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3D genomics mainly focuses on the 3D position of single genes at the cell level, while spatial genomics focuses more on the tissue level. In this exciting new era of 3D/spatial genomics, half-century old FISH and its derivative methods, including Tn5-FISH, play important roles. In this review, we introduce the Tn5-FISH we developed recently, and present six different applications published by our collaborators and us, based on (Tn5-)FISH, which can be either general BAC clone-based FISH or Tn5-FISH. In these interesting cases, (Tn5-)FISH demonstrated its vigorous ability of targeting sub-chromosomal structures across different diseases and cell lines (leukemia, mESCs (mouse embryonic stem cells), and differentiation cell lines). Serving as an effective tool to image genomic structures at the kilobase level, Tn5-FISH holds great potential to detect chromosomal structures in a high-throughput manner, thus bringing the dawn for new discoveries in the great era of 3D/spatial genomics.
Abbas A, He X, Niu J, Zhou B, Zhu G, Ma T, Song J, Gao J, Zhang MQ, Zeng J (2019) Integrating Hi-C and FISH data for modeling of the 3D organization of chromosomes. Nat Commun 10(1): 2049. https://doi.org/10.1038/s41467-019-10005-6
Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Bornholdt J, Boyd M, Chen Y, Zhao X, Schmidl C, Suzuki T, Ntini E, Arner E, Valen E, Li K, Schwarzfischer L, Glatz D, Raithel J, Lilje B, Rapin N, Bagger FO, Jørgensen M, Andersen PR, Bertin N, Rackham O, Burroughs AM, Baillie JK, Ishizu Y, Shimizu Y, Furuhata E, Maeda S, Negishi Y, Mungall CJ, Meehan TF, Lassmann T, Itoh M, Kawaji H, Kondo N, Kawai J, Lennartsson A, Daub CO, Heutink P, Hume DA, Jensen TH, Suzuki H, Hayashizaki Y, Müller F, Forrest ARR, Carninci P, Rehli M, Sandelin A, The FC (2014) An atlas of active enhancers across human cell types and tissues. Nature 507(7493): 455−461
Beliveau BJ, Boettiger AN, Avendaño MS, Jungmann R, McCole RB, Joyce EF, Kim-Kiselak C, Bantignies F, Fonseka CY, Erceg J, Hannan MA, Hoang HG, Colognori D, Lee JT, Shih WM, Yin P, Zhuang X, Wu C-t (2015) Single-molecule super-resolution imaging of chromosomes and in situ haplotype visualization using Oligopaint FISH probes. Nat Commun 6(1): 7147. https://doi.org/10.1038/ncomms8147
Beliveau BJ, Joyce EF, Apostolopoulos N, Yilmaz F, Fonseka CY, McCole RB, Chang Y, Li JB, Senaratne TN, Williams BR, Rouillard J-M, Wu C-t (2012) Versatile design and synthesis platform for visualizing genomes with Oligopaint FISH probes. Proc Natl Acad Sci USA 109(52): 21301−21306
Beliveau BJ, Kishi JY, Nir G, Sasaki HM, Saka SK, Nguyen SC, Wu C-t, Yin P (2018) OligoMiner provides a rapid, flexible environment for the design of genome-scale oligonucleotide in situ hybridization probes. Proc Natl Acad Sci USA 115(10): E2183−E2192
Boettiger AN, Bintu B, Moffitt JR, Wang S, Beliveau BJ, Fudenberg G, Imakaev M, Mirny LA, Wu C-t, Zhuang X (2016) Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 529(7586): 418−422
Britten O, Ragusa D, Tosi S, Mostafa Kamel Y (2019) MLL-rearranged acute leukemia with t(4; 11)(q21; q23) — Current treatment options. Is there a role for CAR-T cell therapy? Cells 8(11): 1341. https://doi.org/10.3390/cells8111341
Cavalli G, Misteli T (2013) Functional implications of genome topology. Nat Struct Mol Biol 20(3): 290−299
