Abstract
The plasma membrane of uterine epithelial cells undergoes a number of changes during early pregnancy. The changes in the basolateral membrane at the time of implantation in particular change from being smooth to highly tortuous in morphology, along with a dramatic increase in the number of morphological caveolae at this time. The major protein of caveolar membranes is caveolin, and previous studies have shown that RNA pol I transcription factor (PTRF) and serum deprivation protein response (SDPR) are the two members of the cavin protein family. These proteins are known to be involved in caveolae biogenesis, where they directly bind to cholesterol and lipids and have been reported to promote membrane curvature. As there is an increase in membrane tortuosity and caveolae at the time of implantation, this study investigated PTRF and SDPR to explore the possible roles that they play in the morphology of the uterine epithelium during early pregnancy. PTRF protein abundance did not change in uterine epithelial cells during early pregnancy or in response to ovarian hormones. At the time of implantation in uterine epithelial cells, PTRF co-immunoprecipitated with caveolin 1, thereby demonstrating an association with caveolin-1 at the basal plasma membrane in caveolae. SDPR protein was observed to be present only at the time of fertilisation, and also under the influence of oestrogen alone, where a cytoplasmic localisation in uterine epithelial cells was observed. The localisation and expression PTRF and SDPR in uterine epithelial cells during early pregnancy suggest that they have roles in the maintenance of lipids and cholesterol in the plasma membrane. PTRF and lack of SDPR may contribute not only to the morphology of the basal plasma membrane as observed at the time of implantation, but also to the maintenance of epithelial polarity during early pregnancy.
Abbreviations
- UEC:
-
Uterine epithelial cell
- SDPR:
-
Serum deprivation protein response
- PTRF:
-
RNA pol I transcription factor
References
Bastiani M et al (2009) MURC/cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol 185:1259–1273. doi:10.1083/jcb.200903053
Bauer M, Pelkmans L (2006) A new paradigm for membrane-organizing and -shaping scaffolds. FEBS Lett 580:5559–5564. doi:10.1016/j.febslet.2006.08.077
Briand N, Dugail I, Le Lay S (2011) Cavin proteins: new players in the caveolae field. Biochimie 93:71–77. doi:10.1016/j.biochi.2010.03.022
Chadda R, Mayor S (2008) PTRF triggers a cave in. Cell 132:23–24. doi:10.1016/j.cell.2007.12.021
Demir R, Kayisli UA, Celik-Ozenci C, Korgun ET, Demir-Weusten AY, Arici A (2002) Structural differentiation of human uterine luminal and glandular epithelium during early pregnancy: an ultrastructural and immunohistochemical study. Placenta 23:672–684
Fra AM, Williamson E, Simons K, Parton RG (1995) De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci USA 92:8655–8659
Hansen CG, Nichols BJ (2010) Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 20:177–186. doi:10.1016/j.tcb.2010.01.005
Hansen CG, Bright NA, Howard G, Nichols BJ (2009) SDPR induces membrane curvature and functions in the formation of caveolae. Nat Cell Biol 11:807–814. doi:10.1038/ncb1887
Hayer A, Stoeber M, Bissig C, Helenius A (2010) Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 11:361–382. doi:10.1111/j.1600-0854.2009.01023.x
Hill MM et al (2008) PTRF-cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132:113–124. doi:10.1016/j.cell.2007.11.042
Hill MM et al (2012) Co-regulation of cell polarization and migration by caveolar proteins PTRF/Cavin-1 and caveolin-1. PLoS ONE 7:e43041. doi:10.1371/journal.pone.0043041
Kaneko Y, Lindsay LA, Murphy CR (2008) Focal adhesions disassemble during early pregnancy in rat uterine epithelial cells. Reprod Fertil Dev 20:892–899
Lecce L, Lindsay L, Kaneko Y, Murphy CR (2013) ICAM-2 and lipid rafts disappear from the basal plasma membrane of uterine epithelial cells during early pregnancy in rats. Cell Tissue Res 353:563–573. doi:10.1007/s00441-013-1656-0
Liu L, Pilch PF (2008) A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J Biol Chem 283:4314–4322. doi:10.1074/jbc.M707890200
Madawala RJ, Dowland S, Poon CE, Lindsay LA, Murphy CR (2014) Caveolins redistribute in uterine epithelial cells during early pregnancy in the rat: an epithelial polarisation strategy? Histochem Cell Biol 142:555–567. doi:10.1007/s00418-014-1236-8
McMahon KA et al (2009) SRBC/cavin-3 is a caveolin adapter protein that regulates caveolae function. EMBO J 28:1001–1015
Mineo C, Ying Y-S, Chapline C, Jaken S, Anderson RGW (1998) Targeting of protein kinase Cα to caveolae. J Cell Biol 141:601–610. doi:10.1083/jcb.141.3.601
Murphy CR, Dwarte DM (1987) Increase in cholesterol in the apical plasma membrane of uterine epithelial cells during early pregnancy in the rat. Acta Anat (Basel) 128:76–79
Murphy CR, Martin B (1985) Cholesterol in the plasma membrane of uterine epithelial cells: a freeze-fracture cytochemical study with digitonin. J Cell Sci 78:163–172
Murphy C, Rogers A (1981) Effects of ovarian hormones on cell membranes in the rat uterus. III. The surface carbohydrates at the apex of the luminal epithelium. Cell Biophys 3:305–320
Nabi IR (2009) Cavin fever: regulating caveolae Nat Cell Biol 11:789–791. doi:10.1038/ncb0709-789
Parr MB (1980) Endocytosis at the basal and lateral membranes of rat uterine epithelial-cells during early-pregnancy. J Reprod Fertil 60:95–99
Parr M (1982) Apical vesicles in the rat uterine epithelium during early pregnancy: a morphometric study. Biol Reprod 26:915–924
Psychoyos A (1973) Hormonal control of ovoimplantation Vitam Horm 31:201–256
Shion YL, Murphy CR (1995) The basal plasma membrane and lamina densa of uterine epithelial cells are both altered during early pregnancy and by ovarian hormones in the rat. Eur J Morphol 33:257–264
Vinten J, Johnsen AH, Roepstorff P, Harpoth J, Tranum-Jensen J (2005) Identification of a major protein on the cytosolic face of caveolae. Biochim Biophys Acta 1717:34–40. doi:10.1016/j.bbamem.2005.09.013
Voldstedlund M, Vinten J, Tranum-Jensen J (2001) cav-p60 expression in rat muscle tissues. Cell Tissue Res 306:265–276. doi:10.1007/s004410100439
Acknowledgments
This work was supported by the Australian Research Council, by the NWG Macintosh Memorial Fund of the Department of Anatomy and Histology and by funds from the Murphy laboratory.
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Madawala, R.J., Poon, C.E., Dowland, S.N. et al. PTRF is associated with caveolin 1 at the time of receptivity: but SDPR is absent at the same time. Histochem Cell Biol 143, 637–644 (2015). https://doi.org/10.1007/s00418-015-1308-4
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DOI: https://doi.org/10.1007/s00418-015-1308-4