Skip to main content
SpringerLink
Log in

Carcinogenesis: Evolution of concepts

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Cancer is considered as an unintended consequence of internal imperfection of multicellular organisms: Darwinian evolution “does not foresee the future and does not plan for it”, it is forced to handle only anything that it has at a given moment “at hand”, which makes inevitable compromises and restrictions. In this case, there are a number of founding dogmas including mutagenesis as the main driving force of carcinogenesis; the environment as the main source of mutagenic effects; tumor monoclonality; cancer cell multistage transformation as Darwinian process of successive mutation—selection cycles. Recent discoveries complicate, supplement, and sometimes transform into an opposite fixed concepts. As a result, a new “image” of carcinogenesis is formed as a biological phenomenon whose conservation is indicative of its evolutionary utility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CSC:

cancer stem cells

ROS:

reactive oxygen species

References

  1. Hoeijmakers, J. H. (2001) Nature, 411, 366–374.

    Article  PubMed  CAS  Google Scholar 

  2. Klein, D., Imrekh, S., and Zabarovskii, E. (2008) Biokhimiya, 73, 597–604.

    Google Scholar 

  3. Belitskii, G. A., and Yakubovskaya, M. G. (2008) Biochemistry (Moscow), 73, 543–554.

    Article  CAS  Google Scholar 

  4. Zaridze, D. G. (2008) Biochemistry (Moscow), 73, 532–542.

    Article  CAS  Google Scholar 

  5. Gurtsevich, B. E. (2008) Biochemistry (Moscow), 73, 504–513.

    Article  CAS  Google Scholar 

  6. Thilly, W. G. (2003) Nat. Genet., 34, 255–259.

    Article  PubMed  CAS  Google Scholar 

  7. Bergsmedh, A., Szeles, A., Henriksson, M., Bratt, A., Folkman, M. J., Spetz, A. L., and Holmgren, L. (2001) Proc. Natl. Acad. Sci. USA, 98, 6407–6411.

    Article  PubMed  CAS  Google Scholar 

  8. Dingli, D., and Nowak, M. A. (2006) Nature, 443, 35–36.

    Article  PubMed  CAS  Google Scholar 

  9. Duelli, D., and Lazebnik, Y. (2003) Cancer Cell, 3, 445–448.

    Article  PubMed  CAS  Google Scholar 

  10. Frumkin, D., Wasserstrom, A., Itzkovitz, S., Stern, T., Harmelin, A., Eilam, R., Rechavi, G., and Shapiro, E. (2008) Cancer Res., 68, 5924–5931.

    Article  PubMed  CAS  Google Scholar 

  11. Lichtenstein, A. V. (2006) Cancer Biol Ther., 5, 1263–1264.

    PubMed  Google Scholar 

  12. Tomlinson, I. P., Novelli, M. R., and Bodmer, W. F. (1996) Proc. Natl. Acad. Sci. USA, 93, 14800–14803.

    Article  PubMed  CAS  Google Scholar 

  13. Wood, L. D., Parsons, D. W., Jones, S., Lin, J., Sjoblom, T., Leary, R. J., Shen, D., Boca, S. M., Barber, T., Ptak, J., Silliman, N., Szabo, S., Dezso, Z., Ustyanksky, V., Nikolskaya, T., Nikolsky, Y., Karchin, R., Wilson, P. A., Kaminker, J. S., Zhang, Z., Croshaw, R., Willis, J., Dawson, D., Shipitsin, M., Willson, J. K. V., Sukumar, S., Polyak, K., Park, B. H., Pethiyagoda, C. L., Pant, P. V. K., Ballinger, D. G., Sparks, A. B., Hartigan, J., Smith, D. R., Suh, E., Papadopoulos, N., Buckhaults, P., Markowitz, S. D., Parmigiani, G., Kinzler, K. W., Velculescu, V. E., and Vogelstein, B. (2007) Science, 318, 1108–1113.

