1932

Abstract

DNA molecules with a total length of two meters contain the genetic information in every cell in our body. To control access to the genes, to organize its spatial structure in the nucleus, and to duplicate and faithfully separate the genetic material, the cell makes use of sophisticated physical mechanisms. Base pair sequences multiplex various layers of information, chromatin remodelers mobilize nucleosomes via twist defects, loop extruders create a system of nonconcatenated rings to spatially organize chromatin, and biomolecular condensates concentrate proteins and nucleic acids in specialized membraneless compartments. In this review, we discuss the current state of understanding of some of these mechanisms that influence the organization of the genetic material in space and time.

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2023-03-10
2024-06-12
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Literature Cited

  1. 1.
    Schiessel H. 2003. J. Phys. Condens. Matter 15:R699–774
    [Google Scholar]
  2. 2.
    Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Nature 389:251–60
    [Google Scholar]
  3. 3.
    Ngo TTM, Zhang Q, Zhou R, Yodh JG, Ha T. 2015. Cell 160:1135–44
    [Google Scholar]
  4. 4.
    Eslami-Mossallam B, Schram RD, Tompitak M, van Noort J, Schiessel H. 2016. PLOS ONE 11:e0156905
    [Google Scholar]
  5. 5.
    Hall MA, Shundrovsky A, Bai L, Fulbright RM, Lis JT, Wang MD. 2009. Nat. Struct. Mol. Biol. 16:124–29
    [Google Scholar]
  6. 6.
    Bustamante C, Marko JF, Siggia ED, Smith S. 1994. Science 265:1599–600
    [Google Scholar]
  7. 7.
    Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D et al. 2009. Nature 458:362–66
    [Google Scholar]
  8. 8.
    Lowary PT, Widom J. 1997. PNAS 94:1183–88
    [Google Scholar]
  9. 9.
    Satchwell SC, Drew HR, Travers AA. 1986. J. Mol. Biol. 191:659–75
    [Google Scholar]
  10. 10.
    Segal E, Fondufe-Mittendorf Y, Chen L, Thåström A, Field Y et al. 2006. Nature 442:772–78
    [Google Scholar]
  11. 11.
    Jin H, Rube HT, Song JS 2016. Nucl. Acids Res. 44:2047–57
    [Google Scholar]
  12. 12.
    Tillo D, Hughes TR 2009. BMC Bioinform. 10:442
    [Google Scholar]
  13. 13.
    Locke G, Tolkunov D, Moqtaderi Z, Struhl K, Morozov AV. 2010. PNAS 107:20998–1003
    [Google Scholar]
  14. 14.
    Struhl K, Segal E. 2013. Nat. Struct. Mol. Biol. 20:267–73
    [Google Scholar]
  15. 15.
    Drillon G, Audit B, Argoul F, Arneodo A 2016. BMC Genom. 17:526
    [Google Scholar]
  16. 16.
    Tompitak M, Vaillant C, Schiessel H. 2017. Biophys. J. 112:505–11
    [Google Scholar]
  17. 17.
    Olson WK, Gorin AA, Lu X-J, Hock LM, Zhurkin VB. 1998. PNAS 95:11163–68
    [Google Scholar]
  18. 18.
    Hinckley DM, Freeman GS, Whitmer JK, de Pablo JJ. 2013. J. Phys. Chem. 139:144903
    [Google Scholar]
  19. 19.
    Lankaš F, Šponer J, Langowski J, Cheatham TE III 2003. Biophys. J. 85:2872–83
    [Google Scholar]
  20. 20.
    Morozov AV, Fortney K, Gaykalova DA, Studitsky VM, Widom J, Siggia ED. 2009. Nucl. Acids Res. 37:4707–22
    [Google Scholar]
  21. 21.
    Freeman GS, Lequieu JP, Hinckley DM, Whitmer JK, de Pablo JJ. 2014. Phys. Rev. Lett. 113:168101
    [Google Scholar]
  22. 22.
