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Published in: European Journal of Medical Research 1/2023

Open Access 01-12-2023 | Endometriosis | Research

Abnormal expression of fission and fusion genes and the morphology of mitochondria in eutopic and ectopic endometrium

Authors: Chaoshuang Ye, Pei Chen, Bingning Xu, Yang Jin, Yongchao Pan, Tianyu Wu, Yongjiang Du, Jingxia Mao, Ruijin Wu

Published in: European Journal of Medical Research | Issue 1/2023

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Abstract

Mitochondria play a pivotal role in physiological and metabolic function of the cell. Mitochondrial dynamics orchestrate mitochondrial function and morphology, involving fission and fusion as well as ultrastructural remodeling. Mounting evidence unravels the close link between mitochondria and endometriosis. However, how mitochondrial architecture changes through fission and fusion in eutopic and ectopic tissues of women with ovarian endometriosis remains unknown. We detected the expression of fission and fusion genes and the morphology of mitochondria in eutopic and ectopic endometrium in ovarian endometriosis. The results showed that the expression of DRP1 and LCLAT1 was upregulated in eutopic endometrial stromal cells (ESCs), and the expression of DRP1, OPA1, MFN1, MFN2, and LCLAT1 was significantly downregulated in ectopic ESCs, and reduced number of mitochondria, wider cristae width and narrower cristae junction width was observed, but there was no difference in cell survival rate. The altered mitochondrial dynamics and morphology might, respectively, provide an advantage for migration and adhesion in eutopic ESCs and be the adaptive response in ectopic endometrial cells to survive under hypoxic and oxidative stress environment.
Literature
2.
go back to reference Chapron C, Marcellin L, Borghese B, Santulli P. Rethinking mechanisms, diagnosis and management of endometriosis. Nat Rev Endocrinol. 2019;15(11):666–82.PubMedCrossRef Chapron C, Marcellin L, Borghese B, Santulli P. Rethinking mechanisms, diagnosis and management of endometriosis. Nat Rev Endocrinol. 2019;15(11):666–82.PubMedCrossRef
3.
go back to reference Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 1927;3(2):93–110. Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 1927;3(2):93–110.
4.
go back to reference Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril. 2012;98(3):511–9.PubMedCrossRef Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril. 2012;98(3):511–9.PubMedCrossRef
5.
go back to reference Chen C, Zhou Y, Hu C, Wang Y, Yan Z, Li Z, et al. Mitochondria and oxidative stress in ovarian endometriosis. Free Radic Biol Med. 2019;136:22–34.PubMedCrossRef Chen C, Zhou Y, Hu C, Wang Y, Yan Z, Li Z, et al. Mitochondria and oxidative stress in ovarian endometriosis. Free Radic Biol Med. 2019;136:22–34.PubMedCrossRef
6.
go back to reference Wang H, Zhao X, Ni C, Dai Y, Guo Y. Zearalenone regulates endometrial stromal cell apoptosis and migration via the promotion of mitochondrial fission by activation of the JNK/DRP1 pathway. Mol Med Rep. 2018;17(6):7797–806.PubMed Wang H, Zhao X, Ni C, Dai Y, Guo Y. Zearalenone regulates endometrial stromal cell apoptosis and migration via the promotion of mitochondrial fission by activation of the JNK/DRP1 pathway. Mol Med Rep. 2018;17(6):7797–806.PubMed
7.
go back to reference Cho S, Lee YM, Choi YS, Yang HI, Jeon YE, Lee KE, et al. Mitochondria DNA polymorphisms are associated with susceptibility to endometriosis. DNA Cell Biol. 2012;31(3):317–22.PubMedCrossRef Cho S, Lee YM, Choi YS, Yang HI, Jeon YE, Lee KE, et al. Mitochondria DNA polymorphisms are associated with susceptibility to endometriosis. DNA Cell Biol. 2012;31(3):317–22.PubMedCrossRef
8.
go back to reference Nasrallah CM, Horvath TL. Mitochondrial dynamics in the central regulation of metabolism. Nat Rev Endocrinol. 2014;10(11):650–8.PubMedCrossRef Nasrallah CM, Horvath TL. Mitochondrial dynamics in the central regulation of metabolism. Nat Rev Endocrinol. 2014;10(11):650–8.PubMedCrossRef
9.
