Ukr.Biochem.J. 2020; Volume 92, Issue 5, Sep-Oct, pp. 62-69

doi: https://doi.org/10.15407/ubj92.05.062

DNA loop domain rearrangements in blast transformed human lymphocytes and lymphoid leukaemic Jurkat T cells

K. Afanasieva1, V. Olefirenko1, A. Martyniak1,
L. Lukash2, A. Sivolob1*

1Taras Shevchenko National University of Kyiv, Ukraine;
2Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine, Kyiv;
*e-mail: sivolob@univ.kiev.ua

Received: 06 April 2020; Accepted: 25 June 2020

Chromatin loops are important elements of both chromatin higher-order structure and transcription regulation system. Our previous works have shown that several features of the loop domain organization could be investigated by single cell gel electrophoresis (the comet assay) using the kinetic approach. In this study we applied this technique to study DNA loop domain organization in lymphoid cells: human lymphocytes, lymphoblasts cultivated during 24 h and 44 h, and T cells of Jurkat cell line. Two features of the loop domain organization were found to depend on the cell functional state. First, DNA fraction in the loops of large sizes (more than ~200 kb) was essentially increased in proliferating (de-differentiated) cells in comparison with terminally differentiated lymphocytes. Second, the linear density of the loops not larger than ~200 kb was decreased in transcriptionally active cells and was increased upon their inactivation.

Keywords: , , , ,


References:

  1. Dekker J, Marti-Renom MA, Mirny LA. Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Nat Rev Genet. 2013;14(6):390-403. PubMed, PubMedCentral, CrossRef
  2. Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID,  Robinson JT, Sanborn AL, Machol I, Omer AD, Lander ES, Aiden FL. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014;159(7):1665-1680. PubMed, PubMedCentral, CrossRef
  3. Dekker J, Mirny L. The 3D Genome as moderator of chromosomal communication. Cell. 2016;164(6):1110-1121. PubMed, PubMedCentral, CrossRef
  4. Hansen AS, Cattoglio C, Darzacq X, Tjian R.  Recent evidence that TADs and chromatin loops are dynamic structures. Nucleus. 2018;9(1):20-32. PubMed, PubMedCentral, CrossRef
  5. Sanborn Al, Rao SSP, Huang SC, Durand NC, Huntley MH, Jewett AI, Bochkov ID, Chinnappan D, Cutkosky A, Li J, Geeting KP, Gnirke A, Melnikov A, McKenna D, Stamenova EK, Lander ES, Aiden EL.  Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc Natl Acad Sci USA. 2015;112(47):E6456-E6465. PubMed, PubMedCentral, CrossRef
  6. Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. Formation of Chromosomal Domains by Loop Extrusion. Cell Rep. 2016;15(9):2038-2049. PubMed, PubMedCentral, CrossRef
  7. Nora EP, Goloborodko A, Valton AL, Gibcus JH, Uebersohn A, Abdennur N, Dekker J, Mirny LA, Bruneau BG. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell. 2017;169(5):930-944. PubMed, PubMedCentral, CrossRef
  8. Rao SSP, Huang SC, St Hilaire BG, Engreitz JM, Perez EM, Kieffer-Kwon KR, Sanborn AL, Johnstone SE, Bascom GD, Bochkov ID, Huang X, Shamim MS, Shin J, Turner D, Ye Z, Omer AD, Robinson JT, Schlick T, Bernstein BE, Casellas R, Lander ES, Aiden EL. Cohesin loss eliminates all loop domains. Cell. 2017;171(2):305-320. PubMed, PubMedCentral, CrossRef
  9. Wutz G, Várnai C, Nagasaka K, Cisneros DA, Stocsits RR, Tang W, Schoenfelder S, Jessberger G, Muhar M, Hossain MJ, Walther N, Koch B, Kueblbeck M, Ellenberg J, Zuber J, Fraser P, Peters JM. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. EMBO J. 2017;36(24):3573-3599. PubMed, PubMedCentral, CrossRef
  10. Vian L, Pękowska A, Rao SSP, Kieffer-Kwon KR, Jung S, Baranello L, Huang  SC, El Khattabi L, Dose M, Pruett N, Sanborn AL, Canela A, Maman Y, Oksanen A, Resch W, Li X, Lee B, Kovalchuk AL, Tang Z, Nelson S, Di Pierro M, Cheng RR, I Machol, B Glenn St Hilaire, Durand NC, Shamim MS, Stamenova EK, Onuchic JN, Ruan Y, Nussenzweig A, Levens D, Aiden EL, Casellas R. The energetics and physiological impact of cohesin extrusion. Cell. 2018;175(1):292-294. PubMed, PubMedCentral, CrossRef
  11. Merkenschlager M, Nora EP. CTCF and cohesin in genome folding and transcriptional gene regulation. Annu Rev Genomics Hum Genet. 2016;17:17-43.
    PubMed, CrossRef
  12. Hansen AS, Hsieh TS, Cattoglio C, Pustova I, Saldaña-Meyer R, Reinberg D, Darzacq X, Tjian R.  Distinct classes of chromatin loops revealed by deletion of an RNA-binding region in CTCF. Mol Cell. 2019;76(3):395-411. PubMed, PubMedCentral, CrossRef
  13. Tang Z, Luo OJ, Li X, Zheng M, Zhu JJ, Szalaj P, Trzaskoma P, Magalska A,  Wlodarczyk J, Ruszczycki B, Michalski P, Piecuch E, Wang P, Wang D, Tian SZ, Penrad-Mobayed M, Sachs LM, Ruan X, Wei CL, Liu ET, Wilczynski GM, Plewczynski D, Li G, Ruan Y. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell. 2015;163(7):1611-1627. PubMed, PubMedCentral, CrossRef
  14. Ji X, Dadon DB, Powell BE, Fan ZP, Borges-Rivera D, Shachar S, Weintraub AS, Hnisz D, Pegoraro G, Lee TI, Misteli T, Jaenisch R, Young RA. 3D chromosome regulatory landscape of human pluripotent cells. Cell Stem Cell. 2016;18(2):262-275. PubMed, PubMedCentral, CrossRef
  15. Kieffer-Kwon KR, Nimura K, Rao SSP, Xu J, Jung S, Pekowska A, Dose M, Stevens E, Mathe E, Dong P, Huang SC, Ricci MA, Baranello L, Zheng Y, Ardori FT, Resch  W, Stavreva D, Nelson S, McAndrew M, Casellas A, Finn E, Gregory C, St Hilaire BG, Johnson SM, Dubois W, Cosma MP, Batchelor E, Levens D, Phair RD, Misteli T, Tessarollo L, Hager G, Lakadamyali M, Liu Z, Floer M, Shroff H, Aiden EL, Casellas R. Myc regulates chromatin decompaction and nuclear architecture during B cell activation. Mol Cell. 2017;67(4):566-578. PubMed, PubMedCentral, CrossRef
  16. Bonev B, Cohen NM, Szabo Q, Fritsch L, Papadopoulos GL, Lubling Y, Xu X, Lv X, Hugnot JP, Tanay A, Cavalli G. Multiscale 3D genome rewiring during mouse neural development. Cell. 2017;171(3):557-572. PubMed, PubMedCentral, CrossRef
  17. Pękowska A, Klaus B, Xiang W, Severino J, Daigle N, Klein FA, Oleś M, Casellas R, Ellenberg J, Steinmetz LM, Bertone P, Huber W. Gain of CTCF-anchored chromatin loops marks the exit from naive pluripotency. Cell Syst. 2018;7(5):482-495. PubMed, PubMedCentral, CrossRef
  18. Afanasieva K, Sivolob A. Physical principles and new applications of comet assay. Biophys Chem. 2018;238:1-7. PubMed, CrossRef
  19. Afanasieva K, Zazhytska M, Sivolob A. Kinetics of comet formation in single-cell gel electrophoresis: loops and fragments. Electrophoresis. 2010;31(3):512-519. PubMed, CrossRef
  20. Afanasieva K, Chopei M, Zazhytska M, Vikhreva M, Sivolob A. DNA loop domain organization as revealed by single-cell gel electrophoresis. Biochim Biophys Acta. 2013;1833(12):3237-3244. PubMed, CrossRef
  21. Afanasieva K, Chopei M, Sivolob A. Single nucleus versus single-cell gel electrophoresis: kinetics of DNA track formation. Electrophoresis. 2015;36(7-8):973-977. PubMed, CrossRef
  22. Afanasieva K, Chopei M, Lozovik A, Semenova A, Lukash L, Sivolob A. DNA loop domain organization in nucleoids from cells of different types. Biochem Biophys Res Commun. 2017;483(1):142-146. PubMed, CrossRef
  23. Kaplan O, Aebersold P, Cohen JS. Metabolism of peripheral lymphocytes, interleukin-2-activated lymphocytes and tumor-infiltrating lymphocytes from 31P NMR studies. FEBS Lett. 1989;258(1):55-58. PubMed, CrossRef
  24. Mookerjee BK, Pauly JL.  Mitogenic effect of interleukin-2 on unstimulated human T cells: an editorial review. J Clin Lab Anal. 1990;4(2):138-149. PubMed, CrossRef
  25. Mzali R, Seguin L, Liot C, Auger A, Pacaud P, Loirand G, Thibault C, Pierre J, Bertoglio J. Regulation of Rho signaling pathways in interleukin-2-stimulated human T-lymphocytes. FASEB J. 2005;19(13):1911-1913. PubMed, CrossRef
  26. Bachmann MF, Oxenius A. Interleukin 2: from immunostimulation to immunoregulation and back again. EMBO Rep. 2007;8(12): 1142-1148. PubMed, PubMedCentral, CrossRef
  27. Abraham RT, Weiss A. Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat Rev Immunol. 2004;4(4):301-308. PubMed, CrossRef

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License.