Effect of dietary supplementation of Nannochloropsis on gene expression and metabolic profile of immune and antioxidant markers in growing Barki lambs
Published:
Jul 11, 2024
Keywords:
Barki lambs gene expression Nannochloropsis antioxidant immune response
Abstract
The aim of the current study was to elaborate the effect of dietary supplementation of Nannochloropsis on gene expression and metabolic profile of immune and antioxidant markers in growing Barki lambs. Sixty apparently healthy growing Barki lambs were enrolled in this study. Lambs were randomly allocated into two equal groups (30 lambs each). The first group considered control group, whereas the second group supplemented with commercially available Nannochloropsis powder for subsequent 30 days. Supplementation of growing lambs with Nannochloropsis could modulate gene expression profile of immune and antioxidant markers. Levels of immune (IL1B, IL2, Il6, IL8, RANTES, NFKB, MASP2 and TNFα) and antioxidant (SOD3, GPX4, PRDX2, and Nrf2) genes expression were significantly up-regulated in lambs supplemented with Nannochloropsis at day 30 than control and day 15. There was a significant (p < 0.05) increase in the serum concentrations of SOD, CAT, TAC, GPx, NO, GSH, lysozyme activity, TNF-α, IL1, IL-6 and IgA with significant decrease in MDA level in supplemented group in relation to control ones. While IgG and IgM levels were not significantly (P > 0.05) differed among the tested groups. The results herein confirm that there was profound immunological, antioxidant alterations associated with dietary supplementation of Nannochloropsis in growing Barki lambs. Gene expression and serum profiles may serve as stand-in markers for immunological status monitoring and the development of an efficient management strategy for enhancing the health of growing Barki lambs.
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Ebissy, E., El-Sayed, A., & Ateya, A. (2024). Effect of dietary supplementation of Nannochloropsis on gene expression and metabolic profile of immune and antioxidant markers in growing Barki lambs. Journal of the Hellenic Veterinary Medical Society, 75(2), 7585–7596. https://doi.org/10.12681/jhvms.35314
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References
Abd El-Hamid I, Fouda W, Shedeed H, Moustafa S, Elbaz A, Bakr S, Mosa B,
Morsy A, Hasan A, Emam K. 2022. Influence of microalgae Nannochloropsis oculata on blood constituents, reproductive performance and productivity in Hi-Plus doe rabbits under North Sinai conditions in Egypt. J
Anim Health Prod 10(2): 135-145. DOI | http://dx.doi.org/10.17582
Abdel-Moneim A-M E, Shehata A M, Mohamed N G, Elbaz A M, Ibrahim N
S. 2022. 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. doi: 10.1007/s12011-021-02662-w.
Abdullah M A M. 2015. The antioxidant effect of dietary microalgae supplementation on milk, blood and rumen of dairy goats. Ph.D Thesis, Faculty
of Animal Science and Aquaculture, Agricultural University of Athens.
.DOI.10.4314/ijbcs.v8i6.33
Al-Batshan H A, Al-Mufarrej S I, Al-Homaidan A A, Qureshi M. 2001. Enhancement of chicken macrophage phagocytic function and nitrite production by dietary Spirulina platensis. Immunopharmacol Immunotoxicol 23(2): 281-289. doi: 10.1081/iph-100103866
Amer S A. 2016. Effect of Spirulina platensis as feed supplement on growth
performance, immune response and antioxidant status of mono-sex Nile
Tilapia (Oreochromis niloticus). B V M J 30(1): 1-10. DOI:10.21608/
bvmj.2016.31332
Ateya A, El-Sayed A, Mohamed R. 2021. Gene expression and serum profile
of antioxidant markers discriminate periparturient period time in dromedary camels. Mammal Res 66: 603-613. DOI:10.1007/s13364-021-
-3
Balachandran P, Pugh N D, Ma G, Pasco D S. 2006. Toll-like receptor 2-dependent activation of monocytes by Spirulina polysaccharide and its
immune enhancing action in mice. Int Immunopharmacol 6(12): 1808-
doi: 10.1016/j.intimp.2006.08.001.