10.
go back to reference Srinivasan S, Guha M, Kashina A, Avadhani NG. Mitochondrial dysfunction and mitochondrial dynamics—the cancer connection. Biochim Biophys Acta Bioenerg. 2017;1858(8):602–14.PubMedCrossRef Srinivasan S, Guha M, Kashina A, Avadhani NG. Mitochondrial dysfunction and mitochondrial dynamics—the cancer connection. Biochim Biophys Acta Bioenerg. 2017;1858(8):602–14.PubMedCrossRef
11.
go back to reference Bertholet AM, Delerue T, Millet AM, Moulis MF, David C, Daloyau M, et al. Mitochondrial fusion/fission dynamics in neurodegeneration and neuronal plasticity. Neurobiol Dis. 2016;90:3–19.PubMedCrossRef Bertholet AM, Delerue T, Millet AM, Moulis MF, David C, Daloyau M, et al. Mitochondrial fusion/fission dynamics in neurodegeneration and neuronal plasticity. Neurobiol Dis. 2016;90:3–19.PubMedCrossRef
12.
go back to reference Li J, Romestaing C, Han X, Li Y, Hao X, Wu Y, et al. Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity. Cell Metab. 2010;12(2):154–65.PubMedPubMedCentralCrossRef Li J, Romestaing C, Han X, Li Y, Hao X, Wu Y, et al. Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity. Cell Metab. 2010;12(2):154–65.PubMedPubMedCentralCrossRef
13.
go back to reference Song C, Zhang J, Qi S, Liu Z, Zhang X, Zheng Y, et al. Cardiolipin remodeling by ALCAT1 links mitochondrial dysfunction to Parkinson’s diseases. Aging Cell. 2019;18(3): e12941.PubMedPubMedCentralCrossRef Song C, Zhang J, Qi S, Liu Z, Zhang X, Zheng Y, et al. Cardiolipin remodeling by ALCAT1 links mitochondrial dysfunction to Parkinson’s diseases. Aging Cell. 2019;18(3): e12941.PubMedPubMedCentralCrossRef
14.
go back to reference Jia D, Zhang J, Nie J, Andersen JP, Rendon S, Zheng Y, et al. Cardiolipin remodeling by ALCAT1 links hypoxia to coronary artery disease by promoting mitochondrial dysfunction. Mol Ther. 2021;29(12):3498–511.PubMedPubMedCentralCrossRef Jia D, Zhang J, Nie J, Andersen JP, Rendon S, Zheng Y, et al. Cardiolipin remodeling by ALCAT1 links hypoxia to coronary artery disease by promoting mitochondrial dysfunction. Mol Ther. 2021;29(12):3498–511.PubMedPubMedCentralCrossRef
15.
go back to reference Wang L, Liu X, Nie J, Zhang J, Kimball SR, Zhang H, et al. ALCAT1 controls mitochondrial etiology of fatty liver diseases, linking defective mitophagy to steatosis. Hepatology. 2015;61(2):486–96.PubMedCrossRef Wang L, Liu X, Nie J, Zhang J, Kimball SR, Zhang H, et al. ALCAT1 controls mitochondrial etiology of fatty liver diseases, linking defective mitophagy to steatosis. Hepatology. 2015;61(2):486–96.PubMedCrossRef
16.
go back to reference Liu X, Ye B, Miller S, Yuan H, Zhang H, Tian L, et al. Ablation of ALCAT1 mitigates hypertrophic cardiomyopathy through effects on oxidative stress and mitophagy. Mol Cell Biol. 2012;32(21):4493–504.PubMedPubMedCentralCrossRef Liu X, Ye B, Miller S, Yuan H, Zhang H, Tian L, et al. Ablation of ALCAT1 mitigates hypertrophic cardiomyopathy through effects on oxidative stress and mitophagy. Mol Cell Biol. 2012;32(21):4493–504.PubMedPubMedCentralCrossRef
17.
go back to reference Cogliati S, Enriquez JA, Scorrano L. Mitochondrial cristae: where beauty meets functionality. Trends Biochem Sci. 2016;41(3):261–73.PubMedCrossRef Cogliati S, Enriquez JA, Scorrano L. Mitochondrial cristae: where beauty meets functionality. Trends Biochem Sci. 2016;41(3):261–73.PubMedCrossRef
18.
go back to reference Hollinshead KER, Parker SJ, Eapen VV, Encarnacion-Rosado J, Sohn A, Oncu T, et al. Respiratory supercomplexes promote mitochondrial efficiency and growth in severely hypoxic pancreatic cancer. Cell Rep. 2020;33(1): 108231.PubMedPubMedCentralCrossRef Hollinshead KER, Parker SJ, Eapen VV, Encarnacion-Rosado J, Sohn A, Oncu T, et al. Respiratory supercomplexes promote mitochondrial efficiency and growth in severely hypoxic pancreatic cancer. Cell Rep. 2020;33(1): 108231.PubMedPubMedCentralCrossRef
19.
