Decreased levels of folate receptor-β and reduced numbers of fetal macrophages (hofbauer cells) in placentas from pregnancies with severe pre-eclampsia

American Journal of Reproductive Immunology

Volumn 70, Issue 2, 2013, Pages 104-115

  Tang, Zhonghua ^a   Buhimschi, Irina A ^a   Buhimschi, Catalin S ^a   Tadesse, Serkalem ^b   Norwitz, Errol ^b   Niven Fairchild, Tracy ^a   Huang, Se Te J ^c   Guller, Seth ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS MEDICAL CENTER   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Fetal macrophages; Folate receptor; Hofbauer cells; Placenta

Indexed keywords

FOLATE RECEPTOR 2;

ADULT; ARTICLE; CELL TYPE; CLINICAL ARTICLE; DISEASE SEVERITY; DNA MICROARRAY; DOWN REGULATION; FEMALE; FOLATE RECEPTOR BETA BLOOD LEVEL; GENE REPRESSION; GESTATIONAL AGE; HUMAN; IMMUNOHISTOCHEMISTRY; MACROPHAGE; PLACENTA; PREECLAMPSIA; PREMATURE LABOR; PRENATAL GROWTH; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

FETAL MACROPHAGES; FOLATE RECEPTOR; HOFBAUER CELLS; PLACENTA;

ADULT; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; DOWN-REGULATION; FEMALE; FOLATE RECEPTOR 2; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; MACROPHAGES; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RECEPTORS, CELL SURFACE; RNA, MESSENGER; YOUNG ADULT;

EID: 84880317288     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12112     Document Type: Article

References (66)

