Formaldehyde crosslinking: A tool for the study of chromatin complexes

Journal of Biological Chemistry

Volumn 290, Issue 44, 2015, Pages 26404-26411

  Hoffman, Elizabeth A ^a   Frey, Brian L ^b   Smith, Lloyd M ^b   Auble, David T ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ANALYSIS; CROSSLINKING; FORMALDEHYDE; PROTEINS;

CHROMATIN FIBERS; CHROMATIN PROTEINS; CHROMATIN STRUCTURE; DETECTION AND QUANTIFICATIONS; FORMALDEHYDE CROSS-LINKING; PROTEIN-DNA INTERACTIONS;

CHROMOSOMES;

FORMALDEHYDE; CHROMATIN; CROSS LINKING REAGENT;

BINDING KINETICS; CELL ASSAY; CELL FUNCTION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; COMPLEX FORMATION; CROSS LINKING; DNA PROTEIN COMPLEX; HUMAN; MOLECULAR DYNAMICS; MOLECULAR STABILITY; PRIORITY JOURNAL; REACTION TIME; REVIEW; STRUCTURE ANALYSIS; ANIMAL; CHEMISTRY; METABOLISM; STRUCTURE ACTIVITY RELATION;

ANIMALS; CHROMATIN; CROSS-LINKING REAGENTS; FORMALDEHYDE; HUMANS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84945946175     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R115.651679     Document Type: Review

References (98)

1. Eckels, K. H., and Putnak, R. (2003) Formalin-inactivated whole virus and recombinant subunit flavivirus vaccines. Adv. Virus Res. 61, 395-418
2. Nencioni, L., Volpini, G., Peppoloni, S., Bugnoli, M., De Magistris, T., Marsili, I., and Rappuoli, R. (1991) Properties of pertussis toxin mutant PT-9K/129G after formaldehyde treatment. Infect. Immun. 59, 625-630
3. Werner, M., Chott, A., Fabiano, A., and Battifora, H. (2000) Effect of formalin tissue fixation and processing on immunohistochemistry. Am. J. Surg. Pathol. 24, 1016-1019
4. Gavrilov, A., and Razin., S. V., and Cavalli, G. (2015) In vivo formaldehyde cross-linking: it is time for black box analysis. Brief. Funct. Genomics 14, 163-165
5. Fraenkel-Conrat, H., Cooper, M., and Olcott, H. S. (1945) The reaction of formaldehyde with proteins. J. Am. Chem. Soc. 67, 950-954
6. Fraenkel-Conrat, H., and Olcott, H. S. (1948) The reaction of formaldehyde with proteins. V. Cross-linking between amino and primary amide or guanidyl groups. J. Am. Chem. Soc. 70, 2673-2684
7. Fraenkel-Conrat, H., and Olcott, H. S. (1948) Reaction of formaldehyde with proteins. VI. Cross-linking of amino groups with phenol, imidazole, or indole groups. J. Biol. Chem. 174, 827-843
8. French, D., and Edsall, J. T. (1945) The reactions of formaldehyde with amino acids and proteins. Adv. Protein Chem. 2, 277-335
9. Sutherland, B. W., Toews, J., and Kast, J. (2008) Utility of formaldehyde cross-linking and mass spectrometry in the study of protein-protein interactions. J. Mass Spectrom. 43, 699-715
10. Metz, B., Kersten, G. F. A., Hoogerhout, P., Brugghe, H. F., Timmermans, H. A. M., de Jong, A., Meiring, H., ten Hove, J., Hennink, W. E., Crommelin, D. J. A., and Jiskoot, W. (2004) Identification of formaldehyde-induced modifications in proteins: reactions with model peptides. J. Biol. Chem. 279, 6235-6243
11. McGhee, J. D., and von Hippel, P. H. (1975) Formaldehyde as a probe of DNA Structure. I. Reaction with exocyclic amino groups of DNA Bases. Biochemistry 14, 1281-1296
12. McGhee, J. D., and von Hippel, P. H. (1975) Formaldehyde as a probe of DNA structure. II. Reaction with endocyclic imino groups of DNA bases. Biochemistry 14, 1297-1303
