Novel splice variants of the receptor for advanced glycation end-products expressed in human vascular endothelial cells and pericytes, and their putative roles in diabetes-induced vascular injury

Biochemical Journal

Volumn 370, Issue 3, 2003, Pages 1097-1109

  Yonekura, Hideto ^a   Yamamoto, Yasuhiko ^a   Sakurai, Shigeru ^a   Petrova, Ralica G ^a   Abedin, Md Joynal ^a   Li, Hui ^a   Yasui, Kiyoshi ^a   Takeuchi, Masayoshi ^b   Makita, Zenji ^c   Takasawa, Shin ^d   Okamoto, Hiroshi ^d   Watanabe, Takuo ^a   Yamamoto, Hiroshi ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

^b HOKURIKU UNIVERSITY   (Japan)

^c KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Alternative splicing; Angiogenesis; Diabetic vascular complication; Non enzymic glycation; Soluble type receptor

Indexed keywords

BIOLOGICAL MEMBRANES; IMMUNOLOGY; MOLECULAR BIOLOGY; PATHOLOGY; PROTEINS; RNA;

GLYCATION;

CELL CULTURE;

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; GROWTH FACTOR; IMMUNOGLOBULIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL MEMBRANE; CONTROLLED STUDY; DIABETIC ANGIOPATHY; DISEASE PREDISPOSITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PERICYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; VASCULAR ENDOTHELIUM;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; DIABETES COMPLICATIONS; DIABETES MELLITUS; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOKINES; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; PERICYTES; PROTEIN BINDING; PROTEIN ISOFORMS; RECEPTORS, IMMUNOLOGIC; SEQUENCE ALIGNMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

ANIMALIA;

EID: 0037444761     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021371     Document Type: Article

References (42)

