Poly(I:C) alters placental and fetal brain amino acid transport in a rat model of maternal immune activation

American Journal of Reproductive Immunology

Volumn 81, Issue 6, 2019, Pages

  McColl, Eliza R ^a   Piquette Miller, Micheline ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

amino acid transporters; amino acids; autism spectrum disorder; inflammation; maternal immune activation; neurodevelopment; placenta; pregnancy; schizophrenia

Indexed keywords

AMINO ACID TRANSPORTER; BRANCHED CHAIN AMINO ACID; EXCITATORY AMINO ACID TRANSPORTER 1; GLYCINE TRANSPORTER 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; POLYINOSINIC POLYCYTIDYLIC ACID; SNAT5 PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; AMINO ACID; IL6 PROTEIN, RAT; IMMUNOLOGIC FACTOR;

AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FETUS BRAIN; FETUS TISSUE; GENE EXPRESSION; GESTATIONAL AGE; HEART ATRIUM SEPTUM DEFECT; IMMUNE RESPONSE; MALE; MATERNAL IMMUNE ACTIVATION; MATERNAL SERUM; MENTAL DISEASE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; WESTERN BLOTTING; ANIMAL; BLOOD; BRAIN; DISEASE MODEL; DRUG EFFECT; GENETICS; METABOLISM; PLACENTA; SPRAGUE DAWLEY RAT;

AMINO ACID TRANSPORT SYSTEMS; AMINO ACIDS; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOLOGIC FACTORS; INTERLEUKIN-6; MALE; PLACENTA; POLY I-C; PREGNANCY; RATS, SPRAGUE-DAWLEY;

EID: 85064508624     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.13115     Document Type: Article

References (70)

