Binding of pregnancy-specific glycoprotein 17 to CD9 on macrophages induces secretion of IL-10, IL-6, PGE 2, and TGF-β 1

Journal of Leukocyte Biology

Volumn 77, Issue 6, 2005, Pages 948-957

  Ha, Cam T ^a   Waterhouse, Roseann ^a   Wessells, Jennifer ^b   Wu, Julie A ^a   Dveksler, Gabriela S ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cytokines; Reproductive immunology

Indexed keywords

CD9 ANTIGEN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOOXYGENASE 2; INTERLEUKIN 10; INTERLEUKIN 6; PREGNANCY ASSOCIATED PROTEIN; PREGNANCY ASSOCIATED PROTEIN 17; PROSTAGLANDIN E2; PROTEIN KINASE C INHIBITOR; RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; CONFERENCE PAPER; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME INHIBITION; FEMALE; IMMUNE RESPONSE; INFLAMMATION; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PLACENTA; PREGNANCY; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REPRODUCTION; SIGNAL PROCESSING;

ANIMALS; ANTIGENS, CD; CYCLOOXYGENASE 2; DINOPROSTONE; GLYCOPROTEINS; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-10; INTERLEUKIN-6; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; PREGNANCY PROTEINS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PROTEIN KINASE C; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ANIMALIA; MURINAE;

EID: 20044367301     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0804453     Document Type: Conference Paper

References (58)

