Genetic susceptibility and the role of hypertension in diabetic nephropathy

Current Opinion in Nephrology and Hypertension

Volumn 6, Issue 2, 1997, Pages 184-191

  Fogarty, Damian G ^a   Krolewski, Andrzej S ^b,c  

^a BELFAST CITY HOSPITAL   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

^c JOSLIN DIABETES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIABETES MELLITUS; DIABETIC NEPHROPATHY; GENETIC SUSCEPTIBILITY; HUMAN; HYPERTENSION; PRIORITY JOURNAL; REVIEW;

EID: 0030906197     PISSN: 10624821     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041552-199703000-00013     Document Type: Review

References (79)

1. United States Renal Data System: USRDS 1994 Annual Data Report: Incidence and causes of treated renal disease. Am J Kidney Dis 1994, 24(suppl):S48-S56.
2. The Diabetes Control and Complications Trial Research Group: The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 1993, 329:989-995.
3. Krolewski AS, Warram JH, Christlieb AR, Busick EJ, Kahn CR: The changing natural history of nephropathy in type I diabetes. Am J Med 1985, 78:785-794.
4. Seaquist ER, Goetz FC, Rich S, Barbosa J: Familial clustering of diabetic kidney disease. Evidence for genetic susceptibility to diabetic nephropathy. N Engl J Med 1989, 320:1161-1165.
5. Borch-Johnsen K, Norgaard K, Hommel E, Mathiesen ER, Jensen JS, Deckert T, Parving HH: Is diabetic nephropathy an inherited complication? Kidney Int 1992, 41:719-722.
6. Quinn M, Angelico MC, Warram JH, Krolewski AS: Familial factors determine the development of diabetic nephropathy in patients with IDDM. Diabetologia 1996, 39:940-945. Previous studies were criticized for positive selection of siblings concordant both for IDDM and for nephropathy. This study avoided ascertainment bias by using cohort and prevalence samples of IDDM patients with IDDM siblings. The cumulative risk of nephropathy in siblings after 25 years of post-puberty IDDM was 71.5% if the proband had persistent proteinuria and 25.4% if the proband did not.
7. Nelson RG, Pettitt DJ, Knowler WC, Bennett PH: Prediabetic blood pressure and familial predisposition to renal disease in Pima Indians with non-insulin-dependent diabetes mellitus. J Diabetes Complications 1995, 9:212-214.
8. Nosadini R, Brocco E, Faronato P, Sfriso A, Muollo B, Frigato F, Velussi M, Tonolo GC, Inchiostro S, Maioli M et al.: Clustering of abnormalities in albumin excretion rate in families of type 2 diabetic patients [Abstract]. Diabetologia 1996, 39:A298.
9. Strojek K, Grzeszczak W, Morawin E, Adamski M, Lacka B, Rudzki H, Keller CK, Schmidt S, Ritz E: Clinical manifestation of hereditary predisposition to nephropathy in type II diabetes [Abstract]. Diabetologia 1996, 39:A298.
10. Julian BA, Quiggins PA, Thompson JS, Woodford SY, Gleason K, Wyatt RJ: Familial IgA nephropathy: evidence of an inherited mechanism of disease. N Engl J Med 1985, 312:202-208.
11. Freedman BI, Bowden DW: The role of genetic factors in the development of end-stage renal disease. Curr Opin Nephrol Hypertens 1995, 4:230-234.
12. Freedman BI, Spray BJ, Tuttle AB, Buckalew JVM: The familial risk of end-stage renal disease in African Americans. Am J Kidney Dis 1993, 21:387-393.
13. Mogensen CE: Systemic blood pressure and glomerular leakage with particular reference to diabetes and hypertension. J Intern Med 1994, 235:297-316.
14. Hansen KW, Petersen MM, Christiansen JS, Mogensen CE: Diurnal blood pressure variations in normoalbuminuric type 1 diabetic patients. J Intern Med 1993, 234:75-180.
15. Microalbuminuria Collaborative Study Group UK: Risk factors for development of microalbuminuria in insulin dependent diabetic patients: a cohort study. Br Med J 1993, 306:1235-1239.
