Skip to main content
SpringerLink
Log in

Mitochondrial distribution and inheritance

  • Milti-Author Reviews
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

Mechanisms mediating the inheritance of mitochondria are poorly understood, but recent studies with the yeastsSaccharomyces cerevisiae andSchizosaccharomyces pombe have begun to identify components that facilitate this essential process. These components have been identified through the analysis of conditional yeast mutants that display aberrant mitochondrial distribution at restrictive conditions. The analysis of these mutants has uncovered several novel proteins that are localized either to cytoskeletal structures or to the mitochondria themselves. Many mitochondrial inheritance mutants also show altered mitochondrial morphology and defects in maintenance of the mitochondrial genome. Although some inheritance components and mechanisms appear to function specifically in certain types of cells, other conserved proteins are likely to mediate mitochondrial behavior in all eukaryotic cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Wilson, E. B. (1925) The Cell in Development and Heredity, Macmillan, New York

    Google Scholar 

  2. Palade G. (1983) Membrane biogenesis: an overview. Methods Enzymol.96: 29–40

    Google Scholar 

  3. Schatz G. and Dobberstein B. (1996) Common principles of protein translocation across membranes. Science271: 1519–1526

    PubMed  Google Scholar 

  4. Ryan K. R. and Jensen R. E. (1995) Protein translocation across mitochondrial membranes: what a long, strage trip it is. Cell83: 517–519

    Article  PubMed  Google Scholar 

  5. Johnson L. V., Walsh M. L. and Chen L. B. (1980) Localization of mitochondria in living cells with rhodamine 123. Proc. Natl. Acad. Sci. USA77: 990–994

    PubMed  Google Scholar 

  6. Bakeeva L. E., Chentsov U. S. and Skulachev V. P. (1986) Mitochondrial framework (reticulum mitochondriale) in rat diaphram muscle. Biochim. Biophys. Acta501: 349–369

    Google Scholar 

  7. Schnedl W. (1994) Changes in mitochondria during the cell cycle. Cytobiol.8: 403–411

    Google Scholar 

  8. Stevens B. J. (1977) Variation in number and volume of the mitochondria in yeast according to growth conditions: a study based on serial sectioning and computer graphics reconstruction. Biol. Cell28: 37–56

    Google Scholar 

  9. Blank R. and Arnold C.-G. (1981) Structural changes of mitochondria inChlamydomonas reinhardii after chloramphenicol treatment. Eur. J. Cell Biol.24: 244–251

    PubMed  Google Scholar 

  10. Bereiter-Hahn J. (1976) Dimethylaminostyrylmethylpyridiniumiodine (DASPMI) as a fluorescent probe for mitochondria in situ. Biochim. Biophys. Acta423: 1–14

    PubMed  Google Scholar 

  11. Chen L. B. (1988) Mitochondrial membrane potential in living cells. Ann. Rev. Cell Biol.4: 155–181

    PubMed  Google Scholar 

  12. Koning A. J., Lum P. Y., Williams J. M. and Wright R. (1993) DiOC6 staining reveals organelle structure and dynamics in living yeast cells. Cell Motil. Cytoskeleton25: 111–128

    Article  PubMed  Google Scholar 

  13. Couchman J. R. and Rees D. A. (1982) Organelle-cytoskeleton relationships in fibroblasts: mitochondria, Golgi apparatus and endoplasmic reticulum in phases of movement and growth. Eur. J. Cell Biol.27: 47–54

    PubMed  Google Scholar 

  14. Stevens B (1981) Mitochondrial structure. In: The Molecular Biology of the YeastSaccharomyces cerevisiae, vol. 1, pp. 471–504, Strathern J. N., Jones E. W. and Broach J. R. (eds), Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  15. Bereiter-Hahn J. (1990) Behavior of mitochondria in the living cell. Int. Rev. Cytol.122: 1–64

    PubMed  Google Scholar 

  16. Yaffe M. P. (1996) The division and inheritance of mitochondria. Adv. Mol. Cell Biol.17: 337–346

    Google Scholar 

  17. Thorsness P. E. and Weber E. R. (1996) Escape and migration of nucleic acids between chloroplasts, mitochondria, and the nucleus. Int. Rev. Cytol.165: 207–234

    PubMed  Google Scholar 

  18. Bereiter-Hahn J. and Voth M. (1994) Dynamics of mitochondria in living cells: shape changes, dislocations, fusion and fission of mitochondria Microsc. Res. Tech.27: 198–219

    Article  PubMed  Google Scholar 

  19. Heggeness M. H., Simon M. and Singer S. J. (1978) Association of mitochondria with microtubules in cultured cells. Proc. Natl. Acad. Sci. USA75: 3863–3866

