The membrane scaffold SLP2 anchors a proteolytic hub in mitochondria containing PARL and the i-AAA protease YME1L

EMBO Reports

Volumn 17, Issue 12, 2016, Pages 1844-1856

  Wai, Timothy ^a,d   Saita, Shotaro ^a   Nolte, Hendrik ^a   Müller, Sebastian ^a   König, Tim ^a   Richter Dennerlein, Ricarda ^a,e   Sprenger, Hans Georg ^a   Madrenas, Joaquin ^b,f   Mühlmeister, Mareike ^c   Brandt, Ulrich ^c   Krüger, Marcus ^a   Langer, Thomas ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MCGILL UNIVERSITY   (Canada)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d INSTITUT NECKER ENFANTS MALADES   (France)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

^f LA Biomedical Research Institute   (United States)

Author keywords

membrane scaffold; mitochondria; OMA1; rhomboid; SLP2; YME1L

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MITOCHONDRIAL PROTEIN; PEPTIDASE; PEPTIDASE OMA1; PHOSPHATASE; PHOSPHOGLYCERATE MUTASE FAMILY MEMBER 5; PHOSPHOTRANSFERASE; PROTEASE PARL; PROTEASE YME1L; PROTEASOME; PROTEIN OPA1; PROTEIN PINK1; PROTEINASE; SCAFFOLD PROTEIN; STOMATIN LIKE PROTEIN 2; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; METALLOPROTEINASE; MOLECULE METALLOPROTEASE-RELATED PROTEIN-1, HUMAN; OPA1 PROTEIN, HUMAN; PARL PROTEIN, HUMAN; PEPTIDE HYDROLASE; PGAM5 PROTEIN, HUMAN; PHOSPHOPROTEIN PHOSPHATASE; PLASMA PROTEIN; PROTEIN BINDING; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; STOML2 PROTEIN, HUMAN; YME1L1 PROTEIN, HUMAN;

ARTICLE; CELL SURVIVAL; COMPLEX FORMATION; DEPOLARIZATION; ENZYME BINDING; INNER MEMBRANE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEOMICS; QUALITY CONTROL; STRESS; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; PHYSIOLOGY;

BLOOD PROTEINS; GTP PHOSPHOHYDROLASES; HEK293 CELLS; HELA CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; METALLOPROTEASES; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; PEPTIDE HYDROLASES; PHOSPHOPROTEIN PHOSPHATASES; PROTEIN BINDING; PROTEIN KINASES; PROTEOLYSIS;

EID: 84991354989     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201642698     Document Type: Article

References (55)

