Cystatin D is a candidate tumor suppressor gene induced by vitamin D in human colon cancer cells
The active vitamin D metabolite 1alpha,25-dihydroxyvitamin D3 [1alpha,25(OH)2D3] has wide but not fully understood antitumor activity. A previous transcriptomic analysis of 1alpha,25(OH)2D3 action on human colon cancer cells revealed cystatin D (CST5), which encodes an inhibitor of several cysteine...
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Published in | The Journal of clinical investigation Vol. 119; no. 8; pp. 2343 - 2358 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
American Society for Clinical Investigation
01.08.2009
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Abstract | The active vitamin D metabolite 1alpha,25-dihydroxyvitamin D3 [1alpha,25(OH)2D3] has wide but not fully understood antitumor activity. A previous transcriptomic analysis of 1alpha,25(OH)2D3 action on human colon cancer cells revealed cystatin D (CST5), which encodes an inhibitor of several cysteine proteases of the cathepsin family, as a candidate target gene. Here we report that 1alpha,25(OH)2D3 induced vitamin D receptor (VDR) binding to, and activation of, the CST5 promoter and increased CST5 RNA and protein levels in human colon cancer cells. In cells lacking endogenous cystatin D, ectopic cystatin D expression inhibited both proliferation in vitro and xenograft tumor growth in vivo. Furthermore, cystatin D inhibited migration and anchorage-independent growth, antagonized the Wnt/beta-catenin signaling pathway, and repressed c-MYC expression. Cystatin D repressed expression of the epithelial-mesenchymal transition inducers SNAI1, SNAI2, ZEB1, and ZEB2 and, conversely, induced E-cadherin and other adhesion proteins. CST5 knockdown using shRNA abrogated the antiproliferative effect of 1alpha,25(OH)2D3, attenuated E-cadherin expression, and increased c-MYC expression. In human colorectal tumors, expression of cystatin D correlated with expression of VDR and E-cadherin, and loss of cystatin D correlated with poor tumor differentiation. Based on these data, we propose that CST5 has tumor suppressor activity that may contribute to the antitumoral action of 1alpha,25(OH)2D3 in colon cancer. |
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AbstractList | The active vitamin D metabolite 1alpha,25-dihydroxyvitamin D3 [1alpha,25(OH)2D3] has wide but not fully understood antitumor activity. A previous transcriptomic analysis of 1alpha,25(OH)2D3 action on human colon cancer cells revealed cystatin D (CST5), which encodes an inhibitor of several cysteine proteases of the cathepsin family, as a candidate target gene. Here we report that 1alpha,25(OH)2D3 induced vitamin D receptor (VDR) binding to, and activation of, the CST5 promoter and increased CST5 RNA and protein levels in human colon cancer cells. In cells lacking endogenous cystatin D, ectopic cystatin D expression inhibited both proliferation in vitro and xenograft tumor growth in vivo. Furthermore, cystatin D inhibited migration and anchorage-independent growth, antagonized the Wnt/beta-catenin signaling pathway, and repressed c-MYC expression. Cystatin D repressed expression of the epithelial-mesenchymal transition inducers SNAI1, SNAI2, ZEB1, and ZEB2 and, conversely, induced E-cadherin and other adhesion proteins. CST5 knockdown using shRNA abrogated the antiproliferative effect of 1alpha,25(OH)2D3, attenuated E-cadherin expression, and increased c-MYC expression. In human colorectal tumors, expression of cystatin D correlated with expression of VDR and E-cadherin, and loss of cystatin D correlated with poor tumor differentiation. Based on these data, we propose that CST5 has tumor suppressor activity that may contribute to the antitumoral action of 1alpha,25(OH)2D3 in colon cancer. The active vitamin D metabolite 1α,25-dihydroxyvitamin [D.sub.3] [1α,25[(OH).sub.2][D.sub.3] has wide but not fully understood antitumor activity. A previous transcriptomic analysis of 1α,25[(OH).sub.2][D.sub.3] action on human colon cancer cells revealed cystatin D (CST5), which encodes an inhibitor of several cysteine proteases of the cathepsin family, as a candidate target gene. Here we report that 1α,25[(OH).sub.2][D.sub.3] induced vitamin D receptor (VDR) binding to, and activation of, the CST5 promoter and increased CST5 RNA and protein levels in human colon cancer cells. In cells lacking endogenous cystatin D, ectopic cystatin D expression inhibited both proliferation in vitro and xenograft tumor growth in vivo. Furthermore, cystatin D inhibited migration and anchorage-independent growth, antagonized the Wnt/β-catenin signaling pathway, and repressed c-MYC expression. Cystatin D repressed expression of the epithelial-mesenchymal transition inducers SNAI1, SNAI2, ZEB1, and ZEB2 and, conversely, induced E-cadherin and other adhesion proteins. CST5 knockdown using shRNA abrogated the antiproliferative effect of 1α,25[(OH).sub.2][D.sub.3], attenuated E-cadherin expression, and increased c-MYC expression. In human colorectal tumors, expression of cystatin D correlated with expression of VDR and E-cadherin, and loss of cystatin D correlated with poor tumor differentiation. Based on these data, we propose that CST5 has tumor suppressor activity that may contribute to the antitumoral action of 1α,25[(OH).sub.2][D.sub.3] in colon cancer. The active vitamin D metabolite 1α,25-dihydroxyvitamin D 3 [1α,25(OH) 2 D 3 ] has wide but not fully understood antitumor activity. A previous transcriptomic analysis of 1α,25(OH) 2 D 3 action on human colon cancer cells revealed cystatin D ( CST5 ), which encodes an inhibitor of several cysteine proteases of the cathepsin family, as a candidate target gene. Here we report that 1α,25(OH) 2 D 3 induced vitamin D receptor (VDR) binding to, and activation of, the CST5 promoter and increased CST5 RNA and protein levels in human colon cancer cells. In cells lacking endogenous cystatin D, ectopic cystatin D expression inhibited both proliferation in vitro and xenograft tumor growth in vivo. Furthermore, cystatin D inhibited migration and anchorage-independent growth, antagonized the Wnt/β-catenin signaling pathway, and repressed c-MYC expression. Cystatin D repressed expression of the epithelial-mesenchymal transition inducers SNAI1 , SNAI2 , ZEB1 , and ZEB2 and, conversely, induced E-cadherin and other adhesion proteins. CST5 knockdown using shRNA abrogated the antiproliferative effect of 1α,25(OH) 2 D 3 , attenuated E-cadherin expression, and increased c-MYC expression. In human colorectal tumors, expression of cystatin D correlated with expression of VDR and E-cadherin, and loss of cystatin D correlated with poor tumor differentiation. Based on these data, we propose that CST5 has tumor suppressor activity that may contribute to the antitumoral action of 1α,25(OH) 2 D 3 in colon cancer. |
Audience | Academic |
Author | Freije, José M P García, José Miguel Bonilla, Félix Valle, Noelia Peña, Cristina Astudillo, Aurora López-Otín, Carlos Alvarez-Díaz, Silvia Muñoz, Alberto Quesada, Víctor |
AuthorAffiliation | 1 Instituto de Investigaciones Biomédicas “Alberto Sols,” Consejo Superior de Investigaciones Científicas–Universidad Autónoma de Madrid, Madrid, Spain. 2 Hospital Universitario Puerta de Hierro, Madrid, Spain. 3 Departamento de Bioquímica y Biología Molecular, Facultad de Medicina, Instituto Universitario de Oncología, Universidad de Oviedo, Oviedo, Spain. 4 Servicio de Anatomía Patológica, Instituto Universitario de Oncología, Hospital Universitario Central de Asturias, Oviedo, Spain |
AuthorAffiliation_xml | – name: 1 Instituto de Investigaciones Biomédicas “Alberto Sols,” Consejo Superior de Investigaciones Científicas–Universidad Autónoma de Madrid, Madrid, Spain. 2 Hospital Universitario Puerta de Hierro, Madrid, Spain. 3 Departamento de Bioquímica y Biología Molecular, Facultad de Medicina, Instituto Universitario de Oncología, Universidad de Oviedo, Oviedo, Spain. 4 Servicio de Anatomía Patológica, Instituto Universitario de Oncología, Hospital Universitario Central de Asturias, Oviedo, Spain |
Author_xml | – sequence: 1 givenname: Silvia surname: Alvarez-Díaz fullname: Alvarez-Díaz, Silvia organization: Instituto de Investigaciones Biomédicas Alberto Sols, Consejo Superior de Investigaciones Científicas-Universidad Autónoma de Madrid, Madrid, Spain – sequence: 2 givenname: Noelia surname: Valle fullname: Valle, Noelia – sequence: 3 givenname: José Miguel surname: García fullname: García, José Miguel – sequence: 4 givenname: Cristina surname: Peña fullname: Peña, Cristina – sequence: 5 givenname: José M P surname: Freije fullname: Freije, José M P – sequence: 6 givenname: Víctor surname: Quesada fullname: Quesada, Víctor – sequence: 7 givenname: Aurora surname: Astudillo fullname: Astudillo, Aurora – sequence: 8 givenname: Félix surname: Bonilla fullname: Bonilla, Félix – sequence: 9 givenname: Carlos surname: López-Otín fullname: López-Otín, Carlos – sequence: 10 givenname: Alberto surname: Muñoz fullname: Muñoz, Alberto |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/19662683$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2009 American Society for Clinical Investigation Copyright American Society for Clinical Investigation Aug 2009 Copyright © 2009, American Society for Clinical Investigation |
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Snippet | The active vitamin D metabolite 1alpha,25-dihydroxyvitamin D3 [1alpha,25(OH)2D3] has wide but not fully understood antitumor activity. A previous... The active vitamin D metabolite 1α,25-dihydroxyvitamin [D.sub.3] [1α,25[(OH).sub.2][D.sub.3] has wide but not fully understood antitumor activity. A previous... The active vitamin D metabolite 1α,25-dihydroxyvitamin D 3 [1α,25(OH) 2 D 3 ] has wide but not fully understood antitumor activity. A previous transcriptomic... |
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SubjectTerms | Alfacalcidol beta Catenin - antagonists & inhibitors Biomedical research Cadherins - analysis Calcifediol Calcitriol - pharmacology Care and treatment Cell Cycle Cell Differentiation Cell growth Cell Line, Tumor Cell Movement - drug effects Cell Proliferation - drug effects Chemical properties Colon cancer Colonic Neoplasms - genetics Colonic Neoplasms - pathology Colorectal cancer Cystatins - genetics Cystatins - physiology Epithelium - pathology Gene expression Genes Genes, myc Genes, Tumor Suppressor - physiology Genetic aspects Health aspects Humans Mesoderm - pathology Promoter Regions, Genetic Proteins Receptors, Calcitriol - analysis Tumor suppressor genes Tumors Vitamin D |
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Title | Cystatin D is a candidate tumor suppressor gene induced by vitamin D in human colon cancer cells |
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