    Article  PubMed  CAS  Google Scholar 

  14. Lotem, J., and Sachs, L. (2002) Semin. Cancer Biol., 12, 339–346.

    Article  PubMed  CAS  Google Scholar 

  15. Baylin, S. B., and Ohm, J. E. (2006) Nat. Rev. Cancer, 6, 107–116.

    Article  PubMed  CAS  Google Scholar 

  16. Feinberg, A. P. (2007) Nature, 447, 433–440.

    Article  PubMed  CAS  Google Scholar 

  17. Hendrix, M. J., Seftor, E. A., Seftor, R. E., Kasemeier-Kulesa, J., Kulesa, P. M., and Postovit, L. M. (2007) Nat. Rev. Cancer, 7, 246–255.

    Article  PubMed  CAS  Google Scholar 

  18. Ryazansky, S. S., and Gvozdev, V. A. (2008) Biochemistry (Moscow), 73, 514–527.

    Article  CAS  Google Scholar 

  19. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., Jaenisch, R., Wagschal, A., Feil, R., Schreiber, S. L., and Lander, E. S. (2006) Cell, 125, 315–326.

    Article  PubMed  CAS  Google Scholar 

  20. Chang, T. C., Wentzel, E. A., Kent, O. A., Ramachandran, K., Mullendore, M., Lee, K. H., Feldmann, G., Yamakuchi, M., Ferlito, M., Lowenstein, C. J., Arking, D. E., Beer, M. A., Maitra, A., and Mendell, J. T. (2007) Mol. Cell, 26, 745–752.

    Article  PubMed  CAS  Google Scholar 

  21. He, L., He, X., Lim, L. P., de Stanchina, E., Xuan, Z., Liang, Y., Xue, W., Zender, L., Magnus, J., Ridzon, D., Jackson, A. L., Linsley, P. S., Chen, C., Lowe, S. W., Cleary, M. A., and Hannon, G. J. (2007) Nature, 447, 1130–1134.

    Article  PubMed  CAS  Google Scholar 

  22. Jones, P. A., and Baylin, S. B. (2007) Cell, 128, 683–692.

    Article  PubMed  CAS  Google Scholar 

  23. Mayr, C., Hemann, M. T., and Bartel, D. P. (2007) Science, 315, 1576–1579.

    Article  PubMed  CAS  Google Scholar 

  24. He, X., He, L., and Hannon, G. J. (2007) Cancer Res., 67, 11099–11101.

    Article  PubMed  CAS  Google Scholar 

  25. Klose, R. J., and Bird, A. P. (2006) Trends Biochem. Sci., 31, 89–97.

    Article  PubMed  CAS  Google Scholar 

  26. Bird, A. (2007) Nature, 447, 396–398.

    Article  PubMed  CAS  Google Scholar 

  27. Fraga, M. F., Ballestar, E., Villar-Garea, A., Boix-Chornet, M., Espada, J., Schotta, G., Bonaldi, T., Haydon, C., Ropero, S., Petrie, K., Iyer, N. G., Perez-Rosado, A., Calvo, E., Lopez, J. A., Cano, A., Calasanz, M. J., Colomer, D., Piris, M. A., Ahn, N., Imhof, A., Caldas, C., Jenuwein, T., and Esteller, M. (2005) Nat. Genet., 37, 391–400.

    Article  PubMed  CAS  Google Scholar 

  28. Sempere, L. F., Christensen, M., Silahtaroglu, A., Bak, M., Heath, C. V., Schwartz, G., Wells, W., Kauppinen, S., and Cole, C. N. (2007) Cancer Res., 67, 11612–11620.

    Article  PubMed  CAS  Google Scholar 

  29. Jacinto, F. V., Ballestar, E., Ropero, S., and Esteller, M. (2007) Cancer Res., 67, 11481–11486.

    Article  PubMed  CAS  Google Scholar 

  30. Feinberg, A. P., Ohlsson, R., and Henikoff, S. (2006) Nat. Rev. Genet., 7, 21–33.

    Article  PubMed  CAS  Google Scholar 

  31. Keshet, I., Schlesinger, Y., Farkash, S., Rand, E., Hecht, M., Segal, E., Pikarski, E., Young, R. A., Niveleau, A., Cedar, H., and Simon, I. (2006) Nat. Genet., 38, 149–153.

