Multi-dimensional correlative imaging of subcellular events: Combining the strengths of light and electron microscopy

Biophysical Reviews

Volumn 2, Issue 3, 2010, Pages 121-135

  Su, Yingying ^a   Nykanen, Marko ^b   Jahn, Kristina A ^a   Whan, Renee ^a   Cantrill, Laurence ^b   Soon, Lilian L ^a   Ratinac, Kyle R ^a   Braet, Filip ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

Author keywords

Combinatorial labeling; Combined microscopy; Correlative morphomics; Electron tomography; Integrated microscopy; Live cell imaging

Indexed keywords

EID: 84858298161     PISSN: 18672450     EISSN: 18672469     Source Type: Journal    
DOI: 10.1007/s12551-010-0035-2     Document Type: Review

References (90)

1. Agronskaia AV, Valentijn JA, van Driel LF, Schneijdenberg CT, Humbel BM, van Bergen En Henegouwen PM, Verkleij AJ, Koster AJ, Gerritsen HC (2008) Integrated fluorescence and transmission electron microscopy. J Struct Biol 164: 183-189.
2. Albrecht RM, Goodman SL, Simmons SR (1989) Distribution and movement of membrane-associated platelet glycoproteins: use of colloidal gold with correlative video-enhanced light microscopy, low-voltage high-resolution scanning electron microscopy, and high-voltage transmission electron microscopy. Am J Anat 185: 149-164.
3. Albrecht RM, Olorundare OE, Simmons SR, Loftus JC, Mosher DF (1992) Use of correlative microscopy with colloidal gold labeling to demonstrate platelet receptor distribution and movement. Methods Enzymol 215: 456-479.
4. Biel SS, Kawaschinski K, Wittern KP, Hintze U, Wepf R (2003) From tissue to cellular ultrastructure: closing the gap between micro- and nanostructural imaging. J Microsc 212: 91-99.
5. Braet F, Ratinac K (2007) Creating next-generation microscopists: structural and molecular biology at the crossroads. J Cell Mol Med 11: 759-763.
6. Braet F, Geerts WJ (2009) Foreword to the themed issue on correlative microscopy. J Microsc 235: 239-240.
7. Braet F, Spector I, Shochet NR, Crews P, Higa T, Menu E, De Zanger R, Wisse E (2002) The new anti-actin agent dihydrohalichondramide reveals fenestrae-forming centers in hepatic endothelial cells. BMC Cell Biol 3: 7.
8. Braet F, Wisse E, Bomans P, Frederik P, Geerts W, Koster A, Soon L, Ringer S (2007) Contribution of high-resolution correlative imaging techniques in the study of the liver sieve in three-dimensions. Microsc Res Tech 70: 230-242.
9. Burton GJ, Thurley KW, Skepper JN (1991) A technique for correlative scanning and transmission electron microscopy of individual human placental villi: an example demonstrating syncytial sprouts in early gestation. Scan Microsc 5: 451-458.
10. Capani F, Saraceno E, Boti VR, Aon-Bertolino L, Fernández JC, Gato F, Kruse MS, Giraldez L, Ellisman MH, Coirini H (2008) A tridimensional view of the organization of actin filaments in the central nervous system by use of fluorescent photooxidation. Biocell 32: 1-8.
11. Chang JC, Su HL, Hsu SH (2008) The use of peptide-delivery to protect human adipose-derived adult stem cells from damage caused by the internalization of quantum dots. Biomaterials 29: 925-936.
12. Chen I, Ting AY (2005) Site-specific labeling of proteins with small molecules in live cells. Curr Opin Biotechnol 16: 35-40.
13. Cheutin T, Sauvage C, Tchélidzé P, O'Donohue MF, Kaplan H, Beorchia A, Ploton D (2007) Visualizing macromolecules with fluoronanogold: from photon microscopy to electron tomography. Methods Cell Biol 79: 559-574.
