Glycolipozyme MPIase is essential for topology inversion of SecG during preprotein translocation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 24, 2013, Pages 9734-9739

  Moser, Michael ^a   Nagamori, Shushi ^b   Huber, Maria ^a   Tokuda, Hajime ^c   Nishiyama, Ken Ichi ^a  

^a IWATE UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c MORIOKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DIMER; GLYCOLIPOZYME; INTEGRASE; MEMBRANE PROTEIN; MEMBRANE PROTEIN INTEGRASE; PRESECRETORY PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM; ENZYME LOCALIZATION; HYDROPHILICITY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE;

BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; IMMUNOBLOTTING; INTEGRASES; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN PRECURSORS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

EUKARYOTA;

EID: 84878973922     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1303160110     Document Type: Article

References (40)

1. Rapoport TA (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450(7170):663-669.
2. Mandon EC, Trueman SF, Gilmore R (2009) Translocation of proteins through the Sec61 and SecYEG channels. Curr Opin Cell Biol 21(4):501-507.
3. du Plessis DJ, Nouwen N, Driessen AJ (2011) The Sec translocase. Biochim Biophys Acta 1808(3):851-865.
4. Breyton C, Haase W, Rapoport TA, Kühlbrandt W, Collinson I (2002) Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418(6898):662-665.
5. Van den Berg B, et al. (2004) X-ray structure of a protein-conducting channel. Nature 427(6969):36-44.
6. Zimmer J, Nam Y, Rapoport TA (2008) Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455(7215):936-943.
7. Tsukazaki T, et al. (2008) Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455(7215):988-991.
8. Mitra K, et al. (2005) Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438(7066):318- 324.
9. Nagamori S, Nishiyama K, Tokuda H (2000) Two SecG molecules present in a single protein translocation machinery are functional even after crosslinking. J Biochem 128(1):129-137. (Pubitemid 30485378)
10. Manting EH, van Der Does C, Remigy H, Engel A, Driessen AJ (2000) SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J 19(5):852-861. (Pubitemid 30119811)
11. Kaufmann A, Manting EH, Veenendaal AK, Driessen AJ, van der Does C (1999) Cysteine-directed cross-linking demonstrates that helix 3 of SecE is close to helix 2 of SecY and helix 3 of a neighboring SecE. Biochemistry 38(28):9115-9125.
12. Duong F (2003) Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase. EMBO J 22(17):4375-4384.
13. Dalal K, Chan CS, Sligar SG, Duong F (2012) Two copies of the SecY channel and acidic lipids are necessary to activate the SecA translocation ATPase. Proc Natl Acad Sci USA 109(11):4104-4109.
14. Osborne AR, Rapoport TA (2007) Protein translocation is mediated by oligomers of the SecY complex with one SecY copy forming the channel. Cell 129(1):97-110. (Pubitemid 46507582)
15. Park E, Rapoport TA (2012) Bacterial protein translocation requires only one copy of the SecY complex in vivo. J Cell Biol 198(5):881-893.
16. Yahr TL, Wickner WT (2000) Evaluating the oligomeric state of SecYEG in preprotein translocase. EMBO J 19(16):4393-4401. (Pubitemid 30623750)
17. Nishiyama K, Suzuki T, Tokuda H (1996) Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell 85(1):71-81. (Pubitemid 26116808)
18. Sugai R, Takemae K, Tokuda H, Nishiyama K (2007) Topology inversion of SecG is essential for cytosolic SecA-dependent stimulation of protein translocation. J Biol Chem 282(40):29540-29548. (Pubitemid 350043362)
19. Morita K, Tokuda H, Nishiyama K (2012) Multiple SecA molecules drive protein translocation across a single translocon with SecG inversion. J Biol Chem 287(1):455-464.
