The adhesion GPCR Gpr56 regulates oligodendrocyte development via interactions with Gα12/13 and RhoA

Nature Communications

Volumn 6, Issue , 2015, Pages

  Ackerman, Sarah D ^a   Garcia, Cynthia ^a   Piao, Xianhua ^b   Gutmann, David H ^a   Monk, Kelly R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G ALPHA 12; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 56; PEPTIDES AND PROTEINS; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; GPR56 PROTEIN, MOUSE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA PROTEIN, MOUSE; RHOA PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ADHESION; APOPTOSIS; CYPRINID; GENE EXPRESSION; MOLECULAR ANALYSIS; MUTATION; NERVOUS SYSTEM; PROTEIN; RODENT;

ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL DEATH; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; MOUSE; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; AMINO ACID SEQUENCE; ANIMAL; AXON; C57BL MOUSE; CELL ADHESION; FEMALE; GENE EXPRESSION REGULATION; KNOCKOUT MOUSE; MALE; METABOLISM; MOLECULAR GENETICS; MUTATION; MYELIN SHEATH; NERVE CELL; PHYSIOLOGY; SEQUENCE HOMOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ZEBRA FISH;

DANIO RERIO; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; AXONS; CELL ADHESION; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MONOMERIC GTP-BINDING PROTEINS; MUTATION; MYELIN SHEATH; NEURONS; OLIGODENDROGLIA; RECEPTORS, G-PROTEIN-COUPLED; RHO GTP-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84938760787     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7122     Document Type: Article

References (65)

