Mechanisms of adaptation of the hepatic vasculature to the deteriorating conditions of blood circulation in liver cirrhosis

World Journal of Hepatology

Volumn 8, Issue 16, 2016, Pages 665-672

  Garbuzenko, Dmitry Victorovich ^a   Arefyev, Nikolay Olegovich ^a   Belov, Dmitry Vladimirovich ^a  

^a SOUTH URAL STATE MEDICAL UNIVERSITY   (Russian Federation)

Author keywords

Endothelial dysfunction; Intrahepatic angiogenesis; Liver cirrhosis; Pathogenesis of portal hypertension; Sinusoidal remodeling

Indexed keywords

EID: 84973293883     PISSN: None     EISSN: 19485182     Source Type: Journal    
DOI: 10.4254/wjh.v8.i16.665     Document Type: Short Survey

References (55)

1. Fernandez M. Molecular pathophysiology of portal hypertension. Hepatology 2015; 61: 1406-1415 [PMID: 25092403 DOI: 10.1002/hep.27343]
2. García-Pagán JC, Gracia-Sancho J, Bosch J. Functional aspects on the pathophysiology of portal hypertension in cirrhosis. J Hepatol 2012; 57: 458-461 [PMID: 22504334 DOI: 10.1016/j.jhep.2012.03.007]
3. Hu LS, George J, Wang JH. Current concepts on the role of nitric oxide in portal hypertension. World J Gastroenterol 2013;19:1707-1717 [PMID: 23555159 DOI: 10.3748/wjg.v19.i11.1707]
4. Hellerbrand C. Hepatic stellate cells--the pericytes in the liver. Pflugers Arch 2013; 465: 775-778 [PMID: 23292551 DOI: 10.1007/s00424-012-1209-5]
5. Ueno T, Bioulac-Sage P, Balabaud C, Rosenbaum J. Innervation of the sinusoidal wall: regulation of the sinusoidal diameter. Anat Rec A Discov Mol Cell Evol Biol 2004; 280: 868-873 [PMID: 15382014]
6. Iizuka M, Murata T, Hori M, Ozaki H. Increased contractility of hepatic stellate cells in cirrhosis is mediated by enhanced Ca2+-dependent and Ca2+-sensitization pathways. Am J Physiol Gastrointest Liver Physiol 2011; 300: G1010-G1021 [PMID: 21393429 DOI: 10.1152/ajpgi.00350.2010]
7. Takashimizu S, Kojima S, Nishizaki Y, Kagawa T, Shiraishi K, Mine T, Watanabe N. Effect of endothelin A receptor antagonist on hepatic hemodynamics in cirrhotic rats. Implications for endothelin-1 in portal hypertension. Tokai J Exp Clin Med 2011; 36: 37-43 [PMID: 21769771]
8. Lugo-Baruqui A, Muñoz-Valle JF, Arévalo-Gallegos S, Armendáriz-Borunda J. Role of angiotensin II in liver fibrosis-induced portal hypertension and therapeutic implications. Hepatol Res 2010; 40: 95-104 [PMID: 19737316 DOI: 10.1111/j.1872-034X.2009.00581. x]
9. Reynaert H, Urbain D, Geerts A. Regulation of sinusoidal perfusion in portal hypertension. Anat Rec (Hoboken) 2008;291:693-698 [PMID: 18484616 DOI: 10.1002/ar.20669]
10. Lee JS, Semela D, Iredale J, Shah VH. Sinusoidal remodeling and angiogenesis: a new function for the liver-specific pericyte? Hepatology 2007; 45: 817-825 [PMID: 17326208]
11. Lee JS, Kang Decker N, Chatterjee S, Yao J, Friedman S, Shah V. Mechanisms of nitric oxide interplay with Rho GTPase family members in modulation of actin membrane dynamics in pericytes and fibroblasts. Am J Pathol 2005; 166: 1861-1870 [PMID: 15920170]
12. Semela D, Das A, Langer D, Kang N, Leof E, Shah V. Plateletderived growth factor signaling through ephrin-b2 regulates hepatic vascular structure and function. Gastroenterology 2008;135:671-679 [PMID: 18570897 DOI: 10.1053/j.gastro.2008.04.010]
