The CD47-binding peptide of thrombospondin-1 induces defenestration of liver sinusoidal endothelial cells

Liver International

Volumn 33, Issue 9, 2013, Pages 1386-1397

  Venkatraman, Lakshmi ^a   Tucker Kellogg, Lisa ^a,b,c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b STONY BROOK UNIVERSITY   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Capillarization; Discontinuous endothelium; Mechanical signal transduction; Myosin light chain

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; IMMUNOGLOBULIN; MYOSIN; RHO KINASE; SIMVASTATIN; THROMBOSPONDIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; IN VITRO STUDY; LIVER FIBROSIS; LIVER SINUSOID; MALE; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION;

CAPILLARIZATION; DISCONTINUOUS ENDOTHELIUM; MECHANICAL SIGNAL TRANSDUCTION; MYOSIN LIGHT CHAIN;

AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD47; ENDOTHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE PROCESSING, COMPUTER-ASSISTED; LIVER; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; MYOSINS; PHOSPHORYLATION; RATS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION;

EID: 84883801838     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/liv.12231     Document Type: Article

References (58)

1. Kyriakides TR, Maclauchlan S. The role of thrombospondins in wound healing, ischemia, and the foreign body reaction. J cell commun signal 2009; 3: 215-25.
2. Maile LA, Allen LB, Hanzaker CF, et al. Glucose regulation of thrombospondin and its role in the modulation of smooth muscle cell proliferation. Exp Diabetes Res 2010; 2010, Article ID: 617052. doi:10.1155/2010/617052.
3. Myung SJ, Yoon JH, Gwak GY, et al. Bile acid-mediated thrombospondin-1 induction in hepatocytes leads to transforming growth factor-beta-dependent hepatic stellate cell activation. Biochem Biophys Res Commun 2007; 353: 1091-6.
4. Breitkopf K, Sawitza I, Westhoff JH, et al. Thrombospondin 1 acts as a strong promoter of transforming growth factor beta effects via two distinct mechanisms in hepatic stellate cells. Gut 2005; 54: 673-81.
5. Murphy-Ullrich JE, Poczatek M. Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev 2000; 11: 59-69.
6. Hayashi H, Sakai K, Baba H, Sakai T. Thrombospondin-1 is a novel negative regulator of liver regeneration after partial hepatectomy through transforming growth factor-beta1 activation in mice. Hepatology 2012; 55: 1562-73.
7. Bornstein P. Thrombospondins function as regulators of angiogenesis. J cell commun signal 2009; 3: 189-200.
8. Short SM, Derrien A, Narsimhan RP, et al. Inhibition of endothelial cell migration by thrombospondin-1 type-1 repeats is mediated by beta1 integrins. J Cell Biol 2005; 168: 643-53.
9. Kaur S, Roberts DD. CD47 applies the brakes to angiogenesis via vascular endothelial growth factor receptor-2. Cell Cycle 2011; 10: 10-2.
10. Isenberg JS, Annis DS, Pendrak ML, et al. Differential interactions of thrombospondin-1, -2, and -4 with CD47 and effects on cGMP signaling and ischemic injury responses. J Biol Chem 2009; 284: 1116-25.
11. Frazier WA, Gao AG, Dimitry J, et al. The thrombospondin receptor integrin-associated protein (CD47) functionally couples to heterotrimeric Gi. J Biol Chem 1999; 274: 8554-60.
12. Braet F, Wisse E. Structural and functional aspects of liver sinusoidal endothelial cell fenestrae: a review. Comp Hepatol 2002; 1: 1.
13. Schaffner F, Poper H. Capillarization of hepatic sinusoids in man. Gastroenterology 1963; 44: 239-42.
14. Xie G, Wang X, Wang L, et al. Role of Differentiation of Liver Sinusoidal Endothelial Cells in Progression and Regression of Hepatic Fibrosis in Rats. Gastroenterology 2012; 142: 918-27.
15. Deleve LD, Wang X, Guo Y. Sinusoidal endothelial cells prevent rat stellate cell activation and promote reversion to quiescence. Hepatology 2008; 48: 920-30.
16. Wang BY, Ju XH, Fu BY, Zhang J, Cao YX. Effects of ethanol on liver sinusoidal endothelial cells-fenestrae of rats. Hepatobiliary Pancreat Dis Int 2005; 4: 422-6.
