Skip to main content
Erschienen in: Metabolic Brain Disease 4/2018

22.03.2018 | Original Article

Impaired lipid metabolism markers to assess the risk of neuroinflammation in autism spectrum disorder

verfasst von: Hanan Qasem, Laila Al-Ayadhi, Geir Bjørklund, Salvatore Chirumbolo, Afaf El-Ansary

Erschienen in: Metabolic Brain Disease | Ausgabe 4/2018

Einloggen, um Zugang zu erhalten

Abstract

Autism spectrum disorder (ASD) is a multifactorial disorder caused by an interaction between environmental risk factors and a genetic background. It is characterized by impairment in communication, social interaction, repetitive behavior, and sensory processing. The etiology of ASD is still not fully understood, and the role of neuroinflammation in autism behaviors needs to be further investigated. The aim of the present study was to test the possible association between prostaglandin E2 (PGE2), cyclooxygenase-2 (COX-2), microsomal prostaglandin E synthase-1 (mPGES-1), prostaglandin PGE2 EP2 receptors and nuclear kappa B (NF-κB) and the severity of cognitive disorders, social impairment, and sensory dysfunction. PGE2, COX-2, mPGES-1, PGE2-EP2 receptors and NF-κB as biochemical parameters related to neuroinflammation were determined in the plasma of 47 Saudi male patients with ASD, categorized as mild to moderate and severe as indicated by the Childhood Autism Rating Scale (CARS) or the Social Responsiveness Scale (SRS) or the Short Sensory Profile (SSP) and compared to 46 neurotypical controls. The data indicated that ASD patients have remarkably higher levels of the measured parameters compared to neurotypical controls, except for EP2 receptors that showed an opposite trend. While the measured parameter did not correlate with the severity of social and cognitive dysfunction, PGE2, COX-2, and mPGES-1 were remarkably associated with the dysfunction in sensory processing. NF-κB was significantly increased in relation to age. Based on the discussed data, the positive correlation between PGE2, COX-2, and mPGES-1 confirm the role of PGE2 pathway and neuroinflammation in the etiology of ASD, and the possibility of using PGE2, COX-2 and mPGES-1 as biomarkers of autism severity. NF-κB as inflammatory inducer showed an elevated level in plasma of ASD individuals. Receiver operating characteristic analysis together with predictiveness diagrams proved that the measured parameters could be used as predictive biomarkers of biochemical correlates to ASD.
Literatur
Zurück zum Zitat Ahmad AS, Zhuang H, Echeverria V, Doré S (2006) Stimulation of prostaglandin EP2 receptors prevents NMDA-induced excitotoxicity. J Neurotrauma 23:1895–1903CrossRefPubMed Ahmad AS, Zhuang H, Echeverria V, Doré S (2006) Stimulation of prostaglandin EP2 receptors prevents NMDA-induced excitotoxicity. J Neurotrauma 23:1895–1903CrossRefPubMed
Zurück zum Zitat Al-Gadani Y, El-Ansary A, Attas O, Al-Ayadhi L (2009) Metabolic biomarkers related to oxidative stress and antioxidant status in Saudi autistic children. Clin Biochem 42:1032–1040CrossRefPubMed Al-Gadani Y, El-Ansary A, Attas O, Al-Ayadhi L (2009) Metabolic biomarkers related to oxidative stress and antioxidant status in Saudi autistic children. Clin Biochem 42:1032–1040CrossRefPubMed
Zurück zum Zitat Allan SM, Rothwell NJ (2003) Inflammation in central nervous system injury. Philos Trans R Soc Lond Ser B Biol Sci 358:1669–1677CrossRef Allan SM, Rothwell NJ (2003) Inflammation in central nervous system injury. Philos Trans R Soc Lond Ser B Biol Sci 358:1669–1677CrossRef
Zurück zum Zitat Bell JG, MacKinlay EE, Dick JR, MacDonald DJ, Boyle RM, Glen AC (2004) Essential fatty acids and phospholipase A2 in autistic spectrum disorders. Prostaglandins Leukot Essent Fatty Acids 71:201–204CrossRefPubMed Bell JG, MacKinlay EE, Dick JR, MacDonald DJ, Boyle RM, Glen AC (2004) Essential fatty acids and phospholipase A2 in autistic spectrum disorders. Prostaglandins Leukot Essent Fatty Acids 71:201–204CrossRefPubMed
Zurück zum Zitat Bezzi P, Volterra A (2001) A neuron-glia signalling network in the active brain. Curr Opin Neurobiol 11:387–394CrossRefPubMed Bezzi P, Volterra A (2001) A neuron-glia signalling network in the active brain. Curr Opin Neurobiol 11:387–394CrossRefPubMed
Zurück zum Zitat Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391:281–285CrossRefPubMed Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391:281–285CrossRefPubMed
