Hypertension and hyperglycemia synergize to cause incipient renal tubular alterations resulting in increased NGAL urinary excretion in rats

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Blázquez Medela, Ana M ^b,c   García Sánchez, Omar ^b,c   Blanco Gozalo, Víctor ^a,b,d   Quiros, Yaremi ^b,d   Montero, María J ^b   Martínez Salgado, Carlos ^a,b,c   López Novoa, José M ^b,c   López Hernández, Francisco J ^a,b,c  

^a HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c Instituto Reina Sofía de Investigación Nefrológica Fundación Iñigo Álvarez de Toledo   (Spain)

^d Bio inRen SL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

N(G) NITROARGININE METHYL ESTER; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; ACUTE PHASE PROTEIN; BIOLOGICAL MARKER; LIPOCALIN; NEUTROPHIL GELATINASE-ASSOCIATED LIPOCALIN PROTEIN, RAT; ONCOPROTEIN;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPERGLYCEMIA; HYPERTENSION; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY PERFUSION; KIDNEY TUBULE DAMAGE; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; RISK FACTOR; SPONTANEOUSLY HYPERTENSIVE RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; URINARY EXCRETION; ANIMAL; BLOOD PRESSURE; CHEMICALLY INDUCED; EXPERIMENTAL DIABETES MELLITUS; GENETICS; KIDNEY TUBULE; METABOLISM; PATHOPHYSIOLOGY; PERFUSION; URINE; WISTAR RAT;

ACUTE-PHASE PROTEINS; ANIMALS; BIOMARKERS; BLOOD PRESSURE; DIABETES MELLITUS, EXPERIMENTAL; HYPERGLYCEMIA; HYPERTENSION; KIDNEY TUBULES; LIPOCALINS; MALE; NG-NITROARGININE METHYL ESTER; PERFUSION; PROTO-ONCOGENE PROTEINS; RATS, INBRED SHR; RATS, WISTAR;

EID: 84921997856     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0105988     Document Type: Article

References (51)

