Evaluation of Recombinant Type-Specific Antigens of Orientia tsutsugamushi Expressed by a Baculovirus-Insect Cell System as Antigens for Indirect Immunofluorescence Assay in the Serological Diagnosis of Scrub Typhus

Scrub typhus (ST) is a mite-borne rickettsiosis caused by the intracellular bacterium Orientia tsutsugamushi (OTS), which is classified as a biosafety level-3 (BSL-3) pathogen. For serological tests of ST, mouse fibroblast cells infected with the five prevalent serotypes of OTS in Japan are generall...

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Published inJapanese Journal of Infectious Diseases Vol. 73; no. 5; pp. 330 - 335
Main Authors Ogawa, Motohiko, Ando, Shuji, Saijo, Masayuki
Format Journal Article
LanguageEnglish
Published Japan National Institute of Infectious Diseases, Japanese Journal of Infectious Diseases Editorial Committee 30.09.2020
Subjects
Animals
Antibodies, Bacterial - blood
Antigens, Bacterial - blood
Baculoviridae - metabolism
Fluorescent Antibody Technique, Indirect - methods
Humans
Immunoglobulin G - blood
Immunoglobulin M - blood
Japan
Mice
Orientia tsutsugamushi
Orientia tsutsugamushi - immunology
Orientia tsutsugamushi - isolation & purification
Recombinant Proteins - immunology
recombinant type-specific antigens
scrub typhus
Scrub Typhus - blood
Scrub Typhus - diagnosis
Serogroup
Serologic Tests
serological diagnosis
Sf9 Cells
Japan
Orientia tsutsugamushi
serological diagnosis
recombinant type-specific antigens
scrub typhus
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Abstract Scrub typhus (ST) is a mite-borne rickettsiosis caused by the intracellular bacterium Orientia tsutsugamushi (OTS), which is classified as a biosafety level-3 (BSL-3) pathogen. For serological tests of ST, mouse fibroblast cells infected with the five prevalent serotypes of OTS in Japan are generally used as antigens for indirect immunofluorescence assay (IFA). In this study, Spodoptera frugiperda derived insect cell line (Sf9) cells infected with recombinant type-specific antigen (rTSA)-expressing baculovirus were used for IFA. The paired serum samples of 15 ST patients, 10 rickettsiosis patients, and 10 control individuals were used. IgM and IgG titers determined by the rTSA-based IFA were correlated with those determined by the OTS-infected cell-based IFA (R2 = 0.7319 to 0.7956). Based on the criteria for serological diagnosis, such as a suitable cutoff for single serum samples (IgM ≥ 1:160) and/or a significant increase in IgG titers between paired sera (≥ 4-fold), all 15 ST patients diagnosed as positive with the OTS-infected cell-based IFA were also diagnosed as positive by the rTSA-based IFA, whereas all 10 rickettsiosis patients and 10 control individuals were not. Thus, the rTSAs, which can be prepared in BSL-2 laboratories, are efficacious for the serological diagnosis of ST.
