Exposure to intrauterine inflammation alters metabolomic profiles in the amniotic fluid, fetal and neonatal brain in the mouse

PLoS ONE

Volumn 12, Issue 10, 2017, Pages

  Brown, Amy G ^a   Tulina, Natalia M ^a   Barila, Guillermo O ^a   Hester, Michael S ^a   Elovitz, Michal A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYLADENOSINE; 6 N METHYLADENOSINE; BIOLOGICAL MARKER; BRANCHED CHAIN AMINO ACID; FATTY ACID; GLUTAMIC ACID; GUANINE; GUANOSINE; HISTIDINE; HYPOXANTHINE; INOSINE; LYSINE; TRYPTOPHAN; URATE; XANTHINE;

AMINO ACID METABOLISM; AMNION FLUID; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BIOCHEMICAL ANALYSIS; BRAIN METABOLISM; CD-1 MOUSE; CONTROLLED STUDY; EMBRYO; FEMALE; FETUS; INFLAMMATION; INTRAUTERINE INFLAMMATION; LIPID METABOLISM; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MALE; METABOLOME; METABOLOMICS; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE METABOLISM; PRENATAL DISORDER; PURINE METABOLISM; SEX DIFFERENCE; SIGNAL TRANSDUCTION; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANIMAL; BRAIN; METABOLISM; PATHOLOGY; PREGNANCY; UTERUS;

AMNIOTIC FLUID; ANIMALS; ANIMALS, NEWBORN; BRAIN; FEMALE; INFLAMMATION; METABOLOMICS; MICE; PREGNANCY; UTERUS;

EID: 85031769546     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0186656     Document Type: Article

References (52)

