Structural changes, increased hypoxia, and oxidative DNA damage in placenta due to maternal smokeless tobacco use.
hypoxia
oxidative DNA damage
placental structure
smokeless tobacco
Journal
Birth defects research
ISSN: 2472-1727
Titre abrégé: Birth Defects Res
Pays: United States
ID NLM: 101701004
Informations de publication
Date de publication:
01 10 2021
01 10 2021
Historique:
revised:
08
06
2021
received:
20
09
2020
accepted:
27
06
2021
pubmed:
22
7
2021
medline:
3
11
2021
entrez:
21
7
2021
Statut:
ppublish
Résumé
Smokeless tobacco (SLT) consumption during pregnancy is a well-recognized health risk that causes placental damage including hypoxia and oxidative damage. Although consumption of SLT by women varies from region to region, majority of tea leave pluckers consume SLT for relieving stress and pain. Still, the effects of SLT consumption have not been evaluated in tea garden workers (TGW). While previous studies have attempted to report effects of cigarette smoke using in vitro model, hypoxia-inducible factor (HIF)-1α expression in human placentae from pregnant women exposed to SLT has not been previously studied. This study was aimed to explore the effects of SLT consumption on placental structure, expression of HIF-1α and oxidative DNA damage in sample population of TGW. A total of 51 placentae were collected from SLT users and nonusers (n = 30 and 21, respectively) with full-term normal delivery, who were involved in the plucking of tea leaves during pregnancy in tea plantation. Low birth weight (LBW, i.e., weight <2,500 g) and normal birth weight (NBW) groups among both SLT user and nonuser were compared for the stated parameters. Placental tissues were processed for transmission electron microscopy (TEM) study and immunohistochemical analysis for the expression of HIF-1α and 8-hydroxy-2'-deoxyguanosine (8-OHdG). Altered ultrastructural characteristics were observed in the tertiary villi of LBW group among SLT users which included endothelial cells protrusion into capillary lumen, degenerated nuclei, significant thickening of trophoblast basement membrane and vasculo-syncytial membrane, abnormalities of the microvilli, swollen or damaged mitochondria, and dilatation in endoplasmic reticulum cisternae. Furthermore, significant reduction in the perimeter, area, and number of the stromal capillary of the tertiary villi of placenta were found in LBW group as compared with NBW group from the SLT users. Enhanced expression for HIF-1α and oxidative DNA damage (8-OHdG) biomarker was observed in SLT users as compared with nonusers. Maternal SLT exposure during pregnancy may be associated with villus hypoxia and consequently oxidative DNA damage. It is presumed that deleterious effect of SLT exposure on placenta could result in impairment of placental barrier, and restrict nutrient and oxygen supply from mother to fetus, and thus could be a cause of fetal growth restriction.
Sections du résumé
BACKGROUND
Smokeless tobacco (SLT) consumption during pregnancy is a well-recognized health risk that causes placental damage including hypoxia and oxidative damage. Although consumption of SLT by women varies from region to region, majority of tea leave pluckers consume SLT for relieving stress and pain. Still, the effects of SLT consumption have not been evaluated in tea garden workers (TGW). While previous studies have attempted to report effects of cigarette smoke using in vitro model, hypoxia-inducible factor (HIF)-1α expression in human placentae from pregnant women exposed to SLT has not been previously studied. This study was aimed to explore the effects of SLT consumption on placental structure, expression of HIF-1α and oxidative DNA damage in sample population of TGW.
METHODS
A total of 51 placentae were collected from SLT users and nonusers (n = 30 and 21, respectively) with full-term normal delivery, who were involved in the plucking of tea leaves during pregnancy in tea plantation. Low birth weight (LBW, i.e., weight <2,500 g) and normal birth weight (NBW) groups among both SLT user and nonuser were compared for the stated parameters. Placental tissues were processed for transmission electron microscopy (TEM) study and immunohistochemical analysis for the expression of HIF-1α and 8-hydroxy-2'-deoxyguanosine (8-OHdG).
