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The oral immunogenicity of BioProtein, a bacterial single-cell protein, is affected by its particulate nature

Published online by Cambridge University Press:  07 June 2007

Hanne R. Christensen*
Affiliation:
BioCentrum-DTU, Section for Biochemistry and Nutrition, Technical University of Denmark, DK-2800 Lyngby, Denmark
Linea C. Larsen
Affiliation:
BioCentrum-DTU, Section for Biochemistry and Nutrition, Technical University of Denmark, DK-2800 Lyngby, Denmark
Hanne Frøkiær
Affiliation:
BioCentrum-DTU, Section for Biochemistry and Nutrition, Technical University of Denmark, DK-2800 Lyngby, Denmark
*
*Corresponding author: Dr Hanne R. Christensen, fax +45 45 88 63 07, email hrc@biocentrum.dtu.dk
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Abstract

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The bacterial single-cell protein BioProtein (BP; Norferm Danmark, Odense, Denmark), produced by fermentation of natural gas with methanotrophic bacteria, is a potential protein source for man and animals. For human consumption, removal of the nucleic acid is necessary. Preliminary studies have shown that ingested BP induces a specific immune response. The objective of the present study was to characterize the type of response, its development over time and product-related causative factors. Mice were fed with diets containing 60 g nucleic acid-reduced BP/kg, 240 g nucleic acid-reduced BP/kg, 240 g untreated BP (basic BP)/kg or 240 g casein/kg (control). In another study, mice were fed 240 g basic BP/kg, whole cell-free BP-culture homogenate or control diet. The immune response was monitored using an ELISA for BP-specific immunoglobulin in blood and BP-specific immunoglobulin A in blood and saliva. Ingested BP induced a steady specific mucosal and systemic immune response, characterized by a dose-dependent production of immunoglobulin and immunoglobulin A in blood and immunoglobulin A in saliva. Basic BP and nucleic acid-reduced BP induced identical responses. However, feeding mice BP-culture homogenate induced immunoglobulin A in saliva but there was no systemic response. The antibodies from BP-fed mice cross-reacted with BP-culture homogenate revealing the presence of the same antigenic components in the two products despite the different oral immunogenicity. Thus, ingestion of BP induces a persistent mucosal and systemic immune response of which the systemic response can be avoided by ingesting a BP preparation free of whole cells. This indicates the importance of the non-particulate constitution of single-cell protein products intended for human or animal consumption.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2003

