The effects of bone morphogenetic protein 2 and 4 (BMP2 and BMP4) on gap junctions during neurodevelopment

Experimental Neurology

Volumn 162, Issue 1, 2000, Pages 13-26

  Bani Yaghoub, Mahmud ^a   Felker, Josh M ^a   Sans, Christopher ^a   Naus, Christian C G ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

BMP; Connexin; Dye coupling; Intercellular communication; Neuronal differentiation; P19

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CONNEXIN 43;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL COMMUNICATION; CELL GROWTH; CONTROLLED STUDY; GAP JUNCTION; MORPHOGENESIS; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 0034073952     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.2000.7294     Document Type: Article

References (126)

1. Attisano L., Wrana J. L. Mads and Smads in TGF beta signalling. Curr. Opin. Cell. Biol. 10:1998;188-194.
2. Autzen P., Robson C. N., Bjartell A., Malcolm A. J., Johnson M. I., Neal D. E., Hamdy F. C. Bone morphogenetic protein 6 in skeletal metastases from prostate cancer and other common human malignancies. Br. J. Cancer. 78:1998;1219-1223.
3. Baker J. C., Harland R. M. From receptor to nucleus: The Smad pathway. Curr. Opin. Genet. Dev. 7:1997;467-473.
4. Bain G., Ray W. J., Yao M., Gottlieb D. I. From embryonal carcinoma cells to neurons: The P19 pathway. BioEssays. 16:1994;343-348.
5. Bani-Yaghoub M., Bechberger J. F., Underhill T. M., Naus C. C. G. The effects of gap junction blockage on neuronal differentiation of human NTera2/clone D1 cells. Exp. Neurol. 156:1999;16-32.
6. Bani-Yaghoub M., Underhill T. M., Naus C. C. G. Gap junction blockage interferes with neuronal and astroglial differentiation of mouse P19 embryonal carcinoma cells. Dev. Genet. 24:1999;69-81.
7. Belliveau D. J., Bechberger J. F., Rogers K. A., Naus C. C. G. Differential expression of gap junctions in neurons and astrocytes derived from P19 embryonal carcinoma cells. Dev. Genet. 21:1997;1-14.
8. Bittman K., Lo Turco J. J. Radial glial cells are coupled to neocortical precursors by gap junctions. Soc. Neurosci. Abstr. 115.2:1998.
9. Bittman K., Owens D. F., Kriegstein A. R., Lo Turco J. J. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J. Neurosci. 17:1997;7037-7044.
10. Boulton T. G., Nye S. H., Robbins D. J., Ip N. Y., Radziejewska E., Morgenbesser S. D., DePinho R. A., Panayotatos N., Cobb M. H., Yancopoulos G. D. ERKs: A family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell. 17:1991;663-675.
11. Bruzzone R., Ressot C. Connexins, gap junctions and cell-cell signaling in the nervous system. Eur. J. Neurosci. 9:1997;1-6.
12. Chen X., Rubock M. J., Whitman M. A transcriptional partner for MAD proteins in TGF-beta signalling. Nature. 383:1996;691-696.
13. Condorelli D. F., Parenti R., Spinella F., Salinaro A. T., Belluardo N. Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur. J. Neurosci. 10:1998;1202-1208.
14. Coucouvanis E., Martin G. R. BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development. 126:1999;535-546.
15. Crick F. Diffusion in embryogenesis. Nature. 225:1970;420-422.
16. Dahl E., Willecke K., Balling R. Segment-specific expression of the gap junction gene connexin31 during hindbrain development. Dev. Genes Evol. 207:1997;359-361.
17. Dermietzel R. Gap junction wiring: A new principle in cell to cell communication in the nervous system. Brain Res. Rev. 26:1998;176-183.
18. Doble B. W., Chen Y., Bosc D. G., Litchfield D. W., Kardami E. Fibroblast growth factor 2 decreases metabolic coupling and stimulates phosphorylation as well as masking of connexin43 epitopes in cardiac myocytes. Circ. Res. 79:1996;647-658.