16. Mathiesen ER, Ronn B, Storm B, Foght H, Deckert T: The natural course of microalbuminuria in insulin-dependent diabetes: a 10-year prospective study. Diabetic Med 1995, 12:482-487.
17. Mogensen CE, Christensen CK: Predicting diabetic nephropathy in insulin-dependent patients. N Engl J Med 1984, 311:89-93.
18. Viberti GC, Keen H, Wiseman MJ: Raised arterial pressure in parents of proteinuric insulin dependent diabetics. Br Med J 1987, 295:515-517.
19. Krolewski AS, Canessa M, Warram JH, Laffel LM, Christlieb AR, Knowler WC, Rand LI: Predisposition to hypertension and susceptibility to renal disease in insulin-dependent diabetes mellitus. N Engl J Med 1988, 318:140-145.
20. Stattin EL, Rudberg S, Dahlquist G: Hereditary risk determinants of micro- and macroalbuminuria in young IDDM patients [Abstract]. Diabetologia 1996, 39:A299.
21. Cruickshanks KJ, Klein R, Klein BEK, Moss SE: Family history of hypertension and diabetic complications [Abstract]. Diabetes 1996, 45:215A.
22. Groop PH, Fagerudd J, Pettersson-Fernholm K, Gronhagen-Riska C: Abnormalities of glucose metabolism in parents of IDDM-patients with diabetic nephropathy [Abstract]. J Am Soc Nephrol 1996, 7:1358.
23. McCance DR, Hanson RL, Pettitt DJ, Jacobsson LT, Bennett PH, Bishop DT, Knowler WC: Diabetic nephropathy: a risk factor for diabetes mellitus in offspring. Diabetologia 1995, 38:221-226.
24. Tamsma JT, Sonnenberg A, Thalen EO, Sandkuijl LA, Lemkes HHPJ: Increased frequency of non-insulin-dependent diabetes mellitus in families of insulin-dependent patients with nephropathy [Abstract]. Diabetes 1996, 45:132A.
25. Breyer JA, Bain RP, Evans JK, Nahman NS Jr, Lewis EJ, Cooper M, McGill J, Berl T and the Collaborative Study Group: Predictors of the progression of renal insufficiency in patients with insulin-dependent diabetes and overt diabetic nephropathy. Kidney Int 1996, 50:1651-1658. This paper outlines the independent predictors of progression of diabetic nephropathy in the 409 patients in the clinical trial of angiotensin-converting enzyme inhibition with captopril. The risk factors that independently predicted progression were onset of IDDM later in life, parental diagnosis of IDDM, presence of edema, increased mean arterial pressure and an abnormal electrocardiograph. Laboratory factors that predicted progression included a low haematocrit, high blood sugar, high protein excretion and elevated serum creatinine.
26. Shoback DM, Williams GH, Moore TJ, Dluhy RG, Podolsky S, Hollenberg NK: Defect in the sodium-modulated responsiveness to angiotensin II in essential hypertension. J Clin Invest 1983, 72:2115-2124.
27. Lifton RP, Hopkins PN, Williams RR, Hollenberg NK, Williams GH, Dluhy RG: Evidence for heritability of non-modulating essential hypertension. Hypertension 1989, 13:884-889.
28. Tuck M, Corry D, Tujillo A: Salt sensitive blood pressure and exaggerated vascular reactivity in the hypertension of diabetes mellitus. Am J Med 1990, 68:210-216.
29. Hare JA, Ferriss JB, Brady D, Twomey B, O'Sullivan DJ: Exchangeable sodium and renin in hypertensive diabetic patients with and without nephropathy. Hypertension 1985, 7(suppl):43-48.
30. Mahnensmith RL, Aronsen PS: The plasma membrane sodiumhydrogen exchange and its role in physiological and pathophysiological processes. Circ Res 1985, 56:773-788.
31. Yip J, Mattock MB, Morocutti A, Sethi M, Trevisan R, Viberti G: Insulin resistance in insulin-dependent diabetic patients with microalbuminuria. Lancet 1993, 342:883-886.
