Antipurinergic Therapy Corrects the Autism-Like Features in the Poly(IC) Mouse Model

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Naviaux, Robert K ^a,b,c,d   Zolkipli, Zarazuela ^a,e   Wang, Lin ^a,b   Nakayama, Tomohiro ^a,e   Naviaux, Jane C ^a,f   Le, Thuy P ^a,c   Schuchbauer, Michael A ^f   Rogac, Mihael ^a,b,g   Tang, Qingbo ^b   Dugan, Laura L ^b   Powell, Susan B ^f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

BUNGAROTOXIN RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CORTICOSTERONE; IMMUNOGLOBULIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; SURAMIN;

AEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTISM; CELL LOSS; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; FEMALE; HYPOTHERMIA; IMMUNOGLOBULIN BLOOD LEVEL; MALE; MITOCHONDRIAL RESPIRATION; MOTOR COORDINATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PURKINJE CELL; RESPIRATORY CHAIN; SENSORIMOTOR INTEGRATION; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR;

ANIMALS; AUTISTIC DISORDER; BEHAVIOR, ANIMAL; BRAIN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CORTICOSTERONE; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT; ENERGY METABOLISM; FEMALE; FRAGILE X MENTAL RETARDATION PROTEIN; HYPOTHERMIA; IMMUNOGLOBULINS; MALE; MICE; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; POLY I-C; PSYCHOMOTOR PERFORMANCE; PURKINJE CELLS; RECEPTORS, NICOTINIC; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SURAMIN; SYNAPTOSOMES;

EID: 84874854729     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057380     Document Type: Article

References (61)

