{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,5]],"date-time":"2026-08-05T12:51:19Z","timestamp":1785934279116,"version":"3.56.0"},"reference-count":66,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2024,1,24]],"date-time":"2024-01-24T00:00:00Z","timestamp":1706054400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"SKB"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Caveolin-1 (Cav1) is a major plasma membrane protein that plays important functions in cellular metabolism, proliferation, and senescence. Mice lacking Cav1 show abnormal gene expression in the fetal brain. Though evidence for placental influence on brain development is emerging, whether the ablation of Cav1 affects the regulation of the brain\u2013placental axis remains unexamined. The current study tests the hypothesis that gene expression changes in specific cells of the placenta and the fetal brain are linked to the deregulation of the brain\u2013placental axis in Cav1-null mice. By performing single-nuclei RNA sequencing (snRNA-seq) analyses, we show that the abundance of the extravillious trophoblast (EVT) and stromal cells, but not the cytotrophoblast (CTB) or syncytiotrophoblast (STB), are significantly impacted due to Cav1 ablation in mice. Interestingly, specific genes related to brain development and neurogenesis were significantly differentially expressed in trophoblast cells due to Cav1 deletion. Comparison of single-cell gene expression between the placenta and the fetal brain further showed that specific genes such as plexin A1 (Plxna1), phosphatase and actin regulator 1 (Phactr1) and amyloid precursor-like protein 2 (Aplp2) were differentially expressed between the EVT and STB cells of the placenta, and also, between the radial glia and ependymal cells of the fetal brain. Bulk RNA-seq analysis of the whole placenta and the fetal brain further identified genes differentially expressed in a similar manner between the placenta and the fetal brain due to the absence of Cav1. The deconvolution of reference cell types from the bulk RNA-seq data further showed that the loss of Cav1 impacted the abundance of EVT cells relative to the stromal cells in the placenta, and that of the glia cells relative to the neuronal cells in the fetal brain. Together, the results of this study suggest that the ablation of Cav1 causes deregulated gene expression in specific cell types of the placenta and the fetal brain in mice.<\/jats:p>","DOI":"10.3390\/cells13030215","type":"journal-article","created":{"date-parts":[[2024,1,24]],"date-time":"2024-01-24T07:42:16Z","timestamp":1706082136000},"page":"215","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Single-Cell Transcriptional Response of the Placenta to the Ablation of Caveolin-1: Insights into the Adaptive Regulation of Brain\u2013Placental Axis in Mice"],"prefix":"10.3390","volume":"13","author":[{"given":"Maliha","family":"Islam","sequence":"first","affiliation":[{"name":"Division of Animal Sciences, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1057-2435","authenticated-orcid":false,"given":"Susanta K.","family":"Behura","sequence":"additional","affiliation":[{"name":"Division of Animal Sciences, University of Missouri, Columbia, MO 65211, USA"},{"name":"MU Institute for Data Science and Informatics, University of Missouri, Columbia, MO 65211, USA"},{"name":"Interdisciplinary Reproduction and Health Group, University of Missouri, Columbia, MO 65211, USA"},{"name":"Interdisciplinary Neuroscience Program, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,1,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"15667","DOI":"10.1073\/pnas.1112239108","article-title":"Roles of the Placenta in Fetal Brain Development","volume":"108","author":"Zeltser","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"S99","DOI":"10.1016\/S0301-2115(03)00179-9","article-title":"Placental Insufficiency and Its Consequences","volume":"110","author":"Gagnon","year":"2003","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/npp.2015.231","article-title":"The Placenta as a Mediator of Stress Effects on Neurodevelopmental Reprogramming","volume":"41","author":"Bronson","year":"2016","journal-title":"Neuropsychopharmacology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"104468","DOI":"10.1016\/j.phrs.2019.104468","article-title":"The Brain-Placental Axis: Therapeutic and Pharmacological Relevancy to Pregnancy","volume":"149","author":"Behura","year":"2019","journal-title":"Pharmacol. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"15237","DOI":"10.1073\/pnas.1106022108","article-title":"Placental Protection of the Fetal Brain during Short-Term Food Deprivation","volume":"108","author":"Broad","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"4261","DOI":"10.1096\/fj.201802037R","article-title":"Evidence for Functional Interactions between the Placenta and Brain in Pregnant Mice","volume":"33","author":"Behura","year":"2019","journal-title":"FASEB J."