Skip to main content
Erschienen in: European Journal of Nutrition 1/2015

01.02.2015 | Original Contribution

Protective effects of l-alpha-glycerylphosphorylcholine on ischaemia–reperfusion-induced inflammatory reactions

verfasst von: Tünde Tőkés, Eszter Tuboly, Gabriella Varga, László Major, Miklós Ghyczy, József Kaszaki, Mihály Boros

Erschienen in: European Journal of Nutrition | Ausgabe 1/2015

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Choline-containing dietary phospholipids, including phosphatidylcholine (PC), may function as anti-inflammatory substances, but the mechanism remains largely unknown. We investigated the effects of l-alpha-glycerylphosphorylcholine (GPC), a deacylated PC derivative, in a rodent model of small intestinal ischaemia–reperfusion (IR) injury.

Methods

Anaesthetized Sprague-Dawley rats were divided into control, mesenteric IR (45 min mesenteric artery occlusion, followed by 180 min reperfusion), IR with GPC pretreatment (16.56 mg kg−1 GPC i.v., 5 min prior to ischaemia) or IR with GPC post-treatment (16.56 mg kg−1 GPC i.v., 5 min prior to reperfusion) groups. Macrohaemodynamics and microhaemodynamic parameters were measured; intestinal inflammatory markers (xanthine oxidoreductase activity, superoxide and nitrotyrosine levels) and liver ATP contents were determined.

Results

The IR challenge reduced the intestinal intramural red blood cell velocity, increased the mesenteric vascular resistance, the tissue xanthine oxidoreductase activity, the superoxide production, and the nitrotyrosine levels, and the ATP content of the liver was decreased. Exogenous GPC attenuated the macro- and microcirculatory dysfunction and provided significant protection against the radical production resulting from the IR stress. The GPC pretreatment alleviated the hepatic ATP depletion, the reductions in the mean arterial pressure and superior mesenteric artery flow, and similarly to the post-treatments with GPC, also decreased the xanthine oxidoreductase activity, the intestinal superoxide production, the nitrotyrosine level, and normalized the microcirculatory dysfunction.

