Abstract
Porphyromonas gingivalis is an oral pathogen with the ability to induce oral dysbiosis and periodontal disease. Nevertheless, the mechanisms by which P. gingivalis could abrogate the host–microbe symbiotic relationship leading to oral dysbiosis remain unclear. We have recently demonstrated that P. gingivalis specifically increased the antimicrobial properties of oral epithelial cells, through a strong induction of the expression of PLA2-IIA in a mechanism that involves activation of the Notch-1 receptor. Moreover, gingival expression of PLA2-IIA was significantly increased during initiation and progression of periodontal disease in non-human primates and interestingly, those PLA2-IIA expression changes were concurrent with oral dysbiosis. In this chapter, we present an innovative hypothesis of a potential mechanism involved in P. gingivalis-induced oral dysbiosis and inflammation based on our previous observations and a robust body of literature that supports the antimicrobial and proinflammatory properties of PLA2-IIA as well as its role in other chronic inflammatory diseases.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Al-Attar, A., Alimova, Y., Kirakodu, S., Kozal, A., Novak, M. J., Stromberg, A. J., et al. (2018). Activation of Notch-1 in oral epithelial cells by P. gingivalis triggers the expression of the antimicrobial protein PLA2-IIA. Mucosal Immunology, 11(4), 1047–1059.
Atsumi, G., Murakami, M., Tajima, M., Shimbara, S., Hara, N., & Kudo, I. (1997). The perturbed membrane of cells undergoing apoptosis is susceptible to type II secretory phospholipase A2 to liberate arachidonic acid. Biochimica et Biophysica Acta, 1349(1), 43–54.
Augert, A., Payre, C., de Launoit, Y., Gil, J., Lambeau, G., & Bernard, D. (2009). The M-type receptor PLA2R regulates senescence through the p53 pathway. EMBO Reports, 10(3), 271–277.
Baek, S. H., Kwon, T. K., Lim, J. H., Lee, Y. J., Chang, H. W., Lee, S. J., et al. (2000). Secretory phospholipase A2-potentiated inducible nitric oxide synthase expression by macrophages requires NF-kappa B activation. Journal of Immunology, 164(12), 6359–6365.
Baek, S. H., Lim, J. H., Park, D. W., Kim, S. Y., Lee, Y. H., Kim, J. R., et al. (2001). Group IIA secretory phospholipase A(2) stimulates inducible nitric oxide synthase expression via ERK and NF-kappaB in macrophages. European Journal of Immunology, 31(9), 2709–2717.
Baker, P. J., Dixon, M., & Roopenian, D. C. (2000). Genetic control of susceptibility to Porphyromonas gingivalis-induced alveolar bone loss in mice. Infection and Immunity, 68(10), 5864–5868.
Baumler, A. J., & Sperandio, V. (2016). Interactions between the microbiota and pathogenic bacteria in the gut. Nature, 535(7610), 85–93.
Bayburt, T., Yu, B. Z., Lin, H. K., Browning, J., Jain, M. K., & Gelb, M. H. (1993). Human nonpancreatic secreted phospholipase A2: Interfacial parameters, substrate specificities, and competitive inhibitors. Biochemistry, 32(2), 573–582.
Beers, S. A., Buckland, A. G., Koduri, R. S., Cho, W., Gelb, M. H., & Wilton, D. C. (2002). The antibacterial properties of secreted phospholipases A2: A major physiological role for the group IIA enzyme that depends on the very high pI of the enzyme to allow penetration of the bacterial cell wall. The Journal of Biological Chemistry, 277(3), 1788–1793.
Boekholdt, S. M., Keller, T. T., Wareham, N. J., Luben, R., Bingham, S. A., Day, N. E., et al. (2005). Serum levels of type II secretory phospholipase A2 and the risk of future coronary artery disease in apparently healthy men and women: The EPIC-Norfolk Prospective Population Study. Arteriosclerosis, Thrombosis, and Vascular Biology, 25(4), 839–846.
Bomalaski, J. S., Lawton, P., & Browning, J. L. (1991). Human extracellular recombinant phospholipase A2 induces an inflammatory response in rabbit joints. Journal of Immunology, 146(11), 3904–3910.
Boudreau, L. H., Duchez, A. C., Cloutier, N., Soulet, D., Martin, N., Bollinger, J., et al. (2014). Platelets release mitochondria serving as substrate for bactericidal group IIA-secreted phospholipase A2 to promote inflammation. Blood, 124(14), 2173–2183.
Brawner, K. M., Kumar, R., Serrano, C. A., Ptacek, T., Lefkowitz, E., Morrow, C. D., et al. (2017). Helicobacter pylori infection is associated with an altered gastric microbiota in children. Mucosal Immunology, 10(5), 1169–1177.
Brglez, V., Lambeau, G., & Petan, T. (2014). Secreted phospholipases A2 in cancer: Diverse mechanisms of action. Biochimie, 107(Pt A), 114–123.
Camelo-Castillo, A., Novoa, L., Balsa-Castro, C., Blanco, J., Mira, A., & Tomas, I. (2015). Relationship between periodontitis-associated subgingival microbiota and clinical inflammation by 16S pyrosequencing. Journal of Clinical Periodontology, 42(12), 1074–1082.
Carding, S., Verbeke, K., Vipond, D. T., Corfe, B. M., & Owen, L. J. (2015). Dysbiosis of the gut microbiota in disease. Microbial Ecology in Health and Disease, 26, 26191.
