Prolactin activates IRF1 and leads to altered balance of histone acetylation: Implications for systemic lupus erythematosus

References

• Lim SS, Bayakly AR, Helmick CG, Gordon C, Easley KA, Drenkard C. The incidence and prevalence of systemic lupus erythematosus, 2002-2004: The Georgia Lupus Registry. Arthritis Rheumatol. 2014;66(2):357–68.
   PubMed Web of Science ®Google Scholar
• Miranda JM, Prieto RE, Paniagua R, Garcia G, Amato D, Barile L, et al. Clinical significance of serum and urine prolactin levels in lupus glomerulonephritis. Lupus. 1998;7(6):387–91.
   PubMed Web of Science ®Google Scholar
• Jara LJ, Gomez-Sanchez C, Silveira LH, Martinez-Osuna P, Vasey FB, Espinoza LR. Hyperprolactinemia in systemic lupus erythematosus: association with disease activity. Am J Med Sci. 1992;303(4):222–6.
   PubMed Web of Science ®Google Scholar
• Fojtikova M, Tomasova Studynkova J, Filkova M, Lacinova Z, Gatterova J, Pavelka K, et al. Elevated prolactin levels in patients with rheumatoid arthritis: association with disease activity and structural damage. Clin Exp Rheumatol. 2010;28:849–54.
   PubMed Web of Science ®Google Scholar
• El Miedany YM, Ahmed I, Moustafa H, El Baddini M. Hyperprolactinemia in Sjogren's syndrome: a patient subset or a disease manifestation? Joint Bone Spine. 2004;71(3):203–8.
   PubMed Web of Science ®Google Scholar
• Sayki Arslan M, Sahin M, Topaloglu O, Tutal E, Karakose M, Gungunes A, et al. Hyperprolactinaemia associated with increased thyroid volume and autoimmune thyroiditis in patients with prolactinoma. Clin Endocrinol. 2013;79(6):882–6.
   PubMed Web of Science ®Google Scholar
• Harris SM, Leong HM, Chowdhury R, Ellis C, Brennan J, Scobie IN. Concomitant myasthenia gravis and macroprolactinoma: the immunomodulatory role of prolactin and its potential therapeutic use. Endocrine. 2014;45(1):9–14.
   PubMed Web of Science ®Google Scholar
• Perimenis P, Bouckenooghe T, Delplanque J, Moitrot E, Eury E, Lobbens S, et al. Placental antiangiogenic prolactin fragments are increased in human and rat maternal diabetes. Biochim Biophys Acta. 2014;1842(9):1783–93.
   PubMed Web of Science ®Google Scholar
• Tripathi A, Sodhi A. Prolactin-induced production of cytokines in macrophages in vitro involves JAK/STAT and JNK MAPK pathways. Int Immunol. 2008;20(3):327–36.
   PubMed Web of Science ®Google Scholar
• Matera L, Contarini M, Bellone G, Forno B, Biglino A. Up-modulation of interferon-gamma mediates the enhancement of spontanous cytotoxicity in prolactin-activated natural killer cells. Immunology. 1999;98(3):386–92.
   PubMed Web of Science ®Google Scholar
• Matera L, Mori M, Galetto A. Effect of prolactin on the antigen presenting function of monocyte-derived dendritic cells. Lupus. 2001;10(10):728–34.
   PubMed Web of Science ®Google Scholar
• Lahat N, Miller A, Shtiller R, Touby E. Differential effects of prolactin upon activation and differentiation of human B lymphocytes. J Neuroimmunol. 1993;47(1):35–40.
   PubMed Web of Science ®Google Scholar
• Saha S, Gonzalez J, Rosenfeld G, Keiser H, Peeva E. Prolactin alters the mechanisms of B cell tolerance induction. Arthritis Rheum. 2009;60(6):1743–52.
   PubMedGoogle Scholar
• L'Hermite M, Vekemans M, Delvoye P, Nokin J, Robyn C. Prolactin studies in normal subjects. Proc R Soc Med. 1973;66(9):864–5.
   PubMedGoogle Scholar
• Vekemans M, Robyn C. Influence of age on serum prolactin levels in women and men. Br Med J. 1975;4(5999):738–9.
   PubMedGoogle Scholar
• Jara LJ, Pacheco-Reyes H, Medina G, Angeles U, Cruz-Cruz P, Saavedra MA. Prolactin levels are associated with lupus activity, lupus anticoagulant, and poor outcome in pregnancy. Ann N Y Acad Sci. 2007;1108(1):218–26.
