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The role of pressure in cancer growth

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Abstract.

The response to external mechanical forces is increasingly seen as a crucial aspect of cancer growth and a topic where the contribution of physics ideas and methods is important. Understanding if tumor progression towards increased malignancy reflects the geometry and mechanics of the microenvironment is an important issue still to be fully explored. In order to grow, tumors have to overcome the mechanical resistance posed by the tissues in which they originate, while cancer cells involved in metastasis are often subject to fluid pressure. Here we review the recent literature describing the role of solid and fluid pressure on tumor growth and progression. We discuss a variety of in vitro experiments as well as computational models used to interpret them. We conclude discussing future perspectives.

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References

  1. Kévin Alessandri, Bibhu Ranjan Sarangi, Vasily Valérïévitch Gurchenkov, Bidisha Sinha, Tobias Reinhold Kießling, Luc Fetler, Felix Rico, Simon Scheuring, Christophe Lamaze, Anthony Simon et al., Proc. Natl. Acad. Sci. U.S.A. 110, 14843 (2013)

    Article  Google Scholar 

  2. R.P. Araujo, D.L.S. McElwain, Bull. Math. Biol. 66, 1039 (2004)

    Article  MathSciNet  Google Scholar 

  3. Thibaut Balois, Martine Ben Amar, Sci. Rep. 4, 3622 (2014)

    Google Scholar 

  4. Thibaut Balois, Clément Chatelain, Martine Ben Amar, J. R. Soc. Interface 11, 20140339 (2014)

    Article  Google Scholar 

  5. Gang Bao, S. Suresh, Nat. Mater. 2, 715 (2003)

    Article  ADS  Google Scholar 

  6. Massimiliano Maria Baraldi, Alexander A. Alemi, James P. Sethna, Sergio Caracciolo, Caterina A.M. La Porta, Stefano Zapperi, J. Stat. Mech. 2013, P02032 (2013)

    Google Scholar 

  7. Markus Basan, Jacques Prost, Jean-François Joanny, Jens Elgeti, Phys. Biol. 8, 026014 (2011)

    Article  ADS  Google Scholar 

  8. Markus Basan, Thomas Risler, Jean-François Joanny, Xavier Sastre-Garau, Jacques Prost, HFSP J. 3, 265 (2009)

    Article  Google Scholar 

  9. Laurence T. Baxter, Rakesh K. Jain, Microvasc. Res. 37, 77 (1989)

    Article  Google Scholar 

  10. M. Ben Amar Avascular tumor growth modelling, in Mathematical Oncology 2013, edited by Alberto d’Onofrio, Alberto Gandolfi (Springer, 2014)

    Article  Google Scholar 

  11. M. Ben Amar, C. Chatelain, P. Ciarletta, Phys. Rev. Lett. 106, 148101 (2011)

    Article  ADS  Google Scholar 

  12. Maximilian Bockhorn, Rakesh K. Jain, Lance L. Munn, Lancet Oncol. 8, 444 (2007)

    Article  Google Scholar 

  13. Yves Boucher, Laurence T. Baxter, Rakesh K. Jain, Cancer Res. 50, 4478 (1990)

    Google Scholar 

  14. Yves Boucher, Rakesh K. Jain, Cancer Res. 52, 5110 (1992)

    Google Scholar 

  15. Helen Byrne, Dirk Drasdo, J. Math. Biol. 58, 657 (2009)

    Article  MATH  MathSciNet  Google Scholar 

  16. Helen M. Byrne, Nat. Rev. Cancer 10, 221 (2010)

    Article  Google Scholar 

  17. Joseph J. Casciari, Stratis V. Sotirchos, Robert M. Sutherland, J. Cell. Physiol. 151, 386 (1992)

    Article  Google Scholar 

  18. Mark A.J. Chaplain, Luigi Graziano, Luigi Preziosi, Math. Med. Biol. 23, 197 (2006)

    Article  MATH  Google Scholar 

  19. Vikash P. Chauhan, Rakesh K. Jain, Nat. Mater. 12, 958 (2013)

    Article  ADS  Google Scholar 

  20. Arnaud Chauvière, Luigi Preziosi, Claude Verdier, Cell mechanics: from single scale-based models to multiscale modeling (CRC Press, 2010)

