1932

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.

[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
2024-06-22
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
    [Google Scholar]
  2. 2.  Menon GI 2010. Rheology of Complex Fluids A Deshpande, J Murali Krishnan, PB Kumar193218 New York: Springer
    [Google Scholar]
  3. 3.  Saintillan D 2018. Annu. Rev. Fluid Mech. 50:563–92
    [Google Scholar]
  4. 4.  Gross P, Kumar KV, Grill SW 2017. Annu. Rev. Biophys. 46:337–56
    [Google Scholar]
  5. 5.  Ramaswamy S 2017. J. Stat. Mech.: Theory Exp. 2017:054002
    [Google Scholar]
  6. 6.  Marchetti MC, Joanny JF, Ramaswamy S, Liverpool TB, Prost J et al. 2013. Rev. Mod. Phys. 85:1143–89
    [Google Scholar]
  7. 7.  Ahmed W, Betz T 2015. Biochim. Biophys. Acta Mol. Cell Res. 1853:3083–94
    [Google Scholar]
  8. 8.  Gennes PGd, Prost J 1995. The Physics of Liquid Crystals Oxford, UK: Clarendon
    [Google Scholar]
  9. 9. Browicz 1890. Zbl. Med. Wiss 28:625
    [Google Scholar]
  10. 10.  Brown R 1828. Philos. Mag. 4:161–73
    [Google Scholar]
  11. 11.  Blowers R, Clarkson E, Maizels M 1951. J. Physiol. 113:228–39
    [Google Scholar]
  12. 12.  Parpart A, Hoffman J 1956. J. Cell Comp. Physiol. 47:295–303
    [Google Scholar]
  13. 13.  Brochard F, Lennon J 1975. J. Phys. 36:1035–47
    [Google Scholar]
  14. 14.  Tuvia S, Almagor A, Bitler A, Levin S, Korenstein R, Yedgar S 1997. PNAS 94:5045–49
    [Google Scholar]
  15. 15.  Evans J, Gratzer W, Mohandas N, Parker K, Sleep J 2008. Biophys. J. 94:4134–44
    [Google Scholar]
  16. 16.  Evans AA, Bhaduri B, Popescu G, Levine AJ 2017. PNAS 114:2865–70
    [Google Scholar]
  17. 17.  Park Y, Best CA, Badizadegan K, Dasari RR, Feld MS et al. 2010. PNAS 107:6731–36
    [Google Scholar]
  18. 18.  Betz T, Lenz M, Joanny JF, Sykes C 2009. PNAS 106:15320–25
    [Google Scholar]
  19. 19.  Szekely D, Yau TW, Kuchel PW 2009. Eur. Biophys. J. 38:923–39
    [Google Scholar]
  20. 20.  Puckeridge M, Chapman BE, Conigrave AD, Kuchel PW 2014. Eur. Biophys. J. 43:169–77
    [Google Scholar]
  21. 21.  Turlier H, Fedosov DA, Audoly B, Auth T, Gov NS et al. 2016. Nat. Phys. 12:513–19
    [Google Scholar]
  22. 22.  Prost J, Bruinsma R 1996. Europhys. Lett. 33:321–26
    [Google Scholar]
  23. 23.  Prost J, Manneville JB, Bruinsma R 1998. Eur. Phys. J. B 1:465–80
    [Google Scholar]
  24. 24.  Ramaswamy S, Toner J, Prost J 2000. Phys. Rev. Lett. 84:3494–97
    [Google Scholar]
  25. 25.  Manneville JB, Bassereau P, Ramaswamy S, Prost J 2001. Phys. Rev. E 64:021908
    [Google Scholar]
  26. 26.  Granek R, Pierrat S 1999. Phys. Rev. Lett. 83:872–75
    [Google Scholar]
  27. 27.  Lenz P, Joanny J, Jülicher F, Prost J 2003. Phys. Rev. Lett. 91:108104
    [Google Scholar]
  28. 28.  Gov N 2004. Phys. Rev. Lett. 93:268104
    [Google Scholar]
  29. 29.  Lacoste D, Lau AWC 2005. Europhys. Lett. 70:418–24
    [Google Scholar]
  30. 30.  Lin LCL, Gov N, Brown FLH 2006. J. Chem. Phys. 124:074903
    [Google Scholar]
  31. 31.  Gov N, Safran S 2005. Biophys. J. 88:1859–74
    [Google Scholar]
  32. 32.  Auth T, Safran SA, Gov NS 2007. New J. Phys. 9:430–30
    [Google Scholar]
  33. 33.  Manneville JB, Bassereau P, Levy D, Prost J 1999. Phys. Rev. Lett. 82:4356–59
    [Google Scholar]
  34. 34.  Seifert U 1997. Adv. Phys. 46:13–137
    [Google Scholar]
  35. 35.  Nelson D, Piran T, Weinberg S 2004. Statistical Mechanics of Membranes and Surfaces Singapore: World Sci.
