Bats Oxidative Stress Defense

Authors

  • Desrayni Hanadhita Department of Anatomy Physiology and Pharmacology, Faculty of Veterinary Medicine, IPB University
  • Aryani Sismin Satyaningtijas Department of Anatomy Physiology and Pharmacology, Faculty of Veterinary Medicine, IPB University
  • Srihadi Agungpriyono Department of Anatomy Physiology and Pharmacology, Faculty of Veterinary Medicine, IPB University

Keywords:

aging, animal model, antioxidant, comparative physiology, free radical

Abstract

Antioxidants and free radicals have long been known to be the main factors in the occurrence of degenerative diseases. Various studies related to antioxidants and free radicals which have implications for oxidative stress have increased in the last decade. Knowledge of stress oxidative physiology in various animals help in understanding the pathophysiology of diseases associated with oxidative stress. Bats are claimed to be the best known animals in term of survival compared to other mammals. Bats are reported to produce low reactive oxygen species (ROS) but high endogenous antioxidants that can prevent oxidative stress. Bats high defense against oxidative stress has implications for their extreme longevity, the role as a reservoir of viruses, and the potential as experimental animals.

References

Altringham, J. D. (2011). Bats from Evolution to Conservation (Second Edi). Oxford: Oxford University Press.

Anindita, P. D., Sasaki, M., Setiyono, A., Handharyani, E., Orba, Y., Kobayashi, S., … Kimura, T. (2015). Detection of coronavirus genomes in Moluccan naked-backed fruit bats in Indonesia. Archives of Virology, 160(4), 1113–1118. https://doi.org/10.1007/s00705-015-2342-1

Ball, H. C., levari-Shariati, S., Cooper, L. N., & Aliani, M. (2018). Comparative metabolomics of aging in a long-lived bat: Insights into the physiology of extreme longevity. PLoS ONE, 13(5), 1–20. https://doi.org/10.1371/journal.pone.0196154

Basri, C., Arifin, E. M. Z., Takemae, H., Hengjan, Y., Iida, K., Sudarnika, E., … Hondo, E. (2017). Potential risk of viral transmission from flying foxes to domestic animals and humans on the southern coast of West Java, Indonesia. Journal of Veterinary Medical Science, 79(9), 1615–1626. https://doi.org/10.1292/jvms.17-0222

Birben, E., Sahiner, U. M., Sackesen, C., Erzurum, S., & Kalayci, O. (2012). Oxidative Stress and Antioxidant Defense. World Allergy Organization Journal, 5(1), 9–19. https://doi.org/10.1097/WOX.0b013e3182439613

Breed, A. C., Field, H. E., Smith, C. S., Edmonston, J., & Meers, J. (2010). Bats without borders: Long-distance movements and implications for disease risk management. EcoHealth, 7(2), 204–212. https://doi.org/10.1007/s10393-010-0332-z

Brown, J. C. L., McClelland, G. B., Faure, P. A., Klaiman, J. M., & Staples, J. F. (2009). Examining the mechanisms responsible for lower ROS release rates in liver mitochondria from the long-lived house sparrow (Passer domesticus) and big brown bat (Eptesicus fuscus) compared to the short-lived mouse (Mus musculus). Mechanisms of Ageing and Development, 130(8), 467–476. https://doi.org/10.1016/j.mad.2009.05.002

Brunet-Rossinni, A. K. (2004). Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifugus) versus two non-flying mammals. Mechanisms of Ageing and Development, 125(1), 11–20. https://doi.org/10.1016/j.mad.2003.09.003

Brunet-Rossinni, A. K., & Austad, S. N. (2004). Ageing studies on bats: A review. Biogerontology, 5(4), 211–222. https://doi.org/10.1023/B:BGEN.0000038022.65024.d8

