Neuronopathic Gaucher disease: Dysregulated mRNAs and miRNAs in brain pathogenesis and effects of pharmacologic chaperone treatment in a mouse model

Human Molecular Genetics

Volumn 24, Issue 24, 2015, Pages 7031-7048

  Dasgupta, Nupur ^a   Xu, You Hai ^a   Li, Ronghua ^a,b   Peng, Yanyan ^a   Pandey, Manoj K ^a,b   Tinch, Stuart L ^a   Liou, Benjamin ^a   Inskeep, Venette ^a   Zhang, Wujuan ^a   Setchell, Kenneth D R ^a,b   Keddache, Mehdi ^a   Grabowski, Gregory A ^a   Sun, Ying ^a,b  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; CD11B ANTIGEN; CD45 ANTIGEN; CHAPERONE; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CX3CR1; CHLORDANE; CYTOCHROME C OXIDASE; ENZYME ACTIVATOR; GLUCOSYLCERAMIDE; GLUCOSYLSPHINGOSINE; INITIATION FACTOR 2; ISOFAGOMINE; LEUCINE RICH REPEAT KINASE 2; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MICRORNA; MICROTUBULE ASSOCIATED PROTEIN 2; NEUROPROTECTIVE AGENT; PIPERIDINE DERIVATIVE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; AFEGOSTAT; IMINOSUGAR; MTOR PROTEIN, MOUSE; PSYCHOSINE; SPHINGOSYL BETA-GLUCOSIDE; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN CORTEX; BRAIN MITOCHONDRION; BRAIN STEM; CEREBELLUM; CONTROLLED STUDY; DETERIORATION; DISEASE COURSE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA SEQUENCE; GAUCHER DISEASE; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ASSOCIATION; GENETIC REGULATION; HUMAN; MESENCEPHALON; MICROGLIA; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE FIBER; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ANALOGS AND DERIVATIVES; ANIMAL; AXON; BRAIN; C57BL MOUSE; DISEASE MODEL; ENCEPHALITIS; GENE EXPRESSION PROFILING; GENETICS; GLIA; METABOLISM; MITOCHONDRION; PATHOLOGY; PHENOTYPE;

ANIMALS; AXONS; BRAIN; DISEASE MODELS, ANIMAL; ENCEPHALITIS; EUKARYOTIC INITIATION FACTOR-2; GAUCHER DISEASE; GENE EXPRESSION PROFILING; GLUCOSYLCERAMIDES; IMINO PYRANOSES; MICE, INBRED C57BL; MICRORNAS; MITOCHONDRIA; MOLECULAR CHAPERONES; NEUROGLIA; NEURONS; PHENOTYPE; PSYCHOSINE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TOR SERINE-THREONINE KINASES;

EID: 84958828265     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv404     Document Type: Article

References (70)

1. Grabowski, G.A., Petsko, G.A. and Kolodny, E.H. (2010) In Valle, D., Beaudet, A., Vogelstein, B., Kinzler, K.W., Antonarakis, S.E. and Ballabio, A. (eds), Metabolic and Molecular Bases of Inherited Disease (OMMBID Mark II). McGraw-Hill Companies, Inc., New York.
2. Koprivica, V., Stone, D.L., Park, J.K., Callahan, M., Frisch, A., Cohen, I.J., Tayebi, N. and Sidransky, E. (2000) Analysis and classification of 304 mutant alleles in patients with type 1 and type 3 Gaucher disease. Am. J. Hum. Genet., 66, 1777-1786.
3. Orvisky, E., Park, J.K., Parker, A., Walker, J.M., Martin, B.M., Stubblefield, B.K., Uyama, E., Tayebi, N. and Sidransky, E. (2002) The identification of eight novel glucocerebrosidase (GBA) mutations in patients with Gaucher disease. Hum. Mutat., 19, 458-459.
4. Gupta, N., Oppenheim, I.M., Kauvar, E.F., Tayebi, N. and Sidransky, E. (2011) Type 2 Gaucher disease: phenotypic variation and genotypic heterogeneity. Blood Cells Mol. Dis., 46, 75-84.
5. Conradi, N.G., Sourander, P., Nilsson, O., Svennerholm, L. and Erikson, A. (1984) Neuropathology of the Norrbottnian type of Gaucher disease. Morphological and biochemical studies. Acta Neuropathol., 65, 99-109.
