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Cited by 29Single-cell and spatial transcriptomicsBioinformatics and Genomic NetworksGenetics, Aging, and Longevity in Model Organisms

Spatiotemporal multi-omics: exploring molecular landscapes in aging and regenerative medicine

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Chu, Liu-Xi, Wang, Wen-Jia, Gu, Xin-Pei, Wu, Ping, Gao, Chen, Zhang, Quan, Wu, Jia, Jiang, Da-Wei +13 more·2024·Military Medical Research
DOI 10.1186/s40779-024-00537-4PMC PMC11129507
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Abstract

Aging and regeneration represent complex biological phenomena that have long captivated the scientific community. To fully comprehend these processes, it is essential to investigate molecular dynamics through a lens that encompasses both spatial and temporal dimensions. Conventional omics methodologies, such as genomics and transcriptomics, have been instrumental in identifying critical molecular facets of aging and regeneration. However, these methods are somewhat limited, constrained by their spatial resolution and their lack of capacity to dynamically represent tissue alterations. The advent of emerging spatiotemporal multi-omics approaches, encompassing transcriptomics, proteomics, metabolomics, and epigenomics, furnishes comprehensive insights into these intricate molecular dynamics. These sophisticated techniques facilitate accurate delineation of molecular patterns across an array of cells, tissues, and organs, thereby offering an in-depth understanding of the fundamental mechanisms at play. This review meticulously examines the significance of spatiotemporal multi-omics in the realms of aging and regeneration research. It underscores how these methodologies augment our comprehension of molecular dynamics, cellular interactions, and signaling pathways. Initially, the review delineates the foundational principles underpinning these methods, followed by an evaluation of their recent applications within the field. The review ultimately concludes by addressing the prevailing challenges and projecting future advancements in the field. Indubitably, spatiotemporal multi-omics are instrumental in deciphering the complexities inherent in aging and regeneration, thus charting a course toward potential therapeutic innovations.

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  1. [1]Khosla S Farr JN Tchkonia T Kirkland JL The role of cellular senescence in ageing and endocrine disease Nat Rev Endocrinol 2020 16 5 263 75 10.1038/s41574-020-0335-y 32161396 PMC7227781 · DOI · Paper page
  2. [2]López-Otín C Blasco MA Partridge L Serrano M Kroemer G The hallmarks of aging Cell 2013 153 6 1194 217 10.1016/j.cell.2013.05.039 23746838 PMC3836174 · DOI · Paper page
  3. [4]Guo J Huang X Dou L Yan M Shen T Tang W Aging and aging-related diseases: from molecular mechanisms to interventions and treatments Signal Transduct Target Ther 2022 7 1 391 10.1038/s41392-022-01251-0 36522308 PMC9755275 · DOI
  4. [6]Faroni A Mobasseri SA Kingham PJ Reid AJ Peripheral nerve regeneration: experimental strategies and future perspectives Adv Drug Deliv Rev 2015 82–83 160 7 10.1016/j.addr.2014.11.010 25446133 · DOI
  5. [7]Gaharwar AK Singh I Khademhosseini A Engineered biomaterials for in situ tissue regeneration Nat Rev Mater 2020 5 9 686 705 10.1038/s41578-020-0209-x · DOI
  6. [8]Chen J Zhou R Feng Y Cheng L Molecular mechanisms of exercise contributing to tissue regeneration Signal Transduct Target Ther 2022 7 1 383 10.1038/s41392-022-01233-2 36446784 PMC9709153 · DOI
  7. [9]Ji SF Zhou LX Sun ZF Xiang JB Cui SY Li Y Small molecules facilitate single factor-mediated sweat gland cell reprogramming Mil Med Res 2022 9 1 13 35351192 PMC8962256
  8. [10]Xiong Y Mi BB Lin Z Hu YQ Yu L Zha KK The role of the immune microenvironment in bone, cartilage, and soft tissue regeneration: from mechanism to therapeutic opportunity Mil Med Res 2022 9 1 65 36401295 PMC9675067
  9. [11]Sahinyan K Lazure F Blackburn DM Soleimani VD Decline of regenerative potential of old muscle stem cells: contribution to muscle aging FEBS J 2023 290 5 1267 89 10.1111/febs.16352 35029021 · DOI
  10. [12]Palmer AK Kirkland JL Aging and adipose tissue: potential interventions for diabetes and regenerative medicine Exp Gerontol 2016 86 97 105 10.1016/j.exger.2016.02.013 26924669 PMC5001933 · DOI
  11. [13]Rhinn M Ritschka B Keyes WM Cellular senescence in development, regeneration and disease Development 2019 146 20 dev151837 10.1242/dev.151837 31575608 · DOI
  12. [14]Moses L Pachter L Museum of spatial transcriptomics Nat Methods. 2022 19 5 534 46 10.1038/s41592-022-01409-2 35273392 · DOI · Paper page
  13. [17]Burgess DJ Spatial transcriptomics coming of age Nat Rev Genet 2019 20 6 317 10.1038/s41576-019-0129-z 30980030 · DOI
  14. [18]Tian L Chen F Macosko EZ The expanding vistas of spatial transcriptomics Nat Biotechnol 2023 41 6 773 82 10.1038/s41587-022-01448-2 36192637 PMC10091579 · DOI · Paper page
  15. [20]Costa V Angelini C De Feis I Ciccodicola A Uncovering the complexity of transcriptomes with RNA-Seq J Biomed Biotechnol 2010 2010 853916 10.1155/2010/853916 20625424 PMC2896904 · DOI
  16. [21]Velculescu VE Madden SL Zhang L Lash AE Yu J Rago C Analysis of human transcriptomes Nat Genet 1999 23 4 387 8 10.1038/70487 10581018 · DOI
  17. [22]Zeng H Huang J Zhou H Meilandt WJ Dejanovic B Zhou Y Integrative in situ mapping of single-cell transcriptional states and tissue histopathology in a mouse model of Alzheimer's disease Nat Neurosci 2023 26 3 430 46 36732642 PMC11332722
  18. [23]Tang F Lao K Surani MA Development and applications of single-cell transcriptome analysis Nat Methods 2011 8 4 Suppl S6 11 10.1038/nmeth.1557 21451510 PMC3408593 · DOI
