Hyperhomocysteinemia induced by methionine supplementation does not independently cause atherosclerosis in C57BL/6J mice

FASEB Journal

Volumn 22, Issue 7, 2008, Pages 2569-2578

  Zhou, Ji ^a,b   Werstuck, Geoff H ^a,b   Lhoták, Šárka ^a,b   Shi, Yuan Y ^a,b   Tedesco, Vivienne ^a   Trigatti, Bernardo ^a   Dickhout, Jeffrey ^a,b   Majors, Alana K ^c   DiBello, Patricia M ^c   Jacobsen, Donald W ^c,d   Austin, Richard C ^a,b,e  

^a MCMASTER UNIVERSITY   (Canada)

^b HENDERSON RESEARCH CENTRE   (Canada)

^c LERNER RESEARCH INSTITUTE   (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

^e ST JOSEPH S HOSPITAL   (Canada)

Author keywords

Atherogenesis; Dietary intervention; Homocysteine; Inflammation; VLDL

Indexed keywords

CHOLESTEROL; CYSTEINE; GLUTATHIONE; HOMOCYSTEINE; HYALURONIC ACID; LOW DENSITY LIPOPROTEIN; METHIONINE; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENDOPLASMIC RETICULUM STRESS; FEMALE; HYPERHOMOCYSTEINEMIA; IMMUNOHISTOCHEMISTRY; LIPID BLOOD LEVEL; LYMPHOCYTE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK FACTOR;

ANIMALS; ATHEROSCLEROSIS; DIET, ATHEROGENIC; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; FEMALE; HOMOCYSTEINE; HYALURONIC ACID; HYPERHOMOCYSTEINEMIA; IMMUNOHISTOCHEMISTRY; LIPIDS; METHIONINE; MICE; MICE, INBRED C57BL;

MUS;

EID: 46749132230     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-105353     Document Type: Article

References (52)

