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Published in: Clinical and Experimental Nephrology 5/2009

01-10-2009 | Review Article

Historical chronology of basic and clinical research in diabetic nephropathy and contributions of Japanese scientists

Authors: Jun Wada, Hirofumi Makino

Published in: Clinical and Experimental Nephrology | Issue 5/2009

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Abstract

The most problematic issue in clinical nephrology worldwide is the relentless and progressive increase in patients with end-stage renal disease (ESRD). Diabetic nephropathy has considerable impact on society in the areas of public health and social economy; many scientists are involved in research for the elucidation of the pathogenesis of diabetic nephropathy and for the prevention and cure of the disease. In contrast, diabetic nephropathy was a neglected or ignored disease in the historical era, and few dedicated physicians recognized the disease process of diabetic nephropathy. In this review, we look back on the history of basic and clinical research on diabetic nephropathy and survey the recent progress of the research, especially focusing on the contribution of Japanese scientists.
Literature
1.
go back to reference Imai E, Horio M, Iseki K, Yamagata K, Watanabe T, Hara S, et al. Prevalence of chronic kidney disease (CKD) in the Japanese general population predicted by the MDRD equation modified by a Japanese coefficient. Clin Exp Nephrol. 2007;11(2):156–63.CrossRefPubMed Imai E, Horio M, Iseki K, Yamagata K, Watanabe T, Hara S, et al. Prevalence of chronic kidney disease (CKD) in the Japanese general population predicted by the MDRD equation modified by a Japanese coefficient. Clin Exp Nephrol. 2007;11(2):156–63.CrossRefPubMed
2.
go back to reference Imai E, Horio M, Nitta K, Yamagata K, Iseki K, Hara S, et al. Estimation of glomerular filtration rate by the MDRD study equation modified for Japanese patients with chronic kidney disease. Clin Exp Nephrol. 2007;11(1):41–50.CrossRefPubMed Imai E, Horio M, Nitta K, Yamagata K, Iseki K, Hara S, et al. Estimation of glomerular filtration rate by the MDRD study equation modified for Japanese patients with chronic kidney disease. Clin Exp Nephrol. 2007;11(1):41–50.CrossRefPubMed
3.
go back to reference Wu AY, Kong NC, de Leon FA, Pan CY, Tai TY, Yeung VT, et al. An alarmingly high prevalence of diabetic nephropathy in Asian type 2 diabetic patients: the MicroAlbuminuria Prevalence (MAP) study. Diabetologia. 2005;48(1):17–26.CrossRefPubMed Wu AY, Kong NC, de Leon FA, Pan CY, Tai TY, Yeung VT, et al. An alarmingly high prevalence of diabetic nephropathy in Asian type 2 diabetic patients: the MicroAlbuminuria Prevalence (MAP) study. Diabetologia. 2005;48(1):17–26.CrossRefPubMed
4.
go back to reference Parving HH, Lewis JB, Ravid M, Remuzzi G, Hunsicker LG. Prevalence and risk factors for microalbuminuria in a referred cohort of type II diabetic patients: a global perspective. Kidney Int. 2006;69(11):2057–63.CrossRefPubMed Parving HH, Lewis JB, Ravid M, Remuzzi G, Hunsicker LG. Prevalence and risk factors for microalbuminuria in a referred cohort of type II diabetic patients: a global perspective. Kidney Int. 2006;69(11):2057–63.CrossRefPubMed
6.
7.
go back to reference Bright R. Cases and observations illustrative of renal disease accompanied with the secretion of albuminous urine. Guy’s Hosp Rep. 1836;1:336. Bright R. Cases and observations illustrative of renal disease accompanied with the secretion of albuminous urine. Guy’s Hosp Rep. 1836;1:336.
10.
go back to reference Murakami R. Beitrag zum Kennttniss der Veranderung des Nierenkorperchens beim diabetes mellitus. Trans Soc Path Jpn. 1936;26:657. Murakami R. Beitrag zum Kennttniss der Veranderung des Nierenkorperchens beim diabetes mellitus. Trans Soc Path Jpn. 1936;26:657.
11.
go back to reference Spuhler O, Zollinger HU. Die diabetische glomerulosklerose. Deutsch Arch Klin Med. 1943;190:321. Spuhler O, Zollinger HU. Die diabetische glomerulosklerose. Deutsch Arch Klin Med. 1943;190:321.
12.
go back to reference Gellman DD, Pirani CL, Soothill JF, Muehrcke RC, Kark RM. Diabetic nephropathy: a clinical and pathologic study based on renal biopsies. Medicine (Baltimore). 1959;38:321–67.CrossRef Gellman DD, Pirani CL, Soothill JF, Muehrcke RC, Kark RM. Diabetic nephropathy: a clinical and pathologic study based on renal biopsies. Medicine (Baltimore). 1959;38:321–67.CrossRef
13.
go back to reference Gellman DD, Pirani CL, Soothill JF, Muehrcke RC, Maduros W, Kark RM. Structure and function in diabetic nephropathy; the importance of diffuse glomerulosclerosis. Diabetes. 1959;8(4):251–6.CrossRefPubMed Gellman DD, Pirani CL, Soothill JF, Muehrcke RC, Maduros W, Kark RM. Structure and function in diabetic nephropathy; the importance of diffuse glomerulosclerosis. Diabetes. 1959;8(4):251–6.CrossRefPubMed
14.
go back to reference Østerby R, Gundersen HJ. Glomerular size and structure in diabetes mellitus. I. Early abnormalities. Diabetologia. 1975;11(3):225–9.CrossRefPubMed Østerby R, Gundersen HJ. Glomerular size and structure in diabetes mellitus. I. Early abnormalities. Diabetologia. 1975;11(3):225–9.CrossRefPubMed
15.
go back to reference Mogensen CE, Christensen CK, Vittinghus E. The stages in diabetic renal disease. With emphasis on the stage of incipient diabetic nephropathy. Diabetes. 1983;32(Suppl 2):64–78.CrossRefPubMed Mogensen CE, Christensen CK, Vittinghus E. The stages in diabetic renal disease. With emphasis on the stage of incipient diabetic nephropathy. Diabetes. 1983;32(Suppl 2):64–78.CrossRefPubMed
16.
