Fisiopatología de la hiperfiltración glomerular en la diabetes. Parte 1

  • Claudio A. Mascheroni Nefrología San Pedro, Buenos Aires

Resumen

La hiperfiltración (HF) glomerular en la enfermedad renal diabética es un complejo fenómeno hemodinámico que ocurre en etapas tempranas de la evolución de la enfermedad, y muy probablemente tenga influencias negativas, en cuanto a la progresión hacia la aparición de la microalbuminuria y la evolución de la nefropatía diabética (NFDBT) evidente. Los factores involucrados en su fisiopatología son múltiples, e incluyen al medio diabético y numerosos factores humorales como óxido nítrico, prostaglandinas, sistema renina angiotensina aldosterona, péptido auricular natriurético, especies reactivas de oxígeno y otros factores humorales y de crecimiento, que actúan básicamente provocando o potenciando la vasodilatación de la arteriola aferente (AA), o factores con propiedad de vasoconstricción de la arteriola eferente, todos considerados como factores vasculares primarios. No obstante, estos factores no pueden explicar otras alteraciones observadas y que componen anormalidades tubulares primarias, como la mayor reabsorción en el túbulo contorneado proximal, probablemente condicionada por el crecimiento renal en la DBT y por la sobreexpresión del cotransportador SGLT2. Esta mayor reabsorción proximal generaría una menor llegada de solutos a la mácula densa (MD), lo cual sería incompatible con una acción del sistema de balance glomérulo tubular, pero sí con una acción mediada por el feedback túbuloglomerular (FBTG) que sensaría esta disminución de la concentración de ClNa en la MD, desactivando el FBTG y produciendo vasodilatación de la AA, con el consiguiente aumento del filtrado glomerular (FG) y del flujo plasmático renal (FPR), característicos del proceso de HF. Estos dos procesos (vascular y tubular) podrían actuar en forma sinérgica o simultánea, dependiendo de las condiciones metabólicas y evolutivas de la enfermedad renal diabética. Similares mecanismos podrían explicar la paradoja de la sal, por la cual una dieta baja en sal exacerbaría el fenómeno de HF, y una dieta alta en sal disminuiría el FG y el FPR, lo cual podría tener implicancias clínicas inesperadas. A las medidas terapéuticas habituales del control metabólico estricto, la dieta hipoproteica y el uso de IECA o bloqueantes AT1, no testeados clínicamente para este fin, pero de extendido uso clínico, parecen agregarse los nuevos inhibidores específicos del cotransportador SGLT2, que han demostrado efectos beneficiosos en varios aspectos del manejo de los diabéticos y ya existen algunos trabajos con efecto específico sobre la HF que parecen ser alentadores. Menos experiencia existe con el uso potencial del péptido C, como herramienta terapéutica en estas situaciones clínicas. Es evidente que determinar con más claridad los mecanismos involucrados en este complejo fenómeno, permitirá un mejor conocimiento del mismo y un mejor abordaje terapéutico.

Citas

Hostetter TH, Troy JL, Brenner BM. Glomerular hemodynamics in experimental diabetes mellitus. Kidney Int. 1981;19:410-5.

O’Donnell MP, Kasiske BL, Keane WF. Glomerular hemodynamic and structural alterations in experimental diabetes mellitus. FASEB J. 1988;2:2339-47.

Carmines PK BJ, Ishii N. Altered renal microvascular function in early diabetes. In: Cortes P MC, ed. The diabetic kidney. Totowa, NJ: Humana

Press; 2006. p. 23–36.

Tucker BJ, Collins RC, Ziegler MG, et al. Disassociation between glomerular hyperfiltration and extracellular volume in diabetic rats. Kidney Int. 1991;39:1176-83.

Miracle CM, Rieg T, Mansoury H, et al. Ornithine decarboxylase inhibitor eliminates hyperresponsiveness of the early diabetic proximal tubule to dietary salt. Am J Physiol Renal Physiol. 2008;295:F995-F1002.

Blantz RC, Singh P. Glomerular and tubular function in the diabetic kidney. Adv Chronic Kidney Dis. 2014;21:297-303.

Carmines PK. The renal vascular response to diabetes. Curr Opin Nephrol Hypertens. 2010;19:85-90.

Vallon V, Komers R. Pathophysiology of the diabetic kidney. Compr Physiol. 2011;1:1175-232.

Wada J, Makino H. Inflammation and the pathogenesis of diabetic nephropathy. Clin Sci (Lond). 2013;124:139-52.

Jerums G, Premaratne E, Panagiotopoulos S, et al. The clinical significance of hyperfiltration in diabetes. Diabetologia. 2010;53:2093-104.

Magee GM, Bilous RW, Cardwell CR, et al. Is hyperfiltration associated with the future risk of developing diabetic nephropathy? A meta-analysis.

Diabetologia. 2009;52:691-7.

Mogensen CE. Prediction of clinical diabetic nephropathy in IDDM patients. Alternatives to microalbuminuria? Diabetes. 1990;39:761-7.

Persson P, Hansell P, Palm F. Tubular reabsorption and diabetes-induced glomerular hyperfiltration. Acta Physiol (Oxf). 2010;200:3-10.

Frische S. Glomerular filtration rate in early diabetes: ongoing discussions of causes and mechanisms. J Nephrol. 2011;24:537-40.

Satirapoj B. Nephropathy in diabetes. Adv Exp Med Biol. 2012;771:107-22.

Wesson DE. Moving closer to an understanding of the hyperfiltration of type 2 diabetes mellitus. Am J Physiol Regul Integr Comp Physiol. 2006;290:R973-4.

Melsom T, Mathisen UD, Ingebretsen OC, et al. Impaired fasting glucose is associated with renal hyperfiltration in the general population. Diabetes Care. 2011;34:1546-51.

Mogensen CE, Andersen MJ. Increased kidney size and glomerular filtration rate in early juvenile diabetes. Diabetes. 1973;22:706-12.

Schmitz RA, Gaffney FA, Scandling DM, et al. Effects of orthostatic and anti-orthostatic stress on patent and stenotic coronary arteries in

swine. Aviat Space Environ Med. 1993;64:839-44.

Damsgaard EM, Mogensen CE. Microalbuminuria in elderly hyperglycaemic patients and controls. Diabet Med. 1986;3:430-5.

