Research status and prospect of DNA methylation in liver regeneration_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

HE Yutao ^1,2 ,  RAN Jianghua ^1,2

1. Department of Hepatobiliary and Pancreatic Surgery, Calmete Hospital Affiliated to Kunming Medical University, Kunming 650011,P. R. China;
2. The First People’s Hospital of Kunming, Kunming 650011, P. R. China;

Corresponding author：

RAN Jianghua, Email: rih2u@163.com

Keywords：

DNA methylation; liver regeneration; epigenetics; DNA methyltransferase; ubiquitin-like plant homeodomain and ring finger domain 1

DOI：

10.7507/1007-9424.201907109

Video：

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Objective To summarize the current research status of the relationship between DNA methylation and liver regeneration.Method The related literatures at home and abroad were searched to review the studies on relationships between the methylation level of liver cells, regulation of gene expression, and methylation related proteins and liver regeneration.Results The DNA methylation was an important epigenetic regulation method in vivo and its role in the liver regeneration had been paid more and more attentions in recent years. The existing studies had found the epigenetic phenomena during the liver regeneration such as the genomic hypomethylation, methylation changes of related proliferating genes and DNA methyltransferase and UHRF1 regulation of the liver regeneration.Conclusions There are many relationships between DNA methylation and liver regeneration. Regulation of liver regeneration from DNA methylation level is expected to become a reality in the near future.

Citation： HE Yutao, RAN Jianghua. Research status and prospect of DNA methylation in liver regeneration. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(4): 494-498. doi: 10.7507/1007-9424.201907109 Copy

