Programmed Cell Death, from a Cancer Perspective: An Overview

  • Abhay P. Mishra
  • Bahare Salehi
  • Mehdi Sharifi-Rad
  • Raffaele Pezzani
  • Farzad Kobarfard
  • Javad Sharifi-Rad
  • Manisha Nigam
Review Article
  • 51 Downloads

Abstract

Programmed cell death (PCD) is probably the most widely discussed subject among the topics of cancer therapy. Over the last 2 decades an astonishing boost in our perception of cell death has been seen, and its role in cancer and cancer therapy has been thoroughly investigated. A number of discoveries have clarified the molecular mechanism of PCD, thus expounding the link between PCD and therapeutic tools. Even though PCD is assumed to play a major role in anticancer therapy, the clinical relevance of its induction remains uncertain. Since PCD involves multiple death programs including programmed necrosis and autophagic cell death, it has contributed to our better understanding of cancer pathogenesis and therapeutics. In this review, we discuss a brief outline of PCD types as well as their role in cancer therapeutics. Since irregularities in the cell death process are frequently found in various cancers, key proteins governing cell death type could be used as therapeutic targets for a wide range of cancer.

Notes

Compliance with Ethical Standards

Conflict of interest

Abhay P. Mishra, Bahare Salehi, Mehdi Sharifi-Rad, Raffaele Pezzani, Farzad Kobarfard, Javad Sharifi-Rad and Manisha Nigam declare no conflict of interest.

Funding

The authors have no funding to declare.