20. Nagamori S, Nishiyama K, Tokuda H (2002) Membrane topology inversion of SecG detected by labeling with a membrane-impermeable sulfhydryl reagent that causes a close association of SecG with SecA. J Biochem 132(4):629-634. (Pubitemid 35238918)
21. Nishiyama K, Tokuda H (2010) Preparation of a highly translocation- competent proOmpA/SecB complex. Protein Sci 19(12):2402-2408.
22. Nishiyama K, Mizushima S, Tokuda H (1993) A novel membrane protein involved in protein translocation across the cytoplasmic membrane of Escherichia coli. EMBO J 12(9):3409-3415. (Pubitemid 23256428)
23. van der Sluis EO, van der Vries E, Berrelkamp G, Nouwen N, Driessen AJ (2006) Topologically fixed SecG is fully functional. J Bacteriol 188(3):1188-1190. (Pubitemid 43146438)
24. Nishiyama K, et al. (2010) A novel complete reconstitution system for membrane integration of the simplest membrane protein. Biochem Biophys Res Commun 394(3):733-736.
25. Nishiyama K, et al. (2012) MPIase is a glycolipozyme essential for membrane protein integration. Nat Commun 3:1260.
26. Nishiyama K, et al. (2006) A derivative of lipid A is involved in signal recognition particle/SecYEG-dependent and -independent membrane integrations. J Biol Chem 281(47):35667-35676. (Pubitemid 46041297)
27. Douville K, Price A, Eichler J, Economou A, Wickner W (1995) SecYEG and SecA are the stoichiometric components of preprotein translocase. J Biol Chem 270(34):20106-20111.
28. van der Does C, et al. (1996) SecA is an intrinsic subunit of the Escherichia coli pre-protein translocase and exposes its carboxyl terminus to the periplasm. Mol Microbiol 22(4):619-629.
29. Duong F, Wickner W (1997) Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J 16(10):2756-2768. (Pubitemid 27226213)
30. Nishiyama K, et al. (1991) SecY is an indispensable component of the protein secretory machinery of Escherichia coli. Biochim Biophys Acta 1065(1):89-97.
31. Brundage L, Hendrick JP, Schiebel E, Driessen AJ, Wickner W (1990) The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation. Cell 62(4):649-657.
32. Guan L, Kaback HR (2007) Site-directed alkylation of cysteine to test solvent accessibility of membrane proteins. Nat Protoc 2(8):2012-2017. (Pubitemid 47308140)
33. Sardis MF, Economou A (2010) SecA: A tale of two protomers. Mol Microbiol 76(5):1070-1081.
34. Economou A, Wickner W (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78(5):835-843. (Pubitemid 24294458)
35. Economou A, Pogliano JA, Beckwith J, Oliver DB, Wickner W (1995) SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell 83(7):1171-1181. (Pubitemid 26007808)
36. Schatz PJ, Bieker KL, Ottemann KM, Silhavy TJ, Beckwith J (1991) One of three transmembrane stretches is sufficient for the functioning of the SecE protein, a membrane component of the E. coli secretion machinery. EMBO J 10(7):1749-1757. (Pubitemid 21905642)
37. Yamada H, Tokuda H, Mizushima S (1989) Proton motive force-dependent and -independent protein translocation revealed by an efficient in vitro assay system of Escherichia coli. J Biol Chem 264(3):1723-1728. (Pubitemid 19051015)
38. Nishiyama K, Hanada M, Tokuda H (1994) Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Escherichia coli at low temperature. EMBO J 13(14):3272-3277. (Pubitemid 24226941)
39. Matsuyama S, Fujita Y, Mizushima S (1993) SecD is involved in the release of translocated secretory proteins from the cytoplasmic membrane of Escherichia coli. EMBO J 12(1):265-270.
40. Narita S, Kanamaru K, Matsuyama S, Tokuda H (2003) A mutation in the membrane subunit of an ABC transporter LolCDE complex causing outer membrane localization of lipoproteins against their inner membrane-specific signals. Mol Microbiol 49(1):167-177. (Pubitemid 36792012)