Zurück zum Zitat Bjørklund G, Saad K, Chirumbolo S, Kern JK, Geier DA, Geier MR, Urbina MA (2016) Immune dysfunction and neuroinflammation in autism spectrum disorder. Acta Neurobiol Exp 76:257–268 Bjørklund G, Saad K, Chirumbolo S, Kern JK, Geier DA, Geier MR, Urbina MA (2016) Immune dysfunction and neuroinflammation in autism spectrum disorder. Acta Neurobiol Exp 76:257–268
Zurück zum Zitat Blais V, Rivest S (2001) Inhibitory action of nitric oxide on circulating tumor necrosis factor-induced NF-kappaB activity and COX-2 transcription in the endothelium of the brain capillaries. J Neuropathol Exp Neurol 60:893–905CrossRefPubMed Blais V, Rivest S (2001) Inhibitory action of nitric oxide on circulating tumor necrosis factor-induced NF-kappaB activity and COX-2 transcription in the endothelium of the brain capillaries. J Neuropathol Exp Neurol 60:893–905CrossRefPubMed
Zurück zum Zitat Blaylock RL, Strunecka A (2009) Immune-glutamatergic dysfunction as a central mechanism of the autism spectrum disorders. Curr Med Chem 16:157–170CrossRefPubMed Blaylock RL, Strunecka A (2009) Immune-glutamatergic dysfunction as a central mechanism of the autism spectrum disorders. Curr Med Chem 16:157–170CrossRefPubMed
Zurück zum Zitat Bonventre JV, Huang Z, Taheri MR, O'Leary E, Li E, Moskowitz MA, Sapirstein A (1997) Reduced fertility and postischaemic brain injury in mice deficient in cytosolic phospholipase A2. Nature 390:622–625CrossRefPubMed Bonventre JV, Huang Z, Taheri MR, O'Leary E, Li E, Moskowitz MA, Sapirstein A (1997) Reduced fertility and postischaemic brain injury in mice deficient in cytosolic phospholipase A2. Nature 390:622–625CrossRefPubMed
Zurück zum Zitat Camacho M, Gerbolés E, Escudero JR, Antón R, García-Moll X, Vila L (2007) Microsomal prostaglandin E synthase-1, which is not coupled to a particular cyclooxygenase isoenzyme, is essential for prostaglandin E(2) biosynthesis in vascular smooth muscle cells. J Thromb Haemost 5:1411–1419CrossRefPubMed Camacho M, Gerbolés E, Escudero JR, Antón R, García-Moll X, Vila L (2007) Microsomal prostaglandin E synthase-1, which is not coupled to a particular cyclooxygenase isoenzyme, is essential for prostaglandin E(2) biosynthesis in vascular smooth muscle cells. J Thromb Haemost 5:1411–1419CrossRefPubMed
Zurück zum Zitat Carrasco E, Werner P, Casper D (2008) Prostaglandin receptor EP2 protects dopaminergic neurons against 6-OHDA-mediated low oxidative stress. Neurosci Lett 441:44–49CrossRefPubMedPubMedCentral Carrasco E, Werner P, Casper D (2008) Prostaglandin receptor EP2 protects dopaminergic neurons against 6-OHDA-mediated low oxidative stress. Neurosci Lett 441:44–49CrossRefPubMedPubMedCentral
Zurück zum Zitat Carrero I, Gonzalo MR, Martin B, Sanz-Anquela JM, Arevalo-Serrano J, Gonzalo-Ruiz A (2012) Oligomers of beta-amyloid protein (Aβ1-42) induce the activation of cyclooxygenase-2 in astrocytes via an interaction with interleukin-1beta, tumour necrosis factor-alpha, and a nuclear factor kappa-B mechanism in the rat brain. Experimental neurology 236(2): 215–227 Carrero I, Gonzalo MR, Martin B, Sanz-Anquela JM, Arevalo-Serrano J, Gonzalo-Ruiz A (2012) Oligomers of beta-amyloid protein (Aβ1-42) induce the activation of cyclooxygenase-2 in astrocytes via an interaction with interleukin-1beta, tumour necrosis factor-alpha, and a nuclear factor kappa-B mechanism in the rat brain. Experimental neurology 236(2): 215–227
Zurück zum Zitat Chauhan A, Chauhan V, Brown WT, Cohen I (2004) Oxidative stress in autism: increased lipid peroxidation and reduced serum levels of ceruloplasmin and transferrin—the antioxidant proteins. Life Sci 75:2539–2549CrossRefPubMed Chauhan A, Chauhan V, Brown WT, Cohen I (2004) Oxidative stress in autism: increased lipid peroxidation and reduced serum levels of ceruloplasmin and transferrin—the antioxidant proteins. Life Sci 75:2539–2549CrossRefPubMed
Zurück zum Zitat Chen C, Magee JC, Bazan NG (2002) Cyclooxygenase-2 regulates prostaglandin E2 signaling in hippocampal long-term synaptic plasticity. J Neurophysiol 87:2851–2857CrossRefPubMed Chen C, Magee JC, Bazan NG (2002) Cyclooxygenase-2 regulates prostaglandin E2 signaling in hippocampal long-term synaptic plasticity. J Neurophysiol 87:2851–2857CrossRefPubMed
Zurück zum Zitat Chez MG, Dowling T, Patel PB, Khanna P, Kominsky M (2007) Elevation of tumor necrosis factor alpha in CSF of autistic children. Pediatr Neurol 36:361–365CrossRefPubMed Chez MG, Dowling T, Patel PB, Khanna P, Kominsky M (2007) Elevation of tumor necrosis factor alpha in CSF of autistic children. Pediatr Neurol 36:361–365CrossRefPubMed
