Ketogenic diet improves behaviors in a maternal immune activation model of autism spectrum disorder

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Ruskin, David N ^a   Murphy, Michelle I ^a   Slade, Sierra L ^a   Masino, Susan A ^a  

^a TRINITY COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; KETONE; POLYINOSINIC POLYCYTIDYLIC ACID; BIOLOGICAL MARKER; GLUCOSE BLOOD LEVEL; KETONE BODY;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; BEHAVIOR; BLOOD ANALYSIS; C57BL 6 MOUSE; COMPULSION; CONTROLLED STUDY; FEMALE; GLUCOSE BLOOD LEVEL; IMMUNITY; INTERPERSONAL COMMUNICATION; KETOGENIC DIET; MALE; MATERNAL IMMUNE ACTIVATION; MOUSE; NONHUMAN; PHENOTYPE; PROGENY; SOCIAL BEHAVIOR; WEANING; YOUNG ADULT; ANIMAL; ANIMAL BEHAVIOR; AUTISM SPECTRUM DISORDER; BLOOD; DISEASE MODEL; IMMUNOLOGY; MATERNAL EXPOSURE; METABOLISM; PREGNANCY; PRENATAL EXPOSURE; PSYCHOLOGY;

ANIMALS; AUTISM SPECTRUM DISORDER; BEHAVIOR, ANIMAL; BIOMARKERS; BLOOD GLUCOSE; DISEASE MODELS, ANIMAL; FEMALE; KETOGENIC DIET; KETONE BODIES; MALE; MATERNAL EXPOSURE; MICE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 85011632713     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0171643     Document Type: Article

References (60)

1. Masino SA, Fortin JA, Murphy MI, Saa L, Ruskin DN. Autism Spectrum Disorder and Homeostasis. In: Boison D, Masino SA, editors. Homeostatic Control of Brain Function. New York: Oxford University Press; 2015. p. 586-609.
2. Patterson PH. Maternal infection: window on neuroimmune interactions in fetal brain development and mental illness. Curr Opin Neurobiol. 2002; 12:115-8. PMID: 11861174
3. Atladóttir HÓ, Thorsen P, Ostergaard L, Schendel DE, Lemcke S, Abdallah M, et al. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2010; 40:1423-30. doi: 10.1007/s10803-010-1006-y PMID: 20414802
4. Atladóttir HÓ, Henriksen TB, Schendel DE, Parner ET. Autism after infection, febrile episodes, and antibiotic use during pregnancy: an exploratory study. Pediatrics. 2012; 130:e1447. doi: 10.1542/peds. 2012-1107 PMID: 23147969
5. Lee BK, Magnusson C, Gardner RM, Blomstrom S, Newschaffer CJ, Burstyn I, et al. Maternal hospitalization with infection during pregnancy and risk of autism spectrum disorders. Brain Behav Immun. 2015; 44:100-5. doi: 10.1016/j.bbi.2014.09.001 PMID: 25218900
6. Zerbo O, Qian Y, Toshida C, Grether JK, Van Der Water J, Croen LA. Maternal infection during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2015; 45:4015-25. doi: 10.1007/s10803-013-2016-3 PMID: 24366406
7. Patterson PH. Maternal infection and immune involvement in autism. Trends Mol Med. 2011; 17:389-94. doi: 10.1016/j.molmed.2011.03.001 PMID: 21482187
8. Smith SEP, Li J, Garbett K, Mirnics K, Patterson PH. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci. 2007; 27:10695-702. doi: 10.1523/JNEUROSCI.2178-07.2007 PMID: 17913903
9. Malkova NV, Yu CZ, Hsiao EY, Moore MJ, Patterson PH. Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun. 2012; 26:607-16. doi: 10.1016/j.bbi.2012.01.011 PMID: 22310922
10. Frye RE, Sreenivasula S, Adams JB. Traditional and non-traditional treatments for autism spectrum disorder with seizures: an on-line survey. BMC Pediatr. 2011; 11:37. doi: 10.1186/1471-2431-11-37 PMID: 21592359
11. Jurecka A, Zikanova M, Jurkiewicz E, Tylki-Szymañska A. Attenuated adenylosuccinate lyase deficiency: a report of one case and a review of the literature. Neuropediatrics. 2014; 45:50-5. doi: 10. 1055/s-0033-1337335 PMID: 23504561
12. Dupuis N, Curatolo N, Benoist J-F, Stephane Auvin S. Ketogenic diet exhibits anti-inflammatory properties. Epilepsia. 2015; 56:e95-e8. doi: 10.1111/epi.13038 PMID: 26011473
