Correlated light and electron microscopy illuminates the role of mitochondrial inner membrane remodeling during apoptosis

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1777, Issue 7-8, 2008, Pages 847-852

  Frey, Terrence G ^a   Sun, Mei G ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Electron microscopy; Electron tomography; Fluorescence microscopy; Membrane remodeling; Mitochondria

Indexed keywords

CYTOCHROME C;

APOPTOSIS; CELL MEMBRANE POTENTIAL; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; HELA CELL; HUMAN; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW;

APOPTOSIS; CYTOCHROMES C; HELA CELLS; HUMANS; MICROSCOPY, CONFOCAL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MODELS, BIOLOGICAL; PERMEABILITY;

EID: 50949127216     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2008.05.011     Document Type: Review

References (44)

1. Frey T., Renken C., and Perkins G. Insight into mitochondrial structure and function from electron tomography. Biochim. Biophys. Acta 1555 (2002) 196-203
2. Frey T.G., and Mannella C.A. The internal structure of mitochondria. Trends Biochem. Sci. 25 (2000) 319-324
3. Mannella C.A., Buttle K., Rath B.K., and Marko M. Electron microscopic tomography of rat-liver mitochondria and their interaction with the endoplasmic reticulum. BioFactors 8 (1998) 225-228
4. Mannella C.A., Marko M., and Buttle K. Reconsidering mitochondrial structure: new views of an old organelle. TIBS 22 (1997) 37-38
5. Gilkerson R.W., Selker J.M., and Capaldi R.A. The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett. 546 (2003) 355-358
6. Mannella C.A., Pfeiffer D.R., Bradshaw P.C., Moraru I.I., Slepchenko B., Loew L.M., Hsieh C.E., Buttle K., and Marko M. Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications. IUBMB Life 52 (2001) 93-100
7. Perkins G., Renken C., Martone M.E., Young S.J., Ellisman M., and Frey T.G. Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts. J. Struct. Biol. 119 (1997) 260-272
8. Perkins G., Song J., Tarsa L., Deerinck T., Ellisman M., and Frey T.G. Electron tomography of mitochondria from brown adipocytes reveals crista junctions. J. Bioenerg. Biomembr. 30 (1998) 431-442
9. Perkins G.A., Renken C.W., van der Klei I.J., Ellisman M.H., Neupert W., and Frey T.G. Electron tomography of mitochondria after the arrest of protein import associated with Tom 19 depletion. Eur. J. Cell Biol. 80 (2001) 139-150
10. Renken C., Siragusa G., Perkins G., Washington L., Nulton J., Salamon P., and Frey T.G. A thermodynamic model describing the nature of the crista junction: a structural motif in the mitochondrion. J. Struct. Biol. 138 (2002) 137-144
11. Meeusen S., Devay R., Block J., Cassidy-Stone A., Wayson S., McCaffery J.M., and Nunnari J. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related gtpase Mgm1. Cell 127 (2006) 383-395
12. Hoppins S., Lackner L., and Nunnari J. The machines that divide and fuse mitochondria. Ann. Rev. Biochem. 76 (2007) 751-780
13. Green D.R., and Kroemer G. The pathophysiology of mitochondrial cell death. Science 305 (2004) 626-629
14. Green D.R., and Reed J.C. Mitochondria and apoptosis. Science 281 (1998) 1309-1312
15. Kuwana T., Mackey M.R., Perkins G., Ellisman M.H., Latterich M., Schneiter R., Green D.R., and Newmeyer D.D. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111 (2002) 331-342
16. Frezza C., Cipolat S., Martins de Brito O., Micaroni M., Beznoussenko G.V., Rudka T., Bartoli D., Polishuck R.S., Danial N.N., De Strooper B., and Scorrano L. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126 (2006) 177-189
17. Scorrano L., Ashiya M., Buttle K., Weiler S., Oakes S.A., Mannella C.A., and Korsmeyer S.J. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell 2 (2002) 55-67
18. Goldstein J.C., Munoz-Pinedo C., Ricci J.E., Adams S.R., Kelekar A., Schuler M., Tsien R.Y., and Green D.R. Cytochrome c is released in a single step during apoptosis. Cell Death Differ. 12 (2005) 453-462
19. Goldstein J.C., Waterhouse N.J., Juin P., Evan G.I., and Green D.R. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat. Cell Biol. 2 (2000) 156-162
20. Gaietta G., Deerinck T.J., Adams S.R., Bouwer J., Tour O., Laird D.W., Sosinsky G.E., Tsien R.Y., and Ellisman M.H. Multicolor and electron microscopic imaging of connexin trafficking. Science 296 (2002) 503-507
