Effects of a low protein soybean meal diet with and without Spirulina platensis freshwater microalgae on antioxidant systems in broiler liver and muscle tissue
Main Article Content
Abstract
With increased demand for soybean meal to feed poultry and livestock, feeding diets with lower crude protein can reduce expense and lower nitrogen waste. Thus, the major objective of this study was to determine the effect of feeding a low crude protein (CP) soybean diet, and one in LCP soybean meal was replaced with Sprirullina platensis microalgae protein on antioxidant redox systems in liver and muscle tissue. Ross 708 male broilers were reared in floor pens and provided access to feed and water ad libitum. From day 1 - 14, all birds were provided a standard commercial corn soy-based starter diet. From d 15 - 37, the birds were divided into three groups (5 pens per diet; 12 birds/pen) and provided either: 1) A standard corn/soybean meal diet (21% CP, 3250 kcal/kg) (Control, CON), 2) a 17% negative control with lower crude protein (17%) (LCP) diet, and 3) the LCP diet in which Spirulina platensis meal was used to replace half of the soybean meal (LCP+AL). At the end of the study, 2 birds per pen (10 birds total per treatment) were randomly selected and humanely euthanized, after which liver and breast muscle samples were obtained and flash frozen in liquid nitrogen. The tissues were analyzed for antioxidant mRNA expression, antioxidant enzyme activity, and levels of reduced and oxidized glutathione (GSH and GSSG, respectively). In the liver, mRNA expression of 7 of 8 antioxidant enzymes analyzed were elevated (P<0.05) in the LCP+AL group compared to CON mRNA expression. However, activities of these enzymes were higher in the CON compared to the LCP+AL group. Both mRNA and enzyme activity values were intermediate for compared to the CON and LCP-AL groups. Hepatic concentrations of GSH, GSSG and thiobarbituric reactive substance were lower in the LCP group compared to CON and LCP+AL groups. In breast muscle, tissue mRNA expression of gamma glutamyl cysteine lyase , and superoxide dismutase 2 were lower (P<0.05), while GSH peroxidase 3 , GSH Reductase , thioredoxin, and GSH levels were higher (P< 0.05) in the LCP+AL compared to CON. Both GSH and GSSG levels were elevated in the LCP+AL group. The results of this study appear to paint a picture of increased antioxidant mRNA expression but decreased enzyme activity in the liver of the LCP+AL group compared to CON. Interestingly, reduced GSH levels in the LCP+AL group in breast muscle were twice as high as the CON and LCP groups indicating that the microalgae protein could provide considerable protection against thiolation of proteins and other structures in the cell.
Keywords:
microalgae, antioxidants, broilers, liver, breast muscle
Article Details
How to Cite
LASSITER, Kentu et al.
Effects of a low protein soybean meal diet with and without Spirulina platensis freshwater microalgae on antioxidant systems in broiler liver and muscle tissue.
Medical Research Archives, [S.l.], v. 12, n. 10, oct. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5697>. Date accessed: 15 nov. 2024.
doi: https://doi.org/10.18103/mra.v12i10.5697.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Mullenix, G. J. et al. Spirulina platensis Inclusion Reverses Circulating Pro-inflammatory (chemo) cytokine profiles in broilers fed low-protein diets. Front. Vet. Sci. 11, 1243 (2021).
2. Abdel-Moneim, A., Shehata, A. M., Mohamed, N. G., Elbaz, A. M. & Abrahim; NS. Synergistic effect of Spirulina platensis and selenium nanoparticles on growth performance, serum metabolites, immune responses, and antioxidant capacity of heat-stressed broiler chickens. Biol Trace Elem Res 200, 768–779 (2022).
3. Holman B.W. & Malau-Aduli A.E. Spirulina as a livestock supplement and animal feed. J. Anim. Physiol. Anim. Nutr. (Berl). . Anim. Physiol. Anim. Nutr. (Berl). 97, 615–623 (2013).
