Progress in gene and cell therapies for the neuronal ceroid lipofuscinoses

References

• Palmer DN, Barry LA, Tyynela J, et al. NCL disease mechanisms. Biochim Biophys Acta. 2013;1832(11):1882–1893.
   PubMed Web of Science ®Google Scholar
• Nita DA, Mole SE, Minassian BA. Neuronal ceroid lipofuscinoses. Epileptic Disord. 2016;18(S2):73–88.
   PubMedGoogle Scholar
• Sleat DE, Gedvilaite E, Zhang Y, et al. Analysis of large-scale whole exome sequencing data to determine the prevalence of genetically-distinct forms of neuronal ceroid lipofuscinosis. Gene. 2016;593(2):284–291.
   PubMed Web of Science ®Google Scholar
• Ferreira CR, Gahl WA. Lysosomal storage diseases. Transl Sci Rare Dis. 2017;2(1–2):1–71.
   PubMedGoogle Scholar
• Braulke T, Bonifacino JS. Sorting of lysosomal proteins. Biochim Biophys Acta. 2009;1793(4):605–614.
   PubMed Web of Science ®Google Scholar
• Fratantoni JC, Hall CW, Neufeld EF. Hurler and Hunter syndromes: mutual correction of the defect in cultured fibroblasts. Science. 1968;162(3853):570–572.
   PubMed Web of Science ®Google Scholar
• Nelvagal HR, Cooper JD. Translating preclinical models of neuronal ceroid lipofuscinosis: progress and prospects. Expert Opinion Orphan Drugs. 2017;5(9):727–740.
   Web of Science ®Google Scholar
• Katz ML, Rustad E, Robinson GO, et al. Canine neuronal ceroid lipofuscinoses: Promising models for preclinical testing of therapeutic interventions. Neurobiol Dis. 2017;108:277–287.
   PubMed Web of Science ®Google Scholar
• Weber K, Pearce DA. Large animal models for Batten disease: a review. J Child Neurol. 2013;28(9):1123–1127.
   PubMed Web of Science ®Google Scholar
• Bond M, Holthaus SM, Tammen I, et al. Use of model organisms for the study of neuronal ceroid lipofuscinosis. Biochim Biophys Acta. 2013;1832(11):1842–1865.
   PubMed Web of Science ®Google Scholar
• Deeg HJ, Shulman HM, Albrechtsen D, et al. Batten’s disease: failure of allogeneic bone marrow transplantation to arrest disease progression in a canine model. Clin Genet. 1990;37(4):264–270.
   PubMed Web of Science ®Google Scholar
• Jolly RD, West DM. Blindness in South Hampshire sheep: a neuronal ceroidlipofuscinosis. N Z Vet J. 1976;24(6):123.
   PubMedGoogle Scholar
• Westlake VJ, Jolly RD, Jones BR, et al. Hematopoietic cell transplantation in fetal lambs with ceroid-lipofuscinosis. Am J Med Genet. 1995;57(2):365–368.
   PubMed Web of Science ®Google Scholar
• Katz ML, Khan S, Awano T, et al. A mutation in the CLN8 gene in English Setter dogs with neuronal ceroid-lipofuscinosis. Biochem Biophys Res Commun. 2005;327(2):541–547.
   PubMed Web of Science ®Google Scholar
• Tammen I, Houweling PJ, Frugier T, et al. A missense mutation (c.184C>T) in ovine CLN6 causes neuronal ceroid lipofuscinosis in Merino sheep whereas affected South Hampshire sheep have reduced levels of CLN6 mRNA. Biochim Biophys Acta. 2006;1762(10):898–905.
   PubMed Web of Science ®Google Scholar
• Lake BD, Henderson DC, Oakhill A, et al. Bone marrow transplantation in Batten disease (neuronal ceroid-lipofuscinosis)will it work? preliminary studies on coculture experiments and on bone marrow transplant in late infantile Batten disease. Am J Med Genet. 1995;57(2):369–373.