1. Burd I, Bentz AI, Chai J, Gonzalez J, Monnerie H, Le Roux PD, et al. (2010) Inflammation-induced preterm birth alters neuronal morphology in the mouse fetal brain. J Neurosci Res 88: 1872–1881. https://doi.org/10.1002/jnr.22368 PMID: 20155801
2. Burd I, Chai J, Gonzalez J, Ofori E, Monnerie H, Le Roux PD, et al. (2009) Beyond white matter damage: fetal neuronal injury in a mouse model of preterm birth. Am J Obstet Gynecol 201: 279 e271–278.
3. Elovitz MA, Brown AG, Breen K, Anton L, Maubert M, Burd I (2011) Intrauterine inflammation, insufficient to induce parturition, still evokes fetal and neonatal brain injury. International Journal of Developmental Neuroscience 29: 663–671. https://doi.org/10.1016/j.ijdevneu.2011.02.011 PMID: 21382466
4. Elovitz MA, Mrinalini C, Sammel MD (2006) Elucidating the Early Signal Transduction Pathways Leading to Fetal Brain Injury in Preterm Birth. Pediatr Res 59: 50–55. https://doi.org/10.1203/01.pdr.0000191141.21932.b6 PMID: 16327009
5. Meyer U (2014) Prenatal Poly(I:C) Exposure and Other Developmental Immune Activation Models in Rodent Systems. Biological Psychiatry 75: 307–315. https://doi.org/10.1016/j.biopsych.2013.07.011 PMID: 23938317
6. Ashdown H, Dumont Y, Ng M, Poole S, Boksa P, Luheshi GN (2005) The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia. Mol Psychiatry 11: 47–55.
7. Brown AS, Vinogradov S, Kremen WS, Poole JH, Deicken RF, Penner JD, et al. (2009) Prenatal Exposure to Maternal Infection and Executive Dysfunction in Adult Schizophrenia. American Journal of Psychiatry 166: 683–690. https://doi.org/10.1176/appi.ajp.2008.08010089 PMID: 19369317
8. Ellman LM, Yolken RH, Buka SL, Torrey EF, Cannon TD (2009) Cognitive Functioning Prior to the Onset of Psychosis: The Role of Fetal Exposure to Serologically Determined Influenza Infection. Biological Psychiatry 65: 1040–1047. https://doi.org/10.1016/j.biopsych.2008.12.015 PMID: 19195645
9. Fatemi SH, Earle J, Kanodia R, Kist D, Emamian ES, Patterson PH, et al. (2002) Prenatal viral infection leads to pyramidal cell atrophy and macrocephaly in adulthood: implications for genesis of autism and schizophrenia. Cell Mol Neurobiol 22: 25–33. PMID: 12064515
10. Rantakallio P, Jones P, Moring J, Von Wendt L (1997) Association between central nervous system infections during childhood and adult onset schizophrenia and other psychoses: a 28-year follow-up. Int J Epidemiol 26: 837–843. PMID: 9279617
11. Bao AM, Swaab DF (2010) Sex differences in the brain, behavior, and neuropsychiatric disorders. Neu-roscientist 16: 550–565. https://doi.org/10.1177/1073858410377005 PMID: 20889965
12. McCarthy MM (2016) Sex differences in the developing brain as a source of inherent risk. Dialogues Clin Neurosci 18: 361–372. PMID: 28179808
13. Bergeron JDL, Deslauriers J, Grignon S, Fortier LC, Lepage M, Stroh T, et al. (2013) White Matter Injury and Autistic-Like Behavior Predominantly Affecting Male Rat Offspring Exposed to Group B Streptococcal Maternal Inflammation. Developmental Neuroscience 35: 504–515. https://doi.org/10.1159/000355656 PMID: 24246964
14. Dada T, Rosenzweig JM, Al Shammary M, Firdaus W, Al Rebh S, Borbiev T, et al. (2014) Mouse model of intrauterine inflammation: Sex-specific differences in long-term neurologic and immune sequelae. Brain, Behavior, and Immunity 38: 142–150. https://doi.org/10.1016/j.bbi.2014.01.014 PMID: 24486323
15. Ophelders DRMG, Gussenhoven R, Lammens M, Küsters B, Kemp MW, Newnham JP, et al. (2016) Neuroinflammation and structural injury of the fetal ovine brain following intra-amniotic Candida albicans exposure. Journal of Neuroinflammation 13: 29. https://doi.org/10.1186/s12974-016-0492-z PMID: 26842664
16. Fatemi SH, Folsom TD, Liesch SB, Kneeland RE, Karkhane Yousefi M, Thuras PD (2016) The effects of prenatal H1N1 infection at E16 on FMRP, glutamate, GABA, and reelin signaling systems in developing murine cerebellum. Journal of Neuroscience Research: n/a–n/a.
