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Stress
The International Journal on the Biology of Stress
Volume 27, 2024 - Issue 1
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How spatial omics approaches can be used to map the biological impacts of stress in psychiatric disorders: a perspective, overview and technical guide

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Article: 2351394 | Received 17 Oct 2023, Accepted 29 Apr 2024, Published online: 16 May 2024

References

  • Argelaguet, R., Cuomo, A. S. E., Stegle, O., & Marioni, J. C. (2021). Computational principles and challenges in single-cell data integration. Nature Biotechnology, 39(10), 1–11. https://doi.org/10.1038/s41587-021-00895-7
  • Ashley-Koch, A. E., Crawford, G. E., Garrett, M. E., Song, L., Safi, A., Johnson, G. D., Wray, G. A., Reddy, T. E., Goes, F. S., Zandi, P., Bryois, J., Jaffe, A. E., Price, A. J., Ivanov, N. A., Collado-Torres, L., Hyde, T. M., Burke, E. E., Kleiman, J. E., Tao, R., … Abyzov, A. (2018). Revealing the brain’s molecular architecture. Science, 362(6420), 1262–1263. https://doi.org/10.1126/science.362.6420.1262
  • Basu, S., & Banerjee, B. (2020). Impact of environmental factors on mental health of children and adolescents: A systematic review. Children and Youth Services Review, 119, 105515. https://doi.org/10.1016/j.childyouth.2020.105515
  • Batiuk, M. Y., Tyler, T., Dragicevic, K., Mei, S., Rydbirk, R., Petukhov, V., Deviatiiarov, R., Sedmak, D., Frank, E., Feher, V., Habek, N., Hu, Q., Igolkina, A., Roszik, L., Pfisterer, U., Garcia-Gonzalez, D., Petanjek, Z., Adorjan, I., Kharchenko, P. V., & Khodosevich, K. (2022). Upper cortical layer-driven network impairment in schizophrenia. Science Advances, 8(41), eabn8367. https://doi.org/10.1126/sciadv.abn8367
  • Black, S., Phillips, D., Hickey, J. W., Kennedy-Darling, J., Venkataraaman, V. G., Samusik, N., Goltsev, Y., Schürch, C. M., & Nolan, G. P. (2021). CODEX multiplexed tissue imaging with DNA-conjugated antibodies. Nature Protocols, 16(8), 3802–3835. https://doi.org/10.1038/s41596-021-00556-8
  • Bloom, A. B., & Zaman, M. H. (2014). Influence of the microenvironment on cell fate determination and migration. Physiological Genomics, 46(9), 309–314. https://doi.org/10.1152/physiolgenomics.00170.2013
  • Brivio, E., Kos, A., Ulivi, A. F., Karamihalev, S., Ressle, A., Stoffel, R., Hirsch, D., Stelzer, G., Schmidt, M. V., Lopez, J. P., & Chen, A. (2023). Sex shapes cell-type-specific transcriptional signatures of stress exposure in the mouse hypothalamus. Cell Reports, 42(8), 112874. https://doi.org/10.1016/j.celrep.2023.112874
  • Cattane, N., Vernon, A. C., Borsini, A., Scassellati, C., Endres, D., Capuron, L., Tamouza, R., Benros, M. E., Leza, J. C., Pariante, C. M., Riva, M. A., & Cattaneo, A. (2022). Preclinical animal models of mental illnesses to translate findings from the bench to the bedside: Molecular brain mechanisms and peripheral biomarkers associated to early life stress or immune challenges. European Neuropsychopharmacology: The Journal of the European College of Neuropsychopharmacology, 58, 55–79. https://doi.org/10.1016/j.euroneuro.2022.02.002