Chalbot, S., Zetterberg, H., Blennow, K., Fladby, T., Grundke-Iqbal, I., & Iqbal, K. (2009). Cerebrospinal fluid secretory Ca2+-dependent phospholipase A2 activity is increased in Alzheimer disease. Clinical Chemistry, 55(12), 2171–2179.
Chung, W. O., & Dale, B. A. (2008). Differential utilization of nuclear factor-kappaB signaling pathways for gingival epithelial cell responses to oral commensal and pathogenic bacteria. Oral Microbiology and Immunology, 23(2), 119–126.
Chung, W. O., Dommisch, H., Yin, L., & Dale, B. A. (2007). Expression of defensins in gingiva and their role in periodontal health and disease. Current Pharmaceutical Design, 13(30), 3073–3083.
Church, W. B., Inglis, A. S., Tseng, A., Duell, R., Lei, P. W., Bryant, K. J., et al. (2001). A novel approach to the design of inhibitors of human secreted phospholipase A2 based on native peptide inhibition. The Journal of Biological Chemistry, 276(35), 33156–33164.
Crowl, R. M., Stoller, T. J., Conroy, R. R., & Stoner, C. R. (1991). Induction of phospholipase A2 gene expression in human hepatoma cells by mediators of the acute phase response. The Journal of Biological Chemistry, 266(4), 2647–2651.
Culmsee, C., & Landshamer, S. (2006). Molecular insights into mechanisms of the cell death program: Role in the progression of neurodegenerative disorders. Current Alzheimer Research, 3(4), 269–283.
Cupillard, L., Mulherkar, R., Gomez, N., Kadam, S., Valentin, E., Lazdunski, M., et al. (1999). Both group IB and group IIA secreted phospholipases A2 are natural ligands of the mouse 180-kDa M-type receptor. The Journal of Biological Chemistry, 274(11), 7043–7051.
da Silva-Boghossian, C. M., do Souto, R. M., Luiz, R. R., & Colombo, A. P. (2011). Association of red complex, A. actinomycetemcomitans and non-oral bacteria with periodontal diseases. Archives of Oral Biology, 56(9), 899–906.
Dale, B. A. (2002). Periodontal epithelium: A newly recognized role in health and disease. Periodontology 2000, 30, 70–78.
Darveau, R. P., Belton, C. M., Reife, R. A., & Lamont, R. J. (1998). Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis. Infection and Immunity, 66(4), 1660–1665.
de Pablo, P., Chapple, I. L., Buckley, C. D., & Dietrich, T. (2009). Periodontitis in systemic rheumatic diseases. Nature Reviews Rheumatology, 5(4), 218–224.
DeGruttola, A. K., Low, D., Mizoguchi, A., & Mizoguchi, E. (2016). Current understanding of dysbiosis in disease in human and animal models. Inflammatory Bowel Diseases, 22(5), 1137–1150.
Dommisch, H., Reinartz, M., Backhaus, T., Deschner, J., Chung, W., & Jepsen, S. (2012). Antimicrobial responses of primary gingival cells to Porphyromonas gingivalis. Journal of Clinical Periodontology, 39(10), 913–922.
Dong, Z., Liu, Y., Scott, K. F., Levin, L., Gaitonde, K., Bracken, R. B., et al. (2010). Secretory phospholipase A2-IIa is involved in prostate cancer progression and may potentially serve as a biomarker for prostate cancer. Carcinogenesis, 31(11), 1948–1955.
Dore, E., & Boilard, E. (2019). Roles of secreted phospholipase A2 group IIA in inflammation and host defense. Biochimica et Biophysica Acta—Molecular and Cell Biology of Lipids, 1864(6), 789–802.
Duchez, A. C., Boudreau, L. H., Naika, G. S., Bollinger, J., Belleannee, C., Cloutier, N., et al. (2015). Platelet microparticles are internalized in neutrophils via the concerted activity of 12-lipoxygenase and secreted phospholipase A2-IIA. Proceedings of the National Academy of Sciences of the United States of America, 112(27), E3564–E3573.
Dutzan, N., Kajikawa, T., Abusleme, L., Greenwell-Wild, T., Zuazo, C. E., Ikeuchi, T., et al. (2018). A dysbiotic microbiome triggers TH17 cells to mediate oral mucosal immunopathology in mice and humans. Science Translational Medicine, 10(463), eaat0797.
Eom, T., Kim, Y. S., Choi, C. H., Sadowsky, M. J., & Unno, T. (2018). Current understanding of microbiota- and dietary-therapies for treating inflammatory bowel disease. Journal of Microbiology, 56(3), 189–198.
Fonteh, A. N., Bass, D. A., Marshall, L. A., Seeds, M., Samet, J. M., & Chilton, F. H. (1994). Evidence that secretory phospholipase A2 plays a role in arachidonic acid release and eicosanoid biosynthesis by mast cells. Journal of Immunology, 152(11), 5438–5446.
Foreman-Wykert, A. K., Weinrauch, Y., Elsbach, P., & Weiss, J. (1999). Cell-wall determinants of the bactericidal action of group IIA phospholipase A2 against Gram-positive bacteria. The Journal of Clinical Investigation, 103(5), 715–721.