go back to reference Boi L, Pisanu A, Palmas MF, Fusco G, Carboni E, Casu MA, et al. Modeling Parkinson's disease neuropathology and symptoms by intranigral inoculation of preformed human alpha-synuclein oligomers. Int J Mol Sci. 2020;21(22):8535. Boi L, Pisanu A, Palmas MF, Fusco G, Carboni E, Casu MA, et al. Modeling Parkinson's disease neuropathology and symptoms by intranigral inoculation of preformed human alpha-synuclein oligomers. Int J Mol Sci. 2020;21(22):8535.
20.
go back to reference Kook SY, Jeong H, Kang MJ, Park R, Shin HJ, Han SH, et al. Crucial role of calbindin-D28k in the pathogenesis of Alzheimer’s disease mouse model. Cell Death Differ. 2014;21(10):1575–87.PubMedPubMedCentralCrossRef Kook SY, Jeong H, Kang MJ, Park R, Shin HJ, Han SH, et al. Crucial role of calbindin-D28k in the pathogenesis of Alzheimer’s disease mouse model. Cell Death Differ. 2014;21(10):1575–87.PubMedPubMedCentralCrossRef
21.
go back to reference Signorile A, De Rasmo D, Cormio A, Musicco C, Rossi R, Fortarezza F, et al. Human ovarian cancer tissue exhibits increase of mitochondrial biogenesis and cristae remodeling. Cancers (Basel). 2019;11(9):1350. Signorile A, De Rasmo D, Cormio A, Musicco C, Rossi R, Fortarezza F, et al. Human ovarian cancer tissue exhibits increase of mitochondrial biogenesis and cristae remodeling. Cancers (Basel). 2019;11(9):1350.
22.
go back to reference Valente AJ, Maddalena LA, Robb EL, Moradi F, Stuart JA. A simple ImageJ macro tool for analyzing mitochondrial network morphology in mammalian cell culture. Acta Histochem. 2017;119(3):315–26.PubMedCrossRef Valente AJ, Maddalena LA, Robb EL, Moradi F, Stuart JA. A simple ImageJ macro tool for analyzing mitochondrial network morphology in mammalian cell culture. Acta Histochem. 2017;119(3):315–26.PubMedCrossRef
23.
go back to reference Wai T, Langer T. Mitochondrial dynamics and metabolic regulation. Trends Endocrinol Metab. 2016;27(2):105–17.PubMedCrossRef Wai T, Langer T. Mitochondrial dynamics and metabolic regulation. Trends Endocrinol Metab. 2016;27(2):105–17.PubMedCrossRef
24.
go back to reference Kannan K, Holcombe RF, Jain SK, Alvarez-Hernandez X, Chervenak R, Wolf RE, et al. Evidence for the induction of apoptosis by endosulfan in a human T-cell leukemic line. Mol Cell Biochem. 2000;205(1–2):53–66.PubMedCrossRef Kannan K, Holcombe RF, Jain SK, Alvarez-Hernandez X, Chervenak R, Wolf RE, et al. Evidence for the induction of apoptosis by endosulfan in a human T-cell leukemic line. Mol Cell Biochem. 2000;205(1–2):53–66.PubMedCrossRef
25.
go back to reference Hu J, Meng Y, Zhang Z, Yan Q, Jiang X, Lv Z, et al. MARCH5 RNA promotes autophagy, migration, and invasion of ovarian cancer cells. Autophagy. 2017;13(2):333–44.PubMedCrossRef Hu J, Meng Y, Zhang Z, Yan Q, Jiang X, Lv Z, et al. MARCH5 RNA promotes autophagy, migration, and invasion of ovarian cancer cells. Autophagy. 2017;13(2):333–44.PubMedCrossRef
26.
go back to reference Jiang Z, Shi C, Han H, Wang Y, Liang R, Chen X, et al. Mitochondria-related changes and metabolic dysfunction in low prognosis patients under the POSEIDON classification. Hum Reprod. 2021;36(11):2904–15.PubMedCrossRef Jiang Z, Shi C, Han H, Wang Y, Liang R, Chen X, et al. Mitochondria-related changes and metabolic dysfunction in low prognosis patients under the POSEIDON classification. Hum Reprod. 2021;36(11):2904–15.PubMedCrossRef
27.
