Seminal fluid factors regulate activin A and follistatin synthesis in female cervical epithelial cells

Molecular and Cellular Endocrinology

Volumn 417, Issue , 2015, Pages 178-190

  Sharkey, David J ^a   Schjenken, John E ^a   Mottershead, David G ^a   Robertson, Sarah A ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Cervical epithelial cells; Cytokines; Inflammation; Seminal fluid

Indexed keywords

ACTIVIN A; FOLLISTATIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; AUTACOID; FST PROTEIN, HUMAN; INHIBIN; INHIBIN BETA A SUBUNIT; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CONTROLLED STUDY; ECT GENE; EPITHELIUM CELL; FEMALE; FST GENE; GENE; GENE IDENTIFICATION; GENE LOCATION; GENE REPRESSION; HORMONE SYNTHESIS; HUMAN; HUMAN CELL; HUMAN TISSUE; INHBA GENE; MICROARRAY ANALYSIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SEMINAL PLASMA; TGFB GENE; UTERINE CERVIX EPITHELIUM; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MALE; METABOLISM; SPERM; UTERINE CERVIX;

CELL LINE; CERVIX UTERI; EPITHELIAL CELLS; FEMALE; FOLLISTATIN; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; INHIBIN-BETA SUBUNITS; LIPOPOLYSACCHARIDES; MALE; SEMEN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84960195933     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.09.022     Document Type: Article

References (76)

1. Abe Y., Marukawa R., Tsuru N., Sato M., Matsuda H., Sadakata H., Kameda T., Minegishi T. Gram-negative bacterial lipopolysaccharide stimulates activin a secretion from human amniotic epithelial cells. Int. J. Endocrinol. 2013, 789012.
2. Abe Y., Komatsubara M., Saito M., Toda M., Shinozaki H., Tamura T., Kasahara Y., Sedakata H., Minegishi T. Activin A is stimulated by tumor necrosis factor-alpha and modulates collagen gene expression in human amniotic cells. J. Endocrinol. Invest. 2013, 36:515-520.
3. Aleman-Muench G.R., Soldevila G. When versatility matters: activins/inhibins as key regulators of immunity. Immunol. Cell Biol. 2012, 90:137-148.
4. Anderson R.A., Evans L.W., Irvine D.S., McIntyre M.A., Groome N.P., Riley S.C. Follistatin and activin A production by the male reproductive tract. Hum. Reprod. 1998, 13:3319-3325.
5. Bernard D.J., Lee K.B., Santos M.M. Activin B can signal through both ALK4 and ALK7 in gonadotrope cells. Reprod. Biol. Endocrinol. 2006, 4:52.
6. Burges A., Shabani N., Bruning A., Mylonas I. Inhibin-betaA and -betaB subunits in normal and malignant glandular epithelium of uterine cervix and HeLa cervical cancer cell line. Arch. Gynecol. Obstet. 2011, 284:981-988.
7. de Jong F.H. Testicular activin-too hot to handle?. Eur. J. Endocrinol. 1997, 137:448-449.
8. Evans L.W., Muttukrishna S., Groome N.P. Development, validation and application of an ultra-sensitive two-site enzyme immunoassay for human follistatin. J. Endocrinol. 1998, 156:275-282.
9. Fichorova R.N., Anderson D.J. Differential expression of immunobiological mediators by immortalized human cervical and vaginal epithelial cells. Biol. Reprod. 1999, 60:508-514.
10. Fichorova R.N., Rheinwald J.G., Anderson D.J. Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissue-specific differentiation proteins. Biol. Reprod. 1997, 57:847-855.
11. Florio P., Severi F.M., Luisi S., Ciarmela P., Calonaci G., Cobellis L., Petraglia F. Endometrial expression and secretion of activin A, but not follistatin, increase in the secretory phase of the menstrual cycle. J. Soc. Gynecol. Investig. 2003, 10:237-243.
