Wednesday, December 4, 2024

GM3 synthase deficiency

Inspired by a patient

Cruz V, Xin B, Wang H. GM3 Synthase Deficiency. 2023 Jul 20. In: Adam MP, Feldman J, Mirzaa GM, Pagon RA, Wallace SE, Amemiya A, editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle; 1993–2024. PMID: 37471511.

Excerpt

Clinical characteristics: Early clinical features of GM3 synthase deficiency include infantile onset of severe irritability with feeding difficulties, early and intractable seizures, growth failure with acquired microcephaly, sensorineural hearing impairment, hypotonia, and poor visual function. Over time, affected individuals experience severe-to-profound developmental delay and intellectual disability, can develop dystonia with hyperkinetic movements, and may develop pigmentary skin changes of the hands and feet. Affected individuals often have frequent ear infections and pneumonia without evidence of immune dysfunction.

Diagnosis/testing: The diagnosis of GM3 synthase deficiency is established in a proband with suggestive findings and biallelic pathogenic variants in ST3GAL5 identified by molecular genetic testing.

Management: Treatment of manifestations: Treatment for new-onset or worsening irritability is based on identification of inciting factors; for example, motility agents for constipation, antibiotic treatment of infections, and standard therapies for GERD, such as proton pump inhibitors. Seizures are treated with anti-seizure medication (ASM), although the majority of electrographic seizures in affected children are clinically silent. No ASM has been demonstrated effective for this condition specifically, ASM treatment may be only partially effective, and multiple ASMs may be required. Feeding therapy may be useful, with consideration of gastrostomy tube placement for persistent poor feeding / growth failure. Hearing aids may be helpful on a case-by-case basis. There is no specific treatment for optic atrophy or cortical blindness, although referral to low vision services is recommended. Dystonia, developmental delay / intellectual disability, sleep disturbances, infectious illnesses, and scoliosis are treated per standard methods.

Surveillance: At each visit: measure growth parameters, evaluate status and safety of oral intake, monitor for new manifestations (seizures, changes in tone, movement disorders), monitor developmental progress, assess for behavioral changes (new-onset or worsening irritability; aggressive or self-injurious behaviors), monitor for constipation/GERD/emesis, monitor for signs/symptoms of pneumonia, and obtain a non-invasive SpO2. Annually: physical exam for signs/symptoms of scoliosis. As clinically indicated: Audiologic evaluation, ophthalmologic evaluation, and assessment of mobility, physical medicine, and OT/PT needs.

Therapies under investigation: Oral supplementation with GM3 gangliosides did not alter disease course and demonstrated only modest short-term benefit to affected individuals.

Genetic counseling: GM3 synthase deficiency is inherited in an autosomal recessive manner. If both parents are known to be heterozygous for an ST3GAL5 pathogenic variant, each sib of an affected individual has at conception a 25% chance of being affected, a 50% chance of being an asymptomatic carrier, and a 25% chance of inheriting neither of the familial pathogenic variants. Once the ST3GAL5 pathogenic variants have been identified in an affected family member, carrier testing for at-risk relatives and prenatal and preimplantation genetic testing are possible.

Yang H, Brown RH Jr, Wang D, Strauss KA, Gao G. Rescue of GM3 synthase deficiency by spatially controlled, rAAV-mediated ST3GAL5 delivery. JCI Insight. 2023 May 8;8(9):e168688. doi: 10.1172/jci.insight.168688. PMID: 37014712; PMCID: PMC10243808.

