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A role for natriuretic peptide in lipopolysaccharide-induced fever in Pekin ducks (Anas platyrhynchos): is natriuretic peptide an endogenous antipyretic in birds?

Abstract

The febrile mechanism in all vertebrates involves endogenous molecules which mediate and attenuate the fever response. This mechanism is considered phylogenetically conserved, and the molecules are thought to be analogous in different species. The above notion is supported by evidence which show avian and mammalian fevers to have similar mediators. There is, however, a paucity of information regarding the modulators of the avian febrile response. Natriuretic peptides were shown to modulate mammalian fevers and, although natriuretic peptides are also present in birds, they have never been investigated in the context of fever. We induced fever in Pekin ducks with lipopolysaccharide and, at the same time, treated the animals with natriuretic peptide antiserum at a dose that effectively inhibited the known renal actions of endogenously secreted natriuretic peptide. We compared fever responses after ducks received either the antiserum or an appropriate control along with the lipopolysaccharide. The antiserum did not attenuate the fever responses of ducks. Our results differ from the results of a study in rats, which demonstrated natriuretic peptides to be potently antipyretic. This molecule seems to be antipyretic in mammals but not in ducks. We suggest a species variation regarding the ability of natriuretic peptides to modulate fever.

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Abbreviations

LPS:

Lipopolysaccharide

Iv:

Intravenous

Im:

Intramuscular

Anti-BNP:

Brain natriuretic peptide antiserum

NP:

Natriuretic peptide

DTRI:

Differential temperature response index

TRI:

Thermal response index

PG:

Prostaglandin

NO:

Nitric oxide

IL:

Interleukin

TNF:

Tumor necrosis factor

References

  • Bicego KC, Barros RCH, Branco LGS (2007) Physiology of temperature regulation: comparative aspects. Comp Biochem Physiol 147:616–639

    Google Scholar 

  • Blatteis CM (2004) The cytokine-prostaglandin cascade in fever production: fact of fancy? J Therm Biol 29:359–368. doi:10.1016/j.jthermbio.2004.08.008

    Article  CAS  Google Scholar 

  • Boorstein SM, Ewald PW (1987) Costs and benefits of behavioral fever in Melanoplus sanuinipes infected by Nosema acridophagus. Physiol Zool 60:586–595

    Google Scholar 

  • Bronstein SM, Conner WE (1984) Endotoxin-induced behavioural fever in the Madagascar cockroach, Gromphadorhina portentosa. J Insect Physiol 30:327–330

    Article  CAS  Google Scholar 

  • Cabanac M, Guelte LL (1980) Temperature regulation and prostaglandin E1 fever in scorpions. J Physiol 303:365–370

    PubMed  CAS  Google Scholar 

  • Casterlin ME, Reynolds WW (1977) Behavioral fever in anuran amphibian larvae. Life Sci 20:593–596

    PubMed  Article  CAS  Google Scholar 

  • Casterlin ME, Reynolds WW (1979) Fever induced in marine arthropods by prostaglandin E1. Life Sci 25:1601–1604

    PubMed  Article  CAS  Google Scholar 

  • Casterlin ME, Reynolds WW (1980) Fever and antipyresis in the crayfish Cambarus bartoni. J Physiol 303:417–421

    PubMed  CAS  Google Scholar 

  • D’Alecy LG, Kluger MJ (1975) Avian febrile response. J Physiol 253:223–232

    PubMed  CAS  Google Scholar 

  • Davis-Sharts J (1978) Mechanisms and manifestations of fever. Am J Nurs 78(11):1874–1877

    PubMed  Article  CAS  Google Scholar 

  • Dawson NJ, Keber AW (1979) Physiology of heat loss from an extremity: the tail of the rat. Clin Exp Pharmacol Physiol 6:69–80

    PubMed  Article  CAS  Google Scholar 

  • De Bold AJ (1979) Heart atria granularity effects of changes in water-electrolyte balance. Proc Soc Exp Biol Med 161:508–511

