Increased angiogenic factor secretion by decidual natural killer cells from pregnancies with high uterine artery resistance alters trophoblast function

Human Reproduction

Volumn 29, Issue 4, 2014, Pages 652-660

  Wallace, A E ^a   Fraser, R ^a   Gurung, S ^a   Goulwara, S S ^a   Whitley, G S ^a   Johnstone, A P ^a   Cartwright, J E ^a  

^a ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

Angiogenin; Decidua; Endostatin; Natural killer cell; Pre eclampsia

Indexed keywords

ANGIOGENIN; ENDOSTATIN; INTERLEUKIN 2 RECEPTOR; PLACENTAL GROWTH FACTOR; ANGIOGENIC FACTOR; PANCREATIC RIBONUCLEASE; PLACENTA PROTEIN;

ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DECIDUA; EMBRYO; FEMALE; FIRST TRIMESTER PREGNANCY; HIGH RISK PREGNANCY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; NATURAL KILLER CELL; PREECLAMPSIA; PREGNANCY TERMINATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; TIME-LAPSE VIDEO MICROSCOPY; TROPHOBLAST; UTERINE ARTERY; VASCULAR RESISTANCE; WESTERN BLOTTING; ADULT; ARTERIAL PRESSURE; BLOOD FLOW; CELL LINE; CYTOLOGY; ECHOGRAPHY; METABOLISM; PHYSIOLOGY; PREGNANCY; SECRETION (PROCESS); SIGNAL TRANSDUCTION; VASCULARIZATION;

ADULT; ANGIOGENESIS INDUCING AGENTS; ARTERIAL PRESSURE; CELL LINE; DECIDUA; ENDOSTATINS; FEMALE; HUMANS; KILLER CELLS, NATURAL; PREGNANCY; PREGNANCY PROTEINS; PREGNANCY TRIMESTER, FIRST; RECEPTORS, INTERLEUKIN-2; REGIONAL BLOOD FLOW; RIBONUCLEASE, PANCREATIC; SIGNAL TRANSDUCTION; TROPHOBLASTS; UTERINE ARTERY;

EID: 84898979648     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deu017     Document Type: Article

References (46)

