Cancer Invasion: Patterns and Mechanisms
- Authors: Krakhmal N.V.1, Zavyalova M.V.1,2,3, Denisov E.V.2,3, Vtorushin S.V.1,2, Perelmuter V.M.1,2
-
Affiliations:
- Siberian State Medical University
- Tomsk Cancer Research Institute
- Tomsk State University
- Issue: Vol 7, No 2 (2015)
- Pages: 17-28
- Section: Reviews
- Submitted: 17.01.2020
- Published: 15.06.2015
- URL: https://actanaturae.ru/2075-8251/article/view/10480
- DOI: https://doi.org/10.32607/20758251-2015-7-2-17-28
- ID: 10480
Cite item
Abstract
Cancer invasion and the ability of malignant tumor cells for directed migration and metastasis have remained a focus of research for many years. Numerous studies have confirmed the existence of two main patterns of cancer cell invasion: collective cell migration and individual cell migration, by which tumor cells overcome barriers of the extracellular matrix and spread into surrounding tissues. Each pattern of cell migration displays specific morphological features and the biochemical/molecular genetic mechanisms underlying cell migration. Two types of migrating tumor cells, mesenchymal (fibroblast-like) and amoeboid, are observed in each pattern of cancer cell invasion. This review describes the key differences between the variants of cancer cell migration, the role of epithelial-mesenchymal, collective-amoeboid, mesenchymal-amoeboid, and amoeboid-mesenchymal transitions, as well as the significance of different tumor factors and stromal molecules in tumor invasion. The data and facts collected are essential to the understanding of how the patterns of cancer cell invasion are related to cancer progression and therapy efficacy. Convincing evidence is provided that morphological manifestations of the invasion patterns are characterized by a variety of tissue (tumor) structures. The results of our own studies are presented to show the association of breast cancer progression with intratumoral morphological heterogeneity, which most likely reflects the types of cancer cell migration and results from different activities of cell adhesion molecules in tumor cells of distinct morphological structures.
About the authors
N. V. Krakhmal
Siberian State Medical University
Email: d_evgeniy@oncology.tomsk.ru
Russian Federation
M. V. Zavyalova
Siberian State Medical University; Tomsk Cancer Research Institute; Tomsk State University
Email: d_evgeniy@oncology.tomsk.ru
Russian Federation
E. V. Denisov
Tomsk Cancer Research Institute; Tomsk State University
Author for correspondence.
Email: d_evgeniy@oncology.tomsk.ru
Russian Federation
S. V. Vtorushin
Siberian State Medical University; Tomsk Cancer Research Institute
Email: d_evgeniy@oncology.tomsk.ru
Russian Federation
V. M. Perelmuter
Siberian State Medical University; Tomsk Cancer Research Institute