Bannerman D. 2009. Pathogen-dependent induction of cytokines and other
soluble inflammatory mediators during intramammary infection of dairy
cows. J Anim Sci 87(suppl_13): 10-25. doi: 10.2527/jas.2008-1187.
Barry M, Ouedraogo M, Sourabie S, Guissou I P. 2014. Intérêt thérapeutique
de la spiruline chez l’homme: revue général. Int J Biol Chem Sci 8(6):
-2749. Doi. 10.4314/ijbcs.v8i6.33
Becker E W. 2007. Micro-algae as a source of protein. Biotechnol Adv 25(2):
Belay A, Kato T, Ota Y. 1996. Spirulina (Arthrospira): potential application as
an animal feed supplement. J Appl Phycol 8: 303-311.
Ben H M, Ben I M, Garrab M, Aly R, Gagnon J, Naghmouchi K. 2017.
Antimicrobial, antioxidant, cytotoxic and anticholinesterase activities
of water-soluble polysaccharides extracted from microalgae Isochrysis
galbana and Nannochloropsis oculata. J Serb Chem Soc 82(5): 509-522.
DOI:10.2298/JSC161016036B
Bendimerad S. 2019. Effects of dietary microalgae Nannochloropsis gaditana
on serum and redox status in obese rats subjected to a high fat diet. Phytothérapie 17: 177-187. https://doi.org/10. 3166/phyto-2018-0019.
Benedict C A, Banks T A, Ware C F. 2003. Death and survival: viral regulation of TNF signaling pathways. Curr Opin Immunol 15(1): 59-65. doi:
1016/s0952-7915(02)00018-3.
Board P G, Menon D. 2013. Glutathione transferases, regulators of cellular
metabolism and physiology. Biochim Biophys Acta (bba)-general subjects 1830(5): 3267-3288. DOI: 10.1016/j.bbagen.2012.11.019
Borish L C, Steinke J W. 2003. 2. Cytokines and chemokines. J Allergy Clin
Immunol 111(2): S460-S475. DOI: 10.1067/mai.2003.108
Bradley J. 2008. TNF‐mediated inflammatory disease. The Journal of Pathology: J Pathol Soc of Great Britain and Ireland 214(2): 149-160. DOI:
1002/path.2287
Bule M H, Ahmed I, Maqbool F, Bilal M, Iqbal H M. 2018. Microalgae as a
source of high-value bioactive compounds. Front Biosci 10(2): 197-216.
DOI: 10.2741/s509
Camacho F, Macedo A, Malcata F. 2019. Potential industrial applications and
commercialization of microalgae in the functional food and feed industries: A short review. Mar Drugs 17(6): 312. DOI: 10.3390/md17060312
Carolina O, Pandeirada, ÉliaMaricato, Sónia, S., Ferreira, Viviana, G.,
Correia, Benedita, A., Pinheirob, Dmitry, V., Evtuguinc, Angelina, S.,
Palmab, Alexandra, Correia, Manuel, Vilanova., Manuel, A., Coimbra,
Cláudia, Nunesa. 2019. Structural analysis and potential immunostimulatory activity of Nannochloropsis oculata polysaccharides. Carbohydr
Polym 222: 114962. https://doi.org/10.1016/j.carbpol.2019.06.001
Cerezuela R, Guardiola F A, Meseguer J, Esteban M Á. 2012. Enrichment of
gilthead seabream (Sparus aurata L.) diet with microalgae: effects on the
immune system. Fish Physiol Biochem 38: 1729-1739. DOI: 10.1007/
s10695-012-9670-9
Chen X, Song L, Wang H, Liu S, Yu H, Wang X, Li R, Liu T, Li P. 2019.
Partial characterization, the immune modulation and anticancer activities
of sulfated polysaccharides from filamentous microalgae Tribonema sp.
