Experimental therapies in the neuronal ceroid lipofuscinoses

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 10, 2015, Pages 2292-2300

  Neverman, Nicole J ^a,b   Best, Hannah L ^a,b   Hofmann, Sandra L ^c   Hughes, Stephanie M ^a,b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b Batten Animal Research Network (BARN)   (New Zealand)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Batten disease; Cell therapy; Enzyme replacement therapy; Gene therapy; Neuronal ceroid lipofuscinosis; Small molecule therapy

Indexed keywords

CHAPERONE; GLUTAMATE RECEPTOR ANTAGONIST; IMMUNOMODULATING AGENT; LENTIVIRUS VECTOR; PARVOVIRUS VECTOR;

CLINICAL TRIAL (TOPIC); ENZYME REPLACEMENT; EXPERIMENTAL THERAPY; GENE THERAPY; HEMATOPOIETIC STEM CELL; HUMAN; NEURAL STEM CELL; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SMALL MOLECULE THERAPY; STEM CELL TRANSPLANTATION;

EID: 84940795360     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.04.026     Document Type: Review

References (102)

1. Abordo-Adesida E., Follenzi A., et al. Stability of lentiviral vector-mediated transgene expression in the brain in the presence of systemic antivector immune responses. Hum. Gene Ther. 2005, 16(6):741-751.
2. Autti T., Raininko R., et al. MRI of neuronal ceroid lipofuscinosis. II. Postmortem MRI and histopathological study of the brain in 16 cases of neuronal ceroid lipofuscinosis of juvenile or late infantile type. Neuroradiology 1997, 39(5):371-377.
3. Awano T., Katz M.L., et al. A frame shift mutation in canine TPP1 (the ortholog of human CLN2) in a juvenile Dachshund with neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2006, 89(3):254-260.
4. Awano T., Katz M.L., et al. A mutation in the cathepsin D gene (CTSD) in American bulldogs with neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2006, 87(4):341-348.
5. BioMarin BioMarin Provides Preliminary Data from Ongoing Phase 1/2 Pivotal Study of BMN190 for Treatment of CLN2 Disorder, a Form of Batten Disease 2014, (Retrieved 12 January, 2015).
6. Boelens J.J., Orchard P.J., et al. Transplantation in inborn errors of metabolism: current considerations and future perspectives. Br. J. Haematol. 2014, 167(3):293-303.
7. Brockstedt D.G., Podsakoff G.M., et al. Induction of immunity to antigens expressed by recombinant adeno-associated virus depends on the route of administration. Clin. Immunol. 1999, 92(1):67-75.
8. Broom M.F., Zhou C., et al. Ovine neuronal ceroid lipofuscinosis: a large animal model syntenic with the human neuronal ceroid lipofuscinosis variant CLN6. J. Med. Genet. 1998, 35(9):717-721.
9. Chang M., Cooper J.D., et al. Intraventricular enzyme replacement improves disease phenotypes in a mouse model of late infantile neuronal ceroid lipofuscinosis. Mol. Ther. 2008, 16(4):649-656.
10. Chattopadhyay S., Ito M., et al. An autoantibody inhibitory to glutamic acid decarboxylase in the neurodegenerative disorder Batten disease. Hum. Mol. Genet. 2002, 11(12):1421-1431.
11. Chen Y.H., Chang M., et al. Molecular signatures of disease brain endothelia provide new sites for CNS-directed enzyme therapy. Nat. Med. 2009, 15(10):1215-1218.
12. Chirmule N., Propert K., et al. Immune responses to adenovirus and adeno-associated virus in humans. Gene Ther. 1999, 6(9):1574-1583.
13. Chirmule N., Xiao W., et al. Humoral immunity to adeno-associated virus type 2 vectors following administration to murine and nonhuman primate muscle. J. Virol. 2000, 74(5):2420-2425.