RESULTS
Altered ultrastructural characteristics were observed in the tertiary villi of LBW group among SLT users which included endothelial cells protrusion into capillary lumen, degenerated nuclei, significant thickening of trophoblast basement membrane and vasculo-syncytial membrane, abnormalities of the microvilli, swollen or damaged mitochondria, and dilatation in endoplasmic reticulum cisternae. Furthermore, significant reduction in the perimeter, area, and number of the stromal capillary of the tertiary villi of placenta were found in LBW group as compared with NBW group from the SLT users. Enhanced expression for HIF-1α and oxidative DNA damage (8-OHdG) biomarker was observed in SLT users as compared with nonusers.
CONCLUSIONS
Maternal SLT exposure during pregnancy may be associated with villus hypoxia and consequently oxidative DNA damage. It is presumed that deleterious effect of SLT exposure on placenta could result in impairment of placental barrier, and restrict nutrient and oxygen supply from mother to fetus, and thus could be a cause of fetal growth restriction.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1198-1214Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Adibi, J. J., Whyatt, R. M., Hauser, R., Bhat, H. K., Davis, B. J., Calafat, A. M., … Williams, P. L. (2010). Transcriptional biomarkers of steroidogenesis and trophoblast differentiation in the placenta in relation to prenatal phthalate exposure. Environmental Health Perspectives, 118(2), 291-296. https://doi.org/10.1289/ehp.0900788
Ali, L. E., Salih, M. M., Elhassan, E. M., Mohmmed, A. A., & Adam, I. (2019). Placental growth factor, vascular endothelial growth factor, and hypoxia-inducible factor-1α in the placentas of women with pre-eclampsia. The Journal of Maternal-Fetal & Neonatal Medicine, 32(16), 2628-2632. https://doi.org/10.1080/14767058.2018.1443066
Ananth, C. V., Savitz, D. A., & Luther, E. R. (1996). Maternal cigarette smoking as a risk factor for placental abruption, placenta previa, and uterine bleeding in pregnancy. American Journal of Epidemiology, 144(9), 881-889. https://doi.org/10.1093/oxfordjournals.aje.a009022
Ansari, T., Fenlon, S., Pasha, S., O'neill, B., Gillan, J. E., Green, C. J., & Sibbons, P. D. (2003). Morphometric assessment of the oxygen diffusion conductance in placentae from pregnancies complicated by intra-uterine growth restriction. Placenta, 24(6), 618-626.
Aruoma, O. I., Halliwell, B., Gajewski, E., & Dizdaroglu, M. (1989). Damage to the bases in DNA induced by hydrogen peroxide and ferric ion chelates. Journal of Biological Chemistry, 264(34), 20509-20512.
Asmussen, I. (1980). Ultrastructure of the villi and fetal capillaries in placentas from smoking and nonsmoking mothers. British Journal of Obstetrics and Gynaecology, 87(3), 239-245. https://doi.org/10.1111/j.1471-0528.1980.tb04527.x
Bastia, B., Kumar, K., Kumar, S. N., Behera, N. R., & Jain, A. K. (2017). Expression of endothelin-1 in human placenta of active smokers: An immunohistochemical study. International Journal of Research Studies in Biosciences (IJRSB), 5(12), 34-40.
Benirschke, K., & Kaufmann, P. (1995). Anatomy and pathology of the placental membranes. In K. Benirschke (Ed.), Pathology of the human placenta (pp. 268-318). Berlin: Springer.
Boyd, J. D., & Hamilton, W. J. (1970). The human placenta (Vol. 212). Cambridge: Heffer.
Burton, G. J., & Tham, S. W. (1992). Formation of vasculo-syncytial membranes in the human placenta. Journal of Developmental Physiology, 18(1), 43-47.
Burton, G. J., Yung, H. W., Cindrova-Davies, T., & Charnock-Jones, D. S. (2009). Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta, 30, S43-S48. https://doi.org/10.1016/j.placenta.2008.11.003
Cantle, S. J., Kaufmann, P., Luckhardt, M., & Schweikhart, G. (1987). Interpretation of syncytial sprouts and bridges in the human placenta. Placenta, 8(3), 221-234.
Daijo, H., Hoshino, Y., Kai, S., Suzuki, K., Nishi, K., Matsuo, Y., … Hirota, K. (2016). Cigarette smoke reversibly activates hypoxia-inducible factor 1 in a reactive oxygen species-dependent manner. Scientific Reports, 6, 34424-34424. https://doi.org/10.1038/srep34424
Demir, R., Demir, A. Y., & Yinanc, M. (1994). Structural changes in placental barrier of smoking mother a quantitative and ulstrastructural study. Pathology-Research and Practice, 190(7), 656-667.
