CaMK-II is a PKD2 target that promotes pronephric kidney development and stabilizes cilia

Development

Volumn 138, Issue 16, 2011, Pages 3387-3397

  Rothschild, Sarah C ^c   Francescatto, Ludmila ^c   Drummond, Iain A ^a   Tombes, Robert M ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c NONE

Author keywords

ADPKD; CaMK II; Cilia; Kidney; PKD2; Zebrafish

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II GAMMA 1; CALCIUM ION; POLYCYSTIN 1; POLYCYSTIN 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CILIATED EPITHELIUM; CLOACA; CLOACAL CILIA; CONTROLLED STUDY; EMBRYO; EMBRYONIC STRUCTURES; FOREBRAIN; GENE MUTATION; INNER EAR; KIDNEY; KIDNEY DEVELOPMENT; KIDNEY POLYCYSTIC DISEASE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PRONEPHRIC CELL; PRONEPHRIC CILIA; PRONEPHRIC CYST; PRONEPHRIC DUCT; TISSUE DIFFERENTIATION; ZEBRA FISH;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CARRIER PROTEINS; CILIA; EMBRYO, NONMAMMALIAN; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; POLYCYSTIC KIDNEY DISEASES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; VERTEBRATA;

EID: 79960795931     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.066340     Document Type: Article

References (76)