   PubMedGoogle Scholar
• Buskila D, Lorber M, Neumann L, Flusser D, Shoenfeld Y. No correlation between prolactin levels and clinical activity in patients with systemic lupus erythematosus. J Rheumatol. 1996;23(4):629–32.
   PubMed Web of Science ®Google Scholar
• Leanos-Miranda A, Cardenas-Mondragon G. Serum free prolactin concentrations in patients with systemic lupus erythematosus are associated with lupus activity. Rheumatology. 2006;45:97–101.
   PubMed Web of Science ®Google Scholar
• Biller BM, Luciano A, Crosignani PG, Molitch M, Olive D, Rebar R, et al. Guidelines for the diagnosis and treatment of hyperprolactinemia. J Reprod Med. 1999;44(12 Suppl):1075–84.
   PubMed Web of Science ®Google Scholar
• Mok CC, Lau CS, Lee KW, Wong RW. Hyperprolactinemia in males with systemic lupus erythematosus. J Rheumatol. 1998;25(12):2357–63.
   PubMed Web of Science ®Google Scholar
• Pacilio M, Migliaresi S, Meli R, Ambrosone L, Bigliardo B, Di Carlo R. Elevated bioactive prolactin levels in systemic lupus erythematosus–association with disease activity. J Rheumatol. 2001;28:2216–21.
   PubMed Web of Science ®Google Scholar
• Jacobi AM, Rohde W, Ventz M, Riemekasten G, Burmester GR, Hiepe F. Enhanced serum prolactin (PRL) in patients with systemic lupus erythematosus: PRL levels are related to the disease activity. Lupus. 2001;10(8):554–61.
   PubMed Web of Science ®Google Scholar
• Cardenas-Mondragon G, Ulloa-Aguirre A, Isordia-Salas I, Goffin V, Leanos-Miranda A. Elevated serum bioactive prolactin concentrations in patients with systemic lupus erythematosus are associated with disease activity as disclosed by homologous receptor bioassays. J Rheumatol. 2007;34:1514–21.
   PubMed Web of Science ®Google Scholar
• Ugarte-Gil MF, Gamboa-Cardenas RV, Zevallos F, Medina M, Cucho-Venegas JM, Perich-Campos RA, et al. High prolactin levels are independently associated with damage accrual in systemic lupus erythematosus patients. Lupus. 2014;23(10):969–74.
   PubMed Web of Science ®Google Scholar
• Karimifar M, Tahmasebi A, Bonakdar ZS, Purajam S. Correlation of serum prolactin levels and disease activity in systematic lupus erythematosus. Rheumatol Int. 2013;33(2):511–6.
   PubMed Web of Science ®Google Scholar
• Orbach H, Zandman-Goddard G, Boaz M, Agmon-Levin N, Amital H, Szekanecz Z, et al. Prolactin and autoimmunity: hyperprolactinemia correlates with serositis and anemia. Clinic Rev Allerg Immunol. 2012;42(2):189–98.
   PubMed Web of Science ®Google Scholar
• Yang J, Li Q, Yang X, Li M. Increased serum level of prolactin is related to autoantibody production in systemic lupus erythematosus. Lupus. 2016;25(5):513–9.
   PubMed Web of Science ®Google Scholar
• Walker SE. Bromocriptine treatment of systemic lupus erythematosus. Lupus. 2001;10(10):762–8.
   PubMed Web of Science ®Google Scholar
• McMurray RW, Weidensaul D, Allen SH, Walker SE. Efficacy of bromocriptine in an open label therapeutic trial for systemic lupus erythematosus. J Rheumatol. 1995;22:2084–91.
   PubMed Web of Science ®Google Scholar
• Jara LJ, Cruz-Cruz P, Saavedra MA, Medina G, Garcia-Flores A, Angeles U, et al. Bromocriptine during pregnancy in systemic lupus erythematosus: a pilot clinical trial. Ann N Y Acad Sci. 2007;1110:297–304.
   PubMed Web of Science ®Google Scholar
• Qian Q, Liuqin L, Hao L, Shiwen Y, Zhongping Z, Dongying C, et al. The effects of bromocriptine on preventing postpartum flare in systemic lupus erythematosus patients from South China. J Immunol Res. 2015;2015:1.
   Google Scholar
• McMurray R, Keisler D, Kanuckel K, Izui S, Walker SE. Prolactin influences autoimmune disease activity in the female B/W mouse. J Immunol. 1991;147:3780–7.
