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Published in: Journal of Neuroinflammation 1/2012

Open Access 01-12-2012 | Research

The enteric bacterial metabolite propionic acid alters brain and plasma phospholipid molecular species: further development of a rodent model of autism spectrum disorders

Authors: Raymond H Thomas, Melissa M Meeking, Jennifer R Mepham, Lisa Tichenoff, Fred Possmayer, Suya Liu, Derrick F MacFabe

Published in: Journal of Neuroinflammation | Issue 1/2012

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Abstract

Gastrointestinal symptoms and altered blood phospholipid profiles have been reported in patients with autism spectrum disorders (ASD). Most of the phospholipid analyses have been conducted on the fatty acid composition of isolated phospholipid classes following hydrolysis. A paucity of information exists on how the intact phospholipid molecular species are altered in ASD. We applied ESI/MS to determine how brain and blood intact phospholipid species were altered during the induction of ASD-like behaviors in rats following intraventricular infusions with the enteric bacterial metabolite propionic acid. Animals were infused daily for 8 days, locomotor activity assessed, and animals killed during the induced behaviors. Propionic acid infusions increased locomotor activity. Lipid analysis revealed treatment altered 21 brain and 30 blood phospholipid molecular species. Notable alterations were observed in the composition of brain SM, diacyl mono and polyunsaturated PC, PI, PS, PE, and plasmalogen PC and PE molecular species. These alterations suggest that the propionic acid rat model is a useful tool to study aberrations in lipid metabolism known to affect membrane fluidity, peroxisomal function, gap junction coupling capacity, signaling, and neuroinflammation, all of which may be associated with the pathogenesis of ASD.
Literature
1.
go back to reference Amminger GP, Berger GE, Schafer MR, Klier C, Friedrich MH, Feucht M: Omega-3 fatty acids supplementation in children with autism: a double-blind randomized, placebo-controlled pilot study. Biol Psychiatry 2007, 61:551–553.CrossRefPubMed Amminger GP, Berger GE, Schafer MR, Klier C, Friedrich MH, Feucht M: Omega-3 fatty acids supplementation in children with autism: a double-blind randomized, placebo-controlled pilot study. Biol Psychiatry 2007, 61:551–553.CrossRefPubMed
2.
go back to reference Finegold SM, Molitoris D, Song Y, Liu C, Vaisanen ML, Bolte E, McTeague M, Sandler R, Wexler H, Marlowe EM, Collins MD, Lawson PA, Summanen P, Baysallar M, Tomzynski TJ, Read E, Johnson E, Rolfe R, Nasir P, Shah H, Haake DA, Manning P, Kaul A: Gastrointestinal microflora studies in late-onset autism. Clin Infect Dis 2002, 35:S6-S16.CrossRefPubMed Finegold SM, Molitoris D, Song Y, Liu C, Vaisanen ML, Bolte E, McTeague M, Sandler R, Wexler H, Marlowe EM, Collins MD, Lawson PA, Summanen P, Baysallar M, Tomzynski TJ, Read E, Johnson E, Rolfe R, Nasir P, Shah H, Haake DA, Manning P, Kaul A: Gastrointestinal microflora studies in late-onset autism. Clin Infect Dis 2002, 35:S6-S16.CrossRefPubMed
3.
go back to reference Hu VW, Frank BC, Heine S, Lee NH, Quackenbush J: Gene expression profiling of lymphoblastoid cell lines from monozygotic twins discordant in severity of autism reveals differential regulation of neurologically relevant genes. BMC Genomics 2006, 7:118.CrossRefPubMedPubMedCentral Hu VW, Frank BC, Heine S, Lee NH, Quackenbush J: Gene expression profiling of lymphoblastoid cell lines from monozygotic twins discordant in severity of autism reveals differential regulation of neurologically relevant genes. BMC Genomics 2006, 7:118.CrossRefPubMedPubMedCentral
4.
go back to reference Sarachana T, Zhou R, Chen G, Manji HK, Hu VW: Investigation of post-transcriptional gene regulatory networks associated with autism spectrum disorders by microRNA expression profiling of lymphoblastoid cell lines. Genome Med 2010, 2:23.CrossRefPubMedPubMedCentral Sarachana T, Zhou R, Chen G, Manji HK, Hu VW: Investigation of post-transcriptional gene regulatory networks associated with autism spectrum disorders by microRNA expression profiling of lymphoblastoid cell lines. Genome Med 2010, 2:23.CrossRefPubMedPubMedCentral
5.
