Regulation by a chaperone improves substrate selectivity during cotranslational protein targeting

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

Volumn 112, Issue 25, 2015, Pages E3169-E3178

  Ariosa, Aileen ^b   Lee, Jae Ho ^a   Wang, Shuai ^a   Saraogi, Ishu ^c   Shan, Shu Ou ^a  

^a California Institute of Technology   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH BHOPAL   (India)

Author keywords

GTPases; Protein biogenesis; Ribosome; Signal recognition particle; Trigger factor

Indexed keywords

CHAPERONE; POLYPEPTIDE; RIBOSOME PROTEIN; SIGNAL RECOGNITION PARTICLE; PROTEIN;

ARTICLE; FLUORESCENCE RESONANCE ENERGY TRANSFER; MICROSOME MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TARGETING; RIBOSOME; AMINO ACID SEQUENCE; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN SYNTHESIS;

AMINO ACID SEQUENCE; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN BIOSYNTHESIS; PROTEINS; SIGNAL RECOGNITION PARTICLE; SUBSTRATE SPECIFICITY;

EID: 84935014070     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1422594112     Document Type: Article

References (78)

1. Merz F, et al. (2008) Molecular mechanism and structure of Trigger Factor bound to the translating ribosome. EMBO J 27(11):1622-1632.
2. Fedyukina DV, Cavagnero S (2011) Protein folding at the exit tunnel. Annu Rev Biophys 40:337-359.
3. Ferbitz L, et al. (2004) Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 431(7008):590-596.
4. Lakshmipathy SK, et al. (2007) Identification of nascent chain interaction sites on trigger factor. J Biol Chem 282(16):12186-12193.
5. Schlünzen F, et al. (2005) The binding mode of the trigger factor on the ribosome: Implications for protein folding and SRP interaction. Structure 13(11):1685-1694.
6. Lill R, Crooke E, Guthrie B, Wickner W (1988) The "trigger factor cycle" includes ribosomes, presecretory proteins, and the plasma membrane. Cell 54(7):1013-1018.
7. Deuerling E, Schulze-Specking A, Tomoyasu T, Mogk A, Bukau B (1999) Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400(6745): 693-696.
8. Beck K, Wu LF, Brunner J, Müller M (2000) Discrimination between SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J 19(1):134-143.
9. del Alamo M, et al. (2011) Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol 9(7):e1001100.
10. Eisner G, Moser M, Schäfer U, Beck K, Müller M (2006) Alternate recruitment of signal recognition particle and trigger factor to the signal sequence of a growing nascent polypeptide. J Biol Chem 281(11):7172-7179.
11. Powers T, Walter P (1996) The nascent polypeptide-associated complex modulates interactions between the signal recognition particle and the ribosome. Curr Biol 6(3): 331-338.
12. Lee HC, Bernstein HD (2002) Trigger factor retards protein export in Escherichia coli. J Biol Chem 277(45):43527-43535.
13. Oh E, et al. (2011) Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 147(6):1295-1308.
14. Kramer G, Boehringer D, Ban N, Bukau B (2009) The ribosome as a platform for cotranslational processing, folding and targeting of newly synthesized proteins. Nat Struct Mol Biol 16(6):589-597.
15. Ullers RS, et al. (2006) Sequence-specific interactions of nascent Escherichia coli polypeptides with trigger factor and signal recognition particle. J Biol Chem 281(20): 13999-14005.
16. Ullers RS, et al. (2003) Interplay of signal recognition particle and trigger factor at L23 near the nascent chain exit site on the Escherichia coli ribosome. J Cell Biol 161(4): 679-684.
17. Buskiewicz I, et al. (2004) Trigger factor binds to ribosome-signal-recognition particle (SRP) complexes and is excluded by binding of the SRP receptor. Proc Natl Acad Sci USA 101(21):7902-7906.
18. Schaffitzel C, et al. (2006) Structure of the E. coli signal recognition particle bound to a translating ribosome. Nature 444(7118):503-506.
19. Raine A, Ivanova N, Wikberg JE, Ehrenberg M (2004) Simultaneous binding of trigger factor and signal recognition particle to the E. coli ribosome. Biochimie 86(7):495-500.
20. Bornemann T, Holtkamp W, Wintermeyer W (2014) Interplay between trigger factor and other protein biogenesis factors on the ribosome. Nat Commun 5:4180.
21. Huber D, et al. (2011) SecA interacts with ribosomes in order to facilitate post-translational translocation in bacteria. Mol Cell 41(3):343-353.
22. Beckmann R, et al. (2001) Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107(3):361-372.
