Vitamin B12 modulates the transcriptome of the skin microbiota in acne pathogenesis

Science Translational Medicine

Volumn 7, Issue 293, 2015, Pages

  Kang, Dezhi ^a   Shi, Baochen ^a   Erfe, Marie C ^b   Craft, Noah ^b   Li, Huiying ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARBOR UCLA MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOCOBALAMIN; PORPHYRIN; RNA; TRANSCRIPTOME;

ACNE; ACNE VULGARIS; ADULT; ARTICLE; BIOSYNTHESIS; CLINICAL ARTICLE; CLINICAL OBSERVATION; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION PROFILING; HUMAN; INFLAMMATION; MALE; METABOLITE; PATHOGENESIS; PRIORITY JOURNAL; PROPIONIBACTERIUM ACNES; PROPIONIBACTERIUM FREUDENREICHII SHERMANII; PSEUDOMONAS; RNA SEQUENCE; SEQUENCE ANALYSIS; SHIGELLA; SKIN FLORA; STAPHYLOCOCCUS; VITAMIN SUPPLEMENTATION; BIOLOGICAL MODEL; CASE CONTROL STUDY; DIETARY SUPPLEMENT; DRUG EFFECTS; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MICROBIOLOGY; MICROFLORA; OPERON; PATHOLOGY; SKIN; YOUNG ADULT;

ACNE VULGARIS; ADULT; CASE-CONTROL STUDIES; DIETARY SUPPLEMENTS; DOWN-REGULATION; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; METABOLIC NETWORKS AND PATHWAYS; MICROBIOTA; MODELS, BIOLOGICAL; OPERON; PORPHYRINS; PROPIONIBACTERIUM ACNES; SKIN; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; VITAMIN B 12; YOUNG ADULT;

EID: 84937611678     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aab2009     Document Type: Article

References (82)

1. The Human Microbiome Project Consortium, Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214 (2012).
2. S. Fitz-Gibbon, S. Tomida, B.-H. Chiu, L. Nguyen, C. Du, M. Liu, D. Elashoff, M. C. Erfe, A. Loncaric, J. Kim, R. L. Modlin, J. F. Miller, E. Sodergren, N. Craft, G. M. Weinstock, H. Li, Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J. Invest. Dermatol. 133, 2152-2160 (2013).
3. E. A. Grice, H. H. Kong, S. Conlan, C. B. Deming, J. Davis, A. C. Young; NISC Comparative Sequencing Program, G. G. Bouffard, R. W. Blakesley, P. R. Murray, E. D. Green, M. L. Turner, J. A. Segre, Topographical and temporal diversity of the human skin microbiome. Science 324, 1190-1192 (2009).
4. I. Cho, M. J. Blaser, The human microbiome: At the interface of health and disease. Nat. Rev. Genet. 13, 260-270 (2012).
5. K. J. Pflughoeft, J. Versalovic, Human microbiome in health and disease. Annu. Rev. Pathol. 7, 99-122 (2012).
6. R. R. Marples, J. J. Leyden, R. N. Stewart, O. H. Mills Jr., A. M. Kligman, The skin microflora in acne vulgaris. J. Invest. Dermatol. 62, 37-41 (1974).
7. J. J. Leyden, K. J. McGinley, O. H. Mills, A. M. Kligman, Propionibacterium levels in patients with and without acne vulgaris. J. Invest. Dermatol. 65, 382-384 (1975).
8. K. T. Holland, W. J. Cunliffe, C. D. Roberts, The role of bacteria in acne vulgaris: A new approach. Clin. Exp. Dermatol. 3, 253-257 (1978).
9. W. J. Cunliffe, D. J. Gould, Prevalence of facial acne vulgaris in late adolescence and in adults. Br. Med. J. 1, 1109-1110 (1979).
10. S. Z. Ghodsi, H. Orawa, C. C. Zouboulis, Prevalence, severity, and severity risk factors of acne in high school pupils: A community-based study. J. Invest. Dermatol. 129, 2136-2141 (2009).
11. M. A. Gupta, A. K. Gupta, Depression and suicidal ideation in dermatology patients with acne, alopecia areata, atopic dermatitis and psoriasis. Br. J. Dermatol. 139, 846-850 (1998).
