Integrins regulate epithelial cell shape by controlling the architecture and mechanical properties of basal actomyosin networks
Autoři:
Carmen Santa-Cruz Mateos aff001; Andrea Valencia-Expósito aff001; Isabel M. Palacios aff002; María D. Martín-Bermudo aff001
Působiště autorů:
Centro Andaluz de Biología del Desarrollo, Universidad Pablo de Olavide/CSIC/JA, Carretera de Utrera,Sevilla, Spain
aff001; School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
aff002
Vyšlo v časopise:
Integrins regulate epithelial cell shape by controlling the architecture and mechanical properties of basal actomyosin networks. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008717
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008717
Souhrn
Forces generated by the actomyosin cytoskeleton are key contributors to many morphogenetic processes. The actomyosin cytoskeleton organises in different types of networks depending on intracellular signals and on cell-cell and cell-extracellular matrix (ECM) interactions. However, actomyosin networks are not static and transitions between them have been proposed to drive morphogenesis. Still, little is known about the mechanisms that regulate the dynamics of actomyosin networks during morphogenesis. This work uses the Drosophila follicular epithelium, real-time imaging, laser ablation and quantitative analysis to study the role of integrins on the regulation of basal actomyosin networks organisation and dynamics and the potential contribution of this role to cell shape. We find that elimination of integrins from follicle cells impairs F-actin recruitment to basal medial actomyosin stress fibers. The available F-actin redistributes to the so-called whip-like structures, present at tricellular junctions, and into a new type of actin-rich protrusions that emanate from the basal cortex and project towards the medial region. These F-actin protrusions are dynamic and changes in total protrusion area correlate with periodic cycles of basal myosin accumulation and constriction pulses of the cell membrane. Finally, we find that follicle cells lacking integrin function show increased membrane tension and reduced basal surface. Furthermore, the actin-rich protrusions are responsible for these phenotypes as their elimination in integrin mutant follicle cells rescues both tension and basal surface defects. We thus propose that the role of integrins as regulators of stress fibers plays a key role on controlling epithelial cell shape, as integrin disruption promotes reorganisation into other types of actomyosin networks, in a manner that interferes with proper expansion of epithelial basal surfaces.
Klíčová slova:
Actins – Cell membranes – Cloning – Cytoskeleton – Integrins – Morphogenesis – Myosins – Membrane structures
Zdroje
1. Murrell M, Oakes PW, Lenz M, Gardel ML. Forcing cells into shape: the mechanics of actomyosin contractility. Nat Rev Mol Cell Biol. 2015;16(8):486–98. doi: 10.1038/nrm4012 26130009.
2. Gunning PW, Ghoshdastider U, Whitaker S, Popp D, Robinson RC. The evolution of compositionally and functionally distinct actin filaments. J Cell Sci. 2015;128(11):2009–19. doi: 10.1242/jcs.165563 25788699.
3. Martin AC, Goldstein B. Apical constriction: themes and variations on a cellular mechanism driving morphogenesis. Development. 2014;141(10):1987–98. Epub 2014/05/08. 141/10/1987 [pii] doi: 10.1242/dev.102228 24803648.
4. Tojkander S, Gateva G, Lappalainen P. Actin stress fibers—assembly, dynamics and biological roles. J Cell Sci. 2012;125(Pt 8):1855–64. doi: 10.1242/jcs.098087 22544950.
5. Chalut KJ, Paluch EK. The Actin Cortex: A Bridge between Cell Shape and Function. Dev Cell. 2016;38(6):571–3. doi: 10.1016/j.devcel.2016.09.011 27676427.
6. Spradling AC. Developmental genetics of oogenesis. The Development of Drosophila melanogaster M Bate and A Martinez-Arias, editors Cold Spring Harbor Lab Press, Cold Spring Harbor, New York. 1993:1–70.
7. King RC. Ovarian development in Drosophila melanogaster. Academic Press, New York, NY. 1970.
8. Calvi BR, Lilly MA, Spradling AC. Cell cycle control of chorion gene amplification. Genes Dev. 1998;12(5):734–44. Epub 1998/04/16. doi: 10.1101/gad.12.5.734 9499407.
9. Gutzeit HO, Eberhardt W, Gratwohl E. Laminin and basement membrane-associated microfilaments in wild type and mutant Drosophila ovarian follicles. J Cell Science. 1991;100:781–88. 1814932
10. Cetera M, Ramirez-San Juan GR, Oakes PW, Lewellyn L, Fairchild MJ, Tanentzapf G, et al. Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation. Nature communications. 2014;5:5511. Epub 2014/11/22. doi: 10.1038/ncomms6511 25413675; PubMed Central PMCID: PMC4241503.
