Citation: | Zhuxia Li, Guangdun Peng. Spatial transcriptomics: new dimension of understanding biological complexity[J]. Biophysics Reports, 2022, 8(3): 119-135. doi: 10.52601/bpr.2021.210037 |
Alturkistani HA, Tashkandi FM, Mohammedsaleh ZM (2015) Histological stains: a literature review and case study. Glob J Health Sci 8(3): 72−79 doi: 10.5539/gjhs.v8n3p72
|
Bandyopadhyay U, Fenton WA, Horwich AL, Nagy M (2014) Production of RNA for transcriptomic analysis from mouse spinal cord motor neuron cell bodies by laser capture microdissection. J Vis Exp 83: e51168. https://doi.org/10.3791/51168
|
Battich N, Stoeger T, Pelkmans L (2013) Image-based transcriptomics in thousands of single human cells at single-molecule resolution. Nat Methods 10(11): 1127−1133 doi: 10.1038/nmeth.2657
|
Beliveau BJ, Joyce EF, Apostolopoulos N, Yilmaz F, Fonseka CY, McCole RB, Chang Y, Li JB, Senaratne TN, Williams BR, Rouillard JM, Wu CT (2012) Versatile design and synthesis platform for visualizing genomes with Oligopaint FISH probes. Proc Natl Acad Sci USA 109(52): 21301−21306 doi: 10.1073/pnas.1213818110
|
Brown VM, Ossadtchi A, Khan AH, Cherry SR, Leahy RM, Smith DJ (2002) High-throughput imaging of brain gene expression. Genome Res 12: 244-254
|
Cabili MN, Dunagin MC, McClanahan PD, Biaesch A, Padovan-Merhar O, Regev A, Rinn JL, Raj A (2015) Localization and abundance analysis of human lncRNAs at single-cell and single-molecule resolution. Genome Biol 16(1): 20. https://doi.org/10.1186/s13059-015-0586-4
|
Cable DM, Murray E, Zou LS, Goeva A, Macosko EZ, Chen F, Irizarry RA (2021) Robust decomposition of cell type mixtures in spatial transcriptomics. Nat Biotechnol. https://doi.org/10.1038/s41587-021-00830-w
|
Chen A, Liao S, Cheng M, Ma K, Wu L, Lai Y, Yang J, Li W, Xu J, Hao S, Lu H, Chen X, Liu X, Huang X, Lin F, Tang X, Li Z, Hong Y, Fu D, Jiang Y, Peng J, Liu S, Shen M, Liu C, Li Q, Wang Z, Wang Z, Huang X, Yuan Y, Volpe G, Ward C, Muñoz-Cánoves P, Thiery JP, Zhao F, Li M, Kuang H, Wang O, Lu H, Wang B, Ni M, Zhang W, Mu F, Yin Y, Yang H, Lisby M, Cornall RJ, Uhlen M, Esteban MA, Li Y, Liu L, Xu X, Wang J (2021) Large field of view-spatially resolved transcriptomics at nanoscale resolution. bioRxiv. https://doi.org/10.1101/2021.01.17.427004
|
Chen H, Murray E, Laumas A, Li J, Nie X, Hotaling J, Guo J, Cairns BR, Macosko EZ, Cheng CY, Chen F (2020) Dissecting mammalian spermatogenesis using spatial transcriptomics. bioRxiv. https://doi.org/10.1101/2020.10.17.343335
|
Chen J, Suo S, Tam PP, Han JJ, Peng G, Jing N (2017) Spatial transcriptomic analysis of cryosectioned tissue samples with Geo-seq. Nat Protoc 12(3): 566−580 doi: 10.1038/nprot.2017.003
|
Chen KH, Boettiger AN, Moffitt JR, Wang S, Zhuang X (2015) RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 348(6233): aaa6090. https://doi.org/10.1126/science.aaa6090
|
Chen X, Sun YC, Zhan H, Kebschull JM, Fischer S, Matho K, Huang ZJ, Gillis J, Zador AM (2019) High-Throughput mapping of long-range neuronal projection using in situ sequencing. Cell 179(3): 772−786 doi: 10.1016/j.cell.2019.09.023
|
