Mucopolysaccharidosis type III: current clinical trials, challenges and recommendations

References

• Muenzer J. Overview of the mucopolysaccharidoses. Rheumatology (Oxford, England). 2011 Dec;50(Suppl 5):v4–12.
   PubMed Web of Science ®Google Scholar
• Valstar MJ, Ruijter GJ, Van Diggelen OP, et al. Sanfilippo syndrome: a mini-review. J Inherit Metab Dis. 2008 Apr;31(2):240–252.
   PubMed Web of Science ®Google Scholar
• McKusick-Nathans Institute of Genetic Medicine JHU. Online Mendelian Inheritance in Man, OMIM®. [cited 2017 Oct]. Available from: https://omim.org/2017.
   Google Scholar
• Heron B, Mikaeloff Y, Froissart R, et al. Incidence and natural history of mucopolysaccharidosis type III in France and comparison with United Kingdom and Greece. Am J Med Genet Part. 2011 Jan;155a(1):58–68.
   PubMed Web of Science ®Google Scholar
• Yogalingam G, Hopwood JJ. Molecular genetics of mucopolysaccharidosis type IIIA and IIIB: diagnostic, clinical, and biological implications. Hum Mutat. 2001 Oct;18(4):264–281.
   PubMed Web of Science ®Google Scholar
• Archer LD, Langford-Smith KJ, Bigger BW, et al. Mucopolysaccharide diseases: a complex interplay between neuroinflammation, microglial activation and adaptive immunity. J Inherit Metab Dis. 2014 Jan;37(1):1–12.
   PubMed Web of Science ®Google Scholar
• McGlynn R, Dobrenis K, Walkley SU. Differential subcellular localization of cholesterol, gangliosides, and glycosaminoglycans in murine models of mucopolysaccharide storage disorders. J Comp Neurol. 2004 Dec 20;480(4):415–426.
   PubMed Web of Science ®Google Scholar
• Ohmi K, Greenberg DS, Rajavel KS, et al. Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1902–1907.
   PubMed Web of Science ®Google Scholar
• Wilkinson FL, Holley RJ, Langford-Smith KJ, et al. Neuropathology in mouse models of mucopolysaccharidosis type I, IIIA and IIIB. PloS One. 2012;7(4):e35787.
   PubMed Web of Science ®Google Scholar
• Fedele AO. Sanfilippo syndrome: causes, consequences, and treatments. Appl Clin Genet. 2015;8:269–281.
   PubMedGoogle Scholar
• Roca C, Motas S, Marco S, et al. Disease correction by AAV-mediated gene therapy in a new mouse model of mucopolysaccharidosis type IIID. Hum Mol Genet. 2017 Apr 15;26(8):1535–1551.
   PubMed Web of Science ®Google Scholar
• Cleary MA, Wraith JE. Management of mucopolysaccharidosis type III. Arch Dis Child. 1993 Sep;69(3):403–406.
   PubMed Web of Science ®Google Scholar
• Shapiro EG, Nestrasil I, Delaney KA, et al. A prospective natural history study of mucopolysaccharidosis type IIIA. J Pediatr. 2016;170:278-87.e1-4.
   PubMed Web of Science ®Google Scholar
• Wijburg FA, Wegrzyn G, Burton BK, et al. Mucopolysaccharidosis type III (Sanfilippo syndrome) and misdiagnosis of idiopathic developmental delay, attention deficit/hyperactivity disorder or autism spectrum disorder. Acta Paediatrica (Oslo, Norway: 1992). 2013 May;102(5):462–470.
   PubMed Web of Science ®Google Scholar
• Lavery C, Hendriksz CJ, Jones SA. Mortality in patients with Sanfilippo syndrome. Orphanet J Rare Dis. 2017 Oct 23;12(1):168.
   PubMedGoogle Scholar
• Valstar MJ, Neijs S, Bruggenwirth HT, et al. Mucopolysaccharidosis type IIIA: clinical spectrum and genotype-phenotype correlations. Ann Neurol. 2010 Dec;68(6):876–887.
