Immune cell and transcriptomic analysis of the human decidua in term and preterm parturition

Molecular Human Reproduction

Volumn 23, Issue 10, 2017, Pages 708-724

  Rinaldi, S F ^a   Makieva, S ^a   Saunders, P T ^a   Rossi, A G ^a   Norman, J E ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Decidua; Immune; Inflammation; Microarray; Parturition; Preterm labour

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CD19 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD56 ANTIGEN; CD8 ANTIGEN; CELL MARKER; IMMEDIATE EARLY RESPONSE 3 PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; LEUCOCYTE IMMUNOGLOBULIN LIKE RECEPTOR SUBFAMILY A (WITHOUT TM DOMAIN) MEMBER 3; MACROPHAGE RECEPTOR WITH COLLAGENOUS STRUCTURE; MESSENGER RNA; PROSTAGLANDIN ENDOPEROXIDE SYNTHASE 2; TCRV ALPHA 24 J ALPHA 18; TUMOR NECROSIS FACTOR ALPHA INDUCED PROTEIN 3; UNCLASSIFIED DRUG; UROKINASE; CYTOKINE; LEUKOCYTE ANTIGEN; TRANSCRIPTOME;

ADOLESCENT; ADULT; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DECIDUA; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROARRAY ANALYSIS; NATURAL KILLER CELL; NATURAL KILLER T CELL; PREMATURE LABOR; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; TRANSCRIPTOMICS; UPREGULATION; CELL LINEAGE; CLASSIFICATION; CYTOLOGY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; LABOR; LYMPHOCYTE; LYMPHOCYTE COUNT; METABOLISM; NEWBORN; PATHOLOGY; PREGNANCY; TERM BIRTH;

ANTIGENS, CD; CELL LINEAGE; CYTOKINES; DECIDUA; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; INFANT, NEWBORN; LABOR, OBSTETRIC; LYMPHOCYTE COUNT; LYMPHOCYTES; MICROARRAY ANALYSIS; OBSTETRIC LABOR, PREMATURE; PREGNANCY; TERM BIRTH; TRANSCRIPTOME;

EID: 85037983241     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gax038     Document Type: Article

References (83)

