IMAGING TECHNIQUES FOR STUDYING VIRUS-CELL INTERACTIONS: A REVIEW OF CURRENT METHODS AND CHALLENGES



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Abstract

Knowledge of virus-host cell interactions is central to the formulation of antiviral therapies and vaccines. Because of their nanoscale size and dynamic nature, viruses are inherently difficult objects to investigate. Virus characterization, such as imaging viral structures, intracellular viral trafficking, and infection molecular mechanisms, has relied heavily on sophisticated imaging approaches. Classical light microscopy imaging, such as fluorescence and super-resolution microscopy, provides information on viral entry, replication, and protein localization within living cells. Electron microscopy (EM) techniques, such as Transmission Electron Microscopy (TEM), Scanning Electron Microscopy (SEM), and Cryo-Electron Microscopy (Cryo-EM), provide high-resolution structural information on the viruses and their replication compartments [53]. Advances in correlative imaging techniques, which include light and electron microscopy, have improved our ability to study virus-induced cellular changes in three dimensions. But in comparison to the earlier developments, it remains challenging in virus imaging: a compromise between resolution and sample preparation, restrictions in labeling methods, the challenge in imaging rapid virus-host interactions, and biosafety limitations for highly pathogenic viruses [10]. Solutions to these types of issues will be provided with the newer techniques such as AI-powered imaging analysis, nanotechnology-based imaging probes, and cryo-electron tomography. This review covers the present imaging methods in virology, their utilities and limitations, as well as future prospects, with an emphasis on microscopy to discern the interaction of viruses with cells [51].

