The activation of membrane targeted CaMK-II in the zebrafish Kupffer's vesicle is required for left-right asymmetry

Development

Volumn 137, Issue 16, 2010, Pages 2753-2762

  Francescatto, Ludmila ^a   Rothschild, Sarah C ^a   Myers, Alexandra L ^a   Tombes, Robert M ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Asymmetry; Calcium; CaMK II (Camk2); Cilia; Kupffer's vesicle; Nodal

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; MEMBRANE PROTEIN; RYANODINE RECEPTOR 3;

ARTICLE; CALCIUM CELL LEVEL; ENZYME ACTIVATION; ENZYME ACTIVE SITE; GENE ACTIVATION; GENE TARGETING; GENETIC CODE; KUPFFER CELL; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMITE; ZEBRA FISH;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BODY PATTERNING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; ENZYME ACTIVATION; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SOMITES; ZEBRAFISH;

DANIO RERIO;

EID: 77955757542     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.049627     Document Type: Article

References (63)

1. Amack, J. D., Wang, X. and Yost, H. J. (2007). Two T-box genes play independent and cooperative roles to regulate morphogenesis of ciliated Kupffer's vesicle in zebrafish. Dev. Biol. 310, 196-210. (Pubitemid 47483670)
2. Bayer, K. U., Harbers, K. and Schulman, H. (1998). AlphaKAP is an anchoring protein for a novel CaM kinase II isoform in skeletal muscle. EMBO J. 17, 5598-5605. (Pubitemid 28445971)
3. Bendtsen, J. D., Nielsen, H., von Heijne, G. and Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795. (Pubitemid 38829638)
4. Bisgrove, B. W., Snarr, B. S., Emrazian, A. and Yost, H. J. (2005). Polaris and Polycystin-2 in dorsal forerunner cells and Kupffer's vesicle are required for specification of the zebrafish left-right axis. Dev. Biol. 287, 274-288. (Pubitemid 41636764)
5. Bustos, R., Kolen, E. R., Braiterman, L., Baines, A. J., Gorelick, F. S. and Hubbard, A. L. (2001). Synapsin I is expressed in epithelial cells: localization to a unique trans-Golgi compartment. J. Cell Sci. 114, 3695-3704.
6. Chung, W. S. and Stainier, D. Y. (2008). Intra-endodermal interactions are required for pancreatic beta cell induction. Dev. Cell 14, 582-593.
7. Colbran, R. J. (2004). Targeting of calcium/calmodulin-dependent protein kinase II. Biochem. J. 378, 1-16.
8. Easley, C. A., Faison, M. O., Kirsch, T. L., Lee, J. A., Seward, M. E. and Tombes, R. M. (2006). Laminin activates CaMK-II to stabilize nascent embryonic axons. Brain Res. 1092, 59-68.
9. Easley, C. A., Brown, C. M., Horwitz, A. F. and Tombes, R. M. (2008). CaMK-II promotes focal adhesion turnover and cell motility by inducing tyrosine dephosphorylation of FAK and paxillin. Cell Motil. Cytoskeleton 65, 662-674.
10. Easom, R. A. (1999). CaM kinase II: a protein kinase with extraordinary talents germane to insulin exocytosis. Diabetes 48, 675-684.
11. Essner, J. J., Amack, J. D., Nyholm, M. K., Harris, E. B. and Yost, H. J. (2005). Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 132, 1247-1260.
12. Fu, X., Wang, Y., Schetle, N., Gao, H., Putz, M., von Gersdorff, G., Walz, G. and Kramer-Zucker, A. G. (2008). The subcellular localization of TRPP2 modulates its function. J. Am. Soc. Nephrol. 19, 1342-1351.
13. Garic-Stankovic, A., Hernandez, M., Flentke, G. R., Zile, M. H. and Smith, S. M. (2008). A ryanodine receptor-dependent Ca(i)(2+) asymmetry at Hensen's node mediates avian lateral identity. Development 135, 3271-3280.
14. Gherman, A., Davis, E. E. and Katsanis, N. (2006). The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat. Genet. 38, 961-962. (Pubitemid 44325911)
15. Gourronc, F., Ahmad, N., Nedza, N., Eggleston, T. and Rebagliati, M. (2007). Nodal activity around Kupffer's vesicle depends on the T-box transcription factors Notail and Spadetail and on Notch signaling. Dev. Dyn. 236, 2131-2146. (Pubitemid 47293757)
