RETRACTED ARTICLE: Dclk1, a tumor stem cell marker, regulates pro-survival signaling and self-renewal of intestinal tumor cells

Abstract Background More than 80% of intestinal neoplasia is associated with the adenomatous polyposis coli (APC) mutation. Doublecortin-like kinase 1 (Dclk1), a kinase protein, is overexpressed in colorectal cancer and specifically marks tumor stem cells (TSCs) that self-renew and increased the tum...

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Main Authors: Parthasarathy Chandrakesan, Jiannan Yao, Dongfeng Qu, Randal May, Nathaniel Weygant, Yang Ge, Naushad Ali, Sripathi M. Sureban, Modhi Gude, Kenneth Vega, Eddie Bannerman-Menson, Lijun Xia, Michael Bronze, Guangyu An, Courtney W. Houchen
Format: Article
Language:English
Published: BMC 2017-02-01
Series:Molecular Cancer
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Online Access:https://doi.org/10.1186/s12943-017-0594-y
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author Parthasarathy Chandrakesan
Jiannan Yao
Dongfeng Qu
Randal May
Nathaniel Weygant
Yang Ge
Naushad Ali
Sripathi M. Sureban
Modhi Gude
Kenneth Vega
Eddie Bannerman-Menson
Lijun Xia
Michael Bronze
Guangyu An
Courtney W. Houchen
author_facet Parthasarathy Chandrakesan
Jiannan Yao
Dongfeng Qu
Randal May
Nathaniel Weygant
Yang Ge
Naushad Ali
Sripathi M. Sureban
Modhi Gude
Kenneth Vega
Eddie Bannerman-Menson
Lijun Xia
Michael Bronze
Guangyu An
Courtney W. Houchen
author_sort Parthasarathy Chandrakesan
collection DOAJ
description Abstract Background More than 80% of intestinal neoplasia is associated with the adenomatous polyposis coli (APC) mutation. Doublecortin-like kinase 1 (Dclk1), a kinase protein, is overexpressed in colorectal cancer and specifically marks tumor stem cells (TSCs) that self-renew and increased the tumor progeny in ApcMin/+ mice. However, the role of Dclk1 expression and its contribution to regulating pro-survival signaling for tumor progression in Apc mutant cancer is poorly understood. Methods We analyzed DCLK1 and pro-survival signaling gene expression datasets of 329 specimens from TCGA Colon Adenocarcinoma Cancer Data. The network of DCLK1 and pro-survival signaling was analyzed utilizing the GeneMANIA database. We examined the expression levels of Dclk1 and other stem cell-associated markers, pro-survival signaling pathways, cell self-renewal in the isolated intestinal epithelial cells of ApcMin/+mice with high-grade dysplasia and adenocarcinoma. To determine the functional role of Dclk1 for tumor progression, we knocked down Dclk1 and determined the pro-survival signaling pathways and stemness. We used siRNA technology to gene silence pro-survival signaling in colon cancer cells in vitro. We utilized FACS, IHC, western blot, RT-PCR, and clonogenic (self-renewal) assays. Results We found a correlation between DCLK1 and pro-survival signaling expression. The expression of Dclk1 and stem cell-associated markers Lgr5, Bmi1, and Musashi1 were significantly higher in the intestinal epithelial cells of ApcMin/+mice than in wild-type controls. Intestinal epithelial cells of ApcMin/+mice showed increased expression of pro-survival signaling, pluripotency and self-renewal ability. Furthermore, the enteroids formed from the intestinal Dclk1+ cells of ApcMin/+mice display higher pluripotency and pro-survival signaling. Dclk1 knockdown in ApcMin/+ mice attenuates intestinal adenomas and adenocarcinoma, and decreases pro-survival signaling and self-renewal. Knocking down RELA and NOTCH1 pro-survival signaling and DCLK1 in HT29 and DLD1 colon cancer cells in vitro reduced the tumor cells’ ability to self-renew and survive. Conclusion Our results indicate that Dclk1 is essential in advancing intestinal tumorigenesis. Knocking down Dclk1 decreases tumor stemness and progression and is thus predicted to regulate pro-survival signaling and tumor cell pluripotency. This study provides a strong rationale to target Dclk1 as a treatment strategy for colorectal cancer.