  21. C.Y. Chen, H.M. Byrne, J.R. King, J. Math. Biol. 43, 191 (2001)

    Article  MATH  MathSciNet  Google Scholar 

  22. Maureen Hong-Sing Chen, George Wai-Cheong Yip, Gary Man-Kit Tse, Takuya Moriya, Philip Chi-Wai Lui, Mar-Lwin Zin, Boon-Huat Bay, Puay-Hoon Tan, Mod. Pathol. 21, 1183 (2008)

    Article  Google Scholar 

  23. Gang Cheng, Janet Tse, Rakesh K. Jain, Lance L. Munn, PLoS One 4, e4632 (2009)

    Article  ADS  Google Scholar 

  24. Magdalena Chrzanowska-Wodnicka, Keith Burridge, J. Cell Biol. 133, 1403 (1996)

    Article  Google Scholar 

  25. P. Ciarletta, L. Foret, M. Ben Amar, J. R. Soc. Interface 8, 345 (2011)

    Article  Google Scholar 

  26. Sarah E. Cross, Yu-Sheng Jin, Jianyu Rao, James K. Gimzewski, Nat. Nanotechnol. 2, 780 (2007)

    Article  ADS  Google Scholar 

  27. Zoe N. Demou, Ann. Biomed. Eng. 38, 3509 (2010)

    Article  Google Scholar 

  28. Gene R. DiResta, Jongbin Lee, John H. Healey, Andrey Levchenko, Steven M. Larson, Ehud Arbit, Ann. Biomed. Eng. 28, 543 (2000)

    Article  Google Scholar 

  29. Dirk Drasdo, Stefan Hoehme, Phys. Biol. 2, 133 (2005)

    Article  Google Scholar 

  30. Dirk Drasdo, Stefan Hoehme, New J. Phys. 14, 055025 (2012)

    Article  ADS  Google Scholar 

  31. Dirk Drasdo, Stefan Hoehme, Michael Block, J. Stat. Phys. 128, 287 (2007)

    Article  MATH  MathSciNet  ADS  Google Scholar 

  32. Adam J. Engler, Maureen A. Griffin, Shamik Sen, Carsten G. Bönnemann, H. Lee Sweeney, Dennis E. Discher, J. Cell Biol. 166, 877 (2004)

    Article  Google Scholar 

  33. Adam J. Engler, Shamik Sen, H. Lee Sweeney, Dennis E. Discher, Cell 126, 677 (2006)

    Article  Google Scholar 

  34. James P. Freyer, Robert M. Sutherland, Cancer Res. 46, 3504 (1986)

    Google Scholar 

  35. Anatol Fritsch, Michael Höckel, Tobias Kiessling, Kenechukwu David Nnetu, Franziska Wetzel, Mareike Zink, Josef A. Käs, Nat. Phys. 6, 730 (2010)

    Article  Google Scholar 

  36. Dai Fukumura, Rakesh K. Jain, J. Cell. Biochem. 101, 937 (2007)

    Article  Google Scholar 

  37. Jörg Galle, Martin Hoffmann, Gabriela Aust, J. Math. Biol. 58, 261 (2009)

    Article  MathSciNet  Google Scholar 

  38. Jörg Galle, Markus Loeffler, Dirk Drasdo, Biophys. J. 88, 62 (2005)

    Article  Google Scholar 

  39. Brian Stephen Garra, Ultrasound Qu. 23, 255 (2007)

    Article  Google Scholar 

  40. Penelope C. Georges, William J. Miller, David F. Meaney, Evelyn S. Sawyer, Paul A. Janmey, Biophys. J. 90, 3012 (2006)

    Article  ADS  Google Scholar 

  41. Randall S. Gieni, Michael J. Hendzel, J. Cell. Biochem. 104, 1964 (2008)

    Article  Google Scholar 

  42. Mark H. Ginsberg, Xiaoping Du, Edward F. Plow, Curr. Opin. Cell Biol. 4, 766 (1992)

    Article  Google Scholar 

  43. Kevin J. Glaser, Joel P. Felmlee, Armando Manduca, Yogesh Kannan Mariappan, Richard L. Ehman, Magn. Reso. Med. 55, 59 (2006)

    Article  Google Scholar 

  44. V.D. Gordon, M.T. Valentine, M.L. Gardel, D. Andor-Ardo, S. Dennison, A.A. Bogdanov, D.A. Weitz, T.S. Deisboeck, Exp. Cell Res. 289, 58 (2003)

    Article  Google Scholar 

  45. Geneviève Griffon-Etienne, Yves Boucher, Christian Brekken, Herman D. Suit, Rakesh K. Jain, Cancer Res. 59, 3776 (1999)