6. Pelled, D., Trajkovic-Bodennec, S., Lloyd-Evans, E., Sidransky, E., Schiffmann, R. and Futerman, A.H. (2005) Enhanced calcium release in the acute neuronopathic form of Gaucher disease. Neurobiol. Dis., 18, 83-88.
7. Enquist, I.B., Lo Bianco, C., Ooka, A., Nilsson, E., Mansson, J.E., Ehinger, M., Richter, J., Brady, R.O., Kirik, D. and Karlsson, S. (2007) Murine models of acute neuronopathic Gaucher disease. Proc. Natl Acad. Sci. U.S.A., 104, 17483-17488.
8. Xu, Y.H., Reboulet, R., Quinn, B., Huelsken, J., Witte, D. and Grabowski, G.A. (2008) Dependence of reversibility and progression of mouse neuronopathic Gaucher disease on acid beta-glucosidase residual activity levels. Mol. Genet. Metab., 94, 190-203.
9. Tybulewicz, V.L., Tremblay, M.L., LaMarca, M.E., Willemsen, R., Stubblefield, B.K., Winfield, S., Zablocka, B., Sidransky, E., Martin, B.M., Huang, S.P. et al. (1992) Animal model of Gaucher's disease from targeted disruption of the mouse glucocerebrosidase gene. Nature, 357, 407-410.
10. Sun, Y., Liou, B., Ran, H., Skelton, M.R., Williams, M.T., Vorhees, C.V., Kitatani, K., Hannun, Y.A., Witte, D.P., Xu, Y.H. et al. (2010) Neuronopathic Gaucher disease in the mouse: viable combined selective saposin C deficiency and mutant glucocerebrosidase (V394L) mice with glucosylsphingosine and glucosylceramide accumulation and progressive neurological deficits. Hum. Mol. Genet., 19, 1088-1097.
11. Xu, Y.H., Quinn, B., Witte, D. and Grabowski, G.A. (2003) Viable mouse models of acid beta-glucosidase deficiency: the defect in Gaucher disease. Am. J. Pathol., 163, 2093-2101.
12. Sun, Y., Ran, H., Zamzow, M., Kitatani, K., Skelton, M.R., Williams, M.T., Vorhees, C.V., Witte, D.P., Hannun, Y.A. and Grabowski, G.A. (2010) Specific saposin C deficiency: CNS impairment and acid beta-glucosidase effects in the mouse. Hum. Mol. Genet., 19, 634-647.
13. Burrow, T.A., Sun, Y., Prada, C.E., Bailey, L., Zhang, W., Brewer, A., Wu, S.W., Setchell, K.D., Witte, D., Cohen, M.B. et al. (2015) CNS, lung, and lymph node involvement in Gaucher disease type 3 after 11 years of therapy: clinical, histopathologic, and biochemical findings. Mol. Genet. Metab, 114, 233-241.
14. Sun, Y., Zhang, W., Xu, Y.H., Quinn, B., Dasgupta, N., Liou, B., Setchell, K.D. and Grabowski, G.A. (2013) Substrate compositional variation with tissue/region and Gba1 mutations in mouse models-implications for Gaucher disease. PLoS One, 8, e57560.
15. Steet, R.A., Chung, S., Wustman, B., Powe, A., Do, H. and Kornfeld, S.A. (2006) The iminosugar isofagomine increases the activity of N370S mutant acid beta-glucosidase in Gaucher fibroblasts by several mechanisms. Proc. Natl Acad. Sci. U.S.A., 103, 13813-13818.
16. Sun, Y., Ran, H., Liou, B., Quinn, B., Zamzow, M., Zhang, W., Bielawski, J., Kitatani, K., Setchell, K.D., Hannun, Y.A. et al. (2011) Isofagomine in vivo effects in a neuronopathic Gaucher disease mouse. PLoS One, 6, e19037.
17. Khanna, R., Benjamin, E.R., Pellegrino, L., Schilling, A., Rigat, B.A., Soska, R., Nafar, H., Ranes, B.E., Feng, J., Lun, Y. et al. (2010) The pharmacological chaperone isofagomine increases the activity of the Gaucher disease L444Pmutant formof betaglucosidase. FEBS J., 277, 1618-1638.