Buffenstein, R., Edrey, Y. H., Yang, T., & Mele, J. (2008). The oxidative stress theory of aging: Embattled or invincible? Insights from non-traditional model organisms. Age, 30(2–3), 99–109. https://doi.org/10.1007/s11357-008-9058-z

Calisher, C. H., Childs, J. E., Field, H. E., Holmes, K. V, & Schountz, T. (2006). Bats: Important reservoir hosts of emerging viruses. Clinical Microbiology Reviews, 19(3), 531–545. https://doi.org/10.1128/CMR.00017-06

Crameri, G., Todd, S., Grimley, S., McEachern, J. A., Marsh, G. A., Smith, C., … Wang, L. F. (2009). Establishment, immortalisation and characterisation of pteropid bat cell lines. PLoS ONE, 4(12). https://doi.org/10.1371/journal.pone.0008266

Crichton, E. G., & Krutzsch, P. H. (2000). Reproductive Biology of Bats. (E. G. Crichton & P. H. Krutzsch, Eds.). London: Academic Press. https://doi.org/10.1017/CBO9781107415324.004

Dharmayanti, N., & Sendow, I. (2015). Ebola : Penyakit Eksotik Zoonosis yang Perlu Diwaspadai. Wartazoa, 25(1), 29–38. https://doi.org/10.14334/wartazoa.v25i1.1126

Filho, D. W., Althoff, S. L., Dafré, A. L., & Boveris, A. (2007). Antioxidant defenses, longevity and ecophysiology of South American bats. Comparative Biochemistry and Physiology - C Toxicology and Pharmacology, 146(1–2 SPEC. ISS.), 214–220. https://doi.org/10.1016/j.cbpc.2006.11.015

Fukai, T., & Ushio-Fukai, M. (2011). Superoxide Dismutases: Role in Redox Signaling, Vascular Function, and Diseases. Antioxidants & Redox Signaling, 15(6), 1583–1606. https://doi.org/10.1089/ars.2011.3999

Galván, I., Garrido-Fernández, J., Ríos, J., Pérez-Gálvez, A., Rodríguez-Herrera, B., & Negro, J. J. (2016). Tropical bat as mammalian model for skin carotenoid metabolism. Proceedings of the National Academy of Sciences, 113(39), 10932–10937. https://doi.org/10.1073/pnas.1609724113

Grotto, D., Santa Maria, L., Valentini, J., Paniz, C., Schmitt, G., Garcia, S. C., … Farina, M. (2009). Importance of the lipid peroxidation biomarkers and methodological aspects for malondialdehyde quantification. Quimica Nova, 32(1), 169–174. https://doi.org/10.1590/S0100-40422009000100032

Gullberg, R. C., Steel, J. J., Moon, S. L., Soltani, E., & Geiss, B. J. (2015). Oxidative stress influences positive strand RNA virus genome synthesis and capping. Virology, 475, 212–229. https://doi.org/10.1038/jid.2014.371

Hanadhita, D., Rahma, A., Prawira, A. Y., Satjaningtyas, A. S., & Agungpriyono, S. (2017). Comparison of Oxidative Stress Status between Lesser Short Nosed Bat ( Cynopterus brachyotis ) and Laboratory Rat ( Rattus Norvegicus ) Related to Their Longevity. In International Scientific Symposium (pp. 17–18). Bogor.

Hanadhita, D., Rahma, A., Prawira, A. Y., Sismin Satyaningtijas, A., & Agungpriyono, S. (2018). Morfometri Limpa Berkaitan dengan Produksi Radikal Bebas dan Antioksidan pada Kelelawar Pemakan Buah Codot Krawar (Cynopterus brachyotis). Jurnal Veteriner, 19(1), 62–70. https://doi.org/10.19087/jveteriner.2018.19.1.62

Hanadhita, D., Satyaningtijas, A. S., & Agungpriyono, S. (2018). Bats As A Viral Reservoir: A Short Review Of Their Ecological Characters And Immune System. In Proceedings of the 1st International Conference in One Health (ICOH 2017) (pp. 124–128). Atlantis Press. https://doi.org/10.2991/icoh-17.2018.25

