Photocrosslinking approaches to interactome mapping

Current Opinion in Chemical Biology

Volumn 17, Issue 1, 2013, Pages 90-101

  Pham, Nam D ^a   Parker, Randy B ^a   Kohler, Jennifer J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; CD22 ANTIGEN; CHAPERONE; GLYCINE; LIPOPOLYSACCHARIDE; MEDIATOR COMPLEX; MEMBRANE PROTEIN; PHENYLALANINE; RNA POLYMERASE II; TRANSCRIPTION FACTOR SNF;

CROSS LINKING; ELECTRON MICROSCOPY; GENETIC TRANSCRIPTION; HUMAN; IMMUNOBLOTTING; IMMUNOCOMPETENT CELL; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; NUCLEAR PORE; NUCLEOCYTOPLASMIC TRANSPORT; PHOTOCROSSLINKING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; REVIEW; TANDEM MASS SPECTROMETRY; TRANSCRIPTION INITIATION; ULTRAVIOLET RADIATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CROSS-LINKING REAGENTS; HUMANS; PHOTOCHEMICAL PROCESSES; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION MAPPING; PROTEINS; PROTEOMICS; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84875260407     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2012.10.034     Document Type: Review

References (72)

1. Stumpf M.P., Thorne T., de Silva E., Stewart R., An H.J., Lappe M., Wiuf C. Estimating the size of the human interactome. Proc Natl Acad Sci USA 2008, 105:6959-6964.
2. Venkatesan K., Rual J.F., Vazquez A., Stelzl U., Lemmens I., Hirozane-Kishikawa T., Hao T., Zenkner M., Xin X., Goh K.I., et al. An empirical framework for binary interactome mapping. Nat Methods 2009, 6:83-90.
3. Charbonnier S., Gallego O., Gavin A.C. The social network of a cell: recent advances in interactome mapping. Biotechnol Annu Rev 2008, 14:1-28.
4. Garner A.L., Janda K.D. Protein-protein interactions and cancer: targeting the central dogma. Curr Top Med Chem 2011, 11:258-280.
5. Tanaka Y., Bond M.R., Kohler J.J. Photocrosslinkers illuminate interactions in living cells. Mol Biosyst 2008, 4:473-480.
6. Gorostiza P., Isacoff E.Y. Optical switches for remote and noninvasive control of cell signaling. Science 2008, 322:395-399.
7. Sutherland B.W., Toews J., Kast J. Utility of formaldehyde cross-linking and mass spectrometry in the study of protein-protein interactions. J Mass Spectrom 2008, 43:699-715.
8. Suchanek M., Radzikowska A., Thiele C. Photo-leucine and photo-methionine allow identification of protein-protein interactions in living cells. Nat Methods 2005, 2:261-267.
9. Davis L., Chin J.W. Designer proteins: applications of genetic code expansion in cell biology. Nat Rev Mol Cell Biol 2012, 13:168-182.
10. Du J., Meledeo M.A., Wang Z., Khanna H.S., Paruchuri V.D.P., Yarema K.J. Metabolic glycoengineering: sialic acid and beyond. Glycobiology 2009, 19:1382-1401.
11. Han S., Collins B.E., Bengtson P., Paulson J.C. Homomultimeric complexes of CD22 in B cells revealed by protein-glycan cross-linking. Nat Chem Biol 2005, 1:93-97.
12. Luchansky S.J., Goon S., Bertozzi C.R. Expanding the diversity of unnatural cell-surface sialic acids. Chembiochem 2004, 5:371-374.
13. Tanaka Y., Kohler J.J. Photoactivatable crosslinking sugars for capturing glycoprotein interactions. J Am Chem Soc 2008, 130:3278-3279.
14. Yu S.H., Boyce M., Wands A.M., Bond M.R., Bertozzi C.R., Kohler J.J. Metabolic labeling enables selective photocrosslinking of O-GlcNAc-modified proteins to their binding partners. Proc Natl Acad Sci USA 2012, 109:4834-4839.
