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Purification and Characterization of a Fimbrial Protein from Porphyromonas Salivosa ATCC 49407

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Purification and Characterization of a Fimbrial Protein from Porphyromonas Salivosa ATCC 49407 FULL PAPER Bacteriology Purification and characterization of a fimbrial protein from Porphyromonas salivosa ATCC 49407 Yasunori KOYATA1), Kiyoko WATANABE1), Toshizo TOYAMA1), Haruka SASAKI1) and Nobushiro HAMADA1)* 1)Division of Microbiology, Department of Oral Science, Kanagawa Dental University, Yokosuka, Kanagawa 238-8580, Japan ABSTRACT. Periodontal disease is a significant problem in companion animals such as dogs and cats. However, there is little information available about fimbriae association of periodontal disease in companion animals. In this study, we have purified and characterized a fimbriae from Porphyromonas salivosa ATCC 49407. The molecular mass of this protein was approximately 60-kDa, as estimated by SDS-PAGE. Immunogold electron microscopy revealed that anti-60-kDa fimbrial serum bound to fimbria on the cell surface of P. salivosa ATCC 49407. However, fimbriae of P. gingivalis and P. gulae were not labeled with the same antibody. Immunoelectron-microscopic studies and immunoblot analysis revealed that antigenicity and molecular weight were distinct from previously reported Porphyromonas fimbrial proteins. The amino acid sequence of the N-terminal 15 residues of the 60-kDa fimbrillin protein revealed only 3 of 15 residues identical to J. Vet. Med. Sci. other Porphyromonas species fimbrillin proteins. Thus, the N-terminal amino acid sequence of the 81(6): 916–923, 2019 60-kDa fimbrillin protein ofP. salivosa clearly differed from previously reported fimbrillin proteins. The level of adherence of the P. salivosa was 1.81%. It was confirmed that P. salivosa can adheres doi: 10.1292/jvms.19-0067 to human cells. These results suggest that the 60-kDa fimbriae ofP. salivosa ATCC 49407 is a new type of fimbria and may have an important factor in the adherence host cells. We suggest that the surface structure of P. salivosa may have a role in the colonization of this organism in periodontal Received: 1 February 2019 pockets in companion animals. Accepted: 11 April 2019 KEY WORDS: fimbria, periodontitis, Porphyromonas gingivalis, Porphyromonas salivosa, 60-kDa Published online in J-STAGE: fimbrial protein 23 April 2019 Porphyromonas salivosa is a black-pigmented, asaccharolytic, anaerobic, non-motile, non-spore-forming, Gram-negative, rod-shaped organism [30]. In 1987, Love et al. [29] described Bacteroides salivosus as a pigmented asaccharolytic pathogen which was isolated from subcutaneous abscesses and pyothoraxes of cats. B. salivosus strains have little DNA-DNA hybridization with members of previously described pigmented asaccharolytic Bacteroides species. In addition, DNA-DNA hybridization experiments revealed that the levels of hybridization between feline strains and Bacteroides macacae ATCC 33141 [7, 28, 45] are not significant. Periodontitis in companion animals is an almost identical disease to that in humans in terms of disease course and clinical presentations [1, 8, 9, 16, 26]. Black-pigmenting anaerobic bacteria have been isolated from the periodontal pockets of several animals. The most frequently isolated black-pigmented anaerobic bacteria in canine periodontal pockets are P. gulae, P. salivosa and P. denticanis [1, 19]. However, several differences between human and companion animal Porphyromonas isolates have been reported [9, 19]. P. gingivalis isolates from humans are catalase-negative, whereas P. gingivalis-like isolates from canine periodontal pockets are catalase-positive. These catalase-positive P. gingivalis-like isolates may be of P. gulae. Periodontal disease is a significant oral problem, characterized by halitosis, gingival inflammation, increased periodontal pocket depth, and alveolar bone loss, which results in loosening and eventual loss of teeth. Periodontal pathogens induce inflammatory reactions in the surrounding tissues [2, 15, 23]. Periodontitis is accepted as the most common cause of tooth loss in dogs and cats [6]. Numerous investigators have shown that periodontal disease in dogs and humans is accompanied by a shift in oral bacterial flora from predominantly aerobic Gram-positive bacteria to anaerobic Gram-negative rods [17, 18, 27, 37, 44]. Studies on feline periodontal disease have shown that the proportions of Gram-negative rods increase as the degree of periodontal disease increase and conversely found a negative correlation between *Correspondence to: Hamada, N.: [email protected] ©2019 The Japanese Society of Veterinary Science This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives (by-nc-nd) License. (CC-BY-NC-ND 4.0: https://creativecommons.org/licenses/by-nc-nd/4.0/) 916 CHARACTERIZATION OF