RGD-peptide lunasin inhibits Akt-mediated NF-κB activation in human macrophages through interaction with the αVβ3 integrin

Molecular Nutrition and Food Research

Volumn 56, Issue 10, 2012, Pages 1569-1581

  Cam, Anthony ^a   de Mejia, Elvira Gonzalez ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Atherosclerosis; Cardiovascular disease; Inflammation; Integrin; RGD Peptide

Indexed keywords

ARGINYL-GLYCYL-ASPARTIC ACID; ARGINYLGLYCYLASPARTIC ACID; CYCLOOXYGENASE 2; GM2S 1 PROTEIN, GLYCINE MAX; GM2S-1 PROTEIN, GLYCINE MAX; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; NITRIC OXIDE; NOS2 PROTEIN, HUMAN; OLIGOPEPTIDE; PROTEIN KINASE B; PTGS2 PROTEIN, HUMAN; SOYBEAN PROTEIN; TUMOR NECROSIS FACTOR ALPHA; VITRONECTIN; VITRONECTIN RECEPTOR;

ARTICLE; CELL LINE; CELL PROLIFERATION; CONFOCAL MICROSCOPY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOPRECIPITATION; INFLAMMATION; MACROPHAGE; METABOLISM; PATHOPHYSIOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

CELL LINE; CELL PROLIFERATION; CYCLOOXYGENASE 2; HUMANS; IMMUNOPRECIPITATION; INFLAMMATION; INTEGRIN ALPHAVBETA3; LIPOPOLYSACCHARIDES; MACROPHAGES; MICROSCOPY, CONFOCAL; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OLIGOPEPTIDES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SOYBEAN PROTEINS; TANDEM MASS SPECTROMETRY; TUMOR NECROSIS FACTOR-ALPHA; VITRONECTIN;

EID: 84867090699     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200301     Document Type: Article

References (59)

