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Widespread Roles of CaMK-II in Developmental Pathways

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Calcium Signaling

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1131))

Abstract

The multifunctional Ca2+/calmodulin-dependent protein kinase type 2 (CaMK-II) was first discovered in brain tissue and shown to have a central role in long term potentiation, responding to Ca2+ elevations through voltage dependent channels. CaMK-II has a unique molecular mechanism that enables it to remain active in proportion to the degree (frequency and amplitude) of Ca2+ elevations, long after such elevations have subsided. Ca2+ is also a rapid activator of early development and CaMK-II is expressed and activated in early development. Using biochemical, pharmacological and genetic approaches, the functions of CaMK-II overlap remarkably well with those for Ca2+ elevations, post-fertilization. Conclusion. Activated CaMK-II plays a central role in decoding Ca2+ signals to activate specific events during early development; a majority of the known functions of elevated Ca2+ act though CaMK-II.

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References

  1. Steinhardt R, Zucker R, Schatten G (1977) Intracellular calcium release at fertilization in the sea urchin egg. Dev Biol 58:185–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Gilkey JC, Jaffe LF, Ridgway EB, Reynolds GT (1978) A free calcium wave traverses the activating egg of the medaka, Oryzias Latipes. J Cell Biol 76:448–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ridgway EB, Gilkey JC, Jaffe LF (1977) Free calcium increases explosively in activating medaka eggs. Proc Natl Acad Sci U S A 74:623–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Cuthbertson KSR, Whittingham DG, Cobbold PH (1981) Free Ca2+ increases in exponential phases during mouse oocyte activation. Nature 294:754–757

    Article  CAS  PubMed  Google Scholar 

  5. Whitaker M (2006) Calcium at fertilization and in early development. Physiol Rev 86(1): 25–88

    Article  CAS  PubMed  Google Scholar 

  6. Stricker SA (1999) Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211(2):157–176

    Article  CAS  PubMed  Google Scholar 

  7. Webb SE, Miller AL (2003) Calcium signalling during embryonic development. Nat Rev Mol Cell Biol 4(7):539–551

    Article  CAS  PubMed  Google Scholar 

  8. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1(1):11–21

    Article  CAS  PubMed  Google Scholar 

  9. Tombes RM, Simerly C, Borisy GG, Schatten G (1992) Meiosis, egg activation and nuclear envelope breakdown are differentially reliant on Ca2+, whereas germinal vesicle breakdown is Ca2+-independent in the mouse oocyte. J Cell Biol 117:799–812

    Article  CAS  PubMed  Google Scholar 

  10. Creton R, Speksnijder JE, Jaffe LF (1998) Patterns of free calcium in zebrafish embryos. J Cell Sci 111(Pt 12):1613–1622

    CAS  PubMed  Google Scholar 

  11. Reinhard E, Yokoe H, Niebling KR, Allbritton NL, Kuhn MA, Meyer T (1995) Localized calcium signals in early zebrafish development. Dev Biol 170(1):50–61

    Article  CAS  PubMed  Google Scholar 

  12. Gilland E, Miller AL, Karplus E, Baker R, Webb SE (1999) Imaging of multicellular large-scale rhythmic calcium waves during zebrafish gastrulation. Proc Natl Acad Sci U S A 96(1):157–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kühl M, Sheldahl LC, Park M, Miller JR, Moon RT (2000) The Wnt/Ca2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genetics 16(7):279–283

    Article  Google Scholar 

  14. Lin S, Baye LM, Westfall TA, Slusarski DC (2010) Wnt5b-Ryk pathway provides directional signals to regulate gastrulation movement. J Cell Biol 190(2):263–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Zhu S, Liu L, Korzh V, Gong Z, Low BC (2006) RhoA acts downstream of Wnt5 and Wnt11 to regulate convergence and extension movements by involving effectors Rho kinase and Diaphanous: use of zebrafish as an in vivo model for GTPase signaling. Cell Signal 18(3):359–372

    Article  CAS  PubMed  Google Scholar 

  16. Kilian B, Mansukoski H, Barbosa FC, Ulrich F, Tada M, Heisenberg CP (2003) The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech Dev 120(4):467–476

    Article  CAS  PubMed  Google Scholar 

  17. Moon RT, Campbell RM, Christian JL, McGrew LL, Shih J, Fraser S (1993) Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. Development 119(1):97–111

    CAS  PubMed  Google Scholar 

  18. Matsui T, Raya A, Kawakami Y, Callol-Massot C, Capdevila J, Rodriguez-Esteban C et al (2005) Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev 19(1):164–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Marlow F, Topczewski J, Sepich D, Solnica-Krezel L (2002) Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr Biol 12(11):876–884