1. Backs, J., Backs, T., Bezprozvannaya, S., McKinsey, T. A. and Olson, E. N. (2008). Histone deacetylase 4 confers CaM kinase II responsiveness to histone deacetylase 5 by oligomerization. Mol. Cell. Biol. 28, 3437-3445.
2. Bershteyn, M., Atwood, S. X., Woo, W. M., Li, M. and Oro, A. E. (2010). MIM and cortactin antagonism regulates ciliogenesis and hedgehog signaling. Dev. Cell 19, 270-283.
3. 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.
4. Cai, Y., Maeda, Y., Cedzich, A., Torres, V. E., Wu, G., Hayashi, T., Mochizuki, T., Park, J. H., Witzgall, R. and Somlo, S. (1999). Identification and characterization of polycystin-2, the PKD2 gene product. J. Biol. Chem. 274, 28557-28565.
5. Cao, Y., Semanchik, N., Lee, S. H., Somlo, S., Barbano, P. E., Coifman, R. and Sun, Z. (2009). Chemical modifier screen identifies HDAC inhibitors as suppressors of PKD models. Proc. Natl. Acad. Sci. USA 106, 21819-21824.
6. Casuscelli, J., Schmidt, S., DeGray, B., Petri, E. T., Celic, A., Folta-Stogniew, E., Ehrlich, B. E. and Boggon, T. J. (2009). Analysis of the cytoplasmic interaction between polycystin-1 and polycystin-2. Am. J. Physiol. Renal Physiol. 297, F1310-F1315.
7. Cizmecioglu, O., Arnold, M., Bahtz, R., Settele, F., Ehret, L., Haselmann-Weiss, U., Antony, C. and Hoffmann, I. (2010). Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome. J. Cell Biol. 191, 731-739.
8. Clapham, D. E. (2003). TRP channels as cellular sensors. Nature 426, 517-524.
9. Daggett, D. F., Domingo, C. R., Currie, P. D. and Amacher, S. L. (2007). Control of morphogenetic cell movements in the early zebrafish myotome. Dev. Biol. 309, 169-179.
10. Drummond, I. A. (2005). Kidney development and disease in the zebrafish. J. Am. Soc. Nephrol. 16, 299-304.
11. Drummond, I. A., Majumdar, A., Hentschel, H., Elger, M., Solnica-Krezel, L., Schier, A. F., Neuhauss, S. C., Stemple, D. L., Zwartkruis, F., Rangini, Z. et al. (1998). Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 125, 4655-4667.
12. 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.
13. 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.
14. Feng, S., Okenka, G. M., Bai, C. X., Streets, A. J., Newby, L. J., DeChant, B. T., Tsiokas, L., Obara, T. and Ong, A. C. (2008). Identification and functional characterization of an N-terminal oligomerization domain for polycystin-2. J. Biol. Chem. 283, 28471-28479.
15. Fliegauf, M., Benzing, T. and Omran, H. (2007). When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8, 880-893.
16. Francescatto, L., Rothschild, S. C., Myers, A. L. and Tombes, R. M. (2010). The activation of membrane targeted CaMK-II in the zebrafish Kupffer's vesicle is required for left-right asymmetry. Development 137, 2753-2762.
17. Gallagher, A. R., Hoffmann, S., Brown, N., Cedzich, A., Meruvu, S., Podlich, D., Feng, Y., Konecke, V., de Vries, U., Hammes, H. P. et al. (2006). A truncated polycystin-2 protein causes polycystic kidney disease and retinal degeneration in transgenic rats. J. Am. Soc. Nephrol. 17, 2719-2730.
18. Gattone, V. H., 2nd, Chen, N. X., Sinders, R. M., Seifert, M. F., Duan, D., Martin, D., Henley, C. and Moe, S. M. (2009). Calcimimetic inhibits late-stage cyst growth in ADPKD. J. Am. Soc. Nephrol. 20, 1527-1532.
19. Giamarchi, A., Feng, S., Rodat-Despoix, L., Xu, Y., Bubenshchikova, E., Newby, L. J., Hao, J., Gaudioso, C., Crest, M., Lupas, A. N. et al. (2010). A polycystin-2 (TRPP2) dimerization domain essential for the function of heteromeric polycystin complexes. EMBO J. 29, 1176-1191.
20. Hanaoka, K., Qian, F., Boletta, A., Bhunia, A. K., Piontek, K., Tsiokas, L., Sukhatme, V. P., Guggino, W. B. and Germino, G. G. (2000). Co-assembly of polycystin-1 and-2 produces unique cation-permeable currents. Nature 408, 990-994.
21. Hatch, E. M., Kulukian, A., Holland, A. J., Cleveland, D. W. and Stearns, T. (2010). Cep152 interacts with Plk4 and is required for centriole duplication. J. Cell Biol. 191, 721-729.
22. Holmfeldt, P., Zhang, X., Stenmark, S., Walczak, C. E. and Gullberg, M. (2005). CaMKIIgamma-mediated inactivation of the Kin I kinesin MCAK is essential for bipolar spindle formation. EMBO J. 24, 1256-1266.
23. Hudmon, A. and Schulman, H. (2002). Neuronal Ca2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu. Rev. Biochem. 71, 473-510.
24. Hudmon, A., Lebel, E., Roy, H., Sik, A., Schulman, H., Waxham, M. N. and De Koninck, P. (2005). A mechanism for Ca2+/calmodulin-dependent protein kinase II clustering at synaptic and nonsynaptic sites based on self-association. J. Neurosci. 25, 6971-6983.
