Mechanisms of programmed cell death: structural and functional pathways. A narrative review.
Mecanismos de muerte celular programada: vías estructurales y funcionales. Una revisión narrativa.
Palabras clave:
apoptosis, caspasas, vía mitocondrial/intrínseca, vía extrínseca, necroptosis, autofagia
Resumen
La apoptosis, la necroptosis y la autofagia son mecanismos celulares mediante los cuales las células se programan para morir bajo una amplia gama de estímulos fisiológicos. Esta revisión describe en los sistemas de muerte celular programada dependientes e independientes de la caspasa. Los estudios incluidos sobre la muerte celular programada dependiente de la caspasa incluyen mecanismos apoptóticos de la vía extrínseca que incluyen fosfatidilserina (PS), FAS (APO-1/CD95), receptor del factor de necrosis tumoral (FNT) tipo 1 (FNT-R1) e inductor de la apoptosis relacionada con ligando FNT (TRAIL) y vía intrínseca o mitocondrial como el citocromo C, la familia de proteínas Bcl-2 y Smac/Diablo. La familia Bcl-2 tiene mediadores apoptóticos, proteína X asociada a Bcl-2 (Bax) y antagonista/asesino homólogo de Bcl-2 (Bak), proteína BIM que interactúa con Bcl-2 (Bim), agonista de la muerte celular de Bcl-2 (Bad), Bid, proteína 1 que interactúa con el adenovirus E1B 19kDa de Bcl-2, NIP3 (Bnip3), BMF, HRK, Noxa y PUMA y proteínas antiapoptóticas como la propia Bcl-2, Mcl-1, Bcl-w, A1 y Bcl-XL. Además, las vías de muerte celular programada independientes de la caspasa incluyen la vía mitocondrial con los mediadores proteicos factor inductor de apoptosis (FIA) y endonucleasa G, las vías necroptosis y autofagia. Comprender la muerte celular programada a partir de los contenidos descritos en esta revisión podría arrojar luz sustancial sobre los procesos de la homeostasis biológica y podría proporcionar la capacidad de modular la respuesta de muerte celular programada y conducir a nuevas intervenciones terapéuticas en una amplia gama de enfermedades.
Descargas
La descarga de datos todavía no está disponible.
Citas
Danial NN, Korsmeyer SJ. Cell Death: Critical control points. Cell 2004;116(2): 205-219. Doi: 10.1016/s0092-8674(04)00046-7
Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell 2011;147(4): 742-758. Doi: 10.1016/j.cell.2011.10.033
Božič B, Rozman B. Apoptosis and autoimmunity. EJIFCC 2006;17(3): 69-74. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5938681/pdf/eji-fcc-17-069.pdf
Marchal JA, Lopez GJ, Peran M, Comino A, Delgado JR, García-García JA, Conde V, Aranda FM, Rivas C, Esteban M, Garcia MA. The impact of PKR activation: from neurodegeneration to cancer. FASEB J 2014;28(5): 1965-1974. Doi: 10.1096/fj.13-248294
Li K, Wu D, Chen X, Zhang T, Zhang L, Yi Y, Miao Z, Jin N, Bi X, Wang H, Xu J, Wang D. Current and emerging biomarkers of cell death in human disease. Bio-med Res Int 2014;2014: 690103. Doi: 10.1155/2014/690103
Galluzzi L, Vanden Berghe T, Vanlangenakker N, Buettner S, Eisenberg T, Vandenabeele P, Madeo F, Kroemer G. Programmed necrosis from molecules to health and disease. Int Rev Cell Mol Biol 2011;289: 1-35. Doi: 10.1016/B978-0-12-386039-2.00001-8
Elmore S. Apoptosis: A review of programmed cell death. Toxicol Pathol 2007;35(4): 495-516. Doi: 10.1080/01926230701320337.
Kerr JFR, Wyllie AH, Currie AR. Apoptosis: A basic biological phenomenon with wideranging implications in tissue kinetics. Br J Cancer 1972;26(4): 239-257. Doi: 10.1038/bjc.1972.33
Yuan J, Kroemer G. Alternative cell death mechanisms in development and beyond. Genes Dev 2010;24(23): 2592-2602. Doi: 10.1101/gad.1984410
Rowan S, Fisher DE. Mechanisms of apoptotic cell death. Leukemia 1997;11(4): 457-465. Doi: 10.1038/sj.leu.2400626
Zhou JX, Li X [Eds.]. Apoptosis in Polycystic Kidney Disease: From Pathogenesis to Treatment. In: Polycystic Kidney Disease [Internet]. Brisbane (AU): Exon Publications; 2015. Chapter 9: 197-230. Doi: 10.15586/codon.pkd.2015.ch9
Strasser A, O’Connor L, Dixit VM. Apoptosis Signaling. Annu Rev Biochem 2000;69: 217-245. Doi: 10.1146/annurev.biochem.69.1.217
Martelli AM, Zweyer M, Ochs RL, Tazzari PL, Tabellini G, Narducci P, Bortul R. Nuclear apoptotic changes: an overview. J Cell Biochem 2001;82(4): 634-646. Doi: 10.1002/jcb.1186
Vitale I, Pietrocola F, Guilbaud E, Aaronson SA, Abrams JM, Adam D, Agostini M, Agostinis P, Alnemri ES, Galluzzi L. Apoptotic cell death in disease—Current understanding of the NCCD 2023. Cell Death Differ 2023;30(5): 1097-1154. Doi: 10.1038/s41418-023-01153-w
Arandjelovic S, Ravichandran KS. Phagocytosis of apoptotic cells in homeostasis. Nat Immunol 2015;16(9): 907-917. Doi: 10.1038/ni.3253
Abraham MC, Shaham S. Death without caspases, caspases without death. Trends Cell Biol 2004;14(4): 184-193. Doi: 10.10 16/j.tcb.2004.03.002
Thornberry NA, Lazebnik Y. Caspases: enemies within. Science 1998;281(5381): 1312-1316. Doi: 10.1126/science.281.53 81.1312
Testa U, Riccioni R. Deregulation of apoptosis in acute myeloid leukemia. Haematologica 2007;92(1): 81-89. Doi: 10.3324/haematol.10279
Thornberry NA. Caspases: A decade of death research. Cell Death Differ 1999;6(11): 1023-1027. Doi: 10.1038/sj.cdd.4400607
