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International Journal of Cell Biology
Volume 2010 (2010), Article ID 370835, 6 pages
http://dx.doi.org/10.1155/2010/370835
Review Article

Evasion of Apoptosis as a Cellular Stress Response in Cancer

Ulm University, Children's Hospital, Eythstraße 24, 89075 Ulm, Germany

Received 27 July 2009; Accepted 6 November 2009

Academic Editor: Adrienne M. Gorman

Copyright © 2010 Simone Fulda. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. A. Lockshin and Z. Zakeri, “Cell death in health and disease,” Journal of Cellular and Molecular Medicine, vol. 11, no. 6, pp. 1214–1224, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. D. Kültz, “Molecular and evolutionary basis of the cellular stress response,” Annual Review of Physiology, vol. 67, pp. 225–257, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Fulda and K.-M. Debatin, “Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy,” Oncogene, vol. 25, no. 34, pp. 4798–4811, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. M. O. Hengartner, “The biochemistry of apoptosis,” Nature, vol. 407, no. 6805, pp. 770–776, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Degterev, M. Boyce, and J. Yuan, “A decade of caspases,” Oncogene, vol. 22, no. 53, pp. 8543–8567, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. F. C. Kischkel, S. Hellbardt, I. Behrmann et al., “Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor,” The EMBO Journal, vol. 14, no. 22, pp. 5579–5588, 1995. View at Google Scholar · View at Scopus
  7. A. Ashkenazi, “Targeting the extrinsic apoptosis pathway in cancer,” Cytokine and Growth Factor Reviews, vol. 19, no. 3-4, pp. 325–331, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. J. M. Adams and S. Cory, “The Bcl-2 apoptotic switch in cancer development and therapy,” Oncogene, vol. 26, no. 9, pp. 1324–1337, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. G. Kroemer, L. Galluzzi, and C. Brenner, “Mitochondrial membrane permeabilization in cell death,” Physiological Reviews, vol. 87, no. 1, pp. 99–163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. E. C. LaCasse, D. J. Mahoney, H. H. Cheung, S. Plenchette, S. Baird, and R. G. Korneluk, “IAP-targeted therapies for cancer,” Oncogene, vol. 27, no. 48, pp. 6252–6275, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Fulda and K.-M. Debatin, “Apoptosis signaling pathways in anticancer therapy,” Current Cancer Therapy Reviews, vol. 4, no. 1, pp. 14–20, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. W. P. Roos and B. Kaina, “DNA damage-induced cell death by apoptosis,” Trends in Molecular Medicine, vol. 12, no. 9, pp. 440–450, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. N. D. Perkins and T. D. Gilmore, “Good cop, bad cop: the different faces of NF-κB,” Cell Death and Differentiation, vol. 13, no. 5, pp. 759–772, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. C. R. Weston and R. J. Davis, “The JNK signal transduction pathway,” Current Opinion in Cell Biology, vol. 19, no. 2, pp. 142–149, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Loesch and G. Chen, “The p38 MAPK stress pathway as a tumor suppressor or more?” Frontiers in Bioscience, vol. 13, no. 9, pp. 3581–3593, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Okada and T. W. Mak, “Pathways of apoptotic and non-apoptotic death in tumour cells,” Nature Reviews Cancer, vol. 4, no. 8, pp. 592–603, 2004. View at Google Scholar · View at Scopus
  17. Y. Kondo, T. Kanzawa, R. Sawaya, and S. Kondo, “The role of autophagy in cancer development and response to therapy,” Nature Reviews Cancer, vol. 5, no. 9, pp. 726–734, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Fulda, “Tumor resistance to apoptosis,” International Journal of Cancer, vol. 124, no. 3, pp. 511–515, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. I. Lavrik, A. Golks, and P. H. Krammer, “Death receptor signaling,” Journal of Cell Science, vol. 118, no. 2, pp. 265–267, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Friesen, S. Fulda, and K.-M. Debatin, “Deficient activation of the CD95 (APO-1/Fas) system in drug-resistant cells,” Leukemia, vol. 11, no. 11, pp. 1833–1841, 1997. View at Google Scholar · View at Scopus