25. Israeli, S., Amsler, K., Zheleznova, N. and Wilson, P. D. (2010). Abnormalities in focal adhesion complex formation, regulation, and function in human autosomal recessive polycystic kidney disease epithelial cells. Am. J. Physiol. Cell Physiol. 298, C831-C846.
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. Kühl, M., Sheldahl, L., Malbon, C. C. and Moon, R. T. (2000). Ca2+/calmodulindependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 275, 12701-12711.
29. Lancaster, M. A. and Gleeson, J. G. (2009). The primary cilium as a cellular signaling center: lessons from disease. Curr. Opin. Genet. Dev. 19, 220-229.
30. Lin, Y. C. and Redmond, L. (2008). CaMKIIbeta binding to stable F-actin in vivo regulates F-actin filament stability. Proc. Natl. Acad. Sci. USA 105, 15791-15796.
31. Little, G. H., Bai, Y., Williams, T. and Poizat, C. (2007). Nuclear calcium/calmodulin-dependent protein kinase IIdelta preferentially transmits signals to histone deacetylase 4 in cardiac cells. J. Biol. Chem. 282, 7219-7231.
32. Liu, J. and Maller, J. L. (2005). Calcium elevation at fertilization coordinates phosphorylation of XErp1/Emi2 by Plx1 and CaMK II to release metaphase arrest by cytostatic factor. Curr. Biol. 15, 1458-1468.
33. Liu, Y., Pathak, N., Kramer-Zucker, A. and Drummond, I. A. (2007). Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros. Development 134, 1111-1122.
34. Lo, S. H., Yu, Q. C., Degenstein, L., Chen, L. B. and Fuchs, E. (1997). Progressive kidney degeneration in mice lacking tensin. J. Cell Biol. 136, 1349-1361.
35. Mably, J. D., Chuang, L. P., Serluca, F. C., Mohideen, M. A., Chen, J. N. and Fishman, M. C. (2006). santa and valentine pattern concentric growth of cardiac myocardium in the zebrafish. Development 133, 3139-3146.
36. Mitra, S. K., Hanson, D. A. and Schlaepfer, D. D. (2005). Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68.
37. Nagao, S., Nishii, K., Yoshihara, D., Kurahashi, H., Nagaoka, K., Yamashita, T., Takahashi, H., Yamaguchi, T., Calvet, J. P. and Wallace, D. P. (2008). Calcium channel inhibition accelerates polycystic kidney disease progression in the Cy/+ rat. Kidney Int. 73, 269-277.
38. Obara, T., Mangos, S., Liu, Y., Zhao, J., Wiessner, S., Kramer-Zucker, A. G., Olale, F., Schier, A. F. and Drummond, I. A. (2006). Polycystin-2 immunolocalization and function in zebrafish. J. Am. Soc. Nephrol. 17, 2706-2718.
39. Okamoto, K., Narayanan, R., Lee, S. H., Murata, K. and Hayashi, Y. (2007). The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure. Proc. Natl. Acad. Sci. USA 104, 6418-6423.
40. 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.
41. Piao, T., Luo, M., Wang, L., Guo, Y., Li, D., Li, P., Snell, W. J. and Pan, J. (2009). A microtubule depolymerizing kinesin functions during both flagellar disassembly and flagellar assembly in Chlamydomonas. Proc. Natl. Acad. Sci. USA 106, 4713-4718.
42. Porter, G. A., Jr, Makuck, R. F. and Rivkees, S. A. (2003). Intracellular calcium plays an essential role in cardiac development. Dev. Dyn. 227, 280-290.
43. Pyati, U. J., Cooper, M. S., Davidson, A. J., Nechiporuk, A. and Kimelman, D. (2006). Sustained Bmp signaling is essential for cloaca development in zebrafish. Development 133, 2275-2284.
44. Qian, F., Germino, F. J., Cai, Y., Zhang, X., Somlo, S. and Germino, G. G. (1997). PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat. Genet. 16, 179-183.
45. Rasmussen, G. and Rasmussen, C. (1995). Calmodulin-dependent protein kinase II is required for G1/S progression in HeLa cells. Biochem. Cell Biol. 73, 201-207.
46. 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.
47. Rothschild, S. C., Easley, C. A., Francescatto, L., Lister, J. A., Garrity, D. M. and Tombes, R. M. (2009). Tbx5-mediated expression of Ca2+/calmodulindependent protein kinase II is necessary for zebrafish cardiac and pectoral fin morphogenesis. Dev. Biol. 330, 175-184.
48. Saarikangas, J., Mattila, P. K., Varjosalo, M., Bovellan, M., Hakanen, J., Calzada-Wack, J., Tost, M., Jennen, L., Rathkolb, B., Hans, W. et al. (2011). Missing-in-metastasis MIM/MTSS1 promotes actin assembly at intercellular junctions and is required for integrity of kidney epithelia. J. Cell Sci. 124, 1245-1255.
49. Sanabria, H., Swulius, M. T., Kolodziej, S. J., Liu, J. and Waxham, M. N. (2009). {beta}CaMKII regulates actin assembly and structure. J. Biol. Chem. 284, 9770-9780.
50. Sawyer, J. M., Harrell, J. R., Shemer, G., Sullivan-Brown, J., Roh-Johnson, M. and Goldstein, B. (2010). Apical constriction: a cell shape change that can drive morphogenesis. Dev. Biol. 341, 5-19.
