Amyloidosis, synucleinopathy, and prion encephalopathy in a neuropathic lysosomal storage disease: The CNS-biomarker potential of peripheral blood

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Naughton, Bartholomew J ^a   Duncan, F Jason ^a   Murrey, Darren ^a   Ware, Tierra ^a   Meadows, Aaron ^a   McCarty, Douglas M ^a,b   Fu, Haiyan ^a,b  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLGLUCOSAMINIDASE; AMYLOIDOSIS; ANIMALS; BIOLOGICAL MARKERS; BRAIN DISEASES; CENTRAL NERVOUS SYSTEM; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENETIC THERAPY; HUMANS; MAZE LEARNING; MICE; MICE, KNOCKOUT; MUCOPOLYSACCHARIDOSIS III; PRION DISEASES; REAL-TIME POLYMERASE CHAIN REACTION; SYNUCLEINS;

EID: 84894262540     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080142     Document Type: Article

References (50)

1. Neufeld EF, Muenzer J (2001) The mucopolysaccharidoses. In: Scriver CR, Beaudet AL, Sly WS, Valle D, editors. The metabolic & molecular basis of inherited disease. 8th ed. New York; St Louis; San Francisco: McGraw-Hill. 3421-3452.
2. Yogalingam G, Hopwood JJ (2001) Molecular genetics of mucopolysaccharidosis type IIIA and IIIB: Diagnostic, clinical, and biological implications. Hum Mutat 18: 264-281.
3. Li HH, Yu WH, Rozengurt N, Zhao HZ, Lyons KM, et al. (1999) Mouse model of Sanfilippo syndrome type B produced by targeted disruption of the gene encoding alpha-N-acetylglucosaminidase. Proc Natl Acad Sci U S A 96: 14505-14510.
4. McGlynn R, Dobrenis K, Walkley SU (2004) Differential subcellular localization of cholesterol, gangliosides, and glycosaminoglycans in murine models of mucopolysaccharide storage disorders. J Comp Neurol 480: 415-426.
5. Wilkinson FL, Holley RJ, Langford-Smith KJ, Badrinath S, Liao A, et al. (2012) Neuropathology in mouse models of mucopolysaccharidosis type I, IIIA and IIIB. PLoS One 7: e35787.
6. Li HH, Zhao HZ, Neufeld EF, Cai Y, Gomez-Pinilla F (2002) Attenuated plasticity in neurons and astrocytes in the mouse model of Sanfilippo syndrome type B. J Neurosci Res 69: 30-38.
7. Ohmi K, Greenberg DS, Rajavel KS, Ryazantsev S, Li HH, et al. (2003) Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc Natl Acad Sci U S A 100: 1902-1907.
8. Tamagawa K, Morimatsu Y, Fujisawa K, Hara A, Taketomi T (1985) Neuropathological study and chemico-pathological correlation in sibling cases of Sanfilippo syndrome type B. Brain Dev 7: 599-609.
9. Villani GR, Gargiulo N, Faraonio R, Castaldo S, Gonzalez YRE, et al. (2007) Cytokines, neurotrophins, and oxidative stress in brain disease from mucopoly-saccharidosis IIIB. J Neurosci Res 85: 612-622.
10. DiRosario J, Divers E, Wang C, Etter J, Charrier A, et al. (2009) Innate and adaptive immune activation in the brain of MPS IIIB mouse model. J Neurosci Res 87: 978-990.
11. Villani GR, Di Domenico C, Musella A, Cecere F, Di Napoli D, et al. (2009) Mucopolysaccharidosis IIIB: oxidative damage and cytotoxic cell involvement in the neuronal pathogenesis. Brain Res 1279: 99-108.
12. Ryazantsev S, Yu WH, Zhao HZ, Neufeld EF, Ohmi K (2007) Lysosomal accumulation of SCMAS (subunit c of mitochondrial ATP synthase) in neurons of the mouse model of mucopolysaccharidosis III B. Mol Genet Metab 90: 393-401.
13. Settembre C, Fraldi A, Jahreiss L, Spampanato C, Venturi C, et al. (2008) A block of autophagy in lysosomal storage disorders. Hum Mol Genet 17: 119-129.