    Article  CAS  PubMed  Google Scholar 

  20. Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, Geisler R et al (2000) Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405(6782):76–81

    Article  CAS  PubMed  Google Scholar 

  21. Lele Z, Bakkers J, Hammerschmidt M (2001) Morpholino phenocopies of the swirl, snailhouse, somitabun, minifin, silberblick, and pipetail mutations. Genesis 30(3):190–194

    Article  CAS  PubMed  Google Scholar 

  22. Wallingford JB, Fraser SE, Harland RM (2002) Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev Cell 2(6):695–706

    Article  CAS  PubMed  Google Scholar 

  23. Andre P, Song H, Kim W, Kispert A, Yang Y (2015) Wnt5a and Wnt11 regulate mammalian anterior-posterior axis elongation. Development 142(8):1516–1527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Slusarski DC, Corces VG, Moon RT (1997) Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390(6658):410–413

    Article  CAS  PubMed  Google Scholar 

  25. Kühl M, Sheldahl L, Malbon CC, Moon RT (2000) Ca2+/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

    Article  PubMed  Google Scholar 

  26. Westfall TA, Hjertos B, Slusarski DC (2003) Requirement for intracellular calcium modulation in zebrafish dorsal-ventral patterning. Dev Biol 259(2):380–391

    Article  CAS  PubMed  Google Scholar 

  27. Westfall TA, Brimeyer R, Twedt J, Gladon J, Olberding A, Furutani-Seiki M et al (2003) Wnt-5/pipetail functions in vertebrate axis formation as a negative regulator of Wnt/beta-catenin activity. J Cell Biol 162(5):889–898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Ulrich F, Concha ML, Heid PJ, Voss E, Witzel S, Roehl H et al (2003) Slb/Wnt11 controls hypoblast cell migration and morphogenesis at the onset of zebrafish gastrulation. Development 130(22):5375–5384

    Article  CAS  PubMed  Google Scholar 

  29. Peeters H, Devriendt K (2006) Human laterality disorders. Eur J Med Genet 49(5):349–362

    Article  PubMed  Google Scholar 

  30. Hirokawa N, Tanaka Y, Okada Y, Takeda S (2006) Nodal flow and the generation of left-right asymmetry. Cell 125(1):33–45

    Article  CAS  PubMed  Google Scholar 

  31. Essner JJ, Amack JD, Nyholm MK, Harris EB, Yost HJ (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(6):1247–1260

    Article  CAS  PubMed  Google Scholar 

  32. Kramer-Zucker AG, Olale F, Haycraft CJ, Yoder BK, Schier AF, Drummond IA (2005) Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132(8):1907–1921

    Article  CAS  PubMed  Google Scholar 

  33. Lee JD, Anderson KV (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(12):3464–3476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Bisgrove BW, Snarr BS, Emrazian A, Yost HJ (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(2):274–288

    Article  CAS  PubMed  Google Scholar 

  35. Schottenfeld J, Sullivan-Brown J, Burdine RD (2007) Zebrafish curly up encodes a Pkd2 ortholog that restricts left-side-specific expression of southpaw. Development 134(8): 1605–1615

    Article  CAS  PubMed  Google Scholar 

  36. Tabin CJ, Vogan KJ (2003) A two-cilia model for vertebrate left-right axis specification. Genes Dev 17(1):1–6

    Article  CAS  PubMed  Google Scholar 

  37. McGrath J, Somlo S, Makova S, Tian X, Brueckner M (2003) Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114(1):61–73

    Article  CAS  PubMed  Google Scholar 

  38. Tanaka Y, Okada Y, 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(7039):172–177

    Article  CAS  PubMed  Google Scholar 

  39. Raya A, Kawakami Y, Rodriguez-Esteban C, Ibanes M, Rasskin-Gutman D, Rodriguez-Leon J et al (2004) Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature 427(6970):121–128

    Article  CAS  PubMed  Google Scholar 

  40. Garic-Stankovic A, Hernandez M, Flentke GR, Zile MH, Smith SM (2008) A ryanodine receptor-dependent Ca(i)(2+) asymmetry at Hensen's node mediates avian lateral identity. Development 135(19):3271–3280

    Article  CAS  PubMed  Google Scholar 

  41. Sarmah B, Latimer AJ, Appel B, Wente SR (2005) Inositol polyphosphates regulate zebrafish left-right asymmetry. Dev Cell 9(1):133–145

