1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Condensed Matter Physics
  4. Volume 8, 2017
  5. Article

Annual Review of Condensed Matter Physics

Volume 8, 2017

Intracellular Oscillations and Waves

Abstract

Dynamic processes in living cells are highly organized in space and time. Unraveling the underlying molecular mechanisms of spatiotemporal pattern formation remains one of the outstanding challenges at the interface between physics and biology. A fundamental recurrent pattern found in many different cell types is that of self-sustained oscillations. They are involved in a wide range of cellular functions, including second messenger signaling, gene expression, and cytoskeletal dynamics. Here, we review recent developments in the field of cellular oscillations and focus on cases where concepts from physics have been instrumental for understanding the underlying mechanisms. We consider biochemical and genetic oscillators as well as oscillations that arise from chemo-mechanical coupling. Finally, we highlight recent studies of intracellular waves that have increasingly moved into the focus of this research field.

Keyword(s): actin waves, biochemical oscillators, chemomechanical coupling, genetic networks, self-sustained oscillations
Loading

Article metrics loading...

/content/journals/10.1146/annurev-conmatphys-031016-025210
2017-03-31
2024-10-07
Loading full text...

Full text loading...

/deliver/fulltext/conmatphys/8/1/annurev-conmatphys-031016-025210.html?itemId=/content/journals/10.1146/annurev-conmatphys-031016-025210&mimeType=html&fmt=ahah

Literature Cited

  1. Dibner C, Schibler U, Albrecht U. 1.  2010. Annu. Rev. Physiol. 72:517–49 [Google Scholar]
  2. Bray D. 2.  2001. Cell Movements: From Molecules to Motility. New York: Taylor & Francis, 2nd ed.. [Google Scholar]
  3. Loose M, Kruse K, Schwille P. 3.  2011. Annu. Rev. Biophys. 40:315–36 [Google Scholar]
  4. Morin X, Bellaïche Y. 4.  2011. Dev. Cell 21:102–19 [Google Scholar]
  5. Marchetti MC, Joanny JF, Ramaswamy S, Liverpool TB, Prost J. 5.  et al. 2013. Rev. Mod. Phys. 85:1143 [Google Scholar]
  6. Hodgkin AL, Huxley AF. 6.  1952. J. Physiol. 117:500–44 [Google Scholar]
  7. Jaffe LF. 7.  1993. Cell Calcium 14:736–45 [Google Scholar]
  8. Raskin DM, de Boer PAJ. 8.  1999. PNAS 96:4971–76 [Google Scholar]
  9. Weiner OD, Marganski WA, Wu LF, Altschuler SJ, Kirschner MW. 9.  2007. PLOS Biol. 5:e221 [Google Scholar]
  10. Strogatz SH. 10.  1994. Nonlinear Dynamics and Chaos: With Applications to Physics, Biology, Chemistry, and Engineering Boulder, CO: Westview [Google Scholar]
  11. Novák B, Tyson JJ. 11.  2008. Nat. Rev. Mol. Cell Biol. 9:981–91 [Google Scholar]
  12. Tsai TYC, Choi YS, Ma W, Pomerening JR, Tang C, Ferrell JE. 12.  2008. Science 321:126–29 [Google Scholar]
  13. Dörfler F, Bullo F. 13.  2014. Automatica 50:1539–64 [Google Scholar]
  14. Aranson IS, Kramer L. 14.  2002. Rev. Mod. Phys. 74:99–143 [Google Scholar]