32. Groop LC, Ekstrand A, Forsblom C, Widen E, Groop PH, Teppo AM, Erikssen J: Insulin resistance, hypertension and microalbuminuria in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 1993, 36:642-647.
33. Sharma AM: Salt sensitivity as a phenotype for genetic studies of human hypertension. Nephrol Dial Transplant 1996, 11:927-929.
34. Hostetter TH, Troy JL, Brenner BM: Glomerular hemodynamics in experimental diabetes mellitus. Kidney Int 1981, 19:410-415.
35. Mogensen CE: Glomerular hyperfiltration in human diabetes. Diabetes Care 1994, 17:770-775.
36. Nelson RG, Bennett PH, Beck GJ, Tan M, Knowler WC, Mitch WE, Hirschman GH, Myers BD, for the Diabetic Renal Disease Study Group: Development and progression of renal disease in Pima Indians with non-insulin-dependent diabetes mellitus. N Engl J Med 1996, 335:1636-1642. This elegant 4-year follow-up study investigated glomerular function in 194 Pima Indian patients selected to represent different stages in the development of diabetic nephropathy. Elevated GFR was demonstrated in newly diagnosed diabetic individuals, increasing further with the development of microalbuminuria before falling slowly and then more rapidly as overt proteinuria appeared. Higher base-line blood pressure predicted increasing urinary albumin excretion and a higher baseline albuminuria predicted a decline in GFR.
37. Pecis M, Gross JL, Azevedo MJ, Fischer A: Higher diastolic night/day ratio blood pressure is associated with glomerular hyperfiltration in normoalbuminuric insulin-dependent diabetic patients [Abstract]. Diabetes 1996, 45:275A.
38. Hannedouche TP, Marques LP, Natov S, Delgado AG, Boitard C, Lacour B, Grünfeld JP: Renal abnormalities in normotensive insulin-dependent diabetic offspring of hypertensive parents. Hypertension 1992, 19:378-384.
39. Campese VM: Salt-sensitivity in hypertension. Renal and cardiovascular complications. Hypertension 1994, 23:531-550.
40. Weir MR, Dengel DR, Mayuga RS, Kairis GM, Goldberg AP: Insulin resistance not dietary salt correlates with elevated glomerular filtration fraction in middle-aged, obese sedentary hypertensives [Abstract]. Am J Hypertens 1996, 9:130A.
41. Jenkins DAS, Cowan P, Collier A, Watson ML, Clarke BF: Blood glucose control determines the renal haemodynamic response to angiotensin converting enzyme inhibition in type 1 diabetes. Diabetic Med 1990, 7:252-257.
42. Rosskopf D, Dusing R, Siffert W: Membrane sodium-proton exchange and primary hypertension. Hypertension 1993, 21:607-617.
43. Walker JD, Tariq T, Viberti G: Sodium-lithium countertransport activity in red cells of patients with insulin dependent diabetes and nephropathy and their parents. Br Med J 1990, 301:635-638.
44. + countertransport) and risk of diabetic nephropathy in childhood diabetes. J Paediatr Child Health 1994, 30:547-549.
45. Boero R, Esposti ED, Fabrri A, Guarena C, Forneris G, Quarello F, Fusaroli M, Piccoli G: Increased sodium-lithium counter-transport activity in red cells of IgA nephropathy patients. Kidney Int 1991, 40:1118-1122.
46. Rosskopf D, Fromter E, Siffert W: Hypertensive sodium-proton exchanger phenotype persists in immortalised lymphoblasts from essential hypertensive patients - a cell culture model for human hypertension. J Clin Invest 1993, 92:2553-2559.
47. + antiporter phenotype, abundance, and phosphorylation of immortalised lymphoblasts from humans with hypertension. Hypertension 1995, 25:971-977. This study demonstrated that a post-translational alteration in the NHE may account for the elevated activity seen in patients with essential hypertension.
48. Thomas TH, Rutherford PA, West IC, Wilkinson R: Sulphydryl group control of sodium-lithium countertransport kinetics: a membrane protein control abnormality in essential hypertension. Eur J Clin Invest 1995, 25:235-240.
