Drosophila integrin adhesion complexes are essential for hemocyte migration in vivo

Biology Open

Volumn 2, Issue 8, 2013, Pages 795-801

  Moreira, Carolina G A ^a   Jacinto, Antonio ^a,b   Prag, Soren ^a,c  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b NOVA MEDICAL SCHOOL   (Portugal)

^c CARL ZEISS SMT AG   (Germany)

Author keywords

Drosophila; Hemocyte; Integrin; Migration

Indexed keywords

EID: 84965131597     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20134564     Document Type: Article

References (53)

1. Alatortsev, V. E., Kramerova, I. A., Frolov, M. V., Lavrov, S. A. and Westphal, E. D. (1997). Vinculin gene is non-essential in Drosophila melanogaster. FEBS Lett. 413, 197-201.
2. Anthis, N. J., Wegener, K. L., Ye, F., Kim, C., Goult, B. T., Lowe, E. D., Vakonakis, I., Bate, N., Critchley, D. R., Ginsberg, M. H. et al. (2009). The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J. 28, 3623-3632.
3. Babcock, D. T., Brock, A. R., Fish, G. S., Wang, Y., Perrin, L., Krasnow, M. A. and Galko, M. J. (2008). Circulating blood cells function as a surveillance system for damaged tissue in Drosophila larvae. Proc. Natl. Acad. Sci. USA 105, 10017-10022.
4. Bainbridge, S. P. and Bownes, M. (1981). Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morphol. 66, 57-80.
5. Baker, B. M. and Chen, C. S. (2012). Deconstructing the third dimension: how 3D culture microenvironments alter cellular cues. J. Cell Sci. 125, 3015-3024.
6. Beerling, E., Ritsma, L., Vrisekoop, N., Derksen, P. W. B. and van Rheenen, J. (2011). Intravital microscopy: new insights into metastasis of tumors. J. Cell Sci. 124, 299-310.
7. Bornens, M. (2008). Organelle positioning and cell polarity. Nat. Rev. Mol. Cell Biol. 9, 874-886.
8. Brown, N. H., Gregory, S. L. and Martin-Bermudo, M. D. (2000). Integrins as mediators of morphogenesis in Drosophila. Dev. Biol. 223, 1-16.
9. Choi, C. K., Vicente-Manzanares, M., Zareno, J., Whitmore, L. A., Mogilner, A. and Horwitz, A. R. (2008). Actin and alpha-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat. Cell Biol. 10, 1039-1050.
10. Coll, J. L., Ben-Ze'ev, A., Ezzell, R. M., Rodríguez Fernández, J. L., Baribault, H., Oshima, R. G. and Adamson, E. D. (1995). Targeted disruption of vinculin genes in F9 and embryonic stem cells changes cell morphology, adhesion, and locomotion. Proc. Natl. Acad. Sci. USA 92, 9161-9165.
11. Deramaudt, T. B., Dujardin, D., Hamadi, A., Noulet, F., Kolli, K., De Mey, J., Takeda, K. and Rondé, P. (2011). FAK phosphorylation at Tyr-925 regulates crosstalk between focal adhesion turnover and cell protrusion. Mol. Biol. Cell 22, 964-975.
12. DiMilla, P. A., Barbee, K. and Lauffenburger, D. A. (1991). Mathematical model for the effects of adhesion and mechanics on cell migration speed. Biophys. J. 60, 15-37.
13. Duffy, J. B. (2002). GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34, 1-15.
14. Fraley, S. I., Feng, Y., Krishnamurthy, R., Kim, D.-H., Celedon, A., Longmore, G. D. and Wirtz, D. (2010). A distinctive role for focal adhesion proteins in threedimensional cell motility. Nat. Cell Biol. 12, 598-604.
15. Goto, A., Kumagai, T., Kumagai, C., Hirose, J., Narita, H., Mori, H., Kadowaki, T., Beck, K. and Kitagawa, Y. (2001). A Drosophila haemocyte-specific protein, hemolectin, similar to human von Willebrand factor. Biochem. J. 359, 99-108.
