Altered sphingolipid metabolism induced by tumor hypoxia - New vistas in glycolipid tumor markers

FEBS Letters

Volumn 584, Issue 9, 2010, Pages 1872-1878

  Yin, Jun ^a   Miyazaki, Keiko ^a   Shaner, Rebecca L ^b   Merrill, Alfred H ^b   Kannagi, Reiji ^a  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Dihydroceramide Delta4 desaturase 1 2; Dihydroceramide synthesis; Fatty acid 2 hydroxylase; Hypoxia inducible factor; N Glycolyl sialic acid; Unsaturated very long chain fatty acid

Indexed keywords

GANGLIOSIDE GD 1A; GANGLIOSIDE GD3; GANGLIOSIDE GM1; GANGLIOSIDE GM3; GLYCOLIPID; HYPOXIA INDUCIBLE FACTOR; PROTEIN P53; SIALYL LEWIS X ANTIGEN; SPHINGOLIPID; TUMOR MARKER; VERY LONG CHAIN FATTY ACID; VON HIPPEL LINDAU PROTEIN; CERAMIDE;

CARCINOGENESIS; EPIGENETICS; GENETIC TRANSCRIPTION; HUMAN; HYPOXIA; LIPID COMPOSITION; LIPID METABOLISM; MALIGNANT TRANSFORMATION; MASS SPECTROMETRY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; UBIQUITINATION; ANIMAL; ANOXIA; BIOLOGICAL MODEL; DISORDERS OF LIPID AND LIPOPROTEIN METABOLISM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; NEOPLASM; PHYSIOLOGY;

ANIMALS; ANOXIA; CERAMIDES; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOLIPIDS; HUMANS; LIPID METABOLISM DISORDERS; MASS SPECTROMETRY; MODELS, BIOLOGICAL; NEOPLASMS; SPHINGOLIPIDS; TUMOR MARKERS, BIOLOGICAL;

EID: 77951887561     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.11.019     Document Type: Review

References (48)

