Constitutively active Myosin Light Chain Kinase alters axon guidance decisions in Drosophila embryos

Developmental Biology

Volumn 249, Issue 2, 2002, Pages 367-381

  Kim, You Seung ^a   Fritz, Janice L ^a   Seneviratne, Ananda K ^a   VanBerkum, Mark F A ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Axon guidance; Calmodulin; Drosophila; Motility; Myosin; Myosin Light Chain Kinase; Repulsion

Indexed keywords

LIGAND; MYOSIN LIGHT CHAIN KINASE; NETRIN; RECEPTOR; SLIT PROTEIN;

ARTICLE; CELL FATE; CENTRAL NERVOUS SYSTEM; EMBRYO; ENZYME ACTIVITY; MUTATION; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

EID: 0036382835     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.2002.0768     Document Type: Article

References (95)

1. Amano, M., Chihara, K., Nakamura, N., Fukata, Y., Yano, T., Shibata, M., Ikebe, M., and Kaibuchi, K. (1998). Myosin II activation promotes neurite retraction during the action of Rho and Rho-kinase. Genes Cells 3, 177-188.
2. Bagchi, I. C., Huang, Q. H., and Means, A. R. (1992a). Identification of amino acids essential for calmodulin binding and activation of smooth muscle myosin light chain kinase. J. Biol. Chem. 267, 3024-3029.
3. Bagchi, I. C., Kemp, B. E., and Means, A. R. (1992b). Intrasteric regulation of myosin light chain kinase: The pseudosubstrate prototope binds to the active site. Mol. Endocrinol. 6, 621-626.
4. Bashaw, G. J., Hu, H., Nobes, C. D., and Goodman, C. S. (2001). A novel Dbl family RhoGEF promotes Rho-dependent axon attraction to the central nervous system midline in Drosophila and overcomes Robo repulsion. J. Cell Biol. 155, 1117-1122.
5. Bashaw, G. J., Kidd, T., Murray, D., Pawson, T., and Goodman, C. S. (2000). Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101, 703-715.
6. Battye, R., Stevens, A., and Jacobs, J. R. (1999). Axon repulsion from the midline of the Drosophila CNS requires slit function. Development 126, 2475-2481.
7. Blake, K. J., Myette, G., and Jack, J. (1998). The products of ribbon and raw are necessary for proper cell shape and cellular localization of nonmuscle myosin in Drosophila. Dev. Biol. 203, 177-188.
8. Bloor, J. W., and Kiehart, D. P. (2001). zipper Nonmuscle myosin-II functions downstream of PS2 integrin in Drosophila myogenesis and is necessary for myofibril formation. Dev. Biol. 239, 215-228.
9. Brand, A. H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
10. Bresnick, A. R. (1999). Molecular mechanisms of nonmuscle myosin-II regulation. Curr. Opin. Cell Biol. 11, 26-33.
11. Brose, K., Bland, K. S., Wang, K. H., Arnott, D., Henzel, W., Goodman, C. S., Tessier-Lavigne, M., and Kidd, T. (1999). Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96, 795-806.
12. Champagne, M. B., Edwards, K. A., Erickson, H. P., and Kiehart, D. P. (2000). Drosophila stretchin-MLCK is a novel member of the Titin/Myosin light chain kinase family. J. Mol. Biol. 300, 759-777.
13. Cheng, S., Geddis, M. S., and Rehder, V. (2002). Local calcium changes regulate the length of growth cone filopodia. J. Neurobiol. 50, 263-275.
14. Daniels, R. H., Hall, P. S., and Bokoch, G. M. (1998). Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J. 17, 754-764.
15. Dharmawardhane, S., Brownson, D., Lennartz, M., and Bokoch, G. M. (1999). Localization of p21-activated kinase 1 (PAK1) to pseudopodia, membrane ruffles, and phagocytic cups in activated human neutrophils. J. Leukoc. Biol. 66, 521-527.
16. Dickson, B. J. (2001). Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11, 103-110.
17. Doe, C. Q., Hiromi, Y., Gehring, W. J., and Goodman, C. S. (1988). Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science 239, 170-175.
18. Edwards, K. A., Chang, X. J., and Kiehart, D. P. (1995). Essential light chain of Drosophila nonmuscle myosin II. J. Muscle Res. Cell Motil. 16, 491-498.
19. Edwards, K. A., and Kiehart, D. P. (1996). Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis. Development 122, 1499-1511.
20. Espindola, F. S., Suter, D. M., Partata, L. B., Cao, T., Wolenski, J. S., Cheney, R. E., King, S. M., and Mooseker, M. S. (2000). The light chain composition of chicken brain myosin-Va: Calmodulin, myosin-II essential light chains, and 8-kDa dynein light chain/ PIN. Cell Motil. Cytoskeleton 47, 269-281.