1. Solek CM, Farooqi N, Verly M, Lim TK, Ruthazer ES. Maternal immune activation in neurodevelopmental disorders. Dev Dyn. 2018;247(4):588-619.
2. Meyer U, Feldon J, Fatemi SH. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci Biobehav Rev. 2009;33(7):1061-1079.
3. McDonald JW, Johnston MV. Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Rev. 1990;15(1):41-70.
4. Tabatabaie L, Klomp LW, Berger R, de Koning TJ. l-Serine synthesis in the central nervous system: a review on serine deficiency disorders. Mol Genet Metab. 2010;99(3):256-262.
5. Tochitani S. Functions of Maternally-Derived Taurine in Fetal and Neonatal Brain Development. In: Lee D-H, Schaffer SW, Park E, Won Kim H, eds. Taurine 10, 975th ed. Dordrecht, Netherlands: Springer; 2017:17-26.
6. Kurbat MN, Lelevich VV. Metabolism of amino acids in the brain. Neurochem J. 2009;3(1):23-28.
7. Walker N, Filis P, Soffientini U, Bellingham M, O’Shaughnessy PJ, Fowler PA. Placental transporter localization and expression in the Human: the importance of species, sex, and gestational age differences. Biol Reprod. 2017;96(4):733-742.
8. Campos-Bedolla P, Walter FR, Veszelka S, Aria M, Deli A. Role of the blood-brain barrier in the nutrition of the central nervous system. Arch Med Res. 2014;45:610-638.
9. Petrovic V, Piquette-Miller M. Impact of polyinosinic/polycytidylic acid on placental and hepatobiliary drug transporters in pregnant rats. Drug Metab Dispos. 2010;38(10):1760-1766.
10. Petrovic V, Kojovic D, Cressman A, Piquette-Miller M. Maternal bacterial infections impact expression of drug transporters in human placenta. Int Immunopharmacol. 2015;26(2):349-356.
11. Petrovic V, Wang JH, Piquette-Miller M. Effect of endotoxin on the expression of placental drug transporters and glyburide disposition in pregnant rats. Drug Metab Dispos. 2008;36(9):1944-1950.
12. Petrovic V, Piquette-Miller M. Polyinosinic/Polycytidylic Acid-mediated changes in maternal and fetal disposition of lopinavir in rats. Drug Metab Dispos. 2015;43(7):951-957.
13. Bala KA, Dogan M, Mutluer T, et al. Plasma amino acid profile in autism spectrum disorder (ASD). Eur Rev Med Pharmacol Sci. 2016;20:923-929.
14. Saleem S, Shaukat F, Gul A, Arooj M, Malik A. Potential role of amino acids in pathogenesis of schizophrenia. Int J Health Sci (Qassim). 2017;11(3):63-68.
15. Tărlungeanu DC, Deliu E, Dotter CP, et al. Impaired amino acid transport at the blood brain barrier is a cause of autism spectrum disorder. Cell. 2016;167:1481-1494.
16. Smith RE, Haroutunian V, Davis KL, Meador-Woodruff JH. Expression of excitatory amino acid transporter transcripts in the thalamus of subjects with schizophrenia. Am J Psychiatry. 2001;158(9):1393-1399.
17. Careaga M, Murai T, Bauman MD. Maternal immune activation and autism spectrum disorder: from rodents to nonhuman and human primates. Biol Psychiatry. 2017;81:391-401.
18. Meyer U, Feldon J. To poly(I:C) or not to poly(I:C): advancing preclinical schizophrenia research through the use of prenatal immune activation models. Neuropharmacology. 2012;62(3):1308-1321.
19. Reisinger S, Khan D, Kong E, Berger A, Pollak A, Pollak DD. The Poly(I:C)-induced maternal immune activation model in preclinical neuropsychiatric drug discovery. Pharmacol Ther. 2015;149:213-226.
20. Meredith RM. Sensitive and critical periods during neurotypical and aberrant neurodevelopment: a framework for neurodevelopmental disorders. Neurosci Biobehav Rev. 2015;50:180-188.
21. Bronson SL, Ahlbrand R, Horn PS, Kern JR, Richtand NM. Individual differences in maternal response to immune challenge predict offspring behavior: contribution of environmental factors. Behav Brain Res. 2011;220(1):55-64.
22. Wolff AR, Cheyne KR, Bilkey DK. Behavioural deficits associated with maternal immune activation in the rat model of schizophrenia. Behav Brain Res. 2011;225:382-387.
23. Yee N, Ribic A, de Roo CC, Fuchs E. Differential effects of maternal immune activation and juvenile stress on anxiety-like behaviour and physiology in adult rats: no evidence for the “double-hit hypothesis”. Behav Brain Res. 2011;224(1):180-188.