1. Baricos WH, Cortez SL, el-Dahr SS, Schnaper HW. ECM degradation by cultured human mesangial cells is mediated by a PA/plasmin/MMP-2 cascade. Kidney Int 1995;47:1039-1047
2. Bartmann C, Segerer SE, Rieger L, Kapp M, Sutterlin M, Kammerer U. Quantification of the predominant immune cell populations in decidua throughout human pregnancy. Am J Reprod Immunol 2014;71:109-119
3. Blencowe H, Cousens S, Chou D, Oestergaard M, Say L, Moller AB, Kinney M, Lawn J, G. Born Too Soon Preterm Birth Action. Born too soon: the global epidemiology of 15 million preterm births. Reprod Health 2013;10:S2
4. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, Adler A, Vera Garcia C, Rohde S, Say L et al. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 2012;379:2162-2172
5. Blumberg RS, Terhorst C, Bleicher P, McDermott FV, Allan CH, Landau SB, Trier JS, Balk SP. Expression of a nonpolymorphic MHC class I-like molecule, CD1D, by human intestinal epithelial cells. J Immunol 1991; 147:2518-2524
6. Bogic LV, Ohira RH, Yamamoto SY, Okazaki KJ, Millar K, Bryant-Greenwood GD. Tissue plasminogen activator and its receptor in the human amnion, chorion, and decidua at preterm and term. Biol Reprod 1999;60:1006-1012
7. Bollapragada S, Youssef R, Jordan F, Greer I, Norman J, Nelson S. Term labor is associated with a core inflammatory response in human fetal membranes, myometrium, and cervix. Am J Obstet Gynecol 2009;200: 104 e101-104 e111
8. Boyson JE, Rybalov B, Koopman LA, Exley M, Balk SP, Racke FK, Schatz F, Masch R, Wilson SB, Strominger JL. CD1d and invariant NKT cells at the human maternal-fetal interface. Proc Natl Acad Sci USA 2002;99:13741-13746
9. Brennan DJ, McGee SF, Rexhepaj E, O'Connor DP, Robson M, O'Herlihy C. Identification of a myometrial molecular profile for dystocic labor. BMC Pregnancy Childbirth 2011;11:74
10. Brennan PJ, Brigl M, Brenner MB. Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 2013;13:101-117
11. Brigl M, Brenner MB. CD1: antigen presentation and T cell function. Annu Rev Immunol 2004;22:817-890
12. Brown D, Trowsdale J, Allen R. The LILR family: modulators of innate and adaptive immune pathways in health and disease. Tissue Antigens 2004; 64:215-225
13. Casey ML, MacDonald PC. Biomolecular processes in the initiation of parturition: decidual activation. Clin Obstet Gynecol 1988;31:533-552
14. Cunningham FG, Leveno KJ, Bloom SL, Spong CY, Dashe JS, Barbara BL, Cassey BM, Sheffield JS Williams Obstetrics, 24th edn. New York, USA: McGraw-Hill Education, 2014
15. Denison FC, Kelly RW, Calder AA, Riley SC. Cytokine secretion by human fetal membranes, decidua and placenta at term. Hum Reprod 1998;13: 3560-3565
16. Eidem HR, Ackerman W. E. t., McGary KL, Abbot P, Rokas A. Gestational tissue transcriptomics in term and preterm human pregnancies: a systematic review and meta-analysis. BMC Med Genomics 2015;8:27
17. Elovitz MA, Baron J, Phillippe M. The role of thrombin in preterm parturition. Am J Obstet Gynecol 2001;185:1059-1063
18. Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002;30: 1575-1584
19. Exley M, Garcia J, Wilson SB, Spada F, Gerdes D, Tahir SM, Patton KT, Blumberg RS, Porcelli S, Chott A et al. CD1d structure and regulation on human thymocytes, peripheral blood T cells, B cells and monocytes. Immunology 2000;100:37-47
20. Gomez-Lopez N, Estrada-Gutierrez G, Jimenez-Zamudio L, Vega-Sanchez R, Vadillo-Ortega F. Fetal membranes exhibit selective leukocyte chemotaxic activity during human labor. J Reprod Immunol 2009; 80:122-131
21. 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
22. Haas DM, Caldwell DM, Kirkpatrick P, McIntosh JJ, Welton NJ. Tocolytic therapy for preterm delivery: systematic review and network metaanalysis. BMJ 2012;345:e6226
23. Hamilton S, Oomomian Y, Stephen G, Shynlova O, Tower CL, Garrod A, Lye SJ, Jones RL. Macrophages infiltrate the human and rat decidua during term and preterm labor: evidence that decidual inflammation precedes labor. Biol Reprod 2012;86:39
