Can We Target Tubular Damage to Prevent Renal Function Decline in Diabetes?

Seminars in Nephrology

Volumn 32, Issue 5, 2012, Pages 452-462

  Bonventre, Joseph V ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

chronic kidney disease; diabetic nephropathy; Fibrosis; kidney; KIM 1

Indexed keywords

ADVANCED GLYCATION END PRODUCT; BARDOXOLONE; COLLAGEN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GLUCOSE; GROWTH FACTOR; LIPID; MICRORNA; PLACEBO; RAMIPRIL; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA1;

ALBUMINURIA; ARTICLE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL PROLIFERATION; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DISEASE ASSOCIATION; DISEASE COURSE; DRUG MECHANISM; DRUG TARGETING; GLOMERULOSCLEROSIS; GLUCOSE BLOOD LEVEL; HUMAN; HYPERGLYCEMIA; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; INTERSTITIAL NEPHRITIS; KIDNEY FAILURE; KIDNEY FIBROSIS; KIDNEY ISCHEMIA; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE DAMAGE; MYOFIBROBLAST; NEPHROTOXICITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PERICYTE; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEINURIA; RENAL PROTECTION;

EID: 84867394203     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2012.07.008     Document Type: Article

References (85)

1. Fioretto P., Mauer M. Histopathology of diabetic nephropathy. Semin Nephrol 2007, 27:195-207.
2. Mauer S.M., Steffes M.W., Ellis E.N., et al. Structural-functional relationships in diabetic nephropathy. J Clin Invest 1984, 74:1143-1155.
3. White K.E., Bilous R.W. Type 2 diabetic patients with nephropathy show structural-functional relationships that are similar to type 1 disease. J Am Soc Nephrol 2000, 11:1667-1673.
4. Najafian B., Kim Y., Crosson J.T., Mauer M. Atubular glomeruli and glomerulotubular junction abnormalities in diabetic nephropathy. J Am Soc Nephrol 2003, 14:908-917.
5. White K.E., Marshall S.M., Bilous R.W. Prevalence of atubular glomeruli in type 2 diabetic patients with nephropathy. Nephrol Dial Transplant 2008, 23:3539-3545.
6. Marcussen N. Atubular glomeruli and the structural basis for chronic renal failure. Lab Invest 1992, 66:265-284.
7. Bader R., Bader H., Grund K.E., et al. Structure and function of the kidney in diabetic glomerulosclerosis. Correlations between morphological and functional parameters. Pathol Res Pract 1980, 167:204-216.
8. Harris R.D., Steffes M.W., Bilous R.W., Sutherland D.E., Mauer S.M. Global glomerular sclerosis and glomerular arteriolar hyalinosis in insulin dependent diabetes. Kidney Int 1991, 40:107-114.
9. Osterby R., Parving H.H., Nyberg G., et al. A strong correlation between glomerular filtration rate and filtration surface in diabetic nephropathy. Diabetologia 1988, 31:265-270.
10. Ziyadeh F.N., Goldfarb S. The renal tubulointerstitium in diabetes mellitus. Kidney Int 1991, 39:464-475.
11. Rodriguez-Iturbe B., Johnson R.J., Herrera-Acosta J. Tubulointerstitial damage and progression of renal failure. Kidney Int Suppl 2005, 99:S82-S86.
12. Humphreys B.D. Targeting pericyte differentation as a strategy to modulate kidney fibrosis in diabetic nephropathy. Semin Nephrol 2012, 32:463-470.
13. Lewis E.J., Hunsicker L.G., Bain R.P., Rohde R.D. The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N Engl J Med 1993, 329:1456-1462.
14. Gurley S.B., Coffman T.M. The renin-angiotensin system and diabetic nephropathy. Semin Nephrol 2007, 27:144-152.
15. Brenner B.M., Cooper M.E., de Zeeuw D., et al. Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 2001, 345:861-869.
16. Lewis E.J., Hunsicker L.G., Clarke W.R., et al. Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N Engl J Med 2001, 345:851-860.
17. Zatz R., Dunn B.R., Meyer T.W., et al. Prevention of diabetic glomerulopathy by pharmacological amelioration of glomerular capillary hypertension. J Clin Invest 1986, 77:1925-1930.
18. Perico N., Benigni A., Remuzzi G. Present and future drug treatments for chronic kidney diseases: evolving targets in renoprotection. Nat Rev Drug Discov 2008, 7:936-953.