go back to reference Nakamoto Y, Takazakura E, Hayakawa H, Kawai K, Dohi K, Fujioka M, et al. Intrarenal microaneurysms in diabetic nephropathy. Lab Invest. 1980;42(4):433–9.PubMed Nakamoto Y, Takazakura E, Hayakawa H, Kawai K, Dohi K, Fujioka M, et al. Intrarenal microaneurysms in diabetic nephropathy. Lab Invest. 1980;42(4):433–9.PubMed
17.
go back to reference Saito Y, Kida H, Takeda S, Yoshimura M, Yokoyama H, Koshino Y, et al. Mesangiolysis in diabetic glomeruli: its role in the formation of nodular lesions. Kidney Int. 1988;34(3):389–96.CrossRefPubMed Saito Y, Kida H, Takeda S, Yoshimura M, Yokoyama H, Koshino Y, et al. Mesangiolysis in diabetic glomeruli: its role in the formation of nodular lesions. Kidney Int. 1988;34(3):389–96.CrossRefPubMed
18.
go back to reference Yajima G. A histopathological study on diabetic nephropathy—light and electron microscopic observations. Acta Pathol Jpn. 1976;26(1):47–62.PubMed Yajima G. A histopathological study on diabetic nephropathy—light and electron microscopic observations. Acta Pathol Jpn. 1976;26(1):47–62.PubMed
19.
go back to reference Nishi S, Ueno M, Hisaki S, Iino N, Iguchi S, Oyama Y, et al. Ultrastructural characteristics of diabetic nephropathy. Med Electron Microsc. 2000;33(2):65–73.CrossRefPubMed Nishi S, Ueno M, Hisaki S, Iino N, Iguchi S, Oyama Y, et al. Ultrastructural characteristics of diabetic nephropathy. Med Electron Microsc. 2000;33(2):65–73.CrossRefPubMed
20.
go back to reference Hayashi H, Karasawa R, Inn H, Saitou T, Ueno M, Nishi S, et al. An electron microscopic study of glomeruli in Japanese patients with non-insulin dependent diabetes mellitus. Kidney Int. 1992;41(4):749–57.CrossRefPubMed Hayashi H, Karasawa R, Inn H, Saitou T, Ueno M, Nishi S, et al. An electron microscopic study of glomeruli in Japanese patients with non-insulin dependent diabetes mellitus. Kidney Int. 1992;41(4):749–57.CrossRefPubMed
21.
go back to reference Suzuki Y, Ueno M, Hayashi H, Nishi S, Satou H, Karasawa R, et al. A light microscopic study of glomerulosclerosis in Japanese patients with noninsulin-dependent diabetes mellitus: the relationship between clinical and histological features. Clin Nephrol. 1994;42(3):155–62.PubMed Suzuki Y, Ueno M, Hayashi H, Nishi S, Satou H, Karasawa R, et al. A light microscopic study of glomerulosclerosis in Japanese patients with noninsulin-dependent diabetes mellitus: the relationship between clinical and histological features. Clin Nephrol. 1994;42(3):155–62.PubMed
22.
go back to reference Ota Z, Shikata K, Ota K. Nephrotic tunnels in glomerular basement membrane as revealed by a new electron microscopic method. J Am Soc Nephrol. 1994;4(12):1965–73.PubMed Ota Z, Shikata K, Ota K. Nephrotic tunnels in glomerular basement membrane as revealed by a new electron microscopic method. J Am Soc Nephrol. 1994;4(12):1965–73.PubMed
23.
go back to reference Hironaka K, Makino H, Yamasaki Y, Ota Z. Renal basement membranes by ultrahigh resolution scanning electron microscopy. Kidney Int. 1993;43(2):334–45.CrossRefPubMed Hironaka K, Makino H, Yamasaki Y, Ota Z. Renal basement membranes by ultrahigh resolution scanning electron microscopy. Kidney Int. 1993;43(2):334–45.CrossRefPubMed
24.
go back to reference Makino H, Yamasaki Y, Haramoto T, Shikata K, Hironaka K, Ota Z, et al. Ultrastructural changes of extracellular matrices in diabetic nephropathy revealed by high resolution scanning and immunoelectron microscopy. Lab Invest. 1993;68(1):45–55.PubMed Makino H, Yamasaki Y, Haramoto T, Shikata K, Hironaka K, Ota Z, et al. Ultrastructural changes of extracellular matrices in diabetic nephropathy revealed by high resolution scanning and immunoelectron microscopy. Lab Invest. 1993;68(1):45–55.PubMed
25.
go back to reference Moriya T, Ohno S, Nakazawa K, Shigematsu H, Yajima Y. Ultrastructural study of glomerular basement membrane in diabetic rats by quick-freezing and deep-etching method. Virchows Arch B Cell Pathol Incl Mol Pathol. 1993;64(2):107–14.CrossRefPubMed Moriya T, Ohno S, Nakazawa K, Shigematsu H, Yajima Y. Ultrastructural study of glomerular basement membrane in diabetic rats by quick-freezing and deep-etching method. Virchows Arch B Cell Pathol Incl Mol Pathol. 1993;64(2):107–14.CrossRefPubMed
26.
go back to reference Moriya T, Ohno S, Tanaka K, Fujita Y. Clinical applications of the quick-freezing and deep-etching method to human diabetic nephropathy. J Electron Microsc (Tokyo). 2006;55(2):69–73.CrossRef Moriya T, Ohno S, Tanaka K, Fujita Y. Clinical applications of the quick-freezing and deep-etching method to human diabetic nephropathy. J Electron Microsc (Tokyo). 2006;55(2):69–73.CrossRef
27.
go back to reference Suzuki D, Miyazaki M, Jinde K, Koji T, Yagame M, Endoh M, et al. In situ hybridization studies of matrix metalloproteinase-3, tissue inhibitor of metalloproteinase-1 and type IV collagen in diabetic nephropathy. Kidney Int. 1997;52(1):111–9.CrossRefPubMed Suzuki D, Miyazaki M, Jinde K, Koji T, Yagame M, Endoh M, et al. In situ hybridization studies of matrix metalloproteinase-3, tissue inhibitor of metalloproteinase-1 and type IV collagen in diabetic nephropathy. Kidney Int. 1997;52(1):111–9.CrossRefPubMed
28.
