Tumour-cell invasion and migration: diversity and escape mechanisms (original) (raw)
Chambers, A. F., Groom, A. C. & MacDonald, I. C. Dissemination and growth of cancer cells in metastatic sites. Nature Rev. Cancer2, 563–572 (2002). CAS Google Scholar
Friedl, P. & Bröcker, E. -B. The biology of cell locomotion within three-dimensional extracellular matrix. Cell. Mol. Life Sci.57, 41–64 (2000). CASPubMed Google Scholar
Abercrombie, M., Dunn, G. A. & Heath, J. P. The shape and movement of fibroblasts in culture. Soc. Gen. Physiol. Ser.32, 57–70 (1977). CASPubMed Google Scholar
Lauffenburger, D. A. & Horwitz, A. F. Cell migration: a physically integrated molecular process. Cell84, 359–369 (1996). The 'bible' for cell migration researchers. CASPubMed Google Scholar
Adams, J. C. Cell-matrix contact structures. Cell. Mol. Life Sci.58, 371–392 (2001). CASPubMed Google Scholar
Burridge, K. & Chrzanowska-Wodicka, M. Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol.12, 463–519 (1996). CASPubMed Google Scholar
Cramer, L. P. Organization and polarity of actin filament networks in cells: implications for the mechanism of myosin-based cell motility. Biochem. Soc. Symp.65, 173–205 (1999). CASPubMed Google Scholar
Rohatgi, R. et al. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell97, 221–231 (1999). CASPubMed Google Scholar
Hynes, R. O. Integrins: bidirectional, allosteric signaling machines. Cell110, 673–687 (2002). CASPubMed Google Scholar
Otey, C. A. & Burridge, K. Patterning of the membrane cytoskeleton by the extracellular matrix. Semin. Cell Biol.1, 391–399 (1990). CASPubMed Google Scholar
Zamir, E. et al. Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nature Cell Biol.2, 191–196 (2000). CASPubMed Google Scholar
Zamir, E. & Geiger, B. Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci.114, 3583–3590 (2001). References 11 and 12 explain the dynamic nature and diversity of cell-matrix interactions. They provide the molecular basis for plasticity and adaptation responses in cell migration. CASPubMed Google Scholar
Regen, C. M. & Horwitz, A. F. Dynamics of beta 1 integrin-mediated adhesive contacts in motile fibroblasts. J. Cell Biol.119, 1347–1359 (1992). CASPubMed Google Scholar
Smilenov, L. B., Mikhailov, A., Pelham, R. J., Marcantonio, E. E. & Gundersen, G. G. Focal adhesion motility revealed in stationary fibroblasts. Science286, 1172–1174 (1999). CASPubMed Google Scholar
Cukierman, E., Pankov, R., Stevens, D. R. & Yamada, K. M. Taking cell-matrix adhesions to the third dimension. Science294, 1708–1712 (2001). CASPubMed Google Scholar
Rabinovitz, I. & Mercurio, A. M. The integrin alpha6beta4 functions in carcinoma cell migration on laminin-1 by mediating the formation and stabilization of actin-containing motility structures. J. Cell Biol.139, 1873–1884 (1997). CASPubMedPubMed Central Google Scholar
Leavesley, D. I., Ferguson, G. D., Wayner, E. A. & Cheresh, D. A. Requirement of the integrin beta 3 subunit for carcinoma cell spreading or migration on vitronectin and fibrinogen. J. Cell Biol.117, 1101–1107 (1992). CASPubMed Google Scholar
Maaser, K. et al. 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. Cell10, 3067–3079 (1999). CASPubMedPubMed Central Google Scholar
Friedl, P. et al. 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.57, 2061–2070 (1997). CASPubMed Google Scholar
Friedl, P. & Wolf, K. Proteolytic and non–proteolytic migration in tumor cells and leukocytes. Biochem. Soc. Symp. (in the press).