Ouyang L, Shi Z, Zhao S, Wang FT, Zhou TT, Liu B, Bao JK. Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis. Cell Prolif 2012;45(6): 487-498. Doi: 10.1111/j.1365-2184.2012.00845.x
Schimmer AD, Dalili S, Batey RA, Riedl SJ. Targeting XIAP for the treatment of malignancy. Cell Death Differ 2006;13(2): 179-188. Doi: 10.1038/sj.cdd.4401826
Lens SM, Wolthuis RM, Klompmaker R, Kauw J, Agami R, Brummelkamp T, Kops G, Medema RH. Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension. EMBO J 2003;22(12): 2934-2947. Doi: 10.1093/emboj/cdg307
Carvalho A, Carmena M, Sambade C, Earnshaw WC, Wheatley SP. Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 2003;116(Pt 14): 2987-2998. Doi: 10.1242/jcs.00612
Altieri DC. New wirings in the survivin networks. Oncogene 2008;27(48): 6276-6284. Doi: 10.1038/onc.2008.303
Tamm I, Richter S, Oltersdorf D, Creutzig U, Harbott J, Scholz F, Karawajew L, Ludwig WD, Wuchter C. High expression levels of X-Linked inhibitor of apoptosis protein and survivin correlate with poor overall survival in childhood de novo acute myeloid leukemia. Clin Cancer Res 2004;10(11): 3737-3744. Doi: 10.1158/1078-0432.CCR-03-0642
Schimmer AD. Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res 2004;64(20): 7183-7190. Doi: 10.1158/0008-5472.CAN-04-1918
Chawla-Sarkar M, Bae SI, Reu FJ, Jacobs BS, Lindner DJ, Borden EC. Down-regulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ 2004;11(8): 915-923. Doi: 10.1038/sj.cdd.4401416
Huang Y, Lu M, Wu H. Antagonizing XIAP- mediated caspase-3 inhibition: Achilles’ heel of cancers? Cancer Cell 2004;5(1): 1-2. Doi: 10.1016/s1535-6108(03)00340-4
Tsuruo T, Naito M, Tomida A, Fujita N, Mashima T, Sakamoto H, Haga N. Molecular targeting therapy of cancer: drug resistance, apoptosis and survival signal. Cancer Sci. 2003;94(1):15-21. Doi: 10.1111/j.1349-7006.2003.tb01345.x.
Eimon PM, Kratz E, Varfolomeev E, Hymowitz SG, Stern H, Zha J, Ashkenazi A. Delineation of the cell-extrinsic apoptosis pathway in the zebrafish. Cell Death Differ 2006;13(10): 1619-1630. Doi: 10.1038/
sj.cdd.4402015.
Diaz Arguello OA, Haisma HJ. Apoptosis-inducing TNF superfamily ligands for cancer therapy. Cancers (Basel) 2021;13(7): 1543. Doi: 10.3390/cancers13071543
Schutters K, Kusters DH, Chatrou ML, Montero-Melendez T, Donners M, Deckers NM, Krysko DV, Vandenabeele P, Perretti M, Schurgers LJ, Reutelingsperger CPM. Cell surface-expressed phosphatidylserine as therapeutic target to enhance phagocytosis of apoptotic cells. Cell Death Differ 2013;20(1): 49-56. Doi: 10.1038/ cdd.2012.107
Tran SEF, Meinander A, Eriksson JE. Instant decisions: transcription-independent control of death-receptor-mediated apoptosis. Trends Biochem Sci 2004;29(11): 601-608. Doi: 10.1016/j.tibs.2004.09.009
Fernández-Lázaro D. Comparative pre-clinical analysis of the efficacy, mechanism of action and resistance mechanisms of two immunomodulatory drugs (IMIDS), lenalidomide and pomalidomide, in multiple myeloma. Doctoral Thesis. University of de Salamanca. 2011. Available from: https://gredos.usal.es/bitstream/handle/10366/110661/DME_Fernandez_Lazaro_D_Analisis_preclinico.pdf?sequence=1&isAllowed=y
Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998;281(5381): 1305-1308. Doi: 10.1126/science.281.5381.1305
Volpe E, Sambucci M, Battistini L, Borsellino G. Fas-fas ligand: Checkpoint of T cell functions in multiple sclerosis. Front Immunol 2016;7: 217466. Doi: 10.3389/fimmu.2016.00382
Fernández-Lázaro D, Fernández-Lázaro CI, Caballero García A, Córdova Martínez A. Immunomodulatory agents (IMiDs): tools for the treatment of multiple myeloma. Rev Med Chil 2018;146(12): 1444-1451. Available from: Doi: https:// www.scielo.cl/scielo.php?script=sci_ arttext&pid= S0034-98872018001201444
Boatright KM, Deis C, Denault JB, Sutherlin DP, Salvesen GS. Activation of caspases-8 and 10 by FLIPL. Biochem J2004;382(Pt 2): 651-657. Doi: 10.1042/ BJ20040809
Mahdizadeh SJ, Thomas M, Eriksson LA. Reconstruction of the Fas-based death-inducing signaling complex (DISC) using a protein-protein docking meta-approach. J Chem Inf Model 2021;61(7): 3543-3558. Doi: 10.1021/acs.jcim.1c00301
Martínez-Reza I, Díaz L, García-Becerra R. Preclinical and clinical aspects of TNF-α and its receptors TNFR1 and TNFR2 in breast cancer. J Biomed Sci 2017;24(1): 90. Doi: 10.1186/s12929-017-0398-9
Harper N, Hughes M, MacFarlane M, Cohen GM. Fas-associated death domain protein and caspase-8 are not recruited to the tumor necrosis factor receptor 1 signaling complex during tumor necrosis factor-induced apoptosis. J Biol Chem 2003;278(28): 25534-25541. Doi: 10.1074/jbc.M303399200
Iordanov MS, Kirsch JD, Ryabinina OP, Wong J, Spitz PN, Korcheva VB, Thorburn A, Magun BE. Recruitment of TRADD, FADD, and caspase 8 to double-stranded RNA-triggered death inducing signaling complexes (dsRNA-DISCs). Apoptosis 2005:10(1): 167-176. Doi: 10.1007/ s10495-005-6071-x
Bodmer JL, Meier P, Tschopp J, Schneider P. Cysteine 230 is essential for the structure and activity of the cytotoxic ligand TRAIL. J Biol Chem 2000;275(27): 20632-20637. Doi: 10.1074/jbc.M909721199
Lemke J, Von Karstedt S, Zinngrebe J, Walczak H. Getting TRAIL back on track for cancer therapy. Cell Death Differ 2014;21(9): 1350-1364. Doi: 10.1038/ cdd.2014.81.