go back to reference Wiest MM, German JB, Harvey DJ, Watkins SM, Hertz-Picciotto I: Plasma fatty acid profiles in autism: a case–control study. Prostaglandins Leukot Essent Fatty Acids 2009, 80:221–227.CrossRefPubMed Wiest MM, German JB, Harvey DJ, Watkins SM, Hertz-Picciotto I: Plasma fatty acid profiles in autism: a case–control study. Prostaglandins Leukot Essent Fatty Acids 2009, 80:221–227.CrossRefPubMed
6.
go back to reference Zerrate MC, Pletnikov M, Connors SL, Vargas DL, Seidler FJ, Zimmerman AW, Slotkin TA, Pardo CA: Neuroinflammation and behavioral abnormalities after neonatal terbutaline treatment in rats: implications for autism. J Pharmacol Exp Ther 2007, 322:16–22.CrossRefPubMed Zerrate MC, Pletnikov M, Connors SL, Vargas DL, Seidler FJ, Zimmerman AW, Slotkin TA, Pardo CA: Neuroinflammation and behavioral abnormalities after neonatal terbutaline treatment in rats: implications for autism. J Pharmacol Exp Ther 2007, 322:16–22.CrossRefPubMed
7.
go back to reference MacFabe DF, Cain DP, Rodriguez-Capote K, Franklin AE, Hoffman JE, Boon F, Taylor AR, Kavaliers M, Ossenkopp KP: Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders. Behav Brain Res 2007, 176:149–169.CrossRefPubMed MacFabe DF, Cain DP, Rodriguez-Capote K, Franklin AE, Hoffman JE, Boon F, Taylor AR, Kavaliers M, Ossenkopp KP: Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders. Behav Brain Res 2007, 176:149–169.CrossRefPubMed
8.
go back to reference MacFabe DF, Rodriguez-Capote K, Hoffman JE, Franklin AE, Mohammad-Asef Y, Taylor A, Boon F, Cain DP, Kavaliers M, Possmayer F, Ossenkopp KP: A novel rodent model of autism: Intraventricular infusions of propionic acid increase locomotor activity and induce neuroinflammation and oxidative stress in discrete regions of adult rat brain. Am J Biochem & Biotech. 2008, 4:146–166.CrossRef MacFabe DF, Rodriguez-Capote K, Hoffman JE, Franklin AE, Mohammad-Asef Y, Taylor A, Boon F, Cain DP, Kavaliers M, Possmayer F, Ossenkopp KP: A novel rodent model of autism: Intraventricular infusions of propionic acid increase locomotor activity and induce neuroinflammation and oxidative stress in discrete regions of adult rat brain. Am J Biochem & Biotech. 2008, 4:146–166.CrossRef
9.
go back to reference MacFabe DF, Cain NE, Boon F, Ossenkopp KP, Cain DP: Effects of the enteric bacterial metabolic product propionic acid on object-directed behavior, social behavior, cognition, and neuroinflammation in adolescent rats: Relevance to autism spectrum disorder. Behav Brain Res 2010, 217:47–54.CrossRefPubMed MacFabe DF, Cain NE, Boon F, Ossenkopp KP, Cain DP: Effects of the enteric bacterial metabolic product propionic acid on object-directed behavior, social behavior, cognition, and neuroinflammation in adolescent rats: Relevance to autism spectrum disorder. Behav Brain Res 2010, 217:47–54.CrossRefPubMed
10.
go back to reference Shultz SR, MacFabe DF, Martin S, Jackson J, Taylor R, Boon F, Ossenkopp KP, Cain DP: Intracerebroventricular injections of the enteric bacterial metabolic product propionic acid impair cognition and sensorimotor ability in the Long-Evans rat: further development of a rodent model of autism. Behav Brain Res 2009, 200:33–41.CrossRefPubMed Shultz SR, MacFabe DF, Martin S, Jackson J, Taylor R, Boon F, Ossenkopp KP, Cain DP: Intracerebroventricular injections of the enteric bacterial metabolic product propionic acid impair cognition and sensorimotor ability in the Long-Evans rat: further development of a rodent model of autism. Behav Brain Res 2009, 200:33–41.CrossRefPubMed
11.
go back to reference Shultz SR, MacFabe DF, Ossenkopp KP, Scratch S, Whelan J, Taylor R, Cain DP: Intracerebroventricular injection of propionic acid, an enteric bacterial metabolic end-product, impairs social behavior in the rat: implications for an animal model of autism. Neuropharmacology 2008, 54:901–911.CrossRefPubMed Shultz SR, MacFabe DF, Ossenkopp KP, Scratch S, Whelan J, Taylor R, Cain DP: Intracerebroventricular injection of propionic acid, an enteric bacterial metabolic end-product, impairs social behavior in the rat: implications for an animal model of autism. Neuropharmacology 2008, 54:901–911.CrossRefPubMed
12.