   PubMed Web of Science ®Google Scholar
• Truxal KV, Fu H, McCarty DM, et al. A prospective one-year natural history study of mucopolysaccharidosis types IIIA and IIIB: implications for clinical trial design. Mol Genet Metab. 2016 Nov;119(3):239–248.
   PubMed Web of Science ®Google Scholar
• Van Der Lee JH, Morton J, Adams HR, et al. Cognitive endpoints for therapy development for neuronopathic mucopolysaccharidoses: results of a consensus procedure. Mol Genet Metab. 2017 Jun;121(2):70–79.
   PubMed Web of Science ®Google Scholar
• Prasad VK, Mendizabal A, Parikh SH, et al. Unrelated donor umbilical cord blood transplantation for inherited metabolic disorders in 159 pediatric patients from a single center: influence of cellular composition of the graft on transplantation outcomes. Blood. 2008 Oct 01;112(7):2979–2989.
   PubMed Web of Science ®Google Scholar
• Shapiro EG, Lockman LA, Balthazor M, et al. Neuropsychological outcomes of several storage diseases with and without bone marrow transplantation. J Inherit Metab Dis. 1995;18(4):413–429.
   PubMed Web of Science ®Google Scholar
• Welling L, Marchal JP, Van Hasselt P, et al. Early umbilical cord blood-derived stem cell transplantation does not prevent neurological deterioration in mucopolysaccharidosis type III. JIMD Reports. 2015;18:63–68.
   PubMedGoogle Scholar
• Piotrowska E, Jakobkiewicz-Banecka J, Baranska S, et al. Genistein-mediated inhibition of glycosaminoglycan synthesis as a basis for gene expression-targeted isoflavone therapy for mucopolysaccharidoses. Europ J Human Genet: EJHG. 2006 Jul;14(7):846–852.
   PubMed Web of Science ®Google Scholar
• Delgadillo V, O’Callaghan Mdel M, Artuch R, et al. Genistein supplementation in patients affected by Sanfilippo disease. J Inherit Metab Dis. 2011 Oct;34(5):1039–1044.
   PubMed Web of Science ®Google Scholar
• Piotrowska E, Jakobkiewicz-Banecka J, Maryniak A, et al. Two-year follow-up of Sanfilippo disease patients treated with a genistein-rich isoflavone extract: assessment of effects on cognitive functions and general status of patients. Med Sci Monit: Internat Med J Exp Clin Res. 2011 Apr;17(4):Cr196–202.
   Google Scholar
• De Ruijter J, Valstar MJ, Narajczyk M, et al. Genistein in Sanfilippo disease: a randomized controlled crossover trial. Ann Neurol. 2012 Jan;71(1):110–120.
   PubMed Web of Science ®Google Scholar
• Treiber A, Morand O, Clozel M. The pharmacokinetics and tissue distribution of the glucosylceramide synthase inhibitor miglustat in the rat. Xenobiotica. 2007 Mar;37(3):298–314.
   PubMed Web of Science ®Google Scholar
• Guffon N, Bin-Dorel S, Decullier E, et al. Evaluation of miglustat treatment in patients with type III mucopolysaccharidosis: a randomized, double-blind, placebo-controlled study. J Pediatr. 2011 Nov;159(5):838–44.e1.
   PubMed Web of Science ®Google Scholar
• Gaffke L, Pierzynowska K, Piotrowska E, et al. How close are we to therapies for Sanfilippo disease? Metab Brain Dis. 2017 Sep 18.
   PubMedGoogle Scholar
• [cited 2017 October]. Available from: http://orchard-tx.com/programmes/#. Orchard Therapeutics.
   Google Scholar
• Naldini L. Gene therapy returns to centre stage. Nature. 2015 Oct 15;526(7573):351–360.
   PubMed Web of Science ®Google Scholar
• Ginn SL, Alexander IE, Edelstein ML, et al. Gene therapy clinical trials worldwide to 2012 – an update. J Gene Med. 2013 Feb;15(2):65–77.