13. Pinzani M. PDGF and signal transduction in hepatic stellate cells. Front Biosci 2002; 7: d1720-d1726 [PMID: 12133817]
14. Cao S, Yaqoob U, Das A, Shergill U, Jagavelu K, Huebert RC, Routray C, Abdelmoneim S, Vasdev M, Leof E, Charlton M, Watts RJ, Mukhopadhyay D, Shah VH. Neuropilin-1 promotes cirrhosis of the rodent and human liver by enhancing PDGF/TGFbeta signaling in hepatic stellate cells. J Clin Invest 2010;120:2379-2394 [PMID: 20577048 DOI: 10.1172/JCI41203]
15. Friedman SL. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev 2008; 88: 125-172 [PMID: 18195085 DOI: 10.1152/physrev.00013.2007]
16. Seki E, Brenner DA. Recent advancement of molecular mechanisms of liver fibrosis. J Hepatobiliary Pancreat Sci 2015;22:512-518 [PMID: 25869468 DOI: 10.1002/jhbp.245]
17. Svegliati-Baroni G, De Minicis S, Marzioni M. Hepatic fibrogenesis in response to chronic liver injury: novel insights on the role of cell-to-cell interaction and transition. Liver Int 2008;28:1052-1064 [PMID: 18783548 DOI: 10.1111/j.1478-3231.2008.01825.x]
18. Rappaport AM, MacPhee PJ, Fisher MM, Phillips MJ. The scarring of the liver acini (Cirrhosis). Tridimensional and microcirculatory considerations. Virchows Arch A Pathol Anat Histopathol 1983; 402: 107-137 [PMID: 6420982]
19. Elpek GÖ. Angiogenesis and liver fibrosis. World J Hepatol 2015; 7: 377-391 [PMID: 25848465 DOI: 10.4254/wjh.v7.i3.377]
20. Folkman J. Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 2007; 6: 273-286 [PMID: 17396134]
21. Skuli N, Majmundar AJ, Krock BL, Mesquita RC, Mathew LK, Quinn ZL, Runge A, Liu L, Kim MN, Liang J, Schenkel S, Yodh AG, Keith B, Simon MC. Endothelial HIF-2α regulates murine pathological angiogenesis and revascularization processes. J Clin Invest 2012; 122: 1427-1443 [PMID: 22426208 DOI: 10.1172/JCI57322]
22. Brandes RP, Miller FJ, Beer S, Haendeler J, Hoffmann J, Ha T, Holland SM, Görlach A, Busse R. The vascular NADPH oxidase subunit p47phox is involved in redox-mediated gene expression. Free Radic Biol Med 2002; 32: 1116-1122 [PMID: 12031896]
23. Chen Z, Lai TC, Jan YH, Lin FM, Wang WC, Xiao H, Wang YT, Sun W, Cui X, Li YS, Fang T, Zhao H, Padmanabhan C, Sun R, Wang DL, Jin H, Chau GY, Huang HD, Hsiao M, Shyy JY. Hypoxia-responsive miRNAs target argonaute 1 to promote angiogenesis. J Clin Invest 2013; 123: 1057-1067 [PMID: 23426184 DOI: 10.1172/JCI65344]
24. Carmeliet P. Manipulating angiogenesis in medicine. J Intern Med 2004; 255: 538-561 [PMID: 15078497]
25. Klein S, Roghani M, Rifkin DB. Fibroblast growth factors as angiogenesis factors: new insights into their mechanism of action. EXS 1997; 79: 159-192 [PMID: 9002232]
26. Hellberg C, Ostman A, Heldin CH. PDGF and vessel maturation. Recent Results Cancer Res 2010; 180: 103-114 [PMID: 20033380 DOI: 10.1007/978-3-540-78281-0_7]
27. Chen JX, Zeng H, Lawrence ML, Blackwell TS, Meyrick B. Angiopoietin-1-induced angiogenesis is modulated by endothelial NADPH oxidase. Am J Physiol Heart Circ Physiol 2006; 291:H1563-H1572 [PMID: 16679392]
28. Pauta M, Ribera J, Melgar-Lesmes P, Casals G, Rodríguez-Vita J, Reichenbach V, Fernandez-Varo G, Morales-Romero B, Bataller R, Michelena J, Altamirano J, Jiménez W, Morales-Ruiz M. Overexpression of angiopoietin-2 in rats and patients with liver fibrosis. Therapeutic consequences of its inhibition. Liver Int 2015; 35: 1383-1392 [PMID: 24612347 DOI: 10.1111/liv.12505]
