Tumor cell invasion is promoted by interstitial flow-induced matrix priming by stromal fibroblasts

Cancer Research

Volumn 71, Issue 3, 2011, Pages 790-800

  Shieh, Adrian C ^a   Rozansky, Hallie A ^a   Hinz, Boris ^b   Swartz, Melody A ^a  

^a EPFL   (Switzerland)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN FIBER; COLLAGENASE; SECONDARY LYMPHOID TISSUE CHEMOKINE; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CANCER INVASION; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; CHEMOTAXIS; COCULTURE; COLLAGEN DEGRADATION; CONTROLLED STUDY; CROSS PRESENTATION; FLUID FLOW; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERSTITIAL FLUID; PRIORITY JOURNAL; SKIN FIBROBLAST; TUMOR CELL;

CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL MOVEMENT; COCULTURE TECHNIQUES; EXTRACELLULAR FLUID; EXTRACELLULAR MATRIX; FIBROBLASTS; HUMANS; MATRIX METALLOPROTEINASE 1; NEOPLASM INVASIVENESS; NEOPLASMS; RHO-ASSOCIATED KINASES; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA1; TUMOR MICROENVIRONMENT;

EID: 79551565642     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-1513     Document Type: Article

References (50)

1. Tlsty TD, Coussens LM. Tumor stroma and regulation of cancer development. Annu Rev Pathol 2006;1:119-50.
2. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009;9:239-52.
3. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006;6:392-401.
4. Kumar S, Weaver VM. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev 2009;28:113-27.
5. Fukumura D, Jain RK. Tumor microenvironment abnormalities: causes, consequences, and strategies to normalize. J Cell Biochem 2007;101:937-49. (Pubitemid 47040874)
6. Provenzano PP, Inman DR, Eliceiri KW Knittel JG, Yan L, Rueden CT, et al. Collagen density promotes mammary tumor initiation and progression. BMC Med 2008;6:11.
7. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002;3:349-63. (Pubitemid 34619269)
8. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009;139:891-906.
9. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005;8:241-54.
10. Provenzano PP, Inman DR, Eliceiri KW, Keely PJ. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 2009;28:4326-43.
11. Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med 2006;4:38.
12. Grinnell F. Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol 2003;13:264-9.
13. Dafni H, Israely T, Bhujwalla ZM, Benjamin LE, Neeman M. Over-expression of vascular endothelial growth factor 165 drives peritumor interstitial convection and induces lymphatic drain: magnetic resonance imaging, confocal microscopy, and histological tracking of triple-labeled albumin. Cancer Res 2002;62:6731-9. (Pubitemid 35364145)
14. Harrell MI, Iritani BM, Ruddell A. Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am J Pathol 2007;170:774-86.
15. Fleury ME, Boardman KC, Swartz MA. Autologous morphogen gradients by subtle interstitial flow and matrix interactions. Biophys J 2006;91:113-21.
16. Helm CL, Fleury ME, Zisch AH, Boschetti F, Swartz MA. Synergy between interstitial flow and VEGF directs capillary morphogenesis in vitro through a gradient amplification mechanism. Proc Natl Acad Sci U S A 2005;102:15779-84.
17. Shields JD, Fleury ME, Yong C, Tomei AA, Randolph GJ, Swartz MA. Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling. Cancer Cell 2007;11:526-38.
18. Ng CP, Hinz B, Swartz MA. Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 2005;118:4731-9. (Pubitemid 41646383)
19. Ng CP, Swartz MA. Fibroblast alignment under interstitial fluid flow using a novel 3-D tissue culture model. Am J Physiol Heart Circ Physiol 2003;284:H1771-7.
20. Shi ZD, Ji XY, Qazi H, Tarbell JM. Interstitial flow promotes vascular fibroblast, myofibroblast, and smooth muscle cell motility in 3-D collagen I via upregulation of MMP-1. Am J Physiol Heart Circ Physiol 2009;297:H1225-34.
21. Provenzano PP, Inman DR, Eliceiri KW, Trier SM, Keely PJ. Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys J 2008;95:5374-84.
22. Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, Velasco P, et al. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 2001;7:192-8.
23. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, Rifkin DB. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem 1994;216:276-84.
24. Uchimura K, Morimoto-Tomita M, Bistrup A, Li J, Lyon M, Gallagher J, et al. HSulf-2, an extracellular endoglucosamine-6-sulfatase, selectively mobilizes heparin-bound growth factors and chemokines: effects on VEGF, FGF-1, and SDF-1. BMC Biochem 2006;7:2.
