Mitochondrial Swelling and Incipient Outer Membrane Rupture in Preapoptotic and Apoptotic Cells

Anatomical Record

Volumn 295, Issue 10, 2012, Pages 1647-1659

  Sesso, A ^a   Belizario J E ^a   Marques, M M ^a   Higuchi, M L ^a   Schumacher, R I ^a   Colquhoun, A ^a   Ito, E ^a   Kawakami, J ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Apoptosis; Electron microscopy; Focal matrix herniation in mitochondria; Inner mitochondrial membrane; Mitochon drial permeability transition; Mitochondria; Mitochondrial outer membrane permeabilization; Mitochondrial proteins of the intermembrane space; Outer mitochon drial membrane; Rupture of the outer mitochondrial membrane

Indexed keywords

MITOCHONDRIAL PROTEIN;

APOPTOSIS; ARTICLE; CELL TYPE; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; INNER MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION SWELLING; OUTER MITOCHONDRIAL MEMBRANE RUPTURE; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; CELL MEMBRANE; CRICETINAE; HL-60 CELLS; HUMANS; INTRACELLULAR MEMBRANES; MITOCHONDRIA; MITOCHONDRIAL SWELLING; PC12 CELLS; RATS;

EID: 84866156089     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.22553     Document Type: Article

References (51)