    Article  CAS  PubMed  Google Scholar 

  42. Jurynec MJ, Xia R, Mackrill JJ, Gunther D, Crawford T, Flanigan KM et al (2008) Selenoprotein N is required for ryanodine receptor calcium release channel activity in human and zebrafish muscle. Proc Natl Acad Sci U S A 105(34):12485–12490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Levin M, 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(21):4703–4714

    CAS  PubMed  Google Scholar 

  44. Hatler JM, Essner JJ, Johnson RG (2009) A gap junction connexin is required in the vertebrate left-right organizer. Dev Biol 336(2):183–191

    Article  CAS  PubMed  Google Scholar 

  45. Fu X, Wang Y, Schetle N, Gao H, Putz M, von Gersdorff G et al (2008) The subcellular localization of TRPP2 modulates its function. J Am Soc Nephrol 19(7):1342–1351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Pennekamp P, Karcher C, Fischer A, Schweickert A, Skryabin B, Horst J et al (2002) The ion channel polycystin-2 is required for left-right axis determination in mice. Curr Biol 12(11):938–943

    Article  CAS  PubMed  Google Scholar 

  47. Webb SE, Miller AL (2000) Calcium signalling during zebrafish embryonic development. BioEssays 22(2):113–123

    Article  CAS  PubMed  Google Scholar 

  48. Ferrari MB, Spitzer NC (1999) Calcium signaling in the developing Xenopus myotome. Dev Biol 213(2):269–282

    Article  CAS  PubMed  Google Scholar 

  49. Porter GA Jr, Makuck RF, Rivkees SA (2003) Intracellular calcium plays an essential role in cardiac development. Dev Dyn 227(2):280–290

    Article  CAS  PubMed  Google Scholar 

  50. Ebert AM, Hume GL, Warren KS, Cook NP, Burns CG, Mohideen MA et al (2005) Calcium extrusion is critical for cardiac morphogenesis and rhythm in embryonic zebrafish hearts. Proc Natl Acad Sci U S A 102(49):17705–17710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Leclerc C, Webb SE, Miller AL, Moreau M (2008) An increase in intracellular Ca2+ is involved in pronephric tubule differentiation in the amphibian Xenopus laevis. Dev Biol 321(2):357–367

    Article  CAS  PubMed  Google Scholar 

  52. Lam PY, Webb SE, Leclerc C, Moreau M, Miller AL (2009) Inhibition of stored Ca2+ release disrupts convergence-related cell movements in the lateral intermediate mesoderm resulting in abnormal positioning and morphology of the pronephric anlagen in intact zebrafish embryos. Develop Growth Differ 51(4):429–442

    Article  CAS  Google Scholar 

  53. Stooke-Vaughan GA, Huang P, Hammond KL, Schier AF, Whitfield TT (2012) The role of hair cells, cilia and ciliary motility in otolith formation in the zebrafish otic vesicle. Development 139(10):1777–1787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Colantonio JR, Vermot J, Wu D, Langenbacher AD, Fraser S, Chen JN et al (2009) The dynein regulatory complex is required for ciliary motility and otolith biogenesis in the inner ear. Nature 457(7226):205–209

    Article  CAS  PubMed  Google Scholar 

  55. Amato V, Vina E, Calavia MG, Guerrera MC, Laura R, Navarro M et al (2012) TRPV4 in the sensory organs of adult zebrafish. Microsc Res Tech 75(1):89–96

    Article  CAS  PubMed  Google Scholar 

  56. Corey DP (2006) What is the hair cell transduction channel? J Physiol 576(Pt 1):23–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Shin JB, Adams D, Paukert M, Siba M, Sidi S, Levin M et al (2005) Xenopus TRPN1 (NOMPC) localizes to microtubule-based cilia in epithelial cells, including inner-ear hair cells. Proc Natl Acad Sci U S A 102(35):12572–12577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301(5629):96–99

    Article  CAS  PubMed  Google Scholar 

  59. Hudmon A, 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

    Article  CAS  PubMed  Google Scholar 

  60. Tobimatsu T, Fujisawa H (1989) Tissue-specific expression of four types of rat calmodulin-dependent protein kinase II mRNAs. J Biol Chem 264:17907–17912

    CAS  PubMed  Google Scholar 

  61. Tombes RM, Faison MO, Turbeville C (2003) Organization and evolution of multifunctional Ca2+/CaM-dependent protein kinase (CaMK-II) genes. Gene 322:17–31