  • Chen, F., Bertelsen, A. B., Holm, I. E., Nyengaard, J. R., Rosenberg, R., & Dorph-Petersen, K.-A. (2020). Hippocampal volume and cell number in depression, schizophrenia, and suicide subjects. Brain Research, 1727, 146546. https://doi.org/10.1016/j.brainres.2019.146546
  • Chen, S., Zhu, B., Huang, S., Hickey, J. W., Lin, K. Z., Snyder, M., Greenleaf, W. J., Nolan, G. P., Zhang, N. R., & Ma, Z. (2023). Integration of spatial and single-cell data across modalities with weakly linked features. Nature Biotechnology. Advance online publication. https://doi.org/10.1038/s41587-023-01935-0
  • Chklovskii, D. B. (2004). Synaptic connectivity and neuronal morphology: Two sides of the same coin. Neuron, 43(5), 609–617. https://doi.org/10.1016/j.neuron.2004.08.012
  • Cobb, J. A., Simpson, J., Mahajan, G. J., Overholser, J. C., Jurjus, G. J., Dieter, L., Herbst, N., May, W., Rajkowska, G., & Stockmeier, C. A. (2013). Hippocampal volume and total cell numbers in major depressive disorder. Journal of Psychiatric Research, 47(3), 299–306. https://doi.org/10.1016/j.jpsychires.2012.10.020
  • Coleman, J. R. I., Peyrot, W. J., Purves, K. L., Davis, K. A. S., Rayner, C., Choi, S. W., Hübel, C., Gaspar, H. A., Kan, C., Van der Auwera, S., Adams, M. J., Lyall, D. M., Choi, K. W., Dunn, E. C., Vassos, E., Danese, A., Maughan, B., Grabe, H. J., Lewis, C. M., … Breen, G. (2020). Genome-wide gene-environment analyses of major depressive disorder and reported lifetime traumatic experiences in UK Biobank. Molecular Psychiatry, 25(7), 1430–1446. https://doi.org/10.1038/s41380-019-0546-6
  • Cruceanu, C., Dony, L., Krontira, A. C., Fischer, D. S., Roeh, S., Di Giaimo, R., Kyrousi, C., Kaspar, L., Arloth, J., Czamara, D., Gerstner, N., Martinelli, S., Wehner, S., Breen, M. S., Koedel, M., Sauer, S., Sportelli, V., Rex-Haffner, M., Cappello, S., Theis, F. J., & Binder, E. B. (2022). Cell-type-specific impact of glucocorticoid receptor activation on the developing brain: A cerebral organoid study. The American Journal of Psychiatry, 179(5), 375–387. https://doi.org/10.1176/appi.ajp.2021.21010095
  • Custódio, C. A., Reis, R. L., & Mano, J. F. (2014). Engineering biomolecular microenvironments for cell instructive biomaterials. Advanced Healthcare Materials, 3(6), 797–810. https://doi.org/10.1002/adhm.201300603
  • Deng, Y., Bartosovic, M., Kukanja, P., Zhang, D., Liu, Y., Su, G., Enninful, A., Bai, Z., Castelo-Branco, G., & Fan, R. (2022). Spatial-CUT&Tag: Spatially resolved chromatin modification profiling at the cellular level. Science (New York, N.Y.), 375(6581), 681–686. https://doi.org/10.1126/science.abg7216
  • Deng, Y., Bartosovic, M., Ma, S., Zhang, D., Kukanja, P., Xiao, Y., Su, G., Liu, Y., Qin, X., Rosoklija, G. B., Dwork, A. J., Mann, J. J., Xu, M. L., Halene, S., Craft, J. E., Leong, K. W., Boldrini, M., Castelo-Branco, G., & Fan, R. (2022). Spatial profiling of chromatin accessibility in mouse and human tissues. Nature, 609(7926), 375–383. https://doi.org/10.1038/s41586-022-05094-1
  • Emmert-Streib, F. (2022). Severe testing with high-dimensional omics data for enhancing biomedical scientific discovery. NPJ Systems Biology and Applications, 8(1), 40. https://doi.org/10.1038/s41540-022-00251-8