19. Doble B. W., Kardami E. Basic fibroblast growth factor stimulates connexin43 expression and intercellular communication of cardiac fibroblasts. Mol. Cell. Biochem. 143:1995;81-87.
20. Dosch R., Gawantka V., Delius H., Blumenstock C., Niehrs C. BMP4 acts as a morphogen in dorsoventral mesoderm patterning in Xenopus. Development. 124:1997;2325-2334.
21. Dudley D. T., Pang L., Decker S. J., Bridges A. J., Saltiel A. R. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA. 92:1995;7686-7689.
22. Ewart J. L., Cohen M. F., Meyer R. A., Huang G. Y., Wessels A., Gourdie R. G., Chin A. J., Park S. M. J., Lazatin B. O., Villabon S., Lo C. W. Heart and neural tube defects in transgenic mice overexpressing the Cx43 gap junction gene. Development. 124:1997;1281-1292.
23. Fainsod A., Deißler K., Yelin R., Marom K., Epstein M., Pillemer G., Steinbeisser H., Blum M. The dorsalizing and neural inducing gene follistatin is an antagonist of BMP4. Mech. Dev. 63:1997;39-50.
24. Fantl W. J., Johnson D. E., Williams L. T. Signalling by receptor tyrosine kinases. Annu. Rev. Biochem. 62:1993;453-481.
25. Geimonen E., Jiang W., Ali M., Fishman G. I., Garfield R. E., Andersen J. Activation of protein kinase C in human uterine smooth muscle induces connexin-43 gene transcription through an AP-1 site in the promoter sequence. J. Biol. Chem. 271:1996;23667-23674.
26. Gilbert S. F. Cellular dialogues in organogenesis. Birth Defects. 30:1996;1-12.
27. Gilula N. B., Reeves R. O., Steinbach A. Metabolic coupling, ionic coupling and cell contacts. Nature. 235:1972;262-265.
28. Glozak M. A., Rogers M. B. Specific induction of apoptosis in P19 embryonal carcinoma cells by retinoic acid and BMP2 or BMP4. Dev. Biol. 179:1996;458-470.
29. Glozak M. A., Rogers M. B. BMP4- and RA-induced apoptosis is mediated through the activation of retinoic acid receptor α and γ in P19 embryonal carcinoma cells. Exp. Cell Res. 242:1998;165-173.
30. Golden J. A., Chernoff G. F. Anterior neural tube closure in the mouse: fuel for disagreement with the classical theory. Clin. Res. 31:1983;127A.
31. Graham A., Francis-West P., Brickell P., Lumsden A. The signalling molecule BMP4 mediates apoptosis in the rhombocephalic neural crest. Nature. 372:1994;684-686.
32. Graham A., Koentges G., Lumsden A. Neural crest apoptosis and the establishment of craniofacial pattern: An honorable death. Mol. Cell Neurosci. 8:1996;76-83.
33. Gross R. E., Mehler M. F., Mabie P. C., Zang Z., Santschi L., Kessler J. A. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron. 17:1996;595-606.
34. Gupta I. R., Piscione T. D., Grisaru S., Phan T., Macias-Silva M., Zhou X., Whiteside C., Wrana J. L., Rosenblum N. D. Protein kinase A is a negative regulator of renal branching morphogenesis and modulates inhibitory and stimulatory bone morphogenetic proteins. J. Biol. Chem. 274:1999;26305-26314.
35. Gustafson T., Wolpert L. Cellular movement and contact in urchin morphogenesis. Biol. Rev. 42:1967;442-498.
36. Hemmati-Brivanlou A., Melton D. Vertebrate embryonic cells will become nerve cells unless told otherwise. Cell. 88:1997;13-17.
37. Hogan B. L. M. Upside-down ideas vindicated. Nature. 376:1995;210-211.
38. Hogan B. L. M. Bone morphogenetic proteins: Multifunctional regulators of vertebrates development. Genes Dev. 10:1996;1580-1594.
39. Hoodless P. A., Haerry T., Abdollah S., Stapleton M., O'Connor M. B., Attisano L., Wrana J. L. MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell. 85:1996;489-500.