4. Taelman, S., De Meeste, S., Van Dijk, W., da Silva, V. & Dewulf, J. Environmental sustainability analysis of a protein-rich livestock feed ingredient in The Netherlands: Microalgae production versus soybean import. Resource Conserv Recycl 101, 61–72 (2015).
5. Becker EW. Microalgae: Biotechnology and Microbiology. (Cambridge University Press, 1994).
6. Kulshreshtha, A. et al. Spirulina in health care management. Curr. Pharm. Biotechnol. 9, 400–405 (2008).
7. Mariey, B., Samak, H. & Ibrahem, M. A. Effect of using Spirulina platensis algae as a feed additive for poultry diets: 1-Productive and reproductive performances of local laying hens. Egypt. Poult. Sci. J. 32, (2012).
8. Eriksen, N. T. Production of phycocyanin - a pigment with applications in biology, biotechnology, foods and medicine. Appl. Microbiol. Biotechnol. 80, 1–14 (2008).
9. Christaki, E., Bonos, E., Giannenas, I. & Florou-Paneri. Functional properties of carotenoids originating from algae. J. Sci. Food Agric. 93, 5–11 (2013).
10. Fathi, M. A., Namra, M. M., Ragab. M.S. & Aly, M. M. Effect of dietary supplementation of algae meal (Spirulina platensis) as growth promotor on performance on performance of broiler chickens. Egypt. Poult. Sci. 38:375–389. 38, 375–389 (2018).
11. Park, J. H., Lee, S. I. & Kim, I. H. Effect of dietary spirulina (arthrospira) platensis on the growth performance, antioxidant enzyme activity, nutrient digestibility, cecal microflora, excreta noxious gas emission, and breast meat quality of broiler chickens. Poult. Sci. 97, 2451–2459 (97AD).
12. Bonos, E. et al. Spirulina as a functional ingredient in broiler chicken diets. S. Afr. J. Anim. Sci. 46, 94–102 (2016).
13. Elbaz, A. M., Ahmed, A. M., Abdel-Maqsoud, A., Badran, A. M. & Abdel-Moneim, A. M. E. Potential ameliorative role of Spirulina platensis in powdered or extract forms against cyclic heat stress in broiler chickens. Environ. Sci. and Pollution Res. 29(30) 97, 45578–45588 (2022).
14. Mujahid A, Akiba Y & Toyomizu M. Olive oil-supplemented diet alleviates heat stress-induced mitochondrial ROS production in chicken skeletal muscle. Am. J. Phys. Regul. Integr. Comp. Physiol. 297, R690–R698 (2009).
15. Mujahid, A. et al. Mitochondrial oxidative damage in chicken skeletal muscle induced by acute heat stress. J. of Poultry Sci. 44, (2007).
16. Mirzaie S, Zirak-Khattab F, Hosseini SA & Donyaei-Darian H. Effects of dietary Spirulina on antioxidant status, lipid profile, immune response and performance characteristics of broiler chickens reared under high ambient temperature. Asian-Australas J. Anim. Sci. 31, 556–563 (2018).
17. Moustafa ES et al. Blue-green algae (Spirulina platensis) alleviates the negative Impact of heat stress on broiler production performance and redox status. Animals 11, 1243 (2021).
18. Yu, B. P. Cellular defenses against damage from reactive oxygen species. Physiol. Rev. 74, 139–162 (1994).
19. Anderson ME, Bridges RJ & Meister A. Direct evidence for interorgan transport of glutathione and that the non-filtration renal mechanism for glutathione utilization involves γ-glutamyl transpeptidase. Biochem. Biophys. Res. Comm 96, 848–853 (1980).
20. Wang, S. et al. Hepatic export of glutathione and uptake of constituent amino acids, glutamate and cysteine, in broilers in vivo. Poult Sci 77, (1998).
21. Amer, E. S. & Holmgren, A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 81, 6102–6109 (2000).
22. Bottje, W. et al. Association of mitochondrial function with feed efficiency within a single genetic line of male broilers. Poult Sci 81, (2002).
23. Tinsley, N. et al. Investigation of mitochondrial protein expression and oxidation in heart muscle in low and high feed efficient male broilers in a single genetic line. Poult Sci 89, (2010).