16. Grabbe, C., Zervas, C. G., Hunter, T., Brown, N. H. and Palmer, R. H. (2004). Focal adhesion kinase is not required for integrin function or viability in Drosophila. Development 131, 5795-5805.
17. Grashoff, C., Hoffman, B. D., Brenner, M. D., Zhou, R., Parsons, M., Yang, M. T., McLean, M. A., Sligar, S. G., Chen, C. S., Ha, T. et al. (2010). Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266.
18. Harburger, D. S., Bouaouina, M. and Calderwood, D. A. (2009). Kindlin-1 and -2 directly bind the C-terminal region of beta integrin cytoplasmic tails and exert integrin-specific activation effects. J. Biol. Chem. 284, 11485-11497.
19. Hoffman, L. M., Jensen, C. C., Kloeker, S., Wang, C.-L. A., Yoshigi, M. and Beckerle, M. C. (2006). Genetic ablation of zyxin causes Mena/VASP mislocalization, increased motility, and deficits in actin remodeling. J. Cell Biol. 172, 771-782.
20. Huelsmann, S., Hepper, C., Marchese, D., Knöll, C. and Reuter, R. (2006). The PDZ-GEF dizzy regulates cell shape of migrating macrophages via Rap1 and integrins in the Drosophila embryo. Development 133, 2915-2924.
21. Humphries, J. D., Wang, P., Streuli, C., Geiger, B., Humphries, M. J. and Ballestrem, C. (2007). Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 179, 1043-1057.
22. Huttenlocher, A. and Horwitz, A. R. (2011). Integrins in cell migration. Cold Spring Harb. Perspect. Biol. 3, a005074.
23. Ilí, D., Kovacic, B., Johkura, K., Schlaepfer, D. D., Tomaseví, N., Han, Q., Kim, J.-B., Howerton, K., Baumbusch, C., Ogiwara, N. et al. (2004). FAK promotes organization of fibronectin matrix and fibrillar adhesions. J. Cell Sci. 117, 177-187.
24. Lämmermann, T., Bader, B. L., Monkley, S. J., Worbs, T., Wedlich-Söldner, R., Hirsch, K., Keller, M., Förster, R., Critchley, D. R., Fässler, R. et al. (2008). Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453, 51-55.
25. Lanot, R., Zachary, D., Holder, F. and Meister, M. (2001). Postembryonic hematopoiesis in Drosophila. Dev. Biol. 230, 243-257.
26. Larjava, H., Plow, E. F. and Wu, C. (2008). Kindlins: essential regulators of integrin signalling and cell-matrix adhesion. EMBO Rep. 9, 1203-1208.
27. Li, R. and Gundersen, G. G. (2008). Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nat. Rev. Mol. Cell Biol. 9, 860-873.
28. Makhijani, K., Alexander, B., Tanaka, T., Rulifson, E. and Brückner, K. (2011). The peripheral nervous system supports blood cell homing and survival in the Drosophila larva. Development 138, 5379-5391.
29. Márkus, R., Laurinyecz, B., Kurucz, E., Honti, V., Bajusz, I., Sipos, B., Somogyi, K., Kronhamn, J., Hultmark, D. and Andó, I. (2009). Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 106, 4805-4809.
30. Mellman, I. and Nelson, W. J. (2008). Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9, 833-845.
31. Mierke, C. T., Kollmannsberger, P., Zitterbart, D. P., Diez, G., Koch, T. M., Marg, S., Ziegler, W. H., Goldmann, W. H. and Fabry, B. (2010). Vinculin facilitates cell invasion into three-dimensional collagen matrices. J. Biol. Chem. 285, 13121-13130.
32. Montell, D. J., Yoon, W. H. and Starz-Gaiano, M. (2012). Group choreography: mechanisms orchestrating the collective movement of border cells. Nat. Rev. Mol. Cell Biol. 13, 631-645.
33. Moreira, C. G. A., Regan, J. C., Zaidman-Rémy, A., Jacinto, A. and Prag, S. (2011). Drosophila hemocyte migration: an in vivo assay for directional cell migration. Methods Mol. Biol. 769, 249-260.
