Role of DCLK1 in oncogenic signaling (Review)
- Authors:
- Qin Lu
- Hailan Feng
- Hong Chen
- Nathaniel Weygant
- Jian Du
- Zixing Yan
- Zhiyun Cao
-
Affiliations: Department of Integrative Medicine, Fujian University of Traditional Chinese Medicine, Fuzhou, Fujian 350122, P.R. China, Affiliated Fuzhou Hospital of Traditional Chinese Medicine, Fujian University of Traditional Chinese Medicine, Fuzhou, Fujian 350001, P.R. China - Published online on: September 21, 2022 https://doi.org/10.3892/ijo.2022.5427
- Article Number: 137
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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. 26:630–637. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Vega KJ, May R, Sureban SM, Lightfoot SA, Qu D, Reed A, Weygant N, Ramanujam R, Souza R, Madhoun M, et al: Identification of the putative intestinal stem cell marker doublecortin and CaM kinase-like-1 in Barrett's esophagus and esophageal adenocarcinoma. J Gastroenterol Hepatol. 27:773–780. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Weygant N, Qu D, May R, Tierney RM, Berry WL, Zhao L, Agarwal S, Chandrakesan P, Chinthalapally HR, Murphy NT, et al: DCLK1 is a broadly dysregulated target against epithelial-mesenchymal transition, focal adhesion, and stemness in clear cell renal carcinoma. Oncotarget. 6:2193–2205. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Nakanishi Y, Seno H, Fukuoka A, Ueo T, Yamaga Y, Maruno T, Nakanishi N, Kanda K, Komekado H, Kawada M, et al: Dclk1 distinguishes between tumor and normal stem cells in the intestine. Nat Genet. 45:98–103. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Delgiorno KE, Hall JC, Takeuchi KK, Pan FC, Halbrook CJ, Washington MK, Olive KP, Spence JR, Sipos B, Wright CV, et al: Identification and manipulation of biliary metaplasia in pancreatic tumors. Gastroenterology. 146:233–244.e5. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Saqui-Salces M, Keeley TM, Grosse AS, Qiao XT, El-Zaatari M, Gumucio DL, Samuelson LC and Merchant JL: Gastric tuft cells express DCLK1 and are expanded in hyperplasia. Histochem Cell Biol. 136:191–204. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Gerbe F, van Es JH, Makrini L, Brulin B, Mellitzer G, Robine S, Romagnolo B, Shroyer NF, Bourgaux JF, Pignodel C, et al: Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. J Cell Biol. 192:767–780. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Howitt MR, Lavoie S, Michaud M, Blum AM, Tran SV, Weinstock JV, Gallini CA, Redding K, Margolskee RF, Osborne LC, et al: Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut. Science. 351:1329–1333. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Westphalen CB, Quante M and Wang TC: Functional implication of Dclk1 and Dclk1-expressing cells in cancer. Small GTPases. 8:164–171. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Yi J, Bergstrom K, Fu J, Shan X, McDaniel JM, McGee S, Qu D, Houchen CW, Liu X and Xia L: Dclk1 in tuft cells promotes inflammation-driven epithelial restitution and mitigates chronic colitis. Cell Death Differ. 26:1656–1669. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Patel O, Dai W, Mentzel M, Griffin MD, Serindoux J, Gay Y, Fischer S, Sterle S, Kropp A, Burns CJ, et al: Biochemical and structural insights into doublecortin-like kinase domain 1. Structure. 24:1550–1561. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Cheung AS, de Rooy C, Levinger I, Rana K, Clarke MV, How JM, Garnham A, McLean C, Zajac JD, Davey RA and Grossmann M: Actin alpha cardiac muscle 1 gene expression is upregulated in the skeletal muscle of men undergoing androgen deprivation therapy for prostate cancer. J Steroid Biochem Mol Biol. 174:56–64. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Matsumoto N, Pilz DT and Ledbetter DH: Genomic structure, chromosomal mapping, and expression pattern of human DCAMKL1 (KIAA0369), a homologue of DCX (XLIS). Genomics. 56:179–183. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Burgess HA and Reiner O: Cleavage of doublecortin-like kinase by calpain releases an active kinase fragment from a microtubule anchorage domain. J Biol Chem. 276:36397–36403. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Kim MH, Cierpicki T, Derewenda U, Krowarsch D, Feng Y, Devedjiev Y, Dauter Z, Walsh CA, Otlewski J, Bushweller JH and Derewenda ZS: The DCX-domain tandems of doublecortin and doublecortin-like kinase. Nat Struct Biol. 10:324–333. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Lin PT, Gleeson JG, Corbo JC, Flanagan L and Walsh CA: DCAMKL1 encodes a protein kinase with homology to doublecortin that regulates microtubule polymerization. J Neurosci. 20:9152–9161. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Engels BM, Schouten TG, van Dullemen J, Gosens I and Vreugdenhil E: Functional differences between two DCLK splice variants. Brain Res Mol Brain Res. 120:103–114. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Burgess HA and Reiner O: Alternative splice variants of doublecortin-like kinase are differentially expressed and have different kinase activities. J Biol Chem. 277:17696–17705. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
O'Connell MR, Sarkar S, Luthra GK, Okugawa Y, Toiyama Y, Gajjar AH, Qiu S, Goel A and Singh P: Epigenetic changes and alternate promoter usage by human colon cancers for expressing DCLK1-isoforms: Clinical Implications. Sci Rep. 5:149832015. View Article : Google Scholar : PubMed/NCBI | |
|
Walker TL, Yasuda T, Adams DJ and Bartlett PF: The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci. 27:3734–3742. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Park SY, Kim JY, Choi JH, Kim JH, Lee CJ, Singh P, Sarkar S, Baek JH and Nam JS: Inhibition of LEF1-mediated DCLK1 by niclosamide attenuates colorectal cancer stemness. Clin Cancer Res. 25:1415–1429. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Sarkar S, Popov VL, O'Connell MR, Stevenson HL, Lee BS, Obeid RA, Luthra GK and Singh P: A novel antibody against cancer stem cell biomarker, DCLK1-S, is potentially useful for assessing colon cancer risk after screening colonoscopy. Lab Invest. 97:1245–1261. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Andresen K, Boberg KM, Vedeld HM, Honne H, Hektoen M, Wadsworth CA, Clausen OP, Karlsen TH, Foss A, Mathisen O, et al: Novel target genes and a valid biomarker panel identified for cholangiocarcinoma. Epigenetics. 7:1249–1257. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Westphalen CB, Takemoto Y, Tanaka T, Macchini M, Jiang Z, Renz BW, Chen X, Ormanns S, Nagar K, Tailor Y, et al: Dclk1 defines quiescent pancreatic progenitors that promote injury-induced regeneration and tumorigenesis. Cell Stem Cell. 18:441–455. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Yamaga Y, Fukuda A, Nakanishi Y, Goto N, Matsumoto Y, Yoshioka T, Maruno T, Chiba T and Seno H: Gene expression profile of Dclk1+ cells in intestinal tumors. Dig Liver Dis. 50:1353–1361. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Ge Y, Liu H, Zhang Y, Liu J, Yan R, Xiao Z, Fan X, Huang X and An G: Inhibition of DCLK1 kinase reverses epithelial-mesenchymal transition and restores T-cell activity in pancreatic ductal adenocarcinoma. Transl Oncol. 17:1013172022.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
|
May R, Sureban SM, Hoang N, Riehl TE, Lightfoot SA, Ramanujam R, Wyche JH, Anant S and Houchen CW: Doublecortin and CaM kinase-like-1 and leucine-rich-repeat-containing G-protein-coupled receptor mark quiescent and cycling intestinal stem cells, respectively. Stem Cells. 27:2571–2579. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Ladang A, Rapino F, Heukamp LC, Tharun L, Shostak K, Hermand D, Delaunay S, Klevernic I, Jiang Z, Jacques N, et al: Elp3 drives Wnt-dependent tumor initiation and regeneration in the intestine. J Exp Med. 212:2057–2075. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Leppänen J, Helminen O, Huhta H, Kauppila JH, Miinalainen I, Ronkainen VP, Saarnio J, Lehenkari PP and Karttunen TJ: Doublecortin-like kinase 1-positive enterocyte-a new cell type in human intestine. APMIS. 124:958–965. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Westphalen CB, Asfaha S, Hayakawa Y, Takemoto Y, Lukin DJ, Nuber AH, Brandtner A, Setlik W, Remotti H, Muley A, et al: Long-lived intestinal tuft cells serve as colon cancer-initiating cells. J Clin Invest. 124:1283–1295. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Qu D, Weygant N, May R, Chandrakesan P, Madhoun M, Ali N, Sureban SM, An G, Schlosser MJ and Houchen CW: Ablation of doublecortin-like kinase 1 in the colonic epithelium exacerbates dextran sulfate sodium-induced colitis. PLoS One. 10:e01342122015. View Article : Google Scholar : PubMed/NCBI | |