14. Cook R.W., Jolly R.D., et al. Neuronal ceroid lipofuscinosis in Merino sheep. Aust. Vet. J. 2002, 80(5):292-297.
15. Cooper J.D., Russell C., et al. Progress towards understanding disease mechanisms in small vertebrate models of neuronal ceroid lipofuscinosis. Biochim. Biophys. Acta 2006, 1762(10):873-889.
16. Cronin J., Zhang X.Y., et al. Altering the tropism of lentiviral vectors through pseudotyping. Curr. Genet. Ther. 2005, 5(4):387-398.
17. Dawson G., Schroeder C., et al. Palmitoyl:protein thioesterase (PPT1) inhibitors can act as pharmacological chaperones in infantile Batten disease. Biochem. Biophys. Res. Commun. 2010, 395(1):66-69.
18. Fan J.Q. A counterintuitive approach to treat enzyme deficiencies: use of enzyme inhibitors for restoring mutant enzyme activity. Biol. Chem. 2008, 389(1):1-11.
19. FDA Guidance for Industry M3(R2) 2010.
20. Finotti A., Breda L., et al. Recent trends in the gene therapy of beta-thalassemia. J. Blood Med. 2015, 6:69-85.
21. Foley C.P., Rubin D.G., et al. Intra-arterial delivery of AAV vectors to the mouse brain after mannitol mediated blood brain barrier disruption. J. Control. Release 2014, 196:71-78.
22. Griffey M., Bible E., 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.
23. Griffey M., Macauley S.L., et al. AAV2-mediated ocular gene therapy for infantile neuronal ceroid lipofuscinosis. Mol. Ther. 2005, 12(3):413-421.
24. Griffey M.A., Wozniak D., 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.
25. Hacein-Bey-Abina S., Von Kalle C., et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003, 302(5644):415-419.
26. Haltia M. The neuronal ceroid-lipofuscinoses: from past to present. Biochim. Biophys. Acta 2006, 1762(10):850-856.
27. Haltia M., Goebel H.H. The neuronal ceroid-lipofuscinoses: a historical introduction. Biochim. Biophys. Acta 2013, 1832(11):1795-1800.
28. Harper P.A., Walker K.H., et al. Neurovisceral ceroid-lipofuscinosis in blind Devon cattle. Acta Neuropathol. 1988, 75(6):632-636.
29. Haskell R.E., Hughes S.M., 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.
30. Hernandez Y.J., Wang J., et al. Latent adeno-associated virus infection elicits humoral but not cell-mediated immune responses in a nonhuman primate model. J. Virol. 1999, 73(10):8549-8558.
31. Hu J., Lu J.Y., et al. Intravenous high-dose enzyme replacement therapy with recombinant palmitoyl-protein thioesterase reduces visceral lysosomal storage and modestly prolongs survival in a preclinical mouse model of infantile neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2012, 107(1-2):213-221.
32. Jolly R.D., Martinus R.D., et al. Sheep and other animals with ceroid-lipofuscinoses: their relevance to Batten disease. Am. J. Med. Genet. 1992, 42(4):609-614.
33. Jolly R.D., Sutton R.H., et al. Ceroid-lipofuscinosis in miniature Schnauzer dogs. Aust. Vet. J. 1997, 75(1):67.
34. Jolly R.D., West D.M. Blindness in South Hampshire sheep: a neuronal ceroid lipofuscinosis. N. Z. Vet. J. 1976, 24(6):123.
35. Kakkis E., McEntee M., et al. Intrathecal enzyme replacement therapy reduces lysosomal storage in the brain and meninges of the canine model of MPS I. Mol. Genet. Metab. 2004, 83(1-2):163-174.
36. Kato S., Kobayashi K., et al. A lentiviral strategy for highly efficient retrograde gene transfer by pseudotyping with fusion envelope glycoprotein. Hum. Gene Ther. 2011, 22(2):197-206.
37. Katz M.L., Coates J.R., et al. Enzyme replacement therapy attenuates disease progression in a canine model of late-infantile neuronal ceroid lipofuscinosis (CLN2 disease). J. Neurosci. Res. 2014, 92(11):1591-1598.
