MicroRNA-382 expression is elevated in the olfactory neuroepithelium of schizophrenia patients

Neurobiology of Disease

Volumn 55, Issue , 2013, Pages 1-10

  Mor, Eyal ^a   Kano, Shin Ichi ^b   Colantuoni, Carlo ^b,c,d   Sawa, Akira ^b   Navon, Ruth ^a   Shomron, Noam ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d LIEBER INSTITUTE FOR BRAIN DEVELOPMENT   (United States)

Author keywords

MicroRNA; MiRNA; Olfactory epithelium; Olfactory neuroepithelium; Schizophrenia

Indexed keywords

BIOLOGICAL MARKER; FIBROBLAST GROWTH FACTOR RECEPTOR 1; MICRORNA; MICRORNA 382; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FIBROBLAST GROWTH FACTOR RECEPTOR 1 GENE; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LASER CAPTURE MICRODISSECTION; LYMPHOBLASTOID CELL; MALE; NEUROEPITHELIUM; NEUROPATHOLOGY; OLFACTORY NEUROEPITHELIUM; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RNA ANALYSIS; SCHIZOPHRENIA; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPROUTY HOMOLOG 4 GENE; UPREGULATION;

ADOLESCENT; ADULT; CELLS, CULTURED; FEMALE; FIBROBLAST GROWTH FACTORS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LASER CAPTURE MICRODISSECTION; MALE; MICROARRAY ANALYSIS; MICRORNAS; MIDDLE AGED; NERVE TISSUE PROTEINS; NEURONS; OLFACTORY MUCOSA; POSTMORTEM CHANGES; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; TRANSFECTION; YOUNG ADULT;

EID: 84876736444     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.03.011     Document Type: Article

References (87)

