ARTICLE

ULTRASTRUCTURAL BASES FOR METABOLICALLY LINKED MECHANICAL ACTIVITY IN MITOCHONDRIA : I. Reversible Ultrastructural Changes with Change in Metabolic Steady State in Isolated Liver Mitochondria

Charles R. Hackenbrock ¹

¹ From the Department of Anatomy, College of Physicians and Surgeons, Columbia University, New York.

Dr. Hackenbrock's present address is the Department of Anatomy, The Johns Hopkins University School of Medicine, Baltimore, Maryland

By means of a new "quick-sampling" method, micropellets of mouse liver mitochondria were rapidly prepared for electron microscopy during the recording of steady state metabolism. Reversible ultrastructural changes were found to accompany change in metabolic steady states. The most dramatic reversible ultrastructural change occurs when ADP is added to systems in which only phosphate acceptor is deficient, i.e., during the State IV to State III transition as defined by Chance and Williams. After 15 min in State IV, mitochondria display an "orthodox" ultrastructural appearance as is usually observed after fixation within intact tissue. On transition to State III, a dramatic change in the manner of folding of the inner membrane takes place. In addition, the electron opacity of the matrix increases as the volume of the matrix decreases, but total mitochondrial volume does not appear to change during this transition. This conformation is called "condensed." Isolated mitochondria were found to oscillate between the orthodox and condensed conformations during reversible transitions between State III and State IV. Various significant ultrastructural changes in mitochondria also occur during transitions in other functional states, e.g., when substrate or substrate and acceptor is made limiting. Internal structural flexibility is discussed with respect to structural and functional integrity of isolated mitochondria. Reversible changes in the manner of folding of the inner membrane and in the manner of packing of small granules in the matrix as respiration is activated by ADP represent an ultrastructural basis for metabolically linked mechanical activity in tightly coupled mitochondria.

CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

This article has been cited by other articles:

• Gerencser, A. A., Doczi, J., Torocsik, B., Bossy-Wetzel, E., Adam-Vizi, V. (2008). Mitochondrial Swelling Measurement In Situ by Optimized Spatial Filtering: Astrocyte-Neuron Differences. Biophys. J 95: 2583-2598 [Abstract] [Full Text]  
• Koopman, W. J. H., Distelmaier, F., Hink, M. A., Verkaart, S., Wijers, M., Fransen, J., Smeitink, J. A. M., Willems, P. H. G. M. (2008). Inherited complex I deficiency is associated with faster protein diffusion in the matrix of moving mitochondria. Am. J. Physiol. Cell Physiol. 294: C1124-C1132 [Abstract] [Full Text]  
• Zheng, J.-Y., Tsai, Y.-C., Kadimcherla, P., Zhang, R., Shi, J., Oyler, G. A., Boustany, N. N. (2008). The C-Terminal Transmembrane Domain of Bcl-xL Mediates Changes in Mitochondrial Morphology. Biophys. J 94: 286-297 [Abstract] [Full Text]  
• Yeo, T., Kintner, J, Armand, R, Perez, R, Lewis, L. (2007). Sublethal concentrations of gemcitabine (2',2'-difluorodeoxycytidine) alter mitochondrial ultrastructure and function without reducing mitochondrial DNA content in BxPC-3 human pancreatic carcinoma cells. Hum Exp Toxicol 26: 911-921 [Abstract]  
• Ju, W.-K., Liu, Q., Kim, K.-Y., Crowston, J. G., Lindsey, J. D., Agarwal, N., Ellisman, M. H., Perkins, G. A., Weinreb, R. N. (2007). Elevated Hydrostatic Pressure Triggers Mitochondrial Fission and Decreases Cellular ATP in Differentiated RGC-5 Cells. IOVS 48: 2145-2151 [Abstract] [Full Text]  
• Benard, G., Bellance, N., James, D., Parrone, P., Fernandez, H., Letellier, T., Rossignol, R. (2007). Mitochondrial bioenergetics and structural network organization. J. Cell Sci. 120: 838-848 [Abstract] [Full Text]  
• Benard, G., Faustin, B., Passerieux, E., Galinier, A., Rocher, C., Bellance, N., Delage, J.-P., Casteilla, L., Letellier, T., Rossignol, R. (2006). Physiological diversity of mitochondrial oxidative phosphorylation. Am. J. Physiol. Cell Physiol. 291: C1172-C1182 [Abstract] [Full Text]  
• Bonanni, L., Chachar, M., Jover-Mengual, T., Li, H., Jones, A., Yokota, H., Ofengeim, D., Flannery, R. J., Miyawaki, T., Cho, C.-H., Polster, B. M., Pypaert, M., Hardwick, J. M., Sensi, S. L., Zukin, R. S., Jonas, E. A. (2006). Zinc-dependent multi-conductance channel activity in mitochondria isolated from ischemic brain.. J. Neurosci. 26: 6851-6862 [Abstract] [Full Text]  
• Yu, T., Robotham, J. L., Yoon, Y. (2006). Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc. Natl. Acad. Sci. USA 103: 2653-2658 [Abstract] [Full Text]  
• Celotto, A. M., Frank, A. C., McGrath, S. W., Fergestad, T., Van Voorhies, W. A., Buttle, K. F., Mannella, C. A., Palladino, M. J. (2006). Mitochondrial Encephalomyopathy in Drosophila. J. Neurosci. 26: 810-820 [Abstract] [Full Text]  
• Morse, D. L., Gray, H., Payne, C. M., Gillies, R. J. (2005). Docetaxel induces cell death through mitotic catastrophe in human breast cancer cells. Molecular Cancer Therapeutics 4: 1495-1504 [Abstract] [Full Text]  
• Riva, A., Tandler, B., Loffredo, F., Vazquez, E., Hoppel, C. (2005). Structural differences in two biochemically defined populations of cardiac mitochondria. Am. J. Physiol. Heart Circ. Physiol. 289: H868-H872 [Abstract] [Full Text]  
• Korge, P., Honda, H. M., Weiss, J. N. (2005). K+-dependent regulation of matrix volume improves mitochondrial function under conditions mimicking ischemia-reperfusion. Am. J. Physiol. Heart Circ. Physiol. 289: H66-H77 [Abstract] [Full Text]  
• Powell, K. (2005). Were mitochondrial contractions driving the cellular energy cycle?. JCB 169: 217-218 [Full Text]  
• Wilson, J. D., Bigelow, C. E., Calkins, D. J., Foster, T. H. (2005). Light Scattering from Intact Cells Reports Oxidative-Stress-Induced Mitochondrial Swelling. Biophys. J 88: 2929-2938 [Abstract] [Full Text]  
• John, G. B., Shang, Y., Li, L., Renken, C., Mannella, C. A., Selker, J. M.L., Rangell, L., Bennett, M. J., Zha, J. (2005). The Mitochondrial Inner Membrane Protein Mitofilin Controls Cristae Morphology. Mol. Biol. Cell 16: 1543-1554 [Abstract] [Full Text]  