    Google Scholar 

  46. Jochen Guck, Stefan Schinkinger, Bryan Lincoln, Falk Wottawah, Susanne Ebert, Maren Romeyke, Dominik Lenz, Harold M. Erickson, Revathi Ananthakrishnan, Daniel Mitchell et al., Biophys. J. 88, 3689 (2005)

    Article  Google Scholar 

  47. Carl-Henrik Heldin, Kristofer Rubin, Kristian Pietras, Arne Östman, Nat. Rev. Cancer 4, 806 (2004)

    Article  Google Scholar 

  48. Gabriel Helmlinger, Paolo A. Netti, Hera C. Lichtenbeld, Robert J. Melder, Rakesh K. Jain, Nat. Biotechnol. 15, 778 (1997)

    Article  Google Scholar 

  49. J. Holash, P.C. Maisonpierre, D. Compton, P. Boland, C.R. Alexander, D. Zagzag, G.D. Yancopoulos, S.J. Wiegand, Science 284, 1994 (1999)

    Article  Google Scholar 

  50. Sui Huang, Donald E. Ingber, Cancer Cell 8, 175 (2005)

    Article  Google Scholar 

  51. Richard O. Hynes, Cell 69, 11 (1992)

    Article  Google Scholar 

  52. Donald E. Ingber, Joseph A. Madri, James D. Jamieson, Proc. Natl. Acad. Sci. U.S.A. 78, 3901 (1981)

    Article  ADS  Google Scholar 

  53. Rakesh K. Jain, Cancer Res. 48, 2641 (1988)

    Google Scholar 

  54. R.K. Jain, D.G. Duda, Vascular and interstitial biology of tumors, in Clinical Oncology, edited by M. Abeleff, J. Armitage, J. Niederhuber, M. Kastan, G. McKenna (editors), pages 153--172, 2004

  55. M. Tse Janet, Gang Cheng, James A. Tyrrell, Sarah A. Wilcox-Adelman, Yves Boucher, Rakesh K. Jain, Lance L. Munn, Proc. Natl. Acad. Sci. U.S.A. 109, 911 (2012)

    Article  ADS  Google Scholar 

  56. Paul A. Janmey, Ursula Euteneuer, Peter Traub, Manfred Schliwa, J. Cell Biol. 113, 155 (1991)

    Article  Google Scholar 

  57. Yi Jiang, Guo-Yang Li, Lin-Xue Qian, Xiang-Dong Hu, Dong Liu, Si Liang, Yanping Cao, Med. Image Anal. 20, 97 (2015)

    Article  Google Scholar 

  58. Sinem Karaman, Michael Detmar, J. Clin. Invest. 124, 922 (2014)

    Article  Google Scholar 

  59. C. Koike, T.D. McKee, A. Pluen, S. Ramanujan, K. Burton, L.L. Munn, Y. Boucher, R.K. Jain, Br. J. Cancer 86, 947 (2002)

    Article  Google Scholar 

  60. Mehmet H. Kural, Kristen L. Billiar, Biomaterials 35, 1128 (2014)

    Article  Google Scholar 

  61. Caterina A.M. La Porta, Anna Ghilardi, Maria Pasini, Lasse Laurson, Mikko J. Alava, Stefano Zapperi, Martine Ben Amar, Eur. Phys. J. Plus 130, 1 (2015)

    Article  Google Scholar 

  62. Mi Kyeong Lee, Vera M. Nikodem, Neuroreport 15, 99 (2004)

    Article  Google Scholar 

  63. M. Lekka, P. Laidler, D. Gil, J. Lekki, Z. Stachura, A.Z. Hrynkiewicz, Eur. Biophys. J. 28, 312 (1999)

    Article  Google Scholar 

  64. Kandice R. Levental, Hongmei Yu, Laura Kass, Johnathon N. Lakins, Mikala Egeblad, Janine T. Erler, Sheri F.T. Fong, Katalin Csiszar, Amato Giaccia, Wolfgang Weninger et al., Cell 139, 891 (2009)

    Article  Google Scholar 

  65. Rowena McBeath, Dana M. Pirone, Celeste M. Nelson, Kiran Bhadriraju, Christopher S. Chen, Dev. Cell 6, 483 (2004)

    Article  Google Scholar 

  66. Donald M. McDonald, Peter L. Choyke, Nat. Med. 9, 713 (2003)

    Article  Google Scholar 

  67. Fabien Montel, Morgan Delarue, Jens Elgeti, Laurent Malaquin, Markus Basan, Thomas Risler, Bernard Cabane, Danijela Vignjevic, Jacques Prost, Giovanni Cappello et al., Phys. Rev. Lett. 107, 188102 (2011)

