Antiphospholipid Antibodies Alter Cell-Death-Regulating Lipid Metabolites in First and Third Trimester Human Placentae

American Journal of Reproductive Immunology

Volumn 74, Issue 2, 2015, Pages 181-199

  Pantham, Priyadarshini ^a,b   Heazell, Alexander E P ^c   Mullard, Graham ^c   Begley, Paul ^c   Chen, Qi ^a   Brown, Maria ^c   Dunn, Warwick B ^c,d   Chamley, Lawrence W ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b Children's Hospital Colorado   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Antiphospholipid antibodies; Apoptosis; Ceramides; Metabolomics; Protein kinase C; Syncytiotrophoblast

Indexed keywords

CERAMIDE; CHORIONIC GONADOTROPIN; DIACYLGLYCEROL; LIPID; PHOSPHOLIPID ANTIBODY; PROTEIN KINASE C EPSILON;

ARTICLE; CELL DEATH; CELL DEATH REGULATING LIPID METABOLITE; CONTROLLED STUDY; FEMALE; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN TISSUE; MATERNAL BLOOD; METABOLITE; METABOLOMICS; PHOSPHOLIPID SYNTHESIS; PLACENTA; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; SPHINGOLIPID METABOLISM; SYNCYTIOTROPHOBLAST; THIRD TRIMESTER PREGNANCY; TROPHOBLAST; DRUG EFFECTS; LIPID METABOLISM; METABOLISM; PREGNANCY;

ANTIBODIES, ANTIPHOSPHOLIPID; CELL DEATH; FEMALE; HUMANS; LIPID METABOLISM; METABOLOMICS; PLACENTA; PREGNANCY; PREGNANCY TRIMESTER, FIRST; PREGNANCY TRIMESTER, THIRD; PROTEIN KINASE C-EPSILON;

EID: 84935757500     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12387     Document Type: Article

References (69)

1. Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, Derksen RH, DE Groot PG, Koike T, Meroni PL, Reber G, Shoenfeld Y, Tincani A, Vlachoyiannopoulos PG, Krilis SA: International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 2006; 4:295-306.
2. Sibai B, Dekker G, Kupferminc M: Pre-eclampsia. Lancet 2005; 365:785-799.
3. Krugner-Higby L, Luck M, Hartley D, Crispen HM, Lubach GR, Coe CL: High-risk pregnancy in rhesus monkeys (Macaca mulatta): a case of ectopic, abdominal pregnancy with birth of a live, term infant, and a case of gestational diabetes complicated by pre-eclampsia. J Med Primatol 2009; 38:252-256.
4. Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK: Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 1989; 161:1200-1204.
5. Poston L: Endothelial dysfunction in pre-eclampsia. Pharmocol Rep 2006; 58:69-74.
6. Schmorl G: Pathologisch-anatomische Untersuchungen über Puerperal-Eklampsie, Leipzig, Verlag FCW, 1893.
7. Chen Q, Stone PR, McCowan LM, Chamley LW: Phagocytosis of necrotic but not apoptotic trophoblasts induces endothelial cell activation. Hypertension 2006; 47:116.
8. Duckitt K, Harrington D: Risk factors for pre-eclampsia at antenatal booking: systematic review of controlled studies. Br Med J 2005; 330:565-567.
9. Viall CA, Chen Q, Liu B, Hickey A, Snowise S, Salmon JE, Stone PR, Chamley LW: Antiphospholipid antibodies internalised by human syncytiotrophoblast cause aberrant cell death and the release of necrotic trophoblast debris. J Autoimmun 2013; 47:45-57.
10. Chen Q, Guo F, Hensby-Bennett S, Stone P, Chamley L: Antiphospholipid antibodies prolong the activation of endothelial cells induced by necrotic trophoblastic debris: implications for the pathogenesis of preeclampsia. Placenta 2012; 33:810-815.
11. Chen Q, Viall C, Kang Y, Liu B, Stone P, Chamley L: Anti-phospholipid antibodies increase non-apoptotic Trophoblast Shedding: a contribution to the pathogenesis of pre-eclampsia in affected women? Placenta 2009; 30:767-773.
12. Chen Q, Viall C, Stone P, Chamley L: Antiphospholipid antibodies, trophoblast deportation and preeclampsia. Placenta 2008; 29:A1-A102.
13. Kell D, Brown M, Davey H, Dunn W, Spasic I, Oliver S: Metabolic footprinting and systems biology: the medium is the message. Nat Rev Microbiol 2005; 3:557.
14. Dunn W, Brown M, Worton S, Crocker I, Broadhurst D, Horgan R, Kenny L, Baker P, Kell D, Heazell A: Changes in the metabolic footprint of placental explant-conditioned culture medium identifies metabolic disturbances related to hypoxia and pre-eclampsia. Placenta 2009; 30:974.
15. Dunn WB, Brown M, Worton SA, Davies K, Jones RL, Kell DB, Heazell AE: The metabolome of human placental tissue: investigation of first trimester tissue and changes related to preeclampsia in late pregnancy. Metabolomics 2012; 8:579-597.
16. Heazell A, Bernatavicius G, Warrander L, Brown M, Dunn W: A metabolomic approach identifies differences in maternal serum in third trimester pregnancies that end in poor perinatal outcome. Reprod Sci 2012; 19:863-875.
17. Heazell A, Brown M, Dunn W, Worton S, Crocker I, Baker P, Kell D: Analysis of the metabolic footprint and tissue metabolome of placental villous explants cultured at different oxygen tensions reveals novel redox biomarkers. Placenta 2008; 29:691-698.
18. Horgan R, Broadhurst D, Dunn W, Brown M, Heazell A, Kell D, Baker P, Kenny L: Changes in the metabolic footprint of placental explant-conditioned medium cultured in different oxygen tensions from placentas of small for gestational age and normal pregnancies. Placenta 2010; 31:893-901.
19. Kenny LC, Broadhurst DI, Dunn W, Brown M, North RA, McCowan L, Roberts C, Cooper GJ, Kell DB, Baker PN: Robust early pregnancy prediction of later preeclampsia using metabolomic biomarkers. Hypertension 2010; 56:741-749.
20. Austdal M, Skrastad RB, Gundersen AS, Austgulen R, Iversen AC, Bathen TF: Metabolomic biomarkers in serum and urine in women with preeclampsia. PLoS ONE 2014; 9:e91923.
21. Bahado-Singh RO, Akolekar R, Mandal R, Dong E, Xia J, Kruger M, Wishart DS, Nicolaides K: Metabolomics and first-trimester prediction of early-onset preeclampsia. J Matern Fetal Neonatal Med 2012; 25:1840-1847.
22. Diaz SO, Barros AS, Goodfellow BJ, Duarte IF, Galhano E, Pita C, Almeida Mdo C, Carreira IM, Gil AM: Second trimester maternal urine for the diagnosis of trisomy 21 and prediction of poor pregnancy outcomes. J Proteome Res 2013; 12:2946-2957.
