Extracellular Proteinases of Miamiensis avidus Causing Scuticociliatosis are Potential Virulence Factors
Miamiensis avidus is the causative agent of scuticociliatosis in various marine fish species. The virulence factors of the parasite have not been identified, so far. In this study, we examined M. avidus extracellular proteinases (ECPs) as potential virulence factors, using culture supernatants as an...
Saved in:
Published in | Fish Pathology Vol. 53; no. 1; pp. 1 - 9 |
---|---|
Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
Published |
Tokyo
The Japanese Society of Fish Pathology
2018
Japan Science and Technology Agency |
Subjects | |
Online Access | Get full text |
Cover
Loading…
Abstract | Miamiensis avidus is the causative agent of scuticociliatosis in various marine fish species. The virulence factors of the parasite have not been identified, so far. In this study, we examined M. avidus extracellular proteinases (ECPs) as potential virulence factors, using culture supernatants as an ECPs source. We investigated the substrate specificity of ECPs using artificial peptides, and the cytotoxicity of the ECPs was examined using CHSE-214 cells. To elucidate the role of ECPs in ciliate growth, M. avidus was cultured on CHSE-214 cells in the presence of proteinase inhibitors. We detected proteinase activities from the supernatant of M. avidus. Viable CHSE-214 cells decreased significantly in number, when incubated in a medium supplemented with the culture supernatant of M. avidus. The growth of ciliates on CHSE-214 cells was delayed in the presence of PMSF (serine proteinase inhibitor) and E-64 (cysteine proteinase inhibitor). These results suggested that the culture supernatant contained ECPs showing cytotoxicity, and the proteinases facilitated nutrient uptake by the ciliates. Thus, ECPs may be responsible for virulence factors of M. avidus. |
---|---|
AbstractList | Miamiensis avidus is the causative agent of scuticociliatosis in various marine fish species. The virulence factors of the parasite have not been identified, so far. In this study, we examined M. avidus extracellular proteinases (ECPs) as potential virulence factors, using culture supernatants as an ECPs source. We investigated the substrate specificity of ECPs using artificial peptides, and the cytotoxicity of the ECPs was examined using CHSE-214 cells. To elucidate the role of ECPs in ciliate growth, M. avidus was cultured on CHSE-214 cells in the presence of proteinase inhibitors. We detected proteinase activities from the supernatant of M. avidus. Viable CHSE-214 cells decreased significantly in number, when incubated in a medium supplemented with the culture supernatant of M. avidus. The growth of ciliates on CHSE-214 cells was delayed in the presence of PMSF (serine proteinase inhibitor) and E-64 (cysteine proteinase inhibitor). These results suggested that the culture supernatant contained ECPs showing cytotoxicity, and the proteinases facilitated nutrient uptake by the ciliates. Thus, ECPs may be responsible for virulence factors of M. avidus. |
Author | Song, Jun-Young Narasaki, Yukie Obayashi, Yumiko Murakami, Shoko Ito, Sayami Nakayama, Kei Kitamura, Shin-Ichi |
