Ceramide biosynthesis and metabolism in trophoblast syncytialization

Molecular and Cellular Endocrinology

Volumn 362, Issue 1-2, 2012, Pages 48-59

  Singh, Ambika T ^a,b   Dharmarajan, Arunasalam ^b   Aye, Irving L M H ^a   Keelan, Jeffrey A ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Acid sphingomyelinase; Cell fusion; Ceramidase; Ceramide kinase; Placenta; Sphingolipid

Indexed keywords

ALKALINE PHOSPHATASE; CASPASE 8; CERAMIDASE; CERAMIDE; CHORIONIC GONADOTROPIN; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; UVOMORULIN;

ARTICLE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL FUSION; CELL ISOLATION; CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; FEMALE; GENETIC TRANSFECTION; HORMONE RELEASE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOBLOTTING; IN VITRO STUDY; LIPID ANALYSIS; LIPID METABOLISM; LIPOGENESIS; LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; SYNCYTIALIZATION; TANDEM MASS SPECTROMETRY; TROPHOBLAST;

ANTHRACENES; ANTIGENS, DIFFERENTIATION; CASPASE 8; CELL DIFFERENTIATION; CELL FUSION; CELLS, CULTURED; CERAMIDASES; CERAMIDES; CHORIONIC GONADOTROPIN; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION; GIANT CELLS; HUMANS; NUCLEAR PROTEINS; OKADAIC ACID; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN PROCESSING, POST-TRANSLATIONAL; PYRANS; SPHINGOMYELIN PHOSPHODIESTERASE; SPIRO COMPOUNDS; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 84865306307     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.05.009     Document Type: Article

References (62)

