Expanding the phenotype of Brunner syndrome from childhood to adulthood: Description of the second pediatric patient and his mother.

Brunner syndrome MAO-A deficiency intellectual disability neurodevelopmental disorder

Journal

American journal of medical genetics. Part A
ISSN: 1552-4833
Titre abrégé: Am J Med Genet A
Pays: United States
ID NLM: 101235741

Informations de publication

Date de publication:
26 Sep 2023
Historique:
revised: 02 08 2023
received: 09 03 2023
accepted: 08 09 2023
medline: 26 9 2023
pubmed: 26 9 2023
entrez: 26 9 2023
Statut: aheadofprint

Résumé

Brunner syndrome is a recessive X-linked disorder caused by pathogenic variants in the monoamine oxidase A gene (MAOA). It is characterized by distinctive aggressive behavior, mild intellectual disability, sleep disturbances, and typical biochemical alterations deriving from the impaired monoamine metabolism. We herein describe a 5-year-old boy with developmental delay, autistic features, and myoclonic epilepsy, and his mother, who had mild intellectual disability and recurrent episodes of palpitations, headache, abdominal pain, and abdominal bloating. Whole exome sequencing allowed detection of the maternally-inherited variant c.410A>G, (p.Glu137Gly) in the MAOA gene. The subsequent biochemical studies confirmed the MAOA deficiency both in the child and his mother. Given the serotonergic symptoms associated with high serotonin levels found in the mother, treatment with a serotonin reuptake inhibitor and dietary modifications were carried out, resulting in regression of the biochemical abnormalities and partial reduction of symptoms. Our report expands the phenotypic spectrum of Brunner disease, bringing new perspectives on the behavioral and neurodevelopmental phenotype from childhood to adulthood.

Identifiants

pubmed: 37750385
doi: 10.1002/ajmg.a.63413
doi:

Types de publication

Case Reports

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Italian Health Ministry
ID : RC 2022

Informations de copyright

© 2023 Wiley Periodicals LLC.