   PubMed Web of Science ®Google Scholar
• Lake BD, Steward CG, Oakhill A, et al. Bone marrow transplantation in late infantile Batten disease and juvenile Batten disease. Neuropediatrics. 1997;28(1):80–81.
   PubMed Web of Science ®Google Scholar
• Yuza Y, Yokoi K, Sakurai K, et al. Allogenic bone marrow transplantation for late-infantile neuronal ceroid lipofuscinosis. Pediatr Int. 2005;47(6):681–683.
   PubMed Web of Science ®Google Scholar
• Lonnqvist T, Vanhanen SL, Vettenranta K, et al. Hematopoietic stem cell transplantation in infantile neuronal ceroid lipofuscinosis. Neurology. 2001;57(8):1411–1416.
   PubMed Web of Science ®Google Scholar
• Uchida N, Buck DW, He D, et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci U S A. 2000;97(26):14720–14725.
   PubMed Web of Science ®Google Scholar
• Tamaki SJ, Jacobs Y, Dohse M, et al. Neuroprotection of host cells by human central nervous system stem cells in a mouse model of infantile neuronal ceroid lipofuscinosis. Cell Stem Cell. 2009;5(3):310–319.
   PubMed Web of Science ®Google Scholar
• Selden NR, Al-Uzri A, Huhn SL, et al. Central nervous system stem cell transplantation for children with neuronal ceroid lipofuscinosis. J Neurosurg Pediatr. 2013;11(6):643–652.
   PubMed Web of Science ®Google Scholar
• Tracy CJ, Whiting RE, Pearce JW, et al. Intravitreal implantation of TPP1-transduced stem cells delays retinal degeneration in canine CLN2 neuronal ceroid lipofuscinosis. Exp Eye Res. 2016;152:77–87.
   PubMed Web of Science ®Google Scholar
• Naso MF, Tomkowicz B, Perry WL 3rd, et al. adeno-associated virus (aav) as a vector for gene therapy. BioDrugs. 2017;31(4):317–334.
   PubMed Web of Science ®Google Scholar
• Levy YS, Gilgun-Sherki Y, Melamed E, et al. Therapeutic potential of neurotrophic factors in neurodegenerative diseases. BioDrugs. 2005;19(2):97–127.
   PubMed Web of Science ®Google Scholar
• Meyer JS, Katz ML, Maruniak JA, et al. Embryonic stem cell-derived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells. 2006;24(2):274–283.
   PubMed Web of Science ®Google Scholar
• Jankowiak W, Kruszewski K, Flachsbarth K, et al. Sustained neural stem cell-based intraocular delivery of cntf attenuates photoreceptor loss in the nclf mouse model of neuronal ceroid lipofuscinosis. PLoS One. 2015;10(5):e0127204.
   PubMed Web of Science ®Google Scholar
• Griffey M, Bible E, Vogler C, et al. Adeno-associated virus 2-mediated gene therapy decreases autofluorescent storage material and increases brain mass in a murine model of infantile neuronal ceroid lipofuscinosis. Neurobiol Dis. 2004;16(2):360–369.
   PubMed Web of Science ®Google Scholar
• Griffey MA, Wozniak D, Wong M, et al. CNS-directed AAV2-mediated gene therapy ameliorates functional deficits in a murine model of infantile neuronal ceroid lipofuscinosis. Mol Ther. 2006;13(3):538–547.
   PubMed Web of Science ®Google Scholar
• Griffey M, Macauley SL, Ogilvie JM, et al. AAV2-mediated ocular gene therapy for infantile neuronal ceroid lipofuscinosis. Mol Ther. 2005;12(3):413–421.
   PubMed Web of Science ®Google Scholar
• Burger C, Gorbatyuk OS, Velardo MJ, et al. Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther. 2004;10(2):302–317.
   PubMed Web of Science ®Google Scholar
• Macauley SL, Roberts MS, Wong AM, et al. Synergistic effects of central nervous system-directed gene therapy and bone marrow transplantation in the murine model of infantile neuronal ceroid lipofuscinosis. Ann Neurol. 2012;71(6):797–804.
