Decidual cell regulation of natural killer cell-recruiting chemokines: Implications for the pathogenesis and prediction of preeclampsia

American Journal of Pathology

Volumn 183, Issue 3, 2013, Pages 841-856

  Lockwood, Charles J ^a   Huang, S Joseph ^a   Chen, Chie Pein ^b   Huang, Yingqun ^c   Xu, Jie ^c   Faramarzi, Saeed ^a   Kayisli, Ozlem ^a   Kayisli, Umit ^a   Koopman, Louise ^d   Smedts, Dineke ^e   Buchwalder, Lynn F ^c   Schatz, Frederick ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b MACKAY MEMORIAL HOSPITAL   (Taiwan)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Celgene Avilomics Research   (United States)

^e ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CXCR3; CXCL11 CHEMOKINE; CYTOKERATIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; VIMENTIN;

ADULT; ARTICLE; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; DECIDUA; FEMALE; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; HUMAN TISSUE; MACROPHAGE; NATURAL KILLER CELL; PATHOGENESIS; PREDICTION; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANTIGENS, CD56; CHEMOKINES; DECIDUA; FEMALE; FLOW CYTOMETRY; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; INTERLEUKINS; KILLER CELLS, NATURAL; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY TRIMESTER, FIRST; RECEPTORS, CHEMOKINE; RECEPTORS, IGG; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84883153997     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.05.029     Document Type: Article

References (59)

