Pre-Weaning Growth Hormone Treatment Reverses Hypertension and Endothelial Dysfunction in Adult Male Offspring of Mothers Undernourished during Pregnancy

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Gray, Clint ^a   Li, Minglan ^a   Reynolds, Clare M ^a   Vickers, Mark H ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIRTH WEIGHT; BLOOD PRESSURE MEASUREMENT; BLOOD VESSEL DIAMETER; BODY GROWTH; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; FEMALE; HORMONAL THERAPY; HYPERTENSION; MALE; MALNUTRITION; NONHUMAN; PREGNANCY; RAT; SYSTOLIC BLOOD PRESSURE; VASODILATATION; VASOMOTOR REFLEX; WEANING;

ACETYLCHOLINE; ADULT; ANIMALS; APAMIN; BLOOD PRESSURE; CARBENOXOLONE; FEMALE; GROWTH HORMONE; HUMANS; HYPERTENSION; MALE; MALNUTRITION; MESENTERIC ARTERIES; NG-NITROARGININE METHYL ESTER; PHENYLEPHRINE; PREGNANCY; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; VASOCONSTRICTION; VASODILATION; WEANING;

RATTUS;

EID: 84872160315     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053505     Document Type: Article

References (64)

1. Barker DJP, Osmond C Golding J, Kuh D, Wadsworth MEJ (1989) Growth inutero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. British Medical Journal 298, 564-567.
2. Woodall SM, Johnston BNM, Breier BH, Gluckman PD, (1996) Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of the offspring. Pediatr Res 40: 438-443.
3. Brawley L, Poston L Hanson MA (2003) Mechanisms underlying the programming of small artery dysfunction: Review of the model using low protein diet in pregnancy in the rat. Arch Physiol Biochem 111, 23-35.
4. Lucas A (1991) Programming by early nutrition in man. In Childhood Environment and Adult Disease, 38-55 [GR Bock and J Whelan, editors].
5. Gluckman PD, Hanson MA (2004) Living with the past: Evolution, development, and patterns of disease. Science 305, 1733-1736.
6. Ozaki T, Nishina H, Hanson MA, Poston L (2001) Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. Journal of Physiology-London 530, 141-152.
7. Pladys P, Lahaie I, Cambonie G, Thibault G, Le NLO, et al. (2004) Role of brain and peripheral angiotensin II in hypertension and altered arterial baroreflex programmed during fetal life in rat. Pediatric Research 55 1042-1049.
8. Alves JG, Vilarim JN, Figueiroa JN (1999) Fetal influences on neonatal blood pressure. J Perinatol 19, 593-595.
9. Li JM, Shah AM (2004) Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 287, R1014-R1030.
10. Hadoke PW, Lindsay RS, Seckl JR, Walker BR, Kenyon CJ, (2006) Altered vascular contractility in adult female rats with hypertension programmed by prenatal glucocorticoid exposure. J Endocrinol. 188(3): 435-42.
11. Franco MC, Arruda RM, Dantas AP, Kawamoto EM, Fortes ZB, et al. (2002) Intrauterine undernutrition: expression and activity of the endothelial nitric oxide synthase in male and female adult offspring. Cardiovasc Res 56, 145-153.
12. Torrens C, Hanson MA, Gluckman PD, Vickers MH (2008) Maternal undernutrition leads to endothelial dysfunction in adult male rat offspring independent of postnatal diet. British Journal of Nutrition, 101, (1), 27-33.
13. Li J, White J, Guo L, Zhao XM, Wang JF et al. (2009) Salt Inactivates Endothelial Nitric Oxide Synthase in Endothelial Cells. Journal of Nutrition 139, 447-451.
14. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP, (2000) Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 127(19): 4195-202.
15. Schreuder MF, van Wijk JA, Delemarre-van de Waal HA, (2006) Intrauterine growth restriction increases blood pressure and central pulse pressure measured with telemetry in aging rats. J Hypertens. (7): 1337-43.
16. Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, et al. (2005) Neonatal leptin treatment reverses developmental programming. Endocrinology. (10): 4211-6.
17. Jackson AA, Dunn RL, Marchand MC, Langley-Evans SC (2002). Increased systolic blood pressure in 380 rats induced by a maternal low- protein diet is reversed by dietary supplementation with lycine. Clin Sci 103(6), 633-639.
18. Torrens C, Brawley L, Anthony FW, (2006) Folate supplementation during pregnancy improves offspring cardiovascular dysfunction induced by protein restriction. Hypertension 47: 982-7.
19. Sherman RC, Langley-Evans SC (1998) Early administration of angiotensin-converting enzyme inhibitor captopril, prevents the development of hypertension programmed by intrauterine exposure to a maternal low-protein diet in the rat. Clinical Science. 94(4), 373-81.
