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.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-conmatphys-040821-115729
2023-03-10
2024-05-13
Loading full text...

Full text loading...

/deliver/fulltext/conmatphys/14/1/annurev-conmatphys-040821-115729.html?itemId=/content/journals/10.1146/annurev-conmatphys-040821-115729&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Schiessel H. 2003. J. Phys. Condens. Matter 15:R699–774
  2. 2.
    Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Nature 389:251–60
  3. 3.
    Ngo TTM, Zhang Q, Zhou R, Yodh JG, Ha T. 2015. Cell 160:1135–44
  4. 4.
    Eslami-Mossallam B, Schram RD, Tompitak M, van Noort J, Schiessel H. 2016. PLOS ONE 11:e0156905
  5. 5.
    Hall MA, Shundrovsky A, Bai L, Fulbright RM, Lis JT, Wang MD. 2009. Nat. Struct. Mol. Biol. 16:124–29
  6. 6.
    Bustamante C, Marko JF, Siggia ED, Smith S. 1994. Science 265:1599–600
  7. 7.
    Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D et al. 2009. Nature 458:362–66
  8. 8.
    Lowary PT, Widom J. 1997. PNAS 94:1183–88
  9. 9.
    Satchwell SC, Drew HR, Travers AA. 1986. J. Mol. Biol. 191:659–75
  10. 10.
    Segal E, Fondufe-Mittendorf Y, Chen L, Thåström A, Field Y et al. 2006. Nature 442:772–78
  11. 11.
    Jin H, Rube HT, Song JS 2016. Nucl. Acids Res. 44:2047–57
  12. 12.
    Tillo D, Hughes TR 2009. BMC Bioinform. 10:442
  13. 13.
    Locke G, Tolkunov D, Moqtaderi Z, Struhl K, Morozov AV. 2010. PNAS 107:20998–1003
  14. 14.
    Struhl K, Segal E. 2013. Nat. Struct. Mol. Biol. 20:267–73
  15. 15.
    Drillon G, Audit B, Argoul F, Arneodo A 2016. BMC Genom. 17:526
  16. 16.
    Tompitak M, Vaillant C, Schiessel H. 2017. Biophys. J. 112:505–11
  17. 17.
    Olson WK, Gorin AA, Lu X-J, Hock LM, Zhurkin VB. 1998. PNAS 95:11163–68
  18. 18.
    Hinckley DM, Freeman GS, Whitmer JK, de Pablo JJ. 2013. J. Phys. Chem. 139:144903
  19. 19.
    Lankaš F, Šponer J, Langowski J, Cheatham TE III 2003. Biophys. J. 85:2872–83
  20. 20.
    Morozov AV, Fortney K, Gaykalova DA, Studitsky VM, Widom J, Siggia ED. 2009. Nucl. Acids Res. 37:4707–22
  21. 21.
    Freeman GS, Lequieu JP, Hinckley DM, Whitmer JK, de Pablo JJ. 2014. Phys. Rev. Lett. 113:168101
  22. 22.
    Zuiddam M, Everaers R, Schiessel H. 2017. Phys. Rev. E 96:052412
  23. 23.
    Neipel J, Brandani G, Schiessel H. 2020. Phys. Rev. E 101:022405
  24. 24.
    Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. 2013. Nat. Methods 10:1213–18
  25. 25.
    Brogaard K, Xi L, Wang JP, Widom J. 2012. Nature 486:496–501
  26. 26.
    Kelly TK, Liu Y, Lay FD, Liang G, Berman BP, Jones PA. 2012. Genome Res. 22:2497–506
  27. 27.
    Kornberg RD, Stryer L. 1988. Nucl. Acids Res. 16:6677–90
  28. 28.
    Chevereau G, Palmeira L, Thermes C, Arneodo A, Vaillant C. 2009. Phys. Rev. Lett. 103:188103
  29. 29.
    Tillo D, Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ et al. 2010. PLOS ONE 5:e9129
  30. 30.