   PubMed Web of Science ®Google Scholar
• Alexander IE, Russell DW, Miller AD. DNA-damaging agents greatly increase the transduction of nondividing cells by adeno-associated virus vectors. J Virol. 1994;68(12):8282–8287.
   PubMed Web of Science ®Google Scholar
• Yalkinoglu AO, Heilbronn R, Burkle A, et al. DNA amplification of adeno-associated virus as a response to cellular genotoxic stress. Cancer Res. 1988;48(11):3123–3129.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Butler JD, Levin SW, et al. Lysosomal ceroid depletion by drugs: therapeutic implications for a hereditary neurodegenerative disease of childhood. Nat Med. 2001;7(4):478–484.
   PubMed Web of Science ®Google Scholar
• Roberts MS, Macauley SL, Wong AM, et al. Combination small molecule PPT1 mimetic and CNS-directed gene therapy as a treatment for infantile neuronal ceroid lipofuscinosis. J Inherit Metab Dis. 2012;35(5):847–857.
   PubMed Web of Science ®Google Scholar
• Macauley SL, Wong AM, Shyng C, et al. An anti-neuroinflammatory that targets dysregulated glia enhances the efficacy of CNS-directed gene therapy in murine infantile neuronal ceroid lipofuscinosis. J Neurosci. 2014;34(39):13077–13082.
   PubMed Web of Science ®Google Scholar
• Shyng C, Nelvagal HR, Dearborn JT, et al. Synergistic effects of treating the spinal cord and brain in CLN1 disease. Proc Natl Acad Sci US. 2017;114(29):E5920–E5929.
   PubMed Web of Science ®Google Scholar
• Foust KD, Nurre E, Montgomery CL, et al. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol. 2009;27(1):59–65.
   PubMed Web of Science ®Google Scholar
• Mendell JR, Al-Zaidy S, Shell R, et al. Single-dose gene-replacement therapy for spinal muscular atrophy. N Engl J Med. 2017;377(18):1713–1722.
   PubMed Web of Science ®Google Scholar
• Lin L, Lobel P. Production and characterization of recombinant human CLN2 protein for enzyme-replacement therapy in late infantile neuronal ceroid lipofuscinosis. Biochem J. 2001;357(Pt 1):49–55.
   PubMedGoogle Scholar
• Haskell RE, Hughes SM, Chiorini JA, et al. Viral-mediated delivery of the late-infantile neuronal ceroid lipofuscinosis gene, TPP-I to the mouse central nervous system. Gene Ther. 2003;10(1):34–42.
   PubMed Web of Science ®Google Scholar
• Sondhi D, Peterson DA, Giannaris EL, et al. AAV2-mediated CLN2 gene transfer to rodent and non-human primate brain results in long-term TPP-I expression compatible with therapy for LINCL. Gene Ther. 2005;12(22):1618–1632.
   PubMed Web of Science ®Google Scholar
• Worgall S, Sondhi D, Hackett NR, et al. Treatment of late infantile neuronal ceroid lipofuscinosis by CNS administration of a serotype 2 adeno-associated virus expressing CLN2 cDNA. Hum Gene Ther. 2008;19(5):463–474.
   PubMed Web of Science ®Google Scholar
• Passini MA, Dodge JC, Bu J, et al. Intracranial delivery of CLN2 reduces brain pathology in a mouse model of classical late infantile neuronal ceroid lipofuscinosis. J Neurosci. 2006;26(5):1334–1342.
   PubMed Web of Science ®Google Scholar
• Sondhi D, Hackett NR, Peterson DA, et al. Enhanced survival of the LINCL mouse following CLN2 gene transfer using the rh.10 rhesus macaque-derived adeno-associated virus vector. Mol Ther. 2007;15(3):481–491.
