Serotonin reverts age-related capillarization and failure of regeneration in the liver through a VEGF-dependent pathway

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 7, 2011, Pages 2945-2950

  Furrer, Katarzyna ^a   Rickenbacher, Andreas ^a   Tian, Yinghua ^a   Jochum, Wolfram ^b   Bittermann, Anne Greet ^a   Käch, Andres ^a   Humar, Bostjan ^a   Graf, Rolf ^a   Moritz, Wolfgang ^a   Clavien, Pierre Alain ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b Institute of Pathology   (Switzerland)

Author keywords

Aging liver; Fenestrations; Sinusoidal microperfusion

Indexed keywords

4 IODO 2,5 DIMETHOXYAMPHETAMINE; SEROTONIN; SEROTONIN RECEPTOR; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; CAPILLARY; CELL ADHESION; CELL PROLIFERATION; ENDOTHELIUM; FENESTRATION; LIVER CELL; LIVER REGENERATION; LIVER SINUSOID; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN SECRETION; SURVIVAL RATE; THROMBOCYTE; UPREGULATION;

AGE FACTORS; AMPHETAMINES; ANIMALS; CELL PROLIFERATION; HEPATECTOMY; HEPATOCYTES; IMMUNOHISTOCHEMISTRY; LIVER; LIVER REGENERATION; MALE; MICE; MICE, INBRED C57BL; MICROCIRCULATION; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; POLYMERASE CHAIN REACTION; REGIONAL BLOOD FLOW; SEROTONIN RECEPTOR AGONISTS; STATISTICS, NONPARAMETRIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA;

EID: 79952578316     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1012531108     Document Type: Article

References (53)