Conclusions

These data demonstrate the effectiveness of GPC therapies and provide indirect evidence that the anti-inflammatory effects of PC could be linked to a reaction involving the polar part of the molecule.
Literatur
1.
Zurück zum Zitat Han JY, Fan JY, Horie Y, Miura S, Cui DH, Ishii H, Hibi T, Tsuneki H, Kimura I (2008) Ameliorating effects of compounds derived from Salvia miltiorrhiza root extract on microcirculatory disturbance and target organ injury by ischemia and reperfusion. Pharmacol Ther 117:280–295CrossRef Han JY, Fan JY, Horie Y, Miura S, Cui DH, Ishii H, Hibi T, Tsuneki H, Kimura I (2008) Ameliorating effects of compounds derived from Salvia miltiorrhiza root extract on microcirculatory disturbance and target organ injury by ischemia and reperfusion. Pharmacol Ther 117:280–295CrossRef
2.
Zurück zum Zitat Breithaupt-Faloppa AC, Fantozzi ET, Assis-Ramos MM, Vitoretti LB, Couto GK, Rossoni LV, Oliveira-Filho RM, Vargaftig BB, Tavares-de-Lima W (2013) Protective effect of estradiol on acute lung inflammation induced by an intestinal ischemic insult is dependent on nitric oxide. Shock 40:203–209. doi:10.1097/SHK.0b013e3182a01e24 CrossRef Breithaupt-Faloppa AC, Fantozzi ET, Assis-Ramos MM, Vitoretti LB, Couto GK, Rossoni LV, Oliveira-Filho RM, Vargaftig BB, Tavares-de-Lima W (2013) Protective effect of estradiol on acute lung inflammation induced by an intestinal ischemic insult is dependent on nitric oxide. Shock 40:203–209. doi:10.​1097/​SHK.​0b013e3182a01e24​ CrossRef
3.
Zurück zum Zitat Cuzzocrea S, Mazzon E, Esposito E, Muià C, Abdelrahman M, Di Paola R, Crisafulli C, Bramanti P, Thiemermann C (2007) Glycogen synthase kinase-3beta inhibition attenuates the development of ischaemia/reperfusion injury of the gut. Intensive Care Med 33:880–893CrossRef Cuzzocrea S, Mazzon E, Esposito E, Muià C, Abdelrahman M, Di Paola R, Crisafulli C, Bramanti P, Thiemermann C (2007) Glycogen synthase kinase-3beta inhibition attenuates the development of ischaemia/reperfusion injury of the gut. Intensive Care Med 33:880–893CrossRef
4.
Zurück zum Zitat Mallick IH, Yang W, Winslet MC, Seifalian AM (2004) Ischemia-reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci 49:1359–1377CrossRef Mallick IH, Yang W, Winslet MC, Seifalian AM (2004) Ischemia-reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci 49:1359–1377CrossRef
5.
Zurück zum Zitat Wada K, Montalto MC, Stahl GL (2001) Inhibition of complement C5 reduces local and remote organ injury after intestinal ischemia/reperfusion in the rat. Gastroenterology 120:126–133CrossRef Wada K, Montalto MC, Stahl GL (2001) Inhibition of complement C5 reduces local and remote organ injury after intestinal ischemia/reperfusion in the rat. Gastroenterology 120:126–133CrossRef
6.
Zurück zum Zitat DeGraba TJ (1998) The role of inflammation after acute stroke: utility of pursuing anti-adhesion molecule therapy. Neurology 51:S62–S68CrossRef DeGraba TJ (1998) The role of inflammation after acute stroke: utility of pursuing anti-adhesion molecule therapy. Neurology 51:S62–S68CrossRef
7.
Zurück zum Zitat Sasaki M, Joh T (2007) Oxidative stress and ischemia-reperfusion injury in gastrointestinal tract and antioxidant, protective agents. J Clin Biochem Nutr 40:1–2. doi:10.3164/jcbn.40.1 CrossRef Sasaki M, Joh T (2007) Oxidative stress and ischemia-reperfusion injury in gastrointestinal tract and antioxidant, protective agents. J Clin Biochem Nutr 40:1–2. doi:10.​3164/​jcbn.​40.​1 CrossRef
8.
