Sex-dependent effect of liver growth factor on atherosclerotic lesions and fatty liver disease in apolipoprotein E knockout mice

Histology and Histopathology

Volumn 25, Issue 5, 2010, Pages 609-618

  Surra, Joaquín C ^a,d   Guillén, Natalia ^a,d   Barranquero, Cristina ^a,d   Arbonés Mainar, José M ^a   Navarro, María A ^a,d   Gascón, Sonia ^b,d   Arnal, Carmen ^b,d   Godino, Javier ^a   Guzmán, Mario A ^a   Díaz Gil, Juan J ^c   Osada, Jesús ^a,d  

^a INSTITUTO ARAGONÉS DE CIENCIAS DE LA SALUD   (Spain)

^b UNIVERSIDAD DE ZARAGOZA   (Spain)

^c HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^d Instituto de Salud Carlos III   (Spain)

Author keywords

Apolipoprotein; Atherosclerosis; Cholesterol; Fatty liver disease; LGF

Indexed keywords

MUS; RATTUS;

ALBUMIN BILIRUBIN COMPLEX; ALBUMIN-BILIRUBIN COMPLEX; APOLIPOPROTEIN A2; APOLIPOPROTEIN E; BILIRUBIN; MESSENGER RNA; SERUM ALBUMIN;

ANIMAL; ARTICLE; ATHEROSCLEROSIS; C57BL MOUSE; COMPARATIVE STUDY; DRUG EFFECT; FATTY LIVER; FEMALE; GENETICS; GLUCOSE BLOOD LEVEL; LIPID METABOLISM; LIVER; MALE; METABOLISM; MOUSE; MOUSE MUTANT; PATHOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; APOLIPOPROTEIN A-II; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BILIRUBIN; BLOOD GLUCOSE; FATTY LIVER; FEMALE; LIPID METABOLISM; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RNA, MESSENGER; SERUM ALBUMIN; SEX CHARACTERISTICS;

EID: 77953080114     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (40)

