Top

Published in:

01-03-2019 | Review

Methods for array tomography with correlative light and electron microscopy

Authors: Taro Koike, Hisao Yamada

Published in: Medical Molecular Morphology | Issue 1/2019

Abstract

The three-dimensional ultra-structure is the comprehensive structure that cannot be observed from a two-dimensional electron micrograph. Array tomography is one method for three-dimensional electron microscopy. In this method, to obtain consecutive cross sections of tissue, connected consecutive sections of a resin block are mounted on a flat substrate, and these are observed with scanning electron microscopy. Although array tomography requires some bothersome manual procedures to prepare specimens, a recent study has introduced some techniques to ease specimen preparation. In addition, array tomography has some advantages compared with other three-dimensional electron microscopy techniques. For example, sections on the substrate are stored semi-eternally, so they can be observed at different magnifications. Furthermore, various staining methods, including post-embedding immunocytochemistry, can be adopted. In the present review, the preparation of specimens for array tomography, including ribbon collection and the staining method, and the adaptability for correlative light and electron microscopy are discussed.

White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1–340CrossRefPubMed

Denk W, Horstmann H (2004) Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2:e329CrossRefPubMedPubMedCentral

Knott G, Marchman H, Wall D, Lich B (2008) Serial section scanning electron microscopy of adult brain tissue using focused ion beam milling. J Neurosci 28:2959–2964CrossRefPubMedPubMedCentral

Micheva KD, Smith SJ (2007) Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55:25–36CrossRefPubMedPubMedCentral

Cardona A, Saalfeld S, Schindelin J, Arganda-Carreras I, Preibisch S, Longair M, Tomancak P, Hartenstein V, Douglas RJ (2012) TrakEM2 software for neural circuit reconstruction. PLoS One 7:e38011CrossRefPubMedPubMedCentral

Saalfeld S, Fetter R, Cardona A, Tomancak P (2012) Elastic volume reconstruction from series of ultra-thin microscopy sections. Nat Methods 9:717–720CrossRefPubMed

Briggman KL, Helmstaedter M, Denk W (2011) Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:183–188CrossRefPubMed

Vihinen H, Belevich I, Jokitalo E (2013) Three dimensional electron microscopy of cellular organ elles by serial block face SEM and ET. Microsc anal 27:7–10

Kopek BG, Shtengel G, Xu CS, Clayton DA, Hess HF (2012) Correlative 3D superresolution fluorescence and electron microscopy reveal the relationship of mitochondrial nucleoids to membranes. Proc Natl Acad Sci USA 109:6136–6141CrossRefPubMed

10.

Wei D, Jacobs S, Modla S, Zhang S, Young CL, Cirino R, Caplan J, Czymmek K (2012) High-resolution three-dimensional reconstruction of a whole yeast cell using focused-ion beam scanning electron microscopy. Biotechniques 53:41–48PubMedCrossRef

11.

Hayworth KJ, Morgan JL, Schalek R, Berger DR, Hildebrand DG, Lichtman JW (2014) Imaging ATUM ultrathin section libraries with WaferMapper: a multi-scale approach to EM reconstruction of neural circuits. Front Neural Circuits 8:68CrossRefPubMedPubMedCentral

12.

Hayworth KJ, Kasthuri N, Schalek R, Lichtman JW (2006) Automating the collection of ultrathin serial sections for large volume TEM reconstructions. Microsc Microanal 12:86–87CrossRef

13.

Terasaki M, Shemesh T, Kasthuri N, Klemm RW, Schalek R, Hayworth KJ, Hand AR, Yankova M, Huber G, Lichtman JW, Rapoport TA, Kozlov MM (2013) Stacked endoplasmic reticulum sheets are connected by helicoidal membrane motifs. Cell 154:285–296CrossRefPubMedPubMedCentral

14.

Koga D, Kusumi S, Ushiki T (2016) Three-dimensional shape of the Golgi apparatus in different cell types: serial section scanning electron microscopy of the osmium-impregnated Golgi apparatus. Microscopy (Oxf) 65:145–157CrossRef

15.

Koga D, Kusumi S, Ushiki T, Watanabe T (2017) Integrative method for three-dimensional imaging of the entire Golgi apparatus by combining thiamine pyrophosphatase cytochemistry and array tomography using backscattered electron-mode scanning electron microscopy. Biomed Res 38:285–296CrossRefPubMed

16.