1. Hakomori S. Glycosylation defining cancer malignancy: new wine in an old bottle. Proc. Natl. Acad. Sci. USA 2002, 99:10231-10233.
2. Hakomori S. Tumor-associated carbohydrate antigens defining tumor malignancy: basis for development of anti-cancer vaccines. Adv. Exp. Med. Biol. 2001, 491:369-402.
3. Sabbatini P.J., Ragupathi G., Hood C., Aghajanian C.A., Juretzka M., Iasonos A., Hensley M.L., Spassova M.K., Ouerfelli O., Spriggs D.R., Tew W.P., Konner J., Clausen H., Abu R.N., Dansihefsky S.J., Livingston P.O. Pilot study of a heptavalent vaccine-keyhole limpet hemocyanin conjugate plus QS21 in patients with epithelial ovarian, fallopian tube, or peritoneal cancer. Clin. Cancer Res. 2007, 13:4170-4177.
4. Livingston P.O., Hood C., Krug L.M., Warren N., Kris M.G., Brezicka T., Ragupathi G. Selection of GM2, fucosyl GM1, globo H and polysialic acid as targets on small cell lung cancers for antibody-mediated immunotherapy. Cancer Immunol. Immunother. 2005, 54:1018-1025.
5. Koike T., Kimura N., Miyazaki K., Yabuta T., Kumamoto K., Takenoshita S., Chen J., Kobayashi M., Hosokawa M., Taniguchi A., Kojima T., Ishida N., Kawakita M., Yamamoto H., Takematsu H., Kozutsumi Y., Suzuki A., Kannagi R. Hypoxia induces adhesion molecules on cancer cells-a missing link between Warburg effect and induction of selectin ligand carbohydrates. Proc. Natl. Acad. Sci. USA 2004, 101:8132-8137.
6. Higashi H., Hirabayashi Y., Fukui Y., Naiki M., Matsumoto M., Ueda S., Kato S. Characterization of N-glycolylneuraminic acid-containing gangliosides as tumor-associated Hanganutziu-Deicher antigen in human colon cancer. Cancer Res. 1985, 45:3796-3802.
7. Kawai T., Kato A., Higashi H., Kato S., Naiki M. Quantitative determination of N-glycolylneuraminic acid expression in human cancerous tissues and avian lymphoma cell lines as a tumor-associated sialic acid by gas chromatography-mass spectrometry. Cancer Res. 1991, 51:1242-1246.
8. Yin J., Hashimoto A., Izawa M., Miyazaki K., Chen G.-Y., Takematsu H., Kozutsumi Y., Suzuki A., Furuhata K., Cheng F.-L., Lin C.-H., Sato C., Kitajima K., Kannagi R. Hypoxic culture induces expression of sialin, a sialic acid transporter, and cancer-associated gangliosides containing non-human sialic acid on human cancer cells. Cancer Res. 2006, 66:2937-2945.
9. Diaz S.L., Padler-Karavani V., Ghaderi D., Hurtado-Ziola N., Yu H., Chen X., Brinkman-Van der Linden E.C., Varki A., Varki N.M. Sensitive and specific detection of the non-human sialic acid N-glycolylneuraminic acid in human tissues and biotherapeutic products. PLoS. ONE 2009, 4:e4241.
10. Byres E., Paton A.W., Paton J.C., Lofling J.C., Smith D.F., Wilce M.C., Talbot U.M., Chong D.C., Yu H., Huang S., Chen X., Varki N.M., Varki A., Rossjohn J., Beddoe T. Incorporation of a non-human glycan mediates human susceptibility to a bacterial toxin. Nature 2008, 456:648-652.
11. Irie A., Suzuki A. CMP-N-Acetylneuraminic acid hydroxylase is exclusively inactive in humans. Biochem. Biophys. Res. Commun. 1998, 248:330-333.
12. Chou H.H., Takematsu H., Diaz S., Iber J., Nickerson E., Wright K.L., Muchmore E.A., Nelson D.L., Warren S.T., Varki A. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc. Natl. Acad. Sci. USA 1998, 95:11751-11756.
13. Chou H.H., Hayakawa T., Diaz S., Krings M., Indriati E., Leakey M., Paabo S., Satta Y., Takahata N., Varki A. Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc. Natl. Acad. Sci. USA 2002, 99:11736-11741.
14. Kandyba A.G., Kobliakov V.A., Kozlov A.M., Nagaev I.Y., Shevchenko V.P., Dyatlovitskaya E.V. Dihydroceramide desaturase activity in tumors. Biochemistry (Moscow) 2002, 67:597-599.
15. Kandyba A.G., Somova O.G., Kozlov A.M., Zubova E.S., Dudnik L.B., Alessenko A.V., Shvetz V.I., Dyatlovitskaya E.V. Sphingolipids of transplantable rat nephroma-RA. Biochemistry (Moscow) 2000, 65:703-706.
