Can oxygen tension contribute to an abnormal placental cytokine milieu?

Morgan R. Peltier, Ellen M. Gurzenda, Amitasrigowri Murthy, Kiranpreet Chawala, Veronica T. Lerner, Ishita Kharode, Yuko Arita, Adam Rhodes, Nisreen Maari, Andrew Moawad, Nazeeh Hanna

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

The aim of this study was to determine whether culturing human placental explants under different oxygen tensions will alter expression of pro- and anti-inflammatory mediators. Methods Placental explant cultures from second-trimester, elective, terminations-of-pregnancy were incubated under 21, 5, or 1% O 2 concentrations for 24hr in the presence or absence of IL-10. Cytokine concentrations in the conditioned medium were quantified by immunoassay. Results Culture of placental explants under 21, 5, or 1% O 2 concentrations produced hyperoxic (143±1.6mmHg), normoxic (37±1.6mmHg), and hypoxic (18.2±1.6mmHg) pO 2 levels for the maternal-fetal interface in the medium. Oxygen tension had profound effects on basal placental cytokine levels as well as on IL-10-stimulated cytokine production. IL-1β and TNF-α, but not IFN-γ production, was reduced by 21% O 2. Moreover, 21% O 2 levels increased the anti-inflammatory cytokines IL-10 and IL-13 while 1% O 2 tended to decrease the production of these cytokines. Conclusions Five percent- O 2 incubation more accurately represents in vivo pO 2 conditions at the maternal-fetal interface. Routine culture of placental explants in room air produces a superphysiologic oxygen tension that tended to increase the production of anti-inflammatory and decrease the production of pro-inflammatory cytokines. In addition, low pO 2 may reduce responsiveness of the placenta to the anti-inflammatory actions of IL-10.

Original languageEnglish (US)
Pages (from-to)279-285
Number of pages7
JournalAmerican Journal of Reproductive Immunology
Volume66
Issue number4
DOIs
StatePublished - Oct 1 2011
Externally publishedYes

Fingerprint

Cytokines
Oxygen
Interleukin-10
Anti-Inflammatory Agents
Mothers
Interleukin-13
Second Pregnancy Trimester
Conditioned Culture Medium
Interleukin-1
Immunoassay
Placenta
Air
Pregnancy

Keywords

  • Cytokine
  • Hyperoxia
  • Hypoxia
  • Inflammation
  • Oxygen tension
  • Placenta

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology
  • Reproductive Medicine
  • Obstetrics and Gynecology

Cite this

Can oxygen tension contribute to an abnormal placental cytokine milieu? / Peltier, Morgan R.; Gurzenda, Ellen M.; Murthy, Amitasrigowri; Chawala, Kiranpreet; Lerner, Veronica T.; Kharode, Ishita; Arita, Yuko; Rhodes, Adam; Maari, Nisreen; Moawad, Andrew; Hanna, Nazeeh.

In: American Journal of Reproductive Immunology, Vol. 66, No. 4, 01.10.2011, p. 279-285.

Research output: Contribution to journalArticle

Peltier, MR, Gurzenda, EM, Murthy, A, Chawala, K, Lerner, VT, Kharode, I, Arita, Y, Rhodes, A, Maari, N, Moawad, A & Hanna, N 2011, 'Can oxygen tension contribute to an abnormal placental cytokine milieu?', American Journal of Reproductive Immunology, vol. 66, no. 4, pp. 279-285. https://doi.org/10.1111/j.1600-0897.2011.00998.x
Peltier, Morgan R. ; Gurzenda, Ellen M. ; Murthy, Amitasrigowri ; Chawala, Kiranpreet ; Lerner, Veronica T. ; Kharode, Ishita ; Arita, Yuko ; Rhodes, Adam ; Maari, Nisreen ; Moawad, Andrew ; Hanna, Nazeeh. / Can oxygen tension contribute to an abnormal placental cytokine milieu?. In: American Journal of Reproductive Immunology. 2011 ; Vol. 66, No. 4. pp. 279-285.
@article{d7a6eac853ea47bfbc2fb9df29a60156,
title = "Can oxygen tension contribute to an abnormal placental cytokine milieu?",
abstract = "The aim of this study was to determine whether culturing human placental explants under different oxygen tensions will alter expression of pro- and anti-inflammatory mediators. Methods Placental explant cultures from second-trimester, elective, terminations-of-pregnancy were incubated under 21, 5, or 1{\%} O 2 concentrations for 24hr in the presence or absence of IL-10. Cytokine concentrations in the conditioned medium were quantified by immunoassay. Results Culture of placental explants under 21, 5, or 1{\%} O 2 concentrations produced hyperoxic (143±1.6mmHg), normoxic (37±1.6mmHg), and hypoxic (18.2±1.6mmHg) pO 2 levels for the maternal-fetal interface in the medium. Oxygen tension had profound effects on basal placental cytokine levels as well as on IL-10-stimulated cytokine production. IL-1β and TNF-α, but not IFN-γ production, was reduced by 21{\%} O 2. Moreover, 21{\%} O 2 levels increased the anti-inflammatory cytokines IL-10 and IL-13 while 1{\%} O 2 tended to decrease the production of these cytokines. Conclusions Five percent- O 2 incubation more accurately represents in vivo pO 2 conditions at the maternal-fetal interface. Routine culture of placental explants in room air produces a superphysiologic oxygen tension that tended to increase the production of anti-inflammatory and decrease the production of pro-inflammatory cytokines. In addition, low pO 2 may reduce responsiveness of the placenta to the anti-inflammatory actions of IL-10.",
keywords = "Cytokine, Hyperoxia, Hypoxia, Inflammation, Oxygen tension, Placenta",
author = "Peltier, {Morgan R.} and Gurzenda, {Ellen M.} and Amitasrigowri Murthy and Kiranpreet Chawala and Lerner, {Veronica T.} and Ishita Kharode and Yuko Arita and Adam Rhodes and Nisreen Maari and Andrew Moawad and Nazeeh Hanna",
year = "2011",
month = "10",
day = "1",
doi = "10.1111/j.1600-0897.2011.00998.x",
language = "English (US)",
volume = "66",
pages = "279--285",
journal = "American Journal of Reproductive Immunology and Microbiology",
issn = "1046-7408",
publisher = "Wiley-Blackwell",
number = "4",

