The role of the tissue microenvironment in the regulation of cancer cell motility and invasion

. 2010 Sep 07 ; 8 () : 22. [epub] 20100907

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid20822526

During malignant neoplastic progression the cells undergo genetic and epigenetic cancer-specific alterations that finally lead to a loss of tissue homeostasis and restructuring of the microenvironment. The invasion of cancer cells through connective tissue is a crucial prerequisite for metastasis formation. Although cell invasion is foremost a mechanical process, cancer research has focused largely on gene regulation and signaling that underlie uncontrolled cell growth. More recently, the genes and signals involved in the invasion and transendothelial migration of cancer cells, such as the role of adhesion molecules and matrix degrading enzymes, have become the focus of research. In this review we discuss how the structural and biomechanical properties of extracellular matrix and surrounding cells such as endothelial cells influence cancer cell motility and invasion. We conclude that the microenvironment is a critical determinant of the migration strategy and the efficiency of cancer cell invasion.

Zobrazit více v PubMed

Kopfstein L, Christofori G. Metastasis: cell-autonomous mechanisms versus contributions by the tumor microenvironment. Cell Mol Life Sci. 2006;63:449–468. doi: 10.1007/s00018-005-5296-8. PubMed DOI PMC

Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D. et al.Tensional homeostasis and the malignant phenotype. Cancer Cell. 2005;8:241–254. doi: 10.1016/j.ccr.2005.08.010. PubMed DOI

Rolli M, Fransvea E, Pilch J, Saven A, Felding-Habermann B. Activated integrin alphavbeta3 cooperates with metalloproteinase MMP-9 in regulating migration of metastatic breast cancer cells. Proc Natl Acad Sci USA. 2003;100:9482–9487. doi: 10.1073/pnas.1633689100. PubMed DOI PMC

Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, Strongin AY, Brocker EB, Friedl P. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol. 2003;160:267–277. doi: 10.1083/jcb.200209006. PubMed DOI PMC

Friedl P, Brocker EB. The biology of cell locomotion within three-dimensional extracellular matrix. Cell Mol Life Sci. 2000;57:41–64. doi: 10.1007/s000180050498. PubMed DOI PMC

Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. Cell migration: integrating signals from front to back. Science. 2003;302:1704–1709. doi: 10.1126/science.1092053. PubMed DOI

Zaman MH, Trapani LM, Sieminski AL, Mackellar D, Gong H, Kamm RD, Wells A, Lauffenburger DA, Matsudaira P. Migration of tumor cells in 3 D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci USA. 2006;103:10889–10894. doi: 10.1073/pnas.0604460103. PubMed DOI PMC

Mierke CT, Rosel D, Fabry B, Brabek J. Contractile forces in tumor cell migration. Eur J Cell Biol. 2008;87:669–676. doi: 10.1016/j.ejcb.2008.01.002. PubMed DOI PMC

Harley BA, Kim HD, Zaman MH, Yannas IV, Lauffenburger DA, Gibson LJ. Microarchitecture of three-dimensional scaffolds influences cell migration behavior via junction interactions. Biophys J. 2008;95:4013–4024. doi: 10.1529/biophysj.107.122598. PubMed DOI PMC

Doyle AD, Wang FW, Matsumoto K, Yamada KM. One-dimensional topography underlies three-dimensional fibrillar cell migration. J Cell Biol. 2009;184:481–490. doi: 10.1083/jcb.200810041. PubMed DOI PMC

Pajerowski JD, Dahl KN, Zhong FL, Sammak PJ, Discher DE. Physical plasticity of the nucleus in stem cell differentiation. Proc Natl Acad Sci USA. 2007;104:15619–15624. doi: 10.1073/pnas.0702576104. PubMed DOI PMC

Dahl KN, Ribeiro AJ, Lammerding J. Nuclear shape, mechanics, and mechanotransduction. Circ Res. 2008;102:1307–1318. doi: 10.1161/CIRCRESAHA.108.173989. PubMed DOI PMC

Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, Stack MS, Friedl P. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol. 2007;9:893–904. doi: 10.1038/ncb1616. PubMed DOI

Friedl P, Wolf K. Plasticity of cell migration: a multiscale tuning model. J Cell Biol. 2010;188:11–19. doi: 10.1083/jcb.200909003. PubMed DOI PMC

Shoulders MD, Raines RT. Collagen structure and stability. Annu Rev Biochem. 2009;78:929–958. doi: 10.1146/annurev.biochem.77.032207.120833. PubMed DOI PMC

Geiger B, Bershadsky A, Pankov R, Yamada KM. Transmembrane crosstalk between the extracellular matrix--cytoskeleton crosstalk. Nat Rev Mol Cell Biol. 2001;2:793–805. doi: 10.1038/35099066. PubMed DOI

Giannone G, Sheetz MP. Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol. 2006;16:213–223. doi: 10.1016/j.tcb.2006.02.005. PubMed DOI

Gehler S, Baldassarre M, Lad Y, Leight JL, Wozniak MA, Riching KM, Eliceiri KW, Weaver VM, Calderwood DA, Keely PJ. Filamin A-beta1 integrin complex tunes epithelial cell response to matrix tension. Mol Biol Cell. 2009;20:3224–3238. doi: 10.1091/mbc.E08-12-1186. PubMed DOI PMC

Kasza KE, Nakamura F, Hu S, Kollmannsberger P, Bonakdar N, Fabry B, Stossel TP, Wang N, Weitz DA. Filamin A is essential for active cell stiffening but not passive stiffening under external force. Biophys J. 2009;96:4326–4335. doi: 10.1016/j.bpj.2009.02.035. PubMed DOI PMC

Mohl C, Kirchgessner N, Schafer C, Kupper K, Born S, Diez G, Goldmann WH, Merkel R, Hoffmann B. Becoming stable and strong: the interplay between vinculin exchange dynamics and adhesion strength during adhesion site maturation. Cell Motil Cytoskeleton. 2009;66:350–364. doi: 10.1002/cm.20375. PubMed DOI

Peyton SR, Kim PD, Ghajar CM, Seliktar D, Putnam AJ. The effects of matrix stiffness and RhoA on the phenotypic plasticity of smooth muscle cells in a 3-D biosynthetic hydrogel system. Biomaterials. 2008;29:2597–2607. doi: 10.1016/j.biomaterials.2008.02.005. PubMed DOI PMC

Ulrich TA, Juan Pardo EM, Kumar S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res. 2009;69:4167–4174. doi: 10.1158/0008-5472.CAN-08-4859. PubMed DOI PMC

Lo CM, Wang HB, Dembo M, Wang YL. Cell movement is guided by the rigidity of the substrate. Biophys J. 2000;79:144–152. doi: 10.1016/S0006-3495(00)76279-5. PubMed DOI PMC

Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SF, Csiszar K, Giaccia A, Weninger W. et al.Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 2009;139:891–906. doi: 10.1016/j.cell.2009.10.027. PubMed DOI PMC

Wolf K, Friedl P. Mapping proteolytic cancer cell-extracellular matrix interfaces. Clin Exp Metastasis. 2009;26:289–298. doi: 10.1007/s10585-008-9190-2. PubMed DOI

Sabeh F, Shimizu-Hirota R, Weiss SJ. Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol. 2009;185:11–19. doi: 10.1083/jcb.200807195. PubMed DOI PMC

Abercrombie M, Turner AA. Contact reactions influencing cell locomotion of a mouse sarcoma in culture. Med Biol. 1978;56:299–303. PubMed

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;95:5374–5384. doi: 10.1529/biophysj.108.133116. PubMed DOI PMC

