Cristae Membrane Dynamics – A Paradigm Change
2020; Elsevier BV; Volume: 30; Issue: 12 Linguagem: Inglês
10.1016/j.tcb.2020.08.008
ISSN1879-3088
AutoresArun Kumar Kondadi, Ruchika Anand, Andreas S. Reichert,
Tópico(s)Metabolism and Genetic Disorders
ResumoCristae membranes are highly dynamic, can reshape on a timescale of seconds, and possibly undergo membrane fission and fusion events.Diffraction-unlimited techniques and sophisticated fluorescence labeling technologies allow us for the first time to study the role of specific lipid and protein nanodomains in cristae of individual mitochondria at high spatial and temporal resolution.Cristae membrane remodeling is regulated by the MICOS (mitochondrial contact site and cristae organizing system) complex, OPA1, F1Fo ATP synthase, and the lipid microenvironment.Cristae dynamics and local changes in mitochondrial membrane potential at the level of individual cristae are predicted to have major consequences for mitochondrial functions such as oxidative phosphorylation, thermogenesis, Ca2+ homeostasis, and apoptosis.Deciphering the regulatory mechanisms in physiological and pathological conditions may boost the development of strategies for treating mitochondrial diseases. Mitochondria are dynamic organelles that have essential metabolic and regulatory functions. Earlier studies using electron microscopy (EM) revealed an immense diversity in the architecture of cristae – infoldings of the mitochondrial inner membrane (IM) – in different cells, tissues, bioenergetic and metabolic conditions, and during apoptosis. However, cristae were considered to be largely static entities. Recently, advanced super-resolution techniques have revealed that cristae are independent bioenergetic units that are highly dynamic and remodel on a timescale of seconds. These advances, coupled with mechanistic and structural studies on key molecular players, such as the MICOS (mitochondrial contact site and cristae organizing system) complex and the dynamin-like GTPase OPA1, have changed our view on mitochondria in a fundamental way. We summarize these recent findings and discuss their functional implications. Mitochondria are dynamic organelles that have essential metabolic and regulatory functions. Earlier studies using electron microscopy (EM) revealed an immense diversity in the architecture of cristae – infoldings of the mitochondrial inner membrane (IM) – in different cells, tissues, bioenergetic and metabolic conditions, and during apoptosis. However, cristae were considered to be largely static entities. Recently, advanced super-resolution techniques have revealed that cristae are independent bioenergetic units that are highly dynamic and remodel on a timescale of seconds. These advances, coupled with mechanistic and structural studies on key molecular players, such as the MICOS (mitochondrial contact site and cristae organizing system) complex and the dynamin-like GTPase OPA1, have changed our view on mitochondria in a fundamental way. We summarize these recent findings and discuss their functional implications. Mitochondria are double-membrane-enclosed organelles of endosymbiotic origin that harbor an outer membrane (OM) and an inner membrane (IM). The immense diversity of mitochondrial ultrastructures was elucidated by electron microscopy (EM) over recent decades, and various models of cristae organization have been put forward [1.Zick M. et al.Cristae formation-linking ultrastructure and function of mitochondria.Biochim. Biophys. Acta. 2009; 1793: 5-19Crossref PubMed Scopus (0) Google Scholar]. The use of 3D electron tomography (ET) in the 1990s to decipher cristae structure by Terry Frey and Carmen Mannella led to seminal contributions that mark a shift in our view on cristae organization [2.Mannella C.A. et al.Reconsidering mitochondrial structure: new views of an old organelle.Trends Biochem. Sci. 1997; 22: 37-38Abstract Full Text PDF PubMed Scopus (102) Google Scholar, 3.Frey T.G. Mannella C.A. The internal structure of mitochondria.Trends Biochem. Sci. 2000; 25: 319-324Abstract Full Text Full Text PDF PubMed Scopus (499) Google Scholar, 4.Frey T.G. et al.Insight into mitochondrial structure and function from electron tomography.Biochim. Biophys. Acta. 2002; 1555: 196-203Crossref PubMed Scopus (0) Google Scholar]. Cristae were no longer seen as extended, broad infoldings of the IM but instead were connected to the inner boundary membrane (IBM; see Glossary) by pore- or slit-like structures called crista junctions (CJs) (Box 1). CJs were proposed to act as diffusion barriers for membrane and soluble proteins, metabolites, and even protons [4.Frey T.G. et al.Insight into mitochondrial structure and function from electron tomography.Biochim. Biophys. Acta. 2002; 1555: 196-203Crossref PubMed Scopus (0) Google Scholar,5.Mannella C.A. et al.Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications.IUBMB Life. 2001; 52: 93-100Crossref PubMed Scopus (0) Google Scholar]. Later studies confirmed that the IM is indeed subcompartmentalized [6.Vogel F. et al.Dynamic subcompartmentalization of the mitochondrial inner membrane.J. Cell Biol. 2006; 175: 237-247Crossref PubMed Scopus (237) Google Scholar, 7.Wurm C.A. Jakobs S. Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast.FEBS Lett. 2006; 580: 5628-5634Crossref PubMed Scopus (0) Google Scholar, 8.Gilkerson R.W. et al.The cristal membrane of mitochondria is the principal site of oxidative phosphorylation.FEBS Lett. 2003; 546: 355-358Crossref PubMed Scopus (174) Google Scholar]. Despite these advances and the conception that cristae are variable in structure, cristae were considered to be static under a particular physiological condition. This view was certainly biased because mitochondrial ultrastructure was studied using EM at high spatial resolution, although in fixed sample specimens. The static nature of cristae was propagated in textbooks for the past 60 years.Box 1Ultrastructure of the Mitochondrial Inner MembraneIn 1950s, the application of EM to mitochondria by Claude, Palade, and Sjöstrand ignited major interest in mitochondrial ultrastructures [92.Rasmussen N. Mitochondrial structure and the practice of cell biology in the 1950s.J. Hist. Biol. 1995; 28: 381-429Crossref PubMed Scopus (0) Google Scholar]. The inner membrane (IM) is subdivided into the inner boundary membrane (IBM) and the cristae membrane (CM), where the latter invaginates towards the matrix whereas the IBM runs parallel to the outer membrane (OM). Cristae have diverse shapes depending on the cell type, bioenergetic status, and developmental stages [1.Zick M. et al.Cristae formation-linking ultrastructure and function of mitochondria.Biochim. Biophys. Acta. 2009; 1793: 5-19Crossref PubMed Scopus (0) Google Scholar,26.Zerbes R.M. et al.Mitofilin complexes: conserved organizers of mitochondrial membrane architecture.Biol. Chem. 2012; 393: 1247-1261Crossref PubMed Scopus (72) Google Scholar]. Several models of IM organization have been proposed: according to the 'baffle model' the IM possesses regularly spaced parallel ridges that invaginate towards the matrix, whereas the 'septum model' suggests that the IM has septae that separate the matrix into many distinct compartments [93.Sjöstrand F.S. Electron microscopy of mitochondria and cytoplasmic double membranes: ultra-structure of rod-shaped mitochondria.Nature. 1953; 171: 30-31Crossref PubMed Scopus (0) Google Scholar,94.Sjöstrand F.S. The ultrastructure of cells as revealed by the electron microscope.in: Bourne G.H. Danielli J.F. International Review of Cytology. Academic Press, 1956: 455-533Google Scholar]. Daems and Wisse described that cristae were attached to the IBM by narrow feet termed 'pediculi cristae' [95.Daems W.T. Wisse E. Shape and attachment of the cristae mitochondriales in mouse hepatic cell mitochondria.J. Ultrastruct. Res. 1966; 16: 123-140Crossref PubMed Google Scholar]. Visualization of the 3D ultrastructure by electron tomography (ET) confirmed the latter view and showed that cristae are invaginated by narrow, pore-like openings termed crista junctions (CJs) [3.Frey T.G. Mannella C.A. The internal structure of mitochondria.Trends Biochem. Sci. 2000; 25: 319-324Abstract Full Text Full Text PDF PubMed Scopus (499) Google Scholar,87.Perkins G. et al.Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts.J. Struct. Biol. 1997; 119: 260-272Crossref PubMed Scopus (0) Google Scholar]. Alterations of ultrastructure were observed in isolated mitochondria by Charles Hackenbrock in the 1960s, where mitochondria adopted an 'orthodox state' (state IV respiration) under ADP-limiting conditions and a 'condensed state' (state III respiration) after addition of ADP. 