Towards a new understanding of NCL pathogenesis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 10, 2015, Pages 2256-2261

  Cooper, Jonathan D ^a   Tarczyluk, Marta A ^a   Nelvagal, Hemanth R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Glial dysfunction; Neuronal ceroid lipofuscinosis; Pathogenesis; Selective neuron loss; Storage material accumulation

Indexed keywords

DISEASE MODEL; GENE MUTATION; GLIA CELL; HUMAN; LYSOSOME STORAGE DISEASE; NERVE CELL DEGENERATION; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW;

EID: 84940790807     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.05.014     Document Type: Review

References (111)

1. Anderson G.W., Goebel H.H., Simonati A. Human pathology in NCL. Biochim. Biophys. Acta 2013, 1832:1807-1826.
2. Arsov T., Smith K.R., Damiano J., Franceschetti S., Canafoglia L., Bromhead C.J., Andermann E., Vears D.F., Cossette P., Rajagopalan S., McDougall A., Sofia V., Farrell M., Aguglia U., Zini A., Meletti S., Morbin M., Mullen S., Andermann F., Mole S.E., Bahlo M., Berkovic S.F. Kufs disease, the major adult form of neuronal ceroid lipofuscinosis, caused by mutations in CLN6. Am. J. Hum. Genet. 2011, 88:566-573.
3. Awano T., Katz M.L., O'Brien D.P., Taylor J.F., Evans J., Khan S., Sohar I., Lobel P., Johnson G.S. A mutation in the cathepsin D gene (CTSD) in American Bulldogs with neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2006, 87:341-348.
4. Awano T., Katz M.L., O'Brien D.P., Sohar I., Lobel P., Coates J.R., Khan S., Johnson G.C., Giger U., Johnson G.S. A frame shift mutation in canine TPP1 (the ortholog of human CLN2) in a juvenile Dachshund with neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2006, 89:254-260.
5. Bible E., Gupta P., Hofmann S.L., Cooper J.D. Regional and cellular neuropathology in the palmitoyl protein thioesterase-1 (PPT1) null mutant mouse model of infantile neuronal ceroid lipofuscinosis. Neurobiol. Dis. 2004, 16:346-359.
6. Bond M., Holthaus S.M., Tammen I., Tear G., Russell C. Use of model organisms for the study of neuronal ceroid lipofuscinosis. Biochim. Biophys. Acta 2013, 1832:1842-1865.
7. Braak H., Del Tredici K. Alzheimer's pathogenesis: is there neuron-to-neuron propagation?. Acta Neuropathol. 2011, 121:589-595.
8. Bras J., Verloes A., Schneider S.A., Mole S.E., Guerreiro R.J. Mutation of the parkinsonism gene ATP13A2 causes neuronal ceroid-lipofuscinosis. Hum. Mol. Genet. 2012, 21:2646-2650.
9. Brooks H., Van Trigt L., Nelvagal H.R., Micsenyi M., Walkley S.U., Cooper J.D. Defining the onset and progression of neuropathological changes in mouse models of LINCL. NCL2014 poster presentation P10. Medicina 2014, 74(Suppl. II):26.
10. Broom M.F., Zhou C., Broom J.E., Barwell K.J., Jolly R.D., Hill D.F. Ovine neuronal ceroid lipofuscinosis: a large animal model syntenic with the human neuronal ceroid lipofuscinosis variant CLN6. J. Med. Genet. 1998, 35:717-721.
11. Burkovetskaya M., Karpuk N., Xiong J., Bosch M., Boska M.D., Takeuchi H., Suzumura A., Kielian T. Evidence for aberrant astrocyte hemichannel activity in Juvenile Neuronal Ceroid Lipofuscinosis (JNCL). PLoS One 2014, 9:e95023. 10.1371/journal.pone.0095023. eCollection 2014.
12. Cárcel-Trullols J., Kovács A.D., Pearce D.A. Cell biology of the NCL proteins: what they do and don't do. Biochim. Biophys. Acta 2015, 1852:2242-2255.
13. Chang M., Cooper J.D., Sleat D.E., Cheng S.H., Dodge J.C., Passini M.A., Lobel P., Davidson B.L. Intraventricular enzyme replacement improves disease phenotypes in a mouse model of late Infantile Neuronal Ceroid Lipofuscinosis. Mol. Ther. 2008, 16:649-656.
