Cleavage of host cytokeratin-6 by lysine-specificgingipain induces gingival inflammation in periodontitis patients

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Tancharoen, Salunya ^a   Matsuyama, Takashi ^b   Kawahara, Ko Ichi ^c   Tanaka, Kenji ^d   Lee, Lyang Ja ^d   Machigashira, Miho ^b   Noguchi, Kazuyuki ^b   Ito, Takashi ^b   Imamura, Takahisa ^e   Potempa, Jan ^f,g   Kikuchi, Kiyoshi ^h   Maruyama, Ikuro ^b  

^a MAHIDOL UNIVERSITY   (Thailand)

^b KAGOSHIMA UNIVERSITY   (Japan)

^c OSAKA INSTITUTE OF TECHNOLOGY   (Japan)

^d Protosera Inc   (Japan)

^e KUMAMOTO UNIVERSITY   (Japan)

^f UNIVERSITY OF LOUISVILLE   (United States)

^g JAGIELLONIAN UNIVERSITY   (Poland)

^h KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CYTOKERATIN 6; CYTOKERATIN 6 FRAGMENT; INTERLEUKIN 6; INTERLEUKIN 8; LYSINE SPECIFIC GINGIPAIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG; VIRULENCE FACTOR; ADHESIN; ARGINGIPAIN, PORPHYROMONAS GINGIVALIS; CYSTEINE PROTEINASE; CYTOKINE;

ADULT; AGED; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ANIMAL CELL; ARTICLE; CELL INVASION; CELL MIGRATION; CHRONIC PERIODONTITIS; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; EPITHELIUM CELL; FEMALE; FIBROBLAST; GINGIVITIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; NONHUMAN; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; RAT; TISSUE DISTRIBUTION; ANIMAL; CELL CULTURE; DRUG EFFECTS; GINGIVA; INFLAMMATION; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS; RATTUS;

ADHESINS, BACTERIAL; ANIMALS; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; CYTOKINES; EPITHELIAL CELLS; GINGIVA; GINGIVAL CREVICULAR FLUID; HUMANS; INFLAMMATION; KERATIN-6; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; RATS; SIGNAL TRANSDUCTION;

EID: 84928914572     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117775     Document Type: Article

References (68)