    Article  ADS  Google Scholar 

  68. Fabien Montel, Morgan Delarue, Jens Elgeti, Danijela Vignjevic, Giovanni Cappello, Jacques Prost, J. Phys. 14, 055008 (2012)

    Google Scholar 

  69. Paolo A. Netti, Laurence T. Baxter, Yves Boucher, Richard Skalak, Rakesh K. Jain, Cancer Res. 55, 5451 (1995)

    Google Scholar 

  70. Paolo A. Netti, David A. Berk, Melody A. Swartz, Alan J. Grodzinsky, Rakesh K. Jain, Cancer Res. 60, 2497 (2000)

    Google Scholar 

  71. M.-B. Nielsen, Soren T. Christensen, Else K. Hoffmann, Am. J. Physiol.-Cell Physiol. 294, C1046 (2008)

    Article  Google Scholar 

  72. Timothy P. Padera, Brian R. Stoll, Jessica B. Tooredman, Diane Capen, Emmanuelle di Tomaso, Rakesh K. Jain, Nature 427, 695 (2004)

    Article  ADS  Google Scholar 

  73. Matthew J. Paszek, Valerie M. Weaver, J. Mammary Gland Biol. neoplasia 9, 325 (2004)

    Article  Google Scholar 

  74. Matthew J. Paszek, Nastaran Zahir, Kandice R. Johnson, Johnathon N. Lakins, Gabriela I. Rozenberg, Amit Gefen, Cynthia A. Reinhart-King, Susan S. Margulies, Micah Dembo, David Boettiger et al., Cancer Cell 8, 241 (2005)

    Article  Google Scholar 

  75. Nils Podewitz, M. Delarue, J. Elgeti, EPL 109, 58005 (2015)

    Article  ADS  Google Scholar 

  76. Paolo P. Provenzano, Kevin W. Eliceiri, Jay M. Campbell, David R. Inman, John G. White, Patricia J. Keely, BMC Med. 4, 38 (2006)

    Article  Google Scholar 

  77. Paolo P. Provenzano, David R. Inman, Kevin W. Eliceiri, Justin G. Knittel, Long Yan, Curtis T. Rueden, John G. White, Patricia J. Keely, BMC Med. 6, 11 (2008)

    Article  Google Scholar 

  78. Jonas Ranft, Markus Basan, Jens Elgeti, Jean-François Joanny, Jacques Prost, Frank Jülicher, Proc. Natl. Acad. Sci. U.S.A. 107, 20863 (2010)

    Article  Google Scholar 

  79. Torsten W. Remmerbach, Falk Wottawah, Julia Dietrich, Bryan Lincoln, Christian Wittekind, Jochen Guck, Cancer Res. 69, 1728 (2009)

    Article  Google Scholar 

  80. Heiko Rieger, Michael Welter, Wiley Interdiscip. Rev.: Syst. Biol. Med. 7, 113 (2015)

    Google Scholar 

  81. Einar K. Rofstad, Siv H. Tunheim, Berit Mathiesen, Bjørn A. Graff, Ellen F. Halsør, Kristin Nilsen, Kanthi Galappathi, Cancer Res. 62, 661 (2002)

    Google Scholar 

  82. Tiina Roose, Paolo A. Netti, Lance L. Munn, Yves Boucher, Rakesh K. Jain, Microvasc. Res. 66, 204 (2003)

    Article  Google Scholar 

  83. Alexei V. Salnikov, Vegard V. Iversen, Markus Koisti, Christian Sundberg, Lars Johansson, Linda B. Stuhr, Mats Sjöquist, Håkan Ahlström, Rolf K. Reed, Kristofer Rubin, FASEB J. 17, 1756 (2003)