19. Decleves A.E., Sharma K. New pharmacological treatments for improving renal outcomes in diabetes. Nat Rev 2010, 6:371-380.
20. de Borst M.H., van Timmeren M.M., Vaidya V.S., et al. Induction of kidney injury molecule-1 in homozygous Ren2 rats is attenuated by blockade of the renin-angiotensin system or p38 MAP kinase. Am J Physiol 2007, 292:F313-F320.
21. Rosolowsky E.T., Skupien J., Smiles A.M., et al. Risk for ESRD in type 1 diabetes remains high despite renoprotection. J Am Soc Nephrol 2011, 22:545-553.
22. de Zeeuw D. Albuminuria: a target for treatment of type 2 diabetic nephropathy. Semin Nephrol 2007, 27:172-181.
23. Yu Y., Jin H., Holder D., et al. Urinary biomarkers trefoil factor 3 and albumin enable early detection of kidney tubular injury. Nat Biotechnol 2010, 28:470-477.
24. Abrass C.K. Diabetic proteinuria. Glomerular or tubular in origin?. Am J Nephrol 1984, 4:337-346.
25. Abbate M., Zoja C., Remuzzi G. How does proteinuria cause progressive renal damage?. J Am Soc Nephrol 2006, 17:2974-2984.
26. Strutz F.M. EMT and proteinuria as progression factors. Kidney Int 2009, 75:475-481.
27. Miltenyi M., Korner A., Tulassay T., Szabo A. Tubular dysfunction in type I diabetes mellitus. Arch Dis Child 1985, 60:929-931.
28. Mogensen C.E., Christensen N.J., Gundersen H.J. The acute effect of insulin on renal haemodynamics and protein excretion in diabetics. Diabetologia 1978, 15:153-157.
29. Watts G.F., Vlitos M.A., Morris R.W., Price R.G. Urinary N-acetyl-beta-D-glucosaminidase excretion in insulin-dependent diabetes mellitus: relation to microalbuminuria, retinopathy and glycaemic control. Diabete Metab 1988, 14:653-658.
30. Gibb D.M., Tomlinson P.A., Dalton N.R., et al. Renal tubular proteinuria and microalbuminuria in diabetic patients. Arch Dis Child 1989, 64:129-134.
31. Vaidya V.S., Niewczas M.A., Ficociello L.H., et al. Regression of microalbuminuria in type 1 diabetes is associated with lower levels of urinary tubular injury biomarkers, kidney injury molecule-1, and N-acetyl-beta-D-glucosaminidase. Kidney Int 2011, 79:464-470.
32. Ziyadeh F.N., Snipes E.R., Watanabe M., et al. High glucose induces cell hypertrophy and stimulates collagen gene transcription in proximal tubule. Am J Physiol 1990, 259:F704-F714.
33. Polhill T.S., Saad S., Poronnik P., Fulcher G.R., Pollock C.A. Short-term peaks in glucose promote renal fibrogenesis independently of total glucose exposure. Am J Physiol 2004, 287:F268-F273.
34. Ihm C.G., Lee G.S., Nast C.C., et al. Early increased renal procollagen alpha 1(IV) mRNA levels in streptozotocin induced diabetes. Kidney Int 1992, 41:768-777.
35. Christiansen J.S., Frandsen M., Parving H.H. Effect of intravenous glucose infusion on renal function in normal man and in insulin-dependent diabetics. Diabetologia 1981, 21:368-373.
36. Vestri S., Okamoto M.M., de Freitas H.S., et al. Changes in sodium or glucose filtration rate modulate expression of glucose transporters in renal proximal tubular cells of rat. J Membr Biol 2001, 182:105-112.
37. Tabatabai N.M., Sharma M., Blumenthal S.S., Petering D.H. Enhanced expressions of sodium-glucose cotransporters in the kidneys of diabetic Zucker rats. Diabetes Res Clin Pract 2009, 83:e27-e30.
38. Zhu Y., Usui H.K., Sharma K. Regulation of transforming growth factor beta in diabetic nephropathy: implications for treatment. Semin Nephrol 2007, 27:153-160.
39. Ziyadeh F.N., Sharma K., Ericksen M., Wolf G. Stimulation of collagen gene expression and protein synthesis in murine mesangial cells by high glucose is mediated by autocrine activation of transforming growth factor-beta. J Clin Invest 1994, 93:536-542.
40. Fraser D., Brunskill N., Ito T., Phillips A. Long-term exposure of proximal tubular epithelial cells to glucose induces transforming growth factor-beta 1 synthesis via an autocrine PDGF loop. Am J Pathol 2003, 163:2565-2574.
