Study of interaction between extracellular matrix proteins and receptors of CD133+ stem cells and CD133– differentiated glioma cells
https://doi.org/10.17650/2313-805X-2019-6-1-63-72
Abstract
Background. Treatment of glioblastoma multiforme remains little effective due to the rapidly developing recurrence of the tumor, due to its high tumorigenic potential, resistance to chemoradiation therapy and increased dissemination of glioma stem cells (GSC). Molecular mechanisms of these cell interaction with extracellular matrix (ECM) are practically not studied. At present, it is also not clear the signaling of the ECM-receptor interaction (ECM-RI) differs for GSC and differentiated glioma cells (GDC).
Objective: using high-resolution proteomic mass spectrometry to study the determinant expression of the ECM-receptor interaction signaling cascade in CD133+ GSC and CD133– GDC.
Results. 1990 proteins are identified, 18 of which are associated with the ECM-RI process. Positive regulation of 14 ECM-RI proteins was found in CD133+ GSC compared with CD133– GDC, ten had more than 2 times increased expression. Increase in the CD133+ GSC level of 4 proteins activating the ECM-RI signaling cascade was noted.
Conclusion. Important regularities are determined that could be used for the development of new approaches for detection of potential therapy targets of glioblastoma multiforme.
About the Authors
V. E. ShevchenkoRussian Federation
24 Kashirskoe Shosse, Moscow 115478.
I. S. Bryukhovetskiy
Russian Federation
8 Sukhanova St., Vladivostok 690091; 17 Pal’chevskogo St., Vladivostok690059.
E. A. Savchenko
Russian Federation
13A Kolomenskiy Proezd, Moscow 115446.
N. E. Arnotskaya
Russian Federation
24 Kashirskoe Shosse, Moscow 115478.
References
1. Holland E.C. Glioblastoma multiforme: the terminator. Proc Natl Acad Sci USA 2000;97(12):6242-4. PMID: 10841526.
2. Huse J.T., Holland E.C. Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer 2010;10(5):319—31. DOI: 10.1038/nrc2818. PMID: 20414201.
3. Beauchesne P. Extra-neural metastases of malignant gliomas: Myth or reality? Cancers 2011;3:461-77. DOI: 10.3390/cancers3010461. PMID: 24212625.
4. Bolteus A.J., Berens M.E., Pilkington G.J. Migration and invasion in brain neoplasms. Curr Neurol Neurosci Rep 2001;1(3):225—32. PMID: 11898522.
5. Cuddapah V.A., Robel S., Watkins S. et al. A neurocentric perspective on glioma invasion. Nat Rev Neurosci 2014;15(7):455—65. DOI: 10.1038/nrn3765. PMID: 24946761.
6. Claes A., Idema A.J., Wesseling P. Diffuse glioma growth: a guerilla war. Acta Neuropathol 2007;114(5):443—58. DOI: 10.1007/s00401-007-0293-7. PMID: 17805551.
7. Cayre M., Canoll P., Goldman J.E. Cell migration in the normal and pathological postnatal mammalian brain. Prog Neurobiol 2009;88(1):41—63. DOI: 10.1016/j.pneurobio.2009.02.001. PMID: 19428961.
8. Le Clainche C., Carlier M.F. Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev 2008;88(2):489—513. DOI: 10.1152/physrev.00021.2007. PMID: 18391171.
9. Huttenlocher A., Horwitz A.R. Integrins in cell migration. Cold Spring Harbor Perspect Biol 2011;3(9):a005074. DOI: 10.1101/cshperspect.a005074. PMID: 21885598.
10. Roos A., Ding Z., Loftus J.C., Tran N.L. Molecular and microenvironmental determinants of glioma stem-like cellsurvival and invasion. Front Oncol 2017;7:120. DOI: 10.3389/fonc.2017.00120. PMID: 28670569.
11. Kang S.K., Park J.B., Cha S.H. Multipotent, dedifferentiated cancer stemlike cells from brain gliomas. Stem Cells Dev 2006;15(3):423—35. DOI: 10.1089/scd.2006.15.423. PMID: 16846378.
12. Chen J., McKay R.M., Parada L.F. Malignant glioma: lessons from genomics, mouse models and stem cells. Cell 2012;149(1):36—47. DOI: 10.1016/j.cell.2012.03.009. PMID: 22464322.
13. Persano L., Rampazzo E., Basso G. et al. Glioblastoma cancer stem cells: Role of the microenvironment and therapeutic targeting. Biochem Pharmacol 2013;85(5):612—22. DOI: 10.1016/j.bcp.2012.10.001. PMID: 23063412.
14. Ortensi B., Osti D., Pellegatta S. et al. Rai is a new regulator of neural progenitor migration and glioblastoma invasion. Stem Cells 2012;30(5):817—32. DOI: 10.1002/stem.1056. PMID: 22311806.
