- 1. Department of Hepatobiliary Surgery, Wuxi Clinical School, Anhui Medical University, Wuxi, Jiangsu 214044, P.R.China;
- 2. Department of Hepatobiliary Surgery, The 101th Hospital of PLA, Wuxi, Jiangsu 214044, P.R.China;
Citation: LIU Weiwei, LUO Kunlun. Research progress in clinical application of liver regeneration. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2017, 24(4): 512-517. doi: 10.7507/1007-9424.201608105 Copy
1. | Fausto N, Campbell JS, Riehle KJ. Liver regeneration. Hepatology, 2006, 43(2 Suppl 1): S45-S53. |
2. | Michalopoulos GK. Liver regeneration. J Cell Physiol, 2007, 213(2): 286-300. |
3. | Clavien PA, Petrowsky H, DeOliveira ML,et al. Strategies for safer liver surgery and partial liver transplantation. N Engl J Med, 2007, 356(15): 1545-1559. |
4. | Duncan AW, Dorrell C, Grompe M. Stem cells and liver regeneration. Gastroenterology, 2009, 137(2): 466-481. |
5. | Duncan AW, Soto-Gutierrez A. Liver repopulation and regeneration: new approaches to old questions. Curr Opin Organ Transplant, 2013, 18(2): 197-202. |
6. | Suzuki Y, Katagiri H, Wang T,et al. Ductular reactions in the liver regeneration process with local inflammation after physical partial hepatectomy. Lab Invest, 2016, 96(11): 1211-1222. |
7. | Albrecht J H. MET and epidermal growth factor signaling: The pillars of liver regeneration? Hepatology, 2016, 64(5): 1427-1429. |
8. | Wang B, Zhao L, Fish M,et al. Self-renewing diploid Axin2+ cells fuel homeostatic renewal of the liver. Nature, 2015, 524(7564): 180-185. |
9. | Li G, L GG. Farnesoid X receptor, the bile acid sensing nuclear receptor, in liver regeneration. Acta Pharm Sin B, 2015, 5(2): 93-98. |
10. | Mortensen KE, Revhaug A. Liver regeneration in surgical animal models—a historical perspective and clinical implications. Eur Surg Res, 2011, 46(1): 1-18. |
11. | Kandilis AN, Koskinas J, Tiniakos DG,et al. Liver regeneration: focus on cell types and topographic differences. Eur Surg Res, 2010, 44(1): 1-12. |
12. | Black D, Lyman S, Heider TR,et al. Molecular and cellular features of hepatic regeneration. J Surg Res, 2004, 117(2): 306-315. |
13. | Zimmermann A. Regulation of liver regeneration. Nephrol Dial Transplant, 2004, 19 Suppl 4: v6-v10. |
14. | Kountouras J, Boura P, Lygidakis NJ. Liver regeneration after hepatectomy. Hepatogastroenterology, 2001, 48(38): 556-562. |
15. | Diehl AM. Cytokine regulation of liver injury and repair. Immunol Rev, 2000, 174: 160-171. |
16. | Kay MA, Fausto N. Liver regeneration: prospects for therapy based on new technologies. Mol Med Today, 1997, 3(3): 108-115. |
17. | Taub R. Liver regeneration 4: transcriptional control of liver regeneration. FASEB J, 1996, 10(4): 413-427. |
18. | Diehl AM, Rai RM. Liver regeneration 3: Regulation of signal transduction during liver regeneration. FASEB J, 1996, 10(2): 215-227. |
19. | Fausto N. Growth factors in liver development, regeneration and carcinogenesis. 1991, 3(3): 219-234. |
20. | Leffert HL, Koch KS, Lu XP,et al. Cellular and molecular biology of hepatocyte growth, regeneration and gene expression. Adv Second Messenger Phosphoprotein Res, 1990, 24: 352-358. |
21. | Michalopoulos GK. Liver regeneration: molecular mechanisms of growth control. FASEB J, 1990, 4(2): 176-187. |
22. | Alison MR. Regulation of hepatic growth. Physiol Rev, 1986, 66(3): 499-541. |
23. | Abshagen K, Eipel C, Vollmar B. A critical appraisal of the hemodynamic signal driving liver regeneration. Langenbecks Arch Surg, 2012, 397(4): 579-590. |
24. | Crumm S, Cofan M, Juskeviciute E,et al. Adenine nucleotide changes in the remnant liver: An early signal for regeneration after partial hepatectomy. Hepatology, 2008, 48(3): 898-908. |
25. | Weiskirchen R, Tacke F. Cellular and molecular functions of hepatic stellate cells in inflammatory responses and liver immunology. Hepatobiliary Surg Nutr, 2014, 3(6): 344-363. |
