Skip to main content
Erschienen in: European Journal of Nutrition 3/2014

01.04.2014 | Original Contribution

Long-term dietary l-arginine supplementation increases endothelial nitric oxide synthase and vasoactive intestinal peptide immunoexpression in rat small intestine

verfasst von: Ksenija Velickovic, Milica Markelic, Igor Golic, Vesna Otasevic, Ana Stancic, Aleksandra Jankovic, Milica Vucetic, Biljana Buzadzic, Bato Korac, Aleksandra Korac

Erschienen in: European Journal of Nutrition | Ausgabe 3/2014

Einloggen, um Zugang zu erhalten

Abstract

Background and aims

Nitric oxide (NO) and vasoactive intestinal polypeptide (VIP) are important intestinal neurotransmitters that coexist in the gut enteric nervous system and play an important role in intestinal physiology (e.g., absorption, motility, fluid secretion and smooth muscle relaxation). It is also known that cold exposure alters several aspects of gastrointestinal physiology and induces hyperphagia to meet increased metabolic demands, but there are no data regarding NO and VIP involvement in intestinal response during acclimation to cold. The objective of this study was to determine the influence of long-term l-arginine supplementation on the expression of the three isoforms of nitric oxide synthase (NOS) and VIP in small intestine of rats acclimated to room temperature or cold.

Methods

Animals (six per group) acclimated to room temperature (22 ± 1 °C) and cold (4 ± 1 °C), respectively, were treated with 2.25 % l-arginine, a substrate for NOSs, or with 0.01 % N ω-nitro-l-arginine methyl ester, an inhibitor of NOSs, for 45 days. The topographical distribution of VIP and NOSs expression in small intestine was studied by immunohistochemistry, and ImageJ software was used for semiquantitative densitometric analysis of their immunoexpression.

Results

Long-term dietary l-arginine supplementation increases VIP and NOSs immunoexpression at room temperature while at cold increases the endothelial NOS, inducible NOS and VIP but decrease neuronal NOS in rat small intestine.

