Microdissection and transcriptional profiling a window into the pathobiology of preclinical prion disease

Prion

Volumn 8, Issue 1, 2014, Pages

  Majer, Anna ^a,b   Booth, Stephanie A ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Public Health Agency of Canada   (Canada)

Author keywords

Animal model; Expression; Gene; MiRNA; Neurodegeneration; Neuroprotection; Preclinical; Prion; Profiling; Transcriptome

Indexed keywords

MICRORNA; STRESS ACTIVATED PROTEIN KINASE;

CELL SURVIVAL; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HIPPOCAMPAL CA1 REGION; HUMAN; MICRODISSECTION; MOLECULAR MECHANICS; NERVE CELL; NERVE DEGENERATION; NONHUMAN; PATHOLOGY; PRION DISEASE; REGULATORY MECHANISM; REVIEW; SYNAPSE; ANIMAL; GENETICS; METABOLISM; MOUSE;

ANIMALS; GENE EXPRESSION PROFILING; MICE; MICRODISSECTION; MICRORNAS; NEURONS; PRION DISEASES; TRANSCRIPTION, GENETIC;

EID: 84896913442     PISSN: 19336896     EISSN: 1933690X     Source Type: Journal    
DOI: 10.4161/pri.27729     Document Type: Review

References (69)

1. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L.A., Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991; 30:572-80; PMID:1789684; http://dx.doi.org/10.1002/ana.410300410
2. Jeffrey M., Halliday W.G., Bell J., Johnston A.R., MacLeod N.K., Ingham C., Sayers A.R., Brown D.A., Fraser JR. Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapieinfected murine hippocampus. Neuropathol Appl Neurobiol 2000; 26:41-54; PMID:10736066; http://dx.doi.org/10. 1046/j.1365-2990.2000.00216.x
3. Mallucci G.R., White M.D., Farmer M., Dickinson A., Khatun H., Powell A.D., Brandner S., Jefferys J.G., Collinge J. Targeting cellular prion protein reverses early cognitive deficits and neurophysiological dysfunction in prion-infected mice. Neuron 2007; 53:325-35; PMID:17270731; http://dx.doi.org/ 10.1016/j.neuron.2007.01.005
4. Sisková Z., Page A., O'Connor V., Perry VH. Degenerating synaptic boutons in prion disease: microglia activation without synaptic stripping. Am J Pathol 2009; 175:1610-21; PMID:19779137; http://dx.doi.org/10.2353/ajpath.2009. 090372
5. Kitamoto T., Shin R.W., Doh-ura K., Tomokane N., Miyazono M., Muramoto T., Tateishi J. Abnormal isoform of prion proteins accumulates in the synaptic structures of the central nervous system in patients with Creutzfeldt-Jakob disease. Am J Pathol 1992; 140:1285-94; PMID:1351366
6. Clinton J., Forsyth C., Royston M.C., Roberts GW. Synaptic degeneration is the primary neuropathological feature in prion disease: a preliminary study. Neuroreport 1993; 4:65-8; PMID:8453038; http://dx.doi.org/10.1097/00001756- 199301000-00017
7. Sikorska B., Liberski P.P., Giraud P., Kopp N., Brown P. Autophagy is a part of ultrastructural synaptic pathology in Creutzfeldt-Jakob disease: a brain biopsy study. Int J Biochem Cell Biol 2004; 36:2563-73; PMID:15325593; http://dx.doi.org/10.1016/j. biocel.2004.04.014
8. Gray B.C., Siskova Z., Perry V.H., O'Connor V. Selective presynaptic degeneration in the synaptopathy associated with ME7-induced hippocampal pathology. Neurobiol Dis 2009; 35:63-74; PMID:19362593; http://dx.doi.org/10. 1016/j.nbd.2009.04.001
9. Sisková Z., Sanyal N.K., Orban A., O'Connor V., Perry VH. Reactive hypertrophy of synaptic varicosities within the hippocampus of prioninfected mice. Biochem Soc Trans 2010; 38:471-5; PMID:20298205; http://dx.doi.org/10. 1042/ BST0380471
10. Cunningham C., Deacon R., Wells H., Boche D., Waters S., Diniz C.P., Scott H., Rawlins J.N., Perry VH. Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur J Neurosci 2003; 17:2147-55; PMID:12786981; http://dx.doi.org/10.1046/j.1460-9568.2003.02662.x
11. Moreno J.A., Halliday M., Molloy C., Radford H., Verity N., Axten J.M., Ortori C.A., Willis A.E., Fischer P.M., Barrett D.A., et al. Oral treatment targeting the unfolded protein response prevents neurodegeneration and clinical disease in prion-infected mice. Sci Transl Med 2013; 5:ra138; PMID:24107777; http://dx.doi.org/10.1126/scitranslmed.3006767
12. Basu U., Guan L., Moore SS. Functional genomics approach for identification of molecular processes underlying neurodegenerative disorders in prion diseases. Curr Genomics 2012; 13:369-78; PMID:23372423; http://dx.doi.org/10.2174/138920212801619223
13. Xiang W., Windl O., Westner I.M., Neumann M., Zerr I., Lederer R.M., Kretzschmar HA. Cerebral gene expression profiles in sporadic Creutzfeldt-Jakob disease. Ann Neurol 2005; 58:242-57; PMID:16049922; http://dx.doi.org/10.1002/ ana.20551
14. Chung C.Y., Seo H., Sonntag K.C., Brooks A., Lin L., Isacson O. Cell type-specific gene expression of midbrain dopaminergic neurons reveals molecules involved in their vulnerability and protection. Hum Mol Genet 2005; 14:1709-25; PMID:15888489; http://dx.doi.org/10.1093/hmg/ddi178
15. Majer A., Medina S.J., Niu Y., Abrenica B., Manguiat K.J., Frost K.L., Philipson C.S., Sorensen D.L., Booth SA. Early mechanisms of pathobiology are revealed by transcriptional temporal dynamics in hippocampal CA1 neurons of prion infected mice. PLoS Pathog 2012; 8:e1003002; PMID:23144617; http://dx.doi.org/10.1371/journal.ppat.1003002
16. Doyle J.P., Dougherty J.D., Heiman M., Schmidt E.F., Stevens T.R., Ma G., Bupp S., Shrestha P., Shah R.D., Doughty M.L., et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 2008; 135:749-62; PMID:19013282; http://dx.doi.org/10.1016/j.cell.2008.10. 029