49. + antiport activity and cell growth in cultured skin fibroblasts of IDDM patients with nephropathy. Diabetes 1992, 41:1239-1246.
50. Morocutti A, Earle K, Sethi M, Piras G, Pal K, Richards D, Rodemann P, Viberti G: Premature senescence of skin fibroblasts from insulin-dependent diabetic patients with kidney disease. Kidney Int 1996, 50:250-256.
51. + antiporter. Kidney Int 1996, 50:1684-1693. In this study, fibroblasts from diabetic nephropathy patients demonstrated a growth phenotype characterized by cell hyperplasia. This abnormal growth pattern was only partly caused by elevated NHE activity.
52. Levy J, Gavin JR III, Sowers JR: Diabetes mellitus: a disease of abnormal cellular calcium metabolism? Am J Med 1994, 96:260-273.
53. Solini A, Di Virgilio F, Sfriso A, Bruseghin M, Crepaldi G, Nosadini R: Intracellular calcium handling by fibroblasts from non-insulin-dependent diabetic patients with and without hypertension and microalbuminuria. Kidney Int 1996, 50:618-626.
54. Krolewski AS, Laffel LM, Krolewski M, Quinn M, Warram JH: Glycosylated hemoglobin and the risk of micro-albuminuria in patients with insulin-dependent diabetes mellitus. N Engl J Med 1995, 332:1251-1255.
55. + exchange in the pathophysiology of essential hypertension. Am J Hypertens 1996, 9:703-707.
56. + antiporter as a candidate gene in human hypertension. Hypertension 1991, 17:8-14.
57. Doria A, Warram JH, Krolewski AS: Genetic susceptibility to nephropathy in insulin-dependent diabetes: from epidemiology to molecular genetics. Diabetes Metab Rev 1995, 11:287-314.
58. Whiteside CI, Thompson J: The role of angiotensin-II in progressive diabetic glomerulopathy in the rat. Endocrinology 1989, 125:1932-1940.
59. Campbell DJ, Lawrence AC, Towrie A, Kladis A, Valentijn AJ: Differential regulation of angiotensin peptide levels in plasma and kidney of the rat Hypertension 1991, 18:763-773.
60. Walker WG, Whelton PK, Saito H, Russel RP, Herman J: Relation between blood pressure and renin, renin substrate, angiotensin II, aldosterone, and urinary sodium and potassium in 574 ambulatory subjects. Hypertension 1979, 1:287-291.
61. Watt GC, Harrap SB, Foy CJ, Holton DW, Edwards HV, Davidson HR, Connor JM, Lever AF, Fraser R: Abnormalities of glucocorticoid metabolism and the renin-angiotensin system: a four corners approach to the identification of genetic determinants of blood pressure. J Hypertens 1992, 10:473-482.
62. Jeunemaitre X, Soubrier F, Kotelevtsev YV, Lifton RP, Williams CS, Charru A, Hunt SC, Hopkins PN, Williams RR, Lalouel JM, Corvol P: Molecular basis of human hypertension: role of angiotensinogen. Cell 1992, 71:169-180.
63. Caulfield M, Lavender P, Farrall M, Munroe P, Lawson M, Turner P, Clark AJ: Linkage of the angiotensinogen gene to essential hypertension. N Engl J Med 1994, 330:1629-1633.
64. Doria A, Onuma T, Gearin G, Freire MBS, Warram JH, Krolewski AS: Angiotensinogen polymorphism M235T, hypertension and nephropathy in insulin-dependent diabetes. Hypertension 1996, 27:1134-1139.
65. Fogarty DG, Harron JC, Hughes AE, Nevin NC, Doherty CC, Maxwell AP: A molecular variant of angiotensinogen is associated with diabetic nephropathy in IDDM. Diabetes 1996, 45:1204-1208.
66. Tarnow L, Cambien F, Rossing P, Nielsen FS, Hansen BV, Ricard S, Poirier O, Parving HH: Angiotensinogen gene polymorphisms in IDDM patients with diabetic nephropathy. Diabetes 1996, 45:367-369.