14. Chattopadhyay S., Ito M., Cooper J.D., Brooks A.I., Curran T.M., Powers J.M., Pearce D.A. An autoantibody inhibitory to glutamic acid decarboxylase in the neurodegenerative disorder Batten Disease. Hum. Mol. Genet. 2002, 11:1421-1431.
15. Cooper J.D. The neuronal ceroid lipofuscinoses: the same, but different?. Biochem. Soc. Trans. 2010, 38:1448-1452.
16. Cooper J.D., Messer A., Feng A.K., Chua-Couzens J., Mobley W.C. Apparent loss and hypertrophy of interneurons in a mouse model of neuronal ceroid lipofuscinosis: evidence for partial response to insulin-like growth factor-1 treatment. J. Neurosci. 1999, 19:2556-2567.
17. Cooper J.D., Russell C.R., Mitchison H.M. Progress towards understanding disease mechanisms in small vertebrate models of neuronal ceroid lipofuscinosis. Biochim. Biophys. Acta 2006, 1762:873-889.
18. Cooper J.D., Parviainen L., Dihanich S., Lange J., Anderson G., Van Trigt L., Williams B.P. Assessing the contribution of glial dysfunction to NCL pathogenesis. NCL2014 oral presentation P12. Medicina 2014, 74(Suppl. II):15.
19. Cooper J.D., Brooks H.R., Nelvagal H.R. Quantifying storage material accumulation in tissue sections. Methods Cell Biol. 2015, 126:349-356. (Epub 2015 Jan 19). 10.1016/bs.mcb.2014.11.010.
20. Cotman S.L., Vrbanac V., Lebel L.A., Lee R.L., Johnson K.A., Donahue L.R., Teed A.M., Antonellis K., Bronson R.T., Lerner T.J., MacDonald M.E. Cln3(Deltaex7/8) knock-in mice with the common JNCL mutation exhibit progressive neurologic disease that begins before birth. Hum. Mol. Genet. 2002, 11:2709-2721.
21. Damme M., Brandenstein L., Fehr S., Jankowiak W., Bartsch U., Schweizer M., Hermans-Borgmeyer I., Storch S. Gene disruption of Mfsd8 in mice provides the first animal model for CLN7 disease. Neurobiol. Dis. 2014, 65:12-24.
22. Drögemüller C., Johnson G.S., Katz M.L., Lingaas F., Palmer D.N., Tammen I. Large Animal Models. Chapter 18 in the Neuronal Ceroid Lipofuscinoses (Batten Disease) 2011, Oxford University Press. S.E. Mole, R.E. Williams, H.H. Goebel (Eds.).
23. Faller K.M., Gutierrez-Quintana R., Mohammed A., Rahim A.A., Tuxworth R.I., Wager K., Bond M. The neuronal ceroid lipofuscinoses: Opportunities from model systems. Biochim Biophys. Acta 2015 Apr 29, pii: S0925-4439(15)00128-3. http://dx.doi.org/10.1016/j.bbadis.2015.04.022. [Epub ahead of print] Review. PMID: 25937302.
24. Fan N., Lai L. Genetically modified pig models for human diseases. J. Genet. Genomics 2013, 40:67-73.
25. Flisikowska T., Kind A., Schnieke A. Genetically modified pigs to model human diseases. J. Appl. Genet. 2014, 55:53-64.
26. Fornito A., Zalesky A., Breakspear M. The connectomics of brain disorders. Nat. Rev. Neurosci. 2015, 16:159-172.
27. Frugier T., Mitchell N.L., Tammen I., Houweling P.J., Arthur D.G., Kay G.W., van Diggelen O.P., Jolly R.D., Palmer D.N. A new large animal model of CLN5 neuronal ceroid lipofuscinosis in Borderdale sheep is caused by a nucleotide substitution at a consensus splice site (c.571+1G>A) leading to excision of exon 3. Neurobiol. Dis. 2008, 29:306-315.
28. Fukumura S., Saito Y., Saito T., Komaki H., Nakagawa E., Sugai K., Sasaki M., Oka A., Takamisawa I. Progressive conduction defects and cardiac death in late infantile neuronal ceroid lipofuscinosis. Dev. Med. Child Neurol. 2012, 54:663-666.
