|
Sign In to gain access to subscriptions and/or personal tools.
|
Hyaluronan Regulates Ceruloplasmin Production By Gliomas and Their Treatment-Resistant Multipotent Progenitors
Sandra L. Tye, MS
Department of Pediatrics, Charles P. Darby Children's Research Institute, College of Medicine, Medical University of South Carolina, South Carolina
Anne G. Gilg, PhD
Department of Pediatrics, Charles P. Darby Children's Research Institute, College of Medicine, Medical University of South Carolina, South Carolina
Lauren B. Tolliver, MS
Department of Pediatrics, Charles P. Darby Children's Research Institute, College of Medicine, Medical University of South Carolina, South Carolina
William G. Wheeler, BS
Department of Pediatrics, Charles P. Darby Children's Research Institute, College of Medicine, Medical University of South Carolina, South Carolina
Bryan P. Toole, PhD
Department of Cell Biology and Anatomy Charles P. Darby Children's Research Institute, College of Medicine, Medical University of South Carolina, South Carolina
Bernard L. Maria, MD MBA
Department of Pediatrics, Charles P. Darby Children's Research Institute, College of Medicine, Medical University of South Carolina, South Carolina, mariabl{at}musc.edu
Ceruloplasmin (glycosylphosphatidylinositol-linked ferroxidase associated with normal astrocytes) can also be secreted by glioma cells, where its function is unknown. Ceruloplasmin is not only present in glioma cells and in human glioma specimens but also is enriched in highly malignant glioma stem-like cells. Hyaluronan is a large extracellular glycosaminoglycan that enhances malignant glioma behaviors by interacting with CD44 receptors and by downstream activation of signaling proteins and transporters associated with malignancy. We examined the relationship between hyaluronan and ceruloplasmin expression in glioma stem-like cells. Antagonism of hyaluronan interactions with short-fragment hyaluronan oligomers decreased ceruloplasmin expression in parental and stem-like glioma cells in vivo and in cell culture, implying that hyaluronan regulates ceruloplasmin expression. Further gain and loss-of-function studies are needed to fully define the relationship between hyaluronan and ceruloplasmin, and ceruloplasmin's effect on malignant behaviors.
Key Words: ceruloplasmin hyaluronan glioma stem-like cells glycosaminoglycan
References
- Fortna RR, Watson HA, Nyquist SE Glycosyl phosphatidylinositol-anchored ceruloplasmin is expressed by rat Sertoli cells and is concentrated in detergent-insoluble membrane fractions Biol Reprod. 1999;61:1042-1049.[Abstract/Free Full Text]
- Klomp LW, Gitlin JD Expression of the ceruloplasmin gene in the human retina and brain: implications for a pathogenic model in aceruloplasminemia. Hum Mol Genet. 1996;5:1989-1996.[Abstract/Free Full Text]
- Patel BN, David S. A novel glycosylphosphatidylinositol-anchored form of ceruloplasmin is expressed by mammalian astrocytes. J Biol Chem. 1997;272:20185-20190.[Abstract/Free Full Text]
- Patel BN, Dunn RJ, David S. Alternative RNA splicing generates a glycosylphosphatidylinositol-anchored form of ceruloplasmin in mammalian brain. J Biol Chem. 2000;275:4305-4310.[Abstract/Free Full Text]
- Salzer JL, Lovejoy L., Linder MC, et al. Ran-2, a glial lineage marker, is a GPI-anchored form of ceruloplasmin. J Neurosci Res. 1998;54:147-157.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Park YS, Suzuki K., Taniguchi N., et al. Glutathione peroxidase-like activity of caeruloplasmin as an important lung antioxidant. FEBS Lett. 1999;458:133-136.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Hellman NE, Gitlin JD Ceruloplasmin metabolism and function. Annu Rev Nutr. 2002;22:439-458.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Messerschmidt A., Rossi A., Ladenstein R., et al. X-ray crystal structure of the blue oxidase ascorbate oxidase from zucchini. Analysis of the polypeptide fold and a model of the copper sites and ligands. J Mol Biol. 1989;206:513-529.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Osaki S., Johnson DA, Frieden E. The possible significance of the ferrous oxidase activity of ceruloplasmin in normal human serum. J Biol Chem. 1966;241:2746-2751.[Abstract/Free Full Text]
- Osaki S., Johnson DA, Frieden E. The mobilization of iron from the perfused mammalian liver by a serum copper enzyme, ferroxidase I. J Biol Chem. 1971;246:3018-3023.
