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Differential Effects of Halothane and Thiopental on Surfactant Protein C

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Differential Effects of Halothane and Thiopental on Surfactant Protein C 805 Anesthesiology 2000; 93:805–10 © 2000 American Society of Anesthesiologists, Inc. Lippincott Williams & Wilkins, Inc. Differential Effects of Halothane and Thiopental on Surfactant Protein C Messenger RNA In Vivo and In Vitro in Rats Catherine Paugam-Burtz, M.D.,* Serge Molliex, M.D, Ph.D.,† Bernard Lardeux, Ph.D.,‡ Corinne Rolland, T.A.,§, Michel Aubier, M.D,ʈ Jean-Marie Desmonts, M.D.,# Bruno Crestani, M.D., Ph.D.** Downloaded from http://pubs.asahq.org/anesthesiology/article-pdf/93/3/805/401255/0000542-200009000-00030.pdf by guest on 28 September 2021 Background: Pulmonary surfactant is a complex mixture of lung SP-C mRNA content to 53% of the value obtained in control proteins and phospholipids synthetized by alveolar type II (nonanesthetized, nonventilated) animals; thiopental anesthe- cells. Volatile anesthetics have been shown to reduce surfactant sia increased to 150% the lung SP-C mRNA content. phospholipid biosynthesis by rat alveolar type II cells. Surfac- Conclusions: These findings indicate that halothane and thio- tant-associated protein C (SP-C) is critical for the alveolar sur- pental used at clinically relevant concentrations modulate the factant functions. Our goal was to evaluate the effects of halo- pulmonary SP-C mRNA content in rats. In vivo, the additive role thane and thiopental on SP-C messenger RNA (mRNA) of mechanical ventilation is suggested. (Key words: Lung; pneu- expression in vitro in rat alveolar type II cells and in vivo in mocytes, volatile anesthetics.) mechanically ventilated rats. Methods: In vitro, freshly isolated alveolar type II cells were exposed to halothane during 4 h (1, 2, 4%) and 8 h (1%), and to PULMONARY surfactant is a complex mixture of pro- thiopental during 4 h (10, 100 ␮M) and 8 h (100 ␮M). In vivo, rats teins and phospholipids synthetized by alveolar type II were anesthetized with intraperitoneal thiopental or inhaled (ATII) epithelial cells. It reduces lung alveolar surface 1% halothane and mechanically ventilated for 4 or 8 h. SP-C tension, maintains alveolar fluid balance, and possibly mRNA expression was evaluated by ribonuclease protection assay. exhibits host-defense properties. Although the phospho- Results: In vitro, 4-h exposure of alveolar type II cells to lipid makeup of surfactant is critical to its functional thiopental 10 and 100 ␮M increased their SP-C mRNA content to integrity, surfactant-associated proteins, particularly the 145 and 197%, respectively, of the control values. In alveolar hydrophobic surfactant-associated protein C (SP-C), have type II cells exposed for4htohalothane 1, 2, and 4%, the SP-C mRNA content increased dose-dependently to 160, 235, and been recognized increasingly as conferring the proper- 275%, respectively, of the control values. In vivo, in mechani- ties of rapid surface adsorption and surface-tension re- cally ventilated rats,4hofhalothane anesthesia decreased the duction to phospholipids during dynamic compres- sion.1,2 SP-C, which is synthesized exclusively by ATII 3 * Associate Professor of Anesthesiology, Service d’Anesthe´sie-Re´ani- cells, facilitates the adsorption and the spreading of the mation Chirurgicale, Hoˆpital Bichat, and Unite´ INSERM 408, Faculte´X. phospholipids to form the surfactant monolayer2,4 and Bichat. enhances in vitro the lipid uptake in ATII cells.5 In vivo, † Professor of Anesthesiology, Unite´ INSERM 408, Faculte´ X. Bichat. in animal models of surfactant deficiency6,7 and in pre- ‡ Physical Doctor, Unite´ INSERM 327, Faculte´ X. Bichat. term infants with respiratory distress syndrome,8 bovine- § Research Associate, Unite´ INSERM 408, Faculte´ X. Bichat. derived exogenous surfactants that contain SP-C are ʈ Professor of Pneumology, Unite´ INSERM 408, Faculte´ X. Bichat. more effective at decreasing the rates of barotrauma and # Professor of Anesthesiology, Service d’Anesthe´sie-Re´animation mortality. Chirurgicale, Hoˆpital Bichat. During inhalation anesthesia, lung alveolar epithelium ** Professor of Pneumology, Unite´ INSERM 408, Faculte´ X. Bichat. is exposed directly to volatile anesthetics. Recently, po- Received from Unite´ Inserm 408, Faculte´ X. Bichat, Paris, France. tentially deleterious effects of halothane on the surfac- Submitted for publication December 22, 1999. Accepted for publica- tant metabolism of ATII cells have been described. Our tion April 24, 2000. Supported by a grant from Assistance Publique– group has shown that halothane at clinically relevant Hoˆpitaux de Paris, Paris, France. concentrations reduces surfactant phospholipid biosyn- Address reprint requests to Dr. Paugam-Burtz: Department of Anes- 9 thesiology, Hoˆpital Bichat, 46, Rue Henri Huchard, 75877 Paris cedex thesis by rat ATII cells in vitro, whereas intravenous 18. Address electronic mail to: [email protected] anesthetic agents such as thiopental have no effect on 10 Individual article reprints may be purchased through the Journal phospholipid surfactant metabolism. These results Web site, www.anesthesiology.org highlight differential effects