Mechanical Tension Drives Cell Membrane Fusion

Developmental Cell

Volumn 32, Issue 5, 2015, Pages 561-573

  Kim, Ji Hoon ^a   Ren, Yixin ^a   Ng, Win Pin ^b   Li, Shuo ^a   Son, Sungmin ^b   Kee, Yee Seir ^a   Zhang, Shiliang ^a   Zhang, Guofeng ^c   Fletcher, Daniel A ^b   Robinson, Douglas N ^a   Chen, Elizabeth H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of California at Berkeley   (United States)

^c NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN II; LIPID BILAYER; MESSENGER RNA; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE;

ARTICLE; CELL ADHESION; CELL FUSION; CELL MEMBRANE; CHANNEL GATING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DROSOPHILA; MECHANICAL STRESS; MICROPIPETTE; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; APOPTOSIS; BIOLOGICAL MODEL; CELL COMMUNICATION; CELL CULTURE; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; ENZYME IMMUNOASSAY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOPRECIPITATION; LIPID BILAYER; MECHANOTRANSDUCTION; MEMBRANE FUSION; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL COMMUNICATION; CELL MEMBRANE; CELL PROLIFERATION; CELLS, CULTURED; DROSOPHILA MELANOGASTER; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; LIPID BILAYERS; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE FUSION; MODELS, BIOLOGICAL; MYOSIN TYPE II; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; RNA, MESSENGER;

EID: 84924287510     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.01.005     Document Type: Article

References (62)

