Enhancement of cortisol-induced SAA1 transcription by SAA1 in the human amnion

in Journal of Molecular Endocrinology

Correspondence should be addressed to K Sun: sungangrenji@hotmail.com
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Our previous studies have demonstrated that human fetal membranes are capable of de novo synthesis of serum amyloid A1 (SAA1), an acute phase protein of inflammation, wherein SAA1 may participate in parturition by inducing a number of inflammation mediators including interleukine-1β, interleukine-6 and prostaglandin E2. However, the regulation of SAA1 expression in the fetal membranes remains largely unknown. In the current study, we examined the regulation of SAA1 expression by cortisol, a crucial steroid produced locally in the fetal membranes at parturition, and the interaction between cortisol and SAA1 in the feed-forward induction of SAA1 expression in human amnion fibroblasts. Results showed that cortisol-induced SAA1 expression in a concentration-dependent manner, which was greatly enhanced by SAA1 despite modest induction of SAA1 expression by itself. Mechanism studies revealed that the induction of SAA1 expression by cortisol and SAA1 was blocked by either the transcription factor STAT3 antagonist AZD0530 or siRNA-mediated knockdown of STAT3. Furthermore, cortisol- and SAA1-induced STAT3 phosphorylation in a sequential order with the induction by SAA1 preceding the induction by cortisol. However, combination of cortisol and SAA1 failed to further intensify the phosphorylation of STAT3. Consistently, cortisol and SAA1 increased the enrichment of STAT3 at the SAA1 promoter. Taking together, this study has demonstrated that cortisol and SAA1 can reinforce each other in the induction of SAA1 expression through sequential phosphorylation of STAT3. The enhancement of cortisol-induced SAA1 expression by SAA1 may lead to excessive SAA1 accumulation resulting in parturition-associated inflammation in the fetal membranes.

 

      Society for Endocrinology

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  • BarnesPJ 2010 Mechanisms and resistance in glucocorticoid control of inflammation. Journal of Steroid Biochemistry and Molecular Biology 120 7685. (https://doi.org/10.1016/j.jsbmb.2010.02.018)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • BlencoweHCousensSOestergaardMZChouDMollerABNarwalRAdlerAVera GarciaCRohdeSSayL 2012 National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 379 21622172. (https://doi.org/10.1016/S0140-6736(12)60820-4)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • ChallisJRLyeSJGibbW 1997 Prostaglandins and parturition. Annals of the New York Academy of Sciences 828 254267. (https://doi.org/10.1111/j.1749-6632.1997.tb48546.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • ConnollyMRooneyPRMcGarryTMarathaAXMcCormickJMigginSMVealeDJFearonU 2016 Acute serum amyloid A is an endogenous TLR2 ligand that mediates inflammatory and angiogenic mechanisms. Annals of the Rheumatic Diseases 75 13921398. (https://doi.org/10.1136/annrheumdis-2015-207655)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • DarnellJEJr 1997 STATs and gene regulation. Science 277 16301635. (https://doi.org/10.1126/science.277.5332.1630)

  • De BuckMGouwyMWangJMVan SnickJProostPStruyfSVan DammeJ 2016 The cytokine-serum amyloid A-chemokine network. Cytokine and Growth Factor Reviews 30 5569. (https://doi.org/10.1016/j.cytogfr.2015.12.010)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • EconomopoulosPSunMPurginaBGibbW 1996 Glucocorticoids stimulate prostaglandin H synthase type-2 (PGHS-2) in the fibroblast cells in human amnion cultures. Molecular and Cellular Endocrinology 117 141147. (https://doi.org/10.1016/0303-7207(95)03739-X)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • GabayCKushnerI 1999 Acute-phase proteins and other systemic responses to inflammation. New England Journal of Medicine 340 448454. (https://doi.org/10.1056/NEJM199902113400607)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • GibbW 1998 The role of prostaglandins in human parturition. Annals of Medicine 30 235241. (https://doi.org/10.3109/07853899809005850)

