Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-20T08:31:27.208Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal copper deficiency perpetuates altered vascular function in Sprague-Dawley rat offspring

Published online by Cambridge University Press:  22 February 2010

C. M. Anderson  and
W. T. Johnson
C. M. Anderson*
Affiliation:
College of Nursing, University of North Dakota, Grand Forks, North Dakota, USA
W. T. Johnson*
Affiliation:
USDA ARS Grand Forks Human Nutrition Research Center1,2, Grand Forks, North Dakota, USA
*
*Address for correspondence: Dr C. M. Anderson, College of Nursing, University of North Dakota, 400 Oxford Street, Room 340D, Grand Forks, North Dakota 58202-9025, USA. (E-mails [email protected], [email protected])
*Address for correspondence: Dr C. M. Anderson, College of Nursing, University of North Dakota, 400 Oxford Street, Room 340D, Grand Forks, North Dakota 58202-9025, USA. (E-mails [email protected], [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Little is known about the consequences of maternal copper (Cu) deficiency on the vascular function of offspring or on perpetuation of vascular effects to a second generation. We examined vascular functional responses in mesenteric arteries from Cu-deficient Sprague-Dawley rat dams and from offspring directly exposed to maternal Cu deficiency during development and lactation and perpetuation of the effects in a second generation of offspring. Dams were fed a diet with marginal (1 mg Cu/kg) or adequate (6 mg Cu/kg) Cu for 3 weeks before conception and throughout pregnancy and lactation periods. Half of the first generation (F1) litters were cross-fostered. At reproductive maturity, F1 pairs were bred within groups resulting in second generation (F2) offspring. At 9 weeks of age, mesenteric artery (200 μm) isometric tension was determined in response to vasoconstrictors and vasorelaxants using a small artery wire myograph. Cu deficiency did not alter the vascular function in dams. In F1 offspring, increased responsiveness to potassium chloride in male offspring was due to direct exposure to maternal Cu deficiency in the birth mother, while enhanced endothelium-dependent relaxation responses in female offspring resulted from postnatal exposure to maternal Cu deficiency. Increased endothelium independent and decreased endothelium-dependent relaxation responses were identified in F2 Cu-deficient male offspring. These data indicate that exposure to maternal Cu deficiency during critical windows of development alter the vascular function across two generations of offspring.

Keywords

copper deficiencyfetal programmingnutritionpregnancyvascular function
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 1 , Issue 2 , April 2010 , pp. 131 - 140
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

1

The US Department of Agriculture, Agricultural Research Service, Northern Plains Area, is an equal opportunity/affirmative action employer and all agency services are available without discrimination.

2

Mention of trade names or commercial products in this article is solely to provide specific information and does not imply recommendation or endorsement by the US Department of Agriculture.

