Quantification of the Predominant Immune Cell Populations in Decidua Throughout Human Pregnancy

American Journal of Reproductive Immunology

Volumn 71, Issue 2, 2014, Pages 109-119

  Bartmann, Catharina ^a   Segerer, Sabine E ^b   Rieger, Lorenz ^c   Kapp, Michaela ^a   Sütterlin, Marc ^d   Kämmerer, Ulrike ^a  

^a UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^b ENDOKRINOLOGIKUM HAMBURG   (Germany)

^c Krankenhaus Landshut Achdorf   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Course of pregnancy; Decidua; Flow cytometry; Immune cells

Indexed keywords

CD16 ANTIGEN; CD19 ANTIGEN; CD209 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD56 ANTIGEN; CD8 ANTIGEN; HLA DR ANTIGEN;

ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CELL POPULATION; CELL SUSPENSION; DECIDUA; FEMALE; FIRST TRIMESTER PREGNANCY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GAMMA DELTA T LYMPHOCYTE; GESTATIONAL AGE; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; LEUKOCYTE COUNT; MAJOR CLINICAL STUDY; NATURAL KILLER CELL; PREGNANCY; PRIORITY JOURNAL; UNWANTED PREGNANCY; CELL SEPARATION; CELLULAR IMMUNITY; DENDRITIC CELL; IMMUNOLOGY; METABOLISM; MONOCYTE; T LYMPHOCYTE; TIME;

ANTIGENS, CD45; CELL SEPARATION; DECIDUA; DENDRITIC CELLS; FEMALE; FLOW CYTOMETRY; GESTATIONAL AGE; HUMANS; IMMUNITY, CELLULAR; KILLER CELLS, NATURAL; MONOCYTES; PREGNANCY; T-LYMPHOCYTES; TIME FACTORS;

EID: 84892419056     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12185     Document Type: Article

References (44)