1. Ach R.A., Wang H., Curry B. Measuring microRNAs: comparisons of microarray and quantitative PCR measurements, and of different total RNA prep methods. BMC Biotechnol. 2008, 8:69.
2. Arnold S.E., et al. Dysregulation of olfactory receptor neuron lineage in schizophrenia. Arch. Gen. Psychiatry 2001, 58:829-835.
3. Aston C., et al. Microarray analysis of postmortem temporal cortex from patients with schizophrenia. J. Neurosci. Res. 2004, 77:858-866.
4. Benes F.M., et al. Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:10164-10169.
5. Beveridge N.J., Cairns M.J. MicroRNA dysregulation in schizophrenia. Neurobiol. Dis. 2011, 46:263-271.
6. Beveridge N.J., et al. Dysregulation of miRNA 181b in the temporal cortex in schizophrenia. Hum. Mol. Genet. 2008, 17:1156-1168.
7. Beveridge N.J., et al. Schizophrenia is associated with an increase in cortical microRNA biogenesis. Mol. Psychiatry 2010, 15:1176-1189.
8. Bowden N.A., et al. Altered gene expression in the superior temporal gyrus in schizophrenia. BMC Genomics 2008, 9:199.
9. Brewer W.J., et al. Neuropsychological, olfactory, and hygiene deficits in men with negative symptom schizophrenia. Biol. Psychiatry 1996, 40:1021-1031.
10. Brewer W.J., et al. Stability of olfactory identification deficits in neuroleptic-naive patients with first-episode psychosis. Am. J. Psychiatry 2001, 158:107-115.
11. Bushati N., Cohen S.M. microRNA functions. Annu. Rev. Cell Dev. Biol. 2007, 23:175-205.
12. Cascella N.G., et al. Neurodevelopmental involvement in schizophrenia: the olfactory epithelium as an alternative model for research. J. Neurochem. 2007, 102:587-594.
13. Choi P.S., Zakhary L., Choi W.Y., Caron S., Alvarez-Saavedra E., Miska E.A., McManus M., Harfe B., Giraldez A.J., Horvitz H.R., et al. Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron 2008, 57(1):41-55.
14. Choi K.H., et al. Expression profiles of schizophrenia susceptibility genes during human prefrontal cortical development. J. Psychiatry Neurosci. 2009, 34:450-458.
15. Cimmino A., et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13944-13949.
16. Coleman E., et al. Odor identification impairments in schizophrenia: relationship with demographic measures, clinical variables, and diagnostic subtypes. CNS Spectr. 2002, 7:43-48.
17. Corcoran C., et al. Olfactory deficits, cognition and negative symptoms in early onset psychosis. Schizophr. Res. 2005, 80:283-293.
18. Feng J., et al. Evidence for X-chromosomal schizophrenia associated with microRNA alterations. PLoS One 2009, 4:e6121.
19. Feron F., et al. Altered adhesion, proliferation and death in neural cultures from adults with schizophrenia. Schizophr. Res. 1999, 40:211-218.
20. Fiore R., et al. Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J. 2009, 28:697-710.
21. Funk A.J., et al. Abnormal activity of the MAPK- and cAMP-associated signaling pathways in frontal cortical areas in postmortem brain in schizophrenia. Neuropsychopharmacology 2012, 37:896-905.
22. Furthauer M., et al. sprouty4 acts in vivo as a feedback-induced antagonist of FGF signaling in zebrafish. Development 2001, 128:2175-2186.
23. Gardiner E., et al. Imprinted DLK1-DIO3 region of 14q32 defines a schizophrenia-associated miRNA signature in peripheral blood mononuclear cells. Mol. Psychiatry 2011, 17(8):827-840.
24. Gaughran F., et al. Hippocampal FGF-2 and FGFR1 mRNA expression in major depression, schizophrenia and bipolar disorder. Brain Res. Bull. 2006, 70:221-227.
25. Genter M.B., et al. Microarray-based discovery of highly expressed olfactory mucosal genes: potential roles in the various functions of the olfactory system. Physiol. Genomics 2003, 16:67-81.
26. Glazov E.A., et al. Origin, evolution, and biological role of miRNA cluster in DLK-DIO3 genomic region in placental mammals. Mol. Biol. Evol. 2008, 25:939-948.
27. Good K.P., et al. Olfactory identification deficits in first-episode psychosis may predict patients at risk for persistent negative and disorganized or cognitive symptoms. Am. J. Psychiatry 2006, 163:932-933.
28. Griffiths-Jones S., et al. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008, 36:D154-D158.
29. Grimson A., et al. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 2007, 27:91-105.
30. Harrison P.J. Schizophrenia: a disorder of neurodevelopment?. Curr. Opin. Neurobiol. 1997, 7:285-289.
