Skip to main content
SpringerLink
Log in

Direct investigation of cell contraction signal networks by light-based perturbation methods

  • Review
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Cell contraction plays an important role in many physiological and pathophysiological processes. This includes functions in skeletal, heart, and smooth muscle cells, which lead to highly coordinated contractions of multicellular assemblies, and functions in non-muscle cells, which are often highly localized in subcellular regions and transient in time. While the regulatory processes that control cell contraction in muscle cells are well understood, much less is known about cell contraction in non-muscle cells. In this review, we focus on the mechanisms that control cell contraction in space and time in non-muscle cells, and how they can be investigated by light-based methods. The review particularly focusses on signal networks and cytoskeletal components that together control subcellular contraction patterns to perform functions on the level of cells and tissues, such as directional migration and multicellular rearrangements during development. Key features of light-based methods that enable highly local and fast perturbations are highlighted, and how experimental strategies can capitalize on these features to uncover causal relationships in the complex signal networks that control cell contraction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

This declaration is not applicable.

References

  1. Acharya BR, Wu SK, Lieu ZZ, Parton RG, Grill SW, Bershadsky AD, Gomez GA, Yap AS (2017) Mammalian diaphanous 1 mediates a pathway for e-cadherin to stabilize epithelial barriers through junctional contractility. Cell Rep 18:2854–2867. https://doi.org/10.1016/j.celrep.2017.02.078

    Article  CAS  PubMed  Google Scholar 

  2. Alvarado J, Sheinman M, Sharma A, Mackintosh FC, Koenderink GH (2013) Molecular motors robustly drive active gels to a critically connected state. Nat Phys 9(9):591–597. https://doi.org/10.1038/nphys2715

    Article  CAS  Google Scholar 

  3. Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y, Kaibuchi K (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem 271:20246–20249. https://doi.org/10.1074/jbc.271.34.20246

    Article  CAS  PubMed  Google Scholar 

  4. Arber S, Barbayannis FA, Hanser H, Schnelder C, Stanyon CA, Bernards O, Caroni P (1998) Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393(6687):805–809. https://doi.org/10.1038/31729

    Article  CAS  PubMed  Google Scholar 

  5. Arnold TR, Stephenson RE, Miller AL (2017) Rho GTPases and actomyosin: partners in regulating epithelial cell-cell junction structure and function. Exp Cell Res 358:20–30. https://doi.org/10.1016/J.YEXCR.2017.03.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ballister ER, Aonbangkhen C, Mayo AM, Lampson MA, Chenoweth DM (2014) Localized light-induced protein dimerization in living cells using a photocaged dimerizer. Nat Commun 5:5475. https://doi.org/10.1038/ncomms6475

    Article  PubMed  Google Scholar 

  7. Beach JR, Bruun KS, Shao L, Li D, Swider Z, Remmert K, Zhang Y, Conti MA, Adelstein RS, Rusan NM, Betzig E, Hammer JA (2017) Actin dynamics and competition for myosin monomer govern the sequential amplification of myosin filaments. Nat Cell Biol 19:85–93. https://doi.org/10.1038/NCB3463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bement WM, Leda M, Moe AM, Kita AM, Larson ME, Golding AE, Pfeuti C, Su KC, Miller AL, Goryachev AB, von Dassow G (2015) Activator-inhibitor coupling between Rho signalling and actin assembly makes the cell cortex an excitable medium. Nat Cell Biol 17:1471–1483. https://doi.org/10.1038/ncb3251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Berlew EE, Kuznetsov IA, Yamada K, Bugaj LJ, Boerckel JD, Chow BY (2021) Single-component optogenetic tools for inducible RhoA GTPase signaling. Adv Biol 5:2100810. https://doi.org/10.1002/ADBI.202100810

    Article  CAS  Google Scholar 

  10. Blanchard GB, Murugesu S, Adams RJ, Martinez-Arias A, Gorfinkiel N (2010) Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 137:2743–2752. https://doi.org/10.1242/dev.045872

    Article  CAS  PubMed  Google Scholar 

  11. Blaser H, Reichman-Fried M, Castanon I, Dumstrei K, Marlow FLL, Kawakami K, Solnica-Krezel L, Heisenberg CP, Raz E (2006) Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev Cell 11:613–627. https://doi.org/10.1016/J.DEVCEL.2006.09.023

