73
Views
3
CrossRef citations to date
0
Altmetric
Hypothesis

The Potentially Therapeutic Role of EPAC in Curbing the Process of Idiopathic Pulmonary Fibrosis via Differential Cellular Pathways

, , &
Pages 611-619 | Published online: 26 Feb 2021

References

  • Nalysnyk L, Cid-Ruzafa J, Rotella P, Esser D. Incidence and prevalence of idiopathic pulmonary fibrosis: review of the literature. Eur Respir Rev. 2012;21(126):355–361. doi:10.1183/09059180.00002512
  • Ahluwalia N, Shea BS, Tager AM. New therapeutic targets in idiopathic pulmonary fibrosis. Aiming to rein in runaway wound-healing responses. Am J Respir Crit Care Med. 2014;190(8):867–878. doi:10.1164/rccm.201403-0509PP
  • Meyer KC. Pulmonary fibrosis, part I: epidemiology, pathogenesis, and diagnosis. Expert Rev Respir Med. 2017;11(5):343–359. doi:10.1080/17476348.2017.1312346
  • Trethewey SP, Walters GI. The role of occupational and environmental exposures in the pathogenesis of idiopathic pulmonary fibrosis: a narrative literature review. Medicina (Kaunas). 2018;54(6).
  • Lederer DJ, Martinez FJ, Longo DL. Idiopathic pulmonary fibrosis. N Engl J Med. 2018;378(19):1811–1823. doi:10.1056/NEJMra1705751
  • Raghu G, Rochwerg B, Zhang Y, et al., European Respiratory, S. Japanese Respiratory, S. Latin American Thoracic, A. An official ATS/ERS/JRS/ALAT clinical practice guideline: treatment of idiopathic pulmonary fibrosis. an update of the 2011 clinical practice guideline. Am J Respir Crit Care Med. 2015;192(2):e3–19. doi:10.1164/rccm.201506-1063ST
  • Somogyi V, Chaudhuri N, Torrisi SE, Kahn N, Muller V, Kreuter M. The therapy of idiopathic pulmonary fibrosis: what is next? Eur Respir Rev. 2019;28(153):153. doi:10.1183/16000617.0021-2019
  • Kawasaki H, Springett GM, Mochizuki N, et al. A family of cAMP-binding proteins that directly activate Rap1. Science. 1998;282(5397):2275–2279. doi:10.1126/science.282.5397.2275
  • Niimura M, Miki T, Shibasaki T, Fujimoto W, Iwanaga T, Seino S. Critical role of the N-terminal cyclic AMP-binding domain of Epac2 in its subcellular localization and function. J Cell Physiol. 2009;219(3):652–658. doi:10.1002/jcp.21709
  • Hoivik EA, Witsoe SL, Bergheim IR, et al. DNA methylation of alternative promoters directs tissue specific expression of Epac2 isoforms. PLoS One. 2013;8(7):e67925. doi:10.1371/journal.pone.0067925
  • Qiao J, Mei FC, Popov VL, Vergara LA, Cheng X. Cell cycle-dependent subcellular localization of exchange factor directly activated by cAMP. J Biol Chem. 2002;277(29):26581–26586. doi:10.1074/jbc.M203571200
  • Ponsioen B, Gloerich M, Ritsma L, Rehmann H, Bos JL, Jalink K. Direct spatial control of Epac1 by cyclic AMP. Mol Cell Biol. 2009;29(10):2521–2531. doi:10.1128/MCB.01630-08
  • Roscioni SS, Elzinga CR, Schmidt M. Epac: effectors and biological functions. Naunyn Schmiedebergs Arch Pharmacol. 2008;377(4–6):345–357. doi:10.1007/s00210-007-0246-7
  • Yokoyama U, Patel HH, Lai NC, Aroonsakool N, Roth DM, Insel PA. The cyclic AMP effector Epac integrates pro- and anti-fibrotic signals. PNAS. 2008;105(17):6386–6391. doi:10.1073/pnas.0801490105
  • Rangarajan S, Enserink JM, Kuiperij HB, et al. Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the beta 2-adrenergic receptor. J Cell Biol. 2003;160(4):487–493. doi:10.1083/jcb.200209105
  • Aslam M, Tanislav C, Troidl C, Schulz R, Hamm C, Gunduz D. cAMP controls the restoration of endothelial barrier function after thrombin-induced hyperpermeability via Rac1 activation. Physiol Rep. 2014;2(10):10. doi:10.14814/phy2.12175
  • Bartram U, Speer CP. The role of transforming growth factor β in lung development and disease. Chest. 2004;125(2):754–765. doi:10.1378/chest.125.2.754
  • Leask A, Abraham DJ. TGF-beta signaling and the fibrotic response. FASEB J. 2004;18(7):816–827. doi:10.1096/fj.03-1273rev
  • Huang SK, Wettlaufer SH, Chung J, Peters-Golden M. Prostaglandin E2 inhibits specific lung fibroblast functions via selective actions of PKA and Epac-1. Am J Respir Cell Mol Biol. 2008;39(4):482–489. doi:10.1165/rcmb.2008-0080OC
  • Dekkers BG, Racke K, Schmidt M. Distinct PKA and Epac compartmentalization in airway function and plasticity. Pharmacol Ther. 2013;137(2):248–265.
