Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T07:03:54.546Z Has data issue: false hasContentIssue false
  • English
  • Français

Sex-specific effects of maternal and postweaning high-fat diet on skeletal muscle mitochondrial respiration

Published online by Cambridge University Press:  16 August 2018

A. V. Khamoui ,
M. Desai ,
M. G. Ross  and
H. B. Rossiter
A. V. Khamoui
Affiliation:
Rehabilitation Clinical Trials Center, Division of Respiratory and Critical Care Physiology and Medicine, Department of Medicine, Rehabilitation Clinical Trials Center, Division of Respiratory and Critical Care Physiology and Medicine, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA Department of Exercise Science and Health Promotion, Florida Atlantic University, Boca Raton, FL, USA
M. Desai
Affiliation:
Perinatal Research Laboratories, Department of Obstetrics and Gynecology, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA
M. G. Ross
Affiliation:
Perinatal Research Laboratories, Department of Obstetrics and Gynecology, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA
H. B. Rossiter*
Affiliation:
Rehabilitation Clinical Trials Center, Division of Respiratory and Critical Care Physiology and Medicine, Department of Medicine, Rehabilitation Clinical Trials Center, Division of Respiratory and Critical Care Physiology and Medicine, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA Faculty of Biological Sciences, University of Leeds, Leeds, UK
*
*Address for correspondence: H. B. Rossiter, Division of Respiratory and Critical Care Physiology and Medicine, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, 1124 W. Carson St., CDCRC Building, Torrance, CA 90502, USA.E-mail: hrossiter@ucla.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Exposure to maternal over-nutrition in utero is linked with developmental programming of obesity, metabolic syndrome and cardiovascular disease in offspring, which may be exacerbated by postnatal high-fat (HF) diet. Skeletal muscle mitochondrial function contributes to substrate metabolism and is impaired in metabolic disease. We examined muscle mitochondrial respiration in male and female mice exposed to maternal HF diet in utero, followed by postweaning HF diet until middle age. After in utero exposure to maternal control (Con) or HF diet (45% kcal fat; 39.4% lard, 5.5% soybean oil), offspring were weaned to Con or HF, creating four groups: Con/Con (male/female (m/f), n=8/8), Con/HF (m/f, n=7/4), HF/Con (m/f, n=9/6) and HF/HF (m/f, n=4/4). Oxidative phosphorylation (OXPHOS) and electron transfer system (ETS) capacity were measured in permeabilized gastrocnemius bundles. Maternal HF diet increased fasting glucose and lean body mass in males and body fat percentage in both sexes (P⩽0.05). Maximal adenosine diphosphate-stimulated respiration (complex I OXPHOS) was decreased by maternal HF diet in female offspring (−21%, P=0.053), but not in male (−0%, P>0.05). Sexually divergent responses were exacerbated in offspring weaned to HF diet. In females, OXPHOS capacity was lower (−28%, P=0.041) when weaned to high-fat (HF/HF) v. control diet (HF/Con). In males, OXPHOS (+33%, P=0.009) and ETS (+42%, P=0.016) capacity increased. Our data suggest that maternal lard-based HF diet, rich in saturated fat, affects offspring skeletal muscle respiration in a sex-dependent manner, and these differences are exacerbated by HF diet in adulthood.

Keywords

developmental programmingfetal programming, oxidative phosphorylationrespirometrysexual dimorphism
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 6 , December 2018 , pp. 670 - 677
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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.)