Cho CS, Xi J, Si Y, Park SR, Hsu JE, Kim M, Jun G, Kang HM, Lee JH (2021) Microscopic examination of spatial transcriptome using Seq-Scope. Cell 184(13): 3559−3572 doi: 10.1016/j.cell.2021.05.010
|
Codeluppi S, Borm LE, Zeisel A, La Manno G, van Lunteren JA, Svensson CI, Linnarsson S (2018) Spatial organization of the somatosensory cortex revealed by osmFISH. Nat Methods 15(11): 932−935 doi: 10.1038/s41592-018-0175-z
|
Datta S, Malhotra L, Dickerson R, Chaffee S, Sen CK, Roy S (2015) Laser capture microdissection: big data from small samples. Histol Histopathol 30(11): 1255−1269
|
Deng Y, Bartosovic M, Ma S, Zhang D, Liu Y, Qin X, Su G, Xu ML, Halene S, Craft JE, Castelo-Branco G, Fan R (2021a) Spatial-ATAC-seq: spatially resolved chromatin accessibility profiling of tissues at genome scale and cellular level. bioRxiv. https://doi.org/10.1101/2021.06.06.447244
|
Deng Y, Zhang D, Liu Y, Su G, Enninful A, Bai Z, Fan R (2021b) Spatial epigenome sequencing at tissue scale and cellular level. bioRxiv. https://doi.org/10.1101/2021.03.11.434985
|
Dou J, Liang S, Mohanty V, Cheng X, Kim S, Choi J, Li Y, Rezvani K, Chen R, Chen K (2020) Unbiased integration of single cell multi-omics data. bioRxiv. https://doi.org/10.1101/2020.12.11.422014
|
Dries R, Zhu Q, Dong R, Linus Eng C-H, Li H, Liu K, Fu Y, Zhao T, Sarkar A, Bao F, George RE, Pierson N, Cai L, Yuan G-C (2021) Giotto, a toolbox for integrative analysis and visualization of spatial expression data. Genome Biol : 22(1): 78. https://doi.org/10.1186/s13059-021-02286-2
|
Elosua-Bayes M, Nieto P, Mereu E, Gut I, Heyn H (2021) SPOTlight: seeded NMF regression to deconvolute spatial transcriptomics spots with single-cell transcriptomes. Nucleic Acids Res 49: e50. https://doi.org/10.1093/nar/gkab043
|
Emmert-Buck MR, Bonner RF, Smith PD, Chuaqui RF, Zhuang Z, Goldstein SR, Weiss RA, Liotta LA (1996) Laser capture microdissection. science 274(5289): 998−1001 doi: 10.1126/science.274.5289.998
|
Femino AM, Fay SF, Fogarty K, Singer RH (1998) Visualization of single RNA transcripts in situ. science 280(5363): 585−590 doi: 10.1126/science.280.5363.585
|
Francoz E, Ranocha P, Pernot C, Le Ru A, Pacquit V, Dunand C, Burlat V (2016) Complementarity of medium-throughput in situ RNA hybridization and tissue-specific transcriptomics: case study of Arabidopsis seed development kinetics. Sci Rep 6: 24644. https://doi.org/10.1038/srep24644
|
Hou X, Yang Y, Li P, Zeng Z, Hu W, Zhe R, Liu X, Tang D, Ou M, Dai Y (2021) Integrating spatial transcriptomics and single-cell RNA-seq reveals the gene expression profling of the human embryonic liver. Front Cell Dev Biol 9: 652408. https://doi.org/10.3389/fcell.2021.652408
|
Hu J, Schroeder A, Coleman K, Chen C, Auerbach BJ, Li M (2021) Statistical and machine learning methods for spatially resolved transcriptomics with histology. Comput Struct Biotechnol J 19: 3829−3841 doi: 10.1016/j.csbj.2021.06.052
|
Hu KH, Eichorst JP, McGinnis CS, Patterson DM, Chow ED, Kersten K, Jameson SC, Gartner ZJ, Rao AA, Krummel MF (2020) ZipSeq: barcoding for real-time mapping of single cell transcriptomes. Nat Methods 17: 833−843 doi: 10.1038/s41592-020-0880-2