  • Floriou-Servou, A., von Ziegler, L., Stalder, L., Sturman, O., Privitera, M., Rassi, A., Cremonesi, A., Thöny, B., & Bohacek, J. (2018). Distinct proteomic, transcriptomic, and epigenetic stress responses in dorsal and ventral hippocampus. Biological Psychiatry, 84(7), 531–541. https://doi.org/10.1016/j.biopsych.2018.02.003
  • Foster, D. S., Januszyk, M., Yost, K. E., Chinta, M. S., Gulati, G. S., Nguyen, A. T., Burcham, A. R., Salhotra, A., Ransom, R. C., Henn, D., Chen, K., Mascharak, S., Tolentino, K., Titan, A. L., Jones, R. E., da Silva, O., Leavitt, W. T., Marshall, C. D., Des Jardins-Park, H. E., … Longaker, M. T. (2021). Integrated spatial multiomics reveals fibroblast fate during tissue repair. Proceedings of the National Academy of Sciences, 118(41), e2110025118. https://doi.org/10.1073/pnas.2110025118
  • Gandal, M. J., Zhang, P., Hadjimichael, E., Walker, R. L., Chen, C., Liu, S., Won, H., van Bakel, H., Varghese, M., Wang, Y., Shieh, A. W., Haney, J., Parhami, S., Belmont, J., Kim, M., Moran Losada, P., Khan, Z., Mleczko, J., Xia, Y., … Geschwind, D. H. (2018). Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder. Science (New York, N.Y.), 362(6420), eaat8127. https://doi.org/10.1126/science.aat8127
  • He, S., Bhatt, R., Brown, C., Brown, E. A., Buhr, D. L., Chantranuvatana, K., Danaher, P., Dunaway, D., Garrison, R. G., Geiss, G., Gregory, M. T., Hoang, M. L., Khafizov, R., Killingbeck, E. E., Kim, D., Kim, T. K., Kim, Y., Klock, A., Korukonda, M., … Beechem, J. M. (2022). High-plex imaging of RNA and proteins at subcellular resolution in fixed tissue by spatial molecular imaging. Nature Biotechnology, 40(12), 1794–1806. https://doi.org/10.1038/s41587-022-01483-z
  • Heim, C. M., Mayberg, H. S., Mletzko, T., Nemeroff, C. B., & Pruessner, J. C. (2013). Decreased cortical representation of genital somatosensory field after childhood sexual abuse. The American Journal of Psychiatry, 170(6), 616–623. https://doi.org/10.1176/appi.ajp.2013.12070950
  • Janesick, A., Shelansky, R., Gottscho, A. D., Wagner, F., Rouault, M., Beliakoff, G., Morrison, C. A., Oliveira, M. F., Sicherman, J. T., Kohlway, A., Abousoud, J., Drennon, T. Y., Mohabbat, S. H., 10x Development Teams & Taylor, S. E. B. (2023). High resolution mapping of the tumor microenvironment using integrated single-cell, spatial and in situ analysis. Nature Communications, 14, 8353. https://doi.org/10.1038/s41467-023-43458-x
  • Kaul, D., Schwab, S. G., Mechawar, N., & Matosin, N. (2021). How stress physically re-shapes the brain: Impact on brain cell shapes, numbers and connections in psychiatric disorders. Neuroscience and Biobehavioral Reviews, 124, 193–215. https://doi.org/10.1016/j.neubiorev.2021.01.025
  • Kaul, D., Smith, C. C., Stevens, J., Fröhlich, A. S., Binder, E. B., Mechawar, N., Schwab, S. G., & Matosin, N. (2020). Severe childhood and adulthood stress associates with neocortical layer-specific reductions of mature spines in psychiatric disorders. Neurobiology of Stress, 13, 100270. https://doi.org/10.1016/j.ynstr.2020.100270
  • Klengel, T., & Binder Elisabeth, B. (2015). Epigenetics of stress-related psychiatric disorders and gene × environment interactions. Neuron, 86(6), 1343–1357. https://doi.org/10.1016/j.neuron.2015.05.036