26. | Yamada Y, Kirillova I, Peschon JJ,et al. Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type Ⅰ tumor necrosis factor receptor. Proc Natl Acad Sci U S A, 1997, 94(4): 1441-1446. |
27. | Mohammed FF, Khokha R. Thinking outside the cell: proteases regulate hepatocyte division. Trends Cell Biol, 2005, 15(10): 555-563. |
28. | Pediaditakis P, Lopez-Talavera JC, Petersen B,et al. The processing and utilization of hepatocyte growth factor/scatter factor following partial hepatectomy in the rat. Hepatology, 2001, 34(4 Pt 1): 688-693. |
29. | Takebe T, Sekine K, Enomura M,et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature, 2013, 499(7459): 481-484. |
30. | Zheng ZY, Weng SY, Yu Y. Signal molecule-mediated hepatic cell communication during liver regeneration. World J Gastroenterol, 2009, 15(46): 5776-5783. |
31. | Apte U, Gkretsi V, Bowen WC,et al. Enhanced liver regeneration following changes induced by hepatocyte-specific genetic ablation of integrin-linked kinase. Hepatology, 2009, 50(3): 844-851. |
32. | 姚豫桐, 李可洲, 吴晓玲, 等. 转化生长因子 α 和 β1 在极限门静脉结扎肝脏组织中的表达及其意义. 中国普外基础与临床杂志, 2010, 17(7): 719-724. |
33. | Michalopoulos GK. Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am J Pathol, 2010, 176(1): 2-13. |
34. | Oe S, Lemmer ER, Conner EA,et al. Intact signaling by transforming growth factor beta is not required for termination of liver regeneration in mice. Hepatology, 2004, 40(5): 1098-1105. |
35. | Bohm F, Kohler UA, Speicher T,et al. Regulation of liver regeneration by growth factors and cytokines. EMBO Mol Med, 2010, 2(8): 294-305. |
36. | Sato Y, Tsukada K, Hatakeyama K. Role of shear stress and immune responses in liver regeneration after a partial hepatectomy. Surg Today, 1999, 29(1): 1-9. |
37. | Schoen JM, Wang HH, Minuk GY,et al. Shear stress-induced nitric oxide release triggers the liver regeneration cascade. Nitric Oxide, 2001, 5(5): 453-464. |
38. | Roskams TA, Theise ND, Balabaud C,et al. Nomenclature of the finer branches of the biliary tree: canals, ductules, and ductular reactions in human livers. Hepatology, 2004, 39(6): 1739-1745. |
39. | Michalopoulos GK. Liver regeneration: alternative epithelial pathways. Int J Biochem Cell Biol, 2011, 43(2): 173-179. |
40. | Forbes SJ, Newsome P N. Liver regeneration - mechanisms and models to clinical application. Nat Rev Gastroenterol Hepatol, 2016, 13(8): 473-485. |
41. | Kauffmann R, Fong Y. Post-hepatectomy liver failure. Hepatobiliary Surg Nutr, 2014, 3(5): 238-246. |
42. | Balzan S, Belghiti J, Farges O,et al. The "50-50 criteria" on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg, 2005, 242(6): 824-828, 829. |
43. | Rahbari NN, Garden OJ, Padbury R,et al. Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery, 2011, 149(5): 713-724. |
44. | Schindl MJ, Redhead DN, Fearon KC,et al. The value of residual liver volume as a predictor of hepatic dysfunction and infection after major liver resection. Gut, 2005, 54(2): 289-296. |
45. | Kinoshita H, Sakai K, Hirohashi K,et al. Preoperative portal vein embolization for hepatocellular carcinoma. World J Surg, 1986, 10(5): 803-808. |
46. | Yokoyama Y, Nagino M, Nimura Y. Mechanisms of hepatic regeneration following portal vein embolization and partial hepatectomy: a review. World J Surg, 2007, 31(2): 367-374. |
47. | Madoff DC, Abdalla EK, Vauthey JN. Portal vein embolization in preparation for major hepatic resection: evolution of a new standard of care. J Vasc Interv Radiol, 2005, 16(6): 779-790. |
48. | Ogata S, Belghiti J, Farges O,et al. Sequential arterial and portal vein embolizations before right hepatectomy in patients with cirrhosis and hepatocellular carcinoma. Br J Surg, 2006, 93(9): 1091-1098. |
49. | Ghobrial RM, Freise CE, Trotter JF,et al. Donor morbidity after living donation for liver transplantation. Gastroenterology, 2008, 135(2): 468-476. |