18. Sun, Y., Jia, L., Williams, M.T., Zamzow, M., Ran, H., Quinn, B., Aronow, B.J., Vorhees, C.V., Witte, D.P. and Grabowski, G.A. (2008) Temporal gene expression profiling reveals CEBPD as a candidate regulator of brain disease in prosaposin deficient mice. BMC Neurosci., 9, 76.
19. Dasgupta, N., Xu, Y.H., Oh, S., Sun, Y., Jia, L., Keddache, M. and Grabowski, G.A. (2013) Gaucher disease: transcriptome analyses using microarray or mRNA sequencing in a Gba1 mutant mouse model treated with velaglucerase alfa or imiglucerase. PLoS One, 8, e74912.
20. Hong, Y.B., Kim, E.Y. and Jung, S.C. (2004) Down-regulation of Bcl-2 in the fetal brain of the Gaucher disease mouse model: a possible role in the neuronal loss. J. Hum. Genet., 49, 349-354.
21. Myerowitz, R., Mizukami, H., Richardson, K.L., Finn, L.S., Tifft, C.J. and Proia, R.L. (2004) Global gene expression in a type 2 Gaucher disease brain. Mol. Genet. Metab., 83, 288-296.
22. Shoffner, J.M.T. and Wallace, D.C. (1990) Oxidative phosphorylation diseases. Disorders of two genomes. Adv. Hum. Genet., 19, 267-330.
23. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y. and Shimizu, N. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature, 392, 605-608.
24. Zimprich, A., Biskup, S., Leitner, P., Lichtner, P., Farrer, M., Lincoln, S., Kachergus, J., Hulihan, M., Uitti, R.J., Calne, D.B. et al. (2004) Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron, 44, 601-607.
25. Mazzulli, J.R., Xu, Y.H., Sun, Y., Knight, A.L., McLean, P.J., Caldwell, G.A., Sidransky, E., Grabowski, G.A. and Krainc, D. (2011) Gaucher disease glucocerebrosidase and alpha-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell, 146, 37-52.
26. Wong, K., Sidransky, E., Verma, A., Mixon, T., Sandberg, G.D., Wakefield, L.K., Morrison, A., Lwin, A., Colegial, C., Allman, J.M. et al. (2004) Neuropathology provides clues to the pathophysiology of Gaucher disease. Mol. Genet. Metab., 82, 192-207.
27. Perrot, V., Vazquez-Prado, J. and Gutkind, J.S. (2002) Plexin B regulates Rho through the guanine nucleotide exchange factors leukemia-associated Rho GEF (LARG) and PDZ-RhoGEF. J. Biol. Chem., 277, 43115-43120.
28. Rodriguez, J., Esteve, P., Weinl, C., Ruiz, J.M., Fermin, Y., Trousse, F., Dwivedy, A., Holt, C. and Bovolenta, P. (2005) SFRP1 regulates the growth of retinal ganglion cell axons through the Fz2 receptor. Nat. Neurosci., 8, 1301-1309.
29. Romi, E., Gokhman, I., Wong, E., Antonovsky, N., Ludwig, A., Sagi, I., Saftig, P., Tessier-Lavigne, M. and Yaron, A. (2014) ADAM metalloproteases promote a developmental switch in responsiveness to the axonal repellant Sema3A. Nat. Commun., 5, 4058.
30. Lewis, B.P., Burge, C.B. and Bartel, D.P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell, 120, 15-20.
31. Xu, Y.H., Xu, K., Sun, Y., Liou, B., Quinn, B., Li, R.H., Xue, L., Zhang, W., Setchell, K.D., Witte, D. et al. (2014) Multiple pathogenic proteins implicated in neuronopathic Gaucher disease mice. Hum. Mol. Genet., 23, 3943-3957.
32. Osellame, L.D. and Duchen, M.R. (2013) Defective quality controlmechanisms and accumulation of damaged mitochondria link Gaucher and Parkinson diseases. Autophagy, 9, 1633-1635.
33. Cleeter, M.W., Chau, K.Y., Gluck, C., Mehta, A., Hughes, D.A., Duchen, M., Wood, N.W., Hardy, J., Mark Cooper, J. and Schapira, A.H. (2013) Glucocerebrosidase inhibition causes mitochondrial dysfunction and free radical damage. Neurochem. Int., 62, 1-7.