    PubMed  Google Scholar 

  • De Bold AJ, Borenstein HB, Veress AT, Sonnenberg H (1981) A rapid and potent natriuretic response to intravenous injection of atrial myocardial extracts in rats. Life Sci 28:89–94

    PubMed  Article  Google Scholar 

  • Ewald P (1980) Evolutionary biology and the treatment of signs and symptoms of infectious disease. J Theor Biol 86:169–176. doi:10.1016/0022-5193(80)90073-9

    PubMed  Article  CAS  Google Scholar 

  • Firth BT, Ralph CL, Boardman TJ (1980) Independent effects of the pineal and a bacterial pyrogen in behavioural thermoregulation in lizards. Nature 285:399–400

    PubMed  Article  CAS  Google Scholar 

  • Fraifeld V, Blaicher-Kulick R, Degen AA, Kaplanski J (1995) Is hypothalamic prostaglandin E2 involved in avian fever? Life Sci 56:1343–1346. doi:10.1016/0024-3205(95)00086-0

    PubMed  Article  CAS  Google Scholar 

  • Grammer RT, Fukumi H, Inagami T, Misono KS (1983) Rat atrial natriuretic factor. Purification and vasorelaxant activity. Biochem Biophys Res Commun 116(2):696–703

    PubMed  CAS  Google Scholar 

  • Gray DA (1993) Pharmacokinetics of atrial natriuretic peptide in Pekin duck. Gen Comp Endocrinol 90:267–271. doi:10.1006/gcen.1993.1126

    Article  Google Scholar 

  • Gray DA (1994a) Role of endogenous atrial natriuretic peptide in volume expansion diuresis and natriuresis of the Pekin duck. J Endocrinol 140:85–90. doi:10.1006/gcen.1994.1014

    PubMed  Article  CAS  Google Scholar 

  • Gray DA (1994b) Atrial natriuretic peptide suppresses osmotically stimulated plasma arginine vasotocin levels in the Pekin duck. Gen Comp Endocrinol 93(1):122–127

    PubMed  Article  CAS  Google Scholar 

  • Gray DA, Downing C, Sayed N (1997) Endogenous plasma atrial natriuretic peptide and the control of salt gland function in Pekin duck. Am J Physiol Regul Integr Comp Physiol 273:R1080–R1085

    CAS  Google Scholar 

  • Gray DA, Maloney SK (1998) Antidiuretic hormone and angiotensin II plasma concentrations in febrile Pekin ducks. J Physiol 511:605–610

    PubMed  Article  CAS  Google Scholar 

  • Gray DA, Schutz H, Gerstberger R (1991) Plasma atrial natriuretic factor responses to blood volume changes in Pekin duck. Endocrinology 128:1655–1660

    PubMed  CAS  Article  Google Scholar 

  • Gray DA, Maloney SK, Kamerman PR (2005) Lipopolysaccharide-induced fever in Pekin ducks is mediated by prostaglandins and nitric oxide and modulated by adrenocortical hormones. Am J Physiol Regul Integr Comp Physiol 289:R1258–R1264

    PubMed  CAS  Google Scholar 

  • Guyton AC, Hall JE (1997) Human physiology and mechanisms of disease. Saunders, Philadelphia

  • Hallman GM, Ortega CE, Towner MC (1990) Effect of bacterial pyrogen on three lizard species. Comp Biochem Physiol A96:383–386

    Article  Google Scholar 

  • Higgins DA, Cromie RL, Srivastava G, Herzbeck H, Schluter C, Gerdes J, Diamanstein T, Flad HD (1993) An examination of the immune system of the duck (Anas platyrhynchos) for factors resembling some defined mammalian cytokines. Dev Comp Immunol 17:341–355. doi:10.1016/0145-305X(93)90006-C

    PubMed  Article  CAS  Google Scholar 

  • Johnson RW, Curtis SE, Dantzer R, Kelley KW (1993) Central and peripheral prostaglandins are involved in sickness behaviour in birds. Physiol Behav 53:127–131

