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Force communication in multicellular tissues addressed by laser nanosurgery

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Abstract

Cell contractility is a prominent mechanism driving multicellular tissue development and remodeling. Forces originated by the actomyosin cytoskeleton not only act within the cell body but can also propagate many layers away from the contraction source and grant tissues the ability to organize collectively and to achieve robust remodeling through development. Tissue tension is being thoroughly investigated in model organisms and increasing evidence is revealing the major role played by the communication, dynamics and propagation of cell-to-cell physical forces in multicellular remodeling. Recently, pulsed-laser-based surgery has fostered in vivo experimental studies to investigate intracellular and supracellular forces in action. The technique offers a unique method to perturb mechanical equilibrium in a subpopulation of cells or in a single cell, while the overall tissue remains intact. In particular, improved ablation precision with short laser pulses and the combination of this technique with biophysical models now allow an in-depth understanding of the role of cellular mechanics in tissue morphogenesis. We first characterize laser ablation modes available to perform intracellular, cellular, or multi-cellular ablation via the example of the model monolayer tissue of the amnioserosa of Drosophila by relating subnanosecond laser pulse energy to ablation efficiency and the probability of cavitation bubble formation. We then review recent laser nanosurgery experiments that have been performed in cultured cells and that tackle actomyosin mechanics and provide molecular insights into force-sensing mechanisms. We finally review studies showing the central role of laser ablation in revealing the nature and orientation of forces involved in intracellular contractility and force mechanosensing in tissue development, e.g., axis elongation, branching morphogenesis, or tissue invagination. We discuss the perspectives offered by the technique in force-based cell-cell communication and mechanosensing pathways.

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References

  • Affolter M, Zeller R, Caussinus E (2009) Tissue remodeling through branching morphogenesis. Nat Rev Mol Cell Biol 10:831–842

    Article  PubMed  CAS  Google Scholar 

  • Ben-Yakar A, Byer RL (2004) Femtosecond laser ablation properties of borosilicate glass. J Appl Phys 96:5316

    Article  Google Scholar 

  • Berns MW, Aist J, Edwards J, Strahs K, Girton J, McNeill P, Rattner JB, Kitzes M, Hammer-Wilson M, Liaw LH, Siemens A, Koonce M, Peterson S, Brenner S, Burt J, Walter R, Bryant PJ, Dyk D van, Coulombe J, Cahill T, Berns GS (1981) Laser microsurgery in cell and developmental biology. Science 213:505–513

    Article  PubMed  CAS  Google Scholar 

  • Bershadsky AD, Balaban NQ, Geiger B (2003) Adhesion-dependent cell mechanosensitivity. Annu Rev Cell Dev Biol 19:677–695

    Article  PubMed  CAS  Google Scholar 

  • Besser A, Colombelli J, Stelzer EHK, Schwarz US (2011) Viscoelastic response of contractile filament bundles. Phys Rev E 83:051902

    Article  Google Scholar 

  • Blanchard GB, Murugesu S, Adams RJ, Martinez-Arias A, Gorfinkel N (2010) Cytoskeletal dynamics and supracellular organization of cell shape fluctuations during dorsal closure. Development 137:2743–2752

    Article  PubMed  CAS  Google Scholar 

  • Botvinick EL, Venugopalan V, Shah JV, Liaw LH, Berns MW (2004) Controlled ablation of microtubules using a picosecond laser. Biophys J 87:4203–4212

    Article  PubMed  CAS  Google Scholar 

  • Caussinus E, Colombelli J, Affolter M (2008) Tip cell migration controls stalk cell intercalation during Drosophila tracheal tube elongation. Curr Biol 18:1727–1734

    Article  PubMed  CAS  Google Scholar 

  • Colombelli J, Grill S, Stelzer EHK (2004) Ultraviolet diffraction limited nanosurgery of live biological tissues. Rev Sci Instrum 75:472–478

    Article  CAS  Google Scholar 

  • Colombelli J, Reynaud EG, Rietdorf J, Pepperkok R, Stelzer EHK (2005) In vivo cytoskeleton dynamics quantification in interphase cells induced by UV pulsed laser nanosurgery. Traffic 6:1093–1102