Zhang Y, Zhang B. TRAIL resistance of breast cancer cells is associated with constitutive endocytosis of death receptors 4 and 5. Mol Cancer Res 2008(12);6: 1861-1871. Doi: 10.1158/1541-7786.MCR-08-0313
Huang Y, Sheikh MS. TRAIL death receptors and cancer therapeutics. Toxicol Appl Pharmacol 2007;224(3): 284-289. Doi: 10.1016/j.taap.2006.12.007
Danish L, Stöhr D, Scheurich P, Pollak N. TRAIL -R3/R4 and Inhibition of TRAIL Signalling in Cancer. [Part of the Resistance to Targeted Anti-Cancer Therapeutics book series (RTACT, vol.12)] Springer, Cham 2017;12: 27-57. Available from: https://link.springer.com/chapter/10.1007/978-3-319-56805-8_2
Boyce BF, Xing L. Biology of RANK, RANKL, and osteoprotegerin. Arthritis Res Ther 2007;9(Suppl 1): S1. Doi: 10.1186/ar2165.
Van Aken O. Mitochondria and Cell Death. Annu Plant Rev 2018;50: 343-372. Doi: https://doi.org/10.1002/9781119312994. apr0553.
Ravagnan L, Roumier T, Kroemer G. Mitochondria, the killer organelles and their weapons. J Cell Physiol 2002;192(2): 131-137. Doi: 10.1002/jcp.10111
D´Arcy MS. Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol Int 2019;43(6): 582-592. Doi: 10.1002/cbin.11137
Cai J, Yang J, Jones DP. Mitochondrial control of apoptosis: the role of cytochrome c. Biochim Biophys Acta 1998;1366(1- 2): 139-149. Doi: 10.1016/s0005-2728(98)00109-1
Jiang X, Wang X. Cytochrome C-mediated apoptosis. Annu Rev Biochem 2004;73: 87-106. Doi: 10.1146/annurev.biochem.73.011303.073706
Singh R, Letai A, Sarosiek K. Regulation of apoptosis in health and disease: the balancing act of BCL -2 family proteins. Nat Rev Mol Cell Biol 2019;20(3): 175-193. Doi: 10.1038/s41580-018-0089-8
Ramírez-García M, Márquez-González H, Barranco-Lampón G, Enrique López-Aguilar J. Bcl-2: its role in the cell cycle, apoptosis and cancer. Residente 2014;9(3): 84-94.
Czabotar PE, Garcia-Saez AJ. Mechanisms of BCL -2 family proteins in mitochondrial apoptosis. Nat Rev Mol Cell Biol 2023;24(10): 732-748. Doi: 10.1038/ s41580-023-00629-4
Fernández-Lazaro D. Biological and molecular bases in the development of pathogenesis in multiple myeloma disease. Invest Clin 2019;60(3): 247-264. Doi: https:// doi.org/10.22209/IC.v60n3a07
Colado E, Paíno T, Maiso P, Ocio EM, Chen X, Álvarez-Fernández S, Gutiérrez NC, Martín-Sánchez J, Flores-Montero J, San Segundo L, Garayoa M, Fernández-Lázaro D, Vidriales MB, Galmarini CM, Avilés P, Cuevas C, Pandiella A, San-Miguel JF. Zalypsis has in vitro activity in acute myeloid blasts and leukemic progenitor cells through the induction of a DNA damage response. Haematologica 2011;96(5): 687-695. Doi: 10.3324/hae- matol.2010.036400
Maiso P, Colado E, Ocio EM, Garayoa M, Martín J, Atadja P, Pandiella A, San-Miguel JF. The synergy of panobinostat plus doxorubicin in acute myeloid leukemia suggests a role for HDAC inhibitors in the control of DNA repair. Leukemia 2009;23(12): 2265-2274. Doi: 10.1038/ leu.2009.182
Anvekar RA, Asciolla JJ, Missert DJ, Chipuk JE. Born to be alive: a role for the BCL -2 family in melanoma tumor cell survival, apoptosis, and treatment. Front Oncol 2011;1(34): 34. Doi: 10.3389/ fonc.2011.00034
Garner TP, Lopez A, Reyna DE, Spitz AZ, Gavathiotis E. Progress in targeting the BCL -2 family of proteins. Curr Opin Chem Biol 2017;39: 133-142. Doi: 10.1016/j. cbpa.2017.06.014
Kastan MB. A BID for the pathway. Nature 2005;437(7062):1103. Doi: 10.1038/ 4371103a
Omonosova E, Hinnadurai G. BH3-only proteins in apoptosis and beyond: an overview. Oncogene 2008;27(Suppl 1): S2-S19. Doi: 10.1038/onc.2009.39