24. Iqbal, M. et al. Low feed efficient broilers within a single genetic line exhibit higher oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity. Poult Sci 83, (2004).
25. Iqbal, M. et al. Compromised liver mitochondrial function and complex activity in low feed efficient broilers are associated with higher oxidative stress and differential protein expression. Poult Sci 84, (2005).
26. Ojano-Dirain, C., Iqbal, M., Wing, T., Cooper, M. & Bottje, W. Glutathione and respiratory chain complex activity in duodenal mitochondria of broilers with low and high feed efficiency. Poult Sci 84, (2005).
27. Lassiter, K. et al. Differential expression of mitochondrial and extramitochondrial proteins in lymphocytes of male broilers with low and high feed efficiency. Poult Sci 85, (2006).
28. Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc 3, 1101–1108 (2008).
29. McGill, M. R. & Jaeschke, M. A direct comparison of methods used to measure oxidized glutathione in biological samples: 2-vinylpyridine and N-ethylmaleimide. Toxicol. Mech. Methods 25, 589–595 (2015).
30. Tietze, F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27, 502–522 (1969).
31. Paglia, D. E. & Valentine, W. N. A direct comparison of methods used to measure oxidized glutathione in biological samples: 2-vinylpyridine and N-ethylmaleimide. J. Lab Clin. Med. 70, 158–169 (1967).
32. Crafton, S. W. Assessment of novel protein ingredient arthrospira platensis (microalgae) and soybean genotype amino acid and oil selection Improvements on broiler performance. (Division of Agriculture, University of Arkansas, 2022).
33. Kumar, A., et al. Antioxidants and phytonutrient activities of Spirulina platensis. Energy Nexus 6, 1–9 (2022).
34. Riss J 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. 55, 7962–7967 (2007).
35. Bermejo-Bescós P, Piñero-Estrada E & Villar del Fresno AM. Neuroprotection by Spirulina platensis protean extract and phycocyanin against iron-induced toxicity in SH-SY5Y neuroblastoma cells. Toxicol. In Vitro 22, 1496–1592 (2008).
36. Karadeniz A, Yildirim A, Simsek N, Kalkan Y & Celebi F. Spirulina platensis protects against gentamicin-induced nephrotoxicity in rats. Phytother. Res. 22, 1506–1510 (2015).
37. Koníčková R et al. Anti-cancer effects of blue-green alga Spirulina platensis, a natural source of bilirubin-like tetrapyrrolic compounds. Ann. Hepatol. 13, 273–283 (2014).
38. Abdelkhalek NK, Ghazy EW & Abdel-Daim MM. Pharmacodynamic interaction of Spirulina platensis and deltamethrin in freshwater fish Nile tilapia, Oreochromis niloticus: impact on lipid peroxidation and oxidative stress. Pollut. Res. Int. 22, 3023–3031 (2015).
39. Galip N, Seyidoglu N, Serdar Z & Savas N. . The effect of Saccharomyces Cerevisiae and Spirulina Platensis on glutathione and leucocytes count in rabbits. J. Res. Vet. Med 38, 71–76 (2019).
40. Wu Q et al. The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: an overview. Arch. Toxicol. 90, 1817–1840 (2016).
41. Deng R & Chow TJ. Hypolipidemic, antioxidant, and antiinflammatory activities of microalgae Spirulina. Cardiovasc. Ther. 28, e33–e45 (2910).
42. Xia D et al. Protective effects of C-phycocyanin on alcohol-induced acute liver injury in mice. J. Oceanol. Limnol. 34, 399–404 (2016).
43. Schafer FQ et al. Comparing beta-carotene, vitamin E and nitric oxide as membrane antioxidants. Biol. Chem 383, 671–681 (2002).
44. Bai SK et al. Beta-Carotene inhibits inflammatory gene expression in lipopolysaccharide-stimulated macrophages by suppressing redox-based NF-kappaB activation. Exp. Mol. Med 37, 323–334 (2009).