    Article  CAS  PubMed  Google Scholar 

  62. Swulius MT, Waxham MN (2008) Ca(2+)/calmodulin-dependent protein kinases. Cell Mol Life Sci 65(17):2637–2657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Rothschild SC, Francescatto L, Tombes RM (2016) Immunostaining phospho-epitopes in ciliated organs of whole mount zebrafish embryos. J Visual Exp JoVE 108:53747

    Google Scholar 

  64. Francescatto L, Rothschild SC, Myers AL, Tombes RM (2010) The activation of membrane targeted CaMK-II in the zebrafish Kupffer's vesicle is required for left-right asymmetry. Development 137(16):2753–2762

    Article  CAS  PubMed  Google Scholar 

  65. Rothschild SC, Francescatto L, Drummond IA, Tombes RM (2011) CaMK-II is a PKD2 target that promotes pronephric kidney development and stabilizes cilia. Development 138(16):3387–3397

    Article  CAS  PubMed  Google Scholar 

  66. Rothschild SC, Lister JA, Tombes RM (2007) Differential expression of CaMK-II genes during early zebrafish embryogenesis. Dev Dyn 236(1):295–305

    Article  CAS  PubMed  Google Scholar 

  67. Lou L, Schulman H (1989) Distinct autophosphorylation sites sequantially produce autonomy and inhibition of the multifunctional Ca2+/calmodulin-dependent protein kinase. J Neurosci 9(6):2020–2032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Hoffman A, Carpenter H, Kahl R, Watt LF, Dickson PW, Rostas JA et al (2014) Dephosphorylation of CaMKII at T253 controls the metaphase-anaphase transition. Cell Signal 26(4):748–756

    Article  CAS  PubMed  Google Scholar 

  69. Tombes RM, Grant S, Westin EH, 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(9):1063–1070

    CAS  PubMed  Google Scholar 

  70. Rasmussen G, Rasmussen C (1995) Calmodulin-dependent protein kinase II is required for G1/S progression in HeLa cells. Biochem Cell Biol 73:201–207

    Article  CAS  PubMed  Google Scholar 

  71. Rothschild SC, Lahvic J, Francescatto L, McLeod JJ, Burgess SM, Tombes RM (2013) CaMK-II activation is essential for zebrafish inner ear development and acts through Delta-Notch signaling. Dev Biol 381(1):179–188

    Article  CAS  PubMed  Google Scholar 

  72. Gardner AJ, Knott JG, Jones KT, Evans JP (2007) CaMKII can participate in but is not sufficient for the establishment of the membrane block to polyspermy in mouse eggs. J Cell Physiol 212(2):275–280

    Article  CAS  PubMed  Google Scholar 

  73. Morin N, Abrieu A, Lorca T, Martin F, Dorée M (1994) The proteolysis-dependent metaphase to anaphase transition: calcium/calmodulin-dependent protein kinase II mediates onset of anaphase in extracts prepared from unfertilized Xenopus eggs. EMBO J 13(18):4343–4352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Dupont G (1998) Link between fertilization-induced Ca2+ oscillations and relief from metaphase II arrest in mammalian eggs: a model based on calmodulin-dependent kinase II activation. Biophys Chem 72(1–2):153–167

    Article  CAS  PubMed  Google Scholar 

  75. Tatone C, Iorio R, Francione A, Gioia L, Colonna R (1999) Biochemical and biological effects of KN-93, an inhibitor of calmodulin-dependent protein kinase II, on the initial events of mouse egg activation induced by ethanol. J Reprod Fertil 115(1):151–157

    Article  CAS  PubMed  Google Scholar 

  76. Backs J, Stein P, Backs T, Duncan FE, Grueter CE, McAnally J et al (2010) The gamma isoform of CaM kinase II controls mouse egg activation by regulating cell cycle resumption. Proc Natl Acad Sci U S A 107(1):81–86

    Article  CAS  PubMed  Google Scholar 

  77. Chang HY, Minahan K, Merriman JA, Jones KT (2009) Calmodulin-dependent protein kinase gamma 3 (CamKIIgamma3) mediates the cell cycle resumption of metaphase II eggs in mouse. Development 136(24):4077–4081

    Article  CAS  PubMed  Google Scholar 

  78. Silva A, Stevens C, Tonegawa S, Wang Y (1992) Deficient hippocampal long term-potentiation in a-calcium-calmodulin kinase II mutant mice. Science 257:201–206

    Article  CAS  PubMed  Google Scholar 

  79. Silva AJ, Paylor R, Wehner JM, Tonegawa S (1992) Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257(5067):206–211