67. Dudley CRK, Keavney B, Stratton IM, Turner RC, Ratcliffe PJ: UK prospective diabetes study XV: Relationship of renin-angiotensin system gene polymorphisms with microalbuminuria in NIDDM. Kidney Int 1995, 48:1907-1911.
68. Hegele RA, Brunt JH, Connelly PW: A polymorphism of the angiotensinogen gene associated with variation in blood pressure in a genetic isolate. Circulation 1994, 90:2207-2212.
69. Warram JH, Laffel LM, Ganda OP, Christlieb AR: Coronary artery disease is the major determinant of excess mortality in patients with insulin-dependent diabetes mellitus and persistent proteinuria. J Am Soc Nephrol 1992, 3(suppl):S104-S110.
70. Ruiz J, Blanche H, Cohen N, Velho G, Cambien F, Cohen D, Passa P, Froguel P: Insertion/deletion polymorphism of the angiotensin-converting enzyme gene is strongly associated with coronary heart disease in non-insulin-dependent diabetes mellitus. Proc Natl Acad Sci USA 1994, 91:3662-3665.
71. Tarnow L, Cambien F, Rossing P, Nielsen FS, Hansen BV, Lecerf L, Poirier O, Danilov S, Boelskifte S, Borch-Johnsen K, Parving HH: Insertion/deletion polymorphism in the angiotensin-I converting enzyme gene is associated with coronary heart disease in IDDM patients with diabetic nephropathy. Diabetologia 1995, 38:798-803.
72. Schmidt S, Ritz E: The role of angiotensin I-converting enzyme gene polymorphism in renal disease. Curr Opin Nephrol Hypertens 1996, 5:552-555.
73. Spielman RS, McGinnis RE, Ewens WJ: Transmission test for linkage disequilibrium: the insulin gene region and insulin-dependent diabetes mellitus. Am J Hum Genet 1993, 52:506-516.
74. Hopkins PN, Litton RP, Hollenberg NK, Jeunemaitre X, Hallouin MC, Skuppin J, Williams CS, Dluhy RG, Lalouel JM, Williams RR, Williams GH: Blunted renal vascular response to angiotensin II is associated with a common variant of the angiotensinogen gene and obesity. J Hypertens 1996, 14:199-207. This clinical investigation demonstrated that individuals who are TT homozygotes at an AGT polymorphism have a blunted response to infused Ang II. This implies that this may be a molecular marker for 'non-modulating' salt-sensitive hypertension. Obesity also caused blunted response to Ang II infusion.
75. Velloso LA, Folli F, Sun XJ, White MF, Saad MJA, Khan CR: Cross-talk between the insulin and angiotensin signalling systems. Proc Natl Acad Sci USA 1996, 93:12490-12495. The levels of intracellular proteins downstream of the insulin receptor were altered by Ang II, infusion an effect completely inhibited by Ang type 1 receptor blockade. This confirms intracellular interactions between the insulin and Ang pathways distal to the receptors and may be relevant to the association of hypertension, diabetes and insulin resistance.
76. McKusick VA: Mendelian Inheritance in Man, 11th edn. Baltimore: Johns Hopkins University Press; 1994.
77. Davies JL, Kawakuchi Y, Bennett ST, Copeman JB, Cordell HJ, Pritchard LE, Reed PW, Gough SCL, Jenkins SC, Palmer SM et al.: A genome-wide search for human type-I diabetes susceptibility genes. Nature 1994, 371:130-136.
78. Rogus JJ, Krolewski AS: Using discordant sib-pairs to map loci for qualitative traits with high sibling recurrence rate. Am J Hum Genet 1996, 59:1376-1381. This paper proposes the theory and simulation for a strategy using discordant sib-pairs to map genetic loci for polygenic diseases where there is high sibling recurrence risk. Using a model based on diabetic nephropathy in IDDM this strategy would achieve the same power as an affected sib-pair study but only using a quarter of the sib-pairs.
79. Santiago JV: Lessons from the Diabetes Control and Complications Trial. Diabetes 1993, 42:1549-1554.