A new paradigm for mechanobiological mechanisms in tumor metastasis

Seminars in Cancer Biology

Volumn 22, Issue 5-6, 2012, Pages 385-395

  Torzilli, Peter A ^a,b   Bourne, Jonathan W ^a,b   Cigler, Tessa ^c   Vincent, C Theresa ^a,d  

^a HOSPITAL FOR SPECIAL SURGERY   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Biomechanical forces; Collagen; Invasion; Metastasis; Stroma; Tumor

Indexed keywords

COLLAGEN FIBRIL; FIBRONECTIN; GELATINASE A; INTEGRIN; PROTEOGLYCAN;

BIOMECHANICS; BREAST CANCER; CANCER GROWTH; CANCER INVASION; CELL INVASION; CELL MIGRATION; CONFORMATIONAL TRANSITION; ENZYMATIC DEGRADATION; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; MECHANICAL STRESS; MECHANICAL TORSION; METASTASIS; MOLECULAR DYNAMICS; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; YOUNG MODULUS;

BIOMECHANICS; BREAST NEOPLASMS; CELL MOVEMENT; COLLAGEN; EPITHELIAL-MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FEMALE; HUMANS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS;

EID: 84866313241     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2012.05.002     Document Type: Review

References (59)

1. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Thun M.J. Cancer statistics, 2009. CA A Cancer Journal for Clinicians 2009, 59(4):225-249.
2. Liedtke C., Mazouni C., Hess K.R., Andre F., Tordai A., Mejia J.A., et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. Journal of Clinical Oncology 2008, 26(8):1275-1281.
3. Lee J.M., Dedhar S., Kalluri R., Thompson E.W. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. Journal of Cell Biology 2006, 172(7):973-981.
4. Provenzano P.P., Eliceiri K.W., Campbell J.M., Inman D.R., White J.G., Keely P.J. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Medicine 2006, 4(1):38-54.
5. Hinz B. The myofibroblast: paradigm for a mechanically active cell. Journal of Biomechanics 2011, 43(1):146-155.
6. Provenzano P.P., Alejandro-Osorio A.L., Valhmu W.B., Jensen K.T., Vanderby R. Intrinsic fibroblast-mediated remodeling of damaged collagenous matrices in vivo. Matrix Biology 2005, 23(8):543-555.
7. Wolf K., Wu Y.I., Liu Y., Geiger J., Tam E., Overall C., et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nature Cell Biology 2007, 9(8):893-904.
8. Rouyer N., Wolf C., Chenard M.P., Rio M.C., Chambon P., Bellocq J.P., et al. Stromelysin-3 gene expression in human cancer: an overview. Invasion and Metastasis 1994, 14(1-6):269-275.
9. Motrescu E.R., Blaise S., Etique N., Messaddeq N., Chenard M.P., Stoll I., et al. Matrix metalloproteinase-11/stromelysin-3 exhibits collagenolytic function against collagen VI under normal and malignant conditions. Oncogene 2008, 27(49):6347-6355.
10. Frantz C., Stewart K.M., Weaver V.M. The extracellular matrix at a glance. Journal of Cell Science 2011, 123(Pt 24):4195-4200.
11. Vincent T., Neve E.P., Johnson J.R., Kukalev A., Rojo F., Albanell J., et al. A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nature Cell Biology 2009, 11(8):943-950.
12. Tan J.L., Tien J., Pirone D.M., Gray D.S., Bhadriraju K., Chen C.S. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(4):1484-1489.
13. Kumar S., Weaver V.M. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer and Metastasis Reviews 2009, 28(1-2):113-127.
14. Hoffman B.D., Grashoff C., Schwartz M.A. Dynamic molecular processes mediate cellular mechanotransduction. Nature 2011, 475(7356):316-323.
15. Mierke C.T., Frey B., Fellner M., Herrmann M., Fabry B. Integrin alpha5beta1 facilitates cancer cell invasion through enhanced contractile forces. Journal of Cell Science 2011, 124(Pt 3):369-383.
16. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8(3):241-254.
17. Levental I., Georges P.C., Janmey P.A. Soft biological materials and their impact on cell function. Soft Matter 2006, 2:1-9.
18. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139(5):891-906.
19. Gjorevski N., Boghaert E., Nelson C.M. Regulation of epithelial-mesenchymal transition by transmission of mechanical stress through epithelial tissues. Cancer Microenvironment 2011, 10.1007/s12307-011-0076-5.
