Placental mitochondrial content and function in intrauterine growth restriction and preeclampsia

American Journal of Physiology - Endocrinology and Metabolism

Volumn 306, Issue 4, 2014, Pages

  Mando C ^a   De Palma, C ^a   Stampalija, T ^b   Anelli, G M ^a   Figus, M ^a   Novielli, C ^a   Parisi, F ^a   Clementi, E ^c   Ferrazzi, E ^b   Cetin, I ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c SCIENTIFIC INSTITUTE   (Italy)

Author keywords

Intrauterine growth restriction; Mitochondria; Placenta; Preeclampsia; Pregnancy

Indexed keywords

INTRAUTERINE GROWTH RESTRICTION; MITOCHONDRIA; PLACENTA; PREECLAMPSIA; PREGNANCY;

ADULT; DNA, MITOCHONDRIAL; FEMALE; FETAL GROWTH RETARDATION; HUMANS; INFANT, NEWBORN; MITOCHONDRIA; NUCLEAR RESPIRATORY FACTOR 1; OXYGEN CONSUMPTION; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; TROPHOBLASTS;

EID: 84894100802     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00426.2013     Document Type: Article

References (60)

1. Barrientos A. In vivo and in organello assessment of OXPHOS activities. Methods 26: 307-316, 2002.
2. Bell AW, Kennaugh JM, Battaglia FC, Makowski EL, Meschia G. Metabolic and circulatory studies of fetal lamb at midgestation. Am J Physiol Endocrinol Metab 250: E538-E544, 1986.
3. Bellotti M, Pennati G, De Gasperi C, Bozzo M, Battaglia FC, Ferrazzi E. Simultaneous measurements of umbilical venous, fetal hepatic, and ductus venosus blood flow in growth-restricted human fetuses. Am J Obstet Gynecol 190: 1347-1358, 2004.
4. Bertino E, Spada E, Occhi L, Coscia A, Giuliani F, Gagliardi L, Gilli G, Bona G, Fabris C, De Curtis M, Milani S. Neonatal anthropometric charts: the Italian neonatal study compared with other European studies. J Pediatr Gastroenterol Nutr 51: 353-361, 2010.
5. Brown MA, Lindheimer MD, de Swiet M, Van Assche A, Moutquin JM. The classification and diagnosis of the hypertensive disorders of pregnancy: statement from the International Society for the Study of Hypertension in Pregnancy (ISSHP). Hypertens Pregnancy 20: IX-XIV, 2001.
6. Campbell CT, Kolesar JE, Kaufman BA. Mitochondrial transcription factor A regulates mitochondrial transcription initiation, DNA packaging, and genome copy number. Biochim Biophys Acta 1819: 921-929, 2012.
7. Cetin I, Alvino G. Intrauterine growth restriction: implications for placental metabolism and transport. A review. Placenta 30, Suppl A: 77-82, 2009.
8. Cetin I, Barberis B, Brusati V, Brighina E, Mandia L, Arighi A, Radaelli T, Biondetti P, Bresolin N, Pardi G, Rango M. Lactate detection in the brain of growth-restricted fetuses with magnetic resonance spectroscopy. Am J Obstet Gynecol 205: 350. e1-e7, 2011.
9. Cetin I, Berti C, Mandò C, Parisi F. Placental iron transport and maternal absorption. Ann Nutr Metab 59: 55-58, 2011.
10. Cetin I, Giovannini N, Alvino G, Agostoni C, Riva E, Giovannini M, Pardi G. Intrauterine growth restriction is associated with changes in polyunsaturated fatty acid fetal-maternal relationships. Pediatr Res 52: 750-755, 2002.
11. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160: 189-200, 2003.
12. Civitarese AE, Smith SR, Ravussin E. Diet, energy metabolism and mitochondrial biogenesis. Curr Opin Clin Nutr Metab Care 10: 679-687, 2007.
13. Colleoni F, Lattuada D, Garretto A, Massari M, Mandò C, Somigliana E, Cetin I. Maternal blood mitochondrial DNA content during normal and intrauterine growth restricted (IUGR) pregnancy. Am J Obstet Gynecol 203: 365. e1-e6, 2010.
14. Constância M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, Stewart F, Kelsey G, Fowden A, Sibley C, Reik W. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417: 945-948, 2002.
15. Ellinger J, Müller DC, Müller SC, Hauser S, Heukamp LC, von Ruecker A, Bastian PJ, Walgenbach-Brunagel G. Circulating mitochondrial DNA in serum: a universal diagnostic biomarker for patients with urological malignancies. Urol Oncol 30: 509-515, 2012.
16. Ferrazzi E, Rigano S, Bozzo M, Bellotti M, Giovannini N, Galan H, Battaglia FC. Umbilical vein blood flow in growth-restricted fetuses. Ultrasound Obstet Gynecol 16: 432-438, 2000.
