Abstract
During early pregnancy, the uterine luminal epithelial cells (UECs) and endometrial stromal cells (ESCs) undergo morphological changes to enable blastocyst implantation. The present study investigates, for the first time, the cytoskeletal-associated proteins and α-actinin superfamily members, α-parvin and β-parvin, during early pregnancy in the rat uterus. These two PARVA proteins are involved in cell adhesion, morphological changes and regulation of other cytoskeletal proteins, through binding with proteins such as actin and integrin-linked kinase. α-parvin is present in UECs at fertilisation and significantly decreases by the time of implantation. β-parvin acts in opposition; significantly increasing in both UECs and ESCs at the time of implantation, suggesting a role in the process of decidualisation. Additionally, the presence of a serine-8 residue-phosphorylated α-parvin, which is associated with cell morphology changes, was found in the nuclear region of both UECs and ESCs during implantation and decidualisation. We also show that the presence of both β-parvin and phosphorylated α-parvin in ESCs is dependent on decidualisation occurring. This study demonstrates that the changing balance and localisation of the two PARVA proteins are dependent on the time of uterine receptivity, suggesting a co-dependent role in the cytoskeletal re-organisation crucial to the changing conditions necessary for implantation and decidualisation.
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References
Abrahamsohn PA, Zorn TM (1993) Implantation and decidualization in rodents. J Exp Zool A Ecol Genet Physiol 266(6):603–628
Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G (2009) Comparative aspects of implantation. Reproduction 138(2):195–209
Bravou V, Antonacopoulou A, Papanikolaou S, Nikou S, Lilis I, Giannopoulou E, Kalofonos HP (2015) Focal adhesion proteins α- and β-parvin are overexpressed in human colorectal cancer and correlate with tumor progression. Cancer Investig 33(8):387–397
Brökelmann J, Biggers JD (1979) Studies on the development of cell contacts and of the intercellular matrix during decidualization in the rat. Arch Gynecol 227(2):103–117
Clarke DM, Brown MC, LaLonde DP, Turner CE (2004) Phosphorylation of actopaxin regulates cell spreading and migration. J Cell Biol 166(6):901–912
Curtis M, Nikolopoulos S, Turner C (2002) Actopaxin is phosphorylated during mitosis and is a substrate for cyclin B1/cdc2 kinase. Biochem J 363:233–242
DeFeo V (1967) Decidualization. Cellular biology of the uterus. Appleton-Century-Crofts, New York, pp 191–220
Finn C, Keen P (1963) The induction of deciduomata in the rat. Development 11(4):673–682
Finn C, McLaren A (1967) A study of the early stages of implantation in mice. J Reprod Fertil 13(2):259–267
Fukuda T, Guo L, Shi X, Wu C (2003) CH-ILKBP regulates cell survival by facilitating the membrane translocation of protein kinase B/Akt. J Cell Biol 160(7):1001–1008
Ito M, Hagiyama M, Mimae T, Inoue T, Kato T, Yoneshige A, Nakanishi J, Kondo T, Okada M, Ito A (2014) α-Parvin, a pseudopodial constituent, promotes cell motility and is associated with lymph node metastasis of lobular breast carcinoma. Breast Cancer Res Treat 144(1):59–69
Kaneko Y, Lindsay LA, Murphy CR (2008) Focal adhesions disassemble during early pregnancy in rat uterine epithelial cells. Reprod Fertil Dev 20(8):892–899
Kennedy TG, Gillio-Meina C, Phang SH (2007) Prostaglandins the initiation of blastocyst implantation decidualization. Reproduction 134(5):635–643
Korenbaum E, Olski TM, Noegel AA (2001) Genomic organization and expression profile of the parvin family of focal adhesion proteins in mice and humans. Gene 279(1):69–79
Lindsay LA, Dowland SN, Murphy CR (2016) Uterine focal adhesions are retained at implantation after rat ovarian hyperstimulation. Reproduction 152(6):753–763
Matsudaira P (1994) Actin crosslinking proteins at the leading edge. Semin Cell Biol 5(3):165–174
Matsudalra P (1991) Modular organization of actin crosslinking proteins. Trends Biochem Sci 16:87–92
Murphy CR (1993) The plasma membrane of uterine epithelial cells: structure and histochemistry. Progress Histochem Cytochem 27(3):III–I66
Murphy CR (1995) The Cytoskeleton of uterine epithelial cells: a new player in uterine receptivity and the plasma membrane transformationo. Hum Reprod Update 1(6):567–580
Murphy CR (2004) Uterine receptivity and the plasma membrane transformation. Cell Res 14(4):259–267
Nikolopoulos SN, Turner CE (2000) Actopaxin, a new focal adhesion protein that binds paxillin LD motifs and actin and regulates cell adhesion. J Cell Biol 151(7):1435–1448
Olski TM, Noegel AA, Korenbaum E (2001) Parvin, a 42 kDa focal adhesion protein, related to the alpha-actinin superfamily. J Cell Sci 114(3):525–538
Pignatelli J, LaLonde SE, LaLonde DP, Clarke D, Turner CE (2012) Actopaxin (α-parvin) phosphorylation is required for matrix degradation and cancer cell invasion. J Biol Chem 287(44):37309–37320
Pollard TD, Cooper JA (1986) Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu Rev Biochem 55(1):987–1035
Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET, Eliceiri KW (2017) ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinform 18(1):529
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9(7):676
Sepulveda JL, Wu C (2006) The parvins. Cell Mol Life Sci 63(1):25–35
Shaw TJ, Terry V, Shorey CD, Murphy CR (1998) Alterations in distribution of actin binding proteins in uterine stromal cells during decidualization in the rat. Cell Biol Int 22(3):237–243
Weeds A, Gooch J, Hawkins M, Pope B, Way M (1991) Role of actin-binding proteins in cytoskeletal dynamics. Portland Press Limited, London
Yamaji S, Suzuki A, Kanamori H, Mishima W, Yoshimi R, Takasaki H, Takabayashi M, Fujimaki K, Fujisawa S, Ohno S (2004) Affixin interacts with α-actinin and mediates integrin signaling for reorganization of F-actin induced by initial cell–substrate interaction. J Cell Biol 165(4):539–551
Zhang Y, Chen K, Tu Y, Wu C (2004) Distinct roles of two structurally closely related focal adhesion proteins, α-parvins and β-parvins, in regulation of cell morphology and survival. J Biol Chem 279(40):41695–41705
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The support and facilities of the Bosch Institute Molecular Biology Facility and the Bosch Institute Advanced Microscopy Facility, The University of Sydney.
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Financial support was provided by the Australian Research Council, The Ann Macintosh Foundation of the Discipline of Anatomy and Histology and the Murphy Laboratory.
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Nicholson, L., Madawala, R., Lindsay, L. et al. α-Parvin and β-parvin in the rat uterus during decidualisation and uterine receptivity. Histochem Cell Biol 151, 395–406 (2019). https://doi.org/10.1007/s00418-018-1761-y
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DOI: https://doi.org/10.1007/s00418-018-1761-y