go back to reference Thomas RH, Foley KA, Mepham JR, Tichenoff LJ, Possmayer F, MacFabe DF: Altered brain phospholipid and acylcarnitine profiles in propionic acid infused rodents: further development of a potential model of autism spectrum disorders. J Neurochem 2010, 113:515–529.CrossRefPubMed Thomas RH, Foley KA, Mepham JR, Tichenoff LJ, Possmayer F, MacFabe DF: Altered brain phospholipid and acylcarnitine profiles in propionic acid infused rodents: further development of a potential model of autism spectrum disorders. J Neurochem 2010, 113:515–529.CrossRefPubMed
13.
go back to reference Mortensen PB, Clausen MR: Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease. Scand J Gastroenterol Suppl 1996, 216:132–148.CrossRefPubMed Mortensen PB, Clausen MR: Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease. Scand J Gastroenterol Suppl 1996, 216:132–148.CrossRefPubMed
14.
go back to reference Finegold SM, Dowd SE, Gontcharova V, Liu C, Henley KE, Wolcott RD, Youn E, Summanen PH, Granpeesheh D, Dixon D, Liu M, Molitoris DR, Green JA: Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 2010, 16:444–453.CrossRefPubMed Finegold SM, Dowd SE, Gontcharova V, Liu C, Henley KE, Wolcott RD, Youn E, Summanen PH, Granpeesheh D, Dixon D, Liu M, Molitoris DR, Green JA: Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 2010, 16:444–453.CrossRefPubMed
15.
go back to reference Brock M, Buckel W: On the mechanism of action of the antifungal agent propionate. Eur J Biochem 2004, 271:3227–3241.CrossRefPubMed Brock M, Buckel W: On the mechanism of action of the antifungal agent propionate. Eur J Biochem 2004, 271:3227–3241.CrossRefPubMed
16.
go back to reference Wajner M, Latini A, Wyse AT, Dutra-Filho CS: The role of oxidative damage in the neuropathology of organic acidurias: insights from animal studies. J Inherit Metab Dis 2004, 27:427–448.CrossRefPubMed Wajner M, Latini A, Wyse AT, Dutra-Filho CS: The role of oxidative damage in the neuropathology of organic acidurias: insights from animal studies. J Inherit Metab Dis 2004, 27:427–448.CrossRefPubMed
17.
go back to reference Conn AR, Fell DI, Steele RD: Characterization of alpha-keto acid transport across blood–brain barrier in rats. Am J Physiol 1983, 245:E253-E260.PubMed Conn AR, Fell DI, Steele RD: Characterization of alpha-keto acid transport across blood–brain barrier in rats. Am J Physiol 1983, 245:E253-E260.PubMed
18.
go back to reference Karuri AR, Dobrowsky E, Tannock IF: Selective cellular acidification and toxicity of weak organic acids in an acidic microenvironment. Br J Cancer 1993, 68:1080–1087.CrossRefPubMedPubMedCentral Karuri AR, Dobrowsky E, Tannock IF: Selective cellular acidification and toxicity of weak organic acids in an acidic microenvironment. Br J Cancer 1993, 68:1080–1087.CrossRefPubMedPubMedCentral
19.
go back to reference Rorig B, Klausa G, Sutor B: Intracellular acidification reduced gap junction coupling between immature rat neocortical pyramidal neurones. J Physiol 1996, 490:31–49.CrossRefPubMedPubMedCentral Rorig B, Klausa G, Sutor B: Intracellular acidification reduced gap junction coupling between immature rat neocortical pyramidal neurones. J Physiol 1996, 490:31–49.CrossRefPubMedPubMedCentral
20.
go back to reference DeCastro M, Nankova BB, Shah P, Patel P, Mally PV, Mishra R, La Gamma EF: Short chain fatty acids regulate tyrosine hydroxylase gene expression through a cAMP-dependent signaling pathway. Brain Res Mol Brain Res 2005, 142:28–38.CrossRefPubMed DeCastro M, Nankova BB, Shah P, Patel P, Mally PV, Mishra R, La Gamma EF: Short chain fatty acids regulate tyrosine hydroxylase gene expression through a cAMP-dependent signaling pathway. Brain Res Mol Brain Res 2005, 142:28–38.CrossRefPubMed
21.
go back to reference Maurer MH, Canis M, Kuschinsky W, Duelli R: Correlation between local monocarboxylate transporter 1 (MCT1) and glucose transporter 1 (GLUT1) densities in the adult rat brain. Neurosci Lett 2004, 355:105–108.CrossRefPubMed Maurer MH, Canis M, Kuschinsky W, Duelli R: Correlation between local monocarboxylate transporter 1 (MCT1) and glucose transporter 1 (GLUT1) densities in the adult rat brain. Neurosci Lett 2004, 355:105–108.CrossRefPubMed
22.
