Erk2 Phosphorylation of Drp1 Promotes Mitochondrial Fission and MAPK-Driven Tumor Growth
Ras is mutated in up to 30% of cancers, including 90% of pancreatic ductal adenocarcinomas, causing it to be constitutively GTP-bound, and leading to activation of downstream effectors that promote a tumorigenic phenotype. As targeting Ras directly is difficult, there is a significant effort to unde...
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| Published in | Molecular cell Vol. 57; no. 3; pp. 537 - 551 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
05.02.2015
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Ras is mutated in up to 30% of cancers, including 90% of pancreatic ductal adenocarcinomas, causing it to be constitutively GTP-bound, and leading to activation of downstream effectors that promote a tumorigenic phenotype. As targeting Ras directly is difficult, there is a significant effort to understand the downstream biological processes that underlie its protumorigenic activity. Here, we show that expression of oncogenic Ras or direct activation of the MAPK pathway leads to increased mitochondrial fragmentation and that blocking this phenotype, through knockdown of the mitochondrial fission-mediating GTPase Drp1, inhibits tumor growth. This fission is driven by Erk2-mediated phosphorylation of Drp1 on Serine 616, and both this phosphorylation and mitochondrial fragmentation are increased in human pancreatic cancer. Finally, this phosphorylation is required for Ras-associated mitochondrial fission, and its inhibition is sufficient to block xenograft growth. Collectively, these data suggest mitochondrial fission may be a target for treating MAPK-driven malignancies.
[Display omitted]
•Drp1 is required for xenograft growth•MAPK promotes mitochondrial fragmentation through Drp1•Erk2 phosphorylates Drp1 to promote mitochondrial fission•Drp1 S616 phosphorylation is required for mitochondrial fission and tumor growth
Mitochondrial function is important for the growth of tumors driven by oncogenic Ras or the MAPK pathway. Kashatus et al. demonstrate that activation of these pathways leads to Mek-dependent phosphorylation of the GTPase Drp1 and subsequent mitochondrial fragmentation. They further demonstrate that inhibition of Drp1 or its phosphorylation blocks tumor growth. |
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| AbstractList | Ras is mutated in up to 30% of cancers, including 90% of pancreatic ductal adenocarcinomas, causing it to be constitutively GTP-bound, and leading to activation of downstream effectors that promote a tumorigenic phenotype. As targeting Ras directly is difficult, there is a significant effort to understand the downstream biological processes that underlie its protumorigenic activity. Here, we show that expression of oncogenic Ras or direct activation of the MAPK pathway leads to increased mitochondrial fragmentation and that blocking this phenotype, through knockdown of the mitochondrial fission-mediating GTPase Drp1, inhibits tumor growth. This fission is driven by Erk2-mediated phosphorylation of Drp1 on Serine 616, and both this phosphorylation and mitochondrial fragmentation are increased in human pancreatic cancer. Finally, this phosphorylation is required for Ras-associated mitochondrial fission, and its inhibition is sufficient to block xenograft growth. Collectively, these data suggest mitochondrial fission may be a target for treating MAPK-driven malignancies.Ras is mutated in up to 30% of cancers, including 90% of pancreatic ductal adenocarcinomas, causing it to be constitutively GTP-bound, and leading to activation of downstream effectors that promote a tumorigenic phenotype. As targeting Ras directly is difficult, there is a significant effort to understand the downstream biological processes that underlie its protumorigenic activity. Here, we show that expression of oncogenic Ras or direct activation of the MAPK pathway leads to increased mitochondrial fragmentation and that blocking this phenotype, through knockdown of the mitochondrial fission-mediating GTPase Drp1, inhibits tumor growth. This fission is driven by Erk2-mediated phosphorylation of Drp1 on Serine 616, and both this phosphorylation and mitochondrial fragmentation are increased in human pancreatic cancer. Finally, this phosphorylation is required for Ras-associated mitochondrial fission, and its inhibition is sufficient to block xenograft growth. Collectively, these data suggest mitochondrial fission may be a target for treating MAPK-driven malignancies. Ras is mutated in up to 30% of cancers, including 90% of pancreatic ductal adenocarcinomas, causing it to be constitutively GTP-bound, and leading to activation of downstream effectors that promote a tumorigenic phenotype. As targeting Ras directly is difficult, there is a significant effort to understand the downstream biological processes that underlie its protumorigenic activity. Here, we show that expression of oncogenic Ras or direct activation of the MAPK pathway leads to increased mitochondrial fragmentation and that blocking this phenotype, through knockdown of the mitochondrial fission-mediating GTPase Drp1, inhibits tumor growth. This fission is driven by Erk2-mediated phosphorylation of Drp1 on Serine 616, and both this phosphorylation and mitochondrial fragmentation are increased in human pancreatic cancer. Finally, this phosphorylation is required for Ras-associated mitochondrial fission, and its inhibition is sufficient to block xenograft growth. Collectively, these data suggest mitochondrial fission may be a target for treating MAPK-driven malignancies. Ras is mutated in up to 30% of cancers, including 90% of pancreatic ductal adenocarcinomas, causing it to be constitutively GTP-bound, and leading to activation of downstream effectors that promote a tumorigenic phenotype. As targeting Ras directly is difficult, there is a significant effort to understand the downstream biological processes that underlie its pro-tumorigenic activity. Here, we show that expression of oncogenic