Functional antagonism between activin and osteogenic protein-1 in human embryonal carcinoma cells

Journal of Cellular Physiology

Volumn 180, Issue 2, 1999, Pages 141-149

  Piek, Ester ^a,b   Afrakhte, Mozhgan ^c   Sampath, Kuber ^d   Van Zoelen, E Joop ^a   Heldin, Carl Henrik ^b   Dijke, Peter Ten ^b  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^c UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^d CURIS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; ACTIVIN RECEPTOR; ALKALINE PHOSPHATASE; OSTEOGENIC PROTEIN 1; PLASMINOGEN ACTIVATOR INHIBITOR 1;

ARTICLE; BINDING COMPETITION; CROSS LINKING; DOSE RESPONSE; EMBRYONAL CARCINOMA; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ACTIVIN RECEPTORS, TYPE I; ACTIVIN RECEPTORS, TYPE II; ACTIVINS; ALKALINE PHOSPHATASE; BLOTTING, NORTHERN; BONE MORPHOGENETIC PROTEINS; DNA-BINDING PROTEINS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REPORTER; GROWTH SUBSTANCES; HUMANS; INHIBINS; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-JUN; RECEPTORS, GROWTH FACTOR; RNA, MESSENGER; SMAD6 PROTEIN; SMAD7 PROTEIN; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED; TUMOR STEM CELLS;

EID: 0032990886     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199908)180:2<141::AID-JCP1>3.0.CO;2-I     Document Type: Article

References (66)