40. Hoodless P. A., Hemmati-Brivanlou A. Inhibitory control of neural differentiation in mammalian cells. Dev. Genes Evol. 207:1997;19-28.
41. Horn V., Minucci S., Ogryzko V. V., Adamson E. D., Howard B. H., Levin A. A., Ozato K. RAR and RXR selective ligands cooperatively induce apoptosis and neuronal differentiation in P19 embryonal carcinoma cells. FASEB J. 10:1996;1071-1077.
42. Husmann M., Gorgen I., Weisgerber C., Bitter-Suermann D. Up-regulation of embryonic NCAM in an EC cell line by retinoic acid. Dev. Biol. 136:1989;194-200.
43. Ikeya M., Lee S. M., Johnson J. E., McMahon A. P., Takada S. Wnt signalling required for expansion of neural crest and CNS progenitors. Nature. 389:1997;966-970.
44. Ishibashi K., Sasaki S., Akiba T., Marumo F. Expression of bone morphogenic protein 7 mRNA in MDCK cells. Biochem. Biophys. Res. Commun. 193:1993;235-239.
45. Iwasaki S., Hattori A., Sato M., Tsujimoto M., Kohno M. Characterization of the bone morphogenetic protein-2 as a neurotrophic factor. J. Biol. Chem. 271:1996;17360-17365.
46. Johnson G. L., Vaillancourt R. R. Sequential protein kinase reactions controlling cell growth and differentiation. Curr. Opin. Cell Biol. 6:1994;230-238.
47. Jones C. M., Smith J. C. Establishment of a BMP-4 morphogen gradient by long range inhibition. Dev. Biol. 194:1998;12-17.
48. Jonk L. J. C., de Jonge M. E. J., Kruyt F. A. E., Mummery C. L., van der Saag P. T., Kruijer W. Aggregation and cell cycle dependent retinoic acid receptor mRNA expression in P19 embryonal carcinoma cells. Mech. Dev. 36:1992;165-172.
49. Karin M., Liu Z. G., Zandi E. AP-1 function and regulation. Curr. Opin. Cell Biol. 9:1997;240-246.
50. Kim J., Johnson K., Chen H. J., Carroll S., Laughon A. Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature. 388:1997;304-308.
51. Kingsley D. M. The TGFβ superfamily: New members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8:1994;133-146.
52. Knecht A. K., Harland R. M. Mechanisms of dorsal-ventral patterning in noggin-induced neural tissue. Development. 124:1997;2477-2488.
53. Lau A. F., Kanemitsu M. Y., Kurata W. E., Danesh S., Boynton A. L. Epidermal growth factor disrupts gap junctional communication and induces phosphorylation of connexin43 on serine. Mol. Biol. Cell. 3:1992;865-874.
54. Lee Y. S., Chuong C. M. Activation of protein kinase A is a pivotal step involved in both BMP-2- and cyclic AMP-induced chondrogenesis. J. Cell Physiol. 170:1997;153-165.
55. Liberati N. T., Datto M. B., Frederick J. P., Shen X., Wong C., Rougier-Chapman E. M., Wang X. F. Smads bind directly to the Jun family of AP-1 transcription factors. Proc. Natl. Acad. Sci. USA. 96:1999;4844-4849.
56. Lefebvre D. L., Piersanti M., Bai X. H., Chen Z. Q., Lye S. J. Myometrial transcriptional regulation of the gap junction gene, connexin-43. Reprod. Fertil. Dev. 7:1995;603-611.
57. Lein P., Guo X., Hedges A. M., Rueger D., Johnson M., Higgins D. The effects of extracellular matrix and osteogenic protein-1 on the morphological differentiation of rat sympathetic neurons. Int. J. Dev. Neurosci. 14:1996;203-215.
58. Lein P., Johnson M., Guo X., Rueger D., Higgins D. Osteogenic protein-1 induces dendritic growth in rat sympathetic neurons. Neuron. 15:1995;597-605.
59. Lemaire P., Yasuo H. Developmental signalling: A careful balancing act. Curr. Biol. 8:1998;R228.
60. Li W., Cogswel C. A., LoTurco J. J. Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J. Neurosci. 18:1998;8853-8862.