- Bielli P., Calabrese L. Structure to function relationships in ceruloplasmin: a `moonlighting' protein. Cell Mol Life Sci. 2002;59:1413-1427.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Laurell CB, Kullander S., Thorell J. Effect of administration of a combined estrogen-progestin contraceptive on the level of individual plasma proteins. Scand J Clin Lab Invest. 1968;21:337-343.[Medline]
[Order article via Infotrieve]
- Hough CD, Cho KR, Zonderman AB, et al. Coordinately up-regulated genes in ovarian cancer. Cancer Res. 2001;61:3869-3876.[Abstract/Free Full Text]
- Kunapuli SP, Singh H., Singh P., et al. Ceruloplasmin gene expression in human cancer cells. Life Sci. 1987;40:2225-2228.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Stassar MJ, Devitt G., Brosius M., et al. Identification of human renal cell carcinoma associated genes by suppression subtractive hybridization. Br J Cancer. 2001;85:1372-1382.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Manjula S., Aroor AR, Raja A., et al. Elevation of serum ceruloplasmin levels in brain tumours. Acta Neurol Scand. 1992;86: 156-158.[Web of Science][Medline]
[Order article via Infotrieve]
- Conley L., Geurs TL, Levin LA Transcriptional regulation of ceruloplasmin by an IL-6 response element pathway. Brain Res Mol Brain Res. 2005;139:235-241.[Medline]
[Order article via Infotrieve]
- di Patti MC, Persichini T., Mazzone V., et al. Interleukin-1beta up-regulates iron efflux in rat C6 glioma cells through modulation of ceruloplasmin and ferroportin-1 synthesis. Neurosci Lett. 2004;363:182-186.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Knapp J., Olson L., Tye S., et al. Case of desmoplastic infantile ganglioglioma secreting ceruloplasmin. J Child Neurol. 2005;20:920-924.[Abstract/Free Full Text]
- Al-Hajj M., Clarke MF Self-renewal and solid tumor stem cells. Oncogene. 2004;23:7274-7282.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Caussinus E., Hirth F. Asymmetric stem cell division in development and cancer. Prog Mol Subcell Biol. 2007;45:205-225.[Medline]
[Order article via Infotrieve]
- Singh SK, Clarke ID, Terasaki M., et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821-5828.[Abstract/Free Full Text]
- Soltysova A., Altanerova V., Altaner C. Cancer stem cells. Neo-plasma. 2005;52:435-440.[Web of Science][Medline]
[Order article via Infotrieve]
- Turley EA, Noble PW, Bourguignon LY Signaling properties of hyaluronan receptors. J Biol Chem. 2002;277:4589-4592.[Free Full Text]
- Toole BP Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004;4:528-539.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Ranuncolo SM, Ladeda V., Specterman S., et al. CD44 expression in human gliomas. J Surg Oncol. 2002;79:30-35; discussion 35-36.[CrossRef][Web of Science]
- Bouvier-Labit C., Liprandi A., Monti G., et al. CD44H is expressed by cells of the oligodendrocyte lineage and by oligodendrogliomas in humans. J Neurooncol. 2002;60:127-134.[CrossRef][Medline]
[Order article via Infotrieve]
- Toole BP Hyaluronan in morphogenesis. Semin Cell Dev Biol. 2001;12:79-87.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Knudson W., Chow G., Knudson CB CD44-mediated uptake and degradation of hyaluronan. Matrix Biol. 2002;21:15-23.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Goodell MA, Brose K., Paradis G., et al. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 1996;183:1797-1806.[Abstract/Free Full Text]
- Kondo T., Setoguchi T., Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci U S A. 2004;101:781-786.[Abstract/Free Full Text]
- Galli R., Binda E., Orfanelli U., et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004;64:7011-7021.[Abstract/Free Full Text]
- Zeng C., Toole BP, Kinney SD, et al. Inhibition of tumor growth in vivo by hyaluronan oligomers. Int J Cancer. 1998;77:396-401.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Muir D., Johnson J., Rojiani M., et al. Assessment of lamininmediated glioma invasion in vitro and by glioma tumors engrafted within rat spinal cord. J Neurooncol. 1996;30:199-211.[Medline]
[Order article via Infotrieve]
- Gilg AG, Tye SL, Tolliver LB, et al. Targeting hyaluronan interactions in malignant gliomas and their drug-resistant multipotent progenitors Clin Cancer Res. 2008;14: 1804-1813.[Abstract/Free Full Text]
- Bao S., Wu Q., McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756-760.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Liu G., Yuan X., Zeng Z., et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 2006;5:67.[CrossRef][Medline]
[Order article via Infotrieve]
- Lo HW, Day CP, Hung MC Cancer-specific gene therapy. Adv Genet. 2005;54:235-255.[Medline]
[Order article via Infotrieve]
- Lee CM, Lo HW, Shao RP, et al. Selective activation of ceruloplasmin promoter in ovarian tumors: potential use for gene therapy. Cancer Res. 2004;64:1788-1793.[Abstract/Free Full Text]
- Kluger HM, Kluger Y., Gilmore-Hebert M., et al. cDNA microarray analysis of invasive and tumorigenic phenotypes in a breast cancer model. Lab Invest. 2004;84:320-331.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Kwok JC, Richardson DR The iron metabolism of neoplastic cells: alterations that facilitate proliferation? Crit Rev Oncol Hematol. 2002;42:65-78.[Web of Science][Medline]
[Order article via Infotrieve]
- Elstner A., Holtkamp N., von Deimling A. Involvement of Hif-1 in desferrioxamine-induced invasion of glioblastoma cells. Clin Exp Metastasis. 2007;24:57-66.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Kato M., Seki N., Sugano S., et al. Identification of sonic hedgehog-responsive genes using cDNA microarray. Biochem Biophys Res Commun. 2001;289:472-478.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Bar EE, Chaudhry A., Lin A., et al. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells. 2007:2007-0166.
