Single-cell in situ imaging of palmitoylation in fatty-acylated proteins

Nature Protocols

Volumn 9, Issue 11, 2014, Pages 2607-2623

  Gao, Xinxin ^a   Hannoush, Rami N ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; H RAS PROTEIN; PALMITIC ACID; RAS PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; PROTEIN; WNT3A PROTEIN;

ARTICLE; CLICK CHEMISTRY; CLINICAL PROTOCOL; FLUORESCENCE MICROSCOPY; HEK293 CELL LINE; MOLECULAR IMAGING; MOUSE; NONHUMAN; PALMITOYLATION; PROCESS DEVELOPMENT; PROCESS OPTIMIZATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; STRUCTURE ANALYSIS; ACYLATION; CHEMISTRY; HELA CELL LINE; HUMAN; LIPOYLATION; METABOLISM; PROCEDURES; SINGLE CELL ANALYSIS;

ACYLATION; CLICK CHEMISTRY; HEDGEHOG PROTEINS; HELA CELLS; HUMANS; LIPOYLATION; MICROSCOPY, FLUORESCENCE; MOLECULAR IMAGING; PALMITIC ACID; PROTEINS; SINGLE-CELL ANALYSIS; WNT3A PROTEIN;

EID: 84908214921     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2014.179     Document Type: Article

References (49)

