Epidermal Growth Factor Receptor–Mediated Membrane Type 1 Matrix Metalloproteinase Endocytosis Regulates the Transition between Invasive versus Expansive Growth of Ovarian Carcinoma Cells in Three-Dimensional Collagen

Moss, Natalie M.; Liu, Yueying; Johnson, Jeff J.; Debiase, Philip; Jones, Jonathan; Hudson, Laurie G.; Munshi, Hidayatullah G.; Stack, M. Sharon

doi:10.1158/1541-7786.mcr-08-0571

Cited by 31 publications

(28 citation statements)

References 108 publications

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“…1E). These results are in agreement with numerous studies demonstrating the relationship between phenotypic three-dimensional spheroid formation with cell migration and invasion (28,29). Thus, our results suggest that SPDEF modulation effects cell migration and invasion, namely when SPDEF expression is high, cells are less motile and invasive, and conversely, when SPDEF expression is low, cells demonstrate increased motility and invasion.…”

Section: Stable Expression Of Spdef Decreases Whereas Spdef Knockdowsupporting

confidence: 93%

The Transcription Factor SPDEF Suppresses Prostate Tumor Metastasis

Steffan

Koul

Meacham

et al. 2012

Journal of Biological Chemistry

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Section: Stable Expression Of Spdef Decreases Whereas Spdef Knockdowsupporting

confidence: 93%

The Transcription Factor SPDEF Suppresses Prostate Tumor Metastasis

Steffan

Koul

Meacham

et al. 2012

Journal of Biological Chemistry

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“…The pattern of tumor cell growth in collagen can occur either invasively or as an expansive, adhesive mass, which may in part depend on MT1-MMP surface levels and activity [38]. In contrast, recombinant MT3-MMP is a poor type I collagenase [16] and unable to drive cell invasion through native polymerized collagen type I matrix [17], [33], although MT3-MMP itself has also been implicated in the remodeling of 3D collagen [40], 41.…”

Section: Discussionmentioning

confidence: 99%

Membrane-Type-3 Matrix Metalloproteinase (MT3-MMP) Functions as a Matrix Composition-Dependent Effector of Melanoma Cell Invasion

et al. 2011

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In primary human melanoma, the membrane-type matrix metalloproteinase, MT3-MMP, is overexpressed in the most aggressive nodular-type tumors. Unlike MT1-MMP and MT2-MMP, which promote cell invasion through basement membranes and collagen type I-rich tissues, the function of MT3-MMP in tumor progression remains unclear. Here, we demonstrate that MT3-MMP inhibits MT1-MMP-driven melanoma cell invasion in three-dimensional collagen, while yielding an altered, yet MT1-MMP-dependent, form of expansive growth behavior that phenocopies the formation of nodular cell colonies. In melanoma cell lines originating from advanced primary or metastatic lesions, endogenous MT3-MMP expression was associated with limited collagen-invasive potential. In the cell lines with highest MT3-MMP expression relative to MT1-MMP, collagen-invasive activity was increased following stable MT3-MMP gene silencing. Consistently, MT3-MMP overexpression in cells derived from less advanced superficially spreading melanoma lesions, or in the MT3-MMP knockdown cells, reduced MT1-MMP-dependent collagen invasion. Rather than altering MT1-MMP transcription, MT3-MMP interacted with MT1-MMP in membrane complexes and reduced its cell surface expression. By contrast, as a potent fibrinolytic enzyme, MT3-MMP induced efficient invasion of the cells in fibrin, a provisional matrix component frequently found at tumor-host tissue interfaces and perivascular spaces of melanoma. Since MT3-MMP was significantly upregulated in biopsies of human melanoma metastases, these results identify MT3-MMP as a matrix-dependent modifier of the invasive tumor cell functions during melanoma progression.

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“…Collagen type I, a native ECM component produced by cells in the stromal environment, influences the growth and metastasis of resident cancer cells (Moss et al, 2009). Collagen can be collected from various biological sources including bovine skin, rat tail and human placenta (Elsdale and Bard, 1972; Pacak et al, 2014).…”

Section: Matrix-assisted Assembly Of 3d Tumor Modelsmentioning

confidence: 99%

Three-dimensional in vitro tumor models for cancer research and drug evaluation

Farach-Carson

Jia

2014

Biotechnology Advances

394

294

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Cancer occurs when cells acquire genomic instability and inflammation, produce abnormal levels of epigenetic factors/proteins and tumor suppressors, reprogram the energy metabolism and evade immune destruction, leading to the disruption of cell cycle/normal growth. An early event in carcinogenesis is loss of polarity and detachment from the natural basement membrane, allowing cells to form distinct three-dimensional (3D) structures that interact with each other and with the surrounding microenvironment. Although valuable information has been accumulated from traditional in vitro studies in which cells are grown on flat and hard plastic surfaces (2D culture), this culture condition does not reflect the essential features of tumor tissues. Further, fundamental understanding of cancer metastasis cannot be obtained readily from 2D studies because they lack the complex and dynamic cell-cell communications and cell-matrix interactions that occur during cancer metastasis. These shortcomings, along with lack of spatial depth and cell connectivity, limit the applicability of 2D cultures to accurate testing of pharmacologically active compounds, free or sequestered in nanoparticles. To recapitulate features of native tumor microenvironments, various biomimetic 3D tumor models have been developed to incorporate cancer and stromal cells, relevant matrix components, and biochemical and biophysical cues, into one spatially and temporally integrated system. In this article, we review recent advances in creating 3D tumor models employing tissue engineering principles. We then evaluate the utilities of these novel models for the testing of anticancer drugs and their delivery systems. We highlight the profound differences in responses from 3D in vitro tumors and conventional monolayer cultures. Overall, strategic integration of biological principles and engineering approaches will both improve understanding of tumor progression and invasion and support discovery of more personalized first line treatments for cancer patients.

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Epidermal Growth Factor Receptor–Mediated Membrane Type 1 Matrix Metalloproteinase Endocytosis Regulates the Transition between Invasive versus Expansive Growth of Ovarian Carcinoma Cells in Three-Dimensional Collagen

Cited by 31 publications

References 108 publications

The Transcription Factor SPDEF Suppresses Prostate Tumor Metastasis

The Transcription Factor SPDEF Suppresses Prostate Tumor Metastasis

Membrane-Type-3 Matrix Metalloproteinase (MT3-MMP) Functions as a Matrix Composition-Dependent Effector of Melanoma Cell Invasion

Three-dimensional in vitro tumor models for cancer research and drug evaluation

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