Prenatal stress programs lipid metabolism enhancing cardiovascular risk in the female F1, F2, and F3 generation in the primate model common marmoset (Callithrix jacchus)

Journal of Medical Primatology

Volumn 41, Issue 4, 2012, Pages 231-240

  Buchwald, Ulrike ^a   Teupser, Daniel ^a,b   Kuehnel, Friederike ^a   Grohmann, Jana ^a   Schmieder, Nancy ^a   Beindorff, Nicola ^c   Schlumbohm, Christina ^c   Fuhrmann, Herbert ^a   Einspanier, Almuth ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY HOSPITAL LEIPZIG   (Germany)

^c GERMAN PRIMATE CENTER   (Germany)

Author keywords

Atherosclerosis; Cholesterol; Dexamethasone; Fatty acid; Glucocorticoid; High density lipoprotein; Imprinting; Lipoprotein; Low density lipoprotein; Triglyceride

Indexed keywords

CHOLESTEROL; DEXAMETHASONE; FATTY ACID; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CALLITHRIX; CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FATTY ACID BLOOD LEVEL; FEMALE; LIPID METABOLISM; LIPOPROTEIN BLOOD LEVEL; NONHUMAN; PRENATAL STRESS; PRIORITY JOURNAL; PROGENY; TRIACYLGLYCEROL BLOOD LEVEL;

ANIMALS; BODY WEIGHT; CALLITHRIX; CARDIOVASCULAR DISEASES; DEXAMETHASONE; FEMALE; GLUCOCORTICOIDS; LIPID METABOLISM; LIPIDS; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STRESS, PHYSIOLOGICAL;

CALLITHRIX JACCHUS; PRIMATES;

EID: 84864099119     PISSN: 00472565     EISSN: 16000684     Source Type: Journal    
DOI: 10.1111/j.1600-0684.2012.00551.x     Document Type: Article

References (58)

