Yeast cell wall (YCW) preparations are important nutritional additives in the aquaculture industry. Head-kidney macrophages play important roles in innate immune functions in fish. However, the mechanisms underlying their stimulation are not yet characterized. The purpose of this study was to investigate the effects of YCW on immunological functions of channel catfish (Ictalurus punctatus) head-kidney macrophages. Our results showed that YCW preparations not only improved the proliferation and phagocytosis of macrophages but also induced the secretion of reactive oxygen species (ROS), nitric oxide (NO), inducible nitric oxide synthase (iNOS), and cytokines, such as tumor necrosis factor-α (TNF-α) and interleukin 1β (IL-1β). At a concentration of 500.0 μg/mL, YCW preparations stimulated macrophage proliferation and phagocytosis to 1.98 and 1.8 times, respectively, when compared with the negative group. Equally, YCW preparations raised the production of NO by inducing iNOS and ROS in a concentration-dependent manner. Furthermore, these preparations enhanced TNF-α and IL-1β mRNA levels to multiple digits from 1.2 to 3.0 times, respectively. In conclusion, the stimulatory effects of YCW on the phagocytic activity of the fish macrophages were associated with respiratory bursts coupled with nitric oxide production.
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Akramienė D, Kondrotas A, Didžiapetrienė J, Egidijus K (2007) Effects of beta-glucans on the immune system. Medicina (Kaunas) 43(8):597–606
Bernard EJJ, Leandro NP, João CSB, José RMC (2006) Characterization of macrophage phagocytosis of the tropical fish Prochilodus scrofa (Steindachner,1881). Aquaculture 251:509–515
Borchani C, Fonteyn F, Jamin G, Paquot M, Thonart P, Blecker C(2016) Physical, functional and structural characterization of the cell wall fractions from baker’s yeast Saccharomyces cerevisiae. Food Chem 1149–1155, 194
Brown GD, Gordon S (2005) Immune recognition of fungal β-glucans. Cell Microbiol 7(4):471–479
Chang CF, Su MS, Chen HY, Liao IC (2003) Dietary β-1,3-glucan effectively improves immunity and survival of Penaeus monodon, challenged with white spot syndrome virus. Fish Shellfish Immun 15(4):297–310
Cheng A, Wan F, Wang JQ, Jin Z, Xu X (2008) Macrophage immunomodulatory activity of polysaccharides isolated from Glycyrrhiza uralensis Fish. Int Immunopharmacol 8:43–50
Crumlish M, Dung TT, Somsiri T, Lnglis V, Thompson KD (2000) Development of a sampling method for the isolation of head kidney macrophages from fish at the pond-side. J Fish Dis 23(4):289–293
Dalmo RA, Ingebrigtsen K, Bogwald J (1997) Non-specific defence mechanisms in fish, with particular reference to the reticuloendothelial system (RES). J Fish Dis 20(4):241–273
Dawar FU, Hu X, Zhao L, Dong X, Xiong Y, Zhou M, Lin L (2017) Transcriptomic analysis reveals differentially expressed genes and a unique apoptosis pathway in channel catfish ovary cells after infection with the channel catfish virus. Fish Shellfish Immun 71:58–68
Eicher SD, Mckee CA, Carroll JA, Pajor EA (2006) Supplemental vitamin C and yeast cell wall beta-glucan as growth enhancers in newborn pigs and as immunomodulators after an endotoxin challenge after weaning. J Anim Sci 84(9):2352–2360
Fang FC (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2(10):820–832
Ferreira IMPLVO, Pinho O, Vieira E, Tavarela JG (2010) Brewer’s Saccharomyces yeast biomass: characteristics and potential applications. Trends Food Sci Technol 21:77–84
Goodridge HS, Wolf AJ, Underhill DM (2009) Beta-glucan recognition by the innate immune system. Immunol Rev 230(1):38–50
Hai NV (2015) Research findings from the use of probiotics in tilapia aquaculture: a review. Fish Shellfish Immun 45:592–597
Harikrishnan R, Kim JS, Balasundaram C, Heo MS (2012) Dietary supplementation with chitin and chitosan on haematology and innate immune response in Epinephelus bruneus against Philasterides dicentrarchi. Exp Parasitol 131(1):116–124
Jarmołowicz S, Rożyński M, Kowalska A, Zakęś Z (2018) Growth in juvenile pikeperch ( Sander lucioperca L.) stimulated with yeast, Saccharomyces cerevisiae, extract. Aquac Res 49(2):614–620
Joerink M, Ribeiro CM, Stet RJ, Hermsen T, Savelkoul HF, Wiegertjes GF (2006) Head kidney-derived macrophages of common carp (Cyprinus carpio L.) show plasticity and functional polarization upon differential stimulation. J Immunol 177:61–69
Kogan G (2000) (1→3,1→6)-β-D-glucans of yeasts and fungi and their biological activity. Stud Nat Prod Chem 23:107–152
Kollar R, Reinhold BB, Petrakova E, Yeh HJC, Ashwell G, Drgonova J, Cabib E (1997) Architecture of the yeast cell wall. J Biol Chem 28:17762–17775
Lee CG, Da Silva CA, Lee J, Hartl D, Elias JA (2008) Chitin regulation of immune responses: an old molecule with new roles. Curr Opin Immunol l20 20:684–689