  • HagiharaKNishikawaTSugamataYSongJIsobeTTagaTYoshizakiK 2005 Essential role of STAT3 in cytokine-driven NF-kappaB-mediated serum amyloid A gene expression. Genes to Cells 10 10511063. (https://doi.org/10.1111/j.1365-2443.2005.00900.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HansenMTForstBCremersNQuagliataLAmbartsumianNGrum-SchwensenBKlingelhoferJAbdul-AlAHerrmannPOsterlandM 2015 A link between inflammation and metastasis: serum amyloid A1 and A3 induce metastasis, and are targets of metastasis-inducing S100A4. Oncogene 34 424435. (https://doi.org/10.1038/onc.2013.568)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • HershkovizRPreciado-PattLLiderOFridkinMDastychJMetcalfeDDMekoriYA 1997 Extracellular matrix-anchored serum amyloid A preferentially induces mast cell adhesion. American Journal of Physiology 273 C179C187. (https://doi.org/10.1152/ajpcell.1997.273.1.C179)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • KumonYSuehiroTHashimotoKSipeJD 2001 Dexamethasone, but not IL-1 alone, upregulates acute-phase serum amyloid A gene expression and production by cultured human aortic smooth muscle cells. Scandinavian Journal of Immunology 53 712. (https://doi.org/10.1046/j.1365-3083.2001.00829.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • LeungMPThompsonBBlackJDaiSAlsweilerJM 2018 The effects of preterm birth on visual development. Clinical and Experimental Optometry 101 412. (https://doi.org/10.1111/cxo.12578)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • LiWGaoLWangYDuanTMyattLSunK 2006 Enhancement of cortisol-induced 11beta-hydroxysteroid dehydrogenase type 1 expression by interleukin 1beta in cultured human chorionic trophoblast cells. Endocrinology 147 24902495. (https://doi.org/10.1210/en.2005-1626)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • LiWWangWZuoRLiuCShuQYingHSunK 2017 Induction of pro-inflammatory genes by serum amyloid A1 in human amnion fibroblasts. Scientific Reports 7 693. (https://doi.org/10.1038/s41598-017-00782-9)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • LiuCGuoCWangWZhuPLiWMiYMyattLSunK 2016 Inhibition of lysyl oxidase by cortisol regeneration in human amnion: implications for rupture of fetal membranes. Endocrinology 157 40554065. (https://doi.org/10.1210/en.2016-1406)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • MacLennanAHThompsonSCGeczJ 2015 Cerebral palsy: causes, pathways, and the role of genetic variants. American Journal of Obstetrics and Gynecology 213 779788. (https://doi.org/10.1016/j.ajog.2015.05.034)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • MauryCPEhnholmCLukkaM 1985 Serum amyloid A protein (SAA) subtypes in acute and chronic inflammatory conditions. Annals of the Rheumatic Diseases 44 711715. (https://doi.org/10.1136/ard.44.10.711)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • MiYWangWLuJZhangCWangYYingHSunK 2018 Proteasome-mediated degradation of collagen III by cortisol in amnion fibroblasts. Journal of Molecular Endocrinology 60 4554. (https://doi.org/10.1530/JME-17-0215)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • MiYWangWZhangCLiuCLuJLiWZuoRMyattLSunK 2017 Autophagic degradation of Collagen 1A1 by cortisol in human amnion fibroblasts. Endocrinology 158 10051014. (https://doi.org/10.1210/en.2016-1829)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • MitchellMDRomeroRJEdwinSSTrautmanMS 1995 Prostaglandins and parturition. Reproduction Fertility and Development 7 623632. (https://doi.org/10.1071/RD9950623)

  • MurphyBE 1977 Chorionic membrane as an extra-adrenal source of foetal cortisol in human amniotic fluid. Nature 266 179181. (https://doi.org/10.1038/266179a0)

