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Brain-wide N2cG compensation permits glycoprotein-deleted rabies virus to trace neural circuits across multiple synapses

    https://doi.org/10.1142/S1793545823400011Cited by:1 (Source: Crossref)

    Rabies-viruses-based retrograde tracers can spread across multiple synapses in a retrograde direction in the nervous system of rodents and primates, making them powerful tools for determining the structure and function of the complicated neural circuits of the brain. However, they have some limitations, such as posing high risks to human health and the inability to retrograde trans-synaptic label inputs from genetically-defined starter neurons. Here, we established a new retrograde trans-multi-synaptic tracing method through brain-wide rabies virus glycoprotein (RVG) compensation, followed by glycoprotein-deleted rabies virus (RV-ΔG) infection in specific brain regions. Furthermore, in combination with the avian tumor virus receptor A (TVA) controlled by a cell-type-specific promoter, we found that EnvA-pseudotyped RV-ΔG can mediate efficient retrograde trans-multi-synaptic transduction from cell-type-specific starter neurons. This study provides new alternative methods for neuroscience researchers to analyze the input neural networks of rodents and nonhuman primates.

    References

    • 1. T. R. Insel , “Rethinking schizophrenia,” Nature 468, 187–193 (2010). Crossref, Web of ScienceGoogle Scholar
    • 2. K. Lin, X. Zhong, M. Ying, L. Li, S. Tao, X. Zhu, X. He, F. Xu , “A mutant vesicular stomatitis virus with reduced cytotoxicity and enhanced anterograde trans-synaptic efficiency,” Mol. Brain 13, 45 (2020). Crossref, Web of ScienceGoogle Scholar
    • 3. Z. Han, N. Luo, J. Kou, L. Li, W. Ma, S. Peng, Z. Xu, W. Zhang, Y. Qiu, Y. Wu, J. Wang, C. Ye, K. Lin, F. Xu, “AAV11 permits efficient retrograde targeting of projection neurons,” bioRxiv (2022). Google Scholar
    • 4. A. R. Weiss, W. A. Liguore, J. S. Domire, D. Button, J. L. McBride , “Intra-striatal AAV2.retro administration leads to extensive retrograde transport in the rhesus macaque brain: Implications for disease modeling and therapeutic development,” Sci. Rep. 10, 6970 (2020). Crossref, Web of ScienceGoogle Scholar
    • 5. Z. Han, N. Luo, J. Kou, L. Li, Z. Xu, S. Wei, Y. Wu, J. Wang, C. Ye, K. Lin, F. Xu , “Brain-wide TVA compensation allows rabies virus to retrograde target cell-type-specific projection neurons,” Mol. Brain 15, 13 (2022). Crossref, Web of ScienceGoogle Scholar
    • 6. D. G. Tervo, B. Y. Hwang, S. Viswanathan, T. Gaj, M. Lavzin, K. D. Ritola, S. Lindo, S. Michael, E. Kuleshova, D. Ojala, C. C. Huang, C. R. Gerfen, J. Schiller, J. T. Dudman, A. W. Hantman, L. L. Looger, D. V. Schaffer, A. Y. Karpova , “A designer AAV variant permits efficient retrograde access to projection neurons,” Neuron 92, 372–382 (2016). Crossref, Web of ScienceGoogle Scholar
    • 7. J. Tordo, C. O’Leary, A. Antunes, N. Palomar, P. Aldrin-Kirk, M. Basche, A. Bennett, Z. D’Souza, H. Gleitz, A. Godwin, R. J. Holley, H. Parker, A. Y. Liao, P. Rouse, A. S. Youshani, L. Dridi, C. Martins, T. Levade, K. B. Stacey, D. M. Davis, A. Dyer, N. Clement, T. Bjorklund, R. R. Ali, M. Agbandje-McKenna, A. A. Rahim, A. Pshezhetsky, S. N. Waddington, R. M. Linden, B. W. Bigger, E. Henckaerts , “A novel adeno-associated virus capsid with enhanced neurotropism corrects a lysosomal transmembrane enzyme deficiency,” Brain J. Neurol. 141, 2014–2031 (2018). Crossref, Web of ScienceGoogle Scholar