17. Heiman M., Schaefer A., Gong S., Peterson J.D., Day M., Ramsey K.E., Suárez-Fariñas M., Schwarz C., Stephan D.A., Surmeier D.J., et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell 2008; 135:738-48; PMID:19013281; http://dx.doi.org/10.1016/j. cell.2008.10.028
18. Arlotta P., Molyneaux B.J., Chen J., Inoue J., Kominami R., Macklis JD. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 2005; 45:207-21; PMID:15664173; http://dx.doi.org/ 10.1016/j.neuron.2004.12.036
19. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., et al. A transcriptome database for astrocytes., neurons., and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 2008; 28:264-78; PMID:18171944; http://dx.doi.org/10.1523/JNEUROSCI.4178-07.2008
20. Sugino K., Hempel C.M., Miller M.N., Hattox A.M., Shapiro P., Wu C., Huang Z.J., Nelson SB. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat Neurosci 2006; 9:99-107; PMID:16369481; http://dx.doi.org/10.1038/nn1618
21. Kamme F., Salunga R., Yu J., Tran D.T., Zhu J., Luo L., Bittner A., Guo H.Q., Miller N., Wan J., et al. Singlecell microarray analysis in hippocampus CA1: demonstration and validation of cellular heterogeneity. J Neurosci 2003; 23:3607-15; PMID:12736331
22. Tarsa L., Goda Y. Synaptophysin regulates activity- dependent synapse formation in cultured hippocampal neurons. Proc Natl Acad Sci U S A 2002; 99:1012-6; PMID:11792847; http://dx.doi.org/10.1073/pnas.022575999
23. Jahn R., Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature 2012; 490:201-7; PMID:23060190; http://dx.doi.org/10.1038/ nature11320
24. Cabin D.E., Shimazu K., Murphy D., Cole N.B., Gottschalk W., McIlwain K.L., Orrison B., Chen A., Ellis C.E., Paylor R., et al. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking alpha-synuclein. J Neurosci 2002; 22:8797-807; PMID:12388586
25. Tomasoni R., Repetto D., Morini R., Elia C., Gardoni F., Di Luca M., Turco E., Defilippi P., Matteoli M. SNAP- 25 regulates spine formation through postsynaptic binding to p140Cap. Nat Commun 2013; 4:2136; PMID:23868368; http://dx.doi.org/10.1038/ ncomms3136
26. Berridge MJ. Neuronal calcium signaling. Neuron 1998; 21:13-26; PMID:9697848; http://dx.doi.org/10.1016/S0896-6273(00)80510-3
27. Xiang W., Windl O., Wünsch G., Dugas M., Kohlmann A., Dierkes N., Westner I.M., Kretzschmar HA. Identification of differentially expressed genes in scrapie-infected mouse brains by using global gene expression technology. J Virol 2004; 78:11051-60; PMID:15452225; http://dx.doi.org/10.1128/ JVI.78.20.11051-11060.2004
28. Skinner P.J., Abbassi H., Chesebro B., Race R.E., Reilly C., Haase AT. Gene expression alterations in brains of mice infected with three strains of scrapie. BMC Genomics 2006; 7:114; PMID:16700923; http://dx.doi.org/10.1186/ 1471-2164-7-114
29. Sorensen G., Medina S., Parchaliuk D., Phillipson C., Robertson C., Booth SA. Comprehensive transcriptional profiling of prion infection in mouse models reveals networks of responsive genes. BMC Genomics 2008; 9:114; PMID:18315872; http://dx.doi.org/10.1186/1471-2164-9-114
30. Hwang D., Lee I.Y., Yoo H., Gehlenborg N., Cho J.H., Petritis B., Baxter D., Pitstick R., Young R., Spicer D., et al. A systems approach to prion disease. Mol Syst Biol 2009; 5:252; PMID:19308092; http://dx.doi.org/10.1038/ msb.2009.10
31. Zhang S.J., Steijaert M.N., Lau D., Schütz G., Delucinge- Vivier C., Descombes P., Bading H. Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 2007; 53:549-62; PMID:17296556; http://dx.doi.org/10.1016/j.neuron.2007.01.025
32. Zhang S.J., Zou M., Lu L., Lau D., Ditzel D.A., Delucinge- Vivier C., Aso Y., Descombes P., Bading H. Nuclear calcium signaling controls expression of a large gene pool: identification of a gene program for acquired neuroprotection induced by synaptic activity. PLoS Genet 2009; 5:e1000604; PMID:19680447; http://dx.doi.org/10.1371/journal.pgen.1000604
33. Hardingham G.E., Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 2010; 11:682-96; PMID:20842175; http://dx.doi.org/10.1038/nrn2911
34. Zhang S.J., Buchthal B., Lau D., Hayer S., Dick O., Schwaninger M., Veltkamp R., Zou M., Weiss U., Bading H. A signaling cascade of nuclear calcium- CREB-ATF3 activated by synaptic NMDA receptors defines a gene repression module that protects against extrasynaptic NMDA receptor-induced neuronal cell death and ischemic brain damage. J Neurosci 2011; 31:4978-90; PMID:21451036; http://dx.doi.org/10.1523/JNEUROSCI.2672-10.2011
