Anti-inflammatory and immunomodulatory effects of Spirulina platensis in comparison to Dunaliella salina in acetic acid-induced rat experimental colitis

Immunopharmacology and Immunotoxicology

Volumn 37, Issue 2, 2015, Pages 126-139

  Abdel Daim, Mohamed M ^a   Farouk, Sameh M ^a   Madkour, Fedekar F ^b   Azab, Samar S ^c  

^a Suez Canal University   (Egypt)

^b Port Said University   (Egypt)

^c African Union Organization St Abbassia   (Egypt)

Author keywords

Lipid peroxidation; Myeloperoxidase; Oxidative stress; Protein carbonyl; Tumor necrosis factor

Indexed keywords

ACETIC ACID; ANTIINFLAMMATORY AGENT; CATALASE; DUNALIELLA SALINA EXTRACT; GLUTATHIONE; IMMUNOMODULATING AGENT; INTERLEUKIN 1BETA; INTERLEUKIN 6; MALONALDEHYDE; MYELOPEROXIDASE; PLANT EXTRACT; PROSTAGLANDIN; SALAZOSULFAPYRIDINE; SPIRULINA EXTRACT; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; IMMUNOLOGIC FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTHROSPIRA PLATENSIS; ARTICLE; BODY WEIGHT; COLON; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG EFFECT; DUNALIELLA SALINA; IMMUNOMODULATION; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; ULCERATIVE COLITIS; ANIMAL; CHEMICALLY INDUCED; COLITIS, ULCERATIVE; DRUG EFFECTS; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; SOLANACEAE; SPIRULINA; WISTAR RAT;

DUNALIELLA; DUNALIELLA SALINA; RATTUS; SPIRULINA; SPIRULINA PLATENSIS;

ACETIC ACID; ANIMALS; ANTI-INFLAMMATORY AGENTS; COLITIS, ULCERATIVE; IMMUNOLOGIC FACTORS; LIPID PEROXIDATION; MALE; OXIDATIVE STRESS; PLANT EXTRACTS; RATS; RATS, WISTAR; SOLANACEAE; SPIRULINA;

EID: 84924704454     PISSN: 08923973     EISSN: 15322513     Source Type: Journal    
DOI: 10.3109/08923973.2014.998368     Document Type: Article

References (55)