   PubMed Web of Science ®Google Scholar
• Verma IM, Somia N. Gene therapy – promises, problems and prospects. Nature. 1997 Sep 18;389(6648):239–242.
   PubMed Web of Science ®Google Scholar
• Sands MS, Davidson BL. Gene therapy for lysosomal storage diseases. Mol Ther:J Am Soc Gene Ther. 2006 May;13(5):839–849.
   PubMed Web of Science ®Google Scholar
• Neufeld EF, Fratantoni JC. Inborn errors of mucopolysaccharide metabolism. Science. 1970;141–146.
   PubMed Web of Science ®Google Scholar
• Duncan FJ, Naughton BJ, Zaraspe K, et al. Broad functional correction of molecular impairments by systemic delivery of scAAVrh74-hSGSH gene delivery in MPS IIIA mice. Mol Ther. 2015;23(4):638–647.
   Google Scholar
• Ribera A, Haurigot V, Garcia M, et al. Biochemical, histological and functional correction of mucopolysaccharidosis type IIIB by intra-cerebrospinal fluid gene therapy. Hum Mol Genet. 2015 Apr 01;24(7):2078–2095.
   PubMed Web of Science ®Google Scholar
• Winner LK, Beard H, Hassiotis S, et al. A preclinical study evaluating AAVrh10-based gene therapy for Sanfilippo syndrome. Hum Gene Ther. 2016 May;27(5):363–375.
   PubMed Web of Science ®Google Scholar
• https://clinicaltrials.gov. ClinicalTrials.gov Identifier: NCT02716246.
   Google Scholar
• [cited 2017 October]. Available from: http://investors.abeonatherapeutics.com/phoenix.zhtml?c=63510&p=irol-newsArticle&ID=2305130.
   Google Scholar
• [cited 2017 October]. Available from: http://abeonatherapeutics.com/research-and-development/. Abeona Therapeutics.
   Google Scholar
• Cosma MP, Pepe S, Annunziata I, et al. The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases. Cell. 2003 May 16;113(4):445–456.
   PubMed Web of Science ®Google Scholar
• Tardieu M, Zerah M, Husson B, et al. Intracerebral administration of adeno-associated viral vector serotype rh.10 carrying human SGSH and SUMF1 cDNAs in children with mucopolysaccharidosis type IIIA disease: results of a phase I/II trial. Hum Gene Ther. 2014 Jun;25(6):506–516.
   PubMed Web of Science ®Google Scholar
• [cited 2017 October]. Available from: http://www.lysogene.com/pioneering-science/pipeline/. Lysogene.
   Google Scholar
• Tardieu M, Zerah M, Gougeon ML, et al. Intracerebral gene therapy in children with mucopolysaccharidosis type IIIB syndrome: an uncontrolled phase 1/2 clinical trial. Lancet Neurol. 2017 Sep;16(9):712–720.
   PubMed Web of Science ®Google Scholar
• Cearley CN, Wolfe JH. Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol Ther:J Am Soc Gene Ther. 2006 Mar;13(3):528–537.
   PubMed Web of Science ®Google Scholar
• Fu H, Dirosario J, Killedar S, et al. Correction of neurological disease of mucopolysaccharidosis IIIB in adult mice by rAAV9 trans-blood-brain barrier gene delivery. Mol Ther:J Am Soc Gene Ther. 2011 Jun;19(6):1025–1033.
   PubMed Web of Science ®Google Scholar
• Ellinwood NM, Ausseil J, Desmaris N, et al. Safe, efficient, and reproducible gene therapy of the brain in the dog models of Sanfilippo and Hurler syndromes. Mol Ther:J Am Soc Gene Ther. 2011 Feb;19(2):251–259.
   PubMed Web of Science ®Google Scholar
• Schaefer RM, Tylki-Szymanska A, Hilz MJ. Enzyme replacement therapy for Fabry disease: a systematic review of available evidence. Drugs. 2009 Nov 12;69(16):2179–2205.