- Ghatak S., Misra S., Toole BP Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway. J Biol Chem. 2002;277:38013-38020.[Abstract/Free Full Text]
- Itano N., Atsumi F., Sawai T., et al. Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration. Proc Natl Acad Sci U S A. 2002;99:3609-3614.[Abstract/Free Full Text]
- Sohara Y., Ishiguro N., Machida K., et al. Hyaluronan activates cell motility of v-Src-transformed cells via Ras-mitogenactivated protein kinase and phosphoinositide 3-kinase-Akt in a tumor-specific manner. Mol Biol Cell. 2001;12:1859-1868.[Abstract/Free Full Text]
- Ward JA, Huang L., Guo H., et al. Perturbation of hyaluronan interactions inhibits malignant properties of glioma cells. Am J Pathol. 2003;162:1403-1409.[Abstract/Free Full Text]
- Dehnhardt M., Zoriy MV, Khan Z., et al. Element distribution is altered in a zone surrounding human glioblastoma multiforme. J Trace Elem Med Biol. 2008;22:17-23.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Brem S., Grossman SA, Carson KA, et al. Phase 2 trial of copper depletion and penicillamine as antiangiogenesis therapy of glioblastoma. Neuro Oncol. 2005;7:246-253.[Abstract]
- Donate F., Juarez JC, Burnett ME, et al. Identification of biomarkers for the antiangiogenic and antitumour activity of the superoxide dismutase 1 (SOD1) inhibitor tetrathiomolybdate (ATN-224). Br J Cancer. 2008;98:776-783.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Lowndes SA, Harris AL The role of copper in tumour angiogenesis J Mammary Gland Biol Neoplasia. 2005;10:299-310.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Mazumder B., Fox PL Delayed translational silencing of ceruloplasmin transcript in gamma interferon-activated U937 monocytic cells: role of the 3' untranslated region. Mol Cell Biol. 1999;19:6898-6905.[Abstract/Free Full Text]
- Mukhopadhyay CK, Mazumder B., Fox PL Role of hypoxia-inducible factor-1 in transcriptional activation of ceruloplasmin by iron deficiency J Biol Chem. 2000;275: 21048-21054.[Abstract/Free Full Text]
- Das D., Tapryal N., Goswami SK, et al. Regulation of ceruloplasmin in human hepatic cells by redox active copper: identification of a novel AP-1 site in the ceruloplasmin gene. Biochem J. 2007;402:135-141.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Comerford KM, Wallace TJ, Karhausen J., et al. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 2002;62:3387-3394.[Abstract/Free Full Text]
- Keith B., Simon MC Hypoxia-inducible factors, stem cells, and cancer. Cell. 2007;129:465-472.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Irie N., Matsuo T., Nagata I. Protocol of radiotherapy for glioblastoma according to the expression of HIF-1. Brain Tumor Pathol. 2004;21:1-6.[CrossRef][Medline]
[Order article via Infotrieve]
- Lee KH, Yun SJ, Nam KN, et al. Activation of microglial cells by ceruloplasmin. Brain Res. 2007;1171:1-8.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Sarkaria JN, Carlson BL, Schroeder MA, et al. Use of an ortho-topic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin Cancer Res. 2006;12:2264-2271.[Abstract/Free Full Text]
Journal of Child Neurology, Vol. 23, No. 10,
1221-1230 (2008)
DOI: 10.1177/0883073808321066

CiteULike Complore Connotea Del.icio.us Digg Reddit Technorati Twitter What's this?
This article has been cited by other articles:

|
 |

|
 |
 
R. A. Brumback
Child Neurologists Should Be Interested In Brain Tumors!
J Child Neurol,
November 1, 2009;
24(11):
1338 - 1340.
[PDF]
|
 |
|
|
|