Zurück zum Zitat Francischetti I, Moreno JB, Scholz M, Yoshida WB (2010) Leukocytes and the inflammatory response in ischemia-reperfusion injury. Rev Bras Cir Cardiovasc 25:575–584CrossRef Francischetti I, Moreno JB, Scholz M, Yoshida WB (2010) Leukocytes and the inflammatory response in ischemia-reperfusion injury. Rev Bras Cir Cardiovasc 25:575–584CrossRef
9.
Zurück zum Zitat Volinsky R, Kinnunen PK (2013) Oxidized phosphatidylcholines in membrane-level cellular signaling: from biophysics to physiology and molecular pathology. FEBS J 280:2806–2816. doi:10.1111/febs.12247 CrossRef Volinsky R, Kinnunen PK (2013) Oxidized phosphatidylcholines in membrane-level cellular signaling: from biophysics to physiology and molecular pathology. FEBS J 280:2806–2816. doi:10.​1111/​febs.​12247 CrossRef
10.
Zurück zum Zitat Stremmel W, Ehehalt R, Staffer S, Stoffels S, Mohr A, Karner M, Braun A (2012) Mucosal protection by phosphatidylcholine. Dig Dis 30(Suppl 3):85–91. doi:10.1159/000342729 CrossRef Stremmel W, Ehehalt R, Staffer S, Stoffels S, Mohr A, Karner M, Braun A (2012) Mucosal protection by phosphatidylcholine. Dig Dis 30(Suppl 3):85–91. doi:10.​1159/​000342729 CrossRef
11.
Zurück zum Zitat Erős G, Ibrahim S, Siebert N, Boros M, Vollmar B (2009) Oral phosphatidylcholine pretreatment alleviates the signs of experimental rheumatoid arthritis. Arthritis Res Ther 11:R43. doi:10.1186/ar2651 CrossRef Erős G, Ibrahim S, Siebert N, Boros M, Vollmar B (2009) Oral phosphatidylcholine pretreatment alleviates the signs of experimental rheumatoid arthritis. Arthritis Res Ther 11:R43. doi:10.​1186/​ar2651 CrossRef
12.
Zurück zum Zitat Hartmann P, Szabó A, Erős G, Gurabi D, Horváth G, Németh I, Ghyczy M, Boros M (2009) Anti-inflammatory effects of phosphatidylcholine in neutrophil leukocyte-dependent acute arthritis in rats. Eur J Pharmacol 622:58–64. doi:10.1016/j.ejphar.2009.09.012 CrossRef Hartmann P, Szabó A, Erős G, Gurabi D, Horváth G, Németh I, Ghyczy M, Boros M (2009) Anti-inflammatory effects of phosphatidylcholine in neutrophil leukocyte-dependent acute arthritis in rats. Eur J Pharmacol 622:58–64. doi:10.​1016/​j.​ejphar.​2009.​09.​012 CrossRef
13.
Zurück zum Zitat Treede I, Braun A, Jeliaskova P, Giese T, Füllekrug J, Griffiths G, Stremmel W, Ehehalt R (2009) TNF-alpha-induced up-regulation of pro-inflammatory cytokines is reduced by phosphatidylcholine in intestinal epithelial cells. BMC Gastroenterol 9:53. doi:10.1186/1471-230X-9-53 CrossRef Treede I, Braun A, Jeliaskova P, Giese T, Füllekrug J, Griffiths G, Stremmel W, Ehehalt R (2009) TNF-alpha-induced up-regulation of pro-inflammatory cytokines is reduced by phosphatidylcholine in intestinal epithelial cells. BMC Gastroenterol 9:53. doi:10.​1186/​1471-230X-9-53 CrossRef
14.
Zurück zum Zitat Tőkés T, Erős G, Bebes A, Hartmann P, Várszegi S, Varga G, Kaszaki J, Gulya K, Ghyczy M, Boros M (2011) Protective effects of a phosphatidylcholine-enriched diet in lipopolysaccharide-induced experimental neuroinflammation in the rat. Shock 36:458–465. doi:10.1097/SHK.0b013e31822f36b0 CrossRef Tőkés T, Erős G, Bebes A, Hartmann P, Várszegi S, Varga G, Kaszaki J, Gulya K, Ghyczy M, Boros M (2011) Protective effects of a phosphatidylcholine-enriched diet in lipopolysaccharide-induced experimental neuroinflammation in the rat. Shock 36:458–465. doi:10.​1097/​SHK.​0b013e31822f36b0​ CrossRef
15.