|
Jemt A, Salmen F, Lundmark A, Mollbrink A, Fernandez Navarro J, Stahl PL, Yucel-Lindberg T, Lundeberg J (2016) An automated approach to prepare tissue-derived spatially barcoded RNA-sequencing libraries. Sci Rep 6: 37137. https://doi.org/10.1038/srep37137
|
Junker JP, Noel ES, Guryev V, Peterson KA, Shah G, Huisken J, McMahon AP, Berezikov E, Bakkers J, van Oudenaarden A (2014) Genome-wide RNA tomography in the zebrafish embryo. Cell 159(3): 662−675 doi: 10.1016/j.cell.2014.09.038
|
Ke R, Mignardi M, Pacureanu A, Svedlund J, Botling J, Wahlby C, Nilsson M (2013) In situ sequencing for RNA analysis in preserved tissue and cells. Nat Methods 10(9): 857−860 doi: 10.1038/nmeth.2563
|
Kueckelhaus J, von Ehr J, Ravi VM, Will P, Joseph K, Beck J, Hofmann UG, Delev D, Schnell O, Heiland DH (2020) Inferring spatially transient gene expression pattern from spatial transcriptomic studies. bioRxiv. https://doi.org/10.1101/2020.10.20.346544
|
Lee JH, Daugharthy ER, Scheiman J, Kalhor R, Yang JL, Ferrante TC, Terry R, Jeanty SS, Li C, Amamoto R, Peters DT, Turczyk BM, Marblestone AH, Inverso SA, Bernard A, Mali P, Rios X, Aach J, Church GM (2014) Highly multiplexed subcellular RNA sequencing in situ. Science 343(6177): 1360−1363 doi: 10.1126/science.1250212
|
Liu Y, Yang M, Deng Y, Su G, Enninful A, Guo CC, 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 doi: 10.1016/j.cell.2020.10.026
|
Liu S, Punthambaker S, Iyer EPR, Ferrante T, Goodwin D, Fürth D, Pawlowski AC, Jindal K, Tam JM, Mifflin L, Alon S, Sinha A, Wassie AT, Chen F, Cheng A, Willocq V, Meyer K, Ling K-H, Camplisson CK, Kohman RE, Aach J, Lee JH, Yankner BA, Boyden ES, Church GM (2021) Barcoded oligonucleotides ligated on RNA amplified for multiplexed and parallel in situ analyses. Nucleic Acids Res 49: e58. https://doi.org/10.1093/nar/gkab120
|
Lohoff T, Ghazanfar S, Missarova A, Koulena N, Pierson N, Griffiths JA, Bardot ES, Eng CL, Tyser R, Argelaguet R, Guibentif C, Srinivas S, Briscoe J, Simons BD, Hadjantonakis AK, Göttgens B, Reik W, Nichols J, Cai L, Marioni JC (2021) Integration of spatial and single-cell transcriptomic data elucidates mouse organogenesis. Nat Biotechnol. https://doi.org/10.1038/s41587-021-01006-2
|
Longo SK, Guo MG, Ji AL, Khavari PA (2021) Integrating single-cell and spatial transcriptomics to elucidate intercellular tissue dynamics. Nat Rev Genet 22(10): 627−644 doi: 10.1038/s41576-021-00370-8
|
Lovatt D, Ruble BK, Lee J, Dueck H, Kim TK, Fisher S, Francis C, Spaethling JM, Wolf JA, Grady MS, Ulyanova AV, Yeldell SB, Griepenburg JC, Buckley PT, Kim J, Sul JY, Dmochowski IJ, Eberwine J (2014) Transcriptome in vivo analysis (TIVA) of spatially defined single cells in live tissue. Nat Methods 11(2): 190−196 doi: 10.1038/nmeth.2804
|
Lubeck E, Coskun AF, Zhiyentayev T, Ahmad M, Cai L (2014) Single-cell in situ RNA profiling by sequential hybridization. Nat Methods 11(4): 360−361 doi: 10.1038/nmeth.2892
|
