JNK‐ and Fos‐regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila
Open accessAbstract
Loss of the epithelial polarity gene scribble in clones of Drosophila imaginal disc cells can cooperate with Ras signaling to induce malignant tumors. Such mutant tissue overproliferates, resists apoptosis, leaves its place of origin and invades other organs, ultimately causing lethality. We show that increased Jun N-terminal kinase (JNK) signaling resulting from the loss of scribble promotes the movement of transformed cells to secondary sites. This effect requires Fos-dependent transcriptional activation of a matrix metalloprotease gene mmp1 downstream of JNK. Expression of the Mmp inhibitor Timp or Mmp RNAi knockdown suppresses cell invasiveness. The proinvasive function of the JNK pathway is revealed in a tumor context when active Ras signaling prevents the apoptotic response to JNK activity as it occurs in nontransformed cells. Based on these results, we present a model that explains the oncogenic cooperation between JNK and Ras, and describes how aberrant regulation of cell survival, proliferation and mobilization cooperate to incite malignant tumor formation.
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Increased JNK or Yki activity has been linked to tumour growth.
“JNK and Yki are known to interact in a context-dependent manner (12-14,32), and increased JNK or Yki activity has been linked to tumour growth (12,33-35).”
From A Tumour-Specific Molecular Network Promotes Tumour Growth in <i>Drosophila</i> by Enforcing a JNK-YKI Feedforward Loop (2023) · cites this paper as [35]
dFos is required for the JNK-mediated invasiveness of Ras V12, scrib- tumours.
“This conclusion is further strengthened by the finding that dFos, a component of the Drosophila AP-1 ( Drosophila Jun and Fos heterodimer) transcription factor, is required for the JNK-mediated invasiveness of Ras V12 , scrib -tumours (35,55).”
From A Tumour-Specific Molecular Network Promotes Tumour Growth in <i>Drosophila</i> by Enforcing a JNK-YKI Feedforward Loop (2023) · cites this paper as [35]
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- Authors
- Uhlirova, M., & Bohmann, D.
- Affiliations
- University of Rochester Medicine (US)
- Corresponding author
- Bohmann, Dirk
- ORCID
- Bohmann, Dirk
- Venue
- The EMBO Journal
- Published
- 2006-11-02
- Volume
- 25
- Issue
- 22
- Pages
- 5294-5304
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC1636619
- OpenAlex
- W2154073936
- Semantic Scholar
- aa1b0aba91265fa46116ad5b4fb1dda9c95d8fac
- Cited by
- 395
- References
- 62
- Citations by year
- 2026: 13 · 2025: 29 · 2024: 25 · 2023: 17 · 2022: 25 · 2021: 20 · 2020: 23 · 2019: 23 · 2018: 31 · 2017: 21 · 2016: 24 · 2015: 27 · 2014: 25 · 2013: 18 · 2012: 17
- FWCI
- 3.53
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Eye Institute (R01EY014624)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- JNK signaling, MMP-1, matrix metalloproteinases, Ras signaling, tumor invasion, Scribble, epithelial polarity, Drosophila imaginal discs, oncogene cooperation, apoptosis resistance, cell proliferation, tissue inhibitors of metalloproteinases, tumor suppressor
- MeSH terms
- Animals, Cell Movement, Cell Survival, Disease Models, Animal, Drosophila, Membrane Proteins, Models, Biological, Mutation, Neoplasm Invasiveness, Signal Transduction, Cell Polarity, Apoptosis, ras Proteins, Tissue Inhibitor of Metalloproteinases, Matrix Metalloproteinase 1, Drosophila Proteins, JNK Mitogen-Activated Protein Kinases, Cell Proliferation
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