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Role of anterior hypothalamic natriuretic peptide in lipopolysaccharide-induced fever in rats

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Abstract

We investigated whether within the preoptic area, natriuretic peptide (NP) acts as an endogenous antipyretic in rats made febrile by systemic administration of bacterial endotoxin (lipopolysaccharide, LPS). Intravenous (i.v.) injection of LPS (2 μg/kg) induced a triphasic fever. The third phase of this fever was (a) significantly enhanced by an intrapreoptic (i.p.o.) injection of the NP-receptor (A-type and B-type) antagonist HS-142-1(1 μg), and (b) significantly attenuated by an i.p.o. injection of atrial NP (ANP, 20 ng). When given i.v., LPS induced significant upregulation of the mRNA coding for C-type NP within the anterior hypothalamus, and tended to upregulate that for ANP. The anterior hypothalamic expression of interleukin-1β mRNA was significantly greater in rats injected i.v. with LPS than in saline-injected rats. These results suggest that NPs produced within the anterior hypothalamus after i.v. injection of LPS may act upon preoptic NP receptors to inhibit the LPS-induced fever, possibly through attenuation of the LPS-induced production of proinflammatory cytokines and/or the subsequent final fever mediator prostaglandin E2.

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References

  • Baxter GF (2004) The natriuretic peptides. An introduction. Basic Res Cardiol 99:71–75

    Article  CAS  PubMed  Google Scholar 

  • Blatteis CM, Li S, Li Z, Feleder C, Perlik V (2005) Cytokines, PGE2 and endotoxic fever: a re-assessment. Prostaglandins Other Lipid Mediat 76:1–18

    CAS  PubMed  Google Scholar 

  • Cartmell T, Luheshi GN, Rothwell NJ (1999) Brain sites of action of endogenous interleukin-1 in the febrile response to localized inflammation in the rat. J Physiol 518(Pt 2):585–594

    Article  CAS  PubMed  Google Scholar 

  • Gabellec MM, Griffais R, Fillion G, Haour F (1995) Expression of interleukin 1α, interleukin 1β and interleukin 1 receptor antagonist mRNA in mouse brain: regulation by bacterial lipopolysaccharide (LPS) treatment. Brain Res Mol Brain Res 31(1–2):122–130

    Article  CAS  PubMed  Google Scholar 

  • Goujon E, Parnet P, Laye S, Combe C, Dantzer R (1996) Adrenalectomy enhances pro-inflammatory cytokines gene expression, in the spleen, pituitary and brain of mice in response to lipopolysaccharide. Mol Brain Res 36:53–62

    Article  CAS  PubMed  Google Scholar 

  • Gutkowska J, Antunes-Rodrigues J, McCann SM (1997) Atrial natriuretic peptide in the brain and pituitary gland. Physiol Rev 77:465–515

    CAS  PubMed  Google Scholar 

  • Harms PG, Ojeda SR (1974) A rapid and simple procedure for chronic cannulation of rat jugular vein. J Appl Physiol 36:391–392

    CAS  PubMed  Google Scholar 

  • Herman JP, Langub MC Jr, Watson RE Jr (1993) Localization of C-type natriuretic peptide mRNA in rat hypothalamus. Endocrinology 133:1903–1906

    Article  CAS  PubMed  Google Scholar 

  • Herman JP, Dolgas CM, Rucker D, Langub MC Jr (1996) Localization of natriuretic peptide-activated guanylate cyclase mRNAs in the rat brain. J Comp Neurol 369:165–187

    Article  CAS  PubMed  Google Scholar 

  • Imura H, Nakao K, Itoh H (1992) The natriuretic peptide system in the brain: implications in the central control of cardiovascular and neuroendocrine functions. Front Neuroendocrinol 13:217–249

    CAS  PubMed  Google Scholar 

  • Jankowski M, Reis AM, Wang D, Gutkowska J (2004) Postnatal ontogeny of natriuretic peptide systems in the rat hypothalamus. Dev Brain Res 152:39–46

    Article  CAS  Google Scholar 

  • Kawata M, Ueda S, Nakao K, Morii N, Kiso Y, Imura H, Sano Y (1985) Immunohistochemical demonstration of α-atrial natriuretic polypeptide-containing neurons in the rat brain. Histochemistry 83(1):1–3

    Article  CAS  PubMed  Google Scholar 

  • Kiemer AK, Vollmar AM (2001) The atrial natriuretic peptide regulates the production of inflammatory mediators in macrophages. Ann Rheum Dis 60:iii68–iii70

    CAS  PubMed  Google Scholar 

  • Komatsu Y, Nakao K, Suga S, Ogawa Y, Mukoyama M, Arai H, Shirakami G, Hosoda K, Nakagawa O, Hama N, Kishimoto I, Imura H (1991) C-type natriuretic peptide (CNP) in rats and humans. Endocrinology 129(2):1104–1106