  15. Richard P. 15.  2003. FEMS Microbiol. Rev. 27:547–57 [Google Scholar]
  16. Berridge MJ, Lipp P, Bootman MD. 16.  2000. Nat. Rev. Mol. Cell Biol. 1:11–21 [Google Scholar]
  17. Falcke M. 17.  2004. Adv. Phys. 53:255–440 [Google Scholar]
  18. Thurley K, Skupin A, Thul R, Falcke M. 18.  2012. Biochim. Biophys. Acta (BBA) Gen. Subj. 1820:1185–94 [Google Scholar]
  19. Martiel JL, Goldbeter A. 19.  1987. Biophys. J. 52:807–28 [Google Scholar]
  20. Skupin A, Kettenmann H, Winkler U, Wartenberg M, Sauer H. 20.  et al. 2008. Biophys. J. 94:2404–11 [Google Scholar]
  21. Skupin A, Kettenmann H, Falcke M. 21.  2010. PLOS Comput. Biol. 6:e1000870 [Google Scholar]
  22. Thurley K, Tovey SC, Moenke G, Prince VL, Meena A. 22.  et al. 2014. Sci. Signal. 7:331ra59 [Google Scholar]
  23. Dyachok O, Isakov Y, Sgetorp J, Tengholm A. 23.  2006. Nature 439:349–52 [Google Scholar]
  24. Garmendia-Torres C, Goldbeter A, Jacquet M. 24.  2007. Curr. Biol. 17:1044–49 [Google Scholar]
  25. Gerisch G, Hess B. 25.  1974. PNAS 71:2118–22 [Google Scholar]
  26. Kessin RH. 26.  2010. Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity Cambridge, UK: Cambridge University Press [Google Scholar]
  27. Goldbeter A. 27.  2006. Bull. Math. Biol. 68:1095–109 [Google Scholar]
  28. Maeda M, Lu S, Shaulsky G, Miyazaki Y, Kuwayama H. 28.  et al. 2004. Science 304:875–78 [Google Scholar]
  29. Kim J, Heslop-Harrison P, Postlethwaite I, Bates DG. 29.  2007. PLOS Comput. Biol. 3:e218 [Google Scholar]
  30. Nagano S, Sakurai S. 30.  2013. Phys. Rev. E 88:062710 [Google Scholar]
  31. Sawai S, Thomason PA, Cox EC. 31.  2005. Nature 433:323–26 [Google Scholar]
  32. Gregor T, Fujimoto K, Masaki N, Sawai S. 32.  2010. Science 328:1021–25 [Google Scholar]
  33. Sgro AE, Schwab DJ, Noorbakhsh J, Mestler T, Mehta P, Gregor T. 33.  2015. Mol. Syst. Biol. 11:779 [Google Scholar]
  34. Schäfer E, Westendorf C, Bodenschatz E, Beta C, Geil B, Janshoff A. 34.  2011. Small 7:723–26 [Google Scholar]
  35. Leonhardt H, Gerhardt M, Höppner N, Krüger K, Tarantola M, Beta C. 35.  2016. Phys. Rev. E 93:012414 [Google Scholar]
  36. Corrigan A, Chubb J. 36.  2014. Curr. Biol. 24:205–11 [Google Scholar]
  37. Cai H, Katoh-Kurasawa M, Muramoto T, Santhanam B, Long Y. 37.  et al. 2014. Science 343:1249531 [Google Scholar]
  38. Johnson CH, Stewart PL, Egli M. 38.  2011. Annu. Rev. Biophys. 40:143–67 [Google Scholar]
  39. Tomita J, Nakajima M, Kondo T, Iwasaki H. 39.  2005. Science 307:251–54 [Google Scholar]
  40. Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y. 40.  et al. 2005. Science 308:414–15 [Google Scholar]
  41. Cohen SE, Golden SS. 41.  2015. Microbiol. Mol. Biol. Rev. 79:373–85 [Google Scholar]
  42. van Zon JS, Lubensky DK, Altena PR, ten Wolde PR. 42.  2007. PNAS 104:7420–25 [Google Scholar]
  43. Lin J, Chew J, Chockanathan U, Rust MJ. 43.  2014. PNAS 111:E3937–45 [Google Scholar]
  44. Qin X, Byrne M, Mori T, Zou P, Williams DR. 44.  et al. 2010. PNAS 107:14805–10 [Google Scholar]
