Maintenance of cancer stemness by miR-196b-5p contributes to chemoresistance of colorectal cancer cells via activating STAT3 signaling pathway
Emerging studies indicated that cancer stem cells represent a subpopulation of cells within the tumor that is responsible for chemotherapeutic resistance. However, the underlying mechanism is still not clarified yet. Here we report that miR-196b-5p is dramatically upregulated in CRC tissues and high...
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| Published in | Oncotarget Vol. 8; no. 30; pp. 49807 - 49823 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Impact Journals LLC
25.07.2017
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Emerging studies indicated that cancer stem cells represent a subpopulation of cells within the tumor that is responsible for chemotherapeutic resistance. However, the underlying mechanism is still not clarified yet. Here we report that miR-196b-5p is dramatically upregulated in CRC tissues and high expression of miR-196b-5p correlates with poor survival in CRC patients. Moreover, recurrent gains (amplification) contribute to the miR-196b-5p overexpression in CRC tissues. Silencing miR-196b-5p suppresses spheroids formation ability, the fraction of SP cells, expression of stem cell factors and the mitochondrial potential, and enhances the apoptosis induced by 5-fluorouracil in CRC cells; while ectopic expression of miR-196b-5p yields an opposite effect. In addition, downregulation of miR-196b-5p resensitizes CRC cells to 5-fluorouracil in vivo. Our results further demonstrate that miR-196b-5p promotes stemness and chemoresistance of CRC cells to 5-fluorouracil via targeting negative regulators SOCS1 and SOCS3 of STAT3 signaling pathway, giving rise to activation of STAT3 signaling. Interestingly, miR-196b-5p is highly enriched in the serum exosomes of patients with CRC compared to the healthy control subjects. Thus, our results unravel a novel mechanism of miR-196b-5p implicating in the maintenance of stem cell property and chemotherapeutic resistance in CRC, offering a potential rational registry of anti-miR-196b-5p combining with conventional chemotherapy against CRC. |
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| AbstractList | Emerging studies indicated that cancer stem cells represent a subpopulation of cells within the tumor that is responsible for chemotherapeutic resistance. However, the underlying mechanism is still not clarified yet. Here we report that miR-196b-5p is dramatically upregulated in CRC tissues and high expression of miR-196b-5p correlates with poor survival in CRC patients. Moreover, recurrent gains (amplification) contribute to the miR-196b-5p overexpression in CRC tissues. Silencing miR-196b-5p suppresses spheroids formation ability, the fraction of SP cells, expression of stem cell factors and the mitochondrial potential, and enhances the apoptosis induced by 5-fluorouracil in CRC cells; while ectopic expression of miR-196b-5p yields an opposite effect. In addition, downregulation of miR-196b-5p resensitizes CRC cells to 5-fluorouracil in vivo. Our results further demonstrate that miR-196b-5p promotes stemness and chemoresistance of CRC cells to 5-fluorouracil via targeting negative regulators SOCS1 and SOCS3 of STAT3 signaling pathway, giving rise to activation of STAT3 signaling. Interestingly, miR-196b-5p is highly enriched in the serum exosomes of patients with CRC compared to the healthy control subjects. Thus, our results unravel a novel mechanism of miR-196b-5p implicating in the maintenance of stem cell property and chemotherapeutic resistance in CRC, offering a potential rational registry of anti-miR-196b-5p combining with conventional chemotherapy against CRC. Emerging studies indicated that cancer stem cells represent a subpopulation of cells within the tumor that is responsible for chemotherapeutic resistance. However, the underlying mechanism is still not clarified yet. Here we report that miR-196b-5p is dramatically upregulated in CRC tissues and high expression of miR-196b-5p correlates with poor survival in CRC patients. Moreover, recurrent gains (amplification) contribute to the miR-196b-5p overexpression in CRC tissues. Silencing miR-196b-5p suppresses spheroids formation ability, the fraction of SP cells, expression of stem cell factors and the mitochondrial potential, and enhances the apoptosis induced by 5-fluorouracil in CRC cells; while ectopic expression of miR-196b-5p yields an opposite effect. In addition, downregulation of miR-196b-5p resensitizes CRC cells to 5-fluorouracil in vivo . Our results further demonstrate that miR-196b-5p promotes stemness and chemoresistance of CRC cells to 5-fluorouracil via targeting negative