    Article  CAS  PubMed  Google Scholar 

  12. Bray D, Heath J, Moss D (1986) The membrane-associated ‘cortex’ of animal cells: its structure and mechanical properties. J Cell Sci 1986:71–88. https://doi.org/10.1242/JCS.1986.SUPPLEMENT_4.5

    Article  Google Scholar 

  13. Burnette DT, Manley S, Sengupta P, Sougrat R, Davidson MW, Kachar B, Lippincott-Schwartz J (2011) A role for actin arcs in the leading-edge advance of migrating cells. Nat Cell Biol 13(4):371–382. https://doi.org/10.1038/ncb2205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Carramusa L, Ballestrem C, Zilberman Y, Bershadsky AD (2007) Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherin-mediated cell-cell junctions. J Cell Sci 120:3870–3882. https://doi.org/10.1242/JCS.014365

    Article  CAS  PubMed  Google Scholar 

  15. Castella LF, Buscemi L, Godbout C, Meister JJ, Hinz B (2010) A new lock-step mechanism of matrix remodelling based on subcellular contractile events. J Cell Sci 123:1751–1760. https://doi.org/10.1242/JCS.066795

    Article  CAS  PubMed  Google Scholar 

  16. Chen M, Pan H, Sun L, Shi P, Zhang Y, Li L, Huang Y, Chen J, Jiang P, Fang X, Wu C, Chen Z (2020) Structure and regulation of human epithelial cell transforming 2 protein. Proc Natl Acad Sci U S A 117:1027–1035. https://doi.org/10.1073/PNAS.1913054117

    Article  CAS  PubMed  Google Scholar 

  17. Chen X, Venkatachalapathy M, Kamps D, Weigel S, Kumar R, Orlich M, Garrecht R, Hirtz M, Niemeyer CM, Wu YW, Dehmelt L (2017) “Molecular activity painting”: switch-like, light-controlled perturbations inside living cells. Angew Chem Int Ed Engl 56:5916–5920. https://doi.org/10.1002/anie.201611432

    Article  CAS  PubMed  Google Scholar 

  18. Chhabra ES, Higgs HN (2007) The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9(10):1110–1121. https://doi.org/10.1038/ncb1007-1110

    Article  CAS  PubMed  Google Scholar 

  19. Dasbiswas K, Hu S, Schnorrer F, Safran SA, Bershadsky AD (2018) Ordering of myosin II filaments driven by mechanical forces: experiments and theory. Phil Trans R Soc B Biol Sci 373. https://doi.org/10.1098/RSTB.2017.0114

  20. David DJ, Tishkina A, Harris TJ (2010) The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development 137:1645–1655. https://doi.org/10.1242/dev.044107

    Article  CAS  PubMed  Google Scholar 

  21. Desai R, Sarpal R, Ishiyama N, Pellikka M, Ikura M, Tepass U (2013) Monomeric α-catenin links cadherin to the actin cytoskeleton. Nat Cell Biol 15(3):261–273. https://doi.org/10.1038/ncb2685

    Article  CAS  PubMed  Google Scholar 

  22. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, Zanconato F, Le Digabel J, Forcato M, Bicciato S, Elvassore N, Piccolo S (2011) Role of YAP/TAZ in mechanotransduction. Nature 474(7350):179–183. https://doi.org/10.1038/nature10137

    Article  CAS  PubMed  Google Scholar 

  23. Fehon RG, McClatchey AI, Bretscher A (2010) Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol 11(4):276–287. https://doi.org/10.1038/nrm2866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Fujiwara K, Pollard TD (1976) Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow, and mitotic spindle of human cells. J Cell Biol 71:848–875. https://doi.org/10.1083/JCB.71.3.848

    Article  CAS  PubMed  Google Scholar 

  25. Furst DO, Osborn M, Nave R, Weber K (1988) The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J Cell Biol 106:1563–1572. https://doi.org/10.1083/JCB.106.5.1563

