Mitochondrial gene expression profiles are associated with maternal psychosocial stress in pregnancy and infant temperament

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Lambertini, Luca ^a   Chen, Jia ^a   Nomura, Yoko ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; TRANSCRIPTOME;

ADULT; ANXIETY; ANXIETY ASSESSMENT; ARTICLE; BEHAVIOR ASSESSMENT; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INFANT; INFANT BEHAVIOR QUESTIONNAIRE REVISED; MALE; MATERNAL STRESS; MENTAL STRESS; MITOCHONDRIAL GENE; MT CO2 GENE; MT ND2 GENE; MT ND6 GENE; NEWBORN; PERCEIVED STRESS SCALE; PREGNANCY RELATED ANXIETIES QUESTIONNAIRE REVISED; PRENATAL EXPOSURE; STATE TRAIT ANXIETY INVENTORY; TEMPERAMENT; CHILD BEHAVIOR; COHORT ANALYSIS; FETUS DEVELOPMENT; GENETICS; METABOLISM; PHYSIOLOGY; PLACENTA; PREGNANCY; PREGNANCY COMPLICATION; PSYCHOLOGY;

ADULT; COHORT STUDIES; FEMALE; FETAL DEVELOPMENT; GENES, MITOCHONDRIAL; HUMANS; INFANT; INFANT BEHAVIOR; MALE; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS; STRESS, PSYCHOLOGICAL; TEMPERAMENT; TRANSCRIPTOME;

EID: 84947930566     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138929     Document Type: Article

References (91)

1. Del Giudice M. Fetal programming by maternal stress: Insights from a conflict perspective. Psychoneuroendocrinology. 2012; 37(10):1614-29. doi: 10.1016/j.psyneuen.2012.05.014 PMID: 22694951
2. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001; 293 (5532):1089-93. PMID: 11498579
3. Santos F, Dean W. Epigenetic reprogramming during early development in mammals. Reproduction. 2004; 127(6):643-51. PMID: 15175501
4. Austin MP, Hadzi-Pavlovic D, Leader L, Saint K, Parker G. Maternal trait anxiety, depression and life event stress in pregnancy: relationships with infant temperament. Early Hum Dev. 2005; 81(2):183-90. PMID: 15748973
5. Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM, et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry. 2010; 68(4):314-9. doi: 10.1016/j.biopsych.2010.05. 028 PMID: 20674602
6. Brand SR, Engel SM, Canfield RL, Yehuda R. The effect of maternal PTSD following in utero trauma exposure on behavior and temperament in the 9-month-old infant. Ann NY Acad Sci. 2006; 1071:454-8. PMID: 16891597
7. Malaspina D, Corcoran C, Kleinhaus KR, Perrin MC, Fennig S, Nahon D, et al. Acute maternal stress in pregnancy and schizophrenia in offspring: a cohort prospective study. BMC psychiatry. 2008; 8:71. doi: 10.1186/1471-244X-8-71 PMID: 18717990
8. Zhu P, Sun MS, Hao JH, Chen YJ, Jiang XM, Tao RX, et al. Does prenatal maternal stress impair cognitive development and alter temperament characteristics in toddlers with healthy birth outcomes? Dev Med Child Neurol. 2014; 56(3):283-9. doi: 10.1111/dmcn.12378 PMID: 24512346
9. Beijers R, Jansen J, Riksen-Walraven M, de Weerth C. Maternal prenatal anxiety and stress predict infant illnesses and health complaints. Pediatrics. 2010; 126(2):e401-9. doi: 10.1542/peds.2009-3226 PMID: 20643724
10. Davis EP, Glynn LM, Waffarn F, Sandman CA. Prenatal maternal stress programs infant stress regulation. J Child Psychol Psychiatry. 2011; 52(2):119-29. doi: 10.1111/j.1469-7610.2010.02314.x PMID: 20854366
11. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev. 2008; 32(6):1073-86. doi: 10.1016/j.neubiorev.2008.03.002 PMID: 18423592
12. Goldenthal MJ, Marin-Garcia J. Mitochondrial signaling pathways: a receiver/integrator organelle. Molecular and cellular biochemistry. 2004; 262(1-2):1-16. PMID: 15532704
13. Manoli I, Alesci S, Blackman MR, Su YA, Rennert OM, Chrousos GP. Mitochondria as key components of the stress response. Trends in endocrinology and metabolism: TEM. 2007; 18(5):190-8. PMID: 17500006