1. Cetin I, Huppertz B, Burton G, Cuckle H, Gonen R, Lapaire O, Mandia L, Nicolaides K, Redman C, Soothill P, Spencer K, Thilaganathan B, Williams D, Meiri H: Pregenesys pre-eclampsia markers consensus meeting: what do we require from markers, risk assessment and model systems to tailor preventive strategies? Placenta 2011; 32(Suppl):S4-S16.
2. Redman CW, Sargent IL: Latest advances in understanding pre-eclampsia. Science 2005; 308:1592-1594.
3. Sargent IL, Borzychowski AM, Redman CW: Immunoregulation in normal pregnancy and pre-eclampsia: an overview. Reprod Biomed Online 2006; 13:680-686.
4. Estelles A, Gilabert J, Keeton M, Eguchi Y, Aznar J, Grancha S, Espna F, Loskutoff DJ, Schleef RR: Altered expression of plasminogen activator inhibitor type 1 in placentas from pregnant women with pre-eclampsia and/or intrauterine fetal growth retardation. Blood 1994; 84:143-150.
5. Salafia CM, Ernst LM, Pezzullo JC, Wolf EJ, Rosenkrantz TS, Vintzileos AM: The very low birthweight infant: maternal complications leading to preterm birth, placental lesions, and intrauterine growth. Am J Perinatol 1995; 12:106-110.
6. Salafia CM, Pezzullo JC, Lopez-Zeno JA, Simmens S, Minior VK, Vintzileos AM: Placental pathologic features of preterm preeclampsia. Am J Obstet Gynecol 1995; 173:1097-1105.
7. Cester N, Staffolani R, Rabini RA, Magnanelli R, Salvolini E, Galassi R, Mazzanti L, Romanini C: Pregnancy induced hypertension: a role for peroxidation in microvillus plasma membranes. Mol Cell Biochem 1994; 131:151-155.
8. Vince GS, Starkey PM, Austgulen R, Kwiatkowski D, Redman CW: Interleukin-6, tumour necrosis factor and soluble tumour necrosis factor receptors in women with pre-eclampsia. Br J Obstet Gynaecol 1995; 102:20-25.
9. Walsh SW, Vaughan JE, Wang Y, Roberts LJ II: Placental isoprostane is significantly increased in preeclampsia. FASEB J 2000; 14:1289-1296.
10. Clark DE, Smith SK, He Y, Day KA, Licence DR, Corps AN, Lammoglia R, Charnock-Jones DS: A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod 1998; 59:1540-1548.
11. Gu Y, Lewis DF, Wang Y: Placental productions and expressions of soluble endoglin, soluble fms-like tyrosine kinase receptor-1, and placental growth factor in normal and preeclamptic pregnancies. J Clin Endocrinol Metab 2008; 93:260-266.
12. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, Karumanchi SA: Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006; 355:992-1005.
13. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA: Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350:672-683.
14. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA: Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003; 111:649-658.
15. Knapen MF, Peters WH, Mulder TP, Merkus HM, Jansen JB, Steegers EA: Glutathione and glutathione-related enzymes in decidua and placenta of controls and women with pre-eclampsia. Placenta 1999; 20:541-546.
16. Wang Y, Walsh SW: Antioxidant activities and mRNA expression of superoxide dismutase, catalase, and glutathione peroxidase in normal and preeclamptic placentas. J Soc Gynecol Investig 1996; 3:179-184.
17. Guller S, Buhimschi CS, Ma YY, Huang ST, Yang L, Kuczynski E, Zambrano E, Lockwood CJ, Buhimschi IA: Placental expression of ceruloplasmin in pregnancies complicated by severe preeclampsia. Lab Invest 2008; 88:1057-1067.
18. Founds SA, Conley YP, Lyons-Weiler JF, Jeyabalan A, Hogge WA, Conrad KP: Altered global gene expression in first trimester placentas of women destined to develop preeclampsia. Placenta 2009; 30:15-24.
19. Farina A, Morano D, Arcelli D, De Sanctis P, Sekizawa A, Purwosunu Y, Zucchini C, Simonazzi G, Okai T, Rizzo N: Gene expression in chorionic villous samples at 11 weeks of gestation in women who develop preeclampsia later in pregnancy: implications for screening. Prenat Diagn 2009; 29:1038-1044.
20. Farina A, Zucchini C, De Sanctis P, Morano D, Sekizawa A, Purwosunu Y, Okai T, Rizzo N: Gene expression in chorionic villous samples at 11 weeks of gestation in women who develop pre-eclampsia later in pregnancy: implications for screening. Prenat Diagn 2011; 31:181-185.
21. Leamon CP, Jackman AL: Exploitation of the folate receptor in the management of cancer and inflammatory disease. Vitam Horm 2008; 79:203-233.
