Propionibacterium acnes activates the NLRP3 inflammasome in human sebocytes

Journal of Investigative Dermatology

Volumn 134, Issue 11, 2014, Pages 2747-2756

  Li, Zheng Jun ^a   Choi, Dae Kyoung ^a   Sohn, Kyung Cheol ^a   Seo, Min Seok ^a   Lee, Hae Eul ^a   Lee, Young ^a   Seo, Young Joon ^a   Lee, Young Ho ^a   Shi, Ge ^b   Zouboulis, Christos C ^c   Kim, Chang Deok ^a   Lee, Jeung Hoon ^a   Im, Myung ^a  

^a Chungnam National University   (South Korea)

^b GUANGDONG MEDICAL UNIVERSITY   (China)

^c DESSAU MEDICAL CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEINASE; REACTIVE OXYGEN METABOLITE; CARRIER PROTEIN; NLRP3 PROTEIN, HUMAN; PEPTIDE HYDROLASE;

ACNE VULGARIS; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROPIONIBACTERIUM ACNES; PROTEIN EXPRESSION; PUNCH BIOPSY; SEBACEOUS CELL; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; IMMUNOLOGY; INFLAMMATION; METABOLISM; MICROBIOLOGY; SEBACEOUS GLAND; SKIN; YOUNG ADULT;

ACNE VULGARIS; ADULT; ANIMALS; CARRIER PROTEINS; CASPASE 1; CELLS, CULTURED; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; MALE; MICE; MICE, INBRED C57BL; PEPTIDE HYDROLASES; PROPIONIBACTERIUM ACNES; REACTIVE OXYGEN SPECIES; SEBACEOUS GLANDS; SKIN; UP-REGULATION; YOUNG ADULT;

EID: 84908562621     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2014.221     Document Type: Article

References (50)

