Endogenous tenascin-C enhances glioblastoma invasion with reactive change of surrounding brain tissue

Cancer Science

Volumn 100, Issue 8, 2009, Pages 1451-1459

  Hirata, Eishu ^a   Arakawa, Yoshiki ^a   Shirahata, Mitsuaki ^a   Yamaguchi, Makoto ^a   Kishi, Yo ^a   Okada, Takashi ^a   Takahashi, Jun A ^b   Matsuda, Michiyuki ^a   Hashimoto, Nobuo ^c  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b Kitano Hospital   (Japan)

^c NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; INTEGRIN; TENASCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CANCER GROWTH; CANCER INVASION; CELL INFILTRATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; MOUSE; NEUROPATHOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN FUNCTION; TUMOR XENOGRAFT;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FLUOCINOLONE ACETONIDE; GENETIC VECTORS; GLIOBLASTOMA; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; LENTIVIRUS; MALE; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; RNA INTERFERENCE; RNA, SMALL INTERFERING; TENASCIN; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 67650648500     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2009.01189.x     Document Type: Article

References (50)

1. Kleihues P, Burger PC, Scheithauer BW. The new WHO classification of brain tumours. Brain Pathol 1993; 3: 255-68.
2. Nakada M, Nakada S, Demuth T, Tran NL, Hoelzinger DB, Berens ME. Molecular targets of glioma invasion. Cell Mol Life Sci 2007; 64: 458-78.
3. Henson JW, Gaviani P, Gonzalez RG. MRI in treatment of adult gliomas. Lancet Oncol 2005; 6: 167-75.
4. Ishihara H, Kubota H, Lindberg RL et al. Endothelial cell barrier impairment induced by glioblastomas and transforming growth factor beta2 involves matrix metalloproteinases and tight junction proteins. J Neuropathol Exp Neurol 2008; 67: 435-48.
5. McKeever PE, Varani J, Papadopoulos SM, Wang M, McCoy JP. Products of cells from gliomas: IX. Evidence that two fundamentally different mechanisms change extracellular matrix expression by gliomas. J Neurooncol 1995; 24: 267-80.
6. Ganslandt O, Stadlbauer A, Fahlbusch R et al. Proton magnetic resonance spectroscopic imaging integrated into image-guided surgery: Correlation to standard magnetic resonance imaging and tumor cell density. Neurosurgery 2005; 56: 291-8.
7. Claes A, Idema AJ, Wesseling P. Diffuse glioma growth: A guerilla war. Acta Neuropathol 2007; 114: 443-58.
8. Nutt CL, Mani DR, Betensky RA et al. Gene expression-based classification of malignant gliomas correlates better with survival than histological classification. Cancer Res 2003; 63: 1602-7.
9. Shirahata M, Iwao-Koizumi K, Saito S et al. Gene expression-based molecular diagnostic system for malignant gliomas is superior to histological diagnosis. Clin Cancer Res 2007; 13: 7341-56.
10. Demuth T, Berens ME. Molecular mechanisms of glioma cell migration and invasion. J Neurooncol 2004; 70: 217-28.
11. Furnari FB, Fenton T, Bachoo RM et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007; 21: 2683-710.
12. Yamana N, Arakawa Y, Nishino T et al. The Rho-mDia1 pathway regulates cell polarity and focal adhesion turnover in migrating cells through mobilizing Apc and c-Src. Mol Cell Biol 2006; 26: 6844-58.
13. Katz BZ, Romer L, Miyamoto S et al. Targeting membrane-localized focal adhesion kinase to focal adhesions: Roles of tyrosine phosphorylation and SRC family kinases. J Biol Chem 2003; 278: 29115-20.
14. Orend G, Chiquet-Ehrismann R. Tenascin-C induced signaling in cancer. Cancer Lett 2006; 244: 143-63.
15. Chiquet-Ehrismann R. Tenascins. Int J Biochem Cell Biol 2004; 36: 986-90.
16. Kawakatsu H, Shiurba R, Obara M, Hiraiwa H, Kusakabe M, Sakakura T. Human carcinoma cells synthesize and secrete tenascin in vitro. Jpn J Cancer Res 1992; 83: 1073-80.
17. Sugawara I, Hirakoshi J, Kusakabe M, Masunaga A, Itoyama S, Sakakura T. Relationships among tenascin expression, DNA ploidy patterns, and multidrug resistance gene product (P-glycoprotein) in human colon carcinoma. Jpn J Cancer Res 1993; 84: 703-7.
18. Sarkar S, Nuttall RK, Liu S, Edwards DR, Yong VW. Tenascin-C stimulates glioma cell invasion through matrix metalloproteinase-12. Cancer Res 2006; 66: 11771-80.
19. Zagzag D, Shiff B, Jallo GI et al. Tenascin-C promotes microvascular cell migration and phosphorylation of focal adhesion kinase. Cancer Res 2002; 62: 2660-8.
20. Ruiz C, Huang W, Hegi ME et al. Growth promoting signaling by tenascin-C [corrected]. Cancer Res 2004; 64: 7377-85.
21. Deryugina EI, Bourdon MA. Tenascin mediates human glioma cell migration and modulates cell migration on fibronectin. J Cell Sci 1996; 109 (Pt 3): 643-52.
22. Lange K, Kammerer M, Hegi ME et al. Endothelin receptor type B counteracts tenascin-C-induced endothelin receptor type A-dependent focal adhesion and actin stress fiber disorganization. Cancer Res 2007; 67: 6163-73.