22. Molloy AM, Kirke PN, Brody LC, Scott JM, Mills JL: Effects of folate and vitamin B12 deficiencies during pregnancy on fetal, infant, and child development. Food Nutr Bull 2008; 29:S101-S111; discussion S112-105.
23. ACOG practice bulletin: Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. Obstet Gynecol 2002; 99:159-167.
24. Newton ER: Preterm labor, preterm premature rupture of membranes, and chorioamnionitis. Clin Perinatol 2005; 32:571-600.
25. Pettker CM, Buhimschi IA, Magloire LK, Sfakianaki AK, Hamar BD, Buhimschi CS: Value of placental microbial evaluation in diagnosing intra-amniotic infection. Obstet Gynecol 2007; 109:739-749.
26. Salafia CM, Weigl C, Silberman L: The prevalence and distribution of acute placental inflammation in uncomplicated term pregnancies. Obstet Gynecol 1989; 73:383-389.
27. NIH Consensus development panel on the effect of corticosteroids for fetal maturation on perinatal outcomes. JAMA 1995; 273:413-418.
28. Lee MJ, Ma Y, LaChapelle L, Kadner SS, Guller S: Glucocorticoid enhances transforming growth factor-beta effects on extracellular matrix protein expression in human placental mesenchymal cells. Biol Reprod 2004; 70:1246-1252.
29. Budwit-Novotny DA, McCarty KS, Cox EB, Soper JT, Mutch DG, Creasman WT, Flowers JL, McCarty KS Jr: Immunohistochemical analyses of estrogen receptor in endometrial adenocarcinoma using a monoclonal antibody. Cancer Res 1986; 46:5419-5425.
30. Snegovskikh VV, Schatz F, Arcuri F, Toti P, Kayisli UA, Murk W, Guoyang L, Lockwood CJ, Norwitz ER: Intra-amniotic infection upregulates decidual cell vascular endothelial growth factor (VEGF) and neuropilin-1 and -2 expression: implications for infection-related preterm birth. Reprod Sci 2009; 16:767-780.
31. Tang Z, Niven-Fairchild T, Tadesse S, Norwitz ER, Buhimschi CS, Buhimschi IA, Guller S: Glucocorticoids enhance CD163 expression in placental Hofbauer cells. Endocrinology 2013; 154:471-482.
32. Haugen F, Ranheim T, Harsem NK, Lips E, Staff AC, Drevon CA: Increased plasma levels of adipokines in preeclampsia: relationship to placenta and adipose tissue gene expression. Am J Physiol Endocrinol Metab 2006; 290:E326-E333.
33. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, Stillman IE, Roberts D, D'Amore PA, Epstein FH, Sellke FW, Romero R, Sukhatme VP, Letarte M, Karumanchi SA: Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006; 12:642-649.
34. Gottfried E, Kunz-Schughart LA, Weber A, Rehli M, Peuker A, Muller A, Kastenberger M, Brockhoff G, Andreesen R, Kreutz M: Expression of CD68 in non-myeloid cell types. Scand J Immunol 2008; 67:453-463.
35. La Rocca G, Anzalone R, Farina F: The expression of CD68 in human umbilical cord mesenchymal stem cells: new evidences of presence in non-myeloid cell types. Scand J Immunol 2009; 70:161-162.
36. Castellucci MKP: Basic structure of villous trees. In: Pathology of the Human Placenta, 4th edn., Benirschke K, Kaufmann P (eds). New York, Springer-Verlag, 2000, pp 50-52.
37. Georgiades P, Ferguson-Smith AC, Burton GJ: Comparative developmental anatomy of the murine and human definitive placentae. Placenta 2002; 23:3-19.
38. Castellucci M, Zaccheo D, Pescetto G: A three-dimensional study of the normal human placental villous core. I. The Hofbauer cells. Cell Tissue Res 1980; 210:235-247.
39. Van Gorp H, Delputte PL, Nauwynck HJ: Scavenger receptor CD163, a Jack-of-all-trades and potential target for cell-directed therapy. Mol Immunol 2010; 47:1650-1660.
40. Lim R, Lappas M: Decreased expression of complement 3a receptor (C3aR) in human placentas from severe preeclamptic pregnancies. Eur J Obstet Gynecol Reprod Biol 2012; 165:194-198.
41. 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; 32:380-385.
42. Seval Y, Korgun ET, Demir R: Hofbauer cells in early human placenta: possible implications in vasculogenesis and angiogenesis. Placenta 2007; 28:841-845.
43. Khan S, Katabuchi H, Araki M, Nishimura R, Okamura H: Human villous macrophage-conditioned media enhance human trophoblast growth and differentiation in vitro. Biol Reprod 2000; 62:1075-1083.
44. Anteby EY, Natanson-Yaron S, Greenfield C, Goldman-Wohl D, Haimov-Kochman R, Holzer H, Yagel S: Human placental Hofbauer cells express sprouty proteins: a possible modulating mechanism of villous branching. Placenta 2005; 26:476-483.