61. Liu F., Hata A., Baker J. C., Doody J., Carcamo J., Harland R. M., Massague J. A human Mad protein acting as a BMP-regulated transcriptional activator. Nature. 381:1996;620-623.
62. Lo C. W. The role of gap junction membrane channels in development. J. Bioenerg. Biomemb. 28:1996;379-385.
63. Lois C., Garcia-Verdugo J. M., Alvarez-Buylla A. Chain migration of neuronal precursors. Science. 271:1996;978-981.
64. Lowenstein W. R. The cell-to-cell channel of gap junction. Cell. 48:1987;725-726.
65. Mabie P. C., Mehler M. F., Kessler J. A. Effects of bone morphogenetic 2 on rat embryonic ventral mesencephalon in vitro. Soc. Neurosci. Abstr. 20:1994;665.
66. Marazzi G., Wang Y., Sassoon D. Msx2 is a transcriptional regulator in the BMP4 mediated programmed cell death pathway. Dev. Biol. 186:1997;127-138.
67. Martin G. Teratocarcinomas and mammalian embryogenesis. Science (Wash. DC). 209:1980;768-775.
68. Massague J., Weis-Garcia F. Serine/threonine kinase receptors: mediators of transforming growth factor beta family signals. Cancer Surv. 27:1996;41-64.
69. McBurney M. W., Rogers B. J. Isolation of male embryonal carcinoma cells and their chromosome replication patterns. Dev. Biol. 89:1982;503-508.
70. Mehler M. F., Goldstein H., Kessler J. A. Effects of cytokines on CNS cells. Ranhosohoff R. M., Benveniste E. M. Cytokines and the CNS. 1996;115-150 CRC Press, Toronto.
71. Mehler M. B., Kessler J. A. Cytokines and neuronal differentiation. Crit. Rev. Neurobiol. 9:1995;419-446.
72. Mehler M. F., Mabie P. C., Zhang D., Kessler J. A. Bone morphogenetic proteins in the nervous system. Trends Neurosci. 20:1997;309-317.
73. Nadarajah B., Makarenkova H., Becker D. L., Evans W. H., Parnavelas J. G. Basic FGF increases communication between cells of the developing neocortex. J. Neurosci. 18:1998;7881-7890.
74. National Institutes of Health, 1998, Neurological Disorders and Stroke Division, Soc. Neurosci. Session, Los Angeles, CA.
75. Naus C. C. G., Bani-Yaghoub M. Gap junctions in the developing nervous system. Cell Biol. Int. 22:1998;751-763.
76. Olson D. J., Christian J. L., Moon R. D. Effects of Wnt-1 and related proteins on gap junctional communication in Xenopus embryos. Science. 252:1991;1173-1176.
77. Olson D. J., Moon R. T. Distinct effects of ectopic expression of Wnt-1, activin B, and bFGF on gap junctional permeability in 32-cell Xenopus embryos. Dev. Biol. 151:1992;204-212.
78. Paul D. L. New functions of gap junctions. Curr. Opin. Cell. Biol. 7:1995;665-672.
79. Peinado A., Yuste R., Katz L. C. Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron. 10:1993;103-114.
80. Piccolo S., Sasai Y., Lu B., De Robertis E. M. Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP4. Cell. 86:1996;589-598.
81. Riley E. H., Lane J. M., Urist M. R., Lyons K. M., Lieberman J. R. Bone morphogenetic protein-2: Biology and applications. Clin. Orthopaed. Rel. Res. 324:1996;39-46.
82. Robinson C. J. M., Scott P. H., Allan A. B., Jess T., Gould G. W., Plevin R. Treatment of vascular smooth muscle cells with antisense phosphorothioate oligodeoxynucleotides directed against p42 and p44 mitogen-activated protein kinase abolishes DNA synthesis in response to platelet-derived growth factors. Biochem. J. 320:1996;123-127.
83. Roelink H. Tripartite signaling of pattern: Interactions between Hedgehogs, BMPs and Wnts in the control of vertebrate development. Curr. Opin. Neurobiol. 6:1996;33-40.