    • 8. K. Lin, X. Zhong, L. Li, M. Ying, T. Yang, Z. Zhang, X. He, F. Xu , “AAV9-Retro mediates efficient transduction with axon terminal absorption and blood-brain barrier transportation,” Mol. Brain 13, 138 (2020). Crossref, Web of ScienceGoogle Scholar
    • 9. S. Tanabe, K. I. Inoue, H. Tsuge, S. Uezono, K. Nagaya, M. Fujiwara, S. Kato, K. Kobayashi, M. Takada , “The use of an optimized chimeric envelope glycoprotein enhances the efficiency of retrograde gene transfer of a pseudotyped lentiviral vector in the primate brain,” Neurosci. Res. 120, 45–52 (2017). Crossref, Web of ScienceGoogle Scholar
    • 10. S. J. Li, A. Vaughan, J. F. Sturgill, A. Kepecs , “A viral receptor complementation strategy to overcome CAV-2 tropism for efficient retrograde targeting of neurons,” Neuron 98, 905–917 e5 (2018). Crossref, Web of ScienceGoogle Scholar
    • 11. E. M. Callaway, L. Luo , “Monosynaptic circuit tracing with glycoprotein-deleted rabies viruses,” J. Neurosci. 35, 8979–8985 (2015). Crossref, Web of ScienceGoogle Scholar
    • 12. P. Su, M. Ying, Z. Han, J. Xia, S. Jin, Y. Li, H. Wang, F. Xu , “High-brightness anterograde transneuronal HSV1 H129 tracer modified using a Trojan horse-like strategy,” Mol. Brain 13, 5 (2020). Crossref, Web of ScienceGoogle Scholar
    • 13. G. E. Pickard, C. A. Smeraski, C. C. Tomlinson, B. W. Banfield, J. Kaufman, C. L. Wilcox, L. W. Enquist, P. J. Sollars , “Intravitreal injection of the attenuated pseudorabies virus PRV Bartha results in infection of the hamster suprachiasmatic nucleus only by retrograde transsynaptic transport via autonomic circuits,” J. Neurosci. 22, 2701–2710 (2002). Crossref, Web of ScienceGoogle Scholar
    • 14. L. A. Schwarz, K. Miyamichi, X. J. Gao, K. T. Beier, B. Weissbourd, K. E. DeLoach, J. Ren, S. Ibanes, R. C. Malenka, E. J. Kremer, L. Luo , “Viral-genetic tracing of the input-output organization of a central noradrenaline circuit,” Nature 524, 88–92 (2015). Crossref, Web of ScienceGoogle Scholar
    • 15. Q. Liu, Y. Wu, H. Wang, F. Jia, F. Xu , “Viral tools for neural circuit tracing,” Neurosci. Bull. 38(12), 1508–1518 (2022). Crossref, Web of ScienceGoogle Scholar
    • 16. E. M. Callaway , “Transneuronal circuit tracing with neurotropic viruses,” Curr. Opin. Neurobiol. 18, 617–623 (2008). Crossref, Web of ScienceGoogle Scholar
    • 17. S. Ohara, K. Inoue, M. P. Witter, T. Iijima , “Untangling neural networks with dual retrograde transsynaptic viral infection,” Front. Neurosci. 3, 344–349 (2009). Crossref, Web of ScienceGoogle Scholar
    • 18. F. Jia, P. Lv, H. Miao, X. W. Shi, H. J. Mei, L. Li, X. Q. Xu, S. J. Tao, F. Q. Xu , “Optimization of the fluorescent protein expression level based on pseudorabies virus bartha strain for neural circuit tracing,” Front. Neuroanat. 13, 63 (2019). Crossref, Web of ScienceGoogle Scholar
    • 19. J. DeFalco, M. Tomishima, H. Y. Liu, C. Zhao, X. L. Cai, J. D. Marth, L. Enquist, J. M. Friedman , “Virus-assisted mapping of neural inputs to a feeding center in the hypothalamus,” Science 291, 2608–2613 (2001). Crossref, Web of ScienceGoogle Scholar
    • 20. L. Sun, Y. Tang, K. Yan, J. Yu, Y. Zou, W. Xu, K. Xiao, Z. Zhang, W. Li, B. Wu, Z. Hu, K. Chen, Z. F. Fu, J. Dai, G. Cao , “Differences in neurotropism and neurotoxicity among retrograde viral tracers,” Mol. Neurodegener. 14, 8 (2019). Crossref, Web of ScienceGoogle Scholar
