Soft matrix is a natural stimulator for cellular invasiveness

Molecular Biology of the Cell

Volumn 25, Issue 4, 2014, Pages 457-469

  Gu, Zhizhan ^a,b   Liu, Fei ^c   Tonkova, Elina A ^a   Lee, Soo Young ^a   Tschumperlin, Daniel J ^c,d   Brenner, Michael B ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIX METALLOPROTEINASE; PROTEIN TYROSINE KINASE;

CELL ADHESION; CELL JUNCTION; CELL MOTION; CELL SURFACE; CHEMISTRY; ELASTICITY; EXTRACELLULAR MATRIX; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; HARDNESS; HUMAN; MECHANOTRANSDUCTION; METABOLISM; PATHOLOGY; PRIMARY CELL CULTURE; SURFACE PROPERTY; TUMOR CELL LINE; TUMOR INVASION; ULTRASTRUCTURE; UMBILICAL VEIN ENDOTHELIAL CELL;

ADHERENS JUNCTIONS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURFACE EXTENSIONS; ELASTICITY; EXTRACELLULAR MATRIX; FIBROBLASTS; GENE EXPRESSION REGULATION; HARDNESS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MATRIX METALLOPROTEINASES; MECHANOTRANSDUCTION, CELLULAR; NEOPLASM INVASIVENESS; PRIMARY CELL CULTURE; SRC-FAMILY KINASES; SURFACE PROPERTIES;

EID: 84894282098     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-05-0260     Document Type: Article

References (63)