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"531543","DOI":"10.3389\/fimmu.2020.531543","article-title":"Maternal-Fetal Inflammation in the Placenta and the Developmental Origins of Health and Disease","volume":"11","author":"Goldstein","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1146\/annurev-neuro-062012-170354","article-title":"Neural Tube Defects","volume":"37","author":"Greene","year":"2014","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1177\/0192623317728134","article-title":"Histology Atlas of the Developing Prenatal and Postnatal Mouse Central Nervous System, with Emphasis on Prenatal Days E7.5 to E18.5","volume":"45","author":"Chen","year":"2017","journal-title":"Toxicol. Pathol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"566","DOI":"10.3389\/fnhum.2016.00566","article-title":"The Indispensable Roles of Microglia and Astrocytes during Brain Development","volume":"10","author":"Reemst","year":"2016","journal-title":"Front. Hum. Neurosci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1038\/s41576-019-0169-4","article-title":"Mechanisms of Early Placental Development in Mouse and Humans","volume":"21","author":"Hemberger","year":"2020","journal-title":"Nat. Rev. Genet."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1038\/s41390-019-0405-9","article-title":"Placental Programming of Neuropsychiatric Disease","volume":"86","author":"Kratimenos","year":"2019","journal-title":"Pediatr. Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"897","DOI":"10.2217\/epi-2022-0061","article-title":"The Placenta Epigenome-Brain Axis: Placental Epigenomic and Transcriptomic Responses That Preprogram Cognitive Impairment","volume":"14","author":"Freedman","year":"2022","journal-title":"Epigenomics"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1002\/jnr.24603","article-title":"The Placenta-Brain-Axis","volume":"99","author":"Rosenfeld","year":"2021","journal-title":"J. Neurosci. Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.neubiorev.2014.11.013","article-title":"Stress-Induced Perinatal and Transgenerational Epigenetic Programming of Brain Development and Mental Health","volume":"48","author":"Babenko","year":"2015","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e23349","DOI":"10.1096\/fj.202301344R","article-title":"Ablation of Placental REST Deregulates Fetal Brain Metabolism and Impacts Gene Expression of the Offspring Brain at the Postnatal and Adult Stages","volume":"38","author":"Islam","year":"2024","journal-title":"FASEB J."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"107710","DOI":"10.1016\/j.isci.2023.107710","article-title":"Role of Caveolin-1 in Metabolic Programming of Fetal Brain","volume":"26","author":"Islam","year":"2023","journal-title":"iScience"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Head, B.P., Peart, J.N., Panneerselvam, M., Yokoyama, T., Pearn, M.L., Niesman, I.R., Bonds, J.A., Schilling, J.M., Miyanohara, A., and Headrick, J. (2010). Loss of Caveolin-1 Accelerates Neurodegeneration and Aging. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0015697"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"15124","DOI":"10.1021\/bi0356348","article-title":"Caveolin-1 Null (-\/-) Mice Show Dramatic Reductions in Life Span","volume":"42","author":"Park","year":"2003","journal-title":"Biochemistry"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"38121","DOI":"10.1074\/jbc.M105408200","article-title":"Caveolin-1 Null Mice Are Viable but Show Evidence of Hyperproliferative and Vascular Abnormalities","volume":"276","author":"Razani","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1768","DOI":"10.2353\/ajpath.2009.090171","article-title":"Vascular Permeability and Pathological Angiogenesis in Caveolin-1-Null Mice","volume":"175","author":"Chang","year":"2009","journal-title":"Am. J. Pathol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Dhakal, P., Strawn, M., Samal, A., and Behura, S.K. (2021). Fetal Brain Elicits Sexually Conflicting Transcriptional Response to the Ablation of Uterine Forkhead Box A2 (Foxa2) in Mice. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22189693"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1152\/physiol.00001.2005","article-title":"Development of Structures and Transport Functions in the Mouse Placenta","volume":"20","author":"Watson","year":"2005","journal-title":"Physiology"},{"key":"ref_24","first-page":"bhad383","article-title":"Association between Placental Oxygen Transport and Fetal Brain Cortical Development: A Study in Monochorionic Diamniotic Twins","volume":"34","author":"Yun","year":"2023","journal-title":"Cereb. Cortex"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: Ultrafast Universal RNA-Seq Aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1038\/nbt.4096","article-title":"Integrating Single-Cell Transcriptomic Data across Different Conditions, Technologies, and Species","volume":"36","author":"Butler","year":"2018","journal-title":"Nat. Biotechnol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"100723","DOI":"10.1016\/j.margen.2019.100723","article-title":"T-Distributed Stochastic Neighbor Embedding (t-SNE): A Tool for Eco-Physiological Transcriptomic Analysis","volume":"51","author":"Cieslak","year":"2020","journal-title":"Mar. Genom."