1. Anand R, Wai T, Baker MJ, Kladt N, Schauss AC, Rugarli E, Langer T (2014) The i-AAA protease YME1L and OMA1 cleave OPA1 to balance mitochondrial fusion and fission. J Cell Biol 204: 919–929
2. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, Rudka T, Bartoli D, Polishuck RS, Danial NN, De Strooper B et al (2006) OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126: 177–189
3. Olichon A, Guillou E, Delettre C, Landes T, Arnaune-Pelloquin L, Emorine LJ, Mils V, Daloyau M, Hamel C, Amati-Bonneau P et al (2006) Mitochondrial dynamics and disease, OPA1. Biochim Biophys Acta 1763: 500–509
4. Potting C, Tatsuta T, Konig T, Haag M, Wai T, Aaltonen MJ, Langer T (2013) TRIAP1/PRELI complexes prevent apoptosis by mediating intramitochondrial transport of phosphatidic acid. Cell Metab 18: 287–295
5. Baker MJ, Lampe PA, Stojanovski D, Korwitz A, Anand R, Tatsuta T, Langer T (2014) Stress-induced OMA1 activation and autocatalytic turnover regulate OPA1-dependent mitochondrial dynamics. EMBO J 33: 578–593
6. Bohovych I, Fernandez MR, Rahn JJ, Stackley KD, Bestman JE, Anandhan A, Franco R, Claypool SM, Lewis RE, Chan SS et al (2015) Metalloprotease OMA1 Fine-tunes Mitochondrial Bioenergetic Function and Respiratory Supercomplex Stability. Sci Rep 5: 13989
7. Ehses S, Raschke I, Mancuso G, Bernacchia A, Geimer S, Tondera D, Martinou JC, Westermann B, Rugarli EI, Langer T (2009) Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J Cell Biol 187: 1023–1036
8. Head B, Griparic L, Amiri M, Gandre-Babbe S, van der Bliek AM (2009) Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J Cell Biol 187: 959–966
9. Käser M, Kambacheld M, Kisters-Woike B, 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
10. Jin SM, Lazarou M, Wang C, Kane LA, Narendra DP, Youle RJ (2010) Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol 191: 933–942
11. Morais VA, Haddad D, Craessaerts K, De Bock PJ, Swerts J, Vilain S, Aerts L, Overbergh L, Grunewald A, Seibler P et al (2014) PINK1 loss-of-function mutations affect mitochondrial complex I activity via NdufA10 ubiquinone uncoupling. Science 344: 203–207
12. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8: e1000298
13. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, May J, Tocilescu MA, Liu W, Ko HS et al (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci USA 107: 378–383
14. Sekine S, Kanamaru Y, Koike M, Nishihara A, Okada M, Kinoshita H, Kamiyama M, Maruyama J, Uchiyama Y, Ishihara N et al (2012) Rhomboid protease PARL mediates the mitochondrial membrane potential loss-induced cleavage of PGAM5. J Biol Chem 287: 34635–34645
15. Chen G, Han Z, Feng D, Chen Y, Chen L, Wu H, Huang L, Zhou C, Cai X, Fu C et al (2014) A regulatory signaling loop comprising the PGAM5 phosphatase and CK2 controls receptor-mediated mitophagy. Mol Cell 54: 362–377
16. Ishida Y, Sekine Y, Oguchi H, Chihara T, Miura M, Ichijo H, Takeda K (2012) Prevention of apoptosis by mitochondrial phosphatase PGAM5 in the mushroom body is crucial for heat shock resistance in Drosophila melanogaster. PLoS ONE 7: e30265
17. Lu W, Karuppagounder SS, Springer DA, Allen MD, Zheng L, Chao B, Zhang Y, Dawson VL, Dawson TM, Lenardo M (2014) Genetic deficiency of the mitochondrial protein PGAM5 causes a Parkinson's-like movement disorder. Nat Commun 5: 4930
18. Wang Z, Jiang H, Chen S, Du F, Wang X (2012) The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 148: 228–243
19. Becker T, Gebert M, Pfanner N, van der Laan M (2009) Biogenesis of mitochondrial membrane proteins. Curr Opin Cell Biol 21: 484–493
20. Daum B, Walter A, Horst A, Osiewacz HD, Kuhlbrandt W (2013) Age-dependent dissociation of ATP synthase dimers and loss of inner-membrane cristae in mitochondria. Proc Natl Acad Sci USA 110: 15301–15306
21. Chaban Y, Boekema EJ, Dudkina NV (2014) Structures of mitochondrial oxidative phosphorylation supercomplexes and mechanisms for their stabilisation. Biochim Biophys Acta 1837: 418–426
22. van der Laan M, Horvath SE, Pfanner N (2016) Mitochondrial contact site and cristae organizing system. Curr Opin Cell Biol 41: 33–42
23. Lapatsina L, Brand J, Poole K, Daumke O, Lewin GR (2012) Stomatin-domain proteins. Eur J Cell Biol 91: 240–245
24. Browman DT, Hoegg MB, Robbins SM (2007) The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol 17: 394–402
25. Osman C, Merkwirth C, Langer T (2009) Prohibitins and the functional compartmentalization of mitochondrial membranes. J Cell Sci 122: 3823–3830
26. Brand J, Smith ES, Schwefel D, Lapatsina L, Poole K, Omerbasic D, Kozlenkov A, Behlke J, Lewin GR, Daumke O (2012) A stomatin dimer modulates the activity of acid-sensing ion channels. EMBO J 31: 3635–3646
27. Tatsuta T, Model K, Langer T (2005) Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol Biol Cell 16: 248–259