15. Yu S.H., Bond M.R., Whitman C.M., Kohler J.J. Metabolic labeling of glycoconjugates with photocrosslinking sugars. Methods Enzymol 2010, 478:541-562.
16. Bond M.R., Whitman C.M., Kohler J.J. Metabolically incorporated photocrosslinking sialic acid covalently captures a ganglioside-protein complex. Mol Biosyst 2010, 6:1796-1799.
17. Leitner A., Walzthoeni T., Kahraman A., Herzog F., Rinner O., Beck M., Aebersold R. Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics. Mol Cell Proteomics 2010, 9:1634-1649.
18. Robinette D., Neamati N., Tomer K.B., Borchers C.H. Photoaffinity labeling combined with mass spectrometric approaches as a tool for structural proteomics. Expert Rev Proteomics 2006, 3:399-408.
19. Lundgren D.H., Hwang S.-I., Wu L., Han D.K. Role of spectral counting in quantitative proteomics. Expert Rev Proteomics 2010, 7:39-53.
20. Mann M. Functional and quantitative proteomics using SILAC. Nat Rev Mol Cell Biol 2006, 7:952-958.
21. Crocker P.R., Paulson J.C., Varki A. Siglecs and their roles in the immune system. Nat Rev Immunol 2007, 7:255-266.
22. Ramya T.N., Weerapana E., Liao L., Zeng Y., Tateno H., Yates J.R., Cravatt B.F., Paulson J.C. In situ trans ligands of CD22 identified by glycan-protein photocross-linking-enabled proteomics. Mol Cell Proteomics 2010, 9:1339-1351.
23. Han S., Collins B.E., Bengtson P., Paulson J.C. Homomultimeric complexes of CD22 in B cells revealed by protein-glycan cross-linking. Nat Chem Biol 2005, 1:93-97.
24. Bond M.R., Zhang H., Vu P.D., Kohler J.J. Photocrosslinking of glycoconjugates using metabolically incorporated diazirine-containing sugars. Nat Protoc 2009, 4:1044-1063.
25. Mori H., Ito K. Different modes of SecY-SecA interactions revealed by site-directed in vivo photo-cross-linking. Proc Natl Acad Sci USA 2006, 103:16159-16164.
26. Tagami S., Sekine S., Kumarevel T., Hino N., Murayama Y., Kamegamori S., Yamamoto M., Sakamoto K., Yokoyama S. Crystal structure of bacterial RNA polymerase bound with a transcription inhibitor protein. Nature 2010, 468:978-982.
27. Mohibullah N., Hahn S. Site-specific cross-linking of TBP in vivo and in vitro reveals a direct functional interaction with the SAGA subunit Spt3. Genes Dev 2008, 22:2994-3006.
28. Chen H.-T., Warfield L., Hahn S. The positions of TFIIF and TFIIE in the RNA polymerase II transcription preinitiation complex. Nat Struct Mol Biol 2007, 14:696-703.
29. Wild T., Cramer P. Biogenesis of multisubunit RNA polymerases. Trends Biochem Sci 2012, 37:99-105.
30. Malik S., Roeder R.G. The metazoan mediator co-activator complex as an integrative hub for transcriptional regulation. Nat Rev Genet 2010, 11:761-772.
31. Soutourina J., Wydau S., Ambroise Y., Boschiero C., Werner M. Direct interaction of RNA polymerase II and mediator required for transcription in vivo. Science 2011, 331:1451-1454.
32. Davis J.A., Takagi Y., Kornberg R.D., Asturias F.A. Structure of the yeast RNA polymerase II holoenzyme: mediator conformation and polymerase interaction. Mol Cell 2002, 10:409-415.
33. Tardiff D.F., Abruzzi K.C., Rosbash M. Protein characterization of Saccharomyces cerevisiae RNA polymerase II after in vivo cross-linking. Proc Natl Acad Sci USA 2007, 104:19948-19953.