Lynch AS, Briggs D, Hope IA (1995) Developmental expression pattern screen for genes predicted in the C. elegans genome sequencing project. Nat Genet 11(3): 309−313 doi: 10.1038/ng1195-309
|
Maynard KR, Collado-Torres L, Weber LM, Uytingco C, Barry BK, Williams SR, Catallini JL, 2nd, Tran MN, Besich Z, Tippani M, Chew J, Yin Y, Kleinman JE, Hyde TM, Rao N, Hicks SC, Martinowich K, Jaffe AE (2021) Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex. Nat Neurosci 24(3): 425−436 doi: 10.1038/s41593-020-00787-0
|
Medaglia C, Giladi A, Stoler-Barak L, De Giovanni M, Salame TM, Biram A, David E, Li H, Iannacone M, Shulman Z, Amit I (2017) Spatial reconstruction of immune niches by combining photoactivatable reporters and scRNA-seq. Science 358(6370): 1622−1626 doi: 10.1126/science.aao4277
|
Merritt CR, Ong GT, Church S, Barker K, Geiss G, Hoang M, Jung J, Liang Y, McKay-Fleisch J, Nguyen K, Sorg K, Sprague I, Warren C, Warren S, Zhou Z, Zollinger DR, Dunaway DL, Mills GB, Beechem JM (2019) High multiplex, digital spatial profiling of proteins and RNA in fixed tissue using genomic detection methods. bioRxiv. https://doi.org/10.1101/559021
|
Moffitt JR, Hao J, Wang G, Chen KH, Babcock HP, Zhuang X (2016) High-throughput single-cell gene-expression profiling with multiplexed error-robust fluorescence in situ hybridization. Proc Natl Acad Sci USA 113(39): 11046−11051 doi: 10.1073/pnas.1612826113
|
Murakami H, Liotta L, Star RA (2000) IF-LCM: laser capture microdissection of immunofluorescently defined cells for mRNA analysis rapid communication. Kidney Int 58(3): 1346−1353 doi: 10.1046/j.1523-1755.2000.00295.x
|
Nagasawa S, Kuze Y, Maeda I, Kojima Y, Motoyoshi A, Onishi T, Iwatani T, Yokoe T, Koike J, Chosokabe M, Kubota M, Seino H, Suzuki A, Seki M, Tsuchihara K, Inoue E, Tsugawa K, Ohta T, Suzuki Y (2021) Genomic profiling reveals heterogeneous populations of ductal carcinoma in situ of the breast. Commun Biol 4(1): 438. https://doi.org/10.1038/s42003-021-01959-9
|
Navarro JF, Sjostrand J, Salmen F, Lundeberg J, Stahl PL (2017) ST Pipeline: an automated pipeline for spatial mapping of unique transcripts. Bioinformatics 33: 2591−2593 doi: 10.1093/bioinformatics/btx211
|
Nguyen HQ, Chattoraj S, Castillo D, Nguyen SC, Nir G, Lioutas A, Hershberg EA, Martins NMC, Reginato PL, Hannan M, Beliveau BJ, Church GM, Daugharthy ER, Marti-Renom MA, Wu CT (2020) 3D mapping and accelerated super-resolution imaging of the human genome using in situ sequencing. Nat Methods 17(8): 822−832 doi: 10.1038/s41592-020-0890-0
|
Padovan-Merhar O, Nair GP, Biaesch AG, Mayer A, Scarfone S, Foley SW, Wu AR, Churchman LS, Singh A, Raj A (2015) Single mammalian cells compensate for differences in cellular volume and DNA copy number through independent global transcriptional mechanisms. Mol Cell 58(2): 339−352 doi: 10.1016/j.molcel.2015.03.005
|
Peng G, Suo S, Chen J, Chen W, Liu C, Yu F, Wang R, Chen S, Sun N, Cui G, Song L, Tam PP, Han JD, Jing N (2016) Spatial transcriptome for the molecular annotation of lineage fates and cell identity in mid-gastrula mouse embryo. Dev Cell 36(6): 681−697 doi: 10.1016/j.devcel.2016.02.020
|
