Increased renal sympathetic nerve activity leads to hypertension and renal dysfunction in offspring from diabetic mothers

American Journal of Physiology - Renal Physiology

Volumn 304, Issue 2, 2013, Pages

  Rodrigues, Aline Fernanda de Almeida Chaves ^a   de Lima, Ingrid Lauren Brites ^a   Bergamaschi, Cássia Toledo ^a   Campos, Ruy Ribeiro ^a   Hirata, Aparecida Emiko ^a   Schoorlemmer, Guus Hermanus Maria ^a   Gomes, Guiomar Nascimento ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Denervation; Maternal diabetes; Renal baroreflex control

Indexed keywords

SODIUM; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; GLOMERULUS FILTRATION RATE; HYPERTENSION; KIDNEY DENERVATION; KIDNEY DISEASE; KIDNEY FUNCTION; MALE; MATING; NONHUMAN; PRESSORECEPTOR; PRIORITY JOURNAL; PROGENY; RAT; SODIUM EXCRETION; SYMPATHETIC NERVE; SYMPATHETIC NERVE ACTIVITY; SYSTOLIC BLOOD PRESSURE; WESTERN BLOTTING;

EID: 84872386603     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00241.2012     Document Type: Article

References (68)

1. Aceti A, Santhakumaran S, Logan K, Philipps L, Prior E, Gale C, Hyde M, Modi N. The diabetic pregnancy and offspring blood pressure in childhood: a systematic review and meta-analysis. Diabetologia 55: 3114-3127, 2012.
2. Agoudemos M, Reinking BE, Koppenhafer SL, Segar JL, Scholz TD. Programming of adult cardiovascular disease following exposure to lategestation hyperglycemia. Neonatology 100: 198-205, 2011.
3. Alexander BT, Hendon AE, Ferril G, Dwyer TM. Renal denervation abolishes hypertension in low-birth-weight offspring from pregnant rats with reduced uterine perfusion. Hypertension 45: 754-758, 2005.
4. Alexander BT, Hendon AE, Ferril G, Dwyer TM. Renal denervation abolishes hypertension in low-birth-weight offspring from pregnant rats with reduced uterine perfusion. Hypertension 45: 754-758, 2005.
5. Anderson EA, Sinkey CA, Lawton WJ, Mark AL. Elevated sympathetic nerve activity in borderline hypertensive humans. Evidence from direct intraneural recordings. Hypertension 14: 177-183, 1989.
6. Arnold AC, Shaltout HA, Gallagher PE, Diz DI. Leptin impairs cardiovagal baroreflex function at the level of the solitary tract nucleus. Hypertension 54: 1001-1008, 2009.
7. Barker DJP. Developmental origins of adult health and disease. J Epidemiol Community Health 58: 114-115, 2004.
8. Bello-Reuss E, Pastoriza-Munoz E, Colindres RE. Acute unilateral renal denervation in rats with extracellular volume expansion. Am J Physiol Renal Fluid Electrolyte Physiol 232: F26-F32, 1977.
9. Bristow JD, Honour AJ, Pickering GW, Sleight P, Smyth HS. Diminished baroreflex sensitivity in high blood pressure. Circulation 39: 48-54, 1969.
10. Campese VM, Ye S, Zhong H, Yanamadala V, Ye Z, Chiu J. Reactive oxygen species stimulate central and peripheral sympathetic nervous system activity. Am J Physiol Heart Circ Physiol 287: H695-H703, 2004.
11. Cavanal Mde F, Gomes GN, Forti AL, Rocha SO, Franco Mdo C, Fortes ZB, Gil FZ. The influence of L-arginine on blood pressure, vascular nitric oxide and renal morphometry in the offspring from diabetic mothers. Pediatr Res 62: 145-150, 2007.
12. Chen YW, Chenier I, Tran S, Scotcher M, Chang SY, Zhang SL. Maternal diabetes programs hypertension and kidney injury in offspring. Pediatr Nephrol 25: 1319-1329, 2010.
13. Dabelea D. The predisposition to obesity and diabetes in offspring of diabetic mothers. Diabetes Care 30: S169-S174, 2007.