    Article  CAS  PubMed  Google Scholar 

  26. Garcia-Mata R, Boulter E, Burridge K (2011) The “invisible hand”: regulation of RHO GTPases by RHOGDIs. Nat Rev Mol Cell Biol 12:493–504. https://doi.org/10.1038/nrm3153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Glaven JA, Whitehead IP, Nomanbhoy T, Kay R, Cerione RA (1996) Lfc and Lsc oncoproteins represent two new guanine nucleotide exchange factors for the Rho GTP-binding protein. J Biol Chem 271:27374–27381. https://doi.org/10.1074/JBC.271.44.27374

    Article  CAS  PubMed  Google Scholar 

  28. Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80:853–924. https://doi.org/10.1152/PHYSREV.2000.80.2.853/ASSET/IMAGES/LARGE/9J0200077008.JPEG

    Article  CAS  PubMed  Google Scholar 

  29. Goryachev AB, Leda M, Miller AL, von Dassow G, Bement WM (2016) How to make a static cytokinetic furrow out of traveling excitable waves. Small GTPases 7:65–70. https://doi.org/10.1080/21541248.2016.1168505

    Article  PubMed  PubMed Central  Google Scholar 

  30. Graessl M, Koch J, Calderon A, Kamps D, Banerjee S, Mazel T, Schulze N, Jungkurth JK, Patwardhan R, Solouk D, Hampe N, Hoffmann B, Dehmelt L, Nalbant P (2017) An excitable Rho GTPase signaling network generates dynamic subcellular contraction patterns. J Cell Biol 216:4271–4285. https://doi.org/10.1083/jcb.201706052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Guilluy C, Garcia-Mata R, Burridge K (2011) Rho protein crosstalk: another social network? Trends Cell Biol 21:718–726. https://doi.org/10.1016/j.tcb.2011.08.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Guo H, Swan M, He B (2022) Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination. Elife 11. https://doi.org/10.7554/ELIFE.69082

  33. Harburger DS, Calderwood DA (2009) Integrin signalling at a glance. J Cell Sci 122:159–163. https://doi.org/10.1242/JCS.018093

    Article  CAS  PubMed  Google Scholar 

  34. Hashimoto H, Munro E (2019) Differential expression of a classic cadherin directs tissue-level contractile asymmetry during neural tube closure. Dev Cell 51:158–172.e4. https://doi.org/10.1016/J.DEVCEL.2019.10.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hirokawa N, Keller TCS, Chasan R, Mooseker MS (1983) Mechanism of brush border contractility studied by the quick-freeze, deep-etch method. J Cell Biol 96:1325–1336. https://doi.org/10.1083/Jcb.96.5.1325

  36. Hirokawa N, Tilnfy LG, Fujiwara K, Heuser JE (1982) Organization of actin, myosin, and intermediate the brush border of intestinal epithelial cells filaments in the brush border of intestinal epithelial cells. J Cell Biol 94(2):425–443. https://doi.org/10.1083/jcb.94.2.425

  37. Hodge RG, Ridley AJ (2016) Regulating Rho GTPases and their regulators. Nat Rev Mol Cell Biol 17:496–510. https://doi.org/10.1038/nrm.2016.67

    Article  CAS  PubMed  Google Scholar 

  38. Hotulainen P, Lappalainen P (2006) Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 173:383–394. https://doi.org/10.1083/JCB.200511093/VIDEO-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Huxley HE (2004) Fifty years of muscle and the sliding filament hypothesis. Eur J Biochem 271:1403–1415. https://doi.org/10.1111/J.1432-1033.2004.04044.X

    Article  CAS  PubMed  Google Scholar 

  40. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687. https://doi.org/10.1016/S0092-8674(02)00971-6

    Article  CAS  PubMed  Google Scholar 

  41. Izquierdo E, Quinkler T, De Renzis S (2018) Guided morphogenesis through optogenetic activation of Rho signalling during early Drosophila embryogenesis. Nat Commun 9(1):1–13. https://doi.org/10.1038/s41467-018-04754-z

    Article  CAS  Google Scholar 

  42. Kamps D, Dehmelt L (2017) Deblurring signal network dynamics. ACS Chem Biol 12:2231–2239. https://doi.org/10.1021/ACSCHEMBIO.7B00451