Byers, H. R. & Fujiwara, K. Stress fibers in cells in situ: immunofluorescence visualization with antiactin, antimyosin, and anti-alpha-actinin. J. Cell Biol.93, 804–811 (1982). CASPubMed Google Scholar
Chew, T. L., Wolf, W. A., Gallagher, P. J., Matsumura, F. & Chisholm, R. L. A fluorescent resonant energy transfer-based biosensor reveals transient and regional myosin light chain kinase activation in lamella and cleavage furrows. J. Cell Biol.156, 543–553 (2002). CASPubMedPubMed Central Google Scholar
Kaibuchi, K., Kuroda, S. & Amano, M. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem.68, 459–486 (1999). CASPubMed Google Scholar
Totsukawa, G. et al. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol.150, 797–806 (2000). CASPubMedPubMed Central Google Scholar
Kamm, K. E. & Stull, J. T. Dedicated myosin light chain kinases with diverse cellular functions. J. Biol. Chem.276, 4527–4530 (2001). CASPubMed Google Scholar
Somlyo, A. V. et al. Rho kinase and matrix metalloproteinase inhibitors cooperate to inhibit angiogenesis and growth of human prostate cancer xenotransplants. FASEB J.17, 223–234 (2003). CASPubMed Google Scholar
Verkhovsky, A. B., Svitkina, T. M. & Borisy, G. G. Myosin II filament assemblies in the active lamella of fibroblasts: their morphogenesis and role in the formation of actin filament bundles. J. Cell Biol.131, 989–1002 (1995). CASPubMed Google Scholar
Friedl, P. & Brocker, E. B. in Image Analysis. Methods and Applications 2nd edn (ed. Hader, D. P.) 9–21 (CRC Press, London, 2001). Google Scholar
Palecek, S. P., Loftus, J. C., Ginsberg, M. H., Lauffenburger, D. A. & Horwitz, A. F. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature385, 537–540 (1997). CASPubMed Google Scholar
Ballestrem, C., Hinz, B., Imhof, B. A. & Wehrle-Haller, B. Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior. J. Cell Biol.155, 1319–1332 (2001). CASPubMedPubMed Central Google Scholar
Friedl, P., Zanker, K. S. & Bröcker, E. -B. Cell migration strategies in 3-D extracellular matrix: differences in morphology, cell matrix interactions, and integrin function. Microsc. Res. Tech.43, 369–378 (1998). CASPubMed Google Scholar
Entschladen, F., Niggemann, B., Zänker, K. S. & Friedl, P. Differential requirement of protein tyrosine kinases and protein kinase C in the regulation of T cell locomotion in three-dimensional collagen matrices. J. Immunol.159, 3203–3210 (1997). CASPubMed Google Scholar
Friedl, P., Entschladen, F., Conrad, C., Niggemann, B. & Zanker, K. S. CD4+ T lymphocytes migrating in three-dimensional collagen lattices lack focal adhesions and utilize beta1 integrin-independent strategies for polarization, interaction with collagen fibers and locomotion. Eur. J. Immunol.28, 2331–2343 (1998). CASPubMed Google Scholar
Yamada, K. M. et al. Monoclonal antibody and synthetic peptide inhibitors of human tumor cell migration. Cancer Res.50, 4485–4496 (1990). CASPubMed Google Scholar
Filardo, E. J., Brooks, P. C., Deming, S. L., Damsky, C. & Cheresh, D. A. Requirement of the NPXY motif in the integrin beta 3 subunit cytoplasmic tail for melanoma cell migration in vitro and in vivo. J. Cell Biol.130, 441–450 (1995). CASPubMed Google Scholar
Flanagan, L. A. et al. Filamin A, the Arp2/3 complex, and the morphology and function of cortical actin filaments in human melanoma cells. J. Cell Biol.155, 511–517 (2001). CASPubMedPubMed Central Google Scholar
Sameni, M., Moin, K. & Sloane, B. F. Imaging proteolysis by living human breast cancer cells. Neoplasia2, 496–504 (2001). Google Scholar
Rosenthal, E. L., Hotary, K., Bradford, C. & Weiss, S. J. Role of membrane type 1-matrix metalloproteinase and gelatinase A in head and neck squamous cell carcinoma invasion in vitro. Otolaryngol. Head Neck Surg.121, 337–343 (1999). CASPubMed Google Scholar
Koblinski, J. E., Ahram, M. & Sloane, B. F. Unraveling the role of proteases in cancer. Clin. Chim. Acta291, 113–135 (2000). CASPubMed Google Scholar
Hofmann, U. B., Westphal, J. R., van Muijen, G. N. & Ruiter, D. J. Matrix metalloproteinases in human melanoma. J. Invest. Dermatol.115, 337–344 (2000). CASPubMed Google Scholar
Deryugina, E. I., Bourdon, M. A., Reisfeld, R. A. & Strongin, A. Remodeling of collagen matrix by human tumor cells requires activation and cell surface association of matrix metalloproteinase-2. Cancer Res.58, 3743–3750 (1998). CASPubMed Google Scholar
Maekawa, K., Sato, H., Furukawa, M. & Yoshizaki, T. Inhibition of cervical lymph node metastasis by marimastat (BB-2516) in an orthotopic oral squamous cell carcinoma implantation model. Clin. Exp. Metastasis19, 513–518 (2002). CASPubMed Google Scholar
