Phagocyte activity reflects mammalian homeo- and hetero-thermic physiological states

. 2020 Jul 06 ; 16 (1) : 232. [epub] 20200706

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32631329

Grantová podpora
17-20286S Grantová Agentura České Republiky

Odkazy

PubMed 32631329
PubMed Central PMC7339577
DOI 10.1186/s12917-020-02450-z
PII: 10.1186/s12917-020-02450-z
Knihovny.cz E-zdroje

BACKGROUND: Emergence of both viral zoonoses from bats and diseases that threaten bat populations has highlighted the necessity for greater insights into the functioning of the bat immune system. Particularly when considering hibernating temperate bat species, it is important to understand the seasonal dynamics associated with immune response. Body temperature is one of the factors that modulates immune functions and defence mechanisms against pathogenic agents in vertebrates. To better understand innate immunity mediated by phagocytes in bats, we measured respiratory burst and haematology and blood chemistry parameters in heterothermic greater mouse-eared bats (Myotis myotis) and noctules (Nyctalus noctula) and homeothermic laboratory mice (Mus musculus). RESULTS: Bats displayed similar electrolyte levels and time-related parameters of phagocyte activity, but differed in blood profile parameters related to metabolism and red blood cell count. Greater mouse-eared bats differed from mice in all phagocyte activity parameters and had the lowest phagocytic activity overall, while noctules had the same quantitative phagocytic values as mice. Homeothermic mice were clustered separately in a high phagocyte activity group, while both heterothermic bat species were mixed in two lower phagocyte activity clusters. Stepwise regression identified glucose, white blood cell count, haemoglobin, total dissolved carbon dioxide and chloride variables as the best predictors of phagocyte activity. White blood cell counts, representing phagocyte numbers available for respiratory burst, were the best predictors of both time-related and quantitative parameters of phagocyte activity. Haemoglobin, as a proxy variable for oxygen available for uptake by phagocytes, was important for the onset of phagocytosis. CONCLUSIONS: Our comparative data indicate that phagocyte activity reflects the physiological state and blood metabolic and cellular characteristics of homeothermic and heterothermic mammals. However, further studies elucidating trade-offs between immune defence, seasonal lifestyle physiology, hibernation behaviour, roosting ecology and geographic patterns of immunity of heterothermic bat species will be necessary. An improved understanding of bat immune responses will have positive ramifications for wildlife and conservation medicine.

Zobrazit více v PubMed

Rosales C, Uribe-Querol E. Phagocytosis: a fundamental process in immunity. Biomed Res Int. 2017;9042851. PubMed PMC

Thomas DC. The phagocyte respiratory burst: historical perspectives and recent advances. Immunol Lett. 2017;192:88–96. PubMed

Dahlgren C, Karlsson A. Respiratory burst in human neutrophils. J Immunol Methods. 1999;232:3–14. PubMed

Marnila P, Tiiska A, Lagerspetz K, Lilius EM. Phagocyte activity in the frog Rana temporaria: whole blood chemiluminescence method and the effects of temperature and thermal acclimation. Comp Biochem Phys A. 1995;111:609–614. PubMed

Papežíková I, Mareš J, Vojtek L, Hyršl P, Marková Z, Šimková A, et al. Seasonal changes in immune parameters of rainbow trout (Oncorhynchus mykiss), brook trout (Salvelinus fontinalis) and brook trout × Arctic charr hybrids (Salvelinus fontinalis × Salvelinus alpinus alpinus) Fish Shellfish Immunol. 2016;57:400–405. PubMed

Lojek A, Ciz M, Marnila P, Duskova M, Lilius E-M. Measurement of whole blood phagocyte chemiluminescence in the Wistar rat. J Biolum Chemilum. 1997;12:225–231. PubMed

Cichoń M, Chadzińska M, Książek A, Konarzewski M. Delayed effects of cold stress on immune response in laboratory mice. P Roy Soc B: Biol Sci. 2002;269:1493–1497. PubMed PMC

Hawley DM, DuRant SE, Wilson AF, Adelman JS, Hopkins WA. Additive metabolic costs of thermoregulation and pathogen infection. Funct Ecol. 2012;26:701–710.

Canale CI, Henry P-Y. Energetic costs of the immune response and torpor use in a primate. Funct Ecol. 2011;25:557–565.