1.	Berasain C, Avila MA. Regulation of hepatocyte identity and quiescence. Cell Mol Life Sci, 2015, 72(20): 3831-3851.
2.	Hammond JS, Guha IN, Beckingham IJ, et al. Prediction, prevention and management of postresection liver failure. Br J Surg, 2011, 98(9): 1188-1200.
3.	Fatemi M, Wade PA. MBD family proteins: reading the epigenetic code. J Cell Sci, 2006, 119(Pt 15): 3033-3037.
4.	Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet, 2012, 13(7): 484-492.
5.	Li Z, Feng J, Sun X. Hypomethylation and hypohydroxymethylation of DNA in hepatocellular carcinoma and cholangiocarcinoma. Hepatology, 2016, 63(5): 1745-1746.
6.	Kanduc D, Ghoshal A, Quagliariello E, et al. DNA hypomethylation in ethionine-induced rat preneoplastic hepatocyte nodules. Biochem Biophys Res Commun, 1988, 150(2): 739-744.
7.	Götze S, Schumacher EC, Kordes C, et al. Epigenetic changes during hepatic stellate cell activation. PLoS One, 2015, 10(6): e0128745.
8.	El Taghdouini A, Sørensen AL, Reiner AH, et al. Genome-wide analysis of DNA methylation and gene expression patterns in purified, uncultured human liver cells and activated hepatic stellate cells. Oncotarget, 2015, 6(29): 26729-26745.
9.	Deng X, Chen YX, Zhang X, et al. Hepatic stellate cells modulate the differentiation of bone marrow mesenchymal stem cells into hepatocyte-like cells. J Cell Physiol, 2008, 217(1): 138-144.
10.	Kocabayoglu P, Zhang DY, Kojima K, et al. Induction and contribution of beta platelet-derived growth factor signalling by hepatic stellate cells to liver regeneration after partial hepatectomy in mice. Liver Int, 2016, 36(6): 874-882.
11.	Donahower BC, McCullough SS, Hennings L, et al. Human recombinant vascular endothelial growth factor reduces necrosis and enhances hepatocyte regeneration in a mouse model of acetaminophen toxicity. J Pharmacol Exp Ther, 2010, 334(1): 33-43.
12.	Ding BS, Nolan DJ, Butler JM, et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature, 2010, 468(7321): 310-315.
13.	Tan Q, Hu J, Yu X, et al. The role of IL-1 family members and Kupffer cells in liver regeneration. Biomed Res Int, 2016, 2016: 6495793.
14.	Zhang W, Chen XP, Zhang WG, et al. Hepatic non-parenchymal cells and extracellular matrix participate in oval cell-mediated liver regeneration. World J Gastroenterol, 2009, 15(5): 552-560.
15.	Yang X, He C, Zhu L, et al. Comparative analysis of regulatory role of Notch signaling pathway in 8 types liver cell during liver regeneration. Biochem Genet, 2019, 57(1): 1-19.
16.	Chang CF, Yang J, Zhao WM, et al. Gene expression profiling analysis of 5-hydroxytryptamine signaling pathway in rat regenerating liver and different types of liver cells. Genet Mol Res, 2015, 14(2): 3409-3420.
17.	Górnikiewicz B, Ronowicz A, Podolak J, et al. Epigenetic basis of regeneration: analysis of genomic DNA methylation profiles in the MRL/MpJ mouse. DNA Res, 2013, 20(6): 605-621.
18.	Liang P, Song F, Ghosh S, et al. Genome-wide survey reveals dynamic widespread tissue-specific changes in DNA methylation during development. BMC Genomics, 2011, 12(1): 231.
19.	Chernyavskaya Y, Mudbhary R, Zhang C, et al. Loss of DNA methylation in zebrafish embryos activates retrotransposons to trigger antiviral signaling. Development, 2017, 144(16): 2925-2939.
20.	Zhang X, Yazaki J, Sundaresan A, et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell, 2006, 126(6): 1189-1201.
21.	White UA, Stephens JM. The gp130 receptor cytokine family: regulators of adipocyte development and function. Curr Pharm Des, 2011, 17(4): 340-346.
22.	Lai HS, Lin WH, Lai SL, et al. Interleukin-6 mediates angio-tensinogen gene expression during liver regeneration. PLoS One, 2013, 8(7): e67868.