34. Simon, A.M., de Maturana, R.L., Ricobaraza, A., Escribano, L., Schiapparelli, L., Cuadrado-Tejedor, M., Perez-Mediavilla, A., Avila, J., Del Rio, J. and Frechilla, D. (2009) Early changes in hippocampal Eph receptors precede the onset of memory decline in mouse models of Alzheimer's disease. J. Alzheimers Dis., 17, 773-786.
35. Bossers, K., Meerhoff, G., Balesar, R., van Dongen, J.W., Kruse, C.G., Swaab, D.F. and Verhaagen, J. (2009) Analysis of gene expression in Parkinson's disease: possible involvement of neurotrophic support and axon guidance in dopaminergic cell death. Brain Pathol., 19, 91-107.
36. Van Hoecke, A., Schoonaert, L., Lemmens, R., Timmers, M., Staats, K.A., Laird, A.S., Peeters, E., Philips, T., Goris, A., Dubois, B. et al. (2012) EPHA4 is a diseasemodifier of amyotrophic lateral sclerosis in animalmodels and in humans. Nat. Med., 18, 1418- 1422.
37. Arvanitis, D.N. and Davy, A. (2012) Regulation and misregulation of Eph/ephrin expression. Cell Adh. Migr., 6, 131-137.
38. Natera-Naranjo, O., Aschrafi, A., Gioio, A.E. and Kaplan, B.B. (2010) Identification and quantitative analyses of microRNAs located in the distal axons of sympathetic neurons. RNA, 16, 1516-1529.
39. Bliss, T.V. and Lomo, T. (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol., 232, 331-356.
40. Ginns, E.I., Mak, S.K., Ko, N., Karlgren, J., Akbarian, S., Chou, V.P., Guo, Y., Lim, A., Samuelsson, S., LaMarca, M.L. et al. (2014) Neuroinflammation and alpha-synuclein accumulation in response to glucocerebrosidase deficiency are accompanied by synaptic dysfunction. Mol. Genet. Metab., 111, 152-162.
41. Stancu, I.C., Ris, L., Vasconcelos, B., Marinangeli, C., Goeminne, L., Laporte, V., Haylani, L.E., Couturier, J., Schakman, O., Gailly, P. et al. (2014) Tauopathy contributes to synaptic and cognitive deficits in a murine model for Alzheimer's disease. FASEB J., 28, 2620-2631.
42. Kitada, T., Pisani, A., Karouani, M., Haburcak, M., Martella, G., Tscherter, A., Platania, P., Wu, B., Pothos, E.N. and Shen, J. (2009) Impaired dopamine release and synaptic plasticity in the striatum of parkin-/- mice. J. Neurochem., 110, 613-621.
43. Kitada, T., Pisani, A., Porter, D.R., Yamaguchi, H., Tscherter, A., Martella, G., Bonsi, P., Zhang, C., Pothos, E.N. and Shen, J. (2007) Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc. Natl Acad. Sci. U. S.A., 104, 11441-11446.
44. Selkoe, D.J. (2002) Alzheimer's disease is a synaptic failure. Science, 298, 789-791.
45. Sha, S., Zhou, L., Yin, J., Takamiya, K., Furukawa, K., Furukawa, K., Sokabe, M. and Chen, L. (2014) Deficits in cognitive function and hippocampal plasticity in GM2/GD2 synthase knockout mice. Hippocampus, 24, 369-382.
46. Greer, P.L. and Greenberg, M.E. (2008) From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron, 59, 846-860.
47. Nicoll, R.A. and Roche, K.W. (2013) Long-term potentiation: peeling the onion. Neuropharmacology, 74, 18-22.
48. Miyamoto, E. (2006) Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J. Pharmacol. Sci., 100, 433-442.
49. Galeotti, N., Quattrone, A., Vivoli, E., Norcini, M., Bartolini, A. and Ghelardini, C. (2008) Different involvement of type 1, 2, and 3 ryanodine receptors in memory processes. Learn Mem., 15, 315-323.
50. Giannini, G., Conti, A., Mammarella, S., Scrobogna, M. and Sorrentino, V. (1995) The ryanodine receptor/calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues. J. Cell Biol., 128, 893- 904.
51. Edwards, T.M. and Rickard, N.S. (2006) Pharmaco-behavioural evidence indicating a complex role for ryanodine receptor calcium release channels in memory processing for a passive avoidance task. Neurobiol. Learn Mem., 86, 1-8.