   PubMed Web of Science ®Google Scholar
• Sondhi D, Peterson DA, Edelstein AM, et al. Survival advantage of neonatal CNS gene transfer for late infantile neuronal ceroid lipofuscinosis. Exp Neurol. 2008;213(1):18–27.
   PubMed Web of Science ®Google Scholar
• Cabrera-Salazar MA, Roskelley EM, Bu J, et al. Timing of therapeutic intervention determines functional and survival outcomes in a mouse model of late infantile batten disease. Mol Ther. 2007;15(10):1782–1788.
   PubMed Web of Science ®Google Scholar
• Katz ML, Tecedor L, Chen Y, et al. AAV gene transfer delays disease onset in a TPP1-deficient canine model of the late infantile form of Batten disease. Sci Transl Med. 2015;7(313):313ra180.
   PubMed Web of Science ®Google Scholar
• Whiting RE, Jensen CA, Pearce JW, et al. Intracerebroventricular gene therapy that delays neurological disease progression is associated with selective preservation of retinal ganglion cells in a canine model of CLN2 disease. Exp Eye Res. 2016;146:276–282.
   PubMed Web of Science ®Google Scholar
• Katz ML, Johnson GC, Leach SB, et al. Extraneuronal pathology in a canine model of CLN2 neuronal ceroid lipofuscinosis after intracerebroventricular gene therapy that delays neurological disease progression. Gene Ther. 2017;24(4):215–223.
   PubMed Web of Science ®Google Scholar
• Hughes SM, Hope KM, Xu JB, et al. Inhibition of storage pathology in prenatal CLN5-deficient sheep neural cultures by lentiviral gene therapy. Neurobiol Dis. 2014;62:543–550.
   PubMed Web of Science ®Google Scholar
• Palmer DN, Neverman NJ, Chen JZ, et al. Recent studies of ovine neuronal ceroid lipofuscinoses from BARN, the Batten Animal Research Network. Biochim Biophys Acta. 2015;1852(10Pt B):2279–2286.
   PubMed Web of Science ®Google Scholar
• Shevtsova Z, Garrido M, Weishaupt J, et al. CNS-expressed cathepsin D prevents lymphopenia in a murine model of congenital neuronal ceroid lipofuscinosis. Am J Pathol. 2010;177(1):271–279.
   PubMed Web of Science ®Google Scholar
• Kao AW, McKay A, Singh PP, et al. Progranulin, lysosomal regulation and neurodegenerative disease. Nat Rev Neurosci. 2017;18(6):325–333.
   PubMed Web of Science ®Google Scholar
• Arrant AE, Onyilo VC, Unger DE, et al. Progranulin gene therapy improves lysosomal dysfunction and microglial pathology associated with frontotemporal dementia and neuronal ceroid lipofuscinosis. J Neurosci. 2018;38(9):2341–2358.
   PubMed Web of Science ®Google Scholar
• Sondhi D, Scott EC, Chen A, et al. Partial correction of the CNS lysosomal storage defect in a mouse model of juvenile neuronal ceroid lipofuscinosis by neonatal CNS administration of an adeno-associated virus serotype rh.10 vector expressing the human CLN3 gene. Hum Gene Ther. 2014;25(3):223–239.
   PubMed Web of Science ®Google Scholar
• Tuxworth RI, Vivancos V, O’Hare MB, et al. Interactions between the juvenile Batten disease gene, CLN3, and the Notch and JNK signalling pathways. Hum Mol Genet. 2009;18(4):667–678.
   PubMed Web of Science ®Google Scholar
• Bosch ME, Aldrich A, Fallet R, et al. Self-Complementary aav9 gene delivery partially corrects pathology associated with juvenile neuronal ceroid lipofuscinosis (CLN3). J Neurosci. 2016;36(37):9669–9682.
   PubMed Web of Science ®Google Scholar
• Kleine Holthaus SM, Ribeiro J, Abelleira-Hervas L, et al. Prevention of photoreceptor cell loss in a cln6(nclf) mouse model of batten disease requires cln6 gene transfer to bipolar cells. Mol Ther. 2018;26(5):1343–1353.
