The TGFβ activated kinase TAK1 regulates vascular development in vivo

Development

Volumn 133, Issue 8, 2006, Pages 1529-1541

  Jadrich, Joy L ^a   O'Connor, Michael B ^a,c   Coucouvanis, Electra ^a,b,c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c RandD Systems Inc   (United States)

Author keywords

ALK1 (ACVRL1); Angiogenesis; HHT; TAK1 (MAP3K7); TGF

Indexed keywords

ENDOGLIN; MORPHOLINE DERIVATIVE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE FUNCTION; GENE INACTIVATION; GENE INSERTION; GENE MUTATION; GENE OVEREXPRESSION; HETEROZYGOSITY; IN VIVO STUDY; MOUSE; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; RENDU OSLER WEBER DISEASE; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE; VASODILATATION; VERTEBRATE; YOLK SAC; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; GENES, LETHAL; HEART; MALE; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MUSCLE, SMOOTH, VASCULAR; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; ZEBRAFISH;

ANIMALIA; DANIO RERIO; VERTEBRATA;

EID: 33646713486     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02333     Document Type: Article

References (88)

1. Adams, R. H., Porras, A., Alonso, G., Jones, M., Vintersten, K., Panelli, S., Valladares, A., Perez, L., Klein, R. and Nebreda, A. R. (2000). Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development. Mol. Cell 6, 109-116.
2. Arceci, R. J., King, A. A., Simon, M. C., Orkin, S. H. and Wilson, D. B. (1993). Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol. Cell. Biol. 13, 2235-2246.
3. Arthur, H. M., Ure, J., Smith, A. J., Renforth, G., Wilson, D. I., Torsney, E., Charlton, R., Parums, D. V., Jowett, T., Marchuk, D. A. et al. (2000). Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev. Biol. 217, 42-53.
4. Baldwin, H. S., Shen, H. M., Yan, H. C., DeLisser, H. M., Chung, A., Mickanin, C., Trask, I., Kirschbaum, N. E., Newman, P. J. and Albelda, S. M. (1994). Platelet endothelial cell adhesion molecule-1 (PECAM-1/ CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 120, 2539-2553.
5. Benus, G. F., Wierenga, A. T., de Gorter, D. J., Schuringa, J. J., van Bennekum, A. M., Drenth-Diephuis, L., Vellenga, E. and Eggen, B. J. (2005). Inhibition of the TGFß pathway by IL-1β Is mediated through TAK1 phosphorylation of SMAD3. Mol. Biol. Cell 16, 3501-3510.
6. Bourdeau, A., Dumont, D. J. and Letarte, M. (1999). A murine model of hereditary hemorrhagic telangiectasia. J. Clin. Invest. 104, 1343-1351.
7. Bradham, C. A., Hatano, E. and Brenner, D. A. (2001). Dominant-negative TAK1 induces c-Myc and G(O) exit in liver. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G1279-G1289.
8. Bruneau, B. G., Nemer, G., Schmitt, J. P., Charron, F., Robitaille, L., Caron, S., Conner, D. A., Gessler, M., Nemer, M., Seidman, C. E. and Seidman, J. G. (2001). A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106, 709-721.
9. Carson-Walter, E. B., Watkins, D. N., Nanda, A., Vogelstein, B., Kinzler, K. W. and St Croix, B. (2001). Cell surface tumor endothelial markers are conserved in mice and humans. Cancer Res. 61, 6649-6655.
10. Carvalho, R. L., Jonker, L., Goumans, M. J., Larsson, J., Bouwman, P., Karlsson, S., Dijke, P. T., Arthur, H. M. and Mummery, C. L. (2004). Defective paracrine signalling by TGFß in yolk sac vasculature of endoglin mutant mice: a paradigm for hereditary haemorrhagic telangiectasia. Development 131, 6237-6247.
11. Corson, L. B., Yamanaka, Y., Lai, K. M. and Rossant, J. (2003). Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development 130, 4527-4537.
12. Cross, J. C., Werb, Z. and Fisher, S. J. (1994). Implantation and the placenta: key pieces of the development puzzle. Science 266, 1508-1518.
13. Dickson, M. C., Martin, J. S., Cousins, F. M., Kulkarni, A. B., Karlsson, S. and Akhurst, R. J. (1995). Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121, 1845-1854.