1. Junemann S, Prior K, Szczepanowski R, Harks I, Ehmke B, etal. (2012) Bacterial community shift in treated periodontitis patients revealed by ion torrent 16S rRNA gene amplicon sequencing. PLoS One 7:e41606. doi: 10.1371/journal.pone.0041606 PMID: 22870235
2. Romanelli R, Mancini S, Laschinger C, Overall CM, Sodek J, etal. (1999) Activation of neutrophil collagenase in periodontitis. Infect Immun 67:2319-2326. PMID: 10225890
3. Kayal RA (2013) The Role of Osteoimmunology in Periodontal Disease. Biomed Res Int 2013:639368. doi: 10.1155/2013/639368 PMID: 24151615
4. Imamura T (2003) The role of gingipains in the pathogenesis of periodontal disease. J Periodontol 74:111-118. PMID: 12593605
5. Grenier D, Imbeault S, Plamondon P, Grenier G, Nakayama K, etal. (2001) Role of gingipains ingrowth of Porphyromonas gingivalis in the presence of human serum albumin. Infect Immun 69:5166-5172. PMID: 11447200
6. Lewis JP, Dawson JA, Hannis JC, Muddiman D, Macrina FL (1999) Hemoglobinase activity of the lysine gingipain protease (Kgp) of Porphyromonas gingivalis W83. J Bacteriol 181:4905-4913. PMID: 10438761
7. Chen TNK, Belliveau L, Duncan MJ (2001) Porphyromonas gingivalis gingipains and adhesion to epithelial cells. Infect Immun 69:3048-3056. PMID: 11292723
8. Sroka A, Sztukowska M, Potempa J, Travis J, Genco CA (2001) Degradation of host heme proteins by lysine- and arginine-specific cysteine proteinases (gingipains) of Porphyromonas gingivalis. J Bacteriol 183:5609-5616. PMID: 11544223
9. O'Brien-Simpson NM, Pathirana RD, Walker GD, Reynolds EC (2009) Porphyromonas gingivalis RgpA-Kgp proteinase-adhesin complexes penetrate gingival tissue and induce proinflammatory cytokines or apoptosis in a concentration-dependent manner. Infect Immun 77:1246-1261. doi: 10.1128/IAI.01038-08 PMID: 19114547
10. Rika Yasuhara YM (2011) Roles of Gingipains in Periodontal Bone Loss. 53:197-205.
11. Fuchs E, Cleveland DW (1998) A structural scaffolding of intermediate filaments in health and disease. Science 279:514-519. PMID: 9438837
12. Coulombe PA, Omary MB (2002) 'Hard'and'soft' principles defining the structure, function and regulation of keratin intermediate filaments. CurrOpin Cell Biol 14:110-122. PMID: 11792552
13. Moll R, Divo M, Langbein L (2008) The human keratins: biology and pathology. Histochem Cell Biol 129:705-733. doi: 10.1007/s00418-008-0435-6 PMID: 18461349
14. Bragulla HH, Homberger DG (2009) Structure and functions of keratin proteins in simple, stratified, keratinized and cornifiedepithelia. J Anat 214:516-559. doi: 10.1111/j.1469-7580.2009.01066.x PMID: 19422428
15. Rothnagel JA, Seki T, Ogo M, Longley MA, Wojcik SM, etal. (1999) The mouse keratin 6 isoformsare differentially expressed in the hair follicle, footpad, tongue and activated epidermis. Differentiation 65:119-130. PMID: 10550545
16. Takahashi KYB, Yamanishi K, Imamura S, Coulombe PA (1998) The two functional keratin 6 genes of mouse are differentially regulated and evolved independently from their human orthologs. Genomics 53:170-183. PMID: 9790766
17. Habtezion A, Toivola DM, Butcher EC, Omary MB (2005) Keratin-8-deficient mice develop chronic spontaneous Th2 colitis amenable to antibiotic treatment. J Cell Sci 118:1971-1980. PMID: 15840656
18. Wojcik SM, Roop DR (2000) Delayed wound healing in keratin 6a knockout mice. MolCell Biol 20:5248-5255. PMID: 10866680
19. Wojcik SM, Seki T, Longley MA, Petherbridge L, Bundman DS, etal. (1999) Expression of MK6a dominant-negative and C-terminal mutant transgenes in mice has distinct phenotypic consequences in the epidermis and hair follicle. Differentiation 65:97-112. PMID: 10550543
20. Takahashi K (1996) A transgenic mouse model with an inducible skin blistering disease phenotype. Proc Natl Acad Sci U S A 93:14776-14781. PMID: 8962131
21. Komine M, Freedberg IM, Simon M, Milisavljevic V, Blumenberg M (2001) Interleukin-1 induces transcription of keratin K6 in human epidermal keratinocytes. J Invest Dermatol 116:330-338. PMID: 11180011
22. Xu Y, Huang CH, Liu XY, Zhong ZH, Hou WL, etal. (2009) Keratin 17 identified by proteomicanalysis may be involved in tumor angiogenesis. BMB Rep 42:344-349. PMID: 19558792
23. Tancharoen S, Abeyama K, Matsushita K, Kawahara K, Sangalungkarn V, et al. (2008) The role of water channel aquaporin3 in the mechanism of TNF-alpha-mediated proinflammatory events: Implication in periodontal inflammation. J Cell Physiol 217:338-349. doi: 10.1002/jcp. 21506 PMID: 18543247