45. Katsuura S, Imamura T, Bando N & Yamanishi, R. Beta-Carotene and beta-cryptoxanthin but not lutein evoke redox and immune changes in RAW264 murine macrophages. Mol. Nutr. Food. Res. 53, 1396–1405 (2009).
46. Lushchak, V. Glutathione homeostasis and functions: Potential targets for medical interventions. J. Amino Acids 2012/e736837., (2012).
47. Maher, P. The effects of stress and aging on glutathione metabolism. Aging Res. Rev. 288–314 (2005).
48. Vivancos Diaz P, Wolff T, Markovic J, Pallardo FV & Foyer CH. A nuclear glutathione cycle within the cell cycle. Biochem. J. 275, 169–178 (2010).
49. Margis R, Dunand C, Teixeira FK & Margis-Pinheiro M. Glutathione peroxidase family-an evolutionary overview. FEBS J. 275, 3959–3970 (2008).
50. Brown KM et al. Effects of organic and inorganic selenium supplementation on selenoenzyme activity in blood lymphocytes, granulocytes, platelets and erythrocytes. Clin. Scl. 98, 593–599 (2000).
51. Herbette S, Roeckel-Drevet P & Drevet JR. Seleno-independent glutathione peroxidases. FEBS J. 1830, 2163–2180 (2007).
52. Deponte, M. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim. Biophys. Acta 1830, 3217–3266 (2013).
53. Aon MA et al. Glutathione/thioredoxin systems modulate mitochondrial H2O2 emission: an experimental-computational study. J. Gen. Physiol. 139, 479–491 (2012).
54. Halliwell, B. Free radicals and antioxidants: A personal view. Nutr. Rev 52, 253–265 (1994).
55. Surai PF, Kochish II, Fisinin VI & Kidd MT. Antioxidant defence systems and oxidative stress in poultry biology: An update. Antioxidants (Basel) 8, 235 (2019).
56. Jackson H, Braun CL & Ernst H. The chemistry of novel xanthophyll carotenoids. Am. J. Cardiol. 101, 95–100 (2008).
57. Faulk, R. M. & Southon, S. Challenges to understanding and measuring carotenoid bioavailability. Biochim. Biophys. Acta 1740, 95–100 (2005).
58. Itoh K, Mimura J & Yamamoto M. Discovery of the negative regulator of Nrf2, Keap1: An historical overview. Antioxid. Redox Signal 13, 1665–1678 (20109).
59. Bellezza I, Giambanco I, Minelli A, 0 & Donato R. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim. Biophys. Acta 1865, 721–733 (2018).
60. Stefanson, A. L. & Bakovic, M. Dietary regulation of Keap1/Nrf2/ARE pathway: focus on plant-derived compounds and trace minerals. Nutirents 6, 3777–3801 (2014).
61. Ben-Dor, A. et al. Carotenoids activate the antioxidant response element transcription system. Mol. Cancer Ther. 2005, 177–186 (2005).
62. Linnewiel K et al. Structure activity relationship of carotenoid derivatives in activation of the electrophile-antioxidant response element transcription system. Free Rad. Biol. Med. 47, 659–667 (2009).
63. Desai, K. & Sivakami, S. Purification and biochemical characterization of a superoxide dismutase from the soluble fraction of the cyanobacteium Spirulina platensis. World J. Micro. Biotech. 23, 1661–1666 (2007).
64. El Baky, H. H., El-Baz, F. K. & Baroty, G. E. Production of phenolic compounds from Spirulina maxima microalgae and its protective effects. Afr. J. Biotech. 8, 7059–7067 (2009).
65. Kong, B.-W. et al. RNA sequencing for global gene expression associated with muscle growth in a single male modern broiler line compared to a foundational Barred Plymouth Rock chicken line. BMC Genomics 18, (2017).
66. Khatri B et al. MicroRNA profiling associated with muscle growth in modern broilers compared to an unselected chicken breed. BMC Genomics 19, 683 (2018).