Rudolph-Owen, L. A., Chan, R., Muller, W. J. & Matrisian, L. M. The matrix metalloproteinase matrilysin influences early-stage mammary tumorigenesis. Cancer Res.58, 5500–5506 (1998). CASPubMed Google Scholar
Sahai, E., Olson, M. F. & Marshall, C. J. Cross-talk between Ras and Rho signalling pathways in transformation favours proliferation and increased motility. EMBO J.20, 755–766 (2001). CASPubMedPubMed Central Google Scholar
Clark, E. A., Golub, T. R., Lander, E. S. & Hynes, R. O. Genomic analysis of metastasis reveals an essential role for RhoC. Nature406, 532–535 (2000). CASPubMed Google Scholar
Itoh, K. et al. An essential part for Rho-associated kinase in the transcellular invasion of tumor cells. Nature Med.5, 221–225 (1999). CASPubMed Google Scholar
Kaneko, K., Satoh, K., Masamune, A., Satoh, A. & Shimosegawa, T. Myosin light chain kinase inhibitors can block invasion and adhesion of human pancreatic cancer cell lines. Pancreas24, 34–41 (2002). PubMed Google Scholar
Allman, R., Cowburn, P. & Mason, M. In vitro and in vivo effects of a cyclic peptide with affinity for the alpha(nu)beta3 integrin in human melanoma cells. Eur. J. Cancer36, 410–422 (2000). CASPubMed Google Scholar
Gianelli, G., Falk-Marzillier, J., Schiraldi, O., Stetler-Stevenson, W. G. & Quaranta, V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science277, 225–228 (1997). Google Scholar
Alper, O. et al. Epidermal growth factor receptor signaling and the invasive phenotype of ovarian carcinoma cells. J. Natl Cancer Inst.93, 1375–1384 (2001). CASPubMed Google Scholar
Seftor, R. E. et al. Cooperative interactions of laminin 5 gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res.61, 6322–6327 (2001). CASPubMed Google Scholar
Brooks, P. C. et al. Insulin-like growth factor receptor cooperates with integrin alpha v beta 5 to promote tumor cell dissemination in vivo. J. Clin. Invest.99, 1390–1398 (1997). CASPubMedPubMed Central Google Scholar
Thiery, J. P. Epithelial–mesenchymal transitions in tumour progression. Nature Rev. Cancer2, 442–454 (2002). Comprehensive review on a classic example of plasticity during tumour invasion. CAS Google Scholar
Enterline, H. T. & Cohen, D. R. The ameboid motility of human and animal neoplastic cells. Cancer3, 1033–1038 (1950). CASPubMed Google Scholar
Wood, S. Jr. Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber. Arch. Pathol.66, 550–568 (1958). Google Scholar
Wolf, K. et al. Compensation mechanism in tumor cell migration: mesenchymal–amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol.160, 267–277 (2003). A novel escape mechanism after the blocking of pericellular proteolysis. By converting to a more 'primitive' amoeboid migration mode, previously proteolytic tumour cells continue to move non-proteolytically by path-finding migration strategies. CASPubMedPubMed Central Google Scholar
Paulus, W., Baur, I., Beutler, A. S. & Reeves, S. A. Diffuse brain invasion of glioma cells requires beta 1 integrins. Lab. Invest.75, 819–826 (1996). CASPubMed Google Scholar
Polette, M. et al. Association of fibroblastoid features with the invasive phenotype in human bronchial cancer cell lines. Clin. Exp. Metastasis16, 105–112 (1998). CASPubMed Google Scholar
Tester, A. M., Ruangpani, N., Anderso, R. L. & Thompson, E. W. MMP-9 secretion and MMP-2 activation distinguish invasive and metastatic sublines of a mouse mammary carcinoma system showing epithelial–mesenchymal transition traits. Clin. Exp. Metastasis18, 553–560 (2000). CASPubMed Google Scholar
Putz, E. et al. Phenotypic characteristics of cell lines derived from disseminated cancer cells in bone marrow of patients with solid epithelial tumors: establishment of working models for human micrometastases. Cancer Res.59, 241–248 (1999). CASPubMed Google Scholar
d'Ortho, M. P. et al. MT1-MMP on the cell surface causes focal degradation of gelatin films. FEBS Lett.421, 159–164 (1998). CASPubMed Google Scholar
Jeffers, M., Rong, S. & Vande, W. G. Enhanced tumorigenicity and invasion-metastasis by hepatocyte growth factor/scatter factor-Met signalling in human cells concomitant with induction of the urokinase proteolysis network. Mol. Cell. Biol16, 1115–1125 (1996). CASPubMedPubMed Central Google Scholar
Pulyaeva, H. et al. MT1-MMP correlates with MMP-2 activation potential seen after epithelial to mesenchymal transition in human breast carcinoma cells. Clin. Exp. Metastasis15, 111–120 (1997). CASPubMed Google Scholar