12. J. A. Halvorsen, R. S. Stern, F. Dalgard, M. Thoresen, E. Bjertness, L. Lien, Suicidal ideation, mental health problems, and social impairment are increased in adolescents with acne: A population-based study. J. Invest. Dermatol. 131, 363-370 (2011).
13. H. Gollnick, Current concepts of the pathogenesis of acne: Implications for drug treatment. Drugs 63, 1579-1596 (2003).
14. U. Jappe, Pathological mechanisms of acne with special emphasis on Propionibacterium acnes and related therapy. Acta Derm. Venereol. 83, 241-248 (2003).
15. G. F. Webster, Inflammation in acne vulgaris. J. Am. Acad. Dermatol. 33, 247-253 (1995).
16. H. C. Williams, R. P. Dellavalle, S. Garner, Acne vulgaris. Lancet 379, 361-372 (2012).
17. S. Tomida, L. Nguyen, B.-H. Chiu, J. Liu, E. Sodergren, G. M. Weinstock, H. Li, Pan-genome and comparative genome analyses of Propionibacterium acnes reveal its genomic diversity in the healthy and diseased human skin microbiome. MBio 4, e00003-e00013 (2013).
18. H. Brüggemann, A. Henne, F. Hoster, H. Liesegang, A. Wiezer, A. Strittmatter, S. Hujer, P. Dürre, G. Gottschalk, The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305, 671-673 (2004).
19. G. Dennis Jr., B. T. Sherman, D. A. Hosack, J. Yang, W. Gao, H. C. Lane, R. A. Lempicki, DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3 (2003).
20. W. Jadassohn, R. Paillard, R. Hofer, M. Golaz, Vitamine B12 et poussée aenéïforme. Dermatologica 116, 349 (1958).
21. A. Puissant, F. Vanbremeersch, J. Monfort, J. N. Lamberton, A new iatrogenic dermatosis: Acne caused by vitamin B 12. Bull. Soc. Fr. Dermatol. Syphiligr. 74, 813-815 (1967).
22. P. Dugois, P. Amblard, R. Imbert, B. de Bignicourt, Acne caused by vitamin B 12. Lyon Med. 221, 1165 (1969).
23. O. Braun-Falco, H. Lincke, The problem of vitamin B6/B12 acne. A contribution on acne medicamentosa (author's transl). MMW Munch. Med. Wochenschr. 118, 155-160 (1976).
24. A. Dupré, N. Albarel, J. Bonafe, B. Christol, J. Lassere, Vitamin B-12 induced acnes. Cutis 24, 210 (1979).
25. E. Sherertz, Acneiform eruption due to "megadose" vitamins B6 and B12. Cutis 48, 119-120 (1991).
26. I. Balta, P. Ozuguz, Vitamin B12-induced acneiform eruption. Cutan. Ocul. Toxicol. 33, 94-95 (2014).
27. 12). Nat. Prod. Rep. 19, 390-412 (2002).
28. 12 repression of the btuB gene in Salmonella typhimurium is mediated via a translational control which requires leader and coding sequences. Mol. Microbiol. 23, 35-42 (1997).
29. X. Nou, R. J. Kadner, Coupled changes in translation and transcription during cobalamindependent regulation of btuB expression in Escherichia coli. J. Bacteriol. 180, 6719-6728 (1998).
30. 12 metabolism and transport in bacteria by a conserved RNA structural element. RNA 9, 1084-1097 (2003).
31. 12 in man after a single parenteral dose of aqueous hydroxocobalamin, aqueous cyanocobalamin and cyanocobalamin zinc-tannate complex. Blood 18, 511-521 (1961).
32. 12 complexes. Am. J. Clin. Nutr. 10, 480-483 (1962).
33. 12, following parenteral administration of hydroxocobalamin (Vibeden). Acta Med. Scand. 180,95-105 (1966).
34. 12 level in psoriatic skin and serum. Br. J. Dermatol. 81, 911-918 (1969).