  19. [25]Wang Y Navin NE Advances and applications of single-cell sequencing technologies Mol Cell 2015 58 4 598 609 10.1016/j.molcel.2015.05.005 26000845 PMC4441954 · DOI
  20. [26]Tian T Wang Y Wang H Zhu Z Xiao Z Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy J Cell Biochem 2010 111 2 488 96 10.1002/jcb.22733 20533300 · DOI
  21. [27]Lange S Katayama Y Schmid M Burkacky O Brauchle C Lamb DC Simultaneous transport of different localized mRNA species revealed by live-cell imaging Traffic 2008 9 8 1256 67 10.1111/j.1600-0854.2008.00763.x 18485054 · DOI
  22. [28]Held M Schmitz MHA Fischer B Walter T Neumann B Olma MH Cell Cognition: time-resolved phenotype annotation in high-throughput live cell imaging Nat Methods 2010 7 9 747 54 10.1038/nmeth.1486 20693996 · DOI
  23. [29]Galluzzi L Yamazaki T Kroemer G Linking cellular stress responses to systemic homeostasis Nat Rev Mol Cell Biol 2018 19 11 731 45 10.1038/s41580-018-0068-0 30305710 · DOI
  24. [30]Yin Y Chen H Wang Y Zhang L Wang X Roles of extracellular vesicles in the aging microenvironment and age-related diseases J Extracell Vesicles 2021 10 12 e12154 10.1002/jev2.12154 34609061 PMC8491204 · DOI
  25. [31]Leontieva OV Natarajan V Demidenko ZN Burdelya LG Gudkov AV Blagosklonny MV Hypoxia suppresses conversion from proliferative arrest to cellular senescence Proc Natl Acad Sci U S A 2012 109 33 13314 8 10.1073/pnas.1205690109 22847439 PMC3421205 · DOI · Paper page
  26. [32]Hu X Xu W Ren Y Wang Z He X Huang R Spinal cord injury: molecular mechanisms and therapeutic interventions Signal Transduct Target Ther 2023 8 1 245 10.1038/s41392-023-01477-6 37357239 PMC10291001 · DOI
  27. [33]Lin D Shen L Luo M Zhang K Li J Yang Q Circulating tumor cells: biology and clinical significance Signal Transduct Target Ther 2021 6 1 404 10.1038/s41392-021-00817-8 34803167 PMC8606574 · DOI
  28. [34]Bai YM Yang F Luo P Xie LL Chen JH Guan YD Single-cell transcriptomic dissection of the cellular and molecular events underlying the triclosan-induced liver fibrosis in mice Mil Med Res 2023 10 1 7 36814339 PMC9945401
  29. [35]Wang Y Wang JY Schnieke A Fischer K Advances in single-cell sequencing: insights from organ transplantation Mil Med Res 2021 8 1 45 34389057 PMC8361611
  30. [36]Tang L Huang ZP Mei H Hu Y Insights gained from single-cell analysis of chimeric antigen receptor T-cell immunotherapy in cancer Mil Med Res 2023 10 1 52 37941075 PMC10631149
  31. [37]Cao J Chen X Huang S Shi W Fan Q Gong Y Microfluidics-based single cell analysis: from transcriptomics to spatiotemporal multi-omics TrAC-Trend Anal Chem 2023 158 116868 10.1016/j.trac.2022.116868 · DOI
  32. [38]Lin S Liu Y Zhang M Xu X Chen Y Zhang H Microfluidic single-cell transcriptomics: moving towards multimodal and spatiotemporal omics Lab Chip 2021 21 20 3829 49 10.1039/D1LC00607J 34541590 · DOI
  33. [39]Magoulopoulou A Salas SM Tiklová K Samuelsson ER Hilscher MM Nilsson M Padlock probe-based targeted in situ sequencing: overview of methods and applications Annu Rev Genomics Hum Genet 2023 24 133 50 10.1146/annurev-genom-102722-092013 37018847 · DOI
  34. [40]Patkulkar PA Subbalakshmi AR Jolly MK Sinharay S Mapping spatiotemporal heterogeneity in tumor profiles by integrating high-throughput imaging and omics analysis ACS Omega 2023 8 7 6126 38 10.1021/acsomega.2c06659 36844580 PMC9948167 · DOI
  35. [41]Chelvanambi S, Hester JM, Sharma S, Lahm T, Frump AL. Slide-seq for spatially mapping gene expression. Metabolic syndrome exacerbates group 2 pulmonary hypertension, and NAD metabolism is influenced by tissue origin. Am J Respir Cell Mol Biol. 2020;62(1):112-4. 31633380
  36. [42]Xia K Sun HX Li J Li J Zhao Y Chen L The single-cell Stereo-seq reveals region-specific cell subtypes and transcriptome profiling in Arabidopsis leaves Dev Cell 2022 57 10 1299 310.e4 10.1016/j.devcel.2022.04.011 35512702 · DOI
  37. [43]Ren J Zhou H Zeng H Wang CK Huang J Qiu X Spatiotemporally resolved transcriptomics reveals the subcellular RNA kinetic landscape Nat Methods 2023 20 5 695 705 10.1038/s41592-023-01829-8 37038000 PMC10172111 · DOI · Paper page
  38. [44]Asp M Bergenstrahle J Lundeberg J Spatially resolved transcriptomes-next generation tools for tissue exploration Bioessays 2020 42 10 e1900221 10.1002/bies.201900221 32363691 · DOI · Paper page
  39. [45]Zhang X Wang Z Zhang C Li Y Lu S Steffens S Laser capture microdissection-based mrna expression microarrays and single-cell rna sequencing in atherosclerosis research Methods Mol Biol 2022 2419 715 26 10.1007/978-1-0716-1924-7_43 35237997 · DOI
  40. [47]Baysoy A Bai Z Satija R Fan R The technological landscape and applications of single-cell multi-omics Nat Rev Mol Cell Biol 2023 24 10 695 713 10.1038/s41580-023-00615-w 37280296 PMC10242609 · DOI · Paper page
  41. [48]McGinnis LM Ibarra-Lopez V Rost S Ziai J Clinical and research applications of multiplexed immunohistochemistry and in situ hybridization J Pathol 2021 254 4 405 17 10.1002/path.5663 33723864 · DOI
  42. [49]Chen TY You L Hardillo JAU Chien MP Spatial transcriptomic technologies Cells 2023 12 16 2042 10.3390/cells12162042 37626852 PMC10453065 · DOI
  43. [50]Cassidy A Jones J Developments in in situ hybridisation Methods 2014 70 1 39 45 10.1016/j.ymeth.2014.04.006 24747923 · DOI
  44. [51]Chen X Sun YC Church GM Lee JH Zador AM Efficient in situ barcode sequencing using padlock probe-based BaristaSeq Nucleic Acids Res 2018 46 4 e22 10.1093/nar/gkx1206 29190363 PMC5829746 · DOI
  45. [52]Bowes AL Tarabichi M Pillay N Van Loo P Leveraging single-cell sequencing to unravel intratumour heterogeneity and tumour evolution in human cancers J Pathol 2022 257 4 466 78 10.1002/path.5914 35438189 PMC9322001 · DOI
  46. [53]Pervez MT Hasnain MJU Abbas SH Moustafa MF Aslam N Shah SSM A comprehensive review of performance of next-generation sequencing platforms Biomed Res Int 2022 2022 3457806 10.1155/2022/3457806 36212714 PMC9537002 · DOI
