Risdiplam: an investigational survival motor neuron 2 (SMN2) splicing modifier for spinal muscular atrophy (SMA)

References

• Lefebvre S, Bürglen L, Reboullet S, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995;80:155–165.
   PubMed Web of Science ®Google Scholar
• Verhaart IEC, Robertson A, Wilson IJ, et al. Prevalence, incidence and carrier frequency of 5q–linked spinal muscular atrophy – a literature review. Orphanet J Rare Dis. 2017;12:124.
   PubMed Web of Science ®Google Scholar
• Crawford TO, Pardo CA. The neurobiology of childhood spinal muscular atrophy. Neurobiol Dis. 1996;3:97–110.
   PubMed Web of Science ®Google Scholar
• Mercuri E, Bertini E, Iannaccone ST. Childhood spinal muscular atrophy: controversies and challenges. Lancet Neurol. 2012;11:443–452.
   PubMed Web of Science ®Google Scholar
• Tisdale S, Pellizzoni L. Disease mechanisms and therapeutic approaches in spinal muscular atrophy. J Neurosci. 2015;35:8691–8700.
   PubMed Web of Science ®Google Scholar
• Shababi M, Lorson CL, Rudnik-Schöneborn SS. Spinal muscular atrophy: a motor neuron disorder or a multi-organ disease? J Anat. 2014;224:15–28.
   PubMed Web of Science ®Google Scholar
• Yeo CJJ, Darras BT. Overturning the paradigm of spinal muscular atrophy as just a motor neuron disease. Pediatr Neurol. 2020;109:12–19.
   PubMed Web of Science ®Google Scholar
• Singh RN, Ottesen EW, Singh NN. The first orally deliverable small molecule for the treatment of spinal muscular atrophy. J Exp Neurosci. 2020;15:263310552097398.
   Google Scholar
• Dhillon S. Risdiplam: first approval. Drugs. 2020;80:1853–1858.
   PubMed Web of Science ®Google Scholar
• Ramdas S, Servais L. New treatments in spinal muscular atrophy: an overview of currently available data. Expert Opin Pharmacother. 2020;21:307–315.
   PubMed Web of Science ®Google Scholar
• Finkel RS, Mercuri E, Darras BT, et al. Nusinersen versus Sham control in infantile-onset spinal muscular atrophy. N Engl J Med. 2017;377:1723–1732.
   PubMed Web of Science ®Google Scholar
• Mercuri E, Muntoni F, Baranello G, et al. Onasemnogene abeparvovec gene therapy for symptomatic infantile-onset spinal muscular atrophy type 1 (STR1VE-EU): an open-label, single-arm, multicentre, phase 3 trial. Lancet Neurol. 2021;20:832–841.
   PubMed Web of Science ®Google Scholar
• Kakazu J, Walker NL, Babin KC, et al. Risdiplam for the use of spinal muscular atrophy. Orthop Rev (Pavia). 2021;13:25579.
   PubMed Web of Science ®Google Scholar
• Servais L, Baranello G, Scoto M, et al. Therapeutic interventions for spinal muscular atrophy: preclinical and early clinical development opportunities. Expert Opin Investig Drugs. 2021;30:519–527.
   PubMed Web of Science ®Google Scholar
• Pinard E, Green L, Reutlinger M, et al. Discovery of a novel class of survival motor neuron 2 splicing modifiers for the treatment of spinal muscular atrophy. J Med Chem. 2017;60:4444–4457.
   PubMed Web of Science ®Google Scholar
• Naryshkin NA, Weetall M, Dakka A, et al. SMN2 splicing modifiers improve motor function and longevity in mice with spinal muscular atrophy. Science. 2014;345:688–693.
   PubMed Web of Science ®Google Scholar
• Ratni H, Karp GM, Weetall M, et al. Specific correction of alternative survival motor neuron 2 splicing by small molecules: discovery of a potential novel medicine to treat spinal muscular atrophy. J Med Chem. 2016;59:6086–6100.
   PubMed Web of Science ®Google Scholar
• Ratni H, Ebeling M, Baird J, et al. Discovery of risdiplam, a selective survival of motor neuron-2 (SMN2) gene splicing modifier for the treatment of spinal muscular atrophy (SMA). J Med Chem. 2018;61:6501–6517.
   PubMed Web of Science ®Google Scholar
• Campagne S, Boigner S, Rüdisser S, et al. Structural basis of a small molecule targeting RNA for a specific splicing correction. Nat Chem Biol. 2019;15:1191–1198.
   PubMed Web of Science ®Google Scholar
• Sivaramakrishnan M, McCarthy KD, Campagne S, et al. Binding to SMN2 pre-mRNA-protein complex elicits specificity for small molecule splicing modifiers. Nat Commun. 2017;8:1476.
