Biomechanical and biochemical remodeling of stromal extracellular matrix in cancer

Trends in Biotechnology

Volumn 33, Issue 4, 2015, Pages 230-236

  Malik, Ruchi ^a,b   Lelkes, Peter I ^a   Cukierman, Edna ^b  

^a Temple University   (United States)

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

Biomechanical and biochemical cues; Cell ECM dynamic reciprocity; Desmoplasia; Extracellular matrix; Integrins; Rho ROCK

Indexed keywords

BIOMECHANICS; CELLS; CYTOLOGY; DISEASES; DYNAMICS;

ARCHITECTURAL CHANGES; BIOCHEMICAL MECHANISMS; BIOMECHANICAL AND BIOCHEMICAL CUES; DESMOPLASIA; EXTRACELLULAR MATRICES; GENETIC ALTERATIONS; HOMEOSTATIC DYNAMICS; INTEGRINS;

CELL SIGNALING;

GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MACROPHAGE ELASTASE; MATRILYSIN; MATRIX METALLOPROTEINASE 14; PROTEIN LYSINE 6 OXIDASE; STROMELYSIN;

ANGIOGENESIS; BIOCHEMISTRY; BIOMECHANICS; CANCER GROWTH; CARCINOGENESIS; CELL INVASION; EXTRACELLULAR MATRIX; GENETIC ENGINEERING; HUMAN; MESENCHYMAL STROMA CELL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; CHEMISTRY; MEDICAL RESEARCH; METABOLISM; MOUSE; NEOPLASM; PATHOPHYSIOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; BIOMEDICAL RESEARCH; CELL LINE, TUMOR; EXTRACELLULAR MATRIX; HUMANS; MICE; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84939572294     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2015.01.004     Document Type: Review

References (80)