Zurück zum Zitat Constantino JN, Davis SA, Todd RD, Schindler MK, Gross MM, Brophy SL, Metzger LM, Shoushtari CS, Splinter R, Reich W (2003) Validation of a brief quantitative measure of autistic traits: comparison of the social responsiveness scale with the autism diagnostic interview-revised. J Autism Dev Disord 33:427–433CrossRefPubMed Constantino JN, Davis SA, Todd RD, Schindler MK, Gross MM, Brophy SL, Metzger LM, Shoushtari CS, Splinter R, Reich W (2003) Validation of a brief quantitative measure of autistic traits: comparison of the social responsiveness scale with the autism diagnostic interview-revised. J Autism Dev Disord 33:427–433CrossRefPubMed
Zurück zum Zitat Das UN (2013) Autism as a disorder of deficiency of brain-derived neurotrophic factor and altered metabolism of polyunsaturated fatty acids. Nutrition 29:1175–1185CrossRefPubMed Das UN (2013) Autism as a disorder of deficiency of brain-derived neurotrophic factor and altered metabolism of polyunsaturated fatty acids. Nutrition 29:1175–1185CrossRefPubMed
Zurück zum Zitat Dunn W (1999) Sensory profile manual. Psychological Corporation, San Antonio Dunn W (1999) Sensory profile manual. Psychological Corporation, San Antonio
Zurück zum Zitat Essa MM, Guillemin GJ, Waly MI, Al-Sharbati MM, Al-Farsi YM, Hakkim FL, Ali A, Al-Shafaee MS (2012) Increased markers of oxidative stress in autistic children of the Sultanate of Oman. Biol Trace Elem Res 147:25–27CrossRefPubMed Essa MM, Guillemin GJ, Waly MI, Al-Sharbati MM, Al-Farsi YM, Hakkim FL, Ali A, Al-Shafaee MS (2012) Increased markers of oxidative stress in autistic children of the Sultanate of Oman. Biol Trace Elem Res 147:25–27CrossRefPubMed
Zurück zum Zitat Foudi N, Louedec L, Cachina T, Brink C, Norel X (2009) Selective cyclooxygenase-2 inhibition directly increases human vascular reactivity to norepinephrine during acute inflammation. Cardiovasc Res 81:269–277CrossRefPubMed Foudi N, Louedec L, Cachina T, Brink C, Norel X (2009) Selective cyclooxygenase-2 inhibition directly increases human vascular reactivity to norepinephrine during acute inflammation. Cardiovasc Res 81:269–277CrossRefPubMed
Zurück zum Zitat Frustaci A, Neri M, Cesario A, Adams JB, Domenici E, Dalla Bernardina B, Bonassi S (2012) Oxidative stress-related biomarkers in autism: systematic review and meta-analyses. Free Radic Biol Med 52:2128–2141CrossRefPubMed Frustaci A, Neri M, Cesario A, Adams JB, Domenici E, Dalla Bernardina B, Bonassi S (2012) Oxidative stress-related biomarkers in autism: systematic review and meta-analyses. Free Radic Biol Med 52:2128–2141CrossRefPubMed
Zurück zum Zitat Goines PE, Ashwood P (2013) Cytokine dysregulation in autism spectrum disorders (ASD): possible role of the environment. Neurotoxicol Teratol 36:67–68CrossRefPubMed Goines PE, Ashwood P (2013) Cytokine dysregulation in autism spectrum disorders (ASD): possible role of the environment. Neurotoxicol Teratol 36:67–68CrossRefPubMed
Zurück zum Zitat Hein AM, Stutzman DL, Bland ST, Barrientos RM, Watkins LR, Rudy JW, Maier SF (2007) Prostaglandins are necessary and sufficient to induce contextual fear learning impairments after interleukin-1 beta injections into the dorsal hippocampus. Neuroscience 150:754–763CrossRefPubMedPubMedCentral Hein AM, Stutzman DL, Bland ST, Barrientos RM, Watkins LR, Rudy JW, Maier SF (2007) Prostaglandins are necessary and sufficient to induce contextual fear learning impairments after interleukin-1 beta injections into the dorsal hippocampus. Neuroscience 150:754–763CrossRefPubMedPubMedCentral
Zurück zum Zitat Innis SM (2000) The role of dietary n-6 and n-3 fatty acids in the developing brain. Dev Neurosci 22:474–480CrossRefPubMed Innis SM (2000) The role of dietary n-6 and n-3 fatty acids in the developing brain. Dev Neurosci 22:474–480CrossRefPubMed
Zurück zum Zitat Jenab S, Quinones-Jenab V (2002) The effects of interleukin-6, leukemia inhibitory factor and interferon-gamma on STAT DNA binding and c-fos mRNA levels in cortical astrocytes and C6 glioma cells. Neuro Endocrinol Lett 23:325–328PubMed Jenab S, Quinones-Jenab V (2002) The effects of interleukin-6, leukemia inhibitory factor and interferon-gamma on STAT DNA binding and c-fos mRNA levels in cortical astrocytes and C6 glioma cells. Neuro Endocrinol Lett 23:325–328PubMed
Zurück zum Zitat Kaufmann WE, Andreasson KI, Isakson PC, Worley PF (1997) Cyclooxygenases and the central nervous system. Prostaglandins 54:601–624CrossRefPubMed Kaufmann WE, Andreasson KI, Isakson PC, Worley PF (1997) Cyclooxygenases and the central nervous system. Prostaglandins 54:601–624CrossRefPubMed
