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PMID: 22610688 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

In vivo protein complex topologies: sights through a cross-linking lens.

Proteomics ·Vol. 12 ·No. 10 ·2012-05-00 ·Pages 1565-75

Bruce JE

Abstract

Proteins are a remarkable class of molecules that exhibit wide diversity of shapes or topological features that underpin protein interactions and give rise to biological function. In addition to quantitation of abundance levels of proteins in biological systems under a variety of conditions, the field of proteome research has as a primary mission the assignment of function for proteins and if possible, illumination of factors that enable function. For many years, chemical cross-linking methods have been used to provide structural data on single purified proteins and purified protein complexes. However, these methods also offer the alluring possibility to extend capabilities to complex biological samples such as cell lysates or intact living cells where proteins may exhibit native topological features that do not exist in purified form. Recent efforts are beginning to provide glimpses of protein complexes and topologies in cells that suggest continued development will yield novel capabilities to view functional topological features of many proteins and complexes as they exist in cells, tissues, or other complex samples. This review will describe rationale, challenges, and a few success stories along the path of development of cross-linking technologies for measurement of in vivo protein interaction topologies.

MeSH Terms
Cross-Linking Reagents/chemistry Protein Conformation Protein Interaction Mapping/methods Proteins/analysis,chemistry,metabolism Proteomics/methods
Chemicals
Cross-Linking Reagents Proteins
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Bruce James E
Department of Genome Sciences, University of Washington, Seattle, WA 98109, USA. jimbruce@u.washington.edu
References (67)
67 references, click to expand
  1. The evolution and functional repertoire of translation proteins following the origin of life.
    Biol Direct. 2010 Apr 08;5:15 PMID: 20377891
  2. Membrane protein structure determination using cryo-electron tomography and 3D image averaging.
    Curr Opin Struct Biol. 2009 Aug;19(4):402-7 PMID: 19646859
  3. A top down approach to protein structural studies using chemical cross-linking and Fourier transform mass spectrometry.
    Rapid Commun Mass Spectrom. 2003;17(2):155-62 PMID: 12512095
  4. The beginning of a beautiful friendship: cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes.
    J Struct Biol. 2011 Mar;173(3):530-40 PMID: 21029779
  5. A novel biotinylated heterobifunctional cross-linking reagent bearing an aromatic diazirine.
    Bioorg Med Chem. 1994 Dec;2(12):1367-73 PMID: 7788299
  6. Probing three-dimensional structure of bovine serum albumin by chemical cross-linking and mass spectrometry.
    J Am Soc Mass Spectrom. 2004 Aug;15(8):1237-47 PMID: 15276171
  7. Ion channel formation by N-terminal domain: a common feature of OprFs of Pseudomonas and OmpA of Escherichia coli.
    FEMS Microbiol Lett. 2000 Sep 15;190(2):261-5 PMID: 11034289
  8. Effects of lysine acetylation in a beta-hairpin peptide: comparison of an amide-pi and a cation-pi interaction.
    J Am Chem Soc. 2006 Oct 18;128(41):13586-91 PMID: 17031973
  9. The expanding view of protein-protein interactions: complexes involving intrinsically disordered proteins.
    Phys Biol. 2011 Jun;8(3):035003 PMID: 21572179
  10. Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics.
    Mol Cell Proteomics. 2010 Aug;9(8):1634-49 PMID: 20360032
  11. Cross-linking reagents as tools for identifying components of the yeast mitochondrial protein import machinery.
    Methods Cell Biol. 1991;34:419-26 PMID: 1943816
  12. Isolation of a high-affinity functional protein complex between OmcA and MtrC: Two outer membrane decaheme c-type cytochromes of Shewanella oneidensis MR-1.
    J Bacteriol. 2006 Jul;188(13):4705-14 PMID: 16788180
  13. In vivo cross-linking and immunoprecipitation for studying dynamic Protein:DNA associations in a chromatin environment.
    Methods. 1999 Nov;19(3):425-33 PMID: 10579938
  14. Universal sharing patterns in proteomes and evolution of protein fold architecture and life.
    J Mol Evol. 2005 Apr;60(4):484-98 PMID: 15883883
  15. Regulation of Escherichia coli SOS mutagenesis by dimeric intrinsically disordered umuD gene products.
    Proc Natl Acad Sci U S A. 2008 Jan 29;105(4):1152-7 PMID: 18216271
  16. Intrinsically unstructured proteins and their functions.
    Nat Rev Mol Cell Biol. 2005 Mar;6(3):197-208 PMID: 15738986