    Zuiddam M, Everaers R, Schiessel H. 2017. Phys. Rev. E 96:052412
    [Google Scholar]
  23. 23.
    Neipel J, Brandani G, Schiessel H. 2020. Phys. Rev. E 101:022405
    [Google Scholar]
  24. 24.
    Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. 2013. Nat. Methods 10:1213–18
    [Google Scholar]
  25. 25.
    Brogaard K, Xi L, Wang JP, Widom J. 2012. Nature 486:496–501
    [Google Scholar]
  26. 26.
    Kelly TK, Liu Y, Lay FD, Liang G, Berman BP, Jones PA. 2012. Genome Res. 22:2497–506
    [Google Scholar]
  27. 27.
    Kornberg RD, Stryer L. 1988. Nucl. Acids Res. 16:6677–90
    [Google Scholar]
  28. 28.
    Chevereau G, Palmeira L, Thermes C, Arneodo A, Vaillant C. 2009. Phys. Rev. Lett. 103:188103
    [Google Scholar]
  29. 29.
    Tillo D, Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ et al. 2010. PLOS ONE 5:e9129
    [Google Scholar]
  30. 30.
    Vavouri T, Lehner B. 2011. PLOS Genet. 7:e1002036
    [Google Scholar]
  31. 31.
    Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. 2009. Nature 460:473–78
    [Google Scholar]
  32. 32.
    Eslami-Mossallam B, Schiessel H, van Noort J. 2016. Adv. Colloid Interface Sci. 232:101–13
    [Google Scholar]
  33. 33.
    Fierz B, Poirier MG. 2019. Annu. Rev. Biophys. 48:321–45
    [Google Scholar]
  34. 34.
    Polach KJ, Widom J. 1995. J. Mol. Biol. 254:130–49
    [Google Scholar]
  35. 35.
    Anderson JD, Lowary PT, Widom J. 2001. J. Mol. Biol. 307:977–85
    [Google Scholar]
  36. 36.
    Li G, Widom J. 2004. Nat. Struct. Mol. Biol. 11:763–69
    [Google Scholar]
  37. 37.
    Li G, Levitus M, Bustamante C, Widom J. 2005. Nat. Struct. Mol. Biol. 12:46–53
    [Google Scholar]
  38. 38.
    Kelbauskas L, Chan N, Bash R, Yodh J, Woodbury N, Lohr D. 2007. Biochemistry 46:2239–48
    [Google Scholar]
  39. 39.
    Koopmans WJA, Brehm A, Logie C, Schmidt T, van Noort J. 2007. J. Fluoresc. 17:785–95
    [Google Scholar]
  40. 40.
    Moyle-Heyrman G, Tims HS, Widom J. 2011. J. Mol. Biol. 412:634–46
    [Google Scholar]
  41. 41.
    Tims HS, Gurunathan K, Levitus M, Widom J. 2011. J. Mol. Biol. 411:430–48
    [Google Scholar]
  42. 42.
    Gansen A, Felekyan S, Kühnemuth R, Lehmann K, Tóth K et al. 2018. Nat. Commun. 9:4628
    [Google Scholar]
  43. 43.
    Konrad SF, Vanderlinden W, Frederickx W, Brouns T, Menze BH et al. 2021. Nanoscale 13:5435–47
    [Google Scholar]
  44. 44.
    Konrad SF, Vanderlinden W, Lipfert J. 2022. Biophys. J. 121:841–51
    [Google Scholar]
  45. 45.
    Prinsen P, Schiessel H. 2010. Biochimie 92:1722–28
    [Google Scholar]
  46. 46.
    Anderson JD, Widom J. 2001. Mol. Cell. Biol. 21:3830–39
    [Google Scholar]
  47. 47.
    Kelbauskis L, Woodbury N, Lohr D. 2009. Biochem. Cell Biol. 87:323–35
    [Google Scholar]
  48. 48.
    Gansen A, Tóth, Schwarz N, Langowski J 2009. J. Phys. Chem. B 113:2604–13
    [Google Scholar]
  49. 49.