Klee M, Pallauf K, Alcalá S, Fleischer A, Pimentel-Muĩos FX. Mitochondrial apoptosis induced by BH3-only molecules in the exclusive presence of endoplasmic reticular Bak. EMBO J 2009;28(12): 1757-1568. Doi: 10.1038/emboj.2009.90
Wei MC, Zong WX, Cheng EHY, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. Proapoptotic BAX, and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001;292(5517): 727-730. Doi: 10.1126/science.1059108
Wilkinson JC, Wilkinson AS, Scott FL, Csomos RA, Salvesen GS, Duckettt CS. Neutralization of Smac/Diablo by inhibitors of apoptosis (IAPs). A caspase independent mechanism for apoptotic inhibition. J Biol Chem 2004;279(49): 51082-51090. Doi: 10.1074/jbc.M408655200
Sun XM, Bratton SB, Butterworth M, MacFarlane M, Cohen GM. Bcl-2 and Bcl-xL inhibit CD95-mediated apoptosis by preventing mitochondrial release of Smac/ DIABLO and subsequent inactivation of X-linked inhibitor-of-apoptosis protein. J Biol Chem 2002;277(13): 11345-11351. Doi: 10.1074/jbc.M109893200
Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F, Youle RJ. Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J 2003;22(17): 4385-4399. Doi: 10.1093/emboj/cdg423
Candé C, Cecconi F, Dessen P, Kroemer G. Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J Cell Sci 2002;115(Pt 24): 4727-4734. Doi: 10.1242/jcs.00210
Kroemer G, Martin SJ. Caspase-independent cell death. Nat Med 2005;11(7): 725- 730. Doi: 10.1038/nm1263
Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001;412(6842):95-99. Doi: 10.1038/35083620
Van Loo G, Schotte P, Van Gurp M, Demol H, Hoorelbeke B, Gevaert K, Rodriguez I, Ruiz-Carrillo A, Vandekerckhove J, Declercq W, Beyaert R, Vandenabeele P. Endonuclease G: a mitochondrial protein released in apoptosis and involved in caspase independent DNA degradation. Cell Death Differ 2001;8(12): 1136-1142. Doi: 10.1038/sj.cdd.4400944
Wu W, Liu P, Li J. Necroptosis: an emerging form of programmed cell death. Crit Rev Oncol Hematol 2012;82(3): 249-258. Doi: 10.1016/j.critrevonc.2011.08.004
Galluzzi L, Vanden Berghe T, Vanlangenakker N, Buettner S, Eisenberg T, Vandenabeele P, Madeo F, Kroemer G. Programmed necrosis from molecules to health and disease. Int Rev Cell Mol Biol 2011;289: 1-35. Doi: 10.1016/B978-0-12-386039-2.00001-8
Günther C, Martini E, Wittkopf N, Amann K, Weigmann B, Neumann H, Waldner MJ, Hedrick SM, Tenzer S, Neurath MF, Becker C. Caspase-8 regulates TNF-α-induced epithelial necroptosis and terminal ileitis. Nature 2011;477(7364): 335-339. Doi:10.1038/nature10400
Duprez L, Takahashi N, Van Hauwermeiren F, Vandendriessche B, Goossens V, Vanden Berghe T, Declercq W, Libert C, Cauwels A, Vandenabeele P. RIP kinase dependent necrosis drives lethal systemic inflammatory response syndrome. Immunity 2011;35(6): 908-918. Doi: 10.1016/j immuni.2011.09.020
McNamara CR, Ahuja R, Osafo-Addo AD, Barrows D, Kettenbach A, Skidan I, Teng X, Cuny GD, Gerber S, Degterev A. Akt Regulates TNFα synthesis downstream of RIP1 kinase activation during necroptosis. PLoS One 2013;8(3): e56576. Doi:10.1371/journal.pone.0056576.
Wajant H, Siegmund D. TNFR1 and TNFR2 in the control of the life and death balance of macrophages. Front Cell Dev Biol 2019;7: 91. Doi: 10.3389/fcell.2019.00091
Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009;137(6): 1112-1123. Doi: 10.1016/j. cell.2009.05.037
Giampietri C, Starace D, Petrungaro S, Filippini A, Ziparo E. Necroptosis: molecular signalling and translational implications. Int J Cell Biol 2014;2014: 49027. Doi: 10.1155/2014/490275
Liu Q, Qiu J, Liang M, Golinski J, Van Leyen K, Jung JE, You Z, Lo EH, Degterev A, Whalen MJ. Akt and mTOR mediate programmed necrosis in neurons. Cell Death Dis 2014;5(2): e1084. Doi: 10.1038/cddis.2014.69.
