The role of the autonomic nervous system in liver_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

WANG Zongding ¹ ,  WEN Hao ^1,2

1. Department of Hepatobiliary and Hydatid Disease, The First Affiliated Hospital of Xinjiang Medical University, Urumqi 830054, P. R. China;
2. State Key Laboratory of Pathogenesis, Prevention and Management of High Incidence Diseases in Central Asia, The First Affiliated Hospital of Xinjiang Medical University, Urumqi 830054, P. R. China;

Corresponding author：

WEN Hao, Email: dr.wenhao.@163.com

Keywords：

sympathetic nerve; vagus nerve; autonomic nerve; hepatic function

DOI：

10.7507/1007-9424.202008016

Video：

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Objective To investigate the anatomic distribution of hepatic nerves in liver and summarize the physiological and pathological functions of autonomic nervous system in liver.Method The literatures of studies related to human and animal liver neuroanatomy and function in recent years were reviewed, and the physiological and pathological functions involved in liver were summarized according to sympathetic nerve and vagus nerve, respectively.Result Hepatic nerves were mainly involved in regulating glucose and lipid metabolism, immune response, inflammation, hemodynamics, alcoholic liver disease, tumor metastasis, and liver regeneration after injury.Conclusion The mechanism of nerve regulation in liver is complex, and understanding these mechanisms provides a general new idea for the future treatment strategies for liver diseases.

Citation： WANG Zongding, WEN Hao. The role of the autonomic nervous system in liver. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(4): 537-543. doi: 10.7507/1007-9424.202008016 Copy