14. Durocher, D., Chen, C. Y., Ardati, A., Schwartz, R. J. and Nemer, M. (1996). The atrial natriuretic factor promoter is a downstream target for Nkx-2.5 in the myocardium. Mol. Cell. Biol. 16, 4648-4655.
15. Eckfeldt, C. E., Mendenhall, E. M., Flynn, C. M., Wang, T., Pickart, M., Grindle, S. M., Ekker, S. C. and Vervaillie, C. M. (2005). Functional analysis of human hematopoietic stem cell gene expression using zebrafish. PLoS Biol. 3, e254.
16. Flamme, I., Frolich, T. and Risau, W. (1997). Molecular mechanisms of vasculogenesis and embryonic angiogenesis. J. Cell. Physiol. 173, 206-210.
17. Freemark, M., Driscoll, P., Maaskant, R., Petryk, A. and Kelly, P. A. (1997). Ontogenesis of prolactin receptors in the human fetus in early gestation. Implications for tissue differentiation and development. J. Clin. Invest. 99, 1107-1117.
18. Goumans, M. J., Valdimarsdottir, G., Itoh, S., Rosendahl, A., Sideras, P. and ten Dijke, P. (2002). Balancing the activation state of the endothelium via two distinct TGF-beta type 1 receptors. EMBO J. 21, 1743-1753.
19. Goumans, M. J., Valdimarsdottir, G., Itoh, S., Lebrin, F., Larsson, J., Mummery, C., Karlsson, S. and ten Dijke, P. (2003). Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol. Cell 12, 817-828.
20. Hanafusa, H., Ninomiya-Tsuji, J., Masuyama, N., Nishita, M., Fujisawa, J., Shibuya, H., Matsumoto, K. and Nishida, E. (1999). Involvement of the p38 mitogen-activated protein kinase pathway in transforming growth factor-beta-induced gene expression. J. Biol. Chem. 274, 27161-27167.
21. Hanks, S. K., Quinn, A. M. and Hunter, T. (1988). The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42-52.
22. Hirakow, R. and Hiruma, T. (1981). Scanning electron microscopic study on the development of primitive blood vessels in chick embryos at the early somite-stage. Anat. Embryol. (Berl.) 163, 299-306.
23. Hirschi, K. K., Rohovsky, S. A. and D'Amore, P. A. (1998). PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J. Cell Biol. 141, 805-814.
24. Hoffmann, A., Preobrazhenska, O., Wodarczyk, C., Medler, Y., Winkel, A., Shahab, S., Huylebroeck, D., Gross, G. and Verschueren, K. (2005). Transforming growth factor-beta-activated kinase-1 (TAK1), a MAP3K, interacts with Smad proteins and interferes with osteogenesis in murine mesenchymal progenitors. J. Biol. Chem. 280, 27271-27283.
25. Hogan, B., Beddington, R., Costantini, F. and and Lacy, E. (1994). Manipulating the Mouse Embryo - A Laboratory Manual. New York, NY: Cold Spring Harbor Laboratory Press.
26. Hyatt, T. M. and Ekker, S. C. (1999). Vectors and techniques for ectopic gene expression in zebrafish. Methods Cell Biol. 59, 117-126.
27. Ihle, J. N. (2000). The challenges of translating knockout phenotypes into gene function. Cell 102, 131-134.
28. Ishitani, T., Kishida, S., Hyodo-Miura, J., Ueno, N., Yasuda, J., Waterman, M., Shibuya, H., Moon, R. T., Ninomiya-Tsuji, J. and Matsumoto, K. (2003). The TAK1 -NLK mitogen-activated protein kinase cascade functions in the Wnt5a/Ca(2+) pathway to antagonize Wnt/ beta-catenin signaling. Mol. Cell. Biol. 23, 131-139.
29. Jadrich, J. L., O'Connor, M. B. and Coucouvanis, E. (2003). Expression of TAK1, a mediator of TGF-beta and BMP signaling, during mouse embryonic development. Gene Expr. Patterns 3, 131-134.
30. Kim, S. and Iwao, H. (2003). Stress and vascular responses: mitogen-activated protein kinases and activator protein-1 as promising therapeutic targets of vascular remodeling. J. Pharmacol. Sci. 91, 177-181.
31. Kuo, C. T., Morrisey, E. E., Anandappa, R., Sigrist, K., Lu, M. M., Parmacek, M. S., Soudais, C. and Leiden, J. M. (1997). GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 11, 1048-1060.
