Antibody Production by B Cells
There are several studies investigating the effect of Spirulina on the antibody production by B cells in response to immunization (primary immune response) and challenge (secondary immune response) with a specific antigen. In the earliest of these studies, mice were fed diets containing 10% or 20% of S. platensis, immunized with sheep red blood cells after 7 weeks, and challenged after 9 weeks.8 Spirulina feeding significantly increased the number of IgM antibody-producing cells in the spleen during the primary immune response, but had little effect on the synthesis of IgG antibodies during the secondary immune response. As discussed previously, this study suffers from the lack of adjustment for the higher protein and essential nutrient content of the Spirulina-supplemented diets.
In contrast, another group of researchers reported that Spirulina enhanced antigen-specific antibody production during the secondary, but not the primary, immune response.6 In their experiments, newly hatched chicks received diets containing between 10 and 10,000 ppm of Spirulina for 3 or 7 weeks. Significantly higher antigen-specific antibody production (IgM and IgG) was seen at all dose levels of Spirulina in the strain treated for 7 weeks. In another strain supplemented for only 3 weeks, there was a significant increase in antigen-specific IgG only at the highest dose level (10,000 ppm).
Another study examined whether a hot water extract of S. platensis could affect experimental food allergy.28 Note that the previous data from these investigators suggest that hot water extracts contain less protein and possibly higher concentrations of polysaccharides compared to whole Spirulina.8 One group of mice received S. platensis one of two concentrations of the extract in their drinking water before they were immunized with, and then orally exposed to, shrimp extract. Another group was given Spirulina extract concomitantly with immunization and antigen stimulation. Concurrent Spirulina treatment did not significantly affect total and antigen-specific IgE concentrations in serum, indicating that it did not enhance the allergic response to this food antigen.28 At the higher dose, Spirulina treatment significantly enhanced total serum levels of IgG1, the most common subclass of IgG, whereas the increase in antigen-specific IgG1 did not reach statistical significance. It also resulted in significantly greater total, but not antigen-specific, IgA levels in the intestinal contents. IgA is the antibody associated with mucosal surfaces. Since these are the major entry sites for many bacteria and viruses, secretory IgA is of central importance in the protection against these pathogens by preventing their adherence to, and penetration of, the epithelium, neutralizing toxins, and preventing viral multiplication.
In mice that received Spirulina extract before immunization and stimulation with shrimp antigens, IgA and IgG1 antibody production was examined in various lymphoid tissues.28 Animals supplemented with the higher dose of Spirulina exhibited a marked increase in total, but not antigen-specific, IgA in the spleen and mesenteric lymph nodes, whereas such an increase was not observed in Peyer's patches. Mesenteric lymph nodes are the lymphatics of the colon, while Peyer's patches are lymph nodes in the intestinal wall near the junction of the ileum and colon. In contrast, total and antigen-specific IgG1 production in spleen and mesenteric lymph nodes did not differ significantly between supplemented and unsupplemented animals. These findings further underscore the ability of Spirulina to enhance the production of protective IgA antibodies overall without increasing the antigen-specific IgA response.
When mice were fed with a crude polysaccharide fraction of Spirulina for at least 4 days, cultured Peyer's patch cells isolated from these animals secreted significantly higher levels of IgA, and these levels were further increased after an additional day of supplementation.36 The synthesis of IL-6 was also markedly increased in these cultures and the time course paralleled that of IgA production. This is consistent with the known ability of this cytokine to induce IgA synthesis in B cells. These findings suggest that polysaccharides participate in the stimulation of nonantigen-specific IgA production.
The effects of phycocyanin on antibody production have also been examined. Six weeks of supplementation with phycocyanin in the drinking water, resulting in a daily intake of ~57.5 mg/kg, was associated with an eightfold increase of antigen-specific IgA in Peyer's patches in response to immunization and rechallenge with ovalbumin (OVA).29 Antigen-specific IgA was not seen in mesenteric lymph nodes of immunized animals that did not receive phycocyanin, but was markedly induced in mesenteric lymph nodes of supplemented animals. In the intestinal mucosa, treatment with phycocyanin substantially increased both total and OVA-specific IgA, whereas only the enhancement of total IgA reached statistical significance in the spleen. Splenic antigen-specific, but not total, IgG1 synthesis was significantly augmented in phycocyanin-treated animals. As had been observed with the hot water extract of whole Spirulina, supplementation with phycocyanin for 6 weeks did not significantly alter the antigen-specific IgE and IgG1 levels. Interestingly, when another strain of mice was supplemented for 6 weeks, the same results were obtained. However, extending the treatment with phycocyanin over a period of 8 weeks resulted in marked reduction in serum concentrations of OVA-specific IgE and IgG1. The levels of total and antigen-specific IgA in the intestinal mucosa were not affected by extended treatment.
