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Cell Stress and Chaperones

, Volume 18, Issue 5, pp 661–665 | Cite as

Butyric acid retention in gingival tissue induces oxidative stress in jugular blood mitochondria

  • Marni E. Cueno
  • Kenichi Imai
  • Noriko Matsukawa
  • Takamitsu Tsukahara
  • Tomoko Kurita-Ochiai
  • Kuniyasu Ochiai
Short Communication

Abstract

Butyric acid (BA) is a major extracellular metabolite produced by anaerobic periodontopathic bacteria and is commonly deposited in the gingival tissue. BA induces mitochondrial oxidative stress in vitro; however, its effects in vivo were never elucidated. Here, we determined the effects of butyric acid retention in the gingival tissues on oxidative stress induction in the jugular blood mitochondria. We established that BA injected in the rat gingival tissue has prolonged retention in gingival tissues. Blood taken at 0, 60, and 180 min after BA injection was used for further analysis. We isolated blood mitochondria, verified its purity, and measured hydrogen peroxide (H2O2), heme, superoxide (SOD), and catalase (CAT) to determine BA effects. We found that H2O2, heme, SOD, and CAT levels all increased after BA injection. This would insinuate that mitochondrial oxidative stress was induced ascribable to BA.

Keywords

Butyric acid Gingival tissue Mitochondria Rat blood Reactive oxygen species homeostasis 

Notes

Acknowledgments

This work was supported by the Dental Research Center-Nihon University School of Dentistry and funded by the Sato Fund-Nihon University School of Dentistry and both the Ministry of Health, Labor and Welfare and the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan through the Strategic Research Base Development Program for Private Universities 2010–2014 (S1001024).