References

Ahmed, T, Sumazaki, R, Nagai, Y, Shibasaki, M & Takita, H (1997) Immune response to food antigens: Kinetics of food-specific antibodies in the normal population. Acta Paediatr Jpn 39, 322328.CrossRefGoogle ScholarPubMed
Anupama, & Ravindra, P (2000) Value-added food: Single cell protein. Biotechnol Adv 18, 459479.CrossRefGoogle ScholarPubMed
Barkholt, V & Jensen, AL (1989) Amino-acid analysis – determination of cystein plus half-cystein in proteins after hydrochloric-acid hydrolysis with a disulfide compound as additive. Anal Biochem 177, 318322.CrossRefGoogle ScholarPubMed
Barnes, RMR, Johnson, PM, Harvey, MM, Blears, J & Finn, R (1988) Human-serum antibodies reactive with dietary proteins – IgG subclass distribution. Int Arch Allergy Appl Immunol 87, 184188.CrossRefGoogle ScholarPubMed
Brandtzaeg, P (1998) Development and basic mechanisms of human gut immunity. Nutr Rev 56, S5S18.CrossRefGoogle ScholarPubMed
Coombs, RRA, Kieffer, M, Fraser, DR & Frazier, PJ (1983) Naturally developing antibodies to wheat gliadin fractions and to other cereal antigens in rabbits, rats and guinea-pigs on normal laboratory diets. Int Arch Allergy Appl Immunol 70, 200204.CrossRefGoogle ScholarPubMed
Dahlgren, UIH, Wold, AE, Hanson, LA & Midtvedt, T (1991) Expression of a dietary-protein in Echerichia coli renders it strongly antigenic to gut lymphoid-tissue. Immunology 73, 394397.Google Scholar
Dannaeus, A (1993) Age-related antibody response to food antigens. Pediatr Allergy Immunol 4(Suppl. 3), 2124.CrossRefGoogle ScholarPubMed
Ermak, TH & Giannasca, PJ (1998) Microparticle targeting to M cells. Adv Drug Deliv Rev 34, 261283.CrossRefGoogle ScholarPubMed
Fjellbirkeland, A, Kleivdal, H, Joergensen, C, Thestrup, H & Jensen, HB (1997) Outer membrane proteins of Methylococcus capsulatus (Bath). Arch Microbiol 168, 128135.CrossRefGoogle ScholarPubMed
Fujihashi, K, Kweon, MN, Kiyono, H, VanCott, JL, vanGinkel, FW, Yamamoto, M & McGhee, JR (1997) A T cell/B cell epithelial cell internet for mucosal inflammation and immunity. Springer Semin Immunopathol 18, 477494.CrossRefGoogle Scholar
Goding, JW (1996) In The Antibody Response. 3rd ed., London: Academic Press.CrossRefGoogle Scholar
Haman, L, El-Samalouti, V, Ulmer, AJ, Flad, H-D & Rietschel, ET (1998) Components of gut bacteria as immunomodulators. Int J Microbiol 41, 141154.CrossRefGoogle Scholar
Husby, S, Oxelius, VA, Teisner, B, Jensenius, JC & Svehag, SE (1985) Humoral immunity to dietary antigens in healthy adults – occurrence, isotype and IgG subclass distribution of serum antibodies to protein antigens. Int Arch Allergy Appl Immunol 77, 416422.CrossRefGoogle ScholarPubMed
Jenkins, PG, Howard, KA, Blackhall, NW, Thomas, NW, Davis, SS & O'Hagan, DT (1994) Microparticulate absorption from the rat intestine. J Control Release 29, 339350.CrossRefGoogle Scholar
Kerr, MA & Loomes, LM (1994) Properties of immunoglobulins. In Immunochemistry Labfax. pp 2342. [Kerr, MA and Thorpe, R, editors]. Oxford: Bios Scientific Publishers.CrossRefGoogle Scholar
Khoury, SJ, Lider, O, Alsabbagh, A & Weiner, HL (1990) Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin basic-protein. 3. Synergistic effect of lipopolysaccharide. Cell Immunol 131, 302310.CrossRefGoogle Scholar
Kim, SM, Enomoto, A, Hachimura, S, Yamauchi, K & Kaminogawa, S (1993) Serum antibody-response elicited by a casein diet is directed to only limited determinants of alpha-s1-casein. Int Arch Allergy Immunol 101, 260265.CrossRefGoogle ScholarPubMed
Kuhad, RC, Singh, A, Tripathi, KK, Saxena, RK & Eriksson, KEL (1997) Microorganisms as an alternative source of protein. Nutr Rev 55, 6575.CrossRefGoogle ScholarPubMed
Larsen, J & Joergensen, L (1996) Reduction of RNA and DNA in Methylococcus capsulatus by endogenous nucleases. Appl Microbiol Biotechnol 45, 137140.CrossRefGoogle ScholarPubMed
Macpherson, AJ, Hunziker, L, McCoy, K & Lamarre, A (2001) IgA responses in the intestinal mucosa against pathogenic and non-pathogenic microorganisms. Microbes Infect 3, 10211035.CrossRefGoogle ScholarPubMed
Matsunaga, Y, Wakatsuki, Y, Tabata, Y, Kawasaki, H, Usui, T, Yoshida, M, Itoh, T, Habu, S & Kita, T (2000) Oral immunization with size-purified microsphere beads as a vehicle selectively induces systemic tolerance and sensitization. Vaccine 19, 579588.CrossRefGoogle ScholarPubMed
Medzhitov, R & Janeway, C (2000) Innate immune recognition: mechanisms and pathways. Immunol Rev 173, 8997.CrossRefGoogle ScholarPubMed
Moeremans, M, Daneels, G & Demey, J (1985) Sensitive colloidal metal (gold or silver) staining of protein blots on nitrocellulose membranes. Anal Biochem 145, 315321.CrossRefGoogle ScholarPubMed
Mølck, A-M, Poulsen, M, Christensen, HR, Lauridsen, TS & Madsen, C (2002) Immunotoxicity of nucleic acid reduced BioProtein – a bacterial derived single cell protein – in Wistar rats. Toxicology 174, 183200.CrossRefGoogle ScholarPubMed
Nakase, H, Okazaki, K, Tabata, Y, et al. (2001) Rectal immunization with antigen-containing microspheres induces stronger Th2 responses than oral immunization: a new method for vaccination. Vaccine 20, 377384.CrossRefGoogle ScholarPubMed
O'Hagan, DT, Palin, K, Davis, SS, Artursson, P & Sjoholm, I (1989) Microparticles as potentially orally active immunological adjuvants. Vaccine 7, 421424.CrossRefGoogle ScholarPubMed
Pulendran, B, Kumar, P, Cutler, CW, Mohamadzadeh, M, Van Dyke, T & Banchereau, J (2001) Lipopolysaccharides from distinct pathogens induce different classes of immune responses in vivo. J Immunol 167, 50675076.CrossRefGoogle ScholarPubMed
Rumbo, M, Chirdo, FG, Anon, MC & Fossati, CA (1998) Detection and characterization of antibodies specific to food antigens (gliadin, ovalbumin and beta-lactoglobulin) in human serum, saliva, colostrum and milk. Clin Exp Immunol 112, 453458.CrossRefGoogle ScholarPubMed
Schagger, H & vonJagow, G (1987) Tricine sodium dodecyl-sulfate polyacrylamide-gel electrophoresis for the separation of proteins in the range from 1-KDa to 100-KDa. Anal Biochem 166, 368379.CrossRefGoogle Scholar
Scrimshaw, NS & Murray, EB (1995) Nutritional value and safety of single cell protein. In Enzymes, Biomass and Feed, pp 221237. [Reed, G and Nagodawithana, TW, editors]. Weinham: VCH.CrossRefGoogle Scholar
Strobel, S & Mowat, AM (1998) Immune responses to dietary antigens: oral tolerance. Immunol Today 19, 173181.CrossRefGoogle ScholarPubMed
Strober, W & Coffman, RL (1997) Tolerance and immunity in the mucosal immune system – Introduction. Res Immunol 148, 489490.CrossRefGoogle ScholarPubMed
Tabata, Y, Inoue, Y & Ikada, Y (1996) Size effect on systemic and mucosal immune responses induced by oral administration of biodegradable microspheres. Vaccine 14, 16771685.CrossRefGoogle ScholarPubMed
Whittenbury, R & Krieg, NR (1984) Methylococcaceae. In Bergey's Manual of Systemic Bacteriology, pp 256261. [Krieg, NR and Holt, JG, editors]. Baltimore, MD: Williams and Wilkins.Google Scholar
Wold, AE, Dahlgren, UIH, Hanson, LA, Mattsbybaltzer, I & Midvetdt, T (1989) Difference between bacterial and food antigens in mucosal immunogenicity. Infect Immun 57, 26662673.CrossRefGoogle ScholarPubMed