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J Nunnari, WF Marshall, A Straight, A Murray, JW Sedat and P Walter
Department of Biochemistry and Biophysics, University of California Medical School, San Francisco 94143-0448, USA.
To gain insight into the process of mitochondrial transmission in yeast, we directly labeled mitochondrial proteins and mitochondrial DNA (mtDNA) and observed their fate after the fusion of two cells. To this end, mitochondrial proteins in haploid cells of opposite mating type were labeled with different fluorescent dyes and observed by fluorescence microscopy after mating of the cells. Parental mitochondrial protein markers rapidly redistributed and colocalized throughout zygotes, indicating that during mating, parental mitochondria fuse and their protein contents intermix, consistent with results previously obtained with a single parentally derived protein marker. Analysis of the three-dimensional structure and dynamics of mitochondria in living cells with wide-field fluorescence microscopy indicated that mitochondria form a single dynamic network, whose continuity is maintained by a balanced frequency of fission and fusion events. Thus, the complete mixing of mitochondrial proteins can be explained by the formation of one continuous mitochondrial compartment after mating. In marked contrast to the mixing of parental mitochondrial proteins after fusion, mtDNA (labeled with the thymidine analogue 5-bromodeoxyuridine) remained distinctly localized to one half of the zygotic cell. This observation provides a direct explanation for the genetically observed nonrandom patterns of mtDNA transmission. We propose that anchoring of mtDNA within the organelle is linked to an active segregation mechanism that ensures accurate inheritance of mtDNA along with the organelle.
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H. Sesaki and R. E. Jensen Division versus Fusion: Dnm1p and Fzo1p Antagonistically Regulate Mitochondrial Shape J. Cell Biol., November 15, 1999; 147(4): 699 - 706. [Abstract] [Full Text] [PDF]
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C. T. Moraes, L. Kenyon, and H. Hao Mechanisms of Human Mitochondrial DNA Maintenance: The Determining Role of Primary Sequence and Length over Function Mol. Biol. Cell, October 1, 1999; 10(10): 3345 - 3356. [Abstract] [Full Text]
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S. Meeusen, Q. Tieu, E. Wong, E. Weiss, D. Schieltz, J. R. Yates, and J. Nunnari Mgm101p Is a Novel Component of the Mitochondrial Nucleoid That Binds DNA and Is Required for the Repair of Oxidatively Damaged Mitochondrial DNA J. Cell Biol., April 19, 1999; 145(2): 291 - 304. [Abstract] [Full Text] [PDF]
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J. D. Cortese Rat liver GTP-binding proteins mediate changes in mitochondrial membrane potential and organelle fusion Am J Physiol Cell Physiol, March 1, 1999; 276(3): C611 - C620. [Abstract] [Full Text] [PDF]
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C. E. Johnson and P. T. Englund Changes in Organization of Crithidia fasciculata Kinetoplast DNA Replication Proteins during the Cell Cycle J. Cell Biol., November 16, 1998; 143(4): 911 - 919. [Abstract] [Full Text] [PDF]
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G. J. Hermann, J. W. Thatcher, J. P. Mills, K. G. Hales, M. T. Fuller, J. Nunnari, and J. M. Shaw Mitochondrial Fusion in Yeast Requires the Transmembrane GTPase Fzo1p J. Cell Biol., October 19, 1998; 143(2): 359 - 373. [Abstract] [Full Text] [PDF]
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T. Rinaldi, C. Ricci, D. Porro, M. Bolotin-Fukuhara, and L. Frontali A Mutation in a Novel Yeast Proteasomal Gene, RPN11/MPR1, Produces a Cell Cycle Arrest, Overreplication of Nuclear and Mitochondrial DNA, and an Altered Mitochondrial Morphology Mol. Biol. Cell, October 1, 1998; 9(10): 2917 - 2931. [Abstract] [Full Text]
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K. Okamoto, P. S. Perlman, and R. A. Butow The Sorting of Mitochondrial DNA and Mitochondrial Proteins in Zygotes: Preferential Transmission of Mitochondrial DNA to the Medial Bud J. Cell Biol., August 10, 1998; 142(3): 613 - 623. [Abstract] [Full Text] [PDF]
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D. Rapaport, M. Brunner, W. Neupert, and B. Westermann Fzo1p Is a Mitochondrial Outer Membrane Protein Essential for the Biogenesis of Functional Mitochondria in Saccharomyces cerevisiae J. Biol. Chem., August 7, 1998; 273(32): 20150 - 20155. [Abstract] [Full Text] [PDF]
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S. Isenmann, Y. Khew-Goodall, J. Gamble, M. Vadas, and B. W. Wattenberg A Splice-Isoform of Vesicle-associated Membrane Protein-1 (VAMP-1) Contains a Mitochondrial Targeting Signal Mol. Biol. Cell, July 1, 1998; 9(7): 1649 - 1660. [Abstract] [Full Text]
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O. Zelenaya-Troitskaya, S. M. Newman, K. Okamoto, P. S. Perlman, and R. A. Butow Functions of the High Mobility Group Protein, Abf2p, in Mitochondrial DNA Segregation, Recombination and Copy Number in Saccharomyces cerevisiae Genetics, April 1, 1998; 148(4): 1763 - 1776. [Abstract] [Full Text] [PDF]
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A. D. Roeder, G. J. Hermann, B. R. Keegan, S. A. Thatcher, and J. M. Shaw Mitochondrial Inheritance Is Delayed in Saccharomyces cerevisiae Cells Lacking the Serine/Threonine Phosphatase PTC1 Mol. Biol. Cell, April 1, 1998; 9(4): 917 - 930. [Abstract] [Full Text]
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S. Fields, M. Conrad, and M Clarke The S. cerevisiae CLU1 and D. discoideum cluA genes are functional homologues that influence mitochondrial morphology and distribution J. Cell Sci., January 6, 1998; 111(12): 1717 - 1727. [Abstract] [PDF]
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