Lipid Rafts and Cytoskeletal Proteins in Placental Microvilli Membranes from Preeclamptic and IUGR Pregnancies

Overview

Journal J Membr Biol

Date 2011 May 17

PMID 21573936

Citations 11

Authors

Gloria Riquelme

Catalina Vallejos

Nicole De Gregorio

Barbara Morales

Valeria Godoy

Macarena Berrios

Noelia Bastias

Carolina Rodriguez

Affiliations

Soon will be listed here.

Abstract

Intrauterine growth restriction (IUGR) and preeclampsia (PE) are leading causes of perinatal and maternal morbidity and mortality. Previously we reported the expression of lipid rafts in classical microvillous membrane (MVM) and light microvillous membrane (LMVM), two subdomains in apical membrane from the human placental syncytiotrophoblast (hSTB), which constitute the epithelium responsible for maternal-fetal transport. Here the aim was to study the raft and cytoskeletal proteins from PE and IUGR. Microdomains from MVM and LMVM were tested with raft markers (placental alkaline phosphatase, lipid ganglioside, and annexin 2) and a nonraft marker (hTf-R). No changes were detected with those markers in whole purified apical membranes in normal, PE, and IUGR pregnancies; however, their patterns of distribution in lipid rafts were different in PE and IUGR. Cholesterol depletion modified their segregation, confirming their presence in lipid rafts, although unlike normal placenta, in these pathologies there is only one type of microdomain. Additionally, the cytoskeleton proteins actin, ezrin, and cytokeratin-7 showed clear differences between normal and pathological membranes. Cytokeratin-7 expression decreased to 50% in PE, and the distribution between LMVM and MVM (~43 and 57%, respectively) changed in both PE and IUGR, in contrast with the asymmetrical enrichment obtained in normal LMVM (~62%). In conclusion, lipid rafts from IUGR and PE have different features compared to rafts from normal placentae, and this is associated with alterations in the expression and distribution of cytoskeletal proteins.

Citing Articles

Paradoxes: Cholesterol and Hypoxia in Preeclampsia.

Hart N Biomolecules. 2024; 14(6).

PMID: 38927094 PMC: 11201883. DOI: 10.3390/biom14060691.

Ezrin and Its Phosphorylated Thr567 Form Are Key Regulators of Human Extravillous Trophoblast Motility and Invasion.

Tabrizi M, Gupta J, Gross S Cells. 2023; 12(5).

PMID: 36899847 PMC: 10000480. DOI: 10.3390/cells12050711.

Maternal plasma syndecan-1: a biomarker for fetal growth restriction.

Juusela A, Jung E, Gallo D, Bosco M, Suksai M, Diaz-Primera R J Matern Fetal Neonatal Med. 2023; 36(1):2150074.

PMID: 36597808 PMC: 10291740. DOI: 10.1080/14767058.2022.2150074.

Data-Mining Approach on Transcriptomics and Methylomics Placental Analysis Highlights Genes in Fetal Growth Restriction.

Chabrun F, Huetz N, Dieu X, Rousseau G, Bouzille G, Chao de la Barca J Front Genet. 2020; 10:1292.

PMID: 31998361 PMC: 6962302. DOI: 10.3389/fgene.2019.01292.

Placenta-Specific Genes, Their Regulation During Villous Trophoblast Differentiation and Dysregulation in Preterm Preeclampsia.

Szilagyi A, Gelencser Z, Romero R, Xu Y, Kiraly P, Demeter A Int J Mol Sci. 2020; 21(2).

PMID: 31963593 PMC: 7013556. DOI: 10.3390/ijms21020628.

References

Johansson M, Karlsson L, Wennergren M, Jansson T, Powell T . Activity and protein expression of Na+/K+ ATPase are reduced in microvillous syncytiotrophoblast plasma membranes isolated from pregnancies complicated by intrauterine growth restriction. J Clin Endocrinol Metab. 2003; 88(6):2831-7. DOI: 10.1210/jc.2002-021926. View

Paradela A, Bravo S, Henriquez M, Riquelme G, Gavilanes F, Gonzalez-Ros J . Proteomic analysis of apical microvillous membranes of syncytiotrophoblast cells reveals a high degree of similarity with lipid rafts. J Proteome Res. 2005; 4(6):2435-41. DOI: 10.1021/pr050308v. View

Meder D, Moreno M, Verkade P, Vaz W, Simons K . Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proc Natl Acad Sci U S A. 2006; 103(2):329-34. PMC: 1324955. DOI: 10.1073/pnas.0509885103. View