   PubMed Web of Science ®Google Scholar
• Zhang YQ, Chandra SS. Oligomerization of cysteine string protein alpha mutants causing adult neuronal ceroid lipofuscinosis. Biochim Biophys Acta. 2014;1842(11):2136–2146.
   PubMed Web of Science ®Google Scholar
• Fernandez-Chacon R, Wolfel M, Nishimune H, et al. The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron. 2004;42(2):237–251.
   PubMed Web of Science ®Google Scholar
• Sweeney P, Park H, Baumann M, et al. Protein misfolding in neurodegenerative diseases: implications and strategies. Transl Neurodegener. 2017;6:6.
   PubMed Web of Science ®Google Scholar
• Henderson MX, Wirak GS, Zhang YQ, et al. Neuronal ceroid lipofuscinosis with DNAJC5/CSPalpha mutation has PPT1 pathology and exhibit aberrant protein palmitoylation. Acta Neuropathol. 2016;131(4):621–637.
   PubMed Web of Science ®Google Scholar
• Yao X, Liu X, Zhang Y, et al. Gene therapy of adult neuronal ceroid lipofuscinoses with crispr/cas9 in zebrafish. Hum Gene Ther. 2017;28(7):588–597.
   PubMed Web of Science ®Google Scholar
• Stoica L, Sena-Esteves M. adeno associated viral vector delivered rnai for gene therapy of sod1 amyotrophic lateral sclerosis. Front Mol Neurosci. 2016;9:56.
   PubMed Web of Science ®Google Scholar
• Castaneda JA, Pearce DA. Identification of alpha-fetoprotein as an autoantigen in juvenile Batten disease. Neurobiol Dis. 2008;29(1):92–102.
   PubMed Web of Science ®Google Scholar
• Ramirez-Montealegre D, Chattopadhyay S, Curran TM, et al. Autoimmunity to glutamic acid decarboxylase in the neurodegenerative disorder Batten disease. Neurology. 2005;64(4):743–745.
   PubMed Web of Science ®Google Scholar
• Lim MJ, Beake J, Bible E, et al. Distinct patterns of serum immunoreactivity as evidence for multiple brain-directed autoantibodies in juvenile neuronal ceroid lipofuscinosis. Neuropathol Appl Neurobiol. 2006;32(5):469–482.
   PubMed Web of Science ®Google Scholar
• Chattopadhyay S, Ito M, Cooper JD, et al. An autoantibody inhibitory to glutamic acid decarboxylase in the neurodegenerative disorder Batten disease. Hum Mol Genet. 2002;11(12):1421–1431.
   PubMed Web of Science ®Google Scholar
• Chattopadhyay S, Kriscenski-Perry E, Wenger DA, et al. An autoantibody to GAD65 in sera of patients with juvenile neuronal ceroid lipofuscinoses. Neurology. 2002;59(11):1816–1817.
   PubMed Web of Science ®Google Scholar
• Seehafer SS, Ramirez-Montealegre D, Wong AM, et al. Immunosuppression alters disease severity in juvenile Batten disease mice. J Neuroimmunol. 2011;230(1–2):169–172.
   PubMed Web of Science ®Google Scholar
• Arellano B, Graber DJ, Sentman CL. Regulatory T cell-based therapies for autoimmunity. Discov Med. 2016;22(119):73–80.
   PubMed Web of Science ®Google Scholar
• Yang B, Li S, Wang H, et al. Global CNS transduction of adult mice by intravenously delivered rAAVrh.8 and rAAVrh.10 and nonhuman primates by rAAVrh.10. Mol Ther. 2014;22(7):1299–1309.
   PubMed Web of Science ®Google Scholar
• Bemelmans AP, Duque S, Riviere C, et al. A single intravenous AAV9 injection mediates bilateral gene transfer to the adult mouse retina. PLoS One. 2013;8(4):e61618.
   PubMed Web of Science ®Google Scholar