1. Adler R.R., Ng A.K., Rote N.S. Monoclonal antiphosphatidylserine antibody inhibits intercellular fusion of the choriocarcinoma line, JAR. Biol. Reprod. 1995, 53(4):905-910.
2. Alsat E., Wyplosz P., Malassine A., Guibourdenche J., Porquet D., Nessmann C., Evain-Brion D. Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast, in vitro. J. Cell. Physiol. 1996, 168(2):346-353.
3. Auge N., Nikolova-Karakashian M.N., Carpentier S., Parthasarathy S., Negre-Salvayre A., Salvayre R., Merrill A.H. Role of sphingosine 1-phosphate in the mitogenesis induced by oxidized low density lipoprotein in smooth muscle cells via activation of sphingomyelinase, ceramidase, and sphingosine kinase. J. Biol. Chem. 1999, 274:21533-21538.
4. Aye I.L., Waddell B.J., Mark P.J., Keelan J.A. Placental ABCA1 and ABCG1 transporters efflux cholesterol and protect trophoblasts from oxysterol induced toxicity. Biochim. Biophys. Acta 2011, 1801(9):1013-1024.
5. Bielawska A., Bielawski J., Szulc Z.M., Mayroo N., Liu X., Bai A. Novel analogs of d-e-MAPP and B13. Part 2: signature effects on bioactive sphingolipids. Bioorg. Med. Chem. 2007, 16:1032-1045.
6. Bielawski J., Szulc Z.M., Hannun Y.A., Bielawska A. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 2006, 39(2):82-91.
7. Bourteele S., Doppler H., Horn-Muller J., Ropke C., Schwarzmann G., Pfizenmaier K., Muller G. Tumor necrosis factor induces ceramide oscillations and negatively controls sphingolipid synthases by caspases in apoptotic Kym-1 cells. J. Biol. Chem. 1998, 273(47):31245-31251.
8. Brosens I., Dixon H.G., Robertson W.B. Fetal growth retardation and the arteries of the placental bed. Br. J. Obstet. Gynaecol. 1977, 84(9):656-663.
9. Chen C.C., Boxer R.B., Stairs D.B., Portocarrero C.P., Horton R.H., Alvarez J.V., Birnbaum M.J., Chodosh L.A. Akt is required for Stat5 activation and mammary differentiation. Breast Cancer Res. 2010, 12(5):R72.
10. Cremesti A.E., Goni F.M., Kolesnick R. Role of sphingomyelinase and ceramide in modulating rafts: do biophysical properties determine biologic outcome?. FEBS Lett. 2002, 531:47-53.
11. Cuvillier O., Pirianov G., Kleuser B., Vanek P.G., Coso O.A., Gutkind S., Spiegel S. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 1996, 381:800-803.
12. Daoud G., Amyot M., Rassart E., Masse A., Simoneau L., Lafond J. ERK1/2 and p38 regulate trophoblasts differentiation in human term placenta. J. Physiol. 2005, 566(Pt 2):409-423.
13. Date T., Mitsutake S., Igarashi Y. Ceramide kinase expression is altered during macrophage-like cell differentiation of the leukemia cell line HL-60. In Vitro Cell. Dev. Biol. Anim. 2007, 43(10):321-323.
14. Delgado A., Casas J., Llebaria A., Abad J.L., Fabrias G. Inhibitors of sphingolipid metabolism enzymes. Biochim. Biophys. Acta 2006, 1758(12):1957-1977.
15. Evseenko D.A., Murthi P., Paxton J.W., Reid G., Emerald B.S., Mohankumar K.M., Lobie P.E., Brennecke S.P., Kalionis B., Keelan J.A. The ABC transporter BCRP/ABCG2 is a placental survival factor, and its expression is reduced in idiopathic human fetal growth restriction. FASEB J. 2007, 21(13):3592-3605.
16. Evseenko D.A., Paxton J.W., Keelan J.A. ABC drug transporter expression and functional activity in trophoblast-like cell lines and differentiating primary trophoblast. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290(3).
17. Frendo J.L., Cronier L., Bertin G., Guibourdenche J., Vidaud M., Evain-Brion D., Malassine A. Involvement of connexin 43 in human trophoblast cell fusion and differentiation. J. Cell Sci. 2003, 116(Pt 16):3413-3421.
18. Frendo J.L., Olivier D., Cheynet V., Blond J.L., Bouton O., Vidaud M., Rabreau M., Evain-Brion D., Mallet F. Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation. Mol. Cell. Biol. 2003, 23(10):3566-3574.
19. Futerman A.H., Hannun Y.A. The complex life of simple sphingolipids. EMBO Rep. 2004, 5(8):777-782.
20. Gangoiti P., Camacho L., Arana L., Ouro A., Granado M.H., Brizuela L., Casas J., Fabrias G., Abad J.L., Delgado A., Gomez-Munoz A. Control of metabolism and signaling of simple bioactive sphingolipids: implications in disease. Prog. Lipid Res. 2010, 49(4):316-334.