Conclusion

Our results demonstrate that long-term dietary l-arginine supplementation modulates NOSs and VIP immunoexpression in rat small intestine with respect to ambient temperature, pointing out the eNOS as a predominant NOS isoform with an immunoexpression pattern similar to VIP.
Literatur
1.
Zurück zum Zitat Wu G, Morris SM Jr (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336:1–17 Wu G, Morris SM Jr (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336:1–17
2.
Zurück zum Zitat Wu X, Ruan Z, Gao Y, Yin Y, Zhou X, Wang L, Geng M, Hou Y, Wu G (2010) Dietary supplementation with l-arginine or N-carbamylglutamate enhances intestinal growth and heat shock protein-70 expression in weanling pigs fed a corn- and soybean- meal-based diet. Amino Acids 39:831–839CrossRef Wu X, Ruan Z, Gao Y, Yin Y, Zhou X, Wang L, Geng M, Hou Y, Wu G (2010) Dietary supplementation with l-arginine or N-carbamylglutamate enhances intestinal growth and heat shock protein-70 expression in weanling pigs fed a corn- and soybean- meal-based diet. Amino Acids 39:831–839CrossRef
3.
Zurück zum Zitat Koppelmann T, Pollak Y, Mogilner J, Bejar J, Coran AG, Sukhotnik I (2012) Dietary l-arginine supplementation reduces Methotrexate-induced intestinal mucosal injury in rat. BMC Gastroenterol 12:41CrossRef Koppelmann T, Pollak Y, Mogilner J, Bejar J, Coran AG, Sukhotnik I (2012) Dietary l-arginine supplementation reduces Methotrexate-induced intestinal mucosal injury in rat. BMC Gastroenterol 12:41CrossRef
4.
Zurück zum Zitat Yao K, Guan S, Li T, Huang R, Wu G, Ruan Z, Yin Y (2011) Dietary l-arginine supplementation enhances intestinal development and expression of vascular endothelial growth factor in weanling piglets. Br J Nutr 105:703–709CrossRef Yao K, Guan S, Li T, Huang R, Wu G, Ruan Z, Yin Y (2011) Dietary l-arginine supplementation enhances intestinal development and expression of vascular endothelial growth factor in weanling piglets. Br J Nutr 105:703–709CrossRef
5.
Zurück zum Zitat Taboada MC, Rodriguez B, Millan R, Miguez I (2006) Role of dietary l-arginine supplementation on serum parameters and intestinal enzyme activities in rats fed an excess-fat diet. Biomed Pharmacother 60:10–13CrossRef Taboada MC, Rodriguez B, Millan R, Miguez I (2006) Role of dietary l-arginine supplementation on serum parameters and intestinal enzyme activities in rats fed an excess-fat diet. Biomed Pharmacother 60:10–13CrossRef
6.
Zurück zum Zitat Janero DR (2001) Nutritional aspects of nitric oxide: human health implications and therapeutic opportunities. Nutrition 17:896–903CrossRef Janero DR (2001) Nutritional aspects of nitric oxide: human health implications and therapeutic opportunities. Nutrition 17:896–903CrossRef
7.
Zurück zum Zitat Petrovic V, Korac A, Buzadzic B, Korac B (2005) The effects of l-arginine and l-NAME supplementation on redox-regulation and thermogenesis in interscapular brown adipose tissue. J Exp Biol 208:4263–4271CrossRef Petrovic V, Korac A, Buzadzic B, Korac B (2005) The effects of l-arginine and l-NAME supplementation on redox-regulation and thermogenesis in interscapular brown adipose tissue. J Exp Biol 208:4263–4271CrossRef
8.
Zurück zum Zitat Beck PL, Xavier R, Wong J, Ezedi I, Mashimo H, Mizoguchi A, Mizoguchi E, Bhan AK, Podolsky DK (2004) Paradoxical roles of different nitric oxide synthase isoforms in colonic injury. Am J Physiol Gastrointest Liver Physiol 286:137–147CrossRef Beck PL, Xavier R, Wong J, Ezedi I, Mashimo H, Mizoguchi A, Mizoguchi E, Bhan AK, Podolsky DK (2004) Paradoxical roles of different nitric oxide synthase isoforms in colonic injury. Am J Physiol Gastrointest Liver Physiol 286:137–147CrossRef
9.
Zurück zum Zitat Petersson J, Schreiber O, Steege A, Patzak A, Hellsten A, Phillipson M, Holm L (2007) eNOS involved in colitis-induced mucosal blood flow increase. Am J Physiol Gastrointest Liver Physiol 293:1281–1287CrossRef Petersson J, Schreiber O, Steege A, Patzak A, Hellsten A, Phillipson M, Holm L (2007) eNOS involved in colitis-induced mucosal blood flow increase. Am J Physiol Gastrointest Liver Physiol 293:1281–1287CrossRef
10.
Zurück zum Zitat Castro M, Munoz JM, Arruebo MP, Murillo MD, Arnal C, Bonafonte JI, Plaza MA (2012) Involvement of neuronal nitric oxide synthase (nNOS) in the regulation of migrating motor complex (MMC) in sheep. Vet J 192:352–358CrossRef Castro M, Munoz JM, Arruebo MP, Murillo MD, Arnal C, Bonafonte JI, Plaza MA (2012) Involvement of neuronal nitric oxide synthase (nNOS) in the regulation of migrating motor complex (MMC) in sheep. Vet J 192:352–358CrossRef
11.
Zurück zum Zitat Hansen MB (2003) Neurohumoral control of gastrointestinal motility. Physiol Res 52:1–30 Hansen MB (2003) Neurohumoral control of gastrointestinal motility. Physiol Res 52:1–30