   PubMed Web of Science ®Google Scholar
• Scott LJ. Eliglustat: A review in Gaucher disease type 1. Drugs. 2015 Sep;75(14):1669–1678.
   PubMed Web of Science ®Google Scholar
• Harmatz P, Giugliani R, Fau - Schwartz I, et al. Enzyme replacement therapy for mucopolysaccharidosis VI: a phase 3, randomized, double-blind, placebo-controlled, multinational study of recombinant human N-acetylgalactosamine 4-sulfatase (recombinant human arylsulfatase B or rhASB) and follow-on, open-label extension study. J Pediatr. 2006;148(4):533–539.
   Google Scholar
• Hendriksz CJ, Burton B, Fau - Fleming TR, et al. Efficacy and safety of enzyme replacement therapy with BMN 110 (elosulfase alfa) for Morquio A syndrome (mucopolysaccharidosis IVA): a phase 3 randomised placebo-controlled study. J Inherit Metab Dis. 2014;37(6):979–990.
   Google Scholar
• Muenzer J, Wraith Je Fau - Beck M, Beck M, et al. A phase II/III clinical study of enzyme replacement therapy with idursulfase in mucopolysaccharidosis II (Hunter syndrome). Genet Med. 2006;8(8):465–473.
   Google Scholar
• Wraith JE, Clarke La Fau - Beck M, Beck M, et al. Enzyme replacement therapy for mucopolysaccharidosis I: a randomized, double-blinded, placebo-controlled, multinational study of recombinant human alpha-L-iduronidase (laronidase). J Pediatr. 2004 M;144(5):581–588.
   Google Scholar
• Fedele AO, Filocamo M, Di Rocco M, et al. Mutational analysis of the HGSNAT gene in Italian patients with mucopolysaccharidosis IIIC (Sanfilippo C syndrome). Mutation in Brief #959. Online. Human Mutation. 2007 May;28(5):523.
   PubMedGoogle Scholar
• Jones SA, Breen C, Heap F, et al. A phase 1/2 study of intrathecal heparan-N-sulfatase in patients with mucopolysaccharidosis IIIA. Mol Genet Metab. 2016 Jul;118(3):198–205.
   PubMed Web of Science ®Google Scholar
• Available from: https://clinicaltrials.gov. ClinicalTrials.gov Identifier: NCT02060526.
   Google Scholar
• [cited 2017 October]. Available from: http://investors.shire.com/~/media/Files/S/Shire-IR/quarterly-reports/2016/shire-release-3Q-2016-results.pdf.
   Google Scholar
• https://clinicaltrials.gov. ClinicalTrials.gov Identifier: NCT02324049.
   Google Scholar
• Sheridan C. FDA approves ‘farmaceutical’ drug from transgenic chickens. Nat Biotechnol. 2016 Feb;34(2):117–119.
   PubMed Web of Science ®Google Scholar
• [cited 2017 October]. Available from: http://news.alexion.com/press-release/product-news/alexion-presents-new-sbc-103-rhnaglu-enzyme-phase-12-data-brain-mri-and-n.
   Google Scholar
• [cited 2017 October]. Available from: http://www.raredr.com/news/alexion-shelves-sanfilippo-ert-drug.
   Google Scholar
• https://clinicaltrials.gov. ClinicalTrials.gov Identifier: NCT02754076.
   Google Scholar
• [cited 2017 October]. Available from: http://www.biomarin.com/products/pipeline/bmn-250/. Biomarin.
   Google Scholar
• Aoyagi-Scharber M, Crippen-Harmon D, Lawrence R, et al. Clearance of heparan sulfate and attenuation of CNS pathology by intracerebroventricular BMN 250 in Sanfilippo type B mice. Molecul Ther Methods Clin Develop. 2017 Sep 15;6:43–53.
   PubMed Web of Science ®Google Scholar
• Malinowska M, Wilkinson FL, Langford-Smith KJ, et al. Genistein improves neuropathology and corrects behaviour in a mouse model of neurodegenerative metabolic disease. PloS One. 2010 Dec 01;5(12):e14192.