1. Ahern TJ, Klibanov AM (1987) Analysis of processes causing thermal inactivation of enzymes. In: Methods of Biochemical Analysis (Glick D ed), John Wiley &Sons Press: Hoboken, 91-127
2. Alestas T, Ganceviciene R, Fimmel S., et al (2006) Enzymes involved in the biosynthesis of leukotriene B4 and prostaglandin E2 are active in sebaceous glands. J Mol Med 84:75-87
3. Aoshiba K, Yasuda K, Yasui S., et al (2001) Serine proteases increase oxidative stress in lung cells. Am J Physiol Lung Cell Mol Physiol 281:556-64
4. Beylot C, Auffret N, Poli F., et al (2014) Propionibacterium acnes: an update on its role in the pathogenesis of acne. J Eur Acad Dermatol Venereol 28: 271-8
5. Brydges SD, Mueller JL, McGeough MD., et al (2009) Inflammasome-mediated disease animal models reveal roles for innate but not adaptive immunity. Immunity 30:875-7
6. Chen W, Obermayer-Pietsch B, Hong J-B., et al (2011) Acne-Associated syndromes: Models for better understanding of acne pathogenesis. J Eur Acad Dermatol Venereol 25:637-46
7. Clarke SB, Nelson AM, George RE., et al (2007) Pharmacologic modulation of sebaceous gland activity: mechanisms and clinical applications. Dermatol Clin 25:137-46
8. Davis BK, Wen H, Ting JP (2011) The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol 29:707-35
9. Di Virgilio F (2007) Liaisons dangereuses: P2X(7) and the inflammasome. Trends Pharmacol Sci 28:465-72
10. Dostert C, Petrilli V, Van Bruggen R., et al (2008) Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320:674-7
11. Georgel P, Crozat K, Lauth X., et al (2005) A toll-like receptor 2-responsive lipid effector pathway protects mammals against skin infections with grampositive bacteria. Infect Immun 73:4512-21
12. Graham GM, Farrar MD, Cruse-Sawyer JE., et al (2004) Proinflammatory cytokine production by human keratinocytes stimulated with Propionibacterium acnes and P acnes GroEL. Br J Dermatol 150:421-8
13. Guy R, Kealey T (1998) The effects of inflammatory cytokines on the isolated human sebaceous infundibulum. J Invest Dermatol 110:410-5
14. HoeZer U (1977) Enzymatic and hemolytic properties of Propionibacterium acnes and related bacteria. J Clin Microbiol 6:555-8
15. Hornung V, Ablasser A, Charrel-Dennis M., et al (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-Activating inflammasome with ASC. Nature 458:514-8
16. Ingham E, Eady EA, Goodwin CE., et al (1992) Pro-inflammatory levels of interleukin-1 alpha-like bioactivity are present in the majority of open comedones in acne vulgaris. J Invest Dermatol 98:895-901
17. Ingram E, Holland KT, Gowland G., et al (1983) Studies of the extracellular proteolytic activity produced by Propionibacterium acnes. J Appl Bacteriol 54:263-71
18. Jahns AC, Lundskog B, Ganceviciene R., et al (2012) An increased incidence of Propionibacterium acnes biofilms in acne vulgaris: a case control study. Br J Dermatol 167:50-8
19. Jin Y, Mailloux CM, Gowan K., et al (2007) NALP1 in vitiligo-Associated multiple autoimmune disease. N Engl J Med 356:1216-25
20. Johansen C, Moeller K, Kragballe K., et al (2007) The activity of caspase-1 is increased in lesional psoriatic epidermis. J Invest Dermatol 127:2857-64
21. Kauffman HF, Tamm M, Timmerman JA., et al (2006) House dust mite major allergens Der p1 and Der p5 activate human airway-derived epithelial cells by protease dependent and protease-independent mechanisms. Clin Mol Allergy 4:5
22. Kim J, Ochoa MT, Krutzik SR., et al (2002) Activation of toll-like receptor 2 in acne triggers inflammatory cytokine responses. J Immunol 169: 1535-41
23. Kistowska M, Gehrke S, Jankovic D., et al (2014) IL-1b drives inflammatory responses to propionibacterium acnes in vitro and in vivo. J Invest Dermatol 134:677-85
24. Koizumi Y, Toma C, Higa N., et al (2012) Inflammasome activation via intracellular NLRs triggered by bacterial infection. Cell Microbiol 14: 149-54
25. Koreck A, Pivarcsi A, Dobozy A., et al (2003) The role of innate immunity in the pathogenesis of acne. Dermatology 206:96-105
26. Kurokawa I, Danby FW, Ju Q., et al (2009) New developments in our understanding of acne pathogenesis and treatment. Exp Dermatol 18: 821-32
27. Lee SE, Kim JM, Jeong SK., et al (2010) Protease-Activated receptor-2 mediates the expression of inflammatory cytokines, antimicrobial peptides, and matrix metalloproteinases in keratinocytes in response to Propionibacterium acnes. Arch Dermatol Res 302:745-56
28. Mariathasan S, Newton K, Monack DM., et al (2004) Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430:213-8
29. Mariathasan S, Weiss DS, Newton K., et al (2006) Cryopyrin activates the inflammasome in response to toxins and ATP Nature 440:228-32
30. Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10:417-26
31. Nagy I, Pivarcsi A, Kis K., et al (2006) Propionibacterium acnes and lipopolysaccharide induce the expression of antimicrobial peptides and proinflammatory cytokines/ chemokines in human sebocytes. Microbes Infect 8:2195-205
32. Nguyen TV, Cowen EW, Leslie KS (2013) Autoinflammation: from monogenic syndromes to common skin Diseases. J Am Acad Dermatol 68:834-53
33. Oeff MK, Seltmann H, Hiroi N., et al (2006) Differential regulation of Toll-like receptor and CD14 pathways by retinoids and corticosteroids in human sebocytes. Dermatology 213:266
34. Ossanna PJ, Test ST, Matheson NR., et al (1986) Oxidative regulation of neutrophil elastase-Alpha-1 proteinase inhibitor interactions. J Clin Invest 77:1939-51
35. Qin M, Pirouz A, Kim MH., et al (2014) Propionibacterium acnes induces IL-1b secretion via the NLRP3 inflammasome in human monocytes. J Invest Dermatol 134:381-8
36. Rattenholl A, Steinho VM (2003) Role of proteinase-Activated receptors in cutaneous biology and disease. Drug Dev Res 59:408-16
37. Shi G, Sohn KC, Li Z., et al (2013) Expression and functional role of Sox9 in human epidermal keratinocytes. PLoS One 8:e54355
38. Shoham NG, Centola M, Mansfield E., et al (2003) Pyrin binds the PSTPIP1/ CD2BP1 protein, defining familial Mediterranean fever and PAPA syndrome as disorders in the same pathway. Proc Natl Acad Sci USA 100:13501-6
39. Speer CP, Pabst MJ, Hedgaard HB., et al (1984) Enhanced release of oxygen metabolites by monocyte-derived macrophages exposed to proteolytic enzymes: activity of neutrophil elastase and cathepsin G. J Immunol 133:2151-6
40. Tschopp J, Schröder K (2010) NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production?. Nat Rev Immunol 10:210-5
41. Vande Walle L, Lamkanfi M (2011) Inflammasomes: caspase-1-Activating platforms with critical roles in host defense. Front Microbiol 2:3
42. Walker NP, Talanian RV, Brady KD., et al (1994) Crystal structure of the cysteine protease interleukin-1 beta-converting enzyme: a (p20/ p10)2 homodimer. Cell 78:343-52
43. Watanabe H, Gaide O, Pétrilli V., et al (2007) Activation of the IL-1betaprocessing inflammasome is involved in contact hypersensitivity. J Invest Dermatol 127:1956-63
44. Weiss SJ, Regiani S (1984) Neutrophils degrade subendothelial matrices in the presence of alpha-1-Antiproteinase inhibitor: cooperative use of lysosomal proteinases and oxygen metabolites. J Clin Invest 73:1297-303
45. Wilmanski JM, Petnicki-Ocwieja T, Kobayashi KS (2008) NLR proteins: integral members of innate immunity and mediators of inflammatory diseases. J Leukoc Biol 83:13-30
46. Zhou R, Tardivel A, Thorens B., et al (2010) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 11: 136-40
47. Zouboulis CC (2001) Is acne vulgaris a genuine inflammatory disease?. Dermatology 203:277-9
48. Zouboulis CC (2005) Acne and sebaceous gland function. Clin Dermatol 22:360-6
49. Zouboulis CC, Seltmann H, Neitzel H., et al (1999) Establishment and characterization of an immortalized human sebaceous gland cell line (SZ95) J Invest Dermatol 113:1011-20
50. Zouboulis CC, Xia L, Akamatsu H., et al (1998) The human sebocyte culture model provides new insights into development and management of seborrhoea and acne. Dermatology 196:21-31