    Article  PubMed  CAS  Google Scholar 

  32. Widschwendter, M., Fiegl, H., Egle, D., Mueller-Holzner, E., Spizzo, G., Marth, C., Weisenberger, D. J., Campan, M., Young, J., Jacobs, I., and Laird, P. W. (2007) Nat. Genet., 39, 157–158.

    Article  PubMed  CAS  Google Scholar 

  33. Gazin, C., Wajapeyee, N., Gobeil, S., Virbasius, C. M., and Green, M. R. (2007) Nature, 449, 1073–1077.

    Article  PubMed  CAS  Google Scholar 

  34. Schlesinger, Y., Straussman, R., Keshet, I., Farkash, S., Hecht, M., Zimmerman, J., Eden, E., Yakhini, Z., Ben Shushan, E., Reubinoff, B. E., Bergman, Y., Simon, I., and Cedar, H. (2007) Nat. Genet., 39, 232–236.

    Article  PubMed  CAS  Google Scholar 

  35. Reya, T., Morrison, S. J., Clarke, M. F., and Weissman, I. L. (2001) Nature, 414, 105–111.

    Article  PubMed  CAS  Google Scholar 

  36. Balkwill, F., and Mantovani, A. (2001) Lancet, 357, 539–545.

    Article  PubMed  CAS  Google Scholar 

  37. Coussens, L. M., and Werb, Z. (2002) Nature, 420, 860–867.

    Article  PubMed  CAS  Google Scholar 

  38. Adams, J. M., Kelly, P. N., Dakic, A., Nutt, S. L., and Strasser, A. (2007) Science, 318, 1722d.

    Article  CAS  Google Scholar 

  39. Kelly, P. N., Dakic, A., Adams, J. M., Nutt, S. L., and Strasser, A. (2007) Science, 317, 337.

    Article  PubMed  CAS  Google Scholar 

  40. Kennedy, J. A., Barabe, F., Poeppl, A. G., Wang, J. C. Y., and Dick, J. E. (2007) Science, 318, 1722c.

    Article  CAS  Google Scholar 

  41. Hermann, P. C., Huber, S. L., and Heeschen, C. (2008) Cell Cycle, 7, 188–193.

    PubMed  CAS  Google Scholar 

  42. Hermann, P. C., Huber, S. L., Herrler, T., Aicher, A., Ellwart, J. W., Guba, M., Bruns, C. J., and Heeschen, C. (2007) Cell Stem Cell, 1, 313–323.