1. Bohn, H. (1971) Detection and characterization of pregnancy proteins in the human placenta and their quantitative immunochemical determination in sera from pregnant women. Arch. Gynakol. 210, 440-457.
2. Lin, T. M., Halbert, S. P., Spellacy, W. N. (1974) Measurement of pregnancy-associated plasma proteins during human gestation. J. Clin. Invest. 54, 576-582.
3. Bohn, H., Weinmann, E. (1976) Antifertility effect of an active immunization of monkeys with human pregnancy-specific β 1-glycoprotein (SP1) (author's transl). Arch. Gynakol. 221, 305-312.
4. Hau, J., Gidley-Baird, A. A., Westergaard, J. G., Teisner, B. (1985) The effect on pregnancy of intrauterine administration of antibodies against two pregnancy-associated murine proteins: murine pregnancy-specific β 1-glycoprotein and murine pregnancy-associated α 2-glycoprotein. Biomed. Biochim. Acta 44, 1255-1259.
5. Tamsen, L. (1984) Pregnancy-specific β 1-glycoprotein (SP1) levels measured by nephelometry in serum from women with vaginal bleeding in the first half of pregnancy. Acta Obstet. Gynecol. Scand. 63, 311-315.
6. MacDonald, D. J., Scott, J. M., Gemmell, R. S., Mack, D. S. (1983) A prospective study of three biochemical fetoplacental tests: serum human placental lactogen, pregnancy-specific β 1-glycoprotein, and urinary estrogens, and their relationship to placental insufficiency. Am. J. Obstet. Gynecol. 147, 430-436.
7. Silver, R. M., Heyborne, K. D., Leslie, K. K. (1993) Pregnancy-specific β 1 glycoprotein (SP-1) in maternal serum and amniotic fluid; pre-eclampsia, small for gestational age fetus and fetal distress. Placenta 14, 583-589.
8. Hertz, J. B., Schultz-Larsen, P. (1983) Human placental lactogen, pregnancy-specific β-1-glycoprotein and α-fetoprotein in serum in threatened abortion. Int. J. Gynaecol. Obstet. 21, 111-117.
9. Chan, W. Y., Tease, L. A., Bates Jr., J. M., Borjigin, J., Shupert, W. L. (1988) Pregnancy-specific β 1 glycoprotein in rat: tissue distribution of the mRNA and identification of testicular cDNA clones. Hum. Reprod. 3, 687-692.
10. McLellan, A. S., Fischer, B., Hameister, H., Dveksler, G., Hori, T., Wynne, F., Ball, M., Okumura, K., Moore, T., Zimmermann, W. (2005) Structure and evolution of the mouse pregnancy-specific glycoprotein (Psg) gene Locus. BMC Genomics 6, 4.
11. Zhou, G. Q., Hammarstrom, S. (2001) Pregnancy-specific glycoprotein (PSG) in baboon (Papio hamadryas): family size, domain structure, and prediction of a functional region in primate PSGs. Biol. Reprod. 64, 90-99.
12. Snyder, S. K., Wessner, D. H., Wessells, J. L., Waterhouse, R. M., Wahl, L. M., Zimmermann, W., Dveksler, G. S. (2001) Pregnancy-specific glycoproteins function as immunomodulators by inducing secretion of IL-10, IL-6 and TGF-β1 by human monocytes. Am. J. Reprod. Immunol. 45, 205-216.
13. Arnold, L. L., Doherty, T. M., Flor, A. W., Simon, J. A., Chou, J. Y., Chan, W. Y., Mansfield, B. C. (1999) Pregnancy-specific glycoprotein gene expression in recurrent aborters: a potential correlation to interleukin-10 expression. Am. J. Reprod. Immunol. 41, 174-182.
14. Wessells, J., Wessner, D., Parsells, R., White, K., Finkenzeller, D., Zimmermann, W., Dveksler, G. S. (2000) Pregnancy specific glycoprotein 18 induces IL-10 expression in murine macrophages. Eur. J. Immunol. 30, 1830-1840.
15. Waterhouse, R., Ha, C., Dveksler, G. S. (2002) Murine CD9 is the receptor for pregnancy-specific glycoprotein 17. J. Exp. Med. 195, 277-282.
16. Ellerman, D. A., Ha, C., Primakoff, P., Myles, D. G., Dveksler, G. S. (2003) Direct binding of the ligand PSG17 to CD9 requires a CD9 site essential for sperm-egg fusion. Mol. Biol. Cell 14, 5098-5103.
17. Takeda, Y., Tachibana, I., Miyado, K., Kobayashi, M., Miyazaki, T., Funakoshi, T., Kimura, H., Yamane, H., Saito, Y., Goto, H., Yoneda, T., Yoshida, M., Kumagai, T., Osaki, T., Hayashi, S., Kawase, I., Mekada, E. (2003) Tetraspanins CD9 and CD81 function to prevent the fusion of mononuclear phagocytes. J. Cell Biol. 161, 945-956.
18. Le Naour, F., Rubinstein, E., Jasmin, C., Prenant, M., Boucheix, C. (2000) Severely reduced female fertility in CD9-deficient mice. Science 287, 319-321.