20. Torrens C, Kelsall CJ, Hopkins LA, Anthony FW, Curzen NP et al. (2009) Atorvastatin restores endothelial function of protein restricted rats in a cholesterol-independent manner. Hypertension 53, 661-667.
21. Isgaard J, Bergh CH, Caidahl K, Lomsky M, Hjalmarson A et al. (1998) A placebo-controlled study of growth hormone in patients with congestive heart failure. European Heart Journal 19 1704-1711.
22. Longobardi S, Cittadini A, Stromer H, Katz SE, Grossman JD et al. (2000) Assessment of cardiac morphology and function in mutant dwarf rats. Growth Hormone and IGF Research 10 242-247.
23. Fazio S, Cittadini A, Sabatini D, Merola B, Colao A et al. (1997) Growth hormone and heart performance. A novel mechanism of cardiac wall stress regulation in humans. European Heart Journal 18 340-347.
24. Khana AS, Saneb DC, Wannenburgb T, Sonntaga WE (2002) Growth hormone, insulin-like growth factor-1 and the aging cardiovascular system. Cardiovascular Research 54 25-35.
25. Boger RH, Skamira C, Bode-Boger SM, Brabant G, von zur Muhlen A et al. (1996) Nitric oxide may mediate the hemodynamic effects of recombinant growth hormone in patients with acquired growth hormone deficiency. A double-blind, placebo-controlled study. Journal of Clinical Investigation 98 2706-2713.
26. Tivesten A, Caidahl K, Kujacic V, Sun XY, Hedner T et al. (2001) Similar cardiovascular effects of growth hormone and insulin-like growth factor-I in rats after experimental myocardial infarction. Growth Hormone and IGF Research 11 187-195.
27. Sas T, de Waal W, Mulder P, Houdijk M, Jansen M, et al. (1999) Growth hormone treatment in children with short stature born small for gestational age: 5-year results of a randomized, double-blind, dose-response trial. J Clin Endocrinol Metab 84: 3064-3070.
28. Verhelst J, (2009) Abs R. Cardiovascular risk factors in hypopituitary GH-deficient adults. Eur J Endocrinol. 161Suppl 1: S41-9.
29. McCallum RW, Petrie JR, Dominiczak AF, Connell JM, (2002) Growth hormone deficiency and vascular risk. Clin Endocrinol (Oxf). 57(1): 11-24.
30. Rossoni G, Locatelli V, De Gennaro Colonna V, Torsello A, Schweiger F, et al. (1999) Growth hormone and hexarelin prevent endothelial vasodilator dysfunction in aortic rings of the hypophysectomized rat. J Cardiovasc Pharmacol. 34(3): 454-60.
31. Nyström HC, Klintland N, Caidah K, Bergström G, Wickman A, (2005) Short-term administration of growth hormone (GH) lowers blood pressure by activating eNOS/nitric oxide (NO)-pathway in male hypophysectomized (Hx) rats. BMC Physiology 5: 17.
32. Egecioglu E, Bjursell M, Ljungberg A, Dickson SL, Kopchick JJ et al. (2005) Growth hormone receptor deficiency results in blunted ghrelin feeding response, obesity, and hypolipidemia in mice. Am J Physiol Endocrinol Metab. E317-25.
33. Vickers MH, Ikenasio BA, Breier BH (2002) Adult growth hormone treatment reduces hypertension and obesity induced by an adverse prenatal environment. J Endocrinol December 1, 175 615-623.
34. Rosen T, Bengtsson BA (1990) Premature mortality due to cardiovascular disease in hypopituitarism. Lancet 336 285-288.
35. Howie GJ, Sloboda DM, Vickers MH, (2012) Maternal undernutrition during critical windows of development results in differential and sex-specific effects on postnatal adiposity and related metabolic profiles in adult rat offspring. Br J Nutr. 108: 298-307.
36. Wolfe D, Gong M, Han G, Magee TR, Ross MG, et al. (2012) Nutrient sensor-mediated programmed nonalcoholic fatty liver disease in low birthweight offspring. Am J Obstet Gynecol. 207(4): 308.e1-6.
37. Laborie C, Molendi-Coste O, Breton C, Montel V, Vandenbulcke F et al. (2011) Maternal perinatal undernutrition has long-term consequences on morphology, function and gene expression of the adrenal medulla in the adult male rat. J Neuroendocrinol. 711-24.
38. Vickers MH, Ikenasio BA, Breier BH, (2002) Adult growth hormone treatment reduces hypertension and obesity induced by an adverse prenatal environment. J Endocrinol. 175(3): 615-23.
39. Vickers MH, Ikenasio BA, Breier BH, (2001) IGF-I treatment reduces hyperphagia, obesity, and hypertension in metabolic disorders induced by fetal programming. Endocrinology. 142(9): 3964-73.
40. Whitesall SE, Hoff JB, Vollmer AP, D'Alecy LG, (2004) Comparison of simultaneous measurement of mouse systolic arterial blood pressure by radiotelemetry and tail-cuff methods. Am J Physiol Heart Circ Physiol. 286(6): H2408-15.