   PubMed Web of Science ®Google Scholar
• Available from: https://www.clinicaltrialsregister.eu/. EudraCT number: 2013-001479-18.
   Google Scholar
• Velasco HM, Sanchez Y, Martin AM, et al. Natural History of Sanfilippo Syndrome Type C in Boyaca, Colombia. J Child Neurol. 2017 Feb;32(2):177–183.
   PubMed Web of Science ®Google Scholar
• Meyer A, Kossow K, Gal A, et al. Scoring evaluation of the natural course of mucopolysaccharidosis type IIIA (Sanfilippo syndrome type A). Pediatrics. 2007 Nov;120(5):e1255–61.
   PubMed Web of Science ®Google Scholar
• Ruijter GJ, Valstar MJ, Van De Kamp JM, et al. Clinical and genetic spectrum of Sanfilippo type C (MPS IIIC) disease in The Netherlands. Mol Genet Metab. 2008 Feb;93(2):104–111.
   PubMed Web of Science ®Google Scholar
• Delgadillo V, O’Callaghan Mdel M, Gort L, et al. Natural history of Sanfilippo syndrome in Spain. Orphanet J Rare Dis. 2013 Dec;06(8):189.
   Google Scholar
• Malm G, Mansson JE. Mucopolysaccharidosis type III (Sanfilippo disease) in Sweden: clinical presentation of 22 children diagnosed during a 30-year period. Acta Paediatrica (Oslo, Norway: 1992). 2010 Aug;99(8):1253–1257.
   PubMed Web of Science ®Google Scholar
• Buhrman D, Thakkar K, Poe M, et al. Natural history of Sanfilippo syndrome type A. J Inherit Metab Dis. 2014 May;37(3):431–437.
   PubMed Web of Science ®Google Scholar
• Available from: https://clinicaltrials.gov. ClinicalTrials.gov Identifier: NCT01509768.
   Google Scholar
• Available from: https://clinicaltrials.gov. ClinicalTrials.gov Identifier: NCT02746341.
   Google Scholar
• Knottnerus SJG, Nijmeijer SCM, Ij L, et al. Prediction of phenotypic severity in mucopolysaccharidosis type IIIA. Ann Neurol. 2017;82(5):686–696.
   PubMed Web of Science ®Google Scholar
• Meijer OL, Welling L, Valstar MJ, et al. Residual N-acetyl-alpha-glucosaminidase activity in fibroblasts correlates with disease severity in patients with mucopolysaccharidosis type IIIB. J Inherit Metab Dis. 2016 May;39(3):437–445.
   PubMed Web of Science ®Google Scholar
• De Ruijter J, De Ru MH, Wagemans T, et al. Heparan sulfate and dermatan sulfate derived disaccharides are sensitive markers for newborn screening for mucopolysaccharidoses types I, II and III. Mol Genet Metab. 2012 Dec;107(4):705–710.
   PubMed Web of Science ®Google Scholar
• Fuller M, Tucker JN, Lang DL, et al. Screening patients referred to a metabolic clinic for lysosomal storage disorders. J Med Genet. 2011 Jun;48(6):422–425.
   PubMed Web of Science ®Google Scholar
• Meikle PJ, Ranieri E, Simonsen H, et al. Newborn screening for lysosomal storage disorders: clinical evaluation of a two-tier strategy. Pediatrics. 2004 Oct;114(4):909–916.
   PubMed Web of Science ®Google Scholar
• Mathijssen IB, Henneman L, Van Eeten-Nijman JM, et al. Targeted carrier screening for four recessive disorders: high detection rate within a founder population. Eur J Med Genet. 2015 Mar;58(3):123–128.
   PubMed Web of Science ®Google Scholar
• Plantinga M, Birnie E, Abbott KM, et al. Population-based preconception carrier screening: how potential users from the general population view a test for 50 serious diseases. Europ J Human Genet: EJHG. 2016;24(10):1417–1423. 10//print.
   PubMed Web of Science ®Google Scholar