Clinical potential of Spirulina as a source of phycocyanobilin

Journal of Medicinal Food

Volumn 10, Issue 4, 2007, Pages 566-570

  McCarty, Mark F ^a  

^a NutriGuard Research   (United States)

Author keywords

Antioxidant; Bilirubin; Biliverdin; Heme oxygenase; Inflammation; NADPH oxidase; Phycocyanin; Phycocyanobilin; Spirulina; Zeaxanthin

Indexed keywords

BILIRUBIN; ENZYME INHIBITOR; PHYCOCYANIN; PHYCOCYANOBILIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; DIETARY INTAKE; ENZYME ACTIVATION; ENZYME ACTIVITY; FRUIT; FRUIT JUICE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOYBEAN MILK; SPIRULINA;

ANTI-INFLAMMATORY AGENTS; DIET; ENZYME INHIBITORS; HUMANS; NADPH OXIDASE; PHYCOBILINS; PHYCOCYANIN; SPIRULINA;

CHLOROPHYTA; CYANOBACTERIA; MAMMALIA; PROTEA; RODENTIA; SPIRULINA;

EID: 37549037040     PISSN: 1096620X     EISSN: None     Source Type: Journal    
DOI: 10.1089/jmf.2007.621     Document Type: Review

References (66)

1. McCarty MF: "Iatrogenic Gilbert syndrome" - a strategy for reducing vascular and cancer risk by increasing plasma unconjugated bilirubin. Med Hypotheses 2007 Sep 5; [Epub ahead of print].
2. Nakagami H, Jensen KS, Liao JK: A novel pleiotropic effect of statins: prevention of cardiac hypertrophy by cholesterol-independent mechanisms. Ann Med 2003;35:398-403.
3. Touyz RM, Tabet F, Schiffrin EL: Redox-dependent signalling by angiotensin II and vascular remodelling in hypertension. Clin Exp Pharmacol Physiol 2003;30:860-866.
4. Lanone S, Bloc S, Foresti R, et al.: Bilirubin decreases nos2 expression via inhibition of NAD(P)H oxidase: implications for protection against endotoxic shock in rats. FASEB J 2005;19:1890-1892.
5. Matsumoto H, Ishikawa K, Itabe H, Maruyama Y: Carbon monoxide and bilirubin from heme oxygenase-1 suppresses reactive oxygen species generation and plasminogen activator inhibitor-1 induction. Mol Cell Biochem 2006;291:21-28.
6. Jiang F, Roberts SJ, Datla S, Dusting GJ: NO modulates NADPH oxidase function via heme oxygenase-1 in human endothelial cells. Hypertension 2006;48:950-957.
7. Cho HY, Reddy SP, Kleeberger SR: Nrf2 defends the lung from oxidative stress. Antioxid Redox Signal 2006;8:76-87.
8. Bach FH: Heme oxygenase-1 as a protective gene. Wien Klin Wochenschr 2002;114(Suppl 4):1-3.
9. Vitek L, Jirsa M, Brodanova M, et al.: Gilbert syndrome and ischemic heart disease: a protective effect of elevated bilirubin levels. Atherosclerosis 2002;160:449-456.
10. Vitek L, Novotny L, Sperl M, Holaj R, Spacil J: The inverse association of elevated serum bilirubin levels with subclinical carotid atherosclerosis. Cerebrovasc Dis 2006;21:408-414.
11. Zucker SD, Horn PS, Sherman KE: Serum bilirubin levels in the U.S. population: gender effect and inverse correlation with colorectal cancer. Hepatology 2004;40:827-835.
12. Exner M, Minar E, Wagner O, Schillinger M: The role of heme oxygenase-1 promoter polymorphisms in human disease. Free Radic Biol Med 2004;37:1097-1104.
13. Brown SB, Houghton JD, Vernon DI: Biosynthesis of phycobilins. Formation of the chromophore of phytochrome, phycocyanin and phycoerythrin. J Photochem Photobiol B 1990;5:3-23.
14. Terry MJ, Maines MD, Lagarias JC: Inactivation of phytochrome-and phycobiliprotein-chromophore precursors by rat liver biliverdin reductase. J Biol Chem 1993;268:26099-26106.
15. Romay C, Armesto J, Remirez D, Gonzalez R, Ledon N, Garcia I: Antioxidant and anti-inflammatory properties of C-phycocyanin from blue-green algae. Inflamm Res 1998;47:36-41.
16. Romay C, Delgado R, Remirez D, Gonzalez R, Rojas A: Effects of phycocyanin extract on tumor necrosis factor-alpha and nitrite levels in serum of mice treated with endotoxin. Arzneimittelforschung 2001;51:733-736.
17. Romay C, Gonzalez R, Ledon N, Remirez D, Rimbau V: C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr Protein Pept Sci 2003;4:207-216.
18. Rimbau V, Camins A, Romay C, Gonzalez R, Pallas M: Protective effects of C-phycocyanin against kainic acid-induced neuronal damage in rat hippocampus. Neurosci Lett 1999;276:75-78.
19. Chamorro G, Perez-Albiter M, Serrano-Garcia N, Mares-Samano JJ, Rojas P: Spirulina maxima pretreatment partially protects against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity. Nutr Neurosci 2006;9:207-212.