Ebina, S., Chiba, T., Ozaki, T., & Kashiwakura, I. (2012). Relationship between 8-hydroxydeoxyguanosine levels in placental/umbilical cord blood and maternal/neonatal obstetric factors. Experimental and Therapeutic Medicine, 4(3), 387-390. https://doi.org/10.3892/etm.2012.617
England, L. J., Kim, S. Y., Tomar, S. L., Ray, C. S., Gupta, P. C., Eissenberg, T., … Tolosa, J. E. (2010). Non-cigarette tobacco use among women and adverse pregnancy outcomes. Acta Obstetricia et Gynecologica Scandinavica, 89(4), 454-464. https://doi.org/10.3109/00016341003605719
Gabory, A., Roseboom, T. J., Moore, T., Moore, L. G., & Junien, C. (2013). Placental contribution to the origins of sexual dimorphism in health and diseases: Sex chromosomes and epigenetics. Biology of Sex Differences, 4(1), 5. https://doi.org/10.1186/2042-6410-4-5
Görlach, A. (2009). Regulation of HIF-1alpha at the transcriptional level. Current Pharmaceutical Design, 15(33), 3844-3852. https://doi.org/10.2174/138161209789649420
Heazell, A. E., Moll, S. J., Jones, C. J., Baker, P. N., & Crocker, I. P. (2007). Formation of syncytial knots is increased by hyperoxia, hypoxia and reactive oxygen species. Placenta, 28, S33-S40. https://doi.org/10.1016/j.placenta.2006.10.007
Herrera, E. A., Krause, B., Ebensperger, G., Reyes, R. V., Casanello, P., Parra-Cordero, M., & Llanos, A. J. (2014). The placental pursuit for an adequate oxidant balance between the mother and the fetus. Frontiers in Pharmacology, 5, 149.
Hung, T.-H., Chen, S.-F., Liou, J.-D., Hsu, J.-J., Li, M.-J., Yeh, Y.-L., & Hsieh, T.-T. (2008). Bax, Bak and mitochondrial oxidants are involved in hypoxia-reoxygenation-induced apoptosis in human placenta. Placenta, 29(7), 565-583.
Huppertz, B., & Kadyrov, M. (2006). Apoptosis and its role in the trophoblast. American Journal of Obstetrics & Gynecology, 195(1), 29-39.
Hutter, D., Kingdom, J., & Jaeggi, E. (2010). Causes and mechanisms of intrauterine hypoxia and its impact on the fetal cardiovascular system: A review. International Journal of Pediatrics, 2010, 401323. https://doi.org/10.1155/2010/401323
Ion, R., & Bernal, A. L. (2015). Smoking and preterm birth. Reproductive Sciences, 22(8), 918-926. https://doi.org/10.1177/1933719114556486
Jauniaux, E., & Burton, G. J. (2007). Morphological and biological effects of maternal exposure to tobacco smoke on the feto-placental unit. Early Human Development, 83(11), 699-706. https://doi.org/10.1016/j.earlhumdev.2007.07.016
Kawashima, A., Koide, K., Ventura, W., Hori, K., Takenaka, S., Maruyama, D., … Sekizawa, A. (2014). Effects of maternal smoking on the placental expression of genes related to angiogenesis and apoptosis during the first trimester. PLoS One, 9(8), e106140. https://doi.org/10.1371/journal.pone.0106140
Kelehan, P., & Downey, P. (2019). Villous oedema. In T. Y. Khong, E. Mooney, P. G. J. Nikkels, T. K. Morgan, & S. J. Gordijn (Eds.), Pathology of the placenta (pp. 153-155). Berlin: Springer.
Kida, N., Matsuo, Y., Hashimoto, Y., Nishi, K., Tsuzuki-Nakao, T., Bono, H., … Okada, H. (2021). Cigarette smoke extract activates hypoxia-inducible factors in a reactive oxygen species-dependent manner in stroma cells from human endometrium. Antioxidants (Basel), 10(1), 48-64. https://doi.org/10.3390/antiox10010048
Kimura, C., Watanabe, K., Iwasaki, A., Mori, T., Matsushita, H., Shinohara, K., & Wakatsuki, A. (2013). The severity of hypoxic changes and oxidative DNA damage in the placenta of early-onset preeclamptic women and fetal growth restriction. The Journal of Maternal-Fetal & Neonatal Medicine, 26(5), 491-496. https://doi.org/10.3109/14767058.2012.733766
Kingdom, J. C., & Kaufmann, P. (1997). Oxygen and placental villous development: Origins of fetal hypoxia. Placenta, 18(8), 613-621.