}

TY - JOUR

T1 - Can oxygen tension contribute to an abnormal placental cytokine milieu?

AU - Peltier, Morgan R.

AU - Gurzenda, Ellen M.

AU - Murthy, Amitasrigowri

AU - Chawala, Kiranpreet

AU - Lerner, Veronica T.

AU - Kharode, Ishita

AU - Arita, Yuko

AU - Rhodes, Adam

AU - Maari, Nisreen

AU - Moawad, Andrew

AU - Hanna, Nazeeh

PY - 2011/10/1

Y1 - 2011/10/1

N2 - The aim of this study was to determine whether culturing human placental explants under different oxygen tensions will alter expression of pro- and anti-inflammatory mediators. Methods Placental explant cultures from second-trimester, elective, terminations-of-pregnancy were incubated under 21, 5, or 1% O 2 concentrations for 24hr in the presence or absence of IL-10. Cytokine concentrations in the conditioned medium were quantified by immunoassay. Results Culture of placental explants under 21, 5, or 1% O 2 concentrations produced hyperoxic (143±1.6mmHg), normoxic (37±1.6mmHg), and hypoxic (18.2±1.6mmHg) pO 2 levels for the maternal-fetal interface in the medium. Oxygen tension had profound effects on basal placental cytokine levels as well as on IL-10-stimulated cytokine production. IL-1β and TNF-α, but not IFN-γ production, was reduced by 21% O 2. Moreover, 21% O 2 levels increased the anti-inflammatory cytokines IL-10 and IL-13 while 1% O 2 tended to decrease the production of these cytokines. Conclusions Five percent- O 2 incubation more accurately represents in vivo pO 2 conditions at the maternal-fetal interface. Routine culture of placental explants in room air produces a superphysiologic oxygen tension that tended to increase the production of anti-inflammatory and decrease the production of pro-inflammatory cytokines. In addition, low pO 2 may reduce responsiveness of the placenta to the anti-inflammatory actions of IL-10.

AB - The aim of this study was to determine whether culturing human placental explants under different oxygen tensions will alter expression of pro- and anti-inflammatory mediators. Methods Placental explant cultures from second-trimester, elective, terminations-of-pregnancy were incubated under 21, 5, or 1% O 2 concentrations for 24hr in the presence or absence of IL-10. Cytokine concentrations in the conditioned medium were quantified by immunoassay. Results Culture of placental explants under 21, 5, or 1% O 2 concentrations produced hyperoxic (143±1.6mmHg), normoxic (37±1.6mmHg), and hypoxic (18.2±1.6mmHg) pO 2 levels for the maternal-fetal interface in the medium. Oxygen tension had profound effects on basal placental cytokine levels as well as on IL-10-stimulated cytokine production. IL-1β and TNF-α, but not IFN-γ production, was reduced by 21% O 2. Moreover, 21% O 2 levels increased the anti-inflammatory cytokines IL-10 and IL-13 while 1% O 2 tended to decrease the production of these cytokines. Conclusions Five percent- O 2 incubation more accurately represents in vivo pO 2 conditions at the maternal-fetal interface. Routine culture of placental explants in room air produces a superphysiologic oxygen tension that tended to increase the production of anti-inflammatory and decrease the production of pro-inflammatory cytokines. In addition, low pO 2 may reduce responsiveness of the placenta to the anti-inflammatory actions of IL-10.

KW - Cytokine

KW - Hyperoxia

KW - Hypoxia

KW - Inflammation

KW - Oxygen tension

KW - Placenta

UR - http://www.scopus.com/inward/record.url?scp=80052562487&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=80052562487&partnerID=8YFLogxK

U2 - 10.1111/j.1600-0897.2011.00998.x

DO - 10.1111/j.1600-0897.2011.00998.x

M3 - Article

VL - 66

SP - 279

EP - 285

JO - American Journal of Reproductive Immunology and Microbiology

JF - American Journal of Reproductive Immunology and Microbiology

SN - 1046-7408

IS - 4

ER -