    Article  PubMed  CAS  Google Scholar 

  • Colombelli J, Reynaud EG, Stelzer EHK (2007) Investigating relaxation processes in cells and developing organisms: from cell ablation to cytoskeleton nanosurgery. Methods Cell Biol 82:267–291

    Article  PubMed  CAS  Google Scholar 

  • Colombelli J, Besser A, Reynaud EG, Girard P, Caussinus E, Haselmann U, Antony C, Pepperkok R, Small JV, Stelzer EHK (2009) Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J Cell Sci 122:1665–1679

    Article  PubMed  CAS  Google Scholar 

  • David DJV, Tishkina A, Harris TJC (2010) The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development 137:1645–1655

    Article  PubMed  CAS  Google Scholar 

  • Dembo M, Wang YL (1999) Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys J 76:2301–2316

    Article  Google Scholar 

  • Drees B, Friederich E, Fradelizi J, Louvard D, Beckerle MC, Golsteyn RM (2000) Characterization of the interaction between zyxin and members of the Ena/vasodilator-stimulated phosphoprotein family of proteins.J Biol Chem 275:22503-22511

    Article  PubMed  CAS  Google Scholar 

  • Duc Q le, Shi Q, Blonk I, Sonnenberg A, Wang N, Leckband D, Rooij J de (2010)Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner.J Cell Biol 189:1107-1115

    Article  PubMed  Google Scholar 

  • Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689

    Article  PubMed  CAS  Google Scholar 

  • Farhadifar R, Röper JC, Aigouy B, Eaton S, Jülicher F (2007)The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol 17:2095-2104

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Gonzalez R, Matos SS de, Roeper J-C, Eaton S, Zallen JA (2009) Myosin II dynamics are regulated by tension in intercalating cells. Dev Cell 17:736–743

    Article  PubMed  CAS  Google Scholar 

  • Friedl P, Wolf K (2009) Plasticity of cell migration: a multiscale tuning model. J Cell Biol 188:11–19

    Article  PubMed  Google Scholar 

  • Grill SW (2011) Growing up is stressful: biophysical laws of morphogenesis. Curr Opin Genet Dev 21:1–6

    Article  Google Scholar 

  • Grill SW, Goenczy P, Stelzer EHK, Hyman AA (2001) Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409:630–633

    Article  PubMed  CAS  Google Scholar 

  • Heidemann SR, Wirtz D (2004) Towards a regional approach to cell mechanics. Trends Cell Biol 14:160–166

    Article  PubMed  CAS  Google Scholar 

  • Heisterkamp A, Maxwell IZ, Mazur E, Underwood JM, Nickerson JA, Kumar S, Ingber DE (2005) Pulse energy dependence of subcellular dissection by femtosecond laser pulses. Opt Express 13:1390–1396

    Article  Google Scholar 

  • Hirata H, Tatsumi H, Sokabe M (2008) Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J Cell Sci 121:2795–2804

    Article  PubMed  CAS  Google Scholar 

  • Hutson MS (2003) Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300:145–149

    Article  PubMed  CAS  Google Scholar 

  • Hutson MS, Ma X (2007) Plasma and cavitation dynamics during pulsed laser microsurgery in vivo. Phys Rev Lett 99:158104

    Article  PubMed  Google Scholar 

  • Iwanaga S, Kaneko T, Fujita K, Smith N, Nakamura O, Takamatsu T, Kawata S (2006) Location-dependent photogeneration of calcium waves in HeLa cells. Cell Biochem Biophys 45:167–176

    Article  PubMed  CAS  Google Scholar 

  • Khodjakov A, Cole RW, Oakley BR, Rieder CL (2000) Centrosome-independent mitotic spindle formation in vertebrates. Curr Biol 10:59–67

    Article  PubMed  CAS  Google Scholar 

  • Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA (2000) Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149:471–490

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Maxwell IZ, Heisterkamp A, Polte TR, Lele TP, Salanga M, Mazur E, Ingber DE (2006) Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys J 90:3762–3773