41. Zhang M., Fraser D., Phillips A. ERK, p38, and Smad signaling pathways differentially regulate transforming growth factor-beta1 autoinduction in proximal tubular epithelial cells. Am J Pathol 2006, 169:1282-1293.
42. Koesters R., Kaissling B., Lehir M., et al. Tubular overexpression of transforming growth factor-beta1 induces autophagy and fibrosis but not mesenchymal transition of renal epithelial cells. Am J Pathol 2010, 177:632-643.
43. Phillips A.O., Steadman R. Diabetic nephropathy: the central role of renal proximal tubular cells in tubulointerstitial injury. Histol Histopathol 2002, 17:247-252.
44. Han H.J., Lee Y.J., Park S.H., Lee J.H., Taub M. High glucose-induced oxidative stress inhibits Na+/glucose cotransporter activity in renal proximal tubule cells. Am J Physiol 2005, 288:F988-F996.
45. Zhong Q., Kowluru R.A. Epigenetic changes in mitochondrial superoxide dismutase in the retina and the development of diabetic retinopathy. Diabetes 2011, 60:1304-1313.
46. Tonna S., El-Osta A., Cooper M.E., Tikellis C. Metabolic memory and diabetic nephropathy: potential role for epigenetic mechanisms. Nat Rev 2010, 6:332-341.
47. Pergola P.E., Raskin P., Toto R.D., et al. Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N Engl J Med 2011, 365:327-336.
48. Dinkova-Kostova A.T., Liby K.T., Stephenson K.K., et al. Extremely potent triterpenoid inducers of the phase 2 response: correlations of protection against oxidant and inflammatory stress. Proc Natl Acad Sci U S A 2005, 102:4584-4589.
49. Tan A.L., Forbes J.M., Cooper M.E. AGE, RAGE, and ROS in diabetic nephropathy. Semin Nephrol 2007, 27:130-143.
50. Gugliucci A., Bendayan M. Renal fate of circulating advanced glycated end products (AGE): evidence for reabsorption and catabolism of AGE-peptides by renal proximal tubular cells. Diabetologia 1996, 39:149-160.
51. Youssef S., Nguyen D.T., Soulis T., et al. Effect of diabetes and aminoguanidine therapy on renal advanced glycation end-product binding. Kidney Int 1999, 55:907-916.
52. Tang S.C., Leung J.C., Chan L.Y., Tsang A.W., Lai K.N. Activation of tubular epithelial cells in diabetic nephropathy and the role of the peroxisome proliferator-activated receptor-gamma agonist. J Am Soc Nephrol 2006, 17:1633-1643.
53. Tang S.C., Chan L.Y., Leung J.C., et al. Differential effects of advanced glycation end-products on renal tubular cell inflammation. Nephrology (Carlton) 2011, 16:417-425.
54. Gallicchio M.A., Bach L.A. Advanced glycation end products inhibit Na+ K+ ATPase in proximal tubule epithelial cells: role of cytosolic phospholipase A2alpha and phosphatidylinositol 4-phosphate 5-kinase gamma. Biochim Biophys Acta 2010, 1803:19-930.
55. Fekete A., Rosta K., Wagner L., et al. Na+,K+-ATPase is modulated by angiotensin II in diabetic rat kidney-another reason for diabetic nephropathy?. J Physiol 2008, 586:5337-5348.
56. Sanchez Mejia R.O., Lam B.K., Arm J.P. Matrix-associated transforming growth factor-beta1 primes mouse bone marrow-derived mast cells for increased high-affinity Fc receptor for immunoglobulin E-dependent eicosanoid biosynthesis. Am J Respir Cell Mol Biol 2000, 22:557-565.
57. Grgic I., Campanholle G., Bijol V., et al. Targeted proximal tubule injury triggers interstitial fibrosis and glomerulosclerosis. Kidney Int 2012, 82:172-183.
58. Tang S., Leung J.C., Abe K., et al. Albumin stimulates interleukin-8 expression in proximal tubular epithelial cells in vitro and in vivo. J Clin Invest 2003, 111:515-527.
59. Duffield J.S. Macrophages and immunologic inflammation of the kidney. Semin Nephrol 2010, 30:234-254.
60. Vernon M.A., Mylonas K.J., Hughes J. Macrophages and renal fibrosis. Semin Nephrol 2010, 30:302-317.
61. Chow F.Y., Nikolic-Paterson D.J., Ozols E., et al. Monocyte chemoattractant protein-1 promotes the development of diabetic renal injury in streptozotocin-treated mice. Kidney Int 2006, 69:73-80.
62. Vielhauer V., Kulkarni O., Reichel C.A., Anders H.J. Targeting the recruitment of monocytes and macrophages in renal disease. Semin Nephrol 2010, 30:318-333.
