Evolution of a novel adrenal cell type that promotes parental care

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  • Arendt, D. et al. The origin and evolution of cell types. Nat. Rev. Genet. 17, 744–757 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tosches, M. A. et al. Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science 360, 881–888 (2018).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Bakken, T. E. et al. Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans. eLife 10, e64875 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Krienen, F. M. et al. Innovations present in the primate interneuron repertoire. Nature 586, 262–269 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hain, D. et al. Molecular diversity and evolution of neuron types in the amniote brain. Science 377, eabp8202 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Woych, J. et al. Cell-type profiling in salamanders identifies innovations in vertebrate forebrain evolution. Science 377, eabp9186 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bakken, T. E. et al. Comparative cellular analysis of motor cortex in human, marmoset and mouse. Nature 598, 111–119 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Callaway, E. M. et al. A multimodal cell census and atlas of the mammalian primary motor cortex. Nature 598, 86–102 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Knoedler, J. R. et al. A functional cellular framework for sex and estrous cycle-dependent gene expression and behavior. Cell 185, 654–671.e22 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kim, D.-W. et al. Multimodal analysis of cell types in a hypothalamic node controlling social behavior. Cell 179, 713–728.e17 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Moffitt, J. R. et al. Molecular, spatial, and functional single-cell profiling of the hypothalamic preoptic region. Science 362, eaau5324 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brückner, A. et al. Evolutionary assembly of cooperating cell types in an animal chemical defense system. Cell 184, 6138–6156.e28 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Khadraoui, M., Merritt, J. R., Hoekstra, H. E. & Bendesky, A. Post-mating parental behavior trajectories differ across four species of deer mice. PLoS ONE 17, e0276052 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Melmed, S., Koenig, R., Rosen, C., Auchus, R. & Goldfine, A. Williams Textbook of Endocrinology 14th edn (Elsevier Health Sciences, 2019).

  • Barresi, M. J. F. & Gilbert, S. F. Developmental Biology 13th edn (Oxford Univ. Press, 2023).