1.	McCuskey RS. Anatomy of efferent hepatic nerves. Anat Rec A Discov Mol Cell Evol Biol, 2004, 280(1): 821-826.
2.	Rogers RC, Hermann GE. Central connections of the hepatic branch of the vagus nerve: a horseradish peroxidase histochemical study. J Auton Nerv Syst, 1983, 7(2): 165-174.
3.	Norgren R, Smith GP. Central distribution of subdiaphragmatic vagal branches in the rat. J Comp Neurol, 1988, 273(2): 207-223.
4.	Zhang X, Renehan WE, Fogel R. Vagal innervation of the rat duodenum. J Auton Nerv Syst, 2000, 79(1): 8-18.
5.	Berthoud HR, Carlson NR, Powley TL. Topography of efferent vagal innervation of the rat gastrointestinal tract. Am J Physiol, 1991, 260(1 Pt 2): R200-R207.
6.	Berthoud HR, Kressel M, Neuhuber WL. An anterograde tracing study of the vagal innervation of rat liver, portal vein and biliary system. Anat Embryol (Berl), 1992, 186(5): 431-442.
7.	Barja F, Mathison R. Sensory innervation of the rat portal vein and the hepatic artery. J Auton Nerv Syst, 1984, 10(2): 117-125.
8.	Akiyoshi H, Gonda T, Terada T. A comparative histochemical and immunohistochemical study of aminergic, cholinergic and peptidergic innervation in rat, hamster, guinea pig, dog and human livers. Liver, 1998, 18(5): 352-359.
9.	Fukuda Y, Imoto M, Koyama Y, et al. Demonstration of noradrenaline-immunoreactive nerve fibres in the liver. J Int Med Res, 1996, 24(6): 466-472.
10.	Lee JA, Ahmed Q, Hines JE, et al. Disappearance of hepatic parenchymal nerves in human liver cirrhosis. Gut, 1992, 33(1): 87-91.
11.	Nobin A, Baumgarten HG, Falck B, et al. Organization of the sympathetic innervation in liver tissue from monkey and man. Cell Tissue Res, 1978, 195(3): 371-380.
12.	Berthoud HR, Kressel M, Neuhuber WL. Vagal afferent innervation of rat abdominal paraganglia as revealed by anterograde DiI-tracing and confocal microscopy. Acta Anat (Basel), 1995, 152(2): 127-132.
13.	Kandilis AN, Papadopoulou IP, Koskinas J, et al. Liver innervation and hepatic function: new insights. J Surg Res, 2015, 194(2): 511-519.
14.	Gardemann A, Püschel GP, Jungermann K. Nervous control of liver metabolism and hemodynamics. Eur J Biochem, 1992, 207(2): 399-411.
15.	Nogueiras R, López M, Diéguez C. Regulation of lipid metabolism by energy availability: a role for the central nervous system. Obes Rev, 2010, 11(3): 185-201.
16.	Yi CX, la Fleur SE, Fliers E, et al. The role of the autonomic nervous liver innervation in the control of energy metabolism. Biochim Biophys Acta, 2010, 1802(4): 416-431.
17.	Püschel GP. Control of hepatocyte metabolism by sympathetic and parasympathetic hepatic nerves. Anat Rec A Discov Mol Cell Evol Biol, 2004, 280(1): 854-867.
18.	Xue C, Aspelund G, Sritharan KC, et al. Isolated hepatic cholinergic denervation impairs glucose and glycogen metabolism. J Surg Res, 2000, 90(1): 19-25.
19.	Latour MG, Lautt WW. The hepatic vagus nerve in the control of insulin sensitivity in the rat. Auton Neurosci, 2002, 95(1-2): 125-130.
20.	Charpentier J, Waget A, Klopp P, et al. Lixisenatide requires a functional gut-vagus nerve-brain axis to trigger insulin secretion in controls and type 2 diabetic mice. Am J Physiol Gastrointest Liver Physiol, 2018, 315(5): 671-684.