23. Kuc S, Koster MP, Pennings JL, Hankemeier T, Berger R, Harms AC, Dane AD, Schielen PC, Visser GH, Vreeken RJ: Metabolomics profiling for identification of novel potential markers in early prediction of preeclampsia. PLoS ONE 2014; 9:e98540.
24. Navaratnam K, Alfirevic Z, Baker PN, Gluud C, Gruttner B, Kublickiene K, Zeeman G, Kenny LC: A multi-centre phase IIa clinical study of predictive testing for preeclampsia: improved pregnancy outcomes via early detection (IMPROvED). BMC Pregnancy Childbirth 2013; 13:226.
25. Matsuura E, Igarashi Y, Yasuda T, Triplett D, Koike T: Anticardiolipin antibodies recognize beta 2-glycoprotein I structure altered by interacting with an oxygen modified solid phase surface. J Exp Med 1994; 179:457.
26. Pantham P, Rosario R, Chen Q, Chamley L: Transcriptomic analysis of placenta affected by antiphospholipid antibodies: following the TRAIL of trophoblast death. J Reprod Immunol 2012; 94:151-154.
27. Odiari E, Mulla M, Sfakianaki A, Paidas M, Stanwood N, Gariepy A, Brosens J, Chamley L, Abrahams V: Pravastatin does not prevent antiphospholipid antibody-mediated changes in human first trimester trophoblast function. Hum Reprod 2012; 27:2933-2940.
28. Dunn WB, Broadhurst D, Begley P, Zelena E, Francis-McIntyre S, Anderson N, Brown M, Knowles JD, Halsall A, Haselden JN: Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc 2011; 6:1060-1083.
29. Smith C, Want E, O'Maille G, Abagyan R, Siuzdak G: XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 2006; 78:779.
30. Brown M, Wedge D, Goodacre R, Kell D, Baker P, Kenny L, Mamas M, Neyses L, Dunn W: Automated workflows for accurate mass-based putative metabolite identification in LC/MS-derived metabolomic datasets. Bioinformatics 2011; 27:1108.
31. Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, Daykin CA, Fan TWM, Fiehn O, Goodacre R, Griffin JL: Proposed minimum reporting standards for chemical analysis. Metabolomics 2007; 3:211-221.
32. Oliveros J: VENNY. An interactive tool for comparing lists with Venn Diagrams. In BioinfoGP, CNB-CSIC, 2007.
33. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F: Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3:research0034.
34. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL: The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009; 55:611-622.
35. Foidart JM, Hustin J, Dubois M, Schaaps JP: The human placenta becomes haemochorial at the 13th week of pregnancy. Int J Dev Biol 1992; 36:451-453.
36. Okazaki T, Bell R, Hannun Y: Sphingomyelin turnover induced by vitamin D3 in HL-60 cells. Role in cell differentiation. J Biol Chem 1989; 264:19076.
37. Haimovitz-Friedman A, Kan C, Ehleiter D, Persaud R, McLoughlin M, Fuks Z, Kolesnick R: Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J Exp Med 1994; 180:525.
38. Verheij M, Bose R, Lin X, Yao B, Jarvis W, Grant S, Birrer M, Szabo E, Zon L, Kyriakis J: Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 1996; 380:75.
39. Hannun Y, Obeid L: Ceramide: an intracellular signal for apoptosis. Trends Biochem Sci 1995; 20:73.
40. Giuliano M, Calvaruso G, Pellerito O, Portanova P, Carlisi D, Vento R, Tesoriere G: Anandamide-induced apoptosis in Chang liver cells involves ceramide and JNK/AP-1 pathway. Int J Mol Med 2006; 17:811.
41. Obeid L, Linardic C, Karolak L, Hannun Y: Programmed cell death induced by ceramide. Science 1993; 259:1769.
42. Ruvolo P: Intracellular signal transduction pathways activated by ceramide and its metabolites. Pharmacol Res 2003; 47:383.
43. Vaandrager AB, Houweling M: Effect of ceramides on phospholipid biosynthesis and its implication for apoptosis. Subcell Biochem 2002; 36:207-227.
44. Sawai H, Okazaki T, Takeda Y, Tashima M, Sawada H, Okuma M, Kishi S, Umehara H, Domae N: Ceramide-induced translocation of protein kinase C-delta and-epsilon to the cytosol. Implications in apoptosis. J Biol Chem 1997; 272:2452.
45. Flores I, Jones DR, Merida I: Changes in the balance between mitogenic and antimitogenic lipid second messengers during proliferation, cell arrest, and apoptosis in T-lymphocytes. FASEB J 2000; 14:1873-1875.
46. Carrasco S, Merida I: Diacylglycerol, when simplicity becomes complex. Trends Biochem Sci 2007; 32:27-36.
47. Nishizuka Y: Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 1992; 258:607.
48. Sillence DJ, Allan D: Utilization of phosphatidylcholine and production of diradylglycerol as a consequence of sphingomyelin synthesis. Biochem J 1998; 331(Pt 1):251-256.
