Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T05:17:22.824Z Has data issue: false hasContentIssue false
  • English
  • Français

Astrocyte proximity modulates the myelination gene fabric of oligodendrocytes

Published online by Cambridge University Press:  05 January 2011

Sanda Iacobas  and
Dumitru A. Iacobas
Sanda Iacobas
Affiliation:
Neuroscience, Albert Einstein College of Medicine, New York, USA
Dumitru A. Iacobas*
Affiliation:
Neuroscience, Albert Einstein College of Medicine, New York, USA
*
Correspondence should be addressed to: Dumitru A. Iacobas, D.P. Purpura Department of Neuroscience, Kennedy Center, Room No. 713, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx-New York, NY 10461, USA phone: (718) 430-3326 fax: (718) 430-8594 email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Extensive literature documented that astrocytes release neurotransmitters, cytokines and other signaling molecules to modulate migration, maturation and myelin synthesis of oligodendrocytes through mechanisms primarily converging on cytosolic [Ca2+] transients. Considering the long-term effects, it is expected that astrocyte-conditioned medium is a major regulator of gene expression in oligodendrocytes even in the absence of cytosol-to-cytosol communication via astrocyte–oligodendrocyte gap junction channels. Indeed, by comparing the transcriptomes of immortalized precursor oligodendrocyte (Oli-neu) cells when cultured alone and co-cultured with non-touching astrocytes we found profound changes in the gene expression level, control and networking. Remarkably, the astrocyte proximity was more effective in remodeling the myelination (MYE) gene fabric and its control by cytokine receptor (CYR)-modulated intercellular Ca2+-signaling (ICS) transcriptomic network than the dibutyryl-cAMP (db-cAMP) treatment-induced transformation into myelin-associated glycoprotein-positive oligodendrocyte-like cells. Moreover, astrocyte proximity up-regulated 37 MYE genes and switched on another 14 MYE, 23 ICS and 4 CYR genes, enhancing the roles of the leukemia inhibitory factor receptor and connexins Cx29 and Cx47. The novel prominent gene analysis identified the enhancer of zeste homolog 2 as the most relevant MYE gene in the astrocyte proximity, notch gene homolog 1 in control and B-cell leukemia/lymphoma 2 in differentiated Oli-neu cells.