1. Kou Y, Betancur C, Xu H, Buxbaum JD, Ma'ayan A, (2012) Network- and attribute-based classifiers can prioritize genes and pathways for autism spectrum disorders and intellectual disability. Am J Med Genet C Semin Med Genet 160C: 130-142.
2. Kohane IS, McMurry A, Weber G, Macfadden D, Rappaport L, et al. (2012) The co-morbidity burden of children and young adults with autism spectrum disorders. PLoS One 7: e33224.
3. Buie T, Fuchs GJ III, Furuta GT, Kooros K, Levy J, et al. (2010) Recommendations for evaluation and treatment of common gastrointestinal problems in children with ASDs. Pediatrics 125 Suppl 1: S19-29.
4. Mulder EJ, Anderson GM, Kema IP, de Bildt A, van Lang ND, et al. (2004) Platelet serotonin levels in pervasive developmental disorders and mental retardation: diagnostic group differences, within-group distribution, and behavioral correlates. J Am Acad Child Adolesc Psychiatry 43: 491-499.
5. Palmieri L, Papaleo V, Porcelli V, Scarcia P, Gaita L, et al. (2010) Altered calcium homeostasis in autism-spectrum disorders: evidence from biochemical and genetic studies of the mitochondrial aspartate/glutamate carrier AGC1. Mol Psychiatry 15: 38-52.
6. Heuer L, Ashwood P, Schauer J, Goines P, Krakowiak P, et al. (2008) Reduced levels of immunoglobulin in children with autism correlates with behavioral symptoms. Autism Res 1: 275-283.
7. Page T, Coleman M, (2000) Purine metabolism abnormalities in a hyperuricosuric subclass of autism. Biochim Biophys Acta 1500: 291-296.
8. James SJ, Melnyk S, Jernigan S, Hubanks A, Rose S, et al. (2008) Abnormal transmethylation/transsulfuration metabolism and DNA hypomethylation among parents of children with autism. J Autism Dev Disord 38: 1966-1975.
9. Waring RH, Klovrza LV, (2000) Sulphur metabolism in autism. Journal of Nutritional and Environmental Medicine (Abingdon) 10: 25-32.
10. James SJ, Melnyk S, Jernigan S, Hubanks A, Rose S, et al. (2008) Abnormal Transmethylation/transsulfuration Metabolism and DNA Hypomethylation Among Parents of Children with Autism. J Autism Dev Disord 38: 1976.
11. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA, (2005) Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 57: 67-81.
12. Courchesne E, Saitoh O, Yeung-Courchesne R, Press GA, Lincoln AJ, et al. (1994) Abnormality of cerebellar vermian lobules VI and VII in patients with infantile autism: identification of hypoplastic and hyperplastic subgroups with MR imaging. AJR Am J Roentgenol 162: 123-130.
13. Bailey A, Luthert P, Dean A, Harding B, Janota I, et al. (1998) A clinicopathological study of autism. Brain 121 (Pt 5) (): 889-905.
14. Jaeschke H, McGill MR, Ramachandran A, (2012) Oxidant stress, mitochondria, and cell death mechanisms in drug-induced liver injury: lessons learned from acetaminophen hepatotoxicity. Drug Metab Rev 44: 88-106.
15. West AP, Shadel GS, Ghosh S, (2011) Mitochondria in innate immune responses. Nat Rev Immunol 11: 389-402.
16. Zhou R, Yazdi AS, Menu P, Tschopp J, (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469: 221-225.
17. Tal MC, Iwasaki A, (2011) Mitoxosome: a mitochondrial platform for cross-talk between cellular stress and antiviral signaling. Immunol Rev 243: 215-234.
18. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H, (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32: 19-29.
19. Junger WG, (2011) Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 11: 201-212.
20. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, et al. (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464: 104-107.
21. Harada K, Hide I, Seki T, Tanaka S, Nakata Y, et al. (2011) Extracellular ATP differentially modulates Toll-like receptor 4-mediated cell survival and death of microglia. J Neurochem 116: 1138-1147.
22. Franke H, Sauer C, Rudolph C, Krugel U, Hengstler JG, et al. (2009) P2 receptor-mediated stimulation of the PI3-K/Akt-pathway in vivo. Glia 57: 1031-1045.
23. Pelegrin P, (2008) Targeting interleukin-1 signaling in chronic inflammation: focus on P2X(7) receptor and Pannexin-1. Drug News Perspect 21: 424-433.
24. Gallego D, Vanden Berghe P, Farre R, Tack J, Jimenez M, (2008) P2Y1 receptors mediate inhibitory neuromuscular transmission and enteric neuronal activation in small intestine. Neurogastroenterol Motil 20: 159-168.
25. Matos JE, Sorensen MV, Geyti CS, Robaye B, Boeynaems JM, et al. (2007) Distal colonic Na(+) absorption inhibited by luminal P2Y(2) receptors. Pflugers Arch 454: 977-987.
26. Surprenant A, North RA, (2009) Signaling at purinergic P2X receptors. Annu Rev Physiol 71: 333-359.
27. Leng Y, Yamamoto T, Kadowaki M, (2008) Alteration of cholinergic, purinergic and sensory neurotransmission in the mouse colon of food allergy model. Neurosci Lett 445: 195-198.
28. Housley GD, Jagger DJ, Greenwood D, Raybould NP, Salih SG, et al. (2002) Purinergic regulation of sound transduction and auditory neurotransmission. Audiol Neurootol 7: 55-61.
29. Speciale A, Chirafisi J, Saija A, Cimino F, (2011) Nutritional antioxidants and adaptive cell responses: an update. Curr Mol Med 11: 770-789.
30. Patterson PH, (2011) Modeling autistic features in animals. Pediatr Res 69: 34R-40R.
31. Bitanihirwe BK, Peleg-Raibstein D, Mouttet F, Feldon J, Meyer U, (2010) Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Neuropsychopharmacology 35: 2462-2478.
