Oryza sativa L. extracts inhibit nitric oxide production and inducible nitric oxide synthase expression in murine macrophage cells and lungs of antigen-challenged allergic mice

Authors

  • Cheol Yong Lee Center for Animal Resources Development, Wonkwang University, 344-2, Sinyong-dong, Jeolabuk-do, Iksan, Republic of Korea Korea, Republic o
  • Min Jung Lee Research center, Dong-A ST, Yong-in, Gyeonggi-do, 446-905, Republic of Korea Korea, Republic of
  • Ju Mi Kim Research center, Dong-A ST, Yong-in, Gyeonggi-do, 446-905, Republic of Korea Korea, Republic of
  • Seul Min Choi Division of Toxicology, College of Pharmacy, Sungkyunkwan University, Chunchun-dong 300, Changan-ku, Suwon, Gyeonggi-do, 440-746, Republic of Korea Korea, Republic o
  • Kyung Koo Kang Research center, Dong-A ST, Yong-in, Gyeonggi-do, 446-905, Republic of Korea Korea, Republic of
  • Ok Jin Kim Center for Animal Resources Development, Wonkwang University, 344-2, Sinyong-dong, Jeolabuk-do, Iksan, Republic of Korea Korea, Republic of
  • Byung Mu Lee 3Division of Toxicology, College of Pharmacy, Sungkyunkwan University, Chunchun-dong 300, Changan-ku, Suwon, Gyeonggi-do, 440-746, Republic of Korea Korea, Republic of

Keywords:

Asthma, Oryza sativa, nitric oxide, iNOS expression, DA-9201

Abstract

Hyper-production of nitric oxide (NO) has been observed in the airways of patients with asthma and may contribute to airway inflammatory responses. Previous studies showed that DA-9201, an ethanolic extract of Oryza sativa L., significantly attenuated airway hyperresponsiveness, airway inflammation, and remodeling in murine models of asthma. The purpose of this study was to examine the effect of DA-9201 on the expression of inducible NO synthase (iNOS) and NO production in RAW 264.7 murine macrophage cells and ovalbumin (OVA)-sensitized allergic mice. The levels of NO and iNOS expression in lipopolysaccharide (LPS)-stimulated RAW 264.7 cells were determined. Allergic inflammation was induced in mice by immunization with OVA and these mice were administered DA-9201 daily at 30, 100 or 300 mg/kg for 2 weeks. Mice were challenged with allergen by inhalation during the last 3 days of DA-9201 treatment and lungs were harvested 24 h after the last challenge. NO levels in blood plasma and iNOS expression in lung tissue were determined by ELISA and western blotting, respectively. DA-9201 inhibited the production of NO and iNOS gene and protein expression in a dose-dependent manner in LPS-stimulated cells. In the lungs of allergen-challenged mice, DA-9201 caused a significant decrease in iNOS protein expression. Furthermore, we found that DA-9201 significantly decreased NO levels in blood plasma. These results suggest that DA-9201 inhibits NO production by limiting the expression of iNOS, which may be one of the underlying mechanisms its anti-asthmatic effect.

References

Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 1991; 43: 109–142

Ricciardolo FL, Sterk PJ, Gaston B, Folkerts G. Nitric oxide in health and disease of the respiratory system. Physiol Rev 2004; 84: 731–765

Dupont LL, Glynos C, Bracke KR, Brouckaert P, Brusselle GG. Role of the nitric oxide-soluble guanylyl cyclase pathway in obstructive airway diseases. Pulm Pharmacol Ther 2014; 29: 1–6

Xie QW, Cho HJ, Calacay J, Mumford RA, Swiderek KM, Lee TD, Ding A, Troso T, Nathan C. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 1992; 256: 225–228

Borish L, Mascali JJ, Dishuck J, Beam WR, Martin RJ, Rosenwasser LJ. Detection of alveolar macrophage-derived IL-1b in asthma: inhibition with corticosteroids. J Immunol 1992; 149: 3078–3082

Cembrzynska-Nowak M, Szlarz E, Inglot AD, Tedodroezyk-Injeyan JA. Elevated release of tumor necrosis factor-alpha and interferon-gamma by bronchoalveolar lavage leukocytes from patients with bronchial asthma. Am Rev Respir Dis 1993; 142: 291–295

Redington AE, Meng QH, Springall DR, Evans TJ, Creminon C, Maclouf J, Holgate S T, Howarth PH, Polak JM. Increased expression of inducible nitric oxide synthase and cyclo-oxygenase-2 in the airway epithelium of asthmatic subjects and regulation by corticosteroid treatment. Thorax 2001; 56: 351–357

Barnes PJ, Liew FY. Nitric oxide and asthmatic inflammation. Immunol Today 1995; 16: 128–130

Hansel TT, Kharitonov SA, Donnelly LE, Erin EM, Currie MG, Moore WM, Manning PT, Recker DP, Barnes PJ. A selective inhibitor of inducible nitric oxide synthase inhibits exhaled breath nitric oxide in healthy volunteers and asthmatics. FASEB J 2003; 17: 1298–1300

Anderson JT, Zeng M, Li Q, Stapley R, Moore DR 2nd, Chenna B, Fineberg N, Zmijewski J, Eltoum IE, Siegal GP, Gaggar A, Barnes S, Velu SE, Thannickal VJ, Abraham E, Patel RP, Lancaster JR Jr, Chaplin DD, Dransfield MT, Deshane JS. Elevated levels of NO are localized to distal airways in asthma. Free Radic Biol Med 2011; 50: 1679–1688

