Antisense RNA inhibition of the β subunit of the Dictyostelium discoideum mitochondrial processing peptidase induces the expression of mitochondrial proteins

Bioscience, Biotechnology and Biochemistry

Volumn 72, Issue 7, 2008, Pages 1836-1846

  Nagayama, Koki ^a,b   Itono, Shiori ^b   Yoshida, Takashi ^b   Ishiguro, Sei Ichi ^b   Ochiai, Hiroshi ^b,c   Ohmachi, Tetsuo ^b  

^a IWATE UNIVERSITY   (Japan)

^b HIROSAKI UNIVERSITY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Antisense RNA; Dictyostelium discoideum; Mitochondrial processing peptidase; Retrograde signaling

Indexed keywords

GENE EXPRESSION; LIFE CYCLE; MATRIX ALGEBRA; NUCLEIC ACIDS; PROTEINS;

ANTISENSE RNA; CDNA ENCODING; DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; EARLY DEVELOPMENT; MITOCHONDRIAL MATRIX; MITOCHONDRIAL PROTEINS; RETROGRADE SIGNALING; SUBFRACTIONS; TRANSFER OF INFORMATION; WESTERN-BLOT ANALYSIS; WILD-TYPE (WT);

RNA;

COMPLEMENTARY RNA; MESSENGER RNA; METALLOPROTEINASE; MITOCHONDRIAL PROCESSING PEPTIDASE; MITOCHONDRIAL PROTEIN; PROTEIN SUBUNIT;

ANIMAL; ARTICLE; DICTYOSTELIUM; DRUG ANTAGONISM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; PHYSIOLOGY;

ANIMALS; DICTYOSTELIUM; GENE EXPRESSION REGULATION; METALLOENDOPEPTIDASES; MITOCHONDRIAL PROTEINS; PROTEIN SUBUNITS; RNA, ANTISENSE; RNA, MESSENGER;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM;

EID: 47949083495     PISSN: 09168451     EISSN: 13476947     Source Type: Journal    
DOI: 10.1271/bbb.80106     Document Type: Article

References (48)

