Propionibacterium acnes and lipopolysaccharide induce the expression of antimicrobial peptides and proinflammatory cytokines/chemokines in human sebocytes

Microbes and Infection

Volumn 8, Issue 8, 2006, Pages 2195-2205

  Nagy, István ^a   Pivarcsi, Andor ^a   Kis, Kornélia ^a   Koreck, Andrea ^a   Bodai, László ^a   McDowell, Andrew ^b   Seltmann, Holger ^c   Patrick, Sheila ^b   Zouboulis, Christos C ^c,d   Kemény, Lajos ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d DESSAU MEDICAL CENTER   (Germany)

Author keywords

Acne; Inflammation; Innate immunity; Pilosebaceous unit; Sebocytes

Indexed keywords

BETA DEFENSIN 2; CHEMOKINE; CYTOKINE; LIPOPOLYSACCHARIDE; MESSENGER RNA;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CELL DIFFERENTIATION; CELL VIABILITY; COCULTURE; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROPIONIBACTERIUM ACNES;

ANTIMICROBIAL CATIONIC PEPTIDES; CELL LINE; CELL SURVIVAL; COCULTURE TECHNIQUES; CYTOKINES; DNA, BACTERIAL; GENE EXPRESSION; HUMANS; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROPIONIBACTERIUM ACNES; REC A RECOMBINASES; RNA; SEBACEOUS GLANDS; SEQUENCE ANALYSIS, DNA;

ESCHERICHIA COLI; PROPIONIBACTERIUM ACNES;

EID: 33748366355     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2006.04.001     Document Type: Article

References (64)