    Article  PubMed  CAS  Google Scholar 

  43. Abelev, G. I., and Eriser, T. L. (2008) Biochemistry (Moscow), 73, 487–497.

    Article  CAS  Google Scholar 

  44. Bissell, M. J., and Radisky, D. (2001) Nat. Rev. Cancer, 1, 46–54.

    Article  PubMed  CAS  Google Scholar 

  45. Perez-Losada, J., and Balmain, A. (2003) Nat. Rev. Cancer, 3, 434–443.

    Article  PubMed  CAS  Google Scholar 

  46. Axelrod, R., Axelrod, D. E., and Pienta, K. J. (2006) Proc. Natl. Acad. Sci. USA, 103, 13474–13479.

    Article  PubMed  CAS  Google Scholar 

  47. Albini, A., and Sporn, M. B. (2007) Nat. Rev. Cancer, 7, 139–147.

    Article  PubMed  CAS  Google Scholar 

  48. Merlo, L. M. F., Pepper, J. W., Reid, B. J., and Maley, C. C. (2006) Nat. Rev. Cancer, 6, 924–935.

    Article  PubMed  CAS  Google Scholar 

  49. Lichtenstein, A. V. (2005) Biochemistry (Moscow), 70, 1055–1064.

    Article  CAS  Google Scholar 

  50. Bjerkvig, R., Tysnes, B. B., Aboody, K. S., Najbauer, J., and Terzis, A. J. (2005) Nat. Rev. Cancer, 5, 899–904.

    Article  PubMed  CAS  Google Scholar 

  51. Clarke, M. F., and Fuller, M. (2006) Cell, 124, 1111–1115.

    Article  PubMed  CAS  Google Scholar 

  52. Lichtenstein, A. V. (2008) Med. Hypotheses, 71, 839–850.

    Article  PubMed  Google Scholar 

  53. Postovit, L. M., Costa, F. F., Bischof, J. M., Seftor, E. A., Wen, B., Seftor, R. E., Feinberg, A. P., Soares, M. B., and Hendrix, M. J. (2007) J. Cell Biochem., 101, 908–917.

    Article  PubMed  CAS  Google Scholar 

  54. Sparmann, A., and van Lohuizen, M. (2006) Nat. Rev. Cancer, 6, 846–856.

    Article  PubMed  CAS  Google Scholar 

  55. Wong, D. J., Liu, H., Ridky, T. W., Cassarino, D., Segal, E., and Chang, H. Y. (2008) Cell Stem Cell, 2, 333–344.

    Article  PubMed  CAS  Google Scholar 

  56. Naxerova, K., Bult, C. J., Peaston, A., Fancher, K., Knowles, B. B., Kasif, S., and Kohane, I. S. (2008) Genome Biol., 9, R108.

    Article  PubMed  CAS  Google Scholar 

  57. Chen, L., Shen, R., Ye, Y., Pu, X. A., Liu, X., Duan, W., Wen, J., Zimmerer, J., Wang, Y., Liu, Y., Lasky, L. C., Heerema, N. A., Perrotti, D., Ozato, K., Kuramochi-Miyagawa, S., Nakano, T., Yates, A. J., Carson III, W. E., Lin, H., Barsky, S. H., and Gao, J. X. (2007) PLoS ONE, 2, e293.

    Article  PubMed  CAS  Google Scholar 

  58. Li, L., and Neaves, W. B. (2006) Cancer Res., 66, 4553–4557.

    Article  PubMed  CAS  Google Scholar 

  59. Walkley, C. R., Shea, J. M., Sims, N. A., Purton, L. E., and Orkin, S. H. (2007) Cell, 129, 1081–1095.

    Article  PubMed  CAS  Google Scholar 

  60. Wu, M., Kwon, H. Y., Rattis, F., Blum, J., Zhao, C., Ashkenazi, R., Jackson, T. L., Gaiano, N., Oliver, T., and Reya, T. (2007) Cell Stem Cell, 1, 541–554.

    Article  PubMed  CAS  Google Scholar 

  61. Mintz, B., and Illmensee, K. (1975) Proc. Natl. Acad. Sci. USA, 72, 3585–3589.

    Article  PubMed  CAS  Google Scholar 

  62. Christiansen, J. J., and Rajasekaran, A. K. (2006) Cancer Res., 66, 8319–8326.

    Article  PubMed  CAS  Google Scholar 

  63. Christofk, H. R., Vander Heiden, M. G., Harris, M. H., Ramanathan, A., Gerszten, R. E., Wei, R., Fleming, M. D., Schreiber, S. L., and Cantley, L. C. (2008) Nature, 452, 230–233.