    PubMed  Article  CAS  Google Scholar 

  • Ivanov AT, Romanovsky AA (2004) Prostaglandin E2 as mediator of fever: synthesis and catabolism. Front Biosci 9:1977–1993

    PubMed  Article  CAS  Google Scholar 

  • Klasing KC (1998) Avian macrophages: regulators of local and systemic immune response. Poult Sci 77:983–989. doi:10.1016/0031-9384(93)90020-G

    PubMed  CAS  Google Scholar 

  • Kluger MJ (1991) Fever: role of pyrogens and cryogens. Physiol Rev 71:93–127

    PubMed  CAS  Google Scholar 

  • Kluger MJ, Kozak W, Conn CA, Leon LR, Soszynski D (1996) The adaptive value of fever. Infect Dis Clin North Am 10(1): 1–20. doi 10.1016/S0891-5520(05)70282-8

    Google Scholar 

  • Kozak W, Kozak A (2003) Differential role of nitric oxide synthase isoforms in fever of different etiologies: studies using NOS gene-deficient mice. J Appl Physiol 94:2534–2544

    PubMed  Article  CAS  Google Scholar 

  • Luheshi G, Miller AJ, Brouwer S, Dascombe MJ, Rothwell NJ, Hopkins SJ (1996) Interleukin-1 receptor antagonist inhibits endotoxin fever and systemic interleukin-6 induction in the rat. Am J Physiol Endocrinol Metab 270:E91–E95

    CAS  Google Scholar 

  • Luker FI, Mitchell D, Laburn HP (2000) Fever and motor activity in rats following day and night injections of Staphylococcus aureus cell walls. Am J Physiol Regul Integr Comp Physiol 279:R610–R616

    PubMed  CAS  Google Scholar 

  • Maloney SK, Gray DA (1998) Characteristics of the febrile response in Pekin ducks. J Comp Physiol B 168:177–182

    PubMed  Article  CAS  Google Scholar 

  • McClellan JL, Klir JJ, Morrow LE, Kluger MJ (1994) Central effects of glucocorticoid receptor antagonist RU-38486 on lipopolysaccharide and stressinduced fever. Am J Physiol 267:R705–R711

    PubMed  CAS  Google Scholar 

  • Miyata A, Minamino N, Kangawa K, Matsuo H (1988) Identification of a 29-amino acid natriuretic peptide in chicken heart. Biochem Biophys Res Commun 155:1330–1337. doi:10.1016/S0006-291X(88)81287-7

    PubMed  Article  CAS  Google Scholar 

  • Miyoshi M, Kitagawa Y, Imoto T, Watanabe T (2006) Effect of natriuretic peptide receptor antagonist on lipopolysaccharide-induced fever in rats: is natriuretic peptide and endogenous antipyretic? J Pharmacol Exp Ther 318:1163–1170

    PubMed  Article  CAS  Google Scholar 

  • Monagas WR, Gatten RE Jr (1983) Behavioural fever in the turtles Terrapene carolina and Chrysemys picta. J Therm Biol 8:285–288

    Article  Google Scholar 

  • Morrow LE, McClellan JL, Conn CA, Kluger MJ (1993) Glucocorticoids alter fever and IL-6 responses to psychological stress and to lipopolysaccharide. Am J Physiol Regul Integr Comp Physiol 64:R1010–R1016

    Google Scholar 

  • Muchlinski AE, Stoutenburgh RJ, Hogan JM (1989) Fever response in laboratory-maintained and free-ranging chuckwallas (Sauromalus obesus). Am J Physiol 257:R150–R155

    PubMed  CAS  Google Scholar 

  • Nomoto S (1996) Diurnal variations in fever induced by intravenous LPS injection in pigeons. Pflügers Arch 431:987–989

    PubMed  CAS  Google Scholar 

  • Oka T (2004) Prostaglandin E2 as a mediator of fever: the role of prostaglandin (EP) receptors. Front Biosci 9:3046–3057

    PubMed  Article  CAS  Google Scholar 

  • Pandey KN (2004) Biology of natriuretic peptides and their receptors. Peptides 26:901–932. doi:10.1016/j.peptides.2005.03.055