1. Boushey, C. J., Beresford, S. A., Omenn, G. S., Motulsky, A. G. (1995) A quantitative assessment of plasma homocysteine as a risk factor for vascular disease. Probable benefits of increasing folic acid intakes. JAMA 274, 1049-1057
2. Eikelboom, J. W., Lonn, E., Genest, J., Jr., Hankey, G., Yusuf, S. (1999) Homocyst(e)ine and cardiovascular disease: a critical review of the epidemiologic evidence. Ann. Intern. Med. 131, 363-375
3. Zhou, J., Moller, J., Danielsen, C. C., Bentzon, J., Ravn, H. B., Austin, R. C., Falk, E. (2001) Dietary supplementation with methionine and homocysteine promotes early atherosclerosis but not plaque rupture in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 21, 1470-1476
4. Hofmann, M. A., Lalla, E., Lu, Y., Gleason, M. R., Wolf, B. M., Tanji, N., Ferran, L. J., Jr., Kohl, B., Rao, V., Kisiel, W., Stern, D. M., Schmidt, A. M. (2001) Hyperhomocysteinemia enhances vascular inflammation and accelerates atherosclerosis in a murine model. J. Clin. Invest. 107, 675-683
5. Zhou, J., Moller, J., Ritskes-Hoitinga, M., Larsen, M. L., Austin, R. C., Falk, E. (2003) Effects of vitamin supplementation and hyperhomocysteinemia on atherosclerosis in apoE-deficient mice. Atherosclerosis 168, 255-262
6. Wang, H., Jiang, X., Yang, F., Gaubatz, J. W., Ma, L., Magera, M. J., Yang, X., Berger, P. B., Durante, W., Pownall, H. J., Schafer, A. I. (2003) Hyperhomocysteinemia accelerates atherosclerosis in cystathionine beta-synthase and apolipoprotein E double knock-out mice with and without dietary perturbation. Blood 101, 3901-3907
7. Matthias, D., Becker, C. H., Riezler, R., Kindling, P. H. (1996) Homocysteine induced arterosclerosis-like alterations of the aorta in normotensive and hypertensive rats following application of high doses of methionine. Atherosclerosis 122, 201-216
8. Donahue, S., Sturman, J. A., Gaull, G. (1974) Arterisclerosis due to homocyst(e)inemia. Failure to reproduce the model in weanling rabbits. Am. J. Pathol. 77, 167-174
9. Reddy, G. S. R., Wilcken, D. E. L. (1982) Experimental homocysteinemia in pigs: comparison with studies in sixteen homocystinuric patients. Metabolism 31, 778-783
10. Harker, L. A., Ross, R., Slichter, S. J., Scott, C. R. (1976) Homocystine-induced arterosclerosis. The role of endothelial cell injury and platelet response in its genesis. J. Clin. Invest. 58, 731-741
11. Mudd, S. H., Skovby, F., Levy, H. L., Pettigrew, K. D., Wilcken, B., Pyeritz, R. E., Andria, G., Boers, G. H. J., Bromberg, I. L., Cerone, R., Fowler, B., Grobe, H., Schmidt, H., Schweitzer, L. (1985) The natural history of homocystinuria due to cystathionine-β-synthase deficiency. Am. J. Hum. Genet. 37, 1-31
12. Rosenblatt, D. S., Fenton, W. A. (2001) Inherited disorders of folate and cobalamin transport and metabolism. In The Metabolic & Molecular Bases of Inherited Disease, 8th Ed (Scriver CR, Beaudet AL, Sly WS, Valle D, Childs B, Kinzler KW, Vogelstein B, eds) pp. 3897-3933, McGraw Hill, New York
13. Rubba, P, Minno, G. D., Andria, G. (2000) Vascular complications of homocystinuria: incidence, clinical pattern and treatment, In Homocysteine and Vascular Disease (Robinson, K., ed), pp. 117-134, Kluwer Academic Publishers, Dordrecht, The Netherlands
14. Wilcken, D. E. L. (2000) Historical aspects of the relationship between homocysteine and vascular disease, In Homocysteine and Vascular Disease (Robinson, K., ed) pp. 5-14, Kluwer Academic Publishers, Dordrecht, The Netherlands
15. Malinow, M. R. (1995) Plasma homocyst(e)ine and arterial occlusive diseases: a mini-review. Clin. Chem. 41, 173-176
16. McQuillan, B. M., Beilby, J. P., Nidorf, M., Thompson, P. L., Hung, J. (1999) Hyperhomocysteinemia but not the C677T mutation of methylenetetrahydrofolate reductase is an independent risk determinant of carotid wall thickening. The Perth Carotid Ultrasound Disease Assessment Study (CUDAS). Circulation 99, 2383-2388
17. Smilde, T. J., van den Berkmortel, F. W., Boers, G. H., Wollersheim, H., de Boo, T., van Langen, H., Stalenhoef, A. F. (1998) Carotid and femoral artery wall thickness and stiffness in patients at risk for cardiovascular disease, with special emphasis on hyperhomocysteinemia. Arterioscler. Thromb. Vasc. Biol. 18, 1958-1963