  • White ES, Atrasz RG, Dickie EG, et al. Prostaglandin E2 inhibits fibroblast migration by E-prostanoid 2 receptor–mediated increase in PTEN activity. Am J Respir Cell Mol Biol. 2005;32(2):135–141. doi:10.1165/rcmb.2004-0126OC
  • Haag S, Warnken M, Juergens UR, Racke K. Role of Epac1 in mediating anti-proliferative effects of prostanoid EP(2) receptors and cAMP in human lung fibroblasts. Naunyn Schmiedebergs Arch Pharmacol. 2008;378(6):617–630. doi:10.1007/s00210-008-0334-3
  • Oga T, Matsuoka T, Yao C, et al. Prostaglandin F(2alpha) receptor signaling facilitates bleomycin-induced pulmonary fibrosis independently of transforming growth factor-beta. Nat Med. 2009;15(12):1426–1430. doi:10.1038/nm.2066
  • Amrani Y, Panettieri RA, Ramos-Ramirez P, Schaafsma D, Kaczmarek K, Tliba O. Important lessons learned from studies on the pharmacology of glucocorticoids in human airway smooth muscle cells: too much of a good thing may be a problem. Pharmacol Ther. 2020;213:107589. doi:10.1016/j.pharmthera.2020.107589
  • Chen YF, Huang G, Wang YM, et al. Exchange protein directly activated by cAMP (Epac) protects against airway inflammation and airway remodeling in asthmatic mice. Respir Res. 2019;20(1):285. doi:10.1186/s12931-019-1260-2
  • Sukhanova IF, Kozhevnikova LM, Popov EG, Podmareva ON, Avdonin PV. Activators of Epac proteins induce relaxation of isolated rat aorta. Dokl Biol Sci. 2006;411(1):441–444. doi:10.1134/S0012496606060044
  • Zieba BJ, Artamonov MV, Jin L, et al. The cAMP-responsive Rap1 guanine nucleotide exchange factor, Epac, induces smooth muscle relaxation by down-regulation of RhoA activity. J Biol Chem. 2011;286(19):16681–16692. doi:10.1074/jbc.M110.205062
  • Roscioni SS, Maarsingh H, Elzinga CR, et al. Epac as a novel effector of airway smooth muscle relaxation. J Cell Mol Med. 2011;15(7):1551–1563. doi:10.1111/j.1582-4934.2010.01150.x
  • Hashimoto N, Phan SH, Imaizumi K, et al. Endothelial-mesenchymal transition in bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol. 2010;43(2):161–172. doi:10.1165/rcmb.2009-0031OC
  • Sayner SL. Emerging themes of cAMP regulation of the pulmonary endothelial barrier. Am J Physiol Lung Cell Mol Physiol. 2011;300(5):L667–78. doi:10.1152/ajplung.00433.2010
  • Sands WA, Woolson HD, Milne GR, Rutherford C, Palmer TM. Exchange protein activated by cyclic AMP (Epac)-mediated induction of suppressor of cytokine signaling 3 (SOCS-3) in vascular endothelial cells. Mol Cell Biol. 2006;26(17):6333–6346. doi:10.1128/MCB.00207-06
  • Gunduz D, Troidl C, Tanislav C, Rohrbach S, Hamm C, Aslam M. Role of PI3K/Akt and MEK/ERK signalling in cAMP/Epac-mediated endothelial barrier stabilisation. Front Physiol. 2019;10:1387. doi:10.3389/fphys.2019.01387
  • Yuan Y, Engler AJ, Raredon MS, et al. Epac agonist improves barrier function in iPSC-derived endothelial colony forming cells for whole organ tissue engineering. Biomaterials. 2019;200:25–34. doi:10.1016/j.biomaterials.2019.02.005
  • Selman M, Rojas M, Mora AL, Pardo A. Aging and interstitial lung diseases: unraveling an old forgotten player in the pathogenesis of lung fibrosis. Semin Respir Crit Care Med. 2010;31(5):607–617. doi:10.1055/s-0030-1265901
  • Selman M, Pardo A. Revealing the pathogenic and aging-related mechanisms of the enigmatic idiopathic pulmonary fibrosis. an integral model. Am J Respir Crit Care Med. 2014;189(10):1161–1172. doi:10.1164/rccm.201312-2221PP
  • Conrotto P, Yakymovych I, Yakymovych M, Souchelnytskyi S. Interactome of transforming growth factor-beta type I receptor (TbetaRI): inhibition of TGFbeta signaling by Epac1. J Proteome Res. 2007;6(1):287–297. doi:10.1021/pr060427q
  • Young BM, Shankar K, Tho CK, Pellegrino AR, Heise RL. Laminin-driven Epac/Rap1 regulation of epithelial barriers on decellularized matrix. Acta Biomater. 2019;100:223–234. doi:10.1016/j.actbio.2019.10.009