About the authors

Sanjeev Kumar Jain

TMMC & RC, Moradabad, UP

Email: jainsanjeevkumar77@gmail.com
ORCID iD: 0000-0002-9609-5950

MD, professor, Department of Anatomy, TMMC & RC, Moradabad, UP

Россия

Sudhir Singh

TMMC & RC, Moradabad, UP

Email: singhdrsudhir4@gmail.com

MD, Professor, Department of Microbiology, TMMC & RC, Moradabad, UP

Индия

Sonika Sharma

TMMC & RC, Moradabad, UP

Email: soniyasharma19922@gmail.com

PhD, Associate Professor, Department of Anatomy, TMMC & RC, Moradabad, UP

Индия

Dr. Vasundhara

TMMC & RC, Moradabad, UP

Author for correspondence.
Email: vasu257@gmail.com

MD, Professor, Department of Microbiology, TMMC & RC, Moradabad, UP

Индия

References

  1. A Nickerson, Huang T, Lin LJ, Nan X. Photoactivated Localization Microscopy with Bimolecular Fluorescence Complementation
  2. J Vis Exp. 2015 Dec 22;(106):e53154 doi: 10.3791/53154. PMID: 26779930; PMCID: PMC4758764.
  3. Bernhard OK, Diefenbach RJ, Cunningham AL. New insights into viral structure and virus-cell interactions through proteomics. Expert Rev Proteomics. 2005 Aug;2(4):577-88. doi: 10.1586/14789450.2.4.577. PMID: 16097890.
  4. Bykov YS, Cortese M, Briggs JAG, Bartenschlager R. Correlative light and electron microscopy methods for the study of virus–cell interactions. FEBS Lett. 2016 Jul;590(13):1877–95. doi: 10.1002/1873-3468.12153
  5. Chen T, Tu S, Ding L, Jin M, Chen H, Zhou H. The role of autophagy in viral infections. J Biomed Sci. 2023 Jan 18;30(1):5. doi: 10.1186/s12929-023-00899-2. PMID: 36653801; PMCID: PMC9846652.
  6. Cole R.
  7. doi: 10.4161/cam.28348 Live-cell imaging. Cell Adh Migr. 2014 Sep;8(5):452–9. doi: 10.4161/cam.28348
  8. Cornish NE, Anderson NL, Arambula DG, Arduino MJ, Bryan A, Burton NC, et.al Clinical Laboratory Biosafety Gaps: Lessons Learned from Past Outbreaks Reveal a Path to a Safer Future. Clin Microbiol Rev. 2021 Jun 16;34(3):e0012618. doi: 10.1128/CMR.00126-18. Epub 2021 Jun 9. PMID: 34105993; PMCID: PMC8262806
  9. Cuervo AM, Knecht E, Terlecky SR, Dice JF. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am J Physiol. 1995;269(5 Pt 1):C1200. doi: 10.1152/ajpcell.1995.269.5.c1200
  10. DiGiuseppe S, Bienkowska-Haba M, Sapp M. Human Papillomavirus Entry: Hiding in a Bubble. J Virol. 2016 Sep;90(18):8032–5. doi: 10.1128/JVI.01065-16
  11. Dimitrov DS. Virus entry: molecular mechanisms and biomedical applications. Nat Rev Microbiol. 2004 Feb;2(2):109–22. doi: 10.1038/nrmicro817
  12. Dobbie IM. Bridging the resolution gap: correlative super-resolution imaging. Nat Rev Microbiol. 2019 Jun;17(6):337. Bridging the resolution gap: correlative super-resolution imaging. Nat Rev Microbiol. 2019 Jun;17(6):337.
  13. Earl LA, Falconieri V, Milne JL, Subramaniam S. Cryo-EM: Beyond the microscope. Curr Opin Struct Biol. 2017 Oct;46:71–8. doi: 10.1016/j.sbi.2017.06.002
  14. Ettinger A, Wittmann T. Fluorescence live cell imaging. Methods Cell Biol. 2014;123:77–94. doi: 10.1016/B978-0-12-420138-5.00005-7
  15. Fish KN. Total internal reflection fluorescence (TIRF) microscopy. Curr Protoc Cytom. 2009 Oct;50(1):12.18.1–13. doi: 10.1002/0471142956.cy1218s50
  16. Giacomelli G. Spatiotemporal localization of proteins in microorganisms via photoactivated localization microscopy. 2021;4(6):2-13 doi: 10.5282/edoc.27360
  17. Haase A, Brahic M, Stowring L, Blum H. Detection of viral nucleic acids by in situ hybridization. In: Methods in Virology. Vol. 7. New York: Academic Press; 1984. p. 189–226.
  18. doi: 10.1016/B978 0 12 470207 3.50013 9.
  19. Hell SW, Wichmann J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett. 1994 Jun;19(11):780. doi: 10.1364/OL.19.000780
  20. Hermann R, Walther P, Müller M. doi: 10.1007/BF02473200
  21. Immunogold labeling in scanning electron microscopy. Histochem Cell Biol. 1996;106(1):31–9. doi: 10.1007/BF02473200
  22. Hess ST, Girirajan TPK, Mason MD. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J. 2006;91(11):4258–72. doi: 10.1529/biophysj.106.091116
  23. Hlawacek G, Veligura V, van Gastel R, Poelsema B. Helium ion microscopy. J Vac Sci Technol B. 2014 Mar;32(2). doi: 10.1116/1.4863676
  24. Hoenen T, Groseth A. Virus–Host Cell Interactions. Cells. 2022 Feb;11(5):804. doi: 10.3390/cells11050804
  25. Jensen E, Crossman DJ. Technical review: Types of imaging—Direct STORM. Anat Rec. 2014 Dec;297(12):2227–31. doi: 10.1002/ar.22960
  26. Johnson DS, Jaiswal JK, Simon S. Total internal reflection fluorescence (TIRF) microscopy illuminator for improved imaging of cell surface events. Curr Protoc Cytom. 2012 Jul;61(1):12.29.1–19. doi: 10.1002/0471142956.cy1229s61
