Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development

Developmental Biology

Volumn 266, Issue 1, 2004, Pages 1-16

  Schulz, Robert A ^a   Yutzey, Katherine E ^b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

C. elegans; Calcineurin; Cardiomyocyte; Drosophila; Fiber type specialization; Hypertrophy; Indirect flight muscle; Interacting genes; NFAT; Signal transduction; Skeletal muscle; Valvuloseptal development; Vascular development

Indexed keywords

CALCINEURIN; CALCIUM; PHOSPHATASE; PROTEIN SUBUNIT; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NFAT;

BLOOD VESSEL; CAENORHABDITIS ELEGANS; CALCIUM SIGNALING; CARDIOVASCULAR SYSTEM; CATALYSIS; CELL DIFFERENTIATION; CELL MATURATION; CELL TYPE; DEVELOPMENT; DROSOPHILA MELANOGASTER; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE LOCUS; GENE MUTATION; GENETIC ANALYSIS; GENETIC CONSERVATION; HEART; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART VALVE; HEART VENTRICLE HYPERTROPHY; HUMAN; INHIBITION KINETICS; INVERTEBRATE; MUSCLE DEVELOPMENT; MUSCLE HYPERTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; T LYMPHOCYTE; VERTEBRATE;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; INVERTEBRATA; VERTEBRATA;

EID: 0345830423     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2003.10.008     Document Type: Review

References (130)

1. Abbott K.L., Friday B.B., Thaloor D., Murphy T.J., Pavlath G.K. Activation and cellular localization of the cyclosporine A-sensitive transcription factor NF-AT in skeletal muscle cells. Mol. Biol. Cell. 9:1998;2905-2916.
2. Adams M.D.et al. The genome sequence of Drosophila melanogaster. Science. 287:2000;2185-2195.
3. Al-Daraji W.I., Grant K.R., Ryan K., Saxton A., Reynolds N.J. Localization of calcineurin/NFAT in human skin and psoriasis and inhibition of calcineurin/NFAT activation in human keratinocytes by cyclosporin A. J. Invest. Dermatol. 118:2002;779-788.
4. Argraves W.S., Larue A.C., Fleming P.A., Drake C.J. VEGF signaling is required for the assembly but not the maintenance of embryonic blood vessels. Dev. Dyn. 225:2002;298-304.
5. Armesilla A.L., Lorenzo E., Arco P.G.D., Martinez-Martinez S., Alfranca A., Redondo J.M. Vascular endothelial growth factor activates nuclear factor of activated T cells in human endothelial cells: a role for tissue factor gene expression. Mol. Cell. Biol. 19:1999;2032-2043.
6. Bailey P., Holowacz T., Lassar A.B. The origin of skeletal muscle stem cells in the embryo and adult. Curr. Opin. Cell Biol. 13:2001;679-689.
7. Baksh S., Burakoff S.J. The role of calcineurin in lymphocyte activation. Semin. Immunol. 12:2000;405-415.
8. Bandyopadhyay J., Lee J., Lee J., Lee J.I., Yu J.-R., Jee C., Cho J.-H., Jung S., Lee M.H., Zannoni S., Singson A., Kim D.H., Koo H.-S., Ahnn J. Calcineurin, a calcium/calmodulin-dependent protein phosphatase, is involved in movement, fertility, egg laying, and growth in Caenorhabditis elegans. Mol. Biol. Cell. 13:2002;3281-3293.
9. Beals C.R., Clipstone N.A., Ho S.N., Crabtree G.R. Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin-sensitive intramolecular interaction. Genes Dev. 11:1997;824-834.
10. Beals C.R., Sheridan C.M., Turek C.W., Gardner P., Crabtree G.R. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science. 275:1997;1930-1934.
11. Bodine S.C., Stitt T.N., Gonzalez M., Kline W.O., Stover G.L., Bauerlein R., Zlotchenko E., Scrimgeour A., Lawrence J.C., Glass D.J., Yancopoulos G.D. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3:2001;1014-1019.
12. Bollag G., Clapp D.W., Shih S., Adler F., Zhang Y.Y., Thompson P., Lange B.J., Freedman M.H., McCormick F., Jacks T., Shannon K. Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in heamatopoietic cells. Nat. Genet. 12:1996;144-148.
