The Importance of Maternal Antioxidants for Embryo Development in Birds

Abstract

Egg yolk is source of maternal effect in birds, and antioxidants are transferred to egg yolk from maternal plasma during yolk development. In fact, maternal antioxidant system affects antioxidant level of the egg yolk. Antioxidants, are not synthesized in the organism in birds, are taken into the body through feed. Therefore, maternal's consumed feed and feed components influence the yolk antioxidant level and antioxidant/pro-oxidant balance in the embryo tissue. Maternal antioxidants in yolk are lipidsoluble antioxidants (vit-A, vit-E and carotenoids) and phosvitin which is in the protein granules of yolk. Maternal antioxidants have the main role on embryo development and prevention of oxidative stress. Egg yolk contains high level of fat and polyunsaturated fatty acids (PUFA) to provide energy and normal development of the embryo. Lipid peroxidation (LPO) via this high level of fat and PUFA can lead to damage in embryo tissues. For that reason, embryo tissues need to contain effective antioxidants which protect to embryo against LPO. Natural antioxidant resources in embryo tissues are not sufficient to protect the embryo which is under risk due to the increase LPO and PUFA and use of oxygen in embryo tissues on the day 19th of embryo development. Maternal antioxidants are also important in reducing the harmful effects of free radicals on the efficiency of the immune system,because newly hatched chick's immune system is not functional. In addition, maternal antioxidants protect newly hatched chick against reactive oxygen species (ROS). The purpose of this review was to evaluate the importance of maternal antioxidants in egg yolk during embryo development.

Keywords

• Embryo development, Maternal effect, Yolk antioxidants

Kanatlılarda Maternal Antioksidanların Embriyo Gelişimi İçin Önemi

Öz

Kanatlılarda maternal (dişi ebeveyn) etkilerin kaynağı yumurta sarısı olup, sarı gelişimi boyunca antioksidanlar yumurtlayan dişi ebeveynin plazmasından sarıya aktarılır. Bu nedenle, dişi ebeveynin antioksidan sistemi, yumurta sarısının antioksidan düzeyini etkiler. Kanatlılarda antioksidanlar organizmada sentezlenmediğinden yem aracılığı ile vücuda alınırlar. Nitekim, dişi ebeveynin tükettiği yem ve yem komponentleri, sarı antioksidan düzeyini ve embriyo dokularındaki antioksidan/pro-oksidan dengeyi etkilemektedir. Sarıdaki maternal kökenli antioksidanlar yağda çözünen (vit-A, vit-E ve karotenoidler) ile sarının protein granüllerinde oluşan fosvitindir. Maternal antioksidanlar, oksidatif stresin önlenmesi ve embriyo gelişimi üzerinde temel role sahiptirler. Yumurta sarısı, embriyonun normal gelişimini sağlamak ve enerji ihtiyacını karşılamak için yüksek düzeyde yağ ve doymamış yağ asitleri (PUFA) içerir. Sarıdaki yüksek yağ ve PUFA düzeyleri lipid peroksidasyona (LPO) yol açarak embriyo dokularına zarar verebilir. Dolayısıyla, embriyoyu LPO’dan korumak için, embriyo dokularında etkili antioksidanların bulunması gerekir. Embriyo gelişiminin 19. gününde embriyo dokularında PUFA, LPO ve oksijen kullanımı arttığından, dokularda doğal antioksidan depoları embriyoyu korumak için yeterli düzeyde olmayıp, bu dönem embriyo için risklidir. Çıkışta civcivin immun sistemi fonksiyonel olmadığından, maternal antioksidanlar immun sistem etkinliği üzerindeki serbest radikallerin zararlı etkilerini azaltma açısından da oldukça önemlidir. Ayrıca, maternal antioksidanlar çıkıştan sonra civcivi reaktif oksijen türlerine (ROS) karşı korur. Bu derlemenin amacı, kanatlılarda yumurta sarısındaki maternal antioksidanlar ile bunların embriyo gelişimi açısından önemini irdelemektir.