52. Korkotian, E., Schwarz, A., Pelled, D., Schwarzmann, G., Segal, M. and Futerman, A.H. (1999) Elevation of intracellular glucosylceramide levels results in an increase in endoplasmic reticulum density and in functional calcium stores in cultured neurons. J. Biol. Chem., 274, 21673-21678.
53. Liu, J., Supnet, C., Sun, S., Zhang, H., Good, L., Popugaeva, E. and Bezprozvanny, I. (2014) The role of ryanodine receptor type 3 in a mouse model of Alzheimer disease. Channels (Austin)., 8, 230-242.
54. Wu, B., Yamaguchi, H., Lai, F.A. and Shen, J. (2013) Presenilins regulate calcium homeostasis and presynaptic function via ryanodine receptors in hippocampal neurons. Proc. Natl Acad. Sci. U.S.A., 110, 15091-15096.
55. Manczak, M., Jung, Y., Park, B.S., Partovi, D. and Reddy, P.H. (2005) Time-course of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J. Neurochem., 92, 494-504.
56. Chen, Z., Li, Y., Zhang, H., Huang, P. and Luthra, R. (2010) Hypoxia- regulated microRNA-210 modulates mitochondrial function and decreases ISCU and COX10 expression. Oncogene, 29, 4362-4368.
57. Ouyang, Y.B., Lu, Y., Yue, S. and Giffard, R.G. (2012) miR-181 targets multiple Bcl-2 family members and influences apoptosis and mitochondrial function in astrocytes. Mitochondrion, 12, 213-219.
58. Casadio, A., Martin, K.C., Giustetto, M., Zhu, H., Chen, M., Bartsch, D., Bailey, C.H. and Kandel, E.R. (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell, 99, 221-237.
59. Kelleher, R.J. 3rd, Govindarajan, A., Jung, H.Y., Kang, H. and Tonegawa, S. (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell, 116, 467- 479.
60. Khan, A., Pepio, A.M. and Sossin, W.S. (2001) Serotonin activates S6 kinase in a rapamycin-sensitive manner in Aplysia synaptosomes. J. Neurosci., 21, 382-391.
61. Takei, N., Kawamura, M., Hara, K., Yonezawa, K. and Nawa, H. (2001) Brain-derived neurotrophic factor enhances neuronal translation by activating multiple initiation processes: comparison with the effects of insulin. J. Biol. Chem., 276, 42818-42825.
62. Garza-Manero, S., Pichardo-Casas, I., Arias, C., Vaca, L. and Zepeda, A. (2014) Selective distribution and dynamic modulation of miRNAs in the synapse and its possible role in Alzheimer's disease. Brain Res., 1584, 80-93.
63. Satoh, J. (2012) Molecular network of microRNA targets in Alzheimer's disease brains. Exp. Neurol., 235, 436-446.
64. Dorval, V., Mandemakers, W., Jolivette, F., Coudert, L., Mazroui, R., De Strooper, B. and Hebert, S.S. (2014) Gene and MicroRNA transcriptome analysis of Parkinson's related LRRK2 mouse models. PLoS One, 9, e85510.
65. Packer, A.N., Xing, Y., Harper, S.Q., Jones, L. and Davidson, B.L. (2008) The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington's disease. J. Neurosci., 28, 14341-14346.
66. Goodall, E.F., Heath, P.R., Bandmann, O., Kirby, J. and Shaw, P.J. (2013) Neuronal dark matter: the emerging role of microRNAs in neurodegeneration. Front Cell Neurosci., 7, 178.
67. Bak, M., Silahtaroglu, A., Moller, M., Christensen, M., Rath, M.F., Skryabin, B., Tommerup, N. and Kauppinen, S. (2008) MicroRNA expression in the adult mouse central nervous system. RNA, 14, 432-444.
68. Juhila, J., Sipila, T., Icay, K., Nicorici, D., Ellonen, P., Kallio, A., Korpelainen, E., Greco, D. and Hovatta, I. (2011) MicroRNA expression profiling reveals miRNA families regulating specific biological pathways in mouse frontal cortex and hippocampus. PLoS One, 6, e21495.
69. Sun, Y., Quinn, B., Witte, D.P. and Grabowski, G.A. (2005) Gaucher disease mouse models: point mutations at the acid beta-glucosidase locus combined with low-level prosaposin expression lead to disease variants. J. Lipid Res., 46, 2102-2113.
70. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc., 57, 289-300.