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spelling doaj-art-fb5fbd23ffd544bda50fcf17577992852025-08-20T02:20:01ZengBMCMolecular Cancer1476-45982017-02-0116111410.1186/s12943-017-0594-yRETRACTED ARTICLE: Dclk1, a tumor stem cell marker, regulates pro-survival signaling and self-renewal of intestinal tumor cellsParthasarathy Chandrakesan0Jiannan Yao1Dongfeng Qu2Randal May3Nathaniel Weygant4Yang Ge5Naushad Ali6Sripathi M. Sureban7Modhi Gude8Kenneth Vega9Eddie Bannerman-Menson10Lijun Xia11Michael Bronze12Guangyu An13Courtney W. Houchen14Division of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterCOARE BiotechnologyOklahoma Medical Research FoundationDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterBeijing Chao-Yang Hospital Department of Oncology, Capital Medical UniversityDivision of Digestive Diseases and Nutrition, Department of Medicine, University of Oklahoma Health Sciences CenterAbstract Background More than 80% of intestinal neoplasia is associated with the adenomatous polyposis coli (APC) mutation. Doublecortin-like kinase 1 (Dclk1), a kinase protein, is overexpressed in colorectal cancer and specifically marks tumor stem cells (TSCs) that self-renew and increased the tumor progeny in ApcMin/+ mice. However, the role of Dclk1 expression and its contribution to regulating pro-survival signaling for tumor progression in Apc mutant cancer is poorly understood. Methods We analyzed DCLK1 and pro-survival signaling gene expression datasets of 329 specimens from TCGA Colon Adenocarcinoma Cancer Data. The network of DCLK1 and pro-survival signaling was analyzed utilizing the GeneMANIA database. We examined the expression levels of Dclk1 and other stem cell-associated markers, pro-survival signaling pathways, cell self-renewal in the isolated intestinal epithelial cells of ApcMin/+mice with high-grade dysplasia and adenocarcinoma. To determine the functional role of Dclk1 for tumor progression, we knocked down Dclk1 and determined the pro-survival signaling pathways and stemness. We used siRNA technology to gene silence pro-survival signaling in colon cancer cells in vitro. We utilized FACS, IHC, western blot, RT-PCR, and clonogenic (self-renewal) assays. Results We found a correlation between DCLK1 and pro-survival signaling expression. The expression of Dclk1 and stem cell-associated markers Lgr5, Bmi1, and Musashi1 were significantly higher in the intestinal epithelial cells of ApcMin/+mice than in wild-type controls. Intestinal epithelial cells of ApcMin/+mice showed increased expression of pro-survival signaling, pluripotency and self-renewal ability. Furthermore, the enteroids formed from the intestinal Dclk1+ cells of ApcMin/+mice display higher pluripotency and pro-survival signaling. Dclk1 knockdown in ApcMin/+ mice attenuates intestinal adenomas and adenocarcinoma, and decreases pro-survival signaling and self-renewal. Knocking down RELA and NOTCH1 pro-survival signaling and DCLK1 in HT29 and DLD1 colon cancer cells in vitro reduced the tumor cells’ ability to self-renew and survive. Conclusion Our results indicate that Dclk1 is essential in advancing intestinal tumorigenesis. Knocking down Dclk1 decreases tumor stemness and progression and is thus predicted to regulate pro-survival signaling and tumor cell pluripotency. This study provides a strong rationale to target Dclk1 as a treatment strategy for colorectal cancer.https://doi.org/10.1186/s12943-017-0594-yDclk1APC mutationCancer stem cellsIntestinal epithelial cellsPro-survival signalingSelf-renewal
spellingShingle Parthasarathy Chandrakesan
Jiannan Yao
Dongfeng Qu
Randal May
Nathaniel Weygant
Yang Ge
Naushad Ali
Sripathi M. Sureban
Modhi Gude
Kenneth Vega
Eddie Bannerman-Menson
Lijun Xia
Michael Bronze
Guangyu An
Courtney W. Houchen
RETRACTED ARTICLE: Dclk1, a tumor stem cell marker, regulates pro-survival signaling and self-renewal of intestinal tumor cells
Molecular Cancer
Dclk1
APC mutation
Cancer stem cells
Intestinal epithelial cells
Pro-survival signaling
Self-renewal
title RETRACTED ARTICLE: Dclk1, a tumor stem cell marker, regulates pro-survival signaling and self-renewal of intestinal tumor cells
title_full RETRACTED ARTICLE: Dclk1, a tumor stem cell marker, regulates pro-survival signaling and self-renewal of intestinal tumor cells
title_fullStr RETRACTED ARTICLE: Dclk1, a tumor stem cell marker, regulates pro-survival signaling and self-renewal of intestinal tumor cells
title_full_unstemmed RETRACTED ARTICLE: Dclk1, a tumor stem cell marker, regulates pro-survival signaling and self-renewal of intestinal tumor cells
title_short RETRACTED ARTICLE: Dclk1, a tumor stem cell marker, regulates pro-survival signaling and self-renewal of intestinal tumor cells
title_sort retracted article dclk1 a tumor stem cell marker regulates pro survival signaling and self renewal of intestinal tumor cells
topic Dclk1
APC mutation
Cancer stem cells
Intestinal epithelial cells
Pro-survival signaling
Self-renewal
url https://doi.org/10.1186/s12943-017-0594-y
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