Peng G, Suo S, Cui G, Yu F, Wang R, Chen J, Chen S, Liu Z, Chen G, Qian Y, Tam P, Han JJ, Jing N (2019) Molecular architecture of lineage allocation and tissue organization in early mouse embryo. Nature 572(7770): 528−532 doi: 10.1038/s41586-019-1469-8
|
Pham D, Tan X, Xu J, Grice LF, Lam PY, Raghubar A, Vukovic J, Ruitenberg MJ, Nguyen Q (2020) stLearn: integrating spatial location, tissue morphology and gene expression to find cell types, cell-cell interactions and spatial trajectories within undissociated tissues. bioRxiv. https://doi.org/10.1101/2020.05.31.125658
|
Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S (2008) Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5(10): 877−879 doi: 10.1038/nmeth.1253
|
Ren X, Zhong G, Zhang Q, Zhang L, Sun Y, Zhang Z (2020) Reconstruction of cell spatial organization based on ligand-receptor mediated self-assembly. bioRxiv. https://doi.org/10.1101/2020.02.13.948521
|
Rodriques SG, Stickels RR, Goeva A, Martin CA, Murray E, Vanderburg CR, Welch J, Chen LM, Chen F, Macosko EZ (2019) Slide-seq: a scalable technology for measuring genome-wide expression at high spatial resolution. Science 363(6434): 1463−1467 doi: 10.1126/science.aaw1219
|
Shah S, Takei Y, Zhou W, Lubeck E, Yun J, Eng CL, Koulena N, Cronin C, Karp C, Liaw EJ, Amin M, Cai L (2018) Dynamics and spatial genomics of the nascent transcriptome by intron seqFISH. Cell 174(2): 363−376 doi: 10.1016/j.cell.2018.05.035
|
Shaffer SM, Dunagin MC, Torborg SR, Torre EA, Emert B, Krepler C, Beqiri M, Sproesser K, Brafford PA, Xiao M, Eggan E, Anastopoulos IN, Vargas-Garcia CA, Singh A, Nathanson KL, Herlyn M, Raj A (2017) Rare cell variability and drug-induced reprogramming as a mode of cancer drug resistance. Nature 546: 431−435 doi: 10.1038/nature22794
|
Skarnes WC, Moss JE, Hurtley SM, Beddington RS (1995) Capturing genes encoding membrane and secreted proteins important for mouse development. Proc Natl Acad Sci USA 92(14): 6592−6596 doi: 10.1073/pnas.92.14.6592
|
Ståhl PL, Salmén F, Vickovic S, Lundmark A, Navarro J F, Magnusson J, Giacomello S, Asp M, Westholm JO, Huss M, Mollbrink A, Linnarsson S, Codeluppi S, Borg Å, Pontén F, Costea P, Sahlén P, Mulder J, Bergmann O, Lundeberg J, Frisén J (2016) visualization and analysis of gene expression in tissue sections by spatial transcriptomics. Science 353(6294): 78−82 doi: 10.1126/science.aaf2403
|
Stoltzfus CR, Filipek J, Gern BH, Olin BE, Leal JM, Wu Y, Lyons-Cohen MR, Huang JY, Paz-Stoltzfus CL, Plumlee CR, Pöschinger T, Urdahl KB, Perro M, Gerner MY (2020) CytoMAP: a spatial analysis toolbox reveals features of myeloid cell organization in lymphoid tissues. Cell Rep 31(3): 107523. https://doi.org/10.1016/j.celrep.2020.107523
|
Sountoulidis A, Liontos A, Nguyen HP, Firsova AB, Fysikopoulos A, Qian X, Seeger W, Sundström E, Nilsson M, Samakovlis C (2020) SCRINSHOT enables spatial mapping of cell states in tissue sections with single-cell resolution. PLoS Biol 18(11): e3000675. https://doi.org/10.1371/journal.pbio.3000675
|
Su G, Qin X, Enninful A, Bai Z, Deng Y, Liu Y, Fan R (2021) Spatial multi-omics sequencing for fixed tissue via DBiT-seq. STAR Protoc 2(2): 100532. https://doi.org/10.1016/j.xpro.2021.100532
