Stress-triggered activation of the metalloprotease Oma1 involves its C-terminal region and is important for mitochondrial stress protection in yeast

Journal of Biological Chemistry

Volumn 289, Issue 19, 2014, Pages 13259-13272

  Bohovych, Iryna ^a   Donaldson, Garrett ^a   Christianson, Sara ^a   Zahayko, Nataliya ^a   Khalimonchuk, Oleh ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ACTIVITY; PHYSIOLOGY; PROTEOLYSIS; QUALITY ASSURANCE; QUALITY CONTROL; YEAST;

CELLULAR PHYSIOLOGY; CONFORMATIONAL CHANGE; CYTOCHROME C OXIDASE; FUNCTIONAL INTEGRITIES; MEMBRANE POTENTIALS; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL STRESS; PROTEOLYTIC ACTIVITIES;

MITOCHONDRIA;

OLIGOMER; PROTEIN OMA1; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL MEMBRANE POTENTIAL; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME STABILITY; FUNGAL STRAIN; HOMEOSTASIS; HYPERPOLARIZATION; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION;

GENETICS; METALLOPROTEASE; MITOCHONDRIA; MITOCHONDRIAL STRESS; OMA1; OXIDATIVE STRESS; PROTEASES; YEAST;

ELECTRON TRANSPORT COMPLEX IV; HOMEOSTASIS; METALLOPROTEASES; MITOCHONDRIA; OXIDATIVE STRESS; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84900396722     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.542910     Document Type: Article

References (63)

