Progressive Retinal Degeneration and Glial Activation in the CLN6nclf Mouse Model of Neuronal Ceroid Lipofuscinosis: A Beneficial Effect of DHA and Curcumin Supplementation

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Mirza, Myriam ^a,b   Volz, Cornelia ^a   Karlstetter, Marcus ^b   Langiu, Monica ^c   Somogyi, Aleksandra ^c   Ruonala, Mika O ^c   Tamm, Ernst R ^a   Jägle, Herbert ^b   Langmann, Thomas ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CURCUMIN; DOCOSAHEXAENOIC ACID; MESSENGER RNA;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE SEVERITY; ELECTRORETINOGRAPHY; EXPERIMENTAL MOUSE; GENE EXPRESSION; GLIA CELL; GLIOSIS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IMMUNOREGULATION; MICROGLIA; MORPHOLOGY; MORPHOMETRICS; MOUSE; MUELLER CELL; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; OPTOKINETIC STIMULATION; PHENOTYPE; PHOTORECEPTOR; RETINA DEGENERATION; RNA GENE;

ANIMALS; CURCUMIN; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; MICE; NEURONAL CEROID-LIPOFUSCINOSES; RETINA;

EID: 84885062246     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075963     Document Type: Article

References (43)

1. Haltia M, (2003) The neuronal ceroid-lipofuscinoses. J Neuropathol Exp Neurol 62: 1-13.
2. Jalanko A, Braulke T, (2009) Neuronal ceroid lipofuscinoses. Biochim Biophys Acta 1793: 697-709.
3. Siintola E, Lehesjoki AE, Mole SE, (2006) Molecular genetics of the NCLs-status and perspectives. Biochim Biophys Acta 1762: 857-864.
4. Kousi M, Lehesjoki AE, Mole SE, (2012) Update of the mutation spectrum and clinical correlations of over 360 mutations in eight genes that underlie the neuronal ceroid lipofuscinoses. Hum Mutat 33: 42-63.
5. Goebel HH, Schochet SS, Jaynes M, Bruck W, Kohlschutter A, et al. (1999) Progress in neuropathology of the neuronal ceroid lipofuscinoses. Mol Genet Metab 66: 367-372.
6. Haltia M, (2006) The neuronal ceroid-lipofuscinoses: from past to present. Biochim Biophys Acta 1762: 850-856.
7. Kohlschutter A, Gardiner RM, Goebel HH, (1993) Human forms of neuronal ceroid-lipofuscinosis (Batten disease): consensus on diagnostic criteria, Hamburg 1992. J Inherit Metab Dis 16: 241-244.
8. Tarkkanen A, Haltai M, Merenmies L, (1977) Ocular pathology in infantile type of neuronal ceroid-lipofuscinosis. J Pediatr Ophthalmol 14: 235-241.
9. Gao H, Boustany RM, Espinola JA, Cotman SL, Srinidhi L, et al. (2002) Mutations in a novel CLN6-encoded transmembrane protein cause variant neuronal ceroid lipofuscinosis in man and mouse. Am J Hum Genet 70: 324-335.
10. Wheeler RB, Sharp JD, Schultz RA, Joslin JM, Williams RE, et al. (2002) The gene mutated in variant late-infantile neuronal ceroid lipofuscinosis (CLN6) and in nclf mutant mice encodes a novel predicted transmembrane protein. Am J Hum Genet 70: 537-542.
11. Arsov T, Smith KR, Damiano J, Franceschetti S, Canafoglia L, et al. (2011) Kufs disease, the major adult form of neuronal ceroid lipofuscinosis, caused by mutations in CLN6. Am J Hum Genet 88: 566-573.
12. Bronson RT, Donahue LR, Johnson KR, Tanner A, Lane PW, et al. (1998) Neuronal ceroid lipofuscinosis (nclf), a new disorder of the mouse linked to chromosome 9. Am J Med Genet 77: 289-297.
13. Thelen M, Damme M, Schweizer M, Hagel C, Wong AM, et al. (2012) Disruption of the autophagy-lysosome pathway is involved in neuropathology of the nclf mouse model of neuronal ceroid lipofuscinosis. PLoS One 7: e35493.
14. Oswald MJ, Palmer DN, Kay GW, Shemilt SJ, Rezaie P, et al. (2005) Glial activation spreads from specific cerebral foci and precedes neurodegeneration in presymptomatic ovine neuronal ceroid lipofuscinosis (CLN6). Neurobiol Dis 20: 49-63.
15. Groh J, Kuhl TG, Ip CW, Nelvagal HR, Sri S, et al. (2013) Immune cells perturb axons and impair neuronal survival in a mouse model of infantile neuronal ceroid lipofuscinosis. Brain 136: 1083-1101.
16. Jang S, Johnson RW, (2010) Can consuming flavonoids restore old microglia to their youthful state? Nutr Rev 68: 719-728.
17. Jung KK, Lee HS, Cho JY, Shin WC, Rhee MH, et al. (2006) Inhibitory effect of curcumin on nitric oxide production from lipopolysaccharide-activated primary microglia. Life Sci 79: 2022-2031.
18. Jin CY, Lee JD, Park C, Choi YH, Kim GY, (2007) Curcumin attenuates the release of pro-inflammatory cytokines in lipopolysaccharide-stimulated BV2 microglia. Acta Pharmacol Sin 28: 1645-1651.
19. Antonietta Ajmone-Cat M, Lavinia Salvatori M, De Simone R, Mancini M, Biagioni S, et al. (2012) Docosahexaenoic acid modulates inflammatory and antineurogenic functions of activated microglial cells. J Neurosci Res 90: 575-587.