Email: d_evgeniy@oncology.tomsk.ru
Russian Federation
References
- van Zijl F., Krupitza G., Mikulits W. // Mutat Res. 2011, V.728, №1-2, P.23-34
- Spano D., Heck C., De Antonellis P., Christofori G., Zollo M. // Semin Cancer Biol. 2012, V.22, №3, P.234-249
- Santibanez J.F. // ISRN Dermatol. 2013, V.2013, P.597927
- Mehlen P., Puisieux A. // Nat Rev Cancer. 2006, V.6, №6, P.449-458
- Nguyen D.X., Bos P.D., Massague J. // Nat Rev Cancer. 2009, V.9, №4, P.274-284
- Monteiro J., Fodde R. // Eur J Cancer. 2010, V.46, №7, P.1198-1203
- Kovalyov A.A. // Zdorovie Ukrainy. 2011, V.4, №17, P.26-28
- Kovalyov A.A., Grudinskaya T.A., Kusnezowa T.P., Kovalyov K.A. // Oncology. 2012, V.14, №2, P.126-129
- Hay E.D. // Acta Anat (Basel). 1995, V.154, №1, P.8-20
- Kalluri R., Weinberg R.A. // J Clin Invest. 2009, V.119, №6, P.1420-1428
- Tam W.L., Weinberg R.A. // Nat Med. 2013, V.19, №11, P.1438-1449
- Cox E.A., Sastry S.K., Huttenlocher A. // Mol Biol Cell. 2001, V.12, №2, P.265-277
- Friedl P., Hegerfeldt Y., Tusch M. // Int J Dev Biol. 2004, V.48, №5-6, P.441-449
- Friedl P., Alexander S. // Cell. 2011, V.147, №5, P.992-1009
- Friedl P., Locker J., Sahai E., Segall J.E. // Nat Cell Biol. 2012, V.14, №8, P.777-783
- Hernandez-Caballero M.E. // Molecular mechanisms of metastasis: epithelial-mesenchymal transition, anoikis and loss of adhesion. In Carcinogenesis, Tonissen K 2013, P.165-194
- Friedl P., Gilmour D. // Nat Rev Mol Cell Biol. 2009, V.10, №7, P.445-457
- Ulrich F., Heisenberg C.P. // Traffic. 2009, V.10, №7, P.811-818
- Khalil A.A., Friedl P. // Integr Biol (Camb). 2010, V.2, №11-12, P.568-574
- Yilmaz M., Christofori G. // Mol Cancer Res. 2010, V.8, №5, P.629-642
- Friedl P., Wolf K. // J Cell Biol. 2010, V.188, №1, P.11-19
- Pankova K., Rosel D., Novotny M., Brabek J. // Cell Mol Life Sci. 2010, V.67, №1, P.63-71
- Scott R.W., Crighton D., Olson M.F. // J Vis Exp. 2011, №58
- Cheung K.J., Gabrielson E., Werb Z., Ewald A.J. // Cell. 2013, V.155, №7, P.1639-1651
- Kitamura T., Kometani K., Hashida H., Matsunaga A., Miyoshi H., Hosogi H., Aoki M., Oshima M., Hattori M., Takabayashi A. // Nat Genet. 2007, V.39, №4, P.467-475
- Giampieri S., Manning C., Hooper S., Jones L., Hill C.S., Sahai E. // Nat Cell Biol. 2009, V.11, №11, P.1287-1296
- Sanz-Moreno V., Marshall C.J. // Curr Opin Cell Biol. 2010, V.22, №5, P.690-696
- Lecaudey V., Cakan-Akdogan G., Norton W.H., Gilmour D. // Development. 2008, V.135, №16, P.2695-2705
- Aman A., Piotrowski T. // Dev Cell. 2008, V.15, №5, P.749-761
- Vitorino P., Meyer T. // Genes Dev. 2008, V.22, №23, P.3268-3281
- Taylor M.A., Parvani J.G., Schiemann W.P. // J Mammary Gland Biol Neoplasia. 2010, V.15, №2, P.169-190
- Barcellos-Hoff M.H., Akhurst R.J. // Breast Cancer Res. 2009, V.11, №1, P.202
