Macrophages regulate expression of α1,2-fucosyltransferase genes in human endometrial epithelial cells

Molecular Human Reproduction

Volumn 18, Issue 4, 2012, Pages 204-215

  Nakamura, Hitomi ^a,b   Jasper, Melinda J ^a   Hull, M Louise ^a   Aplin, John D ^c   Robertson, Sarah A ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Endometrium; Fucose; Implantation; LIF; Macrophage

Indexed keywords

ALPHA1,2 FUCOSYLTRANSFERASE; FUCOSYLTRANSFERASE; GLYCOPROTEIN; INTERLEUKIN 6; LECTIN; MESSENGER RNA; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL CULTURE; CELL PROLIFERATION; CELL SURFACE; COCULTURE; CONTROLLED STUDY; DOLICHOS BIFLORUS; ENDOMETRIUM; ENDOMETRIUM CELL; EPITHELIUM CELL; FEMALE; FLOW CYTOMETRY; FUCOSYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MACROPHAGE; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ULEX EUROPAEUS;

CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; EMBRYO IMPLANTATION; ENDOMETRIUM; EPITHELIAL CELLS; FEMALE; FUCOSYLTRANSFERASES; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-6; LEUKEMIA INHIBITORY FACTOR; MACROPHAGES; RNA, MESSENGER; U937 CELLS;

DOLICHOS BIFLORUS; ULEX EUROPAEUS;

EID: 84858687278     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gar070     Document Type: Article

References (72)