21.	Lee KC, Miller RE. The hepatic vagus nerve and the neural regulation of insulin secretion. Endocrinology, 1985, 117(1): 307-314.
22.	Stümpel F, Kucera T, Bazotte R, et al. Loss of regulation by sympathetic hepatic nerves of liver metabolism and haemodynamics in chronically streptozotocin-diabetic rats. Diabetologia, 1996, 39(2): 161-165.
23.	Tanaka K, Inoue S, Nagase H, et al. Modulation of arginine-induced insulin and glucagon secretion by the hepatic vagus nerve in the rat: effects of celiac vagotomy and administration of atropine. Endocrinology, 1990, 127(4): 2017-2023.
24.	Klieverik LP, Janssen SF, van Riel A, et al. Thyroid hormone modulates glucose production via a sympathetic pathway from the hypothalamic paraventricular nucleus to the liver. Proc Natl Acad Sci U S A, 2009, 106(14): 5966-5971.
25.	Ando H, Gotoh K, Fujiwara K, et al. Glucagon-like peptide-1 reduces pancreatic β-cell mass through hypothalamic neural pathways in high-fat diet-induced obese rats. Sci Rep, 2017, 7(1): 5578.
26.	Liu J, Bisschop PH, Eggels L, et al. Intrahypothalamic estradiol regulates glucose metabolism via the sympathetic nervous system in female rats. Diabetes, 2013, 62(2): 435-443.
27.	Rojas JM, Bruinstroop E, Printz RL, et al. Central nervous system neuropeptide Y regulates mediators of hepatic phospholipid remodeling and very low-density lipoprotein triglyceride secretion via sympathetic innervation. Mol Metab, 2015, 4(3): 210-221.
28.	Bruinstroop E, Pei L, Ackermans MT, et al. Hypothalamic neuropeptide Y (NPY) controls hepatic VLDL-triglyceride secretion in rats via the sympathetic nervous system. Diabetes, 2012, 61(5): 1043-1050.
29.	Kimura I, Inoue D, Maeda T, et al. Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc Natl Acad Sci U S A, 2011, 108(19): 8030-8035.
30.	Xiao F, Guo Y, Deng J, et al. Hepatic c-Jun regulates glucose metabolism via FGF21 and modulates body temperature through the neural signals. Mol Metab, 2019, 20: 138-148.
31.	Kurosawa M, Unno T, Aikawa Y, et al. Neural regulation of hepatic blood flow in rats: an in vivo study. Neurosci Lett, 2002, 321(3): 145-148.
32.	Hsu CT, Schichijo K, Ito M, et al. The effect of chemical sympathectomy on acute liver injury induced by carbon tetrachloride in spontaneously hypertensive rats. J Auton Nerv Syst, 1993, 43(2): 91-96.
33.	Hsu CT. The role of the sympathetic nervous system in promoting liver cirrhosis induced by carbon tetrachloride, using the essential hypertensive animal (SHR). J Auton Nerv Syst, 1992, 37(3): 163-173.
34.	Wheatley AM, Stuart ET, Zhao D, et al. Effect of orthotopic transplantation and chemical denervation of the liver on hepatic hemodynamics in the rat. J Hepatol, 1993, 19(3): 442-450.
35.	van Westerloo DJ, Giebelen IA, Florquin S, et al. The cholinergic anti-inflammatory pathway regulates the host response during septic peritonitis. J Infect Dis, 2005, 191(12): 2138-2148.