1. Afrakhte M, Morén A, Jossan S, Itoh S, Sampath K, Westermark B, Heldin C-H, Heldin N-E, ten Dijke, P. 1998. Induction of inhibitory Smad6 and Smad7 mRNA by TGF-β family members. Biochem Biophys Res Commun 249:505-511.
2. Andrews PW. 1988. Human teratocarcinomas. Biochim Biophys Acta 948:17-36.
3. Andrews PW, Damjanov I, Simon D, Banting GS, Carlin C, Dracopoli NC, Fogh J. 1984. Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2: differentiation in vivo and in vitro. Lab Invest 50:147-162.
4. Andrews PW, Damjanov I, Berends J, Kumpf S, Zappavigna V, Mavilio F, Sampath K. 1994. Inhibition of proliferation and induction of differentiation of pluripotent human embryonal carcinoma cells by osteogenic protein-1 (or bone morphogenetic protein-7). Lab Invest 71:243-251.
5. Asashima M, Nakano H, Shimada K, Kinoshita K, Ishii K, Shibai H, Ueno N. 1990. Mesodermal induction in early amphibian embryos by activin A (erythroid differentiation factor). Roux's Arch Dev Biol 198:330-335.
6. Attisano L, Wrana JL, Cheifetz S, Massagué J. 1992. Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 68:97-108.
7. Attisano L, Cárcamo J, Ventura F, Weis FMB, Massagué J, Wrana JL. 1993. Identification of human activin and TGFβ type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75:671-680.
8. Candia AF, Watabe T, Hawley SHB, Onichtchouk D, Zhang Y, Derynck R, Niehrs C, Cho KWY. 1997. Cellular interpretation of multiple TGF-β signals: intracellular antagonism between activin/BVg1 and BMP-2/4 signaling mediated by Smads. Development 12:4467-4480.
9. Caricasole AAD, van Schaik RHN, Zeinstra LM, Wierikx CDJ, van Gurp RJHLM, van den Pol M, Looijenga LHJ, Oosterhuis JW, Pera MF, Ward A, de Bruijn D, Kramer P, de Jong FH, van den Eijndenvan Raaij AJM. 1998. Human growth-differentiation factor 3 (hGDF3): developmental regulation in human teratocarcinoma cell lines and expression in primary testicular germ cell tumours. Oncogene 16:95-103.
10. Cunningham NS, Paralkar V, Reddi AH. 1992. Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor β1 mRNA expression. Proc Natl Acad Sci USA 89:11740-11744.
11. Findlay J. 1993. An update on the roles of inhibin, activin and follistatin as local regulators of folliculogenesis. Biol Reprod 48:15-23.
12. Frolik CA, Wakefield LM, Smith DM, Sporn MB. 1984. Characterization of a membrane receptor for transforming growth factor-β in normal rat kidney fibroblasts. J Biol Chem 259:10995-11000.
13. Glozak MA, Rogers MB. 1996. Specific induction of apoptosis in P19 embryonal carcinoma cells by retinoic acid and BMP2 or BMP4. Dev Biol 179:458-470.
14. Hashimoto M, Nakamura T, Inoue S, Kondo T, Yamada R, Eto Y, Sugino H, Muramatsu M. 1992. Follistatin is a developmentally regulated cytokine in neural differentiation. J Biol Chem 267:7203-7206.
15. Hashimoto M, Gaddy-Kurten D, Vale W. 1993. Protooncogene junB as a target for activin actions. Endocrinology 133:1934-1940.
16. Hata A, Lagna G, Massagué J, Hemmati-Brivanlou A. 1998. Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 12:186-197.
17. Hayashi H, Abdollah S, Qiu YB, Cai JX, Xu YY, Grinnell BW, Richardson MA, Topper JN, Gimbrone MA, Wrana JL, Falb D. 1997. The Mad related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell 89:1165-1173.
18. Heldin C-H, Miyazono K, ten Dijke P. 1997. TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390: 465-471.
19. Hogan BLM. 1996. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 10:1580-1594.
20. Hoodless PA, Haerry T, Abdollah S, Stapleton M, O'Connor MB, Attisano L, Wrana JL. 1996. MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85:489-500.
21. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, Miyazono K. 1997. Smad6 inhibits signalling by the TGF-β superfamily. Nature 389:622-626.
22. Knezevic V, Ranson M, Mackem S. 1995. The organizer-associated chick homeobox gene, Gnot1, is expressed before gastrulation and regulated synergistically by activin and retinoic acid. Dev Biol 171:458-470.
23. Laiho M, Keski-Oja J. 1989. Growth factors in the regulation of pericellular proteolysis. A review. Cancer Res 49:2533-2553.
24. Lebrun JJ, Vale WW. 1997. Activin and inhibin have antagonistic effects on ligand-dependent heteromerization of the type I and type II activin receptors and human erythroid differentiation. Mol Cell Biol 17:1682-1691.
25. Ling N, Ying S-Y, Ueno N, Simasaki S, Esch F, Hotta M, Guillemin R. 1986. Pituitary FSH is released by a heterodimer of the β-subunits from the two forms of inhibin. Nature 321:779-782.
26. Liu F, Ventura F, Doody J, Massagué J. 1995. Human type II receptor for bone morphogenetic proteins (BMPs): extension of the two-kinase receptor model to the BMPs. Mol Cell Biol 15:3479-3486.
27. Löwik CWGM, Alblas MJ, van de Ruit M, Papapoulos SE, van der Pluijm G. 1993. Quantification of adherent and nonadherent cells cultured in 96-well plates using the supravital stain neutral red. Anal Biochem 213:426-433.
28. Macías-Silva M, Hoodless PA, Tang SJ, Buchwald M, Wrana JL. 1998. Specific activation of Smad1 signaling pathways by the BMP7 type I receptor, ALK2. J Biol Chem 273:25628-25636.
29. Massagué J. 1998. TGF-β signal transduction. Annu Rev Biochem 67:753-791.
30. Mathews LS. 1994. Activin receptors and cellular signaling by the receptor serine kinase family. Endocr Rev 15:310-325.
31. Mathews LS, Vale WW. 1991. Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65:973-982.
32. Mathews LS, Vale WW, Kintner CR. 1992. Cloning of a second type of activin receptor and functional characterization in Xenopus embryos. Science 255:1702-1705.
33. Momoi T, Kawai Y, Momoi M, Etoh Y. 1992. Activin synergistically increased c-jun mRNA in P19 embryonal carcinoma cells in the presence of retinoic acid. Biochem Biophys Res Commun 184:1350-1356.
34. Nakao A, Afrakhte M, Morén A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin N-E, Heldin C-H, ten Dijke P. 1997a. Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 389:631-635.
35. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J-I, Heldin C-H, Miyazono K, ten Dijke P. 1997b. TGF-β receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16:5353-5362.