1. Anderson UD, Olsson MG, Kristensen KH, Akerstrom B, Hansson SR. Review: Biochemical markers to predict preeclampsia. Placenta 2012; 33(Suppl):S42-S47.
2. Ashton SV, Whitley GS, Dash PR, Wareing M, Crocker IP, Baker PN, Cartwright JE. Uterine spiral artery remodeling involves endothelial apoptosis induced by extravillous trophoblasts through Fas/FasL interactions. Arterioscler Thromb Vasc Biol 2005;25:102-108.
3. Athanassiades A, Lala PK. Role of placenta growth factor (PIGF) in human extravillous trophoblast proliferation, migration and invasiveness. Placenta 1998;19:465-473. (Pubitemid 28429999)
4. Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of pre-eclampsia. J Pathol 1970;101:Pvi
5. Cartwright JE, Holden DP, Whitley GS. Hepatocyte growth factor regulates human trophoblast motility and invasion: A role for nitric oxide. Br J Pharmacol 1999;128:181-189.
6. Choy MY, Manyonda IT. The phagocytic activity of human first trimester extravillous trophoblast. Hum Reprod 1998;13:2941-2949. (Pubitemid 28482755)
7. Desai J, Holt-Shore V, Torry RJ, Caudle MR, Torry DS. Signal transduction and biological function of placenta growth factor in primary human trophoblast. Biol Reprod 1999;60:887-892. (Pubitemid 29149373)
8. Engert S, Rieger L, Kapp M, Becker JC, Dietl J, Kammerer U. Profiling chemokines, cytokines and growth factors in human early pregnancy decidua by protein array. Am J Reprod Immunol 2007;58:129-137. (Pubitemid 47097379)
9. Fraser R, Whitley GS, Johnstone AP, Host AJ, Sebire NJ, Thilaganathan B, Cartwright JE. Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance. J Pathol 2012;228:322-332.
10. Furuya M, Kurasawa K, Nagahama K, Kawachi K, Nozawa A, Takahashi T, Aoki I. Disrupted balance of angiogenic and antiangiogenic signalings in preeclampsia. J Pregnancy 2011;2011:123717.
11. Gao X, Xu Z. Mechanisms of action of angiogenin. Acta Biochim Biophys Sin 2008;40:619-624. (Pubitemid 352009084)
12. Grant I, Cartwright JE, Lumicisi B, Wallace AE, Whitley GS. Caffeine inhibits EGF-stimulated trophoblast cell motility through the inhibition of mTORC2 and Akt. Endocrinology 2012;153:4502-4510.
13. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006;12:1065-1074. (Pubitemid 44353388)
14. Harris LK, Smith SD, Keogh RJ, Jones RL, Baker PN, Knofler M, Cartwright JE, Whitley GS, Aplin JD. Trophoblast- and vascular smooth muscle cell-derived MMP-12 mediates elastolysis during uterine spiral artery remodeling. Am J Pathol 2010;177:2103-2115.
15. Hu Y, Eastabrook G, Tan R, MacCalman CD, Dutz JP, von Dadelszen P. Decidual NK cell-derived conditioned medium enhances capillary tube and network organization in an extravillous cytotrophoblast cell line. Placenta 2010;31:213-221.
16. Jovanovic M, Stefanoska I, Radojcic L, Vicovac L. Interleukin-8 (CXCL8) stimulates trophoblast cell migration and invasion by increasing levels of matrix metalloproteinase (MMP)2 and MMP9 and integrins alpha5 and beta1. Reproduction 2010;139:789-798.
17. Karamouzis MV, Moschos SJ. The use of endostatin in the treatment of solid tumors. Expert Opin Biol Ther 2009;9:641-648.
18. Keogh RJ, Harris LK, Freeman A, Baker PN, Aplin JD, Whitley GS, Cartwright JE. Fetal-derived trophoblast use the apoptotic cytokine tumor necrosis factor-alpha-related apoptosis-inducing ligand to induce smooth muscle cell death. Circ Res 2007;100:834-841. (Pubitemid 46555688)
19. Kim YM, Hwang S, Pyun BJ, Kim TY, Lee ST, Gho YS, Kwon YG. Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J Biol Chem 2002; 277:27872-27879. (Pubitemid 34966733)
20. King A, Burrows T, Verma S, Hiby S, LokeYW. Human uterine lymphocytes. Hum Reprod Update 1998;4:480-485.
21. King A, Gardner L, Loke YW. Co-stimulation of human decidual natural killer cells by interleukin-2 and stromal cells. Hum Reprod 1999; 14:656-663. (Pubitemid 29131241)
22. Koga K, Osuga Y, Tsutsumi O, Yano T, Yoshino O, Takai Y, Matsumi H, Hiroi H, Kugu K, Momoeda M et al. Demonstration of angiogenin in human endometrium and its enhanced expression in endometrial tissues in the secretory phase and the decidua. J Clin Endocrinol Metab 2001; 86:5609-5614. (Pubitemid 33070295)
23. LaMarca HL, Dash PR, Vishnuthevan K, Harvey E, Sullivan DE, Morris CA, Whitley GS. Epidermal growth factor-stimulated extravillous cytotrophoblast motility is mediated by the activation of PI3-K, Akt and both p38 and p42/44 mitogen-activated protein kinases. Hum Reprod 2008;23:1733-1741.