17. Fowden AL, Forhead AJ, White KL, Taylor PM. Equine uteroplacental metabolism at mid-and late gestation. Exp Physiol 85: 539-545, 2000.
18. Glazier JD, Cetin I, Perugino G, Ronzoni S, Grey AM, Mahendran D, Marconi AM, Pardi G, Sibley CP. Association between the activity of the system A amino acid transporter in the microvillous plasma membrane of the human placenta and severity of fetal compromise in intrauterine growth restriction. Pediatr Res 42: 514-519, 1997.
19. Gutsaeva DR, Carraway MS, Suliman HB, Demchenko IT, Shitara H, Yonekawa H, Piantadosi CA. Transient hypoxia stimulates mitochondrial biogenesis in brain subcortex by a neuronal nitric oxide synthasedependent mechanism. J Neurosci 28: 2015-2024, 2008.
20. Herrera E, Ortega-Senovilla H. Disturbances in lipid metabolism in diabetic pregnancy-are these the cause of the problem? Best Pract Res Clin Endocrinol Metab 24: 515-525, 2010.
21. Horard B, Vanacker JM. Estrogen receptor-related receptors: orphan receptors desperately seeking a ligand. J Mol Endocrinol 31: 349-357, 2003.
22. Huppertz B. Placental origins of preeclampsia: challenging the current hypothesis. Hypertension 51: 970-975, 2008.
23. Ikeda K, Shiba S, Horie-Inoue K, Shimokata K, Inoue S. A stabilizing factor for mitochondrial respiratory supercomplex assembly regulates energy metabolism in muscle. Nat Commun 4: 2147, 2013.
24. Jones CJ, Fox H. Ultrastructure of the normal human placenta (Review). Electron Microsc Rev 4: 129-178, 1991.
25. Kelly DP, Scarpulla RC. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 18: 357-368, 2004.
26. Kohler C, Radpour R, Barekati Z, Asadollahi R, Bitzer J, Wight E, Bürki N, Diesch C, Holzgreve W, Zhong XY. Levels of plasma circulating cell free nuclear and mitochondrial DNA as potential biomarkers for breast tumors. Mol Cancer 8: 105, 2009.
27. Lapuente-Brun E, Moreno-Loshuertos R, Acín-Pérez R, Latorre-Pellicer A, Colás C, Balsa E, Perales-Clemente E, Quirós PM, Calvo E, Rodríguez-Hernández MA, Navas P, Cruz R, Carracedo Á, López-Otín C, Pérez-Martos A, Fernández-Silva P, Fernández-Vizarra E, Enríquez JA. Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340: 1567-1570, 2013.
28. 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.
29. 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.
30. Lopez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, de Cabo R. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci USA 103: 1768-1773, 2006.
31. Luo J, Sladek R, Carrier J, Bader JA, Richard D, Giguère V. Reduced fat mass in mice lacking orphan nuclear receptor estrogen-related receptor alpha. Mol Cell Biol 23: 7947-7956, 2003.
32. Mandò C, Tabano S, Colapietro P, Pileri P, Colleoni F, Avagliano L, Doi P, Bulfamante G, Miozzo M, Cetin I. Transferrin receptor gene and protein expression and localization in human IUGR and normal term placentas. Placenta 32: 44-50, 2011.
33. Mandò C, Tabano S, Pileri P, Colapietro P, Marino MA, Avagliano L, Doi P, Bulfamante G, Miozzo M, Cetin I. SNAT2 expression and regulation in human growth restricted placentas. Pediatr Res 74: 104-110, 2013.
34. Mark PJ, Smith JT, Waddell BJ. Placental and fetal growth retardation following partial progesterone withdrawal in rat pregnancy. Placenta 27: 208-221, 2006.
35. Mayeur S, Lancel S, Theys N, Lukaszewski MA, Duban-Deweer S, Bastide B, Hachani J, Cecchelli R, Breton C, Gabory A, Storme L, Reusens B, Junien C, Vieau D, Lesage J. Maternal calorie restriction modulates placental mitochondrial biogenesis and bioenergetic efficiency: putative involvement in fetoplacental growth defects in rats. Am J Physiol Endocrinol Metab 304: E14-E22, 2013.
36. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, Sciorati C, Bracale R, Valerio A, Francolini M, Moncada S, Carruba MO. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299: 896-899, 2003.
37. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310: 314-317, 2005.
38. Palliser HK, Yates DM, Hirst JJ. Progesterone receptor isoform expression in response to in utero growth restriction in the fetal guinea pig brain. Neuroendocrinology 96: 60-67, 2012.