References

  1. 1.
    Lockshin RA, Williams CM. Programmed cell death—II. Endocrine potentiation of the breakdown of the intersegmental muscles of silkmoths. J Insect Physiol. 1964;10:643–9.CrossRefGoogle Scholar
  2. 2.
    Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.PubMedCrossRefGoogle Scholar
  3. 3.
    Jensen M, Engert A, Weissinger F, Knauf W, Kimby E, Poynton C, et al. Phase I study of a novel pro-apoptotic drug R-etodolac in patients with B-cell chronic lymphocytic leukemia. Invest New Drugs. 2008;26:139–49.PubMedCrossRefGoogle Scholar
  4. 4.
    Baritaki S, Militello L, Malaponte G, Spandidos DA, Salcedo M, Bonavida B. The anti-CD20 mAb LFB-R603 interrupts the dysregulated NF-κB/Snail/RKIP/PTEN resistance loop in B-NHL cells: role in sensitization to TRAIL apoptosis. Int J Oncol. 2011;38:1683–94.PubMedGoogle Scholar
  5. 5.
    Lockshin RA, Zakeri Z. Apoptosis, autophagy, and more. Int J Biochem Cell Biol. 2004;36:2405–19.PubMedCrossRefGoogle Scholar
  6. 6.
    Tan ML, Ooi JP, Ismail N, Moad AIH, Muhammad TST. Programmed cell death pathways and current antitumor targets. Pharm Res. 2009;26:1547–60.PubMedCrossRefGoogle Scholar
  7. 7.
    Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239–57.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Garg AD, Nowis D, Golab J, Vandenabeele P, Krysko DV, Agostinis P. Immunogenic cell death, DAMPs and anticancer therapeutics: an emerging amalgamation. Biochim Biophys Acta. 2010;1805:53–71.PubMedGoogle Scholar
  9. 9.
    Mariño G, Niso-Santano M, Baehrecke EH, Kroemer G. Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol. 2014;15:81–94.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35:495–516.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, et al. Anti- and pro-tumor functions of autophagy. Nature. 1999;397:441–6.PubMedCrossRefGoogle Scholar
  12. 12.
    Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer. 2002;2:277–88.PubMedCrossRefGoogle Scholar
  13. 13.
    Locksley RM, Killeen N, Lenardo MJ. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell. 2001;104:487–501.PubMedCrossRefGoogle Scholar
  14. 14.
    Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science. 1998;281:1305–8.PubMedCrossRefGoogle Scholar
  15. 15.
    Chicheportiche Y, Bourdon PR, Xu H, Hsu YM, Scott H, Hession C, et al. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem. 1997;272:32401–10.PubMedCrossRefGoogle Scholar
  16. 16.
    Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev. 2007;87:99–163.PubMedCrossRefGoogle Scholar
  17. 17.
    Reed JC. Bcl-2 family proteins: regulators of apoptosis and chemoresistance in hematologic malignancies. Semin Hematol. 1997;34:9–19.PubMedGoogle Scholar
  18. 18.
    Nasu Y, Benke A, Arakawa S, Yoshida GJ, Kawamura G, Manley S, Shimizu S, Ozawa T. In situ characterization of Bak clusters responsible for cell death using single molecule localization microscopy. Sci Rep. 2016;6:27505.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL-2 family reunion. Mol Cell. 2010;37:299–310.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Enari M, Sakahira H, Yokoyama H, Okawa K, Iwamatsu A, Nagata S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature. 1998;391:43–50.PubMedCrossRefGoogle Scholar
  21. 21.
    Tewari M, Quan LT, O’Rourke K, Desnoyers S, Zeng Z, Beidler DR, et al. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 1995;81:801–9.PubMedCrossRefGoogle Scholar
  22. 22.
    Schimmer AD. Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res. 2004;64:7183–90.PubMedCrossRefGoogle Scholar
  23. 23.
    Ghobrial IM, Witzig TE, Adjei AA. Targeting apoptosis pathways in cancer therapy. CA Cancer J Clin. 2005;55:178–94.PubMedCrossRefGoogle Scholar
  24. 24.
    Sakahira H, Enari M, Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature. 1998;391:96–9.PubMedCrossRefGoogle Scholar
  25. 25.
    Krysko DV, D’Herde K, Vandenabeele P. Clearance of apoptotic and necrotic cells and its immunological consequences. Apoptosis. 2006;11:1709–26.PubMedCrossRefGoogle Scholar
  26. 26.
    Ashkenazi A. Targeting the extrinsic apoptosis pathway in cancer. Cytokine Growth Factor Rev. 2008;19:325–31.PubMedCrossRefGoogle Scholar
  27. 27.
