Temperature Effects on Legionella pneumophila Killing by and Multiplication in Phagocytes of Guinea Pigs

Hiroshi Miyamoto, Midori Ogawa, Koji Maruta, Chiyuki Yamamoto, Hatsumi Taniguchi, Shin Ichi Yoshida, Yoshihiko Nikaido

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

We examined the effects of temperature on the interaction between Legionella pneumophila and phagocytes of guinea pigs. The body temperatures of guinea pigs infected with a sublethal dose (1.2 × 10 4 CFU) or a lethal dose (1.0 × 10 5 CFU) of L. pneumophila elevated from 38.4 ± 0.15 C to 40.2 ± 0.42 C or 40.3 ± 0.62 C, respectively. The intracellular bacterial killing by and bacterial proliferation in the phagocytes were examined at 33, 37, 40, and 42 C, using in vitro culture systems of peritoneal macrophages or polymorphonuclear leukocytes (PMN) of guinea pigs. In all the macrophages incubated at different temperatures, significant intracellular bacterial killings were observed at 4 hr after in vitro phagocytosis. After 24 hr of incubation, there was about a 100-fold increase of CFU and the number reached a maximum after 48 hr of incubation in the macrophages incubated at 42 C as well as 37 and 40 C, suggesting that macrophages support the intracellular bacterial growth in hyperthermia. In the PMN, L. pneumophila CFU 4 hr or 12 hr after the infection were significantly lower at 42 C than those at 37 C (P<0.05), indicating that the bactericidal capacity of PMN was enhanced at 42 C compared to 37 C. However, in all the PMN incubated at different temperatures, there were about 10-fold increases of CFU 24 hr after the infection, suggesting that PMN as well as macrophages support intracellular bacterial growth in hyperthermia. The extracellular bacterial growth was examined at 33,37, 40, and 42 C in buffered yeast extract (BYE) broth or RPMI 1640 medium containing 50% guinea pig serum as a permissive or non-permissive liquid medium for the bacterial growth, respectively. Inhibition of bacterial growth in BYE broth at 42 C, and a decrease of CFU in RPMI 1640 medium containing 50% guinea pig serum at 42 C were observed. In conclusion, hyperthermia may be beneficial by restricting extracellular bacterial survival, but it exerts no beneficial effect on the restriction of intracellular bacterial growth in phagocytes, though PMN showed enhanced initial killing at 42 C. These results suggest that fever, or hyperthermia itself, may not largely contribute as a nonspecific host defense early in the course of legionellosis.

Original languageEnglish
Pages (from-to)647-654
Number of pages8
JournalMICROBIOLOGY and IMMUNOLOGY
Volume39
Issue number9
DOIs
Publication statusPublished - Jan 1 1995
Externally publishedYes

Fingerprint

Legionella pneumophila
Phagocytes
Guinea Pigs
Neutrophils
Fever
Temperature
Growth
Macrophages
Yeasts
Legionellosis
Peritoneal Macrophages
Infection
Body Temperature
Serum
Phagocytosis

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Immunology
  • Virology

Cite this

Temperature Effects on Legionella pneumophila Killing by and Multiplication in Phagocytes of Guinea Pigs. / Miyamoto, Hiroshi; Ogawa, Midori; Maruta, Koji; Yamamoto, Chiyuki; Taniguchi, Hatsumi; Yoshida, Shin Ichi; Nikaido, Yoshihiko.

In: MICROBIOLOGY and IMMUNOLOGY, Vol. 39, No. 9, 01.01.1995, p. 647-654.