  47. [54]Kulkarni MM. Digital multiplexed gene expression analysis using the NanoString nCounter system. Curr Protoc Mol Biol. 2011;Chapter 25:Unit25B.10. 21472696
  48. [55]Molania R Gagnon-Bartsch JA Dobrovic A Speed TP A new normalization for Nanostring nCounter gene expression data Nucleic Acids Res 2019 47 12 6073 83 10.1093/nar/gkz433 31114909 PMC6614807 · DOI
  49. [56]Li Z Song T Yong J Kuang R Imputation of spatially-resolved transcriptomes by graph-regularized tensor completion PLoS Comput Biol 2021 17 4 e1008218 10.1371/journal.pcbi.1008218 33826608 PMC8055040 · DOI
  50. [57]Li X Wang CY From bulk, single-cell to spatial RNA sequencing Int J Oral Sci 2021 13 1 36 10.1038/s41368-021-00146-0 34782601 PMC8593179 · DOI · Paper page
  51. [58]Rodriques SG Stickels RR Goeva A Martin CA Murray E Vanderburg CR Slide-seq: a scalable technology for measuring genome-wide expression at high spatial resolution Science 2019 363 6434 1463 7 10.1126/science.aaw1219 30923225 PMC6927209 · DOI · Paper page
  52. [59]Mantri M Scuderi GJ Abedini-Nassab R Wang MFZ McKellar D Shi H Spatiotemporal single-cell RNA sequencing of developing chicken hearts identifies interplay between cellular differentiation and morphogenesis Nat Commun 2021 12 1 1771 10.1038/s41467-021-21892-z 33741943 PMC7979764 · DOI · Paper page
  53. [60]Wei X Fu S Li H Liu Y Wang S Feng W Single-cell Stereo-seq reveals induced progenitor cells involved in axolotl brain regeneration Science 2022 377 6610 eabp9444 10.1126/science.abp9444 36048929 · DOI · Paper page
  54. [62]Cho CS Xi J Si Y Park SR Hsu JE Kim M Microscopic examination of spatial transcriptome using Seq-Scope Cell 2021 184 13 3559 72.e22 10.1016/j.cell.2021.05.010 34115981 PMC8238917 · DOI · Paper page
  55. [64]Srivatsan SR Regier MC Barkan E Franks JM Packer JS Grosjean P Embryo-scale, single-cell spatial transcriptomics Science 2021 373 6550 111 7 10.1126/science.abb9536 34210887 PMC9118175 · DOI
  56. [65]Weber C Single-cell spatial transcriptomics Nat Cell Biol 2021 23 11 1108 34750575
  57. [66]Wang WJ Chu LX He LY Zhang MJ Dang KT Gao C Spatial transcriptomics: recent developments and insights in respiratory research Mil Med Res 2023 10 1 38 37592342 PMC10433685
  58. [67]Li PH Kong XY He YZ Liu Y Peng X Li ZH Recent developments in application of single-cell RNA sequencing in the tumour immune microenvironment and cancer therapy Mil Med Res 2022 9 1 52 36154923 PMC9511789
  59. [68]Hsieh WC Budiarto BR Wang YF Lin CY Gwo MC So DK Spatial multi-omics analyses of the tumor immune microenvironment J Biomed Sci 2022 29 1 96 10.1186/s12929-022-00879-y 36376874 PMC9661775 · DOI
  60. [69]Mund A Brunner AD Mann M Unbiased spatial proteomics with single-cell resolution in tissues Mol Cell 2022 82 12 2335 49 10.1016/j.molcel.2022.05.022 35714588 · DOI · Paper page
  61. [70]Cheng M Jiang Y Xu J Mentis AA Wang S Zheng H Spatially resolved transcriptomics: a comprehensive review of their technological advances, applications, and challenges J Genet Genomics 2023 50 9 625 40 10.1016/j.jgg.2023.03.011 36990426 · DOI
  62. [71]Moffitt JR Lundberg E Heyn H The emerging landscape of spatial profiling technologies Nat Rev Genet 2022 23 12 741 59 10.1038/s41576-022-00515-3 35859028 · DOI · Paper page
  63. [72]Liu C Li R Li Y Lin X Zhao K Liu Q Spatiotemporal mapping of gene expression landscapes and developmental trajectories during zebrafish embryogenesis Dev Cell 2022 57 10 1284 98.e5 10.1016/j.devcel.2022.04.009 35512701 · DOI
  64. [73]Wang M Hu Q Lv T Wang Y Lan Q Xiang R High-resolution 3D spatiotemporal transcriptomic maps of developing Drosophila embryos and larvae Dev Cell 2022 57 10 1271 83.e4 10.1016/j.devcel.2022.04.006 35512700 · DOI
  65. [74]Chen A, Liao S, Cheng M, Ma K, Wu L, Lai Y, et al. Large field of view-spatially resolved transcriptomics at nanoscale resolution. bioRxiv. 2021. 10.1101/2021.01.17.427004. · DOI
  66. [75]Singha M Spitalny L Nguyen K Vandewalle A Spitale RC Chemical methods for measuring RNA expression with metabolic labeling Wiley Interdiscip Rev RNA 2021 12 5 e1650 10.1002/wrna.1650 33738981 · DOI
  67. [76]Schofield JA Duffy EE Kiefer L Sullivan MC Simon MD TimeLapse-seq: adding a temporal dimension to RNA sequencing through nucleoside recoding Nat Methods 2018 15 3 221 5 10.1038/nmeth.4582 29355846 PMC5831505 · DOI
  68. [77]Battich N Beumer J de Barbanson B Krenning L Baron CS Tanenbaum ME Sequencing metabolically labeled transcripts in single cells reveals mRNA turnover strategies Science 2020 367 6482 1151 6 10.1126/science.aax3072 32139547 · DOI
  69. [78]Qiu Q Hu P Qiu X Govek KW Cámara PG Wu H Massively parallel and time-resolved RNA sequencing in single cells with scNT-seq Nat Methods 2020 17 10 991 1001 10.1038/s41592-020-0935-4 32868927 PMC8103797 · DOI
  70. [79]Rodriques SG Chen LM Liu S Zhong ED Scherrer JR Boyden ES RNA timestamps identify the age of single molecules in RNA sequencing Nat Biotechnol 2021 39 3 320 5 10.1038/s41587-020-0704-z 33077959 PMC7956158 · DOI
  71. [80]Han KY Leslie BJ Fei J Zhang J Ha T Understanding the photophysics of the spinach–DFHBI RNA aptamer–fluorogen complex to improve live-cell RNA imaging J Am Chem Soc 2013 135 50 19033 8 10.1021/ja411060p 24286188 PMC3908778 · DOI
  72. [81]Wang D Shalamberidze A Arguello AE Purse BW Kleiner RE Live-cell RNA imaging with metabolically incorporated fluorescent nucleosides J Am Chem Soc 2022 144 32 14647 56 10.1021/jacs.2c04142 35930766 PMC9940818 · DOI
  73. [82]Pade LR Stepler KE Portero EP DeLaney K Nemes P Biological mass spectrometry enables spatiotemporal 'omics: From tissues to cells to organelles Mass Spectrom Rev 2023 43 1 106 38 10.1002/mas.21824 36647247 PMC10668589 · DOI