Krishna, K. (1978). Tobacco chewing in pregnancy. British Journal of Obstetrics and Gynaecology, 85(10), 726-728.
Langston, C., Kaplan, C., Macpherson, T., Manci, E., Peevy, K., Clark, B., … Glenn, G. (1997). Practice guideline for examination of the placenta: Developed by the Placental Pathology Practice Guideline Development Task Force of the College of American Pathologists. Archives of Pathology & Laboratory Medicine, 121(5), 449-476.
Longtine, M. S., & Nelson, D. M. (2011). Placental dysfunction and fetal programming: The importance of placental size, shape, histopathology, and molecular composition. Seminars in Reproductive Medicine, 29(3), 187-196. https://doi.org/10.1055/s-0031-1275515
Mayhew, T. M. (1998). Thinning of the intervascular tissue layers of the human placenta is an adaptive response to passive diffusion in vivo and may help to predict the origins of fetal hypoxia. European Journal of Obstetrics, Gynecology, and Reproductive Biology, 81(1), 101-109.
Mayhew, T. M., Manwani, R., Ohadike, C., Wijesekara, J., & Baker, P. N. (2007). The placenta in pre-eclampsia and intrauterine growth restriction: Studies on exchange surface areas, diffusion distances and villous membrane diffusive conductances. Placenta, 28(2-3), 233-238. https://doi.org/10.1016/j.placenta.2006.02.011
Medhi, G. K., Hazarika, N. C., & Mahanta, J. (2006). Correlates of alcohol consumption and tobacco use among tea industry workers of Assam. Substance Use & Misuse, 41(5), 691-706. https://doi.org/10.1080/10826080500411429
Meng, Q., Shao, L., Luo, X., Mu, Y., Xu, W., Gao, C., … Cui, Y. (2015). Ultrastructure of placenta of gravidas with gestational diabetes mellitus. Obstetrics and Gynecology International, 2015, 283124. https://doi.org/10.1155/2015/283124
National Cancer Institute. (2003). Smokeless tobacco & cancer: Q & A. Retrieved from https://www.cancer.gov/about-cancer/causes-prevention/risk/tobacco/smokeless-fact-sheet
Palaiologou, E., Etter, O., Goggin, P., Chatelet, D. S., Johnston, D. A., Lofthouse, E. M., … Lewis, R. M. (2020). Human placental villi contain stromal macrovesicles associated with networks of stellate cells. Journal of Anatomy, 236(1), 132-141. https://doi.org/10.1111/joa.13082
Pastrakuljic, A., Derewlany, L. O., & Koren, G. (1999). Maternal cocaine use and cigarette smoking in pregnancy in relation to amino acid transport and fetal growth. Placenta, 20(7), 499-512. https://doi.org/10.1053/plac.1999.0418
Patel, J., Landers, K., Mortimer, R. H., & Richard, K. (2010). Regulation of hypoxia inducible factors (HIF) in hypoxia and normoxia during placental development. Placenta, 31(11), 951-957.
Pratinidhi, A., Gandham, S., Shrotri, A., Patil, A., & Pardeshi, S. (2010). Use of 'mishri'a smokeless form of tobacco during pregnancy and its perinatal outcome. Indian Journal of Community Medicine, 35(1), 14.
Proud, C. G. (2007). Signalling to translation: How signal transduction pathways control the protein synthetic machinery. Biochemical Journal, 403(2), 217-234.
Rath, G., Aggarwal, R., Jawanjal, P., Tripathi, R., & Batra, A. (2016). HIF-1 alpha and placental growth factor in pregnancies complicated with preeclampsia: A qualitative and quantitative analysis. Journal of Clinical Laboratory Analysis, 30(1), 75-83. https://doi.org/10.1002/jcla.21819
Rath, G., Dhuria, R., Salhan, S., & Jain, A. K. (2011). Morphology and morphometric analysis of stromal capillaries in full term human placental villi of smoking mothers: An electron microscopic study. La Clinica Terapeutica, 162(4), 301-305.
