Activity of BatIFIT5 in different species of healthy and naturally infected with rabies virus bats

Authors

  • Camila Mosca Barboza Instituto Pasteur, São Paulo, SP, Brazil; Universidade Federal do ABC (UFABC), Santo André, SP, Brazil
  • Juliana Santos Lima Instituto Pasteur, São Paulo, SP, Brazil; Universidade Federal do ABC (UFABC), Santo André, SP, Brazil
  • Bianca Ferreira Gomes Instituto Pasteur, São Paulo, SP, Brazil
  • Jaine Gonçalves Garcia Instituto Pasteur, São Paulo, SP, Brazil; Universidade Federal do ABC (UFABC), Santo André, SP, Brazil
  • Tatiane de Cássia Pardo Souza Instituto Pasteur, São Paulo, SP, Brazil
  • Raphaela Mello Zamudio Instituto Pasteur, São Paulo, SP, Brazil; Universidade Federal do ABC (UFABC), Santo André, SP, Brazil
  • Maria Eduarda Rodrigues Chierato Instituto Pasteur, São Paulo, SP, Brazil
  • Rafael de Novaes Oliveira Instituto Pasteur, São Paulo, SP, Brazil
  • Pedro Carnieli Junior Instituto Pasteur, São Paulo, SP, Brazil
  • Maria Cristina Carlan da Silva Universidade Federal do ABC, Santo André (UFABC), SP, Brazil
  • Willian Oliveira Fahl Instituto Pasteur, São Paulo, SP, Brazil
  • Enio Mori Instituto Pasteur, São Paulo, SP, Brazil
  • Karin Correa Scheffer Instituto Pasteur, São Paulo, SP, Brazil
  • Paulo Michel Roehe Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
  • Ana Claudia Franco Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
  • Helena Beatriz de Carvalho Ruthner Batista Instituto Pasteur, São Paulo, SP, Brazil; Universidade Federal do ABC (UFABC), Santo André, SP, Brazil

DOI:

https://doi.org/10.12834/VetIt.3427.23374.1

Keywords:

bats, batIFIT5, chiroptera, interferon, IFIT5, rabies

Abstract

Bats are mammals with vital role played in numerous ecosystem services, however bats can be important reservoirs or hosts for several microorganisms. Rabies is a zoonosis caused by Rabies lyssavirus (RABV) that affects the central nervous system (CNS) of all mammals, including bats and humans. The action of IFN-stimulated genes (ISGs) could be responsible for inhibiting different stages of the viral replication cycle. A major family of ISGs are the Interferon-induced proteins with tetrapeptide repeats (IFITs) and your action against infections caused by viruses from different families was proven. This study describes the expression of BatIFIT5 by RT-qPCR in different species of healthy and naturally infected with RABV bats. A total, of 36 bats were analyzed (18 positive and 18 negative for rabies) and 16 (44.44%) were positive for BatIFIT5. Here we analyzed fourteen species of bats with different eating and behavioral habits. Seven genetics lineages of RABV were evaluated and included in these 14 species of bats, no cases of RABV spillover were identified. In addition, we did not verified relationship between the bat species expression of BatIFIT5 and RABV. Many points about immunology of bats are unknown and here we analyzed one of these points.

References

Almeida, M. F., Rosa, A. R. D., Martorelli, L. F. A., Kataoka, A. P. A. G., & Aires, C. C. (2019). Rabies virus monitoring in bat populations in Rondônia state, Brazil. Revista da Sociedade Brasileira de Medicina Tropical, 52, e20180199. https://doi.org/10.1590/0037-8682-0199-2018

Barber, M. R., Aldridge, J. R., Jr, Fleming-Canepa, X., Wang, Y. D., Webster, R. G., & Magor, K. E. (2013). Identification of avian RIG-I responsive genes during influenza infection. Molecular immunology, 54(1), 89–97. https://doi.org/10.1016/j.molimm.2012.10.038

Bonilla-Aldana, D. K., Jimenez-Diaz, S. D., Arango-Duque, J. S., Aguirre-Florez, M., Balbin-Ramon, G. J., Paniz-Mondolfi, A., Suárez, J. A., Pachar, M. R., Perez-Garcia, L. A., Delgado-Noguera, L. A., Sierra, M. A., Muñoz-Lara, F., Zambrano, L. I., & Rodriguez-Morales, A. J. (2021). Bats in ecosystems and their Wide spectrum of viral infectious potential threats: SARS-CoV-2 and other emerging viruses. International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases, 102, 87–96. https://doi.org/10.1016/j.ijid.2020.08.050