20. Ebert S, Weigelt K, Walczak Y, Drobnik W, Mauerer R, et al. (2009) Docosahexaenoic acid attenuates microglial activation and delays early retinal degeneration. J Neurochem 110: 1863-1875.
21. Mattapallil MJ, Wawrousek EF, Chan CC, Zhao H, Roychoudhury J, et al. (2012) The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Invest Ophthalmol Vis Sci 53: 2921-2927.
22. Prusky GT, Alam NM, Beekman S, Douglas RM, (2004) Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45: 4611-4616.
23. Douglas RM, Alam NM, Silver BD, McGill TJ, Tschetter WW, et al. (2005) Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system. Vis Neurosci 22: 677-684.
24. Hlawatsch J, Karlstetter M, Aslanidis A, Luckoff A, Walczak Y, et al. (2013) Sterile alpha motif containing 7 (samd7) is a novel crx-regulated transcriptional repressor in the retina. PLoS One 8: e60633.
25. Miller JN, Chan CH, Pearce DA, (2013) The role of nonsense-mediated decay in neuronal ceroid lipofuscinosis. Hum Mol Genet 22: 2723-2734.
26. McGill TJ, Prusky GT, Douglas RM, Yasumura D, Matthes MT, et al. (2012) Discordant anatomical, electrophysiological, and visual behavioral profiles of retinal degeneration in rat models of retinal degenerative disease. Invest Ophthalmol Vis Sci 53: 6232-44.
27. Kanninen KM, Grubman A, Caragounis A, Duncan C, Parker SJ, et al. (2013) Altered biometal homeostasis is associated with CLN6 mRNA loss in mouse neuronal ceroid lipofuscinosis. Biol Open 2: 635-646.
28. Staropoli JF, Haliw L, Biswas S, Garrett L, Holter SM, et al. (2012) Large-scale phenotyping of an accurate genetic mouse model of JNCL identifies novel early pathology outside the central nervous system. PLoS One 7: e38310.
29. Lei B, Tullis GE, Kirk MD, Zhang K, Katz ML, (2006) Ocular phenotype in a mouse gene knockout model for infantile neuronal ceroid lipofuscinosis. J Neurosci Res 84: 1139-1149.
30. Bible E, Gupta P, Hofmann SL, Cooper JD, (2004) Regional and cellular neuropathology in the palmitoyl protein thioesterase-1 null mutant mouse model of infantile neuronal ceroid lipofuscinosis. Neurobiol Dis 16: 346-359.
31. Rattner A, Nathans J, (2005) The genomic response to retinal disease and injury: evidence for endothelin signaling from photoreceptors to glia. J Neurosci 25: 4540-4549.
32. Thelen M, Fehr S, Schweizer M, Braulke T, Galliciotti G, (2012) High expression of disease-related Cln6 in the cerebral cortex, purkinje cells, dentate gyrus, and hippocampal ca1 neurons. J Neurosci Res 90: 568-574.
33. Cao Y, Staropoli JF, Biswas S, Espinola JA, MacDonald ME, et al. (2011) Distinct early molecular responses to mutations causing vLINCL and JNCL presage ATP synthase subunit C accumulation in cerebellar cells. PLoS One 6: e17118.
34. Tammen I, Houweling PJ, Frugier T, Mitchell NL, Kay GW, et al. (2006) 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 1762: 898-905.
35. Kurze AK, Galliciotti G, Heine C, Mole SE, Quitsch A, et al. (2010) Pathogenic mutations cause rapid degradation of lysosomal storage disease-related membrane protein CLN6. Hum Mutat 31: E1163-1174.
36. Seehafer SS, Ramirez-Montealegre D, Wong AM, Chan CH, Castaneda J, et al. (2011) Immunosuppression alters disease severity in juvenile Batten disease mice. J Neuroimmunol 230: 169-172.
37. Ammon HP, Wahl MA, (1991) Pharmacology of Curcuma longa. Planta Med 57: 1-7.
38. He LF, Chen HJ, Qian LH, Chen GY, Buzby JS, (2010) Curcumin protects pre-oligodendrocytes from activated microglia in vitro and in vivo. Brain Res 1339: 60-69.
39. Mandal MN, Patlolla JM, Zheng L, Agbaga MP, Tran JT, et al. (2009) Curcumin protects retinal cells from light-and oxidant stress-induced cell death. Free Radic Biol Med 46: 672-679.
40. Mukherjee PK, Marcheselli VL, Barreiro S, Hu J, Bok D, et al. (2007) Neurotrophins enhance retinal pigment epithelial cell survival through neuroprotectin D1 signaling. Proc Natl Acad Sci U S A 104: 13152-13157.
41. Kohlschutter A, Schade B, Blomer B, Hubner C, (1993) Low erythrocyte plasmalogen and plasma docosahexaenoic acid (DHA) in juvenile neuronal ceroid-lipofuscinosis (JNCL). J Inherit Metab Dis 16: 299-304.
42. Martin RE, Ranchon-Cole I, Brush RS, Williamson CR, Hopkins SA, et al. (2004) P23H and S334ter opsin mutations: Increasing photoreceptor outer segment n-3 fatty acid content does not affect the course of retinal degeneration. Mol Vis 10: 199-207.
43. Graeber MB, Li W, Rodriguez ML, (2011) Role of microglia in CNS inflammation. FEBS Lett 585: 3798-3805.