go back to reference Suzuki D, Miyazaki M, Naka R, Koji T, Yagame M, Jinde K, et al. In situ hybridization of interleukin 6 in diabetic nephropathy. Diabetes. 1995;44(10):1233–8.CrossRefPubMed Suzuki D, Miyazaki M, Naka R, Koji T, Yagame M, Jinde K, et al. In situ hybridization of interleukin 6 in diabetic nephropathy. Diabetes. 1995;44(10):1233–8.CrossRefPubMed
29.
go back to reference Toyoda M, Suzuki D, Honma M, Uehara G, Sakai T, Umezono T, et al. High expression of PKC-MAPK pathway mRNAs correlates with glomerular lesions in human diabetic nephropathy. Kidney Int. 2004;66(3):1107–14.CrossRefPubMed Toyoda M, Suzuki D, Honma M, Uehara G, Sakai T, Umezono T, et al. High expression of PKC-MAPK pathway mRNAs correlates with glomerular lesions in human diabetic nephropathy. Kidney Int. 2004;66(3):1107–14.CrossRefPubMed
30.
go back to reference Kikkawa R, Umemura K, Haneda M, Arimura T, Ebata K, Shigeta Y. Evidence for existence of polyol pathway in cultured rat mesangial cells. Diabetes. 1987;36(2):240–3.CrossRefPubMed Kikkawa R, Umemura K, Haneda M, Arimura T, Ebata K, Shigeta Y. Evidence for existence of polyol pathway in cultured rat mesangial cells. Diabetes. 1987;36(2):240–3.CrossRefPubMed
31.
go back to reference Haneda M, Araki S, Togawa M, Sugimoto T, Isono M, Kikkawa R. Mitogen-activated protein kinase cascade is activated in glomeruli of diabetic rats and glomerular mesangial cells cultured under high glucose conditions. Diabetes. 1997;46(5):847–53.CrossRefPubMed Haneda M, Araki S, Togawa M, Sugimoto T, Isono M, Kikkawa R. Mitogen-activated protein kinase cascade is activated in glomeruli of diabetic rats and glomerular mesangial cells cultured under high glucose conditions. Diabetes. 1997;46(5):847–53.CrossRefPubMed
32.
go back to reference Koya D, Haneda M, Nakagawa H, Isshiki K, Sato H, Maeda S, et al. Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC beta inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J. 2000;14(3):439–47.CrossRefPubMed Koya D, Haneda M, Nakagawa H, Isshiki K, Sato H, Maeda S, et al. Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC beta inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J. 2000;14(3):439–47.CrossRefPubMed
33.
go back to reference Isshiki K, Haneda M, Koya D, Maeda S, Sugimoto T, Kikkawa R. Thiazolidinedione compounds ameliorate glomerular dysfunction independent of their insulin-sensitizing action in diabetic rats. Diabetes. 2000;49(6):1022–32.CrossRefPubMed Isshiki K, Haneda M, Koya D, Maeda S, Sugimoto T, Kikkawa R. Thiazolidinedione compounds ameliorate glomerular dysfunction independent of their insulin-sensitizing action in diabetic rats. Diabetes. 2000;49(6):1022–32.CrossRefPubMed
34.
go back to reference Ishida T, Haneda M, Maeda S, Koya D, Kikkawa R. Stretch-induced overproduction of fibronectin in mesangial cells is mediated by the activation of mitogen-activated protein kinase. Diabetes. 1999;48(3):595–602.CrossRefPubMed Ishida T, Haneda M, Maeda S, Koya D, Kikkawa R. Stretch-induced overproduction of fibronectin in mesangial cells is mediated by the activation of mitogen-activated protein kinase. Diabetes. 1999;48(3):595–602.CrossRefPubMed
35.
go back to reference Makita Z, Radoff S, Rayfield EJ, Yang Z, Skolnik E, Delaney V, et al. Advanced glycosylation end products in patients with diabetic nephropathy. N Engl J Med. 1991;325(12):836–42.CrossRefPubMed Makita Z, Radoff S, Rayfield EJ, Yang Z, Skolnik E, Delaney V, et al. Advanced glycosylation end products in patients with diabetic nephropathy. N Engl J Med. 1991;325(12):836–42.CrossRefPubMed
36.
go back to reference Makino H, Shikata K, Hironaka K, Kushiro M, Yamasaki Y, Sugimoto H, et al. Ultrastructure of nonenzymatically glycated mesangial matrix in diabetic nephropathy. Kidney Int. 1995;48(2):517–26.CrossRefPubMed Makino H, Shikata K, Hironaka K, Kushiro M, Yamasaki Y, Sugimoto H, et al. Ultrastructure of nonenzymatically glycated mesangial matrix in diabetic nephropathy. Kidney Int. 1995;48(2):517–26.CrossRefPubMed
37.
go back to reference Horie K, Miyata T, Maeda K, Miyata S, Sugiyama S, Sakai H, et al. Immunohistochemical colocalization of glycoxidation products and lipid peroxidation products in diabetic renal glomerular lesions. Implication for glycoxidative stress in the pathogenesis of diabetic nephropathy. J Clin Invest. 1997;100(12):2995–3004.CrossRefPubMedPubMedCentral Horie K, Miyata T, Maeda K, Miyata S, Sugiyama S, Sakai H, et al. Immunohistochemical colocalization of glycoxidation products and lipid peroxidation products in diabetic renal glomerular lesions. Implication for glycoxidative stress in the pathogenesis of diabetic nephropathy. J Clin Invest. 1997;100(12):2995–3004.CrossRefPubMedPubMedCentral
38.
go back to reference Makita Z, Bucala R, Rayfield EJ, Friedman EA, Kaufman AM, Korbet SM, et al. Reactive glycosylation endproducts in diabetic uraemia and treatment of renal failure. Lancet. 1994;343(8912):1519–22.CrossRefPubMed Makita Z, Bucala R, Rayfield EJ, Friedman EA, Kaufman AM, Korbet SM, et al. Reactive glycosylation endproducts in diabetic uraemia and treatment of renal failure. Lancet. 1994;343(8912):1519–22.CrossRefPubMed
39.