21. Petronilli V., Miotto G., Canton M., Brini M., Colonna R., Bernardi P., and Di Lisa F. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys. J. 76 (1999) 725-734
22. Sun M.G., Williams J., Munoz-Pinedo C., Perkins G.A., Brown J.M., Ellisman M.H., Green D.R., and Frey T.G. Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis. Nat. Cell Biol. 9 (2007) 1057-1072
23. Sun M.G. Mitochondrial Structure During Apoptosis, Biology, vol. Ph.D. (2007), San Diego State University, San Diego 140
24. Renken C. The Structure of Mitochondria, Biology (2004), San Diego State University, San Diego 200
25. Manor J.C., Frey T., Baljon A., Mahaffy J.M., Nulton J., and Salamon P. Membrane remodeling and diffusion of cytochrome c from a geometrically idealized mitochondrial crista. International Conference on Bioinformatics and Computational Biology (2006), CSREA Press, Las Vegas 310-314
26. Bernardi P., and Azzone G.F. Cytochrome c as an electron shuttle between the outer and inner mitochondrial membranes. J. Biol. Chem. 256 (1981) 7187-7192
27. Ricci J.E., Munoz-Pinedo C., Fitzgerald P., Bailly-Maitre B., Perkins G.A., Yadava N., Scheffler I.E., Ellisman M.H., and Green D.R. Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell 117 (2004) 773-786
28. Chan D.C. Mitochondrial fusion and fission in mammals. Annu .Rev. Cell Dev. Biol. 22 (2006) 79-99
29. Heath-Engel H.M., and Shore G.C. Mitochondrial membrane dynamics, cristae remodelling and apoptosis. Biochim. Biophys. Acta 1763 (2006) 1277-1280
30. Okamoto K., and Shaw J.M. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet 39 (2005) 503-536
31. Karbowski M., Arnoult D., Chen H., Chan D.C., Smith C.L., and Youle R.J. Quantitation of mitochondrial dynamics by photolabeling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis. J. Cell Biol. 164 (2004) 493-499
32. Karbowski M., and Youle R.J. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell. Death Differ. 10 (2003) 870-880
33. Lee Y.J., Jeong S.Y., Karbowski M., Smith C.L., and Youle R.J. Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol. Biol. Cell 15 (2004) 5001-5011
34. Irwin W.A., Bergamin N., Sabatelli P., Reggiani C., Megighian A., Merlini L., Braghetta P., Columbaro M., Volpin D., Bressan G.M., Bernardi P., and Bonaldo P. Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat. Genet. 35 (2003) 367-371
35. Olichon A., Emorine L.J., Descoins E., Pelloquin L., Brichese L., Gas N., Guillou E., Delettre C., Valette A., Hamel C.P., Ducommun B., Lenaers G., and Belenguer P. The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett. 523 (2002) 171-176
36. Olichon A., Baricault L., Gas N., Guillou E., Valette A., Belenguer P., and Lenaers G. Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278 (2003) 7743-7746
37. Griparic L., van der Wel N.N., Orozco I.J., Peters P.J., and van der Bliek A.M. Loss of the intermembrane space protein Mgm1/OPA1 induces swelling and localized constrictions along the lengths of mitochondria. J. Biol. Chem. 279 (2004) 18792-18798
38. Chen H., McCaffery J.M., and Chan D.C. Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130 (2007) 548-562
39. Amutha B., Gordon D.M., Gu Y., and Pain D. A novel role of Mgm1p, a dynamin-related GTPase, in ATP synthase assembly and cristae formation/maintenance. Biochem. J. 381 (2004) 19-23
40. Cipolat S., Rudka T., Hartmann D., Costa V., Serneels L., Craessaerts K., Metzger K., Frezza C., Annaert W., D'Adamio L., Derks C., Dejaegere T., Pellegrini L., D'Hooge R., Scorrano L., and De Strooper B. Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126 (2006) 163-175
41. Shaw J.M., and Nunnari J. Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12 (2002) 178-184
42. Arnoult D., Grodet A., Lee Y.J., Estaquier J., and Blackstone C. Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J. Biol. Chem. 280 (2005) 35742-35750
43. Griparic L., Kanazawa T., and van der Bliek A.M. Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J. Cell Biol. 178 (2007) 757-764
44. Merkwirth C., Dargazanli S., Tatsuta T., Geimer S., Lower B., Wunderlich F.T., von Kleist-Retzow J.C., Waisman A., Westermann B., and Langer T. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev. 22 (2008) 476-488