35. K. Murakami, Y. Hashimoto, Y. Murooka, Cloning and characterization of the gene encoding glutamate 1-semialdehyde 2,1-aminomutase, which is involved in δ-aminolevulinic acid synthesis in Propionibacterium freudenreichii. Appl. Environ. Microbiol. 59, 347-350 (1993).
36. V. BykhovskiѤ, N.I.ZaѤtseva, V. N. Bukin, Possible competition in the use of delta-aminolevulinic acid for the biosynthesis of vitamin B 12 and porphyrin by resting suspensions of Propionibacterium shermanii. Dokl. Akad. Nauk SSSR 180, 232-234 (1968).
37. H. C. Friedmann, L. M. Cagen, Microbial biosynthesis of B12-like compounds. Annu. Rev. Microbiol. 24, 159-208 (1970).
38. N. I. ZaѤtseva, V. BykhovskiѤ, V. N. Bukin, Regulation of vitamin B-12 and prophyrin biosynthesis in Propionibacterium shermanii. Dokl. Akad. Nauk SSSR 190, 1476-1479 (1970).
39. D. Saint-Leger, A. Bague, E. Cohen, M. Chivot, A possible role for squalene in the pathogenesis of acne. I. In vitro study of squalene oxidation. Br. J. Dermatol. 114, 535-542 (1986).
40. E. M. Gribbon, J. G. Shoesmith, W. J. Cunliffe, K. T. Holland, The microaerophily and photosensitivity of Propionibacterium acnes. J. Appl. Bacteriol. 77, 583-590 (1994).
41. M. Schaller, M. Loewenstein, C. Borelli, K. Jacob, M. Vogeser, W. H. Burgdorf, G. Plewig, Induction of a chemoattractive proinflammatory cytokine response after stimulation of keratinocytes with Propionibacterium acnes and coproporphyrin III. Br.J.Dermatol.153, 66-71 (2005).
42. S. Goldblatt, Vitamin B-12 levels in blood serum in acne-like skin diseases. Hautarzt 17, 106-108 (1966).
43. A. S. Karadag, E. Tutal, D. T. Ertugrul, K. O. Akin, Effect of isotretinoin treatment on plasma holotranscobalamin, vitamin B12, folic acid, and homocysteine levels: Non-controlled study. Int. J. Dermatol. 50, 1564-1569 (2011).
44. R. J. Martin, G. Kahn, J. W. Gooding, G. Brown, Cutaneous porphyrin fluorescence as an indicator of antibiotic absorption and effectiveness. Cutis 12, 758-764 (1973).
45. O. H. Mills Jr., A. M. Kligman, P. Pochi, H. Comite, Comparing 2.5%, 5%, and 10% benzoyl peroxide on inflammatory acne vulgaris. Int. J. Dermatol. 25, 664-667 (1986).
46. C. Borelli, K. Merk, M. Schaller, K. Jacob, M. Vogeser, G. Weindl, U. Berger, G. Plewig, In vivo porphyrin production by P. acnes in untreated acne patients and its modulation by acne treatment. Acta Derm. Venereol. 86, 316-319 (2006).
47. S. Mayr-Kanhäuser, B. Kränke, W. Aberer, Efficacy of octenidine dihydrochloride and 2-phenoxyethanol in the topical treatment of inflammatory acne. Acta Dermatovenerol. Alp. Panonica Adriat. 17, 139-143 (2008).
48. G. L. Simon, S. L. Gorbach, Intestinal flora in health and disease. Gastroenterology 86, 174-193 (1984).
49. J. Washio, T. Sato, T. Koseki, N. Takahashi, Hydrogen sulfide-producing bacteria in tongue biofilm and their relationship with oral malodour. J. Med. Microbiol. 54, 889-895 (2005).
50. E. S. Charlson, K. Bittinger, A. R. Haas, A. S. Fitzgerald, I. Frank, A. Yadav, F. D. Bushman, R. G. Collman, Topographical continuity of bacterial populations in the healthy human respiratory tract. Am.J. Respir.Crit.CareMed.184, 957-963 (2011).
51. Z. Ling, X. Liu, X. Chen, H. Zhu, K. E. Nelson, Y. Xia, L. Li, C. Xiang, Diversity of cervicovaginal microbiota associated with female lower genital tract infections. Microb. Ecol. 61, 704-714 (2011).