1. Abmayr S.M., Pavlath G.K. Myoblast fusion: lessons from flies and mice. Development 2012, 139:641-656.
2. Abmayr S.M., Zhuang S., Geisbrecht E.R. Myoblast fusion in Drosophila. Methods Mol. Biol. 2008, 475:75-97.
3. Aguilar P.S., Baylies M.K., Fleissner A., Helming L., Inoue N., Podbilewicz B., Wang H., Wong M. Genetic basis of cell-cell fusion mechanisms. Trends Genet. 2013, 29:427-437.
4. Aguilar-Cuenca R., Juanes-García A., Vicente-Manzanares M. Myosin II in mechanotransduction: master and commander of cell migration, morphogenesis, and cancer. Cell. Mol. Life Sci. 2014, 71:479-492.
5. Amano M., Ito M., Kimura K., Fukata Y., Chihara K., Nakano T., Matsuura Y., Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J.Biol. Chem. 1996, 271:20246-20249.
6. Artero R.D., Castanon I., Baylies M.K. The immunoglobulin-like protein Hibris functions as a dose-dependent regulator of myoblast fusion and is differentially controlled by Ras and Notch signaling. Development 2001, 128:4251-4264.
7. Bour B.A., Chakravarti M., West J.M., Abmayr S.M. Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev. 2000, 14:1498-1511.
8. Bulchand S., Menon S.D., George S.E., Chia W. The intracellular domain of Dumbfounded affects myoblast fusion efficiency and interacts with Rolling pebbles and Loner. PLoS ONE 2010, 5:e9374.
9. Chaudhuri O., Parekh S.H., Fletcher D.A. Reversible stress softening of actin networks. Nature 2007, 445:295-298.
10. Chen E.H. Invasive podosomes and myoblast fusion. Curr. Top. Membr. 2011, 68:235-258.
11. Chen E.H., Olson E.N. Towards a molecular pathway for myoblast fusion in Drosophila. Trends Cell Biol. 2004, 14:452-460.
12. Chen E.H., Olson E.N. Unveiling the mechanisms of cell-cell fusion. Science 2005, 308:369-373.
13. Derganc J., Bozic B., Svetina S., Zeks B. Stability analysis of micropipette aspiration of neutrophils. Biophys. J. 2000, 79:153-162.
14. Discher D.E., Mooney D.J., Zandstra P.W. Growth factors, matrices, and forces combine and control stem cells. Science 2009, 324:1673-1677.
15. Doherty G.J., McMahon H.T. Mechanisms of endocytosis. Annu. Rev. Biochem. 2009, 78:857-902.
16. Dottermusch-Heidel C., Groth V., Beck L., Önel S.F. The Arf-GEF Schizo/Loner regulates N-cadherin to induce fusion competence of Drosophila myoblasts. Dev. Biol. 2012, 368:18-27.
17. Duan R., Jin P., Luo F., Zhang G., Anderson N., Chen E.H. Group I PAKs function downstream of Rac to promote podosome invasion during myoblast fusion invivo. J.Cell Biol. 2012, 199:169-185.
18. Dworak H.A., Charles M.A., Pellerano L.B., Sink H. Characterization of Drosophila hibris, a gene related to human nephrin. Development 2001, 128:4265-4276.
19. Effler J.C., Kee Y.S., Berk J.M., Tran M.N., Iglesias P.A., Robinson D.N. Mitosis-specific mechanosensing and contractile-protein redistribution control cell shape. Curr. Biol. 2006, 16:1962-1967.
20. Farge E. Mechanotransduction in development. Curr. Top. Dev. Biol. 2011, 95:243-265.
21. Fernandez-Gonzalez R., Simoes Sde.M., Röper J.C., Eaton S., Zallen J.A. Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 2009, 17:736-743.
22. Gardel M.L., Shin J.H., MacKintosh F.C., Mahadevan L., Matsudaira P., Weitz D.A. Elastic behavior of cross-linked and bundled actin networks. Science 2004, 304:1301-1305.
23. Gauthier N.C., Masters T.A., Sheetz M.P. Mechanical feedback between membrane tension and dynamics. Trends Cell Biol. 2012, 22:527-535.
24. Geisbrecht E.R., Haralalka S., Swanson S.K., Florens L., Washburn M.P., Abmayr S.M. Drosophila ELMO/CED-12 interacts with Myoblast city to direct myoblast fusion and ommatidial organization. Dev. Biol. 2008, 314:137-149.
25. Guillot C., Lecuit T. Mechanics of epithelial tissue homeostasis and morphogenesis. Science 2013, 340:1185-1189.
26. Haralalka S., Shelton C., Cartwright H.N., Katzfey E., Janzen E., Abmayr S.M. Asymmetric Mbc, active Rac1 and F-actin foci in the fusion-competent myoblasts during myoblast fusion in Drosophila. Development 2011, 138:1551-1562.
27. Jahn R., Südhof T.C. Membrane fusion and exocytosis. Annu. Rev. Biochem. 1999, 68:863-911.
28. Jahn R., Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature 2012, 490:201-207.
29. Jin P., Duan R., Luo F., Zhang G., Hong S.N., Chen E.H. Competition between Blown fuse and WASP for WIP binding regulates the dynamics of WASP-dependent actin polymerization invivo. Dev. Cell 2011, 20:623-638.
30. Kee Y.S., Robinson D.N. Motor proteins: myosin mechanosensors. Curr. Biol. 2008, 18:R860-R862.
31. Kee Y.S., Robinson D.N. Micropipette aspiration for studying cellular mechanosensory responses and mechanics. Methods Mol. Biol. 2013, 983:367-382.
32. Kielian M., Rey F.A. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 2006, 4:67-76.
33. Kim S., Shilagardi K., Zhang S., Hong S.N., Sens K.L., Bo J., Gonzalez G.A., Chen E.H. A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev. Cell 2007, 12:571-586.
