The Possible Role of GPI-Ceruloplasmin in Hypoxia De Novo Creation and Maintenance
Advances in Biochemistry
Volume 1, Issue 2, June 2013, Pages: 22-27
Received: May 30, 2013; Published: Jun. 30, 2013
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Author
Roberto Arrigoni, Department of Biosciences, Biotechnologies and Biopharmaceutics, Laboratory of Biochemistry and Molecular Biology, University of Bari; CNR Institute of Biomembranes and Bioenergetics, via Orabona 4, 70125 Bari, Italy
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Abstract
Ceruloplasmin is a member of the multicopper oxidases family (MCOs), multidomain proteins capable of oxidizing many structurally unrelated compounds reducing oxygen to water. While MCOs show great oxidative versatility, they can only transfer electrons to molecular oxygen, which is the obligate electron acceptor. Therefore, MCOs should also be considered as ‘‘O2 consuming enzymes’’. The glycosylphosphatidylinositol anchored ceruloplasmin (GPI-Cp) isoform present on the surface of the plasma membrane, does not seem to be involved in copper and iron metabolism. Since hypoxia is also a common feature of many rapidly growing solid tumors, we postulate that the regulation of GPI-Cp could be the molecular event in the creation and the maintenance of hypoxia in tumor cells. By inhibiting the GPI-Cp expression, it would appear possible to attempt to overcome tumor hypoxia, thus improving the efficiency of radiotherapy.
Keywords
Hypoxia, Glycosylphosphatidylinositol-Ceruloplasmin, Multicopper Oxidases, Oxygen-Consuming Enzyme, Tumor
To cite this article
Roberto Arrigoni, The Possible Role of GPI-Ceruloplasmin in Hypoxia De Novo Creation and Maintenance, Advances in Biochemistry. Vol. 1, No. 2, 2013, pp. 22-27. doi: 10.11648/j.ab.20130102.13
References
[1]
J. A. Bertout, S. A. Patel, and M. C. Simon, "The impact of O2 availability on human cancer," Nat. Rev. Cancer 2008, vol. 8, pp. 967–975.
[2]
M. C Brahimi-Horn., and J. Pouyssègur, "HIF at a glance," J. Cell Sci. 2009, vol. 122, pp. 1055-57
[3]
S. Rocha, "Gene regulation under low oxygen: holding your breath for transcription," Trends Biochem. Sci. 2007, vol. 32, pp. 389-97.
[4]
G. L. Semenza, "Molecular mechanisms mediating metastasis of hypoxic breast cancer cells," Trends Mol. Med. 2012, vol. 18, pp. 534–543.
[5]
X. Lu and Y. Kang, "Hypoxia and hypoxia-inducible factors: master regulators of metastasis," Clin. Cancer Res. 2011, vol. 16, pp. 5928–5935.
[6]
M. Mimeault, R. Hauke, P. P. Mehta, and S. K. Batra, "Recent advances on cancer stem/progenitor cell research: therapeutic implications for overcoming resistance to the most aggressive cancers," J. Cell Mol. Med. 2007, vol. 11, pp. 981–1011.
[7]
J. P. Cosse and C. Michiels, "Tumour hypoxia affects the responsiveness of cancer cells to chemotherapy and promotes cancer progression," Anticancer Agents Med. Chem. 2008, vol. 8, pp. 790–7.
[8]
P. Vaupel and A. Mayer, "Hypoxia in cancer: significance and impact on clinical outcome," Cancer Metastasis Rev 2007, vol. 26, pp. 225–39.
[9]
Y. Rong, D. L. Durden, E. G. Van Meir, and D. J. Brat, "Pseudopalisading necrosis in glioblastoma: a familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis," J. Neuropathol. 2006, vol. 6, pp. 529–539.
[10]
D. Ribatti, B. Nico, E. Crivellato, and A. Vacca, "The structure of the vascular network of tumors," Cancer Lett. 2007, vol. 248, pp. 18–23.
[11]
P. Buchler, H. A. Reber, R. S. Lavey, J. Tomlinson, M. W. Buchler, H. Friess, and O. J. Hines, "Tumor hypoxia correlates with metastatic tumor growth of pancreatic cancer in orthotopic murine model," J. Surg. Res. 2004, vol. 120, pp. 295–303.
[12]
X. F. Li and J. A. O’Donoghue, "Hypoxia in microcospic tumors," Cancer Lett. 2008, vol. 264, pp. 172–180.
[13]
A. V. Guitart, M. Hammoud, P. Dello Sbarba, Z. Ivanovic, and V. Praliron, "Slow-cycling/quiescence balance of hematopoietic stem cells is related to physiological gradient of oxygen," Exp. Hematol. 2010, vol. 38, pp. 847-51.