67. Palozza, P. Prooxidant actions of carotenoids in biologic systems. Nutr. Rev. 56, 257–265 (1998).
68. Palozza P et al. Beta-carotene at high concentrations induces apoptosis by enhancing oxy-radical production in human adenocarcinoma cells. Free Rad. Biol. Med. 30, 1000–1007 (2001).
69. Paolini M et al. Induction of cytochrome P450 enzymes and over-generation of oxygen radicals in beta-carotene supplemented rats. Carcinogenesis 22, 1483–1495 (2001).
70. Amengual J et al. A mitochondrial enzyme degrades carotenoids and protects against oxidative stress. FASEB J. 25, 948–959 (2011).
71. Johnson JD & Hill GE. Is carotenoid ornamentation linked to the inner mitochondria membrane potential? A hypothesis for the maintenance of signal honesty. Biochimie 21, 436–444 (2013).
72. Mayne, S. T. & Parker, R. S. Subcellular distribution of dietary beta-carotene in chick liver. Lipids 21, 164–169 (1986).
73. Barja, G. Mitochondrial free radical production and aging in mammals and birds. Ann. N.Y. Acad. Sci. 854, 224–238 (1998).
74. Karadas F, Erdogan S, Kor D, Oto G & Uluman M. The effects of different types of antioxidants (Se, Vitamin E and Carotenoids) in broiler diets on the growth performance, skin pigmentation and liver and plasma antioxidant concentrations. . Rev. Bras. Cienc. Avic. 18, 101–115 (2016).
75. Moreno J. A. et al. The distribution of carotenoids in hens fed on biofortified maize is influenced by feed composition, absorption, resource allocation and storage. Sci. Rep. 6, 35346 (2016).
2. Abdel-Moneim, A., Shehata, A. M., Mohamed, N. G., Elbaz, A. M. & Abrahim; NS. Synergistic effect of Spirulina platensis and selenium nanoparticles on growth performance, serum metabolites, immune responses, and antioxidant capacity of heat-stressed broiler chickens. Biol Trace Elem Res 200, 768–779 (2022).
3. Holman B.W. & Malau-Aduli A.E. Spirulina as a livestock supplement and animal feed. J. Anim. Physiol. Anim. Nutr. (Berl). . Anim. Physiol. Anim. Nutr. (Berl). 97, 615–623 (2013).
4. Taelman, S., De Meeste, S., Van Dijk, W., da Silva, V. & Dewulf, J. Environmental sustainability analysis of a protein-rich livestock feed ingredient in The Netherlands: Microalgae production versus soybean import. Resource Conserv Recycl 101, 61–72 (2015).
5. Becker EW. Microalgae: Biotechnology and Microbiology. (Cambridge University Press, 1994).
6. Kulshreshtha, A. et al. Spirulina in health care management. Curr. Pharm. Biotechnol. 9, 400–405 (2008).
7. Mariey, B., Samak, H. & Ibrahem, M. A. Effect of using Spirulina platensis algae as a feed additive for poultry diets: 1-Productive and reproductive performances of local laying hens. Egypt. Poult. Sci. J. 32, (2012).
8. Eriksen, N. T. Production of phycocyanin - a pigment with applications in biology, biotechnology, foods and medicine. Appl. Microbiol. Biotechnol. 80, 1–14 (2008).
9. Christaki, E., Bonos, E., Giannenas, I. & Florou-Paneri. Functional properties of carotenoids originating from algae. J. Sci. Food Agric. 93, 5–11 (2013).
10. Fathi, M. A., Namra, M. M., Ragab. M.S. & Aly, M. M. Effect of dietary supplementation of algae meal (Spirulina platensis) as growth promotor on performance on performance of broiler chickens. Egypt. Poult. Sci. 38:375–389. 38, 375–389 (2018).
11. Park, J. H., Lee, S. I. & Kim, I. H. Effect of dietary spirulina (arthrospira) platensis on the growth performance, antioxidant enzyme activity, nutrient digestibility, cecal microflora, excreta noxious gas emission, and breast meat quality of broiler chickens. Poult. Sci. 97, 2451–2459 (97AD).
