Cellular basis of diabetic nephropathy: V. Endoglin expression levels and diabetic nephropathy risk in patients with Type 1 diabetes

Journal of Diabetes and its Complications

Volumn 24, Issue 4, 2010, Pages 242-249

  Alvarez Muñoz, Patricia ^a   Mauer, Michael ^b,c   Kim, Youngki ^c   Rich, Stephen S ^d   Miller, Michael E ^e   Russell, Gregory B ^e   Lopez Novoa, José M ^a   Caramori, M Luiza ^b,c  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

^e WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Diabetic nephropathy; Endoglin; Type 1 diabetes

Indexed keywords

ENDOGLIN; HEMOGLOBIN A1C; MESSENGER RNA;

ADULT; AGE; ALBUMINURIA; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DIABETIC NEPHROPATHY; DISEASE DURATION; ELECTRON MICROSCOPY; FEMALE; GENDER; GLOMERULUS FILTRATION RATE; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY BIOPSY; MALE; MESANGIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEINURIA; REAL TIME POLYMERASE CHAIN REACTION; SKIN BIOPSY; SKIN FIBROBLAST; WESTERN BLOTTING;

ADULT; ANTIGENS, CD; CELLS; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; DISEASE PROGRESSION; FEMALE; FIBROBLASTS; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, CELL SURFACE; RISK FACTORS; SKIN;

EID: 77953024536     PISSN: 10568727     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jdiacomp.2009.03.004     Document Type: Article

References (55)