    Article  PubMed  CAS  Google Scholar 

  64. Bergers, G., and Benjamin, L. E. (2003) Nat. Rev. Cancer, 3, 401–410.

    Article  PubMed  CAS  Google Scholar 

  65. Kim, R., Emi, M., Tanabe, K., and Arihiro, K. (2006) Cancer Res., 66, 5527–5536.

    Article  PubMed  CAS  Google Scholar 

  66. Simpson, A. J., Caballero, O. L., Jungbluth, A., Chen, Y. T., and Old, L. J. (2005) Nat. Rev. Cancer, 5, 615–625.

    Article  PubMed  CAS  Google Scholar 

  67. Old, L. J. (2001) Cancer Immun., 1, 1–7.

    PubMed  CAS  Google Scholar 

  68. Vijg, J. (2000) Mutat. Res., 447, 117–135.

    PubMed  CAS  Google Scholar 

  69. Shabad, L. M. (1967) in Precancer in the Experimental-Morphological Aspect [in Russian], Meditsina, Moscow, pp. 352–373.

    Google Scholar 

  70. Braakhuis, B. J. M., Tabor, M. P., Kummer, J. A., Leemans, C. R., and Brakenhoff, R. H. (2003) Cancer Res., 63, 1727–1730.

    PubMed  CAS  Google Scholar 

  71. Holmgren, L., Szeles, A., Rajnavolgyi, E., Folkman, J., Klein, G., Ernberg, I., and Falk, K. I. (1999) Blood, 93, 3956–3963.

    PubMed  CAS  Google Scholar 

  72. Rizvi, A. Z., Swain, J. R., Davies, P. S., Bailey, A. S., Decker, A. D., Willenbring, H., Grompe, M., Fleming, W. H., and Wong, M. H. (2006) Proc. Natl. Acad. Sci. USA, 103, 6321–6325.

    Article  PubMed  CAS  Google Scholar 

  73. Duelli, D. M., Padilla-Nash, H. M., Berman, D., Murphy, K. M., Ried, T., and Lazebnik, Y. (2007) Curr. Biol., 17, 431–437.

    Article  PubMed  CAS  Google Scholar 

  74. Pawelek, J. M., and Chakraborty, A. K. (2008) Nat. Rev. Cancer, 8, 377–386.

    Article  PubMed  CAS  Google Scholar 

  75. Balkwill, F. (2004) Nat. Rev. Cancer, 4, 540–550.

    Article  PubMed  CAS  Google Scholar 

  76. Dranoff, G. (2004) Nat. Rev. Cancer, 4, 11–22.

    Article  PubMed  CAS  Google Scholar 

  77. Dolloff, N. G., Russell, M. R., Loizos, N., and Fatatis, A. (2007) Cancer Res., 67, 555–562.

    Article  PubMed  CAS  Google Scholar 

  78. Hayward, S. W., Wang, Y., Cao, M., Hom, Y. K., Zhang, B., Grossfeld, G. D., Sudilovsky, D., and Cunha, G. R. (2001) Cancer Res., 61, 8135–8142.

    PubMed  CAS  Google Scholar 

  79. Hiratsuka, S., Watanabe, A., Aburatani, H., and Maru, Y. (2006) Nat. Cell Biol., 8, 1369–1375.

    Article  PubMed  CAS  Google Scholar 

  80. Kaplan, R. N., Riba, R. D., Zacharoulis, S., Bramley, A.H., Vincent, L., Costa, C., MacDonald, D. D., Jin, D. K., Shido, K., Kerns, S. A., Zhu, Z., Hicklin, D., Wu, Y., Port, J. L., Altorki, N., Port, E. R., Ruggero, D., Shmelkov, S. V., Jensen, K. K., Rafii, S., and Lyden, D. (2005) Nature, 438, 820–827.

    Article  PubMed  CAS  Google Scholar 

  81. Karnoub, A. E., Dash, A. B., Vo, A. P., Sullivan, A., Brooks, M. W., Bell, G. W., Richardson, A. L., Polyak, K., Tubo, R., and Weinberg, R. A. (2007) Nature, 449, 557–563.

    Article  PubMed  CAS  Google Scholar 

  82. Nolan, D. J., Ciarrocchi, A., Mellick, A. S., Jaggi, J. S., Bambino, K., Gupta, S., Heikamp, E., McDevitt, M. R., Scheinberg, D. A., Benezra, R., and Mittal, V. (2007) Genes Dev., 21, 1546–1558.