Roos AB, Mori M, Grönneberg R, Österlund C, Claesson HE, Wahlström J, Grunewald J, Eklund A, Erjefält JS, Lundberg JO, Nord M. Elevated exhaled nitric oxide in allergen-provoked asthma is associated with airway epithelial iNOS. PLoS One 2014; 9: e90018

Fujiwaki T, Furusho K. The effects of rice bran broth bathing in patients with atopic dermatitis. Acta Paediatr Jpn 1992; 34: 505–510

Maeda H, Ichihashi K, Fujii T, Omura K, Zhu X, Anazawa M, Tazawa K. Oral administration of hydrolyzed rice bran prevents the common cold syndrome in the elderly based on its immunomodulatory action. Biofactors 2004; 21: 185–187

Kim HM, Kang CS, Lee EH, Shin TY. The evaluation of the antianaphylactic effect ofOryza sativa L. subsp. hsien Ting in rats. Pharmacol Res 1999; 40: 31–36

Kim HM, Yi DK, Shin HY. The evaluation of antianaphylactic effect of Oryza sativaL. in rats. Am J Chin Med 1996b; 27: 63–71

Ling WH, Wang LL, Ma J. Supplementation of the black rice outer layer fraction to rabbits decreases atherosclerotic plaque formation and increases antioxidant status. J Nutr 2002; 132: 20–26

Miyazawa M, Oshima T, Koshio K, Itsuzaki Y, Anzai J. Tyrosinase inhibitor from black rice bran. J Agric Food Chem 2003; 51: 6953–6956

Lee SH, Seo MJ, Choi SM, Sohn YS, Kang KK, Ahn BO, Kwon JW, Yoo M. DA-9201 shows anti-asthmatic effects by suppressing NF-kappaB expression in an ovalbumin-induced mouse model of asthma. Arch Pharm Res 2005; 28: 1350–1357

Lee SH, Choi, SM, Sohn YS, Kang KK, Yoo M. Effect of Oryza sativa extract on the progression of airway inflammation and remodeling in an experimental animal model of asthma. Planta Med 2006; 72: 405–410

Lee SH, Sohn YS, Kang KK, Kwon JW, Yoo M. Inhibitory Effect of DA-9201, an extract of Oryza sativa L., on airway inflammation and bronchial hyperresponsiveness in mouse asthma model. Biol Pharm Bull 2006; 29: 1148–1153

Denizot F, Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 1986; 89: 271–277

Green LC, Ruiz de Luzuriaga K, Wagner DA, Rand W, Istfan N, Young VR, Tannenbaum SR. Nitrate biosynthesis in man. Proc Natl Acad Sci U S A 1981; 78: 7764–7768

Nijkamp FP, van der Linde HJ, Folkerts G. Nitric oxide synthesis inhibitors induce airway hyperresponsiveness in the guinea pig in vivo and in vitro. Role of the epithelium. Am Rev Respir Dis 1993; 148: 727–734

Feletou M, Lonchampt M, Coge F, Galizzi JP, Bassoullet C, Merial C, Robineau P, Boutin JA, Huang PL, Vanhoutte PM, Canet E. Regulation of murine airway responsiveness by endothelial nitric oxide synthase. Am J Physiol Lung Cell Mol Physiol 2001; 281: 258–267

Zuo L, Koozechian MS, Chen LL. Characterization of reactive nitrogen species in allergic asthma. Ann Allergy Asthma Immunol 2014; 112: 18–22

Xiong Y, Karupiah G, Hogan SP, Foster PS, Ramsay AJ. Inhibition of allergic airway inflammation in mice lacking nitric oxide synthase 2. J Immunol 1999; 162: 445–452

Lowenstein CJ, Alley EW, Raval P, Snowman AM, Snyder SH, Russell SW, Murphy WJ. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc Natl Acad Sci USA 1993; 90:9730–9734

Xie QW, Kashiwabara Y, Nathan, C. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J Biol Chem 1994; 269: 4705–4708

Taylor BS, de Vera ME, Ganster RW, Wang Q, Shapiro RA, Morris SM Jr, Billiar TR, Geller DA. Multiple NF-kappaB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J Biol Chem 1998; 273: 15148–15156

Lin YL, Lin JK. (-)-Epigallocatechin-3-gallate blocks the induction of nitric oxide synthase by down-regulating lipopolysaccharide-induced activity of transcription factor nuclear factor-kappaB. Mol Pharmacol 1997; 52: 465–472

Hwang SJ, Kim YW, Park Y, Lee HJ, Kim KW. Anti-inflammatory effects of chlorogenic acid in lipopolysaccharide-stimulated RAW 264.7 cells. Inflamm Res 2014; 63: 81–90

Kleinert H, Euchenhofer C, Ihrig-Biedert I, Forstermann U. Glucocorticoids inhibit the induction of nitric oxide synthase II by down-regulating cytokine-induced activity of transcription factor nuclear factor-kappa B. Mol Pharmacol 1996; 49: 15–21

Downloads

Published

31-03-2015

How to Cite

1.
Cheol Yong Lee, Min Jung Lee, Ju Mi Kim, Seul Min Choi, Kyung Koo Kang, Ok Jin Kim, Byung Mu Lee. Oryza sativa L. extracts inhibit nitric oxide production and inducible nitric oxide synthase expression in murine macrophage cells and lungs of antigen-challenged allergic mice. ijp [Internet]. 2015 Mar. 31 [cited 2024 Nov. 22];7(1):1-7. Available from: https://ijp.arjournals.org/index.php/ijp/article/view/380

Issue

Section

Original Research Articles