24. Wolff AR, Bilkey DK. Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring. Behav Brain Res. 2008;190(1):156-159.
25. Forrest CM, Khalil OS, Pisar M, Smith RA, Darlington LG, Stone TW. Prenatal activation of Toll-like receptors-3 by administration of the viral mimetic poly(I:C) changes synaptic proteins, N-methyl-D-aspartate receptors and neurogenesis markers in offspring. Mol Brain. 2012;5(1):22.
26. Ohkawara T, Katsuyama T, Ida-Eto M, Narita N, Narita M. Maternal viral infection during pregnancy impairs development of fetal serotonergic neurons. Brain Dev. 2015;37:88-93.
27. Zuckerman L, Rehavi M, Nachman R, Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology. 2003;28(10):1778-1789.
28. Clancy B, Darlington R, Finlay B. Translating developmental time across mammalian species. Neuroscience. 2001;105(1):7-17.
29. Carter AM. Evolution of placental function in mammals: the molecular basis of gas and nutrient transfer, hormone secretion, and immune responses. Physiol Rev. 2012;92:1543-1576.
30. Cleal JK, Lewis RM. The mechanisms and regulation of placental amino acid transport to the human foetus. J Neuroendocrinol. 2008;20:419-426.
31. McCracken AN, Edinger AL. Nutrient transporters: the Achilles’ heel of anabolism. Trends Endocrinol Metab. 2013;24(4):200-208.
32. Jones HN, Jansson T, Powell TL. IL-6 stimulates system A amino acid transporter activity in trophoblast cells through STAT3 and increased expression of SNAT2. Am J Physiol Physiol. 2009;297(5):C1228-C1235.
33. Liong S, Lappas M. Lipopolysaccharide and double stranded viral RNA mediate insulin resistance and increase system a amino acid transport in human trophoblast cells in vitro. Placenta. 2017;51:18-27.
34. Noorlander CW, De Graan P, Nikkels P, Schrama LH, Visser G. Distribution of glutamate transporters in the human placenta. Placenta. 2004;25:489-495.
35. Novak D, Quiggle F, Artime C, Beveridge M. Regulation of glutamate transport and transport proteins in a placental cell line. Am J Physiol Cell Physiol. 2001;281:C1014-C1022.
36. Jansson T. Amino acid transporters in the human placenta. Pediatr Res. 2001;49(2):141-147.
37. Pötgens A, Drewlo S, Kokozidou M, Kaufmann P. Syncytin: the major regulator of trophoblast fusion? Recent developments and hypotheses on its action. Hum Reprod Update. 2004;10(6):487-496.
38. Desforges M, Parsons L, Westwood M, Sibley CP, Greenwood SL. Taurine transport in human placental trophoblast is important for regulation of cell differentiation and survival. Cell Death Dis. 2013;4(3):e559.
39. Nishimura T, Sai Y, Fujii J, et al. Roles of TauT and system A in cytoprotection of rat syncytiotrophoblast cell line exposed to hypertonic stress. Placenta. 2010;31(11):1003-1009.
40. Vaughan OR, Rosario FJ, Powell TL, Jansson T. Regulation of placental amino acid transport and fetal growth. Prog Mol Biol Transl Sci. 2017;145:217-251.
41. Marcaggi P, Attwell D. Role of glial amino acid transporters in synaptic transmission and brain energetics. Glia. 2004;47:217-225.
42. Parkin GM, Udawela M, Gibbons A, Dean B. Glutamate transporters, EAAT1 and EAAT2, are potentially important in the pathophysiology and treatment of schizophrenia and affective disorders. World J psychiatry. 2018;8(2):51-63.
43. DiCicco-Bloom E, Lord C, Zwaigenbaum L, et al. The developmental neurobiology of autism spectrum disorder. J Neurosci. 2006;26(26):6897-6906.
44. Moghaddam B, Javitt D. From revolution to evolution: the glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacol Rev. 2011;37:4-15.
45. Cubelos B, González-González IM, Giménez C, Zafra F. Amino acid transporter SNAT5 localizes to glial cells in the rat brain. Glia. 2005;49(2):230-244.
46. Eulenburg V, Retiounskaia M, Papadopoulos T, Gomeza J, Betz H. Glial glycine transporter 1 function is essential for early postnatal survival but dispensable in adult mice. Glia. 2010;58(9):1066-1073.
47. Brown AG, Tulina NM, Barila GO, Hester MS, Elovitz MA. Exposure to intrauterine inflammation alters metabolomic profiles in the amniotic fluid, fetal and neonatal brain in the mouse. PLoS ONE. 2017;12(10):e0186656.