  • Kos, A., Lopez, J. P., Bordes, J., de Donno, C., Dine, J., Brivio, E., Karamihalev, S., Luecken, M. D., Almeida-Correa, S., Gasperoni, S., Dick, A., Miranda, L., Büttner, M., Stoffel, R., Flachskamm, C., Theis, F. J., Schmidt, M. V., & Chen, A. (2023). Early life adversity shapes social subordination and cell type–specific transcriptomic patterning in the ventral hippocampus. Science Advances, 9(48), eadj3793. https://doi.org/10.1126/sciadv.adj3793
  • Krassowski, M., Das, V., Sahu, S. K., & Misra, B. B. (2020). State of the field in multi-omics research: From computational needs to data mining and sharing. Frontiers in Genetics, 11, 610798. https://doi.org/10.3389/fgene.2020.610798
  • Leem, Y. H., Yoon, S. S., & Jo, S. A. (2020). Imipramine ameliorates depressive symptoms by blocking differential alteration of dendritic spine structure in amygdala and prefrontal cortex of chronic stress-induced mice. Biomolecules & Therapeutics, 28(3), 230–239. https://doi.org/10.4062/biomolther.2019.152
  • Li, M., Santpere, G., Imamura Kawasawa, Y., Evgrafov, O. V., Gulden, F. O., Pochareddy, S., Sunkin, S. M., Li, Z., Shin, Y., Zhu, Y., Sousa, A. M. M., Werling, D. M., Kitchen, R. R., Kang, H. J., Pletikos, M., Choi, J., Muchnik, S., Xu, X., Wang, D., … Sestan, N. (2018). Integrative functional genomic analysis of human brain development and neuropsychiatric risks. Science (New York, N.Y.), 362(6420), eaat7615. https://doi.org/10.1126/science.aat7615
  • Liu, Y., Yang, M., Deng, Y., Su, G., Enninful, A., Guo, C. C., Tebaldi, T., Zhang, D., Kim, D., Bai, Z., Norris, E., Pan, A., Li, J., Xiao, Y., Halene, S., & Fan, R. (2020). High-spatial-resolution multi-omics sequencing via deterministic barcoding in tissue. Cell, 183(6), 1665–1681.e18. https://doi.org/10.1016/j.cell.2020.10.026
  • Long, Y., Ang, K. S., Li, M., Chong, K. L. K., Sethi, R., Zhong, C., Xu, H., Ong, Z., Sachaphibulkij, K., Chen, A., Zeng, L., Fu, H., Wu, M., Lim, L. H. K., Liu, L., & Chen, J. (2023). Spatially informed clustering, integration, and deconvolution of spatial transcriptomics with GraphST. Nature Communications, 14(1), 1155. https://doi.org/10.1038/s41467-023-36796-3
  • Lopez, J. P., Brivio, E., Santambrogio, A., De Donno, C., Kos, A., Peters, M., Rost, N., Czamara, D., Brückl, T. M., Roeh, S., Pöhlmann, M. L., Engelhardt, C., Ressle, A., Stoffel, R., Tontsch, A., Villamizar, J. M., Reincke, M., Riester, A., Sbiera, S., … Chen, A. (2021). Single-cell molecular profiling of all three components of the HPA axis reveals adrenal ABCB1 as a regulator of stress adaptation. Science Advances, 7(5):eabe4497. https://doi.org/10.1126/sciadv.abe4497
  • Matosin, N., Arloth, J., Czamara, D., Edmond, K. Z., Maitra, M., Fröhlich, A. S., Martinelli, S., Kaul, D., Bartlett, R., Curry, A. R., Gassen, N. C., Hafner, K., Müller, N. S., Worf, K., Rehawi, G., Nagy, C., Halldorsdottir, T., Cruceanu, C., Gagliardi, M., … Binder, E. B. (2023). Associations of psychiatric disease and ageing with FKBP5 expression converge on superficial layer neurons of the neocortex. Acta Neuropathologica, 145(4), 439–459. https://doi.org/10.1007/s00401-023-02541-9