Keywords

Calcium signalingconnexinEzh2LifrNotch1
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Issue 3 , August 2010 , pp. 157 - 169
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arthur, A.T., Armati, P.J., Bye, C., Southern MS Genetics Consortium, Heard, R.N., Stewart, G.J. et al. (2008) Genes implicated in multiple sclerosis pathogenesis from consilience of genotyping and expression profiles in relapse and remission. BMC Medical Genetics 9, 17.CrossRefGoogle ScholarPubMed
Bartzokis, G. (2009) Alzheimer's disease as homeostatic responses to age-related myelin breakdown. Neurobiology of Aging [Epub ahead of print] doi: 10.1016/j.neurobiolaging.2009.08.007Google ScholarPubMed
Biancotti, J.C., Kumar, S. and de Vellis, J. (2008) Activation of inflammatory response by a combination of growth factors in cuprizone-induced demyelinated brain leads to myelin repair. Neurochemical Research 33, 2615–2628.CrossRefGoogle ScholarPubMed
Brand-Schieber, E., Werner, P., Iacobas, D.A., Iacobas, S., Beelitz, M., Lowery, S.L. et al. (2005) Connexin43, the major gap junction protein of astrocytes, is down regulated in an animal model of multiple sclerosis. Journal of Neuroscience Research 80, 798–808.CrossRefGoogle Scholar
Brosnan, C.F. and John, G.R. (2009a) Revisiting Notch in remyelination of multiple sclerosis lesions. Journal of Clinical Investigation 119, 10–13.Google ScholarPubMed
Brosnan, C.F. and John, G.R. (2009b) Notch1 signaling plays a role in regulating precursor differentiation during CNS remyelination. Proceedings of the National Academy of Sciences of the U.S.A. 106, 19162–19167.Google Scholar
Butt, A.M. (2006) Neurotransmitter-mediated calcium signalling in oligodendrocyte physiology and pathology. Glia 54, 666–675.CrossRefGoogle ScholarPubMed
Cahoy, J.D., Emery, B., Kaushal, A., Foo, L.C., Zamanian, J.L., Christopherson, K.S. et al. (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. Journal of Neuroscience 28, 264–278.CrossRefGoogle Scholar
Carmel, J.B., Galante, A., Soteropoulos, P., Tolias, P., Recce, M., Young, W. et al. (2001) Gene expression profiling of acute spinal cord injury reveals spreading inflammatory signals and neuron loss. Physiological Genomics 7, 201–213.CrossRefGoogle ScholarPubMed
Chen, Y., Wu, H., Wang, S., Koito, H., Li, J., Ye, F. et al. (2009) The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nature Neuroscience 12, 1398–1406.CrossRefGoogle ScholarPubMed
Chesneau, V., Becherer, J.D., Zheng, Y., Erdjument-Bromage, H., Tempst, P. and Blobel, C.P. (2003) Catalytic properties of ADAM19. Journal of Biological Chemistry 278, 22331–22340.CrossRefGoogle ScholarPubMed
Das Sarma, J., Ciric, B., Marek, R., Sadhukhan, S., Caruso, M.L., Shafagh, J. et al. (2009) Functional interleukin-17 receptor A is expressed in central nervous system glia and upregulated in experimental autoimmune encephalomyelitis. Journal of Neuroinflammation 6, 14.Google ScholarPubMed
Desai, M.K., Sudol, K.L., Janelsins, M.C., Mastrangelo, M.A., Frazer, M.E. and Bowers, W.J. (2009) Triple-transgenic Alzheimer's disease mice exhibit region-specific abnormalities in brain myelination patterns prior to appearance of amyloid and tau pathology. Glia 57, 54–65.CrossRefGoogle ScholarPubMed
Di Giovanni, S., Knoblach, S.M., Brandoli, C., Aden, S.A., Hoffman, E.P. and Faden, A.I. (2003) Gene profiling in spinal cord injury shows role of cell cycle in neuronal death. Annals of Neurology 53, 454–468.CrossRefGoogle ScholarPubMed
Fields, R.D. (2004) Volume transmission in activity-dependent regulation of myelinating glia. Neurochemistry International 45, 503–509. Review.CrossRefGoogle ScholarPubMed
Fields, R.D. (2008) Oligodendrocytes changing the rules: action potentials in glia and oligodendrocytes controlling action potentials. Neuroscientist 14, 540–543.CrossRefGoogle ScholarPubMed
Fields, R.D. and Burnstock, G. (2006) Purinergic signalling in neuron–glia interactions. Nature Reviews Neuroscience 7, 423–436.CrossRefGoogle ScholarPubMed
Finzsch, M., Stolt, C.C., Lommes, P. and Wegner, M. (2008) Sox9 and Sox10 influence survival and migration of oligodendrocyte precursors in the spinal cord by regulating PDGF receptor alpha expression. Development 135, 637–646.CrossRefGoogle ScholarPubMed
