Integrins mediate adhesion of medulloblastoma cells to tenascin and activate pathways associated with survival and proliferation

Laboratory Investigation

Volumn 88, Issue 11, 2008, Pages 1143-1156

  Fiorilli, Paul ^a   Partridge, Darren ^b   Staniszewska, Izabela ^a   Wang, Jin Y ^a   Grabacka, Maja ^a,c   So, Kelvin ^b   Marcinkiewicz, Cezary ^a   Reiss, Krzysztof ^a   Khalili, Kamel ^a   Croul, Sidney E ^a,b,d  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

Extracellular matrix; Integrins; Medulloblastoma; Metastasis

Indexed keywords

ALPHA9 INTEGRIN; BETA1 INTEGRIN; FIBRONECTIN; INTEGRIN; LAMININ; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN SUBUNIT; TENASCIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MEDULLOBLASTOMA; MENINX; PRIORITY JOURNAL; PROTEIN FUNCTION;

CELL ADHESION; CELL LINE, TUMOR; CYTOSKELETAL PROTEINS; EXTRACELLULAR MATRIX; HUMANS; INTEGRINS; MEDULLOBLASTOMA; MENINGEAL NEOPLASMS; NEOPLASM METASTASIS; TENASCIN;

EID: 54949119476     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2008.89     Document Type: Article

References (62)