regulators SOCS1 and SOCS3 of STAT3 signaling pathway, giving rise to activation of STAT3 signaling. Interestingly, miR-196b-5p is highly enriched in the serum exosomes of patients with CRC compared to the healthy control subjects. Thus, our results unravel a novel mechanism of miR-196b-5p implicating in the maintenance of stem cell property and chemotherapeutic resistance in CRC, offering a potential rational registry of anti-miR-196b-5p combining with conventional chemotherapy against CRC. Emerging studies indicated that cancer stem cells represent a subpopulation of cells within the tumor that is responsible for chemotherapeutic resistance. However, the underlying mechanism is still not clarified yet. Here we report that miR-196b-5p is dramatically upregulated in CRC tissues and high expression of miR-196b-5p correlates with poor survival in CRC patients. Moreover, recurrent gains (amplification) contribute to the miR-196b-5p overexpression in CRC tissues. Silencing miR-196b-5p suppresses spheroids formation ability, the fraction of SP cells, expression of stem cell factors and the mitochondrial potential, and enhances the apoptosis induced by 5-fluorouracil in CRC cells; while ectopic expression of miR-196b-5p yields an opposite effect. In addition, downregulation of miR-196b-5p resensitizes CRC cells to 5-fluorouracil in vivo. Our results further demonstrate that miR-196b-5p promotes stemness and chemoresistance of CRC cells to 5-fluorouracil via targeting negative regulators SOCS1 and SOCS3 of STAT3 signaling pathway, giving rise to activation of STAT3 signaling. Interestingly, miR-196b-5p is highly enriched in the serum exosomes of patients with CRC compared to the healthy control subjects. Thus, our results unravel a novel mechanism of miR-196b-5p implicating in the maintenance of stem cell property and chemotherapeutic resistance in CRC, offering a potential rational registry of anti-miR-196b-5p combining with conventional chemotherapy against CRC.Emerging studies indicated that cancer stem cells represent a subpopulation of cells within the tumor that is responsible for chemotherapeutic resistance. However, the underlying mechanism is still not clarified yet. Here we report that miR-196b-5p is dramatically upregulated in CRC tissues and high expression of miR-196b-5p correlates with poor survival in CRC patients. Moreover, recurrent gains (amplification) contribute to the miR-196b-5p overexpression in CRC tissues. Silencing miR-196b-5p suppresses spheroids formation ability, the fraction of SP cells, expression of stem cell factors and the mitochondrial potential, and enhances the apoptosis induced by 5-fluorouracil in CRC cells; while ectopic expression of miR-196b-5p yields an opposite effect. In addition, downregulation of miR-196b-5p resensitizes CRC cells to 5-fluorouracil in vivo. Our results further demonstrate that miR-196b-5p promotes stemness and chemoresistance of CRC cells to 5-fluorouracil via targeting negative regulators SOCS1 and SOCS3 of STAT3 signaling pathway, giving rise to activation of STAT3 signaling. Interestingly, miR-196b-5p is highly enriched in the serum exosomes of patients with CRC compared to the healthy control subjects. Thus, our results unravel a novel mechanism of miR-196b-5p implicating in the maintenance of stem cell property and chemotherapeutic resistance in CRC, offering a potential rational registry of anti-miR-196b-5p combining with conventional chemotherapy against CRC. |
| Author | Zhang, Xin Peng, Yao Li, Ronggang Lin, Bihua Ye, Ziyu Zeng, Jincheng Cao, Longbin Wu, Jinhua Li, Xiangyong Zhou, Keyuan Sun, Lixia Liang, Yangfang Ren, Dong Liu, Qiongru Ma, Yan |
| AuthorAffiliation | 3 Department of Pathology, Jiangmen Central Hospital, Affiliated Jiangmen Hospital of Sun Yat-Sen University, Jiangmen, Guangdong Province, 529030, China 6 Department of Clinical Laboratory, Jiangmen Central Hospital, Affiliated Jiangmen Hospital of Sun Yat-Sen University, Jiangmen, Guangdong Province, 529030, China 4 Department of Gastroenterology, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong Province, 510080, China 2 Department of Orthopedic Surgery, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong Province, 510080, China 1 Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China 5 Department of Pathology, Dongguan Hospital Affiliated to Medical College of Jinan University, The Fifth People's Hospital of Dongguan, Dongguan, Guangdong Prov |
