Noncanonical activation of β-catenin by Porphyromonas gingivalis

Infection and Immunity

Volumn 83, Issue 8, 2015, Pages 3195-3203

  Zhou, Yun ^a   Sztukowska, Maryta ^a   Wang, Qian ^a   Inaba, Hiroaki ^b   Potempa, Jan ^a,c   Scott, David A ^a   Wang, Huizhi ^a   Lamont, Richard J ^a  

^a UNIVERSITY OF LOUISVILLE SCHOOL OF MEDICINE   (United States)

^b ASAHI UNIVERSITY   (Japan)

^c JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BETA CATENIN; CYSTEINE PROTEINASE; GINGIPAIN; GLYCOGEN SYNTHASE KINASE 3BETA; MESSENGER RNA; PROTEIN AXIN1; UNCLASSIFIED DRUG; WNT3A PROTEIN; ADHESIN; ARGINGIPAIN, PORPHYROMONAS GINGIVALIS; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA;

ARTICLE; BIOACCUMULATION; CELL FRACTIONATION; CELL NUCLEUS; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; IMMUNOFLUORESCENCE MICROSCOPY; LUCIFERASE ASSAY; NONHUMAN; PERIODONTAL DISEASE; PHENOTYPE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; WESTERN BLOTTING; BACTEROIDACEAE INFECTION; CELL LINE; ENZYMOLOGY; EPITHELIUM CELL; GENETICS; GINGIVA; HUMAN; METABOLISM; MICROBIOLOGY; PROTEIN TRANSPORT;

ADHESINS, BACTERIAL; BACTEROIDACEAE INFECTIONS; BETA CATENIN; CELL LINE; CELL NUCLEUS; CYSTEINE ENDOPEPTIDASES; EPITHELIAL CELLS; GINGIVA; GLYCOGEN SYNTHASE KINASE 3; HUMANS; PORPHYROMONAS GINGIVALIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT;

EID: 84937786099     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00302-15     Document Type: Article

References (75)