13. Feldman, M. Y. (1973) Reactions of nucleic acids and nucleoproteins with formaldehyde. Prog. Nucleic Acid Res. Mol. Biol. 13, 1-49
14. Solomon, M.J., and Varshavsky, A. (1985) Formaldehyde-mediated DNAprotein crosslinking: a probe for in vivo chromatin structures. Proc. Natl. Acad. Sci. U.S.A. 82, 6470-6474
15. Quievryn, G., and Zhitkovich, A. (2000) Loss of DNA-protein crosslinks from formaldehyde-exposed cells occurs through spontaneous hydrolysis and an active repair process linked to proteosome function. Carcinogenesis 21, 1573-1580
16. Hahnenstein, I., Albert, M., Hasse, H., Kreiter, C. G., and Maurer, G. (1995) NMR spectroscopic and densimetric study of reaction kinetics of formaldehyde polymer formation in water, deuterium oxide, and methanol. Ind. Eng. Chem. Res. 34, 440-450
17. Toews, J., Rogalski, J. C, Clark, T.J., and Kast, J. (2008) Mass spectrometric identification of formaldehyde-induced peptide modifications under in vivo protein cross-linking conditions. Anal. Chim. Acta 618, 168-183
18. Klockenbusch, C, O'Hara, J. E., and Kast, J. (2012) Advancing formaldehyde cross-linking toward quantitative proteomic applications. Anal. Bioanal. Chem. 404, 1057-1067
19. Means, G. E., and Feeney, R. E. (1995) Reductive alkylation of proteins. Anal. Biochem. 224, 1-16
20. Toews, J., Rogalski, J. C, and Kast, J. (2010) Accessibility governs the relative reactivity of basic residues in formaldehyde-induced protein modifications. Anal. Chim. Acta 676, 60-67
21. Jackson, V. (1978) Studies on histone organization in the nucleosome using formaldehyde as a reversible cross-linking agent. Cell 15, 945-954
22. Rohs, R., Jin, X., West, S. M., Joshi, R., Honig, B., and Mann, R. S. (2010) Origins of specificity in protein-DNA recognition. Ann. Rev. Biochem. 79, 233-269
23. Vani, K., and Bogen., S. A., and Sompuram, S. R. (2006) A high throughput combinatorial library technique for identifying formalin-sensitive epitopes. J. Immunol. Methods 317, 80-89
24. Klockenbusch, C, and Kast, J. (2010) Optimization of formaldehyde cross-linking for protein interaction analysis on non-tagged integrin β1. J. Biomed. Biotechnol. 2010, 927585
25. Vasilescu, J., Guo, X., and Kast, J. (2004) Identification of protein-protein interactions using in vivo cross-linking and mass spectrometry. Proteomics 4, 3845-3854
26. Schmiedeberg, L., Skene, P., Deaton, A., and Bird, A. (2009) A temporal threshold for formaldehyde crosslinking and fixation. PLoS ONE 4, e4636
27. Fraenkel-Conrat, H. (1954) Reaction of nucleic acid with formaldehyde. Biochim. Biophys. Acta 15, 307-309
28. Haselkorn, R., and Doty, P. (1961) The reaction of formaldehyde with polynucleotides. J. Biol. Chem. 236, 2738-2745
29. Chang, Y.-T., and Loew, G. H. (1994) Reaction mechanisms of formaldehyde with endocyclic imino groups of nucleic acid bases. J. Am. Chem. Soc. 116, 3548-3555
30. Utiyama, H., and Doty, P. (1971) Kinetic studies of denaturation and reaction with formaldehyde on polydeoxyribonucleotides. Biochemistry 10, 1254-1264
31. Von Hippel, P. H., and Wong, K.-Y. (1971) Dynamic aspects of native DNA structure: Kinetics of the formaldehyde reaction with calf thymus DNA. J. Mol. Biol. 61, 587-613
32. Shikama, K., and Miura, K.-I. (1976) Equilibrium studies on the formaldehyde reaction with native DNA. Eur. J. Biochem. 63, 39-46
