Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: Implications of probiotics in acne vulgaris

Applied Microbiology and Biotechnology

Volumn 98, Issue 1, 2014, Pages 411-424

  Wang, Yanhan ^a   Kuo, Sherwin ^a   Shu, Muya ^a   Yu, Jinghua ^b   Huang, Stephen ^c   Dai, Ashley ^a   Two, Aimee ^a   Gallo, Richard L ^a   Huang, Chun Ming ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BURNHAM INSTITUTE   (United States)

^c Surface Bioadvances Inc   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Acne; Fermentation; P. acnes; Probiotic; S. epidermidis; Skin microbiome

Indexed keywords

FATTY ACIDS; FERMENTATION; GLYCEROL; MAMMALS; NUCLEAR MAGNETIC RESONANCE; PROBIOTICS;

ACNE; EPIDERMIDIS; MICROBIOME; P. ACNES; PROBIOTIC;

BACTERIA;

GLYCEROL; PROBIOTIC AGENT; SHORT CHAIN FATTY ACID; SUCCINIC ACID;

BIOCHEMISTRY; FERMENTATION; FUNCTIONAL ROLE; GROWTH RATE; GROWTH REGULATOR; HOMEOSTASIS; INHIBITION; MICROBIAL COMMUNITY; PATHOGEN; PROBIOTICS; PUBLIC HEALTH; SKIN; SKIN DISORDER;

ACNE VULGARIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIUM COLONY; DISEASE COURSE; FERMENTATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROBIOME; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROPIONIBACTERIUM ACNES; SKIN DISEASE; SKIN FLORA; STAPHYLOCOCCUS EPIDERMIDIS;

ACNE VULGARIS; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBIOSIS; DNA, BACTERIAL; FERMENTATION; GLYCEROL; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PROBIOTICS; PROPIONIBACTERIUM ACNES; SEQUENCE ANALYSIS, DNA; SKIN; STAPHYLOCOCCUS EPIDERMIDIS; SUCCINIC ACID;

EID: 84891846289     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5394-8     Document Type: Article

References (64)