   PubMed Web of Science ®Google Scholar
• Peeva E, Michael D, Cleary J, Rice J, Chen X, Diamond B. Prolactin modulates the naive B cell repertoire. J Clin Investig. 2003;111(2):275–83.
   PubMed Web of Science ®Google Scholar
• Grimaldi CM, Hill L, Xu X, Peeva E, Diamond B. Hormonal modulation of B cell development and repertoire selection. Mol Immunol. 2005;42(7):811–20.
   PubMed Web of Science ®Google Scholar
• Hau CS, Kanda N, Tada Y, Shibata S, Sato S, Watanabe S. Prolactin induces the production of Th17 and Th1 cytokines/chemokines in murine Imiquimod-induced psoriasiform skin. J Eur Acad Dermatol Venereol. 2014;28(10):1370–9.
   PubMed Web of Science ®Google Scholar
• Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev. 1998;19(3):225–68.
   PubMed Web of Science ®Google Scholar
• Jara LJ, Lavalle C, Fraga A, Gomez-Sanchez C, Silveira LH, Martinez-Osuna P, et al. Prolactin, immunoregulation, and autoimmune diseases. Semin Arthritis Rheum. 1991;20(5):273–84.
   PubMed Web of Science ®Google Scholar
• Pezet A, Buteau H, Kelly PA, Edery M. The last proline of Box 1 is essential for association with JAK2 and functional activation of the prolactin receptor. Mol Cell Endocrinol. 1997;129(2):199–208.
   PubMed Web of Science ®Google Scholar
• DaSilva L, Rui H, Erwin RA, Howard OM, Kirken RA, Malabarba MG, et al. Prolactin recruits STAT1, STAT3 and STAT5 independent of conserved receptor tyrosines TYR402, TYR479, TYR515 and TYR580. Mol Cell Endocrinol. 1996;117(2):131–40.
   PubMed Web of Science ®Google Scholar
• Kavarthapu R, Tsai Morris CH, Dufau ML. Prolactin induces up-regulation of its cognate receptor in breast cancer cells via transcriptional activation of its generic promoter by cross-talk between ERalpha and STAT5. Oncotarget. 2014;5:9079–91.
   PubMedGoogle Scholar
• Yu-Lee L. Stimulation of interferon regulatory factor-1 by prolactin. Lupus. 2001;10(10):691–9.
   PubMed Web of Science ®Google Scholar
• Stevens AM, Wang YF, Sieger KA, Lu HF, Yu-Lee LY. Biphasic transcriptional regulation of the interferon regulatory factor-1 gene by prolactin: involvement of gamma-interferon-activated sequence and Stat-related proteins. Mol Endocrinol. 1995;9:513–25.
   PubMedGoogle Scholar
• Schwarz LA, Stevens AM, Hrachovy JA, Yu-Lee LY. Interferon regulatory factor-1 is inducible by prolactin, interleukin-2 and concanavalin A in T cells. Mol Cell Endocrinol. 1992;86(1–2):103–10.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Song L, Maurer K, Petri MA, Sullivan KE. Global H4 acetylation analysis by ChIP-chip in systemic lupus erythematosus monocytes. Genes Immun. 2010;11(2):124–33.
   PubMed Web of Science ®Google Scholar
• Shi L, Zhang Z, Song L, Leung YT, Petri MA, Sullivan KE. Monocyte enhancers are highly altered in systemic lupus erythematosus. Epigenomics. 2015;7(6):921–35.
   PubMed Web of Science ®Google Scholar
• Shi L, Perin JC, Leipzig J, Zhang Z, Sullivan KE. Genome-wide analysis of interferon regulatory factor I binding in primary human monocytes. Gene. 2011;487(1):21–8.
   PubMed Web of Science ®Google Scholar
• Leung YT, Shi L, Maurer K, Song L, Zhang Z, Petri M, et al. Interferon regulatory factor 1 and histone H4 acetylation in systemic lupus erythematosus. Epigenetics. 2015;10(3):191–9.
   PubMed Web of Science ®Google Scholar
• Garrett S, Dietzmann-Maurer K, Song L, Sullivan KE. Polarization of primary human monocytes by IFN-gamma induces chromatin changes and recruits RNA Pol II to the TNF-alpha promoter. J Immunol. 2008;180(8):5257–66.
   PubMed Web of Science ®Google Scholar
• Garrett S, Fitzgerald MC, Sullivan KE. LPS and poly I:C induce chromatin modifications at a novel upstream region of the IL-23 p19 promoter. Inflammation. 2008;31(4):235–46.
