Apoptotic microtubule network organization and maintenance depend on high cellular ATP levels and energized mitochondria

Apoptosis

Volumn 16, Issue 4, 2011, Pages 404-424

  Oropesa, Manuel ^a   De La Mata, Mario ^a   Maraver, Juan Garrido ^a   Cordero, Mario D ^a   Cotán, David ^a   Rodríguez Hernández, Ángeles ^a   Domínguez Moñino, Irene ^a   De Miguel, Manuel ^b   Navas, Plácido ^a   Sánchez Alcázar, José A ^a  

^a CSIC   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Apoptosis; Cytoskeleton; Microtubules; Mitochondria; Mitochondrial membrane potential

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CALCIUM; CAMPTOTHECIN; LACTATE DEHYDROGENASE;

APOPTOSIS; APOPTOTIC MICROTUBULE NETWORK; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL LEVEL; CELL MEMBRANE DEPOLARIZATION; ENERGY YIELD; ENZYME RELEASE; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; MEMBRANE PERMEABILITY; MICROTUBULE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PRIORITY JOURNAL;

ACTINS; ADENOSINE TRIPHOSPHATE; APOPTOSIS; CALCIUM; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CELL LINE, TUMOR; COLCHICINE; CYTOCHROMES C; ENERGY METABOLISM; GLYCOLYSIS; HUMANS; KINETICS; L-LACTATE DEHYDROGENASE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROTUBULES; MITOCHONDRIA; OLIGOMYCINS; PROTON-TRANSLOCATING ATPASES;

SUS;

EID: 79955785663     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-011-0577-1     Document Type: Article

References (44)