1. Achache H, Revel A. Endometrial receptivity markers, the journey to successful embryo implantation. Hum Reprod Update 2006;12:731-746.
2. Anegon I, Grolleau D, Soulillou JP. Regulation of HILDA/LIF gene expression in activated human monocytic cells. J Immunol 1991; 147:3973-3980.
3. Aoki D, Kawakami H, Nozawa S, Udagawa Y, Iizuka R, Hirano H. Differences in lectin binding patterns of normal human endometrium between proliferative and secretory phases. Histochemistry 1989; 92:177-184.
4. Aplin JD. Glycans as biochemical markers of human endometrial secretory differentiation. J Reprod Fertil 1991;92:525-541.
5. Aplin JD. MUC-1 glycosylation in endometrium: possible roles of the apical glycocalyx at implantation. Hum Reprod 1999;14(Suppl 2):17-25.
6. Aplin JD. Embryo implantation: the molecular mechanism remains elusive. Reprod Biomed Online 2007;14(Spec No 1):49-55.
7. Aplin JD, Meseguer M, Simon C, Ortiz ME, Croxatto H, Jones CJ. MUC1, glycans and the cell-surface barrier to embryo implantation. Biochem Soc Trans 2001;29:153-156.
8. Arnold JT, Kaufman DG, Seppala M, Lessey BA. Endometrial stromal cells regulate epithelial cell growth in vitro: a new co-culture model. Hum Reprod 2001;16:836-845.
9. Bagchi IC, Cheon YP, Li Q, Bagchi MK. Progesterone receptor-regulated gene networks in implantation. Front Biosci 2003;8:s852-s861.
10. Bhalla AK, Paavonen T, Williams MM, Delves PJ, Lydyard PM. Regulation of interleukin-1 and tumour necrosis factor gene expression in myelomonocytic cell lines by 1,25-dihydroxyvitamin D3. Immunology 1991;72:61-64.
11. Bigsby RM, Bethin KE. Paracrine mediators of endometrial growth and differentiation. In: Aplin JD, Fazleabas AT, Glasser SR, Guidice LC (eds). The Endometrium. London: Informa Healthcare, 2008, 223.
12. Bonatz G, Hansmann ML, Buchholz F, Mettler L, Radzun HJ, Semm K. Macrophage- and lymphocyte-subtypes in the endometrium during different phases of the ovarian cycle. Int J Gynaecol Obstet 1992;37:29-36.
13. Bonello N, Jasper MJ, Norman RJ. Periovulatory expression of intercellular adhesion molecule-1 in the rat ovary. Biol Reprod 2004; 71:1384-1390.
14. Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA, Yoshinaga K. Embryo implantation. Dev Biol 2000;223:217-237.
15. Catalano RD, Johnson MH, Campbell EA, Charnock-Jones DS, Smith SK, Sharkey AM. Inhibition of Stat3 activation in the endometrium prevents implantation: a nonsteroidal approach to contraception. Proc Natl Acad Sci USA 2005;102:8585-8590.
16. Chang PL, Sauer MV. The oocyte donation model: lessons on endometrial receptivity. In: Glasser SR, Aplin JD, Giudice L, Tabibzadeh S. (eds). The Endometrium. London: Taylor and Francis, 2002, 495-509.
17. Charnock-Jones DS, Sharkey AM, Fenwick P, Smith SK. Leukaemia inhibitory factor mRNA concentration peaks in human endometrium at the time of implantation and the blastocyst contains mRNA for the receptor at this time. J Reprod Fertil 1994;101:421-426.
18. Cullinan EB, Abbondanzo SJ, Anderson PS, Pollard JW, Lessey BA, Stewart CL. Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/ paracrine function in regulating embryo implantation. Proc Natl Acad Sci USA 1996;93:3115-3120.
19. de Vries T, Knegtel RM, Holmes EH, Macher BA. Fucosyltransferases: structure/function studies. Glycobiology 2001;11:119R-128R.
20. Dechaud H, Maudelonde T, Daures JP, Rossi JF, Hedon B. Evaluation of endometrial inflammation by quantification of macrophages, T lymphocytes, and interleukin-1 and -6 in human endometrium. J Assist Reprod Genet 1998;15:612-618.
21. Domino SE, Zhang L, Gillespie PJ, Saunders TL, Lowe JB. Deficiency of reproductive tract alpha (1,2)Fucosylated glycans and normal fertility in mice with targeted deletions of the FUT1 or FUT2 alpha (1,2)Fucosyltransferase locus. Mol Cell Biol 2001;21:8336-8345.
22. Edwards RG. Implantation, interception and contraception. Hum Reprod 1994;9:985-995.
23. Etzler ME, Kabat EA. Purification and characterization of a lectin (plant hemagglutinin) with blood group A specificity from Dolichos biflorus. Biochemistry 1970;9:869-877.
24. Fouladi-Nashta AA, Jones CJ, Nijjar N, Mohamet L, Smith A, Chambers I, Kimber SJ. Characterization of the uterine phenotype during the peri-implantation period for LIF-null, MF1 strain mice. Dev Biol 2005; 281:1-21.
25. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005;5:953-964.
26. Haidet J, Cifarelli V, Trucco M, Luppi P. C-peptide reduces pro-inflammatory cytokine secretion in LPS-stimulated U937 monocytes in condition of hyperglycemia. Inflamm Res 2011. Sep 27. Epub ahead of print. doi: 10.1007/s00011-011-0384-8.
27. Hannan NJ, Paiva P, Dimitriadis E, Salamonsen LA. Models for study of human embryo implantation: choice of cell lines? Biol Reprod 2010; 82:235-245.
28. Henry S, Jovall PA, Ghardashkhani S, Elmgren A, Martinsson T, Larson G, Samuelsson B. Structural and immunochemical identification of Le(a), Le(b), H type 1, and related glycolipids in small intestinal mucosa of a group O Le(a-b-) nonsecretor. Glycoconj J 1997;14:209-223.
29. Hoffman LH, Olson GE, Carson DD, Chilton BS. Progesterone and implanting blastocysts regulate Muc1 expression in rabbit uterine epithelium. Endocrinology 1998;139:266-271.
30. Houser BL, Tilburgs T, Hill J, Nicotra ML, Strominger JL. Two unique human decidual macrophage populations. J Immunol 2011; 186:2633-2642.
31. Hudson SN, Seamark RF, Robertson SA. The effect of restricted nutrition on uterine macrophage populations in mice. J Reprod Immunol 1999; 45:31-48.
32. Hunt JS, Robertson SA. Uterine macrophages and environmental programming for pregnancy success. J Reprod Immunol 1996;32:1-25.
33. Ikewaki N, Tamauchi H, Inoko H. Modulation of cell surface antigens and regulation of phagocytic activity mediated by CD11b in the monocyte-like cell line U937 in response to lipopolysaccharide. Tissue Antigens 1993;42:125-132.
34. Imoedemhe DA, Sigue AB, Pacpaco EL, Olazo AB, Luciano EC. A comparative analysis of embryos derived from routine in-vitro fertilization and subzonal microinsemination. Hum Reprod 1995; 10:2970-2975.
35. Jasper MJ, Care AS, Sullivan B, Ingman WV, Aplin JD, Robertson SA. Macrophage-derived LIF and IL1B regulate alpha(1,2)fucosyltransferase 2 (Fut2) expression in mouse uterine epithelial cells during early pregnancy. Biol Reprod 2010;84:179-188.
36. Jeziorska M, Nagase H, Salamonsen LA, Woolley DE. Immunolocalization of the matrix metalloproteinases gelatinase B and stromelysin 1 in human endometrium throughout the menstrual cycle. J Reprod Fertil 1996;107:43-51.
37. Jones CJ, Aplin JD. Glycosylation at the fetomaternal interface: does the glycocode play a critical role in implantation? Glycoconj J 2009; 26:359-366.
38. Jones CJ, Fazleabas AT, McGinlay PB, Aplin JD. Cyclic modulation of epithelial glycosylation in human and baboon (Papio anubis) endometrium demonstrated by the binding of the agglutinin from Dolichos biflorus. Biol Reprod 1998;58:20-27.
39. Kariya M, Kanzaki H, Takakura K, Imai K, Okamoto N, Emi N, Kariya Y, Mori T. Interleukin-1 inhibits in vitro decidualization of human endometrial stromal cells. J Clin Endocrin Metab 1991; 73:1170-1174.
40. Klentzeris LD, Bulmer JN, Warren MA, Morrison L, Li TC, Cooke ID. Lymphoid tissue in the endometrium of women with unexplained infertility: morphometric and immunohistochemical aspects. Hum Reprod 1994;9:646-652.
41. Klentzeris LD, Bulmer JN, Liu DT, Morrison L. Endometrial leukocyte subpopulations in women with endometriosis. Eur J Obstet Gynecol Reprod Biol 1995;63:41-47.
42. Klisch K, Jeanrond E, Pang PC, Pich A, Schuler G, Dantzer V, Kowalewski MP, Dell A. A tetraantennary glycan with bisecting N-acetylglucosamine and the Sd(a) antigen is the predominant N-glycan on bovine pregnancy-associated glycoproteins. Glycobiology 2008;18:42-52.
43. Koren HS, Anderson SJ, Larrick JW. In vitro activation of a human macrophage-like cell line. Nature 1979;279:328-331.
44. Lessey BA. Adhesion molecules and implantation. J Reprod Immunol 2002a; 55:101-112.
45. Lessey BA. Uterine factors in implantation. In: Glasser SR, Aplin JD, Giudice L, Tabibzadeh S. (eds). The Endometrium. London: Taylor and Francis, 2002b, 208-228.
46. Lessey BA, Castelbaum AJ, Sawin SW, Sun J. Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil Steril 1995;63:535-542.
47. Leung PH, Salamonsen LA, Findlay JK. Immunolocalization of inhibin and activin subunits in human endometrium across the menstrual cycle. Hum Reprod 1998;13:3469-3477.
48. Lindenberg S, Sundberg K, Kimber SJ, Lundblad A. The milk oligosaccharide, lacto-N-fucopentaose I, inhibits attachment of mouse blastocysts on endometrial monolayers. J Reprod Fertil 1988; 83:149-158.
