Galactosylceramide affects tumorigenic and metastatic properties of breast cancer cells as an anti-apoptotic molecule

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Owczarek, Tomasz B ^a,b   Suchanski, Jarosław ^b   Pula, Bartosz ^c   Kmiecik, Alicja M ^a   Chadalski, Marek ^a   Jethon, Aleksandra ^c   Dziegiel, Piotr ^c,d   Ugorski, Maciej ^a,b  

^a INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^b WROCLAW UNIVERSITY OF ENVIRONMENTAL AND LIFE SCIENCES   (Poland)

^c WROCLAW MEDICAL UNIVERSITY   (Poland)

^d UNIVERSITY OF WROC AW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; GALACTOSYLCERAMIDE; GANGLIOSIDE GALACTOSYLTRANSFERASE; MESSENGER RNA; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOACCUMULATION; BREAST CANCER; CANCER CELL; CANCER GROWTH; CARCINOGENICITY; CELL COUNT; CELL PROLIFERATION; CELL STRAIN; CELL STRAIN MDA MB 231; CELL SURVIVAL; CONTROLLED STUDY; DISEASE ACTIVITY; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIPID STORAGE; LIPOGENESIS; METASTASIS POTENTIAL; MOUSE; NONHUMAN; NUDE MOUSE; ORTHOTOPIC TRANSPLANTATION; PROTEIN EXPRESSION;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; DOXORUBICIN; FEMALE; GALACTOSYLCERAMIDES; GANGLIOSIDE GALACTOSYLTRANSFERASE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; LUNG NEOPLASMS; MICE; RNA, SMALL INTERFERING; TUMOR MARKERS, BIOLOGICAL;

EID: 84896692542     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084191     Document Type: Article

References (52)

