Home LiteratureArticle Details
PMID: 19262113 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Role of hyaluronan in glioma invasion.

Cell adhesion & migration ·Vol. 2 ·No. 3 ·2008-00-00 ·Pages 202-7

Park JB, Kwak HJ, Lee SH

Abstract

Gliomas are the most common primary intracranial tumors. Their distinct ability to infiltrate into the extracellular matrix (ECM) of the brain makes it impossible to treat these tumors using surgery and radiation therapy. A number of different studies have suggested that hyaluronan (HA), the principal glycosaminoglycan (GAG) in the ECM of the brain, is the critical factor for glioma invasion. HA-induced glioma invasion was driven by two important molecular events: matrix metalloproteinase (MMP) secretion and up-regulation of cell migration. MMP secretion was triggered by HA-induced focal adhesion kinase (FAK) activation, which transmits its signal through ERK activation and nuclear factor kappa B (NF-kappaB) translocation. Another important molecular event is osteopontin (OPN) expression. OPN expression by AKT activation triggers cell migration. These results suggest that HA-induced glioma invasion is tightly regulated by signaling mechanisms, and a detailed understanding of this molecular mechanism will provide important clues for glioma treatment.

MeSH Terms
Animals Biomarkers, Tumor Cell Movement Glioma/metabolism,pathology Humans Hyaluronic Acid/chemistry,metabolism Neoplasm Invasiveness Prognosis
Chemicals
Biomarkers, Tumor Hyaluronic Acid
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Park Jong Bae
Research Institute and Hospital, National Cancer Center, Goyang Gyeonggi, Korea.
Kwak Hee-Jin
Lee Seung-Hoon
References (91)
91 references, click to expand
  1. Which glioblastoma multiforme patient will become a long-term survivor? A population-based study.
    Ann Neurol. 1999 Aug;46(2):183-8 PMID: 10443883
  2. A role for focal adhesion kinase signaling in tumor necrosis factor-alpha-dependent matrix metalloproteinase-9 production in a cholangiocarcinoma cell line, CCKS1.
    Cancer Res. 2006 Jul 1;66(13):6778-84 PMID: 16818654
  3. Signaling properties of hyaluronan receptors.
    J Biol Chem. 2002 Feb 15;277(7):4589-92 PMID: 11717317
  4. Elevated tissue expression of hyaluronic acid and hyaluronidase validates the HA-HAase urine test for bladder cancer.
    J Urol. 2001 Jun;165(6 Pt 1):2068-74 PMID: 11371930
  5. Focal adhesion kinase overexpression enhances ras-dependent integrin signaling to ERK2/mitogen-activated protein kinase through interactions with and activation of c-Src.
    J Biol Chem. 1997 May 16;272(20):13189-95 PMID: 9148935
  6. A biochemical characterization of the binding of osteopontin to integrins alpha v beta 1 and alpha v beta 5.
    J Biol Chem. 1995 Nov 3;270(44):26232-8 PMID: 7592829
  7. CD44 exhibits a cell type dependent interaction with triton X-100 insoluble, lipid rich, plasma membrane domains.
    J Cell Sci. 1995 Sep;108 ( Pt 9):3127-35 PMID: 8537452
  8. Hyaluronan.
    FASEB J. 1992 Apr;6(7):2397-404 PMID: 1563592
  9. The role of the CD44 transmembrane and cytoplasmic domains in co-ordinating adhesive and signalling events.
    J Cell Sci. 2004 Jan 26;117(Pt 3):373-80 PMID: 14702383
  10. Genetic deletion of the Pten tumor suppressor gene promotes cell motility by activation of Rac1 and Cdc42 GTPases.
    Curr Biol. 2000 Apr 6;10(7):401-4 PMID: 10753747
  11. HYAL1 hyaluronidase in prostate cancer: a tumor promoter and suppressor.
    Cancer Res. 2005 Sep 1;65(17):7782-9 PMID: 16140946
  12. Control of enzymatic degradation of hyaluronan by divalent cations.
    Carbohydr Res. 1999 May 31;318(1-4):26-37 PMID: 10515049
  13. Hyaluronan promotes the malignant phenotype.
    Glycobiology. 2002 Mar;12(3):37R-42R PMID: 11971857
  14. pp60(c-src) is required for cell locomotion regulated by the hyaluronanreceptor RHAMM.
    Oncogene. 1996 Nov 21;13(10):2213-24 PMID: 8950989
  15. CD44 interaction with c-Src kinase promotes cortactin-mediated cytoskeleton function and hyaluronic acid-dependent ovarian tumor cell migration.
