Midkine counteracts the activin signal in mesoderm induction and promotes neural formation

Journal of Biochemistry

Volumn 123, Issue 2, 1998, Pages 339-346

  Yokota, Chika ^a   Takahashi, Shuji ^a   Eisaki, Akira ^a   Asashima, Makoto ^a   Akhter, Shamima ^b   Muramatsu, Takashi ^b   Kadomatsu, Kenji ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Activin; Mesoderm induction; Midkine; Neural formation; Pleiotrophin

Indexed keywords

ACTIVIN; FIBROBLAST GROWTH FACTOR; MIDKINE;

ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; EMBRYO; FIBRINOLYSIS; INVAGINATION; MESODERM; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; XENOPUS;

EID: 0031910637     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.jbchem.a021942     Document Type: Article

References (76)

1. Dawid, I.B., Taira, M., Good, P.J., and Rebagliati, M.R. (1992) The roles of growth factors in embryonic induction. Mol. Reprod. Dev. 32, 136-144
2. Nieuwkoop, P.D. (1969) The formation of mesoderm in urodelean amphibians. I. Induction by the endoderm. Wilhelm Roux' Arch. Entwicklungsmech Mech. Org. 162, 341-373
3. Asashima, M., Nakano, H., Shimada, K., Kinoshita, K., Ishii, K., Shibai, H., and Ueno, N. (1990) Mesoderm induction in early amphibian embryos by activin A (erythroid differentiation factor). Roux's Arch. Dev. Biol. 198, 330-335
4. Smith, J.C., Price, B.M.J., Van Nimmen, K., and Huylebroeck, D. (1990) Identification of a potent Xenopus mesoderm-inducing factor as a homolog of activin A. Nature 345, 729-731
5. Sokol, S., Wong, G.G., and Melton, D.A. (1990) A mouse macrophage factor induces head structures and organizes a body axis in Xenopus. Science 249, 561-564
6. Thomsen, G., Woolf, T., Whitman, M., Sokol, S., Vaughan, J., Vale, W., and Melton, D.A. (1990) Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 63, 485-493
7. Koster, M., Plessow, S., Clement, J.H., Lorenz, A., Tiedemann, H., and Knochel, W. (1991) Bone Morphogenetic Protein 4 (BMP4), a member of the TGF-β family, in early embryos of Xenopus laevis: analysis of mesoderm inducing activity. Mech. Dev. 33, 191-200
8. Dale, L., Howes, G., Price, B.M.J., and Smith, J.C. (1992) Bone morphogenetic protein 4: a ventralizing factor in Xenopus development. Development 115, 573-585
9. Jones, C.M., Lyons, K.M., Lapan, P.M., Wright, C.V.E., and Hogan, B.J.M. (1992) DVR-4 (Bone Morphogenetic Protein-4) as a postero-ventralizing factor in Xenopus mesoderm induction. Development 115, 639-647
10. Dale, L., Mattews, G., and Colman, A. (1993) Secretion and mesoderm inducing activity of the TGFβ related domain of Xenopus Vg1. EMBO J. 12, 4471-4480
11. Thomsen, G. and Melton, D.A. (1993) Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell 74, 433-441
12. Kessler, D.S. and Melton, D.A. (1995) Induction of dorsal mesoderm by soluble, mature Vg1 protein. Development 121, 2155-2164
13. Kimelman, D., Abraham, J.A., Haaparanta, T., Palishi, T.M., and Kirschner, M.W. (1988) The presence of fibroblast growth factor in the frog egg: its role as a natural mesoderm inducer. Science 242, 1053-1056
14. Slack, J.M.W., Isaacs, H.V., and Darlington, B.G. (1988) Inductive effects of fibroblast growth factor and lithium ion on Xenopus blastula ectoderm. Development 103, 581-590
15. Isaacs, H., Tannahill, D., and Slack, J. (1992) Expression of a novel FGF in the Xenopus embryo. A new candidate inducing factor for mesoderm formation and anterioposterior specification. Development 114, 711-720
16. Kessler, D.S. and Melton, D.A. (1994) Vertebrate embryonic induction: mesodermal and neural patterning. Science 166, 596-604
17. Sasai, Y., Lu, B., Steinbeisser, H., Geissert, D., Gont, L.K., and De Robertis, E.M. (1994) Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79, 779-790