Fujita, M., Zhu, K., Fujita, C. K., Zhao, M., Lam, K. S., Kurth, M. J., et al. (2015). Proinflammatory secreted phospholipase A2 type IIA (sPLA-IIA) induces integrin activation through direct binding to a newly identified binding site (site 2) in integrins alphavbeta3, alpha4beta1, and alpha5beta1. The Journal of Biological Chemistry, 290(1), 259–271.
Ganesan, K., Ivanova, T., Wu, Y., Rajasegaran, V., Wu, J., Lee, M. H., et al. (2008). Inhibition of gastric cancer invasion and metastasis by PLA2G2A, a novel beta-catenin/TCF target gene. Cancer Research, 68(11), 4277–4286.
Garcia-Garcia, H. M., & Serruys, P. W. (2009). Phospholipase A2 inhibitors. Current Opinion in Lipidology, 20(4), 327–332.
Ghosh, S. K., Feng, Z., Fujioka, H., Lux, R., McCormick, T. S., & Weinberg, A. (2018). Conceptual perspectives: Bacterial antimicrobial peptide induction as a novel strategy for symbiosis with the human host. Frontiers in Microbiology, 9, 302.
Gibson, F. C., 3rd, Yumoto, H., Takahashi, Y., Chou, H. H., & Genco, C. A. (2006). Innate immune signaling and Porphyromonas gingivalis-accelerated atherosclerosis. Journal of Dental Research, 85(2), 106–121.
Granata, F., Petraroli, A., Boilard, E., Bezzine, S., Bollinger, J., Del Vecchio, L., et al. (2005). Activation of cytokine production by secreted phospholipase A2 in human lung macrophages expressing the M-type receptor. Journal of Immunology, 174(1), 464–474.
Greer, A., Zenobia, C., & Darveau, R. P. (2013). Defensins and LL-37: A review of function in the gingival epithelium. Periodontology 2000, 63(1), 67–79.
Griveau, A., Wiel, C., Le Calve, B., Ziegler, D. V., Djebali, S., Warnier, M., et al. (2018). Targeting the phospholipase A2 receptor ameliorates premature aging phenotypes. Aging Cell, 17(6), e12835.
Gronroos, J. O., Laine, V. J., & Nevalainen, T. J. (2002). Bactericidal group IIA phospholipase A2 in serum of patients with bacterial infections. The Journal of Infectious Diseases, 185(12), 1767–1772.
Gronroos, J. O., Salonen, J. H., Viander, M., Nevalainen, T. J., & Laine, V. J. (2005). Roles of group IIA phospholipase A2 and complement in killing of bacteria by acute phase serum. Scandinavian Journal of Immunology, 62(4), 413–419.
Hajishengallis, G., Liang, S., Payne, M. A., Hashim, A., Jotwani, R., Eskan, M. A., et al. (2011). Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host & Microbe, 10(5), 497–506.
Hayashi, C., Gudino, C. V., Gibson, F. C., 3rd, & Genco, C. A. (2010). Review: Pathogen-induced inflammation at sites distant from oral infection: Bacterial persistence and induction of cell-specific innate immune inflammatory pathways. Molecular Oral Microbiology, 25(5), 305–316.
Hernandez, M., Fuentes, L., Fernandez Aviles, F. J., Crespo, M. S., & Nieto, M. L. (2002). Secretory phospholipase A(2) elicits proinflammatory changes and upregulates the surface expression of fas ligand in monocytic cells: Potential relevance for atherogenesis. Circulation Research, 90(1), 38–45.
Hosokawa, I., Hosokawa, Y., Komatsuzawa, H., Goncalves, R. B., Karimbux, N., Napimoga, M. H., et al. (2006). Innate immune peptide LL-37 displays distinct expression pattern from beta-defensins in inflamed gingival tissue. Clinical and Experimental Immunology, 146(2), 218–225.
Ibeas, E., Fuentes, L., Martin, R., Hernandez, M., & Nieto, M. L. (2009). Secreted phospholipase A2 type IIA as a mediator connecting innate and adaptive immunity: New role in atherosclerosis. Cardiovascular Research, 81(1), 54–63.
Ilic, D., Bollinger, J. M., Gelb, M., & Mauro, T. M. (2014). sPLA2 and the epidermal barrier. Biochimica et Biophysica Acta, 1841(3), 416–421.
Ishida, H., Shinohara, H., Nagata, T., Nishikawa, S., & Wakano, Y. (1994). Phospholipase A(2) activity in gingival crevicular fluid from patients with periodontal disease: A possible marker of disease activity. Mediators of Inflammation, 3(1), 17–21.
Ishizaki, J., Ohara, O., Nakamura, E., Tamaki, M., Ono, T., Kanda, A., et al. (1989). cDNA cloning and sequence determination of rat membrane-associated phospholipase A2. Biochemical and Biophysical Research Communications, 162(3), 1030–1036.
Jacques, C., Bereziat, G., Humbert, L., Olivier, J. L., Corvol, M. T., Masliah, J., et al. (1997). Posttranscriptional effect of insulin-like growth factor-I on interleukin-1beta-induced type II-secreted phospholipase A2 gene expression in rabbit articular chondrocytes. The Journal of Clinical Investigation, 99(8), 1864–1872.
Jamal, O. S., Conaghan, P. G., Cunningham, A. M., Brooks, P. M., Munro, V. F., & Scott, K. F. (1998). Increased expression of human type IIa secretory phospholipase A2 antigen in arthritic synovium. Annals of the Rheumatic Diseases, 57(9), 550–558.