    J Biol Chem. 2001 Mar 9;276(10):7327-36 PMID: 11084024
  16. Tumor cell-associated hyaluronan as an unfavorable prognostic factor in colorectal cancer.
    Cancer Res. 1998 Jan 15;58(2):342-7 PMID: 9443415
  17. Potential impact of a single nucleotide polymorphism in the hyaluronan synthase 1 gene in Waldenstrom's macroglobulinemia.
    Clin Lymphoma. 2005 Mar;5(4):253-6 PMID: 15794859
  18. Expression of focal adhesion kinase in acute myeloid leukemia is associated with enhanced blast migration, increased cellularity, and poor prognosis.
    Cancer Res. 2004 May 1;64(9):3191-7 PMID: 15126359
  19. Stabilin-1 and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues.
    Biochem J. 2002 Feb 15;362(Pt 1):155-64 PMID: 11829752
  20. Hyaluronan: a multifunctional, megaDalton, stealth molecule.
    Curr Opin Cell Biol. 2000 Oct;12(5):581-6 PMID: 10978893
  21. Evaluation of the prognostic potential of hyaluronic acid and hyaluronidase (HYAL1) for prostate cancer.
    Cancer Res. 2003 May 15;63(10):2638-44 PMID: 12750291
  22. Hyaluronan and CD44: strategic players for cell-matrix interactions during chondrogenesis and matrix assembly.
    Birth Defects Res C Embryo Today. 2003 May;69(2):174-96 PMID: 12955860
  23. Aspects of the biology of hyaluronan, a largely neglected but extremely versatile molecule.
    Wien Med Wochenschr. 2006 Nov;156(21-22):563-8 PMID: 17160372
  24. Biological properties of hyaluronan in aqueous solution are controlled and sequestered by reversible tertiary structures, defined by NMR spectroscopy.
    Biomacromolecules. 2002 May-Jun;3(3):547-53 PMID: 12005527
  25. Tumoral invasion in the central nervous system.
    J Neurooncol. 1994;18(2):111-21 PMID: 7964974
  26. A side by side comparison of cytology and biomarkers for bladder cancer detection.
    J Urol. 2004 Sep;172(3):1123-6 PMID: 15311054
  27. Inhibitory effect of emodin on tumor invasion through suppression of activator protein-1 and nuclear factor-kappaB.
    Biochem Pharmacol. 2004 Jul 15;68(2):361-71 PMID: 15194008
  28. Inhibition of prostate tumor cell hyaluronan synthesis impairs subcutaneous growth and vascularization in immunocompromised mice.
    Am J Pathol. 2002 Sep;161(3):849-57 PMID: 12213713
  29. Clinical uses of hyaluronan.
    Ciba Found Symp. 1989;143:265-75; discussion 275-80, 281-5 PMID: 2680347
  30. Transcriptional regulation of osteopontin and the metastatic phenotype: evidence for a Ras-activated enhancer in the human OPN promoter.
    Clin Exp Metastasis. 2003;20(1):77-84 PMID: 12650610
  31. Hyaluronan: from extracellular glue to pericellular cue.
    Nat Rev Cancer. 2004 Jul;4(7):528-39 PMID: 15229478
  32. Hyaluronan and morphogenesis.
    Birth Defects Res C Embryo Today. 2004 Mar;72(1):89-108 PMID: 15054906
  33. The glycosyl-phosphatidylinositol anchor of membrane proteins.
    Biochim Biophys Acta. 1989 Dec 6;988(3):427-54 PMID: 2531614
  34. Landscaping the cancer terrain.
    Science. 1998 May 15;280(5366):1036-7 PMID: 9616081
  35. Expression of osteopontin in human glioma. Its correlation with the malignancy.
    Lab Invest. 1995 Jan;72(1):55-63 PMID: 7837791
  36. Serum hyaluronan is increased in malignant lymphoma.
    Am J Hematol. 1995 Dec;50(4):231-3 PMID: 7485095
  37. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons.
    J Cell Biol. 1994 Jul;126(2):391-401 PMID: 7518464
  38. Vasorelaxants from Chinese herbs, emodin and scoparone, possess immunosuppressive properties.
    Eur J Pharmacol. 1991 Jun 6;198(2-3):211-3 PMID: 1830846
  39. The hyaluronan receptor RHAMM regulates extracellular-regulated kinase.
    J Biol Chem. 1998 May 1;273(18):11342-8 PMID: 9556628
  40. Expression of syndecans, a heparan sulfate proteoglycan, in malignant gliomas: participation of nuclear factor-kappaB in upregulation of syndecan-1 expression.
