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Erschienen in: Journal of Neural Transmission 5-6/2022

28.05.2022 | Psychiatry and Preclinical Psychiatric Studies - Review Article

Modelling the neurodevelopmental pathogenesis in neuropsychiatric disorders. Bioactive kynurenines and their analogues as neuroprotective agents—in celebration of 80th birthday of Professor Peter Riederer

verfasst von: Masaru Tanaka, Eleonóra Spekker, Ágnes Szabó, Helga Polyák, László Vécsei

Erschienen in: Journal of Neural Transmission | Ausgabe 5-6/2022

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Abstract

Following introduction of the monoamine oxidase type B inhibitor selegiline for the treatment of Parkinson’s disease (PD), discovery of the action mechanism of Alzheimer’s disease-modifying agent memantine, the role of iron in PD, and the loss of electron transport chain complex I in PD, and development of the concept of clinical neuroprotection, Peter Riederer launched one of the most challenging research project neurodevelopmental aspects of neuropsychiatric disorders. The neurodevelopmental theory holds that a disruption of normal brain development in utero or during early life underlies the subsequent emergence of neuropsychiatric symptoms during later life. Indeed, the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition and the International Classification of Diseases, 11th Revision categorize autism spectrum disorder and attention deficit hyperactivity disorder in neurodevelopmental disorders (NDDs). More and more evidence, especially from preclinical studies, is revealing that neurodevelopmental pathology is not limited to the diagnostic class above, but also contributes to the development of other psychiatric disorders such as schizophrenia, bipolar disorder, and obsessive–compulsive disorder as well as neurodegenerative diseases such as PD and Huntington’s disease. Preclinical animal research is taking a lead in understanding the pathomechanisms of NDDs, searching for novel targets, and developing new neuroprotective agents against NDDs. This narrative review discusses emerging evidence of the neurodevelopmental etiology of neuropsychiatric disorders, recent advances in modelling neurodevelopmental pathogenesis, potential strategies of clinical neuroprotection using novel kynurenine metabolites and analogues, and future research direction for NDDs.
Literatur
Zurück zum Zitat Asperger H (1944) Die „Autistischen psychopathen” im kindesalter. Arch Psychiatr Nervenkr 117(1):76–136CrossRef Asperger H (1944) Die „Autistischen psychopathen” im kindesalter. Arch Psychiatr Nervenkr 117(1):76–136CrossRef
Zurück zum Zitat Balog A, Varga B, Fülöp F, Lantos I, Toldi G, Vécsei L, Mándi Y (2021) Kynurenic Acid analog attenuates the production of tumor necrosis factor-α, calgranulins (S100A 8/9 and S100A 12), and the secretion of HNP1-3 and stimulates the production of tumor necrosis factor-stimulated gene-6 in whole blood cultures of patients with rheumatoid arthritis. Front Immunol 12:632513. https://doi.org/10.3389/fimmu.2021.632513CrossRefPubMedPubMedCentral Balog A, Varga B, Fülöp F, Lantos I, Toldi G, Vécsei L, Mándi Y (2021) Kynurenic Acid analog attenuates the production of tumor necrosis factor-α, calgranulins (S100A 8/9 and S100A 12), and the secretion of HNP1-3 and stimulates the production of tumor necrosis factor-stimulated gene-6 in whole blood cultures of patients with rheumatoid arthritis. Front Immunol 12:632513. https://​doi.​org/​10.​3389/​fimmu.​2021.​632513CrossRefPubMedPubMedCentral
