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Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis
Abstract
Midkine (MK) and heparin binding-growth associated molecule (HB-GAM or pleiotrophin), constitute a new family of heparin-binding proteins implicated in the regulation of growth and differentiation (T. Muramatsu (1993)Int. J. Dev. Biol. 37, 183-188). We used affinity-purified antibodies against MK and HB-GAM to analyze their distribution during mouse embryonic development. From 9 to 14.5 day post-coitum (dpc), both proteins were detected in central and peripheral nervous systems, facial processes, limb buds, sense organs, respiratory, digestive, urogenital, and skeletal systems. MK and HB-GAM were often localized on the surface of differentiating cells and in basement membranes of organs undergoing epithelial-mesenchymal interactions. The levels of MK protein decreased considerably in the 16.5 dpc embryo, whereas HB-GAM staining persisted in many tissues. Our in situ hybridization results revealed a widespread expression of MK transcripts that was not always consistent with the distribution of MK protein in developing tissues. In many epithelio-mesenchymal organs MK and HB-GAM were codistributed with syndecan-1, a cell surface proteoglycan. In limb buds and facial processes, MK, HB-GAM, and syndecan-1 were localized to the apical epithelium and the adjacent proliferating mesenchyme. Both MK and HB-GAM bound syndecan-1 in solid-phase assays in a heparan sulfate-dependent manner. The biological effects of MK and HB-GAM on limb and facial mesenchyme were studied in vitro by application of beads preloaded with the proteins. Neither MK nor HB-GAM stimulated mesenchymal cell proliferation or induced syndecan-1 expression. Taken together these results indicate that MK and HB-GAM may play regulatory roles in differentiation and morphogenesis of the vertebrate embryo, particularly in epithelio-mesenchymal organs, and suggest molecular interactions with syndecan-1.
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Citations
Cited by
Proteoglycans in the Developing Brain: New Conceptual Insights for Old Proteins
Bandtlow, C. E., & Zimmermann, D. R. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.4.1267 · Cited by 632
Muramatsu, T. (2002) · Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a003231 · Cited by 405
Self-citationShi, Y., Ping, Y.-F., Zhou, W., He, Z.-C., Chen, C., Bian, B.-S.-J., Zhang, L., Chen, L., Lan, X., Zhang, X.-C., et al. (2017) · Nature Communications · doi:10.1038/ncomms15080 · Cited by 344
Midkine (MDK) growth factor: a key player in cancer progression and a promising therapeutic target
Filippou, P. S., Karagiannis, G. S., & Constantinidou, A. (2020) · Oncogene · doi:10.1038/s41388-019-1124-8 · Cited by 331
Growth factors in skeletal muscle regeneration
Husmann, I., Soulet, L., Gautron, J., Martelly, I., & Barritault, D. (1996) · Cytokine & Growth Factor Reviews · doi:10.1016/s1359-6101(96)00029-9 · Cited by 274
Metadata
- Authors
- Mitsiadis, T. A., Salmivirta, M., Muramatsu, T., Muramatsu, H., Rauvala, H., Lehtonen, E., Jalkanen, M., & Thesleff, I.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 1995-01-01
- Volume
- 121
- Issue
- 1
- Pages
- 37-51
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2121308413
- Cited by
- 292
- References
- 0
- FWCI
- 4.97
- Type
- journal article
- Language
- en
- Open access
- closed
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- CoChat. (2026). Citation check: Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. https://app.cochat.ai/papers/10.1242/dev.121.1.37
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- Mitsiadis, T. A., Salmivirta, M., Muramatsu, T., Muramatsu, H., Rauvala, H., Lehtonen, E., Jalkanen, M., & 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. https://doi.org/10.1242/dev.121.1.37
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