Top

Journal of Assisted Reproduction and Genetics

Published in:

01-03-2019 | Embryo Biology

In vitro fertilization alters phospholipid profiles in mouse placenta

Authors: Shuqiang Chen, Jun Wang, Ming Wang, Jie Lu, Yang Cai, Bo Li

Published in: Journal of Assisted Reproduction and Genetics | Issue 3/2019

Abstract

Purpose

Studies on humans and rodents have clearly shown that in vitro fertilization (IVF) is associated with abnormal placenta formation and function. Currently, dysregulated placental lipid metabolism is one of the emerging pathogenetic pathways implicated in adverse pregnancy outcomes. The purpose of this study was to identify the effects of IVF on lipid metabolism in the mouse placenta.

Methods

Two groups of mouse placentas, composed of control and IVF, were collected at embryonic day 18.5. Placental lipid profiles were measured using liquid chromatography coupled with mass spectrometry. The relative levels of individual lipid were examined and compared. The proteins and enzymes that regulate the phospholipid biosynthesis were also compared by western blot.

Results

A significant increase in levels of phosphatidylcholines, phosphatidylethanolamines, phosphatidylinositols, phosphatidylglycerols, lysophosphatidylcholines, and mitochondrial cardiolipin were found in the IVF placenta. In addition, proteins and enzymes that regulate the phospholipid biosynthesis were also altered in IVF placentas.

Conclusions

After lipidomic analysis, we present the first detailed overview of the effect of IVF on lipid metabolism, especially phospholipid profiles in the placenta in a mouse model. The widespread lipidomic shifts identified in this study might explicate some of the placental dysfunction observed after IVF, thereby illustrating that phospholipids serve as early warning biomarkers of health risks in IVF offspring.

Available only for authorised users

Maltepe E, Fisher SJ. Placenta: the forgotten organ. Annu Rev Cell Dev Biol. 2015;31:523–52.PubMedCrossRef

Holland O, Dekker Nitert M, Gallo LA, Vejzovic M, Fisher JJ, Perkins AV. Review: placental mitochondrial function and structure in gestational disorders. Placenta. 2017;54:2–9.PubMedCrossRef

Morgan TK. Role of the placenta in preterm birth: a review. Am J Perinatol. 2016;33(3):258–66.PubMedCrossRef

Hsiao EY, Patterson PH. Placental regulation of maternal-fetal interactions and brain development. Dev Neurobiol. 2012;72(10):1317–26.PubMedCrossRef

Burton GJ, Fowden AL, Thornburg KL. Placental origins of chronic disease. Physiol Rev. 2016;96(4):1509–65.PubMedPubMedCentralCrossRef

Haavaldsen C, Tanbo T, Eskild A. Placental weight in singleton pregnancies with and without assisted reproductive technology: a population study of 536,567 pregnancies. Hum Reprod. 2012;27(2):576–82.PubMedCrossRef

Vrooman LA, Xin F, Bartolomei MS. Morphologic and molecular changes in the placenta: what we can learn from environmental exposures. Fertil Steril. 2016;106(4):930–40.PubMedPubMedCentralCrossRef

Zhang Y, Zhao W, Jiang Y, Zhang R, Wang J, Li C, et al. Ultrastructural study on human placentae from women subjected to assisted reproductive technology treatments. Biol Reprod. 2011;85(3):635–42.PubMedCrossRef

Bloise E, Lin W, Liu X, Simbulan R, Kolahi KS, Petraglia F, et al. Impaired placental nutrient transport in mice generated by in vitro fertilization. Endocrinology. 2012;153(7):3457–67.PubMedPubMedCentralCrossRef

10.

Collier AC, Miyagi SJ, Yamauchi Y, Ward MA. Assisted reproduction technologies impair placental steroid metabolism. J Steroid Biochem Mol Biol. 2009;116(1–2):21–8.PubMedPubMedCentralCrossRef

11.

Chen S, Sun FZ, Huang X, Wang X, Tang N, Zhu B, et al. Assisted reproduction causes placental maldevelopment and dysfunction linked to reduced fetal weight in mice. Sci Rep. 2015;5:10596.PubMedPubMedCentralCrossRef

12.

Rosenhouse-Dantsker A, Mehta D, Levitan I. Regulation of ion channels by membrane lipids. Compr Physiol. 2012;2(1):31–68.PubMed

13.