|
Gerbe F, Brulin B, Makrini L, Legraverend C and Jay P: DCAMKL-1 expression identifies Tuft cells rather than stem cells in the adult mouse intestinal epithelium. Gastroenterology. 137:2179–2181. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Eini L, Naseri M, Karimi-Busheri F, Bozorgmehr M, Ghods R and Madjd Z: Primary colonospheres maintain stem cell-like key features after cryopreservation. J Cell Physiol. 235:2452–2463. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Chandrakesan P, Yao J, Qu D, May R, Weygant N, Ge Y, Ali N, Sureban SM, Gude M, Vega K, et al: Dclk1, a tumor stem cell marker, regulates pro-survival signaling and self-renewal of intestinal tumor cells. Mol Cancer. 16:302017. View Article : Google Scholar : PubMed/NCBI | |
|
Wang X, Yang Y and Huycke MM: Commensal-infected macrophages induce dedifferentiation and reprogramming of epithelial cells during colorectal carcinogenesis. Oncotarget. 8:102176–102190. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Gagliardi G, Goswami M, Passera R and Bellows CF: DCLK1 immunoreactivity in colorectal neoplasia. Clin Exp Gastroenterol. 5:35–42. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Vedeld HM, Skotheim RI, Lothe RA and Lind GE: The recently suggested intestinal cancer stem cell marker DCLK1 is an epigenetic biomarker for colorectal cancer. Epigenetics. 9:346–450. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Takiyama A, Tanaka T, Kazama S, Nagata H, Kawai K, Hata K, Otani K, Nishikawa T, Sasaki K, Kaneko M, et al: DCLK1 expression in colorectal polyps increases with the severity of dysplasia. In Vivo. 32:365–371. 2018.PubMed/NCBI | |
|
Ahmed I, Roy BC, Raach RT, Owens SM, Xia L, Anant S, Sampath V and Umar S: Enteric infection coupled with chronic Notch pathway inhibition alters colonic mucus composition leading to dysbiosis, barrier disruption and colitis. PLoS One. 13:e02067012018. View Article : Google Scholar : PubMed/NCBI | |
|
Mirzaei A, Tavoosidana G, Modarressi MH, Rad AA, Fazeli MS, Shirkoohi R, Tavakoli-Yaraki M and Madjd Z: Upregulation of circulating cancer stem cell marker, DCLK1 but not Lgr5, in chemoradiotherapy-treated colorectal cancer patients. Tumour Biol. 36:4801–4810. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J, Yokoyama Y, Hirose H, Shimomura Y, Bonkobara S, Itakura H, Kouda S, Morimoto Y, Minami K, Takahashi H, et al: Functional assessment of miR-1291 in colon cancer cells. Int J Oncol. 60:132022. View Article : Google Scholar : PubMed/NCBI | |
|
Razi S, Sadeghi A, Asadi-Lari Z, Tam KJ, Kalantari E and Madjd Z: DCLK1, a promising colorectal cancer stem cell marker, regulates tumor progression and invasion through miR-137 and miR-15a dependent manner. Clin Exp Med. 21:139–147. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
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. J Nanobiotechnology. 9:402011. View Article : Google Scholar : PubMed/NCBI | |
|
