DOI QR코드

DOI QR Code

The role of necroptosis in the treatment of diseases

  • Received : 2018.03.20
  • Published : 2018.05.31

Abstract

Necroptosis is an emerging form of programmed cell death occurring via active and well-regulated necrosis, distinct from apoptosis morphologically, and biochemically. Necroptosis is mainly unmasked when apoptosis is compromised in response to tumor necrosis factor alpha. Unlike apoptotic cells, which are cleared by macrophages or neighboring cells, necrotic cells release danger signals, triggering inflammation, and exacerbating tissue damage. Evidence increasingly suggests that programmed necrosis is not only associated with pathophysiology of disease, but also induces innate immune response to viral infection. Therefore, necroptotic cell death plays both physiological and pathological roles. Physiologically, necroptosis induce an innate immune response as well as premature assembly of viral particles in cells infected with virus that abrogates host apoptotic machinery. On the other hand, necroptosis per se is detrimental, causing various diseases such as sepsis, neurodegenerative diseases and ischemic reperfusion injury. This review discusses the signaling pathways leading to necroptosis, associated necroptotic proteins with target-specific inhibitors and diseases involved. Several studies currently focus on protective approaches to inhibiting necroptotic cell death. In cancer biology, however, anticancer drug resistance severely hampers the efficacy of chemotherapy based on apoptosis. Pharmacological switch of cell death finds therapeutic application in drug- resistant cancers. Therefore, the possible clinical role of necroptosis in cancer control will be discussed in brief.