Anahtar Kelimeler

• Embriyo gelişimi, Maternal etki, Sarıdaki antioksidanlar

References

1. Adkins-Regan E, Ottinger MA, Park J (1995). Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J. Exp. Zool. 271: 466-470.
2. Akbari MR, Kermanshahi H, Nassiri Moghaddam H, Heravi Moussavi AR, Tavakkol Afshari J (2008). Effects of wheat-soybean meal based diet supplementation with vitamin A, vitamin E and zinc on blood cells, organ weights and humoral immune response in broiler chickens. Journal of Animal and Veterinary Advances 7(3): 297-304.
3. Anton M, Castellani O, Gue´Rin-Dubiard C (2007). Bioactive egg compounds. Springer-Verlag Berlin Heidelberg, pp. 17-24.
4. Berthouly A, Helfenstein F, Richner H (2007). Cellular immune-response, stress resistance and competitiveness in nestling great tits in relation to maternally transmitted carotenoids. Functional Ecology 21: 335-343.
5. Berthouly A, Helfenstein F, Tanner M, Richner H (2008). Sex-related effects of maternal egg investment on offspring in relation to carotenoid availability in the great tit. Journal of Animal Ecology 77: 74-8
6. Biard C, Surai PF, Mİller, AP (2007). An analysis of pre- and post-hatching maternal effects mediated by carotenoids in the blue tit. Journal of Evolutionary Biology 20: 326-339.
7. Biard C, Gil D, Karadaş F, Saino N, Spottiswoode CN, Surai PF, Mİller AP (2009). Maternal effects mediated by antioxidants and the evolution of carotenoid-based signals in birds. Am. Nat. 174: 696-70
8. Blount JD, Houston DC, Mİller AP (2000). Why egg yolk is yellow. Trends Ecol. Evol. 15: 47-49.

