Persistence of decidual NK cells and KIR genotypes in healthy pregnant and preeclamptic women: A case-control study in the third trimester of gestation

Reproductive Biology and Endocrinology

Volumn 9, Issue , 2011, Pages

  Sánchez Rodríguez, Elly N ^a   Nava Salazar, Sonia ^a   Mendoza Rodríguez, C Adriana ^a   Moran, Carlos ^b   Romero Arauz, Juan F ^b   Ortega, Enrique ^c   Granados, Julio ^d   Cervantes Peredo, Alicia ^e   Cerbón, Marco ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^c INSTITUTO DE INVESTIGACIONES BIOMÉDICAS   (Mexico)

^d INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^e HOSPITAL GENERAL DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD3 ANTIGEN; CD56 ANTIGEN; CD9 ANTIGEN; CELL SURFACE MARKER; GENOMIC DNA; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR;

ARTICLE; CASE CONTROL STUDY; CESAREAN SECTION; CONTROLLED STUDY; DECIDUA; FEMALE; FIRST TRIMESTER PREGNANCY; FLOW CYTOMETRY; GENE FREQUENCY; GENOTYPE; GESTATIONAL AGE; HUMAN; HUMAN CELL; HUMAN TISSUE; LEUKOCYTE; MAJOR CLINICAL STUDY; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PREECLAMPSIA; PREGNANCY; SAMPLING; THIRD TRIMESTER PREGNANCY; CYTOLOGY; IMMUNOLOGY; METABOLISM; PATHOLOGY;

CASE-CONTROL STUDIES; DECIDUA; FEMALE; FLOW CYTOMETRY; HUMANS; KILLER CELLS, NATURAL; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY TRIMESTER, THIRD; RECEPTORS, KIR;

EID: 78651482474     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-9-8     Document Type: Article

References (46)

1. Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 2006, 27:939-958. 10.1016/j.placenta.2005.12.006, 16490251.
2. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Human Reprod 1991, 6:791-798.
3. King A, Loke YW. On the nature and function of human uterine granular lymphocytes. Immunol Today 1991, 12:432-435. 10.1016/0167-5699(91)90014-K, 1786078.
4. Moffet-King A. Natural killer cells and pregnancy. Nat Rev Immunol 2002, 2:656-663. 10.1038/nri886, 12209134.
5. Abadía-Molina AC, Ruiz C, Montes MJ, King A, Loke YW, Olivares EG. Immune phenotype and cytotoxic activity of lymphocytes from human term decidua against trophoblast. J Reprod Immunol 1996, 31:109-123.
6. Abadía-Molina AC, Ruiz C, King A, Loke YW, Olivares EG. Lymphocytes of human term decidua decrease cell adhesion to a plastic substrate. Hum Reprod 1997, 12:2393-2398.
7. Sindram-Trujillo AP, Scherjon SA, van Hulst-van Miert PP, Kanhai HH, Roelen DL, Claas F. Comparison of decidual leukocytes following spontaneous vaginal delivery and elective cesarean section in uncomplicated human term pregnancy. J Reprod Immunol 2004, 62:125-137. 10.1016/j.jri.2003.11.007, 15288188.
8. Poehlmann TG, Schaumann A, Busch S, Fitzgerald JS, Aguerre-Girr M, Le-Bouteiller P, Schleussner E, Markert UR. Inhibition of term decidual NK cell cytotoxicity by soluble HLA-G1. Am J Reprod Immunol 2006, 56:275-285. 10.1111/j.1600-0897.2006.00420.x, 17076671.
9. Williams PJ, Searle RF, Robson SC, Innes BA, Bulmer JN. Decidual leucocyte populations in early to late gestation normal human pregnancy. J Reprod Immunol 2009, 82:24-31. 10.1016/j.jri.2009.08.001, 19732959.
10. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F, Masch R, Lockwood CJ, Schachter AD, Park PJ, Strominger JL. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med 2003, 198:1202-1212.
11. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yuykin V, Benharroch D, Porgador A, Keshet E, Yagel S, Mandelboim O. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006, 12:1065-1074. 10.1038/nm1452, 16892062.
12. Di Santo JP. Functionally distinct NK-cell subsets: developmental origins and biological implications. Eur J Immunol 2008, 38:2948-2951. 10.1002/eji.200838830, 18979515.
13. Mselle TF, Meadows SK, Eriksson M, Smith JM, Shen L, Wira CR, Sentman CL. Unique characteristics of NK cells throughout the human female reproductive tract. Clin Immunol 2007, 124:69-76. 10.1016/j.clim.2007.04.008, 17524808.
14. Manaster I, Mandelboim O. The unique properties of human NK cells in the uterine mucosa. Placenta 2008, 29(Suppl A):60-66.
15. 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. 10.2353/ajpath.2009.080995, 2671283, 19349361.
16. Stallmach T, Hebisch G, Orban P, Lü X. Aberrant positioning of trophoblast and lymphocytes in the feto-maternal interface with pre-eclampsia. Virchows Arch 1999, 434:207-211. 10.1007/s004280050329, 10190299.
17. Wilczyński JR, Tchórzewski H, Banasik M, Głowacka E, Wieczorek A, Lewkowicz P, Malinowski A, Szpakowski M, Wilczyński J. Lymphocyte subset distribution and cytokine secretion in third trimester decidua in normal pregnancy and preclampsia. Eur J Obstet Gynecol Reprod Biol 2003, 109:8-15.
18. Eide IP, Rolfseng T, Isaksen CV, Mecsei R, Roald B, Lydersen S, Salvesen KA, Harsem NK, Austgulen R. Serious foetal growth restriction is associated with reduced proportions of natural killer cells in decidua basalis. Virchows Arch 2006, 448:269-276. 10.1007/s00428-005-0107-z, 16328353.
19. Rieger L, Segerer S, Bernar T, Kapp M, Majic M, Morr AK, Dietl J, Kämmerer U. Specific subsets of immune cells in human decidua differ between normal pregnancy and preclampsia - a prospective observational study. Reprod Biol Endocrinol 2009, 23:132-142.
20. Williams PJ, Bulmer JN, Searle RF, Innes BA, Robson SC. Altered decidual leucocyte populations in the placental bed in pre-eclampsia and foetal growth restriction: a comparison with late normal pregnancy. Reproduction 2009, 138:177-184. 10.1530/REP-09-0007, 19357130.
21. Khong TY. Immunohistologic study of the leukocytic infiltrate in maternal uterine tissues in normal and preeclamptic pregnancies at term. Am J Reprod Immunol Microbiol 1987, 15:1-8.
22. Trowsdale J, Barten R, Haude A, Stewart AC, Beck S, Wilson M. The genomic context of Natural Killer receptor extended gene families. Immunol Rev 2001, 181:20-38. 10.1034/j.1600-065X.2001.1810102.x, 11513141.
23. Bashirova A, Martin P, Mc Vicar W, Carrington M. The killer immunoglobulin like receptor gene cluster: Tuning the genome for defense. Annu Rev Genomics Hum Genet 2006, 7:277-300. 10.1146/annurev.genom.7.080505.115726, 16824023.
24. Carrington M, Martin MP. The impact of variation at the KIR gene cluster on human disease. Curr Top Microbiol Immunol 2006, 298:225-257. full_text, 16329188.