AbstractList Scrub typhus (ST) is a mite-borne rickettsiosis caused by the intracellular bacterium Orientia tsutsugamushi (OTS), which is classified as a biosafety level-3 (BSL-3) pathogen. For serological tests of ST, mouse fibroblast cells infected with the five prevalent serotypes of OTS in Japan are generally used as antigens for indirect immunofluorescence assay (IFA). In this study, Spodoptera frugiperda derived insect cell line (Sf9) cells infected with recombinant type-specific antigen (rTSA)-expressing baculovirus were used for IFA. The paired serum samples of 15 ST patients, 10 rickettsiosis patients, and 10 control individuals were used. IgM and IgG titers determined by the rTSA-based IFA were correlated with those determined by the OTS-infected cell-based IFA (R2 = 0.7319 to 0.7956). Based on the criteria for serological diagnosis, such as a suitable cutoff for single serum samples (IgM ≥ 1:160) and/or a significant increase in IgG titers between paired sera (≥ 4-fold), all 15 ST patients diagnosed as positive with the OTS-infected cell-based IFA were also diagnosed as positive by the rTSA-based IFA, whereas all 10 rickettsiosis patients and 10 control individuals were not. Thus, the rTSAs, which can be prepared in BSL-2 laboratories, are efficacious for the serological diagnosis of ST.Scrub typhus (ST) is a mite-borne rickettsiosis caused by the intracellular bacterium Orientia tsutsugamushi (OTS), which is classified as a biosafety level-3 (BSL-3) pathogen. For serological tests of ST, mouse fibroblast cells infected with the five prevalent serotypes of OTS in Japan are generally used as antigens for indirect immunofluorescence assay (IFA). In this study, Spodoptera frugiperda derived insect cell line (Sf9) cells infected with recombinant type-specific antigen (rTSA)-expressing baculovirus were used for IFA. The paired serum samples of 15 ST patients, 10 rickettsiosis patients, and 10 control individuals were used. IgM and IgG titers determined by the rTSA-based IFA were correlated with those determined by the OTS-infected cell-based IFA (R2 = 0.7319 to 0.7956). Based on the criteria for serological diagnosis, such as a suitable cutoff for single serum samples (IgM ≥ 1:160) and/or a significant increase in IgG titers between paired sera (≥ 4-fold), all 15 ST patients diagnosed as positive with the OTS-infected cell-based IFA were also diagnosed as positive by the rTSA-based IFA, whereas all 10 rickettsiosis patients and 10 control individuals were not. Thus, the rTSAs, which can be prepared in BSL-2 laboratories, are efficacious for the serological diagnosis of ST.
Scrub typhus (ST) is a mite-borne rickettsiosis caused by the intracellular bacterium Orientia tsutsugamushi (OTS), which is classified as a biosafety level-3 (BSL-3) pathogen. For serological tests of ST, mouse fibroblast cells infected with the five prevalent serotypes of OTS in Japan are generally used as antigens for indirect immunofluorescence assay (IFA). In this study, Spodoptera frugiperda derived insect cell line (Sf9) cells infected with recombinant type-specific antigen (rTSA)-expressing baculovirus were used for IFA. The paired serum samples of 15 ST patients, 10 rickettsiosis patients, and 10 control individuals were used. IgM and IgG titers determined by the rTSA-based IFA were correlated with those determined by the OTS-infected cell-based IFA (R2 = 0.7319 to 0.7956). Based on the criteria for serological diagnosis, such as a suitable cutoff for single serum samples (IgM ≥ 1:160) and/or a significant increase in IgG titers between paired sera (≥ 4-fold), all 15 ST patients diagnosed as positive with the OTS-infected cell-based IFA were also diagnosed as positive by the rTSA-based IFA, whereas all 10 rickettsiosis patients and 10 control individuals were not. Thus, the rTSAs, which can be prepared in BSL-2 laboratories, are efficacious for the serological diagnosis of ST.
Scrub typhus (ST) is a mite-borne rickettsiosis caused by the intracellular bacterium Orientia tsutsugamushi (OTS), which is classified as a biosafety level-3 (BSL-3) pathogen. For serological tests of ST, mouse fibroblast cells infected with the five prevalent serotypes of OTS in Japan are generally used as antigens for indirect immunofluorescence assay (IFA). In this study, Spodoptera frugiperda derived insect cell line (Sf9) cells infected with recombinant type-specific antigen (rTSA)-expressing baculovirus were used for IFA. The paired serum samples of 15 ST patients, 10 rickettsiosis patients, and 10 control individuals were used. IgM and IgG titers determined by the rTSA-based IFA were correlated with those determined by the OTS-infected cell-based IFA (R = 0.7319 to 0.7956). Based on the criteria for serological diagnosis, such as a suitable cutoff for single serum samples (IgM ≥ 1:160) and/or a significant increase in IgG titers between paired sera (≥ 4-fold), all 15 ST patients diagnosed as positive with the OTS-infected cell-based IFA were also diagnosed as positive by the rTSA-based IFA, whereas all 10 rickettsiosis patients and 10 control individuals were not. Thus, the rTSAs, which can be prepared in BSL-2 laboratories, are efficacious for the serological diagnosis of ST.