Zurück zum Zitat Erős G, Varga G, Váradi R, Czóbel M, Kaszaki J, Ghyczy M, Boros M (2009) Anti-inflammatory action of a phosphatidylcholine, phosphatidylethanolamine and N-acylphosphatidylethanolamine-enriched diet in carrageenan-induced pleurisy. Eur Surg Res 42:40–48. doi:10.1159/000167856 CrossRef Erős G, Varga G, Váradi R, Czóbel M, Kaszaki J, Ghyczy M, Boros M (2009) Anti-inflammatory action of a phosphatidylcholine, phosphatidylethanolamine and N-acylphosphatidylethanolamine-enriched diet in carrageenan-induced pleurisy. Eur Surg Res 42:40–48. doi:10.​1159/​000167856 CrossRef
16.
Zurück zum Zitat Bochkov VN, Kadl A, Huber J, Gruber F, Binder BR, Leitinger N (2002) Protective role of phospholipid oxidation products in endotoxin-induced tissue damage. Nature 419:77–81CrossRef Bochkov VN, Kadl A, Huber J, Gruber F, Binder BR, Leitinger N (2002) Protective role of phospholipid oxidation products in endotoxin-induced tissue damage. Nature 419:77–81CrossRef
17.
Zurück zum Zitat Nivala AM, Reese L, Frye M, Gentile CL, Pagliassotti MJ (2013) Fatty acid-mediated endoplasmic reticulum stress in vivo: differential response to the infusion of Soybean and Lard Oil in rats. Metabolism 62:753–760. doi:10.1016/j.metabol.2012.12.001 CrossRef Nivala AM, Reese L, Frye M, Gentile CL, Pagliassotti MJ (2013) Fatty acid-mediated endoplasmic reticulum stress in vivo: differential response to the infusion of Soybean and Lard Oil in rats. Metabolism 62:753–760. doi:10.​1016/​j.​metabol.​2012.​12.​001 CrossRef
20.
Zurück zum Zitat Gera L, Varga R, Török L, Kaszaki J, Szabó A, Nagy K, Boros M (2007) Beneficial effects of phosphatidylcholine during hindlimb reperfusion. J Surg Res 139:45–50CrossRef Gera L, Varga R, Török L, Kaszaki J, Szabó A, Nagy K, Boros M (2007) Beneficial effects of phosphatidylcholine during hindlimb reperfusion. J Surg Res 139:45–50CrossRef
21.
Zurück zum Zitat Varga R, Gera L, Török L, Kaszaki J, Szabó A, Nagy K, Boros M (2006) Effects of phosphatidylcholine therapy after hindlimb ischemia and reperfusion. Magy Seb 59:429–436 Varga R, Gera L, Török L, Kaszaki J, Szabó A, Nagy K, Boros M (2006) Effects of phosphatidylcholine therapy after hindlimb ischemia and reperfusion. Magy Seb 59:429–436
22.
Zurück zum Zitat Lamprech W, Trautschold I (1976) Adenosine 5-triphosphate. Determination with hexokinase and glucose 6-phosphate dehydrogenase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 4. Verlag Chemie Weinheim, Academic Press, New York, pp 2101–2109 Lamprech W, Trautschold I (1976) Adenosine 5-triphosphate. Determination with hexokinase and glucose 6-phosphate dehydrogenase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 4. Verlag Chemie Weinheim, Academic Press, New York, pp 2101–2109
23.
Zurück zum Zitat Chen F, Cushion MT (1994) Use of an ATP bioluminescent assay to evaluate viability of Pneumocystis carinii from rats. J Clin Microbiol 32:2791–2800 Chen F, Cushion MT (1994) Use of an ATP bioluminescent assay to evaluate viability of Pneumocystis carinii from rats. J Clin Microbiol 32:2791–2800
24.
Zurück zum Zitat Andreotti PE, Berthold F (1999) Application of a new high sensitivity luminometer for industrial microbiology and molecular biology. Luminescence 14:19–22CrossRef Andreotti PE, Berthold F (1999) Application of a new high sensitivity luminometer for industrial microbiology and molecular biology. Luminescence 14:19–22CrossRef
25.
Zurück zum Zitat Ferdinandy P, Danial H, Ambrus I, Rothery RA, Schulz R (2000) Peroxynitrite is a major contributor to cytokine-induced myocardial contractile failure. Circ Res 87:241–247CrossRef Ferdinandy P, Danial H, Ambrus I, Rothery RA, Schulz R (2000) Peroxynitrite is a major contributor to cytokine-induced myocardial contractile failure. Circ Res 87:241–247CrossRef
26.