12. Bonos, E. et al. Spirulina as a functional ingredient in broiler chicken diets. S. Afr. J. Anim. Sci. 46, 94–102 (2016).
13. Elbaz, A. M., Ahmed, A. M., Abdel-Maqsoud, A., Badran, A. M. & Abdel-Moneim, A. M. E. Potential ameliorative role of Spirulina platensis in powdered or extract forms against cyclic heat stress in broiler chickens. Environ. Sci. and Pollution Res. 29(30) 97, 45578–45588 (2022).
14. Mujahid A, Akiba Y & Toyomizu M. Olive oil-supplemented diet alleviates heat stress-induced mitochondrial ROS production in chicken skeletal muscle. Am. J. Phys. Regul. Integr. Comp. Physiol. 297, R690–R698 (2009).
15. Mujahid, A. et al. Mitochondrial oxidative damage in chicken skeletal muscle induced by acute heat stress. J. of Poultry Sci. 44, (2007).
16. Mirzaie S, Zirak-Khattab F, Hosseini SA & Donyaei-Darian H. Effects of dietary Spirulina on antioxidant status, lipid profile, immune response and performance characteristics of broiler chickens reared under high ambient temperature. Asian-Australas J. Anim. Sci. 31, 556–563 (2018).
17. Moustafa ES et al. Blue-green algae (Spirulina platensis) alleviates the negative Impact of heat stress on broiler production performance and redox status. Animals 11, 1243 (2021).
18. Yu, B. P. Cellular defenses against damage from reactive oxygen species. Physiol. Rev. 74, 139–162 (1994).
19. Anderson ME, Bridges RJ & Meister A. Direct evidence for interorgan transport of glutathione and that the non-filtration renal mechanism for glutathione utilization involves γ-glutamyl transpeptidase. Biochem. Biophys. Res. Comm 96, 848–853 (1980).
20. Wang, S. et al. Hepatic export of glutathione and uptake of constituent amino acids, glutamate and cysteine, in broilers in vivo. Poult Sci 77, (1998).
21. Amer, E. S. & Holmgren, A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 81, 6102–6109 (2000).
22. Bottje, W. et al. Association of mitochondrial function with feed efficiency within a single genetic line of male broilers. Poult Sci 81, (2002).
23. Tinsley, N. et al. Investigation of mitochondrial protein expression and oxidation in heart muscle in low and high feed efficient male broilers in a single genetic line. Poult Sci 89, (2010).
24. Iqbal, M. et al. Low feed efficient broilers within a single genetic line exhibit higher oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity. Poult Sci 83, (2004).
25. Iqbal, M. et al. Compromised liver mitochondrial function and complex activity in low feed efficient broilers are associated with higher oxidative stress and differential protein expression. Poult Sci 84, (2005).
26. Ojano-Dirain, C., Iqbal, M., Wing, T., Cooper, M. & Bottje, W. Glutathione and respiratory chain complex activity in duodenal mitochondria of broilers with low and high feed efficiency. Poult Sci 84, (2005).
27. Lassiter, K. et al. Differential expression of mitochondrial and extramitochondrial proteins in lymphocytes of male broilers with low and high feed efficiency. Poult Sci 85, (2006).
28. Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc 3, 1101–1108 (2008).
29. McGill, M. R. & Jaeschke, M. A direct comparison of methods used to measure oxidized glutathione in biological samples: 2-vinylpyridine and N-ethylmaleimide. Toxicol. Mech. Methods 25, 589–595 (2015).
30. Tietze, F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27, 502–522 (1969).
31. Paglia, D. E. & Valentine, W. N. A direct comparison of methods used to measure oxidized glutathione in biological samples: 2-vinylpyridine and N-ethylmaleimide. J. Lab Clin. Med. 70, 158–169 (1967).
32. Crafton, S. W. Assessment of novel protein ingredient arthrospira platensis (microalgae) and soybean genotype amino acid and oil selection Improvements on broiler performance. (Division of Agriculture, University of Arkansas, 2022).