1. Brownlee, M., Cerami, A. and Vlassara, H. (1988) Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N. Engl. J. Med. 318, 1315-1321
2. Thornalley, P. J. (1998) Cell activation by glycated proteins. AGE receptors, receptor recognition factors and functional classification of AGEs. Cell. Mol. Biol. 44, 1013-1023
3. Schmidt, A. M. and Stern, D. M. (2000) RAGE: a new target for the prevention and treatment of the vascular and inflammatory complications of diabetes. Trends Endocrinol. Metab. 11, 368-375
4. Schmidt, A. M., Vianna, M., Gerlach, M., Brett, J., Ryan, J., Kao, J., Esposito, C., Hegarty, H., Hurley, W., Clauss, M. et al. (1992) Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J. Biol. Chem. 267, 14987-14997
5. Neeper, M., Schmidt, A. M., Brett, J., Yan, S. D., Wang, F., Pan, Y.-C. E., Elliston, K., Stern, D. and Shaw, A. (1992) Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J. Biol. Chem. 267, 14998-15004
6. Hofmann, M. A., Drury, S., Fu, C., Qu, W., Taguchi, A., Lu, Y., Avil, C., Kambham, N., Bierhaus, A., Nawroth, P. et al. (1999) RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell (Cambridge, Mass.) 97, 889-901
7. Huttunen, H. J., Fages, C. and Rauvala, H. (1999) Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-κB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J. Biol. Chem. 274, 19919-19924
8. Brett, J., Schmidt, A. M., Yan, S. D., Zou, Y. S., Weidman, E., Pinsky, D., Nowygrod, R., Neeper, M., Przysiecki, C., Shaw, A. et al. (1993) Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am. J. Pathol. 143, 1699-1712
9. Yamagishi, S., Yonekura, H., Yamamoto, Y., Katsuno, K., Sato, F., Mita, I., Ooka, H., Satozawa, N., Kawakami, T., Nomura, M. et al. (1997) Advanced glycation end products-driven angiogenesis in vitro. Induction of the growth and tube formation of human microvascular endothelial cells through autocrine vascular endothelial growth factor. J. Biol. Chem. 272, 8723-8730
10. Yamagishi, S., Fujimori, H., Yonekura, H., Yamamoto, Y. and Yamamoto, H. (1998) Advanced glycation endproducts inhibit prostacyclin production and induce plasminogen activator inhibitor-1 in human microvascular endothelial cells. Diabetologia 41, 1435-1441
11. Yamagishi, S., Hsu, C.-C., Taniguchi, M., Harada, S., Yamamoto, Y., Ohsawa, K., Kobayashi, K. and Yamamoto, H. (1995) Receptor-mediated toxicity to pericytes of advanced glycosylation end products: a possible mechanism of pericyte loss in diabetic microangiopathy. Biochem. Biophys. Res. Commun. 213, 681-687
12. Cogan, D. G., Toussaint, D. and Kuwabara, T. (1961) Retinal vascular patterns. IV. Diabetic retinopathy. Arch. Ophthalmol. 66, 366-378
13. Yan, S. D., Schmidt, A. M., Anderson, G. M., Zhang, J., Brett, J., Zou, Y. S., Pinsky, D. and Stern, D. (1994) Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J. Biol. Chem. 269, 9889-9897
14. ras-dependent mitogen-activated protein kinase pathway regulated by oxidant stress. J. Biol. Chem. 272, 17810-17814
15. Tanaka, N., Yonekura, H., Yamagishi, S., Fujimori, H., Yamamoto, Y. and Yamamoto, H. (2000) The receptor for advanced glycation end products is induced by the glycation products themselves and tumor necrosis factor-α through nuclear factor-κB, and by 17β-estradiol through Sp-1 in human vascular endothelial cells. J. Biol. Chem. 275, 25781-25790
16. Yamamoto, Y., Kato, I., Doi, T., Yonekura, H., Ohashi, S., Takeuchi, M., Watanabe, T., Yamagishi, S., Sakurai, S., Takasawa, S. et al. (2001) Development and prevention of advanced diabetic nephropathy in RAGE-overexpressing mice. J. Clin. Invest. 108, 261-268
17. Yamamoto, Y., Yamagishi, S., Yonekura, H., Doi, T., Tsuji, H., Kato, I., Takasawa, S., Okamoto, H., Abedin, J., Tanaka, N. et al. (2000) Roles of the AGE-RAGE system in vascular injury in diabetes. Ann. N.Y. Acad. Sci. 902, 163-170
18. Takahashi, K., Sawasaki, Y., Hata, J., Mukai, K. and Goto, T. (1990) Spontaneous transformation and immortalization of human endothelial cells. In Vitro Cell. Dev. Biol. 25, 265-274
19. Bag, J. and Sarkar, S. (1975) Cytoplasmic nonpolysomal messenger ribonucleoprotein containing actin messenger RNA in chicken embryonic muscles Biochemistry 14, 3800-3807
20. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
21. Tarentino, A. L., Gomez, C. M. and Plummer, Jr, T. H. (1985) Deglycosylation of asparagine-linked glycans by peptide: N-glycosidase F. Biochemistry 24, 4665-4671
22. Harada, M., Itoh, H., Nakagawa, O., Ogawa, Y., Miyamoto, Y., Kuwahara, K., Ogawa, E., Igaki, T., Yamashita, J., Masudar I. et al. (1997) Significance of ventricular myocytes and nonmyocytes interaction during cardiocyte hypertrophy: evidence for endothelin-1 as a paracrine hypertrophic factor from cardiac nonmyocytes. Circulation 96, 3737-3744