19. Maecker, H. T., Levy, S. (1997) Normal lymphocyte development but delayed humoral immune response in CD81-null mice. J. Exp. Med. 185, 1505-1510.
20. Cox, G. W., Mathieson, B. J., Gandino, L., Blasi, E., Radzioch, D., Varesio, L. (1989) Heterogeneity of hematopoietic cells immortalized by v-myc/v-raf recombinant retrovirus infection of bone marrow or fetal liver. J. Natl. Cancer Inst. 81, 1492-1496.
21. Silberstein, E., Dveksler, G. S., Kaplan, G. G. (2001) Neutralization of hepatitis A virus (HAV) by an immunoadhesin containing the cysteine-rich region of HAV cellular receptor-1. J. Virol. 75, 717-725.
22. Van der Pouw Kraan, T. C., Boeije, L. C., Smeenk, R. J., Wijdenes, J., Aarden, L. A. (1995) Prostaglandin-E2 is a potent inhibitor of human interleukin 12 production. J. Exp. Med. 181, 775-779.
23. Demeure, C. E., Yang, L. P., Desjardins, C., Raynauld, P., Delespesse, G. (1997) Prostaglandin E2 primes naive T cells for the production of anti-inflammatory cytokines. Eur. J. Immunol. 27, 3526-3531.
24. Hinz, B., Brune, K., Pahl, A. (2000) Prostaglandin E(2) upregulates cyclooxygenase-2 expression in lipopolysaccharide-stimulated RAW 264.7 macrophages. Biochem. Biophys. Res. Commun. 272, 744-748.
25. Breyer, R. M., Bagdassarian, C. K., Myers, S. A., Breyer, M. D. (2001) Prostanoid receptors: subtypes and signaling. Annu. Rev. Pharmacol. Toxicol. 41, 661-690.
26. Misra, U. K., Akabani, G., Pizzo, S. V. (2002) The role of cAMP-dependent signaling in receptor-recognized forms of α 2-macroglobulin-induced cellular proliferation. J. Biol. Chem. 277, 36509-36520.
27. Gross, A., Bouaboula, M., Casellas, P., Liautard, J. P., Dornand, J. (2003) Subversion and utilization of the host cell cyclic adenosine 5′-monophosphate/protein kinase A pathway by Brucella during macrophage infection. J. Immunol. 170, 5607-5614.
28. Uchiya, K., Groisman, E. A., Nikai, T. (2004) Involvement of Salmonella pathogenicity island 2 in the up-regulation of interleukin-10 expression in macrophages: role of protein kinase A signal pathway. Infect. Immun. 72, 1964-1973.
29. Turner, M., Chantry, D., Feldmann, M. (1990) Transforming growth factor β induces the production of interleukin 6 by human peripheral blood mononuclear cells. Cytokine 2, 211-216.
30. Kitani, A., Fuss, I., Nakamura, K., Kumaki, F., Usui, T., Strober, W. (2003) Transforming growth factor (TGF)-β1-producing regulatory T cells induce Smad-mediated interleukin 10 secretion that facilitates coordinated immunoregulatory activity and amelioration of TGF-β1-mediated fibrosis. J. Exp. Med. 198, 1179-1188.
31. Thellin, O., Coumans, B., Zorzi, W., Igout, A., Heinen, E. (2000) Tolerance to the foeto-placental 'graft': ten ways to support a child for nine months. Curr. Opin. Immunol. 12, 731-737.
32. Wegmann, T. G., Lin, H., Guilbert, L., Mosmann, T. R. (1993) Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol. Today 14, 353-356.
33. Raghupathy, R. (1997) Th1-type immunity is incompatible with successful pregnancy. Immunol. Today 18, 478-482.
34. Chaouat, G., Ledee-Bataille, N., Dubanchet, S., Zourbas, S., Sandra, O., Martal, J. (2004) Reproductive immunology 2003: reassessing the Th1/Th2 paradigm? Immunol. Lett. 92, 207-214.
35. Mackler, A. M., Iezza, G., Akin, M. R., McMillan, P., Yellon, S. M. (1999) Macrophage trafficking in the uterus and cervix precedes parturition in the mouse. Biol. Reprod. 61, 879-883.
36. Croy, B. A., Chantakru, S., Esadeg, S., Ashkar, A. A., Wei, Q. (2002) Decidual natural killer cells: key regulators of placental development (a review). J. Reprod. Immunol. 57, 151-168.
37. Hunt, J. S. (1989) Cytokine networks in the uteroplacental unit: macrophages as pivotal regulatory cells. J. Reprod. Immunol. 16, 1-17.
38. Hunt, J. S., Roberson, S. A. (1996) Uterine macrophages and environmental programming for pregnancy success. J. Reprod. Immunol. 32, 1-25.
39. Boucheix, C., Rubinstein, E. (2001) Tetraspanins. Cell. Mol. Life Sci. 58, 1189-1205.