18. Asashima, M., Nakano, H., Uchiyama, H., Sugino, H., Nakamura, T., Eto, Y., Ejima, D., Nishimatsu, S., Ueno, N., and Kinoshita, K. (1991) Presence of activin (erythroid differentiation factor) in unfertilized eggs and blastulae of Xenopus laevis. Proc. Natl. Acad. Sci. USA 88, 6511-6514
19. Cornell, R.A. and Kimelman, D. (1994) Activin-mediated mesoderm induction requires FGF. Development 120, 453-462
20. LaBonne, C. and Whitman, M. (1994) Mesoderm induction by activin requires FGF-mediated intracellular signals. Development 120, 463-472
21. Cornell, R.A., Musci, T.J., and Kimelman, D. (1995) FGF is a prospective competence factor for early activin-type signals in Xenopus mesoderm induction. Development 121, 2429-2437
22. LaBonne, C., Burke, B., and Whitman, M. (1995) Role of MAP kinase in mesoderm induction and axial patterning during Xenopus development. Development 121, 1475-1486
23. Raftery, L.A., Twobly, V., Wharton, K., and Gelbart, W.M. (1995) Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics 139, 241-254
24. Sekelsky, J.J., Newfeld, S.J., Raftery, L.A., Chartoft, E.H., and Gelbart, W.M. (1995) Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139, 1347-1358
25. Graff, J.M., Bansal, A., and Melton, D.A. (1996) Xenopus Mad proteins transduce distinct subsets of signals for the TGF-β superfamily. Cell 85, 479-487
26. Kadomatsu, K., Tomomura, M., and Muramatsu, T. (1988) cDNA cloning and sequencing of a new gene intensely expressed in early differentiation stages of embryonal carcinoma cells and in mid-gestation period of mouse embryogenesis. Biochem. Biophys. Res. Commun. 151, 1312-1318
27. Kadomatsu, K., Huang, R.-P., Suganuma, T., Murata, F., and Muramatsu, T. (1990) A retinoic acid responsive gene MK found in the teratocarcinoma system is expressed in spatially and temporally controlled manner during mouse embryogenesis. J. Cell Biol. 110, 607-616
28. Tomomura, M., Kadomatsu, K., Matsubara, S., and Muramatsu, T. (1990) A retinoic acid-responsive gene, MK, found in the teratocarcinoma system: Heterogeneity of the transcript and the nature of the translation product. J. Biol. Chem. 265, 10765-10770
29. Tomomura, M., Kadomatsu, K., Nakamoto, M., Muramatsu, H., Kondoh, H., Imagawa, K., and Muramatsu, T. (1990) A retinoic acid responsive gene, MK, produces a secreted protein with heparin binding activity. Biochem. Biophys. Res. Commun. 171, 603-609
30. Muramatsu, H., Shirahama, H., Yonezawa, S., Maruta, H., and Muramatsu, T. (1993) Midkine, a retinoic acid-inducible growth/ differentiation factor: immunochemical evidence for the function and distribution. Dev. Biol. 159, 392-402
31. Muramatsu, H., Inui, T., Kimura, T., Sakakibara, S., Song, X.-J., Maruta, H., and Muramatsu, T. (1994) Localization of heparin-binding, neurite outgrowth and antigenic regions in midkine molecule. Biochem. Biophys. Res. Commun. 203, 1131-1139
32. Li, Y.-S., Milner, P.G., Chauhan, A.K., Watson, M.A., Hoffman, R.M., Kodner, C.M., Milbrandt, J., and Deuel, T.F. (1990) Cloning and expression of a developmentally regulated protein that induces mitogenic and neurite outgrowth activity. Science 250, 1690-1694
33. Merenmies, J. and Rauvala, H. (1990) Molecular cloning of the 18-kDa growth-associated protein of developing brain. J. Biol. Chem. 265, 16721-16724
34. Michikawa, M., Kikuchi, S., Muramatsu, H., Muramatsu, T., and Kim, S.U. (1993) Retinoic acid responsive gene product, midkine, has neurotrophic functions for mouse spinal cord and dorsal root ganglion neurons in culture. J. Neurosci. Res. 35, 530-539
35. Muramatsu, T. (1993) Midkine, the product of a retinoic acid responsive gene, and pleiotrophin constitute a new protein family regulating growth and differentiation. Int. J. Dev. Biol. 37, 183-188
36. Tsutsui, J., Kadomatsu, K., Matsubara, S., Nakagawara, A., Hamanoue, M., Takao, S., Shimazu, H., Ohi, Y., and Muramatsu, T. (1993) A new family of heparin-binding growth/differentiation factors: increased midkine expression in Wilms' tumor and other human carcinomas. Cancer Res. 53, 1281-1285
37. Kojima, S., Muramatsu, H., Amanuma, H., and Muramatsu, T. (1995) Midkine enhances fibrolytic activity of bovine endothelial cells. J. Biol. Chem. 270, 9590-9596
38. Unoki, K., Ohba, N., Arimura, H., Muramatsu, H., and Muramatsu, T. (1995) Rescue of photoreceptors from the damaging effects of constant light by midkine, a retinoic acid-responsive gene product. Invest. Ophthalmol. Vis. Sci. 35, 907-915
39. Kadomatsu, K., Hagihara, M., Akhter, S., Fan, Q.-W., Muramatsu, H., and Muramatsu, T. (1997) Midkine induces the transformation of NIH3T3 cells. Br. J. Cancer 75, 354-359
40. Takada, T., Toriyama, K., Muramatsu, H., Song, X.-J., Torii, S., and Muramatsu, T. (1997) Midkine, a retinoic acid-inducible heparin-binding cytokine in inflammatory responses: Chemotactic activity to neutrophils and association with inflammatory synovitis. J. Biochem. 122, 453-458
41. Mitsiadis, T.A., Salmivirta, M., Muramatsu, T., Muramatsu, H., Rauvala, H., Lehtonen, E., Jalkanen, M., and Thesleff, I. (1995) Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. Development 121, 37-51
42. Sekiguchi, K., Yokota, C., Asashima, M., Kaname, T., Fan, Q.-W., Muramatsu, T., and Kadomatsu, K. (1995) Restricted expression of Xenopus midkine gene during early development. J. Biochem. 118, 94-100
43. Kaneda, N., Talukder, A.H., Nishiyama, H., Koizumi, S., and Muramatsu, T. (1996) Midkine, a heparin-binding growth/differentiation factor, exhibits nerve cell adhesion and guidance activity for neunte outgrowth in vitro. J. Biochem. 119, 1150-1156
44. Matsumoto, K., Wanaka, A., Takatsuji, K., Muramatsu, H., Muramatsu, T., and Tohyama, M. (1994) A novel family of heparin-binding growth factors, pleiotrophin and midkine, is expressed in the developing rat cerebral cortex. Dev. Brain Res. 79, 229-241
45. Kaneda, N., Talukder, A.H., Ishihara, M., Hara, S., Yoshida, K., and Muramatsu, T. (1996) Structural characteristics of heparin-like domain required for interaction of midkine with embryonic neurons. Biochem. Biophys. Res. Commun. 220, 108-112
46. Kikuchi, S., Muramatsu, H., Muramatsu, T., and Kim, S.U. (1993) Midkine, a novel neurotrophic factor, promotes survival of mesencephalic neurons in culture. Neurosci. Lett. 160, 9-12
47. Kojima, T., Katsumi, A., Yamazaki, T., Muramatsu, T., Nagasaka, T., Ohsumi, K., and Saito, H. (1996) Human ryudocan from endothelium-like cells binds basic fibroblast growth factor, midkine, and tissue factor pathway inhibitor. J. Biol. Chem. 271, 5914-5920
48. Maeda, N., Nishiwaki, T., Shintani, T., Hamanaka, H., and Noda, M. (1996) 6B4 proteoglycan/phosphacan, an extracellular variant of receptor-like protein-tyrosine phosphatase ζ/RPTPβ, binds pleiotrophin/heparin-binding growth-associated molecule (HB-GAM). J. Biol. Chem. 271, 21446-21452
49. Nakanishi, T., Kadomatsu, K., Okamoto, T., Ichikawa-Tanaka, K., Kojima, T., Saito, H., Tomoda, Y., and Muramatsu, T. (1997) Expression of syndecan-1 and -3 during embryogenesis of the central nervous system in relation to binding with midkine. J. Biochem. 121, 197-205
50. Nieuwkoop, P.D. and Faber, J. (1956) Normal Table of Xenopus laevis (Daudin), North-Holland Publishing, Amsterdam
51. Krieg, P.A. and Melton, D.A. (1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 12, 7057-7070
52. Eto, Y., Tsuji, T., Takezawa, M., Takano, S., Yokogawa, Y., and Shiabai, H. (1987) Purification and characterization of erythroid differentiation factor (EDF) isolated from human leukemia cell line THP-1. Biochem. Biophys. Res. Commun. 142, 1095-1103
53. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159
54. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
55. Smith, J.C., Price, B.M.J., Green, J.B.A., Weigel, D., and Herrmann, B.G. (1991) Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79-87
56. Bouwmeester, T., Kim, S., Sasai, Y., Lu, B., and De Robertis, E.M. (1996) Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemanns organizer. Nature 380, 595-599
57. Stutz, F. and Spohr, G. (1986) Isolation and characterization of sarcomic actin genes expressed in Xenopus laevis embryogenesis. J. Mol. Biol. 187, 349-361
58. Kintner, C.R. and Melton, D.A. (1987) Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. Development 99, 311-325
59. Zaraisky, A.G., Lukyanov, S.A., Vasiliev, O.L., Smirnov, Y.V., Belyavsky, A.V., and Kazanskaya, O.V. (1992) A novel homeobox gene expressed in the anterior neural plate of the Xenopus embryo. Dev. Biol. 152, 373-382
60. Pannese, M., Polo, C., Andreazzoli, M., Vignali, R., Kablar, B., Barasacchi, G., Dekker, E.-J., and Boncinelli, E. (1995) The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 121, 707-720
61. Sive, H.L., Hattori, K., and Weintraub, H. (1989) Progressive determination during formation of the anteroposterior axis in Xenopus laevis. Cell 58, 171-180
62. Itoh, K., Tang, T.L., Nell, B.G., and Sokol, S.Y. (1995) Specific modulation of ectodermal cell fates in Xenopus embryos by glycogen synthase kinase. Development 121, 3979-3988
63. Wright, C.V.E., Morita, E.A., Wilkin, D.J., and De Robertis, E.M. (1990) The Xenopus XlHbox 6 homeo protein, a marker of posterior neural induction, is expressed in proliferating neurons. Development 109, 225-234
64. Klar, A., Baldassare, M., and Jessell, T.M. (1992) F-spondin: A gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 69, 95-110
65. Krieg, P.A., Varnam, S., Wormington, M., and Melton, D.A. (1989) The mRNA encoding elongation factor 1α (EF-1α) is a major transcript at the mid-blastula transition in Xenopus. Dev. Biol. 133, 93-100
66. Wilson, P.A. and Melton, D.A. (1994) Mesodermal patterning by an inducer gradient depends on secondary cell-cell communication. Curr. Biol. 4, 676-686
67. Hatada, S., Kinoshita, M., Noda, M., and Asashima, M. (1995) Identification of a Xenopus glutamine synthetase gene abundantly expressed in the embryonic nervous system but not in adult brain. FEBS Lett. 371, 287-292
68. Sasai, Y., Lu, B., Steinbeisser, H., and De Robertis, E.M. (1995) Regulation of neural induction by the chd and BMP-4 antagonistic patterning signals in Xenopus. Nature 376, 333-336
69. Rosa, F.M. (1989) Mix.1, a homeobox mRNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos. Cell 57, 965-974
70. Slack, J.M.W. (1991) From Egg to Embryo, Cambridge Univ. Press, Cambridge
71. Gurdon, J.B. (1987) Embryonic induction - Molecular prospects. Development 99, 285-306
72. Mitsiadis, T.A., Muramatsu, T., Muramatsu, H., and Thesleff, I. (1995) Midkine (MK), a heparin-binding growth/differentiation factor, is regulated by retinoic acid and epithelial-mesenchymal interactions in the developing mouse tooth, and affects cell proliferation and morphogenesis. J. Cell Biol. 129, 267-281
73. Stern, C.D., Yu, R.T., Kakizuka, A., Kintner, C.R., Mathews, L.S., Vale, W.W., Evans, R.M., and Umesono, K. (1995) Activin and its receptors during gastrulation and the later phases of mesoderm development in the chick embryo. Dev. Biol. 172, 192-205
74. Dohrmann, C.E., Hemmati-Brivanlou, A., Thomsen, G.H., Fields, A., Woolf, T.M., and Melton, D.A. (1993) Expression of activin mRNA during early development in Xenopus laevis. Dev. Biol. 157, 474-483
75. Hemmati-Brivanlou, A., Wright, D.A., and Melton, D.A. (1992) Embryonic expression and functional analysis of a Xenopus activin receptor. Dev. Dyn. 194, 1-11
76. Sive, H. and Bradley, L. (1996) A sticky problem; the Xenopus cement gland as a paradigm for anteroposterior patterning. Dev. Dyn. 205, 265-280