go back to reference Abbade J, Klemetti MM, Farrell A, Ermini L, Gillmore T, Sallais J, et al. Increased placental mitochondrial fusion in gestational diabetes mellitus: an adaptive mechanism to optimize feto-placental metabolic homeostasis? BMJ Open Diabetes Res Care. 2020;8(1):e000923. Abbade J, Klemetti MM, Farrell A, Ermini L, Gillmore T, Sallais J, et al. Increased placental mitochondrial fusion in gestational diabetes mellitus: an adaptive mechanism to optimize feto-placental metabolic homeostasis? BMJ Open Diabetes Res Care. 2020;8(1):e000923.
28.
go back to reference Ni HM, Williams JA, Ding WX. Mitochondrial dynamics and mitochondrial quality control. Redox Biol. 2015;4:6–13.PubMedCrossRef Ni HM, Williams JA, Ding WX. Mitochondrial dynamics and mitochondrial quality control. Redox Biol. 2015;4:6–13.PubMedCrossRef
29.
go back to reference Kung-Chun Chiu D, Pui-Wah Tse A, Law CT, Ming-Jing XuI, Lee D, Chen M, et al. Hypoxia regulates the mitochondrial activity of hepatocellular carcinoma cells through HIF/HEY1/PINK1 pathway. Cell Death Dis. 2019;10(12):934.PubMedPubMedCentralCrossRef Kung-Chun Chiu D, Pui-Wah Tse A, Law CT, Ming-Jing XuI, Lee D, Chen M, et al. Hypoxia regulates the mitochondrial activity of hepatocellular carcinoma cells through HIF/HEY1/PINK1 pathway. Cell Death Dis. 2019;10(12):934.PubMedPubMedCentralCrossRef
30.
go back to reference Zimmet JM, Hare JM. Nitroso-redox interactions in the cardiovascular system. Circulation. 2006;114(14):1531–44.PubMedCrossRef Zimmet JM, Hare JM. Nitroso-redox interactions in the cardiovascular system. Circulation. 2006;114(14):1531–44.PubMedCrossRef
31.
go back to reference Choi IY, Lee JC, Ju C, Hwang S, Cho GS, Lee HW, et al. A3 adenosine receptor agonist reduces brain ischemic injury and inhibits inflammatory cell migration in rats. Am J Pathol. 2011;179(4):2042–52.PubMedPubMedCentralCrossRef Choi IY, Lee JC, Ju C, Hwang S, Cho GS, Lee HW, et al. A3 adenosine receptor agonist reduces brain ischemic injury and inhibits inflammatory cell migration in rats. Am J Pathol. 2011;179(4):2042–52.PubMedPubMedCentralCrossRef
32.
go back to reference Carvalho LF, Samadder AN, Agarwal A, Fernandes LF, Abrao MS. Oxidative stress biomarkers in patients with endometriosis: systematic review. Arch Gynecol Obstet. 2012;286(4):1033–40.PubMedCrossRef Carvalho LF, Samadder AN, Agarwal A, Fernandes LF, Abrao MS. Oxidative stress biomarkers in patients with endometriosis: systematic review. Arch Gynecol Obstet. 2012;286(4):1033–40.PubMedCrossRef
33.
go back to reference Li J, Liu X, Wang H, Zhang W, Chan DC, Shi Y. Lysocardiolipin acyltransferase 1 (ALCAT1) controls mitochondrial DNA fidelity and biogenesis through modulation of MFN2 expression. Proc Natl Acad Sci U S A. 2012;109(18):6975–80.PubMedPubMedCentralCrossRef Li J, Liu X, Wang H, Zhang W, Chan DC, Shi Y. Lysocardiolipin acyltransferase 1 (ALCAT1) controls mitochondrial DNA fidelity and biogenesis through modulation of MFN2 expression. Proc Natl Acad Sci U S A. 2012;109(18):6975–80.PubMedPubMedCentralCrossRef
34.
go back to reference Wu W, Lin C, Wu K, Jiang L, Wang X, Li W, et al. FUNDC1 regulates mitochondrial dynamics at the ER-mitochondrial contact site under hypoxic conditions. EMBO J. 2016;35(13):1368–84.PubMedPubMedCentralCrossRef Wu W, Lin C, Wu K, Jiang L, Wang X, Li W, et al. FUNDC1 regulates mitochondrial dynamics at the ER-mitochondrial contact site under hypoxic conditions. EMBO J. 2016;35(13):1368–84.PubMedPubMedCentralCrossRef
35.