Research output: Contribution to journalArticle

Miyamoto, Hiroshi ; Ogawa, Midori ; Maruta, Koji ; Yamamoto, Chiyuki ; Taniguchi, Hatsumi ; Yoshida, Shin Ichi ; Nikaido, Yoshihiko. / Temperature Effects on Legionella pneumophila Killing by and Multiplication in Phagocytes of Guinea Pigs. In: MICROBIOLOGY and IMMUNOLOGY. 1995 ; Vol. 39, No. 9. pp. 647-654.
@article{0a8873e828fc4012b37cc2d2e43bb694,
title = "Temperature Effects on Legionella pneumophila Killing by and Multiplication in Phagocytes of Guinea Pigs",
abstract = "We examined the effects of temperature on the interaction between Legionella pneumophila and phagocytes of guinea pigs. The body temperatures of guinea pigs infected with a sublethal dose (1.2 × 10 4 CFU) or a lethal dose (1.0 × 10 5 CFU) of L. pneumophila elevated from 38.4 ± 0.15 C to 40.2 ± 0.42 C or 40.3 ± 0.62 C, respectively. The intracellular bacterial killing by and bacterial proliferation in the phagocytes were examined at 33, 37, 40, and 42 C, using in vitro culture systems of peritoneal macrophages or polymorphonuclear leukocytes (PMN) of guinea pigs. In all the macrophages incubated at different temperatures, significant intracellular bacterial killings were observed at 4 hr after in vitro phagocytosis. After 24 hr of incubation, there was about a 100-fold increase of CFU and the number reached a maximum after 48 hr of incubation in the macrophages incubated at 42 C as well as 37 and 40 C, suggesting that macrophages support the intracellular bacterial growth in hyperthermia. In the PMN, L. pneumophila CFU 4 hr or 12 hr after the infection were significantly lower at 42 C than those at 37 C (P<0.05), indicating that the bactericidal capacity of PMN was enhanced at 42 C compared to 37 C. However, in all the PMN incubated at different temperatures, there were about 10-fold increases of CFU 24 hr after the infection, suggesting that PMN as well as macrophages support intracellular bacterial growth in hyperthermia. The extracellular bacterial growth was examined at 33,37, 40, and 42 C in buffered yeast extract (BYE) broth or RPMI 1640 medium containing 50{\%} guinea pig serum as a permissive or non-permissive liquid medium for the bacterial growth, respectively. Inhibition of bacterial growth in BYE broth at 42 C, and a decrease of CFU in RPMI 1640 medium containing 50{\%} guinea pig serum at 42 C were observed. In conclusion, hyperthermia may be beneficial by restricting extracellular bacterial survival, but it exerts no beneficial effect on the restriction of intracellular bacterial growth in phagocytes, though PMN showed enhanced initial killing at 42 C. These results suggest that fever, or hyperthermia itself, may not largely contribute as a nonspecific host defense early in the course of legionellosis.",
author = "Hiroshi Miyamoto and Midori Ogawa and Koji Maruta and Chiyuki Yamamoto and Hatsumi Taniguchi and Yoshida, {Shin Ichi} and Yoshihiko Nikaido",
year = "1995",
month = "1",
day = "1",
doi = "10.1111/j.1348-0421.1995.tb03252.x",
language = "English",
volume = "39",
pages = "647--654",
journal = "Microbiology and Immunology",
issn = "0385-5600",
publisher = "Center for Academic Publications Japan",
number = "9",

}

TY - JOUR

T1 - Temperature Effects on Legionella pneumophila Killing by and Multiplication in Phagocytes of Guinea Pigs