12. Florio P., Gabbanini M., Borges L.E., Bonaccorsi L., Pinzauti S., Reis F.M., Boy Torres P., Rago G., Litta P., Petraglia F. Activins and related proteins in the establishment of pregnancy. Reprod. Sci. 2010, 17:320-330.
13. Fujita Y., Mihara T., Okazaki T., Shitanaka M., Kushino R., Ikeda C., Negishi H., Liu Z., Richards J.S., Shimada M. Toll-like receptors (TLR) 2 and 4 on human sperm recognize bacterial endotoxins and mediate apoptosis. Hum. Reprod. 2011, 26:2799-2806.
14. Gribi R., Tanaka T., Harper-Summers R., Yu J. Expression of activin A in inflammatory arthropathies. Mol. Cell Endocrinol. 2001, 180:163-167.
15. Guerin L.R., Moldenhauer L.M., Prins J.R., Bromfield J.J., Hayball J.D., Robertson S.A. Seminal fluid regulates accumulation of FOXP3(+) regulatory T cells in the preimplantation mouse uterus through expanding the FOXP3(+) cell pool and CCL19-mediated recruitment. Biol. Reprod. 2011, 85:397-408.
16. Hashimoto O., Nakamura T., Shoji H., Shimasaki S., Hayashi Y., Sugino H. A novel role of follistatin, an activin-binding protein, in the inhibition of activin action in rat pituitary cells. Endocytotic degradation of activin and its acceleration by follistatin associated with cell-surface heparan sulfate. J. Biol. Chem. 1997, 272:13835-13842.
17. Hashimoto O., Kawasaki N., Tsuchida K., Shimasaki S., Hayakawa T., Sugino H. Difference between follistatin isoforms in the inhibition of activin signalling: activin neutralizing activity of follistatin isoforms is dependent on their affinity for activin. Cell Signal 2000, 12:565-571.
18. Hedger M.P., Winnall W.R., Phillips D.J., de Kretser D.M. The regulation and functions of activin and follistatin in inflammation and immunity. Vitam. Horm. 2011, 85:255-297.
19. Heldin C.H., Miyazono K., ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997, 390:465-471.
20. Hieshima K., Imai T., Opdenakker G., Van Damme J., Kusuda J., Tei H., Sakaki Y., Takatsuki K., Miura R., Yoshie O., Nomiyama H. Molecular cloning of a novel human CC chemokine liver and activation-regulated chemokine (LARC) expressed in liver. Chemotactic activity for lymphocytes and gene localization on chromosome 2. J. Biol. Chem. 1997, 272:5846-5853.
21. Holdsworth-Carson S.J., Craythorn R.G., Winnall W.R., Dhaliwal K., Genovese R., Nowell C.J., Rogers P.A., de Kretser D.M., Hedger M.P., Girling J.E. Follistatin is essential for normal postnatal development and function of mouse oviduct and uterus. Reprod. Fertil. Dev. 2014, 27:985-999.
22. Huber S., Stahl F.R., Schrader J., Luth S., Presser K., Carambia A., Flavell R.A., Werner S., Blessing M., Herkel J., Schramm C. Activin a promotes the TGF-beta-induced conversion of CD4+CD25- T cells into Foxp3+ induced regulatory T cells. J. Immunol. 2009, 182:4633-4640.
23. Hubner G., Brauchle M., Gregor M., Werner S. Activin A: a novel player and inflammatory marker in inflammatory bowel disease?. Lab. Investig. 1997, 77:311-318.
24. Jasper M.J., Tremellen K.P., Robertson S.A. Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol. Hum. Reprod. 2006, 12:301-308.
25. Jones K.L., Brauman J.N., Groome N.P., de Kretser D.M., Phillips D.J. Activin A release into the circulation is an early event in systemic inflammation and precedes the release of follistatin. Endocrinology 2000, 141:1905-1908.
