Group I PAKs function downstream of Rac to promote podosome invasion during myoblast fusion in vivo

Journal of Cell Biology

Volumn 199, Issue 1, 2012, Pages 169-185

  Duan, Rui ^a   Jin, Peng ^a   Luo, Fengbao ^a   Zhang, Guofeng ^b   Anderson, Nathan ^a   Chen, Elizabeth H ^a  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; P21 ACTIVATED KINASE; PROTEIN DPAK1; PROTEIN DPAK3; RAC PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL FUSION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENZYME ACTIVATION; MYOBLAST; NONHUMAN; PODOSOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; CELL FUSION; CELL SURFACE EXTENSIONS; DROSOPHILA; MYOBLASTS; P21-ACTIVATED KINASES; RAC GTP-BINDING PROTEINS;

EID: 84869127085     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201204065     Document Type: Article

References (75)

1. Abmayr, S.M., and G.K. Pavlath. 2012. Myoblast fusion: lessons from flies and mice. Development. 139:641-656. http://dx.doi.org/10.1242/dev.068353
2. Abmayr, S.M., L. Balagopalan, B.J. Galletta, and S.J. Hong. 2003. Cell and molecular biology of myoblast fusion. Int. Rev. Cytol. 225:33-89. http://dx.doi.org/10.1016/S0074-7696(05)25002-7
3. Abo, A., J. Qu, M.S. Cammarano, C. Dan, A. Fritsch, V. Baud, B. Belisle, and A. Minden. 1998. PAK4, a novel effector for Cdc42Hs, is implicated in the reorganization of the actin cytoskeleton and in the formation of filopodia. EMBO J. 17:6527-6540. http://dx.doi.org/10.1093/emboj/17.22.6527
4. Adam, L., R. Vadlamudi, M. Mandal, J. Chernoff, and R. Kumar. 2000. Regulation of microfilament reorganization and invasiveness of breast cancer cells by kinase dead p21-activated kinase-1. J. Biol. Chem. 275:12041-12050. http://dx.doi.org/10.1074/jbc.275.16.12041
5. Albin, S.D., and G.W. Davis. 2004. Coordinating structural and functional synapse development: postsynaptic p21-activated kinase independently specifies glutamate receptor abundance and postsynaptic morphology. J. Neurosci. 24:6871-6879. http://dx.doi.org/10.1523/JNEUROSCI.1538-04.2004
6. Arias-Romero, L.E., and J. Chernoff. 2008. A tale of two Paks. Biol. Cell. 100:97-108. http://dx.doi.org/10.1042/BC20070109
7. Arias-Romero, L.E., O. Villamar-Cruz, A. Pacheco, R. Kosoff, M. Huang, S.K. Muthuswamy, and J. Chernoff. 2010. A Rac-Pak signaling pathway is essential for ErbB2-mediated transformation of human breast epithelial cancer cells. Oncogene. 29:5839-5849. http://dx.doi.org/10.1038/onc.2010.318
8. Artero, R.D., I. Castanon, and M.K. Baylies. 2001. The immunoglobulin-like protein Hibris functions as a dose-dependent regulator of myoblast fusion and is differentially controlled by Ras and Notch signaling. Development. 128:4251-4264.
9. Ayala, I., M. Baldassarre, G. Giacchetti, G. Caldieri, S. Tetè, A. Luini, and R. Buccione. 2008. Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J. Cell Sci. 121:369-378. http://dx.doi.org/10.1242/jcs.008037
10. Bahri, S.M., J.M. Choy, E. Manser, L. Lim, and X. Yang. 2009. The Drosophila homologue of Arf-GAP GIT1, dGIT, is required for proper muscle morphogenesis and guidance during embryogenesis. Dev. Biol. 325:15-23. http://dx.doi.org/10.1016/j.ydbio.2008.09.001
11. Bahri, S., S. Wang, R. Conder, J. Choy, S. Vlachos, K. Dong, C. Merino, S. Sigrist, C. Molnar, X. Yang, et al. 2010. The leading edge during dorsal closure as a model for epithelial plasticity: Pak is required for recruitment of the Scribble complex and septate junction formation. Development. 137:2023-2032. http://dx.doi.org/10.1242/dev.045088
12. Ben-Yaacov, S., R. Le Borgne, I. Abramson, F. Schweisguth, and E.D. Schejter. 2001. Wasp, the Drosophila Wiskott-Aldrich syndrome gene homologue, is required for cell fate decisions mediated by Notch signaling. J. Cell Biol. 152:1-13.