14. Acton QA Ed. Advances in Overweight Research and Treatment: 2012 Edition: ScholarlyBrief: Scholarly Editions; 2012.
15. Heininger K. The Cerebral Glucose-Fatty Acid Cycle: Evolutionary Roots, Regulation and (Pathophysiological Importance. In: Dwyer DS Ed. Glucose Metabolism in the Brain. Elsevier Science. 2002:103-58.
16. Kubera B, Hubold C, Otte S, Lindenberg AS, Zeiss I, Krause R, et al. Rise in plasma lactate concentrations with psychosocial stress: a possible sign of cerebral energy demand. Obesity facts. 2012; 5(3):384-92. doi: 10.1159/000339958 PMID: 22797365
17. Peters A, Kubera B, Hubold C, Langemann D. The selfish brain: stress and eating behavior. Frontiers in neuroscience. 2011; 5:74. doi: 10.3389/fnins.2011.00074 PMID: 21660101
18. Dalwadi DA, Uht RM. Hypothalamic and amygdalarcell lines differ markedly in mitochondrial rather than nuclear encoded gene expression. BMC Genomics. 2013; 14:413. doi: 10.1186/1471-2164-14-413 PMID: 23800343
19. Fujimoto M, Hayashi T. New insights into the role of mitochondria-associated endoplasmic reticulum membrane. International review of cell and molecular biology. 2011; 292:73-117. doi: 10.1016/B978-0-12-386033-0.00002-5 PMID: 22078959
20. Raturi A, Simmen T. Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM). Biochim Biophys Acta. 2013; 1833(1):213 doi: 10.1016/j.bbamcr.2012.04.013 PMID: 22575682
21. Scatena R, Bottoni P, Giardina B Eds. Advances in Mitochondrial Medicine. Adv Exp Med Biol. 2012; 942:1-461.
22. Adzic M, Djordjevic A, Demonacos C, Krstic-Demonacos M, Radojcic MB. The role of phosphorylated glucocorticoid receptor in mitochondrial functions and apoptotic signalling in brain tissue of stressed Wistar rats. The international journal of biochemistry & cell biology. 2009; 41(11):2181-8.
23. Picard M, Juster RP, McEwen BS. Mitochondrial allostatic load puts the 'gluc' back in glucocorticoids. Nature reviews Endocrinology. 2014; 10(5):303-10. doi: 10.1038/nrendo.2014.22 PMID: 24663223
24. Papa S, Martino PL, Capitanio G, Gaballo A, De Rasmo D, Signorile A, et al. The oxidative phosphorylation system in mammalian mitochondria. Advances in experimental medicine and biology. 2012; 942:3-37. doi: 10.1007/978-94-007-2869-1 1 PMID: 22399416
25. Belkacemi L, Desai M, Nelson DM, Ross MG. Altered mitochondrial apoptotic pathway in placentas from undernourished rat gestations. American journal of physiology Regulatory, integrative and comparative physiology. 2011; 301(6):R1599-615. doi: 10.1152/ajpregu.00100.2011 PMID: 21918224
26. Mayeur S, Lancel S, Theys N, Lukaszewski MA, Duban S, Bastide B, et al. Maternal calorie restriction modulates placental mitochondrial biogenesis and bioenergetic efficiency: involvement in feto-placental growth defects in rats. Am J Physiol Endocrinol Metab. 2012.