1. MacDonald TJ, Rood BR, Santi MR, et al. Advances in the diagnosis, molecular genetics, and treatment of pediatric embryonal CNS tumors. Oncologist 2003;8:174-186.
2. Zeltzer PM, Boyett JM, Finlay JL, et al. Metastasis stage, adjuvant treatment, and residual tumor are prognostic factors for medulloblastoma in children: conclusions from the Children's Cancer Group 921 randomized phase III study. J Clin Oncol 1999;17:832-845.
3. Reardon DA, Rich JN, Friedman HS, et al. Recent advances in the treatment of malignant astrocytoma. J Clin Oncol 2006;24:1253-1265.
4. Mareel M, Leroy A, Bracke M. Cellular and molecular mechanisms of metastasis as applied to carcinomatous meningitis. J Neurooncol 1998;38:97-102.
5. Grotzer MA, Hogarty MD, Janss AJ, et al. MYC messenger RNA expression predicts survival outcome in childhood primitive neuroectodermal tumor/medulloblastoma. Clin Cancer Res 2001;7:2425-2433.
6. MacDonald TJ, Brown KM, LaFleur B, et al. Expression profiling of medulloblastoma: PDGFRA and the RAS/MAPK pathway as therapeutic targets for metastatic disease. Nat Genet 2001;29:143-152. Erratum, Nat Genet. 2003 Nov35(3):287.
7. Pomeroy SL, Tamayo P, Gaasenbeek M, et al. Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 2002;415:436-442.
8. Hernan R, Fasheh R, Calabrese C, et al. ERBB2 up-regulates S100A4 and several other prometastatic genes in medulloblastoma. Cancer Res 2003;63:140-148.
9. Rutka JT, Giblin J, Dougherty DV, et al. An ultrastructural and immunocytochemical analysis of leptomeningeal and meningioma cultures. J Neuropathol Exp Neurol 1986;45:285-303.
10. Rutka JT, Kleppe-Hoifodt H, Emma DA, et al. Characterization of normal human brain cultures. Evidence for the outgrowth of leptomeningeal cells. Lab Invest 1986;55:71-85.
11. Rutka JT, Myatt CA, Giblin JR, et al. Distribution of extracellular matrix proteins in primary human brain tumours: an immunohistochemical analysis. Can J Neurol Sci 1987;14:25-30.
12. Rutka JT, Giblin JR, Apodaca G, et al. Inhibition of growth and induction of differentiation in a malignant human glioma cell line by normal leptomeningeal extracellular matrix proteins. Cancer Res 1987;47:3515-3522.
13. Rutka JT, Dougherty DV, Giblin JR, et al. Growth of a medulloblastoma on normal leptomeningeal cells in culture: interaction of tumor cells and normal cells. Neurosurgery 1987;21:872-878.
14. Rutka JT, Apodaca G, Stern R, et al. The extracellular matrix of the central and peripheral nervous systems: structure and function. J Neurosurg 1988;69:155-170.
15. Wikstrand CJ, Friedman HS, Bigner DD. Medulloblastoma cell-substrate interaction in vitro. Invasion Metastasis 1991;11:310-324.
16. Rougon G, Hobert O. New insights into the diversity and function of neuronal immunoglobulin superfamily molecules. Annu Rev Neurosci 2003;26:207-238.
17. Yamagata M, Sanes JR, Weiner JA. Synaptic adhesion molecules. Curr Opin Cell Biol 2003;15:621-632.
18. Utsuki S, Oka H, Sato Y, et al. E, N-cadherins and beta-catenin expression in medulloblastoma and atypical. Neurol Med Chir (Tokyo) 2004;44:402-406.
19. Longee DC, Wikstrand CJ, Mansson JE, et al. Disialoganglioside GD2 in human neuroectodermal tumor cell lines and gliomas. Acta Neuropathol (Berl) 1991;82:45-54.
20. Molenaar WM, de Leij L, Trojanowski JQ. Neuroectodermal tumors of the peripheral and the central nervous system share neuroendocrine N-CAM-related antigens with small cell lung carcinomas. Acta Neuropathol (Berl) 1991;83:46-54.
21. Son EI, Kim IM, Kim DW, et al. Immunohistochemical analysis for histopathological subtypes in pediatric medulloblastomas. Pathol Int 2003;53:67-73.
22. Figarella-Branger DF, Durbec PL, Rougon GN. Differential spectrum of expression of neural cell adhesion molecule isoforms and L1 adhesion molecules on human neuroectodermal tumors. Cancer Res 1990;50:6364-6370.
23. Patel K, Frost G, Kiely F, et al. Expression of the cluster 1 antigen (neural cell adhesion molecule) in neuroectodermal tumours. Br J Cancer Suppl 1991;14:20-23.
24. Hirsch S, Bahr M. Immunocytochemical characterization of reactive optic nerve astrocytes and meningeal cells. Glia 1999;26:36-46.
25. Kroger S, Niehorster L. Isolation, characterization, and substrate properties of the external limiting membrane from the avian embryonic optic tectum. J Neurosci Res 1990;27:169-183.
26. Stewart GR, Pearlman AL. Fibronectin-like immunoreactivity in the developing cerebral cortex. J Neurosci 1987;7:3325-3333.
27. Morrison JC, Jerdan JA, L0Hernault NL, et al. The extracellular matrix composition of the monkey optic nerve head. Invest Ophthalmol Vis Sci 1988;29:1141-1150.
28. McComb RD, Moul JM, Bigner DD. Distribution of type VI collagen in human gliomas: comparison with fibronectin and gliomamesenchymal matrix glycoprotein. J Neuropathol Exp Neurol 1987;46:623-633.
29. Ajemian A, Ness R, David S. Tenascin in the injured rat optic nerve and in non-neuronal cells in vitro: potential role in neural repair. J Comp Neurol 1994;340:233-242.
30. Kappler J, Stichel CC, Gleichmann M, et al. Developmental regulation of decorin expression in postnatal rat brain. Brain Res 1998;793:328-332.
31. Seiffert D, Iruela-Arispe ML, Sage EH, et al. Distribution of vitronectin mRNA during murine development. Dev Dyn 1995;203:71-79.
32. Iruela-Arispe ML, Liska DJ, Sage EH, et al. Differential expression of thrombospondin 1, 2, and 3 during murine development. Dev Dyn 1993;197:40-56.
33. Barth TF, Bruderlein S, Rinaldi N, et al. Pleural mesothelioma mimics the integrin profile of activated, sessile rather than detached mesothelial cells. Int J Cancer 1997;72:77-86.