    Vavouri T, Lehner B. 2011. PLOS Genet. 7:e1002036
  31. 31.
    Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. 2009. Nature 460:473–78
  32. 32.
    Eslami-Mossallam B, Schiessel H, van Noort J. 2016. Adv. Colloid Interface Sci. 232:101–13
  33. 33.
    Fierz B, Poirier MG. 2019. Annu. Rev. Biophys. 48:321–45
  34. 34.
    Polach KJ, Widom J. 1995. J. Mol. Biol. 254:130–49
  35. 35.
    Anderson JD, Lowary PT, Widom J. 2001. J. Mol. Biol. 307:977–85
  36. 36.
    Li G, Widom J. 2004. Nat. Struct. Mol. Biol. 11:763–69
  37. 37.
    Li G, Levitus M, Bustamante C, Widom J. 2005. Nat. Struct. Mol. Biol. 12:46–53
  38. 38.
    Kelbauskas L, Chan N, Bash R, Yodh J, Woodbury N, Lohr D. 2007. Biochemistry 46:2239–48
  39. 39.
    Koopmans WJA, Brehm A, Logie C, Schmidt T, van Noort J. 2007. J. Fluoresc. 17:785–95
  40. 40.
    Moyle-Heyrman G, Tims HS, Widom J. 2011. J. Mol. Biol. 412:634–46
  41. 41.
    Tims HS, Gurunathan K, Levitus M, Widom J. 2011. J. Mol. Biol. 411:430–48
  42. 42.
    Gansen A, Felekyan S, Kühnemuth R, Lehmann K, Tóth K et al. 2018. Nat. Commun. 9:4628
  43. 43.
    Konrad SF, Vanderlinden W, Frederickx W, Brouns T, Menze BH et al. 2021. Nanoscale 13:5435–47
  44. 44.
    Konrad SF, Vanderlinden W, Lipfert J. 2022. Biophys. J. 121:841–51
  45. 45.
    Prinsen P, Schiessel H. 2010. Biochimie 92:1722–28
  46. 46.
    Anderson JD, Widom J. 2001. Mol. Cell. Biol. 21:3830–39
  47. 47.
    Kelbauskis L, Woodbury N, Lohr D. 2009. Biochem. Cell Biol. 87:323–35
  48. 48.
    Gansen A, Tóth, Schwarz N, Langowski J 2009. J. Phys. Chem. B 113:2604–13
  49. 49.
    Tóth K, Böhm V, Sellmann C, Danner M, Hanne J et al. 2013. Cytometry A 83:839–46
  50. 50.
    Lowary PT, Widom J. 1998. J. Mol. Biol. 276:19–42
  51. 51.
    Mauney AW, Tokuda JM, Gloss LM, Gonzalez O, Pollack M. 2018. Biophys. J. 115:773–81
  52. 52.
    van Deelen K, Schiessel H, de Bruin L. 2020. Biophys. J. 118:2297–308
  53. 53.
    Polach KJ, Widom J. 1996. J. Mol. Biol. 258:800–12
  54. 54.
    Culkin J, de Bruin L, Tompitak M, Phillips R, Schiessel H. 2017. Eur. Phys. J. E 40:106
  55. 55.
    Winogradoff D, Aksimentiev A. 2019. J. Mol. Biol. 431:323–35
  56. 56.
    Armeev GA, Kniazeva AS, Komarova GA, Kirpichnikov MP, Shaytan AK. 2021. Nat. Commun. 12:2387
  57. 57.
    Brower-Toland BD, Smith CL, Yeh RC, Lis JT, Peterson CL, Wang MD. 2002. PNAS 99:1960–65
  58. 58.
    Kulić IM, Schiessel H. 2004. Phys. Rev. Lett. 92:228101
  59. 59.
    Wocjan T, Klenin K, Langowski J. 2009. J. Phys. Chem. B 113:2639–46
  60. 60.
    Sudhanshu B, Mihardja S, Koslover EF, Mehraeen S, Bustamante C, Spakowitz AJ. 2011. PNAS 108:1885–90
  61. 61.