16. Thomlinson R.H., Gray L.H. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br. J. Cancer 1955, 9:539-549.
17. Tei K., Kawakami-Kimura N., Taguchi O., Kumamoto K., Higashiyama S., Taniguchi N., Toda K., Kawata R., Hisa Y., Kannagi R. Roles of cell adhesion molecules in tumor angiogenesis induced by co-transplantation of cancer and endothelial cells to nude rats. Cancer Res. 2002, 62:6289-6296.
18. Takada A., Ohmori K., Takahashi N., Tsuyuoka K., Yago K., Zenita K., Hasegawa A., Kannagi R. Adhesion of human cancer cells to vascular endothelium mediated by a carbohydrate antigen, sialyl Lewis A. Biochem. Biophys. Res. Commun. 1991, 179:713-719.
19. Takada A., Ohmori K., Yoneda T., Tsuyuoka K., Hasegawa A., Kiso M., Kannagi R. Contribution of carbohydrate antigens sialyl Lewis A and sialyl Lewis X to adhesion of human cancer cells to vascular endothelium. Cancer Res. 1993, 53:354-361.
20. Kannagi R. Carbohydrate-mediated cell adhesion involved in hematogenous metastasis of cancer. Glycoconj. J. 1997, 14:577-584.
21. Schwalm S., Doll F., Romer I., Bubnova S., Pfeilschifter J., Huwiler A. Sphingosine kinase-1 is a hypoxia-regulated gene that stimulates migration of human endothelial cells. Biochem. Biophys. Res. Commun. 2008, 368:1020-1025.
22. Anelli V., Gault C.R., Cheng A.B., Obeid L.M. Sphingosine kinase 1 is up-regulated during hypoxia in U87MG glioma cells. Role of hypoxia-inducible factors 1 and 2. J. Biol. Chem. 2008, 283:3365-3375.
23. Bielawska A., Crane H.M., Liotta D., Obeid L.M., Hannun Y.A. Selectivity of ceramide-mediated biology. Lack of activity of erythro-dihydroceramide. J. Biol. Chem. 1993, 268:26226-26232.
24. Hakomori S.I. Structure and function of glycosphingolipids and sphingolipids: recollections and future trends. Biochim. Biophys. Acta 2008, 1780:325-346.
25. Sonnino S., Mauri L., Chigorno V., Prinetti A. Gangliosides as components of lipid membrane domains. Glycobiology 2007, 17:1R-13R.
26. Sonnino S., Prinetti A., Mauri L., Chigorno V., Tettamanti G. Dynamic and structural properties of sphingolipids as driving forces for the formation of membrane domains. Chem. Rev. 2006, 106:2111-2125.
27. Hakomori S. Structure, organization, and function of glycosphingolipids in membrane. Curr. Opin. Hematol. 2003, 10:16-24.
28. Hakomori S., Handa K., Iwabuchi K., Yamamura S., Prinetti A. New insights in glycosphingolipid function: " glycosignaling domain," a cell surface assembly of glycosphingolipids with signal transducer molecules, involved in cell adhesion coupled with signaling. Glycobiology 1998, 8:xi-xix.
29. Kannagi R., Yin J., Miyazaki K., Izawa M. Current relevance of incomplete synthesis and neo-synthesis for cancer-associated alteration of carbohydrate determinants-Hakomori's concepts revisited. Biochim. Biophys. Acta 2008, 1780:525-531.
30. Izawa M., Kumamoto K., Mitsuoka C., Kanamori A., Ohmori K., Ishida H., Nakamura S., Kurata-Miura K., Sasaki K., Nishi T., Kannagi R. Expression of sialyl 6-sulfo Lewis x is inversely correlated with conventional sialyl Lewis x expression in human colorectal cancer. Cancer Res. 2000, 60:1410-1416.
31. Miyazaki K., Ohmori K., Izawa M., Koike T., Kumamoto K., Furukawa K., Ando T., Kiso M., Yamaji T., Hashimoto Y., Suzuki A., Yoshida A., Takeuchi M., Kannagi R. Loss of disialyl Lewisa, the ligand for lymphocyte inhibitory receptor Siglec-7, associated with increased sialyl Lewisa expression on human colon cancers. Cancer Res. 2004, 64:4498-4505.
32. Kannagi R., Izawa M., Koike T., Miyazaki K., Kimura N. Carbohydrate-mediated cell adhesion in cancer metastasis and angiogenesis. Cancer Sci. 2004, 95:377-384.
33. Kannagi R., Stroup R., Cochran N.A., Urdal D.L., Young W.W., Hakomori S. Factors affecting expression of glycolipid tumor antigens: influence of ceramide composition and coexisting glycolipid on the antigenicity of gangliotriaosylceramide in murine lymphoma cells. Cancer Res. 1983, 43:4997-5005.