52. J. J. Leyden, K. J. McGinley, K. M. Nordstrom, G. F. Webster, Skin microflora. J. Invest. Dermatol. 88, 65s-72s (1987).
53. E. A. Grice, J. A. Segre, The skin microbiome. Nat. Rev. Microbiol. 9, 244-253 (2011).
54. V. Tremaroli, F. Bäckhed, Functional interactions between the gut microbiota and host metabolism. Nature 489, 242-249 (2012).
55. I. Cho, S. Yamanishi, L. Cox, B. A. Methé, J. Zavadil, K. Li, Z. Gao, D. Mahana, K. Raju, I. Teitler, H. Li, A. V. Alekseyenko, M. J. Blaser, Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488, 621-626 (2012).
56. L. A. David, C. F. Maurice, R. N. Carmody, D. B. Gootenberg, J. E. Button, B. E. Wolfe, A. V. Ling, A. S. Devlin, Y. Varma, M. A. Fischbach, S. B. Biddinger, R. J. Dutton, P. J. Turnbaugh, Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559-563 (2014).
57. H. J. Haiser, D. B. Gootenberg, K. Chatman, G. Sirasani, E. P. Balskus, P. J. Turnbaugh, Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta. Science 341, 295-298 (2013).
58. G. D. Wu, J. Chen, C. Hoffmann, K. Bittinger, Y. Y. Chen, S. A. Keilbaugh, M. Bewtra, D. Knights, W. A. Walters, R. Knight, R. Sinha, E. Gilroy, K. Gupta, R. Baldassano, L. Nessel, H. Li, F. D. Bushman, J. D. Lewis, Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105-108 (2011).
59. Y. Furusawa, Y. Obata, S. Fukuda, T. A. Endo, G. Nakato, D. Takahashi, Y. Nakanishi, C. Uetake, K. Kato, T. Kato, M. Takahashi, N. N. Fukuda, S. Murakami, E. Miyauchi, S. Hino, K. Atarashi, S. Onawa, Y. Fujimura, T. Lockett, J. M. Clarke, D. L. Topping, M. Tomita, S. Hori, O. Ohara, T. Morita, H. Koseki, J. Kikuchi, K. Honda, K. Hase, H. Ohno, Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504, 446-450 (2013). Downloaded from on June 25, 2015
60. Z. Wang, E. Klipfell, B. J. Bennett, R. Koeth, B. S. Levison, B. DuGar, A. E. Feldstein, E. B. Britt, X. Fu, Y.-M. Chung, Y. Wu, P. Schauer, J. D. Smith, H. Allayee, W. H. Tang, J. A. DiDonato, A. J. Lusis, S. L. Hazen, Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472, 57-63 (2011).
61. S. Yoshimoto, T. M. Loo, K. Atarashi, H. Kanda, S. Sato, S. Oyadomari, Y. Iwakura, K. Oshima, H. Morita, M. Hattori, K. Honda, Y. Ishikawa, E. Hara, N. Ohtani, Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499, 97-101 (2013).
62. A. L. Goodman, N. P. McNulty, Y. Zhao, D. Leip, R. D. Mitra, C. A. Lozupone, R. Knight, J. I. Gordon, Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6, 279-289 (2009).
63. B. Dréno, F. Poli, H. Pawin, C. Beylot, M. Faure, M. Chivot, N. Auffret, D. Moyse, F. Ballanger, J. Revuz, Development and evaluation of a Global Acne Severity Scale (GEA Scale) suitable for France and Europe. J. Eur. Acad. Dermatol. Venereol. 25, 43-48 (2011).
64. The Human Microbiome Project Consortium, A framework for human microbiome research. Nature 486, 215-221 (2012).
65. C. Quast, E. Pruesse, P. Yilmaz, J. Gerken, T. Schweer, P. Yarza, J. Peplies, F. O. Glockner, The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590-D596 (2013).