1. Darveau RP, Hajishengallis G, Curtis MA. 2012. Porphyromonas gingivalis as a potential community activist for disease. J Dent Res 91:816-820. http://dx.doi.org/10.1177/0022034512453589.
2. Hajishengallis G, Lamont RJ. 2012. Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27:409-419. http://dx.doi.org/10.1111/j.2041-1014.2012.00663.x.
3. Lamont RJ, Jenkinson HF. 1998. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 62:1244-1263.
4. Tribble GD, Lamont RJ. 2010. Bacterial invasion of epithelial cells and spreading in periodontal tissue. Periodontol 2000 52:68-83. http://dx.doi.org/10.1111/j.1600-0757.2009.00323.x.
5. Yilmaz O, Verbeke P, Lamont RJ, Ojcius DM. 2006. Intercellular spreading of Porphyromonas gingivalis infection in primary gingival epithelial cells. Infect Immun 74:703-710. http://dx.doi.org/10.1128/IAI.74.1.703-710.2006.
6. Jauregui CE, Wang Q, Wright CJ, Takeuchi H, Uriarte SM, Lamont RJ. 2013. Suppression of T-cell chemokines by Porphyromonas gingivalis. Infect Immun 81:2288-2295. http://dx.doi.org/10.1128/IAI.00264-13.
7. Lamont RJ, Hajishengallis G. 2015. Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med 21:172-183. http://dx.doi.org/10.1016/j.molmed.2014.11.004.
8. Moffatt CE, Lamont RJ. 2011. Porphyromonas gingivalis induction of microRNA-203 expression controls suppressor of cytokine signaling 3 in gingival epithelial cells. Infect Immun 79:2632-2637. http://dx.doi.org/10.1128/IAI.00082-11.
9. kB RelA/p65. PLoS Pathog 9:e1003326.
10. Hajishengallis G. 2014. The inflammophilic character of the periodontitis- associated microbiota. Mol Oral Microbiol 29:248-257. http://dx.doi.org/10.1111/omi.12065.
11. Curtis MA, Aduse-Opoku J, Rangarajan M. 2001. Cysteine proteases of Porphyromonas gingivalis. Crit Rev Oral Biol Med 12:192-216. http://dx.doi.org/10.1177/10454411010120030101.
12. Nakayama K. 2015. Porphyromonas gingivalis and related bacteria: from colonial pigmentation to the type IX secretion system and gliding motility. J Periodontal Res 50:1-8. http://dx.doi.org/10.1111/jre.12255.
13. Veith PD, Chen YY, Gorasia DG, Chen D, Glew MD, O'Brien-Simpson NM, Cecil JD, Holden JA, Reynolds EC. 2014. Porphyromonas gingivalis outer membrane vesicles exclusively contain outer membrane and periplasmic proteins and carry a cargo enriched with virulence factors. J Proteome Res 13:2420-2432. http://dx.doi.org/10.1021/pr401227e.
14. Mantri CK, Chen CH, Dong X, Goodwin JS, Pratap S, Paromov V, Xie H. 2015. Fimbriae-mediated outer membrane vesicle production and invasion of Porphyromonas gingivalis. Microbiologyopen 4:53-65. http://dx.doi.org/10.1002/mbo3.221.
15. Haurat MF, Aduse-Opoku J, Rangarajan M, Dorobantu L, Gray MR, Curtis MA, Feldman MF. 2011. Selective sorting of cargo proteins into bacterial membrane vesicles. J Biol Chem 286:1269-1276. http://dx.doi.org/10.1074/jbc.M110.185744.
16. Glew MD, Veith PD, Peng B, Chen YY, Gorasia DG, Yang Q, Slakeski N, Chen D, Moore C, Crawford S, Reynolds EC. 2012. PG0026 is the C-terminal signal peptidase of a novel secretion system of Porphyromonas gingivalis. J Biol Chem 287:24605-24617. http://dx.doi.org/10.1074/jbc.M112.369223.
17. Bostanci N, Belibasakis GN. 2012. Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen. FEMS Microbiol Lett 333:1-9. http://dx.doi.org/10.1111/j.1574-6968.2012.02579.x.
18. Whitmore SE, Lamont RJ. 2014. Oral bacteria and cancer. PLoS Pathog 10:e1003933.