1. Agarwal SK, Lee DM, Kiener HP, Brenner MB (2008). Coexpression of two mesenchymal cadherins, cadherin 11 and N-cadherin, on murine fibroblast-like synoviocytes. Arthritis Rheum 58, 1044-1054.
2. Alexander NR, Branch KM, Parekh A, Clark ES, Iwueke IC, Guelcher SA, Weaver AM (2008). Extracellular matrix rigidity promotes invadopodia activity. Curr Biol 18, 1295-1299.
3. Ayala I, Baldassarre M, Giacchetti G, Caldieri G, Tete S, Luini A, Buccione R (2008). Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J Cell Sci 121, 369-378.
4. Badowski C, Pawlak G, Grichine A, Chabadel A, Oddou C, Jurdic P, Pfaff M, Albiges-Rizo C, Block MR (2008). Paxillin phosphorylation controls invadopodia/podosomes spatiotemporal organization. Mol Biol Cell 19, 633-645.
5. Bharti S et al. (2007). Src-dependent phosphorylation of ASAP1 regulates podosomes. Mol Cell Biol 27, 8271-8283.
6. Bhowmick NA, Neilson EG, Moses HL (2004). Stromal fibroblasts in cancer initiation and progression. Nature 432, 332-337.
7. Buccione R, Orth JD, McNiven MA (2004). Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat Rev Mol Cell Biol 5, 647-657.
8. Buschman MD, Bromann PA, Cejudo-Martin P, Wen F, Pass I, Courtneidge SA (2009). The novel adaptor protein Tks4 (SH3PXD2B) is required for functional podosome formation. Mol Biol Cell 20, 1302-1311.
9. Carman CV (2009). Mechanisms for transcellular diapedesis: probing and pathfinding by "invadosome-like protrusions." J Cell Sci 122, 3025-3035.
10. Chan KT, Cortesio CL, Huttenlocher A (2009). FAK alters invadopodia and focal adhesion composition and dynamics to regulate breast cancer invasion. J Cell Biol 185, 357-370.
11. Diaz B, Shani G, Pass I, Anderson D, Quintavalle M, Courtneidge SA (2009). Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci Signal 2, ra53.
12. Discher DE, Janmey P, Wang YL (2005). Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143.
13. Duong LT, Lakkakorpi PT, Nakamura I, Machwate M, Nagy RM, Rodan GA (1998). PYK2 in osteoclasts is an adhesion kinase, localized in the sealing zone, activated by ligation of alpha(v)beta3 integrin, and phosphorylated by src kinase. J Clin Invest 102, 881-892.
14. Enomoto M et al. (2009). Autonomous regulation of osteosarcoma cell invasiveness by Wnt5a/Ror2 signaling. Oncogene 28, 3197-3208.
15. Friedl P, Alexander S (2011). Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 147, 992-1009.
16. Friedl P, Borgmann S, Brocker EB (2001). Amoeboid leukocyte crawling through extracellular matrix: lessons from the Dictyostelium paradigm of cell movement. J Leukoc Biol 70, 491-509.
17. Furmaniak-Kazmierczak E, Crawley SW, Carter RL, Maurice DH, Cote GP (2007). Formation of extracellular matrix-digesting invadopodia by primary aortic smooth muscle cells. Circ Res 100, 1328-1336.
18. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K, Sahai E (2007). Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 9, 1392-1400.
19. Gianni D, Diaz B, Taulet N, Fowler B, Courtneidge SA, Bokoch GM (2009). Novel p47(phox)-related organizers regulate localized NADPH oxidase 1 (Nox1) activity. Sci Signal 2, ra54.
20. Gil-Henn H et al. (2007). Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 178, 1053-1064.
21. Gu Z, Noss EH, Hsu VW, Brenner MB (2011). Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. J Cell Biol 193, 61-70.
22. Hauck CR, Hsia DA, Ilic D, Schlaepfer DD (2002). v-Src SH3-enhanced interaction with focal adhesion kinase at beta 1 integrin-containing invadopodia promotes cell invasion. J Biol Chem 277, 12487-12490.
23. Hinz B (2007). Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 127, 526-537.
24. Huang S, Ingber DE (2005). Cell tension, matrix mechanics, and cancer development. Cancer Cell 8, 175-176.
25. Janmey PA, McCulloch CA (2007). Cell mechanics: integrating cell responses to mechanical stimuli. Annu Rev Biomed Eng 9, 1-34.
26. Jiang G, den Hertog J, Su J, Noel J, Sap J, Hunter T (1999). Dimerization inhibits the activity of receptor-like protein-tyrosine phosphatase-alpha. Nature 401, 606-610.
27. Jodele S, Blavier L, Yoon JM, DeClerck YA (2006). Modifying the soil to affect the seed: role of stromal-derived matrix metalloproteinases in cancer progression. Cancer Metastasis Rev 25, 35-43.
28. Kessenbrock K, Plaks V, Werb Z (2010). Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141, 52-67.
29. Lammermann T, Sixt M (2009). Mechanical modes of "amoeboid" cell migration. Curr Opin Cell Biol 21, 636-644.
30. Lee DM, Kiener HP, Agarwal SK, Noss EH, Watts GF, Chisaka O, Takeichi M, Brenner MB (2007). Cadherin-11 in synovial lining formation and pathology in arthritis. Science 315, 1006-1010.
31. Levental KR et al. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906.
32. Linder S (2009). Invadosomes at a glance. J Cell Sci 122, 3009-3013.
33. Liu F, Mih JD, Shea BS, Kho AT, Sharif AS, Tager AM, Tschumperlin DJ (2010). Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J Cell Biol 190, 693-706.