66. B. Langmead, C. Trapnell, M. Pop, S. L. Salzberg, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
67. E. E. Hansen, C. A. Lozupone, F. E. Rey, M. Wu, J. L. Guruge, A. Narra, J. Goodfellow, J. R. Zaneveld, D. T. McDonald, J. A. Goodrich, A. C. Heath, R. Knight, J. I. Gordon, Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins. Proc. Natl. Acad. Sci. U.S.A. 108, 4599-4606 (2011).
68. W. Li, L. Jaroszewski, A. Godzik, Clustering of highly homologous sequences to reduce the size of large protein databases. Bioinformatics 17, 282-283 (2001).
69. C. M. Sharma, S. Hoffmann, F. Darfeuille, J. Reignier, S. Findeiß, A. Sittka, S. Chabas, K. Reiche, J. Hackermüller, R. Reinhardt, P. F. Stadler, J. Vogel, The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464, 250-255 (2010).
70. M. D. Lundrigan, R. J. Kadner, Altered cobalamin metabolism in Escherichia coli btuR mutants affects btuB gene regulation. J. Bacteriol. 171, 154-161 (1989).
71. S. Piomelli, B. Davidow, V. F. Guinee, P. Young, G. Gay, The FEP (free erythrocyte porphyrins) test: A screening micromethod for lead poisoning. Pediatrics 51, 254-259 (1973).
72. E. Kristiansson, P. Hugenholtz, D. Dalevi, ShotgunFunctionalizeR: An R-package for functional comparison of metagenomes. Bioinformatics 25, 2737-2738 (2009).
73. R. Suzuki, H. Shimodaira, Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22, 1540-1542 (2006).
74. J. Frias-Lopez, Y. Shi, G. W. Tyson, M. L. Coleman, S. C. Schuster, S. W. Chisholm, E. F. Delong, Microbial community gene expression in ocean surface waters. Proc. Natl. Acad. Sci. U.S A. 105, 3805-3810 (2008).
75. R. S. Poretsky, N. Bano, A. Buchan, G. LeCleir, J. Kleikemper, M. Pickering, W. M. Pate, M. A. Moran, J. T. Hollibaugh, Analysis of microbial gene transcripts in environmental samples. Appl. Environ. Microbiol. 71, 4121-4126 (2005).
76. R. L. Tatusov, N. D. Fedorova, J. D. Jackson, A. R. Jacobs, B. Kiryutin, E. V. Koonin, D. M. Krylov, R. Mazumder, S. L. Mekhedov, A. N. Nikolskaya, B. S. Rao, S. Smirnov, A. V. Sverdlov, S. Vasudevan, Y. I. Wolf, J. J. Yin, D. A. Natale, The COG database: An updated version includes eukaryotes. BMC Bioinformatics 4, 41 (2003).
77. M. Kanehisa, S. Goto, Y. Sato, M. Furumichi, M. Tanabe, KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109-D114 (2012).
78. J. Oksanen, F. G. Blanchet, R. Kindt, P. Legendre, R. G. O'Hara, G. L. Simpson, P. Solymos, M. Henry, H. Stevens, H. Wagner, vegan: Community ecology package. R package version 1.17-0 (2010); http://cran.r-project.org/web/packages/vegan/.
79. B. Bolker, L. Bonebakker, R. Gentleman, W. H. A. Liaw, T. Lumley, M. Maechler, A. Magnusson, S. Moeller, M. Schwartz, B. Venables, gplots: Various R programming tools for plotting data. R package version 2.7.4 (2009); http://cran.r-project.org/web/packages/gplots/.
80. A. S. Cristino, E. D. Tanaka, M. Rubio, M.-D. Piulachs, X. Belles, Deep sequencing of organ- and stage-specific microRNAs in the evolutionarily basal insect Blattella germanica (L.) (Dictyoptera, Blattellidae). PLOS One 6, e19350 (2011).
81. T. Yamada, I. Letunic, S. Okuda, M. Kanehisa, P. Bork, iPath2.0: Interactive pathway explorer. Nucleic Acids Res. 39, W412-W415 (2011).
82. G. Kasimatis, S. Fitz-Gibbon, S. Tomida, M. Wong, H. Li, Analysis of complete genomes of Propionibacterium acnes reveals a novel plasmid and increased pseudogenes in an acne associated strain. Biomed. Res. Int. 2013, 918320 (2013).