  74. [83]Brozova K Hantusch B Kenner L Kratochwill K Spatial proteomics for the molecular characterization of breast cancer Proteomes 2023 11 2 17 10.3390/proteomes11020017 37218922 PMC10204503 · DOI
  75. [84]Lohani V, A RA, Kundu S, Akhter MQ, Bag S. Single-cell proteomics with spatial attributes: tools and techniques. ACS Omega. 2023;8(20):17499-510. PMC10210017 37251119
  76. [85]de Sousa Abreu R Penalva LO Marcotte EM Vogel C Global signatures of protein and mRNA expression levels Mol Biosyst 2009 5 12 1512 26 20023718 PMC4089977
  77. [86]Bosia C Sgrò F Conti L Baldassi C Brusa D Cavallo F RNAs competing for microRNAs mutually influence their fluctuations in a highly non-linear microRNA-dependent manner in single cells Genome Biol 2017 18 1 37 10.1186/s13059-017-1162-x 28219439 PMC5319025 · DOI
  78. [88]Selkrig J Li N Hausmann A Mangan MSJ Zietek M Mateus A Spatiotemporal proteomics uncovers cathepsin-dependent macrophage cell death during Salmonella infection Nat Microbiol 2020 5 9 1119 33 10.1038/s41564-020-0736-7 32514074 PMC7610801 · DOI
  79. [89]Marmor-Kollet H Siany A Kedersha N Knafo N Rivkin N Danino YM Spatiotemporal proteomic analysis of stress granule disassembly using APEX reveals regulation by SUMOylation and links to ALS pathogenesis Mol Cell 2020 80 5 876 91.e6 10.1016/j.molcel.2020.10.032 33217318 PMC7816607 · DOI
  80. [90]Ke M Yuan X He A Yu P Chen W Shi Y Spatiotemporal profiling of cytosolic signaling complexes in living cells by selective proximity proteomics Nat Commun 2021 12 1 71 10.1038/s41467-020-20367-x 33397984 PMC7782698 · DOI
  81. [91]Mahdessian D Cesnik AJ Gnann C Danielsson F Stenstrom L Arif M Spatiotemporal dissection of the cell cycle with single-cell proteogenomics Nature 2021 590 7847 649 54 10.1038/s41586-021-03232-9 33627808 · DOI
  82. [92]Uhlén M, Fagerberg L, Hallström BM, Lindskog C, Oksvold P, Mardinoglu A, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419. 25613900
  83. [93]Lundberg E Borner GHH Spatial proteomics: a powerful discovery tool for cell biology Nat Rev Mol Cell Biol 2019 20 5 285 302 10.1038/s41580-018-0094-y 30659282 · DOI · Paper page
  84. [94]Hickey JW Neumann EK Radtke AJ Camarillo JM Beuschel RT Albanese A Spatial mapping of protein composition and tissue organization: a primer for multiplexed antibody-based imaging Nat Methods 2022 19 3 284 95 10.1038/s41592-021-01316-y 34811556 PMC9264278 · DOI
  85. [95]Lewis SM Asselin-Labat ML Nguyen Q Berthelet J Tan X Wimmer VC Spatial omics and multiplexed imaging to explore cancer biology Nat Methods 2021 18 9 997 1012 10.1038/s41592-021-01203-6 34341583 · DOI
  86. [96]Murray E Cho JH Goodwin D Ku T Swaney J Kim SY Simple, scalable proteomic imaging for high-dimensional profiling of intact systems Cell 2015 163 6 1500 14 10.1016/j.cell.2015.11.025 26638076 PMC5275966 · DOI
  87. [97]Gerdes MJ Sevinsky CJ Sood A Adak S Bello MO Bordwell A Highly multiplexed single-cell analysis of formalin-fixed, paraffin-embedded cancer tissue Proc Natl Acad Sci U S A 2013 110 29 11982 7 10.1073/pnas.1300136110 23818604 PMC3718135 · DOI
  88. [98]Lin JR Fallahi-Sichani M Sorger PK Highly multiplexed imaging of single cells using a high-throughput cyclic immunofluorescence method Nat Commun 2015 6 8390 10.1038/ncomms9390 26399630 PMC4587398 · DOI
  89. [99]Venkatesan M Zhang N Marteau B Yajima Y De Zarate Garcia NO Fang Z Spatial subcellular organelle networks in single cells Sci Rep 2023 13 1 5374 10.1038/s41598-023-32474-y 37005468 PMC10067843 · DOI
  90. [100]Radtke AJ Kandov E Lowekamp B Speranza E Chu CJ Gola A IBEX: a versatile multiplex optical imaging approach for deep phenotyping and spatial analysis of cells in complex tissues Proc Natl Acad Sci U S A 2020 117 52 33455 65 10.1073/pnas.2018488117 33376221 PMC7776876 · DOI
  91. [101]Gut G Herrmann MD Pelkmans L Multiplexed protein maps link subcellular organization to cellular states Science 2018 361 6401 eaar7042 10.1126/science.aar7042 30072512 · DOI · Paper page
  92. [102]Zhu C Qiu J Pongkitwitoon S Thomopoulos S Xia Y Inverse opal scaffolds with gradations in mineral content for spatial control of osteogenesis Adv Mater 2018 30 29 e1706706 10.1002/adma.201706706 PMC6269221 29847696 · DOI
  93. [103]Giesen C Wang HA Schapiro D Zivanovic N Jacobs A Hattendorf B Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry Nat Methods 2014 11 4 417 22 10.1038/nmeth.2869 24584193 · DOI · Paper page
  94. [104]Angelo M Bendall SC Finck R Hale MB Hitzman C Borowsky AD Multiplexed ion beam imaging of human breast tumors Nat Med 2014 20 4 436 42 10.1038/nm.3488 24584119 PMC4110905 · DOI · Paper page
  95. [105]Liu CC, McCaffrey EF, Greenwald NF, Soon E, Risom T, Vijayaragavan K, et al. Multiplexed ion beam imaging: insights into pathobiology. 2022;17:403-23. 34752710
  96. [106]Wang Y Woehrstein JB Donoghue N Dai M Avendano MS Schackmann RCJ Rapid sequential in situ multiplexing with DNA exchange imaging in neuronal cells and tissues Nano Lett 2017 17 10 6131 9 10.1021/acs.nanolett.7b02716 28933153 PMC5658129 · DOI
  97. [108]Schürch CM Bhate SS Barlow GL Phillips DJ Noti L Zlobec I Coordinated cellular neighborhoods orchestrate antitumoral immunity at the colorectal cancer invasive front Cell 2020 182 5 1341 59.e19 10.1016/j.cell.2020.07.005 32763154 PMC7479520 · DOI
  98. [109]Saka SK Wang Y Kishi JY Zhu A Zeng Y Xie W Immuno-SABER enables highly multiplexed and amplified protein imaging in tissues Nat Biotechnol 2019 37 9 1080 90 10.1038/s41587-019-0207-y 31427819 PMC6728175 · DOI
  99. [110]Spraggins JM Djambazova KV Rivera ES Migas LG Neumann EK Fuetterer A High-performance molecular imaging with MALDI trapped ion-mobility time-of-flight (timsTOF) mass spectrometry Anal Chem 2019 91 22 14552 60 10.1021/acs.analchem.9b03612 31593446 PMC7382025 · DOI