  • Matosin, N., Cruceanu, C., & Binder, E. B. (2017). Preclinical and clinical evidence of DNA methylation changes in response to trauma and chronic stress. Chronic Stress (Thousand Oaks, Calif.), 1,2470547017710764. https://doi.org/10.1177/2470547017710764
  • Matosin, N., Halldorsdottir, T., & Binder, E. B. (2018). Understanding the molecular mechanisms underpinning gene by environment interactions in psychiatric disorders: The FKBP5 model. Biological Psychiatry, 83(10), 821–830. https://doi.org/10.1016/j.biopsych.2018.01.021
  • Maynard, K. R., Collado-Torres, L., Weber, L. M., Uytingco, C., Barry, B. K., Williams, S. R., Catallini, J. L., Tran, M. N., Besich, Z., Tippani, M., Chew, J., Yin, Y., Kleinman, J. E., Hyde, T. M., Rao, N., Hicks, S. C., Martinowich, K., & Jaffe, A. E. (2021). Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex. Nature Neuroscience, 24(3), 425–436. https://doi.org/10.1038/s41593-020-00787-0
  • Merritt, C. R., Ong, G. T., Church, S. E., Barker, K., Danaher, P., Geiss, G., Hoang, M., Jung, J., Liang, Y., McKay-Fleisch, J., Nguyen, K., Norgaard, Z., Sorg, K., Sprague, I., Warren, C., Warren, S., Webster, P. J., Zhou, Z., Zollinger, D. R., … Beechem, J. M. (2020). Multiplex digital spatial profiling of proteins and RNA in fixed tissue. Nature Biotechnology, 38(5), 586–599. https://doi.org/10.1038/s41587-020-0472-9
  • Method of the Year 2020: spatially resolved transcriptomics. (2021). Nature Methods, 18(1), 1. https://doi.org/10.1038/s41592-020-01042-x
  • Miranda, L., Bordes, J., Gasperoni, S., & Lopez, J. P. (2023). Increasing resolution in stress neurobiology: from single cells to complex group behaviors. Stress (Amsterdam, Netherlands), 26(1), 2186141. https://doi.org/10.1080/10253890.2023.2186141
  • Moses, L., & Pachter, L. (2022). Museum of spatial transcriptomics. Nature Methods, 19(5), 534–546. https://doi.org/10.1038/s41592-022-01409-2
  • Navarro, J. F., Croteau, D. L., Jurek, A., Andrusivova, Z., Yang, B., Wang, Y., Ogedegbe, B., Riaz, T., Støen, M., Desler, C., Rasmussen, L. J., Tønjum, T., Galas, M.-C., Lundeberg, J., & Bohr, V. A. (2020). Spatial transcriptomics reveals genes associated with dysregulated mitochondrial functions and stress signaling in Alzheimer disease. iScience, 23(10), 101556. https://doi.org/10.1016/j.isci.2020.101556
  • Negele, A., Kaufhold, J., Kallenbach, L., & Leuzinger-Bohleber, M. (2015). Childhood trauma and its relation to chronic depression in adulthood. Depression Research and Treatment, 2015, 650804. https://doi.org/10.1155/2015/650804
  • Patel, D., Anilkumar, S., Chattarji, S., & Buwalda, B. (2018). Repeated social stress leads to contrasting patterns of structural plasticity in the amygdala and hippocampus. Behavioural Brain Research, 347, 314–324. https://doi.org/10.1016/j.bbr.2018.03.034
  • Penner-Goeke, S., & Binder, E. B. (2019). Epigenetics and depression. Dialogues in Clinical Neuroscience, 21(4), 397–405. https://doi.org/10.31887/DCNS.2019.21.4/ebinder
  • Perng, W., & Aslibekyan, S. (2020). Find the needle in the Haystack, then find it again: Replication and validation in the ‘Omics Era’. Metabolites, 10(7), 286. https://doi.org/10.3390/metabo10070286
  • Porterfield, A. (2022). Retrieved from https://www.10xgenomics.com/blog/expanding-the-spectrum-of-innovation-technologies-to-watch-in-2022