Jang, S. E., Jeong, J. J., Kim, J. K., Han, M. J., & Kim, D. H. (2018). Simultaneous amelioratation of colitis and liver injury in mice by Bifidobacterium longum LC67 and Lactobacillus plantarum LC27. Scientific Reports, 8(1), 7500.
Jaross, W., Eckey, R., & Menschikowski, M. (2002). Biological effects of secretory phospholipase A(2) group IIA on lipoproteins and in atherogenesis. European Journal of Clinical Investigation, 32(6), 383–393.
Jauregui, C. E., Wang, Q., Wright, C. J., Takeuchi, H., Uriarte, S. M., & Lamont, R. J. (2013). Suppression of T-cell chemokines by Porphyromonas gingivalis. Infection and Immunity, 81(7), 2288–2295.
Jensen, M. D., Sheng, W., Simonyi, A., Johnson, G. S., Sun, A. Y., & Sun, G. Y. (2009). Involvement of oxidative pathways in cytokine-induced secretory phospholipase A2-IIA in astrocytes. Neurochemistry International, 55(6), 362–368.
Ji, S., Kim, Y., Min, B. M., Han, S. H., & Choi, Y. (2007). Innate immune responses of gingival epithelial cells to nonperiodontopathic and periodontopathic bacteria. Journal of Periodontal Research, 42(6), 503–510.
Jiang, J., Neubauer, B. L., Graff, J. R., Chedid, M., Thomas, J. E., Roehm, N. W., et al. (2002). Expression of group IIA secretory phospholipase A2 is elevated in prostatic intraepithelial neoplasia and adenocarcinoma. The American Journal of Pathology, 160(2), 667–671.
Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L., & Gordon, J. I. (2011). Human nutrition, the gut microbiome and the immune system. Nature, 474(7351), 327–336.
Kennedy, B. P., Payette, P., Mudgett, J., Vadas, P., Pruzanski, W., Kwan, M., et al. (1995). A natural disruption of the secretory group II phospholipase A2 gene in inbred mouse strains. The Journal of Biological Chemistry, 270(38), 22378–22385.
Khalaf, H., Nakka, S. S., Sanden, C., Svard, A., Hultenby, K., Scherbak, N., et al. (2016). Antibacterial effects of Lactobacillus and bacteriocin PLNC8 alphabeta on the periodontal pathogen Porphyromonas gingivalis. BMC Microbiology, 16(1), 188.
Koduri, R. S., Gronroos, J. O., Laine, V. J., Le Calvez, C., Lambeau, G., Nevalainen, T. J., et al. (2002). Bactericidal properties of human and murine groups I, II, V, X, and XII secreted phospholipases A(2). Journal of Biological Chemistry, 277(8), 5849–5857.
Koll-Klais, P., Mandar, R., Leibur, E., Marcotte, H., Hammarstrom, L., & Mikelsaar, M. (2005). Oral lactobacilli in chronic periodontitis and periodontal health: Species composition and antimicrobial activity. Oral Microbiology and Immunology, 20(6), 354–361.
Kortekangas, P., Aro, H. T., & Nevalainen, T. J. (1994). Group II phospholipase A2 in synovial fluid and serum in acute arthritis. Scandinavian Journal of Rheumatology, 23(2), 68–72.
Kramer, R. M., Hession, C., Johansen, B., Hayes, G., McGray, P., Chow, E. P., et al. (1989). Structure and properties of a human non-pancreatic phospholipase A2. The Journal of Biological Chemistry, 264(10), 5768–5775.
Kugiyama, K., Ota, Y., Takazoe, K., Moriyama, Y., Kawano, H., Miyao, Y., et al. (1999). Circulating levels of secretory type II phospholipase A(2) predict coronary events in patients with coronary artery disease. Circulation, 100(12), 1280–1284.
Kumar, P. S., Griffen, A. L., Moeschberger, M. L., & Leys, E. J. (2005). Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. Journal of Clinical Microbiology, 43(8), 3944–3955.
Kupert, E., Anderson, M., Liu, Y., Succop, P., Levin, L., Wang, J., et al. (2011). Plasma secretory phospholipase A2-IIa as a potential biomarker for lung cancer in patients with solitary pulmonary nodules. BMC Cancer, 11, 513.
Kuwata, H., Sawada, H., Murakami, M., & Kudo, I. (1999). Role of type IIA secretory phospholipase A2 in arachidonic acid metabolism. Advances in Experimental Medicine and Biology, 469, 183–188.
Lambeau, G., & Lazdunski, M. (1999). Receptors for a growing family of secreted phospholipases A2. Trends in Pharmacological Sciences, 20(4), 162–170.
Lamont, R. J., Koo, H., & Hajishengallis, G. (2018). The oral microbiota: Dynamic communities and host interactions. Nature Reviews. Microbiology, 16(12), 745–759.
Lin, M. K., Farewell, V., Vadas, P., Bookman, A. A., Keystone, E. C., & Pruzanski, W. (1996). Secretory phospholipase A2 as an index of disease activity in rheumatoid arthritis. Prospective double blind study of 212 patients. The Journal of Rheumatology, 23(7), 1162–1166.
Madsen, L. M., Inada, M., & Weiss, J. (1996). Determinants of activation by complement of group II phospholipase A2 acting against Escherichia coli. Infection and Immunity, 64(7), 2425–2430.