  • Keeney, D. S., Jenkins, C. M. & Waterman, M. R. Developmentally regulated expression of adrenal 17 α-hydroxylase cytochrome P450 in the mouse embryo. Endocrinology 136, 4872–4879 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ogunsua, A. O., de Nicola, A. F., Traikov, H., Birmingham, M. K. & Levine, S. Adrenal steroid biosynthesis by different species of mouselike rodents. Gen. Comp. Endocrinol. 16, 192–199 (1971).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mao, J., Duan, R. W., Zhong, L., Gibori, G. & Azhar, S. Expression, purification and characterization of the rat luteal 20 α-hydroxysteroid dehydrogenase. Endocrinology 138, 182–190 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Veliça, P. et al. Lack of functional and expression homology between human and mouse aldo-keto reductase 1C enzymes: implications for modelling human cancers. Mol. Cancer 8, 121 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wooldridge, T. B. et al. An enhancer of Agouti contributes to parallel evolution of cryptically colored beach mice. Proc. Natl Acad. Sci. USA 119, e2202862119 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kubli-Garfias, C. & Whalen, R. E. Induction of lordosis behavior in female rats by intravenous administration of progestins. Horm. Behav. 9, 380–386 (1977).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bendesky, A. et al. The genetic basis of parental care evolution in monogamous mice. Nature 544, 434–439 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Williams, J. R., Catania, K. C. & Carter, C. S. Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Horm. Behav. 26, 339–349 (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ogle, T. F. & Beyer, B. K. Steroid-binding specificity of the progesterone receptor from rat placenta. J. Steroid Biochem. 16, 147–150 (1982).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Young, P. C. & Cleary, R. E. Characterization and properties of progesterone-binding components in human endometrium. J. Clin. Endocrinol. Metab. 39, 425–439 (1974).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nowak, F. V., Nuti, K. M. & Karavolas, H. J. Quantitative changes in the metabolism of 20α-hydroxy-4-pregnen-3-one by rat hypothalamus and pituitary during proestrus. Steroids 28, 509–520 (1976).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nowak, F. V. Distribution and metabolism of 20α-hydroxylated progestins in the female rat. J. Steroid Biochem. Mol. Biol. 80, 469–479 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Khanna, M., Qin, K.-N. & Cheng, K.-C. Distribution of 3α-hydroxysteroid dehydrogenase in rat brain and molecular cloning of multiple cDNAs encoding structurally related proteins in humans. J. Steroid Biochem. Mol. Biol. 53, 41–46 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Penning, T. M. et al. Human 3α-hydroxysteroid dehydrogenase isoforms (AKR1C1–AKR1C4) of the aldo-keto reductase superfamily: functional plasticity and tissue distribution reveals roles in the inactivation and formation of male and female sex hormones. Biochem. J 351, 67–77 (2000).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Agís-Balboa, R. C. et al. Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis. Proc. Natl Acad. Sci. USA 103, 14602–14607 (2006).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Russell, D. W. & Wilson, J. D. Steroid 5 α-reductase: two genes/two enzymes. Annu. Rev. Biochem. 63, 25–61 (1994).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • MacKenzie, G. & Maguire, J. Neurosteroids and GABAergic signaling in health and disease. Biomol. Concepts 4, 29–42 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rudolph, S. et al. Cerebellum-specific deletion of the GABAA receptor δ subunit leads to sex-specific disruption of behavior. Cell Rep. 33, 108338 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kohl, J. & Dulac, C. Neural control of parental behaviors. Curr. Opin. Neurobiol. 49, 116–122 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stell, B. M., Brickley, S. G., Tang, C. Y., Farrant, M. & Mody, I. Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by δ subunit-containing GABAA receptors. Proc. Natl Acad. Sci. USA 100, 14439–14444 (2003).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Maguire, J. & Mody, I. GABAAR plasticity during pregnancy: relevance to postpartum depression. Neuron 59, 207–213 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Maguire, J., Ferando, I., Simonsen, C. & Mody, I. Excitability changes related to GABAA receptor plasticity during pregnancy. J. Neurosci. 29, 9592–9601 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Priestley, C. M., Williamson, E. M., Wafford, K. A. & Sattelle, D. B. Thymol, a constituent of thyme essential oil, is a positive allosteric modulator of human GABAA receptors and a homo-oligomeric GABA receptor from Drosophila melanogaster. Br. J. Pharmacol. 140, 1363–1372 (2003).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Belelli, D. & Gee, K. W. 5α-pregnan-3α,20α-diol behaves like a partial agonist in the modulation of GABA-stimulated chlride ion uptake by synaptoneurosomes. Eur. J. Pharmacol. 167, 173–176 (1989).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Farrant, M. & Nusser, Z. Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors. Nat. Rev. Neurosci. 6, 215–229 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bixo, M. et al. Treatment of premenstrual dysphoric disorder with the GABAA receptor modulating steroid antagonist Sepranolone (UC1010)-A randomized controlled trial. Psychoneuroendocrinology 80, 46–55 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Legesse, D. H. et al. Structural insights into opposing actions of neurosteroids on GABAA receptors. Nat. Commun. 14, 5091 (2023).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dolfi, B. et al. Unravelling the sex-specific diversity and functions of adrenal gland macrophages. Cell Rep. 39, 110949 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hanemaaijer, E. S. et al. Single-cell atlas of developing murine adrenal gland reveals relation of Schwann cell precursor signature to neuroblastoma phenotype. Proc. Natl Acad. Sci. USA 118, e2022350118 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huang, L. et al. Single-cell transcriptomes reveal characteristic features of cell types within the human adrenal microenvironment. J. Cell. Physiol. 236, 7308–7321 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lai, S. et al. Mapping a mammalian adult adrenal gland hierarchy across species by microwell-seq. Cell Regen. 9, 11 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mitani, F. Functional zonation of the rat adrenal cortex: the development and maintenance. Proc. Jpn. Acad. Ser. B 90, 163–183 (2014).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Barreto, G. et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445, 671–675 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wingert, S. et al. DNA-damage response gene GADD45A induces differentiation in hematopoietic stem cells without inhibiting cell cycle or survival. Stem Cells 34, 699–710 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhang, R., Shao, J. & Xiang, L. GADD45A protein plays an essential role in active DNA demethylation during terminal osteogenic differentiation of adipose-derived mesenchymal stem cells. J. Biol. Chem. 286, 41083–41094 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tucker, R. P. & Degen, M. The expression and possible functions of tenascin-W during development and disease. Front. Cell Dev. Biol. 7, 1–10 (2019).

    Article 

    Google Scholar
     

  • Merritt, J. R. et al. A supergene-linked estrogen receptor drives alternative phenotypes in a polymorphic songbird. Proc. Natl Acad. Sci. USA 117, 21673–21680 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Florensa, E., Harrison, R., Johnson, M. & Youssefnejadian, E. Plasma 20α-dihydroprogesterone, progesterone and 17-hydroxyprogesterone in normal human pregnancy. Acta Endocrinol. 86, 634–640 (1977).

    CAS 

    Google Scholar
     

  • Abdel-Khalik, J., Björklund, E. & Hansen, M. Simultaneous determination of endogenous steroid hormones in human and animal plasma and serum by liquid or gas chromatography coupled to tandem mass spectrometry. J. Chromatogr. B 928, 58–77 (2013).

    Article 
    CAS 

    Google Scholar
     

  • Jensen, C. C. Quantitative determination of urinary pregnanediol and allopregnanediol for clinical use. Eur. J. Endocrinol. 18, 281–287 (1955).