14. Ginsberg SD, Galvin JE, Lee VM, Rorke LB, Dickson DW, et al. (1999) Accumulation of intracellular amyloid-beta peptide (A beta 1-40) in mucopoly-saccharidosis brains. J Neuropathol Exp Neurol 58: 815-824.
15. Winder-Rhodes SE, Garcia-Reitbock P, Ban M, Evans JR, Jacques TS, et al. (2012) Genetic and pathological links between Parkinson's disease and the lysosomal disorder Sanfilippo syndrome. Mov Disord 27: 312-315.
16. Ohmi K, Kudo LC, Ryazantsev S, Zhao HZ, Karsten SL, et al. (2009) Sanfilippo syndrome type B, a lysosomal storage disease, is also a tauopathy. Proc Natl Acad Sci U S A 106: 8332-8337.
17. Ohmi K, Zhao HZ, Neufeld EF (2011) Defects in the medial entorhinal cortex and dentate gyrus in the mouse model of Sanfilippo syndrome type B. PLoS One 6: e27461.
18. Hamano K, Hayashi M, Shioda K, Fukatsu R, Mizutani S (2008) Mechanisms of neurodegeneration in mucopolysaccharidoses II and IIIB: analysis of human brain tissue. Acta Neuropathol 115: 547-559.
19. Kurihara M, Kumagai K, Yagishita S (1996) Sanfilippo syndrome type C: a clinicopathological autopsy study of a long-term survivor. Pediatr Neurol 14: 317-321.
20. Huang Y, Mucke L (2012) Alzheimer mechanisms and therapeutic strategies. Cell 148: 1204-1222.
21. Eikelenboom P, van Exel E, Hoozemans JJ, Veerhuis R, Rozemuller AJ, et al. (2010) Neuroinflammation - an early event in both the history and pathogenesis of Alzheimer's disease. Neurodegener Dis 7: 38-41.
22. Kumar KR, Djarmati-Westenberger A, Grunewald A (2011) Genetics of Parkinson's disease. Semin Neurol 31: 433-440.
23. Panaro MA, Cianciulli A (2012) Current opinions and perspectives on the role of immune system in the pathogenesis of Parkinson's disease. Curr Pharm Des 18: 200-208.
24. Fu H, Bartz JD, Stephens RL Jr, McCarty DM (2012) Peripheral Nervous System Neuropathology and Progressive Sensory Impairments in a Mouse Model of Mucopolysaccharidosis IIIB. PLoS One 7: e45992.
25. Valayannopoulos V, Wijburg FA (2011) Therapy for the mucopolysaccharidoses. Rheumatology (Oxford) 50 Suppl 5: v49-59.
26. Byrne BJ, Falk DJ, Clement N, Mah CS (2012) Gene therapy approaches for lysosomal storage disease: next-generation treatment. Hum Gene Ther 23: 808-815.
27. High KA, Aubourg P (2011) rAAV human trial experience. Methods Mol Biol 807: 429-457.
28. Fu H, Dirosario J, Killedar S, Zaraspe K, McCarty DM (2011) Correction of neurological disease of mucopolysaccharidosis IIIB in adult mice by rAAV9 trans-blood-brain barrier gene delivery. Mol Ther 19: 1025-1033.
29. Ruzo A, Marco S, Garcia M, Villacampa P, Ribera A, et al. (2012) Correction of Pathological Accumulation of Glycosaminoglycans in Central Nervous System and Peripheral Tissues of MPSIIIA Mice Through Systemic AAV9 Gene Transfer. Hum Gene Ther.
30. Duque S, Joussemet B, Riviere C, Marais T, Dubreil L, et al. (2009) Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol Ther 17: 1187-1196.
31. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, et al. (2009) Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27: 59-65.
32. Foust KD, Wang X, McGovern VL, Braun L, Bevan AK, et al. (2010) Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat Biotechnol 28: 271-274.
33. Randall DR, Colobong KE, Hemmelgarn H, Sinclair GB, Hetty E, et al. (2008) Heparin cofactor II-thrombin complex: a biomarker of MPS disease. Mol Genet Metab 94: 456-461.