Keywords

References

  1. Jouan-Lanhouet S, Arshad MI, Piquet-Pellorce C et al (2012) TRAIL induces necroptosis involving RIPK1/RIPK3- dependent PARP-1 activation. Cell Death Differ 19, 2003-2014 https://doi.org/10.1038/cdd.2012.90
  2. Moriwaki K, Bertin J, Gough PJ, Orlowski GM and Chan FK (2015) Differential roles of RIPK1 and RIPK3 in TNF-induced necroptosis and chemotherapeutic agentinduced cell death. Cell Death Dis 6, e1636 https://doi.org/10.1038/cddis.2015.16
  3. Miao B and Degterev A (2009) Methods to analyze cellular necroptosis. Methods Mol Biol 559, 79-93
  4. Hitomi J, Christofferson DE, Ng A et al (2008) Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135, 1311-1323 https://doi.org/10.1016/j.cell.2008.10.044
  5. Degterev A, Hitomi J, Germscheid M et al (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 4, 313-321 https://doi.org/10.1038/nchembio.83
  6. Cho YS, Challa S, Moquin D et al (2009) Phosphorylationdriven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137, 1112-1123 https://doi.org/10.1016/j.cell.2009.05.037
  7. Sun L, Wang H, Wang Z et al (2012) Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148, 213-227 https://doi.org/10.1016/j.cell.2011.11.031
  8. Wang Z, Jiang H, Chen S, Du F and Wang X (2012) The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 148, 228-243 https://doi.org/10.1016/j.cell.2011.11.030
  9. Feoktistova M and Leverkus M (2015) Programmed necrosis and necroptosis signalling. FEBS J 282, 19-31 https://doi.org/10.1111/febs.13120
  10. Belizario J, Vieira-Cordeiro L and Enns S (2015) Necroptotic Cell Death Signaling and Execution Pathway: Lessons from Knockout Mice. Mediators Inflamm 2015, 128076
  11. Frank S, Gaume B, Bergmann-Leitner ES et al (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 1, 515-525 https://doi.org/10.1016/S1534-5807(01)00055-7
  12. Vanlangenakker N, Vanden Berghe T, Krysko DV, Festjens N and Vandenabeele P (2008) Molecular mechanisms and pathophysiology of necrotic cell death. Curr Mol Med 8, 207-220 https://doi.org/10.2174/156652408784221306
  13. Janko C, Filipovic M, Munoz LE et al (2014) Redox modulation of HMGB1-related signaling. Antioxid Redox Signal 20, 1075-1085 https://doi.org/10.1089/ars.2013.5179
  14. Stern D, Yan SD, Yan SF and Schmidt AM (2002) Receptor for advanced glycation endproducts: a multiligand receptor magnifying cell stress in diverse pathologic settings. Adv Drug Deliv Rev 54, 1615-1625 https://doi.org/10.1016/S0169-409X(02)00160-6
  15. Degterev A, Maki JL and Yuan J (2013) Activity and specificity of necrostatin-1, small-molecule inhibitor of RIP1 kinase. Cell Death Differ 20, 366 https://doi.org/10.1038/cdd.2012.133
  16. Liu ZY, Wu B, Guo YS et al (2015) Necrostatin-1 reduces intestinal inflammation and colitis-associated tumorigenesis in mice. Am J Cancer Res 5, 3174-3185
  17. Nomura M, Ueno A, Saga K, Fukuzawa M and Kaneda Y (2014) Accumulation of cytosolic calcium induces necroptotic cell death in human neuroblastoma. Cancer Res 74, 1056-1066 https://doi.org/10.1158/0008-5472.CAN-13-1283
  18. Roychowdhury S, McMullen MR, Pisano SG, Liu X and Nagy LE (2013) Absence of receptor interacting protein kinase 3 prevents ethanol-induced liver injury. Hepatology 57, 1773-1783 https://doi.org/10.1002/hep.26200
  19. Wang Y, Wang H, Tao Y, Zhang S, Wang J and Feng X (2014) Necroptosis inhibitor necrostatin-1 promotes cell protection and physiological function in traumatic spinal cord injury. Neuroscience 266, 91-101 https://doi.org/10.1016/j.neuroscience.2014.02.007
  20. Harris PA, Bandyopadhyay D, Berger SB et al (2013) Discovery of small molecule RIP1 kinase inhibitors for the treatment of pathologies associated with necroptosis. ACS Med Chem Lett 4, 1238-1243 https://doi.org/10.1021/ml400382p
  21. Berger SB, Harris P, Nagilla R et al (2015) Characterization of GSK'963: a structurally distinct, potent and selective inhibitor of RIP1 kinase. Cell Death Discov 1, 15009
  22. Vandenabeele P, Declercq W, Van Herreweghe F and Vanden Berghe T (2010) The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci Signal 3, re4
  23. Park SY, Shim JH and Cho YS (2014) Distinctive roles of receptor-interacting protein kinases 1 and 3 in caspase-independent cell death of L929. Cell Biochem Funct 32, 62-69 https://doi.org/10.1002/cbf.2972
  24. Fettweis G, Di Valentin E, L'Homme L et al (2017) RIP3 antagonizes a TSC2-mediated pro-survival pathway in glioblastoma cell death. Biochim Biophys Acta 1864, 113-124 https://doi.org/10.1016/j.bbamcr.2016.10.014
  25. Mandal P, Berger SB, Pillay S et al (2014) RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol Cell 56, 481-495 https://doi.org/10.1016/j.molcel.2014.10.021
  26. Yan B, Liu L, Huang S et al (2017) Discovery of a new class of highly potent necroptosis inhibitors targeting the mixed lineage kinase domain-like protein. Chem Commun (Camb) 53, 3637-3640 https://doi.org/10.1039/C7CC00667E
  27. Fauster A, Rebsamen M, Huber KV et al (2015) A cellular screen identifies ponatinib and pazopanib as inhibitors of necroptosis. Cell Death Dis 6, e1767 https://doi.org/10.1038/cddis.2015.130
  28. Feldmann F, Schenk B, Martens S, Vandenabeele P and Fulda S (2017) Sorafenib inhibits therapeutic induction of necroptosis in acute leukemia cells. Oncotarget 8, 68208-68220
  29. Sosna J, Voigt S, Mathieu S et al (2013) The proteases HtrA2/Omi and UCH-L1 regulate TNF-induced necroptosis. Cell Commun Signal 11, 76 https://doi.org/10.1186/1478-811X-11-76
