Oral mucosal lipids are antibacterial against Porphyromonas gingivalis, induce ultrastructural damage, and alter bacterial lipid and protein compositions

Carol L Fischer , Katherine S Walters , David R Drake , Deborah V Dawson , Derek R Blanchette , Kim A Brogden , Philip W Wertz

International Journal of Oral Science ›› 2013, Vol. 5 ›› Issue (3) : 130 -140.

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International Journal of Oral Science ›› 2013, Vol. 5 ›› Issue (3) : 130 -140. DOI: 10.1038/ijos.2013.28
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Oral mucosal lipids are antibacterial against Porphyromonas gingivalis, induce ultrastructural damage, and alter bacterial lipid and protein compositions

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Abstract

Researchers in the USA have identified five naturally occurring molecules that kill bacteria responsible for periodontal disease. The molecules are part of the diverse but sparsely documented countermeasures that the body uses to fight oral pathogens. Led by Philip Wertz and Carol Fischer of the University of Iowa, the researchers characterized the effects of naturally secreted lipids known as sphingoid bases and short-chain fatty acids, which are toxic to many bacteria, on Porphyromonas gingivalis, a key contributor to periodontitis. The two particularly potent molecules that they identified, phytosphingosine and sapienic acid, both killed this bacterium by inflicting severe damage to its outer membrane. Since these lipids are produced by the body and active at physiological concentrations, they may offer a safe and effective alternative to antibiotics for fighting P. gingivalis infection.

Keywords

antimicrobial lipid / fatty acid / Porphyromonas gingivalis / sphingoid base / sphingolipid / ultrastructure

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Carol L Fischer, Katherine S Walters, David R Drake, Deborah V Dawson, Derek R Blanchette, Kim A Brogden, Philip W Wertz. Oral mucosal lipids are antibacterial against Porphyromonas gingivalis, induce ultrastructural damage, and alter bacterial lipid and protein compositions. International Journal of Oral Science, 2013, 5(3): 130-140 DOI:10.1038/ijos.2013.28

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References

[1]

Berglundh T, Donati M. Aspects of adaptive host response in periodontitis. J Clin Periodontol, 2005, 32(6 Suppl): 87-107.

[2]

Eke PI, Dye BA, Wei L. Prevalence of periodontitis in adults in the United States: 2009 and 2010. J Dent Res, 2012, 91(10): 914-920.

[3]

Socransky SS, Haffajee AD. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol, 1992, 63(4 Suppl): 322-331.

[4]

Socransky SS, Haffajee AD, Cugini MA. Microbial complexes in subgingival plaque. J Clin Periodontol, 1998, 25(2): 134-144.

[5]

Hutter G, Schlagenhauf U, Valenza G. Molecular analysis of bacteria in periodontitis: evaluation of clone libraries, novel phylotypes and putative pathogens. Microbiology, 2003, 149(Pt 1): 67-75.

[6]

Kolenbrander PE, Andersen RN, Blehert DS. Communication among oral bacteria. Microbiol Mol Biol Rev, 2002, 66(3): 486-505.

[7]

Holt SC, Kesavalu L, Walker S. Virulence factors of Porphyromonas gingivalis. Periodontol 2000, 1999, 20: 168-238.

[8]

Gorr SU. Antimicrobial peptides in periodontal innate defense. Front Oral Biol, 2012, 15: 84-98.

[9]

Gorr SU. Antimicrobial peptides of the oral cavity. Periodontol 2000, 2009, 51: 152-180.

[10]

Bibel DJ, Aly R, Shah S. Sphingosines: antimicrobial barriers of the skin. Acta Derm Venereol, 1993, 73(6): 407-411.

[11]

Drake DR, Brogden KA, Dawson DV. Thematic review series: skin lipids. Antimicrobial lipids at the skin surface. J Lipid Res, 2008, 49(1): 4-11.

[12]

Brasser A, Barwacz C, Bratt CL. Free sphingosine in human saliva. J Dent Res, 2011, 90(Spec A): 3465.

[13]

Brasser AJ, Barwacz CA, Dawson DV. Presence of wax esters and squalene in human saliva. Arch Oral Biol, 2011, 56(6): 588-591.

[14]

Law SL, Squier CA, Wertz PW. Free sphingosines in oral epithelium. Comp Biochem Physiol B Biochem Mol Biol, 1995, 110(3): 511-513.

[15]

Law S, Wertz PW, Swartzendruber DC. Regional variation in content, composition and organization of porcine epithelial barrier lipids revealed by thin-layer chromatography and transmission electron microscopy. Arch Oral Biol, 1995, 40(12): 1085-1091.

