3,406
Views
70
CrossRef citations to date
0
Altmetric
Editorial

Brain tumor-initiating cells export tenascin-C associated with exosomes to suppress T cell activity

ORCID Icon, ORCID Icon, ORCID Icon, , , ORCID Icon, ORCID Icon & ORCID Icon show all
Article: e1478647 | Received 02 Jan 2018, Accepted 15 May 2018, Published online: 06 Aug 2018

References

  • Stupp R, Mason WP, Van Den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–996. doi:10.1056/NEJMoa043330.
  • Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, Parada LF. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 2012;488:522–526. doi:10.1038/nature11287.
  • Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–760. doi:10.1038/nature05236.
  • Eramo A, Ricci-Vitiani L, Zeuner A, Pallini R, Lotti F, Sette G, Pilozzi E, Larocca LM, Peschle C, De Maria R. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ. 2006;13:1238–1241. doi:10.1038/sj.cdd.4401872.
  • Jacobs JF, Idema AJ, Bol KF, Nierkens S, Grauer OM, Wesseling P, Grotenhuis JA, Hoogerbrugge PM, De Vries IJM, Adema GJ. Regulatory T cells and the PD-L1/PD-1 pathway mediate immune suppression in malignant human brain tumors. Neuro Oncol. 2009;11:394–402. doi:10.1215/15228517-2008-104.
  • Gabrusiewicz K, Rodriguez B, Wei J, Hashimoto Y, Healy LM, Maiti SN, Thomas G, Zhou S, Wang Q, Elakkad A, et al. Glioblastoma-infiltrated innate immune cells resemble M0 macrophage phenotype. JCI Insight. 2016:1.
  • Wei J, Barr J, Kong LY, Wang Y, Wu A, Sharma AK, Gumin J, Henry V, Colman H, Priebe W, et al. Glioblastoma cancer-initiating cells inhibit T-cell proliferation and effector responses by the signal transducers and activators of transcription 3 pathway. Mol Cancer Ther. 2010;9:67–78. doi:10.1158/1535-7163.MCT-09-0734.
  • Dix AR, Brooks WH, Roszman TL, Morford LA. Immune defects observed in patients with primary malignant brain tumors. J Neuroimmunol. 1999;100:216–232. doi:10.1016/S0165-5728(99)00203-9.
  • Ashkenazi E, Deutsch M, Tirosh R, Weinreb A, Tsukerman A, Brodie C. A selective impairment of the IL-2 system in lymphocytes of patients with glioblastomas: increased level of soluble IL-2R and reduced protein tyrosine phosphorylation. Neuroimmunomodulation. 1997;4:49–56. doi:10.1159/000097315.
  • Reinhard J, Brosicke N, Theocharidis U, Faissner A. The extracellular matrix niche microenvironment of neural and cancer stem cells in the brain. Int J Biochem Cell Biol. 2016;81:174–183. doi:10.1016/j.biocel.2016.05.002.
  • Bellail AC, Hunter SB, Brat DJ, Tan C, Van Meir EG. Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion. Int J Biochem Cell Biol. 2004;36:1046–1069. doi:10.1016/j.biocel.2004.01.013.
  • Sarkar S, Mirzaei R, Zemp FJ, Wei W, Senger DL, Robbins SM, Yong VW. Activation of NOTCH signaling by tenascin-C promotes growth of human brain tumor-initiating cells. Cancer Res. 2017;77:3231–3243. doi:10.1158/0008-5472.CAN-16-2171.
  • Brosicke N, Van Landeghem FK, Scheffler B, Faissner A. Tenascin-C is expressed by human glioma in vivo and shows a strong association with tumor blood vessels. Cell Tissue Res. 2013;354:409–430. doi:10.1007/s00441-013-1704-9.
  • Herold-Mende C, Mueller MM, Bonsanto MM, Schmitt HP, Kunze S, Steiner HH. Clinical impact and functional aspects of tenascin-C expression during glioma progression. Int J Cancer. 2002;98:362–369. doi:10.1002/ijc.10233.
  • Leins A, Riva P, Lindstedt R, Davidoff MS, Mehraein P, Weis S. Expression of tenascin-C in various human brain tumors and its relevance for survival in patients with astrocytoma. Cancer. 2003;98:2430–2439. doi:10.1002/(ISSN)1097-0142.
  • Garikapati KR, Patel N, Makani VK, Cilamkoti P, Bhadra U, Bhadra MP. Down-regulation of BORIS/CTCFL efficiently regulates cancer stemness and metastasis in MYCN amplified neuroblastoma cell line by modulating Wnt/beta-catenin signaling pathway. Biochem Biophys Res Commun. 2017;484:93–99. doi:10.1016/j.bbrc.2017.01.066.
  • Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, Downey RJ, Manova-Todorova K, Brogi E, Massagué J. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med. 2011;17:867–874. doi:10.1038/nm.2379.
  • Hibino S, Kato K, Kudoh S, Yagita H, Okumura K. Tenascin suppresses CD3-mediated T cell activation. Biochem Biophys Res Commun. 1998;250:119–124. doi:10.1006/bbrc.1998.9258.