Author_xml | – sequence: 1 fullname: Narasaki, Yukie organization: Graduate School of Science and Engineering, Ehime University – sequence: 2 fullname: Obayashi, Yumiko organization: Center for Marine Environmental Studies (CMES), Ehime University – sequence: 3 fullname: Ito, Sayami organization: Center for Marine Environmental Studies (CMES), Ehime University – sequence: 4 fullname: Murakami, Shoko organization: Center for Marine Environmental Studies (CMES), Ehime University – sequence: 5 fullname: Song, Jun-Young organization: Pathology Division, National Fisheries Research and Development Institute – sequence: 6 fullname: Nakayama, Kei organization: Graduate School of Science and Engineering, Ehime University – sequence: 7 fullname: Kitamura, Shin-Ichi organization: Graduate School of Science and Engineering, Ehime University |
BookMark | eNpF0EtLAzEQB_AgCtbHwW8Q8ORha7JJmix4kdKqoCj4wFvIZmc1ZZvUJCv67d1aH5cZGH4zA_89tO2DB4SOKBkzyuXpIrWrsWBjuoVGVClaSMbENhoRplQhlXreRYcpuZqQkisuZDVCr7OPHI2Frus7E_FdDBmcNwkSDi2-cWbpwCeXsHl3TZ_w1PTJ-Rd8b_vsbLCucyaHbxAB3w3bPjvT4ScX-w68BTw3NoeYDtBOa7oEhz99Hz3OZw_Ty-L69uJqen5dWDERuWgqS2wFTWsrrqScNFBKgJbXhtvalorXRNZV26iqIgq4tE1LpKlLoErUlCu2j443d1cxvPWQsl6EPvrhpS5JWVLKKiEGdbJRNoaUIrR6Fd3SxE9NiV5nqddZasE0HezZxi5SNi_wJ00cEujgX27K79i-mqjBsy9kOYK- |
CitedBy_id | crossref_primary_10_1016_j_aquaculture_2021_736657 crossref_primary_10_1016_j_aquaculture_2019_734311 crossref_primary_10_1016_j_parint_2020_102093 |
Cites_doi | 10.1016/j.ijpara.2006.08.013 10.3354/dao02017 10.1292/jvms.10-0214 10.1016/j.exppara.2010.11.005 10.3354/dao030017 10.3354/dao02116 10.3147/jsfp.35.67 10.3354/dao046047 10.1016/j.parint.2013.12.007 10.3354/dao062239 10.1354/vp.45-4-546 10.3354/dao047049 10.1007/s00436-010-2157-7 10.1111/j.1365-2761.1980.tb00400.x 10.1016/j.dci.2008.05.002 10.3147/jsfp.28.131 10.3354/ame01169 10.1016/S0166-6851(01)00438-8 10.3354/dao064159 10.3354/dao073227 10.1016/j.vetpar.2009.08.005 10.1128/IAI.01671-14 10.1016/j.fsi.2007.02.001 10.1016/j.marenvres.2015.06.011 10.1017/S0031182004004883 10.1046/j.1432-1327.1998.2540006.x 10.3354/dao062233 10.1016/j.micinf.2012.05.014 10.4319/lo.2005.50.2.0722 10.1016/j.parint.2017.10.007 10.1111/j.1365-3024.2011.01310.x 10.1111/j.1365-2761.2009.01089.x |
ContentType | Journal Article |
Copyright | 2018 The Japanese Society of Fish Pathology Copyright Japan Science and Technology Agency 2018 |
Copyright_xml | – notice: 2018 The Japanese Society of Fish Pathology – notice: Copyright Japan Science and Technology Agency 2018 |
DBID | AAYXX CITATION 7TN F1W |
DOI | 10.3147/jsfp.53.1 |
DatabaseName | CrossRef Oceanic Abstracts ASFA: Aquatic Sciences and Fisheries Abstracts |
DatabaseTitle | CrossRef Oceanic Abstracts ASFA: Aquatic Sciences and Fisheries Abstracts |
DatabaseTitleList | Oceanic Abstracts |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Agriculture |
EISSN | 1881-7335 |
EndPage | 9 |
ExternalDocumentID | 10_3147_jsfp_53_1 article_jsfp_53_1_53_1_article_char_en |
GroupedDBID | 2WC 5GY ACGFS AENEX ALMA_UNASSIGNED_HOLDINGS CS3 DIK JSF JSP OK1 P2P RJT AAYXX CITATION 7TN F1W |
ID | FETCH-LOGICAL-c565t-d9c0c9edfc948776de27eef4ba4cbc284b07b9fd89908e47cdf07ab2e185b1483 |
ISSN | 0388-788X |
IngestDate | Thu Oct 10 16:34:27 EDT 2024 Fri Aug 23 01:17:50 EDT 2024 Wed Apr 05 15:00:12 EDT 2023 |
IsDoiOpenAccess | true |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 1 |
Language | English |
LinkModel | OpenURL |