31. Hashimoto T., et al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J. Neurosci. 2003, 23:6315-6326.
32. Hebert J.M., et al. FGF signaling through FGFR1 is required for olfactory bulb morphogenesis. Development 2003, 130:1101-1111.
33. Hornstein E., et al. The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 2005, 438:671-674.
34. Hsu P., et al. Basic fibroblast growth factor and fibroblast growth factor receptors in adult olfactory epithelium. Brain Res. 2001, 896:188-197.
35. Hsu S.D., Chu C.H., Tsou A.P., Chen S.J., Chen H.C., Hsu P.W., Wong Y.H., Chen Y.H., Chen G.H., Huang H.D. miRNAMap 2.0: genomic maps of microRNAs in metazoan genomes. Nucleic Acids Res. 2008, 36:D165-D169. (Database issue).
36. Huang da W., et al. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
37. Huang B., et al. MicroRNA expression profiling during neural differentiation of mouse embryonic carcinoma P19 cells. Acta Biochim. Biophys. Sin. (Shanghai) 2009, 41:231-236.
38. Ishizuka K., et al. Negative symptoms of schizophrenia correlate with impairment on the University of Pennsylvania smell identification test. Neurosci. Res. 2010, 66:106-110.
39. Iwamoto K., et al. Altered expression of mitochondria-related genes in postmortem brains of patients with bipolar disorder or schizophrenia, as revealed by large-scale DNA microarray analysis. Hum. Mol. Genet. 2005, 14:241-253.
40. Jungerius B.J., et al. An association screen of myelin-related genes implicates the chromosome 22q11 PIK4CA gene in schizophrenia. Mol. Psychiatry 2008, 13:1060-1068.
41. Kano S., et al. Altered MHC class I expression in dorsolateral prefrontal cortex of nonsmoker patients with schizophrenia. Neurosci. Res. 2011, 71:289-293.
42. Kano S., et al. Genome-wide profiling of multiple histone methylations in olfactory cells: further implications for cellular susceptibility to oxidative stress in schizophrenia. Mol. Psychiatry 2013, (in press) (Epub ahead of print). 10.1038/mp.2012.120.
43. Kaya K.D., Karakulah G., Yakicier C.M., Acar A.C., Konu O. mESAdb: microRNA expression and sequence analysis database. Nucleic Acids Res. 2011, 39(Database issue):D170-180.
44. Kim S., et al. Suicide candidate genes associated with bipolar disorder and schizophrenia: an exploratory gene expression profiling analysis of post-mortem prefrontal cortex. BMC Genomics 2007, 8:413.
45. Kim A.H., et al. MicroRNA expression profiling in the prefrontal cortex of individuals affected with schizophrenia and bipolar disorders. Schizophr. Res. 2010, 124:183-191.
46. Kocerha J., et al. MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunction. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3507-3512.
47. Labalette C., et al. Hindbrain patterning requires fine-tuning of early krox20 transcription by Sprouty 4. Development 2011, 138:317-326.
48. Lai C.Y., et al. MicroRNA expression aberration as potential peripheral blood biomarkers for schizophrenia. PLoS One 2011, 6:e21635.
49. Layman W.S., et al. Reproductive dysfunction and decreased GnRH neurogenesis in a mouse model of CHARGE syndrome. Hum. Mol. Genet. 2011, 20:3138-3150.
50. Lewis C.M., et al. Genome scan meta-analysis of schizophrenia and bipolar disorder, Part II: schizophrenia. Am. J. Hum. Genet. 2003, 73:34-48.
51. Lin C.Y., et al. Better understanding of mechanisms of schizophrenia and bipolar disorder: from human gene expression profiles to mouse models. Neurobiol. Dis. 2012, 45:48-56.
52. Linsley P.S., et al. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol. Cell. Biol. 2007, 27:2240-2252.
53. Long J., et al. MicroRNA-29c is a signature microRNA under high glucose conditions that targets Sprouty homolog 1, and its in vivo knockdown prevents progression of diabetic nephropathy. J. Biol. Chem. 2011, 286:11837-11848.
54. Malaspina D., Coleman E. Olfaction and social drive in schizophrenia. Arch. Gen. Psychiatry 2003, 60:578-584.
55. McCall M.N., et al. MicroRNA profiling of diverse endothelial cell types. BMC Med. Genomics 2011, 4:78.
56. Meerson A., et al. Changes in brain MicroRNAs contribute to cholinergic stress reactions. J. Mol. Neurosci. 2010, 40:47-55.
57. Meiri E., Levy A., Benjamin H., Ben-David M., Cohen L., Dov A., Dromi N., Elyakim E., Yerushalmi N., Zion O., et al. Discovery of microRNAs and other small RNAs in solid tumors. Nucleic Acids Res. 2010, 38(18):6234-6246.