1. Geiger B., Yamada K.M. Molecular architecture and function of matrix adhesions. Cold Spring Harb. Perspect. Biol. 2011, 3:a005033.
2. Provenzano P.P., et al. Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys. J. 2008, 95:5374-5384.
3. Goetz J.G., et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011, 146:148-163.
4. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 2003, 3:422-433.
5. Badylak S.F., et al. Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater. 2009, 5:1-13.
6. Royer C., Lu X. Epithelial cell polarity: a major gatekeeper against cancer&quest. Cell Death Differ. 2011, 18:1470-1477.
7. PaszeK M.J., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
8. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119:1420-1428.
9. Beacham D.A., Cukierman E. Stromagenesis: the changing face of fibroblastic microenvironments during tumor progression. Semin. Cancer Biol. 2005, 15:329-341.
10. Sherman M.H., et al. Vitamin D receptor-mediated stromal reprogramming suppresses pancreatitis and enhances pancreatic cancer therapy. Cell 2014, 159:80-93.
11. Özdemir B.C., et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 2014, 25:719-734.
12. Rhim A.D., et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 2014, 25:735-747.
13. Provenzano P.P., et al. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 2006, 4:38.
14. Conklin M.W., et al. Aligned collagen is a prognostic signature for survival in human breast carcinoma. Am. J. Pathol. 2011, 178:1221-1232.
15. Rybinski B., et al. The wound healing, chronic fibrosis, and cancer progression triad. Physiol. Genomics 2014, 46:223-244.
16. Condeelis J., Segall J.E. Intravital imaging of cell movement in tumours. Nat. Rev. Cancer 2003, 3:921-930.
17. Amatangelo M.D., et al. Stroma-derived three-dimensional matrices are necessary and sufficient to promote desmoplastic differentiation of normal fibroblasts. Am. J. Pathol. 2005, 167:475-488.
18. Lee H-O., et al. FAP-overexpressing fibroblasts produce an extracellular matrix that enhances invasive velocity and directionality of pancreatic cancer cells. BMC Cancer 2011, 11:245.
19. Castelló-Cros R., et al. Staged stromal extracellular 3D matrices differentially regulate breast cancer cell responses through PI3K and beta1-integrins. BMC Cancer 2009, 9:94.
20. Cukierman E., Bassi D.E. Physico-mechanical aspects of extracellular matrix influences on tumorigenic behaviors. Semin. Cancer Biol. 2010, 20:139-145.
21. Cirri P., Chiarugi P. Cancer associated fibroblasts: the dark side of the coin. Am. J. Cancer Res. 2011, 1:482.
22. Kultti A., et al. Accumulation of extracellular hyaluronan by hyaluronan synthase 3 promotes tumor growth and modulates the pancreatic cancer microenvironment. BioMed Res. Int. 2014, 2014.
23. Silver D.J., et al. Chondroitin sulfate proteoglycans potently inhibit invasion and serve as a central organizer of the brain tumor microenvironment. J. Neurosci. 2013, 33:15603-15617.
24. Rutnam Z.J., et al. miRNAs regulate expression and function of extracellular matrix molecules. Matrix Biol. 2013, 32:74-85.
25. Piccinini A.M., Midwood K.S. Illustrating the interplay between the extracellular matrix and microRNAs. Int. J. Exp. Pathol. 2014, 95:158-180.
26. Stamenkovic I. Extracellular matrix remodelling: the role of matrix metalloproteinases. J. Pathol. 2003, 200:448-464.
27. Birkedal-Hansen H., et al. Matrix metalloproteinases: a review. Crit. Rev. Oral Biol. Med. 1993, 4:197-250.
28. McCawley L.J., Matrisian L.M. Matrix metalloproteinases: they're not just for matrix anymore!. Curr. Opin. Cell Biol. 2001, 13:534-540.
29. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2:161-174.
30. Gross J., Lapiere C.M. Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc. Natl. Acad. Sci. U.S.A. 1962, 48:1014.
31. Pilcher B.K., et al. The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. J. Cell Biol. 1997, 137:1445-1457.
32. Botta G.P., et al. Constitutive K-RasG12D activation of ERK2 specifically regulates 3D invasion of human pancreatic cancer cells via MMP-1. Mol. Cancer Res. 2012, 10:183-196.
33. Zeng Z-S., et al. Loss of basement membrane type IV collagen is associated with increased expression of metalloproteinases 2 and 9 (MMP-2 and MMP-9) during human colorectal tumorigenesis. Carcinogenesis 1999, 20:749-755.
34. Margulis A., et al. MMP dependence of fibroblast contraction and collagen production induced by human mast cell activation in a three-dimensional collagen lattice. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 296:L236-L247.
35. Daniels J.T., et al. Matrix metalloproteinase inhibition modulates fibroblast-mediated matrix contraction and collagen production in vitro. Invest. Ophthalmol. Visual Sci. 2003, 44:1104-1110.
36. Holmbeck K., et al. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999, 99:81-92.
37. Friedl P., Wolf K. Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res. 2008, 68:7247-7249.
38. Lucero H., Kagan H. Lysyl oxidase: an oxidative enzyme and effector of cell function. Cell. Mol. Life Sci. CMLS 2006, 63:2304-2316.
39. Peyrol S., et al. Lysyl oxidase gene expression in the stromal reaction to in situ and invasive ductal breast carcinoma. Am. J. Pathol. 1997, 150:497.
40. Levental K.R., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
41. Mäki J.M., et al. Inactivation of the lysyl oxidase gene Lox leads to aortic aneurysms, cardiovascular dysfunction, and perinatal death in mice. Circulation 2002, 106:2503-2509.