Dondelinger Y, Declercq W, Montessuit S, Roelandt R, Goncalves A, Bruggeman I, Hulpiau P, Weber K, Sehon CA, Marquis RW, Bertin J, Gough PJ, Savvides S, Martinou JC, Bertrand MJ, Vandenabeele P. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep 2014;7(4): 971-981. Doi: 10.1016/j.celrep.2014.04.026
Uchiyama Y, Shibata M, Koike M, Yoshimura K, Sasaki M. Autophagy–physiolo- gy and pathophysiology. Histochem Cell Biol 2008;129(4): 407-420. Doi: 10.1007/ s00418-008-0406-y
Mizushima N and Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011;147(4): 728-741. Doi: 10.1016/j. cell.2011.10.026
Lindqvist LM, Heinlein M, Huang DCS, Vaux DL. Prosurvival Bcl-2 family members affect autophagy only indirectly, by inhibiting Bax and Bak. Proc Natl Acad Sci U S A 2014;111(23): 8512-8517. Doi: 10.1073/ pnas.1406425111
Klionsky DJ, Petroni G, Amaravadi RK, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM, Cadwell K, Cecconi F, Pietrocola F. Autophagy in major human diseases. EMBO J 2021;40(19): e108863. Doi: 10.15252/embj.2021108863
Choi AMK, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med 2013;368(7): 651-662. Doi: 10.1056/ NEJMra1205406
Hale AN, Ledbetter DJ, Gawriluk TR, Rucker EB. Autophagy: regulation and role in development. Autophagy 2013;9(7): 951-972. Doi: 10.4161/auto.24273
Cheng Y, Ren X, Hait WN, Yang JM. Therapeutic targeting of autophagy in disease: biology and pharmacology. Pharmacol Rev 2013;65(4): 1162-1197. Doi: 10.1124/ pr.112.007120
Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011;7(3): 279-296. Doi: 10.4161/auto.7.3.14487
Ryter SW, Mizumura K, Choi AMK. The impact of autophagy on cell death modalities. Int J Cell Biol 2014;2014: 502676. Doi: 10.1155/2014/502676
Kwanten WJ, Martinet W, Michielsen PP, Francque SM. Role of autophagy in the pathophysiology of nonalcoholic fatty liver disease: a controversial issue. World J Gastroenterol 2014;20(23): 7325-7338. Doi: 10.3748/wjg.v20.i23.7325
Ding WX, Yin XM. Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol Chem 2012;393(7): 547-564. Doi: 10.1515/hsz-2012-0119
Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell 2011;147(4): 742-758. Doi: 10.1016/j.cell.2011.10.033
Božič B, Rozman B. Apoptosis and autoimmunity. EJIFCC 2006;17(3): 69-74. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5938681/pdf/eji-fcc-17-069.pdf
Marchal JA, Lopez GJ, Peran M, Comino A, Delgado JR, García-García JA, Conde V, Aranda FM, Rivas C, Esteban M, Garcia MA. The impact of PKR activation: from neurodegeneration to cancer. FASEB J 2014;28(5): 1965-1974. Doi: 10.1096/fj.13-248294
Li K, Wu D, Chen X, Zhang T, Zhang L, Yi Y, Miao Z, Jin N, Bi X, Wang H, Xu J, Wang D. Current and emerging biomarkers of cell death in human disease. Bio-med Res Int 2014;2014: 690103. Doi: 10.1155/2014/690103
Galluzzi L, Vanden Berghe T, Vanlangenakker N, Buettner S, Eisenberg T, Vandenabeele P, Madeo F, Kroemer G. Programmed necrosis from molecules to health and disease. Int Rev Cell Mol Biol 2011;289: 1-35. Doi: 10.1016/B978-0-12-386039-2.00001-8
Elmore S. Apoptosis: A review of programmed cell death. Toxicol Pathol 2007;35(4): 495-516. Doi: 10.1080/01926230701320337.
Kerr JFR, Wyllie AH, Currie AR. Apoptosis: A basic biological phenomenon with wideranging implications in tissue kinetics. Br J Cancer 1972;26(4): 239-257. Doi: 10.1038/bjc.1972.33
Yuan J, Kroemer G. Alternative cell death mechanisms in development and beyond. Genes Dev 2010;24(23): 2592-2602. Doi: 10.1101/gad.1984410
Rowan S, Fisher DE. Mechanisms of apoptotic cell death. Leukemia 1997;11(4): 457-465. Doi: 10.1038/sj.leu.2400626
Zhou JX, Li X [Eds.]. Apoptosis in Polycystic Kidney Disease: From Pathogenesis to Treatment. In: Polycystic Kidney Disease [Internet]. Brisbane (AU): Exon Publications; 2015. Chapter 9: 197-230. Doi: 10.15586/codon.pkd.2015.ch9
Strasser A, O’Connor L, Dixit VM. Apoptosis Signaling. Annu Rev Biochem 2000;69: 217-245. Doi: 10.1146/annurev.biochem.69.1.217
Martelli AM, Zweyer M, Ochs RL, Tazzari PL, Tabellini G, Narducci P, Bortul R. Nuclear apoptotic changes: an overview. J Cell Biochem 2001;82(4): 634-646. Doi: 10.1002/jcb.1186
Vitale I, Pietrocola F, Guilbaud E, Aaronson SA, Abrams JM, Adam D, Agostini M, Agostinis P, Alnemri ES, Galluzzi L. Apoptotic cell death in disease—Current understanding of the NCCD 2023. Cell Death Differ 2023;30(5): 1097-1154. Doi: 10.1038/s41418-023-01153-w
Arandjelovic S, Ravichandran KS. Phagocytosis of apoptotic cells in homeostasis. Nat Immunol 2015;16(9): 907-917. Doi: 10.1038/ni.3253
Abraham MC, Shaham S. Death without caspases, caspases without death. Trends Cell Biol 2004;14(4): 184-193. Doi: 10.10 16/j.tcb.2004.03.002
Thornberry NA, Lazebnik Y. Caspases: enemies within. Science 1998;281(5381): 1312-1316. Doi: 10.1126/science.281.53 81.1312
Testa U, Riccioni R. Deregulation of apoptosis in acute myeloid leukemia. Haematologica 2007;92(1): 81-89. Doi: 10.3324/haematol.10279
Thornberry NA. Caspases: A decade of death research. Cell Death Differ 1999;6(11): 1023-1027. Doi: 10.1038/sj.cdd.4400607
Ouyang L, Shi Z, Zhao S, Wang FT, Zhou TT, Liu B, Bao JK. Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis. Cell Prolif 2012;45(6): 487-498. Doi: 10.1111/j.1365-2184.2012.00845.x
Schimmer AD, Dalili S, Batey RA, Riedl SJ. Targeting XIAP for the treatment of malignancy. Cell Death Differ 2006;13(2): 179-188. Doi: 10.1038/sj.cdd.4401826
Lens SM, Wolthuis RM, Klompmaker R, Kauw J, Agami R, Brummelkamp T, Kops G, Medema RH. Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension. EMBO J 2003;22(12): 2934-2947. Doi: 10.1093/emboj/cdg307
Carvalho A, Carmena M, Sambade C, Earnshaw WC, Wheatley SP. Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 2003;116(Pt 14): 2987-2998. Doi: 10.1242/jcs.00612
Altieri DC. New wirings in the survivin networks. Oncogene 2008;27(48): 6276-6284. Doi: 10.1038/onc.2008.303
Tamm I, Richter S, Oltersdorf D, Creutzig U, Harbott J, Scholz F, Karawajew L, Ludwig WD, Wuchter C. High expression levels of X-Linked inhibitor of apoptosis protein and survivin correlate with poor overall survival in childhood de novo acute myeloid leukemia. Clin Cancer Res 2004;10(11): 3737-3744. Doi: 10.1158/1078-0432.CCR-03-0642
Schimmer AD. Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res 2004;64(20): 7183-7190. Doi: 10.1158/0008-5472.CAN-04-1918
Chawla-Sarkar M, Bae SI, Reu FJ, Jacobs BS, Lindner DJ, Borden EC. Down-regulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ 2004;11(8): 915-923. Doi: 10.1038/sj.cdd.4401416
Huang Y, Lu M, Wu H. Antagonizing XIAP- mediated caspase-3 inhibition: Achilles’ heel of cancers? Cancer Cell 2004;5(1): 1-2. Doi: 10.1016/s1535-6108(03)00340-4
Tsuruo T, Naito M, Tomida A, Fujita N, Mashima T, Sakamoto H, Haga N. Molecular targeting therapy of cancer: drug resistance, apoptosis and survival signal. Cancer Sci. 2003;94(1):15-21. Doi: 10.1111/j.1349-7006.2003.tb01345.x.