23.	Chou CH, Lai SL, Chen CN, et al. IL-6 regulates Mcl-1L expression through the JAK/PI3K/Akt/CREB signaling pathway in hepatocytes: implication of an anti-apoptotic role during liver regeneration. PLoS One, 2013, 8(6): e66268.
24.	Jung J, Moon JW, Choi JH, et al. Epigenetic alterations of IL-6/STAT3 signaling by placental stem cells promote hepatic regeneration in a rat model with CCl4-induced liver injury. Int J Stem Cells, 2015, 8(1): 79-89.
25.	Guo G, Xia J, Bao J, et al. Expression of SOCS3 throughout liver regeneration is not regulated by DNA methylation. Hepatobiliary Pancreat Dis Int, 2012, 11(4): 401-406.
26.	Niwa Y, Kanda H, Shikauchi Y, et al. Methylation silencing of SOCS-3 promotes cell growth and migration by enhancing JAK/STAT and FAK signalings in human hepatocellular carcinoma. Oncogene, 2005, 24(42): 6406-6417.
27.	Tischoff I, Hengge UR, Vieth M, et al. Methylation of SOCS-3 and SOCS-1 in the carcinogenesis of Barrett’s adenocarcinoma. Gut, 2007, 56(8): 1047-1053.
28.	He B, You L, Uematsu K, et al. SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc Natl Acad Sci U S A, 2003, 100(24): 14133-14138.
29.	Weber A, Hengge U R, Bardenheuer W, et al. SOCS-3 is frequently methylated in head and neck squamous cell carcinoma and its precursor lesions and causes growth inhibition. Oncogene, 2005, 24(44): 6699-6708.
30.	Di Gioia S, Bianchi P, Destro A, et al. Quantitative evaluation of RASSF1A methylation in the non-lesional, regenerative and neoplastic liver. BMC Cancer, 2006, 6: 89.
31.	Li D, Fan J, Li Z, et al. DNA methylation dynamics in the rat EGF gene promoter after partial hepatectomy. Genet Mol Biol, 2014, 37(2): 439-443.
32.	Kren BT, Trembley JH, Steer CJ. Alterations in mRNA stability during rat liver regeneration. Am J Physiol, 1996, 270(5 Pt 1): G763-G777.
33.	李紫薇, 徐存拴, 靳伟. 大鼠肝再生中 Fcgr2a 启动子区甲基化变化和作用研究. 河南师范大学, 2016.
34.	Robertson KD, Keyomarsi K, Gonzales FA, et al. Differential mRNA expression of the human DNA methyltransferases (DNMTs) 1, 3a and 3b during the G(0)/G(1) to S phase transition in normal and tumor cells. Nucleic Acids Res, 2000, 28(10): 2108-2113.
35.	Elliott EN, Sheaffer KL, Schug J, et al. DNMT1 is essential to maintain progenitors in the perinatal intestinal epithelium. Development, 2015, 142(12): 2163-2172.
36.	Brown KD, Robertson KD. DNMT1 knockout delivers a strong blow to genome stability and cell viability. Nat Genet, 2007, 39(3): 289-290.
37.	Chen T, Hevi S, Gay F, et al. Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat Genet, 2007, 39(3): 391-396.
38.	Jackson-Grusby L, Beard C, Possemato R, et al. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet, 2001, 27(1): 31-39.
39.	Campbell S, Ismail IH, Young LC, et al. Polycomb repressive complex 2 contributes to DNA double-strand break repair. Cell Cycle, 2013, 12(16): 2675-2683.
40.	Kaji K, Factor VM, Andersen JB, et al. DNMT1 is a required genomic regulator for murine liver histogenesis and regeneration. Hepatology, 2016, 64(2): 582-598.
41.	Sharif J, Muto M, Takebayashi S, et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting DNMT1 to methylated DNA. Nature, 2007, 450(7171): 908-912.
42.	Jacob V, Chernyavskaya Y, Chen X, et al. DNA hypomethylation induces a DNA replication-associated cell cycle arrest to block hepatic outgrowth in uhrf1 mutant zebrafish embryos. Development, 2015, 142(3): 510-521.
43.	Wang S, Zhang C, Hasson D, et al. Epigenetic compensation promotes liver regeneration. Dev Cell, 2019, 50(1): 43-56.
44.	Walter M, Teissandier A, Pérez-Palacios R, et al. An epigenetic switch ensures transposon repression upon dynamic loss of DNA methylation in embryonic stem cells. Elife, 2016, 5: pii: e11418.
45.	Sun X, Chuang JC, Kanchwala M, et al. Suppression of the SWI/SNF component arid1a promotes mammalian regeneration. Cell Stem Cell, 2016, 18(4): 456-466.

