دورية أكاديمية

Cellular Prion protein moonlights vascular smooth muscle cell fate: Surveilled by trophoblast cells.

التفاصيل البيبلوغرافية
العنوان: Cellular Prion protein moonlights vascular smooth muscle cell fate: Surveilled by trophoblast cells.
المؤلفون: Bose R; Division of Cell Biology and Physiology, CSIR-Indian Institute of Chemical Biology, Kolkata, West Bengal, India., Jana SS; Division of Cell Biology and Physiology, CSIR-Indian Institute of Chemical Biology, Kolkata, West Bengal, India., Ain R; Division of Cell Biology and Physiology, CSIR-Indian Institute of Chemical Biology, Kolkata, West Bengal, India.
المصدر: Journal of cellular physiology [J Cell Physiol] 2023 Dec; Vol. 238 (12), pp. 2794-2811. Date of Electronic Publication: 2023 Oct 11.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Wiley-Liss Country of Publication: United States NLM ID: 0050222 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1097-4652 (Electronic) Linking ISSN: 00219541 NLM ISO Abbreviation: J Cell Physiol Subsets: MEDLINE
أسماء مطبوعة: Publication: New York, NY : Wiley-Liss
Original Publication: Philadelphia, Wistar Institute of Anatomy and Biology.
مواضيع طبية MeSH: Muscle, Smooth, Vascular*/metabolism , Prions*/genetics , Prions*/metabolism, Animals ; Female ; Pregnancy ; Rats ; Cell Movement/genetics ; Cells, Cultured ; Endothelial Cells/metabolism ; Myocytes, Smooth Muscle/metabolism ; Prion Proteins/genetics ; Prion Proteins/metabolism ; Trophoblasts/metabolism ; Uterine Artery ; Humans ; Rats, Sprague-Dawley
مستخلص: Uterine spiral artery remodeling (uSAR) is a hallmark of hemochorial placentation. Compromised uSAR leads to adverse pregnancy outcomes. Salient developmental events involved in uSAR are active areas of research and include (a) trophendothelial cell invasion into the spiral arteries, selected demise of endothelial cells; (b) de-differentiation of vascular smooth muscle cells (VSMC); and (c) migration and/or death of VSMCs surrounding spiral arteries. Here we demonstrated that cellular prion (PRNP) is expressed in the rat metrial gland, the entry point of spiral arteries with the highest expression on E16.5, the day at which trophoblast invasion peaks. PRNP is expressed in VSMCs that drift away from the arterial wall. RNA interference of Prnp functionally restricted migration and invasion of rat VSMCs. Furthermore, PRNP interacted with two migration-promoting factors, focal adhesion kinase (FAK) and platelet-derived growth factor receptor-β (PDGFR-β), forming a ter-molecular complex in both the metrial gland and A7r5 cells. The presence of multiple putative binding site of odd skipped related-1 (OSR1) transcription factor on the Prnp promoter was observed using in silico promoter analysis. Ectopic overexpression of OSR1 increased, and knockdown of OSR1 decreased expression of PRNP in VSMCs. Coculture of VSMCs with rat primary trophoblast cells decreased the levels of OSR1 and PRNP. Interestingly, PRNP knockdown led to apoptotic death in ~9% of VSMCs and activated extrinsic apoptotic pathways. PRNP interacts with TRAIL-receptor DR4 and protects VSMCs from TRAIL-mediated apoptosis. These results highlight the biological functions of PRNP in VSMC cell-fate determination during uteroplacental development, an important determinant of healthy pregnancy outcome.
(© 2023 Wiley Periodicals LLC.)
References: Adamson, S. L., Lu, Y., Whiteley, K. J., Holmyard, D., Hemberger, M., Pfarrer, C., & Cross, J. C. (2002). Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Developmental Biology, 250(2), 358-373. https://doi.org/10.1006/dbio.2002.0773.
Ain, R., Canham, L. N., & Soares, M. J. (2003). Gestation stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: Novel endocrine phenotype and regulation. Developmental Biology, 260(1), 176-190. https://doi.org/10.1093/glycob/10.10.959.