Zurück zum Zitat Kawano T, Anrather J, Zhou P, Park L, Wang G, Frys KA, Kunz A, Cho S, Orio M, Iadecola C (2006) Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat Med 12:225–229CrossRefPubMed Kawano T, Anrather J, Zhou P, Park L, Wang G, Frys KA, Kunz A, Cho S, Orio M, Iadecola C (2006) Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat Med 12:225–229CrossRefPubMed
Zurück zum Zitat Kim T, Jae Kim H, Kyung Park J, Woo J, Ho Chung J (2010) Association between polymorphisms of arachidonate 12-lipoxygenase (ALOX12) and schizophrenia in a Korean population. Behav Brain Funct 6:44CrossRefPubMedPubMedCentral Kim T, Jae Kim H, Kyung Park J, Woo J, Ho Chung J (2010) Association between polymorphisms of arachidonate 12-lipoxygenase (ALOX12) and schizophrenia in a Korean population. Behav Brain Funct 6:44CrossRefPubMedPubMedCentral
Zurück zum Zitat King CR (2011) A novel embryological theory of autism causation involving endogenous biochemicals capable of initiating cellular gene transcription: a possible link between twelve autism risk factors and the autism 'epidemic'. Med Hypotheses 76:653–660CrossRefPubMed King CR (2011) A novel embryological theory of autism causation involving endogenous biochemicals capable of initiating cellular gene transcription: a possible link between twelve autism risk factors and the autism 'epidemic'. Med Hypotheses 76:653–660CrossRefPubMed
Zurück zum Zitat Kunz T, Oliw EH (2001) The selective cyclooxygenase-2 inhibitor rofecoxib reduces kainate-induced cell death in the rat hippocampus. Eur J Neurosci 13:569–575CrossRefPubMed Kunz T, Oliw EH (2001) The selective cyclooxygenase-2 inhibitor rofecoxib reduces kainate-induced cell death in the rat hippocampus. Eur J Neurosci 13:569–575CrossRefPubMed
Zurück zum Zitat Kuratko CN, Salem N Jr (2009) Biomarkers of DHA status. Prostaglandins Leukot Essent Fatty Acids 81:111–118CrossRefPubMed Kuratko CN, Salem N Jr (2009) Biomarkers of DHA status. Prostaglandins Leukot Essent Fatty Acids 81:111–118CrossRefPubMed
Zurück zum Zitat Kurumbail RG, Stevens AM, Gierse JK, McDonald JJ, Stegeman RA, Pak JY, Gildehaus D, Miyashiro JM, Penning TD, Seibert K, Isakson PC, Stallings WC (1996) Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature 384:644–648CrossRefPubMed Kurumbail RG, Stevens AM, Gierse JK, McDonald JJ, Stegeman RA, Pak JY, Gildehaus D, Miyashiro JM, Penning TD, Seibert K, Isakson PC, Stallings WC (1996) Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature 384:644–648CrossRefPubMed
Zurück zum Zitat Kwon DJ, Ju SM, Youn GS, Choi SY, Park J (2013) Suppression of iNOS and COX-2 expression by flavokawain A via blockade of NF-κB and AP-1 activation in RAW 264.7 macrophages. Food and chemical toxicology 58:479–486 Kwon DJ, Ju SM, Youn GS, Choi SY, Park J (2013) Suppression of iNOS and COX-2 expression by flavokawain A via blockade of NF-κB and AP-1 activation in RAW 264.7 macrophages. Food and chemical toxicology 58:479–486
Zurück zum Zitat Laflamme N, Lacroix S, Rivest S (1999) An essential role of interleukin-1beta in mediating NF-kappaB activity and COX-2 transcription in cells of the blood-brain barrier in response to a systemic and localized inflammation but not during endotoxemia. J Neurosci 19:10923–10930CrossRefPubMed Laflamme N, Lacroix S, Rivest S (1999) An essential role of interleukin-1beta in mediating NF-kappaB activity and COX-2 transcription in cells of the blood-brain barrier in response to a systemic and localized inflammation but not during endotoxemia. J Neurosci 19:10923–10930CrossRefPubMed
Zurück zum Zitat Lawrence G (2010) The fats of life: essential fatty acids in health and disease. Rutgers University Press, New Brunswick Lawrence G (2010) The fats of life: essential fatty acids in health and disease. Rutgers University Press, New Brunswick
Zurück zum Zitat Lee EO, Shin YJ, Chong YH (2004) Mechanisms involved in prostaglandin E2-mediated neuroprotection against TNF-alpha: possible involvement of multiple signal transduction and beta-catenin/T-cell factor. J Neuroimmunol 155:21–31CrossRefPubMed Lee EO, Shin YJ, Chong YH (2004) Mechanisms involved in prostaglandin E2-mediated neuroprotection against TNF-alpha: possible involvement of multiple signal transduction and beta-catenin/T-cell factor. J Neuroimmunol 155:21–31CrossRefPubMed
Zurück zum Zitat Li W, Xia J, Sun GY (1999) Cytokine induction of iNOS and sPLA2 in immortalized astrocytes (DITNC): response to genistein and pyrrolidine dithiocarbamate. J Interf Cytokine Res 19:121–127CrossRef Li W, Xia J, Sun GY (1999) Cytokine induction of iNOS and sPLA2 in immortalized astrocytes (DITNC): response to genistein and pyrrolidine dithiocarbamate. J Interf Cytokine Res 19:121–127CrossRef