Zurück zum Zitat Battaglia S, Thayer JF (2022) Functional interplay between central and autonomic nervous systems in human fear conditioning. Trends in Neurosciences, in press Battaglia S, Thayer JF (2022) Functional interplay between central and autonomic nervous systems in human fear conditioning. Trends in Neurosciences, in press
Zurück zum Zitat Becker LE, Narayan O, Johnson RT (1974) Comparative studies of viral infections of the developing forebrain. J Neuropathol Exp Neurol 23(4):519–529CrossRef Becker LE, Narayan O, Johnson RT (1974) Comparative studies of viral infections of the developing forebrain. J Neuropathol Exp Neurol 23(4):519–529CrossRef
Zurück zum Zitat Blum K, Gondré-Lewis MC, Modestino EJ, Lott L, Baron D, Siwicki D, McLaughlin T, Howeedy A, Krengel MH, Oscar-Berman M, Thanos PK, Elman I, Hauser M, Fried L, Bowirrat A, Badgaiyan RD (2019) Understanding the scientific basis of post-traumatic stress disorder (PTSD): precision behavioral management overrides stigmatization. Mol Neurobiol 56(11):7836–7850. https://doi.org/10.1007/s12035-019-1600-8CrossRefPubMedPubMedCentral Blum K, Gondré-Lewis MC, Modestino EJ, Lott L, Baron D, Siwicki D, McLaughlin T, Howeedy A, Krengel MH, Oscar-Berman M, Thanos PK, Elman I, Hauser M, Fried L, Bowirrat A, Badgaiyan RD (2019) Understanding the scientific basis of post-traumatic stress disorder (PTSD): precision behavioral management overrides stigmatization. Mol Neurobiol 56(11):7836–7850. https://​doi.​org/​10.​1007/​s12035-019-1600-8CrossRefPubMedPubMedCentral
Zurück zum Zitat Borgomaneri S, Serio G, Battaglia S (2020b) Please, don’t do it! Fifteen years of progress of non-invasive brain stimulation in action inhibition. Cortex 132:404–422CrossRef Borgomaneri S, Serio G, Battaglia S (2020b) Please, don’t do it! Fifteen years of progress of non-invasive brain stimulation in action inhibition. Cortex 132:404–422CrossRef
Zurück zum Zitat Bowirrat A, Chen TJ, Blum K, Madigan M, Bailey JA, Chuan Chen AL, Downs BW, Braverman ER, Radi S, Waite RL, Kerner M, Giordano J, Morse S, Oscar-Berman M, Gold M (2010) Neuro-psychopharmacogenetics and neurological antecedents of posttraumatic stress disorder: unlocking the mysteries of resilience and vulnerability. Curr Neuropharmacol 8(4):335–358. https://doi.org/10.2174/157015910793358123CrossRefPubMedPubMedCentral Bowirrat A, Chen TJ, Blum K, Madigan M, Bailey JA, Chuan Chen AL, Downs BW, Braverman ER, Radi S, Waite RL, Kerner M, Giordano J, Morse S, Oscar-Berman M, Gold M (2010) Neuro-psychopharmacogenetics and neurological antecedents of posttraumatic stress disorder: unlocking the mysteries of resilience and vulnerability. Curr Neuropharmacol 8(4):335–358. https://​doi.​org/​10.​2174/​1570159107933581​23CrossRefPubMedPubMedCentral
Zurück zum Zitat Demeter I, Nagy K, Gellért L, Vécsei L, Fülöp F, Toldi J (2012) A novel kynurenic acid analog (SZR104) inhibits pentylenetetrazole-induced epileptiform seizures. An electrophysiological study: special issue related to kynurenine. J Neural Transmiss 119(2), 151–154. https://doi.org/10.1007/s00702-011-0755-x Demeter I, Nagy K, Gellért L, Vécsei L, Fülöp F, Toldi J (2012) A novel kynurenic acid analog (SZR104) inhibits pentylenetetrazole-induced epileptiform seizures. An electrophysiological study: special issue related to kynurenine. J Neural Transmiss 119(2), 151–154. https://​doi.​org/​10.​1007/​s00702-011-0755-x
Zurück zum Zitat Esquirol E (1838) Des maladies mentales. Paris, France: Baillière; 1838 Esquirol E (1838) Des maladies mentales. Paris, France: Baillière; 1838
Zurück zum Zitat Georget EJ (1820) De la folie. Considérations sur cette maladie. Paris, France: Crévot; p. 102. Georget EJ (1820) De la folie. Considérations sur cette maladie. Paris, France: Crévot; p. 102.
