Time-related immunomodulation by stressors and corticosterone transdermal application in toads


Autoři: Stefanny Christie Monteiro Titon aff001;  Braz Titon, Jr aff001;  Adriana Maria Giorgi Barsotti aff001;  Fernando Ribeiro Gomes aff001;  Vania Regina Assis aff001
Působiště autorů: Departamento de Fisiologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brasil aff001
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222856

Souhrn

Immune responses have been mostly studied at a specific time in anuran species. However, time-changes related to immunomodulation associated with glucocorticoid (GC) alterations following stressors and GC treatment are complex. The present study describes time-related changes in immune response and corticosterone (CORT) plasma levels following restraint challenge, short, mid and long-term captivity, and CORT exogenous administration by transdermal application (TA) in Rhinella ornata toads. We observed increased neutrophil: lymphocyte ratios after restraint challenge and CORT TA, without changes following short and mid-term captivity. Plasma bacterial killing ability was sustained in all treatments, except long-term captivity, with decreased values after 90 days under such conditions. Phagocytic activity of peritoneal cells increased after mid-term captivity, and the phytohemagglutinin swelling response was impaired in those animals treated with CORT TA for 20 consecutive days. Plasma CORT levels increased or were sustained after restraint challenge (depending on initial values), decreased following mid and long-term captivity (for those animals showing high CORT in the field) and increased after 20 days of CORT TA. By performing assessments of time-changes in immune processes and CORT plasma levels in R. ornata, we demonstrate immuno-enhancing effects following restraint, short and mid-term stressors, while long-term stressors and CORT TA promoted immunosuppression in these toads.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Animals – Vertebrates – Amphibians – Toads – Cell biology – Cell processes – Phagocytosis – Cellular stress responses – Cellular types – Animal cells – Blood cells – White blood cells – Neutrophils – Lymphocytes – Immune cells – Anatomy – Body fluids – Blood – Blood plasma – Physiology – Medicine and health sciences – Immunology – Immune response – Diagnostic medicine – Signs and symptoms – Pathology and laboratory medicine – Edema


Zdroje

1. Martin LB. Stress and immunity in wild vertebrates: Timing is everything. Gen Comp Endocrinol. Elsevier Inc.; 2009;163: 70–76. doi: 10.1016/j.ygcen.2009.03.008 19318107

2. Dhabhar FS. Effects of stress on immune function: The good, the bad, and the beautiful. Immunol Res. 2014;58: 193–210. doi: 10.1007/s12026-014-8517-0 24798553

3. Dhabhar FS. Enhancing versus Suppressive Effects of Stress on Immune function. Implications for Immunoprotection and Immunopathology. NeuroImmune Biol. 2008;7: 207–224. doi: 10.1016/S1567-7443(07)00211-6

4. Falso PG, Noble CA, Diaz JM, Hayes TB. The effect of long-term corticosterone treatment on blood cell differentials and function in laboratory and wild-caught amphibian models. Gen Comp Endocrinol. Elsevier Inc.; 2015;212: 73–83. doi: 10.1016/j.ygcen.2015.01.003 25616196

5. Madelaire CB, Cassettari B de O, Gomes FR. Immunomodulation by testosterone and corticosterone in toads: Experimental evidences from transdermal application. Gen Comp Endocrinol. Elsevier; 2019;273: 227–235. doi: 10.1016/j.ygcen.2018.09.005 30195026

6. Berger S, Martin LB, Wikelski M, Romero LM, Kalko EKV, Vitousek MN, et al. Corticosterone suppresses immune activity in territorial Galápagos marine iguanas during reproduction. Horm Behav. 2005;47: 419–429. doi: 10.1016/j.yhbeh.2004.11.011 15777807

7. Martin LB, Gilliam J, Han P, Lee K, Wikelski M. Corticosterone suppresses cutaneous immune function in temperate but not tropical House Sparrows, Passer domesticus. Gen Comp Endocrinol. 2005;140: 126–135. doi: 10.1016/j.ygcen.2004.10.010 15613275

8. Davis AK, Maney DL. The use of glucocorticoid hormones or leucocyte profiles to measure stress in vertebrates: What’s the difference? Methods Ecol Evol. 2018;9: 1556–1568. doi: 10.1111/2041-210X.13020

9. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 2000;21: 55–89. doi: 10.1210/edrv.21.1.0389 10696570

10. Davis AK, Maney DL, Maerz JC. The use of leukocyte profiles to measure stress in vertebrates: A review for ecologists. Funct Ecol. 2008;22: 760–772. doi: 10.1111/j.1365-2435.2008.01467.x

11. Assis VR, Titon SCM, Gomes FR. Acute stress, steroid plasma levels, and innate immunity in Brazilian toads. Gen Comp Endocrinol. Elsevier; 2019;273: 86–97. doi: 10.1016/j.ygcen.2018.05.008 29750968