Molecules 24(2): 322. doi: 10.3390/molecules24020322
Chew K W, Yap J Y, Show P L, Suan N H, Juan J C, Ling T C, Lee D-J,
Chang J-S. 2017. Microalgae biorefinery: high value products perspectives. Bioresour Technol 229: 53-62. https://doi.org/10.1016/j.
biortech.2017.01.006
Chuang W-C, Ho Y-C, Liao J-W, Lu F-J. 2014. Dunaliella salina exhibits an
antileukemic immunity in a mouse model of WEHI-3 leukemia cells. J
Agric Food Chem 62(47): 11479-11487. doi: 10.1021/jf503564b.
de Morais M G, Vaz B d S, de Morais E G, Costa J A V. 2015. Biologically
active metabolites synthesized by microalgae. Biomed Res Int 2015. doi:
1155/2015/835761.
EL-Sabagh M R, Abd Eldaim M A, Mahboub D, Abdel-Daim M. 2014. Effects of Spirulina platensis algae on growth performance, antioxidative
status and blood metabolites in fattening lambs. J Agric Sci 6(3): 92.
DOI:10.5539/jas.v6n3p92
Elbaz A M, Ahmed A M, Abdel-Maqsoud A, Badran A M, Abdel-Moneim
A-M E. 2022. Potential ameliorative role of Spirulina platensis in powdered or extract forms against cyclic heat stress in broiler chickens. Environ Sci Pollut Res 29(30): 45578-45588. doi.org/10.1007/s11356-022-
-z
Elsheikh S, Galal A A, Fadil R. 2018. Hepatoprotective impact of Chlorella
vulgaris powder on deltamethrin intoxicated rats. Z V J 46(1): 17-24.
DOI: 10.21608/zvjz.2018.7620
Flaga J, Górka P, Kowalski Z. 2019. The effect of docosahexaenoic acid-rich
algae supplementation in milk replacer on performance and selected immune system functions in calves. J Dairy Sci 102(10): 8862-8873. doi:
3168/jds.2018-16189
Fremond C M, Yeremeev V, Nicolle D M, Jacobs M, Quesniaux V F, Ryffel
B. 2004. Fatal Mycobacterium tuberculosis infection despite adaptive
immune response in the absence of MyD88. J Clin Invest 114(12): 1790-
doi: 10.1172/JCI21027
Fu J, Wang J, Luo Y, Zhang L, Zhang Y, Dong X, Yu H, Cao M, Ma X. 2016.
Association between MASP-2 gene polymorphism and risk of infection
diseases: a meta-analysis. Microb Pathog 100: 221-228. doi: 10.1016/j.
micpath.2016.10.004.
Furbeyre H, van Milgen J, Mener T, Gloaguen M, Labussière E. 2018. Effects
of oral supplementation with Spirulina and Chlorella on growth and digestive health in piglets around weaning. Animal 12(11): 2264-2273. doi:
1017/S1751731118000125.
Gbadamosi O K, Lupatsch I. 2018. Effects of dietary Nannochloropsis salina
on the nutritional performance and fatty acid profile of Nile tilapia, Oreochromis niloticus. Algal Res 33: 48-54. DOI:10.1016/j.algal.2018.04.030
Ghattas T, Dawoud E, Mahrous A, Elgabry E. 2019. Effect of Spirulina platensis supplementation on growth, some biochemical and immunological
parameters in suckling calves. J Egypt Vet Med Assoc 79: 443-460.
Glasauer A, Chandel N S. 2014. Targeting antioxidants for cancer therapy.
Biochem Pharmacol 92(1): 90-101. doi: 10.1016/j.bcp.2014.07.017.
Gomaa A S, Kholif A E, Kholif A M, Salama R, El-Alamy H A, Olafadehan
O A. 2018. Sunflower oil and Nannochloropsis oculata microalgae as
sources of unsaturated fatty acids for mitigation of methane production
and enhancing diets’ nutritive value. J Agric Food Chem 66(8): 1751-
doi: 10.1021/acs.jafc.7b04704
Hassan S Y, Zahrat, El-Ola Nadra, Mohamed, M., El- Sayed, A.B. 2015. Production and Evaluation of Pasta Supplemented with Spirulina platensis
Biomass. Adv Food Sci 37: 153- 162. DOI | http://dx.doi.org/10.17582
Hibberd D. 1981. Notes on the taxonomy and nomenclature of the algal classes Eustigmatophyceae and Tribophyceae (synonym Xanthophyceae).