Pankova K, Rosel D, Novotny M, Brabek J. The molecular mechanisms of transition between mesenchymal and amoeboid invasiveness in tumor cells. Cell Mol Life Sci. 2010;67:63–71. doi: 10.1007/s00018-009-0132-1. PubMed DOI PMC

Nobes CD, Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 1995;81:53–62. doi: 10.1016/0092-8674(95)90370-4. PubMed DOI

Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 1992;70:401–410. doi: 10.1016/0092-8674(92)90164-8. PubMed DOI

Sheetz MP, Felsenfeld DP, Galbraith CG. Cell migration: regulation of force on extracellular-matrix-integrin complexes. Trends Cell Biol. 1998;8:51–54. doi: 10.1016/S0962-8924(98)80005-6. PubMed DOI

Brooks PC, Stromblad S, Sanders LC, von Schalscha TL, Aimes RT, Stetler-Stevenson WG, Quigley JP, Cheresh DA. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell. 1996;85:683–693. doi: 10.1016/S0092-8674(00)81235-0. PubMed DOI

Wei Y, Lukashev M, Simon DI, Bodary SC, Rosenberg S, Doyle MV, Chapman HA. Regulation of integrin function by the urokinase receptor. Science. 1996;273:1551–1555. doi: 10.1126/science.273.5281.1551. PubMed DOI

Goel A, Chauhan SS. Role of proteases in tumor invasion and metastasis. Indian J Exp Biol. 1997;35:553–564. PubMed

Yumura S, Mori H, Fukui Y. Localization of actin and myosin for the study of ameboid movement in Dictyostelium using improved immunofluorescence. J Cell Biol. 1984;99:894–899. doi: 10.1083/jcb.99.3.894. PubMed DOI PMC

Mandeville JT, Lawson MA, Maxfield FR. Dynamic imaging of neutrophil migration in three dimensions: mechanical interactions between cells and matrix. J Leukoc Biol. 1997;61:188–200. PubMed

Friedl P, Borgmann S, Brocker EB. Amoeboid leukocyte crawling through extracellular matrix: lessons from the Dictyostelium paradigm of cell movement. J Leukoc Biol. 2001;70:491–509. PubMed

Sahai E, Marshall CJ. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol. 2003;5:711–719. doi: 10.1038/ncb1019. PubMed DOI

Wyckoff JB, Pinner SE, Gschmeissner S, Condeelis JS, Sahai E. ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr Biol. 2006;16:1515–1523. doi: 10.1016/j.cub.2006.05.065. PubMed DOI

Rosel D, Brabek J, Tolde O, Mierke CT, Zitterbart DP, Raupach C, Bicanova K, Kollmannsberger P, Pankova D, Vesely P. et al.Up-regulation of Rho/ROCK signaling in sarcoma cells drives invasion and increased generation of protrusive forces. Mol Cancer Res. 2008;6:1410–1420. doi: 10.1158/1541-7786.MCR-07-2174. PubMed DOI

Micuda S, Rosel D, Ryska A, Brabek J. ROCK inhibitors as emerging therapeutic candidates for sarcomas. Curr Cancer Drug Targets. 2010;10:127–134. doi: 10.2174/156800910791054202. PubMed DOI

Maaser K, Wolf K, Klein CE, Niggemann B, Zanker KS, Brocker EB, Friedl P. Functional hierarchy of simultaneously expressed adhesion receptors: integrin alpha2beta1 but not CD44 mediates MV3 melanoma cell migration and matrix reorganization within three-dimensional hyaluronan-containing collagen matrices. Mol Biol Cell. 1999;10:3067–3079. PubMed PMC

Carragher NO, Walker SM, Scott Carragher LA, Harris F, Sawyer TK, Brunton VG, Ozanne BW, Frame MC. Calpain 2 and Src dependence distinguishes mesenchymal and amoeboid modes of tumour cell invasion: a link to integrin function. Oncogene. 2006;25:5726–5740. doi: 10.1038/sj.onc.1209582. PubMed DOI