  17. In vivo identification of the outer membrane protein OmcA-MtrC interaction network in Shewanella oneidensis MR-1 cells using novel hydrophobic chemical cross-linkers.
    J Proteome Res. 2008 Apr;7(4):1712-20 PMID: 18303833
  18. Chemical cross-linking and mass spectrometry for mapping three-dimensional structures of proteins and protein complexes.
    J Mass Spectrom. 2003 Dec;38(12):1225-37 PMID: 14696200
  19. Improved strategies for rapid identification of chemically cross-linked peptides using protein interaction reporter technology.
    J Proteome Res. 2010 Dec 3;9(12):6323-33 PMID: 20886857
  20. Structural analysis of glyceraldehyde 3-phosphate dehydrogenase from Escherichia coli: direct evidence of substrate binding and cofactor-induced conformational changes.
    Biochemistry. 2000 Sep 5;39(35):10702-10 PMID: 10978154
  21. An isotopically coded CID-cleavable biotinylated cross-linker for structural proteomics.
    Mol Cell Proteomics. 2011 Feb;10(2):M110.001420 PMID: 20622150
  22. Chemical cross-linking and mass spectrometry for protein structural modeling.
    J Mol Biol. 2003 Aug 8;331(2):303-13 PMID: 12888339
  23. Collision-induced dissociative chemical cross-linking reagents and methodology: Applications to protein structural characterization using tandem mass spectrometry analysis.
    Anal Chem. 2006 Dec 1;78(23):8059-68 PMID: 17134140
  24. Profiling the membrane proteome of Shewanella oneidensis MR-1 with new affinity labeling probes.
    J Proteome Res. 2007 Feb;6(2):724-34 PMID: 17269728
  25. Collisionally activated dissociation and electron capture dissociation of several mass spectrometry-identifiable chemical cross-linkers.
    Anal Chem. 2006 Dec 15;78(24):8183-93 PMID: 17165806
  26. Elucidation of the protein folding landscape by NMR.
    Methods Enzymol. 2005;394:299-321 PMID: 15808225
  27. An alternative topological model for Escherichia coli OmpA.
    Protein Sci. 1996 Jan;5(1):170-3 PMID: 8771211
  28. Functional dissection of an intrinsically disordered protein: understanding the roles of different domains of Knr4 protein in protein-protein interactions.
    Protein Sci. 2010 Jul;19(7):1376-85 PMID: 20506404
  29. A new cross-linking strategy: protein interaction reporter (PIR) technology for protein-protein interaction studies.
    Mol Biosyst. 2010 Jun;6(6):939-47 PMID: 20485738
  30. Structure of the periplasmic chaperone Skp suggests functional similarity with cytosolic chaperones despite differing architecture.
    Nat Struct Mol Biol. 2004 Oct;11(10):1015-20 PMID: 15361861
  31. Informatics strategies for large-scale novel cross-linking analysis.
    J Proteome Res. 2007 Sep;6(9):3412-21 PMID: 17676784
  32. The origin of protein interactions and allostery in colocalization.
    Nature. 2007 Dec 13;450(7172):983-90 PMID: 18075577
  33. Structure of Escherichia coli tryptophanase.
    Acta Crystallogr D Biol Crystallogr. 2006 Jul;62(Pt 7):814-23 PMID: 16790938
  34. Development of a novel cross-linking strategy for fast and accurate identification of cross-linked peptides of protein complexes.
    Mol Cell Proteomics. 2011 Jan;10(1):M110.002212 PMID: 20736410
  35. Identification of phosphorylation-dependent interaction partners of the adapter protein ADAP using quantitative mass spectrometry: SILAC vs (18)O-labeling.
    J Proteome Res. 2010 Aug 6;9(8):4113-22 PMID: 20568816
  36. The unfoldomics decade: an update on intrinsically disordered proteins.
    BMC Genomics. 2008 Sep 16;9 Suppl 2:S1 PMID: 18831774
  37. Chemical cross-linking and mass spectrometry as a low-resolution protein structure determination technique.
    Anal Chem. 2010 Apr 1;82(7):2636-42 PMID: 20210330
  38. Identification of cross-linked peptides after click-based enrichment using sequential collision-induced dissociation and electron transfer dissociation tandem mass spectrometry.
    Anal Chem. 2009 Jul 1;81(13):5524-32 PMID: 19496583
  39. A novel genetic system to detect protein-protein interactions.
    Nature. 1989 Jul 20;340(6230):245-6 PMID: 2547163
  40. Elucidation of protein-protein interactions using chemical cross-linking or label transfer techniques.
    Curr Opin Chem Biol. 2000 Feb;4(1):28-33 PMID: 10679368
  41. High-resolution structure of the OmpA membrane domain.
    J Mol Biol. 2000 Apr 28;298(2):273-82 PMID: 10764596
  42. Revealing novel telomere proteins using in vivo cross-linking, tandem affinity purification, and label-free quantitative LC-FTICR-MS.
    Mol Cell Proteomics. 2010 Jun;9(6):1144-56 PMID: 20097687
  43. Identification of cross-linked peptides from large sequence databases.
    Nat Methods. 2008 Apr;5(4):315-8 PMID: 18327264
  44. In vivo application of photocleavable protein interaction reporter technology.
    J Proteome Res. 2012 Feb 3;11(2):1027-41 PMID: 22168182