Harman, D. (2006). Free radical theory of aging: An update - Increasing the functional life span. Annals of the New York Academy of Sciences, 1067(1), 10–21. https://doi.org/10.1196/annals.1354.003

Healy, K., Guillerme, T., Finlay, S., Kane, A., Kelly, S. B. A., McClean, D., … Cooper, N. (2014). Ecology and mode-of-life explain lifespan variation in birds and mammals. Proceedings of the Royal Society B: Biological Sciences, 281(1784). https://doi.org/10.1098/rspb.2014.0298

Hengjan, Y., Saputra, V., Mirsageri, M., Pramono, D., Kasmono, S., Basri, C., … Hondo, E. (2018). Nighttime behavioral study of flying foxes on the southern coast of West Java, Indonesia. Journal of Veterinary Medical Science, 80(7), 1146–1152. https://doi.org/10.1292/jvms.17-0665

Ho, E., Karimi Galougahi, K., Liu, C. C., Bhindi, R., & Figtree, G. A. (2013). Biological markers of oxidative stress: Applications to cardiovascular research and practice. Redox Biology, 1(1), 483–491. https://doi.org/10.1016/j.redox.2013.07.006

Holmström, K. M., & Finkel, T. (2014). Cellular mechanisms and physiological consequences of redox-dependent signalling. Nature Reviews Molecular Cell Biology, 15(6), 411–421. https://doi.org/10.1038/nrm3801

Jürgens, K. D., & Prothero, J. (1987). Scaling of maximal lifespan in bats. Comparative Biochemistry and Physiology -- Part A: Physiology, 88(2), 361–367. https://doi.org/10.1016/0300-9629(87)90498-1

Kirkwood, T. B. L. (1989). DNA, mutations and aging. Mutation Research DNAging, 219, 1–7. https://doi.org/10.1016/0921-8734(89)90035-0

Kirkwood, T. B. L., & Austad, S. N. (2000). Why do we age? Nature, 408(6809), 233–238. https://doi.org/10.1038/35041682

Kobayashi, S., Sasaki, M., Nakao, R., Setiyono, A., Handharyani, E., Orba, Y., … Sawa, H. (2015). Detection of novel polyomaviruses in fruit bats in Indonesia. Archives of Virology, 160(4), 1075–1082. https://doi.org/10.1007/s00705-015-2349-7

Kwiecien, S., Jasnos, K., Magierowski, M., Sliwowski, Z., Pajdo, R., Brzozowski, B., … Brzozowski, T. (2014). Lipid peroxidation, reactive oxygen species and antioxidative factors in the pathogenesis of gastric mucosal lesions and mechanism of protection against oxidative stress - induced gastric injury. Journal of Physiology and Pharmacology : An Official Journal of the Polish Physiological Society, 65(5), 613–622.

Lei, M., & Dong, D. (2016). Phylogenomic analyses of bat subordinal relationships based on transcriptome data. Scientific Reports, 6(May), 1–8. https://doi.org/10.1038/srep27726

Lei, X. G., Zhu, J.-H., Cheng, W.-H., Bao, Y., Ho, Y.-S., Reddi, A. R., … Arnér, E. S. J. (2016). Paradoxical Roles of Antioxidant Enzymes: Basic Mechanisms and Health Implications. Physiological Reviews, 96(1), 307–364. https://doi.org/10.1152/physrev.00010.2014

Lilley, T. M., Ruokolainen, L., Meierjohann, A., Kanerva, M., Stauffer, J., Laine, V. N., … Nikinmaa, M. (2013). Resistance to oxidative damage but not immunosuppression by organic tin compounds in natural populations of Daubenton’s bats (Myotis daubentonii). Comparative Biochemistry and Physiology - C Toxicology and Pharmacology, 157(3), 298–305. https://doi.org/10.1016/j.cbpc.2013.01.003