Hresko RC, Kraft TE, Quigley A, Carpenter EP, Hruz PW. Mammalian glucose transporter activity is dependent upon anionic and conical phospholipids. J Biol Chem. 2016;291(33):17271–82.PubMedPubMedCentralCrossRef

14.

Laganowsky A, Reading E, Allison TM, Ulmschneider MB, Degiacomi MT, Baldwin AJ, et al. Membrane proteins bind lipids selectively to modulate their structure and function. Nature. 2014;510(7503):172–5.PubMedPubMedCentralCrossRef

15.

Dilworth MR, Sibley CP. Review: transport across the placenta of mice and women. Placenta. 2013;34(Suppl):S34–9.PubMedCrossRef

16.

Powell TL, Jansson T, Illsley NP, Wennergren M, Korotkova M, Strandvik B. Composition and permeability of syncytiotrophoblast plasma membranes in pregnancies complicated by intrauterine growth restriction. Biochim Biophys Acta. 1999;1420(1–2):86–94.PubMedCrossRef

17.

Omatsu K, Kobayashi T, Murakami Y, Suzuki M, Ohashi R, Sugimura M, et al. Phosphatidylserine/phosphatidylcholine microvesicles can induce preeclampsia-like changes in pregnant mice. Semin Thromb Hemost. 2005;31(3):314–20.PubMedCrossRef

18.

Lu YW, Claypool SM. Disorders of phospholipid metabolism: an emerging class of mitochondrial disease due to defects in nuclear genes. Front Genet. 2015;6:3.PubMedPubMedCentralCrossRef

19.

Baig S, Lim JY, Fernandis AZ, Wenk MR, Kale A, Su LL, et al. Lipidomic analysis of human placental syncytiotrophoblast microvesicles in adverse pregnancy outcomes. Placenta. 2013;34(5):436–42.PubMedCrossRef

20.

Korkes HA, Sass N, Moron AF, Camara NO, Bonetti T, Cerdeira AS, et al. Lipidomic assessment of plasma and placenta of women with early-onset preeclampsia. PLoS One. 2014;9(10):e110747.PubMedPubMedCentralCrossRef

21.

Brown SH, Eather SR, Freeman DJ, Meyer BJ, Mitchell TW. A lipidomic analysis of placenta in preeclampsia: evidence for lipid storage. PLoS One. 2016;11(9):e0163972.PubMedPubMedCentralCrossRef

22.

Lam SM, Chua GH, Li XJ, Su B, Shui G. Biological relevance of fatty acyl heterogeneity to the neural membrane dynamics of rhesus macaques during normative aging. Oncotarget. 2016;7(35):55970–89.PubMedPubMedCentralCrossRef

23.

Lam SM, Tong L, Duan X, Petznick A, Wenk MR, Shui G. Extensive characterization of human tear fluid collected using different techniques unravels the presence of novel lipid amphiphiles. J Lipid Res. 2014;55(2):289–98.PubMedPubMedCentralCrossRef

24.

Shui G, Guan XL, Low CP, Chua GH, Goh JS, Yang H, et al. Toward one step analysis of cellular lipidomes using liquid chromatography coupled with mass spectrometry: application to Saccharomyces cerevisiae and Schizosaccharomyces pombe lipidomics. Mol BioSyst. 2010;6(6):1008–17.PubMedCrossRef

25.

Shui G, Cheong WF, Jappar IA, Hoi A, Xue Y, Fernandis AZ, et al. Derivatization-independent cholesterol analysis in crude lipid extracts by liquid chromatography/mass spectrometry: applications to a rabbit model for atherosclerosis. J Chromatogr A. 2011;1218(28):4357–65.PubMedCrossRef

26.

Santos JM, Kowluru RA. Role of mitochondria biogenesis in the metabolic memory associated with the continued progression of diabetic retinopathy and its regulation by lipoic acid. Invest Ophthalmol Vis Sci. 2011;52(12):8791–8.PubMedPubMedCentralCrossRef

27.

Festing MF. Design and statistical methods in studies using animal models of development. ILAR J. 2006;47(1):5–14.PubMedCrossRef

28.

Chicco AJ, Sparagna GC. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Phys Cell Physiol. 2007;292(1):C33–44.CrossRef

29.