27. Hu D, Cross JC. Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol. 2010; 54(2-3):341-54. doi: 10.1387/ijdb.082768dh PMID: 19876834
28. Kingdom J, Huppertz B, Seaward G, Kaufmann P. Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol. 2000; 92(1):35 PMID: 10986432
29. Molina RD, Meschia G, Wilkening RB. Uterine blood flow, oxygen and glucose uptakes at mid-gestation in the sheep. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine. 1990; 195(3):379-85.
30. Aldoreta PW, Hay WW. Metabolic Substrates for Fetal Energy Metabolism and Growth. Clinics in Perinat. 1995; 22(1):15-37.
31. Martinez F, Milan R, Flores-Herrera O, Olvera-Sanchez S, Gomez-Chang E, Espinosa-Garcia MT. The Role of Mitochondria in Syncytiotrophoblast Cells: Bioenergetics and Steroidogenesis. In: Zheng J Ed. Recent Advances in Research on the Human Placenta. InTech Open Access Publisher:. 2012. p. 397-428.
32. Myatt L. Placental adaptive responses and fetal programming. J Physiol. 2006; 572(Pt 1):25-30. PMID: 16469781
33. Wright RO, Brunst KJ. Programming of respiratory health in childhood: influence of outdoor air pollution. Current opinion in pediatrics. 2013; 25(2):232-9. doi: 10.1097/MOP.0b013e32835e78cc PMID: 23422354
34. Davies W, Isles AR, Wilkinson LS. Imprinted gene expression in the brain. Neurosci Biobehav Rev. 2005; 29(3):421-30. PMID: 15820547
35. Wilkinson LS, Davies W, Isles AR. Genomic imprinting effects on brain development and function. Nat Rev Neurosci. 2007; 8(11):832-43. PMID: 17925812
36. Zeltser LM, Leibel RL. Roles of the placenta in fetal brain development. Proc Natl Acad Sci USA. 2011; 108(38):15667-8. doi: 10.1073/pnas.1112239108 PMID: 21890794
37. Bonnin A, Goeden N, Chen K, Wilson ML, King J, Shih JC, et al. A transient placental source of serotonin for the fetal forebrain. Nature. 2011; 472(7343):347-50. doi: 10.1038/nature09972 PMID: 21512572
38. Nieoullon A. Dopamine and the regulation. of cognition and attention. Prog Neurobiol. 2002; 67(1):53-83. PMID: 12126656
39. Turlejski K. Evolutionary ancient roles of serotonin: long-lasting regulation of activity and development. Actaneurobiologiaeexperimentalis. 1996; 56(2):619-36. PMID: 8768313
40. Holmboe K, Nemoda Z, Fearon RM, Csibra G, Sasvari-Szekely M, Johnson MH. Polymorphisms in dopamine system genes are associated with individual differences in attention in infancy. Developmental psychology. 2010; 46(2):404-16. doi: 10.1037/a0018180 PMID: 20210499
41. Wolpert L, Tickle C, Lawrence P, Meyerowitz E, Robertson E, Smith J, et al. Principles of Development-4th Edition. New York, NY-USA: Oxford University Press; 2010.
42. Callahan JL, Hynan MT. Identifying mothers at risk for postnatal emotional distress: further evidence for the validity of the perinatal posttraumatic stress disorder questionnaire. J Perinatol. 2002; 22(6):448-54. PMID: 12168121
43. DeMier RL, Hynan MT, Hatfield RF, Varner MW, Harris HB, Manniello RL. A measurement model of perinatal stressors: identifying risk for postnatal emotional distress in mothers of high-risk infants. J Clin Psychol. 2000; 56(1):89-100. PMID: 10661371
44. Huizink AC, Mulder EJ, Robles de Medina PG, Visser GH, Buitelaar JK. Is pregnancy anxiety a distinctive syndrome? Early Hum Dev. 2004; 79(2):81-91. PMID: 15324989
45. Spielberger CD. State-Trait Anxiety Inventory: Bibliography (2nd ed.). Palo Alto, CA-USA: Consulting Psychologists Press; 1989.
46. Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav. 1983; 24(4):385-96. PMID: 6668417
47. van den Bergh B. The influence of maternal emotions during pregnancy on fetal and neonatal behavior. Pre Peri Psychol J. 1990; 5:119-30.
48. First MB, Williams JBW, Spitzer RL, Gibbon M. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Clinical Trials Version (SCID-CT). New York (NY), USA: New York: Biometrics Research, New York State Psychiatric Institute; 2007.
49. Weissman MM, Wickramaratne P, Adams P, Wolk S, Verdeli H, Olfson M. Brief screening for family psychiatric history: the family history screen. Arch Gen Psychiatry. 2000; 57(7):675-82. PMID: 10891038
50. Gartstein MA, Rothbart MK. Studying infant temperament via the Revised Infant Behavior Questionnaire. Inf Behav Dev. 2003; 26(1):64-86.
51. Rothbart MK, Ahadi SA, Evans DE. Temperament and personality: origins and outcomes. J Pers Soc Psychol. 2000; 78(1):122-35. PMID: 10653510
52. Goldsmith HH, Campos JJ. The structure of temperamental fear and pleasure in infants: a psychometric perspective. Child Dev. 1990; 61(6):1944-64. PMID: 2083507
53. King JE. Standardized Coefficients in Logistic Regression. Baylor College of Medicine. 2007 [Internet]. Available: www.ccitonline.org/jking/homepage/standardized-paper.doc.
54. Chen J, Li Q, Rialdi A, Mystal E, Ly J, Finik J, et al. Influences of Maternal Stress during Pregnancy on the Epi/genome: Comparison of Placenta and Umbilical Cord Blood. Depress Anxiety. 2014; 3(2):1-6.
55. Du J, Wang Y, Hunter R, Wei Y, Blumenthal R, Falke C, et al. Dynamic regulation of mitochondrial function by glucocorticoids. Proc Natl Acad Sci USA. 2009; 106(9):3543-8. doi: 10.1073/pnas. 0812671106 PMID: 19202080
56. Davis EP, Sandman CA. The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Dev. 2010; 81(1):131-48. doi: 10.1111/j.1467-8624.2009.01385.x PMID: 20331658
57. Nomura Y, Halperin JM, Newcorn JH, Davey C, Fifer WP, Savitz DA, et al. The risk for impaired learning-related abilities in childhood and educational attainment among adults born near-term. J Pediatr Psychol. 2009; 34(4):406-18. doi: 10.1093/jpepsy/jsn092 PMID: 18794190
58. Nomura Y, Rajendran K, Brooks-Gunn J, Newcorn JH. Roles of perinatal problems on adolescent antisocial behaviors among children born after 33 completed weeks: a prospective investigation. J Child Psychol Psychiatry. 2008; 49(10):1108-17. doi: 10.1111/j.1469-7610.2008.01939.x PMID: 18673404
59. Badcock C, Crespi B. Imbalanced genomic imprinting in brain development: an evolutionary basis for the aetiology of autism. J Evol Biol. 2006; 19(4):1007-32. PMID: 16780503
60. Badcock C, Crespi B. Battle of the sexes may set the brain. Nature. 2008; 454(7208):1054-5. doi: 10.1038/4541054a PMID: 18756240
61. Crespi B, Badcock C. Psychosis and autism as diametrical disorders of the social brain. Behav Brain Sci. 2008; 31(3):241-61; discussion 61-320. doi: 10.1017/S0140525X08004214 PMID: 18578904
62. Bergman K, Sarkar P, O'Connor TG, Modi N, Glover V. Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. J Am Acad Child Adolesc Psychiatry. 2007; 46(11):1454-63. PMID: 18049295
63. Laplante DP, Brunet A, Schmitz N, Ciampi A, King S. Project Ice Storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry. 2008; 47(9):1063-72. doi: 10.1097/CHI.0b013e31817eec80 PMID: 18665002