58. Miller B.H., et al. MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3125-3130.
59. Mirnics K., et al. Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 2000, 28:53-67.
60. Moberg P.J., Turetsky B.I. Scent of a disorder: olfactory functioning in schizophrenia. Curr. Psychiatry Rep. 2003, 5:311-319.
61. Moberg P.J., et al. Olfactory functioning in schizophrenia: relationship to clinical, neuropsychological, and volumetric MRI measures. J. Clin. Exp. Neuropsychol. 2006, 28:1444-1461.
62. Mor E., et al. Species-specific microRNA roles elucidated following astrocyte activation. Nucleic Acids Res. 2011, 39:3710-3723.
63. Nielsen C.B., et al. Determinants of targeting by endogenous and exogenous microRNAs and siRNAs. RNA 2007, 13:1894-1910.
64. Penno M.B., Pedrotti-Krueger M., Ray T. Cryopreservation of whole blood and isolated lymphocytes for B-cell immortalization. J. Tissue Cult. Methods 1993, 15:43-48.
65. Perez-Santiago J., et al. A combined analysis of microarray gene expression studies of the human prefrontal cortex identifies genes implicated in schizophrenia. J. Psychiatr. Res. 2012, 46:1464-1474.
66. Perkins D.O., et al. microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol. 2007, 8:R27.
67. Popova T., et al. Effect of RNA quality on transcript intensity levels in microarray analysis of human post-mortem brain tissues. BMC Genomics 2008, 9:91.
68. Qiu S., et al. Single-neuron RNA-Seq: technical feasibility and reproducibility. Front. Genet. 2012, 3:124.
69. Roussos P., et al. A system-level transcriptomic analysis of schizophrenia using postmortem brain tissue samples. Arch. Gen. Psychiatry 2012, 69:1205-1213.
70. Santarelli D.M., et al. Upregulation of dicer and microRNA expression in the dorsolateral prefrontal cortex Brodmann area 46 in schizophrenia. Biol. Psychiatry 2011, 69:180-187.
71. Sattler R., et al. Human nasal olfactory epithelium as a dynamic marker for CNS therapy development. Exp. Neurol. 2011, 232:203-211.
72. Sawa A., Cascella N.G. Peripheral olfactory system for clinical and basic psychiatry: a promising entry point to the mystery of brain mechanism and biomarker identification in schizophrenia. Am. J. Psychiatry 2009, 166:137-139.
73. Sawa A., et al. Increased apoptosis of Huntington disease lymphoblasts associated with repeat length-dependent mitochondrial depolarization. Nat. Med. 1999, 5:1194-1198.
74. Schratt G.M., et al. A brain-specific microRNA regulates dendritic spine development. Nature 2006, 439:283-289.
75. Seitz H., et al. A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res. 2004, 14:1741-1748.
76. Stedman T.J., Clair A.L. Neuropsychological, neurological and symptom correlates of impaired olfactory identification in schizophrenia. Schizophr. Res. 1998, 32:23-30.
77. Tajinda K., et al. Neuronal biomarkers from patients with mental illnesses: a novel method through nasal biopsy combined with laser-captured microdissection. Mol. Psychiatry 2010, 15:231-232.
78. Terwisscha van Scheltinga A.F., et al. Fibroblast growth factors in schizophrenia. Schizophr. Bull. 2010, 36:1157-1166.
79. Urdinguio R.G., et al. Disrupted microRNA expression caused by Mecp2 loss in a mouse model of Rett syndrome. Epigenetics 2010, 5:656-663.
80. Vawter M.P., et al. Genome scans and gene expression microarrays converge to identify gene regulatory loci relevant in schizophrenia. Hum. Genet. 2006, 119:558-570.
81. Vo N., et al. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16426-16431.
82. Volk N., Shomron N. Versatility of MicroRNA biogenesis. PLoS One 2011, 6:e19391.
83. Voorhoeve P.M., et al. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 2006, 124:1169-1181.
84. Wang W.X., et al. Patterns of microRNA expression in normal and early Alzheimer's disease human temporal cortex: white matter versus gray matter. Acta Neuropathol. 2011, 121:193-205.
85. Weickert C.S., et al. Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain. Arch. Gen. Psychiatry 2004, 61:544-555.
86. Yu T., et al. Sprouty genes prevent excessive FGF signalling in multiple cell types throughout development of the cerebellum. Development 2011, 138:2957-2968.
87. Zaharieva I., et al. Association study in the 5q31-32 linkage region for schizophrenia using pooled DNA genotyping. BMC Psychiatry 2008, 8:11.