[16]

Smith KR, Thiboutot DM. Thematic review series: skin lipids. Sebaceous gland lipids: friend or foe. J Lipid Res, 2008, 49(2): 271-281.

[17]

Zouboulis CC. Acne and sebaceous gland function. Clin Dermatol, 2004, 22(5): 360-366.

[18]

Zouboulis CC, Baron JM, Bohm M. Frontiers in sebaceous gland biology and pathology. Exp Dermatol, 2008, 17(6): 542-551.

[19]

Bergsson G, Steingrimsson O, Thormar H. Bactericidal effects of fatty acids and monoglycerides on Helicobacter pylori. Int J Antimicrob Agents, 2002, 20(4): 258-262.

[20]

Bergsson G, Arnfinnsson J, Steingrimsson O. Killing of Gram-positive cocci by fatty acids and monoglycerides. APMIS, 2001, 109(10): 670-678.

[21]

Burtenshaw JM. The mechanism of self-disinfection of the human skin and its appendages. J Hyg (Lond), 1942, 42(2): 184-210.

[22]

Bibel DJ, Aly R, Shinefield HR. Antimicrobial activity of sphingosines. J Invest Dermatol, 1992, 98(3): 269-273.

[23]

Kalfa VC, Jia HP, Kunkle RA. Congeners of SMAP29 kill ovine pathogens and induce ultrastructural damage in bacterial cells. Antimicrob Agents Chemother, 2001, 45(11): 3256-3261.

[24]

Bratt CL, Kohlgraf KG, Yohnke K. Communication: antimicrobial activity of SMAP28 with a targeting domain for Porphyromonas gingivalis. Probiotics Antimicrob Proteins, 2010, 2(1): 21-25.

[25]

Weistroffer PL, Joly S, Srikantha R. SMAP29 congeners demonstrate activity against oral bacteria and reduced toxicity against oral keratinocytes. Oral Microbiol Immunol, 2008, 23(2): 89-95.

[26]

Brogden KA, Kalfa VC, Ackermann MR. The ovine cathelicidin SMAP29 kills ovine respiratory pathogens in vitro and in an ovine model of pulmonary infection. Antimicrob Agents Chemother, 2001, 45(1): 331-334.

[27]

Drake DR, Wiemann AH, Rivera EM. Bacterial retention in canal walls in vitro: effect of smear layer. J Endod, 1994, 20(2): 78-82.

[28]

Wertz PW, Swartzendruber DC, Madison KC. Composition and morphology of epidermal cyst lipids. J Invest Dermatol, 1987, 89(4): 419-425.

[29]

Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem, 1957, 226(1): 497-509.

[30]

Wertz PW, Downing DT. Free sphingosines in porcine epidermis. Biochim Biophys Acta, 1989, 1002(2): 213-217.

[31]

Weerheim A, Ponec M. Determination of stratum corneum lipid profile by tape stripping in combination with high-performance thin-layer chromatography. Arch Dermatol Res, 2001, 293(4): 191-199.

[32]

Mun J, Onorato A, Nichols FC. Structural confirmation of the dihydrosphinganine and fatty acid constituents of the dental pathogen Porphyromonas gingivalis. Org Biomol Chem, 2007, 5(23): 3826-3833.

[33]

Nichols FC, Riep B, Mun J. Structures and biological activities of novel phosphatidylethanolamine lipids of Porphyromonas gingivalis. J Lipid Res, 2006, 47(4): 844-853.

[34]

Nichols FC, Riep B, Mun J. Structures and biological activity of phosphorylated dihydroceramides of Porphyromonas gingivalis. J Lipid Res, 2004, 45(12): 2317-2330.

[35]

Nichols FC. Novel ceramides recovered from Porphyromonas gingivalis: relationship to adult periodontitis. J Lipid Res, 1998, 39(12): 2360-2370.

[36]

Conover WJ . Practical nonparametric Statistics. 3rd ed. New York: Wiley, 1999.

[37]

Dawson DV, Siegler IC. Approaches to the nonparametric analysis of limited longitudinal data sets. Exp Aging Res, 1996, 22(1): 33-57.

[38]

Ghosh M, Grizzle J, Sen PK. Nonparametric methods in longitudinal studies. J Am Stat Assoc, 1973, 68(341): 29-36.

[39]

Mansheim BJ, Coleman SE. Immunochemical differences between oral and nonoral strains of Bacteroides asaccharolyticus. Infect Immun, 1980, 27(2): 589-596.