13. Bour B.A., O'Brien M.A., Lockwood W.L., Goldstein E.S., Bodmer R., Taghert P.H., Abmayr S.M., Nguyen H.T. Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev. 9:1995;730-741.
14. Brown L., Chen M.X., Cohen P.T. Identification of a cDNA encoding a Drosophila calcium/calmodulin regulated protein phosphatase, which has its most abundant expression in the early embryo. FEBS Lett. 339:1994;124-128.
15. Buckingham M. Skeletal muscle formation in vertebrates. Curr. Opin. Genet. Dev. 11:2001;440-448.
16. Bueno O.F., Brandt E.B., Rothenberg M.E., Molkentin J.D. Defective T cell development and function in calcineurin A beta-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 99:2002;9398-9403.
17. Bushdid P.B., Osinska H., Waclaw R.R., Molkentin J.D., Yutzey K.E. NFATc3 and NFATc4 are required for cardiac development and mitochondrial function. Circ. Res. 92:2003;1305-1313.
18. Camenisch T.D., Molin D.G.M., Person A., Runyan R.B., Gittenberger-de Groot A.C., McDonald J.A., Klewer S.E. Temporal and distinct TGFβ ligand requirements during mouse and avian endocardial cushion morphogenesis. Dev. Biol. 248:2002;170-181.
19. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., Fahrig M., Vandenhoeck A., Harpal K., Eberhardt C.et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 380:1996;435-439.
20. Casas C., Martinez S., Pritchard M.A., Fuentes J.J., Nadal M., Guimera J., Arbones M., Florez J., Soriano E., Estivill X., Alcantara S. Dscr1, a novel endogenous inhibitor of calcineurin signaling, is expressed in the primitive ventricle of the heart and during neurogenesis. Mech. Dev. 101:2001;289-292.
21. Chen E.H., Olson E.N. Antisocial, an intracellular adaptor protein, is required for myoblast fusion in Drosophila. Dev. Cell. 1:2002;705-715.
22. Chien K.R., Zhu H., Knowlton K.U., Miller-Hance W., van Bilsen M., O'Brien T.X., Evans S.M. Transcriptional regulation during cardiac growth and development. Annu. Rev. Physiol. 55:1993;77-95.
23. Chin E.R., Olson E.N., Richardson J.A., Yang Q., Humphries C., Shelton J.M., Wu H., Zhu W., Bassel-Duby R., Williams R.S. A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev. 12:1998;2499-2509.
24. Chow C.W., Rincon M., Cavanaugh J., Dickens M., Davis R.J. Nuclear accumulation of NFAT4 opposed by the JNK signal transduction pathway. Science. 278:1997;1638-1641.
25. Conway S.J., Kruzynska-Frejtag A., Kneer P.L., Machnicki M., Koushik S.V. What cardiovascular defect does my prenatal mouse mutant have and why? Genesis. 35:2003;1-21.
26. 2+, calcineurin, and NFAT. Cell. 96:1999;611-614.
27. Crabtree G.R., Olson E.N. NFAT signaling: choreographing the social lives of cells. Cell. 109:2002;S67-S79.
28. Cripps R.M., Olson E.N. Twist is required for muscle template splitting during adult Drosophila myogenesis. Dev. Biol. 203:1998;106-115.
29. de la Pompa J.L., Timmerman L.A., Takimoto H., Yoshida H., Elia A.J., Samper E., Potter J., Wakeham A., Marengere L., Langille B.L., Crabtree G.R., Mak T.W. Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature. 392:1998;182-186.
30. Delling U., Tureckova J., Lim H.W., De Windt L.J., Rotwein P., Molkentin J.D. A calcineurin-NFATc3-dependent pathway regulates skeletal muscle differentiation and slow myosin heavy-chain expression. Mol. Cell. Biol. 20:2000;6600-6611.
31. Dor Y., Camenisch T.D., Itin A., Fishman G.I., McDonald J.A., Carmeliet P., Keshit E. A novel role for VEGF in endocardial cushion formation and its potential contribution to congenital heart defects. Development. 128:2001;1531-1538.