Gokhan, S., Marin-Husstege, M., Yung, S.Y., Fontanez, D., Casaccia-Bonnefil, P. and Mehler, M.F. (2005) Combinatorial profiles of oligodendrocyte-selective classes of transcriptional regulators differentially modulate myelin basic protein gene expression. Journal of Neuroscience 25, 8311–8321.CrossRefGoogle ScholarPubMed
Hakak, Y., Walker, J.R., Li, C., Wong, W.H., Davis, K.L., Buxbaum, J.D. et al. (2001) Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proceedings of the National Academy of Sciences of the U.S.A. 98, 4746–4751.CrossRefGoogle ScholarPubMed
Haroutunian, V., Katsel, P., Dracheva, S., Stewart, D.G. and Davis, K.L. (2007) Variations in oligodendrocyte-related gene expression across multiple cortical regions: implications for the pathophysiology of schizophrenia. International Journal of Neuropsychopharmacology 10, 565–573.CrossRefGoogle ScholarPubMed
He, Y. and Casaccia-Bonnefil, P. (2008) The Yin and Yang of YY1 in the nervous system. Journal of Neurochemistry 106, 1493–1502.CrossRefGoogle ScholarPubMed
He, Y., Sandoval, J. and Casaccia-Bonnefil, P. (2007) Events at the transition between cell cycle exit and oligodendrocyte progenitor differentiation: the role of HDAC and YY1. Neuron Glia Biology 3, 221–231.CrossRefGoogle ScholarPubMed
Iacobas, D.A., Urban, M., Iacobas, S., Scemes, E. and Spray, D.C. (2003) Array analysis of gene expression in connexin-43 null astrocytes. Physiological Genomics 15, 177–190.CrossRefGoogle ScholarPubMed
Iacobas, D.A., Iacobas, S., Urban-Maldonado, M. and Spray, D.C. (2005) Sensitivity of the brain transcriptome to connexin ablation. Biochimica et Biofisica Acta 1711, 183–196.CrossRefGoogle ScholarPubMed
Iacobas, D.A., Iacobas, S., Werner, P., Scemes, E. and Spray, D.C. (2007 a) Alteration of transcriptomic networks in adoptive transfer experimental autoimmune encephalomyelitis. Frontiers in Integrative Neuroscience 1, 10. doi: 10.3389/neuro.07/010.2007.CrossRefGoogle ScholarPubMed
Iacobas, D.A., Iacobas, S. and Spray, D.C. (2007b) Connexin43 and the brain transcriptome of the newborn mice. Genomics 89, 113–123.CrossRefGoogle ScholarPubMed
Iacobas, D.A., Iacobas, S. and Spray, D.C. (2007c) Connexin-dependent transcellular transcriptomic networks in mouse brain. Progress in Biophysics and Molecular Biology 94, 168–184.CrossRefGoogle ScholarPubMed
Iacobas, D.A., Iacobas, S., Urban-Maldonado, M., Scemes, E. and Spray, D.C. (2008) Similar transcriptomic alterations in Cx43 knockdown and knockout astrocytes. Cell Communications and Adhesion 15, 195–206.CrossRefGoogle ScholarPubMed
Iacobas, D.A., Iacobas, S. and Haddad, G.G. (2010a) Heart rhythm genomic fabric in hypoxia. Biochemical and Biophysical Research Communication 391, 1769–1774.CrossRefGoogle ScholarPubMed
Iacobas, D.A., Iacobas, S., Thomas, N. and Spray, D.C. (2010b) Sex-dependent gene regulatory networks of the heart rhythm. Functional and Integrative Genomics. 10, 73–86.CrossRefGoogle ScholarPubMed
Ishibashi, T., Dakin, K.A., Stevens, B., Lee, P.R., Kozlov, S.V., Stewart, C.L. and Fields, R.D. (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49, 823–832.CrossRefGoogle ScholarPubMed
Ishibashi, T., Lee, P.R., Baba, H. and Fields, D.R. (2009) Leukemia inhibitory factor regulates the timing of oligodendrocyte development and myelination in the postnatal optic nerve. Journal of Neuroscience Research 87, 3343–3355.CrossRefGoogle ScholarPubMed
Jayadev, S., Leverenz, J.B., Steinbar, t E., Stahl, J., Klunk, W., Yu, C.E. et al. (2010) Alzheimer's disease phenotypes and genotypes associated with mutations in presenilin 2. Brain 133, 1143–1154.CrossRefGoogle ScholarPubMed
Jung, M., Krämer, E., Grzenkowski, M., Tang, K., Blakemore, W., Aguzz, A. et al. (1995) Lines of murine oligodendroglial precursor cells immortalized by activated neu tyrosine kinase show distinct degrees of interaction with axons in vitro and in vivo. European Journal of Neuroscience 7, 1245–1265.CrossRefGoogle ScholarPubMed
Kieseier, B.C., Pischel, H., Neuen-Jacob, E., Tourtellotte, W.W. and Hartung, H.P. (2003) ADAM-10 and ADAM-17 in the inflamed human CNS. Glia 42, 398–405.CrossRefGoogle ScholarPubMed
