1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Condensed Matter Physics
  4. Volume 10, 2019
  5. Article

Annual Review of Condensed Matter Physics

Volume 10, 2019

Unveiling the Active Nature of Living-Membrane Fluctuations and Mechanics

Abstract

Soft-condensed matter physics has provided, in the past decades, many of the relevant concepts and methods allowing successful description of living cells and biological tissues. This recent quantitative physical description of biological systems has profoundly advanced our understanding of life, which is shifting from a descriptive to a predictive level. Like other active materials investigated in condensed matter physics, biological materials still pose great challenges to modern physics as they form a specific class of nonequilibrium systems. Actively driven membranes have been studied for more than two decades, taking advantage of rapid progress in membrane physics and in the experimental development of reconstituted active membranes. The physical description of activity within living biological membranes remains, however, a key challenge that animates a dynamic research community, bringing together physicists and biologists. Here, we first review the past two decades of experimental and theoretical advances that enabled the characterization of mechanical properties and nonequilibrium fluctuations in active membranes. We distinguish active processes originating from membrane proteins or from external interactions, such as cytoskeletal forces. Then, we focus on the emblematic case of red blood cell flickering, the active origin of which has been debated for decades until recently. We finally close this review by discussing future challenges in this ever more interdisciplinary field.

Keyword(s): active materials, active membranes, biological membranes, fluctuation-dissipation theorem, membrane fluctuations, nonequilibrium physics

[Erratum, Closure]

An erratum has been published for this article:
Erratum: Unveiling the Active Nature of Living-Membrane Fluctuations and Mechanics
Loading

Article metrics loading...