23. Matsumoto K, Takahashi K, Yoshiki A, Kusakabe M, Ariga H. Invasion of melanoma in double knockout mice lacking tenascin-X and tenascin-C. Jpn J Cancer Res 2002; 93: 968-75.
24. Rubinson DA, Dillon CP, Kwiatkowski AV et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 2003; 33: 401-6.
25. Arakawa Y, Cordeiro JV, Schleich S, Newsome TP, Way M. The release of vaccinia virus from infected cells requires RhoA-mDia modulation of cortical actin. Cell Host Microbe 2007; 1: 227-40.
26. Candolfi M, Curtin JF, Nichols WS et al. Intracranial glioblastoma models in preclinical neuro-oncology: Neuropathological characterization and tumor progression. J Neurooncol 2007; 85: 133-48.
27. Toda Y, Kono K, Abiru H et al. Application of tyramide signal amplification system to immunohistochemistry: A potent method to localize antigens that are not detectable by ordinary method. Pathol Int 1999; 49: 479-83.
28. Oda M, Arakawa Y, Kano H et al. Quantitative analysis of topoisomerase IIalpha to rapidly evaluate cell proliferation in brain tumors. Biochem Biophys Res Commun 2005; 331: 971-6.
29. Chiquet-Ehrismann R, Chiquet M. Tenascins: Regulation and putative functions during pathological stress. J Pathol 2003; 200: 488-99.
30. Midwood KS, Schwarzbauer JE. Tenascin-C modulates matrix contraction via focal adhesion kinase- and Rho-mediated signaling pathways. Mol Biol Cell 2002; 13: 3601-13.
31. Oz B, Karayel FA, Gazio NL, Ozlen F, Balci K. The distribution of extracellular matrix proteins and CD44S expression in human astrocytomas. Pathol Oncol Res 2000; 6: 118-24.
32. Behrem S, Zarkovic K, Eskinja N, Jonjic N. Distribution pattern of tenascin-C in glioblastoma: Correlation with angiogenesis and tumor cell proliferation. Pathol Oncol Res 2005; 11: 229-35.
33. Huang W, Chiquet-Ehrismann R, Moyano JV, Garcia-Pardo A, Orend G. Interference of tenascin-C with syndecan-4 binding to fibronectin blocks cell adhesion and stimulates tumor cell proliferation. Cancer Res 2001; 61: 8586-94.
34. Mahesparan R, Read TA, Lund-Johansen M, Skaftnesmo KO, Bjerkvig R, Engebraaten O. Expression of extracellular matrix components in a highly infiltrative in vivo glioma model. Acta Neuropathol 2003; 105: 49-57.
35. Zagzag D, Friedlander DR, Dosik J et al. Tenascin-C expression by angiogenic vessels in human astrocytomas and by human brain endothelial cells in vitro. Cancer Res 1996; 56: 182-9.
36. Zagzag D, Friedlander DR, Miller DC et al. Tenascin expression in astrocytomas correlates with angiogenesis. Cancer Res 1995; 55: 907-14.
37. 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: 362-9.
38. Giuffrida A, Scarpa S, Birarelli P, Modesti A. The interaction of tenascin-C with fibronectin modulates the migration and specific metalloprotease activity in human mesothelioma cell lines of different histotype. Int J Oncol 2004; 25: 745-50.
39. Wenk MB, Midwood KS, Schwarzbauer JE, Tenascin C suppresses Rho activation. J Cell Biol 2000; 150: 913-20.
40. Midwood KS, Valenick LV, Hsia HC, Schwarzbauer JE. Coregulation of fibronectin signaling and matrix contraction by tenascin-C and syndecan-4. Mol Biol Cell 2004; 15: 5670-7.
41. Chintala SK, Sawaya R, Gokaslan ZL, Fuller G, Rao JS. Immunohistochemical localization of extracellular matrix proteins in human glioma, both in vivo and in vitro. Cancer Lett 1996; 101: 107-14.
42. Kochi N, Tani E, Morimura T, Itagaki T. Immunohistochemical study of fibronectin in human glioma and meningioma. Acta Neuropathol 1983; 59: 119-26.
43. Erickson HP, Bourdon MA. Tenascin: An extracellular matrix protein prominent in specialized embryonic tissues and tumors. Annu Rev Cell Biol 1989; 5: 71-92.
44. Brunner A, Mayerl C, Tzankov A et al. Prognostic significance of tenascin-C expression in superficial and invasive bladder cancer. J Clin Pathol 2004; 57: 927-31.
45. Dandachi N, Hauser-Kronberger C, More E et al. Co-expression of tenascin-C and vimentin in human breast cancer cells indicates phenotypic transdifferentiation during tumour progression: Correlation with histopathological parameters, hormone receptors, and oncoproteins. J Pathol 2001; 193: 181-9.
46. Gulubova MV, Vlaykova TI. Significance of tenascin-C, fibronectin, laminin, collagen IV, alpha5beta1 and alpha9beta1 integrins and fibrotic capsule formation around liver metastases originating from cancers of the digestive tract. Neoplasma 2006; 53: 372-83.
47. Ilmonen S, Jahkola T, Turunen JP, Muhonen T, Asko-Seljavaara S. Tenascin-C in primary malignant melanoma of the skin. Histopathology 2004; 45: 405-11.
48. 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: 2430-9.
49. Salmenkivi K, Haglund C, Arola J, Heikkila P. Increased expression of tenascin in pheochromocytomas correlates with malignancy. Am J Surg Pathol 2001; 25: 1419-23.
50. Ishihara A, Yoshida T, Tamaki H, Sakakura T. Tenascin expression in cancer cells and stroma of human breast cancer and its prognostic significance. Clin Cancer Res 1995; 1: 1035-41.