1. Affymetrix Microarray Suite User's Guide Version 5.0. Affymetrix Microarray Suite User's Guide, Version 5.0 (2001) 412-415 Santa Clara, CA
2. Almasy L., and Blangero J. Multipoint quantitative-trait linkage analysis in general pedigrees. American Journal of Human Genetics 62 5 (1998) 1198-1211
3. Barbara N.P., Wrana J.L., and Letarte M. Endoglin is an accessory protein that interacts with the signaling receptor complex of multiple members of the transforming growth factor-beta superfamily. Journal of Biological Chemistry 274 2 (1999) 584-594
4. Border W.A., and Noble N. Cytokines in kidney disease: the role of transforming growth factor beta. American Journal of Kidney Disease 22 1 (1993) 105-113
5. Border W.A., and Ruoslahti E. Transforming growth factor-beta in disease: the dark side of tissue repair. Journal of Clinical Investigation 90 1 (1992) 1-7
6. Caramori M.L., Fioretto P., and Mauer M. Low glomerular filtration rate in normo-albuminuric Type 1 diabetic patients: an indicator of more advanced glomerular lesions. Diabetes 52 4 (2003) 1036-1040
7. Caramori M.L., Kim Y., Fioretto P., Huang C., Rich S.S., Miller M.E., Russell G.B., and Mauer M. Cellular basis of diabetic nephropathy: IV. Antioxidant enzyme mRNA expression levels in skin fibroblasts of Type 1 diabetic sibling pairs. Nephrology and Dialysis Transplantation 21 11 (2006) 3122-3126
8. Caramori M.L., Kim Y., Huang C., Fish A.J., Rich S.S., Miller M.E., Russell G., and Mauer M. Cellular basis of diabetic nephropathy: 1. Study design and renal structural-functional relationships in patients with long-standing diabetes. Diabetes 51 2 (2002) 506-513
9. Ceriello A., Morocutti A., Mercuri F., Quagliaro L., Moro M., Damante G., and Viberti G.C. Defective intracellular antioxidant enzyme production in Type 1 diabetic patients with nephropathy. Diabetes 49 12 (2000) 2170-2177
10. Cheifetz S., Bellon T., Cales C., Vera S., Bernabeu C., Massagué J., and Letarte M. Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. Journal of Biological Chemistry 267 27 (1992) 19027-19030
11. Diez-Marques L., Ortega-Velazquez R., Langa C., Rodriguez-Barbero A., Lopez-Novoa J.M., Lamas S., and Bernabeu C. Expression of endoglin in human mesangial cells: Modulation of extracellular matrix synthesis. Biochimica et Biophysica Acta 1587 1 (2002) 36-44
12. Ellis E.N., Steffes M.W., Goetz F.C., Sutherland D.E.R., and Mauer S.M. Glomerular filtration surface in type I diabetes mellitus. Kidney International 29 4 (1986) 889-894
13. Ewens K.G., George R.A., Sharma K., Ziyadeh F.N., and Spielman R.S. Assessment of 115 candidate genes for diabetic nephropathy by transmission/dis-equilibrium test. Diabetes 54 11 (2005) 3305-3318
14. Fioretto P., Steffes M.W., B osa J., Rich S.S., Miller M.E., and Mauer M. Is diabetic nephropathy inherited? Studies of glomerular structure in Type 1 diabetic sibling pairs. Diabetes 48 4 (1999) 865-869
15. Fioretto P., Steffes M.W., and Mauer M. Glomerular structure in nonproteinuric IDDM patients with various levels of albuminuria. Diabetes 43 11 (1994) 1358-1364
16. Guerrero-Esteo M., Lastres P., Letamendia A., Perez-Alvarez M.J., Langa C., Lopez L.A., Fabra A., Garcia-Pardo A., Vera S., Letarte M., and Bernabeu C. Endoglin overexpression modulates cellular morphology, migration, and adhesion of mouse fibroblasts. European Journal of Cell Biology 78 9 (1999) 614-623
17. Guerrero-Esteo M., Sanchez-Elsner T., Letamendia A., and Bernabeu C. Extracellular and cytoplasmic domains of endoglin interact with the transforming growth factor-beta receptors I and II. Journal of Biological Chemistry 277 32 (2002) 29197-29209
18. Hochberg Y. A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75 4 (1988) 800-803
19. Huang C., Kim Y., Caramori M.L., Fish A.J., Rich S.S., Miller M.E., Russell G.B., and Mauer M. Cellular basis of diabetic nephropathy: III. In vitro GLUT1 mRNA expression and risk of diabetic nephropathy in Type 1 diabetic patients. Diabetologia 47 10 (2004) 1789-1794
20. Huang C., Kim Y., Caramori M.L., Moore J.H., Rich S.S., Mychaleckyj J.C., Walker P.C., and Mauer M. Diabetic nephropathy is associated with gene expression levels of oxidative phosphorylation and related pathways. Diabetes 55 6 (2006) 1826-1831