|
Su JH, Zheng P, Kinrot SS, Bintu B, Zhuang X (2020) Genome-scale imaging of the 3D organization and transcriptional activity of chromatin. Cell 182(6): 1641−1659 doi: 10.1016/j.cell.2020.07.032
|
Sun S, Zhu J, Zhou X (2020) Statistical analysis of spatial expression patterns for spatially resolved transcriptomic studies. Nat Methods 17(2): 193−200 doi: 10.1038/s41592-019-0701-7
|
Svensson V, Teichmann SA, Stegle O (2018) SpatialDE: identification of spatially variable genes. Nat Methods 15(5): 343−346 doi: 10.1038/nmeth.4636
|
Tran M, Yoon S, Teoh M, Andersen S, Lam PY, Purdue P, Raghubar A, Hanson SJ, Devitt K, Jones K, Walters S, Tuong ZK, Kulasinghe A, Monkman J, Soyer HP, Frazer I, Nguyen Q (2021) Spatial analysis of ligand-receptor interaction in skin cancer at genome-wide and single-cell resolution. bioRxiv. https:// doi.org/10.1101/2020.09.10.290833
|
Trcek T, Lionnet T, Shroff H, Lehmann R (2017) mRNA quantification using single-molecule FISH in Drosophila embryos. Nat Protoc 12(7): 1326−1348 doi: 10.1038/nprot.2017.030
|
van den Brink SC, Alemany A, van Batenburg V, Moris N, Blotenburg M, Vivié J, Baillie-Johnson P, Nichols J, Sonnen KF, Martinez Arias A, van Oudenaarden A (2020) Single-cell and spatial transcriptomics reveal somitogenesis in gastruloids. Nature 582: 405−409 doi: 10.1038/s41586-020-2024-3
|
Vickovic S, Eraslan G, Salmen F, Klughammer J, Stenbeck L, Schapiro D, Aijo T, Bonneau R, Bergenstrahle L, Navarro JF, Gould J, Griffin GK, Borg A, Ronaghi M, Frisen J, Lundeberg J, Regev A, Stahl PL (2019) High-definition spatial transcriptomics for in situ tissue profiling. Nat Methods 16(10): 987−990 doi: 10.1038/s41592-019-0548-y
|
Vickovic S, Lötstedt B, Klughammer J, Segerstolpe Å, Rozenblatt-Rosen O, Regev A (2020) SM-Omics: an automated platform for high-throughput spatial multi-omics. bioRxiv. https://doi.org/10.1101/2020.10.14.338418
|
Wang F, Flanagan J, Su N, Wang LC, Bui S, Nielson A, Wu X, Vo HT, Ma XJ, Luo Y (2012) RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues. J Mol Diagn 14(1): 22−29 doi: 10.1016/j.jmoldx.2011.08.002
|
Wang G, Moffitt JR, Zhuang X (2018a) Multiplexed imaging of high-density libraries of RNAs with MERFISH and expansion microscopy. Sci Rep 8(1): 4847. https://doi.org/10.1038/s41598-018-22297-7
|
Wang X, Allen WE, Wright MA, Sylwestrak EL, Samusik N, Vesuna S, Evans K, Liu C, Ramakrishnan C, Liu J, Nolan GP, Bava FA, Deisseroth K (2018b) Three-dimensional intact-tissue sequencing of single-cell transcriptional states. Science 361(6400): eaat5691. https://doi.org/10.1126/science.aat5691
|
Xia C, Babcock HP, Moffitt JR, Zhuang X (2019) Multiplexed detection of RNA using MERFISH and branched DNA amplification. Sci Rep 9(1): 7721. https://doi.org/10.1038/s41598-019-43943-8
|
Zhang L, Mao SQ, Yao ML, Chao N, Yang Y, Ni Y, Song T, Liu Z, Yang Y, Li W (2021) Spatial transcriptome sequencing revealed spatial trajectory in the non-small cell lung cancer. bioRxiv. https://doi.org/10.1101/2021.04.26.441394
|