go back to reference Kobashigawa S, Suzuki K, Yamashita S. Ionizing radiation accelerates DRP1-dependent mitochondrial fission, which involves delayed mitochondrial reactive oxygen species production in normal human fibroblast-like cells. Biochem Biophys Res Commun. 2011;414(4):795–800.PubMedCrossRef Kobashigawa S, Suzuki K, Yamashita S. Ionizing radiation accelerates DRP1-dependent mitochondrial fission, which involves delayed mitochondrial reactive oxygen species production in normal human fibroblast-like cells. Biochem Biophys Res Commun. 2011;414(4):795–800.PubMedCrossRef
36.
go back to reference Peng L, Men X, Zhang W, Wang H, Xu S, Xu M, et al. Dynamin-related protein 1 is implicated in endoplasmic reticulum stress-induced pancreatic beta-cell apoptosis. Int J Mol Med. 2011;28(2):161–9.PubMed Peng L, Men X, Zhang W, Wang H, Xu S, Xu M, et al. Dynamin-related protein 1 is implicated in endoplasmic reticulum stress-induced pancreatic beta-cell apoptosis. Int J Mol Med. 2011;28(2):161–9.PubMed
37.
go back to reference Sha G, Wu D, Zhang L, Chen X, Lei M, Sun H, et al. Differentially expressed genes in human endometrial endothelial cells derived from eutopic endometrium of patients with endometriosis compared with those from patients without endometriosis. Hum Reprod. 2007;22(12):3159–69.PubMedCrossRef Sha G, Wu D, Zhang L, Chen X, Lei M, Sun H, et al. Differentially expressed genes in human endometrial endothelial cells derived from eutopic endometrium of patients with endometriosis compared with those from patients without endometriosis. Hum Reprod. 2007;22(12):3159–69.PubMedCrossRef
38.
go back to reference Houshdaran S, Nezhat CR, Vo KC, Zelenko Z, Irwin JC, Giudice LC. Aberrant endometrial DNA methylome and associated gene expression in women with endometriosis. Biol Reprod. 2016;95(5):93.PubMedPubMedCentralCrossRef Houshdaran S, Nezhat CR, Vo KC, Zelenko Z, Irwin JC, Giudice LC. Aberrant endometrial DNA methylome and associated gene expression in women with endometriosis. Biol Reprod. 2016;95(5):93.PubMedPubMedCentralCrossRef
39.
go back to reference Meola J, Rosa e Silva JC, Dentillo DB, da Silva WA, Jr., Veiga-Castelli LC, Bernardes LA, et al. Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis. Fertil Steril. 2010;93(6):1750–73. Meola J, Rosa e Silva JC, Dentillo DB, da Silva WA, Jr., Veiga-Castelli LC, Bernardes LA, et al. Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis. Fertil Steril. 2010;93(6):1750–73.
40.
go back to reference Braun DP, Ding J, Shaheen F, Willey JC, Rana N, Dmowski WP. Quantitative expression of apoptosis-regulating genes in endometrium from women with and without endometriosis. Fertil Steril. 2007;87(2):263–8.PubMedCrossRef Braun DP, Ding J, Shaheen F, Willey JC, Rana N, Dmowski WP. Quantitative expression of apoptosis-regulating genes in endometrium from women with and without endometriosis. Fertil Steril. 2007;87(2):263–8.PubMedCrossRef
41.
go back to reference Adamczyk M, Wender-Ozegowska E, Kedzia M. Epigenetic factors in eutopic endometrium in women with endometriosis and infertility. Int J Mol Sci. 2022;23(7):3804. Adamczyk M, Wender-Ozegowska E, Kedzia M. Epigenetic factors in eutopic endometrium in women with endometriosis and infertility. Int J Mol Sci. 2022;23(7):3804.
42.
go back to reference Ahn SH, Singh V, Tayade C. Biomarkers in endometriosis: challenges and opportunities. Fertil Steril. 2017;107(3):523–32.PubMedCrossRef Ahn SH, Singh V, Tayade C. Biomarkers in endometriosis: challenges and opportunities. Fertil Steril. 2017;107(3):523–32.PubMedCrossRef
43.