Ain, R., & Soares, M. J. (2004). Is the metrial gland really a gland? Journal of Reproductive Immunology, 61(2), 129-131. https://doi.org/10.1093/glycob/10.10.959.
Alfaidy, N., Chauvet, S., Donadio-Andrei, S., Salomon, A., Saoudi, Y., Richaud, P., Aude-Garcia, C., Hoffmann, P., Andrieux, A., Moulis, J. M., Feige, J. J., & Benharouga, M. (2013). Prion protein expression and functional importance in developmental angiogenesis: Role in oxidative stress and copper homeostasis. Antioxidants & Redox Signaling, 18(4), 400-411. https://doi.org/10.1093/glycob/10.10.959.
Alper, T., Haig, D. A., & Clarke, M. C. (1966). The exceptionally small size of the scrapie agent. Biochemical and Biophysical Research Communications, 22(3), 278-284. https://doi.org/10.1093/glycob/10.10.959.
Basatemur, G. L., Jorgensen, H. F., Clarke, M. C. H., Bennett, M. R., & Mallat, Z. (2019). Vascular smooth muscle cells in atherosclerosis. Nature Reviews Cardiology, 16(12), 727-744. https://doi.org/10.1161/CIRCRESAHA.115.306361.
Bendheim, P. E., Brown, H. R., Rudelli, R. D., Scala, L. J., Goller, N. L., Wen, G. Y., Kascsak, R. J., Cashman, N. R., & Bolton, D. C. (1992). Nearly ubiquitous tissue distribution of the scrapie agent precursor protein. Neurology, 42(1), 149. https://doi.org/10.1093/glycob/10.10.959.
Bornfeldt, K. E., Raines, E. W., Graves, L. M., Skinner, M. P., Krebs, E. G., & Ross, R. (1995). Platelet-derived growth factor: Distinct signal transduction pathways associated with migration versus proliferationa. Annals of the New York Academy of Sciences, 766, 416-430. https://doi.org/10.1093/glycob/10.10.959.
Bragason, B. T., & Palsdottir, A. (2005). Interaction of PrP with NRAGE, a protein involved in neuronal apoptosis. Molecular and Cellular Neuroscience, 29(2), 232-244. https://doi.org/10.1093/glycob/10.10.959.
Bulmer, J. N., Innes, B. A., Levey, J., Robson, S. C., & Lash, G. E. (2012). The role of vascular smooth muscle cell apoptosis and migration during uterine spiral artery remodeling in normal human pregnancy. The FASEB Journal, 26(7), 2975-2985. https://doi.org/10.1089/ars.2012.4637.
Cha, S., Sin, M. J., Kim, M. J., Kim, H. J., Kim, Y. S., Choi, E. K., & Kim, M. Y. (2021). Involvement of cellular prion protein in invasion and metastasis of lung cancer by inducing Treg cell development. Biomolecules, 11(2), 285. https://doi.org/10.1093/biolre/ioaa220.
Chen, D. B., & Magness, R. R. (2021). Vascular smooth muscle cells during spiral artery remodeling in early human pregnancy. Biology of Reproduction, 104(2), 252-254. https://doi.org/10.1093/biolre/ioaa220.
Ding, N. Z., Wang, X. M., Jiao, X. W., Li, R., Zeng, C., Li, S. N., Guo, H. S., Wang, Z. Y., Huang, Z., & He, C. Q. (2018). Cellular prion protein is involved in decidualization of mouse uterus. Biology of Reproduction, 99(2), 319-325. https://doi.org/10.1093/glycob/10.10.959.
Ehsani, S., Tao, R., Pocanschi, C. L., Ren, H., Harrison, P. M., & Schmitt-Ulms, G. (2011). Evidence for retrogene origins of the prion gene family. PLoS One, 6(10), e26800. https://doi.org/10.1371/journal.pone.0026800.