    Article  PubMed  CAS  Google Scholar 

  • Lele TP, Pendse J, Kumar S, Salanga M, Karavitis J, Ingber DE (2006) Mechanical forces alter zyxin unbinding kinetics within focal adhesions of living cells. J Cell Physiol 207:187–194

    Article  PubMed  CAS  Google Scholar 

  • Li B, Trueb B (2001) Analysis of the alpha-actinin/zyxin interaction. J Biol Chem 276:33328–33335

    Article  PubMed  CAS  Google Scholar 

  • Luo Y, Xu X, Lele T, Kumar S, Ingber DE (2008) A multi-modular tensegrity model of an actin stress fiber. J Biomech 41:2379–2387

    Article  PubMed  Google Scholar 

  • Martin AC, Kaschube M, Wieschaus E (2008) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457:495–499

    Article  PubMed  Google Scholar 

  • Martin AC, Gelbart M, Fernandez-Gonzalez R, Kaschube M, Wieschaus E (2010) Integration of contractile forces during tissue invagination. J Cell Biol 198:735–749

    Article  Google Scholar 

  • Nguyen TN, Uemura A, Shih W, Soichiro Y (2010) Zyxin-mediated actin assembly is required for efficient wound closure. J Biol Chem 285:35439–35445

    Article  PubMed  CAS  Google Scholar 

  • Nicolas A, Geiger B, Safran SA (2004) Cell mechanosensitivity controls the anisotropy of focal adhesions. Proc Natl Acad Sci USA 101:12520–12525

    Article  PubMed  CAS  Google Scholar 

  • Nishimura N, Schaffer CB, Friedman B, Tsai PS, Lyden PD, Kleinfeld D (2006) Targeted insult to subsurface cortical blood vessels using ultrashort laser pulsers: three models of stroke. Nat Methods 3:99–108

    Article  PubMed  CAS  Google Scholar 

  • Oda H, Tsukita S (2001) Real time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constrictions of cell. J Cell Sci 114:493–501

    PubMed  CAS  Google Scholar 

  • Prager-Khoutorsky M, Lichtenstein A, Krishnan R, Rajendran K, Mayo A, Kam Z, Geiger B, Bershadsky A (2011) Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat Cell Biol 13:1457–1465

    Article  PubMed  CAS  Google Scholar 

  • Rauzi M, Verant P, Lecuit T, Lenne PF (2008) Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis.Nat Cell Biol 10:1401-1410

    Article  PubMed  CAS  Google Scholar 

  • Rauzi M, Lenne PF, Lecuit T (2010) Planar polarized actomyosin contractile flows control epithelial junction remodelling.Nature 468:1110–1114

    Article  PubMed  CAS  Google Scholar 

  • Rio A del, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP (2009) Stretching single talin rod molecules activates vinculin binding. Science 323:638–641

    Article  PubMed  Google Scholar 

  • Riveline D, Zamior E, Balaban NQ, Schwartz US, Ishizaki T, Narumiya S, Kam Z, Geiger B, Bershadsky AD (2001) Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol 153:1175–1185

    Article  PubMed  CAS  Google Scholar 

  • Royou A, Sullivan W, Karess R (2002) Cortical recruitment of non muscle myosin II in early syncytial Drosophila embryos: its role in nuclear axial expansion and its regulation by Cdc2 activity. J Cell Biol 158:127

    Article  PubMed  CAS  Google Scholar 

  • Sawyer JM, Harrell JR, Shemer G, Sullivan-Brown J, Roh-Johnson M, Goldstein B (2009) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 341:5–19

    Article  PubMed  Google Scholar 

  • Smith MA, Blankman E, Gardel ML, Luettjohann L, Waterman CM, Beckerle MC (2010) A zyxin-mediated mechanism for actin stress fiber maintenance and repair. Dev Cell 19:365–376

    Article  PubMed  CAS  Google Scholar 

  • Solon J, Levental I, Sengupta K, Georges PC, Janmey PA (2006) Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 93:4453–4461

    Article  Google Scholar 

  • Solon J, Kaya-Copur A, Colombelli J, Brunner D (2009) Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137:1331–1342