29. Gao H., Boustany R.M., Espinola J.A., Cotman S.L., Srinidhi L., Antonellis K.A., Gillis T., Qin X., Liu S., Donahue L.R., Bronson R.T., Faust J.R., Stout D., Haines J.L., Lerner T.J., MacDonald M.E. Mutations in a novel CLN6-encoded transmembrane protein cause variant neuronal ceroid lipofuscinosis in man and mouse. Am. J. Hum. Genet. 2006, 70:324-335.
30. Gillingwater T.H., Wishart T.M. Mechanisms underlying synaptic vulnerability and degeneration in neurodegenerative disease. Neuropathol. Appl. Neurobiol. 2013, 39:320-334.
31. Griffey M., Bible E., Vogler C., Levy B., Gupta P., Cooper J.D., Sands M.S. Adeno-associated virus 2-mediated gene therapy decreases autofluorescent storage material and increases brain mass in a murine model of Infantile Neuronal Ceroid Lipofuscinosis (INCL). Neurobiol. Dis. 2004, 16:360-369.
32. Griffey M.A., Wozniak D., Wong M., Bible E., Johnson K., Rothman M.R., Wentz A.E., Cooper J.D., Sands M.S. CNS-directed AAV2-mediated gene therapy ameliorates functional deficits in a murine model of infantile neuronal ceroid lipofuscinosis. Mol. Ther. 2006, 13:538-547.
33. Groh J., Kühl T.G., Duckett S., Ip C.W., Mirza M., Langmann T., Nelvagal H.R., Sri S., Cooper J.D., Martini R. Immune cells mediate neuronal damage in a mouse model of Infantile Neuronal Ceroid Lipofuscinosis. Brain 2013, 136:1083-1101.
34. Groh J., Stadler D., Crocker P., Martini R. Sialoadhesin-positive microglia/macrophages promote neuroinflammation and axonal perturbation in the retinotectal system of two mouse models of neuronal ceroid lipofuscinosis. NCL2014 oral presentation P15. Medicina 2014, 74(Suppl. II):15.
35. Gupta P., Soyombo A.A., Atashband A., Wisniewski K.E., Shelton J.M., Richardson J.A., Hammer R.E., Hofmann S.L. Disruption of PPT1 or PPT2 causes neuronal ceroid lipofuscinosis in knockout mice. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13566-13571.
36. Hofman I.L., van der Wal A.C., Dingemans K.P., Becker A.E. Cardiac pathology in neuronal ceroid lipofuscinoses-a clinicopathologic correlation in three patients. Eur. J. Paediatr. Neurol. 2001, 5(Suppl. A):213-217.
37. Hu J., Lu J.-Y., Wong A.M.S., Hynan L.S., Birnbaum S.G., Yilmaz D.S., Streit B.M., Lenartowicz E.M., Thompson T.C.M., Cooper J.D., Hofmann S.L. 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, 107:213-221.
38. Katz M.L., Khan S., Awano T., Shahid S.A., Siakotos A.N., Johnson G.S. A mutation in the CLN8 gene in English Setter dogs with neuronal ceroid-lipofuscinosis. Biochem. Biophys. Res. Commun. 2005, 327:541-547.
39. Kielar C., Maddox L., Bible E., Pontikis C.C., Macauley S.L., Griffey M.A., Wong M., Sands M.S., Cooper J.D. Successive neuron loss in the thalamus and cortex in a mouse model of infantile neuronal ceroid lipofuscinosis. Neurobiol. Dis. 2007, 25:150-162.
40. Kielar C., Wishart T.M., Palmer A., Dihanich S., Wong A.M., Macauley S.L., Chan C.H., Sands M.S., Pearce D.A., Cooper J.D., Gillingwater T.H. Molecular correlates of axonal and synaptic pathology in mouse models of Batten disease. Hum. Mol. Genet. 2009, 18:4066-4080.
41. Kielian T. Therapeutic targeting of neuroinflammatory pathways in juvenile Batten disease. NCL2014 oral presentation P14. Medicina 2014, 74(Suppl. II):15.
42. Kim S.J., Zhang Z., Sarkar C., Tsai P.C., Lee Y.C., Dye L., Mukherjee A.B. Palmitoyl protein thioesterase-1 deficiency impairs synaptic vesicle recycling at nerve terminals, contributing to neuropathology in humans and mice. J. Clin. Invest. 2008, 118:3075-3086.