20. Provenzano P.P., Inman D.R., Eliceiri K.W., Knittel J.G., Yan L., Rueden C.T., et al. Collagen density promotes mammary tumor initiation and progression. BMC Medicine 2008, 6. 10.1186/741-7015-6-11-1-15.
21. Shieh A.C. Biomechanical forces shape the tumor microenvironment. Annals of Biomedical Engineering 2011, 39(5):1379-1389.
22. Solon J., Levental I., Sengupta K., Georges P.C., Janmey P.A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophysical Journal 2007, 93(12):4453-4461.
23. Wipff P.J., Hinz B. Myofibroblasts work best under stress. Journal of Bodywork and Movements Therapies 2009, 13(2):121-127.
24. Chandler E.M., Berglund C.M., Lee J.S., Polacheck W.J., Gleghorn J.P., Kirby B.J., et al. Stiffness of photocrosslinked RGD-alginate gels regulates adipose progenitor cell behavior. Biotechnology and Bioengineering 2011, 108(7):1683-1692.
25. Keely P.J. Mechanisms by which the extracellular matrix and integrin signaling act to regulate the switch between tumor suppression and tumor promotion. Journal of Mammary Gland Biology and Neoplasia 2011, 16(3):205-219.
26. Provenzano P.P., Keely P.J. Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. Journal of Cell Science 2011, 124(Pt 8):1195-1205.
27. Holton S.E., Walsh M.J., Bhargava R. Subcellular localization of early biochemical transformations in cancer-activated fibroblasts using infrared spectroscopic imaging. Analyst 2011, 136(14):2953-2958.
28. Gullberg D., Reed R.K. Tumor-stroma interactions focus on fibroblasts. Mouse as a model organism 2011, 117-130. Springer, Netherlands. C. Brakebusch, T. Pihlajaniemi (Eds.).
29. Brown T.D. Techniques for mechanical stimulation of cells in vitro: a review. Journal of Biomechanics 2000, 33(1):3-14.
30. Humphrey J.D. Stress, strain, and mechanotransduction in cells. Journal of Biomechanical Engineering 2001, 123(6):638-641.
31. Janmey P.A., Georges P.C., Hvidt S. Basic rheology for biologists. Methods in Cell Biology 2007, 83:3-27.
32. Tang X., Kuhlenschmidt T.B., Zhou J., Bell P., Wang F., Kuhlenschmidt M.S., et al. Mechanical force affects expression of an in vitro metastasis-like phenotype in HCT-8 cells. Biophysical Journal 2010, 99(8):2460-2469.
33. Samani A., Bishop J., Luginbuhl C., Plewes D.B. Measuring the elastic modulus of ex vivo small tissue samples. Physics in Medicine and Biology 2003, 48(14):2183-2198.
34. Nathanson S.D., Nelson L. Interstitial fluid pressure in breast cancer, benign breast conditions, and breast parenchyma. Annals of Surgical Oncology 1994, 1(4):333-338.
35. Nathan S.S., Huvos A.G., Casas-Ganem J.E., Yang R., Linkov I., Sowers R., et al. Tumor interstitial fluid pressure may regulate angiogenic factors in osteosarcoma. Journal of Orthopaedic Research 2008, 26(11):1520-1525.
36. Gonzalez L.O., Gonzalez-Reyes S., Junquera S., Marin L., Gonzalez L., Del Casar J.M., et al. Expression of metalloproteases and their inhibitors by tumor and stromal cells in ductal carcinoma in situ of the breast and their relationship with microinvasive events. Journal of Cancer Research and Clinical Oncology 2010, 136(9):1313-1321.
37. Gonzalez L.O., Junquera S., del Casar J.M., Gonzalez L., Marin L., Gonzalez-Reyes S., et al. Immunohistochemical study of matrix metalloproteinases and their inhibitors in pure and mixed invasive and in situ ductal carcinomas of the breast. Human Pathology 2010, 41(7):980-989.
38. Del Casar J.M., Gonzalez-Reyes S., Gonzalez L.O., Gonzalez J.M., Junquera S., Bongera M., et al. Expression of metalloproteases and their inhibitors in different histological types of breast cancer. Journal of Cancer Research and Clinical Oncology 2010, 136(6):811-819.
39. del Casar J.M., Carreno G., Gonzalez L.O., Junquera S., Gonzalez-Reyes S., Gonzalez J.M., et al. Expression of metalloproteases and their inhibitors in primary tumors and in local recurrences after mastectomy for breast cancer. Journal of Cancer Research and Clinical Oncology 2011, 136(7):1049-1058.
