Impaired mitochondrial function in human placenta with increased maternal adiposity

American Journal of Physiology - Endocrinology and Metabolism

Volumn 307, Issue 5, 2014, Pages E419-E425

  Mele, James ^a   Muralimanoharan, Sribalasubashini ^a   Maloyan, Alina ^a   Myatt, Leslie ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Mitochondria; Obesity; Placenta

Indexed keywords

ADENOSINE TRIPHOSPHATE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR;

ARTICLE; BIOGENESIS; BODY MASS; CESAREAN SECTION; CYTOTROPHOBLAST; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRON TRANSPORT; FEMALE; FETUS DEVELOPMENT; FETUS GROWTH; GENE CONTROL; GESTATIONAL AGE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MALE; MATERNAL OBESITY; MITOCHONDRIAL RESPIRATION; OXYGEN CONSUMPTION; PLACENTA FUNCTION; PREGNANCY; RESPIRATORY CHAIN; SYNCYTIOTROPHOBLAST; TROPHOBLAST; WESTERN BLOTTING; ADULT; CELL CULTURE; CHORION VILLUS; ENERGY METABOLISM; METABOLISM; MITOCHONDRION; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PLACENTA; PREGNANCY COMPLICATION; ULTRASTRUCTURE;

MITOCHONDRIA; OBESITY; PLACENTA;

ADENOSINE TRIPHOSPHATE; ADIPOSITY; ADULT; BODY MASS INDEX; CELLS, CULTURED; CHORIONIC VILLI; ENERGY METABOLISM; FEMALE; HUMANS; MALE; MITOCHONDRIA; OBESITY; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS; REACTIVE OXYGEN SPECIES;

EID: 84907767481     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00025.2014     Document Type: Article

References (65)