AU - Miyamoto, Hiroshi

AU - Ogawa, Midori

AU - Maruta, Koji

AU - Yamamoto, Chiyuki

AU - Taniguchi, Hatsumi

AU - Yoshida, Shin Ichi

AU - Nikaido, Yoshihiko

PY - 1995/1/1

Y1 - 1995/1/1

N2 - We examined the effects of temperature on the interaction between Legionella pneumophila and phagocytes of guinea pigs. The body temperatures of guinea pigs infected with a sublethal dose (1.2 × 10 4 CFU) or a lethal dose (1.0 × 10 5 CFU) of L. pneumophila elevated from 38.4 ± 0.15 C to 40.2 ± 0.42 C or 40.3 ± 0.62 C, respectively. The intracellular bacterial killing by and bacterial proliferation in the phagocytes were examined at 33, 37, 40, and 42 C, using in vitro culture systems of peritoneal macrophages or polymorphonuclear leukocytes (PMN) of guinea pigs. In all the macrophages incubated at different temperatures, significant intracellular bacterial killings were observed at 4 hr after in vitro phagocytosis. After 24 hr of incubation, there was about a 100-fold increase of CFU and the number reached a maximum after 48 hr of incubation in the macrophages incubated at 42 C as well as 37 and 40 C, suggesting that macrophages support the intracellular bacterial growth in hyperthermia. In the PMN, L. pneumophila CFU 4 hr or 12 hr after the infection were significantly lower at 42 C than those at 37 C (P<0.05), indicating that the bactericidal capacity of PMN was enhanced at 42 C compared to 37 C. However, in all the PMN incubated at different temperatures, there were about 10-fold increases of CFU 24 hr after the infection, suggesting that PMN as well as macrophages support intracellular bacterial growth in hyperthermia. The extracellular bacterial growth was examined at 33,37, 40, and 42 C in buffered yeast extract (BYE) broth or RPMI 1640 medium containing 50% guinea pig serum as a permissive or non-permissive liquid medium for the bacterial growth, respectively. Inhibition of bacterial growth in BYE broth at 42 C, and a decrease of CFU in RPMI 1640 medium containing 50% guinea pig serum at 42 C were observed. In conclusion, hyperthermia may be beneficial by restricting extracellular bacterial survival, but it exerts no beneficial effect on the restriction of intracellular bacterial growth in phagocytes, though PMN showed enhanced initial killing at 42 C. These results suggest that fever, or hyperthermia itself, may not largely contribute as a nonspecific host defense early in the course of legionellosis.

AB - We examined the effects of temperature on the interaction between Legionella pneumophila and phagocytes of guinea pigs. The body temperatures of guinea pigs infected with a sublethal dose (1.2 × 10 4 CFU) or a lethal dose (1.0 × 10 5 CFU) of L. pneumophila elevated from 38.4 ± 0.15 C to 40.2 ± 0.42 C or 40.3 ± 0.62 C, respectively. The intracellular bacterial killing by and bacterial proliferation in the phagocytes were examined at 33, 37, 40, and 42 C, using in vitro culture systems of peritoneal macrophages or polymorphonuclear leukocytes (PMN) of guinea pigs. In all the macrophages incubated at different temperatures, significant intracellular bacterial killings were observed at 4 hr after in vitro phagocytosis. After 24 hr of incubation, there was about a 100-fold increase of CFU and the number reached a maximum after 48 hr of incubation in the macrophages incubated at 42 C as well as 37 and 40 C, suggesting that macrophages support the intracellular bacterial growth in hyperthermia. In the PMN, L. pneumophila CFU 4 hr or 12 hr after the infection were significantly lower at 42 C than those at 37 C (P<0.05), indicating that the bactericidal capacity of PMN was enhanced at 42 C compared to 37 C. However, in all the PMN incubated at different temperatures, there were about 10-fold increases of CFU 24 hr after the infection, suggesting that PMN as well as macrophages support intracellular bacterial growth in hyperthermia. The extracellular bacterial growth was examined at 33,37, 40, and 42 C in buffered yeast extract (BYE) broth or RPMI 1640 medium containing 50% guinea pig serum as a permissive or non-permissive liquid medium for the bacterial growth, respectively. Inhibition of bacterial growth in BYE broth at 42 C, and a decrease of CFU in RPMI 1640 medium containing 50% guinea pig serum at 42 C were observed. In conclusion, hyperthermia may be beneficial by restricting extracellular bacterial survival, but it exerts no beneficial effect on the restriction of intracellular bacterial growth in phagocytes, though PMN showed enhanced initial killing at 42 C. These results suggest that fever, or hyperthermia itself, may not largely contribute as a nonspecific host defense early in the course of legionellosis.

UR - http://www.scopus.com/inward/record.url?scp=0029094270&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0029094270&partnerID=8YFLogxK

U2 - 10.1111/j.1348-0421.1995.tb03252.x

DO - 10.1111/j.1348-0421.1995.tb03252.x

M3 - Article

C2 - 8577277

AN - SCOPUS:0029094270

VL - 39

SP - 647

EP - 654

JO - Microbiology and Immunology

JF - Microbiology and Immunology

SN - 0385-5600

IS - 9

ER -