33. McGhee, J. D., and von Hippel, P. H. (1977) Formaldehyde as a probe of DNA structure. 3. Equilibrium denaturation of DNA and synthetic polynucleotides. Biochemistry 16, 3267-3276
34. McGhee, J. D., and von Hippel, P. H. (1977) Formaldehyde as a probe of DNA structure. 4. Mechanism of the initial reaction of formaldehyde with DNA. Biochemistry 16, 3276-3293
35. Gavrilov, A., and Razin, S. V. (2009) Formaldehyde fixation of cells does not greatly reduce the ability to amplify cellular DNA. Anal. Biochem. 390, 94-96
36. Wu, C.-H, Chen, S., Shortreed, M. R., Kreitinger, G. M., Yuan, Y., Frey B. L., Zhang, Y., Mirza, S., Cirillo, L. A., Olivier, M., and Smith, L. M. (2011) Sequence-specific capture of protein-DNA complexes for mass spectrometric protein identification. PLoS ONE 6, e26217
37. Yin, Y., Yang, L., Zheng, G., Gu, C, Yi, C, He, C, and Gao., Y. Q., and Zhao, X. S. (2014) Dynamics of spontaneous flipping of a mismatched base in DNA duplex. Proc. Natl. Acad. Sci. U.S.A. 111, 8043-8048
38. Brutlag, D., Schlehuber, C, and Bonner, J. (1969) Properties of formaldehyde-treated nucleohistone. Biochemistry 8, 3214-3218
39. Gilmour, D. S., and Lis, J. T. (1985) In vivo interactions of RNA polymerase II with genes of Drosophila melanogaster. Mol. Cell. Biol. 5, 2009-2018
40. Solomon, M.J., Larsen, P.L., and Varshavsky, A. (1988) Mapping protein-DNA interactions in vivo with formaldehyde: evidence that histone H4 is retained on a highly transcribed gene. Cell 53, 937-947
41. Collas, P. (2010) The current state of chromatin immunoprecipitation. Mol. Biotechnol. 45, 87-100
42. Aparicio, O. M., and Geisberg., J. V., Sekinger, E. A., Yang, A. S., Moqtaderi, Z., and Struhl, K. (2005) Chromatin immunoprecipitation for determining the association of proteins with specific genomic sequences in vivo. Curr. Protoc. Mol. Biol. Chapter 21, Unit 21.3, 10.1002/0471142727.mb2103s69
43. O'Neill, L. P., and Turner, B. M. (1996) Immunoprecipitation of chromatin. Methods Enzymol. 274, 189-197
44. Kuo, M. H., and Allis, C. D. (1999) In vivo cross-linking and immunoprecipitation for studying dynamic protein: DNA associations in a chromatin environment. Methods 19, 425-433
45. Park, P.J. (2009) ChIP-seq: advantages and challenges of a maturing technology. Nat Rev. Genetics 10, 669-680
46. Kim, T. H., and Ren, B. (2006) Genome-wide analysis of protein-DNA Interactions. Annu. Rev. Genomics Hum. Genet. 7, 81-102
47. Rhee, H. S., and Pugh, B. F. (2012) ChIP-exo method for identifying genomic location of DNA-binding proteins with near-single-nucleotide accuracy. Curr. Protoc. Mol. Biol. Chapter 21, Unit 21.24, 10.1002/0471142727.mb2124s100
48. Schmidt, D., and Wilson., M. D., Spyrou, C, and Brown., G. D., Hadfield, J., and Odom, D. T. (2009) ChIP-seq: using high-throughput sequencing to discover protein-DNA interactions. Methods 48, 240-248
49. Komashko, V. M., and Acevedo., L. G., Squazzo, S. L., Iyengar, S. S., Rabinovich, A., O'Geen, H., Green, R., and Farnham, P. J. (2008) Using ChIP-chip technology to reveal common principles of transcriptional repression in normal and cancer cells. Genome Res. 18, 521-532
50. Kasinathan, S., and Orsi., G. A., Zentner, G. E., Ahmad, K., and Henikoff, S. (2014) High-resolution mapping of transcription factor binding sites on native chromatin. Nat Methods 11, 203-209