14. Cowieson NP, Kobe B, Martin JL (2008) United we stand: combining structural methods. Curr Opin Struct Biol 18: 617-622.
15. Dahan M, Lévi S, Luccardini C, Rostaing P, Riveau B, Triller A (2003) Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 302: 442-445.
16. Darien BJ, Sims PA, Kruseelliott KT, Homan TS, Cashwell RJ, Cooley AJ, Albrecht RM (1995) Use of colloidal gold and neutron-activation in correlative microscopic labeling and label quantitation. Scan Microsc 9: 773-780.
17. Deerinck TJ (2008) The application of fluorescent quantum dots to confocal, multiphoton, and electron microscopic imaging. Toxicol Pathol 36: 112-116.
18. Deerinck TJ, Martone ME, Lev-Ram V, Green DP, Tsien RY, Spector DL, Huang S, Ellisman MH (1994) Fluorescence photooxidation with eosin: a method for high resolution immunolocalization and in situ hybridization detection for light and electron microscopy. J Cell Biol 126: 901-910.
19. Deerinck TJ, Giepmans BNG, Smarr BL, Martone ME, Ellisman MH (2007) Light and electron microscopic localization of multiple proteins using quantum dots. Methods Mol Biol 374: 43-53.
20. DeFelipe J, Fairén A (1993) A simple and reliable method for correlative light and electron microscopic studies. J Histochem Cytochem 41: 769-772.
21. Derfus AM, Chan WCW, Bhatia SM (2004) Intracellular delivery of quantum dots for live cell labeling and organelle tracking. Adv Mater 16: 961-966.
22. Donnell C, Hyde B, Dowling EA (1988) Correlative light and scanning electron-microscopy of endometrium in postmenopausal hormone replacement candidates. Mod Pathol 1: A25-A25.
23. Dubertret B, Skourides P, Norris DJ, Noireaux V, Brivanlou AH, Libchaber A (2002) In vivo imaging of quantum dots encapsulated in phospholipid micelles. Science 298: 1759-1762.
24. Ellis EA (2008) Correlative transmission microscopy: cytochemical localization and immunocytochemical localization in studies of oxidative and nitrosative stress. Methods Mol Biol 477: 41-48.
25. Fomina AF, Deerinck TJ, Ellisman MH, Cahalan MD (2003) Regulation of membrane trafficking and subcellular organization of endocytic compartments revealed with FM1-43 in resting and activated human T cells. Exp Cell Res 291: 150-166.
26. Frey TG, Sun MG (2008) Correlated light and electron microscopy illuminates the role of mitochondrial inner membrane remodeling during apoptosis. Biochim Biophys Acta 1777: 847-852.
27. Fucikova A, Valenta J, Pelant I, Brezina V (2009) Novel use of silicon nanocrystals and nanodiamonds in biology. Chem Pap 63: 704-708.
28. Geissinger HD (1974) A precise stage arrangement for correlative microscopy for specimens mounted on glass slides, stubs or EM grids. J Microsc 100: 113-117.
29. Giepmans BN (2008) Bridging fluorescence microscopy and electron microscopy. Histochem Cell Biol 130: 211-217.
30. Giepmans BN, Deerinck TJ, Smarr BL, Jones YZ, Ellisman MH (2005) Correlated light and electron microscopic imaging of multiple endogenous proteins using Quantum dots. Nat Methods 10: 743-749.
31. Goodman SL, Albrecht RM (1987) Correlative light and electron-microscopy of platelet-adhesion and fibrinogen receptor expression using colloidal-gold labeling. Scan Microsc 1: 727-734.
32. Grabenbauer M, Geerts WJ, Fernadez-Rodriguez J, Hoenger A, Koster AJ, Nilsson T (2005) Correlative microscopy and electron tomography of GFP through photooxidation. Nat Methods 14: 857-862.