  21. S. Fulda, M. Los, C. Friesen, and K.-M. Debatin, “Chemosensitivity of solid tumor cells in vitro is related to activation of the CD95 system,” International Journal of Cancer, vol. 76, no. 1, pp. 105–114, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. Z. Jin, E. R. McDonald III, D. T. Dicker, and W. S. El-Deiry, “Deficient tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor transport to the cell surface in human colon cancer cells selected for resistance to TRAIL-induced apoptosis,” The Journal of Biological Chemistry, vol. 279, no. 34, pp. 35829–35839, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. I. Petak, R. P. Danam, D. M. Tillman et al., “Hypermethylation of the gene promoter and enhancer region can regulate Fas expression and sensitivity in colon carcinoma,” Cell Death and Differentiation, vol. 10, no. 2, pp. 211–217, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. M. M. Van Noesel, S. Van Bezouw, G. S. Salomons et al., “Tumor-specific down-regulation of the tumor necrosis factor-related apoptosis-inducing ligand decoy receptors DcR1 and DcR2 is associated with dense promoter hypermethylation,” Cancer Research, vol. 62, no. 7, pp. 2157–2161, 2002. View at Google Scholar · View at Scopus
  25. R. M. Pitti, S. A. Marsters, D. A. Lawrence et al., “Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer,” Nature, vol. 396, no. 6712, pp. 699–703, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. W. Roth, S. Isenmann, M. Nakamura et al., “Soluble decoy receptor 3 is expressed by malignant gliomas and suppresses CD95 ligand-induced apoptosis and chemotaxis,” Cancer Research, vol. 61, no. 6, pp. 2759–2765, 2001. View at Google Scholar · View at Scopus
  27. M. S. Sheikh, Y. Huang, E. A. Fernandez-Salas et al., “The antiapoptotic decoy receptor TRID/TRAIL-R3 is a p53-regulated DNA damage-inducible gene that is overexpressed in primary tumors of the gastrointestinal tract,” Oncogene, vol. 18, no. 28, pp. 4153–4159, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. O. Micheau, “Cellular FLICE-inhibitory protein: an attractive therapeutic target?” Expert Opinion on Therapeutic Targets, vol. 7, no. 4, pp. 559–573, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. B. C. Barnhart, J. C. Lee, E. C. Alappat, and M. E. Peter, “The death effector domain protein family,” Oncogene, vol. 22, no. 53, pp. 8634–8644, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. X. Wang, Y. Wang, H. P. Kim, A. M. K. Choi, and S. W. Ryter, “FLIP inhibits endothelial cell apoptosis during hyperoxia by suppressing Bax,” Free Radical Biology and Medicine, vol. 42, no. 10, pp. 1599–1609, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. H. S. Kim, J. W. Lee, Y. H. Soung et al., “Inactivating mutations of caspase-8 gene in colorectal carcinomas,” Gastroenterology, vol. 125, no. 3, pp. 708–715, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Mandruzzato, F. Brasseur, G. Andry, T. Boon, and P. Van der Bruggen, “A CASP-8 mutation recognized by cytolytic T lymphocytes on a human head and neck carcinoma,” Journal of Experimental Medicine, vol. 186, no. 5, pp. 785–793, 1997. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Teitz, W. Wei, M. B. Valentine et al., “Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN,” Nature Medicine, vol. 6, no. 5, pp. 529–535, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. M. A. Miller, B. Karacay, X. Zhu, M. S. O'Dorisio, and A. D. Sandler, “Caspase 8L, a novel inhibitory isoform of caspase 8, is associated with undifferentiated neuroblastoma,” Apoptosis, vol. 11, no. 1, pp. 15–24, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Mohr, R. M. Zwacka, G. Jarmy et al., “Caspase-8L expression protects CD34+ hematopoietic progenitor cells and leukemic cells from CD95-mediated apoptosis,” Oncogene, vol. 24, no. 14, pp. 2421–2429, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Fulda, M. U. Küfer, E. Meyer, F. van Valen, B. Dockhorn-Dworniczak, and K.