   PubMed Web of Science ®Google Scholar
• Yu-Lee LY, Hrachovy JA, Stevens AM, Schwarz LA. Interferon-regulatory factor 1 is an immediate-early gene under transcriptional regulation by prolactin in Nb2 T cells. Mol Cell Biol. 1990;10(6):3087–94.
   PubMed Web of Science ®Google Scholar
• Shi L, Zhang Z, Yu AM, Wang W, Wei Z, Akhter E, et al. The SLE transcriptome exhibits evidence of chronic endotoxin exposure and has widespread dysregulation of non-coding and coding RNAs. PLoS One. 2014;9(5):e93846.
   PubMed Web of Science ®Google Scholar
• Karanam B, Wang L, Wang D, Liu X, Marmorstein R, Cotter R, et al. Multiple roles for acetylation in the interaction of p300 HAT with ATF-2. Biochemistry. 2007;46(28):8207–16.
   PubMed Web of Science ®Google Scholar
• Alvarez-Nemegyei J, Cobarrubias-Cobos A, Escalante-Triay F, Sosa-Munoz J, Miranda JM, Jara LJ. Bromocriptine in systemic lupus erythematosus: a double-blind, randomized, placebo-controlled study. Lupus. 1998;7(6):414–9.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Shi L, Song L, Maurer K, Petri MA, Sullivan KE. Overall downregulation of mRNAs and enrichment of H3K4me3 change near genome-wide association study signals in systemic lupus erythematosus: cell-specific effects. Front Immunol. 2018;9:497.
   PubMed Web of Science ®Google Scholar
• Kyogoku C, Smiljanovic B, Grun JR, Biesen R, Schulte-Wrede U, Haupl T, et al. Cell-specific type I IFN signatures in autoimmunity and viral infection: what makes the difference? PLoS One. 2013;8(12):e83776.
   PubMed Web of Science ®Google Scholar
• Sharma S, Jin Z, Rosenzweig E, Rao S, Ko K, Niewold TB. Widely divergent transcriptional patterns between SLE patients of different ancestral backgrounds in sorted immune cell populations. J Autoimmun. 2015;60:51–8.
   PubMed Web of Science ®Google Scholar
• Olferiev M, Jacek E, Kirou KA, Crow MK. Novel molecular signatures in mononuclear cell populations from patients with systemic lupus erythematosus. Clin Immunol. 2016;172:34–43.
   PubMed Web of Science ®Google Scholar
• Liu Q, Zhu Y, Yong WK, Sze NS, Tan NS, Ding JL. Cutting edge: synchronization of IRF1, JunB, and C/EBPbeta activities during TLR3-TLR7 cross-talk orchestrates timely cytokine synergy in the proinflammatory response. J Immunol. 2015;195(3):801–5.
   PubMed Web of Science ®Google Scholar
• Negishi H, Fujita Y, Yanai H, Sakaguchi S, Ouyang X, Shinohara M, et al. Evidence for licensing of IFN-gamma-induced IFN regulatory factor 1 transcription factor by MyD88 in Toll-like receptor-dependent gene induction program. Proc Natl Acad Sci U S A. 2006;103(41):15136–41.
   PubMed Web of Science ®Google Scholar
• Masumi A, Wang IM, Lefebvre B, Yang XJ, Nakatani Y, Ozato K. The histone acetylase PCAF is a phorbol-ester-inducible coactivator of the IRF family that confers enhanced interferon responsiveness. Mol Cell Biol. 1999;19(3):1810–20.
   PubMed Web of Science ®Google Scholar
• Merika M, Williams AJ, Chen G, Collins T, Thanos D. Recruitment of CBP/p300 by the IFN beta enhanceosome is required for synergistic activation of transcription. Mol Cell. 1998;1(2):277–87.
   PubMed Web of Science ®Google Scholar
• Witte S, Bradley A, Enright AJ, Muljo SA. High-density P300 enhancers control cell state transitions. BMC Genomics. 2015;16:903.
   PubMed Web of Science ®Google Scholar
• Raisner R, Kharbanda S, Jin L, Jeng E, Chan E, Merchant M, et al. Enhancer activity requires CBP/P300 bromodomain-dependent histone H3K27 acetylation. Cell Rep. 2018;24(7):1722–9.
   PubMed Web of Science ®Google Scholar
• Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V, Zlobin A, et al. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development. 2009;136(18):3131–41.
   PubMed Web of Science ®Google Scholar