23. Mitra K, et al. (2005) Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438(7066):318-324.
24. Houben ENG, et al. (2002) YidC and SecY mediate membrane insertion of a Type I transmembrane domain. J Biol Chem 277(39):35880-35886.
25. Wickles S, et al. (2014) A structural model of the active ribosome-bound membrane protein insertase YidC. eLife 3:e03035.
26. Brandman O, et al. (2012) A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 151(5):1042-1054.
27. Bengtson MH, Joazeiro CA (2010) Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 467(7314):470-473.
28. Defenouillère Q, et al. (2013) Cdc48-associated complex bound to 60S particles is required for the clearance of aberrant translation products. Proc Natl Acad Sci USA 110(13):5046-5051.
29. Inada T (2013) Quality control systems for aberrant mRNAs induced by aberrant translation elongation and termination. Biochim Biophys Acta 1829(6-7):634-642.
30. Verma R, Oania RS, Kolawa NJ, Deshaies RJ (2013) Cdc48/p97 promotes degradation of aberrant nascent polypeptides bound to the ribosome. eLife 2:e00308.
31. Akopian D, Shen K, Zhang X, Shan S-O (2013) Signal recognition particle: An essential protein-targeting machine. Annu Rev Biochem 82:693-721.
32. Zhang X, Kung S, Shan SO (2008) Demonstration of a multistep mechanism for assembly of the SRP x SRP receptor complex: Implications for the catalytic role of SRP RNA. J Mol Biol 381(3):581-593.
33. Zhang X, Schaffitzel C, Ban N, Shan SO (2009) Multiple conformational switches in a GTPase complex control co-translational protein targeting. Proc Natl Acad Sci USA 106(6):1754-1759.
34. Holtkamp W, et al. (2012) Dynamic switch of the signal recognition particle from scanning to targeting. Nat Struct Mol Biol 19(12):1332-1337.
35. Zhang X, et al. (2011) Direct visualization reveals dynamics of a transient intermediate during protein assembly. Proc Natl Acad Sci USA 108(16):6450-6455.
36. Egea PF, et al. (2004) Substrate twinning activates the signal recognition particle and its receptor. Nature 427(6971):215-221.
37. Focia PJ, Shepotinovskaya IV, Seidler JA, Freymann DM (2004) Heterodimeric GTPase core of the SRP targeting complex. Science 303(5656):373-377.
38. Lam VQ, Akopian D, Rome M, Henningsen D, Shan S-O (2010) Lipid activation of the signal recognition particle receptor provides spatial coordination of protein targeting. J Cell Biol 190(4):623-635.
39. Zhang X, Shan S-O (2014) Fidelity of cotranslational protein targeting by the signal recognition particle. Annu Rev Biophys 43:381-408.
40. Zhang X, Rashid R, Wang K, Shan SO (2010) Sequential checkpoints govern substrate selection during cotranslational protein targeting. Science 328(5979):757-760.
41. Saraogi I, Akopian D, Shan S-O (2014) Regulation of cargo recognition, commitment, and unloading drives cotranslational protein targeting. J Cell Biol 205(5):693-706.
42. Shen K, Zhang X, Shan S-O (2011) Synergistic actions between the SRP RNA and translating ribosome allow efficient delivery of the correct cargos during cotranslational protein targeting. RNA 17(5):892-902.
43. Maier R, Eckert B, Scholz C, Lilie H, Schmid FX (2003) Interaction of trigger factor with the ribosome. J Mol Biol 326(2):585-592.
44. Kramer G, et al. (2002) L23 protein functions as a chaperone docking site on the ribosome. Nature 419(6903):171-174.
45. Kaiser CM, et al. (2006) Real-time observation of trigger factor function on translating ribosomes. Nature 444(7118):455-460.
46. Rutkowska A, et al. (2008) Dynamics of trigger factor interaction with translating ribosomes. J Biol Chem 283(7):4124-4132.
47. Siegel V, Walter P (1988) The affinity of signal recognition particle for presecretory proteins is dependent on nascent chain length. EMBO J 7(6):1769-1775.
48. Saraogi I, Zhang D, Chandrasekaran S, Shan S-O (2011) Site-specific fluorescent labeling of nascent proteins on the translating ribosome. J Am Chem Soc 133(38): 14936-14939.
49. Valent QA, et al. (1995) Early events in preprotein recognition in E. coli: Interaction of SRP and trigger factor with nascent polypeptides. EMBO J 14(22):5494-5505.
50. von Loeffelholz O, et al. (2013) Structural basis of signal sequence surveillance and selection by the SRP-FtsY complex. Nat Struct Mol Biol 20(5):604-610.
51. Szabady RL, Peterson JH, Skillman KM, Bernstein HD (2005) An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter. Proc Natl Acad Sci USA 102(1):221-226.
