Cancer Invasion: Patterns and Mechanisms

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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.


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

  1. van Zijl F., Krupitza G., Mikulits W. // Mutat Res. 2011, V.728, №1-2, P.23-34
  2. Spano D., Heck C., De Antonellis P., Christofori G., Zollo M. // Semin Cancer Biol. 2012, V.22, №3, P.234-249
  3. Santibanez J.F. // ISRN Dermatol. 2013, V.2013, P.597927
  4. Mehlen P., Puisieux A. // Nat Rev Cancer. 2006, V.6, №6, P.449-458
  5. Nguyen D.X., Bos P.D., Massague J. // Nat Rev Cancer. 2009, V.9, №4, P.274-284
  6. Monteiro J., Fodde R. // Eur J Cancer. 2010, V.46, №7, P.1198-1203
  7. Kovalyov A.A. // Zdorovie Ukrainy. 2011, V.4, №17, P.26-28
  8. Kovalyov A.A., Grudinskaya T.A., Kusnezowa T.P., Kovalyov K.A. // Oncology. 2012, V.14, №2, P.126-129
  9. Hay E.D. // Acta Anat (Basel). 1995, V.154, №1, P.8-20
  10. Kalluri R., Weinberg R.A. // J Clin Invest. 2009, V.119, №6, P.1420-1428
  11. Tam W.L., Weinberg R.A. // Nat Med. 2013, V.19, №11, P.1438-1449
  12. Cox E.A., Sastry S.K., Huttenlocher A. // Mol Biol Cell. 2001, V.12, №2, P.265-277
  13. Friedl P., Hegerfeldt Y., Tusch M. // Int J Dev Biol. 2004, V.48, №5-6, P.441-449
  14. Friedl P., Alexander S. // Cell. 2011, V.147, №5, P.992-1009
  15. Friedl P., Locker J., Sahai E., Segall J.E. // Nat Cell Biol. 2012, V.14, №8, P.777-783
  16. Hernandez-Caballero M.E. // Molecular mechanisms of metastasis: epithelial-mesenchymal transition, anoikis and loss of adhesion. In Carcinogenesis, Tonissen K 2013, P.165-194
  17. Friedl P., Gilmour D. // Nat Rev Mol Cell Biol. 2009, V.10, №7, P.445-457
  18. Ulrich F., Heisenberg C.P. // Traffic. 2009, V.10, №7, P.811-818
  19. Khalil A.A., Friedl P. // Integr Biol (Camb). 2010, V.2, №11-12, P.568-574
  20. Yilmaz M., Christofori G. // Mol Cancer Res. 2010, V.8, №5, P.629-642
  21. Friedl P., Wolf K. // J Cell Biol. 2010, V.188, №1, P.11-19
  22. Pankova K., Rosel D., Novotny M., Brabek J. // Cell Mol Life Sci. 2010, V.67, №1, P.63-71
  23. Scott R.W., Crighton D., Olson M.F. // J Vis Exp. 2011, №58
  24. Cheung K.J., Gabrielson E., Werb Z., Ewald A.J. // Cell. 2013, V.155, №7, P.1639-1651
  25. 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
  26. Giampieri S., Manning C., Hooper S., Jones L., Hill C.S., Sahai E. // Nat Cell Biol. 2009, V.11, №11, P.1287-1296
  27. Sanz-Moreno V., Marshall C.J. // Curr Opin Cell Biol. 2010, V.22, №5, P.690-696
  28. Lecaudey V., Cakan-Akdogan G., Norton W.H., Gilmour D. // Development. 2008, V.135, №16, P.2695-2705
  29. Aman A., Piotrowski T. // Dev Cell. 2008, V.15, №5, P.749-761
  30. Vitorino P., Meyer T. // Genes Dev. 2008, V.22, №23, P.3268-3281
  31. Taylor M.A., Parvani J.G., Schiemann W.P. // J Mammary Gland Biol Neoplasia. 2010, V.15, №2, P.169-190
  32. Barcellos-Hoff M.H., Akhurst R.J. // Breast Cancer Res. 2009, V.11, №1, P.202
  33. Lebrun J.J. // ISRN Molecular Biology. doi: 10.5402/2012/381428 2012, V.2012
  34. 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
  35. Wicki A., Christofori G. // Br J Cancer. 2007, V.96, №1, P.1-5
  36. 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
  37. Friedl P., Wolf K. // Cancer Research 2008, V.68, №18, P.7247-7249
  38. 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
  39. Schoumacher M., Goldman R.D., Louvard D., Vignjevic D.M. // J Cell Biol. 2010, V.189, №3, P.541-556
  40. Friedl P. // Curr Opin Cell Biol. 2004, V.16, №1, P.14-23
  41. Madsen C.D., Sahai E. // Dev Cell. 2010, V.19, №1, P.13-26
  42. 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
  43. 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
  44. Yamazaki D., Kurisu S., Takenawa T. // Oncogene. 2009, V.28, №13, P.1570-1583
  45. 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
  46. Friedl P., Wolf K., Lammerding J. // Curr Opin Cell Biol. 2011, V.23, №1, P.55-64
  47. Chikina A.S., Aleksandrova A.Yu. // Molecular Biology. 2014, V.48, №2, P.165-180
  48. 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
  49. Abreu-Blanco M.T., Verboon J.M., Parkhurst S.M. // Curr Biol. 2014, V.24, №2, P.144-155
  50. Li H., Peyrollier K., Kilic G., Brakebusch C. // Biofactors. 2014, V.40, №2, P.226-235
  51. 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