20. Remirez D, Gonzalez R, Merino N, Rodriguez S, Ancheta O: Inhibitory effects of Spirulina in zymosan-induced arthritis in mice. Mediators Inflamm 2002;11:75-79.
21. Rasool M, Sabina EP, Lavanya B: Anti-inflammatory effect of Spirulina fusiformis on adjuvant-induced arthritis in mice. Biol Pharm Bull 2006;29:2483-2487.
22. Khan M, Shobha JC, Mohan IK, et al.: Protective effect of Spirulina against doxorubicin-induced cardiotoxicity. Phytother Res 2005;19:1030-1037.
23. Mohan IK, Khan M, Shobha JC, et al.: Protection against cisplatin-induced nephrotoxicity by Spirulina in rats. Cancer Chemother Pharmacol 2006;58:802-808.
24. Khan M, Shobha JC, Mohan IK, Rao Naidu MU, Prayag A, Kutala VK: Spirulina attenuates cyclosporine-induced nephrotoxicity in rats. J Appl Toxicol 2006;26:444-451.
25. Nakagami T, Toyomura K, Kinoshita T, Morisawa S: A beneficial role of bile pigments as an endogenous tissue protector: anti-complement effects of biliverdin and conjugated bilirubin. Biochim Biophys Acta 1993;1158:189-193.
26. Nakao A, Otterbein LE, Overhaus M, et al.: Biliverdin protects the functional integrity of a transplanted syngeneic small bowel. Gastroenterology 2004;127:595-606.
27. Yamashita K, McDaid J, Ollinger R, et al.: Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. FASEB J 2004;18:765-767.
28. Mukougawa K, Kanamoto H, Kobayashi T, Yokota A, Kohchi T: Metabolic engineering to produce phytochromes with phytochromobilin, phycocyanobilin, or phycoerythrobilin chromophore in Escherichia coli. FEBS Lett 2006;580:1333-1338.
29. Padyana AK, Bhat VB, Madyastha KM, Rajashankar KR, Ramakumar S: Crystal structure of a light-harvesting protein C-phycocyanin from Spirulina platensis. Biochem Biophys Res Commun 2001;282:893-898.
30. Travis CC: Interspecies extrapolation in risk analysis. Ann Ist Super Sanita 1991;27:581-593.
31. Darveau CA, Suarez RK, Andrews RD, Hochachka PW: Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 2002;417:166-170.
32. Lindstedt L, Schaeffer PJ: Use of allometry in predicting anatomical and physiological parameters of mammals. Lab Anim 2002;36:1-19.
33. 't Hart BA, Bakker NP, Labadie RP, Simons JM: The newly developed neutrophil oxidative burst antagonist apocynin inhibits joint-swelling in rat collagen arthritis. Agents Actions Suppl 1991;32:179-184.
34. van Lent PL, Nabbe KC, Blom AB, et al.: NADPH-oxidase-driven oxygen radical production determines chondrocyte death and partly regulates metalloproteinase-mediated cartilage matrix degradation during interferon-gamma-stimulated immune complex arthritis. Arthritis Res Ther 2005;7:R885-R895.
35. Miesel R, Sanocka D, Kurpisz M, Kroger H: Antiinflammatory effects of NADPH oxidase inhibitors. Inflammation 1995;19:347-362.
36. Hougee S, Hartog A, Sanders A, et al.: Oral administration of the NADPH-oxidase inhibitor apocynin partially restores diminished cartilage proteoglycan synthesis and reduces inflammation in mice. Eur J Pharmacol 2006;531:264-269.
37. Gao HM, Liu B, Zhang W, Hong JS: Critical role of microglial NADPH oxidase-derived free radicals in the in vitro MPTP model of Parkinson's disease. FASEB J 2003;17:1954-1956.
38. Wu DC, Teismann P, Tieu K, et al.: NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Proc Natl Acad Sci U S A 2003;100:6145-6150.
39. Deng S, Kruger A, Kleschyov AL, Kalinowski L, Daiber A, Wojnowski L: Gp91phox-containing NAD(P)H oxidase increases superoxide formation by doxorubicin and NADPH. Free Radic Biol Med 2007;42:466-473.
40. Wojnowski L, Kulle B, Schirmer M, et al.: NAD(P)H oxidase and multidrug resistance protein genetic polymorphisms are associated with doxorubicin-induced cardiotoxicity. Circulation 2005;112:3754-3762.
41. Kawai Y, Nakao T, Kunimura N, Kohda Y, Gemba M: Relationship of intracellular calcium and oxygen radicals to cisplatin-related renal cell injury. J Pharmacol Sci 2006;100:65-72.
42. Zhong Z, Connor HD, Yin M, Wheeler MD, Mason RP, Thurman RG: Viral delivery of superoxide dismutase gene reduces cyclosporine A-induced nephrotoxicity. Kidney Int 2001;59:1397-1404.