32. Laird, P. W., Zijderveld, A., Linders, K., Rudnicki, M. A., Jaenisch, R. and Berns, A. (1991). Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19, 4293.
33. Larsson, J., Goumans, M. J., Sjostrand, L. J., van Rooijen, M. A., Ward, D., Leveen, P., Xu, X., ten Dijke, P., Mummery, C. L. and Karlsson, S. (2001). Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type 1 receptor-deficient mice. EMBO J. 20, 1663-1673.
34. Lebrin, F., Goumans, M. J., Jonker, L., Carvalho, R. L., Valdimarsdottir, G., Thorikay, M., Mummery, C., Arthur, H. M. and Dijke, P. T. (2004). Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J. 23, 4018-4028.
35. Lebrin, F., Deckers, M., Bertolino, P. and Ten Dijke, P. (2005). TGF-beta receptor function in the endothelium. Cardiovasc. Res. 65, 599-608.
36. Lele, Z., Bakkers, J. and Hammerschmidt M. (2001). Morpholino phenocopies of the swirl, snailhouse, somitabun, minifin, silberblick, and pipetail mutations. Genesis 30, 190-194.
37. Letamendia, A., Lastres, P., Botella, L. M., Raab, U., Langa, C., Velasco, B., Attisano, L. and Bernabeu, C. (1998). Role of endoglin in cellular responses to transforming growth factor-beta. A comparative study with betaglycan. J. Biol. Chem. 273, 33011-33019.
38. Li, D. Y., Sorensen, L. K., Brooke, B. S., Urness, L. D., Davis, E. C., Taylor, D. G., Boak, B. B. and Wendel, D. P. (1999). Defective angiogenesis in mice lacking endoglin. Science 284, 1534-1537.
39. Liu, F. (2003). Receptor-regulated Smads in TGF-beta signaling. Front. Biosci. 8, s1280-s1303.
40. Mann, C. J., Honeyman, K., Cheng, A. J., Ly, T., Lloyd, F., Fletcher, S., Morgan, J. E., Partridge, T. A. and Wilton, S. D. (2001). Antisense-induced exon skipping and synthesis of dystrophin in the mdx mouse. Proc. Natl. Acad. Sci. USA 98, 42-47.
41. Massague, J. (1998). TGF-beta signal transduction. Annu. Rev. Biochem. 67, 753-791.
42. Meneghini, M. D., Ishitani, T., Carter, J. C., Hisamoto, N., Ninomiya-Tsuji, J., Thorpe, C. J., Hamill, D. R., Matsumoto, K. and Bowerman, B. (1999). MAP kinase and Wnt pathways converge to downregulate an HMG-clomain repressor in Caenorhabditis elegans. Nature 399, 793-797.
43. Molkentin, J. D., Lin, Q., Duncan, S. A. and Olson, E. N. (1997). Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11, 1061-1072.
44. Monzen, K., Shiojima, I., Hiroi, Y., Kudoh, S., Oka, T., Takimoto, E., Hayashi, D., Hosoda, T., Habara-Ohkubo, A. and Nakaoka, T. et al. (1999). Bone morphogenetic proteins induce cardiomyocyte differentiation through the mitogen-activated protein kinase kinase kinase TAK1 and cardiac transcription factors Csx/Nkx-2.5 and GATA-4. Mol. Cell. Biol. 19, 7096-7105.
45. Monzen, K., Hiroi, Y., Kudoh, S., Akazawa, H., Oka, T., Takimoto, E., Hayashi, D., Hosoda, T., Kawabata, M. and Miyazono, K. et al. (2001). Smads, TAK1, and their common target ATF-2 play a critical role in cardiomyocyte differentiation. J. Cell Biol. 153, 687-698.
46. Moriguchi, T., Kuroyanagi, N., Yamaguchi, K., Gotoh, Y., Irie, K., Kano, T., Shirakabe, K., Muro, Y., Shibuya, H., Matsumoto, K., Nishida, E. and Hagiwara, M. (1996). A novel kinase cascade mediated by mitogen-activated protein kinase kinase 6 and MKK3. J. Biol. Chem. 271, 13675-13679.
47. Mudgett, J. S., Ding, J., Guh-Siesel, L., Chartrain, N. A., Yang, L., Gopal, S. and Shen, M. M. (2000). Essential role for p38alpha mitogen-activated protein kinase in placental angiogenesis. Proc. Natl. Acad. Sci. USA 97, 10454-10459.
48. Mulder, K. M. (2000). Role of Ras and Mapks in TGFbeta signaling. Cytokine Growth Factor Rev. 11, 23-35.
49. Ninomiya-Tsuji, J., Kishimoto, K., Hiyama, A., Inoue, J., Cao, Z. and Matsumoto, K. (1999). The kinase TAK1 can activate the NIK-1 kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398, 252-256.