Zurück zum Zitat Beckman JS, Parks DA, Pearson JD, Marshall PA, Freeman BA (1989) A sensitive fluorometric assay for measuring xanthine dehydrogenase and oxidase in tissues. Free Rad Biol Med 6:607–615CrossRef Beckman JS, Parks DA, Pearson JD, Marshall PA, Freeman BA (1989) A sensitive fluorometric assay for measuring xanthine dehydrogenase and oxidase in tissues. Free Rad Biol Med 6:607–615CrossRef
27.
Zurück zum Zitat Berland T, Oldenburg WA (2008) Acute mesenteric ischemia. Curr Gastroenterol Rep 10:341–346CrossRef Berland T, Oldenburg WA (2008) Acute mesenteric ischemia. Curr Gastroenterol Rep 10:341–346CrossRef
28.
Zurück zum Zitat Eckstein HH (2003) Acute mesenteric ischemia. Resection or reconstruction? Chirurg 74:419–431CrossRef Eckstein HH (2003) Acute mesenteric ischemia. Resection or reconstruction? Chirurg 74:419–431CrossRef
29.
Zurück zum Zitat Liu P, Hock CE, Nagele R, Wong PY (1997) Formation of nitric oxide, superoxide, and peroxynitrite in myocardial ischemia-reperfusion injury in rats. Am J Physiol 272:H2327–H2336 Liu P, Hock CE, Nagele R, Wong PY (1997) Formation of nitric oxide, superoxide, and peroxynitrite in myocardial ischemia-reperfusion injury in rats. Am J Physiol 272:H2327–H2336
32.
Zurück zum Zitat Erős G, Kaszaki J, Czóbel M, Boros M (2006) Systemic phosphatidylcholine pretreatment protects canine esophageal mucosa during acute experimental biliary reflux. World J Gastroenterol 12:271–279 Erős G, Kaszaki J, Czóbel M, Boros M (2006) Systemic phosphatidylcholine pretreatment protects canine esophageal mucosa during acute experimental biliary reflux. World J Gastroenterol 12:271–279
33.
Zurück zum Zitat Ghyczy M, Torday C, Kaszaki J, Szabó A, Czóbel M, Boros M (2008) Oral phosphatidylcholine pretreatment decreases ischemia-reperfusion-induced methane generation and the inflammatory response in the small intestine. Shock 30:596–602. doi:10.1097/SHK.0b013e31816f204a CrossRef Ghyczy M, Torday C, Kaszaki J, Szabó A, Czóbel M, Boros M (2008) Oral phosphatidylcholine pretreatment decreases ischemia-reperfusion-induced methane generation and the inflammatory response in the small intestine. Shock 30:596–602. doi:10.​1097/​SHK.​0b013e31816f204a​ CrossRef
35.
Zurück zum Zitat Chao W, Spragg RG, Smith RM (1995) Inhibitory effect of porcine surfactant on the respiratory burst oxidase in human neutrophils. Attenuation of p47phox and p67phox membrane translocation as the mechanism. J Clin Invest 96:2654–2660CrossRef Chao W, Spragg RG, Smith RM (1995) Inhibitory effect of porcine surfactant on the respiratory burst oxidase in human neutrophils. Attenuation of p47phox and p67phox membrane translocation as the mechanism. J Clin Invest 96:2654–2660CrossRef
36.
Zurück zum Zitat Zeplin PH, Larena-Avellaneda A, Jordan M, Laske M, Schmidt K (2010) Phosphorylcholine-coated silicone implants: effect on inflammatory response and fibrous capsule formation. Ann Plast Surg 65:560–564. doi:10.1097/SAP.0b013e3181d6e326 CrossRef Zeplin PH, Larena-Avellaneda A, Jordan M, Laske M, Schmidt K (2010) Phosphorylcholine-coated silicone implants: effect on inflammatory response and fibrous capsule formation. Ann Plast Surg 65:560–564. doi:10.​1097/​SAP.​0b013e3181d6e326​ CrossRef
37.
Zurück zum Zitat Onishchenko LS, Gaikova ON, Yanishevskii SN (2008) Changes at the focus of experimental ischemic stroke treated with neuroprotective agents. Neurosci Behav Physiol 38:49–54CrossRef Onishchenko LS, Gaikova ON, Yanishevskii SN (2008) Changes at the focus of experimental ischemic stroke treated with neuroprotective agents. Neurosci Behav Physiol 38:49–54CrossRef