    • 21. I. R. Wickersham, D. C. Lyon, R. J. Barnard, T. Mori, S. Finke, K. K. Conzelmann, J. A. Young, E. M. Callaway , “Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons,” Neuron 53, 639–647 (2007). Crossref, Web of ScienceGoogle Scholar
    • 22. I. R. Wickersham, S. Finke, K. K. Conzelmann, E. M. Callaway , “Retrograde neuronal tracing with a deletion-mutant rabies virus,” Nat. Meth. 4, 47–49 (2007). Crossref, Web of ScienceGoogle Scholar
    • 23. T. R. Reardon, A. J. Murray, G. F. Turi, C. Wirblich, K. R. Croce, M. J. Schnell, T. M. Jessell, A. Losonczy , “Rabies virus CVS-N2c(DeltaG) strain enhances retrograde synaptic transfer and neuronal viability,” Neuron 89, 711–724 (2016). Crossref, Web of ScienceGoogle Scholar
    • 24. K. Lin, L. Li, W. Ma, X. Yang, Z. Han, N. Luo, F. Xu, “A rabies virus-based toolkit for efficient retrograde labeling and monosynaptic tracing,” Neural. Regen. Res. 18, 1827–1833 (2023). Google Scholar
    • 25. Y. H. Chen, M. S. Keiser, B. L. Davidson , “Adeno-associated virus production, purification, and titering,” Curr. Protoc. Mouse Biol. 8, e56 (2018). CrossrefGoogle Scholar
    • 26. G. Paxinos, K. Franklin , Paxinos and Franklin’s the Mouse Brain in Stereotaxic Coordinates, Elsevier/Academic Press, Amsterdam (2012). Google Scholar
    • 27. K. T. Beier, A. Saunders, I. A. Oldenburg, K. Miyamichi, N. Akhtar, L. Luo, S. P. Whelan, B. Sabatini, C. L. Cepko , “Anterograde or retrograde transsynaptic labeling of CNS neurons with vesicular stomatitis virus vectors,” Proc. Natl. Acad. Sci. USA 108, 15414–15419 (2011). Crossref, Web of ScienceGoogle Scholar
    • 28. K. T. Beier, A. B. Saunders, I. A. Oldenburg, B. L. Sabatini, C. L. Cepko , “Vesicular stomatitis virus with the rabies virus glycoprotein directs retrograde transsynaptic transport among neurons in vivo,” Front. Neural Circuits 7, 11 (2013). Crossref, Web of ScienceGoogle Scholar
    • 29. R. M. Kelly, P. L. Strick , “Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate,” J. Neurosci. 23, 8432–8444 (2003). Crossref, Web of ScienceGoogle Scholar
    • 30. E. Hoshi, L. Tremblay, J. Féger, P. L. Carras, P. L. Strick , “The cerebellum communicates with the basal ganglia,” Nat. Neurosci. 8, 1491–1493 (2005). Crossref, Web of ScienceGoogle Scholar
    • 31. S. Ohara, Y. Sota, S. Sato, K. I. Tsutsui, T. Iijima , “Increased transgene expression level of rabies virus vector for transsynaptic tracing,” PLoS One 12, e0180960 (2017). Crossref, Web of ScienceGoogle Scholar
    • 32. D. Goertsen, N. C. Flytzanis, N. Goeden, M. R. Chuapoco, A. Cummins, Y. Chen, Y. Fan, Q. Zhang, J. Sharma, Y. Duan, L. Wang, G. Feng, Y. Chen, N. Y. Ip, J. Pickel, V. Gradinaru , “AAV capsid variants with brain-wide transgene expression and decreased liver targeting after intravenous delivery in mouse and marmoset,” Nat. Neurosci. 25, 106–115 (2022). Crossref, Web of ScienceGoogle Scholar
    • 33. Y. Yao, J. Wang, Y. Liu, Y. Qu, K. Wang, Y. Zhang, Y. Chang, Z. Yang, J. Wan, J. Liu, H. Nakashima, S. E. Lawler, E. A. Chiocca, C. F. Cho, F. Bei , “Variants of the adeno-associated virus serotype 9 with enhanced penetration of the blood–brain barrier in rodents and primates,” Nat. Biomed. Eng. 6, 1257–1271 (2022). Crossref, Web of ScienceGoogle Scholar