Gragnoli G, Signorini AM, Tanganelli I, et al. Prevalence of glomerular hyperfiltration and nephromegaly in normoand microalbuminuric type 2

diabetic patients. Nephron. 1993;65:206-11.

Vora J, Cooper J, Thomas JP. Polyarteritis nodosa presenting with hypertensive encephalopathy. Br J Clin Pract. 1992;46:144-5.

Rius F, Rey MJ. Behavioral disturbances and disorientation in a 67-year-old woman. Med Clin (Barc). 1994;103:229-35.

Vedel P, Obel J, Nielsen FS, et al. Glomerular hyperfiltration in microalbuminuric NIDDM patients. Diabetologia. 1996;39:1584-9.

Sasson AN, Cherney DZ. Renal hyperfiltration related to diabetes mellitus and obesity in human disease. World J Diabetes. 2012;3:1-6.

Thomas MC, Moran JL, Harjutsalo V, et al. Hyperfiltration in type 1 diabetes: does it exist and does it matter for nephropathy? Diabetologia. 2012;55:1505-13.

Rius FC, Massaguer Avelli JM. Classification of cervical adenopathies. Acta Otorinolaryngol Iber Am. 1969;20:246-50.

Premaratne E, Macisaac RJ, Tsalamandris C, et al. Renal hyperfiltration in type 2 diabetes: effect of age-related decline in glomerular filtration rate. Diabetologia. 2005;48:2486-93.

Chagnac A, Herskovitz P, Weinstein T, et al. The peritoneal membrane in peritoneal dialysis patients: estimation of its functional surface area by applying stereologic methods to computerized tomography scans. J Am Soc Nephrol. 1999;10:342-6.

Monami M, Pala L, Bardini G, et al. Glomerular hyperfiltration and metabolic syndrome: results from the FIrenze-BAgno A Ripoli (FIBAR) Study. Acta Diabetol. 2009;46:191-6.

Knight SF, Imig JD. Obesity, insulin resistance, and renal function. Microcirculation. 2007;14:349-62.

Myers BD, Nelson RG, Williams GW, et al. Glomerular function in Pima Indians with noninsulindependent diabetes mellitus of recent onset. J Clin

Invest. 1991;88:524-30.

Palmisano JJ, Lebovitz HE. Renal function in black americans with type II diabetes. J Diabet Complications. 1989;3:40-4.

Vora JP, Dolben J, Williams JD, et al. Impact of initial treatment on renal function in newly-diagnosed type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia. 1993;36:734-40.

Nelson RG, Bennett PH, Beck GJ, et al. Development and progression of renal disease in Pima Indians with non-insulin-dependent diabetes

mellitus. Diabetic Renal Disease Study Group. N Engl J Med. 1996;335:1636-42.

Brenner BM, Lawler EV, Mackenzie HS. The hyperfiltration theory: a paradigm shift in nephrology. Kidney Int. 1996;49:1774-7.

Stanton RC. Sodium glucose transport 2 (SGLT2) inhibition decreases glomerular hyperfiltration: is there a role for SGLT2 inhibitors in diabetic kidney disease? Circulation. 2014;129:542-4.

Amin R, Turner C, van Aken S, et al. The relationship between microalbuminuria and glomerular filtration rate in young type 1 diabetic subjects: The Oxford Regional Prospective Study. Kidney Int. 2005;68:1740-9.

Dahlquist G, Stattin EL, Rudberg S. Urinary albumin excretion rate and glomerular filtration rate in the prediction of diabetic nephropathy; a

long-term follow-up study of childhood onset type-1 diabetic patients. Nephrol Dial Transplant. 2001;16:1382-6.

Mogensen CE. Early glomerular hyperfiltration in insulin-dependent diabetics and late nephropathy. Scand J Clin Lab Invest. 1986;46:201-6.

Rudberg S, Persson B, Dahlquist G. Increased glomerular filtration rate as a predictor of diabetic nephropathy, an 8-year prospective study. Kidney Int. 1992;41:822-8.

Steinke JM, Sinaiko AR, Kramer MS, et al. The early natural history of nephropathy in Type 1 Diabetes: III. Predictors of 5-year urinary albumin excretion rate patterns in initially normoalbuminuric patients. Diabetes. 2005;54:2164-71.

Caramori ML, Gross JL, Pecis M, et al. Glomerular filtration rate, urinary albumin excretion rate, and blood pressure changes in normoalbuminuric normotensive type 1 diabetic patients: an 8-year follow-up study. Diabetes Care. 1999;22:1512-6.

Mogensen CE, Christensen CK. Predicting diabetic nephropathy in insulin-dependent patients. N Engl J Med. 1984;311:89-93.

Lervang HH, Jensen S, Brochner-Mortensen J, et al. Early glomerular hyperfiltration and the development of late nephropathy in type 1 (insulin-dependent) diabetes mellitus. Diabetologia. 1988;31:723-9.

Ruggenenti P, Porrini EL, Gaspari F, et al. Glomerular hyperfiltration and renal disease progression in type 2 diabetes. Diabetes Care. 2012;35:2061-8.

Yip JW, Jones SL, Wiseman MJ, et al. Glomerular hyperfiltration in the prediction of nephropathy in IDDM: a 10-year follow-up study. Diabetes. 1996;45:1729-33.

Ficociello LH, Perkins BA, Roshan B, et al. Renal hyperfiltration and the development of microalbuminuria in type 1 diabetes. Diabetes Care. 2009;32:889-93.

Cotroneo P, Manto A, Todaro L, et al. Hyperfiltration in patients with type I diabetes mellitus: a prevalence study. Clin Nephrol. 1998;50:214-7.

Rossing P, Tarnow L, Nielsen FS, et al. Low birth weight. A risk factor for development of diabetic nephropathy? Diabetes. 1995;44:1405-7.

Chang S, Caramori ML, Moriya R, et al. Having one kidney does not accelerate the rate of development of diabetic nephropathy lesions in type 1 diabetic patients. Diabetes. 2008;57:1707-11.

Rudberg S, Osterby R, Dahlquist G, et al. Predictors of renal morphological changes in the early stage of microalbuminuria in adolescents with IDDM. Diabetes Care. 1997;20:265-71.