Kwon MS, Chung HK, Xiao L, Yu TX, Wang SR, Piao JJ, Gorospe M and Wang JY: MicroRNA-195 regulates Tuft cell function in the intestinal epithelium by altering translation of DCLK1. Am J Physiol Cell Physiol. 320:C1042–C1054. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Neradugomma NK, Subramaniam D, Tawfik OW, Goffin V, Kumar TR, Jensen RA and Anant S: Prolactin signaling enhances colon cancer stemness by modulating Notch signaling in a Jak2-STAT3/ERK manner. Carcinogenesis. 35:795–806. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Ahmed I, Roy BC, Subramaniam D, Ganie SA, Kwatra D, Dixon D, Anant S, Zargar MA and Umar S: An ornamental plant targets epigenetic signaling to block cancer stem cell-driven colon carcinogenesis. Carcinogenesis. 37:385–396. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Ponnurangam S, Dandawate PR, Dhar A, Tawfik OW, Parab RR, Mishra PD, Ranadive P, Sharma R, Mahajan G, Umar S, et al: Quinomycin A targets Notch signaling pathway in pancreatic cancer stem cells. Oncotarget. 7:3217–3232. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Venugopal A, Subramaniam D, Balmaceda J, Roy B, Dixon DA, Umar S, Weir SJ and Anant S: RNA binding protein RBM3 increases β-catenin signaling to increase stem cell characteristics in colorectal cancer cells. Mol Carcinog. 55:1503–1516. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Krishnamachary B, Subramaniam D, Dandawate P, Ponnurangam S, Srinivasan P, Ramamoorthy P, Umar S, Thomas SM, Dhar A, Septer S, et al: Targeting transcription factor TCF4 by γ-mangostin, a natural xanthone. Oncotarget. 10:5576–5591. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Osman J, Bellamkonda K, Liu Q, Andersson T and Sjölander A: The WNT5A agonist Foxy5 reduces the number of colonic cancer stem cells in a xenograft mouse model of human colonic cancer. Anticancer Res. 39:1719–1728. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Hammond DE, Mageean CJ, Rusilowicz EV, Wickenden JA, Clague MJ and Prior IA: Differential reprogramming of isogenic colorectal cancer cells by distinct activating KRAS mutations. J Proteome Res. 14:1535–1546. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Qiu W, Remotti HE, Tang SM, Wang E, Dobberteen L, Lee Youssof A, Lee JH, Cheung EC and Su GH: Pancreatic DCLK1+ cells originate distinctly from PDX1+ progenitors and contribute to the initiation of intraductal papillary mucinous neoplasm in mice. Cancer Lett. 423:71–79. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Bailey JM, Alsina J, Rasheed ZA, McAllister FM, Fu YY, Plentz R, Zhang H, Pasricha PJ, Bardeesy N, Matsui W, et al: DCLK1 marks a morphologically distinct subpopulation of cells with stem cell properties in preinvasive pancreatic cancer. Gastroenterology. 146:245–256. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
May R, Sureban SM, Lightfoot SA, Hoskins AB, Brackett DJ, Postier RG, Ramanujam R, Rao CV, Wyche JH, Anant S and Houchen CW: Identification of a novel putative pancreatic stem/progenitor cell marker DCAMKL-1 in normal mouse pancreas. Am J Physiol Gastrointest Liver Physiol. 299:G303–G310. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Sureban SM, May R, Qu D, Weygant N, Chandrakesan P, Ali N, Lightfoot SA, Pantazis P, Rao CV, Postier RG and Houchen CW: DCLK1 regulates pluripotency and angiogenic factors via microRNA-dependent mechanisms in pancreatic cancer. PLoS One. 8:e739402013. View Article : Google Scholar : PubMed/NCBI | |
|
Yao ZX, Qin ML, Liu JJ, Chen XS and Zhou DS: In vitro cultivation of human fetal pancreatic ductal stem cells and their differentiation into insulin-producing cells. World J Gastroenterol. 10:1452–1456. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Seeley ES, Carrière C, Goetze T, Longnecker DS and Korc M: Pancreatic cancer and precursor pancreatic intraepithelial neoplasia lesions are devoid of primary cilia. Cancer Res. 69:422–430. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Lee H, Basso IN and Kim DDH: Target spectrum of the BCR-ABL tyrosine kinase inhibitors in chronic myeloid leukemia. Int J Hematol. 113:632–641. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Y, Gao C, Cao F, Wu Y, Chen S, Han X, Mo J, Qiu Z, Fan W, Zhou P and Shen L: Pan-cancer analysis of IGF-1 and IGF-1R as potential prognostic biomarkers and immunotherapy targets. Front Oncol. 11:7553412021. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Y, Zoltan M, Riquelme E, Xu H, Sahin I, Castro-Pando S, Montiel MF, Chang K, Jiang Z, Ling J, et al: Immune cell production of interleukin 17 induces stem cell features of pancreatic intraepithelial neoplasia cells. Gastroenterology. 155:210–223.e3. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