References

  1. Ajioka RS, Phillips JD, Kushner JP (2006) Biosynthesis of heme in mammals. Biochim Biophys Acta 1763:723–736PubMedCrossRefGoogle Scholar
  2. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341PubMedCrossRefGoogle Scholar
  3. Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82:1227–1238Google Scholar
  4. Balla J, Balla G, Jeney V, Kakuk G, Jacob HS, Vercellotti GM (2000) Ferriporphyrins and endothelium: a 2-edged sword-promotion of oxidation and induction of cytoprotectants. Blood 95:3442–3450PubMedGoogle Scholar
  5. Bhandari V, Maulik N, Kresch M (2000) Hyperoxia causes an increase in antioxidant enzyme activity in adult and fetal rat type II pneumocytes. Lung 178:53–60PubMedCrossRefGoogle Scholar
  6. Brandes RP (2005) Triggering mitochondrial radical release: a new function for NADPH oxidases. Hypertension 45:847–848PubMedCrossRefGoogle Scholar
  7. Chandra J, Samali A, Orrenius S (2000) Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 29:323–333PubMedCrossRefGoogle Scholar
  8. Chen Y, Zychlinsky A (1994) Apoptosis induced by bacterial pathogens. Microb Pathog 17:203–212PubMedCrossRefGoogle Scholar
  9. Daiber A (2010) Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim Biophys Acta 1797:897–906PubMedCrossRefGoogle Scholar
  10. Du YY, Wang PC, Chen J, Song CP (2008) Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana. J Integr Plant Biol 50:1318–1326PubMedCrossRefGoogle Scholar
  11. Giorgio M, Trinei M, Migliaccio E, Pelicci PG (2007) Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol 8:722–728PubMedCrossRefGoogle Scholar
  12. Hasan RN, Schafer AI (2008) Hemin upregulates Egr-1 expression in vascular smooth muscle cells via reactive oxygen species ERK-1/2-Elk-1 and NF-kappaB. Circ Res 102:42–50PubMedCrossRefGoogle Scholar
  13. Hu S, Dong TS, Dalal SR, Wu F, Bissonnette M, Kwon JH, Chang EB (2011) The microbe-derived short chain fatty acid butyrate targets miRNA-dependent p21 gene expression in human colon cancer. PLoS One 6:e16221PubMedCrossRefGoogle Scholar
  14. Imai K, Ochiai K, Okamoto T (2009) Reactivation of latent HIV-1 infection by the periodontopathic bacterium Porphyromonas gingivalis involves histone modification. J Immunol 182:3688–3695PubMedCrossRefGoogle Scholar
  15. Imai K, Inoue H, Tamura M, Cueno ME, Takeichi O, Kusama K, Saito I, Ochiai K (2012) The periodontal pathogen Porphyromonas gingivalis induces the Epstein-Barr virus lytic switch transactivator ZEBRA by histone modification. Biochimie 94:839–846PubMedCrossRefGoogle Scholar
  16. Kurita-Ochiai T, Ochiai K (2010) Butyric acid induces apoptosis via oxidative stress in Jurkat T-cells. J Dent Res 89:689–694PubMedCrossRefGoogle Scholar
  17. Kurita-Ochiai T, Fukushima K, Ochiai K (1997) Butyric acid-induced apoptosis of murine thymocytes, splenic T cells, and human Jurkat T cells. Infect Immun 65:35–41PubMedGoogle Scholar
  18. Kurita-Ochiai T, Ochiai K, Fukushima K (1998) Volatile fatty acid, metabolic by-product of periodontopathic bacteria, induces apoptosis in WEHI 231 and RAJI B lymphoma cells and splenic B cells. Infect Immun 66:2587–2594PubMedGoogle Scholar
  19. Kurita-Ochiai T, Fukushima K, Ochiai K (1999) Lipopolysaccharide stimulates butyric acid-induced apoptosis in human peripheral blood mononuclear cells. Infect Immun 67:22–29PubMedGoogle Scholar
  20. Kurita-Ochiai T, Amano S, Fukushima K, Ochiai K (2003) Cellular events involved in butyric acid-induced T cell apoptosis. J Immunol 171:3576–3584PubMedGoogle Scholar
  21. Kurita-Ochiai T, Seto S, Suzuki N, Yamamoto M, Otsuka K, Abe K, Ochiai K (2008) Butyric acid induces apoptosis in inflamed fibroblasts. J Dent Res 87:51–55PubMedCrossRefGoogle Scholar
  22. Liu B, Chen Y, St Clair DK (2008) ROS and p53: a versatile partnership. Free Radic Biol Med 44:1529–1535PubMedCrossRefGoogle Scholar
  23. Louis P, Young P, Holtrop G, Flint HJ (2010) Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ Microbiol 12:304–314PubMedCrossRefGoogle Scholar
  24. MacMillan-Crow LA, Crow JP, Thompson JA (1998) Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 37:1613–1622PubMedCrossRefGoogle Scholar
  25. Margolis HC, Duckworth JH, Moreno EC (1988) Composition and buffer capacity of pooled starved plaque fluid from caries-free and caries-susceptible individuals. J Dent Res 67:1476–1482PubMedCrossRefGoogle Scholar
  26. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, Schilter HC, Rolph MS, Mackay F, Artis D, Xavier RJ, Teixeira MM, Mackay CR (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461:1282–1286PubMedCrossRefGoogle Scholar
  27. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  28. Ponka P (1997) Tissue-specific regulation of iron metabolism and heme synthesis: distinct control mechanisms in erythroid cells. Blood 89:1–25PubMedGoogle Scholar
  29. Ponka P (1999) Cell biology of heme. Am J Med Sci 318:241–256PubMedCrossRefGoogle Scholar
  30. Radi R, Cassina A, Hodara R, Quijano C, Castro L (2002) Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33:1451–1464PubMedCrossRefGoogle Scholar
  31. Sasaki A, Yamada T, Inoue K, Momoi T, Tokunaga H, Sakiyama K, Kanegae H, Suda N, Amano O (2011) Localization of heat shock protein 27 (hsp27) in the rat gingiva and its changes with tooth eruption. Acta Histochem Cytochem 44:17–24PubMedCrossRefGoogle Scholar
  32. Scandalios JG (2002) The rise of ROS. Trends Biochem Sci 27:483–486PubMedCrossRefGoogle Scholar
  33. Socransky SS, Haffajee AD (1991) Microbial mechanisms in the pathogenesis of destructive periodontal diseases: a critical assessment. J Periodontal Res 26:195–212PubMedCrossRefGoogle Scholar
  34. Soder PO, Jin LJ, Soder B (1993) DNA probe detection of periodontopathogens in advanced periodontitis. Scand J Dent Res 101:363–370PubMedGoogle Scholar
  35. Squier CA (1991) The permeability of oral mucosa. Crit Rev Oral Biol Med 2:13–32PubMedGoogle Scholar
  36. Suzuki YJ, Forman HJ, Sevanian A (1997) Oxidants as stimulators of signal transduction. Free Radic Biol Med 22:269–285PubMedCrossRefGoogle Scholar
  37. Takada Y, Hachiya M, Park SH, Osawa Y, Ozawa T, Akashi M (2002) Role of reactive oxygen species in cells overexpressing manganese superoxide dismutase: mechanism for induction of radioresistance. Mol Cancer Res 1:137–146PubMedGoogle Scholar
  38. Teng YT, Taylor GW, Scannapieco F, Kinane DF, Curtis M, Beck JD, Kogon S (2002) Periodontal health and systemic disorders. J Can Dent Assoc 68:188–192PubMedGoogle Scholar
  39. Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378PubMedCrossRefGoogle Scholar
  40. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160:1–40PubMedCrossRefGoogle Scholar
  41. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84PubMedCrossRefGoogle Scholar
  42. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40:235–243PubMedCrossRefGoogle Scholar
  43. Zitomer RS, Lowry CV (1992) Regulation of gene expression by oxygen in Saccharomyces cerevisiae. Microbiol Rev 56:1–11PubMedGoogle Scholar

Copyright information

© Cell Stress Society International 2013

Authors and Affiliations

  • Marni E. Cueno
    • 1
  • Kenichi Imai
    • 1
  • Noriko Matsukawa
    • 2
  • Takamitsu Tsukahara
    • 2
  • Tomoko Kurita-Ochiai
    • 3
  • Kuniyasu Ochiai
    • 1
  1. 1.Department of Microbiology, Division of Immunology and Pathobiology, Dental Research CenterNihon University School of DentistryTokyoJapan
  2. 2.Kyoto Institute of Nutrition and Pathology Inc.KyotoJapan
  3. 3.Department of Microbiology and ImmunologyNihon University School of Dentistry at MatsudoMatsudoJapan

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