Eimon PM, Kratz E, Varfolomeev E, Hymowitz SG, Stern H, Zha J, Ashkenazi A. Delineation of the cell-extrinsic apoptosis pathway in the zebrafish. Cell Death Differ 2006;13(10): 1619-1630. Doi: 10.1038/
sj.cdd.4402015.
Diaz Arguello OA, Haisma HJ. Apoptosis-inducing TNF superfamily ligands for cancer therapy. Cancers (Basel) 2021;13(7): 1543. Doi: 10.3390/cancers13071543
Schutters K, Kusters DH, Chatrou ML, Montero-Melendez T, Donners M, Deckers NM, Krysko DV, Vandenabeele P, Perretti M, Schurgers LJ, Reutelingsperger CPM. Cell surface-expressed phosphatidylserine as therapeutic target to enhance phagocytosis of apoptotic cells. Cell Death Differ 2013;20(1): 49-56. Doi: 10.1038/ cdd.2012.107
Tran SEF, Meinander A, Eriksson JE. Instant decisions: transcription-independent control of death-receptor-mediated apoptosis. Trends Biochem Sci 2004;29(11): 601-608. Doi: 10.1016/j.tibs.2004.09.009
Fernández-Lázaro D. Comparative pre-clinical analysis of the efficacy, mechanism of action and resistance mechanisms of two immunomodulatory drugs (IMIDS), lenalidomide and pomalidomide, in multiple myeloma. Doctoral Thesis. University of de Salamanca. 2011. Available from: https://gredos.usal.es/bitstream/handle/10366/110661/DME_Fernandez_Lazaro_D_Analisis_preclinico.pdf?sequence=1&isAllowed=y
Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998;281(5381): 1305-1308. Doi: 10.1126/science.281.5381.1305
Volpe E, Sambucci M, Battistini L, Borsellino G. Fas-fas ligand: Checkpoint of T cell functions in multiple sclerosis. Front Immunol 2016;7: 217466. Doi: 10.3389/fimmu.2016.00382
Fernández-Lázaro D, Fernández-Lázaro CI, Caballero García A, Córdova Martínez A. Immunomodulatory agents (IMiDs): tools for the treatment of multiple myeloma. Rev Med Chil 2018;146(12): 1444-1451. Available from: Doi: https:// www.scielo.cl/scielo.php?script=sci_ arttext&pid= S0034-98872018001201444
Boatright KM, Deis C, Denault JB, Sutherlin DP, Salvesen GS. Activation of caspases-8 and 10 by FLIPL. Biochem J2004;382(Pt 2): 651-657. Doi: 10.1042/ BJ20040809
Mahdizadeh SJ, Thomas M, Eriksson LA. Reconstruction of the Fas-based death-inducing signaling complex (DISC) using a protein-protein docking meta-approach. J Chem Inf Model 2021;61(7): 3543-3558. Doi: 10.1021/acs.jcim.1c00301
Martínez-Reza I, Díaz L, García-Becerra R. Preclinical and clinical aspects of TNF-α and its receptors TNFR1 and TNFR2 in breast cancer. J Biomed Sci 2017;24(1): 90. Doi: 10.1186/s12929-017-0398-9
Harper N, Hughes M, MacFarlane M, Cohen GM. Fas-associated death domain protein and caspase-8 are not recruited to the tumor necrosis factor receptor 1 signaling complex during tumor necrosis factor-induced apoptosis. J Biol Chem 2003;278(28): 25534-25541. Doi: 10.1074/jbc.M303399200
Iordanov MS, Kirsch JD, Ryabinina OP, Wong J, Spitz PN, Korcheva VB, Thorburn A, Magun BE. Recruitment of TRADD, FADD, and caspase 8 to double-stranded RNA-triggered death inducing signaling complexes (dsRNA-DISCs). Apoptosis 2005:10(1): 167-176. Doi: 10.1007/ s10495-005-6071-x
Bodmer JL, Meier P, Tschopp J, Schneider P. Cysteine 230 is essential for the structure and activity of the cytotoxic ligand TRAIL. J Biol Chem 2000;275(27): 20632-20637. Doi: 10.1074/jbc.M909721199
Lemke J, Von Karstedt S, Zinngrebe J, Walczak H. Getting TRAIL back on track for cancer therapy. Cell Death Differ 2014;21(9): 1350-1364. Doi: 10.1038/ cdd.2014.81.