32. Drake C.J., Little C.D. Exogenous vascular endothelial growth factor induces malformed and hyperfused vessels during embryonic neovascularization. Proc. Natl. Acad. Sci. U. S. A. 92:1995;7657-7661.
33. Dunn S.E., Burns J.L., Michel R.N. Calcineurin is required for skeletal muscle hypertrophy. J. Biol. Chem. 274:1999;21908-21912.
34. Dunn S.E., Simard A.R., Bassel-Duby R., Williams R.S., Michel R.N. Nerve activity-dependent modulation of calcineurin signaling in adult fast and slow skeletal muscle fibers. J. Biol. Chem. 276:2001;45243-45254.
35. Dupont-Versteegden E.E., Knox M., Gurley C.M., Houle J.D., Peterson C.A. Maintenance of muscle mass is not dependent on the calcineurin-NFAT pathway. Am. J. Physiol.: Cell Physiol. 282:2002;C1387-C1395.
36. Eisenberg L.M., Markwald R.R. Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ. Res. 77:1995;1-6.
37. Fantel A.G., Person R.E. Involvement of mitochondria and other free radical sources in normal and abnormal fetal development. Ann. N. Y. Acad. Sci. 959:2002;424-433.
38. Fernandes J.J., Keshishian H. Patterning the dorsal longitudinal flight muscles (DLM) of Drosophila: insights from the ablation of larval scaffolds. Development. 122:1996;3755-3763.
39. Fernandes J., Bate M., Vijayraghavan K. Development of indirect flight muscles of Drosophila. Development. 113:1991;67-77.
40. Ferrara N., Carver-Moore K., Chen H., Dowd M., Lu L., O'Shea K.S., Powell-Braxton L., Hillan K.J., Moore M.W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 380:1996;439-442.
41. Flamme I., Reutern M.V., Drexler H.C.A., Syed-Ali S., Risau W. Overexpression of vascular endothelial growth factor in embryos induces hypervascularization and increased vascular permeability without alterations in embryonic pattern formation. Dev. Biol. 171:1995;399-414.
42. Flanagan M.W., Corthesy B., Bram R.J., Crabtree G.R. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature. 352:1991;803-807.
43. Florini J., Ewton D., Magri K. Hormones, growth factors, and myogenic differentiation. Annu. Rev. Physiol. 53:1991;201-216.
44. Franco D., Lamers W.H., Moorman A.F.M. Patterns of expression in the developing myocardium: towards a morphologically integrated transcriptional model. Cardiovasc. Res. 38:1998;25-53.
45. Freeman S.B., Taft L.F., Dooley K.J., Allran K., Sherman S.L., Hassold T.J., Khoury M.J., Saker D.M. Population-based study of congenital heart defects in Down syndrome. Am. J. Med. Genet. 80:1998;213-217.
46. Frey N., Richardson J.A., Olson E.N. Calsarcins, a novel family of sarcomeric calcineurin-binding proteins. Proc. Natl. Acad. Sci. U. S. A. 97:2000;14632-14637.
47. Friday B.B., Horsley V., Pavlath G.K. Calcineurin activity is required for the initiation of skeletal muscle differentiation. J. Cell Biol. 149:2000;657-665.
48. Friedman J.M., Arbiser J., Epstein J.A., Gutmann D.H., Huot S.J., Lin A.E., McManus B., Korf B.R. Cardiovascular disease in neurofibromatosis 1: report of the NF1 cardiovascular task force. Genet. Med. 4:2002;105-111.
49. Gajewski K., Wang J., Molkentin J.D., Chen E.H., Olson E.N., Schulz R.A. Requirement of the calcineurin subunit gene canB2 for indirect flight muscle formation in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 100:2003;1040-1045.
50. Gitler A.D., Zhu Y., Ismat F.A., Lu M.M., Yamauchi Y., Parada L.F., Epstein J.A. Nf1 has an essential role in endothelial cells. Nat. Genet. 33:2003;75-79.
51. 2+/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell. 105:2001;863-875.
