A Conserved Trimerization Motif Controls the Topology of Short Coiled Coils

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2005 Sep 21

PMID 16172398

Citations 43

Authors

Richard A Kammerer

Dirk Kostrewa

Pavlos Progias

Srinivas Honnappa

David Avila

Ariel Lustig

Fritz K Winkler

Jean Pieters

Michel O Steinmetz

Affiliations

Soon will be listed here.

Abstract

In recent years, short coiled coils have been used for applications ranging from biomaterial to medical sciences. For many of these applications knowledge of the factors that control the topology of the engineered protein systems is essential. Here, we demonstrate that trimerization of short coiled coils is determined by a distinct structural motif that encompasses specific networks of surface salt bridges and optimal hydrophobic packing interactions. The motif is conserved among intracellular, extracellular, viral, and synthetic proteins and defines a universal molecular determinant for trimer formation of short coiled coils. In addition to being of particular interest for the biotechnological production of candidate therapeutic proteins, these findings may be of interest for viral drug development strategies.

Citing Articles

The interferon stimulated gene-encoded protein HELZ2 inhibits human LINE-1 retrotransposition and LINE-1 RNA-mediated type I interferon induction.

Luqman-Fatah A, Watanabe Y, Uno K, Ishikawa F, Moran J, Miyoshi T Nat Commun. 2023; 14(1):203.

PMID: 36639706 PMC: 9839780. DOI: 10.1038/s41467-022-35757-6.

Nucleation, stabilization, and disassembly of branched actin networks.

Gautreau A, Fregoso F, Simanov G, Dominguez R Trends Cell Biol. 2021; 32(5):421-432.

PMID: 34836783 PMC: 9018471. DOI: 10.1016/j.tcb.2021.10.006.

Structural insights into coronin oligomerization domain and F-actin interaction.

Parihar P, Singh A, Karade S, Sahasrabuddhe A, Pratap J Curr Res Struct Biol. 2021; 3:268-276.

PMID: 34746809 PMC: 8554105. DOI: 10.1016/j.crstbi.2021.10.002.

Steroidal glycoalkaloids from target cytoskeletal proteins: an analysis.

Ahmad R PeerJ. 2019; 7:e6012.

PMID: 30627484 PMC: 6321755. DOI: 10.7717/peerj.6012.

The FapF Amyloid Secretion Transporter Possesses an Atypical Asymmetric Coiled Coil.

Rouse S, Stylianou F, Wu H, Berry J, Sewell L, Morgan R J Mol Biol. 2018; 430(20):3863-3871.

PMID: 29886016 PMC: 6173795. DOI: 10.1016/j.jmb.2018.06.007.

References

Tripet B, Wagschal K, Lavigne P, Mant C, Hodges R . Effects of side-chain characteristics on stability and oligomerization state of a de novo-designed model coiled-coil: 20 amino acid substitutions in position "d". J Mol Biol. 2000; 300(2):377-402. DOI: 10.1006/jmbi.2000.3866. View

Gatfield J, Albrecht I, Zanolari B, Steinmetz M, Pieters J . Association of the leukocyte plasma membrane with the actin cytoskeleton through coiled coil-mediated trimeric coronin 1 molecules. Mol Biol Cell. 2005; 16(6):2786-98. PMC: 1142424. DOI: 10.1091/mbc.e05-01-0042. View

Rieker J, Hu J . Molecular applications of fusions to leucine zippers. Methods Enzymol. 2000; 328:282-96. DOI: 10.1016/s0076-6879(00)28403-6. View

Burkhard P, Meier M, Lustig A . Design of a minimal protein oligomerization domain by a structural approach. Protein Sci. 2001; 9(12):2294-301. PMC: 2144530. DOI: 10.1110/ps.9.12.2294. View

Walshaw J, Woolfson D . Socket: a program for identifying and analysing coiled-coil motifs within protein structures. J Mol Biol. 2001; 307(5):1427-50. DOI: 10.1006/jmbi.2001.4545. View

Akey D, Malashkevich V, Kim P . Buried polar residues in coiled-coil interfaces. Biochemistry. 2001; 40(21):6352-60. DOI: 10.1021/bi002829w. View