1. Adam-Vizi, V., and Chinopoulos, C. (2006) Bioenergetics and the formation of mitochondrial reactive oxygen species. Trends Pharmacol. Sci. 27, 639-645
2. Baker, B. M., and Haynes, C. M. (2011) Mitochondrial quality control during biogenesis and aging. Trends Biochem. Sci. 36, 254-261
3. Tatsuta, T., and Langer, T. (2008) Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J. 27, 306-314
4. Baker, M. J., Tatsuta, T., and Langer, T. (2011) Quality control of mitochondrial proteostasis. Cold Spring Harb. Perspect. Biol. 3, pii: a007559
5. Rugarli, E. I., and Langer, T. (2012) Mitochondrial quality control: a matter of life and death for neurons. EMBO J. 31, 1336-1349
6. Gomis-Rüth, F. X. (2009) Cataytic domain architecture of metzincin metalloproteases. J. Biol. Chem. 284, 15353-15357
7. López-Pelegrín, M., Cerdà-Costa, N., Martínez-Jiménez, F., Cintas-Pedrola, A., Canals, A., Peinado, J. R., Marti-Renom, M. A., López-Otín, C., Arolas, J. L., and Gomis-Rüth, F. X. (2013) A novel family of soluble minimal scaffolds provides structural insight into the catalytic domains of integral membrane metallopeptidases. J. Biol. Chem. 288, 21279-21294
8. Kaser, M., Kambacheld, M., Kisters-Woike, B., and Langer, T. (2003) Oma1, a novel membrane-bound metallopeptidase in mitochondria with activities overlapping with the m-AAA protease. J. Biol. Chem. 278, 46414-46423
9. Khalimonchuk, O., Jeong, M. Y., Watts, T., Ferris, E., and Winge, D. R. (2012) Selective Oma1 protease-mediated proteolysis of Cox1 subunit of cytochrome oxidase in assembly mutants. J. Biol. Chem. 287, 7289-7300
10. Ehses, S., Raschke, I., Mancuso, G., Bernacchia, A., Geimer, S., Tondera, D., Martinou, J. C., Westermann, B., Rugarli, E. I., and Langer, T. (2009) Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell Biol. 187, 1023-1036
11. Head, B., Griparic, L., Amiri, M., Gandre-Babbe, S., and Van Der Bliek, A. M. (2009) Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J. Cell Biol. 187, 959-966
12. Shimohata, N., Chiba, S., Saikawa, N., Ito, K., and Akiyama, Y. (2002) The Cpx stress response system of Escherichia coli senses plasma membrane proteins and controls HtpX, a membrane protease with a cytosolic active site. Genes Cells 7, 653-662
13. Sakoh, M., Ito, K., and Akiyama, Y. (2005) Proteolytic activity of HtpX, a membrane-bound and stress-controlled protease from Escherichia coli. J. Biol. Chem. 280, 33305-33310
14. Bestwick, M., Khalimonchuk, O., Pierrel, F., and Winge, D. R. (2010) The role of Coa2 in hemylation of yeast Cox1 revealed by its genetic interaction with Cox10. Mol. Cell. Biol. 30, 172-185
15. Hornig-Do, H. T., Tatsuta, T., Buckermann, A., Bust, M., Kollberg, G., Rötig, A., Hellmich, M., Nijtmans, L., and Wiesner, R. J. (2012) Nonsense mutations in the COX1 subunit impair the stability of respiratory chain complexes rather than their assembly. EMBO J. 31, 1293-1307
16. Quirós, P. M., Ramsay, A. J., Sala, D., Fernández-Vizarra, E., Rodríguez, F., Peinado, J. R., Fernández-García, M. S., Vega, J. A., Enríquez, J. A., Zorzano, A., and López-Otín, C. (2012) Loss of mitochondrial protease OMA1 alters processing of the GTPase OPA1 and causes obesity and defective thermogenesis in mice. EMBO J. 31, 2117-2133
17. Hoppins, S., Edlich, F., Cleland, M. M., Banerjee, S., McCaffery, J. M., Youle, R. J., and Nunnari, J. (2011) The soluble form of Bax regulates mitochondrial fusion via MFN2 homotypic complexes. Mol. Cell 41, 150-160
18. Pierrel, F., Bestwick, M. L., Cobine, P. A., Khalimonchuk, O., Cricco, J. A., and Winge, D. R. (2007) Coa1 links the Mss51 post-translational function to Cox1 cofactor insertion in cytochrome c oxidase assembly. EMBOJ. 26, 4335-4346
19. Goldstein, A. L., Pan, X., and McCusker, J. H. (1999) Heterologous URA3MX cassettes for gene replacement in Saccharomyces cerevisiae. Yeast 15, 507-511
20. Mumberg, D., Müller, R., and Funk, M. (1994) Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22, 5767-5768
21. Ocampo, A., Zambrano, A., and Barrientos, A. (2010) Suppression of polyglutamineinduced cytotoxicity in Saccharomyces cerevisiae by enhancement of mitochondrial biogenesis. FASEB J. 24, 1431-1441
22. Bender, T., Lewrenz, I., Franken, S., Baitzel, C., and Voos, W. (2011) Mitochondrial enzymes are protected from stress-induced aggregation by mitochondrial chaperones and the Pim1/LON protease. Mol. Biol. Cell 22, 541-554