    Article  CAS  Google Scholar 

  • Reynolds WW, Casterlin ME, Covert JB (1976) Behavioural fever in teleost fishes. Nature 259:41–42

    PubMed  Article  CAS  Google Scholar 

  • Roth J (2006) Endogenous antipyretics. Clin Chim Acta 371:13–24. doi:10.1016/j.cca.2006.02.013

    PubMed  Article  CAS  Google Scholar 

  • Roth J, De Souza GEP (2001) Fever induction pathways: evidence from responses to systemic or local cytokine formation. Braz J Med Biol Res 34:301–314

    PubMed  Article  CAS  Google Scholar 

  • Romanovsky AA, Almeida MC, Aronoff DM, Ivanov AI, Konsman JP, Steiner AA, Turek VF (2005) Fever and hypothermia in systemic inflammation: recent discoveries and revisions. Front Biosci 10:2193–2216. doi:10.2741/1690

    PubMed  Article  CAS  Google Scholar 

  • Rothwell NJ, Luheshi G, Toulmond S (1996) Cytokines and their receptors in the central nervous system: physiology, pharmacology and pathology. Pharmacol Ther 69:85–95. doi:10.1016/0163-7258(95)02033-0

    PubMed  Article  CAS  Google Scholar 

  • Scammell TE, Griffin JD, Elmquist JK, Saper CB (1998) Micro-injection of cyclo-oxygenase inhibitor into the antero-ventral pre-optic region attenuates LPS fever. Am J Physiol 274:R783–R789

    PubMed  CAS  Google Scholar 

  • Schutz H, Gray DA, Gerstberger R (1992) Modulation of kidney function in conscious Pekin ducks by atrial natriuretic factor. Endocrinology 130:678–684

    PubMed  Article  CAS  Google Scholar 

  • Sherman E, Baldwin L, Fernandez G, Deurell E (1991) Fever and thermal tolerance in the toad Bufo marinus. J Therm Biol 16:297–301

    Article  Google Scholar 

  • Sehic C, Szekely M, Ungar L, Oladehin A, Blatteis CM (1996) Hypothalamic prostaglandin E2 during lipopolysaccharide-induced fever in guinea pigs. Brain Res Bull 39:391–399

    PubMed  Article  CAS  Google Scholar 

  • Simon E, Martin R, Simon-Oppermann C (1981) Central nervous versus total body thermosensitivity of the duck. Int J Biometeorol 25(3):249–256. doi:10.1007/BF02184526

    PubMed  Article  CAS  Google Scholar 

  • Simon-Oppermann C, Simon E, Jessen C, Hammel HT (1978) Hypothalamic thermosensitivity in conscious Pekin ducks. Am J Physiol Regul Integr Comp Physiol 235:130–140

    Google Scholar 

  • Springate JE, Fildes RD, Hong SK, Feld LG, Acara M (1987) Renal effects of atrial natriuretic factor in domestic fowl. Life Sci 40:915–920

    PubMed  Article  CAS  Google Scholar 

  • Toop T, Donald JA (2004) Comparative aspects of natriuretic peptide physiology in nonmammalian vertebrates: A review. J Comp Physiol B 174:189–204

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

The care provided for the animals by the Central Animal Service of the University of the Witwatersrand is gratefully appreciated. The procedures of this study were approved by the Animal Ethics Committee of the University of the Witwatersrand (application no: 2007/26/04).

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Correspondence to Manette Marais.

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Communicated by G. Heldmaier.

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Marais, M., Gray, D.A. A role for natriuretic peptide in lipopolysaccharide-induced fever in Pekin ducks (Anas platyrhynchos): is natriuretic peptide an endogenous antipyretic in birds?. J Comp Physiol B 179, 125–132 (2009). https://doi.org/10.1007/s00360-008-0295-3

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  • DOI: https://doi.org/10.1007/s00360-008-0295-3

Keywords

  • Febrile response
  • Lipopolysaccharide
  • Pekin duck
  • Fever
  • Natriuretic peptide