Neuroendocrine mechanisms for immune system regulation during stress in fish

Fish and Shellfish Immunology

Volumn 40, Issue 2, 2014, Pages 531-538

  Nardocci, Gino ^a   Navarro, Cristina ^a   Cortés, Paula P ^a   Imarai, Mónica ^b   Montoya, Margarita ^b   Valenzuela, Beatriz ^b   Jara, Pablo ^b   Acuña Castillo, Claudio ^b   Fernández, Ricardo ^a  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

^b UNIVERSIDAD DE SANTIAGO DE CHILE   (Chile)

Author keywords

Fish; Hypothalamus pituitary interrenal axis; Immunology; Neuroendocrine; Stress

Indexed keywords

ANIMAL; FISH; IMMUNE SYSTEM; IMMUNOLOGY; NEUROSECRETION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; FISHES; IMMUNE SYSTEM; NEUROSECRETORY SYSTEMS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84908256502     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2014.08.001     Document Type: Review

References (106)

1. McEwen B.S., Wingfield J.C. The concept of allostasis in biology and biomedicine. Horm Behav 2003, 43:2-15.
2. McEwen B.S., Gianaros P.J. Stress- and allostasis-induced brain plasticity. Annu Rev Med 2011, 62:431-445.
3. McEwen B.S., Wingfield J.C. What is in a name? Integrating homeostasis, allostasis and stress. Horm Behav 2010, 57:105-111.
4. Elenkov I.J., Chrousos G.P. Stress system-organization, physiology and immunoregulation. Neuroimmunomodulation 2006, 13:257-267.
5. Edwards K.M., Burns V.E., Carroll D., Drayson M., Ring C. The acute stress-induced immunoenhancement hypothesis. Exerc Sport Sci Rev 2007, 35:150-155.
6. Fast M.D., Hosoya S., Johnson S.C., Afonso L.O. Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short- and long-term stress. Fish Shellfish Immunol 2008, 24:194-204.
7. Viveros-Paredes J.M., Puebla-Perez A.M., Gutierrez-Coronado O., Sandoval-Ramirez L., Villasenor-Garcia M.M. Dysregulation of the Th1/Th2 cytokine profile is associated with immunosuppression induced by hypothalamic-pituitary-adrenal axis activation in mice. Int Immunopharmacol 2006, 6:774-781.
8. Weyts F.A., Flik G., Rombout J.H., Verburg-van Kemenade B.M. Cortisol induces apoptosis in activated B cells, not in other lymphoid cells of the common carp, Cyprinus carpio L. Dev Comp Immunol 1998, 22:551-562.
9. Pacak K., Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 2001, 22:502-548.
10. Barton B.A. Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 2002, 42:517-525.
11. Pacak K., Baffi J.S., Kvetnansky R., Goldstein D.S., Palkovits M. Stressor-specific activation of catecholaminergic systems: implications for stress-related hypothalamic-pituitary-adrenocortical responses. Adv Pharmacol 1998, 42:561-564.
12. Turnbull A.V., Rivier C.L. Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev 1999, 79:1-71.
13. Sorensen C., Bohlin L.C., Overli O., Nilsson G.E. Cortisol reduces cell proliferation in the telencephalon of rainbow trout (Oncorhynchus mykiss). Physiol Behav 2011, 102:518-523.
14. Sorensen C., Nilsson G.E., Summers C.H., Overli O. Social stress reduces forebrain cell proliferation in rainbow trout (Oncorhynchus mykiss). Behav Brain Res 2012, 227:311-318.
15. Engelsma M.Y., Hougee S., Nap D., Hofenk M., Rombout J.H., van Muiswinkel W.B., et al. Multiple acute temperature stress affects leucocyte populations and antibody responses in common carp, Cyprinus carpio L. Fish Shellfish Immunol 2003, 15:397-410.