1. Hannoush, R.N. & Sun, J. The chemical toolbox for monitoring protein fatty acylation and prenylation. Nat. Chem. Biol. 6, 498-506 (2010).
2. Salaun, C., Greaves, J. & Chamberlain, L.H. The intracellular dynamic of protein palmitoylation. J. Cell Biol. 191, 1229-1238 (2010).
3. Eisenberg, S. et al. The role of palmitoylation in regulating Ras localization and function. Biochem. Soc. Trans. 41, 79-83 (2013).
4. Linder, M.E. & Deschenes, R.J. Palmitoylation: policing protein stability and traffic. Nat. Rev. Mol. Cell Biol. 8, 74-84 (2007).
5. Pepinsky, R.B. et al. Identification of a palmitic acid-modified form of human Sonic Hedgehog. J. Biol. Chem. 273, 14037-14045 (1998).
6. Porter, J.A., Young, K.E. & Beachy, P.A. Cholesterol modification of Hedgehog signaling proteins in animal development. Science 274, 255-259 (1996).
7. Takada, R. et al. Monounsaturated fatty acid modification of Wnt protein: its role in Wnt secretion. Dev. Cell 11, 791-801 (2006).
8. Gao, X. & Hannoush, R.N. Single-cell imaging of Wnt palmitoylation by the acyltransferase porcupine. Nat. Chem. Biol. 10, 61-68 (2014).
9. Peseckis, S.M., Deichaite, I. & Resh, M.D. Iodinated fatty acids as probes for myristate processing and function. Incorporation into pp60v-src. J. Biol. Chem. 268, 5107-5114 (1993).
10. Schlesinger, M.J., Magee, A.I. & Schmidt, M.F. Fatty acid acylation of proteins in cultured cells. J. Biol. Chem. 255, 10021-10024 (1980).
11. Gao, X. & Hannoush, R.N. Method for cellular imaging of palmitoylated proteins with clickable probes and proximity ligation applied to Hedgehog, tubulin and Ras. J. Am. Chem. Soc. 136, 4544-4550 (2014).
12. Hannoush, R.N. & Arenas-Ramirez, N. Imaging the lipidome: ω-alkynyl fatty acids for detection and cellular visualization of lipid-modified proteins. ACS Chem. Biol. 4, 581-587 (2009).
13. Fredriksson, S. et al. Protein detection using proximity-dependent DNA ligation assays. Nat. Biotechnol. 20, 473-477 (2002).
14. Gullberg, M. et al. Cytokine detection by antibody-based proximity ligation. Proc. Natl. Acad. Sci. USA 101, 8420-8424 (2004).
15. Soderberg, O. et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000 (2006).
16. Gao, X., Arenas-Ramirez, N., Scales, S.J. & Hannoush, R.N. Membrane targeting of palmitoylated Wnt and Hedgehog revealed by chemical probes. FEBS Lett. 585, 2501-2506 (2011).
17. Charron, G. et al. Robust fluorescent detection of protein fatty-acylation with chemical reporters. J. Am. Chem. Soc. 131, 4967-4975 (2009).
18. Martin, B.R. & Cravatt, B.F. Large-scale profiling of protein palmitoylation in mammalian cells. Nat. Methods 6, 135-138 (2009).
19. Yap, M.C. et al. Rapid and selective detection of fatty acylated proteins using omega-alkynyl-fatty acids and click chemistry. J. Lipid Res. 51, 1566-1580 (2010).
20. Hannoush, R.N. Development of chemical probes for biochemical detection and cellular imaging of myristoylated and palmitoylated proteins. Curr. Protoc. Chem. Biol. 3, 15-26 (2011).
21. Hannoush, R.N. Profiling cellular myristoylation and palmitoylation using omega-alkynyl fatty acids. Methods Mol. Biol. 800, 85-94 (2012).
22. Wang, Q. et al. Bioconjugation by copper(I)-catalyzed azide-alkyne [3 + 2] cycloaddition. J. Am. Chem. Soc. 125, 3192-3193 (2003).
23. Vocadlo, D.J., Hang, H.C., Kim, E.J., Hanover, J.A. & Bertozzi, C.R. A chemical approach for identifying O-GlcNAc-modified proteins in cells. Proc. Natl. Acad. Sci. USA 100, 9116-9121 (2003).
24. Zaro, B.W., Yang, Y.Y., Hang, H.C. & Pratt, M.R. Chemical reporters for fluorescent detection and identification of O-GlcNAc-modified proteins reveal glycosylation of the ubiquitin ligase NEDD4-1. Proc. Natl. Acad. Sci. USA 108, 8146-8151 (2011).
25. Clark, P.M. et al. Direct in-gel fluorescence detection and cellular imaging of O-GlcNAc-modified proteins. J. Am. Chem. Soc. 130, 11576-11577 (2008).
26. Golks, A., Tran, T.T., Goetschy, J.F. & Guerini, D. Requirement for O-linked N-acetylglucosaminyltransferase in lymphocytes activation. EMBO J. 26, 4368-4379 (2007).
27. Lamarre-Vincent, N. & Hsieh-Wilson, L.C. Dynamic glycosylation of the transcription factor CREB: a potential role in gene regulation. J. Am. Chem. Soc. 125, 6612-6613 (2003).
28. Ozcan, S., Andrali, S.S. & Cantrell, J.E. Modulation of transcription factor function by O-GlcNAc modification. Biochim. Biophys. Acta 1799, 353-364 (2010).
29. Yang, W.H. et al. Modification of p53 with O-linked N-acetylglucosamine regulates p53 activity and stability. Nat. Cell Biol. 8, 1074-1083 (2006).
30. Heal, W.P. et al. Bioorthogonal chemical tagging of protein cholesterylation in living cells. Chem. Commun. (Camb) 47, 4081-4083 (2011).
31. Bothwell, I.R. et al. Se-adenosyl-l-selenomethionine cofactor analogue as a reporter of protein methylation. J. Am. Chem. Soc. 134, 14905-14912 (2012).
32. Willnow, S., Martin, M., Luscher, B. & Weinhold, E. A selenium-based click AdoMet analogue for versatile substrate labeling with wild-type protein methyltransferases. Chembiochem 13, 1167-1173 (2012).
33. Yang, Y.Y., Ascano, J.M. & Hang, H.C. Bioorthogonal chemical reporters for monitoring protein acetylation. J. Am. Chem. Soc. 132, 3640-3641 (2010).
34. Grammel, M., Luong, P., Orth, K. & Hang, H.C. A chemical reporter for protein AMPylation. J. Am. Chem. Soc. 133, 17103-17105 (2011).
35. Paulsen, C.E. et al. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat. Chem. Biol. 8, 57-64 (2012).
36. Schermelleh, L. et al. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320, 1332-1336 (2008).
37. Requejo-Isidro, J. Fluorescence nanoscopy. Methods and applications. J. Chem. Biol. 6, 97-120 (2013).
38. Koos, B. et al. Analysis of protein interactions in situ by proximity ligation assays. Curr. Top. Microbiol. Immunol. 377, 11-26 (2013).
39. Leuchowius, K.J., Weibrecht, I. & Soderberg, O. In situ proximity ligation assay for microscopy and flow cytometry. Curr. Protoc. Cytom. 56, 9361-93615 (2011).
40. Chen, B. et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 5, 100-107 (2009).
41. Petrova, E., Rios-Esteves, J., Ouerfelli, O., Glickman, J.F. & Resh, M.D. Inhibitors of Hedgehog acyltransferase block Sonic Hedgehog signaling. Nat. Chem. Biol. 9, 247-249 (2013).
42. Proffitt, K.D. et al. Pharmacological inhibition of the Wnt acyltransferase PORCN prevents growth of WNT-driven mammary cancer. Cancer Res. 73, 502-507 (2013).
43. Liu, J. et al. Targeting Wnt-driven cancer through the inhibition of Porcupine by LGK974. Proc. Natl. Acad. Sci. USA 110, 20224-20229 (2013).
44. Zheng, B. et al. 2-Bromopalmitate analogues as activity-based probes to explore palmitoyl acyltransferases. J. Am. Chem. Soc. 135, 7082-7085 (2013).
45. Jennings, B.C. et al. 2-Bromopalmitate and 2-(2-hydroxy-5-nitro-benzylidene)-benzo[b]thiophen-3-one inhibit DHHC-mediated palmitoylation in vitro. J. Lipid Res. 50, 233-242 (2009).
46. Ducker, C.E. et al. Discovery and characterization of inhibitors of human palmitoyl acyltransferases. Mol. Cancer Ther. 5, 1647-1659 (2006).
47. Lawrence, D.S., Zilfou, J.T. & Smith, C.D. Structure-activity studies of cerulenin analogues as protein palmitoylation inhibitors. J. Med. Chem. 42, 4932-4941 (1999).
48. Draper, J.M. & Smith, C.D. Palmitoyl acyltransferase assays and inhibitors (Review). Mol. Membr. Biol. 26, 5-13 (2009).
49. Patterson, S.I. & Skene, J.H. Inhibition of dynamic protein palmitoylation in intact cells with tunicamycin. Methods Enzymol. 250, 284-300 (1995).