Sternlicht, M. D. et al. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell98, 137–146 (1999). CASPubMedPubMed Central Google Scholar
Yoshioka, K., Nakamori, S. & Itoh, K. Overexpression of small GTP-binding protein RhoA promotes invasion of tumor cells. Cancer Res.59, 2004–2010 (1999). CASPubMed Google Scholar
Condeelis, J., Jones, J. & Segall, J. E. Chemotaxis of metastatic tumor cells: clues to mechanisms from the Dictyostelium paradigm. Cancer Metastasis Rev.11, 55–68 (1992). CASPubMed Google Scholar
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.99, 894–899 (1984). CASPubMed Google Scholar
Devreotes, P. N. & Zigmond, S. H. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu. Rev. Cell Biol.4, 649–686 (1988). CASPubMed Google Scholar
Fey, P., Stephens, S., Titus, M. A. & Chisholm, R. L. SadA, a novel adhesion receptor in Dictyostelium. J. Cell Biol.159, 1109–1119 (2002). CASPubMedPubMed Central Google Scholar
Farina, K. L. et al. Cell motility of tumor cells visualized in living intact primary tumors using green fluorescent protein. Cancer Res.58, 2528–2532 (1998). Fascinatingin vivoimaging of amoeboid tumour-cell movement. CASPubMed Google Scholar
Friedl, P., Borgmann, S. & Brocker, E. B. Leukocyte crawling through extracellular matrix and the Dictyostelium paradigm of movement: lessons from a social amoeba. J. Leukoc. Biol.70, 491–509 (2001). CASPubMed Google Scholar
Lewis, W. H. On the locomotion of the polymorphonuclear neutrophiles of the rat in autoplasma cultures. Bull. Johns Hopkins. Hosp.4, 273–279 (1934). One of the first papers showing shape change as a mechanism to bypass ECM barriers. Google Scholar
Werr, J., Xie, X., Hedqvist, P., Ruoslahti, E. & Lindbom, L. Beta1 integrins are critically involved in neutrophil locomotion in extravascular tissue in vivo. J. Exp. Med.187, 2091–2096 (1998). CASPubMedPubMed Central Google Scholar
Brakebusch, C. et al. Beta1 integrin is not essential for hematopoiesis but is necessary for the T cell-dependent IgM antibody response. Immunity16, 465–477 (2002). CASPubMed Google Scholar
Haston, W. S., Shields, J. M. & Wilkinson, P. C. Lymphocyte locomotion and attachment on two-dimensional surfaces and in three-dimensional matrices. J. Cell Biol.92, 747–752 (1982). Provides the first example of 'non-adhesive' migration in 3D collagen lattices. CASPubMedPubMed Central Google Scholar
Mandeville, J. T., Lawson, M. A. & Maxfield, F. R. Dynamic imaging of neutrophil migration in three dimensions: mechanical interactions between cells and matrix. J. Leukoc. Biol.61, 188–200 (1997). CASPubMed Google Scholar
Verschueren, H., de Baetselier, P. & Bereiter-Hahn, J. Dynamic morphology of metastatic mouse T-lymphoma cells invading through monolayers of 10T1/2 cells. Cell Motil. Cytoskeleton20, 203–214 (1991). CASPubMed Google Scholar
Rintoul, R. C. & Sethi, T. The role of extracellular matrix in small-cell lung cancer. Lancet Oncol.2, 437–442 (2002). Google Scholar
Falcioni, R. et al. Expression of beta 1, beta 3, beta 4, and beta 5 integrins by human lung carcinoma cells of different histotypes. Exp. Cell Res.210, 113–122 (1994). CASPubMed Google Scholar
Jaspars, L. H., Bonnet, P., Bloemena, E. & Meijer, C. J. Extracellular matrix and beta 1 integrin expression in nodal and extranodal T-cell lymphomas. J. Pathol.178, 36–43 (1996). CASPubMed Google Scholar
Kraus, A. C. et al. In vitro chemo- and radio-resistance in small cell lung cancer correlates with cell adhesion and constitutive activation of AKT and MAP kinase pathways. Oncogene21, 8683–8695 (2002). CASPubMed Google Scholar
Jacques, T. S. et al. Neural precursor cell chain migration and division are regulated through different beta1 integrins. Development125, 3167–3177 (1998). CASPubMed Google Scholar
El Fahime, E., Torrente, Y., Caron, N. J., Bresolin, M. D. & Tremblay, J. P. In vivo migration of transplanted myoblasts requires matrix metalloproteinase activity. Exp. Cell Res.258, 279–287 (2000). CASPubMed Google Scholar
Page, D. L., Anderson, T. J. & Sakamoto, G. in Diagnostic Histopathology of the Breast 219–222 (Churchill Livingstone, New York, 1987). Google Scholar
Pitts, W. C. et al. Carcinomas with metaplasia and sarcomas of the breast. Am. J. Clin. Pathol.95, 623–632 (1991). CASPubMed Google Scholar
Seftor, E. A. et al. Molecular determinants of human uveal melanoma invasion and metastasis. Clin. Exp. Metastasis19, 233–246 (2002). CASPubMed Google Scholar