Maekawa, T., Krauss, J. L., Abe, T., Jotwani, R., Triantafilou, M., Triantafilou, K., et al. (2014). Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis. Cell Host & Microbe, 15(6), 768–778.
Magrioti, V., & Kokotos, G. (2010). Phospholipase A2 inhibitors as potential therapeutic agents for the treatment of inflammatory diseases. Expert Opinion on Therapeutic Patents, 20(1), 1–18.
Magrioti, V., & Kokotos, G. (2013). Phospholipase A2 inhibitors for the treatment of inflammatory diseases: A patent review (2010—present). Expert Opinion on Therapeutic Patents, 23(3), 333–344.
Mallat, Z., Benessiano, J., Simon, T., Ederhy, S., Sebella-Arguelles, C., Cohen, A., et al. (2007). Circulating secretory phospholipase A2 activity and risk of incident coronary events in healthy men and women: The EPIC-Norfolk study. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(5), 1177–1183.
Marshall, J., Krump, E., Lindsay, T., Downey, G., Ford, D. A., Zhu, P., et al. (2000). Involvement of cytosolic phospholipase A2 and secretory phospholipase A2 in arachidonic acid release from human neutrophils. Journal of Immunology, 164(4), 2084–2091.
Maruvada, P., Leone, V., Kaplan, L. M., & Chang, E. B. (2017). The human microbiome and obesity: Moving beyond associations. Cell Host & Microbe, 22(5), 589–599.
Menschikowski, M., Kasper, M., Lattke, P., Schiering, A., Schiefer, S., Stockinger, H., et al. (1995). Secretory group II phospholipase A2 in human atherosclerotic plaques. Atherosclerosis, 118(2), 173–181.
Menschikowski, M., Hagelgans, A., Schuler, U., Froeschke, S., Rosner, A., & Siegert, G. (2013). Plasma levels of phospholipase A2-IIA in patients with different types of malignancies: Prognosis and association with inflammatory and coagulation biomarkers. Pathology Oncology Research, 19(4), 839–846.
Miller, D. P., Wang, Q., Weinberg, A., & Lamont, R. J. (2018). Transcriptome analysis of Porphyromonas gingivalis and Acinetobacter baumannii in polymicrobial communities. Molecular Oral Microbiology, 33(5), 364–377.
Minami, T., Tojo, H., Shinomura, Y., Tarui, S., & Okamoto, M. (1992). Raised serum activity of phospholipase A2 immunochemically related to group II enzyme in inflammatory bowel disease: Its correlation with disease activity of Crohn’s disease and ulcerative colitis. Gut, 33(7), 914–921.
Minami, T., Tojo, H., Shinomura, Y., Matsuzawa, Y., & Okamoto, M. (1994). Increased group II phospholipase A2 in colonic mucosa of patients with Crohn’s disease and ulcerative colitis. Gut, 35(11), 1593–1598.
Minami, T., Shinomura, Y., Miyagawa, J., Tojo, H., Okamoto, M., & Matsuzawa, Y. (1997). Immunohistochemical localization of group II phospholipase A2 in colonic mucosa of patients with inflammatory bowel disease. The American Journal of Gastroenterology, 92(2), 289–292.
Moses, G. S., Jensen, M. D., Lue, L. F., Walker, D. G., Sun, A. Y., Simonyi, A., et al. (2006). Secretory PLA2-IIA: A new inflammatory factor for Alzheimer’s disease. Journal of Neuroinflammation, 3, 28.
Mounier, C., Faili, A., Vargaftig, B. B., Bon, C., & Hatmi, M. (1993). Secretory phospholipase A2 is not required for arachidonic acid liberation during platelet activation. European Journal of Biochemistry, 216(1), 169–175.
Mounier, C. M., Wendum, D., Greenspan, E., Flejou, J. F., Rosenberg, D. W., & Lambeau, G. (2008). Distinct expression pattern of the full set of secreted phospholipases A2 in human colorectal adenocarcinomas: sPLA2-III as a biomarker candidate. British Journal of Cancer, 98(3), 587–595.
Movert, E., Wu, Y., Lambeau, G., Kahn, F., Touqui, L., & Areschoug, T. (2013). Secreted group IIA phospholipase A2 protects humans against the group B streptococcus: Experimental and clinical evidence. The Journal of Infectious Diseases, 208(12), 2025–2035.
Mueller, H. W., Pritzker, C. R., Kubik, A., & Deykin, D. (1993). Characterization of phospholipase A2 secretion from human platelets. Thrombosis Research, 72(6), 519–530.
Murakami, M., Nakatani, Y., & Kudo, I. (1996). Type II secretory phospholipase A2 associated with cell surfaces via C-terminal heparin-binding lysine residues augments stimulus-initiated delayed prostaglandin generation. The Journal of Biological Chemistry, 271(47), 30041–30051.
Murakami, M., Kuwata, H., Amakasu, Y., Shimbara, S., Nakatani, Y., Atsumi, G., et al. (1997a). Prostaglandin E2 amplifies cytosolic phospholipase A2- and cyclooxygenase-2-dependent delayed prostaglandin E2 generation in mouse osteoblastic cells. Enhancement by secretory phospholipase A2. The Journal of Biological Chemistry, 272(32), 19891–19897.