  • Wang XF, Song SD, Li YJ, et al. Protective effect of quercetin in LPS-induced murine acute lung injury mediated by cAMP-Epac pathway. Inflammation. 2018;41(3):1093–1103. doi:10.1007/s10753-018-0761-3
  • Jansen SR, Poppinga WJ, de Jager W, et al. Epac1 links prostaglandin E2 to beta-catenin-dependent transcription during epithelial-to-mesenchymal transition. Oncotarget. 2016;7(29):46354–46370. doi:10.18632/oncotarget.10128
  • Lim JA, Juhnn YS. Isoproterenol increases histone deacetylase 6 expression and cell migration by inhibiting ERK signaling via PKA and Epac pathways in human lung cancer cells. Exp Mol Med. 2016;48(1):e204. doi:10.1038/emm.2015.98
  • El Agha E, Kramann R, Schneider RK, et al. Mesenchymal stem cells in fibrotic disease. Cell Stem Cell. 2017;21(2):166–177. doi:10.1016/j.stem.2017.07.011
  • Yu JL, Deng R, Chung SK, Chan GC. Epac activation regulates human mesenchymal stem cells migration and adhesion. Stem Cells. 2016;34(4):948–959. doi:10.1002/stem.2264
  • Willis GR, Fernandez-Gonzalez A, Anastas J, et al. Mesenchymal stromal cell exosomes ameliorate experimental bronchopulmonary dysplasia and restore lung function through macrophage immunomodulation. Am J Respir Crit Care Med. 2018;197(1):104–116. doi:10.1164/rccm.201705-0925OC
  • Tan JL, Lau SN, Leaw B, et al. Amnion epithelial cell-derived exosomes restrict lung injury and enhance endogenous lung repair. Stem Cells Transl Med. 2018;7(2):180–196. doi:10.1002/sctm.17-0185
  • Fujita Y, Kadota T, Araya J, Ochiya T, Kuwano K. Clinical application of mesenchymal stem cell-derived extracellular vesicle-based therapeutics for inflammatory lung diseases. J Clin Med. 2018;7(10):10. doi:10.3390/jcm7100355
  • Shentu TP, Huang TS, Cernelc-Kohan M, et al. Thy-1 dependent uptake of mesenchymal stem cell-derived extracellular vesicles blocks myofibroblastic differentiation. Sci Rep. 2017;7(1):18052. doi:10.1038/s41598-017-18288-9
  • Hartopo AB, Emoto N, Vignon-Zellweger N, et al. Endothelin-converting enzyme-1 gene ablation attenuates pulmonary fibrosis via CGRP-cAMP/EPAC1 pathway. Am J Respir Cell Mol Biol. 2013;48(4):465–476. doi:10.1165/rcmb.2012-0354OC
  • Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11(11):723–737. doi:10.1038/nri3073
  • Aronoff DM, Canetti C, Serezani CH, Luo M, Peters-Golden M. Cutting edge: macrophage inhibition by cyclic AMP (cAMP): differential roles of protein kinase A and exchange protein directly activated by cAMP-1. J Immunol. 2005;174(2):595–599. doi:10.4049/jimmunol.174.2.595
  • Lorenowicz MJ, van Gils J, de Boer M, Hordijk PL, Fernandez-Borja M. Epac1-Rap1 signaling regulates monocyte adhesion and chemotaxis. J Leukoc Biol. 2006;80(6):1542–1552. doi:10.1189/jlb.0506357
  • Cao Q, Wang Y, Zheng D, et al. IL-10/TGF-beta-modified macrophages induce regulatory T cells and protect against adriamycin nephrosis. J Am Soc Nephrol. 2010;21(6):933–942. doi:10.1681/ASN.2009060592
  • Lo R, Lecocq S, Uwambayinema M, et al. Platelet-derived growth factor-producing CD4+ Foxp3+ regulatory T lymphocytes promote lung fibrosis. Am J Respir Crit Care Med. 2011;184(11):1270–1281. doi:10.1164/rccm.201103-0516OC
  • Sebzda E, Bracke M, Tugal T, Hogg N, Cantrell DA. Rap1A positively regulates T cells via integrin activation rather than inhibiting lymphocyte signaling. Nat Immunol. 2002;3(3):251–258. doi:10.1038/ni765
  • de-Rooij J, Zwartkruis F, Verheijen M, et al. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP (see comments). Nature. 1998;396(6710):474–477. doi:10.1038/24884
  • Almahariq M, Mei FC, Wang H, et al. Exchange protein directly activated by cAMP modulates regulatory T-cell-mediated immunosuppression. Biochem J. 2015;465(2):295–303. doi:10.1042/BJ20140952
  • Olman MA. Beyond TGF-beta: a prostaglandin promotes fibrosis. Nat Med. 2009;15(12):1360–1361. doi:10.1038/nm1209-1360
  • Insel PA, Murray F, Yokoyama U, et al. cAMP and Epac in the regulation of tissue fibrosis. Br J Pharmacol. 2012;166(2):447–456. doi:10.1111/j.1476-5381.2012.01847.x