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Vaccination with Intradermal Bacillus Calmette–Guérin Provides Robust Protection against Extrapulmonary Tuberculosis but Not Pulmonary Infection in Cynomolgus Macaques

Yusuke Tsujimura, Yumiko Shiogama, Shogo Soma, Tomotaka Okamura, Junichiro Takano, Emiko Urano, Yoshiko Murakata, Akira Kawano, Natsuko Yamakawa, Masamitsu N. Asaka, Kazuhiro Matsuo and Yasuhiro Yasutomi
J Immunol October 23, 2020, ji2000386; DOI: https://doi.org/10.4049/jimmunol.2000386
Yusuke Tsujimura
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
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Yumiko Shiogama
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
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Shogo Soma
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
†Department of Immunoregulation, Mie University Graduate School of Medicine, 514-8507 Tsu, Mie, Japan; and
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Tomotaka Okamura
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
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Junichiro Takano
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
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Emiko Urano
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
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Yoshiko Murakata
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
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Akira Kawano
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
†Department of Immunoregulation, Mie University Graduate School of Medicine, 514-8507 Tsu, Mie, Japan; and
‡Research and Development Department, Japan BCG Laboratory, 204-0022 Kiyose, Tokyo, Japan
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Natsuko Yamakawa
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
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Masamitsu N. Asaka
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
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Kazuhiro Matsuo
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
‡Research and Development Department, Japan BCG Laboratory, 204-0022 Kiyose, Tokyo, Japan
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Yasuhiro Yasutomi
*Laboratory of Immunoregulation and Vaccine Research, Tsukuba Primate Research Center, National Institutes of Biomedical Innovation, Health and Nutrition, 305-0843 Tsukuba, Ibaraki, Japan;
†Department of Immunoregulation, Mie University Graduate School of Medicine, 514-8507 Tsu, Mie, Japan; and
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Key Points

  • Intradermal BCG vaccination cannot protect cynomolgus macaques against pulmonary TB.

  • Extrapulmonary TB is strongly controlled in intradermal BCG–vaccinated monkeys.

Abstract

Recently, the efficacy of Mycobacterium bovis bacillus Calmette–Guérin (BCG) vaccination is being reassessed in accordance with the achievements of clinical tuberculosis (TB) vaccine research. However, the mechanisms ultimately determining the success or failure of BCG vaccination to prevent pulmonary TB remain poorly understood. In this study, we analyzed the protective effects of intradermal BCG vaccination by using specific pathogen–free cynomolgus macaques of Asian origin that were intradermally vaccinated with BCG (Tokyo strain) followed by Mycobacterium tuberculosis (Erdman strain) infection. Intradermal BCG administration generated TB Ag-specific multifunctional CD4 T cell responses in peripheral blood and bronchoalveolar lavage and almost completely protected against the development of TB pathogenesis with aggravation of clinical parameters and high levels of bacterial burdens in extrapulmonary organs. However, interestingly, there were no differences in bacterial quantitation and pathology of extensive granulomas in the lungs between BCG-vaccinated monkeys and control animals. These results indicated that the changes in clinical parameters, immunological responses, and quantitative gross pathology that are used routinely to determine the efficacy of TB vaccines in nonhuman primate models might not correlate with the bacterial burden and histopathological score in the lung as measured in this study.

Footnotes

  • This work was supported by Health Science Research grants from the Ministry of Health, Labor and Welfare of Japan (17H04079), the Ministry of Education, Culture, Sports, Science and Technology of Japan (19K08968), and Research on Development of New Drugs, Research Program on Emerging and Re-emerging Infectious Diseases from the Japan Agency for Medical Research and Development (18fk0108007h0003, 19ak0101047h0004). The funders had no role in the study design, data collection, interpretation, and decision to submit this work for publication.

  • The online version of this article contains supplemental material.

  • Received April 8, 2020.
  • Accepted September 22, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 208 (11)
The Journal of Immunology
Vol. 208, Issue 11
1 Jun 2022
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Vaccination with Intradermal Bacillus Calmette–Guérin Provides Robust Protection against Extrapulmonary Tuberculosis but Not Pulmonary Infection in Cynomolgus Macaques
Yusuke Tsujimura, Yumiko Shiogama, Shogo Soma, Tomotaka Okamura, Junichiro Takano, Emiko Urano, Yoshiko Murakata, Akira Kawano, Natsuko Yamakawa, Masamitsu N. Asaka, Kazuhiro Matsuo, Yasuhiro Yasutomi
The Journal of Immunology October 23, 2020, ji2000386; DOI: 10.4049/jimmunol.2000386

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Vaccination with Intradermal Bacillus Calmette–Guérin Provides Robust Protection against Extrapulmonary Tuberculosis but Not Pulmonary Infection in Cynomolgus Macaques
Yusuke Tsujimura, Yumiko Shiogama, Shogo Soma, Tomotaka Okamura, Junichiro Takano, Emiko Urano, Yoshiko Murakata, Akira Kawano, Natsuko Yamakawa, Masamitsu N. Asaka, Kazuhiro Matsuo, Yasuhiro Yasutomi
The Journal of Immunology October 23, 2020, ji2000386; DOI: 10.4049/jimmunol.2000386
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