1. Lopez-Novoa JM, Martinez-Salgado C, Rodriguez-Peña AB, López-Hernández FJ (2010) Common pathophysiological mechanisms of chronic kidney disease: therapeutic perspectives. Pharmacol Ther 128: 61-81.
2. Lopez-Novoa JM, Rodriguez-Peña AB, Ortiz A, Martinez-Salgado C, López Hernández FJ (2011) Etiopathology of chronic tubular, glomerular and renovascular nephropathies: Clinical implications. J Transl Med 9: 13.
3. De Zeeuw D, Hillege HL, de Jong PE (2005) The kidney, a cardiovascular risk marker, and a new target for therapy. Kidney Int Suppl (Suppl 98): S25-S29.
4. Atkins RC (2005) The epidemiology of chronic kidney disease. Kidney Int Suppl (94): S14-S18.
5. Remuzzi G, Benigni A, Remuzzi A (2006) Mechanisms of progression and regression of renal lesions of chronic nephropathies and diabetes. J Clin Invest 116: 288-296. (Pubitemid 43228342)
6. Carrero JJ, Stenvinkel P (2011) Predialysis chronic kidney disease in 2010: Novel targets for slowing CKD progression. Nat Rev Nephrol 7: 65-66.
7. Xue JL, Ma JZ, Louis TA, Collins AJ (2001) Forecast of the number of patients with end-stage renal disease in the United States to the year 2010. J Am Soc Nephrol 12: 2753-2758.
8. Winkelmayer WC, Weinstein MC, Mittleman MA, Glynn RJ, Pliskin JS (2002) Health economic evaluations: The special case of end stage renal disease treatment. Med Decis Mak 22: 4172430.
9. Szczech LA, Lazar IL (2004) Projecting the United States ESRD population: Issues regarding treatment of patients with ESRD. Kidney Int Suppl (90): S32-S7.
10. U.S. Renal Data System, USRDS (2009) 2009 Annual Data Report: Atlas of end-stage renal disease in the United States. Bethesda, MD: National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases http://www.usrds.org/2009/slides/indiv/INDEX-CKD.HTML.
11. Basi S, Fesler P, Mimran A, Lewis JB (2008) Microalbuminuria in type 2 diabetes and hypertension: a marker, treatment target, or innocent bystander? Diabetes Care (Suppl 2): S194-S201.
12. Gohda T, Niewczas MA, Ficociello LH, Walker WH, Skupien J, et al. (2012) Circulating TNF receptors 1 and 2 predict stage 3 CKD in type 1 diabetes. J Am Soc Nephrol 23: 516-524.
13. Gohda T, Tomino Y (2013) Novel biomarkers for the progression of diabetic nephropathy: soluble TNF receptors. Curr Diab Rep 13: 560-566.
14. Niewczas MA, Gohda T, Skupien J, Smiles AM, Walker WH, et al. (2012) Circulating TNF receptors 1 and 2 predict ESRD in type 2 diabetes. J Am Soc Nephrol 23: 507-515.
15. Izumi Y, Yabe D, Taniguchi A, Fukushima M, Nakai Y, et al. (2013) Circulating TNF receptor 2 is associated with the development of chronic kidney disease in non-obese Japanese patients with type 2 diabetes. Diabetes Res Clin Pract 99: 145-150.
16. Soni SS, Cruz D, Bobek I, Chionh CY, Nalesso F, et al. (2010) NGAL: a biomarker of acute kidney injury and other systemic conditions. Int Urol Nephrol 42: 141-150.
17. Vaidya VS, Ferguson MA, Bonventre JV (2008) Biomarkers of acute kidney injury. Annu Rev Pharmacol Toxicol 48: 463-493. (Pubitemid 351738161)
18. Devarajan P (2010) Neutrophil gelatinase-associated lipocalin: a promising biomarker for human acute kidney injury. Biomark Med 4: 265-280.
19. Devarajan P (2008) Neutrophil gelatinase-associated lipocalin (NGAL): a new marker of kidney disease. Scand J Clin Lab Invest Suppl 241: 89-94.
20. Mishra J, Mori K, Ma Q, Kelly C, Barasch J, et al. (2004) Neutrophil gelatinase-associated lipocalin: a novel early urinary biomarker for cisplatin nephrotoxicity. Am J Nephrol 24: 307-315. (Pubitemid 39070114)
21. Gaspari F, Cravedi P, Mandalà M, Perico N, de Leon FR, et al. (2010) Predicting Cisplatin-Induced Acute Kidney Injury by Urinary Neutrophil Gelatinase-Associated Lipocalin Excretion: A Pilot Prospective Case-Control Study. Nephron Clin Pract 115: c154-c160.
22. Wasilewska A, Zoch-Zwierz W, Taranta-Janusz K, Michaluk-Skutnik J (2010) Neutrophil gelatinase-associated lipocalin (NGAL): a new marker of cyclosporine nephrotoxicity? Pediatr Nephrol 25: 889-897.
23. Lebkowska U, Malyszko J, Lebkowska A, Koc-Zorawska E, Lebkowski W, et al. (2009) Neutrophil gelatinase-associated lipocalin and cystatin C could predict renal outcome in patients undergoing kidney allograft transplantation: a prospective study. Transplant Proc 41: 154-157.
24. Ko GJ, Grigoryev DN, Linfert D, Jang HR, Watkins T, et al. (2010) Transcriptional analysis of kidneys during repair from AKI reveals possible roles for NGAL and KIM-1 as biomarkers of AKI to CKD transition. Am J Physiol Renal Physiol 298: F1472-F1483.
25. Malyszko J, Bachorzewska-Gajewska H, Sitniewska E, Malyszko JS, Poniatowski B, et al. (2008) Serum neutrophil gelatinase-associated lipocalin as a marker of renal function in non-diabetic patients with stage 2-4 chronic kidney disease. Ren Fail 30: 625-628.