84. Rogers M. B., Rosen V., Wozney J. M., Gudas L. J. Bone morphogenetic proteins-2 and -4 are involved in the retinoic acid-induced differentiation of embryonal carcinoma cells. Mol. Biol. Cell. 3:1992;189-196.
85. Rudnicki M. A., McBurney M. W. Cell culture methods and induction of differentiation of embryonal carcinoma cell lines. Robertson E. J. Teratocarcinoma and Embryonic Stem Cells: A Practical Approach. 1987;19-50 IRL Press, Washington.
86. Sale E. M., Atkinson P. G., Sale G. J. Requirement of MAP kinase for differentiation of fibroblasts to adipocytes, for insulin activation of p90 S6 kinase and for insulin or serum stimulation of DNA synthesis. EMBO J. 14:1995;674-684.
87. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning, A Laboratory Manual. 1989;7.3-7.84 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
88. Sasai Y., Lu B., Steinbeisser H., de Robertis E. M. Regulation of neural induction by the Chd and BMP-4 antagonistic patterning signals in Xenopus. Nature. 376:1995;333-336.
89. Schmitt J. M., Hwang K., Winn S. R., Hollinger J. O. Bone morphogenetic proteins: An update on basic biology and clinical relevance. J. Orthop. Res. 7:1999;269-278.
90. Shi X., Yang X., Chen D., Chang Z., Cao X. Smad1 interacts with homeobox DNA-binding proteins in bone morphogenetic protein signaling. J. Biol. Chem. 274:1999;13711-13717.
91. Slack R. S., Skerjanc I. S., Lach B., Craig J., Jardine K. Cells differentiating into neuroectoderm undergo apoptosis in the absence of functional retinoblastoma family proteins. J. Cell Biol. 129:1995;779-788.
92. Sohl G., Degen J., Teubner B., Willecke K. The murine gap junction gene connexin36 is highly expressed in mouse retina and regulated during brain development. FEBS Lett. 428:1998;27-31.
93. Tanabe Y., Jessel T. M. Diversity and pattern in the developing spinal cord. Science. 274:1996;1115-1123.
94. Turing A. M. The chemical basis of morphogenesis. Phil. Trans. R. Soc. Lond. B. 237:1952;37-72.
95. Ullrich A., Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell. 61:1990;203-212.
96. Urist M. R. Bone formation by autoinduction. Science. 150:1965;893-899.
97. Urist M. R., Mikulski A., Lietze A. Solubilized and insolubilized bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA. 76:1979;1828-1832.
98. Vaahtokari A., Aberg T., Jernvall J., Keranen S., Thesleff I. The enamel knot as a signaling centre in the developing mouse tooth. Mech. Dev. 54:1996;39-43.
99. Vaahtokari A., Aberg T., Thesleff I. Apoptosis in the developing tooth: Association with an embryonic signaling centre and supression by EGF and FGF. Development. 122:1996;121-129.
100. Vainio S., Karavanova I., Jowett A., Thesleff I. Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell. 75:1993;45-58.
101. Van der Heyden M. A. G., Rook M. B., Hermans M. P., Rijksen G., Boonstra J., Defize L. H. K., Destree H. J. Identification of connexin43 as a functional target for Wnt signalling. J. Cell Sci. 111:1998;1741-1749.
102. Varley J. E., McPherson C. E., Zou H., Niswander L., Maxwell G. D. Expression of a constitutively active type I BMP receptor using a retroviral vector promotes the development of adrenergic cells in neural crest cultures. Dev. Biol. 196:1998;107-118.
103. Walton P. A., Gould S. J., Subramani S., Feramisco J. R. Transport of microinjected alcohol oxidase from Pichia pastoris into vesicles in mammalian cells: Involvement of the peroxisomal targeting signal. J. Cell Biol. 118:1992;499-508.
104. Wang Y., Sassoon D. Ectoderm-mesenchyme and mesenchyme-mesenchyme interactions regulate Msx-1 expression and cellular differentiation in the murine limb bud. Dev. Biol. 168:1995;374-382.
