Regulation of Structural Dynamics Within a Signal Recognition Particle Promotes Binding of Protein Targeting Substrates

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2015 Apr 29

PMID 25918165

Citations 14

Authors

Feng Gao

Alicia D Kight

Rory Henderson

Srinivas Jayanthi

Parth Patel

Marissa Murchison

Priyanka Sharma

Robyn L Goforth

Thallapuranam Krishnaswamy Suresh Kumar

Ralph L Henry

Colin D Heyes

Affiliations

Soon will be listed here.

Abstract

Protein targeting is critical in all living organisms and involves a signal recognition particle (SRP), an SRP receptor, and a translocase. In co-translational targeting, interactions among these proteins are mediated by the ribosome. In chloroplasts, the light-harvesting chlorophyll-binding protein (LHCP) in the thylakoid membrane is targeted post-translationally without a ribosome. A multidomain chloroplast-specific subunit of the SRP, cpSRP43, is proposed to take on the role of coordinating the sequence of targeting events. Here, we demonstrate that cpSRP43 exhibits significant interdomain dynamics that are reduced upon binding its SRP binding partner, cpSRP54. We showed that the affinity of cpSRP43 for the binding motif of LHCP (L18) increases when cpSRP43 is complexed to the binding motif of cpSRP54 (cpSRP54pep). These results support the conclusion that substrate binding to the chloroplast SRP is modulated by protein structural dynamics in which a major role of cpSRP54 is to improve substrate binding efficiency to the cpSRP.

Citing Articles

The role of chloroplast SRP54 domains and its C-terminal tail region in post- and co-translational protein transport in vivo.

Bischoff A, Ortelt J, Dunschede B, Zegarra V, Bedrunka P, Bange G J Exp Bot. 2024; 75(18):5734-5749.

PMID: 38989593 PMC: 11427828. DOI: 10.1093/jxb/erae293.

cpSRP43 Is Both Highly Flexible and Stable: Structural Insights Using a Combined Experimental and Computational Approach.

Benton M, Furr M, Govind Kumar V, Polasa A, Gao F, Heyes C J Chem Inf Model. 2023; 63(13):4125-4137.

PMID: 37336508 PMC: 10336970. DOI: 10.1021/acs.jcim.3c00319.

Protein Targeting Into the Thylakoid Membrane Through Different Pathways.

Zhu D, Xiong H, Wu J, Zheng C, Lu D, Zhang L Front Physiol. 2022; 12:802057.

PMID: 35095563 PMC: 8790069. DOI: 10.3389/fphys.2021.802057.

Transient local secondary structure in the intrinsically disordered C-term of the Albino3 insertase.

Baucom D, Furr M, Govind Kumar V, Okoto P, Losey J, Henry R Biophys J. 2021; 120(22):4992-5004.

PMID: 34662559 PMC: 8633824. DOI: 10.1016/j.bpj.2021.10.013.

A Disorder-to-Order Transition Activates an ATP-Independent Membrane Protein Chaperone.

Siegel A, McAvoy C, Lam V, Liang F, Kroon G, Miaou E J Mol Biol. 2020; 432(24):166708.

PMID: 33188783 PMC: 7780713. DOI: 10.1016/j.jmb.2020.11.007.

References

Lewis N, Marty N, Kathir K, Rajalingam D, Kight A, Daily A . A dynamic cpSRP43-Albino3 interaction mediates translocase regulation of chloroplast signal recognition particle (cpSRP)-targeting components. J Biol Chem. 2010; 285(44):34220-30. PMC: 2962520. DOI: 10.1074/jbc.M110.160093. View

Cui B, Wu C, Chen L, Ramirez A, Bearer E, Li W . One at a time, live tracking of NGF axonal transport using quantum dots. Proc Natl Acad Sci U S A. 2007; 104(34):13666-71. PMC: 1959439. DOI: 10.1073/pnas.0706192104. View

Groves M, Mant A, Kuhn A, Koch J, Dubel S, Robinson C . Functional characterization of recombinant chloroplast signal recognition particle. J Biol Chem. 2001; 276(30):27778-86. DOI: 10.1074/jbc.M103470200. View

