Activin/inhibin βB subunit gene disruption leads to defects in eyelid development and female reproduction

Genes and Development

Volumn 8, Issue 4, 1994, Pages 414-427

  Vassalli, Anne ^a,b   Matzuk, Martin M ^c   Gardner, Humphrey A R ^a   Lee, Kuo Fen ^a   Jaenisch, Rudolf ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

activin B inhibin B; eyelid fusion; female reproduction; gene targeting; Mouse

Indexed keywords

ACTIVIN; INHIBIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONGENITAL MALFORMATION; DEVELOPMENTAL DISORDER; EMBRYO DEVELOPMENT; EYE MALFORMATION; EYELID; FEMALE; FEMALE FERTILITY; GENE MUTATION; MALE; MOUSE; NONHUMAN; PERINATAL MORTALITY; PRIORITY JOURNAL;

ANIMALIA; VERTEBRATA;

EID: 0028176755     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.8.4.414     Document Type: Article

References (71)

1. Albano, R.M., S.F. Godsave, D. Huylebroeck, K. Van Nimmen, H.V. Isaacs; J.M. Slack, and J.C. Smith. 1990. A mesoderm-inducing factor produced by WEHI-3 murine myelomonocytic leukemia cells is activin A. Development 110: 435-443.
2. Albano, R.M., N. Groome, and J.C. Smith. 1993. Activins are expressed in preimplantation mouse embryos and in ES and EC cells and are regulated on their differentiation. Development 117: 711-723.
3. Asashima, M.; H. Nakano, K. Shimada, K. Kinoshita, K. Ishii, H. Shibai, and N. Ueno. 1990. Mesodermal induction in early amphibian embryos by activin A (erythroid differentiation factor). Wilhelm Roux's Arch. Dev. Biol. 198: 330-335.
4. Asashima, M., H. Nakano, H. Uchiyama, H. Sugino, T. Nakamura, Y. Eto, D. Ejima, S. Nishimatsu, N. Ueno, and K. Kinoshita. 1991. Presence of activin (erythroid differentiation factor) in unfertilized eggs and blastulae of Xenopus laevis. Proc. Natl. Acad. Sci. 88: 6511-6514.
5. Bradley, A. 1987. Production and analysis of chimaeric mice. In Teratocarcinomas and embryonic stem cells: A practical approach (ed. E. J. Robertson), IRL Press, Oxford, England.
6. Cho, K.W., B. Blumberg, H. Steinbeisser, and E. De Robertis. 1991. Molecular nature of Spemann's organizer; The role of the Xenopus homeobox gene goosecoid. Cell 67: 1111-1120.
7. Chomczynski, P. and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal Biochem. 162: 156-159.
8. Dale, L., G. Howes, B.M. Price, and J.C. Smith. 1992. Bone morphogenetic protein 4: A ventralizing factor in early Xenopus development. Development 115: 573-585.
9. de Jong, F., A.J. Grootenhuis, I.A. Klaij, and W. Van Beurden. 1990. Inhibin and related proteins: Localization, regulation, and effects. Adv. Exp. Med. Biol. 274: 271-293.
10. Doetschman, T.C., H. Eistetter, M. Ratz, W. Schmidt, and R. Kemler. 1985. The in vitro development of blastocyst-derived embryonic stem cell lines: Formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol 87: 27-45.
11. Dohrmann, C.E., A. Hemmati-Brivanlou, G.H. Thomsen, A. Fields, T.M. Woolf, and D.A. Melton. 1993. Expression of activin mRNA during early development in Xenopus laevis. Dev. Biol. 157: 474-483.
12. Esch, F.S., S. Shimasaki, K. Cooksey, M. Mercado, A.J. Mason, S.Y. Ying, N. Ueno, and N. Ling. 1987. Complementary deoxyribonucleic acid (cDNA) cloning and DNA sequence analysis of rat ovarian inhibins. Mol. Endocrinol. 1: 388-396.
13. Feng, Z.M., C.W. Bardin, and C.L. Chen. 1989a. Characterization and regulation of testicular inhibin beta-subunit mRNA. Mol. Endocrinol. 3: 939-948.