14. Dagan A, Kwon HM, Dwarakanath V, Baum M. Effect of renal denervation on prenatal programming of hypertension and renal tubular transporter abundance. Am J Physiol Renal Physiol 295: F29-F34, 2008.
15. Dampney RAL, Coleman MJ, Fontes MAP, Hirooka Y, Horiuchi J, Li YW, Polson JW, Potts PD, Tagawa T. Central mechanisms underlying short- and long-term regulation of the cardiovascular system. Clin Exp Pharmacol Physiol 29: 261-268, 2002.
16. DiBona GF. Nervous kidney: interaction between renal sympathetic nerves and the renin-angiotensin system in the control of renal function. Hypertension 36: 1083-1088, 2000.
17. DiBona GF. Neural control of the kidney: functionally specific renal sympathetic nerve fibers. Am J Physiol Regul Integr Comp Physiol 279: R1517-R1524, 2000.
18. DiBona GF, Kopp UC. Neural control of renal function. Physiol Rev 77: 75-197, 1997.
19. Draper ML, Wang J, Valego N, Block WA, Rose JC. Effect of renal denervation on renin gene expression, concentration, and secretion in mature ovine fetus. Am J Physiol Regul Integr Comp Physiol 279: R263-R270, 2000.
20. Esler M, Jennings G, Lambert G. Noradrenaline release and the pathophysiology of primary human hypertension. Am J Hypertens 2: 140S-146S, 1989.
21. Esler MD, Krum H, Sobotka PA, Schlaich MP, Schmieder RE, Bohm M. Renal sympathetic denervation in patients with treatment-resistant hypertension (The Symplicity HTN-2 Trial): a randomised controlled trial. Lancet 376: 1903-1909, 2010.
22. Farah VM, Moreira ED, Pires MD, Irigoyen MC, Krieger EM. Comparison of three methods for the determination of baroreflex sensitivity in conscious rats. Braz J Med Biol Res 32: 361-369, 1999.
23. Flores Mendoza I, Mello Aires M, Malnic G. Effect of furosemide on urinary acidification during alterations of acid-base equilibrium in the rat. J Bras Nephrol 1: 51-58, 1979.
24. Gattone VH II, Shattuck M, Luft FC, Overhage JM, Willis LR, Evan AP. Effect of denervation on the afferent arteriole in the SHR. Jpn Heart J 25: 745-753, 1984.
25. Golin R, Pieruzzi F, Munforti C, Busca G, Di Blasio A, Zanchetti A. Role of the renal nerves in the control of renin synthesis during different sodium intakes in the rat. J Hypertens 19: 1271-1277, 2001.
26. Greenberg SG, Tershner S, Osborn JL. Neurogenic regulation of rate of achieving sodium balance after increasing sodium intake. Am J Physiol Renal Fluid Electrolyte Physiol 261: F300-F307, 1991.
27. Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci 7: 335-346, 2006.
28. Hiraoka T, Kudo T, Kishimoto Y. Catecholamines in experimentally growth-retarded rat fetus. Asia Oceania J Obstet Gynaecol 17: 341-348, 1991.
29. Hopf HB, Schlaghecke R, Peters J. Sympathetic neural blockade by thoracic epidural anesthesia suppresses renin release in response to arterial hypotension. Anesthesiology 80: 992-999, 1994.
30. Jacob F, Ariza P, Osborn JW. Renal denervation chronically lowers arterial pressure independent of dietary sodium intake in normal rats. Am J Physiol Heart Circ Physiol 284: H2302-H2310, 2003.
31. Jaramillo-Juarez F, Aires MM, Malnic G. Urinary and proximal tubule acidification during reduction of renal blood flow in the rat. J Physiol 421: 475-483, 1990.
32. Johns EJ, Kopp UC, DiBona GF. Neural control of renal function. In: Comprehensive Physiology. New York: Wiley, 2011.