17. McCuskey RS, Ito Y, Robertson GR, et al. Hepatic microvascular dysfunction during evolution of dietary steatohepatitis in mice. Hepatology 2004; 40: 386-93.
18. Fraser R, Cogger VC, Dobbs B, et al. The liver sieve and atherosclerosis. Pathology 2012; 44: 181-6.
19. Narmada BC, Kang Y, Venkatraman L, et al. HSC-targeted delivery of HGF transgene via bile duct infusion enhances its expression at fibrotic foci to regress DMN-induced liver fibrosis. Hum Gene Ther (2013); 24: 508-19.
20. ++-calmodulin-actomyosin system in the contractility of hepatic sinusoidal endothelial fenestrae. In: Knook DL, Wisse E, eds. Cells of the Hepatic Sinusoid 4. Leiden: Kupffer Cell Foundation, 1993; 174-8.
21. Yokomori H, Yoshimura K, Funakoshi S, et al. Rho modulates hepatic sinusoidal endothelial fenestrae via regulation of the actin cytoskeleton in rat endothelial cells. Lab Invest 2004; 84: 857-64.
22. Rombouts K, Kisanga E, Hellemans K, et al. Effect of HMG-CoA reductase inhibitors on proliferation and protein synthesis by rat hepatic stellate cells. J Hepatol 2003; 38: 564-72.
23. Braet F, De Zanger R, Sasaoki T, et al. Assessment of a method of isolation, purification, and cultivation of rat liver sinusoidal endothelial cells. Lab Invest 1994; 70: 944-52.
24. Fleming YM, Ferguson GJ, Spender LC, et al. TGF-beta-mediated activation of RhoA signalling is required for efficient (V12)HaRas and (V600E)BRAF transformation. Oncogene 2009; 28: 983-93.
25. Wakefield LM, Winokur TS, Hollands RS, et al. Recombinant latent transforming growth factor beta 1 has a longer plasma half-life in rats than active transforming growth factor beta 1, and a different tissue distribution. J Clin Investig 1990; 86: 1976-84.
26. Isenberg JS, Ridnour LA, Dimitry J, et al. CD47 is necessary for inhibition of nitric oxide-stimulated vascular cell responses by thrombospondin-1. J Biol Chem 2006; 281: 26069-80.
27. Acquavella N, Quiroga MF, Wittig O, Cardier JE. Effect of simvastatin on endothelial cell apoptosis mediated by Fas and TNF-alpha. Cytokine 2010; 49: 45-50.
28. Wisse E, Braet F, Duimel H, et al. Fixation methods for electron microscopy of human and other liver. World J Gastroenterol 2010; 16: 2851-66.
29. Cheluvappa R, Shimmon R, Dawson M, Hilmer SN, Le Couteur DG. Reactions of Pseudomonas aeruginosa pyocyanin with reduced glutathione. Acta Biochim Pol 2008; 55: 571-80.
30. Bergseth G, Lappegard KT, Videm V, Mollnes TE. A novel enzyme immunoassay for plasma thrombospondin Comparison with beta-thromboglobulin as platelet activation marker in vitro and in vivo. Thromb Res 2000; 99: 41-50.
31. Switalska HI, Niewiarowski S, Tuszynski GP, et al. Radioimmunoassay of human platelet thrombospondin: different patterns of thrombospondin and beta-thromboglobulin antigen secretion and clearance from the circulation. J Lab Clin Med 1985; 106: 690-700.
32. Dawes J, Clemetson KJ, Gogstad GO, et al. A radioimmunoassay for thrombospondin, used in a comparative study of thrombospondin, beta-thromboglobulin and platelet factor 4 in healthy volunteers. Thromb Res 1983; 29: 569-81.
33. Couvelard A, Scoazec JY, Feldmann G. Expression of cell-cell and cell-matrix adhesion proteins by sinusoidal endothelial cells in the normal and cirrhotic human liver. Am J Pathol 1993; 143: 738-52.
34. Tamaki S, Ueno T, Torimura T, Sata M, Tanikawa K. Evaluation of hyaluronic acid binding ability of hepatic sinusoidal endothelial cells in rats with liver cirrhosis. Gastroenterology 1996; 111: 1049-57.
35. Suzuki A, Angulo P, Lymp J, et al. Hyaluronic acid, an accurate serum marker for severe hepatic fibrosis in patients with non-alcoholic fatty liver disease. Liver Int 2005; 25: 779-86.
36. Kondou H, Mushiake S, Etani Y, et al. A blocking peptide for transforming growth factor-beta1 activation prevents hepatic fibrosis in vivo. J Hepatol 2003; 39: 742-8.