Davidson, L. A. & Keller, R. E. Neural tube closure in Xenopus laevis involves medial migration, directed protrusive activity, cell intercalation and convergent extension. Development126, 4547–4556 (1999). CASPubMed Google Scholar
Klinowska, T. C. et al. Laminin and beta1 integrins are crucial for normal mammary gland development in the mouse. Dev. Biol.215, 13–32 (1999). CASPubMed Google Scholar
Simian, M. et al. The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development128, 3117–3131 (2001). CASPubMed Google Scholar
Hiraoka, N., Allen, E., Apel, I. J., Gyetko, M. R. & Weiss, S. J. Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell95, 365–377 (1998). CASPubMed Google Scholar
Collen, A. et al. Membrane-type matrix metalloproteinase-mediated angiogenesis in a fibrin-collagen matrix. Blood101, 1810–1817 (2003). CASPubMed Google Scholar
Vaughan, R. B. & Trinkaus, J. P. Movements of epithelial cell sheets in vitro. J. Cell Sci.1, 407–413 (1966). CASPubMed Google Scholar
Kolega, J. The movement of cell clusters in vitro: morphology and directionality. J. Cell Sci.49, 15–32 (1981). Provides a detailed description of how clustered cells move as a functional unit. CASPubMed Google Scholar
Friedl, P. et al. Migration of coordinated cell clusters in mesenchymal and epithelial cancer explants in vitro. Cancer Res.55, 4557–4560 (1995). CASPubMed Google Scholar
Nabeshima, K. et al. Ultrastructural study of TPA-induced cell motility: human well-differentiated rectal adenocarcinoma cells move as coherent sheets via localized modulation of cell–cell adhesion. Clin. Exp. Metastasis13, 499–508 (1995). CASPubMed Google Scholar
Hegerfeldt, Y., Tusch, M., Brocker, E. B. & Friedl, P. Collective cell movement in primary melanoma explants: plasticity of cell-cell interaction, β1-integrin function, and migration strategies. Cancer Res.62, 2125–2130 (2002). First example of collective–amoeboid transition after blocking of β1-integrins — another escape mechanism. CASPubMed Google Scholar
Nabeshima, K. et al. Front-cell-specific expression of membrane-type 1 matrix metalloproteinase and gelatinase A during cohort migration of colon carcinoma cells induced by hepatocyte growth factor/scatter factor. Cancer Res.60, 3364–3369 (2000). CASPubMed Google Scholar
Bell, C. D. & Waizbard, E. Variability of cell size in primary and metastatic human breast carcinoma. Invasion Metastasis6, 11–20 (1986). CASPubMed Google Scholar
Nabeshima, K., Inoue, T., Shimao, Y., Kataoka, H. & Koono, M. Cohort migration of carcinoma cells: differentiated colorectal carcinoma cells move as coherent cell clusters or sheets. Histol. Histopathol.14, 1183–1197 (1999). CASPubMed Google Scholar
Ackerman, A. B. & Ragaz, A. in The Lives of Lesions (ed. Ackerman, A. B.) 147–158 (Masson Publishers, New York, 1984). Google Scholar
Hashizume, R., Koizumi, H., Ihara, A., Ohta, T. & Uchikoshi, T. Expression of beta-catenin in normal breast tissue and breast carcinoma: a comparative study with epithelial cadherin and alpha-catenin. Histopathology29, 139–146 (1996). CASPubMed Google Scholar
Madhavan, M. et al. Cadherins as predictive markers of nodal metastasis in breast cancer. Mod. Pathol.14, 423–427 (2001). CASPubMed Google Scholar
Byers, S. W., Sommers, C. L., Hoxter, B., Mercurio, A. M. & Tozeren, A. Role of E-cadherin in the response of tumor cell aggregates to lymphatic, venous and arterial flow: measurement of cell–cell adhesion strength. J. Cell Sci.108, 2053–2064 (1995). CASPubMed Google Scholar
Brandt, B. et al. Isolation of prostate-derived single cells and cell clusters from human peripheral blood. Cancer Res.56, 4556–4561 (1996). CASPubMed Google Scholar
Pishvaian, M. J. et al. Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Res.59, 947–952 (1999). CASPubMed Google Scholar
Hsu, M., Andl, T., Li, G., Meinkoth, J. L. & Herlyn, M. Cadherin repertoire determines partner-specific gap junctional communication during melanoma progression. J. Cell Sci.113, 1535–1542 (2000). CASPubMed Google Scholar
Moll, R., Mitze, M., Frixen, U. H. & Birchmeier, W. Differential loss of E-cadherin expression in infiltrating ductal and lobular breast carcinomas. Am. J. Pathol.143, 1731–1742 (1993). CASPubMedPubMed Central Google Scholar
Klein, C. E., Steinmayer, T., Kaufmann, D., Weber, L. & Brocker, E. B. Identification of a melanoma progression antigen as integrin VLA-2. J. Invest. Dermatol.96, 281–284 (1991). CASPubMed Google Scholar
Trikha, M. et al. The high affinity alphaIIb beta3 integrin is involved in invasion of human melanoma cells. Cancer Res.57, 2522–2528 (1997). CASPubMed Google Scholar