16. Terova G., Gornati R., Rimoldi S., Bernardini G., Saroglia M. Quantification of a glucocorticoid receptor in sea bass (Dicentrarchus labrax, L.) reared at high stocking density. Gene 2005, 357:144-151.
17. Wendelaar Bonga S.E. The stress response in fish. Physiol Rev 1997, 77:591-625.
18. Weyts F.A., Flik G., Verburg-van Kemenade B.M. Cortisol inhibits apoptosis in carp neutrophilic granulocytes. Dev Comp Immunol 1998, 22:563-572.
19. Godin P.J., Buchman T.G. Uncoupling of biological oscillators: a complementary hypothesis concerning the pathogenesis of multiple organ dysfunction syndrome. Crit Care Med 1996, 24:1107-1116.
20. Herman J.P., McKlveen J.M., Solomon M.B., Carvalho-Netto E., Myers B. Neural regulation of the stress response: glucocorticoid feedback mechanisms. Braz J Med Biol Res 2012, 45:292-298.
21. Freeman M.E., Kanyicska B., Lerant A., Nagy G. Prolactin: structure, function, and regulation of secretion. Physiol Rev 2000, 80:1523-1631.
22. Hart B.B., Stanford G.G., Ziegler M.G., Lake C.R., Chernow B. Catecholamines: study of interspecies variation. Crit Care Med 1989, 17:1203-1222.
23. Elenkov I.J., Wilder R.L., Chrousos G.P., Vizi E.S. The sympathetic nerve-an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 2000, 52:595-638.
24. Fernandez R., Acuna-Castillo C. Neural reflex control of inflammation during sepsis syndromes. Sepsis - an ongoing and significant challenge 2012, 133-156. InTech, Rijeka. L. Azevedo (Ed.).
25. Elenkov I.J., Chrousos G.P. Stress hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends Endocrinol Metab 1999, 10:359-368.
26. Miksa M., Das P., Zhou M., Wu R., Dong W., Ji Y., et al. Pivotal role of the alpha(2A)-adrenoceptor in producing inflammation and organ injury in a rat model of sepsis. PLoS One 2009, 4:e5504.
27. Borovikova L.V., Ivanova S., Zhang M., Yang H., Botchkina G.I., Watkins L.R., et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000, 405:458-462.
28. Wang H., Yu M., Ochani M., Amella C.A., Tanovic M., Susarla S., et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003, 421:384-388.
29. Huston J.M., Ochani M., Rosas-Ballina M., Liao H., Ochani K., Pavlov V.A., et al. Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. JExp Med 2006, 203:1623-1628.
30. Mignini F., Streccioni V., Amenta F. Autonomic innervation of immune organs and neuroimmune modulation. Auton Autacoid Pharmacol 2003, 23:1-25.
31. Berthoud H.R., Powley T.L. Interaction between parasympathetic and sympathetic nerves in prevertebral ganglia: morphological evidence for vagal efferent innervation of ganglion cells in the rat. Microsc Res Tech 1996, 35:80-86.
32. Felten D.L., Ackerman K.D., Wiegand S.J., Felten S.Y. Noradrenergic sympathetic innervation of the spleen: I. Nerve fibers associate with lymphocytes and macrophages in specific compartments of the splenic white pulp. JNeurosci Res 1987, 18:28-36.
33. Reyes E.P., Abarzua S., Martin A., Rodriguez J., Cortes P.P., Fernandez R. LPS-induced c-Fos activation in NTS neurons and plasmatic cortisol increases in septic rats are suppressed by bilateral carotid chemodenervation. Adv Exp Med Biol 2012, 758:185-190.
34. Alvarez-Pellitero P. Diseases caused by flagellates. Fish diseases 2008, 421-515. Science Publishers, Enfield, NH. J. Eiras, H. Segner, B.G. Kapoor (Eds.).
35. Rombout J.H., Huttenhuis H.B., Picchietti S., Scapigliati G. Phylogeny and ontogeny of fish leucocytes. Fish Shellfish Immunol 2005, 19:441-455.