34. Freinkman E., Chng S.S., Kahne D. The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. Proc Natl Acad Sci USA 2011, 108:2486-2491.
35. Collins B.E., Paulson J.C. Cell surface biology mediated by low affinity multivalent protein-glycan interactions. Curr Opin Chem Biol 2004, 8:617-625.
36. Hulsmann B.B., Labokha A.A., Gorlich D. The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 2012, 150:738-751.
37. Hartl F.U., Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 2002, 295:1852-1858.
38. Khan S.H., Kumar R. An overview of the importance of conformational flexibility in gene regulation by the transcription factors. J Biophys 2009, 2009:210485.
39. Fuxreiter M., Tompa P., Simon I., Uversky V.N., Hansen J.C., Asturias F.J. Malleable machines take shape in eukaryotic transcriptional regulation. Nat Chem Biol 2008, 4:728-737.
40. Perkins J.R., Diboun I., Dessailly B.H., Lees J.G., Orengo C. Transient protein-protein interactions: structural, functional, and network properties. Structure 2010, 18:1233-1243.
41. Dyson H.J., Wright P.E. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 2005, 6:197-208.
42. Taylor M.E., Drickamer K. Structural insights into what glycan arrays tell us about how glycan-binding proteins interact with their ligands. Glycobiology 2009, 19:1155-1162.
43. Dunker A.K., Obradovic Z., Romero P., Garner E.C., Brown C.J. Intrinsic protein disorder in complete genomes. Genome Inform 2000, 11:161-171.
44. Essentials of Glycobiology 2009, Cold Spring Harbor Laboratory Press. A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, M.E. Etzler (Eds.).
45. Singh G.P., Ganapathi M., Dash D. Role of intrinsic disorder in transient interactions of hub proteins. Proteins 2007, 66:761-765.
46. Liu J., Perumal N.B., Oldfield C.J., Su E.W., Uversky V.N., Dunker A.K. Intrinsic disorder in transcription factors. Biochemistry 2006, 45:6873-6888.
47. Wu J.I., Lessard J., Crabtree G.R. Understanding the words of chromatin regulation. Cell 2009, 136:200-206.
48. Krishnamurthy M., Dugan A., Nwokoye A., Fung Y.H., Lancia J.K., Majmudar C.Y., Mapp A.K. Caught in the act: covalent cross-linking captures activator-coactivator interactions in vivo. ACS Chem Biol 2011, 6:1321-1326.
49. Hanover J.A., Cohen C.K., Willingham M.C., Park M.K. O-linked N-acetylglucosamine is attached to proteins of the nuclear pore. Evidence for cytoplasmic and nucleoplasmic glycoproteins. J Biol Chem 1987, 262:9887-9894.
50. Bukau B., Weissman J., Horwich A. Molecular chaperones and protein quality control. Cell 2006, 125:443-451.
51. Liu C., Young A.L., Starling-Windhof A., Bracher A., Saschenbrecker S., Rao B.V., Rao K.V., Berninghausen O., Mielke T., Hartl F.U., et al. Coupled chaperone action in folding and assembly of hexadecameric Rubisco. Nature 2010, 463:197-202.
52. Schlieker C., Weibezahn J., Patzelt H., Tessarz P., Strub C., Zeth K., Erbse A., Schneider-Mergener J., Chin J.W., Schultz P.G., et al. Substrate recognition by the AAA+ chaperone ClpB. Nat Struct Mol Biol 2004, 11:607-615.
53. Haslberger T., Weibezahn J., Zahn R., Lee S., Tsai F.T., Bukau B., Mogk A. M domains couple the ClpB threading motor with the DnaK chaperone activity. Mol Cell 2007, 25:247-260.
54. Lakshmipathy S.K., Tomic S., Kaiser C.M., Chang H.C., Genevaux P., Georgopoulos C., Barral J.M., Johnson A.E., Hartl F.U., Etchells S.A. Identification of nascent chain interaction sites on trigger factor. J Biol Chem 2007, 282:12186-12193.