Blumer MJ, Gahleitner P, Narzt T, Handl C, Ruthensteiner B (2002) Ribbons of semithin sections: an advanced method with a new type of diamond knife. J Neurosci Methods 120:11–16CrossRefPubMed

17.

Horstmann H, Korber C, Satzler K, Aydin D, Kuner T (2012) Serial section scanning electron microscopy (S3EM) on silicon wafers for ultra-structural volume imaging of cells and tissues. PLoS One 7:e35172CrossRefPubMedPubMedCentral

18.

Spomer W, Hofmann A, Wacker I, Ness L, Brey P, Schröder R R, Gengenbach U (2015) Advanced substrate holder and multi-axis manipulation tool for ultramicrotomyAdvanced substrate holder and multi-axis manipulation tool for ultramicrotomy. Microsc Microanal 21:1277–1278CrossRef

19.

Wacker I, Spomer W, Hofmann A, Thaler M, Hillmer S, Gengenbach U, Schroder RR (2016) Hierarchical imaging: a new concept for targeted imaging of large volumes from cells to tissues. BMC Cell Biol 17:38CrossRefPubMedPubMedCentral

20.

Koike T, Kataoka Y, Maeda M, Hasebe Y, Yamaguchi Y, Suga M, Saito A, Yamada H (2017) A Device for Ribbon Collection for Array Tomography with Scanning Electron Microscopy. Acta Histochem Cytochem 50:135–140CrossRefPubMedPubMedCentral

21.

Tapia JC, Kasthuri N, Hayworth KJ, Schalek R, Lichtman JW, Smith SJ, Buchanan J (2012) High-contrast en bloc staining of neuronal tissue for field emission scanning electron microscopy. Nat Protoc 7:193–206CrossRefPubMedPubMedCentral

22.

Wacker I, Chockley P, Bartels C, Spomer W, Hofmann A, Gengenbach U, Singh S, Thaler M, Grabher C, Schroder RR (2015) Array tomography: characterizing FAC-sorted populations of zebrafish immune cells by their 3D ultrastructure. J Microsc 259:105–113CrossRefPubMedPubMedCentral

23.

Shodo R, Hayatsu M, Koga D, Horii A, Ushiki T (2017) Three-dimensional reconstruction of root cells and interdental cells in the rat inner ear by serial section scanning electron microscopy. Biomed Res 38:239–248CrossRefPubMed

24.

Armstrong WE, Rubrum A, Teruyama R, Bond CT, Adelman JP (2005) Immunocytochemical localization of small-conductance, calcium-dependent potassium channels in astrocytes of the rat supraoptic nucleus. J Comp Neurol 491:175–185CrossRefPubMed

25.

Yi H, Leunissen J, Shi G, Gutekunst C, Hersch S (2001) A novel procedure for pre-embedding double immunogold-silver labeling at the ultrastructural level. J Histochem Cytochem 49:279–284CrossRefPubMed

26.

Koffie RM, Meyer-Luehmann M, Hashimoto T, Adams KW, Mielke ML, Garcia-Alloza M, Micheva KD, Smith SJ, Kim ML, Lee VM, Hyman BT, Spires-Jones TL (2009) Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci U S A 106:4012–4017CrossRefPubMedPubMedCentral

27.

Soiza-Reilly M, Commons KG (2011) Quantitative analysis of glutamatergic innervation of the mouse dorsal raphe nucleus using array tomography. J Comp Neurol 519:3802–3814CrossRefPubMedPubMedCentral

28.

Yamashita S (2010) The post-embedding method for immunoelectron microscopy of mammalian tissues: a standardized procedure based on heat-induced antigen retrieval. Methods Mol Biol 657:237–248CrossRefPubMed

29.

Nakai Y, Iwashita T (1976) Correlative light and electron microscopy of the frog adrenal gland cells using adjacent epon-embedded sections. Arch Histol Jpn 39:183–191CrossRefPubMed

30.

Watari N, Tsukagoshi N, Honma Y (1970) The correlative light and electron microscopy of the islets of Langerhans in some lower vertebrates. Arch Histol Jpn 31:371–392CrossRefPubMed

31.

de Boer P, Hoogenboom JP, Giepmans BN (2015) Correlated light and electron microscopy: ultrastructure lights up! Nat Methods 12:503–513CrossRefPubMed

32.