13. Nandivada P, Fell GL, Pan AH, Nose V, Ling P-R, Bistrian BR, et al. Eucaloric ketogenic diet reduces hypoglycemia and inflammation in mice with endotoxemia. Lipids. 2016; 51:703-14. doi: 10.1007/ s11745-016-4156-7 PMID: 27117864
14. Spilioti M, Pavlou E, Gogou M, Katsanika I, Papadopoulou-Alataki E, Grafakou O, et al. Valproate effect on ketosis in children under ketogenic diet. Eur J Paediatr Neurol. 2016; 20:555-9. doi: 10.1016/j.ejpn. 2016.04.003 PMID: 27117552
15. Jiang Y, Yang Y, Wang S, Ding Y, Guo Y, Zhang M-M, et al. Ketogenic diet protects against epileptogenesis as well as neuronal loss in amygdaloid-kindling seizures. Neurosci Lett. 2012; 508:22-6. doi: 10.1016/j.neulet.2011.12.002 PMID: 22178860
16. Lusardi TA, Akula KK, Coffman SQ, Ruskin DN, Masino SA, Boison D. Ketogenic diet prevents epileptogenesis and disease progression in adult mice and rats. Neuropharmacology. 2015; 99:500-9. doi: 10.1016/j.neuropharm.2015.08.007 PMID: 26256422
17. Chen JY, Tran C, Hwang L, Deng G, Jung ME, Faull KF, et al. Partial amelioration of peripheral and central symptoms of Huntington's disease via modulation of lipid metabolism. J Huntingtons Dis. 2016; 5:65-81. doi: 10.3233/JHD-150181 PMID: 27031732
18. Castro K, Faccioli LS, Baronio D, Gottfried C, Perry IS, Riesgo RdS. Effect of a ketogenic diet on autism spectrum disorder: A systematic review. Res Autism Spectr Dis. 2015; 20:31-8.
19. Arvio M, Kuisma L, Pöntinen M. [The modified Atkins diet brought back the joy of life to a developmentally severely disabled youth.] Duodecim. 2010; 126:557-60. PMID: 20597309
20. Herbert MR, Buckley JA. Autism and dietary therapy: case report and review of the literature. J Child Neurol. 2013; 28:975-82. doi: 10.1177/0883073813488668 PMID: 23666039
21. Evangeliou A, Vlachonikolis I, Mihailidou H, Spilioti M, Skarpalezou A, Makaronas N, et al. Application of a ketogenic diet in children with autistic behavior: pilot study. J Child Neurol. 2003; 18:113-8. PMID: 12693778
22. Masino SA, Svedova J, Kawamura M Jr., DiMario FD Jr., et al. Adenosine and Autism-Recent Research and a New Perspective. In: Eapen V, editor. Autism-A Neurodevelopmental Journey from Genes to Behaviour. Rijeka, Croatia: InTech; 2011. p. 103-22.
23. Spilioti M, Evangeliou AE, Tramma D, Theodoridou Z, Metaxas S, Michailidi E, et al. Evidence for treatable inborn errors of metabolism in a cohort of 187 Greek patients with autism spectrum disorder (ASD). Front Hum Neurosci. 2013; 7:858. doi: 10.3389/fnhum.2013.00858 PMID: 24399946
24. Ruskin DN, Svedova J, Cote JL, Sandau U, Rho JM, Kawamura M Jr, et al. Ketogenic diet improves core symptoms of autism in BTBR mice. PLOS ONE. 2013; 8:e65021. doi: 10.1371/journal.pone. 0065021 PMID: 23755170
25. Ruskin DN, Fortin JA, Bisnauth S, Masino SA. Ketogenic diets improve behaviors associated with autism spectrum disorder in a sex-specific manner in the EL mouse. Physiol Behav. 2017; 168:138-45. doi: 10.1016/j.physbeh.2016.10.023 PMID: 27836684
26. Verpeut JL, DiCicco-Bloom E, Bello NT. Ketogenic diet exposure during the juvenile period increases social behaviors and forebrain neural activation in adult Engrailed 2 null mice. Physiol Behav. 2016; 161:90-8. doi: 10.1016/j.physbeh.2016.04.001 PMID: 27080080
27. Ahn Y, Narous M, Tobias R, Rho JM, Mychasiuk R. The ketogenic diet modifies social and metabolic alterations identified in the prenatal valproic acid model of autism spectrum disorder. Dev Neurosci. 2014; 36:371-80. doi: 10.1159/000362645 PMID: 25011527
28. Castro K, Baronio D, Perry IS, Riesgo RdS, Gottfried C. The effect of ketogenic diet in an animal model of autism induced by prenatal exposure to valproic acid. Nutr Neurosci. 2016;in press.