Murakami, M., Nakatani, Y., Atsumi, G., Inoue, K., & Kudo, I. (1997b). Regulatory functions of phospholipase A2. Critical Reviews in Immunology, 17(3–4), 225–283.
Murakami, M., Taketomi, Y., Miki, Y., Sato, H., Hirabayashi, T., & Yamamoto, K. (2011a). Recent progress in phospholipase A(2) research: From cells to animals to humans. Progress in Lipid Research, 50(2), 152–192.
Murakami, M., Taketomi, Y., Sato, H., & Yamamoto, K. (2011b). Secreted phospholipase A2 revisited. Journal of Biochemistry, 150(3), 233–255.
Murakami, M., Taketomi, Y., Miki, Y., Sato, H., Yamamoto, K., & Lambeau, G. (2014). Emerging roles of secreted phospholipase A2 enzymes: The 3rd edition. Biochimie, 107(Pt A), 105–113.
Murakami, M., Nakatani, Y., Atsumi, G. I., Inoue, K., & Kudo, I. (2017). Regulatory functions of phospholipase A2. Critical Reviews in Immunology, 37(2–6), 121–179.
Nevalainen, T. J., & Haapanen, T. J. (1993). Distribution of pancreatic (group I) and synovial-type (group II) phospholipases A2 in human tissues. Inflammation, 17(4), 453–464.
Nevalainen, T. J., Marki, F., Kortesuo, P. T., Grutter, M. G., Di Marco, S., & Schmitz, A. (1993). Synovial type (group II) phospholipase A2 in cartilage. The Journal of Rheumatology, 20(2), 325–330.
Nevalainen, T. J., Aho, H. J., & Peuravuori, H. (1994). Secretion of group 2 phospholipase A2 by lacrimal glands. Investigative Ophthalmology & Visual Science, 35(2), 417–421.
Nevalainen, T. J., Graham, G. G., & Scott, K. F. (2008). Antibacterial actions of secreted phospholipases A2. Review. Biochimica et Biophysica Acta, 1781(1–2), 1–9.
O’Donoghue, M. L., Mallat, Z., Morrow, D. A., Benessiano, J., Sloan, S., Omland, T., et al. (2011). Prognostic utility of secretory phospholipase A(2) in patients with stable coronary artery disease. Clinical Chemistry, 57(9), 1311–1317.
Okita, Y., Shiono, T., Yahagi, A., Hamada, S., Umemura, M., & Matsuzaki, G. (2016). Interleukin-22-induced antimicrobial phospholipase A2 group IIA mediates protective innate immunity of nonhematopoietic cells against Listeria monocytogenes. Infection and Immunity, 84(2), 573–579.
Oliveira, R. R., Fermiano, D., Feres, M., Figueiredo, L. C., Teles, F. R., Soares, G. M., et al. (2016). Levels of candidate periodontal pathogens in subgingival biofilm. Journal of Dental Research, 95(6), 711–718.
Ouellette, A. J. (2011). Paneth cell alpha-defensins in enteric innate immunity. Cellular and Molecular Life Sciences, 68(13), 2215–2229.
Paganelli, F. L., Leavis, H. L., He, S., van Sorge, N. M., Payre, C., Lambeau, G., et al. (2018). Group IIA-secreted phospholipase A2 in human serum kills commensal but not clinical Enterococcus faecium isolates. Infection and Immunity, 86(8), e00180–e00118.
Perez-Chaparro, P. J., Goncalves, C., Figueiredo, L. C., Faveri, M., Lobao, E., Tamashiro, N., et al. (2014). Newly identified pathogens associated with periodontitis: A systematic review. Journal of Dental Research, 93(9), 846–858.
Pernet, E., Guillemot, L., Burgel, P. R., Martin, C., Lambeau, G., Sermet-Gaudelus, I., et al. (2014). Pseudomonas aeruginosa eradicates Staphylococcus aureus by manipulating the host immunity. Nature Communications, 5, 5105.
Pernet, E., Brunet, J., Guillemot, L., Chignard, M., Touqui, L., & Wu, Y. (2015). Staphylococcus aureus adenosine inhibits sPLA2-IIA-mediated host killing in the airways. Journal of Immunology, 194(11), 5312–5319.
Piris-Gimenez, A., Paya, M., Lambeau, G., Chignard, M., Mock, M., Touqui, L., et al. (2005). In vivo protective role of human group IIa phospholipase A2 against experimental anthrax. Journal of Immunology, 175(10), 6786–6791.
Pruzanski, W., Vadas, P., Stefanski, E., & Urowitz, M. B. (1985). Phospholipase A2 activity in sera and synovial fluids in rheumatoid arthritis and osteoarthritis. Its possible role as a proinflammatory enzyme. The Journal of Rheumatology, 12(2), 211–216.
Pruzanski, W., Keystone, E. C., Sternby, B., Bombardier, C., Snow, K. M., & Vadas, P. (1988). Serum phospholipase A2 correlates with disease activity in rheumatoid arthritis. The Journal of Rheumatology, 15(9), 1351–1355.
Pruzanski, W., Bogoch, E., Stefanski, E., Wloch, M., & Vadas, P. (1990). Synthesis and release of phospholipase A2 by unstimulated human articular chondrocytes. The Journal of Rheumatology, 17(10), 1386–1391.
