315
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Single-Cell Profiling Uncovers the Roles of Endometrial Fibrosis and Microenvironmental Changes in Adenomyosis

, , , , , , , & show all
Pages 1949-1965 | Received 12 Jan 2023, Accepted 29 Mar 2023, Published online: 05 May 2023

References

  • Benagiano G, Habiba M, Brosens I. The pathophysiology of uterine adenomyosis: an update. Fertil Steril. 2012;98(3):572–579. doi:10.1016/j.fertnstert.2012.06.044
  • Kitawaki J. Adenomyosis: the pathophysiology of an oestrogen-dependent disease. Best Pract Res. 2006;20(4):493–502. doi:10.1016/j.bpobgyn.2006.01.010
  • Benagiano G, Brosens I, Habiba M. Structural and molecular features of the endomyometrium in endometriosis and adenomyosis. Hum Reprod Update. 2014;20(3):386–402. doi:10.1093/humupd/dmt052
  • Wood C. Adenomyosis: difficult to diagnose, and difficult to treat. Diagn Ther Endosc. 2001;7(2):89–95. doi:10.1155/DTE.7.89
  • Kobayashi H, Kishi Y, Matsubara S. Mechanisms underlying adenomyosis-related fibrogenesis. Gynecol Obstet Invest. 2020;85(1):1–12. doi:10.1159/000502822
  • Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest. 2007;117(3):524–529. doi:10.1172/JCI31487
  • Daimon E, Shibukawa Y, Wada Y. Calponin 3 regulates stress fiber formation in dermal fibroblasts during wound healing. Arch Dermatol Res. 2013;305(7):571–584. doi:10.1007/s00403-013-1343-8
  • Bodur S, Dundar O, Pektas MK, Babayigit MA, Ozden O, Kucukodaci Z. The clinical significance of classical and new emerging determinants of adenomyosis. Int J Clin Exp Med. 2015;8(5):7958–7964.
  • Capobianco A, Monno A, Cottone L, et al. Proangiogenic Tie2(+) macrophages infiltrate human and murine endometriotic lesions and dictate their growth in a mouse model of the disease. Am J Pathol. 2011;179(5):2651–2659. doi:10.1016/j.ajpath.2011.07.029
  • Duan J, Liu X, Wang H, Guo SW. The M2a macrophage subset may be critically involved in the fibrogenesis of endometriosis in mice. Reprod Biomed Online. 2018;37(3):254–268. doi:10.1016/j.rbmo.2018.05.017
  • Lappalainen H, Laine P, Pentikainen MO, Sajantila A, Kovanen PT. Mast cells in neovascularized human coronary plaques store and secrete basic fibroblast growth factor, a potent angiogenic mediator. Arterioscler Thromb Vasc Biol. 2004;24(10):1880–1885. doi:10.1161/01.ATV.0000140820.51174.8d
  • Komi DEA, Khomtchouk K, Santa Maria PL. A review of the contribution of mast cells in wound healing: involved molecular and cellular mechanisms. Clin Rev Allergy Immunol. 2020;58(3):298–312. doi:10.1007/s12016-019-08729-w
  • Artegiani B, Lyubimova A, Muraro M, van Es JH, van Oudenaarden A, Clevers H. A single-cell RNA sequencing study reveals cellular and molecular dynamics of the hippocampal neurogenic niche. Cell Rep. 2017;21(11):3271–3284. doi:10.1016/j.celrep.2017.11.050
  • MacParland SA, Liu JC, Ma XZ, et al. Single cell RNA sequencing of human liver reveals distinct intrahepatic macrophage populations. Nat Commun. 2018;9(1):4383. doi:10.1038/s41467-018-06318-7
  • Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. doi:10.1093/bioinformatics/bts635
  • Butler A, Hoffman P, Smibert P, Papalexi E, Satija R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat Biotechnol. 2018;36(5):411–420. doi:10.1038/nbt.4096
