Streptococcus pneumoniae-induced pneumonia and citrobacter rodentium-induced gut infection differentially alter vitamin A concentrations in the lung and liver of mice

Katherine H. Restori, Kaitlin L. McDaniel, Amanda E. Wray, Margherita Teresa-Anna Cantorna, A. Catharine Ross

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Abstract

In the developing world, vitamin A (VA) deficiency is endemic in populations that are also at great risk of morbidity and mortality because of pneumococcal pneumonia and enteric infections. To better understand how lung and gastrointestinal pathogens affect VA status, we assessed VA concentrations in serum, lung, and liver during an invasive pneumonia infection induced by Streptococcus pneumoniae serotype 3, and a noninvasive gut infection induced by Citrobacter rodentium, in vitamin A-adequate (VAA) and vitamin A-deficient (VAD) mice. For pneumonia infection, mice were immunized with pneumococcal polysaccharide serotype 3 (PPS3), or not (infected-control), 5 d prior to intranasal inoculation with S. pneumoniae. Two days post-inoculation, immunization was protective against systemic infection regardless of VA status as PPS3 immunization decreased bacteremia compared with infected-control mice (P < 0.05). Retinol concentrations in the lung were higher in infected-control VAAmice (15.7 nmol/g: P < 0.05) compared with PPS3-immunizedmice (8.23 nmol/g), but this was not associated with increased lung bacterial burden. VAA mice had reduced severity of C. rodentium-induced gut infection as measured by fecal bacterial shedding compared with VAD mice (P < 0.05). Liver retinol and retinyl ester concentrations in VAA mice decreased at the peak of infection (retinol, 8.1 nmol/g; retinyl esters, 985 nmol/g; P < 0.05, compared with uninfectedmice; retinol, 29.5 nmol/g; retinyl esters, 1730 nmol/g), whereas tissue VA concentrations were low in VAD mice during both infections. Colonic mucin gene expression was also depressed at peak infection compared with uninfected mice (P < 0.05). Overall, pneumonia had less effect on VA status than gastrointestinal infection, predominantly owing to reduced hepatic VA storage at the peak of gut infection.

Original languageEnglish (US)
Pages (from-to)392-398
Number of pages7
JournalJournal of Nutrition
Volume144
Issue number3
DOIs
StatePublished - Mar 1 2014

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Citrobacter rodentium
Streptococcus pneumoniae
Vitamin A
Pneumonia
Lung
Liver
Infection
Polysaccharides
Pneumococcal Infections
Esters
Bacterial Shedding
Immunization
Pneumococcal Pneumonia

All Science Journal Classification (ASJC) codes

  • Medicine (miscellaneous)
  • Nutrition and Dietetics

Cite this

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title = "Streptococcus pneumoniae-induced pneumonia and citrobacter rodentium-induced gut infection differentially alter vitamin A concentrations in the lung and liver of mice",
abstract = "In the developing world, vitamin A (VA) deficiency is endemic in populations that are also at great risk of morbidity and mortality because of pneumococcal pneumonia and enteric infections. To better understand how lung and gastrointestinal pathogens affect VA status, we assessed VA concentrations in serum, lung, and liver during an invasive pneumonia infection induced by Streptococcus pneumoniae serotype 3, and a noninvasive gut infection induced by Citrobacter rodentium, in vitamin A-adequate (VAA) and vitamin A-deficient (VAD) mice. For pneumonia infection, mice were immunized with pneumococcal polysaccharide serotype 3 (PPS3), or not (infected-control), 5 d prior to intranasal inoculation with S. pneumoniae. Two days post-inoculation, immunization was protective against systemic infection regardless of VA status as PPS3 immunization decreased bacteremia compared with infected-control mice (P < 0.05). Retinol concentrations in the lung were higher in infected-control VAAmice (15.7 nmol/g: P < 0.05) compared with PPS3-immunizedmice (8.23 nmol/g), but this was not associated with increased lung bacterial burden. VAA mice had reduced severity of C. rodentium-induced gut infection as measured by fecal bacterial shedding compared with VAD mice (P < 0.05). Liver retinol and retinyl ester concentrations in VAA mice decreased at the peak of infection (retinol, 8.1 nmol/g; retinyl esters, 985 nmol/g; P < 0.05, compared with uninfectedmice; retinol, 29.5 nmol/g; retinyl esters, 1730 nmol/g), whereas tissue VA concentrations were low in VAD mice during both infections. Colonic mucin gene expression was also depressed at peak infection compared with uninfected mice (P < 0.05). Overall, pneumonia had less effect on VA status than gastrointestinal infection, predominantly owing to reduced hepatic VA storage at the peak of gut infection.",
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Streptococcus pneumoniae-induced pneumonia and citrobacter rodentium-induced gut infection differentially alter vitamin A concentrations in the lung and liver of mice. / Restori, Katherine H.; McDaniel, Kaitlin L.; Wray, Amanda E.; Cantorna, Margherita Teresa-Anna; Ross, A. Catharine.