36.	Li Y, Xu Z, Yu Y, et al. The vagus nerve attenuates fulminant hepatitis by activating the Src kinase in Kuppfer cells. Scand J Immunol, 2014, 79(2): 105-112.
37.	Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature, 2000, 405(6785): 458-462.
38.	Abdel-Salam OM, Abdel-Rahman RF, Sleem AA, et al. Effects of afferent and efferent denervation of vagal nerve on endotoxin-induced oxidative stress in rats. J Neural Transm (Vienna), 2013, 120(12): 1673-1688.
39.	Xia H, Liu Z, Liang W, et al. Vagus nerve stimulation alleviates hepatic ischemia and reperfusion injury by regulating glutathione production and transformation. Oxid Med Cell Longev, 2020, 2020: 1079129.
40.	Lin JC, Peng YJ, Wang SY, et al. Role of the sympathetic nervous system in carbon tetrachloride-induced hepatotoxicity and systemic inflammation. PLoS One, 2015, 10(3): e0121365.
41.	Zhu H, Guo YZ, Zhang J, et al. Donor denervation and elimination of Kupffer cells affect expression of P-selectin and ICAM-1 in liver graft. Hepatobiliary Pancreat Dis Int, 2007, 6(4): 379-382.
42.	Worlicek M, Knebel K, Linde HJ, et al. Splanchnic sympathectomy prevents translocation and spreading of E coli but not S aureus in liver cirrhosis. Gut, 2010, 59(8): 1127-1134.
43.	Huang J, Wang Y, Jiang D, et al. The sympathetic-vagal balance against endotoxemia. J Neural Transm (Vienna), 2010, 117(6): 729-735.
44.	Hoover DB. Cholinergic modulation of the immune system presents new approaches for treating inflammation. Pharmacol Ther, 2017, 179: 1-16.
45.	Henriksen JH, Møller S, Ring-Larsen H, et al. The sympathetic nervous system in liver disease. J Hepatol, 1998, 29(2): 328-341.
46.	Oben JA, Roskams T, Yang S, et al. Hepatic fibrogenesis requires sympathetic neurotransmitters. Gut, 2004, 53(3): 438-445.
47.	Hendrickse MT, Thuluvath PJ, Triger DR. Natural history of autonomic neuropathy in chronic liver disease. Lancet, 1992, 339(8807): 1462-1464.
48.	Willett I, Esler M, Burke F, et al. Total and renal sympathetic nervous system activity in alcoholic cirrhosis. J Hepatol, 1985, 1(6): 639-648.
49.	Henriksen JH, Ring-Larsen H, Kanstrup IL, et al. Splanchnic and renal elimination and release of catecholamines in cirrhosis. Evidence of enhanced sympathetic nervous activity in patients with decompensated cirrhosis. Gut, 1984, 25(10): 1034-1043.
50.	Hadengue A, Moreau R, Lee SS, et al. Liver hypermetabolism during alcohol withdrawal in humans. Role of sympathetic overactivity. Gastroenterology, 1988, 94(4): 1047-1052.
51.	Bockx I, Verdrengh K, Vander Elst I, et al. High-frequency vagus nerve stimulation improves portal hypertension in cirrhotic rats. Gut, 2012, 61(4): 604-612.
52.	Huan HB, Wen XD, Chen XJ, et al. Sympathetic nervous system promotes hepatocarcinogenesis by modulating inflammation through activation of alpha1-adrenergic receptors of Kupffer cells. Brain Behav Immun, 2017, 59: 118-134.
53.	Hiramoto T, Yoshihara K, Asano Y, et al. Protective role of the hepatic vagus nerve against liver metastasis in mice. Neuroimmunomodulation, 2017, 24(6): 341-347.
54.	Kamimura K, Inoue R, Nagoya T, et al. Autonomic nervous system network and liver regeneration. World J Gastroenterol, 2018, 24(15): 1616-1621.
