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Mapping of NPR-B immunoreactivity in the brainstem of Macaca fascicularis

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Abstract

C-type natriuretic peptide (CNP), the most abundant natriuretic peptide hormone in the brain, plays an important role in neuroendocrine function. The physiological effects of CNP are mediated by the natriuretic peptide receptor-B (NPR-B). Although CNP and NPR-B have been detected in several brain regions, little is known about the neuroanatomical localization of NPR-B protein in the brainstem. In the present study, we investigated the topographical distribution of NPR-B immunoreactivity in the monkey brainstem. The data demonstrate widespread NPR-B immunoreactivity throughout the brainstem. NPR-B immunoreactivity was located in the superior colliculus, inferior colliculus, periaqueductal gray, oculomotor nucleus, red nucleus, ventral tegmental area, substantia nigra, and cerebral peduncle of the midbrain, as well as in the abducens nucleus, medial vestibular nucleus, lateral vestibular nucleus, parabrachial nucleus, locus coeruleus, trigeminal motor nucleus, pontine reticular nucleus, facial nucleus, oral part of the spinal trigeminal nucleus, cochlear nucleus, raphe magnus nucleus, raphe pallidus nucleus, pontine nucleus of the pons, the dorsal motor nucleus of the vagus, hypoglossal nucleus, nucleus tractus solitarius, gracile nucleus, cuneate nucleus, medial vestibular nucleus, spinal trigeminal nucleus, nucleus ambiguus, lateral paragigantocellular nucleus, lateral reticular nucleus, and the inferior olivary nucleus of the medulla oblongata. The widespread distribution of NPR-B-immunoreactive structures throughout the monkey brainstem indicates that CNP may be involved in several physiological mechanisms, acting as a neurotransmitter and/or neuromodulator.

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References

  • Abdelalim EM, Takada T, Torii R, Tooyama I (2006) Molecular cloning of BNP from heart and its immunohistochemical localization in the hypothalamus of monkey. Peptides 27:1886–1893

    Article  PubMed  CAS  Google Scholar 

  • Abdelalim EM, Osman AHK, Takada T, Torii R, Tooyama I (2007) Immunohistochemical mapping of NPR-A in the brainstem of Macaca fascicularis. Neuroscience 145:1087–1096

    Article  PubMed  CAS  Google Scholar 

  • Abdelalim EM, Masuda C, Bellier JP, Saito A, Yamamoto S, Mori N, Tooyama I (2008a) Distribution of natriuretic peptide receptor-C immunoreactivity in the rat brainstem and its relationship to cholinergic and catecholaminergic neurons. Neuroscience 155:192–202

    Article  PubMed  CAS  Google Scholar 

  • Abdelalim EM, Masuda C, Tooyama I (2008b) Expression of natriuretic peptide-activated guanylate cyclases by cholinergic and dopaminergic amacrine cells of the rat retina. Peptides 29:622–628

    Article  PubMed  CAS  Google Scholar 

  • Anand-Srivastava MB, Trachte GT (1993) Atrial natriuretic factor receptors and signal transduction mechanisms. Pharmacol Rev 45:455–497

    PubMed  CAS  Google Scholar 

  • Anselmo-Francil JA, Rocha MJA, Peres-Polon VL, Moreira ER, Antunes-Rodrigues J, Franci CR (1999) Role of the locus coeruleus on blood pressure response and atrial natriuretic peptide secretion following extracellular volume expansion. Brain Res Bull 50:173–177

    Article  Google Scholar 

  • Brown DL, Guyenet PG (1984) Cardiovascular neurons of brainstem with projections to spinal cord. Am J Physiol 247:R1009–R1016

    PubMed  CAS  Google Scholar 

  • Burry RW (2000) Specificity controls for immunocytochemical methods. J Histochem Cytochem 48:163–165

    Article  PubMed  CAS  Google Scholar 

  • Cameron VA, Cumming SA, Espiner EA, Nicholls G, Richards M (2001) C-type natriuretic peptide expression in olfactory regions of rat brain is modulated by acute water deprivation, salt loading and central angiotensin II. Neuroendocrinology 73:46–53

    Article  PubMed  CAS  Google Scholar 

  • Carrive P, Bandler R, Dampney RA (1989) Viscerotopic control of regional vascular beds by discrete groups of neurons within the midbrain periaqueductal gray. Brain Res 493:385–390

    Article  PubMed  CAS  Google Scholar 

  • Chamberlin NL, Saper CB (1992) Topographic organization of cardiovascular responses to electrical and glutamate microstimulation of the parabrachial nucleus of the rat. J Comp Neurol 326:245–262