23. Khalimonchuk, O., Bird, A., and Winge, D. R. (2007) Evidence for a prooxidant intermediate in the assembly of cytochrome oxidase. J. Biol. Chem. 282, 17442-17449
24. Sambrook, J., Fritsch, E. F., and Manniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
25. Soto, I. C., Fontanesi, F., Valledor, M., Horn, D., Singh, R., and Barrientos, A. (2009) Synthesis of cytochrome c oxidase subunit 1 is translationally downregulated in the absence of functional F1F0-ATP synthase. Biochim. Biophys. Acta 1793, 1776-1786
26. Heo, J. M., Livnat-Levanon, N., Taylor, E. B., Jones, K. T., Dephoure, N., Ring, J., Xie, J., Brodsky, J. L., Madeo, F., Gygi, S. P., Ashrafi, K., Glickman, M. H., and Rutter, J. (2010) A stress-responsive system for mitochondrial protein degradation. Mol. Cell 40, 465-480
27. Diekert, K., De Kroon, A. I., Kispal, G., and Lill, R. (2001) Isolation and subfractionation of mitochondria from the yeast Saccharomyces cerevisiae. Methods Cell Biol. 65, 37-51
28. Boudina, S., Bugger, H., Sena, S., O'Neill, B. T., Zaha, V. G., Ilkun, O., Wright, J. J., Mazumder, P. K., Palfreyman, E., Tidwell, T. J., Theobald, H., Khalimonchuk, O., Wayment, B., Sheng, X., Rodnick, K. J., Centini, R., Chen, D., Litwin, S. E., Weimer, B. E., and Abel, E. D. (2009) Contribution of impaired myocardial insulin signaling to mitochondrial dysfunction and oxidative stress in the heart. Circulation 119, 1272-1283
29. Khalimonchuk, O., Bestwick, M., Meunier, B., Watts, T. C., and Winge, D. R. (2010) Formation of the redox cofactor centers during Cox1 maturation in yeast cytochrome oxidase. Mol. Cell. Biol. 30, 1004-1017
30. Gardner, P. R., Nguyen, D. D., and White, C. W. (1994) Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and rat lungs. Proc. Natl. Acad. Sci. U. S. A. 91, 12248-12252
31. Bharadwaj, A. G., Rector, K., and Simpson, M. A. (2007) Inducible hyaluronan production reveals differential effects on prostate tumor cell growth and tumor angiogenesis. J. Biol. Chem. 282, 20561-20572
32. Gietz, R. D., and Schiestl, R. H. (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2, 31-34
33. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890
34. Pierrel, F., Khalimonchuk, O., Cobine, P. A., Bestwick, M., and Winge, D. R. (2008) Coa2 is an assembly factor for yeast cytochrome c oxidase biogenesis that facilitates the maturation of Cox1. Mol. Cell. Biol. 28, 4927-4939
35. Nolden, M., Ehses, S., Koppen, M., Bernacchia, A., Rugarli, E. I., and Langer, T. (2005) The m-AAA protease defective in hereditary spastic paraplegia controls ribosome assembly in mitochondria. Cell 123, 277-289
36. Longo, V. D., Gralla, E. B., and Valentine, J. S. (1996) Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J. Biol. Chem. 271, 12275-12280
37. Longo, V. D., Liou, L. L., Valentine, J. S., and Gralla, E. B., (1999) Mitochondrial superoxide decreases yeast survival in stationary phase. Arch. Biochem. Biophys. 365, 131-142
38. Pain, J., Balamurali, M. M., Dancis, A., and Pain, D. (2010) Mitochondrial NADH kinase, Pos5p, is required for efficient iron-sulfur cluster biogenesis in Saccharomyces cerevisiae. J. Biol. Chem. 285, 39409-39424
39. Outeiro, T. F., and Lindquist, S. (2003) Yeast cells provide insight into β-synuclein biology and pathobiology. Science 302, 1772-1775
40. Solans, A., Zambrano, A., Rodríguez, M., and Barrientos, A. (2006) Cytotoxicity of a mutant huntingtin fragment in yeast involves early alterations in mitochondrial OXPHOS complexes II and III. Hum. Mol. Genet. 15, 3063-3081
41. Costa, V., and Scorrano, L. (2012) Shaping the role of mitochondria in the pathogenesis of Huntington's disease. EMBO J. 31, 1853-1864
42. Dienhart, M. K., and Stuart, R. A. (2008) The yeast Aac2 protein exists in physical association with the cytochrome bc1-COX supercomplex and the TIM23 machinery. Mol. Biol. Cell 19, 3934-3943
43. Claypool, S. M., Whited, K., Srijumnong, S., Han, X., and Koehler, C. M. (2011) Barth syndrome mutations that cause tafazzin complex lability. J. Cell Biol. 192, 447-462
44. Leonhard, K., Guiard, B., Pellecchia, G., Tzagoloff, A., Neupert, W., and Langer, T. (2000) Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Mol. Cell 5, 629-638
45. Lemaire, C., Hamel, P., Velours, J., and Dujardin, G. (2000) Absence of the mitochondrial AAA protease Yme1p restores F0-ATPase subunit accumulation in an oxa1 deletion mutant of Saccharomyces cerevisiae. J. Biol. Chem. 275, 23471-23475