12. Assis VR, Titon SCM, Queiroz-Hazarbassanov NGT, Massoco CO, Gomes FR. Corticosterone transdermal application in toads (Rhinella icterica): Effects on cellular and humoral immunity and steroid plasma levels. J Exp Zool Part A Ecol Integr Physiol. 2017;327: 200–213. doi: 10.1002/jez.2093 29356458

13. Barsotti AMG, Titon Junior B, Titon SCM, Gomes FR. Dehydration as a stressor in toads (Rhinella ornata). J Exp Zool Part A Ecol Integr Physiol. 2019;331: 168–174. doi: 10.1002/jez.2250 30569667

14. Barriga C, Martín MI, Tabla R, Ortega E, Rodríguez AB. Circadian rhythm of melatonin, corticosterone and phagocytosis: Effect of stress. J Pineal Res. 2001;30: 180–187. doi: 10.1034/j.1600-079X.2001.300307.x 11316329

15. Dhabhar FS, McEwen BS. Acute stress enhances while chronic stress suppresses immune function in vivo: A potential role for leukocyte trafficking. Brain Behav Immun. 1997;11: 286–306. doi: 10.1006/brbi.1997.0508 9512816

16. Dhabhar FS, McEwen BS. Enhancing versus suppressive effects of stress hormones on skin immune function. Proc Natl Acad Sci. 1999;96: 1059–1064. doi: 10.1073/pnas.96.3.1059 9927693

17. Dhabhar FS, McEwen BS. Stress-induced enhancement of antigen-specific cell-mediated immunity. J Immunol. 1996;156: 2608–2615. Available: http://www.jimmunol.org/content/156/7/2608 8786326

18. Silberman DM, Wald MR, Genaro AM. Acute and chronic stress exert opposing effects on antibody responses associated with changes in stress hormone regulation of T-lymphocyte reactivity. J Neuroimmunol. 2003;144: 53–60. doi: 10.1016/j.jneuroim.2003.08.031 14597098

19. Webster Marketon JI, Glaser R. Stress hormones and immune function. Cell Immunol. 2008;252: 16–26. doi: 10.1016/j.cellimm.2007.09.006 18279846

20. Barsotti AMG, de Assis VR, Titon SCM, Titon B, da Silva Ferreira ZF, Gomes FR. ACTH modulation on corticosterone, melatonin, testosterone and innate immune response in the tree frog Hypsiboas faber. Comp Biochem Physiol -Part A Mol Integr Physiol. Elsevier Inc.; 2017;204: 177–184. doi: 10.1016/j.cbpa.2016.12.002 27923708

21. Assis VR, Titon SCM, Barsotti AMG, Titon B, Gomes FR. Effects of acute restraint stress, prolonged captivity stress and transdermal corticosterone application on immunocompetence and plasma levels of corticosterone on the cururu toad (Rhinella icterica). PLoS One. 2015;10: 1–21. doi: 10.1371/journal.pone.0121005 25831055

22. Gomes FR, Oliveira RV, Assis VR de, Junior BT, Moretti EH, Mendonça MT. Interspecific Variation in Innate Immune Defenses and Stress Response of Toads from Botucatu (São Paulo, Brazil). South Am J Herpetol. 2012;7: 1–8. doi: 10.2994/057.007.0101

23. Graham SP, Kelehear C, Brown GP, Shine R. Corticosterone-immune interactions during captive stress in invading Australian cane toads (Rhinella marina). Horm Behav. Elsevier Inc.; 2012;62: 146–153. doi: 10.1016/j.yhbeh.2012.06.001 22713726

24. Narayan EJ, Hero JM. Repeated thermal stressor causes chronic elevation of baseline corticosterone and suppresses the physiological endocrine sensitivity to acute stressor in the cane toad (Rhinella marina). J Therm Biol. Elsevier; 2014;41: 72–76. doi: 10.1016/j.jtherbio.2014.02.011 24679975

25. Narayan EJ, Cockrem JF, Hero JM. Urinary corticosterone metabolite responses to capture and captivity in the cane toad (Rhinella marina). Gen Comp Endocrinol. 2011;173: 371–377. doi: 10.1016/j.ygcen.2011.06.015 21756910

26. Narayan EJ, Hero JM. Acute thermal stressor increases glucocorticoid response but minimizes testosterone and locomotor performance in the cane toad (Rhinella marina). PLoS One. 2014;9: 1–6. doi: 10.1371/journal.pone.0092090 24643017

27. Titon SCM, Titon Junior B, Assis VR, Kinker GS, Fernandes PACM, Gomes FR. Interplay among steroids, body condition and immunity in response to long-term captivity in toads. Sci Rep. 2018;8: 17168. doi: 10.1038/s41598-018-35495-0 30464319

28. Titon SCM, Assis VR, Titon B Junior, Cassettari B de O, Fernandes PACM, Gomes FR. Captivity effects on immune response and steroid plasma levels of a Brazilian toad (Rhinella schneideri). J Exp Zool Part A Ecol Integr Physiol. 2017;327: 127–138. doi: 10.1002/jez.2078 29356402