1. Alonso A, Martinez-Gonzalez MA, Serrano-Martinez M: Fish omega-3 fatty acids and risk of coronary heart disease. Med Clin 2003; 121:28-35.
2. Bagi CM, Volberg M, Moalli M, Shen V, Olson E, Hanson N, Berryman E, Andresen CJ: Age-related changes in marmoset trabecular and cortical bone and response to alendronate therapy resemble human bone physiology and architechture. Anat Rec (Hoboken) 2007; 290:1005-16.
3. Barker DJP, Hales CN, Fall CHD, Osmond C, Phipps K, Clark PMS: Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993; 36:62-7.
4. Beindorff N, Schlumbohm C, Einspanier A: Effects of synthetic pre-natal glucocorticoid application on foetal development of common marmoset monkeys (Callithrix jacchus). Reprod Domest Anim 2006; 41:16.
5. Bloom SL, Sheffield JS, McIntire DD, Leveno KJ: Antenatal dexamethasone and decreased birth weight. Obstet Gynecol 2001; 97:485-90.
6. Brown RW, Diaz R, Robson AC, Kotelevtsev YV, Mullins JJ, Kaufman MH, Seckl JR: The ontogeny of 11beta-hydroxysteroid dehydrogenase type 2 and mineralocorticoid receptor gene expression reveal intricate control of glucocorticoid action in development. Endocrinology 1996; 137:794-7.
7. Buitelaar JK, Huizink AC, Mulder EJ, de Medina PGR, Visser GHA: Prenatal stress and cognitive development and temperament in infants. Neurobiol Aging 2003; 24:S53-60.
8. Calder PC: N-3 fatty acids and cardiovascular disease: evidence explained and mechanisms explored. Clin Sci 2004; 107:1-11.
9. Carlsson L, Lind L, Larsson A: Reference values for 27 clinical chemistry tests in 70-year-old males and females. Gerontology 2010; 56:259-65.
10. Chapman MJ, Mc Taggart F, Goldstein S: Density distribution, characterization, and comparative aspects of the major serum lipoproteins in the common marmoset (Callithrix jacchus), a new world primate with potential use in lipoprotein research. Biochemistry 1979; 18:5096-108.
11. Charnock JS, Abeywardena MY, Poletti VM, McLennan PL: Differences in fatty-acid composition of various tissues of the marmoset monkey (Callithrix jacchus) after different lipid supplemented diets. Comp Biochem Physiol 1992; 101:387-93.
12. Copans SA: Human prenatal effects - methodological problems and some suggested solutions. Merrill Palmer Quart 1974; 20:43-52.
13. Dalziel SR, Walker NK, Parag V, Mantell C, Rea HH, Rodgers A, Harding JE: Cardiovascular risk factors after antenatal exposure to betamethasone: 30-year follow-up of a randomised controlled trial. Lancet 2005; 365:1856-62.
14. De Blasio MJ, Dodic M, Jefferies AJ, Moritz KM, Wintour EM, Owens JA: Maternal exposure to dexamethasone or cortisol in early pregnancy differentially alters insulin secretion and glucose homeostasis in adult male sheep offspring. Am J Physiol Endocrinol Metab 2007; 293:E75-82.
15. De Vries A, Holmes MC, Heijnis A, Seier JV, Heerden J, Louw J, Wolfe-Coote S, Meaney MJ, Levitt NS, Seckl JR: Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic-pituitary-adrenal axis function. J Clin Invest 2007; 117:1058-67.
16. Drake AJ, Liu L: Intergenerational transmission of programmed effects: public health concequences. Trends Endocrinol Metab 2010; 21:206-13.
17. Drake AJ, Walker BR: The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk. J Endocrinol 2004; 180:1-16.
18. Einspanier A, Lieder K, Brüns A, Husen B, Thole H, Simon C: Induction of endometriosis in the marmoset monkey (Callithrix jacchus). Mol Hum Reprod 2006; 12:291-9.
19. Einspanier A, Lieder K, Einspanier R, Husen B: The common marmoset monkey as a model for implantation and early pregnancy research. Methods Mol Med 2006; 121:111-21.
20. Einspanier A, Schlumbohm C, Beindorff N: Effects of synthetic glucocorticoid application on foetal and adult programming of the female marmoset monkey. J Reprod Fertil Abstr Ser 2006; 33:P22.
21. Emack J, Kostaki A, Walker CD, Matthews SG: Chronic maternal stress affects growth, behaviour and hypothalamo-pituitary-adrenal function in juvenile offspring. Horm Behav 2008; 54:514-20.
22. Eslamboli A: Marmoset monkey models of Parkinson's disease: which model, when and why? Brain Res Bull 2005; 68:140-9.
23. Fowden AL, Forhead AJ: Endocrine mechanisms of intrauterine programming. Reproduction 2004; 127:515-26.
24. French NP, Hagan R, Evans SF, Godfrey M, Newnham J: Repeated antenatal corticosteroids: size at birth and subsequent development. Am J Obstet Gynecol 1999; 180:114-21.
25. Fride E, Dan Y, Feldon J, Halevy G, Weinstock M: Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav 1986; 37:681-7.
26. Fuhrmann H, Zimmermann A, Gueck T, Oechtering G: Erythrocyte and plasma fatty acid patterns in dogs with atopic dermatitis and healthy dogs in the same household. Can J Vet Res 2006; 70:191-6.
27. Hauser J, Dettling-Artho A, Pilloud S, Maier C, Knapman A, Feldon J, Pryce CR: Effects of prenatal dexamethasone treatment on postnatal physical, endocrine, and social development in the common marmoset monkey. Endocrinology 2007; 148:1813-22.
28. Ikegami M, Jobe AH, Newnham J, Polk DH, Willet KE, Sly P: Repetitive prenatal glucocorticoids improve lung function and decrease growth in preterm lambs. Am J Respir Crit Care Med 1997; 156:178-84.
29. Jones A, Godfrey KM, Wood P, Osmond C, Goulden P, Phillips DIW: Fetal growth and the adrenocortical response to psychological stress. J Clin Endocrinol Metab 2006; 91:1868-71.