14. Feng, Z.M., Y.P. Li, and C.L. Chen. 1989b. Analysis of the 5′-flanking regions of rat inhibin alpha- and beta-B-subunit genes suggests two different regulatory mechanisms, Mol. Endocrinol. 3: 1914-1925.
15. Findlay, J.K. 1993. An update on the roles of inhibin, activin, and follistatin as local regulators of folliculogenesis. Biol. Reprod. 48: 15-23.
16. Gray, A.M. and A.J. Mason. 1990. Requirement for activin A and transforming growth factor-beta 1 pro-regions in homodimer assembly. Science 247: 1328-1330.
17. Green, J.B., H.V. New, and J.C. Smith. 1992. Responses of embryonic Xenopus cells to activin and FGF are separated by multiple dose thresholds and correspond to distinct axes of the mesoderm. Cell 71: 731-739.
18. Hashimoto, M., S. Kondo, T. Sakurai, Y. Eton, H. Shibai, and M. Muramatsu. 1990. Activin/EDF as an inhibitor of neural differentiation. Biochem. Biophys. Res. Commun. 173: 193-200.
19. Hemmati-Brivanlou, A. and D.A. Melton. 1992. A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature 359: 609-614.
20. Herrmann, B.G., S. Labeit, A. Poustka, T.R. King, and H. Lehrach. 1990. Cloning of the T gene required in mesoderm formation in the mouse. Nature 343: 617-622.
21. Jones, C.M., K.M. Lyons, P.M. Lapan, C.V. Wright, and B.L. Hogan. 1992. DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction. Development 115: 639-647.
22. Juriloff, D.M. and M.J. Harris. 1993. Retinoic acid, cortisone, or thyroxine suppresses the mutant phenotype of the eyelid development mutation, lgMl, in mice. J. Exp. Zool. 265: 144-152.
23. Kaipia, A., T.L. Penttila, S. Shimasaki, N. Ling, M. Parvinen, and J. Toppari. 1992. Expression of inhibin beta A and beta B, follistatin and activin-A receptor messenger ribonucleic acids in the rat seminiferous epithelium. Endocrinology 131: 2703-2710.
24. Kaipia, A., M. Parvinen, and J. Toppari. 1993, Localization of activin receptor (ActR-IIB2) mRNA in the rat seminiferous epithelium. Endocrinology 132: 477-479.
25. Kimelman, D. and M. Kirschner. 1987. Synergistic induction of mesoderm by FGF and TGF-beta and the identification of an mRNA coding for FGF in the early Xenopus embryo. Cell 51: 869-877.
26. Kimelman, D., J.L. Christian, and R.T. Moon. 1992. Synergistic principles of development: Overlapping patterning systems in Xenopus mesoderm induction. Development 116: 1-9.
27. Koster, M., S. Plessow, J.H. Clement, A. Lorenz, H. Tiedemann, and W. Knochel. 1991. Bone morphogenetic protein 4 (BMP-4), a member of the TGF-beta family, in early embryos of Xenopus laevis: Analysis of mesoderm inducing activity. Mech. Dev. 33: 191-199.
28. Laird, P.W., A. Zijderveld, K. Linders, M.A. Rudnicki, R. Jaenisch, and A. Berns. 1991. Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19: 4293.
29. Lee, K.F., E. Li, L.J. Huber, S.C. Landis, A.H. Sharpe, M.V. Chao, and R. Jaenisch. 1992. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69: 737-749.
30. Lefebvre, D.L., A. Giaid, H. Bennett, R. Lariviere, and H.H. Zingg. 1992. Oxytocin gene expression in rat uterus. Science 256: 1553-1555.
31. Li, E., T.H. Bestor, and R. Jaenisch. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915-926.
32. Ling, N., S.Y. Ying, N. Ueno, S. Shimasaki, F. Esch, M. Hotta, and R. Guillemin. 1986. Pituitary FSH is released by a heterodimer of the beta-subunits from the two forms of inhibin. Nature 321: 779-782.
33. Luetteke, N.C., T.H. Qiu, R.L. Peiffer, P. Oliver, O. Smithies, and D.C. Lee. 1993. TGF alpha deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell 73: 263-278.
