Differential immunophenotype of macrophages in acute and chronic chorioamnionitis
-
Go-Eun Bae
, Ha Young Park
Abstract
Aim:
The aim of this study was to investigate the involvement and immunophenotype of macrophages in acute chorioamnionitis (ACA) and chronic chorioamnionitis (CCA), marking amniotic fluid infection and anti-fetal rejection, respectively.
Methods:
Chorioamniotic membranes from (1) gestational age-matched cases without chorioamnionitis, (2) cases with ACA, and (3) cases with CCA were studied after immunohistochemical staining using antibodies against CD14, CD68, CD163, and DC-SIGN.
Results:
Macrophages increased prominently in the chorionic trophoblastic layer of both ACA and CCA cases in contrast to non-inflammatory cases. Macrophages in the decidua and the chorioamniotic membranes of ACA cases expressed CD14. Macrophages in the chorionic trophoblastic layer of CCA cases were characterized by CD68 positivity. DC-SIGN-positive cells were increased in the chorioamniotic mesodermal layer of CCA cases.
Conclusions:
Macrophages participate in the inflammatory response in ACA and CCA. The differential immunophenotypes of macrophages in the decidua and chorioamniotic membranes of ACA and CCA cases suggest their disease-specific and region-specific roles at the feto-maternal interface.
Funding source: Ministry of Science ICT and Future Planning
Funding source: Ministry of Health and Welfare
Award Identifier / Grant number: NRF-2012R1A1A3012668
Award Identifier / Grant number: HI1200024 (A120035)
Funding statement: This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (NRF-2012R1A1A3012668) and by the Korean Health Technology R&D Project, Ministry of Health & Welfare [HI1200024 (A120035)], Republic of Korea. The authors are indebted to J. Patrick Barren, professor emeritus of Tokyo Medical University and adjunct professor of Seoul National University Bundang Hospital for his editing of this manuscript.
Acknowledgments:
This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (NRF-2012R1A1A3012668) and by the Korean Health Technology R&D Project, Ministry of Health & Welfare [HI1200024 (A120035)], Republic of Korea. The authors are indebted to J. Patrick Barren, professor emeritus of Tokyo Medical University and adjunct professor of Seoul National University Bundang Hospital for his editing of this manuscript.
References
[1] Abrahams VM, Kim YM, Straszewski SL, Romero R, Mor G. Macrophages and apoptotic cell clearance during pregnancy. Am J Reprod Immunol. 2004;51:275–82.10.1111/j.1600-0897.2004.00156.xSuche in Google Scholar
[2] Fest S, Aldo PB, Abrahams VM, Visintin I, Alvero A, Chen R, et al. Trophoblast-macrophage interactions: a regulatory network for the protection of pregnancy. Am J Reprod Immunol. 2007;57:55–66.10.1111/j.1600-0897.2006.00446.xSuche in Google Scholar
[3] Vince GS, Starkey PM, Jackson MC, Sargent IL, Redman CW. Flow cytometric characterisation of cell populations in human pregnancy decidua and isolation of decidual macrophages. J Immunol Methods. 1990;132:181–9.10.1016/0022-1759(90)90028-TSuche in Google Scholar
[4] Heikkinen J, Mottonen M, Komi J, Alanen A, Lassila O. Phenotypic characterization of human decidual macrophages. Clin Exp Immunol. 2003;131:498–505.10.1046/j.1365-2249.2003.02092.xSuche in Google Scholar
[5] Gustafsson C, Mjosberg J, Matussek A, Geffers R, Matthiesen L, Berg G, et al. Gene expression profiling of human decidual macrophages: evidence for immunosuppressive phenotype. PLoS One. 2008;3:e2078.10.1371/journal.pone.0002078Suche in Google Scholar
[6] Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004;25:677–86.10.1016/j.it.2004.09.015Suche in Google Scholar
[7] Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol. 2013;229:176–85.10.1002/path.4133Suche in Google Scholar
[8] Hoyes AD. Ultrastructure of the mesenchymal layers of the human chorion laeve. J Anat. 1971;109:17–30.Suche in Google Scholar