| AuthorAffiliation_xml | – name: 2 Department of Orthopedic Surgery, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong Province, 510080, China – name: 1 Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China – name: 5 Department of Pathology, Dongguan Hospital Affiliated to Medical College of Jinan University, The Fifth People's Hospital of Dongguan, Dongguan, Guangdong Province, 523905, China – name: 4 Department of Gastroenterology, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong Province, 510080, China – name: 3 Department of Pathology, Jiangmen Central Hospital, Affiliated Jiangmen Hospital of Sun Yat-Sen University, Jiangmen, Guangdong Province, 529030, China – name: 6 Department of Clinical Laboratory, Jiangmen Central Hospital, Affiliated Jiangmen Hospital of Sun Yat-Sen University, Jiangmen, Guangdong Province, 529030, China |
| Author_xml | – sequence: 1 givenname: Dong surname: Ren fullname: Ren, Dong organization: Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China, Department of Orthopedic Surgery, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong Province, 510080, China – sequence: 2 givenname: Bihua surname: Lin fullname: Lin, Bihua organization: Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China – sequence: 3 givenname: Xin surname: Zhang fullname: Zhang, Xin organization: Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China, Department of Pathology, Jiangmen Central Hospital, Affiliated Jiangmen Hospital of Sun Yat-Sen University, Jiangmen, Guangdong Province, 529030, China – sequence: 4 givenname: Yao surname: Peng fullname: Peng, Yao organization: Department of Gastroenterology, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong Province, 510080, China – sequence: 5 givenname: Ziyu surname: Ye fullname: Ye, Ziyu organization: Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China – sequence: 6 givenname: Yan surname: Ma fullname: Ma, Yan organization: Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China – sequence: 7 givenname: Yangfang surname: Liang fullname: Liang, Yangfang organization: Department of Pathology, Dongguan Hospital Affiliated to Medical College of Jinan University, The Fifth People's Hospital of Dongguan, Dongguan, Guangdong Province, 523905, China – sequence: 8 givenname: Longbin surname: Cao fullname: Cao, Longbin organization: Department of Gastroenterology, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong Province, 510080, China – sequence: 9 givenname: Xiangyong surname: Li fullname: Li, Xiangyong organization: Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China – sequence: 10 givenname: Ronggang surname: Li fullname: Li, Ronggang organization: Department of Pathology, Jiangmen Central Hospital, Affiliated Jiangmen Hospital of Sun Yat-Sen University, Jiangmen, Guangdong Province, 529030, China – sequence: 11 givenname: Lixia surname: Sun fullname: Sun, Lixia organization: Department of Pathology, Jiangmen Central Hospital, Affiliated Jiangmen Hospital of Sun Yat-Sen University, Jiangmen, Guangdong Province, 529030, China – sequence: 12 givenname: Qiongru surname: Liu fullname: Liu, Qiongru organization: Department of Pathology, Jiangmen Central Hospital, Affiliated Jiangmen Hospital of Sun Yat-Sen University, Jiangmen, Guangdong Province, 529030, China – sequence: 13 givenname: Jinhua surname: Wu fullname: Wu, Jinhua organization: Department of Clinical Laboratory, Jiangmen Central Hospital, Affiliated Jiangmen Hospital of Sun Yat-Sen University, Jiangmen, Guangdong Province, 529030, China – sequence: 14 givenname: Keyuan surname: Zhou fullname: Zhou, Keyuan organization: Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China – sequence: 15 givenname: Jincheng surname: Zeng fullname: Zeng, Jincheng organization: Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Key Laboratory of Medical Bioactive Molecular Research for Department of Education of Guangdong Province, Guangdong Medical University, Dongguan, Guangdong Province, 523808, China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28591704$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Animals Antineoplastic Agents - pharmacology Cell Line, Tumor Cell Proliferation Colorectal Neoplasms - genetics Colorectal Neoplasms - metabolism Colorectal Neoplasms - mortality Colorectal Neoplasms - pathology Disease Models, Animal Drug Resistance, Neoplasm - genetics Exosomes - metabolism Gene Expression Regulation, Neoplastic Humans Janus Kinase 2 - metabolism Mice MicroRNAs - genetics Models, Biological Neoplastic Stem Cells - drug effects Neoplastic Stem Cells - metabolism Prognosis Research Paper Signal Transduction STAT3 Transcription Factor - metabolism Suppressor of Cytokine Signaling 1 Protein - genetics Suppressor of Cytokine Signaling 3 Protein - genetics Xenograft Model Antitumor Assays |
| Title | Maintenance of cancer stemness by miR-196b-5p contributes to chemoresistance of colorectal cancer cells via activating STAT3 signaling pathway |
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