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Collagen network and the mechanical microenvironment of cancer cells

Sun Bo

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Collagen network and the mechanical microenvironment of cancer cells

Sun Bo
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  • Mechanical interaction between cancer cells and their microenvironment plays a central role in the progression of tumors. In vitro models based on biopolymer networks have been successfully employed to simulate the 3D extracellular matrix (ECM) of tumors. In this review, we focus on type I collagen gel. We describe the hierarchical structural and mechanical properties of type I collagen ECM. We demonstrate that corresponding to the scales of adhesion sites, single cells and cell colonies, the mechanics of the ECM is dominated by single fibers, fiber clusters and rheology of the whole fiber network. In the end, we discuss the limitations of reconstituted type I collagen as in vitro ECM.
    [1]

    Balkwill F, Capasso M, Hagemann T 2012 J. Cell Science 125 5591

    [2]

    Allinen M et al. 2004 Cancer Cell 6 17

    [3]

    Friedl P, Alexander S 2011 Cell 147 992

    [4]

    Hanahan D, Weinberg R 2000 Cell 100 57

    [5]

    Bierie B, Moses H 2006 Nature Reviews Cancer 6 506

    [6]

    Muhammad S 2014 World Journal of Gastroenterology 20 17011

    [7]

    Soon P, Kiaris, H 2013 Endocrine-Related Cancer 20 257

    [8]

    Zigrino P, Loffek S, Mauch C 2005 Biochimie 87 321

    [9]

    Hua Y, Korty M, Pardoll D 2007 Nature Reviews Immunology 7 41

    [10]

    Ulrich T, Pardo E, Kumar S 2009 Cancer Research 69

    [11]

    Yeung T et al. 2005 Effects of substrate stiffness on cell morphology, cytosckeletal structure and adhesion. Cell Motility and the Cytoskeleton, p60

    [12]

    Lopez J, You I, McDonald D, Weaver V 2011 Integrative Biology 3 910

    [13]

    Dingal P, Discher D 2014 Biophysical Journal 107 2734

    [14]

    Seewaldt V 2014 Nature Medicine 20 332

    [15]

    Bordeleau F, Alcoser T, Reinhart-King C 2014 Americal Journal of Physiology: Cell Physiology 306 C110

    [16]

    Barcellos-Hoff M, Ravani S 2000 Cancer Research 60 1254

    [17]

    Luo T, Mohan K, Robinson D 2013 Nature Materials 12 1064

    [18]

    Silver F, Siperko L 2003 Critical Review of Biomedical Engineering 31 255

    [19]

    Dufort C, Paszek M, Weaver V 2011 Nature Review Molecular Cell Biology 12 308

    [20]

    Desgrosellier J, Cheresh D 2010 Nature Review Cancer 10 9

    [21]

    Varner J, Cheresh D 1996 Current Opinion in Cell Biology 8 724

    [22]

    Juliano R, Varner J 2004 Current Opinion in Cell Biology 5 812

    [23]

    Mierke C et al 2010 The Journal of Biological Chemistry 285 13121

    [24]

    Egeblad M, Werb Z 2002 Nature Reviews Cancer 2 161

    [25]

    Itoh Y, Nagase H 2002 Essays Biochemistry 38 21

    [26]

    Gialeli C, Achilleas D 2011 The FEBS Journal 278 16

    [27]

    Yamazaki D, Kurisu S, Takenawa T 2005 Cancer Science 96 379

    [28]

    Olson M, Sahai E 2009 Clinical Experimental Metastasis 26 273

    [29]

    Parker A, Kavallaris M, McCarroll J 2014 Microtubules and their role in cellular stress in cancer. Frontiers in Oncology, p00153

    [30]

    Shtil A et al. 1999 Oncogene 18 377

    [31]

    Tseng Y, Wirtz D 2001 Biophysical Journal 81 1643

    [32]

    Courson D, Rock R 2010 The Journal of Biological Chemistry 285 26350

    [33]

    Wyckoff J et al. 2006 Current Biology 16 1515

    [34]

    Sabeh F, Shimizu-Hirota R, Weiss S 2009 Journal of Cell Biology 185 11

    [35]

    Friedl P, Wolf K 2003 Nature Reviews Cancer 3 362

    [36]

    Aung A et al. 2014 Biophysical Journal 107 2528

    [37]

    Reichl E et al. 2008 Current Biology 18 471

    [38]

    Robinson D, Spudich J 2004 Current Opinions in Cell Biology 16 182

    [39]

    Cao R et al. 2014 British Journal of Cancer 111 539

    [40]

    Laakso J, Lewis J, Shuman H, Ostap E 2008 Science 321 133

    [41]

    Pruitt B, Dunn A, Weis W, Nelson W 2014 PLoS Biology 12 e1001996

    [42]

    Suresh S 2007 Acta Biomaterial 3 413

    [43]

    Hao J et al. 2013 Cell Biology International 37 888

    [44]

    Liu L et al. 2013 Proceedings of the National Academy of Science 110 1686

    [45]

    Anon 2006 Nature Reviews Molecular Biology 7 211

    [46]