go back to reference Mitsuhashi T, Nakayama H, Itoh T, Kuwajima S, Aoki S, Atsumi T, et al. Immunochemical detection of advanced glycation end products in renal cortex from STZ-induced diabetic rat. Diabetes. 1993;42(6):826–32.CrossRefPubMed Mitsuhashi T, Nakayama H, Itoh T, Kuwajima S, Aoki S, Atsumi T, et al. Immunochemical detection of advanced glycation end products in renal cortex from STZ-induced diabetic rat. Diabetes. 1993;42(6):826–32.CrossRefPubMed
40.
go back to reference Yamagishi S, Inagaki Y, Okamoto T, Amano S, Koga K, Takeuchi M, et al. Advanced glycation end product-induced apoptosis and overexpression of vascular endothelial growth factor and monocyte chemoattractant protein-1 in human-cultured mesangial cells. J Biol Chem. 2002;277(23):20309–15.CrossRefPubMed Yamagishi S, Inagaki Y, Okamoto T, Amano S, Koga K, Takeuchi M, et al. Advanced glycation end product-induced apoptosis and overexpression of vascular endothelial growth factor and monocyte chemoattractant protein-1 in human-cultured mesangial cells. J Biol Chem. 2002;277(23):20309–15.CrossRefPubMed
41.
go back to reference Yamamoto Y, Kato I, Doi T, Yonekura H, Ohashi S, Takeuchi M, et al. Development and prevention of advanced diabetic nephropathy in RAGE-overexpressing mice. J Clin Invest. 2001;108(2):261–8.CrossRefPubMedPubMedCentral Yamamoto Y, Kato I, Doi T, Yonekura H, Ohashi S, Takeuchi M, et al. Development and prevention of advanced diabetic nephropathy in RAGE-overexpressing mice. J Clin Invest. 2001;108(2):261–8.CrossRefPubMedPubMedCentral
42.
go back to reference Uesugi N, Sakata N, Horiuchi S, Nagai R, Takeya M, Meng J, et al. Glycoxidation-modified macrophages and lipid peroxidation products are associated with the progression of human diabetic nephropathy. Am J Kidney Dis. 2001;38(5):1016–25.CrossRefPubMed Uesugi N, Sakata N, Horiuchi S, Nagai R, Takeya M, Meng J, et al. Glycoxidation-modified macrophages and lipid peroxidation products are associated with the progression of human diabetic nephropathy. Am J Kidney Dis. 2001;38(5):1016–25.CrossRefPubMed
43.
go back to reference Fukuhara-Takaki K, Sakai M, Sakamoto Y, Takeya M, Horiuchi S. Expression of class A scavenger receptor is enhanced by high glucose in vitro and under diabetic conditions in vivo: one mechanism for an increased rate of atherosclerosis in diabetes. J Biol Chem. 2005;280(5):3355–64.CrossRefPubMed Fukuhara-Takaki K, Sakai M, Sakamoto Y, Takeya M, Horiuchi S. Expression of class A scavenger receptor is enhanced by high glucose in vitro and under diabetic conditions in vivo: one mechanism for an increased rate of atherosclerosis in diabetes. J Biol Chem. 2005;280(5):3355–64.CrossRefPubMed
44.
go back to reference Iwano M, Kubo A, Nishino T, Sato H, Nishioka H, Akai Y, et al. Quantification of glomerular TGF-beta 1 mRNA in patients with diabetes mellitus. Kidney Int. 1996;49(4):1120–6.CrossRefPubMed Iwano M, Kubo A, Nishino T, Sato H, Nishioka H, Akai Y, et al. Quantification of glomerular TGF-beta 1 mRNA in patients with diabetes mellitus. Kidney Int. 1996;49(4):1120–6.CrossRefPubMed
45.
go back to reference Isaka Y, Fujiwara Y, Ueda N, Kaneda Y, Kamada T, Imai E. Glomerulosclerosis induced by in vivo transfection of transforming growth factor-beta or platelet-derived growth factor gene into the rat kidney. J Clin Invest. 1993;92(6):2597–601.CrossRefPubMedPubMedCentral Isaka Y, Fujiwara Y, Ueda N, Kaneda Y, Kamada T, Imai E. Glomerulosclerosis induced by in vivo transfection of transforming growth factor-beta or platelet-derived growth factor gene into the rat kidney. J Clin Invest. 1993;92(6):2597–601.CrossRefPubMedPubMedCentral
46.
go back to reference Isaka Y, Akagi Y, Ando Y, Tsujie M, Sudo T, Ohno N, et al. Gene therapy by transforming growth factor-beta receptor-IgG Fc chimera suppressed extracellular matrix accumulation in experimental glomerulonephritis. Kidney Int. 1999;55(2):465–75.CrossRefPubMed Isaka Y, Akagi Y, Ando Y, Tsujie M, Sudo T, Ohno N, et al. Gene therapy by transforming growth factor-beta receptor-IgG Fc chimera suppressed extracellular matrix accumulation in experimental glomerulonephritis. Kidney Int. 1999;55(2):465–75.CrossRefPubMed
47.
go back to reference Haneda M, Kikkawa R, Koya D, Uzu T, Maeda S, Togawa M, et al. Alteration of mesangial response to ANP and angiotensin II by glucose. Kidney Int. 1993;44(3):518–26.CrossRefPubMed Haneda M, Kikkawa R, Koya D, Uzu T, Maeda S, Togawa M, et al. Alteration of mesangial response to ANP and angiotensin II by glucose. Kidney Int. 1993;44(3):518–26.CrossRefPubMed
48.
go back to reference Haneda M, Kikkawa R, Maeda S, Togawa M, Koya D, Horide N, et al. Dual mechanism of angiotensin II inhibits ANP-induced mesangial cGMP accumulation. Kidney Int. 1991;40(2):188–94.CrossRefPubMed Haneda M, Kikkawa R, Maeda S, Togawa M, Koya D, Horide N, et al. Dual mechanism of angiotensin II inhibits ANP-induced mesangial cGMP accumulation. Kidney Int. 1991;40(2):188–94.CrossRefPubMed
49.