11. Squarr AJ, Brinkmann K, Chen B, Steinbacher T, Ebnet K, Rosen MK, et al. Fat2 acts through the WAVE regulatory complex to drive collective cell migration during tissue rotation. J Cell Biol. 2016;212(5):591–603. doi: 10.1083/jcb.201508081 26903538; PubMed Central PMCID: PMC4772498.
12. Delon I, Brown NH. The integrin adhesion complex changes its composition and function during morphogenesis of an epithelium. J Cell Sci. 2009;122(Pt 23):4363–74. Epub 2009/11/12. jcs.055996 [pii] doi: 10.1242/jcs.055996 19903692.
13. Haigo SL, Bilder D. Global tissue revolutions in a morphogenetic movement controlling elongation. Science. 2011;331(6020):1071–4. Epub 2011/01/08. science.1199424 [pii] doi: 10.1126/science.1199424 21212324.
14. Diaz de la Loza MC, Diaz-Torres A, Zurita F, Rosales-Nieves, Moeendarbary E, Franze K, et al. Laminin Levels Regulate Tissue Migration and Anterior-Posterior Polarity during Egg Morphogenesis in Drosophila. Cell Rep. 2017;20(1):211–23. doi: 10.1016/j.celrep.2017.06.031 28683315; PubMed Central PMCID: PMC5507772.
15. Couchman JR, Rees DA. The behaviour of fibroblasts migrating from chick heart explants: changes in adhesion, locomotion and growth, and in the distribution of actomyosin and fibronectin. J Cell Sci. 1979;39:149–65. 575139.
16. Bateman J, Reddy R, Saito H, Van Vactor D. The receptor tyrosine phsphatase Dlar and integrins organize actin filaments in the Drosophila follicular epithelium. Curr Biol. 2001;11:1317–27. doi: 10.1016/s0960-9822(01)00420-1 11553324
17. Schotman H, Karhinen L, Rabouille C. dGRASP-mediated noncanonical integrin secretion is required for Drosophila epithelial remodeling. Dev Cell. 2008;14(2):171–82. doi: 10.1016/j.devcel.2007.12.006 18267086.
18. He L, Wang X, Tang HL, Montell DJ. Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat Cell Biol. 2010;12(12):1133–42. Epub 2010/11/26. ncb2124 [pii] doi: 10.1038/ncb2124 21102441.
19. Qin X, Park BO, Liu J, Chen B, Choesmel-Cadamuro V, Belguise K, et al. Cell-matrix adhesion and cell-cell adhesion differentially control basal myosin oscillation and Drosophila egg chamber elongation. Nature communications. 2017;8:14708. doi: 10.1038/ncomms14708 28406187; PubMed Central PMCID: PMC5399299.
20. Martin AC, Kaschube M, Wieschaus EF. Pulsed contractions of an actin-myosin network drive apical constriction. Nature. 2009;457(7228):495–9. Epub 2008/11/26. nature07522 [pii] doi: 10.1038/nature07522 19029882.
21. Morin X, Daneman R, Zavortink M, Chia W. A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci U S A. 2001;98(26):15050–5. doi: 10.1073/pnas.261408198 11742088; PubMed Central PMCID: PMC64981.
22. Badley RA, Woods A, Carruthers L, Rees DA. Cytoskeleton changes in fibroblast adhesion and detachment. J Cell Sci. 1980;43:379–90. 6774989.
23. Farhadifar R, Roper JC, Aigouy B, Eaton S, Julicher F. The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol. 2007;17(24):2095–104. Epub 2007/12/18. S0960-9822(07)02334-2 [pii] doi: 10.1016/j.cub.2007.11.049 18082406.
24. Hutson MS, Tokutake Y, Chang MS, Bloor JW, Venakides S, Kiehart DP, et al. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science. 2003;300(5616):145–9. Epub 2003/02/08. doi: 10.1126/science.1079552 12574496.
25. Diz-Munoz A, Fletcher DA, Weiner OD. Use the force: membrane tension as an organizer of cell shape and motility. Trends Cell Biol. 2013;23(2):47–53. doi: 10.1016/j.tcb.2012.09.006 23122885; PubMed Central PMCID: PMC3558607.
26. Wildt B, Wirtz D, Searson PC. Programmed subcellular release for studying the dynamics of cell detachment. Nat Methods. 2009;6(3):211–3. doi: 10.1038/nmeth.1299 19182793; PubMed Central PMCID: PMC2882093.