Berg UB, Torbjornsdotter TB, Jaremko G, et al. Kidney morphological changes in relation to long-term renal function and metabolic control in adolescents with IDDM. Diabetologia. 1998;41:1047-56.

Drummond K, Mauer M. The early natural history of nephropathy in type 1 diabetes: II. Early renal structural changes in type 1 diabetes. Diabetes. 2002;51:1580-7.

Andrianesis V, Doupis J. The role of kidney in glucose homeostasis, SGLT2 inhibitors, a new approach in diabetes treatment. Expert Rev Clin Pharmacol. 2013;6:519-39.

Guyton AC, Hall JE. Urine formation by the kidneys: II tubular processing of the glomerular filtrate. En: Guyton AC ed. Textbook Of Medical Physiology. Philadelphia, Penn. : Elsevier-Saunders, 2006; p. 327–47.

Wright EM, Hirayama BA, Loo DF. Active sugar transport in health and disease. J Intern Med. 2007;261:32-43

Chen LH, Leung PS. Inhibition of the sodium glucose co-transporter-2: its beneficial action and potential combination therapy for type 2 diabetes mellitus. Diabetes Obes Metab. 2013;15:392-402.

Wright EM, Loo DD, Hirayama BA. Biology of human sodium glucose transporters. Physiol Rev. 2011;91:733-94.

Barfuss DW, Schafer JA. Differences in active and passive glucose transport along the proximal nephron. Am J Physiol. 1981;241:F322-32.

Vallon V, Platt KA, Cunard R, et al. SGLT2 mediates glucose reabsorption in the early proximal tubule. J Am Soc Nephrol. 2011;22:104-12.

Rieg T, Masuda T, Gerasimova M, et al. Increase in SGLT1-mediated transport explains renal glucose reabsorption during genetic and pharmacologic SGLT2 inhibition in euglycemia. Am J Physiol Renal Physiol. 2014;306:F188-93.

Kumpers P, Hafer C, Lukasz A, et al. Serum neutrophil gelatinase-associated lipocalin at inception of renal replacement therapy predicts survival in critically ill patients with acute kidney injury. Crit Care. 2010;14:R9.

Mogensen CE. Maximum tubular reabsorption capacity for glucose and renal hemodynamcis during rapid hypertonic glucose infusion in normal and diabetic subjects. Scand J Clin Lab Invest. 1971;28:101-9.

Vestri S, Okamoto MM, de Freitas HS, 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;182:105-12.

Marks J, Carvou NJ, Debnam ES, et al. Diabetes increases facilitative glucose uptake and GLUT2 expression at the rat proximal tubule brush border membrane. J Physiol. 2003;553:137-45.

Rahmoune H, Thompson PW, Ward JM, et al. Glucose transporters in human renal proximal tubular cells isolated from the urine of patients with non-insulin-dependent diabetes. Diabetes. 2005;54:3427-34.

Guder WG, Ross BD. Enzyme distribution along the nephron. Kidney Int. 1984;26:101-11.

Wirthensohn G, Guder WG. Renal substrate metabolism. Physiol Rev. 1986;66:469-97.

Schoolwerth AC, Smith BC, Culpepper RM. Renal gluconeogenesis. Miner Electrolyte Metab. 1988;14:347-61.

Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54:1615-25.

Heilig CW, Kreisberg JI, Freytag S, et al. Antisense GLUT-1 protects mesangial cells from glucose induction of GLUT-1 and fibronectin expression. Am J Physiol Renal Physiol. 2001;280:F657-66.

Morrisey K, Steadman R, Williams JD, et al. Renal proximal tubular cell fibronectin accumulation in response to glucose is polyol pathway dependent. Kidney Int. 1999;55:160-7.

Kanwar YS, Wada J, Sun L, et al. Diabetic nephropathy: mechanisms of renal disease progression. Exp Biol Med. (Maywood) 2008;233:4-11.

Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414:813-20.

Tan AL, Forbes JM, Cooper ME. AGE, RAGE, and ROS in diabetic nephropathy. Semin Nephrol. 2007;27:130-43.

Schena FP, Gesualdo L. Pathogenetic mechanisms of diabetic nephropathy. J Am Soc Nephrol. 2005;16(Suppl 1):S30-3.

Jandeleit-Dahm K, Cooper ME. Hypertension and diabetes: role of the renin-angiotensin system. Endocrinol Metab Clin North Am. 2006;35:469-90,vii.

Christiansen JS, Gammelgaard J, Orskov H, et al. Kidney function and size in normal subjects before and during growth hormone administration for one week. Eur J Clin Invest. 1981;11:487-90.

Christiansen JS, Gammelgaard J, Tronier B, et al. Kidney function and size in diabetics before and during initial insulin treatment. Kidney Int. 1982;21:683-8.

Parving HH, Christiansen JS, Noer I, et al. The effect of glucagon infusion on kidney function in short-term insulin-dependent juvenile diabetics. Diabetologia. 1980;19:350-4.

Stackhouse S, Miller PL, Park SK, et al. Reversal of glomerular hyperfiltration and renal hypertrophy by blood glucose normalization in diabetic rats. Diabetes. 1990;39:989-95.

Tucker BJ, Anderson CM, Thies RS, et al. Glomerular hemodynamic alterations during acute hyperinsulinemia in normal and diabetic rats. Kidney Int. 1992;42:1160-8.

Hills CE, Brunskill NJ, Squires PE. C-peptide as a therapeutic tool in diabetic nephropathy. Am J Nephrol. 2010;31:389-97.

Huang DY, Richter K, Breidenbach A, et al. Human C-peptide acutely lowers glomerular hyperfiltration and proteinuria in diabetic rats: a doseresponse study. Naunyn Schmiedebergs Arch Pharmacol. 2002;365:67-73.

Rebsomen L, Khammar A, Raccah D, et al. C-Peptide effects on renal physiology and diabetes. Exp Diabetes Res. 2008;2008:281536.

Forst T, Kunt T, Pfutzner A, et al. New aspects on biological activity of C-peptide in IDDM patients. Exp Clin Endocrinol Diabetes. 1998;106:270-6.

Horwitz DL, Starr JI, Mako ME, et al. Proinsulin, insulin, and C-peptide concentrations in human portal and peripheral blood. J Clin Invest. 1975;55:1278-83.