    Article  PubMed  CAS  Google Scholar 

  83. Sawyers, C. L. (2007) Nat. Med., 13, 1144–1145.

    Article  PubMed  CAS  Google Scholar 

  84. Williams, R. T., den Besten, W., and Sherr, C. J. (2007) Genes Dev., 21, 2283–2287.

    Article  PubMed  CAS  Google Scholar 

  85. Wyckoff, J. B., Wang, Y., Lin, E. Y., Li, J. F., Goswami, S., Stanley, E. R., Segall, J. E., Pollard, J. W., and Condeelis, J. (2007) Cancer Res., 67, 2649–2656.

    Article  PubMed  CAS  Google Scholar 

  86. Elenbaas, B., and Weinberg, R. A. (2001) Exp. Cell Res., 264, 169–184.

    Article  PubMed  CAS  Google Scholar 

  87. Orimo, A., Gupta, P. B., Sgroi, D. C., Arenzana-Seisdedos, F., Delaunay, T., Naeem, R., Carey, V. J., Richardson, A. L., and Weinberg, R. A. (2005) Cell, 121, 335–348.

    Article  PubMed  CAS  Google Scholar 

  88. Kalluri, R., and Zeisberg, M. (2006) Nat. Rev. Cancer, 6, 392–401.

    Article  PubMed  CAS  Google Scholar 

  89. Pollard, J. W. (2004) Nat. Rev. Cancer, 4, 71–78.

    Article  PubMed  CAS  Google Scholar 

  90. Condeelis, J., and Pollard, J. W. (2006) Cell, 124, 263–266.

    Article  PubMed  CAS  Google Scholar 

  91. Sahai, E. (2007) Nat. Rev. Cancer, 7, 737–749.

    Article  PubMed  CAS  Google Scholar 

  92. Ardi, V. C., Kupriyanova, T. A., Deryugina, E. I., and Quigley, J. P. (2007) Proc. Natl. Acad. Sci. USA, 104, 20262–20267.

    Article  PubMed  CAS  Google Scholar 

  93. Balkwill, F., and Mantovani, A. (2001) Lancet, 357, 539–545.

    Article  PubMed  CAS  Google Scholar 

  94. Gupta, G. P., and Massague, J. (2006) Cell, 127, 679–695.

    Article  PubMed  CAS  Google Scholar 

  95. Shojaei, F., Wu, X., Zhong, C., Yu, L., Liang, X. H., Yao, J., Blanchard, D., Bais, C., Peale, F. V., van Bruggen, N., Ho, C., Ross, J., Tan, M., Carano, R. A. D., Meng, Y. G., and Ferrara, N. (2007) Nature, 450, 825–831.

    Article  PubMed  CAS  Google Scholar 

  96. Gaggioli, C., Hooper, S., Hidalgo-Carcedo, C., Grosse, R., Marshall, J. F., Harrington, K., and Sahai, E. (2007) Nat. Cell Biol., 9, 1392–1400.

    Article  PubMed  CAS  Google Scholar 

  97. Kaplan, R. N., Rafii, S., and Lyden, D. (2006) Cancer Res., 66, 11089–11093.

    Article  PubMed  CAS  Google Scholar 

  98. Qian, C. N., Berghuis, B., Tsarfaty, G., Bruch, M., Kort, E. J., Ditlev, J., Tsarfaty, I., Hudson, E., Jackson, D. G., Petillo, D., Chen, J., Resau, J. H., and Teh, B. T. (2006) Cancer Res., 66, 10365–10376.

    Article  PubMed  CAS  Google Scholar 

  99. Witz, I. P. (2008) Cancer Res., 68, 9–13.

    Article  PubMed  CAS  Google Scholar 

  100. Koebel, C. M., Vermi, W., Swann, J. B., Zerafa, N., Rodig, S. J., Old, L. J., Smyth, M. J., and Schreiber, R. D. (2007) Nature, 450, 903–907.

