Single-molecule superresolution imaging allows quantitative analysis of RAF multimer formation and signaling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 46, 2013, Pages 18519-18524

  Nan, Xiaolin ^a,b,e   Collisson, Eric A ^b,c   Lewis, Sophia ^b   Huang, Jing ^b   Tamgüney, Tanja M ^c   Liphardt, Jan T ^a   McCormick, Frank ^c   Gray, Joe W ^b,c,e   Chu, Steven ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d STANFORD UNIVERSITY   (United States)

^e Oregon Health and Science University Department of Biomedical Engineering   (United States)

Author keywords

Cancer signaling; Single molecule imaging; Superresolution optical microscopy

Indexed keywords

CYTOPLASM PROTEIN; DIMER; POLYMER; RAF PROTEIN; RAS PROTEIN; TETRAMER;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DIMERIZATION; IMAGING; INTRACELLULAR SIGNALING; MICROSCOPY; PHOTOACTIVATED LOCALIZATION MICROSCOPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MULTIMERIZATION; QUANTITATIVE ANALYSIS; SPATIAL ANALYSIS; STOICHIOMETRY;

CANCER SIGNALING; SINGLE MOLECULE IMAGING; SUPERRESOLUTION OPTICAL MICROSCOPY;

ANIMALS; CARCINOGENESIS; CELL LINE; CRICETINAE; ENZYME ACTIVATION; MICROSCOPY; MOLECULAR IMAGING; PROTEIN MULTIMERIZATION; RAF KINASES; RAS PROTEINS; SIGNAL TRANSDUCTION;

EID: 84887425345     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1318188110     Document Type: Article

References (39)