1. Blank-Porat D, Gruss-Fischer T, Tarasenko N, Malik Z, Nudelman A, Rephaeli A (2007) The anticancer prodrugs of butyric acid AN-7 and AN-9, possess antiangiogenic properties. Cancer Lett 256(1):39-48. doi: 10.1016/j.canlet. 2007.05.011
2. Burtenshaw JM (1942) The mechanism of self-disinfection of the human skin and its appendages. J Hyg (Lond) 42(2):184-210
3. Chakravortty D, Koide N, Kato Y, Sugiyama T, Mu MM, Yoshida T, Yokochi T (2000) The inhibitory action of butyrate on lipopolysaccharide-induced nitric oxide production in RAW 264.7 murine macrophage cells. J Endotoxin Res 6(3):243-7
4. Chitarra LG, Breeuwer P, Van Den Bulk RW, Abee T (2000) Rapid fluorescence assessment of intracellular pH as a viability indicator of Clavibacter michiganensis subsp. michiganensis. J Appl Microbiol 88(5):809-16
5. Chow V, Nong G, St John FJ, Rice JD, Dickstein E, Chertkov O, Bruce D, Detter C, Brettin T, Han J, Woyke T, Pitluck S, Nolan M, Pati A, Martin J, Copeland A, Land ML, Goodwin L, Jones JB, Ingram LO, Shanmugam KT, Preston JF (2012) Complete genome sequence of Paenibacillus sp. strain JDR-2. Stand Genomic Sci 6(1):1-10. doi: 10.4056/sigs.2374349 sigs.2374349
6. Cogen AL, Yamasaki K, Sanchez KM, Dorschner RA, Lai Y, MacLeod DT, Torpey JW, Otto M, Nizet V, Kim JE, Gallo RL (2010) Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J Invest Dermatol 130(1):192-200. doi: 10.1038/jid.2009.243
7. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336(6086):1255-62. doi: 10.1126/science.1224203
8. Cove JH, Holland KT, Cunliffe WJ (1983) Effects of oxygen concentration on biomass production, maximum specific growth rate and extracellular enzyme production by three species of cutaneous propionibacteria grown in continuous culture. J Gen Microbiol 129(11):3327-34
9. Demaerel P, Van Hecke P, Van Oostende S, Baert AL, Jaeken J, Declercq PE, Eggermont E, Plets C (1994) Bacterial metabolism shown by magnetic resonance spectroscopy. Lancet 344(8931):1234-5
10. Dudley R (2004) Ethanol, fruit ripening, and the historical origins of human alcoholism in primate frugivory. Integr Comp Biol 44(4):315-23. doi: 10.1093/icb/44.4.315
11. Fitz-Gibbon S, Tomida S, Chiu BH, Nguyen L, Du C, Liu M, Elashoff D, Erfe MC, Loncaric A, Kim J, Modlin RL, Miller JF, Sodergren E, Craft N, Weinstock GM, Li H (2013) Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J Invest Dermatol 133(9):2152-60. doi: 10.1038/jid.2013.21jid201321
12. Fluhr JW, Darlenski R, Surber C (2008) Glycerol and the skin: holistic approach to its origin and functions. Br J Dermatol 159(1):23-34. doi: 10.1111/j.1365-2133.2008.08643.x
13. Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN, Pace NR (2010) The human nasal microbiota and Staphylococcus aureus carriage. PLoS One 5(5):e10598. doi: 10.1371/journal.pone.0010598
14. Fujimura KE, Slusher NA, Cabana MD, Lynch SV (2010) Role of the gut microbiota in defining human health. Expert Rev Anti Infect Ther 8(4):435-54. doi: 10.1586/eri.10.14
15. Gorbach SL, Mayhew JW, Bartlett JG, Thadepalli H, Onderdonk AB (1976) Rapid diagnosis of anaerobic infections by direct gas-liquid chromatography of clinical speciments. J Clin Invest 57(2):478-84. doi: 10.1172/JCI108300
16. Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9(4):244-53. doi: 10.1038/nrmicro2537
17. Haider A, Shaw JC (2004) Treatment of acne vulgaris. JAMA 292(6):726-35. doi: 10.1001/jama.292.6.726 292/6/726
18. Huang CP, Liu YT, Nakatsuji T, Shi Y, Gallo RR, Lin SB, Huang CM (2008) Proteomics integrated with Escherichia coli vector-based vaccines and antigen microarrays reveals the immunogenicity of a surface sialidase-like protein of Propionibacterium acnes. Proteomics Clin Appl 2(9):1234-45. doi: 10.1002/prca.200780103
19. Imahiyerobo-Ip JI, Dinulos JG (2011) Changing the topography of acne with topical medications. Curr Opin Pediatr 23(1):121-5. doi: 10.1097/MOP. 0b013e3283425457
20. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, Agata T, Mizunoe Y (2010) Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465(7296):346-9. doi: 10.1038/nature09074
21. Ji G, Beavis R, Novick RP (1997) Bacterial interference caused by autoinducing peptide variants. Science 276(5321):2027-30
22. Kanikkannan N, Kandimalla K, Lamba SS, Singh M (2000) Structure-activity relationship of chemical penetration enhancers in transdermal drug delivery. Curr Med Chem 7(6):593-608