  52. Militello R., Colombo M.I. // Commun Integr Biol. 2013, V.6, №5, P.e25460
  53. Bloomfield G., Skelton J., Ivens A., Tanaka Y., Kay R.R. // Science. 2010, V.330, №6010, P.1533-1536
  54. Sabeh F., Shimizu-Hirota R., Weiss S.J. // J Cell Biol. 2009, V.185, №1, P.11-19
  55. Gadea G., Sanz-Moreno V., Self A., Godi A., Marshall C.J. // Curr Biol. 2008, V.18, №19, P.1456-1465
  56. 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
  57. 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
  58. Miyazawa Y., Uekita T., Ito Y., Seiki M., Yamaguchi H., Sakai R. // Mol Cancer Res. 2013, V.11, №6, P.628-637
  59. Razidlo G.L., Schroeder B., Chen J., Billadeau D.D., Mc-Niven M.A. // Curr Biol. 2014, V.24, №1, P.86-93
  60. Bakal C. // J Cell Biol. 2013, V.203, №3, P.378-379
  61. Synek L., Sekeres J., Zarsky V. // Front Plant Sci. 2014, V.4, P.543
  62. Pinner S.E., Sahai E. // F1000 Biol Rep. 2009, V.1, P.67
  63. Gerlitz G., Bustin M. // Trends Cell Biol. 2011, V.21, №1, P.6-11
  64. Condeelis J., Segall J.E. // Nat Rev Cancer. 2003, V.3, №12, P.921-930
  65. Ewald P.W., Swain Ewald H.A. // Evol Appl. 2013, V.6, №1, P.70-81
  66. 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
  67. Häger A., Alexander S., Friedl P. // European Journal of Cancer Supplements. 2013, V.11, №2, P.291-293
  68. Vasil’ev Yu.M., Gel’fand I.M. // Biochemistry (Mosc). 2006, V.71, №8, P.821-826
  69. Micalizzi D.S., Farabaugh S.M., Ford H.L. // J Mammary Gland Biol Neoplasia. 2010, V.15, №2, P.117-134
  70. Said N.A., Williams E.D. // Cells Tissues Organs. 2011, V.193, №1-2, P.85-97
  71. Kim S., Lee J.W. // Genomics Inform. 2014, V.12, №1, P.12-20
  72. Tsai J.H., Yang J. // Genes Dev. 2013, V.27, №20, P.2192-2206
  73. Gotte M., Kersting C., Radke I., Kiesel L., Wulfing P. // Breast Cancer Res. 2007, V.9, №1, P.R8
  74. Savagner P. // Ann Oncol. 2010, V.21, S7, P.vii89-vii92
  75. 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
  76. Tsai J.H., Donaher J.L., Murphy D.A., Chau S., Yang J. // Cancer Cell. 2012, V.22, №6, P.725-736
  77. 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
  78. Giannoni E., Parri M., Chiarugi P. // Antioxid Redox Signal. 2012, V.16, №11, P.1248-1263
  79. 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
  80. 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
  81. Vandewalle C., Van Roy F., Berx G. // Cell Mol Life Sci. 2009, V.66, №5, P.773-787
  82. Samatov T.R., Tonevitsky A.G., Schumacher U. // Mol Cancer. 2013, V.12, №1, P.107
  83. 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
  84. De Craene B., Berx G. // Nat Rev Cancer. 2013, V.13, №2, P.97-110
  85. Friedl P., Wolf K. // Nat Rev Cancer. 2003, V.3, №5, P.362-374
  86. Tsuji T., Ibaragi S., Hu G.F. // Cancer Research 2009, V.69, №18, P.7135-7139
  87. 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
  88. 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
  89. 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
  90. Alexander S., Friedl P. // Trends Mol Med. 2012, V.18, №1, P.13-26
  91. Goswami S., Wang W., Wyckoff J.B., Condeelis J.S. // Cancer Research 2004, V.64, №21, P.7664-7667
  92. Mallini P., Lennard T., Kirby J., Meeson A. // Cancer Treat Rev. 2014, V.40, №3, P.341-348
  93. 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
  94. 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
  95. 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
  96. 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
  97. Watanabe S. // Cancer. 1954, V.7, №2, P.215-223
  98. Fidler I.J. // Eur J Cancer. 1973, V.9, №3, P.223-227
  99. Liotta L.A., Saidel M.G., Kleinerman J. // Cancer Research 1976, V.36, №3, P.889-894
  100. Yu M., Stott S., Toner M., Maheswaran S., Haber D.A. // J Cell Biol. 2011, V.192, №3, P.373-382
  101. Greene B.T., Hughes A.D., King M.R. // Front Oncol. 2012, V.2, P.69
  102. 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
  103. 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
  104. 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
  105. 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
  106. 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
  107. 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

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