Energy use by biological protein transport pathways

Trends in Biochemical Sciences

Volumn 28, Issue 8, 2003, Pages 442-451

  Alder, Nathan N ^a   Theg, Steven M ^b  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CARRIER PROTEIN; CIS ACTING ELEMENT; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; TRANS ACTING FACTOR;

CELL FUNCTION; CELL MEMBRANE; CELL MOTION; CELL STRUCTURE; ENERGY; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; PROTON MOTIVE FORCE; REVIEW; THERMODYNAMICS;

EID: 0041656271     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0968-0004(03)00167-1     Document Type: Review

References (75)

1. Schatz G., Dobberstein B. Common principles of protein translocation across membranes. Science. 271:1996;1519-1525.
2. Manting E.H., Driessen A.J.M. Escherichia coli translocase: the unraveling of a molecular machine. Mol. Microbiol. 37:2000;226-238.
3. Johnson A.E., van Waes M.A. The translocon: a dynamic gateway at the ER membrane. Annu. Rev. Cell Dev. Biol. 15:1999;799-842.
4. Rapoport T.A., et al. Posttranslational protein translocation across the membrane of the endoplasmic reticulum. Biol. Chem. 380:1999;1143-1150.
5. Robinson C., Bolhuis A. Protein targeting by the twin-arginine translocation pathway. Nat. Rev. Mol. Cell Biol. 2:2001;350-356.
6. Luirink J., et al. YidC/Oxa1p/Alb3: evolutionarily conserved mediators of membrane protein assembly. FEBS Lett. 501:2001;1-5.
7. Neupert W., Brunner M. The protein import motor of mitochondria. Nat. Rev. Mol. Cell Biol. 3:2002;555-565.
8. Jensen R.E., Dunn C.D. Protein import into and across the mitochondrial inner membrane: role of the TIM23 and TIM22 translocons. Biochim. Biophys. Acta. 1592:2002;25-34.
9. Jarvis P., Soll J. Toc, Tic, and chloroplast protein import. Biochim. Biophys. Acta. 1541:2001;64-79.
10. Jackson-Constan D., et al. Molecular chaperones involved in chloroplast protein import. Biochim. Biophys. Acta. 1541:2001;102-113.
11. + and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell. 64:1991;927-939.
12. van der Wolk J.P.W., et al. The catalytic cycle of the Escherichia coli SecA ATPase comprises two distinct preprotein translocation events. EMBO J. 16:1997;7297-7304.
13. Karamanou S., et al. A molecular switch in SecA protein couples ATP hydrolysis to protein translocation. Mol. Microbiol. 34:1999;1133-1145.
14. Sianidis G., et al. Cross-talk between catalytic and regulatory elements in a DEAD motor domain is essential for SecA function. EMBO J. 20:2001;961-970.
15. Baud C., et al. Allosteric communication between signal peptides and the SecA protein DEAD motor ATPase domain. J. Biol. Chem. 277:2002;13724-13731.
16. den Blaauwen T., et al. Thermodynamics of nucleotide binding to NBS-I of the Bacillus subtilis preprotein translocase subunit SecA. FEBS Lett. 458:1999;145-150.
17. Hunt J.F., et al. Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science. 297:2002;2018-2026.
18. Sharma V., et al. Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase. Proc. Natl. Acad. Sci. U. S. A. 100:2003;2243-2248.
19. Caruthers J.M., McKay D.B. Helicase structure and mechanism. Curr. Opin. Struct. Biol. 12:2002;123-133.
20. Dapic V., Oliver D. Distinct membrane binding properties of N- and C-terminal domains of Escherichia coli SecA ATPase. J. Biol. Chem. 275:2000;25000-25007.
21. Lill R., et al. SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli. EMBO J. 8:1989;961-966.
22. Ramamurthy V., Oliver D. Topology of the integral membrane form of Escherichia coli SecA protein reveals multiple periplasmically exposed regions and modulation by ATP binding. J. Biol. Chem. 272:1997;23239-23246.
23. Duong F., Wickner W. The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J. 16:1997;4871-4879.
24. Nishiyama K.-I., et al. Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell. 85:1996;71-81.