36. Paralkar VM, Weeks BS, Yu YM, Kleinman HK, Reddi AH. 1992. Recombinant human bone morphogenetic protein 2B stimulates PC12 cell differentiation: potentiation and binding to type IV collagen. J Cell Biol 119:1721-1728.
37. Pendes G, Safran RM, Downing LA, Charness ME. 1994. Regulation of neural cell adhesion molecule and L1 by the transforming growth factor-β superfamily: selective effects of the bone morphogenetic proteins. J Biol Chem 269:765-770.
38. Pertovaara L, Sistonen L, Bos TJ, Vogt PK, Keski-Oja J, Alitalo K. 1989. Enhanced jun gene expression is an early genomic response to transforming growth factor β stimulation. Mol Cell Biol 9:1255-1262.
39. Piek E, Franzén P, Heldin C-H, ten Dijke P. 1997. Characterization of a 60-kDa cell surface-associated transforming growth factor-β binding protein that can interfere with transforming growth factor-β receptor binding. J Cell Physiol 173:447-459.
40. Reddi AH. 1997. Bone morphogenetic proteins: an unconventional approach to isolation of first mammalian morphogens. Cytokine Growth Factor Rev 8:11-20.
41. Roberts AB, Sporn MB. 1990. Transforming growth factor-βs. In: Sporn MB, Roberts AB, editors. Peptide growth factors and their receptors: Part 1. Berlin: Springer Verlag, p 419-472.
42. Rosenzweig BL, Imamura T, Okadome T, Cox GN, Yamashita H, ten Dijke P, Heldin C-H, Miyazono K. 1995. Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc Natl Acad Sci USA 92:7632-7636.
43. Scheibe RJ, Möller-Runge I, Müller WH. 1991. Retinoic acid induces the expression of alkaline phosphatase in P19 teratocarcinoma cells. J Biol Chem 266:21300-21305.
44. Schubert D, Kimura H, LaCorbiere M, Vaughan J, Karr D, Fisher W. 1990. Activin is a nerve cell survival molecule. Nature 330:765-767.
45. Shiozaki M, Sakai R, Tabuchi M, Nakamura T, Sugino K, Sugino H, Eto Y. 1992. Evidence for the participation of endogenous activin A/erythroid differentiation factor in the regulation of erythropoiesis. Proc Natl Acad Sci USA 89:1553-1556.
46. Smith JC, Price BMJ, Van Nimmen K, Huylebroeck D. 1990. Identification of potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature 345:729-731.
47. Souchelnytskyi S, Nakayama T, Nakao A, Morén A, Heldin C-H, Christian JL, ten Dijke P. 1998. Physical and functional interaction of mouse and Xenopus Smad7 with bone morphogenetic protein receptors and transforming growth factor-β receptors. J Biol Chem 273:25364-25370.
48. Takase M, Imamura T, Sampath TK, Takeda K, Ichijo H, Miyazono K, Kawabata M. 1998. Induction of Smad6 mRNA by bone morphogenetic proteins. Biochem Biophys Res Commun 244:26-29.
49. ten Dijke P, Yamashita H, Ichijo H, Franzén P, Laiho M, Miyazono K, Heldin C-H. 1994a. Characterization of type I receptors for transforming growth factor-β and activin. Science 264:101-104.
50. ten Dijke P, Yamashita H, Sampath TK, Reddi AH, Estevez M, Riddle DL, Ichijo H, Heldin C-H, Miyazono K. 1994b. Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J Biol Chem 269:16985-16988.
51. Thompson S, Stern PL, Webb M, Walsh FS, Engström W, Evans EP, Shi WK, Hopkins B, Graham CF. 1984. Cloned human teratoma cells differentiate into neuron-like cells and other cell types in retinoic acid. J Cell Sci 72:37-64.
52. Thomsen G, Wool T, Whiteman M, Sokol S, Vaughan J, Vale W, Melton DA. 1990. Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 63:485-493.
53. Tienari J, Alanko T, Lehtonen E, Saksela O. 1991. The expression and localization of urokinase-type plasminogen activator and its type I inhibitor are regulated by retinoic acid and fibroblast growth factor in human teratocarcinoma cells. Cell Regul 2:285-297.
54. Vale W, Rivier J, Vaughan J, McClintock R, Corrigan A, Woo W, Karr D, Spiess J. 1986. Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature 321: 776-779.
55. van den Eijnden-van Raaij AJ, van Zoelent EJ, van Nimmen K, Koster CH, Snoek GT, Durston AJ, Huylebroeck D. 1990. Activin-like factor from a Xenopus laevis cell line responsible for mesoderm induction. Nature 345:732-734.
56. van den Eijnden-van Raaij AJ, van Achterberg TA, van der Kruijssen CM, Piersma AH, Huylebroeck D, de Laat SW, Mummery CL. 1991. Differentiation of aggregated murine P19 embryonal carcinoa cells is induced by a novel visceral endoderm-specific FGF-like factor and inhibited by activin A. Mech Dev 33:157-165.
57. van der Plas A, Aarden EM, Feijen JHM, de Boer AH, Wiltink A, Alblas MJ, de Leij L, Nijweide PJ. 1994. Characteristics and properties of osteocytes in culture. J Bone Miner Res 9:1697-1704.
58. Vidricaire G, Jardine K, McBurney MW. 1994. Expression of the Brachyury gene during mesoderm development in differentiating embryonal carcinoma cell cultures. Development 120:115-122.
59. Vukicevic S, Luyten FP, Reddi AH. 1989. Stimulation of the expression of osteogenic and chondrogenic phenotypes in vitro by osteogenin. Proc Natl Acad Sci USA 86:8793-8797.
60. Weima SM, van Rooijen MA, Feijen A, Mummery CL, van Zoelen EJJ, de Laat SW, van den Eijnden-van Raaij AJM. 1989. Transforming growth factor-β and its receptor are differentially regulated in human embryonal carcinoma cells. Differentiation 41:245-253.
61. Whitman M. 1998a. Feedback from inhibitory SMADs. Nature 389: 549-551.
62. Whitman M. 1998b. Smads and early developmental signaling by the TGFβ superfamily. Genes Dev 12:2445-2462.
63. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA. 1988. Novel regulators of bone formation: molecular clones and activities. Science 242:1528-1534.
64. Xu J, McKeehan K, Matsuzaki K, McKeehan WL. 1995. Inhibin antagonizes inhibition of liver cell growth by activin by a dominant-negative mechanism. J Biol Chem 270:6308-6313.
65. Yamashita H, ten Dijke P, Huylebroeck D, Sampath TK, Andries M, Smith JC, Heldin C-H, Miyazono K. 1995. Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J Cell Biol 130:217-226.
66. Zhou H, Manji SS, Findlay DM, Martin TJ, Heath JK, Wah Ng K. 1994. Novel action of retinoic acid. Stabilization of newly synthesized alkaline phosphatase transcripts. J Biol Chem 269:22433-22439.