43. Koch S., Molchanova S.M., Wright A.K., Edwards A., Cooper J.D., Taira T., Gillingwater T.H., Tyynelä J. Morphological and functional correlates of synaptic pathology in the cathepsin D knock-out mouse model of congenital neuronal ceroid-lipofuscinosis. J. Neuropathol. Exp. Neurol. 2011, 70:1089-1096.
44. Koike M., Nakanishi H., Saftig P., Ezaki J., Isahara K., Ohsawa Y., Schulz-Schaeffer W., Watanabe T., Waguri S., Kametaka S., Shibata M., Yamamoto K., Kominami E., Peters C., von Figura K., Uchiyama Y. Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons. J. Neurosci. 2000, 20:6898-6906.
45. Kollmann K., Uusi-Rauva K., Scifo E., Tyynelä J., Jalanko A., Braulke T. Cell biology and function of neuronal ceroid lipofuscinosis-related proteins. Biochim. Biophys. Acta 2013, 1832:1866-1881.
46. Kopra O., Vesa J., von Schantz C., Manninen T., Minye H., Fabritius A.L., Rapola J., van Diggelen O.P., Saarela J., Jalanko A., Peltonen L. A mouse model for Finnish variant late infantile neuronal ceroid lipofuscinosis, CLN5, reveals neuropathology associated with early aging. Hum. Mol. Genet. 2004, 13:2893-2906.
47. Kovács A.D., Saje A., Wong A., Szénási G., Kiricsi P., Szabó E., Cooper J.D., Pearce D.A. Temporary inhibition of AMPA receptors induces a prolonged improvement of motor performance in a mouse model of juvenile Batten disease. Neuropharmacology 2011, 60:405-409.
48. Kovács A.D., Saje A., Wong A.M.S., Ramji S., Cooper J.D., Pearce D.A. Age-dependent therapeutic effect of memantine in a mouse model of juvenile Batten disease. Neuropharmacology 2012, 3:769-775.
49. Kuronen M., Lehesjoki A.-E., Jalanko A., Cooper J.D., Kopra O. Selective spatiotemporal patterns of glial activation and neuron loss in the sensory thalamocortical pathways of neuronal ceroid lipofuscinosis 8 mice. Neurobiol. Dis. 2012, 47:444-457.
50. Lange J., Cooper J.D., Williams B.P., Anderson G. Evidence for impaired glial biology in infantile NCL. NCL2014 poster presentation P1. Medicina 2014, 74(Suppl. II):24.
51. Levin S.W., Baker E.H., Zein W.M., Zhang Z., Quezado Z.M., Miao N., Gropman A., Griffin K.J., Bianconi S., Chandra G., Khan O.I., Caruso R.C., Liu A., Mukherjee A.B. Oral cysteamine bitartrate and N-acetylcysteine for patients with infantile neuronal ceroid lipofuscinosis: a pilot study. Lancet Neurol. 2014, 13:777-787.
52. Lim M.J., Alexander N.A., Benedict J.W., Chattopadhyay S., Shemilt S.J.A., Guérin C.J., Cooper J.D., Pearce D.A. IgG entry and deposition are components of the neuroimmune response Batten Disease. Neurobiol. Dis. 2007, 25:239-251.
53. Lu J.Y., Hu J., Hofmann S.L. Human recombinant palmitoyl-protein thioesterase-1 (PPT1) for preclinical evaluation of enzyme replacement therapy for infantile neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2010, 99:374-378.
54. Lu J.Y., Nelvagal H.R., Wang L., Birnbaum S.G., Cooper J.D., Hofmann S.L. Intrathecal enzyme replacement therapy improves motor function and survival in a preclinical mouse model of infantile neuronal ceroid lipofuscinosis. Mol. Genet. Metab 2015 May 12, pii: S1096-7192(15)30012-3. http://dx.doi.org/10.1016/j.ymgme.2015.05.005. [Epub ahead of print] PMID: 25982063.
55. Macauley S.L., Wozniak D.F., Kielar C., Tan Y., Cooper J.D., Sands M.S. Cerebellar pathology and motor deficits in the palmitoyl protein thioesterase 1-deficient mouse. Exp. Neurol. 2009, 217:124-135.