52. Graef I.A., Gastier J.M., Francke U., Crabtree G.R. Evolutionary relationships among Rel domains indicate functional diversification by recombination. Proc. Natl. Acad. Sci. U. S. A. 98:2001;5740-5745.
53. Graef I.A., Wang F., Charron F., Chen L., Neilson J., Tessier-Lavigne M., Crabtree G.R. Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons. Cell. 113:2003;657-670.
54. Gregorio C.C., Antin P.B. To the heart of myofibril assembly. Trends Cell Biol. 10:2000;355-362.
55. Guerini D., Montell C., Klee C.B. Molecular cloning and characterization of the genes encoding two subunits of Drosophila melanogaster calcineurin. J. Biol. Chem. 267:1992;22542-22549.
56. Guo L., Nakamura K., Lynch J., Opas M., Olson E.N., Agellon L.B., Michalek M. Cardiac-specific expression of calcineurin reverses embryonic lethality in calreticulin-deficient mouse. J. Biol. Chem. 277:2002;50776-50779.
57. Hernandez G.L., Volpert O.V., Iniguez M.A., Lorenzo E., Martinez-Martinez S., Grau R., Fresno M., Redondo J.M. Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin A: roles of the nuclear factor of activated T cells and cyclooxygenase 2. J. Exp. Med. 193:2001;607-620.
58. Ho I.C., Kim J.H., Rooney J.W., Speigelman B.M., Glimcher L.H. A potential role for the nuclear factor of activated T cells family of transcriptional regulatory proteins in adipogenesis. Proc. Natl. Acad. Sci. U. S. A. 95:1998;15537-15541.
59. Horsley V., Friday B.B., Matteson S., Kegley K.M., Gephart J., Pavlath G.K. Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J. Cell Biol. 153:2001;329-338.
60. Horsley V., Jansen K.M., Mills S.T., Pavlath G.K. IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell. 113:2003;483-494.
61. Hughes S.M. Muscle development: electrical control of gene expression. Curr. Biol. 8:1998;R892-R894.
62. Icardo J.M., Colvee E. Atrioventricular valves of the mouse II: light and transmission electron microscopy. Anat. Rec. 241:1995;391-400.
63. Icardo J.M., Arrechedera H., Colvee E. The atrioventricular valves of the mouse I: scanning electron microscope study. J. Anat. 182:1993;87-94.
64. Johnson E.N., Lee Y.M., Sander T.L., Rabkin E., Schoen F.J., Kaushal S., Bischoff J. NFATc1 mediates vascular endothelial growth factor-induced proliferation of human pulmonary valve endothelial cells. J. Biol. Chem. 278:2003;1686-1692.
65. Kayyali U.S., Zhang W., Yee A.G., Seidman J.G., Potter H. Cytoskeletal changes in the brains of mice lacking calcineurin A alpha. J. Neurochem. 68:1999;1668-1678.
66. -/- mice leads to decreased muscle size in the adult. Dev. Biol. 232:2001;115-126.
67. Kronert W.A., O'Donnell P.T., Fieck A., Lawn A., Vigoreaux J.O., Sparrow J.C., Bernstein S.I. Defects in the Drosophila myosin rod permit sarcomere assembly but cause flight muscle degeneration. J. Mol. Biol. 249:1995;111-125.
68. Kronert W.A., Acebes A., Ferrus A., Bernstein S.I. Specific myosin heavy chain mutations suppress troponin I defects in Drosophila muscles. J. Cell Biol. 144:1999;989-1000.
69. Kuhara A., Inada H., Katsura I., Mori I. Negative regulation and gain control of sensory neurons by the C. elegans calcineurin TAX-6. Neuron. 33:2002;751-763.
70. Kumai M., Nishii K., Nakamura K., Takeda N., Suzuki M., Shibata Y. Loss of connexin45 causes a cushion defect in early cardiogenesis. Development. 127:2000;3501-3512.
71. Lakkis M.M., Epstein J.A. Neurofibromin modulation of ras activity is required for normal endocardial-mesenchymal transformation in the developing heart. Development. 125:1998;4359-4367.
72. Lange A.W., Molkentin J.D., Yutzey K.E. DSCR1 gene expression is dependent on NFATc1 during cardiac valve formation and colocalizes with anomalous organ development in trisomy 16 mice. Dev. Biol. 2004;. (in press).
