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References

  1. Al-Asmakh M, Anuar F, Zadjali F, Rafter J, Pettersson S. 2012. Gut microbial communities modulating brain development and function. Gut Microbes 3: 366-373.
    Pubmed PMC CrossRef
  2. Al-Asmakh M, Stukenborg JB, Reda A, Anuar F, Strand ML, Hedin L, et al. 2014. The gut microbiota and developmental programming of the testis in mice. PLoS One 9: e103809.
    Pubmed PMC CrossRef
  3. Arvidsson C, Hallén A, Bäckhed F. 2012. Generating and analyzing germ-free mice. Curr. Protoc. Mouse Biol. 2: 307-316.
    CrossRef
  4. Bjorkholm B, Bok CM, Lundin A, Rafter J, Hibberd ML, Pettersson S. 2009. Intestinal microbiota regulate xenobiotic metabolism in the liver. PLoS One 4: e6958.
    Pubmed PMC CrossRef
  5. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Toth M, et al. 2014. The gut microbiota influences bloodbrain barrier permeability in mice. Sci. Transl. Med. 6:263ra158.
    Pubmed PMC CrossRef
  6. Brown K, DeCoffe D, Molcan E, Gibson DL. 2012. Dietinduced dysbiosis of the intestinal microbiota and the effects on immunity and disease. Nutrients 4: 1095-1119.
    Pubmed PMC CrossRef
  7. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, et al. 2011. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. USA 108: 3047-3052.
    Pubmed PMC CrossRef
  8. Fritz JV, Desai MS, Shah P, Schneider JG, Wilmes P. 2013. From meta-omics to causality: experimental models for human microbiome research. Microbiome 1: 14.
    Pubmed PMC CrossRef
  9. Goodman AL, Kallstrom G, Faith JJ, Reyes A, Moore A, Dantas G, Gordon JI. 2011. Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc. Natl. Acad. Sci. USA 108: 6252-6257.
    Pubmed PMC CrossRef
  10. Gootenberg DB, Turnbaugh PJ. 2011. Companion animals symposium: humanized animal models of the microbiome. J. Anim. Sci. 89: 1531-1537.
    Pubmed CrossRef
  11. Gordon HA, Pesti L. 1971. The gnotobiotic animal as a tool in the study of host microbial relationships. Bacteriol. Rev. 35: 390-429.
    Pubmed PMC CrossRef
  12. Gustafsson BE. 1959. Lightweight stainless steel systems for rearing germfree animals. Ann. NY Acad. Sci. 78: 17-28.
    Pubmed CrossRef
  13. Hecht G, Bar-Nathan C, Milite G, Alon I, Moshe Y, Greenfeld L, et al. 2014. A simple cage-autonomous method for the maintenance of the barrier status of germ-free mice during experimentation. Lab. Anim. 48: 292-297.
    Pubmed CrossRef
  14. Inzunza J, Midtvedt T, Fartoo M, Norin E, Osterlund E, Persson AK, Ahrlund-Richter L. 2005. Germfree status of mice obtained by embryo transfer in an isolator environment. Lab. Anim. 39: 421-427.
    Pubmed CrossRef
  15. Kostic AD, Howitt MR, Garrett WS. 2013. Exploring hostmicrobiota interactions in animal models and humans. Genes Dev. 27: 701-718.
    Pubmed PMC CrossRef
  16. McVey Neufeld KA, Perez-Burgos A, Mao YK, Bienenstock J, Kunze WA. 2015. The gut microbiome restores intrinsic and extrinsic nerve function in germ-free mice accompanied by changes in calbindin. Neurogastroenterol. Motil. 27: 627-636.
    Pubmed CrossRef
  17. Neufeld KM, Kang N, Bienenstock J, Foster JA. 2011. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol. Motil. 23: 255264, e119.
    Pubmed CrossRef
  18. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. 2012. Host-gut microbiota metabolic interactions. Science 336: 1262-1267.
    Pubmed CrossRef
  19. Nicklas W, Baneux P, Boot R, Decelle T, Deeny AA, Fumanelli M, et al. 2002. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab. Anim. 36: 20-42.
    Pubmed CrossRef
  20. O'Hara AM, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Rep. 7: 688-693.
    Pubmed PMC CrossRef
  21. Rautava S, Luoto R, Salminen S, Isolauri E. 2012. Microbial contact during pregnancy, intestinal colonization and human disease. Nat. Rev. Gastroenterol. Hepatol. 9: 565-576.
    Pubmed CrossRef
  22. Sanz Y. 2011. Gut microbiota and probiotics in maternal and infant health. Am. J. Clin. Nutr. 94: 2000S-2005S.
    Pubmed CrossRef
  23. Shimizu K, Muranaka Y, Fujimura R, Ishida H, Tazume S, Shimamura T. 1998. Normalization of reproductive function in germfree mice following bacterial contamination. Exp. Anim. 47: 151-158.
    Pubmed CrossRef
  24. Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, et al. 2012. The gut microbiota regulates bone mass in mice. J. Bone Miner. Res. 27: 1357-1367.
    Pubmed PMC CrossRef
  25. Smith K, McCoy KD, Macpherson AJ. 2007. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin. Immunol. 19: 59-69.
    Pubmed CrossRef
  26. Sommer F, Backhed F. 2013. The gut microbiota--masters of host development and physiology. Nat. Rev. Microbiol. 11:227-238.
    Pubmed CrossRef
  27. Stepankova R, Tonar Z, Bartova J, Nedorost L, Rossman P, Poledne R, et al. 2010. Absence of microbiota (germ-free conditions) accelerates the atherosclerosis in ApoE-deficient mice fed standard low cholesterol diet. J. Atheroscler. Thromb. 17: 796-804.
    Pubmed CrossRef
  28. Wostmann BS. 1981. The germfree animal in nutritional studies. Annu. Rev. Nutr. 1: 257-279.
    Pubmed CrossRef
  29. Wostmann BS. 1996. Germfree and Gnotobiotic Animal Models:Background and Applications, CRC Press FL, USA.
  30. Yi P, Li L. 2012. The germfree murine animal: an important animal model for research on the relationship between gut microbiota and the host. Vet. Microbiol. 157: 1-7.
    Pubmed CrossRef