9. Blount JD, Surai PF, Nager RG, Houston DC, Mİller AP, Trewby ML, Kennedy MW (2002). Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: A supplemental feeding study of maternal effects. Proceedings of the Royal Society of London B 269: 26-36.
10. Blount JD, Houston DC, Surai PF, Moller AP (2004). Egg-laying capacity is limited by carotenoid pigment availability in wild gulls Larus fuscus. Proceedings of the Royal Society of London Series B 271: 71–81.
11. Bollengier-Lee S, Mitchell MA, Utomo DB, Williams PE, Whitehead CC (1998). Influence of high dietary vitamin E supplementation on egg production and plasma characteristics in hens subjected to heat stress. British Poultry Science 39: 106-112.
12. Bollengier-Lee S, Williams PE, Whitehead CC (1999). Optimal dietary concentration of vitamin E for alleviating the effect of heat stress on egg production in laying hens. British Poultry Science 40: 102-10
13. Brush AH (1990). Metabolism of carotenoid pigments in birds. FASEB J. 4: 2969-2977.
14. Burley RW, Cook WH, (1961). Isolation and composition of avian egg yolk granules and their constituent alpha- and beta-lipovitellins. Can. J. Biochem. Physiol. 39: 1295-1307.
15. Burton GW, Ingold KU (1984). Beta-carotene an unusual type of lipid antioxidant. Science 224: 569-573. Chalghoumi R, Beckers Y, Portetelle D, Théwis A (2009). Hen egg yolk antibodies (IgY), production and use for passive immunization against bacterial enteric infections in chicken: A review. Biotechnol. Agron. Soc. Environ. 13: 295-308.
16. Cherian G, Sim ES (1997). Egg yolk polyunsaturated fatty acids and vitamin E content alters the tocopherol status of hatched chicks. Poultry Science 76: 1753-1759.
17. Fang YZ, Yang S, Wu G (2002). Free radicals, antioxidants, and nutrition. Nutrition 18: 872-879.
18. Fronning GV (1998). Recent advances in egg products research and development. Egg Processing Workshop Riverside and Modesto, June 2-3, University of California, America.
19. Gaal T, Miklos M, Raymond CN, Dixon J, Speake BK (1995). Development of antioxidant capacity in tissues of the chick embryo. Comp. Biochem. Physiol. 112B :711-716.
20. Grindstaff JL, Brodie ED, Ketterson ED (2003). Immune function across generations: Integrating mechanism and evolutionary process in maternal antibody transmission. Proceedings of the Royal Society of London Series B-Biological Sciences 270: 2309-2319.
21. Groothuis TGG, Eising CM, Blount JD, Surai PF, Apanius V, Dijkstra C, Müller W (2006). Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. Journal of Evolutionary Biology 19: 1304-1313.
22. Halliwell B, Gutteridge JMC (1999). Free Radicals in Biology and Medicine. Oxford University Press, Oxford, UK.
23. Haq A, Bailey CA, Chinnah A (1996). Effect of ß-carotene, canthaxan-thin, lutein, and vitamin E on neonatal immunity of chicks when supplemented in the broiler breeder diets. Poultry Science 75: 1092– 1097.
24. Hayward LS, Wingfield JC (2004). Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. General and Comparative Endocrinology 135: 365-371.
25. Hõrak P, Surai PF, Mİller AP (2002). Fat-soluble antioxidants in the eggs of great tits Parus major in relation to breeding habitat and laying sequence. Avian Science, 2: 1-8.
26. Joshi PS, Mathur SN, Murthy SK, Ganguly J (1973). Vitamin A economy of the developing chick embryo and of the freshly hatched chick. Biochem. J. 136: 757-761.
27. Lin YF, Tsai HL, Lee YC, Chang SJ (2005). Maternal vitamin E supplementation affects the antioxidant capability and oxidative status of hatching chicks. The Journal of Nutrition 135(10): 2457-2461. Lu CL, Baker RC (1986). Characteristics of egg yolk phosvitin as an antioxidant for inhibiting metalcatalyzed phospholipid oxidations. Poultry Science 65: 2065–70.
28. McGraw KJ, Adkins-Regan E, Parker RS (2005). Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird. Naturwissenschaften 92: 375380.
29. Moran ET (2007). Nutrition of the developing embryo and hatchling. Poultry Science 86: 1043–1049.
30. Müller W (2004). General introduction, pp. 1-36. Maternal phenotypic engineering adaptation and constraint in prenatal maternal effects, The University of Groningen, The Netherlands.
31. Nager RG, Monaghan P, Houston DC, Arnold KE, Blount JD, Verboven N (2006). Maternal effects through the avian egg. Acta Zoologica Sinica, 52: 658–661.
32. Navara JK, Badyaev VA, Mendonça MT, Hill GE (2006). Yolk antioxidants vary with male attractiveness and female condition in the house finch (Carpodacus mexicanus). Physiological and Biochemical Zoology, 79(6): 1098–1105.
33. Noble RC, Spake BK (1997). Prenatal and neonatal medicine. 2:92-100.
34. Percival M (1998). Antioxidants. Clinical Nutrition Insights, NUT031 1/96 Rev. 10-98.
35. Remes V, Krist M, Bertacche V, Stradi R (2007). Maternal carotenoid supplementation does not affect breeding performance in the Great Tit (Parus major). Functional Ecology 21: 776-783.