51. Lu, K., Ye, W., Zhou, L., Collins, L. B., Chen, X., Gold, A., Ball, L. M., and Swenberg, J. A. (2010) Structural characterization of formaldehyde-induced cross-links between amino acids and deoxynucleosides and their oligomers. J. Am. Chem. Soc. 132, 3388-3399
52. Siomin, Y. A., and Simonov., V. V., and Poverenny, A. M. (1973) The reaction of formaldehyde with deoxynucleotides and DNA in the presence of amino acids and lysine-rich histone. Biochim. Biophys. Acta 331, 27-32
53. Jencks, W. P. (1997) From chemistry to biochemistry to catalysis to movement. Annu. Rev. Biochem. 66, 1-18
54. Zeng, P.-Y., Vakoc, C. R., Chen, Z.-C, Blobel, G.A., and Berger, S.L. (2006) In vivo dual cross-linking for identification of indirect DNA-associated proteins by chromatin immunoprecipitation. BioTechniques 41, 694-698
55. Nowak, D. E., Tian, B., and Brasier, A. R. (2005) Two-step cross-linking method for identification of NF-κB gene network by chromatin immunoprecipitation. BioTechniques 39, 715-725
56. Harbison, C. T., and Gordon., D. B., Lee, T. I., Rinaldi, N. J., and Macisaac., K. D., Danford, T. W., Hannett, N. M., Tagne, J.-B., and Reynolds., D. B., Yoo, J., Jennings, E. G., Zeitlinger, J., and Pokholok., D. K., Kellis, M., Rolfe, P. A., and Takusagawa., K. T., Lander, E. S., Gifford, D. K., Fraenkel, E., and Young, R. A. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431, 99-104
57. Venters, B. J., Wachi, S., Mavrich, T. N, Andersen, B. E., Jena, P., and Sinnamon., A. J., Jain, P., Rolleri, N. S., Jiang, C, Hemeryck-Walsh, C, and Pugh, B. F. (2011) A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol. Cell 41, 480-492
58. Ren, B., Robert, F., Wyrick, J. J., Aparicio, O., and Jennings., E. G., Simon, I., Zeitlinger, J., Schreiber, J., Hannett, N, Kanin, E., Volkert, T. L., and Wilson., C. J., Bell, S. P., and Young, R. A. (2000) Genome-wide location and function of DNA binding proteins. Science 290, 2306-2309
59. Hammar, P., Leroy, P., Mahmutovic, A., Marklund, E. G., and Berg., O. G., and Elf, J. (2012) The lac repressor displays facilitated diffusion in living cells. Science 336, 1595-1598
60. Elf, J., and Li., G. W., and Xie, X. S. (2007) Probing transcription factor dynamics at the single-molecule level in a living cell. Science 316, 1191-1194
61. Hager, G. L., and McNally., J. G., and Misteli, T. (2009) Transcription dynamics. Mol. Cell 35, 741-753
62. Mirny, L., Slutsky, M., Wunderlich, Z., Tafvizi, A., Leith, J., and Kosmrlj, A. (2009) How a protein searches for its site on DNA: the mechanism of facilitated diffusion. J. Phys. A: Math. Theor. 42, 434013
63. Hall, D. B., and Struhl, K. (2002) The VP16 activation domain interacts with multiple transcriptional components as determined by protein-protein crosslinking in vivo. J. Biol. Chem. 277, 46043-46050
64. Buck, M. J., and Lieb, J. D. (2004) ChIP-chip: Considerations for the design, analysis, and application of genome-wide chromatin immunoprecipitation experiments. Genomics 83, 349-360
65. Struhl, K. (2007) Interpreting chromatin immunoprecipitation experiments. in Evaluating Techniques in Biochemical Research (Zuk, D., ed.) pp. 29-33, Cell Press, Cambridge, MA
66. Mazza, D., Mueller, F., Stasevich, T. J., and McNally, J. G. (2013) Convergence of chromatin binding estimates in live cells. Nat. Methods 10, 691-692