1. Heron, M. P., Hoyert, D. L., Murphy, S. L., Xu, J. Q. et al., Deaths: final data for 2006. National Vital Statistics Reports. Natl. Vital Stat. Rep. 2009, 57, 1-134.
2. Lloyd-Jones, D., Adams, R. J., Brown, T. M., Carnethon, M. et al., Executive summary: heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 2010, 121, 948-954.
3. Heidenreich, P. A., Trogdon, J. G., Khavjou, O. A., Butler, J. et al., Forecasting the future of cardiovascular disease in the United States. A policy statement from the American Heart Association. Circulation 2011, 123, 933-944.
4. Moore, K. J., Tabas, I., Macrophages in the pathogenesis of atherosclerosis. Cell 2011, 145, 341-355.
5. Dia, V. P., Berhow, M. A., De Mejia, E. G., Bowman-Birk inhibitor and genistein among soy compounds that synergistically inhibit nitric oxide and prostaglandin E(2) pathways in lipopolysaccharide-induced macrophages. J. Agric. Food Chem. 2008, 56, 11707-11717.
6. de Mejia, E. G., Dia, V. P., Lunasin and lunasin-like peptides inhibit inflammation through suppression of NF-kappaB pathway in the macrophage. Peptides 2009, 30, 2388-2398.
7. Martinez-Villaluenga, C., Dia, V. P., Berhow, M., Bringe, N. A., de Mejia, E. G., Protein hydrolysates from β-conglycinin enriched soybean genotypes inhibit lipid accumulation and inflammation in vitro. Mol. Nutr. Food Res. 2009, 53, 1007-1018.
8. Food labeling: health claims; soy protein and coronary heart disease. Food and Drug Administration, HHS. Final rule. Fed. Regist. 1999, 64, 57700-57733.
9. Anderson, J. W., Bush, H. M., Soy protein effects on serum lipoproteins: a quality assessment and meta-analysis of randomized, controlled studies. J. Am. Coll. Nutr. 2011, 30, 79-91.
10. Tabas, I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 2010, 10, 36-46.
11. Dia, V. P., de Mejia, E. G., Lunasin induces apoptosis and modifies the expression of genes associated with extracellular matrix and cell adhesion in human metastatic colon cancer cells. Mol. Nutr. Food Res. 2011, 55, 623-634.
12. Dia, V. P., Torres, S., de Lumen, B. O., Erdman, J. W., Jr, de Mejia, E. G., Presence of lunasin in plasma of men after soy protein consumption. J. Agric. Food Chem. 2009, 57, 1260-1266.
13. Campbell, I. D., Humphries, M. J., Integrin structure, activation, and interactions. Cold Spring Harb. Perspect. Biol. 2011, 3, a004994.
14. Springer, T. A., Dustin, M. L., Integrin inside-out signaling and the immunological synapse. Curr. Opin. Cell Biol. 2012, 24, 107-115.
15. Kim, C., Ye, F., Ginsberg, M. H., Regulation of integrin activation. Annu. Rev. Cell Dev. Biol. 2011, 27, 321-345.
16. Kuphal, S., Bauer, R., Bosserhoff, A. K., Integrin signaling in malignant melanoma. Cancer Metastasis Rev. 2005, 24, 195-222.
17. Tan, T. W., Yang, W. H., Lin, Y. T., Hsu, S. F. et al., Cyr61 increases migration and MMP-13 expression via alphavbeta3 integrin, FAK, ERK and AP-1-dependent pathway in human chondrosarcoma cells. Carcinogenesis 2009, 30, 258-268.
18. Marsh, N., Williams, V., Practical applications of snake venom toxins in haemostasis. Toxicon 2005, 45, 1171-1181.
19. Furundzija, V., Fritzsche, J., Kaufmann, J., Meyborg, H. et al., IGF-1 increases macrophage motility via PKC/p38-dependent alphavbeta3-integrin inside-out signaling. Biochem. Biophys. Res. Commun. 2010, 394, 786-791.
20. Kitagawa, T., Kosuge, H., Uchida, M., Dua, M. M. et al., RGD-conjugated human ferritin nanoparticles for imaging vascular inflammation and angiogenesis in experimental carotid and aortic disease. Mol. Imaging Biol. 2011, 3, 315-324.
21. Antonov, A. S., Antonova, G. N., Munn, D. H., Mivechi, N. et al., Alpha V beta 3 Integrin regulates macrophage inflammatory responses via PI3 Kinase/Akt-dependent NF-kappa B activation. J. Cell. Physiol. 2011, 226, 469-476.