55.	Wang L, Zhu L, Wu K, et al. Mitochondrial general control of amino acid synthesis 5 like 1 regulates glutaminolysis, mammalian target of rapamycin complex 1 activity, and murine liver regeneration. Hepatology, 2020, 71(2): 643-657.
56.	Kiba T. The role of the autonomic nervous system in liver regeneration and apoptosis—recent developments. Digestion, 2002, 66(2): 79-88.
57.	Kiba T, Tanaka K, Endo O, et al. Role of vagus nerve in increased DNA synthesis after hypothalamic ventromedial lesions in rat liver. Am J Physiol, 1992, 262(3 Pt 1): G483-G487.
58.	Cassiman D, Libbrecht L, Sinelli N, et al. The vagal nerve stimulates activation of the hepatic progenitor cell compartment via muscarinic acetylcholine receptor type 3. Am J Pathol, 2002, 161(2): 521-530.
59.	Ikeda O, Ozaki M, Murata S, et al. Autonomic regulation of liver regeneration after partial hepatectomy in mice. J Surg Res, 2009, 152(2): 218-223.
60.	Izumi T, Imai J, Yamamoto J, et al. Vagus-macrophage-hepatocyte link promotes post-injury liver regeneration and whole-body survival through hepatic FoxM1 activation. Nat Commun, 2018, 9(1): 5300.
61.	Inoue R, Kamimura K, Nagoya T, et al. Effect of a neural relay on liver regeneration in mice: activation of serotonin release from the gastrointestinal tract. FEBS Open Bio, 2018, 8(3): 449-460.
62.	Oben JA, Diehl AM. Sympathetic nervous system regulation of liver repair. Anat Rec A Discov Mol Cell Evol Biol, 2004, 280(1): 874-883.
63.	Oben JA, Roskams T, Yang S, et al. Sympathetic nervous system inhibition increases hepatic progenitors and reduces liver injury. Hepatology, 2003, 38(3): 664-673.
64.	Xia F, He Z, Li K, et al. Evaluation of the role of sympathetic denervation on hepatic function. Hepatol Res, 2006, 36(4): 259-264.
65.	Chida Y, Sudo N, Takaki A, et al. The hepatic sympathetic nerve plays a critical role in preventing Fas induced liver injury in mice. Gut, 2005, 54(7): 994-1002.
66.	Kandilis AN, Koskinas J, Vlachos I, et al. Liver regeneration: immunohistochemical study of intrinsic hepatic innervation after partial hepatectomy in rats. BMC Gastroenterol, 2014, 14: 202.
67.	Tanimizu N, Ichinohe N, Mitaka T. Intrahepatic bile ducts guide establishment of the intrahepatic nerve network in developing and regenerating mouse liver. Development, 2018, 145(9): dev159095.
68.	Shibata S. Neural regulation of the hepatic circadian rhythm. Anat Rec A Discov Mol Cell Evol Biol, 2004, 280(1): 901-909.
69.	Louis-Sylvestre J, Servant JM, Molimard R, et al. Effect of liver denervation on the feeding pattern of rats. Am J Physiol, 1980, 239(1): R66-R70.
70.	Hayes MR, Kanoski SE, De Jonghe BC, et al. The common hepatic branch of the vagus is not required to mediate the glycemic and food intake suppressive effects of glucagon-like-peptide-1. Am J Physiol Regul Integr Comp Physiol, 2011, 301(5): R1479-R1485.
71.	Niijima A. Effects of taste stimulation on the efferent activity of the autonomic nerves in the rat. Brain Res Bull, 1991, 26(1): 165-167.