33. Hainfeld JF, Furuya FR (1992) A 1. 4-nm gold cluster covalently attached to antibodies improves immunolabeling. J Histochem Cytochem 40: 177-184.
34. Hekking LH, Lebbink MN, De Winter DA, Schneijdenberg CT, Brand CM, Humbel BM, Verkleij AJ, Post JA (2009) Focused ion beam-scanning electron microscope: exploring large volumes of atherosclerotic tissue. J Microsc 235: 336-347.
35. Hirabayashi Y, Yamada K (1998) A histochemical approach to correlative light and electron microscopic detection of acidic glycoconjugates by a sensitized high iron diamine method. J Histochem Cytochem 46: 767-770.
36. Ho Y-P, Leong KW (2010) Quantum dot-based theranostics. Nanoscale 2: 60-68.
37. Hwang RD, Chen CC, Knecht DA (2009) ReAsH: another viable option for in vivo protein labelling in Dictyostelium. J Microsc 234: 9-15.
38. Jahn KA, Braet F (2008) Monitoring membrane rafts in colorectal cancer cells by means of correlative fluorescence electron microscopy (CFEM). Micron 39: 1393-1397.
39. Jahn K, Barton D, Braet F (2007) Correlative fluorescence- and scanning, transmission electron microscopy for biomolecular investigation. In: Díaz J, Méndez-Vilas A (eds) Modern research and educational topics in microscopy. Formatex Press, Badajoz, pp 203-211.
40. Jahn KA, Barton DA, Su Y, Riches J, Kable EPW, Soon LL, Braet F (2009) Correlative fluorescence and transmission electron microscopy imaging of the actin cytoskeleton of whole-mount (breast) cancer cells. J Microsc 235: 282-292.
41. Kushida T, Nagato Y, Iijima H, Kushida H (1993) Correlative light and electron microscopy of the same sections embedded in HPMA, Quetol 523 and MMA. Okajimas Folia Anat Jpn 69: 277-287.
42. Larson DR, Zipfel WR, Williams RM, Clark SW, Bruchez MP, Wise FW, Webb WW (2003) Water-soluble quantum dots for multiphoton fluorescence imaging in vivo. Science 300: 1434-1436.
43. Lin MZ, Wang L (2008) Selective labeling of proteins with chemical probes in living cells. Physiology 23: 131-141.
44. Lübke J (1993) Photoconversion of diaminobenzidine with different fluorescent neuronal markers into a light and electron microscopic dense reaction product. Microsc Res Tech 24: 2-14.
45. Martin BR, Giepmans BN, Adams SR, Tsien RY (2005) Mammalian cell-based optimization of the biarsenical binding tetracycteine motif for improved fluorescence and affinity. Nat Biotechnol 23: 1308-1314.
46. Mattheakis LC, Dias JM, Choi Y-J, Gong J (2004) Optical coding of mammalian cells using semiconductor quantum dots. Anal Biochem 327: 200-208.
47. McCann CM, Bareyre FM, Lichtman JW, Sanes JR (2005) Peptide tags for labeling membrane proteins in live cells with multiple fluorophores. Biotechniques 38: 945-952.
48. McDonald K (2009) A review of high-pressure freezing preparation techniques for correlative light and electron microscopy of the same cells and tissues. J Microsc 235: 273-281.
49. McDonald LW, Hayes TL (1969) Correlation of scanning electron microscope and light microscope images of individual cells in human blood and blood clots. Exp Mol Pathol 10: 186-198.
50. Meißlitzer-Ruppitsch C, Röhrl CR, Neumuller J, Pavelka M, Ellinger A (2009) Photooxidation technology for correlated light and electron microscopy. J Microsc 235: 322-335.
51. Miller SE, Howell DN (1997) Concerted use of immunologic and ultrastructural analyses in diagnostic medicine: Immunoelectron microscopy and correlative microscopy. Immunol Invest 26: 29-38.
52. Mironov AA, Beznoussenko GV (2009) Correlative microscopy: a potent tool for the study of rare or unique cellular and tissue events. J Microsc 235: 308-321.