25. Hiby SE, Walker JJ, O'shaughnessy KM, Redman CW, Carrington M, Trowsdale J, Moffet A. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med 2004, 200:957-965. 10.1084/jem.20041214, 2211839, 15477349.
26. ACOG Committee on Practice Bulletins-Obstetrics ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. Obstet Gynecol 2002, 99:159-167. 10.1016/S0029-7844(01)01747-1, 16175681, ACOG Committee on Practice Bulletins-Obstetrics.
27. Tuffnell DJ, Shennan AH, Waugh JJ, Walker JJ. The management of severe pre-eclampsia/eclampsia. RCOG Guidelines 2006, Guideline 10(A):1-11.
28. Romero-Arauz JF. Epidemiología, clasificación y factores de riesgo en preeclampsia. Preeclampsia. Enfermedades hipertensivas del embarazo 2009, 1-15. Mexico: McGrawHill.
29. Arcuri F, Cintorino M, Carducci A, Papa S, Riparbelli MG, Mangioni S, Di Blasio AM, Tosi P, Viganò P. Human decidual natural killer cells as a source and target of macrophage migration inhibitory factor. Reproduction 2006, 131:175-182. 10.1530/rep.1.00857, 16388020.
30. King A, Burrows T, Verma S, Hiby S, Loke YW. Human uterine lymphocytes. Hum Reprod Update 1998, 4:480-485. 10.1093/humupd/4.5.480, 10027599.
31. Redman CW, Sargent IL. Pre-eclampsia, the placenta and the maternal systemic inflammatory response--a review. Placenta 2003, 24(Suppl A):21-27.
32. Borzychowski AM, Croy BA, Chan WL, Redman CW, Sargent IL. Changes in systemic type 1 and type 2 immunity in normal pregnancy and pre-eclampsia may be mediated by natural killer cells. Eur J Immunol 2005, 35:3054-3063. 10.1002/eji.200425929, 16134082.
33. Haller H, Radillo O, Rukavina D, Tedesco F, Candussi G, Petrović O, Randić L. An immunohistochemical study of leucocytes in human endometrium, first and third trimester basal decidua. J Reprod Immunol 1993, 23:41-49. 10.1016/0165-0378(93)90025-D, 8429523.
34. Vargas ML, Sántos JL, Ruiz C, Montes MJ, Alemán P, García-Tortosa C, García-Olivares E. Comparison of the proportions of leukocytes in early and term decidua. Am J Reprod Immunol 1993, 29:135-140.
35. Hirano T, Higuchi T, Ueda M, Inoue T, Kataoka N, Maeda M, Fujiwara H, Fujii S. CD9 is expressed in extravillous trhophoblast in association with integrin alpha3 and integrin alpha5. Mol Hum Reprod 1999, 5:162-167. 10.1093/molehr/5.2.162, 10065872.
36. Tohami T, Drucker L, Radnay J, Shapira H, Lishner M. Expression of tetraspanins in peripheral blood leukocytes: a comparison between normal and infectious conditions. Tissue Antigens 2004, 64:235-242. 10.1111/j.1399-0039.2004.00271.x, 15304003.
37. Waterhouse R, Ha C, Devksler GS. Murine CD9 is the receptor for pregnancy-specific glycoprotein 17. J Exp Med 2002, 195:277-282. 10.1084/jem.20011741, 2193606, 11805154.
38. Wilczyński JR, Tchórzewski H, Głowacka E, Banasik M, Lewkowicz P, Szpakowski M, Zeman K, Wilczyński J. Cytokine secretion by decidual lymphocytes in transient hypertension of pregnancy and pre-eclampsia. Mediators Inflamm 2002, 11:105-111. 1781645, 12061422.
39. Sasaki Y, Darmochwal-Kolarz D, Suzuki D, Sakai M, Ito M, Shima T, Shiozaki A, Rolinski J, Saito S. Proportion of peripherals blood and decidual CD4(+) CD25(bright) regulatory T cells in pre-eclampsia. Clin Exp Immunol 2007, 149:139-145. 10.1111/j.1365-2249.2007.03397.x, 1942015, 17459078.
40. Gutiérrez-Rodríguez ME, Sandoval-Ramírez L, Díaz-Flores M, Marsh SG, Valladares-Salgado A, Madrigal JA, Mejía-Aranguere JM, García CA, Huerta-Zepeda A, Ibarra-Cortés B, Ortega-Camarillo C, Cruz M. KIR gene in ethnic and Mestizo populations from Mexico. Hum Immunol 2006, 67:85-93.
41. Contreras G, Aláez C, Murguía A, García D, Flores H, Gorodezky C. Distribution of the killer cell immunoglobulin-like receptors in Mexican Mestizos. Tissue Antigens 2007, 69(Suppl 1):125-129. 10.1111/j.1399-0039.2006.76212.x, 17445185.
42. Flores AC, Marcos CY, Paladino N, Arruvito L, Williams F, Middleton D, Fainboim L. KIR receptors and HLA-C in the maintenance of pregnancy. Tissue Antigens 2007, 69(Suppl 1):112-113. 10.1111/j.1399-0039.2006.762_8.x, 17445181.
43. Saito S, Takeda Y, Sakai M, Nakabayahi M, Hayakawa S. The incidence of pre-eclampsia among couples consisting of Japanese women and Caucasian men. J Reprod Immunol 2006, 70:93-98. 10.1016/j.jri.2005.12.005, 16427138.
44. Borzychowsky AM, Croy BA, Chan WL, Redman CW, Sargent IL. Changes in systemic type 1 and type 2 immunity in normal pregnancy and pre-eclampsia may be mediated by natural killer cells. Eur J Immunol 2005, 35:3054-3063. 10.1002/eji.200425929, 16134082.
45. Tilburgs T, van der Mast BJ, Nagtzaam NM, Roelen DL, Scherjon SA, Claas FH. Expression of NK cell receptor son decidual T cells in human pregnancy. J Reprod Immunol 2009, 80:22-32. 10.1016/j.jri.2009.02.004, 19394706.
46. Sharkey AM, Gardner L, Hiby S, Farrell L, Apps R, Masters L, Goodridge J, Lathbury L, Stewart CA, Verma S, Moffett A. Killer-Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age. J Immunol 2008, 181:39-46.