Nabholz, B., Glémin, S., & Galtier, N. (2008). Strong variations of mitochondrial mutation rate across mammals - The longevity hypothesis. Molecular Biology and Evolution, 25(1), 120–130. https://doi.org/10.1093/molbev/msm248

Norquay, K. J., Martinez-Nunez, F., Dubois, J. E., Monson, K. M., & Willis, C. K. (2013). Long-distance movements of little brown bats (Myotis lucifugus). Journal of Mammalogy, 94(2), 506–515. https://doi.org/10.1644/12-MAMM-A-065.1

O’Shea, T. J., Cryan, P. M., Cunningham, A. A., Fooks, A. R., Hayman, D. T. S., Luis, A. D., … Wood, J. L. N. (2014). Bat flight and zoonotic viruses. Emerging Infectious Diseases, 20(5), 741–745. https://doi.org/10.3201/eid2005.130539

Oliveira, J. M., Losano, N. F., Condessa, S. S., de Freitas, R. M. P., Cardoso, S. A., Freitas, M. B., & de Oliveira, L. L. (2018). Exposure to deltamethrin induces oxidative stress and decreases of energy reserve in tissues of the Neotropical fruit-eating bat Artibeus lituratus. Ecotoxicology and Environmental Safety, 148(July 2017), 684–692. https://doi.org/10.1016/j.ecoenv.2017.11.024

Pavlovich, S. S., Lovett, S. P., Koroleva, G., Guito, J. C., Arnold, C. E., Nagle, E. R., … Palacios, G. (2018). The egyptian rousette genome reveals unexpected features of bat antiviral immunity. Cell, 173(5), 1098–1110.e18. https://doi.org/10.1016/j.cell.2018.03.070

Podlutsky, A. J., Khritankov, A. M., Ovodov, N. D., & Austad, S. N. (2005). A new field record for bat longevity. Journals of Gerontology - Series A Biological Sciences and Medical Sciences, 60(11), 1366–1368. https://doi.org/10.1093/gerona/60.11.1366

Reinke, N. B., & O’Brien, G. M. (2006). High activity antioxidant enzymes protect flying-fox haemoglobin against damage: An evolutionary adaptation for flight? Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 176(8), 729–737. https://doi.org/10.1007/s00360-006-0094-7

Roberts, B. J., Catterall, C. P., Eby, P., & Kanowski, J. (2012). Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: Implications for management. PLoS ONE, 7(8), 23–25. https://doi.org/10.1371/journal.pone.0042532

Ruiz, S. R., Eeva, T., Kanerva, M., Blomberg, A., & Lilley, T. M. (2019). Metal and metalloid exposure and oxidative status in free-living individuals of Myotis daubentonii. Ecotoxicology and Environmental Safety, 169(May 2018), 93–102. https://doi.org/10.1016/j.ecoenv.2018.10.083

Sasaki, M., Gonzalez, G., Wada, Y., Setiyono, A., Handharyani, E., Rahmadani, I., … Sawa, H. (2016). Divergent bufavirus harboured in megabats represents a new lineage of parvoviruses. Scientific Reports, 6(April), 1–8. https://doi.org/10.1038/srep24257

Sasaki, M., Setiyono, A., Handharyani, E., Kobayashi, S., Rahmadani, I., Taha, S., … Kimura, T. (2014). Isolation and characterization of a novel alphaherpesvirus in fruit bats. Journal of Virology, 88(17), 9819–9829. https://doi.org/10.1128/JVI.01277-14

Sasaki, M., Setiyono, A., Handharyani, E., Rahmadani, I., Taha, S., Adiani, S., … Kimura, T. (2012). Molecular detection of a novel paramyxovirus in fruit bats from Indonesia. Virology Journal, 9, 1–7. https://doi.org/10.1186/1743-422X-9-240