  45. Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions.
    Mass Spectrom Rev. 2006 Jul-Aug;25(4):663-82 PMID: 16477643
  46. Characterization of segments from the central region of BRCA1: an intrinsically disordered scaffold for multiple protein-protein and protein-DNA interactions?
    J Mol Biol. 2005 Jan 14;345(2):275-87 PMID: 15571721
  47. Lysine acetylation is a highly abundant and evolutionarily conserved modification in Escherichia coli.
    Mol Cell Proteomics. 2009 Feb;8(2):215-25 PMID: 18723842
  48. Chemical cross-linking and mass spectrometric identification of sites of interaction for UreD, UreF, and urease.
    J Biol Chem. 2004 Apr 9;279(15):15305-13 PMID: 14749331
  49. Mapping low-resolution three-dimensional protein structures using chemical cross-linking and Fourier transform ion-cyclotron resonance mass spectrometry.
    Rapid Commun Mass Spectrom. 2003;17(17):2005-14 PMID: 12913864
  50. Refolded outer membrane protein A of Escherichia coli forms ion channels with two conductance states in planar lipid bilayers.
    J Biol Chem. 2000 Jan 21;275(3):1594-600 PMID: 10636850
  51. Cross-linking measurements of in vivo protein complex topologies.
    Mol Cell Proteomics. 2011 Oct;10(10):M110.006841 PMID: 21697552
  52. Chemical cross-linking and mass spectrometry as structure determination tools.
    Eur J Mass Spectrom (Chichester). 2007;13(2):105-13 PMID: 17881777
  53. Identification of protein-protein interactions and topologies in living cells with chemical cross-linking and mass spectrometry.
    Mol Cell Proteomics. 2009 Mar;8(3):409-20 PMID: 18936057
  54. Selective enrichment and identification of azide-tagged cross-linked peptides using chemical ligation and mass spectrometry.
    J Am Soc Mass Spectrom. 2010 Aug;21(8):1432-45 PMID: 20472459
  55. Chemical cross-linking of a dimeric protein on a modified lectin matrix. A general probe for the chemical topology of oligomeric glycoproteins.
    Biochem J. 1981 Mar 1;193(3):825-8 PMID: 6796053
  56. Combinatorial electrostatic collision-induced dissociative chemical cross-linking reagents for probing protein surface topology.
    Anal Chem. 2010 Jul 15;82(14):6215-23 PMID: 20560670
  57. Chemical cross-linking and protein-protein interactions-a review with illustrative protocols.
    Bioorg Chem. 2004 Dec;32(6):451-72 PMID: 15530987
  58. Phosphorylation-dependent protein interaction with Trypanosoma brucei 14-3-3 proteins that display atypical target recognition.
    PLoS One. 2010 Dec 21;5(12):e15566 PMID: 21203569
  59. Mass spectrometry identifiable cross-linking strategy for studying protein-protein interactions.
    Anal Chem. 2005 Jan 1;77(1):311-8 PMID: 15623310
  60. Short Linear Motifs recognized by SH2, SH3 and Ser/Thr Kinase domains are conserved in disordered protein regions.
    BMC Genomics. 2008 Sep 16;9 Suppl 2:S26 PMID: 18831792
  61. Identification of protein-protein interactions using in vivo cross-linking and mass spectrometry.
    Proteomics. 2004 Dec;4(12):3845-54 PMID: 15540166
  62. The cavity-chaperone Skp protects its substrate from aggregation but allows independent folding of substrate domains.
    Proc Natl Acad Sci U S A. 2009 Feb 10;106(6):1772-7 PMID: 19181847
  63. Xlink-identifier: an automated data analysis platform for confident identifications of chemically cross-linked peptides using tandem mass spectrometry.
    J Proteome Res. 2011 Mar 4;10(3):923-31 PMID: 21175198
  64. Signal transduction via unstructured protein conduits.
    Nat Chem Biol. 2008 Apr;4(4):229-30 PMID: 18347590
  65. Mapping the topology and determination of a low-resolution three-dimensional structure of the calmodulin-melittin complex by chemical cross-linking and high-resolution FTICRMS: direct demonstration of multiple binding modes.
    Biochemistry. 2004 Apr 27;43(16):4703-15 PMID: 15096039
  66. A photocleavable and mass spectrometry identifiable cross-linker for protein interaction studies.
    Anal Chem. 2010 May 1;82(9):3556-66 PMID: 20373789
  67. Cleavable cross-linker for protein structure analysis: reliable identification of cross-linking products by tandem MS.
    Anal Chem. 2010 Aug 15;82(16):6958-68 PMID: 20704385
Article Info
Journal
Proteomics
Abbr.
Proteomics
ISSN
1615-9861
Published
2012-05-00
Pages
1565-75
Language
English
Region
Germany
NLM ID
101092707
PMCID
PMC3654877
Subset
IM
Grants
NIGMS NIH HHS · R01 GM097112 · United States
NIGMS NIH HHS · 1R01GM097112 · United States
NHLBI NIH HHS · R01 HL110879 · United States
NIGMS NIH HHS · R01 GM086688 · United States
NHLBI NIH HHS · 1R01HL110879 · United States
NCRR NIH HHS · R01 RR023334 · United States
NIGMS NIH HHS · 5R01GM086688 · United States
NCRR NIH HHS · 5R01RR023334 · United States
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