17. Fatemi SH, Folsom TD, Reutiman TJ, Huang H, Oishi K, Mori S (2009) Prenatal viral infection of mice at E16 causes changes in gene expression in hippocampi of the offspring. European Neuropsychophar-macology 19: 648–653. https://doi.org/10.1016/j.euroneuro.2009.03.004 PMID: 19501487
18. Fatemi SH, Reutiman TJ, Folsom TD, Huang H, Oishi K, Mori S, et al. (2008) Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: Implications for genesis of neurodevelopmental disorders. Schizophrenia Research 99: 56–70. https://doi.org/10.1016/j.schres.2007.11.018 PMID: 18248790
19. Zuckerman L, Weiner I (2005) Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. Journal of Psychiatric Research 39: 311–323. https://doi.org/10.1016/j.jpsychires.2004.08.008 PMID: 15725430
20. Sévin DC, Kuehne A, Zamboni N, Sauer U (2015) Biological insights through nontargeted metabolomics. Current Opinion in Biotechnology 34: 1–8. https://doi.org/10.1016/j.copbio.2014.10.001 PMID: 25461505
21. Chun PT, McPherson RJ, Marney LC, Zangeneh SZ, Parsons BA, Shojaie A, et al. (2015) Serial plasma metabolites following hypoxic-ischemic encephalopathy in a nonhuman primate model. Dev Neurosci 37: 161–171. https://doi.org/10.1159/000370147 PMID: 25765047
22. Keller M, Enot DP, Hodson MP, Igwe EI, Deigner HP, Dean J, et al. (2011) Inflammatory-induced hibernation in the fetus: priming of fetal sheep metabolism correlates with developmental brain injury. PLoS One 6: e29503. https://doi.org/10.1371/journal.pone.0029503 PMID: 22242129
23. Yi L, Shi S, Wang Y, Huang W, Xia ZA, Xing Z, et al. (2016) Serum Metabolic Profiling Reveals Altered Metabolic Pathways in Patients with Post-traumatic Cognitive Impairments. Sci Rep 6: 21320. https://doi.org/10.1038/srep21320 PMID: 26883691
24. Burd I, Breen K, Friedman A, Chai J, Elovitz MA (2010) Magnesium sulfate reduces inflammation-associated brain injury in fetal mice. Am J Obstet Gynecol 202: 292 e291–299.
25. Andrikopoulou M, Almalki A, Farzin A, Cordeiro CN, Johnston MV, Burd I (2014) Perinatal biomarkers in prematurity: early identification of neurologic injury. Int J Dev Neurosci 36: 25–31. https://doi.org/10.1016/j.ijdevneu.2014.04.002 PMID: 24768951
26. Graham EM, Burd I, Everett AD, Northington FJ (2016) Blood Biomarkers for Evaluation of Perinatal Encephalopathy. Front Pharmacol 7: 196. https://doi.org/10.3389/fphar.2016.00196 PMID: 27468268
27. Burnstock G, Krugel U, Abbracchio MP, Illes P (2011) Purinergic signalling: from normal behaviour to pathological brain function. Prog Neurobiol 95: 229–274. https://doi.org/10.1016/j.pneurobio.2011.08.006 PMID: 21907261
28. de Azevedo MI, Ferreiro L, Da Silva AS, Tonin AA, Monteiro DU, Casali EA, et al. (2016) Participation of purines in the modulation of inflammatory response in rats experimentally infected by Cryptococcus neoformans. Microb Pathog 99: 36–40. https://doi.org/10.1016/j.micpath.2016.07.015 PMID: 27469575
29. Tonin AA, Da Silva AS, Thome GR, Schirmbeck GH, Cardoso VV, Casali EA, et al. (2014) Changes in purine levels associated with cellular brain injury in gerbils experimentally infected with Neospora cani-num. Res Vet Sci 96: 507–511. https://doi.org/10.1016/j.rvsc.2014.03.004 PMID: 24702899
30. Lin JH, Takano T, Arcuino G, Wang X, Hu F, Darzynkiewicz Z, et al. (2007) Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev Biol 302: 356–366. https://doi.org/10.1016/j.ydbio.2006.09.017 PMID: 17188262
31. Boccazzi M, Rolando C, Abbracchio MP, Buffo A, Ceruti S (2014) Purines regulate adult brain subven-tricular zone cell functions: contribution of reactive astrocytes. Glia 62: 428–439. https://doi.org/10.1002/glia.22614 PMID: 24382645
32. Dachir S, Shabashov D, Trembovler V, Alexandrovich AG, Benowitz LI, Shohami E (2014) Inosine improves functional recovery after experimental traumatic brain injury. Brain Res 1555: 78–88. https://doi.org/10.1016/j.brainres.2014.01.044 PMID: 24502983
33. Shen H, Chen GJ, Harvey BK, Bickford PC, Wang Y (2005) Inosine reduces ischemic brain injury in rats. Stroke 36: 654–659. https://doi.org/10.1161/01.STR.0000155747.15679.04 PMID: 15692110