Samnegard B, Jacobson SH, Jaremko G, et al. Effects of C-peptide on glomerular and renal size and renal function in diabetic rats. Kidney Int. 2001;60:1258-65.

Johansson BL, Sjoberg S, Wahren J. The influence of human C-peptide on renal function and glucose utilization in type 1 (insulin-dependent) diabetic patients. Diabetologia. 1992;35:121-8.

Samnegard B, Jacobson SH, Jaremko G, et al. C-peptide prevents glomerular hypertrophy and mesangial matrix expansion in diabetic rats. Nephrol Dial Transplant. 2005;20:532-8.

Samnegard B, Jacobson SH, Johansson BL, et al. C-peptide and captopril are equally effective in lowering glomerular hyperfiltration in diabetic rats. Nephrol Dial Transplant. 2004;19:1385-91.

Nordquist L, Wahren J. C-Peptide: the missing link in diabetic nephropathy? Rev Diabet Stud. 2009;6:203-10.

Nordquist L, Lai EY, Sjoquist M, et al. Proinsulin C-peptide constricts glomerular afferent arterioles in diabetic mice. A potential renoprotective mechanism. Am J Physiol Regul Integr Comp Physiol. 2008;294:R836-41.

Pihl L, Persson P, Fasching A, et al. Insulin induces the correlation between renal blood flow and glomerular filtration rate in diabetes:

implications for mechanisms causing hyperfiltration. Am J Physiol Regul Integr Comp Physiol. 2012;303:R39-47.

Troncoso Brindeiro CM, Fallet RW, Lane PH, et al. Potassium channel contributions to afferent arteriolar tone in normal and diabetic rat kidney. Am J Physiol Renal Physiol. 2008;295:F171-8.

Carmines PK, Ohishi K, Ikenaga H. Functional impairment of renal afferent arteriolar voltage-gated calcium channels in rats with diabetes mellitus. J Clin Invest. 1996;98:2564-71.

Hetrick EM, Schoenfisch MH. Analytical chemistry of nitric oxide. Annu Rev Anal Chem. (Palo Alto Calif) 2009;2:409-33.

Prabhakar SS. Role of nitric oxide in diabetic nephropathy. Semin Nephrol. 2004;24:333-44.

Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1980;288:373-6.

Munger K. The renal circulations and glomerular ultrafiltration. En: Taal MW, Chertow GM, Marsden PA, et al. Brenner and Rector´s The Kidney. 9th ed. Philadelphia, PA: Elsevier, Saunders, 2012; p. 94-137.

Blantz RC, Deng A, Lortie M, et al. The complex role of nitric oxide in the regulation of glomerular ultrafiltration. Kidney Int. 2002;61:782-5.

Mount PF, Power DA. Nitric oxide in the kidney: functions and regulation of synthesis. Acta Physiol. (Oxf) 2006;187:433-46.

Artificial kidney bibliography. Michigan: University of Michigan Library, 2009.

Levin-Iaina N, Iaina A, Raz I. The emerging role of NO and IGF-1 in early renal hypertrophy in STZ-induced diabetic rats. Diabetes Metab Res

Rev. 2011;27:235-43.

Komers R, Anderson S. Paradoxes of nitric oxide in the diabetic kidney. Am J Physiol Renal Physiol. 2003;284:F1121-37.

Brands MW, Bell TD, Gibson B. Nitric oxide may prevent hypertension early in diabetes by counteracting renal actions of superoxide. Hypertension. 2004;43:57-63.

Cherney DZ, Scholey JW, Miller JA. Insights into the regulation of renal hemodynamic function in diabetic mellitus. Curr Diabetes Rev. 2008;4:280-90.

Cherney DZ, Reich HN, Jiang S, et al. Hyperfiltration and effect of nitric oxide inhibition on renal and endothelial function in humans with uncomplicated type 1 diabetes mellitus. Am J Physiol Regul Integr Comp Physiol. 2012;303:R710-8.

Komers R, Oyama TT, Chapman JG, et al. Effects of systemic inhibition of neuronal nitric oxide synthase in diabetic rats. Hypertension. 2000;35:655-61.

O’Byrne S, Forte P, Roberts LJ 2nd, et al. Nitric oxide synthesis and isoprostane production in subjects with type 1 diabetes and normal

urinary albumin excretion. Diabetes. 2000;49:857-62.

Chiarelli F, Cipollone F, Romano F, et al. Increased circulating nitric oxide in young patients with type 1 diabetes and persistent microalbuminuria: relation to glomerular hyperfiltration. Diabetes. 2000;49:1258-63.

Montanari A, Biggi A, Cabassi A, et al. Renal hemodynamic response to L-arginine in uncomplicated, type 1 diabetes mellitus: the role of buffering anions and tubuloglomerular feedback. Am J Physiol Renal Physiol. 2012;303:F648-58.

Goligorsky MS, Chen J, Brodsky S. Workshop: endothelial cell dysfunction leading to diabetic nephropathy : focus on nitric oxide. Hypertension. 2001;37:744-8.

Mattar AL, Fujihara CK, Ribeiro MO, et al. Renal effects of acute and chronic nitric oxide inhibition in experimental diabetes. Nephron. 1996;74:136-43.

Tolins JP, Shultz PJ, Raij L, et al. Abnormal renal hemodynamic response to reduced renal perfusion pressure in diabetic rats: role of NO. Am J Physiol. 1993;265:F886-95.

Vallon V, Thomson S. Inhibition of local nitric oxide synthase increases homeostatic efficiency of tubuloglomerular feedback. Am J Physiol. 1995;269:F892-9.

Vallon V, Traynor T, Barajas L, et al. Feedback control of glomerular vascular tone in neuronal nitric oxide synthase knockout mice. J Am Soc Nephrol. 2001;12:1599-606.

Levine DZ. Hyperfiltration, nitric oxide, and diabetic nephropathy. Curr Hypertens Rep. 2006;8:153-7.

Brooks B, Delaney-Robinson C, Molyneaux L, et al. Endothelial and neural regulation of skin microvascular blood flow in patients with diabetic

peripheral neuropathy: effect of treatment with the isoform-specific protein kinase C beta inhibitor, ruboxistaurin. J Diabetes Complications. 2008;22:88-95.