1. Thudichum LJW (1874) Researches on the chemical constitution of the brain. In: Reports of the medical officer of the Privy Council and Local Government Board. New Series, No. III. pp. 113-247.
2. Carter HE, Greenwood FL (1952) Biochemistry of the sphingolipides. VII. Structure of the cerebrosides. J Biol Chem 199: 283-288.
3. Morell P, Radin NS (1969) Synthesis of cerebroside by brain from uridine diphosphate galactose and ceramide containing hydroxy fatty acid. Biochemistry 8: 506-12.
4. Marcus J, Popko B (2002) Galactolipids are molecular determinants of myelin development and axio-glial organization. Biochim Biophys Acta 1573: 406-413. (Pubitemid 35335451)
5. Nilsson O, Svennerholm L (1982) Characterization and quantitative determination of ganglioside and neutral glycosphingolipids in human liver. J Lipid Res 23: 327-334. (Pubitemid 12106211)
6. Davidoff MS, Middendorff R, Köfüncü E, Müller D, Jezek D, et al. (2002) Leydig cells of the human testis possess astrocyte and oligodendrocyte marker molecules. Acta Histochem 104: 39-49. (Pubitemid 34289839)
7. Sung CC, Collins R, Li J, Pearl DK, Coons SW, et al. (1996) Glycolipid and myelin proteins in human oligodendrogliomas. Glycoconj J 13: 433-443. (Pubitemid 26179976)
8. Popko B, Pearl DK, Walker DM, Comas TC, Baerwald KD, et al. (2002) Molecular markers that identify human astrocytomas and oligodendrogliomas. J Nauropathol Exp Neurol 61: 329-338. (Pubitemid 34266784)
9. Sprong H, Kruithof B, Leijendekker R, Slot JW, van Meer G, et al. (1998) UDP-galactose: ceramide galactosyltransferase is a class I integral membrane protein of the endoplasmic reticulum. J Biol Chem 273: 25880-25888.
10. Yang F, Foekens JA, Yu J, Sieuwerts AM, Timmermans M, et al. (2006) Laser microdissection and microarray analysis of breast tumors reveal ER-alpha related genes and pathways. Oncogene 25: 1413-1419. (Pubitemid 43336470)
11. Ruckhaberle E, Rody A, Engels K, Gaetje R, von Minckwitz G, et al. (2008) Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer. Breast Cancer Res Treat 112: 41-52.
12. Liu Y, Chen Y, Momin A, Shaner R, Wang E, et al. (2010) Elevation of sulfatides in ovarian cancer: an integrated transcriptomic and lipidomic analysis including tissue-imaging mass spectrometry. Mol Cancer 9: 186.
13. Landemaine T, Jackson A, Bellahcene A, Rucci N, Sin S, et al. (2008) A six-gene signature predicting breast cancer lung metastasis. Cancer Res 68: 6092-6099.
14. Dziegiel P, Owczarek T, Plazuk E, Gomulkiewicz A, Majchrzak M, et al. (2010) Ceramide galactosyltransferase (UGT8) is a molecular marker of breast cancer malignancy and lung metastases. Br J Cancer 103: 524-531.
15. Ogretmen B, Hannun YA (2001) Updates on functions of ceramide in chemotherapy-induced cell death and in multidrug resistance. Drug Resist Updat 4: 368-377. (Pubitemid 34746871)
16. Nikolova-Karakashian MN, Rozenova KA (2010) Ceramide in stress response. Adv Exp Med Biol 688: 86-108.
17. Carpinteiro A, Dumitru C, Schenck M, Gulbins E (2008) Ceramide-induced cell death in malignant cells. Cancer Lett 264: 1-10.
18. Reynolds PC, Maurer BJ, Kolesnick RN (2004) Ceramide synthesis and metabolism as a target for cancer therapy. Cancer Lett 206: 169-180. (Pubitemid 38317287)
19. Perry DK, Carton J, Shah AK, Meredith F, Uhlinger DJ, et al. (2000) Serine palmitoyltransferase regulates de novo ceramide generation during etoposide-induced apoptosis. J Biol Chem 275: 9078-9084. (Pubitemid 30180269)
20. Bose R, Verheij M, Haimovitz-Friedman A, Scotto K, Fuks Z, et al. (1995) Ceramide synthase mediates daunorubicin-induced apoptosis: An alternative mechanism for generating death signals. Cell 82: 405-414.
21. Zeidan YH, Wu BX, Jenkins RW, Obeid LM, Hannun YA (2008) A novel role for protein kinase Cdelta-mediated phosphorylation of acid sphingomyelinase in UV light-induced mitochondrial injury. FASEB J 22: 183-93.
22. Gulbins E, Kolesnick R (2003) Raft ceramide in molecular medicine. Oncogene 22: 7070-7077. (Pubitemid 37386676)
23. Luberto C, Hassler DF, Signorelli P, Okamoto Y, Sawai H, et al. (2002) Inhibition of tumor necrosis factor-induced cell death in MCF7 by a novel inhibitor of neutral sphingomyelinase. J Biol Chem 277: 41128-41139. (Pubitemid 35215704)
24. Gomez-Munoz A (2006) Ceramide 1-phosphate/ceramide, a switch between life and death. Biochim Biophys Acta 1758: 2049-2056.
25. Ponnusamy S, Meyers-Needham M, Senkal CE, Saddoughi SA, Sentelle D, et al. (2010) Future Oncol 6: 1603-1624.
26. Hannun YA, Luberto C, Argraves KM (2001) Enzymes of sphingolipid metabolism: from modular to integrative signaling. Biochemistry 40: 4893-4903. (Pubitemid 32332534)
27. Hiraoka M, Abe A, Shayman JA (2002) Cloning and characterization of a lysosomal phospholip-ase A2, 1-O-acylceramide synthase. J Biol Chem 277: 10090-10099. (Pubitemid 34968119)
28. Liu YY, Han TY, Giuliano AE, Cabot MC (2001) Ceramide glycosylation potentiates cellular multidrug resistance. FASEB J 15: 719-730. (Pubitemid 32245990)