19. Atanasova KR, Yilmaz O. 2014. Looking in the Porphyromonas gingivalis cabinet of curiosities: the microbium, the host and cancer association. Mol Oral Microbiol 29:55-66. http://dx.doi.org/10.1111/omi.12047.
20. Mao S, Park Y, Hasegawa Y, Tribble GD, James CE, Handfield M, Stavropoulos MF, Yilmaz O, Lamont RJ. 2007. Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis. Cell Microbiol 9:1997-2007. http://dx.doi.org/10.1111/j.1462-5822.2007.00931.x.
21. Yao L, Jermanus C, Barbetta B, Choi C, Verbeke P, Ojcius DM, Yilmaz O. 2010. Porphyromonas gingivalis infection sequesters proapoptotic Bad through Akt in primary gingival epithelial cells. Mol Oral Microbiol 25:89-101. http://dx.doi.org/10.1111/j.2041-1014.2010.00569.x.
22. Kuboniwa M, Hasegawa Y, Mao S, Shizukuishi S, Amano A, Lamont RJ, Yilmaz O. 2008. Porphyromonas gingivalis accelerates gingival epithelial cell progression through the cell cycle. Microbes Infect 10:122-128. http://dx.doi.org/10.1016/j.micinf.2007.10.011.
23. Handfield M, Mans JJ, Zheng G, Lopez MC, Mao S, Progulske-Fox A, Narasimhan G, Baker HV, Lamont RJ. 2005. Distinct transcriptional profiles characterize oral epithelium-microbiota interactions. Cell Microbiol 7:811-823. http://dx.doi.org/10.1111/j.1462-5822.2005.00513.x.
24. Clevers H, Nusse R. 2012. Wnt/beta-catenin signaling and disease. Cell 149:1192-1205. http://dx.doi.org/10.1016/j.cell.2012.05.012.
25. Kikuchi A, Kishida S, Yamamoto H. 2006. Regulation of Wnt signaling by protein-protein interaction and posttranslational modifications. Exp Mol Med 38:1-10. http://dx.doi.org/10.1038/emm.2006.1.
26. Dierick H, Bejsovec A. 1999. Cellular mechanisms of wingless/Wnt signal transduction. Curr Top Dev Biol 43:153-190.
27. Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, Mills GB, Kobayashi R, Hunter T, Lu Z. 2007. Phosphorylation of β-catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem 282:11221-11229. http://dx.doi.org/10.1074/jbc.M611871200.
28. Huang H, He X. 2008. Wnt/βcatenin signaling: new (and old) players and new insights. Curr Opin Cell Biol 20:119-125. http://dx.doi.org/10.1016/j.ceb.2008.01.009.
29. Brembeck FH, Rosario M, Birchmeier W. 2006. Balancing cell adhesion and Wnt signaling, the key role of βcatenin. Curr Opin Genet Dev 16:51-59. http://dx.doi.org/10.1016/j.gde.2005.12.007.
30. Fracalossi AC, Silva MDS, Oshima CT, Ribeiro DA. 2010. Wnt/betacatenin signaling pathway following rat tongue carcinogenesis induced by 4-nitroquinoline 1-oxide. Exp Mol Pathol 88:176-183. http://dx.doi.org/10.1016/j.yexmp.2009.11.004.
31. Lo Muzio L. 2001. A possible role for the WNT-1 pathway in oral carcinogenesis. Crit Rev Oral Biol Med 12:152-165. http://dx.doi.org/10.1177/10454411010120020501.
32. Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. 2013. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe 14:195-206. http://dx.doi.org/10.1016/j.chom.2013.07.012.
33. Yilmaz O, Watanabe K, Lamont RJ. 2002. Involvement of integrins in fimbria-mediated binding and invasion by Porphyromonas gingivalis. Cell Microbiol 4:305-314. http://dx.doi.org/10.1046/j.1462-5822.2002.00192.x.
34. Nakayama K, Kadowaki T, Okamoto K, Yamamoto K. 1995. Construction and characterization of arginine-specific cysteine proteinase (Arggingipain)- deficient mutants of Porphyromonas gingivalis: evidence for significant contribution of Arg-gingipain to virulence. J Biol Chem 270:23619-23626.