Bowen, R. A., O'Shea, T. J., Shankar, V., Neubaum, M. A., Neubaum, D. J., & Rupprecht, C. E. (2013). Prevalence of neutralizing antibodies to rabies virus in serum of seven species of insectivorous bats from Colorado and New Mexico, United States. Journal of wildlife diseases, 49(2), 367–374. https://doi.org/10.7589/2012-05-124

Campos, A. C., Melo, F. L., Romano, C. M., Araujo, D. B., Cunha, E. M., Sacramento, D. R., de Andrade Zanotto, P. M., Durigon, E. L., & Favoretto, S. R. (2011). One-step protocol for amplification of near full-length cDNA of the rabies virus genome. Journal of virological methods, 174(1-2), 1–6. https://doi.org/10.1016/j.jviromet.2011.03.030

Carnieli, P., Jr, Fahl, W.deO., Castilho, J. G., Oliveira, R.deN., Macedo, C. I., Durymanova, E., Jorge, R. S., Morato, R. G., Spíndola, R. O., Machado, L. M., Ungar de Sá, J. E., Carrieri, M. L., & Kotait, I. (2008). Characterization of Rabies virus isolated from canids and identification of the main wild canid host in Northeastern Brazil. Virus research, 131(1), 33–46. https://doi.org/10.1016/j.virusres.2007.08.007

Costa, L. J. C., Martorelli, L. F. A., Barone, G. T., Rosa, E. S. T., Vasconcelos, P. F. C., Pereira, A. S., & Fernandes, M. E. B. (2017). Seroprevalence of rabies virus antibodies in bats from high risk areas in Brazilian Amazonia between 2013 and 2015. Transactions of the Royal Society of Tropical Medicine and Hygiene, 111(8), 363–369. https://doi.org/10.1093/trstmh/trx069

Dean, D.J.; Abelseth, M.K.; Athanasiu, P. The fluorescent antibody test. In Laboratory techniques in rabies; Meslin, F.X., Kaplan, M.M., Koprowski, H., Eds.; World Health Organization: Geneva, 1996.

Diamond, M. S., & Farzan, M. (2013). The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nature reviews. Immunology, 13(1), 46–57. https://doi.org/10.1038/nri3344

Feng, F., Yuan, L., Wang, Y. E., Crowley, C., Lv, Z., Li, J., Liu, Y., Cheng, G., Zeng, S., & Liang, H. (2013). Crystal structure and nucleotide selectivity of human IFIT5/ISG58. Cell research, 23(8), 1055–1058. https://doi.org/10.1038/cr.2013.80

Fensterl, V., & Sen, G. C. (2015). Interferon-induced Ifit proteins: their role in viral pathogenesis. Journal of virology, 89(5), 2462–2468. https://doi.org/10.1128/JVI.02744-14

Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular marine biology and biotechnology, 3(5), 294–299.

Goubau, D., Deddouche, S., & Reis e Sousa, C. (2013). Cytosolic sensing of viruses. Immunity, 38(5), 855–869. https://doi.org/10.1016/j.immuni.2013.05.007

Gregorin, R.; Taddei, V.A. Chave Artificial Para a Identificação de Molossídeos Brasileiros (Mammalia, Chiroptera). Mastozoología Neotrop. 2002, 9, 13–32.

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic acids symposium series, 41 (41), 95-98.

Han, H. J., Wen, H. L., Zhou, C. M., Chen, F. F., Luo, L. M., Liu, J. W., & Yu, X. J. (2015). Bats as reservoirs of severe emerging infectious diseases. Virus research, 205, 1–6. https://doi.org/10.1016/j.virusres.2015.05.006

ICTV Genus: Lyssavirus - Rhabdoviridae - Mononegavirales - International Committee on Taxonomy of Viruses (ICTV) Available online: https://talk.ictvonline.org/ictv-reports/ictv_online_report/negative-sense-rna viruses/mononegavirales/w/rhabdoviridae/795/genus-lyssavirus (accessed on 26 July 2021).

International, B.C. Conservation Progress in Latin America - Bat Conservation International Available online: https://www.batcon.org/article/conservation-progress-in-latin-america/ (accessed on 28 July 2021).

Jackson A. C. (2002). Rabies pathogenesis. Journal of neurovirology, 8(4), 267–269. https://doi.org/10.1080/13550280290100725

Jiang, Y., Wang, L., Lu, Z., Xuan, H., Han, X., Xia, X., Zhao, F., & Tu, C. (2010). Seroprevalence of rabies virus antibodies in bats from southern China. Vector borne and zoonotic diseases (Larchmont, N.Y.), 10(2), 177–181. https://doi.org/10.1089/vbz.2008.0212

Jones Jr, J. K., & Carter, D. C. (1976). Annotated checklist, with keys to subfamilies and genera. Biology of bats of the new world family Phyllostomidae, part I. Lubbock: Museum Texas Tech. University, 7-38.

Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L., & Daszak, P. (2008). Global trends in emerging infectious diseases. Nature, 451(7181), 990–993. https://doi.org/10.1038/nature06536

Kunz, T. H., Braun de Torrez, E., Bauer, D., Lobova, T., & Fleming, T. H. (2011). Ecosystem services provided by bats. Annals of the New York Academy of Sciences, 1223, 1–38. https://doi.org/10.1111/j.1749-6632.2011.06004.x

Li, J. J., Yin, Y., Yang, H. L., Yang, C. W., Yu, C. L., Wang, Y., Yin, H. D., Lian, T., Peng, H., Zhu, Q., & Liu, Y. P. (2020). mRNA expression and functional analysis of chicken IFIT5 after infected with Newcastle disease virus. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases, 86, 104585. https://doi.org/10.1016/j.meegid.2020.104585

Liu, Y., Zhang, Y. B., Liu, T. K., & Gui, J. F. (2013). Lineage-specific expansion of IFIT gene family: an insight into coevolution with IFN gene family. PloS one, 8(6), e66859. https://doi.org/10.1371/journal.pone.0066859

Martins, F. M., Templeton, A. R., Pavan, A. C., Kohlbach, B. C., & Morgante, J. S. (2009). Phylogeography of the common vampire bat (Desmodus rotundus): marked population structure, Neotropical Pleistocene vicariance and incongruence between nuclear and mtDNA markers. BMC evolutionary biology, 9, 294. https://doi.org/10.1186/1471-2148-9-294

Nowak, R.M. Walkers’ Mammals of the World; 6th ed.; Johns Hopkins University Press: Baltimore, 1999.

Oliveira, R. de N., de Souza, S. P., Lobo, R. S., Castilho, J. G., Macedo, C. I., Carnieli, P., Jr, Fahl, W. O., Achkar, S. M., Scheffer, K. C., Kotait, I., Carrieri, M. L., & Brandão, P. E. (2010). Rabies virus in insectivorous bats: implications of the diversity of the nucleoprotein and glycoprotein genes for molecular epidemiology. Virology, 405(2), 352–360. https://doi.org/10.1016/j.virol.2010.05.030

O'Shea, T. J., Bowen, R. A., Stanley, T. R., Shankar, V., & Rupprecht, C. E. (2014). Variability in seroprevalence of rabies virus neutralizing antibodies and associated factors in a Colorado population of big brown bats (Eptesicus fuscus). PloS one, 9(1), e86261. https://doi.org/10.1371/journal.pone.0086261

Santhakumar, D., Rohaim, M. A. M. S., Hussein, H. A., Hawes, P., Ferreira, H. L., Behboudi, S., Iqbal, M., Nair, V., Arns, C. W., & Munir, M. (2018). Chicken Interferon-induced Protein with Tetratricopeptide Repeats 5 Antagonizes Replication of RNA Viruses. Scientific reports, 8(1), 6794. https://doi.org/10.1038/s41598-018-24905-y

Seetahal, J. F. R., Greenberg, L., Satheshkumar, P. S., Sanchez-Vazquez, M. J., Legall, G., Singh, S., Ramkissoon, V., Schountz, T., Munster, V., Oura, C. A. L., & Carrington, C. V. F. (2020). The Serological Prevalence of Rabies Virus-Neutralizing Antibodies in the Bat Population on the Caribbean Island of Trinidad. Viruses, 12(2), 178. https://doi.org/10.3390/v12020178

Seidlova, V., Zukal, J., Brichta, J., Anisimov, N., Apoznański, G., Bandouchova, H., Bartonička, T., Berková, H., Botvinkin, A. D., Heger, T., Dundarova, H., Kokurewicz, T., Linhart, P., Orlov, O. L., Piacek, V., Presetnik, P., Shumkina, A. P., Tiunov, M. P., Treml, F., & Pikula, J. (2020). Active surveillance for antibodies confirms circulation of lyssaviruses in Palearctic bats. BMC veterinary research, 16(1), 482. https://doi.org/10.1186/s12917-020-02702-y

Soares, R. M., Bernardi, F., Sakamoto, S. M., Heinemann, M. B., Cortez, A., Alves, L. M., Meyer, A. D., Ito, F. H., & Richtzenhain, L. J. (2002). A heminested polymerase chain reaction for the detection of Brazilian rabies isolates from vampire bats and herbivores. Memorias do Instituto Oswaldo Cruz, 97(1), 109–111. https://doi.org/10.1590/s0074-02762002000100019

