Proteins at the polypeptide tunnel exit of the yeast mitochondrial ribosome.
Oxidative phosphorylation in mitochondria requires the synthesis of proteins encoded in the mitochondrial DNA. The mitochondrial translation machinery differs significantly from that of the bacterial ancestor of the organelle. This is especially evident from many mitochondria-specific ribosomal proteins. An important site of the ribosome is the polypeptide tunnel exit. Here, nascent chains are exposed to an aqueous environment for the first time. Many biogenesis factors interact with the tunnel exit of pro- and eukaryotic ribosomes to help the newly synthesized proteins to mature. To date, nothing is known about the organization of the tunnel exit of mitochondrial ribosomes. We therefore undertook a comprehensive approach to determine the composition of the yeast mitochondrial ribosomal tunnel exit. Mitochondria contain homologues of the ribosomal proteins located at this site in bacterial ribosomes. Here, we identified proteins located in their proximity by chemical cross-linking and mass spectrometry. Our analysis revealed a complex network of interacting proteins including proteins and protein domains specific to mitochondrial ribosomes. This network includes Mba1, the membrane-bound ribosome receptor of the inner membrane, as well as Mrpl3, Mrpl13, and Mrpl27, which constitute ribosomal proteins exclusively found in mitochondria. This unique architecture of the tunnel exit is presumably an adaptation of the translation system to the specific requirements of the organelle.
Gruschke
Steffi
S
Abteilung Zellbiologie, Technische Universität Kaiserslautern, 67663 Kaiserslautern, Germany.
Gröne
Kerstin
K
Heublein
Manfred
M
Hölz
Stefanie
S
Israel
Lars
L
Imhof
Axel
A
Herrmann
Johannes M
JM
Ott
Martin
M
D002462:Cell Membrane / Q000378:metabolism; D003432:Cross-Linking Reagents / Q000737:chemistry; D020285:Cryoelectron Microscopy / Q000379:methods; D004272:DNA, Mitochondrial / Q000378:metabolism; D013058:Mass Spectrometry / Q000379:methods; D008565:Membrane Proteins / Q000378:metabolism*; D008928:Mitochondria / Q000378:metabolism*; D024101:Mitochondrial Proteins / Q000737:chemistry* / Q000378:metabolism*; D018384:Oxidative Stress; D010455:Peptides / Q000737:chemistry*; D010766:Phosphorylation; D011487:Protein Conformation; D017434:Protein Structure, Tertiary; D012269:Ribosomal Proteins / Q000737:chemistry*; D012270:Ribosomes / Q000378:metabolism*; D012441:Saccharomyces cerevisiae / Q000378:metabolism*; D029701:Saccharomyces cerevisiae Proteins / Q000737:chemistry* / Q000378:metabolism*
D003432:Cross-Linking Reagents; D004272:DNA, Mitochondrial; C100490:MBA1 protein, S cerevisiae; C489211:MRPL13 protein, S cerevisiae; C550930:MRPL3 protein, S cerevisiae; D008565:Membrane Proteins; D024101:Mitochondrial Proteins; D010455:Peptides; D012269:Ribosomal Proteins; D029701:Saccharomyces cerevisiae Proteins; C072325:mitochondrial ribosomal protein YmL27
EMBO J. 2006 Apr 19;25(8):1603-10
16601683
J Biol Chem. 2005 Apr 1;280(13):13004-11
15654078
J Biol Chem. 2001 Nov 23;276(47):43958-69
11551941
Mol Cell. 2009 May 15;34(3):344-53
19450532
Mol Biol Cell. 2009 May;20(10):2615-25
19339279
Cell. 1978 Nov;15(3):705-23
153200
Prog Nucleic Acid Res Mol Biol. 2004;77:211-61
15196894
EMBO J. 2003 Dec 15;22(24):6448-57
14657018
Eukaryot Cell. 2009 Nov;8(11):1792-802
19783770
Nucleic Acids Res. 2007;35(14):4686-703
17604309
Science. 2000 Aug 11;289(5481):905-20
10937989
Nucleic Acids Res. 1996 Sep 1;24(17):3469-71
8811105
J Cell Biol. 2005 Jul 4;170(1):27-35
15983062
J Biol Chem. 2001 Aug 31;276(35):33181-95
11402041
Eukaryot Cell. 2005 Feb;4(2):337-45
15701796
J Biol Chem. 1982 Nov 10;257(21):13028-33
6290489
Cell. 2003 Oct 3;115(1):97-108
14532006
EMBO J. 1985 Aug;4(8):2087-92
3905388
EMBO J. 2003 Dec 15;22(24):6438-47
14657017
J Cell Biol. 2001 May 28;153(5):1085-96
11381092
Nat Struct Mol Biol. 2009 Jun;16(6):589-97
19491936
Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9637-42
19497863