  45. Abe J, Hiyama TB, Mukaiyama A, Son S, Mori T. 45.  et al. 2015. Science 349:312–16 [Google Scholar]
  46. Teng SW, Mukherji S, Moffitt JR, Buyl Sd, O'Shea EK. 46.  2013. Science 340:737–40 [Google Scholar]
  47. Reddy AB, Rey G. 47.  2014. Annu. Rev. Biochem. 83:165–89 [Google Scholar]
  48. Zhang EE, Kay SA. 48.  2010. Nat. Rev. Mol. Cell Biol. 11:764–76 [Google Scholar]
  49. Bhargava A, Herzel H, Ananthasubramaniam B. 49.  2015. BMC Syst. Biol. 9:78 [Google Scholar]
  50. Hardin PE, Hall JC, Rosbash M. 50.  1990. Nature 343:536–40 [Google Scholar]
  51. Richards J, Gumz ML. 51.  2012. FASEB J. 26:3602–13 [Google Scholar]
  52. Borgs L, Beukelaers P, Vandenbosch R, Belachew S, Nguyen L, Malgrange B. 52.  2009. Cell Cycle 8:832–37 [Google Scholar]
  53. Reddy AB, O'Neill JS. 53.  2010. Trends Cell Biol. 20:36–44 [Google Scholar]
  54. Fuhr L, Abreu M, Pett P, Relgio A. 54.  2015. Comput. Struct. Biotechnol. J. 13:417–26 [Google Scholar]
  55. Hubaud A, Pourquié O. 55.  2014. Nat. Publ. Group 15:709–21 [Google Scholar]
  56. Palmeirim I, Henrique D, Ish-Horowicz D, Pourquié O. 56.  1997. Cell 91:639–48 [Google Scholar]
  57. Masamizu Y, Ohtsuka T, Takashima Y, Nagahara H, Takenaka Y. 57.  et al. 2006. PNAS 103:1313–18 [Google Scholar]
  58. Webb AB, Lengyel IM, Jörg DJ, Valentin G, Jülicher F. 58.  et al. 2016. Elife 5:e08438 [Google Scholar]
  59. Aulehla A, Wiegraebe W, Baubet V, Wahl MB, Deng C. 59.  et al. 2008. Nat. Cell Biol. 10:186–93 [Google Scholar]
  60. Jiang YJ, Aerne BL, Smithers L, Haddon C, Ish-Horowicz D, Lewis J. 60.  2000. Nature 408:475–79 [Google Scholar]
  61. Yeung M, Strogatz SH. 61.  1999. Phys. Rev. Lett. 82:648–51 [Google Scholar]
  62. Ares S, Morelli LG, Jörg DJ, Oates AC, Jülicher F. 62.  2012. Phys. Rev. Lett. 108:204101 [Google Scholar]
  63. Soroldoni D, Jörg DJ, Morelli LG, Richmond DL, Schindelin J. 63.  et al. 2014. Science 345:222–25 [Google Scholar]
  64. Tsai TYC, Theriot JA, Ferrell JE. 64.  2014. PLOS Biol. 12:e1001788 [Google Scholar]
  65. Sagara H, Ohshima D, Ichikawa K. 65.  2015. IET Syst. Biol. 9:41–51 [Google Scholar]
  66. Ashall L, Horton CA, Nelson DE, Paszek P, Harper CV. 66.  et al. 2009. Science 324:242–46 [Google Scholar]
  67. Mothes J, Busse D, Kofahl B, Wolf J. 67.  2015. BioEssays 37:452–62 [Google Scholar]
  68. Hughey JJ, Gutschow MV, Bajar BT, Covert MW. 68.  2015. Mol. Biol. Cell 26:583–90 [Google Scholar]
  69. Vousden KH, Lane DP. 69.  2007. Nat. Rev. Mol. Cell Biol. 8:275–83 [Google Scholar]
  70. Purvis JE, Karhohs KW, Mock C, Batchelor E, Loewer A, Lahav G. 70.  2012. Science 336:1440–44 [Google Scholar]
  71. Ru P, Garcia-Ojalvo J. 71.  2013. Annu. Rev. Biophys. 42:605–27 [Google Scholar]
  72. Isomura A, Kageyama R. 72.  2014. Development 141:3627–36 [Google Scholar]
  73. Cameron DE, Bashor CJ, Collins JJ. 73.  2014. Nat. Rev. Microbiol. 12:381–90 [Google Scholar]
  74. Purcell O, Savery NJ, Grierson CS, di Bernardo M. 74.  2010. J. R. Soc. Interface 7:1503–24 [Google Scholar]