Espinoza, J., Romero, R., Mee Kim, Y., Kusanovic, J. P., Hassan, S., Erez, O., Gotsch, F., Gabor Than, N., Papp, Z., & Jai Kim, C. (2006). Normal and abnormal transformation of the spiral arteries during pregnancy. Journal of Perinatal Medicine, 34(6), 447-458. https://doi.org/10.1515/JPM.2006.089.
French, W. J., Creemers, E. E., & Tallquist, M. D. (2008). Platelet-derived growth factor receptors direct vascular development independent of vascular smooth muscle cell function. Molecular and Cellular Biology, 28(18), 5646-5657. https://doi.org/10.1128/MCB.00441-08.
Gerthoffer, W. T. (2007). Mechanisms of vascular smooth muscle cell migration. Circulation Research, 100(5), 607-621. https://doi.org/10.1161/01.RES.0000258492.96097.47.
Harris, L. K., Keogh, R. J., Wareing, M., Baker, P. N., Cartwright, J. E., Aplin, J. D., & Whitley, G. S. J. (2006). Invasive trophoblasts stimulate vascular smooth muscle cell apoptosis by a Fas Ligand-Dependent mechanism. The American Journal of Pathology, 169(5), 1863-1874. https://doi.org/10.2353/ajpath.2006.060265.
Hauck, C. R., Hsia, D. A., & Schlaepfer, D. D. (2000). Focal adhesion kinase facilitates platelet-derived growth Factor-BB-stimulated ERK2 activation required for chemotaxis migration of vascular smooth muscle cells. Journal of Biological Chemistry, 275(52), 41092-41099. https://doi.org/10.1074/jbc.M005450200.
He, C., Medley, S. C., Hu, T., Hinsdale, M. E., Lupu, F., Virmani, R., & Olson, L. E. (2015). PDGFRβ signalling regulates local inflammation and synergizes with hypercholesterolaemia to promote atherosclerosis. Nature Communications, 6, 7770. https://doi.org/10.1038/ncomms8770.
Helwig, J. J., & Le Bouteiller, P. (2007). Physiological smooth muscle cell apoptosis contributes to the uterine vascular remodeling in human early pregnancy. Circulation Research, 100(6), 754-756. https://doi.org/10.1161/01.RES.0000263394.59727.ca.
James, R. G., Kamei, C. N., Wang, Q., Jiang, R., & Schultheiss, T. M. (2006). Odd-skipped related 1 is required for development of the metanephric kidney and regulates formation and differentiation of kidney precursor cells. Development, 133(15), 2995-3004. https://doi.org/10.1242/dev.02442.
Keogh, R. J., Harris, L. K., Freeman, A., Baker, P. N., Aplin, J. D., Whitley, G. S., & Cartwright, J. E. (2007). Fetal-derived trophoblast use the apoptotic cytokine tumor necrosis factor-α-related apoptosis-inducing ligand to induce smooth muscle cell death. Circulation Research, 100(6), 834-841. https://doi.org/10.1161/01.RES.0000261352.81736.37.
Kim, M., Park, H. J., Seol, J. W., Jang, J. Y., Cho, Y. S., Kim, K. R., Choi, Y., Lydon, J. P., Demayo, F. J., Shibuya, M., Ferrara, N., Sung, H. K., Nagy, A., Alitalo, K., & Koh, G. Y. (2013). VEGF-A regulated by progesterone governs uterine angiogenesis and vascular remodelling during pregnancy. EMBO Molecular Medicine, 5(9), 1415-1430. https://doi.org/10.1002/emmm.201302618.
Koyama, N., Morisaki, N., Saito, Y., & Yoshida, S. (1992). Regulatory effects of platelet-derived growth factor-AA homodimer on migration of vascular smooth muscle cells. Journal of Biological Chemistry, 267(32), 22806-22812.
Levéen, P., Pekny, M., Gebre-Medhin, S., Swolin, B., Larsson, E., & Betsholtz, C. (1994). Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes & Development, 8(16), 1875-1887. https://doi.org/10.1101/gad.8.16.1875.