    Wong RS. Apoptosis in cancer: from pathogenesis to treatment. J Exp Clin Cancer Res. 2011;30:87.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Bai L, Wang S. Targeting apoptosis pathways for new cancer therapeutics. Annu Rev Med. 2014;65:139–55.PubMedCrossRefGoogle Scholar
  29. 29.
    Stupack DG. Caspase-8 as a therapeutic target in cancer. Cancer Lett. 2013;332:133–40.PubMedCrossRefGoogle Scholar
  30. 30.
    Wang S, Yu Q, Zhang R, Liu B. Core signaling pathways of survival/death in autophagy-related cancer networks. Int J Biochem Cell Biol. 2011;43:1263–6.PubMedCrossRefGoogle Scholar
  31. 31.
    Pyo JO, Nah J, Jung YK. Molecules and their functions in autophagy. Exp Mol Med. 2012;44:73–80.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Liu B, Bao J-K, Yang J-M, Cheng Y. Targeting autophagic pathways for cancer drug discovery. Chin J Cancer. 2013;32:113–20.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Grasso D, Vaccaro MI. Macroautophagy and the oncogene-induced senescence. Front Endocrinol (Lausanne). 2014;5:157.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Cuervo AM, Wong E. Chaperone-mediated autophagy: roles in disease and aging. Cell Res. 2014;24:92–104.PubMedCrossRefGoogle Scholar
  35. 35.
    Vakifahmetoglu-Norberg H, Kim M, Xia H-G, Iwanicki MP, Ofengeim D, Coloff JL, et al. Chaperone-mediated autophagy degrades mutant p53. Genes Dev. 2013;27:1718–30.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Han Q, Deng Y, Chen S, Chen R, Yang M, Zhang Z, et al. Downregulation of ATG5-dependent macroautophagy by chaperone-mediated autophagy promotes breast cancer cell metastasis. Sci Rep. 2017;7:4759.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Green DR, Levine B. To be or not to be? How selective autophagy and cell death govern cell fate. Cell. 2014;157:65–75.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Morselli E, Galluzzi L, Kepp O, Vicencio J-M, Criollo A, Maiuri MC, et al. Anti- and pro-tumor functions of autophagy. BBA-Mol Cell Res. 2009;1793:1524–32.Google Scholar
  39. 39.
    Shimizu S, Yoshida T, Tsujioka M, Arakawa S. Autophagic cell death and cancer. Int J Mol Sci. 2014;15:3145–53.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Gozuacik D, Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene. 2004;23:2891–906.PubMedCrossRefGoogle Scholar
  41. 41.
    Arakawa S, Tsujioka M, Yoshida T, Sakurai HT, Nishida Y, Matsuoka Y, et al. Role of Atg5-dependent cell death in the embryonic development of Bax/Bak double-knockout mice. Cell Death Differ. 2017;24:1598–608.PubMedCrossRefGoogle Scholar
  42. 42.
    Corcelle EA, Puustinen P, Jäättelä M. Apoptosis and autophagy: targeting autophagy signalling in cancer cells -’trick or treats’? FEBS J. 2009;276:6084–96.PubMedCrossRefGoogle Scholar
  43. 43.
    Bhutia SK, Kegelman TP, Das SK, Azab B, Su Z-Z, Lee S-G, et al. Astrocyte elevated gene-1 induces protective autophagy. Proc Natl Acad Sci USA. 2010;107:22243–8.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Yang J, Takahashi Y, Cheng E, Liu J, Terranova PF, Zhao B, et al. GSK-3beta promotes cell survival by modulating Bif-1-dependent autophagy and cell death. J Cell Sci. 2010;123:861–70.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Wu WKK, Cho CH, Lee CW, Wu YC, Yu L, Li ZJ, et al. Macroautophagy and ERK phosphorylation counteract the antiproliferative effect of proteasome inhibitor in gastric cancer cells. Autophagy. 2010;6:228–38.PubMedCrossRefGoogle Scholar
  46. 46.
    Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol. 2000;150:1507–13.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Hara T, Takamura A, Kishi C, Iemura S, Natsume T, Guan J-L, et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol. 2008;181:497–510.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Suzuki K, Kubota Y, Sekito T, Ohsumi Y. Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells. 2007;12:209–18.PubMedCrossRefGoogle Scholar
  49. 49.
    Feng Z, Zhang H, Levine AJ, Jin S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci USA. 2005;102:8204–9.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Inoki K, Li Y, Zhu T, Wu J, Guan K-L. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol. 2002;4:648–57.PubMedCrossRefGoogle Scholar