1. Koreck A., Pivarcsi A., Dobozy A., and Kemeny L. The role of innate immunity in the pathogenesis of acne. Dermatology 206 (2003) 96-105
2. Toyoda M., and Morohashi M. Pathogenesis of acne. Med. Electron. Microsc. 34 (2001) 29-40
3. Thiboutot D. Regulation of human sebaceous glands. J. Invest. Dermatol. 123 (2004) 1-12
4. Zouboulis C.C., Eady A., Philpott M., Goldsmith L.A., Orfanos C., Cunliffe W.C., and Rosenfield R. What is the pathogenesis of acne?. Exp. Dermatol. 14 (2005) 143-152
5. Zouboulis C.C. Is acne vulgaris a genuine inflammatory disease?. Dermatology 203 (2001) 277-279
6. Zouboulis C.C. Acne and sebaceous gland function. Clin. Dermatol. 22 (2004) 360-366
7. Slominski A., Ermak G., Hwang J., Chakroborty A., Mazurkiewitz J., and Mihm M. Proopiomelanocortin, corticotrophin releasing hormone and cortocotrophin releasing hormone receptor genes are expressed in human skin. FEBS Lett. 374 (1995) 113-116
8. Zouboulis C.C., Seltmann H., Hiroi N., Chen W., Young M., Oeff M., Scherbaum W.A., Orfanos C.E., McCann S.M., and Bornstein S.R. Corticotropin-releasing hormone/ An autocrine hormone that promotes lipogenesis in human sebocytes. PNAS 99 (2002) 7148-7153
9. Bohm M., Schiller M., Stander S., Seltmann H., Li Z., Brzoska T., Metze D., Schioth H.B., Skottner A., Seiffert K., Zouboulis C.C., and Luger T.A. Evidence for expression of melanocortin-1 receptor in human sebocytes in vitro and in situ. J. Invest. Dermatol. 118 (2002) 533-539
10. Bohm M., Zouboulis C.C., and Luger T.A. Evidence for expression of mu-opoid receptors on human sebocytes which mediate paracrine and/or endocrine action of beta-endorphin (abstract). J. Invest. Dermatol. 119 (2002) 278
11. Seiffert K., Zouboulis C.C., Seltmann H., and Granstein R.D. Expression of neuropeptide receptors by human sebocytes and stimulatory effect of their agonists on cytokine production (abstract). Horm. Res. 53 (2000) 102
12. Zouboulis C.C., and Bohm M. Neuroendocrine regulation of sebocytes-a pathogenic link between stress and acne. Exp. Dermatol. 13 Suppl. 4 (2004) 31-35
13. Leeming J.P., Holland K.T., and Cunliffe W.J. The microbial colonization of inflamed acne vulgaris lesions. Br. J. Dermatol. 118 (1988) 203-208
14. Leyden J.J., McGinley K.J., and Vowels B. Propionibacterium acnes colonization in acne and non-acne. Dermatology 196 (1988) 55-58
15. Graham G.M., Farrar M.D., Cruse-Sawyer J.E., Holland K.T., and Ingham E. Proinflammatory cytokine production by human keratinocytes stimulated with Propionibacterium acnes and P. acnes GroEL. Br. J. Dermatol. 150 (2004) 421-428
16. Nagy I., Pivarcsi A., Koreck A., Szell M., Urban E., and Kemeny L. Distinct strains of Propionibacterium acnes induces selective human β-defensin-2 and interleukin-8 expression in human keratinocytes through Toll-like receptors. J. Invest. Dermatol. 124 (2005) 931-938
17. Schaller M., Loewenstein M., Borelli C., Jacob K., Vogeser M., Burgdorf W.H., and Plewig G. Induction of a chemoattractive proinflammatory cytokine response after stimulation of keratinocytes with Propionibacterium acnes and coproporphyrin III. Br. J. Derm. 153 (2005) 66-71
18. McDowell A., Valanne S., Ramage G., Tunney M.M., Glenn J.V., McLorinan G.C., Bhatia A., Maisonneuve J.F., Lodes M., Persing D.H., and Patrick S. Propionibacterium acnes types I and II represent phylogenetically distinct groups. J. Clin. Microbiol. 43 (2005) 326-334
19. Valanne S., McDowell A., Ramage G., Tunney M.M., Einarsson G.G., O'Hagan S., Wisdom G.B., Fairley D., Bhatia A., Maisonneuve J.F., Lodes M., Persing D.H., and Patrick S. CAMP factor homologues in Propionibacterium acnes: a new protein family differentially expressed by types I and II. Microbiology 151 (2005) 1369-1379
20. Takeda K., and Akira S. Microbial recognition by Toll-like receptors. J. Dermatol. Sci. 34 (2004) 73-82
21. Netea M.G., Van der Graaf C., Van der Meer J.W., and Kullberg B.J. Toll-like receptors and the host defense against microbial pathogens: bringing specificity to the innate-immune system. J. Leukoc. Biol. 75 (2004) 749-755
