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. 2005 Dec 10;27(2):107–116. doi: 10.1007/s11357-005-1627-9

Decreased alpha-adrenergic constriction of renal preglomerular arteries occurs with age and is gender-specific in the rat

Jeff C Falcone 1,✉, Irving G Joshua 1, John C Passmore 1
PMCID: PMC3458505  PMID: 23598616

Abstract

Age and/or gender appear to moderate alpha-adrenergic mediated constrictor mechanisms found in the interlobar arteries of the Munich Wistar rat. We have determined the extent of constriction to alpha-adrenergic receptor stimulation using norepinephrine, phenylephrine and A61603 (α1A-adrenergic receptor agonist) as a function of age and gender. Norepinephrine produced less constriction in male-derived arteries at ages greater than eight months as compared to the younger adult male (four to six months). The arteries derived from females did not demonstrate altered constriction until greater than 15 months of age. Similarly, arteries derived from the male demonstrated weaker constrictions to phenylephrine (10−6 to 10−3 M) at ages greater than eight months while arteries from females showed differences at greater than 15 months. In contrast, the effective concentration of norepinephrine to cause a 50% maximal constriction (EC50) was significantly less in the four to five-month-old male rats compared to the pooled data from older groups. Interestingly, four to five month old males had A61603 EC50 values similar to the 8 to 12-month and 15+ old females. These studies conclude that an age related loss of sympathetic α-adrenergic constriction of renal interlobar arteries is present in Munich Wistar rats. Furthermore, this loss, while similar along longitudinal aspects of age, is also different as a function of gender with the loss of α-adrenergic constrictor function delayed in the female when compared to the male.

Key words: aging, alpha adrenergic receptors, gender differences, rat, renal preglomerular arteries