35. Shi Y, Ratnayake DB, Okamoto K, Abe N, Yamamoto K, Nakayama K. 1999. Genetic analyses of proteolysis, hemoglobin binding, and hemagglutination of Porphyromonas gingivalis: construction of mutants with a combination of rgpA, rgpB, kgp, and hagA. J Biol Chem 274:17955-17960.
36. Moffatt-Jauregui CE, Robinson B, de Moya AV, Brockman RD, Roman AV, Cash MN, Culp DJ, Lamont RJ. 2013. Establishment and characterization of a telomerase immortalized human gingival epithelial cell line. J Periodontal Res 48:713-721. http://dx.doi.org/10.1111/jre.12059.
37. Veillard F, Sztukowska M, Mizgalska D, Ksiazek M, Houston J, Potempa B, Enghild JJ, Thogersen IB, Gomis-Ruth FX, Nguyen KA, Potempa J. 2013. Inhibition of gingipains by their profragments as the mechanism protecting Porphyromonas gingivalis against premature activation of secreted proteases. Biochim Biophys Acta 1830:4218-4228. http://dx.doi.org/10.1016/j.bbagen.2013.04.005.
38. Chen JS, Li HC, Lin SI, Yang CH, Chien WY, Syu CL, Lo SY. 2015. Cleavage of dicer protein by I7 protease during vaccinia virus infection. PLoS One 10:e0120390.
39. Hirano T, Beck DA, Wright CJ, Demuth DR, Hackett M, Lamont RJ.2013. Regulon controlled by the GppX hybrid two-component system in Porphyromonas gingivalis. Mol Oral Microbiol 28:70-81. http://dx.doi.org/10.1111/omi.12007.
40. Moffatt CE, Inaba H, Hirano T, Lamont RJ. 2012. Porphyromonas gingivalis SerB-mediated dephosphorylation of host cell cofilin modulates invasion efficiency. Cell Microbiol 14:577-588. http://dx.doi.org/10.1111/j.1462-5822.2011.01743.x.
41. Wang H, Kumar A, Lamont RJ, Scott DA. 2014. GSK3β and the control of infectious bacterial diseases. Trends Microbiol 22:208-217. http://dx.doi.org/10.1016/j.tim.2014.01.009.
42. Duan Y, Liao AP, Kuppireddi S, Ye Z, Ciancio MJ, Sun J. 2007. beta-Catenin activity negatively regulates bacterium-induced inflammation. Lab Invest 87:613-624.
43. Lu R, Wu S, Zhang YG, Xia Y, Liu X, Zheng Y, Chen H, Schaefer KL, Zhou Z, Bissonnette M, Li L, Sun J. 2014. Enteric bacterial protein AvrA promotes colonic tumorigenesis and activates colonic betacatenin signaling pathway. Oncogenesis 3:e105.
44. Silva-Garcia O, Valdez-Alarcon JJ, Baizabal-Aguirre VM. 2014. The Wnt/beta-catenin signaling pathway controls the inflammatory response in infections caused by pathogenic bacteria. Mediators Inflamm 2014:310183. http://dx.doi.org/10.1155/2014/310183.
45. Larabee JL, DeGiusti K, Regens JL, Ballard JD. 2008. Bacillus anthracis edema toxin activates nuclear glycogen synthase kinase 3β. Infect Immun 76:4895-4904. http://dx.doi.org/10.1128/IAI.00889-08.
46. Bezerra Lima B, Faria Fonseca B, da Graca Amado N, Moreira Lima D, Albuquerque Ribeiro R, Garcia Abreu J, de Castro Brito GA. 2014. Clostridium difficile toxin A attenuates Wnt/beta-catenin signaling in intestinal epithelial cells. Infect Immun 82:2680-2687. http://dx.doi.org/10.1128/IAI.00567-13.
47. Rims CR, McGuire JK. 2014. Matrilysin (MMP-7) catalytic activity regulates beta-catenin localization and signaling activation in lung epithelial cells. Exp Lung Res 40:126-136. http://dx.doi.org/10.3109/01902148.2014.890681.
48. Scragg MA, Alsam A, Rangarajan M, Slaney JM, Shepherd P, Williams DM, Curtis MA. 2002. Nuclear targeting of Porphyromonas gingivalis W50 protease in epithelial cells. Infect Immun 70:5740-5750. http://dx.doi.org/10.1128/IAI.70.10.5740-5750.2002.