105. Warner A. E. Permeability of gap junctions at the segmental border in insect epidermis. Cell. 28:1982;243-252.
106. Welch R. D., Jones A. L., Bucholz R. W., Reinert C. M., Tjia J. S., Pierce W. A., Wozney J. M., Li X. J. Effects of recombinant human bone morphogenetic protein-2 on fracture healing in a goat tibial fracture model. J. Bone Miner. Res. 13:1998;1483-1490.
107. White T. W., Paul D. L. Genetic diseases and gene knockouts reveal diverse connexin functions. Annu. Rev. Physiol. 61:1999;283-310.
108. Wilson P. A., Hemmati-Brivanlou A. Induction of epidermis and inhibition of neural fate by BMP4. Nature. 376:1995;331-333.
109. Winnier G., Blessing M., Labosky P. A., Hogan B. L. M. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9:1995;2105-2116.
110. Wolpert L. Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25:1969;1-47.
111. Wozney J. M., Rosen V., Celeste A. J., Mitsock L. M., Whitters M. J., Kriz R. W., Hewick R. M., Wang E. A. Novel regulators of bone formation: Molecular clones and activities. Science. 242:1988;1528-1534.
112. Wrana J. L., Attisano L. MAD-related proteins in TGF-beta signalling. Trends Genet. 12:1996;493-496.
113. Wrana J. L., Attisano L., Wieser R., Ventura F., Massague J. Mechanism of activation of the TGF-beta receptor. Nature. 370:1994;341-347.
114. Xu R. H., Kim J., Taira M., Zhan S., Redni D., Kung D. A dominant negative bone morphogenetic protein 4 receptor causes neutralization in Xenopus ectoderm. Biochem. Biophys. Res. Commun. 212:1995;212-219.
115. Xu R. H., Lechleider R. J., Shih H. M., Hao C. F., Sredni D., Roberts A. B., Kung H. F. Functional analysis of human Smad1: Role of the amino-terminal domain. Biochem. Biophys. Res. Commun. 258:1999;366-373.
116. Yamaguchi, Shirakabe K. K., Shibuya H., Irie K., Oishi I., Uenom N., Taniguchi T., Nishida E., Matsumoto K. Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science. 270:1995;2008-2011.
117. Yamaguchi K., Nagai S., Ninomiya-Tsuji J., Nishita M., Tamai K., Irie K., Ueno N., Nishida E., Shibuya H., Matsumoto K. XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB1-TAK1 in the BMP signaling pathway. EMBO J. 18:1999;179-187.
118. Yamashita H., Ten Dijke P., Heldin C. H., Miyazono K. Bone morphogenetic protein receptors. Bone. 19:1996;569-574.
119. Yeager M., Nicholson B. Structure of gap junction intercellular channels. Curr. Opin. Struct. Biol. 6:1996;183-192.
120. Yeager M., Unger V. M., Falk M. M. Synthesis, assembly and structure of gap junction intercellular channels. Curr. Opin. Struct. Biol. 8:1998;517-524.
121. Yu W., Dahl G., Werner R. The connexin43 gene is responsive to oestrogen. Proc. R. Soc. Lond. B. Biol. Sci. 255:1994;125-132.
122. Yuste R., Peinado A., Katz L. C. Neuronal domain in developing neocortex. Science. 257:1992;665-669.
123. Zang Z., Mehler M. F., Marmur R., Wozney J. M., Kessler J. A. Bone morphogenetic proteins are expressed in developing mouse brain and are neurotrophic in vitro. Soc. Neurosci. Abstr. 20:1994;1307.
124. Zhang D., Mehler M. F., Song Q., Kessler J. A. Development of bone morphogenetic protein receptors in the nervous system and possible roles in regulating trkC expression. J. Neurosci. 18:1998;3314-3326.
125. Zhu D., Kidder G. M., Caveney S., Naus C. C. G. Growth retardation in glioma cells cocultured with cells overexpressing a gap junction protein. Proc. Natl. Acad. Sci. USA. 89:1992;10218-10221.
126. Zimmerman C. M., Kariapper M. S., Mathews L. S. Smad proteins physically interact with calmodulin. J. Biol. Chem. 273:1998;677-680.