Chi X, Chatterjee PK, Wilson III W, Zhang S-X, DeMayo FJ, Schwartz RJ (2005) Complex cardiac Nkx2-5 gene expression activated by noggin-sensitive enhancers followed by chamber-specific modules. Proc Natl Acad Sci USA 102(38): 13490−13495
Dekker J, Mirny L (2016) The 3D Genome as Moderator of Chromosomal Communication. Cell 164(6): 1110−1121
Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295(5558): 1306−1311
Danielian PS, Echelard Y, Vassileva G, McMahon AP (1997) A 5.5-kb enhancer is both necessary and sufficient for regulation of Wnt-1transcription in vivo. Develop Biol 192(2): 300−309
Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485(7398): 376−380
Fabre PJ, Benke A, Joye E, Nguyen Huynh TH, Manley S, Duboule D (2015) Nanoscale spatial organization of the <i>HoxD</i> gene cluster in distinct transcriptional states. Proc Natl Acad Sci USA 112(45): 13964−13969
Faerman A, Goldhamer DJ, Puzis R, Emerson CP, Shani M (1995) The distal human myoD enhancer sequences direct unique muscle-specific patterns of lacZ expression during mouse development. Dev Biol 171(1): 27−38
Fudenberg G, Imakaev M (2017) FISH-ing for captured contacts: towards reconciling FISH and 3C. Nat Methods 14(7): 673−678
Hnisz D, Abraham BJ, Lee TI, Lau A, Saint-André V, Sigova AA, Hoke HA, Young RA (2013) Super-enhancers in the control of cell identity and disease. Cell 155(4): 934−947
Kassar-Duchossoy L, Gayraud-Morel B, Gomès D, Rocancourt D, Buckingham M, Shinin V, Tajbakhsh S (2004) Mrf4 determines skeletal muscle identity in Myf5: Myod double-mutant mice. Nature 431(7007): 466−471
Kim UJ, Shizuya H, Kang HL, Choi SS, Garrett CL, Smink LJ, Birren BW, Korenberg JR, Dunham I, Simon MI (1996) A bacterial artificial chromosome-based framework contig map of human chromosome 22q. Proc Natl Acad Sci USA 93(13): 6297−6301
Li Y, He Y, Liang Z, Wang Y, Chen F, Djekidel MN, Li G, Zhang X, Xiang S, Wang Z, Gao J, Zhang MQ, Chen Y (2018) Alterations of specific chromatin conformation affect ATRA-induced leukemia cell differentiation. Cell Death Dis 9(2): 200. https://doi.org/10.1038/s41419-017-0173-6
Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326(5950): 289−293
Ma Y, Guo W, Mou Q, Shao X, Lyu M, Garcia V, Kong L, Lewis W, Ward C, Yang Z (2023) Spatial imaging of glycoRNA in single cells with ARPLA. Nat Biotechnol. https://doi.org/10.1038/s41587-023-01801-z
Megeney LA, Kablar B, Garrett K, Anderson JE, Rudnicki MA (1996) MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev 10(10): 1173−1183
Montarras D, Lindon C, Pinset C, Domeyne P (2000) Cultured myf5 null and myoD null muscle precursor cells display distinct growth defects. Biol Cell 92(8-9): 565−572
Murmann AE, Gao J, Encinosa M, Gautier M, Peter ME, Eils R, Lichter P, Rowley JD (2005) Local gene density predicts the spatial position of genetic loci in the interphase nucleus. Exp Cell Res 311(1): 14−26
Niu J, Zhang X, Li G, Yan P, Yan Q, Dai Q, Jin D, Shen X, Wang J, Zhang MQ, Gao J (2020) A novel cytogenetic method to image chromatin interactions at subkilobase resolution: Tn5 transposase-based fluorescence in situ hybridization. J Genet Genomics 47(12): 727−735
Ott MO, Bober E, Lyons G, Arnold H, Buckingham M (1991) Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111(4): 1097−1107
Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, Sanborn AL, Machol I, Omer AD, Lander ES (2014) A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159(7): 1665−1680
Rowley MJ, Corces VG (2018) Organizational principles of 3D genome architecture. Nat Rev Genet 19(12): 789−800
Rudnicki MA, Braun T, Hinuma S, Jaenisch R (1992) Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71(3): 383−390
Rudnicki MA, Schnegelsberg PNJ, Stead RH, Braun T, Arnold H-H, Jaenisch R (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75(7): 1351−1359
Sabourin LA, Girgis-Gabardo A, Seale P, Asakura A, Rudnicki MA (1999) Reduced differentiation potential of primary MyoD−/− myogenic cells derived from adult skeletal muscle. J Cell Biol 144(4): 631−643
Sassoon D, Lyons G, Wright WE, Lin V, Lassar A, Weintraub H, Buckingham M (1989) Expression of two myogenic regulatory factors myogenin and MyoDl during mouse embryogenesis. Nature 341(6240): 303−307
Schmidt TL, Beliveau BJ, Uca YO, Theilmann M, Da Cruz F, Wu C-T, Shih WM (2015) Scalable amplification of strand subsets from chip-synthesized oligonucleotide libraries. Nat Commun 6(1): 8634. https://doi.org/10.1038/ncomms9634
Shachar S, Voss Ty C, Pegoraro G, Sciascia N, Misteli T (2015) Identification of gene positioning factors using high-throughput imaging mapping. Cell 162(4): 911−923
Shizuya H, Kouros-Mehr H (2001) The development and applications of the bacterial artificial chromosome cloning system. Keio J Med 50(1): 26−30
Tajbakhsh S, Bober E, Babinet C, Pournin S, Arnold H, Buckingham M (1996) Gene targeting the myf-5 locus with nlacZ reveals expression of this myogenic factor in mature skeletal muscle fibres as well as early embryonic muscle. 3.0.CO;2-D">Dev Dyn 206(3): 291−300
Wang R, Chen F, Chen Q, Wan X, Shi M, Chen AK, Ma Z, Li G, Wang M, Ying Y, Liu Q, Li H, Zhang X, Ma J, Zhong J, Chen M, Zhang MQ, Zhang Y, Chen Y, Zhu D (2022) MyoD is a 3D genome structure organizer for muscle cell identity. Nat Commun 13(1): 205. https://doi.org/10.1038/s41467-021-27865-6
Wei C, Jia L, Huang X, Tan J, Wang M, Niu J, Hou Y, Sun J, Zeng P, Wang J, Qing L, Ma L, Liu X, Tang X, Li F, Jiang S, Liu J, Li T, Fan L, Sun Y, Gao J, Li C, Ding J (2022) CTCF organizes inter-Compartment A interactions through RYBP-dependent phase separation. Cell Res 32(8): 744−760
Whyte Warren A, Orlando David A, Hnisz D, Abraham Brian J, Lin Charles Y, Kagey Michael H, Rahl Peter B, Lee Tong I, Young Richard A (2013) Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153(2): 307−319
Yan P, Lu JY, Niu J, Gao J, Zhang MQ, Yin Y, Shen X (2020) LncRNA Platr22 promotes super-enhancer activity and stem cell pluripotency. J Mol Cell Biol 13(4): 295−313
Zhang J, Han B, Li X, Bies J, Jiang P, Koller RP, Wolff L (2016) Distal regulation of c-myb expression during IL-6-induced differentiation in murine myeloid progenitor M1 cells. Cell Death Dis 7(9): e2364. https://doi.org/10.1038/cddis.2016.267
Ziemin-van der Poel S, McCabe NR, Gill HJ, Espinosa R, Patel Y, Harden A, Rubinelli P, Smith SD, LeBeau MM, Rowley JD (1991) Identification of a gene, MLL, that spans the breakpoint in 11q23 translocations associated with human leukemias. Proc Natl Acad Sci USA 88(23): 10735−10739
Zotova O, Lukianova A, Valchuk M, Karol YS, Shalay O, Novak V, Loginsky V (2021) 11q23/MLL rearrangements in adult acute leukemia. Exp Oncol 43: 229−233
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