Renal sensory and sympathetic nerves reinnervate the kidney in a similar time-dependent fashion after renal denervation in rats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 304, Issue 8, 2013, Pages

  Mulder, Jan ^a   Hökfelt, Tomas ^a   Knuepfer, Mark M ^b   Kopp, Ulla C ^c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

CGRP; Hypertension; Nerve regeneration; Renal cortex; Renal pelvic wall; Substance P

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; NEUROPEPTIDE Y; SUBSTANCE P; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; KIDNEY CORTEX; KIDNEY DENERVATION; KIDNEY INNERVATION; KIDNEY NERVE; KIDNEY TUBULE PRESSURE; MALE; NONHUMAN; OPTICAL DENSITY; PRIORITY JOURNAL; RAT; REINNERVATION; SYMPATHETIC FUNCTION; ADRENERGIC SYSTEM; ANIMAL; DENERVATION; IMAGE PROCESSING; INNERVATION; KIDNEY; KIDNEY PELVIS; METABOLISM; NERVE REGENERATION; PHYSIOLOGY; REGRESSION ANALYSIS; SENSORY RECEPTOR; SPRAGUE DAWLEY RAT; SYMPATHECTOMY;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; DENERVATION; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY PELVIS; MALE; NERVE REGENERATION; NEUROPEPTIDE Y; RATS; RATS, SPRAGUE-DAWLEY; REGRESSION ANALYSIS; SENSORY RECEPTOR CELLS; SUBSTANCE P; SYMPATHECTOMY; SYMPATHETIC NERVOUS SYSTEM; TYROSINE 3-MONOOXYGENASE;

MLCS; MLOWN;

EID: 84878439419     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00599.2012     Document Type: Article

References (59)

