Stochastic approach to the molecular counting problem in superresolution microscopy

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

Volumn 112, Issue 2, 2015, Pages E110-E118

  Rollins, Geoffrey C ^a   Shin, Jae Yen ^b   Bustamante, Carlos ^b   Pressé, Steve ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INDIANA UNIVERSITY   (United States)

Author keywords

Counting problem; Fluorescence; Protein complexes; Single molecule; Superresolution

Indexed keywords

ION CHANNEL; FLUORESCENT DYE; MACROMOLECULE; MULTIPROTEIN COMPLEX;

ACCURACY; ANATOMICAL CONCEPTS; ARTICLE; DIFFRACTION; DYNAMICS; KINETICS; MATHEMATICAL COMPUTING; MICROSCOPY; MOLECULAR COUNTING PROBLEM; PREDICTION; PRIORITY JOURNAL; STOCHASTIC MODEL; STOICHIOMETRY; SUPERRESOLUTION MICROSCOPY; CHEMICAL MODEL; CHEMISTRY; FLUORESCENCE MICROSCOPY; MACROMOLECULE; MOLECULAR IMAGING; PHOTOCHEMISTRY; PROBABILITY; PROCEDURES; STATISTICAL MODEL; STATISTICS; STATISTICS AND NUMERICAL DATA;

FLUORESCENT DYES; LIKELIHOOD FUNCTIONS; MACROMOLECULAR SUBSTANCES; MARKOV CHAINS; MICROSCOPY; MICROSCOPY, FLUORESCENCE; MODELS, CHEMICAL; MOLECULAR IMAGING; MULTIPROTEIN COMPLEXES; PHOTOCHEMICAL PROCESSES; STOCHASTIC PROCESSES;

EID: 84920972458     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1408071112     Document Type: Article

References (66)