go back to reference Kikkawa R, Haneda M, Sakamoto K, Koya D, Shikano T, Nakanishi S, et al. Antagonist for atrial natriuretic peptide receptors ameliorates glomerular hyperfiltration in diabetic rats. Biochem Biophys Res Commun. 1993;193(2):700–5.CrossRefPubMed Kikkawa R, Haneda M, Sakamoto K, Koya D, Shikano T, Nakanishi S, et al. Antagonist for atrial natriuretic peptide receptors ameliorates glomerular hyperfiltration in diabetic rats. Biochem Biophys Res Commun. 1993;193(2):700–5.CrossRefPubMed
50.
go back to reference Makino H, Mukoyama M, Mori K, Suganami T, Kasahara M, Yahata K, et al. Transgenic overexpression of brain natriuretic peptide prevents the progression of diabetic nephropathy in mice. Diabetologia. 2006;49(10):2514–24.CrossRefPubMed Makino H, Mukoyama M, Mori K, Suganami T, Kasahara M, Yahata K, et al. Transgenic overexpression of brain natriuretic peptide prevents the progression of diabetic nephropathy in mice. Diabetologia. 2006;49(10):2514–24.CrossRefPubMed
51.
go back to reference Sugimoto H, Shikata K, Matsuda M, Kushiro M, Hayashi Y, Hiragushi K, et al. Increased expression of endothelial cell nitric oxide synthase (ecNOS) in afferent and glomerular endothelial cells is involved in glomerular hyperfiltration of diabetic nephropathy. Diabetologia. 1998;41(12):1426–34.CrossRefPubMed Sugimoto H, Shikata K, Matsuda M, Kushiro M, Hayashi Y, Hiragushi K, et al. Increased expression of endothelial cell nitric oxide synthase (ecNOS) in afferent and glomerular endothelial cells is involved in glomerular hyperfiltration of diabetic nephropathy. Diabetologia. 1998;41(12):1426–34.CrossRefPubMed
52.
go back to reference Hiragushi K, Wada J, Eguchi J, Matsuoka T, Yasuhara A, Hashimoto I, et al. The role of adrenomedullin and receptors in glomerular hyperfiltration in streptozotocin-induced diabetic rats. Kidney Int. 2004;65(2):540–50.CrossRefPubMed Hiragushi K, Wada J, Eguchi J, Matsuoka T, Yasuhara A, Hashimoto I, et al. The role of adrenomedullin and receptors in glomerular hyperfiltration in streptozotocin-induced diabetic rats. Kidney Int. 2004;65(2):540–50.CrossRefPubMed
53.
go back to reference Yamamoto Y, Maeshima Y, Kitayama H, Kitamura S, Takazawa Y, Sugiyama H, et al. Tumstatin peptide, an inhibitor of angiogenesis, prevents glomerular hypertrophy in the early stage of diabetic nephropathy. Diabetes. 2004;53(7):1831–40.CrossRefPubMed Yamamoto Y, Maeshima Y, Kitayama H, Kitamura S, Takazawa Y, Sugiyama H, et al. Tumstatin peptide, an inhibitor of angiogenesis, prevents glomerular hypertrophy in the early stage of diabetic nephropathy. Diabetes. 2004;53(7):1831–40.CrossRefPubMed
54.
go back to reference Ichinose K, Maeshima Y, Yamamoto Y, Kitayama H, Takazawa Y, Hirokoshi K, et al. Antiangiogenic endostatin peptide ameliorates renal alterations in the early stage of a type 1 diabetic nephropathy model. Diabetes. 2005;54(10):2891–903.CrossRefPubMed Ichinose K, Maeshima Y, Yamamoto Y, Kitayama H, Takazawa Y, Hirokoshi K, et al. Antiangiogenic endostatin peptide ameliorates renal alterations in the early stage of a type 1 diabetic nephropathy model. Diabetes. 2005;54(10):2891–903.CrossRefPubMed
55.
go back to reference Ichinose K, Maeshima Y, Yamamoto Y, Kinomura M, Hirokoshi K, Kitayama H, et al. 2-(8-hydroxy-6-methoxy-1-oxo-1h–2-benzopyran-3-yl) propionic acid, an inhibitor of angiogenesis, ameliorates renal alterations in obese type 2 diabetic mice. Diabetes. 2006;55(5):1232–42.CrossRefPubMed Ichinose K, Maeshima Y, Yamamoto Y, Kinomura M, Hirokoshi K, Kitayama H, et al. 2-(8-hydroxy-6-methoxy-1-oxo-1h–2-benzopyran-3-yl) propionic acid, an inhibitor of angiogenesis, ameliorates renal alterations in obese type 2 diabetic mice. Diabetes. 2006;55(5):1232–42.CrossRefPubMed
56.
go back to reference Furuta T, Saito T, Ootaka T, Soma J, Obara K, Abe K, et al. The role of macrophages in diabetic glomerulosclerosis. Am J Kidney Dis. 1993;21(5):480–5.CrossRefPubMed Furuta T, Saito T, Ootaka T, Soma J, Obara K, Abe K, et al. The role of macrophages in diabetic glomerulosclerosis. Am J Kidney Dis. 1993;21(5):480–5.CrossRefPubMed
57.
go back to reference Sugimoto H, Shikata K, Hirata K, Akiyama K, Matsuda M, Kushiro M, et al. Increased expression of intercellular adhesion molecule-1 (ICAM-1) in diabetic rat glomeruli: glomerular hyperfiltration is a potential mechanism of ICAM-1 upregulation. Diabetes. 1997;46(12):2075–81.CrossRefPubMed Sugimoto H, Shikata K, Hirata K, Akiyama K, Matsuda M, Kushiro M, et al. Increased expression of intercellular adhesion molecule-1 (ICAM-1) in diabetic rat glomeruli: glomerular hyperfiltration is a potential mechanism of ICAM-1 upregulation. Diabetes. 1997;46(12):2075–81.CrossRefPubMed
58.