1. Barajas L, Powers K. Monoaminergic innervation of the rat kidney: a quantitative study. Am J Physiol Renal Fluid Electrolyte Physiol 259: F503-F511, 1990.
2. Barajas L, Powers K, Wang P. Innervation of the renal cortical tubules: a quantitative study. Am J Physiol Renal Fluid Electrolyte Physiol 247: F50-F60, 1984.
3. Calaresu FR, Ciriello J. Renal afferent nerves affect discharge rate of medullary and hypothalamic single units in cat. J Auton Nerv Syst 3: 311-320, 1981.
4. Campese VM, Kogosov E. Renal afferent denervation prevents hypertension in rats with chronic renal failure. Hypertension 25: 878-882, 1995.
5. Campese VM, Ku E, Park J. Sympathetic renal innervation and resistant hypertension. Int J Hypertension 2011: 1-6, 2011.
6. Ciriello J, Calaresu FR. Central projection of afferent renal fibers in the rat: an anterograde transport study of horseradish peroxidase. J Auton Nerv Syst 8: 273-285, 1983.
7. Chien CT, Chien HF, Cheng YJ, Chen CF, Hsu SM. Renal afferent signaling diuretic response is impaired in streptozotocin-induced diabetic rats. Kidney Int 57: 203-214, 2000.
8. Christensson-Nylander I, Herrera-Marschitz M, Staines W, Hökfelt T, Terenius L, Ungerstedt U, Cuello C, Oertel WH, Goldstein M. Striato-nigral dynorphin and substance P pathways in the rat. Exp Brain Res 64: 169-192, 1986.
9. Converse RL Jr, Jacobsen TN, Toto RD, Jost CM, Cosentino F, Fouad-Tarazi F, Victor RG. Sympathetic overactivity in patients with chronic renal failure. N Engl J Med 327: 1912-1918, 1992.
10. Couch NP, McBride RA, Dammin GJ, Murray JE. Observations on the nature of the enlargement, the regeneration of the nerves and the function of the canine renal autograft. Br J Exp Pathol 42: 106-113, 1961.
11. DiBona GF, Kopp UC. Neural control of renal function. Physiol Rev 77: 75-197, 1997.
12. DiBona GF, Sawin LL. Renal nerves in renal adaptation to dietary sodium restriction. Am J Physiol Renal Fluid Electrolyte Physiol 245: F322-F328, 1983.
13. Ditting T, Christian Fiedler C, Freisinger W, Siegel K, Heinlein S, Schmidt ST, Neuhuber W, Ott C, Schmieder RE, Amann K, Veelken R. Evidence for afferent reinnervation after renal denervation in rats (Abstract). Hypertension 60: A473, 2012.
14. Esler MD, Krum H, Sobotka PA, Schlaich MP, Schmieder RE, Böhm M. Renal sympathetic denervation in patients with treatment-resistant hypertension (The Symplicity HTN-2 Trial): a randomized controlled trial. Lancet 376: 1903-1909, 2010.
15. Ferguson M, Bell C. Substance P-immunoreactive nerves in the rat kidney. Neurosci Lett 60: 183-188, 1985.
16. Gazdar AF, Dammin GJ. Neural degeneration and regeneration in human renal transplants. N Engl J Med 283: 222-224, 1970.
17. Genovesi S, Pieruzzi F, Wijnmaalen P, Centonza L, Golin R, Zanchetti A, Stella A. Renal afferents signaling diuretic activity in the cat. Circ Res 73: 906-913, 1993.
18. Hausberg M, Kosch M, Harmelink P, Barenbrock M, Hohage H, Kisters K, Dietl KH, Rahn KH. Sympathetic nerve activity in end-stage renal disease. Circulation 106: 1974-1979, 2002.
19. Hering D, Lambert EA, Marusic P, Walton AS, Krum H, Lambert GW, Esler MD, Schlaich MP. Substantial reduction in single sympathetic nerve firing after renal denervation in patients with resistant hypertension. Hypertension 61: 457-464, 2013.
20. Katholi RE, Naftilan AJ, Oparil S. Importance of renal sympathetic tone in the development of DOCA-salt hypertension in the rat. Hypertension 2: 266-273, 1980.
21. Katholi RE, Whitlow PL, Winternitz SR, Oparil S. Importance of the renal nerves in established two-kidney, one-clip Goldblatt hypertension. Hypertension 4: II166-II174, 1982.
22. Katholi RE, Winternitz SR, Oparil S. Role of the renal nerves in the pathogenesis of one-kidney renal hypertension in the rat. Hypertension 3: 404-409, 1981.
23. Kline RL, Mercer PF. Functional reinnervation and development of supersensitivity to NE after denervation. Am J Physiol Regul Integr Comp Physiol 238: R353-R358, 1980.
24. Kopp UC, Buckley-Bleiler RL. Impaired renorenal reflexes in two-kidney, one clip hypertensive rats. Hypertension 14: 445-452, 1989.
25. Kopp UC, Cicha MZ. Impaired substance P release from renal sensory nerves in SHR involves a pertussis toxin-sensitive mechanism. Am J Physiol Regul Integr Comp Physiol 286: R326-R333, 2004.
26. 2 mediated stimulation of renal sensory nerves. Am J Physiol Renal Physiol 287: F1269-F1282, 2004.
27. Kopp UC, Cicha MZ, Yorek MA. Impaired responsiveness of renal sensory nerves in streptozotocin-treated rats and obese Zucker diabetic fatty rats: role of angiotensin. Am J Physiol Regul Integr Comp Physiol 294: R858-R866, 2008.
28. Kopp UC, Cicha MZ, Smith LA. Arterial pressure increases in afferent renal denervated rats on high-sodium diet. Hypertension 42: 968-973, 2003.
29. 2-adrenoceptors. Hypertension 57: 640-647, 2011.
30. Kopp UC, Cicha MZ, Smith LA. Impaired responsiveness of renal mechanosensory nerves in heart failure: role of endogenous angiotensin. Am J Physiol Regul Integr Comp Physiol 284: R116-R124, 2003.