29. Byers SL, Wiles MV, Dunn SL, Taft RA. Mouse estrous cycle identification tool and images. PLOS ONE. 2012; 7:e35538. doi: 10.1371/journal.pone.0035538 PMID: 22514749
30. Napoli E, Dueñas N, Giulivi C. Potential therapeutic use of the ketogenic diet in autism spectrum disorders. Front Pediatr. 2014; 2:69. doi: 10.3389/fped.2014.00069 PMID: 25072037
31. Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, Magnuson TR, et al. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 2004; 3:287-302. doi: 10.1111/j.1601-1848.2004.00076.x PMID: 15344922
32. Galef BG Jr., Wigmore SW. Transfer of information concerning distant foods: a laboratory investigation of the 'information-centre' hypothesis. Anim Behav. 1983; 31:748-58.
33. Centers for Disease Control and Prevention. Prevalence of autism spectrum disorder among children aged 8 years-autism and developmental disabilities monitoring network, 11 sites, United States, 2010. MMWR Surveill Summ. 2014; 63(SS02):1-21.
34. Xuan ICY, Hampson DR. Gender-dependent effects of maternal immune activation on the behavior of mouse offspring. PLOS ONE. 2014; 9:e104433. doi: 10.1371/journal.pone.0104433 PMID: 25111339
35. Mueller BR, Bale TL. Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol Behav. 2007; 93:55-65.
36. Grindstaff JL, Hunsaker VR, Cox SN. rnal and developmental immune challenges alter behavior and learning ability of offspring. Horm Behav. 2012; 62:337-44. doi: 10.1016/j.yhbeh.2012.04.005 PMID: 22522078
37. Todorova MT, Tandon P, Madore RA, Stafstrom CE, Seyfried TN. The ketogenic diet inhibits epileptogenesis in EL mice: a genetic model for idiopathic epilepsy. Epilepsia. 2000; 41:933-40. PMID: 10961617
38. Haas RH, Rice MA, Tauner DA, Merritt TA. Therapeutic effects of a ketogenic diet in Rett syndrome. Am J Med Genet Suppl. 1986; 1:225-46. PMID: 3087185
39. Liebhaber GM, Riemann E, Baumeister FA. Ketogenic diet in Rett syndrome. J Child Neurol. 2003; 18:74-5. PMID: 12661945
40. Zilkha N, Kuperman Y, Kimchi T. High-fat diet exacerbates cognitive rigidity and social deficiency in the BTBR mouse model of autism. Neuroscience. in press.
