Cell-type-specific Jumonji histone demethylase gene expression in the healthy rat CNS: Detection by a novel flow cytometry method

ASN Neuro

Volumn 6, Issue 3, 2014, Pages 193-207

  Smith, Stephanie M C ^a   Kimyon, Rebecca S ^a   Watters, Jyoti J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Adult; Cell sorting; Epigenetic; Gene expression; miRNA; Zinc fixation

Indexed keywords

BETA TUBULIN; CD11B ANTIGEN; CD68 ANTIGEN; CELL SURFACE MARKER; EXCITATORY AMINO ACID TRANSPORTER 1; GLIAL FIBRILLARY ACIDIC PROTEIN; HISTONE DEMETHYLASE; HISTONE H3; MESSENGER RNA; MICRORNA; SMALL UNTRANSLATED RNA; EXCITATORY AMINO ACID TRANSPORTER 2; NERVE PROTEIN; SLC1A2 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL POPULATION; CELL SELECTION; CELL SPECIFICITY; CENTRAL NERVOUS SYSTEM; FLOW CYTOMETRY; GENE CONTROL; GENE EXPRESSION; HISTONE METHYLATION; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANALYSIS OF VARIANCE; ANIMAL; CYTOLOGY; ENZYMOLOGY; GENETICS; GLIA; METABOLISM; NERVE CELL; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD11B; CENTRAL NERVOUS SYSTEM; EXCITATORY AMINO ACID TRANSPORTER 2; FLOW CYTOMETRY; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MALE; MICRORNAS; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 84901723152     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1042/AN20130050     Document Type: Article

References (53)