36. Blalock J.E. The immune system as a sensory organ. JImmunol 1984, 132:1067-1070.
37. Ader R., Cohen N., Felten D. Psychoneuroimmunology: interactions between the nervous system and the immune system. Lancet 1995, 345:99-103.
38. Palaksha K.J., Shin G.W., Kim Y.R., Jung T.S. Evaluation of non-specific immune components from the skin mucus of olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol 2008, 24:479-488.
39. Whyte S.K. The innate immune response of finfish - a review of current knowledge. Fish Shellfish Immunol 2007, 23:1127-1151.
40. Secombes C. Will advances in fish immunology change vaccination strategies?. Fish Shellfish Immunol 2008, 25:409-416.
41. Verburg-van Kemenade B.M., Ribeiro C.M., Chadzinska M. Neuroendocrine-immune interaction in fish: differential regulation of phagocyte activity by neuroendocrine factors. Gen Comp Endocrinol 2011, 172:31-38.
42. Chadzinska M., Tertil E., Kepka M., Hermsen T., Scheer M., Verburg-van Kemenade B.M. Adrenergic regulation of the innate immune response in common carp (Cyprinus carpio L.). Dev Comp Immunol 2012, 36:306-316.
43. Arnold R.E., Rice C.D. Channel catfish, Ictalurus punctatus, leukocytes secrete immunoreactive adrenal corticotropin hormone (ACTH). Fish Physiol Biochem 2000, 22:303-310.
44. Weyts F.A., Cohen N., Flik G., Verburg-van Kemenade B.M. Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish Shellfish Immunol 1999, 9:1-20.
45. Gallo V.P., Civinini A. Survey of the adrenal homolog in teleosts. Int Rev Cytol 2003, 230:89-187.
46. Verburg-van Kemenade B.M., Nowak B., Engelsma M.Y., Weyts F.A. Differential effects of cortisol on apoptosis and proliferation of carp B-lymphocytes from head kidney, spleen and blood. Fish Shellfish Immunol 1999, 9:405-415.
47. Mommsen T., Vijayan M., Moon T.W. Cortisol in teleost: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 1999, 9:211-268.
48. Huising M.O., Metz J.R., van S.C., Taverne-Thiele A.J., Hermsen T., Verburg-van Kemenade B.M., et al. Structural characterisation of a cyprinid (Cyprinus carpio L.) CRH, CRH-BP and CRH-R1, and the role of these proteins in the acute stress response. JMol Endocrinol 2004, 32:627-648.
49. Metz J.R., Huising M.O., Meek J., Taverne-Thiele A.J., Wendelaar Bonga S.E., Flik G. Localization, expression and control of adrenocorticotropic hormone in the nucleus preopticus and pituitary gland of common carp (Cyprinus carpio L.). JEndocrinol 2004, 182:23-31.
50. Thornton J.W. Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci U S A 2001, 98:5671-5676.
51. Stolte E.H., van Kemenade B.M., Savelkoul H.F., Flik G. Evolution of glucocorticoid receptors with different glucocorticoid sensitivity. JEndocrinol 2006, 190:17-28.
52. Bridgham J.T., Carroll S.M., Thornton J.W. Evolution of hormone-receptor complexity by molecular exploitation. Science 2006, 312:97-101.
53. Ducouret B., Tujague M., Ashraf J., Mouchel N., Servel N., Valotaire Y., et al. Cloning of a teleost fish glucocorticoid receptor shows that it contains a deoxyribonucleic acid-binding domain different from that of mammals. Endocrinology 1995, 136:3774-3783.
54. Stolte E.H., Nabuurs S.B., Bury N.R., Sturm A., Flik G., Savelkoul H.F., et al. Stress and innate immunity in carp: corticosteroid receptors and pro-inflammatory cytokines. Mol Immunol 2008, 46:70-79.
55. Stolte E.H., de Mazon A.F., Leon-Koosterziel K.M., Jesiak M., Bury N.R., Sturm A., et al. Corticosteroid receptors involved in stress regulation in common carp, Cyprinus carpio. JEndocrinol 2008, 198:403-417.