Strobel, T. & Cannistra, S. A. Beta1-integrins partly mediate binding of ovarian cancer cells to peritoneal mesothelium in vitro. Gynecol. Oncol.73, 362–367 (1999). CASPubMed Google Scholar
Chao, C., Lotz, M. M., Clarke, A. C. & Mercurio, A. M. A function for the integrin alpha6beta4 in the invasive properties of colorectal carcinoma cells. Cancer Res.56, 4811–4819 (1996). CASPubMed Google Scholar
Cress, A. E., Rabinovitz, I., Zhu, W. & Nagle, R. B. The alpha 6 beta 1 and alpha 6 beta 4 integrins in human prostate cancer progression. Cancer Metastasis Rev.14, 219–228 (1995). CASPubMed Google Scholar
Danen, E. H. J. et al. Regulation of integrin-mediated adhesion to laminin and collagen in human melanocytes and in non-metastatic and highly metastatic human melanoma cells. Int. J. Cancer54, 315–321 (1993). CASPubMed Google Scholar
Zutter, M. M., Santoro, S. A., Staatz, W. D. & Tsung, Y. L. Re-expression of the alpha 2 beta 1 integrin abrogates the malignant phenotype of breast carcinoma cells. Proc. Natl Acad. Sci. USA92, 7411–7415 (1995). CASPubMedPubMed Central Google Scholar
Schirner, M. et al. Integrin alpha5beta1: a potent inhibitor of experimental lung metastasis. Clin. Exp. Metastasis16, 427–435 (1998). CASPubMed Google Scholar
Mignatti, P., Robbins, E. & Rifkin, D. B. Tumor invasion through the human amniotic membrane: requirement for a proteinase cascade. Cell47, 487–498 (1986). CASPubMed Google Scholar
Kurschat, P. et al. Tissue inhibitor of matrix metalloproteinase-2 regulates matrix metalloproteinase-2 activation by modulation of membrane-type 1 matrix metalloproteinase activity in high and low invasive melanoma cell lines. J. Biol. Chem.274, 21056–21062 (1999). CASPubMed Google Scholar
Ntayi, C., Lorimier, S., Berthier-Vergnes, O., Hornebeck, W. & Bernard, P. Cumulative influence of matrix metalloproteinase-1 and -2 in the migration of melanoma cells within three-dimensional type I collagen lattices. Exp. Cell Res.270, 110–118 (2001). CASPubMed Google Scholar
Hotary, K., Allen, E., Punturieri, A., Yana, I. & Weiss, S. J. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J. Cell Biol.149, 1309–1323 (2000). Together with references 63 and 159, this paper shows that MT1-MMP is the most important collagenase in invading tumour cells. They formally prove the concept that pericellular proteolysis contributes to invasion. CASPubMedPubMed Central Google Scholar
Wang, X., Fu, X., Brown, P. D., Crimmin, M. J. & Hoffman, R. M. Matrix metalloproteinase inhibitor BB-94 (batimastat) inhibits human colon tumor growth and spread in a patient-like orthotopic model in nude mice. Cancer Res.54, 4726–4728 (1994). CASPubMed Google Scholar
Maki, H. et al. Augmented anti-metastatic efficacy of a selective matrix metalloproteinase inhibitor, MMI-166, in combination with CPT-11. Clin. Exp. Metastasis19, 519–526 (2002). CASPubMed Google Scholar
Kruger, A. et al. Hydroxamate-type matrix metalloproteinase inhibitor batimastat promotes liver metastasis. Cancer Res.61, 1272–1275 (2001). CASPubMed Google Scholar
Della, P. P. et al. Combined treatment with serine protease inhibitor aprotinin and matrix metalloproteinase inhibitor Batimastat (BB-94) does not prevent invasion of human esophageal and ovarian carcinoma cells in vivo. Anticancer Res.19, 3809–3816 (1999). Google Scholar
Zucker, S., Cao, J. & Chen, W. T. Critical appraisal of the use of matrix metalloproteinase inhibitors in cancer treatment. Oncogene19, 6642–6650 (2000). CASPubMed Google Scholar
Coussens, L. M., Fingleton, B. & Matrisian, L. M. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science295, 2387–2392 (2002). CASPubMed Google Scholar
Overall, C. M. & Lopez-Otin, C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nature Rev. Cancer2, 657–672 (2002). References 127–129 summarize and explain the failure of clinical trials of matrix metalloproteinase inhibitors in late-stage cancer patients. It sets the scene for future work in the MMP field. CAS Google Scholar
Lochter, A., Navre, M., Werb, Z. & Bissell, M. J. alpha1 and alpha2 integrins mediate invasive activity of mouse mammary carcinoma cells through regulation of stromelysin-1 expression. Mol. Biol. Cell10, 271–282 (1999). CASPubMedPubMed Central Google Scholar
Sternlicht, M. D. & Werb, Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol.17, 463–516 (2001). CASPubMedPubMed Central Google Scholar
Sakkab, D. et al. Signaling of hepatocyte growth factor/scatter factor (HGF) to the small GTPase Rap1 via the large docking protein Gab1 and the adapter protein CRKL. J. Biol. Chem.275, 10772–10778 (2000). CASPubMed Google Scholar