26. Chaudhary K, Phadke G, Nistala R, Weidmeyer CE, McFarlane SI, et al. (2010) The emerging role of biomarkers in diabetic and hypertensive chronic kidney disease. Curr Diab Rep 10: 37-42.
27. Kuwabara T, Mori K, Mukoyama M, Kasahara M, Yokoi H, et al. (2009) Urinary neutrophil gelatinase-associated lipocalin levels reflect damage to glomeruli, proximal tubules, and distal nephrons. Kidney Int 75: 285-294.
28. Bolignano D, Lacquaniti A, Coppolino G, Donato V, Fazio MR, et al. (2009) Neutrophil gelatinase-associated lipocalin as an early biomarker of nephropathy in diabetic patients. Kidney Blood Press Res 32: 91-98.
29. Malyszko J, Bachorzewska-Gajewska H, Malyszko JS, Pawlak K, Dobrzycki S (2008) Serum neutrophil gelatinase-associated lipocalin as a marker of renal function in hypertensive and normotensive patients with coronary artery disease. Nephrology (Carlton) 13: 153-156. (Pubitemid 351232835)
30. Bradford MM (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.
31. Quiros Y, Ferreira L, Sancho-Martínez SM, González-Buitrago JM, López-Novoa JM, et al. (2010) Sub-nephrotoxic doses of gentamicin predispose animals to developing acute kidney injury and to excrete ganglioside M2 activator protein. Kidney Int 78: 1006-1015.
32. López-Novoa JM, Santos JC, Villamediana LM, Garrote FJ, Thim L, et al. (1986) Renal catabolism of 125I-glicentin. Am J Physiol 250: E545-E550.
33. Bergeron M, Mayers P, Brown D (1996) Specific effect of maleate on an apical membrane glycoprotein (gp330) in proximal tubule of rat kidneys. Am J Physiol Renal Fluid Electrolyte Physiol 271: F908-F916.
34. Nagai J, Tanaka H, Nakanishi N, Murakami T, Takano M (2001) Role of megalin in renal handling of aminoglycosides. Am J Physiol Renal Physiol 281: F337-F344.
35. Martínez Seeber A, Vila SB, Catanzaro OL (1982) The mechanism of urinary kallikrein excretion in the rat. Clin Sci (Lond) 63: 217-218. (Pubitemid 12000386)
36. Mishra J, Ma Q, Prada A, Mitsnefes M, Zahedi K, et al. (2003) Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J Am Soc Nephrol 14: 2534-2543. (Pubitemid 37169339)
37. Mancia G (2005) The association of hypertension and diabetes: prevalence, cardiovascular risk and protection by blood pressure reduction. Acta Diabetol (Suppl 1): S17-S25.
38. Grossman E, Messerli FH (2008) Hypertension and diabetes. Adv Cardiol 45: 82-106.
39. Sahakyan K, Klein BE, Myers CE, Tsai MY, Klein R (2010) Novel risk factors in long-term hypertension incidence in type 1 diabetes mellitus. Am Heart J 159: 1074-1080.
40. U.S. Renal Data System, USRDS 2007 Annual Data Report. Atlas of Chronic Kidney Disease and End-Stage Renal Disease in the United States, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases. http://www.usrds.org/adr-2007.htm.
41. Flower DR, North AC, Sansom CE (2000) The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta 1482: 9-24.
42. Devireddy LR, Gazin C, Zhu X, Green MR (2005) A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell 123: 1293-1305. (Pubitemid 41821786)
43. Cowland JB, Borregaard N (1997) Molecular characterization and pattern of tissue expression of the gene for neutrophil gelatinase-associated lipocalin from humans. Genomics 45: 17-23. (Pubitemid 27449379)
44. Carlson M, Raab Y, Sevéus L, Xu S, Hällgren R, et al. (2002) Human neutrophil lipocalin is a unique marker of neutrophil inflammation in ulcerative colitis and proctitis. Gut 50: 501-506. (Pubitemid 34638869)
45. Mori K, Lee HT, Rapoport D, Drexler IR, Foster K, et al. (2005) Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J Clin Invest 115: 610-621. (Pubitemid 40322235)
46. Viau A, El Karoui K, Laouari D, Drexler IR, Foster K, et al. (2010) Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 120: 4065-4076.
47. Bolignano D, Coppolino G, Lacquaniti A, Buemi M (2010) From kidney to cardiovascular diseases: NGAL as a biomarker beyond the confines of nephrology. Eur J Clin Invest 40: 273-276.
48. Mori K, Nakao K (2007) Neutrophil gelatinase-associated lipocalin as the realtime indicator of active kidney damage. Kidney Int 71: 967-970. (Pubitemid 46741985)
49. Hvidberg V, Jacobsen C, Strong RK, Cowland JB, Moestrup SK, et al. (2005) The endocytic receptor megalin binds the iron transporting neutrophil- gelatinase-associated lipocalin with high affinity and mediates its cellular uptake. FEBS Lett 579: 773-777.
50. Tojo A, Onozato ML, Ha H, Kurihara H, Sakai T, et al. (2001) Reduced albumin reabsorption in the proximal tubule of early-stage diabetic rats. Histochem Cell Biol 116: 269-276. (Pubitemid 32930140)
51. Hryciw DH, Lee EM, Pollock CA, Poronnik P (2004) Molecular changes in proximal tubule function in diabetes mellitus. Clin Exp Pharmacol Physiol 31: 372-379. (Pubitemid 38803085)