-M. Debatin, “Sensitization for death receptor- or drug-induced apoptosis by re-expression of caspase-8 through demethylation or gene transfer,” Oncogene, vol. 20, no. 41, pp. 5865–5877, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Hopkins-Donaldson, A. Ziegler, S. Kurtz et al., “Silencing of death receptor and caspase-8 expression in small cell lung carcinoma cell lines tumors by DNA methylation,” Cell Death and Differentiation, vol. 10, no. 3, pp. 356–364, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Pingoud-Meier, D. Lang, A. J. Janss et al., “Loss of caspase-8 protein expression correlates with unfavorable survival outcome in childhood medulloblastoma,” Clinical Cancer Research, vol. 9, no. 17, pp. 6401–6409, 2003. View at Google Scholar · View at Scopus
  39. K. Harada, S. Toyooka, N. Shivapurkar et al., “Deregulation of caspase 8 and 10 expression in pediatric tumors and cell lines,” Cancer Research, vol. 62, no. 20, pp. 5897–5901, 2002. View at Google Scholar · View at Scopus
  40. S. Cursi, A. Rufini, V. Stagni et al., “Src kinase phosphorylates caspase-8 on Tyr380: a novel mechanism of apoptosis suppression,” The EMBO Journal, vol. 25, no. 9, pp. 1895–1905, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Letai, M. C. Bassik, L. D. Walensky, M. D. Sorcinelli, S. Weiler, and S. J. Korsmeyer, “Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics,” Cancer Cell, vol. 2, no. 3, pp. 183–192, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Chen, S. N. Willis, A. Wei et al., “Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function,” Molecular Cell, vol. 17, no. 3, pp. 393–403, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. S. N. Willis, J. I. Fletcher, T. Kaufmann et al., “Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak,” Science, vol. 315, no. 5813, pp. 856–859, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. Z. X. Chen and S. Pervaiz, “BCL-2: pro-or anti-oxidant?” Frontiers in Bioscience, vol. 1, pp. 263–268, 2009. View at Google Scholar
  45. W. Dröge, “Free radicals in the physiological control of cell function,” Physiological Reviews, vol. 82, no. 1, pp. 47–95, 2002. View at Google Scholar · View at Scopus
  46. D. M. Hockenbery, Z. N. Oltvai, X.-M. Yin, C. L. Milliman, and S. J. Korsmeyer, “Bcl-2 functions in an antioxidant pathway to prevent apoptosis,” Cell, vol. 75, no. 2, pp. 241–251, 1993. View at Publisher · View at Google Scholar · View at Scopus
  47. M.-V. Clément, J. L. Hirpara, and S. Pervaiz, “Decrease in intracellular superoxide sensitizes Bcl-2-overexpressing tumor cells to receptor and drug-induced apoptosis independent of the mitochondria,” Cell Death and Differentiation, vol. 10, no. 11, pp. 1273–1285, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. Z. T. Schafer and S. Kornbluth, “The apoptosome: physiological, developmental, and pathological modes of regulation,” Developmental Cell, vol. 10, no. 5, pp. 549–561, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. V. Borutaite and G. C. Brown, “Mitochondrial regulation of caspase activation by cytochrome oxidase and tetramethylphenylenediamine via cytosolic cytochrome c redox state,” The Journal of Biological Chemistry, vol. 282, no. 43, pp. 31124–31130, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. Z. Pan, D. W. Voehringer, and R. E. Meyn, “Analysis of redox regulation of cytochrome c-induced apoptosis in a cell-free system,” Cell Death and Differentiation, vol. 6, no. 7, pp. 683–688, 1999. View at Google Scholar · View at Scopus