56. Macauley S.L., Roberts M.S., Wong A.M.S., McSloy F., Reddy A.S., Cooper J.D., Sands M.S. Synergistic effects of CNS-directed gene therapy and bone marrow transplantation in the murine model of infantile neuronal ceroid lipofuscinosis. Ann. Neurol. 2012, 71:797-804.
57. Melville S.A., Wilson C.L., Chiang C.S., Studdert V.P., Lingaas F., Wilton A.N. A mutation in canine CLN5 causes neuronal ceroid lipofuscinosis in Border collie dogs. Genomics 2005, 86:287-294.
58. Meng Y., Sohar I., Wang L., Sleat D.E., Lobel P. Systemic administration of tripeptidyl peptidase I in a mouse model of late infantile neuronal ceroid lipofuscinosis: effect of glycan modification. PLoS One 2012, 7:e40509.
59. Meng Y., Sohar I., Sleat D.E., Richardson J.R., Reuhl K.R., Jenkins R.B., Sarkar G., Lobel P. Effective intravenous therapy for neurodegenerative disease with a therapeutic enzyme and a peptide that mediates delivery to the brain. Mol. Ther. 2014, 22:547-553.
60. Mitchison H.M., Bernard D.J., Greene N.D.E., Cooper J.D., Junaid M.A., Pullarkat R.K., Vos N., Breuning M.H., Owens J.W., Mobley W.C., Gardiner R.M., Lake B.D., Taschner P.E.M., Nussbaum R.L. Targeted disruption of the Cln3 gene provides a mouse model for Batten Disease. The Batten Mouse Model Consortium. Neurobiol. Dis. 1999, 6:321-334.
61. Mitchison H.M., Lim M.J., Cooper J.D. Selectivity and types of cell death in the Neuronal Ceroid Lipofuscinoses (NCLs). Brain Pathol. 2004, 14:86-96.
62. Mole S.E., Cotman S.L. Genetics of the Neuronal Ceroid Lipofuscinoses (Batten disease). Biochim. Biophys. Acta 2015 May 27, 1852:2237-2241.
63. Morgan J.P., Magee H., Wong A., Nelson T., Koch B., Cooper J.D., Weimer J.M. A murine model of variant late infantile ceroid lipofuscinosis recapitulates behavioral and pathological phenotypes of human disease. PLoS One Nov 1 2013, 8(11):e78694. 10.1371/journal.pone.0078694.
64. Nelvagal H.R., Dmytrus J., Sri S., Dearborn J., Sands M.S., Cooper J.D. Defining of the nature and progression of spinal cord and brainstem pathology in Ppt1-/- mice. NCL2014 oral presentation P17. Medicina 2014, 74(Suppl. II):16.
65. Neverman N.J., Best H.L., Hofmann S.L., Hughes S.M. Experimental therapies in the neuronal ceroid lipofuscinoses. Biochim. Biophys. Acta 2015 May 6, 1852:2292-2300.
66. Nosková L., Stránecký V., Hartmannová H., Přistoupilová A., Barešová V., Ivánek R., Hůlková H., Jahnová H., van der Zee J., Staropoli J.F., Sims K.B., Tyynelä J., Van Broeckhoven C., Nijssen P.C., Mole S.E., Elleder M., Kmoch M.S. Mutations in DNAJC5, encoding cysteine-string protein alpha, cause autosomal-dominant adult-onset neuronal ceroid lipofuscinosis. Am. J. Hum. Genet. 2011, 89:241-252.
67. Ostergaard J.R., Rasmussen T.B., Mølgaard H. Cardiac involvement in juvenile neuronal ceroid lipofuscinosis (Batten disease). Neurology 2011, 76:1245-1251.
68. Oswald M.J., Palmer D.N., Kay G.W., Shemilt S.J.A., Rezaie P., Cooper J.D. Glial activation spreads from specific cerebral foci and precedes neurodegeneration in presymptomatic ovine neuronal ceroid lipofuscinosis (CLN6). Neurobiol. Dis. 2005, 20:49-63.
69. Oswald M.J., Palmer D.N., Kay G.W., Barwell K.J., Cooper J.D. Location and connectivity determine GABAergic interneuron survival in the brains of South Hampshire sheep with CLN6 neuronal ceroid lipofuscinosis. Neurobiol. Dis. 2008, 32:50-65.