40. Folgueras A.R., Pendas A.M., Sanchez L.M., Lopez-Otin C. Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. International Journal of Developmental Biology 2004, 48(5-6):411-424.
41. Xu X., Wang Y., Chen Z., Sternlicht M.D., Hidalgo M., Steffensen B. Matrix metalloproteinase-2 contributes to cancer cell migration on collagen. Cancer Research 2005, 65(1):130-136.
42. Overall C.M. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Molecular Biotechnology 2002, 22(1):51-86.
43. Tam E.M., Moore T.R., Butler G.S., Overall C.M. Characterization of the distinct collagen binding, helicase and cleavage mechanisms of matrix metalloproteinase 2 and 14 (gelatinase A and MT1-MMP): the differential roles of the MMP hemopexin c domains and the MMP-2 fibronectin type II modules in collagen triple helicase activities. Journal of Biological Chemistry 2004, 279(41):43336-43344.
44. Wyatt K.E., Bourne J.W., Torzilli P.A. Deformation-dependent enzyme mechanokinetic cleavage of type I collagen. Journal of Biomechanical Engineering 2009, 131(5):051004.
45. Huang C., Yannas I.V. Mechanochemical studies of enzymatic degradation of insoluble collagen fibers. Journal of Biomedical Materials Research 1977, 11(1):137-154.
46. Bhole A.P., Flynn B.P., Liles M., Saeidi N., Dimarzio C.A., Ruberti J.W. Mechanical strain enhances survivability of collagen micronetworks in the presence of collagenase: implications for load-bearing matrix growth and stability. Philosophical Transactions. Series A, Mathematical, Physical, and Engineering Sciences 2009, 367(1902):3339-3362.
47. Camp R.J., Liles M., Beale J., Saeidi N., Flynn B.P., Moore E., et al. Molecular mechanochemistry: low force switch slows enzymatic cleavage of human type I collagen monomer. Journal of the American Chemical Society 2011, 133(11):4073-4078.
48. Nabeshima Y., Grood E.S., Sakurai A., Herman J.H. Uniaxial tension inhibits tendon collagen degradation by collagenase in vitro. Journal of Orthopaedic Research 1996, 14(1):123-130.
49. Bourne J.W., Torzilli P.A. Molecular simulations predict novel collagen conformations during cross-link loading. Matrix Biology 2011, 30(5-6):356-360.
50. in't Veld P.J., Stevens M.J. Simulation of the mechanical strength of a single collagen molecule. Biophysical Journal 2008, 95(1):33-39.
51. Gautieri A., Vesentini S., Montevecchi F.M., Redaelli A. Mechanical properties of physiological and pathological models of collagen peptides investigated via steered molecular dynamics simulations. Journal of Biomechanics 2008, 41(14):3073-3077.
52. Gautieri A., Vesentini S., Redaelli A., Buehler M.J. Single molecule effects of osteogenesis imperfecta mutations in tropocollagen protein domains. Protein Science 2009, 18(1):161-168.
53. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., et al. Scalable molecular dynamics with NAMD. Journal of Computational Chemistry 2005, 26(16):1781-1802.
54. Uzel S.G., Buehler M.J. Molecular structure, mechanical behavior and failure mechanism of the C-terminal cross-link domain in type I collagen. Journal of the Mechanical Behavior of Biomedical and Materials 2011, 4(2):153-161.
55. Buehler M. Atomistic and continuum modeling of mechanical properties of collagen: elasticity, fracture and self-assembly. Journal of Materials Research 2006, 21(8):1947-1961.
56. Grandbois M., Beyer M., Rief M., Clausen-Schaumann H., Gaub H.E. How strong is a covalent bond?. Science 1999, 283(5408):1727-1730.
57. Eilaghi A., Flanagan J.G., Tertinegg I., Simmons C.A., Wayne Brodland G., Ross Ethier C. Biaxial mechanical testing of human sclera. Journal of Biomechanics 2010, 43(9):1696-1701.
58. Pai S., Ledoux W.R. The compressive mechanical properties of diabetic and non-diabetic plantar soft tissue. Journal of Biomechanics 2010, 43(9):1754-1760.
59. Sasaki N., Odajima S. Stress-strain curve and Young's modulus of a collagen molecule as determined by the X-ray diffraction technique. Journal of Biomechanics 1996, 29(5):655-658.