Lockhart CJ, Agnew CE, McCann A, et al. Impaired flow-mediated dilatation response in uncomplicated Type 1 diabetes mellitus: influence of shear stress and microvascular reactivity. Clin Sci. (Lond) 2011;121:129-39.

Henry RM, Ferreira I, Kostense PJ, et al. Type 2 diabetes is associated with impaired endotheliumdependent, flow-mediated dilation, but impaired glucose metabolism is not; The Hoorn Study. Atherosclerosis. 2004;174:49-56.

Hiragushi K, Sugimoto H, Shikata K, et al. Nitric oxide system is involved in glomerular hyperfiltration in Japanese normo- and micro-albuminuric patients with type 2 diabetes. Diabetes Res Clin Pract. 2001;53:149-59.

Montanari A, Pela G, Musiari L, et al. Nitric oxideangiotensin II interactions and renal hemodynamic function in patients with uncomplicated type 1 diabetes. Am J Physiol Renal Physiol. 2013;305:F42-51.

Bech JN, Nielsen CB, Ivarsen P, et al. Dietary sodium affects systemic and renal hemodynamic response to NO inhibition in healthy humans. Am J Physiol. 1998;274:F914-23.

Llinas MT, Gonzalez JD, Nava E, et al. Role of angiotensin II in the renal effects induced by nitric oxide and prostaglandin synthesis inhibition. J Am Soc Nephrol. 1997;8:543-50.

Sigmon DH, Carretero OA, Beierwaltes WH. Angiotensin dependence of endothelium-mediated renal hemodynamics. Hypertension. 1992;20:643-50.

Hollenberg NK, Price DA, Fisher ND, et al. Glomerular hemodynamics and the renin-angiotensin system in patients with type 1 diabetes mellitus. Kidney Int. 2003;63:172-8.

Lansang MC, Hollenberg NK. Renal perfusion and the renal hemodynamic response to blocking the renin system in diabetes: are the forces leading to vasodilation and vasoconstriction linked? Diabetes. 2002;51:2025-8.

Miller JA. Impact of hyperglycemia on the renin angiotensin system in early human type 1 diabetes mellitus. J Am Soc Nephrol. 1999;10:1778-85.

Price DA, Porter LE, Gordon M, et al. The paradox of the low-renin state in diabetic nephropathy. J Am Soc Nephrol. 1999;10:2382-91.

Sochett EB, Cherney DZ, Curtis JR, et al. Impact of renin angiotensin system modulation on the hyperfiltration state in type 1 diabetes. J Am Soc Nephrol. 2006;17:1703-9.

Eleftheriadis T, Antoniadi G, Pissas G, et al. The renal endothelium in diabetic nephropathy. Ren Fail. 2013;35:592-9.

Forbes JM, Coughlan MT, Cooper ME. Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes. 2008;57:1446-54.

Griendling KK, Ushio-Fukai M, Lassegue B, et al. Angiotensin II signaling in vascular smooth muscle. New concepts. Hypertension. 1997;29:366-73.

Ohishi K, Carmines PK. Superoxide dismutase restores the influence of nitric oxide on renal arterioles in diabetes mellitus. J Am Soc Nephrol. 1995;5:1559-66.

Schnackenberg CG, Wilcox CS. The SOD mimetic tempol restores vasodilation in afferent arterioles of experimental diabetes. Kidney Int. 2001;59:1859-64.

Koya D, Lee IK, Ishii H, et al. Prevention of glomerular dysfunction in diabetic rats by treatment with d-alpha-tocopherol. J Am Soc Nephrol. 1997;8:426-35.

Palm F, Cederberg J, Hansell P, et al. Reactive oxygen species cause diabetes-induced decrease in renal oxygen tension. Diabetologia. 2003;46:1153-60.

Chen YF, Li PL, Zou AP. Oxidative stress enhances the production and actions of adenosine in the kidney. Am J Physiol Regul Integr Comp Physiol. 2001;281:R1808-16.

Komers R, Lindsley JN, Oyama TT, et al. Immunohistochemical and functional correlations of renal cyclooxygenase-2 in experimental diabetes. J Clin Invest. 2001;107:889-98.

Li J, Chen YJ, Quilley J. Effect of tempol on renal cyclooxygenase expression and activity in experimental diabetes in the rat. J Pharmacol Exp Ther. 2005;314:818-24.

Chen YJ, Li J, Quilley J. Effect of inhibition of nitric oxide synthase on renal cyclooxygenase in the diabetic rat. Eur J Pharmacol. 2006;541:80-6.

Cherney DZ, Miller JA, Scholey JW, et al. The effect of cyclooxygenase-2 inhibition on renal hemodynamic function in humans with type 1 diabetes. Diabetes. 2008;57:688-95.

Cherney DZ, Miller JA, Scholey JW, et al. Renal hyperfiltration is a determinant of endothelial function responses to cyclooxygenase 2 inhibition in type 1 diabetes. Diabetes Care. 2010;33:1344-6.

Ortola FV, Ballermann BJ, Anderson S, et al. Elevated plasma atrial natriuretic peptide levels in diabetic rats. Potential mediator of J Clin Invest. 1987;80:670-4.

Zhang PL, Mackenzie HS, Troy JL, et al. Effects of an atrial natriuretic peptide receptor antagonist on glomerular hyperfiltration in diabetic rats. J Am Soc Nephrol. 1994;4:1564-70.

Vervoort G, Veldman B, Berden JH, et al. Glomerular hyperfiltration in type 1 diabetes mellitus results from primary changes in proximal tubular sodium handling without changes in volume expansion. Eur J Clin Invest. 2005;35:330-6.

Jacobs EM, Vervoort G, Branten AJ, et al. Atrial natriuretic peptide increases albuminuria in type I diabetic patients: evidence for blockade of tubular protein reabsorption. Eur J Clin Invest. 1999;29:109-15.

Benigni A, Colosio V, Brena C, et al. Unselective inhibition of endothelin receptors reduces renal dysfunction in experimental diabetes. Diabetes. 1998;47:450-6.

Kontessis PS, Jones SL, Barrow SE, et al. Effect of selective inhibition of thromboxane synthesis on renal function in diabetic nephropathy. J Lab Clin Med. 1993;121:415-23.