    Article  PubMed  Google Scholar 

  • Strahs KR, Berns MW (1979) Laser microirradiation of stress fibers and intermediate filaments in non-muscle cells from cultured rat heart. Exp Cell Res 119:31–45

    Article  PubMed  CAS  Google Scholar 

  • Supatto W, Débarre D, Moulia B, Brouzés E, Martin J-L, Farge E, Beaurepaire E (2005) In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses. Proc Natl Acad Sci USA 102:1047–1052

    Article  PubMed  CAS  Google Scholar 

  • Taengemo C, Ronchi P, Colombelli J, Haselmann U, Simpson JC, Antony C, Staler EHK, Pepperkok R, Reynaud EG (2009) A novel laser nanosurgery approach supports de novo Golgi biogenesis in mammalian cells. J Cell Sci 124:978–987

    Article  Google Scholar 

  • Tagushi K, Ishiushi T, Takeichi M (2011) Mechanosensitive EPLIN-dependent remodeling of adherens junctions regulates epithelial reshaping. J Cell Biol 194:643–656

    Article  Google Scholar 

  • Tamada M, Perez TD, Nelson JW, Sheetz MP (2007) Two distinct modes of myosin assembly and dynamics during epithelial wound closure. J Cell Biol 176:27–33

    Article  PubMed  CAS  Google Scholar 

  • Thery M, Racina V, Pepin A, Piel M, Chen Y, Sibarita J-B, Bornens M (2005) The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol 7:947–953

    Article  PubMed  CAS  Google Scholar 

  • Trepat X, Wasserman MR, Angelini TE, Millet E, Weitz DA, Butler JP, Fredberg JJ (2009) Physical forces during collective cell migration. Nat Phys 5:426–430

    Article  CAS  Google Scholar 

  • Vogel A, Venugopalan V (2003) Mechanisms of pulsed laser ablation of biological tissues. Chem Rev 103:577–644

    Article  PubMed  CAS  Google Scholar 

  • Vogel A, Noack J, Huttman G, Paltauf G (2005) Mechanisms of femtosecond laser nanosurgery of cells and tissues. Appl Phys B 81:1015–1047

    Article  CAS  Google Scholar 

  • Vogel A, Linz N, Freidank S, Noack J, Paltauf G (2008a) Femtosecond and nanosecond laser-induced nanoeffects for cell surgery and modification of glass. Proceedings of Conference on Quantum Electronics and Laser Science, 2008, http://www.opticsinfobase.org/abstract.cfm?URI=CLEO-2008-CMHH1

  • Vogel A, Linz N, Freidank S, Paltauf G (2008b) Femtosecond-laser-induced nanocavitation in water: implications for optical breakdown threshold and cell surgery. Phys Rev Lett 100:038102

    Article  PubMed  Google Scholar 

  • Wood W, Jacinto A, Grose R, Woolner S, Gale J, Wilson C, Martin P (2002) Wound healing recapitulates morphogenesis in Drosophila embryos. Nat Cell Biol 4:907–912

    Article  PubMed  CAS  Google Scholar 

  • Yonemura S, Wada Y, Watanabe T, Nagafushi A, Shibata M (2010) α-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 12:533–542

    Article  PubMed  CAS  Google Scholar 

  • Zaidel-Bar R, Milo R, Kam Z, Geiger B (2006) A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J Cell Sci 120:137–148

    Article  PubMed  Google Scholar 

  • Zaidel-Bar R, Itzkovitz S, Ma’ayan A, Iyengar R, Geiger B (2007) Functional atlas of the integrin adhesome. Nat Cell Biol 9:858–867

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute for Research in Biomedicine (IRB Barcelona), c/ Baldiri Reixac 10-12, 08028, Barcelona, Spain

    Julien Colombelli

  2. Center for Genomic Regulation (CRG), c/ Dr. Aiguader 88, 08003, Barcelona, Spain

    Jérôme Solon

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  1. Julien Colombelli
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  2. Jérôme Solon
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Correspondence to Julien Colombelli.

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Colombelli, J., Solon, J. Force communication in multicellular tissues addressed by laser nanosurgery. Cell Tissue Res 352, 133–147 (2013). https://doi.org/10.1007/s00441-012-1445-1

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