70. Palmer D.N., Oswald M.J., Westlake V.J., Kay G.W. The origin of fluorescence in the neuronal ceroid lipofuscinoses (Batten disease) and neuron cultures from affected sheep for studies of neurodegeneration. Arch. Gerontol. Geriatr. 2002, 34:343-357.
71. Palmer D.N., Barry L.A., Tyynelä J., Cooper J.D. NCL disease mechanisms. Biochim. Biophys. Acta 2013, 1832:1882-1893.
72. Palmer D.N., Neverman N.J., Chen J.Z., Chang C.-T., Houweling P.J., Barry L.A., Tammen I., Hughes S.M., Mitchell N.L. Recent studies of ovine neuronal ceroid lipofuscinoses from BARN, the Batten Animal Research Network. Biochim. Biophys. Acta 2015, 1852:2279-2286.
73. Partanen S., Haapanen A., Kielar C., Pontikis C., Alexander N., Inkinen T., Saftig P., Gillingwater T.H., Cooper J.D., Tyynelä J. Synaptic changes in the thalamocortical system of cathepsin D-deficient mice: a model of human congenital neuronal ceroid-lipofuscinosis. J. Neuropathol. Exp. Neurol. 2008, 67:16-29.
74. Passini M.A., Dodge J.C., Bu J., Yang W., Zhao Q., Sondhi D., Hackett N.R., Kaminsky S.M., Mao Q., Shihabuddin L.S., Cheng S.H., Sleat D.E., Stewart G.R., Davidson B.L., Lobel P., Crystal R.G. Intracranial delivery of CLN2 reduces brain pathology in a mouse model of classical late infantile neuronal ceroid lipofuscinosis. J. Neurosci. 2006, 26:1334-1342.
75. Pontikis C.C., Cella C.V., Parihar N., Lim M.J., Chakrabarti S., Mitchison H.M., Mobley W.C., Rezaie P., Pearce D.A., Cooper J.D. Late onset neurodegeneration in the Cln3-/- mouse model of juvenile neuronal ceroid lipofuscinosis is preceded by low level glial activation. Brain Res. 2004, 1023:231-242.
76. Pontikis C.C., Cotman S.L., MacDonald M.E., Cooper J.D. Thalamocortical neuron loss and localized astrocytosis in the Cln3δex7/8 knock-in mouse model of Batten disease. Neurobiol. Dis. 2005, 20:823-836.
77. Radke J., Stenzel W., Goebel H.H. Human NCL Neuropathology. Biochim. Biophys. Acta 2015 May 16, 1852:2262-2266.
78. Raj A., Kuceyeski A., Weiner M. A network diffusion model of disease progression in dementia. Neuron 2012, 73:1204-1215.
79. Ranta S., Zhang Y., Ross B., Lonka L., Takkunen E., Messer A., Sharp J., Wheeler R., Kusumi K., Mole S., Liu W., Soares M.B., Bonaldo M.F., Hirvasniemi A., de la Chapelle A., Gilliam T.C., Lehesjoki A.E. The neuronal ceroid lipofuscinoses in human EPMR and mnd mutant mice are associated with mutations in CLN8. Nat. Genet. 1999, 23:233-236.
80. Sarkar C., Chandra G., Peng S., Zhang Z., Liu A., Mukherjee A.B. Neuroprotection and lifespan extension in Ppt1(-/-) mice by NtBuHA: therapeutic implications for INCL. Nat. Neurosci. 2013, 16:1608-1617.
81. Schulz A., Kohlschütter A., Mink J., Simonati A., Williams R. NCL diseases - clinical perspectives. Biochim. Biophys. Acta 2013, 1832:1801-1806.
82. Schmiedt M.-L., Blom T., Blom T., Kopra O., Wong A.M.S., von Schantz-Fant C., Ikonen E., Kuronen M., Jauhiainen M., Cooper J.D., Jalanko A. Cln5-deficiency in mice leads to microglial activation, defective myelination and changes in lipid metabolism. Neurobiol. Dis. 2012, 46:19-29.
83. Seehafer S.S., Ramirez-Montealegre D., Wong A.M., Chan C.H., Castaneda J., Horak M., Ahmadi S.M., Lim M.J., Cooper J.D., Pearce D.A. Immunosuppression alters disease severity in juvenile Batten disease mice. J. Neuroimmunol. 2011, 230:169-172.