38.
Zurück zum Zitat Kidd PM (2009) Integrated brain restoration after ischemic stroke–medical management, risk factors, nutrients, and other interventions for managing inflammation and enhancing brain plasticity. Altern Med Rev 14:14–35 Kidd PM (2009) Integrated brain restoration after ischemic stroke–medical management, risk factors, nutrients, and other interventions for managing inflammation and enhancing brain plasticity. Altern Med Rev 14:14–35
39.
Zurück zum Zitat De Jesus Moreno Moreno M (2003) Cognitive improvement in mild to moderate Alzheimer’s dementia after treatment with the acetylcholine precursor choline alfoscerate: a multicenter, double-blind, randomized, placebo-controlled trial. Clin Ther 25:178–193CrossRef De Jesus Moreno Moreno M (2003) Cognitive improvement in mild to moderate Alzheimer’s dementia after treatment with the acetylcholine precursor choline alfoscerate: a multicenter, double-blind, randomized, placebo-controlled trial. Clin Ther 25:178–193CrossRef
40.
Zurück zum Zitat Alkondon M, Pereira EF, Cortes WS, Maelicke A, Albuquerque EX (1997) Choline is a selective agonist of alpha7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci 9:2734–2742CrossRef Alkondon M, Pereira EF, Cortes WS, Maelicke A, Albuquerque EX (1997) Choline is a selective agonist of alpha7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci 9:2734–2742CrossRef
41.
Zurück zum Zitat Guseva MV, Hopkins DM, Pauly JR (2006) An autoradiographic analysis of rat brain nicotinic receptor plasticity following dietary choline modification. Pharmacol Biochem Behav 84:26–34CrossRef Guseva MV, Hopkins DM, Pauly JR (2006) An autoradiographic analysis of rat brain nicotinic receptor plasticity following dietary choline modification. Pharmacol Biochem Behav 84:26–34CrossRef
42.
Zurück zum Zitat Tribollet E, Bertrand D, Marguerat A, Raggenbass M (2004) Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: an autoradiographic study in the rat brain. Neuroscience 124:405–420CrossRef Tribollet E, Bertrand D, Marguerat A, Raggenbass M (2004) Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: an autoradiographic study in the rat brain. Neuroscience 124:405–420CrossRef
43.
Zurück zum Zitat Nott A, Levin ED (2006) Dorsal hippocampal alpha7 and alpha4beta2 nicotinic receptors and memory. Brain Res 1081:72–78CrossRef Nott A, Levin ED (2006) Dorsal hippocampal alpha7 and alpha4beta2 nicotinic receptors and memory. Brain Res 1081:72–78CrossRef
44.
Zurück zum Zitat Shytle RD, Mori T, Townsend K, Vendrame M, Sun N, Zeng J, Ehrhart J, Silver AA, Sanberg PR, Tan J (2004) Cholinergic modulation of microglial activation by alpha 7 nicotinic receptors. J Neurochem 89:337–343CrossRef Shytle RD, Mori T, Townsend K, Vendrame M, Sun N, Zeng J, Ehrhart J, Silver AA, Sanberg PR, Tan J (2004) Cholinergic modulation of microglial activation by alpha 7 nicotinic receptors. J Neurochem 89:337–343CrossRef
45.
Zurück zum Zitat Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384–388CrossRef Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384–388CrossRef
46.
Zurück zum Zitat Bernik TR, Friedman SG, Ochani M, DiRaimo R, Susarla S, Czura CJ, Tracey KJ (2002) Cholinergic antiinflammatory pathway inhibition of tumor necrosis factor during ischemia reperfusion. J Vasc Surg 36:1231–1236CrossRef Bernik TR, Friedman SG, Ochani M, DiRaimo R, Susarla S, Czura CJ, Tracey KJ (2002) Cholinergic antiinflammatory pathway inhibition of tumor necrosis factor during ischemia reperfusion. J Vasc Surg 36:1231–1236CrossRef