1. Newmeyer, D. D., and Ferguson-Miller, S., Mitochondria: releasing power for life and unleashing the machineries of death. Cell, 112, 481-490 (2003).
2. Taylor, S. W., Fahy, E., Zhang, B., Glenn, G. M., Warnock, D. E., Wiley, S., Murphy, A. N., Gaucher, S. P., Capaldi, R. A., Gibson, B. W., and Ghosh, S. S., Characterization of the human heart mitochondrial proteome. Nat. Biotechnol., 21, 281-286 (2003).
3. Sickmann, A., Reinders, J., Wagner, Y., Joppich, C., Zahedi, R., Meyer, H. E., Schönfisch, B., Perschil, I., Chacinska, A., Guiard, B., Rehling, P., Pfanner, N., and Meisinger, C., The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. USA, 100, 13207-13212 (2003).
4. Gakh, O., Cavadini, P., and Isaya, G., Mitochondrial processing peptidases. Biochem. Biophys. Acta, 1592, 63-77 (2002).
5. Koehler, C. M., New developments in mitochondrial assembly. Annu. Rev. Cell Dev. Biol., 20, 309-335 (2004).
6. Hawlitschek, G., Schneider, H., Schmidt, B., Tropschug, M., Hartl, F. U., and Neupert, W., Mitochondrial protein import: identification of processing peptidase and of PEP, a processing enhancing protein. Cell, 53, 795-806 (1988).
7. Yang, M., Jensen, R. E., Yaffe, M. P., Oppliger, W., and Schatz, G., Import of proteins into yeast mitochondria: the purified matrix processing protease contains two subunits which are encoded by the nuclear MAS1 and MAS2 genes. EMBO J., 7, 3857-3862 (1988).
8. Ou, W. J., Ito, A., Okazaki, H., and Omura, T., Purification and characterization of a processing protease from rat liver mitochondria. EMBO J., 8, 2605-2612 (1989).
9. Kleiber, J., Kalousek, F., Swaroop, M., and Rosenberg, L. E., The general mitochondrial matrix processing protease from rat liver: structural characterization of the catalytic subunit. Proc. Natl. Acad. Sci. USA, 87, 7978-7982 (1990).
10. Braun, H. P., Emmermann, M., Kruft, V., and Schmitz, U. K., The general mitochondrial processing peptidase from potato is an integral part of cytochrome c reductase of the respiratory chain. EMBO J., 11, 3219-3227 (1992).
11. Kitada, S., Shimokata, K., Niidome, T., Ogishima, T., and Ito, A., A putative metal-binding site in the β-subunit of rat mitochondrial processing peptidase is essential for its catalytic activity. J. Biochem., 117, 1148-1150 (1995).
12. Shimokata, K., Kitada, S., Ogishima, T., and Ito, A., Role of α-subunit of mitochondrial processing peptidase in subunit recognition. J. Biol. Chem., 273, 25158-25163 (1998).
13. von Heijne, G., The signal peptide. J. Membr. Biol., 115, 195-201 (1990).
14. Ito, A., Mitochondrial processing peptidase: multiplesite recognition of precursor proteins. Biochem. Biophys. Res. Commun., 265, 611-616 (1999).
15. Kitada, S., Yamasaki, E., Kojima, K., and Ito, A., Determination of the cleavage site of the presequence by mitochondrial processing peptidase on the substrate binding scafford and the multiple subsites inside a molecular cavity. J. Biol. Chem., 278, 1879-1885 (2003).
16. Inazu, Y., Chae, S. C., and Maeda, Y., Transient expression of a mitochondrial gene cluster including rps4 is essential for the phase-shift of Dictyostelium cells from growth to differentiation. Dev. Genet., 25, 339-352 (1999).
17. Wilczynska, Z., Barth, C., and Fisher, P. R., Mitochondrial mutations impair signal transduction in Dictyostelium discoideum slugs. Biochem. Biophys. Res. Commun., 234, 39-43 (1997).
18. Chida, J., Yamaguchi, H., Amagai, A., and Maeda, Y., The necessity of mitochondrial genome DNA for normal development of Dictyostelium cells. J. Cell Sci., 117, 3141-3152 (2004).
19. van Es, S., Wessels, D., Soll, D. R., Borleis, J., and Devreotes, P. N., Tortoise, a novel mitochondrial protein, is required for directional responses of Dictyostelium in chemotactic gradients. J. Cell Biol., 152, 621-632 (2001).
20. Kotsifas, M., Barth, C., Lozanne, A. D., Lay, S. T., and Fisher, P. R., Chaperonin 60 and mitochondrial disease in Dictyostelium. J. Muscle Res. Cell Motil., 23, 839-852 (2002).
21. Sussman, R., and Sussman, M., Cultivation of Dictyostelium discoideum in axenic medium. Biochem. Biophys. Res. Commun., 29, 53-55 (1967).
22. Alton, T. H., and Lodish, H. F., Developmental changes in messenger RNAs and protein synthesis in Dictyostelium discoideum. Dev. Biol., 60, 180-206 (1977).
23. Firtel, R. A., and Bonner, J., Characterization of the genome of the slime mold Dictyostelium discoideum. J. Mol. Biol., 66, 339-361 (1972).
24. Beverley, S. M., Enzymatic amplification of RNA by PCR. In "Current Protocols in Molecular Biology," eds. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K., John Wiley and Sons, New York, 15.4.1-15.4.6 (1995).
