Disruption of sphingolipid metabolism augments ceramide-induced autophagy in preeclampsia

Autophagy

Volumn 11, Issue 4, 2015, Pages 653-669

  Melland Smith, Megan ^a,b   Ermini, Leonardo ^c   Chauvin, Sarah ^a,b   Craig Barnes, Hayley ^c   Tagliaferro, Andrea ^a   Todros, Tullia ^d   Post, Martin ^b,c,e,f   Caniggia, Isabella ^a,b,c  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c Institute of Medical Science   (Canada)

^d UNIVERSITY OF TURIN   (Italy)

^e UNIVERSITY OF TORONTO   (Canada)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Autophagy; BOK; MCL1; Oxidative stress; Placenta; Preeclampsia; Sphingolipid metabolism

Indexed keywords

CERAMIDE; SERINE PALMITOYLTRANSFERASE; SPHINGOLIPID;

ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; ENZYME ACTIVITY; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PREECLAMPSIA; PROTEIN EXPRESSION; SPHINGOLIPID METABOLISM; TANDEM MASS SPECTROMETRY; TROPHOBLAST; ANIMAL; CELL CULTURE; DRUG EFFECTS; FEMALE; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; PLACENTA; PRE-ECLAMPSIA; PREGNANCY;

ANIMALS; AUTOPHAGY; CELLS, CULTURED; CERAMIDES; FEMALE; HUMANS; LIPID METABOLISM; MICE; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; SPHINGOLIPIDS;

EID: 84950106833     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1034414     Document Type: Article

References (52)

1. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 2008; 9:139-50; PMID:18216770; http://dx.doi.org/10.1038/nrm2329
2. Hannun YA. Functions of ceramide in coordinating cellular responses to stress. Science 1996; 274:1855-9; PMID:8943189; http://dx.doi.org/10.1126/science.274.5294.1855
3. Ferlinz K, Kopal G, Bernardo K, Linke T, Bar J, Breiden B, Neumann U, Lang F, Schuchman EH, Sandhoff K. Human acid ceramidase: processing, glycosylation, and lysosomal targeting. J Biol Chem 2001; 276:35352-60; PMID:11451951; http://dx.doi.org/10.1074/jbc.M103066200
4. Ferlinz K, Hurwitz R, Moczall H, Lansmann S, Schuchman EH, Sandhoff K. Functional characterization of the N-glycosylation sites of human acid sphingomyelinase by site-directed mutagenesis. Eur J Biochem 1997; 243:511-7; PMID:9030779; http://dx.doi.org/10.1111/j.1432-1033.1997.511_1a.x
5. Jenkins RW, Idkowiak-Baldys J, Simbari F, Canals D, Roddy P, Riner CD, Clarke JC, Hannun YA. A novel mechanism of lysosomal acid sphingomyelinase maturation: requirement for carboxyl-terminal proteolytic processing. J Biol Chem 2011; 286:3777-88; PMID:21098024; http://dx.doi.org/10.1074/jbc.M110.155234
6. Brady RO, Kanfer JN, Mock MB, Fredrickson DS. The metabolism of sphingomyelin. II. evidence of an enzymatic deficiency in niemann-pick disease. Proc Nat Acad Sci U S A 1966; 55:366-9; PMID:5220952; http://dx.doi.org/10.1073/pnas.55.2.366
7. Park JH, Schuchman EH. Acid ceramidase and human disease. Biochim Biophys Acta 2006; 1758:2133-8; PMID:17064658; http://dx.doi.org/10.1016/j.bbamem.2006.08.019
8. Kolesnick RN, Kronke M. Regulation of ceramide production and apoptosis. Annual Rev Physiol 1998; 60:643-65; PMID:9558480; http://dx.doi.org/10.1146/annurev.physiol.60.1.643
9. Zheng W, Kollmeyer J, Symolon H, Momin A, Munter E, Wang E, Kelly S, Allegood JC, Liu Y, Peng Q, et al. Ceramides and other bioactive sphingolipid backbones in health and disease: lipidomic analysis, metabolism and roles in membrane structure, dynamics, signaling and autophagy. Biochim Biophys Acta 2006; 1758:1864-84; PMID: 17052686; http://dx.doi.org/10.1016/j.bbamem.2006.08.009
10. Young MM, Kester M, Wang HG. Sphingolipids: regulators of crosstalk between apoptosis and autophagy. J Lipid Res 2013; 54:5-19; PMID:23152582; http://dx.doi.org/10.1194/jlr.R031278
11. Spiegel S, Cuvillier O, Edsall LC, Kohama T, Menzeleev R, Olah Z, Olivera A, Pirianov G, Thomas DM, Tu Z, et al. Sphingosine-1-phosphate in cell growth and cell death. Ann N Y Acad Sci 1998; 845:11-8; PMID:9668339; http://dx.doi.org/10.1111/j.1749-6632.1998.tb09658.x
12. Soleymanlou N, Wu Y, Wang JX, Todros T, Ietta F, Jurisicova A, Post M, Caniggia I. A novel Mtd splice isoform is responsible for trophoblast cell death in pre-eclampsia. Cell Death Differ 2005; 12:441-52; PMID:15775999; http://dx.doi.org/10.1038/sj.cdd.4401593
13. ACOG. Hypertension in pregnancy. Report of the american college of obstetricians and gynecologists’ task force on hypertension in pregnancy. Obstet Gynecol 2013; 122:1122-31; PMID:24150027; http://dx.doi.org/10.1097/01.AOG.0000437382.03963.88
14. Soleymanlou N, Jurisica I, Nevo O, Ietta F, Zhang X, Zamudio S, Post M, Caniggia I. Molecular evidence of placental hypoxia in preeclampsia. J Clin Endocrinol Metab 2005; 90:4299-308; PMID:15840747; http://dx.doi.org/10.1210/jc.2005-0078
15. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005; 308:1592-4; PMID:15947178; http://dx.doi.org/10.1126/science.1111726
16. Hubel CA. Oxidative stress in the pathogenesis of preeclampsia. Proc Society Exp Biol Med 1999; 222:222-35; http://dx.doi.org/10.1046/j.1525-1373.1999.d01-139.x
17. Soleymanlou N, Jurisicova A, Wu Y, Chijiiwa M, Ray JE, Detmar J, Todros T, Zamudio S, Post M, Caniggia I. Hypoxic switch in mitochondrial myeloid cell leukemia factor-1/Mtd apoptotic rheostat contributes to human trophoblast cell death in preeclampsia. Am J Pathol 2007; 171:496-506; PMID:17600131; http://dx.doi.org/10.2353/ajpath.2007.070094