    Article  PubMed  CAS  Google Scholar 

  101. Prehn, R. T. (1994) Cancer Res., 54, 908–914.

    PubMed  CAS  Google Scholar 

  102. De Visser, K. E., Eichten, A., and Coussens, L. M. (2006) Nat. Rev. Cancer, 6, 24–37.

    Article  PubMed  CAS  Google Scholar 

  103. Hill, R., Song, Y., Cardiff, R. D., and van Dyke, T. (2005) Cell, 123, 1001–1011.

    Article  PubMed  CAS  Google Scholar 

  104. Gallagher, P. G., Bao, Y., Prorock, A., Zigrino, P., Nischt, R., Politi, V., Mauch, C., Dragulev, B., and Fox, J. W. (2005) Cancer Res., 65, 4134–4146.

    Article  PubMed  CAS  Google Scholar 

  105. Lichtenstein, A. V. (2005) Cancer Cell Int., 5, 5 (http://www.cancerci.com/content/5/1/5).

    Article  PubMed  CAS  Google Scholar 

  106. Hanahan, D., and Weinberg, R. A. (2000) Cell, 100, 57–70.

    Article  PubMed  CAS  Google Scholar 

  107. Tisdale, M. J. (2002) Nat. Rev. Cancer, 2, 862–871.

    Article  PubMed  CAS  Google Scholar 

  108. Finora, K. (2003) Clin. Tech. Small Anim. Pract., 18, 123–126.

    Article  PubMed  Google Scholar 

  109. Posner, J. B. (2003) Ann. N. Y. Acad. Sci., 998, 178–186.

    Article  PubMed  CAS  Google Scholar 

  110. Sato, K., Onuma, E., Yocum, R. C., and Ogata, E. (2003) Semin. Oncol., 30, 167–173.

    Article  PubMed  CAS  Google Scholar 

  111. Yamada, G., Ohguro, H., Aketa, K., Itoh, T., Shijubo, N., Takahashi, H., Fujiwara, O., Satoh, M., Ohtsuka, K., and Abe, S. (2003) Hum. Pathol., 34, 717–719.

    Article  PubMed  Google Scholar 

  112. Kim, Y. T., Rha, S. Y., Shim, C. Y., Sohn, J. H., Kim, C., Yu, N. C., Chung, H. C., Kim, J. H., Han, D. S., Kim, B. S., and Roh, J. K. (2003) Yonsei Med. J., 44, 539–543.

    PubMed  Google Scholar 

  113. Spivak, J. L. (2005) Nat. Rev. Cancer, 5, 543–555.

    Article  PubMed  CAS  Google Scholar 

  114. Rak, J., Yu, J. L., Luyendyk, J., and Mackman, N. (2006) Cancer Res., 66, 10643–10646.

    Article  PubMed  CAS  Google Scholar 

  115. Kritchevsky, S. B., Wilcosky, T. C., Morris, D. L., Truong, K. N., and Tyroler, H. A. (1991) Cancer Res., 51, 3198–3203.

    PubMed  CAS  Google Scholar 

  116. Grosvenor, M., Bulcavage, L., and Chlebowski, R. T. (1989) Cancer, 63, 330–334.

    Article  PubMed  CAS  Google Scholar 

  117. Johnen, H., Lin, S., Kuffner, T., Brown, D. A., Tsai, V. W.-W., Bauskin, A. R., Wu, L., Pankhurst, G., Jiang, L., Junankar, S., Hunter, M., Fairlie, W. D., Lee, N. J., Enriquez, R. F., Baldock, P. A., Corey, E., Apple, F. S., Murakami, M. M., Lin, E. J., Wang, C., During, M. J., Sainsbury, A., Herzog, H., and Breit, S. N. (2007) Nat. Med., 13, 1333–1340.