Zurück zum Zitat Li X, Chauhan A, Sheikh AM, Patil S, Chauhan V, Li XM, Ji L, Brown T, Malik M (2009) Elevated immune response in the brain of autistic patients. J Neuroimmunol 207:111–116CrossRefPubMedPubMedCentral Li X, Chauhan A, Sheikh AM, Patil S, Chauhan V, Li XM, Ji L, Brown T, Malik M (2009) Elevated immune response in the brain of autistic patients. J Neuroimmunol 207:111–116CrossRefPubMedPubMedCentral
Zurück zum Zitat Liu D, Wu L, Breyer R, Mattson MP, Andreasson K (2005) Neuroprotection by the PGE2 EP2 receptor in permanent focal cerebral ischemia. Ann Neurol 57:758–761CrossRefPubMed Liu D, Wu L, Breyer R, Mattson MP, Andreasson K (2005) Neuroprotection by the PGE2 EP2 receptor in permanent focal cerebral ischemia. Ann Neurol 57:758–761CrossRefPubMed
Zurück zum Zitat Liu YQ, Hu XY, Lu T, Cheng YN, Young CY, Yuan HQ, Lou HX (2012) Retigeric acid B exhibits antitumor activity through suppression of nuclear factor-κB signaling in prostate cancer cells in vitro and in vivo. PloS one 7(5):e38000 Liu YQ, Hu XY, Lu T, Cheng YN, Young CY, Yuan HQ, Lou HX (2012) Retigeric acid B exhibits antitumor activity through suppression of nuclear factor-κB signaling in prostate cancer cells in vitro and in vivo. PloS one 7(5):e38000
Zurück zum Zitat Manna SK, Zhang HJ, Yan T, Oberley LW, Aggarwal BB (1998) Overexpression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of 10.1007/s11011-018-0206-6 nuclear transcription factor-κB and activated protein-1. Journal of Biological Chemistry, 273(21), 13245–13254 Manna SK, Zhang HJ, Yan T, Oberley LW, Aggarwal BB (1998) Overexpression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of 10.1007/s11011-018-0206-6 nuclear transcription factor-κB and activated protein-1. Journal of Biological Chemistry, 273(21), 13245–13254
Zurück zum Zitat Mark KS, Trickler WJ, Miller DW (2001) Tumor necrosis factor-alpha induces cyclooxygenase-2 expression and prostaglandin release in brain microvessel endothelial cells. J Pharmacol Exp Ther 297:1051–1058PubMed Mark KS, Trickler WJ, Miller DW (2001) Tumor necrosis factor-alpha induces cyclooxygenase-2 expression and prostaglandin release in brain microvessel endothelial cells. J Pharmacol Exp Ther 297:1051–1058PubMed
Zurück zum Zitat Marshall PJ, Kulmacz RJ, Lands WE (1987) Constraints on prostaglandin biosynthesis in tissues. J Biol Chem 262:3510–3517PubMed Marshall PJ, Kulmacz RJ, Lands WE (1987) Constraints on prostaglandin biosynthesis in tissues. J Biol Chem 262:3510–3517PubMed
Zurück zum Zitat Marusic S, Leach MW, Pelker JW, Azoitei ML, Uozumi N, Cui J, Shen MW, DeClercq CM, Miyashiro JS, Carito BA, Thakker P, Simmons DL, Leonard JP, Shimizu T, Clark JD (2005) Cytosolic phospholipase A2 alpha-deficient mice are resistant to experimental autoimmune encephalomyelitis. J Exp Med 202:841–851CrossRefPubMedPubMedCentral Marusic S, Leach MW, Pelker JW, Azoitei ML, Uozumi N, Cui J, Shen MW, DeClercq CM, Miyashiro JS, Carito BA, Thakker P, Simmons DL, Leonard JP, Shimizu T, Clark JD (2005) Cytosolic phospholipase A2 alpha-deficient mice are resistant to experimental autoimmune encephalomyelitis. J Exp Med 202:841–851CrossRefPubMedPubMedCentral
Zurück zum Zitat McCullough L, Wu L, Haughey N, Liang X, Hand T, Wang Q, Breyer RM, Andreasson K (2004) Neuroprotective function of the PGE2 EP2 receptor in cerebral ischemia. J Neurosci 24:257–268CrossRefPubMed McCullough L, Wu L, Haughey N, Liang X, Hand T, Wang Q, Breyer RM, Andreasson K (2004) Neuroprotective function of the PGE2 EP2 receptor in cerebral ischemia. J Neurosci 24:257–268CrossRefPubMed
Zurück zum Zitat Meguid NA, Dardir AA, Abdel-Raouf ER, Hashish A (2011) Evaluation of oxidative stress in autism: defective antioxidant enzymes and increased lipid peroxidation. Biol Trace Elem Res 143:58–65CrossRefPubMed Meguid NA, Dardir AA, Abdel-Raouf ER, Hashish A (2011) Evaluation of oxidative stress in autism: defective antioxidant enzymes and increased lipid peroxidation. Biol Trace Elem Res 143:58–65CrossRefPubMed
Zurück zum Zitat Mick K (2005) Diagnosing autism: comparison of the childhood autism rating scale (CARS) and the autism diagnostic observation schedule (ADOS). Dissertation, Wichita State University Mick K (2005) Diagnosing autism: comparison of the childhood autism rating scale (CARS) and the autism diagnostic observation schedule (ADOS). Dissertation, Wichita State University