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References

  1. Anderson S, Brenner BM. The role of intraglomerular pressure in the initiation and progression of renal disease. J Hypertens Suppl. 1986;4(5):S236–S238. [PubMed] [Google Scholar]
  2. Anderson S, Diamond JR, Karnovsky MJ, Brenner BM. Mechanisms underlying transition from acute glomerular injury to late glomerular sclerosis in a rat model of nephrotic syndrome. J Clin Invest. 1988;82(5):1757–1768. doi: 10.1172/JCI113789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson S, Rennke HG, Zatz R. Glomerular adaptations with normal aging and with long-term converting enzyme inhibition in rats. Am J Physiol. 1994;267(1 Pt. 2):F35–F43. doi: 10.1152/ajprenal.1994.267.1.F35. [DOI] [PubMed] [Google Scholar]
  4. Baylis C. Age-dependent glomerular damage in the rat. Dissociation between glomerular injury and both glomerular hypertension and hypertrophy. Male gender as a primary risk factor. J Clin Invest. 1994;94(5):1823–1829. doi: 10.1172/JCI117531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baylis C. Age dependent glomerular damage in the rat. J Clin Invest. 1996;94:1823–1829. doi: 10.1172/JCI117531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blue DR, Jr, Vimont RL, Clarke DE. Evidence for a noradrenergic innervation to alpha 1A-adrenoceptors in rat kidney. Br J Pharmacol. 1992;107(2):414–417. doi: 10.1111/j.1476-5381.1992.tb12760.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brenner BM, Anderson S. The interrelationships among filtration surface area, blood pressure, and chronic renal disease. J Cardiovasc Pharmacol. 1992;19(Suppl. 6):S1–S7. doi: 10.1097/00005344-199219006-00002. [DOI] [PubMed] [Google Scholar]
  8. Brenner BM, Garcia DL, Anderson S. Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens. 1988;1(4 Pt. 1):335–347. doi: 10.1093/ajh/1.4.335. [DOI] [PubMed] [Google Scholar]
  9. Casellas D, Carmines PK, Navar LG. Microvascular reactivity of in vitro blood perfused juxtamedullary nephrons from rats. Kidney Int. 1985;28:752–759. doi: 10.1038/ki.1985.194. [DOI] [PubMed] [Google Scholar]
  10. Castellani S, Ungar A, Cantini C, Cava G, Serio C, Valloti B. Impaired renal adaptation to stress in the elderly with isolated systolic hypertension. Hypertension. 1999;34:1106–1111. doi: 10.1161/01.hyp.34.5.1106. [DOI] [PubMed] [Google Scholar]
  11. Esler MD, Thompson JM, Kaye DM, Turner AG, Jennings GL, Cox HS. Effects of aging on the responsiveness of the human cardiac sympathetic nerves to stressors. Circulation. 1995;91(2):351–358. doi: 10.1161/01.cir.91.2.351. [DOI] [PubMed] [Google Scholar]
  12. Falcone JC, Davis MJ, Meininger GA. Endothelial independence of the myogenic response in isolated skeletal muscle arterioles. Am J Physiol. 1991;260:H130–H135. doi: 10.1152/ajpheart.1991.260.1.H130. [DOI] [PubMed] [Google Scholar]
  13. Falcone JC, Kuo L, Meininger GA. Endothelial cell calcium increases during flow-induced dilation in isolated arterioles. Am J Physiol. 1993;264:H653–H659. doi: 10.1152/ajpheart.1993.264.2.H653. [DOI] [PubMed] [Google Scholar]
  14. Falcone JC, Granger HJ, Meininger GA. Enhanced myogenic activation in skeletal muscle arterioles from spontaneously hypertensive rats. Am J Physiol. 1993;265:H1847–H1855. doi: 10.1152/ajpheart.1993.265.6.H1847. [DOI] [PubMed] [Google Scholar]
  15. Galbusera M, Garatini S, Remuzzi G, Mennini T. Catecholamine receptor binding in rat kidney: effect of aging. Kidney Int. 1988;33:1073–1077. doi: 10.1038/ki.1988.113. [DOI] [PubMed] [Google Scholar]
  16. Hajduczok G, Chapleau MW, Johnson SL, Abboud FM. Increase in sympathetic activity age: I. Role of impairment of arterial baroreflexes. Am J Physiol. 1991;260:H1113–H1120. doi: 10.1152/ajpheart.1991.260.4.H1113. [DOI] [PubMed] [Google Scholar]