Zurück zum Zitat Hsu YL, Hung HS, Tsai CW, Liu SP, Chiang YT, Kuo YH, Shyu WC, Lin SZ, Fu RH (2021) Peiminine reduces ARTS-mediated degradation of XIAP by modulating the PINK1/parkin pathway to ameliorate 6-hydroxydopamine toxicity and α-synuclein accumulation in Parkinson’s disease models in vivo and in vitro. Int J Mol Sci 22(19):10240. https://doi.org/10.3390/ijms221910240CrossRefPubMedPubMedCentral Hsu YL, Hung HS, Tsai CW, Liu SP, Chiang YT, Kuo YH, Shyu WC, Lin SZ, Fu RH (2021) Peiminine reduces ARTS-mediated degradation of XIAP by modulating the PINK1/parkin pathway to ameliorate 6-hydroxydopamine toxicity and α-synuclein accumulation in Parkinson’s disease models in vivo and in vitro. Int J Mol Sci 22(19):10240. https://​doi.​org/​10.​3390/​ijms221910240CrossRefPubMedPubMedCentral
Zurück zum Zitat Kanner L (1943) Autistic disturbances of affective contact. Nervous Child 2:217–250 Kanner L (1943) Autistic disturbances of affective contact. Nervous Child 2:217–250
Zurück zum Zitat Knyihar-Csillik E, Mihaly A, Krisztin-Peva B, Robotka H, Szatmari I, Fulop F, Toldi J, Csillik B, Vecsei L (2008) The kynurenate analog SZR-72 prevents the nitroglycerol-induced increase of c-fos immunoreactivity in the rat caudal trigeminal nucleus: comparative studies of the effects of SZR-72 and kynurenic acid. Neurosci Res 61(4):429–432. https://doi.org/10.1016/j.neures.2008.04.009CrossRefPubMed Knyihar-Csillik E, Mihaly A, Krisztin-Peva B, Robotka H, Szatmari I, Fulop F, Toldi J, Csillik B, Vecsei L (2008) The kynurenate analog SZR-72 prevents the nitroglycerol-induced increase of c-fos immunoreactivity in the rat caudal trigeminal nucleus: comparative studies of the effects of SZR-72 and kynurenic acid. Neurosci Res 61(4):429–432. https://​doi.​org/​10.​1016/​j.​neures.​2008.​04.​009CrossRefPubMed
Zurück zum Zitat Lajkó N, Kata D, Szabó M, Mátyás A, Dulka K, Földesi I, Fülöp F, Gulya K, Vécsei L, Mihály A (2020) Sensitivity of rodent microglia to kynurenines in models of epilepsy and inflammation in vivo and in vitro: microglia activation is inhibited by kynurenic acid and the synthetic analogue SZR104. Int J Mol Sci 21(23):9333. https://doi.org/10.3390/ijms21239333CrossRefPubMedCentral Lajkó N, Kata D, Szabó M, Mátyás A, Dulka K, Földesi I, Fülöp F, Gulya K, Vécsei L, Mihály A (2020) Sensitivity of rodent microglia to kynurenines in models of epilepsy and inflammation in vivo and in vitro: microglia activation is inhibited by kynurenic acid and the synthetic analogue SZR104. Int J Mol Sci 21(23):9333. https://​doi.​org/​10.​3390/​ijms21239333CrossRefPubMedCentral
Zurück zum Zitat Langdon J, Down H (1862) On the condition of the mouth in idiocy. The Lancet Langdon J, Down H (1862) On the condition of the mouth in idiocy. The Lancet
Zurück zum Zitat Lejeune J, Gauthier M, Turpin R (1959) Les chromosomes humains en culture de tissus [The human chromosomes in tissue culture]. C R Hebd Seances Acad Sci 248:602–603PubMed Lejeune J, Gauthier M, Turpin R (1959) Les chromosomes humains en culture de tissus [The human chromosomes in tissue culture]. C R Hebd Seances Acad Sci 248:602–603PubMed
Zurück zum Zitat Liu XC, Holtze M, Powell SB, Terrando N, Larsson MK, Persson A, Olsson SK, Orhan F, Kegel M, Asp L, Goiny M, Schwieler L, Engberg G, Karlsson H, Erhardt S (2014) Behavioral disturbances in adult mice following neonatal virus infection or kynurenine treatment–role of brain kynurenic acid. Brain Behav Immun 36:80–89. https://doi.org/10.1016/j.bbi.2013.10.010CrossRefPubMed Liu XC, Holtze M, Powell SB, Terrando N, Larsson MK, Persson A, Olsson SK, Orhan F, Kegel M, Asp L, Goiny M, Schwieler L, Engberg G, Karlsson H, Erhardt S (2014) Behavioral disturbances in adult mice following neonatal virus infection or kynurenine treatment–role of brain kynurenic acid. Brain Behav Immun 36:80–89. https://​doi.​org/​10.​1016/​j.​bbi.​2013.​10.​010CrossRefPubMed