50. | Soejima Y, Taketomi A, Yoshizumi T,et al. Feasibility of left lobe living donor liver transplantation between adults: an 8-year, single-center experience of 107 cases. Am J Transplant, 2006, 6(5 Pt 1): 1004-1011. |
51. | Soejima Y, Shimada M, Suehiro T,et al. Outcome analysis in adult-to-adult living donor liver transplantation using the left lobe. Liver Transpl, 2003, 9(6): 581-586. |
52. | Ikegami T, Shimada M, Imura S,et al. Current concept of small-for-size grafts in living donor liver transplantation. Surg Today, 2008, 38(11): 971-982. |
53. | Schnitzbauer AA, Lang SA, Goessmann H,et al. Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling 2-staged extended right hepatic resection in small-for-size settings. Ann Surg, 2012, 255(3): 405-414. |
54. | Knoefel WT, Gabor I, Rehders A,et al. In situ liver transection with portal vein ligation for rapid growth of the future liver remnant in two-stage liver resection. Br J Surg, 2013, 100(3): 388-394. |
55. | Zhang GQ, Zhang ZW, Lau WY,et al. Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): a new strategy to increase resectability in liver surgery. Int J Surg, 2014, 12(5): 437-441. |
56. | Takahashi K, Tanabe K, Ohnuki M,et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 2007, 131(5): 861-872. |
57. | Kuijk E W, Rasmussen S, Blokzijl F,et al. Generation and characterization of rat liver stem cell lines and their engraftment in a rat model of liver failure. Sci Rep, 2016, 6: 22154. |
58. | Kakinuma S, Nakauchi H, Watanabe M. Hepatic stem/progenitor cells and stem-cell transplantation for the treatment of liver disease. J Gastroenterol, 2009, 44(3): 167-172. |
59. | Cordeiro-Spinetti E, de Mello W, Trindade LS,et al. Human bone marrow mesenchymal progenitors: perspectives on an optimizedin vitro manipulation. Front Cell Dev Biol, 2014, 2: 7. |
60. | Langer R, Vacanti JP. Tissue engineering. Science, 1993, 260(5110): 920-926. |
61. | Hoshiba T, Lu H, Kawazoe N,et al. Decellularized matrices for tissue engineering. Expert Opin Biol Ther, 2010, 10(12): 1717-1728. |
62. | Ott HC, Clippinger B, Conrad C,et al. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med, 2010, 16(8): 927-933. |
63. | Uygun BE, Soto-Gutierrez A, Yagi H,et al. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med, 2010, 16(7): 814-820. |
- 1. Fausto N, Campbell JS, Riehle KJ. Liver regeneration. Hepatology, 2006, 43(2 Suppl 1): S45-S53.
- 2. Michalopoulos GK. Liver regeneration. J Cell Physiol, 2007, 213(2): 286-300.
- 3. Clavien PA, Petrowsky H, DeOliveira ML,et al. Strategies for safer liver surgery and partial liver transplantation. N Engl J Med, 2007, 356(15): 1545-1559.
- 4. Duncan AW, Dorrell C, Grompe M. Stem cells and liver regeneration. Gastroenterology, 2009, 137(2): 466-481.
- 5. Duncan AW, Soto-Gutierrez A. Liver repopulation and regeneration: new approaches to old questions. Curr Opin Organ Transplant, 2013, 18(2): 197-202.
- 6. Suzuki Y, Katagiri H, Wang T,et al. Ductular reactions in the liver regeneration process with local inflammation after physical partial hepatectomy. Lab Invest, 2016, 96(11): 1211-1222.
- 7. Albrecht J H. MET and epidermal growth factor signaling: The pillars of liver regeneration? Hepatology, 2016, 64(5): 1427-1429.
- 8. Wang B, Zhao L, Fish M,et al. Self-renewing diploid Axin2+ cells fuel homeostatic renewal of the liver. Nature, 2015, 524(7564): 180-185.
- 9. Li G, L GG. Farnesoid X receptor, the bile acid sensing nuclear receptor, in liver regeneration. Acta Pharm Sin B, 2015, 5(2): 93-98.
- 10. Mortensen KE, Revhaug A. Liver regeneration in surgical animal models—a historical perspective and clinical implications. Eur Surg Res, 2011, 46(1): 1-18.
- 11. Kandilis AN, Koskinas J, Tiniakos DG,et al. Liver regeneration: focus on cell types and topographic differences. Eur Surg Res, 2010, 44(1): 1-12.
- 12. Black D, Lyman S, Heider TR,et al. Molecular and cellular features of hepatic regeneration. J Surg Res, 2004, 117(2): 306-315.