Références

Beikmann, B. S., Tomlinson, I. D., Rosenthal, S. J., & Andrews, A. M. (2013). Serotonin uptake is largely mediated by platelets versus lymphocytes in peripheral blood cells. ACS Chemical Neuroscience, 4(1), 161-170. https://doi.org/10.1021/cn300146w
Bortolato, M., Chen, K., & Shih, J. C. (2008). Monoamine oxidase inactivation: From pathophysiology to therapeutics. Advanced Drug Delivery Reviews, 60(13-14), 1527-1533. https://doi.org/10.1016/j.addr.2008.06.002
Bortolato, M., Floris, G., & Shih, J. C. (2018). From aggression to autism: New perspectives on the behavioral sequelae of monoamine oxidase deficiency. Journal of Neural Transmission (Vienna), 125(11), 1589-1599. https://doi.org/10.1007/s00702-018-1888-y
Brunner, H. G., Nelen, M., Breakefield, X. O., Ropers, H. H., & van Oost, B. A. (1993). Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science, 262(5133), 578-580. https://doi.org/10.1126/science.8211186
Brunner, H. G., Nelen, M. R., van Zandvoort, P., Abeling, N. G., van Gennip, A. H., Wolters, E. C., Kuiper, M. A., Ropers, H. H., & van Oost, B. A. (1993). X-linked borderline mental retardation with prominent behavioral disturbance: Phenotype, genetic localization, and evidence for disturbed monoamine metabolism. American Journal of Human Genetics, 52(6), 1032-1039.
Cases, O., Seif, I., Grimsby, J., Gaspar, P., Chen, K., Pournin, S., Muller, U., Aguet, M., Babinet, C., & Shih, J. C. (1995). Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science, 268(5218), 1763-1766. https://doi.org/10.1126/science.7792602
Chen, K., Holschneider, D. P., Wu, W., Rebrin, I., & Shih, J. C. (2004). A spontaneous point mutation produces monoamine oxidase A/B knock-out mice with greatly elevated monoamines and anxiety-like behavior. The Journal of Biological Chemistry, 279(38), 39645-39652. https://doi.org/10.1074/jbc.M405550200
Chen, Z. Y., Hotamisligil, G. S., Huang, J. K., Wen, L., Ezzeddine, D., Aydin-Muderrisoglu, N., Powell, J. F., Huang, R. H., Breakefield, X. O., Craig, I., & Hsu, Y. P. P. (1991). Structure of the human gene for monoamine oxidase type A. Nucleic Acids Research, 19(16), 4537-4541. https://doi.org/10.1093/nar/19.16.4537
Cheung, N. W., & Earl, J. (2001). Monoamine oxidase deficiency: A cause of flushing and attention-deficit/ hyperactivity disorder? Archives of Internal Medicine, 161(20), 2503-2504. https://doi.org/10.1001/archinte.161.20.2503
Ellard, S., Baple, E. L., Callaway, A., Berry, I., Forrester, N., Turnbull, C., Owens, M., Eccles, D. M., Abbs, S., Scott, R., Deans, Z. C., Lester, T., Campbell, J., Newman, W. G., Ramsden, S., & McMullan, D. J. (2020). ACGS best practice guidelines for variant classification in rare disease. Association for Clinical Genomics Science. https://www.acgs.uk.com/media/11631/uk-practice-guidelines-for-variant-classification-v4-01-2020.pdf
Godar, S. C., Bortolato, M., Castelli, M. P., Casti, A., Casu, A., Chen, K., Ennas, M. G., Tambaro, S., & Shih, J. C. (2014). The aggression and behavioral abnormalities associated with monoamine oxidase A deficiency are rescued by acute inhibition of serotonin reuptake. Journal of Psychiatric Research, 56, 1-9. https://doi.org/10.1016/j.jpsychires.2014.04.014
Levitt, P., Harvey, J. A., Friedman, E., Simansky, K., & Murphy, E. H. (1997). New evidence for neurotransmitter influences on brain development. Trends in Neurosciences, 20(6), 269-274. https://doi.org/10.1016/s0166-2236(96)01028-4
Ozelius, L., Hsu, Y. P., Bruns, G., Powell, J. F., Chen, S., Weyler, W., Utterback, M., Zucker, D., Haines, J., Trofatter, J. A., Conneally, P. M., Gusella, J. F., & Breakefield, X. O. (1988). Human monoamine oxidase gene (MAOA): Chromosome position (Xp21-p11) and DNA polymorphism. Genomics, 3(1), 53-58. https://doi.org/10.1016/0888-7543(88)90159-0
Palmer, E. E., Leffler, M., Rogers, C., Shaw, M., Carroll, R., Earl, J., Cheung, N. W., Champion, B., Hu, H., Haas, S. A., Kalscheuer, V. M., Gecz, J., & Field, M. (2016). New insights into Brunner syndrome and potential for targeted therapy. Clinical Genetics, 89(1), 120-127. https://doi.org/10.1111/cge.12589
Piton, A., Poquet, H., Redin, C., Masurel, A., Lauer, J., Muller, J., Thevenon, J., Herenger, Y., Chancenotte, S., Bonnet, M., Pinoit, J. M., Huet, F., Thauvin-Robinet, C., Jaeger, A. S., Le Gras, S., Jost, B., Gérard, B., Peoc'h, K., Launay, J. M., … Mandel, J. L. (2014). 20 ans après: A second mutation in MAOA identified by targeted high-throughput sequencing in a family with altered behavior and cognition. European Journal of Human Genetics, 22(6), 776-783. https://doi.org/10.1038/ejhg.2013.243
Richards, S., Aziz, N., Bale, S., Bick, D., Das, S., Gastier-Foster, J., Grody, W. W., Hegde, M., Lyon, E., Spector, E., Voelkerding, K., Rehm, H. L., & ACMG Laboratory Quality Assurance Committee. (2015). Standards and guidelines for the interpretation of sequence variants: A joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genetics in Medicine, 17(5), 405-424. https://doi.org/10.1038/gim.2015.30
Scott, A. L., Bortolato, M., Chen, K., & Shih, J. C. (2008). Novel monoamine oxidase A knock out mice with human-like spontaneous mutation. Neuroreport, 19(7), 739-743. https://doi.org/10.1097/WNR.0b013e3282fd6e88
Shih, J. C., Chen, K., & Ridd, M. J. (1999). Monoamine oxidase: From genes to behavior. Annual Review of Neuroscience, 22, 197-217. https://doi.org/10.1146/annurev.neuro.22.1.197
Teskey, G. C., Radford, K. S., Seif, I., & Dyck, R. H. (2004). MAOA knockout mice are more susceptible to seizures but show reduced epileptogenesis. Epilepsy Research, 59(1), 25-34. https://doi.org/10.1016/j.eplepsyres.2004.03.001
van Rhijn, J. R., Shi, Y., Bormann, M., Mossink, B., Frega, M., Recaioglu, H., Hakobjan, M., Klein Gunnewiek, T., Schoenmaker, C., Palmer, E., Faivre, L., Kittel-Schneider, S., Schubert, D., Brunner, H., Franke, B., & Nadif, K. N. (2022). Brunner syndrome associated MAOA mutations result in NMDAR hyperfunction and increased network activity in human dopaminergic neurons. Neurobiology of Disease, 163, 105587. https://doi.org/10.1016/j.nbd.2021.105587

Auteurs

Maria Letizia Minniti (ML)

Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy.
Department of Child Neurology and Psychiatry, IRCCS Mondino Foundation, Pavia, Italy.

Silvia Kalantari (S)

Department of Medical Sciences, University of Turin, Turin, Italy.

Ludovica Pasca (L)

Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy.
Department of Child Neurology and Psychiatry, IRCCS Mondino Foundation, Pavia, Italy.

Samantha Bruno (S)

Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy.
Department of Child Neurology and Psychiatry, IRCCS Mondino Foundation, Pavia, Italy.

Sebastiano Arceri (S)

IRCCS, Mondino Foundation, Pavia, Italy.

Elisa Novello (E)

Department of Molecular Medicine, University of Pavia, Pavia, Italy.

Elisa Giorgio (E)

Department of Molecular Medicine, University of Pavia, Pavia, Italy.
IRCCS Mondino Foundation, Neurogenetics Research Center, Pavia, Italy.

Vittoria Rizzo (V)

Department of Molecular Medicine, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.

Renato Borgatti (R)

Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy.
Department of Child Neurology and Psychiatry, IRCCS Mondino Foundation, Pavia, Italy.

Enza Maria Valente (EM)

Department of Molecular Medicine, University of Pavia, Pavia, Italy.
IRCCS Mondino Foundation, Neurogenetics Research Center, Pavia, Italy.

Antonio Pisani (A)

Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy.
IRCCS, Mondino Foundation, Pavia, Italy.

Simona Orcesi (S)

Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy.
Department of Child Neurology and Psychiatry, IRCCS Mondino Foundation, Pavia, Italy.

Fabio Sirchia (F)

Department of Molecular Medicine, University of Pavia, Pavia, Italy.
Medical Genetic Unit, Department of Diagnostic Medicine, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.

Classifications MeSH