    PubMed  Google Scholar 

  20. Summerhayes I. C., Wong D. and Chen L. B. (1983) Effect of microtubules and intermediate filaments on mitochondrial distribution. J. Cell Sci.61: 87–105

    PubMed  Google Scholar 

  21. David-Ferreira K. L. and David-Ferreira J. F. (1980) Association between intermediate-sized filaments and mitochondria in rat Leidyg cells. Int. Cell Biol. Rep.4: 655–662

    Article  Google Scholar 

  22. Ball E. H. and Singer S. J. (1982) Mitochondria are associated with microtubules and not with intermediate filaments in cultured fibroblasts. Proc. Natl. Acad. Sci. USA79: 123–126

    PubMed  Google Scholar 

  23. Baumann O. and Murphy D. B. (1995) Microtubule-associated movement of mitochondria and small particles inAcanthamoeba castellanii. Cell Motil. Cytoskeleton32: 305–317

    Article  PubMed  Google Scholar 

  24. Steinberg G. and Schliwa M. (1993) Organelle movements in the wild type and wall-less fz;sg;os-1 mutants ofNeurospora crassa are mediated by cytoplasmic microtubules. J. Cell Sci.106: 555–564

    PubMed  Google Scholar 

  25. Vale R. D. (1987) Intracellular transport using microtubule-based motors. Ann. Rev. Cell Biol.3: 347–378

    PubMed  Google Scholar 

  26. McConnell S. J., Stewart L. C., Talin A. and Yaffe M. P. (1990) Temperature-sensitive yeast mutants defective in mitochondrial inheritance. J. Cell Biol.111: 967–976

    Article  PubMed  Google Scholar 

  27. McConnell S. J. and Yaffe M. P. (1992) Nuclear and mitochondrial inheritance in yeast depends on novel cytoplasmic structures defined by the MDM1 protein. J. Cell Biol.118: 385–395

    Article  PubMed  Google Scholar 

  28. McConnell S. J. and Yaffe M. P. (1993) Intermediate filament formation by a yeast protein essential for organelle inheritance. Science260: 687–689

    PubMed  Google Scholar 

  29. Mose-Larsen P., Bravo R., Fey S. J., Small J. V. and Celis J. E. (1982) Putative association of mitochondria with a subpopulation of intermediate-sized filaments in cultured human skin fibroblasts. Cell31: 681–692

    Article  PubMed  Google Scholar 

  30. Shortle D., Novick P. and Botstein D. (1984) Construction and genetic characterization of temperature-sensitive mutant alleles of the yeast actin gene. Proc. Natl. Acad. Sci. USA81: 4889–4893

    PubMed  Google Scholar 

  31. Novick P. and Botstein D. (1985) Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell40: 405–416

    Article  PubMed  Google Scholar 

  32. Drubin D. G., Jones H. D. and Wertman K. F. (1993) Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site. Mol. Biol. Cell4: 1277–1294

    PubMed  Google Scholar 

  33. Smith M. G., Simon V. R., O'Sullivan H. and Pon L. A. (1995) Organelle-cytoskeletal interactions: actin mutations inhibit meiosis-dependent mitochondrial arrangement in the budding yeast Saccharomyces cerevisiae. Mol. Biol. Cell6: 1381–1396

    PubMed  Google Scholar 

  34. Liu H. and Bretscher A. (1989) Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell57: 233–242

    Article  PubMed  Google Scholar 

  35. Lazzarino D. A., Boldogh I., Smith M. G., Rosand J. and Pon L. A. (1994) Yeast mitochondria contain ATP-sensitive, reversible actin-binding activity. Mol. Biol. Cell5: 807–818

    PubMed  Google Scholar 

  36. Simon V. R., Swayne T. C. and Pon L. A. (1995) Actin-dependent mitochondrial motility in mitotic yeast and cell-free systems: identification of a motor activity on the mitochondrial surface. J. Cell Biol.130: 345–354

    Article  PubMed  Google Scholar 

  37. Hirokawa N. (1982) Cross-linker system between neurofilaments, microtubules and membranous organelles in frog axons revealed by the quick-freeze, deep-etch method. J. Cell Biol.94: 129–142

    Article  PubMed  Google Scholar 

  38. Nangaku M., Sato-Yoshitake R., Okada Y., Noda Y., Takemura R., Yamazaki H. et al. (1994) KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell79: 1209–1220

    Article  PubMed  Google Scholar 

  39. Morris R. L. and Hollenbeck P. J. (1995) Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J. Cell Biol.131: 1315–1326

