Plant mitochondrial rhomboid, AtRBL12, has different substrate specificity from its yeast counterpart

Plant Molecular Biology

Volumn 68, Issue 1-2, 2008, Pages 159-171

  Kmiec Wisniewska, Beata ^a   Krumpe, Katrin ^b   Urantowka, Adam ^a   Sakamoto, Wataru ^c   Pratje, Elke ^b   Janska, Hanna ^a  

^a UNIVERSITY OF WROC AW   (Poland)

^b UNIVERSITY OF HAMBURG   (Germany)

^c OKAYAMA UNIVERSITY   (Japan)

Author keywords

AtRBL12; Intramembrane proteolysis; Pcp1; Plant mitochondria; Rhomboid proteases

Indexed keywords

ARABIDOPSIS PROTEIN; FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE; HYBRID PROTEIN; MITOCHONDRIAL PROTEIN; RBL12 PROTEIN, ARABIDOPSIS; SERINE PROTEINASE;

ARABIDOPSIS; ARTICLE; CHEMISTRY; CHLOROPLAST; CLASSIFICATION; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; PHYLOGENY; YEAST;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; FUNGAL PROTEINS; GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; MITOCHONDRIAL PROTEINS; PHYLOGENY; RECOMBINANT FUSION PROTEINS; SERINE ENDOPEPTIDASES; SUBSTRATE SPECIFICITY; YEASTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 48149115851     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-008-9359-8     Document Type: Article

References (48)