12.
Zurück zum Zitat Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347(6295):768–770CrossRef Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347(6295):768–770CrossRef
13.
Zurück zum Zitat Suthamnatpong N, Hata F, Kanada A, Takeuchi T, Yagasaki O (1993) Mediators of nonadrenergic, noncholinergic inhibition in the proximal, middle and distal regions of rat colon. Br J Pharmacol 108:348–355CrossRef Suthamnatpong N, Hata F, Kanada A, Takeuchi T, Yagasaki O (1993) Mediators of nonadrenergic, noncholinergic inhibition in the proximal, middle and distal regions of rat colon. Br J Pharmacol 108:348–355CrossRef
14.
Zurück zum Zitat Furness JB, Bornstein JC, Murphy R, Pompolo S (1992) Roles of peptides in transmission in the enteric nervous system. Trends Neurosci 15:66–71CrossRef Furness JB, Bornstein JC, Murphy R, Pompolo S (1992) Roles of peptides in transmission in the enteric nervous system. Trends Neurosci 15:66–71CrossRef
15.
Zurück zum Zitat Dick JM, Van Molle W, Brouckaert P, Lefebvre RA (2002) Relaxation by vasoactive intestinal polypeptide in the gastric fundus of nitric oxide synthase-deficient mice. J Physiol 538:133–143CrossRef Dick JM, Van Molle W, Brouckaert P, Lefebvre RA (2002) Relaxation by vasoactive intestinal polypeptide in the gastric fundus of nitric oxide synthase-deficient mice. J Physiol 538:133–143CrossRef
16.
Zurück zum Zitat Grider JR (1993) Interplay of VIP and nitric oxide in regulation of the descending relaxation phase of peristalsis. Am J Physiol 264:334–340 Grider JR (1993) Interplay of VIP and nitric oxide in regulation of the descending relaxation phase of peristalsis. Am J Physiol 264:334–340
17.
Zurück zum Zitat Murthy KS, Grider JR, Jin JG, Makhlouf GM (1996) Interplay of VIP and nitric oxide in the regulation of neuromuscular function in the gut. Ann NY Acad Sci 805:355–362CrossRef Murthy KS, Grider JR, Jin JG, Makhlouf GM (1996) Interplay of VIP and nitric oxide in the regulation of neuromuscular function in the gut. Ann NY Acad Sci 805:355–362CrossRef
18.
Zurück zum Zitat Grider JR, Murthy KS (2008) Autoinhibition of endothelial nitric oxide synthase (eNOS) in gut smooth muscle by nitric oxide. Regul Pept 151:75–79CrossRef Grider JR, Murthy KS (2008) Autoinhibition of endothelial nitric oxide synthase (eNOS) in gut smooth muscle by nitric oxide. Regul Pept 151:75–79CrossRef
19.
Zurück zum Zitat Kaushik S, Kaur J (2003) Chronic cold exposure affects the antioxidant defense system in various rat tissues. Clin Chim Acta 333:69–77CrossRef Kaushik S, Kaur J (2003) Chronic cold exposure affects the antioxidant defense system in various rat tissues. Clin Chim Acta 333:69–77CrossRef
20.
Zurück zum Zitat Kaushik S, Kaur J (2005) Effect of chronic cold stress on intestinal epithelial cell proliferation and inflammation in rats. Stress 8:191–197CrossRef Kaushik S, Kaur J (2005) Effect of chronic cold stress on intestinal epithelial cell proliferation and inflammation in rats. Stress 8:191–197CrossRef
21.
Zurück zum Zitat Soderholm JD, Perdue MH (2001) Stress and gastrointestinal tract. II. Stress and intestinal barrier function. Am J Physiol Gastrointest Liver Physiol 280:7–13 Soderholm JD, Perdue MH (2001) Stress and gastrointestinal tract. II. Stress and intestinal barrier function. Am J Physiol Gastrointest Liver Physiol 280:7–13
22.
Zurück zum Zitat Irwin N, Francis JM, Flatt PR (2011) Alterations of glucose-dependent insulinotropic polypeptide (GIP) during cold acclimation. Regul Pept 167:91–96CrossRef Irwin N, Francis JM, Flatt PR (2011) Alterations of glucose-dependent insulinotropic polypeptide (GIP) during cold acclimation. Regul Pept 167:91–96CrossRef
23.
Zurück zum Zitat Saha SK, Ohinata H, Kuroshima A (1996) Effects of acute and chronic inhibition of nitric oxide synthase on brown adipose tissue thermogenesis. Jpn J Physiol 46:375–382CrossRef Saha SK, Ohinata H, Kuroshima A (1996) Effects of acute and chronic inhibition of nitric oxide synthase on brown adipose tissue thermogenesis. Jpn J Physiol 46:375–382CrossRef
24.
Zurück zum Zitat Petrovic V, Buzadzic B, Korac A, Vasilijevic A, Jankovic A, Micunovic K, Korac B (2008) Antioxidative defence alterations in skeletal muscle during prolonged acclimation to cold: role of l-arginine/NO-producing pathway. J Exp Biol 211:114–120CrossRef Petrovic V, Buzadzic B, Korac A, Vasilijevic A, Jankovic A, Micunovic K, Korac B (2008) Antioxidative defence alterations in skeletal muscle during prolonged acclimation to cold: role of l-arginine/NO-producing pathway. J Exp Biol 211:114–120CrossRef
25.
