MDM2 Promotes Cell Motility and Invasiveness by Regulating E-Cadherin Degradation

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Published inMolecular and Cellular Biology Vol. 26; no. 19; pp. 7269 - 7282
Main Authors Yang, Jer-Yen, Zong, Cong S., Xia, Weiya, Wei, Yongkun, Ali-Seyed, Mohamed, Li, Zheng, Broglio, Kristine, Berry, Donald A., Hung, Mien-Chie
Format Journal Article
LanguageEnglish
Published United States American Society for Microbiology 01.10.2006
Taylor & Francis
Subjects
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Breast Neoplasms - ultrastructure
Cadherins - metabolism
Cell Movement
Endocytosis - physiology
Endosomes - ultrastructure
Female
Gene Expression
Gene Expression Profiling
HeLa Cells
Humans
Lymph Nodes - pathology
Neoplasm Invasiveness
Neoplasm Metastasis
Protein Binding
Protein Processing, Post-Translational
Protein Transport
Proto-Oncogene Proteins c-mdm2 - metabolism
Tumor Cells, Cultured
Ubiquitin - metabolism
Online AccessGet full text

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Gene amplification and protein overexpression of MDM2, which is often found in certain types of cancers, indicate that MDM2 plays an important role in tumorigenesis. Interestingly, several clinical reports have demonstrated that amplification of the MDM2 gene correlates with the metastatic stage. Using an antibody array assay, we identified E-cadherin as an MDM2-binding protein and confirmed that E-cadherin is a substrate for the MDM2 E3 ubiquitin ligase. We demonstrate that MDM2 interacts in vivo with E-cadherin, resulting in its ubiquitination and degradation. This regulation appears to be clinically relevant, as we found a significant correlation between high MDM2 and low E-cadherin protein levels in resected tumor specimens recovered from breast cancer patients with lymph node metastases. Ectopic expression of MDM2 in breast cancer cells was found to disrupt cell-cell contacts and enhance cell motility and invasive potential. We found that E-cadherin and MDM2 colocalized on the plasma membrane and in the early endosome, where ubiquitin moieties were attached to E-cadherin. Blocking endocytosis with dominant-negative mutants of dynamin abolished the association of MDM2 with E-cadherin, prevented E-cadherin degradation, and attenuated cell motility as observed by fluorescence microscopy. Thus, we provide evidence to support a novel role for MDM2 in regulating cell adhesions by a mechanism that involves degrading and down-regulating the expression of E-cadherin via an endosome pathway. This novel MDM2-regulated pathway is likely to play a biologically relevant role in cancer metastasis.
Gene amplification and protein overexpression of MDM2, which is often found in certain types of cancers, indicate that MDM2 plays an important role in tumorigenesis. Interestingly, several clinical reports have demonstrated that amplification of the MDM2 gene correlates with the metastatic stage. Using an antibody array assay, we identified E-cadherin as an MDM2-binding protein and confirmed that E-cadherin is a substrate for the MDM2 E3 ubiquitin ligase. We demonstrate that MDM2 interacts in vivo with E-cadherin, resulting in its ubiquitination and degradation. This regulation appears to be clinically relevant, as we found a significant correlation between high MDM2 and low E-cadherin protein levels in resected tumor specimens recovered from breast cancer patients with lymph node metastases. Ectopic expression of MDM2 in breast cancer cells was found to disrupt cell-cell contacts and enhance cell motility and invasive potential. We found that E-cadherin and MDM2 colocalized on the plasma membrane and in the early endosome, where ubiquitin moieties were attached to E-cadherin. Blocking endocytosis with dominant-negative mutants of dynamin abolished the association of MDM2 with E-cadherin, prevented E-cadherin degradation, and attenuated cell motility as observed by fluorescence microscopy. Thus, we provide evidence to support a novel role for MDM2 in regulating cell adhesions by a mechanism that involves degrading and down-regulating the expression of E-cadherin via an endosome pathway. This novel MDM2-regulated pathway is likely to play a biologically relevant role in cancer metastasis.Gene amplification and protein overexpression of MDM2, which is often found in certain types of cancers, indicate that MDM2 plays an important role in tumorigenesis. Interestingly, several clinical reports have demonstrated that amplification of the MDM2 gene correlates with the metastatic stage. Using an antibody array assay, we identified E-cadherin as an MDM2-binding protein and confirmed that E-cadherin is a substrate for the MDM2 E3 ubiquitin ligase. We demonstrate that MDM2 interacts in vivo with E-cadherin, resulting in its ubiquitination and degradation. This regulation appears to be clinically relevant, as we found a significant correlation between high MDM2 and low E-cadherin protein levels in resected tumor specimens recovered from breast cancer patients with lymph node metastases. Ectopic expression of MDM2 in breast cancer cells was found to disrupt cell-cell contacts and enhance cell motility and invasive potential. We found that E-cadherin and MDM2 colocalized on the plasma membrane and in the early endosome, where ubiquitin moieties were attached to E-cadherin. Blocking endocytosis with dominant-negative mutants of dynamin abolished the association of MDM2 with E-cadherin, prevented E-cadherin degradation, and attenuated cell motility as observed by fluorescence microscopy. Thus, we provide evidence to support a novel role for MDM2 in regulating cell adhesions by a mechanism that involves degrading and down-regulating the expression of E-cadherin via an endosome pathway. This novel MDM2-regulated pathway is likely to play a biologically relevant role in cancer metastasis.