39. Pardi G, Cetin I, Marconi AM, Bozzetti P, Buscaglia M, Makowski EL, Battaglia FC. Venous drainage of the human uterus: respiratory gas studies in normal and fetal growth-retarded pregnancies. Am J Obstet Gynecol 166: 699-706, 1992.
40. Pardi G, Cetin I, Marconi AM, Lanfranchi A, Bozzetti P, Ferrazzi E, Buscaglia M, Battaglia FC. Diagnostic value of blood sampling in fetuses with growth retardation. N Engl J Med 328: 692-696, 1993.
41. Pejznochova M, Tesarova M, Hansikova H, Magner M, Honzik T, Vinsova K, Hajkova Z, Havlickova V, Zeman J. Mitochondrial DNA content and expression of genes involved in mtDNA transcription, regulation and maintenance during human fetal development. Mitochondrion 10: 321-329, 2010.
42. Pepe GJ, Albrecht ED. Actions of placental and fetal adrenal steroid hormones in primate pregnancy. Endocr Rev 16: 608-648, 1995.
43. Pesta D, Gnaiger E. High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. Methods Mol Biol 810: 25-58, 2012.
44. Poidatz D, Dos Santos E, Brulé A, De Mazancourt P, Dieudonné MN. Estrogen-related receptor gamma modulates energy metabolism target genes in human trophoblast. Placenta 33: 688-695, 2012.
45. Poston L, Igosheva N, Mistry HD, Seed PT, Shennan AH, Rana S, Karumanchi SA, Chappell LC. Role of oxidative stress and antioxidant supplementation in pregnancy disorders. Am J Clin Nutr 94, Suppl 6: 1980S-1985S, 2011.
46. th World Congress on Ultrasound in Obstetrics and Gynecology (ISUOG); Firenze, Italy; October 7-11, 2007 Ultrasound Obstet Gynecol 30: 444, 2007. Abstract OC250.
47. Ramenghi LA, Martinelli A, De Carli A, Brusati V, Mandia L, Fumagalli M, Triulzi F, Mosca F, Cetin I. Cerebral maturation in IUGR and appropriate for gestational age preterm babies. Reprod Sci 18: 469-475, 2011.
48. Ranhotra HS. The estrogen-related receptors: orphans orchestrating myriad functions. J Recept Signal Transduct Res 32: 47-56, 2012.
49. Regnault TR, de Vrijer B, Galan HL, Wilkening RB, Battaglia FC, Meschia G. Development and mechanisms of fetal hypoxia in severe fetal growth restriction. Placenta 28: 714-723, 2007.
50. Salvolini E, Vignini A, Nanetti L, Raffaelli F, Di Primio R, Mazzanti L, Tranquilli AL. Glutamate in vitro effects on human term placental mitochondria. J Matern Fetal Neonatal Med 25: 952-956, 2012.
51. Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 88: 611-638, 2008.
52. Schaiff WT, Bildirici I, Cheong M, Chern PL, Nelson DM, Sadovsky Y. Peroxisome proliferator-activated receptor-gamma and retinoid X receptor signaling regulate fatty acid uptake by primary human placental trophoblasts. J Clin Endocrinol Metab 90: 4267-4275, 2005.
53. Sibley CP, Turner MA, Cetin I, Ayuk P, Boyd CA, D'Souza SW, Glazier JD, Greenwood SL, Jansson T, Powell T. Placental phenotypes of intrauterine growth. Pediatr Res 58: 827-832, 2005.
54. Todros T, Ferrazzi E, Groli C, Nicolini U, Parodi L, Pavoni M, Zorzoli A, Zucca S. Fitting growth curves to head and abdomen measurements of the fetus: a multicentric study. J Clin Ultrasound 15: 95-105, 1987.
55. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: research0034, 2002.
56. Vartak R, Porras CA, Bai Y. Respiratory supercomplexes: structure, function and assembly. Protein Cell 4: 582-590, 2013.
57. Wakefield SL, Lane M, Mitchell M. Impaired mitochondrial function in the preimplantation embryo perturbs fetal and placental development in the mouse. Biol Reprod 84: 572-580, 2011.
58. Williams MA, Sanchez SE, Ananth CV, Hevner K, Qiu C, Enquobahrie DA. Maternal blood mitochondrial DNA copy number and placental abruption risk: results from a preliminary study. Int J Mol Epidemiol Genet 4: 120-127, 2013.
59. Zachariah R, Schmid S, Radpour R, Buerki N, Fan AX, Hahn S, Holzgreve W, Zhong XY. Circulating cell-free DNA as a potential biomarker for minimal and mild endometriosis. Reprod Biomed Online 18: 407-411, 2009.
60. Zung M, Alcolea MP, Garcμa-Palmer FJ, Young ME, Essop MF. Genomic modulation of mitochondrial respiratory genes in the hypertrophied heart reflects adaptive changes in mitochondrial and contractile function. Am J Physiol Heart Circ Physiol 293: H2819-H2825, 2007.