29. Narayan E, Hero JM. Urinary corticosterone responses and haematological stress indicators in the endangered Fijian ground frog (Platymantis vitiana) during transportation and captivity. Aust J Zool. 2011;59: 79–85. doi: 10.1071/ZO11030

30. Narayan EJ, Hero J-M, Cockrem JF. Inverse urinary corticosterone and testosterone metabolite responses to different durations of restraint in the cane toad (Rhinella marina). Gen Comp Endocrinol. 2012;179: 345–349. doi: 10.1016/j.ygcen.2012.09.017 23036735

31. Romero LM. Physiological stress in ecology: Lessons from biomedical research. Trends Ecol Evol. 2004;19: 249–255. doi: 10.1016/j.tree.2004.03.008 16701264

32. Assis VR, Navas CA, Mendonça MT, Gomes FR. Vocal and territorial behavior in the Smith frog (Hypsiboas faber): Relationships with plasma levels of corticosterone and testosterone. Comp Biochem Physiol—A Mol Integr Physiol. Elsevier Inc.; 2012;163: 265–271. doi: 10.1016/j.cbpa.2012.08.002 22903053

33. DuRant SE, Hopkins WA, Davis AK, Romero LM. Evidence of ectoparasite-induced endocrine disruption in an imperiled giant salamander, the eastern hellbender (Cryptobranchus alleganiensis). J Exp Biol. 2015;218: 2297–2304. doi: 10.1242/jeb.118703 26034123

34. Düring K, Porsch P, Mahn A, Brinkmann O, Gieffers W. The non-enzymatic microbicidal activity of lysozymes. FEBS Lett. 1999;449: 93–100. doi: 10.1016/s0014-5793(99)00405-6 10338111

35. Sarma JV, Ward PA. The complement system. Cell Tissue Res. 2011;343: 227–235. doi: 10.1007/s00441-010-1034-0 20838815

36. Buehler DM, Bhola N, Barjaktarov D, Goymann W, Schwabl I, Tieleman BI, et al. Constitutive Immune Function Responds More Slowly to Handling Stress than Corticosterone in a Shorebird. Physiol Biochem Zool. 2008;81: 673–681. doi: 10.1086/588591 18752420

37. French SS, Denardo DF, Greives TJ, Strand CR, Demas GE. Human disturbance alters endocrine and immune responses in the Galapagos marine iguana (Amblyrhynchus cristatus). Horm Behav. Elsevier Inc.; 2010;58: 792–799. doi: 10.1016/j.yhbeh.2010.08.001 20708010

38. Zylberberg M. Common measures of immune function vary with time of day and sampling protocol in five passerine species. J Exp Biol. 2015;218: 757–766. doi: 10.1242/jeb.111716 25617452

39. Hernández-Arciga U, Herrera M LG, Ibáñez-Contreras A, Miranda-Labra RU, Flores-Martínez JJ, Königsberg M. Baseline and post-stress seasonal changes in immunocompetence and redox state maintenance in the fishing bat Myotis vivesi. PLoS One. 2018;13: 1–27. doi: 10.1371/journal.pone.0190047 29293551

40. Hopkins WA, DuRant SE. Innate immunity and stress physiology of eastern hellbenders (Cryptobranchus alleganiensis) from two stream reaches with differing habitat quality. Gen Comp Endocrinol. Elsevier Inc.; 2011;174: 107–115. doi: 10.1016/j.ygcen.2011.08.006 21872597

41. Tort L. Stress and immune modulation in fish. Dev Comp Immunol. Elsevier Ltd; 2011;35: 1366–1375. doi: 10.1016/j.dci.2011.07.002 21782845

42. Thomas JR, Woodley SK. Treatment with corticosterone delays cutaneous wound healing in male and female salamanders. Gen Comp Endocrinol. Elsevier Inc.; 2015;216: 33–38. doi: 10.1016/j.ygcen.2015.04.013 25913258

43. Campbell T. Hematology of Amphibians. In: Trall M, editor. Veterinary Hematology and Clinical Chemistry. Oxford, UK.: John Wiley & Sons, Inc; 2012.

44. Assis VR de Titon SCM, Barsotti AMG, Spira B, Gomes FR. Antimicrobial Capacity of Plasma from Anurans of the Atlantic Forest. South Am J Herpetol. 2013;8: 155–160. doi: 10.2994/SAJH-D-13-00007.1

45. Titon SCM, de Assis VR, Titon B, Barsotti AMG, Flanagan SP, Gomes FR. Calling rate, corticosterone plasma levels and immunocompetence of Hypsiboas albopunctatus. Comp Biochem Physiol -Part A Mol Integr Physiol. Elsevier Inc.; 2016;201: 53–60. doi: 10.1016/j.cbpa.2016.06.023 27364933


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