    Ettig R, Kepper N, Stehr R, Wedemann G, Rippe K. 2011. Biophys. J. 101:1999–2008
  62. 62.
    Mollazadeh-Beidokhti L, Mohammad-Rafiee F, Schiessel H. 2012. Biophys. J. 102:2235–40
  63. 63.
    Lanzani G, Schiessel H. 2012. Europhys. Lett. 100:48001
  64. 64.
    Mochrie SGJ, Mack AH, Schlingwein DJ, Collins R, Kamenetska M, Regan L 2013. Phys. Rev. E 87:012710
  65. 65.
    Mack AH, Schlingman DJ, Salinas RD, Regan L, Mochrie SGJ 2015. J. Phys. Condens. Matter 27:064106
  66. 66.
    Lequieu J, Córdoba A, Schwartz DC, de Pablo JJ. 2016. ACS Cent. Sci. 2:660–66
  67. 67.
    Khodabandeh F, Fatemi H, Mohammad-Rafiee F. 2020. Soft Matter 16:4806–13
  68. 68.
    Reddy G, Thirumalai D. 2021. Nucl. Acids Res. 49:4907–18
  69. 69.
    de Bruin L, Tompitak M, Eslami-Mossallam B, Schiessel H. 2016. J. Phys. Chem. B 120:5855–63
  70. 70.
    Tompitak M, de Bruin L, Eslami-Mossallam B, Schiessel H. 2017. Phys. Rev. E 95:052402
  71. 71.
    Durkin SG, Glover TW. 2007. Annu. Rev. Genet. 41:169–92
  72. 72.
    Chan KL, Palmai-Pallag T, Ying S, Hickson ID 2009. Nat. Cell Biol. 11:753–60
  73. 73.
    Biebricher A, Hirano S, Enzlin JH, Wiechens N, Streicher WW et al. 2013. Mol. Cell 51:691–701
  74. 74.
    Meersseman G, Pennings S, Bradbury EM. 1992. EMBO J. 11:2951–59
  75. 75.
    Kulić IM, Schiessel H. 2003. Phys. Rev. Lett. 91:148103
  76. 76.
    Mohammad-Rafiee F, Kulić IM, Schiessel H. 2004. J. Mol. Biol. 344:47–58
  77. 77.
    Brandani GB, Niina T, Tan C, Takada S. 2018. Nucl. Acids Res. 46:2788–801
  78. 78.
    Schiessel H, Widom J, Bruinsma RF, Gelbart WM. 2001. Phys. Rev. Lett. 86:4414–17
  79. 79.
    Kulić IM, Schiessel H. 2003. Biophys. J. 84:3197–211
  80. 80.
    Lequieu J, Schwartz DC, de Pablo JJ. 2017. PNAS 114:E9197–205
  81. 81.
    Niina T, Brandani GB, Tan C, Takada S. 2017. PLOS Comput. Biol. 13:e1005880
  82. 82.
    Rudnizky S, Khamis H, Malik O, Melamed P, Kaplan A. 2019. PNAS 116:12161–66
  83. 83.
    Winger J, Nodelman IM, Levendosky RF, Bowman GD 2018. eLife 7:e34100
  84. 84.
    Li M, Xia X, Tian Y, Jia Q, Liu X et al. 2019. Nature 567:409–13
  85. 85.
    Sabantsev A, Levendosky RF, Zhuang X, Bowman GD, Deindl S. 2019. Nat. Commun. 10:1720
  86. 86.
    Brandani GB, Takada S. 2018. PLOS Comput. Biol. 14:e1006512
  87. 87.
    Segal E, Widom J. 2009. Trend Genet. 25:335–43
  88. 88.
    Nodelman IM, Das S, Faustino AM, Fried SD, Bowman GD, Armache JP. 2022. Nat. Struct. Mol. Biol. 29:121–29
  89. 89.