Bot J Linn Soc 82(2): 93-119. https://doi.org/10.1111/j.1095-8339.1981.
tb00954.x
Ighodaro O, Akinloye O. 2018. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their
fundamental role in the entire antioxidant defence grid. Alexandria J Med
(4): 287-293. https://doi.org/10.1016/j.ajme.2017.09.001
Ingebrigtsen R A, Hansen E, Andersen J H, Eilertsen H C. 2016. Light and
temperature effects on bioactivity in diatoms. J Appl Phycol 28: 939-950.
DOI 10.1007/s10811-015-0631-4
Jackson P G, Cockcroft P D, Elmhurst S (2002). Clinical examination of farm
animals, Wiley Online Library.
Khan M I, Shin J H, Kim J D. 2018. The promising future of microalgae:
current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microbial cell factories 17(1): 1-21. Khan et al. Microb Cell Fact (2018) 17:36 https://doi.
org/10.1186/s12934-018-0879-x
Kholif A E, Gouda G A, Hamdon H A. 2020. Performance and milk composition of Nubian goats as affected by increasing level of Nannochloropsis
oculata microalgae. Animals 10(12): 2453. doi: 10.3390/ani10122453
Lager K, Jordan E (2012). The metabolic profile for the modern transition
dairy cow. Mid-South Ruminant Nutrition Conference.
Lamminen M, Halmemies-Beauchet-Filleau A, Kokkonen T, Jaakkola S, Vanhatalo A. 2019. Different microalgae species as a substitutive protein feed
for soya bean meal in grass silage based dairy cow diets. Anim. Feed Sci
Technol 247: 112-126. https://doi.org/10.1016/j.anifeedsci.2018.11.005
Lauritano C, Andersen J H, Hansen E, Albrigtsen M, Escalera L, Esposito F,
Helland K, Hanssen K Ø, Romano G, Ianora A. 2016. Bioactivity screening of microalgae for antioxidant, anti-inflammatory, anticancer, anti-diabetes, and antibacterial activities. Front Mar Sci 3: 68. doi.org/10.3389/
fmars.2016.00068
Lavy A, Naveh Y, Coleman R, Mokady S, Werman M J. 2003. Dietary
Dunaliella bardawil, a β-carotene-rich alga, protects against acetic acid-induced small bowel inflammation in rats. Inflamm Bowel Dis 9(6):
-379. doi: 10.1097/00054725-200311000-00005.
Lester D H, Russell G, Barendse W, Williams J. 1996. The use of denaturing gradient gel electrophoresis in mapping the bovine tumor necrosis
factor α gene locus. Mammalian Genome 7(3): 250-252. DOI:10.1292/
jvms.15-0506
Levering J, Broddrick J, Zengler K. 2015. Engineering of oleaginous organisms for lipid production. Curr Opin Biotechnol 36: 32-39. doi:
1016/j.copbio.2015.08.001.
Liemburg-Apers D C, Willems P H, Koopman W J, Grefte S. 2015. Interactions between mitochondrial reactive oxygen species and cellular
glucose metabolism. Arch Toxicol 89: 1209-1226. doi: 10.1007/s00204-
-1520-y
Loor J. 2010. Genomics of metabolic adaptations in the peripartal cow. Animal 4(7): 1110-1139. doi: 10.1017/S1751731110000960.
Manzo E, Gallo C, Fioretto L, Nuzzo G, Barra G, Pagano D, Krauss I R,
Paduano L, Ziaco M, DellaGreca M. 2019. Diasteroselective colloidal
self-assembly affects the immunological response of the molecular adjuvant sulfavant. ACS omega 4(4): 7807-7814. doi: 10.1021/acsomega.8b03304.
Masella R, Di Benedetto R, Varì R, Filesi C, Giovannini C. 2005. Novel
mechanisms of natural antioxidant compounds in biological systems:
involvement of glutathione and glutathione-related enzymes. J Nutr Biochem 16(10): 577-586. doi: 10.1016/j.jnutbio.2005.05.013.