73. Liberatore C.M., Yutzey K.E. Calcineurin signaling in avian cardiovascular development. Dev. Dyn. 2004;. (in press).
74. Lilly B., Zhao B., Ranganayakulu G., Paterson B.M., Schulz R.A., Olson E.N. Requirement of MADS domain transcription factor DMEF2 for muscle formation in Drosophila. Science. 267:1995;688-693.
75. Lyons G.E. In situ analysis of the cardiac muscle program during embryogenesis. Trends Cardiovasc. Med. 4:1994;70-77.
76. Macian F., Lopez-Rodriquez C., Rao A. Partners in transcription: NFAT and AP1. Oncogene. 20:2001;2476-2489.
77. Matilla P.S., Ullman K.S., Fiering S., Emmel E.A., McCutcheon M., Crabtree G.R., Herzenberg L.A. The action of cyclosporin A and FK506 suggest a novel step in the activation of T lymphocytes. EMBO J. 9:1990;4425-4433.
78. Mesaeli N., Nakamura K., Zvaritch E., Dickie P., Dziak E., Krause K.H., Opas M., MacLennan D.H., Michalek M. Calreticulin is essential for cardiac development. J. Cell Biol. 144:1999;857-868.
79. Miquerol L., Langille B.L., Nagy A. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development. 127:2000;3941-3946.
80. Mitchell P.O., Mills S.T., Pavlath G.K. Calcineurin differentially regulates maintenance and growth of phenotypically distinct muscles. Am. J. Physiol.: Cell Physiol. 282:2002;C984-C992.
81. Molkentin J.D. Calcineurin and beyond; cardiac hypertrophic signaling. Circ. Res. 87:2000;731-738.
82. Molkentin J.D., Lu J.-R., Antos C.L., Markham B., Richardson J., Robbins J., Grant S.R., Olson E.N. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 93:1998;215-228.
83. Musaro A., McCullagh K.J.A., Naya F.J., Olson E.N., Rosenthal N. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NFATc1. Nature. 400:1999;581-585.
84. Naya F.J., Wu C., Richardson J.A., Overbeek P., Olson E.N. Transcriptional activity of MEF2 during mouse embryogenesis monitored with a MEF2-dependent transgene. Development. 126:1999;2045-2052.
85. Naya F.J., Mercer B., Shelton J., Richardson J.A., Williams R.S., Olson E.N. Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J. Biol. Chem. 275:2000;4545-4548.
86. Nemer G., Nemer M. Cooperative interaction between GATA5 and NF-ATc regulates endothelial-endocardial differentiation of cardiogenic cells. Development. 129:2002;4045-4055.
87. Olson E.N., Williams R.S. Calcineurin signaling and muscle remodeling. Cell. 101:2000;689-692.
88. Olson E.N., Williams R.S. Remodeling muscles with calcineurin. BioEssays. 22:2000;510-519.
89. Oukka M., Ho I.C., de la Brousse F.C., Hoey T., Grusby M.J., Glimcher L.H. The transcription factor NFAT4 is involved in the generation and survival of T cells. Immunity. 9:1998;295-304.
90. Pallafacchina G., Calabria E., Serrano A.L., Kalhovde J.M., Schiaffino S. A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc. Natl. Acad. Sci. U. S. A. 99:2002;9213-9218.
91. Pan S., Koyano-Nakagawa N., Tsuruta L., Amasaki Y., Yokota T., Mori S., Arai N., Arai K. Molecular cloning and functional characterization of murine cDNA encoding transcription factor NFATc. Biochem. Biophys. Res. Commun. 240:1997;314-323.
92. Paranya G., Vineberg S., Dvorin E., Kaushal S., Roth S.J., Rabkin E., Schoen F.J., Bischoff J. Aortic valve endothelial cells undergo transforming growth factor β-mediated and non-transforming growth factor β-mediated transdifferentiation in vitro. Am. J. Pathol. 159:2001;1335-1343.
93. Parsons S.A., Wilkins B.J., Bueno O.F., Molkentin J.D. Altered skeletal muscle phenotypes in calcineurin Aα and Aβ gene-targeted mice. Mol. Cell. Biol. 23:2003;4331-4343.