53. Mironov AA, Polishchuk RS, Luini A (2000) Visualizing membrane traffic in vivo by combined video fluorescence and 3D electron microscopy. Trends Cell Biol 8: 349-353.
54. Monosov EZ, Wenzel TJ, Lüers GH, Heyman JA, Subramani S (1996) Labeling of peroxisomes with green fluorescent protein in living P. pastoris cells. J Histochem Cytochem 44: 581-589.
55. Morphew MHW, Bjorkman PJ, McIntosh JR (2008) Silver enhancement of nanogold particles during freeze substitution for electron microscopy. J Microsc 230: 263-267.
56. Nishiyama H, Suga M, Ogura T, Maruyama Y, Koizumi M, Mio K, Kitamura S, Sato C (2010) Atmospheric scanning electron microscope observes cells and tissues in open medium through silicon nitride film. J Struct Biol 169: 438-449.
57. Nisman R, Dellaire G, Ren Y, Li R, Bazett-Jones DP (2004) Application of quantum dots as probes for correlative fluorescence, conventional, and energy-filtered transmission electron microscopy. J Histochem Cytochem 52: 13-18.
58. Nixon SJ, Webb RI, Floetenmeyer M, Schieber N, Lo HP, Parton RG (2009) A single method for cryofixation and correlative light, electron microscopy and tomography of zebrafish embryos. Traffic 10: 131-136.
59. Nykänen M (2009) Correlation of light with electron microscopy: a correlative microscopy platform. In: Goldys EM (ed) Fluorescence applications in biotechnology and life sciences. Wiley-Blackwell, Hoboken, pp 141-156.
60. Oehring H, Halbhuber KJ (1991) Employment of merocyanine 540 fluorescence to form diaminobenzidine (DAB) oxidation product: a photoconversion method for the visualization of erythrocyte membrane fluidity for light and electron microscopy. Acta Histochem 90: 127-134.
61. Pagano RE, Sepanski MA, Martin OC (1989) Molecular trapping of a fluorescent ceramide analogue at the Golgi apparatus of fixed cells: interaction with endogenous lipids provides a trans-Golgi marker for both light and electron microscopy. J Cell Biol 109: 2067-2079.
62. Park H, Hanson GT, Duff SR, Selvin PR (2004) Nanometre localization of single ReAsH molecules. J Microsc 216: 199-205.
63. Peachey LD, Ishikawa H, Murakami T (1996) Correlated confocal and intermediate voltage electron microscopy imaging of the same cells using sequential fluorescence labeling, fixation, and critical point dehydration. Scan Microsc 10: 237-247.
64. Peng XG (2003) Mechanisms for the shape-control and shape-evolution of colloidal semiconductor nanocrystals. Adv Mater 15: 459-463.
65. Perinetti G, Müller T, Spaar A, Polishchuk R, Luini A, Egner A (2009) Correlation of 4Pi and electron microscopy to study transport through single Golgi stacks in living cells with super resolution. Traffic 10: 379-391.
66. Plitzko JM, Rigort A, Leis A (2009) Correlative cryo-light microscopy and cryo-electron tomography: from cellular territories to molecular landscapes. Curr Opin Biotechnol 20: 83-89.
67. Powell RD, Halsey CM, Hainfeld JF (1998) Combined fluorescent and gold immunoprobes: reagents and methods for correlative light and electron microscopy. Microsc Res Tech 42: 2-12.
68. Rash JE, Yasumura T, Dudek FE (1998) Ultrastructure, histological distribution, and freeze-fracture immunocytochemistry of gap junctions in rat brain and spinal cord. Cell Biol Int 22: 731-749.
69. Razi M, Tooze SA (2009) Correlative light and electron microscopy. Methods Enzymol 452: 261-275.