    [Google Scholar]
  36. 36.  Canham PB 1970. J. Theor. Biol. 26:61–81
    [Google Scholar]
  37. 37.  Helfrich W 1973. Z. Naturforschung C 28:693–703
    [Google Scholar]
  38. 38.  Seifert U 1995. Z. Phys. B Condens. Matter 97:299–309
    [Google Scholar]
  39. 39.  Girard P, Prost J, Bassereau P 2005. Phys. Rev. Lett. 94:088102
    [Google Scholar]
  40. 40.  Deuling H, Helfrich W 1976. J. Phys. 37:1335–45
    [Google Scholar]
  41. 41.  Loubet B, Seifert U, Lomholt MA 2012. Phys. Rev. E 85:031913
    [Google Scholar]
  42. 42.  Fournier JB, Lacoste D, Raphael E 2004. Phys. Rev. Lett. 92:018102
    [Google Scholar]
  43. 43.  Helfrich W, Servuss RM 1984. Il Nuovo Cim. D 3:137–51
    [Google Scholar]
  44. 44.  Schneider M, Jenkins J, Webb W 1984. Biophys. J. 45:891–99
    [Google Scholar]
  45. 45.  Betz T, Sykes C 2012. Soft Matter 8:5317–26
    [Google Scholar]
  46. 46.  Evans E, Needham D 1987. J. Phys. Chem. 91:4219–28
    [Google Scholar]
  47. 47.  Evans E, Rawicz W 1990. Phys. Rev. Lett. 64:2094–97
    [Google Scholar]
  48. 48.  Evans E, Rawicz W 1997. Phys. Rev. Lett. 79:2379–82
    [Google Scholar]
  49. 49.  Rawicz W, Olbrich K, McIntosh T, Needham D, Evans E 2000. Biophys. J. 79:328–39
    [Google Scholar]
  50. 50.  Lanyi JK 2004. Annu. Rev. Physiol. 66:665–88
    [Google Scholar]
  51. 51.  Ramaswamy S, Toner J, Prost J 1999. Pramana 53:237–42
    [Google Scholar]
  52. 52.  Andelman D, Kawakatsu T, Kawasaki K 1992. Europhys. Lett. 19:57–62
    [Google Scholar]
  53. 53.  Lomholt MA 2006. Phys. Rev. E 73:061914
    [Google Scholar]
  54. 54.  Chen HY 2004. Phys. Rev. Lett. 92:168101
    [Google Scholar]
  55. 55.  Monzel C, Sengupta K 2016. J. Phys. D: Appl. Phys. 49:243002
    [Google Scholar]
  56. 56.  Engelhardt H, Duwe H, Sackmann E 1985. J. Phys. Lett. 46:395–400
    [Google Scholar]
  57. 57.  Duwe HP, Zeman K, Sackmann E 1989. Trends in Colloid and Interface Science III H-G Kilian, G Lagaly610 Darmstadt, Germ.: Steinkopff Verlag
    [Google Scholar]
  58. 58.  Milner ST, Safran SA 1987. Phys. Rev. A 36:4371–79
    [Google Scholar]
  59. 59.  Faris MDEA, Lacoste D, Pecreaux J, Joanny JF, Prost J, Bassereau P 2009. Phys. Rev. Lett. 102:038102
    [Google Scholar]
  60. 60.  Bouvrais H, Cornelius F, Ipsen JH, Mouritsen OG 2012. PNAS 109:18442–46
    [Google Scholar]
  61. 61.  Loubet B, Lomholt MA, Khandelia H 2013. J. Chem. Phys. 139:164902
    [Google Scholar]
  62. 62.  Lemiere J, Guevorkian K, Campillo C, Sykes C, Betz T 2013. Soft Matter 9:3181
    [Google Scholar]
  63. 63.  Bezanilla M, Gladfelter AS, Kovar DR, Lee WL 2015. J. Cell Biol. 209:329–37
    [Google Scholar]
  64. 64.  Lux SE 2015. Blood 127:187–99
    [Google Scholar]
  65. 65.  Salbreux G, Charras G, Paluch E 2012. Trends Cell Biol. 22:536–45
    [Google Scholar]
  66. 66.  Sackmann E, Smith AS 2014. Soft Matter 10:1644