49. Furuta N, Takeuchi H, Amano A. 2009. Entry of Porphyromonas gingivalis outer membrane vesicles into epithelial cells causes cellular functional impairment. Infect Immun 77:4761-4770. http://dx.doi.org/10.1128/IAI.00841-09.
50. Inaba H, Amano A, Lamont RJ, Murakami Y. Involvement of proteaseactivated receptor 4 in overexpression of matrix metalloproteinase 9 induced by Porphyromonas gingivalis. Med Microbiol Immunol, in press.
51. Inaba H, Sugita H, Kuboniwa M, Iwai S, Hamada M, Noda T, Morisaki I, Lamont RJ, Amano A. 2014. Porphyromonas gingivalis promotes invasion of oral squamous cell carcinoma through induction of proMMP9 and its activation. Cell Microbiol 16:131-145. http://dx.doi.org/10.1111/cmi.12211.
52. Tokuda M, Karunakaran T, Duncan M, Hamada N, Kuramitsu H. 1998. Role of Arg-gingipain A in virulence of Porphyromonas gingivalis. Infect Immun 66:1159-1166.
53. Tancharoen S, Matsuyama T, Kawahara KI, Tanaka K, Lee LJ, Machigashira M, Noguchi K, Ito T, Imamura T, Potempa J, Kikuchi K, Maruyama I. 2015. Cleavage of host cytokeratin-6 by lysine-specific gingipain induces gingival inflammation in periodontitis patients. PLoS One 10:e0117775.
54. Nakayama M, Inoue T, Naito M, Nakayama K, Ohara N. 2015. Attenuation of the PI3 kinase/Akt signaling pathway by Porphyromonas gingivalis gingipains RgpA, RgpB, and Kgp. J Biol Chem 290:5190-5202. http://dx.doi.org/10.1074/jbc.M114.591610.
55. Stafford P, Higham J, Pinnock A, Murdoch C, Douglas CW, Stafford GP, Lambert DW. 2013. Gingipain-dependent degradation of mammalian target of rapamycin pathway proteins by the periodontal pathogen Porphyromonas gingivalis during invasion. Mol Oral Microbiol 28:366-378. http://dx.doi.org/10.1111/omi.12030.
56. Kinane JA, Benakanakere MR, Zhao J, Hosur KB, Kinane DF. 2012. Porphyromonas gingivalis influences actin degradation within epithelial cells during invasion and apoptosis. Cell Microbiol 14:1085-1096. http://dx.doi.org/10.1111/j.1462-5822.2012.01780.x.
57. Inaba H, Kuboniwa M, Sugita H, Lamont RJ, Amano A. 2012. Identification of signaling pathways mediating cell cycle arrest and apoptosis induced by Porphyromonas gingivalis in human trophoblasts. Infect Immun 80:2847-2857. http://dx.doi.org/10.1128/IAI.00258-12.
58. Palm E, Khalaf H, Bengtsson T. 2015. Suppression of inflammatory responses of human gingival fibroblasts by gingipains from Porphyromonas gingivalis. Mol Oral Microbiol 30:74-85. http://dx.doi.org/10.1111/omi.12073.
59. Nishikawa K, Duncan MJ. 2010. Histidine kinase-mediated production and autoassembly of Porphyromonas gingivalis fimbriae. J Bacteriol 192:1975-1987. http://dx.doi.org/10.1128/JB.01474-09.
60. Aduse-Opoku J, Slaney JM, Hashim A, Gallagher A, Gallagher RP, Rangarajan M, Boutaga K, Laine ML, Van Winkelhoff AJ, Curtis MA. 2006. Identification and characterization of the capsular polysaccharide (K-antigen) locus of Porphyromonas gingivalis. Infect Immun 74:449-460. http://dx.doi.org/10.1128/IAI.74.1.449-460.2006.
61. Tribble GD, Kerr JE, Wang BY. 2013. Genetic diversity in the oral pathogen Porphyromonas gingivalis: molecular mechanisms and biological consequences. Future Microbiol 8:607-620. http://dx.doi.org/10.2217/fmb.13.30.
62. Wang J, Dai J, Liu B, Gu S, Cheng L, Liang J. 2013. Porphyromonas gingivalis lipopolysaccharide activates canonical Wnt/βcatenin and p38 MAPK signaling in stem cells from the apical papilla. Inflammation 36:1393-1402. http://dx.doi.org/10.1007/s10753-013-9679-y.