33. Kumar, A., et al. Antioxidants and phytonutrient activities of Spirulina platensis. Energy Nexus 6, 1–9 (2022).
34. Riss J 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. 55, 7962–7967 (2007).
35. Bermejo-Bescós P, Piñero-Estrada E & Villar del Fresno AM. Neuroprotection by Spirulina platensis protean extract and phycocyanin against iron-induced toxicity in SH-SY5Y neuroblastoma cells. Toxicol. In Vitro 22, 1496–1592 (2008).
36. Karadeniz A, Yildirim A, Simsek N, Kalkan Y & Celebi F. Spirulina platensis protects against gentamicin-induced nephrotoxicity in rats. Phytother. Res. 22, 1506–1510 (2015).
37. Koníčková R et al. Anti-cancer effects of blue-green alga Spirulina platensis, a natural source of bilirubin-like tetrapyrrolic compounds. Ann. Hepatol. 13, 273–283 (2014).
38. Abdelkhalek NK, Ghazy EW & Abdel-Daim MM. Pharmacodynamic interaction of Spirulina platensis and deltamethrin in freshwater fish Nile tilapia, Oreochromis niloticus: impact on lipid peroxidation and oxidative stress. Pollut. Res. Int. 22, 3023–3031 (2015).
39. Galip N, Seyidoglu N, Serdar Z & Savas N. . The effect of Saccharomyces Cerevisiae and Spirulina Platensis on glutathione and leucocytes count in rabbits. J. Res. Vet. Med 38, 71–76 (2019).
40. Wu Q et al. The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: an overview. Arch. Toxicol. 90, 1817–1840 (2016).
41. Deng R & Chow TJ. Hypolipidemic, antioxidant, and antiinflammatory activities of microalgae Spirulina. Cardiovasc. Ther. 28, e33–e45 (2910).
42. Xia D et al. Protective effects of C-phycocyanin on alcohol-induced acute liver injury in mice. J. Oceanol. Limnol. 34, 399–404 (2016).
43. Schafer FQ et al. Comparing beta-carotene, vitamin E and nitric oxide as membrane antioxidants. Biol. Chem 383, 671–681 (2002).
44. Bai SK et al. Beta-Carotene inhibits inflammatory gene expression in lipopolysaccharide-stimulated macrophages by suppressing redox-based NF-kappaB activation. Exp. Mol. Med 37, 323–334 (2009).
45. Katsuura S, Imamura T, Bando N & Yamanishi, R. Beta-Carotene and beta-cryptoxanthin but not lutein evoke redox and immune changes in RAW264 murine macrophages. Mol. Nutr. Food. Res. 53, 1396–1405 (2009).
46. Lushchak, V. Glutathione homeostasis and functions: Potential targets for medical interventions. J. Amino Acids 2012/e736837., (2012).
47. Maher, P. The effects of stress and aging on glutathione metabolism. Aging Res. Rev. 288–314 (2005).
48. Vivancos Diaz P, Wolff T, Markovic J, Pallardo FV & Foyer CH. A nuclear glutathione cycle within the cell cycle. Biochem. J. 275, 169–178 (2010).
49. Margis R, Dunand C, Teixeira FK & Margis-Pinheiro M. Glutathione peroxidase family-an evolutionary overview. FEBS J. 275, 3959–3970 (2008).
50. Brown KM et al. Effects of organic and inorganic selenium supplementation on selenoenzyme activity in blood lymphocytes, granulocytes, platelets and erythrocytes. Clin. Scl. 98, 593–599 (2000).
51. Herbette S, Roeckel-Drevet P & Drevet JR. Seleno-independent glutathione peroxidases. FEBS J. 1830, 2163–2180 (2007).
52. Deponte, M. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim. Biophys. Acta 1830, 3217–3266 (2013).
53. Aon MA et al. Glutathione/thioredoxin systems modulate mitochondrial H2O2 emission: an experimental-computational study. J. Gen. Physiol. 139, 479–491 (2012).