25. Shimada, N., Nishino, K., Maeda, M., Urushihara, H., and Kawata, T., Extracellular matrix family proteins that are potential targets of Dd-STATa in Dictyostelium discoideum. J. Plant Res., 117, 345-353 (2004).
26. Laemmli, U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London), 227, 680-685 (1970).
27. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J., Protein measurement with the folin phenol reagent. J. Biol. Chem., 193, 265-275 (1951).
28. Howard, P. K., Aher, K. G., and Firtel, R. A., Establishment of a transient expression system for Dictyostelium discoideum. Nucleic Acids Res., 16, 2613-2623 (1988).
29. Kitada, S., Kojima, K., Shimokata, K., Ogishima, T., and Ito, A., Glutamate residures required for substrate binding and cleavage activity in mitochondrial processing. J. Biol. Chem., 273, 32547-32553 (1998).
30. Kitada, S., Kojima, K., and Ito, A., Glu191 and Asp195 in rat mitochondrial processing peptidase β-subunit are involved in effective cleavage of precursor protein through interaction with the proximal arginine. Biochem. Biophys. Res. Commun., 287, 594-599 (2001).
31. Early, A., McRobbie, S. J., Duffy, K. T., Jermyn, K. A., Tilly, R., Ceccarelli, A., and Williams, J. G., Structural and functional characterization of genes encoding Dictyostelium prestalk and prespore cell-specific proteins. Dev. Genet., 9, 383-402 (1988).
32. Glaser, E., and Dessi, P., Integration of the mitochondrial-processing peptidase into the cytochrome bc1 complex in plants. J. Bioenerg. Biomembr., 31, 259-274 (1999).
33. Braun, H. P., and Schmitz, U. K., Are the "core" proteins of the mitochondrial bc1 complex evolutionary relics of a processing protease? Trends Biochem. Sci., 20, 171-175 (1995).
34. Witte, C., Jensen, R. E., Yaffe, M. P., and Schatz, G., MAS1, a gene essential for yeast mitochondrial assembly, encodes a subunit of the mitochondrial processing protease. EMBO J., 7, 1439-1447 (1988).
35. Jensen, R. E., and Yaffe, M. P., Import of proteins into yeast mitochondria: the nuclear MAS2 gene encodes a component of the processing protease that is homologous to the MAS1-encoded subunit. EMBO J., 7, 3863-3871 (1988).
36. Schulte, U., Arretz, M., Schneider, H., Tropschug, M., Wachter, E., Neupert, W., and Weiss, H., A family of mitochondrial proteins involved in bioenergetics and biogenesis. Nature, 339, 147-149 (1989).
37. Rocha, C. R., and Gomes, S. L., Characterization and submitochondrial localization of the alpha subunit of the mitochondrial processing peptidase from the aquatic fungus Blastocladiella emersonii. J. Bacteriol., 181, 4257-4265 (1999).
38. Birney, M. A., and Klein, C., Cloning and expression of the α subunit of succinyl-CoA synthetase from Dictyostelium discoideum. Arch. Biochem. Biophys., 319, 93-101 (1995).
39. Komori, K., Kuroe, K., Yanagisawa, K., and Tanaka, Y., Cloning and characterization of the gene encoding a mitochondrially localized DNA topoisomerase II in Dictyostelium discoideum. Biochim. Biophys. Acta, 1352, 63-72 (1997).
40. Bof, M., Brandolin, G., Satre, M., and Klein, G., The mitochondrial adenine nucleotide translocator from Dictyostelium discoideum: functional characterization and DNA sequencing. Eur. J. Biochem., 259, 795-800 (1999).
41. Yaffe, P. M., and Schatz, G., Two nuclear mutations that block mitochondrial protein import in yeast. Proc. Natl. Acad. Sci. USA, 81, 4819-4823 (1984).
42. Nomura, H., Athauda, S. B., Wada, H., Maruyama, Y., Takahashi, K., and Inoue, H., Identification and reverse genetic analysis of mitochondrial processing peptidase and the core protein of the cytochrome bc1 complex of Caenorhabditis elegans, a model parasitic nematode. J. Biochem., 139, 967-979 (2006).
43. Butow, R. A., and Avadhani, N. G., Mitochondrial signaling: the retrograde response. Mol. Cell, 14, 1-15 (2004).
44. Rohas, L. M., St.-Pierre, J., Uldry, M., Jager, S., Handschin, C., and Spiegelman, B. M., A fundamental system of cellular energy homeostasis regulated by PGC-1a. Proc. Natl. Acad. Sci. USA, 104, 7933-7938 (2007).
45. Hardie, D. G., Scott, J. W., Pan, D. A., and Hudson, E. R., Management of cellular energy by the AMPactivated protein kinase system. FEBS Lett., 546, 113-120 (2003).
46. Hardie, D. G., and Sakamoto, K., AMPK: a key sensor of fuel and energy status in skeletal muscle. Physiol., 21, 48-60 (2005).
47. Bokko, P. B., Francione, L., Bandala-Sanchez, E., Ahmed, A. U., Annesley, S. J., Huang, X., Khurana, T., Kimmel, A. R., and Fisher, P. R., Diverse cytopathologies in mitochondrial disease are caused by AMP-activated protein kinase signaling. Mol. Biol. Cell, 18, 1874-1886 (2007).
48. Jäger, S., Handschin, C., St.-Pierre, J., and Spiegelman, B. M., AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. USA, 104, 12017-12022 (2007).