Kippert, A., Trajkovic, K., Fitzner, D., Opitz, L. and Simons, M. (2008) Identification of Tmem10/Opalin as a novel marker for oligodendrocytes using gene expression profiling. BMC Neuroscience 25, 40.CrossRefGoogle Scholar
Kumar, S., Mattan, N.S. and de Vellis, J. (2006) Canavan disease: a white matter disorder. Mental Retardation and Developmental Disabilities Research Reviews 12, 157–165.CrossRefGoogle ScholarPubMed
Lauriat, T.L., Shiue, L., Haroutunian, V., Verbitsky, M., Ares, M. Jr., Ospina, L. et al. (2008) Developmental expression profile of quaking, a candidate gene for schizophrenia, and its target genes in human prefrontal cortex and hippocampus shows regional specificity. Journal of Neuroscience Research 86, 785–796.CrossRefGoogle ScholarPubMed
Lee, P.R. and Fields, R.D. (2009) Regulation of myelin genes implicated in psychiatric disorders by functional activity in axons. Frontiers in Neuroanatomy 3, 4.CrossRefGoogle ScholarPubMed
Linker, R., Gold, R. and Luhder, F. (2009) Function of neurotrophic factors beyond the nervous system: inflammation and autoimmune demyelination. Critical Reviews in Immunology 29, 43–68.CrossRefGoogle ScholarPubMed
Lock, C., Hermans, G., Pedotti, R., Brendolan, A., Schadt, E., Garren, H. et al. (2002) Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nature Medicine 8, 500–508.CrossRefGoogle ScholarPubMed
Lutz, S.E., Zhao, Y., Gulinello, M., Lee, S.C., Raine, C.S. and Brosnan, C.F. (2009) Deletion of astrocyte connexins 43 and 30 leads to a dysmyelinating phenotype and hippocampal CA1 vacuolation. Journal of Neuroscience 29, 7743–7752.CrossRefGoogle ScholarPubMed
Marin-Husstege, M., He, Y., Li, J., Kondo, T., Sablitzky, F. and Casaccia-Bonnefil, P. (2006) Multiple roles of Id4 in developmental myelination: predicted outcomes and unexpected findings. Glia 54, 285–296.CrossRefGoogle ScholarPubMed
Marta, C.B., Montano, M.B., Taylor, C.M., Taylor, A.L., Bansal, R. and Pfeiffer, S.E. (2005) Signaling cascades activated upon antibody cross-linking of myelin oligodendrocyte glycoprotein: potential implications for multiple sclerosis. Journal of Biological Chemistry 280, 8985–8993.CrossRefGoogle ScholarPubMed
Maysami, S., Nguyen, D., Zobel, F., Pitz, C., Heine, S., Höpfner, M. et al. (2006) Modulation of rat oligodendrocyte precursor cells by the chemokine CXCL12. Neuroreport 17, 1187–1190.CrossRefGoogle ScholarPubMed
McCullumsmith, R.E., Gupta, D., Beneyto, M., Kreger, E., Haroutunian, V., Davis, K.L. et al. (2007) Expression of transcripts for myelination-related genes in the anterior cingulate cortex in schizophrenia. Schizophrenia Research 90, 15–27.CrossRefGoogle ScholarPubMed
Mehler, M.F. (2002) Mechanisms regulating lineage diversity during mammalian cerebral cortical neurogenesis and gliogenesis. Results and Problems in Cell Differentiation 39, 27–52. Review.CrossRefGoogle ScholarPubMed
Menichella, D.M., Goodenough, D.A., Sirkowski, E., Scherer, S.S. and Paul, D.L. (2003) Connexins are cirtical for normal myelination in the CNS. Journal of Neuroscience 23, 5963–5973.CrossRefGoogle Scholar
Nair, A., Frederick, T.J. and Miller, S.D. (2008) Astrocytes in multiple sclerosis: a product of their environment. Cellular and Molecular Life Sciences 65, 2702–2720.CrossRefGoogle ScholarPubMed
Omari, K.M., Lutz, S.E., Santambrogio, L., Lira, S.A. and Raine, C.S. (2009) Neuroprotection and remyelination after autoimmune demyelination in mice that inducibly overexpress CXCL1. American Journal of Pathology 174, 164–176.CrossRefGoogle ScholarPubMed
Orthmann-Murphy, J.L., Abrams, C.K. and Scherer, S.S. (2008) Gap junctions couple astrocytes and oligodendrocytes. Journal of Molecular Neuroscience 35, 101–116.CrossRefGoogle ScholarPubMed
Parenti, R., Cicirata, F., Zappalà, A., Catania, A., La Delia, F., Cicirata, V. et al. (2010) Dynamic expression of Cx47 in mouse brain development and in the cuprizone model of myelin plasticity. Glia. 58, 1594–1609.CrossRefGoogle ScholarPubMed
Raser, J.M. and O'Shea, E.K. (2005) Noise in gene expression: origins, on sequences, and control. Science 309, 2010–2013.CrossRefGoogle Scholar