Pruzanski, W., Greenwald, R. A., Street, I. P., Laliberte, F., Stefanski, E., & Vadas, P. (1992). Inhibition of enzymatic activity of phospholipases A2 by minocycline and doxycycline. Biochemical Pharmacology, 44(6), 1165–1170.
Pruzanski, W., Albin-Cook, K., Laxer, R. M., MacMillan, J., Stefanski, E., Vadas, P., et al. (1994). Phospholipase A2 in juvenile rheumatoid arthritis: Correlation to disease type and activity. The Journal of Rheumatology, 21(10), 1951–1954.
Richards, A. M., Abu Kwaik, Y., & Lamont, R. J. (2015). Code blue: Acinetobacter baumannii, a nosocomial pathogen with a role in the oral cavity. Molecular Oral Microbiology, 30(1), 2–15.
Rizzatti, G., Lopetuso, L. R., Gibiino, G., Binda, C., & Gasbarrini, A. (2017). Proteobacteria: A common factor in human diseases. BioMed Research International, 2017, 9351507.
Sanchez-Mejia, R. O., Newman, J. W., Toh, S., Yu, G. Q., Zhou, Y., Halabisky, B., et al. (2008). Phospholipase A2 reduction ameliorates cognitive deficits in a mouse model of Alzheimer’s disease. Nature Neuroscience, 11(11), 1311–1318.
Schaeffer, E. L., da Silva, E. R., Novaes Bde, A., Skaf, H. D., & Gattaz, W. F. (2010). Differential roles of phospholipases A2 in neuronal death and neurogenesis: Implications for Alzheimer disease. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 34(8), 1381–1389.
Schewe, M., Franken, P. F., Sacchetti, A., Schmitt, M., Joosten, R., Bottcher, R., et al. (2016). Secreted phospholipases A2 are intestinal stem cell niche factors with distinct roles in homeostasis, inflammation, and cancer. Cell Stem Cell, 19(1), 38–51.
Schmitter, T., Fiebich, B. L., Fischer, J. T., Gajfulin, M., Larsson, N., Rose, T., et al. (2018). Ex vivo anti-inflammatory effects of probiotics for periodontal health. Journal of Oral Microbiology, 10(1), 1502027.
Scott, D. L., White, S. P., Browning, J. L., Rosa, J. J., Gelb, M. H., & Sigler, P. B. (1991). Structures of free and inhibited human secretory phospholipase A2 from inflammatory exudate. Science, 254(5034), 1007–1010.
Seilhamer, J. J., Pruzanski, W., Vadas, P., Plant, S., Miller, J. A., Kloss, J., et al. (1989). Cloning and recombinant expression of phospholipase A2 present in rheumatoid arthritic synovial fluid. The Journal of Biological Chemistry, 264(10), 5335–5338.
Shinohara, H., Komatsubara, T., Tojo, H., Okamoto, M., Nishikawa, S., Nagata, T., et al. (1995). Group II phospholipase A(2) in human gingiva with periodontal disease. Mediators of Inflammation, 4(2), 95–97.
Silliman, C. C., Moore, E. E., Zallen, G., Gonzalez, R., Johnson, J. L., Elzi, D. J., et al. (2002). Presence of the M-type sPLA(2) receptor on neutrophils and its role in elastase release and adhesion. American Journal of Physiology. Cell Physiology, 283(4), C1102–C1113.
Sun, G. Y., Xu, J., Jensen, M. D., & Simonyi, A. (2004). Phospholipase A2 in the central nervous system: Implications for neurodegenerative diseases. Journal of Lipid Research, 45(2), 205–213.
Sun, G. Y., Shelat, P. B., Jensen, M. B., He, Y., Sun, A. Y., & Simonyi, A. (2010). Phospholipases A2 and inflammatory responses in the central nervous system. Neuromolecular Medicine, 12(2), 133–148.
Sun, C. Q., Zhong, C. Y., Sun, W. W., Xiao, H., Zhu, P., Lin, Y. Z., et al. (2016). Elevated type II secretory phospholipase A2 increases the risk of early atherosclerosis in patients with newly diagnosed metabolic syndrome. Scientific Reports, 6, 34929.
Takada, Y., & Fujita, M. (2017). Secreted phospholipase A2 type IIA (sPLA2-IIA) activates integrins in an allosteric manner. Advances in Experimental Medicine and Biology, 925, 103–115.
Takeuchi, H., Hirano, T., Whitmore, S. E., Morisaki, I., Amano, A., & Lamont, R. J. (2013). The serine phosphatase SerB of Porphyromonas gingivalis suppresses IL-8 production by dephosphorylation of NF-kappaB RelA/p65. PLoS Pathogens, 9(4), e1003326.
Tan, T. L., & Goh, Y. Y. (2017). The role of group IIA secretory phospholipase A2 (sPLA2-IIA) as a biomarker for the diagnosis of sepsis and bacterial infection in adults—A systematic review. PLoS One, 12(7), e0180554.
Teanpaisan, R., Piwat, S., & Dahlen, G. (2011). Inhibitory effect of oral Lactobacillus against oral pathogens. Letters in Applied Microbiology, 53(4), 452–459.
Thomas, G., Bertrand, F., & Saunier, B. (2000). The differential regulation of group II(A) and group V low molecular weight phospholipases A(2) in cultured rat astrocytes. The Journal of Biological Chemistry, 275(15), 10876–10886.
