Neuronal nitric oxide synthase: its role and regulation in macula densa cells

J Am Soc Nephrol. 2003 Oct;14(10):2475-83. doi: 10.1097/01.asn.0000088737.05283.2b.

Abstract

Macula densa (MD) cells detect changes in distal tubular sodium chloride concentration ([NaCl](L)), at least in part, through an apical Na:2Cl:K co-transporter. This co-transporter may be a site for regulation of tubuloglomerular feedback (TGF), and recently angiotensin II (Ang II) was shown to regulate the MD Na:2Cl:K co-transporter. In addition, nitric oxide (NO) produced via neuronal NO synthase (nNOS) in MD cells attenuates MD-TGF signaling. This study investigated [NaCl](L)-dependent MD-NO production, the regulation of co-transporter activity by NO, and the possible interaction of NO with Ang II. MD cell Na(+) concentration ([Na(+)](i)) and NO production were measured using sodium-binding benzofuran isophthalate and 4-amino-5-methylamino-2',7'-difluorescein diacetate, respectively, using fluorescence microscopy. Na:2Cl:K co-transport activity was assessed as the initial rate of increase in [Na(+)](i) when [NaCl](L) was elevated from 25 to 150 mM. 10(-4) M 7-nitroindazole, a specific nNOS blocker, significantly increased by twofold the initial rate of rise in [Na(+)](i) when [NaCl](L) was increased from 25 to 150 mM, indicating co-transporter stimulation. There was no evidence for an interaction between the stimulatory effect of Ang II and the inhibitory effect of NO on co-transport activity, and, furthermore, Ang II failed to alter MD-NO production. NO production was sensitive to [NaCl](L) but increased only when [NaCl](L) was elevated from 60 to 150 mM. These studies indicate that MD-NO directly inhibits Na:2Cl:K co-transport and that NO and Ang II independently alter co-transporter activity. In addition, generation of MD-NO seems to occur only at markedly elevated [NaCl](L), suggesting that NO may serve as a buffer against high rates of MD cell transport and excessive TGF-mediated vasoconstriction.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Angiotensin II / pharmacology
  • Animals
  • Arginine / pharmacology
  • Biological Transport / drug effects
  • Enzyme Inhibitors / pharmacology
  • Indazoles / pharmacology
  • Juxtaglomerular Apparatus / cytology
  • Juxtaglomerular Apparatus / enzymology*
  • Loop of Henle / cytology
  • Loop of Henle / enzymology*
  • Nitric Oxide / metabolism
  • Nitric Oxide Donors / pharmacology
  • Nitric Oxide Synthase / metabolism*
  • Nitric Oxide Synthase Type I
  • Rabbits
  • Sodium Chloride / pharmacokinetics
  • Sodium-Potassium-Chloride Symporters / metabolism
  • Vasoconstrictor Agents / pharmacology

Substances

  • Enzyme Inhibitors
  • Indazoles
  • Nitric Oxide Donors
  • Sodium-Potassium-Chloride Symporters
  • Vasoconstrictor Agents
  • Angiotensin II
  • Nitric Oxide
  • Sodium Chloride
  • Arginine
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type I
  • 7-nitroindazole