1. McCuskey RS. Anatomy of efferent hepatic nerves. Anat Rec A Discov Mol Cell Evol Biol, 2004, 280(1): 821-826.
2. Rogers RC, Hermann GE. Central connections of the hepatic branch of the vagus nerve: a horseradish peroxidase histochemical study. J Auton Nerv Syst, 1983, 7(2): 165-174.
3. Norgren R, Smith GP. Central distribution of subdiaphragmatic vagal branches in the rat. J Comp Neurol, 1988, 273(2): 207-223.
4. Zhang X, Renehan WE, Fogel R. Vagal innervation of the rat duodenum. J Auton Nerv Syst, 2000, 79(1): 8-18.
5. Berthoud HR, Carlson NR, Powley TL. Topography of efferent vagal innervation of the rat gastrointestinal tract. Am J Physiol, 1991, 260(1 Pt 2): R200-R207.
6. Berthoud HR, Kressel M, Neuhuber WL. An anterograde tracing study of the vagal innervation of rat liver, portal vein and biliary system. Anat Embryol (Berl), 1992, 186(5): 431-442.
7. Barja F, Mathison R. Sensory innervation of the rat portal vein and the hepatic artery. J Auton Nerv Syst, 1984, 10(2): 117-125.
8. Akiyoshi H, Gonda T, Terada T. A comparative histochemical and immunohistochemical study of aminergic, cholinergic and peptidergic innervation in rat, hamster, guinea pig, dog and human livers. Liver, 1998, 18(5): 352-359.
9. Fukuda Y, Imoto M, Koyama Y, et al. Demonstration of noradrenaline-immunoreactive nerve fibres in the liver. J Int Med Res, 1996, 24(6): 466-472.
10. Lee JA, Ahmed Q, Hines JE, et al. Disappearance of hepatic parenchymal nerves in human liver cirrhosis. Gut, 1992, 33(1): 87-91.
11. Nobin A, Baumgarten HG, Falck B, et al. Organization of the sympathetic innervation in liver tissue from monkey and man. Cell Tissue Res, 1978, 195(3): 371-380.
12. Berthoud HR, Kressel M, Neuhuber WL. Vagal afferent innervation of rat abdominal paraganglia as revealed by anterograde DiI-tracing and confocal microscopy. Acta Anat (Basel), 1995, 152(2): 127-132.
13. Kandilis AN, Papadopoulou IP, Koskinas J, et al. Liver innervation and hepatic function: new insights. J Surg Res, 2015, 194(2): 511-519.
14. Gardemann A, Püschel GP, Jungermann K. Nervous control of liver metabolism and hemodynamics. Eur J Biochem, 1992, 207(2): 399-411.
15. Nogueiras R, López M, Diéguez C. Regulation of lipid metabolism by energy availability: a role for the central nervous system. Obes Rev, 2010, 11(3): 185-201.
16. Yi CX, la Fleur SE, Fliers E, et al. The role of the autonomic nervous liver innervation in the control of energy metabolism. Biochim Biophys Acta, 2010, 1802(4): 416-431.
17. Püschel GP. Control of hepatocyte metabolism by sympathetic and parasympathetic hepatic nerves. Anat Rec A Discov Mol Cell Evol Biol, 2004, 280(1): 854-867.
18. Xue C, Aspelund G, Sritharan KC, et al. Isolated hepatic cholinergic denervation impairs glucose and glycogen metabolism. J Surg Res, 2000, 90(1): 19-25.
19. Latour MG, Lautt WW. The hepatic vagus nerve in the control of insulin sensitivity in the rat. Auton Neurosci, 2002, 95(1-2): 125-130.
20. Charpentier J, Waget A, Klopp P, et al. Lixisenatide requires a functional gut-vagus nerve-brain axis to trigger insulin secretion in controls and type 2 diabetic mice. Am J Physiol Gastrointest Liver Physiol, 2018, 315(5): 671-684.
21. Lee KC, Miller RE. The hepatic vagus nerve and the neural regulation of insulin secretion. Endocrinology, 1985, 117(1): 307-314.
22. Stümpel F, Kucera T, Bazotte R, et al. Loss of regulation by sympathetic hepatic nerves of liver metabolism and haemodynamics in chronically streptozotocin-diabetic rats. Diabetologia, 1996, 39(2): 161-165.
23. Tanaka K, Inoue S, Nagase H, et al. Modulation of arginine-induced insulin and glucagon secretion by the hepatic vagus nerve in the rat: effects of celiac vagotomy and administration of atropine. Endocrinology, 1990, 127(4): 2017-2023.
24. Klieverik LP, Janssen SF, van Riel A, et al. Thyroid hormone modulates glucose production via a sympathetic pathway from the hypothalamic paraventricular nucleus to the liver. Proc Natl Acad Sci U S A, 2009, 106(14): 5966-5971.
25. Ando H, Gotoh K, Fujiwara K, et al. Glucagon-like peptide-1 reduces pancreatic β-cell mass through hypothalamic neural pathways in high-fat diet-induced obese rats. Sci Rep, 2017, 7(1): 5578.
