Glycodelin-A stimulates interleukin-6 secretion by human monocytes and macrophages through L-selectin and the extracellular signal-regulated kinase pathway

Journal of Biological Chemistry

Volumn 287, Issue 44, 2012, Pages 36999-37009

  Lee, Cheuk Lun ^a   Lam, Eve Y F ^a   Lam, Kevin K W ^a   Koistinen, Hannu ^b   Seppälä, Markku ^b   Ng, Ernest H Y ^a   Yeung, William S B ^a   Chiu, Philip C N ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY PREGNANCY; EXTRACELLULAR SIGNAL-REGULATED KINASE; HUMAN MONOCYTES; IL-6 EXPRESSION; IMMUNE CELLS; INTERLEUKIN-6; L-SELECTIN; MONOCYTES/MACROPHAGES; T CELLS;

BIOCHEMISTRY; BIOLOGY;

OBSTETRICS;

GAMMA INTERFERON; GLYCAN; GLYCODELIN A PROTEIN; GLYCOPROTEIN; INTERLEUKIN 6; L SELECTIN; MITOGEN ACTIVATED PROTEIN KINASE; SIALIC ACID; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVITY; CELL DEATH; CELL FUNCTION; CELL PHAGOCYTOSIS; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; FEMALE; FETOPLACENTAL UNIT; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INTRACELLULAR SIGNALING; MACROPHAGE; MONOCYTE; PREGNANCY DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; REGULATORY MECHANISM; SIALYLATION; T LYMPHOCYTE; TH1 CELL; TH1 TH2 BALANCE;

AMNIOTIC FLUID; CELLS, CULTURED; CYTOKINES; FEMALE; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; INTERLEUKIN-6; L-SELECTIN; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MONOCYTES; PREGNANCY; PREGNANCY PROTEINS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIALIC ACIDS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84868224949     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.385336     Document Type: Article

References (71)

