Abstract
Tenascin is a large extracellular matrix (ECM) glycoprotein found in restricted tissue locations in the adult organism. It is copiously synthesized in regenerative organs or regenerating tissues and by certain tumors. We have analyzed the expression of tenascin in human long term bone marrow cultures as well as in cryostat sections of native bone marrow and found it strongly expressed by the stromal cells of the microenvironment. Two different protein subunits of 280 and 220 kD were detected by immunoblotting. These two forms are derived most likely from two different mRNA splice variants of 6 and 8 kb detected by Northern blotting. The in vivo analysis of cryostat sections showed a codistribution with other ECM molecules such as fibronectin and collagen type III in the microenvironment surrounding the maturing hematopoietic cells. Using two independent cell adhesion assays tenascin could be shown to function as a cytoadhesive molecule for hematopoietic cells. These data suggest a direct involvement of tenascin in the retention of hematopoietic progenitor cells in the stroma.
Full Text
The Full Text of this article is available as a PDF (2.9 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aufderheide E., Chiquet-Ehrismann R., Ekblom P. Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme. J Cell Biol. 1987 Jul;105(1):599–608. doi: 10.1083/jcb.105.1.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aufderheide E., Ekblom P. Tenascin during gut development: appearance in the mesenchyme, shift in molecular forms, and dependence on epithelial-mesenchymal interactions. J Cell Biol. 1988 Dec;107(6 Pt 1):2341–2349. doi: 10.1083/jcb.107.6.2341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bentley S. A. Close range cell:cell interaction required for stem cell maintenance in continuous bone marrow culture. Exp Hematol. 1981 Mar;9(3):308–312. [PubMed] [Google Scholar]
- Bourdon M. A., Ruoslahti E. Tenascin mediates cell attachment through an RGD-dependent receptor. J Cell Biol. 1989 Mar;108(3):1149–1155. doi: 10.1083/jcb.108.3.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Campbell A. D., Long M. W., Wicha M. S. Developmental regulation of granulocytic cell binding to hemonectin. Blood. 1990 Nov 1;76(9):1758–1764. [PubMed] [Google Scholar]
- Campbell A. D., Long M. W., Wicha M. S. Haemonectin, a bone marrow adhesion protein specific for cells of granulocyte lineage. Nature. 1987 Oct 22;329(6141):744–746. doi: 10.1038/329744a0. [DOI] [PubMed] [Google Scholar]
- Campbell A. D., Wicha M. S. Extracellular matrix and the hematopoietic microenvironment. J Lab Clin Med. 1988 Aug;112(2):140–146. [PubMed] [Google Scholar]
- Carnemolla B., Borsi L., Bannikov G., Troyanovsky S., Zardi L. Comparison of human tenascin expression in normal, simian-virus-40-transformed and tumor-derived cell lines. Eur J Biochem. 1992 Apr 15;205(2):561–567. doi: 10.1111/j.1432-1033.1992.tb16813.x. [DOI] [PubMed] [Google Scholar]
- Chiquet-Ehrismann R. Anti-adhesive molecules of the extracellular matrix. Curr Opin Cell Biol. 1991 Oct;3(5):800–804. doi: 10.1016/0955-0674(91)90053-2. [DOI] [PubMed] [Google Scholar]
- Chiquet-Ehrismann R., Kalla P., Pearson C. A., Beck K., Chiquet M. Tenascin interferes with fibronectin action. Cell. 1988 May 6;53(3):383–390. doi: 10.1016/0092-8674(88)90158-4. [DOI] [PubMed] [Google Scholar]
- Chiquet-Ehrismann R., Mackie E. J., Pearson C. A., Sakakura T. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell. 1986 Oct 10;47(1):131–139. doi: 10.1016/0092-8674(86)90374-0. [DOI] [PubMed] [Google Scholar]
- Chiquet-Ehrismann R. What distinguishes tenascin from fibronectin? FASEB J. 1990 Jun;4(9):2598–2604. doi: 10.1096/fasebj.4.9.1693347. [DOI] [PubMed] [Google Scholar]
- Dexter T. M., Coutinho L. H., Spooncer E., Heyworth C. M., Daniel C. P., Schiro R., Chang J., Allen T. D. Stromal cells in haemopoiesis. Ciba Found Symp. 1990;148:76–95. doi: 10.1002/9780470513880.ch6. [DOI] [PubMed] [Google Scholar]
- Dexter T. M., Spooncer E., Schofield R., Lord B. I., Simmons P. Haemopoietic stem cells and the problem of self-renewal. Blood Cells. 1984;10(2-3):315–339. [PubMed] [Google Scholar]
- Dexter T. M., Spooncer E., Simmons P., Allen T. D. Long-term marrow culture: an overview of techniques and experience. Kroc Found Ser. 1984;18:57–96. [PubMed] [Google Scholar]
- Engler-Blum G., Meier M., Frank J., Müller G. A. Reduction of background problems in nonradioactive northern and Southern blot analyses enables higher sensitivity than 32P-based hybridizations. Anal Biochem. 1993 May 1;210(2):235–244. doi: 10.1006/abio.1993.1189. [DOI] [PubMed] [Google Scholar]
- Erickson H. P., Bourdon M. A. Tenascin: an extracellular matrix protein prominent in specialized embryonic tissues and tumors. Annu Rev Cell Biol. 1989;5:71–92. doi: 10.1146/annurev.cb.05.110189.000443. [DOI] [PubMed] [Google Scholar]
- Gartner S., Kaplan H. S. Long-term culture of human bone marrow cells. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4756–4759. doi: 10.1073/pnas.77.8.4756. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Giancotti F. G., Comoglio P. M., Tarone G. Fibronectin-plasma membrane interaction in the adhesion of hemopoietic cells. J Cell Biol. 1986 Aug;103(2):429–437. doi: 10.1083/jcb.103.2.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gordon M. Y. Adhesive properties of haemopoietic stem cells. Br J Haematol. 1988 Feb;68(2):149–151. doi: 10.1111/j.1365-2141.1988.tb06181.x. [DOI] [PubMed] [Google Scholar]
- Gordon M. Y., Riley G. P., Watt S. M., Greaves M. F. Compartmentalization of a haematopoietic growth factor (GM-CSF) by glycosaminoglycans in the bone marrow microenvironment. 1987 Mar 26-Apr 1Nature. 326(6111):403–405. doi: 10.1038/326403a0. [DOI] [PubMed] [Google Scholar]
- Gulcher J. R., Nies D. E., Marton L. S., Stefansson K. An alternatively spliced region of the human hexabrachion contains a repeat of potential N-glycosylation sites. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1588–1592. doi: 10.1073/pnas.86.5.1588. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoffman S., Crossin K. L., Jones F. S., Friedlander D. R., Edelman G. M. Cytotactin and cytotactin-binding proteoglycan. An interactive pair of extracellular matrix proteins. Ann N Y Acad Sci. 1990;580:288–301. doi: 10.1111/j.1749-6632.1990.tb17938.x. [DOI] [PubMed] [Google Scholar]
- Klein G., Langegger M., Timpl R., Ekblom P. Role of laminin A chain in the development of epithelial cell polarity. Cell. 1988 Oct 21;55(2):331–341. doi: 10.1016/0092-8674(88)90056-6. [DOI] [PubMed] [Google Scholar]
- Lightner V. A., Gumkowski F., Bigner D. D., Erickson H. P. Tenascin/hexabrachion in human skin: biochemical identification and localization by light and electron microscopy. J Cell Biol. 1989 Jun;108(6):2483–2493. doi: 10.1083/jcb.108.6.2483. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Long M. W., Dixit V. M. Thrombospondin functions as a cytoadhesion molecule for human hematopoietic progenitor cells. Blood. 1990 Jun 15;75(12):2311–2318. [PubMed] [Google Scholar]
- Mackie E. J., Halfter W., Liverani D. Induction of tenascin in healing wounds. J Cell Biol. 1988 Dec;107(6 Pt 2):2757–2767. doi: 10.1083/jcb.107.6.2757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matsuoka Y., Spring J., Ballmer-Hofer K., Hofer U., Chiquet-Ehrismann R. Differential expression of tenascin splicing variants in the chick gizzard and in cell cultures. Cell Differ Dev. 1990 Dec 2;32(3):417–423. doi: 10.1016/0922-3371(90)90058-5. [DOI] [PubMed] [Google Scholar]
- Natali P. G., Nicotra M. R., Bigotti A., Botti C., Castellani P., Risso A. M., Zardi L. Comparative analysis of the expression of the extracellular matrix protein tenascin in normal human fetal, adult and tumor tissues. Int J Cancer. 1991 Apr 1;47(6):811–816. doi: 10.1002/ijc.2910470603. [DOI] [PubMed] [Google Scholar]
- Nies D. E., Hemesath T. J., Kim J. H., Gulcher J. R., Stefansson K. The complete cDNA sequence of human hexabrachion (Tenascin). A multidomain protein containing unique epidermal growth factor repeats. J Biol Chem. 1991 Feb 15;266(5):2818–2823. [PubMed] [Google Scholar]
- Patel V. P., Lodish H. F. Loss of adhesion of murine erythroleukemia cells to fibronectin during erythroid differentiation. Science. 1984 Jun 1;224(4652):996–998. doi: 10.1126/science.6585955. [DOI] [PubMed] [Google Scholar]
- Patel V. P., Lodish H. F. The fibronectin receptor on mammalian erythroid precursor cells: characterization and developmental regulation. J Cell Biol. 1986 Feb;102(2):449–456. doi: 10.1083/jcb.102.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roberts R., Gallagher J., Spooncer E., Allen T. D., Bloomfield F., Dexter T. M. Heparan sulphate bound growth factors: a mechanism for stromal cell mediated haemopoiesis. Nature. 1988 Mar 24;332(6162):376–378. doi: 10.1038/332376a0. [DOI] [PubMed] [Google Scholar]
- Rüegg C. R., Chiquet-Ehrismann R., Alkan S. S. Tenascin, an extracellular matrix protein, exerts immunomodulatory activities. Proc Natl Acad Sci U S A. 1989 Oct;86(19):7437–7441. doi: 10.1073/pnas.86.19.7437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saga Y., Yagi T., Ikawa Y., Sakakura T., Aizawa S. Mice develop normally without tenascin. Genes Dev. 1992 Oct;6(10):1821–1831. doi: 10.1101/gad.6.10.1821. [DOI] [PubMed] [Google Scholar]
- Saginati M., Siri A., Balza E., Ponassi M., Zardi L. A simple procedure for tenascin purification. Eur J Biochem. 1992 Apr 15;205(2):545–549. doi: 10.1111/j.1432-1033.1992.tb16811.x. [DOI] [PubMed] [Google Scholar]
- Salmivirta M., Elenius K., Vainio S., Hofer U., Chiquet-Ehrismann R., Thesleff I., Jalkanen M. Syndecan from embryonic tooth mesenchyme binds tenascin. J Biol Chem. 1991 Apr 25;266(12):7733–7739. [PubMed] [Google Scholar]
- Siri A., Carnemolla B., Saginati M., Leprini A., Casari G., Baralle F., Zardi L. Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucleic Acids Res. 1991 Feb 11;19(3):525–531. doi: 10.1093/nar/19.3.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spring J., Beck K., Chiquet-Ehrismann R. Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments. Cell. 1989 Oct 20;59(2):325–334. doi: 10.1016/0092-8674(89)90294-8. [DOI] [PubMed] [Google Scholar]
- Thesleff I., Mackie E., Vainio S., Chiquet-Ehrismann R. Changes in the distribution of tenascin during tooth development. Development. 1987 Oct;101(2):289–296. doi: 10.1242/dev.101.2.289. [DOI] [PubMed] [Google Scholar]
- Weller A., Beck S., Ekblom P. Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis. J Cell Biol. 1991 Jan;112(2):355–362. doi: 10.1083/jcb.112.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]