  27. Junod SL, Saredy J, Yang W. Nuclear import of adeno-associated viruses imaged by high-speed single-molecule microscopy. Viruses. 2021 Jan;13(2):167. doi: 10.3390/v13020167
  28. Laue M. Electron Microscopy of Viruses. Methods Cell Biol. 2010;96:1–20. doi: 10.1016/S0091-679X(10)96001-9
  29. Levsky JM, Singer RH. Fluorescence in situ hybridization: past, present and future. J Cell Sci. 2003 Jul 15;116(Pt 14):2833-8. doi: 10.1242/jcs.00633. PMID: 12808017.
  30. Lichtman JW, Conchello JA.
  31. Fluorescence microscopy. Nat Methods. 2005 Nov;2(12):910–9. doi: 10.1038/nmeth817
  32. Lu M. Single-molecule FRET imaging of virus spike–host interactions. Viruses. 2021;13(2):332. doi: 10.3390/v13020332
  33. Lucic V, Leis A, Baumeister W. . Cryo-electron tomography of cells: Connecting structure and function. Histochem Cell Biol. 2008 Aug;130(2):185–96. doi: 10.1007/s00418-008-0459-y
  34. McClelland RD, Culp TN, Marchant DJ. Imaging Flow Cytometry and Confocal Immunofluorescence Microscopy of Virus-Host Cell Interactions. Front Cell Infect Microbiol. 2021 Oct;11:749039. doi: 10.3389/fcimb.2021.749039
  35. Mohammed A, Abdullah A. Scanning electron microscopy (SEM): A review.
  36. Mukherjee S, Boutant E, Réal E, Mély Y, Anton H.
  37. Imaging viral infection by fluorescence microscopy: Focus on HIV-1 early stage. Viruses. 2021 Jan;13(2):213. doi: 10.3390/v13020213
  38. Murphy DB. Digital light microscopy techniques for the study. In: Murphy DB, editor. Fundamentals of Light Microscopy and Electronic Imaging. New York: Wiley-Liss; 1999. p. 1–32.
  40. Müller T, Schumann C, Kraegeloh A. STED Microscopy and its Applications: New Insights into Cellular Processes on the Nanoscale. ChemPhysChem. 2012 Jun;13(8):1986–2000. doi: 10.1002/cphc.201100986
  41. Müller TG, Sakin V, Müller B. A Spotlight on Viruses—Application of Click Chemistry to Visualize Virus-Cell Interactions. Molecules. 2019 Jan;24(3):481. doi: 10.3390/molecules24030481
  42. Nickerson A, Huang T, Lin LJ, Nan X.
  43. Photoactivated localization microscopy with bimolecular fluorescence complementation (BiFC-PALM). J Vis Exp. 2015 Dec;(106):e53154. doi: 10.3791/53154
  44. Parveen N, Borrenberghs D, Rocha S, Hendrix J. Single viruses on the fluorescence microscope: Imaging molecular mobility, interactions and structure sheds new light on viral replication. Viruses. 2018 May;10(5):250. doi: 10.3390/v10050250
  45. Payne S. Virus Interactions With the Cell. In: Viruses. 2017. p. 23. doi: 10.1016/B978-0-12-803109-4.00003-9
  46. Peddie CJ, Genoud C, Kreshuk A, Meechan K, Micheva KD, Narayan K et.al Volume electron microscopy. Nat Rev Methods Primers. 2022 Jul 7;2:51. Volume electron microscopy. Nat Rev Methods Primers. 2022 Jul 7;2:51.
  47. Rajcani J. Molecular mechanisms of virus spread and virion components as tools of virulence: A review. Acta Microbiol Immunol Hung. 2003;50(4):407–31. doi: 10.1556/AMicr.50.2003.4.8
  48. Razi M, Tooze SA. Chapter 17 Correlative light and electron microscopy. Methods Enzymol. 2009;452:261–75. doi: 10.1016/S0076-6879(08)03617-3
  49. Richert-Pöggeler KR, Franzke K, Hipp K, Kleespies RG. Electron microscopy methods for virus diagnosis and high resolution analysis of viruses. Front Microbiol. 2019 Jan;10:421852. doi: 10.3389/fmicb.2018.03255
  50. Risco C. Application of Advanced Imaging to the Study of Virus-Host Interactions. Viruses. 2021 Sep 29;13(10):1958. doi: 10.3390/v13101958. PMID: 34696388; PMCID: PMC8541363.
  51. Robb NC. Virus morphology: Insights from super-resolution fluorescence microscopy. Biochim Biophys Acta Mol Basis Dis. 2022 Apr;1868(4):166347. doi: 10.1016/j.bbadis.2022.166347
  52. Rust MJ, Bates M, Zhuang X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods. 2006 Oct;3(10):793–5. doi: 10.1038/nmeth929
  53. Ryan J, Gerhold AR, Boudreau V, Smith L, Maddox PS. Introduction to modern methods in light microscopy. Methods Mol Biol. 2017;1563:1–15. doi: 10.1007/978-1-4939-6810-7_1
  54. Saffarian S. Application of advanced light microscopy to the study of HIV and its interactions with the host. Viruses. 2021 Feb;13(2):223. doi: 10.3390/v13020223
  55. Saibil H, White N.
  56. Recent advances in biological imaging. Biosci Rep. 1989 Aug;9(4):437–49. doi: 10.1007/BF01117046
  57. Sakin V, Paci G, Lemke EA, Müller B. Lemke EA, Müller B. Labeling of virus components for advanced, quantitative imaging analyses. FEBS Lett. 2016 Jul;590(13):1896-914. doi: 10.1002/1873-3468.12131. Epub 2016 May 24. PMID: 26987299.