In: Journal of Nutrition, Vol. 144, No. 3, 01.03.2014, p. 392-398.

Research output: Contribution to journalArticle

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N2 - In the developing world, vitamin A (VA) deficiency is endemic in populations that are also at great risk of morbidity and mortality because of pneumococcal pneumonia and enteric infections. To better understand how lung and gastrointestinal pathogens affect VA status, we assessed VA concentrations in serum, lung, and liver during an invasive pneumonia infection induced by Streptococcus pneumoniae serotype 3, and a noninvasive gut infection induced by Citrobacter rodentium, in vitamin A-adequate (VAA) and vitamin A-deficient (VAD) mice. For pneumonia infection, mice were immunized with pneumococcal polysaccharide serotype 3 (PPS3), or not (infected-control), 5 d prior to intranasal inoculation with S. pneumoniae. Two days post-inoculation, immunization was protective against systemic infection regardless of VA status as PPS3 immunization decreased bacteremia compared with infected-control mice (P < 0.05). Retinol concentrations in the lung were higher in infected-control VAAmice (15.7 nmol/g: P < 0.05) compared with PPS3-immunizedmice (8.23 nmol/g), but this was not associated with increased lung bacterial burden. VAA mice had reduced severity of C. rodentium-induced gut infection as measured by fecal bacterial shedding compared with VAD mice (P < 0.05). Liver retinol and retinyl ester concentrations in VAA mice decreased at the peak of infection (retinol, 8.1 nmol/g; retinyl esters, 985 nmol/g; P < 0.05, compared with uninfectedmice; retinol, 29.5 nmol/g; retinyl esters, 1730 nmol/g), whereas tissue VA concentrations were low in VAD mice during both infections. Colonic mucin gene expression was also depressed at peak infection compared with uninfected mice (P < 0.05). Overall, pneumonia had less effect on VA status than gastrointestinal infection, predominantly owing to reduced hepatic VA storage at the peak of gut infection.

AB - In the developing world, vitamin A (VA) deficiency is endemic in populations that are also at great risk of morbidity and mortality because of pneumococcal pneumonia and enteric infections. To better understand how lung and gastrointestinal pathogens affect VA status, we assessed VA concentrations in serum, lung, and liver during an invasive pneumonia infection induced by Streptococcus pneumoniae serotype 3, and a noninvasive gut infection induced by Citrobacter rodentium, in vitamin A-adequate (VAA) and vitamin A-deficient (VAD) mice. For pneumonia infection, mice were immunized with pneumococcal polysaccharide serotype 3 (PPS3), or not (infected-control), 5 d prior to intranasal inoculation with S. pneumoniae. Two days post-inoculation, immunization was protective against systemic infection regardless of VA status as PPS3 immunization decreased bacteremia compared with infected-control mice (P < 0.05). Retinol concentrations in the lung were higher in infected-control VAAmice (15.7 nmol/g: P < 0.05) compared with PPS3-immunizedmice (8.23 nmol/g), but this was not associated with increased lung bacterial burden. VAA mice had reduced severity of C. rodentium-induced gut infection as measured by fecal bacterial shedding compared with VAD mice (P < 0.05). Liver retinol and retinyl ester concentrations in VAA mice decreased at the peak of infection (retinol, 8.1 nmol/g; retinyl esters, 985 nmol/g; P < 0.05, compared with uninfectedmice; retinol, 29.5 nmol/g; retinyl esters, 1730 nmol/g), whereas tissue VA concentrations were low in VAD mice during both infections. Colonic mucin gene expression was also depressed at peak infection compared with uninfected mice (P < 0.05). Overall, pneumonia had less effect on VA status than gastrointestinal infection, predominantly owing to reduced hepatic VA storage at the peak of gut infection.

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