Author Ogawa, Motohiko
Ando, Shuji
Saijo, Masayuki
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Cites_doi 10.11150/kansenshogakuzasshi1970.75.359
10.1099/00207713-45-3-589
10.1016/j.vaccine.2012.05.005
10.1196/annals.1374.069
10.1111/j.1651-2227.2006.00178.x
10.4269/ajtmh.14-0627
10.1128/JVI.01403-18
10.1007/978-1-60761-913-0_16
10.1128/CDLI.5.4.519-526.1998
10.1128/jcm.9.1.38-48.1979
10.11150/kansenshogakuzasshi1970.63.109
10.1016/j.micinf.2014.09.004
10.4269/ajtmh.18-0391
10.1128/JCM.31.3.598-605.1993
10.1111/j.1348-0421.1986.tb02988.x
10.1093/infdis/159.6.1122
10.1186/s12866-016-0910-5
10.1038/227680a0
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serological diagnosis
recombinant type-specific antigens
scrub typhus
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References 9. Yang SL, Tsai KH, Chen HF, et al. Evaluation of enzyme-linked immunosorbent assay using recombinant 56-kDa type-specific antigens derived from multiple Orientia tsutsugamushi strains for detection of scrub typhus infection. Am J Trop Med Hyg. 2019; 100: 532-9.
11. Uchida T, Yu XJ, Uchiyama T, et al. Identification of a unique spotted fever group rickettsia from humans in Japan. J Infect Dis. 1989; 159: 1122-6.
18. Santiago FW, Lambert Emo K, Fitzgerald T, et al. Antigenic and immunogenic properties of recombinant hemagglutinin proteins from H1N1 A/Brisbane/59/07 and B/Florida/04/06 when produced in various protein expression systems. Vaccine. 2012; 30: 4606-16.
10. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227: 680-5.
2. Kawamura A, Tanaka H, Tamura A. Epidemiological and clinical aspects. In: Kawamura A, Tanaka H, Tamura A, editors. Tsutsugamushi Disease. Tokyo, Japan: University of Tokyo Press; 1995. p.105-58.
3. Ministry of Health, Labour and Welfare and National Institute of Infectious Diseases. [Annual cases of scrub typhus], Infect Dis Wkly Rep Jpn. Available at: <http://www.nih.go.jp/niid/en/idwr-e.html>. Japanese.
1. Tamura A, Ohashi N, Urakami H, et al. Classification of Rickettsia tsutsugamushi in a new genus, Orientia gen. nov., as Orientia tsutsugamushi comb. nov. Int J Syst Bacteriol. 1995; 45: 589-91.
14. Dasch GA, Halle S, Bourgeois AL. Sensitive microplate enzyme-linked immunosorbent assay for detection of antibodies against the scrub typhus rickettsia, Rickettsia tsutsugamushi. J Clin Microbiol. 1979; 9: 38-48.
19. Urbanowicz RA, Wang R, Schiel JE, et al. Antigenicity and immunogenicity of differentially glycosylated hepatitis C virus E2 envelope proteins expressed in mammalian and insect cells. J Virol. 2019; 93: e01403-18.
12. Ogawa M, Fukasawa M, Satoh M, et al. The intracellular pathogen Orientia tsutsugamushi responsible for scrub typhus induces lipid droplet formation in mouse fibroblasts. Microbes Infect. 2014; 16: 962-6.
13. Ogawa M, Matsumoto K, Parola P, et al. Expression of rOmpA and rOmpB protein in Rickettsia massiliae during the Rhipicephalus turanicus life cycle. Ann N Y Acad Sci. 2006; 1078: 352-6.
4. Yamamoto S, Kawabata N, Ooura K, et al. Antigenic types of Rickettsia tsutsugamushi isolated from patients with tsutsugamushi fever and their distribution in Miyazaki Prefecture. Kansenshogaku Zasshi. 1989; 63: 109-17. Japanese.
6. Ogawa M, Hagiwara T, Kishimoto T, et al. Tsutsugamushi disease (scrub typhus) in Japan: epidemiological aspects. Kansenshogaku Zasshi. 2001; 75: 353-8. Japanese.
5. Yamamoto S, Kawabata N, Tamura A, et al. Immunological properties of Rickettsia tsutsugamushi, Kawasaki strain, isolated from a patient in Kyushu. Microbiol Immunol. 1986; 30: 611-20.
17. O'Shaughnessy L, Doyle S. Purification of proteins from baculovirus-infected insect cells. Methods Mol Biol. 2011; 681: 295-309.