    Article  CAS  PubMed  Google Scholar 

  43. Kamps D, Koch J, Juma VO, Campillo-Funollet E, Graessl M, Banerjee S, Mazel T, Chen X, Wu YW, Portet S, Madzvamuse A, Nalbant P, Dehmelt L (2020) Optogenetic tuning reveals Rho amplification-dependent dynamics of a cell contraction signal network. Cell Rep 33:108467. https://doi.org/10.1016/j.celrep.2020.108467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW, Hess HF, Waterman CM (2010) Nanoscale architecture of integrin-based cell adhesions. Nature 468(7323):580–584. https://doi.org/10.1038/nature09621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Kennedy MJ, Hughes RM, Peteya LA, Schwartz JW, Ehlers MD, Tucker CL (2010) Rapid blue-light-mediated induction of protein interactions in living cells. Nat Methods 7:973–975. https://doi.org/10.1038/nmeth.1524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Kimura K, Fukata Y, Matsuoka Y, Bennett V, Matsuura Y, Okawa K, Iwamatsu A, Kaibuchi K (1998) Regulation of the association of adducin with actin filaments by Rho- associated kinase (Rho-kinase) and myosin phosphatase. J Biol Chem 273:5542–5548. https://doi.org/10.1074/jbc.273.10.5542

    Article  CAS  PubMed  Google Scholar 

  47. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A (1979) Kaibuchi K (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273:245–248. https://doi.org/10.1126/SCIENCE.273.5272.245

    Article  Google Scholar 

  48. Klughammer N, Bischof J, Schnellbächer ND, Callegari A, Lénárt P, Schwarz US (2018) Cytoplasmic flows in starfish oocytes are fully determined by cortical contractions. PLoS Comput Biol 14:e1006588. https://doi.org/10.1371/JOURNAL.PCBI.1006588

    Article  PubMed  PubMed Central  Google Scholar 

  49. Koenderink GH, Paluch EK (2018) Architecture shapes contractility in actomyosin networks. Curr Opin Cell Biol 50:79–85. https://doi.org/10.1016/J.CEB.2018.01.015

    Article  CAS  PubMed  Google Scholar 

  50. Kolodney MS, Thimgan MS, Honda HM, Tsai G, Yee HF (1999) Ca2+-independent myosin II phosphorylation and contraction in chicken embryo fibroblasts. J Physiol 515:87–92. https://doi.org/10.1111/J.1469-7793.1999.087AD.X

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kowalczyk M, Kamps D, Wu Y, Dehmelt L, Nalbant P (2021) Monitoring the response of multiple signal network components to acute chemo-optogenetic perturbations in living cells. Chembiochem e202100582. https://doi.org/10.1002/cbic.202100582

  52. Le Bras S, Le Borgne R (2014) Epithelial cell division - multiplying without losing touch. J Cell Sci 127:5127–5137. https://doi.org/10.1242/JCS.151472/259089/AM/EPITHELIAL-CELL-DIVISION-MULTIPLYING-WITHOUT

    Article  PubMed  Google Scholar 

  53. Lee CS, Choi CK, Shin EY, Schwartz MA, Kim EG (2010) Myosin II directly binds and inhibits Dbl family guanine nucleotide exchange factors: a possible link to Rho family GTPases. J Cell Biol 190:663–674. https://doi.org/10.1083/jcb.201003057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Lee S, Kumar S (2020) Cofilin is required for polarization of tension in stress fiber networks during migration. J Cell Sci 133. https://doi.org/10.1242/JCS.243873/VIDEO-10

  55. Lee S, Park H, Kyung T, Kim NY, Kim S, Kim J, Do HW (2014) Reversible protein inactivation by optogenetic trapping in cells. Nat Methods 11:633–636. https://doi.org/10.1038/NMETH.2940

    Article  CAS  PubMed  Google Scholar 

  56. Legate KR, Wickström SA, Fässler R (2009) Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 23:397–418. https://doi.org/10.1101/GAD.1758709

    Article  CAS  PubMed  Google Scholar 

  57. Lehtimaki J, Hakala M, Lappalainen P (2017) Actin filament structures in migrating cells. Handb Exp Pharmacol 235:123–152. https://doi.org/10.1007/164_2016_28/FIGURES/2

    Article  CAS  PubMed  Google Scholar 

  58. Lehtimäki JI, Rajakylä EK, Tojkander S, Lappalainen P (2021) Generation of stress fibers through myosin-driven reorganization of the actin cortex. Elife 10:1–43. https://doi.org/10.7554/ELIFE.60710