37. Halder SK, Beauchamp RD, Datta PK. A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia 2005; 7: 509-21.
38. Shimada H, Staten NR, Rajagopalan LE. TGF-beta1 mediated activation of Rho kinase induces TGF-beta2 and endothelin-1 expression in human hepatic stellate cells. J Hepatol 2011; 54: 521-8.
39. Barazi HO, Li Z, Cashel JA, et al. Regulation of integrin function by CD47 ligands. Differential effects on alpha vbeta 3 and alpha 4beta1 integrin-mediated adhesion. J Biol Chem 2002; 277: 42859-66.
40. Gao AG, Lindberg FP, Finn MB, et al. Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin. J Biol Chem 1996; 271: 21-4.
41. Chao MP, Tang C, Pachynski RK, et al. Extranodal dissemination of non-Hodgkin lymphoma requires CD47 and is inhibited by anti-CD47 antibody therapy. Blood 2011; 118: 4890-901.
42. Braet F, De Zanger R, Baekeland M, et al. Structure and dynamics of the fenestrae-associated cytoskeleton of rat liver sinusoidal endothelial cells. Hepatology 1995; 21: 180-9.
43. Yokomori H, Yoshimura K, Nagai T, et al. Sinusoidal endothelial fenestrae organization regulated by myosin light chain kinase and Rho-kinase in cultured rat sinusoidal endothelial cells. Hepatol Res 2004; 30: 169-74.
44. Murata T, Arii S, Mori A, Imamura M. Therapeutic significance of Y-27632, a Rho-kinase inhibitor, on the established liver fibrosis. J Surg Res 2003; 114: 64-71.
45. Trebicka J, Hennenberg M, Laleman W, et al. Atorvastatin lowers portal pressure in cirrhotic rats by inhibition of RhoA/Rho-kinase and activation of endothelial nitric oxide synthase. Hepatology 2007; 46: 242-53.
46. Abraldes JG, Albillos A, Banares R, et al. Simvastatin lowers portal pressure in patients with cirrhosis and portal hypertension: a randomized controlled trial. Gastroenterology 2009; 136: 1651-8.
47. Kureishi Y, Luo Z, Shiojima I, et al. The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat Med 2000; 6: 1004-10.
48. El-Youssef M, Mu Y, Huang L, Stellmach V, Crawford SE. Increased expression of transforming growth factor-beta1 and thrombospondin-1 in congenital hepatic fibrosis: possible role of the hepatic stellate cell. J Pediatr Gastroenterol Nutr 1999; 28: 386-92.
49. Hayashi K, Kurohiji T, Shirouzu K. Localization of thrombospondin in hepatocellular carcinoma. Hepatology 1997; 25: 569-74.
50. Azcutia V, Stefanidakis M, Tsuboi N, et al. Endothelial CD47 promotes vascular endothelial-cadherin tyrosine phosphorylation and participates in T cell recruitment at sites of inflammation in vivo. J Immunol 2012; 189: 2553-62.
51. Chao MP, Alizadeh AA, Tang C, et al. Therapeutic antibody targeting of CD47 eliminates human acute lymphoblastic leukemia. Cancer Res 2011; 71: 1374-84.
52. Chao MP, Alizadeh AA, Tang C, et al. Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-Hodgkin lymphoma. Cell 2010; 142: 699-713.
53. Zhou Q, Hennenberg M, Trebicka J, et al. Intrahepatic upregulation of RhoA and Rho-kinase signalling contributes to increased hepatic vascular resistance in rats with secondary biliary cirrhosis. Gut 2006; 55: 1296-305.
54. Nunes KP, Rigsby CS, Webb RC. RhoA/Rho-kinase and vascular diseases: what is the link? Cell Mol Life Sci 2010; 67: 3823-36.
55. Ming XF, Viswambharan H, Barandier C, et al. Rho GTPase/Rho kinase negatively regulates endothelial nitric oxide synthase phosphorylation through the inhibition of protein kinase B/Akt in human endothelial cells. Mol Cell Biol 2002; 22: 8467-77.
56. Suzuki H, Kimura K, Shirai H, et al. Endothelial nitric oxide synthase inhibits G12/13 and rho-kinase activated by the angiotensin II type-1 receptor: implication in vascular migration. Arterioscler Thromb Vasc Biol 2009; 29: 217-24.
57. Brouet A, Sonveaux P, Dessy C, et al. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ Res 2001; 89: 866-73.
58. Marrone G, Russo L, Rosado E, et al. The transcription factor KLF2 mediates hepatic endothelial protection and paracrine endothelial-stellate cell deactivation induced by statins. J Hepatol 2012; 58: 98-103.