go back to reference Nakao S, Moriya Y, Furuyama S, Niederman R, Sugiya H: Propionic acid stimulates superoxide generation in human neutrophils. Cell Biol Int 1998, 22:331–337.CrossRefPubMed Nakao S, Moriya Y, Furuyama S, Niederman R, Sugiya H: Propionic acid stimulates superoxide generation in human neutrophils. Cell Biol Int 1998, 22:331–337.CrossRefPubMed
23.
go back to reference Hara H, Haga S, Aoyama Y, Kiriyama S: Short-chain fatty acids suppress cholesterol synthesis in rat liver and intestine. J Nutr 1999, 129:942–948.PubMed Hara H, Haga S, Aoyama Y, Kiriyama S: Short-chain fatty acids suppress cholesterol synthesis in rat liver and intestine. J Nutr 1999, 129:942–948.PubMed
24.
go back to reference Le Poul E, Loison C, Struyf S, Springael JY, Lannoy V, Decobecq ME, Brezillon S, Dupriez V, Vassart G, Van Damme J, Parmentier M, Detheux M: Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 2003, 278:25481–25489.CrossRefPubMed Le Poul E, Loison C, Struyf S, Springael JY, Lannoy V, Decobecq ME, Brezillon S, Dupriez V, Vassart G, Van Damme J, Parmentier M, Detheux M: Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 2003, 278:25481–25489.CrossRefPubMed
25.
go back to reference Parab S, Nankova BB, La Gamma EF: Differential regulation of the tyrosine hydroxylase and enkephalin neuropeptide transmitter genes in rat PC12 cells by short chain fatty acids: concentration-dependent effects on transcription and RNA stability. Brain Res 2007, 1132:42–50.CrossRefPubMed Parab S, Nankova BB, La Gamma EF: Differential regulation of the tyrosine hydroxylase and enkephalin neuropeptide transmitter genes in rat PC12 cells by short chain fatty acids: concentration-dependent effects on transcription and RNA stability. Brain Res 2007, 1132:42–50.CrossRefPubMed
26.
go back to reference Frye RE, Rossignol DA: Mitochondrial dysfunction can connect the diverse medical symptoms associated with autism spectrum disorders. Pediatr Res 2011, 69:41R-47R.CrossRefPubMedPubMedCentral Frye RE, Rossignol DA: Mitochondrial dysfunction can connect the diverse medical symptoms associated with autism spectrum disorders. Pediatr Res 2011, 69:41R-47R.CrossRefPubMedPubMedCentral
27.
go back to reference Pastural E, Ritchie S, Lu Y, Jin W, Kavianpour A, Khine Su-Myat K, Heath D, Wood PL, Fisk M, Goodenowe DB: Novel plasma phospholipid biomarkers of autism: Mitochondrial dysfunction as a putative causative mechanism. Prostaglandins Leukot Essent Fatty Acids 2009, 81:253–264.CrossRefPubMed Pastural E, Ritchie S, Lu Y, Jin W, Kavianpour A, Khine Su-Myat K, Heath D, Wood PL, Fisk M, Goodenowe DB: Novel plasma phospholipid biomarkers of autism: Mitochondrial dysfunction as a putative causative mechanism. Prostaglandins Leukot Essent Fatty Acids 2009, 81:253–264.CrossRefPubMed
28.
go back to reference Tamiji J, Crawford DA: The neurobiology of lipid metabolism in autism spectrum disorders. Neurosignals 2010, 18:98–112.CrossRefPubMed Tamiji J, Crawford DA: The neurobiology of lipid metabolism in autism spectrum disorders. Neurosignals 2010, 18:98–112.CrossRefPubMed
29.
go back to reference Bell JG, MacKinlay EE, Dick JR, MacDonald DJ, Boyle RM, Glen AC: Essential fatty acids and phospholipase A2 in autistic spectrum disorders. Prostaglandins Leukot. Essent Fatty Acids 2004, 71:201–204.CrossRefPubMed Bell JG, MacKinlay EE, Dick JR, MacDonald DJ, Boyle RM, Glen AC: Essential fatty acids and phospholipase A2 in autistic spectrum disorders. Prostaglandins Leukot. Essent Fatty Acids 2004, 71:201–204.CrossRefPubMed
30.