35. Liu Y., Wong T.P., Aarts M., Rooyakkers A., Liu L., Lai T.W., Wu D.C., Lu J., Tymianski M., Craig A.M., et al. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J Neurosci 2007; 27:2846-57; PMID:17360906; http://dx.doi.org/10.1523/JNEUROSCI. 0116-07.2007
36. Li S.T., Ju JG. Functional roles of synaptic and extrasynaptic NMDA receptors in physiological and pathological neuronal activities. Curr Drug Targets 2012; 13:207-21; PMID:22204320; http://dx.doi.org/10.2174/ 138945012799201630
37. Salih D.A., Brunet A. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol 2008; 20:126-36; PMID:18394876; http://dx.doi.org/10.1016/j. ceb.2008.02.005
38. Collinge J., Whittington M.A., Sidle K.C., Smith C.J., Palmer M.S., Clarke A.R., Jefferys JG. Prion protein is necessary for normal synaptic function. Nature 1994; 370:295-7; PMID:8035877; http://dx.doi.org/10.1038/ 370295a0
39. Maglio L.E., Perez M.F., Martins V.R., Brentani R.R., Ramirez OA. Hippocampal synaptic plasticity in mice devoid of cellular prion protein. Brain Res Mol Brain Res 2004; 131:58-64; PMID:15530652; http://dx.doi.org/10.1016/j. molbrainres.2004.08.004
40. Khosravani H., Zhang Y., Tsutsui S., Hameed S., Altier C., Hamid J., Chen L., Villemaire M., Ali Z., Jirik F.R., et al. Prion protein attenuates excitotoxicity by inhibiting NMDA receptors. J Cell Biol 2008; 181:551-65; PMID:18443219; http://dx.doi.org/10.1083/ jcb.200711002
41. Mucke L., Selkoe DJ. Neurotoxicity of amyloid ?-protein: synaptic and network dysfunction. Cold Spring Harb Perspect Med 2012; 2:a006338; PMID:22762015; http://dx.doi.org/10.1101/cshperspect.a006338
42. Sitia R., Braakman I. Quality control in the endoplasmic reticulum protein factory. Nature 2003; 426:891-4; PMID:14685249; http://dx.doi.org/10. 1038/nature02262
43. Galehdar Z., Swan P., Fuerth B., Callaghan S.M., Park D.S., Cregan SP. Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4- CHOP-mediated induction of the Bcl-2 homology 3-only member PUMA. J Neurosci 2010; 30:16938-48; PMID:21159964; http://dx.doi.org/10.1523/ JNEUROSCI.1598-10.2010
44. Brown A.R., Rebus S., McKimmie C.S., Robertson K., Williams A., Fazakerley JK. Gene expression profiling of the preclinical scrapie-infected hippocampus. Biochem Biophys Res Commun 2005; 334:86-95; PMID:15992767; http://dx.doi.org/10.1016/j. bbrc.2005.06.060
45. Moreno J.A., Radford H., Peretti D., Steinert J.R., Verity N., Martin M.G., Halliday M., Morgan J., Dinsdale D., Ortori C.A., et al. Sustained translational repression by eIF2?-P mediates prion neurodegeneration. Nature 2012; 485:507-11; PMID:22622579
46. Barbato C., Ruberti F. MicroRNA Regulation of Neuronal Differentiation and Plasticity. In: Mallick B., Ghosh Z., editors. Regulatory RNAs Basics., Methods and Applications. Springer Berlin Heidelberg. 2010; Pp. 175-195.
47. McNeill E., Van Vactor D. MicroRNAs shape the neuronal landscape. Neuron 2012; 75:363-79; PMID:22884321; http://dx.doi.org/10.1016/j. neuron.2012.07.005
48. Cuellar T.L., Davis T.H., Nelson P.T., Loeb G.B., Harfe B.D., Ullian E., McManus MT. Dicer loss in striatal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proc Natl Acad Sci U S A 2008; 105:5614-9; PMID:18385371; http://dx.doi.org/10.1073/pnas. 0801689105
49. Damiani D., Alexander J.J., O'Rourke J.R., McManus M., Jadhav A.P., Cepko C.L., Hauswirth W.W., Harfe B.D., Strettoi E. Dicer inactivation leads to progressive functional and structural degeneration of the mouse retina. J Neurosci 2008; 28:4878-87; PMID:18463241; http://dx.doi.org/10.1523/ JNEUROSCI.0828-08.2008
50. Davis T.H., Cuellar T.L., Koch S.M., Barker A.J., Harfe B.D., McManus M.T., Ullian EM. Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J Neurosci 2008; 28:4322-30; PMID:18434510; http://dx.doi.org/10.1523/JNEUROSCI.4815-07.2008
51. Haramati S., Chapnik E., Sztainberg Y., Eilam R., Zwang R., Gershoni N., McGlinn E., Heiser P.W., Wills A.M., Wirguin I., et al. miRNA malfunction causes spinal motor neuron disease. Proc Natl Acad Sci U S A 2010; 107:13111-6; PMID:20616011; http://dx.doi.org/10.1073/pnas.1006151107
