Regulation of vascular tone in animals overexpressing the sarcolemmal calcium pump

J Biol Chem. 2003 Oct 17;278(42):41246-52. doi: 10.1074/jbc.M307606200. Epub 2003 Aug 4.

Abstract

The mechanisms governing vascular smooth muscle tone are incompletely understood. In particular, the role of the sarcolemmal calcium pump PMCA (plasma membrane calmodulin-dependent calcium ATPase), which extrudes Ca2+ from the cytosol, and its importance compared with the sodium/calcium exchanger remain speculative. To test whether the PMCA is a regulator of vascular tone, we generated transgenic mice overexpressing the human PMCA4b under control of the arterial smooth muscle-specific SM22alpha promoter. This resulted in an elevated systolic blood pressure compared with littermate controls. In PMCA-overexpressing mice, endothelium-dependent relaxation of norepinephrine-preconstricted aortic rings to acetylcholine did not differ from wild type controls (76 +/- 8% versus 79 +/- 8% of maximum relaxation; n = 12, n.s.). De-endothelialized aortas of transgenic mice exhibited stronger maximum contraction to KCl (100 mmol/liter) compared with controls (86 +/- 6% versus 68 +/- 7% of reference KCl contraction at the beginning of the experiment; p <0.05). Preincubation of de-endothelialized vessels with the nitric oxide synthase (NOS) inhibitor l-NAME (l-N(G)-nitroarginine methyl ester) (10-5 mol/liter) resulted in a stronger contraction to KCl (p <0.05 versus without l-NAME), thus unmasking vasodilatory effects of inherent NO production. Maximum contraction to KCl after preincubation with l-NAME did not differ between PMCA mice and controls. In analogy to the results in PMCA-overexpressing mice, contractions of de-endothelialized aortas of neuronal NOS-deficient mice to KCl were significantly increased compared with controls (151 +/- 5% versus 131 +/- 6% of reference KCl contraction; p <0.05). In conclusion, our data suggest a model in which the sarcolemmal Ca2+ pump down-regulates activity of the vascular smooth muscle Ca2+/calmodulin-dependent neuronal NOS by a functionally relevant interaction. Therefore, the PMCA represents a novel regulator of vascular tone.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / pharmacology
  • Animals
  • Aorta / drug effects
  • Blood Pressure
  • Calcium / metabolism*
  • Calcium-Transporting ATPases / metabolism*
  • Calmodulin / metabolism
  • Cation Transport Proteins
  • Cytosol / metabolism
  • Dose-Response Relationship, Drug
  • Hemodynamics
  • Humans
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Models, Genetic
  • Muscle, Smooth / metabolism
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitroprusside / pharmacology
  • Plasma Membrane Calcium-Transporting ATPases
  • Potassium Chloride / pharmacology
  • Promoter Regions, Genetic
  • RNA, Messenger / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sarcolemma / metabolism*
  • Time Factors
  • Tissue Distribution
  • Transgenes
  • Vasodilator Agents / pharmacology

Substances

  • Calmodulin
  • Cation Transport Proteins
  • RNA, Messenger
  • Vasodilator Agents
  • Nitroprusside
  • Potassium Chloride
  • Nitric Oxide Synthase
  • Plasma Membrane Calcium-Transporting ATPases
  • Calcium-Transporting ATPases
  • Acetylcholine
  • Calcium
  • NG-Nitroarginine Methyl Ester