13. Benner, G.E., P.B. Dennis, and R.A. Masaracchia. 1995. Activation of an S6/H4 kinase (PAK 65) from human placenta by intramolecular and intermolecular autophosphorylation. J. Biol. Chem. 270:21121-21128. http://dx.doi.org/10.1074/jbc.270.36.21121
14. Bokoch, G.M. 2003. Biology of the p21-activated kinases. Annu. Rev. Biochem. 72:743-781. http://dx.doi.org/10.1146/annurev.biochem.72.121801.161742
15. Bour, B.A., M. Chakravarti, J.M. West, and S.M. Abmayr. 2000. Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev. 14:1498-1511.
16. Chen, E.H. 2011. Invasive podosomes and myoblast fusion. Curr Top Membr. 68:235-258. http://dx.doi.org/10.1016/B978-0-12-385891-7.00010-6
17. Chen, E.H., and E.N. Olson. 2004. Towards a molecular pathway for myoblast fusion in Drosophila. Trends Cell Biol. 14:452-460. http://dx.doi.org/10.1016/j.tcb.2004.07.008
18. Chong, C., L. Tan, L. Lim, and E. Manser. 2001. The mechanism of PAK activation. Autophosphorylation events in both regulatory and kinase domains control activity. J. Biol. Chem. 276:17347-17353. http://dx.doi.org/10.1074/jbc.M009316200
19. Claessens, M.M., M. Bathe, E. Frey, and A.R. Bausch. 2006. Actin-binding proteins sensitively mediate F-actin bundle stiffness. Nat. Mater. 5:748-753. http://dx.doi.org/10.1038/nmat1718
20. Conder, R., H. Yu, M. Ricos, H. Hing, W. Chia, L. Lim, and N. Harden. 2004. dPak is required for integrity of the leading edge cytoskeleton during Drosophila dorsal closure but does not signal through the JNK cascade. Dev. Biol. 276:378-390. http://dx.doi.org/10.1016/j.ydbio.2004.08.044
21. Conder, R., H. Yu, B. Zahedi, and N. Harden. 2007. The serine/threonine kinase dPak is required for polarized assembly of F-actin bundles and apical-basal polarity in the Drosophila follicular epithelium. Dev. Biol. 305:470-482. http://dx.doi.org/10.1016/j.ydbio.2007.02.034
22. Duan, H., J.B. Skeath, and H.T. Nguyen. 2001. Drosophila Lame duck, a novel member of the Gli superfamily, acts as a key regulator of myogenesis by controlling fusion-competent myoblast development. Development. 128:4489-4500.
23. Dworak, H.A., M.A. Charles, L.B. Pellerano, and H. Sink. 2001. Characterization of Drosophila hibris, a gene related to human nephrin. Development. 128:4265-4276.
24. Erickson, M.R., B.J. Galletta, and S.M. Abmayr. 1997. Drosophila myoblast city encodes a conserved protein that is essential for myoblast fusion, dorsal closure, and cytoskeletal organization. J. Cell Biol. 138:589-603. http://dx.doi.org/10.1083/jcb.138.3.589
25. Eswaran, J., M. Soundararajan, R. Kumar, and S. Knapp. 2008. UnPAKing the class differences among p21-activated kinases. Trends Biochem. Sci. 33:394-403. http://dx.doi.org/10.1016/j.tibs.2008.06.002
26. Galletta, B.J., M. Chakravarti, R. Banerjee, and S.M. Abmayr. 2004. SNS: adhesive properties, localization requirements and ectodomain dependence in S2 cells and embryonic myoblasts. Mech. Dev. 121:1455-1468. http://dx.doi.org/10.1016/j.mod.2004.08.001
27. Gatti, A., Z. Huang, P.T. Tuazon, and J.A. Traugh. 1999. Multisite autophosphorylation of p21-activated protein kinase gamma-PAK as a function of activation. J. Biol. Chem. 274:8022-8028. http://dx.doi.org/10.1074/jbc.274.12.8022
28. Geisbrecht, E.R., S. Haralalka, S.K. Swanson, L. Florens, M.P. Washburn, and S.M. Abmayr. 2008. Drosophila ELMO/CED-12 interacts with Myoblast city to direct myoblast fusion and ommatidial organization. Dev. Biol. 314:137-149. http://dx.doi.org/10.1016/j.ydbio.2007.11.022