94. Peng S.L., Gerth A.J., Ranger A.M., Glimcher L.H. NFATc1 and NFATc2 together control both T and B cell activation and differentiation. Immunity. 14:2001;13-20.
95. Pimentel R.C., Yamada K.A., Kleber A.G., Saffitz J.E. Autocrine regulation of myocyte Cx43 expression by VEGF. Circ. Res. 90:2002;671-677.
96. Poole T.J., Finkelstein E.B., Cox C.M. The role of FGF and VEGF in angioblast induction and migration during vascular development. Dev. Dyn. 220:2001;1-17.
97. Ranganayakulu G., Zhao B., Dokidis A., Molkentin J.D., Olson E.N., Schulz R.A. A series of mutations in the D-MEF2 transcription factor reveal multiple functions in larval and adult myogenesis in Drosophila. Dev. Biol. 171:1995;169-181.
98. Ranger A.M., Grusby M.J., Gravellese E.M., de la Brousse F.C., Hoey T., Mickanin C., Baldwin H.S., Glimcher L.H. The transcription factor NF-ATc is essential for cardiac valve formation. Nature. 392:1998;186-190.
99. Ranger A.M., Gerstenfeld L.C., Wang J., Kon T., Bae H., Gravellese E.M., Glimcher M.J., Glimcher L.H. The nuclear factor of activated T cells (NFAT) transcription factor NFATp (NFATc2) is a repressor of chondrogenesis. J. Exp. Med. 191:2000;9-21.
100. Rao A., Luo C., Hogan P.G. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15:1997;707-747.
101. Rommel C., Bodine S.C., Clarke B.A., Rossman R., Nunez L., Stitt T.N., Yancopoulos G.D., Glass D.J. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 3:2001;1009-1013.
102. Rosenthal N., Xavier-Neto J. From the bottom of the heart: anteroposterior decisions in cardiac muscle differentiation. Curr. Opin. Cell Biol. 12:2000;742-746.
103. Rossant J., Howard L. Signaling pathways in vascular development. Annu. Rev. Cell Dev. Biol. 18:2002;541-573.
104. Rothermel B., Vega R.B., Yang J., Wu H., Bassel-Duby R., Williams R.S. A protein encoded within the Down syndrome critical region is enriched in striated muscle and inhibits calcineurin signaling. J. Biol. Chem. 275:2000;8719-8725.
105. Rothermel B.A., Vega R.B., Olson E.N. The role of modulatory calcineurin-interacting proteins in calcineurin signaling. Trends Cardiovasc. Med. 13:2003;15-21.
106. -/- embryos. Development. 125:1998;533-544.
107. Rusnak F., Mertz P. Calcineurin: form and function. Physiol. Rev. 80:2000;1483-1521.
108. Sadoshima J., Izumo S. The cellular and molecular response of cardiac myocytes to mechanical stress. Annu. Rev. Physiol. 59:1997;551-571.
109. Saneyoshi T., Kume S., Amasaki Y., Mikoshiba K. The Wnt/calcium pathway activated NF-AT and promotes ventral cell fate in Xenopus embryos. Nature. 417:2002;295-299.
110. Santini M.P., Talora C., Seki T., Bolgan L., Dotto G.P. Cross talk among calcineurin, Sp1/Sp3, and NFAT in control of p21(WAF1/CIP1) expression in keratinocyte differentiation. Proc. Natl. Acad. Sci. U. S. A. 98:2001;9575-9580.
111. Sato T.N., Loughna S. Vasculogenesis and angiogenesis. Rossant J., Tam P.P.L. Mouse Development: Patterning, Morphogenesis, and Organogenesis. 2002;211-233 Academic Press, San Diego.
112. Schubert W., Yang X.Y., Yang T.T.C., Factor S.M., Lisanti M.P., Molkentin J.D., Rincon M., Chow C.-W. Requirement of transcription factor NFAT in developing atrial myocardium. J. Cell Biol. 161:2003;861-874.
113. 2+-dependent calcineurin signaling pathway. Nature. 400:1999;576-581.