  51. 51.
    Shimizu S, Konishi A, Nishida Y, Mizuta T, Nishina H, Yamamoto A, Tsujimoto Y. Involvement of JNK in the regulation of autophagic cell death. Oncogene. 2010;29:2070–82.PubMedCrossRefGoogle Scholar
  52. 52.
    Zhou Y-Y, Li Y, Jiang W-Q, Zhou L-F. MAPK/JNK signalling: a potential autophagy regulation pathway. Biosci Rep. 2015;35(3):e00199.PubMedPubMedCentralGoogle Scholar
  53. 53.
    Zhang Y, Chen P, Hong H, Wang L, Zhou Y, Lang Y. JNK pathway mediates curcumin-induced apoptosis and autophagy in osteosarcoma MG63 cells. Exp Ther Med. 2017;14:593–9.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer. 2009;9:537–49.PubMedCrossRefGoogle Scholar
  55. 55.
    Masri J, Bernath A, Martin J, Jo OD, Vartanian R, Funk A, et al. mTORC2 activity is elevated in gliomas and promotes growth and cell motility via overexpression of rictor. Cancer Res. 2007;67:11712–20.PubMedCrossRefGoogle Scholar
  56. 56.
    Wang MH, Sun R, Zhou XM, Zhang MY, Lu JB, Yang Y, et al. Epithelial cell adhesion molecule overexpression regulates epithelial-mesenchymal transition, stemness and metastasis of nasopharyngeal carcinoma cells via the PTEN/AKT/mTOR pathway. Cell Death Dis. 2018;9:2.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Ni J, Cozzi P, Hao J, Beretov J, Chang L, Duan W, et al. Epithelial cell adhesion molecule (EpCAM) is associated with prostate cancer metastasis and chemo/radioresistance via the PI3K/Akt/mTOR signaling pathway. Int J Biochem Cell Biol. 2013;45(12):2736–48.PubMedCrossRefGoogle Scholar
  58. 58.
    Rebecca VW, Amaravadi RK. Emerging strategies to effectively target autophagy in cancer. Oncogene. 2016;35:1–11.PubMedCrossRefGoogle Scholar
  59. 59.
    Catena V, Fanciulli M. Deptor: not only a mTOR inhibitor. J Exp Clin Cancer Res. 2017;36:12.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Hu B, Lv X, Gao F, Chen S, Wang S, Qing X, et al. Downregulation of DEPTOR inhibits the proliferation, migration, and survival of osteosarcoma through PI3K/Akt/mTOR pathway. Onco Targets Ther. 2017;10:4379.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Langedijk J, Mantel-Teeuwisse AK, Slijkerman DS, Schutjens MH. Drug repositioning and repurposing: terminology and definitions in literature. Drug Discov Today. 2015;20(8):1027–34.PubMedCrossRefGoogle Scholar
  62. 62.
    Tommasino C, Gambardella L, Buoncervello M, Griffin RJ, Golding BT, Alberton M, et al. New derivatives of the antimalarial drug Pyrimethamine in the control of melanoma tumor growth: an in vitro and in vivo study. J Exp Clin. Cancer Res. 2016;35(1):137.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Yoshida GJ. Therapeutic strategies of drug repositioning targeting autophagy to induce cancer cell death: from pathophysiology to treatment. J Hematol Oncol. 2017;10:67.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Chang C, Simmons DT, Martin MA, Mora PT. Identification and partial characterization of new antigens from simian virus 40-transformed mouse cells. J Virol. 1979;31:463–71.PubMedPubMedCentralGoogle Scholar
  65. 65.
    DeLeo AB, Jay G, Appella E, Dubois GC, Law LW, Old LJ. Detection of a transformation-related antigen in chemically induced sarcomas and other transformed cells of the mouse. Proc Natl Acad Sci USA. 1979;76:2420–4.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Kress M, May E, Cassingena R, May P. Simian virus 40-transformed cells express new species of proteins precipitable by anti-simian virus 40 tumor serum. J Virol. 1979;31:472–83.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Lane DP, Crawford LV. T antigen is bound to a host protein in SV40-transformed cells. Nature. 1979;278:261–3.PubMedCrossRefGoogle Scholar
  68. 68.
    Chaabane W, User SD, El-Gazzah M, Jaksik R, Sajjadi E, Rzeszowska-Wolny J, et al. Autophagy, apoptosis, mitoptosis and necrosis: interdependence between those pathways and effects on cancer. Arch Immunol Ther Exp (Warsz.). 2013;61:43–58.CrossRefGoogle Scholar
  69. 69.