23. Karaki S, Mitsui R, Hayashi H, Kato I, Sugiya H, Iwanaga T, Furness JB, Kuwahara A (2006) Short-chain fatty acid receptor, GPR43, is expressed by enteroendocrine cells and mucosal mast cells in rat intestine. Cell Tissue Res 324(3):353-60. doi: 10.1007/s00441-005-0140-x
24. Kim J (2005) Review of the innate immune response in acne vulgaris: activation of Toll-like receptor 2 in acne triggers inflammatory cytokine responses. Dermatology 211(3):193-8. doi: 10.1159/000087011
25. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111-20. doi: 10.1007/BF01731581
26. Kligman AM (1974) An overview of acne. J Invest Dermatol 62(3):268-87
27. Layton AM, Dreno B, Gollnick HP, Zouboulis CC (2006) A review of the European Directive for prescribing systemic isotretinoin for acne vulgaris. J Eur Acad Dermatol Venereol 20(7):773-6. doi: 10.1111/j.1468-3083.2006.01671.x
28. Lemon KP, Armitage GC, Relman DA, Fischbach MA (2012) Microbiota-targeted therapies: an ecological perspective. Sci Transl Med 4(137):137rv5. doi: 10.1126/scitranslmed.3004183
29. Levine RM, Rasmussen JE (1983) Intralesional corticosteroids in the treatment of nodulocystic acne. Arch Dermatol 119(6):480-1
30. Lindh JM, Terenius O, Faye I (2005) 16S rRNA gene-based identification of midgut bacteria from field-caught Anopheles gambiae sensu lato and A. funestus mosquitoes reveals new species related to known insect symbionts. Appl Environ Microbiol 71(11):7217-23. doi: 10.1128/AEM.71.11.7217-7223.2005
31. Liu PF, Nakatsuji T, Zhu W, Gallo RL, Huang CM (2011) Passive immunoprotection targeting a secreted CAMP factor of Propionibacterium acnes as a novel immunotherapeutic for acne vulgaris. Vaccine 29(17):3230-8. doi: 10.1016/j.vaccine.2011.02.036
32. Lo CW, Lai YK, Liu YT, Gallo RL, Huang CM (2011) Staphylococcus aureus hijacks a skin commensal to intensify its virulence: immunization targeting beta-hemolysin and CAMP factor. J Invest Dermatol 131(2):401-9. doi: 10.1038/jid.2010.319
33. Marino C, Stoughton RB (1982) Clinical use of a selective culture medium for wild and antibiotic-resistant Propionibacterium acnes. J Am Acad Dermatol 6(5):902-8. doi: 10.1016/S0190-9622(82)80124-2
34. Martin-Pelaez S, Costabile A, Hoyles L, Rastall RA, Gibson GR, La Ragione RM, Woodward MJ, Mateu E, Martin-Orue SM (2010) Evaluation of the inclusion of a mixture of organic acids or lactulose into the feed of pigs experimentally challenged with Salmonella typhimurium. Vet Microbiol 142(3-4):337-45. doi: 10.1016/j.vetmic.2009.09.061
35. Menon S, Bharadwaj R, Chowdhary AS, Kaundinya DV, Palande DA (2007) Rapid identification of non-sporing anaerobes using nuclear magnetic resonance spectroscopy and an identification strategy. Indian J Med Microbiol 25(4):330-5
36. Moon SH, Roh HS, Kim YH, Kim JE, Ko JY, Ro YS (2012) Antibiotic resistance of microbial strains isolated from Korean acne patients. J Dermatol 39(10):833-7. doi: 10.1111/j.1346-8138.2012.01626.x
37. Moss CW, Dowell VR Jr, Lewis VJ, Schekter MA (1967) Cultural characteristics and fatty acid composition of Corynebacterium acnes. J Bacteriol 94(5):1300-5
38. Nagy I, Pivarcsi A, Koreck A, Szell M, Urban E, Kemeny L (2005) Distinct strains of Propionibacterium acnes induce selective human beta-defensin-2 and interleukin-8 expression in human keratinocytes through toll-like receptors. J Invest Dermatol 124(5):931-8. doi: 10.1111/j.0022-202X.2005.23705.x
39. Nakatsuji T, Liu YT, Huang CP, Zoubouis CC, Gallo RL, Huang CM (2008a) Antibodies elicited by inactivated propionibacterium acnes-based vaccines exert protective immunity and attenuate the IL-8 production in human sebocytes: relevance to therapy for acne vulgaris. J Invest Dermatol 128(10):2451-7. doi: 10.1038/jid.2008.117
40. Nakatsuji T, Liu YT, Huang CP, Zouboulis CC, Gallo RL, Huang CM (2008b) Vaccination targeting a surface sialidase of P. acnes: implication for new treatment of acne vulgaris. PLoS One 3(2):e1551
41. Nakatsuji T, Shi Y, Zhu W, Huang CP, Chen YR, Lee DY, Smith JW, Zouboulis CC, Gallo RL, Huang CM (2008c) Bioengineering a humanized acne microenvironment model: proteomics analysis of host responses to Propionibacterium acnes infection in vivo. Proteomics 8(16):3406-15. doi: 10.1002/pmic.200800044
42. Nakatsuji T, Tang DC, Zhang L, Gallo RL, Huang CM (2011) Propionibacterium acnes CAMP factor and host acid sphingomyelinase contribute to bacterial virulence: potential targets for inflammatory acne treatment. PLoS One 6(4):e14797. doi: 10.1371/journal.pone.0014797