24. Lash GE, Schiessl B, Kirkley M, Innes BA, Cooper A, Searle RF, Robson SC, Bulmer JN. Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J Leukoc Biol 2006; 80:572-580. (Pubitemid 44835791)
25. Meekins JW, Pijnenborg R, Hanssens M, McFadyen IR, van Asshe A. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol 1994; 101:669-674. (Pubitemid 24251519)
26. Melchiorre K, Wormald B, Leslie K, Bhide A, Thilaganathan B. First-trimester uterine artery Doppler indices in term and preterm pre-eclampsia. Ultrasound Obstet Gynecol 2008;32:133-137.
27. Moroianu J, Riordan JF. Nuclear translocation of angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc Natl Acad Sci USA 1994;91:1677-1681. (Pubitemid 24080268)
28. Murphy SP, Tayade C, Ashkar AA, Hatta K, Zhang J, Croy BA. Interferon gamma in successful pregnancies. Biol Reprod 2009;80:848-859.
29. Nasu K, Nishida M, Fukuda J, Kawano Y, Nishida Y, Miyakawa I. Hypoxia simultaneously inhibits endostatin production and stimulates vascular endothelial growth factor production by cultured human endometrial stromal cells. Fertil Steril 2004;82:756-759. (Pubitemid 39243208)
30. Pijnenborg R, Anthony J, Davey DA, Rees A, Tiltman A, Vercruysse L, van Assche A. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 1991;98:648-655.
31. Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: Facts and controversies. Placenta 2006;27:939-958. (Pubitemid 44204033)
32. Pollheimer J, Bauer S, Huber A, Husslein P, Aplin JD, Knofler M. Expression pattern of collagen XVIII and its cleavage product, the angiogenesis inhibitor endostatin, at the fetal-maternal interface. Placenta 2004; 25:770-779. (Pubitemid 39276942)
33. Pollheimer J, Haslinger P, Fock V, Prast J, Saleh L, Biadasiewicz K, Jetne-Edelmann R, Haraldsen G, Haider S, Hirtenlehner-Ferber K et al. Endostatin suppresses IGF-II-mediated signaling and invasion of human extravillous trophoblasts. Endocrinology 2011;152:4431-4442.
34. Prefumo F, Sebire NJ, Thilaganathan B. Decreased endovascular trophoblast invasion in first trimester pregnancies with high-resistance uterine artery Doppler indices. Hum Reprod 2004;19:206-209. (Pubitemid 38072033)
35. Prefumo F, Fratelli N, Ganapathy R, Bhide A, Frusca T, Thilaganathan B. First trimester uterine artery Doppler in women with previous pre-eclampsia. Acta Obstet Gynecol Scand 2008;87:1271-1275.
36. Rajashekhar G, Loganath A, Roy AC, Chong SS, Wong YC. Hypoxia up-regulated angiogenin and down-regulated vascular cell adhesion molecule-1 expression and secretion in human placental trophoblasts. J Soc Gynecol Investig 2005;12:310-319. (Pubitemid 40848454)
37. Rehn M, Veikkola T, Kukk-Valdre E, Nakamura H, Ilmonen M, Lombardo C, Pihlajaniemi T, Alitalo K, Vuori K. Interaction of endostatin with integrins implicated in angiogenesis. Proc Natl Acad Sci USA 2001;98:1024-1029. (Pubitemid 32121180)
38. Santoni A, Zingoni A, Cerboni C, Gismondi A. Natural killer (NK) cells from killers to regulators: Distinct features between peripheral blood and decidual NK cells. Am J Reprod Immunol 2007;58:280-288. (Pubitemid 47249066)
39. Scaife PJ, Bulmer JN, Robson SC, Innes BA, Searle RF. Effector activity of decidual CD8+ T lymphocytes in early human pregnancy. Biol Reprod 2006;75:562-567. (Pubitemid 44465797)
40. Smith SD, Dunk CE, Aplin JD, Harris LK, Jones RL. Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy. Am J Pathol 2009;174:1959-1971.
41. Treiber-Held S, Stewart DM, Kurman CC, Nelson DL. IL-15 induces the release of soluble IL-2Ralpha from human peripheral blood mononuclear cells. Clin Immunol Immunopathol 1996;79:71-78. (Pubitemid 26151410)
42. Verma S, Hiby SE, Loke YW, King A. Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol Reprod 2000;62:959-968. (Pubitemid 30173809)
43. Wallace AE, Fraser R, Cartwright JE. Extravillous trophoblast and decidual natural killer cells: A remodelling partnership. Hum Reprod Update 2012; 18:458-471.
44. Wallace AE, Host AJ, Whitley GS, Cartwright JE. Decidual natural killer cell interactions with trophoblasts are impaired in pregnancies at an increased risk of preeclampsia. Am J Pathol 2013;183: 1853-1861.
45. Wei S, Gao X, Du J, Su J, Xu Z. Angiogenin enhances cell migration by regulating stress fiber assembly and focal adhesion dynamics. PLoS One 2011;6:e28797.
46. Zhou Y, Fisher SJ, Janatpour M, Genbacev O, Dejana E, Wheelock M, Damsky CH. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasioń J Clin Invest 1997;99:2139-2151.