25. Nishiyama K., et al. Membrane deinsertion of SecA underlying proton motive force-dependent stimulation of protein translocation. EMBO J. 18:1999;1049-1058.
26. Bukau B., Horwich A.L. The Hsp70 and Hsp60 chaperone machines. Cell. 92:1998;351-366.
27. Flaherty K.M., et al. Structural basis of the 70-kilodalton heat shock cognate protein ATP hydrolytic activity. II. Structure of the active site with ADP or ATP bound to wild type and mutant ATPase fragment. J. Biol. Chem. 269:1994;12899-12907.
28. Zhu X., et al. Structural analysis of substrate binding by the molecular chaperone DnaK. Science. 272:1996;1606-1614.
29. Corsi A.K., Schekman R. The lumenal domain of Sec63p stimulates the ATPase activity of BiP and mediates BiP recruitment to the translocon in Saccharomyces cerevisiae. J. Cell Biol. 137:1997;1483-1493.
30. Chung K.T., et al. BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. J. Biol. Chem. 277:2002;47557-47563.
31. Lim J.H., et al. The mitochondrial Hsp70-dependent import system actively unfolds preproteins and shortens the lag phase of translocation. EMBO J. 20:2001;941-950.
32. Chauwin J.F., et al. Strong precursor-pore interactions constrain models for mitochondrial protein import. Biophys. J. 74:1998;1732-1743.
33. Voisine C., et al. The protein import motor of mitochondria: unfolding and trapping of preproteins are distinct and separable functions of matrix Hsp70. Cell. 97:1999;565-574.
34. Strub A., et al. The Hsp70 peptide-binding domain determines the interaction of the ATPase domain with Tim44 in mitochondria. EMBO J. 21:2002;2626-2635.
35. Ungermann C., et al. The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science. 266:1994;1250-1253.
36. Matlack K.E., et al. BiP acts as a molecular ratchet during posttranslational transport of prepro-α factor across the ER membrane. Cell. 97:1999;553-564.
37. Moro F., et al. Mitochondrial protein import: molecular basis of the ATP-dependent interaction of MtHsp70 with Tim44. J. Biol. Chem. 277:2002;6874-6880.
38. Misselwitz B., et al. (1999) Interaction of BiP with the J-domain of the sec63p component of the endoplasmic reticulum protein translocation complex. J. Biol. Chem. 274:1999;20110-20115.
39. Okamoto K., et al. The protein import motor of mitochondria: a targeted molecular ratchet driving unfolding and translocation. EMBO J. 21:2002;3659-3671.
40. Liu Q., et al. Regulated cycling of mitochondrial Hsp70 at the protein import channel. Science. 300:2003;139-141.
41. Theg S.M., et al. Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes. J. Biol. Chem. 264:1989;6730-6736.
42. Bourne H.R., et al. The GTPase superfamily: a conserved switch for diverse cell functions. Nature. 348:1990;125-132.
43. Bourne H.R., et al. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 349:1991;117-127.
44. Yarus M. Proofreading, NTPases and translation: constraints on accurate biochemistry. Trends Biochem. Sci. 17:1992;130-133.
45. Keenan R.J., et al. The signal recognition particle. Annu. Rev. Biochem. 70:2001;755-775.
46. Rapiejko P.J., Gilmore R. Empty site forms of the SRP54 and SR alpha GTPases mediate targeting of ribosome-nascent chain complexes to the endoplasmic reticulum. Cell. 89:1997;703-713.
47. Smith M.D., et al. The targeting of the atToc159 preprotein receptor to the chloroplast outer membrane is mediated by its GTPase domain and is regulated by GTP. J. Cell Biol. 159:2002;833-843.
48. Schleiff E., et al. A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proc. Natl. Acad. Sci. U. S. A. 100:2003;4604-4609.
49. Martin J., et al. Role of an energized inner membrane in mitochondrial protein import. Δψ drives the movement of presequences. J. Biol. Chem. 266:1991;18051-18057.
50. Huang S., et al. Protein unfolding by the mitochondrial membrane potential. Nat. Struct. Biol. 9:2002;301-307.
51. Rehling P., et al. Protein insertion into the mitochondrial inner membrane by a twin-pore translocase. Science. 299:2003;1747-1751.