    Brown R 2013 Experimental Cell Research 319 2460

    [47]

    Lodish H et al. 2000 Molecular Cell Biology (4th Ed.) (New York: W. H. Freeman)

    [48]

    Paszek M et al. 2005 Cancer Cell 8 241

    [49]

    Petrie R, Yamada K 2012 Journal of Cell Science 125 5917

    [50]

    Schmitt F, Hall C, Jakus M 2005 Journal of Cellular Physiology 20 11

    [51]

    Shoulders M, Raines R 2009 Annual Review of Biochemcistry 78 929

    [52]

    Yang Y, Motte S, LJ K 2010 Biomaterials 31 5678

    [53]

    Lang N et al. 2013 Biophysical Journal 105 1967

    [54]

    Raspanti M, Alessandrini A, Gobbi P, Ruggeri A 1996 Microscopy Research Techniques 35 87

    [55]

    Raspanti M, Alessandrini A, Ottani V, Ruggeri A 1997 Journal of Structure Biology 119 118

    [56]

    Brightman A et al. 2000 Biopolymers 54 222

    [57]

    Yang Y, Kaufman L 2009 Biophysics Journal 96 1566

    [58]

    Williams R, Zipfel W, Webb W 2005 Biophysics Journal 88 1377

    [59]

    Cox G et al. 2003 Journal of Structural Biology 141 53

    [60]

    Jones C et al. 2014 Soft Matter 10 8855

    [61]

    Reymann A et al. 2012 Science 336 6086

    [62]

    Etienne-Manneville S 2013 Annual Review of Cell and Developmental Biology 29 471

    [63]

    Singh P, Carraher C, Schwarzbauer J 2010 Annual Review of Cell and Developmental Biology 26 397

    [64]

    Shayegan M, Forde N 2013 PLoS One 8 e70590

    [65]

    Stein A, Vader D, Weitz D, Sander L 2011 Complexity 16 22

    [66]

    Curtis J, Koss B, Grier D 2002 Optics Communications 207 169

    [67]

    Broedersz C M M 2014 Rev. Mod. Phys 86

    [68]

    Baldwin S J 2014 Biophysical Journal 107 1794

    [69]

    Gautieri A S 2011 Nano Letters 11 757

    [70]

    Orgel J, Irving T A M, Wess T 2006 Proceedings of National Academy of Sciences America 103 9001

    [71]

    Apel-Sarid L et al. 2010 Journal of Neuronsurgical Pediatrics 6 38

    [72]

    Provenzano P et al. 2006 BMC Medicine 4 38

    [73]

    Li Y, Yu S 2013 Current Opinions in Chemical Biology 17 968

    [74]

    Silva E A, Mooney D J 2004 Current Topics in Development Biology 64 181

    [75]

    Lutolf M, Hubbell J 2005 Nature Biotechnology 23 47

  • [1]

    Balkwill F, Capasso M, Hagemann T 2012 J. Cell Science 125 5591

    [2]

    Allinen M et al. 2004 Cancer Cell 6 17

    [3]

    Friedl P, Alexander S 2011 Cell 147 992

    [4]

    Hanahan D, Weinberg R 2000 Cell 100 57

    [5]

    Bierie B, Moses H 2006 Nature Reviews Cancer 6 506

    [6]

    Muhammad S 2014 World Journal of Gastroenterology 20 17011

    [7]

    Soon P, Kiaris, H 2013 Endocrine-Related Cancer 20 257

    [8]

    Zigrino P, Loffek S, Mauch C 2005 Biochimie 87 321

    [9]

    Hua Y, Korty M, Pardoll D 2007 Nature Reviews Immunology 7 41

    [10]

    Ulrich T, Pardo E, Kumar S 2009 Cancer Research 69

    [11]

    Yeung T et al. 2005 Effects of substrate stiffness on cell morphology, cytosckeletal structure and adhesion. Cell Motility and the Cytoskeleton, p60

    [12]

    Lopez J, You I, McDonald D, Weaver V 2011 Integrative Biology 3 910

    [13]

    Dingal P, Discher D 2014 Biophysical Journal 107 2734

    [14]

    Seewaldt V 2014 Nature Medicine 20 332

    [15]

    Bordeleau F, Alcoser T, Reinhart-King C 2014 Americal Journal of Physiology: Cell Physiology 306 C110

    [16]

    Barcellos-Hoff M, Ravani S 2000 Cancer Research 60 1254

    [17]

    Luo T, Mohan K, Robinson D 2013 Nature Materials 12 1064

    [18]

    Silver F, Siperko L 2003 Critical Review of Biomedical Engineering 31 255

    [19]

    Dufort C, Paszek M, Weaver V 2011 Nature Review Molecular Cell Biology 12 308

    [20]

    Desgrosellier J, Cheresh D 2010 Nature Review Cancer 10 9

    [21]

    Varner J, Cheresh D 1996 Current Opinion in Cell Biology 8 724

    [22]

    Juliano R, Varner J 2004 Current Opinion in Cell Biology 5 812

    [23]