34. Lorentzen A, Bamber J, Sadok A, Elson-Schwab I, Marshall CJ (2011). An ezrin-rich, rigid uropod-like structure directs movement of amoeboid blebbing cells. J Cell Sci 124, 1256-1267.
35. Magalhaes MA, Larson DR, Mader CC, Bravo-Cordero JJ, Gil-Henn H, Oser M, Chen X, Koleske AJ, Condeelis J (2011). Cortactin phosphorylation regulates cell invasion through a pH-dependent pathway. J Cell Biol 195, 903-920.
36. Mizutani K, Miki H, He H, Maruta H, Takenawa T (2002). Essential role of neural Wiskott-Aldrich syndrome protein in podosome formation and degradation of extracellular matrix in src-transformed fibroblasts. Cancer Res 62, 669-674.
37. Murphy DA, Courtneidge SA (2011). The "ins" and "outs" of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 12, 413-426.
38. Myers KA, Applegate KT, Danuser G, Fischer RS, Waterman CM (2011). Distinct ECM mechanosensing pathways regulate microtubule dynamics to control endothelial cell branching morphogenesis. J Cell Biol 192, 321-334.
39. Nada S, Okada M, MacAuley A, Cooper JA, Nakagawa H (1991). Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature 351, 69-72.
40. Nagase H, Visse R, Murphy G (2006). Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69, 562-573.
41. Neilson EG (2006). Mechanisms of disease: fibroblasts - a new look at an old problem. Nat Clin Pract Nephrol 2, 101-108.
42. Nelson CM, Vanduijn MM, Inman JL, Fletcher DA, Bissell MJ (2006). Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science 314, 298-300.
43. Ng MR, Brugge JS (2009). A stiff blow from the stroma: collagen crosslinking drives tumor progression. Cancer Cell 16, 455-457.
44. Oneyama C, Hikita T, Enya K, Dobenecker MW, Saito K, Nada S, Tarakhovsky A, Okada M (2008). The lipid raft-anchored adaptor protein Cbp controls the oncogenic potential of c-Src. Mol Cell 30, 426-436.
45. Parekh A, Ruppender NS, Branch KM, Sewell-Loftin MK, Lin J, Boyer PD, Candiello JE, Merryman WD, Guelcher SA, Weaver AM (2011). Sensing and modulation of invadopodia across a wide range of rigidities. Biophys J 100, 573-582.
46. Parsons JT, Parsons SJ (1997). Src family protein tyrosine kinases: cooperating with growth factor and adhesion signaling pathways. Curr Opin Cell Biol 9, 187-192.
47. Pathak A, Kumar S (2012). Independent regulation of tumor cell migration by matrix stiffness and confinement. Proc Natl Acad Sci USA 109, 10334-10339.
48. Pelham RJ Jr, Wang Y (1997). Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 94, 13661-13665.
49. Pignatelli J, Tumbarello DA, Schmidt RP, Turner CE (2012). Hic-5 promotes invadopodia formation and invasion during TGF-beta-induced epithelial- mesenchymal transition. J Cell Biol 197, 421-437.
50. Poincloux R, Collin O, Lizarraga F, Romao M, Debray M, Piel M, Chavrier P (2011). Contractility of the cell rear drives invasion of breast tumor cells in 3D Matrigel. Proc Natl Acad Sci USA 108, 1943-1948.
51. Sabeh F, Li XY, Saunders TL, Rowe RG, Weiss SJ (2009). Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion. J Biol Chem 284, 23001-23011.
52. Schwartz MA, Schaller MD, Ginsberg MH (1995). Integrins: emerging paradigms of signal transduction. Annu Rev Cell Dev Biol 11, 549-599.
53. Shibue T, Brooks MW, Inan MF, Reinhardt F, Weinberg RA (2012). The outgrowth of micrometastases is enabled by the formation of filopodium-like protrusions. Cancer Discov 2, 706-721.
54. Superti-Furga G, Fumagalli S, Koegl M, Courtneidge SA, Draetta G (1993). Csk inhibition of c-Src activity requires both the SH2 and SH3 domains of Src. EMBO J 12, 2625-2634.
55. Valencia X et al. (2004). Cadherin-11 provides specific cellular adhesion between fibroblast-like synoviocytes. J Exp Med 200, 1673-1679.
56. Wang HB, Dembo M, Wang YL (2000). Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am J Physiol Cell Physiol 279, C1345-C1350.
57. Williams KC, Coppolino MG (2011). Phosphorylation of membrane type 1-matrix metalloproteinase (MT1-MMP) and its vesicle-associated membrane protein 7 (VAMP7)-dependent trafficking facilitate cell invasion and migration. J Biol Chem 286, 43405-43416.
58. Wolf K, Friedl P (2011). Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol 21, 736-744.
59. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, Stack MS, Friedl P (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 9, 893-904.
60. Yamaguchi H et al. (2005). Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol 168, 441-452.
61. Yamaguchi H, Yoshida S, Muroi E, Yoshida N, Kawamura M, Kouchi Z, Nakamura Y, Sakai R, Fukami K (2011). Phosphoinositide 3-kinase signaling pathway mediated by p110alpha regulates invadopodia formation. J Cell Biol 193, 1275-1288.
62. Zachary I, Rozengurt E (1992). Focal adhesion kinase (p125FAK): a point of convergence in the action of neuropeptides, integrins, and oncogenes. Cell 71, 891-894.
63. Zaman MH, Trapani LM, Sieminski AL, Mackellar D, Gong H, Kamm RD, Wells A, Lauffenburger DA, Matsudaira P (2006). Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci USA 103, 10889-10894.