34. Kovács M., Thirumurugan K., Knight P.J., Sellers J.R. Load-dependent mechanism of nonmuscle myosin 2. Proc. Natl. Acad. Sci. USA 2007, 104:9994-9999.
35. Laakso J.M., Lewis J.H., Shuman H., Ostap E.M. Myosin I can act as a molecular force sensor. Science 2008, 321:133-136.
36. Lecuit T., Lenne P.F., Munro E. Force generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 2011, 27:157-184.
37. Luo T., Mohan K., Srivastava V., Ren Y., Iglesias P.A., Robinson D.N. Understanding the cooperative interaction between myosin II and actin cross-linkers mediated by actin filaments during mechanosensation. Biophys. J. 2012, 102:238-247.
38. Luo T., Mohan K., Iglesias P.A., Robinson D.N. Molecular mechanisms of cellular mechanosensing. Nat. Mater. 2013, 12:1064-1071.
39. Mammoto T., Mammoto A., Ingber D.E. Mechanobiology and developmental control. Annu. Rev. Cell Dev. Biol. 2013, 29:27-61.
40. Martens S., McMahon H.T. Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 2008, 9:543-556.
41. Melikyan G.B. Common principles and intermediates of viral protein-mediated fusion: the HIV-1 paradigm. Retrovirology 2008, 5:111.
42. Octtaviani E., Effler J.C., Robinson D.N. Enlazin, a natural fusion of two classes of canonical cytoskeletal proteins, contributes to cytokinesis dynamics. Mol. Biol. Cell 2006, 17:5275-5286.
43. Özkan E., Chia P.H., Wang R.R., Goriatcheva N., Borek D., Otwinowski Z., Walz T., Shen K., Garcia K.C. Extracellular architecture of the SYG-1/SYG-2 adhesion complex instructs synaptogenesis. Cell 2014, 156:482-494.
44. Prokop A., Martín-Bermudo M.D., Bate M., Brown N.H. Absence of PS integrins or laminin A affects extracellular adhesion, but not intracellular assembly, of hemiadherens and neuromuscular junctions in Drosophila embryos. Dev. Biol. 1998, 196:58-76.
45. Purcell T.J., Sweeney H.L., Spudich J.A. A force-dependent state controls the coordination of processive myosin V. Proc. Natl. Acad. Sci. USA 2005, 102:13873-13878.
46. Ren Y., Effler J.C., Norstrom M., Luo T., Firtel R.A., Iglesias P.A., Rock R.S., Robinson D.N. Mechanosensing through cooperative interactions between myosin II and the actin crosslinker cortexillin I. Curr. Biol. 2009, 19:1421-1428.
47. Richardson B.E., Beckett K., Nowak S.J., Baylies M.K. SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development 2007, 134:4357-4367.
48. Risca V.I., Wang E.B., Chaudhuri O., Chia J.J., Geissler P.L., Fletcher D.A. Actin filament curvature biases branching direction. Proc. Natl. Acad. Sci. USA 2012, 109:2913-2918.
49. Rochlin K., Yu S., Roy S., Baylies M.K. Myoblast fusion: when it takes more to make one. Dev. Biol. 2010, 341:66-83.
50. Rosenbluth M.J., Lam W.A., Fletcher D.A. Force microscopy of nonadherent cells: a comparison of leukemia cell deformability. Biophys. J. 2006, 90:2994-3003.
51. Ruiz-Gómez M., Coutts N., Price A., Taylor M.V., Bate M. Drosophila dumbfounded: a myoblast attractant essential for fusion. Cell 2000, 102:189-198.
52. Sapir A., Avinoam O., Podbilewicz B., Chernomordik L.V. Viral and developmental cell fusion mechanisms: conservation and divergence. Dev. Cell 2008, 14:11-21.
53. Sens K.L., Zhang S., Jin P., Duan R., Zhang G., Luo F., Parachini L., Chen E.H. An invasive podosome-like structure promotes fusion pore formation during myoblast fusion. J.Cell Biol. 2010, 191:1013-1027.
54. Shelton C., Kocherlakota K.S., Zhuang S., Abmayr S.M. The immunoglobulin superfamily member Hbs functions redundantly with Sns in interactions between founder and fusion-competent myoblasts. Development 2009, 136:1159-1168.
55. Shilagardi K., Li S., Luo F., Marikar F., Duan R., Jin P., Kim J.H., Murnen K., Chen E.H. Actin-propelled invasive membrane protrusions promote fusogenic protein engagement during cell-cell fusion. Science 2013, 340:359-363.
56. Simões Sde.M., Blankenship J.T., Weitz O., Farrell D.L., Tamada M., Fernandez-Gonzalez R., Zallen J.A. Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation. Dev. Cell 2010, 19:377-388.
57. Strünkelnberg M., Bonengel B., Moda L.M., Hertenstein A., de Couet H.G., Ramos R.G., Fischbach K.F. rst and its paralogue kirre act redundantly during embryonic muscle development in Drosophila. Development 2001, 128:4229-4239.
58. Uehara R., Goshima G., Mabuchi I., Vale R.D., Spudich J.A., Griffis E.R. Determinants of myosin II cortical localization during cytokinesis. Curr. Biol. 2010, 20:1080-1085.
59. Vogel V., Sheetz M.P. Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways. Curr. Opin. Cell Biol. 2009, 21:38-46.
60. Xu J., Tseng Y., Wirtz D. Strain hardening of actin filament networks. Regulation by the dynamic cross-linking protein alpha-actinin. J.Biol. Chem. 2000, 275:35886-35892.
61. Zajac A.L., Discher D.E. Cell differentiation through tissue elasticity-coupled, myosin-driven remodeling. Curr. Opin. Cell Biol. 2008, 20:609-615.
62. Zhang S., Chen E.H. Ultrastructural analysis of myoblast fusion in Drosophila. Cell Fusion: Overviews and Methods 2008, 275-297. Humana Press, New Jersey. E.H. Chen (Ed.).