34. Underwood MA, Gilbert WM, Sherman MP (2005) Amniotic fluid: not just fetal urine anymore. J Perina-tol 25: 341–348. https://doi.org/10.1038/sj.jp.7211290 PMID: 15861199
35. El-Ansary A, Al-Ayadhi L (2014) GABAergic/glutamatergic imbalance relative to excessive neuroinflam-mation in autism spectrum disorders. J Neuroinflammation 11: 189. https://doi.org/10.1186/s12974-014-0189-0 PMID: 25407263
36. Funk CB, Prasad AN, Frosk P, Sauer S, Kolker S, Greenberg CR, et al. (2005) Neuropathological, biochemical and molecular findings in a glutaric acidemia type 1 cohort. Brain 128: 711–722. https://doi.org/10.1093/brain/awh401 PMID: 15689364
37. Harting I, Neumaier-Probst E, Seitz A, Maier EM, Assmann B, Baric I, et al. (2009) Dynamic changes of striatal and extrastriatal abnormalities in glutaric aciduria type I. Brain 132: 1764–1782. https://doi.org/10.1093/brain/awp112 PMID: 19433437
38. Strauss KA, Puffenberger EG, Robinson DL, Morton DH (2003) Type I glutaric aciduria, part 1: natural history of 77 patients. Am J Med Genet C Semin Med Genet 121C: 38–52. https://doi.org/10.1002/ajmg.c.20007 PMID: 12888985
39. Pershing ML, Bortz DM, Pocivavsek A, Fredericks PJ, Jorgensen CV, Vunck SA, et al. (2015) Elevated levels of kynurenic acid during gestation produce neurochemical, morphological, and cognitive deficits in adulthood: implications for schizophrenia. Neuropharmacology 90: 33–41. https://doi.org/10.1016/j.neuropharm.2014.10.017 PMID: 25446576
40. Pershing ML, Phenis D, Valentini V, Pocivavsek A, Lindquist DH, Schwarcz R, et al. (2016) Prenatal kynurenine exposure in rats: age-dependent changes in NMDA receptor expression and conditioned fear responding. Psychopharmacology (Berl) 233: 3725–3735.
41. Larsson MK, Faka A, Bhat M, Imbeault S, Goiny M, Orhan F, et al. (2016) Repeated LPS Injection Induces Distinct Changes in the Kynurenine Pathway in Mice. Neurochem Res 41: 2243–2255. https://doi.org/10.1007/s11064-016-1939-4 PMID: 27165635
42. Schwarcz R, Bruno JP, Muchowski PJ, Wu H-Q (2012) Kynurenines in the mammalian brain: when physiology meets pathology. Nat Rev Neurosci 13: 465–477. https://doi.org/10.1038/nrn3257 PMID: 22678511
43. Burrage LC, Nagamani SC, Campeau PM, Lee BH (2014) Branched-chain amino acid metabolism: from rare Mendelian diseases to more common disorders. Hum Mol Genet 23: R1–8. https://doi.org/10.1093/hmg/ddu123 PMID: 24651065
44. Yudkoff M (2017) Interactions in the Metabolism of Glutamate and the Branched-Chain Amino Acids and Ketoacids in the CNS. Neurochem Res 42: 10–18. https://doi.org/10.1007/s11064-016-2057-z PMID: 27696119
45. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, et al. (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155: 1451–1463. https://doi.org/10.1016/j.cell.2013.11.024 PMID: 24315484
46. Maceyka M, Spiegel S (2014) Sphingolipid metabolites in inflammatory disease. Nature 510: 58–67. https://doi.org/10.1038/nature13475 PMID: 24899305
47. Petrov AM, Kasimov MR, Zefirov AL (2016) Brain Cholesterol Metabolism and Its Defects: Linkage to Neurodegenerative Diseases and Synaptic Dysfunction. Acta Naturae 8: 58–73. PMID: 27099785
48. Jansen M, Wang W, Greco D, Bellenchi GC, di Porzio U, Brown AJ, et al. (2013) What dictates the accumulation of desmosterol in the developing brain? The FASEB Journal 27: 865–870. https://doi.org/10.1096/fj.12-211235 PMID: 23230282
49. Fernandis AZ, Wenk MR (2007) Membrane lipids as signaling molecules. Curr Opin Lipidol 18: 121–128. https://doi.org/10.1097/MOL.0b013e328082e4d5 PMID: 17353659
50. Piomelli D, Astarita G, Rapaka R (2007) A neuroscientist’s guide to lipidomics. Nat Rev Neurosci 8: 743–754. https://doi.org/10.1038/nrn2233 PMID: 17882252
51. Jaeger C, Glaab E, Michelucci A, Binz TM, Koeglsberger S, Garcia P, et al. (2015) The mouse brain metabolome: region-specific signatures and response to excitotoxic neuronal injury. Am J Pathol 185: 1699–1712. https://doi.org/10.1016/j.ajpath.2015.02.016 PMID: 25934215
52. Blaise BJ, Schwendimann L, Chhor V, Degos V, Hodson MP, Dallmann G, et al. (2017) Persistently Altered Metabolic Phenotype following Perinatal Excitotoxic Brain Injury. Dev Neurosci.