  30. Ardestani S, Deskins DL and Young PP (2013) Membrane TNF-alpha-activated programmed necrosis is mediated by ceramide-induced reactive oxygen species. J Mol Signal 8, 12 https://doi.org/10.1186/1750-2187-8-12
  31. Lin Y, Choksi S, Shen HM et al (2004) Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem 279, 10822-10828 https://doi.org/10.1074/jbc.M313141200
  32. Dong W, Li Z, Chen Y et al (2017) NADPH oxidase inhibitor, diphenyleneiodonium prevents necroptosis in HK-2 cells. Biomed Rep 7, 226-230 https://doi.org/10.3892/br.2017.948
  33. Fulda S (2016) Regulation of necroptosis signaling and cell death by reactive oxygen species. Biol Chem 397, 657-660
  34. Galluzzi L and Kroemer G (2008) Necroptosis: a specialized pathway of programmed necrosis. Cell 135, 1161-1163 https://doi.org/10.1016/j.cell.2008.12.004
  35. Liu C, Zhang K, Shen H, Yao X, Sun Q and Chen G (2018) Necroptosis: A novel manner of cell death, associated with stroke (Review). Int J Mol Med 41, 624-630
  36. Benedict CA, Norris PS, Prigozy TI et al (2001) Three adenovirus E3 proteins cooperate to evade apoptosis by tumor necrosis factor-related apoptosis-inducing ligand receptor-1 and -2. J Biol Chem 276, 3270-3278 https://doi.org/10.1074/jbc.M008218200
  37. Nichols DB, De Martini W and Cottrell J (2017) Poxviruses Utilize Multiple Strategies to Inhibit Apoptosis. Viruses 9
  38. Jerome KR, Fox R, Chen Z, Sears AE, Lee H and Corey L (1999) Herpes simplex virus inhibits apoptosis through the action of two genes, Us5 and Us3. J Virol 73, 8950-8957
  39. Lu JV, Weist BM, van Raam BJ et al (2011) 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 U S A 108, 15312-15317 https://doi.org/10.1073/pnas.1102779108
  40. Wang YQ, Wang L, Zhang MY et al (2012) Necrostatin-1 suppresses autophagy and apoptosis in mice traumatic brain injury model. Neurochem Res 37, 1849-1858 https://doi.org/10.1007/s11064-012-0791-4
  41. Xu X, Chua CC, Kong J et al (2007) Necrostatin-1 protects against glutamate-induced glutathione depletion and caspase-independent cell death in HT-22 cells. J Neurochem 103, 2004-2014 https://doi.org/10.1111/j.1471-4159.2007.04884.x
  42. Zhu S, Zhang Y, Bai G and Li H (2011) Necrostatin-1 ameliorates symptoms in R6/2 transgenic mouse model of Huntington's disease. Cell Death Dis 2, e115 https://doi.org/10.1038/cddis.2010.94
  43. Re DB, Le Verche V, Yu C et al (2014) Necroptosis drives motor neuron death in models of both sporadic and familial ALS. Neuron 81, 1001-1008 https://doi.org/10.1016/j.neuron.2014.01.011
  44. Murakami Y, Matsumoto H, Roh M et al (2014) Programmed necrosis, not apoptosis, is a key mediator of cell loss and DAMP-mediated inflammation in dsRNAinduced retinal degeneration. Cell Death Differ 21, 270-277 https://doi.org/10.1038/cdd.2013.109
  45. Veyer DL, Carrara G, Maluquer de Motes C and Smith GL (2017) Vaccinia virus evasion of regulated cell death. Immunol Lett 186, 68-80 https://doi.org/10.1016/j.imlet.2017.03.015
  46. Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L and Sad S (2012) Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat Immunol 13, 954-962 https://doi.org/10.1038/ni.2397
  47. Sridharan H and Upton JW (2014) Programmed necrosis in microbial pathogenesis. Trends Microbiol 22, 199-207 https://doi.org/10.1016/j.tim.2014.01.005
  48. Kaminskyy V and Zhivotovsky B (2010) To kill or be killed: how viruses interact with the cell death machinery. J Intern Med 267, 473-482 https://doi.org/10.1111/j.1365-2796.2010.02222.x
  49. Lin J, Li H, Yang M et al (2013) A role of RIP3-mediated macrophage necrosis in atherosclerosis development. Cell Rep 3, 200-210 https://doi.org/10.1016/j.celrep.2012.12.012
  50. Han W, Li L, Qiu S et al (2007) Shikonin circumvents cancer drug resistance by induction of a necroptotic death. Mol Cancer Ther 6, 1641-1649 https://doi.org/10.1158/1535-7163.MCT-06-0511
  51. Alameda JP, Moreno-Maldonado R, Navarro M et al (2010) An inactivating CYLD mutation promotes skin tumor progression by conferring enhanced proliferative, survival and angiogenic properties to epidermal cancer cells. Oncogene 29, 6522-6532 https://doi.org/10.1038/onc.2010.378
  52. Yang Y, Hu W, Feng S, Ma J and Wu M (2005) RIP3 beta and RIP3 gamma, two novel splice variants of receptor-interacting protein 3 (RIP3), downregulate RIP3-induced apoptosis. Biochem Biophys Res Commun 332, 181-187 https://doi.org/10.1016/j.bbrc.2005.04.114
  53. Wu W, Liu P and Li J (2012) Necroptosis: an emerging form of programmed cell death. Crit Rev Oncol Hematol 82, 249-258 https://doi.org/10.1016/j.critrevonc.2011.08.004
  54. Oliver Metzig M, Fuchs D, Tagscherer KE, Grone HJ, Schirmacher P and Roth W (2016) Inhibition of caspases primes colon cancer cells for 5-fluorouracil-induced TNF-alpha-dependent necroptosis driven by RIP1 kinase and NF-kappaB. Oncogene 35, 3399-3409 https://doi.org/10.1038/onc.2015.398
  55. Najafov A, Chen H and Yuan J (2017) Necroptosis and Cancer. Trends Cancer 3, 294-301 https://doi.org/10.1016/j.trecan.2017.03.002
  56. Wu W, Zhu H, Fu Y et al (2014) Clinical significance of down-regulated cylindromatosis gene in chronic lymphocytic leukemia. Leuk Lymphoma 55, 588-594 https://doi.org/10.3109/10428194.2013.809077
  57. Feng X, Song Q, Yu A, Tang H, Peng Z and Wang X (2015) Receptor-interacting protein kinase 3 is a predictor of survival and plays a tumor suppressive role in colorectal cancer. Neoplasma 62, 592-601 https://doi.org/10.4149/neo_2015_071
  58. Ruan J, Mei L, Zhu Q, Shi G and Wang H (2015) Mixed lineage kinase domain-like protein is a prognostic biomarker for cervical squamous cell cancer. Int J Clin Exp Pathol 8, 15035-15038