21. Huang C., Kim Y., Caramori M.L.A., Fish A.J., Rich S.S., Miller M.E., Russell G., and Mauer M. Cellular basis of diabetic nephropathy II. The TGF-system and diabetic nephropathy lesions in Type 1 diabetes. Diabetes 51 12 (2002) 3577-3581
22. Iori E., Marescotti M.C., Vedovato M., Ceolotto G., Avogaro A., Tiengo A., Del Prato S., and Trevisan R. In situ protein Kinase C activity is increased in cultured fibroblasts from Type 1 diabetic patients with nephropathy. Diabetologia 46 4 (2003) 524-530
23. Krolewski A.S. Genetics of diabetic nephropathy: evidence for major and minor gene effects. Kidney International 55 4 (1999) 1582-1596
24. Lastres P., Letamendia A., Zhang H., Rius C., Almendro N., Raab U., Lopez L.A., Langa C., Fabra A., Letarte M., and Bernabeu C. Endoglin modulates cellular responses to TGF-beta 1. Journal of Cell Biology 133 5 (1996) 1109-11021
25. Letamendia A., Lastres P., Botella L.M., Raab U., Langa C., Valasco B., Attisano L., and Bernabeu C. Role of endoglin in cellular responses to transforming growth factor-beta. A comparative study with betaglycan. Journal of Biological Chemistry 273 49 (1998) 33011-33019
26. Levine R.J., Lam C., Qian C., Yu K.F., Maynard S.E., Sachs B.P., Sibai B.M., Epstein F.H., Romero R., Thadhani R., Karumanchi S.A., and CPEP Study Group. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. New England Journal of Medicine 355 10 (2006) 992-1005
27. Li D., Chen H., and Mehta J.L. Angiotensin II via activation of Type 1 receptor upregulates expression of endoglin in human coronary artery endothelial cells. Hypertension 38 5 (2001) 1062-1067
28. Llorca O., Trujillo A., Blanco F.J., and Bernabeu C. Structural model of human endoglin, a transmembrane receptor responsible for hereditary hemorrhagic telangiectasia. Journal of Molecular Biology 65 3 (2007) 694-705
29. Luque A., Cabanas C., Raab U., Letamendia A., Paez E., Herreros L., Sanchez-Madrid F., and Bernabeu C. The use of recombinant vaccinia virus to generate monoclonal antibodies against the cell-surface glycoprotein endoglin. FEBS Letters 413 2 (1997) 265-268
30. Lurbe A., Fioretto P., Mauer M., LaPointe M.S., and Batlle D. Growth phenotype of cultured skin fibroblasts from IDDM patients with and without nephropathy and overactivity of the Na+/H+ antiporter. Kidney International 50 5 (1996) 1684-1693
31. Massagué J. TGF-beta signal transduction. Annual Review of Biochemistry 67 (1998) 753-791
32. McAllister K.A., Grogg K.M., Johnson D.W., Gallione C.J., Baldwin M.A., Jackson C.E., Helmbold E.A., Markel D.S., McKinnon W.C., Murrell J., McCormick M.K., Pericak-Vance M.A., Heutink P., Oostra B.A., Haitjema T., Westerman C.J.J., Porteous M.E., Guttmacher A.E., Letarte M., and Marchuk D.A. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia Type 1. Nature Genetics 8 4 (1994) 345-351
33. McKnight A.J., Maxwell A.P., Sawcer S., Compston A., Setakis E., Patterson C.C., Brady H.R., and Savage D.A. A genome-wide DNA microsatellite association screen to identify chromosomal regions harboring candidate genes in diabetic nephropathy. Journal of the American Society of Nephrology 17 3 (2006) 831-836
34. Obreo J., Diez-Marques L., Lamas S., Duwell A., Eleno N., Bernabeu C., Pandiella A., Lopez-Novoa J.M., and Rodriguez-B ero A. Endoglin expression regulates basal and TGF-beta1-induced extracellular matrix synthesis in cultured L6E9 myoblasts. Cellular Physiology and Biochemistry 14 4-6 (2004) 301-310
35. Osterholm A.M., He B., Pitkaniemi J., Albinsson L., Berg T., Sarti C., Tuomilehto J., and Tryggvason K. Genome-wide scan for Type 1 diabetic nephropathy in the Finnish population reveals suggestive linkage to a single locus on chromosome 3q. Kidney International 71 2 (2007) 140-145
36. Pérez-Gómez E., Eleno N., López-Novoa J.M., Ramirez J.R., Velasco B., Letarte M., Bernabéu C., and Quintanilla M. Characterization of murine S-endoglin isoform and its effects on tumor development. Oncogene 24 27 (2005) 4450-4461
37. Prieto M., Rodriguez-Pena A., Arevalo M., Rivas J.V., Duwel A., Eleno N., Sanchez R.J., Morales A.I., Lopez-Novoa J.M., and Perez-Barriocanal F. Effect of the long-term treatment with trandolapril on endoglin expression in rats with experimental renal fibrosis induced by renal mass reduction. Kidney Blood Pressure Research 28 1 (2005) 32-40