41. S Moncada, DD Rees, R Schulz, RMJ Palmer (1991) Development and mechanism of a specific supersensitivity to nitrovasodilators after inhibition of vascular nitric oxide synthesis in vivo Proc. Nati. Acad. Sci. USA Vol. 88, 2166-2170, Physiology/Pharmacology.
42. PRR Gangula, P Lanlua, RD Bukoski, SJ Wimalawansa, C Yallampalli (2004) Mesenteric Arterial Relaxation to Calcitonin Gene-Related Peptide Is Increased During Pregnancy and by Sex Steroid Hormones. Biology of Reproduction, vol. 71 no. 5 1739-1745.
43. GF Chen, DW Cheung, (1992) Characterization of acetylcholine-induced membrane hyperpolarization in endothelial cells. Circ Res. 70: 257-263.
44. Chadha PS, Liu L, Rikard-Bell M, Senadheera S, Howitt L, et al. (2010) Endothelium-dependent vasodilation in human mesenteric artery is primarily mediated by myoendothelial gap junctions intermediate conductance calcium-activated K+ channel and nitric oxide. J Pharmacol Exp Ther. 336(3): 701-8.
45. Yasuo Kansui Y, Garland CJ, Dora KA, (2008) Enhanced spontaneous Ca2+ events in endothelial cells reflect signalling through myoendothelial gap junctions in pressurized mesenteric arteriesCell Calcium. 44(2): 135-146.
46. Murphy ME, Brayden JE (1995) Apamin-sensitive K+ channels mediate an endothelium-dependent hyperpolarization in rabbit mesenteric arteries. Journal of Physiology, 489.3, 723-734.
47. Stankevicius E, Dalsgaard T, Kroigaard C, Beck L, Boedtkjer E et al. (2011) Opening of small and intermediate calcium-activated potassium channels induce relaxation mainly mediated by NO release in large arteries and EDHF in small arteries from rat. JPET, jpet.111.179242.
48. Yang R, Bunting S, Gillett N, Clark R, Jin H, (1995) Growth hormone improves cardiac performance in experimental heart failure. Circulation. 92(2): 262-7.
49. Goto K, Fujii K, Kansui Y, Abe I, Iida M, (2002) Critical role of gap junctions in endothelium-dependent hyperpolarization in rat mesenteric arteries. Clin. Exp. Pharmacol. Physiol. 29: 595-602.
50. Schilling T, Eder C, (2007) TRAM-34 inhibits nonselective cation channels. Pflugers Arch. 454(4): 559-63.
51. Wulff H, Gutman GA, Cahalan MD, Chandy KG, (2001) Delineation of the clotrimazole/TRAM-34 binding site on the intermediate-conductance calcium-activated potassium channel, IKCa1. Journal of Biological Chemistry 276: 32040-32045.
52. Woodall SM, Breier BH, Johnston BM, Gluckman PD (1996) A model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: effects on the somatotrophic axis and postnatal growth. J Endocrinol. 150 231-242.
53. Takezawa H, Hayashi H, Sano H, Saito H, Ebihara S, (1994) Circadian and estrous cycle-dependent variations in blood pressure and heart rate in female rats. Am J Physiol. 267(5 Pt 2): R1250-6.
54. Juszczak GR, Swiergiel AH, (2009) Properties of gap junction blockers and their behavioural, cognitive and electrophysiological effects: Animal and human studies. Prog Neuropsychopharmacol Biol Psychiatry. 33: 181-198.
55. Rozental R, Srinivas M, Spray DC, (2001) How to close a gap junction channel: Efficacies and potencies of uncoupling agents. Methods Mol Biol. 154: 447-476.
56. Connors BW, (2012) Tales of a Dirty Drug: Carbenoxolone, Gap Junctions, and Seizures. Epilepsy Curr. 12(2): 66-68.
57. Chaytor AT, Martin PE, Evans WH, Randall MD, Griffith TM, (1999) The endothelial component of cannabinoid-induced relaxation in rabbit mesenteric artery depends on gap junctional communication. J. Physiol. (Lond.) 520: 539-550.
58. Kenny LC, Baker PN, Kendall DA, Randall MD, Dunn WR, (2002) The role of gap junctions in mediating endothelium-dependent responses to bradykinin in myometrial small arteries isolated from pregnant women. Br J Pharmacol. 136(8): 1085-1088.
59. Coleman HA, Tare M, Parkington HC (2001) K+ currents underlying the action of endothelium-derived hyperpolarizing factor in guinea-pig, rat and human blood vessels. The Journal of Physiology, 531, 359-373.
60. Chaytor AT, Evans WH, Griffith TM, (1998) Central role of heterocellular gap junctional communication in endothelium-dependent relaxations of rabbit arteries. J Physiol 508(2): 561-73.
61. Edwards G, Félétou M, Gardener MJ, Thollon C, Vanhoutte PM, et al. (1999) Role of gap junctions in the responses to EDHF in rat and guinea-pig small arteries. Br J Pharmacol. 128(8): 1788-1794.
62. Gibbons GH, Dzau VJ, (1994) The emerging concept of vascular remodeling. N Engl J Med. 330(20): 1431-8.
63. Mulvany MJ, Halpern W, (1977) Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ Res 41: 19-26.
64. Mulvany MJ, (1984) Determinants of vascular hemodynamic characteristics Hypertension. 6(S3): III-13-III-18.