Zhang Y, Zhang B. TRAIL resistance of breast cancer cells is associated with constitutive endocytosis of death receptors 4 and 5. Mol Cancer Res 2008(12);6: 1861-1871. Doi: 10.1158/1541-7786.MCR-08-0313
Huang Y, Sheikh MS. TRAIL death receptors and cancer therapeutics. Toxicol Appl Pharmacol 2007;224(3): 284-289. Doi: 10.1016/j.taap.2006.12.007
Danish L, Stöhr D, Scheurich P, Pollak N. TRAIL -R3/R4 and Inhibition of TRAIL Signalling in Cancer. [Part of the Resistance to Targeted Anti-Cancer Therapeutics book series (RTACT, vol.12)] Springer, Cham 2017;12: 27-57. Available from: https://link.springer.com/chapter/10.1007/978-3-319-56805-8_2
Boyce BF, Xing L. Biology of RANK, RANKL, and osteoprotegerin. Arthritis Res Ther 2007;9(Suppl 1): S1. Doi: 10.1186/ar2165.
Van Aken O. Mitochondria and Cell Death. Annu Plant Rev 2018;50: 343-372. Doi: https://doi.org/10.1002/9781119312994. apr0553.
Ravagnan L, Roumier T, Kroemer G. Mitochondria, the killer organelles and their weapons. J Cell Physiol 2002;192(2): 131-137. Doi: 10.1002/jcp.10111
D´Arcy MS. Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol Int 2019;43(6): 582-592. Doi: 10.1002/cbin.11137
Cai J, Yang J, Jones DP. Mitochondrial control of apoptosis: the role of cytochrome c. Biochim Biophys Acta 1998;1366(1- 2): 139-149. Doi: 10.1016/s0005-2728(98)00109-1
Jiang X, Wang X. Cytochrome C-mediated apoptosis. Annu Rev Biochem 2004;73: 87-106. Doi: 10.1146/annurev.biochem.73.011303.073706
Singh R, Letai A, Sarosiek K. Regulation of apoptosis in health and disease: the balancing act of BCL -2 family proteins. Nat Rev Mol Cell Biol 2019;20(3): 175-193. Doi: 10.1038/s41580-018-0089-8
Ramírez-García M, Márquez-González H, Barranco-Lampón G, Enrique López-Aguilar J. Bcl-2: its role in the cell cycle, apoptosis and cancer. Residente 2014;9(3): 84-94.
Czabotar PE, Garcia-Saez AJ. Mechanisms of BCL -2 family proteins in mitochondrial apoptosis. Nat Rev Mol Cell Biol 2023;24(10): 732-748. Doi: 10.1038/ s41580-023-00629-4
Fernández-Lazaro D. Biological and molecular bases in the development of pathogenesis in multiple myeloma disease. Invest Clin 2019;60(3): 247-264. Doi: https:// doi.org/10.22209/IC.v60n3a07
Colado E, Paíno T, Maiso P, Ocio EM, Chen X, Álvarez-Fernández S, Gutiérrez NC, Martín-Sánchez J, Flores-Montero J, San Segundo L, Garayoa M, Fernández-Lázaro D, Vidriales MB, Galmarini CM, Avilés P, Cuevas C, Pandiella A, San-Miguel JF. Zalypsis has in vitro activity in acute myeloid blasts and leukemic progenitor cells through the induction of a DNA damage response. Haematologica 2011;96(5): 687-695. Doi: 10.3324/hae- matol.2010.036400
Maiso P, Colado E, Ocio EM, Garayoa M, Martín J, Atadja P, Pandiella A, San-Miguel JF. The synergy of panobinostat plus doxorubicin in acute myeloid leukemia suggests a role for HDAC inhibitors in the control of DNA repair. Leukemia 2009;23(12): 2265-2274. Doi: 10.1038/ leu.2009.182
Anvekar RA, Asciolla JJ, Missert DJ, Chipuk JE. Born to be alive: a role for the BCL -2 family in melanoma tumor cell survival, apoptosis, and treatment. Front Oncol 2011;1(34): 34. Doi: 10.3389/ fonc.2011.00034
Garner TP, Lopez A, Reyna DE, Spitz AZ, Gavathiotis E. Progress in targeting the BCL -2 family of proteins. Curr Opin Chem Biol 2017;39: 133-142. Doi: 10.1016/j. cbpa.2017.06.014
Kastan MB. A BID for the pathway. Nature 2005;437(7062):1103. Doi: 10.1038/ 4371103a
Omonosova E, Hinnadurai G. BH3-only proteins in apoptosis and beyond: an overview. Oncogene 2008;27(Suppl 1): S2-S19. Doi: 10.1038/onc.2009.39
Klee M, Pallauf K, Alcalá S, Fleischer A, Pimentel-Muĩos FX. Mitochondrial apoptosis induced by BH3-only molecules in the exclusive presence of endoplasmic reticular Bak. EMBO J 2009;28(12): 1757-1568. Doi: 10.1038/emboj.2009.90
Wei MC, Zong WX, Cheng EHY, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. Proapoptotic BAX, and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001;292(5517): 727-730. Doi: 10.1126/science.1059108
Wilkinson JC, Wilkinson AS, Scott FL, Csomos RA, Salvesen GS, Duckettt CS. Neutralization of Smac/Diablo by inhibitors of apoptosis (IAPs). A caspase independent mechanism for apoptotic inhibition. J Biol Chem 2004;279(49): 51082-51090. Doi: 10.1074/jbc.M408655200
Sun XM, Bratton SB, Butterworth M, MacFarlane M, Cohen GM. Bcl-2 and Bcl-xL inhibit CD95-mediated apoptosis by preventing mitochondrial release of Smac/ DIABLO and subsequent inactivation of X-linked inhibitor-of-apoptosis protein. J Biol Chem 2002;277(13): 11345-11351. Doi: 10.1074/jbc.M109893200
Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F, Youle RJ. Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J 2003;22(17): 4385-4399. Doi: 10.1093/emboj/cdg423
Candé C, Cecconi F, Dessen P, Kroemer G. Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J Cell Sci 2002;115(Pt 24): 4727-4734. Doi: 10.1242/jcs.00210