    Article  PubMed  CAS  Google Scholar 

  • Charles CJ, Richards AM, Espiner EA (1992) Central C-type natriuretic peptide but not atrial natriuretic factor lowers blood pressure and adrenocortical secretion in normal conscious sheep. Endocrinology 131:1721–1726

    Article  PubMed  CAS  Google Scholar 

  • Decker JM, Wojtowicz AM, Liotta BA, Braunewell KH, Heinemann U, Behrens CJ (2010) C-type natriuretic peptide modulates bidirectional plasticity in hippocampal area in CA1 in vitro. Neuroscience 169:8–22

    Article  PubMed  CAS  Google Scholar 

  • Deschepper CF, Picard S (1994) Effects of C-type natriuretic peptide on rat astrocytes: regional differences and characterization of receptors. J Neurochem 62:1974–1982

    Article  PubMed  CAS  Google Scholar 

  • Dev BR, Nandakumaran M, Philip L, John SJ (1998) Brain natriuretic peptide-mediated changes in the extracellular neurotransmitter turnover in the rostral ventrolateral medulla. Neuroscience 84:255–262

    Article  PubMed  CAS  Google Scholar 

  • Ermirio R, Ruggeri P, Cogo CE, Molinari C, Calaresu FR (1989) Neuronal and cardiovascular responses to ANF microinjected into the solitary nucleus. Am J Physiol 256:R577–R582

    PubMed  CAS  Google Scholar 

  • Ermirio R, Ruggeri P, Cogo CE, Molinari C, Calaresu FR (1991) Neuronal and cardiovascular responses to ANF microinjected into nucleus ambiguus. Am J Physiol 260:R1089–R1094

    PubMed  CAS  Google Scholar 

  • Espiner EA, Richards AM, Yandle TG, Nicholls MG (1995) Natriuretic hormones. Endocrinol Metab Clin North Am 24:481–509

    PubMed  CAS  Google Scholar 

  • Fernandez-Durango R, Nunez DJ, Brown MJ (1995) Messenger RNAs encoding the natriuretic peptides and their receptors are expressed in the eye. Exp Eye Res 61:723–729

    Article  PubMed  CAS  Google Scholar 

  • Fiscus RR, Tu AW, Chew SB (2001) Natriuretic peptides inhibit apoptosis and prolong the survival of serum-deprived PC12 cells. Neuroreport 12:185–189

    Article  PubMed  CAS  Google Scholar 

  • Garbers DL (1992) Guanylyl cyclase receptors and their endocrine, paracrine and autocrine ligands. Cell 71:1–4

    Article  PubMed  CAS  Google Scholar 

  • Garbers DL, Chrisman TD, Wiegn P, Katafuchi T, Albanesi JP, Bielinski V, Barylko B, Redfield MM, Burnett JC Jr (2006) Membrane guanylyl cyclase receptors: an update. Trends Endocrinol Metab 17:251–258

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Imura H, Nakao N, 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

    PubMed  CAS  Google Scholar 

  • Inui K, Murase S, Nosaka S (1994) Facilitation of the arterial baroreflex by the ventrolateral part of the midbrain periaqueductal gray matter in rats. J Physiol 477(Pt 1):89–101

    PubMed  Google Scholar 

  • Jouvert P, Revel MO, Lazaris A, Aunis D, Langley K, Zwiller J (2004) Activation of the cGMP pathway in dopaminergic structures reduces cocaine-induced EGR-1 expression and locomotor activity. J Neurosci 24:10716–10725

    Article  PubMed  CAS  Google Scholar 

  • Koller KJ, Lowe DG, Bennett GL, Minamino N, Kangawa K, Matsuo H, Goeddel DV (1991) Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science 252:120–123

    Article  PubMed  CAS  Google Scholar 

  • Kuhun M (2003) Structure, regulation, and function of mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclase-A. Circ Res 93:700–709

    Article  Google Scholar 

  • Kuribayashi K, Kitaoka Y, Kumai T, Munemasa Y, Kitaoka Y, Isenoumi K, Motoki M, Kogo J, Hayashi Y, Kobayashi D, Ueno S (2006) Neuroprotective effect of atrial natriuretic peptide against NMDA-induced neurotoxicity in the rat retina. Brain Res 1071:34–41

    Article  PubMed  CAS  Google Scholar 

  • Langub MC Jr, Warson RE Jr, Herman JP (1995) Distribution of natriuretic peptide precursor mRNA in the rat brain. J Comp Neurol 356:183–199

    Article  PubMed  CAS  Google Scholar 

  • Levin ER, Gardner DG, Samson WK (1998) Natriuretic peptides. N Engl J Med 339:321–328