   PubMed Web of Science ®Google Scholar
• Poirier A, Weetall M, Heinig K, et al. Risdiplam distributes and increases SMN protein in both the central nervous system and peripheral organs. Pharmacol Res Perspect. 2018;6:e00447.
   PubMed Web of Science ®Google Scholar
• EVRYSDI: prescribing information [Internet] Last accessed March 2022. Available from: https://www.gene.com/download/pdf/evrysdi_prescribing.pdf
   Google Scholar
• Sturm S, Günther A, Jaber B, et al. A phase 1 healthy male volunteer single escalating dose study of the pharmacokinetics and pharmacodynamics of risdiplam (RG7916, RO7034067), a SMN2 splicing modifier. Br J Clin Pharmacol. 2019;85:181–193.
   PubMed Web of Science ®Google Scholar
• Baranello G, Darras BT, Day JW, et al. Risdiplam in Type 1 spinal muscular atrophy. N Engl J Med. 2021;384:915–923.
   PubMed Web of Science ®Google Scholar
• Finkel RS, McDermott MP, Kaufmann P, et al. Observational study of spinal muscular atrophy type I and implications for clinical trials. Neurology. 2014;83:810–817.
   PubMed Web of Science ®Google Scholar
• Kolb SJ, Coffey CS, Yankey JW, et al. Natural history of infantile‐onset spinal muscular atrophy. Ann Neurol. 2017;82:883–891.
   PubMed Web of Science ®Google Scholar
• Darras BT, Masson R, Mazurkiewicz-Bełdzińska M, et al. Risdiplam-treated infants with Type 1 spinal muscular atrophy versus historical controls. N Engl J Med. 2021;385:427–435.
   PubMed Web of Science ®Google Scholar
• De Sanctis R, Coratti G, Pasternak A, et al. Developmental milestones in type I spinal muscular atrophy. Neuromuscul Disord. 2016;26:754–759.
   PubMed Web of Science ®Google Scholar
• Kolb SJ, Coffey CS, Yankey JW, et al. Baseline results of the Neuro NEXT spinal muscular atrophy infant biomarker study. Ann Clin Transl Neurol. 2016;3:132–145.
   PubMed Web of Science ®Google Scholar
• Servais L, Baranello G, Masson R, et al. FIREFISH Part 2: efficacy and safety of risdiplam (RG7916) in infants with Type 1 spinal muscular atrophy (SMA) (1302). Neurology. 2020;94:1302.
   Web of Science ®Google Scholar
• Mercuri E, Baranello G, Boespflug-Tanguy O, et al. Risdiplam in Types 2 and 3 Spinal Muscular Atrophy: a randomised, placebo-controlled, dose-finding trial followed by 24 months of treatment at the pivotal dose (submitted).
   Google Scholar
• Muntoni F, Bertini E, Comi G, et al. Long-term follow-up of patients with type 2 and non-ambulant type 3 spinal muscular atrophy (SMA) treated with olesoxime in the OLEOS trial. Neuromuscul Disord. 2020;30:959–969.
   PubMed Web of Science ®Google Scholar
• Annoussamy M, Seferian AM, Daron A, et al. Natural history of Type 2 and 3 spinal muscular atrophy: 2‐year NatHis‐SMA study. Ann Clin Transl Neurol. 2021;8:359–373.
   PubMed Web of Science ®Google Scholar
• Mercuri E, Deconinck N, Mazzone ES, et al. Safety and efficacy of once-daily risdiplam in type 2 and non-ambulant type 3 spinal muscular atrophy (SUNFISH part 2): a phase 3, double-blind, randomised, placebo-controlled trial. Lancet Neurol. 2022;21:42–52.
   PubMed Web of Science ®Google Scholar
• Chiriboga C, Bruno C, Duong T, et al. EP.279 JEWELFISH: safety, pharmacodynamic and exploratory efficacy data in non-naïve patients with spinal muscular atrophy (SMA) receiving risdiplam. Neuromuscul Disord. 2021;31:S134–S135.
   PubMed Web of Science ®Google Scholar
• Finkel RS, Farrar MA, Vlodavets D, et al. RAINBOWFISH: preliminary efficacy and safety data in risdiplam-treated infants with presymptomatic SMA. Muscular Dystrophy Association Clinical and Scientific Conference; 2022 Mar 13-16; Nashville, USA
   Google Scholar
• Baranello G, Servais L, Bertini E, et al. Pooled safety data from the risdiplam clinical trial development program. British Paediatric Neurology Association; 2022 Jan; Virtual Congress.