Zurück zum Zitat Moolwaney AS, Igwe OJ (2005) Regulation of the cyclooxygenase-2 system by interleukin-1beta through mitogen-activated protein kinase signaling pathways: a comparative study of human neuroglioma and neuroblastoma cells. Brain Res Mol Brain Res 137:202–212CrossRefPubMed Moolwaney AS, Igwe OJ (2005) Regulation of the cyclooxygenase-2 system by interleukin-1beta through mitogen-activated protein kinase signaling pathways: a comparative study of human neuroglioma and neuroblastoma cells. Brain Res Mol Brain Res 137:202–212CrossRefPubMed
Zurück zum Zitat O'Banion MK, Miller JC, Chang JW, Kaplan MD, Coleman PD (1996) Interleukin-1 beta induces prostaglandin G/H synthase-2 (cyclooxygenase-2) in primary murine astrocyte cultures. J Neurochem 66:2532–2540CrossRefPubMed O'Banion MK, Miller JC, Chang JW, Kaplan MD, Coleman PD (1996) Interleukin-1 beta induces prostaglandin G/H synthase-2 (cyclooxygenase-2) in primary murine astrocyte cultures. J Neurochem 66:2532–2540CrossRefPubMed
Zurück zum Zitat Pooler AM, Arjona AA, Lee RK, Wurtman RJ (2004) Prostaglandin E2 regulates amyloid precursor protein expression via the EP2 receptor in cultured rat microglia. Neurosci Lett 362:127–130CrossRefPubMed Pooler AM, Arjona AA, Lee RK, Wurtman RJ (2004) Prostaglandin E2 regulates amyloid precursor protein expression via the EP2 receptor in cultured rat microglia. Neurosci Lett 362:127–130CrossRefPubMed
Zurück zum Zitat Pugh CR, Kumagawa K, Fleshner M, Watkins LR, Maier SF, Rudy JW (1998) Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain Behav Immun 12:212–229CrossRefPubMed Pugh CR, Kumagawa K, Fleshner M, Watkins LR, Maier SF, Rudy JW (1998) Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain Behav Immun 12:212–229CrossRefPubMed
Zurück zum Zitat Pun PB, Lu J, Moochhala S (2009) Involvement of ROS in BBB dysfunction. Free Radic Res 43:348–364CrossRefPubMed Pun PB, Lu J, Moochhala S (2009) Involvement of ROS in BBB dysfunction. Free Radic Res 43:348–364CrossRefPubMed
Zurück zum Zitat Richardson AJ (2004) Long-chain polyunsaturated fatty acids in childhood developmental and psychiatric disorders. Lipids 39:1215–1222CrossRefPubMed Richardson AJ (2004) Long-chain polyunsaturated fatty acids in childhood developmental and psychiatric disorders. Lipids 39:1215–1222CrossRefPubMed
Zurück zum Zitat Rossignol DA, Frye RE (2012) A review of research trends in physiological abnormalities in autism spectrum disorders: immune dysregulation, inflammation, oxidative stress, mitochondrial dysfunction and environmental toxicant exposures. Mol Psychiatry 17:389–401CrossRefPubMed Rossignol DA, Frye RE (2012) A review of research trends in physiological abnormalities in autism spectrum disorders: immune dysregulation, inflammation, oxidative stress, mitochondrial dysfunction and environmental toxicant exposures. Mol Psychiatry 17:389–401CrossRefPubMed
Zurück zum Zitat Samuelsson B, Morgenstern R, Jakobsson PJ (2007) Membrane prostaglandin E synthase-1: a novel therapeutic target. Pharmacol Rev 59:207–224CrossRefPubMed Samuelsson B, Morgenstern R, Jakobsson PJ (2007) Membrane prostaglandin E synthase-1: a novel therapeutic target. Pharmacol Rev 59:207–224CrossRefPubMed
Zurück zum Zitat Sang N, Zhang J, Marcheselli V, Bazan NG, Chen C (2005) Postsynaptically synthesized prostaglandin E2 (PGE2) modulates hippocampal synaptic transmission via a presynaptic PGE2 EP2 receptor. J Neurosci 25:9858–9870CrossRefPubMed Sang N, Zhang J, Marcheselli V, Bazan NG, Chen C (2005) Postsynaptically synthesized prostaglandin E2 (PGE2) modulates hippocampal synaptic transmission via a presynaptic PGE2 EP2 receptor. J Neurosci 25:9858–9870CrossRefPubMed
Zurück zum Zitat Sareddy GR, Geeviman K, Ramulu C, Babu PP (2012) The nonsteroidal anti-inflammatory drug celecoxib suppresses the growth and induces apoptosis of human glioblastoma cells via the NF-κB pathway. J Neuro-Oncol 106:99–109CrossRef Sareddy GR, Geeviman K, Ramulu C, Babu PP (2012) The nonsteroidal anti-inflammatory drug celecoxib suppresses the growth and induces apoptosis of human glioblastoma cells via the NF-κB pathway. J Neuro-Oncol 106:99–109CrossRef
Zurück zum Zitat Savonenko A, Munoz P, Melnikova T, Wang Q, Liang X, Breyer RM, Montine TJ, Kirkwood A, Andreasson K (2009) Impaired cognition, sensorimotor gating, and hippocampal long-term depression in mice lacking the prostaglandin E2 EP2 receptor. Exp Neurol 217:63–73CrossRefPubMedPubMedCentral Savonenko A, Munoz P, Melnikova T, Wang Q, Liang X, Breyer RM, Montine TJ, Kirkwood A, Andreasson K (2009) Impaired cognition, sensorimotor gating, and hippocampal long-term depression in mice lacking the prostaglandin E2 EP2 receptor. Exp Neurol 217:63–73CrossRefPubMedPubMedCentral