  • MurphyBE 1981 Ontogeny of cortisol-cortisone interconversion in human tissues: a role for cortisone in human fetal development. Journal of Steroid Biochemistry 14 811817. (https://doi.org/10.1016/0022-4731(81)90226-0)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • OlsonDM 2003 The role of prostaglandins in the initiation of parturition. Best Practice and Research: Clinical Obstetrics and Gynaecology 17 717730. (https://doi.org/10.1016/S1521-6934(03)00069-5)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • PatelHFellowesRCoadeSWooP 1998 Human serum amyloid A has cytokine-like properties. Scandinavian Journal of Immunology 48 410418. (https://doi.org/10.1046/j.1365-3083.1998.00394.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • RomeroREspinozaJKusanovicJPGotschFHassanSErezOChaiworapongsaTMazorM 2006 The preterm parturition syndrome. British Journal of Obstetrics and Gynaecology 113 (Supplement 3) 1742. (https://doi.org/10.1111/j.1471-0528.2006.01120.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • SunKHePYangK 2002 Intracrine induction of 11beta-hydroxysteroid dehydrogenase type 1 expression by glucocorticoid potentiates prostaglandin production in the human chorionic trophoblast. Biology of Reproduction 67 14501455. (https://doi.org/10.1095/biolreprod.102.005892)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • SunKMaRCuiXCamposBWebsterRBrockmanDMyattL 2003 Glucocorticoids induce cytosolic phospholipase A2 and prostaglandin H synthase type 2 but not microsomal prostaglandin E synthase (PGES) and cytosolic PGES expression in cultured primary human amnion cells. Journal of Clinical Endocrinology and Metabolism 88 55645571. (https://doi.org/10.1210/jc.2003-030875)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • SunKMyattL 2003 Enhancement of glucocorticoid-induced 11beta-hydroxysteroid dehydrogenase type 1 expression by proinflammatory cytokines in cultured human amnion fibroblasts. Endocrinology 144 55685577. (https://doi.org/10.1210/en.2003-0780)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • SunLYeRD 2016 Serum amyloid A1: structure, function and gene polymorphism. Gene 583 4857. (https://doi.org/10.1016/j.gene.2016.02.044)

  • ThornCFWhiteheadAS 2002 Differential glucocorticoid enhancement of the cytokine-driven transcriptional activation of the human acute phase serum amyloid A genes, SAA1 and SAA2. Journal of Immunology 169 399406. (https://doi.org/10.4049/jimmunol.169.1.399)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • TiwariPTripathiLPNishikawa-MatsumuraTAhmadSSongSNIsobeTMizuguchiKYoshizakiK 2013 Prediction and experimental validation of a putative non-consensus binding site for transcription factor STAT3 in serum amyloid A gene promoter. Biochimica and Biophysica Acta 1830 36503655. (https://doi.org/10.1016/j.bbagen.2013.01.024)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • WangWChenZJMyattLSunK 2018 11beta-HSD1 in human fetal membranes as a potential therapeutic target for preterm birth. Endocrine Reviews 39 241260. (https://doi.org/10.1210/er.2017-00188)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • WangWGuoCZhuPLuJLiWLiuCXieHMyattLChenZJSunK 2015 Phosphorylation of STAT3 mediates the induction of cyclooxygenase-2 by cortisol in the human amnion at parturition. Science Signaling 8 ra106. (https://doi.org/10.1126/scisignal.aac6151)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • WangWLiuCSunK 2016 Induction of amnion epithelial apoptosis by cortisol via tPA/plasmin system. Endocrinology 157 44874498. (https://doi.org/10.1210/en.2016-1464)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • YanQSunLZhuZWangLLiSYeRD 2014 Jmjd3-mediated epigenetic regulation of inflammatory cytokine gene expression in serum amyloid A-stimulated macrophages. Cellular Signalling 26 17831791. (https://doi.org/10.1016/j.cellsig.2014.03.025)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • YangZGuoCZhuPLiWMyattLSunK 2007 Role of glucocorticoid receptor and CCAAT/enhancer-binding protein alpha in the feed-forward induction of 11beta-hydroxysteroid dehydrogenase type 1 expression by cortisol in human amnion fibroblasts. Journal of Endocrinology 195 241253. (https://doi.org/10.1677/JOE-07-0303)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • ZakarTHirstJJMijovicJEOlsonDM 1995 Glucocorticoids stimulate the expression of prostaglandin endoperoxide H synthase-2 in amnion cells. Endocrinology 136 16101619. (https://doi.org/10.1210/endo.136.4.7895671)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • ZhangCWangWLiuCLuJSunK 2017 Role of NF-kappaB/GATA3 in the inhibition of lysyl oxidase by IL-1beta in human amnion fibroblasts. Immunology and Cell Biology 95 943952. (https://doi.org/10.1038/icb.2017.73)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • ZhuXOYangZGuoCMNiXTLiJNGeYCMyattLSunK 2009 Paradoxical stimulation of cyclooxygenase-2 expression by glucocorticoids via a cyclic AMP response element in human amnion fibroblasts. Molecular Endocrinology 23 18391849. (https://doi.org/10.1210/me.2009-0201)

    • Crossref
    • Search Google Scholar
    • Export Citation