  100. [111]Gekenidis MT Studer P Wuthrich S Brunisholz R Drissner D Beyond the matrix-assisted laser desorption ionization (MALDI) biotyping workflow: in search of microorganism-specific tryptic peptides enabling discrimination of subspecies Appl Environ Microbiol 2014 80 14 4234 41 10.1128/AEM.00740-14 24795381 PMC4068689 · DOI
  101. [112]Palla G Fischer DS Regev A Theis FJ Spatial components of molecular tissue biology Nat Biotechnol 2022 40 3 308 18 10.1038/s41587-021-01182-1 35132261 · DOI
  102. [114]Li L Sun C Sun Y Dong Z Wu R Sun X Spatially resolved proteomics via tissue expansion Nat Commun 2022 13 1 7242 10.1038/s41467-022-34824-2 36450705 PMC9712279 · DOI
  103. [115]Scholey JM Brust-Mascher I Mogilner A Cell division Nature 2003 422 6933 746 52 10.1038/nature01599 12700768 · DOI
  104. [116]Salazar-Roa M Malumbres M Fueling the cell division cycle Trends Cell Biol 2017 27 1 69 81 10.1016/j.tcb.2016.08.009 27746095 · DOI
  105. [117]Karlsson J Kroneis T Jonasson E Larsson E Stahlberg A Transcriptomic characterization of the human cell cycle in individual unsynchronized cells J Mol Biol 2017 429 24 3909 24 10.1016/j.jmb.2017.10.011 29045817 · DOI
  106. [118]Macieira-Coelho A Cell division and aging of the organism Biogerontology 2011 12 6 503 15 10.1007/s10522-011-9346-3 21732041 · DOI
  107. [119]Polymenis M Kennedy BK Unbalanced growth, senescence and aging Adv Exp Med Biol 2017 1002 189 208 10.1007/978-3-319-57127-0_8 28600787 PMC6345385 · DOI
  108. [121]Subramanian I Verma S Kumar S Jere A Anamika K Multi-omics data integration, interpretation, and its application Bioinform Biol Insights 2020 14 1177932219899051 10.1177/1177932219899051 32076369 PMC7003173 · DOI · Paper page
  109. [122]Irie M Fujimura Y Yamato M Miura D Wariishi H Integrated MALDI-MS imaging and LC-MS techniques for visualizing spatiotemporal metabolomic dynamics in a rat stroke model Metabolomics 2014 10 473 83 10.1007/s11306-013-0588-8 24772057 PMC3984668 · DOI
  110. [123]Jin B Pang X Zang Q Ga M Xu J Luo Z Spatiotemporally resolved metabolomics and isotope tracing reveal CNS drug targets Acta Pharm Sin B 2023 13 4 1699 710 10.1016/j.apsb.2022.11.011 37139420 PMC10149982 · DOI
  111. [124]Yuan Z Zhou Q Cai L Pan L Sun W Qumu S SEAM is a spatial single nuclear metabolomics method for dissecting tissue microenvironment Nat Methods 2021 18 10 1223 32 10.1038/s41592-021-01276-3 34608315 · DOI
  112. [125]Fehr M Frommer WB Lalonde S Visualization of maltose uptake in living yeast cells by fluorescent nanosensors Proc Natl Acad Sci U S A 2002 99 15 9846 51 10.1073/pnas.142089199 12097642 PMC125039 · DOI
  113. [126]Han G Wei P He M Teng H Chu Y Metabolomic profiling of the aqueous humor in patients with wet age-related macular degeneration using UHPLC-MS/MS J Proteome Res 2020 19 6 2358 66 10.1021/acs.jproteome.0c00036 32293180 · DOI
  114. [127]Spraker JE Luu GT Sanchez LM Imaging mass spectrometry for natural products discovery: a review of ionization methods Nat Prod Rep 2020 37 2 150 62 10.1039/C9NP00038K 31364647 PMC6992513 · DOI
  115. [128]Chu L Huang Y Xu Y Wang LK Lu Q An LC-APCI+-MS/MS-based method for determining the concentration of neurosteroids in the brain of male mice with different gut microbiota J Neurosci Methods 2021 360 109268 10.1016/j.jneumeth.2021.109268 34171313 · DOI
  116. [129]Chu L Li N Deng J Wu Y Yang H Wang W LC-APCI+-MS/MS method for the analysis of ten hormones and two endocannabinoids in plasma and hair from the mice with different gut microbiota J Pharm Biomed Anal 2020 185 113223 10.1016/j.jpba.2020.113223 32145535 · DOI
  117. [130]Chu L Shu X Huang Y Chu T Ge M Lu Q Sex steroid hormones in urinary exosomes as biomarkers for the prediction of prostate cancer Clinica Chimica Acta 2022 531 389 98 10.1016/j.cca.2022.04.995 35487250 · DOI
  118. [131]Murayama C Kimura Y Setou M Imaging mass spectrometry: principle and application Biophys Rev 2009 1 3 131 10.1007/s12551-009-0015-6 28509996 PMC5425681 · DOI
  119. [132]Stoeckli M Chaurand P Hallahan DE Caprioli RM Imaging mass spectrometry: a new technology for the analysis of protein expression in mammalian tissues Nat Med 2001 7 4 493 6 10.1038/86573 11283679 · DOI
  120. [133]Kaufmann R Matrix-assisted laser desorption ionization (MALDI) mass spectrometry: a novel analytical tool in molecular biology and biotechnology J Biotechnol 1995 41 2–3 155 75 10.1016/0168-1656(95)00009-F 7654348 · DOI
  121. [134]Takats Z Wiseman JM Gologan B Cooks RG Mass spectrometry sampling under ambient conditions with desorption electrospray ionization Science. 2004 306 5695 471 3 10.1126/science.1104404 15486296 · DOI
  122. [135]Takats Z Wiseman JM Cooks RG Ambient mass spectrometry using desorption electrospray ionization (DESI): instrumentation, mechanisms and applications in forensics, chemistry, and biology J Mass Spectrom 2005 40 10 1261 75 10.1002/jms.922 16237663 · DOI
  123. [136]Taylor MJ Lukowski JK Anderton CR Spatially resolved mass spectrometry at the single cell: recent innovations in proteomics and metabolomics J Am Soc Mass Spectrom 2021 32 4 872 94 10.1021/jasms.0c00439 33656885 PMC8033567 · DOI
  124. [137]Rappez L Stadler M Triana S Gathungu RM Ovchinnikova K Phapale P SpaceM reveals metabolic states of single cells Nat Methods 2021 18 7 799 805 10.1038/s41592-021-01198-0 34226721 PMC7611214 · DOI
  125. [138]Zavalin A Todd EM Rawhouser PD Yang J Norris JL Caprioli RM Direct imaging of single cells and tissue at sub-cellular spatial resolution using transmission geometry MALDI MS J Mass Spectrom 2012 47 11 i 10.1002/jms.3108 23147833 PMC3507384 · DOI
  126. [139]Kauppila TJ Talaty N Kuuranne T Kotiaho T Kostiainen R Cooks RG Rapid analysis of metabolites and drugs of abuse from urine samples by desorption electrospray ionization-mass spectrometry Analyst 2007 132 9 868 75 10.1039/b703524a 17710261 · DOI