26. Jones R.L., Salamonsen L.A., Findlay J.K. Potential roles for endometrial inhibins, activins and follistatin during human embryo implantation and early pregnancy. Trends Endocrinol. Metab. 2002, 13:144-150.
27. Jones K.L., de Kretser D.M., Patella S., Phillips D.J. Activin A and follistatin in systemic inflammation. Mol. Cell Endocrinol. 2004, 225:119-125.
28. Jones K.L., de Kretser D.M., Clarke I.J., Scheerlinck J.P., Phillips D.J. Characterisation of the rapid release of activin A following acute lipopolysaccharide challenge in the ewe. J. Endocrinol. 2004, 182:69-80.
29. Jones K.L., Mansell A., Patella S., Scott B.J., Hedger M.P., de Kretser D.M., Phillips D.J. Activin A is a critical component of the inflammatory response, and its binding protein, follistatin, reduces mortality in endotoxemia. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:16239-16244.
30. Kariyawasam H.H., Pegorier S., Barkans J., Xanthou G., Aizen M., Ying S., Kay A.B., Lloyd C.M., Robinson D.S. Activin and transforming growth factor-beta signaling pathways are activated after allergen challenge in mild asthma. J. Allergy Clin. Immunol. 2009, 124:454-462.
31. Keelan J.A., Groome N.P., Mitchell M.D. Regulation of activin-A production by human amnion, decidua and placenta in vitro by pro-inflammatory cytokines. Placenta 1998, 19:429-434.
32. Lerch T.F., Shimasaki S., Woodruff T.K., Jardetzky T.S. Structural and biophysical coupling of heparin and activin binding to follistatin isoform functions. J. Biol. Chem. 2007, 282:15930-15939.
33. Leung P.H., Salamonsen L.A., Findlay J.K. Immunolocalization of inhibin and activin subunits in human endometrium across the menstrual cycle. Hum. Reprod. 1998, 13:3469-3477.
34. Loras B., Vetele F., El Malki A., Rollet J., Soufir J.C., Benahmed M. Seminal transforming growth factor-beta in normal and infertile men. Hum. Reprod. 1999, 14:1534-1539.
35. Massague J., Gomis R.R. The logic of TGFbeta signaling. FEBS Lett. 2006, 580:2811-2820.
36. Musso T., Scutera S., Vermi W., Daniele R., Fornaro M., Castagnoli C., Alotto D., Ravanini M., Cambieri I., Salogni L., Elia A.R., Giovarelli M., et al. Activin A induces Langerhans cell differentiation in vitro and in human skin explants. PLoS One 2008, 3:e3271.
37. Nakamura T., Sugino K., Titani K., Sugino H. Follistatin, an activin-binding protein, associates with heparan sulfate chains of proteoglycans on follicular granulosa cells. J. Biol. Chem. 1991, 266:19432-19437.
38. Nocera M., Chu T.M. Transforming growth factor beta as an immunosuppressive protein in human seminal plasma. Am. J. Reprod. Immunol. 1993, 30:1-8.
39. O'Leary S., Jasper M.J., Warnes G.M., Armstrong D.T., Robertson S.A. Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. Reproduction 2004, 128:237-247.
40. O'Leary S., Armstrong D.T., Robertson S.A. Transforming growth factor-beta (TGFbeta) in porcine seminal plasma. Reprod. Fertil. Dev. 2011, 23:748-758.
41. Ochsenkuhn R., O'Connor A.E., Hirst J.J., Gordon Baker H.W., de Kretser D.M., Hedger M.P. The relationship between immunosuppressive activity and immunoregulatory cytokines in seminal plasma: influence of sperm autoimmunity and seminal leukocytes. J. Reprod. Immunol. 2006, 71:57-74.
42. Ogawa K., Funaba M., Chen Y., Tsujimoto M. Activin A functions as a Th2 cytokine in the promotion of the alternative activation of macrophages. J. Immunol. 2006, 177:6787-6794.