  75. Elowitz MB, Leibler S. 75.  2000. Nature 403:335–38 [Google Scholar]
  76. Atkinson MR, Savageau MA, Myers JT, Ninfa AJ. 76.  2003. Cell 113:597–607 [Google Scholar]
  77. Fung E, Wong WW, Suen JK, Bulter T, Lee Sg, Liao JC. 77.  2005. Nature 435:118–22 [Google Scholar]
  78. Stricker J, Cookson S, Bennett MR, Mather WH, Tsimring LS, Hasty J. 78.  2008. Nature 456:516–19 [Google Scholar]
  79. Tigges M, Marquez-Lago TT, Stelling J, Fussenegger M. 79.  2009. Nature 457:309–12 [Google Scholar]
  80. Chen Y, Kim JK, Hirning AJ, Josic K, Bennett MR. 80.  2015. Science 349:986–89 [Google Scholar]
  81. Kim J, Winfree E. 81.  2011. Mol. Syst. Biol. 7:465 [Google Scholar]
  82. Montagne K, Plasson R, Sakai Y, Fujii T, Rondelez Y. 82.  2011. Mol. Syst. Biol. 7:466 [Google Scholar]
  83. Weitz M, Kim J, Kapsner K, Winfree E, Franco E, Simmel FC. 83.  2014. Nat. Chem. 6:295–302 [Google Scholar]
  84. Carlier MF, Melki R, Pantaloni D, Hill TLL, Chen Y. 84.  1987. PNAS 84:5257–61 [Google Scholar]
  85. Zelinski B, Kierfeld J. 85.  2013. Phys. Rev. E 87:012703 [Google Scholar]
  86. Prost J. 86.  2002. Physics of Bio-Molecules and Cells, Les Houches Session LXXV, 2–27 July 2001 H Flyvbjerg, F Jülicher, P Ormos, F David New York: Springer [Google Scholar]
  87. Cameron LA, Footer MJ, van Oudenaarden A, Theriot JA. 87.  1999. PNAS 96:4908–13 [Google Scholar]
  88. Boukellal H, Campas O, Joanny JF, Prost J, Sykes C. 88.  2004. Phys. Rev. E 69:061906 [Google Scholar]
  89. Bernheim-Groswasser A, Wiesner S, Golsteyn RM, Carlier MF, Sykes C. 89.  2002. Nature 417:308–11 [Google Scholar]
  90. Placais PY, Balland M, Guerin T, Joanny JF, Martin P. 90.  2009. Phys. Rev. Lett. 103:158102 [Google Scholar]
  91. Günther S, Kruse K. 91.  2007. New J. Phys. 9:417 [Google Scholar]
  92. Paluch E, Piel M, Prost J, Bornens M, Sykes C. 92.  2005. Biophys. J. 89:724–33 [Google Scholar]
  93. Jülicher F, Prost J. 93.  1997. Phys. Rev. Lett. 78:4510–13 [Google Scholar]
  94. Jülicher F, Prost J. 94.  1995. Phys. Rev. Lett. 75:2618–21 [Google Scholar]
  95. Grill SW, Kruse K, Jülicher F. 95.  2005. Phys. Rev. Lett. 94:108104 [Google Scholar]
  96. Guerin T, Prost J, Joanny JF. 96.  2010. Phys. Rev. Lett. 104:248102 [Google Scholar]
  97. Okamura N, Ishiwata S. 97.  1988. J. Muscle Res. Cell. Motil. 9:111–19 [Google Scholar]
  98. Sato K, Kuramoto Y, Ohtaki M, Shimamoto Y, Ishiwata S. 98.  2013. Phys. Rev. Lett. 111:108104 [Google Scholar]
  99. Kozlowski C, Srayko M, Nedelec F. 99.  2007. Cell 129:499–510 [Google Scholar]
  100. Pecreaux J, Röper JC, Kruse K, Jülicher F, Hyman AA. 100.  et al. 2006. Curr. Biol. 16:2111–22 [Google Scholar]
  101. Skibbens RV, Skeen VP, Salmon ED. 101.  1993. J. Cell Biol. 122:859–75 [Google Scholar]
  102. Campàs O, Sens P. 102.  2006. Phys. Rev. Lett. 97:128102 [Google Scholar]
  103. Joglekar AP, Hunt AJ. 103.  2002. Biophys. J. 83:42–58 [Google Scholar]
  104. Civelekoglu-Scholey G, Sharp DJ, Mogilner A, Scholey JM. 104.  2006. Biophys. J. 90:3966–82 [Google Scholar]