Springer, M. S., Teeling, E. C., Madsen, O., Stanhope, M. J., & de Jong, W. W. (2001). Integrated fossil and molecular data reconstruct bat echolocation. Proceedings of the National Academy of Sciences of the United States of America, 98(11), 6241–6246. https://doi.org/10.1073/pnas.111551998

Stetson, D. B., & Medzhitov, R. (2006). Type I interferons in host defense. Immunity, 25(3), 373–381. https://doi.org/10.1016/j.immuni.2006.08.007

Tamura K. (1992). Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular biology and evolution, 9(4), 678–687. https://doi.org/10.1093/oxfordjournals.molbev.a040752

Tamura, K., & Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular biology and evolution, 10(3), 512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023

Teeling, E. C., Madsen, O., Van den Bussche, R. A., de Jong, W. W., Stanhope, M. J., & Springer, M. S. (2002). Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats. Proceedings of the National Academy of Sciences of the United States of America, 99(3), 1431–1436. https://doi.org/10.1073/pnas.022477199

Teeling, E. C., Scally, M., Kao, D. J., Romagnoli, M. L., Springer, M. S., & Stanhope, M. J. (2000). Molecular evidence regarding the origin of echolocation and flight in bats. Nature, 403(6766), 188–192. https://doi.org/10.1038/35003188

Teeling, E. C., Springer, M. S., Madsen, O., Bates, P., O'brien, S. J., & Murphy, W. J. (2005). A molecular phylogeny for bats illuminates biogeography and the fossil record. Science (New York, N.Y.), 307(5709), 580–584. https://doi.org/10.1126/science.1105113

Thirumal Kumar, D., Mendonca, E., Priyadharshini Christy, J., George Priya Doss, C., & Zayed, H. (2019). A computational model to predict the structural and functional consequences of missense mutations in O6-methylguanine DNA methyltransferase. Advances in protein chemistry and structural biology, 115, 351–369. https://doi.org/10.1016/bs.apcsb.2018.11.006

Vizzoto, L.; Taddei, V. Chave Para a Determinação de Quirópteros Brasileiros; Gráfica Francal: São José do Rio Preto, 1973.

Wang, B., Chen, Y., Mu, C., Su, Y., Liu, R., Huang, Z., Li, Y., Yu, Q., Chang, G., Xu, Q., & Chen, G. (2015). Identification and expression analysis of the interferon-induced protein with tetratricopeptide repeats 5 (IFIT5) gene in duck (Anas platyrhynchos domesticus). PloS one, 10(3), e0121065. https://doi.org/10.1371/journal.pone.0121065

WHO Expert Consultation on Rabies: Third Report; WHO technical report series;1012; World Health Organization, 2018.

Wynne, J. W., & Wang, L. F. (2013). Bats and viruses: friend or foe?. PLoS pathogens, 9(10), e1003651. https://doi.org/10.1371/journal.ppat.1003651

Zhang, B., Liu, X., Chen, W., & Chen, L. (2013). IFIT5 potentiates anti-viral response through enhancing innate immune signaling pathways. Acta biochimica et biophysica Sinica, 45(10), 867–874. https://doi.org/10.1093/abbs/gmt088

Downloads

Published

2024-07-31

How to Cite

Mosca Barboza, C., Santos Lima, J., Ferreira Gomes, B., Gonçalves Garcia , J., Pardo Souza, T. de C., Mello Zamudio, R., … de Carvalho Ruthner Batista, H. B. . (2024). Activity of BatIFIT5 in different species of healthy and naturally infected with rabies virus bats. Veterinaria Italiana, 60(2). https://doi.org/10.12834/VetIt.3427.23374.1

Issue

Vol. 60 No. 2 (2024)

Section

Paper

License

Copyright (c) 2024 Camila Mosca Barboza, Juliana Santos Lima, Bianca Ferreira Gomes, Jaine Gonçalves Garcia , Tatiane de Cássia Pardo Souza, Raphaela Mello Zamudio, Maria Eduarda Rodrigues Chierato, Rafael de Novaes Oliveira , Pedro Carnieli Junior, Maria Cristina Carlan da Silva , Willian Oliveira Fahl, Enio Mori, Karin Correa Scheffer, Paulo Michel Roehe, Ana Claudia Franco, Helena Beatriz de Carvalho Ruthner Batista

Similar Articles

You may also start an advanced similarity search for this article.