Quirt, I. et al. Phase II study of marimastat (BB-2516) in malignant melanoma: a clinical and tumor biopsy study of the National Cancer Institute of Canada Clinical Trials Group. Invest. New Drugs20, 431–437 (2002). CASPubMed Google Scholar
Bonomi, P. Matrix metalloproteinases and matrix metalloproteinase inhibitors in lung cancer. Semin. Oncol.29, 78–86 (2002). CASPubMed Google Scholar
Harbeck, N., Kates, R. E. & Schmitt, M. Clinical relevance of invasion factors urokinase-type plasminogen activator and plasminogen activator inhibitor type 1 for individualized therapy decisions in primary breast cancer is greatest when used in combination. J. Clin. Oncol.20, 1000–1007 (2002). PubMed Google Scholar
Leung-Toung, R., Li, W., Tam, T. F. & Karimian, K. Thiol-dependent enzymes and their inhibitors: a review. Curr. Med. Chem.9, 979–1002 (2002). CASPubMed Google Scholar
Fassler, R. & Meyer, M. Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev.9, 1896–1908 (1995). CASPubMed Google Scholar
Fassler, R. et al. Lack of beta 1 integrin gene in embryonic stem cells affects morphology, adhesion, and migration but not integration into the inner cell mass of blastocysts. J. Cell Biol.128, 979–988 (1995). Together with references 35, 76 and 77, this paper shows that β1 integrins can be dispensable for cell movement and positioning in 3D tissue structures. CASPubMed Google Scholar
Lombardi, L. et al. Ultrastructural cytoskeleton alterations and modification of actin expression in the NIH/3T3 cell line after transformation with Ha-ras-activated oncogene. Cell Motil. Cytoskeleton15, 220–229 (1990). CASPubMed Google Scholar
Dartsch, P. C., Ritter, M., Haussinger, D. & Lang, F. Cytoskeletal reorganization in NIH 3T3 fibroblasts expressing the Ras oncogene. Eur. J. Cell Biol.63, 316–325 (1994). CASPubMed Google Scholar
Khosravi-Far, R. et al. Dbl and Vav mediate transformation via mitogen-activated protein kinase pathways that are distinct from those activated by oncogenic Ras. Mol. Cell. Biol.14, 6848–6857 (1994). CASPubMedPubMed Central Google Scholar
Qiu, R. G., Chen, J., McCormick, F. & Symons, M. A role for Rho in Ras transformation. Proc. Natl Acad. Sci. USA92, 11781–11785 (1995). CASPubMedPubMed Central Google Scholar
Whittard, J. D. & Akiyama, S. K. Activation of beta1 integrins induces cell–cell adhesion. Exp. Cell Res.263, 65–76 (2001). CASPubMed Google Scholar
Robinson, E. E., Zazzali, K. M., Corbett, S. A. & Foty, R. A. Alpha5beta1 integrin mediates strong tissue cohesion. J. Cell Sci.116, 377–386 (2003). CASPubMed Google Scholar
Whittard, J. D. et al. E-cadherin is a ligand for integrin alpha2beta1. Matrix Biol.21, 525–532 (2002). CASPubMed Google Scholar
Hynes, R. O. & Zhao, Q. The evolution of cell adhesion. J. Cell Biol.150, F89–F96 (2000). Insightful overview of how adhesion receptors evolved in the context of increasing tissue complexity and segregation. CASPubMed Google Scholar
Blanchoin, L. et al. Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nature404, 1007–1011 (2000). CASPubMed Google Scholar
Nobes, C. D. & Hall, A. Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell81, 53–62 (1995). CASPubMed Google Scholar
Ren, X. D. et al. Physical association of the small GTPase Rho with a 68-kDa phosphatidylinositol 4-phosphate 5-kinase in Swiss 3T3 cells. Mol. Biol. Cell7, 435–442 (1996). CASPubMedPubMed Central Google Scholar
Leopoldt, D. et al. Gbetagamma stimulates phosphoinositide 3-kinase-gamma by direct interaction with two domains of the catalytic p110 subunit. J. Biol. Chem.273, 7024–7029 (1998). CASPubMed Google Scholar
Tsutsumi, S., Gupta, S. K., Hogan, V., Collard, J. G. & Raz, A. Activation of small GTPase Rho is required for autocrine motility factor signaling. Cancer Res.62, 4484–4490 (2002). CASPubMed Google Scholar
Miyamoto, S. et al. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol.131, 791–805 (1995). CASPubMed Google Scholar
Calderwood, D. A., Shattil, S. J. & Ginsberg, M. H. Integrins and actin filaments: reciprocal regulation of cell adhesion and signaling. J. Biol. Chem.275, 22607–22610 (2000). CASPubMed Google Scholar
Degani, S. et al. The integrin cytoplasmic domain-associated protein ICAP-1 binds and regulates Rho family GTPases during cell spreading. J. Cell Biol.156, 377–387 (2002). CASPubMedPubMed Central Google Scholar
DeMali, K. A., Barlow, C. A. & Burridge, K. Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion. J. Cell Biol.159, 881–891 (2002). CASPubMedPubMed Central Google Scholar