26. Liu J, Bisschop PH, Eggels L, et al. Intrahypothalamic estradiol regulates glucose metabolism via the sympathetic nervous system in female rats. Diabetes, 2013, 62(2): 435-443.
27. Rojas JM, Bruinstroop E, Printz RL, et al. Central nervous system neuropeptide Y regulates mediators of hepatic phospholipid remodeling and very low-density lipoprotein triglyceride secretion via sympathetic innervation. Mol Metab, 2015, 4(3): 210-221.
28. Bruinstroop E, Pei L, Ackermans MT, et al. Hypothalamic neuropeptide Y (NPY) controls hepatic VLDL-triglyceride secretion in rats via the sympathetic nervous system. Diabetes, 2012, 61(5): 1043-1050.
29. Kimura I, Inoue D, Maeda T, et al. Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc Natl Acad Sci U S A, 2011, 108(19): 8030-8035.
30. Xiao F, Guo Y, Deng J, et al. Hepatic c-Jun regulates glucose metabolism via FGF21 and modulates body temperature through the neural signals. Mol Metab, 2019, 20: 138-148.
31. Kurosawa M, Unno T, Aikawa Y, et al. Neural regulation of hepatic blood flow in rats: an in vivo study. Neurosci Lett, 2002, 321(3): 145-148.
32. Hsu CT, Schichijo K, Ito M, et al. The effect of chemical sympathectomy on acute liver injury induced by carbon tetrachloride in spontaneously hypertensive rats. J Auton Nerv Syst, 1993, 43(2): 91-96.
33. Hsu CT. The role of the sympathetic nervous system in promoting liver cirrhosis induced by carbon tetrachloride, using the essential hypertensive animal (SHR). J Auton Nerv Syst, 1992, 37(3): 163-173.
34. Wheatley AM, Stuart ET, Zhao D, et al. Effect of orthotopic transplantation and chemical denervation of the liver on hepatic hemodynamics in the rat. J Hepatol, 1993, 19(3): 442-450.
35. van Westerloo DJ, Giebelen IA, Florquin S, et al. The cholinergic anti-inflammatory pathway regulates the host response during septic peritonitis. J Infect Dis, 2005, 191(12): 2138-2148.
36. Li Y, Xu Z, Yu Y, et al. The vagus nerve attenuates fulminant hepatitis by activating the Src kinase in Kuppfer cells. Scand J Immunol, 2014, 79(2): 105-112.
37. Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature, 2000, 405(6785): 458-462.
38. Abdel-Salam OM, Abdel-Rahman RF, Sleem AA, et al. Effects of afferent and efferent denervation of vagal nerve on endotoxin-induced oxidative stress in rats. J Neural Transm (Vienna), 2013, 120(12): 1673-1688.
39. Xia H, Liu Z, Liang W, et al. Vagus nerve stimulation alleviates hepatic ischemia and reperfusion injury by regulating glutathione production and transformation. Oxid Med Cell Longev, 2020, 2020: 1079129.
40. Lin JC, Peng YJ, Wang SY, et al. Role of the sympathetic nervous system in carbon tetrachloride-induced hepatotoxicity and systemic inflammation. PLoS One, 2015, 10(3): e0121365.
41. Zhu H, Guo YZ, Zhang J, et al. Donor denervation and elimination of Kupffer cells affect expression of P-selectin and ICAM-1 in liver graft. Hepatobiliary Pancreat Dis Int, 2007, 6(4): 379-382.
42. Worlicek M, Knebel K, Linde HJ, et al. Splanchnic sympathectomy prevents translocation and spreading of E coli but not S aureus in liver cirrhosis. Gut, 2010, 59(8): 1127-1134.
43. Huang J, Wang Y, Jiang D, et al. The sympathetic-vagal balance against endotoxemia. J Neural Transm (Vienna), 2010, 117(6): 729-735.
44. Hoover DB. Cholinergic modulation of the immune system presents new approaches for treating inflammation. Pharmacol Ther, 2017, 179: 1-16.
45. Henriksen JH, Møller S, Ring-Larsen H, et al. The sympathetic nervous system in liver disease. J Hepatol, 1998, 29(2): 328-341.
46. Oben JA, Roskams T, Yang S, et al. Hepatic fibrogenesis requires sympathetic neurotransmitters. Gut, 2004, 53(3): 438-445.
47. Hendrickse MT, Thuluvath PJ, Triger DR. Natural history of autonomic neuropathy in chronic liver disease. Lancet, 1992, 339(8807): 1462-1464.
48. Willett I, Esler M, Burke F, et al. Total and renal sympathetic nervous system activity in alcoholic cirrhosis. J Hepatol, 1985, 1(6): 639-648.
49. Henriksen JH, Ring-Larsen H, Kanstrup IL, et al. Splanchnic and renal elimination and release of catecholamines in cirrhosis. Evidence of enhanced sympathetic nervous activity in patients with decompensated cirrhosis. Gut, 1984, 25(10): 1034-1043.