23. Takeuchi, M. and Makita, Z. (2000) Alternative routes for the formation of immunochemically distinct advanced glycation end-products in vivo. Curr. Mol. Med. 1, 305-315
24. Takeuchi, M., Makita, Z., Bucala, R., Suzuki, T., Koike, T. and Kameda, Y. (2000) Immunological evidence that non-carboxymethyllysine advanced glycation end-products are produced from short chain sugars and dicarbonyl compounds in vivo, Mol. Med. 6, 114-125
25. Nomura, M., Yamagishi, S., Harada, S., Hayashi, Y., Yamashima, T., Yamashita, J. and Yamamoto, H. (1995) Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J. Biol. Chem. 270, 28316-28324
26. Yonekura, H., Sakurai, S., Liu, X., Migita, H., Wang, H., Yamagishi, S., Nomura, M., Abedin, Md. J., Unoki, H., Yamamoto, Y. et al. (1999) Placenta growth factor and vascular endothelial growth factor B and C expression in microvascular endothelial cells and pericytes. Implication in autocrine and paracrine regulation of angiogenesis. J. Biol. Chem. 274, 35172-35178
27. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63
28. Akaogi, K., Okabe, Y., Sato, J., Nagashima, Y., Yasumitsu, H., Sugahara, K. and Miyazaki, K. (1996) Specific accumulation of tumor-derived adhesion factor in tumor blood vessels and in capillary tube-like structures of cultured vascular endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 93, 8384-8389
29. Kim, K.-Y., Jeong, S.-Y., Won, J., Ryu, P.-D. and Nam, M.-J. (2001) Induction of angiogenesis by expression of soluble type II transforming growth factor-β receptor in mouse hepatoma. J. Biol. Chem. 276, 38781-38786
30. Tusnady, G. E. and Simon, I. (1998) Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. Mol. Biol. 283, 489-506
31. Treins, C., Giorgetti-Perardi, S., Murdaca, J. and Van Obberghen, E. (2001) Regulation of vascular endothelial growth factor expression by advanced glycation end products. J. Biol. Chem. 276, 43836-43841
32. Hori, O., Brett, J., Slattery, T., Cao, R., Zhang, J., Chen, J., Nagashima, M., Lundh, E. R., Vijay, S., Nitecki, D. et al. (1995) The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of rage and amphoterin in the developin9 nervous system. J. Biol. Chem. 270, 25752-25761
33. Yan, S. D., Chen, X., Fu, J., Chen, M., Zhu, H., Roher, A., Slattery, T., Zhao, L., Nagashima, M., Morser, J. et al. (1996) RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature (London) 382, 685-691
34. Yamagishi, S., Yamamoto, Y., Harada, S., Hsu, C.-C. and Yamamoto, H. (1996) Advanced glycosylation end products stimulate the growth but inhibit the prostacyclin-producing ability of endothelial cells through interactions with their receptors. FEBS Lett. 384, 103-106
35. Schmidt, A. M., Hasu, M., Popov, D., Zhang, J. H., Chen, J., Yan, S. D., Brett, J., Cao, R., Kuwabara, K., Costache, G. et al. (1994) Receptor for advanced glycation end products (AGEs) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. Proc. Natl. Acad. Sci. U.S.A. 91, 8807-8811
36. Wautier, J. L., Zoukourian, C., Chappey, O., Wautier, M. P., Guillausseau, P. J., Cao, R., Hori, O., Stern, D. and Schmidt, A. M. (1996) Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy. Soluble receptor for advanced glycation end products blocks hyperpermeability in diabetic rats. J. Clin. Invest. 97, 238-243
37. Tsuji, H., Iehara, N., Masegi, T., Imura, M., Ohkawa, J., Arai, H., Ishii, K., Kita, T. and Doi, T. (1998) Ribozyme targeting of receptor for advanced glycation end products in mouse mesangial cells. Biochem. Biophys. Res. Commun. 245, 583-588
38. Park, L., Raman, K. G., Lee, K. J., Lu, Y., Ferran, Jr, L. J., Chow, W. S., Stern, D. and Schmidt, A. M. (1998) Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat. Med. 4, 1025-1031
39. Schmidt, A. M., Hori, O., Chen, J. X., Li, J. F., Crandall, J., Zhang, J., Cao, R., Yan, S. D., Brett, J. and Stern, D. (1995) Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes. J. Clin. Invest. 96, 1395-1403
40. Malherbe, P., Richards, J. G., Galliard, H., Thompson, A., Diener, C., Schuler, A. and Huber, G. (1999) cDNA cloning of a novel secreted isoform of the human receptor for advanced glycation end products and characterization of cells co-expressing cell-surface scavenger receptors and Swedish mutant amyloid precursor protein. Brain Res. Mol. Brain Res. 71, 159-170
41. ε-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modurate gene expression. J. Biol. Chem. 274, 31740-31749
42. Sugaya, K., Fukagawa, T., Matsumoto, K., Mita, K., Takahashi, E., Ando, A., Inoko, H. and Ikemura, T. (1994) Three genes in the human MHC class III region near the junction with the class II: gene for receptor of advanced glycosylation end products, PBX2 homeobox gene and a notch homolog, human counterpart of mouse mammary tumor gene int-3. Genomics 23, 408-419