Antiphospholipid Antibodies Affect Human Endometrial Angiogenesis: Protective Effect of a Synthetic Peptide (TIFI) Mimicking the Phospholipid Binding Site of β2glycoprotein I

American Journal of Reproductive Immunology

Volumn 70, Issue 4, 2013, Pages 299-308

  Di Simone, Nicoletta ^a   D'Ippolito, Silvia ^a   Marana, Riccardo ^a   Di Nicuolo, Fiorella ^a   Castellani, Roberta ^a   Pierangeli, Silvia S ^b   Chen, Pojen ^c   Tersigni, Chiara ^a   Scambia, Giovanni ^a   Meroni, Pier Luigi ^d  

^a CATHOLIC UNIVERSITY   (Italy)

^b University of Texas Medical Branch School of Medicine   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

Antiphospholipid antibodies; Endometrial angiogenesis; TIFL

Indexed keywords

BETA2 GLYCOPROTEIN 1; DNA; GELATINASE A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOLIPID; PHOSPHOLIPID ANTIBODY; SYNTHETIC PEPTIDE; SYNTHETIC PEPTIDE TIFI; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA BINDING; DRUG EFFECT; ENDOMETRIAL ENDOTHELIAL CELL; ENDOMETRIUM; ENDOTHELIUM; ENDOTHELIUM CELL; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MEDIATOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANTIPHOSPHOLIPID ANTIBODIES; ENDOMETRIAL ANGIOGENESIS; TIFL;

ANTIBODIES, ANTIPHOSPHOLIPID; ANTIBODIES, BLOCKING; BETA 2-GLYCOPROTEIN I; BINDING SITES, ANTIBODY; BINDING, COMPETITIVE; CELLS, CULTURED; ENDOMETRIUM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; MATRIX METALLOPROTEINASE 2; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; NF-KAPPA B; PEPTIDES; PHOSPHOLIPIDS; PROTEIN BINDING; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84884205055     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12130     Document Type: Article

References (44)