    Google Scholar 

  84. Abbas Samani, Jonathan Bishop, Chris Luginbuhl, Donald B. Plewes, Phys. Med. Biol. 48, 2183 (2003)

    Article  Google Scholar 

  85. Joseph W. Sanger, Proc. Nat. Acad. Sci. 72, 1913 (1975)

    Article  ADS  Google Scholar 

  86. Gernot Schaller, Michael Meyer-Hermann, Phys. Rev. E 71, 051910 (2005)

    Article  MathSciNet  ADS  Google Scholar 

  87. Marco Scianna, C.G. Bell, Luigi Preziosi, J. Theor. Biol. 333, 174 (2013)

    Article  Google Scholar 

  88. Richard Skalak, Stephen Zargaryan, Rakesh K. Jain, Paolo A. Netti, Anne Hoger, J. Math. Biol. 34, 889 (1996)

    Article  MATH  Google Scholar 

  89. Triantafyllos Stylianopoulos, John D. Martin, Vikash P. Chauhan, Saloni R. Jain, Benjamin Diop-Frimpong, Nabeel Bardeesy, Barbara L. Smith, Cristina R. Ferrone, Francis J. Hornicek, Yves Boucher et al., Proc. Natl. Acad. Sci. U.S.A. 109, 15101 (2012)

    Article  ADS  Google Scholar 

  90. Triantafyllos Stylianopoulos, John D. Martin, Matija Snuderl, Fotios Mpekris, Saloni R. Jain, Rakesh K. Jain, Cancer Res. 73, 3833 (2013)

    Article  Google Scholar 

  91. Subra Suresh, Acta Mater. 55, 3989 (2007)

    Article  Google Scholar 

  92. Alessandro Taloni, Alexander A. Alemi, Emilio Ciusani, James P. Sethna, Stefano Zapperi, Caterina A.M. La Porta, PloS one 9, e94229 (2014)

    Article  ADS  Google Scholar 

  93. P. Tracqui, Rep. Progr. Phys. 72, 056701 (2009)

    Article  ADS  Google Scholar 

  94. Scott Valastyan, Robert A. Weinberg, Cell 147, 275 (2011)

    Article  Google Scholar 

  95. Emmanuel Vial, Erik Sahai, Christopher J. Marshall, Cancer Cell 4, 67 (2003)

    Article  Google Scholar 

  96. K.Y. Volokh, Acta Biomater. 2, 493 (2006)

    Article  Google Scholar 

  97. Rebecca G. Wells, J. Clin. Gastroenterol. 39, S158 (2005)

    Article  Google Scholar 

  98. M. Welter, H. Rieger, Eur. Phys. J. E 33, 149 (2010)

    Article  Google Scholar 

  99. Michael Welter, Heiko Rieger, PloS one 8, e70395 (2013)

    Article  Google Scholar 

  100. Joanne Whitehead, Danijela Vignjevic, Claus Fütterer, Emmanuel Beaurepaire, Sylvie Robine, Emmanuel Farge, HFSP J. 2, 286 (2008)

    Article  Google Scholar 

  101. Min Wu, Hermann B. Frieboes, Steven R. McDougall, Mark A.J. Chaplain, Vittorio Cristini, John Lowengrub, J. Theor. Biol. 320, 131 (2013)

    Article  Google Scholar 

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Authors and Affiliations

  1. Center for Complexity & Biosystems, University of Milan, Milan, Italy

    Alessandro Taloni, Stefano Zapperi & Caterina A.M. La Porta

  2. Department of Physics, University of Milan, Milan, Italy

    Alessandro Taloni & Stefano Zapperi

  3. Institute for Scientific Interchange Foundation, Turin, Italy

    Alessandro Taloni & Stefano Zapperi

  4. Laboratoire de Physique Statistique, Ecole Normale Supérieure, UPMC Univ. Paris 06, Paris, France

    Martine Ben Amar

  5. Institut Universitaire de Cancérologie, Faculté de médecine, Université Pierre et Marie-Curie Paris 6, Paris, France

    Martine Ben Amar

  6. CNR - IENI, Milan, Italy

    Stefano Zapperi

  7. Department of Applied Physics, Aalto University, Espoo, Finland

    Stefano Zapperi

  8. Department of Bioscience, University of Milan, Milan, Italy

    Caterina A.M. La Porta

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  1. Alessandro Taloni
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  2. Martine Ben Amar
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  3. Stefano Zapperi
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  4. Caterina A.M. La Porta
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Correspondence to Caterina A.M. La Porta.

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Contribution to the Focus Point on “The Physics of Cancer” edited by M. Ben Amar.

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Taloni, A., Ben Amar, M., Zapperi, S. et al. The role of pressure in cancer growth. Eur. Phys. J. Plus 130, 224 (2015). https://doi.org/10.1140/epjp/i2015-15224-0

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