Adenovirus-mediated hepatic syndecan-1 overexpression induces hepatocyte proliferation and hyperlipidaemia in mice

Liver International

Volumn 27, Issue 4, 2007, Pages 569-581

  Cortés, Víctor ^a,b   Amigo, Ludwig ^a   Donoso, Katherine ^a   Valencia, Ilse ^c   Quiñones, Verónica ^a   Zanlungo, Silvana ^a   Brandan, Enrique ^b   Rigotti, Attilio ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c HOSPITAL PADRE HURTADO   (Chile)

Author keywords

Apoptosis; Bile; Cell growth; Cholesterol; HDL; Heparan sulfate proteoglycans; LDL; Lipoproteins; Liver; Syndecan 1; Triglycerides

Indexed keywords

ADENOVIRUS VECTOR; ALANINE AMINOTRANSFERASE; APOLIPOPROTEIN B; APOLIPOPROTEIN E; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN; LIPOPROTEIN; PROTEOHEPARAN SULFATE; SYNDECAN 1; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ADENOVIRUS; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL PROLIFERATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE TRANSFER; HYPERLIPIDEMIA; IN VIVO STUDY; LIPID METABOLISM; LIPOPROTEIN SYNTHESIS; LIVER CELL; LIVER REGENERATION; MALE; MOUSE; NONHUMAN; PLASMA CLEARANCE; PLEIOTROPY; PROTEIN DOMAIN; TRIACYLGLYCEROL BLOOD LEVEL;

ADENOVIRIDAE; ANIMALS; CELL PROLIFERATION; HEPARIN; HEPATOCYTES; HYPERLIPIDEMIAS; LIPID METABOLISM; MICE; MICE, TRANSGENIC; PROTEOGLYCANS; SYNDECAN-1; TRANSFECTION;

EID: 34047236123     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/j.1478-3231.2007.01442.x     Document Type: Article

References (59)