go back to reference Okada S, Shikata K, Matsuda M, Ogawa D, Usui H, Kido Y, et al. Intercellular adhesion molecule-1-deficient mice are resistant against renal injury after induction of diabetes. Diabetes. 2003;52(10):2586–93.CrossRefPubMed Okada S, Shikata K, Matsuda M, Ogawa D, Usui H, Kido Y, et al. Intercellular adhesion molecule-1-deficient mice are resistant against renal injury after induction of diabetes. Diabetes. 2003;52(10):2586–93.CrossRefPubMed
59.
go back to reference Usui HK, Shikata K, Sasaki M, Okada S, Matsuda M, Shikata Y, et al. Macrophage scavenger receptor-a-deficient mice are resistant against diabetic nephropathy through amelioration of microinflammation. Diabetes. 2007;56(2):363–72.CrossRefPubMed Usui HK, Shikata K, Sasaki M, Okada S, Matsuda M, Shikata Y, et al. Macrophage scavenger receptor-a-deficient mice are resistant against diabetic nephropathy through amelioration of microinflammation. Diabetes. 2007;56(2):363–72.CrossRefPubMed
60.
go back to reference Usui H, Shikata K, Matsuda M, Okada S, Ogawa D, Yamashita T, et al. HMG-CoA reductase inhibitor ameliorates diabetic nephropathy by its pleiotropic effects in rats. Nephrol Dial Transplant. 2003;18(2):265–72.CrossRefPubMed Usui H, Shikata K, Matsuda M, Okada S, Ogawa D, Yamashita T, et al. HMG-CoA reductase inhibitor ameliorates diabetic nephropathy by its pleiotropic effects in rats. Nephrol Dial Transplant. 2003;18(2):265–72.CrossRefPubMed
61.
go back to reference Ohga S, Shikata K, Yozai K, Okada S, Ogawa D, Usui H, Wada J, Shikata Y, Makino H. Thiazolidinedione ameliorates renal injury in experimental diabetic rats through anti-inflammatory effects mediated by inhibition of NF-{kappa}B activation. Am J Physiol Renal Physiol. 2007;292(4):F1141–50.CrossRefPubMed Ohga S, Shikata K, Yozai K, Okada S, Ogawa D, Usui H, Wada J, Shikata Y, Makino H. Thiazolidinedione ameliorates renal injury in experimental diabetic rats through anti-inflammatory effects mediated by inhibition of NF-{kappa}B activation. Am J Physiol Renal Physiol. 2007;292(4):F1141–50.CrossRefPubMed
62.
go back to reference Yozai K, Shikata K, Sasaki M, Tone A, Ohga S, Usui H, et al. Methotrexate prevents renal injury in experimental diabetic rats via anti-inflammatory actions. J Am Soc Nephrol. 2005;16(11):3326–38.CrossRefPubMed Yozai K, Shikata K, Sasaki M, Tone A, Ohga S, Usui H, et al. Methotrexate prevents renal injury in experimental diabetic rats via anti-inflammatory actions. J Am Soc Nephrol. 2005;16(11):3326–38.CrossRefPubMed
63.
go back to reference Tone A, Shikata K, Sasaki M, Ohga S, Yozai K, Nishishita S, et al. Erythromycin ameliorates renal injury via anti-inflammatory effects in experimental diabetic rats. Diabetologia. 2005;48(11):2402–11.CrossRefPubMed Tone A, Shikata K, Sasaki M, Ohga S, Yozai K, Nishishita S, et al. Erythromycin ameliorates renal injury via anti-inflammatory effects in experimental diabetic rats. Diabetologia. 2005;48(11):2402–11.CrossRefPubMed
64.
go back to reference Miyata T, Nangaku M, Suzuki D, Inagi R, Uragami K, Sakai H, et al. A mesangium-predominant gene, megsin, is a new serpin upregulated in IgA nephropathy. J Clin Invest. 1998;102(4):828–36.CrossRefPubMedPubMedCentral Miyata T, Nangaku M, Suzuki D, Inagi R, Uragami K, Sakai H, et al. A mesangium-predominant gene, megsin, is a new serpin upregulated in IgA nephropathy. J Clin Invest. 1998;102(4):828–36.CrossRefPubMedPubMedCentral
65.
go back to reference Inagi R, Yamamoto Y, Nangaku M, Usuda N, Okamato H, Kurokawa K, et al. A severe diabetic nephropathy model with early development of nodule-like lesions induced by megsin overexpression in RAGE/iNOS transgenic mice. Diabetes. 2006;55(2):356–66.CrossRefPubMed Inagi R, Yamamoto Y, Nangaku M, Usuda N, Okamato H, Kurokawa K, et al. A severe diabetic nephropathy model with early development of nodule-like lesions induced by megsin overexpression in RAGE/iNOS transgenic mice. Diabetes. 2006;55(2):356–66.CrossRefPubMed
66.
go back to reference Wada J, Kanwar YS. Characterization of mammalian translocase of inner mitochondrial membrane (Tim44) isolated from diabetic newborn mouse kidney. Proc Natl Acad Sci USA. 1998;95(1):144–9.CrossRefPubMedPubMedCentral Wada J, Kanwar YS. Characterization of mammalian translocase of inner mitochondrial membrane (Tim44) isolated from diabetic newborn mouse kidney. Proc Natl Acad Sci USA. 1998;95(1):144–9.CrossRefPubMedPubMedCentral
67.
go back to reference Yang Q, Dixit B, Wada J, Tian Y, Wallner EI, Srivastva SK, et al. Identification of a renal-specific oxido-reductase in newborn diabetic mice. Proc Natl Acad Sci USA. 2000;97(18):9896–901.CrossRefPubMedPubMedCentral Yang Q, Dixit B, Wada J, Tian Y, Wallner EI, Srivastva SK, et al. Identification of a renal-specific oxido-reductase in newborn diabetic mice. Proc Natl Acad Sci USA. 2000;97(18):9896–901.CrossRefPubMedPubMedCentral
68.