Uriu K, Kaizu K, Hashimoto O, et al. Acute and chronic effects of thromboxane A2 inhibition on the renal hemodynamics in streptozotocin-induced diabetic rats. Kidney Int. 1994;45:794-802.

Lansang MC, Price DA, Laffel LM, et al. Renal vascular responses to captopril and to candesartan in patients with type 1 diabetes mellitus. Kidney Int. 2001;59:1432-8.

Tikellis C, Brown R, Head GA, et al. Angiotensin Converting Enzyme 2 and hyperfiltration associated with diabetes. Am J Physiol Renal Physiol. 2014;306(7):F773-80.

Li N, Zimpelmann J, Cheng K, et al. The role of angiotensin converting enzyme 2 in the generation of angiotensin 1-7 by rat proximal tubules. Am J Physiol Renal Physiol. 2005;288:F353-62.

Rasch R. Tubular lesions in streptozotocin-diabetichyperfiltration. Diabetologia. 1984;27:32-7.

Christiansen JS, Gammelgaard J, Frandsen M, et al. Increased kidney size, glomerular filtration rate and renal plasma flow in short-term insulin-dependent diabetics. Diabetologia. 1981;20:451-6.

Rasch R, Dorup J. Quantitative morphology of the rat kidney during diabetes mellitus and insulin treatment. Diabetologia. 1997;40:802-9.

Seyer-Hansen K, Hansen J, Gundersen HJ. Renal hypertrophy in experimental diabetes. A morphometric study. Diabetologia. 1980;18:501-5.

Huang HC, Preisig PA. G1 kinases and transforming growth factor-beta signaling are associated with a growth pattern switch in diabetes-induced renal growth. Kidney Int. 2000;58:162-72.

Burns KD. Angiotensin II and its receptors in the diabetic kidney. Am J Kidney Dis. 2000;36:449-67.

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:C374-80.

Vallon V, Thomson SC. Renal function in diabetic disease models: the tubular system in the pathophysiology of the diabetic kidney. Annu Rev Physiol. 2012;74:351-75

Meier M, Park JK, Overheu D, et al. Deletion of protein kinase C-beta isoform in vivo reduces renal hypertrophy but not albuminuria in the streptozotocininduced diabetic mouse model. Diabetes. 2007;56:346-54.

Vallon V. The proximal tubule in the pathophysiology of the diabetic kidney. Am J Physiol Regul Integr Comp Physiol. 2011;300(5):R1009-22.

Lorenzen JM, Kielstein JT, Hafer C, et al. Circulating miR-210 predicts survival in critically ill patients with acute kidney injury. Clin J Am Soc Nephrol. 2011;6:1540-6.

Lorenzen JM, Hafer C, Faulhaber-Walter R, et al. Osteopontin predicts survival in critically ill patients with acute kidney injury. Nephrol Dial Transplant. 2011;26:531-7.

Pedersen SB, Flyvbjerg A, Richelsen B. Inhibition of renal ornithine decarboxylase activity prevents kidney hypertrophy in experimental diabetes. Am J Physiol. 1993;264:C453-6.

Pedersen SB, Flyvbjerg A, Gronbaek H, et al. Increased ornithine decarboxylase activity in kidneys undergoing hypertrophy in experimental diabetes. Mol Cell Endocrinol. 1992;86:67-72.

Deng A, Munger KA, Valdivielso JM, et al. Increased expression of ornithine decarboxylase in distal tubules of early diabetic rat kidneys: are polyamines paracrine hypertrophic factors? Diabetes. 2003;52:1235-9.

Thomson SC, Deng A, Bao D, et al. Ornithine decarboxylase, kidney size, and the tubular hypothesis of glomerular hyperfiltration in experimental diabetes. J Clin Invest. 2001;107:217-24.

Vallon V, Rose M, Gerasimova M, et al. Knockout of Na-glucose transporter SGLT2 attenuates hyperglycemia and glomerular hyperfiltration but not kidney growth or injury in diabetes mellitus. Am J Physiol Renal Physiol. 2013;304:F156-67.

Rasch R, Norgaard JO. Renal enlargement: comparative autoradiographic studies of 3H-thymidine uptake in diabetic and uninephrectomized rats. Diabetologia. 1983;25:280-7.

Bak M, Thomsen K, Christiansen T, et al. Renal enlargement precedes renal hyperfiltration in early experimental diabetes in rats. J Am Soc Nephrol. 2000;11:1287-92.

Satriano J, Vallon V. Primary kidney growth and its consequences at the onset of diabetes mellitus. Amino Acids. 2006;31:1-9.

Bognetti E, Zoja A, Meschi F, et al. Relationship between kidney volume, microalbuminuria and duration of diabetes mellitus. Diabetologia. 1996;39:1409.

Baumgartl HJ, Sigl G, Banholzer P, et al. On the prognosis of IDDM patients with large kidneys. Nephrol Dial Transplant. 1998;13:630-4.

Lawson ML, Sochett EB, Chait PG, et al. Effect of puberty on markers of glomerular hypertrophy and hypertension in IDDM. Diabetes. 1996;45:51-5.

Zerbini G, Bonfanti R, Meschi F, et al. Persistent renal hypertrophy and faster decline of glomerular filtration rate precede the development of microalbuminuria in type 1 diabetes. Diabetes. 2006;55:2620-5.

Kleinman KS, Fine LG. Prognostic implications of renal hypertrophy in diabetes mellitus. Diabetes Metab Rev. 1988;4:179-89.

Tobar A, Ori Y, Benchetrit S, et al. Proximal tubular hypertrophy and enlarged glomerular and proximal tubular urinary space in obese subjects with proteinuria. PLoS One. 2013;8:e75547.

Cupples WA. Interactions contributing to kidney blood flow autoregulation. Curr Opin Nephrol Hypertens. 2007;16:39-45.

Brenner & Rector’s the kidney. 9th ed. [edited by] Maarten W. Taal, et al. Philadelphia, PA: Elsevier-Saunders, 2012. 2 v. xxviii, 2868 p.

Cupples WA, Braam B. Assessment of renal autoregulation. Am J Physiol Renal Physiol. 2007;292:F1105-23.

Bayliss W. On the local reactions of the artrial wall to changes in internal pressure. J Physiol. 1902;28(3):220-31.

Just A. Mechanisms of renal blood flow autoregulation: dynamics and contributions. Am J Physiol Regul Integr Comp Physiol. 2007;292:R1-17.