34. Lyon, M. and A.G. Searle, eds. 1989. Genetic variants and stiains of the laboratory mouse. Oxford University Press, Oxford, England.
35. MacMurray, A. and H.S. Shin. 1988. The antimorphic nature of the Tc allele at the mouse T locus. Genetics 120: 545-550.
36. Mann, G.B., K.J. Fowler, A. Gabriel, E.G. Nice, R.L. Williams, and A.R. Dunn. 1993. Mice with a null mutation of the TGF alpha gene have abnormal skin architecture, wavy hair, and curly whiskers and often develop corneal inflammation. Cell 73: 249-261.
37. Manova, K., B.V. Paynton, and R.F. Bachvarova. 1992. Expression of activins and TGF beta 1 and beta 2 RNAs in early postimplantation mouse embryos and uterine decidua. Mech. Dev. 36: 141-152.
38. Mason, A.J., L.M. Berkemeier, C.H. Schmelzer, and R.H. Schwall. 1989. Activin B: Precursor sequences, genomic structure and in vitro activities. Mol Endocrinol. 3: 1352-1358.
39. Mather, J.P., T.K. Woodruff, and L.A. Krummen. 1992. Paracrine regulation of reproductive function by inhibin and activin. Proc. Soc. Exp. Biol. Med. 201: 1-15.
40. Matzuk, M.M., M.J. Finegold, J.G. Su, A.J. Hsueh, and A. Bradley. 1992. Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360: 313-319.
41. McBurney, M.W., L.C. Sutherland, C.N. Adra, B. Leclair, M.A. Rudnicki, and K. Jardine. 1991. The mouse Pgk-1 gene promoter contains an upstream activator sequence. Nucleic Acids Res. 19: 5755-5761.
42. Meunier, H., C. Rivier, R.M. Evans, and W. Vale. 1988. Gonadal and extragonadal expression of inhibin alpha, beta A, and beta B subunits in various tissues predicts diverse functions. Proc. Natl. Acad. Sci. 85: 247-251.
43. Mitrani, E., T. Ziv, G. Thomsen, Y. Shimoni, D.A. Melton, and A. Bril. 1990. Activin can induce the formation of axial structures and is expressed in the hypoblast of the chick. Cell 63: 495-501.
44. Murata, M., Y. Eto, H. Shibai, M. Sakai, and M. Muramatsu. 1988. Erythroid differentiation factor is encoded by the same mRNA as that of the inhibin βA chain. Proc. Natl. Acad. Sci. 85: 2434-2438.
45. Petraglia, F., L. Calza, G.G. Garuti, M. Abrate, L. Giardino, A.R. Genazzani, W. Vale, and H. Meunier. 1990. Presence and synthesis of inhibin subunits in human decidua. J. Clin. Endocrinol. Metab. 71: 487-492.
46. Robertson, E.J., ed. 1987. Embryo-derived stem cell lines. In Teratocarcinomas and embryonic stem cells: A practical approach. IRL Press, Oxford, England.
47. Rugh, R. 1990. The mouse: Its reproduction and development. Oxford University Press, Oxford, England.
48. Sawchenko, P.E., P.M. Plotsky, S.W. Pfeiffer, E.J. Cunningham, J. Vaughan, J. Rivier, and W. Vale. 1988. Inhibin beta in central neural pathways involved in the control of oxytocin secretion. Nature 334: 615-617.
49. Schubert, D., H. Kimura, C.M. La, J. Vaughan, D. Karr, and W.H. Fischer. 1990. Activin is a nerve cell survival molecule. Nature 344: 868-870.
50. Schwartzberg, P.L., A.M. Stall, J.D. Hardin; K.S. Bowdish, T. Humaran, S. Boast, M.L. Harbison, E.J. Robertson, and S.P. Goff. 1991. Mice homozygous for the ablml mutation show poor viability and depletion of selected B and T cell populations. Cell 65: 1165-1175.
51. Sive, H.L. 1993. The frog prince-ss: A molecular formula for dorsoventral patterning in Xenopus. Genes & Dev. 7: 1-12.
52. Slack, I.M., B.C. Darlington, J.K. Heath, and S.F. Godsave. 1987. Mesoderm induction in early Xenopus embryos by heparinbinding growth factors. Nature 326: 197-200.