1. Podolsky DK. Inflammatory bowel disease. N Engl J Med 2002;347:417-429.
2. Fiocchi C. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 1998;115:182-205.
3. Loftus Jr EV. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology 2004;126:1504-1517.
4. Korzenik JR, Podolsky DK. Evolving knowledge and therapy of inflammatory bowel disease. Nat Rev Drug Discov 2006;5:197-209.
5. Ardizzone S, Bianchi Porro G. Biologic therapy for inflammatory bowel disease. Drugs 2005;65:2253-2286.
6. Nakamura K, Honda K, Mizutani T, et al. Novel strategies for the treatment of inflammatory bowel disease: selective inhibition of cytokines and adhesion molecules. World J Gastroenterol 2006;12:4628-4635.
7. Krimsky M, Yedgar S, Aptekar L, et al. Amelioration of TNBS-induced colon inflammation in rats by phospholipase A2 inhibitor. Am J Physiol Gastrointest Liver Physiol 2003;285:G586-G592.
8. Dionne S, Hiscott J, D'Agata I, et al. Quantitative PCR analysis of TNF-alpha and IL-1 beta mRNA levels in pediatric IBD mucosal biopsies. Dig Dis Sci 1997;42:1557-1566.
9. Munakata W, Liu Q, Shimoyama T, et al. Ecabet sodium attenuates reactive oxygen species produced by neutrophils after priming with bacterial lipopolysaccharides. Luminescence 2003;18:330-333.
10. Simon LS. Role and regulation of cyclooxygenase-2 during inflammation. Am J Med 1999;106:37S-42S.
11. Nussler AK, Billiar TR. Inflammation, immunoregulation, and inducible nitric oxide synthase. J Leukoc Biol 1993;54:171-178.
12. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J 1992;6:3051-3064.
13. Sartor RB. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 2004;126:1620-1633.
14. Abdel-Daim MM. Pharmacodynamic interaction of Spirulina platensis with erythromycin in Egyptian Baladi bucks (Capra hircus). Small Ruminant Res 2014;120:234-241.
15. Ibrahim A, Abdel Daim M. Modulating effects of Spirulina platensis against tilmicosin-induced cardiotoxicity in mice. Cell Journal (Yakhteh) 2015;17. (in press).
16. Madkour FF, Abdel-Daim MM. Hepatoprotective and antioxidant activity of Dunaliella salina in paracetamol-induced acute toxicity in rats. Indian J Pharm Sci 2013;75:642-648.
17. Dillon JC, Phuc AP, Dubacq JP. Nutritional value of the alga Spirulina. World Rev Nutr Diet 1995;77:32-46.
18. Reddy MC, Subhashini J, Mahipal SV, et al. C-Phycocyanin, a selective cyclooxygenase-2 inhibitor, induces apoptosis in lipopolysaccharide- stimulated RAW 264.7 macrophages. Biochem Biophys Res Commun 2003;304:385-392.
19. Chidambara Murthy KN, Vanitha A, Rajesha J, et al. In vivo antioxidant activity of carotenoids from Dunaliella salina - a green microalga. Life Sci 2005;76:1381-1390.
20. van Poppel G, Goldbohm RA. Epidemiologic evidence for beta-carotene and cancer prevention. Am J Clin Nutr 1995;62:1393S-1402S.
21. Hughes DA, Wright AJ, Finglas PM, et al. The effect of beta-carotene supplementation on the immune function of blood monocytes from healthy male nonsmokers. J Lab Clin Med 1997;129:309-317.
22. Acevedo P, Bertram JS. Liarozole potentiates the cancer chemopreventive activity of and the up-regulation of gap junctional communication and connexin43 expression by retinoic acid and beta-carotene in 10T1/2 cells. Carcinogenesis 1995;16:2215-2222.
23. El-Abhar HS, Hammad LN, Gawad HS. Modulating effect of ginger extract on rats with ulcerative colitis. J Ethnopharmacol 2008;118:367-372.
24. Abdel-Daim MM, Abuzead SM, Halawa SM. Protective role of Spirulina platensis against acute deltamethrin-induced toxicity in rats. PLoS One 2013;8:e72991.
25. Millar AD, Rampton DS, Chander CL, et al. Evaluating the antioxidant potential of new treatments for inflammatory bowel disease using a rat model of colitis. Gut 1996;39:407-415.
26. Mustafa A, El-Medany A, Hagar HH, El-Medany G. Ginkgo biloba attenuates mucosal damage in a rat model of ulcerative colitis. Pharmacol Res 2006;53:324-330.
27. Cao YB, Zhang JD, Diao YY, et al. Effects of Changtai granules, a traditional compound Chinese medicine, on chronic trinitrobenzene sulfonic acid-induced colitis in rats. World J Gastroenterol 2005;11:3539-3543.
28. Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978;86:271-278.