40. Kaji, K., Oda, S., Miyazaki, S., Kudo, A. (2002) Infertility of CD9-deficient mouse eggs is reversed by mouse CD9, human CD9, or mouse CD81; polyadenylated mRNA injection developed for molecular analysis of sperm-egg fusion. Dev. Biol. 247, 327-334.
41. Pileri, P., Uematsu, Y., Campagnoli, S., Galli, G., Falugi, F., Petracca, R., Weiner, A. J., Houghton, M., Rosa, D., Grandi, G., Abrignani, S. (1998) Binding of hepatitis C virus to CD81. Science 282, 938-941.
42. Chaouat, G., Cayol, V., Mairovitz, V., Dubanchet, S. (1999) Localization of the Th2 cytokines IL-3, IL-4, IL-10 at the fetomaternal interface during human and murine pregnancy and lack of requirement for Fas/Fas ligand interaction for a successful allogeneic pregnancy. Am. J. Reprod. Immunol. 42, 1-13.
43. Xing, Z., Gauldie, J., Cox, G., Baumann, H., Jordana, M., Lei, X. F., Achong, M. K. (1998) IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J. Clin. Invest. 101, 311-320.
44. De, M., Sanford, T. R., Wood, G. W. (1993) Expression of interleukin 1, interleukin 6 and tumor necrosis factor α in mouse uterus during the peri-implantation period of pregnancy. J. Reprod. Fertil. 97, 83-89.
45. Robertson, S. A., Mayrhofer, G., Seamark, R. F. (1992) Uterine epithelial cells synthesize granulocyte-macrophage colony-stimulating factor and interleukin-6 in pregnant and nonpregnant mice. Biol. Reprod. 46, 1069-1079.
46. Liang, L., Kover, K., Dey, S. K., Andrews, G. K. (1996) Regulation of interleukin-6 and interleukin-1 β gene expression in the mouse deciduum. J. Reprod. Immunol. 30, 29-52.
47. Nishino, E., Matsuzaki, N., Masuhiro, K., Kameda, T., Taniguchi, T., Takagi, T., Saji, F., 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.
48. Williams, J. A., Pontzer, C. H., Shacter, E. (2000) Regulation of macrophage interleukin-6 (IL-6) and IL-10 expression by prostaglandin E2: the role of p38 mitogen-activated protein kinase. J. Interferon Cytokine Res. 20, 291-298.
49. Mestre, J. R., Mackrell, P. J., Rivadeneira, D. E., Stapleton, P. P., Tanabe, T., Daly, J. M. (2001) Redundancy in the signaling pathways and promoter elements regulating cyclooxygenase-2 gene expression in endotoxin-treated macrophage/monocytic cells. J. Biol. Chem. 276, 3977-3982.
50. Uchiya, K., Groisman, E. A., Nikai, T. (2004) Involvement of Salmonella pathogenicity island 2 in the up-regulation of interleukin-10 expression in macrophages: role of protein kinase A signal pathway. Infect. Immun. 72, 1964-1973.
51. Platzer, C., Meisel, C., Vogt, K., Platzer, M., Volk, H. D. (1995) Up-regulation of monocytic IL-10 by tumor necrosis factor-α and cAMP elevating drugs. Int. Immunol. 7, 517-523.
52. Platzer, C., Fritsch, E., Elsner, T., Lehmann, M. H., Volk, H. D., Prosch, S. (1999) Cyclic adenosine monophosphate-responsive elements are involved in the transcriptional activation of the human IL-10 gene in monocytic cells. Eur. J. Immunol. 29, 3098-3104.
53. Turner, M., Chantry, D., Feldmann, M. (1990) Transforming growth factor β induces the production of interleukin 6 by human peripheral blood mononuclear cells. Cytokine 2, 211-216.
54. Maeda, H., Kuwahara, H., Ichimura, Y., Ohtsuki, M., Kurakata, S., Shiraishi, A. (1995) TGF-β enhances macrophage ability to produce IL-10 in normal and tumor-bearing mice. J. Immunol. 155, 4926-4932.
55. Kitani, A., Fuss, I., Nakamura, K., Kumaki, F., Usui, T., Strober, W. (2003) Transforming growth factor (TGF)-β1-producing regulatory T cells induce Smad-mediated interleukin 10 secretion that facilitates coordinated immunoregulatory activity and amelioration of TGF-β1-mediated fibrosis. J. Exp. Med. 198, 1179-1188.
56. Giroux, M., Descoteaux, A. (2000) Cyclooxygenase-2 expression in macrophages: modulation by protein kinase C-α. J. Immunol. 165, 3985-3991.
57. Zhang, X. A., Bontrager, A. L., Hemler, M. E. (2001) Transmembrane-4 superfamily proteins associate with activated protein kinase C (PKC) and link PKC to specific β(1) integrins. J. Biol. Chem. 276, 25005-25013.
58. Taniguchi, H., Kato, N., Otsuka, M., Goto, T., Yoshida, H., Shiratori, Y., Omata, M. (2004) Hepatitis C virus core protein upregulates transforming growth factor-β 1 transcription. J. Med. Virol. 72, 52-59.