Experimental hyperleptinemia in neonatal rats leads to selective leptin responsiveness, hypertension, and altered myocardial function

Hypertension

Volumn 62, Issue 3, 2013, Pages 627-633

  Samuelsson, Anne Maj ^a   Clark, James ^b   Rudyk, Olena ^b   Shattock, Michael J ^b   Bae, Sung Eun ^a   South, Timothy ^a   Pombo, Joaquim ^a   Redington, Kathrine ^a   Uppal, Esna ^a   Coen, Clive W ^a   Poston, Lucilla ^a   Taylor, Paul D ^a  

^a ST THOMAS HOSPITAL   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

developmental programming; hypertension; leptin; obesity; rats; sympathetic nervous system; ventricular dysfunction

Indexed keywords

INSULIN; LEPTIN; PROPRANOLOL; TERAZOSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR RESPONSE; CELL STRUCTURE; CHRONOTROPISM; ECHOCARDIOGRAPHY; EXPERIMENTAL HYPERLEPTINEMIA; FAT MASS; FEMALE; FOOD INTAKE; HEART FUNCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE CELL; HEART PRELOAD; HEART RATE VARIABILITY; HEART WEIGHT; HYPERLEPTINEMIA; HYPERTENSION; INOTROPISM; INSULIN BLOOD LEVEL; LOCOMOTION; MALE; MEAN ARTERIAL PRESSURE; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; SYSTOLIC BLOOD PRESSURE;

DEVELOPMENTAL PROGRAMMING; HYPERTENSION; LEPTIN; OBESITY; RATS; SYMPATHETIC NERVOUS SYSTEM; VENTRICULAR DYSFUNCTION;

ADIPOSE TISSUE; ANIMALS; ANIMALS, NEWBORN; BLOOD PRESSURE; BODY WEIGHT; CARDIOVASCULAR SYSTEM; FEMALE; HEART; HEART RATE; HYPERTENSION; LEPTIN; MALE; MYOCARDIAL CONTRACTION; MYOCARDIUM; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84883294081     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.111.00691     Document Type: Article

References (37)