55. Kaiser C.M., Chang H.C., Agashe V.R., Lakshmipathy S.K., Etchells S.A., Hayer-Hartl M., Hartl F.U., Barral J.M. Real-time observation of trigger factor function on translating ribosomes. Nature 2006, 444:455-460.
56. Zhang M., Lin S., Song X., Liu J., Fu Y., Ge X., Fu X., Chang Z., Chen P.R. A genetically incorporated crosslinker reveals chaperone cooperation in acid resistance. Nat Chem Biol 2011, 7:671-677.
57. Gajiwala K.S., Burley S.K. HDEA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J Mol Biol 2000, 295:605-612.
58. Muir T.W., Sondhi D., Cole P.A. Expressed protein ligation: a general method for protein engineering. Proc Natl Acad Sci USA 1998, 95:6705-6710.
59. Shah N.H., Vila-Perello M., Muir T.W. Kinetic control of one-pot trans-splicing reactions by using a wild-type and designed split intein. Angew Chem 2011, 50:6511-6515.
60. Fernandez-Suarez M., Baruah H., Martinez-Hernandez L., Xie K.T., Baskin J.M., Bertozzi C.R., Ting A.Y. Redirecting lipoic acid ligase for cell surface protein labeling with small-molecule probes. Nat Biotechnol 2007, 25:1483-1487.
61. Baruah H., Puthenveetil S., Choi Y.A., Shah S., Ting A.Y. An engineered aryl azide ligase for site-specific mapping of protein-protein interactions through photo-cross-linking. Angew Chem 2008, 47:7018-7021.
62. Tsukiji S., Miyagawa M., Takaoka Y., Tamura T., Hamachi I. Ligand-directed tosyl chemistry for protein labeling in vivo. Nat Chem Biol 2009, 5:341-343.
63. Tamura T., Tsukiji S., Hamachi I. Native FKBP12 engineering by ligand-directed tosyl chemistry: labeling properties and application to photo-cross-linking of protein complexes in vitro and in living cells. J Am Chem Soc 2012, 134:2216-2226.
64. Neumann H., Wang K., Davis L., Garcia-Alai M., Chin J.W. Encoding multiple unnatural amino acids via evolution of a quadruplet-decoding ribosome. Nature 2010, 464:441-444.
65. Whitman C.M., Yang F., Kohler J.J. Modified GM3 gangliosides produced by metabolic oligosaccharide engineering. Bioorg Med Chem Lett 2011, 21:5006-5010.
66. Fra A.M., Masserini M., Palestini P., Sonnino S., Simons K. A photo-reactive derivative of ganglioside GM1 specifically cross-links VIP21-caveolin on the cell surface. FEBS Lett 1995, 375:11-14.
67. Ono M., Handa K., Sonnino S., Withers D.A., Nagai H., Hakomori S. GM3 ganglioside inhibits CD9-facilitated haptotactic cell motility: coexpression of GM3 and CD9 is essential in the downregulation of tumor cell motility and malignancy. Biochemistry 2001, 40:6414-6421.
68. Wendeler M., Hoernschemeyer J., Hoffmann D., Kolter T., Schwarzmann G., Sandhoff K. Photoaffinity labelling of the human GM2-activator protein. Mechanistic insight into ganglioside GM2 degradation. Eur J Biochem 2004, 271:614-627.
69. Vodovozova E.L. Photoaffinity labeling and its application in structural biology. Biochemistry (Moscow) 2007, 72:1-20.
70. Haberkant P., van Meer G. Protein-lipid interactions: paprazzi hunting for snap-shots. Biol Chem 2009, 390:795-803.
71. Kayser H., Zeitler R., Kannicht C., Grunow D., Nuck R., Reutter W. Biosynthesis of a nonphysiological sialic-acid in different rat organs, using N-propanoyl-d-hexosamines as precursors. J Biol Chem 1992, 267:16934-16938.
72. Greiss S., Chin J.W. Expanding the genetic code of an animal. J Am Chem Soc 2011, 133:14196-14199.