    Rotter V. p53, a transformation-related cellular-encoded protein, can be used as a biochemical marker for the detection of primary mouse tumor cells. Proc Natl Acad Sci USA. 1983;80:2613–7.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Balaburski GM, Hontz RD, Murphy ME. p53 and ARF: unexpected players in autophagy. Trends Cell Biol. 2010;20:363–9.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Budanov AV, Karin M. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell. 2008;134:451–60.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Crighton D, Wilkinson S, O’Prey J, Syed N, Smith P, Harrison PR, et al. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell. 2006;126:121–34.PubMedCrossRefGoogle Scholar
  73. 73.
    Crighton D, O’Prey J, Bell HS, Ryan KM. p73 regulates DRAM-independent autophagy that does not contribute to programmed cell death. Cell Death Differ. 2007;14:1071–9.PubMedCrossRefGoogle Scholar
  74. 74.
    Newton K, Manning G. Necroptosis and Inflammation. Annu Rev Biochem. 2016;85:743–63.PubMedCrossRefGoogle Scholar
  75. 75.
    Su Z, Yang Z, Xu Y, Chen Y, Yu Q. Apoptosis, autophagy, necroptosis, and cancer metastasis. Mol Cancer. 2015;14:48.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Cho YS, Park SY. Harnessing of programmed necrosis for fighting against cancers. Biomol Ther (Seoul). 2014;22:167–75.CrossRefGoogle Scholar
  77. 77.
    Wang T, Jin Y, Yang W, Zhang L, Jin X, Liu X, et al. Necroptosis in cancer: an angel or a demon? Tumour Biol. 2017;39:1–11.Google Scholar
  78. 78.
    Chan FK-M. Programmed necrosis/necroptosis: an inflammatory form of cell death. In: Wu H, editor. Cell death: mechanism and disease. New York: Springer; 2014. p. 211–28.CrossRefGoogle Scholar
  79. 79.
    Ch’en IL, Tsau JS, Molkentin JD, Komatsu M, Hedrick SM. Mechanisms of necroptosis in T cells. J Exp Med. 2011;208:633–41.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Lu JV, Chen HC, Walsh CM. Necroptotic signaling in adaptive and innate immunity. Semin Cell Dev Biol. 2014;35:33–9.PubMedCrossRefGoogle Scholar
  81. 81.
    Dempsey LA. Interferon-induced necroptosis. Nat Immunol. 2013;14:892.Google Scholar
  82. 82.
    He S, Liang Y, Shao F, Wang X. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc Natl Acad Sci USA. 2011;108:20054–9.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol. 2005;1:112–9.PubMedCrossRefGoogle Scholar
  84. 84.
    Vandenabeele P, Declercq W, Van Herreweghe F, Vanden Berghe T. The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci Signal. 2010;3:4.CrossRefGoogle Scholar
  85. 85.
    Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol. 2010;11:700–14.PubMedCrossRefGoogle Scholar
  86. 86.
    Wright A, Reiley WW, Chang M, Jin W, Lee AJ, Zhang M, et al. Regulation of early wave of germ cell apoptosis and spermatogenesis by deubiquitinating enzyme CYLD. Dev Cell. 2007;13:705–16.PubMedCrossRefGoogle Scholar
  87. 87.
    Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell. 2003;114:181–90.PubMedCrossRefGoogle Scholar
  88. 88.
    Lin Y, Devin A, Rodriguez Y, Liu ZG. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 1999;13:2514–26.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Christofferson DE, Yuan J. Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol. 2010;22:263–8.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Sun L, Wang H, Wang Z, He S, Chen S, Liao D, et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 2012;148:213–27.PubMedCrossRefGoogle Scholar
  91. 91.
    Tenev T, Bianchi K, Darding M, Broemer M, Langlais C, Wallberg F, et al. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell. 2011;43:432–48.PubMedCrossRefGoogle Scholar
  92. 92.
    Xu YZ, Kanagaratham C, Youssef M, Radzioch D. New frontiers in cancer chemotherapy—targeting cell death pathways. In: Najman S, editor. Cell biology—new insights. Rijeka: InTech; 2016. p. 93–140.Google Scholar
  93. 93.
    Su Z, Yang Z, Xu Y, Chen Y, Yu Q. Apoptosis, autophagy, necroptosis, and cancer metastasis. Mol Cancer. 2015;14:48.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Fu Z, Deng B, Liao Y, Shan L, Yin F, Wang Z, et al. The anti-tumor effect of shikonin on osteosarcoma by inducing RIP1 and RIP3 dependent necroptosis. BMC Cancer. 2013;13:580.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Buchheit CL, Rayavarapu RR, Schafer ZT. The regulation of cancer cell death and metabolism by extracellular matrix attachment. Semin Cell Dev Biol. 2012;23:402–11.PubMedCrossRefGoogle Scholar