- Lebrun J.J. // ISRN Molecular Biology. doi: 10.5402/2012/381428 2012, V.2012
- Matise L.A., Palmer T.D., Ashby W.J., Nashabi A., Chytil A., Aakre M., Pickup M.W., Gorska A.E., Zijlstra A., Moses H.L. // Breast Cancer Res. 2012, V.14, №4, P.R98
- Wicki A., Christofori G. // Br J Cancer. 2007, V.96, №1, P.1-5
- Gaggioli C., Hooper S., Hidalgo-Carcedo C., Grosse R., Marshall J.F., Harrington K., Sahai E. // Nat Cell Biol. 2007, V.9, №12, P.1392-1400
- Friedl P., Wolf K. // Cancer Research 2008, V.68, №18, P.7247-7249
- Scott R.W., Hooper S., Crighton D., Li A., Konig I., Munro J., Trivier E., Wickman G., Morin P., Croft D.R. // J Cell Biol. 2010, V.191, №1, P.169-185
- Schoumacher M., Goldman R.D., Louvard D., Vignjevic D.M. // J Cell Biol. 2010, V.189, №3, P.541-556
- Friedl P. // Curr Opin Cell Biol. 2004, V.16, №1, P.14-23
- Madsen C.D., Sahai E. // Dev Cell. 2010, V.19, №1, P.13-26
- Sanz-Moreno V., Gadea G., Ahn J., Paterson H., Marra P., Pinner S., Sahai E., Marshall C.J. // Cell. 2008, V.135, №3, P.510-523
- Carragher N.O., Walker S.M., Scott Carragher L.A., Harris F., Sawyer T.K., Brunton V.G., Ozanne B.W., Frame M.C. // Oncogene. 2006, V.25, №42, P.5726-5740
- Yamazaki D., Kurisu S., Takenawa T. // Oncogene. 2009, V.28, №13, P.1570-1583
- Siletz A., Schnabel M., Kniazeva E., Schumacher A.J., Shin S., Jeruss J.S., Shea L.D. // PLoS One. 2013, V.8, №4, P.e57180
- Friedl P., Wolf K., Lammerding J. // Curr Opin Cell Biol. 2011, V.23, №1, P.55-64
- Chikina A.S., Aleksandrova A.Yu. // Molecular Biology. 2014, V.48, №2, P.165-180
- Ehrbar M., Sala A., Lienemann P., Ranga A., Mosiewicz K., Bittermann A., Rizzi S.C., Weber F.E., Lutolf M.P. // Biophys J. 2011, V.100, №2, P.284-293
- Abreu-Blanco M.T., Verboon J.M., Parkhurst S.M. // Curr Biol. 2014, V.24, №2, P.144-155
- Li H., Peyrollier K., Kilic G., Brakebusch C. // Biofactors. 2014, V.40, №2, P.226-235
- Lash L.L., Wallar B.J., Turner J.D., Vroegop S.M., Kilkuskie R.E., Kitchen-Goosen S.M., Xu H.E., Alberts A.S. // Cancer Research 2013, V.73, №22, P.6793-6803
- Militello R., Colombo M.I. // Commun Integr Biol. 2013, V.6, №5, P.e25460
- Bloomfield G., Skelton J., Ivens A., Tanaka Y., Kay R.R. // Science. 2010, V.330, №6010, P.1533-1536
- Sabeh F., Shimizu-Hirota R., Weiss S.J. // J Cell Biol. 2009, V.185, №1, P.11-19
- Gadea G., Sanz-Moreno V., Self A., Godi A., Marshall C.J. // Curr Biol. 2008, V.18, №19, P.1456-1465
- Chaussepied M., Janski N., Baumgartner M., Lizundia R., Jensen K., Weir W., Shiels B.R., Weitzman J.B., Glass E.J., Werling D. // PLoS Pathog. 2010, V.6, №11, P.e1001197
- Tozluoglu M., Tournier A.L., Jenkins R.P., Hooper S., Bates P.A., Sahai E. // Nat Cell Biol. 2013, V.15, №7, P.751-762
- Miyazawa Y., Uekita T., Ito Y., Seiki M., Yamaguchi H., Sakai R. // Mol Cancer Res. 2013, V.11, №6, P.628-637