Ras or direct activation of the MAPK pathway leads to increased mitochondrial fragmentation and that blocking this phenotype, through knockdown of the mitochondrial fission-mediating GTPase Drp1, inhibits tumor growth. This fission is driven by Erk2-mediated phosphorylation of Drp1 on Serine 616 and both this phosphorylation and mitochondrial fragmentation are increased in human pancreatic cancer. Finally, this phosphorylation is required for Ras-associated mitochondrial fission and its inhibition is sufficient to block xenograft growth. Collectively, these data suggest mitochondrial fission may be a target for treating MAPK-driven malignancies. Ras is mutated in up to 30% of cancers, including 90% of pancreatic ductal adenocarcinomas, causing it to be constitutively GTP-bound, and leading to activation of downstream effectors that promote a tumorigenic phenotype. As targeting Ras directly is difficult, there is a significant effort to understand the downstream biological processes that underlie its protumorigenic activity. Here, we show that expression of oncogenic Ras or direct activation of the MAPK pathway leads to increased mitochondrial fragmentation and that blocking this phenotype, through knockdown of the mitochondrial fission-mediating GTPase Drp1, inhibits tumor growth. This fission is driven by Erk2-mediated phosphorylation of Drp1 on Serine 616, and both this phosphorylation and mitochondrial fragmentation are increased in human pancreatic cancer. Finally, this phosphorylation is required for Ras-associated mitochondrial fission, and its inhibition is sufficient to block xenograft growth. Collectively, these data suggest mitochondrial fission may be a target for treating MAPK-driven malignancies. [Display omitted] •Drp1 is required for xenograft growth•MAPK promotes mitochondrial fragmentation through Drp1•Erk2 phosphorylates Drp1 to promote mitochondrial fission•Drp1 S616 phosphorylation is required for mitochondrial fission and tumor growth Mitochondrial function is important for the growth of tumors driven by oncogenic Ras or the MAPK pathway. Kashatus et al. demonstrate that activation of these pathways leads to Mek-dependent phosphorylation of the GTPase Drp1 and subsequent mitochondrial fragmentation. They further demonstrate that inhibition of Drp1 or its phosphorylation blocks tumor growth. |
| Author | Kashatus, Jennifer A. Myers, Lindsey J. Sher, Annie Byrne, Frances L. Kashatus, David F. Counter, Christopher M. Hoehn, Kyle L. Nascimento, Aldo |
| AuthorAffiliation | 2 Department of Pharmacology and Cancer Biology, Department of Radiation Oncology, Duke University Medical Center, Durham, NC 27710 3 Department of Pharmacology, University of Virginia Health System, Charlottesville, VA 22908 1 Department of Microbiology, Immunology and Cancer Biology, University of Virginia Health System, Charlottesville, VA 22908 |
| AuthorAffiliation_xml | – name: 1 Department of Microbiology, Immunology and Cancer Biology, University of Virginia Health System, Charlottesville, VA 22908 – name: 2 Department of Pharmacology and Cancer Biology, Department of Radiation Oncology, Duke University Medical Center, Durham, NC 27710 – name: 3 Department of Pharmacology, University of Virginia Health System, Charlottesville, VA 22908 |
| Author_xml | – sequence: 1 givenname: Jennifer A. surname: Kashatus fullname: Kashatus, Jennifer A. organization: Department of Microbiology, Immunology and Cancer Biology, University of Virginia Health System, Charlottesville, VA 22908, USA – sequence: 2 givenname: Aldo surname: Nascimento fullname: Nascimento, Aldo organization: Department of Microbiology, Immunology and Cancer Biology, University of Virginia Health System, Charlottesville, VA 22908, USA – sequence: 3 givenname: Lindsey J. surname: Myers fullname: Myers, Lindsey J. organization: Department of Microbiology, Immunology and Cancer Biology, University of Virginia Health System, Charlottesville, VA 22908, USA – sequence: 4 givenname: Annie surname: Sher fullname: Sher, Annie organization: Department of Pharmacology and Cancer Biology, Department of Radiation Oncology, Duke University Medical Center, Durham, NC 27710, USA – sequence: 5 givenname: Frances L. surname: Byrne fullname: Byrne, Frances L. organization: Department of Pharmacology, University of Virginia Health System, Charlottesville, VA 22908, USA – sequence: 6 givenname: Kyle L. surname: Hoehn fullname: Hoehn, Kyle L. organization: Department of Pharmacology, University of Virginia Health System, Charlottesville, VA 22908, USA – sequence: 7 givenname: Christopher M. surname: Counter fullname: Counter, Christopher M. organization: Department of Pharmacology and Cancer Biology, Department of Radiation Oncology, Duke University Medical Center, Durham, NC 27710, USA – sequence: 8 givenname: David F. surname: Kashatus fullname: Kashatus, David F. email: kashatus@virginia.edu organization: Department of Microbiology, Immunology and Cancer Biology, University of Virginia Health System, Charlottesville, VA 22908, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25658205$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | adenocarcinoma Animals Benzamides - pharmacology Cell Line, Tumor Diphenylamine - analogs & derivatives Diphenylamine - pharmacology Gene Knockdown Techniques GTP Phosphohydrolases - genetics GTP Phosphohydrolases - metabolism guanosinetriphosphatase HEK293 Cells HeLa Cells Humans Mice Mice, Nude Microtubule-Associated Proteins - genetics Microtubule-Associated Proteins - metabolism mitochondria Mitochondrial Dynamics - drug effects Mitochondrial Proteins - genetics Mitochondrial Proteins - metabolism mitogen-activated protein kinase Mitogen-Activated Protein Kinase 1 - metabolism Neoplasms, Experimental - metabolism pancreatic neoplasms Pancreatic Neoplasms - metabolism phenotype Phosphorylation ras Proteins - metabolism serine Serine - metabolism |
| Title | Erk2 Phosphorylation of Drp1 Promotes Mitochondrial Fission and MAPK-Driven Tumor Growth |
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