Field KA, Sewall BJ, Prokkola JM, Turner GG, Gagnon MF, Lilley TM, et al. Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats. Mol Ecol. 2018;27:3727–3743. PubMed

Mandl JN, Ahmed R, Barreiro LB, Daszak P, Epstein JH, Virgin HW, et al. Reservoir host immune responses to emerging zoonotic viruses. Cell. 2015;160:20–35. PubMed PMC

Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, et al. Bat white-nose syndrome: an emerging fungal pathogen? Science. 2009;323:227. PubMed

Willis CKR. Trade-offs influencing the physiological ecology of hibernation in temperate-zone bats. Integr Comp Biol. 2017;57:1214–1224. PubMed

Webb PI, Speakman JR, Racey PA. How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can J Zool. 1996;74:761–765.

Perry RW. A review of factors affecting cave climates for hibernating bats in temperate North America. Environ Rev. 2013;21:28–39.

Boyer B, Barnes B. Molecular and metabolic aspects of mammalian hibernation expression of the hibernation phenotype results from the coordinated regulation of multiple physiological and molecular events during preparation for and entry into torpor. BioScience. 1999;49:713–724.

Carey HV, Andrews MT, Martin SL. Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev. 2003;83:1153–1181. PubMed

Andrews MT. Advances in molecular biology of hibernation in mammals. Bioessays. 2007;29:431–440. PubMed

Xu Y, Shao C, Fedorov V, Goropashnaya A, Barnes B, Yan J. Molecular signatures of mammalian hibernation: comparisons with alternative phenotypes. BMC Genomics. 2013;14:567. PubMed PMC

Dietz M, Kalko EK. Seasonal changes in daily torpor patterns of free-ranging female and male Daubenton's bats (Myotis daubentonii) J Comp Physiol B. 2006;176:223–231. PubMed

Wojciechowski MS, Jefimow M, Tegowska E. Environmental conditions, rather than season, determine torpor use and temperature selection in large mouse-eared bats (Myotis myotis) Comp Biochem Physiol A Mol Integr Physiol. 2007;147:828–840. PubMed

Bartonicka T, Bandouchova H, Berkova H, Blazek J, Lucan R, Horacek I, et al. Deeply torpid bats can change position without elevation of body temperature. J Therm Biol. 2017;63:119–123. PubMed

Roy VK, Krishna A. Changes in glucose and carnitine levels and their transporters in utero-tubal junction in relation to sperm storage in the vespertilionid bat, Scotophilus heathi. J Exp Zool Part A. 2013;319:517–526. PubMed

Bandouchova H, Bartonička T, Berkova H, Brichta J, Kokurewicz T, Kovacova V, et al. Alterations in the health of hibernating bats under pathogen pressure. Sci Rep-UK. 2018;8:6067. PubMed PMC

Musacchia X, Volkert W. Blood gases in hibernating and active ground squirrels: HbO2 affinity at 6 and 38 C. Am J Phys. 1971;221:128–130. PubMed

Geiser F. Hibernation: endotherms in eLS. Chichester: Wiley, Ltd; 2011.

Bouma HR, Carey HV, Kroese FGM. Hibernation: the immune system at rest? J Leukoc Biol. 2010;88:619–624. PubMed

Bouma HR, Dugbartey GJ, Boerema AS, Talaei F, Herwig A, Goris M, et al. Reduction of body temperature governs neutrophil retention in hibernating and nonhibernating animals by margination. J Leukoc Biol. 2013;94:431–437. PubMed

Moore MS, Reichard JD, Murtha TD, Zahedi B, Fallier R, Kunz TH. Specific alterations in complement protein activity of little brown Myotis (Myotis lucifugus) hibernating in white-nose syndrome affected sites. PLoS One. 2011;6:e27430. PubMed PMC

Hecht AM, Braun BC, Krause E, Voigt CC, Greenwood AD, Czirják GÁ. Plasma proteomic analysis of active and torpid greater mouse-eared bats (Myotis myotis) Sci Rep UK. 2015;5:16604. PubMed PMC

Casadevall A, Pirofski L-A. Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect Immun. 1999;67:3703–3713. PubMed PMC

Smith LM, May RC. Mechanisms of microbial escape from phagocyte killing. Biochem Soc T. 2013;41:475. PubMed

Boratynski JS, Rusiński M, Kokurewicz T, Bereszyński A, Wojciechowski MS. Clustering behavior in wintering greater mouse-eared bats Myotis myotis - the effect of micro-environmental conditions. Acta Chiropterol. 2012;14:417–424.

Ruczynski I, Bogdanowicz W. Roost cavity selection by Nyctalus noctula and N. leisleri (Vespertilionidae, Chiroptera) in Bialowieza primeval forest, eastern Poland. J Mammal. 2005;86:921–930.