Schneeberger, K., Czirják, G. Á., & Voigt, C. C. (2014). Frugivory is associated with low measures of plasma oxidative stress and high antioxidant concentration in free-ranging bats. Naturwissenschaften, 101(4), 285–290. https://doi.org/10.1007/s00114-014-1155-5

Schountz, T., Baker, M. L., Butler, J., & Munster, V. (2017). Immunological control of viral infections in bats and the emergence of viruses highly pathogenic to humans. Frontiers in Immunology, 8(SEP). https://doi.org/10.3389/fimmu.2017.01098

Sendow, I., Field, H. E., Adjid, A., Ratnawati, A., Breed, A. C., Darminto, … Daniels, P. (2010). Screening for Nipah virus infection in West Kalimantan Province, Indonesia. Zoonoses and Public Health, 57(7–8), 499–503. https://doi.org/10.1111/j.1863-2378.2009.01252.x

Sendow, I., Ratnawati, A., Taylor, T., Adjid, R. M. A., Saepulloh, M., Barr, J., … Field, H. (2013). Nipah Virus in the fruit bat Pteropus vampyrus in Sumatera, Indonesia. PLoS ONE, 8(7). https://doi.org/10.1371/journal.pone.0069544

Sies, H. (2015). Oxidative stress: A concept in redox biology and medicine. Redox Biology, 4, 180–183. https://doi.org/10.1016/j.redox.2015.01.002

Simmons, N. B. (2000). Bat phylogeny: an evolutionary context for comparative studies. In R. A. Adams & S. C. Pedersen (Eds.), Ontogeny, Functional Ecology, and Evolution of Bats (pp. 9–58). New York: Cambridge University Press.

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, 307(5709), 580–584. https://doi.org/10.1126/science.1105113

Ungvari, Z., Buffenstein, R., Austad, S. N., Podlutsky, A., Kaley, G., & Csiszar, A. (2008). Oxidative stress in vascular senescence: lessons from successfully aging species. Frontiers in Bioscience : A Journal and Virtual Library, 13(March 2015), 5056–5070. https://doi.org/10.2741/3064

Wada, Y., Sasaki, M., Setiyono, A., Handharyani, E., Rahmadani, I., Taha, S., … Sawa, H. (2018). Detection of novel gammaherpesviruses from fruit bats in Indonesia. Journal of Medical Microbiology, 67(3). https://doi.org/10.1099/jmm.0.000689

Wang, L. F., Walker, P. J., & Poon, L. L. M. (2011). Mass extinctions, biodiversity and mitochondrial function: Are bats “special” as reservoirs for emerging viruses? Current Opinion in Virology, 1(6), 649–657. https://doi.org/10.1016/j.coviro.2011.10.013

Wilhelm Filho, D., Althoff, S. L., Dafré, A. L., & Boveris, A. (2007). Antioxidant defenses, longevity and ecophysiology of South American bats. Comparative Biochemistry and Physiology - C Toxicology and Pharmacology, 146(1–2 SPEC. ISS.), 214–220. https://doi.org/10.1016/j.cbpc.2006.11.015

Wilkinson, G. S., & South, J. M. (2002). Life history, ecology and longevity in bats. Aging Cell, 1, 124–131. https://doi.org/10.1046/j.1474-9718.2002.00020sm.x

Wresdiyati, T., Astawan, M., Fithriani, D., Adnyane, I. K. M., Novelina, S., & Aryani, S. (2007). the Effect of Α-Tocopherol on the Profiles of Superoxide Dismutase and Malondialdehyde in the Liver of Rats Under Stress Condition. Jurnal Veteriner, 2(12), 202–209.

Yin, Q., Ge, H., Liao, C. C., Liu, D., Zhang, S., & Pan, Y. H. (2016). Antioxidant defenses in the brains of bats during hibernation. PLoS ONE, 11(3), 1–17. https://doi.org/10.1371/journal.pone.0152135

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2019-01-30

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