30. Kannel WB, Ho K, Thom T: Changing epidemiological features of cardiac failure. Br Heart J 1994; 72:S3-9.
31. Kaplan E, Shelmidine N: Factors influencing weight changes in callitrichids at the Bronx Zoo. Zoo Biol 2010; 29:551-66.
32. Kappler PM, Pereira ME: Primate Life Histories and Sociology. Chicago, IL: University of Chicago Press, 2003; p21.
33. Kinsella JE, Lokesh B, Stone RA: Dietary n-3 polyunsaturated fatty acids and amelioration of cardiovascular disease: possible mechanisms. Am J Clin Nutr 1990; 52:1-28.
34. Law CM, Shiell AW: Is blood pressure inversely related to birth weight? The strength of evidence from a systematic review of the literature. J Hypertens 1996; 14:935-41.
35. Li J, Olsen J, Vestergaard M, Obel C, Baker JL, Sorensen TIA: Prenatal stress exposure related to maternal bereavement and risk of childhood overweight. PLoS ONE 2010; 5:e11896.
36. Lusis AJ, Fogelman AM, Fonarow GC: Genetic basis of atherosclerosis: part I - new genes and pathways. Circulation 2004; 110:1868-73.
37. Marshall JW, Ridley RM: Assessment of cognitive and motor deficits in a marmoset model of stroke. ILAR J 2003; 44:153-60.
38. National Cholesterol Education Program (NCEP) 2002: Third report of the NCEP expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult treatment panel III) final report. National Institutes of Health (NIH) Publication Sep 2002; No.02-5215.
39. Nyirenda MJ, Carter R, Tang JI, de Vries A, Schlumbohm C, Hillier SG, Streit F, Oellerich M, Armstrong VW, Fuchs E, Seckl JR: Prenatal programming of metabolic syndrome in the common marmoset is associated with increased expression of 11 beta-hydroxysteroid dehydrogenase type 1. Diabetes 2009; 52:2873-9.
40. O'Regan D, Kenyon CJ, Seckl JR, Holmes MC: Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology. Am J Physiol Endocrinol Metab 2004; 287:E863-70.
41. Schmieder N, Tätzner S, Einspanier A: Prenatal glucocorticoid application has gender specific effects on marmoset offspring. Reprod Domest Anim 2009; 44:32.
42. Schneider ML: Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus-monkey infants. Dev Psychobiol 1992; 25:529-40.
43. Schwab M: Intrauterine Programmierung von Störungen der Hirnfunktion im späteren Leben. Gynäkol Geburtshilfliche Runds 2009; 49:13-8.
44. Seckl JR: Physiologic programming of the fetus. Clin Perinatol 1998; 25:939-62.
45. Seckl JR, Nyirenda MJ, Walker BR, Chapman KE: Glucocorticoids and fetal programming. Biochem Soc Trans 1999; 27:74-8.
46. Segal NL, Feng R, McGuire SA, Allison DB, Miller S: Genetic and environmental contributions to body mass index: comparative analysis of monozygotic twins, dizygotic twins, and same-age unrelated siblings. Int J Obes 2009; 33:37-41.
47. Siemelink M, Verhoef A, Dormans JAMA, Span PN, Piersma AH: Dietary fatty acid composition during pregnancy and lactation in the rat programs growth and glucose metabolism in the offspring. Diabetologia 2002; 45:1397-403.
48. Silventoinen K, Rokholm B, Kaprio J, Sorensen TIA: The genetic and environmental influences on childhood obesity: a systematic review of twin and adoption studies. Int J Obes 2010; 34:29-40.
49. Sugden MC, Langdown ML, Munns MJ, Holness MJ: Maternal glucocorticoid treatment modulates placental leptin and leptin receptor expression and materno-fetal leptin physiology during late pregnancy, and elicits hypertension associated with hyperleptinaemia in the early-growth-retarded adult offspring. Eur J Endocrinol 2001; 145:529-39.
50. 't Hart BA, Massacesi L: Clinical, pathological and immunologic aspects of the multiple sclerosis model in common marmosets (Callithrix jacchus). J Neuropathol Exp Neurol 2009; 68:341-55.
51. Tamashiro KLK, Moran TH: Perinatal environment and its influences on metabolic programming of offspring. Physiol Behav 2010; 100:560-6.
52. Tamashiro KLK, Terrillion CE, Hyun J, Koenig JI, Moran TH: Prenatal stress or high-fat diet increases susceptibility to diet-induced obesity in rat offspring. Diabetes 2009; 58:1116-25.
53. Tardif SD, Power ML, Ross CN, Rutherford JN, Layne-Colon DG, Paulik MA: Characterization of obese phenotypes in a small nonhuman primate, the common marmoset (Callithrix jacchus). Obesity 2009; 17:1499-505.
54. Tegethoff M, Pryce C, Meinlschmidt G: Effects of intrauterine exposure to synthetic glucocorticoids on fetal, newborn, and infant hypothalamic-pituitary-adrenal axis function in humans: a systematic review. Endocr Rev 2009; 30:753-89.
55. Woods LL, Weeks DA: Prenatal programming of adult blood pressure: role of maternal corticosteroids. Am J Physiol Regul Integr Comp Physiol 2005; 289:R955-62.
56. World Health Organization (WHO): Prevention of cardiovascular disease: guidelines for assessment and management of cardiovascular risk. Geneva: WHO Library Cataloguing-in-Publication Data, 2007.
57. Wright LL, Verter J, Younes N, Stevenson D, Fanaroff AA, Shankaran S, Ehrenkranz RA, Donovan EF: Antenatal corticosteroid administration and neonatal outcome in very low birth weight infants - the NICHD Neonatal Research Network. Am J Obstet Gynecol 1995; 173:269-74.
58. Zarrow MX, Philpott JE, Denenber VH: Passage of 14C-4-corticosterone from the rat mother to foetus and neonate. Nature 1970; 226:1058.