Julienne CM, Tardieu M, Chevalier S, Pinault M, Bougnoux P, Labarthe F, et al. Cardiolipin content is involved in liver mitochondrial energy wasting associated with cancer-induced cachexia without the involvement of adenine nucleotide translocase. Biochim Biophys Acta. 2014;1842(5):726–33.PubMedCrossRef

30.

Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, Leevers S, et al. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab. 2008;8(3):224–36.PubMedPubMedCentralCrossRef

31.

Liu YY, Chen MB, Cheng L, Zhang ZQ, Yu ZQ, Jiang Q, et al. microRNA-200a downregulation in human glioma leads to Galphai1 over-expression, Akt activation, and cell proliferation. Oncogene. 2018;37(8):1119.PubMedCrossRef

32.

McMaster CR. From yeast to humans - roles of the Kennedy pathway for phosphatidylcholine synthesis. FEBS Lett. 2017;592(8):1256–72.PubMedCrossRef

33.

Saini-Chohan HK, Holmes MG, Chicco AJ, Taylor WA, Moore RL, McCune SA, et al. Cardiolipin biosynthesis and remodeling enzymes are altered during development of heart failure. J Lipid Res. 2009;50(8):1600–8.PubMedPubMedCentralCrossRef

34.

Lane M, Robker RL, Robertson SA. Parenting from before conception. Science. 2014;345(6198):756–60.PubMedCrossRef

35.

Luke B, Gopal D, Cabral H, Stern JE, Diop H. Adverse pregnancy, birth, and infant outcomes in twins: effects of maternal fertility status and infant gender combinations; the Massachusetts Outcomes Study of Assisted Reproductive Technology. Am J Obstet Gynecol. 2017;217(3):330–e1- e15.PubMedPubMedCentralCrossRef

36.

Moessinger C, Klizaite K, Steinhagen A, Philippou-Massier J, Shevchenko A, Hoch M, et al. Two different pathways of phosphatidylcholine synthesis, the Kennedy pathway and the lands cycle, differentially regulate cellular triacylglycerol storage. BMC Cell Biol. 2014;15:43.PubMedPubMedCentralCrossRef

37.

Rexhaj E, Paoloni-Giacobino A, Rimoldi SF, Fuster DG, Anderegg M, Somm E, et al. Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span. J Clin Invest. 2013;123(12):5052–60.PubMedPubMedCentralCrossRef

38.

Seli E, Babayev E, Collins SC, Nemeth G, Horvath TL. Minireview: metabolism of female reproduction: regulatory mechanisms and clinical implications. Mol Endocrinol. 2014;28(6):790–804.PubMedPubMedCentralCrossRef

39.

Prates EG, Nunes JT, Pereira RM. A role of lipid metabolism during cumulus-oocyte complex maturation: impact of lipid modulators to improve embryo production. Mediat Inflamm. 2014;2014:692067.CrossRef

40.

Fayezi S, Darabi M, Darabi M, Nouri M, Rahimipour A, Mehdizadeh A. Analysis of follicular fluid total phospholipids in women undergoing in-vitro fertilisation. J Obstet Gynaecol. 2014;34(3):259–62.PubMedCrossRef

41.

Bradley J, Pope I, Masia F, Sanusi R, Langbein W, Swann K, et al. Quantitative imaging of lipids in live mouse oocytes and early embryos using CARS microscopy. Development. 2016;143(12):2238–47.PubMedPubMedCentralCrossRef

42.

Vilella F, Ramirez LB, Simon C. Lipidomics as an emerging tool to predict endometrial receptivity. Fertil Steril. 2013;99(4):1100–6.PubMedCrossRef

43.

Barrett HL, Dekker Nitert M, McIntyre HD, Callaway LK. Normalizing metabolism in diabetic pregnancy: is it time to target lipids? Diabetes Care. 2014;37(5):1484–93.PubMedCrossRef

44.

Baumann M, Korner M, Huang X, Wenger F, Surbek D, Albrecht C. Placental ABCA1 and ABCG1 expression in gestational disease: pre-eclampsia affects ABCA1 levels in syncytiotrophoblasts. Placenta. 2013;34(11):1079–86.PubMedCrossRef

45.

Dhalwani NN, Boulet SL, Kissin DM, Zhang Y, McKane P, Bailey MA, et al. Assisted reproductive technology and perinatal outcomes: conventional versus discordant-sibling design. Fertil Steril. 2016;106(3):710–6 e2.PubMedCrossRef

46.

