MIEN1, a novel interactor of Annexin A2, promotes tumor cell migration by enhancing AnxA2 cell surface expression
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BACKGROUND: Migration and invasion enhancer 1 (MIEN1) is a novel gene found to be abundantly expressed in breast tumor tissues and functions as a critical regulator of tumor cell migration and invasion to promote systemic metastases. Previous studies have identified post-translational modifications by isoprenylation at the C-terminal tail of MIEN1 to favor its translocation to the inner leaflet of plasma membrane and its function as a membrane-bound adapter molecule. However, the exact molecular events at the membrane interface activating the MIEN1-driven tumor cell motility are vaguely understood. METHODS: MIEN1 was first studied using in-silico analysis on available RNA sequencing data of human breast tissues and its expression was ascertained in breast cells. We performed several assays including co-immunoprecipitation, wound healing, western blotting and immunofluorescence to decipher the molecular events involved in MIEN1-mediated tumor cell migration. RESULTS: Clinically, MIEN1 is predominantly overexpressed in Her-2 and luminal B subtypes of breast tumors, and its increased expression correlates with poor disease free survival. Molecular studies identified a phosphorylation-dependent activation signal in the immunoreceptor tyrosine based activation motif (ITAM) of MIEN1 and the phosphorylation-deficient MIEN1-mutants (Y39F/50 F) to regulate filopodia generation, migration and invasion. We found that ITAM-phosphorylation of MIEN1 is significantly impaired in isoprenylation-deficient MIEN1 mutants indicating that prenylation of MIEN1 and membrane association is required for cross-phosphorylation of tyrosine residues. Furthermore, we identified MIEN1 as a novel interactor of Annexin A2 (AnxA2), a Ca(2+) -dependent phospholipid binding protein, which serves as an extracellular proteolytic center regulating plasmin generation. Fluorescence resonance energy transfer (FRET) confirmed that MIEN1 physically interacts with AnxA2 and functional studies revealed that they mutually cooperate to accentuate tumor cell motility. Interestingly, our study identified that ectopic overexpression of MIEN1 significantly enhances Tyr23-phosphorylation on AnxA2, thereby stimulating cell surface translocation of AnxA2 and catalyzing the activation of its proteolytic activity. CONCLUSION: Our data show that the presence and interaction of both MIEN1 and AnxA2 in breast tumors are crucial drivers of cell motility. Our study has now deciphered a novel regulatory network governing the vicious process of breast tumor cell invasion-metastasis, and findings suggest MIEN1-AnxA2 as prospective targets to counter the deadly disease.
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ANXA2 has previously been shown to regulate cell migration in other disease settings including carcinogenesis.
“ANXA2, which we have identified as a key marker in both human and mouse migratory hepatocytes, has been previously shown to regulate cell migration in other disease settings including carcinogenesis21–23”
From Multimodal decoding of human liver regeneration (2024) · cites this paper as [22]
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- Authors
- Kpetemey, M., Dasgupta, S., Rajendiran, S., Das, S., Gibbs, L. D., Shetty, P., Gryczynski, Z., & Vishwanatha, J. K.
- Affiliations
- University of North Texas Health Science Center (US)
- Corresponding author
- Vishwanatha, Jamboor K.
- ORCID
- Venue
- Molecular Cancer
- Published
- 2015-08-15
- Volume
- 14
- Issue
- 1
- Pages
- 156-156
- ISSN
- 1476-4598 (ISSN-L)
- PMC
- PMC4536591
- OpenAlex
- W2112965924
- Cited by
- 68
- References
- 51
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 11 · 2023: 1 · 2022: 6 · 2021: 8 · 2020: 4 · 2019: 9 · 2018: 5 · 2017: 10 · 2016: 4
- FWCI
- 2.75
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Molecular Cancer (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institute on Minority Health and Health Disparities (1P20 MD006882)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › S100 Proteins and Annexins
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Keywords
- annexin A2, tumor cell migration, breast cancer, isoprenylation, ITAM phosphorylation, filopodia, cell surface translocation, plasminogen activation, protein-protein interaction, metastasis, luminal B, HER2-positive breast cancer, disease-free survival, tyrosine phosphorylation, tumor invasion, proteolytic activity
- MeSH terms
- Animals, Breast Neoplasms, Carrier Proteins, Cell Membrane, Cell Movement, Extracellular Space, Humans, Neoplasm Proteins, Phosphorylation, Protein Binding, Protein Processing, Post-Translational, Gene Expression, Annexin A2, Amino Acid Motifs, Protein Transport, Cell Line, Tumor, Intracellular Signaling Peptides and Proteins, Mice, Protein Interaction Domains and Motifs, Proteolysis
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