43. Nicoll TR, Jensen MM (1987) Staphylococcosis of turkeys. 5. Large-scale control programs using bacterial interference. Avian Dis 31(1):85-8
44. Nishijima S, Kurokawa I, Katoh N, Watanabe K (2000) The bacteriology of acne vulgaris and antimicrobial susceptibility of Propionibacterium acnes and Staphylococcus epidermidis isolated from acne lesions. J Dermatol 27(5):318-23
45. Ostling CE, Lindgren SE (1993) Inhibition of enterobacteria and Listeria growth by lactic, acetic and formic acids. J Appl Bacteriol 75(1):18-24
46. Otto M (2009) Staphylococcus epidermidis - the 'accidental' pathogen. Nat Rev Microbiol 7(8):555-67. doi: 10.1038/nrmicro2182
47. Park JS, Lee EJ, Lee JC, Kim WK, Kim HS (2007) Anti-inflammatory effects of short chain fatty acids in IFN-gamma-stimulated RAW 264.7 murine macrophage cells: involvement of NF-kappaB and ERK signaling pathways. Int Immunopharmacol 7(1):70-7. doi: 10.1016/j.intimp.2006.08.015
48. Ricke SC (2003) Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult Sci 82(4):632-9
49. Rigo M, Alegre RM (2004) Isolation and selection of phenol-degrading microorganisms from industrial wastewaters and kinetics of the biodegradation. Folia Microbiol (Praha) 49(1):41-5
50. Ryssel H, Kloeters O, Germann G, Schafer T, Wiedemann G, Oehlbauer M (2009) The antimicrobial effect of acetic acid - an alternative to common local antiseptics? Burns 35(5):695-700. doi: 10.1016/j.burns.2008.11.009
51. Scanlan PD, Buckling A, Kong W, Wild Y, Lynch SV, Harrison F (2012) Gut dysbiosis in cystic fibrosis. J Cyst Fibros 11(5):454-5. doi: 10.1016/j.jcf.2012.03.007 S1569-1993(12)00046-X
52. Schroder O, Opritz J, Stein J (2000) Substrate and inhibitor specificity of butyrate uptake in apical membrane vesicles of the rat distal colon. Digestion 62(2-3):152-8
53. Sebastian S, Phillip LE, Fellner V, Idziak ES (1996) Comparative assessment of bacterial inoculation and propionic acid treatment of aerobic stability and microbial populations of ensiled high-moisture ear corn. J Anim Sci 74(2):447-56
54. Shinefield HR, Ribble JC, Boris M (1971) Bacterial interference between strains of Staphylococcus aureus, 1960 to 1970. Am J Dis Child 121(2):148-52
55. Shu M, Wang Y, Yu J, Kuo S, Coda A, Jiang Y, Gallo RL, Huang CM (2013) Fermentation of Propionibacterium acnes, a commensal bacterium in the human skin microbiome, as skin probiotics against methicillin-resistant Staphylococcus aureus. PLoS One 8(2):e55380. doi: 10.1371/journal.pone
56. Sivakanesan R, Dawes EA (1980) Anaerobic glucose and serine metabolism in Staphylococcus epidermidis. J Gen Microbiol 118(1):143-57
57. Stein J, Zores M, Schroder O (2000) Short-chain fatty acid (SCFA) uptake into Caco-2 cells by a pH-dependent and carrier mediated transport mechanism. Eur J Nutr 39(3):121-5
58. Uckay I, Dinh A, Vauthey L, Asseray N, Passuti N, Rottman M, Biziragusenyuka J, Riche A, Rohner P, Wendling D, Mammou S, Stern R, Hoffmeyer P, Bernard L (2010) Spondylodiscitis due to Propionibacterium acnes: report of twenty-nine cases and a review of the literature. Clin Microbiol Infect 16(4):353-8. doi: 10.1111/j.1469-0691.2009.02801
59. Ushijima T, Takahashi M, Ozaki Y (1984) Acetic, propionic, and oleic acid as the possible factors influencing the predominant residence of some species of Propionibacterium and coagulase-negative Staphylococcus on normal human skin. Can J Microbiol 30(5):647-52
60. Vinolo MA, Rodrigues HG, Nachbar RT, Curi R (2011) Regulation of inflammation by short chain fatty acids. Nutrients 3(10):858-76. doi: 10.3390/nu3100858
61. Wei W, Cao Z, Zhu YL, Wang X, Ding G, Xu H, Jia P, Qu D, Danchin A, Li Y (2006) Conserved genes in a path from commensalism to pathogenicity: comparative phylogenetic profiles of Staphylococcus epidermidis RP62A and ATCC12228. BMC Genomics 7:112. doi: 10.1186/1471-2164-7-112
62. Whitehead SS, Leavitt RW, Jensen MM (1993) Staphylococcosis of turkeys. 6. Development of penicillin resistance in an interfering strain of Staphylococcus epidermidis. Avian Dis 37(2):536-41
63. Wilkinson DM, Jensen MM (1987) Staphylococcosis of turkeys. 4. Characterization of a bacteriocin produced by an interfering Staphylococcus. Avian Dis 31(1):80-4
64. Zheng X, Bollinger Bollag W (2003) Aquaporin 3 colocates with phospholipase d2 in caveolin-rich membrane microdomains and is downregulated upon keratinocyte differentiation. J Invest Dermatol 121(6):1487-95. doi: 10.1111/j.1523-1747.2003.12614