Research progress in the role and mechanism of Porphyromonas gingivalis in promoting oral squamous cell carcinoma

doi:10.19438/j.cjoms.2023.02.015

Abstract

Abstract: A large number of studies have shown that P.gingivalis is one of the bacterial species, as an important risk factor, of oral squamous cell carcinoma (OSCC). P.gingivalis is closely associated with the pathogenicity, development, invasion, metastasis and prognosis of OSCC. For its potential mechanisms, it may accelerate OSCC occurrence and progress probably through multiple ways as follows: resisting and destroying the innate immune system of the host, promoting epithelial-mesenchymal transition, promoting cancerous invasion and metastasis, inhibiting cell apoptosis, activating cell proliferation. This review summarized the research progress in the role and mechanism of P.gingivalis in promoting OSCC.

Key words: Porphyromonas gingivalis, Oral squamous cell carcinoma, Mechanism of action

CLC Number:

R739.8

REZIWANGULI·Yasen, MAIREPATI·Maiming, LI Chen-xi, GONG Zhong-cheng. Research progress in the role and mechanism of Porphyromonas gingivalis in promoting oral squamous cell carcinoma[J]. China Journal of Oral and Maxillofacial Surgery, 2023, 21(2): 186-190.

References

[1] Dewhirst FE, Chen T, Izard J, et al.The human oral micro- biome[J].J Bacteriol, 2010, 192(19): 5002-5017.
[2] Hajishengallis G.Porphyromonas gingivalis-host interactions: open war or intelligent guerilla tactics?[J]. Microbes Infect, 2009,11(6-7): 637-645.
[3] 黄定明,吴亚菲,周学东.牙龈卟啉单胞菌的分型及其致病作用[J].国外医学(口腔医学册), 2002, 29(4): 213-215.
Huang DM, Wu YF, Zhou XD.Classification and pathogenic role of Porphyromonas gingivalis[J]. International Journal of Stomatology, 2002, 29(4): 213-215.
[4] Bray F, Ferlay J, Soerjomataram I, et al.Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries[J].CA Cancer J Clin, 2018, 68(6): 394-424.
[5] Wen L, Mu W, Lu H, et al.Porphyromonas gingivalis promotes oral squamous cell carcinoma progression in an immune microenvironment[J].J Dent Res, 2020, 99(6): 666-675.
[6] Torre LA, Sauer AM, Chen MS Jr, et al.Cancer statistics for Asian Americans, Native Hawaiians, and Pacific Islanders, 2016: converging incidence in males and females[J] .CA Cancer J Clin, 2016, 66(3): 182-202.
[7] Grivennikov SI, Greten FR, Karin M.Immunity, inflammation, and cancer[J]. Cell, 2010, 140(6): 883-899.
[8] aiswal S, Chao MP, Majeti R, et al. Macrophages as mediators of tumor immunosurveillance[J]. Trends Immunol, 2010, 31(6): 212-219.
[9] Willingham SB, Volkmer JP, Gentles AJ, et al.The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors[J]. Proc Natl Acad Sci USA, 2012, 109(17): 6662-6667.
[10] Liu S, Zhou X, Peng X, et al.Porphyromonas gingivalis promotes immunoevasion of oral cancer by protecting cancer from macrophage attack[J]. J Immunol, 2020,205(1): 282-289.
[11] Yahaya MAF, Lila MAM, Ismail S, et al.Tumour-associated macrophages (TAMs) in colon cancer and how to reeducate them[J].J Immunol Res, 2019: 2368249.
[12] Song H,Lou C,Ma J, et al.Single-cell transcriptome analysis reveals changes of tumor immune microenvironment in oral squamous cell carcinoma after chemotherapy[J]. Front Cell Dev Biol, 2022,10: 914120.
[13] Santambrogio L.Molecular determinants regulating the plasticity of the MHC ClassⅡimmunopeptidome[J]. Front Immunol, 2022, 13: 878271.
[14] Chen Y, Su Y, Chang M,et al.Low-level MHC Class Ⅱ expression leads to suboptimal Th cell response, increased autoaggression, and heightened cytokine inducibility[J].J Immunol, 2017, 198(5): 1928-1943.
[15] Liu Y, Cao X.The origin and function of tumor-associated macrophages[J]. Cell Mol Immunol, 2015, 12(1): 1-4.
[16] Yang L, Zhang Y.Tumor-associated macrophages: from basic research to clinical application[J]. J Hematol Oncol, 2017, 10(1): 58-70.
[17] El-Awady Ahmed R, Miles B, Scisci E, et al. Porphyromonas gingivalis evasion of autophagy and intracellular killing by human myeloid dendritic cells involves DC-SIGN-TLR2 crosstalk[J]. PLoS Pathog, 2015, 10(2): e1004647.
[18] Arjunan P, Meghil MM, Pi W, et al.Oral pathobiont activates anti-apoptotic pathway, promoting both immune suppression and oncogenic cell proliferation[J]. Sci Rep, 2018, 8(1): 16607.
[19] Irfan M, Delgado RZR, Frias-Lopez J.The oral microbiome and cancer[J]. Front Immunol, 2020, 11: 591088-591128.
[20] Geng F, Liu J, Guo Y, et al.Porphyromonas gingivalis persistent exposure to promotes proliferative and invasion capabilities, and tumorigenic properties of human immortalized oral epithelial cells[J]. Front Cell Infect Microbiol, 2017,7(1): 57-73.
[21] Inaba H, Sugita H, Kuboniwa M, et al.Porphyromonas gingivalis promotes invasion of oral squamous cell carcinoma through induction of proMMP9 and its activation[J]. Cell Microbiol, 2014, 16(1): 131-145.