53. Smith, f.C. and J.E. Howard. 1992. Mesoderm-inducing factors and the control of gastrulation. Development (Suppl.) 127-136.
54. Smith, J.C., B.M. Price, K. Van Nimmen, and D. Huylebroeck. 1990. Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature 345: 729-731.
55. Smith, J.C., B.M. Price, J.B. Green, D. Weigel, and B.C. Herrmann. 1991. Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67: 79-87.
56. Smith, W.C. and R.M. Harland. 1991. Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67: 753-765.
57. _. 1992. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70: 829-840.
58. Sokol, S., J.L. Christian, R.T. Moon, and D.A. Melton. 1991. Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 67: 741-752.
59. Stewart, C.L., P. Kaspar, L.J. Brunet, H. Bhatt, I. Gadi, F. Kontgen, and S.J. Abbondanzo. 1992. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359: 76-79.
60. Thomas, K.R. and M.R. Capecchi. 1987. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51: 503-512.
61. Thomsen, G.H. and D.A. Melton. 1993. Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell 74: 433-441.
62. Thomsen, G., T. Woolf, M. Whitman, S. Sokol, I- Vaughan, W. Vale, and D.A. Melton. 1990. Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 63: 485-493.
63. Tybulewicz, V.L., C.E. Crawford, P.K. Jackson, R.T. Bronson, and R.C. Mulligan. 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl protooncogene. Cell 65: 1153-1163.
64. Vale, W., J. Rivier, J. Vaughan, R. McClintock, A. Corrigan, W. Woo, D. Karr, and J. Spiess. 1986. Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature 321: 776-779.
65. Vale, W.; A. Hsueh, C. Rivier, and J. Yu. 1990. The inhibin/ activin family of hormones and growth factors. In Peptide growth factors and their receptors: Handbook of experimental pharmacology (ed. M.A. Sporn and A.B. Roberts), pp. 211-248. Springer-Verlag, Berlin, Germany.
66. van den Eijnden-Van Raaij, A., E. van Zoelent, K. van Nimmen, C.H. Koster, G.T. Snoek, A.J. Durston, and D. Huylebroeck. 1990. Activin-like factor from a Xenopus laevis cell line responsible for mesoderm induction. Nature 345: 732-734.
67. van den Eijnden-van Raaij, A., T. van Achterberg, C. van der Kruijssen, A.H. Piersma, D. Huylebroeck, S. de Laat, and C.L. Mummery. 1991. Differentiation of aggregated murine P19 embryonal carcinoma cells is induced by a novel visceral endoderm-specific FGF-like factor and inhibited by activin A. Mech. Dev. 33: 157-165.
68. van den Eijnden-van Raaij, A.J., A. Feijen, K.A. Lawson, and C.L. Mummery. 1992. Differential expression of inhibin subunits and follistatin, but not of activin receptor type II, during early murine embryonic development. Dev. Biol. 154: 356-365.
69. Vaughan, J., J. Rivier, A.Z. Corrigan, R. McClintock, C.A. Campen, D. Jolley, J.K. Voglmayr, C.W. Bardin, C. Rivier, and W. Vale. 1989. Detection and purification of inhibin using antisera generated against synthetic peptide fragments. In Hormone action: Part K neuroendocrine peptides (ed. P.M. Conn), pp. 588-617. Academic Press, New York.
70. Zhou, X., H. Sasaki, L. Lowe, B.L. Hogan, and M.R. Kuehn. 1993. Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature 361: 543-547.
71. Zijlstra, M., E. Li, F. Sajjadi, S. Subramani, and R. Jaenisch. 1989. Germ-line transmission of a disrupted β2-microglobulin gene produced by homologous recombination in embryonic stem cells. Nature 342: 435-438.