go back to reference Matsuoka T, Wada J, Hashimoto I, Zhang Y, Eguchi J, Ogawa N, et al. Gene delivery of Tim44 reduces mitochondrial superoxide production and ameliorates neointimal proliferation of injured carotid artery in diabetic rats. Diabetes. 2005;54(10):2882–90.CrossRefPubMed Matsuoka T, Wada J, Hashimoto I, Zhang Y, Eguchi J, Ogawa N, et al. Gene delivery of Tim44 reduces mitochondrial superoxide production and ameliorates neointimal proliferation of injured carotid artery in diabetic rats. Diabetes. 2005;54(10):2882–90.CrossRefPubMed
69.
go back to reference Zhang Y, Wada J, Hashimoto I, Eguchi J, Yasuhara A, Kanwar YS, et al. Therapeutic approach for diabetic nephropathy using gene delivery of translocase of inner mitochondrial membrane 44 by reducing mitochondrial superoxide production. J Am Soc Nephrol. 2006;17(4):1090–101.CrossRefPubMed Zhang Y, Wada J, Hashimoto I, Eguchi J, Yasuhara A, Kanwar YS, et al. Therapeutic approach for diabetic nephropathy using gene delivery of translocase of inner mitochondrial membrane 44 by reducing mitochondrial superoxide production. J Am Soc Nephrol. 2006;17(4):1090–101.CrossRefPubMed
70.
go back to reference Okada T, Wada J, Hida K, Eguchi J, Hashimoto I, Baba M, et al. Thiazolidinediones ameliorate diabetic nephropathy via cell cycle-dependent mechanisms. Diabetes. 2006;55(6):1666–77.CrossRefPubMed Okada T, Wada J, Hida K, Eguchi J, Hashimoto I, Baba M, et al. Thiazolidinediones ameliorate diabetic nephropathy via cell cycle-dependent mechanisms. Diabetes. 2006;55(6):1666–77.CrossRefPubMed
71.
go back to reference Nagai K, Arai H, Yanagita M, Matsubara T, Kanamori H, Nakano T, et al. Growth arrest-specific gene 6 is involved in glomerular hypertrophy in the early stage of diabetic nephropathy. J Biol Chem. 2003;278(20):18229–34.CrossRefPubMed Nagai K, Arai H, Yanagita M, Matsubara T, Kanamori H, Nakano T, et al. Growth arrest-specific gene 6 is involved in glomerular hypertrophy in the early stage of diabetic nephropathy. J Biol Chem. 2003;278(20):18229–34.CrossRefPubMed
72.
go back to reference Nagai K, Matsubara T, Mima A, Sumi E, Kanamori H, Iehara N, et al. Gas6 induces Akt/mTOR-mediated mesangial hypertrophy in diabetic nephropathy. Kidney Int. 2005;68(2):552–61.CrossRefPubMed Nagai K, Matsubara T, Mima A, Sumi E, Kanamori H, Iehara N, et al. Gas6 induces Akt/mTOR-mediated mesangial hypertrophy in diabetic nephropathy. Kidney Int. 2005;68(2):552–61.CrossRefPubMed
74.
go back to reference Yanagita M. The role of the vitamin K-dependent growth factor Gas6 in glomerular pathophysiology. Curr Opin Nephrol Hypertens. 2004;13(4):465–70.CrossRefPubMed Yanagita M. The role of the vitamin K-dependent growth factor Gas6 in glomerular pathophysiology. Curr Opin Nephrol Hypertens. 2004;13(4):465–70.CrossRefPubMed
75.
go back to reference Suganami T, Mukoyama M, Mori K, Yokoi H, Koshikawa M, Sawai K, et al. Prevention and reversal of renal injury by leptin in a new mouse model of diabetic nephropathy. FASEB J. 2005;19(1):127–9.CrossRefPubMed Suganami T, Mukoyama M, Mori K, Yokoi H, Koshikawa M, Sawai K, et al. Prevention and reversal of renal injury by leptin in a new mouse model of diabetic nephropathy. FASEB J. 2005;19(1):127–9.CrossRefPubMed
76.
go back to reference Shimazaki A, Kawamura Y, Kanazawa A, Sekine A, Saito S, Tsunoda T, et al. Genetic variations in the gene encoding ELMO1 are associated with susceptibility to diabetic nephropathy. Diabetes. 2005;54(4):1171–8.CrossRefPubMed Shimazaki A, Kawamura Y, Kanazawa A, Sekine A, Saito S, Tsunoda T, et al. Genetic variations in the gene encoding ELMO1 are associated with susceptibility to diabetic nephropathy. Diabetes. 2005;54(4):1171–8.CrossRefPubMed
77.
go back to reference Tanaka N, Babazono T, Saito S, Sekine A, Tsunoda T, Haneda M, et al. Association of solute carrier family 12 (sodium/chloride) member 3 with diabetic nephropathy, identified by genome-wide analyses of single nucleotide polymorphisms. Diabetes. 2003;52(11):2848–53.CrossRefPubMed Tanaka N, Babazono T, Saito S, Sekine A, Tsunoda T, Haneda M, et al. Association of solute carrier family 12 (sodium/chloride) member 3 with diabetic nephropathy, identified by genome-wide analyses of single nucleotide polymorphisms. Diabetes. 2003;52(11):2848–53.CrossRefPubMed
78.
go back to reference Hayashi Y, Makino H, Ota Z. Serum and urinary concentrations of type IV collagen and laminin as a marker of microangiopathy in diabetes. Diabet Med. 1992;9(4):366–70.CrossRefPubMed Hayashi Y, Makino H, Ota Z. Serum and urinary concentrations of type IV collagen and laminin as a marker of microangiopathy in diabetes. Diabet Med. 1992;9(4):366–70.CrossRefPubMed
79.
go back to reference Okonogi H, Nishimura M, Utsunomiya Y, Hamaguchi K, Tsuchida H, Miura Y, et al. Urinary type IV collagen excretion reflects renal morphological alterations and type IV collagen expression in patients with type 2 diabetes mellitus. Clin Nephrol. 2001;55(5):357–64.PubMed Okonogi H, Nishimura M, Utsunomiya Y, Hamaguchi K, Tsuchida H, Miura Y, et al. Urinary type IV collagen excretion reflects renal morphological alterations and type IV collagen expression in patients with type 2 diabetes mellitus. Clin Nephrol. 2001;55(5):357–64.PubMed
80.