  96. 96.
    Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell. 2009;137:1112–23.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Yang WS, Stockwell BR. Ferroptosis: death by lipid peroxidation. Trends Cell Biol. 2016;26:165–76.PubMedCrossRefGoogle Scholar
  98. 98.
    Yang WS, SriRamaratnam R, Welsch ME, Shimada K, Skouta R, Viswanathan VS, et al. Regulation of ferroptotic cancer cell death by GPX4. Cell. 2014;156:317–31.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Jiang L, Kon N, Li T, Wang SJ, Su T, Hibshoosh H, Baer R, Gu W, et al. Ferroptosis as a p53-mediated activity during tumour suppression. Nature. 2015;520:57–62.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Gao M, Monian P, Pan Q, Zhang W, Xiang J, Jiang X. Ferroptosis is an autophagic cell death process. Cell Res. 2016;26(9):1021–32.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Cho YS, Park HL. Exploitation of necroptosis for treatment of caspase-compromised cancers. Oncol Lett. 2017;14:1207–14.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Los M, Mozoluk M, Ferrari D, Stepczynska A, Stroh C, Renz A, et al. Activation and caspase-mediated inhibition of PARP: a molecular switch between fibroblast necrosis and apoptosis in death receptor signaling. Mol Biol Cell. 2002;13:978–88.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Vandenabeele P, Vanden Berghe T, Festjens N. Caspase inhibitors promote alternative cell death pathways. Sci STKE. 2006;6:pe44.Google Scholar
  104. 104.
    Lu JV, Weist BM, van Raam BJ, Marro BS, Nguyen LV, Srinivas P, et al. Complementary roles of Fas-associated death domain (FADD) and receptor interacting protein kinase-3 (RIPK3) in T-cell homeostasis and antiviral immunity. Proc Natl Acad Sci USA. 2011;108:15312–7.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Nigam M, Ranjan V, Srivastava S, Sharma R, Balapure AK. Centchroman induces G0/G1 arrest and caspase-dependent apoptosis involving mitochondrial membrane depolarization in MCF-7 and MDA MB-231 human breast cancer cells. Life Sci. 2008;82:577–90.PubMedCrossRefGoogle Scholar
  106. 106.
    Nigam M, Singh N, Ranjan V, Zaidi D, Sharma R, Nigam D, et al. Centchroman mediated apoptosis involves cross-talk between extrinsic/intrinsic pathways and oxidative regulation. Life Sci. 2010;87:750–8.PubMedCrossRefGoogle Scholar
  107. 107.
    Singh N, Nigam M, Ranjan V, Sharma R, Balapure AK, Rath SK. Caspase mediated enhanced apoptotic action of cyclophosphamide- and resveratrol-treated MCF-7 cells. J Pharmacol Sci. 2009;109:473–85.PubMedCrossRefGoogle Scholar
  108. 108.
    Sharifi-Rad J, Sureda A, Tenore GC, Daglia M, Sharifi-Rad M, Valussi M, Tundis R, Sharifi-Rad M, Loizzo MR, Ademiluyi AO, Sharifi-Rad R, Ayatollahi SA, Iriti M. Biological activities of essential oils: from plant chemoecology to traditional healing systems. Molecules. 2017;22:70.CrossRefGoogle Scholar
  109. 109.
    Singh N, Nigam M, Ranjan V, Zaidi D, Garg VK, Sharma S, et al. Resveratrol as an adjunct therapy in cyclophosphamide-treated MCF-7 cells and breast tumor explants. Cancer Sci. 2011;102:1059–67.PubMedCrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Pharmaceutical ChemistryH. N. B. Garhwal (A Central) UniversitySrinagar GarhwalIndia
  2. 2.Medical Ethics and Law Research CenterShahid Beheshti University of Medical SciencesTehranIran
  3. 3.Department of Medical ParasitologyZabol University of Medical SciencesZabolIran
  4. 4.OU Endocrinology, Dept. Medicine (DIMED)University of PadovaPaduaItaly
  5. 5.AIROB, Associazione Italiana per la Ricerca Oncologica di BasePaduaItaly
  6. 6.Phytochemistry Research CenterShahid Beheshti University of Medical SciencesTehranIran
  7. 7.Department of Medicinal Chemistry, School of PharmacyShahid Beheshti University of Medical SciencesTehranIran
  8. 8.Department of Chemistry, Richardson College for the Environmental Science ComplexThe University of WinnipegWinnipegCanada
  9. 9.Department of BiochemistryH. N. B. Garhwal (A Central) UniversitySrinagar GarhwalIndia

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