References

1.Carlson, S, Aupperle, P. Nutrient requirements and fetal development: recommendations for best outcomes. J Fam Pract. 2007; 56(Suppl 11 Womens), S1–S6.Google ScholarPubMed
2.Uusitalo, L, Kenward, MG, Virtanen, SM, et al. Intake of antioxidant vitamins and trace elements during pregnancy and risk of advanced beta cell autoimmunity in the child. Am J Clin Nutr. 2008; 88, 458–464.CrossRefGoogle ScholarPubMed
3.Yajnik, CS, Deshmukh, US. Maternal nutrition, intrauterine programming and consequential risks in the offspring. Rev Endocr Metab Disord. 2008; 9, 203–211.CrossRefGoogle ScholarPubMed
4.Symonds, ME, Budge, H, Stephenson, T, Gardner, DS. Experimental evidence for long-term programming effects of early diet. Adv Exp Med Biol. 2005; 569, 24–32.CrossRefGoogle ScholarPubMed
5.Yates, Z, Tarling, EJ, Langley-Evans, SC, Salter, AM. Maternal undernutrition programmes atherosclerosis in the ApoE*3-Leiden mouse. Br J Nutr. 2008, 1–10.Google ScholarPubMed
6.Milne, DB. Copper intake and assessment of copper status. Am J Clin Nutr. 1998; 67(Suppl 5), 1041S–1045S.CrossRefGoogle ScholarPubMed
7.Alebic-Juretic, A, Frkovic, A. Plasma copper concentrations in pathological pregnancies. J Trace Elem Med Biol. 2005; 19, 191–194.CrossRefGoogle ScholarPubMed
8.Saari, JT, Schuschke, DA. Cardiovascular effects of dietary copper deficiency. Biofactors. 1999; 10, 359–375.CrossRefGoogle ScholarPubMed
9.Schuschke, DA. Dietary copper in the physiology of the microcirculation. J Nutr. 1997; 127, 2274–2281.CrossRefGoogle ScholarPubMed
10.Saari, JT. Copper deficiency and cardiovascular disease: role of peroxidation, glycation, and nitration. Can J Physiol Pharmacol. 2000; 78, 848–855.CrossRefGoogle ScholarPubMed
11.Li, Y, Wang, L, Schuschke, DA, et al. Marginal dietary copper restriction induces cardiomyopathy in rats. J Nutr. 2005; 135, 2130–2136.CrossRefGoogle ScholarPubMed
12.Uriu-Adams, JY, Keen, CL. Copper, oxidative stress, and human health. Mol Aspects Med. 2005; 26, 268–298.CrossRefGoogle ScholarPubMed
13.Klevay, L. Hypertension in rats due to copper deficiency. Nutr Rep Int. 1987; 35, 999–1005.Google Scholar
14.Mederios, D. Hypertension in the Wistar-Kyoto rat as a result of post-weaning copper restriction. Nutr Res. 1987; 7, 231–235.CrossRefGoogle Scholar
15.Wu, B, Mederios, DM, Lin, KN, Thorn, BM. Long term effects of dietary copper and sodium upon blood pressure in the Long-Evans rat. Nutr Res. 1984; 4, 305–314.CrossRefGoogle Scholar
16.Didion, SP, Ryan, MJ, Didion, LA, et al. Increased superoxide and vascular dysfunction in CuZnSOD-deficient mice. Circ Res. 2002; 91, 938–944.CrossRefGoogle ScholarPubMed
17.Schuschke, DA, Falcone, JC, Saari, JT, et al. Endothelial cell calcium mobilization to acetylcholine is attenuated in copper-deficient rats. Endothelium. 2000; 7, 83–92.CrossRefGoogle ScholarPubMed
18.Lynch, SM, Frei, B, Morrow, JD, et al. Vascular superoxide dismutase deficiency impairs endothelial vasodilator function through direct inactivation of nitric oxide and increased lipid peroxidation. Arterioscler Thromb Vasc Biol. 1997; 17, 2975–2981.CrossRefGoogle ScholarPubMed
19.Saari, JT. Dietary copper deficiency and endothelium-dependent relaxation of rat aorta. Proc Soc Exp Biol Med. 1992; 200, 19–24.CrossRefGoogle ScholarPubMed
20.Schuschke, DA, Reed, MW, Saari, JT, Miller, FN. Copper deficiency alters vasodilation in the rat cremaster muscle microcirculation. J Nutr. 1992; 122, 1547–1552.CrossRefGoogle ScholarPubMed
21.Schuschke, DA, Saari, JT, Miller, FN. A role for dietary copper in nitric oxide-mediated vasodilation. Microcirculation. 1995; 2, 371–376.CrossRefGoogle ScholarPubMed
22.Reeves, PG, Nielsen, FH, Fahey, GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123, 1939–1951.CrossRefGoogle Scholar
23.Johnson, WT, Kramer, TR. Effect of copper deficiency on erythrocyte membrane proteins of rats. J Nutr. 1987; 117, 1085–1090.CrossRefGoogle ScholarPubMed
24.Johnson, WT, Anderson, CM. Cardiac cytochrome C oxidase activity and contents of subunits 1 and 4 are altered in offspring by low prenatal copper intake by rat dams. J Nutr. 2008; 138, 1269–1273.CrossRefGoogle ScholarPubMed
25.Mulvany, MJ, Halpern, W. Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ Res. 1977; 41, 19–26.CrossRefGoogle ScholarPubMed
26.Anderson, CM, Lopez, F, Zhang, HY, Pavlish, K, Benoit, JN. Reduced uteroplacental perfusion alters uterine arcuate artery function in the pregnant Sprague-Dawley rat. Biol Reprod. 2005; 72, 762–766.CrossRefGoogle ScholarPubMed
27.Klevay, LM. Cardiovascular disease from copper deficiency--a history. J Nutr. 2000; 130(Suppl 2S), 489S–492S.CrossRefGoogle ScholarPubMed
28.Schuschke, DA, Percival, SS, Saari, JT, et al. Relationship between dietary copper concentration and acetylcholine-induced vasodilation in the microcirculation of rats. Biofactors. 1999; 10, 321–332.CrossRefGoogle ScholarPubMed
29.Gambling, L, Dunford, S, Wallace, DI, et al. Iron deficiency during pregnancy affects postnatal blood pressure in the rat. J Physiol. 2003; 552, 603–610.CrossRefGoogle ScholarPubMed
30.Hemmings, DG, Williams, SJ, Davidge, ST. Increased myogenic tone in 7-month-old adult male but not female offspring from rat dams exposed to hypoxia during pregnancy. Am J Physiol Heart Circ Physiol. 2005; 289, H674–H682.CrossRefGoogle Scholar
31.Waterland, RA, Michels, KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007; 27, 363–388.CrossRefGoogle ScholarPubMed
32.Gicquel, C, El-Osta, A, Le Bouc, Y. Epigenetic regulation and fetal programming. Best Pract Res Clin Endocrinol Metab. 2008; 22, 1–16.CrossRefGoogle ScholarPubMed
33.Gluckman, PD, Hanson, MA, Cooper, C, Thornburg, KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008; 359, 61–73.CrossRefGoogle ScholarPubMed
34.Gartner, EM, Griffith, KA, Pan, Q, et al. A pilot trial of the anti-angiogenic copper lowering agent tetrathiomolybdate in combination with irinotecan, 5-flurouracil, and leucovorin for metastatic colorectal cancer. Invest New Drugs. 2009; 27, 159–165.CrossRefGoogle ScholarPubMed
35.Zhou, Y, Jiang, Y, Kang, YJ. Copper reverses cardiomyocyte hypertrophy through vascular endothelial growth factor-mediated reduction in the cell size. J Mol Cell Cardiol. 2008; 45, 106–117.CrossRefGoogle ScholarPubMed
36.Smith-Mungo, LI, Kagan, HM. Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol. 1998; 16, 387–398.CrossRefGoogle ScholarPubMed
37.Hawk, SN, Lanoue, L, Keen, CL, et al. Copper-deficient rat embryos are characterized by low superoxide dismutase activity and elevated superoxide anions. Biol Reprod. 2003; 68, 896–903.CrossRefGoogle ScholarPubMed
38.Beckers-Trapp, ME, Lanoue, L, Keen, CL, et al. Abnormal development and increased 3-nitrotyrosine in copper-deficient mouse embryos. Free Radic Biol Med. 2006; 40, 35–44.CrossRefGoogle ScholarPubMed