1. JF Kerr AH Wyllie AR Currie 1972 Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics Br J Cancer 26 239 257 4561027 10.1038/bjc.1972.33 1:STN:280:DyaE3s%2FgsFSksw%3D%3D
2. LP Erwig PM Henson 2008 Clearance of apoptotic cells by phagocytes Cell Death Differ 15 243 250 17571081 10.1038/sj.cdd.4402184 1:CAS:528: DC%2BD1cXmsVOrtg%3D%3D
3. J Savill I Dransfield C Gregory C Haslett 2002 A blast from the past: clearance of apoptotic cells regulates immune responses Nat Rev Immunol 2 965 975 12461569 10.1038/nri957 1:CAS:528:DC%2BD38XptFKnu7c%3D (Pubitemid 37323217)
4. MR Wilson 1998 Apoptosis: unmasking the executioner Cell Death Differ 5 646 652 10200519 10.1038/sj.cdd.4400394 1:CAS:528:DyaK1cXlslWgtr0%3D (Pubitemid 28391366)
5. S Afford S Randhawa 2000 Apoptosis Mol Pathol 53 55 63 10889903 10.1136/mp.53.2.55 1:CAS:528:DC%2BD3cXivFOnur0%3D (Pubitemid 30183077)
6. JC Mills NL Stone RN Pittman 1999 Extranuclear apoptosis. The role of the cytoplasm in the execution phase J Cell Biol 146 703 708 10459006 10.1083/jcb.146.4.703 1:CAS:528:DyaK1MXls1Srtrc%3D (Pubitemid 29408897)
7. S Pittman M Geyp M Fraser K Ellem A Peaston C Ireland 1997 Multiple centrosomal microtubule organising centres and increased microtubule stability are early features of VP-16-induced apoptosis in CCRF-CEM cells Leuk Res 21 491 499 10.1016/S0145-2126(97)00038-6 1:CAS:528:DyaK2sXlvFelur4%3D (Pubitemid 27389473)
8. SM Pittman D Strickland CM Ireland 1994 Polymerization of tubulin in apoptotic cells is not cell cycle dependent Exp Cell Res 215 263 272 7982469 10.1006/excr.1994.1342 1:CAS:528:DyaK2MXisVWhuro%3D (Pubitemid 24381076)
9. DK Moss VM Betin SD Malesinski JD Lane 2006 A novel role for microtubules in apoptotic chromatin dynamics and cellular fragmentation J Cell Sci 119 2362 2374 16723742 10.1242/jcs.02959 1:CAS:528:DC%2BD28Xms1Gis7g%3D (Pubitemid 43960325)
10. DK Moss JD Lane 2006 Microtubules: forgotten players in the apoptotic execution phase Trends Cell Biol 16 330 338 16765597 10.1016/j.tcb.2006.05.005 1:CAS:528:DC%2BD28XntFWrt7c%3D (Pubitemid 44062317)
11. JA Sanchez-Alcazar A Rodriguez-Hernandez MD Cordero, et al. 2007 The apoptotic microtubule network preserves plasma membrane integrity during the execution phase of apoptosis Apoptosis 12 1195 1208 17245640 10.1007/s10495-006-0044-6 (Pubitemid 46890376)
12. DK Moss A Wilde JD Lane 2009 Dynamic release of nuclear RanGTP triggers TPX2-dependent microtubule assembly during the apoptotic execution phase J Cell Sci 122 644 655 19208764 10.1242/jcs.037259 1:CAS:528:DC%2BD1MXktVWru7w%3D
13. L Ravagnan T Roumier G Kroemer 2002 Mitochondria, the killer organelles and their weapons J Cell Physiol 192 131 137 12115719 10.1002/jcp.10111 1:CAS:528:DC%2BD38Xlt1Kqurg%3D (Pubitemid 34747781)
14. M Ankarcrona JM Dypbukt E Bonfoco, et al. 1995 Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function Neuron 15 961 973 7576644 10.1016/0896-6273(95)90186-8 1:CAS:528:DyaK2MXptV2gsLc%3D
15. L Jia PD Allen MG Macey MF Grahn AC Newland SM Kelsey 1997 Mitochondrial electron transport chain activity, but not ATP synthesis, is required for drug-induced apoptosis in human leukaemic cells: a possible novel mechanism of regulating drug resistance Br J Haematol 98 686 698 9332327 10.1046/j.1365-2141. 1997.2683085.x 1:CAS:528:DyaK2sXmt1Krsb0%3D (Pubitemid 27386552)
16. N Zamzami P Marchetti M Castedo, et al. 1996 Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis FEBS Lett 384 53 57 8797802 10.1016/0014-5793(96) 00280-3 1:CAS:528:DyaK28XisFWgtbg%3D (Pubitemid 26114720)