    Article  CAS  PubMed  Google Scholar 

  80. van Woerden GM, Hoebeek FE, Gao Z, Nagaraja RY, Hoogenraad CC, Kushner SA et al (2009) betaCaMKII controls the direction of plasticity at parallel fiber-Purkinje cell synapses. Nat Neurosci 12:823–825

    Article  PubMed  CAS  Google Scholar 

  81. Backs J, Backs T, Neef S, Kreusser MM, Lehmann LH, Patrick DM et al (2009) The delta isoform of CaM kinase II is required for pathological cardiac hypertrophy and remodeling after pressure overload. Proc Natl Acad Sci U S A 106(7):2342–2347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Liu J, Maller JL (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(16):1458–1468

    Article  CAS  PubMed  Google Scholar 

  83. Hansen DV, Tung JJ, Jackson PK (2006) CaMKII and polo-like kinase 1 sequentially phosphorylate the cytostatic factor Emi2/XErp1 to trigger its destruction and meiotic exit. Proc Natl Acad Sci U S A 103(3):608–613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Tombes RM, Peppers LS (1995) Sea urchin fertilization stimulates CaM kinase-II (multifunctional (type II) Ca2+/CaM Kinase) activity and association with p34cdc2. Dev Growth Differ 37(5):589–596

    Article  CAS  Google Scholar 

  85. Creton R (2004) The calcium pump of the endoplasmic reticulum plays a role in midline signaling during early zebrafish development. Brain Res Dev Brain Res 151(1–2):33–41

    Article  CAS  PubMed  Google Scholar 

  86. Kohn AD, Moon RT (2005) Wnt and calcium signaling: beta-catenin-independent pathways. Cell Calcium 38(3–4):439–446

    Article  CAS  PubMed  Google Scholar 

  87. Pfleiderer PJ, Lu KK, Crow MT, Keller RS, Singer HA (2004) Modulation of vascular smooth muscle cell migration by calcium/calmodulin-dependent protein kinase II-delta 2. Am J Physiol Cell Physiol 286(6):C1238–C1245

    Article  CAS  PubMed  Google Scholar 

  88. Bilato C, Curto KA, Monticone RE, Pauly RR, White AJ, Crow MT (1997) The inhibition of vascular smooth muscle cell migration by peptide and antibody antagonists of the alphavbeta3 integrin complex is reversed by activated calcium/calmodulin- dependent protein kinase II. J Clin Invest 100(3):693–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Bouvard D, Block MR (1998) Calcium/calmodulin-dependent protein kinase II controls integrin alpha5beta1-mediated cell adhesion through the integrin cytoplasmic domain associated protein-1alpha. Biochem Biophys Res Commun 252(1):46–50

    Article  CAS  PubMed  Google Scholar 

  90. Lundberg MS, Curto KA, Bilato C, Monticone RE, Crow MT (1998) Regulation of vascular smooth muscle migration by mitogen-activated protein kinase and calcium/calmodulin-dependent protein kinase II signaling pathways. J Mol Cell Cardiol 30(11):2377–2389

    Article  CAS  PubMed  Google Scholar 

  91. Easley CA, Brown CM, Horwitz AF, Tombes RM (2008) CaMK-II promotes focal adhesion turnover and cell motility by inducing tyrosine dephosphorylation of FAK and paxillin. Cell Motil Cytoskeleton 65(8):662–674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Rothschild SC, Easley CA, Francescatto L, Lister JA, Garrity DM, Tombes RM (2009) Tbx5-mediated expression of Ca2+/calmodulin-dependent protein kinase II is necessary for zebrafish cardiac and pectoral fin morphogenesis. Dev Biol 330(1):175–184

    Article  CAS  PubMed  Google Scholar 

  93. Lantsman K, Tombes RM (2005) CaMK-II oligomerization potential determined using CFP/YFP FRET. Biochim Biophys Acta 1746(1):45–54

    Article  CAS  PubMed  Google Scholar 

  94. Webb SE, Miller AL (2006) Ca2+ signaling and early embryonic patterning during the Blastula and Gastrula Periods of Zebrafish and Xenopus development. Biochim Biophys Acta 1763:1192–1208

    Article  CAS  PubMed  Google Scholar 

  95. Kuhl M, Geis K, Sheldahl LC, Pukrop T, Moon RT, Wedlich D (2001) Antagonistic regulation of convergent extension movements in Xenopus by Wnt/beta-catenin and Wnt/Ca2+ signaling. Mech Dev 106(1–2):61–76

    Article  CAS  PubMed  Google Scholar 

  96. Baitinger C, Alderton J, Poenie M, Schulman H, Steinhardt RA (1990) Multifunctional Ca2+/calmodulin-dependent protein kinase is necessary for nuclear envelope breakdown. J Cell Biol 111:1763–1773

