Processing of the dynamin Msp1p in S. pombe reveals an evolutionary switch between its orthologs Mgm1p in S. cerevisiae and OPA1 in mammals

FEBS Letters

Volumn 584, Issue 14, 2010, Pages 3153-3157

  Leroy, Ingrid ^a   Khosrobakhsh, Farnoosh ^a   Diot, Alan ^a   Daloyau, Marlène ^a   Arnauné Pelloquin, Laetitia ^a   Cavelier, Cindy ^a   Emorine, Laurent J ^a   Belenguer, Pascale ^a  

^a Institut National de la Sant é et de la Recherche Medicale   (France)

Author keywords

Mgm1p; Mitochondria; Mitochondrial dynamics; Mitochondrial proteases; Msp1p; OPA1

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DYNAMIN; HYBRID PROTEIN; ISOPROTEIN; PROTEIN MGM1P; PROTEIN MSP1P; PROTEIN OPA1; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; MAMMAL; MITOCHONDRION; MOLECULAR EVOLUTION; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; ANIMAL; AUTOSOMAL DOMINANT OPTIC ATROPHY; EVOLUTION; GENETICS; HUMAN; MEMBRANE FUSION; METABOLISM; SCHIZOSACCHAROMYCES;

MAMMALIA; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; DYNAMINS; EVOLUTION; HUMANS; MAMMALS; MEMBRANE FUSION; MITOCHONDRIA; OPTIC ATROPHY, AUTOSOMAL DOMINANT; PROTEIN ISOFORMS; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES;

EID: 77954174214     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.05.060     Document Type: Article

References (32)

1. Detmer S.A., Chan D.C. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 2007, 8:870-879.
2. Hoppins S., Lackner L., Nunnari J. The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 2007, 76:751-780.
3. Olichon A., et al. Mitochondrial dynamics and disease, OPA1. Biochim. Biophys. Acta 2006, 1763:500-509.
4. Song Z., Chen H., Fiket M., Alexander C., Chan D.C. OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J. Cell Biol. 2007, 178:749-755.
5. Olichon A., et al. The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett. 2002, 523:171-176.
6. Landes, T. et al. (2010) OPA1 (dys)functions. Semin. Cell Dev. Biol., doi:10.1016/j.semcdb.2009.12.012.
7. Cipolat S., et al. Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 2006, 126:163-175.
8. Duvezin-Caubet S., et al. OPA1 processing reconstituted in yeast depends on the subunit composition of the m-AAA protease in mitochondria. Mol. Biol. Cell 2007, 18:3582-3590.
9. Griparic L., Kanazawa T., van der Bliek A.M. Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J. Cell Biol. 2007, 178:757-764.
10. Ishihara N., Fujita Y., Oka T., Mihara K. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 2006, 25:2966-2977.
11. Guillery O., et al. Metalloprotease-mediated OPA1 processing is modulated by the mitochondrial membrane potential. Biol. Cell 2008, 100:315-325.
12. Herlan M., Vogel F., Bornhovd C., Neupert W., Reichert A.S. Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J. Biol. Chem. 2003, 278:27781-27788.
13. Herlan M., Bornhovd C., Hell K., Neupert W., Reichert A.S. Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor. J. Cell Biol. 2004, 165:167-173.
14. McQuibban G.A., Saurya S., Freeman M. Mitochondrial membrane remodelling regulated by a conserved rhomboid protease. Nature 2003, 423:537-541.
15. Sesaki H., Southard S.M., Hobbs A.E., Jensen R.E. Cells lacking Pcp1p/Ugo2p, a rhomboid-like protease required for Mgm1p processing, lose mtDNA and mitochondrial structure in a Dnm1p-dependent manner, but remain competent for mitochondrial fusion. Biochem. Biophys. Res. Commun. 2003, 308:276-283.
16. Chiron S., Gaisne M., Guillou E., Belenguer P., Clark-Walker G.D., Bonnefoy N. Methods in Molecular Biology. Mitochondria: Practical protocols 2007, 372:91-106.
17. Haffter P., Fox T.D. Nuclear mutations in the petite-negative yeast Schizosaccharomyces pombe allow growth of cells lacking mitochondrial DNA. Genetics 1992, 131:255-260.
18. Massardo D.R., Manna F., Schafer B., Wolf K., Del Giudice L. Complete absence of mitochondrial DNA in the petite-negative yeast Schizosaccharomyces pombe leads to resistance towards the alkaloid lycorine. Curr. Genet. 1994, 25:80-83.
19. Baricault L., Segui B., Guegand L., Olichon A., Valette A., Larminat F., Lenaers G. OPA1 cleavage depends on decreased mitochondrial ATP level and bivalent metals. Exp. Cell Res. 2007, 313:3800-3808.
20. Bahler J., et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 1998, 14:943-951.
21. Hentges P., Van Driessche B., Tafforeau L., Vandenhaute J., Carr A.M. Three novel antibiotic marker cassettes for gene disruption and marker switching in Schizosaccharomyces pombe. Yeast 2005, 22:1013-1019.
22. Guillou E., Bousquet C., Daloyau M., Emorine L.J., Belenguer P. Msp1p is an intermembrane space dynamin-related protein that mediates mitochondrial fusion in a Dnm1p-dependent manner in S. Pombe. FEBS Lett. 2005, 579:1109-1116.
23. Pelloquin L., Belenguer P., Menon Y., Ducommun B. Identification of a fission yeast dynamin-related protein involved in mitochondrial DNA maintenance. Biochem. Biophys. Res. Commun. 1998, 251:720-726.
24. Polanshek M.M. Effects of heat shock and cycloheximide on growth and division of the fission yeast, Schizosaccharomyces pombe. With an Appendix. Estimation of division delay for S. pombe from cell plate index curves. J. Cell Sci. 1977, 23:1-23.
25. Diot A., Guillou E., Daloyau M., Arnaune-Pelloquin L., Emorine L.J., Belenguer P. Transmembrane segments of the dynamin Msp1p uncouple its functions in the control of mitochondrial morphology and genome maintenance. J. Cell Sci. 2009, 122:2632-2639.
26. DeVay R.M., Dominguez-Ramirez L., Lackner L.L., Hoppins S., Stahlberg H., Nunnari J. Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion. J. Cell Biol. 2009, 186:793-803.
27. Zick M., Duvezin-Caubet S., Schafer A., Vogel F., Neupert W., Reichert A.S. Distinct roles of the two isoforms of the dynamin-like GTPase Mgm1 in mitochondrial fusion. FEBS Lett. 2009, 583:2237-2243.
28. Sesaki H., Dunn C.D., Iijima M., Shepard K.A., Yaffe M.P., Machamer C.E., Jensen R.E. Ups1p, a conserved intermembrane space protein, regulates mitochondrial shape and alternative topogenesis of Mgm1p. J. Cell Biol. 2006, 173:651-658.
29. Ehses S., et al. Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell Biol. 2009, 187:1023-1036.
30. Head B., Griparic L., Amiri M., Gandre-Babbe S., van der Bliek A.M. Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J. Cell Biol. 2009, 187:959-966.
31. Esser K., Tursun B., Ingenhoven M., Michaelis G., Pratje E. A novel two-step mechanism for removal of a mitochondrial signal sequence involves the mAAA complex and the putative rhomboid protease Pcp1. J. Mol. Biol. 2002, 323:835-843.
32. Koppen M., Langer T. Protein degradation within mitochondria: versatile activities of AAA proteases and other peptidases. Crit. Rev. Biochem. Mol. Biol. 2007, 42:221-242.