20. Rodkvamtook W, Zhang Z, Chao CC, et al. Dot-ELISA rapid test using recombinant 56-kDa protein antigens for serodiagnosis of scrub typhus. Am J Trop Med Hyg. 2015; 92: 967-71.
15. Ogawa M, Satoh M, Saijo M, et al. Evaluation of a broad-ranging and convenient enzyme-linked immunosorbent assay using the lysate of infected cells with five serotypes of Orientia tsutsugamushi, a causative agent of scrub typhus. BMC Microbiol. 2017; 17: 7.
7. Ching WM, Wang H, Eamsila C, et al. Expression and refolding of truncated recombinant major outer membrane protein antigen (r56) of Orientia tsutsugamushi and its use in enzyme-linked immunosorbent assays. Clin Diagn Lab Immunol. 1998; 5: 519-26.
16. Akobeng AK. Understanding diagnostic tests 3: Receiver operating characteristic curves. Acta Paediatr. 2007; 96: 644-7.
8. Kim IS, Seong SY, Woo SG, et al. High-level expression of a 56-kilodalton protein gene (bor56) of Rickettsia tsutsugamushi Boryong and its application to enzyme-linked immunosorbent assays. J Clin Microbiol. 1993; 31: 598-605.
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12
13
14
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16
17
18
19
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2
3
4
5
6
7
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References_xml – reference: 15. Ogawa M, Satoh M, Saijo M, et al. Evaluation of a broad-ranging and convenient enzyme-linked immunosorbent assay using the lysate of infected cells with five serotypes of Orientia tsutsugamushi, a causative agent of scrub typhus. BMC Microbiol. 2017; 17: 7.
– reference: 3. Ministry of Health, Labour and Welfare and National Institute of Infectious Diseases. [Annual cases of scrub typhus], Infect Dis Wkly Rep Jpn. Available at: <http://www.nih.go.jp/niid/en/idwr-e.html>. Japanese.
– reference: 5. Yamamoto S, Kawabata N, Tamura A, et al. Immunological properties of Rickettsia tsutsugamushi, Kawasaki strain, isolated from a patient in Kyushu. Microbiol Immunol. 1986; 30: 611-20.
– reference: 16. Akobeng AK. Understanding diagnostic tests 3: Receiver operating characteristic curves. Acta Paediatr. 2007; 96: 644-7.
– reference: 14. Dasch GA, Halle S, Bourgeois AL. Sensitive microplate enzyme-linked immunosorbent assay for detection of antibodies against the scrub typhus rickettsia, Rickettsia tsutsugamushi. J Clin Microbiol. 1979; 9: 38-48.
– reference: 18. Santiago FW, Lambert Emo K, Fitzgerald T, et al. Antigenic and immunogenic properties of recombinant hemagglutinin proteins from H1N1 A/Brisbane/59/07 and B/Florida/04/06 when produced in various protein expression systems. Vaccine. 2012; 30: 4606-16.
– reference: 11. Uchida T, Yu XJ, Uchiyama T, et al. Identification of a unique spotted fever group rickettsia from humans in Japan. J Infect Dis. 1989; 159: 1122-6.
– reference: 1. Tamura A, Ohashi N, Urakami H, et al. Classification of Rickettsia tsutsugamushi in a new genus, Orientia gen. nov., as Orientia tsutsugamushi comb. nov. Int J Syst Bacteriol. 1995; 45: 589-91.
– reference: 12. Ogawa M, Fukasawa M, Satoh M, et al. The intracellular pathogen Orientia tsutsugamushi responsible for scrub typhus induces lipid droplet formation in mouse fibroblasts. Microbes Infect. 2014; 16: 962-6.
– reference: 17. O'Shaughnessy L, Doyle S. Purification of proteins from baculovirus-infected insect cells. Methods Mol Biol. 2011; 681: 295-309.
– reference: 20. Rodkvamtook W, Zhang Z, Chao CC, et al. Dot-ELISA rapid test using recombinant 56-kDa protein antigens for serodiagnosis of scrub typhus. Am J Trop Med Hyg. 2015; 92: 967-71.
– reference: 6. Ogawa M, Hagiwara T, Kishimoto T, et al. Tsutsugamushi disease (scrub typhus) in Japan: epidemiological aspects. Kansenshogaku Zasshi. 2001; 75: 353-8. Japanese.