52. Peterson JH, Szabady RL, Bernstein HD (2006) An unusual signal peptide extension inhibits the binding of bacterial presecretory proteins to the signal recognition particle, trigger factor, and the SecYEG complex. J Biol Chem 281(14):9038-9048.
53. Valent QA, et al. (1997) Nascent membrane and presecretory proteins synthesized in Escherichia coli associate with signal recognition particle and trigger factor. Mol Microbiol 25(1):53-64.
54. Walter P, Blobel G (1981) Translocation of proteins across the endoplasmic reticulum III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J Cell Biol 91(2 Pt 1):557-561.
55. Saraogi I, Shan SO (2011) Molecular mechanism of co-translational protein targeting by the signal recognition particle. Traffic 12(5):535-542.
56. Estrozi LF, Boehringer D, Shan S-O, Ban N, Schaffitzel C (2011) Cryo-EM structure of the E. coli translating ribosome in complex with SRP and its receptor. Nat Struct Mol Biol 18(1):88-90.
57. Flanagan JJ, et al. (2003) Signal recognition particle binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J Biol Chem 278(20):18628-18637.
58. Noriega TR, et al. (2014) Signal recognition particle-ribosome binding is sensitive to nascent chain length. J Biol Chem 289(28):19294-19305.
59. Drew D, Fröderberg L, Baars L, de Gier J-WL (2003) Assembly and overexpression of membrane proteins in Escherichia coli. Biochim Biophys Acta 1610(1):3-10.
60. Shan S-O, Chandrasekar S, Walter P (2007) Conformational changes in the GTPase modules of the signal reception particle and its receptor drive initiation of protein translocation. J Cell Biol 178(4):611-620.
61. Powers T, Walter P (1997) Co-translational protein targeting catalyzed by the Escherichia coli signal recognition particle and its receptor. EMBO J 16(16):4880-4886.
62. Schulze RJ, et al. (2014) Membrane protein insertion and proton-motive-force-dependent secretion through the bacterial holo-translocon SecYEG-SecDF-YajC-YidC. Proc Natl Acad Sci USA 111(13):4844-4849.
63. Koch HG, et al. (1999) In vitro studies with purified components reveal signal recognition particle (SRP) and SecA/SecB as constituents of two independent protein-targeting pathways of Escherichia coli. Mol Biol Cell 10(7):2163-2173.
64. Neumann-Haefelin C, Schäfer U, Müller M, Koch HG (2000) SRP-dependent cotranslational targeting and SecA-dependent translocation analyzed as individual steps in the export of a bacterial protein. EMBO J 19(23):6419-6426.
65. Valent QA, et al. (1998) The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J 17(9):2504-2512.
66. Leidig C, et al. (2013) Structural characterization of a eukaryotic chaperone - The ribosome-associated complex. Nat Struct Mol Biol 20(1):23-28.
67. Frauenfeld J, et al. (2011) Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nat Struct Mol Biol 18(5):614-621.
68. Gogala M, et al. (2014) Structures of the Sec61 complex engaged in nascent peptide translocation or membrane insertion. Nature 506(7486):107-110.
69. Knoops K, Schoehn G, Schaffitzel C (2012) Cryo-electron microscopy of ribosomal complexes in cotranslational folding, targeting, and translocation. Wiley Interdiscip Rev RNA 3(3):429-441.
70. Bingel-Erlenmeyer R, et al. (2008) A peptide deformylase-ribosome complex reveals mechanism of nascent chain processing. Nature 452(7183):108-111.
71. Kohler R, et al. (2009) YidC and Oxa1 form dimeric insertion pores on the translating ribosome. Mol Cell 34(3):344-353.
72. Halic M, et al. (2006) Following the signal sequence from ribosomal tunnel exit to signal recognition particle. Nature 444(7118):507-511.
73. Park E, et al. (2014) Structure of the SecY channel during initiation of protein translocation. Nature 506(7486):102-106.
74. Voorhees RM, Fernández IS, Scheres SH, Hegde RS (2014) Structure of the mammalian ribosome-Sec61 complex to 3.4 Å resolution. Cell 157(7):1632-1643.
75. Zhang D, Shan S-O (2012) Translation elongation regulates substrate selection by the signal recognition particle. J Biol Chem 287(10):7652-7660.
76. Peluso P, Shan SO, Nock S, Herschlag D, Walter P (2001) Role of SRP RNA in the GTPase cycles of Ffh and FtsY. Biochemistry 40(50):15224-15233.
77. Kramer G, et al. (2004) Functional dissection of Escherichia coli trigger factor: Unraveling the function of individual domains. J Bacteriol 186(12):3777-3784.
78. Schaffitzel C, Ban N, Shan S-O (2007) Generation of ribosome nascent chain complexes for structural and functional studies. J Struct Biol 158(3):463-471.