64. van den Bergh BR, Mennes M, Oosterlaan J, Stevens V, Stiers P, Marcoen A, et al. High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neurosci Biobehav Rev. 2005; 29(2):259-69. PMID: 15811497
65. van den Bergh BR, Mennes M, Stevens V, van der Meere J, Borger N, Stiers P, et al. ADHD deficit as measured in adolescent boys with a continuous performance task is related to antenatal maternal anxiety. Pediatr Res. 2006; 59(1):78-82. PMID: 16327007
66. Murray L, Carothers AD. The validation of the Edinburgh Post-natal Depression Scale on a community sample. Br J Psychiatry. 1990; 157:288-90. PMID: 2224383
67. Buss KA, Dennis TA, Brooker RJ, Sippel LM. An ERP study of conflict monitoring in 4-8-year old children: associations with temperament. Developmental cognitive neuroscience. 2011; 1(2):131-40. doi: 10.1016/j.dcn.2010.12.003 PMID: 21666879
68. Ferguson E, Semper H, Yates J, Fitzgerald JE, Skatova A, James D. The 'dark side' and 'bright side' of personality: when too much conscientiousness and too little anxiety are detrimental with respect to the acquisition of medical knowledge and skill. PLoS One. 2014; 9(2):e88606. doi: 10.1371/journal.pone.0088606 PMID: 24586353
69. Hagekull B, Bohlin G. Early temperament and attachment as predictors of the Five Factor Model of personality. Attachment & human development. 2003; 5(1):2-18.
70. Choe DE, Lane JD, Grabell AS, Olson SL. Developmental precursors of young school-age children's hostile attribution bias. Developmental psychology. 2013; 49(12):2245-56. doi: 10.1037/a0032293 PMID: 23527492
71. Minamoto T, Osaka M, Yaoi K, Osaka N. Extrapunitive and intropunitive individuals activate different parts of the prefrontal cortex under an ego-blocking frustration. PLoS One. 2014; 9(1):e86036. doi: 10.1371/journal.pone.0086036 PMID: 24454951
72. Hunte C, Zickermann V, Brandt U. Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science. 2010; 329(5990):448-51. doi: 10.1126/science.1191046 PMID: 20595580
73. Mimaki M, Wang X, McKenzie M, Thorburn DR, Ryan MT. Understanding mitochondrial complex I assembly in health and disease. Biochim Biophys Acta. 2012; 1817(6):851-62. doi: 10.1016/j.bbabio.2011.08.010 PMID: 21924235
74. Ugalde C, Vogel R, Huijbens R, Van Den Heuvel B, Smeitink J, Nijtmans L. Human mitochondrial complex I assembles through the combination of evolutionary conserved modules: a framework to interpret complex I deficiencies. Hum Mol Genet. 2004; 13(20):2461 PMID: 15317750
75. Petruzzella V, Sardanelli AM, Scacco S, Panelli D, Papa F, Trentadue R, et al. Dysfunction of mitochondrial respiratory chain complex I in neurological disorders: genetics and pathogenetic mechanisms. Advances in experimental medicine and biology. 2012; 942:371-84. doi: 10.1007/978-94-007-2869-1 17 PMID: 22399432
76. Smeitink J, van den Heuvel L, DiMauro S. The genetics and pathology of oxidative phosphorylation. Nat Rev Genet. 2001; 2(5):342-52. PMID: 11331900
77. Lazarou M, Thorburn DR, Ryan MT, McKenzie M. Assembly of mitochondrial complex I and defects in disease. Biochim Biophys Acta. 2009; 1793(1):78-88. doi: 10.1016/j.bbamcr.2008.04.015 PMID: 18501715