– reference: 13. Ogawa M, Matsumoto K, Parola P, et al. Expression of rOmpA and rOmpB protein in Rickettsia massiliae during the Rhipicephalus turanicus life cycle. Ann N Y Acad Sci. 2006; 1078: 352-6.
– reference: 9. Yang SL, Tsai KH, Chen HF, et al. Evaluation of enzyme-linked immunosorbent assay using recombinant 56-kDa type-specific antigens derived from multiple Orientia tsutsugamushi strains for detection of scrub typhus infection. Am J Trop Med Hyg. 2019; 100: 532-9.
– reference: 8. Kim IS, Seong SY, Woo SG, et al. High-level expression of a 56-kilodalton protein gene (bor56) of Rickettsia tsutsugamushi Boryong and its application to enzyme-linked immunosorbent assays. J Clin Microbiol. 1993; 31: 598-605.
– reference: 10. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227: 680-5.
– reference: 19. Urbanowicz RA, Wang R, Schiel JE, et al. Antigenicity and immunogenicity of differentially glycosylated hepatitis C virus E2 envelope proteins expressed in mammalian and insect cells. J Virol. 2019; 93: e01403-18.
– reference: 7. Ching WM, Wang H, Eamsila C, et al. Expression and refolding of truncated recombinant major outer membrane protein antigen (r56) of Orientia tsutsugamushi and its use in enzyme-linked immunosorbent assays. Clin Diagn Lab Immunol. 1998; 5: 519-26.
– reference: 2. Kawamura A, Tanaka H, Tamura A. Epidemiological and clinical aspects. In: Kawamura A, Tanaka H, Tamura A, editors. Tsutsugamushi Disease. Tokyo, Japan: University of Tokyo Press; 1995. p.105-58.
– reference: 4. Yamamoto S, Kawabata N, Ooura K, et al. Antigenic types of Rickettsia tsutsugamushi isolated from patients with tsutsugamushi fever and their distribution in Miyazaki Prefecture. Kansenshogaku Zasshi. 1989; 63: 109-17. Japanese.
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  doi: 10.1111/j.1651-2227.2006.00178.x
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  doi: 10.4269/ajtmh.14-0627
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  doi: 10.1128/JVI.01403-18
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  doi: 10.1007/978-1-60761-913-0_16
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  doi: 10.1128/CDLI.5.4.519-526.1998
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  doi: 10.1128/jcm.9.1.38-48.1979
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  doi: 10.11150/kansenshogakuzasshi1970.63.109
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  doi: 10.1016/j.micinf.2014.09.004
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  doi: 10.4269/ajtmh.18-0391
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  doi: 10.1128/JCM.31.3.598-605.1993
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  doi: 10.1111/j.1348-0421.1986.tb02988.x
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  doi: 10.1093/infdis/159.6.1122
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  doi: 10.1038/227680a0
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Snippet Scrub typhus (ST) is a mite-borne rickettsiosis caused by the intracellular bacterium Orientia tsutsugamushi (OTS), which is classified as a biosafety level-3...
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SubjectTerms Animals
Antibodies, Bacterial - blood
Antigens, Bacterial - blood
Baculoviridae - metabolism
Fluorescent Antibody Technique, Indirect - methods
Humans
Immunoglobulin G - blood
Immunoglobulin M - blood
Japan
Mice
Orientia tsutsugamushi
Orientia tsutsugamushi - immunology
Orientia tsutsugamushi - isolation & purification
Recombinant Proteins - immunology
recombinant type-specific antigens
scrub typhus
Scrub Typhus - blood
Scrub Typhus - diagnosis
Serogroup
Serologic Tests
serological diagnosis
Sf9 Cells
Title Evaluation of Recombinant Type-Specific Antigens of Orientia tsutsugamushi Expressed by a Baculovirus-Insect Cell System as Antigens for Indirect Immunofluorescence Assay in the Serological Diagnosis of Scrub Typhus
URI https://www.jstage.jst.go.jp/article/yoken/73/5/73_JJID.2019.334/_article/-char/en
https://www.ncbi.nlm.nih.gov/pubmed/32350215
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ispartofPNX Japanese Journal of Infectious Diseases, 2020/09/30, Vol.73(5), pp.330-335
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linkProvider Geneva Foundation for Medical Education and Research
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