Schwartz, M. A. & Shattil, S. J. Signaling networks linking integrins and Rho family GTPases. Trends Biochem. Sci.25, 388–391 (2000). CASPubMed Google Scholar
Ilic, D. et al. Reduced cell motility and anhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature377, 539–544 (1995). CASPubMed Google Scholar
Mueller, S. C. et al. A novel protease-docking function of integrin at invadopodia. J. Biol. Chem.274, 24947–24952 (1999). CASPubMed Google Scholar
Ohuchi, E. et al. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J. Biol. Chem.272, 2446–2451 (1997). CASPubMed Google Scholar
Dumin, J. A. et al. Pro-collagenase-1 (matrix metalloproteinase-1) binds the alpha(2)beta(1) integrin upon release from keratinocytes migrating on type I collagen. J. Biol. Chem.276, 29368–29374 (2001). CASPubMed Google Scholar
Brooks, P. C., Silletti, S., von Schalscha, T. L., Friedlander, M. & Cheresh, D. A. Disruption of angiogenesis by PEX, a noncatalytic metalloproteinase fragment with integrin binding activity. Cell92, 391–400 (1998). CASPubMed Google Scholar
Ellerbroek, S. M., Wu, Y. I., Overall, C. M. & Stack, M. S. Functional interplay between type I collagen and cell surface matrix metalloproteinase activity. J. Biol. Chem.276, 24833–24842 (2001). CASPubMed Google Scholar
Galvez, B. G., Matias-Roman, S., Yanez-Mo, M., Sanchez-Madrid, F. & Arroyo, A. G. ECM regulates MT1-MMP localization with beta1 or alphavbeta3 integrins at distinct cell compartments modulating its internalization and activity on human endothelial cells. J. Cell Biol.159, 509–521 (2002). CASPubMedPubMed Central Google Scholar
Tam, E. M., Wu, Y. I., Butler, G. S., Stack, M. S. & Overall, C. M. Collagen binding properties of the membrane type-1 matrix metalloproteinase (MT1-MMP) hemopexin C domain. The ectodomain of the 44-kDa autocatalytic product of MT1-MMP inhibits cell invasion by disrupting native type I collagen cleavage. J. Biol. Chem.277, 39005–39014 (2002). CASPubMed Google Scholar
Fukata, Y., Amano, M. & Kaibuchi, K. Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol. Sci.22, 32–39 (2001). CASPubMed Google Scholar
Wear, M. A., Schafer, D. A. & Cooper, J. A. Actin dynamics: assembly and disassembly of actin networks. Curr. Biol.10, R891–R895 (2000). CASPubMed Google Scholar
Zeng, L. et al. PTP alpha regulates integrin-stimulated FAK autophosphorylation and cytoskeletal rearrangement in cell spreading and migration. J. Cell Biol.160, 137–146 (2003). CASPubMedPubMed Central Google Scholar
Pfaff, M., Du, X. & Ginsberg, M. H. Calpain cleavage of integrin beta cytoplasmic domains. FEBS Lett.460, 17–22 (1999). CASPubMed Google Scholar
Moss, M. L. & Lambert, M. H. Shedding of membrane proteins by ADAM family proteases. Essays Biochem.38, 141–153 (2002). CASPubMed Google Scholar
Carragher, N. O., Levkau, B., Ross, R. & Raines, E. W. Degraded collagen fragments promote rapid disassembly of smooth muscle focal adhesions that correlates with cleavage of pp125(FAK), paxillin, and talin. J. Cell Biol.147, 619–630 (1999). CASPubMedPubMed Central Google Scholar
Bretscher, M. S. Getting membrane flow and the cytoskeleton to cooperate in moving cells. Cell87, 601–606 (1996). CASPubMed Google Scholar
Firtel, R. A. & Meili, R. Dictyostelium: a model for regulated cell movement during morphogenesis. Curr. Opin. Genet. Dev.10, 421–427 (2000). CASPubMed Google Scholar
Scotton, C. J. et al. Multiple actions of the chemokine CXCL12 on epithelial tumor cells in human ovarian cancer. Cancer Res.62, 5930–5938 (2002). CASPubMed Google Scholar
Price, J. T., Tiganis, T., Agarwal, A., Djakiew, D. & Thompson, E. W. Epidermal growth factor promotes MDA-MB-231 breast cancer cell migration through a phosphatidylinositol 3′-kinase and phospholipase C-dependent mechanism. Cancer Res.59, 5475–5478 (1999). CASPubMed Google Scholar
Sawada, K. et al. Alendronate inhibits lysophosphatidic acid-induced migration of human ovarian cancer cells by attenuating the activation of Rho. Cancer Res.62, 6015–6020 (2002). CASPubMed Google Scholar
Doerr, M. E. & Jones, J. I. The roles of integrins and extracellular matrix proteins in the insulin-like growth factor 1-stimulated chemotaxis of human breast cancer cells. J. Biol. Chem.271, 2443–2447 (1996). CASPubMed Google Scholar
Guvakova, M. A. & Surmacz, E. The activated insulin-like growth factor 1 receptor induces depolarization in breast epithelial cells characterized by actin filament disassembly and tyrosine dephosphorylation of FAK, Cas, and paxillin. Exp. Cell Res.251, 244–255 (1999). CASPubMed Google Scholar