• Gerencser, A. A., Adam-Vizi, V. (2005). Mitochondrial Ca2+ Dynamics Reveals Limited Intramitochondrial Ca2+ Diffusion. Biophys. J 88: 698-714 [Abstract] [Full Text]  
• Feldkamp, T., Kribben, A., Roeser, N. F., Senter, R. A., Kemner, S., Venkatachalam, M. A., Nissim, I., Weinberg, J. M. (2004). Preservation of complex I function during hypoxia-reoxygenation-induced mitochondrial injury in proximal tubules. Am. J. Physiol. Renal Physiol. 286: F749-F759 [Abstract] [Full Text]  
• Rossignol, R., Gilkerson, R., Aggeler, R., Yamagata, K., Remington, S. J., Capaldi, R. A. (2004). Energy Substrate Modulates Mitochondrial Structure and Oxidative Capacity in Cancer Cells. Cancer Res. 64: 985-993 [Abstract] [Full Text]  
• Seo, Y.-W., Shin, J. N., Ko, K. H., Cha, J. H., Park, J. Y., Lee, B. R., Yun, C.-W., Kim, Y. M., Seol, D.-w., Kim, D.-w., Yin, X.-M., Kim, T.-H. (2003). The Molecular Mechanism of Noxa-induced Mitochondrial Dysfunction in p53-Mediated Cell Death. J. Biol. Chem. 278: 48292-48299 [Abstract] [Full Text]  
• Wagner, O. I., Lifshitz, J., Janmey, P. A., Linden, M., McIntosh, T. K., Leterrier, J.-F. (2003). Mechanisms of Mitochondria-Neurofilament Interactions. J. Neurosci. 23: 9046-9058 [Abstract] [Full Text]  
• Gottlieb, E., Armour, S. M., Thompson, C. B. (2002). Mitochondrial respiratory control is lost during growth factor deprivation. Proc. Natl. Acad. Sci. USA 99: 12801-12806 [Abstract] [Full Text]  
• Boustany, N. N., Drezek, R., Thakor, N. V. (2002). Calcium-Induced Alterations in Mitochondrial Morphology Quantified in Situ with Optical Scatter Imaging. Biophys. J 83: 1691-1700 [Abstract] [Full Text]  
• Chi, M. M.-Y., Hoehn, A., Moley, K. H. (2002). Metabolic changes in the glucose-induced apoptotic blastocyst suggest alterations in mitochondrial physiology. Am. J. Physiol. Endocrinol. Metab. 283: E226-E232 [Abstract] [Full Text]  
• Zhou, R., Vander Heiden, M. G., Rudin, C. M. (2002). Genotoxic Exposure Is Associated with Alterations in Glucose Uptake and Metabolism. Cancer Res. 62: 3515-3520 [Abstract] [Full Text]  
• Jauniaux, E., Watson, A. L., Hempstock, J., Bao, Y.-P., Skepper, J. N., Burton, G. J. (2000). Onset of Maternal Arterial Blood Flow and Placental Oxidative Stress : A Possible Factor in Human Early Pregnancy Failure. Am. J. Pathol. 157: 2111-2122 [Abstract] [Full Text]  
• Cortese, J. D. (1999). Rat liver GTP-binding proteins mediate changes in mitochondrial membrane potential and organelle fusion. Am. J. Physiol. Cell Physiol. 276: C611-C620 [Abstract] [Full Text]  
• Rojo, G., Chamorro, M., Salas, M. L., Vinuela, E., Cuezva, J. M., Salas, J. (1998). Migration of Mitochondria to Viral Assembly Sites in African Swine Fever Virus-Infected Cells. J. Virol. 72: 7583-7588 [Abstract] [Full Text]  
• Jeannot, V., Salmon, J.-M., Deumie, M., Viallet, P. (1997). Intracellular Accumulation of Rhodamine 110 in Single Living Cells. J. Histochem. Cytochem. 45: 403-412 [Abstract] [Full Text]  
• Hill Lucas, J., Emery, D. G., Rosenberg, L. J. (1997). REVIEW {blacksquare} : Physical Injury of Neurons: Important Roles for Sodium and Chloride Ions. Neuroscientist 3: 89-101 [Abstract]  
• You, K (1983). Salicylate and mitochondrial injury in Reye's syndrome. Science 221: 163-165 [Abstract]  
• Askew, J. B. Jr., Fechner, R. E., Bentinck, D. C., Jenson, A. B. (1971). Epithelial and Myoepithelial Oncocytes: Ultrastructural Study of a Salivary Gland Oncocytoma. Arch Otolaryngol Head Neck Surg 93: 46-54 [Abstract]  
• Harris, R. A., Williams, C. H., Caldwell, M., Green, D. E., Valdivia, E. (1969). Energized Configurations of Heart Mitochondria in situ. Science 165: 700-702 [Abstract]  

Home | Help | Feedback | Subscriptions | Archive | Search | Table of Contents