24. Hamilton SA, Tower CL, Jones RL. Identification of chemokines associated with the recruitment of decidual leukocytes in human labour: potential novel targets for preterm labour. PLoS One 2013;8:e56946
25. Hassan SS, Romero R, Haddad R, Hendler I, Khalek N, Tromp G, Diamond MP, Sorokin Y, Malone J Jr. The transcriptome of the uterine cervix before and after spontaneous term parturition. Am J Obstet Gynecol 2006;195:778-786
26. Hirayasu K, Arase H. Functional and genetic diversity of leukocyte immunoglobulin-like receptor and implication for disease associations. J Hum Genet 2015;60:703-708
27. Ibrahim SA, Ackerman W. E. t., Summerfield TL, Lockwood CJ, Schatz F, Kniss DA. Inflammatory gene networks in term human decidual cells define a potential signature for cytokine-mediated parturition. Am J Obstet Gynecol 2016;214:284 e281-284 e247
28. Ito K, Karasawa M, Kawano T, Akasaka T, Koseki H, Akutsu Y, Kondo E, Sekiya S, Sekikawa K, Harada M et al. Involvement of decidual Valpha14 NKT cells in abortion. Proc Natl Acad Sci USA 2000;97:740-744
29. Kauffmann A, Huber W. Microarray data quality control improves the detection of differentially expressed genes. Genomics 2010;95:138-142
30. Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD. Cytokines, prostaglandins and parturition-a review. Placenta 2003;24: S33-S46
31. Kelly RW, Leask R, Calder AA. Choriodecidual production of interleukin-8 and mechanism of parturition. Lancet 1992;339:776-777
32. Kim SY, Romero R, Tarca AL, Bhatti G, Kim CJ, Lee J, Elsey A, Than NG, Chaiworapongsa T, Hassan SS et al. Methylome of fetal and maternal monocytes and macrophages at the feto-maternal interface. Am J Reprod Immunol 2012;68:8-27
33. Li L, Yang J, Jiang Y, Tu J, Schust DJ. Activation of decidual invariant natural killer T cells promotes lipopolysaccharide-induced preterm birth. Mol Hum Reprod 2015;21:369-381
34. Li L, Yang J, Ren L, Su N, Fang Y, Lin Y. Invariant NKT cells increase lipopolysacchride-induced pregnancy loss by a mechanism involving Th1 and Th17 responses. J Matern Fetal Neonatal Med 2013;26: 1212-1218
35. Li LP, Fang YC, Dong GF, Lin Y, Saito S. Depletion of invariant NKT cells reduces inflammation-induced preterm delivery in mice. J Immunol 2012; 188:4681-4689
36. Li W, Alfaidy N, Challis JR. Expression of extracellular matrix metalloproteinase inducer in human placenta and fetal membranes at term labor. J Clin Endocrinol Metab 2004;89:2897-2904
37. Liu YX, Hu ZY, Liu K, Byrne S, Zou RJ, Ny T, d'Lacey C, Ockleford CD. Localization and distribution of tissue type and urokinase type plasminogen activators and their inhibitors Type 1 and 2 in human and rhesus monkey fetal membranes. Placenta 1998;19:171-180
38. Makino S, Zaragoza DB, Mitchell BF, Robertson S, Olson DM. Prostaglandin F2alpha and its receptor as activators of human decidua. Semin Reprod Med 2007;25:60-68
39. Matsumoto J, Kawana K, Nagamatsu T, Schust DJ, Fujii T, Sato H, Hyodo H, Yasugi T, Kozuma S, Taketani Y. Expression of surface CD1d in the extravillous trophoblast cells of early gestational placenta is downregulated in a manner dependent on trophoblast differentiation. Biochem Biophys Res Commun 2008;371:236-241
40. Milne SA, McGregor AL, McCulloch J, Sharkey J. Increased expression of macrophage receptor with collagenous structure (MARCO) in mouse cortex following middle cerebral artery occlusion. Neurosci Lett 2005; 383:58-62
41. Mittal P, Romero R, Tarca AL, Gonzalez J, Draghici S, Xu Y, Dong Z, Nhan-Chang CL, Chaiworapongsa T, Lye S et al. Characterization of the myometrial transcriptome and biological pathways of spontaneous human labor at term. J Perinat Med 2010;38:617-643
42. Negishi Y, Shima Y, Takeshita T, Takahashi H. Distribution of invariant natural killer T cells and dendritic cells in late pre-term birth without acute chorioamnionitis. Am J Reprod Immunol 2017;77(6). doi: 10.1111/aji.12658