Malashkevich V, Singh M, Kim P . The trimer-of-hairpins motif in membrane fusion: Visna virus. Proc Natl Acad Sci U S A. 2001; 98(15):8502-6. PMC: 37465. DOI: 10.1073/pnas.151254798. View

Arndt K, Muller K, Pluckthun A . Helix-stabilized Fv (hsFv) antibody fragments: substituting the constant domains of a Fab fragment for a heterodimeric coiled-coil domain. J Mol Biol. 2001; 312(1):221-8. DOI: 10.1006/jmbi.2001.4915. View

Eckert D, Kim P . Design of potent inhibitors of HIV-1 entry from the gp41 N-peptide region. Proc Natl Acad Sci U S A. 2001; 98(20):11187-92. PMC: 58705. DOI: 10.1073/pnas.201392898. View

10.

Tai L, McFall S, Huang K, Demeler B, Fox S, Brubaker K . Structure-function analysis of the heat shock factor-binding protein reveals a protein composed solely of a highly conserved and dynamic coiled-coil trimerization domain. J Biol Chem. 2001; 277(1):735-45. DOI: 10.1074/jbc.M108604200. View

11.

Contegno F, Cioce M, Pelicci P, Minucci S . Targeting protein inactivation through an oligomerization chain reaction. Proc Natl Acad Sci U S A. 2002; 99(4):1865-9. PMC: 122285. DOI: 10.1073/pnas.042460299. View

12.

Frank S, Schulthess T, Landwehr R, Lustig A, Mini T, Jeno P . Characterization of the matrilin coiled-coil domains reveals seven novel isoforms. J Biol Chem. 2002; 277(21):19071-9. DOI: 10.1074/jbc.M202146200. View

13.

Burkhard P, Ivaninskii S, Lustig A . Improving coiled-coil stability by optimizing ionic interactions. J Mol Biol. 2002; 318(3):901-10. DOI: 10.1016/S0022-2836(02)00114-6. View

14.

Meier M, Lustig A, Aebi U, Burkhard P . Removing an interhelical salt bridge abolishes coiled-coil formation in a de novo designed peptide. J Struct Biol. 2002; 137(1-2):65-72. DOI: 10.1006/jsbi.2002.4467. View

15.

Vinson C, Myakishev M, Acharya A, Mir A, Moll J, Bonovich M . Classification of human B-ZIP proteins based on dimerization properties. Mol Cell Biol. 2002; 22(18):6321-35. PMC: 135624. DOI: 10.1128/MCB.22.18.6321-6335.2002. View

16.

Ryadnov M, Ceyhan B, Niemeyer C, Woolfson D . "Belt and braces": a peptide-based linker system of de novo design. J Am Chem Soc. 2003; 125(31):9388-94. DOI: 10.1021/ja0352045. View

17.

Latvanlehto A, Snellman A, Tu H, Pihlajaniemi T . Type XIII collagen and some other transmembrane collagens contain two separate coiled-coil motifs, which may function as independent oligomerization domains. J Biol Chem. 2003; 278(39):37590-9. DOI: 10.1074/jbc.M305974200. View

18.

McAlinden A, Smith T, Sandell L, Ficheux D, Parry D, Hulmes D . Alpha-helical coiled-coil oligomerization domains are almost ubiquitous in the collagen superfamily. J Biol Chem. 2003; 278(43):42200-7. DOI: 10.1074/jbc.M302429200. View

19.

Kammerer R, Kostrewa D, Zurdo J, Detken A, Garcia-Echeverria C, Green J . Exploring amyloid formation by a de novo design. Proc Natl Acad Sci U S A. 2004; 101(13):4435-40. PMC: 384765. DOI: 10.1073/pnas.0306786101. View

20.

Cho C, Kammerer R, Lee H, Steinmetz M, Ryu Y, Lee S . COMP-Ang1: a designed angiopoietin-1 variant with nonleaky angiogenic activity. Proc Natl Acad Sci U S A. 2004; 101(15):5547-52. PMC: 397420. DOI: 10.1073/pnas.0307574101. View