67. Chen, J., Zhang, Z., Li, L., Chen, B.-C., Revyakin, A., Hajj, B., Legant, W., Dahan, M., Lionnet, T., Betzig, E., Tjian, R., and Liu, Z. (2014) Singlemolecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156, 1274-1285
68. Stasevich, T. J., Hayashi-Takanaka, Y., Sato, Y., Maehara, K., Ohkawa, Y., Sakata-Sogawa, K., Tokunaga, M., Nagase, T., Nozaki, N., McNally, J. G., and Kimura, H. (2014) Regulation of RNA polymerase II activation by histone acetylation in single living cells. Nature 516, 272-275
69. Voss, T. C., and Hager, G. L. (2008) Visualizing chromatin dynamics in intact cells. Biochim. Biophys. Acta 1783, 2044-2051
70. Toth, J., and Biggin, M. D. (2000) The specificity of protein-DNA cross-linking by formaldehyde: in vitro and in Drosophila embryos. Nucleic Acids Res. 28, e4
71. Kaplan, T., Li, X.-Y., and Sabo., P. J., Thomas, S., Stamatoyannopoulos, J. A., and Biggin., M. D., and Eisen, M. B. (2011) Quantitative models of the mechanisms that control genome-wide patterns of transcription factor binding during early Drosophila development. PLoS Genet. 7, e1001290
72. Guerrero, C., Tagwerker, C., Kaiser, P., and Huang, L. (2006) An integrated mass spectrometry-based proteomic approach: quantitative analysis of tandem affinity-purified in vivo cross-linked protein complexes (qtax) to decipher the 26s proteasome-interacting network. Mol. Cell. Proteomics 5, 366-378
73. Tagwerker, C., Flick, K., Cui, M., Guerrero, C., Dou, Y., Auer, B., Baldi, P., Huang, L., and Kaiser, P. (2006) A tandem affinity tag for two-step purification under fully denaturing conditions: applicationinubiquitin profiling and protein complex identification combined with in vivo cross-Linking. Mol. Cell. Proteomics 5, 737-748
74. Schmitt-Ulms, G., Hansen, K., Liu, J., Cowdrey, C., Yang, J., and DeArmond., S. J., Cohen, F. E., Prusiner, S. B., and Baldwin, M. A. (2004) Time-controlled transcardiac perfusion cross-linking for the study of protein interactions in complex tissues. Nat. Biotechnol. 22, 724-731
75. Déjardin, J., and Kingston, R. E. (2009) Purification of proteins associated with specific genomic loci. Cell 136, 175-186
76. Kennedy-Darling, J., Guillen-Ahlers, H., Shortreed, M. R., Scalf, M., and Frey., B. L., Kendziorski, C., Olivier, M., Gasch, A. P., and Smith, L. M. (2014) Discovery of chromatin-associated proteins via sequence-specific capture and mass spectrometric protein identification in Saccharomyces cerevisiae. J. Proteome Res. 13, 3810-3825
77. Antão, J. M., Mason, J. M., Déjardin, J., and Kingston, R. E. (2012) Protein landscape at Drosophila melanogaster telomere-associated sequence repeats. Mol. Cell. Biol. 32, 2170-2182
78. Byrum, S. D., Raman, A., Taverna, S. D., and Tackett, A. J. (2012) ChAPMS: a method for identification of proteins and histone posttranslational modifications at a single genomic locus. Cell Rep. 2, 198-205
79. Byrum, S. D., and Taverna., S. D., and Tackett, A. J. (2013) Purification of a specific native genomic locus for proteomic analysis. Nucleic Acids Res. 41, e195
80. Byrum, S. D., and Taverna., S. D., and Tackett, A. J. (2015) Purification of specific chromatin loci for proteomic analysis. Methods Mol. Biol. 1228, 83-92