1. Acín S., Navarro M.A., Carnicer R., Arbonés-Mainar J.M., Guzmán M.A., Arnal C., Beltrán G., Uceda M., Maeda N. and Osada J. (2005). Dietary cholesterol suppresses the ability of olive oil to delay the development of atherosclerotic lesions in apolipoprotein E knockout mice. Atherosclerosis 182, 17-28.
2. Acín S., Navarro M.A., Perona J.S., Surra J.C., Guillén N., Arnal C., Sarría A.J., Arbonés-Mainar J.M., Carnicer R., Ruiz-Gutiérrez V. and Osada J. (2007). Microarray analysis of hepatic genes differentially expressed in the presence of the unsaponifiable fraction of olive oil in apolipoprotein E-deficient mice. Br. J. Nutr. 97, 628-638.
3. Amarenco P., Labreuche J. and Touboul P.J. (2008). High-density lipoprotein-cholesterol and risk of stroke and carotid atherosclerosis: a systematic review. Atherosclerosis 196, 489-496.
4. Antuna-Puente B., Fevec B., Fellahi S. and Bastard J.P. (2008). Adipokines: The missing link between insulin resistance and obesity. Diabete Metab. 34, 2-11.
5. Aouizerat B.E. and Kane J.P. (2003). Apolipoprotein A-II: active or passive role in familial combined hyperlipidemia. Circ. Res. 92, 1179-1181.
6. Arbonés-Mainar J.M., Navarro M.A., Acín S., Guzmán M.A., Arnal C., Surra J.C., Carnicer R., Roche H.M. and Osada J. (2006a). Trans-10, cis-12- and cis-9, trans-11-conjugated linoleic acid isomers selectively modify HDL-apolipoprotein composition in apolipoprotein E knockout mice. J. Nutr. 136, 353-359.
7. Arbonés-Mainar J.M., Navarro M.A., Guzmán M.A., Arnal C., Surra J.C., Acín S., Carnicer R., Osada J. and Roche H.M. (2006b). Selective effect of conjugated linoleic acid isomers on atherosclerotic lesion development in apolipoprotein E knockout mice. Atherosclerosis 189, 318-327.
8. Assmann G. and Nofer J.R. (2003). Atheroprotective effects of high-density lipoproteins. Annu. Rev. Med. 54, 321-341.
9. Caligiuri G., Nicoletti A., Zhou X., Tornberg I. and Hansson G.K. (1999). Effects of sex and age on atherosclerosis and autoimmunity in apoE-deficient mice. Atherosclerosis 145, 301-308.
10. Castellani L.W., Navab M., Van Lenten B.J., Hedrick C.C., Hama S.Y., Goto A.M., Fogelman A.M. and Lusis A.J. (1997). Overexpression of apolipoprotein AII in transgenic mice converts high density lipoproteins to proinflammatory particles. J. Clin. Invest. 100, 464-474.
11. Castellani L.W., Nguyen C.N., Charugundla S., Weinstein M.M., Doan C.X., Blaner W.S., Wongsiriroj N. and Lusis A.J. (2008). Apolipoprotein AII is a regulator of very low density lipoprotein metabolism and insulin resistance. J. Biol. Chem. 283, 11633-11644.
12. Condezo-Hoyos L., Abderrahim F., Victoria Conde M., Susín C., Díaz-Gil J.J., Carmen González M. and Arribas S.M. (2009). Antioxidant activity of liver growth factor, a bilirubin covalently bound to albumin. Free Radic Biol Med 46, 656-662.
13. Cusa C. and Mazzone A. (2002). The effects of cytokines on the atherosclerotic process. Drugs Today (Barc) 38, 699-712.
14. Díaz-Gil J.J., Escartín P., García-Cañero R., Trilla C., Veloso J.J., Sánchez G., Moreno-Caparrós A., Enrique de Salamanca C., Lozano R., Gavilanes J.G. and García Segura J.M. (1986). Purification of a liver DNA-synthesis promoter from plasma of partially hepatectomized rats. Biochem. J. 235, 49-55.
15. Díaz-Gil J.J., Majano P.L., López-Cabrera M., Sánchez-López V., Rúa C., Machín C., Trilla C., García-Cañero R. and Moreno-Otero R. (2003). The mitogenic activity of the liver growth factor is mediated by tumor necrosis factor alpha in rat liver. J. Hepatol. 38, 598-604.
16. Díaz-Gil J.J., García-Monzón C., Rúa C., Martín-Sanz P., Cereceda R.M., Miquilena-Colina M.E., Machín C., Fernández-Martínez A. and García-Cañero R. (2008). The anti-fibrotic effect of liver growth factor is associated with decreased intrahepatic levels of matrix metalloproteinases 2 and 9 and transforming growth factor beta 1 in bile duct-ligated rats. Histol. Histopathol. 23, 583-591.
17. Díaz-Gil J.J., García-Monzón C., Rúa C., Martín-Sanz P., Cereceda R.M., Miquilena-Colina M.E., Machín C., Fernández-Martínez A. and García-Cañero R. (2009). Liver growth factor antifibrotic activity in vivo is associated with a decrease in activation of hepatic stellate cells. Histol. Histopathol. 24, 473-479.
18. Elhage R., Arnal J.F., Pieraggi M.T., Duverger N., Fievet C., Faye J.C. and Bayard F. (1997). 17 beta-estradiol prevents fatty streak formation in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 17, 2679-2684.