38. Katz M.L., Farias F.H., et al. A missense mutation in canine CLN6 in an Australian shepherd with neuronal ceroid lipofuscinosis. J. Biomed. Biotechnol. 2011, 2011:198042.
39. Kay G.W., Palmer D.N. Chronic oral administration of minocycline to sheep with ovine CLN6 neuronal ceroid lipofuscinosis maintains pharmacological concentrations in the brain but does not suppress neuroinflammation or disease progression. J. Neuroinflammation 2013, 10:97.
40. Khalili K., Gordon J., et al. Genome editing strategies: potential tools for eradicating HIV-1/AIDS. J. Neurovirol. 2015, Feb 26 2015.
41. Konitsiotis S., Blanchet P.J., et al. AMPA receptor blockade improves levodopa-induced dyskinesia in MPTP monkeys. Neurology 2000, 54(8):1589-1595.
42. Koppang N. The English setter with ceroid-lipofuscinosis: a suitable model for the juvenile type of ceroid-lipofuscinosis in humans. Am. J. Med. Genet. Suppl. 1988, 5:117-125.
43. Kousi M., Lehesjoki A.E., et al. Update of the mutation spectrum and clinical correlations of over 360 mutations in eight genes that underlie the neuronal ceroid lipofuscinoses. Hum. Mutat. 2012, 33(1):42-63.
44. Kovacs A.D., Pearce D.A. Attenuation of AMPA receptor activity improves motor skills in a mouse model of juvenile Batten disease. Exp. Neurol. 2008, 209(1):288-291.
45. Kovacs A.D., Saje A., et al. Temporary inhibition of AMPA receptors induces a prolonged improvement of motor performance in a mouse model of juvenile Batten disease. Neuropharmacology 2011, 60(2-3):405-409.
46. Lake B.D., Cavanagh N.P. Early-juvenile Batten's disease-a recognisable sub-group distinct from other forms of Batten's disease. Analysis of 5 patients. J. Neurol. Sci. 1978, 36(2):265-271.
47. Lake B.D., Steward C.G., et al. Bone marrow transplantation in late infantile Batten disease and juvenile Batten disease. Neuropediatrics 1997, 28(1):80-81.
48. Leinekugel P., Michel S., et al. Quantitative correlation between the residual activity of beta-hexosaminidase A and arylsulfatase A and the severity of the resulting lysosomal storage disease. Hum. Genet. 1992, 88(5):513-523.
49. Levin S.W., Baker E.H., et al. Oral cysteamine bitartrate and N-acetylcysteine for patients with infantile neuronal ceroid lipofuscinosis: a pilot study. Lancet Neurol. 2014, 13(8):777-787.
50. Lim M.J., Beake J., 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.
51. 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.
52. Linterman K.S., Palmer D.N., et al. Lentiviral-mediated gene transfer to the sheep brain: implications for gene therapy in Batten disease. Hum. Gene Ther. 2011, 22(8):1011-1020.
53. Linthorst G.E., De Rie M.A., et al. Misdiagnosis of Fabry disease: importance of biochemical confirmation of clinical or pathological suspicion. Br. J. Dermatol. 2004, 150(3):575-577.
54. Lonnqvist T., Vanhanen S.L., et al. Hematopoietic stem cell transplantation in infantile neuronal ceroid lipofuscinosis. Neurology 2001, 57(8):1411-1416.
55. Lu J.Y., Hu J., et al. Human recombinant palmitoyl-protein thioesterase-1 (PPT1) for preclinical evaluation of enzyme replacement therapy for infantile neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2010, 99(4):374-378.
56. Ma Y., Zhang X., et al. Generating rats with conditional alleles using CRISPR/Cas9. Cell Res. 2014, 24(1):122-125.
57. Macauley S.L., Roberts M.S., 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.
58. Martinus R.D., Harper P.A., et al. Bovine ceroid-lipofuscinosis (Batten's disease): the major component stored is the DCCD-reactive proteolipid, subunit C, of mitochondrial ATP synthase. Vet. Res. Commun. 1991, 15(2):85-94.