1. Zamft B, Bintu L, Ishibashi T, Bustamante C (2012) Nascent RNA structure modules the transcription dynamics of RNA polymerases. Proc Natl Acad Sci USA 109(23): 8948-8953.
2. Boyer PD (1997) The ATP synthase-a splendid molecular machine. Annu Rev Biochem 66:717-749.
3. Cimini D (2008) Merotelic kinetochore orientation, aneuploidy, and cancer. Biochimica et Biophysica Acta Rev Cancer 1786(1):32-40.
4. Cai S, O'Connell CB, Khodjakov A, Walczak CE (2009) Chromosome congression in the absence of kinetochore fibres. Nat Cell Biol 11(7):832-838.
5. Nakajo K, Ulbrich MH, Kubo Y, Isacoff EY (2010) Stoichiometry of the KCNQ1-KCNE1 ion channel complex. Proc Natl Acad Sci USA 107(44):18862-18867.
6. Osteen JD, Sampson KJ, Kass RS (2010) The cardiac IKs channel, complex indeed. Proc Natl Acad Sci USA 107(44):18751-18752.
7. Morin TJ, Kobertz WR (2008) Counting membrane-embedded KCNE beta-subunits in functioning K+ channel complexes. Proc Natl Acad Sci USA 105(5):1478-1482.
8. Yano M, et al. (2000) Altered stoichiometry of FKBP12. 6 versus ryanodine receptor as a cause of abnormal Ca(2+) leak through ryanodine receptor in heart failure. Circulation 102(17):2131-2136.
9. Lacoste TD, et al. (2000) Ultrahigh-resolution multicolor colocalization of single fluorescent probes. Proc Natl Acad Sci USA 97(17):9461-9466.
10. Gordon MP, Ha T, Selvin PR (2004) Single-molecule high-resolution imaging with photobleaching. Proc Natl Acad Sci USA 101(17):6462-6465.
11. Huang B, Bates M, Zhuang X (2009) Super-resolution fluorescence microscopy. Annu Rev Biochem 78:993-1016.
12. Qu X, Wu D, Mets L, Scherer NF (2004) Nanometer-localized multiple single-molecule fluorescence microscopy. Proc Natl Acad Sci USA 101(31):11298-11303.
13. Dedecker P, De Schryver FC, Hofkens J (2013) Fluorescent proteins: Shine on, you crazy diamond. J Am Chem Soc 135(7):2387-2402.
14. Wiedenmann J, et al. (2004) EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc Natl Acad Sci USA 101(45):15905-15910.
15. Gurskaya NG, et al. (2006) Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat Biotechnol 24(4):461-465.
16. Fron E, et al. (2013) Revealing the excited-state dynamics of the fluorescent protein Dendra2. J Phys Chem B 117(8):2300-2313.
17. Wu DM, et al. (2006) KCNE2 is colocalized with KCNQ1 and KCNE1 in cardiac myocytes and may function as a negative modulator of I(Ks) current amplitude in the heart. Heart Rhythm 3(12):1469-1480.
18. Coffman VC, Wu P, Parthun MR, Wu JQ (2011) CENP-A exceeds microtubule attachment sites in centromere clusters of both budding and fission yeast. J Cell Biol 195(4): 563-572.
19. Lawrimore J, Bloom KS, Salmon ED (2011) Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. J Cell Biol 195(4):573-582.
20. Leake MC, et al. (2006) Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443(7109):355-358.
21. Ulbrich MH, Isacoff EY (2007) Subunit counting in membrane-bound proteins. Nat Methods 4(4):319-321.
22. Hastie P, et al. (2013) AMPA receptor/TARP stoichiometry visualized by single-molecule subunit counting. Proc Natl Acad Sci USA 110(13):5163-5168.
23. Delalez NJ, et al. (2010) Signal-dependent turnover of the bacterial flagellar switch protein FliM. Proc Natl Acad Sci USA 107(25):11347-11351.
24. Heilemann M, Dedecker P, Hofkens J, Sauer M (2009) Photoswitches: Key molecules for subdiffraction-resolution fluorescence imaging and molecular quantification. Laser Photon Rev 3(1-2):180-202.
25. Roy A, Field MJ, Adam V, Bourgeois D (2011) The nature of transient dark states in a photoactivatable fluorescent protein. J Am Chem Soc 133(46):18586-18589.
26. Schäfer LV, Groenhof G, Boggio-Pasqua M, Robb MA, Grubmüller H (2008) Chromophore protonation state controls photoswitching of the fluoroprotein asFP595. PLOS Comput Biol 4(3):e1000034.
27. Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY (2001) Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J Biol Chem 276(31):29188-29194.
28. McKinney SA, Murphy CS, Hazelwood KL, Davidson MW, Looger LL (2009) A bright and photostable photoconvertible fluorescent protein. Nat Methods 6(2):131-133.
29. Lukyanov KA, Chudakov DM, Lukyanov S, Verkhusha VV (2005) Innovation: Photoactivatable fluorescent proteins. Nat Rev Mol Cell Biol 6(11):885-891.
30. Lippincott-Schwartz J, Patterson GH (2003) Development and use of fluorescent protein markers in living cells. Science 300(5616):87-91.
31. Dickson RM, Cubitt AB, Tsien RY, Moerner WE (1997) On/off blinking and switching behaviour of single molecules of green fluorescent protein. Nature 388(6640): 355-358.
32. Remington SJ (2006) Fluorescent proteins: Maturation, photochemistry and photophysics. Curr Opin Struct Biol 16(6):714-721.
33. Chudakov DM, Feofanov AV, Mudrik NN, Lukyanov S, Lukyanov KA (2003) Chromophore environment provides clue to "kindling fluorescent protein" riddle. J Biol Chem 278(9):7215-7219.