29. Ryland LK, Fox TE, Liu X, Loughran TP, Kester M (2011) Dysregulation of sphingolipid metabolism in cancer. Cancer Biol Ther 11: 138-149.
30. Beier UH, Görögh T (2005) Implications of galactocerebrosidase and galactosylcerebroside metabolism in cancer cells. Int J Cancer 115: 6-10. (Pubitemid 40559664)
31. Xie K, Huang S (2003) Regulation of cancer metastasis by stress pathways. Clin Exp Metastasis 20: 31-43. (Pubitemid 36308134)
32. Niimura Y, Nagai K (2008) Metabolic responses of sulfatide and related glycolipids in Madin-Darby canine kidney (MDCK) cells under osmotic stresses. Comp. Biochem. Physiol 149B:161-167. (Pubitemid 350217042)
33. Niimura Y, Moue T, Takahashi N, Nagai K (2010) Modification of sphingolipids and sulfolipids In kidney cell lines dunder heat stress: acvtivation of monohexosylceramide synthesis as a ceramide scavenger. Glycobiology 20: 710-717.
34. Solatycka A, Owczarek T, Piller F, Piller V, Pula B, et al. (2012) MUC1 in human and murine mammary carcinoma cells decreases the expression of core 2 β1,6-N-acetylglucosaminyltransferase and β-galactoside α2,3-sialyltransferase. Glycobiology 8: 1042-54.
35. Ugorski M, Pahlsson P, Dus D, Nilsson B, Radzikowski C (1989) Glycosphingolipids of human urothelial cell lines with different grades of transformation. Glycoconj J 6: 303-318. (Pubitemid 19232058)
36. Ogawa K, Fujiwara Y, Sugamata K, Abe T (1988) Thin-layer chromatography of neutral glycosphingolipids an improved simple method for the resolution of GlcCer, LacCer and GalCer. J Chromatogr 426: 188-193.
37. Grazide S, Terrisse AD, Lerouge S, Laurent G, Jaffrezou JP (2004) Cytoprotective effect of glucosylceramide synthase inhibition against daunorubicin-induced apoptosis in human leukemic cell lines. J Biol Chem 279: 18256-18261. (Pubitemid 38623239)
38. Kok JW, Veldman RJ, Klappe K, Koning H, Filipeanu CM, et al. (2000) Differential expression of sphingolipids in MRP1 overexpressing HT29 cells. Int J Cancer 87: 172-178. (Pubitemid 30434341)
39. Veldman RJ, Klappe K, Hinrichs J, Hummel J, van der Schaaf G, et al. (2002) Altered sphingolipid metabolism in drug-resistant ovarian cancer cells is due to uncoupling of glycolipid biosynthesis in the Golgi apparatus. FASEB J 16: 1111-1113.
40. Lavie Y, Cao H, Bursten SL, Giuliano AE, Cabot MC (1996) Accumulation of glucosylceramides in multidrug-resistance cancer cells. J Biol Chem 271: 19530-19536. (Pubitemid 26271630)
41. Lucci A, Han TY, Liu YY, Giuliano AE, Cabot MC (1999) Multidrug resistance modulators and doxorubicin synergize to elevate ceramide levels and elcit apoptosis in drug-resistant cancer cells. Cancer 86: 300-311. (Pubitemid 29327587)
42. Spinedi A, Bartolomeo SD, Piacentini M (1998) Apoptosis induced by N-hexanoylsphingosine in CHP-100 cells associates with accumulation of endogenous ceramide and is potentiated by inhibition of glucosylcerebroside synthesis. Cell Death Differ 5: 785-791. (Pubitemid 28439119)
43. Li CH, To KF, Tong JHM, Ciao Z, Xia T, et al. (2013) Enhancer of zeste homolog 2 sielnces microRNA-218 in human pancreatic ductal adenocarcinoma cells by inducing formation of heterochromatin. Gastroenterology 144: 1086-1097
44. Kültz D (2006) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol. 67: 225-257.
45. Bartkowiak K, Riethdorf S, Pantel K (2012) The interrelating dynamics of hypoxic tumor microenvironments and cancer cell phenotypes in cancer metastasis. Cancer Microenviron 5: 59-72.
46. Biberich E (2004) Integration of glycosphingolipid metabolism and cell-fate decisions in cancer and stem cells: review and hypothesis. Glycoconjugate J 2: 315-327.
47. Uchida Y, Itoch M, Taguchi Y, Yamaoka S, Umchara H, et al. (2004) Ceramide reduction and transcriptional up-regulation of glucosylceramide synthase through doxorubicin-activated Sp1 in drug-resistance HL-60/ADR cells. Cancer Res 64: 6271-6279. (Pubitemid 39129431)
48. Itoh M, Kitano T, Watanabe M, Kondo T, Yabu T, et al. (2003) Possible role of ceramide as an indicator of chemoresistane: decrease of the ceramide content via activation of glucosylceramide synthase and sphingomyelin synthase in chemoresistant leukemia. Clin Cancer Res 8: 415-423. (Pubitemid 36109759)
49. Liu YY, Yu JY, Yin D, Patwardhan GA, Gupta V, et al. (2008) A role for ceramide in driving cancer cell resistance to doxorubicin. FASEB J 22: 2541-2551. (Pubitemid 351948671)
50. Zhang X, Wu X, Su P, Gao Y, Meng B, Sun Y, et al. (2012) Doxorubicin influences the expression of glucosylceramide synthese in invasive ductal breast cancer. PLoS ONE 7: e48492-e48492.
51. Aroui S, Brahim S, De Waard M, Breard J, Kenani A (2009) Efficient induction of apoptosis coupled to cell-penetrating peptides compared to unconjugated doxorubicin in the human breast cancer cell line MDA-MB-231. Cancer Lett 285: 28-38.
52. Liu YY, Hill RA, Li YT (2013) Ceramide glycosylation catalyzed by glucosylceramide synthase and cancer drug resistance. Adv Cancer Res 117: 59-89.