114. Shepard T.H., Muffley L.A., Smith L.T. Ultrastructural study of mitochondria and their cristae in embryonic rats and primate (N. nemistrina). Anat. Rec. 252:1998;383-392.
115. Sheridan C.M., Heist E.K., Beals C.R., Crabtree G.R., Gardner P. Protein kinase A negatively modulates the nuclear accumulation of NF-ATc1 by priming for subsequent phosphorylation by glycogen synthase kinase-3. J. Biol. Chem. 277:2002;48664-48676.
116. 2+-calmodulin-activated protein phosphatase calcineurin negatively regulates Egf receptor signaling in Drosophila development. Genetics. 161:2002;183-193.
117. Sussman M.A., Lim H.W., Gude N., Taigen T., Olson E.N., Robbins J., Colbert M.C., Gualberto A., Wieczorek D.F., Molkentin J.D. Prevention of cardiac hypertrophy in mice by calcineurin inhibition. Science. 281:1998;1690-1693.
118. Takayanagi H., Kim S., Koga T., Nishina H., Isshiki M., Yoshida H., Saiura A., Isobe M., Yokochi T., Inoue J.-I., Wagner E.F., Mak T.W., Kodama T., Taniguchi T. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell. 3:2002;889-901.
119. Tomita M., Reinhold M.I., Molkentin J.D., Naski M.C. Calcineurin and NFAT4 induce chondrogenesis. J. Biol. Chem. 277:2002;42214-42218.
120. Warren W.D., Phillips A.M., Howells A.J. Drosophila melanogaster contains both X-linked and autosomal homologues of the gene encoding calcineurin B. Gene. 177:1996;149-153.
121. Weinstein B. What guides early embryonic blood vessel formation? Dev. Dyn. 215:1999;2-11.
122. Wilkins B.J., de Windt L.J., Bueno O.F., Braz J.C., Glascock B.J., Kimball T.F., Molkentin J.D. Targeted disruption of NFATc3, but not NFATc4, reveals an intrinsic defect in calcineurin-mediated cardiac hypertrophic growth. Mol. Cell. Biol. 22:2002;7603-7613.
123. Wu H., Rothermel B., Kanatous S., Rosenberg P., Naya F.J., Shelton J.M., Hutcheson K.A., DiMaio J.M., Olson E.N., Bassel-Duby R., Williams R.S. Activation of MEF2 by muscle activity is mediated through a calcineurin- dependent pathway. EMBO J. 20:2001;6414-6423.
124. Xia Y., McMillin J.B., Lewis A., Moore M., Zhu W.G., Williams R.S., Kellems R.E. Electrical stimulation of neonatal cardiac myocytes activates the NFAT3 and GATA4 pathways and up-regulates the adenylsuccinate synthetase 1 gene. J. Biol. Chem. 275:2000;1855-1863.
125. Yancopoulos G.D., Davis S., Gale N.W., Rudge J.S., Wiegand S.J., Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 407:2000;242-248.
126. Yang J., Rothermel B., Vega R.B., Frey N., McKinsey T.A., Olson E.N., Bassel-Duby R., Williams R.S. Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles. Circ. Res. 87:2000;e61-e68.
127. Yang T.T., Xiong Q., Enslen H., Davis R.J., Chow C.W. Phosphorylation of NFATc4 by p38 mitogen-activated protein kinases. Mol. Cell. Biol. 22:2002;3892-3904.
128. Yutzey K.E., Kirby M.L. Wherefore heart thou? Embryonic origins of cardiogenic mesoderm. Dev. Dyn. 223:2002;307-320.
129. Zhang B.W., Zimmer G., Chen J., Ladd D., Li E., Alt F.W., Wiederrecht G., Cryan J., O'Neill E.A., Seidman C.E., Abbas A.K., Seidman J.G. T cell responses in calcineurin Aα-deficient mice. J. Exp. Med. 183:1996;413-420.
130. Zhu J., Shibasaki F., Price R., Guillemot J.C., Yano T., Dotsch V., Wagner G., Ferrara P., McKeon F. Intramolecular masking of nuclear import signal on NF-AT4 by casein kinase I and MEKK1. Cell. 93:1998;851-861.