go back to reference Bell JG, Sargent JR, Tocher DR, Dick JR: Red blood cell fatty acid compositions in a patient with autistic spectrum disorder: a characteristic abnormality in neurodevelopmental disorders? Prostaglandins Leukot. Essent Fatty Acids 2000, 63:21–25.CrossRef Bell JG, Sargent JR, Tocher DR, Dick JR: Red blood cell fatty acid compositions in a patient with autistic spectrum disorder: a characteristic abnormality in neurodevelopmental disorders? Prostaglandins Leukot. Essent Fatty Acids 2000, 63:21–25.CrossRef
31.
go back to reference Richardson AJ: Clinical trials of fatty acid treatment in ADHD, dyslexia, dyspraxia and the autistic spectrum. Prostaglandins Leukot Essent Fatty Acids 2004, 70:383–390.CrossRefPubMed Richardson AJ: Clinical trials of fatty acid treatment in ADHD, dyslexia, dyspraxia and the autistic spectrum. Prostaglandins Leukot Essent Fatty Acids 2004, 70:383–390.CrossRefPubMed
32.
go back to reference Vancassel S, Durand G, Barthelemy C, Lejeune B, Martineau J, Guilloteau D, Andres C, Chalon S: Plasma fatty acid levels in autistic children. Prostaglandins Leukot Essent Fatty Acids 2001, 65:1–7.CrossRefPubMed Vancassel S, Durand G, Barthelemy C, Lejeune B, Martineau J, Guilloteau D, Andres C, Chalon S: Plasma fatty acid levels in autistic children. Prostaglandins Leukot Essent Fatty Acids 2001, 65:1–7.CrossRefPubMed
33.
go back to reference Brugger B, Erben G, Sandhoff R, Wieland FT, Lehmann WD: Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc Natl Acad Sci U S A 1997, 94:2339–2344.CrossRefPubMedPubMedCentral Brugger B, Erben G, Sandhoff R, Wieland FT, Lehmann WD: Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc Natl Acad Sci U S A 1997, 94:2339–2344.CrossRefPubMedPubMedCentral
34.
go back to reference Postle AD, Heeley EL, Wilton DC: A comparison of the molecular species compositions of mammalian lung surfactant phospholipids. Comp Biochem Physiol A Mol Integr Physiol 2001, 129:65–73.CrossRefPubMed Postle AD, Heeley EL, Wilton DC: A comparison of the molecular species compositions of mammalian lung surfactant phospholipids. Comp Biochem Physiol A Mol Integr Physiol 2001, 129:65–73.CrossRefPubMed
35.
go back to reference Pulfer M, Murphy RC: Electrospray mass spectrometry of phospholipids. Mass Spectrom Rev 2003, 22:332–364.CrossRefPubMed Pulfer M, Murphy RC: Electrospray mass spectrometry of phospholipids. Mass Spectrom Rev 2003, 22:332–364.CrossRefPubMed
36.
go back to reference Meguid NA, Atta HM, Gouda AS, Khalil RO: Role of polyunsaturated fatty acids in the management of Egyptian children with autism. Clin Biochem 2008, 41:1044–1048.CrossRefPubMed Meguid NA, Atta HM, Gouda AS, Khalil RO: Role of polyunsaturated fatty acids in the management of Egyptian children with autism. Clin Biochem 2008, 41:1044–1048.CrossRefPubMed
37.
go back to reference Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates. Montreal: Academic Press; 1986. Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates. Montreal: Academic Press; 1986.
38.
go back to reference Folch J, Lees M, Sloane Stanley GH: A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957, 226:497–509.PubMed Folch J, Lees M, Sloane Stanley GH: A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957, 226:497–509.PubMed
39.
go back to reference Sherma J, Fried B: Handbook of Thin Layer Chromatography. New York, NY: Marcel and Dekker; 2003:pp. ii-991.CrossRef Sherma J, Fried B: Handbook of Thin Layer Chromatography. New York, NY: Marcel and Dekker; 2003:pp. ii-991.CrossRef
40.
go back to reference Deeley JM, Mitchell TW, Wei X, Korth J, Nealon JR, Blanksby SJ, Truscott RJ: Human lens lipids differ markedly from those of commonly used experimental animals. Biochim Biophys Acta 2008, 1781:288–298.CrossRefPubMed Deeley JM, Mitchell TW, Wei X, Korth J, Nealon JR, Blanksby SJ, Truscott RJ: Human lens lipids differ markedly from those of commonly used experimental animals. Biochim Biophys Acta 2008, 1781:288–298.CrossRefPubMed
41.
go back to reference Volkmar FR, Lord C, Bailey A, Schultz RT, Klin A: Autism and pervasive developmental disorders. J Child Psychol Psychiatry 2004, 45:135–170.CrossRefPubMed Volkmar FR, Lord C, Bailey A, Schultz RT, Klin A: Autism and pervasive developmental disorders. J Child Psychol Psychiatry 2004, 45:135–170.CrossRefPubMed
42.