go back to reference Janikiewicz J, Hanzelka K, Dziewulska A, Kozinski K, Dobrzyn P, Bernas T, et al. Inhibition of SCD1 impairs palmitate-derived autophagy at the step of autophagosome-lysosome fusion in pancreatic beta-cells. J Lipid Res. 2015;56(10):1901–11.PubMedPubMedCentralCrossRef Janikiewicz J, Hanzelka K, Dziewulska A, Kozinski K, Dobrzyn P, Bernas T, et al. Inhibition of SCD1 impairs palmitate-derived autophagy at the step of autophagosome-lysosome fusion in pancreatic beta-cells. J Lipid Res. 2015;56(10):1901–11.PubMedPubMedCentralCrossRef
44.
go back to reference Lin X, Dai Y, Xu W, Shi L, Jin X, Li C, et al. Hypoxia promotes ectopic adhesion ability of endometrial stromal cells via TGF-beta1/Smad signaling in endometriosis. Endocrinology. 2018;159(4):1630–41.PubMedCrossRef Lin X, Dai Y, Xu W, Shi L, Jin X, Li C, et al. Hypoxia promotes ectopic adhesion ability of endometrial stromal cells via TGF-beta1/Smad signaling in endometriosis. Endocrinology. 2018;159(4):1630–41.PubMedCrossRef
45.
go back to reference Rodrigues T, Ferraz LS. Therapeutic potential of targeting mitochondrial dynamics in cancer. Biochem Pharmacol. 2020;182: 114282.PubMedCrossRef Rodrigues T, Ferraz LS. Therapeutic potential of targeting mitochondrial dynamics in cancer. Biochem Pharmacol. 2020;182: 114282.PubMedCrossRef
46.
go back to reference An J, Shi J, He Q, Lui K, Liu Y, Huang Y, et al. CHCM1/CHCHD6, novel mitochondrial protein linked to regulation of mitofilin and mitochondrial cristae morphology. J Biol Chem. 2012;287(10):7411–26.PubMedPubMedCentralCrossRef An J, Shi J, He Q, Lui K, Liu Y, Huang Y, et al. CHCM1/CHCHD6, novel mitochondrial protein linked to regulation of mitofilin and mitochondrial cristae morphology. J Biol Chem. 2012;287(10):7411–26.PubMedPubMedCentralCrossRef
47.
go back to reference Pernas L, Scorrano L. Mito-morphosis: mitochondrial fusion, fission, and cristae remodeling as key mediators of cellular function. Annu Rev Physiol. 2016;78:505–31.PubMedCrossRef Pernas L, Scorrano L. Mito-morphosis: mitochondrial fusion, fission, and cristae remodeling as key mediators of cellular function. Annu Rev Physiol. 2016;78:505–31.PubMedCrossRef
48.
go back to reference Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, Rudka T, et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell. 2006;126(1):177–89. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, Rudka T, et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell. 2006;126(1):177–89.
49.
go back to reference Emanuele S, D’Anneo A, Bellavia G, Vassallo B, Lauricella M, De Blasio A, et al. Sodium butyrate induces apoptosis in human hepatoma cells by a mitochondria/caspase pathway, associated with degradation of beta-catenin, pRb and Bcl-XL. Eur J Cancer. 2004;40(9):1441–52.PubMedCrossRef Emanuele S, D’Anneo A, Bellavia G, Vassallo B, Lauricella M, De Blasio A, et al. Sodium butyrate induces apoptosis in human hepatoma cells by a mitochondria/caspase pathway, associated with degradation of beta-catenin, pRb and Bcl-XL. Eur J Cancer. 2004;40(9):1441–52.PubMedCrossRef
50.
go back to reference Shan A, Li M, Li X, Li Y, Yan M, Xian P, et al. BDE-47 decreases progesterone levels in BeWo cells by interfering with mitochondrial functions and genes related to cholesterol transport. Chem Res Toxicol. 2019;32(4):621–8.PubMedCrossRef Shan A, Li M, Li X, Li Y, Yan M, Xian P, et al. BDE-47 decreases progesterone levels in BeWo cells by interfering with mitochondrial functions and genes related to cholesterol transport. Chem Res Toxicol. 2019;32(4):621–8.PubMedCrossRef
Metadata
Title
Abnormal expression of fission and fusion genes and the morphology of mitochondria in eutopic and ectopic endometrium
Authors
Chaoshuang Ye
Pei Chen
Bingning Xu
Yang Jin
Yongchao Pan
Tianyu Wu
Yongjiang Du
Jingxia Mao
Ruijin Wu
Publication date
01-12-2023
Publisher
BioMed Central
Keyword
Endometriosis
Published in
European Journal of Medical Research / Issue 1/2023
Electronic ISSN: 2047-783X
DOI
https://doi.org/10.1186/s40001-023-01180-w

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