Caught in the act: Covalent cross-linking captures activator-coactivator interactions in Vivo

ACS Chemical Biology

Volumn 6, Issue 12, 2011, Pages 1321-1326

  Krishnamurthy, Malathy ^a   Dugan, Amanda ^a   Nwokoye, Adaora ^a   Fung, Yik Hong ^a   Lancia, Jody K ^a   Majmudar, Chinmay Y ^a   Mapp, Anna K ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; AMTOLMETIN GUACIL; ETOPOSIDE; P BENZOYLPHENYLALANINE DERIVATIVE; PROTEIN; SNF2 PROTEIN; SWI/SNF RELATED MATRIX ASSOCIATED ACTIN DEPENDENT REGULATOR OF CHROMATIN SUBFAMILY B MEMBER 1; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG; 4 BENZOYLPHENYLALANINE; 4-BENZOYLPHENYLALANINE; BENZOPHENONE DERIVATIVE; CROSS LINKING REAGENT; DRUG DERIVATIVE; PHENYLALANINE; SACCHAROMYCES CEREVISIAE PROTEIN; SNF2 PROTEIN, S CEREVISIAE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BINDING AFFINITY; CHEMICAL INTERACTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; COVALENT BOND; CROSS LINKING; ENZYME ACTIVATION; EUKARYOTE; GENETIC CODE; IN VIVO STUDY; NONHUMAN; PHOTOACTIVATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION INITIATION; CHEMISTRY; LETTER; METABOLISM;

ADENOSINE TRIPHOSPHATASES; BENZOPHENONES; CROSS-LINKING REAGENTS; HERPES SIMPLEX VIRUS PROTEIN VMW65; PHENYLALANINE; PROTEIN INTERACTION MAPS; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84859702645     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb200308e     Document Type: Article

References (60)