[22] Harris TM, Du P, Kawachi N, et al.Proteomic analysis of oral cavity squamous cell carcinoma specimens identifies patient outcome-associated proteins[J]. Arch Pathol Lab Med, 2015, 139(4): 494-507.
[23] Perera M, Al-Hebshi NN, Speicher DJ, et al.Emerging role of bacteria in oral carcinogenesis: a review with special reference to perio-pathogenic bacteria[J]. J Oral Microbiol, 2016, 8: 32762-32772.
[24] Inaba Hiroaki, Sugita Hideyuki, Kuboniwa Masae, et al.Porphyromonas gingivalis promotes invasion of oral squamous cell carcinoma through induction of proMMP9 and its activation[J]. Cell Microbiol, 2014, 16(1): 131-145.
[25] Fitzsimonds ZR, Rodriguez-Hernandez CJ, Bagaitkar J, et al.From beyond the pale to the pale riders: the emerging association of bacteria with oral cancer[J]. J Dent Res, 2020, 99(6): 604-612.
[26] Sztukowska MN, Ojo A, Ahmed S, et al.Porphyromonas gingivalis initiates a mesenchymal-like transition through ZEB1 in gingival epithelial cells[J]. Cell Microbiol, 2016, 18(6): 844-858.
[27] Valle-Mendiola A, Soto-Cruz I.Energy metabolism in cancer: the roles of STAT3 and STAT5 in the regulation of metabolism-related genes[J]. Cancers (Basel), 2020, 12(1): 124-147.
[28] Heppler LN, Frank DA.Targeting oncogenic transcription factors: therapeutic implications of endogenous STAT inhibitors[J]. Trends Cancer, 2017, 3(12): 816-827.
[29] Egusquiaguirre SP, Yeh JE, Walker SR, et al.The STAT3 target gene TNFRSF1A modulates the NF-κB pathway in breast cancer cells[J]. Neoplasia, 2018, 20(5): 489-498.
[30] Tošic I, Frank DA.STAT3 as a mediator of oncogenic cellular metabolism: pathogenic and therapeutic implications[J]. Neoplasia, 2021, 23(12): 1167-1178.
[31] Landskron G, De la Fuente M, Thuwajit P, et al. Chronic inflammation and cytokines in the tumor microenvironment[J]. J Immunol Res, 2014: 149185.
[32] Andrian E, Grenier D, Rouabhia M. In vitro models of tissue penetration and destruction by Porphyromonas gingivalis[J]. Infect Immun, 2004, 72(8): 4689-4698.
[33] Kuboniwa M, Hasegawa Y, Mao S, et al.P.gingivalis accelerates gingival epithelial cell progression through the cell cycle[J]. Microbes Infect, 2008,10(2): 122-128.
[34] Chang C,Wang H, Liu J, et al.Porphyromonas gingivalis infection promoted the proliferation of oral squamous cell carcinoma cells through the miR-21/PDCD4/AP-1 negative signaling pathway[J].ACS Infect Dis, 2019, 5(8): 1336-1347.
[35] Zhou Y, Sztukowska M, Wang Q, et al.Noncanonical activation of beta-catenin by Porphyromonas gingivalis[J]. Infect Immun, 2015,83(8): 3195-3203.
[36] Mao S, Park Y, Hasegawa Y, et al.Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis[J]. Cell Microbiol, 2007, 9(8): 1997-2007.
[37] Yilmaz O, Jungas T, Verbeke P, et al.Activation of the phosphati-dylinositol 3-kinase/Akt pathway contributes to survival of primary epithelial cells infected with the periodontal pathogen Porphyromonas gingivalis[J]. Infect Immun, 2004, 72(7): 3743-3751.
[38] Yao L, Jermanus C, Barbetta B, et al.Porphyromonas gingivalis infection sequesters pro-apoptotic Bad through Akt in primary gingival epithelial cells[J]. Mol Oral Microbiol, 2010, 25(2): 89-101.
[39] Moffatt CE, Lamont RJ.Porphyromonas gingivalis induction of microRNA-203 expression controls suppressor of cytokine signaling 3 in gingival epithelial cells[J]. Infect Immun, 2011, 79(7): 2632-2637.
[40] Fan X, Alekseyenko AV, Wu J, et al.Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study[J]. Gut, 2018, 67(1): 120-127.
[41] Wang X, Jia Y, Wen L, et al.Correction: Porphyromonas gingivalis promotes colorectal carcinoma by activating the hematopoietic NLRP3 inflammasome[J]. Cancer Res, 2022, 82(11): 2196.
[42] Hussain M, Stover CM, Dupont A.P.gingivalis in periodontal disease and atherosclerosis - scenes of action for antimicrobial peptides and complement[J].Front Immunol, 2015, 6(1): 45-50.
[43] Schulz S, Schlitt A, Hofmann B, et al.Periodontal pathogens and their role in cardiovascular outcome[J]. J Clin Periodontol, 2020, 47(12): 173-181.
[44] Yamada C, Akkaoui J, Ho A, et al.Potential role of phosphoglycerol dihydroceramide produced by periodontal pathogen Porphyromonas gingivalis in the pathogenesis of Alzheimer's disease[J] .Front Immunol, 2020, 11: 591571.
[45] Zhang J, Yu C, Zhang X, et al.Porphyromonas gingivalis lipopolysaccharide induces cognitive dysfunction, mediated by neuronal inflammation via activation of the TLR4 signaling pathway in C57BL/6 mice[J]. J Neuroinflammation, 2018, 15(1): 37-51.
[46] Wang Y, Kang X, Cao Y, et al.Porphyromonas gingivalis induces depression via downregulating p75NTR-mediated BDNF maturation in astrocytes[J]. Brain Behav Immun, 2019, 81: 523-534.