[40]

Mayrand D, Holt SC. Biology of asaccharolytic black-pigmented Bacteroides species. Microbiol Rev, 1988, 52(1): 134-152.

[41]

Parent R, Mouton C, Lamonde L. Human and animal serotypes of Bacteroides gingivalis defined by crossed immunoelectrophoresis. Infect Immun, 1986, 51(3): 909-918.

[42]

McBain AJ, Ledder RG, Sreenivasan P. Selection for high-level resistance by chronic triclosan exposure is not universal. J Antimicrob Chemother, 2004, 53(5): 772-777.

[43]

do Amorim CV, Aun CE, Mayer MP. Susceptibility of some oral microorganisms to chlorhexidine and paramonochlorophenol. Braz Oral Res, 2004, 18(3): 242-246.

[44]

Fischer CL, Drake DR, Dawson DV. Antibacterial activity of sphingoid bases and fatty acids against Gram-positive and Gram-negative bacteria. Antimicrob Agents Chemother, 2012, 56(3): 1157-1161.

[45]

Fischer CL, Walters KS, Drake DR. Sphingoid bases are taken up by Escherichia coli and Staphylococcus aureus and induce ultrastructural damage. Skin Pharmacol Physiol, 2013, 26(1): 36-44.

[46]

Khulusi S, Ahmed HA, Patel P. The effects of unsaturated fatty acids on Helicobacter pylori in vitro. J Med Microbiol, 1995, 42(4): 276-282.

[47]

Brogden KA, De Lucca AJ, Bland J. Isolation of an ovine pulmonary surfactant-associated anionic peptide bactericidal for Pasteurella haemolytica. Proc Natl Acad Sci U S A, 1996, 93(1): 412-416.

[48]

Harder J, Bartels J, Christophers E. Isolation and characterization of human beta -defensin-3, a novel human inducible peptide antibiotic. J Biol Chem, 2001, 276(8): 5707-5713.

[49]

Shimoda M, Ohki K, Shimamoto Y. Morphology of defensin-treated Staphylococcus aureus. Infect Immun, 1995, 63(8): 2886-2891.

[50]

Brogden K. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria. Nat Rev Microbiol, 2005, 3(3): 238-250.

[51]

Desbois AP, Smith VJ. Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol, 2010, 85(6): 1629-1642.

[52]

Saito H, Tomioka H, Yoneyama T. Growth of group IV mycobacteria on medium containing various saturated and unsaturated fatty acids. Antimicrob Agents Chemother, 1984, 26(2): 164-169.

[53]

Kabara JJ, Conley AJ, Truant JP. Relationship of chemical structure and antimicrobial activity of alkyl amides and amines. Antimicrob Agents Chemother, 1972, 2(6): 492-498.

[54]

Zheng CJ, Yoo JS, Lee TG. Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Lett, 2005, 579(23): 5157-5162.

[55]

Willett NP, Morse GE. Long-chain fatty acid inhibition of growth of Streptococcus agalactiae in a chemically defined medium. J Bacteriol, 1966, 91(6): 2245-2250.

[56]

Galbraith H, Miller TB, Paton AM. Antibacterial activity of long chain fatty acid and the reversal with calcium, magnesium, ergocalciferol and cholesterol. J Appl Bacteriol, 1971, 34(4): 803-813.

[57]

Shelburne CE, Gleason RM, Coulter WA. Differential display analysis of Porphyromonas gingivalis gene activation response to heat and oxidative stress. Oral Microbiol Immunol, 2005, 20(4): 233-238.

[58]

Amano A, Sharma A, Sojar HT. Effects of temperature stress on expression of fimbriae and superoxide dismutase by Porphyromonas gingivalis. Infect Immun, 1994, 62(10): 4682-4685.

[59]

Vayssier C, Mayrand D, Grenier D. Detection of stress proteins in Porphyromonas gingivalis and other oral bacteria by Western immunoblotting analysis. FEMS Microbiol Lett, 1994, 121(3): 303-307.

[60]

Lu B, McBride BC. Stress response of Porphyromonas gingivalis. Oral Microbiol Immunol, 1994, 9(3): 166-173.

[61]

Percival RS, Marsh PD, Devine DA. Effect of temperature on growth, hemagglutination, and protease activity of Porphyromonas gingivalis. Infect Immun, 1999, 67(4): 1917-1921.

[62]

Murakami Y, Masuda T, Imai M. Analysis of major virulence factors in Porphyromonas gingivalis under various culture temperatures using specific antibodies. Microbiol Immunol, 2004, 48(8): 561-569.