  • Ravi, V. M., Will, P., Kueckelhaus, J., Sun, N., Joseph, K., Salié, H., Vollmer, L., Kuliesiute, U., von Ehr, J., Benotmane, J. K., Neidert, N., Follo, M., Scherer, F., Goeldner, J. M., Behringer, S. P., Franco, P., Khiat, M., Zhang, J., Hofmann, U. G., … Heiland, D. H. (2022). Spatially resolved multi-omics deciphers bidirectional tumor-host interdependence in glioblastoma. Cancer Cell, 40(6), 639–655.e13. https://doi.org/10.1016/j.ccell.2022.05.009
  • Saka, S. K., Wang, Y., Kishi, J. Y., Zhu, A., Zeng, Y., Xie, W., Kirli, K., Yapp, C., Cicconet, M., Beliveau, B. J., Lapan, S. W., Yin, S., Lin, M., Boyden, E. S., Kaeser, P. S., Pihan, G., Church, G. M., & Yin, P. (2019). Immuno-SABER enables highly multiplexed and amplified protein imaging in tissues. Nature Biotechnology, 37(9), 1080–1090. https://doi.org/10.1038/s41587-019-0207-y
  • Sandi, C., & Haller, J. (2015). Stress and the social brain: behavioural effects and neurobiological mechanisms. Nature Reviews. Neuroscience, 16(5), 290–304. https://doi.org/10.1038/nrn3918
  • Schoenfeld, T. J., McCausland, H. C., Morris, H. D., Padmanaban, V., & Cameron, H. A. (2017). Stress and loss of adult neurogenesis differentially reduce hippocampal volume. Biological Psychiatry, 82(12), 914–923. https://doi.org/10.1016/j.biopsych.2017.05.013
  • Seah, C., Breen, M. S., Rusielewicz, T., Bader, H. N., Xu, C., Hunter, C. J., McCarthy, B., Deans, P. J. M., Chattopadhyay, M., Goldberg, J., Desarnaud, F., Makotkine, I., Flory, J. D., Bierer, L. M., Staniskyte, M., Noggle, S. A., Huckins, L. M., Paull, D., Brennand, K. J., & Yehuda, R. (2022). Modeling gene x environment interactions in PTSD using human neurons reveals diagnosis-specific glucocorticoid-induced gene expression. Nature Neuroscience, 25(11), 1434–1445. https://doi.org/10.1038/s41593-022-01161-y
  • Shepherd, G. M. G., Stepanyants, A., Bureau, I., Chklovskii, D., & Svoboda, K. (2005). Geometric and functional organisation of cortical circuits. Nature Neuroscience, 8(6), 782–790. https://doi.org/10.1038/nn1447
  • Ståhl, P. L., Salmén, F., Vickovic, S., Lundmark, A., Navarro, J. F., Magnusson, J., Giacomello, S., Asp, M., Westholm, J. O., Huss, M., Mollbrink, A., Linnarsson, S., Codeluppi, S., Borg, Å., Pontén, F., Costea, P. I., Sahlén, P., Mulder, J., Bergmann, O., Lundeberg, J., & Frisén, J. (2016). Visualisation and analysis of gene expression in tissue sections by spatial transcriptomics. Science (New York, N.Y.), 353(6294), 78–82. https://doi.org/10.1126/science.aaf2403
  • Stickels, R. R., Murray, E., Kumar, P., Li, J., Marshall, J. L., Di Bella, D. J., Arlotta, P., Macosko, E. Z., & Chen, F. (2021). Highly sensitive spatial transcriptomics at near-cellular resolution with Slide-seqV2. Nature Biotechnology, 39(3), 313–319. https://doi.org/10.1038/s41587-020-0739-1
  • Stockmeier, C. A., & Rajkowska, G. (2004). Cellular abnormalities in depression: evidence from postmortem brain tissue. Dialogues in Clinical Neuroscience, 6(2), 185–197. https://doi.org/10.31887/DCNS.2004.6.2/cstockmeier