36. Remes V, Matysiokova B, Klejdus B (2011). Egg yolk antioxidant deposition as a function of parental ornamentation, age, and environment in Great Tits (Parus major). J. Avian Biol. 42: 387-396.
37. Royle NJ, Surai PF, McCartney RJ, Speake BK (1999). Parental investment and egg yolk lipid composition in gulls. Functional Ecology 13: 298-306.
38. Royle NJ, Surai PF, Hartley IR (2001). Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behavioral Ecology 12: 381-385.
39. Royle NJ, Surai PF, Hartley IR (2003). The effect of variation in dietary intake on maternal deposition of antioxidants in zebra finch eggs. Functional Ecology 17: 472-481.
40. Rubolini D, Romano M, Bonisoli Alquati A, Saino N (2006). Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of Yellow-legged Gull (Larus michahellis) chicks. Journal Compilation European Society For Evolutionary Biology 19: 1571158
41. Rubolini D, Romano M, Navara KJ, Karadas F, Ambrosini R, Caprioli M, Saino N (2011). Maternal effects mediated by egg quality in the Yellow-legged Gull Larus michahellis in relation to laying order and embryo sex. Frontiers in Zoology 8: 1-15. DOI:10.1186/1742-9994-8-24
42. Saino N, Ferrari RP, Romano M, Martinelli R, Mİller AP (2003). Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc. R Soc. Lond. B Biol. Sci. 270: 2485–2489.
43. Samaraweera H, Zhang W, Lee EJ, Ahn DU (2011). Egg yolk phosvitin and functional phosphopeptides—Review. Journal of Food Science 76: 143-150.
44. Schwabl H (1993). Yolk is a source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. 90: 11446-11450.
45. Surai PF, Noble RC, Speake BK (1996). Tissue-specific differences in antioxidant distribution and susceptibility to lipid peroxidation during development of the chick embryo. Biochim. Biophys. Acta 1304: 1–10.
46. Surai PF, Speake BK (1998). Distribution of carotenoids from the yolk to the tissues of the chick embryo. J. Nutr. Biochem. 9: 645– 651.
47. Surai PF, Ionov IA, Kuchmistova E, Noble RC, Speake B (1998a). The relationship between the levels of α-tocopherol and carotenoids in the maternal feed, yolk and neonatal tissues: Comparison between the chicken, turkey, duck and goose. Journal of the Science of Food and Agriculture, 76: 593-598.
48. Surai PF, Ionov IA, Kuklenko TV, Kostjuk IA, Macpherson A, Speake BK, Noble RC, Sparks NHC (1998b). Effect of supplementing the hen’s diet with vitamin A on the accumulation of vitamins A and E, ascorbic acid and carotenoids in the egg yolk and in the embryonic liver. British Poultry Science 39: 257–263.
49. Surai PF (1999). Tissue-specific changes in the activities of antioxidant enzymes during the development of the chicken embryo. British Poultry Science 40: 397– 405.
50. Surai PF, Noble RC, Speake BK (1999). Relationship between vitamin E content and susceptibility to lipid peroxidation in tissues of the newly hatched chick. British Poultry Science 40: 406-410.
51. Surai PF (2000). Effect of the selenium and vitamin E content of the maternal diet on the antioxidant system of the yolk and the developing chick. British Poultry Science 41: 235-243.
52. Surai PF (2001). The relevance of the antioxidant system to the health and growth of the developing chick. Aust. Poult. Sci. Sym. 2001. Sydney, Austuralia. pp.126-134.
53. Surai PF (2002). Natural Antioxidants in Avian Nutrition and Reproduction. Nottingham University, Nottingham.
54. Surai PF, Steinberg W, Wakeman WG, Speake BK, Sparks NHC (2003). Effect of canthaxanthin content of the maternal diet on the antioxidant system of the developing chick. British Poultry Science 44: 612–619.
55. Surai PF, Sparks NHC, Speake BK (2006). The role of antioxidants in reproduction and fertility of poultry. XII. European Poultry Conference, September 10-14, Verona, Italy, pp. 354-358.
56. Surai PF (2010). Natural antioxidants in poultry nutrition: New developments. 16 th Europen Symposium on Poultry Nutrition, August 26-30, Strasbourg, France, pp. 669-676.
57. Tanvez A, Amy M, Chastel O, Leboucher G (2009). Maternal effects and β-carotene assimilation in Canary chicks. Physiology & Behavior 96: 389–393.
58. Verboven N, Evans NP, D’Alba L (2005). Intra-specific interactions influence egg composition in the lesser black backed gull (Larus fuscus). Behavioral Ecology and Sociobiology 57: 357–365.
59. Vleck CM, Bucher TL (1998). Energy metabolism, gas exchange, and ventilation. In: JM Starck and RE Ricklefs, Editors, Avian Growth and Development: Evolution within the Altricial-precocial Spectrum. Oxford University Press, Oxford.
60. Von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999). Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. Lond. B 266: 1-12.
61. Willimson KA, Surai PF, Graves JA (2006). Yolk antioxidants and mate attractiveness in the Zebra Finch. Functional Ecology 20: 354–359.
62. Young AJ, Lowe GM (2001). Antioxidant and pro-oxidant properties of carotenoids. Archives of Biochemistry and Biophysics 385(1): 20-27.