54. Halliwell, B. Free radicals and antioxidants: A personal view. Nutr. Rev 52, 253–265 (1994).
55. Surai PF, Kochish II, Fisinin VI & Kidd MT. Antioxidant defence systems and oxidative stress in poultry biology: An update. Antioxidants (Basel) 8, 235 (2019).
56. Jackson H, Braun CL & Ernst H. The chemistry of novel xanthophyll carotenoids. Am. J. Cardiol. 101, 95–100 (2008).
57. Faulk, R. M. & Southon, S. Challenges to understanding and measuring carotenoid bioavailability. Biochim. Biophys. Acta 1740, 95–100 (2005).
58. Itoh K, Mimura J & Yamamoto M. Discovery of the negative regulator of Nrf2, Keap1: An historical overview. Antioxid. Redox Signal 13, 1665–1678 (20109).
59. Bellezza I, Giambanco I, Minelli A, 0 & Donato R. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim. Biophys. Acta 1865, 721–733 (2018).
60. Stefanson, A. L. & Bakovic, M. Dietary regulation of Keap1/Nrf2/ARE pathway: focus on plant-derived compounds and trace minerals. Nutirents 6, 3777–3801 (2014).
61. Ben-Dor, A. et al. Carotenoids activate the antioxidant response element transcription system. Mol. Cancer Ther. 2005, 177–186 (2005).
62. Linnewiel K et al. Structure activity relationship of carotenoid derivatives in activation of the electrophile-antioxidant response element transcription system. Free Rad. Biol. Med. 47, 659–667 (2009).
63. Desai, K. & Sivakami, S. Purification and biochemical characterization of a superoxide dismutase from the soluble fraction of the cyanobacteium Spirulina platensis. World J. Micro. Biotech. 23, 1661–1666 (2007).
64. El Baky, H. H., El-Baz, F. K. & Baroty, G. E. Production of phenolic compounds from Spirulina maxima microalgae and its protective effects. Afr. J. Biotech. 8, 7059–7067 (2009).
65. Kong, B.-W. et al. RNA sequencing for global gene expression associated with muscle growth in a single male modern broiler line compared to a foundational Barred Plymouth Rock chicken line. BMC Genomics 18, (2017).
66. Khatri B et al. MicroRNA profiling associated with muscle growth in modern broilers compared to an unselected chicken breed. BMC Genomics 19, 683 (2018).
67. Palozza, P. Prooxidant actions of carotenoids in biologic systems. Nutr. Rev. 56, 257–265 (1998).
68. Palozza P et al. Beta-carotene at high concentrations induces apoptosis by enhancing oxy-radical production in human adenocarcinoma cells. Free Rad. Biol. Med. 30, 1000–1007 (2001).
69. Paolini M et al. Induction of cytochrome P450 enzymes and over-generation of oxygen radicals in beta-carotene supplemented rats. Carcinogenesis 22, 1483–1495 (2001).
70. Amengual J et al. A mitochondrial enzyme degrades carotenoids and protects against oxidative stress. FASEB J. 25, 948–959 (2011).
71. Johnson JD & Hill GE. Is carotenoid ornamentation linked to the inner mitochondria membrane potential? A hypothesis for the maintenance of signal honesty. Biochimie 21, 436–444 (2013).
72. Mayne, S. T. & Parker, R. S. Subcellular distribution of dietary beta-carotene in chick liver. Lipids 21, 164–169 (1986).
73. Barja, G. Mitochondrial free radical production and aging in mammals and birds. Ann. N.Y. Acad. Sci. 854, 224–238 (1998).
74. Karadas F, Erdogan S, Kor D, Oto G & Uluman M. The effects of different types of antioxidants (Se, Vitamin E and Carotenoids) in broiler diets on the growth performance, skin pigmentation and liver and plasma antioxidant concentrations. . Rev. Bras. Cienc. Avic. 18, 101–115 (2016).
75. Moreno J. A. et al. The distribution of carotenoids in hens fed on biofortified maize is influenced by feed composition, absorption, resource allocation and storage. Sci. Rep. 6, 35346 (2016).