1. Berasain C, Avila MA. Regulation of hepatocyte identity and quiescence. Cell Mol Life Sci, 2015, 72(20): 3831-3851.
2. Hammond JS, Guha IN, Beckingham IJ, et al. Prediction, prevention and management of postresection liver failure. Br J Surg, 2011, 98(9): 1188-1200.
3. Fatemi M, Wade PA. MBD family proteins: reading the epigenetic code. J Cell Sci, 2006, 119(Pt 15): 3033-3037.
4. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet, 2012, 13(7): 484-492.
5. Li Z, Feng J, Sun X. Hypomethylation and hypohydroxymethylation of DNA in hepatocellular carcinoma and cholangiocarcinoma. Hepatology, 2016, 63(5): 1745-1746.
6. Kanduc D, Ghoshal A, Quagliariello E, et al. DNA hypomethylation in ethionine-induced rat preneoplastic hepatocyte nodules. Biochem Biophys Res Commun, 1988, 150(2): 739-744.
7. Götze S, Schumacher EC, Kordes C, et al. Epigenetic changes during hepatic stellate cell activation. PLoS One, 2015, 10(6): e0128745.
8. El Taghdouini A, Sørensen AL, Reiner AH, et al. Genome-wide analysis of DNA methylation and gene expression patterns in purified, uncultured human liver cells and activated hepatic stellate cells. Oncotarget, 2015, 6(29): 26729-26745.
9. Deng X, Chen YX, Zhang X, et al. Hepatic stellate cells modulate the differentiation of bone marrow mesenchymal stem cells into hepatocyte-like cells. J Cell Physiol, 2008, 217(1): 138-144.
10. Kocabayoglu P, Zhang DY, Kojima K, et al. Induction and contribution of beta platelet-derived growth factor signalling by hepatic stellate cells to liver regeneration after partial hepatectomy in mice. Liver Int, 2016, 36(6): 874-882.
11. Donahower BC, McCullough SS, Hennings L, et al. Human recombinant vascular endothelial growth factor reduces necrosis and enhances hepatocyte regeneration in a mouse model of acetaminophen toxicity. J Pharmacol Exp Ther, 2010, 334(1): 33-43.
12. Ding BS, Nolan DJ, Butler JM, et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature, 2010, 468(7321): 310-315.
13. Tan Q, Hu J, Yu X, et al. The role of IL-1 family members and Kupffer cells in liver regeneration. Biomed Res Int, 2016, 2016: 6495793.
14. Zhang W, Chen XP, Zhang WG, et al. Hepatic non-parenchymal cells and extracellular matrix participate in oval cell-mediated liver regeneration. World J Gastroenterol, 2009, 15(5): 552-560.
15. Yang X, He C, Zhu L, et al. Comparative analysis of regulatory role of Notch signaling pathway in 8 types liver cell during liver regeneration. Biochem Genet, 2019, 57(1): 1-19.
16. Chang CF, Yang J, Zhao WM, et al. Gene expression profiling analysis of 5-hydroxytryptamine signaling pathway in rat regenerating liver and different types of liver cells. Genet Mol Res, 2015, 14(2): 3409-3420.
17. Górnikiewicz B, Ronowicz A, Podolak J, et al. Epigenetic basis of regeneration: analysis of genomic DNA methylation profiles in the MRL/MpJ mouse. DNA Res, 2013, 20(6): 605-621.
18. Liang P, Song F, Ghosh S, et al. Genome-wide survey reveals dynamic widespread tissue-specific changes in DNA methylation during development. BMC Genomics, 2011, 12(1): 231.
19. Chernyavskaya Y, Mudbhary R, Zhang C, et al. Loss of DNA methylation in zebrafish embryos activates retrotransposons to trigger antiviral signaling. Development, 2017, 144(16): 2925-2939.
20. Zhang X, Yazaki J, Sundaresan A, et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell, 2006, 126(6): 1189-1201.
21. White UA, Stephens JM. The gp130 receptor cytokine family: regulators of adipocyte development and function. Curr Pharm Des, 2011, 17(4): 340-346.
22. Lai HS, Lin WH, Lai SL, et al. Interleukin-6 mediates angio-tensinogen gene expression during liver regeneration. PLoS One, 2013, 8(7): e67868.
23. Chou CH, Lai SL, Chen CN, et al. IL-6 regulates Mcl-1L expression through the JAK/PI3K/Akt/CREB signaling pathway in hepatocytes: implication of an anti-apoptotic role during liver regeneration. PLoS One, 2013, 8(6): e66268.