  • Vento-Tormo R, Efremova M, Botting RA, et al. Single-cell reconstruction of the early maternal-fetal interface in humans. Nature. 2018;563(7731):347–353. doi:10.1038/s41586-018-0698-6
  • Dou S, Wang Q, Qi X, et al. Molecular identity of human limbal heterogeneity involved in corneal homeostasis and privilege. Ocul Surf. 2021;21:206–220. doi:10.1016/j.jtos.2021.04.010
  • Liu Z, Sun Z, Liu H, et al. Single-cell transcriptomic analysis of eutopic endometrium and ectopic lesions of adenomyosis. Cell Biosci. 2021;11(1):51. doi:10.1186/s13578-021-00562-z
  • Liu G, Cooley MA, Jarnicki AG, et al. Fibulin-1c regulates transforming growth factor-beta activation in pulmonary tissue fibrosis. JCI Insight. 2019;5. doi:10.1172/jci.insight.124529
  • Neame PJ, Kay CJ, McQuillan DJ, Beales MP, Hassell JR. Independent modulation of collagen fibrillogenesis by decorin and lumican. Cell Mol Life Sci. 2000;57(5):859–863. doi:10.1007/s000180050048
  • Tanjore H, Lawson WE, Blackwell TS. Endoplasmic reticulum stress as a pro-fibrotic stimulus. Biochim Biophys Acta. 2013;1832(7):940–947. doi:10.1016/j.bbadis.2012.11.011
  • Mechsner S, Grum B, Gericke C, Loddenkemper C, Dudenhausen JW, Ebert AD. Possible roles of oxytocin receptor and vasopressin-1 alpha receptor in the pathomechanism of dysperistalsis and dysmenorrhea in patients with adenomyosis uteri. Fertil Steril. 2010;94(7):2541–2546. doi:10.1016/j.fertnstert.2010.03.015
  • Itoga T, Matsumoto T, Takeuchi H, et al. Fibrosis and smooth muscle metaplasia in rectovaginal endometriosis. Pathol Int. 2003;53(6):371–375. doi:10.1046/j.1440-1827.2003.01483.x
  • Koike N, Tsunemi T, Uekuri C, et al. Pathogenesis and malignant transformation of adenomyosis (review). Oncol Rep. 2013;29(3):861–867. doi:10.3892/or.2012.2184
  • Ohkouchi S, Ono M, Kobayashi M, et al. Myriad functions of stanniocalcin-1 (STC1) cover multiple therapeutic targets in the complicated pathogenesis of idiopathic pulmonary fibrosis (IPF). Circulat Respir Pulmon Med. 2015;9(Suppl 1):91–96. doi:10.4137/CCRPM.S23285
  • Law AY, Wong CK. Stanniocalcin-1 and −2 promote angiogenic sprouting in HUVECs via VEGF/VEGFR2 and angiopoietin signaling pathways. Mol Cell Endocrinol. 2013;374(1–2):73–81. doi:10.1016/j.mce.2013.04.024
  • Yang EM, Park JS, Joo SY, Bae EH, Ma SK, Kim SW. Stanniocalcin1 suppresses TGFbetainduced mitochondrial dysfunction and cellular fibrosis in human renal proximal tubular cells. Int J Mol Med. 2022;50(2). doi:10.3892/ijmm.2022.5163
  • Ohkouchi S, Kanehira M, Saigusa D, et al. Metabolic and epigenetic regulation of SMAD7 by stanniocalcin-1 (STC1) ameliorates lung fibrosis. Am J Respir Cell Mol Biol. 2022;67:320–333. doi:10.1165/rcmb.2021-0445OC
  • Chan KK, Hon TC, Au KY, et al. Stanniocalcin 1 is a serum biomarker and potential therapeutic target for HBV-associated liver fibrosis. J Pathol. 2022;257(2):227–238. doi:10.1002/path.5880
  • Ke J, Ye J, Li M, Zhu Z. The role of matrix metalloproteinases in endometriosis: a potential target. Biomolecules. 2021;11(11):1739. doi:10.3390/biom11111739
  • Liu G, Cooley MA, Jarnicki AG, et al. Fibulin-1 regulates the pathogenesis of tissue remodeling in respiratory diseases. JCI Insight. 2016;1(9). doi:10.1172/jci.insight.86380.