21. Gauster M., Moser G., Orendi K., Huppertz B. Factors involved in regulating trophoblast fusion: potential role in the development of preeclampsia. Placenta 2009, 30(Suppl. A):S49-S54.
22. Guilbert L.J., Riddell M., Winkler-Lowen B. Caspase activation is not required for villous cytotrophoblast fusion into syncytiotrophoblasts. Placenta 2010, 31(11):982-988.
23. Hannun Y.A., Obeid L.M. The ceramide-centric universe of lipid-mediated cell regulation: stress encounters of lipid kind. J. Biol. Chem. 2002, 277:25847-25850.
24. Himmelmann K., Himmelmann A., Niklasson A., Svensson A. Hypertension in pregnancy and size at birth. Blood Press. 1996, 5(5):278-284.
25. Houben E., Uchida Y., Nieuwenhuizen W.F., De Paepe K., Vanhaecke T., Holleran W.M., Rogiers V. Kinetic characteristics of acidic and alkaline ceramidase in human epidermis. Skin Pharmacol. Physiol. 2007, 20(4):187-194.
26. Huppertz B., Burton G., Cross J.C., Kingdom J.C. Placental morphology: from molecule to mother - a dedication to Peter Kaufmann - a review. Placenta 2006, 27(Suppl A):S3-S8.
27. Huppertz B., Frank H.G., Kingdom J.C.P., Reister F., Kaufmann P. Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta. Histochem. Cell Biol. 1998, 110:495-508.
28. Huppertz B., Frank H.G., Reister F., Kingdom J.C.P., Korr H., Kaufmann P. Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab. Invest. 1999, 79:1687-1702.
29. Jarvis W.D., Kolesnick R.N., Fornari F.A., Traylor R.S., Gewirtz D.A., Grant S. Induction of apoptotic DNA damage and cell death by activation of the sphingomyelin pathway. Proc. Nat. Acad. Sci. USA 1994, 91:73-77.
30. Kao L.C., Caltabiano S., Wu S., Strauss J.F., Kliman H.J. The human villous cytotrophoblast: interactions with extracellular matrix proteins, endocrine function, and cytoplasmic differentiation in the absence of syncytium formation. Dev. Biol. 1988, 130(2):693-702.
31. Knerr I., Schubert S.W., Wich C., Amann K., Aigner T., Vogler T., Jung R., Dotsch J., Rascher W., Hashemolhosseini S. Stimulation of GCMa and syncytin via cAMP mediated PKA signaling in human trophoblastic cells under normoxic and hypoxic conditions. FEBS Lett. 2005, 579(18):3991-3998.
32. Kudo Y., Boyd C.A., Sargent I.L., Redman C.W. Hypoxia alters expression and function of syncytin and its receptor during trophoblast cell fusion of human placental BeWo cells: implications for impaired trophoblast syncytialisation in pre-eclampsia. Biochim. Biophys. Acta 2003, 1638(1):63-71.
33. Lyden T.W., Ng A.K., Rote N.S. Modulation of phosphatidylserine epitope expression by BeWo cells during forskolin treatment. Placenta 1993, 14(2):177-186.
34. Mao C., Obeid L.M. Ceramidases: regulators of cellular responses mediated by ceramide, sphingosine, and sphingosine-1-phosphate. Biochim. Biophys. Acta 2008, 1781(9):424-434.
35. Mathias S., Younes A., Kan C.C., Orlow I., Joseph C., Kolesnick R.N. Activation of the sphingomyelin signaling pathway in intact EL4 cells and in a cell-free system by IL-1 beta. Science 1993, 259(5094):519-522.
36. Mi S., Lee X., Li X., Veldman G.M., Finnerty H., Racie L., LaVallie E., Tang X.Y., Edouard P., Howes S., Keith J.C., McCoy J.M. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 2000, 403(6771):785-789.
37. Mizugishi K., Li C., Olivera A., Bielawski J., Bielawska A., Deng C.X., Proia R.L. Maternal disturbance in activated sphingolipid metabolism causes pregnancy loss in mice. J. Clin. Invest. 2007, 117(10):2993-3006.
38. Morales A., Lee H., Goni F.M., Kolesnick R., Fernandez-Checa J.C. Sphingolipids and cell death. Apoptosis 2007, 12(5):923-939.
39. Morrish D.W., Bhardwaj D., Dabbagh L.K., Marusyk H., Siy O. Epidermal growth factor induces differentiation and secretion of human chorionic gonadotropin and placental lactogen in normal human placenta. J. Clin. Endocrinol. Metab. 1987, 65(6):1282-1290.
40. Newhouse S.M., Davidge S.T., Winkler-Lowen B., Demianczuk N., Guilbert L.J. In vitro differentiation of villous trophoblasts from pregnancies complicated by intrauterine growth restriction with and without pre-eclampsia. Placenta 2007, 28(10):999-1003.
41. Nikolova-Karakashian M.N., Morgan E.T., Alexander C., Liotta D.C., Merrill A.H. Bimodal regulation of ceramidase by interleukin-1. Implications for the regulation of cytochrome p450 2C11 (CYP2C11). J. Biol. Chem. 1997, 272:18718-18724.