25. Wipff PJ, Rifkin DB, Meister JJ, Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 2007;179:1311-23. (Pubitemid 350277747)
26. Cordeiro MF, Bhattacharya SS, Schultz GS, Khaw PT. TGF-beta1, -beta2, and -beta3 in vitro: biphasic effects on Tenon's fibroblast contraction, proliferation, and migration. Invest Ophthalmol Vis Sci 2000;41:756-63.
27. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J 2002;21:1743-53.
28. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010;141:52-67.
29. Singer CF, Kronsteiner N, Marton E, Kubista M, Cullen KJ, Hirtenlehner K, et al. MMP-2 and MMP-9 expression in breast cancer-derived human fibroblasts is differentially regulated by stromal-epithelial interactions. Breast Cancer Res Treat 2002;72:69-77.
30. Kim A, Lakshman N, Petroll WM. Quantitative assessment of local collagen matrix remodeling in 3-D culture: the role of Rho kinase. Exp Cell Res 2006;312:3683-92.
31. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K, et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 2007;9:1392-400.
32. Beningo KA, Hamao K, Dembo M, Wang YL, Hosoya H. Traction forces of fibroblasts are regulated by the Rho-dependent kinase but not by the myosin light chain kinase. Arch Biochem Biophys 2006;456:224-31. (Pubitemid 44880290)
33. Totsukawa G, Wu Y, Sasaki Y, Hartshorne DJ, Yamakita Y, Yamashiro S, et al. Distinct roles of MLCK and ROCK in the regulation of membrane protrusions and focal adhesion dynamics during cell migration of fibroblasts. J Cell Biol 2004;164:427-39.
34. Even-Ram S, Doyle AD, Conti MA, Matsumoto K, Adelstein RS, Yamada KM. Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat Cell Biol 2007;9:299-309.
35. Niggli V, Schmid M, Nievergelt A. Differential roles of Rho-kinase and myosin light chain kinase in regulating shape, adhesion, and migration of HT1080 fibrosarcoma cells. Biochem Biophys Res Commun 2006;343:602-8.
36. Bierie B, Moses HL. Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer 2006;6:506-20.
37. Postlethwaite AE, Keski-Oja J, Moses HL, Kang AH. Stimulation of the chemotactic migration of human fibroblasts by transforming growth factor beta. J Exp Med 1987;165:251-6.
38. Brenmoehl J, Miller SN, Hofmann C, Vogl D, Falk W, Schölmerich J, et al. Transforming growth factor-beta 1 induces intestinal myofibroblast differentiation and modulates their migration. World J Gastroenterol 2009;15:1431-42.
39. Ahamed J, Burg N, Yoshinaga K, Janczak CA, Rifkin DB, Coller BS. In vitro and in vivo evidence for shear-induced activation of latent transforming growth factor-beta1. Blood 2008;112:3650-60.
40. Jenkins G. The role of proteases in transforming growth factor-beta activation. Int J Biochem Cell Biol 2008;40:1068-78.
41. Wipff PJ, Hinz B. Integrins and the activation of latent transforming growth factor beta1-an intimate relationship. Eur J Cell Biol 2008;87:601-15.
42. Pedersen JA, Boschetti F, Swartz MA. Effects of extracellular fiber architecture on cell membrane shear stress in a 3D fibrous matrix. J Biomech 2007;40:1484-92.
43. Pedersen JA, Lichter S, Swartz MA. Cells in 3D matrices under interstitial flow: effects of extracellular matrix alignment on cell shear stress and drag forces. J Biomech 2010;43:900-5.
44. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 2007;9:893-904. (Pubitemid 47190444)
45. Friedl P, Maaser K, Klein CE, Niggemann B, Krohne G, Zanker KS. Migration of highly aggressive MV3 melanoma cells in 3-dimensional collagen lattices results in local matrix reorganization and shedding of alpha2 and beta1 integrins and CD44. Cancer Res 1997;57:2061-70.
46. Yanase M, Ikeda H, Ogata I, Matsui A, Noiri E, Tomiya T, et al. Functional diversity between Rho-kinase- and MLCK-mediated cytoskeletal actions in a myofibroblast-like hepatic stellate cell line. Biochem Biophys Res Commun 2003;305:223-8.
47. Follonier Castella L, Gabbiani G, McCulloch CA, Hinz B. Regulation of myofibroblast activities: calcium pulls some strings behind the scene. Exp Cell Res 2010;316:2390-401.
48. Winer JP, Oake S, Janmey PA. Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation. PLoS One 2009;4:e6382.
49. Ulrich TA, de Juan Pardo EM, Kumar S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res 2009;69:4167-74.
50. Ulrich TA, Jain A, Tanner K, MacKay JL, Kumar S. Probing cellular mechanobiology in three-dimensional culture with collagen-agarose matrices. Biomaterials 2010;31:1875-84.