22. Nichols, T. C., du Laney, T., Zheng, B., Bellinger, D. A. et al., Reduction in atherosclerotic lesion size in pigs by alphaVbeta3 inhibitors is associated with inhibition of insulin-like growth factor-I-mediated signaling. Circ. Res. 1999, 85, 1040-1045.
23. Maile, L. A., Busby, W. H., Nichols, T. C., Bellinger, D. A. et al., A monoclonal antibody against alphaVbeta3 integrin inhibits development of atherosclerotic lesions in diabetic pigs. Sci. Transl. Med. 2010, 2, 18ra11.
24. Lee, C., Huang, C., Chen, M., Lin, C. et al., IL-8 increases integrin expression and cell motility in human chondrosarcoma cells. J. Cell. Biochem. 2011, 112, 2549-2557.
25. Dia, V. P., Wang, W., Oh, V. L., de Lumen, B. O., de Mejia, E. G., Isolation, purification and characterisation of lunasin from defatted soybean flour and in vitro evaluation of its anti-inflammatory activity. Food Chem. 2009, 114, 108-115.
26. Green, L., Wagner, D., Glogowski, J., Skipper, P. et al., Analysis of nitrate, nitrite, and [N-15]-labeled nitrate in biological fluids. Anal. Biochem. 1982, 126, 131-138.
27. Libby, P., Okamoto, Y., Rocha, V. Z., Folco, E., Inflammation in atherosclerosis: transition from theory to practice. Circ. J. 2010, 74, 213-220.
28. Aguzzi, M. S., Fortugno, P., Giampietri, C., Ragone, G. et al., Intracellular targets of RGDS peptide in melanoma cells. Mol. Cancer 2010, 9, 84.
29. Laitinen, I., Saraste, A., Weidl, E., Poethko, T. et al., Evaluation of alphavbeta3 integrin-targeted positron emission tomography tracer 18F-galacto-RGD for imaging of vascular inflammation in atherosclerotic mice. Circ. Cardiovasc. Imaging 2009, 2, 331-338.
30. Calleja, V., Alcor, D., Laguerre, M., Park, J. et al., Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo RID E-7465-2010. PLoS Biol. 2007, 5, 780-791.
31. Hers, I., Vincent, E. E., Tavare, J. M., Akt signalling in health and disease. Cell Signal. 2011, 23, 1515-1527.
32. Hsu, C. C., Chuang, W. J., Chang, C. H., Tseng, Y. L. et al., Improvements in endotoxemic syndromes using a disintegrin, rhodostomin, through integrin alpha v beta 3-dependent pathway. J. Thromb. Haemost. 2011, 9, 593-602.
33. Yasuda, T., Hyaluronan inhibits Akt, leading to nuclear factor-kappa B down-regulation in lipopolysaccharide-stimulated U937 macrophages. J. Pharmacol. Sci. 2011, 115, 509-515.
34. Foerstermann, U., Oxidative stress in vascular disease: causes, defense mechanisms and potential therapies. Nat. Clin. Pract. Cardiovasc. Med. 2008, 5, 338-349.
35. Forstermann, U., Nitric oxide and oxidative stress in vascular disease. Pflugers Arch. 2010, 459, 923-939.
36. Behr-Roussel, D., Rupin, A., Sansilvestri-Morel, P., Fabiani, J. et al., Histochemical evidence for inducible nitric oxide synthase in advanced but non-ruptured human atherosclerotic carotid arteries. Histochem. J. 2000, 32, 41-51.
37. Terashima, M., Ehara, S., Yang, E., Kosuge, H. et al., In vivo bioluminescence imaging of inducible nitric oxide synthase gene expression in vascular inflammation. Mol. Imaging Biol. 2011, 13, 1061-1066.
38. Detmers, P., Hernandez, M., Mudgett, J., Hassing, H. et al., Deficiency in inducible nitric oxide synthase results in reduced atherosclerosis in apolipoprotein E-deficient mice RID D-2074-2010. J. Immunol. 2000, 165, 3430-3435.
39. Hayashi, T., Matsui-Hirai, H., Fukatsu, A., Surni, D. et al., Selective iNOS inhibitor, ONO1714 successfully retards the development of high cholesterol diet-induced atherosclerosis by novel mechanism. Atherosclerosis 2006, 187, 316-324.
40. Pistoia, F., Cipollone, F., Ferri, C., Sara, M. et al., Cyclooxygenase and atherosclerosis: a smoking area. Curr. Pharm. Des. 2010, 16, 2567-2571.
41. Jeffes, E., McCullough, J., Pittelkow, M., McCormick, A. et al., Methotrexate therapy of psoriasis-differential sensitivity of proliferating lymphoid and epithelial-cells to the cytotoxic and growth-inhibitory effects of methotrexate. J. Invest. Dermatol. 1995, 104, 183-188.