21. Fournier, A. E., Kalb, R. G., and Strittmatter, S. M. (2000a). Rho GTPases and axonal growth cone collapse. Methods Enzymol. 325, 473-482.
22. Fournier, A. E., Nakamura, F., Kawamoto, S., Goshima, Y., Kalb, R. G., and Strittmatter, S. M. (2000b). Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse. J. Cell Biol. 149, 411-422.
23. Fritz, J. L., and VanBerkum, M. F. (2000). Calmodulin and Son of sevenless dependent signaling pathways regulate midline crossing of axons in the Drosophila CNS. Development 127, 1991-2000.
24. Fukata, Y., Amano, M., and Kaibuchi, K. (2001). Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol. Sci. 22, 32-39.
25. Gallo, G., and Letourneau, P. C. (1999). Axon guidance: A balance of signals sets axons on the right track. Curr. Biol. 9, R490-R492.
26. 2+ binding sites. J. Biol. Chem. 268, 20096-20104.
27. Gomez, T. M., Robles, E., Poo, M., and Spitzer, N. C. (2001). Filopodial calcium transients promote substrate-dependent growth cone turning. Science 291, 1983-1987.
28. Gomez, T. M., and Spitzer, N. C. (1999). In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature 397, 350-355.
29. Gomez, T. M., and Spitzer, N. C. (2000). Regulation of growth cone behavior by calcium: New dynamics to earlier perspectives. J. Neurobiol. 44, 174-183.
30. Hall, A., and Nobes, C. D. (2000). Rho GTPases: Molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 965-970.
31. Harris, R., Sabatelli, L. M., and Seeger, M. A. (1996). Guidance cues at the Drosophila CNS midline: Identification and characterization of two Drosophila Netrin/UNC-6 homologs. Neuron 17, 217-228.
32. Hidalgo, A., and Brand, A. H. (1997). Targeted neuronal ablation: the role of pioneer neurons in guidance and fasciculation in the CNS of Drosophila. Development 124, 3253-3262.
33. Hiramoto, M., Hiromi, Y., Giniger, E., and Hotta, Y. (2000). The Drosophila Netrin receptor Frazzled guides axons by controlling Netrin distribution. Nature 406, 886-889.
34. Hirose, M., Ishizaki, T., Watanabe, N., Uehata, M., Kranenburg, O., Moolenaar, W. H., Matsumura, F., Maekawa, M., Bito, H., and Narumiya, S. (1998). Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141, 1625-1636.
35. Homma, K., Saito, J., Ikebe, R., and Ikebe, M. (2000). Ca(2+)-dependent regulation of the motor activity of myosin V. J. Biol. Chem. 275, 34766-34771.
36. Ikebe, M., Stepinska, M., Kemp, B. E., Means, A. R., and Hartshorne, D. J. (1987). Proteolysis of smooth muscle myosin light chain kinase. Formation of inactive and calmodulin-independent fragments. J. Biol. Chem. 262, 13828-13834.
37. Ito, M., Guerriero, V., Jr., Chen, X. M., and Hartshorne, D. J. (1991). Definition of the inhibitory domain of smooth muscle myosin light chain kinase by site-directed mutagenesis. Biochemistry 30, 3498-3503.
38. Jay, D. G. (2000). The clutch hypothesis revisited: Ascribing the roles of actin-associated proteins in filopodial protrusion in the nerve growth cone. J. Neurobiol. 44, 114-125.
39. Jian, X., Hidaka, H., and Schmidt, J. T. (1994). Kinase requirement for retinal growth cone motility. J. Neurobiol. 25, 1310-1328.
40. Jian, X., Szaro, B. G., and Schmidt, J. T. (1996). Myosin light chain kinase: Expression in neurons and upregulation during axon regeneration. J. Neurobiol. 31, 379-391.
41. Jordan, P., and Karess, R. (1997). Myosin light chain-activating phosphorylation sites are required for oogenesis in Drosophila. J. Cell Biol. 139, 1805-1819.
42. Karess, R. E., Chang, X. J., Edwards, K. A., Kulkarni, S., Aguilera, I., and Kiehart, D. P. (1991). The regulatory light chain of non-muscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65, 1177-1189.
43. Kawano, Y., Fukata, Y., Oshiro, N., Amano, M., Nakamura, T., Ito, M., Matsumura, F., Inagaki, M., and Kaibuchi, K. (1999). Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147, 1023-1038.
44. Kemp, B. E., Pearson, R. B., and House, C. M. (1991). Pseudosubstrate-based peptide inhibitors. Methods Enzymol. 201, 287-304.
45. Ketchum, A. S., Stewart, C. T., Stewart, M., and Kiehart, D. P. (1990). Complete sequence of the Drosophila nonmuscle myosin heavy-chain transcript: conserved sequences in the myosin tail and differential splicing in the 5′ untranslated sequence. Proc. Natl. Acad. Sci. USA 87, 6316-6320.