    Article  Google Scholar 

  59. Leung DW, Otomo C, Chory J, Rosen MK (2008) Genetically encoded photoswitching of actin assembly through the Cdc42-WASP-Arp2/3 complex pathway. Proc Natl Acad Sci U S A 105:12797–12802. https://doi.org/10.1073/PNAS.0801232105/SUPPL_FILE/0801232105SI.PDF

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Leung T, Chen X-Q, Manser E, Lim L (2023) The p160 RhoA-binding kinase ROKα is a member of a kinase family and is involved in the reorganization of the cytoskeleton 16:5313–5327. https://doi.org/10.1128/MCB.16.10.5313

  61. Levskaya A, Weiner OD, Lim WA, Voigt CA (2009) Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461:997–1001. https://doi.org/10.1038/nature08446

  62. Litschko C, Brühmann S, Csiszár A, Stephan T, Dimchev V, Damiano-Guercio J, Junemann A, Körber S, Winterhoff M, Nordholz B, Ramalingam N, Peckham M, Rottner K, Merkel R, Faix J (2019) Functional integrity of the contractile actin cortex is safeguarded by multiple Diaphanous-related formins. Proc Natl Acad Sci U S A 116:3594–3603. https://doi.org/10.1073/PNAS.1821638116/SUPPL_FILE/PNAS.1821638116.SM10.AVI

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Luo W, Yu C-h, Lieu ZZ, Allard J, Mogilner A, Sheetz MP, Bershadsky AD (2013) Analysis of the local organization and dynamics of cellular actin networks. J Cell Biol 202:1057–1073. https://doi.org/10.1083/JCB.201210123/VIDEO-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Maddox AS, Burridge K (2003) RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J Cell Biol 160:255–265. https://doi.org/10.1083/jcb.200207130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Maitre JL, Niwayama R, Turlier H, Nedelec F, Hiiragi T (2015) Pulsatile cell-autonomous contractility drives compaction in the mouse embryo. Nat Cell Biol 17:849–855. https://doi.org/10.1038/ncb3185

    Article  CAS  PubMed  Google Scholar 

  66. Martin AC, Gelbart M, Fernandez-Gonzalez R, Kaschube M, Wieschaus EF (2010) Integration of contractile forces during tissue invagination. J Cell Biol 188:735–749. https://doi.org/10.1083/jcb.200910099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457:495–499. https://doi.org/10.1038/nature07522

    Article  CAS  PubMed  Google Scholar 

  68. Matsui T, Amano M, Yamamoto T, Chihara K, Nakafuku M, Ito M, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K (1996) Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. EMBO J 15:2208–2216. https://doi.org/10.1002/J.1460-2075.1996.TB00574.X

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Matsui T, Maeda M, Doi Y, Yonemura S, Amano M, Kaibuchi K, Tsukita S, Tsukita S (1998) Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J Cell Biol 140:647–657. https://doi.org/10.1083/JCB.140.3.647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. McGregor A, Blanchard AD, Rowe AJ, Critchley DR (1994) Identification of the vinculin-binding site in the cytoskeletal protein α-actinin. Biochem J 301:225–233. https://doi.org/10.1042/BJ3010225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Medina F, Carter AM, Dada O, Gutowski S, Hadas J, Chen Z, Sternweis PC (2013) Activated RhoA is a positive feedback regulator of the Lbc family of Rho guanine nucleotide exchange factor proteins. J Biol Chem 288:11325–11333. https://doi.org/10.1074/jbc.M113.450056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Meinhardt H (2004) Out-of-phase oscillations and traveling waves with unusual properties: the use of three-component systems in biology. Physica D 199:264–277

    Article  Google Scholar 

  73. Méry A, Ruppel A, Revilloud J, Balland M, Cappello G, Boudou T (2023) Light-driven biological actuators to probe the rheology of 3D microtissues. Nat Commun 14(1):1–12. https://doi.org/10.1038/s41467-023-36371-w

    Article  CAS  Google Scholar 

  74. Michaud A, Leda M, Swider ZT, Kim S, He J, Landino J, Valley JR, Huisken J, Goryachev AB, Von Dassow G, Bement WM (2022) A versatile cortical pattern-forming circuit based on Rho, F-actin, Ect2, and RGA-3/4. J Cell Biol 221. https://doi.org/10.1083/JCB.202203017