Nicolson GL, Ash ME. Membrane lipid replacement for chronic illnesses, aging and cancer using oral glycerolphospholipid formulations with fructooligosaccharides to restore phospholipid function in cellular membranes, organelles, cells and tissues. Biochim Biophys Acta. 2017;1859(9 Pt B):1704–24.CrossRef

47.

van der Veen JN, Kennelly JP, Wan S, Vance JE, Vance DE, Jacobs RL. The critical role of phosphatidylcholine and phosphatidylethanolamine metabolism in health and disease. Biochim Biophys Acta. 2017;1859(9 Pt B):1558–72.CrossRef

48.

Dumas JF, Goupille C, Julienne CM, Pinault M, Chevalier S, Bougnoux P, et al. Efficiency of oxidative phosphorylation in liver mitochondria is decreased in a rat model of peritoneal carcinosis. J Hepatol. 2011;54(2):320–7.PubMedCrossRef

49.

Babayev E, Seli E. Oocyte mitochondrial function and reproduction. Curr Opin Obstet Gynecol. 2015;27(3):175–81.PubMedPubMedCentralCrossRef

50.

Choi S, Hedman AC, Sayedyahossein S, Thapa N, Sacks DB, Anderson RA. Agonist-stimulated phosphatidylinositol-3,4,5-trisphosphate generation by scaffolded phosphoinositide kinases. Nat Cell Biol. 2016;18(12):1324–35.PubMedPubMedCentralCrossRef

51.

Viaud J, Mansour R, Antkowiak A, Mujalli A, Valet C, Chicanne G, et al. Phosphoinositides: important lipids in the coordination of cell dynamics. Biochimie. 2016;125:250–8.PubMedCrossRef

52.

Li B, Xiao X, Chen S, Huang J, Ma Y, Tang N, et al. Changes of phospholipids in fetal liver of mice conceived by in vitro fertilization. Biol Reprod. 2016;94(5):105.PubMed

53.

Shimano H, Sato R. SREBP-regulated lipid metabolism: convergent physiology - divergent pathophysiology. Nat Rev Endocrinol. 2017;13(12):710–30.PubMedCrossRef

54.

Eberle D, Hegarty B, Bossard P, Ferre P, Foufelle F. SREBP transcription factors: master regulators of lipid homeostasis. Biochimie. 2004;86(11):839–48.PubMedCrossRef

55.

Shao W, Espenshade PJ. Expanding roles for SREBP in metabolism. Cell Metab. 2012;16(4):414–9.PubMedPubMedCentralCrossRef

56.

Jeon TI, Osborne TF. SREBPs: metabolic integrators in physiology and metabolism. Trends Endocrinol Metab. 2012;23(2):65–72.PubMedCrossRef

57.

Cornell RB, Ridgway ND. CTP:phosphocholine cytidylyltransferase: function, regulation, and structure of an amphitropic enzyme required for membrane biogenesis. Prog Lipid Res. 2015;59:147–71.PubMedCrossRef

Title: In vitro fertilization alters phospholipid profiles in mouse placenta
Authors: Shuqiang Chen
Jun Wang
Ming Wang
Jie Lu
Yang Cai
Bo Li
Publication date: 01-03-2019
Publisher: Springer US
Published in: Journal of Assisted Reproduction and Genetics / Issue 3/2019
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI: https://doi.org/10.1007/s10815-018-1387-y

Keynote webinar | Spotlight on medication adherence

Springer Medicine

In vitro fertilization alters phospholipid profiles in mouse placenta

Abstract

Purpose

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 3/2019

Rare genetic variants potentially involved in ovarian hyperstimulation syndrome

Effects of the microfluidic chip technique in sperm selection for intracytoplasmic sperm injection for unexplained infertility: a prospective, randomized controlled trial

Medical or surgical treatment before embryo transfer improves outcomes in women with abnormal endometrial BCL6 expression

Male infertility: establishing sperm aneuploidy thresholds in the laboratory

Overcoming bioethical, legal, and hereditary barriers to mitochondrial replacement therapy in the USA

Cumulus-corona gene expression analysis combined with morphological embryo scoring in single embryo transfer cycles increases live birth after fresh transfer and decreases time to pregnancy