70. Reynolds AM, Sculimbrene BR, Imperiali B (2008) Lanthanide-binding tags with unnatural amino acids: sensitizing Tb3+ and Eu3+ luminescence at longer wavelengths. Bioconjug Chem 19: 588-591.
71. Rieder CL, Bowser SS (1985) Correlative immunofluorescence and electron-microscopy on the same section of epon-embedded material. J Histochem Cytochem 33: 165-171.
72. Robinson JM, Vandré DD (1997) Efficient immunocytochemical labeling of leukocyte microtubules with FluoroNanogold: an important tool for correlative microscopy. J Histochem Cytochem 45: 631-642.
73. Säälik P, Padari K, Niinep A, Lorents A, Hansen M, Jokitalo E, Langel Ü, Pooga M (2009) Protein delivery with transportans is mediated by caveolae rather than flotillin-dependent pathways. Bioconjug Chem 20: 877-887.
74. Schmued LC, Snavely LF (1993) Photoconversion and electron microscopic localization of the fluorescent axon tracer fluoro-ruby (rhodamine-dextran-amine). J Histochem Cytochem 41: 777-782.
75. Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Methods 2: 905-909.
76. Simmons SR, Pawley JB, Albrecht RM (1990) Optimizing parameters for correlative immunogold localization by video-enhanced light microscopy, high-voltage transmission electron microscopy, and field emission scanning electron microscopy. J Histochem Cytochem 38: 1781-1785.
77. Sletten EM, Bertozzi CR (2009) Bioorthogonal chemistry: fishing for selectivity in a sea of functionality. Angew Chem Int Ed Eng 48: 6974-6998.
78. Smith A, Ruan G, Rhyner M, Nie S (2006) Engineering luminescent quantum dots for in vivo molecular and cellular imaging. Ann Biomed Eng 34: 3-14.
79. Sosinsky GE, Giepmans BN, Deerinck TJ, Gaietta GM, Ellisman MH (2007) Markers for correlated light and electron microscopy. Methods Cell Biol 79: 575-591.
80. Subramaniam S (2005) Bridging the imaging gap: visualizing subcellular architecture with electron tomography. Curr Opin Microbiol 8: 316-322.
81. Sun MG, Williams J, Munoz-Pinedo C, Perkins GA, Brown JM, Ellisman MH, Green DR, Frey TG (2007) Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis. Nat Cell Biol 9: 1057-1072.
82. Sunbul M, Yen M, Zou Y, Yin J (2008) Enzyme catalyzed site-specific protein labeling and cell imaging with quantum dots. Chem Commun 45: 5927-5929.
83. Swanson JA, Peters PJ (2005) Subcellular imaging technologies - microscopic visual thinking. Curr Opin Microbiol 8: 313-315.
84. Takizawa T, Robinson JM (2000) Analysis of antiphotobleaching reagents for use with fluoronanogold in correlative microscopy. J Histochem Cytochem 48: 433-436.
85. Verkade P (2008) Moving EM: the Rapid Transfer System as a new tool for correlative light and electron microscopy and high throughput for high-pressure freezing. J Microsc 230: 317-328.
86. Walling MA, Novak JA, Shepard JR (2009) Quantum dots for live cell and in vivo imaging. Int J Mol Sci 10: 441-491.
87. Walther C, Meyer K, Rennert R, Neundorf I (2008) Quantum dot-carrier peptide conjugates suitable for imaging and delivery applications. Bioconjug Chem 19: 2346-2356.
88. Wynford-Thomas D, Jasani B, Newman GR (1986) Immunohistochemical localization of cell surface receptors using a novel method permitting simple, rapid and reliable LM/EM correlation. Histochem J 18: 387-396.
89. Zhang Y, So MK, Rao J (2006) Protease-modulated cellular uptake of quantum dots. Nano Lett 6: 1988-1992.
90. Zipfel W, Williams R, Webb W (2003) Nonlinear magic: multiphoton microscopy in the biosciences. Nat Biotechnol 21: 1369-1377.