  17. Haley DP, Bulger RE. The aging male rat: structure and function of the kidney. Am J Anat. 1983;167:1–13. doi: 10.1002/aja.1001670102. [DOI] [PubMed] [Google Scholar]
  18. Irigoyen MC, Moreira ED, Werner A, Pires IA, Cestari IA, Kreiger EM. Aging and baroreflex control of RSNA and heart rate in rats. Am J Physiol, Regul Integr Comp Physiol. 2000;279:1865–1871. doi: 10.1152/ajpregu.2000.279.5.R1865. [DOI] [PubMed] [Google Scholar]
  19. Ishikawa Y, Gee MV, Baum BJ, Roth GS. Decreased signal transduction in rat parotid cell aggregates during aging is not due to loss of alpha1 adrenergic receptors. Exp Gerontol. 1989;24:25–36. doi: 10.1016/0531-5565(89)90032-6. [DOI] [PubMed] [Google Scholar]
  20. Jones PP, Christou DD, Jordan J, Seals DR. Baroreflex buffering is reduced with age in healthy men. Circulation. 2003;107:1770–1774. doi: 10.1161/01.CIR.0000057811.86187.88. [DOI] [PubMed] [Google Scholar]
  21. Kenny WL, Zappe DH. Effect of age on renal blood flow during exercise. Aging (Milano) 1994;6:293–302. doi: 10.1007/BF03324255. [DOI] [PubMed] [Google Scholar]
  22. Khraibi AA, Heublein DM, Knox FG, Burnett JC., Jr Increased plasma level of endothelin-1 in the Okamoto spontaneously hypertensive rat. Mayo Clin Proc. 1993;68(1):42–46. doi: 10.1016/s0025-6196(12)60017-2. [DOI] [PubMed] [Google Scholar]
  23. Kuo L, Davis MJ, Chilian WM. Myogenic activity in isolated subepicardial and subendocardial coronary arterioles. Am J Physiol. 1988;255:H1558–H1562. doi: 10.1152/ajpheart.1988.255.6.H1558. [DOI] [PubMed] [Google Scholar]
  24. Lindeman RD. Renal physiology and pathophysiology of aging. Contrib Nephro. 1993;105:1–12. doi: 10.1159/000422463. [DOI] [PubMed] [Google Scholar]
  25. Meyer TW, Anderson S, Brenner BM. Dietary protein intake and progressive glomerular sclerosis: The role of capillary hypertension and hyperperfusion in the progression of renal disease. Ann Intern Med. 1983;98(5 Pt. 2):832–838. doi: 10.7326/0003-4819-98-5-832. [DOI] [PubMed] [Google Scholar]
  26. Miller PL, Rennke HG, Meyer TW. Hypertension and progressive glomerular injury caused by focal glomerular ischemia. Am J Physiol. 1990;259(2 Pt. 2):F239–F245. doi: 10.1152/ajprenal.1990.259.2.F239. [DOI] [PubMed] [Google Scholar]
  27. Miyauchi T, Yanagisawa M, Suzuki N, Iida K, Sugishita T, Fujino M, Saito T, et al. Venous plasma concentrations of endothelin in normal and hypertensive subjects Circulation 1989805732766510 [Google Scholar]
  28. Miyauchi T, Yanagisawa M, Iida K, Ajisaka R, Suzuki N, Fujino M, et al. Age- and sex-related variation of plasma endothelin-1 concentration in normal and hypertensive subjects. Am Heart J. 1992;123(4):1092–1093. doi: 10.1016/0002-8703(92)90734-D. [DOI] [PubMed] [Google Scholar]
  29. Myamoto A, Villalobos-Molina R, Kowatch MA, Roth GS. Altered coupling of alpha 1-adrenergic receptor-G protein in rat parotid during aging. Am J Physiol. 1992;262:C1181–C1188. doi: 10.1152/ajpcell.1992.262.5.C1181. [DOI] [PubMed] [Google Scholar]
  30. Neuringer JR, Brenner BM. Glomerular hypertension: cause and consequence of renal injury. J Hypertens Suppl. 1992;10(7):S91–S97. doi: 10.1097/00004872-199212000-00011. [DOI] [PubMed] [Google Scholar]
  31. Ng AV, Callister R, Johnson DG, Seals DR. Age and gender influence muscle sympathetic nerve activity at rest in healthy humans. Hypertension. 1993;21(4):498–503. doi: 10.1161/01.hyp.21.4.498. [DOI] [PubMed] [Google Scholar]
  32. Parekh VV, Falcone JC, Wills-Frank LA, Joshua IG, Dholakia JN, Passmore JC. Protein kinase B, P34cdc2 kinase, and p21 ras GTP-binding in kidneys of aging rats. Exp Biol Med. 2004;229:850–856. doi: 10.1177/153537020422900819. [DOI] [PubMed] [Google Scholar]
  33. Passmore JC, Rowell PP, Joshua IG, Porter JP, Patel DH and Falcone JC (2005) Alpha 1 adrenergic receptor control of renal blood vessels during aging. Can J Physiol Pharmacol 83 (in press) [DOI] [PubMed]