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Article

Minireview

J. Microbiol. Biotechnol. 2015; 25(10): 1583-1588

Published online October 28, 2015 https://doi.org/10.4014/jmb.1501.01039

Copyright © The Korean Society for Microbiology and Biotechnology.

Use of Germ-Free Animal Models in Microbiota-Related Research

Maha Al-Asmakh 1, 2* and Fahad Zadjali 3

1Department of Health Sciences, College of Arts and Sciences, Qatar University, P.O. Box 2713, Doha, Qatar, 2Department of Microbiology, Tumor and Cell Biology, Karolinska Institute, 171 77 Stockholm, Sweden, 3College of Medicine and Health Sciences, Sultan Qaboos University, 123 Alkoudh, Oman

Received: January 14, 2015; Accepted: June 2, 2015

Abstract

The large intestine is a home for trillions of microbiota, which confer many benefits on the
host, including production of vitamins, absorption of nutrients, pathogen displacement, and
development of the immune system. For several decades, germ-free animals have been used to
study the interaction between the host and its microbiota. This minireview describes the
technical aspects for establishing and maintaining germ-free animals and highlights the
advantages and disadvantages for germ-free animals as experimental models.

Keywords: Germ-free animals, Germ-free mice, microbiota, Isolator technology

References

  1. Al-Asmakh M, Anuar F, Zadjali F, Rafter J, Pettersson S. 2012. Gut microbial communities modulating brain development and function. Gut Microbes 3: 366-373.
    Pubmed KoreaMed CrossRef
  2. Al-Asmakh M, Stukenborg JB, Reda A, Anuar F, Strand ML, Hedin L, et al. 2014. The gut microbiota and developmental programming of the testis in mice. PLoS One 9: e103809.
    Pubmed KoreaMed CrossRef
  3. Arvidsson C, Hallén A, Bäckhed F. 2012. Generating and analyzing germ-free mice. Curr. Protoc. Mouse Biol. 2: 307-316.
    CrossRef
  4. Bjorkholm B, Bok CM, Lundin A, Rafter J, Hibberd ML, Pettersson S. 2009. Intestinal microbiota regulate xenobiotic metabolism in the liver. PLoS One 4: e6958.
    Pubmed KoreaMed CrossRef
  5. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Toth M, et al. 2014. The gut microbiota influences bloodbrain barrier permeability in mice. Sci. Transl. Med. 6:263ra158.
    Pubmed KoreaMed CrossRef
  6. Brown K, DeCoffe D, Molcan E, Gibson DL. 2012. Dietinduced dysbiosis of the intestinal microbiota and the effects on immunity and disease. Nutrients 4: 1095-1119.
    Pubmed KoreaMed CrossRef
  7. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, et al. 2011. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. USA 108: 3047-3052.
    Pubmed KoreaMed CrossRef
  8. Fritz JV, Desai MS, Shah P, Schneider JG, Wilmes P. 2013. From meta-omics to causality: experimental models for human microbiome research. Microbiome 1: 14.
    Pubmed KoreaMed CrossRef
  9. Goodman AL, Kallstrom G, Faith JJ, Reyes A, Moore A, Dantas G, Gordon JI. 2011. Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc. Natl. Acad. Sci. USA 108: 6252-6257.
    Pubmed KoreaMed CrossRef
  10. Gootenberg DB, Turnbaugh PJ. 2011. Companion animals symposium: humanized animal models of the microbiome. J. Anim. Sci. 89: 1531-1537.
    Pubmed CrossRef
  11. Gordon HA, Pesti L. 1971. The gnotobiotic animal as a tool in the study of host microbial relationships. Bacteriol. Rev. 35: 390-429.
    Pubmed KoreaMed CrossRef