29. Gildor, B., R. Massarwa, B.Z. Shilo, and E.D. Schejter. 2009. The SCAR and WASp nucleation-promoting factors act sequentially to mediate Drosophila myoblast fusion. EMBO Rep. 10:1043-1050. http://dx.doi.org/10.1038/embor.2009.129
30. Gringel, A., D. Walz, G. Rosenberger, A. Minden, K. Kutsche, P. Kopp, and S. Linder. 2006. PAK4 and alphaPIX determine podosome size and number in macrophages through localized actin regulation. J. Cell. Physiol. 209:568-579. http://dx.doi.org/10.1002/jcp.20777
31. Hakeda-Suzuki, S., J. Ng, J. Tzu, G. Dietzl, Y. Sun, M. Harms, T. Nardine, L. Luo, and B.J. Dickson. 2002. Rac function and regulation during Drosophila development. Nature. 416:438-442. http://dx.doi.org/10.1038/416438a
32. Haralalka, S., C. Shelton, H.N. Cartwright, E. Katzfey, E. Janzen, and S.M. Abmayr. 2011. Asymmetric Mbc, active Rac1 and F-actin foci in the fusion-competent myoblasts during myoblast fusion in Drosophila. Development. 138:1551-1562. http://dx.doi.org/10.1242/dev.057653
33. Harden, N., J. Lee, H.Y. Loh, Y.M. Ong, I. Tan, T. Leung, E. Manser, and L. Lim. 1996. A Drosophila homolog of the Racand Cdc42-activated serine/threonine kinase PAK is a potential focal adhesion and focal complex protein that colocalizes with dynamic actin structures. Mol. Cell. Biol. 16:1896-1908.
34. Hing, H., J. Xiao, N. Harden, L. Lim, and S.L. Zipursky. 1999. Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell. 97:853-863. http://dx.doi.org/10.1016/S0092-8674(00)80798-9
35. Hsu, R.M., M.H. Tsai, Y.J. Hsieh, P.C. Lyu, and J.S. Yu. 2010. Identification of MYO18A as a novel interacting partner of the PAK2/betaPIX/GIT1 complex and its potential function in modulating epithelial cell migration. Mol. Biol. Cell. 21:287-301. http://dx.doi.org/10.1091/mbc.E09-03-0232
36. Hummel, T., K. Leifker, and C. Klämbt. 2000. The Drosophila HEM-2/NAP1 homolog KETTE controls axonal pathfinding and cytoskeletal organization. Genes Dev. 14:863-873.
37. Jin, P., R. Duan, F. Luo, G. Zhang, S.N. Hong, and E.H. Chen. 2011. Competition between Blown fuse and WASP for WIP binding regulates the dynamics of WASP-dependent actin polymerization in vivo. Dev. Cell. 20:623638. http://dx.doi.org/10.1016/j.devcel.2011.04.007
38. Kesper, D.A., C. Stute, D. Buttgereit, N. Kreisköther, S. Vishnu, K.F. Fischbach, and R. Renkawitz-Pohl. 2007. Myoblast fusion in Drosophila melanogaster is mediated through a fusion-restricted myogenic-adhesive structure (FuRMAS). Dev. Dyn. 236:404-415. http://dx.doi.org/10.1002/dvdy.21035
39. Kiehart, D.P., and R. Feghali. 1986. Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol. 103:1517-1525. http://dx.doi.org/10.1083/jcb.103.4.1517
40. Kim, S., K. Shilagardi, S. Zhang, S.N. Hong, K.L. Sens, J. Bo, G.A. Gonzalez, and E.H. Chen. 2007. A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev. Cell. 12:571-586. http://dx.doi.org/10.1016/j.devcel.2007.02.019
41. Kocherlakota, K.S., J.M. Wu, J. McDermott, and S.M. Abmayr. 2008. Analysis of the cell adhesion molecule sticks-and-stones reveals multiple redundant functional domains, protein-interaction motifs and phosphorylated tyrosines that direct myoblast fusion in Drosophila melanogaster. Genetics. 178:1371-1383. http://dx.doi.org/10.1534/genetics.107.083808
42. Lei, M., W. Lu, W. Meng, M.C. Parrini, M.J. Eck, B.J. Mayer, and S.C. Harrison. 2000. Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell. 102:387-397. http://dx.doi.org/10.1016/S0092-8674(00)00043-X