  • Puente Navazo MD, Valmori D, Ruegg C. The alternatively spliced domain TnFnIII A1A2 of the extracellular matrix protein tenascin-C suppresses activation-induced T lymphocyte proliferation and cytokine production. J Immunol (Baltimore, Md: 1950). 2001;167:6431–6440. doi:10.4049/jimmunol.167.11.6431.
  • Jachetti E, Caputo S, Mazzoleni S, Brambillasca CS, Parigi SM, Grioni M, Piras IS, Restuccia U, Calcinotto A, Freschi M, et al. Tenascin-C protects cancer stem-like cells from immune surveillance by arresting T-cell activation. Cancer Res. 2015;75:2095–2108. doi:10.1158/0008-5472.CAN-14-2346.
  • Huang JY, Cheng YJ, Lin YP, Lin HC, Su CC, Juliano R, Yang B-C. Extracellular matrix of glioblastoma inhibits polarization and transmigration of T cells: the role of tenascin-C in immune suppression. J Immunol (Baltimore, Md: 1950). 2010;185:1450–1459. doi:10.4049/jimmunol.0901352.
  • Didem T, Faruk T, Senem K, Derya D, Murat S, Murat G, Oznur K. Clinical significance of serum tenascin-c levels in epithelial ovarian cancer. Tumour Biol: J Int Soc Oncodevelopmental Biol Med. 2014;35:6777–6782. doi:10.1007/s13277-014-1923-z.
  • Riedl S, Bodenmuller H, Hinz U, Holle R, Moller P, Schlag P, Herfarth C, Faissner A. Significance of tenascin serum level as tumor marker in primary colorectal carcinoma. Int J Cancer. 1995;64:65–69. doi:10.1002/(ISSN)1097-0215.
  • Pardridge WM. Blood-brain barrier drug targeting enables neuroprotection in brain ischemia following delayed intravenous administration of neurotrophins. Adv Exp Med Biol. 2002;513:397–430.
  • Erickson HP, Bourdon MA. 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.
  • Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell. 2016;30:836–848. doi:10.1016/j.ccell.2016.10.009.
  • Zhou W, Fong MY, Min Y, Somlo G, Liu L, Palomares MR, Yu Y, Chow A, O’Connor S, Chin A, et al. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell. 2014;25:501–515. doi:10.1016/j.ccr.2014.03.007.
  • Tominaga N, Kosaka N, Ono M, Katsuda T, Yoshioka Y, Tamura K, Lötvall J, Nakagama H, Ochiya T. Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier. Nat Commun. 2015;6:6716. doi:10.1038/ncomms7716.
  • Domenis R, Cesselli D, Toffoletto B, Bourkoula E, Caponnetto F, Manini I, Beltrami AP, Ius T, Skrap M, Di Loreto C, et al. Systemic T cells immunosuppression of glioma stem cell-derived exosomes is mediated by monocytic myeloid-derived suppressor cells. PLoS One. 2017;12:e0169932. doi:10.1371/journal.pone.0169932.
  • Skog J, Wurdinger T, Van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–1476. doi:10.1038/ncb1800.
  • Pisklakova A, McKenzie B, Zemp F, Lun X, Kenchappa RS, Etame AB, Rahman MM, Reilly K, Pilon-Thomas S, McFadden G, et al. M011L-deficient oncolytic myxoma virus induces apoptosis in brain tumor-initiating cells and enhances survival in a novel immunocompetent mouse model of glioblastoma. Neuro Oncol. 2016. doi:10.1093/neuonc/now006.
  • Kominsky S, Johnson HM, Bryan G, Tanabe T, Hobeika AC, Subramaniam PS, Torres B. IFNgamma inhibition of cell growth in glioblastomas correlates with increased levels of the cyclin dependent kinase inhibitor p21WAF1/CIP1. Oncogene. 1998;17:2973–2979. doi:10.1038/sj.onc.1202217.
  • Sarkar S, Doring A, Zemp FJ, Silva C, Lun X, Wang X, Kelly J, Hader W, Hamilton M, Mercier P, et al. Therapeutic activation of macrophages and microglia to suppress brain tumor-initiating cells. Nat Neurosci. 2014;17:46–55. doi:10.1038/nn.3597.
  • Zou JP, Morford LA, Chougnet C, Dix AR, Brooks AG, Torres N, Shuman JD, Coligan JE, Brooks WH, Roszman TL, et al. Human glioma-induced immunosuppression involves soluble factor(s) that alters monocyte cytokine profile and surface markers. J Immunol (Baltimore, Md: 1950). 1999;162:4882–4892.
  • Nduom EK, Weller M, Heimberger AB. Immunosuppressive mechanisms in glioblastoma. Neuro Oncol. 2015;17(Suppl 7):vii9–vii14. doi:10.1093/neuonc/nov151.
  • Lochter A, Vaughan L, Kaplony A, Prochiantz A, Schachner M, Faissner A. J1/tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth. J Cell Biol. 1991;113:1159–1171. doi:10.1083/jcb.113.5.1159.
