β-Glucan successfully stimulated the immune system in different jawed vertebrate species

https://doi.org/10.1016/j.cimid.2018.11.006Get rights and content

Highlights

  • Diets with two β-glucan molecules were examined in four vertebrate species.

  • β-Glucans exhibited different magnitudes of effects on immune responses.

  • β-Glucans promoted immune stimulation in immune responses in all species.

Abstract

Several reports have shown the positive effects of β-glucans on the immune. Howeverthese studies have a broad experimental design including β-glucans compounds. Consequently, a study using the same β-glucan molecule, administration route and experimental design is needed to compare the effects of β-glucan across vertebrate species. For this end, during 28 days we fed four different vertebrate species: mice, dogs, piglets and chicks, with two β-glucan molecules (BG01 and BG02). We measured the serum interleukin 2 as an indicator of innate immune response, the neutrophils and monocytes phagocytosis index as a cellular response and antibody formation as an adaptive response. The results clearly showed that the different β-glucan molecules exhibited biologically differently behaviors, but both molecules stimulate the immune system in a similar pattern in these four species. This finding suggests that vertebrates shared similar mechanisms/patterns in recognizing the β-glucans and confirms the benefits of β-glucans across different vertebrate species.

Introduction

A variety of natural polysaccharides have shown the ability to stimulate the immune system of invertebrate and vertebrate species. Among these compounds, the glucans stand out and their role as a biologically active immunomodulator has been well documented for more than 40 years. ‘Glucans’ is the common name given to a group of polysaccharide polymers, classified based on interchain linkages as either α- or β-linked. They are widely distributed in bacteria, algae, fungi and plants, with different structural types [(see Barsanti et al. [1]]. Their structure is comprised of a main chain of β-(1,3)- and/or β-(1,4)-D-glucopyranosyl units in non-repeating but non-random order, with side chains of varying lengths [2].

Specifically, the β-glucans are the most well-known ‘glucans’ and their benefits have been investigated in a wide range of vertebrates such as humans [3], dogs [4,5], pigs [6], cattle [7], horses [8], sheep [9], chickens [10], frogs [11], fish [12] and invertebrates such as shrimp [13], crab [14], and insects such as bees [15] and drosophila [16]. These benefits include lower stress [17], anti-cancer [18], anti-allergies [19], regulate blood sugar levels [20], prebiotics [21,22], reduce serum cholesterol in hypercholesterolemic animals [23], increase wound healing [24], immune adjuvant [25] and they are extensively used to improve health, growth and general performance in farm animals. In a recent review, Petit and Wiegertjes [26] provided evidence that β-glucans are also able to stimulate a new concept called trained immunity or innate immune memory, which allows macrophages, monocytes, and natural killer cells to show enhanced responsiveness when they reencounter pathogens [27]. In addition, β-glucans have also been successfully used in diverse administration routes such as oral [12], injection or bath [28].

In a review, Soltanian et al. [29] suggested that β-glucan is an immunostimulant that is active across the evolutionary spectrum. Although it is plausible, the studies referred to in the review and also on the current literature did not have the appropriate experimental design to reach this conclusion. The effects of β-glucan are influenced by their molecular weight, degree of branching [2,30], purity, source and extraction process as demonstrated by Pilarski et al. [12]. In addition, the diversity of experimental designs, methods, and administration routes as mentioned before is an aggravating factor for comparing/extrapolating β-glucans’ effects across species. Thus, in this study, we fed four different vertebrate species: mice, dog, piglets and chicks, with two β-glucan molecules (BG01 and BG02) and control diet for 28 days. We measured the serum IL-2 production as an indicator of innate immune response, the neutrophils and monocytes phagocytosis index as a cellular immune response and anti-body production against ovoalbumin as an adaptive immune response. This is the first report of this nature on jawed vertebrates.

Section snippets

Experimental animals and welfare statement

Male and female dogs (average age 2.5 ± 0.5 years, average weight 14.5 ± 2.1 kg, 61% males, and different breeds) were purchased from Marshall Farms, North Rose, NY, USA. Piglets (all white Yorkshire x Landrace; age 3 weeks, average weight 6.3 ± 0.7 kg, 54% males) were obtained from Oak Hill Genetics (Ewing, IL, USA) and leghorn chickens (age 10 days, average weight 65 ± 17.1 g, 50% males) from Hy-Line International, Bryan, TX, USA. All mice used were 8-week-old females of the BALB/c strain

Results

As shown in Table 1, purity of BG01 is 77%, whereas purity of BG02 is 55%. In order to use similar doses of glucan, we used different dose (15 mg/kg or 25 mg/kg) to make the treatments more comparable regard glucan level, since that it is the major active compound. Although it not to be the exactly same glucan level, the small difference between glucan levels in the diet (11.5 mg for BG01 and 13.7 mg for BG02) are really biologically irrelevant and not responsible to trigger the quite different