    Narlikar GJ. 2010. Curr. Opin. Chem. Biol. 14:660–65
  90. 90.
    Schiessel H, Blossey R. 2020. Phys. Rev. E 101:040401(R)
  91. 91.
    Eltsov M, MacLellan KM, Maeshima K, Frangakis AS, Dubochet J. 2008. PNAS 105:19732–37
  92. 92.
    Joti Y, Hikima T, Nishino Y, Kamada F, Hihara S et al. 2012. Nucleus 3:404–10
  93. 93.
    Ricci MA, Manzo C, García-Parajo MF, Lakadamyali M, Cosma MP. 2015. Cell 160:1145–58
  94. 94.
    Portillo-Ledesma S, Tsao LH, Wagley M, Lakadamyali M, Cosma MP, Schlick T. 2021. J. Mol. Biol. 433:166701
  95. 95.
    Sazer S, Schiessel H. 2018. Traffic 19:87–104
  96. 96.
    de Gennes PG. 1979. Scaling Concepts in Polymer Physics Ithaka, NY: Cornell Univ. Press
  97. 97.
    van den Engh G, Sachs R, Trask BJ. 1992. Science 257:1410–12
  98. 98.
    Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K et al. 2005. PLOS Biol. 3:e157
  99. 99.
    Emanuel M, Radja NH, Henriksson A, Schiessel H. 2009. Phys. Biol. 6:025008
  100. 100.
    Mateos-Langerak J, Bohn M, de Leeuw W, Giromus O, Manders EMM et al. 2009. PNAS 106:3812–17
  101. 101.
    Maeshima K, Rogge R, Tamura S, Joti Y, Hikima T et al. 2016. EMBO J. 35:1115–32
  102. 102.
    Gibson BA, Doolittle LK, Schneider MWG, Jensen LE, Gamarra N et al. 2019. Cell 179:470–84
  103. 103.
    Strickfaden H, Tolsma TO, Sharma A, Underhill DA, Hansen JC, Hendzel MJ. 2020. Cell 183:1772–84
  104. 104.
    Bajpai G, Pavlov DA, Lorber D, Volk T, Safran S 2021. eLife 10:e63976
  105. 105.
    Amiad-Pavlov D, Lorber D, Bajpai G, Reuveny A, Roncato F et al. 2021. Sci. Adv. 7:eabf6251
  106. 106.
    Farr SE, Woods EJ, Joseph JA, Garaizar A, Collepardo-Guevara R. 2021. Nat. Commun. 12:2883
  107. 107.
    Lua R, Borovinskiy AL, Grosberg AY. 2004. Polymer 45:717–31
  108. 108.
    Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. 2009. Science 326:289–93
  109. 109.
    Grosberg A, Rabin R, Havlin S, Neer A. 1993. Europhys. Lett. 23:373–78
  110. 110.
    Smrek J, Grosberg AY. 2013. Physica A 392:6375–88
  111. 111.
    Schram RD, Barkema GT, Schiessel H. 2013. J. Chem. Phys. 138:224901
  112. 112.
    Sikorav JL, Jannink G. 1994. Biophys. J. 66:827–37
  113. 113.
    Rosa A, Everaers R. 2008. PLOS Comput. Biol. 4:e1000153
  114. 114.
    Schiessel H. 2022. Biophysics for Beginners: A Journey Through the Cell Nucleus Singapore: Jenny Stanford Publ. , 2nd ed..
  115. 115.
    Halverson JD, Lee WB, Grest GS, Grosberg AY, Kremer K. 2011. J. Chem. Phys. 134:204904
  116. 116.
    Rosa A, Everaers R. 2014. Phys. Rev. Lett. 112:118302
  117. 117.
    Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID et al. 2014. Cell 159:1665–80
  118. 118.
    Golfier S, Quail T, Kimura H, Brugués 2020. eLife 9:e53885
  119. 119.
    Fudenberg G, Imakaev M, Lu C, Goloborodko A, Mirny LA. 2016. Cell Rep. 15:2038–49
  120. 120.