15. Cheng L., Wu Q., Guryanova O.A. et al. Elevated invasive potential of glioblastoma stem cells. Biochem Biophys Res Commun 2011;406(4):643—8. DOI: 10.1016/j.bbrc.2011.02.123. PMID: 21371437.
16. Safa A.R., Saadatzadeh M.R., Cohen-Gadol A.A. et al. Glioblastoma stem cells (GSCs) epigenetic plasticity and interconversion between differentiated non-GSCs and GSCs. Genes Dis 2015;2(2):152—63. DOI: 10.1016/j.gendis.2015.02.001. PMID: 26137500.
17. Tirino V., Desiderio V., Paino F. et al. Methods for cancer stem cell detection and isolation. Methods Mol Biol 2012;879:513—29. DOI: 10.1007/978-1-61779-815-3_32. PMID: 22610581.
18. Bryukhovetskiy A., Shevchenko V., Kovalev S. et al. To the novel paradigmof proteome-based cell therapy of tumors: through comparative proteome mapping of tumor stem cells and tissue-specific stem cells of humans. Cell Transplantation 2014;9:1—42. DOI: 10.3727/096368914X684907. PMID: 25303679.
19. Singh S.K., Hawkins C., Clarke I.D. et al. Identification of human brain tumour initiating cells. Nature 2004;432(7015):396—401. DOI: 10.1038/nature03128. PMID: 15549107.
20. Beier D., Hau P., Proescholdt M. et al. CD133(+) and CD133(—) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007;67(9):4010—5. PMID: 17483311.
21. Beier C.P., Beier D. CD133 negative cancer stem cells in glioblastoma. Front Biosci (Elite Ed) 2011;3:701—10. PMID: 21196345.
22. Munthe S., Petterson S.A., Dahlrot R.H. et al. Glioma cells in the tumor periphery have a stem cell phenotype. PloS One 2016;11(5):e0155106. DOI: 10.1371/journal.pone.0155106. PMID: 27171431.
23. Cheng L., Huang Z., Zhou W. et al. Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 2013;153(1):139—52. DOI: 10.1016/j.cell.2013.02.021. PMID: 23540695.
24. Hambardzumyan D., Bergers G. Glioblastoma: defining tumor niches. Trends Cancer 2015;1(4):252—65. DOI: 10.1016/j.trecan.2015.10.009. PMID: 27088132.
25. Matsukado Y., Maccarty C.S., Kernohan J.W. The growth of glioblastoma multiforme (astrocytomas, grades 3 and 4) in neurosurgical practice. J Neurosurg 1961;18:636—44. DOI: 10.3171/jns.1961.18.5.0636. PMID: 13768222.
26. Muller C., Holtschmidt J., Auer M. et al. Hematogenous dissemination of glioblastoma multiforme. Sci Transl Med 2014;6(247):247ra101. DOI: 10.1126/scitransLmed.3009095. PMID: 25080476.
27. Glass R., Synowitz M. CNS macrophages and peripheral myeloid cells in brain tumours. Acta Neuropathol 2014;128:347-62. DOI: 10.1007/s00401-014-1274-2. PMID: 24722970.
28. Wu C. Focal adhesion: a focal point in current cell biology and molecular medicine. Cell Adhesion Mig 2007;1(1):13—8. PMID: 19262093.
29. Arnaout M.A., Goodman S.L., Xiong J.P. Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol 2007;19(5):495—507. DOI: 10.1016/j.ceb.2007.08.002. PMID: 17928215.
30. Humphries J.D., Byron A., Humphries M.J. Integrin ligands at a glance. J Cell Sci 2006; 119(Pt 19):3901—3. DOI: 10.1242/jcs.03098. PMID: 16988024.
31. Madamanchi A., Santoro SA., Zutter M.M. alpha2beta1 Integrin. Adv Exp Med Biol 2014;819:41-60. DOI: 10.1007/978-94-017-9153-3_3. PMID: 25023166.
32. Danen E.H. Integrins: regulators of tissue function and cancer progression. Curr Pharm Des 2005;11(7):881—91. PMID: 15777241.
33. Xie J.J., Guo J.C., Wu Z.Y. et al. Integrin alpha5 promotes tumor progression and is an independent unfavorable prognostic factor in esophageal squamous cell carcinoma. Hum Pathol 2016;48:69-75. DOI: 10.1016/j.humpath.2015.09.029. PMID: 26772401.
34. Feng L., Ma J., Ji H. et al. miR-330-5p suppresses glioblastoma cell proliferation and invasiveness through targeting ITGA5. Biosci Rep 2017;37(3). DOI: 10.1042/BSR20170019. PMID: 28336765.
35. Skuli N., Monferran S., Delmas C. et al. Alphavbeta3/alphavbeta5 integrins-FAK-RhoB: a novel pathway for hypoxia regulation in glioblastoma. Cancer Res 2009;69(8):3308—16. DOI: 10.1158/0008-5472.CAN-08-2158. PMID: 19351861.