Kroemer G, Martin SJ. Caspase-independent cell death. Nat Med 2005;11(7): 725- 730. Doi: 10.1038/nm1263
Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001;412(6842):95-99. Doi: 10.1038/35083620
Van Loo G, Schotte P, Van Gurp M, Demol H, Hoorelbeke B, Gevaert K, Rodriguez I, Ruiz-Carrillo A, Vandekerckhove J, Declercq W, Beyaert R, Vandenabeele P. Endonuclease G: a mitochondrial protein released in apoptosis and involved in caspase independent DNA degradation. Cell Death Differ 2001;8(12): 1136-1142. Doi: 10.1038/sj.cdd.4400944
Wu W, Liu P, Li J. Necroptosis: an emerging form of programmed cell death. Crit Rev Oncol Hematol 2012;82(3): 249-258. Doi: 10.1016/j.critrevonc.2011.08.004
Galluzzi L, Vanden Berghe T, Vanlangenakker N, Buettner S, Eisenberg T, Vandenabeele P, Madeo F, Kroemer G. Programmed necrosis from molecules to health and disease. Int Rev Cell Mol Biol 2011;289: 1-35. Doi: 10.1016/B978-0-12-386039-2.00001-8
Günther C, Martini E, Wittkopf N, Amann K, Weigmann B, Neumann H, Waldner MJ, Hedrick SM, Tenzer S, Neurath MF, Becker C. Caspase-8 regulates TNF-α-induced epithelial necroptosis and terminal ileitis. Nature 2011;477(7364): 335-339. Doi:10.1038/nature10400
Duprez L, Takahashi N, Van Hauwermeiren F, Vandendriessche B, Goossens V, Vanden Berghe T, Declercq W, Libert C, Cauwels A, Vandenabeele P. RIP kinase dependent necrosis drives lethal systemic inflammatory response syndrome. Immunity 2011;35(6): 908-918. Doi: 10.1016/j immuni.2011.09.020
McNamara CR, Ahuja R, Osafo-Addo AD, Barrows D, Kettenbach A, Skidan I, Teng X, Cuny GD, Gerber S, Degterev A. Akt Regulates TNFα synthesis downstream of RIP1 kinase activation during necroptosis. PLoS One 2013;8(3): e56576. Doi:10.1371/journal.pone.0056576.
Wajant H, Siegmund D. TNFR1 and TNFR2 in the control of the life and death balance of macrophages. Front Cell Dev Biol 2019;7: 91. Doi: 10.3389/fcell.2019.00091
Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009;137(6): 1112-1123. Doi: 10.1016/j. cell.2009.05.037
Giampietri C, Starace D, Petrungaro S, Filippini A, Ziparo E. Necroptosis: molecular signalling and translational implications. Int J Cell Biol 2014;2014: 49027. Doi: 10.1155/2014/490275
Liu Q, Qiu J, Liang M, Golinski J, Van Leyen K, Jung JE, You Z, Lo EH, Degterev A, Whalen MJ. Akt and mTOR mediate programmed necrosis in neurons. Cell Death Dis 2014;5(2): e1084. Doi: 10.1038/cddis.2014.69.
Dondelinger Y, Declercq W, Montessuit S, Roelandt R, Goncalves A, Bruggeman I, Hulpiau P, Weber K, Sehon CA, Marquis RW, Bertin J, Gough PJ, Savvides S, Martinou JC, Bertrand MJ, Vandenabeele P. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep 2014;7(4): 971-981. Doi: 10.1016/j.celrep.2014.04.026
Uchiyama Y, Shibata M, Koike M, Yoshimura K, Sasaki M. Autophagy–physiolo- gy and pathophysiology. Histochem Cell Biol 2008;129(4): 407-420. Doi: 10.1007/ s00418-008-0406-y
Mizushima N and Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011;147(4): 728-741. Doi: 10.1016/j. cell.2011.10.026
Lindqvist LM, Heinlein M, Huang DCS, Vaux DL. Prosurvival Bcl-2 family members affect autophagy only indirectly, by inhibiting Bax and Bak. Proc Natl Acad Sci U S A 2014;111(23): 8512-8517. Doi: 10.1073/ pnas.1406425111
Klionsky DJ, Petroni G, Amaravadi RK, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM, Cadwell K, Cecconi F, Pietrocola F. Autophagy in major human diseases. EMBO J 2021;40(19): e108863. Doi: 10.15252/embj.2021108863
Choi AMK, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med 2013;368(7): 651-662. Doi: 10.1056/ NEJMra1205406
Hale AN, Ledbetter DJ, Gawriluk TR, Rucker EB. Autophagy: regulation and role in development. Autophagy 2013;9(7): 951-972. Doi: 10.4161/auto.24273
Cheng Y, Ren X, Hait WN, Yang JM. Therapeutic targeting of autophagy in disease: biology and pharmacology. Pharmacol Rev 2013;65(4): 1162-1197. Doi: 10.1124/ pr.112.007120
Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011;7(3): 279-296. Doi: 10.4161/auto.7.3.14487
Ryter SW, Mizumura K, Choi AMK. The impact of autophagy on cell death modalities. Int J Cell Biol 2014;2014: 502676. Doi: 10.1155/2014/502676
Kwanten WJ, Martinet W, Michielsen PP, Francque SM. Role of autophagy in the pathophysiology of nonalcoholic fatty liver disease: a controversial issue. World J Gastroenterol 2014;20(23): 7325-7338. Doi: 10.3748/wjg.v20.i23.7325
Ding WX, Yin XM. Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol Chem 2012;393(7): 547-564. Doi: 10.1515/hsz-2012-0119
Publicado
2024-05-21
Cómo citar
Fernández-Lázaro , D., Sanz, B., & Seco-Calvo, J. (2024). Mechanisms of programmed cell death: structural and functional pathways. A narrative review.: Mecanismos de muerte celular programada: vías estructurales y funcionales. Una revisión narrativa. Investigación Clínica, 65(2), 230-252. https://doi.org/10.54817/IC.v65n2a09
Sección
Revisiones