46. Kidd, T., Bland, K. S., and Goodman, C. S. (1999). Slit is the midline repellent for the robo receptor in Drosophila. Cell 96, 785-794.
47. Kidd, T., Brose, K., Mitchell, K. J., Fetter, R. D., Tessier-Lavigne, M., Goodman, C. S., and Tear, G. (1998a). Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92, 205-215.
48. Kidd, T., Russell, C., Goodman, C. S., and Tear, G. (1998b). Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 20, 25-33.
49. Kiehart, D. P., and Feghali, R. (1986). Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol. 103, 1517-1525.
50. Kim, Y. S., Furman, S., Sink, H., and VanBerkum, M. F. (2001). Calmodulin and profilin coregulate axon outgrowth in Drosophila. J. Neurobiol. 47, 26-38.
51. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
52. Kolodziej, P. A., Timpe, L. C., Mitchell, K. J., Fried, S. R., Goodman, C. S., Jan, L. Y., and Jan, Y. N. (1996). frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87, 197-204.
53. Lanier, L. M., and Gertler, F. B. (2000). From Abl to actin: Abl tyrosine kinase and associated proteins in growth cone motility. Curr. Opin. Neurobiol. 10, 80-87.
54. Li, X., Saint-Cyr-Proulx, E., Aktories, K., and Lamarche-Vane, N. (2002). Rac1 and Cdc42 but not RhoA or Rho kinase activities are required for neurite outgrowth induced by the Netrin-1 receptor DCC (Deleted in Colorectal Cancer) in N1E-115 neuroblastoma cells. J. Biol. Chem. 277, 15207-15214.
55. Lin, C. H., Espreafico, E. M., Mooseker, M. S., and Forscher, P. (1996). Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16, 769-782.
56. Lin, C. H., and Forscher, P. (1995). Growth cone advance is inversely proportional to retrograde F-actin flow. Neuron 14, 763-771.
57. Lin, D. M., Fetter, R. D., Kopczynski, C., Grenningloh, G., and Goodman, C. S. (1994). Genetic analysis of Fasciclin II in Drosophila: Defasciculation, refasciculation, and altered fasciculation. Neuron 13, 1055-1069.
58. Machesky, L. M., and Insall, R. H. (1999). Signaling to actin dynamics. J. Cell Biol. 146, 267-272.
59. Mermall, V., Post, P. L., and Mooseker, M. S. (1998). Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279, 527-533.
60. Mitchell, K. J., Doyle, J. L., Serafini, T., Kennedy, T. E., Tessier-Lavigne, M., Goodman, C. S., and Dickson, B. J. (1996). Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17, 203-215.
61. Murray, M. J., and Whitington, P. M. (1999). Effects of roundabout on growth cone dynamics, filopodial length, and growth cone morphology at the midline and throughout the neuropile. J. Neurosci. 19, 7901-7912.
62. Nakamura, F., Kalb, R. G., and Strittmatter, S. M. (2000). Molecular basis of semaphorin-mediated axon guidance. J. Neurobiol. 44, 219-229.
63. Oberstar, J. V., Challacombe, J. F., Roche, F. K., and Letourneau, P. C. (1997). Concentration-dependent stimulation and inhibition of growth cone behavior and neurite elongation by protein kinase inhibitors KT5926 and K-252a. J. Neurobiol. 33, 161-171.
64. Olson, N. J., Pearson, R. B., Needleman, D. S., Hurwitz, M. Y., Kemp, B. E., and Means, A. R. (1990). Regulatory and structural motifs of chicken gizzard myosin light chain kinase. Proc. Natl. Acad. Sci. USA 87, 2284-2288.
65. 2+-sensitive motility. J. Biol. Chem. 275, 21618-21623.
66. Rehder, V., Jensen, J. R., Dou, P., and Kater, S. B. (1991). A comparison of calcium homeostasis in isolated and attached growth cones of the snail Helisoma. J. Neurobiol. 22, 499 -511.
67. Ruchhoeft, M. L., and Harris, W. A. (1997). Myosin functions in Xenopus retinal ganglion cell growth cone motility in vivo. J. Neurobiol. 32, 567-578.
68. Sanders, L. C., Matsumura, F., Bokoch, G. M., and de Lanerolle, P. (1999). Inhibition of myosin light chain kinase by p21-activated kinase. Science 283, 2083-2085.
69. Seeger, M., Tear, G., Ferres-Marco, D., and Goodman, C. S. (1993). Mutations affecting growth cone guidance in Drosophila: Genes necessary for guidance toward or away from the midline. Neuron 10, 409-426.
70. Sellers, J. R. (2000). Myosins: A diverse superfamily. Biochim. Biophys. Acta 1496, 3-22.
71. Shekarabi, M., and Kennedy, T. E. (2002). The netrin-1 receptor DCC promotes filopodia formation and cell spreading by activating Cdc42 and Rac1. Mol. Cell. Neurosci. 19, 1-17.