1. Oteng-Ntim E, Doyle P. Maternal outcomes in obese pregnancy. In: Gillman MW, Poston L, eds. In Maternal Obesity. Cambridge, UK: Cambridge University Press; 2012:35-44.
2. Poston L. Gestational weight gain: Influences on the long-term health of the child. Curr Opin Clin Nutr Metab Care. 2012;15:252-257.
3. Norman JE, Reynolds RM, Reynolds R. The consequences of obesity and excess weight gain in pregnancy. Proc Nutr Soc. 2011;70:450-456.
4. Hochner H, Friedlander Y, Calderon-Margalit R, Meiner V, Sagy Y, Avgil-Tsadok M, Burger A, Savitsky B, Siscovick DS, Manor O. Associations of maternal prepregnancy body mass index and gestational weight gain with adult offspring cardiometabolic risk factors: The Jerusalem Perinatal Family Follow-up Study. Circulation. 2012;125:1381-1389.
5. Lucilla P, Taylor PD, Nathanielsz P. Influences of maternal obesity on the health of the offspring: A review of animal models. In: Gillman MW, Poston L, eds. Maternal Obesity. New York, NY: Cambridge University Press; 2012:100-114.
6. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EH, Piersma AH, Ozanne SE, Twinn DF, Remacle C, Rowlerson A, Poston L, Taylor PD. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: A novel murine model of developmental programming. Hypertension. 2008;51:383-392.
7. Samuelsson AM, Morris A, Igosheva N, Kirk SL, Pombo JM, Coen CW, Poston L, Taylor PD. Evidence for sympathetic origins of hypertension in juvenile offspring of obese rats. Hypertension. 2010;55:76-82.
8. Dong M, Zheng Q, Ford SP, Nathanielsz PW, Ren J. Maternal obesity, lipotoxicity and cardiovascular diseases in offspring. J Mol Cell Cardiol. 2013;55:111-116.
9. Kirk SL, Samuelsson AM, Argenton M, Dhonye H, Kalamatianos T, Poston L, Taylor PD, Coen CW. Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLoS One. 2009;4:e5870.
10. Shek EW, Brands MW, Hall JE. Chronic leptin infusion increases arterial pressure. Hypertension. 1998;31(1 Pt 2):409-414.
11. Haynes WG, Morgan DA, Djalali A, Sivitz WI, Mark AL. Interactions between the melanocortin system and leptin in control of sympathetic nerve traffic. Hypertension. 1999;33(1 Pt 2):542-547.
12. Rahmouni K, Correia ML, Haynes WG, Mark AL. Obesity-associated hypertension: New insights into mechanisms. Hypertension. 2005;45:9-14.
13. Bouret SG. Neurodevelopmental actions of leptin. Brain Res. 2010;1350:2-9.
14. Nivoit P, Morens C, Van Assche FA, Jansen E, Poston L, Remacle C, Reusens B. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia. 2009;52:1133-1142.
15. Fernandez-Twinn DS, Blackmore HL, Siggens L, Giussani DA, Cross CM, Foo R, Ozanne SE. The programming of cardiac hypertrophy in the offspring by maternal obesity is associated with hyperinsulinemia, AKT, ERK, and mTOR activation. Endocrinology. 2012;153:5961-5971.
16. Tajmir P, Ceddia RB, Li RK, Coe IR, Sweeney G. Leptin increases cardiomyocyte hyperplasia via extracellular signal-regulated kinase- and phosphatidylinositol 3-kinase-dependent signaling pathways. Endocrinology. 2004;145:1550-1555.
17. Rajapurohitam V, Gan XT, Kirshenbaum LA, Karmazyn M. The obesityassociated peptide leptin induces hypertrophy in neonatal rat ventricular myocytes. Circ Res. 2003;93:277-279.
18. Yura S, Itoh H, Sagawa N, Yamamoto H, Masuzaki H, Nakao K, Kawamura M, Takemura M, Kakui K, Ogawa Y, Fujii S. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab. 2005;1:371-378.
19. Toste FP, de Moura EG, Lisboa PC, Fagundes AT, de Oliveira E, Passos MC. Neonatal leptin treatment programmes leptin hypothalamic resistance and intermediary metabolic parameters in adult rats. Br J Nutr. 2006;95:830-837.
20. Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, Gertler A, Breier BH, Harris M. The effect of neonatal leptin treatment on postnatal weight gain in male rats is dependent on maternal nutritional status during pregnancy. Endocrinology. 2008;149:1906-1913.
21. Mark AL, Correia M, Morgan DA, Shaffer RA, Haynes WG. State-of-theart-lecture: Obesity-induced hypertension: New concepts from the emerging biology of obesity. Hypertension. 1999;33(1 Pt 2):537-541.
22. Ozata M, Ozdemir IC, Licinio J. Human leptin deficiency caused by a missense mutation: Multiple endocrine defects, decreased sympathetic tone, and immune system dysfunction indicate new targets for leptin action, greater central than peripheral resistance to the effects of leptin, and spontaneous correction of leptin-mediated defects. J Clin Endocrinol Metab. 1999;84:3686-3695.
23. Mark AL, Agassandian K, Morgan DA, Liu X, Cassell MD, Rahmouni K. Leptin signaling in the nucleus tractus solitarii increases sympathetic nerve activity to the kidney. Hypertension. 2009;53:375-380.
24. Shankar A, Xiao J. Positive relationship between plasma leptin level and hypertension. Hypertension. 2010;56:623-628.
25. Erkonen GE, Hermann GM, Miller RL, Thedens DL, Nopoulos PC, Wemmie JA, Roghair RD. Neonatal leptin administration alters regional brain volumes and blocks neonatal growth restriction-induced behavioral and cardiovascular dysfunction in male mice. Pediatr Res. 2011;69 (5 Pt 1):406-412.
26. Trevenzoli IH, Valle MM, Machado FB, Garcia RM, Passos MC, Lisboa PC, Moura EG. Neonatal hyperleptinaemia programmes adrenal medullary function in adult rats: Effects on cardiovascular parameters. J Physiol. 2007;580(Pt 2):629-637.
27. Plagemann A. Perinatal nutrition and hormone-dependent programming of food intake. Horm Res. 2006;65(Suppl 3):83-89.
28. Rajani CK, Samuelsson AM, Clark J, Shattock M, Poston L, Taylor PD. Developmental programming of myocardial dysfunction arising from maternal obesity in a murine model. J DOHAD. 2009;1:S247.
29. Hein S, Arnon E, Kostin S, Schönburg M, Elsässer A, Polyakova V, Bauer EP, Klövekorn WP, Schaper J. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: Structural deterioration and compensatory mechanisms. Circulation. 2003;107:984-991.
30. Soonpaa MH, Kim KK, Pajak L, Franklin M, Field LJ. Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol. 1996;271(5 Pt 2):H2183-H2189.
31. Barbera A, Giraud GD, Reller MD, Maylie J, Morton MJ, Thornburg KL. Right ventricular systolic pressure load alters myocyte maturation in fetal sheep. Am J Physiol Regul Integr Comp Physiol. 2000;279:R1157-R1164.
32. Schulze PC, Kratzsch J, Linke A, Schoene N, Adams V, Gielen S, Erbs S, Moebius-Winkler S, Schuler G. Elevated serum levels of leptin and soluble leptin receptor in patients with advanced chronic heart failure. Eur J Heart Fail. 2003;5:33-40.
33. Aiken CE, Ozanne SE. Sex differences in developmental programming models. Reproduction. 2013;145:R1-13.
34. Grove KL, Grayson BE, Glavas MM, Xiao XQ, Smith MS. Development of metabolic systems. Physiol Behav. 2005;86:646-660.
35. Catalano PM, Presley L, Minium J, Hauguel-de Mouzon S. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care. 2009;32:1076-1080.
36. Lindsay RS, Nelson SM, Walker JD, Greene SA, Milne G, Sattar N, Pearson DW. Programming of adiposity in offspring of mothers with type 1 diabetes at age 7 years. Diabetes Care. 2010;33:1080-1085.
37. Ye ZY, Li DP. Activation of the melanocortin-4 receptor causes enhanced excitation in presympathetic paraventricular neurons in obese Zucker rats. Regul Pept. 2011;166:112-120.