43. Massarwa, R., S. Carmon, B.Z. Shilo, and E.D. Schejter. 2007. WIP/WASpbased actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev. Cell. 12:557-569. http://dx.doi.org/10.1016/j.devcel.2007.01.016
44. Menon, S.D., and W. Chia. 2001. Drosophila rolling pebbles: a multidomain protein required for myoblast fusion that recruits D-Titin in response to the myoblast attractant Dumbfounded. Dev. Cell. 1:691-703. http://dx.doi.org/10.1016/S1534-5807(01)00075-2
45. Mentzel, B., and T. Raabe. 2005. Phylogenetic and structural analysis of the Drosophila melanogaster p21-activated kinase DmPAK3. Gene. 349:2533. http://dx.doi.org/10.1016/j.gene.2004.12.030
46. Molli, P.R., D.Q. Li, B.W. Murray, S.K. Rayala, and R. Kumar. 2009. PAK signaling in oncogenesis. Oncogene. 28:2545-2555. http://dx.doi.org/10.1038/onc.2009.119
47. Morita, T., T. Mayanagi, T. Yoshio, and K. Sobue. 2007. Changes in the balance between caldesmon regulated by p21-activated kinases and the Arp2/3 complex govern podosome formation. J. Biol. Chem. 282:8454-8463. http://dx.doi.org/10.1074/jbc.M609983200
48. Morreale, A., M. Venkatesan, H.R. Mott, D. Owen, D. Nietlispach, P.N. Lowe, and E.D. Laue. 2000. Structure of Cdc42 bound to the GTPase binding domain of PAK. Nat. Struct. Biol. 7:384-388. http://dx.doi.org/10.1038/75158
49. Nguyen, H.T., R. Bodmer, S.M. Abmayr, J.C. McDermott, and N.A. Spoerel. 1994. D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryogenesis. Proc. Natl. Acad. Sci. USA. 91:7520-7524. http://dx.doi.org/10.1073/pnas.91.16.7520
50. Ozdowski, E.F., S. Gayle, H. Bao, B. Zhang, and N.T. Sherwood. 2011. Loss of Drosophila melanogaster p21-activated kinase 3 suppresses defects in synapse structure and function caused by spastin mutations. Genetics. 189:123-135. http://dx.doi.org/10.1534/genetics.111.130831
51. Parks, A.L., K.R. Cook, M. Belvin, N.A. Dompe, R. Fawcett, K. Huppert, L.R. Tan, C.G. Winter, K.P. Bogart, J.E. Deal, et al. 2004. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36:288-292. http://dx.doi.org/10.1038/ng1312
52. Parrini, M.C., M. Lei, S.C. Harrison, and B.J. Mayer. 2002. Pak1 kinase homodimers are autoinhibited in trans and dissociated upon activation by Cdc42 and Rac1. Mol. Cell. 9:73-83. http://dx.doi.org/10.1016/S1097-2765(01)00428-2
53. Paululat, A., A. Holz, and R. Renkawitz-Pohl. 1999. Essential genes for myoblast fusion in Drosophila embryogenesis. Mech. Dev. 83:17-26. http://dx.doi.org/10.1016/S0925-4773(99)00029-5
54. Pirruccello, M., H. Sondermann, J.G. Pelton, P. Pellicena, A. Hoelz, J. Chernoff, D.E. Wemmer, and J. Kuriyan. 2006. A dimeric kinase assembly underlying autophosphorylation in the p21 activated kinases. J. Mol. Biol. 361:312-326. http://dx.doi.org/10.1016/j.jmb.2006.06.017
55. Richardson, B.E., K. Beckett, S.J. Nowak, and M.K. Baylies. 2007. SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development. 134:4357-4367. http://dx.doi.org/10.1242/dev.010678
56. Rochlin, K., S. Yu, S. Roy, and M.K. Baylies. 2010. Myoblast fusion: when it takes more to make one. Dev. Biol. 341:66-83. http://dx.doi.org/10.1016/j.ydbio.2009.10.024
57. Ruiz-Gómez, M., N. Coutts, A. Price, M.V. Taylor, and M. Bate. 2000. Drosophila dumbfounded: a myoblast attractant essential for fusion. Cell. 102:189-198. http://dx.doi.org/10.1016/S0092-8674(00)00024-6
58. Rushton, E., R. Drysdale, S.M. Abmayr, A.M. Michelson, and M. Bate. 1995. Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development. 121:1979-1988.