42. Fedorov, S. N., Makarieva, T. N., Guzii, A. G., Shubina, L. K. et al., Marine two-headed sphingolipid-like compound Rhizochalin inhibits EGF-induced transformation of JB6 P(+) Cl41 cells. Lipids 2009, 44, 777-785.
43. Parameswaran, N., Patial, S., Tumor necrosis factor-alpha signaling in macrophages. Crit. Rev. Eukaryot. Gene Expr. 2010, 20, 87-103.
44. Hsu, H., Twu, Y., Tumor necrosis factor-alpha-mediated protein kinases in regulation of scavenger receptor and foam cell formation on macrophage. J. Biol. Chem. 2000, 275, 41035-41048.
45. McLaren, J.E., Calder, C. J., McSharry, B.P., Sexton, K. et al., The TNF-like protein 1A-death receptor 3 pathway promotes macrophage foam cell formation in vitro. J. Immunol. 2010, 184, 5827-5834.
46. Kurihara, Y., Nakahara, T., Furue, M., Alpha V beta 3-integrin expression through ERK activation mediates cell attachment and is necessary for production of tumor necrosis factor alpha in monocytic THP-1 cells stimulated by phorbol myristate acetate. Cell. Immunol. 2011, 270, 25-31.
47. Hernandez-Ledesma, B., Hsieh, C., de Lumen, B. O., Antioxidant and anti-inflammatory properties of cancer preventive peptide lunasin in RAW 264.7 macrophages. Biochem. Biophys. Res. Commun. 2009, 390, 803-808.
48. Howell, K. W., Meng, X., Fullerton, D. A., Jin, C. et al., Toll-like receptor 4 mediates oxidized LDL-induced macrophage differentiation to foam cells. J. Surg. Res. 2011, 171, E27-E31.
49. Jialal, I., Huet, B. A., Kaur, H., Chien, A., Devaraj, S., Increased toll-like receptor activity in patients with metabolic syndrome. Diabetes Care 2012, 35, 900-904.
50. Scholtes, V. P. W., Versteeg, D., de Vriest, J. P. M., Hoefer, I. E. et al., Toll-like receptor 2 and 4 stimulation elicits an enhanced inflammatory response in human obese patients with atherosclerosis. Clin. Sci. 2011, 121, 205-214.
51. Dufourcq, P., Couffinhal, T., Alzieu, P., Daret, D. et al., Vitronectin is up-regulated after vascular injury and vitronectin blockade prevents neointima formation. Cardiovasc. Res. 2002, 53, 952-962.
52. Ekmekci, O., Ekmekci, H., Vitronectin in atherosclerotic disease. Clin. Chim. Acta 2006, 368, 77-83.
53. Choi, E., Engel, L., Callow, A., Sun, S. et al., Inhibition of neointimal hyperplasia by blocking alpha(v)beta(3), integrin with a small peptide antagonist Gpengrgdspca. J. Vasc. Surg. 1994, 19, 125-134.
54. Srivatsa, S., Fitzpatrick, L., Tsao, P., Reilly, T. et al., Selective alpha v beta 3 integrin blockade potently limits neointimal hyperplasia and lumen stenosis following deep coronary arterial stent injury: evidence for the functional importance of integrin alpha v beta 3 and osteopontin expression during neointima formation. Cardiovasc. Res. 1997, 36, 408-428.
55. Xiong, J., Stehle, T., Zhang, R., Joachimiak, A. et al., Crystal structure of the extracellular segment of integrin alpha V beta 3 in complex with an Arg-Gly-Asp ligand. Science 2002, 296, 151-155.
56. Margadant, C., Monsuur, H. N., Norman, J. C., Sonnenberg, A., Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 2011, 23, 607-614.
57. Sancey, L., Garanger, E., Foillard, S., Schoehn, G. et al., Clustering and internalization of integrin alphavbeta3 with a tetrameric RGD-synthetic peptide. Mol. Ther. 2009, 17, 837-843.
58. Castel, S., Pagan, R., Mitjans, F., Piulats, J. et al., RGD peptides and monoclonal antibodies, antagonists of alpha(v)-integrin, enter the cells by independent endocytic pathways. Lab. Invest. 2001, 81, 1615-1626.
59. Szabo, A. M., Howell, N. R., Pellegrini, P., Greguric, I. et al., Development and validation of competition binding assays for affinity to the extracellular matrix receptors, alpha(v)beta(3) and alpha(IIb)beta(3) integrin. Anal. Biochem. 2012, 423, 70-77.