18. Burke, A. P., Fonseca, V., Kolodgie, F., Zieske, A., Fink, L., Virmani, R. (2002) Increased serum homocysteine and sudden death resulting from coronary atherosclerosis with fibrous plaques. Arterioscler. Thromb. Vasc. Biol. 22, 1936-1941
19. Jacobsen, D. W., Gatautis, V. J., Green, R., Robinson, K., Savon, S. R., Secic, M., Ji, J., Otto, J. M., Taylor, L. M., Jr. (1994) Rapid HPLC determination of total homocysteine and other thiols in serum and plasma: sex differences and correlation with cobalamin and folate levels in normal subjects. Clin. Chem. 40, 873-881
20. Rigotti, A., Trigatti, B. L., Penman, M., Rayburn, H., Herz, J., Krieger, M. (1997) A targeted mutation in the murine gene encoding the high-density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc. Natl. Acad. Sci. U. S. A. 94, 12610-12615
21. Paigen, B., Morrow, A., Holmes, P. A., Mitchell, D., Williams, R. A. (1987) Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis 68, 231-240
22. Dixon, J. L., Shen, S., Vuchetich, J. P., Wysocka, E., Sun, G. Y., Sturek, M. (2002) Increased atherosclerosis in diabetic dyslipidemic swine: protection by atorvastatin involves decreased VLDL triglycerides but minimal effects on the lipoprotein profile. J. Lipid. Res. 43, 1618-1629
23. Zhou, J., Werstuck, G. H., Lhoták, S., de Koning, A. B. L., Sood, S. K., Hossain, G. S., Møller, J., Ritskes-Hoitinga, M., Falk, E., Dayal, S., Lentz, S. R., Austin, R. C. (2004) Association of multiple cellular stress pathways with accelerated atherosclerosis in hyperhomocysteinemic apolipoprotein E-deficient mice. Circulation 110, 207-213
24. Majors, A. K., Austin, R. C., de la Motte, C. A., Pyeritz, R. E., Hascall, V. C., Kessler, S. P., Sen, G., Strong, S. A. (2003) Endoplasmic reticulum stress induces hyaluronan deposition and leukocyte adhesion. J. Biol. Chem. 278, 47223-47231
25. Hascall, V. C., Majors, A. K., De La Motte, C. A., Evanko, S. P., Wang, A., Drazba, J. A., Strong, S. A., Wight, T. N. (2004) Intracellular hyaluronan: a new frontier for inflammation? Biochim. Biophys. Acta 1673, 3-12
26. Zhou, J., Lhotak, S., Hilditch, B. A., Austin, R. C. (2005) Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 111, 1814-1821
27. Paigen, B., Morrow, A., Brandon, C., Mitchell, D., Holmes, P. (1985) Variation in susceptibility to atherosclerosis among inbred strains of mice. Atherosclerosis 57, 65-73
28. Sampedro, M. C., Motrán, C., Gruppi, A., Kivatinitz, S. C. (2001) VLDL modulates the cytokine secretion profile to a proinflmmatory pattern. Biochem. Biophys. Res. Commun. 285, 393-399
29. Stollenwerk, M. M., Lindholm, M. W., Pörn-Ares, M. I., Larsson, A., Nilsson, J., Ares, M. P. (2005) Very low-density lipoprotein induces interleukin-1β expression in macrophages. Biochem. Biophys. Res. Commun. 335, 603-608
30. Stollenwerk, M. M., Schiopu, A., Fredrikson, G. N., Dichtl, W., Nilsson, J., Ares, M. P. (2005) Very low density lipoprotein potentiates tumor necrosis factor-alpha expression in macrophages. Atherosclerosis 179, 247-254
31. Vergnes, L., Phan, J., Strauss, M., Tafuri, S., Reue, K. (2003) Cholesterol and cholate components of an atherogenic diet induce distinct changes of hepatic inflammatory gene expression. J. Biol. Chem. 278, 42774-42784
32. Zulli, A., Hare, D. L., Buxton, B. F., Black, M. J. (2004) High dietary methionine plus cholesterol exacerbates atherosclerosis formation in the left main coronary artery of rabbits. Atherosclerosis 176, 83-89
33. Werstuck, G. H., Lentz, S. R., Dayal, S., Hossain, G. S., Sood, S. K., Shi, Y. Y., Zhou, J., Maeda, N., Krisans, S. K., Malinow, M. R., Austin, R. C. (2001) Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J. Clin. Invest. 107, 1263-1273
34. Ji, C., Kaplowitz, N. (2003) Betaine decreases hyperhomocysteinemia, endoplasmic reticulum stress, and liver injury in alcohol-fed mice. Gastroenterol. 124, 1488-1499
35. Colgan, S. M., Tang, D., Werstuck, G. H., Austin, R. C. (2007) Endoplasmic reticulum stress causes the activation of sterol regulatory element binding protein-2. Int. J. Biochem. Cell. Biol. 39, 1843-1851