  127. [140]Kauppila TJ Wiseman JM Ketola RA Kotiaho T Cooks RG Kostiainen R Desorption electrospray ionization mass spectrometry for the analysis of pharmaceuticals and metabolites Rapid Commun Mass Spectrom 2006 20 3 387 92 10.1002/rcm.2304 16381061 · DOI
  128. [141]Wiseman JM Ifa DR Venter A Cooks RG Ambient molecular imaging by desorption electrospray ionization mass spectrometry Nat Protoc 2008 3 3 517 24 10.1038/nprot.2008.11 18323820 · DOI
  129. [142]Roach PJ Laskin J Laskin A Nanospray desorption electrospray ionization: an ambient method for liquid-extraction surface sampling in mass spectrometry Analyst 2010 135 9 2233 6 10.1039/c0an00312c 20593081 · DOI
  130. [143]Walther F Koerver R Fuchs T Ohno S Sann J Rohnke M Visualization of the interfacial decomposition of composite cathodes in argyrodite-based all-solid-state batteries using time-of-flight secondary-ion mass spectrometry Chem Mater 2019 31 10 3745 55 10.1021/acs.chemmater.9b00770 · DOI
  131. [144]Kotowska AM Trindade GF Mendes PM Williams PM Aylott JW Shard AG Protein identification by 3D OrbiSIMS to facilitate in situ imaging and depth profiling Nat Commun 2020 11 1 5832 10.1038/s41467-020-19445-x 33203841 PMC7672064 · DOI
  132. [145]Passarelli MK Pirkl A Moellers R Grinfeld D Kollmer F Havelund R The 3D OrbiSIMS-label-free metabolic imaging with subcellular lateral resolution and high mass-resolving power Nat Methods 2017 14 12 1175 83 10.1038/nmeth.4504 29131162 · DOI
  133. [147]Fitz-James MH Cavalli G Molecular mechanisms of transgenerational epigenetic inheritance Nat Rev Genet 2022 23 6 325 41 10.1038/s41576-021-00438-5 34983971 PMC7619059 · DOI · Paper page
  134. [148]Foley DL Craig JM Morley R Olsson CA Dwyer T Smith K Prospects for epigenetic epidemiology Am J Epidemiol 2009 169 4 389 400 10.1093/aje/kwn380 19139055 PMC3290967 · DOI · Paper page
  135. [149]Tollefsbol TO Advances in epigenetic technology Methods Mol Biol 2011 791 1 10 10.1007/978-1-61779-316-5_1 21913067 PMC3227536 · DOI
  136. [150]Wu Y, Terekhanova NV, Caravan W, Naser Al Deen N, Lal P, Chen S, et al. Epigenetic and transcriptomic characterization reveals progression markers and essential pathways in clear cell renal cell carcinoma. Nat Commun. 2023;14(1):1681. PMC10042888 36973268
  137. [151]Ramalingam N Jeffrey SS Future of liquid biopsies with growing technological and bioinformatics studies: opportunities and challenges in discovering tumor heterogeneity with single-cell level analysis Cancer J 2018 24 2 104 8 10.1097/PPO.0000000000000308 29601337 PMC5880298 · DOI
  138. [152]Trapp A Kerepesi C Gladyshev VN Profiling epigenetic age in single cells Nat Aging 2021 1 12 1189 201 10.1038/s43587-021-00134-3 36211119 PMC9536112 · DOI
  139. [153]Bheda P Schneider R Epigenetics reloaded: the single-cell revolution Trends Cell Biol 2014 24 11 712 23 10.1016/j.tcb.2014.08.010 25283892 · DOI
  140. [154]Rudolph KL DNA-methylation aging at single-cell level Nature Aging 2021 1 12 1086 7 10.1038/s43587-021-00154-z 37117522 · DOI
  141. [155]Casado-Pelaez M Bueno-Costa A Esteller M Single cell cancer epigenetics Trends Cancer 2022 8 10 820 38 10.1016/j.trecan.2022.06.005 35821003 · DOI
  142. [156]Kaya-Okur HS Wu SJ Codomo CA Pledger ES Bryson TD Henikoff JG CUT&Tag for efficient epigenomic profiling of small samples and single cells Nat Commun 2019 10 1 1930 10.1038/s41467-019-09982-5 31036827 PMC6488672 · DOI · Paper page
  143. [158]Liu Y Yang M Deng Y Su G Enninful A Guo CC High-spatial-resolution multi-omics sequencing via deterministic barcoding in tissue Cell 2020 183 6 1665 81.e18 10.1016/j.cell.2020.10.026 33188776 PMC7736559 · DOI · Paper page
  144. [159]Yu P Xiao S Xin X Song CX Huang W McDee D Spatiotemporal clustering of the epigenome reveals rules of dynamic gene regulation Genome Res 2013 23 2 352 64 10.1101/gr.144949.112 23033340 PMC3561876 · DOI
  145. [160]Smallwood SA Lee HJ Angermueller C Krueger F Saadeh H Peat J Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity Nat Methods 2014 11 8 817 20 10.1038/nmeth.3035 25042786 PMC4117646 · DOI · Paper page
  146. [162]Angermueller C Clark SJ Lee HJ Macaulay IC Teng MJ Hu TX Parallel single-cell sequencing links transcriptional and epigenetic heterogeneity Nat Methods 2016 13 3 229 32 10.1038/nmeth.3728 26752769 PMC4770512 · DOI · Paper page
  147. [163]Macaulay IC Haerty W Kumar P Li YI Hu TX Teng MJ G&T-seq: parallel sequencing of single-cell genomes and transcriptomes Nat Methods 2015 12 6 519 22 10.1038/nmeth.3370 25915121 · DOI · Paper page
  148. [164]Buenrostro JD Giresi PG Zaba LC Chang HY Greenleaf WJ Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position Nat Methods 2013 10 12 1213 8 10.1038/nmeth.2688 24097267 PMC3959825 · DOI · Paper page
  149. [165]Ma A McDermaid A Xu J Chang Y Ma Q Integrative methods and practical challenges for single-cell multi-omics Trends Biotechnol 2020 38 9 1007 22 10.1016/j.tibtech.2020.02.013 32818441 PMC7442857 · DOI
  150. [167]Skene PJ Henikoff S An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites Elife 2017 6 e21856 10.7554/eLife.21856 28079019 PMC5310842 · DOI
  151. [169]Janssens DH Otto DJ Meers MP Setty M Ahmad K Henikoff S CUT&Tag2for1: a modified method for simultaneous profiling of the accessible and silenced regulome in single cells Genome Biol 2022 23 1 81 10.1186/s13059-022-02642-w 35300717 PMC8928696 · DOI
  152. [170]Zhang B Srivastava A Mimitou E Stuart T Raimondi I Hao Y Characterizing cellular heterogeneity in chromatin state with scCUT&Tag-pro Nat Biotechnol 2022 40 8 1220 30 10.1038/s41587-022-01250-0 35332340 PMC9378363 · DOI · Paper page
  153. [172]Xiong H Luo Y Wang Q Yu X He A Single-cell joint detection of chromatin occupancy and transcriptome enables higher-dimensional epigenomic reconstructions Nat Methods 2021 18 6 652 60 10.1038/s41592-021-01129-z 33958790 · DOI · Paper page