1. Aguer C, Gambarotta D, Mailloux RJ, Moffat C, Dent R, McPherson R, Harper ME. Galactose enhances oxidative metabolism and reveals mitochondrial dysfunction in human primary muscle cells. PLoS One 6: e28536, 2011.
2. Barker DJ. The fetal and infant origins of adult disease. BMJ 301: 1111, 1990.
3. Bax BE, Bloxam DL. Energy metabolism and glycolysis in human placental trophoblast cells during differentiation. Biochim Biophys Acta 1319: 283-292, 1997.
4. Brand MD, Nicholls DG. Assessing mitochondrial dysfunction in cells. Biochem J 435: 297-312, 2011.
5. Bullock GC, Delehanty LL, Talbot AL, Gonias SL, Tong WH, Rouault TA, Dewar B, Macdonald JM, Chruma JJ, Goldfarb AN. Iron control of erythroid development by a novel aconitase-associated regulatory pathway. Blood 116: 97-108, 2010.
6. Catalano PM. Obesity and pregnancy—the propagation of a viscous cycle? J Clin Endocrinol Metab 88: 3505-3506, 2003.
7. Clifton VL. Sexually dimorphic effects of maternal asthma during pregnancy on placental glucocorticoid metabolism and fetal growth. Cell Tissue Res 322: 63-71, 2005.
8. Crunkhorn S, Dearie F, Mantzoros C, Gami H, da Silva WS, Espinoza D, Faucette R, Barry K, Bianco AC, Patti ME. Peroxisome proliferator activator receptor gamma coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation. J Biol Chem 282: 15439-15450, 2007.
9. Cui X., Brockman D, Campos B, Myatt L. Expression of NADPH oxidase isoform 1 (Nox1) in human placenta: involvement in preeclampsia. Placenta 27: 422-431, 2006.
10. Eriksson JG, Kajantie E, Osmond C, Thornburg K, Barker DJ. Boys live dangerously in the womb. Am J Hum Biol 22: 330-335, 2010.
11. Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9: 203-209, 2009.
12. Forsén T, Eriksson JG, Tuomilehto J, Teramo K, Osmond C, Barker DJ. Mother’s weight in pregnancy and coronary heart disease in a cohort of Finnish men: follow up study. BMJ 315: 837-840, 1997.
13. Galtier-Dereure F, Boegner C, Bringer J. Obesity and pregnancy: complications and cost. Am J Clin Nutr 71: 1242S-1248S, 2000.
14. Gohil VM, Sheth SA, Nilsson R, Wojtovich AP, Lee JH, Perocchi F, Chen W, Clish CB, Ayata C, Brookes PS, Mootha VK. Nutrient sensitized screening for drugs that shift energy metabolism from mitochondrial respiration to glycolysis. Nat Biotechnol 28: 249-255, 2010.
15. Guelinckx I, Devlieger R, Beckers K, Vansant G. Maternal obesity: pregnancy complications, gestational weight gain and nutrition. Obes Rev 9: 140-150, 2008.
16. Guillet C, Delcourt I, Rance M, Giraudet C, Walrand S, Bedu M, Duche P, Boirie Y. Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men. J Clin Endocrinol Metab 94: 3044-3050, 2009.
17. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK, Story M, Le QT, Giaccia AJ. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 35: 856-867, 2009.
18. Jarvie E, Hauguel-de-Mouzon S, Nelson SM, Sattar N, Catalano PM, Freeman DJ. Lipotoxicity in obese pregnancy and its potential role in adverse pregnancy outcome and obesity in the offspring. Clin Sci (Lond) 119: 123-129, 2010.
19. Justo R, Boada J, Frontera M, Oliver J, Bermúdez J, Gianotti M. Gender dimorphism in rat liver mitochondrial oxidative metabolism and biogenesis. Am J Physiol Cell Physiol 289: C372-C378, 2005.
20. Kalichman MW, Powell HC, Mizisin AP. Reactive, degenerative, and proliferative Schwann cell responses in experimental galactose and human diabetic neuropathy. Acta Neuropathol 95: 47-56, 1998.
21. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
22. Lagranha CJ, Deschamps A, Aponte A, Steenbergen C, Murphy E. Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res 106: 1681-1691, 2010.
23. Larsen S, Stride N, Hey-Mogensen M, Hansen CN, Bang LE, Bund-gaard H, Nielsen LB, Helge JW, Dela F. Simvastatin effects on skeletal muscle: relation to decreased mitochondrial function and glucose intolerance. J Am Coll Cardiol 61: 44-53, 2013.
24. Lattuada D, Colleoni F, Martinelli A, Garretto A, Magni R, Radaelli T, Cetin I. Higher mitochondrial DNA content in human IUGR placenta. Placenta 29: 1029-1033, 2008.
25. Leduc L, Levy E, Bouity-Voubou M, Delvin E. Fetal programming of atherosclerosis: possible role of the mitochondria. Eur J Obstet Gynecol Reprod Biol 149: 127-130, 2010.
26. Lee HC, Wei YH. Oxidative stress, mitochondrial DNA mutation, and apoptosis in aging. Exp Biol Med (Maywood) 232: 592-606, 2007.
27. Llurba E, Gratacós E, Martín-Gallán P, Cabero L, Dominguez C. A comprehensive study of oxidative stress and antioxidant status in preeclampsia and normal pregnancy. Free Radic Biol Med 37: 557-570, 2004.
28. Maloyan A, Mele J, Muralimanohara B, Myatt L. Measurement of mitochondrial respiration in trophoblast culture. Placenta 33: 456-458, 2012.
29. Mao J, Zhang X, Sieli PT, Falduto MT, Torres KE, Rosenfeld CS. Contrasting effects of different maternal diets on sexually dimorphic gene expression in the murine placenta. Proc Natl Acad Sci USA 107: 5557-5562, 2010.
30. Marroquin LD, Hynes J, Dykens JA, Jamieson JD, Will Y. Circumventing the Crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants. Toxicol Sci 97: 539-547, 2007.
31. Mayhew TM. Taking tissue samples from the placenta: an illustration of principles and strategies. Placenta 29: 1-14, 2008.
32. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273, 2003.
