1887

Abstract

imaging is a noninvasive method that enables real-time monitoring of viral infection dynamics in a small animal, which allows a better understanding of viral pathogenesis. bioluminescence imaging of virus infection is widely used but, despite its advantage over bioluminescence that no substrate administration is required, fluorescence imaging is not used because of severe autofluorescence. Recently, several far-red and near-infrared (NIR) fluorescent proteins (FPs) have been developed and shown to be useful for whole-body fluorescence imaging. Here, we report comparative testing of far-red and NIR FPs in the imaging of rabies virus (RABV) infection. Using the highly neuroinvasive 1088 strain, we generated recombinant RABV that expressed FPs such as Katushka2S, E2-Crimson, iRFP670 or iRFP720. After intracerebral inoculation to nude mice, the 1088 strain expressing iRFP720, the most red-shifted FP, was detected the earliest with the highest signal-to-noise ratio using a filter set for >700 nm, in which the background signal level was very low. Furthermore, we could also track viral dissemination from the spinal cord to the brain in nude mice after intramuscular inoculation of iRFP720-expressing 1088 into the hind limb. Hence, we conclude that the NIR FP iRFP720 used with a filter set for >700 nm is useful for fluorescence imaging not only for RABV infection but also for other virus infections. Our findings will also be useful for developing dual-optical imaging of virus–host interaction dynamics using bioluminescence reporter mice for inflammation imaging.

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2017-11-01
2024-03-29
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References