84. Shacka J.J. Mouse models of neuronal ceroid lipofuscinoses: useful pre-clinical tools to delineate disease pathophysiology and validate therapeutics. Brain Res. Bull. 2012, 88:43-57.
85. Simonati A., Pezzini F., Moro F., Santorelli F.M. Neuronal Ceroid Lipofuscinosis: The Increasing Spectrum of an Old Disease. Curr. Mol. Med 2014 Oct 10, [Epub ahead of print] PMID: 25323868.
86. Sleat D.E., Wiseman J.A., El-Banna M., Kim K.H., Mao Q., Price S., Macauley S.L., Sidman R.L., Shen M.M., Zhao Q., Passini M.A., Davidson B.L., Stewart G.R., Lobel P. 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, 24:9117-9126.
87. Smith K.R., Damiano J., Franceschetti S., Carpenter S., Canafoglia L., Morbin M., Rossi G., Pareyson D., Mole S.E., Staropoli J.F., Sims K.B., Lewis J., Lin W.L., Dickson D.W., Dahl H.H., Bahlo M., Berkovic S.F. Strikingly different clinicopathological phenotypes determined by progranulin-mutation dosage. Am. J. Hum. Genet. 2012, 90:1102-1107.
88. Smith K.R., Dahl H.H., Canafoglia L., Andermann E., Damiano J., Morbin M., Bruni A.C., Giaccone G., Cossette P., Saftig P., Grötzinger J., Schwake M., Andermann F., Staropoli J.F., Sims K.B., Mole S.E., Franceschetti S., Alexander N.A., Cooper J.D., Chapman H.A., Carpenter S., Berkovic S.F., Bahlo M. Cathepsin F mutations cause type B Kufs disease, an adult-onset neuronal ceroid lipofuscinosis. Hum. Mol. Genet. 2013, 22:1417-1423.
89. Sohar I., Sleat D.E., Jadot M., Lobel P. Biochemical characterization of a lysosomal protease deficient in classical late infantile neuronal ceroid lipofuscinosis (LINCL) and development of an enzyme-based assay for diagnosis and exclusion of LINCL in human specimens and animal models. J. Neurochem. 1999, 73:700-711.
90. Sondhi D., Hackett N.R., Peterson D.A., Stratton J., Baad M., Travis K.M., Wilson J.M., Crystal R.G. Enhanced survival of the LINCL mouse following CLN2 gene transfer using the rh.10 rhesus macaque-derived adeno-associated virus vector. Mol. Ther. 2007, 15:481-491.
91. Sondhi D., Peterson D.A., Edelstein A.M., del Fierro K., Hackett N.R., Crystal R.G. Survival advantage of neonatal CNS gene transfer for late infantile neuronal ceroid lipofuscinosis. Exp. Neurol. 2008, 213:18-27.
92. Staropoli J.F., Karaa A., Lim E.T., Kirby A., Elbalalesy N., Romansky S.G., Leydiker K.B., Coppel S.H., Barone R., Xin W., MacDonald M.E., Abdenur J.E., Daly M.J., Sims K.B., Cotman S.L. A homozygous mutation in KCTD7 links neuronal ceroid lipofuscinosis to the ubiquitin-proteasome system. Am. J. Hum. Genet. 2012, 91:202-208.
93. Tamaki S.J., Jacobs Y., Dohse M., Capela A., Cooper J.D., Reitsma M., He D., Tushinski R., Belichenko P.V., Salehi A., Mobley W.C., Gage F.H., Huhn S., Tsukamoto A.S., Weissman I.L., Uchida N. Neuroprotection of host cells by human central nervous system-stem cells in a mouse model of infantile neuronal ceroid lipofuscinosis. Cell Stem Cell 2009, 5:310-319.
94. Tammen I., Cook R.W., Nicholas F.W., Raadsma H.W. Neuronal ceroid lipofuscinosis in Australian Merino sheep: a new animal model. Eur. J. Paediatr. Neurol. 2001, 5(Suppl. A):37-41.
95. Tarczyluk M.A., Salzlechner C., Smith D., Lim M.J., Pearce D.A., Platt F.M., Williams B.P., Cooper J.D. Combination therapies for juvenile Batten disease. NCL2014 poster presentation P26. Medicina 2014, 74(Suppl. II):30.