    [Google Scholar]
  67. 67.  Manno S, Takakuwa Y, Mohandas N 2004. J. Biol. Chem. 280:7581–87
    [Google Scholar]
  68. 68.  Ben-Isaac E, Park Y, Popescu G, Brown FLH, Gov NS, Shokef Y 2011. Phys. Rev. Lett. 106:238103
    [Google Scholar]
  69. 69.  Zhang R, Brown FLH 2008. J. Chem. Phys. 129:065101
    [Google Scholar]
  70. 70.  Dubus C, Fournier JB 2006. Europhys. Lett. 75:181–87
    [Google Scholar]
  71. 71.  Okamoto R, Komura S, Fournier JB 2017. Phys. Rev. E 96:012416
    [Google Scholar]
  72. 72.  Biswas A, Alex A, Sinha B 2017. Biophys. J. 113:1768–81
    [Google Scholar]
  73. 73.  Hui KL, Wang C, Grooman B, Wayt J, Upadhyaya A 2012. Biophys. J. 102:1524–33
    [Google Scholar]
  74. 74.  Kabaso D, Shlomovitz R, Schloen K, Stradal T, Gov NS 2011. PLOS Comput. Biol. 7:e1001127
    [Google Scholar]
  75. 75.  Gov NS, Gopinathan A 2006. Biophys. J. 90:454–69
    [Google Scholar]
  76. 76.  Shlomovitz R, Gov NS 2008. Phys. Rev. E 78:041911
    [Google Scholar]
  77. 77.  Srivastava P, Shlomovitz R, Gov NS, Rao M 2013. Phys. Rev. Lett. 110:168104
    [Google Scholar]
  78. 78.  Seifert U 1994. Phys. Rev. E 49:3124–27
    [Google Scholar]
  79. 79.  Fenz SF, Bihr T, Schmidt D, Merkel R, Seifert U et al. 2017. Nat. Phys. 13:906–13
    [Google Scholar]
  80. 80.  Rozycki B, Lipowsky R, Weikl TR 2006. Phys. Rev. Lett. 96:048101
    [Google Scholar]
  81. 81.  Charras GT, Coughlin M, Mitchison TJ, Mahadevan L 2008. Biophys. J. 94:1836–53
    [Google Scholar]
  82. 82.  Peukes J, Betz T 2014. Biophys. J. 107:1810–20
    [Google Scholar]
  83. 83.  Goudarzi M, Tarbashevich K, Mildner K, Begemann I, Garcia J et al. 2017. Dev. Cell 43:577–87
    [Google Scholar]
  84. 84.  Montigny C, Lyons J, Champeil P, Nissen P, Lenoir G 2016. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1861:767–83
    [Google Scholar]
  85. 85.  Hankins H, Baldridge R, Xu P, Graham T 2015. Traffic 16:35–47
    [Google Scholar]
  86. 86.  Papadopulos A, Vehring S, Lopez-Montero I, Kutschenko L, Stockl M et al. 2007. J. Biol. Chem. 282:15559–68
    [Google Scholar]
  87. 87.  Ramachandran S, Kumar PBS, Laradji M 2008. J. Chem. Phys. 129:125104
    [Google Scholar]
  88. 88.  Rao M, Sarasij RC 2001. Phys. Rev. Lett. 87:128101
    [Google Scholar]
  89. 89.  Ramaswamy S, Rao M 2001. C. R. Acad. Sci. Ser. IV Phys. Astrophys. 2:817–39
    [Google Scholar]
  90. 90.  Sens P 2004. Phys. Rev. Lett. 93:108103
    [Google Scholar]
  91. 91.  Sinha B, Köster D, Ruez R, Gonnord P, Bastiani M et al. 2011. Cell 144:402–13
    [Google Scholar]
  92. 92.  Solon J, Pecreaux J, Girard P, Faure MC, Prost J, Bassereau P 2006. Phys. Rev. Lett. 97:098103
    [Google Scholar]
  93. 93.  Junge W, Nelson N 2015. Annu. Rev. Biochem. 84:631–57
    [Google Scholar]
  94. 94.  Almendro-Vedia V, Natale P, Mell M, Bonneau S, Monroy F et al. 2017. PNAS 114:11291–96