    Article  CAS  PubMed  Google Scholar 

  97. Knott JG, Gardner AJ, Madgwick S, Jones KT, Williams CJ, Schultz RM (2006) Calmodulin-dependent protein kinase II triggers mouse egg activation and embryo development in the absence of Ca2+ oscillations. Dev Biol 296(2):388–395

    Article  CAS  PubMed  Google Scholar 

  98. Markoulaki S, Matson S, Ducibella T (2004) Fertilization stimulates long-lasting oscillations of CaMKII activity in mouse eggs. Dev Biol 272(1):15–25

    Article  CAS  PubMed  Google Scholar 

  99. Markoulaki S, Matson S, Abbott AL, Ducibella T (2003) Oscillatory CaMKII activity in mouse egg activation. Dev Biol 258(2):464–474

    Article  CAS  PubMed  Google Scholar 

  100. Johnson J, Bierle BM, Gallicano GI, Capco DG (1998) Calcium/calmodulin-dependent protein kinase II and calmodulin: regulators of the meiotic spindle in mouse eggs. Dev Biol 204(2):464–477

    Article  CAS  PubMed  Google Scholar 

  101. Morris TA, DeLorenzo RJ, Tombes RM (1998) CaMK-II inhibition reduces cyclin D1 levels and enhances the association of p27kip1 with cdk2 to cause G1 arrest in NIH 3T3 cells. Exp Cell Res 240:218–227

    Article  CAS  PubMed  Google Scholar 

  102. Zhu W, Woo AY, Yang D, Cheng H, Crow MT, Xiao RP (2007) Activation of CaMKIIdeltaC is a common intermediate of diverse death stimuli-induced heart muscle cell apoptosis. J Biol Chem 282(14):10833–10839

    Article  CAS  PubMed  Google Scholar 

  103. Hagemann D, Bohlender J, Hoch B, Krause EG, Karczewski P (2001) Expression of Ca2+/calmodulin-dependent protein kinase II delta-subunit isoforms in rats with hypertensive cardiac hypertrophy. Mol Cell Biochem 220(1–2):69–76

    Article  CAS  PubMed  Google Scholar 

  104. Zhang T, Maier LS, Dalton ND, Miyamoto S, Ross J Jr, Bers DM et al (2003) The deltaC isoform of CaMKII is activated in cardiac hypertrophy and induces dilated cardiomyopathy and heart failure. Circ Res 92(8):912–919

    Article  CAS  PubMed  Google Scholar 

  105. Zhang R, Khoo MS, Wu Y, Yang Y, Grueter CE, Ni G et al (2005) Calmodulin kinase II inhibition protects against structural heart disease. Nat Med 11(4):409–417

    Article  CAS  PubMed  Google Scholar 

  106. Grueter CE, Colbran RJ, Anderson ME (2007) CaMKII, an emerging molecular driver for calcium homeostasis, arrhythmias, and cardiac dysfunction. J Mol Med (Berlin, Germany) 85(1):5–14

    Article  CAS  Google Scholar 

  107. Yang Y, Zhu WZ, Joiner ML, Zhang R, Oddis CV, Hou Y et al (2006) Calmodulin kinase II inhibition protects against myocardial cell apoptosis in vivo. Am J Physiol 291(6):H3065–H3075

    CAS  Google Scholar 

  108. Baltas LG, Karczewski P, Krause EG (1995) The cardiac sarcoplasmic reticulum phospholamban kinase is a distinct delta-CaM kinase isozyme. FEBS Lett 373(1):71–75

    Article  CAS  PubMed  Google Scholar 

  109. Grueter CE, Abiria SA, Dzhura I, Wu Y, Ham AJ, Mohler PJ et al (2006) L-type Ca2+ channel facilitation mediated by phosphorylation of the beta subunit by CaMKII. Mol Cell 23(5):641–650

    Article  CAS  PubMed  Google Scholar 

  110. Hudmon A, Schulman H, Kim J, Maltez JM, Tsien RW, Pitt GS (2005) CaMKII tethers to L-type Ca2+ channels, establishing a local and dedicated integrator of Ca2+ signals for facilitation. J Cell Biol 171(3):537–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Lee TS, Karl R, Moosmang S, Lenhardt P, Klugbauer N, Hofmann F et al (2006) Calmodulin kinase II is involved in voltage-dependent facilitation of the L-type Cav1.2 calcium channel: identification of the phosphorylation sites. J Biol Chem 281(35):25560–25567