/content/journals/10.1146/annurev-conmatphys-031218-013757
2019-03-10
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/conmatphys/10/1/annurev-conmatphys-031218-013757.html?itemId=/content/journals/10.1146/annurev-conmatphys-031218-013757&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Ramaswamy S 2010. Annu. Rev. Condens. Matter Phys. 1:323–45
  2. 2.  Menon GI 2010. Rheology of Complex Fluids A Deshpande, J Murali Krishnan, PB Kumar193–218 New York: Springer
  3. 3.  Saintillan D 2018. Annu. Rev. Fluid Mech. 50:563–92
  4. 4.  Gross P, Kumar KV, Grill SW 2017. Annu. Rev. Biophys. 46:337–56
  5. 5.  Ramaswamy S 2017. J. Stat. Mech.: Theory Exp. 2017:054002
  6. 6.  Marchetti MC, Joanny JF, Ramaswamy S, Liverpool TB, Prost J et al. 2013. Rev. Mod. Phys. 85:1143–89
  7. 7.  Ahmed W, Betz T 2015. Biochim. Biophys. Acta Mol. Cell Res. 1853:3083–94
  8. 8.  Gennes PGd, Prost J 1995. The Physics of Liquid Crystals Oxford, UK: Clarendon
  9. 9. Browicz 1890. Zbl. Med. Wiss 28:625
  10. 10.  Brown R 1828. Philos. Mag. 4:161–73
  11. 11.  Blowers R, Clarkson E, Maizels M 1951. J. Physiol. 113:228–39
  12. 12.  Parpart A, Hoffman J 1956. J. Cell Comp. Physiol. 47:295–303
  13. 13.  Brochard F, Lennon J 1975. J. Phys. 36:1035–47
  14. 14.  Tuvia S, Almagor A, Bitler A, Levin S, Korenstein R, Yedgar S 1997. PNAS 94:5045–49
  15. 15.  Evans J, Gratzer W, Mohandas N, Parker K, Sleep J 2008. Biophys. J. 94:4134–44
  16. 16.  Evans AA, Bhaduri B, Popescu G, Levine AJ 2017. PNAS 114:2865–70
  17. 17.  Park Y, Best CA, Badizadegan K, Dasari RR, Feld MS et al. 2010. PNAS 107:6731–36
  18. 18.  Betz T, Lenz M, Joanny JF, Sykes C 2009. PNAS 106:15320–25
  19. 19.  Szekely D, Yau TW, Kuchel PW 2009. Eur. Biophys. J. 38:923–39
  20. 20.  Puckeridge M, Chapman BE, Conigrave AD, Kuchel PW 2014. Eur. Biophys. J. 43:169–77
  21. 21.  Turlier H, Fedosov DA, Audoly B, Auth T, Gov NS et al. 2016. Nat. Phys. 12:513–19
  22. 22.  Prost J, Bruinsma R 1996. Europhys. Lett. 33:321–26
  23. 23.  Prost J, Manneville JB, Bruinsma R 1998. Eur. Phys. J. B 1:465–80
  24. 24.  Ramaswamy S, Toner J, Prost J 2000. Phys. Rev. Lett. 84:3494–97
  25. 25.  Manneville JB, Bassereau P, Ramaswamy S, Prost J 2001. Phys. Rev. E 64:021908
  26. 26.  Granek R, Pierrat S 1999. Phys. Rev. Lett. 83:872–75
  27. 27.  Lenz P, Joanny J, Jülicher F, Prost J 2003. Phys. Rev. Lett. 91:108104
  28. 28.  Gov N 2004. Phys. Rev. Lett. 93:268104
  29. 29.  Lacoste D, Lau AWC 2005. Europhys. Lett. 70:418–24
  30. 30.  Lin LCL, Gov N, Brown FLH 2006. J. Chem. Phys. 124:074903
  31. 31.  Gov N, Safran S 2005. Biophys. J. 88:1859–74
  32. 32.  Auth T, Safran SA, Gov NS 2007. New J. Phys. 9:430–30
  33. 33.  Manneville JB, Bassereau P, Levy D, Prost J 1999. Phys. Rev. Lett. 82:4356–59
  34. 34.  Seifert U 1997. Adv. Phys. 46:13–137
  35. 35.  Nelson D, Piran T, Weinberg S 2004. Statistical Mechanics of Membranes and Surfaces Singapore: World Sci.
  36. 36.  Canham PB 1970. J. Theor. Biol. 26:61–81
  37. 37.  Helfrich W 1973. Z. Naturforschung C 28:693–703