  154. [173]Deng Y Bartosovic M Ma S Zhang D Kukanja P Xiao Y Spatial profiling of chromatin accessibility in mouse and human tissues Nature 2022 609 7926 375 83 10.1038/s41586-022-05094-1 35978191 PMC9452302 · DOI · Paper page
  155. [174]Liu Y, DiStasio M, Su G, Asashima H, Enninful A, Qin X, et al. Spatial-CITE-seq: spatially resolved high-plex protein and whole transcriptome co-mapping. Res Sq [Preprint]. 2022. PMC10567548 36823353
  156. [176]Hahn O Foltz AG Atkins M Kedir B Moran-Losada P Guldner IH Atlas of the aging mouse brain reveals white matter as vulnerable foci Cell 2023 186 19 4117 4133.e22 10.1016/j.cell.2023.07.027 37591239 PMC10528304 · DOI · Paper page
  157. [177]Lee S Devanney NA Golden LR Smith CT Schwartz JL Walsh AE APOE modulates microglial immunometabolism in response to age, amyloid pathology, and inflammatory challenge Cell Rep 2023 42 3 112196 10.1016/j.celrep.2023.112196 36871219 PMC10117631 · DOI · Paper page
  158. [178]Stoeger T Grant RA McQuattie-Pimentel AC Anekalla KR Liu SS Tejedor-Navarro H Aging is associated with a systemic length-associated transcriptome imbalance Nat Aging 2022 2 12 1191 206 10.1038/s43587-022-00317-6 37118543 PMC10154227 · DOI
  159. [179]Russ JE Haywood ME Lane SL Schoolcraft WB Katz-Jaffe MG Spatially resolved transcriptomic profiling of ovarian aging in mice iScience 2022 25 8 104819 10.1016/j.isci.2022.104819 35996587 PMC9391589 · DOI
  160. [181]Dries R Zhu Q Dong R Eng CL Li H Liu K Giotto: a toolbox for integrative analysis and visualization of spatial expression data Genome Biol 2021 22 1 78 10.1186/s13059-021-02286-2 33685491 PMC7938609 · DOI
  161. [182]Sun S Zhu J Zhou X Statistical analysis of spatial expression patterns for spatially resolved transcriptomic studies Nat Methods 2020 17 2 193 200 10.1038/s41592-019-0701-7 31988518 PMC7233129 · DOI · Paper page
  162. [183]Zhao E Stone MR Ren X Guenthoer J Smythe KS Pulliam T Spatial transcriptomics at subspot resolution with BayesSpace Nat Biotechnol 2021 39 11 1375 84 10.1038/s41587-021-00935-2 34083791 PMC8763026 · DOI
  163. [184]Shang L Zhou X Spatially aware dimension reduction for spatial transcriptomics Nat Commun 2022 13 1 7203 10.1038/s41467-022-34879-1 36418351 PMC9684472 · DOI
  164. [185]LaRocca TJ Cavalier AN Wahl D Repetitive elements as a transcriptomic marker of aging: Evidence in multiple datasets and models Aging Cell 2020 19 7 e13167 10.1111/acel.13167 32500641 PMC7412685 · DOI · Paper page
  165. [186]Kasemeier-Kulesa JC Morrison JA McKinney S Li H Gogol M Hall K Cell-type profiling of the sympathetic nervous system using spatial transcriptomics and spatial mapping of mRNA Dev Dyn 2023 252 8 1130 42 10.1002/dvdy.577 36840366 · DOI
  166. [187]Zhao D Chen S Failures at every level: breakdown of the epigenetic machinery of aging Life Medicine 2022 1 2 81 3 10.1093/lifemedi/lnac016 PMC11749257 39871931 · DOI
  167. [188]Djuric U Rodrigues DC Batruch I Ellis J Shannon P Diamandis P Spatiotemporal proteomic profiling of human cerebral development Mol Cell Proteomics 2017 16 9 1548 62 10.1074/mcp.M116.066274 28687556 PMC5587857 · DOI
  168. [189]Wei J Dai S Yan Y Li S Yang P Zhu R Spatiotemporal proteomic atlas of multiple brain regions across early fetal to neonatal stages in cynomolgus monkey Nat Commun 2023 14 1 3917 10.1038/s41467-023-39411-7 37400444 PMC10317979 · DOI
  169. [190]Hosp F Gutiérrez-Ángel S Schaefer MH Cox J Meissner F Hipp MS Spatiotemporal proteomic profiling of Huntington’s disease inclusions reveals widespread loss of protein function Cell Rep 2017 21 8 2291 303 10.1016/j.celrep.2017.10.097 29166617 PMC5714591 · DOI
  170. [192]Schey KL Wang Z Friedrich MG Garland DL Truscott RJW Spatiotemporal changes in the human lens proteome: Critical insights into long-lived proteins Prog Retin Eye Res 2020 76 100802 10.1016/j.preteyeres.2019.100802 31704338 PMC7328127 · DOI
  171. [193]Budayeva HG Cristea IM Human sirtuin 2 localization, transient interactions, and impact on the proteome point to its role in intracellular trafficking Mol Cell Proteomics 2016 15 10 3107 25 10.1074/mcp.M116.061333 27503897 PMC5054338 · DOI
  172. [194]Zhang J Qiu Z Zhang Y Wang G Hao H Intracellular spatiotemporal metabolism in connection to target engagement Adv Drug Deliv Rev 2023 200 115024 10.1016/j.addr.2023.115024 37516411 · DOI
  173. [195]Schulz C Massberg S Inflammaging aggravates stroke pathology Nat Immunol 2023 24 6 887 8 10.1038/s41590-023-01516-y 37188943 · DOI
  174. [196]Huang Z Merrihew GE Larson EB Park J Plubell D Fox EJ Brain proteomic analysis implicates actin filament processes and injury response in resilience to Alzheimer's disease Nat Commun 2023 14 1 2747 10.1038/s41467-023-38376-x 37173305 PMC10182086 · DOI · Paper page
  175. [197]Walker JM Orr ME Orr TC Thorn EL Christie TD Yokoda RT Spatial proteomics of hippocampal subfield-specific pathology in Alzheimer's disease and primary age-related tauopathy Alzheimers Dement 2024 20 2 783 97 10.1002/alz.13484 37777848 PMC10916977 · DOI
  176. [198]Thul PJ Akesson L Wiking M Mahdessian D Geladaki A Ait Blal H A subcellular map of the human proteome Science 2017 356 6340 eaal3321 10.1126/science.aal3321 28495876 · DOI · Paper page
  177. [199]Hogan KA Zeidler JD Beasley HK Alsaadi AI Alshaheeb AA Chang YC Using mass spectrometry imaging to visualize age-related subcellular disruption Front Mol Biosci 2023 10 906606 10.3389/fmolb.2023.906606 36968274 PMC10032471 · DOI
  178. [200]Simpson CE Ambade AS Harlan R Roux A Graham D Klauer N Spatial and temporal resolution of metabolic dysregulation in the Sugen hypoxia model of pulmonary hypertension Pulm Circ 2023 13 3 e12260 10.1002/pul2.12260 37404901 PMC10315560 · DOI
  179. [201]Zhao C Dong J Deng L Tan Y Jiang W Cai Z Molecular network strategy in multi-omics and mass spectrometry imaging Curr Opin Chem Biol 2022 70 102199 10.1016/j.cbpa.2022.102199 36027696 · DOI