    [Google Scholar]
  95. 95.  Paoluzzi M, Leonardo RD, Marchetti MC, Angelani L 2016. Sci. Rep. 6:34146
    [Google Scholar]
  96. 96.  Bar-Ziv R, Moses E, Nelson P 1998. Biophys. J. 75:294–320
    [Google Scholar]
  97. 97.  Brown A, Kotar J, Cicuta P 2011. Phys. Rev. E Stat. Nonlinear Soft Matter Phys. 84:021930
    [Google Scholar]
  98. 98.  Ziebert F, Bazant MZ, Lacoste D 2010. Phys. Rev. E 81:031912
    [Google Scholar]
  99. 99.  Lacoste D, Lagomarsino MC, Joanny JF 2007. Europhys. Lett. 77:18006
    [Google Scholar]
  100. 100.  Ambjornsson T, Lomholt MA, Hansen PL 2007. Phys. Rev. E 75:051916
    [Google Scholar]
  101. 101.  Callen HB, Welton TA 1951. Phys. Rev. 83:34–40
    [Google Scholar]
  102. 102.  Boss D, Hoffmann A, Rappaz B, Depeursinge C, Magistretti PJ et al. 2012. PLOS ONE 7:e40667
    [Google Scholar]
  103. 103.  Rodriguez-Garcia R, Lopez-Montero I, Mell M, Egea G, Gov N, Monroy F 2016. Biophys. J. 111:1101
    [Google Scholar]
  104. 104.  Monzel C, Schmidt D, Kleusch C, Kirchenbuchler D, Seifert U et al. 2015. Nat. Commun. 6:9162
    [Google Scholar]
  105. 105.  Park Y, Best CA, Auth T, Gov NS, Safran SA et al. 2010. PNAS 107:1289–94
    [Google Scholar]
  106. 106.  Gögler M, Betz T, Käs JA 2007. Opt. Lett. 32:1893
    [Google Scholar]
  107. 107.  Mizuno D, Tardin C, Schmidt CF, MacKintosh FC 2007. Science 315:370–73
    [Google Scholar]
  108. 108.  Martin P, Hudspeth AJ, Jülicher F 2001. PNAS 98:14380–85
    [Google Scholar]
  109. 109.  Yoon YZ, Kotar J, Brown AT, Cicuta P 2011. Soft Matter 7:2042–51
    [Google Scholar]
  110. 110.  Manno S, Takakuwa Y, Nagao K, Mohandas N 1995. J. Biol. Chem. 270:5659–65
    [Google Scholar]
  111. 111.  Seifert U, Langer SA 1994. Biophys. Chem. 49:13–22
    [Google Scholar]
  112. 112.  Gov NS 2007. Phys. Rev. E 75:011921
    [Google Scholar]
  113. 113.  Subrahmanyam G, Bertics PJ, Anderson RA 1991. PNAS 88:5222–26
    [Google Scholar]
  114. 114.  Sheetz MP 1977. J. Cell Biol. 73:638–46
    [Google Scholar]
  115. 115.  Rangamani P, Mandadap K, Oster G 2014. Biophys. J. 107:751–62
    [Google Scholar]
  116. 116.  Gauthier NC, Fardin MA, Roca-Cusachs P, Sheetz MP 2011. PNAS 108:14467–72
    [Google Scholar]
  117. 117.  Charras GT, Williams BA, Sims SM, Horton MA 2004. Biophys. J. 87:2870–84
    [Google Scholar]
  118. 118.  Lin LCL, Brown FL 2004. Biophys. J. 86:764–80
    [Google Scholar]
  119. 119.  Mostowy S, Cossart P 2012. Nat. Rev. Mol. Cell Biol. 13:183–94
    [Google Scholar]
  120. 120.  Loose M, Mitchison TJ 2013. Nat. Cell Biol. 16:38–46
    [Google Scholar]
  121. 121.  Rao M, Mayor S 2014. Curr. Opin. Cell Biol. 29:126–32
    [Google Scholar]
  122. 122.  Small J, Stradal T, Vignal E, Rottner K 2002. Trends Cell Biol. 12:112–20
    [Google Scholar]