'Orthodox state' mitochondria exhibit low oxygen consumption compared with the matrix 'condensed state'. The latter displayed increased continuity of the IM, decreased matrix volume, and increased intracristal space (ICS) volume compared with the orthodox state. However, massive reorganization of the mitochondrial internal structure between the two states could only be observed in 2D sections at that time. The development of ET confirmed these observations in 3D [3.Frey T.G. Mannella C.A. The internal structure of mitochondria.Trends Biochem. Sci. 2000; 25: 319-324Abstract Full Text Full Text PDF PubMed Scopus (499) Google Scholar,5.Mannella C.A. et al.Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications.IUBMB Life. 2001; 52: 93-100Crossref PubMed Scopus (0) Google Scholar,11.Mannella C.A. Structure and dynamics of the mitochondrial inner membrane cristae.Biochim. Biophys. Acta. 2006; 1763: 542-548Crossref PubMed Scopus (245) Google Scholar]. The role of CJs as diffusion barriers resulting in a spatial segregation of proteins localized at the IBM and CM obtained strong support from several studies [6.Vogel F. et al.Dynamic subcompartmentalization of the mitochondrial inner membrane.J. Cell Biol. 2006; 175: 237-247Crossref PubMed Scopus (237) Google Scholar, 7.Wurm C.A. Jakobs S. Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast.FEBS Lett. 2006; 580: 5628-5634Crossref PubMed Scopus (0) Google Scholar, 8.Gilkerson R.W. et al.The cristal membrane of mitochondria is the principal site of oxidative phosphorylation.FEBS Lett. 2003; 546: 355-358Crossref PubMed Scopus (174) Google Scholar]. This included large-scale immunogold EM analysis of the IM demonstrating that the IBM is indeed enriched in proteins participating in mitochondrial fusion and protein import, whereas the CM is enriched in proteins belonging to Fe–S cluster biogenesis, mitochondrial protein synthesis, and OXPHOS [6.Vogel F. et al.Dynamic subcompartmentalization of the mitochondrial inner membrane.J. Cell Biol. 2006; 175: 237-247Crossref PubMed Scopus (237) Google Scholar]. Dimerization of F1Fo ATP synthase is known to be required for cristae formation [1.Zick M. et al.Cristae formation-linking ultrastructure and function of mitochondria.Biochim. Biophys. Acta. 2009; 1793: 5-19Crossref PubMed Scopus (0) Google Scholar], and these dimers (and rows of dimers) are located at the edges of tightly curved cristae, whereas complex I is primarily located in flat mitochondrial membranes [70.Davies K.M. et al.Macromolecular organization of ATP synthase and complex I in whole mitochondria.Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 14121-14126Crossref PubMed Scopus (261) Google Scholar]. In 1950s, the application of EM to mitochondria by Claude, Palade, and Sjöstrand ignited major interest in mitochondrial ultrastructures [92.Rasmussen N. Mitochondrial structure and the practice of cell biology in the 1950s.J. Hist. Biol. 1995; 28: 381-429Crossref PubMed Scopus (0) Google Scholar]. The inner membrane (IM) is subdivided into the inner boundary membrane (IBM) and the cristae membrane (CM), where the latter invaginates towards the matrix whereas the IBM runs parallel to the outer membrane (OM). Cristae have diverse shapes depending on the cell type, bioenergetic status, and developmental stages [1.Zick M. et al.Cristae formation-linking ultrastructure and function of mitochondria.Biochim. Biophys. Acta. 2009; 1793: 5-19Crossref PubMed Scopus (0) Google Scholar,26.Zerbes R.M. et al.Mitofilin complexes: conserved organizers of mitochondrial membrane architecture.Biol. Chem. 2012; 393: 1247-1261Crossref PubMed Scopus (72) Google Scholar]. Several models of IM organization have been proposed: according to the 'baffle model' the IM possesses regularly spaced parallel ridges that invaginate towards the matrix, whereas the 'septum model' suggests that the IM has septae that separate the matrix into many distinct compartments [93.Sjöstrand F.S. Electron microscopy of mitochondria and cytoplasmic double membranes: ultra-structure of rod-shaped mitochondria.Nature. 