Liu, H., Ning, F., & Lash, G. E. (2022). Contribution of vascular smooth muscle cell apoptosis to spiral artery remodeling in early human pregnancy. Placenta, 120, 10-17. https://doi.org/10.1016/j.placenta.2022.02.005.
Makzhami, S., Passet, B., Halliez, S., Castille, J., Moazami-Goudarzi, K., Duchesne, A., Vilotte, M., Laude, H., Mouillet-Richard, S., Béringue, V., Vaiman, D., & Vilotte, J. L. (2014). The prion protein family: A view from the placenta. Frontiers in Cell and Developmental Biology, 2, 35. https://doi.org/10.3389/fcell.2014.00035.
Meekins, J. W., Pijnenborg, R., Hanssens, M., MCFadyen, I. R., & van Asshe, A. (1994). A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. BJOG: An International Journal of Obstetrics & Gynaecology, 101(8), 669-674. https://doi.org/10.1111/j.1471-0528.1994.tb13182.x.
Nandy, D., Das, S., Islam, S., & Ain, R. (2020). Molecular regulation of vascular smooth muscle cell phenotype switching by trophoblast cells at the maternal-fetal interface. Placenta, 93, 64-73. https://doi.org/10.1016/j.placenta.2020.02.017.
Nishizawa, H., Pryor-Koishi, K., Kato, T., Kowa, H., Kurahashi, H., & Udagawa, Y. (2007). Microarray analysis of differentially expressed fetal genes in placental tissue derived from early and late onset severe pre-eclampsia. Placenta, 28(5-6), 487-497. https://doi.org/10.1016/j.placenta.2006.05.010.
O'Brien, L. L., Guo, Q., Bahrami-Samani, E., Park, J. S., Hasso, S. M., Lee, Y. J., Fang, A., Kim, A. D., Guo, J., Hong, T. M., Peterson, K. A., Lozanoff, S., Raviram, R., Ren, B., Fogelgren, B., Smith, A. D., Valouev, A., & McMahon, A. P. (2018). Transcriptional regulatory control of mammalian nephron progenitors revealed by multi-factor cistromic analysis and genetic studies. PLoS Genetics, 14(1), e1007181. https://doi.org/10.1371/journal.pgen.1007181.
Owens, L. V., Xu, L., Marston, W. A., Yang, X., Farber, M. A., Iacocca, M. V., Cance, W. G., & Keagy, B. A. (2001). Overexpression of the focal adhesion kinase (p125FAK in the vascular smooth muscle cells of intimal hyperplasia. Journal of Vascular Surgery, 34(2), 344-349. https://doi.org/10.1067/mva.2001.114814.
Pahk, K., Joung, C., Jung, S. M., Young Song, H., Yong Park, J., Woo Byun, J., Lee, Y. S., Chul Paeng, J., Kim, C., Kim, S., & Kim, W. K. (2017). Visualization of synthetic vascular smooth muscle cells in atherosclerotic carotid rat arteries by F-18 FDG PET. Scientific Reports, 7(1), 6989. https://doi.org/10.1038/s41598-017-07073-3.
Pan, Y., Zhao, L., Liang, J., Liu, J., Shi, Y., Liu, N., Zhang, G., Jin, H., Gao, J., Xie, H., Wang, J., Liu, Z., Fan, D. (2006). Cellular prion protein promotes invasion and metastasis of gastric cancer. The FASEB Journal, 20(11), 1886-1888. https://doi.org/10.1096/fj.06-6138fje.
Passet, B., Young, R., Makhzami, S., Vilotte, M., Jaffrezic, F., Halliez, S., Bouet, S., Marthey, S., Khalifé, M., Kanellopoulos-Langevin, C., Béringue, V., Le Provost, F., Laude, H., & Vilotte, J. L. (2012). Prion protein and Shadoo are involved in overlapping embryonic pathways and trophoblastic development. PLoS One, 7(7), e41959. https://doi.org/10.1371/journal.pone.0041959.
Paul, M., Chakraborty, S., Islam, S., & Ain, R. (2022). Trans-differentiation of trophoblast stem cells: Implications in placental biology. Life Science Alliance, 6(3), e202201583. https://doi.org/10.26508/lsa.202201583.