MergedId | FETCHMERGED-LOGICAL-c565t-d9c0c9edfc948776de27eef4ba4cbc284b07b9fd89908e47cdf07ab2e185b1483 |
OpenAccessLink | https://www.jstage.jst.go.jp/article/jsfp/53/1/53_1/_article/-char/en |
PQID | 2022113955 |
PQPubID | 2048484 |
PageCount | 9 |
ParticipantIDs | proquest_journals_2022113955 crossref_primary_10_3147_jsfp_53_1 jstage_primary_article_jsfp_53_1_53_1_article_char_en |
PublicationCentury | 2000 |
PublicationDate | 2018-00-00 |
PublicationDateYYYYMMDD | 2018-01-01 |
PublicationDate_xml | – year: 2018 text: 2018-00-00 |
PublicationDecade | 2010 |
PublicationPlace | Tokyo |
PublicationPlace_xml | – name: Tokyo |
PublicationTitle | Fish Pathology |
PublicationTitleAlternate | Fish Pathol. |
PublicationYear | 2018 |
Publisher | The Japanese Society of Fish Pathology Japan Science and Technology Agency |
Publisher_xml | – name: The Japanese Society of Fish Pathology – name: Japan Science and Technology Agency |
References | Rossteuscher, S., C. Wenker, T. Jermann, T. Wahli, E. Oldenberg and H. Schmidt-Posthaus (2008): Severe scuticociliate (Philasterides dicentrarchi) infection in a population of sea dragons (Phycodurus eques and Phyllopteryx taeniolatus). Vet. Pathol., 45, 546-550. Ruszczyk, A., M. Forlenza, M. Joerink, C. M. S. Ribeiro, P. Jurecka and G. F. Wiegertjes (2008): Trypanoplasma borreli cysteine proteinase activities support a conservation of function with respect to digestion of host proteins in common carp. Dev. Comp. Immunol., 32, 1348-1361. Paramá, A., R. Castro, J. Lamas, M. L. Sanmartín, M. T. Santamarina and J. Leiro (2007a): Scuticociliate proteinases may modulate turbot immune response by inducing apoptosis in pronephric leucocytes. Int. J. Parasitol., 37, 87-95. Jung, S. J., S. I. Kitamura, J. Y. Song and M. J. Oh (2007): Miamiensis avidus (Ciliophora: Scuticociliatida) causes systemic infection of olive flounder Paralichthys olivaceus and is a senior synonym of Philasterides dicentrarchi. Dis. Aquat. Organ., 73, 227-234. Sako, Y., K. Nakaya and A. Ito (2011): Echinococcus multilocularis: Identification and functional characterization of cathepsin B-like peptidases from metacestode. Exp. Parasitol., 127, 693-701. Cheung, P. J., R. F. Nigrelli and G. D. Ruggieri (1980): Studies on the morphology of Uronema marinum Dujardin (Ciliatea: Uronematidae) with a description of the histopathology of the infection in marine fishes. J. Fish Dis., 3, 295-303. Paramá, A., R. Iglesias, M. F. Álvarez, J. Leiro, F. M. Ubeira and M. L. Sanmartín (2004): Cysteine proteinase activities in the fish pathogen Philasterides dicentrarchi (Ciliophora: Scuticociliatida). Parasitology, 128, 541-548. Suzuki, K. M., N. Hayashi, N. Hosoya, T. Takahashi, T. Kosaka and H. Hosoya (1998): Secretion of tetrain, a Tetrahymena cysteine protease, as a mature enzyme and its identification as a member of the cathepsin L subfamily. Eur. J. Biochem., 254, 6-13. Moustafa, E. M. M., N. Tange, A. Shimada and T. Morita (2010): Experimental scuticociliatosis in Japanese flounder (Paralichthys olivaceus) infected with Miamiensis avidus: pathological study on the possible neural routes of invasion and dissemination of the scuticociliate inside the fish body. J. Vet. Med. Sci., 72, 1557-1563. Kim, S. M., J. B. Cho, S. K. Kim, Y. K. Nam and K. H. Kim (2004b): Occurrence of scuticociliatosis in olive flounder Paralichthys