Adipose tissue is the first colonization site of Leptospira interrogans in subcutaneously infected hamsters

Ryo Ozuru, Mitsumasa Saito, Takaaki Kanemaru, Satoshi Miyahara, Sharon Y.A.M. Villanueva, Gerald L. Murray, Ben Adler, Jun Fujii, Shin Ichi Yoshida

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Leptospirosis is one of the most widespread zoonoses in the world, and its most severe form in humans, Weil's disease,° may lead to jaundice, hemorrhage, renal failure, pulmonary hemorrhage syndrome, and sometimes,fatal multiple organ failure. Although the mechanisms underlying jaundice in leptospirosis have been gradually unraveled, the pathophysiology and distribution of leptospires during the early stage of infection are not well understood. Therefore, we investigated the hamster leptospirosis model, which is the accepted animal model of human Weil's disease, by using an in vivo imaging system to observe the whole bodies of animals infected with Leptospira interrogans and to identify the colonization and growth sites of the leptospires during the early phase of infection. Hamsters, infected subcutaneously with 104 bioluminescent leptospires, were analyzed by in vivo imaging, organ culture, and microscopy. The results showed that the luminescence from the leptospires spread through each hamster's body sequentially. The luminescence was first detected at the injection site only, and finally spread to the central abdomen, in the liver area. Additionally, the luminescence observed in the adipose tissue was the earliest detectable compared with the other organs, indicating that the leptospires colonized the adipose tissue at the early stage of leptospirosis. Adipose tissue cultures of the leptospires became positive earlier than the blood cultures. Microscopic analysis revealed that the leptospires colonized the inner walls of the blood vessels in the adipose tissue. In conclusion, this is the first study to report that adipose tissue is an important colonization site for leptospires, as demonstrated by microscopy and culture analyses of adipose tissue in the hamster model of Weil's disease.

Original languageEnglish
Article numbere0172973
Number of pages13
JournalPLoS ONE
Volume12
Issue number2
DOIs
Publication statusPublished - 28 Feb 2017

Keywords

  • hamsters
  • luminescence
  • leptospira
  • adipose tissue
  • leptospira interrogans
  • leptospirosis
  • blood
  • blood vessels

Cite this

Ozuru, R., Saito, M., Kanemaru, T., Miyahara, S., Villanueva, S. Y. A. M., Murray, G. L., ... Yoshida, S. I. (2017). Adipose tissue is the first colonization site of Leptospira interrogans in subcutaneously infected hamsters. PLoS ONE, 12(2), [e0172973]. https://doi.org/10.1371/journal.pone.0172973
Ozuru, Ryo ; Saito, Mitsumasa ; Kanemaru, Takaaki ; Miyahara, Satoshi ; Villanueva, Sharon Y.A.M. ; Murray, Gerald L. ; Adler, Ben ; Fujii, Jun ; Yoshida, Shin Ichi. / Adipose tissue is the first colonization site of Leptospira interrogans in subcutaneously infected hamsters. In: PLoS ONE. 2017 ; Vol. 12, No. 2.
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title = "Adipose tissue is the first colonization site of Leptospira interrogans in subcutaneously infected hamsters",
abstract = "Leptospirosis is one of the most widespread zoonoses in the world, and its most severe form in humans, Weil's disease,° may lead to jaundice, hemorrhage, renal failure, pulmonary hemorrhage syndrome, and sometimes,fatal multiple organ failure. Although the mechanisms underlying jaundice in leptospirosis have been gradually unraveled, the pathophysiology and distribution of leptospires during the early stage of infection are not well understood. Therefore, we investigated the hamster leptospirosis model, which is the accepted animal model of human Weil's disease, by using an in vivo imaging system to observe the whole bodies of animals infected with Leptospira interrogans and to identify the colonization and growth sites of the leptospires during the early phase of infection. Hamsters, infected subcutaneously with 104 bioluminescent leptospires, were analyzed by in vivo imaging, organ culture, and microscopy. The results showed that the luminescence from the leptospires spread through each hamster's body sequentially. The luminescence was first detected at the injection site only, and finally spread to the central abdomen, in the liver area. Additionally, the luminescence observed in the adipose tissue was the earliest detectable compared with the other organs, indicating that the leptospires colonized the adipose tissue at the early stage of leptospirosis. Adipose tissue cultures of the leptospires became positive earlier than the blood cultures. Microscopic analysis revealed that the leptospires colonized the inner walls of the blood vessels in the adipose tissue. In conclusion, this is the first study to report that adipose tissue is an important colonization site for leptospires, as demonstrated by microscopy and culture analyses of adipose tissue in the hamster model of Weil's disease.",
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author = "Ryo Ozuru and Mitsumasa Saito and Takaaki Kanemaru and Satoshi Miyahara and Villanueva, {Sharon Y.A.M.} and Murray, {Gerald L.} and Ben Adler and Jun Fujii and Yoshida, {Shin Ichi}",
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Ozuru, R, Saito, M, Kanemaru, T, Miyahara, S, Villanueva, SYAM, Murray, GL, Adler, B, Fujii, J & Yoshida, SI 2017, 'Adipose tissue is the first colonization site of Leptospira interrogans in subcutaneously infected hamsters', PLoS ONE, vol. 12, no. 2, e0172973. https://doi.org/10.1371/journal.pone.0172973