1. RP Baker K Young L Feng Y Shi S Urban 2007 Enzymatic analysis of a rhomboid intramembrane protease implicates transmembrane helix 5 as the lateral substrate gate Proc Natl Acad Sci USA 104 8257 8262 10.1073/pnas.0700814104
2. H Bannai Y Tamada O Maruyama K Nakai S Miyano 2002 Extensive feature detection of N-terminal protein sorting signals Bioinformatics 18 298 305 10.1093/bioinformatics/18.2.298
3. A Ben-Shem D Fass E Bibi 2007 Structural basis for intramembrane proteolysis by rhomboid serine proteases Proc Natl Acad Sci USA 104 462 466 10.1073/pnas.0609773104
4. B Bolter A Nada H Fulgosi J Soll 2006 A chloroplastic inner envelope membrane protease is essential for plant development FEBS Lett 580 789 794 10.1016/j.febslet.2005.12.098
5. S Cipolat T Rudka D Hartmann V Costa L Serneels K Craessaerts 2006 Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling Cell 126 163 175 10.1016/j.cell.2006.06.021
6. G Daum SM Gasser G Schatz 1982 Import of proteins into mitochondria. Energy-dependent, two-step processing of the intermembrane space enzyme cytochrome b2 by isolated yeast mitochondria J Biol Chem 257 13075 13080
7. TJ Dowse D Soldati 2005 Rhomboid-like proteins in Apicomplexa: phylogeny and nomenclature Trends Parasitol 21 254 258 10.1016/j.pt.2005.04.009
8. S Duvezin-Caubet M Koppen J Wagener M Zick L Israel A Bernacchia 2007 OPA1 processing reconstituted in yeast depends on the subunit composition of the m-AAA rotease in mitochondria Mol Biol Cell 18 3582 3590 10.1091/mbc.E07-02- 0164
9. O Emanuelsson H Nielsen S Brunak G von Heijne 2000 Predicting subcellular localization of proteins based on their N-terminal amino acid sequence J Mol Biol 300 1005 1016 10.1006/jmbi.2000.3903
10. K Esser B Tursun M Ingenhoven G Michaelis E Pratje 2002 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 323 835 843 10.1016/S0022-2836(02)01000-8
11. RD Finn J Mistry B Schuster-Bockler S Griffiths-Jones V Hollich T Lassmann 2006 Pfam: clans, web tools and services Nucleic Acids Res 34 D247 D251 10.1093/nar/gkj149
12. M Garcia-Lorenzo A Sjodin S Jansson C Funk 2006 Protease gene families in Populus and Arabidopsis BMC Plant Biol 6 30 10.1186/1471-2229-6-30
13. M Herlan F Vogel C Bornhovd W Neupert AS Reichert 2003 Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA J Biol Chem 278 27781 27788 10.1074/jbc.M211311200
14. M Herlan C Bornhövd K Hell W Neupert AS Reichert 2004 Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor J Cell Biol 165 167 173 10.1083/jcb.200403022
15. K Hofmann W Stoffel 1993 TMbase - a database of membrane spanning proteins segments Biol Chem Hoppe Seyler 374 166
16. F Jeanmougin JD Thompson M Gouy DG Higgins TJ Gibson 1998 Multiple sequence alignment with Clustal X Trends Biochem Sci 23 403 405 10.1016/S0968-0004(98)01285-7
17. MM Kanaoka S Urban M Freeman K Okada 2005 An Arabidopsis Rhomboid homolog is an intramembrane protease in plants FEBS Lett 579 5723 5728
18. K Karakasis D Taylor K Ko 2007 Uncovering a link between a plastid translocon component and rhomboid proteases using yeast mitochondria-based assays Plant Cell Physiol 48 655 661 10.1093/pcp/pcm031
19. Kaiser C, Michaelis S, Mitchel A (1994) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
20. EV Koonin KS Makarova IB Rogozin L Davidovic MC Letellier L Pellegrini 2003 The rhomboids: a nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers Genome Biol 4 R19 10.1186/gb-2003-4-3-r19
21. A Krogh B Larsson G von Heijne EL Sonnhammer 2001 Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes J Mol Biol 305 567 580 10.1006/jmbi.2000.4315
22. S Kumar K Tamura M Nei 2004 MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment Brief Bioinform 5 150 163 10.1093/bib/5.2.150
23. MK Lemberg M Freeman 2007 Functional and evolutionary implications of enhanced genomic analysis of rhomboid intermembrane proteases Genome Res 17 1634 1646 10.1101/gr.6425307
24. DC Logan 2006 Plant mitochondrial dynamics Biochim Biophys Acta 1763 430 441 10.1016/j.bbamcr.2006.01.003
25. O Lohi S Urban M Freeman 2004 Diverse substrate recognition mechanisms for rhomboids; thrombomodulin is cleaved by Mammalian rhomboids Curr Biol 14 236 241
26. GA McQuibban S Saurya M Freeman 2003 Mitochondrial membrane remodelling regulated by a conserved rhomboid protease Nature 423 537 541 10.1038/nature01633
27. GA McQuibban JR Lee L Zheng M Juusola M Freeman 2006 Normal mitochondrial dynamics requires rhomboid-7 and affects Drosophila lifespan and neuronal function Curr Biol 16 982 989 10.1016/j.cub.2006.03.062
28. G Michaelis K Esser B Tursun JP Stohn S Hanson E Pratje 2005 Mitochondrial signal peptidases of yeast: the rhomboid peptidase Pcp1 and its substrate cytochrome c peroxidase Gene 354 58 63 10.1016/j.gene.2005.04.020
29. F Passardi N Bakalovic FK Teixeira M Margis-Pinheiro C Penel C Dunand 2007 Prokaryotic origins of the non-animal peroxidase superfamily and organelle-mediated transmission to eukaryotes Genomics 89 567 579 10.1016/j.ygeno.2007.01.006
30. GJ Praefcke HT McMahon 2004 The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5 133 147 10.1038/nrm1313
31. E Quevillon V Silventoinen S Pillai N Harte N Mulder R Apweiler 2005 InterProScan: protein domains identifier Nucleic Acids Res 33 W116 120 10.1093/nar/gki442
32. Rose MD, Winston F, Hieter P (1990) Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
33. Sakamoto W, Tamura T, Hanba-Tomita Y, Murata M, Sodmergen (2002) The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7:769-780. doi: 10.1046/j.1365-2443.2002.00558.x
34. W Sakamoto A Zaltsman Z Adam Y Takahashi 2003 Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes Plant Cell 15 2843 2855 10.1105/tpc.017319
35. H Schagger G von Jagow 1987 Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa Anal Biochem 166 368 379 10.1016/0003-2697(87)90587-2
36. I Small N Peeters F Legeai C Lurin 2004 Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences Proteomics 4 1581 1590 10.1002/pmic.200300776
37. T Tatsuta S Augustin M Nolden B Friedrichs T Langer 2007 m-AAA protease-driven membrane dislocation allows intramembrane cleavage by rhomboid in mitochondria EMBO J 26 325 335 10.1038/sj.emboj.7601514
38. LP Tripathi R Sowdhamini 2006 Cross genome comparisons of serine proteases in Arabidopsis and rice BMC Genomics 7 200 10.1186/1471-2164-7-200
39. A Urantowka C Knorpp T Olczak M Kolodziejczak H Janska 2005 Plant mitochondria contain at least two i-AAA-like complexes Plant Mol Biol 59 239 252 10.1007/s11103-005-8766-3
40. S Urban 2006 Rhomboid proteins: conserved membrane proteases with divergent biological functions Genes Dev 20 3054 3068 10.1101/gad.1488606
41. S Urban JR Lee M Freeman 2001 Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases Cell 107 173 182 10.1016/S0092-8674(01) 00525-6
42. S Urban D Schlieper M Freeman 2002 Conservation of intramembrane proteolytic activity and substrate specificity in prokaryotic and eukaryotic rhomboids Curr Biol 12 1507 1512 10.1016/S0960-9822(02)01092-8
43. Y Wang Y Ha 2007 Open-cap conformation of intramembrane protease GlpG Proc Natl Acad Sci USA 104 2098 2102 10.1073/pnas.0611080104
44. Y Wang Y Zhang Y Ha 2006 Crystal structure of a rhomboid family intramembrane protease Nature 444 179 180 10.1038/nature05255
45. J Whelan C Knorpp MA Harmey E Glaser 1991 Specificity of leaf mitochondrial and chloroplast processing systems for nuclear-encoded precursor proteins Plant Mol Biol 16 283 292 10.1007/BF00020559
46. EA Winzeler 1999 Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis Science 285 901 906 10.1126/science.285. 5429.901
47. MS Wolfe R Kopan 2004 Intramembrane proteolysis: theme and variations Science 305 1119 1123 10.1126/science.1096187
48. Z Wu N Yan L Feng A Oberstein H Yan RP Baker 2006 Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry Nat Struct Mol Biol 13 1084 1091 10.1038/nsmb1179