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. Giannakopoulos B, Passam F, Rahgozar S, Krilis SA: Current concepts on the pathogenesis of the antiphospholipid syndrome (Review). Blood 2007; 109: 422-430.
3. Pierangeli SS, Chen PP, Raschi E, Scurati S, Grossi C, Borghi MO, Palomo I, Harris EN, Meroni PL: Antiphospholipid antibodies and the antiphospholipid syndrome: pathogenic mechanisms. Semin Thromb Hemost 2008; 34: 236-250.
4. Meroni PL, Borghi MO, Raschi E, Tedesco F: Pathogenesis of the antiphospholipid syndrome (APS): understanding the antibodies (Review). Nat Rev Rheumatol 2011; 7: 330-339.
5. Meroni PL: Pathogenesis of the antiphospholipid syndrome: an additional example of the mosaic of autoimmunity (Review). J Autoimmun 2008; 30: 99-103.
6. Blank M, Shoenfeld Y, Cabilly S, Heldman Y, Fridkin M, Katchalski-Katzir E: Prevention of experimental antiphospholipid syndrome and endothelial cell activation by synthetic peptides. Proc Natl Acd Sci USA 1999; 96: 5164-5168.
7. Ioannou Y, Romay-Penabad Z, Pericleous C, Giles I, Papalardo E, Vargas G, Shilagard T, Latchman DS, Isenberg DA, Rahman A, Pierangeli S: In vivo inhibition of antiphospholipid antibody-induced pathogenicity utilizing the antigenic target peptide domain I of β2-glycoprotein I: proof of concept. J Thromb Haemost 2009; 7: 833-842.
8. Blank M, Baraam L, Eisenstein M, Fridkin M, Dardik R, Heldman Y, Katchalski-Katzir E, Shoenfeld Y: β2-Glycoprotein-I based peptide regulate endothelial-cells tissue-factor expression via negative regulation of pGSK3β expression and reduces experimental-antiphospholipid-syndrome. J Autoimmun 2011; 37: 8-17.
9. Kolyada A, Lee CJ, De Biasio A, Beglova N: A novel dimeric inhibitor targeting Beta2GPI in Beta2GPI/antibody complexes implicated in antiphospholipid syndrome. PLoS ONE 2010; 5: e15345.
10. Ostertag MV, Liu X, Henderson V, Pierangeli SS: A peptide that mimics the Vth region of beta-2-glycoprotein I reverses antiphospholipid-mediated thrombosis in mice. Lupus 2006; 15: 358-365.
11. 2 glycoprotein I phospholipid-binding site. Implications for human fetal loss. J Autoimmun 2012; 38: J209-J215.
12. Gharavi AE, Pierangeli SS, Espinola RG, Liu X, Colden-Stanfield M, Harris EN: Antiphospholipid antibodies induced in mice by immunization with a cytomegalovirus-derived peptide cause thrombosis and activation of endothelial cells in vivo. Arthritis Rheum 2002; 46: 545-552.
13. Gharavi AE, Vega-Ostertag M, Espinola RG, Liu X, Cole L, Cox NT, Romagnoli P, Labat K, Pierangeli SS: Intrauterine fetal death in mice caused by cytomegalovirus derived peptide induced aPL antibodies. Lupus 2004; 13: 17-23.
14. Del Papa N, Sheng YH, Raschi E, Kandiah DA, Tincani A, Khamashta MA, Atsumi T, Hughes GR, Ichikawa K, Koike T, Balestrieri G, Krilis SA, Meroni PL: Human beta 2-glycoprotein I binds to endothelial cells through a cluster of lysine residues that are critical for anionic phospholipid binding and offers epitopes for anti-beta 2-glycoprotein I antibodies. J Immunol 1998; 160: 5572-5578.
15. Di Simone N, Raschi E, Testoni C, Castellani R, D'Asta M, Shi T, Krilis SA, Caruso A, Meroni PL: Pathogenic role of anti-ß2-glycoprotein I antibodies in antiphospholipid associated fetal loss: characterization of ß2-glycoprotein I binding to trophoblast cells and functional effects of anti-ß2-glycoprotein I antibodies in vitro. Ann Rheum Dis 2005; 64: 462-467.
16. Peaceman AM, Rehnberg KA: The effect of immunoglobulin G fractions from patients with lupus anticoagulant on placental prostacyclin and thromboxane production. Am J Obstet Gynecol 1993; 169: 1403-1406.
17. Nayar R, Lage JM: Placental changes in a first trimester missed abortion in maternal systemic lupus erythematosus with antiphospholipid syndrome; a case report and review of the literature. Hum Pathol 1996; 27: 201-206.
18. Rand JH, Wu XX, Quinn AS, Taatjes DJ: The annexin A5-mediated pathogenic mechanism in the antiphospholipid syndrome: role in pregnancy losses and thrombosis. Lupus 2010; 19: 460-469.
19. Holers VM, Girardi G, Mo L, Guthridge JM, Molina H, Pierangeli SS: Complement C3 activation is required for antiphospholipid antibody-induced fetal loss. J Exp Med 2002; 195: 211-220.
20. Girardi G, Berman J, Redecha P, Spruce L, Thurman JM, Kraus D, Hollmann TJ, Casali P, Caroll MC, Wetsel RA, Lambris JD, Holers VM, Salmon JE: Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J Clin Invest 2003; 112: 1644-1654.
21. Berman J, Girardi G, Salmon JE: TNF-α is a critical effector and a target for therapy in antiphospholipid antibody-induced pregnancy loss. J Immunol 2005; 174: 485-490.
22. Di Simone N, Meroni PL, D'Asta M, Di Nicuolo F, D'Alessio MC, Caruso A: Pathogenic role of anti-beta2-glycoprotein I antibodies on human placenta: functional effects related to implantation and roles of heparin. Hum Reprod Update 2007; 13: 189-196.
23. Meroni PL, Tedesco F, Locati M, Vecchi A, Di Simone N, Acaia B, Pierangeli SS, Borghi MO: Anti-phospholipid antibody mediated fetal loss: still an open question from a pathogenic point of view. Lupus 2010; 19: 453-456.