34. Casey RC, Burleson KM, Skubitz KM, et al. Beta 1-integrins regulate the formation and adhesion of ovarian carcinoma multicellularspheroids. Am J Pathol 2001;159:2071-2080.
35. Klominek J, Sumitran Karuppan S, Hauzenberger D. Differential motile response of human malignant mesothelioma cells to fibronectin, laminin and collagen type IV: the role of beta1 integrins. Int J Cancer 1997;72:1034-1044.
36. Lessan K, Aguiar DJ, Oegema T, et al. CD44 and beta1 integrin mediate ovarian carcinoma cell adhesion to peritoneal mesothelial cells. Am J Pathol 1999;154:1525-1537.
37. Hehlgans S, Haase M, Cordes N. Signalling via integrins: implications for cell survival and anticancer strategies. Biochim Biophys Acta 2007;1775:163-180.
38. Hannigan G, Troussard AA, Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer 2005;5:51-63.
39. Cordes N, Seidler J, Durzok R, et al. Beta1-integrin-mediated signaling essentially contributes to cell survival after radiation-induced genotoxic injury. Oncogene 2006;25:1378-1390.
40. Müller HL, Oh Y, Gargosky SE, et al. Concentrations of insulin-like growth factor (IGF)-binding protein-3 (IGFBP-3), IGF, and IGFBP-3 protease activity in cerebrospinal fluid of children with leukemia, central nervous system tumor, or meningitis. J Clin Endocrinol Metab 1993;77:1113-1119.
41. Weigel R, Schilling L, Schmiedek P. Specific pattern of growth factor distribution in chronic subdural hematoma (CSH): evidence for an angiogenic disease. Acta Neurochir (Wien) 2001;143:811-818.
42. Marcinkiewicz C, Taooka Y, Yokosaki Y, et al. Inhibitory effects of MLDG-containing heterodimeric disintegrins reveal distinct structural requirements for interaction of the integrin alpha 9beta 1 with VCAM-1, tenascin-C, and osteopontin. J Biol Chem 2000;275:31930-31937.
43. Bazan-Socha S, Kisiel DG, Young B, et al. Structural requirements of MLD-containing disintegrins for functional interaction with α4β1 ανδ α9β1 integrins. Biochemistry 2004;43:1639-1647.
44. Cormack DH (ed). Ham's Histology ed 9, 9 Lippincott: Philadelphia, PA, 1987, pp 366-367.
45. Peters A, Palay SL, Webster H deF (ed). The Fine Structure of the Nervous System. WB Saunders: Philadelphia, 1976, pp 332-343.
46. Jones PA. Construction of an artificial blood vessel wall from cultured endothelial and smooth muscle cells. Proc Natl Acad Sci USA 1979;76:1882-1886.
47. Marcinkiewicz C, Rosenthal LA, Mosser DM, et al. Immunological characterization of eristostatin and echistatin binding sites on alpha IIb beta 3 and alpha V beta 3 integrins. Biochem J 1996;317(Part 3):817-825.
48. Franciosi S, De Gasperi R, Dickstein DL, et al. Pepsin pretreatment allows collagen IV immunostaining of blood vessels in adult mouse brain. J Neurosci Methods 2007;163:76-82.
49. Krum JM, More NS, Rosenstein JM. Brain angiogenesis: variations in vascular basement membrane glycoprotein immunoreactivity. Exp Neurol 1991;111:152-165.
50. Robinson Jr JR, Awad IA, Zhou P, et al. Expression of basement membrane and endothelial cell adhesion molecules in vascular malformations of the brain: preliminary observations and working hypothesis. Neurol Res 1995;17:49-58.
51. Nag S, Venugopalan R, Stewart DJ. Increased caveolin-1 expression precedes decreased expression of occludin and claudin-5 during blood-brain barrier breakdown. Acta Neuropathol 2007;114:459-469.
52. Sobel RA, Mitchell ME. Fibronectin in multiple sclerosis lesions. Am J Pathol 1989;135:161-168.
53. Papierz W, Alwasiak J, Kolasa P, et al. Primitive neuroectodermal tumors: ultrastructural and immunohistochemical studies. Ultrastruct Pathol 1995;19:147-166.
54. Gutowski NJ, Newcombe J, Cuzner ML. Tenascin-R and C in multiple sclerosis lesions: relevance to extracellular matrix remodelling. Neuropathol Appl Neurobiol 1999;25:207-214.
55. Campbell S, Otis M, Côté M, et al. Connection between integrins and cell activation in rat adrenal glomerulosa cells: a role for Arg-Gly-Asp peptide in the activation of the p42/p44(mapk) pathway and intracellular calcium. Endocrinology 2003;144:1486-1495.
56. Fornaro M, Steger CA, Bennett AM, et al. Differential role of beta(1C) and beta(1A) integrin cytoplasmic variants in modulating focal adhesion kinase, protein kinase B/AKT, and Ras/Mitogen-activated protein kinase pathways. Mol Biol Cell 2000;11:2235-2249.
57. Aplin A, Stewart S, Assoian R, et al. Integrin-mediated Adhesion Regulates ERK Nuclear Translocation and Phosphorylation of Elk-1. J Cell Biol 2001;153:273-281.
58. Roovers K, Assoian RK. Integrating the MAP kinase signal into the G1 phase cell cycle machinery. Bioessays 2000;22:818-826.
59. Palmer EL, Ruegg C, Ferrando R, et al. Sequence and tissue distribution of the integrin alpha 9 subunit, a novel partner of beta 1 that is widely distributed in epithelia and muscle. J Cell Biol 1993;123:1289-1297.
60. Hyduk SJ, Cybulsky MI. Alpha 4 integrin signaling activates phosphatidylinositol 3-kinase and stimulates T cell adhesion to intercellular adhesion molecule-1 to a similar extent as CD3, but induces a distinct rearrangement of the actin cytoskeleton. J Immunol 2002;168:696-704.
61. Ohta K, Inokuchi T, Hayashida Y, et al. Regional diminution of von Willebrand factor expression on the endothelial covering arachnoid granulations of human, monkey and dog brain. Kurume Med J 2002;49:177-183.
62. Brandsma D, Reijneveld JC, Taphoorn MJ, et al. Vascular cell adhesion molecule-1 is a key adhesion molecule in melanoma cell adhesion to the leptomeninges. Lab Invest 2002;82:1493-1502.