  105. Chikashige Y, Ding DQ, Funabiki T, Haraguchi T, Mashiko S. 105.  et al. 1994. Science 264:270–73 [Google Scholar]
  106. Vogel SK, Pavin N, Maghelli N, Jülicher F, Tolić-Nørrelykke IM. 106.  2009. PLOS Biol. 7:e1000087 [Google Scholar]
  107. Camalet S, Jülicher F. 107.  2000. New J. Phys. 2:24 [Google Scholar]
  108. Sanchez T, Welch D, Nicastro D, Dogic Z. 108.  2011. Science 333:456–59 [Google Scholar]
  109. Brumley DR, Polin M, Pedley TJ, Goldstein RE. 109.  2015. J. R. Soc. Interface 12:20141358 [Google Scholar]
  110. Quaranta G, Aubin-Tam ME, Tam D. 110.  2015. Phys. Rev. Lett. 115:238101 [Google Scholar]
  111. Martin P, Hudspeth AJ. 111.  1999. PNAS 96:14306–11 [Google Scholar]
  112. Camalet S, Duke T, Jülicher F, Prost J. 112.  2000. PNAS 97:3183–88 [Google Scholar]
  113. Eguíluz VM, Ospeck M, Choe Y, Hudspeth AJ, Magnasco MO. 113.  2000. Phys. Rev. Lett. 84:5232–35 [Google Scholar]
  114. Balakrishnan J, Ashok B. 114.  2010. J. Theor. Biol. 265:126–35 [Google Scholar]
  115. Mora T, Bialek W. 115.  2011. J. Stat. Phys. 144:268–302 [Google Scholar]
  116. Kay LM, Beshel J, Brea J, Martin C, Rojas-Líbano D, Kopell N. 116.  2009. Trends Neurosci. 32:207–14 [Google Scholar]
  117. Koepsell K, Wang X, Hirsch JA, Sommer FT. 117.  2010. Front. Neurosci. 4:53–61 [Google Scholar]
  118. Arnal LH, Giraud AL. 118.  2012. Trends Cogn. Sci. 16:390–98 [Google Scholar]
  119. Bornens M, Paintrand M, Celati C. 119.  1989. J. Cell Biol. 109:1071–83 [Google Scholar]
  120. Pletjushkina OJ, Rajfur Z, Pomorski P, Oliver TN, Vasiliev JM, Jacobson KA. 120.  2001. Cell Motil. Cytoskeleton 48:235–44 [Google Scholar]
  121. Salbreux G, Joanny JF, Prost J, Pullarkat P. 121.  2007. Phys. Biol. 4:268–84 [Google Scholar]
  122. Sedzinski J, Biro M, Oswald A, Tinevez JY, Salbreux G, Paluch E. 122.  2011. Nature 476:462–66 [Google Scholar]
  123. Martin AC, Kaschube M, Wieschaus EF. 123.  2009. Nature 457:495–99 [Google Scholar]
  124. Solon J, Kaya-Copur A, Colombelli J, Brunner D. 124.  2009. Cell 137:1331–42 [Google Scholar]
  125. Westendorf C, Negrete J, Bae AJ, Sandmann R, Bodenschatz E, Beta C. 125.  2013. PNAS 110:3853–58 [Google Scholar]
  126. Huang CH, Tang M, Shi C, Iglesias PA, Devreotes PN. 126.  2013. Nat. Cell Biol. 15:1307–16 [Google Scholar]
  127. Hoeller O, Toettcher JE, Cai H, Sun Y, Huang CH. 127.  et al. 2016. PLOS Biol. 14:e1002381 [Google Scholar]
  128. Vecchiarelli AG, Li M, Mizuuchi M, Hwang LC, Seol Y. 128.  et al. 2016. PNAS 113:E1479–88 [Google Scholar]
  129. Fischer-Friedrich E, Meacci G, Lutkenhaus J, Chaté H, Kruse K. 129.  2010. PNAS 107:6134–39 [Google Scholar]
  130. Bonny M, Fischer-Friedrich E, Loose M, Schwille P, Kruse K. 130.  2013. PLOS Comput. Biol. 9:e1003347 [Google Scholar]
  131. Loose M, Fischer-Friedrich E, Ries J, Kruse K, Schwille P. 131.  2008. Science 320:789–92 [Google Scholar]
  132. Loose M, Fischer-Friedrich E, Herold C, Kruse K, Schwille P. 132.  2011. Nat. Struct. Mol. Biol. 18:577–83 [Google Scholar]
