Summary
The mitochondrion has been mainly given attention as a self-reproductive and respiratory organelle. We report here that the mitochondrion may participate in the formation of a cell-type-specific organelle, coupling with the Golgi complex. During the development ofDictyostelium discoideum, the two types of cells, i.e., the anterior prestalk cells and the posterior prespore cells form a polarized cell mass. Prespore differentiation is characterized by the presence of unique vacuoles named PSVs (prespore-specific vacuoles) in the cytoplasm. Thus the PSV is the most essential organelle to understand the structural basis of cell differention in this organism. In differentiating prespore cells, the mitochondrion exerts a remarkable transformation to form a sort of vacuole (M-vacuole). Using a PSV specific antibody, it was immunocytochemically shown that a PSV antigen (C-10) is localized in the M-vacuole as well as in the lining membrane of PSV. Interestingly, the C-10 antigen was also noticed in the Golgi cisternae that had fused with M-vacuole. Based on these findings, we propose here a promising model which suggests how both mitochondria and Golgi cisternae may be coordinately involved in the PSV formation. This model will provide a new aspect of mitochondrial functions in cell differentiation.
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References
Bonner JT (1947) Evidence for the formation of cell aggregates by chemotaxis in the development of the cellular slime moldDictyostelium discoideum. J Exp Zool 106: 1–26
Galfre G, Howe SC, Milstein C, Butcer GW, Howard JC (1977) Antibody to major histocompatibility antigens produced by hybrid cell lines. Nature 226: 550–552
Gerisch G (1987) Cyclic AMP and other signals controlling cell development and differentiation inDictyostelium. Annu Rev Biochem 56: 853–879
Haberstroh L, Galino J, Firtel RA (1991) Developmental and spatial regulation of aDictyostelium prespore gene: cis-acting elements and a cAMP-induced, developmentally regulated DNA binding activity. Development 113: 947–958
Hohl HR, Hamamoto ST (1969) Ultrastructure of spore differentiation inDictyostelium discoideum: the spore vacuole. J Ultrastruct Res 26: 442–453
Ikeda A, Takeuchi I (1971) Isolation and characterization of a prespore specific structure of the cellular slime moldDictyostelium discoideum. Dev Growth Differ 13: 221–227
Inouye K (1988) Induction by acid load of the maturation of prestalk cells inDictyostelium discoideum. Development 104: 669–681
Kobayashi S, Okada M (1989) Restoration of pole-cell-forming ability to u. v.-irradiatedDrosophila embryos by injection of mitochondrial IrRNA. Development 107: 733–742
Maeda Y (1971a) Studies on a specific structure in differentiating slime mold cells. Mem Fac Sci Kyoto Univ Ser Biol 4: 97–107
— (1971b) Formation of a prespore specific structure from a mitochondrion during development of the cellular slime moldDictyostelium discoideum. Dev Growth Differ 13: 211–219
—, Takeuchi I (1969) Cell differentiation and fine structures in the development of the cellular slime molds. Dev Growth Differ 11: 232–245
Matsuyama S, Maeda Y (1995) Involvement of cyanide-resistant respiration in cell-type proportioning duringDictyostelium development. Dev Biol 172: 182–191
Massover WH (1971) Intramitochondrial yolk-crystals of frog oocytes. J Cell Biol 48: 266–279
Oyama M. Maeda Y, Takeuchi I (1984) Development of prespore vacuoles inDictyostelium discoideum cells differentiaing in a liquid shake culture. Protoplasma 123: 152–159
Reynolds ES (1963) The use of lead citrate at high pH as an electronopaque stain in electronmicroscopy. J Cell Biol 17: 208–212
Robert D (1969) Cytologie vegetate evolution du guelques cerganites cytoplasmique au cours de la maturation du coosphase deSelaginella kraussiana. C R Acad Sci Ser D 268: 2775–2788
Seligman AM, Karnovsky MJ, Wasserkrug HL, Hanker JS (1968) Nondroplet ultrastructural demonstration of cytochrome oxidase activity with a polymerizing osmiophilic reagent, diaminobenzidine (DAB). J Cell Biol 38: 1–14
Shaulsky G, Loomis WF (1995) Mitochondrial DNA replication but no nuclear DNA replication during development ofDictyostelium. Proc Natl Acad Sci USA 92: 5660–5663
Sternfeld J (1988) Proportion reguration inDictyostelium is altered by oxygen. Differentiation 37: 173–179
Takemoto K, Yamamoto A, Takeuchi I (1985) The origin of prespore vacuole inDictyostelium discoideum cells analysed by electron-microscopic immunocytochemistry and radioautography. J Cell Sci 77: 93–108
Takeuchi I (1960) The correlation of cellular changes with succinic dehydrogenase and cytochrome oxidase activities in the development of the cellular slime molds. Dev Biol 2: 343–366
—, Yabuno K (1970) Disaggregation of slime mold pseudoplasmodia using EDTA and various proteolytic enzymes. Exp Cell Res 61: 183–190
Tasaka M, Maeda Y (1983) Ultrastractural changes of the two types of differentiated cells during migration and early culmination stages ofDictyostelium discoideum. Dev Growth Differ 25: 353–360
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350–4354
Wilcznska Z, Barth C, Fisher PR (1997) Mitochondrial mutation impair signal transduction inDictyostelium discoideum slugs. Biochem Biophys Res Commun 234: 39–43
Williams JG, Duffy KT, Lane DP, McRobbie SJ, Harwood AJ, Traynor D, Kay RR, Jermyn KA (1989) Origins of the prestalk-prespore pattern inDictyostelium development. Cell 59: 1157–1163
Wischnitzer S (1967) Intramitochondrial transformations during oocyte maturation in the mouse. J Morphol 121: 29–45
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Matsuyama, S.I., Maeda, Y. A mitochondrion as the structural basis of the formation of a cell-type-specific organelle inDictyostelium development. Protoplasma 201, 172–179 (1998). https://doi.org/10.1007/BF01287413
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DOI: https://doi.org/10.1007/BF01287413