- 13. Zimmermann A. Regulation of liver regeneration. Nephrol Dial Transplant, 2004, 19 Suppl 4: v6-v10.
- 14. Kountouras J, Boura P, Lygidakis NJ. Liver regeneration after hepatectomy. Hepatogastroenterology, 2001, 48(38): 556-562.
- 15. Diehl AM. Cytokine regulation of liver injury and repair. Immunol Rev, 2000, 174: 160-171.
- 16. Kay MA, Fausto N. Liver regeneration: prospects for therapy based on new technologies. Mol Med Today, 1997, 3(3): 108-115.
- 17. Taub R. Liver regeneration 4: transcriptional control of liver regeneration. FASEB J, 1996, 10(4): 413-427.
- 18. Diehl AM, Rai RM. Liver regeneration 3: Regulation of signal transduction during liver regeneration. FASEB J, 1996, 10(2): 215-227.
- 19. Fausto N. Growth factors in liver development, regeneration and carcinogenesis. 1991, 3(3): 219-234.
- 20. Leffert HL, Koch KS, Lu XP,et al. Cellular and molecular biology of hepatocyte growth, regeneration and gene expression. Adv Second Messenger Phosphoprotein Res, 1990, 24: 352-358.
- 21. Michalopoulos GK. Liver regeneration: molecular mechanisms of growth control. FASEB J, 1990, 4(2): 176-187.
- 22. Alison MR. Regulation of hepatic growth. Physiol Rev, 1986, 66(3): 499-541.
- 23. Abshagen K, Eipel C, Vollmar B. A critical appraisal of the hemodynamic signal driving liver regeneration. Langenbecks Arch Surg, 2012, 397(4): 579-590.
- 24. Crumm S, Cofan M, Juskeviciute E,et al. Adenine nucleotide changes in the remnant liver: An early signal for regeneration after partial hepatectomy. Hepatology, 2008, 48(3): 898-908.
- 25. Weiskirchen R, Tacke F. Cellular and molecular functions of hepatic stellate cells in inflammatory responses and liver immunology. Hepatobiliary Surg Nutr, 2014, 3(6): 344-363.
- 26. Yamada Y, Kirillova I, Peschon JJ,et al. Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type Ⅰ tumor necrosis factor receptor. Proc Natl Acad Sci U S A, 1997, 94(4): 1441-1446.
- 27. Mohammed FF, Khokha R. Thinking outside the cell: proteases regulate hepatocyte division. Trends Cell Biol, 2005, 15(10): 555-563.
- 28. Pediaditakis P, Lopez-Talavera JC, Petersen B,et al. The processing and utilization of hepatocyte growth factor/scatter factor following partial hepatectomy in the rat. Hepatology, 2001, 34(4 Pt 1): 688-693.
- 29. Takebe T, Sekine K, Enomura M,et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature, 2013, 499(7459): 481-484.
- 30. Zheng ZY, Weng SY, Yu Y. Signal molecule-mediated hepatic cell communication during liver regeneration. World J Gastroenterol, 2009, 15(46): 5776-5783.
- 31. Apte U, Gkretsi V, Bowen WC,et al. Enhanced liver regeneration following changes induced by hepatocyte-specific genetic ablation of integrin-linked kinase. Hepatology, 2009, 50(3): 844-851.
- 32. 姚豫桐, 李可洲, 吴晓玲, 等. 转化生长因子 α 和 β1 在极限门静脉结扎肝脏组织中的表达及其意义. 中国普外基础与临床杂志, 2010, 17(7): 719-724.
- 33. Michalopoulos GK. Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am J Pathol, 2010, 176(1): 2-13.
- 34. Oe S, Lemmer ER, Conner EA,et al. Intact signaling by transforming growth factor beta is not required for termination of liver regeneration in mice. Hepatology, 2004, 40(5): 1098-1105.
- 35. Bohm F, Kohler UA, Speicher T,et al. Regulation of liver regeneration by growth factors and cytokines. EMBO Mol Med, 2010, 2(8): 294-305.
- 36. Sato Y, Tsukada K, Hatakeyama K. Role of shear stress and immune responses in liver regeneration after a partial hepatectomy. Surg Today, 1999, 29(1): 1-9.
- 37. Schoen JM, Wang HH, Minuk GY,et al. Shear stress-induced nitric oxide release triggers the liver regeneration cascade. Nitric Oxide, 2001, 5(5): 453-464.
- 38. Roskams TA, Theise ND, Balabaud C,et al. Nomenclature of the finer branches of the biliary tree: canals, ductules, and ductular reactions in human livers. Hepatology, 2004, 39(6): 1739-1745.