36. Wilson, K. M., McCaw, R. B., Leo, L., Arning, E., Lhoták, S., Bottiglieri, T., Austin, R. C., Lentz, S. R. (2007) Prothrombotic effects of hyperhomocysteinemia and hypercholesterolemia in apoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 27, 233-240
37. Iciek, M., Chwatko, G., Lorenc-Koci, E., Bald, E., Wlodek, L. (2004) Plasma levels of total, free and protein bound thiols as well as sulfane sulfur in different age groups of rats. Acta Biochim. Pol. 51, 815-824
38. Kokame, K., Kato, H., Miyata, T. (1996) Homocysteine-respondent genes in vascular endothelial cells identified by differential display analysis. BRP78/BiP and novel genes. J. Biol. Chem. 271, 29659-29665
39. Chen, Z., Ge, B., Hudson, T. J., Rozen, R. (2002) Microarray analysis of brain RNA in mice with methylenetetrahydrofolate reductase deficiency and hyperhomocysteinemia. Brain Res. Gene Expr. Patterns 1, 89-93
40. Srivastava, R. A., Averna, M., Srivastava, N., Pape, M. E. (2001) Dietary cholate increases plasma levels of apolipoprotein B in mice by posttranscriptional mechanisms. Int. J. Biochem. Cell. Biol. 33, 1215-1226
41. Tatami, R., Mabuchi, H., Ueda, K., Ueda, R., Haba, T., Kametani, T., Ito, S., Koizumi, J., Ohta. M., Miyamoto, S., Nakayama, A., Kanaya, H., Oiwake, H., Genda, A., Takeda, R. (1981) Intermediate-density lipoprotein and cholesterol-rich very low density lipoprotein in angiographically determined coronary artery disease. Circulation 64, 1174-1184
42. Mack, W. J., Krauss, R. M., Hodis, H. N. (1996) Lipoprotein subclasses in the Monitored Atherosclerosis Regression Study (MARS). Treatment effects and relation to coronary angiographic progression. Arterioscler. Thromb. Vasc. Biol. 16, 697-704
43. Srivastava, R. A., Srivastava, N., Averna, M. (2000) Dietary cholic acid lowers plasma levels of mouse and human apolipoprotein A-I primarily via a transcriptional mechanism. Eur. J. Biochem. 267, 4272-4280
44. Olszanecki, R., Jawień J, Gajda, M., Mateuszuk, L., Gebska, A., Korabiowska, M., Chłopicki, S., and Korbut, R. (2005) Effect of curcumin on atherosclerosis in apoE/LDLR-double knockout mice. J. Physiol. Pharmacol. 56, 627-635
45. Norata, G. D., Marchesi, P., Passamonti, S., Pirillo, A., Violi, F., and Catapano, A. L. (2007) Anti-inflammatory and antiatherogenic effects of cathecin, caffeic acid and trans-resveratrol in apolipoprotein E deficient mice. Atherosclerosis 191, 265-271
46. Burleigh, M. E., Babaev, V. R., Patel, M. B., Crews, B. C., Remmel, R. P., Morrow, J. D., Oates, J. A., Marnett, L. J., Fazio, S., and Linton, M. F. (2005) Inhibition of cyclooxygenase with indomethacin phenethylamide reduces atherosclerosis in apoE-null mice. Biochem. Pharmacol. 70, 334-342
47. Monetti, M., Canavesi, M., Camera, M., Parente, R., Paoletti, R., Tremoli, E., Corsini, A., and Bellosta, S. (2007) Rosuvastatin displays anti-atherothrombotic and anti-inflammatory properties in apoE-deficient mice. Pharmacol. Res. 55, 441-449
48. Scalia, R., Gooszen, M. E., Jones, S. P., Hoffmeyer, M., Rimmer, D. M., Trocha, S. D., Huang, P. L., Smith, M. B., Lefer, A. M., and Lefer, D. J. (2001) Simvastatin exerts both anti-inflammatory and cardioprotective effects in apolipoprotein E-deficient mice. Circulation 103, 2598-2603
49. Kleeman, R., Princen, H. M., Emeis, J. J., Jukema, J. W., Fontijn, R. D., Horrevoets, A. J., Kooistra, T., and Haveke, L. M. (2003) Rosuvastatin reduces atherosclerosis development beyond and independent of its plasma cholesterol-lowering effect in APO*3-Leiden transgenic mice: evidence for anti-inflammatory effects of rosuvastatin. Circulation 108, 1368-1374
50. Chai, S., Chai, Q., Danielsen, C. C., Hjorth, P., Nyengaard, J. R., Ledet, T., Yamaguchi, Y., Rasmussen, L. M., Wogensen, L. (2005) Overexpression of hyaluronan in the tunica media promotes the development of atherosclerosis. Circ. Res. 96, 583-591
51. Bernstein, H., Payne, C. M., Bernstein, C., Schneider, J., Beard, S. E., Crowley, C. L. (1999) Activation of the promoters of genes associated with DNA damage, oxidative stress, ER stress and protein malfolding by the bile salt, deoxycholate. Toxicol. Lett. 108, 37-46
52. McCully, K. S. (1969) Vascular pathology of homocysteinemia: implications for the pathogenesis of arteriosclerosis. Am. J. Pathol. 56, 111-128