34. Merrill A.H., Stokes T.H., Momin A., Park H., Portz B.J., Kelly S., Wang E., Sullards M.C., Wang M.D. Sphingolipidomics: a valuable tool for understanding the roles of sphingolipids in biology and disease. J. Lipid Res. 2009, 50(Suppl.):S97-S102.
35. Sullards M.C., Allegood J.C., Kelly S., Wang E., Haynes C.A., Park H., Chen Y., Merrill A.H. Structure-specific, quantitative methods for analysis of sphingolipids by liquid chromatography-tandem mass spectrometry: " inside-out" sphingolipidomics. Meth. Enzymol. 2007, 432:83-115.
36. Haus J.M., Kashyap S.R., Kasumov T., Zhang R., Kelly K.R., DeFronzo R.A., Kirwan J.P. Plasma ceramides are elevated in obese subjects with type 2 diabetes and correlate with the severity of insulin resistance. Diabetes 2009, 58:337-343.
37. Ichi I., Nakahara K., Miyashita Y., Hidaka A., Kutsukake S., Inoue K., Maruyama T., Miwa Y., Harada-Shiba M., Tsushima M., Kojo S. Association of ceramides in human plasma with risk factors of atherosclerosis. Lipids 2006, 41:859-863.
38. Auray-Blais C., Cyr D., Ntwari A., West M.L., Cox-Brinkman J., Bichet D.G., Germain D.P., Laframboise R., Melancon S.B., Stockley T., Clarke J.T., Drouin R. Urinary globotriaosylceramide excretion correlates with the genotype in children and adults with Fabry disease. Mol. Genet. Metab. 2008, 93:331-340.
39. Drobnik W., Liebisch G., Audebert F.X., Frohlich D., Gluck T., Vogel P., Rothe G., Schmitz G. Plasma ceramide and lysophosphatidylcholine inversely correlate with mortality in sepsis patients. J. Lipid Res. 2003, 44:754-761.
40. Kyogashima M., Tamiya-Koizumi K., Ehara T., Li G., Hu R., Hara A., Aoyama T., Kannagi R. Rapid demonstration of diversity of sulfatide molecular species from biological materials by MALDI-TOF MS. Glycobiology 2006, 16:719-728.
41. Hu R., Li G., Kamijo Y., Aoyama T., Nakajima T., Inoue T., Node K., Kannagi R., Kyogashima M., Hara A. Serum sulfatides as a novel biomarker for cardiovascular disease in patients with end-stage renal failure. Glycoconj. J. 2007, 24:565-571.
42. Misonou Y., Shida K., Korekane H., Seki Y., Noura S., Ohue M., Miyamoto Y. Comprehensive clinico-glycomic study of 16 colorectal cancer specimens: elucidation of aberrant glycosylation and its mechanistic causes in colorectal cancer cells. J. Proteome. Res. 2009, 8:2990-3005.
43. Wing D.R., Garner B., Hunnam V., Reinkensmeier G., Andersson U., Harvey D.J., Dwek R.A., Platt F.M., Butters T.D. High-performance liquid chromatography analysis of ganglioside carbohydrates at the picomole level after ceramide glycanase digestion and fluorescent labeling with 2-aminobenzamide. Anal. Biochem. 2001, 298:207-217.
44. Nagahori N., Abe M., Nishimura S. Structural and functional glycosphingolipidomics by glycoblotting with an aminooxy-functionalized gold nanoparticle. Biochemistry 2009, 48:583-594.
45. Chen Y., Allegood J., Liu Y., Wang E., Cachon-Gonzalez B., Cox T.M., Merrill A.H., Sullards M.C. Imaging MALDI mass spectrometry using an oscillating capillary nebulizer matrix coating system and its application to analysis of lipids in brain from a mouse model of Tay-Sachs/Sandhoff disease. Anal. Chem. 2008, 80:2780-2788.
46. Sugiura Y., Shimma S., Konishi Y., Yamada M.K., Setou M. Imaging mass spectrometry technology and application on ganglioside study; visualization of age-dependent accumulation of C20-ganglioside molecular species in the mouse hippocampus. PLoS. ONE 2008, 3:e3232.
47. Chan K., Lanthier P., Liu X., Sandhu J.K., Stanimirovic D., Li J. MALDI mass spectrometry imaging of gangliosides in mouse brain using ionic liquid matrix. Anal. Chim. Acta 2009, 639:57-61.
48. Yuyama Y., Dohi T., Morita H., Furukawa K., Oshima M. Enhanced expression of GM2/GD2 synthase mRNA in human gastrointestinal cancer. Cancer 1995, 75:1273-1280.