  1. Cook SH, Griffin DE. Luciferase imaging of a neurotropic viral infection in intact animals. J Virol 2003; 77:5333–5338 [View Article][PubMed]
    [Google Scholar]
  2. Mehle A. Fiat Luc: bioluminescence imaging reveals in vivo viral replication dynamics. PLoS Pathog 2015; 11:e1005081 [View Article][PubMed]
    [Google Scholar]
  3. Tran V, Poole DS, Jeffery JJ, Sheahan TP, Creech D et al. Multi-modal imaging with a toolbox of influenza A reporter viruses. Viruses 2015; 7:5319–5327 [View Article][PubMed]
    [Google Scholar]
  4. Frangioni JV. In vivo near-infrared fluorescence imaging. Curr Opin Chem Biol 2003; 7:626–634 [View Article][PubMed]
    [Google Scholar]
  5. Weissleder R. A clearer vision for in vivo imaging. Nat Biotechnol 2001; 19:316–317 [View Article][PubMed]
    [Google Scholar]
  6. Amiot CL, Xu S, Liang S, Pan L, Zhao JX. Near-infrared fluorescent materials for sensing of biological targets. Sensors 2008; 8:3082–3105 [View Article][PubMed]
    [Google Scholar]
  7. Hong G, Antaris AL, Dai H. Near-infrared fluorophores for biomedical imaging. Nat Biomed Eng 2017; 1:0010 [View Article]
    [Google Scholar]
  8. Luker KE, Pata P, Shemiakina II, Pereverzeva A, Stacer AC et al. Comparative study reveals better far-red fluorescent protein for whole body imaging. Sci Rep 2015; 5:10332 [View Article][PubMed]
    [Google Scholar]
  9. Shcherbo D, Merzlyak EM, Chepurnykh TV, Fradkov AF, Ermakova GV et al. Bright far-red fluorescent protein for whole-body imaging. Nat Methods 2007; 4:741–746 [View Article][PubMed]
    [Google Scholar]
  10. Strack RL, Hein B, Bhattacharyya D, Hell SW, Keenan RJ et al. A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling. Biochemistry 2009; 48:8279–8281 [View Article][PubMed]
    [Google Scholar]
  11. Barbier M, Damron FH. Rainbow vectors for broad-range bacterial fluorescence labeling. PLoS One 2016; 11:e0146827 [View Article][PubMed]
    [Google Scholar]
  12. Shcherbakova DM, Verkhusha VV. Near-infrared fluorescent proteins for multicolor in vivo imaging. Nat Methods 2013; 10:751–754 [View Article][PubMed]
    [Google Scholar]
  13. Mifune K, Makino Y, Mannen K. Susceptibility of various cell lines to rabies virus. Japan J Trop Med Hyg 1979; 7:201–208 [View Article]
    [Google Scholar]
  14. Yamada K, Park CH, Noguchi K, Kojima D, Kubo T et al. Serial passage of a street rabies virus in mouse neuroblastoma cells resulted in attenuation: potential role of the additional N-glycosylation of a viral glycoprotein in the reduced pathogenicity of street rabies virus. Virus Res 2012; 165:34–45 [View Article][PubMed]
    [Google Scholar]
  15. Mebatsion T, Schnell MJ, Cox JH, Finke S, Conzelmann KK. Highly stable expression of a foreign gene from rabies virus vectors. Proc Natl Acad Sci USA 1996; 93:7310–7314 [View Article][PubMed]
    [Google Scholar]
  16. Ceccaldi PE, Fayet J, Conzelmann KK, Tsiang H. Infection characteristics of rabies virus variants with deletion or insertion in the pseudogene sequence. J Neurovirol 1998; 4:115–119 [View Article][PubMed]
    [Google Scholar]
  17. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE et al. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 2004; 22:1567–1572 [View Article][PubMed]
    [Google Scholar]
  18. Nogales A, Baker SF, Martínez-Sobrido L. Replication-competent influenza A viruses expressing a red fluorescent protein. Virology 2015; 476:206–216 [View Article][PubMed]
    [Google Scholar]
  19. Spronken MI, Short KR, Herfst S, Bestebroer TM, Vaes VP et al. Optimisations and challenges involved in the creation of various bioluminescent and fluorescent influenza A virus strains for in vitro and in vivo applications. PLoS One 2015; 10:e0133888 [View Article][PubMed]
    [Google Scholar]
  20. Dietzschold B, Wunner WH, Wiktor TJ, Lopes AD, Lafon M et al. Characterization of an antigenic determinant of the glycoprotein that correlates with pathogenicity of rabies virus. Proc Natl Acad Sci USA 1983; 80:70–74 [View Article][PubMed]
    [Google Scholar]
  21. Yang C, Jackson AC. Basis of neurovirulence of avirulent rabies virus variant Av01 with stereotaxic brain inoculation in mice. J Gen Virol 1992; 73:895–900 [View Article][PubMed]
    [Google Scholar]
  22. Ito N, Takayama M, Yamada K, Sugiyama M, Minamoto N. Rescue of rabies virus from cloned cDNA and identification of the pathogenicity-related gene: glycoprotein gene is associated with virulence for adult mice. J Virol 2001; 75:9121–9128 [View Article][PubMed]
    [Google Scholar]
  23. Faber M, Faber ML, Papaneri A, Bette M, Weihe E et al. A single amino acid change in rabies virus glycoprotein increases virus spread and enhances virus pathogenicity. J Virol 2005; 79:14141–14148 [View Article][PubMed]
    [Google Scholar]
  24. Takayama-Ito M, Inoue K, Shoji Y, Inoue S, Iijima T et al. A highly attenuated rabies virus HEP-Flury strain reverts to virulent by single amino acid substitution to arginine at position 333 in glycoprotein. Virus Res 2006; 119:208–215 [View Article][PubMed]
    [Google Scholar]
  25. Anindita PD, Sasaki M, Nobori H, Sato A, Carr M et al. Generation of recombinant rabies viruses encoding NanoLuc luciferase for antiviral activity assays. Virus Res 2016; 215:121–128 [View Article][PubMed]
    [Google Scholar]
  26. Luo J, Zhao J, Tian Q, Mo W, Wang Y et al. A recombinant rabies virus carrying GFP between N and P affects viral transcription in vitro . Virus Genes 2016; 52:379–387 [View Article][PubMed]
    [Google Scholar]
  27. Lemon K, de Vries RD, Mesman AW, McQuaid S, van Amerongen G et al. Early target cells of measles virus after aerosol infection of non-human primates. PLoS Pathog 2011; 7:e1001263 [View Article][PubMed]
    [Google Scholar]
  28. Rennick LJ, de Vries RD, Carsillo TJ, Lemon K, van Amerongen G et al. Live-attenuated measles virus vaccine targets dendritic cells and macrophages in muscle of nonhuman primates. J Virol 2015; 89:2192–2200 [View Article][PubMed]
    [Google Scholar]
  29. de Swart RL, de Vries RD, Rennick LJ, van Amerongen G, McQuaid S et al. Needle-free delivery of measles virus vaccine to the lower respiratory tract of non-human primates elicits optimal immunity and protection. NPJ Vaccines 2017; 2:22 [View Article]
    [Google Scholar]
  30. Luker KE, Luker GD. Bioluminescence imaging of reporter mice for studies of infection and inflammation. Antiviral Res 2010; 86:93–100 [View Article][PubMed]
    [Google Scholar]
  31. Ito N, Takayama-Ito M, Yamada K, Hosokawa J, Sugiyama M et al. Improved recovery of rabies virus from cloned cDNA using a vaccinia virus-free reverse genetics system. Microbiol Immunol 2003; 47:613–617 [View Article][PubMed]
    [Google Scholar]
  32. Yamada K, Noguchi K, Nonaka D, Morita M, Yasuda A et al. Addition of a single N-glycan to street rabies virus glycoprotein enhances virus production. J Gen Virol 2013; 94:270–275 [View Article][PubMed]
    [Google Scholar]
  33. Nishizono A, Khawplod P, Ahmed K, Goto K, Shiota S et al. A simple and rapid immunochromatographic test kit for rabies diagnosis. Microbiol Immunol 2008; 52:243–249 [View Article][PubMed]
    [Google Scholar]
  34. Schneider CA, Rasband WS, Eliceiri KW. NIH image to imageJ: 25 years of image analysis. Nat Methods 2012; 9:671–675 [View Article][PubMed]
    [Google Scholar]
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