1. Bernfield M, Gotte M, Park PW, et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 1999; 68: 729-77.
2. Park PW, Reizes O, Bernfield M. Cell surface heparan sulfate proteoglycans: Selective regulators of ligand-receptor encounters. J Biol Chem 2000; 275: 29923-6.
3. Forsberg E, Kjellen L. Heparan sulfate: Lessons from knockout mice. J Clin Invest 2001; 108: 175-80.
4. Schuppan D. Structure of the extracellular matrix in normal and fibrotic liver: Collagens and glycoproteins. Semin Liver Dis 1990; 10: 1-10.
5. Horner AA. Rat heparan sulphates. A study of the antithrombin-binding properties of heparan sulphate chains from rat adipose tissue, brain, carcase, heart, intestine, kidneys, liver, lungs, skin and spleen. Biochem J 1990; 266: 553-9.
6. Libeu CP, Lund-Katz S, Phillips MC, et al. New insights into the heparan sulfate proteoglycan-binding activity of apolipoprotein E. J Biol Chem 2001; 276: 39138-44.
7. Barth H, Schafer C, Adah MI, et al. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 2003; 278: 41003-12.
8. Shayakhmetov DM, Gaggar A, Ni S, et al. Adenovirus binding to blood factors results in liver cell infection and hepatotoxicity. J Virol 2005; 79: 7478-91.
9. Cerami C, Frevert U, Sinnis P, et al. The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 1992; 70: 1021-33.
10. Turnbull JE, Fernig DG, Ke Y, et al. Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J Biol Chem 1992; 267: 10337-41.
11. Lyon M, Deakin JA, Mizuno K, et al. Interaction of hepatocyte growth factor with heparan sulfate. Elucidation of the major heparan sulfate structural determinants. J Biol Chem 1994; 269: 11216-23.
12. Roskams T, De Vos R, David G, et al. Heparan sulphate proteoglycan expression in human primary liver tumours. J Pathol 1998; 185: 290-7.
13. Hilgard P, Stockert R. Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology 2000; 32: 1069-77.
14. Murata K, Ochiai Y, Akashio K. Polydispersity of acidic glycosaminoglycan components in human liver and the changes at different stages in liver cirrhosis. Gastroenterology 1985; 89: 1248-57.
15. Gressner AM, Krull N, Bachem MG. Regulation of proteoglycan expression in fibrotic liver and cultured fat-storing cells. Pathol Res Pract 1994; 190: 864-82.
16. Otsu K, Kato S, Ohtake K, et al. Alteration of rat liver proteoglycans during regeneration. Arch Biochem Biophys 1992; 294: 544-9.
17. Carey DJ, Bendt KM, Stahl RC. The cytoplasmic domain of syndecan-1 is required for cytoskeleton association but not detergent insolubility. Identification of essential cytoplasmic domain residues. J Biol Chem 1996; 271: 15253-60.
18. Bass MD, Humphries MJ. Cytoplasmic interactions of syndecan-4 orchestrate adhesion receptor and growth factor receptor signalling. Biochem J 2002; 368: 1-15.
19. Kovalszky H, Gallai M, Armbrust T, et al. Syndecan-1 gene expression in isolated rat liver cells (hepatocytes, Kupffer cells, endothelial and Ito cells). Biochem Biophys Res Commun 1994; 204: 944-9.
20. Roskams T, Moshage H, De Vos R, et al. Heparan sulfate proteoglycan expression in normal human liver. Hepatology 1995; 21: 950-8.
21. Couchman JR. Syndecans: Proteoglycan regulators of cell-surface microdomains? Nat Rev Mol Cell Biol 2003; 4: 926-37.
22. Matsumoto A, Ono M, Fujimoto Y, et al. Reduced expression of syndecan-1 in human hepatocellular carcinoma with high metastatic potential. Int J Cancer 1997; 74: 482-91.
23. Salmivirta M, Heino J, Jalkanen M. Basic fibroblast growth factor-syndecan complex at cell surface or immobilized to matrix promotes cell growth. J Biol Chem 1992; 267: 17606-10.
24. Mali M, Elenius K, Miettinen HM, et al. Inhibition of basic fibroblast growth factor-induced growth promotion by overexpression of syndecan-1. J Biol Chem 1993; 268: 24215-22.
25. Kolset SO, Salmivirta M. Cell surface heparan sulfate proteoglycans and lipoprotein metabolism. Cell Mol Life Sci 1999; 56: 857-70.
26. Ji ZS, Sanan DA, Mahley RW. Intravenous heparinase inhibits remnant lipoprotein clearance from the plasma and uptake by the liver: In vivo role of heparan sulfate proteoglycans. J Lipid Res 1995; 36: 583-92.
27. He TC, Zhou S, da Costa LT, et al. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 1998; 95: 2509-14.
28. Mardones P, Pilon A, Bouly M, et al. Fibrates down-regulate hepatic scavenger receptor class B type I protein expression in mice. J Biol Chem 2003; 278: 7884-90.
29. Amigo L, Mardones P, Ferrada C, et al. Biliary lipid secretion, bile acid metabolism, and gallstone formation are not impaired in hepatic lipase-deficient mice. Hepatology 2003; 38: 726-34.
30. Mardones P, Quinones V, Amigo L, et al. Hepatic cholesterol and bile acid metabolism and intestinal cholesterol absorption in scavenger receptor class B type I-deficient mice. J Lipid Res 2001; 42: 170-80.