50. Hadengue A, Moreau R, Lee SS, et al. Liver hypermetabolism during alcohol withdrawal in humans. Role of sympathetic overactivity. Gastroenterology, 1988, 94(4): 1047-1052.
51. Bockx I, Verdrengh K, Vander Elst I, et al. High-frequency vagus nerve stimulation improves portal hypertension in cirrhotic rats. Gut, 2012, 61(4): 604-612.
52. Huan HB, Wen XD, Chen XJ, et al. Sympathetic nervous system promotes hepatocarcinogenesis by modulating inflammation through activation of alpha1-adrenergic receptors of Kupffer cells. Brain Behav Immun, 2017, 59: 118-134.
53. Hiramoto T, Yoshihara K, Asano Y, et al. Protective role of the hepatic vagus nerve against liver metastasis in mice. Neuroimmunomodulation, 2017, 24(6): 341-347.
54. Kamimura K, Inoue R, Nagoya T, et al. Autonomic nervous system network and liver regeneration. World J Gastroenterol, 2018, 24(15): 1616-1621.
55. Wang L, Zhu L, Wu K, et al. Mitochondrial general control of amino acid synthesis 5 like 1 regulates glutaminolysis, mammalian target of rapamycin complex 1 activity, and murine liver regeneration. Hepatology, 2020, 71(2): 643-657.
56. Kiba T. The role of the autonomic nervous system in liver regeneration and apoptosis—recent developments. Digestion, 2002, 66(2): 79-88.
57. Kiba T, Tanaka K, Endo O, et al. Role of vagus nerve in increased DNA synthesis after hypothalamic ventromedial lesions in rat liver. Am J Physiol, 1992, 262(3 Pt 1): G483-G487.
58. Cassiman D, Libbrecht L, Sinelli N, et al. The vagal nerve stimulates activation of the hepatic progenitor cell compartment via muscarinic acetylcholine receptor type 3. Am J Pathol, 2002, 161(2): 521-530.
59. Ikeda O, Ozaki M, Murata S, et al. Autonomic regulation of liver regeneration after partial hepatectomy in mice. J Surg Res, 2009, 152(2): 218-223.
60. Izumi T, Imai J, Yamamoto J, et al. Vagus-macrophage-hepatocyte link promotes post-injury liver regeneration and whole-body survival through hepatic FoxM1 activation. Nat Commun, 2018, 9(1): 5300.
61. Inoue R, Kamimura K, Nagoya T, et al. Effect of a neural relay on liver regeneration in mice: activation of serotonin release from the gastrointestinal tract. FEBS Open Bio, 2018, 8(3): 449-460.
62. Oben JA, Diehl AM. Sympathetic nervous system regulation of liver repair. Anat Rec A Discov Mol Cell Evol Biol, 2004, 280(1): 874-883.
63. Oben JA, Roskams T, Yang S, et al. Sympathetic nervous system inhibition increases hepatic progenitors and reduces liver injury. Hepatology, 2003, 38(3): 664-673.
64. Xia F, He Z, Li K, et al. Evaluation of the role of sympathetic denervation on hepatic function. Hepatol Res, 2006, 36(4): 259-264.
65. Chida Y, Sudo N, Takaki A, et al. The hepatic sympathetic nerve plays a critical role in preventing Fas induced liver injury in mice. Gut, 2005, 54(7): 994-1002.
66. Kandilis AN, Koskinas J, Vlachos I, et al. Liver regeneration: immunohistochemical study of intrinsic hepatic innervation after partial hepatectomy in rats. BMC Gastroenterol, 2014, 14: 202.
67. Tanimizu N, Ichinohe N, Mitaka T. Intrahepatic bile ducts guide establishment of the intrahepatic nerve network in developing and regenerating mouse liver. Development, 2018, 145(9): dev159095.
68. Shibata S. Neural regulation of the hepatic circadian rhythm. Anat Rec A Discov Mol Cell Evol Biol, 2004, 280(1): 901-909.
69. Louis-Sylvestre J, Servant JM, Molimard R, et al. Effect of liver denervation on the feeding pattern of rats. Am J Physiol, 1980, 239(1): R66-R70.
70. Hayes MR, Kanoski SE, De Jonghe BC, et al. The common hepatic branch of the vagus is not required to mediate the glycemic and food intake suppressive effects of glucagon-like-peptide-1. Am J Physiol Regul Integr Comp Physiol, 2011, 301(5): R1479-R1485.
71. Niijima A. Effects of taste stimulation on the efferent activity of the autonomic nerves in the rat. Brain Res Bull, 1991, 26(1): 165-167.

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The role of the autonomic nervous system in liver

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