1. Seppälä, M., Taylor, R. N., Koistinen, H., Koistinen, R., and Milgrom, E. (2002) Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation. Endocr. Rev. 23, 401-430
2. Lee, C. L., Lam, K. K., Koistinen, H., Seppälä, M., Kurpisz, M., Fernandez, N., Pang, R. T., Yeung, W. S., and Chiu, P. C. (2011) Glycodelin-A as a paracrine regulator in early pregnancy. J. Reprod. Immunol. 90, 29-34
3. Yaniv, E., Borovsky, Z., Mishan-Eisenberg, G., and Rachmilewitz, J. (2003) Placental protein 14 regulates selective B-cell responses. Cell. Immunol. 222, 156-163
4. Scholz, C., Toth, B., Brunnhuber, R., Rampf, E., Weissenbacher, T., Santoso, L., Friese, K., and Jeschke, U. (2008) Glycodelin-A induces a tolerogenic phenotype in monocyte-derived dendritic cells in vitro. Am. J. Reprod. Immunol. 60, 501-512
5. Lee, C. L., Chiu, P. C., Lam, K. K., Chan, R. W., Chu, I. K., Koistinen, R., Koistinen, H., Seppälä, M., Lee, K. F., and Yeung, W. S. (2010) Glycodelin- A modulates cytokine production of peripheral blood natural killer cells. Fertil. Steril. 94, 769-771
6. Lee, C. L., Chiu, P. C., Lam, K. K., Siu, S. O., Chu, I. K., Koistinen, R., Koistinen, H., Seppälä, M., Lee, K. F., and Yeung, W. S. (2011) Differential actions of glycodelin-A on Th-1 and Th-2 cells: a paracrine mechanism that could produce the Th-2-dominant environment during pregnancy. Hum. Reprod. 26, 517-526
7. Mishan-Eisenberg, G., Borovsky, Z., Weber, M. C., Gazit, R., Tykocinski, M. L., and Rachmilewitz, J. (2004) Differential regulation of Th-1/Th-2 cytokine responses by placental protein 14. J. Immunol. 173, 5524-5530
8. Mackenna, A., Li, T. C., Dalton, C., Bolton, A., and Cooke, I. (1993) Placental protein 14 levels in uterine flushing and plasma of women with unexplained infertility. Fertil. Steril. 59, 577-582
9. Mor, G., and Abrahams, V. M. (2003) Potential role of macrophages as immunoregulators of pregnancy. Reprod. Biol. Endocrinol. 1, 119
10. Renaud, S. J., and Graham, C. H. (2008) The role of macrophages in uteroplacental interactions during normal and pathological pregnancy. Immunol. Invest. 37, 535-564
11. Duclos, A. J., Haddad, E. K., and Baines, M. G. (1995) Presence of activated macrophages in a murine model of early embryo loss. Am. J. Reprod. Immunol. 33, 354-366
12. Lee, C. L., Pang, P. C., Yeung, W. S., Tissot, B., Panico, M., Lao, T. T., Chu, I. K., Lee, K. F., Chung, M. K., Lam, K. K., Koistinen, R., Koistinen, H., Seppälä, M., Morris, H. R., Dell, A., and Chiu, P. C. (2009) Effects of differential glycosylation of glycodelins on lymphocyte survival. J. Biol. Chem. 284, 15084-15096
13. Chiu, P. C., Chung, M. K., Koistinen, R., Koistinen, H., Seppälä, M., Ho, P. C., Ng, E. H., Lee, K. F., and Yeung, W. S. (2007) Glycodelin-A interacts with fucosyltransferase on human sperm plasma membrane to inhibit spermatozoa-zona pellucida binding. J. Cell Sci. 120, 33-44
14. Lam, K. K., Chiu, P. C., Lee, C. L., Pang, R. T., Leung, C. O., Koistinen, H., Seppälä, M., Ho, P. C., and Yeung, W. S. (2011) Glycodelin-A protein interacts with siglec-6 protein to suppress trophoblast invasiveness by down-regulating extracellular signal-regulated kinase (ERK)/c-Jun signaling pathway. J. Biol. Chem. 286, 37118-37127
15. Lee, C. L., Chiu, P. C., Pang, P. C., Chu, I. K., Lee, K. F., Koistinen, R., Koistinen, H., Seppälä, M., Morris, H. R., Tissot, B., Panico, M., Dell, A., and Yeung, W. S. (2011) Glycosylation failure extends to glycoproteins in gestational diabetes mellitus: evidence from reduced α2-6 sialylation and impaired immunomodulatory activities of pregnancy-related glycodelin- A. Diabetes 60, 909-917
16. Riittinen, L., Julkunen, M., Seppälä, M., Koistinen, R., and Huhtala, M. L. (1989) Purification and characterization of endometrial protein PP14 from mid-trimester amniotic fluid. Clin. Chim. Acta 184, 19-29