33. Langley-Evans SC, Phillips GJ, Benediktsson R, Gardner DS, Edwards CRW, Jackson AA, Seckl JR. Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta 17: 169-172.
34. Law C, Egger P, Dada O, Delgado H, Kylberg E, Lavin P, Tang GH, von Hertzen H, Shiell A, Barker D. Body size at birth and blood pressure among children in developing countries. Int J Epidemiol 30: 52-57, 2001.
35. Lemos VS, Silva DM, Walther T, Alenina N, Bader M, Santos RA. The endothelium-dependent vasodilator effect of the nonpeptide Ang(1-7) mimic AVE 0991 is abolished in the aorta of mas-knockout mice. J Cardiovasc Pharmacol 46: 274-279, 2005.
36. Levy RL, White PD, Stroud WD, Hillman CC. Sustained hypertension. JAMA 135: 77-80, 1947.
37. Lohmeier TE, Iliescu R, Liu B, Henegar JR, Maric-Bilkan C, Irwin ED. Systemic and renal-specific sympathoinhibition in obesity hypertension. Hypertension 58: 331-338, 2012, 2011.
38. Luippold G, Beilharz M, Muhlbauer B. Chronic renal denervation prevents glomerular hyperfiltration in diabetic rats. Nephrol Dial Transplant 19: 342-347, 2004.
39. Lynch SA, Wright C. Sirenomelia, limb reduction defects, cardiovascular malformation, renal agenesis in an infant born to a diabetic mother. Clin Dysmorphol 6: 75-80, 1997.
40. Magaton A, Gil F, Casarini D, Cavanal MDF, Gomes G. Maternal diabetes mellitus-early consequences for the offspring. Pediatr Nephrol 22: 37-43, 2007.
41. Malpas SC. Sympathetic nervous system overactivity and its role in the development of cardiovascular disease. Physiol Rev 90: 513-557, 2010.
42. Manderson JG, Mullan B, Patterson CC, Hadden DR, Traub AI, McCance DR. Cardiovascular and metabolic abnormalities in the offspring of diabetic pregnancy. Diabetologia 45: 991-996, 2002.
43. Mills JL. Malformations in infants of diabetic mothers. Teratology 25: 385-394, 1982.
44. Mizelle HL, Hall JE, Woods LL, Montani JP, Dzielak DJ, Pan YJ. Role of renal nerves in compensatory adaptation to chronic reductions in sodium intake. Am J Physiol Renal Fluid Electrolyte Physiol 252: F291-F298, 1987.
45. Ojeda NB, Johnson WR, Dwyer TM, Alexander BT. Early renal denervation prevents development of hypertension in growth-restricted offspring. Clin Exp Pharmacol Physiol 34: 1212-1216, 2007.
46. Pedregosa JF, Haidar AA, Hirata AE, Franco M, Gomes GN, Bueno V. TLR2 and TLR4 expression after kidney ischemia and reperfusion injury in mice treated with FTY720. Int Immunopharmacol 11: 1311-1318, 2011.
47. Persson B, Westgren M, Celsi G, Nord E, Ortqvist E. Leptin concentrations in cord blood in normal newborn infants and offspring of diabetic mothers. Horm Metab Res 31: 467-471, 1999.
48. Petry CJ, Dorling MW, Wang CL, Pawlak DB, Ozanne SE. Catecholamine levels and receptor expression in low protein rat offspring. Diabet Med 17: 848-853, 2000.
49. Plagemann A, Harder T, Janert U, Rake A, Rittel F, Rohde W, Dorner G. Malformations of hypothalamic nuclei in hyperinsulinemic offspring of rats with gestational diabetes. Dev Neurosci 21: 58-67, 1999.
50. Rajdl D, Racek J, Steinerová A, Novotný Z, Stožický F, Trefil L, Siala K. Markers of oxidative stress in diabetic mothers and their infants during delivery. Physiol Res 54: 429-436, 2005.
51. Rocco L, Gil F, da Fonseca Pletiskaitz T, de Fátima Cavanal M, Gomes G. Effect of sodium overload on renal function of offspring from diabetic mothers. Pediatr Nephrol 23: 2053-2060, 2008.
