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(Circulation Research. 1995;76:566-574.)
© 1995 American Heart Association, Inc.

Articles

Effects of Second Messengers on the Permeability and Morphology of Eel Rete Capillaries

Eugenio A. Rasio, Moïse Bendayan, Carl A. Goresky

From the Department of Medicine, Hôpital Notre-Dame, and the Department of Anatomy, Université de Montréal (E.A.R., M.B.), and the McGill University Medical Clinic and the Department of Medicine, Montreal General Hospital (C.A.G.), Montreal, Quebec, Canada.

Correspondence to Dr Carl A. Goresky, McGill University Medical Clinic, Rm C10.148, Montreal General Hospital, 1650, Cedar Ave, Montreal, Quebec, Canada, H3G 1A4.

Abstract The effects of second-messenger concentration changes on capillary diffusion capacity (permeability–surface area product [PS]) to cellular and paracellular tracers and on capillary ultrastructure were studied during countercurrent perfusion of the rete of the eel swim bladder. Cyclic nucleotide effects were investigated with isoproterenol, forskolin, and dibutyryl cAMP. Isoproterenol (5x10^-6 mol/L) did not modify water and solute permeability or capillary structure. Forskolin (10^-4 mol/L) immediately raised the concentrations of cAMP in the rete and produced interstitial edema but did not change permeability. The addition of dibutyryl cAMP (10^-6 mol/L) to the perfusate had rapid effects: it reduced the PS of [³H]water and oxygen and increased the PS of [¹²⁵I]albumin, [¹⁴C]sucrose, and ²²Na. No structural changes were observed. Phosphoinositide effects were studied with 1,2-dioctanoyl-sn-glycerol (DG) and phorbol 12-myristate 13-acetate (PMA). DG (10^-5 mol/L) had no effect on the permeability of the rete to water and solutes, while inducing cell membrane vacuolization. PMA (10^-5 mol/L) progressively reduced the PS of [³H]water. In contrast, PS values of [¹²⁵I]albumin, [¹⁴C]sucrose, and ²²Na rose gradually. Membrane vacuoles bulging into the lumen and in the cytoplasm were a common feature. The Ca²⁺ effect was investigated with the Ca²⁺ ionophore A23187. At 5x10^-6 mol/L, unsteady permeability changes and extensive cytolysis were observed. At 5x10^-7 mol/L, the PS of [¹²⁵I]albumin, [¹⁴C]sucrose, and ²²Na rapidly increased. The PS values for water were not modified. No structural changes were identified. It is concluded that increments of second-messenger concentrations in the rete induce characteristic selective effects on the paracellular and transcellular pathways of transport and create significant but nonselective alterations of capillary structure.

Key Words: rete mirabile • capillary permeability • capillary ultrastructure • second messengers

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