1. Y. Zhou, S.J. Fisher, M. Janatpour, O. Genbacev, E. Dejana, M. Wheelock, and C.H. Damsky Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J Clin Invest 99 1997 2139 2151
2. R. Pijnenborg, L. Vercruysse, and I. Brosens Deep placentation Best Pract Res Clin Obstet Gynaecol 25 2011 273 285
3. B.C. Young, R.J. Levine, and S.A. Karumanchi Pathogenesis of preeclampsia Annu Rev Pathol 5 2010 173 192
4. E.A. Steegers, P. von Dadelszen, J.J. Duvekot, and R. Pijnenborg Pre-eclampsia Lancet 376 2010 631 644
5. M. Silasi, B. Cohen, S.A. Karumanchi, and S. Rana Abnormal placentation, angiogenic factors, and the pathogenesis of preeclampsia Obstet Gynecol Clin North Am 37 2010 239 253
6. A. Trundley, and A. Moffett Human uterine leukocytes and pregnancy Tissue Antigens 63 2004 1 12
7. I. Manaster, and O. Mandelboim The unique properties of uterine NK cells Am J Reprod Immunol 63 2010 434 444
8. Y.T. Bryceson, S.C. Chiang, S. Darmanin, C. Fauriat, H. Schlums, J. Theorell, and S.M. Wood Molecular mechanisms of natural killer cell activation J Innate Immun 3 2011 216 226
9. M.A. Caligiuri Human natural killer cells Blood 112 2008 461 469
10. R. Trotta, L. Chen, D. Ciarlariello, S. Josyula, C. Mao, S. Costinean, L. Yu, J.P. Butchar, S. Tridandapani, C.M. Croce, and M.A. Caligiuri miR-155 regulates IFN-gamma production in natural killer cells Blood 119 2012 3478 3485
11. S. Kalkunte, C.O. Chichester, F. Gotsch, C.L. Sentman, R. Romero, and S. Sharma Evolution of non-cytotoxic uterine natural killer cells Am J Reprod Immunol 59 2008 425 432
12. G.E. Lash, S.C. Robson, and J.N. Bulmer Review: Functional role of uterine natural killer (uNK) cells in human early pregnancy decidua Placenta 31 Suppl 2010 S87 S92
13. H.D. Kopcow, and S.A. Karumanchi Angiogenic factors and natural killer (NK) cells in the pathogenesis of preeclampsia J Reprod Immunol 76 2007 23 29
14. M.A. Cooper, T.A. Fehniger, and M.A. Caligiuri The biology of human natural killer-cell subsets Trends Immunol 22 2001 633 640
15. U. Singh, G. Nicholson, B.C. Urban, I.L. Sargent, U. Kishore, and A.L. Bernal Immunological properties of human decidual macrophages: a possible role in intrauterine immunity Reproduction 129 2005 631 637
16. G. Trinchieri Type I interferon: friend or foe? J Exp Med 207 2010 2053 2063
17. L.A. Koopman, H.D. Kopcow, B. Rybalov, J.E. Boyson, J.S. Orange, F. Schatz, R. Masch, C.J. Lockwood, A.D. Schachter, P.J. Park, and J.L. Strominger Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential J Exp Med 198 2003 1201 1212
18. A. Arici, P.B. Marshburn, P.C. MacDonald, and R.A. Dombrowski Progesterone metabolism in human endometrial stromal and gland cells in culture Steroids 64 1999 530 534
19. S.J. Huang, F. Schatz, R. Masch, M. Rahman, L. Buchwalder, T. Niven-Fairchild, C. Tang, V.M. Abrahams, G. Krikun, and C.J. Lockwood Regulation of chemokine production in response to pro-inflammatory cytokines in first trimester decidual cells J Reprod Immunol 72 2006 60 73
20. M. Zhang, S. Guller, and Y. Huang Method to enhance transfection efficiency of cell lines and placental fibroblasts Placenta 28 2007 779 782
21. ACOG Committee on Practice Bulletins - Obstetrics ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002 Obstet Gynecol 99 2002 159 167
22. J.D. Greenwood, K. Minhas, J.P. di Santo, M. Makita, Y. Kiso, and B.A. Croy Ultrastructural studies of implantation sites from mice deficient in uterine natural killer cells Placenta 21 2000 693 702
23. H. He, D.J. McCartney, Q. Wei, S. Esadeg, J. Zhang, R.A. Foster, M.A. Hayes, C. Tayade, F. Van Leuven, and B.A. Croy Characterization of a murine alpha 2 macroglobulin gene expressed in reproductive and cardiovascular tissue Biol Reprod 72 2005 266 275
24. A.A. Ashkar, and B.A. Croy Functions of uterine natural killer cells are mediated by interferon gamma production during murine pregnancy Semin Immunol 13 2001 235 241
25. S. Chantakru, W.C. Wang, M. van den Heuvel, S. Bashar, A. Simpson, Q. Chen, B.A. Croy, and S.S. Evans Coordinate regulation of lymphocyte-endothelial interactions by pregnancy-associated hormones J Immunol 171 2003 4011 4019
26. M.J. Bilinski, J.G. Thorne, M.J. Oh, S. Leonard, C. Murrant, C. Tayade, and B.A. Croy Uterine NK cells in murine pregnancy Reprod Biomed Online 16 2008 218 226
27. M.J. Guimond, B. Wang, and B.A. Croy Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice J Exp Med 187 1998 217 223
28. J. Hanna, O. Wald, D. Goldman-Wohl, D. Prus, G. Markel, R. Gazit, G. Katz, R. Haimov-Kochman, N. Fujii, S. Yagel, A. Peled, and O. Mandelboim CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells Blood 102 2003 1569 1577
29. S.D. Smith, C.E. Dunk, J.D. Aplin, L.K. Harris, and R.L. Jones Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy Am J Pathol 174 2009 1959 1971
30. R. Pijnenborg, L. Vercruysse, and M. Hanssens The uterine spiral arteries in human pregnancy: facts and controversies Placenta 27 2006 939 958
31. C.M. Craven, T. Morgan, and K. Ward Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts Placenta 19 1998 241 252
32. R. Pijnenborg, W.B. Robertson, and I. Brosens The arterial migration of trophoblast in the uterus of the golden hamster, Mesocricetus auratus J Reprod Fertil 40 1974 269 280