34. Beesley CE, Young EP, Finnegan N, Jackson M, Mills K, et al. (2009) Discovery of a new biomarker for the mucopolysaccharidoses (MPS), dipeptidyl peptidase IV (DPP-IV; CD26), by SELDI-TOF mass spectrometry. Mol Genet Metab 96: 218-224.
35. Lawrence R, Brown JR, Al-Mafraji K, Lamanna WC, Beitel JR, et al. (2012) Disease-specific non-reducing end carbohydrate biomarkers for mucopoly-saccharidoses. Nat Chem Biol 8: 197-204.
36. Fu H, Samulski RJ, McCown TJ, Picornell YJ, Fletcher D, et al. (2002) Neurological correction of lysosomal storage in a mucopolysaccharidosis IIIB mouse model by adeno-associated virus-mediated gene delivery. Mol Ther 5: 42-49.
37. Zolotukhin S, Byrne BJ, Mason E, Zolotukhin I, Potter M, et al. (1999) Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 6: 973-985.
38. Warburton EC, Baird A, Morgan A, Muir JL, Aggleton JP (2001) The conjoint importance of the hippocampus and anterior thalamic nuclei for allocentric spatial learning: evidence from a disconnection study in the rat. J Neurosci 21: 7323-7330.
39. Thompson JN, Nowakowski RW (1991) Enzymatic diagnosis of selected mucopolysaccharidoses: Hunter, Morquio type A, and Sanfilippo types A, B, C, and D, and procedures for measurement of 35SO4-glycosaminoglycans. In: Hommes FA, editor. Techniques in diagnostic human biochemical genetics - a laboratory manual. New York: Wiley-Liss. 567-586.
40. van de Lest CH, Versteeg EM, Veerkamp JH, van Kuppevelt TH (1994) Quantification and characterization of glycosaminoglycans at the nanogram level by a combined azure A-silver staining in agarose gels. - Anal Biochem 221: 356-61: 356-361.
41. Fu H, Kang L, Jennings JS, Moy SS, Perez A, et al. (2007) Significantly increased lifespan and improved behavioral performances by rAAV gene delivery in adult mucopolysaccharidosis IIIB mice. Gene Ther 14: 1065-1077.
42. de Jong JG, Wevers RA, Laarakkers C, Poorthuis BJ (1989) Dimethylmethylene blue-based spectrophotometry of glycosaminoglycans in untreated urine: a rapid screening procedure for mucopolysaccharidoses. - Clin Chem 35: 1472-7: 1472-1477.
43. Naughton BJ, Thirtamara-Rajamani K, Wang C, During MJ, Gu HH (2012) Specific knockdown of the D2 long dopamine receptor variant. Neuroreport 23: 1-5.
44. Mougeot JL, Li Z, Price AE, Wright FA, Brooks BR (2011) Microarray analysis of peripheral blood lymphocytes from ALS patients and the SAFE detection of the KEGG ALS pathway. BMC Med Genomics 4: 74.
45. Scherzer CR, Eklund AC, Morse LJ, Liao Z, Locascio JJ, et al. (2007) Molecular markers of early Parkinson's disease based on gene expression in blood. Proc Natl Acad Sci U S A 104: 955-960.
46. Henchcliffe C, Dodel R, Beal MF (2011) Biomarkers of Parkinson's disease and Dementia with Lewy bodies. Prog Neurobiol 95: 601-613.
47. Zou WQ, Zhou X, Yuan J, Xiao X (2011) Insoluble cellular prion protein and its association with prion and Alzheimer diseases. Prion 5: 172-178.
48. Aguzzi A (2009) Cell biology: Beyond the prion principle. Nature 459: 924-925.
49. Hu W, Kieseier B, Frohman E, Eagar TN, Rosenberg RN, et al. (2008) Prion proteins: physiological functions and role in neurological disorders. J Neurol Sci 264: 1-8.
50. Resenberger UK, Harmeier A, Woerner AC, Goodman JL, Muller V, et al. (2011) The cellular prion protein mediates neurotoxic signalling of beta-sheetrich conformers independent of prion replication. EMBO J 30: 2057-2070.