Discussion

So far, no published study has investigated the effects of β-glucan molecules on different vertebrate species using the same experimental protocol. Here, we show that both β-glucan molecules stimulate four individual immune responses in similar patterns in mice, dogs, piglets and chicks, but with different magnitudes of responses between individual β-glucan samples. Pilarski et al. [12] using the same two β-glucan molecules from this study also showed that the β-glucan samples exhibited

Conclusions

The current literature recognizes more than 31,000 papers that discuss the immunological and other physiological activities of glucans. However, scientific reports directly comparing individual glucans are limited [12,[67], [68], [69]], and a direct comparison of the effects of glucan in several species is completely absent. Therefore, this report is not important because it describes the biological activity of two samples of glucan, but because it is the first report demonstrating that two

Acknowledgments

The authors would like to thank Biorigin for their β-glucan donation and financial support. The funders had no role in the study design, data collection and analysis, or decision to publish. The authors have no competing interests to declare.

References (69)

  • A.H. Kwon et al.

    Effects of medicinal mushroom (Sparassis crispa) on wound healing in streptozotocin-induced diabetic rats

    Am. J. Surg.

    (2009)
  • V. Selvaraj et al.

    Adjuvant and immunostimulatory effects of beta-glucan administration in combination with lipopolysaccharide enhances survival and some immune parameters in carp challenged with Aeromonas hydrophila

    Vet. Immunol. Immunopathol.

    (2006)
  • J. Petit et al.

    Long-lived effects of administering beta-glucans: indications for trained immunity in fish

    Dev. Comp. Immunol.

    (2016)
  • D.A. Przybylska-Diaz et al.

    β-glucan enriched bath directly stimulates the wound healing process in common carp (Cyprinus carpio L.)

    Fish Shellfish Immunol.

    (2013)
  • V. Vetvicka et al.

    Phagocytosis of human blood leukocytes: a simple micromethod

    Immunol. Lett.

    (1982)
  • V. Vetvicka et al.

    Alpha-fetoprotein and phagocytosis in athymic nude mice

    Immunol. Lett.

    (1988)
  • N. Arenas-Ramirez et al.

    Interleukin-2: biology, design and application

    Trends Immunol.

    (2015)
  • S.L. Gaffen et al.

    Overview of interleukin-2 function, production and clinical applications

    Cytokine

    (2004)
  • L. Mo et al.

    Anti-tumor effects of (1--&3)-beta-d-glucan from Saccharomyces cerevisiae in S180 tumor-bearing mice

    Int. J. Biol. Macromol.

    (2017)
  • G. Abel et al.

    Stimulation of human monocyte beta-glucan receptors by glucan particles induces production of TNF-alpha and IL-1 beta

    Int. J. Immunopharmacol.

    (1992)
  • K.L. Chen et al.

    Direct enhancement of the phagocytic and bactericidal capability of abdominal macrophage of chicks by beta-1,3-1,6-glucan

    Poult. Sci.

    (2008)
  • V.K. Lowry et al.

    Purified beta-glucan as an abiotic feed additive up-regulates the innate immune response in immature chickens against Salmonella enterica serovar Enteritidis

    Int. J. Food Microbiol.

    (2005)
  • J.J. Volman et al.

    Dietary modulation of immune function by beta-glucans

    Physiol. Behav.

    (2008)
  • V. Vetvicka et al.

    Orally administered marine (1--&3)-beta-D-glucan Phycarine stimulates both humoral and cellular immunity

    Int. J. Biol. Macromol.

    (2007)
  • I. Suzuki et al.

    Effect of orally administered beta-glucan on macrophage function in mice

    Int. J. Immunopharmacol.

    (1990)
  • C. Tsukada et al.

    Immunopotentiation of intraepithelial lymphocytes in the intestine by oral administrations of beta-glucan

    Cell. Immunol.

    (2003)
  • D.S. Donaldson et al.

    M cell-depletion blocks oral prion disease pathogenesis

    Mucosal Immunol.

    (2012)
  • D.J. Brayden et al.

    Keynote review: intestinal Peyer’s patch M cells and oral vaccine targeting

    Drug Discov. Today

    (2005)
  • P. Kanjan et al.

    Immune effects of β-glucan are determined by combined effects on Dectin-1, TLR2, 4 and 5

    J. Funct. Foods

    (2017)
  • Q. Zhao et al.

    Physicochemical properties and regulatory effects on db/db diabetic mice of beta-glucans extracted from oat, wheat and barley

    Food Hydrocoll.

    (2014)
  • L. Barsanti et al.

    Chemistry, physico-chemistry and applications linked to biological activities of beta-glucans

    Nat. Prod. Rep.

    (2011)
  • E.A. Murphy et al.

    Immune modulating effects of beta-glucan

    Curr. Opin. Clin. Nutr. Metab. Care

    (2010)
  • V. Vetvicka et al.

    Beta(1-3)(1-6)-D-glucans modulate immune status in pigs: potential importance for efficiency of commercial farming

    Ann. Transl. Med.

    (2014)
  • V. Vetvicka et al.

    Β(1-3)(1-6)-D-glucans modulate immune status and blood glucose levels in dogs

    Br. J. Pharm. Res.

    (2014)
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