29. Patsenker E, Popov Y, Stickel F, Schneider V, Ledermann M, Sägesser H, Niedobitek G, Goodman SL, Schuppan D. Pharmacological inhibition of integrin alphavbeta3 aggravates experimental liver fibrosis and suppresses hepatic angiogenesis. Hepatology 2009; 50: 1501-1511 [PMID: 19725105 DOI: 10.1002/hep.23144]
30. Kevil CG, Payne DK, Mire E, Alexander JS. Vascular permeability factor/vascular endothelial cell growth factor-mediated permeability occurs through disorganization of endothelial junctional proteins. J Biol Chem 1998; 273: 15099-15103 [PMID: 9614120]
31. Elpek GO, Gokhan GA, Bozova S. Thrombospondin-1 expression correlates with angiogenesis in experimental cirrhosis. World J Gastroenterol 2008; 14: 2213-2217 [PMID: 18407596]
32. Eriksson K, Magnusson P, Dixelius J, Claesson-Welsh L, Cross MJ. Angiostatin and endostatin inhibit endothelial cell migration in response to FGF and VEGF without interfering with specific intracellular signal transduction pathways. FEBS Lett 2003;536:19-24 [PMID: 12586331]
33. Jagavelu K, Routray C, Shergill U, O'Hara SP, Faubion W, Shah VH. Endothelial cell toll-like receptor 4 regulates fibrosisassociated angiogenesis in the liver. Hepatology 2010; 52: 590-601 [PMID: 20564354 DOI: 10.1002/hep.23739]
34. Melgar-Lesmes P, Pauta M, Reichenbach V, Casals G, Ros J, Bataller R, Morales-Ruiz M, Jiménez W. Hypoxia and proinflammatory factors upregulate apelin receptor expression in human stellate cells and hepatocytes. Gut 2011; 60: 1404-1411 [PMID: 21450694 DOI: 10.1136/gut.2010.234690]
35. Huebert RC, Jagavelu K, Hendrickson HI, Vasdev MM, Arab JP, Splinter PL, Trussoni CE, Larusso NF, Shah VH. Aquaporin-1 promotes angiogenesis, fibrosis, and portal hypertension through mechanisms dependent on osmotically sensitive microRNAs. Am J Pathol 2011; 179: 1851-1860 [PMID: 21854740 DOI: 10.1016/j.ajpath.2011.06.045]
36. Sahin H, Borkham-Kamphorst E, Kuppe C, Zaldivar MM, Grouls C, Al-samman M, Nellen A, Schmitz P, Heinrichs D, Berres ML, Doleschel D, Scholten D, Weiskirchen R, Moeller MJ, Kiessling F, Trautwein C, Wasmuth HE. Chemokine Cxcl9 attenuates liver fibrosis-associated angiogenesis in mice. Hepatology 2012;55:1610-1619 [PMID: 22237831 DOI: 10.1002/hep.25545]
37. Staton CA, Kumar I, Reed MW, Brown NJ. Neuropilins in physiological and pathological angiogenesis. J Pathol 2007;212:237-248 [PMID: 17503412]
38. Fernández M, Semela D, Bruix J, Colle I, Pinzani M, Bosch J. Angiogenesis in liver disease. J Hepatol 2009; 50: 604-620 [PMID: 19157625 DOI: 10.1016/j.jhep.2008.12.011]
39. Ehling J, Bartneck M, Wei X, Gremse F, Fech V, Möckel D, Baeck C, Hittatiya K, Eulberg D, Luedde T, Kiessling F, Trautwein C, Lammers T, Tacke F. CCL2-dependent infiltrating macrophages promote angiogenesis in progressive liver fibrosis. Gut 2014;63:1960-1971 [PMID: 24561613 DOI: 10.1136/gutjnl-2013-306294]
40. Chaparro M, Sanz-Cameno P, Trapero-Marugan M, Garcia-Buey L, Moreno-Otero R. Mechanisms of angiogenesis in chronic inflammatory liver disease. Ann Hepatol 2007; 6: 208-213 [PMID: 18007549]
41. Steib CJ. Kupffer cell activation and portal hypertension. Gut 2011; 60: 1307-1308 [PMID: 21708827 DOI: 10.1136/gut.2011.242560]