42. Okazaki T., Bell R.M., Hannun Y.A. Sphingomyelin turnover induced by vitamin D3 in HL-60 cells. Role in cell differentiation. J. Biol. Chem. 1989, 264(32):19076-19080.
43. Orendi K., Gauster M., Moser G., Meiri H., Huppertz B. The choriocarcinoma cell line BeWo: syncytial fusion and expression of syncytium-specific proteins. Reproduction 2010, 140(5):759-766.
44. Pettus B.J., Bielawski J., Porcelli A.M., Reames D.L., Johnson K.R., Morrow J., Chalfant C.E., Obeid L.M., Hannun Y.A. The sphingosine kinase 1/sphingosine-1-phosphate pathway mediates COX-2 induction and PGE2 production in response to TNF-alpha. FASEB J. 2003, 17(11):1411-1421.
45. Pettus B.J., Chalfant C.E., Hannun Y.A. Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta 2002, 1585:114-125.
46. Raisova M., Goltz G., Bektas M., Bielawska A., Riebeling C., Hossini A.M., Eberle J., Hannun Y.A., Orfanos C.E., Geilen C.C. Bcl-2 overexpression prevents apoptosis induced by ceramidase inhibitors in malignant melanoma and HaCaT keratinocytes. FEBS Lett. 2002, 516(1-3):47-52.
47. Rote N.S., Wei B.R., Xu C., Luo L. Caspase 8 and human villous cytotrophoblast differentiation. Placenta 2010, 31(2):89-96.
48. Rotolo J.A., Zhang J., Donepudi M., Lee H., Fuks Z., Kolesnick R. Caspase-dependent and -independent activation of acid sphingomyelinase signaling. J. Biol. Chem. 2005, 280(28):26425-26434.
49. Ruvolo P.P. Ceramide regulates cellular homeostasis via diverse stress signaling pathways. Leukemia 2001, 15(8):153-160.
50. Ruvolo P.P. Intracellular signal transduction pathways activated by ceramide and its metabolites. Pharmacol. Res. 2003, 47(5):383-392.
51. Samsel L., Zaidel G., Drumgoole H.M., Jelovac D., Drachenberg C., Rhee J.G., Brodie A.M., Bielawska A., Smyth M.J. The ceramide analog, B13, induces apoptosis in prostate cancer cell lines and inhibits tumor growth in prostate cancer xenografts. Prostate 2004, 58(4):382-393.
52. Schoenfeld A., Abramovici A., Klibanski C., Ovadia J. Placental ultrasonographic biochemical and histochemical studies in human fetuses affected with Niemann-Pick disease type A. Placenta 1985, 6(1):33-43.
53. Selzner M., Bielawska A., Morse M.A., Rudiger H.A., Sindram D., Hannun Y.A., Clavien P.A. Induction of apoptotic cell death and prevention of tumor growth by ceramide analogues in metastatic human colon cancer. Cancer Res. 2001, 61(3):1233-1240.
54. Singh A.T., Dharmarajan A., Aye I.L., Keelan J.A. Sphingosine-sphingosine-1-phosphate pathway regulates trophoblast differentiation and syncytialization. Reprod. Biomed. Online 2011, 24(2):224-234.
55. Sun W., Xu R., Hu W., Jin J., Crellin H.A., Bielawski J., Szulc Z.M., Thiers B.H., Obeid L.M., Mao C. Upregulation of the human alkaline ceramidase 1 and acid ceramidase mediates calcium-induced differentiation of epidermal keratinocytes. J. Invest. Dermatol. 2008, 128(2):389-397.
56. Sweeney E.A., Inokuchi J., Igarashi Y. Inhibition of sphingolipid induced apoptosis by caspase inhibitors indicates that sphingosine acts in an earlier part of the apoptotic pathway than ceramide. FEBS Lett. 1998, 425:61-65.
57. Taha T.A., Mullen T.D., Obeid L.M. A house divided: ceramide, sphingosine, and sphingosine-1-phosphate in programmed cell death. Biochim. Biophys. Acta 2006, 1758(12):2027-2036.
58. van Blitterswijk W.J., van der Luit A.H., Veldman R.J., Verheij M., Borst J. Ceramide: second messenger or modulator of membrane structure and dynamics?. Biochem. J. 2003, 369(Pt 2):199-211.
59. van Lijnschoten G., Groener J.E., Maas S.M., Ben-Yoseph Y., Dingemans K.P., Offerhaus G.J. Intrauterine fetal death due to Farber disease: case report. Pediatr. Dev. Pathol. 2000, 3(6):597-602.
60. Wagner E.F., Nebreda A.R. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat. Rev. Cancer 2009, 9(8):537-549.
61. Yang M., Lei Z.M., Rao Ch V. The central role of human chorionic gonadotropin in the formation of human placental syncytium. Endocrinology 2003, 144(3):1108-1120.
62. Yu C., Shen K., Lin M., Chen P., Lin C., Chang G.D., Chen H. GCMa regulates the syncytin-mediated trophoblastic fusion. J. Biol. Chem. 2002, 277(51):50062-50068.