1. Wellbrock C, Karasarides M, Marais R (2004) The RAF proteins take centre stage. Nat Rev Mol Cell Biol 5(11):875-885. (Pubitemid 39486539)
2. Seger R, Krebs EG (1995) The MAPK signaling cascade. FASEB J 9(9):726-735.
3. Roberts PJ, Der CJ (2007) Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 26(22):3291-3310. (Pubitemid 46763022)
4. Schubbert S, Shannon K, Bollag G (2007) Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 7(4):295-308. (Pubitemid 46480970)
5. McCormick F (2007) Success and failure on the ras pathway. Cancer Biol Ther 6(10):1654-1659.
6. Su F, et al. (2012) RAS mutations in cutaneous squamous-cell carcinomas in patients treated with BRAF inhibitors. N Engl J Med 366(3):207-215.
7. Hansen JD, et al. (2008) Potent and selective pyrazole-based inhibitors of B-Raf kinase. Bioorg Med Chem Lett 18(16):4692-4695.
8. Tsai J, et al. (2008) Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc Natl Acad Sci USA 105(8):3041-3046. (Pubitemid 351723664)
9. Nazarian R, et al. (2010) Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 468(7326):973-977.
10. Oberholzer PA, et al. (2012) RAS mutations are associated with the development of cutaneous squamous cell tumors in patients treated with RAF inhibitors. J Clin Oncol 30(3):316-321.
11. Rajakulendran T, Sahmi M, Lefrançois M, Sicheri F, Therrien M (2009) A dimerization-dependent mechanism drives RAF catalytic activation. Nature 461(7263):542-545.
12. Hatzivassiliou G, et al. (2010) RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 464(7287):431-435.
13. Poulikakos PI, Zhang C, Bollag G, Shokat KM, Rosen N (2010) RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 464(7287):427-430.
14. Poulikakos PI, et al. (2011) RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 480(7377):387-390.
15. Weber CK, Slupsky JR, Kalmes HA, Rapp UR (2001) Active Ras induces heterodimerization of cRaf and BRaf. Cancer Res 61(9):3595-3598. (Pubitemid 32694968)
16. Rushworth LK, Hindley AD, O'Neill E, Kolch W (2006) Regulation and role of Raf-1/BRaf heterodimerization. Mol Cell Biol 26(6):2262-2272.
17. Farrar MA, Alberol-Ila J, Perlmutter RM (1996) Activation of the Raf-1 kinase cascade by coumermycin-induced dimerization. Nature 383(6596):178-181. (Pubitemid 26303982)
18. Luo Z, et al. (1996) Oligomerization activates c-Raf-1 through a Ras-dependent mechanism. Nature 383(6596):181-185. (Pubitemid 26303983)
19. Goetz CA, O' Neil JJ, Farrar MA (2003) Membrane localization, oligomerization, and phosphorylation are required for optimal raf activation. J Biol Chem 278(51):51184-51189. (Pubitemid 38020355)
20. Bollag G, et al. (2010) Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature 467(7315):596-599.
21. Betzig E, et al. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313(5793):1642-1645. (Pubitemid 44414039)
22. Hess ST, Girirajan TP, Mason MD (2006) Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91(11):4258-4272. (Pubitemid 44887284)
23. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3(10):793-795. (Pubitemid 44445825)
24. Subach FV, et al. (2009) Photoactivatable mCherry for high-resolution two-color fluorescence microscopy. Nat Methods 6(2):153-159.
25. Ha T, Tinnefeld P (2012) Photophysics of fluorescent probes for single-molecule biophysics and super-resolution imaging. Annu Rev Phys Chem 63(1):595-617.
26. Annibale P, Vanni S, Scarselli M, Rothlisberger U, Radenovic A (2011) Quantitative photo activated localization microscopy: Unraveling the effects of photoblinking. PLoS ONE 6(7):e22678.
27. Greenfield D, et al. (2009) Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol 7(6):e1000137.
28. Sengupta P, et al. (2011) Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nat Methods 8(11):969-975.
29. Renz M, Daniels BR, Vámosi G, Arias IM, Lippincott-Schwartz J (2012) Plasticity of the asialoglycoprotein receptor deciphered by ensemble FRET imaging and single-molecule counting PALM imaging. Proc Natl Acad Sci USA 109(44):E2989-E2997.
30. Ripley BD (1977) Modelling spatial patterns. J Royal Stat Soc B 39(2):172-212.
31. Ester M, Kriegel H-P, Jörg S, Xu X (1996) A density-based algorithm for discovering clusters in large spatial databases with noise. Proceedings of the 2nd International Conference on Knowledge Discovery and Data Mining (AAAI Press, Menlo Park, CA), pp 226-231.
32. Marais R, Light Y, Paterson HF, Marshall CJ (1995) Ras recruits Raf-1 to the plasma membrane for activation by tyrosine phosphorylation. EMBO J 14(13):3136-3145.
33. Murphy DA, Courtneidge SA (2011) The 'ins' and 'outs' of podosomes and invadopodia: Characteristics, formation and function. Natl Rev 12(7):413-426.
34. Stanton VP, Jr., Cooper GM (1987) Activation of human raf transforming genes by deletion of normal amino-terminal coding sequences. Mol Cell Biol 7(3):1171-1179.
35. Heidecker G, et al. (1990) Mutational activation of c-raf-1 and definition of the minimal transforming sequence. Mol Cell Biol 10(6):2503-2512.
36. Cutler RE, Jr., Stephens RM, Saracino MR, Morrison DK (1998) Autoregulation of the Raf-1 serine/threonine kinase. Proc Natl Acad Sci USA 95(16):9214-9219. (Pubitemid 28506211)
37. Plowman SJ, Muncke C, Parton RG, Hancock JF (2005) H-ras, K-ras, and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton. Proc Natl Acad Sci USA 102(43):15500-15505. (Pubitemid 41528086)
38. Leevers SJ, Paterson HF, Marshall CJ (1994) Requirement for Ras in Raf activation is overcome by targeting Raf to the plasma membrane. Nature 369(6479):411-414. (Pubitemid 24184056)
39. Stokoe D, Macdonald SG, Cadwallader K, Symons M, Hancock JF (1994) Activation of Raf as a result of recruitment to the plasma membrane. Science 264(5164):1463-1467. (Pubitemid 24217138)