47.
Zurück zum Zitat Guarini S, Altavilla D, Cainazzo MM, Giuliani D, Bigiani A, Marini H, Squadrito G, Minutoli L, Bertolini A, Marini R, Adamo EB, Venuti FS, Squadrito F (2003) Efferent vagal fibre stimulation blunts nuclear factor–kappaB activation and protects against hypovolemic hemorrhagic shock. Circulation 107:1189–1194CrossRef Guarini S, Altavilla D, Cainazzo MM, Giuliani D, Bigiani A, Marini H, Squadrito G, Minutoli L, Bertolini A, Marini R, Adamo EB, Venuti FS, Squadrito F (2003) Efferent vagal fibre stimulation blunts nuclear factor–kappaB activation and protects against hypovolemic hemorrhagic shock. Circulation 107:1189–1194CrossRef
48.
Zurück zum Zitat Mioni C, Bazzani C, Giuliani D, Altavilla D, Leone S, Ferrari A, Minutoli L, Bitto A, Marini H, Zaffe D, Botticelli AR, Iannone A, Tomasi A, Bigiani A, Bertolini A, Squadrito F, Guarini S (2005) Activation of an efferent cholinergic pathway produces strong protection against myocardial ischemia/reperfusion injury in rats. Crit Care Med 33:2621–2628CrossRef Mioni C, Bazzani C, Giuliani D, Altavilla D, Leone S, Ferrari A, Minutoli L, Bitto A, Marini H, Zaffe D, Botticelli AR, Iannone A, Tomasi A, Bigiani A, Bertolini A, Squadrito F, Guarini S (2005) Activation of an efferent cholinergic pathway produces strong protection against myocardial ischemia/reperfusion injury in rats. Crit Care Med 33:2621–2628CrossRef
49.
Zurück zum Zitat van Westerloo DJ, Giebelen IA, Florquin S, Bruno MJ, Larosa GJ, Ulloa L, Tracey KJ, van der Poll T (2006) The vagus nerve and nicotinic receptors modulate experimental pancreatitis severity in mice. Gastroenterology 130:1822–1830CrossRef van Westerloo DJ, Giebelen IA, Florquin S, Bruno MJ, Larosa GJ, Ulloa L, Tracey KJ, van der Poll T (2006) The vagus nerve and nicotinic receptors modulate experimental pancreatitis severity in mice. Gastroenterology 130:1822–1830CrossRef
50.
51.
Zurück zum Zitat Ghyczy M, Torday C, Kaszaki J, Szabó A, Czóbel M, Boros M (2008) Hypoxia-induced generation of methane in mitochondria and eukaryotic cells: an alternative approach to methanogenesis. Cell Physiol Biochem 21:251–258. doi:10.1159/000113766 CrossRef Ghyczy M, Torday C, Kaszaki J, Szabó A, Czóbel M, Boros M (2008) Hypoxia-induced generation of methane in mitochondria and eukaryotic cells: an alternative approach to methanogenesis. Cell Physiol Biochem 21:251–258. doi:10.​1159/​000113766 CrossRef
52.
Zurück zum Zitat Tuboly E, Szabó A, Garab D, Bartha G, Janovszky Á, Erős G, Szabó A, Mohácsi Á, Szabó G, Kaszaki J, Ghyczy M, Boros M (2013) Methane biogenesis during sodium azide-induced chemical hypoxia in rats. Am J Physiol Cell Physiol 304:C207–C214. doi:10.1152/ajpcell.00300.2012 CrossRef Tuboly E, Szabó A, Garab D, Bartha G, Janovszky Á, Erős G, Szabó A, Mohácsi Á, Szabó G, Kaszaki J, Ghyczy M, Boros M (2013) Methane biogenesis during sodium azide-induced chemical hypoxia in rats. Am J Physiol Cell Physiol 304:C207–C214. doi:10.​1152/​ajpcell.​00300.​2012 CrossRef
Metadaten
Titel
Protective effects of l-alpha-glycerylphosphorylcholine on ischaemia–reperfusion-induced inflammatory reactions
verfasst von
Tünde Tőkés
Eszter Tuboly
Gabriella Varga
László Major
Miklós Ghyczy
József Kaszaki
Mihály Boros
Publikationsdatum
01.02.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nutrition / Ausgabe 1/2015
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-014-0691-2

Weitere Artikel der Ausgabe 1/2015

European Journal of Nutrition 1/2015 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.