Skip to main content
Log in

The renal nerves in the newborn rat

  • Renal Nerves
  • Original Article
  • Published:
Pediatric Nephrology Aims and scope Submit manuscript

Abstract

Immunocytochemical methods were used to investigate the distribution of afferent [calcitonin gene-related peptide-(CGRP) immunoreactive and substance P-immunoreactive] nerves and efferent (neuropeptide Y-immunoreactive and dopamine β-hydroxylase-immunoreactive) nerves in the kidneys of rats within the 1st day of life. The newborn rat kidney possesses an afferent and efferent innervation. Both afferent and efferent nerves reach the kidney in the same bundles. The afferent sensory fibers predominate overwhelmingly in the renal pelvis and ureter while the efferent fibers clearly predominate in the vasculature. The corticomedullary connective tissue contains both types of innervation with a more prominent afferent innervation (CGRP immunoreactive). Only afferent arterioles of perihilar nephrons were innervated by efferent sympathetic fibers. The distribution and extent of afferent and efferent innervation is consistent with the renal nerves playing a significant role in the transition from fetal to newborn life. The close proximity between afferent and efferent fibers suggests a possible interaction between the two systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Barajas L, Liu L, Powers K (1992) Anatomy of the renal innervation: intrarenal aspects and ganglia of origin. Can J Physiol Pharmacol 70: 735–749

    Google Scholar 

  2. Barajas L, Powers K (1990) Monoaminergic innervation of the rat kidney: a quantitative study. Am J Physiol 259: F503-F511

    Google Scholar 

  3. Geppetti P, Baldi E, Castellucci A, Bianco ED, Santicioli P, Maggi CA, Lippe IT, Amann R, Skofitsch G, Theodorsson E, Manzini S (1989) Calcitonin gene-related peptide in the rat kidney: occurrence, sensitivity to capsaicin, and stimulation of adenylate cyclase. Neuroscience 30: 503–513

    Google Scholar 

  4. Kurtz A, Muff R, Fischer JA (1989) Calcitonin gene products and the kidney. Klin Wochenschr 67: 870–875

    Google Scholar 

  5. Reinecke M, Forssmann WG (1988) Neuropeptide (neuropeptide Y, neurotensin, vasoactive intestinal polypeptide, substance P, calcitonin gene-related peptide, somatostatin) immunohistochemistry and ultrastructure of renal nerves. Histochemistry 89: 1–9

    Google Scholar 

  6. Su HC, Wharton J, Polak JM, Mulderry PK, Ghatei MA, Gibson SJ, Terenghi G, Morrison JFB, Ballesta J, Bloom SR (1986) Calcitonin gene-related peptide immunoreactivity in afferent neurons supplying the urinary tract: combined retrograde tracing and immunohistochemistry. Neuroscience 18: 727–747

    Google Scholar 

  7. Barajas L, Liu L, Nishiyama C (1991) Prenatal and postnatal development of the CGRP-immunoreactive innervation in the rat kidney. Neurosci Lett 133: 219–224

    Google Scholar 

  8. Knight DS, Cicero S, Beal JA (1991) Calcitonin gene-related peptide-immunoreactive nerves in the rat kidney. Am J Anat 190: 31–40

    Google Scholar 

  9. DiBona GF (1982) The functions of the renal nerves. Rev Physiol Biochem Pharmacol 94: 76–181

    Google Scholar 

  10. Robillard JE, Nakamura KT (1988) Neurohormonal regulation of renal function during development. Am J Physiol 254: F771-F779

    Google Scholar 

  11. Gray JA, Kavlock RJ, Seidler FJ, Slotkin TA (1991) Neural factors in the development of renal function — effect of neonatal central catecholaminergic lesions with 6-hydroxydopamine. J Dev Physiol 15: 325–330

    Google Scholar 

  12. Slotkin TA, Lau C, Kavlock RJ, Gray JA, Orband-Miller L, Queen KL, Baker FE, Cameron AM, Anolick L, Haim K, Bartolome M, Bartolome J (1988) Role of sympathetic neurons in biochemical and functional development of the kidney: neonatal sympathectomy with 6-hydroxydopamine. J Pharmacol Exp Ther 246: 427–433

    Google Scholar 

  13. Slotkin TA, Levant B, Orband-Miller L, Queen KL, Stasheff S (1988) Do sympathetic neurons coordinate cellular development in the heart and kidney? Effects of cardiac and renal nucleic acids and proteins. J Pharmacol Exp Ther 244: 166–172

    Google Scholar 

  14. Slotkin TA, Seidler FJ, Haim K, Cameron AM, Antolick L, Lau C (1988) Neonatal central catecholaminergic lesions with intracisternal 6-hydroxydopamine: effects on development of presynaptic and postsynaptic components of peripheral sympathetic pathways and on the ornithine decarboxylase/polyamine system in heart, lung and kidney. J Pharmacol Exp Ther 247: 975–982

    Google Scholar 

  15. Smith FG, Klinkefus JM, Robillard JE (1992) Effects of volume expansion on renal sympathetic nerve activity, cardiovascular and renal function in lambs. Am J Physiol 262: R651-R658

    Google Scholar 

  16. Smith FG, Smith BA, Guillery EN, Robillard JE (1991) Role of the renal sympathetic nerves in lambs during the transition from fetal to newborn life. J Clin Invest 88: 1988–1994