   Google Scholar
• Sergott RC, Amorelli GM, Baranello G, et al. Risdiplam treatment has not led to retinal toxicity in patients with spinal muscular atrophy. Ann Clin Transl Neurol. 2021;8:54–65.
   PubMed Web of Science ®Google Scholar
• Dangouloff T, Botty C, Beaudart C, et al. Systematic literature review of the economic burden of spinal muscular atrophy and economic evaluations of treatments. Orphanet J Rare Dis. 2021;16:47.
   PubMed Web of Science ®Google Scholar
• Boemer F, Caberg J-H, Beckers P, et al. Three years pilot of spinal muscular atrophy newborn screening turned into official program in Southern Belgium. Sci Rep. 2021;11(1):19922.
   PubMed Web of Science ®Google Scholar
• Glascock J, Sampson J, Connolly AM, et al. Revised recommendations for the treatment of infants diagnosed with spinal muscular atrophy via newborn screening who have 4 copies of SMN2. J Neuromuscul Dis. 2020;7:97–100.
   PubMedGoogle Scholar
• Dangouloff T, Servais L. Clinical evidence supporting early treatment o patients with spinal muscular atrophy: current perspectives. Tcrm. 2019;15:1153–1161.
   Google Scholar
• Pera MC, Coratti G, Berti B, et al. Diagnostic journey in spinal muscular atrophy: is it still an odyssey? PLoS One. 2020;15:e0230677.
   PubMed Web of Science ®Google Scholar
• Dangouloff T, Vrščaj E, Servais L, et al. Newborn screening programs for spinal muscular atrophy worldwide: where we stand and where to go. Neuromuscul Disord. 2021;31:574–582.
   PubMed Web of Science ®Google Scholar
• Dangouloff T, Burghes A, Tizzano EF, et al. 244th ENMC international workshop: newborn screening in spinal muscular atrophy May 10-12, 2019, Hoofdorp, The Netherlands. Neuromuscul Disord. 2020;30:93–103.
   PubMed Web of Science ®Google Scholar
• Deng S, Lee BH, Ciafaloni E. Parent perceptions in choosing treatment for infants with spinal muscular atrophy diagnosed through newborn screening. J Child Neurol. 2021 37 ;43–49.
   PubMed Web of Science ®Google Scholar
• Hagenacker T, Wurster CD, Günther R, et al. Nusinersen in adults with 5q spinal muscular atrophy: a non-interventional, multicentre, observational cohort study. Lancet Neurol. 2020;19:317–325.
   PubMed Web of Science ®Google Scholar
• Rudnik-Schöneborn S, Vogelgesang S, Armbrust S, et al. Digital necroses and vascular thrombosis in severe spinal muscular atrophy. Muscle Nerve. 2010;42:144–147.
   PubMed Web of Science ®Google Scholar
• Deguise M-O, Chehade L, Kothary R. Metabolic dysfunction in spinal muscular atrophy. Int J Mol Sci. 2021;22:5913.
   PubMed Web of Science ®Google Scholar
• Carey KA, Farrar MA, Kasparian NA, et al. F amily, healthcare professional, and societal preferences for the treatment of infantile spinal muscular atrophy: a discrete choice experiment. Dev Med Child Neurol. 2021. (Online ahead of printing). DOI:https://doi.org/10.1111/dmcn.15135.
   Google Scholar
• Chabanon A, Seferian AM, Daron A, et al. Prospective and longitudinal natural history study of patients with Type 2 and 3 spinal muscular atrophy: baseline data NatHis-SMA study. PLoS One. 2018;13:e0201004.
   PubMed Web of Science ®Google Scholar
• Lilien C, Reyngoudt H, Seferian AM, et al. Upper limb disease evolution in exon 53 skipping eligible patients with Duchenne muscular dystrophy. Ann Clin Transl Neurol. 2021;8:1938–1950.
   PubMed Web of Science ®Google Scholar
• Fouarge E, Monseur A, Boulanger B, et al. Hierarchical Bayesian modelling of disease progression to inform clinical trial design in centronuclear myopathy. Orphanet J Rare Dis. 2021;16:3.
   PubMed Web of Science ®Google Scholar
• Bertini E, Dessaud E, Mercuri E, et al. Safety and efficacy of olesoxime in patients with type 2 or non-ambulatory type 3 spinal muscular atrophy: a randomised, double-blind, placebo-controlled phase 2 trial. Lancet Neurol. 2017;16:513–522.
   PubMed Web of Science ®Google Scholar
• Trundell D, Skalicky A, Staunton H, et al. Development of the SMA Independence scale-upper limb module (SMAIS-ULM): a novel scale for individuals with Type 2 and non-ambulant Type 3 SMA. J Neurol Sci. 2022;432:120059.
   PubMedGoogle Scholar