17. So, K. H., Lee, C. L., Yeung, W. S., and Lee, K. F. (2012) Glycodelin suppresses endometrial cell migration and invasion but stimulates spheroid attachment. Reprod. Biomed. Online 24, 639-645
18. Hashimoto, S., Suzuki, T., Dong, H. Y., Yamazaki, N., and Matsushima, K. (1999) Serial analysis of gene expression in human monocytes and macrophages. Blood 94, 837-844
19. Martínez, E., Sureda, A., Dalmases, C. D., Sánchez, J. A., Amill, B., Tugues, D., Sardá, P., Miralles, A., Brunet, S., Domingo-Albós, A., and García, J. (1996) Mobilization of peripheral blood progenitor cells by cyclophosphamide and rhGM-CSF in multiple myeloma. Bone Marrow Transplant. 18, 1-7
20. Lehtonen, A., Ahlfors, H., Veckman, V., Miettinen, M., Lahesmaa, R., and Julkunen, I. (2007) Gene expression profiling during differentiation of human monocytes to macrophages or dendritic cells. J. Leukoc. Biol. 82, 710-720
21. Ulevitch, R. J. (1993) Recognition of bacterial endotoxins by receptordependent mechanisms. Adv. Immunol. 53, 267-289
22. Vellenga, E., Tuyt, L., Wierenga, B. J., Müller, M., and Dokter, W. (1999) Interleukin-6 production by activated human monocytic cells is enhanced by MK-571, a specific inhibitor of the multidrug resistance protein-1. Br. J. Pharmacol. 127, 441-448
23. Prieto, J., Eklund, A., and Patarroyo, M. (1994) Regulated expression of integrins and other adhesion molecules during differentiation of monocytes into macrophages. Cell. Immunol. 156, 191-211
24. Haugen, T. S., Skjonsberg, O. H., Nakstad, B., and Lyberg, T. (1999) Modulation of adhesion molecule profiles on alveolar macrophages and blood leukocytes. Respiration 66, 528-537
25. Vigne, J. L., Hornung, D., Mueller, M. D., and Taylor, R. N. (2001) Purification and characterization of an immunomodulatory endometrial protein, glycodelin. J. Biol. Chem. 276, 17101-17105
26. Alok, A., Mukhopadhyay, D., and Karande, A. A. (2009) Glycodelin-A, an immunomodulatory protein in the endometrium, inhibits proliferation and induces apoptosis in monocytic cells. Int. J. Biochem. Cell Biol. 41, 1138-1147
27. Tseng, S. S., Van Duuren, B. L., and Solomon, J. J. (1977) Synthesis of 4a α-phorbol 9-myristate 9a-acetate and related esters. J. Org. Chem. 42, 3645-3649
28. Kohro, T., Tanaka, T., Murakami, T., Wada, Y., Aburatani, H., Hamakubo, T., and Kodama, T. (2004)Acomparison of differences in the gene expression profiles of phorbol 12-myristate 13-acetate-differentiated THP-1 cells and human monocyte-derived macrophage. J. Atheroscler. Thromb. 11, 88-97
29. Daigneault, M., Preston, J. A., Marriott, H. M., Whyte, M. K., and Dockrell, D. H. (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS ONE 5, e8668
30. Mukhopadhyay, D., Sundereshan, S., Rao, C., and Karande, A. A. (2001) Placental protein 14 induces apoptosis in T-cells but not in monocytes. J. Biol. Chem. 276, 28268-28273
31. Tee, M. K., Vigne, J. L., Yu, J., and Taylor, R. N. (2008) Natural and recombinant human glycodelin activate a pro-apoptotic gene cascade in monocyte cells. J. Leukoc. Biol. 83, 843-852
32. Seppälä, M., Koistinen, H., Koistinen, R., Chiu, P. C., and Yeung, W. S. (2007) Glycosylation-related actions of glycodelin: gamete, cumulus cell, immune cell, and clinical associations. Hum. Reprod. Update 13, 275-287
33. Link, A., Hummel, B., Schwerdt, H., Schwamborn, J., Jung, F., and Schieffer, H. (1997) Influence of neutrophil separation on the expression of adhesion molecules. Clin. Hemorheol. Microcirc. 17, 175-180
34. Breckpot, K., Corthals, J., Heirman, C., Bonehill, A., Michiels, A., Tuyaerts, S., De Greef, C., and Thielemans, K. (2004) Activation of monocytes via the CD14 receptor leads to the enhanced lentiviral transduction of immature dendritic cells. Hum. Gene Ther. 15, 562-573