50. Nohe, A., Hassel, S., Ehrlich, M., Neubauer, F., Sebald, W., Henis, Y. I. and Knaus, P. (2002). The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J. Biol. Chem. 277, 5330-5338.
51. Oh, S. P., Seki, T., Goss, K. A., Imamura, T., Yi, Y., Donahoe, P. K., Li, L., Miyazono, K., ten Dijke, P., Kim, S. and Li, E. (2000). Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc. Natl. Acad. Sci. USA 97, 2626-2631.
52. Ohkawara, B., Shirakabe, K., Hyodo-Miura, J., Matsuo, R., Ueno, N., Matsumoto, K. and Shibuya, H. (2004). Role of the TAK1-NLK-STAT3 pathway in TGF-beta-mediated mesoderm induction. Genes Dev. 18, 381-386.
53. Ono, K., Ohtomo, T., Ninomiya-Tsuji, J. and Tsuchiya, M. (2003). A dominant negative TAK1 inhibits cellular fibrotic responses induced by TGF-beta. Biochem. Biophys. Res. Commun. 307, 332-337.
54. Oshima, M., Oshima, H. and Taketo, M. M. (1996). TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev. Biol. 179, 297-302.
55. Owens, G. K., Kumar, M. S. and Wamhoff, B. R. (2004). Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801.
56. Park, J. M., Brady, H., Ruocco, M. G., Sun, H., Williams, D., Lee, S. J., Kato, T., Jr, Richards, N., Chan, K., Mercurio, F., Karin, M. and Wasserman, S. A. (2004). Targeting of TAK1 by the NF-kappa B protein Relish regulates the JNK-mediated immune response in Drosophila. Genes Dev. 18, 584-594.
57. Parlakian, A., Tuil, D., Hamard, G., Tavernier, G., Hentzen, D., Concordet, J. P., Paulin, D., Li, Z. and Daegelen, D. (2004). Targeted inactivation of serum response factor in the developing heart results in myocardial defects and embryonic lethality. Mol. Cell. Biol. 24, 5281-5289.
58. Pepper, M. S. (1997). Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity Cytokine Growth Factor Rev. 8, 21-43.
59. Pepper, M. S. (2001). Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler. Thromb. Vasc. Biol. 21, 1104-1117.
60. Plauchu, H., de Chadarevian, J. P., Bideau, A. and Robert, J. M. (1989). Age-related clinical profile of hereditary hemorrhagic telangiectasia in an epidemiologically recruited population. Am. J. Med. Genet. 32, 291-297.
61. Risau, W. (1997). Mechanisms of angiogenesis. Nature 386, 671-674.
62. Risau, W. and Flamme, I. (1995). Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11, 73-91.
63. Roman, B. L., Pham, V. N., Lawson, N. D., Kulik, M., Childs, S., Lekven, A. C., Garrity, D. M., Moon, R. T., Fishman, M. C., Lechleider, R. J. and Weinstein, B. M. (2002). Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129, 3009-3019.
64. Rossant, J. and Cross, J. C. (2001). Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2, 538-548.
65. Sano, Y., Harada, J., Tashiro, S., Gotoh-Mandeville, R., Maekawa, T. and Ishii, S. (1999). ATF-2 is a common nuclear target of Smad and TAK1 pathways in transforming growth factor-beta signaling. J. Biol. Chem. 274, 8949-8957.
66. Sato, S., Sanjo, H., Takeda, K., Ninomiya-Tsuji, J., Yamamoto, M., Kawai, T., Matsumoto, K., Takeuchi, O. and Akira, S. (2005). Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 11, 1087-1095.
67. Seki, T., Yun, J. and Oh, S. P. (2003). Arterial endothelium-specific activin receptor-like kinase 1 expression suggests its role in arterialization and vascular remodeling. Circ. Res. 93, 682-689.
68. Seki, T., Hong, K. H. and Oh, S. P. (2006). Nonoverlapping expression patterns of ALK1 and ALK5 reveal distinct roles of each receptor in vascular development. Lab Invest. 86, 116-129.
69. Shi, Y. and Massague, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113, 685-700.
70. Shibuya, H., Iwata, H., Masuyama, N., Gotoh, Y., Yamaguchi, K., Irie, K., Matsumoto, K., Nishida, E. and Ueno, N. (1998). Role of TAK1 and TAB1 in BMP signaling in early Xenopus development. EMBO J. 17, 1019-1028.