Zukal J, Berková H, Řehák Z. Activity and shelter selection by Myotis myotis and Rhinolophus hipposideros hibernating in Kateřinská cave (Czech Republic) Mamm Biol. 2005;70:271–281.

Kruger P, Saffarzadeh M, Weber ANR, Rieber N, Radsak M, von Bernuth H, et al. Neutrophils: between host defence, immune modulation, and tissue injury. PLoS Pathog. 2015;11:e1004651. PubMed PMC

Pikula J, Amelon SK, Bandouchova H, Bartonička T, Berkova H, Brichta J, et al. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS One. 2017;12:e0180435. PubMed PMC

Maina JN, King AS. Correlations between structure and function in the design of the bat lung: a morphometric study. J Exp Biol. 1984;111:43–61. PubMed

Rodríguez-Durán A, Padilla-Rodríguez E. Blood characteristics, heart mass, and wing morphology of Antillean bats. Caribb J Sci. 2008;44:375–379.

Glette J, Solberg CO, Lehmann V. Factors influencing human polymorphonuclear leukocyte chemiluminescence. Acta Pathol Microbiol Scandinavica C Immunol. 1982;90C:91–95. PubMed

Winterbourn CC, Stern A. Human red cells scavenge extracellular hydrogen peroxide and inhibit formation of hypochlorous acid and hydroxyl radical. J Clin Invest. 1987;80:1486–1491. PubMed PMC

Chapman ALP, Hampton MB, Senthilmohan R, Winterbourn CC, Kettle AJ. Chlorination of bacterial and neutrophil proteins during phagocytosis and killing of Staphylococcus aureus. J Biol Chem. 2002;277:9757–9762. PubMed

Gaut JP, Yeh GC, Tran HD, Byun J, Henderson JP, Richter GM, et al. Neutrophils employ the myeloperoxidase system to generate antimicrobial brominating and chlorinating oxidants during sepsis. P Natl Acad Sci USA. 2001;98:11961. PubMed PMC

Cryan PM, Meteyer CU, Blehert DS, Lorch JM, Reeder DM, Turner GG, et al. Electrolyte depletion in white-nose syndrome bats. J Wildlife Dis. 2013;49:398–402. PubMed

Voyles J, Berger L, Young S, Speare R, Webb R, Warner J, et al. Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Dis Aquat Org. 2007;77:113–118. PubMed

Heard DJ, Huft VJ. The effects of short-term physical restraint and isoflurane anesthesia on hematology and plasma biochemistry in the island flying fox (Pteropus hypomelanus) J Zoo Wildl Med. 1998;29:14–17. PubMed

Strobel S, Becker NI, Encarnação JA. No short-term effect of handling and capture stress on immune responses of bats assessed by bacterial killing assay. Mamm Biol. 2015;80:312–315. PubMed PMC

Luis AD, Hudson PJ. Hibernation patterns in mammals: a role for bacterial growth? Funct Ecol. 2006;20:471–477.

Martínková N, Pikula J, Zukal J, Kovacova V, Bandouchova H, Bartonička T, et al. Hibernation temperature-dependent Pseudogymnoascus destructans infection intensity in Palearctic bats. Virulence. 2018;9:1734–1750. PubMed PMC

Martínková N, Škrabánek P, Pikula J. Modelling invasive pathogen load from non-destructive sampling data. J Theor Biol. 2019;464:98–103. PubMed

Bergman A, Casadevall A. Mammalian endothermy optimally restricts fungi and metabolic costs. mBio. 2010;1:e00212–e00210. PubMed PMC

Mayberry HW, McGuire LP, Willis CKR. Body temperatures of hibernating little brown bats reveal pronounced behavioural activity during deep torpor and suggest a fever response during white-nose syndrome. J Comp Physiol B. 2018;188:333–343. PubMed

Babior BM. Phagocytes and oxidative stress. Am J Med. 2000;109:33–44. PubMed

Costantini D, Møller AP. Does immune response cause oxidative stress in birds? A meta-analysis. Comp Biochem Phys A. 2009;153:339–344. PubMed

Vitula F, Peckova L, Bandouchova H, Pohanka M, Novotny L, Jira D, et al. Mycoplasma gallisepticum infection in the grey partridge Perdix perdix: outbreak description, histopathology, biochemistry and antioxidant parameters. BMC Vet Res. 2011;7:12. PubMed PMC