Zurück zum Zitat Schuchardt JP, Huss M, Stauss-Grabo M, Hahn A (2010) Significance of long-chain polyunsaturated fatty acids (PUFAs) for the development and behaviour of children. Eur J Pediatr 169:149–164CrossRefPubMed Schuchardt JP, Huss M, Stauss-Grabo M, Hahn A (2010) Significance of long-chain polyunsaturated fatty acids (PUFAs) for the development and behaviour of children. Eur J Pediatr 169:149–164CrossRefPubMed
Zurück zum Zitat Silver WG, Rapin I (2012) Neurobiological basis of autism. Pediatr Clin N Am 59:45–61CrossRef Silver WG, Rapin I (2012) Neurobiological basis of autism. Pediatr Clin N Am 59:45–61CrossRef
Zurück zum Zitat Simmons DL, Botting RM, Hla T (2004) Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 56:387–437CrossRefPubMed Simmons DL, Botting RM, Hla T (2004) Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 56:387–437CrossRefPubMed
Zurück zum Zitat Song C, Horrobin D (2004) Omega-3 fatty acid ethyl -eicosapentaenoate, but not soybean oil, attenuates memory impairment induced by central IL-1 beta administration. J Lipid Res 45:1112–1121CrossRefPubMed Song C, Horrobin D (2004) Omega-3 fatty acid ethyl -eicosapentaenoate, but not soybean oil, attenuates memory impairment induced by central IL-1 beta administration. J Lipid Res 45:1112–1121CrossRefPubMed
Zurück zum Zitat Sun Q, Ma J, Campos H, Hankinson SE, Hu FB (2007) Comparison between plasma and erythrocyte fatty acid content as biomarkers of fatty acid intake in US women. Am J Clin Nutr 86:74–81CrossRefPubMed Sun Q, Ma J, Campos H, Hankinson SE, Hu FB (2007) Comparison between plasma and erythrocyte fatty acid content as biomarkers of fatty acid intake in US women. Am J Clin Nutr 86:74–81CrossRefPubMed
Zurück zum Zitat Swiergiel AH, Dunn AJ (2002) Distinct roles for cyclooxygenases 1 and 2 in interleukin-1-induced behavioral changes. J Pharmacol Exp Ther 302:1031–1036CrossRefPubMed Swiergiel AH, Dunn AJ (2002) Distinct roles for cyclooxygenases 1 and 2 in interleukin-1-induced behavioral changes. J Pharmacol Exp Ther 302:1031–1036CrossRefPubMed
Zurück zum Zitat Tammali R, Ramana KV, Srivastava SK (2007) Aldose reductase regulates TNF-alpha-induced PGE2 production in human colon cancer cells. Cancer Lett 252:299–306CrossRefPubMedPubMedCentral Tammali R, Ramana KV, Srivastava SK (2007) Aldose reductase regulates TNF-alpha-induced PGE2 production in human colon cancer cells. Cancer Lett 252:299–306CrossRefPubMedPubMedCentral
Zurück zum Zitat Tassoni D, Kaur G, Weisinger RS, Sinclair AJ (2008) The role of eicosanoids in the brain. Asia Pac J Clin Nutr 17(Suppl 1):220–228PubMed Tassoni D, Kaur G, Weisinger RS, Sinclair AJ (2008) The role of eicosanoids in the brain. Asia Pac J Clin Nutr 17(Suppl 1):220–228PubMed
Zurück zum Zitat Tian J, Kim SF, Hester L, Snyder SH (2008) S-nitrosylation/activation of COX-2 mediates NMDA neurotoxicity. Proc Natl Acad Sci U S A 105:10537–10540CrossRefPubMedPubMedCentral Tian J, Kim SF, Hester L, Snyder SH (2008) S-nitrosylation/activation of COX-2 mediates NMDA neurotoxicity. Proc Natl Acad Sci U S A 105:10537–10540CrossRefPubMedPubMedCentral
Zurück zum Zitat Uozumi N, Kume K, Nagase T, Nakatani N, Ishii S, Tashiro F, Komagata Y, Maki K, Ikuta K, Ouchi Y, Miyazaki J, Shimizu T (1997) Role of cytosolic phospholipase A2 in allergic response and parturition. Nature 390:618–622CrossRefPubMed Uozumi N, Kume K, Nagase T, Nakatani N, Ishii S, Tashiro F, Komagata Y, Maki K, Ikuta K, Ouchi Y, Miyazaki J, Shimizu T (1997) Role of cytosolic phospholipase A2 in allergic response and parturition. Nature 390:618–622CrossRefPubMed
Zurück zum Zitat Uracz W, Uracz D, Olszanecki R, Gryglewski RJ (2002) Interleukin 1beta induces functional prostaglandin E synthase in cultured human umbilical vein endothelial cells. J Physiol Pharmacol 53:643–654PubMed Uracz W, Uracz D, Olszanecki R, Gryglewski RJ (2002) Interleukin 1beta induces functional prostaglandin E synthase in cultured human umbilical vein endothelial cells. J Physiol Pharmacol 53:643–654PubMed
Zurück zum Zitat Vancassel S, Durand G, Barthélémy C, Lejeune B, Martineau J, Guilloteau D, Andrès C, Chalon S (2001) Plasma fatty acid levels in autistic children. Prostaglandins Leukot Essent Fatty Acids 65:1–7CrossRefPubMed Vancassel S, Durand G, Barthélémy C, Lejeune B, Martineau J, Guilloteau D, Andrès C, Chalon S (2001) Plasma fatty acid levels in autistic children. Prostaglandins Leukot Essent Fatty Acids 65:1–7CrossRefPubMed
Zurück zum Zitat Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA (2005) Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 57:67–81CrossRefPubMed Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA (2005) Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 57:67–81CrossRefPubMed