Friedl P, Noble PB, Shields ED, Zanker KS. Locomotor phenotypes of unstimulated CD45RAhigh and CD45ROhigh CD4+ and CD8+ lymphocytes in three-dimensional collagen lattices. Immunology. 1994;82:617–624. PubMed PMC

Ramnath N, Creaven PJ. Matrix metalloproteinase inhibitors. Curr Oncol Rep. 2004;6:96–102. doi: 10.1007/s11912-004-0020-7. PubMed DOI

Van Goethem E, Poincloux R, Gauffre F, Maridonneau-Parini I, Le CV. Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J Immunol. 2010;184:1049–1061. doi: 10.4049/jimmunol.0902223. PubMed DOI

Liotta LA, Steeg PS, Stetler-Stevenson WG. Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell. 1991;64:327–336. doi: 10.1016/0092-8674(91)90642-C. PubMed DOI

Langley RR, Fidler IJ. Tumor cell-organ microenvironment interactions in the pathogenesis of cancer metastasis. Endocr Rev. 2007;28:297–321. doi: 10.1210/er.2006-0027. PubMed DOI

Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med. 2006;12:895–904. doi: 10.1038/nm1469. PubMed DOI

Luzzi KJ, MacDonald IC, Schmidt EE, Kerkvliet N, Morris VL, Chambers AF, Groom AC. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am J Pathol. 1998;153:865–873. PubMed PMC

Weis S, Cui J, Barnes L, Cheresh D. Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J Cell Biol. 2004;167:223–229. doi: 10.1083/jcb.200408130. PubMed DOI PMC

Voura EB, Ramjeesingh RA, Montgomery AM, Siu CH. Involvement of integrin alpha(v)beta(3) and cell adhesion molecule L1 in transendothelial migration of melanoma cells. Mol Biol Cell. 2001;12:2699–2710. PubMed PMC

Tremblay PL, Auger FA, Huot J. Regulation of transendothelial migration of colon cancer cells by E-selectin-mediated activation of p38 and ERK MAP kinases. Oncogene. 2006;25:6563–6573. doi: 10.1038/sj.onc.1209664. PubMed DOI

Sandig M, Voura EB, Kalnins VI, Siu CH. Role of cadherins in the transendothelial migration of melanoma cells in culture. Cell Motil Cytoskeleton. 1997;38:351–364. doi: 10.1002/(SICI)1097-0169(1997)38:4<351::AID-CM5>3.0.CO;2-6. PubMed DOI

Fidler IJ, Hart IR. Biological diversity in metastatic neoplasms: origins and implications. Science. 1982;217:998–1003. doi: 10.1126/science.7112116. PubMed DOI

Nicolson GL. Metastatic tumor cell interactions with endothelium, basement membrane and tissue. Curr Opin Cell Biol. 1989;1:1009–1019. doi: 10.1016/0955-0674(89)90073-2. PubMed DOI

Stetler-Stevenson WG, Aznavoorian S, Liotta LA. Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu Rev Cell Biol. 1993;9:541–573. doi: 10.1146/annurev.cb.09.110193.002545. PubMed DOI

Zijlstra A, Lewis J, Degryse B, Stuhlmann H, Quigley JP. The inhibition of tumor cell intravasation and subsequent metastasis via regulation of in vivo tumor cell motility by the tetraspanin CD151. Cancer Cell. 2008;13:221–234. doi: 10.1016/j.ccr.2008.01.031. PubMed DOI PMC

Kedrin D, Gligorijevic B, Wyckoff J, Verkhusha VV, Condeelis J, Segall JE, van Rheenen J. Intravital imaging of metastatic behavior through a mammary imaging window. Nat Methods. 2008;5:1019–1021. doi: 10.1038/nmeth.1269. PubMed DOI PMC

Mierke CT, Zitterbart DP, Kollmannsberger P, Raupach C, Schlotzer-Schrehardt U, Goecke TW, Behrens J, Fabry B. Breakdown of the endothelial barrier function in tumor cell transmigration. Biophys J. 2008;94:2832–2846. doi: 10.1529/biophysj.107.113613. PubMed DOI PMC