42. Lochhead PA, Gilley R, Cook SJ. ERK5 and its role in tumour development. Biochem Soc Trans 2012; 40: 251-256 [PMID: 22260700 DOI: 10.1042/BST20110663]
43. Dewhirst MW, Cao Y, Moeller B. Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat Rev Cancer 2008; 8: 425-437 [PMID: 18500244 DOI: 10.1038/nrc2397]
44. Ko HM, Seo KH, Han SJ, Ahn KY, Choi IH, Koh GY, Lee HK, Ra MS, Im SY. Nuclear factor kappaB dependency of plateletactivating factor-induced angiogenesis. Cancer Res 2002;62:1809-1814 [PMID: 11912159]
45. Franceschini B, Ceva-Grimaldi G, Russo C, Dioguardi N, Grizzi F. The complex functions of mast cells in chronic human liver diseases. Dig Dis Sci 2006; 51: 2248-2256 [PMID: 17103041]
46. Marra F. Chemokines in liver inflammation and fibrosis. Front Biosci 2002; 7: d1899-d1914 [PMID: 12161342]
47. Copple BL, Bai S, Burgoon LD, Moon JO. Hypoxia-inducible factor-1α regulates the expression of genes in hypoxic hepatic stellate cells important for collagen deposition and angiogenesis. Liver Int 2011; 31: 230-244 [PMID: 20880076 DOI: 10.1111/j.1478-3231.2010.02347.x]
48. Lemoinne S, Cadoret A, El Mourabit H, Thabut D, Housset C. Origins and functions of liver myofibroblasts. Biochim Biophys Acta 2013; 1832: 948-954 [PMID: 23470555 DOI: 10.1016/j. bbadis.2013.02.019]
49. Yokomori H, Oda M, Yoshimura K, Hibi T. Enhanced expressions of apelin on proliferative hepatic arterial capillaries in human cirrhotic liver. Hepatol Res 2012; 42: 508-514 [PMID: 22502744 DOI: 10.1111/j.1872-034X.2011.00945.x]
50. Coulon S, Heindryckx F, Geerts A, Van Steenkiste C, Colle I, Van Vlierberghe H. Angiogenesis in chronic liver disease and its complications. Liver Int 2011; 31: 146-162 [PMID: 21073649 DOI: 10.1111/j.1478-3231.2010.02369.x]
51. Novo E, Povero D, Busletta C, Paternostro C, di Bonzo LV, Cannito S, Compagnone A, Bandino A, Marra F, Colombatto S, David E, Pinzani M, Parola M. The biphasic nature of hypoxiainduced directional migration of activated human hepatic stellate cells. J Pathol 2012; 226: 588-597 [PMID: 21959987 DOI: 10.1002/path.3005]
52. Novo E, Cannito S, Zamara E, Valfrè di Bonzo L, Caligiuri A, Cravanzola C, Compagnone A, Colombatto S, Marra F, Pinzani M, Parola M. Proangiogenic cytokines as hypoxia-dependent factors stimulating migration of human hepatic stellate cells. Am J Pathol 2007; 170: 1942-1953 [PMID: 17525262]
53. Vanheule E, Geerts AM, Van Huysse J, Schelfhout D, Praet M, Van Vlierberghe H, De Vos M, Colle I. An intravital microscopic study of the hepatic microcirculation in cirrhotic mice models:relationship between fibrosis and angiogenesis. Int J Exp Pathol 2008; 89: 419-432 [PMID: 19134051 DOI: 10.1111/j.1365-2613.2008.00608.x]
54. Kaur S, Tripathi D, Dongre K, Garg V, Rooge S, Mukopadhyay A, Sakhuja P, Sarin SK. Increased number and function of endothelial progenitor cells stimulate angiogenesis by resident liver sinusoidal endothelial cells (SECs) in cirrhosis through paracrine factors. J Hepatol 2012; 57: 1193-1198 [PMID: 22824816 DOI: 10.1016/j.jhep.2012.07.016]
55. Chen CH, Chang LT, Tung WC, Chen YL, Chang CL, Leu S, Sun CK, Tsai TH, Tsai IT, Chang HW, Yip HK. Levels and values factors, and mononuclear cell apoptosis in liver cirrhosis patients. J Biomed Sci 2012; 19: 66 [PMID: 22809449 DOI: 10.1186/1423-0127-19-66]