24. Somerman MJ, Imm GR, Foster RA (1998) A comparative study of human periodontal ligament cells and gingival fibroblasts in vitro. J Dent Res 67:66-70.
25. Tancharoen S, Imamura T, Biswas KK, Matsushita K, Tatsuyama S, etal. (2005) Neuropeptide release from dental pulp cells by RgpBviaproteinases-activated receptor-2 signaling. J Immunol 174:5796-5804. PMID: 15843583
26. Fujimura S, Shibata Y, Nakayama K, Nakamura T (1998) Comparative properties of envelope-associated arginine-gingipains and lysine-gingipain of Porphyromonas gingivalis. FEMS Microbiol Lett 163:173-179. PMID: 9673019
27. Kenji T, Nao T, Young-Ok K, Nobuya S, Ushio T, et al. (2009) A new rapid and comprehensive peptidome analysis by one-step direct transfer technology for 1-D elecrophoresis/MALDI mass spectrometry. Biochemical and Biophysical Research Communications 379:110-114. doi: 10.1016/j.bbrc.2008. 12.016 PMID: 19073144
28. Yoshihiko A, Atsushi T, Mayuko M, Takeaki N, Hitoshi I, etal. (2011) Quantitative peptidomicanalysis by a newly developed one-step direct transfer technology without depletion of major blood proteins: Its potential utility for monitoring of pathophysiological status in pregnancy-induced hypertension. Proteomics 11:2727-2737. doi: 10.1002/pmic.201000753 PMID: 21630454
29. Tetsuya A, Naoko Y, Kaneyuki T, Hiroshi S, Ko-ichi KA, etal. (2003) Synoviolin/Hrd1, an E3 ubiquitin ligase, as a novel pathogenic factor for arthropathy. Genes Dev 17:2436-2449. PMID: 12975321
30. Noursadeghi M, Haustein T, Miller RF, Chain BM, Katz DR (2008) Quantitative imaging assay for NF-kappaB nuclear translocation in primary human macrophages. J Immunol Methods 329:194-200. PMID: 18036607
31. Kamath L, Foss F, Kuliopulos A (2001) Signaling from protease-activated receptor-1 inhibits migration and invasion of breast cancer cells. Cancer Res 61:5933-5940. PMID: 11479236
32. Dey M, Su LY, Segall AM (2013) Tumor Cell Death Mediated by Peptides That Recognize Branched Intermediates of DNA Replication and Repair. PLoS One 8:e78751. doi: 10.1371/journal.pone.0078751 PMID: 24244353
33. Subrahmanyam MV (2003) G ingival crevicular fluid a marker of the periodontal disease activity. Indian J Clin Biochem 18:5-7. doi: 10.1007/BF02867658 PMID: 23105364
34. Gibson FC, Van Dyke TE, Genco CA (2005) Gingipain-specific IgG in the sera of patients with periodontal disease is necessary for opsonophagocytosis of Porphyromonas gingivalis. J Periodontol 76:1629-1636. PMID: 16253083
35. NM-005555.3 NRS (2014) Homo sapiens keratin 6B (KRT6B), mRNA.
36. Veith PD, Chen YY, Reynolds EC (2004) Porphyromonas gingivalis RgpA and Kgp proteinases and adhesins are C terminally processed by the carboxypeptidase CPG70. Infect Immun 72:3655-3657. PMID: 15155679
37. Ara T, Kurata K, Hirai K, Uchihashi T, Uematsu T, etal. (2009) Human gingival fibroblasts are critical in sustaining inflammation in periodontal disease. J Periodontal Res 44:21-27. doi: 10.1111/j.1600-0765.2007.01041.x PMID: 19515019
38. Graves DT (1999) The potential role of chemokines and inflammatory cytokines in periodontal disease progression. Clin Infect Dis 28:482-490. PMID: 10194065
39. Kinane DFGJ, Gorr SU, Stathopoulou PG, Benakanakere M (2008) P.gingivalis interactions with epithelial cells. Frontiers in Bioscience 13:966-984. PMID: 17981604
40. James A, Kinane MRB, Zhao J, Kavita B, Denis F (2012) Porphyromonas gingivalis influences actin degradation within epithelial cells during invasion and apoptosis. Cellular Microbiology 14:1085-1096. doi: 10.1111/j.1462-5822.2012.01780.x PMID: 22381126
41. Matthias B, Cimasoni G (1985) The pH of human crevicular fluid measured by a new microanalytical technique. Journal of Periodontal Research 20:35-40. PMID: 3156233
42. Yongqing T, Potempa J, Pike RN, Wijeyewickrema LC (2011) The lysine-specific gingipain of Porphyromonas gingivalis: importance to pathogenicity and potential strategies for inhibition. Adv Exp Med Biol 712:15-29. doi: 10.1007/978-1-4419-8414-2 2 PMID: 21660656
43. Chen AL, Johnson KA, Lee JK, Sutterlin C, Tan M (2012) CPAF: a Chlamydial protease in search of an authentic substrate. PLoS Pathog 8:e1002842. doi: 10.1371/journal.ppat.1002842 PMID: 22876181
44. Dong F, Su H, Huang Y, Zhong Y, Zhong G (2004) Cleavage of host keratin 8 by a Chlamydia-secreted protease. Infect Immun 72:3863-3868. PMID: 15213128
45. Seipelt J, Liebig HD, Sommergruber W, Gerner C, Kuechler E (2000) 2A proteinase of human rhinovirus cleaves cytokeratin 8 in infected HeLacells. J BiolChem 275:20084-20089. PMID: 10867028