17. A Rodriguez-Hernandez G Brea-Calvo DJ Fernandez-Ayala M Cordero P Navas JA Sanchez-Alcazar 2006 Nuclear caspase-3 and caspase-7 activation, and Poly(ADP-ribose) polymerase cleavage are early events in camptothecin-induced apoptosis Apoptosis 11 131 139 16374543 10.1007/s10495-005-3276-y 1:CAS:528:DC%2BD28XovFynsQ%3D%3D (Pubitemid 43151651)
18. B Kadenbach 2003 Intrinsic and extrinsic uncoupling of oxidative phosphorylation Biochim Biophys Acta 1604 77 94 12765765 10.1016/S0005-2728(03) 00027-6 1:CAS:528:DC%2BD3sXjvFahs7k%3D (Pubitemid 36588693)
19. C von Ballmoos A Wiedenmann P Dimroth 2009 Essentials for ATP synthesis by F1F0 ATP synthases Annu Rev Biochem 78 649 672 10.1146/annurev.biochem.78. 081307.104803
20. HA Lardy D Johnson WC McMurray 1958 Antibiotics as tools for metabolic studies. I. A survey of toxic antibiotics in respiratory, phosphorylative and glycolytic systems Arch Biochem Biophys 78 587 597 13618041 10.1016/0003- 9861(58)90383-7 1:CAS:528:DyaG1MXlt1Srsg%3D%3D
21. C Duanmu CM Lin E Hamel 1986 Tubulin polymerization with ATP is mediated through the exchangeable GTP site Biochim Biophys Acta 881 113 123 3004597 1:CAS:528:DyaL28XhsVChtLs%3D (Pubitemid 16053258)
22. M Leist B Single AF Castoldi S Kuhnle P Nicotera 1997 Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis J Exp Med 185 1481 1486 9126928 10.1084/jem.185.8.1481 1:CAS:528:DyaK2sXjtFensbs%3D (Pubitemid 27187604)
23. P Nicotera M Leist E Ferrando-May 1998 Intracellular ATP, a switch in the decision between apoptosis and necrosis Toxicol Lett 102-103 139 142 10022245 10.1016/S0378-4274(98)00298-7 (Pubitemid 29021213)
24. C Richter M Schweizer A Cossarizza C Franceschi 1996 Control of apoptosis by the cellular ATP level FEBS Lett 378 107 110 8549813 10.1016/0014-5793(95) 01431-4 1:CAS:528:DyaK28Xns1yrug%3D%3D (Pubitemid 26015556)
25. Y Eguchi S Shimizu Y Tsujimoto 1997 Intracellular ATP levels determine cell death fate by apoptosis or necrosis Cancer Res 57 1835 1840 9157970 1:CAS:528:DyaK2sXjtlGntr0%3D (Pubitemid 27209706)
26. M Leist B Single H Naumann, et al. 1999 Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis Exp Cell Res 249 396 403 10366439 10.1006/excr.1999.4514 1:CAS:528:DyaK1MXjslSlsL0%3D (Pubitemid 29397947)
27. A Atlante S Giannattasio A Bobba, et al. 2005 An increase in the ATP levels occurs in cerebellar granule cells en route to apoptosis in which ATP derives from both oxidative phosphorylation and anaerobic glycolysis Biochim Biophys Acta 1708 50 62 15949983 10.1016/j.bbabio.2005.01.009 1:CAS:528:DC%2BD2MXltFSktb0%3D (Pubitemid 40798530)
28. MV Zamaraeva RZ Sabirov E Maeno Y Ando-Akatsuka SV Bessonova Y Okada 2005 Cells die with increased cytosolic ATP during apoptosis: a bioluminescence study with intracellular luciferase Cell Death Differ 12 1390 1397 15905877 10.1038/sj.cdd.4401661 1:CAS:528:DC%2BD2MXhtV2kt7zJ (Pubitemid 41521929)
29. JA Sanchez-Alcazar J Ruiz-Cabello I Hernandez-Munoz, et al. 1997 Tumor necrosis factor-alpha increases ATP content in metabolically inhibited L929 cells preceding cell death J Biol Chem 272 30167 30177 9374498 10.1074/jbc.272.48.30167 1:CAS:528:DyaK2sXnslGhtbo%3D (Pubitemid 27512217)
30. DR Green JC Reed 1998 Mitochondria and apoptosis Science 281 1309 1312 9721092 10.1126/science.281.5381.1309 1:CAS:528:DyaK1cXlvVegsLo%3D (Pubitemid 28406816)