[63]

Bonass WA, Marsh PD, Percival RS. Identification of ragAB as a temperature-regulated operon of Porphyromonas gingivalis W50 using differential display of randomly primed RNA. Infect Immun, 2000, 68(7): 4012-4017.

[64]

Lopatin DE, Jaramillo E, Edwards CA. Cellular localization of a Hsp90 homologue in Porphyromonas gingivalis. FEMS Microbiol Lett, 1999, 181(1): 9-16.

[65]

Meuric V, Gracieux P, Tamanai-Shacoori Z. Expression patterns of genes induced by oxidative stress in Porphyromonas gingivalis. Oral Microbiol Immunol, 2008, 23(4): 308-314.

[66]

Vanterpool E, Aruni AW, Roy F. regT can modulate gingipain activity and response to oxidative stress in Porphyromonas gingivalis. Microbiology, 2010, 156(Pt 10): 3065-3072.

[67]

Dashper SG, Ang CS, Veith PD. Response of Porphyromonas gingivalis to heme limitation in continuous culture. J Bacteriol, 2009, 191(3): 1044-1055.

[68]

Hosogi Y, Duncan MJ. Gene expression in Porphyromonas gingivalis after contact with human epithelial cells. Infect Immun, 2005, 73(4): 2327-2335.

[69]

Brogden KA, Drake DR, Dawson DV. Antimicrobial lipids of the skin and oral mucosa. // Dayan N, Wertz PW. Innate immune system of skin and oral mucosa, 2011 Hoboken: John Wiley & Sons, Inc 75-81.

[70]

Bratt CL, Dawson D, Drake D. Oral mucosal lipids: antibacterial activity and induction of ultrastructural damage. J Dent Res, 2010, 89(Spec A): 679.

[71]

Hosea Blewett HJ, Cicalo MC, Holland CD. The immunological components of human milk. Adv Food Nutr Res, 2008, 54: 45-80.

[72]

Field CJ. The immunological components of human milk and their effect on immune development in infants. J Nutr, 2005, 135(1): 1-4.

[73]

Wille JJ, Kydonieus A. Palmitoleic acid isomer (C16:1delta6) in human skin sebum is effective against Gram-positive bacteria. Skin Pharmacol Appl Skin Physiol, 2003, 16(3): 176-187.

[74]

Takigawa H, Nakagawa H, Kuzukawa M. Deficient production of hexadecenoic acid in the skin is associated in part with the vulnerability of atopic dermatitis patients to colonization by Staphylococcus aureus. Dermatology, 2005, 211(3): 240-248.

[75]

Arikawa J, Ishibashi M, Kawashima M. Decreased levels of sphingosine, a natural antimicrobial agent, may be associated with vulnerability of the stratum corneum from patients with atopic dermatitis to colonization by Staphylococcus aureus. J Invest Dermatol, 2002, 119(2): 433-439.

[76]

Strandvik B, Gronowitz E, Enlund F. Essential fatty acid deficiency in relation to genotype in patients with cystic fibrosis. J Pediatr, 2001, 139(5): 650-655.

[77]

Freedman SD, Blanco PG, Zaman MM. Association of cystic fibrosis with abnormalities in fatty acid metabolism. N Engl J Med, 2004, 350(6): 560-569.

[78]

Georgel P, Crozat K, Lauth X. A Toll-like receptor 2-responsive lipid effector pathway protects mammals against skin infections with gram-positive bacteria. Infect Immun, 2005, 73(8): 4512-4521.

[79]

Thormar H, Hilmarsson H. The role of microbicidal lipids in host defense against pathogens and their potential as therapeutic agents. Chem Phys Lipids, 2007, 150(1): 1-11.

[80]

Anon. Undecylenic acid. Monograph. Altern Med Rev 2002; 7( 1): 68–70.

[81]

Shapiro AL, Rothman S. August 1945: undecylenic acid in the treatment of dermatomycosis. Arch Dermatol, 1983, 119(4): 345-350.

[82]

Thormar H, Bergsson G, Gunnarsson E. Hydrogels containing monocaprin have potent microbicidal activities against sexually transmitted viruses and bacteria in vitro. Sex Transm Infect, 1999, 75(3): 181-185.

[83]

Neyts J, Kristmundsdottir T, de Clercq E. Hydrogels containing monocaprin prevent intravaginal and intracutaneous infections with HSV-2 in mice: impact on the search for vaginal microbicides. J Med Virol, 2000, 61(1): 107-110.

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