Author Kristine Broglio
Weiya Xia
Jer-Yen Yang
Zheng Li
Mohamed Ali-Seyed
Mien-Chie Hung
Yongkun Wei
Donald A. Berry
Cong S. Zong
AuthorAffiliation Department of Molecular and Cellular Oncology, 1 Graduate School of Biomedical Sciences, 2 Department of Biostatistics and Applied Mathematics, University of Texas M. D. Anderson Cancer Center, Houston, Texas 77030 3
AuthorAffiliation_xml – name: Department of Molecular and Cellular Oncology, 1 Graduate School of Biomedical Sciences, 2 Department of Biostatistics and Applied Mathematics, University of Texas M. D. Anderson Cancer Center, Houston, Texas 77030 3
Author_xml – sequence: 1
  givenname: Jer-Yen
  surname: Yang
  fullname: Yang, Jer-Yen
  organization: Graduate School of Biomedical Sciences
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  givenname: Cong S.
  surname: Zong
  fullname: Zong, Cong S.
  organization: Department of Molecular and Cellular Oncology
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  givenname: Weiya
  surname: Xia
  fullname: Xia, Weiya
  organization: Department of Molecular and Cellular Oncology
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  givenname: Yongkun
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  fullname: Wei, Yongkun
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  givenname: Mohamed
  surname: Ali-Seyed
  fullname: Ali-Seyed, Mohamed
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  givenname: Zheng
  surname: Li
  fullname: Li, Zheng
  organization: Department of Molecular and Cellular Oncology
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  givenname: Kristine
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  givenname: Donald A.
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  fullname: Berry, Donald A.
  organization: Department of Biostatistics and Applied Mathematics, University of Texas M. D. Anderson Cancer Center
– sequence: 9
  givenname: Mien-Chie
  surname: Hung
  fullname: Hung, Mien-Chie
  email: mhung@mdanderson.org
  organization: Graduate School of Biomedical Sciences
BackLink https://www.ncbi.nlm.nih.gov/pubmed/16980628$$D View this record in MEDLINE/PubMed
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J.-Y.Y. and C.S.Z. contributed equally.
Corresponding author. Mailing address: Department of Molecular and Cellular Oncology, University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Boulevard, Unit 108, Houston, TX 77030. Phone: (713) 792-3668. Fax: (713) 794-0209. E-mail: mhung@mdanderson.org.
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SSID ssj0006903
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Snippet Article Usage Stats Services MCB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley...
Gene amplification and protein overexpression of MDM2, which is often found in certain types of cancers, indicate that MDM2 plays an important role in...
SourceID pubmedcentral
proquest
pubmed
crossref
informaworld
highwire
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 7269
SubjectTerms Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Breast Neoplasms - ultrastructure
Cadherins - metabolism
Cell Movement
Endocytosis - physiology
Endosomes - ultrastructure
Female
Gene Expression
Gene Expression Profiling
HeLa Cells
Humans
Lymph Nodes - pathology
Neoplasm Invasiveness
Neoplasm Metastasis
Protein Binding
Protein Processing, Post-Translational
Protein Transport
Proto-Oncogene Proteins c-mdm2 - metabolism
Tumor Cells, Cultured
Ubiquitin - metabolism
Title MDM2 Promotes Cell Motility and Invasiveness by Regulating E-Cadherin Degradation
URI http://mcb.asm.org/content/26/19/7269.abstract
https://www.tandfonline.com/doi/abs/10.1128/MCB.00172-06
https://www.ncbi.nlm.nih.gov/pubmed/16980628
https://www.proquest.com/docview/19334177
https://www.proquest.com/docview/68862566
https://pubmed.ncbi.nlm.nih.gov/PMC1592879
Volume 26
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