72. Somlyo, A. P., and Somlyo, A. V. (2000). Signal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J. Physiol. 522, 177-185.
73. Stein, E., and Tessier-Lavigne, M. (2001). Hierarchical organization of guidance receptors: Silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291, 1928-1938.
74. 2+-dependent cell signaling through calmodulin-activated protein phosphatase and protein kinases minireview series. J. Biol. Chem. 276, 2311-2312.
75. Stull, J. T., Lin, P. J., Krueger, J. K., Trewhella, J., and Zhi, G. (1998). Myosin light chain kinase: Functional domains and structural motifs. Acta Physiol. Scand. 164, 471-482.
76. Suter, D. M., Errante, L. D., Belotserkovsky, V., and Forscher, P. (1998). The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J. Cell Biol. 141, 227-240.
77. Suter, D. M., Espindola, F. S., Lin, C. H., Forscher, P., and Mooseker, M. S. (2000). Localization of unconventional myosins V and VI in neuronal growth cones. J. Neurobiol. 42, 370-382.
78. Suter, D. M., and Forscher, P. (2000). Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J. Neurobiol. 44, 97-113.
79. Takano-Ohmuro, H., Takahashi, S., Hirose, G., and Maruyama, K. (1990). Phosphorylated and dephosphorylated myosin light chains of Drosophila fly and larva. Comp. Biochem. Physiol. [B] 95, 171-177.
80. Tear, G., Harris, R., Sutaria, S., Kilomanski, K., Goodman, C. S., and Seeger, M. A. (1996). commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 16, 501-514.
81. Tessier-Lavigne, M., and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
82. van Leeuwen, F. N., van Delft, S., Kain, H. E., van der Kammen, R. A., and Collard, J. G. (1999). Rac regulates phosphorylation of the myosin-II heavy chain, actinomyosin disassembly and cell spreading. Nat. Cell Biol. 1, 242-248.
83. VanBerkum, M. F., and Goodman, C. S. (1995). Targeted disruption of Ca(2+)-calmodulin signaling in Drosophila growth cones leads to stalls in axon extension and errors in axon guidance. Neuron 14, 43-56.
84. VanBerkum, M. F., and Means, A. R. (1991). Three amino acid substitutions in domain I of calmodulin prevent the activation of chicken smooth muscle myosin light chain kinase. J. Biol. Chem. 266, 21488-21495.
85. Wang, F. S., Wolenski, J. S., Cheney, R. E., Mooseker, M. S., and Jay, D. G. (1996). Function of myosin-V in filopodial extension of neuronal growth cones. Science 273, 660-663.
86. Welnhofer, E. A., Zhao, L., and Cohan, C. S. (1999). Calcium influx alters actin bundle dynamics and retrograde flow in Helisoma growth cones. J. Neurosci. 19, 7971-7982.
87. Wheatley, S., Kulkarni, S., and Karess, R. (1995). Drosophila non-muscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 121, 1937-1946.
88. Winter, C. G., Wang, B., Ballew, A., Royou, A., Karess, R., Axelrod, J. D., and Luo, L. (2001). Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81-91.
89. Wong, K., Ren, X. R., Huang, Y. Z., Xie, Y., Liu, G., Saito, H., Tang, H., Wen, L., Brady-Kalnay, S. M., Mei, L., Wu, J. Y., Xiong, W. C., and Rao, Y. (2001). Signal transduction in neuronal migration: Roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 107, 209-221.
90. Wu, X., Jung, G., and Hammer, J. A., 3rd. (2000). Functions of unconventional myosins. Curr. Opin. Cell Biol. 12, 42-51.
91. Wylie, S. R., Wu, P. J., Patel, H., and Chantler, P. D. (1998). A conventional myosin motor drives neurite outgrowth. Proc. Natl. Acad. Sci. USA 95, 12967-12972.
92. Young, P. E., Pesacreta, T. C., and Kiehart, D. P. (1991). Dynamic changes in the distribution of cytoplasmic myosin during Drosophila embryogenesis. Development 111, 1-14.
93. Young, P. E., Richman, A. M., Ketchum, A. S., and Kiehart, D. P. (1993). Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 7, 29-41.
94. Zhao, D. B., Cote, S., Jahnig, F., Haller, J., and Jackle, H. (1988). Zipper encodes a putative integral membrane protein required for normal axon patterning during Drosophila neurogenesis. EMBO J. 7, 1115-1119.
95. Zhou, F. Q., and Cohan, C. S. (2001). Growth cone collapse through coincident loss of actin bundles and leading edge actin without actin depolymerization. J. Cell Biol. 153, 1071-1084.