Md A, Jin F, Jeong U-C, Choi J-K, Lee D-I, Yu H S, Kang S-J. 2018. Effects
of Nannochloropsis concentration in diet on growth, survival and anti-inflammatory cytokine (Interleukin-10) production of the sea cucumber
Apostichopus japonicus. Turk J Fish Aquat Sci 18(4): 567-575. DOI:
4194/1303-2712-v18_4_08
Mesalam N M, Aldhumri S A, Gabr S A, Ibrahim M A, Al-Mokaddem A K,
Abdel-Moneim A-M E. 2021. Putative abrogation impacts of Ajwa seeds
on oxidative damage, liver dysfunction and associated complications in
rats exposed to carbon tetrachloride. Mol Biol Rep 48: 5305-5318. doi:
1007/s11033-021-06544-1
Nacer W, Fatima, Z.B., Merzouk, H., Benyagoub, O., Bouanane, S. 2020.
Evaluation of the anti-inflammatory and antioxidant effects of the microalgae Nannochloropsis gaditana in streptozotocin-induced diabetic
rats. J Diabetes Metab Disord 19: 1483-1490. https://doi.org/10.1007/
s40200- 020-00681-3
Nutt S L, Hodgkin P D, Tarlinton D M, Corcoran L M. 2015. The generation
of antibody-secreting plasma cells. Nat Rev Immunol 15(3): 160-171.
DOI: 10.1038/nri3795
Oliva A, Kinter A L, Vaccarezza M, Rubbert A, Catanzaro A, Moir S, Monaco
J, Ehler L, Mizell S, Jackson R. 1998. Natural killer cells from human
immunodeficiency virus (HIV)-infected individuals are an important
source of CC-chemokines and suppress HIV-1 entry and replication in
vitro. J Clin Invest 102(1): 223-231. doi: 10.1172/JCI2323
Panahi Y, Mostafazadeh B, Abrishami A, Saadat A, Beiraghdar F, Tavana S,
Pishgoo B, Parvin S, Sahebkar A. 2013. Investigation of the effects of
Chlorella vulgaris supplementation on the modulation of oxidative stress
in apparently healthy smokers. Clin Lab 59(5-6): 579-587. doi: 10.7754/
clin.lab.2012.120110.
Pfaffl M W. 2001. A new mathematical model for relative quantification in
real-time RT-PCR. Nucleic Acids Res 29(9): e45-e45. DOI: 10.1093/
nar/29.9.e45
Guillard, RR and Ryther, JH. 1962. Studies of marine planktonic diatoms. 1.
Cyclotella nana Hustedt, and Detonula confervacea (cleve) gran. Can J
Microbiol 8: 229-239. doi: 10.1139/m62-029.
Ruminants N R C C o N R o S (2007). Nutrient requirements of small ruminants: sheep, goats, cervids, and new world camelids, 中国法制出版社.
Salim T, Sershen C L, May E E. 2016. Investigating the role of TNF-α and
IFN-γ activation on the dynamics of iNOS gene expression in LPS stimulated macrophages. PloS one 11(6): e0153289. DOI: 10.1371/journal.
pone.0153289
Samarakoon K W, Ko J-Y, Rahman S M M, Lee J-H, Kang M-C, Kwon O-N,
Lee J-B, Jeon Y-J. 2013. In vitro studies of anti-inflammatory and anticancer activities of organic solvent extracts from cultured marine microalgae. Algae 28(1): 111-119. doi.org/10.4490/algae.2013.28.1.111
Sies H. 1991. Oxidative stress: from basic research to clinical application. Am
J Med 91(3): S31-S38. https://doi.org/10.1016/0002-9343(91)90281-2
Sordillo L M. 2013. Selenium-dependent regulation of oxidative stress
and immunity in periparturient dairy cattle. Vet Med Int 2013. doi.
org/10.1155/2013/154045
Sucu E, Udum D, Güneş N, Canpolat Ö, Filya İ. 2016. Influence of supplementing diet with microalgae (Schizochytrium limacinum) on growth
and metabolism in lambs during the summer. Turk J Vet Anim Sci 41:
-174. DOI.10.3906/vet-1606-65
Taub D D, Sayers T J, Carter C, Ortaldo J R. 1995. Alpha and beta chemokines induce NK cell migration and enhance NK-mediated cytolysis. J
Immunol (Baltimore, Md.: 1950) 155(8): 3877-3888.