  38. 38.  Seifert U 1995. Z. Phys. B Condens. Matter 97:299–309
  39. 39.  Girard P, Prost J, Bassereau P 2005. Phys. Rev. Lett. 94:088102
  40. 40.  Deuling H, Helfrich W 1976. J. Phys. 37:1335–45
  41. 41.  Loubet B, Seifert U, Lomholt MA 2012. Phys. Rev. E 85:031913
  42. 42.  Fournier JB, Lacoste D, Raphael E 2004. Phys. Rev. Lett. 92:018102
  43. 43.  Helfrich W, Servuss RM 1984. Il Nuovo Cim. D 3:137–51
  44. 44.  Schneider M, Jenkins J, Webb W 1984. Biophys. J. 45:891–99
  45. 45.  Betz T, Sykes C 2012. Soft Matter 8:5317–26
  46. 46.  Evans E, Needham D 1987. J. Phys. Chem. 91:4219–28
  47. 47.  Evans E, Rawicz W 1990. Phys. Rev. Lett. 64:2094–97
  48. 48.  Evans E, Rawicz W 1997. Phys. Rev. Lett. 79:2379–82
  49. 49.  Rawicz W, Olbrich K, McIntosh T, Needham D, Evans E 2000. Biophys. J. 79:328–39
  50. 50.  Lanyi JK 2004. Annu. Rev. Physiol. 66:665–88
  51. 51.  Ramaswamy S, Toner J, Prost J 1999. Pramana 53:237–42
  52. 52.  Andelman D, Kawakatsu T, Kawasaki K 1992. Europhys. Lett. 19:57–62
  53. 53.  Lomholt MA 2006. Phys. Rev. E 73:061914
  54. 54.  Chen HY 2004. Phys. Rev. Lett. 92:168101
  55. 55.  Monzel C, Sengupta K 2016. J. Phys. D: Appl. Phys. 49:243002
  56. 56.  Engelhardt H, Duwe H, Sackmann E 1985. J. Phys. Lett. 46:395–400
  57. 57.  Duwe HP, Zeman K, Sackmann E 1989. Trends in Colloid and Interface Science III H-G Kilian, G Lagaly6–10 Darmstadt, Germ.: Steinkopff Verlag
  58. 58.  Milner ST, Safran SA 1987. Phys. Rev. A 36:4371–79
  59. 59.  Faris MDEA, Lacoste D, Pecreaux J, Joanny JF, Prost J, Bassereau P 2009. Phys. Rev. Lett. 102:038102
  60. 60.  Bouvrais H, Cornelius F, Ipsen JH, Mouritsen OG 2012. PNAS 109:18442–46
  61. 61.  Loubet B, Lomholt MA, Khandelia H 2013. J. Chem. Phys. 139:164902
  62. 62.  Lemiere J, Guevorkian K, Campillo C, Sykes C, Betz T 2013. Soft Matter 9:3181
  63. 63.  Bezanilla M, Gladfelter AS, Kovar DR, Lee WL 2015. J. Cell Biol. 209:329–37
  64. 64.  Lux SE 2015. Blood 127:187–99
  65. 65.  Salbreux G, Charras G, Paluch E 2012. Trends Cell Biol. 22:536–45
  66. 66.  Sackmann E, Smith AS 2014. Soft Matter 10:1644
  67. 67.  Manno S, Takakuwa Y, Mohandas N 2004. J. Biol. Chem. 280:7581–87
  68. 68.  Ben-Isaac E, Park Y, Popescu G, Brown FLH, Gov NS, Shokef Y 2011. Phys. Rev. Lett. 106:238103
  69. 69.  Zhang R, Brown FLH 2008. J. Chem. Phys. 129:065101
  70. 70.  Dubus C, Fournier JB 2006. Europhys. Lett. 75:181–87
  71. 71.  Okamoto R, Komura S, Fournier JB 2017. Phys. Rev. E 96:012416
  72. 72.  Biswas A, Alex A, Sinha B 2017. Biophys. J. 113:1768–81
  73. 73.  Hui KL, Wang C, Grooman B, Wayt J, Upadhyaya A 2012. Biophys. J. 102:1524–33
  74. 74.  Kabaso D, Shlomovitz R, Schloen K, Stradal T, Gov NS 2011. PLOS Comput. Biol. 7:e1001127
  75. 75.  Gov NS, Gopinathan A 2006. Biophys. J. 90:454–69
  76. 76.  Shlomovitz R, Gov NS 2008. Phys. Rev. E 78:041911
  77. 77.  Srivastava P, Shlomovitz R, Gov NS, Rao M 2013. Phys. Rev. Lett. 110:168104
  78. 78.  Seifert U 1994. Phys. Rev. E 49:3124–27
  79. 79.  Fenz SF, Bihr T, Schmidt D, Merkel R, Seifert U et al. 2017. Nat. Phys. 13:906–13