24. Jung J, Moon JW, Choi JH, et al. Epigenetic alterations of IL-6/STAT3 signaling by placental stem cells promote hepatic regeneration in a rat model with CCl4-induced liver injury. Int J Stem Cells, 2015, 8(1): 79-89.
25. Guo G, Xia J, Bao J, et al. Expression of SOCS3 throughout liver regeneration is not regulated by DNA methylation. Hepatobiliary Pancreat Dis Int, 2012, 11(4): 401-406.
26. Niwa Y, Kanda H, Shikauchi Y, et al. Methylation silencing of SOCS-3 promotes cell growth and migration by enhancing JAK/STAT and FAK signalings in human hepatocellular carcinoma. Oncogene, 2005, 24(42): 6406-6417.
27. Tischoff I, Hengge UR, Vieth M, et al. Methylation of SOCS-3 and SOCS-1 in the carcinogenesis of Barrett’s adenocarcinoma. Gut, 2007, 56(8): 1047-1053.
28. He B, You L, Uematsu K, et al. SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc Natl Acad Sci U S A, 2003, 100(24): 14133-14138.
29. Weber A, Hengge U R, Bardenheuer W, et al. SOCS-3 is frequently methylated in head and neck squamous cell carcinoma and its precursor lesions and causes growth inhibition. Oncogene, 2005, 24(44): 6699-6708.
30. Di Gioia S, Bianchi P, Destro A, et al. Quantitative evaluation of RASSF1A methylation in the non-lesional, regenerative and neoplastic liver. BMC Cancer, 2006, 6: 89.
31. Li D, Fan J, Li Z, et al. DNA methylation dynamics in the rat EGF gene promoter after partial hepatectomy. Genet Mol Biol, 2014, 37(2): 439-443.
32. Kren BT, Trembley JH, Steer CJ. Alterations in mRNA stability during rat liver regeneration. Am J Physiol, 1996, 270(5 Pt 1): G763-G777.
33. 李紫薇, 徐存拴, 靳伟. 大鼠肝再生中 Fcgr2a 启动子区甲基化变化和作用研究. 河南师范大学, 2016.
34. Robertson KD, Keyomarsi K, Gonzales FA, et al. Differential mRNA expression of the human DNA methyltransferases (DNMTs) 1, 3a and 3b during the G(0)/G(1) to S phase transition in normal and tumor cells. Nucleic Acids Res, 2000, 28(10): 2108-2113.
35. Elliott EN, Sheaffer KL, Schug J, et al. DNMT1 is essential to maintain progenitors in the perinatal intestinal epithelium. Development, 2015, 142(12): 2163-2172.
36. Brown KD, Robertson KD. DNMT1 knockout delivers a strong blow to genome stability and cell viability. Nat Genet, 2007, 39(3): 289-290.
37. Chen T, Hevi S, Gay F, et al. Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat Genet, 2007, 39(3): 391-396.
38. Jackson-Grusby L, Beard C, Possemato R, et al. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet, 2001, 27(1): 31-39.
39. Campbell S, Ismail IH, Young LC, et al. Polycomb repressive complex 2 contributes to DNA double-strand break repair. Cell Cycle, 2013, 12(16): 2675-2683.
40. Kaji K, Factor VM, Andersen JB, et al. DNMT1 is a required genomic regulator for murine liver histogenesis and regeneration. Hepatology, 2016, 64(2): 582-598.
41. Sharif J, Muto M, Takebayashi S, et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting DNMT1 to methylated DNA. Nature, 2007, 450(7171): 908-912.
42. Jacob V, Chernyavskaya Y, Chen X, et al. DNA hypomethylation induces a DNA replication-associated cell cycle arrest to block hepatic outgrowth in uhrf1 mutant zebrafish embryos. Development, 2015, 142(3): 510-521.
43. Wang S, Zhang C, Hasson D, et al. Epigenetic compensation promotes liver regeneration. Dev Cell, 2019, 50(1): 43-56.
44. Walter M, Teissandier A, Pérez-Palacios R, et al. An epigenetic switch ensures transposon repression upon dynamic loss of DNA methylation in embryonic stem cells. Elife, 2016, 5: pii: e11418.
45. Sun X, Chuang JC, Kanchwala M, et al. Suppression of the SWI/SNF component arid1a promotes mammalian regeneration. Cell Stem Cell, 2016, 18(4): 456-466.

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Research status and prospect of DNA methylation in liver regeneration

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