52. Sonntag KC. MicroRNAs and deregulated gene expression networks in neurodegeneration. Brain Res 2010; 1338:48-57; PMID:20380815; http://dx.doi.org/10.1016/j.brainres.2010.03.106
53. Majer A., Boese A.S., Booth SA. The role of microRNAs in neurodegenerative diseases: Implications for early detection and treatment. In: Mallick B., Ghosh Z., editors. Regulatory RNAs Basics., Methods and Applications. Springer Berlin Heidelberg. 2012; Pp. 443-473.
54. Siegel G., Saba R., Schratt G. microRNAs in neurons: manifold regulatory roles at the synapse. Curr Opin Genet Dev 2011; 21:491-7; PMID:21561760; http://dx.doi.org/10.1016/j.gde.2011.04.008
55. Cheng L.C., Pastrana E., Tavazoie M., Doetsch F. miR- 124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 2009; 12:399-408; PMID:19287386; http://dx.doi.org/10.1038/ nn.2294
56. Arvanitis D.N., Jungas T., Behar A., Davy A. Ephrin-B1 reverse signaling controls a posttranscriptional feedback mechanism via miR-124. Mol Cell Biol 2010; 30:2508-17; PMID:20308325; http://dx.doi.org/10.1128/MCB.01620-09
57. Sanuki R., Onishi A., Koike C., Muramatsu R., Watanabe S., Muranishi Y., Irie S., Uneo S., Koyasu T., Matsui R., et al. miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression. Nat Neurosci 2011; 14:1125-34; PMID:21857657; http://dx.doi.org/10.1038/ nn.2897
58. Wayman G.A., Davare M., Ando H., Fortin D., Varlamova O., Cheng H.Y., Marks D., Obrietan K., Soderling T.R., Goodman R.H., et al. An activityregulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc Natl Acad Sci U S A 2008; 105:9093-8; PMID:18577589; http://dx.doi.org/10.1073/pnas. 0803072105
59. Li B., Sun H. MiR-26a promotes neurite outgrowth by repressing PTEN expression. Mol Med Rep 2013; 8:676-80; PMID:23783805
60. McAllister AK. Cellular and molecular mechanisms of dendrite growth. Cereb Cortex 2000; 10:963-73; PMID:11007547; http://dx.doi.org/10.1093/ cercor/10.10.963
61. Lippi G., Steinert J.R., Marczylo E.L., D'Oro S., Fiore R., Forsythe I.D., Schratt G., Zoli M., Nicotera P., Young KW. Targeting of the Arpc3 actin nucleation factor by miR-29a/b regulates dendritic spine morphology. J Cell Biol 2011; 194:889-904; PMID:21930776; http://dx.doi.org/10.1083/jcb.201103006
62. Abe M., Bonini NM. MicroRNAs and neurodegeneration: role and impact. Trends Cell Biol 2013; 23:30-6; PMID:23026030; http://dx.doi.org/10.1016/j. tcb.2012.08.013
63. Wanet A., Tacheny A., Arnould T., Renard P. miR- 212/132 expression and functions: within and beyond the neuronal compartment. Nucleic Acids Res 2012; 40:4742-53; PMID:22362752; http://dx.doi.org/10.1093/nar/gks151
64. Riemer C., Neidhold S., Burwinkel M., Schwarz A., Schultz J., Krätzschmar J., Mönning U., Baier M. Gene expression profiling of scrapie-infected brain tissue. Biochem Biophys Res Commun 2004; 323:556-64; PMID:15369787; http://dx.doi.org/10.1016/j. bbrc.2004.08.124
65. Booth S., Bowman C., Baumgartner R., Sorensen G., Robertson C., Coulthart M., Phillipson C., Somorjai RL. Identification of central nervous system genes involved in the host response to the scrapie agent during preclinical and clinical infection. J Gen Virol 2004; 85:3459-71; PMID:15483264; http://dx.doi.org/10.1099/vir.0.80110-0
66. Kim H.O., Snyder G.P., Blazey T.M., Race R.E., Chesebro B., Skinner PJ. Prion disease induced alterations in gene expression in spleen and brain prior to clinical symptoms. Adv Appl Bioinform Chem 2008; 1:29-50; PMID:21918605
67. Kyrkanides S., Olschowka J.A., Williams J.P., Hansen J.T., O'Banion MK. TNF alpha and IL-1beta mediate intercellular adhesion molecule-1 induction via microglia-astrocyte interaction in CNS radiation injury. J Neuroimmunol 1999; 95:95-106; PMID:10229119; http://dx.doi.org/10.1016/ S0165-5728(98)00270-7
68. Saba R., Gushue S., Huzarewich R.L., Manguiat K., Medina S., Robertson C., Booth SA. MicroRNA 146a (miR-146a) is over-expressed during prion disease and modulates the innate immune response and the microglial activation state. PLoS One 2012; 7:e30832; PMID:22363497; http://dx.doi.org/10.1371/journal.pone. 0030832
69. Mor E., Cabilly Y., Goldshmit Y., Zalts H., Modai S., Edry L., Elroy-Stein O., Shomron N. Species-specific microRNA roles elucidated following astrocyte activation. Nucleic Acids Res 2011; 39:3710-23; PMID:21247879; http://dx.doi.org/10.1093/nar/ gkq1325