33. L. Lynch, L. Golden-Mason, M. Eogan, C. O'Herlihy, and C. O'Farrelly Cells with haematopoietic stem cell phenotype in adult human endometrium: relevance to infertility? Hum Reprod 22 2007 919 926
34. V. Male, T. Hughes, S. McClory, F. Colucci, M.A. Caligiuri, and A. Moffett Immature NK cells, capable of producing IL-22, are present in human uterine mucosa J Immunol 185 2010 3913 3918
35. D.B. Keskin, D.S. Allan, B. Rybalov, M.M. Andzelm, J.N. Stern, H.D. Kopcow, L.A. Koopman, and J.L. Strominger TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells Proc Natl Acad Sci U S A 104 2007 3378 3383
36. D.S. Allan, B. Rybalov, G. Awong, J.C. Zuniga-Pflucker, H.D. Kopcow, J.R. Carlyle, and J.L. Strominger TGF-beta affects development and differentiation of human natural killer cell subsets Eur J Immunol 40 2010 2289 2295
37. T. Yamaguchi, K. Kitaya, N. Daikoku, T. Yasuo, S. Fushiki, and H. Honjo Potential selectin L ligands involved in selective recruitment of peripheral blood CD16(-) natural killer cells into human endometrium Biol Reprod 74 2006 35 40
38. H.Y. Sela, D.S. Goldman-Wohl, R. Haimov-Kochman, C. Greenfield, S. Natanson-Yaron, Y. Hamani, A. Revel, Y. Lavy, O. Singer, N. Yachimovich-Cohen, T. Turetsky, O. Mandelboim, B. Reubinoff, and S. Yagel Human trophectoderm apposition is regulated by interferon gamma-induced protein 10 (IP-10) during early implantation Placenta 34 2013 222 230
39. I.L. Sargent, A.M. Borzychowski, and C.W. Redman NK cells and human pregnancy - an inflammatory view Trends Immunol 27 2006 399 404
40. C. Carlino, H. Stabile, S. Morrone, R. Bulla, A. Soriani, C. Agostinis, F. Bossi, C. Mocci, F. Sarazani, F. Tedesco, A. Santoni, and A. Gismondi Recruitment of circulating NK cells through decidual tissues: a possible mechanism controlling NK cell accumulation in the uterus during early pregnancy Blood 111 2008 3108 3115
41. C.L. Dunn, H.O. Critchley, and R.W. Kelly IL-15 regulation in human endometrial stromal cells J Clin Endocrinol Metab 87 2002 1898 1901
42. S. Verma, S.E. Hiby, Y.W. Loke, and A. King Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15 Biol Reprod 62 2000 959 968
43. W.E. Carson, J.G. Giri, M.J. Lindemann, M.L. Linett, M. Ahdieh, R. Paxton, D. Anderson, J. Eisenmann, K. Grabstein, and M.A. Caligiuri Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor J Exp Med 180 1994 1395 1403
44. H.D. Kopcow, D.S. Allan, X. Chen, B. Rybalov, M.M. Andzelm, B. Ge, and J.L. Strominger Human decidual NK cells form immature activating synapses and are not cytotoxic Proc Natl Acad Sci U S A 102 2005 15563 15568
45. S.S. Kalkunte, T.F. Mselle, W.E. Norris, C.R. Wira, C.L. Sentman, and S. Sharma Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface J Immunol 182 2009 4085 4092
46. J. Hanna, D. Goldman-Wohl, Y. Hamani, I. Avraham, C. Greenfield, S. Natanson-Yaron, D. Prus, L. Cohen-Daniel, T.I. Arnon, I. Manaster, R. Gazit, V. Yutkin, D. Benharroch, A. Porgador, E. Keshet, S. Yagel, and O. Mandelboim Decidual NK cells regulate key developmental processes at the human fetal-maternal interface Nat Med 12 2006 1065 1074
47. J. Hanna, and O. Mandelboim When killers become helpers Trends Immunol 28 2007 201 206
48. C.L. Dunn, R.W. Kelly, and H.O. Critchley Decidualization of the human endometrial stromal cell: an enigmatic transformation Reprod Biomed Online 7 2003 151 161
49. K. Red-Horse, P.M. Drake, and S.J. Fisher Human pregnancy: the role of chemokine networks at the fetal-maternal interface Expert Rev Mol Med 6 11 2004 1 14
50. Horvath CM: The Jak-STAT pathway stimulated by interferon gamma. Sci STKE 2004, 260:tr8. http://dx.doi.org/10.1126/stke.2602004tr8
51. M. Li, Z.M. Wu, H. Yang, and S.J. Huang NFkappaB and JNK/MAPK activation mediates the production of major macrophage- or dendritic cell-recruiting chemokine in human first trimester decidual cells in response to proinflammatory stimuli J Clin Endocrinol Metab 96 2011 2502 2511
52. H. Hagmann, R. Thadhani, T. Benzing, S.A. Karumanchi, and H. Stepan The promise of angiogenic markers for the early diagnosis and prediction of preeclampsia Clin Chem 58 2012 837 845
53. Z. Zhao, K.H. Moley, and A.M. Gronowski Diagnostic potential for miRNAs as biomarkers for pregnancy-specific diseases Clin Biochem 46 2013 953 960
54. C.W. Redman, and I.L. Sargent Immunology of pre-eclampsia Am J Reprod Immunol 63 2010 534 543
55. G.J. Burton, H.W. Yung, T. Cindrova-Davies, and D.S. Charnock-Jones Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia Placenta 30 Suppl A 2009 S43 S48
56. S.J. Huang, C.P. Chen, F. Schatz, M. Rahman, V.M. Abrahams, and C.J. Lockwood Pre-eclampsia is associated with dendritic cell recruitment into the uterine decidua J Pathol 214 2008 328 336
57. Z.M. Wu, H. Yang, M. Li, C.C. Yeh, F. Schatz, C.J. Lockwood, W. Di, and S.J. Huang Pro-inflammatory cytokine-stimulated first trimester decidual cells enhance macrophage-induced apoptosis of extravillous trophoblasts Placenta 33 2012 188 194
58. G.E. Lash, and J.N. Bulmer Do uterine natural killer (uNK) cells contribute to female reproductive disorders? J Reprod Immunol 88 2011 156 164
59. S.E. Hiby, R. Apps, A.M. Sharkey, L.E. Farrell, L. Gardner, A. Mulder, F.H. Claas, J.J. Walker, C.W. Redman, L. Morgan, C. Tower, L. Regan, G.E. Moore, M. Carrington, and A. Moffett Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2 J Clin Invest 120 2010 4102 4110