  75. Michaud A, Swider ZT, Landino J, Leda M, Miller AL, von Dassow G, Goryachev AB, Bement WM (2021) Cortical excitability and cell division. Curr Biol 31:R553–R559. https://doi.org/10.1016/j.cub.2021.02.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Munjal A, Philippe JM, Munro E, Lecuit T (2015) A self-organized biomechanical network drives shape changes during tissue morphogenesis. Nature 524:351–355. https://doi.org/10.1038/nature14603

    Article  CAS  PubMed  Google Scholar 

  77. Nalbant P, Dehmelt L (2018) Exploratory cell dynamics: a sense of touch for cells? Biol Chem 399:809–819. https://doi.org/10.1515/hsz-2017-0341

    Article  CAS  PubMed  Google Scholar 

  78. Nishikawa M, Naganathan SR, Julicher F, Grill SW (2017) Controlling contractile instabilities in the actomyosin cortex. Elife 6. https://doi.org/10.7554/eLife.19595

  79. Nobes CD, Hall A (1995) Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53–62

    Article  CAS  PubMed  Google Scholar 

  80. Oda H, Tsukita S (2001) Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells. J Cell Sci 114:493–501. https://doi.org/10.1242/JCS.114.3.493

    Article  CAS  PubMed  Google Scholar 

  81. Ohashi K, Nagata K, Maekawa M, Ishizaki T, Narumiya S, Mizuno K (2000) Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J Biol Chem 275:3577–3582. https://doi.org/10.1074/jbc.275.5.3577

    Article  CAS  PubMed  Google Scholar 

  82. Pollard TD, O’Shaughnessy B (2019) Molecular mechanism of cytokinesis. https://doi.org/10.1146/annurev-biochem-062917-012530 88:661–689. https://doi.org/10.1146/ANNUREV-BIOCHEM-062917-012530

  83. Qin X, Hannezo E, Mangeat T, Liu C, Majumder P, Liu J, Choesmel-Cadamuro V, McDonald JA, Liu Y, Yi B, Wang X (2018) A biochemical network controlling basal myosin oscillation. Nat Commun 9(1):1–15. https://doi.org/10.1038/s41467-018-03574-5

    Article  CAS  Google Scholar 

  84. Ridley AJ (2011) Life at the leading edge. Cell 145:1012–1022. https://doi.org/10.1016/J.CELL.2011.06.010

    Article  CAS  PubMed  Google Scholar 

  85. Ridley AJ, Hall A (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389–399. https://doi.org/10.1016/0092-8674(92)90163-7

    Article  CAS  PubMed  Google Scholar 

  86. Rolo A, Skoglund P, Keller R (2009) Morphogenetic movements driving neural tube closure in Xenopus require myosin IIB. Dev Biol 327:327–338. https://doi.org/10.1016/J.YDBIO.2008.12.009

    Article  CAS  PubMed  Google Scholar 

  87. Sahai E, Marshall CJ (2003) Differing modes for tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 5:711–719. https://doi.org/10.1038/NCB1019

    Article  CAS  PubMed  Google Scholar 

  88. Sampayo RG, Sakamoto M, Wang M, Kumar S, Schaffer DV (2023) Mechanosensitive stem cell fate choice is instructed by dynamic fluctuations in activation of Rho GTPases. Proc Natl Acad Sci 120:e2219854120. https://doi.org/10.1073/PNAS.2219854120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Sawyer JM, Harrell JR, Shemer G, Sullivan-Brown J, Roh-Johnson M, Goldstein B (2010) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 341:5–19. https://doi.org/10.1016/J.YDBIO.2009.09.009

    Article  CAS  PubMed  Google Scholar 

  90. Schroeder TE (1973) Actin in dividing cells: contractile ring filaments bind heavy meromyosin. Proc Natl Acad Sci 70:1688–1692. https://doi.org/10.1073/PNAS.70.6.1688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Schulze N, Graessl M, Blancke Soares A, Geyer M, Dehmelt L, Nalbant P (2014) FHOD1 regulates stress fiber organization by controlling the dynamics of transverse arcs and dorsal fibers. J Cell Sci 127:1379–1393. https://doi.org/10.1242/jcs.134627