59. Masat E., Pavani G., et al. Humoral immunity to AAV vectors in gene therapy: challenges and potential solutions. Disc. Med. 2013, 15(85):379-389.
60. Mastakov M.Y., Baer K., et al. Immunological aspects of recombinant adeno-associated virus delivery to the mammalian brain. J. Virol. 2002, 76(16):8446-8454.
61. Mingozzi F., High K.A. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat. Rev. Genet. 2011, 12(5):341-355.
62. Mingozzi F., High K.A. Immune responses to AAV vectors: overcoming barriers to successful gene therapy. Blood 2013, 122(1):23-36.
63. Nightingale S.J., Hollis R.P., et al. Transient gene expression by nonintegrating lentiviral vectors. Mol. Ther. 2006, 13(6):1121-1132.
64. Oswald M.J., Palmer D.N., et al. Glial activation spreads from specific cerebral foci and precedes neurodegeneration in presymptomatic ovine neuronal ceroid lipofuscinosis (CLN6). Neurobiol. Dis. 2005, 20(1):49-63.
65. Palmer D.N., Jolly R.D., et al. Different patterns of hydrophobic protein storage in different forms of neuronal ceroid lipofuscinosis (NCL, Batten disease). Neuropediatrics 1997, 28(1):45-48.
66. Passini M.A., Dodge J.C., 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.
67. Pearce D.A. New animal models for the study of Batten disease. 14th International Conference on Neuronal Ceroid Lipofuscinoses (Batten Disease), Cordoba, Argentina 2014.
68. Pears M.R., Cooper J.D., et al. High resolution 1H NMR-based metabolomics indicates a neurotransmitter cycling deficit in cerebral tissue from a mouse model of Batten disease. J. Biol. Chem. 2005, 280(52):42508-42514.
69. Philippe S., Sarkis C., et al. Lentiviral vectors with a defective integrase allow efficient and sustained transgene expression in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(47):17684-17689.
70. Rahim A.A., Wong A.M., et al. In utero gene transfer to the mouse nervous system. Biochem. Soc. Trans. 2010, 38(6):1489-1493.
71. Rahim A.A., Wong A.M., et al. Efficient gene delivery to the adult and fetal CNS using pseudotyped non-integrating lentiviral vectors. Gene Ther. 2009, 16(4):509-520.
72. Ramachandran N., Girard J.M., et al. The autosomal recessively inherited progressive myoclonus epilepsies and their genes. Epilepsia 2009, 50(Suppl. 5):29-36.
73. Rider J.A., Rider D.L. Batten disease: past, present, and future. Am. J. Med. Genet. Suppl. 1988, 5:21-26.
74. Roberts M.S., Macauley S.L., 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.
75. Sands M.S., Davidson B.L. Gene therapy for lysosomal storage diseases. Mol. Ther. 2006, 13(5):839-849.
76. Schiffmann R., Heyes M.P., et al. Prospective study of neurological responses to treatment with macrophage-targeted glucocerebrosidase in patients with type 3 Gaucher's disease. Ann. Neurol. 1997, 42(4):613-621.
77. Schoderboeck L., Riad S., et al. Chimeric rabies SADB19-VSVg-pseudotyped lentiviral vectors mediate long-range retrograde transduction from the mouse spinal cord. Gene Ther. 2015, 22(5):357-364.
78. Schueler U.H., Kolter T., et al. Correlation between enzyme activity and substrate storage in a cell culture model system for Gaucher disease. J. Inherit. Metab. Dis. 2004, 27(5):649-658.
79. Schulz A., Kohlschutter A. NCL disorders: frequent causes of childhood dementia. Iran. J. Child Neurol. 2013, 7(1):1-8.
80. Sebastiano V., Maeder M.L., et al. In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases. Stem Cells 2011, 29(11):1717-1726.