43. Norman JE, Morris C, Chalmers J. The effect of changing patterns of obstetric care in Scotland (1980-04) on rates of preterm birth and its neonatal consequences: perinatal database study. PLoS Med 2009;6: e1000153
44. Norman JE, Shennan AH. Prevention of preterm birth-why can't we do any better? The Lancet 2013;381:184-185
45. Norwitz ER, Bonney EA, Snegovskikh VV, Williams MA, Phillippe M, Park JS, Abrahams VM. Molecular regulation of parturition: the role of the decidual clock. Cold Spring Harb Perspect Med 2015;5(11). pii: a023143. doi: 10.1101/cshperspect.a023143
46. Norwitz ER, Snegovskikh V, Schatz F, Foyouzi N, Rahman M, Buchwalder L, Lee HJ, Funai EF, Buhimschi CS, Buhimschi IA et al. Progestin inhibits and thrombin stimulates the plasminogen activator/inhibitor system in term decidual stromal cells: implications for parturition. Am J Obstet Gynecol 2007;196:382 e381-382 e388
47. Osman I, Young A, Jordan F, Greer IA, Norman JE. Leukocyte density and proinflammatory mediator expression in regional human fetal membranes and decidua before and during labor at term. J Soc Gynecol Investig 2006;13:97-103
48. Osman I, Young A, Ledingham MA, Thomson AJ, Jordan F, Greer IA, Norman JE. Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol Hum Reprod 2003;9:41-45
49. Osmers RG, Blaser J, Kuhn W, Tschesche H. Interleukin-8 synthesis and the onset of labor. Obstet Gynecol 1995;86:223-229
50. Phillippe M, Diamond AK, Sweet LM, Oppenheimer KH, Bradley DF. Expression of coagulation-related protein genes during LPS-induced preterm delivery in the pregnant mouse. Reprod Sci 2011;18:1071-1079
51. Rinaldi SF, Catalano RD, Wade J, Rossi AG, Norman JE. Decidual neutrophil infiltration is not required for preterm birth in a mouse model of infection-induced preterm labor. J Immunol 2014;192:2315-2325
52. Rinaldi SF, Hutchinson JL, Rossi AG, Norman JE. Anti-inflammatory mediators as physiological and pharmacological regulators of parturition. Expert Rev Clin Immunol 2011;7:675-696
53. Rinaldi SF, Rossi AG, Saunders PT, Norman JE. Immune cells and preterm labour: do invariant NKT cells hold the key? Mol Hum Reprod 2015;21:309-312
54. Roh CR, Oh WJ, Yoon BK, Lee JH. Up-regulation of matrix metalloproteinase-9 in human myometrium during labour: a cytokinemediated process in uterine smooth muscle cells. Mol Hum Reprod 2000;6:96-102
55. Romero R, Ceska M, Avila C, Mazor M, Behnke E, Lindley I. Neutrophil attractant/activating peptide-1/interleukin-8 in term and preterm parturition. Am J Obstet Gynecol 1991;165:813-820
56. Romero R, Dey SK, Fisher SJ. Preterm labor: one syndrome, many causes. Science 2014;345:760-765
57. Sennstrom MB, Ekman G, Westergren-Thorsson G, Malmstrom A, Bystrom B, Endresen U, Mlambo N, Norman M, Stabi B, Brauner A. Human cervical ripening, an inflammatory process mediated by cytokines. Mol Hum Reprod 2000;6:375-381
58. Seta N, Granfors K, Sahly H, Kuipers JG, Song YW, Baeten D, Veys EM, Maksymowych W, Marker-Hermann E, Gu J et al. Expression of host defense scavenger receptors in spondylarthropathy. Arthritis Rheum 2001;44:931-939
59. Shankar R, Johnson MP, Williamson NA, Cullinane F, Purcell AW, Moses EK, Brennecke SP. Molecular markers of preterm labor in the choriodecidua. Reprod Sci 2010;17:297-310
60. Shao L, Jacobs AR, Johnson VV, Mayer L. Activation of CD8+ regulatory T cells by human placental trophoblasts. J Immunol 2005;174:7539-7547
61. Sharp GC, Hutchinson JL, Hibbert N, Freeman TC, Saunders PT, Norman JE. Transcription analysis of the myometrium of labouring and nonlabouring women. PLoS One 2016;11:e0155413
62. Shynlova O, Nedd-Roderique T, Li Y, Dorogin A, Lye SJ. Myometrial immune cells contribute to term parturition, preterm labour and postpartum involution in mice. J Cell Mol Med 2013a;17:90-102
63. Shynlova O, Nedd-Roderique T, Li Y, Dorogin A, Nguyen T, Lye SJ. Infiltration of myeloid cells into decidua is a critical early event in the labour cascade and post-partum uterine remodelling. J Cell Mol Med 2013b;17:311-324