    Mierke C et al 2010 The Journal of Biological Chemistry 285 13121

    [24]

    Egeblad M, Werb Z 2002 Nature Reviews Cancer 2 161

    [25]

    Itoh Y, Nagase H 2002 Essays Biochemistry 38 21

    [26]

    Gialeli C, Achilleas D 2011 The FEBS Journal 278 16

    [27]

    Yamazaki D, Kurisu S, Takenawa T 2005 Cancer Science 96 379

    [28]

    Olson M, Sahai E 2009 Clinical Experimental Metastasis 26 273

    [29]

    Parker A, Kavallaris M, McCarroll J 2014 Microtubules and their role in cellular stress in cancer. Frontiers in Oncology, p00153

    [30]

    Shtil A et al. 1999 Oncogene 18 377

    [31]

    Tseng Y, Wirtz D 2001 Biophysical Journal 81 1643

    [32]

    Courson D, Rock R 2010 The Journal of Biological Chemistry 285 26350

    [33]

    Wyckoff J et al. 2006 Current Biology 16 1515

    [34]

    Sabeh F, Shimizu-Hirota R, Weiss S 2009 Journal of Cell Biology 185 11

    [35]

    Friedl P, Wolf K 2003 Nature Reviews Cancer 3 362

    [36]

    Aung A et al. 2014 Biophysical Journal 107 2528

    [37]

    Reichl E et al. 2008 Current Biology 18 471

    [38]

    Robinson D, Spudich J 2004 Current Opinions in Cell Biology 16 182

    [39]

    Cao R et al. 2014 British Journal of Cancer 111 539

    [40]

    Laakso J, Lewis J, Shuman H, Ostap E 2008 Science 321 133

    [41]

    Pruitt B, Dunn A, Weis W, Nelson W 2014 PLoS Biology 12 e1001996

    [42]

    Suresh S 2007 Acta Biomaterial 3 413

    [43]

    Hao J et al. 2013 Cell Biology International 37 888

    [44]

    Liu L et al. 2013 Proceedings of the National Academy of Science 110 1686

    [45]

    Anon 2006 Nature Reviews Molecular Biology 7 211

    [46]

    Brown R 2013 Experimental Cell Research 319 2460

    [47]

    Lodish H et al. 2000 Molecular Cell Biology (4th Ed.) (New York: W. H. Freeman)

    [48]

    Paszek M et al. 2005 Cancer Cell 8 241

    [49]

    Petrie R, Yamada K 2012 Journal of Cell Science 125 5917

    [50]

    Schmitt F, Hall C, Jakus M 2005 Journal of Cellular Physiology 20 11

    [51]

    Shoulders M, Raines R 2009 Annual Review of Biochemcistry 78 929

    [52]

    Yang Y, Motte S, LJ K 2010 Biomaterials 31 5678

    [53]

    Lang N et al. 2013 Biophysical Journal 105 1967

    [54]

    Raspanti M, Alessandrini A, Gobbi P, Ruggeri A 1996 Microscopy Research Techniques 35 87

    [55]

    Raspanti M, Alessandrini A, Ottani V, Ruggeri A 1997 Journal of Structure Biology 119 118

    [56]

    Brightman A et al. 2000 Biopolymers 54 222

    [57]

    Yang Y, Kaufman L 2009 Biophysics Journal 96 1566

    [58]

    Williams R, Zipfel W, Webb W 2005 Biophysics Journal 88 1377

    [59]

    Cox G et al. 2003 Journal of Structural Biology 141 53

    [60]

    Jones C et al. 2014 Soft Matter 10 8855

    [61]

    Reymann A et al. 2012 Science 336 6086

    [62]

    Etienne-Manneville S 2013 Annual Review of Cell and Developmental Biology 29 471

    [63]

    Singh P, Carraher C, Schwarzbauer J 2010 Annual Review of Cell and Developmental Biology 26 397

    [64]

    Shayegan M, Forde N 2013 PLoS One 8 e70590

    [65]

    Stein A, Vader D, Weitz D, Sander L 2011 Complexity 16 22

    [66]

    Curtis J, Koss B, Grier D 2002 Optics Communications 207 169

    [67]

    Broedersz C M M 2014 Rev. Mod. Phys 86

    [68]

    Baldwin S J 2014 Biophysical Journal 107 1794

    [69]

    Gautieri A S 2011 Nano Letters 11 757

    [70]

    Orgel J, Irving T A M, Wess T 2006 Proceedings of National Academy of Sciences America 103 9001

    [71]

    Apel-Sarid L et al. 2010 Journal of Neuronsurgical Pediatrics 6 38

    [72]

    Provenzano P et al. 2006 BMC Medicine 4 38

    [73]

    Li Y, Yu S 2013 Current Opinions in Chemical Biology 17 968

    [74]

    Silva E A, Mooney D J 2004 Current Topics in Development Biology 64 181

    [75]

    Lutolf M, Hubbell J 2005 Nature Biotechnology 23 47

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Publishing process
  • Received Date:  16 January 2015
  • Accepted Date:  14 February 2015
  • Published Online:  05 March 2015

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