28. Richter-Dennerlein R, Korwitz A, Haag M, Tatsuta T, Dargazanli S, Baker M, Decker T, Lamkemeyer T, Rugarli EI, Langer T (2014) DNAJC19, a mitochondrial cochaperone associated with cardiomyopathy, forms a complex with prohibitins to regulate cardiolipin remodeling. Cell Metab 20: 158–171
29. Steglich G, Neupert W, Langer T (1999) Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol Cell Biol 19: 3435–3442
30. Merkwirth C, Dargazanli S, Tatsuta T, Geimer S, Lower B, Wunderlich FT, von Kleist-Retzow JC, Waisman A, Westermann B, Langer T (2008) Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 22: 476–488
31. He J, Cooper HM, Reyes A, Di Re M, Sembongi H, Litwin TR, Gao J, Neuman KC, Fearnley IM, Spinazzola A et al (2012) Mitochondrial nucleoid interacting proteins support mitochondrial protein synthesis. Nucleic Acids Res 40: 6109–6121
32. Korwitz A, Merkwirth C, Richter-Dennerlein R, Troder SE, Sprenger HG, Quiros PM, Lopez-Otin C, Rugarli EI, Langer T (2016) Loss of OMA1 delays neurodegeneration by preventing stress-induced OPA1 processing in mitochondria. J Cell Biol 212: 157–166
33. Hajek P, Chomyn A, Attardi G (2007) Identification of a novel mitochondrial complex containing mitofusin 2 and stomatin-like protein 2. J Biol Chem 282: 5670–5681
34. Christie DA, Mitsopoulos P, Blagih J, Dunn SD, St-Pierre J, Jones RG, Hatch GM, Madrenas J (2012) Stomatin-like protein 2 deficiency in T cells is associated with altered mitochondrial respiration and defective CD4+ T cell responses. J Immunol 189: 4349–4360
35. Mitsopoulos P, Chang YH, Wai T, Konig T, Dunn SD, Langer T, Madrenas J (2015) Stomatin-like protein 2 is required for in vivo mitochondrial respiratory chain supercomplex formation and optimal cell function. Mol Cell Biol 35: 1838–1847
36. Christie DA, Lemke CD, Elias IM, Chau LA, Kirchhof MG, Li B, Ball EH, Dunn SD, Hatch GM, Madrenas J (2011) Stomatin-like protein 2 binds cardiolipin and regulates mitochondrial biogenesis and function. Mol Cell Biol 31: 3845–3856
37. Da Cruz S, Parone PA, Gonzalo P, Bienvenut WV, Tondera D, Jourdain A, Quadroni M, Martinou JC (2008) SLP-2 interacts with prohibitins in the mitochondrial inner membrane and contributes to their stability. Biochim Biophys Acta 1783: 904–911
38. Cipolat S, Rudka T, Hartmann D, Costa V, Serneels L, Craessaerts K, Metzger K, Frezza C, Annaert W, D'Adamio L et al (2006) Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126: 163–175
39. Heide H, Bleier L, Steger M, Ackermann J, Drose S, Schwamb B, Zornig M, Reichert AS, Koch I, Wittig I et al (2012) Complexome profiling identifies TMEM126B as a component of the mitochondrial complex I assembly complex. Cell Metab 16: 538–549
40. Rainbolt TK, Atanassova N, Genereux JC, Wiseman RL (2013) Stress-regulated translational attenuation adapts mitochondrial protein import through Tim17A degradation. Cell Metab 18: 908–919
41. Lo SC, Hannink M (2008) PGAM5 tethers a ternary complex containing Keap1 and Nrf2 to mitochondria. Exp Cell Res 314: 1789–1803
42. Tondera D, Grandemange S, Jourdain A, Karbowski M, Mattenberger Y, Herzig S, Da Cruz S, Clerc P, Raschke I, Merkwirth C et al (2009) SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J 28: 1589–1600
43. Chen AC, Kim S, Shepardson N, Patel S, Hong S, Selkoe DJ (2015) Physical and functional interaction between the alpha- and gamma-secretases: a new model of regulated intramembrane proteolysis. J Cell Biol 211: 1157–1176
44. Quiros PM, Ramsay AJ, Sala D, Fernandez-Vizarra E, Rodriguez F, Peinado JR, Fernandez-Garcia MS, Vega JA, Enriquez JA, Zorzano A et al (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
45. Gomes LC, Di Benedetto G, Scorrano L (2011) During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 13: 589–598
46. Rambold AS, Kostelecky B, Elia N, Lippincott-Schwartz J (2011) Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci USA 108: 10190–10195
47. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8: 2281–2308
48. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856–2860
49. Rappsilber J, Ishihama Y, Mann M (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 75: 663–670
50. Nolte H, Konzer A, Ruhs A, Jungblut B, Braun T, Kruger M (2014) Global protein expression profiling of zebrafish organs based on in vivo incorporation of stable isotopes. J Proteome Res 13: 2162–2174
51. Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367–1372
52. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10: 1794–1805
53. Cox J, Hein MY, Luber CA, Paron I, Nagaraj N, Mann M (2014) Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics 13: 2513–2526
54. Vizcaino JA, Csordas A, del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T et al (2016) 2016 update of the PRIDE database and its related tools. Nucleic Acids Res 44: D447–D456
55. Koppen M, Metodiev MD, Casari G, Rugarli EI, Langer T (2007) Variable and Tissue-Specific Subunit Composition of Mitochondrial m-AAA Protease Complexes Linked to Hereditary Spastic Paraplegia. Mol Cell Biol 27: 758–767