- Razidlo G.L., Schroeder B., Chen J., Billadeau D.D., Mc-Niven M.A. // Curr Biol. 2014, V.24, №1, P.86-93
- Bakal C. // J Cell Biol. 2013, V.203, №3, P.378-379
- Synek L., Sekeres J., Zarsky V. // Front Plant Sci. 2014, V.4, P.543
- Pinner S.E., Sahai E. // F1000 Biol Rep. 2009, V.1, P.67
- Gerlitz G., Bustin M. // Trends Cell Biol. 2011, V.21, №1, P.6-11
- Condeelis J., Segall J.E. // Nat Rev Cancer. 2003, V.3, №12, P.921-930
- Ewald P.W., Swain Ewald H.A. // Evol Appl. 2013, V.6, №1, P.70-81
- Berton S., Belletti B., Wolf K., Canzonieri V., Lovat F., Vecchione A., Colombatti A., Friedl P., Baldassarre G. // Mol Cell Biol. 2009, V.29, №18, P.5031-5045
- Häger A., Alexander S., Friedl P. // European Journal of Cancer Supplements. 2013, V.11, №2, P.291-293
- Vasil’ev Yu.M., Gel’fand I.M. // Biochemistry (Mosc). 2006, V.71, №8, P.821-826
- Micalizzi D.S., Farabaugh S.M., Ford H.L. // J Mammary Gland Biol Neoplasia. 2010, V.15, №2, P.117-134
- Said N.A., Williams E.D. // Cells Tissues Organs. 2011, V.193, №1-2, P.85-97
- Kim S., Lee J.W. // Genomics Inform. 2014, V.12, №1, P.12-20
- Tsai J.H., Yang J. // Genes Dev. 2013, V.27, №20, P.2192-2206
- Gotte M., Kersting C., Radke I., Kiesel L., Wulfing P. // Breast Cancer Res. 2007, V.9, №1, P.R8
- Savagner P. // Ann Oncol. 2010, V.21, S7, P.vii89-vii92
- Lu M., Jolly M.K., Levine H., Onuchic J.N., Ben-Jacob E. // Proc Natl Acad Sci U S A. 2013, V.110, №45, P.18144-18149
- Tsai J.H., Donaher J.L., Murphy D.A., Chau S., Yang J. // Cancer Cell. 2012, V.22, №6, P.725-736
- Taddei M.L., Giannoni E., Morandi A., Ippolito L., Ramazzotti M., Callari M., Gandellini P., Chiarugi P. // Cell Commun Signal. 2014, V.12, P.24
- Giannoni E., Parri M., Chiarugi P. // Antioxid Redox Signal. 2012, V.16, №11, P.1248-1263
- Ocana O.H., Corcoles R., Fabra A., Moreno-Bueno G., Acloque H., Vega S., Barrallo-Gimeno A., Cano A., Nieto M.A. // Cancer Cell. 2012, V.22, №6, P.709-724
- Bindels S., Mestdagt M., Vandewalle C., Jacobs N., Volders L., Noel A., van Roy F., Berx G., Foidart J.M., Gilles C. // Oncogene. 2006, V.25, №36, P.4975-4985
- Vandewalle C., Van Roy F., Berx G. // Cell Mol Life Sci. 2009, V.66, №5, P.773-787
- Samatov T.R., Tonevitsky A.G., Schumacher U. // Mol Cancer. 2013, V.12, №1, P.107
- Sanchez-Tillo E., Liu Y., de Barrios O., Siles L., Fanlo L., Cuatrecasas M., Darling D.S., Dean D.C., Castells A., Postigo A. // Cell Mol Life Sci. 2012, V.69, №20, P.3429-3456
- De Craene B., Berx G. // Nat Rev Cancer. 2013, V.13, №2, P.97-110
- Friedl P., Wolf K. // Nat Rev Cancer. 2003, V.3, №5, P.362-374
- Tsuji T., Ibaragi S., Hu G.F. // Cancer Research 2009, V.69, №18, P.7135-7139
- Zavyalova M.V., Perelmuter V.M., Vtorushin S.V., Denisov E.V., Litvyakov N.V., Slonimskaya E.M., Cherdyntseva N.V. // Diagn Cytopathol. 2013, V.41, №3, P.279-282