  133. Schweizer J, Loose M, Bonny M, Kruse K, Mönch I, Schwille P. 133.  2012. PNAS 109:15283–88 [Google Scholar]
  134. Zieske K, Schwille P. 134.  2013. Angew. Chem. Int. Ed. Engl. 52:459–62 [Google Scholar]
  135. Allard J, Mogilner A. 135.  2013. Curr. Opin. Cell Biol. 25:107–15 [Google Scholar]
  136. Alt W, Brosteanu O, Hinz B, Kaiser HW. 136.  1995. Biochem. Cell Biol. 73:441–59 [Google Scholar]
  137. Vicker MG, Xiang W, Plath PJ, Wosniok W. 137.  1997. Phys. D: Nonlinear Phenom. 101:317–32 [Google Scholar]
  138. Verkhovsky AB. 138.  2015. Curr. Opin. Cell Biol. 36:113–21 [Google Scholar]
  139. Giannone G, Dubin-Thaler BJ, Döbereiner HG, Kieffer N, Bresnick AR, Sheetz MP. 139.  2004. Cell 116:431–43 [Google Scholar]
  140. Machacek M, Danuser G. 140.  2006. Biophys. J. 90:1439–52 [Google Scholar]
  141. Döbereiner HG, Dubin-Thaler BJ, Hofman JM, Xenias HS, Sims TN. 141.  et al. 2006. Phys. Rev. Lett. 97:038102 [Google Scholar]
  142. Driscoll MK, Losert W, Jacobson K, Kapustina M. 142.  2015. Cytoskeleton 72:268–81 [Google Scholar]
  143. Driscoll MK, McCann C, Kopace R, Homan T, Fourkas JT. 143.  et al. 2012. PLOS Comput. Biol. 8:e1002392 [Google Scholar]
  144. Wang C, Chowdhury S, Driscoll M, Parent CA, Gupta SK, Losert W. 144.  2014. J. R. Soc. Interface 11:20140684 [Google Scholar]
  145. Barnhart EL, Lee KC, Keren K, Mogilner A, Theriot JA. 145.  2011. PLOS Biol. 9:e1001059 [Google Scholar]
  146. Buccione R, Orth JD, McNiven MA. 146.  2004. Nat. Rev. Mol. Cell Biol. 5:647–57 [Google Scholar]
  147. Bernitt E, Koh CG, Gov N, Döbereiner HG. 147.  2015. PLOS ONE 10:e0115857 [Google Scholar]
  148. Gerisch G, Bretschneider T, Müller-Taubenberger A, Simmeth E, Ecke M. 148.  et al. 2004. Biophys. J. 87:3493–503 [Google Scholar]
  149. Gerhardt M, Ecke M, Walz M, Stengl A, Beta C, Gerisch G. 149.  2014. J. Cell Sci. 127:4507–17 [Google Scholar]
  150. Bement WM, Leda M, Moe AM, Kita AM, Larson ME. 150.  et al. 2015. Nat. Cell Biol. 17:1471–83 [Google Scholar]
  151. Asano Y, Nagasaki A, Uyeda TQ. 151.  2008. Cell Motil. Cytoskeleton 65:923–34 [Google Scholar]
  152. Wu M, Wu X, Camilli PD. 152.  2013. PNAS 110:1339–44 [Google Scholar]
  153. Xiong D, Xiao S, Guo S, Lin Q, Nakatsu F, Wu M. 153.  2016. Nat. Chem. Biol. 12:159–66 [Google Scholar]
  154. Case LB, Waterman CM. 154.  2011. PLOS ONE 6:e26631 [Google Scholar]
  155. Sun X, Driscoll MK, Guven C, Das S, Parent CA. 155.  et al. 2015. PNAS 112:12557–62 [Google Scholar]
  156. Guetta-Terrier C, Monzo P, Zhu J, Long H, Venkatraman L. 156.  et al. 2015. J. Cell Biol. 211:683–701 [Google Scholar]
  157. Doubrovinski K, Kruse K. 157.  2008. Europhys. Lett. 83:18003 [Google Scholar]
  158. Whitelam S, Bretschneider T, Burroughs NJ. 158.  2009. Phys. Rev. Lett. 102:198103 [Google Scholar]
  159. Carlsson AE. 159.  2010. Phys. Rev. Lett. 104:228102 [Google Scholar]
  160. Holmes WR, Carlsson AE, Edelstein-Keshet L. 160.  2012. Phys. Biol. 9:046005 [Google Scholar]