  34. Properzi G, Cordeschi G, Francavilla S. Postnatal development and distribution of peptide-containing nerves in the genital system of the male rat. Histochemistry. 1992;97:61–68. doi: 10.1007/BF00271282. [DOI] [PubMed] [Google Scholar]
  35. Reckelhoff JF, Samsell L, Dey R, Racusen L, Baylis C. The effect of aging on glomerular hemodynamics in the rat. Am J Kidney Dis. 1992;20(1):70–75. doi: 10.1016/s0272-6386(12)80319-2. [DOI] [PubMed] [Google Scholar]
  36. Remuzzi A, Puntorieri S, Alfano M, Macconi D, Abbate M, Bertani T, et al. Pathophysiologic implications of proteinuria in a rat model of progressive glomerular injury. Lab Invest. 1992;67(5):572–579. [PubMed] [Google Scholar]
  37. Rennke HG. Glomerular adaptations to renal injury or ablation. Role of capillary hypertension in the pathogenesis of progressive glomerulosclerosis. Blood Purif. 1988;6(4):230–239. doi: 10.1159/000169549. [DOI] [PubMed] [Google Scholar]
  38. Robert A, Tran NN, Giummelly P, Atkinson J, Capdeville-Atkinson C. Sensitivity of norepinephrine-evoked vasoconstriction to pertussis toxin in the old rat. Am J Physiol. 1998;274(6 Pt. 2):R1604–R1612. doi: 10.1152/ajpregu.1998.274.6.R1604. [DOI] [PubMed] [Google Scholar]
  39. Roth GS, Brennecke LH, French AW, Williams NG, Waggie KS, Spurgeon HA, et al. Pathological characterization of male Wistar rats from the gerontology research center. J Gerontol. 1993;48:B213–B230. doi: 10.1093/geronj/48.6.B213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sawaki K, Baum BJ, Roth GS, Ambudkar IS. Decreased m3-muscarinic and α1-adrenergic receptor stimulation of PIP2 hydrolysis in parotid gland membranes from aged rats: Defect in activation of Gαq/11. Arch Biochem Biophys. 1995;322(2):319–326. doi: 10.1006/abbi.1995.1470. [DOI] [PubMed] [Google Scholar]
  41. Scolnick M, Tykochinsky G, Servadio C, Abramovici A. The development of vascular supply of normal rat prostate during the sexual maturation: an angiographic study. Prostate. 1992;21:1–14. doi: 10.1002/pros.2990210102. [DOI] [PubMed] [Google Scholar]
  42. Shanley PF. The pathology of chronic renal ischemia. Semin Nephrol. 1996;16(1):21–32. [PubMed] [Google Scholar]
  43. Silbiger SR, Neugarten J. The impact of gender on the progression of chronic renal disease. Am J Kidney Dis. 1995;25:515–533. doi: 10.1016/0272-6386(95)90119-1. [DOI] [PubMed] [Google Scholar]
  44. Simons JL, Provoost AP, Anderson S, Rennke HG, Troy JL, Brenner BM. Modulation of glomerular hypertension defines susceptibility to progressive glomerular injury. Kidney Int. 1994;46(2):396–404. doi: 10.1038/ki.1994.287. [DOI] [PubMed] [Google Scholar]
  45. Stauss HM, Morgan DA, Anderson KE, Massett MP, Kregel KC. Aging is not accompanied by sympathetic hyperresponsiveness to air-jet-stress. Am J Physiol (Heart Circ Physiol) 1996;271:H768–H775. doi: 10.1152/ajpheart.1996.271.2.H768. [DOI] [PubMed] [Google Scholar]
  46. Tidgren B, Hjemdahl P. Renal responses to mental stress and epinephrine in humans. Am J Physiol Renal Fluid Electrolyte Physiol. 1989;257:F682–F689. doi: 10.1152/ajprenal.1989.257.4.F682. [DOI] [PubMed] [Google Scholar]
  47. Wesson LG. Physiology of the Human Kidney. New York: Grune and Stratton; 1969. pp. 99–100. [Google Scholar]
  48. Wolff DW, Gesek FA, Strandhoy JW. In vivo assessment of rat renal alpha adrenoceptors. J Pharmacol Exp Ther. 1987;241:472–476. [PubMed] [Google Scholar]
  49. Young JB, Rowe JW, Pallotta JA, Sparrow D, Landsberg L. Enhanced plasma norepinephrine response to upright posture and oral glucose administration in elderly human subjects. Metabolism. 1980;29(6):532–539. doi: 10.1016/0026-0495(80)90078-5. [DOI] [PubMed] [Google Scholar]
  50. Ziegler MG, Lake CR, Kopin IJ. Plasma noradrenaline increases with age. Nature. 1976;261(5558):333–335. doi: 10.1038/261333a0. [DOI] [PubMed] [Google Scholar]

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