56. Acerete L., Balasch J.C., Castellana B., Redruello B., Roher N., Canario A.V., et al. Cloning of the glucocorticoid receptor (GR) in gilthead seabream (Sparus aurata). Differential expression of GR and immune genes in gilthead seabream after an immune challenge. Comp Biochem Physiol B Biochem Mol Biol 2007, 148:32-43.
57. Saeij J.P., Verburg-van Kemenade L.B., van Muiswinkel W.B., Wiegertjes G.F. Daily handling stress reduces resistance of carp to Trypanoplasma borreli: invitro modulatory effects of cortisol on leukocyte function and apoptosis. Dev Comp Immunol 2003, 27:233-245.
58. Metz J.R., Huising M.O., Leon K., Verburg-van Kemenade B.M., Flik G. Central and peripheral interleukin-1beta and interleukin-1 receptor I expression and their role in the acute stress response of common carp, Cyprinus carpio L. JEndocrinol 2006, 191:25-35.
59. Law W.Y., Chen W.H., Song Y.L., Dufour S., Chang C.F. Differential invitro suppressive effects of steroids on leukocyte phagocytosis in two teleosts, tilapia and common carp. Gen Comp Endocrinol 2001, 121:163-172.
60. Wang R., Belosevic M. The invitro effects of estradiol and cortisol on the function of a long-term goldfish macrophage cell line. Dev Comp Immunol 1995, 19:327-336.
61. Esteban M.A., Rodriguez A., Ayala A.G., Meseguer J. Effects of high doses of cortisol on innate cellular immune response of seabream (Sparus aurata L.). Gen Comp Endocrinol 2004, 137:89-98.
62. Pagniello K.B., Bols N.C., Lee L.E. Effect of corticosteroids on viability and proliferation of the rainbow trout monocyte/macrophage cell line, RTS11. Fish Shellfish Immunol 2002, 13:199-214.
63. Gadan K., Marjara I.S., Sundh H., Sundell K., Evensen O. Slow release cortisol implants result in impaired innate immune responses and higher infection prevalence following experimental challenge with infectious pancreatic necrosis virus in Atlantic salmon (Salmo salar) parr. Fish Shellfish Immunol 2012, 32:637-644.
64. Saha N.R., Usami T., Suzuki Y. Invitro effects of steroid hormones on IgM-secreting cells and IgM secretion in common carp (Cyprinus carpio). Fish Shellfish Immunol 2004, 17:149-158.
65. Saha N.R., Usami T., Suzuki Y. Adouble staining flow cytometric assay for the detection of steroid induced apoptotic leucocytes in common carp (Cyprinus carpio). Dev Comp Immunol 2003, 27:351-363.
66. Weyts F.A., Verburg-van Kemenade B.M., Flik G., Lambert J.G., Wendelaar Bonga S.E. Conservation of apoptosis as an immune regulatory mechanism: effects of cortisol and cortisone on carp lymphocytes. Brain Behav Immun 1997, 11:95-105.
67. Flik G., Klaren P.H., van den Burg E.H., Metz J.R., Huising M.O. CRF and stress in fish. Gen Comp Endocrinol 2006, 146:36-44.
68. Alderman S.L., McGuire A., Bernier N.J., Vijayan M.M. Central and peripheral glucocorticoid receptors are involved in the plasma cortisol response to an acute stressor in rainbow trout. Gen Comp Endocrinol 2012, 176:79-85.
69. Arends R.J., Mancera J.M., Munoz J.L., Wendelaar Bonga S.E., Flik G. The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. JEndocrinol 1999, 163:149-157.
70. Weld M.M., Fryer J.N., Rivier J., Lederis K. Inhibition of CRF- and urotensin I-stimulated ACTH release from goldfish pituitary cell columns by the CRF analogue alpha-helical CRF-(9-41). Regul Pept 1987, 19:273-280.