49. Lopez-Ferrer A, de Bolos C. The expression of human FUT1 in HT-29/ M3 colon cancer cells instructs the glycosylation of MUC1 and MUC5AC apomucins. Glycoconj J 2002;19:13-21.
50. Ma WG, Song H, Das SK, Paria BC, Dey SK. Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc Natl Acad Sci USA 2003;100:2963-2968.
51. Ma B, Simala-Grant JL, Taylor DE. Fucosylation in prokaryotes and eukaryotes. Glycobiology 2006;16:158R-184R.
52. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 2009; 27:451-483.
53. Marwood M, Visser K, Salamonsen LA, Dimitriadis E. Interleukin-11 and leukemia inhibitory factor regulate the adhesion of endometrial epithelial cells: implications in fertility regulation. Endocrinology 2009; 150:2915-2923.
54. Miller DL, Jones CJ, Aplin JD, Nardo LG. Altered glycosylation in peri-implantation phase endometrium in women with stages III and IV endometriosis. Hum Reprod 2010;25:406-411.
55. Nakamura H, Kimura T, Ogita K, Nakamura T, Takemura M, Shimoya K, Koyama S, Tsujie T, Koyama M, Murata Y. NF-kappaB activation at implantation window of the mouse uterus. Am J Reprod Immunol 2004; 51:16-21.
56. Nakamura H, Kimura T, Koyama S, Ogita K, Tsutsui T, Shimoya K, Taniguchi T, Koyama M, Kaneda Y, Murata Y. Mouse model of human infertility: transient and local inhibition of endometrial STAT-3 activation results in implantation failure. FEBS Lett 2006; 580:2717-2722.
57. Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Am J Obstet Gynecol 1975;122:262-263.
58. 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.
59. Rioux N, Castonguay A. 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone modulation of cytokine release in U937 human macrophages. Cancer Immunol Immunother 2001;49:663-670.
60. Schofield G, Kimber SJ. Leukocyte subpopulations in the uteri of leukemia inhibitory factor knockout mice during early pregnancy. Biol Reprod 2005;72:872-878.
61. Sharkey AM, Smith SK. The endometrium as a cause of implantation failure. Best Pract Res 2003;17:289-307.
62. Simon C, Rubio C, Vidal F, Gimenez C, Moreno C, Parrilla JJ, Pellicer A. Increased chromosome abnormalities in human preimplantation embryos after in-vitro fertilization in patients with recurrent miscarriage. Reprod Fertil Dev 1998;10:87-92.
63. Skovlund VR. ABH and related histo-blood group antigens in normal & malignant human endometrium in relation to genetic and hormonal factors. APMIS 1997;69:1-33.
64. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992;359:76-79.
65. Svensson J, Jenmalm MC, Matussek A, Geffers R, Berg G, Ernerudh J. Macrophages at the Fetal-Maternal Interface Express Markers of Alternative Activation and Are Induced by M-CSF and IL-10. J Immunol 2011;187:3671-3682.
66. Van der Elst J, Van den Abbeel E, Camus M, Smitz J, Devroey P, Van Steirteghem A. Long-term evaluation of implantation of fresh and cryopreserved human embryos following ovarian stimulation with buserelin acetate-human menopausal gonadotrophin (HMG) or clomiphene citrate-HMG. Hum Reprod 1996;11:2097-2106.
67. Vidal F, Gimenez C, Rubio C, Simon C, Pellicer A, Santalo J, Egozcue J. FISH preimplantation diagnosis of chromosome aneuploidy in recurrent pregnancy wastage. J Assist Reprod Genet 1998;15:310-313.
68. Vogiagis D, Marsh MM, Fry RC, Salamonsen LA. Leukaemia inhibitory factor in human endometrium throughout the menstrual cycle. J Endocrinol 1996;148:95-102.
69. White S, Kimber SJ. Changes in alpha (1-2)-fucosyltransferase activity in the murine endometrial epithelium during the estrous cycle, early pregnancy, and after ovariectomy and hormone replacement. Biol Reprod 1994;50:73-81.
70. Yan LM, Lin B, Zhu LC, Hao YY, Qi Y,Wang CZ, Gao S, Liu SC, Zhang SL, Iwamori M. Enhancement of the adhesive and spreading potentials of ovarian carcinoma RMG-1 cells due to increased expression of integrin alpha5beta1 with the Lewis Y-structure on transfection of the alpha1,2-fucosyltransferase gene. Biochimie 2010;92:852-857.
71. Zhang X, Mosser DM. Macrophage activation by endogenous danger signals. J Pathol 2008;214:161-178.
72. Zhang Y, Liu S, Liu Y, Wang Z, Wang X, Yan Q. Overexpression of fucosyltransferase VII (FUT7) promotes embryo adhesion and implantation. Fertil Steril 2008;91:908-914.