Riding the crest of the wave: parallels between the neural crest and cancer in epithelial‐to‐mesenchymal transition and migration

Focus Article

Davalyn R. Powell, Alex J. Blasky, Steven G. Britt, Kristin B. Artinger

Published Online: Apr 10 2013

DOI: 10.1002/wsbm.1224

Full article on Wiley Online Library: HTML PDF

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Abstract The neural crest (NC) is first induced as an epithelial population of cells at the neural plate border requiring complex signaling between bone morphogenetic protein, Wnt, and fibroblast growth factors to differentiate the neural and NC fate from the epidermis. Remarkably, following induction, these cells undergo an epithelial‐to‐mesenchymal transition (EMT), delaminate from the neural tube, and migrate through various tissue types and microenvironments before reaching their final destination where they undergo terminal differentiation. This process is mirrored in cancer metastasis, where a primary tumor will undergo an EMT before migrating and invading other cell populations to create a secondary tumor site. In recent years, as our understanding of NC EMT and migration has deepened, important new insights into tumorigenesis and metastasis have also been achieved. These discoveries have been driven by the observation that many cancers misregulate developmental genes to reacquire proliferative and migratory states. In this review, we examine how the NC provides an excellent model for studying EMT and migration. These data are discussed from the perspective of the gene regulatory networks that control both NC and cancer cell EMT and migration. Deciphering these processes in a comparative manner will expand our knowledge of the underlying etiology and pathogenesis of cancer and promote the development of novel targeted therapeutic strategies for cancer patients. WIREs Syst Biol Med 2013, 5:511–522. doi: 10.1002/wsbm.1224 This article is categorized under: Biological Mechanisms > Cell Fates Biological Mechanisms > Cell Signaling Developmental Biology > Developmental Processes in Health and Disease

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Comparison of transcriptional regulation in neural crest (NC) cells and cancer cells. The diagram depicts the role of growth factors and their signaling pathways in initiating epithelial‐to‐mesenchymal transition (EMT) and migration in both NC cells and cancer cells. The actions of the specific transcription factors discussed in the text are indicated.

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Pathway analysis showing integration between signaling pathways, transcription factors, and adhesion genes. Wnt and BMP act at the top of the hierarchy to initiate the induction of EMT cascade. The transcriptional network, including Twist1/2, Zeb1/2, Snail1/2, Sox10, and Mitf, is active both in neural crest development and cancer. The transcription factors then interact with adhesion genes on the cell surface including N‐cadherin (N‐cad), E‐cadherin (E‐cad), Occludins (Ocln), Claudins (Cldn), and extracellular matrix proteins such as fibronectin (FN) and intermediate filament proteins such as vimentin (Vim). (The network was built with Ingenuity Pathway Analysis, Ingenuity Systems, Inc., Redwood City, CA and modified in Adobe Illustrator).

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Comparison of migration and guidance in neural crest (NC) cells and cancer cells. The diagram depicts degradation of the extracellular matrix (ECM; red intertwined lines and red broken fragments) and the role of guidance cues (ligands shown as spirals and receptors shown as ) during EMT and migration in NC cells (light blue) and cancer cells (green).

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Comparison of cell adhesion and polarity changes in neural crest (NC) cells and cancer cells. The diagram depicts alterations in tight junction components (circle barbells), adherens junction components (square barbells), and polarity proteins (stars) during epithelial‐to‐mesenchymal transition (EMT) and migration in NC cells (light blue) and cancer cells (green) as they differentiate and migrate away from normal epithelial cells (white). Passage of cells through the basement membrane and disruption of the extracellular matrix (ECM; red intertwined lines and red broken fragments) is indicated.

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