    Article  CAS  PubMed  Google Scholar 

  • Lange J, Brockway B, Azar S (1991) Telemetric monitoring of laboratory animals: an advanced technique that has come of age. Lab Anim 20:28–31

    Google Scholar 

  • Langub MC Jr, Dolgas CM, Watson RE Jr, Herman JP (1995) The C type natriuretic peptide receptor is the predominant natriuretic peptide receptor mRNA expressed in rat hypothalamus. J Neuroendocrinol 7:305–309

    Article  CAS  PubMed  Google Scholar 

  • Maeder M, Fehr T, Rickli H, Ammann P (2006) Sepsis-associated myocardial dysfunction. Chest 129:1349–1366

    Article  CAS  PubMed  Google Scholar 

  • Matsuda Y (1997) Design and utilization of natriuretic peptide antagonists. In: Samson WK, Levin ER (eds) Contemporary endocrinology: natriuretic peptides in health and disease. Humana Press, Totowa, pp 289–307

    Google Scholar 

  • Minamino N, Aburaya M, Kojima M, Miyamoto K, Kangawa K, Matsuo H (1993) Distribution of C-type natriuretic peptide and its messenger RNA in rat central nervous system and peripheral tissue. Biochem Biophys Res Commun 197:326–335

    Article  CAS  PubMed  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 an endogenous antipyretic? J Pharmacol Exp Ther 318(3):1163–1170

    Article  CAS  PubMed  Google Scholar 

  • Pandey KN (2005) Biology of natriuretic peptides and their receptors. Peptides 26:901–932

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  • Romanovsky A, 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

    Article  CAS  PubMed  Google Scholar 

  • Satta MA, Jacobs RA, Kaltsas GA, Grossman AB (1998) Endotoxin induces interleukin-1β and nitric oxide synthase mRNA in rat hypothalamus and pituitary. Neuroendocrinology 67(2):109–116

    Article  CAS  PubMed  Google Scholar 

  • Totsune K, Takahashi K, Ohneda M, Itoi K, Murakami O, Mouri T (1994) C-type natriuretic peptide in the human central nervous system: distribution and molecular form. Peptides 15(1):37–40

    Article  CAS  PubMed  Google Scholar 

  • Ueda S, Minamino N, Aburaya M, Kangawa K, Matsukura S, Matsuo H (1991) Distribution and characterization of immunoreactive porcine C-type natriuretic peptide. Biochem Biophys Res Commun 175:759–767

    Article  CAS  PubMed  Google Scholar 

  • Vila G, Resl M, Stelzeneder D, Struck J, Maier C, Riedl M, Hulsmann M, Pacher R, Luger A, Clodi M (2008) Plasma NT-proBNP increases in response to LPS administration in healthy men. J Appl Physiol 105:1741–1745

    Article  CAS  PubMed  Google Scholar 

  • Vollmar AM (2005) The role of atrial natriuretic peptide in the immune system. Peptides 26:1086–1094

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Morimoto A, Murakami N (1991) ACTH response in rats during biphasic fever induced by interleukin-1. Am J Physiol Regul Integr Comp Physiol 261:R1104–R1108

    CAS  Google Scholar 

  • Watanabe T, Clark WG, Ceriani G, Lipton JM (1994) Elevation of plasma ACTH concentration in rabbits made febrile by systemic injection of bacterial endotoxin. Brain Res 652:201–206

    Article  CAS  PubMed  Google Scholar 

  • Watson RE Jr, Hutchinson RK, Langub MC Jr, Landis JW, Seksaria S, Rainey DM, Keil LC (1994) Colocalization of natriuretic peptide and estrogen receptor immunoreactivities in preoptic nuclei in the female rat. J Neuroendocrinol 6(1):79–87

    Article  CAS  PubMed  Google Scholar 

  • Weil ZM, Bowers SL, Pyter LM, Nelson RJ (2006) Social interactions alter proinflammatory cytokine gene expression and behavior following endotoxin administration. Brain Behav Immun 20:72–79

    Article  CAS  PubMed  Google Scholar 

  • Woodard GE, Zhao J, Rosado JA, Brown J (2003) Differences between natriuretic peptide receptors in the olfactory bulb and hypothalamus from spontaneously hypertensive and normotensive rat brain. Neurosci Res 47:421–429

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Dr. Robert J. Timms for his critical reading of the English manuscript. We thank Kyowa Hakko Kirin Co. Ltd for the kind supply of HS-142-1. We would like to express our gratitude to Dr Makoto Taniguchi for his valuable suggestions. This work was partly supported by the Ministry of Education, Science and Culture with a Grant-in-Aid for Scientific Research (C19590225).

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Correspondence to Tatsuo Watanabe.

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Miyoshi, M., Watanabe, T. Role of anterior hypothalamic natriuretic peptide in lipopolysaccharide-induced fever in rats. Eur J Appl Physiol 109, 49–57 (2010). https://doi.org/10.1007/s00421-009-1157-8

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