1. Abdelwahid E, Yokokura T, Krieser RJ, Balasundaram S, Fowle WH, White K. 2007. Mitochondrial disruption in Drosophila apoptosis. Dev Cell 12: 793-806.
2. Angermüller S, Kunstle G, Tiegs G. 1998. Preapoptotic alterations in hepatocytes of TNF α-treated galactosamine-sensitized mice. J Histochem Cytochem 46: 1175-1183.
3. Armstrong JS. 2006. The role of the mitochondrial permeability transition in cell death. Mitochondrion 6: 225-234.
4. Basañez G, Nechushtan A, Drozhinin O, Chanturiya A, Choe E, Tutt S, Wood KA, Hsu Y, Zimmerberg J, Youle RJ. 1999. Bax, but not Bcl-xL, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc Natl Acad Sci USA 96: 5492-5497.
5. Basañez G, Sharpe JC, Galanis J, Brandt TB, Hardwick JM, Zimmerberg J. 2002. Baxtype apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem 277: 49360-49365.
6. Brenner C, Kroemer G. 2000. Apoptosis. Mitochondria-the death signal integrators. Science 289: 1150-1151.
7. Charlot JF, Prétet JL, Haughey C, Mougin C. 2004. Mitochondrial translocation of p53 and mitochondrial membrane potential (Delta Psi m) dissipation are early events in staurosporine-induced apoptosis of wild type and mutated p53 epithelial cells. Apoptosis 9: 333-343.
8. Chipuk JE, Bouchier-Hayes L, Green DR. 2006. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ 13: 1396-1402.
9. Desagher S, Martinou JC. 2000. Mitochondria as the central control point of apoptosis. Trends Cell Biol 10: 369-377.
10. Düssmann H, Rehm M, Kögel D, Prehn JH. 2003. Outer mitochondrial membrane permeabilization during apoptosis triggers caspase-independent mitochondrial and caspase-dependent plasma membrane potential depolarization: a single-cell analysis. J Cell Sci 116: 525-536.
11. Feldmann G, Haouzi D, Moreau A, Durand-Schneider AM, Bringuier A, Berson A. 2000. Opening of the mitochondrial permeability transition pore causes matrix expansion and outer membrane rupture in Fas-mediated hepatic apoptosis in mice. Hepatology 31: 674-683.
12. Garcia-Perez C, Roy SS, Naghdi S, Lin X, Davies E, Hajnóczky G. 2012. Bid-induced mitochondrial membrane permeabilization waves propagated by local reactive oxygen species (ROS) signaling. Proc Natl Acad Sci U S A 109: 4497-4502.
13. Gogvadze V, Orrenius S, Zhivotovsky B. 2006. Multiple pathways of cytochrome c release from mitochondria in apoptosis. Biochim Biophys Acta 1757: 639-647.
14. Green DR. 2006. At the gates of death. Cancer Cell 9: 328-330.
15. Green DR, Kroemer G. 2004. The pathophysiology of mitochondrial cell death. Science 305: 626-629.
16. Green DR, Reed JC. 1998. Mitochondria and apoptosis. Science 281: 1309-1312.
17. Grimm S, Brdiczka D. 2007. The permeability transition pore in cell death. Apoptosis 12: 841-855.
18. Hackenbrock CR. 1966. Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J Cell Biol 30: 269-297.
19. Higuchi Y, Miura T, Kajimoto T, Ohta Y. 2005. Effects of disialoganglioside GD3 on the mitochondrial membrane potential. FEBS Lett 579: 3009-3013.
20. Indran IR, Tufo G, Pervaiz S, Brenner C. 2011. Recent advances in apoptosis, mitochondria and drug resistance in cancer cells. Biochim Biophys Acta 1807: 735-745.
21. Ho PL, Raw I. 1992. Cyclic AMP potentiates bFGF-induced neurite outgrowth in PC12 cells. J Cell Physiol 150: 647-656.
22. Karpinich NO, Tafani M, Rothman RJ, Russo MA, Farber JL. 2002. The course of etoposide-induced apoptosis from damage to DNA and p53 activation to mitochondrial release of cytochrome c. J Biol Chem 277: 16547-16552.
23. Kinnally KW, Antonsson B. 2007. A tale of two mitochondrial channels, Mac and PTP, in apoptosis. Apoptosis 12: 857-868.
24. Kinnally KW, Peixoto PM, Ryu SY, Dejean LM. 2010. Is mPTP the gatekeeper for necrosis, apoptosis, or both? Biochim Biophys Acta; doi:10.1016/j.bbamcr.2010.09.13.
25. Kowaltowski AJ, Castilho RF, Vercesi AE. 2001. Mitochondrial permeability transition and oxidative stress. FEBS Lett 495: 12-15.
26. Kroemer G, Galluzzi L, Brenner C. 2007. Mitochondrial membrane permeabilization in cell death. Physiol Rev 87: 99-163.
27. Kwong J, Choi HL, Huang Y, Chan FL. 1999. Ultrastructural and biochemical observations on the early changes in apoptotic epithelial cells of the rat prostate induced by castration. Cell Tissue Res 298: 123-136.
28. Lemasters JJ, Theruvath TP, Zhong Z, Nieminen AL. 2009. Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta 1787: 1395-1401.
29. Li H, Zhu H, Xu CJ, Yuan J. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94: 491-501.
30. Liu J, St Clair DK, Gu X, Zhao Y. 2008. Blocking mitochondrial permeability transition prevents p53 mitochondrial translocation during skin tumor promotion. FEBS Lett 582: 1319-1324.
31. Ly JD, Grubb DR, Lawen A. 2003. The mitochondrial membrane potential (deltapsi(m)) in apoptosis; an update. Apoptosis 8: 115-128.
32. Machida K, Osada H. 2003. Molecular interaction between cyclophilin D and adenine nucleotide translocase in cytochrome c release: does it determine whether cytochrome c release is dependent on permeability transition or not? Ann N Y Acad Sci 1010: 182-185.
33. Martinou JC, Green DR. 2001. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2: 63-67.
34. Ott M, Gogvadzev V, Orrenius S, Zhitovotovsky B. 2007. Mitochondria, oxidative stress and cell death. Apoptosis 12: 913-922.
35. Petit PX, Goubern M, Diolez P, Susin SA, Zamzami N, Kroemer G. 1998. Disruption of the outer mitochondrial membrane as a result of large amplitude swelling: the impact of irreversible permeability transition. FEBS Lett 426: 111-116.
36. Petit PX, Susin SA, Zamzami N, Mignotte B, Kroemer G. 1996. Mitochondria and programmed cell death: back to the future. FEBS Lett 396: 7-13.
37. Rasola A, Bernardi P. 2007. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 12: 815-833.
38. Reed JC, Green DR. 2002. Remodeling for demolition: changes in mitochondrial ultrastructure during apoptosis. Moll Cell 9: 1-3.
39. Robertson JD, Zhivotovsky B, Gogvadze V, Orrenius S. 2003. Outer mitochondrial membrane permeabilization: an open-and-shut case? Cell Death Differ 10: 485-487.
40. Scarlett JL, Murphy MP. 1997. Release of apoptogenic proteins from the mitochondrial intermembrane space during the mitochondrial permeability transition. FEBS Lett 418: 282-286.
41. Schafer B, Quispe J, Choudhary V, Chipuk JE, Ajero TG, Du H, Schneiter R, Kuwana T. 2009. Mitochondrial outer membrane proteins assist Bid in Bax-mediated lipidic pore formation. Mol Biol Cell 20: 2276-2285.
42. Sesso A. 2006. Pitfalls in the use of electron microscopy to study the mitochondrial membrane permeability transition in apoptotic cells and pellets: where do we stand in relation to the incidence of mitochondrial swelling in apoptosis? Braz J Morphol Sci 23: 57-74. Download in http://antses88.sites.uol.com.br/bjms.html.
43. Sesso A, Fujiwara DT, Jaeger M, Jaeger R, Li TC, Monteiro MM, Correa H, Ferreira MA, Schumacher RI, Belisário J, Kachar B, Chen EJ. 1999. Structural elements common to mitosis and apoptosis. Tissue Cell 31: 357-371.
44. Sesso A, Marques MM, Monteiro MM, Schumacher RI, Colquhoun A, Belizário J, Konno SN, Felix TB, Botelho LA, Santos VZ, Da Silva GR, Higuchi Mde L, Kawakami JT. 2004. Morphology of mitochondrial permeability transition: morphometric volumetry in apoptotic cells. Anat Rec A Discov Mol Cell Evol Biol 281: 1337-1351.
45. Sharpe JC, Arnoult D, Youle RJ. 2004. Control of mitochondrial permeability by Bcl-2 family members. Biochim Biophys Acta 1644: 107-113.
46. Shimizu T, Numata T, Okada Y. 2004. A role of reactive oxygen species in apoptotic activation of volume-sensitive Cl(-) channel. Proc Natl Acad Sci U S A 17: 6770-6773.
47. Skulachev VP. 1996. Why are mitochondria involved in apoptosis? Permeability transition pores and apoptosis as selective mechanisms to eliminate superoxideproducing mitochondria and cell. FEBS Lett 397: 7-10.
48. Stoner CD, Sirak HD. 1969. Osmotically-induced alterations in volume and ultrastructure of mitochondria isolated from rat liver and bovine heart. J Cell Biol 43: 521-538.
49. Tafani M, Minchenko DA, Serroni A, Farber JL. 2001. Induction of the mitochondrial permeability transition mediates the killing of HeLa cells by staurosporine. Cancer Res 61: 2459-2466.
50. Vogler M, Dinsdale D, Sun XM, Young KW, Butterworth M, Nicotera P, Dyer MJ, Cohen GM. 2008. A novel paradigm for rapid ABT-737-induced apoptosis involving outer mitochondrial membrane rupture in primary leukemia and lymphoma cells. Cell Death Differ 15: 820-830.
51. Zoratti M, Szabò I, De Marchi U. 2005. Mitochondrial permeability transitions: how many doors to the house? Biochim Biophys Acta 1706: 40-52.