  123. 123.  Mattila PK, Lappalainen P 2008. Nat. Rev. Mol. Cell Biol. 9:446–54
    [Google Scholar]
  124. 124.  Dmitrieff S, Nedelec F 2015. PLOS Comput. Biol. 11:e1004538
    [Google Scholar]
  125. 125.  Köster DV, Husain K, Iljazi E, Bhat A, Bieling P et al. 2016. PNAS 113:E1645–54
    [Google Scholar]
  126. 126.  Prost J, Jülicher F, Joanny JF 2015. Nat. Phys. 11:111–17
    [Google Scholar]
  127. 127.  Turlier H, Audoly B, Prost J, Joanny JF 2014. Biophys. J. 106:114–23
    [Google Scholar]
  128. 128.  Salbreux G, Jülicher F 2017. Phys. Rev. E 96:032404
    [Google Scholar]
  129. 129.  Shlomovitz R, Gov N 2009. Phys. Biol. 6:046017
    [Google Scholar]
  130. 130.  Maitra A, Srivastava P, Rao M, Ramaswamy S 2014. Phys. Rev. Lett. 112:258101
    [Google Scholar]
  131. 131.  Caorsi V, Lemiere J, Campillo C, Bussonnier M, Manzi J et al. 2016. Soft Matter 12:6223–31
    [Google Scholar]
  132. 132.  Guevorkian K, Manzi J, Pontani LL, Brochard-Wyart F, Sykes C 2015. Biophys. J. 109:2471–79
    [Google Scholar]
  133. 133.  Carvalho K, Tsai FC, Lees E, Voituriez R, Koenderink GH, Sykes C 2013. PNAS 110:16456–61
    [Google Scholar]
  134. 134.  Carvalho K, Lemiere J, Faqir F, Manzi J, Blanchoin L et al. 2013. Philos. Trans. R. Soc. B: Biol. Sci. 368:20130005
    [Google Scholar]
  135. 135.  Enas AS, Kinneret K 2013. Front. Immunol. 4:01001
    [Google Scholar]
  136. 136.  Linsmeier I, Banerjee S, Oakes PW, Jung W, Kim T, Murrell MP 2016. Nat. Commun. 7:12615
    [Google Scholar]
  137. 137.  Loiseau E, Schneider JAM, Keber FC, Pelzl C, Massiera G et al. 2016. Sci. Adv. 2:e1500465
    [Google Scholar]
  138. 138.  Lin LCL, Brown FLH 2004. Phys. Rev. Lett. 93:256001
    [Google Scholar]
  139. 139.  Brannigan G, Lin LCL, Brown FLH 2005. Eur. Biophys. J. 35:104–24
    [Google Scholar]
  140. 140.  Lin LCL, Brown FLH 2006. J. Chem. Theory Comput. 2:472–83
    [Google Scholar]
  141. 141.  Peskin CS 2002. Acta Numerica 2002 A Iserles479518 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  142. 142.  Eggleton CD, Popel AS 1998. Phys. Fluids 10:1834–45
    [Google Scholar]
  143. 143.  Pozrikidis C 2005. Ann. Biomed. Eng. 33:165–78
    [Google Scholar]
  144. 144.  Hoogerbrugge PJ, Koelman JMVA 1992. Europhys. Lett. 19:155–60
    [Google Scholar]
  145. 145.  Peng Z, Asaro RJ, Zhu Q 2011. J. Fluid Mech. 686:299–337
    [Google Scholar]
  146. 146.  Atzberger PJ, Kramer PR, Peskin CS 2007. J. Comput. Phys. 224:1255–92
    [Google Scholar]
  147. 147.  Fedosov DA, Caswell B, Karniadakis GE 2010. Biophys. J. 98:2215–25
    [Google Scholar]
  148. 148.  Peng Z, Li X, Pivkin IV, Dao M, Karniadakis GE, Suresh S 2013. PNAS 110:13356–61
    [Google Scholar]
/content/journals/10.1146/annurev-conmatphys-031218-013757
Loading
/content/journals/10.1146/annurev-conmatphys-031218-013757
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