16. Griffith, L. C. (2004). Regulation of calcium/calmodulin-dependent protein kinase II activation by intramolecular and intermolecular interactions. J. Neurosci. 24, 8394-8398. (Pubitemid 39313759)
17. Hashimoto, H., Rebagliati, M., Ahmad, N., Muraoka, O., Kurokawa, T., Hibi, M. and Suzuki, T. (2004). The Cerberus/Dan-family protein Charon is a negative regulator of Nodal signaling during left-right patterning in zebrafish. Development 131, 1741-1753. (Pubitemid 38559842)
18. Hatler, J. M., Essner, J. J. and Johnson, R. G. (2009). A gap junction connexin is required in the vertebrate left-right organizer. Dev. Biol. 336, 183-191.
19. Herrmann, T. L., Morita, C. T., Lee, K. and Kusner, D. J. (2005). Calmodulin kinase II regulates the maturation and antigen presentation of human dendritic cells. J. Leukocyte Biol. 78, 1397-1407. (Pubitemid 41779246)
20. Hirokawa, N., Tanaka, Y., Okada, Y. and Takeda, S. (2006). Nodal flow and the generation of left-right asymmetry. Cell 125, 33-45.
21. 2+/Calmodulin- dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu. Rev. Biochem. 71, 473-510.
22. 2+/calmodulin-dependent protein kinase II. Biochem. J. 364, 593-611.
23. 2+/calmodulin-dependent protein kinase II clustering at synaptic and nonsynaptic sites based on self-association. J. Neurosci. 25, 6971-6983.
24. 2+/Calmodulin-dependent protein kinase II isozyme-specific induction of neurite outgrowth in P19 embryonal carcinoma cells. J. Neurochem. 75, 2380-2391.
25. Jurynec, M. J., Xia, R., Mackrill, J. J., Gunther, D., Crawford, T., Flanigan, K. M., Abramson, J. J., Howard, M. T. and Grunwald, D. J. (2008). Selenoprotein N is required for ryanodine receptor calcium release channel activity in human and zebrafish muscle. Proc. Natl. Acad. Sci. USA 105, 12485-12490.
26. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
27. Kramer-Zucker, A. G., Olale, F., Haycraft, C. J., Yoder, B. K., Schier, A. F. and Drummond, I. A. (2005). Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132, 1907-1921.
28. 2+/Calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 275, 12701-12711.
29. 2+ signaling. Mech. Dev. 106, 61-76.
30. Langenbacher, A. and Chen, J. N. (2008). Calcium signaling: a common thread in vertebrate left-right axis development. Dev. Dyn. 237, 3491-3496.
31. Lantsman, K. and Tombes, R. M. (2005). CaMK-II oligomerization potential determined using CFP/YFP FRET. Biochim. Biophys. Acta 1746, 45-54.
32. Lee, J. D. and Anderson, K. V. (2008). Morphogenesis of the node and notochord: the cellular basis for the establishment and maintenance of left-right asymmetry in the mouse. Dev. Dyn. 237, 3464-3476.
33. Levin, M. and Mercola, M. (1999). Gap junction-mediated transfer of left-right patterning signals in the early chick blastoderm is upstream of Shh asymmetry in the node. Development 126, 4703-4714.
34. Long, S., Ahmad, N. and Rebagliati, M. (2003). The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 130, 2303-2316. (Pubitemid 36722383)
35. 2+/calmodulin- dependent protein kinase (CaMK) in excitation-contraction coupling in the heart. Cardiovasc. Res. 73, 631-640.
36. McGrath, J., Somlo, S., Makova, S., Tian, X. and Brueckner, M. (2003). Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114, 61-73. (Pubitemid 36859841)
37. 2+/calmodulin- dependent protein kinase II phosphorylation of the presynaptic protein synapsin I is persistently increased during long-term potentiation. Proc. Natl. Acad. Sci. USA 93, 15451-15456.
38. Nori, A., Lin, P. J., Cassetti, A., Villa, A., Bayer, K. U. and Volpe, P. (2003). Targeting of alpha-kinase-anchoring protein (alpha KAP) to sarcoplasmic reticulum and nuclei of skeletal muscle. Biochem. J. 370, 873-880. (Pubitemid 36399079)
39. O'Leary, H., Lasda, E. and Bayer, K. U. (2006). CaMKIIbeta association with the actin cytoskeleton is regulated by alternative splicing. Mol. Biol. Cell 17, 4656-4665.