22. Pasare C., and Medzhitov R. Toll-like receptors: linking innate and adaptive immunity. Microbes Infect. 6 (2004) 1382-1387
23. Oeff M.K., Seltmann H., Hakiy N., Bogdanoff B., Nastos A., Walters R., Bornstein S.R., and Zouboulis C.C. Toll-like Receptor 2 and 4-dependent regulation of inflammatory signaling in human sebocytes (abstract). J. Invest. Dermatol. 119 (2002) 736
24. Georgel P., Crozat K., Lauth X., Makrantonaki E., Seltmann H., Sovath S., Hoebe K., Du X., Rutshmann S., Jiang Z., Bigby T., Nizet V., Zouboulis C.C., and Beutler B. A TLR2-responsive lipid effector pathway protects mammals against Gram-positive bacterial skin infections. Infect. Immun. 73 (2005) 4512-4521
25. Kumar S., Tamura K., and Nei M. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5 (2004) 150-163
26. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
27. Zouboulis C.C., Seltmann H., Neitzel H., and Orfanos E. Establishment and characterization of an immortalized human sebaceous gland cell line (SZ95). J. Invest. Dermatol. 113 (1999) 1011-1020
28. Pivarcsi A., Bodai L., Rethi B., Kenderessy-Szabo A., Koreck A., Szell M., Beer Z., Bata-Csorgoo Z., Magocsi M., Rajnavolgyi E., Dobozy A., and Kemeny L. Expression and function of Toll-like receptors 2 and 4 in human keratinocytes. Int. Immunol. 15 (2003) 721-730
29. Pivarcsi A., Nagy I., Koreck A., Kis K., Kenderessy-Szabo A., Szell M., Dobozy A., and Kemeny L. Microbial compounds induce the expression of pro-inflammatory cytokines, chemokines and human β-defensin-2 in vaginal epithelial cells. Microbes Infect 7 (2005) 1117-1127
30. Tunney M.M., Patrick S., Curran M.D., Ramage G., Hanna D., Nixon J.R., Gorman S.P., Davis R.I., and Anderson N. Detection of prosthetic hip infection at revision arthroplasty by immunofluorescence microscopy and PCR amplification of the bacterial 16S rRNA gene. J. Clin. Microbiol. 37 (1999) 3281-3290
31. Dinulos J.G.H., Mentele L., Frederics L.P., Dale B.A., and Darmstadt G.L. Keratinocyte expression of human β defensin 2 following bacterial infection: role in cutaneous host defense. Clin. Diagn. Lab. Immunol. 10 (2003) 161-166
32. Kurzen H., Berger H., Jager C., Hartschuh W., Naher H., Gratchev A., Goerdt S., and Diechmann M. Phenotypical and molecular profiling of the extraneuronal cholinergic system of the skin. J. Invest. Dermatol. 123 (2004) 937-949
33. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983) 55-63
34. Dreno B., and Poli F. Epidemiology of acne. Dermatology 206 (2003) 7-10
35. Mouser P.E., Baker B.S., Seaton E.D., and Chu A.C. Propionibacterium acnes-reactive T helper-1 cells in the skin of patients with acne vulgaris. J. Invest. Dermatol. 121 (2003) 1226-1228
36. McGinley K.J., Webster G.F., Ruggieri M.R., and Leyden J.J. Regional variations in density of cutaneous propionibacteria: Correlation of Propionibacterium acnes populations with sebaceous secretion. J. Clin. Microbiol. 12 (1980) 672-675
37. Jappe U., Boit R., Farrar M.D., Ingham E., Sandoe J., and Holland K.T. Evidence for diversity within Propionibacterium acnes: a comparison of the T-cell stimulatory activity of isolates from inflammatory acne, endocarditis and the laboratory. J. Eur. Acad. Dermatol. Venereol. 18 (2004) 450-454
38. Johnson J.L., and Cummins C.S. Cell wall composition and deoxyribonucleic acid similarities among the anaerobic coryneforms, classical propionibacteria, and strains of Arachnia propionica. J. Bacteriol. 109 (1972) 1047-1066
39. Kim J., Ochoa M.T., Krutzik S.R., Takeuchi O., Uematsu S., Legaspi A.J., Brightbill H.D., Holland D., Cunliffe W.J., Akira S., Sieling P.A., Godowski P.J., and Modlin R.L. Activation of toll-like receptor 2 in acne triggers inflammatory cytokine responses. J. Immunol. 169 (2002) 1535-1541
40. Jeremy A.H., Holland D.B., Roberts S.G., Thomson K.F., and Cunliffe W.J. Inflammatory events are involved in acne lesion initiation. J. Invest. Dermatol. 121 (2003) 20-27
41. Harder J., Bartels J., Christophers E., and Schroder J.M. A peptide antibiotic from human skin. Nature 387 (1997) 861
42. Schroder J.M. Epithelial peptide antibiotics. Biochem. Pharmacol. 57 (1999) 121-134