33. Muralimanoharan S, Maloyan A, Mele J, Guo C, Myatt L., Myatt L. MIR-210 modulates mitochondrial respiration in placenta with preeclampsia. Placenta 33: 816-823, 2012.
34. Muralimanoharan S, Maloyan A, Myatt L. Evidence of sexual dimorphism in the placental function with severe preeclampsia. Placenta 34: 1183-1189, 2013.
35. Murphy VE, Gibson P, Talbot PI, Clifton VL. Severe asthma exacerbations during pregnancy. Obstet Gynecol 106: 1046-1054, 2005.
36. Murphy VE, Gibson PG, Giles WB, Zakar T, Smith R, Bisits AM, Kessell CG, Clifton VL. Maternal asthma is associated with reduced female fetal growth. Am J Respir Crit Care Med 168: 1317-1323, 2003.
37. Myatt L, Cui X. Oxidative stress in the placenta. Histochem Cell Biol 122: 369-382, 2004.
38. Nakamura MT, Yudell BE, Loor JJ. Regulation of energy metabolism by long-chain fatty acids. Prog Lipid Res 53: 124-144, 2014.
39. Noland RC, Koves TR, Seiler SE, Lum H, Lust RM, Ilkayeva O, Stevens RD, Hegardt FG, Muoio DM. Carnitine insufficiency caused by aging and overnutrition compromises mitochondrial performance and metabolic control. J Biol Chem 284: 22840-22852, 2009.
40. Olivera AA, Meigs RA. Mitochondria from human term placenta. I. Isolation and assay conditions for oxidative phosphorylation. Biochim Biophys Acta 376: 426-435, 1975.
41. Osei-Kumah A, Smith R, Jurisica I, Caniggia I, Clifton VL. Sex-specific differences in placental global gene expression in pregnancies complicated by asthma. Placenta 32: 570-578, 2011.
42. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, Landaker EJ, Goldfine AB, Mun E, DeFronzo R, Finlayson J, Kahn CR, Mandarino LJ. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 100: 8466-8471, 2003.
43. Prescott SL, Clifton V. Asthma and pregnancy: emerging evidence of epigenetic interactions in utero. Curr Opin Allergy Clin Immunol 9: 417-426, 2009.
44. Pruis MG, van Ewijk PA, Schrauwen-Hinderling VB, Plösch T. Lipotoxicity and the role of maternal nutrition. Acta Physiol (Oxf). In press.
45. Ritov VB, Menshikova EV, Azuma K, Wood R, Toledo FG, Goodpaster BH, Ruderman NB, Kelley DE. Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity. Am J Physiol Endocrinol Metab 298: E49-E58, 2010.
46. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54: 8-14, 2005.
47. Robinson BH, Petrova-Benedict R, Buncic JR, Wallace DC. Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts. Biochem Med Metab Biol 48: 122-126, 1992.
48. Rossignol R, Gilkerson R, Aggeler R, Yamagata K, Remington SJ, Capaldi RA. Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res 64: 985-993, 2004.
49. Sanz A, Hiona A, Kujoth GC, Seo AY, Hofer T, Kouwenhoven E, Kalani R, Prolla TA, Barja G, Leeuwenburgh C. Evaluation of sex differences on mitochondrial bioenergetics and apoptosis in mice. Exp Gerontol 42: 173-182, 2007.
50. Schmatz M, Madan J, Marino T, Davis J. Maternal obesity: the interplay between inflammation, mother and fetus. J Perinatol 30: 441-446, 2010.
51. Schonfeld P, Wojtczak L. Fatty acids as modulators of the cellular production of reactive oxygen species. Free Radic Biol Med 45: 231-241, 2008.
52. Sena LA, Chandel NS. Physiological roles of mitochondrial reactive oxygen species. Mol Cell 48: 158-167, 2012.
53. Sood R, Zehnder JL, Druzin ML, Brown PO. Gene expression patterns in human placenta. Proc Natl Acad Sci USA 103: 5478-5483, 2006.
54. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA, Smith SR. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54: 1926-1933, 2005.
55. Stark MJ, Clifton V., Wright IMR. Sex-specific differences in peripheral microvascular blood flow in preterm infants. Pediatr Res 63: 415-419, 2008.
56. Sun G, Ukkola O, Rankinen T, Joanisse DR, Bouchard C. Skeletal muscle characteristics predict body fat gain in response to overfeeding in never-obese young men. Metabolism 51: 451-456, 2002.
57. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 552: 335-344, 2003.
58. Valerio A, Cardile A, Cozzi V, Bracale R, Tedesco L, Pisconti A, Palomba L, Cantoni O, Clementi E, Moncada S, Carruba MO, Nisoli E. TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 116: 2791-2798, 2006.
59. Valsamakis G, Kanaka-Gantenbein C, Malamitsi-Puchner A, Mastorakos G. Causes of intrauterine growth restriction and the postnatal development of the metabolic syndrome. Ann NY Acad Sci 1092: 138-147, 2006.
60. Venegas V, Wang J, Dimmock D, Wong LJ. Real-time quantitative PCR analysis of mitochondrial DNA content. Curr Protoc Hum Genet Chapter 19: Unit 19.7, 2011.
61. Wang Y, Walsh SW. Placental mitochondria as a source of oxidative stress in pre-eclampsia. Placenta 19: 581-586, 1998.
62. Watson AL, Skepper JN, Jauniaux E, Burton GJ. Susceptibility of human placental syncytiotrophoblastic mitochondria to oxygen-mediated damage in relation to gestational age. J Clin Endocrinol Metab 83: 1697-1705, 1998.
63. Wilson-Fritch L, Nicoloro S, Chouinard M, Lazar MA, Chui PC, Leszyk J, Straubhaar J, Czech MP, Corvera S. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J Clin Invest 114: 1281-1289, 2004.
64. Wu G, Imhoff-Kunsch B, Girard AW. Biological mechanisms for nutritional regulation of maternal health and fetal development. Paediatr Perinat Epidemiol 26, Suppl 1: 4-26, 2012.
65. Yen SS. The placenta as the third brain. J Reprod Med 39: 277-280, 1994.