45. Ingman K, Cookson VJ, Jones CJ, Aplin JD: Characterisation of Hofbauer cells in first and second trimester placenta: incidence, phenotype, survival in vitro and motility. Placenta 2010; 31:535-544.
46. Sica A, Mantovani A: Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122:787-795.
47. Tang Z, Abrahams VM, Mor G, Guller S: Placental Hofbauer cells and complications of pregnancy. Ann N Y Acad Sci 2011; 1221:103-108.
48. Kim JS, Romero R, Kim MR, Kim YM, Friel L, Espinoza J, Kim CJ: Involvement of Hofbauer cells and maternal T cells in villitis of unknown aetiology. Histopathology 2008; 52:457-464.
49. Kim MJ, Romero R, Kim CJ, Tarca AL, Chhauy S, LaJeunesse C, Lee DC, Draghici S, Gotsch F, Kusanovic JP, Hassan SS, Kim JS: 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; 182:3919-3927.
50. Redline RW: Placental inflammation. Semin Neonatol 2004; 9:265-274.
51. Toti PAF, Arcuri F, Tang Z, Schatz F, Zambrano E, Mor G, Niven-Fairchild T, Abrahams VM, Krikun G, Lockwood CJ, Guller S: Focal increases of fetal macrophages in placentas from pregnancies with histological chorioamnionitis: potential role of fibroblast monocyte chemotactic protein-1. Am J Reprod Immunol 2011; 65:470-479.
52. Hung TH, Chen SF, Hsu JJ, Hsieh CC, Hsueh S, Hsieh TT: Tumour necrosis factor-alpha converting enzyme in human gestational tissues from pregnancies complicated by chorioamnionitis. Placenta 2006; 27:996-1006.
53. Vinnars MT, Rindsjo E, Ghazi S, Sundberg A, Papadogiannakis N: The number of CD68+ (Hofbauer) cells is decreased in placentas with chorioamnionitis and with advancing gestational age. Pediatr Dev Pathol 2010; 13:300-304.
54. Crocker IP, Cooper S, Ong SC, Baker PN: Differences in apoptotic susceptibility of cytotrophoblasts and syncytiotrophoblasts in normal pregnancy to those complicated with preeclampsia and intrauterine growth restriction. Am J Pathol 2003; 162:637-643.
55. DiFederico E, Genbacev O, Fisher SJ: Preeclampsia is associated with widespread apoptosis of placental cytotrophoblasts within the uterine wall. Am J Pathol 1999; 155:293-301.
56. Ishihara N, Matsuo H, Murakoshi H, Laoag-Fernandez JB, Samoto T, Maruo T: Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation. Am J Obstet Gynecol 2002; 186:158-166.
57. Aly AS, Khandelwal M, Zhao J, Mehmet AH, Sammel MD, Parry S: Neutrophils are stimulated by syncytiotrophoblast microvillous membranes to generate superoxide radicals in women with preeclampsia. Am J Obstet Gynecol 2004; 190:252-258.
58. Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CW, Sargent IL, von Dadelszen P: Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta 2006; 27:56-61.
59. Gupta AK, Rusterholz C, Huppertz B, Malek A, Schneider H, Holzgreve W, Hahn S: A comparative study of the effect of three different syncytiotrophoblast micro-particles preparations on endothelial cells. Placenta 2005; 26:59-66.
60. Knight M, Redman CW, Linton EA, Sargent IL: Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies. Br J Obstet Gynaecol 1998; 105:632-640.
61. Anderson UD, Olsson MG, Rutardottir S, Centlow M, Kristensen KH, Isberg PE, Thilaganathan B, Akerstrom B, Hansson SR: Fetal hemoglobin and alpha(1)-microglobulin as first- and early second-trimester predictive biomarkers for preeclampsia. Am J Obstet Gynecol 2011; 204:520.e521-525.
62. Centlow M, Carninci P, Nemeth K, Mezey E, Brownstein M, Hansson SR: Placental expression profiling in preeclampsia: local overproduction of hemoglobin may drive pathological changes. Fertil Steril 2008; 90:1834-1843.
63. Myatt L, Rosenfield RB, Eis AL, Brockman DE, Greer I, Lyall F: Nitrotyrosine residues in placenta. Evidence of peroxynitrite formation and action. Hypertension 1996; 28:488-493.
64. Cervar M, Blaschitz A, Dohr G, Desoye G: Paracrine regulation of distinct trophoblast functions in vitro by placental macrophages. Cell Tissue Res 1999; 295:297-305.
65. Uren SJ, Boyle W: Class II MHC antigen-positive macrophages from human placentae suppress strong MLR and CML reactions. Cell Immunol 1990; 125:235-246.
66. Wetzka B, Clark DE, Charnock-Jones DS, Zahradnik HP, Smith SK: PGE2 and TXA2 production by isolated macrophages from human placenta. Adv Exp Med Biol 1997; 433:403-406.