31. Saunders S, Jalkanen M, O'Farrell S, et al. Molecular cloning of syndecan, an integral membrane proteoglycan. J Cell Biol 1989; 108: 1547-56.
32. Derksen PW, Keehnen RM, Evers LM, et al. Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma. Blood 2002; 99: 1405-10.
33. Alexander CM, Reichsman F, Hinkes MT, et al. Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat Genet 2000; 25: 329-32.
34. Andersen NF, Standal T, Nielsen JL, et al. Syndecan-1 and angiogenic cytokines in multiple myeloma: Correlation with bone marrow angiogenesis and survival. Br J Haematol 2005; 128: 210-7.
35. Seidel C, Borset M, Hjertner O, et al. High levels of soluble syndecan-1 in myeloma-derived bone marrow: Modulation of hepatocyte growth factor activity. Blood 2000; 96: 3139-46.
36. Gallai M, Sebestyen A, Nagy P, et al. Proteoglycan gene expression in rat liver after partial hepatectomy. Biochem Biophys Res Commun 1996; 228: 690-4.
37. Braun L, Mead JE, Panzica M, et al. Transforming growth factor beta mRNA increases during liver regeneration: A possible paracrine mechanism of growth regulation. Proc Natl Acad Sci USA 1988; 85: 1539-43.
38. Modrowski D, Basle M, Lomri A, et al. Syndecan-2 is involved in the mitogenic activity and signaling of granulocyte-macrophage colony-stimulating factor in osteoblasts. J Biol Chem 2000; 275: 9178-85.
39. Filmus J, Selleck SB. Glypicans: Proteoglycans with a surprise. J Clin Invest 2001; 108: 497-501.
40. Johnson NA, Sengupta S, Saidi SA, et al. Endothelial cells preparing to die by apoptosis initiate a program of transcriptome and glycome regulation. FASEB J 2004; 18: 188-90.
41. Ikeguchi M, Hirooka Y, Kaibara N. Heparanase gene expression and its correlation with spontaneous apoptosis in hepatocytes of cirrhotic liver and carcinoma. Eur J Cancer 2003; 39: 86-90.
42. Lai JP, Chien JR, Moser DR, et al. hSulf1 Sulfatase promotes apoptosis of hepatocellular cancer cells by decreasing heparin-binding growth factor signaling. Gastroenterology 2004; 126: 231-48.
43. Mali M, Andtfolk H, Miettinen HM, et al. Suppression of tumor cell growth by syndecan-1 ectodomain. J Biol Chem 1994; 269: 27795-8.
44. Kato M, Wang H, Kainulainen V, et al. Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat Med 1998; 4: 691-7.
45. Fraser R, Dobbs BR, Rogers GW. Lipoproteins and the liver sieve: The role of the fenestrated sinusoidal endothelium in lipoprotein metabolism, atherosclerosis, and cirrhosis. Hepatology 1995; 21: 863-74.
46. Cogger VC, Hilmer SN, Sullivan D, et al. Hyperlipidemia and surfactants: the liver sieve is a link. Atherosclerosis 2006.
47. Carpenter B, Lin Y, Stoll S, et al. VEGF is crucial for the hepatic vascular development required for lipoprotein uptake. Development 2005; 132: 3293-303.
48. Vergani C, Trovato G, Delu A, et al. Serum total lipids, lipoprotein cholesterol, and apolipoprotein A in acute viral hepatitis and chronic liver disease. J Clin Pathol 1978; 31: 772-8.
49. Kanel GC, Radvan G, Peters RL. High-density lipoprotein cholesterol and liver disease. Hepatology 1983; 3: 343-8.
50. Ahaneku JE, Olubuyide IO, Agbedana EO, et al. Changes in plasma high density lipoprotein cholesterol and phospholipid in acute viral hepatitis and cholestatic jaundice. J Intern Med 1991; 229: 17-21.
51. Siagris D, Christofidou M, Theocharis GJ, et al. Serum lipid pattern in chronic hepatitis C: Histological and virological correlations. J Viral Hepat 2006; 13: 56-61.
52. Monroe P, Vlahcevic ZR, Swell L. In vivo evaluation of lipoprotein cholesterol ester metabolism in patients with liver disease. Gastroenterology 1983; 85: 820-9.
53. Erickson SK, Lear SR, Barker ME, et al. Regulation of cholesterol metabolism in the ethionine-induced premalignant rat liver. J Lipid Res 1990; 31: 933-45.
54. Fukushima N, Yamamoto K, Ozaki I, et al. Apolipoprotein A-I, E, C-III and LDL-receptor mRNA expression in liver diseases. Nippon Rinsho 1993; 51: 407-13.
55. Field FJ, Mathur SN, LaBrecque DR. Cholesterol metabolism in regenerating liver of the rat. Am J Physiol 1985; 249: G679-84.
56. de Moura Espindola R, Mazzantini RP, Ong TP, et al. Geranylgeraniol and beta-ionone inhibit hepatic preneoplastic lesions, cell proliferation, total plasma cholesterol and DNA damage during the initial phases of hepatocarcinogenesis, but only the former inhibits NF-kappaB activation. Carcinogenesis 2005; 26: 1091-9.
57. Roos F, Ryan AM, Chamow SM, et al. Induction of liver growth in normal mice by infusion of hepatocyte growth factor/scatter factor. Am J Physiol 1995; 268: G380-6.
58. Kaibori M, Kwon AH, Oda M, et al. Hepatocyte growth factor stimulates synthesis of lipids and secretion of lipoproteins in rat hepatocytes. Hepatology 1998; 27: 1354-61.
59. Miettinen HM, Edwards SN, Jalkanen M. Analysis of transport and targeting of syndecan-1: Effect of cytoplasmic tail deletions. Mol Biol Cell 1994; 5: 1325-39.