40. Peeters, H. and Devriendt, K. (2006). Human laterality disorders. Eur. J. Med. Genet. 49, 349-362.
41. Pennekamp, P., Karcher, C., Fischer, A., Schweickert, A., Skryabin, B., Horst, J., Blum, M. and Dworniczak, B. (2002). The ion channel polycystin-2 is required for left-right axis determination in mice. Curr. Biol. 12, 938-943. (Pubitemid 34689231)
42. Raya, A., Kawakami, Y., Rodriguez-Esteban, C., Ibanes, M., Rasskin-Gutman, D., Rodriguez-Leon, J., Buscher, D., Feijo, J. A. and Izpisua Belmonte,J. C. (2004). Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature 427, 121-128. (Pubitemid 38094947)
43. 2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 273, 28424-28429.
44. Rothschild, S. C., Lister, J. A. and Tombes, R. M. (2007). Differential expression of CaMK-II genes during early zebrafish embryogenesis. Dev. Dyn. 236, 295-305.
45. 2+/calmodulin-dependent protein kinase II is necessary for zebrafish cardiac and pectoral fin morphogenesis. Dev. Biol. 330, 175-184.
46. Sarmah, B., Latimer, A. J., Appel, B. and Wente, S. R. (2005). Inositol polyphosphates regulate zebrafish left-right asymmetry. Dev. Cell 9, 133-145.
47. Schottenfeld, J., Sullivan-Brown, J. and Burdine, R. D. (2007). Zebrafish curly up encodes a Pkd2 ortholog that restricts left-side-specific expression of southpaw. Development 134, 1605-1615.
48. Seward, M. E., Easley, C. A., 4th, McLeod, J. J., Myers, A. L. and Tombes, R. M. (2008). Flightless-I, a gelsolin family member and transcriptional regulator, preferentially binds directly to activated cytosolic CaMK-II. FEBS Lett. 582, 2489-2495.
49. 2+ flux, PKC, and CaMKII in vertebrate embryos. J. Cell Biol. 161, 769-777.
50. Shiratori, H. and Hamada, H. (2006). The left-right axis in the mouse: from origin to morphology. Development 133, 2095-2104. (Pubitemid 43986120)
51. Shu, X., Huang, J., Dong, Y., Choi, J., Langenbacher, A. and Chen, J. N. (2007). Na,K-ATPase alpha2 and Ncx4a regulate zebrafish left-right patterning. Development 134, 1921-1930.
52. Singh, P., Leddy, J. J., Chatzis, G. J., Salih, M. and Tuana, B. S. (2005). Alternative splicing generates a CaM kinase II beta isoform in myocardium that targets the sarcoplasmic reticulum through a putative alphaKAP and regulates GAPDH. Mol. Cell Biochem. 270, 215-221. (Pubitemid 40425250)
53. Sun, Z., Amsterdam, A., Pazour, G. J., Cole, D. G., Miller, M. S. and Hopkins, N. (2004). A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development 131, 4085-4093. (Pubitemid 39232166)
54. Swulius, M. T. and Waxham, M. N. (2008). Ca(2+)/Calmodulin-dependent protein kinases. Cell. Mol. Life Sci. 65, 2637-2657.
55. Tabin, C. J. and Vogan, K. J. (2003). A two-cilia model for vertebrate left-right axis specification. Genes Dev. 17, 1-6.
56. Tanaka, Y., Okada, Y. and Hirokawa, N. (2005). FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 435, 172-177. (Pubitemid 40685936)
57. 2+/CaM kinase). Cell Growth Differ. 6, 1063-1070.
58. 2+/CaM-dependent protein kinase (CaMK-II) genes. Gene 322, 17-31.
59. Wang, X. and Yost, H. J. (2008). Initiation and propagation of posterior to anterior (PA) waves in zebrafish left-right development. Dev. Dyn. 237, 3640-3547.
60. Westerfield, M. (1993). The Zebrafish Book: a Guide for The Laboratory use of Zebrafish (Brachydanio rerio). Eugene OR: University of Oregon Press.
61. Whitaker, M. (2006). Calcium at fertilization and in early development. Physiol. Rev. 86, 25-88.
62. Yamamoto, M., Mine, N., Mochida, K., Sakai, Y., Saijoh, Y., Meno, C. and Hamada, H. (2003). Nodal signaling induces the midline barrier by activating Nodal expression in the lateral plate. Development 130, 1795-1804. (Pubitemid 36575907)
63. Zalk, R., Lehnart, S. E. and Marks, A. R. (2007). Modulation of the ryanodine receptor and intracellular calcium. Annu. Rev. Biochem. 76, 367-385.