- Gerashchenko T.S., Denisov E.V., Litviakov N.V., Zavyalova M.V., Vtorushin S.V., Tsyganov M.M., Perelmuter V.M., Cherdyntseva N.V. // Biochemistry (Mosc). 2013, V.78, №11, P.1201-1215
- Denisov E.V., Geraschenko T.S., Zavyalova M.V., Litviakov N.V., Tsyganov M.M., Kaigorodova E.V., Slonimskaya E.M., Kzhyshkowska J., Cherdyntseva N.V., Perelmuter V.M. // Neoplasma. 2015, P.doi: 10.4149/neo_2015_041
- Alexander S., Friedl P. // Trends Mol Med. 2012, V.18, №1, P.13-26
- Goswami S., Wang W., Wyckoff J.B., Condeelis J.S. // Cancer Research 2004, V.64, №21, P.7664-7667
- Mallini P., Lennard T., Kirby J., Meeson A. // Cancer Treat Rev. 2014, V.40, №3, P.341-348
- Chen W.J., Wang H., Tang Y., Liu C.L., Li H.L., Li W.T. // Chin J Cancer. 2010, V.29, №2, P.151-157
- Li Q.Q., Xu J.D., Wang W.J., Cao X.X., Chen Q., Tang F., Chen Z.Q., Liu X.P., Xu Z.D. // Clin Cancer Res. 2009, V.15, №8, P.2657-2665
- Zavyalova M.V., Litvyakov N.V., Garbukov E.Y., Vtorushin S.V., Stakheeva M.N., Savenkova O.V., Kritskaya N.G., Perelmuter V.M., Slonimskaya E.M., Cherdyntseva N.V. // Siberian Journal of Oncology. 2008, V.6, P.30-34
- Denisov E.V., Litviakov N.V., Zavyalova M.V., Perelmuter V.M., Vtorushin S.V., Tsyganov M.M., Gerashchenko T.S., Garbukov E.Y., Slonimskaya E.M., Cherdyntseva N.V. // Sci Rep. 2014. V. 4. № 2014, V.4, P.4709
- Watanabe S. // Cancer. 1954, V.7, №2, P.215-223
- Fidler I.J. // Eur J Cancer. 1973, V.9, №3, P.223-227
- Liotta L.A., Saidel M.G., Kleinerman J. // Cancer Research 1976, V.36, №3, P.889-894
- Yu M., Stott S., Toner M., Maheswaran S., Haber D.A. // J Cell Biol. 2011, V.192, №3, P.373-382
- Greene B.T., Hughes A.D., King M.R. // Front Oncol. 2012, V.2, P.69
- Kusters B., Kats G., Roodink I., Verrijp K., Wesseling P., Ruiter D.J., de Waal R.M., Leenders W.P. // Oncogene. 2007, V.26, №39, P.5808-5815
- Hou J.M., Krebs M.G., Lancashire L., Sloane R., Backen A., Swain R.K., Priest L.J., Greystoke A., Zhou C., Morris K. // J Clin Oncol. 2012, V.30, №5, P.525-532
- Tsuji T., Ibaragi S., Shima K., Hu M.G., Katsurano M., Sasaki A., Hu G.F. // Cancer Research 2008, V.68, №24, P.10377-10386
- Zavyalova M.V., Perelmuter V.M., Slonimskaya E.M., Vtorushin S.V., Garbukov E.Y., Glushenko S.A. // Siberian Journal of Oncology. 2006, V.1, P.32-35
- Zavyalova M.V., Denisov E.V., Tashireva L.A., Gerashchenko T.S., Litviakov N.V., Skryabin N.A., Vtorushin S.V., Telegina N.S., Slonimskaya E.M., Cherdyntseva N.V. // BioResearch Open Access. 2013, V.2, №2, P.148-154
- Perel’muter V.M., Zav’ialova M.V., Vtorushin S.V., Slonimskaia E.M., Kritskaia N.G., Garbukov E., Litviakov N.V., Stakheeva M.N., Babyshkina N.N., Malinovskaia E.A. // Adv Gerontol (Russian). 2008, V.21, №4, P.643-653