References

1. World Health Organization. Chapter 7. Global Target: 7: halt the rise in diabetes and obesity. Global Status Report on Noncommunicable Diseases. 2014; pp. 79–93. WHO Press: Geneva.Google Scholar
2. Kelly, T, Yang, W, Chen, CS, Reynolds, K, He, J. Global burden of obesity in 2005 and projections to 2030. Int J Obes (Lond). 2008; 32, 1431–1437.Google Scholar
3. Wang, Y, Beydoun, MA, Liang, L, Caballero, B, Kumanyika, SK. Will all Americans become overweight or obese? Estimating the progression and cost of the US obesity epidemic. Obesity (Silver Spring). 2008; 16, 2323–2330.Google Scholar
4. Flegal, KM, Carroll, MD, Kit, BK, Ogden, CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA. 2012; 307, 491–497.Google Scholar
5. Fisher, SC, Kim, SY, Sharma, AJ, Rochat, R, Morrow, B. Is obesity still increasing among pregnant women? Prepregnancy obesity trends in 20 states, 2003-2009. Prev Med. 2013; 56, 372–378.Google Scholar
6. Baeten, JM, Bukusi, EA, Lambe, M. Pregnancy complications and outcomes among overweight and obese nulliparous women. Am J Public Health. 2001; 91, 436–440.Google Scholar
7. White, CL, Purpera, MN, Morrison, CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R1464–R1472.Google Scholar
8. Srinivasan, M, Katewa, SD, Palaniyappan, A, Pandya, JD, Patel, MS. Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood. Am J Physiol Endocrinol Metab. 2006; 291, E792–E799.Google Scholar
9. Barker, DJ. The developmental origins of adult disease. J Am Coll Nutr. 2004; 23(6 Suppl.), 588S–595S.Google Scholar
10. Desai, M, Jellyman, JK, Han, G, et al. Maternal obesity and high-fat diet program offspring metabolic syndrome. Am J Obstet Gynecol. 2014; 211, 237 e231–237 e213.Google Scholar
11. Guberman, C, Jellyman, JK, Han, G, Ross, MG, Desai, M. Maternal high-fat diet programs rat offspring hypertension and activates the adipose renin-angiotensin system. Am J Obstet Gynecol. 2013; 209, 262 e261–262 e268.Google Scholar
12. Lee, KK, Raja, EA, Lee, AJ, et al. Maternal obesity during pregnancy associates with premature mortality and major cardiovascular events in later life. Hypertension. 2015; 66, 938–944.Google Scholar
13. Reynolds, RM, Allan, KM, Raja, EA, et al. Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. BMJ. 2013; 347, f4539.Google Scholar
14. Turdi, S, Ge, W, Hu, N, et al. Interaction between maternal and postnatal high fat diet leads to a greater risk of myocardial dysfunction in offspring via enhanced lipotoxicity, IRS-1 serine phosphorylation and mitochondrial defects. J Mol Cell Cardiol. 2013; 55, 117–129.Google Scholar
15. Shankar, K, Harrell, A, Liu, X, et al. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R528–R538.Google Scholar
16. Page, KC, Malik, RE, Ripple, JA, Anday, EK. Maternal and postweaning diet interaction alters hypothalamic gene expression and modulates response to a high-fat diet in male offspring. Am J Physiol Regul Integr Comp Physiol. 2009; 297, R1049–R1057.Google Scholar
17. Muralimanoharan, S, Gao, X, Weintraub, S, Myatt, L, Maloyan, A. Sexual dimorphism in activation of placental autophagy in obese women with evidence for fetal programming from a placenta-specific mouse model. Autophagy. 2016; 12, 752–769.Google Scholar
18. Muralimanoharan, S, Guo, C, Myatt, L, Maloyan, A. Sexual dimorphism in miR-210 expression and mitochondrial dysfunction in the placenta with maternal obesity. Int J Obes (Lond). 2015; 39, 1274–1281.Google Scholar
19. Mele, J, Muralimanoharan, S, Maloyan, A, Myatt, L. Impaired mitochondrial function in human placenta with increased maternal adiposity. Am J Physiol Endocrinol Metab. 2014; 307, E419–E425.Google Scholar
20. Aiken, CE, Tarry-Adkins, JL, Penfold, NC, Dearden, L, Ozanne, SE. Decreased ovarian reserve, dysregulation of mitochondrial biogenesis, and increased lipid peroxidation in female mouse offspring exposed to an obesogenic maternal diet. FASEB J. 2016; 30, 1548–1556.Google Scholar
21. Fernandez-Twinn, DS, Blackmore, HL, Siggens, L, et al. 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.Google Scholar
22. Alfaradhi, MZ, Fernandez-Twinn, DS, Martin-Gronert, MS, et al. Oxidative stress and altered lipid homeostasis in the programming of offspring fatty liver by maternal obesity. Am J Physiol Regul Integr Comp Physiol. 2014; 307, R26–R34.Google Scholar
23. Borengasser, SJ, Faske, J, Kang, P, et al. In utero exposure to prepregnancy maternal obesity and postweaning high-fat diet impair regulators of mitochondrial dynamics in rat placenta and offspring. Physiol Genomics. 2014; 46, 841–850.Google Scholar
24. Latouche, C, Heywood, SE, Henry, SL, et al. Maternal overnutrition programs changes in the expression of skeletal muscle genes that are associated with insulin resistance and defects of oxidative phosphorylation in adult male rat offspring. J Nutr. 2014; 144, 237–244.Google Scholar
25. Battaglia, GM, Zheng, D, Hickner, RC, Houmard, JA. Effect of exercise training on metabolic flexibility in response to a high-fat diet in obese individuals. Am J Physiol Endocrinol Metab. 2012; 303, E1440–E1445.Google Scholar
26. Galgani, JE, Moro, C, Ravussin, E. Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab. 2008; 295, E1009–E1017.Google Scholar
27. Chomentowski, P, Coen, PM, Radikova, Z, Goodpaster, BH, Toledo, FG. Skeletal muscle mitochondria in insulin resistance: differences in intermyofibrillar versus subsarcolemmal subpopulations and relationship to metabolic flexibility. J Clin Endocrinol Metab. 2011; 96, 494–503.Google Scholar
28. Dube, JJ, Coen, PM, DiStefano, G, et al. Effects of acute lipid overload on skeletal muscle insulin resistance, metabolic flexibility, and mitochondrial performance. Am J Physiol Endocrinol Metab. 2014; 307, E1117–E1124.Google Scholar
29. Saben, JL, Boudoures, AL, Asghar, Z, et al. Maternal Metabolic Syndrome Programs Mitochondrial Dysfunction via Germline Changes across Three Generations. Cell Rep. 2016; 16, 1–8.Google Scholar
30. Pileggi, CA, Hedges, CP, Segovia, SA, et al. Maternal high fat diet alters skeletal muscle mitochondrial catalytic activity in adult male rat offspring. Front Physiol. 2016; 7, 546.Google Scholar
31. Hellgren, LI, Jensen, RI, Waterstradt, MS, Quistorff, B, Lauritzen, L. Acute and perinatal programming effects of a fat-rich diet on rat muscle mitochondrial function and hepatic lipid accumulation. Acta Obstet Gynecol Scand. 2014; 93, 1170–1180.Google Scholar
32. Miller, VM, Reckelhoff, JF. Sex as a biological variable: now what?! Physiology (Bethesda). 2016; 31, 78–80.Google Scholar
33. Khan, IY, Taylor, PD, Dekou, V, et al. Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension. 2003; 41, 168–175.Google Scholar
34. Morrow, RM, Picard, M, Derbeneva, O, et al. Mitochondrial energy deficiency leads to hyperproliferation of skeletal muscle mitochondria and enhanced insulin sensitivity. Proc Natl Acad Sci U S A. 2017; 114, 2705–2710.Google Scholar
35. Pesta, D, Gnaiger, E. High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. Methods Mol Biol. 2012; 810, 25–58.Google Scholar
36. Kuznetsov, AV, Veksler, V, Gellerich, FN, et al. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc. 2008; 3, 965–976.Google Scholar
37. Shelley, P, Martin-Gronert, MS, Rowlerson, A, et al. Altered skeletal muscle insulin signaling and mitochondrial complex II-III linked activity in adult offspring of obese mice. Am J Physiol Regul Integr Comp Physiol. 2009; 297, R675–R681.Google Scholar
38. Simar, D, Chen, H, Lambert, K, Mercier, J, Morris, MJ. Interaction between maternal obesity and post-natal over-nutrition on skeletal muscle metabolism. Nutr Metab Cardiovasc Dis. 2012; 22, 269–276.Google Scholar
39. Divakaruni, AS, Brand, MD. The regulation and physiology of mitochondrial proton leak. Physiology (Bethesda). 2011; 26, 192–205.Google Scholar
40. Moran, A, Jacobs, DR Jr, Steinberger, J, et al. Changes in insulin resistance and cardiovascular risk during adolescence: establishment of differential risk in males and females. Circulation. 2008; 117, 2361–2368.Google Scholar
41. Newbold, RR, Padilla-Banks, E, Snyder, RJ, Jefferson, WN. Perinatal exposure to environmental estrogens and the development of obesity. Mol Nutr Food Res. 2007; 51, 912–917.Google Scholar
42. Newbold, RR, Padilla-Banks, E, Jefferson, WN. Environmental estrogens and obesity. Mol Cell Endocrinol. 2009; 304, 84–89.Google Scholar
43. Van Pelt, RE, Gozansky, WS, Schwartz, RS, Kohrt, WM. Intravenous estrogens increase insulin clearance and action in postmenopausal women. Am J Physiol Endocrinol Metab. 2003; 285, E311–E317.Google Scholar
44. Grantham, JP, Henneberg, M. The estrogen hypothesis of obesity. PLoS One. 2014; 9, e99776.Google Scholar
45. Levadoux, E, Morio, B, Montaurier, C, et al. Reduced whole-body fat oxidation in women and in the elderly. Int J Obes Relat Metab Disord. 2001; 25, 39–44.Google Scholar
46. Uranga, AP, Levine, J, Jensen, M. Isotope tracer measures of meal fatty acid metabolism: reproducibility and effects of the menstrual cycle. Am J Physiol Endocrinol Metab. 2005; 288, E547–E555.Google Scholar
47. Tarnopolsky, MA. Sex differences in exercise metabolism and the role of 17-beta estradiol. Med Sci Sports Exerc. 2008; 40, 648–654.Google Scholar
48. Pavlisova, J, Bardova, K, Stankova, B, et al. Corn oil versus lard: metabolic effects of omega-3 fatty acids in mice fed obesogenic diets with different fatty acid composition. Biochimie. 2016; 124, 150–162.Google Scholar