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Spatial association of renin-containing cells and nerve fibers in developing rat kidney

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Abstract

The development of renin-containing cells and nerve fibers was studied in Sprague-Dawley rat kidneys during the last third of gestation and the first 15 days of postnatal life. Kidney tissue sections were stained for nerve fibers or double stained employing an anti-rat renin polyclonal antibody and a monoclonal antibody (TUJ1) directed against a neuron-specific class III beta-tubulin isotype. Renin-containing cells and nerve fibers were detected at 17 days of gestation, in close spatial relationship along the main branches of the renal artery. During fetal life, renin-containing cells and nerve fibers were spatially associated along arcuate and interlobular arteries, renincontaining cells being also present throughout the entire length of afferent arterioles supplying juxtamedullary glomeruli. During postnatal life the distribution of renincontaining cells progressively shifted to a restricted juxtaglomerular position in afferent arterioles. Simultaneously, density and organization of nerve fibers increased with age along the arterial vascular tree. Our results suggest that innervation of renin-containing cells is present in fetal life and follows the centrifugal pattern of renin distribution and nephrovascular development.

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References

  1. Taugner C, Poulsen K, Hackenthal E, Taugner R (1979) Immunocytochemical localization of renin in mouse kidney. Histochemistry 62: 19–27

    PubMed  Google Scholar 

  2. Barajas L, Powers K, Carretero O, Scicli AG, Inagami T (1986) Immunocytochemical localization of renin and kallikrein in the rat renal cortex. Kidney Int 29: 965–970

    PubMed  Google Scholar 

  3. Gomez RA, Chevalier RL, Sturgill BC, Johns DW, Peach MJ, Carey RM (1986) Maturation of the intrarenal renin distribution in Wistar-Kyoto rats. J Hypertens 4 [Suppl 5]: S31-S33

    Google Scholar 

  4. Richoux JP, Amsaguine S, Grignon G, Bouhnik J, Menard J, Corvol P (1987) Earliest renin-containing cell differentiation during ontogenesis in the rat. An immunocytochemical study. Histochemistry 88: 41–46

    PubMed  Google Scholar 

  5. Minuth M, Hackenthal E, Poulsen K, Rix E, Taugner R (1981) Renin immunocytochemistry of the differentiating juxtaglomerular apparatus. Anat Embryol (Berl) 162: 173–181

    Google Scholar 

  6. Egerer G, Taugner R, Tiedemann K (1984) Renin immunohistochemistry in the mesonephros and metanephros of the pig embryo. Histochemistry 81: 385–390

    PubMed  Google Scholar 

  7. Celio MR, Groscurth P, Inagami T (1985) Ontogeny of renin immunoreactive cells in the human kidney. Anat Embryol (Berl) 173: 149–155

    Google Scholar 

  8. Johnson JA, Davis JO, Witty RT (1971) Effects of catecholamines and renal nerve stimulation on renin release in the non-filtering kidney. Circ Res 29: 646–653

    PubMed  Google Scholar 

  9. Taher MS, McLain LG, McDonald KM, Schrier RW (1976) Effect of beta-adrenergic blockage on renin response to renal nerve stimulation. J Clin Invest 57: 459–465

    PubMed  Google Scholar 

  10. Wagermark J, Ungerstedt U, Ljungqvist A (1968) Sympathetic innervation of the juxtaglomerular cells of the kidney. Circ Res 22: 149–153

    PubMed  Google Scholar 

  11. Dolezel S, Edvinsson L, Owman C, Owman T (1976) Fluorescence histochemistry and autoradiography of adrenergic nerves in the renal juxtaglomerular complex of mammals and man, with special regard to the efferent arteriole. Cell Tissue Res 169: 211–220

    PubMed  Google Scholar 

  12. Barajas L, Muller J (1973) The innervation of the juxtaglomerular apparatus and surrounding tubules: a quantitative analysis by serial section electron microscopy. J Ultrastruct Res 43: 107–132

    PubMed  Google Scholar 

  13. Ferguson M, Ryan GB, Bell C (1988) The innervation of the renal cortex in the dog. An ultrastructural study. Cell Tissue Res 253: 539–546

    PubMed  Google Scholar 

  14. Sripanidkulchai B, Wyss MJ (1987) The development of alfa2-adrenoceptors in the rat kidney: correlation with noradrenergic innervation. Brain Res 400: 91–100

    PubMed  Google Scholar 

  15. Grignolo A, Seidler FJ, Bartolome M, Kuhn CM, Slotkin TA, Schanberg SM (1982) Norepinephrine content of the rat kidney during development: alterations induced by perinatal methadone. Life Sci 31: 3009–3016

    PubMed  Google Scholar 

  16. Nakamura KT, Page WV, Sato T, Klinkefus JM, Robillard JE (1989) Ontogeny of isoproterenol-stimulated renin secretion from sheep renal cortical slices. Am J Physiol 256: R1258-R1263