1953; 171: 30-31Crossref PubMed Scopus (0) Google Scholar,94.Sjöstrand F.S. The ultrastructure of cells as revealed by the electron microscope.in: Bourne G.H. Danielli J.F. International Review of Cytology. Academic Press, 1956: 455-533Google Scholar]. Daems and Wisse described that cristae were attached to the IBM by narrow feet termed 'pediculi cristae' [95.Daems W.T. Wisse E. Shape and attachment of the cristae mitochondriales in mouse hepatic cell mitochondria.J. Ultrastruct. Res. 1966; 16: 123-140Crossref PubMed Google Scholar]. Visualization of the 3D ultrastructure by electron tomography (ET) confirmed the latter view and showed that cristae are invaginated by narrow, pore-like openings termed crista junctions (CJs) [3.Frey T.G. Mannella C.A. The internal structure of mitochondria.Trends Biochem. Sci. 2000; 25: 319-324Abstract Full Text Full Text PDF PubMed Scopus (499) Google Scholar,87.Perkins G. et al.Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts.J. Struct. Biol. 1997; 119: 260-272Crossref PubMed Scopus (0) Google Scholar]. Alterations of ultrastructure were observed in isolated mitochondria by Charles Hackenbrock in the 1960s, where mitochondria adopted an 'orthodox state' (state IV respiration) under ADP-limiting conditions and a 'condensed state' (state III respiration) after addition of ADP. 'Orthodox state' mitochondria exhibit low oxygen consumption compared with the matrix 'condensed state'. The latter displayed increased continuity of the IM, decreased matrix volume, and increased intracristal space (ICS) volume compared with the orthodox state. However, massive reorganization of the mitochondrial internal structure between the two states could only be observed in 2D sections at that time. The development of ET confirmed these observations in 3D [3.Frey T.G. Mannella C.A. The internal structure of mitochondria.Trends Biochem. Sci. 2000; 25: 319-324Abstract Full Text Full Text PDF PubMed Scopus (499) Google Scholar,5.Mannella C.A. et al.Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications.IUBMB Life. 2001; 52: 93-100Crossref PubMed Scopus (0) Google Scholar,11.Mannella C.A. Structure and dynamics of the mitochondrial inner membrane cristae.Biochim. Biophys. Acta. 2006; 1763: 542-548Crossref PubMed Scopus (245) Google Scholar]. The role of CJs as diffusion barriers resulting in a spatial segregation of proteins localized at the IBM and CM obtained strong support from several studies [6.Vogel F. et al.Dynamic subcompartmentalization of the mitochondrial inner membrane.J. Cell Biol. 2006; 175: 237-247Crossref PubMed Scopus (237) Google Scholar, 7.Wurm C.A. Jakobs S. Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast.FEBS Lett. 2006; 580: 5628-5634Crossref PubMed Scopus (0) Google Scholar, 8.Gilkerson R.W. et al.The cristal membrane of mitochondria is the principal site of oxidative phosphorylation.FEBS Lett. 2003; 546: 355-358Crossref PubMed Scopus (174) Google Scholar]. This included large-scale immunogold EM analysis of the IM demonstrating that the IBM is indeed enriched in proteins participating in mitochondrial fusion and protein import, whereas the CM is enriched in proteins belonging to Fe–S cluster biogenesis, mitochondrial protein synthesis, and OXPHOS [6.Vogel F. et al.Dynamic subcompartmentalization of the mitochondrial inner membrane.J. Cell Biol. 2006; 175: 237-247Crossref PubMed Scopus (237) Google Scholar]. Dimerization of F1Fo ATP synthase is known to be required for cristae formation [1.Zick M. et al.Cristae formation-linking ultrastructure and function of mitochondria.Biochim. Biophys. Acta. 2009; 1793: 5-19Crossref PubMed Scopus (0) Google Scholar], and these dimers (and rows of dimers) are located at the edges of tightly curved cristae, whereas complex I is primarily located in flat mitochondrial membranes [70.Davies K.M. et al.Macromolecular organization of ATP synthase and complex I in whole mitochondria.Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 14121-14126Crossref PubMed Scopus (261) Google Scholar]. In the 1960s, Charles Hackenbrock observed that addition of ADP could reversibly change the IM connectivity coupled with changes in mitochondrial matrix volume in isolated rat liver mitochondria [9.Hackenbrock C.R. 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. 1966; 30: 269-297Crossref PubMed Google Scholar,10.Hackenbrock C.R. Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states.Proc. Natl. Acad. Sci. U. S. A. 1968; 61: 598-605Crossref PubMed Google Scholar], and this was corroborated using 3D ET experiments almost three decades later [3.Frey T.G. Mannella C.A. The internal structure of mitochondria.Trends Biochem. Sci. 2000; 25: 319-324Abstract Full Text Full Text PDF PubMed Scopus (499) Google Scholar,5.Mannella C.A. et al.Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications.IUBMB Life. 2001; 52: 93-100Crossref PubMed Scopus (0) Google Scholar,11.Mannella C.A. Structure and dynamics of the mitochondrial inner membrane cristae.Biochim. Biophys. Acta. 2006; 1763: 542-548Crossref PubMed Scopus (245) Google Scholar]. The latter studies also led to the proposal that cristae membrane (CM) reorganization might involve membrane fusion and fission events [5.Mannella C.A. et al.Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications.IUBMB Life. 2001; 52: 93-100Crossref PubMed Scopus (0) Google Scholar]. In addition, induction of apoptosis was accompanied by changes in the IM shape, connectivity, and matrix volume [12.Scorrano L. et al.A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis.Dev. Cell. 2002; 2: 55-67Abstract Full Text Full Text PDF PubMed Scopus (805) Google Scholar], which strongly suggested that cristae can dynamically change their structure. Hence, there were clear indications that CM remodeling can be induced by altered physiological conditions. The use of advanced super-resolution (SR) nanoscopy (Box 2) in recent studies gave us a glimpse of CM dynamics in living cells [13.Kondadi A.K. et al.Cristae undergo continuous cycles of membrane remodelling in a MICOS-dependent manner.EMBO Rep. 2020; 21e49776Crossref PubMed Scopus (0) Google Scholar, 14.Wang C. et al.A photostable fluorescent marker for the superresolution live imaging of the dynamic structure of the mitochondrial cristae.Proc. Natl. Acad. Sci. U. S. A. 2019; 116: 15817-15822Crossref PubMed Scopus (0) Google Scholar, 15.Stephan T. et al.Live-cell STED nanoscopy of mitochondrial cristae.Sci. Rep. 2019; 912419Crossref PubMed Scopus (0) Google Scholar, 16.Huang X. et al.Fast, long-term, super-resolution imaging with Hessian structured illumination microscopy.Nat. Biotechnol. 2018; 36: 451-459Crossref PubMed Scopus (91) Google Scholar]. Several important scientific contributions illustrating the paradigm changes in cristae architecture and dynamics are outlined in Table 1. In this review we discuss recent advances demonstrating novel aspects of the dynamic nature of cristae and CJs and its implications for bioenergetics and metabolism. This is preceded by an updated overview on the molecular basis for cristae and CJ formation involving key molecular players, including the mitochondrial contact site and cristae organizing system (MICOS) complex, optic atrophy type 1 (OPA1), F1Fo ATP synthase, and the lipid microenvironment.Box 2Microscopy Techniques Used for Resolving Mitochondrial MembranesThe different imaging techniques are reviewed in Table I and representative images are shown in Figure I.Table IImaging Techniques for Visualizing Mitochondrial MembranesMicroscopy techniqueDescriptionAdvantageLimitationElectron microscopy (EM)An electron beam is used to illuminate a sample to obtain high-resolution images of biological structures that are differentiated based on their local electron densityNanometer-range resolution in xy (~1–10 nm)Fixed samples, limited resolution in z, prone to artefacts caused by sample preparationElectron tomography (ET)A 3D imaging technique, based on EM, for imaging a sample by reconstruction of 2D images acquired from a wide range of viewing angles3D images are acquired at nanometer resolution (~1–10 nm)Fixed samples of limited thickness (~200–350 nm), extensive and time-consuming data processingAiryscan microscopyExtended-resolution confocal fluorescence microscopy technique using multi-detection elements comprising smaller pinholes sizes. A combination of robust deconvolution reconstruction and pixel-rearrangement principles are applied to enhance the spatial resolution and signal-to-noise ratioFast, easily adaptable to existing top-end confocal microscopes, good signal-to-noise ratio, live-cell optionsThe improvement of resolution relative to confocal microscopes is only up to 1.7-foldStructured illumination microscopy (SIM)SIM (linear) is an extended-resolution technique in which images are analytically processed