  • Garcion E, Halilagic A, Faissner A, ffrench-Constant C. Generation of an environmental niche for neural stem cell development by the extracellular matrix molecule tenascin C. Development. 2004;131:3423–3432. doi:10.1242/dev.01202.
  • Karus M, Denecke B, ffrench-Constant C, Wiese S, Faissner A. The extracellular matrix molecule tenascin C modulates expression levels and territories of key patterning genes during spinal cord astrocyte specification. Development. 2011;138:5321–5331. doi:10.1242/dev.067413.
  • Tucker RP, Chiquet-Ehrismann R. Tenascin-C: its functions as an integrin ligand. Int J Biochem Cell Biol. 2015;65:165–168. doi:10.1016/j.biocel.2015.06.003.
  • Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006. Chapter 3:Unit3.22. doi:10.1002/0471143030.cb0322s30.
  • Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401. doi:10.1038/nature03128.
  • Cao L, Zhou Y, Zhai B, Liao J, Xu W, Zhang R, Li J, Zhang Y, Chen L, Qian H, et al. Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines. BMC Gastroenterol. 2011;11:71. doi:10.1186/1471-230X-11-71.
  • Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11:69–82. doi:10.1016/j.ccr.2006.11.020.
  • Faissner A, Roll L, Theocharidis U. Tenascin-C in the matrisome of neural stem and progenitor cells. Mol Cell Neurosci. 2017;81:22–31. doi:10.1016/j.mcn.2016.11.003.
  • Orend G, Chiquet-Ehrismann R. Tenascin-C induced signaling in cancer. Cancer Lett. 2006;244:143–163. doi:10.1016/j.canlet.2006.02.017.
  • Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol. 2004;5:816–826. doi:10.1038/nrm1490.
  • Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer. 2010;10:9–22. doi:10.1038/nrc2748.
  • Paron I, Berchtold S, Voros J, Shamarla M, Erkan M, Hofler H, Esposito I, Gottardi C. Tenascin-C enhances pancreatic cancer cell growth and motility and affects cell adhesion through activation of the integrin pathway. PLoS One. 2011;6:e21684. doi:10.1371/journal.pone.0021684.
  • Saci A, Cantley LC, Carpenter CL. Rac1 regulates the activity of mTORC1 and mTORC2 and controls cellular size. Mol Cell. 2011;42:50–61. doi:10.1016/j.molcel.2011.03.017.
  • Hauzenberger D, Olivier P, Gundersen D, Ruegg C. Tenascin-C inhibits beta1 integrin-dependent T lymphocyte adhesion to fibronectin through the binding of its fnIII 1-5 repeats to fibronectin. Eur J Immunol. 1999;29:1435–1447. doi:10.1002/(SICI)1521-4141(199905)29:05<1435::AID-IMMU1435>3.0.CO;2-N.
  • Hellwinkel JE, Redzic JS, Harland TA, Gunaydin D, Anchordoquy TJ, Graner MW. Glioma-derived extracellular vesicles selectively suppress immune responses. Neuro Oncol. 2016;18:497–506. doi:10.1093/neuonc/nov170.
  • Ren Y, Yang J, Xie R, Gao L, Yang Y, Fan H, Qian K. Exosomal-like vesicles with immune-modulatory features are present in human plasma and can induce CD4+ T-cell apoptosis in vitro. Transfusion. 2011;51:1002–1011. doi:10.1111/trf.2011.51.issue-5.
  • Esposito I, Penzel R, Chaib-Harrireche M, Barcena U, Bergmann F, Riedl S, Kayed H, Giese N, Kleeff J, Friess H, et al. Tenascin C and annexin II expression in the process of pancreatic carcinogenesis. J Pathol. 2006;208:673–685. doi:10.1002/(ISSN)1096-9896.
  • Czopka T, Von Holst A, ffrench-Constant C, Faissner A. Regulatory mechanisms that mediate tenascin C-dependent inhibition of oligodendrocyte precursor differentiation. J Neuroscience: Official Journal Soc Neurosci. 2010;30:12310–12322. doi:10.1523/JNEUROSCI.4957-09.2010.
  • Gotz B, Scholze A, Clement A, Joester A, Schutte K, Wigger F, Frank R, Spiess E, Ekblom P, Faissner A. Tenascin-C contains distinct adhesive, anti-adhesive, and neurite outgrowth promoting sites for neurons. J Cell Biol. 1996;132:681–699. doi:10.1083/jcb.132.4.681.
  • Lun X, Wells JC, Grinshtein N, King JC, Hao X, Dang NH, Wang X, Aman A, Uehling D, Datti A, et al. Disulfiram when combined with copper enhances the therapeutic effects of temozolomide for the treatment of glioblastoma. Clin Cancer Res. 2016;22:3860–3875. doi:10.1158/1078-0432.CCR-15-1798.
  • Vecil GG, Larsen PH, Corley SM, Herx LM, Besson A, Goodyer CG, Yong VW. Interleukin-1 is a key regulator of matrix metalloproteinase-9 expression in human neurons in culture and following mouse brain trauma in vivo. J Neurosci Res. 2000;61:212–224. doi:10.1002/(ISSN)1097-4547.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.