    Article  CAS  PubMed  Google Scholar 

  112. Zalk R, Lehnart SE, Marks AR (2007) Modulation of the ryanodine receptor and intracellular calcium. Annu Rev Biochem 76:367–385

    Article  CAS  PubMed  Google Scholar 

  113. Backs J, Song K, Bezprozvannaya S, Chang S, Olson EN (2006) CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J Clin Invest 116(7):1853–1864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Little GH, Bai Y, Williams T, Poizat C (2007) Nuclear calcium/calmodulin-dependent protein kinase IIdelta preferentially transmits signals to histone deacetylase 4 in cardiac cells. J Biol Chem 282(10):7219–7231

    Article  CAS  PubMed  Google Scholar 

  115. Rothschild SC, Lee HJ, Ingram SR, Mohammadi DK, Walsh GS, Tombes RM (2018) Calcium signals act through histone deacetylase to mediate pronephric kidney morphogenesis. Dev Dyn 247(6):807–817

    Article  CAS  PubMed  Google Scholar 

  116. Garriock RJ, D'Agostino SL, Pilcher KC, Krieg PA (2005) Wnt11-R, a protein closely related to mammalian Wnt11, is required for heart morphogenesis in Xenopus. Dev Biol 279(1):179–192

    Article  CAS  PubMed  Google Scholar 

  117. Eisenberg CA, Eisenberg LM (1999) WNT11 promotes cardiac tissue formation of early mesoderm. Dev Dyn 216(1):45–58

    Article  CAS  PubMed  Google Scholar 

  118. Pandur P, Lasche M, Eisenberg LM, Kuhl M (2002) Wnt-11 activation of a non-canonical Wnt signaling pathway is required for cardiogenesis. Nature 418(6898):636–641

    Article  CAS  PubMed  Google Scholar 

  119. Fleming IN, Elliott CM, Buchanan FG, Downes CP, Exton JH (1999) Ca2+/calmodulin-dependent protein kinase II regulates Tiam1 by reversible protein phosphorylation. J Biol Chem 274(18):12753–12758

    Article  CAS  PubMed  Google Scholar 

  120. Seward ME, Easley CA, McLeod JJ, Myers AL, Tombes RM (2008) Flightless-I, a gelsolin family member and transcriptional regulator, preferentially binds directly to activated cytosolic CaMK-II. FEBS Lett 582(17):2489–2495

    Article  CAS  PubMed  Google Scholar 

  121. Tsiokas L (2009) Function and regulation of TRPP2 at the plasma membrane. Am J Physiol Renal Physiol 297(1):F1–F9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Obara T, Mangos S, Liu Y, Zhao J, Wiessner S, Kramer-Zucker AG et al (2006) Polycystin-2 immunolocalization and function in zebrafish. J Am Soc Nephrol 17(10):2706–2718

    Article  CAS  PubMed  Google Scholar 

  123. Backs J, Backs T, Bezprozvannaya S, McKinsey TA, Olson EN (2008) Histone deacetylase 4 confers CaM kinase II responsiveness to histone deacetylase 5 by oligomerization. Mol Cell Biol 28(10):3437–3445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Zhang T, Kohlhaas M, Backs J, Mishra S, Phillips W, Dybkova N et al (2007) CaMKIIdelta isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses. J Biol Chem 282(48):35078–35087

    Article  CAS  PubMed  Google Scholar 

  125. Di Giorgio E, Brancolini C (2016) Regulation of class IIa HDAC activities: it is not only matter of subcellular localization. Epigenomics 8(2):251–269

    Article  PubMed  CAS  Google Scholar 

  126. Di Giorgio E, Clocchiatti A, Piccinin S, Sgorbissa A, Viviani G, Peruzzo P et al (2013) MEF2 is a converging hub for histone deacetylase 4 and phosphatidylinositol 3-kinase/Akt-induced transformation. Mol Cell Biol 33(22):4473–4491

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. McKinsey TA, Zhang CL, Olson EN (2002) MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci 27(1):40–47

    Article  CAS  PubMed  Google Scholar 

  128. Bershteyn M, Atwood SX, Woo WM, Li M, Oro AE (2010) MIM and cortactin antagonism regulates ciliogenesis and hedgehog signaling. Dev Cell 19(2):270–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Saarikangas J, Mattila PK, Varjosalo M, Bovellan M, Hakanen J, Calzada-Wack J 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(Pt 8):1245–1255