43. Pandya I.J., Cohen J. The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil. Steril. 1985, 43:417-421.
44. Petraglia F., Gallinelli A., Grande A., Florio P., Ferrari S., Genazzani A.R., Ling N., DePaolo L.V. Local production and action of follistatin in human placenta. J. Clin. Endocrinol. Metab. 1994, 78:205-210.
45. Phillips D.J., de Kretser D.M. Follistatin: a multifunctional regulatory protein. Front. Neuroendocrinol. 1998, 19:287-322.
46. Phillips D.J., Jones K.L., McGaw D.J., Groome N.P., Smolich J.J., Parsson H., de Kretser D.M. Release of activin and follistatin during cardiovascular procedures is largely due to heparin administration. J. Clin. Endocrinol. Metab. 2000, 85:2411-2415.
47. Phillips D.J., de Kretser D.M., Hedger M.P. Activin and related proteins in inflammation: not just interested bystanders. Cytokine Growth Factor Rev. 2009, 20:153-164.
48. Refaat B., Amer S., Ola B., Chapman N., Ledger W. The expression of activin-betaA- and -betaB-subunits, follistatin, and activin type II receptors in fallopian tubes bearing an ectopic pregnancy. J. Clin. Endocrinol. Metab. 2008, 93:293-299.
49. Rheinwald J.G., Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 1975, 6:331-343.
50. Robertson S.A., Sharkey D.J. The role of semen in induction of maternal immune tolerance to pregnancy. Semin. Immunol. 2001, 13:243-254.
51. Robertson S.A., Mau V.J., Tremellen K.P., Seamark R.F. Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J. Reprod. Fertil. 1996, 107:265-277.
52. Robertson S.A., Mau V.J., Hudson S.N., Tremellen K.P. Cytokine-leukocyte networks and the establishment of pregnancy. Am. J. Reprod. Immunol. 1997, 37:438-442.
53. Robertson S.A., Bromfield J.J., Tremellen K.P. Seminal 'priming' for protection from pre-eclampsia-a unifying hypothesis. J. Reprod. Immunol. 2003, 59:253-265.
54. Robertson S.A., Guerin L.R., Bromfield J.J., Branson K.M., Ahlstrom A.C., Care A.S. Seminal fluid drives expansion of the CD4+CD25+ T regulatory cell pool and induces tolerance to paternal alloantigens in mice. Biol. Reprod. 2009, 80:1036-1045.
55. Robson N.C., Phillips D.J., McAlpine T., Shin A., Svobodova S., Toy T., Pillay V., Kirkpatrick N., Zanker D., Wilson K., Helling I., Wei H., et al. Activin-A: a novel dendritic cell-derived cytokine that potently attenuates CD40 ligand-specific cytokine and chemokine production. Blood 2008, 111:2733-2743.
56. Salogni L., Musso T., Bosisio D., Mirolo M., Jala V.R., Haribabu B., Locati M., Sozzani S. Activin A induces dendritic cell migration through the polarized release of CXC chemokine ligands 12 and 14. Blood 2009, 113:5848-5856.
57. Segerer S.E., Muller N., Brandt J., Kapp M., Dietl J., Reichardt H.M., Rieger L., Kammerer U. The glycoprotein-hormones activin A and inhibin A interfere with dendritic cell maturation. Reprod. Biol. Endocrinol. 2008, 6:17.
58. Seshadri S., Bates M., Vince G., Jones D.I. The role of cytokine expression in different subgroups of subfertile men. Am. J. Reprod. Immunol. 2009, 62:275-282.
59. Sharkey D.J., Macpherson A.M., Tremellen K.P., Robertson S.A. Seminal plasma differentially regulates inflammatory cytokine gene expression in human cervical and vaginal epithelial cells. Mol. Hum. Reprod. 2007, 13:491-501.
60. Sharkey D.J., Tremellen K.P., Jasper M.J., Gemzell-Danielsson K., Robertson S.A. Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J. Immunol. 2012, 188:2445-2454.