    Article 
    CAS 

    Google Scholar
     

  • Patterson, R., Balan, I., Morrow, A. L. & Meltzer-Brody, S. Novel neurosteroid therapeutics for post-partum depression: perspectives on clinical trials, program development, active research, and future directions. Neuropsychopharmacology 49, 67–72 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hobert, O. & Kratsios, P. Neuronal identity control by terminal selectors in worms, flies, and chordates. Curr. Opin. Neurobiol. 56, 97–105 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lynch, V. J. et al. Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals. Proc. Natl Acad. Sci. USA 105, 14928–14933 (2008).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lynch, V. J., May, G. & Wagner, G. P. Regulatory evolution through divergence of a phosphoswitch in the transcription factor CEBPB. Nature 480, 383–386 (2011).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Chiquet-Ehrismann, R., Orend, G., Chiquet, M., Tucker, R. P. & Midwood, K. S. Tenascins in stem cell niches. Matrix Biol. 37, 112–123 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pesheva, P., Gloor, S., Schachner, M. & Probstmeier, R. Tenascin-R is an intrinsic autocrine factor for oligodendrocyte differentiation and promotes cell adhesion by a sulfatide-mediated mechanism. J. Neurosci. 17, 4642–4651 (1997).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kimura, H., Akiyama, H., Nakamura, T. & Crombrugghe, B. Tenascin-W inhibits proliferation and differentiation of preosteoblasts during endochondral bone formation. Biochem. Biophys. Res. Commun. 356, 935–941 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Czopka, T., Von Holst, A., Schmidt, G., Ffrench-Constant, C. & Faissner, A. Tenascin C and tenascin R similarly prevent the formation of myelin membranes in a RhoA-dependent manner, but antagonistically regulate the expression of myelin basic protein via a separate pathway. Glia 57, 1790–1801 (2009).

    Article 
    PubMed 

    Google Scholar
     

  • Uhlén, M. et al. Tissue-based map of the human proteome. Science 347, 1260419 (2015).

    Article 
    PubMed 

    Google Scholar
     

  • Choi, H. M. T. et al. Third-generation in situ hybridization chain reaction: multiplexed, quantitative, sensitive, versatile, robust. Development 145, dev165753 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kuehn, E. et al. Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii. J. Exp. Zoolog. B 338, 225–240 (2022).

    Article 

    Google Scholar
     

  • Renier, N. et al. iDISCO: A simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159, 896–910 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bedford, N. L. et al. Automated tracking reveals the social network of beach mice and their burrows. Preprint at bioRxiv https://doi.org/10.1101/2021.08.07.455531 (2021).

  • Kingsley, E. P., Kozak, K. M., Pfeifer, S. P., Yang, D.-S. & Hoekstra, H. E. The ultimate and proximate mechanisms driving the evolution of long tails in forest deer mice. Evolution 71, 261–273 (2017).

    Article 
    PubMed 

    Google Scholar
     

  • Pallares, L. F., Picard, S. & Ayroles, J. F. TM3′seq: a tagmentation-mediated 3′ sequencing approach for improving scalability of RNA-seq experiments. G3 10, 143–150 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Picelli, S. et al. Tn5 transposase and tagmentation procedures for massively scaled sequencing projects. Genome Res. 24, 2033–2040 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Turro, E. et al. Haplotype and isoform specific expression estimation using multi-mapping RNA-seq reads. Genome Biol. 12, R13 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Detlefsen, A. J., Wangtrakuldee, P. & Penning, T. M. Characterization of the major single nucleotide polymorphic variants of aldo-keto reductase 1C3 (type 5 17β-hydroxysteroid dehydrogenase). J. Steroid Biochem. Mol. Biol. 221, 106121 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Friard, O. & Gamba, M. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol. Evol. 7, 1325–1330 (2016).

    Article 

    Google Scholar
     

  • Bright, D. P. & Smart, T. G. Methods for recording and measuring tonic GABAA receptor-mediated inhibition. Front. Neural Circuits 7, 193 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fleming, S. J. et al. Unsupervised removal of systematic background noise from droplet-based single-cell experiments using CellBender. Nat. Methods 20, 1323–1335 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587.e29 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huang, Y., McCarthy, D. J. & Stegle, O. Vireo: Bayesian demultiplexing of pooled single-cell RNA-seq data without genotype reference. Genome Biol. 20, 273 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hao, Y. et al. Dictionary learning for integrative, multimodal and scalable single-cell analysis. Nat. Biotechnol. 42, 293–304 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mi, H. et al. Protocol update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0). Nat. Protoc. 14, 703–721 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kirilenko, B. M. et al. Integrating gene annotation with orthology inference at scale. Science 380, eabn3107 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Corbett-Detig, R. & Nielsen, R. A hidden Markov model approach for simultaneously estimating local ancestry and admixture time using next generation sequence data in samples of arbitrary ploidy. PLoS Genet. 13, e1006529 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Broman, K. W., Wu, H., Sen, Ś. & Churchill, G. A. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889–890 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wickham, H. Ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2016).

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