1. Michalopoulos GK, DeFrances MC (1997) Liver regeneration. Science 276:60-66.
2. Clavien PA, et al. (2010) What is critical for liver surgery and partial liver transplantation: Size or quality? Hepatology 52:715-729.
3. Lesurtel M, et al. (2006) Platelet-derived serotonin mediates liver regeneration. Science 312:104-107.
4. Schmucker DL (2005) Age-related changes in liver structure and function: Implications for disease? Exp Gerontol 40:650-659.
5. Fausto N, Campbell JS, Riehle KJ (2006) Liver regeneration. Hepatology 43 (2 Suppl 1): S45-S53.
6. Timchenko NA (2009) Aging and liver regeneration. Trends Endocrinol Metab 20: 171-176.
7. Mackey S, Singh P, Darlington GJ (2003) Making the liver young again. Hepatology 38: 1349-1352. (Pubitemid 37466957)
8. Tian Y, et al. (2006) Kupffer cell-dependent TNF-alpha signaling mediates injury in the arterialized small-for-size liver transplantation in the mouse. Proc Natl Acad Sci USA 103:4598-4603.
9. Taub R (1996) Liver regeneration in health and disease. Clin Lab Med 16:341-360.
10. Kaita KD, Pettigrew N, Minuk GY (1997) Hepatic regeneration in humans with various liver disease as assessed by Ki-67 staining of formalin-fixed paraffin-embedded liver tissue. Liver 17:13-16. (Pubitemid 27092776)
11. Clavien PA, Petrowsky H, DeOliveira ML, Graf R (2007) Strategies for safer liver surgery and partial liver transplantation. N Engl J Med 356:1545-1559. (Pubitemid 46588419)
12. Jin J, Wang GL, Shi X, Darlington GJ, Timchenko NA (2009) The age-associated decline of glycogen synthase kinase 3beta plays a critical role in the inhibition of liver regeneration. Mol Cell Biol 29:3867-3880.
13. Guerrieri F, Capozza G, Kalous M, Papa S (1992) Age-related changes of mitochondrial F0F1 ATP synthase. Ann N Y Acad Sci 671:395-402. (Pubitemid 23087669)
14. Selzner M, Selzner N, Jochum W, Graf R, Clavien PA (2007) Increased ischemic injury in old mouse liver: An ATP-dependent mechanism. Liver Transpl 13:382-390. (Pubitemid 46444467)
15. Woodhouse KW, Wynne HA (1988) Age-related changes in liver size and hepatic blood flow. The influence on drug metabolism in the elderly. Clin Pharmacokinet 15:287-294.
16. Le Couteur DG, et al. (2001) Pseudocapillarization and associated energy limitation in the aged rat liver. Hepatology 33:537-543. (Pubitemid 32185214)
17. Woodhouse K, Wynne HA (1992) Age-related changes in hepatic function. Implications for drug therapy. Drugs Aging 2:243-255.
18. Woodhouse K (1992) Drugs and the liver. Part III: Ageing of the liver and the metabolism of drugs. Biopharm Drug Dispos 13:311-320.
19. McLean AJ, Le Couteur DG (2004) Aging biology and geriatric clinical pharmacology. Pharmacol Rev 56:163-184. (Pubitemid 38720828)
20. Clavien PA, et al. (2003) A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg 238:843-850.
21. Petrowsky H, et al. (2006) A prospective, randomized, controlled trial comparing intermittent portal triad clamping versus ischemic preconditioning with continuous clamping for major liver resection. Ann Surg 244:921-928. (Pubitemid 44808626)
22. Krupczak-Hollis K, Wang X, Dennewitz MB, Costa RH (2003) Growth hormone stimulates proliferation of old-aged regenerating liver through forkhead box m1b. Hepatology 38:1552-1562. (Pubitemid 37466981)
23. Ikegami T, et al. (2000) The impact of donor age on living donor liver transplantation. Transplantation 70:1703-1707. (Pubitemid 32064823)
24. Hilmer SN, et al. (2005) Age-related changes in the hepatic sinusoidal endothelium impede lipoprotein transfer in the rat. Hepatology 42:1349-1354. (Pubitemid 43260037)
25. Le Couteur DG, Fraser R, Cogger VC, McLean AJ (2002) Hepatic pseudocapillarisation and atherosclerosis in ageing. Lancet 359:1612-1615. (Pubitemid 34621132)
26. Le Couteur DG, et al. (2007) Age-related changes in the liver sinusoidal endothelium: A mechanism for dyslipidemia. Ann N Y Acad Sci 1114:79-87. (Pubitemid 350070372)
27. Jansen PL (2002) Liver disease in the elderly. Best Pract Res Clin Gastroenterol 16:149-158.
28. Dobbs BR, Rogers GW, Xing HY, Fraser R (1994) Endotoxin-induced defenestration of the hepatic sinusoidal endothelium: A factor in the pathogenesis of cirrhosis? Liver 14:230-233.
29. Mori T, et al. (1993) Defenestration of the sinusoidal endothelial cell in a rat model of cirrhosis. Hepatology 17:891-897. (Pubitemid 23150099)
30. Tian Y, et al. (2011) Activation of serotonin receptor-2B rescues small-for-size liver graft failure in mice. Hepatology 53:253-262.
31. Soll C, et al. (2010) Serotonin promotes tumor growth in human hepatocellular cancer. Hepatology 51:1244-1254.
32. Nocito A, et al. (2008) Serotonin regulates macrophage-mediated angiogenesis in a mouse model of colon cancer allografts. Cancer Res 68:5152-5158.
33. Jackson LN, et al. (2009) Development and characterization of a novel in vivo model of carcinoid syndrome. Clin Cancer Res 15:2747-2755.
34. Ho-Tin-Noé B, Goerge T, Cifuni SM, Duerschmied D, Wagner DD (2008) Platelet granule secretion continuously prevents intratumor hemorrhage. Cancer Res 68:6851-6858.
35. Nocito A, et al. (2007) Serotonin mediates oxidative stress and mitochondrial toxicity in a murine model of nonalcoholic steatohepatitis. Gastroenterology 133:608-618. (Pubitemid 47187345)
36. García JJ, et al. (2001) N-acetylserotonin suppresses hepatic microsomal membrane rigidity associated with lipid peroxidation. Eur J Pharmacol 428:169-175. (Pubitemid 33000138)
37. Ito Y, et al. (2007) Age-related changes in the hepatic microcirculation in mice. Exp Gerontol 42:789-797. (Pubitemid 47058865)
38. Wisse E, De Zanger RB, Charels K, Van Der Smissen P, McCuskey RS (1985) The liver sieve: Considerations concerning the structure and function of endothelial fenestrae, the sinusoidal wall and the space of Disse. Hepatology 5:683-692. (Pubitemid 15029744)
39. McLean AJ, et al. (2003) Age-related pseudocapillarization of the human liver. J Pathol 200:112-117. (Pubitemid 36592644)
40. Fraser R, Dobbs BR, Rogers GW (1995) Lipoproteins and the liver sieve: The role of the fenestrated sinusoidal endothelium in lipoprotein metabolism, atherosclerosis, and cirrhosis. Hepatology 21:863-874.
41. Schaffner F, Poper H (1963) Capillarization of hepatic sinusoids in man. Gastroenterology 44:239-242.
42. Cogger VC, et al. (2003) Hepatic sinusoidal pseudocapillarization with aging in the non-human primate. Exp Gerontol 38:1101-1107. (Pubitemid 37324421)
43. Zeeh J, Platt D (2002) The aging liver: Structural and functional changes and their consequences for drug treatment in old age. Gerontology 48:121-127. (Pubitemid 34310065)
44. Funyu J, Mochida S, Inao M, Matsui A, Fujiwara K (2001) VEGF can act as vascular permeability factor in the hepatic sinusoids through upregulation of porosity of endothelial cells. Biochem Biophys Res Commun 280:481-485. (Pubitemid 32912816)
45. Heffelfinger SC, Hawkins HH, Barrish J, Taylor L, Darlington GJ (1992) SK HEP-1: A human cell line of endothelial origin. In Vitro Cell Dev Biol 28A:136-142.
46. Iakova P, Awad SS, Timchenko NA (2003) Aging reduces proliferative capacities of liver by switching pathways of C/EBPalpha growth arrest. Cell 113:495-506. (Pubitemid 36588752)
47. Wang GL, et al. (2007) Growth hormone corrects proliferation and transcription of phosphoenolpyruvate carboxykinase in livers of old mice via elimination of CCAAT/enhancer-binding protein alpha-Brm complex. J Biol Chem 282:1468-1478.
48. Corsonello A, Pedone C, Incalzi RA (2010) Age-related pharmacokinetic and pharmacodynamic changes and related risk of adverse drug reactions. Curr Med Chem 17:571-584.
49. Xu J, et al. (2007) Characterization of a putative intrarenal serotonergic system. Am J Physiol Renal Physiol 293:F1468-F1475. (Pubitemid 350085982)
50. Yamaji M, et al. (2010) VEGF-A loss in the haematopoietic and endothelial lineages exacerbates age-induced renal changes. Microvasc Res 80:372-383.
51. Selzner N, et al. (2003) ICAM-1 triggers liver regeneration through leukocyte recruitment and Kupffer cell-dependent release of TNF-alpha/IL-6 in mice. Gastroenterology 124:692-700. (Pubitemid 36268488)
52. Higgins GM, Anderson RM (1931) Experimental pathology of the liver. I. Restoration of the liver of the white rat following partial surgical removal. Arch Pathol (Chic) 12:186-202.
53. Furrer K, et al. (2008) Selective portal vein embolization and ligation trigger different regenerative responses in the rat liver. Hepatology 47:1615-1623. (Pubitemid 351702744)