Walker M 3rd, Harrison-Bernard LM, Cook AK, et al. Dynamic interaction between myogenic and TGF mechanisms in afferent arteriolar blood flow autoregulation. Am J Physiol Renal Physiol. 2000;279:F858-65.

Parving HH, Kastrup H, Smidt UM, et al. Impaired autoregulation of glomerular filtration rate in type 1 (insulin-dependent) diabetic patients with nephropathy. Diabetologia. 1984;27:547-52.

Ishida K, Ishibashi F, Takashina S. Comparison of renal hemodynamics in early non-insulin-dependent and insulin-dependent diabetes mellitus. J Diabet Complications. 1991;5:143-5.

Bell TD, DiBona GF, Wang Y, et al. Mechanisms for renal blood flow control early in diabetes as revealed by chronic flow measurement and transfer function analysis. J Am Soc Nephrol. 2006;17:2184-92.

Hashimoto S, Yamada K, Kawata T, et al. Abnormal autoregulation and tubuloglomerular feedback in prediabetic and diabetic OLETF rats. Am J Physiol Renal Physiol. 2009;296:F598-604.

Hashimoto Y, Ideura T, Yoshimura A, et al. Autoregulation of renal blood flow in streptozocin-induced diabetic rats. Diabetes. 1989;38:1109-13.

Lau C, Sudbury I, Thomson M, et al. Salt-resistant blood pressure and salt-sensitive renal autoregulation in chronic streptozotocin diabetes. Am J Physiol Regul Integr Comp Physiol. 2009;296:R1761-70.

Taejoon Hwang P, Kwon OD, Kim HJ, et al. Hyperglycemia Decreases the Expression of ATP Synthase beta Subunit and Enolase 2 in Glomerular Epithelial Cells. Tohoku J Exp Med. 2012;231:45-56.

Wei J, Shi Y, Hou Y, et al. Knockdown of thioredoxininteracting protein ameliorates high glucose-induced epithelial to mesenchymal transition in renal tubular epithelial cells. Cell Signal. 2013;25(12):2788-96.

Scherban T. [Neutrophils expression of adhesion molecules in diabetic nephropaty patients]. Georgian Med News. 2013:24-7.

Reddy MA, Tak Park J, Natarajan R. Epigenetic modifications in the pathogenesis of diabetic nephropathy. Semin Nephrol. 2013;33:341-53.

Jensen PK, Christiansen JS, Steven K, et al. Renal function in streptozotocin-diabetic rats. Diabetologia. 1981;21:409-14.

Zatz R, Dunn BR, Meyer TW, et al. Prevention of diabetic glomerulopathy by pharmacological amelioration of glomerular capillary hypertension. J Clin Invest. 1986;77:1925-30.

Zatz R, Meyer TW, Rennke HG, et al. Predominance of hemodynamic rather than metabolic factors in the pathogenesis of diabetic glomerulopathy. Proc Natl Acad Sci U S A. 1985;82:5963-7.

Ohishi K, Okwueze MI, Vari RC, et al. Juxtamedullary microvascular dysfunction during the hyperfiltration stage of diabetes mellitus. Am J Physiol. 1994;267:F99-105.

O’Donnell MP, Kasiske BL, Daniels FX, et al. Effects of nephron loss on glomerular hemodynamics and morphology in diabetic rats. Diabetes. 1986;35:1011-5.

Mauer SM, Steffes MW, Azar S, et al. The effects of Goldblatt hypertension on development of the glomerular lesions of diabetes mellitus in the rat. Diabetes. 1978;27:738-44.

Brochner-Mortensen J, Stockel M, Sorensen PJ, et al. Proximal glomerulo-tubular balance in patients with type 1 (insulin-dependent) diabetes mellitus. Diabetologia. 1984;27:189-92.

Hannedouche TP, Delgado AG, Gnionsahe DA, et al. Renal hemodynamics and segmental tubular reabsorption in early type 1 diabetes. Kidney Int. 1990;37:1126-33.

Mbanya JC, Thomas TH, Taylor R, et al. Increased proximal tubular sodium reabsorption in hypertensive patients with type 2 diabetes. Diabet Med. 1989;6:614-20.

Vidotti DB, Arnoni CP, Maquigussa E, et al. Effect of long-term type 1 diabetes on renal sodium and water transporters in rats. Am J Nephrol. 2008;28:107-14.

Vallon V. The proximal tubule in the pathophysiology of the diabetic kidney. Am J Physiol Regul Integr Comp Physiol. 2011;300:R1009-22.

Bank N, Aynedjian HS. Progressive increases in luminal glucose stimulate proximal sodium absorption in normal and diabetic rats. J Clin Invest. 1990;86:309-16.

O’Hagan M, Howey J, Greene SA. Increased proximal tubular reabsorption of sodium in childhood diabetes mellitus. Diabet Med. 1991;8:44-8.

Pollock CA, Lawrence JR, Field MJ. Tubular sodium handling and tubuloglomerular feedback in experimental diabetes mellitus. Am J Physiol. 1991;260:F946-52.

Vallon V, Blantz RC, Thomson S. Homeostatic efficiency of tubuloglomerular feedback is reduced in established diabetes mellitus in rats. Am J Physiol. 1995;269:F876-83.

Vallon V, Richter K, Blantz RC, et al. Glomerular hyperfiltration in experimental diabetes mellitus: potential role of tubular reabsorption. J Am Soc Nephrol. 1999;10:2569-76.

Singh P, Thomson SC. Renal homeostasis and tubuloglomerular feedback. Curr Opin Nephrol Hypertens. 2010;19:59-64.

Vallon V, Blantz R, Thomson S. The salt paradox and its possible implications in managing hypertensive diabetic patients. Curr Hypertens Rep. 2005;7:141-7.

Thomson SC, Vallon V, Blantz RC. Kidney function in early diabetes: the tubular hypothesis of glomerular filtration. Am J Physiol Renal Physiol. 2004;286:F8-15.

Vallon V, Blantz RC, Thomson S. Glomerular hyperfiltration and the salt paradox in early [corrected] type 1 diabetes mellitus: a tubulo-centric view. J Am Soc Nephrol. 2003;14:530-7.