    J Neurooncol. 2006 Mar;77(1):25-32 PMID: 16132527
  41. Hyaluronate receptors mediating glioma cell migration and proliferation.
    J Neurooncol. 2001 Jun;53(2):115-27 PMID: 11716065
  42. Hyaluronan-binding proteins: tying up the giant.
    J Biol Chem. 2002 Feb 15;277(7):4585-8 PMID: 11717315
  43. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties.
    J Biol Chem. 1999 Aug 27;274(35):25085-92 PMID: 10455188
  44. Signaling through CD44 is mediated by tyrosine kinases. Association with p56lck in T lymphocytes.
    J Biol Chem. 1996 Feb 2;271(5):2863-7 PMID: 8576267
  45. CD44-mediated uptake and degradation of hyaluronan.
    Matrix Biol. 2002 Jan;21(1):15-23 PMID: 11827788
  46. Dual regulation of IL-1 beta-mediated matrix metalloproteinase-9 expression in mesangial cells by NF-kappa B and AP-1.
    Am J Physiol. 1996 Jan;270(1 Pt 2):F123-30 PMID: 8769830
  47. PTEN suppresses hyaluronic acid-induced matrix metalloproteinase-9 expression in U87MG glioblastoma cells through focal adhesion kinase dephosphorylation.
    Cancer Res. 2002 Nov 1;62(21):6318-22 PMID: 12414663
  48. Transmembrane domain of CD44 is required for its detergent insolubility in fibroblasts.
    J Cell Sci. 1995 Mar;108 ( Pt 3):1033-41 PMID: 7542666
  49. Importance of hyaluronan biosynthesis and degradation in cell differentiation and tumor formation.
    Braz J Med Biol Res. 2003 Aug;36(8):967-73 PMID: 12886450
  50. HYAL1 hyaluronidase: a molecular determinant of bladder tumor growth and invasion.
    Cancer Res. 2005 Mar 15;65(6):2243-50 PMID: 15781637
  51. Glioma invasion in the central nervous system.
    Neurosurgery. 1996 Aug;39(2):235-50; discussion 250-2 PMID: 8832660
  52. Sera of children with renal tumours contain low-molecular-mass hyaluronic acid.
    Int J Cancer. 1989 Sep 15;44(3):445-8 PMID: 2550372
  53. Activate NF-kappa B or die?
    Curr Biol. 1997 Feb 1;7(2):R94-6 PMID: 9081673
  54. Expression of hyaluronan in human tumor progression.
    J Carcinog. 2006 Jan 10;5:2 PMID: 16401353
  55. Long-term survivors of glioblastoma: statistical aberration or important unrecognized molecular subtype?
    Cancer J. 2003 May-Jun;9(3):214-21 PMID: 12952306
  56. ECM dependent and integrin mediated tumor cell migration of human glioma and melanoma cell lines under serum-free conditions.
    Anticancer Res. 1996 Nov-Dec;16(6B):3679-87 PMID: 9042241
  57. Ankyrin-binding domain of CD44(GP85) is required for the expression of hyaluronic acid-mediated adhesion function.
    J Cell Biol. 1994 Aug;126(4):1099-109 PMID: 7519619
  58. Glioma invasion in vitro is mediated by CD44-hyaluronan interactions.
    J Pathol. 1997 Apr;181(4):434-8 PMID: 9196442
  59. CD44 is the principal cell surface receptor for hyaluronate.
    Cell. 1990 Jun 29;61(7):1303-13 PMID: 1694723
  60. Targeting hyaluronan interactions in malignant gliomas and their drug-resistant multipotent progenitors.
    Clin Cancer Res. 2008 Mar 15;14(6):1804-13 PMID: 18347183
  61. Rho-kinase (ROK) promotes CD44v(3,8-10)-ankyrin interaction and tumor cell migration in metastatic breast cancer cells.
    Cell Motil Cytoskeleton. 1999;43(4):269-87 PMID: 10423269
  62. Hyaluronan synthase 3 overexpression promotes the growth of TSU prostate cancer cells.
    Cancer Res. 2001 Jul 1;61(13):5207-14 PMID: 11431361
  63. Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease.
    J Cell Biol. 1994 Jul;126(1):111-26 PMID: 7517942
  64. High stromal hyaluronan level is associated with poor differentiation and metastasis in prostate cancer.
    Eur J Cancer. 2001 May;37(7):849-56 PMID: 11313172
  65. Serum hyaluronan as a disease marker.
    Ann Med. 1996 Jun;28(3):241-53 PMID: 8811168
  66. Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival.
    Am J Pathol. 2000 Feb;156(2):529-36 PMID: 10666382
  67. CD44: from adhesion molecules to signalling regulators.
    Nat Rev Mol Cell Biol. 2003 Jan;4(1):33-45 PMID: 12511867
  68. Immunohistochemical analyses of focal adhesion kinase expression in benign and malignant human breast and colon tissues: correlation with preinvasive and invasive phenotypes.