  51. D. Suto, K. Sato, Y. Ohba, T. Yoshimura, and J. Fujii, “Suppression of the pro-apoptotic function of cytochrome c by singlet oxygen via a haem redox state-independent mechanism,” Biochemical Journal, vol. 392, no. 2, part 2, pp. 399–406, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. I. Sturm, A. G. Bosanquet, S. Radetzki, M. Hummel, B. Dörken, and P. T. Daniel, “Silencing of APAF-1 in B-CLL results in poor prognosis in the case of concomitant p53 mutation,” International Journal of Cancer, vol. 118, no. 9, pp. 2329–2336, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. M. S. Soengas, P. Capodieci, D. Polsky et al., “Inactivation of the apoptosis effector Apaf-1 in malignant melanoma,” Nature, vol. 409, no. 6817, pp. 207–211, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. W.-N. Fu, F. Bertoni, S. M. Kelsey et al., “Role of DNA methylation in the suppression of Apaf-1 protein in human leukaemia,” Oncogene, vol. 22, no. 3, pp. 451–455, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. H.-L. Wang, H. Bai, Y. Li, J. Sun, and X.-Q. Wang, “Rationales for expression and altered expression of apoptotic protease activating factor-1 gene in gastric cancer,” World Journal of Gastroenterology, vol. 13, no. 38, pp. 5060–5064, 2007. View at Google Scholar · View at Scopus
  56. T. Watanabe, Y. Hirota, Y. Arakawa et al., “Frequent LOH at chromosome 12q22-23 and Apaf-1 inactivation in glioblastoma,” Brain Pathology, vol. 13, no. 4, pp. 431–439, 2003. View at Google Scholar · View at Scopus
  57. S. Fulda, “Targeting inhibitor of apoptosis proteins (IAPs) for cancer therapy,” Anti-Cancer Agents in Medicinal Chemistry, vol. 8, no. 5, pp. 533–539, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. E. N. Shiozaki and Y. Shi, “Caspases, IAPs and Smac/DIABLO: mechanisms from structural biology,” Trends in Biochemical Sciences, vol. 29, no. 9, pp. 486–494, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. B. P. Eckelman, G. S. Salvesen, and F. L. Scott, “Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family,” The EMBO Reports, vol. 7, no. 10, pp. 988–994, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. S. M. Lewis and M. Holcik, “IRES in distress: translational regulation of the inhibitor of apoptosis proteins XIAP and HIAP2 during cell stress,” Cell Death and Differentiation, vol. 12, no. 6, pp. 547–553, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. X. Saelens, M. Kalai, and P. Vandenabeele, “Translation inhibition in apoptosis: caspase-dependent PKR activation and eIF2-α phosphorylation,” The Journal of Biological Chemistry, vol. 276, no. 45, pp. 41620–41628, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. L. D. Kapp and J. R. Lorsch, “The molecular mechanics of eukaryotic translation,” Annual Review of Biochemistry, vol. 73, pp. 657–704, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Holcik, C. Yeh, R. G. Korneluk, and T. Chow, “Translational upregulation of X-linked inhibitor of apoptosis (XIAP) increases resistance to radiation induced cell death,” Oncogene, vol. 19, no. 36, pp. 4174–4177, 2000. View at Google Scholar · View at Scopus
  64. M. Holcik, C. Lefebvre, C. Yeh, T. Chow, and R. G. Korneluk, “A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection,” Nature Cell Biology, vol. 1, no. 3, pp. 190–192, 1999. View at Google Scholar · View at Scopus
  65. D. Warnakulasuriyarachchi, S. Cerquozzi, H. H. Cheung, and M. Holcík, “Translational induction of the inhibitor of apoptosis protein HIAP2 during endoplasmic reticulum stress attenuates cell death and is mediated via an inducible internal ribosome entry site element,” The Journal of Biological Chemistry, vol. 279, no. 17, pp. 17148–17157, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. M. E. Van Eden, M. P. Byrd, K. W. Sherrill, and R. E. Lloyd, “Translation of cellular inhibitor of apoptosis protein 1 (c-IAP1) mRNA is IRES mediated and regulated during cell stress,” RNA, vol. 10, no. 3, pp. 469–481, 2004. View at Publisher · View at Google Scholar · View at Scopus