[9] Kim SS, Romero R, Kim JS, Abbas A, Espinoza J, Kusanovic JP, et al. Coexpression of myofibroblast and macrophage markers: novel evidence for an in vivo plasticity of chorioamniotic mesodermal cells of the human placenta. Lab Invest. 2008;88:365–74.10.1038/labinvest.3700749Suche in Google Scholar
[10] Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 2012;336:86–90.10.1126/science.1219179Suche in Google Scholar
[11] Yoon BH, Romero R, Park JS, Chang JW, Kim YA, Kim JC, et al. Microbial invasion of the amniotic cavity with ureaplasma urealyticum is associated with a robust host response in fetal, amniotic, and maternal compartments. Am J Obstet Gynecol. 1998;179:1254–60.10.1016/S0002-9378(98)70142-5Suche in Google Scholar
[12] Martinelli P, Sarno L, Maruotti GM, Paludetto R. Chorioamnionitis and prematurity: a critical review. J Matern Fetal Neonatal Med. 2012;25(Suppl 4):29–31.10.3109/14767058.2012.714981Suche in Google Scholar
[13] Redline RW, Faye-Petersen O, Heller D, Qureshi F, Savell V, Vogler C, et al. Amniotic infection syndrome: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol. 2003;6:435–48.10.1007/s10024-003-7070-ySuche in Google Scholar
[14] Gersell DJ, Phillips NJ, Beckerman K. Chronic chorioamnionitis: a clinicopathologic study of 17 cases. Int J Gynecol Pathol. 1991;10:217–29.10.1097/00004347-199107000-00001Suche in Google Scholar
[15] Jacques SM, Qureshi F. Chronic chorioamnionitis: a clinicopathologic and immunohistochemical study. Hum Pathol. 1998;29:1457–61.10.1016/S0046-8177(98)90016-8Suche in Google Scholar
[16] Kim CJ, Romero R, Kusanovic JP, Yoo W, Dong Z, Topping V, et al. The frequency, clinical significance, and pathological features of chronic chorioamnionitis: a lesion associated with spontaneous preterm birth. Mod Pathol. 2010;23:1000–11.10.1038/modpathol.2010.73Suche in Google Scholar PubMed PubMed Central
[17] Lee J, Kim JS, Park JW, Park CW, Park JS, Jun JK, et al. Chronic chorioamnionitis is the most common placental lesion in late preterm birth. Placenta. 2013;34:681–9.10.1016/j.placenta.2013.04.014Suche in Google Scholar PubMed
[18] Lee J, Romero R, Dong Z, Xu Y, Qureshi F, Jacques S, et al. Unexplained fetal death has a biological signature of maternal anti-fetal rejection: chronic chorioamnionitis and alloimmune anti-human leucocyte antigen antibodies. Histopathology. 2011;59:928–38.10.1111/j.1365-2559.2011.04038.xSuche in Google Scholar PubMed PubMed Central
[19] Kim MJ, Romero R, Kim CJ, Tarca AL, Chhauy S, LaJeunesse C, et al. Villitis of unknown etiology is associated with a distinct pattern of chemokine up-regulation in the feto-maternal and placental compartments: implications for conjoint maternal allograft rejection and maternal anti-fetal graft-versus-host disease. J Immunol. 2009;182:3919–27.10.4049/jimmunol.0803834Suche in Google Scholar PubMed PubMed Central
[20] Lee J, Romero R, Xu Y, Kim JS, Park JY, Kusanovic JP, et al. Maternal HLA panel-reactive antibodies in early gestation positively correlate with chronic chorioamnionitis: evidence in support of the chronic nature of maternal anti-fetal rejection. Am J Reprod Immunol. 2011;66:510–26.10.1111/j.1600-0897.2011.01066.xSuche in Google Scholar PubMed PubMed Central
[21] Lee J, Romero R, Xu Y, Kim JS, Topping V, Yoo W, et al. A signature of maternal anti-fetal rejection in spontaneous preterm birth: chronic chorioamnionitis, anti-human leukocyte antigen antibodies, and C4d. PLoS One. 2011;6:e16806.10.1371/journal.pone.0016806Suche in Google Scholar PubMed PubMed Central
[22] Bang H, Bae GE, Park HY, Kim YM, Choi SJ, Oh SY, et al. Chronic placental inflammation in twin pregnancies. J Pathol Transl Med. 2015;49:489–96.10.4132/jptm.2015.09.09Suche in Google Scholar
[23] Kaiserling E, Xiao JC, Ruck P, Horny HP. Aberrant expression of macrophage-associated antigens (CD68 and Ki-M1P) by Schwann cells in reactive and neoplastic neural tissue. Light- and electron-microscopic findings. Mod Pathol. 1993;6:463–8.Suche in Google Scholar