Romanenko V, Fang Y, Byfield F, Travis A, Vandenberg C, Rothblat G . Cholesterol sensitivity and lipid raft targeting of Kir2.1 channels. Biophys J. 2004; 87(6):3850-61. PMC: 1304896. DOI: 10.1529/biophysj.104.043273. View

Guller S, Ma Y, Fu H, Krikun G, Abrahams V, Mor G . The placental syncytium and the pathophysiology of preeclampsia and intrauterine growth restriction: a novel assay to assess syncytial protein expression. Ann N Y Acad Sci. 2008; 1127:129-33. PMC: 3671376. DOI: 10.1196/annals.1434.015. View

Harder T, Scheiffele P, Verkade P, Simons K . Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol. 1998; 141(4):929-42. PMC: 2132776. DOI: 10.1083/jcb.141.4.929. View

Godoy V, Riquelme G . Distinct lipid rafts in subdomains from human placental apical syncytiotrophoblast membranes. J Membr Biol. 2008; 224(1-3):21-31. DOI: 10.1007/s00232-008-9125-5. View

Jahn K, Braet F . Monitoring membrane rafts in colorectal cancer cells by means of correlative fluorescence electron microscopy (CFEM). Micron. 2008; 39(8):1393-7. DOI: 10.1016/j.micron.2008.04.003. View

Norberg S, Powell T, Jansson T . Intrauterine growth restriction is associated with a reduced activity of placental taurine transporters. Pediatr Res. 1998; 44(2):233-8. DOI: 10.1203/00006450-199808000-00016. View

10.

Riquelme G, Parra M . Regulation of human placental chloride channel by arachidonic acid and other cis unsaturated fatty acids. Am J Obstet Gynecol. 1999; 180(2 Pt 1):469-75. DOI: 10.1016/s0002-9378(99)70234-6. View

11.

Wiechelman K, Braun R, Fitzpatrick J . Investigation of the bicinchoninic acid protein assay: identification of the groups responsible for color formation. Anal Biochem. 1988; 175(1):231-7. DOI: 10.1016/0003-2697(88)90383-1. View

12.

BRETSCHER A . Microfilament structure and function in the cortical cytoskeleton. Annu Rev Cell Biol. 1991; 7:337-74. DOI: 10.1146/annurev.cb.07.110191.002005. View

13.

Belkacemi L, Bainbridge S, Dickinson M, Smith G, Graham C . Glyceryl trinitrate inhibits hypoxia/reoxygenation-induced apoptosis in the syncytiotrophoblast of the human placenta: therapeutic implications for preeclampsia. Am J Pathol. 2007; 170(3):909-20. PMC: 1864864. DOI: 10.2353/ajpath.2007.060665. View

14.

Berryman M, Gary R, BRETSCHER A . Ezrin oligomers are major cytoskeletal components of placental microvilli: a proposal for their involvement in cortical morphogenesis. J Cell Biol. 1995; 131(5):1231-42. PMC: 2120629. DOI: 10.1083/jcb.131.5.1231. View

15.

Harder T, Gerke V . The annexin II2p11(2) complex is the major protein component of the triton X-100-insoluble low-density fraction prepared from MDCK cells in the presence of Ca2+. Biochim Biophys Acta. 1994; 1223(3):375-82. DOI: 10.1016/0167-4889(94)90098-1. View

16.

Arkwright P, Rademacher T, Dwek R, Redman C . Pre-eclampsia is associated with an increase in trophoblast glycogen content and glycogen synthase activity, similar to that found in hydatidiform moles. J Clin Invest. 1993; 91(6):2744-53. PMC: 443340. DOI: 10.1172/JCI116515. View

17.

Tyska M, Mackey A, Huang J, Copeland N, Jenkins N, Mooseker M . Myosin-1a is critical for normal brush border structure and composition. Mol Biol Cell. 2005; 16(5):2443-57. PMC: 1087248. DOI: 10.1091/mbc.e04-12-1116. View

18.

Rajendran L, Masilamani M, Solomon S, Tikkanen R, Stuermer C, Plattner H . Asymmetric localization of flotillins/reggies in preassembled platforms confers inherent polarity to hematopoietic cells. Proc Natl Acad Sci U S A. 2003; 100(14):8241-6. PMC: 166213. DOI: 10.1073/pnas.1331629100. View

19.

Lichtenberg D, Goni F, Heerklotz H . Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem Sci. 2005; 30(8):430-6. DOI: 10.1016/j.tibs.2005.06.004. View

20.

Huppertz B, Kadyrov M, Kingdom J . Apoptosis and its role in the trophoblast. Am J Obstet Gynecol. 2006; 195(1):29-39. DOI: 10.1016/j.ajog.2005.07.039. View