43. Sorensen O.E., Thapa D.R., Rosenthal A., Liu L., Roberts A.A., and Ganz T. Differential regulation of β-defensin expression in human skin by microbial stimuli. J. Immunol. 174 (2005) 4870-4879
44. Yang D., Chertov O., Bykovskaia S.N., Chen Q., Buffo M.J., Shogan J., Anderson M., Schroder J.M., Wang J.M., Howard O.M., and Oppenheim J.J. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286 (1999) 525-528
45. Niyonsaba F., Ogawa H., and Nagaoka I. Human beta-defensin-2 functions as a chemotactic agent for tumour necrosis factor-alpha-treated human neutrophils. Immunology 111 (2004) 273-281
46. Chronnell C.M., Ghali L.R., Ali R.S., Quinn A.G., Holland D.B., Bull J.J., Cunliffe W.J., McKay I.A., Philpott M.P., and Muller-Rover S. Human beta defensin-1 and -2 expression in human pilosebaceous units: upregulation in acne vulgaris lesions. J. Invest. Dermatol. 117 (2001) 1120-1125
47. Philpott M.P. Defensins and acne. Mol. Immunol. 40 (2003) 457-462
48. Pivarcsi A., Nagy I., and Kemeny L. Innate immunity of the skin: how keratinocytes fight against pathogens. Curr. Immunol. Rev. 1 (2005) 29-42
49. Chen Q., Koga T., Uchi H., Hara H., Terao H., Moroi Y., Urabe K., and Furue M. Propionibacterium acnes-induced IL-8 production may be mediated by NF-κB activation in human monocytes. J. Dermatol. Sci. 29 (2002) 97-103
50. Newton R., Adcock I.M., and Barnes P.J. Superinduction of NF-kappa B by actinomycin D and cycloheximide in epithelial cells. Biochem. Biophys. Res. Commun. 218 (1996) 518-523
51. Gillitzer R., and Goebeler M. Chemokines in cutaneous wound healing. J. Leukoc. Biol. 69 (2001) 513-521
52. Michel G., Kemeny L., Peter R.U., Beetz A., Ried C., Arenberger P., and Ruzicka T. Interleukin-8 receptor-mediated chemotaxis of normal human epidermal cells. FEBS Lett. 305 (1992) 241-243
53. Tomari Y., and Zamore P.D. Perspective: machines for RNAi. Genes Dev. 19 (2005) 517-529
54. Bhattacharjee R.N., and Akira S. Toll-like receptor signaling: emerging opportunities in human diseases and medicine. Curr. Immunol. Rev. 1 (2005) 81-90
55. Vega-Diaz B., Jonard A., and Michel S. Regulation of human monocyte toll-like receptor 2 (TLR2) expression by adapalene (abstract). J. Eur. Acad. Dermatol. Venereol. 16 (2002) 123-124
56. Liu P.T., Krutzik S.R., Kim J., and Modlin R.A. Cutting Edge: All-trans retinoic acid downregulates TLR2 expression and function. J. Immunol. 174 (2005) 2461-2470
57. Farrar M.D., Ingham E., and Holland K.T. Heat shock proteins and inflammatory acne vulgaris: molecular cloning, overexpression and purification of a Propionibacterium acnes GroEL and DnaK homologue. FEMS Microbiol. Lett. 191 (2000) 183-186
58. Whale G.A., Sutcliffe I.C., Morrisson A.R., Pretswell E.L., and Emmison N. Purification and characterization of lipoglycan macroamphiphiles from Propionibacterium acnes. Antonie Van Leeuwenhoek 86 (2004) 77-85
59. Bruggemann H., Henne A., Hoster F., Liesegang H., Wiezer A., Strittmatter A., Hujer S., Durre P., and Gottschalk G. The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305 (2004) 671-673
60. McLorinan G.C., Glenn J.V., McMullan M.G., and Patrick S. Propionibacterium acnes wound contamination at the time of spinal surgery. Clin. Orthop. Relat. Res. 437 (2005) 67-73
61. Zouboulis C.C., Nestoris S., Adler Y.D., Orth M., Orfanos C.E., Picardo M., Camera E., and Cunliffe W.J. A new concept for acne therapy: a pilot study with zileuton, an oral 5-lipoxygenase inhibitor. Arch. Dermatol. 139 (2003) 668-670
62. Skidmore R., Kovach R., Walker C., Thomas J., Bradshaw M., Leyden J., Powala C., and Ashley R. Effects of subantimicrobial-dose doxycycline in the treatment of moderate acne. Arch. Dermatol. 139 (2003) 459-464
63. Ross J.I., Snelling A.M., Carnegie E., Coates P., Cunliffe W.J., Bettoli V., Tosti G., Katsambas A., Galvan Perez Del Pulgar J.I., Rollmann O., Torok L., Eady E.A., and Cove J.H. Antibiotic-resistant acne: lessons from Europe. Br. J. Dermatol. 148 (2003) 467-478
64. Zouboulis C.C., and Piquero-Martin J. Update and future of systemic acne treatment. Dermatology 206 (2003) 37-53