  80. 80.  Rozycki B, Lipowsky R, Weikl TR 2006. Phys. Rev. Lett. 96:048101
  81. 81.  Charras GT, Coughlin M, Mitchison TJ, Mahadevan L 2008. Biophys. J. 94:1836–53
  82. 82.  Peukes J, Betz T 2014. Biophys. J. 107:1810–20
  83. 83.  Goudarzi M, Tarbashevich K, Mildner K, Begemann I, Garcia J et al. 2017. Dev. Cell 43:577–87
  84. 84.  Montigny C, Lyons J, Champeil P, Nissen P, Lenoir G 2016. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1861:767–83
  85. 85.  Hankins H, Baldridge R, Xu P, Graham T 2015. Traffic 16:35–47
  86. 86.  Papadopulos A, Vehring S, Lopez-Montero I, Kutschenko L, Stockl M et al. 2007. J. Biol. Chem. 282:15559–68
  87. 87.  Ramachandran S, Kumar PBS, Laradji M 2008. J. Chem. Phys. 129:125104
  88. 88.  Rao M, Sarasij RC 2001. Phys. Rev. Lett. 87:128101
  89. 89.  Ramaswamy S, Rao M 2001. C. R. Acad. Sci. Ser. IV Phys. Astrophys. 2:817–39
  90. 90.  Sens P 2004. Phys. Rev. Lett. 93:108103
  91. 91.  Sinha B, Köster D, Ruez R, Gonnord P, Bastiani M et al. 2011. Cell 144:402–13
  92. 92.  Solon J, Pecreaux J, Girard P, Faure MC, Prost J, Bassereau P 2006. Phys. Rev. Lett. 97:098103
  93. 93.  Junge W, Nelson N 2015. Annu. Rev. Biochem. 84:631–57
  94. 94.  Almendro-Vedia V, Natale P, Mell M, Bonneau S, Monroy F et al. 2017. PNAS 114:11291–96
  95. 95.  Paoluzzi M, Leonardo RD, Marchetti MC, Angelani L 2016. Sci. Rep. 6:34146
  96. 96.  Bar-Ziv R, Moses E, Nelson P 1998. Biophys. J. 75:294–320
  97. 97.  Brown A, Kotar J, Cicuta P 2011. Phys. Rev. E Stat. Nonlinear Soft Matter Phys. 84:021930
  98. 98.  Ziebert F, Bazant MZ, Lacoste D 2010. Phys. Rev. E 81:031912
  99. 99.  Lacoste D, Lagomarsino MC, Joanny JF 2007. Europhys. Lett. 77:18006
  100. 100.  Ambjornsson T, Lomholt MA, Hansen PL 2007. Phys. Rev. E 75:051916
  101. 101.  Callen HB, Welton TA 1951. Phys. Rev. 83:34–40
  102. 102.  Boss D, Hoffmann A, Rappaz B, Depeursinge C, Magistretti PJ et al. 2012. PLOS ONE 7:e40667
  103. 103.  Rodriguez-Garcia R, Lopez-Montero I, Mell M, Egea G, Gov N, Monroy F 2016. Biophys. J. 111:1101
  104. 104.  Monzel C, Schmidt D, Kleusch C, Kirchenbuchler D, Seifert U et al. 2015. Nat. Commun. 6:9162
  105. 105.  Park Y, Best CA, Auth T, Gov NS, Safran SA et al. 2010. PNAS 107:1289–94
  106. 106.  Gögler M, Betz T, Käs JA 2007. Opt. Lett. 32:1893
  107. 107.  Mizuno D, Tardin C, Schmidt CF, MacKintosh FC 2007. Science 315:370–73
  108. 108.  Martin P, Hudspeth AJ, Jülicher F 2001. PNAS 98:14380–85
  109. 109.  Yoon YZ, Kotar J, Brown AT, Cicuta P 2011. Soft Matter 7:2042–51
  110. 110.  Manno S, Takakuwa Y, Nagao K, Mohandas N 1995. J. Biol. Chem. 270:5659–65
  111. 111.  Seifert U, Langer SA 1994. Biophys. Chem. 49:13–22
  112. 112.  Gov NS 2007. Phys. Rev. E 75:011921
  113. 113.  Subrahmanyam G, Bertics PJ, Anderson RA 1991. PNAS 88:5222–26
  114. 114.  Sheetz MP 1977. J. Cell Biol. 73:638–46
  115. 115.  Rangamani P, Mandadap K, Oster G 2014. Biophys. J. 107:751–62
  116. 116.  Gauthier NC, Fardin MA, Roca-Cusachs P, Sheetz MP 2011. PNAS 108:14467–72