1. Blackwell T. S, Christman JW (1997) The role of nuclear factor-κB in cytokine gene regulation. Am J Resp Cell Mol Biol 17:3-9.
2. Castermans D., Vermeesch JR, Fryns J-P, Steyaert JG, Van de Ven WJ, Creemers JW, Devriendt K (2007) Identification and characterization of the TRIP8 and REEP3 genes on chromosome 10q21. 3 as novel candidate genes for autism. Eur J Hum Genet 15:422-431.
3. Chassevent A., Daver A, Bertrand G, Coic H, Geslin J, Bidabe MC, George P, Larra F. (1984) Comparative flow DNA analysis of different cell suspensions in breast carcinoma. Cytometry 5:263-267.
4. Das N. D, Jung KH, Chai YG (2010) The role of NF-kappaB and H3K27me3 demethylase, Jmjd3, on the anthrax lethal toxin tolerance of RAW 264.7 cells. PLoS ONE 5:e9913.
5. De Santa F, Narang V, Yap ZH, Tusi BK, Burgold T, Austenaa L, Bucci G, Caganova M., Notarbartolo S, Casola S, Testa G, Sung WK, Wei CL, Natoli G (2009) Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J 28:3341-3352.
6. Diez C., Bertsch G, Simm A (1999) Isolation of full-size mRNA from cells sorted by flow cytometry. J Biochem Biophys Methods 40:69-80.
7. Doyle J. P, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, Ma G, Bupp S, Shrestha P., Shah RD, Doughty ML, Gong S, Greengard P, Heintz N (2008) Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135:749-762.
8. Doyle S. L, O'Neill LA (2006) Toll-like receptors: from the discovery of NF-κB to new insights into transcriptional regulations in innate immunity. Biochem Pharmacol 72:1102-1113.
9. Esser C., Gottlinger C, Kremer J, Hundeiker C, Radbruch A (1995) Isolation of full-size mRNA from ethanol-fixed cells after cellular immunofluorescence staining and fluorescence-activated cell sorting (FACS). Cytometry 21:382-386.
10. Fanous S., Guez-Barber DH, Goldart EM, Schrama R, Theberge FRM, Shaham Y, Hope B. T (2013) Unique gene alterations are induced in FACS-purified Fos-positive neurons activated during cue-induced relapse to heroin seeking. J Neurochem 124:100-108.
11. Guez-Barber D, Fanous S, Golden SA, Schrama R, Koya E, Stern AL, Bossert JM, Harvey B. K, Picciotto MR, Hope BT (2011a) FACS identifies unique cocaine-induced gene regulation in selectively activated adult striatal neurons. J Neurosci 31:4251-4259.
12. Guez-Barber D, Fanous S, Golden SA, Schrama R, Koya E, Stern AL, Bossert JM, Harvey B. K, Picciotto MR, Hope BT (2011b) FACS identifies unique cocaine-induced gene regulation in selectively activated adult striatal neurons. J Neurosci 31:4251-4259.
13. Guez-Barber D, Fanous S, Harvey BK, Zhang Y, Lehrmann E, Becker KG, Picciotto M. R, Hope BT (2012) FACS purification of immunolabeled cell types from adult rat brain. J Neurosci Methods 203:10-18.
14. Heiman M., Schaefer A, Gong S, Peterson JD, Day M, Ramsey KE, Suárez-Fariñas M, Schwarz C, Stephan DA, Surmeier DJ, Greengard P, Heintz N. (2008) A translational profiling approach for the molecular characterization of CNS cell types. Cell 135:738-748.
15. Huang C., Chen J, Zhang T, Zhu Q, Xiang Y, Chen CD, Jing N (2010a) The dual histone demethylase KDM7A promotes neural induction in early chick embryos. Dev Dyn 239:3350-3357.
16. Huang C., Xiang Y, Wang Y, Li X, Xu L, Zhu Z, Zhang T, Zhu Q, Zhang K, Jing N, Chen C. D (2010b) Dual-specificity histone demethylase KIAA1718 (KDM7A) regulates neural differentiation through FGF4. Cell Res 20:154-165.
17. Jensen U. B, Owens DM, Pedersen S, Christensen R (2010) Zinc fixation preserves flow cytometry scatter and fluorescence parameters and allows simultaneous analysis of DNA content and synthesis, and intracellular and surface epitopes. Cytometry A 77A:798-804.
18. Kimelberg H. K (2004) The problem of astrocyte identity. Neurochem Int 45:191-202.
19. Kleine-Kohlbrecher D, Christensen J, Vandamme J, Abarrategui I, Bak M, Tommerup N., Shi X, Gozani O, Rappsilber J, Salcini AE, Helin K (2010) A functional link between the histone demethylase PHF8 and the transcription factor ZNF711 in X-linked mental retardation. Mol Cell 38:165-178.
20. Kooistra S. M, Helin K (2012) Molecular mechanisms and potential functions of histone demethylases. Nat Rev Mol Cell Biol 13:297-311.
21. Laumonnier F., Holbert S, Ronce N, Faravelli F, Lenzner S, Schwartz CE, Lespinasse J., Van Esch H, Lacombe D, Goizet C, Phan-Dinh Tuy F, van Bokhoven H., Fryns J-P, Chelly J, Ropers H-H, Moraine C, Hamel BCJ, Briault S. (2005) Mutations in PHF8 are associated with X linked mental retardation and cleft lip/cleft palate. J Med Genet 42:780-786.
22. Lederer D., Grisart B, Digilio Maria C, Benoit V, Crespin M, Ghariani Sophie C, Maystadt I., Dallapiccola B, Verellen-Dumoulin C (2012) Deletion of KDM6A, a histone demethylase interacting with MLL2, in three patients with Kabuki syndrome. Am J Hum Genet 90:119-124.
23. Liu Q.-R, Rubio FJ, Bossert JM, Marchant NJ, Fanous S, Hou X, Shaham Y, Hope BT (2014) Detection of molecular alterations in methamphetamine-activated Fos-expressing neurons from a single rat dorsal striatum using fluorescence-activated cell sorting (FACS). J Neurochem 128:173-185.
24. Livak K. J, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-__CT method. Methods 25:402-408.
25. Lobo M. K, Karsten SL, Gray M, Geschwind DH, Yang XW (2006) FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains. Nat Neurosci 9:443-452.
26. Luo C. X, Zhu XJ, Zhou QG, Wang B, Wang W, Cai HH, Sun YJ, Hu M, Jiang J, Hua Y., Han X, Zhu DY (2007) Reduced neuronal nitric oxide synthase is involved in ischemia-induced hippocampal neurogenesis by up-regulating inducible nitric oxide synthase expression. J Neurochem 103: 1872-1882.