35. Jauniaux, E., Gulbis, B., Schandene, L., Collette, J., and Hustin, J. (1996) Distribution of interleukin-6 in maternal and embryonic tissues during the first trimester. Mol. Hum. Reprod. 2, 239-243
36. Dimitriadis, E., White, C. A., Jones, R. L., and Salamonsen, L. A. (2005) Cytokines, chemokines, and growth factors in endometrium related to implantation. Hum. Reprod. Update 11, 613-630
37. Li, C., Houser, B. L., Nicotra, M. L., and Strominger, J. L. (2009) HLA-G homodimer-induced cytokine secretion through HLA-G receptors on human decidual macrophages and natural killer cells. Proc. Natl. Acad. Sci. U.S.A. 106, 5767-5772
38. Houser, B. L., Tilburgs, T., Hill, J., Nicotra, M. L., and Strominger, J. L. (2011) Two unique human decidual macrophage populations. J. Immunol. 186, 2633-2642
39. Laird, S. M., Tuckerman, E., Li, T. C., and Bolton, A. E. (1994) Stimulation of human endometrial epithelial cell interleukin-6 production by interleukin- 1 and placental protein 14. Hum. Reprod. 9, 1339-1343
40. Silver, R. M., Schwinzer, B., and McGregor, J. A. (1993) Interleukin-6 levels in amniotic fluid in normal and abnormal pregnancies: preeclampsia, small-for-gestational-age fetus, and premature labor. Am. J. Obstet. Gynecol. 169, 1101-1105
41. Meisser, A., Cameo, P., Islami, D., Campana, A., and Bischof, P. (1999) Effects of interleukin-6 (IL-6) on cytotrophoblastic cells. Mol. Hum. Reprod. 5, 1055-1058
42. Smith, S. D., Dunk, C. E., Aplin, J. D., Harris, L. K., and Jones, R. L. (2009) Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy. Am. J. Pathol. 174, 1959-1971
43. Nishino, E., Matsuzaki, N., Masuhiro, K., Kameda, T., Taniguchi, T., Takagi, T., Saji, F., and Tanizawa, O. (1990) Trophoblast-derived interleukin- 6 (IL-6) regulates human chorionic gonadotropin release through IL-6 receptor on human trophoblasts. J. Clin. Endocrinol. Metab. 71, 436-441
44. Dominguez, F., Martínez, S., Quiñonero, A., Loro, F., Horcajadas, J. A., Pellicer, A., and Simón, C. (2008) CXCL10 and IL-6 induce chemotaxis in human trophoblast cell lines. Mol. Hum. Reprod. 14, 423-430
45. Zhao, S., Gu, Y., Dong, Q., Fan, R., and Wang, Y. (2008) Altered interleukin- 6 receptor, IL-6R and gp130, production and expression and decreased SOCS-3 expression in placentas from women with preeclampsia. Placenta 29, 1024-1028
46. Saito, S., Nakashima, A., Shima, T., and Ito, M. (2010) Th-1/Th-2/Th-17 and regulatory T-cell paradigm in pregnancy. Am. J. Reprod. Immunol. 63, 601-610
47. Piccinni, M. P. (2007) Role of T-cell cytokines in decidua and in cumulus oophorus during pregnancy. Gynecol. Obstet. Invest. 64, 144-148
48. Diehl, S., and Rincón, M. (2002) The two faces of IL-6 on Th-1/Th-2 differentiation. Mol. Immunol. 39, 531-536
49. Challis, J. R., Lockwood, C. J., Myatt, L., Norman, J. E., Strauss, J. F., 3rd, and Petraglia, F. (2009) Inflammation and pregnancy. Reprod. Sci. 16, 206-215
50. Murphy, S. P., Tayade, C., Ashkar, A. A., Hatta, K., Zhang, J., and Croy, B. A. (2009) Interferon γ in successful pregnancies. Biol. Reprod. 80, 848-859
51. Laird, S. M., Tuckerman, E. M., Cork, B. A., Linjawi, S., Blakemore, A. I., and Li, T. C. (2003) A review of immune cells and molecules in women with recurrent miscarriage. Hum. Reprod. Update 9, 163-174
52. Kim, J. H., Studer, R. K., Vo, N. V., Sowa, G. A., and Kang, J. D. (2009) p38 MAPKinhibition selectively mitigates inflammatory mediators and VEGF production in AF cells co-cultured with activated macrophage-like THP-1 cells. Osteoarthritis Cartilage 17, 1662-1669
53. Olsnes, C., Olofsson, J., and Aarstad, H. J. (2011) MAPKs ERK and p38, but not JNK phosphorylation, modulate IL-6 and TNF-α secretion following OK-432 in vitro stimulation of purified human monocytes. Scand. J. Immunol. 74, 114-125