36. Desgrosellier J.S., Cheresh D.A. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010;10(1):9—22. DOI: 10.1038/nrc2748. PMID: 20029421.
37. Klekner A., Hutoczki G., Virga J. et al. Expression pattern of invasionrelated molecules in the peritumoral brain. Clin Neurol Neurosurg 2015;139:138—43. PMID: 26451999.
38. Serres E., Debarbieux F., Stanchi F. et al. Fibronectin expression in glioblastomas promotes cell cohesion, collective invasion of basement membrane in vitro and orthotopic tumor growth in mice. Oncogene 2014;33(26):3451—62. DOI: 10.1038/onc.2013.305. PMID: 23912459.
39. Ryan M.C., Christiano A.M., Engvall E. et al. The functions of laminins: lessons from in vivo studies. Matrix Biol 1996;15(6):369—81. PMID: 9049976.
40. Caffo M., Germano A., Caruso G. et al. An immunohistochemical study of extracellular matrixproteins laminin, fibronectin and type IV collagen in paediatric glioblastoma multiforme. Acta Neurochir (Wien) 2004;146(10):1113—8. DOI: 10.1007/s00701-004-0344-y. PMID: 15309586.
41. Yu Q., Xue Y., Liu J. et al. Fibronectin promotes the malignancy of glioma stemlike cells via modulation of cell adhesion, differentiation, proliferation and chemoresistance. Front Mol Neurosci 2018;11:130. DOI: 10.3389/fnmol.2018.00130. PMID: 29706869.
42. Yeh W.L., Lu D.Y., Liou H.C. et al. A forward loop between glioma and microglia: glioma-derived extracellular matrix-activated microglia secrete IL-18 to enhance the migration of glioma cells. J Cell Physiol 2012;227(2):558—68. DOI: 10.1002/jcp.22746. PMID: 21442623
43. Wiranowska M., Ladd S., Moscinski L.C. et al. Modulation of hyaluronan production by CD44 positive glioma cells. Int J Cancer 2010;127(3):532—42. DOI: 10.1002/ijc.25085. PMID: 19957333.
44. Turley E.A., Noble P.W., Bourguignon L.Y. Signaling properties of hyaluronan receptors. J Biol Chem 2002;277(7):4589—92. DOI: 10.1074/jbc.R100038200. PMID: 11717317.
45. Anido J., Saez-Borderias A., Gonzalez-Junca A. et al. TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell 2010;18(6):655—68. DOI: 10.1016/j.ccr.2010.10.023. PMID: 21156287.
46. Hamilton S.R., Fard S.F., Paiwand F.F. et al. The hyaluronan receptors CD44 and Rhamm(CD168) form complexes with ERK1,2 that sustain high basal motility in breast cancer cells. J Biol Chem 2007;282(22):16667—80. DOI: 10.1074/jbc.M702078200. PMID: 17392272.
47. Zhao T., Guan L., Yu Y. et al. Kindlin-2 promotes genome instability in breast cancer cells. Cancer Lett 2013;330(2):208—16. DOI: 10.1016/j.canlet.2012.11.043. PMID: 23211537.
48. Ghobrial I.M., Witzig T.E., Adjei A.A. Targeting apoptosis pathways in cancer therapy. CA Cancer J Clin 2005;55(3):178—94. PMID: 15890640.
49. Kim Y.M., Kim E.C., Kim Y. The human lysyl oxidase-like 2 protein functions as an amine oxidase toward collagen and elastin. Mol Biol Rep 2011;38(1):145—9. DOI: 10.1007/s11033-010-0088-0. PMID: 20306300.
50. Du X.G., Zhu M.J. Clinical relevance of lysyl oxidase-like 2 and functional mechanisms in glioma. Onco Targets Ther 2018;11:2699—708. DOI: 10.2147/OTT.S164056. PMID: 29785119.
51. Guo Q., Song Y., Zhang H. et al. Detection of hypermethylated fibrillin-1 in the stool samples of colorectal cancer patients. Med Oncol 2013;30(4):695. DOI: 10.1007/s12032-013-0695-4. PMID: 23963856.
52. Cierna Z., Mego M., Jurisica I. et al. Fibrillin-1 (FBN-1) a new marker of germ cell neoplasia in situ. BMC Cancer 2016;16:597. DOI: 10.1186/s12885-016-2644-z. PMID: 27487789.
Review
For citations:
Shevchenko V.E., Bryukhovetskiy I.S., Savchenko E.A., Arnotskaya N.E. Study of interaction between extracellular matrix proteins and receptors of CD133+ stem cells and CD133– differentiated glioma cells. Advances in Molecular Oncology. 2019;6(1):63-72. (In Russ.) https://doi.org/10.17650/2313-805X-2019-6-1-63-72