  161. Khamviwath V, Hu J, Othmer HG. 161.  2013. PLOS ONE 8:e64272 [Google Scholar]
  162. Wasnik V, Mukhopadhyay R. 162.  2014. Phys. Rev. E 90:052707 [Google Scholar]
  163. Doubrovinski K, Kruse K. 163.  2007. Phys. Rev. Lett. 99:228104 [Google Scholar]
  164. Shlomovitz R, Gov NS. 164.  2007. Phys. Rev. Lett. 98:168103 [Google Scholar]
  165. Gholami A, Enculescu M, Falcke M. 165.  2012. New J. Phys. 14:115002 [Google Scholar]
  166. Bois JS, Jülicher F, Grill SW. 166.  2011. Phys. Rev. Lett. 106:028103 [Google Scholar]
  167. Radszuweit M, Alonso S, Engel H, Bär M. 167.  2013. Phys. Rev. Lett. 110:138102 [Google Scholar]
  168. Vicker MG. 168.  2000. Biophys. Chem. 84:87–98 [Google Scholar]
  169. Bretschneider T, Anderson K, Ecke M, Müller-Taubenberger A, Schroth-Diez B. 169.  et al. 2009. Biophys. J. 96:2888–900 [Google Scholar]
  170. Taniguchi D, Ishihara S, Oonuki T, Honda-Kitahara M, Kaneko K, Sawai S. 170.  2013. PNAS 110:5016–21 [Google Scholar]
  171. Doubrovinski K, Kruse K. 171.  2011. Phys. Rev. Lett. 107:258103 [Google Scholar]
  172. Dreher A, Aranson IS, Kruse K. 172.  2014. New J. Phys. 16:055007 [Google Scholar]
  173. Gerisch G, Ecke M, Schroth-Diez B, Gerwig S, Engel U. 173.  et al. 2009. Cell Adhes. Migr. 3:373–82 [Google Scholar]
  174. Gerisch G. 174.  2010. PMC Biophys. 3:7 [Google Scholar]
  175. Brzeska H, Pridham K, Chery G, Titus MA, Korn ED. 175.  2014. PLOS ONE 9:e94306 [Google Scholar]
  176. Gerisch G, Schroth-Diez B, Müller-Taubenberger A, Ecke M. 176.  2012. Biophys. J. 103:1170–78 [Google Scholar]
  177. Knoch F, Tarantola M, Bodenschatz E, Rappel WJ. 177.  2014. Phys. Biol. 11:046002 [Google Scholar]
  178. Arai Y, Shibata T, Matsuoka S, Sato MJ, Yanagida T, Ueda M. 178.  2010. PNAS 107:12399–404 [Google Scholar]
  179. Nishikawa M, Hörning M, Ueda M, Shibata T. 179.  2014. Biophys. J. 106:723–34 [Google Scholar]
  180. Gerhardt M, Walz M, Beta C. 180.  2014. J. Cell Sci. 127:5115–25 [Google Scholar]
  181. Shibata T, Nishikawa M, Matsuoka S, Ueda M. 181.  2012. J. Cell Sci. 125:5138–50 [Google Scholar]
  182. Sasaki AT, Janetopoulos C, Lee S, Charest PG, Takeda K. 182.  et al. 2007. J. Cell Biol. 178:185–91 [Google Scholar]
  183. Xiong Y, Huang CH, Iglesias PA, Devreotes PN. 183.  2010. PNAS 107:17079–86 [Google Scholar]
  184. Hecht I, Skoge ML, Charest PG, Ben-Jacob E, Firtel RA. 184.  et al. 2011. PLOS Comput. Biol. 7:e1002044 [Google Scholar]
  185. Tang M, Wang M, Shi C, Iglesias PA, Devreotes PN, Huang CH. 185.  2014. Nat. Commun.5 [Google Scholar]
  186. Laughlin RB. 186.  2015. PNAS 112:10371–76 [Google Scholar]
/content/journals/10.1146/annurev-conmatphys-031016-025210
Loading
Intracellular Oscillations and Waves
Annual Review of Condensed Matter Physics 8, 239 (2017); https://doi.org/10.1146/annurev-conmatphys-031016-025210
/content/journals/10.1146/annurev-conmatphys-031016-025210
/content/journals/10.1146/annurev-conmatphys-031016-025210
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