[14]
K. Parmar, P. Mauch, J. A. Vergilio, R. Sackstein, and J. D. Down, "Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia," Proc. Natl. Acad. Sci. USA 2007, vol. 104, pp. 5431–5436
[15]
A. Messerschmidt and R. Huber, "The blue oxidases, ascorbate oxidase, laccase and ceruplasmin," Eur. J. Biochem. 1990, vol. 187, pp. 341–352.
[16]
S. A. Roberts, A. Weichsel, G. Grass, K. Thakali, J. T. Hazzard, G. Tollin, C. Rensing, and W. R. Montfort, "Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli," Proc. Natl. Acad. Sci. USA 2002, vol. 99, pp. 2766–2771.
[17]
G. R. Lee, G. E. Cartwright, and M. M. Wintrobe, "Heme biosynthesis in copper deficient swine," Proc. Soc. Exp. Biol. Med. 1968; vol. 127, pp. 977-81.
[18]
G. R. Lee, Nacht S., J. N. Lukens, and G. E. Cartwright, "Iron metabolism in copper-deficient swine," J. Clin. Invest. 1968, vol. 47, pp. 2058-69.
[19]
H. A. Ragan, S. Nacht, G. R. Lee, C. R. Bishop, and G. E. Cartwright "Effect of ceruloplasmin on plasma iron in copper-deficient swine" Am. J. Physiol. 1969, vol. 217, pp. 1320-3.
[20]
S. Osaki, D. A. Johnson, and E. Frieden, "The possible significance of the ferrous oxidase activity of ceruloplasmin in normal human serum," J Biol Chem 1966, vol. 241, pp. 2746-51.
[21]
P. Vachette, E. Dainese, V. B. Vasyliev, P. Di Muro, M. Beltramini, D. I. Svergun, V. De Filippis, and B. Salvato, "A key structural role for active site type 3 copper ions in human ceruloplasmin," J Biol Chem 2002; vol. 277, pp. 40823-31.
[22]
B. N. Patel and S. David, "A novel GPI_anchored form of ceruloplasmin expressed by astrocytes," J. Biol. Chem. 1997, vol. 272, pp. 20185–20190.
[23]
R. R. Fortna, H. A. Watson, and S. E. Nyquist, "Glycosylphosphatidylinositol-anchored ceruloplasmin is expressed by rat Sertoli cells and is concentrated in detergent-insoluble membrane fractions," Biol. Reprod. 1999, vol. 61, pp. 1042–1049.
[24]
J. H. Lee, C. E. Horak, C. Khanna, Z. Meng, L. R. Yu, T. D. Veenstra, and P. S. Steeg, "Alterations in Gemin5 expression contribute to alternative mRNA splicing patterns and tumor cell motility," Cancer Res. 2008, vol. 68, pp. 639–644.
[25]
E. J. Mostad and J. R. Prohaska, "Glycosylphosphatidylinositol-linked ceruloplasmin is expressed in multiple rodent organs and is lower following dietary copper deficiency," Exp. Biol. Med. 2011, vol. 236, pp. 298-308.
[26]
L. Marques, A. Auriac, A. Willemetz, J. Banha, B. Silva, F. Canonne-Hergaux, and L. Costa, "Immune cells and hepatocytes express glycosylphosphatidylinositol-anchored ceruloplasmin at their cell surface," Blood Cells Mol Dis. 2012, vol. 48, pp. 110–120.
[27]
Y. Ke and Z. Ming Qian, "Iron misregulation in the brain: a primary cause of neurodegenerative disorders" Lancet Neurol. 2003, vol. 2, pp. 246-53.
[28]
L. Zecca, M. B. Youdim, P. Riederer, J. R. Connor, and R. R. Crichton, "Iron, brain ageing and neurodegenerative disorders" Nat. Rev. Neurosci. 2004, vol. 5, pp. 863-73.
[29]
T. Ganz, "Cellular iron: ferroportin is the only way out," Cell Metabolism 2005, vol. 1, pp. 155-157.
[30]
L. W. J. Klomp and J. D. Gitlin, "Expression of the ceruloplasmin gene in the human retina and brain: implications for a pathogenic model in aceruloplasminemia," Human Molecular Genetics 1996, vol. 5, pp. 1989-1996.
[31]
H. Hochstrasser, J. Tomiuk, U. Walter, S. Behnke, J. Spiegel, R. Kruger, G. Becker, O. Riess, and D. Berg, "Functional relevance of ceruloplasmin mutations in Parkinson’s disease," FASEB Journal 2005, vol. 19, pp. 1851-1853.