- 39. Michalopoulos GK. Liver regeneration: alternative epithelial pathways. Int J Biochem Cell Biol, 2011, 43(2): 173-179.
- 40. Forbes SJ, Newsome P N. Liver regeneration - mechanisms and models to clinical application. Nat Rev Gastroenterol Hepatol, 2016, 13(8): 473-485.
- 41. Kauffmann R, Fong Y. Post-hepatectomy liver failure. Hepatobiliary Surg Nutr, 2014, 3(5): 238-246.
- 42. Balzan S, Belghiti J, Farges O,et al. The "50-50 criteria" on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg, 2005, 242(6): 824-828, 829.
- 43. Rahbari NN, Garden OJ, Padbury R,et al. Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery, 2011, 149(5): 713-724.
- 44. Schindl MJ, Redhead DN, Fearon KC,et al. The value of residual liver volume as a predictor of hepatic dysfunction and infection after major liver resection. Gut, 2005, 54(2): 289-296.
- 45. Kinoshita H, Sakai K, Hirohashi K,et al. Preoperative portal vein embolization for hepatocellular carcinoma. World J Surg, 1986, 10(5): 803-808.
- 46. Yokoyama Y, Nagino M, Nimura Y. Mechanisms of hepatic regeneration following portal vein embolization and partial hepatectomy: a review. World J Surg, 2007, 31(2): 367-374.
- 47. Madoff DC, Abdalla EK, Vauthey JN. Portal vein embolization in preparation for major hepatic resection: evolution of a new standard of care. J Vasc Interv Radiol, 2005, 16(6): 779-790.
- 48. Ogata S, Belghiti J, Farges O,et al. Sequential arterial and portal vein embolizations before right hepatectomy in patients with cirrhosis and hepatocellular carcinoma. Br J Surg, 2006, 93(9): 1091-1098.
- 49. Ghobrial RM, Freise CE, Trotter JF,et al. Donor morbidity after living donation for liver transplantation. Gastroenterology, 2008, 135(2): 468-476.
- 50. Soejima Y, Taketomi A, Yoshizumi T,et al. Feasibility of left lobe living donor liver transplantation between adults: an 8-year, single-center experience of 107 cases. Am J Transplant, 2006, 6(5 Pt 1): 1004-1011.
- 51. Soejima Y, Shimada M, Suehiro T,et al. Outcome analysis in adult-to-adult living donor liver transplantation using the left lobe. Liver Transpl, 2003, 9(6): 581-586.
- 52. Ikegami T, Shimada M, Imura S,et al. Current concept of small-for-size grafts in living donor liver transplantation. Surg Today, 2008, 38(11): 971-982.
- 53. Schnitzbauer AA, Lang SA, Goessmann H,et al. Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling 2-staged extended right hepatic resection in small-for-size settings. Ann Surg, 2012, 255(3): 405-414.
- 54. Knoefel WT, Gabor I, Rehders A,et al. In situ liver transection with portal vein ligation for rapid growth of the future liver remnant in two-stage liver resection. Br J Surg, 2013, 100(3): 388-394.
- 55. Zhang GQ, Zhang ZW, Lau WY,et al. Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): a new strategy to increase resectability in liver surgery. Int J Surg, 2014, 12(5): 437-441.
- 56. Takahashi K, Tanabe K, Ohnuki M,et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 2007, 131(5): 861-872.
- 57. Kuijk E W, Rasmussen S, Blokzijl F,et al. Generation and characterization of rat liver stem cell lines and their engraftment in a rat model of liver failure. Sci Rep, 2016, 6: 22154.
- 58. Kakinuma S, Nakauchi H, Watanabe M. Hepatic stem/progenitor cells and stem-cell transplantation for the treatment of liver disease. J Gastroenterol, 2009, 44(3): 167-172.
- 59. Cordeiro-Spinetti E, de Mello W, Trindade LS,et al. Human bone marrow mesenchymal progenitors: perspectives on an optimizedin vitro manipulation. Front Cell Dev Biol, 2014, 2: 7.
- 60. Langer R, Vacanti JP. Tissue engineering. Science, 1993, 260(5110): 920-926.
- 61. Hoshiba T, Lu H, Kawazoe N,et al. Decellularized matrices for tissue engineering. Expert Opin Biol Ther, 2010, 10(12): 1717-1728.
- 62. Ott HC, Clippinger B, Conrad C,et al. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med, 2010, 16(8): 927-933.
- 63. Uygun BE, Soto-Gutierrez A, Yagi H,et al. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med, 2010, 16(7): 814-820.