of anesthetic agents on Anesthesiology, V 93, No 3, Sep 2000 806 PAUGAM-BURTZ ET AL. physiologic functions of ATII cells. Whether or not pul- thane, or thiopental). Each experiment was performed monary SP-C is affected by volatile anesthetics remains to three times. be determined. The present study was designed to assess Freshly isolated ATII cells were exposed to halothane the effects of halothane and thiopental on surfactant SP-C using a 12-l airtight Lwoff chamber (Lequeux, Paris, messenger RNA (mRNA) expression, in vitro in freshly France) as previously described.9,12 The chamber atmo- isolated ATII cells and in vivo in mechanically ventilated sphere was kept continuously saturated with water at rats. 37°C. In preliminary experiments, we observed that over an 8-h period the different culture conditions usedDownloaded from http://pubs.asahq.org/anesthesiology/article-pdf/93/3/805/401255/0000542-200009000-00030.pdf by guest on 28 September 2021 in our experiments did not influence SP-C mRNA expres- Materials and Methods sion by ATII cells, the expression being similar in a standard incubator and in the sealed chamber flushed Animals were treated according to the guidelines of with a 95% air–5% CO mixture. Halothane was vapor- the French Institut National de la Sante´ et de la Recher- 2 ized by directing a 95% air–5% CO mixture at 5 l/min che Me´dicale (INSERM) for laboratory care of animals. 2 through a calibrated Fluotec Mark II vaporizer (Abott, Paris, France) placed at the entrance of the chamber.9 Materials Halothane concentration was monitored at the chamber Adult male pathogen-free Sprague–Dawley rats (200- exit port using a halogen monitor (Capnomac Datex, 220g) (Charles Rivers Breeders, St Aubin les Elbeuf, Helsinki, Finland). The effects of halothane on SP-C France) were used within 4 days of delivery. Animals mRNA expression of ATII cells were assessed during a were killed by exsanguination under general anesthesia. 4-h exposure with various halothane concentrations (1, Halothane was purchased from Trofield (London, United 2, and 4%) and during 8-h exposure with 1% halothane. Kingdom). Sodium thiopental was purchased from Spe- Exposure of freshly isolated ATII cells to thiopental cia (Paris, France). TEMED, ammonium persulfate, and was achieved by addition of sodium thiopental (molec- guanidine thiocyanate were from Sigma (La Verpille`re, ular weight: 264) to the culture medium (final concen- France). [␣-32P]UTP (128 ϫ 1011 Bq/mmol) was from trations: 10 and 100 ␮M). The cell plates were returned Amersham (Les Ulis, France). RNAse-free DNAse I and to a standard 95% air–5% CO2 incubator for the desired ribonucleases A and T1 were supplied from Boehringer period of time (4 or 8 h). We chose thiopental concen- (Mannheim, Germany). Acrylamide–bisacrylamide, phe- trations consistent with those that may be observed in nol, urea, and proteinase K were from Appligene plasma in clinical practice.13,14 (Illkirch, France). BSU36I restriction enzyme was from For each exposure condition, a control point was ob- New England Biolabs (Beverly, MA). Tissue culture me- tained simultaneously with ATII cells cultured in a stan- dia, supplements, and fetal bovine serum were from dard 95% air–5% CO incubator without anesthetic ex- Gibco BRL Life Technologies (Cergy Pontoise, France). 2 posure. At the end of each experiment, supernatants and Tissue culture plastic was from Costar (Cambridge, MA). adherent cells were frozen immediately in liquid nitro- gen and stored at Ϫ80°C until RNA extraction. In Vitro Study Alveolar type II cells were isolated from rat lungs by elastase dissociation and purified by differential adher- In Vivo Study ence to plastic as previously described.9,11 Cell isolation In all animals (adult rats weighting 200–220 g), anes- yield per rat and cellular viability (assessed by the Trypan thesia was induced initially with ether vapor, and then blue exclusion test) were 25 Ϯ 1.106 and 95 Ϯ 5% the trachea was cannulated with a 14-gauge catheter. (mean Ϯ SD, n ϭ 30). In this preparation, about 60% of Animals were assigned randomly for maintenance of the cells are ATII cells.11 For each experiment, freshly anesthesia to inhaled 1% halothane or intraperitoneal isolated cells from four different rats were pooled and injection of thiopental. Halothane was vaporized at 1% immediately plated in 10-cm diameter cell culture plastic inspired concentration (one minimal alveolar concentra- dishes (20 ϫ 106 cells/dish) with 20 ml of Dulbecco’s tion for rats)15 monitored by a halogen monitor (Capno- modified Eagle’s medium containing 10% fetal bovine mac Datex). Rats then were ventilated for 4 and8h(nϭ serum, 105 U/l penicillin, 100 mg/l streptomycin, and 6 animals for each duration). Thiopental-anesthetized 0.25 mg/L amphotericin B; the cells then were exposed rats received a first intraperitoneal injection of thiopen- to the different experimental conditions (control, halo- tal (12.5 mg/100 g weight). Three animals ventilated Anesthesiology, V 93, No 3, Sep 2000 807 EFFECTS OF HALOTHANE AND THIOPENTAL ON SP-C mRNA during 8 h needed extra doses of thiopental (3 mg/100 g were expressed versus control (nonexposed) cells or con- weight) at the 6th h of ventilation.
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