go back to reference Tomino Y, Suzuki S, Azushima C, Shou I, Iijima T, Yagame M, et al. Asian multicenter trials on urinary type IV collagen in patients with diabetic nephropathy. J Clin Lab Anal. 2001;15(4):188–92.CrossRefPubMed Tomino Y, Suzuki S, Azushima C, Shou I, Iijima T, Yagame M, et al. Asian multicenter trials on urinary type IV collagen in patients with diabetic nephropathy. J Clin Lab Anal. 2001;15(4):188–92.CrossRefPubMed
81.
go back to reference Yoshikawa R, Wada J, Seiki K, Matsuoka T, Miyamoto S, Takahashi K, et al. Urinary PGDS levels are associated with vascular injury in type 2 diabetes patients. Diabetes Res Clin Pract. 2007;76(3):358–67.CrossRefPubMed Yoshikawa R, Wada J, Seiki K, Matsuoka T, Miyamoto S, Takahashi K, et al. Urinary PGDS levels are associated with vascular injury in type 2 diabetes patients. Diabetes Res Clin Pract. 2007;76(3):358–67.CrossRefPubMed
82.
go back to reference Nakamura T, Sugaya T, Kawagoe Y, Ueda Y, Osada S, Koide H. Effect of pitavastatin on urinary liver-type fatty acid-binding protein levels in patients with early diabetic nephropathy. Diabetes Care. 2005;28(11):2728–32.CrossRefPubMed Nakamura T, Sugaya T, Kawagoe Y, Ueda Y, Osada S, Koide H. Effect of pitavastatin on urinary liver-type fatty acid-binding protein levels in patients with early diabetic nephropathy. Diabetes Care. 2005;28(11):2728–32.CrossRefPubMed
83.
go back to reference Nakamura T, Sugaya T, Koide H. Angiotensin II receptor antagonist reduces urinary liver-type fatty acid-binding protein levels in patients with diabetic nephropathy and chronic renal failure. Diabetologia. 2007;50(2):490–2.CrossRefPubMed Nakamura T, Sugaya T, Koide H. Angiotensin II receptor antagonist reduces urinary liver-type fatty acid-binding protein levels in patients with diabetic nephropathy and chronic renal failure. Diabetologia. 2007;50(2):490–2.CrossRefPubMed
84.
go back to reference Suzuki K, Babazono T, Murata H, Iwamoto Y. Clinical significance of urinary liver-type fatty acid-binding protein in patients with diabetic nephropathy. Diabetes Care. 2005;28(8):2038–9.CrossRefPubMed Suzuki K, Babazono T, Murata H, Iwamoto Y. Clinical significance of urinary liver-type fatty acid-binding protein in patients with diabetic nephropathy. Diabetes Care. 2005;28(8):2038–9.CrossRefPubMed
85.
go back to reference Taguma Y, Kitamoto Y, Futaki G, Ueda H, Monma H, Ishizaki M, et al. Effect of captopril on heavy proteinuria in azotemic diabetics. N Engl J Med. 1985;313(26):1617–20.CrossRefPubMed Taguma Y, Kitamoto Y, Futaki G, Ueda H, Monma H, Ishizaki M, et al. Effect of captopril on heavy proteinuria in azotemic diabetics. N Engl J Med. 1985;313(26):1617–20.CrossRefPubMed
86.
go back to reference Ohkubo Y, Kishikawa H, Araki E, Miyata T, Isami S, Motoyoshi S, et al. Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: a randomized prospective 6-year study. Diabetes Res Clin Pract. 1995;28(2):103–17.CrossRefPubMed Ohkubo Y, Kishikawa H, Araki E, Miyata T, Isami S, Motoyoshi S, et al. Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: a randomized prospective 6-year study. Diabetes Res Clin Pract. 1995;28(2):103–17.CrossRefPubMed
87.
go back to reference Makino H, Haneda M, Babazono T, Moriya T, Ito S, Iwamoto Y, et al. Prevention of transition from incipient to overt nephropathy with telmisartan in patients with type 2 diabetes. Diabetes Care. 2007;30(6):1577–8.CrossRefPubMed Makino H, Haneda M, Babazono T, Moriya T, Ito S, Iwamoto Y, et al. Prevention of transition from incipient to overt nephropathy with telmisartan in patients with type 2 diabetes. Diabetes Care. 2007;30(6):1577–8.CrossRefPubMed
88.
go back to reference Uzu T, Sawaguchi M, Maegawa H, Kashiwagi A. Reduction of microalbuminuria in patients with type 2 diabetes: the Shiga Microalbuminuria Reduction Trial (SMART). Diabetes Care. 2007;30(6):1581–3.CrossRefPubMed Uzu T, Sawaguchi M, Maegawa H, Kashiwagi A. Reduction of microalbuminuria in patients with type 2 diabetes: the Shiga Microalbuminuria Reduction Trial (SMART). Diabetes Care. 2007;30(6):1581–3.CrossRefPubMed
89.
go back to reference Araki SI, Haneda M, Koya D, Hidaka H, Sugimoto T, Isono M, Isshiki K, Chin-Kanasaki M, Uzu T, Kashiwagi A. Reduction in microalbuminuria as an integrated indicator for renal and cardiovascular risk reduction in patients with type 2 diabetes mellitus. Diabetes. 2007;56(6):1727–30.CrossRefPubMed Araki SI, Haneda M, Koya D, Hidaka H, Sugimoto T, Isono M, Isshiki K, Chin-Kanasaki M, Uzu T, Kashiwagi A. Reduction in microalbuminuria as an integrated indicator for renal and cardiovascular risk reduction in patients with type 2 diabetes mellitus. Diabetes. 2007;56(6):1727–30.CrossRefPubMed
Metadata
Title
Historical chronology of basic and clinical research in diabetic nephropathy and contributions of Japanese scientists
Authors
Jun Wada
Hirofumi Makino
Publication date
01-10-2009
Publisher
Springer Japan
Published in
Clinical and Experimental Nephrology / Issue 5/2009
Print ISSN: 1342-1751
Electronic ISSN: 1437-7799
DOI
https://doi.org/10.1007/s10157-009-0175-5

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