PL EN


Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2017 | 19 | 2 |

Tytuł artykułu

A potent anti-inflammatory response in bat macrophages may be linked to extended longevity and viral tolerance

Warianty tytułu

Języki publikacji

EN

Abstrakty

EN
Bats are unique among mammals given their ability to fly, apparent tolerance of deadly viruses and extraordinary longevity. We propose that these traits are linked and driven by adaptations of the innate immune system. To explore this hypothesis we challenged macrophages from the greater mouse-eared bat, Myotis myotis and the house mouse, Mus musculus with toll like receptors (TLRs) ligands, lipopolysaccharides, LPS and polyinosinic-polycytidylic acid, Poly(I:C). Macrophages from both species presented a high level of mRNA induction of inferon β (INF-β), tumor necrosis factor (TNF) and interleukin-1β (Il-1β). However, in bat macrophages, this antiviral, proinflammatory response was balanced by a sustained high-level transcription of the anti-inflammatory cytokine Il-10, which was not observed in mouse, potentially resulting from adaptive regulation in bats. Additionally, phylogenomic selection tests across the basal divergences in mammals (n = 39) uncovered bat-specific adaptations in six genes involved in antiviral and proinflammatory signalling. Based on this pilot study, we put forward a hypothesis that bats may have evolved unique anti-inflammatory responses to neutralize proinflammatory stimuli resulting from flight. This in turn may drive their extraordinary longevity and viral tolerance by limiting inflammation driven ageing and infection-induced immunopathology. Further data from other individuals and bat species are required to advance this intriguing hypothesis.

Słowa kluczowe

Wydawca

-

Rocznik

Tom

19

Numer

2

Opis fizyczny

p.219-228,fig.,ref.

Twórcy

autor
  • School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland
autor
  • School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland
  • School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, 152-160 Pearse Street, Dublin 2, Ireland
autor
  • School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, 152-160 Pearse Street, Dublin 2, Ireland
  • Zoological Institute and Museum, Greifswald University, Soldmann-Straβe 14, D-17489, Greifswald, Germany
  • School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, 152-160 Pearse Street, Dublin 2, Ireland
autor
  • School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland

Bibliografia

  • 1. Ahn, M., J. Cut, A. T. Irving, and L.-F. Wang. 2016. Unique loss of the PYHIN gene family in bats amongst mammals: implications for inflammasome sensing. Scientific Reports, 6: 21722. Google Scholar
  • 2. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nature Reviews: Immunology, 4: 499–511. Google Scholar
  • 3. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215: 403–410. Google Scholar
  • 4. Arai, Y., C. M. Martin-Ruiz, M. Takayama, Y. Abe, T. Takebayashi, S. Koyasu, M. Suematsu, N. Hirose, and T. von Zglinicki. 2015. Inflammation, but not telomere length, predicts successful ageing at extreme old age: a longitudinal study of semi-supercentenarians. EBioMedicine, 2: 1549–1558. Google Scholar
  • 5. Austad, S. N. 2010. Methusaleh's Zoo: how Nature provides us with clues for extending human health span. Journal of Comparative Pathology, 142: S10–S21. Google Scholar
  • 6. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57B: 289–300. Google Scholar
  • 7. Benson, D. A., K. Clark, I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, and E. W. Sayers. 2015. GenBank. Nucleic Acids Research, 43: D30–D35. Google Scholar
  • 8. Brook, C. E., and A. P. Dobson. 2015. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends in Microbiology, 23: 172–180. Google Scholar
  • 9. Brooks, D. G., M. J. Trifilo, K. H. Edelmann, L. Teyton, D. B. McGavern, and M. B. A. Oldstone. 2006. Interleukin-10 determines viral clearance or persistence in vivo. Nature Medicine, 12: 1301–1309. Google Scholar
  • 10. Buffenstein, R., Y. H. Edrey, T. Yang, and J. Mele. 2008. The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organisms. Age, 30: 99–109. Google Scholar
  • 11. Burdette, D. L., and R. E. Vance. 2013. STING and the innate immune response to nucleic acids in the cytosol. Nature Immunology, 14: 19–26. Google Scholar
  • 12. Dimitrijević, M., S. Stanojević, V. Vujić, I. Aleksić, I. Pilipović, and G. Leposavić. 2014. Aging oppositely affects TNF-α and IL-10 production by macrophages from different rat strains. Biogerontology, 15: 475–486. Google Scholar
  • 13. Dinarello, C. A. 2011. A clinical perspective of IL-1β as the gatekeeper of inflammation. European Journal of Immunology, 41: 1203–1217. Google Scholar
  • 14. Dinarello, C., D. Novick, S. Kim, and G. Kaplanski. 2013. Interleukin-18 and IL-18 binding protein. Frontiers in Immunology, 4: 289. Google Scholar
  • 15. Ding, X., S. Jin, Y. Tong, X. Jiang, Z. Chen, S. Mei, L. Zhang, T. R. Billiar, and Q. Li. 2017. TLR4 signaling induces TLR3 up-regulation in alveolar macrophages during acute lung injury. Scientific Reports, 7: 34278. Google Scholar
  • 16. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32: 1792–1797. Google Scholar
  • 17. Foley, N. M., M. S. Springer, and E. C. Teeling. 2016. Mammal madness: is the mammal tree of life not yet resolved? Philosophical Transactions of the Royal Society, 371B: 20150140. Google Scholar
  • 18. Franceschi, C., and J. Campisi. 2014. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. The Journals of Gerontology, 69A: S4–S9. Google Scholar
  • 19. Gaisler, J., V. Hanák, V. Hanzal, and V. Jarský. 2003. Results of bat banding in the Czech and Slovak Republics, 1948–2000. Vespertilio, 7: 3–61. Google Scholar
  • 20. Greer, D. L., and D. N. McMurray. 1981. Pathogenesis of experimental histoplasmosis in the bat, Artibeus lituratus.The American Journal of Tropical Medicine and Hygiene, 30: 653–659. Google Scholar
  • 21. Guarda, G., M. Braun, F. Staehli, A. Tardivel, C. Mattmann, I. Förster, M. Farlik, T. Decker, R. A. Du Pasquier, P. Romero , et al. 2011. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity, 34: 213–223. Google Scholar
  • 22. Guiyedi, V., C. Bécavin, F. Herbert, J. Gray, P.-A. Cazenave, M. Kombila, A. Crisanti, C. Fesel, and S. Pied. 2015. Asymptomatic Plasmodium falciparum infection in children is associated with increased auto-antibody production, high IL-10 plasma levels and antibodies to merozoite surface protein 3. Malaria Journal, 14: 162. Google Scholar
  • 23. Guo, H., J. B. Callaway, and J. P. Y. Ting. 2015. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nature Medicine, 21: 677–687. Google Scholar
  • 24. Hayman, D. T. S., P. Emmerich, M. Yu, L.-F. Wang, R. Suu-Ire, A. R. Fooks, A. A. Cunningham, and J. L. N. Wood. 2010. Long-term survival of an urban fruit bat seropositive for Ebola and Lagos bat viruses. PLoS ONE, 5: e11978. Google Scholar