81. Seehafer S.S., Ramirez-Montealegre D., et al. Immunosuppression alters disease severity in juvenile Batten disease mice. J. Neuroimmunol. 2011, 230(1-2):169-172.
82. Selden N.R., Al-Uzri A., et al. Central nervous system stem cell transplantation for children with neuronal ceroid lipofuscinosis. J. Neurosurg. Pediatr. 2013, 11(6):643-652.
83. Shevtsova Z., Garrido M., 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.
84. Sleat D.E., El-Banna M., et al. Residual levels of tripeptidyl-peptidase I activity dramatically ameliorate disease in late-infantile neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2008, 94(2):222-233.
85. Sleat D.E., Wiseman J.A., et al. A mouse model of classical late-infantile neuronal ceroid lipofuscinosis based on targeted disruption of the CLN2 gene results in a loss of tripeptidyl-peptidase I activity and progressive neurodegeneration. J. Neurosci. 2004, 24(41):9117-9126.
86. Sondhi D., Hackett N.R., 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.
87. Sondhi D., Johnson L., et al. Long-term expression and safety of administration of AAVrh.10hCLN2 to the brain of rats and nonhuman primates for the treatment of late infantile neuronal ceroid lipofuscinosis. Hum. Genet. Ther. Methods 2012, 23(5):324-335.
88. Souweidane M.M., Fraser J.F., et al. Gene therapy for late infantile neuronal ceroid lipofuscinosis: neurosurgical considerations. J. Neurosurg. Pediatr. 2010, 6(2):115-122.
89. Staropoli J.F., Haliw L., et al. Large-scale phenotyping of an accurate genetic mouse model of JNCL identifies novel early pathology outside the central nervous system. PLoS ONE 2012, 7(6):e38310.
90. Sun B., Bird A., et al. Enhanced response to enzyme replacement therapy in Pompe disease after the induction of immune tolerance. Am. J. Hum. Genet. 2007, 81(5):1042-1049.
91. Tamaki S.J., Jacobs Y., 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.
92. Taylor R.M., Farrow B.R. Ceroid lipofuscinosis in the border collie dog: retinal lesions in an animal model of juvenile Batten disease. Am. J. Med. Genet. 1992, 42(4):622-627.
93. Tecedor LK, Young W., Coates J.R., McBride J.L., Davidson B.L. Gene therapy for late infantile neuronal ceroid lipofuscinosis in large animal models. 14th International Conference on Neuronal Ceroid Lipofuscinoses (Batten Disease). Cordoba, Argentina, Medicina 2014.
94. Tyynela J., Sohar I., et al. Congenital ovine neuronal ceroid lipofuscinosis-a cathepsin D deficiency with increased levels of the inactive enzyme. Eur. J. Paediatr. Neurol. 2001, 5(Suppl. A):43-45.
95. Url A., Bauder B., et al. Equine neuronal ceroid lipofuscinosis. Acta Neuropathol. 2001, 101(4):410-414.
96. Valenzano K.J., Khanna R., et al. Identification and characterization of pharmacological chaperones to correct enzyme deficiencies in lysosomal storage disorders. Assay Drug Dev. Technol. 2011, 9(3):213-235.
97. Whiting R.E., Narfstrom K., et al. Enzyme replacement therapy delays pupillary light reflex deficits in a canine model of late infantile neuronal ceroid lipofuscinosis. Exp. Eye Res. 2014, 125:164-172.
98. Worgall S., Sondhi D., 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.
99. Wraith J.E., Clarke L.A., 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, 144(5):581-588.
100. Yin H., Xue W., et al. Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat. Biotechnol. 2014, 32(6):551-553.
101. Zhu W., Lei R., et al. The CRISPR/Cas9 system inactivates latent HIV-1 proviral DNA. Retrovirology 2015, 12(1):22.
102. Wong A.M., et al. Current therapies for the soluble lysosomal forms of neuronal ceroid lipofuscinosis. Biochem. Soc. Trans. 2010, 38(6):1484-1488.