63. Banba N., Nakamura T., Matsumura M., et al. Possible relationship of monocyte chemoattractant protein-1 with diabetic nephropathy. Kidney Int 2000, 58:684-690.
64. Morii T., Fujita H., Narita T., et al. Association of monocyte chemoattractant protein-1 with renal tubular damage in diabetic nephropathy. J Diabetes Complications 2003, 17:11-15.
65. Takebayashi K., Matsumoto S., Aso Y., Inukai T. Aldosterone blockade attenuates urinary monocyte chemoattractant protein-1 and oxidative stress in patients with type 2 diabetes complicated by diabetic nephropathy. J Clin Endocrinol Metab 2006, 91:2214-2217.
66. Fardon N.J., Wilkinson R., Thomas T.H. Abnormalities in primary granule exocytosis in neutrophils from type I diabetic patients with nephropathy. Clin Sci (Lond) 2002, 102:69-75.
67. Takahashi T., Hato F., Yamane T., et al. Increased spontaneous adherence of neutrophils from type 2 diabetic patients with overt proteinuria: possible role of the progression of diabetic nephropathy. Diabetes Care 2000, 23:417-418.
68. Tang S.C., Leung J.C., Lai K.N. Diabetic tubulopathy: an emerging entity. Contrib Nephrol 2011, 170:124-134.
69. Moon J.Y., Jeong K.H., Lee T.W., et al. Aberrant recruitment and activation of T cells in diabetic nephropathy. Am J Nephrol 2012, 35:164-194.
70. Hagerty D.T., Allen P.M. Processing and presentation of self and foreign antigens by the renal proximal tubule. J Immunol 1992, 148:2324-2330.
71. Lai K.N., Leung J.C., Chan L.Y., Guo H., Tang S.C. Interaction between proximal tubular epithelial cells and infiltrating monocytes/T cells in the proteinuric state. Kidney Int 2007, 71:526-538.
72. Pickup J.C., Mattock M.B., Chusney G.D., Burt D. NIDDM as a disease of the innate immune system: association of acute-phase reactants and interleukin-6 with metabolic syndrome X. Diabetologia 1997, 40:1286-1292.
73. Lin M., Yiu W.H., Wu H.J., et al. Toll-like receptor 4 promotes tubular inflammation in diabetic nephropathy. J Am Soc Nephrol 2012, 23:86-102.
74. Horlyck A., Gundersen H.J., Osterby R. The cortical distribution pattern of diabetic glomerulopathy. Diabetologia 1986, 29:146-150.
75. Huang H.C., Preisig P.A. G1 kinases and transforming growth factor-beta signaling are associated with a growth pattern switch in diabetes-induced renal growth. Kidney Int 2000, 58:162-172.
76. Thomson S.C., Deng A., Bao D., et al. Ornithine decarboxylase, kidney size, and the tubular hypothesis of glomerular hyperfiltration in experimental diabetes. J Clin Invest 2001, 107:217-224.
77. Okada R., Yasuda Y., Tsushita K., et al. Glomerular hyperfiltration in prediabetes and prehypertension. Nephrol Dial Transplant 2012, 27:1821-1825.
78. Verzola D., Gandolfo M.T., Gaetani G., et al. Accelerated senescence in the kidneys of patients with type 2 diabetic nephropathy. Am J Physiol 2008, 295:F1563-F1573.
79. Satriano J., Mansoury H., Deng A., et al. Transition of kidney tubule cells to a senescent phenotype in early experimental diabetes. Am J Physiol Cell Physiol 2010, 299:C374-C380.
80. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 1965, 37:614-636.
81. Yang L., Besschetnova T.Y., Brooks C.R., Shah J.V., Bonventre J.V. Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med 2010, 16:535-543. 1p following 143.
82. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001, 15:2177-2196.
83. Goodarzi A.A., Block W.D., Lees-Miller S.P. The role of ATM and ATR in DNA damage-induced cell cycle control. Prog Cell Cycle Res 2003, 5:393-411.
84. Kobayashi T., Okada H., Inoue T., Kanno Y., Suzuki H. Tubular expression of connective tissue growth factor correlates with interstitial fibrosis in type 2 diabetic nephropathy. Nephrol Dial Transplant 2006, 21:548-549.
85. Guha M., Xu Z.G., Tung D., Lanting L., Natarajan R. Specific down-regulation of connective tissue growth factor attenuates progression of nephropathy in mouse models of type 1 and type 2 diabetes. FASEB J 2007, 21:3355-3368.