64. Sindram-Trujillo A, Scherjon S, Kanhai H, Roelen D, Claas F. Increased Tcell activation in decidua parietalis compared to decidua basalis in uncomplicated human term pregnancy. Am J Reprod Immunol 2003a;49: 261-268
65. 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 2003b;64:921-929
66. Sindram-Trujillo AP, Scherjon SA, van Hulst-van Miert PP, Kanhai HH, Roelen DL, Claas FH. Comparison of decidual leukocytes following spontaneous vaginal delivery and elective cesarean section in uncomplicated human term pregnancy. J Reprod Immunol 2004;62:125-137
67. Skold M, Xiong X, Illarionov PA, Besra GS, Behar SM. Interplay of cytokines and microbial signals in regulation of CD1d expression and NKT cell activation. J Immunol 2005;175:3584-3593
68. Snegovskikh VV, Bhandari V, Wright JR, Tadesse S, Morgan T, Macneill C, Foyouzi N, Park JS, Wang Y, Norwitz ER. Surfactant protein-A (SP-A) selectively inhibits prostaglandin F2alpha (PGF2alpha) production in term decidua: implications for the onset of labor. J Clin Endocrinol Metab 2011;96:E624-E632
69. St Louis D, Romero R, Plazyo O, Arenas-Hernandez M, Panaitescu B, Xu Y, Milovic T, Xu Z, Bhatti G, Mi QS et al. Invariant NKT cell activation induces late preterm birth that is attenuated by Rosiglitazone. J Immunol 2016;196:1044-1059
70. Stephen GL, Lui S, Hamilton SA, Tower CL, Harris LK, Stevens A, Jones RL. Transcriptomic profiling of human choriodecidua during term labor: inflammation as a key driver of labor. Am J Reprod Immunol 2015;73:36-55
71. Thelen T, Hao Y, Medeiros AI, Curtis JL, Serezani CH, Kobzik L, Harris LH, Aronoff DM. The class A scavenger receptor, macrophage receptor with collagenous structure, is the major phagocytic receptor for Clostridium sordellii expressed by human decidual macrophages. J Immunol 2010;185:4328-4335
72. Theocharidis A, van Dongen S, Enright AJ, Freeman TC. Network visualization and analysis of gene expression data using BioLayout Express (3D). Nat Protoc 2009;4:1535-1550
73. Thomson AJ, Telfer JF, Young A, Campbell S, Stewart CJ, Cameron IT, Greer IA, Norman JE. Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Hum Reprod 1999;14:229-236
74. Tornblom SA, Klimaviciute A, Bystrom B, Chromek M, Brauner A, Ekman-Ordeberg G. Non-infected preterm parturition is related to increased concentrations of IL-6, IL-8 and MCP-1 in human cervix. Reprod Biol Endocrinol 2005;3:39
75. Tsuda H, Sakai M, Michimata T, Tanebe K, Hayakawa S, Saito S. Characterization of NKT cells in human peripheral blood and decidual lymphocytes. Am J Reprod Immunol 2001;45:295-302
76. Ulug U, Goldman S, Ben-Shlomo I, Shalev E. Matrix metalloproteinase (MMP)-2 and MMP-9 and their inhibitor, TIMP-1, in human term decidua and fetal membranes: the effect of prostaglandin F(2alpha) and indomethacin. Mol Hum Reprod 2001;7:1187-1193
77. van der Laan LJ, Dopp EA, Haworth R, Pikkarainen T, Kangas M, Elomaa O, Dijkstra CD, Gordon S, Tryggvason K, Kraal G. Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J Immunol 1999;162:939-947
78. Vassalli JD, Sappino AP, Belin D. The plasminogen activator/plasmin system. J Clin Invest 1991;88:1067-1072
79. Velez DR, Fortunato SJ, Thorsen P, Lombardi SJ, Williams SM, Menon R. Preterm birth in Caucasians is associated with coagulation and inflammation pathway gene variants. PLoS One 2008;3:e3283
80. Weiner CP, Mason CW, Dong Y, Buhimschi IA, Swaan PW, Buhimschi CS. Human effector/initiator gene sets that regulate myometrial contractility during term and preterm labor. Am J Obstet Gynecol 2010;202: 474 e471-420
81. 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
82. Young A, Thomson AJ, Ledingham M, Jordan F, Greer IA, Norman JE. Immunolocalization of proinflammatory cytokines in myometrium, cervix, and fetal membranes during human parturition at term. Biol Reprod 2002;66:445-449
83. Zhao Y, Lyons CE Jr, Xiao A, Templeton DJ, Sang QA, Brew K, Hussaini IM. Urokinase directly activates matrix metalloproteinases-9: a potential role in glioblastoma invasion. Biochem Biophys Res Commun 2008;369: 1215-1220