[24] Saito N, Pulford KA, Breton-Gorius J, Masse JM, Mason DY, Cramer EM. Ultrastructural localization of the CD68 macrophage-associated antigen in human blood neutrophils and monocytes. Am J Pathol. 1991;139:1053–9.Suche in Google Scholar
[25] Fujihara M, Muroi M, Tanamoto K, Suzuki T, Azuma H, Ikeda H. Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex. Pharmacol Ther. 2003;100:171–94.10.1016/j.pharmthera.2003.08.003Suche in Google Scholar
[26] Bockle BC, Solder E, Kind S, Romani N, Sepp NT. DC-sign+ CD163+ macrophages expressing hyaluronan receptor LYVE-1 are located within chorion villi of the placenta. Placenta. 2008;29:187–92.10.1016/j.placenta.2007.11.003Suche in Google Scholar
[27] Geijtenbeek TB, Torensma R, van Vliet SJ, van Duijnhoven GC, Adema GJ, van Kooyk Y, et al. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell. 2000;100:575–85.10.1016/S0092-8674(00)80693-5Suche in Google Scholar
[28] Dominguez-Soto A, Sierra-Filardi E, Puig-Kroger A, Perez-Maceda B, Gomez-Aguado F, Corcuera MT, et al. Dendritic cell-specific ICAM-3-grabbing nonintegrin expression on M2-polarized and tumor-associated macrophages is macrophage-CSF dependent and enhanced by tumor-derived IL-6 and IL-10. J Immunol. 2011;186:2192–200.10.4049/jimmunol.1000475Suche in Google Scholar
[29] Nagaoka K, Takahara K, Minamino K, Takeda T, Yoshida Y, Inaba K. Expression of C-type lectin, SIGNR3, on subsets of dendritic cells, macrophages, and monocytes. J Leukoc Biol. 2010;88:913–24.10.1189/jlb.0510251Suche in Google Scholar
[30] Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol. 2006;177:7303–11.10.4049/jimmunol.177.10.7303Suche in Google Scholar
[31] Joerink M, Rindsjo E, van Riel B, Alm J, Papadogiannakis N. Placental macrophage (Hofbauer cell) polarization is independent of maternal allergen-sensitization and presence of chorioamnionitis. Placenta. 2011;32:380–5.10.1016/j.placenta.2011.02.003Suche in Google Scholar
[32] Gardner L, Moffett A. Dendritic cells in the human decidua. Biol Reprod. 2003;69:1438–46.10.1095/biolreprod.103.017574Suche in Google Scholar
[33] Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TB, Dietl J, et al. Unique appearance of proliferating antigen- presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am J Pathol. 2003;162:887–96.10.1016/S0002-9440(10)63884-9Suche in Google Scholar
[34] Schonkeren D, van der Hoorn ML, Khedoe P, Swings G, van Beelen E, Claas F, et al. Differential distribution and phenotype of decidual macrophages in preeclamptic versus control pregnancies. Am J Pathol. 2011;178:709–17.10.1016/j.ajpath.2010.10.011Suche in Google Scholar PubMed PubMed Central
[35] Hsu P, Santner-Nanan B, Dahlstrom JE, Fadia M, Chandra A, Peek M, et al. Altered decidual DC-SIGN+ antigen-presenting cells and impaired regulatory T-cell induction in preeclampsia. Am J Pathol. 2012;181:2149–60.10.1016/j.ajpath.2012.08.032Suche in Google Scholar PubMed
[36] Kim JS, Romero R, Kim MR, Kim YM, Friel L, Espinoza J, et al. Involvement of Hofbauer cells and maternal T cells in villitis of unknown aetiology. Histopathology. 2008;52:457–64.10.1111/j.1365-2559.2008.02964.xSuche in Google Scholar PubMed PubMed Central
[37] Magil AB. Monocytes/macrophages in renal allograft rejection. Transplant Rev (Orlando). 2009;23:199–208.10.1016/j.trre.2009.06.005Suche in Google Scholar PubMed
[38] Jose MD, Ikezumi Y, van Rooijen N, Atkins RC, Chadban SJ. Macrophages act as effectors of tissue damage in acute renal allograft rejection. Transplantation. 2003;76:1015–22.10.1097/01.TP.0000083507.67995.13Suche in Google Scholar PubMed
[39] Wyburn K, Wu H, Yin J, Jose M, Eris J, Chadban S. Macrophage-derived interleukin-18 in experimental renal allograft rejection. Nephrol Dial Transplant. 2005;20:699–706.10.1093/ndt/gfh712Suche in Google Scholar PubMed
[40] Guiducci C, Vicari AP, Sangaletti S, Trinchieri G, Colombo MP. Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res. 2005;65:3437–46.10.1158/0008-5472.CAN-04-4262Suche in Google Scholar PubMed