    Article  PubMed  CAS  Google Scholar 

  118. Khare, A., and Shaulsky, G. (2006) Nat. Rev. Genet., 7, 577–584.

    Article  PubMed  CAS  Google Scholar 

  119. Li, W., and Baker, N. E. (2007) Cell, 129, 1215–1225.

    Article  PubMed  CAS  Google Scholar 

  120. Moreno, E. (2008) Nat. Rev. Cancer, 8, 141–147.

    Article  PubMed  CAS  Google Scholar 

  121. Lugini, L., Matarrese, P., Tinari, A., Lozupone, F., Federici, C., Iessi, E., Gentile, M., Luciani, F., Parmiani, G., Rivoltini, L., Malorni, W., and Fais, S. (2006) Cancer Res., 66, 3629–3638.

    Article  PubMed  CAS  Google Scholar 

  122. Greaves, M. (2007) Nat. Rev. Cancer, 7, 213–221.

    Article  PubMed  CAS  Google Scholar 

  123. Sommer, S. S. (1994) Hum. Mutat., 3, 166–169.

    Article  PubMed  CAS  Google Scholar 

  124. Hamilton, W. D. (1964) J. Theor. Biol., 7, 1–52.

    Article  PubMed  CAS  Google Scholar 

  125. Graham, J. (1992) in Cancer Selection: The New Theory of Evolution, Aculeus Press, Lexington, USA.

    Google Scholar 

  126. Leroi, A. M., Koufopanou, V., and Burt, A. (2003) Nat. Rev. Cancer, 3, 226–231.

    Article  PubMed  CAS  Google Scholar 

  127. Manskikh, V. N. (2006) Biochemistry (Moscow), 71, 933–936.

    Article  CAS  Google Scholar 

  128. Thomas, M. A., Weston, B., Joseph, M., Wu, W., Nekrutenko, A., and Tonellato, P. J. (2003) Mol. Biol. Evol., 20, 964–968.

    Article  PubMed  CAS  Google Scholar 

  129. Frank, S. A. (2004) Proc. Natl. Acad. Sci. USA, 101, 8061–8065.

    Article  PubMed  CAS  Google Scholar 

  130. Ponder, B. A. (2001) Nature, 411, 336–341.

    Article  PubMed  CAS  Google Scholar 

  131. Kirkwood, T. B., and Austad, S. N. (2000) Nature, 408, 233–238.

    Article  PubMed  CAS  Google Scholar 

  132. Campisi, J. (2003) Nat. Rev. Cancer, 3, 339–349.

    Article  PubMed  CAS  Google Scholar 

  133. Flatt, T., and Promislow, D. E. (2007) Science, 318, 1255–1256.

    Article  PubMed  CAS  Google Scholar 

  134. Campisi, J. (2005) Cell, 120, 513–522.

    Article  PubMed  CAS  Google Scholar 

  135. Longo, V. D., Mitteldorf, J., and Skulachev, V. P. (2005) Nat Rev. Genet., 6, 866–872.

    Article  PubMed  CAS  Google Scholar 

  136. Budovskaya, Y. V., Wu, K., Southworth, L. K., Jiang, M., Tedesco, P., Johnson, T. E., and Kim, S. K. (2008) Cell, 134, 291–303.

    Article  PubMed  CAS  Google Scholar 

  137. Langowski, J. L., Zhang, X., Wu, L., Mattson, J. D., Chen, T., Smith, K., Basham, B., McClanahan, T., Kastelein, R. A., and Oft, M. (2006) Nature, 442, 461–465.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Blokhin Russian Cancer Research Center, Russian Academy of Medical Sciences, Kashirskoe Shosse 24, 115478, Moscow, Russia

    A. V. Lichtenstein

Authors
  1. A. V. Lichtenstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. V. Lichtenstein.

Additional information

Original Russian Text © A. V. Lichtenstein, 2009, published in Biokhimiya, 2009, Vol. 74, No. 4, pp. 437–447.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lichtenstein, A.V. Carcinogenesis: Evolution of concepts. Biochemistry Moscow 74, 353–361 (2009). https://doi.org/10.1134/S0006297909040014

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297909040014

Key words

Search

Navigation