24. Di Simone N, Marana R, Castellani R, Di Nicuolo F, D'Alessio MC, Raschi E, Borghi MO, Chen PP, Sanguinetti M, Caruso A, Meroni PL: Decreased expression of heparin-binding epidermal growth factor-like growth factor as a newly identified pathogenic mechanism of antiphospholipid-mediated defective placentation. Arthr Rheum 2010; 62: 1504-1512.
25. Di Simone N, Di Nicuolo F, D'Ippolito S, Castellani R, Tersigni C, Caruso A, Meroni P, Marana R: Antiphospholipid antibodies affect human endometrial angiogenesis. Biol Reprod 2010; 83: 212-219.
26. Huppertz B, Peeters LL: Vascular biology in implantation and placentation. Angiogenesis 2005; 8: 157-167.
27. Reynolds LP, Borowicz PP, Caton JS, Vonnahme KA, Luther JS, Buchanan DS, Hafez SA, Grazul-Bilska AT, Redmer DA: Uteroplacental vascular development and placental function: an update. Int J Dev Biol 2010; 54: 355-366.
28. Cullinan-Bove K, Koos R: Vascular endothelial growth factor/vascular permeability factor expression in the rat uterus: rapid stimulation by estrogen correlates with estrogen-induced increases in uterine capillary permeability and growth. Endocrinol 1993; 133: 829-837.
29. Chrzanowska-Wodnicka M, Kraus AE, Gale D: Defective angiogenesis, endothelial migration, proliferation, and MAPK signaling in Rap1b-deficient mice. Blood 2008; 111: 2647-2656.
30. Zhu M, Olee T, Le DT, Roubey RA, Hahn BH, Woods VL Jr, Chen PP: Characterization of IgG monoclonal anti-cardiolipin/anti-β2GPI antibodies from two patients with the anti-phospholipid syndrome reveals three species of antibodies. Br J Haematol 1999; 105: 102-109.
31. Kupai K, Szucs G, Cseh S, Hajdu I, Csonka C, Csont T, Ferdinandy P: Matrix metalloproteinase activity assays: Importance of zymography. J Pharmacol Toxicol Methods 2010; 61: 205-209.
32. Burbridge MF, Coge′ F, Galizzi JP, Boutin JA, West DC, Tucker DC: The role of the matrix metalloproteinases during in vitro vessel formation. Angiogenesis 2002; 5: 215-226.
33. Moon DO, Choi YH, Moon SK, Kim WJ, Kim GY: Butein suppresses the expression of nuclear factor-kappa B-mediated matrix metalloproteinase-9 and vascular endothelial growth factor in prostate cancer cells. Toxicol In Vitro 2010; 24: 1927-1934.
34. Buteau-Lozano H, Ancelin M, Lardeux B, Milanini J, Perrot-Applanat M: Transcriptional regulation of vascular endothelial growth factor by estradiol and tamoxifen in breast cancer cells: a complex interplay between estrogen receptors m and β. Cancer Res 2002; 62: 4977-4984.
35. Rhee JW, Lee KW, Sohn WJ, Lee Y, Jeon OH, Kwon H, Kim DS: Regulation of matrix metalloproteinase-9 and cell migration by NF-kappa B in response to CpG-oligodeoxynucleotides in RAW 264.7 cells. Mol Immunol 2007; 44: 1393-1400.
36. Zhou WH, Du MR, Dong L, Zhu XY, Yang JY, He YY, Li DJ: Cyclosporin A increases expression of matrix metalloproteinase 9 and 2 and invasiveness in vitro of the first-trimester human trophoblast cells via the mitogen-activated protein kinase pathway. Hum Reprod 2007; 22: 2743-2750.
37. Kim HN, Kim H, Kong JM, Bae S, Kim YS, Lee N, Cho BJ, Lee SK, Kim HR, Hwang YI, Kang JS, Lee WJ: Vitamin C down-regulates VEGF production in B16F10 murine melanoma cells via the suppression of p42/44 MAPK activation. J Cell Biochem 2011; 112: 894-901.
38. Mak IY, Brosens JJ, Christian M, Hills FA, Chamley L, Regan L, White JO: Regulated expression of signal transducer and activator of transcription, Stat5, and its enhancement of PRL expression in human endometrial stromal cells in vitro. J Clin Endocrinol Metab 2002; 87: 2581-2588.
39. Tincani A, Andreoli L, Chighizola C, Tincani A, Andreoli L, Chighizola C, Meroni PL: The interplay between the antiphospholipid syndrome and systemic lupus erythematosus. Autoimmunity 2009; 42: 257-259.
40. Pierangeli SS, Liu X, Espinola R, Olee T, Zhu M, Harris NE, Chen PP: Functional analyses of patient-derived IgG monoclonal anticardiolipin antibodies using in vivo thrombosis and in vivo microcirculation models. Thromb Haemost 2000; 84: 388-395.
41. Cowchock FS, Reece EA, Balaban D, Branch DW, Plouffe L: Repeated fetal losses associated with antiphospholipid antibodies: a collaborative randomized trial comparing prednisone with low-dose heparin treatment. Am J Obstet Gynecol 1992; 166: 1318-1323.
42. Bramham K, Thomas M, Nelson-Piercy C, Khamashta M, Hunt BJ: First-trimester low-dose prednisolone in refractory antiphospholipid antibody-related pregnancy loss. Blood 2011; 117: 6948-6951.
43. Ziakas PD, Pavlou M, Voulgarelis M: Heparin treatment in antiphospholipid syndrome with recurrent pregnancy loss: a systematic review and meta-analysis. Obstet Gynecol 2010; 115: 1256-1262.
44. Rovere-Querini P, Canti V, Mosca M, Mitic G, Bertero MT, Pengo V, Boffa MC, Tincani A: Risk factors for pregnancy failure in patients with anti-phospholipid syndrome treated with conventional therapies: a multicentre, case-control study. Rheumatology 2011; 50: 1684-1689.