71. Baker B.I., Bird D.J., Buckingham J.C. Salmonid melanin-concentrating hormone inhibits corticotrophin release. JEndocrinol 1985, 106:R5-R8.
72. Baker B.I., Bird D.J., Buckingham J.C. Effects of chronic administration of melanin-concentrating hormone on corticotrophin, melanotrophin, and pigmentation in the trout. Gen Comp Endocrinol 1986, 63:62-69.
73. Baker B.I., Rance T.A. Differences in concentrations of plasma cortisol in the trout and the eel following adaptation to black or white backgrounds. JEndocrinol 1981, 89:135-140.
74. Gilham I.D., Baker B.I. Ablack background facilitates the response to stress in teleosts. JEndocrinol 1985, 105:99-105.
75. Kawauchi H., Kawazoe I., Tsubokawa M., Kishida M., Baker B.I. Characterization of melanin-concentrating hormone in chum salmon pituitaries. Nature 1983, 305:321-323.
76. Qu D., Ludwig D.S., Gammeltoft S., Piper M., Pelleymounter M.A., Cullen M.J., et al. Arole for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 1996, 380:243-247.
77. Matsuda K., Shimakura S., Maruyama K., Miura T., Uchiyama M., Kawauchi H., et al. Central administration of melanin-concentrating hormone (MCH) suppresses food intake, but not locomotor activity, in the goldfish, Carassius auratus. Neurosci Lett 2006, 399:259-263.
78. Pavlov V.A. Cholinergic modulation of inflammation. Int J Clin Exp Med 2008, 1:203-212.
79. Pavlov V.A., Tracey K.J. Controlling inflammation: the cholinergic anti-inflammatory pathway. Biochem Soc Trans 2006, 34:1037-1040.
80. Kawashima K., Fujii T. The lymphocytic cholinergic system and its contribution to the regulation of immune activity. Life Sci 2003, 74:675-696.
81. Roy B., Rai U. Role of adrenoceptor-coupled second messenger system in sympatho-adrenomedullary modulation of splenic macrophage functions in live fish Channa punctatus. Gen Comp Endocrinol 2008, 155:298-306.
82. Flory C.M. Autonomic innervation of the spleen of the coho salmon, Oncorhynchus kisutch. A histochemical demonstration and preliminary assessment of its immunoregulatory role. Brain Behav Immun 1989, 3:331-344.
83. Jozefowski S.J., Plytycz B. Characterization of beta-adrenergic receptors in fish and amphibian lymphoid organs. Dev Comp Immunol 1998, 22:587-603.
84. Finkenbine S.S., Gettys T.W., Burnett K.G. Beta-adrenergic receptors on leukocytes of the channel catfish, Ictalurus punctatus. Comp Biochem Physiol C Toxicol Pharmacol 2002, 131:27-37.
85. Dugan S.G., Lortie M.B., Nickerson J.G., Moon T.W. Regulation of the rainbow trout (Oncorhynchus mykiss) hepatic beta2-adrenoceptor by adrenergic agonists. Comp Biochem Physiol B Biochem Mol Biol 2003, 136:331-342.
86. Fabbri E., Chen X., Capuzzo A., Moon T.W. Binding kinetics and sequencing of hepatic alpha1-adrenergic receptors in two marine teleosts, mackerel (Scomber scombrus) and anchovy (Engraulis encrasicolus). JExp Zool Part A Ecol Genet Physiol 2008, 309:157-165.
87. Flory C.M. Phylogeny of neuroimmunoregulation: effects of adrenergic and cholinergic agents on the invitro antibody response of the rainbow trout, Onchorynchus mykiss. Dev Comp Immunol 1990, 14:283-294.
88. Flory C.M., Bayne C.J. The influence of adrenergic and cholinergic agents on the chemiluminescent and mitogenic responses of leukocytes from the rainbow trout, Oncorhynchus mykiss. Dev Comp Immunol 1991, 15:135-142.