[41] Shaul ME, Bennett G, Strissel KJ, Greenberg AS, Obin MS. Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet–induced obesity in mice. Diabetes. 2010;59:1171–81.10.2337/db09-1402Suche in Google Scholar PubMed PubMed Central
[42] Bystrom J, Evans I, Newson J, Stables M, Toor I, van Rooijen N, et al. Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP. Blood. 2008;112:4117–27.10.1182/blood-2007-12-129767Suche in Google Scholar PubMed PubMed Central
[43] McNamara MF, Wallis T, Qureshi F, Jacques SM, Gonik B. Determining the maternal and fetal cellular immunologic contributions in preterm deliveries with clinical or subclinical chorioamnionitis. Infect Dis Obstet Gynecol. 1997;5:273–9.10.1155/S1064744997000471Suche in Google Scholar PubMed PubMed Central
The authors stated that there are no conflicts of interest regarding the publication of this article.
©2017 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Editorial
- Antepartum care
- Academy’s Paper
- Late pregnancy – a clue to prolonging life?
- Highlight articles
- The effect of cigarette smoking on fetal heart rate tracing during pregnancy
- Correlation between markers of DNA and lipid oxidative damage in maternal and fetoplacental compartment in the mid-trimester of pregnancy
- Hyperemesis gravidarum is associated with increased maternal serum ischemia-modified albumin
- Can prepartum thromboelastometry-derived parameters and fibrinogen levels really predict postpartum hemorrhage?
- Effect of DHA supplements during pregnancy on the concentration of PUFA in breast milk of Chinese lactating mothers
- Ferric carboxymaltose vs. oral iron in the treatment of pregnant women with iron deficiency anemia: an international, open-label, randomized controlled trial (FER-ASAP)
- Maternal and perinatal outcomes in pregnancies with multiple sclerosis: a case-control study
- The role of vitamin B1-B2 and plasma lipid profile in intrahepatic cholestasis of pregnancy
- Hyponatremia associated with preeclampsia
- Impact of routine transvaginal ultrasound monitoring of cervical length in twins on administration of antenatal corticosteroids
- Does an ideal prototype of a twin mother exist?
- Differential immunophenotype of macrophages in acute and chronic chorioamnionitis
- Longitudinal changes of cardiotocographic parameters throughout pregnancy: a prospective cohort study comparing small-for-gestational-age and normal fetuses from 24 to 40 weeks
- Congress Calendar
- Congress Calendar
Artikel in diesem Heft
- Frontmatter
- Editorial
- Antepartum care
- Academy’s Paper
- Late pregnancy – a clue to prolonging life?
- Highlight articles
- The effect of cigarette smoking on fetal heart rate tracing during pregnancy
- Correlation between markers of DNA and lipid oxidative damage in maternal and fetoplacental compartment in the mid-trimester of pregnancy
- Hyperemesis gravidarum is associated with increased maternal serum ischemia-modified albumin
- Can prepartum thromboelastometry-derived parameters and fibrinogen levels really predict postpartum hemorrhage?
- Effect of DHA supplements during pregnancy on the concentration of PUFA in breast milk of Chinese lactating mothers
- Ferric carboxymaltose vs. oral iron in the treatment of pregnant women with iron deficiency anemia: an international, open-label, randomized controlled trial (FER-ASAP)
- Maternal and perinatal outcomes in pregnancies with multiple sclerosis: a case-control study
- The role of vitamin B1-B2 and plasma lipid profile in intrahepatic cholestasis of pregnancy
- Hyponatremia associated with preeclampsia
- Impact of routine transvaginal ultrasound monitoring of cervical length in twins on administration of antenatal corticosteroids
- Does an ideal prototype of a twin mother exist?
- Differential immunophenotype of macrophages in acute and chronic chorioamnionitis
- Longitudinal changes of cardiotocographic parameters throughout pregnancy: a prospective cohort study comparing small-for-gestational-age and normal fetuses from 24 to 40 weeks
- Congress Calendar
- Congress Calendar