52. Rocha SO, Gomes GN, Forti AL, do Carmo Pinho Franco M., Fortes ZB, de Fatima Cavanal M, Gil FZ. Long-term effects of maternal diabetes on vascular reactivity and renal function in rat male offspring. Pediatr Res 58: 1274-1279, 2005.
53. Roks AJ, van Geel PP, Pinto YM, Buikema H, Henning RH, de Zeeuw D, van Gilst WH. Angiotensin-(1-7) is a modulator of the human renin-angiotensin system. Hypertension 34: 296-301, 1999.
54. Säynävälammi P, Vaalasti A, Pyykönen ML, Ylitalo P, Vapaatalo H. The effect of renal sympathectomy on blood pressure and plasma renin activity in spontaneously hypertensive and normotensive rats. Acta Physiol Scand 115: 289-293, 1982.
55. Scherrer U, Sartori C. Insulin as a vascular and sympathoexcitatory hormone: implications for blood pressure regulation, insulin sensitivity, and cardiovascular morbidity. Circulation 96: 4104-4113, 1997.
56. Schlaich MP, Lambert E, Kaye DM, Krozowski Z, Campbell DJ, Lambert G, Hastings J, Aggarwal A, Esler MD. Sympathetic augmentation in hypertension: role of nerve firing, norepinephrine reuptake, and angiotensin neuromodulation. Hypertension 43: 169-175, 2004.
57. Shaltout HA, Rose JC, Chappell MC, Diz DI. Angiotensin-(1-7) deficiency and baroreflex impairment precede the antenatal betamethasone exposure-induced elevation in blood pressure. Hypertension 59: 453-458, 2012.
58. Shimokawa A, Kunitake T, Takasaki M, Kannan H. Differential effects of anesthetics on sympathetic nerve activity and arterial baroreceptor reflex in chronically instrumented rats. J Auton Nerv Syst 72: 46-54, 1998.
59. Smith H, Finkelstein N, Aliminosa L, Crawford B, Graber M. The renal clearances of substituted hippuric acid derivates and other aromatic acids in dog and man. J Clin Invest 24: 388-404, 1945.
60. Steculorum SM, Bouret SG. Maternal diabetes compromises the organization of hypothalamic feeding circuits and impairs leptin sensitivity in offspring. Endocrinology 152: 4171-4179, 2011.
61. Symplicity HTN-1 Investigators. Catheter-based renal sympathetic denervation for resistant hypertension: durability of blood pressure reduction out to 24 months. Hypertension 57: 911-917, 2011.
62. Terui N, Saeki Y, Kumada M. Barosensory neurons in the rostral ventrolateral medulla mediate the renal-sympathetic reflex in rabbits. Clin Exp Hypertens A 10, Suppl 1: 269-274, 1988.
63. Tran S, Chen YW, Chenier I, Chan JSD, Quaggin S, Hébert MJ, Ingelfinger JR, Zhang SL. Maternal diabetes modulates renal morphogenesis in offspring. J Am Soc Nephrol 19: 943-952, 2008.
64. Wagner C, Hinder M, Krämer BK, Kurtz A. Role of renal nerves in the stimulation of the renin system by reduced renal arterial pressure. Hypertension 34: 1101-1105, 1999.
65. Wang HJ, Pan YX, Wang WZ, Gao L, Zimmerman MC, Zucker IH, Wang W. Exercise training prevents the exaggerated exercise pressor reflex in rats with chronic heart failure. J Appl Physiol 108: 1365-1375, 2010.
66. Weinstock M, Gorodetsky E, Kalman R. Renal denervation prevents sodium retention and hypertension in salt-sensitive rabbits with genetic baroreflex impairment. Clin Sci (Lond) 90: 287-293, 1996.
67. Wichi RB, Souza SB, Casarini DE, Morris M, Barreto-Chaves ML, Irigoyen MC. Increased blood pressure in the offspring of diabetic mothers. Am J Physiol Regul Integr Comp Physiol 288: R1129-R1133, 2005.
68. Winternitz SR, Katholi RE, Oparil S. Role of the renal sympathetic nerves in the development and maintenance of hypertension in the spontaneously hypertensive rat. J Clin Invest 66: 971-978, 1980.