1. Soderstrom-Anttila V: Pregnancy and child outcome after oocyte donation. Hum Reprod Update 2001; 7:28-32.
2. Bansal AS: Joining the immunological dots in recurrent miscarriage. Am J Reprod Immunol 2010; 64:307-315.
3. 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.
4. Rieger L, Segerer S, Bernar T, Kapp M, Majic M, Morr AK, Dietl J, Kammerer U: Specific subsets of immune cells in human decidua differ between normal pregnancy and preeclampsia-a prospective observational study. Reprod Biol Endocrinol 2009; 7:132.
5. Starkey PM, Sargent IL, Redman CW: Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry. Immunology 1988; 65:129-134.
6. Maruyama T, Makino T, Sugi T, Matsubayashi H, Ozawa N, Nozawa S: Flow-cytometric analysis of immune cell populations in human decidua from various types of first-trimester pregnancy. Hum Immunol 1992; 34:212-218.
7. Kalkunte S, Chichester CO, Gotsch F, Sentman CL, Romero R, Sharma S: Evolution of non-cytotoxic uterine natural killer cells. Am J Reprod Immunol 2008; 59:425-432.
8. King A, Balendran N, Wooding P, Carter NP, Loke YW: CD3- leukocytes present in the human uterus during early placentation: phenotypic and morphologic characterization of the CD56 + + population. Dev Immunol 1991; 1:169-190.
9. Loke YW, King A, Burrows TD: Decidua in human implantation. Hum Reprod 1995; 10(Suppl 2):14-21.
10. Moffett-King A: Natural killer cells and pregnancy. Nat Rev Immunol 2002; 2:656-663.
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, Yutkin 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.
12. Robson A, Harris LK, Innes BA, Lash GE, Aljunaidy MM, Aplin JD, Baker PN, Robson SC, Bulmer JN: Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB J 2012; 26:4876-4885.
13. Park DW, Lee HJ, Park CW, Hong SR, Kwak-Kim J, Yang KM: Peripheral blood NK cells reflect changes in decidual NK cells in women with recurrent miscarriages. Am J Reprod Immunol 2010; 63:173-180.
14. 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.
15. Mor G, Cardenas I, Abrahams V, Guller S: Inflammation and pregnancy: the role of the immune system at the implantation site. Ann N Y Acad Sci 2011; 1221:80-87.
16. Exley MA, Boyson JE: Protective role of regulatory decidual γδ T cells in pregnancy. Clin Immunol 2011; 141:236-239.
17. Fan DX, Duan J, Li MQ, Xu B, Li DJ, Jin LP: The decidual gamma-delta T cells up-regulate the biological functions of trophoblasts via IL-10 secretion in early human pregnancy. Clin Immunol 2011; 141:284-292.
18. Mjosberg J, Berg G, Jenmalm MC, Ernerudh J: FOXP3+ regulatory T cells and T helper 1, T helper 2, and T helper 17 cells in human early pregnancy decidua. Biol Reprod 2010; 82:698-705.
19. Trundley A, Moffett A: Human uterine leukocytes and pregnancy. Tissue Antigens 2004; 63:1-12.
20. Rieger L, Honig A, Sutterlin M, Kapp M, Dietl J, Ruck P, Kammerer U: Antigen-presenting cells in human endometrium during the menstrual cycle compared to early pregnancy. J Soc Gynecol Investig 2004; 11:488-493.
21. Sundberg EJ, Deng L, Mariuzza RA: TCR recognition of peptide/MHC class II complexes and superantigens. Semin Immunol 2007; 19:262-271.
22. McIntire RH, Ganacias KG, Hunt JS: Programming of human monocytes by the uteroplacental environment. Reprod Sci 2008; 15:437-447.
23. Kammerer U, Schoppet M, McLellan AD, Kapp M, Huppertz HI, Kampgen E, Dietl J: Human decidua contains potent immunostimulatory CD83(+) dendritic cells. Am J Pathol 2000; 157:159-169.
24. Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TB, Dietl J, van KY, Kampgen E: Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am J Pathol 2003; 162:887-896.
25. Blois SM, Kammerer U, Alba SC, Tometten MC, Shaikly V, Barrientos G, Jurd R, Rukavina D, Thomson AW, Klapp BF, Fernandez N, Arck PC: Dendritic cells: key to fetal tolerance? Biol Reprod 2007; 77:590-598.
26. 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.
27. Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel L, Hassan S: The role of inflammation and infection in preterm birth. Semin Reprod Med 2007; 25:21-39.
28. Goldenberg RL, Hauth JC, Andrews WW: Intrauterine infection and preterm delivery. N Engl J Med 2000; 342:1500-1507.
29. Barton JR, Sibai BM: Severe sepsis and septic shock in pregnancy. Obstet Gynecol 2012; 120:689-706.
30. Saji F, Samejima Y, Kamiura S, Sawai K, Shimoya K, Kimura T: Cytokine production in chorioamnionitis. J Reprod Immunol 2000; 47:185-196.
31. Holm S: A simple sequentially rejective multiple test procedure. Scand J Statistics 1979; 6:65-70.
32. Chaouat G: The Th1/Th2 paradigm: still important in pregnancy? Semin Immunopathol 2007; 29:95-113.
33. Sindram-Trujillo AP, Scherjon SA, van Hulst-van Miert PP, van Schip JJ, Kanhai HH, Roelen DL, Claas FH: Differential distribution of NK cells in decidua basalis compared with decidua parietalis after uncomplicated human term pregnancy. Hum Immunol 2003; 64:921-929.
34. Male V, Sharkey A, Masters L, Kennedy PR, Farrell LE, Moffett A: The effect of pregnancy on the uterine NK cell KIR repertoire. Eur J Immunol 2011; 41:3017-3027.
35. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D: Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 1991; 6:791-798.
36. Haller H, Radillo O, Rukavina D, Tedesco F, Candussi G, Petrovic O, Randic L: An immunohistochemical study of leucocytes in human endometrium, first and third trimester basal decidua. J Reprod Immunol 1993; 23:41-49.
37. 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.
38. Tirado-Gonzalez I, Munoz-Fernandez R, Prados A, Leno-Duran E, Martin F, Abadia-Molina AC, Olivares EG: Apoptotic DC-SIGN+ cells in normal human decidua. Placenta 2012; 33:257-263.
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.
40. Gomez-Lopez N, Vega-Sanchez R, Castillo-Castrejon M, Romero R, Cubeiro-Arreola K, Vadillo-Ortega F: Evidence for a role for the adaptive immune response in human term parturition. Am J Reprod Immunol 2013; 69:212-230.
41. Szekeres-Bartho J, Faust Z, Varga P, Szereday L, Kelemen K: The immunological pregnancy protective effect of progesterone is manifested via controlling cytokine production. Am J Reprod Immunol 1996; 35:348-351.
42. Szekeres-Bartho J, Barakonyi A, Par G, Polgar B, Palkovics T, Szereday L: Progesterone as an immunomodulatory molecule. Int Immunopharmacol 2001; 1:1037-1048.
43. Steinborn A, Kuhnert M, Halberstadt E: Immunomodulating cytokines induce term and preterm parturition. J Perinat Med 1996; 24:381-390.
44. Steinborn A, Gunes H, Roddiger S, Halberstadt E: Elevated placental cytokine release, a process associated with preterm labor in the absence of intrauterine infection. Obstet Gynecol 1996; 88:534-539.