49. Musashi M, Ota S, Shiroshita N: The role of protein kinase C isoforms in cell proliferation and apoptosis. Int J Hematol 2000; 72:12.
50. Gubina E, Rinaudo M, Szallasi Z, Blumberg P, Mufson R: Overexpression of protein kinase C isoform epsilon but not delta in human interleukin-3-dependent cells suppresses apoptosis and induces bcl-2 expression. Blood 1998; 91:823.
51. Emoto Y, Manome Y, Meinhardt G, Kisaki H, Kharbanda S, Robertson M, Ghayur T, Wong WW, Kamen R, Weichselbaum R: Proteolytic activation of protein kinase C delta by an ICE-like protease in apoptotic cells. EMBO J 1995; 14:6148-6156.
52. Graler MH, Goetzl EJ: Lysophospholipids and their G protein-coupled receptors in inflammation and immunity. Biochim Biophys Acta 2002; 1582:168-174.
53. Peter C, Waibel M, Radu CG, Yang LV, Witte ON, Schulze-Osthoff K, Wesselborg S, Lauber K: Migration to apoptotic "find-me" signals is mediated via the phagocyte receptor G2A. J Biol Chem 2008; 283:5296-5305.
54. Abumaree MH, Stone PR, Chamley LW: The effects of apoptotic, deported human placental trophoblast on macrophages: possible consequences for pregnancy. J Reprod Immunol 2006; 72:33-45.
55. Denzlinger C, Rapp S, Hagmann W, Keppler D: Leukotrienes as mediators in tissue trauma. Science 1985; 230:330.
56. Smith WL: The eicosanoids and their biochemical mechanisms of action. Biochem J 1989; 259:315-324.
57. McCrae K, DeMichele A, Pandhi P, Balsai M, Samuels P, Graham C, Lala P, Cines D: Detection of antitrophoblast antibodies in the sera of patients with anticardiolipin antibodies and fetal loss. Blood 1993; 82:2730.
58. Carreras L, Vermylen J, Spitz B, Van Assche A: "Lupus" anticoagulant and inhibition of prostacyclin formation in patients with repeated abortion, intrauterine growth retardation and intrauterine death. Br J Obstet Gynaecol 1981; 88:890.
59. Lellouche F, Martinuzzo M, Said P, Maclouf J, Carreras L: Imbalance of thromboxane/prostacyclin biosynthesis in patients with lupus anticoagulant. Blood 1991; 78:2894.
60. Pierro E, Cirino G, Bucci M, Lazzarin N, Andreani C, Mancuso S, Lanzone A, Navarra P: Antiphospholipid antibodies inhibit prostaglandin release by decidual cells of early pregnancy: possible involvement of extracellular secretory phospholipase A2. Fertil Steril 1999; 71:342.
61. Schafer ZT, Grassian AR, Song L, Jiang Z, Gerhart-Hines Z, Irie HY, Gao S, Puigserver P, Brugge JS: Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 2009; 461:109-113.
62. Boren J, Brindle KM: Apoptosis-induced mitochondrial dysfunction causes cytoplasmic lipid droplet formation. Cell Death Differ 2012; 19:1561-1570.
63. May K, Rosenlöf L, Olsson M, Centlow M, Mörgelin M, Larsson I, Cederlund M, Rutardottir S, Siegmund W, Schneider H: Perfusion of human placenta with hemoglobin introduces preeclampsia-like injuries that are prevented by α1-microglobulin. Placenta 2011; 32:323.
64. Anderson UD, Olsson MG, Rutardóttir S, Centlow M, Kristensen KH, Isberg PE, Thilaganathan B, Åkerström B, Hansson SR: Fetal hemoglobin and α1-microglobulin as first-and early second-trimester predictive biomarkers for preeclampsia. Am J Obstet Gynecol 2011; 204:520. e521-520. e525.
65. Olsson M, Centlow M, Rutardóttir S, Stenfors I, Larsson J, Hosseini-Maaf B, Olsson M, Hansson S, Akerström B: Increased levels of cell-free hemoglobin, oxidation markers, and the antioxidative heme scavenger alpha (1)-microglobulin in preeclampsia. Free Radic Biol Med 2010; 48:284.
66. Centlow M, Carninci P, Nemeth K, Mezey E, Brownstein M, Hansson SR: Placental expression profiling in preeclampsia: local overproduction of hemoglobin may drive pathological changes. Fertil Steril 2008; 90:1834.
67. Delgado Alves J, Mason LJ, Ames PR, Chen PP, Rauch J, Levine JS, Subang R, Isenberg DA: Antiphospholipid antibodies are associated with enhanced oxidative stress, decreased plasma nitric oxide and paraoxonase activity in an experimental mouse model. Rheumatology 2005; 44:1238-1244.
68. Chamley L, Duncalf A, Mitchell M, Johnson P: Action of anticardiolipin and antibodies to beta2-glycoprotein-I on trophoblast proliferation as a mechanism for fetal death. Lancet 1998; 352:1037.
69. Tong M, Viall CA, Chamley LW: Antiphospholipid antibodies and the placenta: a systematic review of their in vitro effects and modulation by treatment. Hum Reprod Update 2015; 21:97-118.