46. Senga Y, Hattori T, Yoshida K (1996) Clinical evaluation of soluble cytokeratin 19 fragments (CYFRA 21-1) in serum and urine of patients with bladder cancer. Urology 1996 Nov; 48 (5) :703-10 48:703-710. PMID: 8911513
47. Wong PEC-G, Takahashi K, Gu C, Babinet C, Coulombe PA (2000) Introducing a Null Mutation in the Mouse K6a and K6f3 Genes Reveals Their Essential Structural Role in the Oral Mucosa. The Journal of Cell Biology 150:921-928. PMID: 10953016
48. Andrian E, Grenier D, Rouabhia M (2004) In vitro models of tissue penetration and destruction by Porphyromonas gingivalis. Infect Immun 72:4689-4698. PMID: 15271930
49. Barth K, Remick DG, Genco CA (2013) Disruption of immune regulation by microbial pathogens and resulting chronic inflammation. J Cell Physiol 228:1413-1422. doi: 10.1002/jcp. 24299 PMID: 23255141
50. Rika Y, Miyamoto Y (2011) Roles of Gingipains in Periodontal Bone Loss. Journal of Oral Biosciences 53:197-205.
51. Elisoa A, Yakout M, Mahmoud R, Grenier D (2007) Regulation of matrix metalloproteinases by porphylomonas gingivalis in an engineered human oral mucosa model. Journal of Cellular Physiology 211:56-62. PMID: 17226791
52. Andrian E, Grenier D, Rouabhia M (2006) Porphyromonas gingivalis gingipains mediate the shedding of syndecan-1 from the surface of gingival epithelial cells. Oral Microbiol Immunol 21:123-128. PMID: 16476022
53. Yasuhara R, Miyamoto Y, Takami M, Imamura T, Potempa J, etal. (2009) Lysine-specific gingipain promotes lipopolysaccharide- and active-vitamin D3-induced osteoclast differentiation by degrading osteoprotegerin. Biochem J 419:159-166. doi: 10.1042/BJ20081469 PMID: 19102726
54. Mezyk-Kopec R, Bzowska M, Potempa J, Bzowska M, Jura N, et al. (2005) Inactivation of membrane tumor necrosis factor alpha by gingipains from Porphyromonas gingivalis. Infect Immun 73:1506-1514. PMID: 15731048
55. Silva-Boghossian CM, Colombo AP, Tanaka M, Rayo C, Xiao Y, etal. (2013) Quantitative proteomic analysis of gingival crevicular fluid in different periodontal conditions. PLoSOne 8:e75898. doi: 10. 1371/journal.pone.0075898 PMID: 24098404
56. Uitto VJ (1991) Extracellular Matrix Molecules and their Receptors: An Overview with Special Emphasis on Periodontal Tissues. Crit Rev Oral Biol Med 2:323-354. PMID: 1654140
57. Ekuni D, Tomofuji T, Yamanaka R, Tachibana K, Yamamoto T, et al. (2005) Initial apical migration of junctional epithelium in rats following application of lipopolysaccharide and proteases. J Periodontol 76:43-48. PMID: 15830636
58. Sanale AR, Firth JD, Uitto VJ, Putnins EE (2002) Keratinocyte growth factor (KGF)-1 and -2 protein and gene expression in human gingival fibroblasts. J Periodontal Res 37:66-74. PMID: 11842940
59. Robinson MJCM (1997) Mitogen-activated protein kinase Pathways. CurrOpin Cell Biol 9:180-186. PMID: 9069255
60. Huang C, Jacobson K, Schaller MD (2004) MAP kinases and cell migration. J Cell Sci 117:4619-4628. PMID: 15371522
61. Vanhaesebroeck B, Ahmadi K, Timms J, Katso R, Driscoll PC, etal. (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70:535-602. PMID: 11395417
62. Watanabe K, Nakhjiri SF, Belton CM, Lamont RJ (2001) Association of Mitogen-Activated Protein Kinase Pathways with Gingival Epithelial Cell Responses to Porphyromonas gingivalis Infection. Infect Immun 69:6731-6737. PMID: 11598045
63. Yun-Jung Yoo H-GP, Kim JH, Cha JH, Bak EJ (2013) Induction of IL-6and IL-8 Expression by Leptin Treatment in Periodontal Ligament Cells and Gingival Fibroblasts. International journal of oral biology 38:73-80.
64. Hanazawa YK, Takeshita A, Kumada H, Okithu M, Tanaka S, etal. (1993) Expression of monocyte chemoattractant protein 1 (MCP-1) in adult periodontal disease: increased monocyte chemotactic activity in crevicular fluids and induction of MCP-1 expression in gingival tissues. Infect Immun 61:5219-5224. PMID: 8225596
65. Hirose M, Saito A, Nakagawa T, Yamada S, Okuda K (2001) Expression of cytokines and inducible nitric oxide synthase in inflamed gingival tissue. J Periodontol 72:590-597. PMID: 11394393
66. Graves DT, Jiang Y (1995) Chemokines, a family of chemotactic cytokines. Crit Rev Oral Biol Med 6:109-118. PMID: 7548618
67. Angelucci C, Maulucci G, Lama G, Proietti G, Colabianchi A, etal. (2012) Epithelial-stromal interactions in human breast cancer: effects on adhesion, plasma membrane fluidity and migration speed and directness. PLoS One 7:e50804. doi: 10.1371/journal.pone.0050804 PMID: 23251387
68. Comoglio PM, Filogamo G (1973) Plasma membrane fluidity and surface motility of mouse C-1300 neuroblastoma cells. J Cell Sci 13:415-420. PMID: 4760592