Tavares E, Miñano F J. 2004. Differential sensitivities of pyrogenic chemokine fevers to CC chemokine receptor 5 antibodies. Fundam Clin Pharmacol 18(2): 163-169. DOI: 10.1111/j.1472-8206.2003.00227.x
Tsakanova G, Stepanyan A, Nahapetyan K, Sim R B, Arakelyan A, Boyajyan
A. 2018. Serine proteases of the complement lectin pathway and their
genetic variations in ischaemic stroke. J Clin Pathol 71(2): 141-147. doi:
1111/jpn.12671.
Tsiplako E, Abdullah, M.A.M., Mavrommatis, A., Chatzikonstantinou, M.,
Skliros, D., Sotirakoglou, K., Flemetakis, E., N. E. Labrou, N.E., Zervas,
G. 2016. The effect of dietary Chlorella vulgaris inclusion on goat’s milk
chemical composition, fatty acids profile and enzymes activities related
to oxidation. J Anim Physiol Anim Nutr 102: 142-151. DOI: 10.1111/
jpn.12671
Vakifahmetoglu-Norberg H, Ouchida A T, Norberg E. 2017. The role of mitochondria in metabolism and cell death. Biochem Biophys Res Commun
(3): 426-431. doi: 10.1016/j.bbrc.2016.11.088.
Van Harten S, Brito R, Almeida A, Scanlon T, Kilminster T, Milton J, Greeff
J, Oldham C, Cardoso L. 2013. Gene expression of regulatory enzymes
involved in the intermediate metabolism of sheep subjected to feed restriction. Animal 7(3): 439-445. doi: 10.1017/S1751731112001589.
Wu J, Bai J, Li L, Huang S, Li C, Wang G. 2015. Genetic polymorphisms of
the BMAP-28 and MASP-2 genes and their correlation with the somatic cell score in Chinese Holstein cattle. Genet Mol Res 14(1): 1-8. doi:
4238/2015.January.15.1.
Yaakob Z, Ali E, Zainal A, Mohamad M, Takriff M S. 2014. An overview:
biomolecules from microalgae for animal feed and aquaculture. J Biol
Res (Thessalon) 21: 1-10. doi: 10.1186/2241-5793-21-6
Yadav J, Kumar R. 2018. Effect of Spirulina (Spirulina platensis) Supplementation on Antioxidant Status and Immunity in Growing Barbari Goats. Int
J Livest Res 8(12): 252-257. doi: 10.5455/ijlr.20180403064752
Yamamoto M, Kensler T W, Motohashi H. 2018. The KEAP1-NRF2 system:
a thiol-based sensor-effector apparatus for maintaining redox homeostasis. Physiol Rev 98(3): 1169-1203. doi: 10.1152/physrev.00023.2017.
Ye Z-W, Zhang J, Townsend D M, Tew K D. 2015. Oxidative stress, redox
regulation and diseases of cellular differentiation. Biochim Biophys
Acta (BBA)-General Subjects 1850(8): 1607-1621. doi: 10.1016/j.
bbagen.2014.11.010.
Ytting H, Christensen I, Steffensen R, Alsner J, Thiel S, Jensenius J C, Hansen
U, Nielsen H. 2011. Mannan‐binding lectin (MBL) and MBL‐associated
serine protease 2 (MASP‐2) genotypes in colorectal cancer. Scand J Immunol 73(2): 122-127. doi: 10.1111/j.1365-3083.2010.02480.x.
Yu B P. 1994. Cellular defenses against damage from reactive oxygen species.
Physiol Rev 74(1): 139-162. doi: 10.1152/physrev.1994.74.1.139.
Zhang H, Wei Y, Zhang F, Liu Y, Li Y, Li G, Han B, Wang H, Zhao W, Wang
C. 2019. Polymorphisms of MASP2 gene and its relationship with mastitis and milk production in Chinese Holstein cattle. Biotechnol Biotechnol
Equip 33(1): 589-596. https://doi.org/10.1080/13102818.2019.1596755