63. Tang Y, Zhou X, Gao B, Xu X, Sun J, Cheng L, Zheng L. 2014. Modulation of Wnt/beta-catenin signaling attenuates periapical bone lesions. J Dent Res 93:175-182. http://dx.doi.org/10.1177/0022034513512507.
64. Xing Q, Ye Q, Fan M, Zhou Y, Xu Q, Sandham A. 2010. Porphyromonas gingivalis lipopolysaccharide inhibits the osteoblastic differentiation of preosteoblasts by activating Notch1 signaling. J Cell Physiol 225:106-114. http://dx.doi.org/10.1002/jcp.22201.
65. Kandasamy AD, Chow AK, Ali MA, Schulz R. 2010. Matrix metalloproteinase-2 and myocardial oxidative stress injury: beyond the matrix. Cardiovasc Res 85:413-423. http://dx.doi.org/10.1093/cvr/cvp268.
66. Herbst A, Jurinovic V, Krebs S, Thieme SE, Blum H, Goke B, Kolligs FT. 2014. Comprehensive analysis of beta-catenin target genes in colorectal carcinoma cell lines with deregulated Wnt/beta-catenin signaling. BMC Genomics 15:74. http://dx.doi.org/10.1186/1471-2164-15-74.
67. Debelec-Butuner B, Alapinar C, Ertunc N, Gonen-Korkmaz C, Yorukoglu K, Korkmaz KS. 2014. TNFβmediated loss of beta-catenin/Ecadherin association and subsequent increase in cell migration is partially restored by NKX3.1 expression in prostate cells. PLoS One 9:e109868.
68. Keerthivasan S, Aghajani K, Dose M, Molinero L, Khan MW, Venkateswaran V, Weber C, Emmanuel AO, Sun T, Bentrem DJ, Mulcahy M, Keshavarzian A, Ramos EM, Blatner N, Khazaie K, Gounari F. 2014.βCatenin promotes colitis and colon cancer through imprinting of proinflammatory properties in T cells. Sci Transl Med 6:225ra28. http://dx.doi.org/10.1126/scitranslmed.3007607.
69. Uraguchi M, Morikawa M, Shirakawa M, Sanada K, Imai K. 2004. Activation of WNT family expression and signaling in squamous cell carcinomas of the oral cavity. J Dent Res 83:327-332. http://dx.doi.org/10.1177/154405910408300411.
70. Chaw SY, Majeed AA, Dalley AJ, Chan A, Stein S, Farah CS. 2012. Epithelial to mesenchymal transition (EMT) biomarkers-E-cadherin, beta-catenin, APC and Vimentin-in oral squamous cell carcinogenesis and transformation. Oral Oncol 48:997-1006. http://dx.doi.org/10.1016/j.oraloncology.2012.05.011.
71. Tanaka N, Odajima T, Ogi K, Ikeda T, Satoh M. 2003. Expression of E-cadherin, alpha-catenin, and beta-catenin in the process of lymph node metastasis in oral squamous cell carcinoma. Br J Cancer 89:557-563. http://dx.doi.org/10.1038/sj.bjc.6601124.
72. Nagy KN, Sonkodi I, Szoke I, Nagy E, Newman HN. 1998. The microflora associated with human oral carcinomas. Oral Oncol 34:304-308. http://dx.doi.org/10.1016/S1368-8375(98)00008-6.
73. Katz J, Onate MD, Pauley KM, Bhattacharyya I, Cha S. 2011. Presence of Porphyromonas gingivalis in gingival squamous cell carcinoma. Int J Oral Sci 3:209-215. http://dx.doi.org/10.4248/IJOS11075.
74. Lang M, Borgmann M, Oberhuber G, Evstatiev R, Jimenez K, Dammann KW, Jambrich M, Khare V, Campregher C, Ristl R, Gasche C. 2013. Thymoquinone attenuates tumor growth in ApcMin mice by interference with Wnt-signaling. Mol Cancer 12:41. http://dx.doi.org/10.1186/1476-4598-12-41.
75. Peng Y, Zhao S, Song L, Wang M, Jiao K. 2013. Sertad1 encodes a novel transcriptional coactivator of SMAD1 in mouse embryonic hearts. Biochem Biophys Res Commun 441:751-756. http://dx.doi.org/10.1016/j.bbrc.2013.10.127.