Zurück zum Zitat He J, Sun X, Qian K-Q, Liu X, Wang Z, Chen Y (2009) Protection of cerulein-induced pancreatic fibrosis by pancreas-specific expression of Smad7. Biochim Biophys Acta 1792:56–60CrossRef He J, Sun X, Qian K-Q, Liu X, Wang Z, Chen Y (2009) Protection of cerulein-induced pancreatic fibrosis by pancreas-specific expression of Smad7. Biochim Biophys Acta 1792:56–60CrossRef
26.
Zurück zum Zitat Qu XW, Wang H, De Plaen IG, Rozenfeld RA, Hsueh W (2001) Neuronal nitric oxide synthase (NOS) regulates the expression of inducible NOS in rat small intestine via modulation of nuclear factor kappa B. FASEB J 15:439–446CrossRef Qu XW, Wang H, De Plaen IG, Rozenfeld RA, Hsueh W (2001) Neuronal nitric oxide synthase (NOS) regulates the expression of inducible NOS in rat small intestine via modulation of nuclear factor kappa B. FASEB J 15:439–446CrossRef
27.
Zurück zum Zitat Teshfam M, Brujeni GN, Hassanpour H (2006) Evaluation of endothelial and inducible nitric oxide synthase mRNA expression in the lung of broiler chickens with developmental pulmonary hypertension due to cold stress. Br Poult Sci 47:223–229CrossRef Teshfam M, Brujeni GN, Hassanpour H (2006) Evaluation of endothelial and inducible nitric oxide synthase mRNA expression in the lung of broiler chickens with developmental pulmonary hypertension due to cold stress. Br Poult Sci 47:223–229CrossRef
28.
Zurück zum Zitat Mourad FH, Barada KA, Abdel-Malak N, Bou Rached NA, Khoury CI, Saade NE, Nassar CF (2003) Interplay between nitric oxide and vasoactive intestinal polypeptide in inducing fluid secretion in rat jejunum. J Physiol 550:863–871CrossRef Mourad FH, Barada KA, Abdel-Malak N, Bou Rached NA, Khoury CI, Saade NE, Nassar CF (2003) Interplay between nitric oxide and vasoactive intestinal polypeptide in inducing fluid secretion in rat jejunum. J Physiol 550:863–871CrossRef
29.
Zurück zum Zitat Nishizaki K, Nakao K, Ishii H, Yamanaka H, Tokunaga A, Nakagawa K, Yamamura T, Noguchi K (2003) Induction of neuronal nitric oxide synthase by sympathetic denervation is mediated via alpha 2-adrenoceptors in the jejunal myenteric plexus. Brain Res 965:121–129CrossRef Nishizaki K, Nakao K, Ishii H, Yamanaka H, Tokunaga A, Nakagawa K, Yamamura T, Noguchi K (2003) Induction of neuronal nitric oxide synthase by sympathetic denervation is mediated via alpha 2-adrenoceptors in the jejunal myenteric plexus. Brain Res 965:121–129CrossRef
30.
Zurück zum Zitat Takahashi T (2003) Pathophysiological significance of neuronal nitric oxide synthase in the gastrointestinal tract. J Gastroenterol 38:421–430CrossRef Takahashi T (2003) Pathophysiological significance of neuronal nitric oxide synthase in the gastrointestinal tract. J Gastroenterol 38:421–430CrossRef
31.
Zurück zum Zitat Xie QW, Cho HJ, Calaycay J, Mumford RA, Swiderek KM, Lee TD, Ding A, Troso T, Nathan C (1992) Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256:225–228CrossRef Xie QW, Cho HJ, Calaycay J, Mumford RA, Swiderek KM, Lee TD, Ding A, Troso T, Nathan C (1992) Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256:225–228CrossRef
32.
Zurück zum Zitat Porras M, Martin MT, Torres R, Vergara P (2006) Cyclical upregulated iNOS and long-term downregulated nNOS are the bases for relapse and quiescent phases in a rat model of IBD. Am J Physiol Gastrointest Liver Physiol 290:423–430CrossRef Porras M, Martin MT, Torres R, Vergara P (2006) Cyclical upregulated iNOS and long-term downregulated nNOS are the bases for relapse and quiescent phases in a rat model of IBD. Am J Physiol Gastrointest Liver Physiol 290:423–430CrossRef
33.
Zurück zum Zitat Wang XY, Paterson C, Huizinga JD (2003) Cholinergic and nitrergic innervation of ICC-DMP and ICC-IM in the human small intestine. Neurogastroenterol Motil 15:531–543CrossRef Wang XY, Paterson C, Huizinga JD (2003) Cholinergic and nitrergic innervation of ICC-DMP and ICC-IM in the human small intestine. Neurogastroenterol Motil 15:531–543CrossRef
34.
Zurück zum Zitat Streutker CJ, Huizinga JD, Driman DK, Riddell RH (2007) Interstitial cells of Cajal in health and disease. Part I: normal ICC structure and function with associated motility disorders. Histopathology 50:176–189CrossRef Streutker CJ, Huizinga JD, Driman DK, Riddell RH (2007) Interstitial cells of Cajal in health and disease. Part I: normal ICC structure and function with associated motility disorders. Histopathology 50:176–189CrossRef
Metadaten
Titel
Long-term dietary l-arginine supplementation increases endothelial nitric oxide synthase and vasoactive intestinal peptide immunoexpression in rat small intestine
verfasst von
Ksenija Velickovic
Milica Markelic
Igor Golic
Vesna Otasevic
Ana Stancic
Aleksandra Jankovic
Milica Vucetic
Biljana Buzadzic
Bato Korac
Aleksandra Korac
Publikationsdatum
01.04.2014
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nutrition / Ausgabe 3/2014
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-013-0585-8