48. Park E, Cohen I, Gonzalez M, et al. Is Taurine a Biomarker in Autistic Spectrum Disorder? In: Lee D-H, Schaffer SW, Park E, Won Kim H, eds. Taurine 10, 975th ed. Dordrecht, Netherlands: Springer; 2017:3-16.
49. Cetin FH, Tunca H, Güney E, Iseri E. Neurotransmitter Systems in Autism Spectrum Disorder. In: Fitzgerald M, ed. Autism Spectrum Disorder - Recent Advances. London, UK: InTech; 2015:15-30.
50. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 2005;6(4):312-324.
51. Sperringer JE, Addington A, Hutson SM. Branched-chain amino acids and brain metabolism. Neurochem Res. 2017;42:1697-1709.
52. Tărlungeanu DC, Deliu E, Dotter CP, et al. Impaired amino acid transport at the blood brain barrier is a cause of autism spectrum disorder HHS Public Access. Cell. 2016;167(6):1481-1494.
53. Novarino G, El-Fishawy P, Kayserili H, et al. Mutations in BCKD-kinase lead to a potentially treatable form of autism with epilepsy. Science. 2012;338(6105):394-397.
54. Fortier M-E, Kent S, Ashdown H, Poole S, Boksa P, Luheshi GN. The viral mimic, polyinosinic:polycytidylic acid, induces fever in rats via an interleukin-1-dependent mechanism. Am J Physiol Integr Comp Physiol. 2004;287(4):R759-R766.
55. Cole JT. Metabolism of BCAAs. In: Rajendram R, Preedy VR, Patel VB, eds. Branched Chain Amino Acids in Clinical Nutrition. Vol 1. New York, NY: Springer Science+Business Media; 2015:13-25.
56. Kanehisa Laboratories. KEGG PATHWAY: Cysteine and methionine metabolism - Homo sapiens (human). https://www.genome.jp/kegg-bin/show_pathway?org_name=hsa&mapno=00270&mapscale=&show_description=hide. Published 2018. Accessed October 23, 2018.
57. Ofner M, Coles A, Decou ML, et al.Autism Spectrum Disorder Among Children and Youth in Canada 2018: A Report of the National Autism Spectrum Disorder Surveillance System. Ottawa; 2018. https://www.canada.ca/content/dam/phac-aspc/documents/services/publications/diseases-conditions/autism-spectrum-disorder-children-youth-canada-2018/autism-spectrum-disorder-children-youth-canada-2018.pdf. Accessed April 3, 2018.
58. Abel KM, Drake R, Goldstein JM. Sex differences in schizophrenia. Int Rev Psychiatry. 2010;22(5):417-428.
59. Hsiao EY, Patterson PH. Activation of the maternal immune system induces endocrine changes in the placenta via IL-6. Brain Behav Immun. 2011;25:604-615.
60. Koga K, Cardenas I, Aldo P, et al. Activation of TLR3 in the trophoblast is associated with preterm delivery. Am J Reprod Immunol. 2009;61(3):196-212.
61. Wu W-L, Hsiao EY, Yan Z, Mazmanian SK, Patterson PH. The placental interleukin-6 signaling controls fetal brain development and behavior. Brain Behav Immun. 2017;62:11-23.
62. Dahlgren J, Samuelsson A-M, Jansson T, Holmäng A. Interleukin-6 in the maternal circulation reaches the rat fetus in mid-gestation. Pediatr Res. 2006;60(2):147-151.
63. Fischer CP, Bode BP, Takahashi K, Tanabe KK, Souba WW. Glucocorticoid-dependent induction of interleukin-6 receptor expression in human hepatocytes facilitates interleukin-6 stimulation of amino acid transport. Ann Surg. 1996;223(5):610-618.
64. Parker-Athill CE, Tan J. Maternal immune activation and autism spectrum disorder: interleukin-6 signaling as a key mechanistic pathway. Neurosignals. 2010;18:113-128.
65. Abualsunun WA, Piquette-Miller M. Involvement of nuclear factor κB, not pregnane X receptor, in inflammation-mediated regulation of hepatic transporters. Drug Metab Dispos. 2017;45(10):1077-1083.
66. Smith S, Li J, Garbett K, Mirnics K, Patterson PH. Maternal immune activation alters fetal brain development through interleukin-6. Neurobiol Dis. 2007;27(40):10695-10702.
67. Simmons WW, Closs EI, Cunningham JM, Smith TW, Kelly RA. Cytokines and insulin induce Cationic Amino Acid Transporter (CAT) expression in cardiac myocytes. J Biol Chem. 1996;271(20):11694-11702.
68. Abbott NJ, Patabendige A, Dolman D, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2009;37:13-25.
69. Jansson T. Reviews of placental amino acid transport and metabolism. Pediatr Res. 2001;49(2):141-147.
70. Kohlmeier M. Amino Acids and Nitrogen Compounds. In: Nutrient Metabolism. San Diego, CA: Elsevier; 2015;265-477.