go back to reference Cannizzaro C, Monastero R, Vacca M, Martire M: [3 H]-DA release evoked by low pH medium and internal H + accumulation in rat hypothalamic synaptosomes: involvement of calcium ions. Neurochem Int 2003, 43:9–17.CrossRefPubMed Cannizzaro C, Monastero R, Vacca M, Martire M: [3 H]-DA release evoked by low pH medium and internal H + accumulation in rat hypothalamic synaptosomes: involvement of calcium ions. Neurochem Int 2003, 43:9–17.CrossRefPubMed
43.
go back to reference Remblier C, Pontcharraud R, Tallineau C, Piriou A, Huguet F: Lactic acid-induced increase of extracellular dopamine measured by microdialysis in rat striatum: evidence for glutamatergic and oxidative mechanisms. Brain Res 1999, 837:22–28.CrossRefPubMed Remblier C, Pontcharraud R, Tallineau C, Piriou A, Huguet F: Lactic acid-induced increase of extracellular dopamine measured by microdialysis in rat striatum: evidence for glutamatergic and oxidative mechanisms. Brain Res 1999, 837:22–28.CrossRefPubMed
44.
go back to reference Severson CA, Wang W, Pieribone VA, Dohle CI, Richerson GB: Midbrain serotonergic neurons are central pH chemoreceptors. Nat Neurosci 2003, 6:1139–1140.CrossRefPubMed Severson CA, Wang W, Pieribone VA, Dohle CI, Richerson GB: Midbrain serotonergic neurons are central pH chemoreceptors. Nat Neurosci 2003, 6:1139–1140.CrossRefPubMed
45.
go back to reference Bronstein JM, Farber DB, Wasterlain CG: Regulation of type-II calmodulin kinase: functional implications. Brain Res Rev 1993, 18:135–147.CrossRefPubMed Bronstein JM, Farber DB, Wasterlain CG: Regulation of type-II calmodulin kinase: functional implications. Brain Res Rev 1993, 18:135–147.CrossRefPubMed
46.
go back to reference Nakao S, Fujii A, Niederman R: Alteration of cytoplasmic Ca2+ in resting and stimulated human neutrophils by short-chain carboxylic acids at neutral pH. Infect Immun 1992, 60:5307–5311.PubMedPubMedCentral Nakao S, Fujii A, Niederman R: Alteration of cytoplasmic Ca2+ in resting and stimulated human neutrophils by short-chain carboxylic acids at neutral pH. Infect Immun 1992, 60:5307–5311.PubMedPubMedCentral
47.
go back to reference Fukuchi M, Nii T, Ishimaru N, Minamino A, Hara D, Takasaki I, Tabuchi A, Tsuda M: Valproic acid induces up- or down-regulation of gene expression responsible for the neuronal excitation and inhibition in rat cortical neurons through its epigenetic actions. Neurosci Res 2009, 65:35–43.CrossRefPubMed Fukuchi M, Nii T, Ishimaru N, Minamino A, Hara D, Takasaki I, Tabuchi A, Tsuda M: Valproic acid induces up- or down-regulation of gene expression responsible for the neuronal excitation and inhibition in rat cortical neurons through its epigenetic actions. Neurosci Res 2009, 65:35–43.CrossRefPubMed
48.
go back to reference Bayir H, Tyurin VA, Tyurina YY, Viner R, Ritov V, Amoscato AA, Zhao Q, Zhang XJ, Janesko-Feldman KL, Alexander H, Basova LV, Clark RS, Kochanek PM, Kagan VE: Selective early cardiolipin peroxidation after traumatic brain injury: an oxidative lipidomics analysis. Ann Neurol 2007, 62:154–169.CrossRefPubMed Bayir H, Tyurin VA, Tyurina YY, Viner R, Ritov V, Amoscato AA, Zhao Q, Zhang XJ, Janesko-Feldman KL, Alexander H, Basova LV, Clark RS, Kochanek PM, Kagan VE: Selective early cardiolipin peroxidation after traumatic brain injury: an oxidative lipidomics analysis. Ann Neurol 2007, 62:154–169.CrossRefPubMed
49.
go back to reference Little SJ, Lynch MA, Manku M, Nicolaou A: Docosahexaenoic acid-induced changes in phospholipids in cortex of young and aged rats: a lipidomic analysis. Prostaglandins Leukot Essent Fatty Acids 2007, 77:155–162.CrossRefPubMed Little SJ, Lynch MA, Manku M, Nicolaou A: Docosahexaenoic acid-induced changes in phospholipids in cortex of young and aged rats: a lipidomic analysis. Prostaglandins Leukot Essent Fatty Acids 2007, 77:155–162.CrossRefPubMed
50.