Roy R, Hohng S, Ha T . A practical guide to single-molecule FRET. Nat Methods. 2008; 5(6):507-16. PMC: 3769523. DOI: 10.1038/nmeth.1208. View

Brooks B, Brooks 3rd C, MacKerell Jr A, Nilsson L, Petrella R, Roux B . CHARMM: the biomolecular simulation program. J Comput Chem. 2009; 30(10):1545-614. PMC: 2810661. DOI: 10.1002/jcc.21287. View

Marty N, Rajalingam D, Kight A, Lewis N, Fologea D, Kumar T . The membrane-binding motif of the chloroplast signal recognition particle receptor (cpFtsY) regulates GTPase activity. J Biol Chem. 2009; 284(22):14891-903. PMC: 2685671. DOI: 10.1074/jbc.M900775200. View

Arkhipov A, Freddolino P, Schulten K . Stability and dynamics of virus capsids described by coarse-grained modeling. Structure. 2006; 14(12):1767-77. DOI: 10.1016/j.str.2006.10.003. View

Cain P, Holdermann I, Sinning I, Johnson A, Robinson C . Binding of chloroplast signal recognition particle to a thylakoid membrane protein substrate in aqueous solution and delineation of the cpSRP43-substrate interaction domain. Biochem J. 2011; 437(1):149-55. DOI: 10.1042/BJ20110270. View

Yang H, Luo G, Karnchanaphanurach P, Louie T, Rech I, Cova S . Protein conformational dynamics probed by single-molecule electron transfer. Science. 2003; 302(5643):262-6. DOI: 10.1126/science.1086911. View

10.

Jaru-Ampornpan P, Shen K, Lam V, Ali M, Doniach S, Jia T . ATP-independent reversal of a membrane protein aggregate by a chloroplast SRP subunit. Nat Struct Mol Biol. 2010; 17(6):696-702. PMC: 2917185. DOI: 10.1038/nsmb.1836. View

11.

Nishimura S, Lord S, Klein L, Willets K, He M, Lu Z . Diffusion of lipid-like single-molecule fluorophores in the cell membrane. J Phys Chem B. 2006; 110(15):8151-7. PMC: 1702323. DOI: 10.1021/jp0574145. View

12.

Payan L, Cline K . A stromal protein factor maintains the solubility and insertion competence of an imported thylakoid membrane protein. J Cell Biol. 1991; 112(4):603-13. PMC: 2288854. DOI: 10.1083/jcb.112.4.603. View

13.

Lu H, Xun L, Xie X . Single-molecule enzymatic dynamics. Science. 1998; 282(5395):1877-82. DOI: 10.1126/science.282.5395.1877. View

14.

Wriggers W . Using Situs for the integration of multi-resolution structures. Biophys Rev. 2010; 2(1):21-27. PMC: 2821521. DOI: 10.1007/s12551-009-0026-3. View

15.

Pettersen E, Goddard T, Huang C, Couch G, Greenblatt D, Meng E . UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25(13):1605-12. DOI: 10.1002/jcc.20084. View

16.

Tzvetkova-Chevolleau T, Hutin C, Noel L, Goforth R, Carde J, Caffarri S . Canonical signal recognition particle components can be bypassed for posttranslational protein targeting in chloroplasts. Plant Cell. 2007; 19(5):1635-48. PMC: 1913721. DOI: 10.1105/tpc.106.048959. View

17.

Talaga D, Lau W, Roder H, Tang J, Jia Y, Degrado W . Dynamics and folding of single two-stranded coiled-coil peptides studied by fluorescent energy transfer confocal microscopy. Proc Natl Acad Sci U S A. 2000; 97(24):13021-6. PMC: 27171. DOI: 10.1073/pnas.97.24.13021. View

18.

Henry R . SRP: adapting to life in the chloroplast. Nat Struct Mol Biol. 2010; 17(6):676-7. DOI: 10.1038/nsmb0610-676. View

19.

Phillips J, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E . Scalable molecular dynamics with NAMD. J Comput Chem. 2005; 26(16):1781-802. PMC: 2486339. DOI: 10.1002/jcc.20289. View

20.

Dickson R, Cubitt A, Tsien R, Moerner W . On/off blinking and switching behaviour of single molecules of green fluorescent protein. Nature. 1997; 388(6640):355-8. DOI: 10.1038/41048. View