Zurück zum Zitat Verhoeven JS, De Cock P, Lagae L, Sunaert S (2010) Neuroimaging of autism. Neuroradiology 52:3–14CrossRefPubMed Verhoeven JS, De Cock P, Lagae L, Sunaert S (2010) Neuroimaging of autism. Neuroradiology 52:3–14CrossRefPubMed
Zurück zum Zitat Vila L (2004) Cyclooxygenase and 5-lipoxygenase pathways in the vessel wall: role in atherosclerosis. Med Res Rev 24:399–424CrossRefPubMed Vila L (2004) Cyclooxygenase and 5-lipoxygenase pathways in the vessel wall: role in atherosclerosis. Med Res Rev 24:399–424CrossRefPubMed
Zurück zum Zitat Wallace JL (2001) Prostaglandin biology in inflammatory bowel disease. Gastroenterol Clin N Am 30:971–980CrossRef Wallace JL (2001) Prostaglandin biology in inflammatory bowel disease. Gastroenterol Clin N Am 30:971–980CrossRef
Zurück zum Zitat Wang F, Wu H, Xu S, Guo X, Yang J, Shen X (2011) Macrophage migration inhibitory factor activates cyclooxygenase 2-prostaglandin E2 in cultured spinal microglia. Neurosci Res 71:210–218CrossRefPubMed Wang F, Wu H, Xu S, Guo X, Yang J, Shen X (2011) Macrophage migration inhibitory factor activates cyclooxygenase 2-prostaglandin E2 in cultured spinal microglia. Neurosci Res 71:210–218CrossRefPubMed
Zurück zum Zitat Warner TD, Vojnovic I, Giuliano F, Jiménez R, Bishop-Bailey D, Mitchell JA (2004) Cyclooxygenases 1, 2, and 3 and the production of prostaglandin I2: investigating the activities of acetaminophen and cyclooxygenase-2-selective inhibitors in rat tissues. J Pharmacol Exp Ther 310:642–647CrossRefPubMed Warner TD, Vojnovic I, Giuliano F, Jiménez R, Bishop-Bailey D, Mitchell JA (2004) Cyclooxygenases 1, 2, and 3 and the production of prostaglandin I2: investigating the activities of acetaminophen and cyclooxygenase-2-selective inhibitors in rat tissues. J Pharmacol Exp Ther 310:642–647CrossRefPubMed
Zurück zum Zitat World Medical Association (2000) World Medical Association declaration of Helsinki: ethical principles for medical research involving human subjects. Edinburgh, Canary Publications World Medical Association (2000) World Medical Association declaration of Helsinki: ethical principles for medical research involving human subjects. Edinburgh, Canary Publications
Zurück zum Zitat Xu J, Yu S, Sun AY, Sun GY (2003) Oxidant-mediated AA release from astrocytes involves cPLA(2) and iPLA(2). Free Radic Biol Med 34:1531–1543CrossRefPubMed Xu J, Yu S, Sun AY, Sun GY (2003) Oxidant-mediated AA release from astrocytes involves cPLA(2) and iPLA(2). Free Radic Biol Med 34:1531–1543CrossRefPubMed
Zurück zum Zitat Yamagata K, Andreasson KI, Kaufmann WE, Barnes CA, Worley PF (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11:371–786CrossRefPubMed Yamagata K, Andreasson KI, Kaufmann WE, Barnes CA, Worley PF (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11:371–786CrossRefPubMed
Zurück zum Zitat Yang H, Zhang J, Breyer RM, Chen C (2009) Altered hippocampal long-term synaptic plasticity in mice deficient in the PGE2 EP2 receptor. J Neurochem 108:295–304CrossRefPubMed Yang H, Zhang J, Breyer RM, Chen C (2009) Altered hippocampal long-term synaptic plasticity in mice deficient in the PGE2 EP2 receptor. J Neurochem 108:295–304CrossRefPubMed
Zurück zum Zitat Yoo HJ, Kim H-W, Cho IH, Kim SA, Park M, Kim JW (2008) Are the behavioural phenotypes different according to the genotype of iNOS and COX-2 genes in autism spectrum disorders? Int. J. Devl. Neuroscience 26:867–892 Yoo HJ, Kim H-W, Cho IH, Kim SA, Park M, Kim JW (2008) Are the behavioural phenotypes different according to the genotype of iNOS and COX-2 genes in autism spectrum disorders? Int. J. Devl. Neuroscience 26:867–892
Zurück zum Zitat Zonta M, Sebelin A, Gobbo S, Fellin T, Pozzan T, Carmignoto G (2003) Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes. J Physiol 553:407–414CrossRefPubMedPubMedCentral Zonta M, Sebelin A, Gobbo S, Fellin T, Pozzan T, Carmignoto G (2003) Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes. J Physiol 553:407–414CrossRefPubMedPubMedCentral
Metadaten
Titel
Impaired lipid metabolism markers to assess the risk of neuroinflammation in autism spectrum disorder
verfasst von
Hanan Qasem
Laila Al-Ayadhi
Geir Bjørklund
Salvatore Chirumbolo
Afaf El-Ansary
Publikationsdatum
22.03.2018
Verlag
Springer US
Erschienen in
Metabolic Brain Disease / Ausgabe 4/2018
Print ISSN: 0885-7490
Elektronische ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-018-0206-6

Weitere Artikel der Ausgabe 4/2018

Metabolic Brain Disease 4/2018 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.