Zurück zum Zitat Marosi M, Nagy D, Farkas T, Kis Z, Rózsa E, Robotka H, Fülöp F, Vécsei L, Toldi J (2010) A novel kynurenic acid analogue: a comparison with kynurenic acid. An in vitro electrophysiological study. Journal of neural transmission (Vienna, Austria: 1996), 117(2), 183–188. https://doi.org/10.1007/s00702-009-0346-2 Marosi M, Nagy D, Farkas T, Kis Z, Rózsa E, Robotka H, Fülöp F, Vécsei L, Toldi J (2010) A novel kynurenic acid analogue: a comparison with kynurenic acid. An in vitro electrophysiological study. Journal of neural transmission (Vienna, Austria: 1996), 117(2), 183–188. https://​doi.​org/​10.​1007/​s00702-009-0346-2
Zurück zum Zitat Ramírez Ortega D, Ugalde Muñiz PE, Blanco Ayala T, Vázquez Cervantes GI, Lugo Huitrón R, Pineda B, González Esquivel DF, Pérez de la Cruz G, Pedraza Chaverrí J, Sánchez Chapul L, Gómez-Manzo S, Pérez de la Cruz V (2021) On the antioxidant properties of L-kynurenine: an efficient ROS scavenger and enhancer of rat brain antioxidant defense. Antioxidants (basel, Switzerland) 11(1):31. https://doi.org/10.3390/antiox11010031CrossRef Ramírez Ortega D, Ugalde Muñiz PE, Blanco Ayala T, Vázquez Cervantes GI, Lugo Huitrón R, Pineda B, González Esquivel DF, Pérez de la Cruz G, Pedraza Chaverrí J, Sánchez Chapul L, Gómez-Manzo S, Pérez de la Cruz V (2021) On the antioxidant properties of L-kynurenine: an efficient ROS scavenger and enhancer of rat brain antioxidant defense. Antioxidants (basel, Switzerland) 11(1):31. https://​doi.​org/​10.​3390/​antiox11010031CrossRef
Zurück zum Zitat Scandurra V, Emberti Gialloreti L, Barbanera F, Scordo MR, Pierini A, Canitano R (2019) Neurodevelopmental disorders and adaptive functions: a study of children with autism spectrum disorders (ASD) and/or attention deficit and hyperactivity disorder (ADHD). Front Psych 10:673. https://doi.org/10.3389/fpsyt.2019.00673CrossRef Scandurra V, Emberti Gialloreti L, Barbanera F, Scordo MR, Pierini A, Canitano R (2019) Neurodevelopmental disorders and adaptive functions: a study of children with autism spectrum disorders (ASD) and/or attention deficit and hyperactivity disorder (ADHD). Front Psych 10:673. https://​doi.​org/​10.​3389/​fpsyt.​2019.​00673CrossRef
Zurück zum Zitat Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S, Brynjolfsson J, Gunnarsdottir S, Ivarsson O, Chou TT, Hjaltason O, Birgisdottir B, Jonsson H, Gudnadottir VG, Gudmundsdottir E, Bjornsson A, Ingvarsson B, Ingason A, Sigfusson S, Hardardottir H, Stefansson K (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 71(4):877–892. https://doi.org/10.1086/342734CrossRefPubMedPubMedCentral Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S, Brynjolfsson J, Gunnarsdottir S, Ivarsson O, Chou TT, Hjaltason O, Birgisdottir B, Jonsson H, Gudnadottir VG, Gudmundsdottir E, Bjornsson A, Ingvarsson B, Ingason A, Sigfusson S, Hardardottir H, Stefansson K (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 71(4):877–892. https://​doi.​org/​10.​1086/​342734CrossRefPubMedPubMedCentral
Zurück zum Zitat Sumitomo A, Horike K, Hirai K, Butcher N, Boot E, Sakurai T, Nucifora FC, Bassett AS, Sawa A, Tomoda T (2018) A mouse model of 22q11.2 deletions: Molecular and behavioral signatures of Parkinson's disease and schizophrenia. Sci Adv 4(8): eaar6637. https://doi.org/10.1126/sciadv.aar6637 Sumitomo A, Horike K, Hirai K, Butcher N, Boot E, Sakurai T, Nucifora FC, Bassett AS, Sawa A, Tomoda T (2018) A mouse model of 22q11.2 deletions: Molecular and behavioral signatures of Parkinson's disease and schizophrenia. Sci Adv 4(8): eaar6637. https://​doi.​org/​10.​1126/​sciadv.​aar6637