59. Schäfer, G., S. Weber, A. Holz, S. Bogdan, S. Schumacher, A. Müller, R. Renkawitz-Pohl, and S.F. Onel. 2007. The Wiskott-Aldrich syndrome protein (WASP) is essential for myoblast fusion in Drosophila. Dev. Biol. 304:664-674. http://dx.doi.org/10.1016/j.ydbio.2007.01.015
60. Schneeberger, D., and T. Raabe. 2003. Mbt, a Drosophila PAK protein, combines with Cdc42 to regulate photoreceptor cell morphogenesis. Development. 130:427-437. http://dx.doi.org/10.1242/dev.00248
61. Schröter, R.H., S. Lier, A. Holz, S. Bogdan, C. Klämbt, L. Beck, and R. Renkawitz-Pohl. 2004. kette and blown fuse interact genetically during the second fusion step of myogenesis in Drosophila. Development. 131:4501-4509. http://dx.doi.org/10.1242/dev.01309
62. Sens, K.L., S. Zhang, P. Jin, R. Duan, G. Zhang, F. Luo, L. Parachini, and E.H. Chen. 2010. An invasive podosome-like structure promotes fusion pore formation during myoblast fusion. J. Cell Biol. 191:1013-1027. http://dx.doi.org/10.1083/jcb.201006006
63. Shelton, C., K.S. Kocherlakota, S. Zhuang, and S.M. Abmayr. 2009. The immunoglobulin superfamily member Hbs functions redundantly with Sns in interactions between founder and fusion-competent myoblasts. Development. 136:1159-1168. http://dx.doi.org/10.1242/dev.026302
64. Stofega, M.R., L.C. Sanders, E.M. Gardiner, and G.M. Bokoch. 2004. Constitutive p21-activated kinase (PAK) activation in breast cancer cells as a result of mislocalization of PAK to focal adhesions. Mol. Biol. Cell. 15:2965-2977. http://dx.doi.org/10.1091/mbc.E03-08-0604
65. Strünkelnberg, M., B. Bonengel, L.M. Moda, A. Hertenstein, H.G. de Couet, R.G. Ramos, and K.F. Fischbach. 2001. rst and its paralogue kirre act redundantly during embryonic muscle development in Drosophila. Development. 128:4229-4239.
66. Tang, Y., Z. Chen, D. Ambrose, J. Liu, J.B. Gibbs, J. Chernoff, and J. Field. 1997. Kinase-deficient Pak1 mutants inhibit Ras transformation of Rat-1 fibroblasts. Mol. Cell. Biol. 17:4454-4464.
67. Thompson, G., D. Owen, P.A. Chalk, and P.N. Lowe. 1998. Delineation of the Cdc42/Rac-binding domain of p21-activated kinase. Biochemistry. 37:7885-7891. http://dx.doi.org/10.1021/bi980140+
68. Vadlamudi, R.K., and R. Kumar. 2003. P21-activated kinases in human cancer. Cancer Metastasis Rev. 22:385-393. http://dx.doi.org/10.1023/A:1023729130497
69. Vadlamudi, R.K., L. Adam, R.A. Wang, M. Mandal, D. Nguyen, A. Sahin, J. Chernoff, M.C. Hung, and R. Kumar. 2000. Regulatable expression of p21-activated kinase-1 promotes anchorage-independent growth and abnormal organization of mitotic spindles in human epithelial breast cancer cells. J. Biol. Chem. 275:36238-36244. http://dx.doi.org/10.1074/jbc.M002138200
70. Weaver, A.M. 2006. Invadopodia: specialized cell structures for cancer invasion. Clin. Exp. Metastasis. 23:97-105. http://dx.doi.org/10.1007/s10585-006-9014-1
71. Webb, B.A., R. Eves, S.W. Crawley, S. Zhou, G.P. Côté, and A.S. Mak. 2005. PAK1 induces podosome formation in A7r5 vascular smooth muscle cells in a PAK-interacting exchange factor-dependent manner. Am. J. Physiol. Cell Physiol. 289:C898-C907. http://dx.doi.org/10.1152/ajpcell.00095.2005
72. Whale, A., F.N. Hashim, S. Fram, G.E. Jones, and C.M. Wells. 2011. Signalling to cancer cell invasion through PAK family kinases. Front. Biosci. 16:849-864. http://dx.doi.org/10.2741/3724
73. Zallen, J.A., Y. Cohen, A.M. Hudson, L. Cooley, E. Wieschaus, and E.D. Schejter. 2002. SCAR is a primary regulator of Arp2/3-dependent morphological events in Drosophila. J. Cell Biol. 156:689-701. http://dx.doi.org/10.1083/jcb.200109057
74. Zhang, S., and E.H. Chen. 2008. Ultrastructural analysis of myoblast fusion in Drosophila. In Cell Fusion: Overviews and Methods. E.H. Chen, editor. Humana Press, NJ. 275-297.
75. Zhao, Z.S., E. Manser, X.Q. Chen, C. Chong, T. Leung, and L. Lim. 1998. A conserved negative regulatory region in alphaPAK: inhibition of PAK kinases reveals their morphological roles downstream of Cdc42 and Rac1. Mol. Cell. Biol. 18:2153-2163.