Laferriere J, Houle F, Taher MM, Valerie K, Huot J. Transendothelial migration of colon carcinoma cells requires expression of E-selectin by endothelial cells and activation of stress-activated protein kinase-2 (SAPK2/p38) in the tumor cells. J Biol Chem. 2001;276:33762–33772. doi: 10.1074/jbc.M008564200. PubMed DOI

Rousseau S, Houle F, Landry J, Huot J. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene. 1997;15:2169–2177. doi: 10.1038/sj.onc.1201380. PubMed DOI

Li YH, Zhu C. A modified Boyden chamber assay for tumor cell transendothelial migration in vitro. Clin Exp Metastasis. 1999;17:423–429. doi: 10.1023/A:1006614232388. PubMed DOI

Heyder C, Gloria-Maercker E, Entschladen F, Hatzmann W, Niggemann B, Zanker KS, Dittmar T. Realtime visualization of tumor cell/endothelial cell interactions during transmigration across the endothelial barrier. J Cancer Res Clin Oncol. 2002;128:533–538. doi: 10.1007/s00432-002-0377-7. PubMed DOI

Khuon S, Liang L, Dettman RW, Sporn PH, Wysolmerski RB, Chew TL. Myosin light chain kinase mediates transcellular intravasation of breast cancer cells through the underlying endothelial cells: a three-dimensional FRET study. J Cell Sci. 2010;123:431–440. doi: 10.1242/jcs.053793. PubMed DOI PMC

Wittchen ES, Worthylake RA, Kelly P, Casey PJ, Quilliam LA, Burridge K. Rap1 GTPase inhibits leukocyte transmigration by promoting endothelial barrier function. J Biol Chem. 2005;280:11675–11682. doi: 10.1074/jbc.M412595200. PubMed DOI

Chandrasekharan UM, Siemionow M, Unsal M, Yang L, Poptic E, Bohn J, Ozer K, Zhou Z, Howe PH, Penn M. et al.Tumor necrosis factor alpha (TNF-alpha) receptor-II is required for TNF-alpha-induced leukocyte-endothelial interaction in vivo. Blood. 2007;109:1938–1944. doi: 10.1182/blood-2006-05-020875. PubMed DOI PMC

McGettrick HM, Lord JM, Wang KQ, Rainger GE, Buckley CD, Nash GB. Chemokine- and adhesion-dependent survival of neutrophils after transmigration through cytokine-stimulated endothelium. J Leukoc Biol. 2006;79:779–788. doi: 10.1189/jlb.0605350. PubMed DOI PMC

Gallatin WM, Weissman IL, Butcher EC. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature. 1983;304:30–34. doi: 10.1038/304030a0. PubMed DOI

Carraway RE, Cochrane DE, Salmonsen R. Increased plasma levels of leukotrienes in response to neurotensin. Ann N Y Acad Sci. 1992;668:317–319. doi: 10.1111/j.1749-6632.1992.tb27362.x. PubMed DOI

Reiland J, Furcht LT, McCarthy JB. CXC-chemokines stimulate invasion and chemotaxis in prostate carcinoma cells through the CXCR2 receptor. Prostate. 1999;41:78–88. doi: 10.1002/(SICI)1097-0045(19991001)41:2<78::AID-PROS2>3.0.CO;2-P. PubMed DOI

Al Mehdi AB, Tozawa K, Fisher AB, Shientag L, Lee A, Muschel RJ. Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat Med. 2000;6:100–102. doi: 10.1038/71429. PubMed DOI

Tolde O, Rosel D, Vesely P, Folk P, Brabek J. The structure of invadopodia in a complex 3 D environment. Eur J Cell Biol. 2010;89:674–680. doi: 10.1016/j.ejcb.2010.04.003. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...