    Tóth K, Böhm V, Sellmann C, Danner M, Hanne J et al. 2013. Cytometry A 83:839–46
    [Google Scholar]
  50. 50.
    Lowary PT, Widom J. 1998. J. Mol. Biol. 276:19–42
    [Google Scholar]
  51. 51.
    Mauney AW, Tokuda JM, Gloss LM, Gonzalez O, Pollack M. 2018. Biophys. J. 115:773–81
    [Google Scholar]
  52. 52.
    van Deelen K, Schiessel H, de Bruin L. 2020. Biophys. J. 118:2297–308
    [Google Scholar]
  53. 53.
    Polach KJ, Widom J. 1996. J. Mol. Biol. 258:800–12
    [Google Scholar]
  54. 54.
    Culkin J, de Bruin L, Tompitak M, Phillips R, Schiessel H. 2017. Eur. Phys. J. E 40:106
    [Google Scholar]
  55. 55.
    Winogradoff D, Aksimentiev A. 2019. J. Mol. Biol. 431:323–35
    [Google Scholar]
  56. 56.
    Armeev GA, Kniazeva AS, Komarova GA, Kirpichnikov MP, Shaytan AK. 2021. Nat. Commun. 12:2387
    [Google Scholar]
  57. 57.
    Brower-Toland BD, Smith CL, Yeh RC, Lis JT, Peterson CL, Wang MD. 2002. PNAS 99:1960–65
    [Google Scholar]
  58. 58.
    Kulić IM, Schiessel H. 2004. Phys. Rev. Lett. 92:228101
    [Google Scholar]
  59. 59.
    Wocjan T, Klenin K, Langowski J. 2009. J. Phys. Chem. B 113:2639–46
    [Google Scholar]
  60. 60.
    Sudhanshu B, Mihardja S, Koslover EF, Mehraeen S, Bustamante C, Spakowitz AJ. 2011. PNAS 108:1885–90
    [Google Scholar]
  61. 61.
    Ettig R, Kepper N, Stehr R, Wedemann G, Rippe K. 2011. Biophys. J. 101:1999–2008
    [Google Scholar]
  62. 62.
    Mollazadeh-Beidokhti L, Mohammad-Rafiee F, Schiessel H. 2012. Biophys. J. 102:2235–40
    [Google Scholar]
  63. 63.
    Lanzani G, Schiessel H. 2012. Europhys. Lett. 100:48001
    [Google Scholar]
  64. 64.
    Mochrie SGJ, Mack AH, Schlingwein DJ, Collins R, Kamenetska M, Regan L 2013. Phys. Rev. E 87:012710
    [Google Scholar]
  65. 65.
    Mack AH, Schlingman DJ, Salinas RD, Regan L, Mochrie SGJ 2015. J. Phys. Condens. Matter 27:064106
    [Google Scholar]
  66. 66.
    Lequieu J, Córdoba A, Schwartz DC, de Pablo JJ. 2016. ACS Cent. Sci. 2:660–66
    [Google Scholar]
  67. 67.
    Khodabandeh F, Fatemi H, Mohammad-Rafiee F. 2020. Soft Matter 16:4806–13
    [Google Scholar]
  68. 68.
    Reddy G, Thirumalai D. 2021. Nucl. Acids Res. 49:4907–18
    [Google Scholar]
  69. 69.
    de Bruin L, Tompitak M, Eslami-Mossallam B, Schiessel H. 2016. J. Phys. Chem. B 120:5855–63
    [Google Scholar]
  70. 70.
    Tompitak M, de Bruin L, Eslami-Mossallam B, Schiessel H. 2017. Phys. Rev. E 95:052402
    [Google Scholar]
  71. 71.
    Durkin SG, Glover TW. 2007. Annu. Rev. Genet. 41:169–92
    [Google Scholar]
  72. 72.
    Chan KL, Palmai-Pallag T, Ying S, Hickson ID 2009. Nat. Cell Biol. 11:753–60
    [Google Scholar]
  73. 73.