Thwin, M. M., Satyanarayanajois, S. D., Nagarajarao, L. M., Sato, K., Arjunan, P., Ramapatna, S. L., et al. (2007). Novel peptide inhibitors of human secretory phospholipase A2 with antiinflammatory activity: Solution structure and molecular modeling. Journal of Medicinal Chemistry, 50(24), 5938–5950.
Triggiani, M., Granata, F., Oriente, A., Gentile, M., Petraroli, A., Balestrieri, B., et al. (2002). Secretory phospholipases A2 induce cytokine release from blood and synovial fluid monocytes. European Journal of Immunology, 32(1), 67–76.
Triggiani, M., Granata, F., Balestrieri, B., Petraroli, A., Scalia, G., Del Vecchio, L., et al. (2003). Secretory phospholipases A2 activate selective functions in human eosinophils. Journal of Immunology, 170(6), 3279–3288.
Vadas, P., Stefanski, E., & Pruzanski, W. (1985). Characterization of extracellular phospholipase A2 in rheumatoid synovial fluid. Life Sciences, 36(6), 579–587.
Velsko, I. M., Chukkapalli, S. S., Rivera-Kweh, M. F., Zheng, D., Aukhil, I., Lucas, A. R., et al. (2015). Periodontal pathogens invade gingiva and aortic adventitia and elicit inflammasome activation in alphavbeta6 integrin-deficient mice. Infection and Immunity, 83(12), 4582–4593.
Villanueva, E. B., Little, J. P., Lambeau, G., & Klegeris, A. (2012). Secreted phospholipase A(2) group IIA is a neurotoxin released by stimulated human glial cells. Molecular and Cellular Neurosciences, 49(4), 430–438.
Wang, M., Krauss, J. L., Domon, H., Hosur, K. B., Liang, S., Magotti, P., et al. (2010). Microbial hijacking of complement-toll-like receptor crosstalk. Science Signaling, 3(109), ra11.
Wang, X., Huang, C. J., Yu, G. Z., Wang, J. J., Wang, R., Li, Y. M., et al. (2013). Expression of group IIA phospholipase A2 is an independent predictor of favorable outcome for patients with gastric cancer. Human Pathology, 44(10), 2020–2027.
Wang, J., Ji, H., Wang, S., Liu, H., Zhang, W., Zhang, D., et al. (2018). Probiotic Lactobacillus plantarum promotes intestinal barrier function by strengthening the epithelium and modulating gut microbiota. Frontiers in Microbiology, 9, 1953.
Weiss, J. P. (2015). Molecular determinants of bacterial sensitivity and resistance to mammalian Group IIA phospholipase A2. Biochimica et Biophysica Acta, 1848(11 Pt B), 3072–3077.
Wery, J. P., Schevitz, R. W., Clawson, D. K., Bobbitt, J. L., Dow, E. R., Gamboa, G., et al. (1991). Structure of recombinant human rheumatoid arthritic synovial fluid phospholipase A2 at 2.2 A resolution. Nature, 352(6330), 79–82.
Wu, Y., Zhang, Q., Ren, Y., & Ruan, Z. (2017). Effect of probiotic Lactobacillus on lipid profile: A systematic review and meta-analysis of randomized, controlled trials. PLoS One, 12(6), e0178868.
Yagami, T., Ueda, K., Asakura, K., Hata, S., Kuroda, T., Sakaeda, T., et al. (2002). Human group IIA secretory phospholipase A2 induces neuronal cell death via apoptosis. Molecular Pharmacology, 61(1), 114–126.
Yin, X., Heeney, D., Srisengfa, Y., Golomb, B., Griffey, S., & Marco, M. (2018). Bacteriocin biosynthesis contributes to the anti-inflammatory capacities of probiotic Lactobacillus plantarum. Beneficial Microbes, 9(2), 333–344.
Zvaritch, E., Lambeau, G., & Lazdunski, M. (1996). Endocytic properties of the M-type 180-kDa receptor for secretory phospholipases A2. The Journal of Biological Chemistry, 271(1), 250–257.
Acknowledgements
Findings reported in this review were funded by NIH/NIDCR grant DE024804, NIH/NIGMS P20GM103538 and College of Dentistry University of Kentucky. We thank Drs. Yongzheng Wu and Lhousseine Touqi from Institute Pasteur for kindly sharing the hPLA2-IIA-Tg mice as well as Drs. Jorge Frias (U. of Florida) and Sreenatha Kirakodu (U. of Kentucky) for their support in oral microbiome preliminary analysis. We also are grateful to Dr. Brittany Camenisch and Division of Periodontology for supporting the ongoing preliminary clinical study in salivary PLA2-IIA levels.
Conflict of Interest: The authors have no conflicts of interest.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this paper
Cite this paper
Gonzalez, O.A., Euzebio-Alves, V., Alimova, Y., Al-Attar, A., Ebersole, J.L. (2019). A Potential Role of Phospholipase 2 Group IIA (PLA2-IIA) in P. gingivalis-Induced Oral Dysbiosis. In: Belibasakis, G.N., Hajishengallis, G., Bostanci, N., Curtis, M.A. (eds) Oral Mucosal Immunity and Microbiome. Advances in Experimental Medicine and Biology, vol 1197. Springer, Cham. https://doi.org/10.1007/978-3-030-28524-1_7
Download citation
DOI: https://doi.org/10.1007/978-3-030-28524-1_7
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-28523-4
Online ISBN: 978-3-030-28524-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)