    Article  PubMed  CAS  Google Scholar 

  • Maack T (1992) Receptors of atrial natriuretic factors. Annu Rev Physiol 54:11–27

    Article  PubMed  CAS  Google Scholar 

  • Machado BH, Brody MJ (1988) Role of the nucleus ambiguus in the regulation of heart rate and arterial pressure. Hypertension 11:602–607

    PubMed  CAS  Google Scholar 

  • Matsukawa N, Grzesik WJ, Takahashi N, Pandey KN, Pang S, Yamauchi M, Smithies O (1999) The natriuretic peptide clearance receptor locally modulates the physiological effects of the natriuretic peptide system. Proc Nalt Acad Sci USA 96:7403–7408

    Article  CAS  Google Scholar 

  • Nakao K, Ogawa Y, Suga SI, Imura H (1992) Molecular biology and biochemistry of the natriuretic peptide system: II. Natriuretic peptide receptors. J Hypertens 10:1111–1114

    Article  PubMed  CAS  Google Scholar 

  • Paton JFR (1999) Nucleus tractus solitarii: integrating structures. Exp Physiol 84:815–833

    Article  PubMed  CAS  Google Scholar 

  • Potter LR, Abbey-Hosch S, Dickey DM (2006) Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev 27:47–72

    Article  PubMed  CAS  Google Scholar 

  • Reiner A (1994) Catecholaminergic innervation of the basal ganglia in mammals: anatomy and function In: Smeets WJAJ, Reiner A (eds) Phylogeny and development of catecholamine systems in the CNS of vertebrates. Cambridge University Press, Cambridge, pp 247–272

  • Sabbatini ME, Rodriguez MR, Corbo NS, Vatta MS, Bianciotti LG (2005) C-type natriuretic peptide applied to the brain enhances exocrine pancreatic secretion through a vagal pathway. Eur J Pharmacol 524:67–74

    Article  PubMed  CAS  Google Scholar 

  • Schreihofer AM, Guyenet PG (1997) Identification of C1 presympathetic neurons in rat rostral ventrolateral medulla by juxtacellular labeling in vivo. J Comp Neurol 387:524–536

    Article  PubMed  CAS  Google Scholar 

  • Scudder CA, Kaneko CRS, Fuchs AF (2002) The brainstem burst generator for saccadic eye movements. Exp Brain Res 142:439–462

    Article  PubMed  Google Scholar 

  • Sparks DL (1999) Conceptual issues related to the role of the superior colliculus in the control of gaze. Curr Opin Neurobiol 9:698–707

    Article  PubMed  CAS  Google Scholar 

  • Szabo J, Cowan WM (1984) A stereotaxic atlas of the brain of the cynomologus monkey (Macaca fascicularis). J Comp Neurol 222:265–300

    Article  PubMed  CAS  Google Scholar 

  • Telegdy G, Kokavszky K, Nyerges A (1999) Action of C-type natriuretic peptide (CNP) on passive avoidance learning in rats: involvement of transmitters. Eur J Neurosci 11:3302–3306

    Article  PubMed  CAS  Google Scholar 

  • Thiriet N, Jouvert P, Gobaille S, Solov’eva O, Gough B, Aunis D, Ali S, Zwiller J (2001) C-type natriuretic peptide (CNP) regulates cocaine-induced dopamine increase and immediate early gene expression in rat brain. Eur J Neurosci 14:1702–1708

    Article  PubMed  CAS  Google Scholar 

  • Thomas CJ, Rankin AJ, Head GA, Woods RL (1997) ANP enhances bradycardic reflexes in normotensive but not spontaneously hypertensive rats. Hypertension 29:1126–1132

    PubMed  CAS  Google Scholar 

  • Wilcox JN, Augustine A, Goeddel DV, Lowe DG (1991) Differential regional expression of three natriuretic peptide receptor genes within primate tissue. Mol Cell Biol 11:3454–3462

    PubMed  CAS  Google Scholar 

  • Yasoda A, Komatsu Y, Chusho H, Miyazawa T, Ozasa A, Miura M, Kurihara T, Rogi T, Tanaka S, Suda M, Tamura N, Ogawa Y, Nakao K (2004) Overexpression of CNP in chondrocytes rescues achondroplasia through a MAPK-dependent pathway. Nat Med 10:80–86

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by a Grant-in-Aid for Scientific Research (no. 21-09133) from the Japan Society for the Promotion of Science.

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Correspondence to Essam M. Abdelalim.

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Abdelalim, E.M., Tooyama, I. Mapping of NPR-B immunoreactivity in the brainstem of Macaca fascicularis . Brain Struct Funct 216, 387–402 (2011). https://doi.org/10.1007/s00429-011-0313-1

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