Abstract

GM3 synthase deficiency (GM3SD) is an infantile-onset epileptic encephalopathy syndrome caused by biallelic loss-of-function mutations in ST3GAL5. Loss of ST3GAL5 activity in humans results in systemic ganglioside deficiency and severe neurological impairment. No disease-modifying treatment is currently available. Certain recombinant adeno-associated viruses (rAAVs) can cross the blood-brain barrier to induce widespread, long-term gene expression in the CNS and represent a promising therapeutic strategy. Here, we show that a first-generation rAAV-ST3GAL5 replacement vector using a ubiquitous promoter restored tissue ST3GAL5 expression and normalized cerebral gangliosides in patient-derived induced pluripotent stem cell neurons and brain tissue from St3gal5-KO mice but caused fatal hepatotoxicity when administered systemically. In contrast, a second-generation vector optimized for CNS-restricted ST3GAL5 expression, administered by either the intracerebroventricular or i.v. route at P1, allowed for safe and effective rescue of lethality and behavior impairment in symptomatic GM3SD mice up to a year. These results support further clinical development of ST3GAL5 gene therapy.

Wang AS, Kilbane C. Dystonia Due to GM3 Synthase Deficiency. Mov Disord Clin Pract. 2022 Jan 5;9(2):236-239. doi: 10.1002/mdc3.13399. PMID: 35146061; PMCID: PMC8810422.

Abstract

Background: Gangliosides are expressed in neuronal membranes, and play roles in neuronal differentiation and cell regulation during brain development. The ST3GAL5 gene encodes the enzyme GM3 synthase, and its deficiency causes a rare condition described to cause refractory epilepsy, profound intellectual disability, quadriplegia, choreoathetosis, and pigmentary skin changes. GM3 synthase deficiency is rarely reported to cause dystonia. We report five cases of GM3 synthase deficiency involving a dystonic phenotype.

Cases: The five reported individuals were born of unaffected consanguineous parents from Old Order Amish families. They all developed refractory epilepsy and developmental regression within the first few months of life. They exhibit variable degrees of extrapyramidal movements, including orofacial, cervical, and limb dystonia, as well as choreoathetosis.

Conclusions: We report five individuals with GM3 synthase deficiency who developed dystonic features. Dystonia has previously been reported in only one case of GM3 synthase deficiency.

Heide S, Jacquemont ML, Cheillan D, Renouil M, Tallot M, Schwartz CE, Miquel J, Bintner M, Rodriguez D, Darcel F, Buratti J, Haye D, Passemard S, Gras D, Perrin L, Capri Y, Gérard B, Piton A, Keren B, Thauvin-Robinet C, Duffourd Y, Faivre L, Poe C, Pervillé A, Héron D, Thévenon J, Arnaud L, LeGuern E, La Selva L, Vetro A, Guerrini R, Nava C, Mignot C. GM3 synthase deficiency in non-Amish patients. Genet Med. 2022 Feb;24(2):492-498. doi: 10.1016/j.gim.2021.10.007. Epub 2021 Nov 30. PMID: 34906476.

Abstract

Purpose: Biallelic loss-of-function variants in ST3GAL5 cause GM3 synthase deficiency (GM3SD) responsible for Amish infantile epilepsy syndrome. All Amish patients carry the homozygous p.(Arg288Ter) variant arising from a founder effect. To date only 10 patients from 4 non-Amish families have been reported. Thus, the phenotypical spectrum of GM3SD due to other variants and other genetic backgrounds is still poorly known.

Methods: We collected clinical and molecular data from 16 non-Amish patients with pathogenic ST3GAL5 variants resulting in GM3SD.

Results: We identified 12 families originating from Reunion Island, Ivory Coast, Italy, and Algeria and carrying 6 ST3GAL5 variants, 5 of which were novel. Genealogical investigations and/or haplotype analyses showed that 3 of these variants were founder alleles. Glycosphingolipids quantification in patients' plasma confirmed the pathogenicity of 4 novel variants. All patients (N = 16), aged 2 to 12 years, had severe to profound intellectual disability, 14 of 16 had a hyperkinetic movement disorder, 11 of 16 had epilepsy and 9 of 16 had microcephaly. Other main features were progressive skin pigmentation anomalies, optic atrophy or pale papillae, and hearing loss.

Conclusion: The phenotype of non-Amish patients with GM3SD is similar to the Amish infantile epilepsy syndrome, which suggests that GM3SD is associated with a narrow and severe clinical spectrum.

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