Reeves, T.M., Phillips, L.L. and Povlishock, J.T. (2005) Myelinated and unmyelinated axons of the corpus callosum differ in vulnerability and functional recovery following traumatic brain injury. Experimental Neurology 96, 126–137.CrossRefGoogle Scholar
Rowe, W.B., Blalock, E.M., Chen, K.C., Kadish, I., Wang, D., Barrett, J.E. et al. (2007) Hippocampal expression analyses reveal selective association of immediate-early, neuroenergetic, and myelinogenic pathways with cognitive impairment in aged rats. Journal of Neuroscience 27, 3098–3110.CrossRefGoogle ScholarPubMed
Scherer, S.S. and Wrabetz, L. (2008) Molecular mechanisms of inherited demyelinating neuropathies. Glia 56, 1578–1589.CrossRefGoogle ScholarPubMed
See, J.M. and Grinspan, J.B. (2009) Sending mixed signals: bone morphogenetic protein in myelination and demyelination. Journal of Neuropathology and Experimental Neurology 68, 595–604.CrossRefGoogle ScholarPubMed
Seifert, T., Bauer, J., Weissert, R., Fazekas, F. and Storch, M.K. (2007) Notch1 and its ligand Jagged1 are present in remyelination in a T-cell- and antibody-mediated model of inflammatory demyelination. Acta Neuropathologica 113, 195–203.CrossRefGoogle Scholar
Sher, F., Rössler, R., Brouwer, N., Balasubramaniyan, V., Boddeke, E. and Copray, S. (2008) Differentiation of neural stem cells into oligodendrocytes: involvement of the polycomb group protein Ezh2. Stem Cells 26, 2875–2883.CrossRefGoogle ScholarPubMed
Simons, M. and Trotter, J. (2007) Wrapping it up: the cell biology of myelination. Current Opinion in Neurobiology 17, 533–540.CrossRefGoogle ScholarPubMed
Spray, D.C. (2005) Illuminating gap junctions. Nature Methods 2, 12–14.CrossRefGoogle ScholarPubMed
Spray, D.C. and Iacobas, D.A. (2007) Organizational principles of the connexin-related brain transcriptome. Journal of Membrane Biology 218, 39–47.CrossRefGoogle ScholarPubMed
Stevens, B., Porta, S., Haak, L.L., Gallo, V. and Fields, R.D. (2002) Adenosine: a neuron–glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36, 855–868.CrossRefGoogle ScholarPubMed
Trapp, B.D. and Kidd, G.J. (2004) Structure of the myelinated axon. In Lazzarini, R.L. (ed) Myelin Biology and Disorders. Elsevier, San Diego, pp. 3–27.Google Scholar
Veeraraghavalu, K., Choi, S.H., Zhang, X. and Sisodia, S.S. (2010) Presenilin 1 mutants impair the self-renewal and differentiation of adult murine subventricular zone-neuronal progenitors via cell-autonomous mechanisms involving notch signaling. Journal of Neuroscience 30, 6903–6915.CrossRefGoogle ScholarPubMed
White, R., Gonsior, C., Krämer-Albers, E.M., Stöhr, N., Hüttelmaier, S. and Trotter, J. (2008) Activation of oligodendroglial Fyn kinase enhances translation of mRNAs transported in hnRNP A2-dependent RNA granules. Journal of Cell Biology 181, 579–586.CrossRefGoogle ScholarPubMed
Wu, M.C. and Lin, X. (2009) Prior biological knowledge-based approaches for the analysis of genome-wide expression profiles using gene sets and pathways. Statistical Methods in Medical Research 18, 577–593.CrossRefGoogle ScholarPubMed
Yang, J., Jiang, Z., Fitzgerald, D.C., Ma, C., Yu, S., Li, H., Zhao, Z., Li, Y., Ciric, B., Curtis, M., Rostami, A. and Zhang, G.X. (2009) Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis. Journal of Clinical Investigation 119, 3678–3691.CrossRefGoogle ScholarPubMed
Zhang, Y., Taveggia, C., Melendez-Vasquez, C., Einheber, S., Raine, C.S., Salzer, J.L. et al. (2006) Interleukin-11 potentiates oligodendrocyte survival and maturation, and myelin formation. Journal of Neuroscience 26, 12174–12185.CrossRefGoogle ScholarPubMed
Zhang, Y., Argaw, A.T., Gurfein, B.T., Zameer, A., Snyder, B.J., Ge, C. et al. (2009) Notch1 signaling plays a role in regulating precursor differentiation during CNS remyelination. Proceedings of the National Academy of Sciences of the U.S.A. 106, 19162–19167.CrossRefGoogle Scholar
Supplementary material: PDF

Iacobas supplementary material

Supplementary figure 1

Download Iacobas supplementary material(PDF)
PDF 28.9 MB
Supplementary material: PDF

Iacobas supplementary material

Supplementary figure 2

Download Iacobas supplementary material(PDF)
PDF 824.1 KB