    PubMed  Google Scholar 

  17. Celio MR (1986) Renin-containing cells in kidney transplants into the anterior eye chamber. Kidney Int 29: 1234–1236

    PubMed  Google Scholar 

  18. El Dahr SS, Gomez RA, Gray MS, Peach MJ, Carey RM, Chevalier RL (1990) Renal nerves modulate renin gene expression and growth in the developing kidney. Pediatr Res 27: 328 A

    Google Scholar 

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

    PubMed  Google Scholar 

  20. Zimmermann HD (1972) Elektronenmikkroskopische Befunde zur Innervation des Nephron nach Untersuchungen an der fetalen Nachniere des Menschen. Zellforschung 129: 65–75

    Google Scholar 

  21. Hsu S-M, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29: 577–580

    PubMed  Google Scholar 

  22. Gomez RA, Sturgill BC, Chevalier RL, Boyd DG, Lessard JL, Owens GK, Peach MJ (1987) Fetal expression of muscle-specific isoactins in multiple organs of the Wistar-Kyoto rat. Cell Tissue Res 250: 7–12

    PubMed  Google Scholar 

  23. Frankfurter A, Binder LI, Rebhun LI (1986) Identification of a neuron-specific beta-tubulin (abstract). Neurosci Abstr 12: 1123

    Google Scholar 

  24. Frankfurter A, Binder LI, Rebhun LI (1986) Limited tissue distribution of a novel beta-tubulin isoform (abstract). J Cell Biol 103: 273a

    Google Scholar 

  25. Lee M, Tuttle JB, Rebhun LI, Cleveland DW, Frankfurter A (1991) The expression and post-translational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton (in press)

  26. Moody SA, Quigg MS, Frankfurter A (1989) Development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti-beta-tubulin monoclonal antibody. J Comp Neurol 279: 567–580

    PubMed  Google Scholar 

  27. Naruse K, Takii Y, Inagami T (1981) Immunohistochemical localization of renin in luteinizing hormone-producing cells of rat pituitary. Proc Natl Acad Sci USA 78: 7579–7583

    PubMed  Google Scholar 

  28. Takii Y, Figueiredo AFS, Inagami T (1985) Application of immunochemical methods to the identification and characterization of rat kidney inactive renin. Hypertension 7: 236–243

    PubMed  Google Scholar 

  29. Childs (Moriarty) GV, Naor Z, Hazum E, Tibolt R, Westlund KN, Hancock MB (1983) Cytochemical characterization of pituitary target cells for biotinylated gonadotropin releasing hormone. Peptides 4: 549–555

    PubMed  Google Scholar 

  30. Bruhl U, Taugner R, Forssmann WG (1974) Studies on the juxtaglomerular apparatus. I. Perinatal development in the rat. Cell Tissue Res 151: 433–456

    PubMed  Google Scholar 

  31. Robillard JE, Nakamura KT, Di Bona GF (1986) Effects of renal denervation on renal responses to hypoxemia in fetal lambs. Am J Physiol 250: F294-F301

    PubMed  Google Scholar 

  32. Robillard JE, Nakamura KT, Wilkin MK, McWeeny OJ, Di Bona GF (1987) Ontogeny of renal hemodynamic response to renal nerve stimulation in sheep. Am J Physiol 252: F605-F612

    PubMed  Google Scholar 

  33. Felder RA, Pelayo JC, Calcagno PL, Eisner GM, Jose PA (1983) Alpha-adrenoceptors in developing kidney. Pediatr Res 17: 177–180

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  35. Gomez RA, Meernik JG, Kuehl WD, Robillard JE (1984) Developmental aspects of the renal response to hemorrhage during fetal life. Pediatr Res 18: 40–46

    PubMed  Google Scholar 

  36. Robillard JE, Ayres NA, Gomez RA, Nakamura KT, Smith FG Jr (1984) Factors controlling aldosterone secretion during hypoxemia in fetal lambs. Pediatr Res 18: 607–611

    PubMed  Google Scholar 

  37. Sariola H, Ekblom P, Henke-Fahle S (1989) Embryonic neurons as in vitro inducers of differentiation of nephrogenic mesenchyme. J Dev Biol 132: 271–281

    Google Scholar 

  38. Gomez RA, Lynch KR, Sturgill BC, Elwood JP, Chevalier RL, Carey RM, Peach MJ (1989) Distribution of renin mRNA and its protein in the developing kidney. Am J Physiol 257: F850-F858

    PubMed  Google Scholar 

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Pupilli, C., Gomez, R.A., Tuttle, J.B. et al. Spatial association of renin-containing cells and nerve fibers in developing rat kidney. Pediatr Nephrol 5, 690–695 (1991). https://doi.org/10.1007/BF00857873

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  • DOI: https://doi.org/10.1007/BF00857873

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