42. Cohen S.J., et al. Fibroblast activation protein and its relationship to clinical outcome in pancreatic adenocarcinoma. Pancreas 2008, 37:154-158.
43. Maekawa M., et al. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 1999, 285:895-898.
44. Provenzano P.P., Keely P.J. Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J. Cell Sci. 2011, 124:1195-1205.
45. Raftopoulou M., Hall A. Cell migration: Rho GTPases lead the way. Dev. Biol. 2004, 265:23-32.
46. Gaggioli C., et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 2007, 9:1392-1400.
47. Wolf K., et al. Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J. Cell Biol. 2013, 201:1069-1084.
48. Drab M., et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001, 293:2449-2452.
49. Joshi B., et al. Phosphorylated caveolin-1 regulates Rho/ROCK-dependent focal adhesion dynamics and tumor cell migration and invasion. Cancer Res. 2008, 68:8210-8220.
50. Xian X., et al. Syndecans as receptors and organizers of the extracellular matrix. Cell tissue Res. 2010, 339:31-46.
51. Carey D. Syndecans: multifunctional cell-surface co-receptors. Biochem. J. 1997, 327:1-16.
52. Yang N., et al. Syndecan-1 in breast cancer stroma fibroblasts regulates extracellular matrix fiber organization and carcinoma cell motility. Am. J. Pathol. 2011, 178:325-335.
53. Low B.C., et al. YAP/TAZ as mechanosensors and mechanotransducers in regulating organ size and tumor growth. FEBS Lett. 2014, 588:2663-2670.
54. Dupont S., et al. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474:179-183.
55. Kim K.M., et al. Shear stress induced by an interstitial level of slow flow increases the osteogenic differentiation of mesenchymal stem cells through TAZ activation. PLoS ONE 2014, 9:e92427.
56. Aragona M., et al. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 2013, 154:1047-1059.
57. Graziano L., Preziosi L. Mechanics in tumor growth. Modeling of Biological Materials 2007, 263-321. Springer. F. Mollica (Ed.).
58. Ng C.P., Swartz M.A. Mechanisms of interstitial flow-induced remodeling of fibroblast-collagen cultures. Ann. Biomed. Eng. 2006, 34:446-454.
59. Thomopoulos S., et al. The development of structural and mechanical anisotropy in fibroblast populated collagen gels. J. Biomech. Eng. 2005, 127:742-750.
60. + T regulatory cells: role of tumor-derived TGF-beta. J. Immunol. 2007, 178:2883-2892.
61. Desmouliere A., et al. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J. Cell Biol. 1993, 122:103-111.
62. Hinz B., et al. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol. Biol. Cell 2001, 12:2730-2741.
63. Wang J., et al. Mechanical force regulation of myofibroblast differentiation in cardiac fibroblasts. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H1871-H1881.
64. Seliktar D., et al. The role of matrix metalloproteinase-2 in the remodeling of cell-seeded vascular constructs subjected to cyclic strain. Ann. Biomed. Eng. 2001, 29:923-934.
65. Breen E.C. Mechanical strain increases type I collagen expression in pulmonary fibroblasts in vitro. J. Appl. Physiol. 2000, 88:203-209.
66. Kanematsu A., et al. Type I collagen can function as a reservoir of basic fibroblast growth factor. J. Control. Release 2004, 99:281-292.
67. Hinz B. Tissue stiffness, latent TGF-β1 activation, and mechanical signal transduction: implications for the pathogenesis and treatment of fibrosis. Curr. Rheumatol. Rep. 2009, 11:120-126.
68. Smith M.L., et al. Force-induced unfolding of fibronectin in the extracellular matrix of living cells. PLoS Biol. 2007, 5:e268.
69. Ingham K.C., et al. Localization of a cryptic binding site for tenascin on fibronectin. J. Biol. Chem. 2004, 279:28132-28135.
70. Engler A.J., et al. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
71. Xu R., et al. Tissue architecture and function: dynamic reciprocity via extra-and intra-cellular matrices. Cancer Metastasis Rev. 2009, 28:167-176.
72. Nelson C.M., Bissell M.J. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 2006, 22:287.
73. Maller O., et al. Extracellular matrix composition reveals complex and dynamic stromal-epithelial interactions in the mammary gland. J. Mammary Gland Biol. Neoplasia 2010, 15:301-318.
74. Mitra S.K., Schlaepfer D.D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 2006, 18:516-523.
75. Huveneers S., Danen E.H. Adhesion signaling - crosstalk between integrins, Src and Rho. J. Cell Sci. 2009, 122:1059-1069.
76. Grande-García A., et al. Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J. Cell Biol. 2007, 177:683-694.
77. Chung K-M., et al. Fibroblast activation protein (FAP) Is essential for the migration of bone marrow mesenchymal stem cells through RhoA activation. PLoS ONE 2014, 9:e88772.
78. Halder G., et al. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 2012, 13:591-600.
79. Riveline D., et al. Focal contacts as mechanosensors externally applied local mechanical force induces growth of focal contacts by an mdia1-dependent and rock-independent mechanism. J. Cell Biol. 2001, 153:1175-1186.
80. Bijlsma M.F., van Laarhoven H.W. The conflicting roles of tumor stroma in pancreatic cancer and their contribution to the failure of clinical trials: a systematic review and critical appraisal. Cancer Metastasis Rev. 2015, Published online January 8, 2015. http://dx.doi.org/10.1007/s10555-014-9541-1.