18. Kalkat M, Garcia J, Ebrahimi J, Melland-Smith M, Todros T, Post M, Caniggia I. Placental autophagy regulation by the BOK-MCL1 rheostat. Autophagy 2013; 9:2140-53; PMID:24113155; http://dx.doi.org/10.4161/auto.26452
19. Redman CW, Sargent IL. Microparticles and immunomodulation in pregnancy and pre-eclampsia. J Rep Immunol 2007; 76:61-7; PMID: 17482271; http://dx.doi.org/10.1016/j.jri.2007.03.008
20. Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, Kuliszewski M, Post M. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest 2000; 105:577-87; PMID:10712429; http://dx.doi.org/10.1172/JCI8316
21. Myatt L, Cui X. Oxidative stress in the placenta. Histochem Cell Biol 2004; 122:369-82; PMID:15248072; http://dx.doi.org/10.1007/s00418-004-0677-x
22. Marchesini N, Hannun YA. Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem Cell Biol 2004; 82:27-44; PMID:15052326; http://dx.doi.org/10.1139/o03-091
23. Roberts JM, Hubel CA. Oxidative stress in preeclampsia. Am J Obstetric Gynecol 2004; 190:1177-8; PMID: 15167813; http://dx.doi.org/10.1016/j.ajog.2004.04.001
24. Das G, Shravage BV, Baehrecke EH. Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb Perspect Biol 2012; 4:1-14; PMID:22661635; http://dx.doi.org/10.1101/cshperspect.a008813
25. Oh SY, Choi SJ, Kim KH, Cho EY, Kim JH, Roh CR. Autophagy-related proteins, LC3 and Beclin-1, in placentas from pregnancies complicated by preeclampsia. Reproductive Sci 2008; 15:912-20; PMID: 19050324; http://dx.doi.org/10.1177/1933719108319159
26. Proksch D, Klein JJ, Arenz C. Potent inhibition of acid ceramidase by novel B-13 analogues. J Lipids 2011; 2011:1-8; PMID: 21490813; http://dx.doi.org/10.1155/2011/971618
27. Longtine MS, Chen B, Odibo AO, Zhong Y, Nelson DM. Villous trophoblast apoptosis is elevated and restricted to cytotrophoblasts in pregnancies complicated by preeclampsia, IUGR, or preeclampsia with IUGR. Placenta 2012; 33:352-9; PMID:22341340; http://dx.doi.org/10.1016/j.placenta.2012.01.017
28. Schulze H, Sandhoff K. Lysosomal lipid storage diseases. Cold Spring Harb Perspect Biol 2011; 3: a004804; PMID: 21502308; http://dx.doi.org/10.1101/cshperspect.a004804
29. Spijkers LJ, Alewijnse AE, Peters SL. Sphingolipids and the orchestration of endothelium-derived vasoactive factors: when endothelial function demands greasing. Mol Cells 2010; 29:105-11; PMID:20127284; http://dx.doi.org/10.1007/s10059-010-0042-y
30. Spijkers LJ, van den Akker RF, Janssen BJ, Debets JJ, De Mey JG, Stroes ES, van den Born BJ, Wijesinghe DS, Chalfant CE, MacAleese L, et al. Hypertension is associated with marked alterations in sphingolipid biology: a potential role for ceramide. PloS One 2011; 6: e21817; PMID:21818267; http://dx.doi.org/10.1371/journal.pone.0021817
31. Brodlie M, McKean MC, Johnson GE, Gray J, Fisher AJ, Corris PA, Lordan JL, Ward C. Ceramide is increased in the lower airway epithelium of people with advanced cystic fibrosis lung disease. Am J Resp Critical Care Med 2010; 182:369-75; PMID: 20395562; http://dx.doi.org/10.1164/rccm.200905-0799OC
32. Furuya H, Shimizu Y, Kawamori T. Sphingolipids in cancer. Cancer Metastasis Rev 2011; 30:567-76; PMID:22005951; http://dx.doi.org/10.1007/s10555-011-9304-1
33. Ogretmen B, Hannun YA. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer 2004; 4:604-16; PMID:15286740; http://dx.doi.org/10.1038/nrc1411
34. Olivier S, Fillet M, Malaise M, Piette J, Bours V, Merville MP, Franchimont. Sodium nitroprussideinduced osteoblast apoptosis is mediated by long chain ceramide and is decreased by raloxifene. Biochemical Pharmacol 2005; 69:891-901; PMID: 20395562; http://dx.doi.org/10.1016/j.bcp.2004.11.030
35. Boslem E, Meikle PJ, Biden TJ. Roles of ceramide and sphingolipids in pancreatic b-cell function and dysfunction. Islets 2012; 4:177-87; PMID:22847494; http://dx.doi.org/10.4161/isl.20102
36. Pattingre S, Bauvy C, Carpentier S, Levade T, Levine B, Codogno P. Role of JNK1-dependent Bcl¡2 phosphorylation in ceramide-induced macroautophagy. J Biol Chem 2009; 284:2719-28; PMID:19029119; http://dx.doi.org/10.1074/jbc.M805920200
