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Platelet “first responders” in wound response, cancer, and metastasis

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Abstract

Platelets serve as “first responders” during normal wounding and homeostasis. Arising from bone marrow stem cell lineage megakaryocytes, anucleate platelets can influence inflammation and immune regulation. Biophysically, platelets are optimized due to size and discoid morphology to distribute near vessel walls, monitor vascular integrity, and initiate quick responses to vascular lesions. Adhesion receptors linked to a highly reactive filopodia-generating cytoskeleton maximizes their vascular surface contact allowing rapid response capabilities. Functionally, platelets normally initiate rapid clotting, vasoconstriction, inflammation, and wound biology that leads to sterilization, tissue repair, and resolution. Platelets also are among the first to sense, phagocytize, decorate, or react to pathogens in the circulation. These platelet first responder properties are commandeered during chronic inflammation, cancer progression, and metastasis. Leaky or inflammatory reaction blood vessel genesis during carcinogenesis provides opportunities for platelet invasion into tumors. Cancer is thought of as a non-healing or chronic wound that can be actively aided by platelet mitogenic properties to stimulate tumor growth. This growth ultimately outstrips circulatory support leads to angiogenesis and intravasation of tumor cells into the blood stream. Circulating tumor cells reengage additional platelets, which facilitates tumor cell adhesion, arrest and extravasation, and metastasis. This process, along with the hypercoagulable states associated with malignancy, is amplified by IL6 production in tumors that stimulate liver thrombopoietin production and elevates circulating platelet numbers by thrombopoiesis in the bone marrow. These complex interactions and the “first responder” role of platelets during diverse physiologic stresses provide a useful therapeutic target that deserves further exploration.

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Acknowledgements

Grant and other support

Boone Pickens Distinguished Chair for Early Prevention of Cancer, Duncan Family Institute, Colorectal Cancer Moon Shot, P30CA016672-41, 1R01CA187238-01, 5R01CA172670-03, and 1R01CA184843-01A1, CA177909, and the American Cancer Society Research Professor Award.

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Authors and Affiliations

  1. Department of Gastrointestinal Medical Oncology, M. D. Anderson Cancer Center, Room#: FC10.3004, 1515 Holcombe Boulevard--Unit 0426, Houston, TX, 77030, USA

    David G. Menter, Scott Kopetz & Jonathan M. Loree

  2. Office of the Vice President Cancer Prevention & Population Science, M. D. Anderson Cancer Center, Unit 1370, 1515 Holcombe Boulevard, Houston, TX, 77054, USA

    Ernest Hawk

  3. Gynocologic Oncology & Reproductive Medicine, M. D. Anderson Cancer Center, Unit 1362, 1515 Holcombe Boulevard, Houston, TX, 77054, USA

    Anil K. Sood

  4. Department of Cancer Biology, M. D. Anderson Cancer Center, Unit 1362, 1515 Holcombe Boulevard, Houston, TX, 77054, USA

    Anil K. Sood

  5. Center for RNA Interference and Non-Coding RNA The University of Texas MD Anderson Cancer Center, Houston, TX, 77054, USA

    Anil K. Sood

  6. Department of Medicine, Section of Internal and Cardiovascular Medicine, University of Perugia, Via E. Dal Pozzo, 06126, Perugia, Italy

    Paolo Gresele

  7. Bioactive Lipids Research Program, Department of Pathology, Wayne State University, 431 Chemistry Bldg, 5101 Cass Avenue, Detroit, MI, 48202, USA

    Kenneth V. Honn

  8. Department of Pathology, Wayne State University, 431 Chemistry Bldg, 5101 Cass Avenue, Detroit, MI, 48202, USA

    Kenneth V. Honn

  9. Cancer Biology Division, Wayne State University School of Medicine, 431 Chemistry Bldg, 5101 Cass Avenue, Detroit, MI, 48202, USA

    Kenneth V. Honn

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  1. David G. Menter
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Menter, D.G., Kopetz, S., Hawk, E. et al. Platelet “first responders” in wound response, cancer, and metastasis. Cancer Metastasis Rev 36, 199–213 (2017). https://doi.org/10.1007/s10555-017-9682-0

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