89. Narnaware Y.K., Baker B.I., Tomlinson M.G. The effect of various stresses, corticosteroids and adrenergic agents on phagocytosis in the rainbow trout Oncorhynchus mykiss. Fish Physiol Biochem 1994, 13:31-40.
90. Chen W.H., Sun L.T., Tsai C.L., Song Y.L., Chang C.F. Cold-stress induced the modulation of catecholamines, cortisol, immunoglobulin M, and leukocyte phagocytosis in tilapia. Gen Comp Endocrinol 2002, 126:90-100.
91. Kepka M., Verburg-van Kemenade B.M., Chadzinska M. Neuroendocrine modulation of the inflammatory response in common carp: adrenaline regulates leukocyte profile and activity. Gen Comp Endocrinol 2013, 188:102-109.
92. Quan N., Banks W.A. Brain-immune communication pathways. Brain Behav Immun 2007, 21:727-735.
93. Perry S.F., Capaldo A. The autonomic nervous system and chromaffin tissue: neuroendocrine regulation of catecholamine secretion in non-mammalian vertebrates. Auton Neurosci 2011, 165:54-66.
94. Mazon A.F., Verburg-van Kemenade B.M., Flik G., Huising M.O. Corticotropin-releasing hormone-receptor 1 (CRH-R1) and CRH-binding protein (CRH-BP) are expressed in the gills and skin of common carp Cyprinus carpio L. and respond to acute stress and infection. JExp Biol 2006, 209:510-517.
95. Yada T. Growth hormone and fish immune system. Gen Comp Endocrinol 2007, 152:353-358.
96. Kelley K.W., Weigent D.A., Kooijman R. Protein hormones and immunity. Brain Behav Immun 2007, 21:384-392.
97. Ottaviani E., Franchini A., Franceschi C. Evidence for the presence of immunoreactive POMC-derived peptides and cytokines in the thymus of the goldfish (Carassius c. auratus). Histochem J 1995, 27:597-601.
98. Mola L., Gambarelli A., Pederzoli A., Ottaviani E. ACTH response to LPS in the first stages of development of the fish Dicentrarchus labrax L. Gen Comp Endocrinol 2005, 143:99-103.
99. Bayne C.J., Levy S. Modulation of the oxidative burst in trout myeloid cells by adrenocorticotropic hormone and catecholamines: mechanisms of action. JLeukoc Biol 1991, 50:554-560.
100. Sharp B.M. Multiple opioid receptors on immune cells modulate intracellular signaling. Brain Behav Immun 2006, 20:9-14.
101. Chadzinska M., Savelkoul H.F., Verburg-van Kemenade B.M. Morphine affects the inflammatory response in carp by impairment of leukocyte migration. Dev Comp Immunol 2009, 33:88-96.
102. Chadzinska M., Hermsen T., Savelkoul H.F., Verburg-van Kemenade B.M. Cloning of opioid receptors in common carp (Cyprinus carpio L.) and their involvement in regulation of stress and immune response. Brain Behav Immun 2009, 23:257-266.
103. Verburg-van Kemenade B.M., Savelkoul H.F., Chadzinska M. Function of the opioid system during inflammation in carp. Ann N Y Acad Sci 2009, 1163:528-532.
104. Ball J.N., Hawkins E.F. Adrenocortical (interrenal) responses to hypophysectomy and adenohypophysial hormones in the teleost Poecilia latipinna. Gen Comp Endocrinol 1976, 28:59-70.
105. Patino R., Xia Z., Gale W.L., Wu C., Maule A.G., Chang X. Novel transcripts of the estrogen receptor alpha gene in channel catfish. Gen Comp Endocrinol 2000, 120:314-325.
106. Cabas I., Rodenas M.C., Abellan E., Meseguer J., Mulero V., Garcia-Ayala A. Estrogen signaling through the G protein-coupled estrogen receptor regulates granulocyte activation in fish. JImmunol 2013, 191:4628-4639.