Pijnenborg, R., Vercruysse, L., & Hanssens, M. (2006). The uterine spiral arteries in human pregnancy: Facts and controversies. Placenta, 27(9-10), 939-958. https://doi.org/10.1016/j.placenta.2005.12.006.
Prusiner, S. B. (1998). Prions. Proceedings of the National Academy of Sciences USA. 95(23), 13363-13383. https://doi.org/10.1073/pnas.95.23.13363.
Puig, B., Altmeppen, H., & Glatzel, M. (2014). The GPI-anchoring of PrP. Prion, 8(1), 11-18. https://doi.org/10.1089/ars.2012.4637.
Rensen, S. S. M., Doevendans, P. A. F. M., & VanEys, G. J. J. M. (2007). Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Netherlands Heart Journal, 15(3), 100-108. https://doi.org/10.1007/BF03085963.
Robertson, W. B., & Warner, B. (1974). The ultrastructure of the human placental bed. The Journal of Pathology, 112(4), 203-211. https://doi.org/10.1002/path.1711120403.
Robson, A., Harris, L. K., Innes, B. A., Lash, G. E., Aljunaidy, M. M., Aplin, J. D., Baker, P. N., Robson, S. C., & Bulmer, J. N. (2012). Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. The FASEB Journal, 26(12), 4876-4885. https://doi.org/10.1096/fj.12-210310.
Rosario, G. X., Ain, R., Konno, T., & Soares, M. J. (2009). Intrauterine fate of invasive trophoblast cells. Placenta, 30(5), 457-463. https://doi.org/10.1016/j.placenta.2009.02.008.
Rosario, G. X., Konno, T., & Soares, M. J. (2008). Maternal hypoxia activates endovascular trophoblast cell invasion. Developmental Biology, 314(2), 362-375. https://doi.org/10.1016/j.ydbio.2007.12.007.
Roucou, X., Guo, Q., Zhang, Y., Goodyer, C. G., & Leblanc, A. C. (2003). Cytosolic prion protein is not toxic and protects against Bax-mediated cell death in human primary neurons. Journal of Biological Chemistry, 278(42), 40877-40881. https://doi.org/10.1074/jbc.M306177200.
Schmitt-Ulms, G., Ehsani, S., Watts, J. C., Westaway, D., & Wille, H. (2009). Evolutionary descent of prion genes from the ZIP family of metal ion transporters. PLoS One, 4(9), e7208. https://doi.org/10.1371/journal.pone.0007208.
Wang, Q., Qian, J., Wang, F., & Ma, Z. (2012). Cellular prion protein accelerates colorectal cancer metastasis via the Fyn-SP1-SATB1 axis. Oncology Reports, 28(6), 2029-2034. https://doi.org/10.3892/or.2012.2025.
Whitley, G. S. J., & Cartwright, J. E. (2009). Trophoblast-mediated spiral artery remodelling: A role for apoptosis. Journal of Anatomy, 215(1), 21-26. https://doi.org/10.1111/j.1469-7580.2008.01039.x.
Zuegg, J., & Gready, J. E. (2000). Molecular dynamics simulation of human prion protein including both N-linked oligosaccharides and the GPI anchor. Glycobiology, 10(10), 959-974. https://doi.org/10.1093/glycob/10.10.959.
معلومات مُعتمدة: Indian Council of Medical Research
فهرسة مساهمة: Keywords: TRAIL; apoptosis; cell migration; metrial gland; odd-skipped-related1; spiral artery remodeling
المشرفين على المادة: 0 (Prion Proteins)
0 (Prions)
EC 2.7.11.1 (Oxsr1 protein, rat)
تواريخ الأحداث: Date Created: 20231011 Date Completed: 20231218 Latest Revision: 20240201
رمز التحديث: 20240201
DOI: 10.1002/jcp.31130
PMID: 37819170
قاعدة البيانات: MEDLINE
الوصف
تدمد:1097-4652
DOI:10.1002/jcp.31130