37. Deroyer C, Renert AF, Merville MP, Fillet M. New role for EMD (emerin), a key inner nuclear membrane protein, as an enhancer of autophagosome formation in the C16-ceramide autophagy pathway. Autophagy 2014; 10:1229-40; PMID:24819607; http://dx.doi.org/10.4161/auto.28777
38. Li CM, Park JH, Simonaro CM, He X, Gordon RE, Friedman AH, Ehleiter D, Paris F, Manova K, Hepbildikler S, et al. Insertional mutagenesis of the mouse acid ceramidase gene leads to early embryonic lethality in homozygotes and progressive lipid storage disease in heterozygotes. Genomics 2002; 79:218-24; PMID:11829492; http://dx.doi.org/10.1006/geno.2002.6686
39. Liu X, Cheng JC, Turner LS, Elojeimy S, Beckham TH, Bielawska A, Keane, TE, Hannun YA, Norris JS. Acid ceramidase upregulation in prostate cancer: role in tumor development and implications for therapy. Expert Opin Therap Target 2009; 13:1449-58; PMID: 19874262; http://dx.doi.org/10.1517/14728220903357512
40. Li CM, Park JH, He X, Levy B, Chen F, Arai K, Adler DA, Disteche CM, Koch J, Sandhoff K, et al. The human acid ceramidase gene (ASAH): structure, chromosomal location, mutation analysis, and expression. Genomics 1999; 62:223-31; PMID:10610716; http://dx.doi.org/10.1006/geno.1999.5940
41. Mayhew TM. A stereological perspective on placental morphology in normal and complicated pregnancies. J Anatomy 2009; 215:77-90; PMID: 19141109; http://dx.doi.org/10.1111/j.1469-7580.2008.00994.x
42. Santana P, Pena LA, Haimovitz-Friedman A, Martin S, Green D, McLoughlin M, Cordon-Cardo C, Schuchman EH, Fuks Z, Kolesnick R. Acid sphingomyelinasedeficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell 1996; 86:189-99; PMID:8706124; http://dx.doi.org/10.1016/S0092-8674(00)80091-4
43. Jin J, Hou Q, Mullen TD, Zeidan YH, Bielawski J, Kraveka JM, Bielawska A, Obeid LM, Hannun YA, Hsu YT. Ceramide generated by sphingomyelin hydrolysis and the salvage pathway is involved in hypoxia/ reoxygenation-induced Bax redistribution to mitochondria in NT-2 cells. J Biol Chem 2008; 283:26509-17; PMID:18676372; http://dx.doi.org/10.1074/jbc.M801597200
44. Shirato K, Nakajima K, Korekane H, Takamatsu S, Gao C, Angata T, Ohtsubo K, Taniguchi N. Hypoxic regulation of glycosylation via the N-acetylglucosamine cycle. J Clinical Biochem Nutrition 2011; 48:20-5; PMID: 21297907; http://dx.doi.org/10.3164/jcbn.11-015FR
45. Ietta F, Wu Y, Winter J, Xu J, Wang J, Post M, Caniggia I. Dynamic HIF1A regulation during human placental development. Biol Reprod 2006; 75:112-21; PMID:16611863; http://dx.doi.org/10.1095/biolreprod.106.051557
46. Romanowicz L, Bankowski E. Lipid compounds of human wharton’s jelly and their alterations in preeclampsia. Int J Exp Pathol 2010; 91:1-9; PMID:19878355; http://dx.doi.org/10.1111/j.1365-2613.2009.00675.x
47. ACOG PB. Practice bulletin # 33: diagnosis and management of preeclampsia and eclampsia. Obstetric Gynecol 2002; 99:159-67; http://dx.doi.org/10.1016/S0029-7844(01)01747-1
48. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Canadian J Biochem Physiol 1959; 37:911-7; PMID: 13671378; http://dx.doi.org/10.1139/o59-099
49. Ray JE, Garcia J, Jurisicova A, Caniggia I. Mtd/Bok takes a swing: proapoptotic Mtd/Bok regulates trophoblast cell proliferation during human placental development and in preeclampsia. Cell Death Differ 2010; 17:846-59; PMID:19942931; http://dx.doi.org/10.1038/cdd.2009.167
50. Luo D, Wang J, Li J, Post M. Mouse snail is a target gene for HIF. Mol Cancer Res 2011; 9:234-45; PMID:21257819; http://dx.doi.org/10.1158/1541-7786.MCR-10-0214
51. Rutti MF, Richard S, Penno A, von Eckardstein A, Hornemann T. An improved method to determine serine palmitoyltransferase activity. J Lipid Res 2009; 50:1237-44; PMID:19181628; http://dx.doi.org/10.1194/jlr.D900001-JLR200
52. Realini N, Solorzano C, Pagliuca C, Pizzirani D, Armirotti A, Luciani R, Costi MP, Bandiera T, Piomelli D. Discovery of highly potent acid ceramidase inhibitors with in vitro tumor chemosensitizing activity. Sci Rep 2013; 3:1-7; PMID: 23301156; http://dx.doi.org/10.1038/srep01035