    Banigan EJ, van den Berg AA, Brandão HB, Marko JF, Mirny LA 2020. eLife 9:e53558
  121. 121.
    Banigan EJ, Mirny LA 2020. eLife 9:e63528
  122. 122.
    Sanborn AL, Rao SSP, Huang SC, Durand NC, Huntley MH et al. 2015. PNAS 112:E6456–65
  123. 123.
    Grosberg AY, Khalatur PG, Khokhlov AR. 1982. Makromol. Chem. Rapid Commun. 3:709–13
  124. 124.
    Terakawa T, Bisht S, Eeftens JM, Dekker C, Haering CH, Greene EC. 2017. Science 358:672–76
  125. 125.
    Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A et al. 2018. Science 360:102–5
  126. 126.
    Gibcus JH, Samejima K, Goloborodko A, Samejima I, Naumova N et al. 2018. Science 359:eaao6135
  127. 127.
    Goloborodko A, Imakaev MV, Marko JF, Mirny L 2016. eLife 5:e14864
  128. 128.
    Shintomi K, Inoue F, Watanabe H, Ohsumi K, Ohsugi M, Hirano T. 2017. Science 356:1284–87
  129. 129.
    Shintomi K, Hirano T. 2021. Nat. Commun. 12:2917
  130. 130.
    Yamamoto T, Schiessel H. 2022. Biophys. J. 121:142742–50
  131. 131.
    Cortini R, Barbi M, Caré BR, Lavelle C, Lesne A et al. 2016. Rev. Mod. Phys. 88:025002
  132. 132.
    Yu C, Gan H, Serra-Cardona A, Zhang L, Gan S et al. 2018. Science 361:1386–89
  133. 133.
    Barkess G, West AG 2012. Epigenomics 4:67–80
  134. 134.
    Gazner M, Felsenfeld G. 2006. Nat. Rev. 7:703–13
  135. 135.
    Larson AG, Elnatan D, Keenen MM, Trnka MJ, Johnston JB et al. 2017. Nature 547:236–40
  136. 136.
    Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH. 2017. Nature 547:241–45
  137. 137.
    Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO et al. 2001. Nature 410:120–24
  138. 138.
    Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. 2001. Nature 410:116–20
  139. 139.
    Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SIS. 2001. Science 292:110–13
  140. 140.
    Banani SF, Lee HO, Hyman AA, Rosen MK. 2017. Nat. Rev. Mol. Cell Biol. 18:285–98
  141. 141.
    Sommer J-U, Daoud M. 1996. Phys. Rev. E 53:905–20
  142. 142.
    Aagaard L, Laible G, Selenko P, Schmid M, Dorn R et al. 1999. EMBO J. 18:1923–38
  143. 143.
    Raurell-Vila H, Bosch-Presegue L, Gonzalez J, Kane-Goldsmith N, Casal C et al. 2017. Epigenetics 12:166–75
  144. 144.
    Sommer J-U, Merlitz H, Schiessel H. 2022. Macromolecules 55:114841–51
  145. 145.
    Sandholtz SH, MacPherson Q, Spakowitz AJ. 2020. PNAS 117:20423–29
  146. 146.
    Eeftens JM, Kapoor M, Michieletto D, Brangwynne CP. 2021. Nat. Commun. 12:5888
  147. 147.
    Kireeva ML, Walter W, Tchernajenko V, Bondarenko V, Kashlev M, Studitsky VM. 2002. Mol. Cell 9:541–52
  148. 148.
    Zidovska A, Weitz DA, Mitchison TJ. 2013. PNAS 110:15555–60
  149. 149.
    Shaban HA, Barth R, Bystricky K. 2018. Nucl. Acids Res. 46:e77
  150. 150.
    Eshghi I, Eaton JA, Zidovska A. 2021. Phys. Rev. Lett. 126:228101
/content/journals/10.1146/annurev-conmatphys-040821-115729
Loading
/content/journals/10.1146/annurev-conmatphys-040821-115729
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error