ueo T, Yamaga Y, Maruno T, Nakanishi N, Kanda K, Komekado H, Kawada M, Isomura A, Kawada K, Sakai Y, Yanagita M, KageyamaR, Kawaguchi Y and et al. Dclk1 distinguishes between tumor and normal stem cells in the intestine. Nature genetics. 2013; 45(1):98-9103.
16. Bailey JM, Alsina J, Rasheed ZA, McAllister FM, Fu YY, Plentz R, Zhang H, Pasricha PJ, Bardeesy N, Matsui W, Maitra A and Leach SD. DCLK1 marks a morphologically distinct subpopulation of cells with stem cell properties in preinvasive pancreatic cancer. Gastroenterology. 2014; 146(1):245-256.
17. Nakanishi Y, Seno H, Fukuoka A, Ueo T, YamagaY, Maruno T, Nakanishi N, Kanda K, Komekado H, KawadaM, Isomura A, Kawada K, Sakai Y, YanagitaM, Kageyama R, Kawaguchi Y and et al. Dclk1 distinguishes between tumor and normal stem cells in the intestine. Nature genetics. 2013; 45(1):98-103.
18. Weygant N, Qu D, Berry WL, May R, ChandrakesanP, Owen DB, Sureban SM, Ali N, Janknecht R and Houchen CW. Small molecule kinase inhibitor LRRK2-IN-1 demonstrates potent activity against colorectal and pancreatic cancer through inhibition of doublecortin-like kinase 1. Molecular cancer. 2014; 13(1):103.
19. Sureban SM, May R, Weygant N, Qu D, Chandrakesan P, Bannerman-Menson E, Ali N, Pantazis P, Westphalen CB, Wang TC and Houchen CW. XMD8-92 inhibits pancreatic tumor xenograft growth via DCLK1-dependent mechanism. Cancer letters. 2014.
20. Floor S, van Staveren WCG, Larsimont D, Dumont JE and Maenhaut C. Cancer cells in epithelial-to-mesenchymal transition and tumor-propagating-cancer stem cells: distinct, overlapping or same populations. Oncogene. 2011; 30(46):4609-4621.
21. Nimmo RA and Slack FJ. An elegant miRror: microRNAs in stem cells, developmental timing and cancer. Chromosoma. 2009; 118(4):405-418.
22. Ivey KN and Srivastava D. MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell. 2010; 7(1):36-41.
23. Westphalen CB, Asfaha S, Hayakawa Y, Takemoto Y, Lukin DJ, Nuber AH, Brandtner A, Setlik W, Remotti H, Muley A, Chen X, May R, Houchen CW, Fox JG, Gershon MD, Quante M and et al. Long-lived intestinal tuft cells serve as colon cancer-initiating cells. The Journal of clinical investigation. 2014; 124(3):1283-1295.
24. Zeki SS, Graham TA and Wright NA. Stem cells and their implications for colorectal cancer. Nat Rev Gastroenterol Hepatol. 2011; 8(2):90-100.
25. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J and WeinbergRA. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008; 133(4):704-715.
26. Chang C-J, Chao C-H, Xia W, Yang J-Y, Xiong Y, Li C-W, Yu W-H, Rehman SK, Hsu JL, Lee H-H, Liu M, Chen C-T, Yu D and Hung M-C. p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nature cell biology. 2011; 13(3):317-323.
27. Heinrich E-M and Dimmeler S. MicroRNAs and stem cells: control of pluripotency, reprogramming, and lineage commitment. Circ Res. 2012; 110(7):1014-1022.
28. Shaw P and Clarke AR. Murine models of intestinal cancer: recent advances. DNA repair. 2007; 6(10):1403-1412.
29. Sureban SM, May R, Mondalek FG, Qu D, Ponnurangam S, Pantazis P, Anant S, Ramanujam RP and Houchen CW. Nanoparticle-based delivery of siDCAMKL-1 increases microRNA-144 and inhibits colorectal cancer tumor growth via a Notch-1 dependent mechanism. Journal of nanobiotechnology. 2011; 9:40-40.
30. Chandrakesan P, Ahmed I, Anwar T, Wang Y, SarkarS, Singh P, Peleg S and Umar S. Novel changes in NF-{kappa}B activity during progression and regression phases of hyperplasia: role of MEK, ERK, and p38. J Biol Chem. 2010; 285(43):33485-33498.
31. Chandrakesan P, Ahmed I, Chinthalapally A, Singh P, Awasthi S, Anant S and Umar S. Distinct compartmen-talization of NF-kappaB activity in crypt and crypt-denuded lamina propria precedes and accompanies hyperplasia and/or colitis following bacterial infection. Infection and immunity. 2012; 80(2):753-767.
32. Chandrakesan P, Roy B, Jakkula LU, Ahmed I, Ramamoorthy P, Tawfik O, Papineni R, Houchen C, Anant S and Umar S. Utility of a bacterial infection model to study epithelial-mesenchymal transition, mesenchymal-epithelial transition or tumorigenesis. Oncogene. 2014; 33:2639-2654.
33. Chandrakesan P, Jakkula LU, Ahmed I, Roy B, Anant S and Umar S. Differential Effects of beta-catenin and NF-kappaB Interplay in the Regulation of Cell Proliferation, Inflammation and Tumorigenesis in Response to Bacterial Infection. PloS one. 2013; 8(11):e79432.