81. Dedon, P. C., and Soults., J. A., Allis, C. D., and Gorovsky, M. A. (1991) Formaldehyde cross-linking and immunoprecipitation demonstrate developmental changes in H1 association with transcriptionally active genes. Mol. Cell. Biol. 11, 1729-1733
82. Katan-Khaykovich, Y., and Struhl, K. (2002) Dynamics of global histone acetylation and deacetylation in vivo: rapid restoration of normal histone acetylation status upon removal of activators and repressors. Genes Dev. 16, 743-752
83. Poorey, K., Viswanathan, R., Carver, M. N., and Karpova., T. S., Cirimotich, S. M., McNally, J. G., Bekiranov, S., and Auble, D. T. (2013) Measuring chromatin interaction dynamics on the second time scale at single-copy genes. Science 342, 369-372
84. Shi, S.-R., Taylor, C. R., and Fowler., C. B., and Mason, J. T. (2013) Complete solubilization of formalin-fixed, paraffin-embedded tissue may improve proteomic studies. Proteomics Clin. Appl. 7, 264-272
85. Wisńiewski, J. R., Dus̈, K., and Mann, M. (2013) Proteomic workflow for analysis of archival formalin-fixed and paraffin-embedded clinical samples to a depth of 10, 000 proteins. Proteomics Clin. Appl. 7, 225-233
86. Kennedy-Darling, J., and Smith, L. M. (2014) Measuring the formaldehyde protein-DNA cross-link reversal rate. Anal. Chem. 86, 5678-5681
87. de Wit, E., and de Laat, W. (2012) A decade of 3C technologies: insights into nuclear organization. Genes Dev. 26, 11-24
88. Splinter, E., Grosveld, F., and de Laat, W. (2004) 3C technology: analyzing the spatial organization of genomic loci in vivo. Methods Enzymol. 375, 493-507
89. Hagège, H., Klous, P., Braem, C., Splinter, E., Dekker, J., Cathala, G., de Laat, W., and Forné, T. (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat. Protoc. 2, 1722-1733
90. Miele, A., and Dekker, J. (2009) Mapping cis- and trans-chromatin interaction networks using chromosome conformation capture (3C). Methods Mol. Biol. 464, 105-121
91. Kawashima, Y., Kodera, Y., Singh, A., Matsumoto, M., and Matsumoto, H. (2014) Efficient extraction of proteins from formalin-fixed paraffin-embedded tissues requires higher concentration of tris(hydroxymethyl) aminomethane. Clin. Proteomics 11, 4
92. Viswanathan, R., and Hoffman., E. A., Shetty, S. J., Bekiranov, S., and Auble, D. T. (2014) Analysis of chromatin binding dynamics using the crosslinking kinetics (CLK) method. Methods 70, 97-107
93. Orlando, V. (2000) Mapping chromosomal proteins in vivo by formaldehyde-crosslinked-chromatin immunoprecipitation. Trends Biochem. Sci. 25, 99-104
94. Fan, X., Lamarre-Vincent, N., Wang, Q., and Struhl, K. (2008) Extensive chromatin fragmentation improves enrichment of protein binding sites in chromatin immunoprecipitation experiments. Nucleic Acids Res. 36, e125
95. Fan, X., and Struhl, K. (2009) Where does Mediator bind in vivo? PLoS ONE 4, e5029
96. Teytelman, L., and Thurtle., D. M., Rine, J., and van Oudenaarden, A. (2013) Highly expressed loci are vulnerable to misleading ChIP localization of multiple unrelated proteins. Proc. Natl. Acad. Sci. U.S.A. 110, 18602-18607
97. Nacheva, G. A., and Guschin., D. Y., Preobrazhenskaya, O. V., Karpov, V. L., and Ebralidse., K. K., and Mirzabekov, A. D. (1989) Change in the pattern of histone binding to DNA upon transcriptional activation. Cell 58, 27-36
98. Voit, E. O., Martens, H.A., and Omholt, S. W. (2015) 150 years of the mass action law. PLoS Comput. Biol. 11, e1004012