31. JM Kim HR Bae BS Park, et al. 2003 Early mitochondrial hyperpolarization and intracellular alkalinization in lactacystin-induced apoptosis of retinal pigment epithelial cells J Pharmacol Exp Ther 305 474 481 12606642 10.1124/jpet.102.047811 1:CAS:528:DC%2BD3sXjt12mtLY%3D (Pubitemid 36459160)
32. PF Li R Dietz R von Harsdorf 1999 p53 regulates mitochondrial membrane potential through reactive oxygen species and induces cytochrome c-independent apoptosis blocked by Bcl-2 EMBO J 18 6027 6036 10545114 10.1093/emboj/18.21.6027 1:CAS:528:DyaK1MXns1entro%3D (Pubitemid 29515679)
33. I Marzo C Brenner N Zamzami, et al. 1998 Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis Science 281 2027 2031 9748162 10.1126/science.281.5385.2027 1:CAS:528:DyaK1cXmtlKmsLk%3D (Pubitemid 28475490)
34. P Matarrese L Falzano A Fabbri, et al. 2007 Clostridium difficile toxin B causes apoptosis in epithelial cells by thrilling mitochondria. Involvement of ATP-sensitive mitochondrial potassium channels J Biol Chem 282 9029 9041 17220295 10.1074/jbc.M607614200 1:CAS:528:DC%2BD2sXivV2mtrY%3D (Pubitemid 47093530)
35. P Matarrese L Gambardella A Cassone S Vella R Cauda W Malorni 2003 Mitochondrial membrane hyperpolarization hijacks activated T lymphocytes toward the apoptotic-prone phenotype: homeostatic mechanisms of HIV protease inhibitors J Immunol 170 6006 6015 12794128 1:CAS:528:DC%2BD3sXktlKrtrs%3D (Pubitemid 36682581)
36. A Perl P Gergely Jr G Nagy A Koncz K Banki 2004 Mitochondrial hyperpolarization: a checkpoint of T-cell life, death and autoimmunity Trends Immunol 25 360 367 15207503 10.1016/j.it.2004.05.001 1:CAS:528: DC%2BD2cXltVKjtLc%3D (Pubitemid 38780952)
37. MG Vander Heiden NS Chandel EK Williamson PT Schumacker CB Thompson 1997 Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria Cell 91 627 637 9393856 10.1016/S0092-8674(00)80450-X 1:STN:280: DyaK1c%2FlsVSjtw%3D%3D (Pubitemid 27513654)
38. AR Khaled DA Reynolds HA Young CB Thompson K Muegge SK Durum 2001 Interleukin-3 withdrawal induces an early increase in mitochondrial membrane potential unrelated to the Bcl-2 family. Roles of intracellular pH, ADP transport, and F(0)F(1)-ATPase J Biol Chem 276 6453 6462 11102440 10.1074/jbc.M006391200 1:CAS:528:DC%2BD3MXhslShtLY%3D
39. DG Nicholls SL Budd 2000 Mitochondria and neuronal survival Physiol Rev 80 315 360 10617771 1:CAS:528:DC%2BD3cXmtl2isg%3D%3D (Pubitemid 30060567)
40. S Matsuyama J Llopis QL Deveraux RY Tsien JC Reed 2000 Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis Nat Cell Biol 2 318 325 10854321 10.1038/35014006 1:CAS:528:DC%2BD3cXlt1Sls70%3D
41. G Santamaria M Martinez-Diez I Fabregat JM Cuezva 2006 Efficient execution of cell death in non-glycolytic cells requires the generation of ROS controlled by the activity of mitochondrial H+-ATP synthase Carcinogenesis 27 925 935 16361271 10.1093/carcin/bgi315 1:CAS:528:DC%2BD28XjslKrs7s%3D
42. C Chinopoulos V Adam-Vizi 2010 Mitochondria as ATP consumers in cellular pathology Biochim Biophys Acta 1802 221 227 19715757 1:CAS:528: DC%2BD1MXhsFanurnK
43. KK Peachman DS Lyles DA Bass 2001 Mitochondria in eosinophils: functional role in apoptosis but not respiration Proc Natl Acad Sci USA 98 1717 1722 11172017 10.1073/pnas.98.4.1717 1:CAS:528:DC%2BD3MXhsVWisrw%3D (Pubitemid 32165564)
44. G Kroemer N Zamzami SA Susin 1997 Mitochondrial control of apoptosis Immunol Today 18 44 51 9018974 10.1016/S0167-5699(97)80014-X 1:CAS:528:DyaK2sXotFygtA%3D%3D (Pubitemid 27072433)