  • 25. Healy, K., T. Guillerme, S. Finlay, A. Kane, S. B. A. Kelly, D. McClean, D. J. Kelly, I. Donohue, A. L. Jackson, and N. Cooper. 2014. Ecology and mode-of-life explain life-span variation in birds and mammals. Proceedings of the Royal Society, 281B: 20140298. Google Scholar
  • 26. Huang, Z., A. Gallot, N. T. Lao, S. J. Puechmaille, N. M. Foley, D. Jebb, M. Bekaert, and E. C. Teeling. 2016. A nonlethal sampling method to obtain, generate and assemble whole blood transcriptomes from small, wild mammals. Molecular Ecology Resources, 16: 150–162. Google Scholar
  • 27. Kelly, B., and L. A. J. O'Neill. 2015. Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Research, 25: 771–784. Google Scholar
  • 28. Kirwan, J. D., M. Bekaert, J. M. Commins, K. T. J. Davies, S. J. Rossiter, and E. C. Teeling. 2013. A phylomedicine approach to understanding the evolution of auditory sensory perception and disease in mammals. Evolutionary Applications, 6: 412–422. Google Scholar
  • 29. Kosoy, M., Y. Bai, T. Lynch, I. V. Kuzmin, M. Niezgoda, R. Franka, B. Agwanda, R. F. Breiman, and C. E. Rupprecht. 2010. Bartonella spp. in bats, Kenya. Emerging Infectious Diseases, 16: 1875–1881. Google Scholar
  • 30. Ksiażek, A., and M. Konarzewski. 2012. Effect of dietary restriction on immune response of laboratory mice divergently selected for basal metabolic rate. Physiological and Biochemical Zoology, 85: 51–61. Google Scholar
  • 31. Kühl, A., M. Hoffmann, M. A. Müller, V. J. Munster, K. Gnirss, M. Kiene, T. S. Tsegaye, G. Behrens, G. Herrler, H. Feldmann , et al. 2011. Comparative analysis of Ebola virus glycoprotein interactions with human and bat cells. The Journal of Infectious Diseases, 204: S840–S849. Google Scholar
  • 32. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25: 402–408. Google Scholar
  • 33. Lood, C., L. P. Blanco, M. M. Purmalek, C. Carmona-Rivera, S. S. De Ravin, C. K. Smith, H. L. Malech, J. A. Ledbetter, K. B. Elkon and M. J. Kaplan. 2016. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nature Medicine, 22: 146–153. Google Scholar
  • 34. Lu, Y.-C., W.-C. Yeh, and P. S. Ohashi. 2008. LPS/TLR4 signal transduction pathway. Cytokine, 42: 145–151. Google Scholar
  • 35. Matsumoto, M., and T. Seya. 2008. TLR3: Interferon induction by double-stranded RNA including poly(I:C). Advanced Drug Delivery Reviews, 60: 805–812. Google Scholar
  • 36. Medzhitov, R., and C. Janeway. 2000. Innate immunity. New England Journal of Medicine, 343: 338–344. Google Scholar
  • 37. Meredith, R. W., J. E. Janečka, J. Gatesy, O. A. Ryder, C. A. Fisher, E. C. Teeling, A. Goodbla, E. Eizirik, T. L. L. Simão, T. Stadler , et al. 2011. Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science, 334: 521–524. Google Scholar
  • 38. Miller, M. R., R. J. McMinn, V. Misra, T. Schountz, M. A. Müller, A. Kurth, and V. J. Munster. 2016. Broad and temperature independent replication potential of filoviruses on cells derived from Old and New World bat species. The Journal of Infectious Diseases, 214: S297–S302. Google Scholar
  • 39. Munshi-South, J., and G. S. Wilkinson. 2010. Bats and birds: exceptional longevity despite high metabolic rates. Ageing Research Reviews, 9: 12–19. Google Scholar
  • 40. Nath, I. 2008. Immune mechanisms against intracellular pathogens. eLS Journal, https://doi.org/10.1002/9780470015902.a0000480. pub2. Google Scholar
  • 41. Okumura, A., P. M. Pitha, A. Yoshimura, and R. N. Harty. 2010. Interaction between Ebola virus glycoprotein and host toll-like receptor 4 leads to induction of pro inflammatory cytokines and SOCS1. Journal of Virology, 84: 27–33. Google Scholar
  • 42. Onoguchi, K., M. Yoneyama, and T. Fujita. 2010. Retinoic acid-inducible gene-I-like receptors. Journal of Interferon & Cytokine Research, 31: 27–31. Google Scholar
  • 43. O'Shea, T. J., P. M. Cryan, A. A. Cunningham, A. R. Fooks, D. T. S. Hayman, A. D. Luis, A. J. Peel, R. K. Plowright, and J. L. N. Wood. 2014. Bat flight and zoonotic viruses. Emerging Infectious Disease Journal, 20: 741. Google Scholar
  • 44. Otálora-Ardila, A., L. G. Herrera M, J. J. Flores-Martínez, and K. C. Welch, Jr . 2016. Metabolic cost of the activation of immune response in the fish-eating myotis (Myotis vivesi): the effects of inflammation and the acute phase response. PLoS ONE, 11: e0164938. Google Scholar
  • 45. R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Available at: http://www.R-project.org/ . Google Scholar