41. Ruskin DN, Suter TACS, Ross JL, Masino SA. Ketogenic diets and thermal pain: dissociation of hypoalgesia, elevated ketones, and lowered glucose in rats. J Pain. 2013; 14:467-74. doi: 10.1016/j.jpain. 2012.12.015 PMID: 23499319
42. Gano LB, Patel M, Rho JM. Ketogenic diets, mitochondria, and neurological diseases. J Lipid Res. 2014; 55:2211-28. doi: 10.1194/jlr.R048975 PMID: 24847102
43. Ruskin DN, Masino SA. The nervous system and metabolic dysregulation: emerging evidence converges on ketogenic diet therapy. Front Neurosci. 2012; 6:33. doi: 10.3389/fnins.2012.00033 PMID: 22470316
44. Masino SA, Kawamura M Jr., Wasser CD, Pomeroy LT, Ruskin DN. Adenosine, ketogenic diet and epilepsy: the emerging therapeutic relationship between metabolism and brain activity. Curr Neuropharmacol. 2009; 7:257-68. doi: 10.2174/157015909789152164 PMID: 20190967
45. Masino SA, Kawamura M Jr., Plotkin LM, Svedova J, DiMario FJ, et al. The relationship between the neuromodulator adenosine and behavioral symptoms of autism. Neurosci Lett. 2011; 500:1-5. doi: 10. 1016/j.neulet.2011.06.007 PMID: 21693172
46. Masino SA, Kawamura M Jr., Cote JL, Williams RB, Ruskin DN. Adenosine and autism: a spectrum of opportunities. Neuropharmacology. 2013; 68:116-21. doi: 10.1016/j.neuropharm.2012.08.013 PMID: 22940000
47. Kawamura M Jr, Ruskin DN, Masino SA. Metabolic autocrine regulation of neurons involves cooperation among pannexin hemichannels, adenosine receptors and KATP channels. J Neurosci. 2010; 30:3886-95. doi: 10.1523/JNEUROSCI.0055-10.2010 PMID: 20237259
48. Masino SA, Li T, Theofilas P, Sandau U, Ruskin DN, Fredholm BB, et al. A ketogenic diet suppresses seizures in mice through adenosine A1 receptors. J Clin Invest. 2011; 121:2679-83. doi: 10.1172/ JCI57813 PMID: 21701065
49. Kawamura M Jr, Ruskin DN, Geiger JD, Boison D, Masino SA. Ketogenic diet sensitizes glucose control of hippocampal excitability. J Lipid Res. 2014; 55:2254-60. doi: 10.1194/jlr.M046755 PMID: 25170119
50. Coleman M, Landgrebe MA, Landgrebe AR. Purine autism. Hyperuricosuria in autistic children: does this identify a subgroup of autism? In: Coleman M, editor. The Autistic Syndromes. New York: Elsevier;1976. p. 183-214.
51. Marie S, Race V, Nassogne MC, Vincent MF, Van den Berghe G. Mutation of a nuclear respiratory factor 2 binding site in the 5' untranslated region of the ADSL gene in three patients with adenylosuccinate lyase deficiency. Amer J Hum Genet. 2002; 71:14-21. doi: 10.1086/341036 PMID: 12016589
52. Page T, Coleman M. Purine metabolism abnormalities in a hyperuricosuric subclass of autism. Biochim Biophys Acta. 2000; 1500:291-6. PMID: 10699370
53. Page T, Moseley C. Metabolic treatment of hyperuricosuric autism. Prog Neuropsychopharmacol Biol Psychiatry. 2002; 26:397-400. PMID: 11817520
54. Naviaux RK, Zolkipli Z, Wang L, Nakayama T, Naviaux JC, Le TP, et al. Antipurinergic therapy corrects the autism-like features in the poly(IC) mouse model. PLOS ONE. 2013; 8:e57380. doi: 10.1371/ journal.pone.0057380 PMID: 23516405
55. Naviaux JC, Schuchbauer MA, Li K, Risbrough VB, Powell SB, Naviaux RK. Reversal of autism-like behaviors and metabolism in adult mice with single-dose antipurinergic therapy. Transl Psychiatry. 2014; 4:e400. doi: 10.1038/tp.2014.33 PMID: 24937094
56. Oliveira G, Diogo L, Grazina M, Garcia P, Ataide A, Marques C, et al. Mitochondrial dysfunction in autism spectrum disorders: a population-based study. Dev Med Child Neurol. 2005; 47:185-9. PMID: 15739723
57. Weissman JR, Kelley RI, Bauman ML, Cohen BH, Murray KF, Mitchell RL, et al. Mitochondrial disease in autism spectrum disorder patients: a cohort analysis. PLOS ONE. 2008; 3:e3815. doi: 10.1371/ journal.pone.0003815 PMID: 19043581
58. El-Ansary A, Al-Daihan S, Al-Dbass A, Al-Ayadhi L. Measurement of selected ions related to oxidative stress and energy metabolism in Saudi autistic children. Clin Biochem. 2010; 43:63-70. doi: 10.1016/j. clinbiochem.2009.09.008 PMID: 19781542
59. Smith J, Rho JM, Teskey GC. Ketogenic diet restores aberrant cortical motor maps and excitation-toinhibition imbalance in the BTBR mouse model of autism spectrum disorder. Behav Brain Res. 2016; 304:67-70. doi: 10.1016/j.bbr.2016.02.015 PMID: 26876011
60. Rubenstein JLR, Merzenich MM. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003; 2:255-7. PMID: 14606691