51. 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.
52. Slanchev, K., Putz, M., Schmitt, A., Kramer-Zucker, A. and Walz, G. (2011). Nephrocystin-4 is required for pronephric duct-dependent cloaca formation in zebrafish. Hum. Mol. Genet. (in press).
53. Sullivan-Brown, J., Schottenfeld, J., Okabe, N., Hostetter, C. L., Serluca, F. C., Thiberge, S. Y. and Burdine, R. D. (2008). Zebrafish mutations affecting cilia motility share similar cystic phenotypes and suggest a mechanism of cyst formation that differs from pkd2 morphants. Dev. Biol. 314, 261-275.
54. 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.
55. Tobimatsu, T. and Fujisawa, H. (1989). Tissue-specific expression of four types of rat calmodulin-dependent protein kinase II mRNAs. J. Biol. Chem. 264, 17907-17912.
56. Tobin, J. L. and Beales, P. L. (2008). Restoration of renal function in zebrafish models of ciliopathies. Pediatr. Nephrol. 23, 2095-2099.
57. Tombes, R. M., Westin, E., Grant, S. and Krystal, G. (1995). G1 cell cycle arrest and apoptosis are induced in NIH 3T3 cells by KN-93, an inhibitor of CaMK-II (the multifunctional Ca2+/CaM kinase). Cell Growth Differ. 6, 1063-1070.
58. Tombes, R. M., Faison, M. O. and Turbeville, C. (2003). Organization and evolution of multifunctional Ca2+/CaM-dependent protein kinase (CaMK-II) genes. Gene 322, 17-31.
59. Torres, V. E., Harris, P. C. and Pirson, Y. (2007). Autosomal dominant polycystic kidney disease. Lancet 369, 1287-1301.
60. Tsiokas, L. (2009). Function and regulation of TRPP2 at the plasma membrane. Am. J. Physiol. Renal Physiol. 297, F1-F9.
61. Tsiokas, L., Kim, E., Arnould, T., Sukhatme, V. P. and Walz, G. (1997). Homoand heterodimeric interactions between the gene products of PKD1 and PKD2. Proc. Natl. Acad. Sci. USA 94, 6965-6970.
62. Vandorpe, D. H., Chernova, M. N., Jiang, L., Sellin, L. K., Wilhelm, S., Stuart-Tilley, A. K., Walz, G. and Alper, S. L. (2001). The cytoplasmic C-terminal fragment of polycystin-1 regulates a Ca2+-permeable cation channel. J. Biol. Chem. 276, 4093-4101.
63. Vasilyev, A., Liu, Y., Mudumana, S., Mangos, S., Lam, P. Y., Majumdar, A., Zhao, J., Poon, K. L., Kondrychyn, I., Korzh, V. et al. (2009). Collective cell migration drives morphogenesis of the kidney nephron. PLoS Biol. 7, e9.
64. Veland, I. R., Awan, A., Pedersen, L. B., Yoder, B. K. and Christensen, S. T. (2009). Primary cilia and signaling pathways in mammalian development, health and disease. Nephron Physiol. 111, p39-p53.
65. Webb, S. E. and Miller, A. L. (2003). Calcium signalling during embryonic development. Nat. Rev. Mol. Cell Biol. 4, 539-551.
66. Webb, S. E. and Miller, A. L. (2007). Ca2+ signalling and early embryonic patterning during zebrafish development. Clin. Exp. Pharmacol. Physiol. 34, 897-904.
67. Whitaker, M. (2006). Calcium at fertilization and in early development. Physiol. Rev. 86, 25-88.
68. Wilson, P. D. (2001). Polycystin: new aspects of structure, function, and regulation. J. Am. Soc. Nephrol. 12, 834-845.
69. Wilson, P. D. (2004). Polycystic kidney disease. N. Engl. J. Med. 350, 151-164.
70. Wilson, P. D. (2008). Mouse models of polycystic kidney disease. Curr. Top. Dev. Biol. 84, 311-350.
71. Wilson, P. D., Geng, L., Li, X. and Burrow, C. R. (1999). The PKD1 gene product, "polycystin-1, " is a tyrosine-phosphorylated protein that colocalizes with alpha2beta1-integrin in focal clusters in adherent renal epithelia. Lab. Invest. 79, 1311-1323.
72. Wingert, R. A. and Davidson, A. J. (2008). The zebrafish pronephros: a model to study nephron segmentation. Kidney Int. 73, 1120-1127.
73. Wingert, R. A., Selleck, R., Yu, J., Song, H. D., Chen, Z., Song, A., Zhou, Y., Thisse, B., Thisse, C., McMahon, A. P. et al. (2007). The cdx genes and retinoic acid control the positioning and segmentation of the zebrafish pronephros. PLoS Genet. 3, 1922-1938.
74. Wu, G., Markowitz, G. S., Li, L., D'Agati, V. D., Factor, S. M., Geng, L., Tibara, S., Tuchman, J., Cai, Y., Park, J. H. et al. (2000). Cardiac defects and renal failure in mice with targeted mutations in Pkd2. Nat. Genet. 24, 75-78.
75. Xia, S., Li, X., Johnson, T., Seidel, C., Wallace, D. P. and Li, R. (2010). Polycystin-dependent fluid flow sensing targets histone deacetylase 5 to prevent the development of renal cysts. Development 137, 1075-1084.
76. Zhang, T., Kohlhaas, M., Backs, J., Mishra, S., Phillips, W., Dybkova, N., Chang, S., Ling, H., Bers, D. M., Maier, L. S. et al. (2007). CaMKIIdelta isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses. J. Biol. Chem. 282, 35078-35087.