27. Luo X., Liu Y, Kubicek S, Myllyharju J, Tumber A, Ng S, Che KH, Podoll J, Heightman T. D, Oppermann U, Schreiber SL, Wang X (2011) A selective inhibitor and probe of the cellular functions of Jumonji C domain-containing histone demethylases. J Am Chem Soc 133:9451-9456.
28. Lykidis D., Van Noorden S, Armstrong A, Spencer-Dene B, Li J, Zhuang Z, Stamp GWH (2007) Novel zinc-based fixative for high quality DNA, RNA and protein analysis. Nucleic Acids Res 35:e85.
29. Miyake N., Koshimizu E, Okamoto N, Mizuno S, Ogata T, Nagai T, Kosho T, Ohashi H., Kato M, Sasaki G, Mabe H, Watanabe Y, Yoshino M, Matsuishi T, Takanashi J, Shotelersuk V, Tekin M, Ochi N, Kubota M, Ito N, Ihara K, Hara T., Tonoki H, Ohta T, Saito K, Matsuo M, Urano M, Enokizono T, Sato A, Tanaka H, Ogawa A, Fujita T, Hiraki Y, Kitanaka S, Matsubara Y, Makita T, Taguri M, Nakashima M, Tsurusaki Y, Saitsu H, Yoshiura K, Matsumoto N, Niikawa N (2013) MLL2 and KDM6A mutations in patients with Kabuki syndrome. Am J Med Genet A. 161:2234-2243.
30. Molofsky A. V, Krenick R, Ullian E, Tsai H-h, Deneen B, Richardson WD, Barres BA, Rowitch DH (2012) Astrocytes and disease: a neurodevelopmental perspective. Genes Dev 26:891-907.
31. Nikodemova M., Watters JJ (2012) Efficient isolation of live microglia with preserved phenotypes from adult mouse brain. J Neuroinflammation 9:147.
32. O'Connell RM, Zhao JL, Rao DS (2011) MicroRNA function in myeloid biology. Blood 118:2960-2969.
33. Perez O. D, Mitchell D, Campos R, Gao G-J, Li L, Nolan GP (2001) Multiparameter analysis of intracellular phosphoepitopes in immunophenotyped cell populations by flow cytometry. In Current Protocols in Cytometry, Wiley.
34. Ponomarev E. D, Veremeyko T, Weiner HL (2013) MicroRNAs are universal regulators of differentiation, activation, and polarization of microglia and macrophages in normal and diseased CNS. Glia 61:91-103.
35. Qiu J., Shi G, Jia Y, Li J, Wu M, Li J, Dong S, Wong J (2010) The X-linked mental retardation gene PHF8 is a histone demethylase involved in neuronal differentiation. Cell Res 20:908-918.
36. Rom S., Rom I, Passiatore G, Pacifici M, Radhakrishnan S, Del Valle L, Piña-Oviedo S, Khalili K, Eletto D, Peruzzi F (2010) CCL8/MCP-2 is a target for mir-146a in HIV-1-infected human microglial cells. FASEB J 24:2292-2300.
37. Saba R., Gushue S, Huzarewich RL, Manguiat K, Medina S, Robertson C, Booth SA (2012) MicroRNA 146a (miR-146a) is over-expressed during prion disease and modulates the innate immune response and the microglial activation state. PLoS ONE 7:e30832.
38. Saldanha A. J (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20:3246-3248.
39. Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, Freeman T., Saporta S, Janssen W, Patel N, Cooper DR, Sanberg PR (2000) Adult Bone Marrow Stromal Cells Differentiate into Neural Cells in Vitro. Exp Neurol 164:247-256.
40. Sanz E., Yang L, Su T, Morris DR, McKnight GS, Amieux PS (2009) Cell-type-specific isolation of ribosome-associated mRNA from complex tissues. Proc Natl Acad Sci USA 106:13939-13944.
41. Satoh T., Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, Kumagai Y, Miyake T, Matsushita K., Okazaki T, Saitoh T, Honma K, Matsuyama T, Yui K, Tsujimura T., Standley DM, Nakanishi K, Nakai K, Akira S (2010) The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nature Immunol 11:936-944.
42. Schmid I., Merlin S, Perfetto SP (2003) Biosafety concerns for shared flow cytometry core facilities. Cytometry A 56A:113-119.
43. Shapiro H. (1988) Parameters and probes. In Practical Flow Cytometry, 2nd edn., Alan R. Liss, New York, NY.
44. Shin S., Janknecht R (2007) Activation of androgen receptor by histone demethylases JMJD2A and JMJD2D. Biochem Biophys Res Commun 359:742-746.
45. Shulha H. P, Cheung I, Whittle C, Wang J, Virgil D, Lin CL, Guo Y, Lessard A, Akbarian S., Weng Z (2012) Epigenetic signatures of autism: trimethylated H3K4 landscapes in prefrontal neurons. Arch Gen Psychiatry 69:314.
46. Smirnova L., Gräfe A, Seiler A, Schumacher S, Nitsch R, Wulczyn FG (2005) Regulation of miRNA expression during neural cell specification. Eur J Neurosci 21:1469-1477.
47. Takeuchi T., Watanabe Y, Takano-Shimizu T, Kondo S (2006) Roles of jumonji and jumonji family genes in chromatin regulation and development. Dev Dyn 235:2449-2459.
48. Tang Y., Li T, Li J, Yang J, Liu H, Zhang XJ, Le W (2014) Jmjd3 is essential for the epigenetic modulation of microglia phenotypes in the immune pathogenesis of Parkinson's disease. Cell Death Differ 21: 369-380.
49. Vincent V. A, DeVoss JJ, Ryan HS, Murphy GM (2002) Analysis of neuronal gene expression with laser capture microdissection. J Neurosci Res 69:578-586.
50. Wester K., Asplund A, Bäckvall H, Micke P, Derveniece A, Hartmane I, Malmström P-U, Pontén F (2003) Zinc-based fixative improves preservation of genomic DNA and proteins in histoprocessing of human tissues. Lab Investig 83:889-899.
51. Wolf S. S, Patchev VK, Obendorf M (2007) A novel variant of the putative demethylase gene, s-JMJD1C, is a coactivator of the AR. Arch Biochem Biophys 460:56-66.
52. Xu J., Deng X, Watkins R, Disteche CM (2008) Sex-specific differences in expression of histone demethylases Utx and Uty in mouse brain and neurons. J Neurosci 28:4521-4527.
53. Youn M.-Y, Yokoyama A, Fujiyama-Nakamura S, Ohtake F, Minehata K-i, Yasuda H., Suzuki T, Kato S, Imai Y (2012) JMJD5, a Jumonji C (JmjC) domain-containing protein, negatively regulates osteoclastogenesis by facilitating NFATc1 protein degradation. J Biol Chem 287: 12994-13004.