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Human pancreatic stellate cells modulate 3D collagen alignment to promote the migration of pancreatic ductal adenocarcinoma cells

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Abstract

A hallmark of pancreatic ductal adenocarcinoma (PDAC) is the ability for cancer cells to aggressively infiltrate and navigate through a dense stroma during the metastatic process. Key features of the PDAC stroma include an abundant population of activated pancreatic stellate cells (PSCs) and highly aligned collagen fibers; however, important questions remain regarding how collagen becomes aligned and what the biological manifestations are. To better understand how PSCs, aligned collagen, and PDAC cells might cooperate during the transition to invasion, we utilized a microchannel-based in vitro tumor model and advanced imaging technologies to recreate and examine in vivo-like heterotypic interactions. We found that PSCs participate in a collaborative process with cancer cells by orchestrating the alignment of collagen fibers that, in turn, are permissive to enhanced cell migration. Additionally, direct contact between PSCs, collagen, and PDAC cells is critical to invasion and co-migration of both cell types. This suggests PSCs may accompany and assist in navigating PDAC cells through the stromal terrain. Together, our data provides a new role for PSCs in stimulating the metastatic process and underscores the importance of collagen alignment in cancer progression.

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Acknowledgments

The authors would like to acknowledge the Translational Research Initiatives in Pathology Laboratory, Translational Science BioBank, and Experimental Pathology Laboratory for services including histology and tissue acquisition. We also thank Dr. Patricia Keely for useful discussions, and members of the Beebe Lab for help with microchannel fabrication. We acknowledge funding from the Laboratory for Optical and Computational Instrumentation, the UW School of Pharmacy, and the National Institutes of Health (NIH) grant P30 CA014520 to the University of Wisconsin Carbone Cancer Center (for shared services).

Author contributions

CRD, AGL, SMW, KWE, and WJK conceived and designed the study. CRD performed all experiments and analyzed data with support from CRE. CRD, KWE, and WJK wrote the manuscript.

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Authors and Affiliations

  1. Department of Biomedical Engineering, University of Wisconsin, Madison, WI, USA

    Cole R. Drifka, Kevin W. Eliceiri & W. John Kao

  2. Laboratory for Optical and Computational Instrumentation (LOCI), University of Wisconsin, Madison, WI, USA

    Cole R. Drifka, Corinne R. Esquibel & Kevin W. Eliceiri

  3. Morgridge Institute for Research, Madison, WI, USA

    Cole R. Drifka & Kevin W. Eliceiri

  4. Department of Surgical Pathology, University of Wisconsin, Madison, WI, USA

    Agnes G. Loeffler

  5. University of Wisconsin Comprehensive Carbone Cancer Center, Madison, WI, USA

    Agnes G. Loeffler, Sharon M. Weber, Kevin W. Eliceiri & W. John Kao

  6. Department of Surgery, University of Wisconsin, Madison, WI, USA

    Sharon M. Weber & W. John Kao

  7. Faculties of Medicine and Engineering, University of Hong Kong, Pokfulam Road, Pokfulam, Hong Kong

    W. John Kao

Authors
  1. Cole R. Drifka
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  2. Agnes G. Loeffler
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  3. Corinne R. Esquibel
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  4. Sharon M. Weber
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  5. Kevin W. Eliceiri
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Correspondence to W. John Kao.

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Drifka, C.R., Loeffler, A.G., Esquibel, C.R. et al. Human pancreatic stellate cells modulate 3D collagen alignment to promote the migration of pancreatic ductal adenocarcinoma cells. Biomed Microdevices 18, 105 (2016). https://doi.org/10.1007/s10544-016-0128-1

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