  117. 117.  Charras GT, Williams BA, Sims SM, Horton MA 2004. Biophys. J. 87:2870–84
  118. 118.  Lin LCL, Brown FL 2004. Biophys. J. 86:764–80
  119. 119.  Mostowy S, Cossart P 2012. Nat. Rev. Mol. Cell Biol. 13:183–94
  120. 120.  Loose M, Mitchison TJ 2013. Nat. Cell Biol. 16:38–46
  121. 121.  Rao M, Mayor S 2014. Curr. Opin. Cell Biol. 29:126–32
  122. 122.  Small J, Stradal T, Vignal E, Rottner K 2002. Trends Cell Biol. 12:112–20
  123. 123.  Mattila PK, Lappalainen P 2008. Nat. Rev. Mol. Cell Biol. 9:446–54
  124. 124.  Dmitrieff S, Nedelec F 2015. PLOS Comput. Biol. 11:e1004538
  125. 125.  Köster DV, Husain K, Iljazi E, Bhat A, Bieling P et al. 2016. PNAS 113:E1645–54
  126. 126.  Prost J, Jülicher F, Joanny JF 2015. Nat. Phys. 11:111–17
  127. 127.  Turlier H, Audoly B, Prost J, Joanny JF 2014. Biophys. J. 106:114–23
  128. 128.  Salbreux G, Jülicher F 2017. Phys. Rev. E 96:032404
  129. 129.  Shlomovitz R, Gov N 2009. Phys. Biol. 6:046017
  130. 130.  Maitra A, Srivastava P, Rao M, Ramaswamy S 2014. Phys. Rev. Lett. 112:258101
  131. 131.  Caorsi V, Lemiere J, Campillo C, Bussonnier M, Manzi J et al. 2016. Soft Matter 12:6223–31
  132. 132.  Guevorkian K, Manzi J, Pontani LL, Brochard-Wyart F, Sykes C 2015. Biophys. J. 109:2471–79
  133. 133.  Carvalho K, Tsai FC, Lees E, Voituriez R, Koenderink GH, Sykes C 2013. PNAS 110:16456–61
  134. 134.  Carvalho K, Lemiere J, Faqir F, Manzi J, Blanchoin L et al. 2013. Philos. Trans. R. Soc. B: Biol. Sci. 368:20130005
  135. 135.  Enas AS, Kinneret K 2013. Front. Immunol. 4:01001
  136. 136.  Linsmeier I, Banerjee S, Oakes PW, Jung W, Kim T, Murrell MP 2016. Nat. Commun. 7:12615
  137. 137.  Loiseau E, Schneider JAM, Keber FC, Pelzl C, Massiera G et al. 2016. Sci. Adv. 2:e1500465
  138. 138.  Lin LCL, Brown FLH 2004. Phys. Rev. Lett. 93:256001
  139. 139.  Brannigan G, Lin LCL, Brown FLH 2005. Eur. Biophys. J. 35:104–24
  140. 140.  Lin LCL, Brown FLH 2006. J. Chem. Theory Comput. 2:472–83
  141. 141.  Peskin CS 2002. Acta Numerica 2002 A Iserles479–518 Cambridge, UK: Cambridge Univ. Press
  142. 142.  Eggleton CD, Popel AS 1998. Phys. Fluids 10:1834–45
  143. 143.  Pozrikidis C 2005. Ann. Biomed. Eng. 33:165–78
  144. 144.  Hoogerbrugge PJ, Koelman JMVA 1992. Europhys. Lett. 19:155–60
  145. 145.  Peng Z, Asaro RJ, Zhu Q 2011. J. Fluid Mech. 686:299–337
  146. 146.  Atzberger PJ, Kramer PR, Peskin CS 2007. J. Comput. Phys. 224:1255–92
  147. 147.  Fedosov DA, Caswell B, Karniadakis GE 2010. Biophys. J. 98:2215–25
  148. 148.  Peng Z, Li X, Pivkin IV, Dao M, Karniadakis GE, Suresh S 2013. PNAS 110:13356–61
/content/journals/10.1146/annurev-conmatphys-031218-013757
Loading
Unveiling the Active Nature of Living-Membrane Fluctuations and Mechanics
Annual Review of Condensed Matter Physics 10, 213 (2019); https://doi.org/10.1146/annurev-conmatphys-031218-013757
/content/journals/10.1146/annurev-conmatphys-031218-013757
/content/journals/10.1146/annurev-conmatphys-031218-013757
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

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