52. Bakker E.P., Randall L.L. The requirement for energy during export of β-lactamase in Escherichia coli is fulfilled by the total protonmotive force. EMBO J. 3:1984;895-900.
53. Mitchell P. Chemiosmotic Coupling and Energy Transduction. 1968;Glynn Research Ltd.
54. Griwatz C., Junge W. Cooperative transient trapping of protons by structurally distorted chloroplast ATPase: evidence for the proton well? Biochim. Biophys. Acta. 1101:1992;244-248.
55. Shiozuka K., et al. The proton motive force lowers the level of ATP required for the in vitro translocation of a secretory protein in Escherichia coli. J. Biol. Chem. 265:1990;18843-18847.
56. Mori H., Ito K. Biochemical characterization of a mutationally altered protein translocase: proton motive force stimulation of the initiation phase of translocation. J. Bacteriol. 185:2003;405-412.
57. Driessen A.J.M., Wickner W. Proton transfer is rate-limiting for translocation of precursor proteins by the Escherichia coli translocase. Proc. Natl. Acad. Sci. U. S. A. 88:1991;2471-2475.
58. Kawasaki S., et al. Membrane vesicles containing overproduced SecY and SecE exhibit high translocation ATPase activity and countermovement of protons in a SecA- and presecretory protein-dependent manner. J. Biol. Chem. 268:1993;8193-8198.
59. + dependency of in vitro protein translocation into Escherichia coli inner-membrane vesicles varies with the signal-sequence core-region composition. Mol. Microbiol. 19:1996;1205-1214.
60. Finazzi G., et al. Thylakoid targeting of Tat passenger proteins shows no delta pH dependence in vivo. EMBO J. 22:2003;807-815.
61. Junge W., et al. The buffering capacity of the internal phase of thylakoids and the magnitude of the pH changes inside under flashing light. Biochim. Biophys. Acta. 546:1979;121-141.
62. Ma X., Cline K. Precursors bind to specific sites on thylakoid membranes prior to transport on the ΔpH protein translocation system. J. Biol. Chem. 275:2000;10016-10022.
63. Musser S.M., Theg S.M. Characterization of the early steps of OE17 precursor transport by the thylakoid ΔpH/Tat machinery. Eur. J. Biochem. 267:2000;2588-2598.
64. Musser S.M., Theg S.M. Proton transfer limits protein translocation rate by the thylakoid ΔpH/Tat machinery. Biochemistry. 39:2000;8228-8233.
65. Alder N.N., Theg S.M. Energetics of protein transport across biological membranes: a study of the thylakoid ΔpH-dependent/cpTat pathway. Cell. 112:2003;231-242.
66. Truscott K.N., et al. A presequence- and voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23. Nat. Struct. Biol. 8:2001;1074-1082.
67. Kovermann P., et al. Tim22, the essential core of the mitochondrial protein insertion complex, forms a voltage-activated and signal-gated channel. Mol. Cell. 9:2002;363-373.
68. Mori H., Cline K. A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid ΔpH/Tat translocase. J. Cell Biol. 157:2002;205-210.
69. Tani K., et al. Translocation of proOmpA possessing an intramolecular disulfide bridge into membrane vesicles of Escherichia coli. Effect of membrane energization. J. Biol. Chem. 265:1990;17341-17347.
70. von Heijne G. Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature. 341:1989;456-458.
71. Huang S., et al. Mitochondria unfold precursor proteins by unraveling them from their N-termini. Nat. Struct. Biol. 6:1999;1132-1138.
72. Bassilana M., et al. The role of the mature domain of proOmpA in the translocation ATPase reaction. J. Biol. Chem. 267:1992;25246-25250.
73. Driessen A.J.M. Precursor protein translocation by the Escherichia coli translocase is directed by the protonmotive force. EMBO J. 11:1992;847-853.
74. Ishijima A., et al. Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin. Cell. 92:1998;161-171.
75. Pierpaoli E.V., et al. The power stroke of the DnaK/DnaJ/GrpE molecular chaperone system. J. Mol. Biol. 269:1997;757-768.