    Article  CAS  PubMed  Google Scholar 

  92. Sluysmans S, Vasileva E, Spadaro D, Shah J, Rouaud F, Citi S (2017) The role of apical cell–cell junctions and associated cytoskeleton in mechanotransduction. Biol Cell 109:139–161. https://doi.org/10.1111/BOC.201600075

    Article  PubMed  Google Scholar 

  93. Smutny M, Cox HL, Leerberg JM, Kovacs EM, Conti MA, Ferguson C, Hamilton NA, Parton RG, Adelstein RS, Yap AS (2010) Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat Cell Biol 12(7):696–702. https://doi.org/10.1038/ncb2072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Strickland D, Lin Y, Wagner E, Hope CM, Zayner J, Antoniou C, Sosnick TR, Weiss EL, Glotzer M (2012) TULIPs: tunable, light-controlled interacting protein tags for cell biology. Nat Methods 9:379–384. https://doi.org/10.1038/nmeth.1904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Sumi A, Hayes P, D’Angelo A, Colombelli J, Salbreux G, Dierkes K, Solon J (2018) Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling. Dev Cell 47:453-463.e3. https://doi.org/10.1016/j.devcel.2018.10.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Svitkina TM (2020) Actin cell cortex: structure and molecular organization. Trends Cell Biol 30:556–565. https://doi.org/10.1016/j.tcb.2020.03.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Svitkina TM, Verkhovsky AB, McQuade KM, Borisy GG (1997) Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J Cell Biol 139:397–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Sweeney HL, Hammers DW (2018) Muscle contraction. Cold Spring Harb Perspect Biol 10. https://doi.org/10.1101/CSHPERSPECT.A023200

  99. Swider ZT, Michaud A, Leda M, Landino J, Goryachev AB, Bement WM (2022) Cell cycle and developmental control of cortical excitability in Xenopus laevis. Mol Biol Cell 33. https://doi.org/10.1091/MBC.E22-01-0025

  100. Takeya R, Taniguchi K, Narumiya S, Sumimoto H (2008) The mammalian formin FHOD1 is activated through phosphorylation by ROCK and mediates thrombin-induced stress fibre formation in endothelial cells. EMBO J 27:618–628. https://doi.org/10.1038/EMBOJ.2008.7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Tatsumoto T, Xie X, Blumenthal R, Okamoto I, Miki T (1999) Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J Cell Biol 147:921–927. https://doi.org/10.1083/JCB.147.5.921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Taubenberger AV, Baum B, Matthews HK (2020) The mechanics of mitotic cell rounding. Front Cell Dev Biol 8:687. https://doi.org/10.3389/FCELL.2020.00687/BIBTEX

    Article  PubMed  PubMed Central  Google Scholar 

  103. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial–mesenchymal transitions. Nat Rev Mol Cell Biol 7(2):131–142. https://doi.org/10.1038/nrm1835

    Article  CAS  PubMed  Google Scholar 

  104. Tojkander S, Gateva G, Lappalainen P (2012) Actin stress fibers–assembly, dynamics and biological roles. J Cell Sci 125:1855–1864. https://doi.org/10.1242/jcs.098087

    Article  CAS  PubMed  Google Scholar 

  105. Turing AM (1952) The chemical basis of morphogenesis. Philos Trans R Soc Lond B Biol Sci 237:37–72

    Article  Google Scholar 

  106. Tyson JJ, Chen KC, Novak B (2003) Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr Opin Cell Biol 15:221–231

    Article  CAS  PubMed  Google Scholar 

  107. Valencia FR, Sandoval E, Du J, Iu E, Liu J, Plotnikov SV (2021) Force-dependent activation of actin elongation factor mDia1 protects the cytoskeleton from mechanical damage and promotes stress fiber repair. Dev Cell 56:3288-3302.e5. https://doi.org/10.1016/j.devcel.2021.11.004

    Article  CAS  PubMed  Google Scholar 

  108. Valon L, Marín-Llauradó A, Wyatt T, Charras G, Trepat X (2017) Optogenetic control of cellular forces and mechanotransduction. Nat Commun 8. https://doi.org/10.1038/NCOMMS14396