1. Lee, L. W., and Mapp, A. K. (2010) Transcriptional switches: chemical approaches to gene regulation. J. Biol. Chem. 285, 11033- 11038.
2. Koehler, A. N. (2010) A complex task? Direct modulation of transcription factors with small molecules. Curr. Opin. Chem. Biol. 14, 331-340.
3. Arkin, M. R., and Whitty, A. (2009) The road less traveled: modulating signal transduction enzymes by inhibiting their proteinprotein interactions. Curr. Opin. Chem. Biol. 13, 284-290.
4. Evans, C. G., Chang, L., and Gestwicki, J. E. (2010) Heat shock protein 70 (hsp70) as an emerging drug target. J. Med. Chem. 53, 4585-4602.
5. Ong, D. S., and Kelly, J. W. (2011) Chemical and/or biological therapeutic strategies to ameliorate protein misfolding diseases. Curr. Opin. Cell Biol. 23, 231-238.
6. Berg, T. (2008) Inhibition of transcription factors with small organic molecules. Curr. Opin. Chem. Biol. 12, 464-471.
7. Arndt, H. D. (2006) Small molecule modulators of transcription. Angew. Chem., Int. Ed. 45, 4552-4560.
8. Blazer, L. L., and Neubig, R. R. (2009) Small molecule proteinprotein interaction inhibitors as CNS therapeutic agents: current progress and future hurdles. Neuropsychopharmacology 34, 126-141.
9. Berggard, T., Linse, S., and James, P. (2007) Methods for the detection and analysis of protein-protein interactions. Proteomics 7, 2833-2842.
10. Tanaka, Y., Bond, M. R., and Kohler, J. J. (2008) Photocrosslinkers illuminate interactions in living cells. Mol. Biosyst. 4, 473-480.
11. Melcher, K. (2004) New chemical crosslinking methods for the identification of transient protein-protein interactions with multiprotein complexes. Curr. Protein Pept. Sci. 5, 287-296.
12. Perkins, J. R., Diboun, I., Dessailly, B. H., Lees, J. G., and Orengo, C. (2010) Transient protein-protein interactions: structural, functional, and network properties. Structure 18, 1233-1243.
13. Wilson, B. G., and Roberts, C. W. (2011) SWI/SNF nucleosome remodellers and cancer. Nat. Rev. Cancer 11, 481-492.
14. Hang, C. T., Yang, J., Han, P., Cheng, H. L., Shang, C., Ashley, E., Zhou, B., and Chang, C. P. (2010) Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 466, 62-67.
15. Hargreaves, D. C., and Crabtree, G. R. (2011) ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21, 396-420.
16. Wands, A. M., Wang, N., Lum, J. K., Hsieh, J., Fierke, C. A., and Mapp, A. K. (2011) Transient-state kinetic analysis of transcriptional activator.DNA complexes interacting with a key coactivator. J. Biol. Chem. 286, 16238-16245.
17. Ferreira, M. E., Hermann, S., Prochasson, P., Workman, J. L., Berndt, K. D., and Wright, A. P. H. (2005) Mechanism of transcription factor recruitment by acidic activators. J. Biol. Chem. 280, 21779-21784.
18. Fuxreiter, M., Tompa, P., Simon, I., Uversky, V. N., Hansen, J. C., and Asturias, F. J. (2008) Malleable machines take shape in eukaryotic transcriptional regulation. Nat. Chem. Biol. 4, 728-737.
19. Mapp, A. K., and Ansari, A. Z. (2007) A TAD further: Exogenous control of gene activation. ACS Chem. Biol. 2, 62-75.
20. Herbig, E., Warfield, L., Fish, L., Fishburn, J., Knutson, B. a., Moorefield, B., Pacheco, D., and Hahn, S. (2010) Mechanism of Mediator recruitment by tandem Gcn4 activation domains and three Gal11 activator-binding domains. Mol. Cell. Biol. 30, 2376-2390.
21. Melcher, K. (2000) The strength of acidic activation domains correlates with their affinity for both transcriptional and non-Transcriptional proteins. J. Mol. Biol. 301, 1097-1112.
22. Majmudar, C. Y., Lee, L. W., Lancia, J. K., Nwokoye, A., Wang, Q., Wands, A. M., Wang, L., and Mapp, A. K. (2009) Impact of nonnatural amino acid mutagenesis on the in vivo function and binding modes of a transcriptional activator. J. Am. Chem. Soc. 131, 14240- 14242.
23. Ptashne, M., Gann, A. (2001) Genes & Signals, Cold Spring Harbor Laboratory, New York.
24. Bryant, G. O., and Ptashne, M. (2003) Independent recruitment in vivo by Gal4 of two complexes required for transcription. Mol. Cell 11, 1301-1309.
25. Cosma, M. P., Tanaka, T., and Nasmyth, K. (1999) Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle-And developmentally regulated promoter. Cell 97, 299-311.
26. Hall, D. B., and Struhl, K. (2002) The VP16 activation domain interacts with multiple transcriptional components as determined by protein-protein cross-linking in vivo. J. Biol. Chem. 277, 46043-46050.
27. Memedula, S., and Belmont, A. S. (2003) Sequential recruitment of HAT and SWI/SNF components to condensed chromatin by VP16. Curr. Biol. 13, 241-246.
28. Yudkovsky, N., Logie, C., Hahn, S., and Peterson, C. L. (1999) Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators. Genes Dev. 13, 2369-2374.
29. Herrera, F. J., and Triezenberg, S. J. (2004) VP16-dependent association of chromatin-modifying coactivators and underrepresentation of histones at immediate-early gene promoters during herpes simplex virus infection. J. Virol. 78, 9689-9696.
30. Hassan, A. H., Neely, K. E., and Workman, J. L. (2001) Histone acetyltransferase complexes stabilize SWI/SNF binding to promoter nucleosomes. Cell 104, 817-827.
31. Neely, K. E., Hassan, A. H., Wallberg, A. E., Steger, D. J., Cairns, B. R., Wright, A. P., and Workman, J. L. (1999) Activation domain-mediated targeting of the SWI/SNF complex to promoters stimulates transcription from nucleosome arrays. Mol. Cell 4, 649-655.
32. Dechassa, M. L., Zhang, B., Horowitz-Scherer, R., Persinger, J., Woodcock, C. L., Peterson, C. L., and Bartholomew, B. (2008) Architecture of the SWI/SNF-nucleosome complex. Mol. Cell. Biol. 28, 6010-6021.