Adipose tissue is the first colonization site of Leptospira interrogans in subcutaneously infected hamsters. / Ozuru, Ryo; Saito, Mitsumasa; Kanemaru, Takaaki; Miyahara, Satoshi; Villanueva, Sharon Y.A.M.; Murray, Gerald L.; Adler, Ben; Fujii, Jun; Yoshida, Shin Ichi.

In: PLoS ONE, Vol. 12, No. 2, e0172973, 28.02.2017.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Adipose tissue is the first colonization site of Leptospira interrogans in subcutaneously infected hamsters

AU - Ozuru, Ryo

AU - Saito, Mitsumasa

AU - Kanemaru, Takaaki

AU - Miyahara, Satoshi

AU - Villanueva, Sharon Y.A.M.

AU - Murray, Gerald L.

AU - Adler, Ben

AU - Fujii, Jun

AU - Yoshida, Shin Ichi

PY - 2017/2/28

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N2 - Leptospirosis is one of the most widespread zoonoses in the world, and its most severe form in humans, Weil's disease,° may lead to jaundice, hemorrhage, renal failure, pulmonary hemorrhage syndrome, and sometimes,fatal multiple organ failure. Although the mechanisms underlying jaundice in leptospirosis have been gradually unraveled, the pathophysiology and distribution of leptospires during the early stage of infection are not well understood. Therefore, we investigated the hamster leptospirosis model, which is the accepted animal model of human Weil's disease, by using an in vivo imaging system to observe the whole bodies of animals infected with Leptospira interrogans and to identify the colonization and growth sites of the leptospires during the early phase of infection. Hamsters, infected subcutaneously with 104 bioluminescent leptospires, were analyzed by in vivo imaging, organ culture, and microscopy. The results showed that the luminescence from the leptospires spread through each hamster's body sequentially. The luminescence was first detected at the injection site only, and finally spread to the central abdomen, in the liver area. Additionally, the luminescence observed in the adipose tissue was the earliest detectable compared with the other organs, indicating that the leptospires colonized the adipose tissue at the early stage of leptospirosis. Adipose tissue cultures of the leptospires became positive earlier than the blood cultures. Microscopic analysis revealed that the leptospires colonized the inner walls of the blood vessels in the adipose tissue. In conclusion, this is the first study to report that adipose tissue is an important colonization site for leptospires, as demonstrated by microscopy and culture analyses of adipose tissue in the hamster model of Weil's disease.

AB - Leptospirosis is one of the most widespread zoonoses in the world, and its most severe form in humans, Weil's disease,° may lead to jaundice, hemorrhage, renal failure, pulmonary hemorrhage syndrome, and sometimes,fatal multiple organ failure. Although the mechanisms underlying jaundice in leptospirosis have been gradually unraveled, the pathophysiology and distribution of leptospires during the early stage of infection are not well understood. Therefore, we investigated the hamster leptospirosis model, which is the accepted animal model of human Weil's disease, by using an in vivo imaging system to observe the whole bodies of animals infected with Leptospira interrogans and to identify the colonization and growth sites of the leptospires during the early phase of infection. Hamsters, infected subcutaneously with 104 bioluminescent leptospires, were analyzed by in vivo imaging, organ culture, and microscopy. The results showed that the luminescence from the leptospires spread through each hamster's body sequentially. The luminescence was first detected at the injection site only, and finally spread to the central abdomen, in the liver area. Additionally, the luminescence observed in the adipose tissue was the earliest detectable compared with the other organs, indicating that the leptospires colonized the adipose tissue at the early stage of leptospirosis. Adipose tissue cultures of the leptospires became positive earlier than the blood cultures. Microscopic analysis revealed that the leptospires colonized the inner walls of the blood vessels in the adipose tissue. In conclusion, this is the first study to report that adipose tissue is an important colonization site for leptospires, as demonstrated by microscopy and culture analyses of adipose tissue in the hamster model of Weil's disease.

KW - hamsters

KW - luminescence

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KW - leptospira interrogans

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Ozuru R, Saito M, Kanemaru T, Miyahara S, Villanueva SYAM, Murray GL et al. Adipose tissue is the first colonization site of Leptospira interrogans in subcutaneously infected hamsters. PLoS ONE. 2017 Feb 28;12(2). e0172973. https://doi.org/10.1371/journal.pone.0172973