78. Mathiesen C, Hagerhall C. The 'antiporter module' of respiratory chain complex I includes the MrpC/NuoK subunit - a revision of the modular evolution scheme. FEBS letters. 2003; 549(1-3):7-13. PMID: 12914915
79. Gureje O, Oladeji B, Hwang I, Chiu WT, Kessler RC, Sampson NA, et al. Parental psychopathology and the risk of suicidal behavior in their offspring: results from the World Mental Health surveys. Mol Psychiatry. 2011; 16(12):1221-33. doi: 10.1038/mp.2010.111 PMID: 21079606
80. Hirshfeld-Becker DR, Micco JA, Henin A, Petty C, Faraone SV, Mazursky H, et al. Psychopathology in adolescent offspring of parents with panic disorder, major depression, or both: a 10-year follow-up. Am J Psychiatry. 2012; 169(11):1175-84. PMID: 23534056
81. Vera J, Granero R, Ezpeleta L. Father's and mother's perceptions of parenting styles as mediators of the effects of parental psychopathology on antisocial behavior in outpatient children and adolescents. Child psychiatry and human development. 2012; 43(3):376-92. doi: 10.1007/s10578-011-0272-z PMID: 22120423
82. Vidair HB, Fichter CN, Kunkle KL, Boccia AS. Targeting parental psychopathology in child anxiety. Child Adolesc Psychiatr Clin N Am. 2012; 21(3):669-89. doi: 10.1016/j.chc.2012.05.007 PMID: 22801001
83. Oliva K, Barker G, Riley C, Bailey MJ, Permezel M, Rice GE, et al. The effect of pre-existing maternal obesity on the placental proteome: two-dimensional difference gel electrophoresis coupled with mass spectrometry. Journal of molecular endocrinology. 2012; 48(2):139-49. doi: 10.1530/JME-11-0123 PMID: 22301947
84. Azzu V, Jastroch M, Divakaruni AS, Brand MD. The regulation and turnover of mitochondrial uncoupling proteins. Biochim Biophys Acta. 2010; 1797(6-7):785-91. doi: 10.1016/j.bbabio.2010.02.035 PMID: 20211596
85. Echtay KS. Mitochondrial uncoupling proteins-what is their physiological role? Free radical biology & medicine. 2007; 43(10):1351-71.
86. Sluse FE. Uncoupling proteins: molecular, functional, regulatory, physiological and pathological aspects. Advances in experimental medicine and biology. 2012; 942:137-56. doi: 10.1007/978-94-007-2869-1 6 PMID: 22399421
87. Nicholls TJ, Rorbach J, Minczuk M. Mitochondria: Mitochondrial RNA metabolism and human disease. The international journal of biochemistry & cell biology. 2013.
88. Reinecke F, Smeitink JA, van der Westhuizen FH. OXPHOS gene expression and control in mitochondrial disorders. Biochim Biophys Acta. 2009; 1792(12):1113-21. doi: 10.1016/j.bbadis.2009.04.003 PMID: 19389473
89. Lazarou M, Smith SM, Thorburn DR, Ryan MT, McKenzie M. Assembly of nuclear DNA-encoded sub-units into mitochondrial complex IV, and their preferential integration into supercomplex forms in patient mitochondria. The FEBS journal. 2009; 276(22):6701-13. doi: 10.1111/j.1742-4658.2009.07384.x PMID: 19843159
90. Demonacos C, Djordjevic-Markovic R, Tsawdaroglou N, Sekeris CE. The mitochondrion as a primary site of action of glucocorticoids: the interaction of the glucocorticoid receptor with mitochondrial DNA sequences showing partial similarity to the nuclear glucocorticoid responsive elements. J Steroid Bio-chem Mol Biol. 1995; 55(1):43-55. PMID: 7577720
91. Berdanier CD. Mitochondrial gene expression: influence of nutrients and hormones. Exp Biol Med (Maywood). 2006; 231(10):1593-601.