DelGiorno KE, Naeem RF, Fang L, Chung CY, Ramos C, Luhtala N, O'Connor C, Hunter T, Manor U and Wahl GM: Tuft cell formation reflects epithelial plasticity in pancreatic injury: Implications for modeling human pancreatitis. Front Physiol. 11:882020. View Article : Google Scholar : PubMed/NCBI | |
|
Park JT and Leach SD: Zebrafish model of KRAS-initiated pancreatic cancer. Anim Cells Syst (Seoul). 22:353–359. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou B, Irwanto A, Guo YM, Bei JX, Wu Q, Chen G, Zhang TP, Lei JJ, Feng QS, Chen LZ, et al: Exome sequencing and digital PCR analyses reveal novel mutated genes related to the metastasis of pancreatic ductal adenocarcinoma. Cancer Biol Ther. 13:871–879. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Qu D, Weygant N, Yao J, Chandrakesan P, Berry WL, May R, Pitts K, Husain S, Lightfoot S, Li M, et al: Overexpression of DCLK1-AL increases tumor cell invasion, drug resistance, and KRAS activation and can be targeted to inhibit tumorigenesis in pancreatic cancer. J Oncol. 2019:64029252019. View Article : Google Scholar : PubMed/NCBI | |
|
Chandrakesan P, Panneerselvam J, May R, Weygant N, Qu D, Berry WR, Pitts K, Stanger BZ, Rao CV, Bronze MS and Houchen CW: DCLK1-isoform2 alternative splice variant promotes pancreatic tumor immunosuppressive M2-macrophage polarization. Mol Cancer Ther. 19:1539–1549. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Xu Z, Pang TCY, Liu AC, Pothula SP, Mekapogu AR, Perera CJ, Murakami T, Goldstein D, Pirola RC, Wilson JS and Apte MV: Targeting the HGF/c-MET pathway in advanced pancreatic cancer: A key element of treatment that limits primary tumour growth and eliminates metastasis. Br J Cancer. 122:1486–1495. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Rieder S, Michalski CW, Friess H and Kleeff J: Insulin-like growth factor signaling as a therapeutic target in pancreatic cancer. Anticancer Agents Med Chem. 11:427–433. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Sureban SM, May R, Lightfoot SA, Hoskins AB, Lerner M, Brackett DJ, Postier RG, Ramanujam R, Mohammed A, Rao CV, et al: DCAMKL-1 regulates epithelial-mesenchymal transition in human pancreatic cells through a miR-200a-dependent mechanism. Cancer Res. 71:2328–2338. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Bjerknes M, Khandanpour C, Moroy T, Fujiyama T, Hoshino M, Klisch TJ, Ding Q, Gan L, Wang J, Martín MG and Cheng H: Origin of the brush cell lineage in the mouse intestinal epithelium. Dev Biol. 362:194–218. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Ali Y, Lin Y, Gharibo MM, Gounder MK, Stein MN, Lagattuta TF, Egorin MJ, Rubin EH and Poplin EA: Phase I and pharmacokinetic study of imatinib mesylate (Gleevec) and gemcitabine in patients with refractory solid tumors. Clin Cancer Res. 13:5876–5882. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Giannakis M, Stappenbeck TS, Mills JC, Leip DG, Lovett M, Clifton SW, Ippolito JE, Glasscock JI, Arumugam M, Brent MR and Gordon JI: Molecular properties of adult mouse gastric and intestinal epithelial progenitors in their niches. J Biol Chem. 281:11292–11300. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Weygant N, Ge Y, Qu D, Kaddis JS, Berry WL, May R, Chandrakesan P, Bannerman-Menson E, Vega KJ, Tomasek JJ, et al: Survival of patients with gastrointestinal cancers can be predicted by a surrogate microRNA signature for cancer stem-like cells marked by DCLK1 kinase. Cancer Res. 76:4090–4099. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Y and Huang X: Investigation of doublecortin and calcium/calmodulin-dependent protein kinase-like-1-expressing cells in the mouse stomach. J Gastroenterol Hepatol. 25:576–582. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Meng QB, Yu JC, Kang WM, Ma ZQ, Zhou WX, Li J, Zhou L, Cao ZJ and Tian SB: Expression of doublecortin-like kinase 1 in human gastric cancer and its correlation with prognosis. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 35:639–644. 2013.(In Chinese). PubMed/NCBI | |
|