  • Argraves WS, Tran H, Burgess WH, Dickerson K. Fibulin is an extracellular matrix and plasma glycoprotein with repeated domain structure. J Cell Biol. 1990;111(6 Pt 2):3155–3164. doi:10.1083/jcb.111.6.3155
  • Karamanou K, Perrot G, Maquart FX, Brezillon S. Lumican as a multivalent effector in wound healing. Adv Drug Deliv Rev. 2018;129:344–351. doi:10.1016/j.addr.2018.02.011
  • Pilling D, Vakil V, Cox N, Gomer RH. TNF-alpha-stimulated fibroblasts secrete lumican to promote fibrocyte differentiation. Proc Natl Acad Sci USA. 2015;112(38):11929–11934. doi:10.1073/pnas.1507387112
  • Huveneers S, Danen EH. Adhesion signaling - crosstalk between integrins, Src and Rho. J Cell Sci. 2009;122(Pt 8):1059–1069. doi:10.1242/jcs.039446
  • Margadant C, Sonnenberg A. Integrin-TGF-beta crosstalk in fibrosis, cancer and wound healing. EMBO Rep. 2010;11(2):97–105. doi:10.1038/embor.2009.276
  • Guo SW. Cancer driver mutations in endometriosis: variations on the major theme of fibrogenesis. Reprod Med Biol. 2018;17(4):369–397. doi:10.1002/rmb2.12221
  • Urushiyama H, Terasaki Y, Nagasaka S, et al. Role of alpha1 and alpha2 chains of type IV collagen in early fibrotic lesions of idiopathic interstitial pneumonias and migration of lung fibroblasts. Lab Investig. 2015;95(8):872–885. doi:10.1038/labinvest.2015.66
  • Han ZJ, Li YB, Yang LX, Cheng HJ, Liu X, Chen H. Roles of the CXCL8-CXCR1/2 Axis in the Tumor Microenvironment and Immunotherapy. Molecules. 2021;27(1):137. doi:10.3390/molecules27010137
  • Kendall RT, Feghali-Bostwick CA. Fibroblasts in fibrosis: novel roles and mediators. Front Pharmacol. 2014;5:123. doi:10.3389/fphar.2014.00123
  • Moore MW, Herzog EL. Regulatory T cells in idiopathic pulmonary fibrosis: too much of a good thing? Am J Pathol. 2016;186(8):1978–1981. doi:10.1016/j.ajpath.2016.06.002
  • Zhang L, Wang Y, Wu G, Xiong W, Gu W, Wang CY. Macrophages: friend or foe in idiopathic pulmonary fibrosis? Respir Res. 2018;19(1):170. doi:10.1186/s12931-018-0864-2
  • Barron L, Wynn TA. Fibrosis is regulated by Th2 and Th17 responses and by dynamic interactions between fibroblasts and macrophages. Am J Physiol. 2011;300(5):G723–728. doi:10.1152/ajpgi.00414.2010
  • Bacci M, Capobianco A, Monno A, et al. Macrophages are alternatively activated in patients with endometriosis and required for growth and vascularization of lesions in a mouse model of disease. Am J Pathol. 2009;175(2):547–556. doi:10.2353/ajpath.2009.081011
  • Vallve-Juanico J, Santamaria X, Vo KC, Houshdaran S, Giudice LC. Macrophages display proinflammatory phenotypes in the eutopic endometrium of women with endometriosis with relevance to an infectious etiology of the disease. Fertil Steril. 2019;112(6):1118–1128. doi:10.1016/j.fertnstert.2019.08.060
  • Wu A, Zhang L, Chen J, et al. Limb-bud and Heart (LBH) mediates proliferation, fibroblast-to-myofibroblast transition and EMT-like processes in cardiac fibroblasts. Mol Cell Biochem. 2021;476(7):2685–2701. doi:10.1007/s11010-021-04111-7
  • Maleszewska M, Gjaltema RA, Krenning G, Harmsen MC. Enhancer of zeste homolog-2 (EZH2) methyltransferase regulates transgelin/smooth muscle-22 alpha expression in endothelial cells in response to interleukin-1beta and transforming growth factor-beta2. Cell Signal. 2015;27(8):1589–1596. doi:10.1016/j.cellsig.2015.04.008
  • Shibata T, Shibata S, Ishigaki Y, et al. Tropomyosin 2 heterozygous knockout in mice using CRISPR-Cas9 system displays the inhibition of injury-induced epithelial-mesenchymal transition, and lens opacity. Mech Ageing Dev. 2018;171:24–30. doi:10.1016/j.mad.2018.03.001