  58. Salpeter MM, McHenry FA
  59. Electron microscope autoradiography. Adv Tech Biol Electron Microsc. 1973;113–52.
  60. doi: 10.1002/1873-3468.12131. Epub 2016 May 24. PMID: 26987299.
  61. Sanderson MJ, Smith I, Parker I, Bootman MD. Fluorescence microscopy. Cold Spring Harb Protoc. 2014 Oct;2014(10):071-795. doi: 10.1101/pdb.top071795
  62. Santarella-Mellwig R, et al. Correlative Light Electron Microscopy (CLEM) for Tracking and Imaging Viral Protein Associated Structures in Cryo-immobilized Cells. J Vis Exp. 2018 Sep;(139):e58-154. doi: 10.3791/58154
  63. doi: 10.3791/58154
  64. Schmidt M, Byrne JM, Maasilta IJ. . Bio-imaging with the helium-ion microscope: A review. Beilstein J Nanotechnol. 2021 Jan;12:1–23. doi: 10.3762/bjnano.12.1
  65. Schnell U, Dijk F, Sjollema KA, Giepmans BNG. Immunolabeling artifacts and the need for live-cell imaging. Nat Methods. 2012 Feb;9(2):152–8. doi: 10.1038/nmeth.1855
  66. Shotton DM. Video-enhanced light microscopy and its applications in cell biology. J Cell Sci. 1988;89(Pt 2):129–50. doi: 10.1242/jcs.89.2.129
  67. Stewart PL, Dermody TS, Nemerow GR. Structural basis of nonenveloped virus cell entry. Adv Protein Chem. 2003;64:455–91.
  68. doi: 10.1016/S0065-3233(03)01013-1
  69. Sun E, He J, Zhuang X. Live cell imaging of viral entry. Curr Opin Virol. 2013 Feb;3(1):34–43. doi: 10.1016/j.coviro.2013.01.005
  70. Sung MH, McNally JG. Live cell imaging and systems biology. Wiley Interdiscip Rev Syst Biol Med. 2011 Mar;3(2):167–82. doi: 10.1002/wsbm.108
  71. Tam J, Merino D. Stochastic optical reconstruction microscopy (STORM) in comparison with stimulated emission depletion (STED) and other imaging methods. J Neurochem. 2015 Nov;135(4):643–58. doi: 10.1111/jnc.13257
  72. Tang CY, Yang Z.
  73. Transmission electron microscopy (TEM). In: Membrane Characterization. 2017. p. 145–59. doi: 10.1016/B978-0-444-63776-5.00008-5
  74. Timmermans FJ, Otto C. Contributed review: Review of integrated correlative light and electron microscopy. Rev Sci Instrum. 2015 Jan;86(1). doi: 10.1063/1.4905434
  75. Trache A, Meininger GA. Total internal reflection fluorescence (TIRF) microscopy. Curr Protoc Microbiol. 2008 Aug;10(1):2A.2.1–22. doi: 10.1002/9780471729259.mc02a02s10
  76. Turk M, Baumeister W. The promise and the challenges of cryo-electron tomography. FEBS Lett. 2020 Oct;594(20):3243–61. doi: 10.1002/1873-3468.13948
  77. Van den Dries K, Fransen J, Cambi A. Fluorescence CLEM in biology: historic developments and current super-resolution applications. FEBS Lett. 2022 Oct;596(19):2486–96. doi: 10.1002/1873-3468.14421
  78. doi: 10.1002/1873-3468.14421
  79. Vicidomini G, Bianchini P, Diaspro A. STED super-resolved microscopy. Nat Methods. 2018 Mar;15(3):173–82. doi: 10.1038/nmeth.4593
  80. Wang IH, Burckhardt CJ, Yakimovich A, Greber UF. Imaging, Tracking and Computational Analyses of Virus Entry and Egress with the Cytoskeleton. Viruses. 2018 Mar 31;10(4):166 doi: 10.3390/v10040166. PMID: 29614729; PMCID: PMC5923460.
  81. Wirtz T, De Castro O, Audinot JN, Philipp P. Imaging and analytics on the helium ion microscope. Annu Rev Anal Chem. 2019 Jun;12:523–43.
  82. doi: 10.1146/annurev-anchem-061318-115457
  83. Witte R, Andriasyan V, Georgi F, Yakimovich A, Greber UF. Concepts in Light Microscopy of Viruses. Viruses. 2018 Apr 18;10(4):202. doi: 10.3390/v10040202. PMID: 29670029; PMCID: PMC5923496.
  84. Wolff G, Bárcena M. Multiscale electron microscopy for the study of viral replication organelles. Viruses. 2021 Feb;13(2):197. doi: 10.3390/v13020197
  85. Xu CS, et al. Enhanced FIB-SEM systems for large-volume 3D imaging. Elife. 2017 May;6:e25916. doi: 10.7554/elife.25916
  86. Yi H, et al. Native immunogold labeling of cell surface proteins and viral glycoproteins for cryo-electron microscopy and cryo-electron tomography applications. J Histochem Cytochem. 2015 Oct;63(10):780–92. doi: 10.1369/0022155415593323
  87. Zhong H. Photoactivated localization microscopy (PALM): An optical technique for achieving ~10-nm resolution. Cold Spring Harb Protoc. 2010 Dec;2010(12):pdb.top91. doi: 10.1101/pdb.top91
  88. Zhou W, Apkarian R, Wang ZL, Joy D. Fundamentals of scanning electron microscopy (SEM). In: Scanning Microscopy for Nanotechnology: Techniques and Applications. 2006. p. 1–40. doi: 10.1007/978-0-387-39620-0_1

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