54. Libermann, T. A., and Baltimore, D. (1990) Activation of interleukin-6 gene expression through the NF-κB transcription factor. Mol. Cell. Biol. 10, 2327-2334
55. Chiu, P. C., Wong, B. S., Lee, C. L., Lam, K. K., Chung, M. K., Lee, K. F., Koistinen, R., Koistinen, H., Gupta, S. K., Seppälä, M., and Yeung, W. S. (2010) Zona pellucida-induced acrosome reaction in human spermatozoa is potentiated by glycodelin-A via down-regulation of extracellular signalregulated kinases and up-regulation of zona pellucida-induced calcium influx. Hum. Reprod. 25, 2721-2733
56. Varki, A. (2009) Essentials of Glycobiology, 2nd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
57. Rachmilewitz, J., Borovsky, Z., Riely, G. J., Miller, R., and Tykocinski, M. L. (2003) Negative regulation of T-cell activation by placental protein 14 is mediated by the tyrosine phosphatase receptor CD45. J. Biol. Chem. 278, 14059-14065
58. Poornima, B. L., and Karande, A. A. (2007) Differential sialylation regulates the apoptotic activity of glycodelin-A. FEBS Lett. 581, 4366-4370
59. Lam, K. K., Chiu, P. C., Chung, M. K., Lee, C. L., Lee, K. F., Koistinen, R., Koistinen, H., Seppälä, M., Ho, P. C., and Yeung, W. S. (2009) Glycodelin- A as a modulator of trophoblast invasion. Hum. Reprod. 24, 2093-2103
60. Chiu, P. C., Chung, M. K., Koistinen, R., Koistinen, H., Seppälä, M., Ho, P. C., Ng, E. H., Lee, K. F., and Yeung, W. S. (2007) Cumulus oophorusassociated glycodelin-C displaces sperm-bound glycodelin-A and -F and stimulates spermatozoa-zona pellucida binding. J. Biol. Chem. 282, 5378-5388
61. Yeung, W. S., Lee, K. F., Koistinen, R., Koistinen, H., Seppälä, M., and Chiu, P. C. (2009) Effects of glycodelins on functional competence of spermatozoa. J. Reprod. Immunol. 83, 26-30
62. Crocker, P. R., Paulson, J. C., and Varki, A. (2007) Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7, 255-266
63. Patel, K. D., Cuvelier, S. L., and Wiehler, S. (2002) Selectins: critical mediators of leukocyte recruitment. Semin. Immunol. 14, 73-81
64. Juliano, R. L. (2002) Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin superfamily members. Annu. Rev. Pharmacol. Toxicol. 42, 283-323
65. Crockett-Torabi, E. (1998) Selectins and mechanisms of signal transduction. J. Leukoc. Biol. 63, 1-14
66. Grailer, J. J., Kodera, M., and Steeber, D. A. (2009) L-selectin: role in regulating homeostasis and cutaneous inflammation. J. Dermatol. Sci. 56, 141-147
67. Laudanna, C., Constantin, G., Baron, P., Scarpini, E., Scarlato, G., Cabrini, G., Dechecchi, C., Rossi, F., Cassatella, M. A., and Berton, G. (1994) Sulfatides trigger increase of cytosolic free calcium and enhanced expression of tumor necrosis factor-α and interleukin-8 mRNA in human neutro- phils. Evidence for a role of L-selectin as a signaling molecule. J. Biol. Chem. 269, 4021-4026
68. Po, J. L., Mazer, B., and Jensen, G. S. (1995) The L-selectin antibody FMC46 mediates rapid, transient increase in intracellular calcium in human peripheral blood mononuclear cells and Daudi lymphoma cells. Biochem. Biophys. Res. Commun. 217, 1145-1150
69. Waddell, T. K., Fialkow, L., Chan, C. K., Kishimoto, T. K., and Downey, G. P. (1995) Signaling functions of L-selectin. Enhancement of tyrosine phosphorylation and activation of MAP kinase. J. Biol. Chem. 270, 15403-15411
70. Smolen, J. E., Petersen, T. K., Koch, C., O'Keefe, S. J., Hanlon, W. A., Seo, S., Pearson, D., Fossett, M. C., and Simon, S. I. (2000) L-selectin signaling of neutrophil adhesion and degranulation involves p38 mitogen-activated protein kinase. J. Biol. Chem. 275, 15876-15884
71. lck. Proc. Natl. Acad. Sci. U.S.A. 93, 15376-15381