olivaceus by Phiasterides dicentrarchi (Ciliophora: Scuticociliatida). Dis. Aquat. Organ., 62, 233-238. Iglesias, R., A. Paramá, M. F. Alvarez, J. Leiro, J. Fernández and M. L. Sanmartín (2001): Philasterides dicentrarchi (Ciliophora, Scuticociliatida) as the causative agent of scuticociliatosis in farmed turbot Scophthalmus maximus in Galicia (NW Spain). Dis. Aquat. Organ., 46, 47-55. Dragesco, A., J. Dragesco, F. Coste, C. Gasc, B. Romestand, J. C. Raymond and G. Bouix (1995): Philasterides dicentrarchi, n. sp., (Ciliophora, Scuticociliatida), a histophagous opportunistic parasite of Dicentrarchus labrax (Linnaeus, 1758), a reared marine fish. Eur. J. Protistol., 31, 327-340. Sajid, M. and J. H. McKerrow (2002): Cysteine proteases of parasitic organisms. Mol. Biochem. Parasitol., 120, 1-21. Song, J. Y., S. I. Kitamura, M. J. Oh, H. S. Kang, J. Lee, S. Tanaka and S. J. Jung (2009a): Pathogenicity of Miamiensis avidus (syn. Philasterides dicentrarchi), Pseudocohnilembus persalinus, Pseudocohnilembus hargisi and Uronema marinum (Ciliophora, Scuticociliatida). Dis. Aquat. Organ., 83, 133-143. Yoshinaga, T. and J. Nakazoe (1993): Isolation and in vitro cultivation of an unidentified ciliate causing scuticociliatosis in Japanese flounder (Paralichthys olivaceus). Fish Pathol., 28, 131-134. Jung, S. J., E. Y. Im, M. C. Strüder-Kypke, S. I. Kitamura and P. T. K. Woo (2011): Small subunit ribosomal RNA and mitochondrial cytochrome c oxidase subunit 1 gene sequences of 21 strains of the parasitic scuticociliate Miamiensis avidus (Ciliophora, Scuticociliatia). Parasitol. Res., 108, 1153-1161. Motokawa, S., Y. Narasaki, J. Y. Song, Y. Yokoyama, E. Hirose, S. Murakami, S. J. Jung, M. J. Oh, K. Nakayama and S. I. Kitamura (2018): Analysis of genes encoding high-antigenicity polypeptides in three serotypes of Miamiensis avidus. Parasitol. Int., 67, 196-202. Tolbert, M. K., S. H. Stauffer, M. D. Brand and J. L. Gookin (2014): Cysteine protease activity of feline Tritrichomonas foetus promotes adhesion-dependent cytotoxicity to intestinal epithelial cells. Infect. Immun., 82, 2851-2859. Cawthorn, R. J., D. H. Lynn, B. Despres, R. MacMillan, R. Maloney, M. Loughlin and R. Bayer (1996): Description of Anophyroides haemophila n. sp. (Scuticociliatida: Orchitophryidae), a pathogen of American lobsters Homarus americanus. Dis. Aquat. Organ., 24, 143-148. Munday, B. L., P. J. O’Donoghue, M. Watts, K. Rough and T. Hawkesford (1997): Fatal encephalitis due to the scuticociliate Uronema nigricans in sea-caged, southern bluefin tuna Thunnus maccoyii. Dis. Aquat. Organ., 30, 17-25. Imai, S., S. Tsurimaki, E. Goto, K. Wakita and K. Hatai (2000): Tetrahymena infection in guppy Poecilia reticulata. Fish Pathol., 35, 67-72. Olivier, M., V. D. Atayde, A. Isnard, K. Hassani and M. T. Shio (2012): Leishmania virulence factors: focus on the metalloprotease GP63. Microbes Infect., 14, 1377-1389. Thao, N. V., A. Nozawa, Y. Obayashi, S. I. Kitamura, T. Yokokawa and S. Suzuki (2015): Extracellular proteases are released by ciliates in defined seawater microcosms. Mar. Environ. Res., 109, 95-102. Jee, B. Y., Y. C. Kim and M. S. Park (2001): Morphology and biology of parasite responsible for scuticociliatosis of cultured olive flounder Paralichthys olivaceus. Dis. Aquat. Organ., 47, 49-55. Piazzon, C., J. Lamas