go back to reference Hon GM, Hassan MS, van Rensburg SJ, Abel S, van JP, Erasmus RT, Matsha T: Red blood cell membrane fluidity in the etiology of multiple sclerosis. J Membr Biol 2009, 232:25–34.CrossRefPubMed Hon GM, Hassan MS, van Rensburg SJ, Abel S, van JP, Erasmus RT, Matsha T: Red blood cell membrane fluidity in the etiology of multiple sclerosis. J Membr Biol 2009, 232:25–34.CrossRefPubMed
51.
go back to reference Kakela R, Somerharju P, Tyynela J: Analysis of phospholipid molecular species in brains from patients with infantile and juvenile neuronal-ceroid lipofuscinosis using liquid chromatography-electrospray ionization mass spectrometry. J Neurochem 2003, 84:1051–1065.CrossRefPubMed Kakela R, Somerharju P, Tyynela J: Analysis of phospholipid molecular species in brains from patients with infantile and juvenile neuronal-ceroid lipofuscinosis using liquid chromatography-electrospray ionization mass spectrometry. J Neurochem 2003, 84:1051–1065.CrossRefPubMed
52.
go back to reference Bu B, Ashwood P, Harvey D, King IB, Water JV, Jin LW: Fatty acid compositions of red blood cell phospholipids in children with autism. Prostaglandins Leukot Essent Fatty Acids 2006, 74:215–221.CrossRefPubMed Bu B, Ashwood P, Harvey D, King IB, Water JV, Jin LW: Fatty acid compositions of red blood cell phospholipids in children with autism. Prostaglandins Leukot Essent Fatty Acids 2006, 74:215–221.CrossRefPubMed
53.
go back to reference Sliwinski S, Croonenberghs J, Christophe A, Deboutte D, Maes M: Polyunsaturated fatty acids: do they have a role in the pathophysiology of autism? Neuro Endocrinol Lett 2006, 27:465–471.PubMed Sliwinski S, Croonenberghs J, Christophe A, Deboutte D, Maes M: Polyunsaturated fatty acids: do they have a role in the pathophysiology of autism? Neuro Endocrinol Lett 2006, 27:465–471.PubMed
54.
go back to reference Farooqui AA, Ong WY, Horrocks LA: Biochemical aspects of neurodegeneration in human brain: involvement of neural membrane phospholipids and phospholipases A2. Neurochem Res 2004, 29:1961–1977.CrossRefPubMed Farooqui AA, Ong WY, Horrocks LA: Biochemical aspects of neurodegeneration in human brain: involvement of neural membrane phospholipids and phospholipases A2. Neurochem Res 2004, 29:1961–1977.CrossRefPubMed
55.
go back to reference Chauhan A, Chauhan V: Oxidative stress in autism. Pathophysiology. 2006, 13:171–181.PubMed Chauhan A, Chauhan V: Oxidative stress in autism. Pathophysiology. 2006, 13:171–181.PubMed
56.
go back to reference Chauhan A, Chauhan V, Brown WT, Cohen I: Oxidative stress in autism: increased lipid peroxidation and reduced serum levels of ceruloplasmin and transferrin–the antioxidant proteins. Life Sci 2004, 75:2539–2549.CrossRefPubMed Chauhan A, Chauhan V, Brown WT, Cohen I: Oxidative stress in autism: increased lipid peroxidation and reduced serum levels of ceruloplasmin and transferrin–the antioxidant proteins. Life Sci 2004, 75:2539–2549.CrossRefPubMed
57.
go back to reference Chauhan V, Chauhan A, Cohen IL, Brown WT, Sheikh A: Alteration in amino-glycerophospholipids levels in the plasma of children with autism: a potential biochemical diagnostic marker. Life Sci 2004, 74:1635–1643.CrossRefPubMed Chauhan V, Chauhan A, Cohen IL, Brown WT, Sheikh A: Alteration in amino-glycerophospholipids levels in the plasma of children with autism: a potential biochemical diagnostic marker. Life Sci 2004, 74:1635–1643.CrossRefPubMed
58.
go back to reference Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA: Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 2004, 57:67–81.CrossRef Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA: Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 2004, 57:67–81.CrossRef
59.
go back to reference Farooqui AA, Horrocks LA: Plasmalogens, phospholipase A(2), and docosahexaenoic acid turnover in brain tissue. J Mol Neurosci 2001, 16:263–272.CrossRefPubMed Farooqui AA, Horrocks LA: Plasmalogens, phospholipase A(2), and docosahexaenoic acid turnover in brain tissue. J Mol Neurosci 2001, 16:263–272.CrossRefPubMed
60.