and reconstructed using the structured illumination principle that is based on high spatial frequency laser interferenceLow phototoxicity good for live-cell imaging, high-throughput applications, easy multicolor imagingPost-processing required, risk of reconstruction artefactsStochastic optical reconstruction microscopy (STORM) and photoactivated localization microscopy (PALM)A SR technique that relies on stochastic activation of photoactivable or photoconvertible fluorophores. The process is sequentially repeated to reconstruct the image determined by position of the photons detected from activation eventsCan be implemented with a standard microscope set-upPost processing required, reconstruction artefacts may occurStimulated emission depletion (STED)A SR technique that exploits selective (stimulated) depletion of a fluorophore using a strong laser to decrease the area of illumination of the sample to break the diffraction limit of lightSR images are directly obtained. Live-imaging at high resolution is possibleSlow acquisition, phototoxicity; multicolor imaging choices are restricted because of the limited availability of STED-compatible dyes3D minimal emission fluxes (3D MINFLUX)MINFLUX combines the advantages of the PALM/STROM, where the molecules can be stochastically turned on or off, and the STED principle by employing a donut laser to determine localizationSuper-high resolution in the range of a few nanometers is achievableFixed samples, post-processing algorithms are required Open table in a new tab Table 1Landmarks in Mitochondrial Ultrastructure: Organelle to Cristae DynamicsYearDiscoveryKey techniquesRefs1841 and 1857First descriptions of (pale) grain-like structures in muscle sectionsBright-field microscopy[108.Henle J. Allgemeine Anatomie. Lehre von den Mischungs- und Formbestandtheilen des menschlichen Körpers.in: von Sömmering S.T. Vom Baue des menschlichen Körpers. Verlag von Leopold Voß, 1841: 573-612Google Scholar,109.Kölliker A. Einige Bemerkungen über die Endigungen der Hautnerven und den Bau der Muskeln.in: von Siebold C.T. Zeitschrift für wissenschaftliche Zoologie. Verlag von Wilhelm Engelmann, 1857: 311-325Google Scholar]1890Richard Altmann's initial description of mitochondria as bioblasts or cell granulesBright-field microscopy[110.Altmann R. Die Elementarorganismen und ihre Beziehungen zu den Zellen. Veit and Comp, 1890Google Scholar]1898Coining of the word 'mitochondria' by Carl Benda[111.Benda C. Ueber die Spermatogenese der Vertebraten und höherer Evertebraten, II. Theil: Die Histiogenese der Spermien.Arch. Anat. Physiol. 1898; 73: 393-398Google Scholar]1914Margaret Lewis and Warren Lewis proposed the existence of mitochondrial dynamicsBright-field microscopy[112.Lewis M.R. Lewis W.H. Mitochondria in tissue culture.Science. 1914; 39: 330-333Crossref PubMed Google Scholar]1952George Palade unraveled mitochondrial ultrastructureEM[113.Palade G.E. The fine structure of mitochondria.Anat. 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Res. 1966; 16: 123-140Crossref PubMed Google Scholar]1966Charles Hackenbrock showed that isolated mitochondria exist in 'orthodox' and matrix 'condensed' statesEM[9.Hackenbrock C.R. 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. 1966; 30: 269-297Crossref PubMed Google Scholar]1994Discovery of mitochondrial dynamics including fission and fusionFluorescence microscopy[115.Bereiter-Hahn J. Voth M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria.Microsc. Res. Tech. 1994; 27: 198-219Crossref PubMed Google Scholar]1994 to 1997Descriptions of tubular connections between cristae and IBM by Terrence Frey and Carmen Mannella. The term 'crista junctions' was coined in 1997ET[87.Perkins G. et al.Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts.J. Struct. Biol. 1997; 119: 260-272Crossref PubMed Scopus (0) Google Scholar,116.Mannella C.A. et al.The internal compartmentation of rat-liver mitochondria: tomographic study using the high-voltage transmission electron microscope.Microsc. Res. Tech. 1994; 27: 278-283Crossref PubMed Google Scholar]2002Apoptosis-dependent cristae remodeling was observed accompanied by IM reorganization and Cyt c redistributionET[12.Scorrano L. et al.A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis.Dev. 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