27. Kolahi KS, White PF, Shreter DM, Classen AK, Bilder D, Mofrad MR. Quantitative analysis of epithelial morphogenesis in Drosophila oogenesis: New insights based on morphometric analysis and mechanical modeling. Dev Biol. 2009;331(2):129–39. doi: 10.1016/j.ydbio.2009.04.028 19409378; PubMed Central PMCID: PMC3145632.
28. Gomez-Lamarca MJ, Cobreros-Reguera L, Ibanez-Jimenez B, Palacios IM, Martin-Bermudo MD. Integrins regulate epithelial cell differentiation by modulating Notch activity. J Cell Sci. 2014;127(Pt 21):4667–78. doi: 10.1242/jcs.153122 25179603; PubMed Central PMCID: PMC4215713.
29. Cooper G M. The Cell: A Molecular Approach. 2nd edition. Sunderland (MA) Sinauer Associates; Structure and Organization of Actin Filaments. 2000.
30. Li MA, Alls JD, Avancini RM, Koo K, Godt D. The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nat Cell Biol. 2003;5(11):994–1000. doi: 10.1038/ncb1058 14578908.
31. Franke JD, Montague RA, Kiehart DP. Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr Biol. 2005;15(24):2208–21. doi: 10.1016/j.cub.2005.11.064 16360683.
32. Tojkander S, Gateva G, Husain A, Krishnan R, Lappalainen P. Generation of contractile actomyosin bundles depends on mechanosensitive actin filament assembly and disassembly. Elife. 2015;4:e06126. doi: 10.7554/eLife.06126 26652273; PubMed Central PMCID: PMC4714978.
33. Zemel A, Rehfeldt F, Brown AE, Discher DE, Safran SA. Cell shape, spreading symmetry and the polarization of stress-fibers in cells. J Phys Condens Matter. 2010;22(19):194110. doi: 10.1088/0953-8984/22/19/194110 20458358; PubMed Central PMCID: PMC2865697.
34. Laukaitis CM, Webb DJ, Donais K, Horwitz AF. Differential dynamics of alpha 5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells. J Cell Biol. 2001;153(7):1427–40. doi: 10.1083/jcb.153.7.1427 11425873; PubMed Central PMCID: PMC2150721.
35. Serrels B, Serrels A, Brunton VG, Holt M, McLean GW, Gray CH, et al. Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat Cell Biol. 2007;9(9):1046–56. doi: 10.1038/ncb1626 17721515.
36. Kumar S, Maxwell IZ, Heisterkamp A, Polte TR, Lele TP, Salanga M, et al. Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys J. 2006;90(10):3762–73. doi: 10.1529/biophysj.105.071506 16500961; PubMed Central PMCID: PMC1440757.
37. Baird MA, Billington N, Wang A, Adelstein RS, Sellers JR, Fischer RS, et al. Local pulsatile contractions are an intrinsic property of the myosin 2A motor in the cortical cytoskeleton of adherent cells. Mol Biol Cell. 2017;28(2):240–51. doi: 10.1091/mbc.E16-05-0335 27881665; PubMed Central PMCID: PMC5231893.
38. Yamane J, Ohnishi H, Sasaki H, Narimatsu H, Ohgushi H, Tachibana K. Formation of microvilli and phosphorylation of ERM family proteins by CD43, a potent inhibitor for cell adhesion: cell detachment is a potential cue for ERM phosphorylation and organization of cell morphology. Cell Adh Migr. 2011;5(2):119–32. doi: 10.4161/cam.5.2.13908 21045567; PubMed Central PMCID: PMC3084977.
39. Koster DV, Husain K, Iljazi E, Bhat A, Bieling P, Mullins RD, et al. Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer. Proc Natl Acad Sci U S A. 2016;113(12):E1645–54. doi: 10.1073/pnas.1514030113 26929326; PubMed Central PMCID: PMC4812753.
40. Frydman HM, Spradling AC. The receptor-like tyrosine phosphatase lar is required for epithelial planar polarity and for axis determination within drosophila ovarian follicles. Development. 2001;128(16):3209–20. Epub 2001/11/02. 11688569.
41. Nakata T, Okimura C, Mizuno T, Iwadate Y. The Role of Stress Fibers in the Shape Determination Mechanism of Fish Keratocytes. Biophys J. 2016;110(2):481–92. doi: 10.1016/j.bpj.2015.12.014 26789770; PubMed Central PMCID: PMC4724663.
