Nitric oxide inhibits capacitative Ca2+ entry by suppression of mitochondrial Ca2+ handling

Br J Pharmacol. 2002 Nov;137(6):821-30. doi: 10.1038/sj.bjp.0704949.

Abstract

1. Nitric oxide (NO) is a key modulator of cellular Ca(2+) signalling and a determinant of mitochondrial function. Here, we demonstrate that NO governs capacitative Ca(2+) entry (CCE) into HEK293 cells by impairment of mitochondrial Ca(2+) handling. 2. Authentic NO as well as the NO donors 1-[2-(carboxylato)pyrrolidin-1-yl]diazem-1-ium-1,2-diolate (ProliNO) and 2-(N,N-diethylamino)-diazenolate-2-oxide (DEANO) suppressed CCE activated by thapsigargin (TG)-induced store depletion. Threshold concentrations for inhibition of CCE by ProliNO and DEANO were 0.3 and 1 micro M, respectively. 3. NO-induced inhibition of CCE was not mimicked by peroxynitrite (100 micro M), the peroxynitrite donor 3-morpholino-sydnonimine (SIN-1, 100 micro M) or 8-bromoguanosine 3',5'-cyclic monophosphate (8-BrcGMP, 1 mM). In addition, the guanylyl cyclase inhibitor 1H-[1,2,4] oxadiazole[4,3-a] quinoxalin-1-one (ODQ, 30 micro M) failed to antagonize the inhibitory action of NO on CCE. 4. DEANO (1-10 micro M) suppressed mitochondrial respiration as evident from inhibition of cellular oxygen consumption. Experiments using fluorescent dyes to monitor mitochondrial membrane potential and mitochondrial Ca(2+) levels, respectively, indicated that DEANO (10 micro M) depolarized mitochondria and suppressed mitochondrial Ca(2+) sequestration. The inhibitory effect of DEANO on Ca(2+) uptake into mitochondria was confirmed by recording mitochondrial Ca(2+) during agonist stimulation in HEK293 cells expressing ratiometric-pericam in mitochondria. 5. DEANO (10 micro M) failed to inhibit Ba(2+) entry into TG-stimulated cells when extracellular Ca(2+) was buffered below 1 micro M, while clear inhibition of Ba(2+) entry into store depleted cells was observed when extracellular Ca(2+) levels were above 10 micro M. Moreover, buffering of intracellular Ca(2+) by use of N,N'-[1,2-ethanediylbis(oxy-2,1-phenylene)] bis [N-[25-[(acetyloxy) methoxy]-2-oxoethyl]]-, bis[(acetyloxy)methyl] ester (BAPTA/AM) eliminated inhibition of CCE by NO, indicating that the observed inhibitory effects are based on an intracellular, Ca(2+) dependent-regulatory process. 6. Our data demonstrate that NO effectively inhibits CCE cells by cGMP-independent suppression of mitochondrial function. We suggest disruption of local Ca(2+) handling by mitochondria as a key mechanism of NO induced suppression of CCE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Barium / metabolism
  • Calcium / metabolism*
  • Cell Line
  • Cyclic GMP / analogs & derivatives*
  • Cyclic GMP / pharmacology
  • Diethylamines / pharmacology
  • Dose-Response Relationship, Drug
  • Humans
  • Intracellular Membranes / drug effects
  • Intracellular Membranes / physiology
  • Membrane Potentials / drug effects
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Mitochondria / physiology
  • Molsidomine / analogs & derivatives*
  • Molsidomine / pharmacology
  • Nitric Oxide / pharmacology*
  • Nitric Oxide Donors / pharmacology*
  • Nitrogen Oxides
  • Oxadiazoles / pharmacology
  • Oxygen Consumption / drug effects
  • Peroxynitrous Acid / pharmacology
  • Quinoxalines / pharmacology
  • Thapsigargin / pharmacology
  • Time Factors

Substances

  • 1H-(1,2,4)oxadiazolo(4,3-a)quinoxalin-1-one
  • Diethylamines
  • Nitric Oxide Donors
  • Nitrogen Oxides
  • Oxadiazoles
  • Quinoxalines
  • Peroxynitrous Acid
  • Barium
  • 8-bromocyclic GMP
  • Nitric Oxide
  • linsidomine
  • Thapsigargin
  • diethylamine dinitric oxide adduct
  • Molsidomine
  • Cyclic GMP
  • Calcium