19. Guillén N., Acín S., Navarro M.A., Perona J.S., Arbonés-Mainar J.M., Arnal C., Sarría A.J., Surra J.C., Carnicer R., Orman I., Segovia J.C., Ruiz-Gutiérrez V. and Osada J. (2008). Squalene in a sex-dependent manner modulates atherosclerotic lesion which correlates with hepatic fat content in apoE-knockout male mice. Atherosclerosis 197, 72-83.
20. Guillén N., Navarro M.A., Arnal C., Noone E., Arbonés- Mainar J.M., Acín S., Surra J.C., Muniesa P., Roche H.M. and Osada J. (2009). Microarray analysis of hepatic gene expression identifies new genes involved in steatotic liver. Physiol. Genomics 37, 187-198.
21. Jeong S. and Yoon M. (2007). Inhibition of the actions of peroxisome proliferator-activated receptor alpha on obesity by estrogen. Obesity (Silver Spring) 15, 1430-1440.
22. Jou J., Choi S.S. and Diehl A.M. (2008). Mechanisms of disease progression in nonalcoholic fatty liver disease. Semin. Liver Dis. 28, 370-379.
23. Kastelein J.J., van Leuven S.I., Burgess L., Evans G.W., Kuivenhoven J.A., Barter P.J., Revkin J.H., Grobbee D.E., Riley W.A., Shear C.L., Duggan W.T. and Bots M.L. (2007). Effect of torcetrapib on carotid atherosclerosis in familial hypercholesterolemia. N. Engl. J. Med. 356, 1620-1630.
24. Kawakami M., Koda M. and Murawaki Y. (2007). The prevalence of atherosclerosis in cirrhotic patients: assessment of two aspects of atherosis and sclerosis. Hepatol. Res. 37, 152-157.
25. Kontush A. and Chapman M.J. (2006). Antiatherogenic small, dense HDL - guardian angel of the arterial wall? Nat. Clin. Pract. Cardiovasc. Med. 3, 144-153.
26. Kuipers F., Jong M.C., Lin Y., Van Eck M., Havinga R., Bloks V., Verkade H.J., Hofker M.H., Moshage H., Van Berkel T.J.C., Vonk R.J. and Havekes L.M. (1997). Impaired secretion of very low density lipoprotein-triglycerides by apolipoprotein E-deficient mouse hepatocytes. J. Clin. Invest. 100, 2915-2922.
27. Libby P. and Aikawa M. (2002). Stabilization of atherosclerotic plaques: New mechanisms and clinical targets. Nature Med 8, 1257-1262.
28. Mensenkamp A.R., Havekes L.M., Romijn J.A. and Kuipers F. (2001). Hepatic steatosis and very low density lipoprotein secretion: the involvement of apolipoprotein E. J. Hepatol. 35, 816-822.
29. Meyers C.D. and Kashyap M.L. (2004). Pharmacologic elevation of high-density lipoproteins: recent insights on mechanism of action and atherosclerosis protection. Curr. Opin. Cardiol. 19, 366-373.
30. Navarro M.A., Carpintero R., Acín S., Arbonés-Mainar J.M., Calleja L., Carnicer R., Surra J.C., Guzmán-García M.A., González-Ramón N., Iturralde M., Lampreave F., Piñeiro A. and Osada J. (2005). Immune-regulation of the apolipoprotein A-I/C-III/A-IV gene cluster in experimental inflammation. Cytokine 31, 52-63.
31. Puri V. and Czech M.P. (2008). Lipid droplets: FSP27 knockout enhances their sizzle. J. Clin. Invest. 118, 2693-2696.
32. Rader D.J. (2002). High-density lipoproteins and atherosclerosis. Am. J. Cardiol. 90, 62i-70i.
33. Sarría A.J., Surra J.C., Acín S., Carnicer R., Navarro M.A., Arbonés-Mainar J.M., Guillén N., Martínez-Gracia M.V., Arnal C. and Osada J. (2006). Understanding the role of dietary components on atherosclerosis using genetic engineered mouse models. Front Biosci. 11, 955-967.
34. Somoza B., Abderrahim F., González J.M., Conde M.V., Arribas S.M., Starcher B., Regadera J., Fernández-Alfonso M.S., Díaz-Gil J.J. and González M.C. (2006). Short-term treatment of spontaneously hypertensive rats with liver growth factor reduces carotid artery fibrosis, improves vascular function, and lowers blood pressure. Cardiovasc. Res. 69, 764-771.
35. Tailleux A., Duriez P., Fruchart J.C. and Clavey V. (2002). Apolipoprotein A-II, HDL metabolism and atherosclerosis. Atherosclerosis 164, 1-13.
36. Tall A.R. (1990). Plasma high density lipoproteins. Metabolism and relationship to atherogenesis. J. Clin. Invest. 86, 379-384.
37. Turkish A.R. (2008). Nonalcoholic fatty liver disease: emerging mechanisms and consequences. Curr. Opin. Clin. Nutr. Metab. Care 11, 128-133.
38. Warden C.H., Hedrick C.C., Qiao J.H., Castellani L.W. and Lusis A.J. (1993). Atherosclerosis in transgenic mice overexpressing apolipoprotein A-II. Science 261, 469-472.
39. Weiss J.S., Gautam A., Lauff J.J., Sundberg M.W., Jatlow P., Boyer J.L. and Seligson D. (1983). The clinical importance of a protein-bound fraction of serum bilirubin in patients with hyperbilirubinemia. N. Engl. J. Med. 309, 147-150.
40. Wilson P.W., D'Agostino R.B., Levy D., Belanger A.M., Silbershatz H. and Kannel W.B. (1998). Prediction of coronary heart disease using risk factor categories. Circulation 97, 1837-1847.