  • Tanti, A., Belliveau, C., Nagy, C., Maitra, M., Denux, F., Perlman, K., Chen, F., Mpai, R., Canonne, C., Théberge, S., McFarquhar, A., Davoli, M. A., Belzung, C., Turecki, G., & Mechawar, N. (2022). Child abuse associates with increased recruitment of perineuronal nets in the ventromedial prefrontal cortex: A possible implication of oligodendrocyte progenitor cells. Molecular Psychiatry, 27(3), 1552–1561. https://doi.org/10.1038/s41380-021-01372-y
  • Tomoda, A., Polcari, A., Anderson, C. M., & Teicher, M. H. (2012). Reduced visual cortex gray matter volume and thickness in young adults who witnessed domestic violence during childhood. PloS One, 7(12), e52528. https://doi.org/10.1371/journal.pone.0052528
  • Van de Sande, B., Lee, J. S., Mutasa-Gottgens, E., Naughton, B., Bacon, W., Manning, J., Wang, Y., Pollard, J., Mendez, M., Hill, J., Kumar, N., Cao, X., Chen, X., Khaladkar, M., Wen, J., Leach, A., & Ferran, E. (2023). Applications of single-cell RNA sequencing in drug discovery and development. Nature Reviews. Drug Discovery, 22(6), 496–520. https://doi.org/10.1038/s41573-023-00688-4
  • Vandereyken, K., Sifrim, A., Thienpont, B., & Voet, T. (2023). Methods and applications for single-cell and spatial multi-omics. Nature Reviews. Genetics, 24(8), 494–515. https://doi.org/10.1038/s41576-023-00580-2
  • Vicari, M., Mirzazadeh, R., Nilsson, A., Shariatgorji, R., Bjärterot, P., Larsson, L., Lee, H., Nilsson, M., Foyer, J., Ekvall, M., Czarnewski, P., Zhang, X., Svenningsson, P., Käll, L., Andrén, P. E., & Lundeberg, J. (2023). Spatial multimodal analysis of transcriptomes and metabolomes in tissues. Nature Biotechnology. https://doi.org/10.1038/s41587-023-01937-y
  • Vizgen. (2023). MERSCOPE® platform for spatial transcriptomics. Retrieved from https://vizgen.com/products/#:∼:text=ACCESS%20DATA%20RELEASE-,MERSCOPE%20Instrument,box%20and%20a%20processing%20computer
  • von Dawans, B., Strojny, J., & Domes, G. (2021). The effects of acute stress and stress hormones on social cognition and behavior: Current state of research and future directions. Neuroscience and Biobehavioral Reviews, 121, 75–88. https://doi.org/10.1016/j.neubiorev.2020.11.026
  • Warhaftig, G., Almeida, D., & Turecki, G. (2023). Early life adversity across different cell- types in the brain. Neuroscience and Biobehavioral Reviews, 148, 105113. https://doi.org/10.1016/j.neubiorev.2023.105113
  • x Genomics. (2023). Visium spatial gene expression: 10x genomics. Retrieved from https://www.10xgenomics.com/products/spatial-gene-expression
  • Xu, Y., & McCord, R. P. (2022). Diagonal integration of multimodal single-cell data: Potential pitfalls and paths forward. Nature Communications, 13(1), 3505. https://doi.org/10.1038/s41467-022-31104-x
  • Zhang, D., Deng, Y., Kukanja, P., Agirre, E., Bartosovic, M., Dong, M., Ma, C., Ma, S., Su, G., Bao, S., Liu, Y., Xiao, Y., Rosoklija, G. B., Dwork, A. J., Mann, J. J., Leong, K. W., Boldrini, M., Wang, L., Haeussler, M., … Fan, R. (2023). Spatial epigenome–transcriptome co-profiling of mammalian tissues. Nature, 616(7955), 113–122. https://doi.org/10.1038/s41586-023-05795-1
  • Zhu, X., Xu, T., Peng, C., & Wu, S. (2021). Advances in MALDI mass spectrometry imaging single cell and tissues. Frontiers in Chemistry, 9, 782432. https://doi.org/10.3389/fchem.2021.782432