González E, Salomonsson M, Muller-Suur C, et al. Measurements of macula densa cell volume changes in isolated and perfused rabbit cortical thick ascending limb. I. Isosmotic and anisosmotic cell volume changes. Acta Physiol Scand. 1988;133:149-57.

González E, Salomonsson M, Muller-Suur C, et al. Measurements of macula densa cell volume changes in isolated and perfused rabbit cortical thick ascending limb. II. Apical and basolateral cell osmotic water permeabilities. Acta Physiol Scand. 1988;133:159-66.

Vallon V. Tubuloglomerular feedback and the control of glomerular filtration rate. News Physiol Sci. 2003;18:169-74.

Persson AE, Lai EY, Gao X, et al. Interactions between adenosine, angiotensin II and nitric oxide on the afferent arteriole influence sensitivity of the tubuloglomerular feedback. Front Physiol. 2013;4:187.

Hanefeld M, Forst T. Dapagliflozin, an SGLT2 inhibitor, for diabetes. Lancet. 2010;375(9733):2196-8.

Washburn WN, Poucher SM. Differentiating sodiumglucose co-transporter-2 inhibitors in development for the treatment of type 2 diabetes mellitus. Expert Opin Investig Drugs. 2013;22:463-86.

Rizos EC, Elisaf MS. Sodium-glucose co-transporter 2 inhibition in diabetes treatment: current evidence and future perspectives. Curr Pharm Des. 2014;20(22):3647-56.

Said S, Hernandez GT. Sodium glucose co-transporter 2 (SGLT2) inhibition with canagliflozin in type 2 diabetes mellitus. Cardiovasc Hematol Agents Med Chem. 2013;11(3):203-6.

Fujita Y, Inagaki N. Renal sodium glucose cotransporter 2 inhibitors as a novel therapeutic approach to treatment of type 2 diabetes: Clinical data and mechanism of action. J Diabetes Investig. 2014;5(3):265-75.

De Nicola L, Gabbai FB, Liberti ME, et al. Sodium/Glucose Cotransporter 2 Inhibitors and prevention of diabetic nephropathy: targeting the renal tubule in diabetes. Am J Kidney Dis. 2014;64:16-24.

Barnett AH. Impact of sodium glucose cotransporter 2 inhibitors on weight in patients with type 2 diabetes mellitus. Postgrad Med. 2013;125(5):92-100.

Vasilakou D, Karagiannis T, Athanasiadou E, et al. Sodium-glucose cotransporter 2 inhibitors for type 2 diabetes: a systematic review and meta-analysis. Ann Intern Med. 2013;159:262-74.

Kurosaki E, Ogasawara H. Ipragliflozin and other sodium-glucose cotransporter-2 (SGLT2) inhibitors in the treatment of type 2 diabetes: preclinical and clinical data. Pharmacol Ther. 2013;139:51-9.

Cangoz S, Chang YY, Chempakaseril SJ, et al. The kidney as a new target for antidiabetic drugs: SGLT2 inhibitors. J Clin Pharm Ther. 2013;38:350-9.

Boyle LD, Wilding JP. Emerging sodium/glucose cotransporter 2 inhibitors for type 2 diabetes. Expert Opin Emerg Drugs. 2013;18:375-91.

Toderika Y, Ferguson N. Canagliflozin: a new class of antidiabetic agent targeting the sodium-glucose cotransporter. Cardiol Rev. 2014;22(2):97-104.

Nisly SA, Kolanczyk DM, Walton AM. Canagliflozin, a new sodium-glucose cotransporter 2 inhibitor, in the treatment of diabetes. Am J Health Syst Pharm. 2013;70:311-9.

Sällström J, Eriksson T, Fredholm BB, et al. Inhibition of sodium-linked glucose reabsorption normalizes diabetes-induced glomerular hyperfiltration in conscious adenosine A₁-receptor deficient mice. Acta Physiol (Oxf). 2014;210(2):440-5.

Vallon V, Gerasimova M, Rose MA, et al. SGLT2 inhibitor empagliflozin reduces renal growth and albuminuria in proportion to hyperglycemia and prevents glomerular hyperfiltration in diabetic Akita mice. Am J Physiol Renal Physiol. 2014;306:F194-204.

Lambers Heerspink HJ, de Zeeuw D, Wie L, et al. Dapagliflozin a glucose-regulating drug with diuretic properties in subjects with type 2 diabetes. Diabetes Obes Metab. 2013;15:853-62.

Musso G, Gambino R, Cassader M, et al. A novel approach to control hyperglycemia in type 2 diabetes: sodium glucose co-transport (SGLT) inhibitors: systematic review and meta-analysis of randomized trials. Ann Med. 2012;44:375-93.

List JF, Woo V, Morales E, et al. Sodium-glucose cotransport inhibition with dapagliflozin in type 2 diabetes. Diabetes Care. 2009;32:650-7.

Wilding JP, Woo V, Soler NG, et al. Long-term efficacy of dapagliflozin in patients with type 2 diabetes mellitus receiving high doses of insulin: a randomized trial. Ann Intern Med. 2012;156:405-15.

Cefalu WT, Leiter LA, Yoon KH, et al. Efficacy and safety of canagliflozin versus glimepiride in patients with type 2 diabetes inadequately controlled with metformin (CANTATA-SU): 52 week results from a randomised, double-blind, phase 3 non-inferiority trial. Lancet. 2013;382:941-50.

Kohan DE, Fioretto P, Tang W, et al. Long-term study of patients with type 2 diabetes and moderate renal impairment shows that dapagliflozin reduces weight and blood pressure but does not improve glycemic control. Kidney Int. 2014;85:962-71.

Cherney DZ, Perkins BA, Soleymanlou N, et al. Renal hemodynamic effect of sodium-glucose cotransporter 2 inhibition in patients with type 1 diabetes mellitus. Circulation. 2014;129:587-97.

Publicado
2014-09-01
Cómo citar
1.
Mascheroni CA. Fisiopatología de la hiperfiltración glomerular en la diabetes. Parte 1. Rev Nefrol Dial Traspl. [Internet]. 1 de septiembre de 2014 [citado 28 de marzo de 2024];34(3):130-54. Disponible en: http://vps-1689312-x.dattaweb.com/index.php/rndt/article/view/116
Sección
Artículo de Revisión