33. Prochasson, P., Neely, K. E., Hassan, A. H., Li, B., and Workman, J. L. (2003) Targeting activity is required for SWI/SNF function in vivo and is accomplished through two partially redundant activatorinteraction domains. Mol. Cell 12, 983-990.
34. Neely, K. E., Hassan, A. H., Brown, C. E., Howe, L., and Workman, J. L. (2002) Transcription activator interactions with multiple SWI/SNF subunits. Mol. Cell. Biol. 22, 1615-1625.
35. Chin, J. W., and Schultz, P. G. (2002) In vivo photocrosslinking with unnatural amino acid mutagenesis. ChemBioChem 3, 1135-1137.
36. Mohibullah, N., and Hahn, S. (2008) Site-specific cross-linking of TBP in vivo and in vitro reveals a direct functional interaction with the SAGA subunit Spt3. Genes Dev. 22, 2994-3006.
37. Hino, N., Okazaki, Y., Kobayashi, T., and Hayashi, A. (2005) Protein photo-cross-linking in mammalian cells by site-specific incorporation of a photoreactive amino acid. Nat. Methods 2, 3-8.
38. Thoden, J. B., Ryan, L. A., Reece, R. J., and Holden, H. M. (2008) The interaction between an acidic transcriptional activator and its inhibitor. The molecular basis of Gal4p recognition by Gal80p. J. Biol. Chem. 283, 30266-30272.
39. Majmudar, C. Y., Wang, B., Lum, J. K., Hakansson, K., and Mapp, A. K. (2009) A high-resolution interaction map of three transcriptional activation domains with a key coactivator from photo-crosslinking and multiplexed mass spectrometry. Angew. Chem., Int. Ed. 48, 7021-7024.
40. Triezenberg, S. J., Kingsbury, R. C., and McKnight, S. L. (1988) Functional dissection of VP16, the trans-Activator of herpes simplex virus immediate early gene expression. Genes Dev. 2, 718-729.
41. Regier, J. L., Shen, F., and Triezenberg, S. J. (1993) Pattern of aromatic and hydrophobic amino acids critical for one of two subdomains of the VP16 transcriptional activator. Proc. Natl. Acad. Sci. U.S.A. 90, 883-887.
42. Consistent with other reports, expression of the full length VP16 TAD proved to be toxic in yeast. Therefore, we chose to use individual subdomains of the VP16 TAD which did not result in cell death.
43. Chin, J. W., Cropp, T. A., Anderson, J. C., Mukherji, M., Zhang, Z., and Schultz, P. G. (2003) An expanded eukaryotic genetic code. Science 301, 964-967.
44. Wang, Q., and Wang, L. (2008) New methods enabling efficient incorporation of unnatural amino acids in yeast. J. Am. Chem. Soc. 130, 6066-6067.
45. Cote, J., Quinn, J., Workman, J. L., and Peterson, C. L. (1994) Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265, 53-60.
46. Lemieux, K., and Gaudreau, L. (2004) Targeting of Swi/Snf to the yeast GAL1 UAS G requires the Mediator, TAF IIs, and RNA polymerase II. EMBO J. 23, 4040-4050.
47. Peterson, C. L., and Workman, J. L. (2000) Promoter targeting and chromatin remodeling by the SWI/SNF complex. Curr. Opin. Genet. Dev. 10, 187-192.
48. Jonker, H. R., Wechselberger, R. W., Boelens, R., Folkers, G. E., and Kaptein, R. (2005) Structural properties of the promiscuous VP16 activation domain. Biochemistry 44, 827-839.
49. Uesugi, M., Nyanguile, O., Lu, H., Levine, A. J., and Verdine, G. L. (1997) Induced alpha helix in the VP16 activation domain upon binding to a human TAF. Science 277, 1310-1313.
50. Yang, F., DeBeaumont, R., Zhou, S., and Naar, A. M. (2004) The activator-recruited cofactor/Mediator coactivator subunit ARC92 is a functionally important target of the VP16 transcriptional activator. Proc. Natl. Acad. Sci. U.S.A. 101, 2339-2344.
51. Although this hypothesis is supported by the lack of Snf2 crosslinking with three different VP16N Bpa mutants and by biochemical binding data from other laboratories, 34 an alternative hypothesis is that none of the VP16N Bpa mutants in our study are properly positioned for Bpa cross-linking with Snf2.
52. Sinz, A. (2010) Investigation of protein-protein interactions in living cells by chemical crosslinking and mass spectrometry. Anal. Bioanal. Chem. 8, 3433-3440.
53. Soutourina, J., Wydau, S., Ambroise, Y., Boschiero, C., and Werner, M. (2011) Direct interaction of RNA polymerase II and mediator required for transcription in vivo. Science 331, 1451-1454.
54. Laurent, B. C., Treich, I., and Carlson, M. (1993) The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for transcriptional activation. Genes Dev. 7, 583-591.
55. Ferreira, M. E., Prochasson, P., Berndt, K. D., Workman, J. L., and Wright, A. P. H. (2009) Activator-binding domains of the SWI/SNF chromatin remodeling complex characterized in vitro are required for its recruitment to promoters in vivo. FEBS J. 276, 2557-2565.
56. Schwabish, M. A., and Struhl, K. (2007) The Swi/Snf complex is important for histone eviction during transcriptional activation and RNA polymerase II elongation in vivo. Mol. Cell. Biol. 27, 6987-6995.
57. Bryant, G. O., Prabhu, V., Floer, M., Wang, X., Spagna, D., Schreiber, D., and Ptashne, M. (2008) Activator control of nucleosome occupancy in activation and repression of transcription. PLoS Biol. 6, 2928-2939.
58. Govind, C. K., Yoon, S., Qiu, H., Govind, S., and Hinnebusch, A. G. (2005) Simultaneous recruitment of coactivators by Gcn4p stimulates multiple steps of transcription in vivo. Mol. Cell. Biol. 25, 5626-5638.
59. Swanson, M. J., Qiu, H., Sumibcay, L., Krueger, A., Kim, S., Natarajan, K., Yoon, S., and Hinnebusch, A. G. (2003) A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo. Mol. Cell. Biol. 23, 2800-2820.
60. Reisman, D., Glaros, S., and Thompson, E. A. (2009) The SWI/SNF complex and cancer. Oncogene 28, 1653-1668.