  • 46. Rouse, B. T., and S. Sehrawat. 2010. Immunity and immunopathology to viruses: what decides the outcome? Nature reviews. Immunology, 10: 514–526. Google Scholar
  • 47. Ruedi, M., B. Stadelmann, Y. Gager, E. J. P. Douzery, C. M. Francis, L.-K. Lin, A. Guillén-Servent, and A. Cibois. 2013. Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera). Molecular Phylogenetics and Evolution, 69: 437–449. Google Scholar
  • 48. Sabharwal, S. S., and P. T. Schumacker. 2014. Mitochondrial ROS in cancer: initiators, amplifiers or an Achilles' heel? Nature Reviews Cancer, 14: 709–721. Google Scholar
  • 49. Schaer, J., S. L. Perkins, J. Decher, F. H. Leendertz, J. Fahr, N. Weber, and K. Matuschewski. 2013. High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa. Proceedings of the National Academy of Sciences of the USA, 110: 17415–17419. Google Scholar
  • 50. Schneeberger, K., G. Á. Czirják, and C. C. Voigt. 2013. Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal. The Journal of Experimental Biology, 216: 4514–4519. Google Scholar
  • 51. Schwarz, F., O. M. T. Pearce, X. Wang, A. N. Samraj, H. Läubli, J. O. Garcia, H. Lin, X. Fu, A. Garcia-Bingman, P. Secrest , et al. 2015. Siglec receptors impact mammalian lifespan by modulating oxidative stress. eLife, 4: e06184. Google Scholar
  • 52. Speakman, J. R., and D. W. Thomas. 2003. Physiological ecology and energetics of bats. Pp. 430–490, in Bat ecology (T. H. Kunz and M. B. Fenton, eds.). University of Chicago Press, Chicago, 779 pp. Google Scholar
  • 53. Stockmaier, S., D. K. N. Dechmann, R. A. Page, and M. T. O'Mara. 2015. No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat. Biology Letters, 11: 20150576. Google Scholar
  • 54. Suyama, M., D. Torrents, and P. Bork. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Research, 34: W609–W612. Google Scholar
  • 55. Tannahill, G. M., A. M. Curtis, J. Adamik, E. M. Palsson-McDermott, A. F. McGetterick, G. Goel, C. Frezza, N. J. Bernard, B. Kelly, N. H. Foley , et al. 2013. Succinate is a danger signal that induces IL-1β via HIF-1α. Nature, 496: 238–242. Google Scholar
  • 56. Tatematsu, M., T. Seya, and M. Matsumoto. 2014. Beyond dsRNA: Toll-like receptor 3 signalling in RNA-induced immune responses. Biochemical Journal, 458: 195–201. Google Scholar
  • 57. Tisoncik, J. R., M. J. Korth, C. P. Simmons, J. Farrar, T. R. Martin, and M. G. Katze. 2012. Into the eye of the cytokine storm. Microbiology and Molecular Biology Reviews, 76: 16–32. Google Scholar
  • 58. Untergasser, A., I. Cutcutache, T. Koressaar, J. Ye, B. C. Faircloth, M. Remm, and S. G. Rozen. 2012. Primer3 — new capabilities and interfaces. Nucleic Acids Research, 40: e115. Google Scholar
  • 59. Wang, F., T. Alain, K. J. Szretter, K. Stephenson, J. G. Pol, M. J. Atherton, H.-D. Hoang, B. D. Fonseca, C. Zakaria, L. Chen , et al. 2016. S6K-STING interaction regulates cytosolic DNA-mediated activation of the transcription factor IRF3. Nature Immunology, 17: 514–522. Google Scholar
  • 60. Weyer, J., A. Grobbelaar, and L. Blumberg. 2015. Ebola virus disease: history, epidemiology and outbreaks. Current Infectious Disease Reports, 17: 21. Google Scholar
  • 61. Yang, Z. 2007. PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24: 1586–1591. Google Scholar
  • 62. Yang, Z., W. S. W. Wong, and R. Nielsen. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution, 22: 1107–1118. Google Scholar
  • 63. Zhang, G., C. Cowled, Z. Shi, Z. Huang, K. A. Bishop-Lilly, X. Fang, J. W. Wynne, Z. Xiong, M. L. Baker, W. Zhao , et al. 2013. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science, 339: 456–460. Google Scholar
  • 64. Zhou, P., M. Tachedjian, J. W. Wynne, V. Boyd, J. Cui, I. Smith, C. Cowled, J. H. J. Ng, L. Mok, W. P. Michalski , et al. 2016a . Contraction of the type I IFN locus and unusual constitutive expression of IFN-α in bats. Proceedings of the National Academy of Sciences of the USA, 113: 2696–2701. Google Scholar
  • 65. Zhou, P., Y. T. Chionh, S. E. Irac, M. Ahn, J. H. Jia Ng, E. Fossum, B. Bogen, F. Ginhoux, A. T. Irving, C.-A. Dutertre , et al. 2016b . Unlocking bat immunology: establishment of Pteropus alecto bone marrow-derived dendritic cells and macrophages. Scientific Reports, 6: 38597. Google Scholar

Typ dokumentu

Bibliografia

Identyfikator YADDA

bwmeta1.element.agro-90fd419f-efe2-46a3-898c-f0a609be53f7
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.