[32]
K. Nakamura and N. Go, "Function and molecular evolution of multicopper blue proteins," Cell Mol. Life Sci. 2005, vol. 62, pp. 2050–2066.
[33]
J. T. Hoopes and J. F. Dean, "Ferroxidase activity in a laccase-like multicopper oxidase from Liriodendron tulipifera," Plant Physiol. Biochem. 2004, vol. 42, pp. 27–33.
[34]
P. Bielli and L. Calabrese, "Structure to function relationships in ceruloplasmin: a ‘‘moonlighting’’ protein," Cell Mol. Life Sci. 2002, vol. 59, pp. 1413–1427.
[35]
G. Floris, R. Medda, A. Padiglia, and G. Musci, "The physiopathological significance of ceruloplasmin. A possible therapeutic approach," Biochem. Pharmacol. 2000, vol. 60, pp. 1735–1741.
[36]
R. D. Braun and A. L. Beatty, "Modeling of oxygen transport across tumor multicellular layers," Microvasc. Res. 2006, vol. 73, pp. 113–123.
[37]
J. Healy and K. Tipton, "Ceruloplasmin and what it might do," J. Neural Trasnm. 2007, vol. 114, pp. 777–781.
[38]
E. D. Harris, "Ceruloplasmin and iron: vindication after 30 years," Nutrition 1999, vol. 15, pp. 72–73.
[39]
V. Seshadri, P. L. Fox, and C. K. Mukhopadhyay, "Dual role of insulin in transcriptional regulation of the acute phase reactant ceruloplasmin," J. Biol. Chem. 2002, vol. 277, pp. 27903-11.
[40]
C. K. Mukhopadhyay, B. Mazumder, and P. L. Fox, "Role of hypoxia-inducible factor-1 in transcriptional activation of ceruloplasmin by iron deficiency," J. Biol. Chem. 2000, vol. 275, pp. 21048-54
[41]
F. Martin, T. Linden, D. M. Katschinski, F. Oehme, I. Flamme, C. K. Mukhopadhyay, K. Eckhardt, J. Troger, S. Barth, G. Camenisch, and R. H. Wenger, "Copper-dependent activation of hypoxia-inducible factor (HIF)-1: implications for ceruloplasmin regulation," Blood 2005, vol. 105, pp. 4613-9.
[42]
J. Sarkar, V. Seshadri, N. A. Tripoulas, M. E. Ketterer, P. L. Fox, "Role of ceruloplasmin in macrophage iron efflux during hypoxia," J. Biol. Chem. 2003, vol. 278, pp. 44018–24.
[43]
O. Erel, "Automated measurement of serum ferroxidase activity," Clin. Chem. 1998, vol. 44, pp. 2313-9.
[44]
M. I. Surks, K. S. Chinn, and L. R. Matoush, "Alterations in body composition in man after acute exposure to high altitude," J. Appl. Physiol. 1966, vol. 21, pp. 1741-6.
[45]
R. E. Fleming, I. P. Whitman, and J. D. Gitlin, "Induction of ceruloplasmin gene expression in rat lung during inflammation and hyperoxia," Am. J. Physiol. 1991, vol. 260, pp. 68–74.
[46]
S. Guller, C. S. Buhimschi, Y. Y. Ma, S. T. Huang, L. Yang, E. Kuczynski, E. Zambrano, C. J. Lockwood, and I. A. Buhimschi, "Placental expression of ceruloplasmin in pregnancies complicated by severe preeclampsia," Lab. Invest. 2008, vol. 88, pp. 1057–67.
[47]
J. Bourhis, "Hypoxia response pathways and radiotherapy for head and neck cancer," J. Clin. Oncol. 2006, vol. 24, pp. 725–726.
[48]
S. D. Young, R. S. Marshall, and R. P. Hill, "Hypoxia induces DNA over replication and enhances metastatic potential of murine tumor cells," Proc. Natl. Acad. Sci. USA 1988, vol. 85, pp. 9533–9537.
[49]
Y. Guan, K. R. Reddy, Q. Zhu, Y. Li, P. Weerasinghe, J. Prchal, G. L. Semenza, and N. Jing, "G-rich oligonucleotides inhibit HIF-1 alpha and HIF-2 alpha and block tumor growth," Mol. Ther. 2010, vol. 18, pp. 188–97.
[50]
Y. Huang, J. Yu, C. Yan, J. Hou, G. Zhang, Z. Fu, and X. Wang, "Effect of small interfering RNA targeting hypoxia-inducible factor-1 alpha on radiosensitivity of PC3 cell line," Urology 2012, vol. 79, pp. 744.e17–24.
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