    Biebricher A, Hirano S, Enzlin JH, Wiechens N, Streicher WW et al. 2013. Mol. Cell 51:691–701
    [Google Scholar]
  74. 74.
    Meersseman G, Pennings S, Bradbury EM. 1992. EMBO J. 11:2951–59
    [Google Scholar]
  75. 75.
    Kulić IM, Schiessel H. 2003. Phys. Rev. Lett. 91:148103
    [Google Scholar]
  76. 76.
    Mohammad-Rafiee F, Kulić IM, Schiessel H. 2004. J. Mol. Biol. 344:47–58
    [Google Scholar]
  77. 77.
    Brandani GB, Niina T, Tan C, Takada S. 2018. Nucl. Acids Res. 46:2788–801
    [Google Scholar]
  78. 78.
    Schiessel H, Widom J, Bruinsma RF, Gelbart WM. 2001. Phys. Rev. Lett. 86:4414–17
    [Google Scholar]
  79. 79.
    Kulić IM, Schiessel H. 2003. Biophys. J. 84:3197–211
    [Google Scholar]
  80. 80.
    Lequieu J, Schwartz DC, de Pablo JJ. 2017. PNAS 114:E9197–205
    [Google Scholar]
  81. 81.
    Niina T, Brandani GB, Tan C, Takada S. 2017. PLOS Comput. Biol. 13:e1005880
    [Google Scholar]
  82. 82.
    Rudnizky S, Khamis H, Malik O, Melamed P, Kaplan A. 2019. PNAS 116:12161–66
    [Google Scholar]
  83. 83.
    Winger J, Nodelman IM, Levendosky RF, Bowman GD 2018. eLife 7:e34100
    [Google Scholar]
  84. 84.
    Li M, Xia X, Tian Y, Jia Q, Liu X et al. 2019. Nature 567:409–13
    [Google Scholar]
  85. 85.
    Sabantsev A, Levendosky RF, Zhuang X, Bowman GD, Deindl S. 2019. Nat. Commun. 10:1720
    [Google Scholar]
  86. 86.
    Brandani GB, Takada S. 2018. PLOS Comput. Biol. 14:e1006512
    [Google Scholar]
  87. 87.
    Segal E, Widom J. 2009. Trend Genet. 25:335–43
    [Google Scholar]
  88. 88.
    Nodelman IM, Das S, Faustino AM, Fried SD, Bowman GD, Armache JP. 2022. Nat. Struct. Mol. Biol. 29:121–29
    [Google Scholar]
  89. 89.
    Narlikar GJ. 2010. Curr. Opin. Chem. Biol. 14:660–65
    [Google Scholar]
  90. 90.
    Schiessel H, Blossey R. 2020. Phys. Rev. E 101:040401(R)
    [Google Scholar]
  91. 91.
    Eltsov M, MacLellan KM, Maeshima K, Frangakis AS, Dubochet J. 2008. PNAS 105:19732–37
    [Google Scholar]
  92. 92.
    Joti Y, Hikima T, Nishino Y, Kamada F, Hihara S et al. 2012. Nucleus 3:404–10
    [Google Scholar]
  93. 93.
    Ricci MA, Manzo C, García-Parajo MF, Lakadamyali M, Cosma MP. 2015. Cell 160:1145–58
    [Google Scholar]
  94. 94.
    Portillo-Ledesma S, Tsao LH, Wagley M, Lakadamyali M, Cosma MP, Schlick T. 2021. J. Mol. Biol. 433:166701
    [Google Scholar]
  95. 95.
    Sazer S, Schiessel H. 2018. Traffic 19:87–104
    [Google Scholar]
  96. 96.
    de Gennes PG. 1979. Scaling Concepts in Polymer Physics Ithaka, NY: Cornell Univ. Press
    [Google Scholar]
  97. 97.
    van den Engh G, Sachs R, Trask BJ. 1992. Science 257:1410–12
    [Google Scholar]
  98. 98.
    Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K et al. 2005. PLOS Biol. 3:e157
    [Google Scholar]
  99. 99.
    Emanuel M, Radja NH, Henriksson A, Schiessel H. 2009. Phys. Biol. 6:025008
    [Google Scholar]
  100. 100.
    Mateos-Langerak J, Bohn M, de Leeuw W, Giromus O, Manders EMM et al. 2009. PNAS 106:3812–17
    [Google Scholar]
  101. 101.
    Maeshima K, Rogge R, Tamura S, Joti Y, Hikima T et al. 2016. EMBO J. 35:1115–32
    [Google Scholar]
  102. 102.
    Gibson BA, Doolittle LK, Schneider MWG, Jensen LE, Gamarra N et al. 2019. Cell 179:470–84
    [Google Scholar]
  103. 103.
    Strickfaden H, Tolsma TO, Sharma A, Underhill DA, Hansen JC, Hendzel MJ. 2020. Cell 183:1772–84
    [Google Scholar]
  104. 104.
    Bajpai G, Pavlov DA, Lorber D, Volk T, Safran S 2021. eLife 10:e63976
    [Google Scholar]
  105. 105.
    Amiad-Pavlov D, Lorber D, Bajpai G, Reuveny A, Roncato F et al. 2021. Sci. Adv. 7:eabf6251
    [Google Scholar]
  106. 106.
    Farr SE, Woods EJ, Joseph JA, Garaizar A, Collepardo-Guevara R. 2021. Nat. Commun. 12:2883
    [Google Scholar]
  107. 107.
    Lua R, Borovinskiy AL, Grosberg AY. 2004. Polymer 45:717–31
    [Google Scholar]
  108. 108.
    Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. 2009. Science 326:289–93
    [Google Scholar]
  109. 109.
    Grosberg A, Rabin R, Havlin S, Neer A. 1993. Europhys. Lett. 23:373–78
    [Google Scholar]
  110. 110.
    Smrek J, Grosberg AY. 2013. Physica A 392:6375–88
    [Google Scholar]
  111. 111.
    Schram RD, Barkema GT, Schiessel H. 2013. J. Chem. Phys. 138:224901
    [Google Scholar]
  112. 112.
    Sikorav JL, Jannink G. 1994. Biophys. J. 66:827–37
    [Google Scholar]
  113. 113.
    Rosa A, Everaers R. 2008. PLOS Comput. Biol. 4:e1000153
    [Google Scholar]
  114. 114.
    Schiessel H. 2022. Biophysics for Beginners: A Journey Through the Cell Nucleus Singapore: Jenny Stanford Publ. , 2nd ed..
    [Google Scholar]
  115. 115.
    Halverson JD, Lee WB, Grest GS, Grosberg AY, Kremer K. 2011. J. Chem. Phys. 134:204904
    [Google Scholar]
  116. 116.
    Rosa A, Everaers R. 2014. Phys. Rev. Lett. 112:118302
    [Google Scholar]
  117. 117.
    Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID et al. 2014. Cell 159:1665–80
    [Google Scholar]
  118. 118.
    Golfier S, Quail T, Kimura H, Brugués 2020. eLife 9:e53885
    [Google Scholar]
  119. 119.
    Fudenberg G, Imakaev M, Lu C, Goloborodko A, Mirny LA. 2016. Cell Rep. 15:2038–49
    [Google Scholar]
  120. 120.
    Banigan EJ, van den Berg AA, Brandão HB, Marko JF, Mirny LA 2020. eLife 9:e53558
    [Google Scholar]
  121. 121.
    Banigan EJ, Mirny LA 2020. eLife 9:e63528
    [Google Scholar]
  122. 122.
    Sanborn AL, Rao SSP, Huang SC, Durand NC, Huntley MH et al. 2015. PNAS 112:E6456–65
    [Google Scholar]
  123. 123.
    Grosberg AY, Khalatur PG, Khokhlov AR. 1982. Makromol. Chem. Rapid Commun. 3:709–13
    [Google Scholar]
  124. 124.