go back to reference Allen HG, Allen JC, Boyd LC, ston-Mills BP, Fenner GP: Determination of membrane lipid differences in insulin resistant diabetes mellitus type 2 in whites and blacks. Nutrition 2006, 22:1096–1102.CrossRefPubMed Allen HG, Allen JC, Boyd LC, ston-Mills BP, Fenner GP: Determination of membrane lipid differences in insulin resistant diabetes mellitus type 2 in whites and blacks. Nutrition 2006, 22:1096–1102.CrossRefPubMed
61.
go back to reference Schuchardt JP, Huss M, Stauss-Grabo M, Hahn A: Significance of long-chain polyunsaturated fatty acids (PUFAs) for the development and behaviour of children. Eur J Pediatr 2009, 169:149–164.CrossRefPubMed Schuchardt JP, Huss M, Stauss-Grabo M, Hahn A: Significance of long-chain polyunsaturated fatty acids (PUFAs) for the development and behaviour of children. Eur J Pediatr 2009, 169:149–164.CrossRefPubMed
62.
go back to reference Gorgas K, Teigler A, Komljenovic D, Just WW: The ether lipid-deficient mouse: tracking down plasmalogen functions. Biochim Biophys Acta 2006, 1763:1511–1526.CrossRefPubMed Gorgas K, Teigler A, Komljenovic D, Just WW: The ether lipid-deficient mouse: tracking down plasmalogen functions. Biochim Biophys Acta 2006, 1763:1511–1526.CrossRefPubMed
63.
go back to reference Dommels YE, Alink GM, Linssen JP, van OB: Effects of n-6 and n-3 polyunsaturated fatty acids on gap junctional intercellular communication during spontaneous differentiation of the human colon adenocarcinoma cell line Caco-2. Nutr Cancer 2002, 42:125–130.CrossRefPubMed Dommels YE, Alink GM, Linssen JP, van OB: Effects of n-6 and n-3 polyunsaturated fatty acids on gap junctional intercellular communication during spontaneous differentiation of the human colon adenocarcinoma cell line Caco-2. Nutr Cancer 2002, 42:125–130.CrossRefPubMed
64.
go back to reference Martinez AD, Saez JC: Regulation of astrocyte gap junctions by hypoxia-reoxygenation. Brain Res Brain Res Rev 2000, 32:250–258.CrossRefPubMed Martinez AD, Saez JC: Regulation of astrocyte gap junctions by hypoxia-reoxygenation. Brain Res Brain Res Rev 2000, 32:250–258.CrossRefPubMed
65.
go back to reference Aylsworth CF, Trosko JE, Welsch CW: Influence of lipids on gap-junction-mediated intercellular communication between Chinese hamster cells in vitro. Cancer Res 1986, 46:4527–4533.PubMed Aylsworth CF, Trosko JE, Welsch CW: Influence of lipids on gap-junction-mediated intercellular communication between Chinese hamster cells in vitro. Cancer Res 1986, 46:4527–4533.PubMed
66.
go back to reference Champeil-Potokar G, Chaumontet C, Guesnet P, Lavialle M, Denis I: Docosahexaenoic acid (22:6n-3) enrichment of membrane phospholipids increases gap junction coupling capacity in cultured astrocytes. Eur J Neurosci 2006, 24:3084–3090.CrossRefPubMed Champeil-Potokar G, Chaumontet C, Guesnet P, Lavialle M, Denis I: Docosahexaenoic acid (22:6n-3) enrichment of membrane phospholipids increases gap junction coupling capacity in cultured astrocytes. Eur J Neurosci 2006, 24:3084–3090.CrossRefPubMed
67.
go back to reference Rouach N, Avignone E, Meme W, Koulakoff A, Venance L, Blomstrand F, Giaume C: Gap junctions and connexin expression in the normal and pathological central nervous system. Biol Cell 2002, 94:457–475.CrossRefPubMed Rouach N, Avignone E, Meme W, Koulakoff A, Venance L, Blomstrand F, Giaume C: Gap junctions and connexin expression in the normal and pathological central nervous system. Biol Cell 2002, 94:457–475.CrossRefPubMed
Metadata
Title
The enteric bacterial metabolite propionic acid alters brain and plasma phospholipid molecular species: further development of a rodent model of autism spectrum disorders
Authors
Raymond H Thomas
Melissa M Meeking
Jennifer R Mepham
Lisa Tichenoff
Fred Possmayer
Suya Liu
Derrick F MacFabe
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2012
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/1742-2094-9-153

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