Liu L, Zhou Y, Zhao X, Wang H, Wang L, Yuan G, Lin L (2014) Oligochitosan stimulated phagocytic activity of macrophages from blunt snout bream (Megalobrama amblycephala) associated with respiratory burst coupled with nitric oxide production. Dev Comp Immunol l47 47(1):17–24
Liu Z, Liu S, Yao J, Bao L, Zhang J, Li Y, Waldbieser GC (2016) The channel catfish genome sequence provides insights into the evolution of scale formation in teleosts. Nat Commun 7:11757
Macmicking J, Xie QW, Nathan C (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15:323–350
Meena DK, Das P, Kumar S, Mandal SC, Prusty AK, Singh SK, Mukherjee SC (2013) Beta-glucan: an ideal immunostimulant in aquaculture (a review). Fish Physiol Biochem 39(3):431–457
Natalia H, André F, Luana S, Jaqueline B, Leonardo S (2017) Dietary carbohydrates and protein of yeast modulate the early stages of innate immune response in tilapia (Oreochromis niloticus) primarily after LPS inoculation. Aquac Int 25:755–776
Nguyen TH, Fleet GH, Rogers PL (1998) Composition of the cell walls of several yeast species. Appl Microbiol Biotechnol 50:206–212
Øverland M, Skrede A (2017) Yeast derived from lignocellulosic biomass as a sustainable feed resource for use in aquaculture. J Sci Food Agric 97(3):733–742
Pietretti D, Vera-Jimenez NI, Hoole WGF (2013) Oxidative burst and nitric oxide responses in carp macrophages induced by zymosan, MacroGard (R) and selective Dectin-1 agonists suggest recognition by multiple pattern recognition receptors. Fish Shellfish Immun 35(3):847–857
Refstie S, Baeverfjord G, Seim RR, Elvebø O (2010) Effects of dietary yeast cell wall β-glucans and MOS on performance, gut health, and salmon lice resistance in Atlantic salmon (Salmo salar) fed sunflower and soybean meal. Aquaculture 305:109–116
Rieger AM, Barreda DR (2011) Antimicrobial mechanisms of fish leukocytes. Dev Comp Immunol l35 35:1238–1245
Rodrı’guez I, Chamorro R, Novoa B, Figueras A (2009) β-Glucan administration enhances disease resistance and some innate immune responses in zebrafish (Danio rerio). Fish Shellfish Immun 27:369–373
Secombes CJ (1990) Isolation of salmonid macrophages and analysis of their killing activity. In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, Muiswinkel WB (eds) Techniques in fish immunology. SOS Publications, NJ, pp 138–154
Secombes CJ, Stolen JS, Fletcher TC, Anderson DP, Robertsen BS (1990) Isolation of salmonid macrophages and analysis of their killing activity. Techniques in Fish Immunology 1:137–155
Shurson GC (2018) Yeast and yeast derivatives in feed additives and ingredients: sources, characteristics, animal responses, and quantification methods. Anim Feed Sci Technol 235:60–76
Soltanian S, Dhont J, Sorgeloos P, Bossier P (2007) Influence of different yeast cell-wall mutants on performance and protection against pathogenic bacteria (Vibrio campbellii) in gnotobiotically-grown Artemia. Fish Shellfish Immun 23(1):141–153
Takahashi KG, Izumi-Nakajima N, Mori K (2017) Unique phagocytic properties of hemocytes of Pacific oyster Crassostrea gigas against yeast and yeast cell-wall derivatives. Fish Shellfish Immun 70:575–582
Wang Y, Tian Y, Shao J, Shu X, Jia J, Ren X, Guan Y (2018) Macrophage immunomodulatory activity of the polysaccharide isolated from Collybia radicata mushroom. Int J Biol Macromol 108:300–306
Yu HH, Han F, Xue M, Wang J, Tacon P, Zheng YH, Wu XF, Zhang YJ (2014) Efficacy and tolerance of yeast cell wall as an immunostimulant in the diet of Japanese seabass (Lateolabrax japonicus). Aquaculture 432:217–224
Zhao HG, Li C, Beck BH, Zhang R, Tongda W, Davis DA, Peatmana E (2015a) Impact of feed additives on surface mucosal health and columnaris susceptibility in channel catfish fingerlings, Ictalurus punctatus. Fish Shellfish Immun 46(2):624–637
Zhao X, Liu L, Hegazyc AM, Wang H, Li J, Lin L (2015b) Mannose receptor mediated phagocytosis of bacteria in macrophages of blunt snout bream (Megalobrama amblycephala) in a Ca2+-dependent manner. Fish Shellfish Immun 43(2):357–363
We thank the International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript.
This work was funded by the Science and Technology Project of Hubei Province Department of Education (B2018076), the Open Research Project from Key Laboratory of Fishery Drug Development Ministry of Agriculture (201505), the Introduction Talent Research Start-up Fund of Wuhan Polytechnic University (2016284), and the Wuhan Polytechnic University Scientific Research Project (201740).
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Zhou, J., Gao, Z., Wang, W. et al. Yeast cell walls stimulate viability, respiratory burst, and phagocytosis in channel catfish (Ictalurus punctatus) head-kidney macrophages. Aquacult Int 27, 1655–1665 (2019). https://doi.org/10.1007/s10499-019-00417-y
- Yeast cell wall
- Channel catfish
- Head-kidney macrophage
- Respiratory burst