  109. van den Boom F, Dussmann H, Uhlenbrock K, Abouhamed M, Bahler M (2007) The myosin IXb motor activity targets the myosin IXb RhoGAP domain as cargo to sites of actin polymerization. Mol Biol Cell 18:1507–1518. https://doi.org/10.1091/mbc.E06-08-0771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10:778–790. https://doi.org/10.1038/nrm2786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Wang H, Vilela M, Winkler A, Tarnawski M, Schlichting I, Yumerefendi H, Kuhlman B, Liu R, Danuser G, Hahn KM (2016) LOVTRAP: an optogenetic system for photoinduced protein dissociation. Nat Methods 13:755–758. https://doi.org/10.1038/nmeth.3926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Wang Z, Raunser S (2023) Structural biochemistry of muscle contraction. Annu Rev Biochem 92. https://doi.org/10.1146/ANNUREV-BIOCHEM-052521-042909

  113. Watanabe N, Kato T, Fujita A, Ishizaki T, Narumiya S (1999) Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1:136–143. https://doi.org/10.1038/11056

    Article  CAS  PubMed  Google Scholar 

  114. Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S (1997) p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 16:3044–3056. https://doi.org/10.1093/EMBOJ/16.11.3044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Weiss A, Leinwand LA (2003) The mammalian myosin heavy chain gene family. https://doi.org/10.1146/annurev.cellbio121417 12:417–439. https://doi.org/10.1146/ANNUREV.CELLBIO.12.1.417

  116. Weng M, Wieschaus E (2016) Myosin-dependent remodeling of adherens junctions protects junctions from Snail-dependent disassembly. J Cell Biol 212:219–229. https://doi.org/10.1083/JCB.201508056/VIDEO-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Wennerberg K, Rossman KL, Der CJ (2005) The Ras superfamily at a glance. J Cell Sci 118:843–846. https://doi.org/10.1242/JCS.01660

    Article  CAS  PubMed  Google Scholar 

  118. Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I, Kuhlman B, Hahn KM (2009) A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461:104–108. nature08241 [pii] https://doi.org/10.1038/nature08241

  119. Yamamoto K, Miura H, Ishida M, Mii Y, Kinoshita N, Takada S, Ueno N, Sawai S, Kondo Y, Aoki K (2021) Optogenetic relaxation of actomyosin contractility uncovers mechanistic roles of cortical tension during cytokinesis. Nat Commun 12(1):1–13. https://doi.org/10.1038/s41467-021-27458-3

  120. Zhou XX, Chung HK, Lam AJ (1979) Lin MZ (2012) Optical control of protein activity by fluorescent protein domains. Science 338:810–814. https://doi.org/10.1126/science.1226854

    Article  CAS  Google Scholar 

Download references

Funding

This work was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) Priority Program SPP 1926 under the grant number NA 413/4–1 to P. N. and J. W., and the DFG Principal Investigator grant DE 823/10–1 to L. D.

Author information

Authors and Affiliations

  1. Department of Molecular Cell Biology, Center of Medical Biotechnology, University of Duisburg-Essen, Room T03 R01 D33, Universitätsstrasse 2, 45141, Essen, Germany

    Perihan Nalbant & Jessica Wagner

  2. Department of Systemic Cell Biology, Fakultät für Chemie und Chemische Biologie, Max Planck Institute of Molecular Physiology, and Dortmund University of Technology, Room CP-02-157, Otto-Hahn-Str. 4a, 44227, Dortmund, Germany

    Leif Dehmelt

Authors
  1. Perihan Nalbant
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jessica Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leif Dehmelt
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

P. N. and L. D. wrote the main manuscript text. All authors prepared the figures. All authors reviewed the manuscript.

Corresponding authors

Correspondence to Perihan Nalbant or Leif Dehmelt.

Ethics declarations

Ethics approval

This declaration is not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the special issue on Next-generation optogenetics in Pflügers Archiv—European Journal of Physiology.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nalbant, P., Wagner, J. & Dehmelt, L. Direct investigation of cell contraction signal networks by light-based perturbation methods. Pflugers Arch - Eur J Physiol 475, 1439–1452 (2023). https://doi.org/10.1007/s00424-023-02864-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-023-02864-2

Keywords

Search

Navigation