Weitere Artikel der Ausgabe 3/2014

European Journal of Nutrition 3/2014 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Notfall-TEP der Hüfte ist auch bei 90-Jährigen machbar

26.04.2024 Hüft-TEP Nachrichten

Ob bei einer Notfalloperation nach Schenkelhalsfraktur eine Hemiarthroplastik oder eine totale Endoprothese (TEP) eingebaut wird, sollte nicht allein vom Alter der Patientinnen und Patienten abhängen. Auch über 90-Jährige können von der TEP profitieren.

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Bei schweren Reaktionen auf Insektenstiche empfiehlt sich eine spezifische Immuntherapie

Insektenstiche sind bei Erwachsenen die häufigsten Auslöser einer Anaphylaxie. Einen wirksamen Schutz vor schweren anaphylaktischen Reaktionen bietet die allergenspezifische Immuntherapie. Jedoch kommt sie noch viel zu selten zum Einsatz.

Therapiestart mit Blutdrucksenkern erhöht Frakturrisiko

25.04.2024 Hypertonie Nachrichten

Beginnen ältere Männer im Pflegeheim eine Antihypertensiva-Therapie, dann ist die Frakturrate in den folgenden 30 Tagen mehr als verdoppelt. Besonders häufig stürzen Demenzkranke und Männer, die erstmals Blutdrucksenker nehmen. Dafür spricht eine Analyse unter US-Veteranen.

Update Innere Medizin

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