    Article  CAS  PubMed  Google Scholar 

  130. Xia S, Li X, Johnson T, Seidel C, Wallace DP, Li R (2010) Polycystin-dependent fluid flow sensing targets histone deacetylase 5 to prevent the development of renal cysts. Development 137(7):1075–1084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Haddon C, Jiang YJ, Smithers L, Lewis J (1998) Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant. Development 125(23):4637–4644

    CAS  PubMed  Google Scholar 

  132. Haddon C, Mowbray C, Whitfield T, Jones D, Gschmeissner S, Lewis J (1999) Hair cells without supporting cells: further studies in the ear of the zebrafish mind bomb mutant. J Neurocytol 28(10–11):837–850

    Article  CAS  PubMed  Google Scholar 

  133. Itoh M, Kim CH, Palardy G, Oda T, Jiang YJ, Maust D et al (2003) Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev Cell 4(1):67–82

    Article  CAS  PubMed  Google Scholar 

  134. Kandachar V, Roegiers F (2012) Endocytosis and control of Notch signaling. Curr Opin Cell Biol 24(4):534–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Matsuda M, Chitnis AB (2009) Interaction with Notch determines endocytosis of specific Delta ligands in zebrafish neural tissue. Development 136(2):197–206

    Article  CAS  PubMed  Google Scholar 

  136. Matsumoto K, Fukunaga K, Miyazaki J, Shichiri M, Miyamoto E (1995) Ca2+/calmodulin-dependent protein kinase II and synapsin I-like protein in mouse insulinoma MIN6 cells. Endocrinology 136(9):3784–3793

    Article  CAS  PubMed  Google Scholar 

  137. Nielander HB, Onofri F, Valtorta F, Schiavo G, Montecucco C, Greengard P et al (1995) Phosphorylation of VAMP/synaptobrevin in synaptic vesicles by endogenous protein kinases. J Neurochem 65(4):1712–1720

    Article  CAS  PubMed  Google Scholar 

  138. Popoli M (1993) Synaptotagmin is endogenously phosphorylated by Ca2+/calmodulin protein kinase II in synaptic vesicles. FEBS Lett 317(1–2):85–88

    Article  CAS  PubMed  Google Scholar 

  139. Bustos R, Kolen ER, Braiterman L, Baines AJ, Gorelick FS, Hubbard AL (2001) Synapsin I is expressed in epithelial cells: localization to a unique trans-Golgi compartment. J Cell Sci 114(Pt 20):3695–3704

    CAS  PubMed  Google Scholar 

  140. Marcet B, Chevalier B, Luxardi G, Coraux C, Zaragosi LE, Cibois M et al (2011) Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat Cell Biol 13(6):693–699

    Article  CAS  PubMed  Google Scholar 

  141. Ann EJ, Kim HY, Seo MS, Mo JS, Kim MY, Yoon JH et al (2012) Wnt5a controls Notch1 signaling through CaMKII-mediated degradation of the SMRT corepressor protein. J Biol Chem 287(44):36814–36829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Mamaeva OA, Kim J, Feng G, McDonald JM (2009) Calcium/calmodulin-dependent kinase II regulates notch-1 signaling in prostate cancer cells. J Cell Biochem 106(1):25–32

    Article  CAS  PubMed  Google Scholar 

  143. Bayer KU, De Koninck P, Schulman H (2002) Alternative splicing modulates the frequency-dependent response of CaMKII to Ca2+ oscillations. EMBO J 21(14):3590–3597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. De Koninck P, Schulman H (1998) Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279(5348):227–230

    Article  PubMed  Google Scholar 

  145. Kinoshita N, Iioka H, Miyakoshi A, Ueno N (2003) PKC delta is essential for Dishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements. Genes Dev 17(13):1663–1676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Horne-Badovinac S, Lin D, Waldron S, Schwarz M, Mbamalu G, Pawson T et al (2001) Positional cloning of heart and soul reveals multiple roles for PKC lambda in zebrafish organogenesis. Curr Biol 11(19):1492–1502

    Article  CAS  PubMed  Google Scholar 

  147. Gagnon JA, Valen E, Thyme SB, Huang P, Ahkmetova L, Pauli A et al (2014) Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. PLoS One 9(5):e98186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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  1. Life Sciences, Virginia Commonwealth University, Richmond, VA, USA

    Sarah C. Rothschild & Robert M. Tombes

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    Md. Shahidul Islam

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Rothschild, S.C., Tombes, R.M. (2020). Widespread Roles of CaMK-II in Developmental Pathways. In: Islam, M. (eds) Calcium Signaling. Advances in Experimental Medicine and Biology, vol 1131. Springer, Cham. https://doi.org/10.1007/978-3-030-12457-1_21

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