Robbins, J. R., Skrzypczynska, K. M., Zeldovich, V. B., Kapidzic, M., & Bakardjiev, A. I. (2010). Placental syncytiotrophoblast constitutes a major barrier to vertical transmission of Listeria monocytogenes. PLoS Pathogens, 6(1), e1000732. https://doi.org/10.1371/journal.ppat.1000732
Rosenfeld, C. S. (2015). Sex-specific placental responses in fetal development. Endocrinology, 156(10), 3422-3434. https://doi.org/10.1210/en.2015-1227
Salgado, S. S., & Salgado, M. K. R. (2011). Structural changes in pre-eclamptic and eclamptic placentas: an ultrastructural study. Journal of the College of Physicians and Surgeons-Pakistan, 21(8), 482-486.
Saxena, P., Pradhan, D., Verma, R., Kumar, S. N., Deval, R., & A, K. J. (2018). Up-regulation of fibroblast growth factor receptor 1 due to prenatal tobacco exposure can lead to developmental defects in new born. The Journal of Maternal-Fetal & Neonatal Medicine, 33(10), 1732-1743.
Sbrana, E., Suter, M. A., Abramovici, A. R., Hawkins, H. K., Moss, J. E., Patterson, L., … Aagaard-Tillery, K. (2011). Maternal tobacco use is associated with increased markers of oxidative stress in the placenta. American Journal of Obstetrics and Gynecology, 205(3), 246. https://doi.org/10.1016/j.ajog.2011.06.023
Schoots, M. H., Gordijn, S. J., Scherjon, S. A., van Goor, H., & Hillebrands, J. L. (2018). Oxidative stress in placental pathology. Placenta, 69, 153-161. https://doi.org/10.1016/j.placenta.2018.03.003
Sferruzzi-Perri, A. N., Higgins, J. S., Vaughan, O. R., Murray, A. J., & Fowden, A. L. (2019). Placental mitochondria adapt developmentally and in response to hypoxia to support fetal growth. Proceedings of the National Academy of Sciences, 116(5), 1621-1626.
Stepanov, I., Gupta, P. C., Dhumal, G., Yershova, K., Toscano, W., Hatsukami, D., & Parascandola, M. (2015). High levels of tobacco-specific N-nitrosamines and nicotine in Chaini Khaini, a product marketed as snus. Tobacco Control, 24(e4), e271-e274. https://doi.org/10.1136/tobaccocontrol-2014-051744
Tal, R., Shaish, A., Barshack, I., Polak-Charcon, S., Afek, A., Volkov, A., … Harats, D. (2010). Effects of hypoxia-inducible factor-1alpha overexpression in pregnant mice: Possible implications for preeclampsia and intrauterine growth restriction. The American Journal of Pathology, 177(6), 2950-2962. https://doi.org/10.2353/ajpath.2010.090800
Velicky, P., Knofler, M., & Pollheimer, J. (2016). Function and control of human invasive trophoblast subtypes: Intrinsic vs. maternal control. Cell Adhesion & Migration, 10(1-2), 154-162. https://doi.org/10.1080/19336918.2015.1089376
Warnakulasuriya, S., & Straif, K. (2018). Carcinogenicity of smokeless tobacco: Evidence from studies in humans & experimental animals. The Indian Journal of Medical Research, 148(6), 681-686. https://doi.org/10.4103/ijmr.IJMR_149_18
Yavuz, D., Nergiz, Y., Evsen, M. S., & Ercan, A. Y. A. Z. (2016). The ultrastructure of placental syncytial knots in normotensive, Preeclamptic and HELLP syndrome patients. International Archives of Medical Research, 8(1), 1-11.
Zakowski, M. I., & Herman, N. L. (2004). The placenta: Anatomy, physiology, and transfer of drugs. In D. H. Chestnut (Ed.), Chestnut's obstetric anesthesia: principles and practice (p. 60). Philadelphia: Mosby, Inc.
Zhang, Y., Zhao, W., Jiang, Y., Zhang, R., Wang, J., Li, C., … Wang, L. (2011). Ultrastructural study on human placentae from women subjected to assisted reproductive technology treatments. Biology of Reproduction, 85(3), 635-642. https://doi.org/10.1095/biolreprod.110.090589