Together, these results suggest that neither Spirulina nor its polysaccharides nor phycocyanin significantly affect the induction of antigen-specific IgE, suggesting little potential to increase allergic sensitization. All three fractions are able to markedly enhance total, but not antigen-specific IgA levels. This is likely to provide increased protection from invading pathogens.
In vitro, a hot-water extract of S. platensis dose dependently induced the proliferation of mouse spleen cells, but not thymus cells.8 Together with the observation that the Spirulina extract enhanced macrophage functions, including phagocytosis and IL-1 production, these results suggested that Spirulina did not affect T cell function directly, but through activation of macrophages. In the same investigation, spleen cells from mice fed diets containing 10% or 20% Spirulina extract also exhibited significantly increased proliferation in response to T-cell mitogens, but not to a B-cell mitogen. Similarly, dietary supplementation of newly hatched chicks with Spirulina for 7 weeks significantly enhanced T lymphocyte proliferation at the highest dose provided (10,000 ppm), but not at 10 or 100 ppm.6 No significant effect on lymphoproliferation was seen in another strain of chicks supplemented for 3 weeks only.
Dietary administration of a crude polysaccharide fraction of Spirulina significantly augmented the secretion of INF-y by spleen cells starting 3 days after the beginning of supplementation, with further incremental increases seen after one and two additional days.36 The cellular source was not determined but is likely to be T cells or NK cells.
Spirulina and the Generation of Immune Cells (Hematopoiesis)
It was recently shown that a hot water extract of S. platensis, phycocyanin, and a cell wall extract (presumably containing mostly polysaccharides) all induced proliferation in bone marrow cells.37 When spleen or peritoneal-exudate cells were incubated with these extracts, the culture supernatants induced colony formation in bone marrow cells. Each colony represents the progeny of a single precursor or stem cell. This ability seemed to be at least partly attributable to the induction of granulocyte-macrophage colony-stimulating factor (GM-CSF) and IL-3. Serum and supernatant from cultures of lymphoid organs obtained from mice that had been orally treated with the different Spirulina extracts also induced significant colony formation in bone marrow cells. Even greater induction was obtained with serum from mice that had received the extracts intraperitoneally. Note, however, that serum from these mice reportedly did not contain detectable levels of GM-CSF or IL-3.
Several different polysaccharide fractions have been isolated from Spirulina, some of them with molecular weights exceeding 10 million Da.14,38 These polysaccharides were shown to exhibit biological activities, such as immunomodulation and enhancement of hematopoiesis, not only in vitro but also after oral administration.36-38 This is consistent with the findings that oral administration of certain mushroom polysaccharides can enhance immune functions and inhibit carcinogenesis.39 Other fungal polysaccharides, however, are ineffective when given orally, although they show significant biological activity after intravenous or intraperitoneal administration. Humans and many animals can digest certain types of polysaccharides into small fragments or even their individual sugar constituents and subsequently absorb these oligo- or monosaccharides. It seems highly unlikely that such small fragments retain any biological activity. Many other plant, fungal, and bacterial polysaccharides are indigestible for humans and many animals because of the lack of the enzymes capable of breaking the types of linkages between individual sugars within these macromolecules.
It had long been thought that the inability to digest polysaccharides would prevent their absorption completely and that they would simply be excreted. The question then arises as to how these polysaccharides exert their effects after oral administration. Several groups of researchers demonstrated that, following the oral intake of some indigestible polysaccharides, fragments as large as 20,000 Da, (approximately 150 monosaccharides) reach the circulation.39 However, the biological activity of polysaccharides in vitro and in vivo frequently declines with decreasing molecular weight,39 as has also been demonstrated for certain activities of a Spirulina polysaccharide fraction.40 An alternative explanation could be that contact between polysaccharides and intestinal epithelial cells or cellular components of the gut-associated lymphoid tissue ultimately results in the priming or activation of other immune cells. These activated cells could subsequently migrate to other tissues and thereby exert systemic immunomodulatory effects.
It also remains to be established how phycocyanin exerts biological activities in vivo since proteins are generally broken down into individual amino acids or small oligopeptides before absorption. The phycocyanobilin chromophore, however, structurally resembles the bile pigment bilirubin, which can be absorbed from any part of the small or large intestine as long as it remains unconjugated. This would suggest that the phycocyanobilin part of phycocyanin is mainly responsible for the antioxidant and anti-inflammatory effects seen after oral administration of phycocyanin. This is supported by the observation that this chromophore accounts for much of the radical scavenging and antioxidant properties of phycocyanin and Spirulina.41
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