34. Niethammer, P., Grabher, C., Look, A. T. and Mitchison, T. J. (2009). A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459, 996-999.
35. Palecek, S. P., Loftus, J. C., Ginsberg, M. H., Lauffenburger, D. A. and Horwitz, A. F. (1997). Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385, 537-540.
36. Parsons, J. T., Horwitz, A. R. and Schwartz, M. A. (2010). Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11, 633-643.
37. Siekhaus, D., Haesemeyer, M., Moffitt, O. and Lehmann, R. (2010). RhoL controls invasion and Rap1 localization during immune cell transmigration in Drosophila. Nat. Cell Biol. 12, 605-610.
38. Sinenko, S. A. and Mathey-Prevot, B. (2004). Increased expression of Drosophila tetraspanin, Tsp68C, suppresses the abnormal proliferation of ytr-deficient and Ras/ Raf-activated hemocytes. Oncogene 23, 9120-9128.
39. Smith, M. A., Blankman, E., Gardel, M. L., Luettjohann, L., Waterman, C. M. and Beckerle, M. C. (2010). A zyxin-mediated mechanism for actin stress fiber maintenance and repair. Dev. Cell 19, 365-376.
40. Stofanko, M., Kwon, S. Y. and Badenhorst, P. (2008). A misexpression screen to identify regulators of Drosophila larval hemocyte development. Genetics 180, 253-267.
41. Stramer, B., Wood, W., Galko, M. J., Redd, M. J., Jacinto, A., Parkhurst, S. M. and Martin, P. (2005). Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J. Cell Biol. 168, 567-573.
42. Stramer, B., Moreira, S., Millard, T., Evans, I., Huang, C.-Y., Sabet, O., Milner, M., Dunn, G., Martin, P. and Wood, W. (2010). Clasp-mediated microtubule bundling regulates persistent motility and contact repulsion in Drosophila macrophages in vivo. J. Cell Biol. 189, 681-689.
43. Tirouvanziam, R., Davidson, C. J., Lipsick, J. S. and Herzenberg, L. A. (2004). Fluorescence-activated cell sorting (FACS) of Drosophila hemocytes reveals important functional similarities to mammalian leukocytes. Proc. Natl. Acad. Sci. USA 101, 2912-2917.
44. Toetsch, S., Olwell, P., Prina-Mello, A. and Volkov, Y. (2009). The evolution of chemotaxis assays from static models to physiologically relevant platforms. Integr. Biol. 1, 170-181.
45. Tolde, O., Rösel, D., Janoštiak, R., Veselý, P. and Brábek, J. (2012). Dynamics and morphology of focal adhesions in complex 3D environment. Folia Biologica 58, 177-184.
46. Weijer, C. J. (2009). Collective cell migration in development. J. Cell Sci. 122, 3215-3223.
47. Wood, W. and Jacinto, A. (2007). Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat. Rev. Mol. Cell Biol. 8, 542-551.
48. Wu, J. S. and Luo, L. (2007). A protocol for mosaic analysis with a repressible cell marker (MARCM) in Drosophila. Nat. Protoc. 1, 2583-2589.
49. Ye, F., Kim, C. and Ginsberg, M. H. (2011). Molecular mechanism of inside-out integrin regulation. J. Thromb. Haemost. 9 Suppl. 1, 20-25.
50. Yoshigi, M., Hoffman, L. M., Jensen, C. C., Yost, H. J. and Beckerle, M. C. (2005). Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J. Cell Biol. 171, 209-215.
51. Zaidel-Bar, R., Ballestrem, C., Kam, Z. and Geiger, B. (2003). Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J. Cell Sci. 116, 4605-4613.
52. Zaidel-Bar, R., Itzkovitz, S., Ma'ayan, A., Iyengar, R. and Geiger, B. (2007). Functional atlas of the integrin adhesome. Nat. Cell Biol. 9, 858-867.
53. Zettervall, C.-J., Anderl, I., Williams, M. J., Palmer, R., Kurucz, E., Ando, I. and Hultmark, D. (2004). A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA 101, 14192-14197.