    Terakawa T, Bisht S, Eeftens JM, Dekker C, Haering CH, Greene EC. 2017. Science 358:672–76
    [Google Scholar]
  125. 125.
    Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A et al. 2018. Science 360:102–5
    [Google Scholar]
  126. 126.
    Gibcus JH, Samejima K, Goloborodko A, Samejima I, Naumova N et al. 2018. Science 359:eaao6135
    [Google Scholar]
  127. 127.
    Goloborodko A, Imakaev MV, Marko JF, Mirny L 2016. eLife 5:e14864
    [Google Scholar]
  128. 128.
    Shintomi K, Inoue F, Watanabe H, Ohsumi K, Ohsugi M, Hirano T. 2017. Science 356:1284–87
    [Google Scholar]
  129. 129.
    Shintomi K, Hirano T. 2021. Nat. Commun. 12:2917
    [Google Scholar]
  130. 130.
    Yamamoto T, Schiessel H. 2022. Biophys. J. 121:142742–50
    [Google Scholar]
  131. 131.
    Cortini R, Barbi M, Caré BR, Lavelle C, Lesne A et al. 2016. Rev. Mod. Phys. 88:025002
    [Google Scholar]
  132. 132.
    Yu C, Gan H, Serra-Cardona A, Zhang L, Gan S et al. 2018. Science 361:1386–89
    [Google Scholar]
  133. 133.
    Barkess G, West AG 2012. Epigenomics 4:67–80
    [Google Scholar]
  134. 134.
    Gazner M, Felsenfeld G. 2006. Nat. Rev. 7:703–13
    [Google Scholar]
  135. 135.
    Larson AG, Elnatan D, Keenen MM, Trnka MJ, Johnston JB et al. 2017. Nature 547:236–40
    [Google Scholar]
  136. 136.
    Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH. 2017. Nature 547:241–45
    [Google Scholar]
  137. 137.
    Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO et al. 2001. Nature 410:120–24
    [Google Scholar]
  138. 138.
    Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. 2001. Nature 410:116–20
    [Google Scholar]
  139. 139.
    Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SIS. 2001. Science 292:110–13
    [Google Scholar]
  140. 140.
    Banani SF, Lee HO, Hyman AA, Rosen MK. 2017. Nat. Rev. Mol. Cell Biol. 18:285–98
    [Google Scholar]
  141. 141.
    Sommer J-U, Daoud M. 1996. Phys. Rev. E 53:905–20
    [Google Scholar]
  142. 142.
    Aagaard L, Laible G, Selenko P, Schmid M, Dorn R et al. 1999. EMBO J. 18:1923–38
    [Google Scholar]
  143. 143.
    Raurell-Vila H, Bosch-Presegue L, Gonzalez J, Kane-Goldsmith N, Casal C et al. 2017. Epigenetics 12:166–75
    [Google Scholar]
  144. 144.
    Sommer J-U, Merlitz H, Schiessel H. 2022. Macromolecules 55:114841–51
    [Google Scholar]
  145. 145.
    Sandholtz SH, MacPherson Q, Spakowitz AJ. 2020. PNAS 117:20423–29
    [Google Scholar]
  146. 146.
    Eeftens JM, Kapoor M, Michieletto D, Brangwynne CP. 2021. Nat. Commun. 12:5888
    [Google Scholar]
  147. 147.
    Kireeva ML, Walter W, Tchernajenko V, Bondarenko V, Kashlev M, Studitsky VM. 2002. Mol. Cell 9:541–52
    [Google Scholar]
  148. 148.
    Zidovska A, Weitz DA, Mitchison TJ. 2013. PNAS 110:15555–60
    [Google Scholar]
  149. 149.
    Shaban HA, Barth R, Bystricky K. 2018. Nucl. Acids Res. 46:e77
    [Google Scholar]
  150. 150.
    Eshghi I, Eaton JA, Zidovska A. 2021. Phys. Rev. Lett. 126:228101
    [Google Scholar]
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