Brook CE, Dobson AP. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends Microbiol. 2015;23:172–180. PubMed PMC

Wang L-F, Walker PJ, Poon LLM. Mass extinctions, biodiversity and mitochondrial function: are bats ‘special’ as reservoirs for emerging viruses? Curr Opin Virol. 2011;1:649–657. PubMed PMC

Mandl JN, Schneider C, Schneider SD, Baker ML. Going to bat(s) for studies of disease tolerance. Front Immunol. 2018;9:2112. PubMed PMC

Kacprzyk J, Hughes GM, Palsson-McDermott EM, Quinn SR, Puechmaille SJ, O'Neill LAJ, et al. A potent anti-inflammatory response in bat macrophages may be linked to extended longevity and viral tolerance. Acta Chiropterol. 2017;19:219–228.

Zukal J, Bandouchova H, Brichta J, Cmokova A, Jaron KS, Kolarik M, et al. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci Rep UK. 2016;6:19829. PubMed PMC

Meteyer CU, Barber D, Mandl JN. Pathology in euthermic bats with white nose syndrome suggests a natural manifestation of immune reconstitution inflammatory syndrome. Virulence. 2012;3:583–588. PubMed PMC

Flieger M, Bandouchova H, Cerny J, Chudíčková M, Kolarik M, Kovacova V, et al. Vitamin B2 as a virulence factor in Pseudogymnoascus destructans skin infection. Sci Rep UK. 2016;6:33200. PubMed PMC

Medzhitov R, Schneider DS, Soares MP. Disease tolerance as a defence strategy. Science. 2012;335:936–941. PubMed PMC

Becker DJ, Albery GF, Kessler MK, Lunn TJ, Falvo CA, Czirják GÁ, et al. Macroimmunology: the drivers and consequences of spatial patterns in wildlife immune defence. J Anim Ecol. 2020;00:1–24. doi: 10.1111/1365-2656.13166. PubMed DOI PMC

Gaisler J, Hanák V, Hanzal V, Jarský V. Results of bat banding in the Czech and Slovak republics, 1948-2000. Vespertilio. 2003;7:3–61.

Kokurewicz T, Apoznanski G, Gyselings R, Kirkpatrick L, de Bruyn L, Haddow J, et al. 45 years of bat study and conservation in Nietoperek bat reserve (Western Poland) Nyctalus. 2019;3:252–269.

Strelkov PP. Migratory and stationary bats (Chiroptera) of the European part of the Soviet Union. Acta Zool Cracoviensia. 1969;14:93–439.

Allen LC, Turmelle AS, Mendonça MT, Navara KJ, Kunz TH, McCracken GF, et al. Roosting ecology and variation in adaptive and innate immune system function in the Brazilian free-tailed bat (Tadarida brasiliensis) J Comp Physiol B. 2008;179:315–323. PubMed PMC

Linhart P, Bandouchova H, Zukal J, Votýpka J, Kokurewicz T, Dundarova H, et al. Trypanosomes in eastern and central European bats. Acta Vet Brno. 2020;89:69–78.

Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T. Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev. 2006;19:531–545. PubMed PMC

Baker ML, Schountz T, Wang L-F. Antiviral immune responses of bats: a review. Zoonoses Public Hlth. 2013;60:104–116. PubMed PMC

He X, Korytář T, Zhu Y, Pikula J, Bandouchova H, Zukal J, et al. Establishment of Myotis myotis cell lines - model for investigation of host-pathogen interaction in a natural host for emerging viruses. PLoS One. 2014;9:e109795. PubMed PMC

Parasuraman S, Raveendran R, Kesavan R. Blood sample collection in small laboratory animals. J Pharmacol Pharmacother. 2010;1:87–93. PubMed PMC

Pikula J, Bandouchova H, Kovacova V, Linhart P, Piacek V, Zukal J. Reproduction of rescued vespertilionid bats (Nyctalus noctula) in captivity: veterinary and physiological aspects. Vet Clin North Am Exot Anim Pract. 2017;20:665–677. PubMed

Heger T, Zukal J, Seidlova V, Nemcova M, Necas D, Papezikova I, et al. Measurement of phagocyte activity in heterotherms. Acta Vet Brno. 2020;89:79–87.

Wang M, Wright J, Brownlee A, Buswell R. A comparison of approaches to stepwise regression on variables sensitivities in building simulation and analysis. Energ Buildings. 2016;127:313–326.

Venables WN, Riple BD. Modern applied statistics with S. 4. New York: Springer; 2002.

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace