Induction of tenascin in cancer cells by interactions with embryonic mesenchyme mediated by a diffusible factor

N. Hiraiwa; H. Kida; T. Sakakura; M. Kusakabe

Summary

Human cancer cell lines A431 and MCF7, which do not produce tenascin (TN) in vitro, were found to produce TN when injected into nude mice or co-cultured with the embryonic mesenchyme. The TN expression in the developing A431 solid tumor was demonstrated by immunohistochemistry and by in situ hybridization. Human TN was detected in culture media by western blot analysis using human specific monoclonal antibody (RCB-1). During tumorigenesis, in the early stage, mouse TN was actively induced and deposited in the peri- and intertumor spaces surrounding the developing tumor. Two days later, TN derived from human epithelial cancer cells was induced and mainly deposited in the intertumor basement membrane. After this stage, tumor cells were actively producing TN. On the other hand, TN induction in non TN-producing cells, such as A431 and MCF7 cell lines, was also observed in vitro. Although cell lines such as NIH-3T3, phi 2, STO, 2H6, 3E5 and CMT315, had no effect on the TN induction, primary cultured embryonic mesenchyme effectively stimulated the TN expression in the cancer cell lines. This mesenchymal effect decreased with age and was entirely lost postnatally. Furthermore, conditioned media from these embryonic mesenchymes could reproduce the same effects on TN induction as observed in the co-culture study. In conclusion, these findings suggest that TN induction in epithelial cancer cells may depend on interactions with the surrounding environment, that these interactions may be mediated by a soluble factor(s) derived from the surrounding mesenchyme and that the TN induction observed in the tumorigenesis may reflect histogenesis during the embryonic period.

REFERENCES

1. Aufderheide E.,
2. Chiquet-Ehrismann R. and
3. Ekblom P.
(1987). Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in mesenchyme. J. Cell Biol. 105, 599–608
1. Aufderheide E. and
2. Ekblom P.
(1988). Tenascin during gut development: appearance in the mesenchyme shift in molecular forms, and dependence on epithelial-mesenchymal interactions. J. Cell Biol. 105, 2341–2349
1. Bourdon M. A.,
2. Wikstrand C. J.,
3. Furthmaryr H.,
4. Matthews T. J. and
5. Bigner D. D.
(1983). Human glioma-mesenchymal extracellular matrix antigen defined by monoclonal antibody. Cancer Res. 43, 2796–2805
1. Chiquet-Ehrismann R.
(1990). What distinguishes tenascin from fibronectin? FASEB J. 4, 2598–2604
1. Chiquet-Ehrismann R.,
2. Mackie E. J.,
3. Pearson C. A. and
4. Sakakura T.
(1986). Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47, 131–139
1. Chiquet-Ehrismann R.,
2. Kalla P.,
3. Pearson C. A.,
4. Beck K. and
5. Chiquet M.
(1988). Tenascin interferences with fibronectin action. Cell 53, 383–390
1. Daniloff J. K.,
2. Crossin K. L.,
3. Pincon-Raymond M.,
4. Murawsky M.,
5. Rieger F. and
6. Edelman G. M.
(1989). Expression of cytotactin in the normal and regenerating nueromuscular system. J. Cell Biol. 108, 625–635
1. Friedlander D. R.,
2. Hoffman S. and
3. Edelman G. M.
(1988). Functional mapping of cytotactin: proteolytic fragments active in cell-substrate adhesion. J. Cell Biol. 107, 2329–2340
1. Herlyn M.,
2. Graevev U.,
3. Speicher D.,
4. Sela B. A.,
5. Bennicelli J. L.,
6. Kath R. and
7. Guerry I. V. D.
(1991). Characterization of tenascin secreted by human melanoma cells. Cancer Res. 51, 4853–4858
1. Inaguma Y.,
2. Kusakabe M.,
3. Mackie E. J.,
4. Pearson C. A.,
5. Chiquet-Ehrismann R. and
6. Sakakura T.
(1988). Epithelial induction of stromal tenascin in the mouse mammary gland: from embryogenesis to carcinogenesis. Dev. Biol. 128, 245–255
1. Jones F. S.,
2. Hahhman S.,
3. Cunningham B. A. and
4. Edelman G. M.
(1989). A detailed structural model of cytotactin: protein, homologies, alternative RNA splicing and binding regions. Proc. Nat. Acad. Sci. USA 86, 1905–1909
1. Koch M.,
2. Wehrle-Haller B.,
3. Baumgartner S.,
4. Spring J.,
5. Brubacher D. and
6. Chiquet M.
(1991). Epithelial synthesis of tenascin at tips of growing bronchi and graded accummulation in basement membrane and mesenchyme. Exp. Cell Res. 194, 297–300
1. Kusakabe M.,
2. Yokoyama M.,
3. Sakakura T.,
4. Nomura T.,
5. Hosick H. L. and
6. Nishizuka Y.
(1988). A novel methodology for analysis of cell distribution in chimeric mouse organs using a strain specific antibody. J. Cell Biol. 107, 257–265
1. Laemmli U. K.
(1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685
1. Mackie E. J.,
2. Halfter W. and
3. Liverani D.
(1988). Induction of tenascin in healing wounds. J. Cell Biol. 107, 2757–2767
1. Mackie E. J.,
2. Chiquet-Ehrismann R.,
3. Pearson C. A.,
4. Inaguma Y.,
5. Taya K.,
6. Kawarada Y. and
7. Sakakura T.
(1989). Tenascin is a stromal marker for epithelial malignancy in the mammary gland. Proc. Nat. Acad. Sci. USA 84, 4621–4625
1. Natali P. G.,
2. Nicotra M. R.,
3. Bortolazzi A.,
4. Mottolese M.,
5. Coscia N.,
6. Bigotti A. and
7. Zardi L.
(1990). Expression and production of tenascin in benign and malignant lesions of melanocyte lineage. Int. J. Cancer. 46, 586–590
1. Nies D. E.,
2. Hemesath T. J.,
3. Kim J. H.,
4. Gulcher J. R. and
5. Stefansson K.
(1991). The complete cDNA sequence of human hexabrachion(tenascin). J. Biol. Chem. 266, 2818–2823
1. Nishi T.,
2. Weinstein J.,
3. Gillespie W. M. and
4. Paulson J. C.
(1991). Complete primary structure of porcine tenascin. Eur. J. Biochem. 202, 643–648
1. Oike Y.,
2. Hiraiwa H.,
3. Kawakatsu H.,
4. Nishikai M.,
5. Okinaka T.,
6. Suzuki T.,
7. Okada A.,
8. Yatani R. and
9. Sakakura T.
(1990). Isolation and characterization of human fibroblast tenascin. An extracellular matrix glycoprotein of interest for developmental studies. Int. J. Dev. Biol. 34, 309–317
1. Pearson C. A.,
2. Pearson D.,
3. Shibahara S.,
4. Hofsteenge J. and
5. Chiquet-Ehrismann R.
(1988). Tenascin: cDNA cloning and induction by TGF-β. EMBO J. 7, 2977–2981
1. Sakakura T.,
2. Kusano I.,
3. Kusakabe M.,
4. Inaguma Y. and
5. Nishizuka Y.
(1987). Biology of mammary fat pad in fetal mouse: capacity to support development of various fetal epithelia in vivo. Development 100, 421–430
1. Sakakura T. and
2. Kusano I.
(1991). Tenascin in tissue perturbation repair. Acta Pathologica Japonica 41, 247–258
1. Saga Y.,
2. Tsukamoto T.,
3. Jing N.,
4. Kusakabe M. and
5. Sakakura T.
(1991). Mouse tenascin: cDNA cloning structure and temporal expression of isoforms. Gene 104, 177–185
1. Siri A.,
2. Carnemolla B.,
3. Saginati M.,
4. Leprini A.,
5. Casari G.,
6. Baralle F. and
7. Zardi L.
(1991). Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucl. Acid Res. 19, 525–531
1. Tucker R. P.
(1991). The sequential expression of tenascin mRNA in epithelium and mesenchyme during feather morphogenesis. Roux's Arch. Dev. Biol. 200, 108–112
1. Tucker R. P. and
2. McKay S.E.
(1991). The expression of tenascin by neural crest and glia. Development 112, 1031–1039
1. Tsukamoto T.,
2. Kusakabe M. and
3. Saga Y.
(1991). In situ hybridization with non-radioactive digoxigenin-11-UTP-labeled cRNA probes: localization of developmentally regulated mouse tenascin mRNAs. Int. J. Dev. Biol. 35, 25–32
1. Vainio S.,
2. Jalkanen M. and
3. Thesleff I.
(1989). Syndecan and tenascin expression is inducted by epithelial-mesenchymal interactions in embryonic tooth mesenchyme. J. Cell Biol. 108, 1945–1954
1. Weller A.,
2. Beck S. and
3. Ekblom P.
(1991). Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis. J. Cell Biol. 112, 355–362
1. Whitby D. J. and
2. Ferguson M. W. J.
(1991). The extracellular matrix of lipwounds in fetal, neonatal and adult mice. Development 112, 538–587

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[1] Aufderheide E.,
Chiquet-Ehrismann R. and
Ekblom P.
(1987). Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in mesenchyme. J. Cell Biol. 105, 599–608

[2] Aufderheide E.,

[3] Chiquet-Ehrismann R. and

[4] Ekblom P.

[5] Aufderheide E. and
Ekblom P.
(1988). Tenascin during gut development: appearance in the mesenchyme shift in molecular forms, and dependence on epithelial-mesenchymal interactions. J. Cell Biol. 105, 2341–2349

[6] Aufderheide E. and

[7] Ekblom P.

[8] Bourdon M. A.,
Wikstrand C. J.,
Furthmaryr H.,
Matthews T. J. and
Bigner D. D.
(1983). Human glioma-mesenchymal extracellular matrix antigen defined by monoclonal antibody. Cancer Res. 43, 2796–2805

[9] Bourdon M. A.,

[10] Wikstrand C. J.,

[11] Furthmaryr H.,

[12] Matthews T. J. and

[13] Bigner D. D.

[14] Chiquet-Ehrismann R.
(1990). What distinguishes tenascin from fibronectin? FASEB J. 4, 2598–2604

[15] Chiquet-Ehrismann R.

[16] Chiquet-Ehrismann R.,
Mackie E. J.,
Pearson C. A. and
Sakakura T.
(1986). Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47, 131–139

[17] Chiquet-Ehrismann R.,

[18] Mackie E. J.,

[19] Pearson C. A. and

[20] Sakakura T.

[21] Chiquet-Ehrismann R.,
Kalla P.,
Pearson C. A.,
Beck K. and
Chiquet M.
(1988). Tenascin interferences with fibronectin action. Cell 53, 383–390

[22] Chiquet-Ehrismann R.,

[23] Kalla P.,

[24] Pearson C. A.,

[25] Beck K. and

[26] Chiquet M.

[27] Daniloff J. K.,
Crossin K. L.,
Pincon-Raymond M.,
Murawsky M.,
Rieger F. and
Edelman G. M.
(1989). Expression of cytotactin in the normal and regenerating nueromuscular system. J. Cell Biol. 108, 625–635

[28] Daniloff J. K.,

[29] Crossin K. L.,

[30] Pincon-Raymond M.,

[31] Murawsky M.,

[32] Rieger F. and

[33] Edelman G. M.

[34] Friedlander D. R.,
Hoffman S. and
Edelman G. M.
(1988). Functional mapping of cytotactin: proteolytic fragments active in cell-substrate adhesion. J. Cell Biol. 107, 2329–2340

[35] Friedlander D. R.,

[36] Hoffman S. and

[37] Edelman G. M.

[38] Herlyn M.,
Graevev U.,
Speicher D.,
Sela B. A.,
Bennicelli J. L.,
Kath R. and
Guerry I. V. D.
(1991). Characterization of tenascin secreted by human melanoma cells. Cancer Res. 51, 4853–4858

[39] Herlyn M.,

[40] Graevev U.,

[41] Speicher D.,

[42] Sela B. A.,

[43] Bennicelli J. L.,

[44] Kath R. and

[45] Guerry I. V. D.

[46] Inaguma Y.,
Kusakabe M.,
Mackie E. J.,
Pearson C. A.,
Chiquet-Ehrismann R. and
Sakakura T.
(1988). Epithelial induction of stromal tenascin in the mouse mammary gland: from embryogenesis to carcinogenesis. Dev. Biol. 128, 245–255

[47] Inaguma Y.,

[48] Kusakabe M.,

[49] Mackie E. J.,

[50] Pearson C. A.,

[51] Chiquet-Ehrismann R. and

[52] Sakakura T.

[53] Jones F. S.,
Hahhman S.,
Cunningham B. A. and
Edelman G. M.
(1989). A detailed structural model of cytotactin: protein, homologies, alternative RNA splicing and binding regions. Proc. Nat. Acad. Sci. USA 86, 1905–1909

[54] Jones F. S.,

[55] Hahhman S.,

[56] Cunningham B. A. and

[57] Edelman G. M.

[58] Koch M.,
Wehrle-Haller B.,
Baumgartner S.,
Spring J.,
Brubacher D. and
Chiquet M.
(1991). Epithelial synthesis of tenascin at tips of growing bronchi and graded accummulation in basement membrane and mesenchyme. Exp. Cell Res. 194, 297–300

[59] Koch M.,

[60] Wehrle-Haller B.,

[61] Baumgartner S.,

[62] Spring J.,

[63] Brubacher D. and

[64] Chiquet M.

[65] Kusakabe M.,
Yokoyama M.,
Sakakura T.,
Nomura T.,
Hosick H. L. and
Nishizuka Y.
(1988). A novel methodology for analysis of cell distribution in chimeric mouse organs using a strain specific antibody. J. Cell Biol. 107, 257–265

[66] Kusakabe M.,

[67] Yokoyama M.,

[68] Sakakura T.,

[69] Nomura T.,

[70] Hosick H. L. and

[71] Nishizuka Y.

[72] Laemmli U. K.
(1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685

[73] Laemmli U. K.

[74] Mackie E. J.,
Halfter W. and
Liverani D.
(1988). Induction of tenascin in healing wounds. J. Cell Biol. 107, 2757–2767

[75] Mackie E. J.,

[76] Halfter W. and

[77] Liverani D.

[78] Mackie E. J.,
Chiquet-Ehrismann R.,
Pearson C. A.,
Inaguma Y.,
Taya K.,
Kawarada Y. and
Sakakura T.
(1989). Tenascin is a stromal marker for epithelial malignancy in the mammary gland. Proc. Nat. Acad. Sci. USA 84, 4621–4625

[79] Mackie E. J.,

[80] Chiquet-Ehrismann R.,

[81] Pearson C. A.,

[82] Inaguma Y.,

[83] Taya K.,

[84] Kawarada Y. and

[85] Sakakura T.

[86] Natali P. G.,
Nicotra M. R.,
Bortolazzi A.,
Mottolese M.,
Coscia N.,
Bigotti A. and
Zardi L.
(1990). Expression and production of tenascin in benign and malignant lesions of melanocyte lineage. Int. J. Cancer. 46, 586–590

[87] Natali P. G.,

[88] Nicotra M. R.,

[89] Bortolazzi A.,

[90] Mottolese M.,

[91] Coscia N.,

[92] Bigotti A. and

[93] Zardi L.

[94] Nies D. E.,
Hemesath T. J.,
Kim J. H.,
Gulcher J. R. and
Stefansson K.
(1991). The complete cDNA sequence of human hexabrachion(tenascin). J. Biol. Chem. 266, 2818–2823

[95] Nies D. E.,

[96] Hemesath T. J.,

[97] Kim J. H.,

[98] Gulcher J. R. and

[99] Stefansson K.

[100] Nishi T.,
Weinstein J.,
Gillespie W. M. and
Paulson J. C.
(1991). Complete primary structure of porcine tenascin. Eur. J. Biochem. 202, 643–648

[101] Nishi T.,

[102] Weinstein J.,

[103] Gillespie W. M. and

[104] Paulson J. C.

[105] Oike Y.,
Hiraiwa H.,
Kawakatsu H.,
Nishikai M.,
Okinaka T.,
Suzuki T.,
Okada A.,
Yatani R. and
Sakakura T.
(1990). Isolation and characterization of human fibroblast tenascin. An extracellular matrix glycoprotein of interest for developmental studies. Int. J. Dev. Biol. 34, 309–317

[106] Oike Y.,

[107] Hiraiwa H.,

[108] Kawakatsu H.,

[109] Nishikai M.,

[110] Okinaka T.,

[111] Suzuki T.,

[112] Okada A.,

[113] Yatani R. and

[114] Sakakura T.

[115] Pearson C. A.,
Pearson D.,
Shibahara S.,
Hofsteenge J. and
Chiquet-Ehrismann R.
(1988). Tenascin: cDNA cloning and induction by TGF-β. EMBO J. 7, 2977–2981

[116] Pearson C. A.,

[117] Pearson D.,

[118] Shibahara S.,

[119] Hofsteenge J. and

[120] Chiquet-Ehrismann R.

[121] Sakakura T.,
Kusano I.,
Kusakabe M.,
Inaguma Y. and
Nishizuka Y.
(1987). Biology of mammary fat pad in fetal mouse: capacity to support development of various fetal epithelia in vivo. Development 100, 421–430

[122] Sakakura T.,

[123] Kusano I.,

[124] Kusakabe M.,

[125] Inaguma Y. and

[126] Nishizuka Y.

[127] Sakakura T. and
Kusano I.
(1991). Tenascin in tissue perturbation repair. Acta Pathologica Japonica 41, 247–258

[128] Sakakura T. and

[129] Kusano I.

[130] Saga Y.,
Tsukamoto T.,
Jing N.,
Kusakabe M. and
Sakakura T.
(1991). Mouse tenascin: cDNA cloning structure and temporal expression of isoforms. Gene 104, 177–185

[131] Saga Y.,

[132] Tsukamoto T.,

[133] Jing N.,

[134] Kusakabe M. and

[135] Sakakura T.

[136] Siri A.,
Carnemolla B.,
Saginati M.,
Leprini A.,
Casari G.,
Baralle F. and
Zardi L.
(1991). Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucl. Acid Res. 19, 525–531

[137] Siri A.,

[138] Carnemolla B.,

[139] Saginati M.,

[140] Leprini A.,

[141] Casari G.,

[142] Baralle F. and

[143] Zardi L.

[144] Tucker R. P.
(1991). The sequential expression of tenascin mRNA in epithelium and mesenchyme during feather morphogenesis. Roux's Arch. Dev. Biol. 200, 108–112

[145] Tucker R. P.

[146] Tucker R. P. and
McKay S.E.
(1991). The expression of tenascin by neural crest and glia. Development 112, 1031–1039

[147] Tucker R. P. and

[148] McKay S.E.

[149] Tsukamoto T.,
Kusakabe M. and
Saga Y.
(1991). In situ hybridization with non-radioactive digoxigenin-11-UTP-labeled cRNA probes: localization of developmentally regulated mouse tenascin mRNAs. Int. J. Dev. Biol. 35, 25–32

[150] Tsukamoto T.,

[151] Kusakabe M. and

[152] Saga Y.

[153] Vainio S.,
Jalkanen M. and
Thesleff I.
(1989). Syndecan and tenascin expression is inducted by epithelial-mesenchymal interactions in embryonic tooth mesenchyme. J. Cell Biol. 108, 1945–1954

[154] Vainio S.,

[155] Jalkanen M. and

[156] Thesleff I.

[157] Weller A.,
Beck S. and
Ekblom P.
(1991). Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis. J. Cell Biol. 112, 355–362

[158] Weller A.,

[159] Beck S. and

[160] Ekblom P.

[161] Whitby D. J. and
Ferguson M. W. J.
(1991). The extracellular matrix of lipwounds in fetal, neonatal and adult mice. Development 112, 538–587

[162] Whitby D. J. and

[163] Ferguson M. W. J.

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Other journals from The Company of Biologists

Introducing FocalPlane’s new Community Manager, Esperanza Agullo-Pascual

New funding scheme supports sustainable events

Read & Publish participation continues to grow

Cell scientist to watch: Romain Levayer

Live lactating mammary tissue

JCS and COVID-19

Main menu

User menu

Search

Summary

REFERENCES

Citation Manager Formats

Article navigation

Related articles

Cited by...

More in this TOC section

Similar articles

Other journals from The Company of Biologists

Introducing FocalPlane’s new Community Manager, Esperanza Agullo-Pascual

New funding scheme supports sustainable events

Read & Publish participation continues to grow

Cell scientist to watch: Romain Levayer

Live lactating mammary tissue

JCS and COVID-19