43. Louhelainen M, Merasto S, Finckenberg P, Lapatto R, Cheng ZJ, Mervaala EM: Lipoic acid supplementation prevents cyclosporine-induced hypertension and nephrotoxicity in spontaneously hypertensive rats. J Hypertens 2006;24:947-956.
44. Vetter M, Chen ZJ, Chang GD, Che D, Liu S, Chang CH: Cyclosporin A disrupts bradykinin signaling through superoxide. Hypertension 2003;41:1136-1142.
45. Park YM, Park MY, Suh YL, Park JB: NAD(P)H oxidase inhibitor prevents blood pressure elevation and cardiovascular hypertrophy in aldosterone-infused rats. Biochem Biophys Res Commun 2004;313:812-817.
46. Ghosh M, Wang HD, McNeill JR: Role of oxidative stress and nitric oxide in regulation of spontaneous tone in aorta of DOCA-salt hypertensive rats. Br J Pharmacol 2004;141:562-573.
47. Virdis A, Neves MF, Amiri F, Touyz RM, Schiffrin EL: Role of NAD(P)H oxidase on vascular alterations in angiotensin II-infused mice. J Hypertens 2004;22:535-542.
48. Zimmerman MC, Dunlay RP, Lazartigues E, et al.: Requirement for Rac1-dependent NADPH oxidase in the cardiovascular and dipsogenic actions of angiotensin II in the brain. Circ Res 2004;95:532-539.
49. Zhang Y, Chan MM, Andrews MC, et al.: Apocynin but not allopurinol prevents and reverses adrenocorticotropic hormone-induced hypertension in the rat. Am J Hypertens 2005;18:910-916.
50. Hu L, Zhang Y, Lim PS, et al.: Apocynin but not L-arginine prevents and reverses dexamethasone-induced hypertension in the rat. Am J Hypertens 2006;19:413-418.
51. Lodi F, Cogolludo A, Duarte J, et al.: Increased NADPH oxidase activity mediates spontaneous aortic tone in genetically hypertensive rats. Eur J Pharmacol 2006;544:97-103.
52. Salazar M, Chamorro GA, Salazar S, Steele CE: Effect of Spirulina maxima consumption on reproduction and peri- and postnatal development in rats. Food Chem Toxicol 1996;34:353-359.
53. Chamorro G, Salazar M, Favila L, Bourges H: [Pharmacology and toxicology of Spirulina alga]. Rev Invest Clin 1996;48:389-399.
54. Salazar M, Martinez E, Madrigal E, Ruiz LE, Chamorro GA: Subchronic toxicity study in mice fed Spirulina maxima. J Ethnopharmacol 1998;62:235-241.
55. Ahmed SS, Lott MN, Marcus DM: The macular xanthophylls. Surv Ophthalmol 2005;50:183-193.
56. O'Connell E, Neelam K, Nolan J, Au Eong KG, Beatty S: Macular carotenoids and age-related maculopathy. Ann Acad Med Singapore 2006;35:821-830.
57. Al Batshan HA, Al Mufarrej SI, Al Homaidan AA, Qureshi MA: Enhancement of chicken macrophage phagocytic function and nitrite production by dietary Spirulina platensis. Immunopharmacol Immunotoxicol 2001;23:281-289.
58. Balachandran P, Pugh ND, Ma G, Pasco DS: Toll-like receptor 2-dependent activation of monocytes by Spirulina polysaccharide and its immune enhancing action in mice. Int Immunopharmacol 2006;6:1808-1814.
59. Pugh N, Ross SA, ElSohly HN, ElSohly MA, Pasco DS: Isolation of three high molecular weight polysaccharide preparations with potent immunostimulatory activity from Spirulina platensis, aphanizomenon flos-aquae and Chlorella pyrenoidosa. Planta Med 2001;67:737-742.
60. Kaji T, Okabe M, Shimada S, et al.: Sodium spirulan as a potent inhibitor of arterial smooth muscle cell proliferation in vitro. Life Sci 2004;74:2431-2439.
61. Zurier RB, Rossetti RG, Jacobson EW, et al.: Gamma-linolenic acid treatment of rheumatoid arthritis. A randomized, placebo-controlled trial. Arthritis Rheum 1996;39:1808-1817.
62. Parikh P, Mani U, Iyer U: Role of Spirulina in the control of glycemia and lipidemia in type 2 diabetes mellitus. J Med Food 2001;4:193-199.
63. Roos D, van Bruggen R, Meischl C: Oxidative killing of microbes by neutrophils. Microbes Infect 2003;5:1307-1315.
64. Maemura K, Zheng Q, Wada T, et al.: Reactive oxygen species are essential mediators in antigen presentation by Kupffer cells. Immunol Cell Biol 2005;83:336-343.
65. Ganz T: Oxygen-independent microbicidal mechanisms of phagocytes. Proc Assoc Am Physicians 1999;111:390-395.
66. Riss J, Decorde K, Sutra T, et al.: Phycobiliprotein C-phycocyanin from Spirulina platensis is powerfully responsible for reducing oxidative stress and NADPH oxidase expression induced by an atherogenic diet in hamsters. J Agric Food Chem 2007;55:7962-7967.