46. Kambacheld, M., Augustin, S., Tatsuta, T., Müller, S., and Langer, T. (2005) Role of the novel metallopeptidase Mop112 and saccharolysin for the complete degradation of proteins residing in different subcompartments of mitochondria. J. Biol. Chem. 280, 20132-20139
47. Wagner, I., Arlt, H., Van Dyck, L., Langer, T., Neupert, W. (1994) Molecular chaperones cooperate with PIM1 protease in the degradation of misfolded proteins in mitochondria. EMBO J. 13, 5135-5145
48. Suzuki, C. K., Suda, K., Wang, N., and Schatz, G. (1994) Requirement for the yeast gene LON in intramitochondrial proteolysis and maintenance of respiration. Science 264, 273-276
49. Schäfer, A., Zick, M., Kief, J., Steger, M., Heide, H., Duvezin-Caubet, S., Neupert, W., and Reichert, A. S. (2010) Intramembrane proteolysis of Mgm1 by the mitochondrial rhomboid protease is highly promiscuous regarding the sequence of the cleaved hydrophobic segment. J. Mol. Biol. 401, 182-193
50. Duvezin-Caubet, S., Koppen, M., Wagener, J., Zick, M., Israel, L., Bernacchia, A., Jagasia, R., Rugarli, E. I., Imhof, A., Neupert, W., Langer, T., and Reichert, A. S. (2007) OPA1 processing reconstituted in yeast depends on the subunit composition of the m-AAA protease in mitochondria. Mol. Biol. Cell 18, 3582-3590
51. 1+ in S. cerevisiae and OPA1 in mammals. FEBS Lett. 584, 3153-3157
52. Erjavec, N., Bayot, A., Gareil, M., Camougrand, N., Nystrom, T., Friguet, B., and Bulteau, A.-L. (2013) Deletion of the mitochondrial Pim1/Lon protease in yeast results in accelerated aging and impairment of the proteasome. Free Radic. Biol. Med. 56, 9-16
53. Daoud, H., Valdmanis, P. N., Gros-Louis, F., Belzil, V., Spiegelman, D., Henrion, E., Diallo, O., Desjarlais, A., Gauthier, J., Camu, W., Dion, P. A., and Rouleau, G. A. (2011) Resequencing of 29 candidate genes in patients with familial and sporadic amyotrophic lateral sclerosis. Arch. Neurol. 68, 587-593
54. Walsh, N. P., Alba, B. M., Bose, B., Gross, C. A., and Sauer, R. T. (2003) OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113, 61-71
55. Wilken, C., Kitzing, K., Kurzbauer, R., Ehrmann, M., and Clausen, T. (2004) Crystal structure of the DegS stress sensor: How a PDZ domain recognizes misfolded protein and activates a protease. Cell 117, 483-494
56. Sohn, J., Grant, R. A., and Sauer, R. T. (2007) Allosteric activation of DegS, a stress sensor PDZ protease. Cell 131, 572-583
57. Biswas, T., Small, J., Vandal, O., Odaira, T., Deng, H., Ehrt, S., and Tsodikov, O. V. (2010) Structural insight into serine protease Rv3671c that protects M. tuberculosis from oxidative and acidic stress. Structure 18, 1353-1363
58. Xue, Y., Chowdhury, S., Liu, X., Akiyama, Y., Ellman, J., and Ha, Y. (2012) Conformational change in rhomboid protease GlpG induced by inhibitor binding to its Sβ subsites. Biochemistry 51, 3723-3731
59. Roy, A., Kucukural, A., and Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738
60. Gray, J. V., Petsko, G. A., Johnston, G. C., Ringe, D., Singer, R. A., and Werner-Washburne, M. (2004) "Sleeping beauty": quiescence in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 68, 187-206
61. Bender, T., Leidhold, C., Ruppert, T., Franken, S., and Voos, W. (2010) The role of protein quality control in mitochondrial protein homeostasis under oxidative stress. Proteomics 10, 1426-1443
62. Costanzo, M., Baryshnikova, A., Bellay, J., Kim, Y., Spear, E. D., Sevier, C. S., Ding, H., Koh, J. L., Toufighi, K., Mostafavi, S., Prinz, J., St. Onge, R. P., Vander Sluis, B., Makhnevych, T., Vizeacoumar, F. J., Alizadeh, S., Bahr, S., Brost, R. L., Chen, Y., Cokol, M., Deshpande, R., Li, Z., Lin, Z. Y., Liang, W., Marback, M., Paw, J., San Luis, B. J., Shuteriqi, E., Tong, A. H., Van Dyk, N., Wallace, I. M., Whitney, J. A., Weirauch, M. T., Zhong, G., Zhu, H., Houry, W. A., Brudno, M., Ragibizadeh, S., Papp, B., Pál, C., Roth, F. P., Giaever, G., Nislow, C., Troyanskaya, O. G., Bussey, H., Bader, G. D., Gingras, A. C., Morris, Q. D., Kim, P. M., Kaiser, C. A., Myers, C. L., Andrews, B. J., and Boone, C. (2010) The genetic landscape of a cell. Science 327, 425-431
63. Baker, M. J., Lampe, P. A., Stojanovski, D., Korwitz, A., Anand, R., Tatsuta, T., and Langer, T. (2014) Stress-induced OMA1 activation and autocatalytic turnover regulates OPA1-dependent mitochondrial dynamics. EMBO J. 33, 578-593