96. Thelen M., Damme M., Schweizer M., Hagel C., Wong A.M.S., Cooper J.D., Braulke T., Galliciotti G. Autophagy, proteasomal degradation of mutant Cln6 and reactive gliosis are involved in the neuropathology of nclf mice. PLoS One 2012, 7:e35493. (Epub 2012 Apr 20).
97. Tomiyasu H., Takahashi W., Ohta T., Yoshii F., Shibuya M., Shinohara Y. An autopsy case of juvenile neuronal ceroid-lipofuscinosis with dilated cardiomyopathy. Rinsho Shinkeigaku 2000, 40:350-357.
98. Tyynelä J., Cooper J.D., Khan M.N., Shemilt S.J.A., Haltia M. Specific patterns of storage deposition, neurodegeneration, and glial activation in the hippocampus of patients with neuronal ceroid-lipofuscinoses. Brain Pathol. 2004, 14:349-357.
99. Verkruyse L.A., Hofmann S.L. Lysosomal targeting of palmitoyl-protein thioesterase. J. Biol. Chem. 1996, 271:15831-15836.
100. von Schantz C., Kielar C., Hansen S.N., Pontikis C.C., Alexander N.A., Kopra O., Jalanko A., Cooper J.D. Progressive thalamocortical neuron loss in Cln5 deficient mice: distinct effects in Finnish variant late infantile NCL. Neurobiol. Dis. 2009, 34:308-319.
101. Vuillemenot B.R., Kennedy D., Cooper J.D., Wong A.M.S., Sri S., Doeleman T., Katz M.L., Coates J.R., Johnson G.C., Reed R.P., Adams E.L., Butt M.T., Musson D.G., Henshaw J., Keve S., Cahayag R., Tsuruda L.S., O'Neill C.A. Nonclinical evaluation of CNS-administered TPP1 enzyme replacement in canine CLN2 neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2015, 114:281-293.
102. Warrier V., Vieira M., Mole S.E. Genetic basis and phenotypic correlations of the neuronal ceroid lipofusinoses. Biochim. Biophys. Acta 2013, 1832:1827-1830.
103. Weimer J.M., Custer A.W., Benedict J.W., Alexander N.A., Kingsley E., Federoff H.J., Cooper J.D., Pearce D.A. Visual deficits in a mouse model of Batten disease are the result of optic nerve degeneration and loss of dorsal lateral geniculate thalamic neurons. Neurobiol. Dis. 2006, 22:284-293.
104. Weimer J.M., Benedict J.W., Getty A.L., Pontikis C.C., Lim M.J., Cooper J.D., Pearce D.A. Cerebellar defects in a mouse model of juvenile neuronal ceroid lipofuscinosis. Brain Res. 2009, 1266:93-107.
105. Williams R.E., Mole S.E. New nomenclature and classification scheme for the neuronal ceroid lipofuscinoses. Neurology 2012, 79:183-191.
106. Williams R.E., Aberg L., Autti T., Goebel H.H., Kohlschütter A., Lönnqvist T. Diagnosis of the neuronal ceroid lipofuscinoses: an update. Biochim. Biophys. Acta 2006, 1762:865-872.
107. Wong A.M., Rahim A.A., Waddington S.N., Cooper J.D. Current therapies for the soluble lysosomal forms of neuronal ceroid lipofuscinosis. Biochem. Soc. Trans. 2010, 38:1484-1488.
108. Xiong J., Kielian T. Microglia in juvenile neuronal ceroid lipofuscinosis are primed toward a pro-inflammatory phenotype. J. Neurochem. 2013, 127:245-258.
109. Yates D. Neurodegenerative disease: neurodegenerative networking. Nat. Rev. Neurosci. 2012, 13:288-289.
110. Zhang Z., Butler J.D., Levin S.W., Wisniewski K.E., Brooks S.S., Mukherjee A.B. Lysosomal ceroid depletion by drugs: therapeutic implications for a hereditary neurodegenerative disease of childhood. Nat. Med. 2001, 7:478-484.
111. Roberts M.S., Macauley S.L., Wong A.M., Yilmas D., Hohm S., Cooper J.D., Sands M.S. 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. 10.1007/s10545-011-9446-x.