Sureban SM, Qu D and Houchen CW: Regulation of miRNAs by agents targeting the tumor stem cell markers DCLK1, MSI1, LGR5, and BMI1. Curr Pharmacol Rep. 1:217–222. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Liu ZQ, He WF, Wu YJ, Zhao SL, Wang L, Ouyang YY and Tang SY: LncRNA SNHG1 promotes EMT process in gastric cancer cells through regulation of the miR-15b/DCLK1/Notch1 axis. BMC Gastroenterol. 20:1562020. View Article : Google Scholar : PubMed/NCBI | |
|
Carli ALE, Afshar-Sterle S, Rai A, Fang H, O'Keefe R, Tse J, Ferguson FM, Gray NS, Ernst M, Greening DW and Buchert M: Cancer stem cell marker DCLK1 reprograms small extracellular vesicles toward migratory phenotype in gastric cancer cells. Proteomics. 21:e20000982021. View Article : Google Scholar : PubMed/NCBI | |
|
Dai J, Li ZX, Zhang Y, Ma JL, Zhou T, You WC, Li WQ and Pan KF: Whole genome messenger RNA profiling identifies a novel signature to predict gastric cancer survival. Clin Transl Gastroenterol. 10:e000042019. View Article : Google Scholar : PubMed/NCBI | |
|
Schellnegger R, Quante A, Rospleszcz S, Schernhammer M, Höhl B, Tobiasch M, Pastula A, Brandtner A, Abrams JA, Strauch K, et al: Goblet cell ratio in combination with differentiation and stem cell markers in barrett esophagus allow distinction of patients with and without esophageal adenocarcinoma. Cancer Prev Res (Phila). 10:55–66. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Ge Y, Fan X, Huang X, Weygant N, Xiao Z, Yan R, Liu H, Liu J, An G and Yao J: DCLK1-short splice variant promotes esophageal squamous cell carcinoma progression via the MAPK/ERK/MMP2 pathway. Mol Cancer Res. 19:1980–1991. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang L, Zhou S, Guo E, Chen X, Yang J and Li X: DCLK1 inhibition attenuates tumorigenesis and improves chemosensitivity in esophageal squamous cell carcinoma by inhibiting β-catenin/c-Myc signaling. Pflugers Arch. 472:1041–1049. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Whorton J, Sureban SM, May R, Qu D, Lightfoot SA, Madhoun M, Johnson M, Tierney WM, Maple JT, Vega KJ and Houchen CW: DCLK1 is detectable in plasma of patients with Barrett's esophagus and esophageal adenocarcinoma. Dig Dis Sci. 60:509–513. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Quante M, Bhagat G, Abrams JA, Marache F, Good P, Lee MD, Lee Y, Friedman R, Asfaha S, Dubeykovskaya Z, et al: Bile acid and inflammation activate gastric cardia stem cells in a mouse model of Barrett-like metaplasia. Cancer Cell. 21:36–51. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Haakensen VD, Bjøro T, Lüders T, Riis M, Bukholm IK, Kristensen VN, Troester MA, Homen MM, Ursin G, Børresen-Dale AL and Helland Å: Serum estradiol levels associated with specific gene expression patterns in normal breast tissue and in breast carcinomas. BMC Cancer. 11:3322011. View Article : Google Scholar : PubMed/NCBI | |
|
Liu YH, Tsang JY, Ni YB, Hlaing T, Chan SK, Chan KF, Ko CW, Mujtaba SS and Tse GM: Doublecortin-like kinase 1 expression associates with breast cancer with neuroendocrine differentiation. Oncotarget. 7:1464–1476. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao S, Ma D, Xiao Y, Li XM, Ma JL, Zhang H, Xu XL, Lv H, Jiang WH, Yang WT, et al: Molecular subtyping of triple-negative breast cancers by immunohistochemistry: Molecular Basis and clinical relevance. Oncologist. 25:e1481–e1491. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Ramamoorthy P, Dandawate P, Jensen RA and Anant S: Celastrol and triptolide suppress stemness in triple negative breast cancer: Notch as a therapeutic target for stem cells. Biomedicines. 9:4822021. View Article : Google Scholar : PubMed/NCBI | |
|
Wang YL, Li Y, Ma YG and Wu WY: DCLK1 promotes malignant progression of breast cancer by regulating Wnt/β-catenin signaling pathway. Eur Rev Med Pharmacol Sci. 23:9489–9498. 2019.PubMed/NCBI | |
|
Liu H, Wen T, Zhou Y, Fan X, Du T, Gao T, Li L, Liu J, Yang L, Yao J, et al: DCLK1 plays a metastatic-promoting role in human breast cancer cells. Biomed Res Int. 2019:10619792019.PubMed/NCBI | |
|