},{"key":"ref_28","first-page":"baz046","article-title":"PanglaoDB: A Web Server for Exploration of Mouse and Human Single-Cell RNA Sequencing Data","volume":"2019","author":"Gan","year":"2019","journal-title":"Database"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e22463","DOI":"10.1096\/fj.202200255RR","article-title":"Fetal Origin of Sex-Bias Brain Aging","volume":"36","author":"Islam","year":"2022","journal-title":"FASEB J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","article-title":"Fastp: An Ultra-Fast All-in-One FASTQ Preprocessor","volume":"34","author":"Chen","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","article-title":"edgeR: A Bioconductor Package for Differential Expression Analysis of Digital Gene Expression Data","volume":"26","author":"Robinson","year":"2010","journal-title":"Bioinformatics"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.jare.2023.02.017","article-title":"Single-Cell Sequencing Reveals the Evolution of Immune Molecules across Multiple Vertebrate Species","volume":"55","author":"Jiao","year":"2024","journal-title":"J. Adv. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2093","DOI":"10.1093\/bioinformatics\/bty926","article-title":"Dtangle: Accurate and Robust Cell Type Deconvolution","volume":"35","author":"Hunt","year":"2019","journal-title":"Bioinformatics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"R43","DOI":"10.1530\/JOE-17-0402","article-title":"Trophoblast Lineage Specification, Differentiation, and Their Regulation by Oxygen Tension","volume":"236","author":"Chang","year":"2018","journal-title":"J. Endocrinol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"354","DOI":"10.2174\/138920210791616680","article-title":"Functional Genomics: New Insights into the \u201cFunction\u201d of Low Levels of Gene Expression in Stem Cells","volume":"11","author":"Hipp","year":"2010","journal-title":"Curr. Genom."},{"key":"ref_36","first-page":"6435","article-title":"Placental Expression of PAPPA, PAPPA-2 and PLAC-1 in Pregnacies Is Associated with FGR","volume":"17","author":"Sifakis","year":"2018","journal-title":"Mol. Med. Rep."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1824","DOI":"10.1161\/CIRCULATIONAHA.117.028110","article-title":"Disturbed Placental Imprinting in Preeclampsia Leads to Altered Expression of DLX5, a Human-Specific Early Trophoblast Marker","volume":"136","author":"Zadora","year":"2017","journal-title":"Circulation"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Lunghi, L., Ferretti, M.E., Medici, S., Biondi, C., and Vesce, F. (2007). Control of Human Trophoblast Function. Reprod. Biol. Endocrinol., 5.","DOI":"10.1186\/1477-7827-5-6"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1038\/nprot.2013.092","article-title":"Large-Scale Gene Function Analysis with the PANTHER Classification System","volume":"8","author":"Mi","year":"2013","journal-title":"Nat. Protoc."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.nbd.2010.08.016","article-title":"Amyloid Precursor-like Protein 2 Cleavage Contributes to Neuronal Intranuclear Inclusions and Cytotoxicity in Spinocerebellar Ataxia-7 (SCA7)","volume":"41","author":"Breidert","year":"2011","journal-title":"Neurobiol. Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1111\/j.1365-2990.2006.00815.x","article-title":"Caveolin-1 and -2 and Their Relationship to Cerebral Amyloid Angiopathy in Alzheimer\u2019s Disease","volume":"33","author":"Miners","year":"2007","journal-title":"Neuropathol. Appl. Neurobiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1242\/jcs.122440","article-title":"APLP2 Regulates Neuronal Stem Cell Differentiation during Cortical Development","volume":"126","author":"Shariati","year":"2013","journal-title":"J. Cell Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1016\/S0197-4580(97)00151-6","article-title":"Generation of APLP2 KO Mice and Early Postnatal Lethality in APLP2\/APP Double KO Mice","volume":"18","author":"Zheng","year":"1997","journal-title":"Neurobiol. Aging"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1016\/j.celrep.2017.12.044","article-title":"PlexinA2 Forward Signaling through Rap1 GTPases Regulates Dentate Gyrus Development and Schizophrenia-like Behaviors","volume":"22","author":"Zhao","year":"2018","journal-title":"Cell Rep."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e60266","DOI":"10.7554\/eLife.60266","article-title":"Single Nuclei RNA-Seq of Mouse Placental Labyrinth Development","volume":"9","author":"Marsh","year":"2020","journal-title":"Elife"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.neures.2017.08.002","article-title":"Expression Analyses of Phactr1 (Phosphatase and Actin Regulator 1) during Mouse Brain Development","volume":"128","author":"Ito","year":"2018","journal-title":"Neurosci. Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1668","DOI":"10.1016\/j.biochi.2011.07.010","article-title":"Depletion of the Novel Protein PHACTR-1 from Human Endothelial Cells Abolishes Tube Formation and Induces Cell Death Receptor Apoptosis","volume":"93","author":"Jarray","year":"2011","journal-title":"Biochimie"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1812","DOI":"10.1242\/jcs.02894","article-title":"Caveolin-1 Controls Cell Proliferation and Cell Death by Suppressing Expression of the Inhibitor of Apoptosis Protein Survivin","volume":"119","author":"Torres","year":"2006","journal-title":"J. Cell Sci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1022431","DOI":"10.3389\/fncel.2022.1022431","article-title":"What Microglia Depletion Approaches Tell Us about the Role of Microglia on Synaptic Function and Behavior","volume":"16","author":"Basilico","year":"2022","journal-title":"Front. Cell Neurosci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1186\/s13041-017-0307-x","article-title":"An Updated Assessment of Microglia Depletion: Current Concepts and Future Directions","volume":"10","author":"Han","year":"2017","journal-title":"Mol. Brain"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Song, Z., Li, B., Li, M., Luo, J., Hong, Y., He, Y., Chen, S., Yang, Z., Liang, C., and Yang, Z. (2022). Caveolin-1 Regulation and Function in Mouse Uterus during Early Pregnancy and under Human In Vitro Decidualization. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23073699"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1007\/s00418-014-1236-8","article-title":"Caveolins Redistribute in Uterine Epithelial Cells during Early Pregnancy in the Rat: An Epithelial Polarisation Strategy?","volume":"142","author":"Madawala","year":"2014","journal-title":"Histochem. Cell Biol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"41295","DOI":"10.1074\/jbc.R200020200","article-title":"Multiple Functions of Caveolin-1","volume":"277","author":"Liu","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1057","DOI":"10.1071\/RD18296","article-title":"Caveolin-1 Promotes Trophoblast Cell Invasion through the Focal Adhesion Kinase (FAK) Signalling Pathway during Early Human Placental Development","volume":"31","author":"Dai","year":"2019","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.placenta.2009.11.007","article-title":"The Expression of Caveolin-1 and the Distribution of Caveolae in the Murine Placenta and Yolk Sac: Parallels to the Human Placenta","volume":"31","author":"Mohanty","year":"2010","journal-title":"Placenta"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.isci.2018.08.014","article-title":"Caveolin-1 Promotes Early Neuronal Maturation via Caveolae-Independent Trafficking of N-Cadherin and L1","volume":"7","author":"Shikanai","year":"2018","journal-title":"iScience"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1093\/neuonc\/nos079","article-title":"Caveolin-1, Caveolae, and Glioblastoma","volume":"14","author":"Parat","year":"2012","journal-title":"Neuro Oncol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"3416","DOI":"10.1091\/mbc.02-05-0071","article-title":"Caveolin-1-Deficient Mice Show Accelerated Mammary Gland Development During Pregnancy, Premature Lactation, and Hyperactivation of the Jak-2\/STAT5a Signaling Cascade","volume":"13","author":"Park","year":"2002","journal-title":"Mol. Biol. Cell"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"746","DOI":"10.2353\/ajpath.2009.080658","article-title":"Caveolin-1\u2212\/\u2212 Null Mammary Stromal Fibroblasts Share Characteristics with Human Breast Cancer-Associated Fibroblasts","volume":"174","author":"Sotgia","year":"2009","journal-title":"Am. J. Pathol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1702","DOI":"10.1016\/j.ajpath.2011.12.018","article-title":"Altered Angiogenesis in Caveolin-1 Gene-Deficient Mice Is Restored by Ablation of Endothelial Nitric Oxide Synthase","volume":"180","author":"Morais","year":"2012","journal-title":"Am. J. Pathol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"4374","DOI":"10.1073\/pnas.1217505110","article-title":"Lifespan of Neurons Is Uncoupled from Organismal Lifespan","volume":"110","author":"Magrassi","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"9772","DOI":"10.1523\/JNEUROSCI.1604-11.2011","article-title":"The Master Negative Regulator REST\/NRSF Controls Adult Neurogenesis by Restraining the Neurogenic Program in Quiescent Stem Cells","volume":"31","author":"Gao","year":"2011","journal-title":"J. Neurosci."},{"key":"ref_63","first-page":"80","article-title":"Placental Cell Turnover in Health and Disease","volume":"6","author":"Heazell","year":"2006","journal-title":"Rev. Gynaecol. Perinat. Pract."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.placenta.2014.01.011","article-title":"Turnover of Human Villous Trophoblast in Normal Pregnancy: What Do We Know and What Do We Need to Know?","volume":"35","author":"Mayhew","year":"2014","journal-title":"Placenta"},{"key":"ref_65","first-page":"222","article-title":"Scalable in Situ Single-Cell Profiling by Electrophoretic Capture of mRNA Using EEL FISH","volume":"41","author":"Borm","year":"2023","journal-title":"Nat. Biotechnol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/j.mad.2011.11.001","article-title":"Caveolin-1, Cellular Senescence and Age-Related Diseases","volume":"132","author":"Zou","year":"2011","journal-title":"Mech. 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