  180. [202]Zheng P Zhang N Ren D Yu C Zhao B Zhang Y Integrated spatial transcriptome and metabolism study reveals metabolic heterogeneity in human injured brain Cell Rep Med 2023 4 6 101057 10.1016/j.xcrm.2023.101057 37263268 PMC10313933 · DOI
  181. [203]Horvath S DNA methylation age of human tissues and cell types Genome Biol. 2013 14 10 R115 10.1186/gb-2013-14-10-r115 24138928 PMC4015143 · DOI · Paper page
  182. [204]Jones PA Functions of DNA methylation: islands, start sites, gene bodies and beyond Nat Rev Genet 2012 13 7 484 92 10.1038/nrg3230 22641018 · DOI · Paper page
  183. [205]Horvath S Raj K DNA methylation-based biomarkers and the epigenetic clock theory of ageing Nat Rev Genet 2018 19 6 371 84 10.1038/s41576-018-0004-3 29643443 · DOI · Paper page
  184. [206]Rodriguez-Muela N Litterman NK Norabuena EM Mull JL Galazo MJ Sun C Single-cell analysis of SMN reveals its broader role in neuromuscular disease Cell Rep 2017 18 6 1484 98 10.1016/j.celrep.2017.01.035 28178525 PMC5463539 · DOI
  185. [207]Zocher S Overall RW Lesche M Dahl A Kempermann G Environmental enrichment preserves a young DNA methylation landscape in the aged mouse hippocampus Nat Commun 2021 12 1 3892 10.1038/s41467-021-23993-1 34162876 PMC8222384 · DOI
  186. [208]Smith ZD Chan MM Mikkelsen TS Gu H Gnirke A Regev A A unique regulatory phase of DNA methylation in the early mammalian embryo Nature 2012 484 7394 339 44 10.1038/nature10960 22456710 PMC3331945 · DOI
  187. [209]Wu Z Lu M Liu D Shi Y Ren J Wang S m6A epitranscriptomic regulation of tissue homeostasis during primate aging Nat Aging 2023 3 6 705 21 10.1038/s43587-023-00393-2 37118553 · DOI
  188. [210]Yi SJ Kim K New insights into the role of histone changes in aging Int J Mol Sci 2020 21 21 8241 10.3390/ijms21218241 33153221 PMC7662996 · DOI
  189. [211]DiTacchio L Le HD Vollmers C Hatori M Witcher M Secombe J Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock Science 2011 333 6051 1881 5 10.1126/science.1206022 21960634 PMC3204309 · DOI
  190. [213]Zhang B Long Q Wu S Xu Q Song S Han L KDM4 orchestrates epigenomic remodeling of senescent cells and potentiates the senescence-associated secretory phenotype Nat Aging 2021 1 5 454 72 10.1038/s43587-021-00063-1 34263179 PMC8277122 · DOI
  191. [215]Mescher AL Macrophages and fibroblasts during inflammation and tissue repair in models of organ regeneration Regeneration (Oxf) 2017 4 2 39 53 10.1002/reg2.77 28616244 PMC5469729 · DOI
  192. [216]Wang Z Zhao H Tang X Meng T Khutsishvili D Xu B CNS organoid surpasses cell-laden microgel assembly to promote spinal cord injury repair Research (Wash D C) 2022 2022 9832128 36061824 PMC9394056
  193. [217]You WJ Xu ZY Chen WT Yang X Liu SQ Wang LY Cellular and transcriptional dynamics during brown adipose tissue regeneration under acute injury Research 2023 6 0268 10.34133/research.0268 38434240 PMC10907023 · DOI
  194. [218]Brockes JP Kumar A Comparative aspects of animal regeneration Annu Rev Cell Dev Biol 2008 24 525 49 10.1146/annurev.cellbio.24.110707.175336 18598212 · DOI
  195. [219]Maddaluno L Urwyler C Werner S Fibroblast growth factors: key players in regeneration and tissue repair Development 2017 144 22 4047 60 10.1242/dev.152587 29138288 · DOI
  196. [220]Jiao L Liu Y Yu XY Pan X Zhang Y Tu J Ribosome biogenesis in disease: new players and therapeutic targets Signal Transduct Target Ther 2023 8 1 15 10.1038/s41392-022-01285-4 36617563 PMC9826790 · DOI
  197. [221]Fu M Hu Y Lan T Guan KL Luo T Luo M The Hippo signalling pathway and its implications in human health and diseases Signal Transduct Target Ther 2022 7 1 376 10.1038/s41392-022-01191-9 36347846 PMC9643504 · DOI
  198. [222]Li G Han Q Lu P Zhang L Zhang Y Chen S Construction of dual-biofunctionalized chitosan/collagen scaffolds for simultaneous neovascularization and nerve regeneration Research (Wash D C) 2020 2020 2603048 32851386 PMC7436332
  199. [223]Wang F Ye Y Zhang Z Teng W Sun H Chai X PDGFR in PDGF-BB/PDGFR signaling pathway does orchestrates osteogenesis in a temporal manner Research (Wash D C) 2023 6 0086 37223474 PMC10202377
  200. [224]Chen Y Ren B Yang J Wang H Yang G Xu R The role of histone methylation in the development of digestive cancers: a potential direction for cancer management Signal Transduct Target Ther 2020 5 1 143 10.1038/s41392-020-00252-1 32747629 PMC7398912 · DOI

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Authors
Chu, L.-X., Wang, W.-J., Gu, X.-P., Wu, P., Gao, C., Zhang, Q., Wu, J., Jiang, D.-W., Huang, J.-Q., Ying, X.-W., Shen, J.-M., Jiang, Y., Luo, L.-H., Xu, J.-P., Ying, Y.-B., Chen, H.-M., Fang, A., Feng, Z.-Y., An, S.-H., Li, X.-K., & Wang, Z.-G.
Affiliations
  • Wenzhou Medical University (CN)
  • State Key Laboratory of Digital Medical Engineering (CN)
  • University of Tennessee Health Science Center (US)
ORCID
Venue
Military Medical Research
Publisher
Elsevier BV
Published
2024-05-27
Volume
11
Issue
1
Pages
31-31
ISSN
2054-9369 (ISSN-L)
DOI
10.1186/s40779-024-00537-4
PMC
PMC11129507
OpenAlex
W4399053043
Cited by
29
References
29
Citations by year
2026: 8 · 2025: 19 · 2024: 2
FWCI
1.19
Type
journal article
Language
en
Open access
Licence
Locations
  • Military Medical Research (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China (82271629, 82301790)
  • Leading Innovative and Entrepreneur Team Introduction Program of Zhejiang (2023R01002)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords
aging, regenerative medicine, spatial transcriptomics, spatial proteomics, spatial metabolomics, spatial epigenomics, molecular landscape, tissue dynamics, cellular interactions, signaling pathways
MeSH terms
Multiomics, Aging, Humans, Genomics, Proteomics, Regenerative Medicine, Metabolomics, Epigenomics

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