42. Poujade M, Grasland-Mongrain E, Hertzog A, Jouanneau J, Chavrier P, Ladoux B, et al. Collective migration of an epithelial monolayer in response to a model wound. Proc Natl Acad Sci U S A. 2007;104(41):15988–93. doi: 10.1073/pnas.0705062104 17905871; PubMed Central PMCID: PMC2042149.
43. Ramirez NE, Zhang Z, Madamanchi A, Boyd KL, O'Rear LD, Nashabi A, et al. The alpha(2)beta(1) integrin is a metastasis suppressor in mouse models and human cancer. J Clin Invest. 2011;121(1):226–37. doi: 10.1172/JCI42328 21135504; PubMed Central PMCID: PMC3007139.
44. Newell-Litwa KA, Horwitz R, Lamers ML. Non-muscle myosin II in disease: mechanisms and therapeutic opportunities. Dis Model Mech. 2015;8(12):1495–515. doi: 10.1242/dmm.022103 26542704; PubMed Central PMCID: PMC4728321.
45. Bunch TA, Salatino R, Engelsgjerd MC, Mukai L, West RF, Brower DL. Characterization of mutant alleles of myospheroid,the gene encoding the b subunit of the Drosophila PS integrins. Genetics. 1992;132:519–28. 1427041
46. Royou A, Field C, Sisson JC, Sullivan W, Karess R. Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos. Mol Biol Cell. 2004;15(2):838–50. Epub 2003/12/06. doi: 10.1091/mbc.E03-06-0440 E03-06-0440 [pii]. 14657248.
47. Tanentzapf G, Devenport D, Godt D, Brown NH. Integrin-dependent anchoring of a stem-cell niche. Nat Cell Biol. 2007;9(12):1413–8. Epub 2007/11/06. ncb1660 [pii] doi: 10.1038/ncb1660 17982446.
48. Martin AC, Gelbart M, Fernandez-Gonzalez R, Kaschube M, Wieschaus EF. Integration of contractile forces during tissue invagination. J Cell Biol. 2010;188(5):735–49. Epub 2010/03/03. jcb.200910099 [pii] doi: 10.1083/jcb.200910099 20194639.
49. Struhl G, Basler K. Organizing activity of wingless protein in Drosophila. Cell. 1993;72(4):527–40. doi: 10.1016/0092-8674(93)90072-x 8440019.
50. Chou TB, Perrimon N. Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics. 1992;131:643–53. 1628809
51. Prasad M, Montell DJ. Cellular and molecular mechanisms of border cell migration analysed using time-lapse live-cell imaging. Dev Cell. 2007;12:997–1005. doi: 10.1016/j.devcel.2007.03.021 17543870
52. Valencia-Exposito A, Grosheva I, Miguez DG, Gonzalez-Reyes A, Martin-Bermudo MD. Myosin light-chain phosphatase regulates basal actomyosin oscillations during morphogenesis. Nature communications. 2016;7:10746. doi: 10.1038/ncomms10746 26888436; PubMed Central PMCID: PMC4759631.
53. Fernandez-Espartero CH, Ramel D, Farago M, Malartre M, Luque CM, Limanovich S, et al. GTP exchange factor Vav regulates guided cell migration by coupling guidance receptor signalling to local Rac activation. J Cell Sci. 2013;126(Pt 10):2285–93. doi: 10.1242/jcs.124438 23525006.
54. Sanchez-Sanchez BJ, Urbano JM, Comber K, Dragu A, Wood W, Stramer B, et al. Drosophila Embryonic Hemocytes Produce Laminins to Strengthen Migratory Response. Cell Rep. 2017;21(6):1461–70. doi: 10.1016/j.celrep.2017.10.047 29117553; PubMed Central PMCID: PMC5695906.
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 6
- Může hubnutí souviset s vyšším rizikem nádorových onemocnění?
- Raději si zajděte na oční! Jak souvisí citlivost zraku s rozvojem demence?
- Co způsobuje pooperační infekce? Na vině může být i naše vlastní mikrobiota
- Čeká nás průlom v diagnostice karcinomu pankreatu?
- Polibek, který mi „vzal nohy“ aneb vzácný výskyt EBV u 70leté ženy – kazuistika
Nejčtenější v tomto čísle
- AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization
- Osteocalcin promotes bone mineralization but is not a hormone
- Super-resolution imaging of RAD51 and DMC1 in DNA repair foci reveals dynamic distribution patterns in meiotic prophase
- Steroid hormones regulate genome-wide epigenetic programming and gene transcription in human endometrial cells with marked aberrancies in endometriosis