  12. Gustafsson BE. 1959. Lightweight stainless steel systems for rearing germfree animals. Ann. NY Acad. Sci. 78: 17-28.
    Pubmed CrossRef
  13. Hecht G, Bar-Nathan C, Milite G, Alon I, Moshe Y, Greenfeld L, et al. 2014. A simple cage-autonomous method for the maintenance of the barrier status of germ-free mice during experimentation. Lab. Anim. 48: 292-297.
    Pubmed CrossRef
  14. Inzunza J, Midtvedt T, Fartoo M, Norin E, Osterlund E, Persson AK, Ahrlund-Richter L. 2005. Germfree status of mice obtained by embryo transfer in an isolator environment. Lab. Anim. 39: 421-427.
    Pubmed CrossRef
  15. Kostic AD, Howitt MR, Garrett WS. 2013. Exploring hostmicrobiota interactions in animal models and humans. Genes Dev. 27: 701-718.
    Pubmed KoreaMed CrossRef
  16. McVey Neufeld KA, Perez-Burgos A, Mao YK, Bienenstock J, Kunze WA. 2015. The gut microbiome restores intrinsic and extrinsic nerve function in germ-free mice accompanied by changes in calbindin. Neurogastroenterol. Motil. 27: 627-636.
    Pubmed CrossRef
  17. Neufeld KM, Kang N, Bienenstock J, Foster JA. 2011. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol. Motil. 23: 255264, e119.
    Pubmed CrossRef
  18. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. 2012. Host-gut microbiota metabolic interactions. Science 336: 1262-1267.
    Pubmed CrossRef
  19. Nicklas W, Baneux P, Boot R, Decelle T, Deeny AA, Fumanelli M, et al. 2002. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab. Anim. 36: 20-42.
    Pubmed CrossRef
  20. O'Hara AM, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Rep. 7: 688-693.
    Pubmed KoreaMed CrossRef
  21. Rautava S, Luoto R, Salminen S, Isolauri E. 2012. Microbial contact during pregnancy, intestinal colonization and human disease. Nat. Rev. Gastroenterol. Hepatol. 9: 565-576.
    Pubmed CrossRef
  22. Sanz Y. 2011. Gut microbiota and probiotics in maternal and infant health. Am. J. Clin. Nutr. 94: 2000S-2005S.
    Pubmed CrossRef
  23. Shimizu K, Muranaka Y, Fujimura R, Ishida H, Tazume S, Shimamura T. 1998. Normalization of reproductive function in germfree mice following bacterial contamination. Exp. Anim. 47: 151-158.
    Pubmed CrossRef
  24. Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, et al. 2012. The gut microbiota regulates bone mass in mice. J. Bone Miner. Res. 27: 1357-1367.
    Pubmed KoreaMed CrossRef
  25. Smith K, McCoy KD, Macpherson AJ. 2007. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin. Immunol. 19: 59-69.
    Pubmed CrossRef
  26. Sommer F, Backhed F. 2013. The gut microbiota--masters of host development and physiology. Nat. Rev. Microbiol. 11:227-238.
    Pubmed CrossRef
  27. Stepankova R, Tonar Z, Bartova J, Nedorost L, Rossman P, Poledne R, et al. 2010. Absence of microbiota (germ-free conditions) accelerates the atherosclerosis in ApoE-deficient mice fed standard low cholesterol diet. J. Atheroscler. Thromb. 17: 796-804.
    Pubmed CrossRef
  28. Wostmann BS. 1981. The germfree animal in nutritional studies. Annu. Rev. Nutr. 1: 257-279.
    Pubmed CrossRef
  29. Wostmann BS. 1996. Germfree and Gnotobiotic Animal Models:Background and Applications, CRC Press FL, USA.
  30. Yi P, Li L. 2012. The germfree murine animal: an important animal model for research on the relationship between gut microbiota and the host. Vet. Microbiol. 157: 1-7.
    Pubmed CrossRef