Maternal smoke exposure impairs the long-term fertility of female offspring in a murine model

Nicole J. Camlin, Alexander P. Sobinoff, Jessie M. Sutherland, Emma L. Beckett, Andrew G. Jarnicki, Rebecca L. Vanders, Philip M. Hansbro, Eileen A. McLaughlin, Janet E. Holt

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

The theory of fetal origins of adult disease was first proposed in 1989, and in the decades since, a wide range of other diseases from obesity to asthma have been found to originate in early development. Because mammalian oocyte development begins in fetal life it has been suggested that environmental and lifestyle factors of the mother could directly impact the fertility of subsequent generations. Cigarette smoke is a known ovotoxicant in active smokers, yet disturbingly 13% of Australian and 12% of US women continue to smoke throughout pregnancy. The focus of our investigation was to characterize the adverse effects of smoking on ovary and oocyte quality in female offspring exposed in utero. Pregnant mice were nasally exposed to cigarette smoke for 12 wk throughout pregnancy/lactation, and ovary and oocyte quality of the F1 (maternal smoke exposed) generation was examined. Neonatal ovaries displayed abnormal somatic cell proliferation and increased apoptosis, leading to a reduction in follicle numbers. Further investigation found that altered somatic cell proliferation and reduced follicle number continued into adulthood; however, apoptosis did not. This reduction in follicles resulted in decreased oocyte numbers, with these oocytes found to have elevated levels of oxidative stress, altered metaphase II spindle, and reduced sperm-egg interaction. These ovarian and oocyte changes ultimately lead to subfertility, with maternal smoke-exposed animals having smaller litters and also taking longer to conceive. In conclusion, our results demonstrate that in utero and lactational exposure to cigarette smoke can have long-lasting effects on the fertility of the next generation of females.

Original languageEnglish
Article number39
Pages (from-to)1-12
Number of pages12
JournalBiology of Reproduction
Volume94
Issue number2
DOIs
Publication statusPublished - 1 Feb 2016
Externally publishedYes

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Maternal Exposure
Smoke
Oocytes
Fertility
Tobacco Products
Ovary
Mothers
Cell Proliferation
Apoptosis
Sperm-Ovum Interactions
Pregnancy
Metaphase
Lactation
Infertility
Life Style
Oxidative Stress
Asthma
Obesity
Smoking

Cite this

Camlin, N. J., Sobinoff, A. P., Sutherland, J. M., Beckett, E. L., Jarnicki, A. G., Vanders, R. L., ... Holt, J. E. (2016). Maternal smoke exposure impairs the long-term fertility of female offspring in a murine model. Biology of Reproduction, 94(2), 1-12. [39]. https://doi.org/10.1095/biolreprod.115.135848
Camlin, Nicole J. ; Sobinoff, Alexander P. ; Sutherland, Jessie M. ; Beckett, Emma L. ; Jarnicki, Andrew G. ; Vanders, Rebecca L. ; Hansbro, Philip M. ; McLaughlin, Eileen A. ; Holt, Janet E. / Maternal smoke exposure impairs the long-term fertility of female offspring in a murine model. In: Biology of Reproduction. 2016 ; Vol. 94, No. 2. pp. 1-12.
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Camlin, NJ, Sobinoff, AP, Sutherland, JM, Beckett, EL, Jarnicki, AG, Vanders, RL, Hansbro, PM, McLaughlin, EA & Holt, JE 2016, 'Maternal smoke exposure impairs the long-term fertility of female offspring in a murine model', Biology of Reproduction, vol. 94, no. 2, 39, pp. 1-12. https://doi.org/10.1095/biolreprod.115.135848

Maternal smoke exposure impairs the long-term fertility of female offspring in a murine model. / Camlin, Nicole J.; Sobinoff, Alexander P.; Sutherland, Jessie M.; Beckett, Emma L.; Jarnicki, Andrew G.; Vanders, Rebecca L.; Hansbro, Philip M.; McLaughlin, Eileen A.; Holt, Janet E.

In: Biology of Reproduction, Vol. 94, No. 2, 39, 01.02.2016, p. 1-12.

Research output: Contribution to journalArticle

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AU - Sutherland, Jessie M.

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AU - Jarnicki, Andrew G.

AU - Vanders, Rebecca L.

AU - Hansbro, Philip M.

AU - McLaughlin, Eileen A.

AU - Holt, Janet E.

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Camlin NJ, Sobinoff AP, Sutherland JM, Beckett EL, Jarnicki AG, Vanders RL et al. Maternal smoke exposure impairs the long-term fertility of female offspring in a murine model. Biology of Reproduction. 2016 Feb 1;94(2):1-12. 39. https://doi.org/10.1095/biolreprod.115.135848