Wang J, Wang S, Zhou J and Qian Q: miR-424-5p regulates cell proliferation, migration and invasion by targeting doublecortin-like kinase 1 in basal-like breast cancer. Biomed Pharmacother. 102:147–152. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Ge Y, Weygant N, Qu D, May R, Berry WL, Yao J, Chandrakesan P, Zheng W, Zhao L, Zhao KL, et al: Alternative splice variants of DCLK1 mark cancer stem cells, promote self-renewal and drug-resistance, and can be targeted to inhibit tumorigenesis in kidney cancer. Int J Cancer. 143:1162–1175. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Ding L, Yang Y, Ge Y, Lu Q, Yan Z, Chen X, Du J, Hafizi S, Xu X, Yao J, et al: Inhibition of DCLK1 with DCLK1-IN-1 suppresses renal cell carcinoma invasion and stemness and promotes cytotoxic T-cell-mediated anti-tumor immunity. Cancers (Basel). 13:57292021. View Article : Google Scholar : PubMed/NCBI | |
|
Sureban SM, Madhoun MF, May R, Qu D, Ali N, Fazili J, Weygant N, Chandrakesan P, Ding K, Lightfoot SA and Houchen CW: Plasma DCLK1 is a marker of hepatocellular carcinoma (HCC): Targeting DCLK1 prevents HCC tumor xenograft growth via a microRNA-dependent mechanism. Oncotarget. 6:37200–37215. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Ali N, Chandrakesan P, Nguyen CB, Husain S, Gillaspy AF, Huycke M, Berry WL, May R, Qu D, Weygant N, et al: Inflammatory and oncogenic roles of a tumor stem cell marker doublecortin-like kinase (DCLK1) in virus-induced chronic liver diseases. Oncotarget. 6:20327–20344. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Girotto G, Vuckovic D, Buniello A, Lorente-Cánovas B, Lewis M, Gasparini P and Steel KP: Expression and replication studies to identify new candidate genes involved in normal hearing function. PLoS One. 9:e853522014. View Article : Google Scholar : PubMed/NCBI | |
|
Srikrishna G: S100A8 and S100A9: New insights into their roles in malignancy. J Innate Immun. 4:31–40. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Wilen CB, Lee S, Hsieh LL, Orchard RC, Desai C, Hykes BL Jr, McAllaster MR, Balce DR, Feehley T, Brestoff JR, et al: Tropism for tuft cells determines immune promotion of norovirus pathogenesis. Science. 360:204–208. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Ali N, Nguyen CB, Chandrakesan P, Wolf RF, Qu D, May R, Goretsky T, Fazili J, Barrett TA, Li M, et al: Doublecortin-like kinase 1 promotes hepatocyte clonogenicity and oncogenic programming via non-canonical β-catenin-dependent mechanism. Sci Rep. 10:105782020. View Article : Google Scholar : PubMed/NCBI | |
|
Ali N, Allam H, May R, Sureban SM, Bronze MS, Bader T, Umar S, Anant S and Houchen CW: Hepatitis C virus-induced cancer stem cell-like signatures in cell culture and murine tumor xenografts. J Virol. 85:12292–12303. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Ali N, Allam H, Bader T, May R, Basalingappa KM, Berry WL, Chandrakesan P, Qu D, Weygant N, Bronze MS, et al: Fluvastatin interferes with hepatitis C virus replication via microtubule bundling and a doublecortin-like kinase-mediated mechanism. PLoS One. 8:e803042013. View Article : Google Scholar : PubMed/NCBI | |
|
Pattabiraman DR and Weinberg RA: Tackling the cancer stem cells-what challenges do they pose? Nat Rev Drug Discov. 13:497–512. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Brooks MD, Burness ML and Wicha MS: Therapeutic implications of cellular heterogeneity and plasticity in breast cancer. Cell Stem Cell. 17:260–271. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Weygant N, Qu D, Berry WL, May R, Chandrakesan P, 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. Mol Cancer. 13:1032014. View Article : Google Scholar : PubMed/NCBI | |
|
Ferguson FM, Nabet B, Raghavan S, Liu Y, Leggett AL, Kuljanin M, Kalekar RL, Yang A, He S, Wang J, et al: Discovery of a selective inhibitor of doublecortin like kinase 1. Nat Chem Biol. 16:635–643. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Sureban SM, Berahovich R, Zhou H, Xu S, Wu L, Ding K, May R, Qu D, Bannerman-Menson E, Golubovskaya V and Houchen CW: DCLK1 monoclonal antibody-based CAR-T cells as a novel treatment strategy against human colorectal cancers. Cancers (Basel). 12:542019. View Article : Google Scholar : PubMed/NCBI | |