    Article  PubMed  Google Scholar 

  40. Huffaker T. C., Thomas J. H. and Botstein D. (1988) Diverse effects ofβ-tubulin mutations on microtubule formation and function. J. Cell Biol.106: 1997–2010

    Article  PubMed  Google Scholar 

  41. Jacobs C. W., Adams A. E. M., Szaniszlo P. J. and Pringle J. R. (1988) Functions of microtubules in theSaccharomyces cerevisiae cell cycle. J. Cell Biol.107: 1409–1426

    Article  PubMed  Google Scholar 

  42. Yaffe M. P., Harata D., Verde F., Eddison M., Toda T. and Nurse P. (1996) Microtubules mediate mitochondrial distribution in fission yeast. Proc. Natl. Acad. Sci. USA93: 11664–11668

    Article  PubMed  Google Scholar 

  43. Yaffe M. P. and Schatz G. (1984) The future of mitochondrial research. Trends Biochem. Sci.9: 179–181

    Article  Google Scholar 

  44. Sogo L. F. and Yaffe M. P. (1994) Regulation of mitochondrial morphology and inheritance by Mdm 10p, a protein of the mitochondrial outer membrane. J. Cell Biol.126: 1361–1373

    PubMed  Google Scholar 

  45. Burgess S. M., Delannoy M. and Jensen R. E. (1994)MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. J. Cell Biol.126: 1375–1391

    Article  PubMed  Google Scholar 

  46. Myers A. M., Pape L. K. and Tzagoloff A. (1985) Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes inSaccharomyces cerevisiae. EMBO J.4: 2087–2092

    PubMed  Google Scholar 

  47. Jones B. A. and Fangman W. L. (1992) Mitochondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin. Genes Dev.6: 380–389

    PubMed  Google Scholar 

  48. Guan K., Farh L., Marshall T. K. and Deschenes R. J. (1993) Normal mitochondrial structure and genome maintenance in yeast requires the dynamin-like product of the MGM1 gene. Curr. Genet.24: 141–148

    Article  PubMed  Google Scholar 

  49. Vallee R. B. (1992) Dynamin: motor protein or regulatory GTPase. J. Muscle Res. Cell Motil.13: 493–496

    Article  PubMed  Google Scholar 

  50. Shpetner H. S. and Vallee R. B. (1992) Dynamin is a GTPase stimulated to high levels of activity by microtubules. Nature355: 733–735

    Article  PubMed  Google Scholar 

  51. Thorsness P. E. and Fox T. D. (1993) Nuclear mutations inSaccharomyces cerevisiae that affect the escape of mitochondrial DNA from mitochondria to the nucleus. Genetics134: 21–28

    PubMed  Google Scholar 

  52. Thorsness P. E., White K. H. and Fox T. D. (1993) Inactivation of YME1, a member of theftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria inSaccharomyces cerevisiae. Mol. Cell. Biol.13: 5418–5426

    PubMed  Google Scholar 

  53. Campbell C. L., Tanaka N., White K. H. and Thorsness P. E. (1994) Mitochondrial morphological and functional defects in yeast caused byyme1 are suppressed by mutation of a 26S protease subunit homologue. Mol. Biol. Cell5: 899–905

    PubMed  Google Scholar 

  54. Weber E. R., Hanekamp T. and Thorsness P. E. (1996) Biochemical and functional analysis of theYME1 gene product, an ATP and zinc-dependent mitochondrial protease fromS. cerevisiae. Mol. Biol. Cell7: 307–317

    PubMed  Google Scholar 

  55. Stewart L. C. and Yaffe M. P. (1991) A role for unsaturated fatty acids in mitochondrial movement and inheritance. J. Cell Biol.115: 1249–1257

    Article  PubMed  Google Scholar 

  56. Azpiroz R. and Butow R. A. (1993) Patterns of mitochondrial sorting in yeast zygotes. Mol. Biol. Cell.4: 21–36

    PubMed  Google Scholar 

  57. Miyakawa I., Aoi H., Sando N. and Kuroiwa T. (1984) Fluorescence microscopic studies of mitochondrial nucleoids during meiosis and sporulation in the yeast,Saccharomyces cerevisiae. J. Cell Sci.66: 21–38

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of California, 92093-0347, San Diego, La Jolla, California, USA

    K. H. Berger & M. P. Yaffe

Authors
  1. K. H. Berger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. P. Yaffe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. P. Yaffe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berger, K.H., Yaffe, M.P. Mitochondrial distribution and inheritance. Experientia 52, 1111–1116 (1996). https://doi.org/10.1007/BF01952109

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01952109

Key words

Search

Navigation