29. Levine RL, Garland D, Oliver CN, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 1990;186:464-478.
30. Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med 1963;61:882-888.
31. Nishikimi M, Appaji N, Yagi K. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 1972;46:849-854.
32. Aebi H. Catalase in vitro. Methods Enzymol 1984;105:121-126.
33. Krawisz JE, Sharon P, Stenson WF. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 1984;87:1344-1350.
34. Reinecker HC, Steffen M, Witthoeft T, et al. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin Exp Immunol 1993;94:174-181.
35. Lantz RC, Chen GJ, Sarihan M, et al. The effect of extracts from ginger rhizome on inflammatory mediator production. Phytomedicine 2007;14:123-128.
36. Banchroft JD, Stevens A, Turner DR. Theory and practice of histological techniques. 4th edn. New York, London, San Francisco, Tokyo: Churchil Livingstone; 1996.
37. Schreiber O, Petersson J, Walden T, et al. iNOS-dependent increase in colonic mucus thickness in DSS-colitic rats. PLoS One 2013;8:e71843.
38. Kotakadi VS, Jin Y, Hofseth AB, et al. Ginkgo biloba extract EGb 761 has anti-inflammatory properties and ameliorates colitis in mice by driving effector T cell apoptosis. Carcinogenesis 2008;29:1799-1806.
39. Nagib MM, Tadros MG, ElSayed MI, Khalifa AE. Anti-inflammatory and anti-oxidant activities of olmesartan medoxomil ameliorate experimental colitis in rats. Toxicol Appl Pharmacol 2013;271:106-113.
40. Celinski K, Dworzanski T, Korolczuk A, et al. Effects of peroxisome proliferator-activated receptors-gamma ligands on dextran sodium sulphate-induced colitis in rats. J Physiol Pharmacol 2011;62:347-356.
41. Kruidenier L, Verspaget HW. Review article: oxidative stress as a pathogenic factor in inflammatory bowel disease - radicals or ridiculous? Aliment Pharmacol Ther 2002;16:1997-2015.
42. Buffinton GD, Doe WF. Depleted mucosal antioxidant defences in inflammatory bowel disease. Free Radic Biol Med 1995;19:911-918.
43. Boughton-Smith NK, Wallace JL, Morris GP, Whittle BJ. The effect of anti-inflammatory drugs on eicosanoid formation in a chronic model of inflammatory bowel disease in the rat. Br J Pharmacol 1988;94:65-72.
44. Laroui H, Ingersoll SA, Liu HC, et al. Dextran sodium sulfate (DSS) induces colitis in mice by forming nano-lipocomplexes with medium-chain-length fatty acids in the colon. PLoS One 2012;7:e32084.
45. Akgun E, Caliskan C, Celik HA, et al. Effects of N-acetylcysteine treatment on oxidative stress in acetic acid-induced experimental colitis in rats. J Int Medical Res 2005;33:196-206.
46. Kruidenier L, Kuiper I, Lamers CB, Verspaget HW. Intestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants. J Pathol 2003;201:28-36.
47. Sartor RB. Cytokines in intestinal inflammation: pathophysiological and clinical considerations. Gastroenterology 1994;106:533-539.
48. Stallmach A, Schuppan D, Riese HH, et al. Increased collagen type III synthesis by fibroblasts isolated from strictures of patients with Crohn's disease. Gastroenterology 1992;102:1920-1929.
49. Siegmund B. Interleukin-1beta converting enzyme (caspase-1) in intestinal inflammation. Biochem Pharmacol 2002;64:1-8.
50. Otani T, Yamaguchi K, Scherl E, et al. Levels of NAD(+)-dependent 15-hydroxyprostaglandin dehydrogenase are reduced in inflammatory bowel disease: evidence for involvement of TNFalpha. Am J Physiol Gastrointest Liver Physiol 2006;290:G361-G368.
51. Kobayashi O, Miwa H, Watanabe S, et al. Cyclooxygenase-2 downregulates inducible nitric oxide synthase in rat intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2001;281:G688-G696.
52. Salvemini D, Settle SL, Masferrer JL, et al. Regulation of prostaglandin production by nitric oxide; an in vivo analysis. Br J Pharmacol 1995;114:1171-1178.
53. MacMicking J, Xie QW, Nathan C. Nitric oxide and macrophage function. Ann Rev Immunol 1997;15:323-350.
54. Petersson J, Schreiber O, Steege A, et al. eNOS involved in colitis-induced mucosal blood flow increase. Am J Physiol Gastrointest Liver Physiol 2007;293:G1281-G1287.
55. Miller MJ, Thompson JH, Zhang XJ, et al. Role of inducible nitric oxide synthase expression and peroxynitrite formation in guinea pig ileitis. Gastroenterology 1995;109:1475-1483.