32. Traynor TR, Majde JA, Bohnet SG, Krueger JM, (2004) Intratracheal double-stranded RNA plus interferon-gamma: a model for analysis of the acute phase response to respiratory viral infections. Life Sci 74: 2563-2576.
33. Light AR, Wu Y, Hughen RW, Guthrie PB, (2006) Purinergic receptors activating rapid intracellular Ca increases in microglia. Neuron Glia Biol 2: 125-138.
34. Dunn PM, Blakeley AG, (1988) Suramin: a reversible P2-purinoceptor antagonist in the mouse vas deferens. Br J Pharmacol 93: 243-245.
35. Adriaan Bouwknecht J, Olivier B, Paylor RE, (2007) The stress-induced hyperthermia paradigm as a physiological animal model for anxiety: a review of pharmacological and genetic studies in the mouse. Neurosci Biobehav Rev 31: 41-59.
36. Moy SS, Nadler JJ, Young NB, Nonneman RJ, Segall SK, et al. (2008) Social approach and repetitive behavior in eleven inbred mouse strains. Behav Brain Res 191: 118-129.
37. Pallier PN, Drew CJ, Morton AJ, (2009) The detection and measurement of locomotor deficits in a transgenic mouse model of Huntington's disease are task- and protocol-dependent: influence of non-motor factors on locomotor function. Brain Res Bull 78: 347-355.
38. Hatefi Y, (1978) Reconstitution of the electron-transport system of bovine heart mitochondria. Methods Enzymol 53: 48-54.
39. Barrientos A, (2002) In vivo and in organello assessment of OXPHOS activities. Methods 26: 307-316.
40. Stumpf DA, Parks JK, (1981) Human mitochondrial electron transport chain: assay of succinate: cytochrome c reductase in leukocytes, platelets and cultured fibroblasts. Biochem Med 25: 234-238.
41. Wharton DC, Tzagoloff A, (1967) Cytochrome oxidase from beef heart. Methods Enzymol 10: 245-250.
42. Shepherd D, Garland PB, (1969) Citrate synthase from rat liver. Methods in Enzymology 13: 11-16.
43. Kobayashi K, Weiss RE, Vogelzang NJ, Vokes EE, Janisch L, et al. (1996) Mineralocorticoid insufficiency due to suramin therapy. Cancer 78: 2411-2420.
44. Frenzel M, Rommelspacher H, Sugawa MD, Dencher NA, (2010) Ageing alters the supramolecular architecture of OxPhos complexes in rat brain cortex. Exp Gerontol 45: 563-572.
45. Korjamo T, Heikkinen AT, Monkkonen J, (2009) Analysis of unstirred water layer in in vitro permeability experiments. J Pharm Sci 98: 4469-4479.
46. Leon D, Hervas C, Miras-Portugal MT, (2006) P2Y1 and P2X7 receptors induce calcium/calmodulin-dependent protein kinase II phosphorylation in cerebellar granule neurons. Eur J Neurosci 23: 2999-3013.
47. Khera TK, Dick AD, Nicholson LB, (2010) Fragile X-related protein FXR1 controls post-transcriptional suppression of lipopolysaccharide-induced tumour necrosis factor-alpha production by transforming growth factor-beta1. FEBS J 277: 2754-2765.
48. Tracey KJ, (2009) Reflex control of immunity. Nat Rev Immunol 9: 418-428.
49. Jones CK, Byun N, Bubser M, (2012) Muscarinic and nicotinic acetylcholine receptor agonists and allosteric modulators for the treatment of schizophrenia. Neuropsychopharmacology 37: 16-42.
50. Hashimoto T, Tayama M, Murakawa K, Yoshimoto T, Miyazaki M, et al. (1995) Development of the brainstem and cerebellum in autistic patients. J Autism Dev Disord 25: 1-18.
51. Naviaux RK, Nyhan WL, Barshop BA, Poulton J, Markusic D, et al. (1999) Mitochondrial DNA polymerase gamma deficiency and mtDNA depletion in a child with Alpers' syndrome. Ann Neurol 45: 54-58.
52. Greco CM, Navarro CS, Hunsaker MR, Maezawa I, Shuler JF, et al. (2011) Neuropathologic features in the hippocampus and cerebellum of three older men with fragile X syndrome. Mol Autism 2: 2.
53. Shi L, Smith SE, Malkova N, Tse D, Su Y, et al. (2009) Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav Immun 23: 116-123.
54. Zerbo O, Iosif AM, Walker C, Ozonoff S, Hansen RL, et al. (2012) Is Maternal Influenza or Fever During Pregnancy Associated with Autism or Developmental Delays? Results from the CHARGE (CHildhood Autism Risks from Genetics and Environment) Study. J Autism Dev Disord.
55. Yang D, Kim KH, Phimister A, Bachstetter AD, Ward TR, et al. (2009) Developmental exposure to polychlorinated biphenyls interferes with experience-dependent dendritic plasticity and ryanodine receptor expression in weanling rats. Environ Health Perspect 117: 426-435.
56. Bouma HR, Verhaag EM, Otis JP, Heldmaier G, Swoap SJ, et al. (2012) Induction of torpor: mimicking natural metabolic suppression for biomedical applications. J Cell Physiol 227: 1285-1290.
57. Pesta D, Hoppel F, Macek C, Messner H, Faulhaber M, et al. (2011) Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans. Am J Physiol Regul Integr Comp Physiol 301: R1078-1087.
58. Tulapurkar ME, Schafer R, Hanck T, Flores RV, Weisman GA, et al. (2005) Endocytosis mechanism of P2Y2 nucleotide receptor tagged with green fluorescent protein: clathrin and actin cytoskeleton dependence. Cell Mol Life Sci 62: 1388-1399.
59. Rosas-Ballina M, Olofsson PS, Ochani M, Valdes-Ferrer SI, Levine YA, et al. (2011) Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 334: 98-101.
60. Galassetti PR, Novak B, Nemet D, Rose-Gottron C, Cooper DM, et al. (2005) Breath ethanol and acetone as indicators of serum glucose levels: an initial report. Diabetes Technol Ther 7: 115-123.
61. Voogd TE, Vansterkenburg EL, Wilting J, Janssen LH, (1993) Recent research on the biological activity of suramin. Pharmacol Rev 45: 177-203.