P. SALIVOSA FIMBRIAE the degree of periodontal disease and the number of facultative/aerobic Gram-positive rods [36]. Porphyromonas gingivalis is an obligate anaerobic Gram-negative coccobacillus that has been associated with periodontal destruction in humans [23]. The feline Porphyromonas species, P. circumdentaria and P. salivosa were isolated from oral-associated diseases in domestic cats and from normal gingival margins of adolescent cats [31–35]. Moreover, Porphyromonas-like Gram-negative rods resembling human strains of P. gingivalis, P. endodontalis and feline strains of P. salivosa were isolated from dogs with periodontitis [5, 21, 43]. These findings suggested that Porphyromonas species had an ecological niche within the feline oral cavity. Human periodontitis has been associated with subgingival plaque containing elevated levels of a specific Gram-negative anaerobic bacteria. P. gingivalis is a pathogen that causes periodontal disease, which is a typical chronic inflammatory disease [10, 23, 25, 47]. Bacterial fimbria is an important cell structure that contributes to the adherence and invasion of host cells [3, 20, 24, 42, 48], and induces inflammatory processes in periodontal tissues through a number of mechanisms [2, 11]. P. gingivalis fimbriae bind specifically to components lining the oral cavity, such as salivary proteins, commensal bacteria, several types of extracellular matrices, and host cells, including gingival fibroblasts, epithelial cells, and endothelial cells [15]. These adhesive abilities are a pathogenic trait that causes periodontal tissue destruction [38]. Moreover, fimbriae function as virulence factors in inflammatory reactions because they stimulate the production of inflammatory cytokines by macrophages and fibroblasts. These observations suggest the involvement of fimbriae as regulators of inflammatory reactions caused by bacterial infection [42]. In humans, much progress has been made in understanding the disease etiology and interaction between host and periodontal pathogens. These pathogens possess virulence factors that include collagenase, lipopolysaccharides, a trypsin-like protease and fimbriae [23]. Fimbriae in particular have an important role in facilitating the initial interaction between the bacteria and host [3, 14, 49]. In this study, to clarify the presence of new type of fimbriae in Porphyromonas species, we purified and characterized a fimbrial protein from P. salivosa ATCC 49407. MATERIALS AND METHODS Strains and cultivation conditions P. salivosa ATCC 49407, P. gingivalis ATCC 33277 and P. gulae ATCC 51700 were cultivated (15% CO2, 15% H2 and 70% N2) in an anaerobic chamber (ANX-1; HIRASAWA, Tokyo, Japan) at 37°C in pre-reduced brain heart infusion (BHI) broth (Becton Dickinson Co., Sparks, MD, U.S.A.) supplemented with 0.5% yeast extract (Becton Dickinson Co.), 5 µg/ml hemin (Sigma- Aldrich, St. Louis, MO, U.S.A.), and 1 µg/ml vitamin K1 (Sigma-Aldrich). Isolation and purification of the 60-kDa fimbriae from P. salivosa P. salivosa was incubated anaerobically for 18 hr in BHI broth. The bacterial cell pellet was harvested by centrifugation at 8,000 × g for 30 min and washed twice with 20 mM Tris-HCl buffer (pH 8.0) containing 10 mM MgCl2 and 0.15 M NaCl by repeated pipetting. The suspension was subjected to ultrasonication with a 3-mm microtip (Branson Ultrasonics Corporation, Danbury, CT, U.S.A.) at 25 W output on the pulse setting with 5 cycles of 1 min in an icebox. The supernatant of the sonic extract collected by centrifugation at 10,000 × g for 30 min was subjected to 40% ammonium sulfate saturation by the stepwise addition of ammonium sulfate. The precipitated protein was collected by centrifugation at 10,000 × g for 30 min at 4°C, suspended in a minimum volume of 20 mM Tris buffer, pH 8.0, and dialyzed against the same buffer. The dialysate sample containing most of the fimbriae was subjected to further purification on a diethylaminoethyl (DEAE) Sepharose CL-6B (GE Healthcare Bio-Sciences, Pittsburgh, PA, U.S.A.) column equilibrated with 20 mM Tris buffer (pH 8.0). The column was washed with 20 mM Tris buffer and then eluted with a linear gradient of 0 M to 0.3 M NaCl. The protein content of the fractions was measured by ultraviolet light adsorption at 280 nm. Sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE) Protein extracts were heated at 100°C for 5 min in loading buffer. Samples were applied to 12.0% polyacrylamide gel with a 4% stacking gel, and electrophoresed at 30 mA constant current for 1 hr. The proteins were stained with Coomassie brilliant blue R-250 (Bio-Rad Laboratories, Inc. Hercules, CA, U.S.A.). For molecular weight calibration, a low-molecular weight marker kit (ATTO, Tokyo, Japan) was used. Polyclonal antibodies Polyclonal antibodies (PAbs) against the 60-kDa fimbrial protein were prepared using the purified
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