    Google Scholar 

  17. Page WV, Perlman S, Smith FG, Segar JL, Robillard JE (1992) Renal nerves modulate kidney renin gene expression during the transition from fetal to newborn life. Am J Physiol 262: R459-R463

    Google Scholar 

  18. Lundberg JM, Anggard A, Pernow J, Hoekfelt T (1985) Neuropeptide Y-, substance P- and VIP-immunoreactive nerves in cat spleen in relation to autonomic vascular and volume control. Cell Tissue Res 239: 9–18

    Google Scholar 

  19. Marfurt CF, Echtenkamp SF (1991) Sensory Innervation of the rat kidney and ureter as revealed by the anterograde transport of wheat germ agglutinin-horseradish peroxidase (WGA-HRP) from dorsal root ganglia. J Comp Neurol 311: 389–404

    Google Scholar 

  20. Moss NG (1989) Electrophysiological characteristic of renal sensory receptors and afferent nerves. Miner Electrolyte Metab 15: 59–65

    Google Scholar 

  21. Dixon JS, Gosling JA (1971) Histochemical and electron microscopic observations on the innervations of the upper segment of the mammalian ureter. J Anat 110: 57–66

    Google Scholar 

  22. Ferguson M, Bell C (1988) Ultrastructural localization and characterization of sensory nerves in the rad kidney. J Comp Neurol 274: 9–16

    Google Scholar 

  23. Maggi CA, Theodorsson E, Santicioli P, Giuliani S (1992) Tachykinins and calcitonin gene-related peptide as co-transmitters in local motor responses produced by sensory nerve activation in the guineapig isolated renal pelvis. Neuroscience 46: 546–559

    Google Scholar 

  24. McKenna OC, Angelakos ET (1970) Development of adrenergic innervation in the puppy kidney. Anat Rec 167: 115–126

    Google Scholar 

  25. Gattone VH, Evan AP, Overhage JM, Severs WB (1990) Developing renal innervation in the spontaneously hypertensive rat: evidence for a role of the sympathetic nervous system in renal damage. J Hypertens 8: 423–428

    Google Scholar 

  26. Casellas D, Navar LG (1984) In vitro perfusion of juxtamedullary nephrons in rats. Am J Physiol 246: F349-F358

    Google Scholar 

  27. Casellas D, Moore LC (1990) Autoregulation and tubuloglomerular feeback in juxtamedullary glomerular arterioles. Am J Physiol 258: F660-F669

    Google Scholar 

  28. Pupilli C, Gomez RA, Tuttle JB, Peach MJ, Carey RM (1991) Spatial association of renin-containing cells and nerve fibers in developing rat kidney. Pediatr Nephrol 5: 690–695

    Google Scholar 

  29. Allen JM, Raine AEG, Ledingham JGG, Bloom SR (1985) Neuropeptide Y: a novel renal peptide with vasoconstrictor and natriuretic activity. Clin Sci 68: 373–377

    Google Scholar 

  30. Ballesta J, Polak JM, Allen JM, Bloom SR (1984) The nerves of the juxtaglomerular apparatus of man and other mammals contain potent peptide NPY. Histochemistry 80: 483–485

    Google Scholar 

  31. Westfall TC, Chen X, Ciarleglio A, Henderson K, Del Valle K, Curfman-Falvey M, Naes L (1990) In vitro effects of neuropeptide Y at the vascular neuroeffector junction. Ann NY Acad Sci 611: 145–155

    Google Scholar 

  32. Lundberg JM, Pernow J, Tatemoto K, Dahloef C (1985) Pre-and postjunctional effects of NPY on sympathetic control of rat femoral artery. Acta Physiol Scand 123: 511–513

    Google Scholar 

  33. Kawasaki H, Nuki C, Saito A, Takasaki K (1990) Adrenergic modulation of calcitonin gene-related peptide (CGRP)-containing nervemediated vasodilation in the rat mesenteric resistance vessel. Brain Res 506: 287–290

    Google Scholar 

  34. Kawasaki H, Nuki C, Saito A, Takasaki K (1990) Role of calcitonin gene-related peptide-containing nerves in the vascular adrenergic neurotransmission. J Pharmacol Exp Ther 252: 403–409

    Google Scholar 

  35. Kawasaki H, Nuki C, Saito A, Takasaki K (1991) NPY modulates neurotransmission of CGRP-containing vasodilator nerves in rat mesenteric arteries. Am J Physiol 261: H683-H690

    Google Scholar 

  36. Kopp UC (1989) Renorenal reflexes in normotension and hypertension. Miner Electrolyte Metab 15: 66–73

    Google Scholar 

  37. Kopp UC, Smith LA, DiBona GF (1985) Renorenal reflexes: neural components of ipsilateral and contralateral renal responses. Am J Physiol 249: F507-F517

    Google Scholar 

  38. Kopp UC, Smith LA, DiBona GF (1987) Facilitatory role of renal efferent nerve activity on renal sensory receptors. Am J Physiol 253: F767-F777

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barajas, L., Liu, L. The renal nerves in the newborn rat. Pediatr Nephrol 7, 657–666 (1993). https://doi.org/10.1007/BF00852575

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00852575

Key words

Navigation