|
Cao Z, Weygant N, Chandrakesan P, Houchen CW, Peng J and Qu D: Tuft and cancer stem cell marker DCLK1: A new target to enhance anti-tumor immunity in the tumor microenvironment. Cancers (Basel). 12:38012020. View Article : Google Scholar : PubMed/NCBI | |
|
Chae YC and Kim JH: Cancer stem cell metabolism: Target for cancer therapy. BMB Rep. 51:319–326. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Sancho P, Barneda D and Heeschen C: Hallmarks of cancer stem cell metabolism. Br J Cancer. 114:1305–1312. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Verissimo CS, Elands R, Cheng S, Saaltink DJ, ter Horst JP, Alme MN, Pont C, van de Water B, Håvik B, Fitzsimons CP and Vreugdenhil E: Silencing of doublecortin-like (DCL) results in decreased mitochondrial activity and delayed neuroblastoma tumor growth. PLoS One. 8:e757522013. View Article : Google Scholar : PubMed/NCBI | |
|
Patel O, Roy MJ, Kropp A, Hardy JM, Dai W and Lucet IS: Structural basis for small molecule targeting of doublecortin like kinase 1 with DCLK1-IN-1. Commun Biol. 4:11052021. View Article : Google Scholar : PubMed/NCBI | |
|
Oliveras-Ferraros C, Vazquez-Martin A, Cuyàs E, Corominas-Faja B, Rodríguez-Gallego E, Fernández-Arroyo S, Martin-Castillo B, Joven J and Menendez JA: Acquired resistance to metformin in breast cancer cells triggers transcriptome reprogramming toward a degradome-related metastatic stem-like profile. Cell Cycle. 13:1132–1144. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Nakane T, Ido A, Higuchi T, Todaka H, Morisawa K, Nagamine T, Fukunaga K, Sakamoto S, Murao K and Sugiyama Y: Candidate plasticity gene 16 mediates suppression of insulin gene expression in rat insulinoma INS-1 cells under glucotoxic conditions. Biochem Biophys Res Commun. 512:189–195. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Nakane T, Matsumoto S, Iida S, Ido A, Fukunaga K, Murao K and Sugiyama Y: Candidate plasticity gene 16 and jun dimerization protein 2 are involved in the suppression of insulin gene expression in rat pancreatic INS-1 β-cells. Mol Cell Endocrinol. 527:1112402021. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao H, Duan Q, Zhang Z, Li H, Wu H, Shen Q, Wang C and Yin T: Up-regulation of glycolysis promotes the stemness and EMT phenotypes in gemcitabine-resistant pancreatic cancer cells. J Cell Mol Med. 21:2055–2067. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Ponnurangam S, Mammen JM, Ramalingam S, He Z, Zhang Y, Umar S, Subramaniam D and Anant S: Honokiol in combination with radiation targets notch signaling to inhibit colon cancer stem cells. Mol Cancer Ther. 11:963–972. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Ahmed I, Roy BC, Rao Jakkula LUM, Subramaniam D, Dandawate P, Anant S, Sampath V and Umar S: Infection-induced signals generated at the plasma membrane epigenetically regulate Wnt signaling in vitro and in vivo. J Biol Chem. 295:1021–1035. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Dandawate P, Subramaniam D, Panovich P, Standing D, Krishnamachary B, Kaushik G, Thomas SM, Dhar A, Weir SJ, Jensen RA and Anant S: Cucurbitacin B and I inhibits colon cancer growth by targeting the Notch signaling pathway. Sci Rep. 10:12902020. View Article : Google Scholar : PubMed/NCBI | |
|
Sameri S, Saidijam M, Bahreini F and Najafi R: Cancer chemopreventive activities of silibinin on colorectal cancer through regulation of E-cadherin/β-catenin pathway. Nutr Cancer. 73:1389–1399. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
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 a DCLK1-dependent mechanism. Cancer Lett. 351:151–161. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Kato H, Tateishi K, Fujiwara H, Ijichi H, Yamamoto K, Nakatsuka T, Kakiuchi M, Sano M, Kudo Y, Hayakawa Y, et al: Deletion of histone methyltransferase G9a suppresses mutant kras-driven pancreatic carcinogenesis. Cancer Genomics Proteomics. 17:695–705. 2020. View Article : Google Scholar : PubMed/NCBI |