and J. M. Leiro (2011): Role of scuticociliate proteinases in infection success in turbot, Psetta maxima (L.). Parasite Immunol., 33, 535-544. Obayashi, Y. and S. Suzuki (2008): Occurrence of exo- and endopeptidases in dissolved and particulate fractions of coastal seawater. Aquat. Microb. Ecol., 50, 231-237. Song, J. Y., K. Sasaki, T. Okada, M. Sakashita, H. Kawakami, S. Matsuoka, H. S. Kang, K. Nakayama, S. J. Jung, M. J. Oh and S. I. Kitamura (2009b): Antigenic differences of the scuticociliate Miamiensis avidus from Japan. J. Fish Dis., 32, 1027-1034. Castellino, F. J. and V. A. Ploplis (2005): Structure and function of the plasminogen/plasmin system. Thromb. Haemost., 93, 647-654. Takagishi, N., T. Yoshinaga and K. Ogawa (2009): Effect of hyposalinity on the infection and pathogenicity of Miamiensis avidus causing scuticociliatosis in olive flounder Paralichthys olivaceus. Dis. Aquat. Organ., 86, 175-179. Jung, S. J., S. I. Kitamura, J. Y. Song, I. Y. Joung and M. J. Oh (2005): Complete small subunit rRNA gene sequence of the scuticociliate Miamiensis avidus pathogenic to olive flounder Paralichthys olivaceus. Dis. Aquat. Organ., 64, 159-162. Paramá, A., R. Castro, J. A. Arranz, M. L. Sanmartín, J. Lamas and J. Leiro (2007b): Scuticociliate cysteine proteinases modulate turbot leucocyte functions. Fish Shellfish Immunol., 23, 945-956. Völkel, H., U. Kurz, J. Linder, S. Klumpp, V. Gnau, G. Jung and J. E. Schultz (1996): Cathepsin L is an intracellular and extracellular protease in Paramecium tetraurelia. Purification, cloning, sequencing and specific inhibition by its expressed propeptide. Eur. J. Biochem., 238, 198-206. Obayashi, Y. and S. Suzuki (2005): Proteolytic enzymes in coastal surface seawater: Significant activity of endopeptidases and exopeptidases. Limnol. Oceanogr., 50, 722-726. Shin, S. P., S. Y. Han, J. E. Han, J. W. Jun, J. H. Kim and S. C. Park (2014): Expression and characterization of cathepsin L-like cysteine protease from Philasterides dicentrarchi. Parasitol. Int., 63, 359-365. Leibowitz, M. P., R. Ofir, A. Golan-Goldhirsh and D. Zilberg (2009): Cysteine proteases and acid phosphatases contribute to Tetrahymena spp. pathogenicity in guppies, Poecilia reticulata. Vet. Parasitol., 166, 21-26. Kim, S. M., J. B. Cho, E. H. Lee, S. R. Kwon, S. K. Kim, Y. K. Nam and K. H. Kim (2004a): Pseudocohnilembus persalinus (Ciliophora: Scuticociitida) is an additional species causing scuticociliatosis in olive flounder Paralichthys olivaceus. Dis. Aquat. Organ., 62, 239-244. 22 23 24 25 26 27 28 29 30 31 10 32 11 33 12 34 13 35 14 36 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
References_xml | – ident: 2 – ident: 21 doi: 10.1016/j.ijpara.2006.08.013 – ident: 4 – ident: 29 doi: 10.3354/dao02017 – ident: 35 – ident: 15 doi: 10.1292/jvms.10-0214 – ident: 27 doi: 10.1016/j.exppara.2010.11.005 – ident: 16 doi: 10.3354/dao030017 – ident: 32 doi: 10.3354/dao02116 – ident: 6 doi: 10.3147/jsfp.35.67 – ident: 5 doi: 10.3354/dao046047 – ident: 28 doi: 10.1016/j.parint.2013.12.007 – ident: 11 doi: 10.3354/dao062239 – ident: 24 doi: 10.1354/vp.45-4-546 – ident: 7 doi: 10.3354/dao047049 – ident: 10 doi: 10.1007/s00436-010-2157-7 – ident: 3 doi: 10.1111/j.1365-2761.1980.tb00400.x – ident: 25 doi: 10.1016/j.dci.2008.05.002 – ident: 36 doi: 10.3147/jsfp.28.131 – ident: 18 doi: 10.3354/ame01169 – ident: 26 doi: 10.1016/S0166-6851(01)00438-8 – ident: 1 – ident: 8 doi: 10.3354/dao064159 – ident: 9 doi: 10.3354/dao073227 – ident: 13 doi: 10.1016/j.vetpar.2009.08.005 – ident: 34 doi: 10.1128/IAI.01671-14 – ident: 22 doi: 10.1016/j.fsi.2007.02.001 – ident: 33 doi: 10.1016/j.marenvres.2015.06.011 – ident: 20 doi: 10.1017/S0031182004004883 – ident: 31 doi: 10.1046/j.1432-1327.1998.2540006.x – ident: 12 doi: 10.3354/dao062233 – ident: 19 doi: 10.1016/j.micinf.2012.05.014 – ident: 17 doi: 10.4319/lo.2005.50.2.0722 – ident: 14 doi: 10.1016/j.parint.2017.10.007 – ident: 23 doi: 10.1111/j.1365-3024.2011.01310.x – ident: 30 doi: 10.1111/j.1365-2761.2009.01089.x |
SSID | ssib002484579 ssj0056303 |
Score | 2.1843095 |
Snippet | Miamiensis avidus is the causative agent of scuticociliatosis in various marine fish species. The virulence factors of the parasite have not been identified,... |
SourceID | proquest crossref jstage |
SourceType | Aggregation Database Publisher |
StartPage | 1 |
SubjectTerms | Cells Cytotoxicity Extracellular extracellular proteinase Fish Inhibitors Marine fishes Miamiensis avidus Mineral nutrients Nutrient uptake Peptides Proteinase inhibitors scuticociliatosis Serine Specificity Uptake Virulence virulence factor |
Title | Extracellular Proteinases of Miamiensis avidus Causing Scuticociliatosis are Potential Virulence Factors |
URI | https://www.jstage.jst.go.jp/article/jsfp/53/1/53_1/_article/-char/en https://www.proquest.com/docview/2022113955 |
Volume | 53 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
ispartofPNX | Fish Pathology, 2018, Vol.53(1), pp.1-9 |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3Lb9MwGLfK4AAHxFMrDGQhdooymsRpkmNVWgaMbdJaVE6R7dhbV5ZMaSJRTvzpfH40TbUJAZeotd2k8vfL9_L3QOit7HMQY17sxkBTl3DQ4ZgUvhsIUEd9JjnT1fa_HPcPp-TTLJx1Or9aUUt1xQ74z1vzSv6HqjAGdFVZsv9A2eamMACfgb5wBQrD9a9oPPpRlVS53nUs6akquTDPQSyZwBaVsq3C05eOiluvl86Q1tozcMaVBxuo8h3oUugFpXBO4dd5pRzoX-dlrXORnLHpxtPWYD-sCrYq9ofD_Zg4C5EvVnXjUKYlXVLTB_tbvZg3mDlhdKWaNpmJq_miaBCpuzg5ZzB_NW8Rny7gu565KOxq65qwfFQLDBD0G-6kTgA2BwXOQCeVtvhcAGQFS3xmRJLhw3HsuVFgKpmsGbWpKrwFSMN1vdtkQeARdRp9uZTXB2Fw4G0E3vqQ__gkHU-PjtLJaDa5g-76wKpUUOj7j59bCkxM9Dmmke2qmJppuG3_sqlVpR71rnnQloZz7xKU_PObkl6rL5NH6KG1O_DAgOgx6oj8CXowOC9t7RXxFF1swQm34IQLiTdwwgZO2MIJ34ATBjjhBk64gRO2cHqGpuPRZHjo2kYcLgd9v3KzhPd4IjLJE7Bvo34m_EgISRglnHFQcFgvYonMwHbvxYJEPJO9iDJfgDLIwN4OnqOdvMjFLsLES6RgxBNhEhASKntdCklFn1HKkox20Zv15qXXpt5KCnaq2uFU7XAaBqnXRaHZ1maJfQU3S8xlPawyGIFhdNHemgqpfY2XqQ9arAd2UBi--PP0S3Rfgdz43_bQTlXW4hVopBV7rUHzG2dAmAI |
link.rule.ids | 315,783,787,4031,27935,27936,27937 |
linkProvider | Flying Publisher |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Extracellular+Proteinases+of+Miamiensis+avidus+Causing+Scuticociliatosis+are+Potential+Virulence+Factors&rft.jtitle=Gyobyo%CC%84+kenkyu&rft.au=Narasaki%2C+Yukie&rft.au=Obayashi%2C+Yumiko&rft.au=Ito%2C+Sayami&rft.au=Murakami%2C+Shoko&rft.date=2018&rft.pub=Japan+Science+and+Technology+Agency&rft.issn=0388-788X&rft.eissn=1881-7335&rft.volume=53&rft.issue=1&rft.spage=1&rft_id=info:doi/10.3147%2Fjsfp.53.1&rft.externalDBID=NO_FULL_TEXT |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0388-788X&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0388-788X&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0388-788X&client=summon |