38. Prieto M., Rodríguez-Peña A.B., Düwel A., Rivas J.V., Docherty N., Perez-Barriocanal F., Arevalo M., Vary C.P., Bernabeu C., Lopez-Novoa J.M., and Eleno N. Temporal changes in renal endoglin and TGF-beta 1 expression following ureteral obstruction in rats. Journal of Physiological Biochemistry 6 3 (2005) 457-467
39. Rich S.S. Genetics of diabetes and its complications. Journal of the American Society of Nephrology 17 2 (2006) 353-360
40. Roberts A.B., McCune B.K., and Sporn M.B. TGF-beta: regulation of extracellular matrix. Kidney International 41 3 (1992) 557-559
41. Rodriguez-B ero A., Obreo J., Alvarez-Munoz P., Pandiella A., Bernabeu C., and Lopez-Novoa J.M. Endoglin modulation of TGF-beta1-induced collagen synthesis is dependent on ERK1/MAPK activation. Cellular Physiology and Biochemistry 18 1-3 (2006) 135-142
42. Rodriguez-B ero A., Obreo J., Eleno N., Rodriguez A., Bernabeu C., and Lopez-Novoa J.M. Endoglin expression in human and rat mesangial cells and its upregulation by TGF-beta 1. Biochemical and Biophysical Research Communications 282 1 (2001) 142-147
43. Rodriguez-Peña A., Eleno N., Duwell A., Arevalo M., Perez-Barriocanal F., Flores O., Docherty N., Bernabeu C., Letarte M., and Lopez-Novoa J.M. Endoglin upregulation during experimental renal interstitial fibrosis in mice. Hypertension 40 5 (2002) 713-720
44. Rodriguez-Peña A., Prieto M., Duwel A., Rivas J.V., Eleno N., Perez-Barriocanal F., Arevalo M., Smith J.D., Vary C.P., Bernabeu C., and Lopez-Novoa J.M. Up-regulation of endoglin, a TGF-beta-binding protein in rats with experimental renal fibrosis induced by renal mass reduction. Nephrology and Dialysis Transplantation 16 Suppl 1 (2001) 34-39
45. Roy-Chaudhury P., Simpson J.G., and Power D.A. Endoglin, a transforming growth factor-beta-binding protein, is upregulated in chronic progressive renal disease. Experimenal Nephrology 5 1 (1997) 55-60
46. Schnaper H.W., Hayashida T., and Poncelet A.C. It's a Smad world: regulation of TGF-beta signaling in the kidney. Journal of the American Society of Nephrology 13 4 (2002) 1126-1128
47. Sharma K., and Ziyadeh F.N. Renal hypertrophy is associated with upregulation of TGF-beta 1 gene expression in diabetic BB rat and NOD mouse. American Journal of Physiology 267 6 Pt 2 (1994) F1094-F1101
48. + exchanger isoform-1 abundance in skin fibroblasts of type I diabetic patients with nephropathy. Metabolism 44 6 (1995) 791-795
49. Tessari P., Puricelli L., Iori E., Arrigoni G., Vedovato M., James P., Coracina A., and Millioni R. Altered chaperone and protein turnover regulators expression in cultured skin fibroblasts from Type 1 diabetes mellitus with nephropathy. Journal of Proteome Research 6 3 (2007) 976-986
50. Torbjörnsdotter T.B., Perrin N.E., Jaremko G.A., and Berg U.B. Widening of foot processes in normoalbuminuric adolescents with Type 1 diabetes. Pediatric Nephrology 20 6 (2005) 750-758
51. Trevisan R., Fioretto P., B osa J., and Mauer M. Insulin-dependent diabetic sibling pairs are concordant for sodium-hydrogen antiport activity. Kidney International 55 6 (1999) 2383-2389
52. Trevisan R., Yip J., Sarika L., Li L.K., and Viberti G. Enhanced collagen synthesis in cultured skin fibroblasts from insulin-dependent diabetic patients with nephropathy. Journal of the American Society of Nephrology 8 7 (1997) 1133-1139
53. Velasco S., Alvarez-Muñoz P., Pericacho M., Dijke P.T., Bernabéu C., López-Novoa J.M., and Rodríguez-B ero A. l- and S-endoglin differentially modulate TGFbeta1 signaling mediated by ALK1 and ALK5 in L6E9 myoblasts. Journal of Cell Science 121 Pt 6 (2008) 913-919
54. Venkatesha S., Toporsian M., Lam C., Hanai J., Mammoto T., Kim Y.M., Bdolah Y., Lim K.H., Yuan H.T., Libermann T.A., Stillman I.E., Roberts D., D'Amore P.A., Epstein F.H., Sellke F.W., Romero R., Sukhatme V.P., Letarte M., and Karumanchi S.A. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nature Medicine 12 6 (2006) 642-649
55. Zhu Y., Usui H.K., and Sharma K. Regulation of transforming growth factor beta in diabetic nephropathy: Implications for treatment. Seminars in Nephrology 27 2 (2007) 153-160