Kim D, Deerinck TJ, Sigal YM, Babcock HP, Ellisman MH, Zhuang X (2015) Correlative stochastic optical reconstruction microscopy and electron microscopy. PLoS One 10:e0124581CrossRefPubMedPubMedCentral

33.

Koga D, Kusumi S, Bochimoto H, Watanabe T, Ushiki T (2015) Correlative light and scanning electron microscopy for observing the three-dimensional ultrastructure of membranous cell organelles in relation to their molecular components. J Histochem Cytochem 63:968–979CrossRefPubMedPubMedCentral

34.

Saitoh S, Ohno N, Saitoh Y, Terada N, Shimo S, Aida K, Fujii H, Kobayashi T, Ohno S (2018) improved serial sectioning techniques for correlative light-electron microscopy mapping of human langerhans islets. Acta Histochem Cytochem 51:9–20CrossRefPubMedPubMedCentral

35.

Sengle G, Tufa SF, Sakai LY, Zulliger MA, Keene DR (2013) A correlative method for imaging identical regions of samples by micro-CT, light microscopy, and electron microscopy: imaging adipose tissue in a model system. J Histochem Cytochem 61:263–271CrossRefPubMedPubMedCentral

36.

Collman F, Buchanan J, Phend KD, Micheva KD, Weinberg RJ, Smith SJ (2015) Mapping synapses by conjugate light-electron array tomography. J Neurosci 35:5792–5807CrossRefPubMedPubMedCentral

37.

Micheva KD, Busse B, Weiler NC, O’Rourke N, Smith SJ (2010) Single-synapse analysis of a diverse synapse population: proteomic imaging methods and markers. Neuron 68:639–653CrossRefPubMedPubMedCentral

38.

Oberti D, Kirschmann MA, Hahnloser RH (2010) Correlative microscopy of densely labeled projection neurons using neural tracers. Front Neuroanat 4:24PubMedPubMedCentral

39.

Oberti D, Kirschmann MA, Hahnloser RH (2011) Projection neuron circuits resolved using correlative array tomography. Front Neurosci 5:50CrossRefPubMedPubMedCentral

40.

Koga D, Kusumi S, Shodo R, Dan Y, Ushiki T (2015) High-resolution imaging by scanning electron microscopy of semithin sections in correlation with light microscopy. Microscopy (Oxf) 64:387–394CrossRef

41.

Beckwith MS, Beckwith KS, Sikorski P, Skogaker NT, Flo TH, Halaas O (2015) Seeing a mycobacterium-infected cell in nanoscale 3D: correlative imaging by light microscopy and FIB/SEM tomography. PLoS One 10:e0134644CrossRefPubMedPubMedCentral

42.

Booth DG, Beckett AJ, Molina O, Samejima I, Masumoto H, Kouprina N, Larionov V, Prior IA, Earnshaw WC (2016) 3D-CLEM Reveals that a Major Portion of Mitotic Chromosomes Is Not Chromatin. Mol Cell 64:790–802CrossRefPubMedPubMedCentral

43.

Shtengel G, Wang Y, Zhang Z, Goh WI, Hess HF, Kanchanawong P (2014) Imaging cellular ultrastructure by PALM, iPALM, and correlative iPALM-EM. Methods Cell Biol 123:273–294CrossRefPubMed

Title: Methods for array tomography with correlative light and electron microscopy
Authors: Taro Koike
Hisao Yamada
Publication date: 01-03-2019
Publisher: Springer Japan
Published in: Medical Molecular Morphology / Issue 1/2019
Print ISSN: 1860-1480
Electronic ISSN: 1860-1499
DOI: https://doi.org/10.1007/s00795-018-0194-y

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Methods for array tomography with correlative light and electron microscopy

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2019

Immunoreactivity patterns of tight junction proteins are useful for differential diagnosis of human salivary gland tumors

Mucinous adenocarcinoma, gastric type of the uterine cervix: clinical features and HER2 amplification

Physical exercise alters hepatic morphology of low-density lipoprotein receptor knockout ovariectomized mice

Combination of APD668, a G protein-coupled receptor 119 agonist with linagliptin, a DPPIV inhibitor, prevents progression of steatohepatitis in a murine model of non-alcoholic steatohepatitis with diabetes

BRI2 as an anti-Alzheimer gene

Positive correlation between the density of macrophages and T-cells in undifferentiated sarcoma