31. Kopp UC, Cicha MZ, Smith LA. PGE2 increases release of substance P from renal sensory nerves by activating the cAMP-PKA transduction cascade. Am J Physiol Regul Integr Comp Physiol 282: R1618-R1627, 2002.
32. Kopp UC, Cicha MZ, Smith LA, Hökfelt T. Nitric oxide modulates renal sensory nerve fibers by mechanisms related to substance P receptor activation. Am J Physiol Regul Integr Comp Physiol 281: R279-R290, 2001.
33. 2-adrenoceptors on renal sensory nerve fibers. Am J Physiol Regul Integr Comp Physiol 293: R1561-R1572, 2007.
34. 2-adrenoceptors on renal sensory nerves. Am J Physiol Regul Integr Comp Physiol 300: R298-R310, 2011.
35. Kopp UC, Jones SY, DiBona GF. Afferent renal denervation impairs baroreflex control of efferent renal sympathetic nerve activity. Am J Physiol Regul Integr Comp Physiol 295: R1882-R1890, 2008.
36. +-ATPase inhibition sensitizes renal mechanoreceptors activated by increases in renal pelvic pressure. Am J Physiol Regul Integr Comp Physiol 267: R1109-R1117, 1994.
37. Kopp UC, Olson LA, DiBona GF. Renorenal reflex responses to mechano- and chemoreceptor stimulation in the dog and rat. Am J Physiol Renal Fluid Electrolyte Physiol 246: F67-F77, 1984.
38. Krum H, Barman N, Schlaich M, Sobotka P, Esler M, Mahfoud F, Bohm M, Dunlap M. Catheter-based renal sympathetic denervation for resistant hypertension. Durability of blood pressure reduction out to 24 months. Hypertension 57: 911-917, 2011.
39. Krum H, Schlaich M, Whitbourn R, Sobotka PA, Sadowski J, Bartus K, Kapelak B, Walton A, Sievert H, Thambar S, Abraham WT, Esler M. Catheter-based renal sympathetic denervation for resistant hypertension: a multicentre safety and proof-of-principle cohort study. Lancet 373: 1275-1281, 2009.
40. Liu L, Barajas L. The rat renal nerves during development. Anat Embryol 188: 345-361, 1993.
41. Maggi CA. Tachykinins and calcitonin gene-related peptide (CGRP) as co-transmitters released from peripheral endings of sensory nerves. Progr Neurobiol 45: 1-98, 1995.
42. Malpas SC. Sympathetic nervous system overactivity and its role in the development of cardiovascular disease. Physiol Rev 90: 513-557, 2009.
43. Markey KA, Kondo H, Shenkman L, Goldstein M. Purification and characterization of tyrosine hydroxylase from a clonal pheochromocytoma cell line. Mol Pharmacol 17: 79-85, 1980.
44. Masuo K, Lambert GW, Esler MD, Rakugi H, Ogihara T, Schlaich MP. The role of sympathetic nervous activity in renal injury and end-stage renal disease. Hypertens Res 33: 521-528, 2010.
45. Mogil RA, Itskovitz HD, Russell JH, Murphy JJ. Renal innervation and renin activity in salt metabolism and hypertension. Am J Physiol 216: 693-697, 1969.
46. Mohanty PK, Thames MD, Capehart JR, Kawaguchi A, Ballon B, Lower RR. Afferent reinnervation of the autotransplanted heart in dogs. J Am Coll Cardiol 7: 414-418, 1986.
47. Morsing P, Persson AEG. Pelvic pressure and tubuloglomerular feedback in hydronephrosis. Renal Physiol Biochem 13: 181-189, 1990.
48. Norman RA, Dzielak DJ. Role of renal nerves in onset and maintenance of spontaneous hypertension. Am J Physiol Heart Circ Physiol 243: H284-H288, 1982.
49. Norvell JE, Banes RT. Histofluorescence and fluorometric analysis of adrenergic reinnervation in the dog kidney following autotransplantation. Transplantation 27: 69-70, 1979.
50. Orazzo C, Pieribone VA, Ceccatelli S, Terenius L, Hökfelt T. CGRPlike immunoreactivity in A11 dopamine neurons projecting to the spinal cord and a note on CGRP-CCK cross-reactivity. Brain Res 600: 39-48, 1993.
51. Peleshok JC, Ribeiro-da-Silva A. Delayed reinnervation by nonpeptidergic nociceptive afferents of the glabrous skin of the rat hindpaw in a neuropathic pain model. J Comp Neurol 519: 49-63, 2011.
52. Sankari B, Stowe N, Gavin JP, Satoh S, Nally JV, Novick AC. Studies on the afferent and efferent renal nerves following autotransplantation of the canine kidney. J Urol 148: 206-210, 1992.
53. Schlaich MP, Sobotka PA, Krum H, Lambert E, Esler MD. Renal sympathetic-nerve ablation for uncontrolled hypertension. N Engl J Med 361: 932-934, 2009.
54. Smyth TB, Shortliffe LMD, Constantinou CE. The effect of urinary flow and bladder fullness on renal pelvic pressure in a rat model. J Urol 146: 592-596, 1991.
55. Solano-Flores LP, Rosa-Arellano MP, Ciriello J. Fos induction in central structures after afferent renal stimulation. Brain Res 753: 102-119, 1997.
56. Stark RP, McGinn AL, Wilson RF. Chest pain in cardiac-transplant recipients. Evidence of sensory reinnervation after cardiac transplantation. N Engl J Med 324: 1791-1794, 1991.
57. Theodorsson-Norheim E, Hemsén A, Lundberg JM. Radioimmunoassay for neuropeptide Y (NPY): chromatographic characterization of immunoreactivity in plasma and tissue extracts. Scand J Clin Lab Invest 45: 355-365, 1985.
58. Winternitz SR, Katholi RE, Oparil S. Decrease in hypothalamic norepinephrine content following renal denervation in the one-kidney, one clip Goldblatt hypertensive rat. Hypertension 4: 369-373, 1982.
59. Winternitz SR, Katholi RE, Oparil S. Role of the renal sympathetic nerves in the development and maintenance of hypertension in the spontaneously hypertensive rat. J Clin Invest 66: 971-978, 1980.