61. Sharkey D.J., Macpherson A.M., Tremellen K.P., Mottershead D.G., Gilchrist R.B., Robertson S.A. TGF-beta mediates proinflammatory seminal fluid signaling in human cervical epithelial cells. J. Immunol. 2012, 189:1024-1035.
62. Shimasaki S., Koga M., Esch F., Cooksey K., Mercado M., Koba A., Ueno N., Ying S.Y., Ling N., Guillemin R. Primary structure of the human follistatin precursor and its genomic organization. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:4218-4222.
63. Sierra-Filardi E., Puig-Kroger A., Blanco F.J., Nieto C., Bragado R., Palomero M.I., Bernabeu C., Vega M.A., Corbi A.L. Activin A skews macrophage polarization by promoting a proinflammatory phenotype and inhibiting the acquisition of anti-inflammatory macrophage markers. Blood 2011, 117:5092-5101.
64. Southern P.J., Horbul J.E., Miller B.R., Maher D.M. Coming of age: reconstruction of heterosexual HIV-1 transmission in human ex vivo organ culture systems. Mucosal Immunol. 2011, 4:383-396.
65. Sozzani S., Musso T. The yin and yang of activin A. Blood 2011, 117:5013-5015.
66. Stoitzner P., Stossel H., Wankell M., Hofer S., Heufler C., Werner S., Romani N. Langerhans cells are strongly reduced in the skin of transgenic mice overexpressing follistatin in the epidermis. Eur. J. Cell Biol. 2005, 84:733-741.
67. Thomas T.Z., Wang H., Niclasen P., O'Bryan M.K., Evans L.W., Groome N.P., Pedersen J., Risbridger G.P. Expression and localization of activin subunits and follistatins in tissues from men with high grade prostate cancer. J. Clin. Endocrinol. Metab. 1997, 82:3851-3858.
68. Thompson L.A., Barratt C.L., Bolton A.E., Cooke I.D. The leukocytic reaction of the human uterine cervix. Am. J. Reprod. Immunol. 1992, 28:85-89.
69. Thompson T.B., Lerch T.F., Cook R.W., Woodruff T.K., Jardetzky T.S. The structure of the follistatin: activin complex reveals antagonism of both type I and type II receptor binding. Dev. Cell 2005, 9:535-543.
70. Tsuchida K., Nakatani M., Yamakawa N., Hashimoto O., Hasegawa Y., Sugino H. Activin isoforms signal through type I receptor serine/threonine kinase ALK7. Mol. Cell Endocrinol. 2004, 220:59-65.
71. Tsuchida K., Nakatani M., Uezumi A., Murakami T., Cui X. Signal transduction pathway through activin receptors as a therapeutic target of musculoskeletal diseases and cancer. Endocr. J. 2008, 55:11-21.
72. Vliegen M.K., Schlatt S., Weinbauer G.F., Bergmann M., Groome N.P., Nieschlag E. Localization of inhibin/activin subunits in the testis of adult nonhuman primates and men. Cell Tissue Res. 1993, 273:261-268.
73. WHO WHO Laboratory Manual for the Examination and Processing of Human Semen 2010, World Health Organization, Geneva.
74. Wilson K.M., Smith A.I., Phillips D.J. Stimulatory effects of lipopolysaccharide on endothelial cell activin and follistatin. Mol. Cell Endocrinol. 2006, 253:30-35.
75. Wu H., Chen Y., Winnall W.R., Phillips D.J., Hedger M.P. Regulation of activin A release from murine bone marrow-derived neutrophil precursors by tumour necrosis factor-alpha and insulin. Cytokine 2013, 61:199-204.
76. Zhu J., Li Y., Shen W., Qiao C., Ambrosio F., Lavasani M., Nozaki M., Branca M.F., Huard J. Relationships between transforming growth factor-beta1, myostatin, and decorin: implications for skeletal muscle fibrosis. J. Biol. Chem. 2007, 282:25852-25863.