    Clin Cancer Res. 2000 Jun;6(6):2417-23 PMID: 10873094
  69. Hyaluronan and hyaluronectin in the extracellular matrix of human brain tumour stroma.
    Eur J Cancer. 1993;29A(7):1012-7 PMID: 7684596
  70. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses.
    Annu Rev Immunol. 1998;16:225-60 PMID: 9597130
  71. CD44v(3,8-10) is involved in cytoskeleton-mediated tumor cell migration and matrix metalloproteinase (MMP-9) association in metastatic breast cancer cells.
    J Cell Physiol. 1998 Jul;176(1):206-15 PMID: 9618160
  72. Mechanisms of glioma invasion: role of matrix-metalloproteinases.
    Can J Neurol Sci. 1997 Feb;24(1):3-15 PMID: 9043741
  73. Novel type of potential anticancer agents derived from chrysophanol and emodin. Some structure-activity relationship studies.
    J Med Chem. 1988 Feb;31(2):283-4 PMID: 3339601
  74. Hyaluronan in serum as an indicator of progressive disease in hyaluronan-producing malignant mesothelioma.
    Cancer. 1999 Nov 15;86(10):2000-5 PMID: 10570424
  75. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN.
    Science. 1998 Jun 5;280(5369):1614-7 PMID: 9616126
  76. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation.
    FASEB J. 2006 Jan;20(1):9-22 PMID: 16394262
  77. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
  78. Bladder tumor markers for monitoring recurrence and screening comparison of hyaluronic acid-hyaluronidase and BTA-Stat tests.
    Cancer. 2002 Jul 1;95(1):61-72 PMID: 12115318
  79. EGF receptor modifies cellular responses to hyaluronan in glioblastoma cell lines.
    J Clin Neurosci. 2002 May;9(3):282-8 PMID: 12093135
  80. CD44 splice variants: metastases meet lymphocytes.
    Immunol Today. 1993 Aug;14(8):395-9 PMID: 7691067
  81. Subcellular distribution, calmodulin interaction, and mitochondrial association of the hyaluronan-binding protein RHAMM in rat brain.
    J Neurosci Res. 2001 Jul 1;65(1):6-16 PMID: 11433424
  82. Expression of hyaluronan receptors CD44 and RHAMM in stomach cancers: relevance with tumor progression.
    Int J Oncol. 2000 Nov;17(5):927-32 PMID: 11029494
  83. High levels of stromal hyaluronan predict poor disease outcome in epithelial ovarian cancer.
    Cancer Res. 2000 Jan 1;60(1):150-5 PMID: 10646867
  84. Prognostic value of hyaluronan expression in non-small-cell lung cancer: Increased stromal expression indicates unfavorable outcome in patients with adenocarcinoma.
    Int J Cancer. 2001 Jan 20;95(1):12-7 PMID: 11241304
  85. Hyaluronic acid induces osteopontin via the phosphatidylinositol 3-kinase/Akt pathway to enhance the motility of human glioma cells.
    Cancer Res. 2005 Feb 1;65(3):686-91 PMID: 15705860
  86. The extracellular matrix of the central and peripheral nervous systems: structure and function.
    J Neurosurg. 1988 Aug;69(2):155-70 PMID: 3292716
  87. Emodin suppresses hyaluronic acid-induced MMP-9 secretion and invasion of glioma cells.
    Int J Oncol. 2005 Sep;27(3):839-46 PMID: 16077936
  88. Hyaluronan and hyaluronan synthases: potential therapeutic targets in cancer.
    Curr Drug Targets Cardiovasc Haematol Disord. 2005 Feb;5(1):3-14 PMID: 15720220
  89. A lymphocyte molecule implicated in lymph node homing is a member of the cartilage link protein family.
    Cell. 1989 Mar 24;56(6):1057-62 PMID: 2466575
  90. CD44 mediates human glioma cell adhesion and invasion in vitro.
    Cancer Res. 1994 Aug 1;54(15):3988-92 PMID: 7518347
  91. Characterisation of the murine gene encoding the intracellular hyaluronan receptor IHABP (RHAMM).
    Gene. 1999 Jan 8;226(1):41-50 PMID: 9889313
Article Info
Journal
Cell adhesion & migration
Abbr.
Cell Adh Migr
ISSN
1933-6926
DOI
10.4161/cam.2.3.6320
Published
2008-00-00
Epub
2008-00-21
Pages
202-7
Language
English
Region
United States
NLM ID
101469464
PMCID
PMC2634087
Subset
IM
External Links
PubMed source DOI: 10.4161/cam.2.3.6320 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2