Zurück zum Zitat Tanaka M, Szabó A, Lőrinczi B, Szatmári I, Fülö, F, Vécsei, L (2021a) Antidepressant-like Effects of Kynurenic Acid Analogues, in Proceedings of the 1st International Electronic Conference on Biomedicine, 1–26 June, MDPI: Basel, Switzerland, https://doi.org/10.3390/ECB2021a-10301 Tanaka M, Szabó A, Lőrinczi B, Szatmári I, Fülö, F, Vécsei, L (2021a) Antidepressant-like Effects of Kynurenic Acid Analogues, in Proceedings of the 1st International Electronic Conference on Biomedicine, 1–26 June, MDPI: Basel, Switzerland, https://​doi.​org/​10.​3390/​ECB2021a-10301
Zurück zum Zitat Thapar A, Rutter M (2015) Neurodevelopmental disorders. In: Thapar A, Pine DS, Leckman JF, Scott S, Snowling MJ, Taylor E, editors. Rutter’s child and adolescent psychiatry. 6th ed. Oxford: Wiley Blackwell; 2015 Thapar A, Rutter M (2015) Neurodevelopmental disorders. In: Thapar A, Pine DS, Leckman JF, Scott S, Snowling MJ, Taylor E, editors. Rutter’s child and adolescent psychiatry. 6th ed. Oxford: Wiley Blackwell; 2015
Zurück zum Zitat Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, González-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks WP, Latchman DS, Harvey RJ, Dallapiccola B, Wood NW (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science (New York, N.Y.), 304(5674), 1158–1160. https://doi.org/10.1126/science.1096284 Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, González-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks WP, Latchman DS, Harvey RJ, Dallapiccola B, Wood NW (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science (New York, N.Y.), 304(5674), 1158–1160. https://​doi.​org/​10.​1126/​science.​1096284
Zurück zum Zitat Widhalm S (1985) Current status of conservative therapy of extrapyramidal movement disorders in childhood and adolescence. Wien Med Wochenschr Suppl 88:1–23PubMed Widhalm S (1985) Current status of conservative therapy of extrapyramidal movement disorders in childhood and adolescence. Wien Med Wochenschr Suppl 88:1–23PubMed
Zurück zum Zitat Wulansari N, Darsono W, Woo H J, Chang MY, Kim J, Bae EJ, Sun W, Lee JH, Cho IJ, Shin H, Lee SJ, Lee SH (2021) Neurodevelopmental defects and neurodegenerative phenotypes in human brain organoids carrying Parkinson's disease-linked DNAJC6 mutations. Sci Adv 7(8), eabb1540. https://doi.org/10.1126/sciadv.abb1540 Wulansari N, Darsono W, Woo H J, Chang MY, Kim J, Bae EJ, Sun W, Lee JH, Cho IJ, Shin H, Lee SJ, Lee SH (2021) Neurodevelopmental defects and neurodegenerative phenotypes in human brain organoids carrying Parkinson's disease-linked DNAJC6 mutations. Sci Adv 7(8), eabb1540. https://​doi.​org/​10.​1126/​sciadv.​abb1540
Zurück zum Zitat Zádori D, Nyiri G, Szonyi A, Szatmári I, Fülöp F, Toldi J, Freund TF, Vécsei L, Klivényi P (2011) Neuroprotective effects of a novel kynurenic acid analogue in a transgenic mouse model of Huntington’s disease. J Neural Transmis (vienna, Austria: 1996) 118(6):865–875. https://doi.org/10.1007/s00702-010-0573-6CrossRef Zádori D, Nyiri G, Szonyi A, Szatmári I, Fülöp F, Toldi J, Freund TF, Vécsei L, Klivényi P (2011) Neuroprotective effects of a novel kynurenic acid analogue in a transgenic mouse model of Huntington’s disease. J Neural Transmis (vienna, Austria: 1996) 118(6):865–875. https://​doi.​org/​10.​1007/​s00702-010-0573-6CrossRef
Metadaten
Titel
Modelling the neurodevelopmental pathogenesis in neuropsychiatric disorders. Bioactive kynurenines and their analogues as neuroprotective agents—in celebration of 80th birthday of Professor Peter Riederer
verfasst von
Masaru Tanaka
Eleonóra Spekker
Ágnes Szabó
Helga Polyák
László Vécsei
Publikationsdatum
28.05.2022
Verlag
Springer Vienna
Erschienen in
Journal of Neural Transmission / Ausgabe 5-6/2022
Print ISSN: 0300-9564
Elektronische ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-022-02513-5

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