71. Shim, J., Xiao, C., Paschal, A. E., Bailey, S. T., Rao, P., Hayden, M. S., Lee, K., Bussey, C., Steckel, M., Tanaka, N., Yamada, G., Akira, S., Matsumoto, K. and Ghosh, S. (2005). Tak1, but not TAB1 or Tab2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19, 2668-2681.
72. Shirakabe, K., Yamaguchi, K., Shibuya, H., Irie, K., Matsuda, S., Moriguchi, T., Gotoh, Y., Matsumoto, K. and Nishida, E. (1997). TAK1 mediates the ceramide signaling to stress-activated protein kinase/c-Jun N-terminal kinase. J. Biol. Chem. 272, 8141-8144.
73. Srinivasan, S., Hanes, M. A., Dicken, T., Porteous, M. E., Oh, S. P., Hale, L. P. and Marchuk, D. A. (2003). A mouse model for hereditary hemorrhagic telangiectasia (HHT) type 2. Hum. Mol. Genet. 12, 473-482.
74. St Croix, B., Rago, C., Velculescu, V., Traverso, G., Romans, K. E., Montgomery, E., Lal, A., Riggins, G. J., Lengauer, C., Vogelstein, B. and Kinzlier, K. W. (2000). Genes expressed in human tumor endothelium. Science 289, 1197-1202.
75. Stryke, D., Kawamoto, M., Huang, C. C., Johns, S. J., King, L. A., Harper, C. A., Meng, E. C., Lee, R. E., Yee, A. and L'Italien, L. et al. (2003). BayGenomics: a resource of insertional mutations in mouse embryonic stem cells. Nucleic Acids Res. 31, 278-281.
76. Takahashi, Y., Imanaka, T. and Takano, T. (1996). Spatial and temporal pattern of smooth muscle cell differentiation during development of the vascular system in the mouse embryo. Anat. Embryol. (Bert.) 194, 515-526.
77. Urness, L. D., Sorensen, L. K. and Li, D. Y. (2000). Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat. Genet. 26, 328-331.
78. van den Driesche, S., Mummery, C. L. and Westermann C. J. (2003). Hereditary hemorrhagic telangiectasia: an update on transforming growth factor beta signaling in vasculogenesis and angiogenesis. Cardiovasc. Res. 58, 20-31.
79. Vidal, S., Khush, R. S., Leulier, F., Tzou, P., Nakamura, M. and Lemaitre, B. (2001). Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/NF-kappaB-dependent innate immune responses. Genes Dev. 15, 1900-1912.
80. Wallace, G. M. and Shovlin, C. L. (2000). A hereditary haemorrhagic telangiectasia family with pulmonary involvement is unlinked to the known HHT genes, endoglin and ALK-1. Thorax 55, 685-690.
81. Wilkinson, D. G. and Nieto, M. A. (1993). Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 225, 361-373.
82. Yamaguchi, K., Shirakabe, K., Shibuya, H., Irie, K., Oishi, I., Ueno, N., Taniguchi, T., Nishida, E. and Matsumoto, K. (1995). Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 270, 2008-2011.
83. Yang, X., Castilla, L. H., Xu, X., Li, C., Gotay, J., Weinstein, M., Liu, P. P. and Deng, C. X. (1999). Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development 126, 1571-1580.
84. Yue, J. and Mulder, K. M. (2000). Requirement of Ras/MAPK pathway activation by transforming growth factor beta for transforming growth factor beta 1 production in a smad-dependent pathway. J. Biol. Chem. 275, 30765-30773.
85. Yue, J., Sun, B., Liu, G. and Mulder, K. M. (2004). Requirement of TGF-beta receptor-dependent activation of c-Jun N-terminal kinases (JNKs)/stress-activated protein kinases (Sapks) for TGF-beta up-regulation of the urokinase-type plasminogen activator receptor. J. Cell. Physiol. 199, 284-292.
86. Zeller, R., Bloch, K. D., Williams, B. S., Arceci, R. J. and Seidman, C. E. (1987). Localized expression of the atrial natriuretic factor gene during cardiac embryogenesis. Genes Dev. 1, 693-698.
87. Zhang, D., Gaussin, V., Taffet, G. E., Belaguli, N. S., Yamada, M., Schwartz, R. J., Michael, L. H., Overbeek, P. A. and Schneider, M. D. (2000). TAK1 is activated in the myocardium after pressure overload and is sufficient to provoke heart failure in transgenic mice. Nat. Med. 6, 556-563.
88. Zhang, Y., Feng, X. H. and Derynck, R. (1998). Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-beta-induced transcription. Nature 394, 909-913.