34. Colquhoun D, Hawkes AG (1981) On the stochastic properties of single ion channels. Proc R Soc Lond B Biol Sci 211(1183):205-235.
35. Kienker P (1989) Equivalence of aggregated Markov models of ion-channel gating. Proc R Soc Lond B Biol Sci 236(1284):269-309.
36. Colquhoun D, Hawkes AG, Srodzinski K (1996) Joint distributions of apparent open and shut times of single-ion channels and maximum likelihood fitting of mechanisms. Philos Trans R Soc A-Math Phys Eng Sci 354:2555-2590.
37. Qin F, Auerbach A, Sachs F (1996) Estimating single-channel kinetic parameters from idealized patch-clamp data containing missed events. Biophys J 70(1):264-280.
38. Qin F, Auerbach A, Sachs F (1997) Maximum likelihood estimation of aggregated Markov processes. Proc Biol Sci 264(1380):375-383.
39. Coltharp C, Kessler RP, Xiao J (2012) Accurate construction of photoactivated localization microscopy (PALM) images for quantitative measurements. PLoS ONE 7(12):e51725.
40. Lee SH, Shin JY, Lee A, Bustamante C (2012) Counting single photoactivatable fluorescent molecules by photoactivated localization microscopy (PALM). Proc Natl Acad Sci USA 109(43):17436-17441.
41. Annibale P, Vanni S, Scarselli M, Rothlisberger U, Radenovic A (2011) Identification of clustering artifacts in photoactivated localization microscopy. Nat Methods 8(7): 527-528.
42. 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.
43. Gillespie DT (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81(25):2340-2361.
44. Durisic N, Laparra-Cuervo L, Sandoval-Alvarez A, Borbely JS, Lakadamyali M (2014) Single-molecule evaluation of fluorescent protein photoactivation efficiency using an in vivo nanotemplate. Nat Methods 11(2):156-162.
45. Zhang L, et al. (2007) Method for real-time monitoring of protein degradation at the single cell level. Biotechniques 42(4):446-450, 448, 450.
46. McKinney SA, Murphy CS, Hazelwood KL, Davidson MW, Looger LL (2009) A bright and photostable photoconvertible fluorescent protein. Nat Methods 6(2):131-133.
47. Johnston K, et al. (2010) Vertebrate kinetochore protein architecture: Protein copy number. J Cell Biol 189(6):937-943.
48. Efron B (1979) Bootstrap methods: Another look at the jackknife. Ann Stat 7(1):1-26.
49. Efron B, Tibshirani R (1991) Statistical data analysis in the computer age. Science 253(5018):390-395.
50. Corey S, Krapivinsky G, Krapivinsky L, Clapham DE (1998) Number and stoichiometry of subunits in the native atrial G-protein-gated K+ channel, IKACh. J Biol Chem 273(9):5271-5278.
51. Bisetto E, et al. (2008) Functional and stoichiometric analysis of subunit e in bovine heart mitochondrial F(0)F(1)ATP synthase. J Bioenerg Biomembr 40(4):257-267.
52. Huh WK, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425(6959):686-691.
53. Newman JR, et al. (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441(7095):840-846.
54. Joglekar AP, Salmon ED, Bloom KS (2008) Counting kinetochore protein numbers in budding yeast using genetically encoded fluorescent proteins. Methods Cell Biol 85: 127-151.
55. Wu JQ, McCormick CD, Pollard TD (2008) Chapter 9: Counting proteins in living cells by quantitative fluorescence microscopy with internal standards. Methods Cell Biol 89:253-273.
56. Coffman VC, Wu JQ (2012) Counting protein molecules using quantitative fluorescence microscopy. Trends Biochem Sci 37(11):499-506.
57. Collins KA, Furuyama S, Biggins S (2004) Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr Biol 14(21): 1968-1972.
58. Meluh PB, Yang P, Glowczewski L, Koshland D, Smith MM (1998) Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94(5):607-613.
59. Joglekar AP, Bouck DC, Molk JN, Bloom KS, Salmon ED (2006) Molecular architecture of a kinetochore-microtubule attachment site. Nat Cell Biol 8(6):581-585.
60. Jiang M, et al. (2009) Dynamic partnership between KCNQ1 and KCNE1 and influence on cardiac IKs current amplitude by KCNE2. J Biol Chem 284(24):16452-16462.
61. Bendahhou S, et al. (2005) In vitro molecular interactions and distribution of KCNE family with KCNQ1 in the human heart. Cardiovasc Res 67(3):529-538.
62. Yano M, et al. (2003) FKBP12. 6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure. Circulation 107(3):477-484.
63. Cingolani E, et al. (2007) Gene therapy to inhibit the calcium channel beta subunit: Physiological consequences and pathophysiological effects in models of cardiac hypertrophy. Circ Res 101(2):166-175.
64. Yu H, et al. (2013) Dynamic subunit stoichiometry confers a progressive continuum of pharmacological sensitivity by KCNQ potassium channels. Proc Natl Acad Sci USA 110(21):8732-8737.
65. Roux B, Sauvé R (1985) A general solution to the time interval omission problem applied to single channel analysis. Biophys J 48(1):149-158.
66. Zhu CY, Byrd RH, Lu PH, Nocedal J (1997) Algorithm 778: L-BFGS-B: Fortran subroutines for large-scale bound-constrained optimization. ACM Trans Math Softw 23(4):550-560.