1. Nave, K. A. & Trapp, B. D. Axon-glial signaling and the glial support of axon function. Annu. Rev. Neurosci. 31, 535-561 (2008).
2. Fünfschilling, U. et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485, 517-522 (2012).
3. Lee, Y. et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487, 443-448 (2012).
4. Snaidero, N. et al. Myelin membrane wrapping of CNS axons by PI(3,4,5)P3-dependent polarized growth at the inner tongue. Cell 156, 277-290 (2014).
5. Runia, T. F., van Pelt-Gravesteijn, E. D. & Hintzen, R. Q. Recent gains in clinical multiple sclerosis research. CNS Neurol. Disord. Drug Targets 11, 497-505 (2012).
6. Colognato, H. & Tzvetanova, I. D. Glia unglued: how signals from the extracellular matrix regulate the development of myelinating glia. Dev. Neurobiol. 71, 924-955 (2011).
7. Chernousov1, M. A., Yu2, W., Chen2, Z., Carey, D. J. & Strickland, S. Regulation of Schwann cell function by the extracellular matrix. Glia 56, 1498-1507 (2008).
8. Liebscher, I., Schöneberg, T. & Prömel, S. Progress in demystification of adhesion G protein-coupled receptors. Biol. Chem. 8, 937-950 (2013).
9. Shin, D., Lin, S. T., Fu, Y. H. & Ptácek, L. J. Very large G protein-coupled receptor 1 regulates myelin-associated glycoprotein via Gas/Gaq-mediated protein kinases A/C. Proc. Natl Acad. Sci. USA 110, 19101-19106 (2013).
10. Monk, K. R. et al. A G protein-coupled receptor is essential for schwann cells to initiate myelination. Science 325, 1402-1405 (2009).
11. Monk, K. R., Oshima, K., Simone, J., Heller, S. & Talbot, W. S. Gpr126 is essential for peripheral nerve development and myelination in mammals. Development 138, 2673-2680 (2011).
12. Glenn, T. D. & Talbot, W. S. Analysis of Gpr126 function defines distinct mechanisms controlling the initiation and maturation of myelin. Development 140, 3167-3175 (2013).
13. Mogha, A. et al. Gpr126 functions in Schwann cells to control differentiation and myelination via G-protein activation. J. Neurosci. 33, 17976-17985 (2013).
14. Prömel, S. et al. The GPS motif is a molecular switch for bimodal activities of adhesion class G protein-couples receptors. Cell Rep. 2, 321-331 (2012).
15. Araç, D. et al. A novel evolutionarily conserved domain of cell-adhesion-GPCRs mediates autoproteolysis. EMBO Mol. Med. 31, 1364-1378 (2012).
16. Paavola, K. J., Stephenson, J. R., Ritter, S. L., Alter, S. P. & Hall, R. A. The N terminus of the adhesion G protein-coupled receptor GPR56 controls receptor signaling activity. J. Biol. Chem. 286, 28914-28921 (2011).
17. Lein, E. S. et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176 (2007).
18. Cahoy, J. D. et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28, 264-278 (2008).
19. Piao, X. et al. G protein-coupled receptor-dependent development of human frontal cortex. Science 303, 2033-2036 (2004).
20. Piao, X. et al. Genotype-phenotype analysis of human frontoparietal polymicrogyria syndromes. Ann. Neurol. 58, 680-687 (2005).
21. Piao, X. et al. An autosomal recessive form of bilateral frontoparietal polymicrogyria maps to chromosome 16q12.2-21. Am. J. Hum. Genet. 70, 1028-1033 (2002).
22. Bahi-Buisson, N. et al. GPR56-related bilateral frontoparietal polymicrogyria: further evidence for an overlap with the cobblestone complex. Brain 133, 3194-3209 (2010)
23. Curr. Biol. 18, 511-512 (2008).
24. Zalc, B., Goujet, D. & Colman, D. The origin of the myelination program in vertebrates. Curr. Biol. 18, R511-R512 (2008).
25. Kirby, B. B. et al. In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat. Neurosci. 9, 1506-1511 (2006).
26. Kucenas, S., Snell, H. & Appel, B. nkx2.2a promotes specification and differentiation of a myelinating subset of oligodendrocyte lineage cells in zebrafish. Neuron Glia Biol. 4, 71-81 (2008).
27. Cermak, T. et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82 (2011).
28. Jin, Z., Luo, R. & Piao, X. GPR56 and its related diseases. Prog. Mol. Biol. Transl Sci. 89, 1-13 (2009).
29. Emery, B. Regulation of oligodendrocyte differentiation and myelination. Science 330, 779-782 (2010).
30. Li, S. et al. GPR56 regulates pial basement membrane integrity and cortical lamination. J. Neurosci. 28, 5817-5826 (2008).
31. Lee, D. Y., Gianino, S. M. & Gutmann, D. H. Innate neural stem cell heterogeneity determines the patterning of glioma formation in children. Cancer Cell 22, 131-138 (2012).
32. Mattan, N. S. et al. Aspartoacylase deficiency affects early postnatal development of oligodendrocytes and myelination. Neurobiol Dis. 40, 432-443 (2010).
33. Mori, S. & Leblond, C. P. Electron microscopic identification of three classes of oligodendrocytes and a preliminary study of their proliferative activity in the corpus callosum of young rats. J. Comp. Neurol. 139, 1-28 (1970).
34. Peters, A., Palay, S. L. & Webster, H. d. The Fine Structure of the Nervous System: Neurons and Their Supporting Cells (Oxford University Press, 1991).
35. Almeida, R. G., Czopka, T., ffrench-Constant, C. & Lyons, D. A. Individual axons regulate the myelinating potential of single oligodendrocytes in vivo. Development 138, 4443-4450 (2011).
36. Iguchi, T. et al. Orphan G Protein-coupled receptor GPR56 regulates neural progenitor cell migration via a Gα12/13 and Rho pathway. J. Biol. Chem. 283, 14469-14478 (2008).
37. Luo, R. et al. G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination. Proc. Natl Acad. Sci. USA 108, 12925-12930 (2011).
38. Liang, X., Draghi, N. A. & Resh, M. D. Signaling from integrins to Fyn to Rho Family GTPases regulates morphologic differentiation of oligodendrocytes. J. Neurosci. 24, 7140-7149 (2004).
39. Lin, F. et al. Gα12/13 regulate epiboly by inhibiting E-cadherin activity and modulating the actin cytoskeleton. J. Cell Biol. 184, 909-921 (2009).
40. Buhl, A. M., Johnson, N. L., Dhanasekaran, N. & Johnson, G. L. G alpha 12 and G alpha 13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J. Biol. Chem. 270, 24631-24634 (1995).
41. Barres, B. A. & Raff, M. C. Control of oligodendrocyte number in the developing rat optic nerve. Neuron 12, 935-942 (1994).
42. Calver, A. R. et al. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 20, 869-882 (1998).
43. Zhu, Q. et al. Genetic evidence that Nkx2.2 and Pdgfra are major determinants of the timing of oligodendrocyte differentiation in the developing CNS. Development 141, 548-555 (2014).
44. Baron, W., Shattil, S. J. & ffrench-Constant, C. The oligodendrocyte mitogen PDGF stimulates proliferation by activation of αvβ3 integrins. EMBO J. 21, 1957-1966 (2002).
45. Baron, W., Colognato, H. & ffrench-Constant, C. Integrin-growth factor interactions as regulators of oligodendroglial development and function. Glia 49, 467-479 (2005).
46. Czopka, T., Ffrench-Constant, C. & Lyons, D. A. Individual oligodendrocytes have only a few hours in which to generate new myelin sheaths in vivo. Dev. Cell. 25, 599-609 (2013).
47. Huang, J. K. et al. Myelin regeneration in multiple sclerosis: targeting endogenous stem cells. Neurotherapeutics 8, 650-658 (2011).
48. Chen, Y. et al. The oligodendrocyte-specific G-protein coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat. Neurosci. 12, 1398-1406 (2009).
49. Xu, L., Begum, S., Hearn, J. D. & Hynes, R. O. GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc. Natl Acad. Sci. USA 103, 9023-9028 (2006).
50. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. & Schilling, T. F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310 (1995).
51. Bernardos, R. L. & Raymond, P. A. GFAP transgenic zebrafish. Gene Expr. Patterns 6, 1007-1013 (2006).
52. Shin, J. et al. Neural cell fate analysis in zebrafish using olig2 BAC transgenics. Methods Cell Sci. 25, 7-14 (2003).
53. Sato, T., Takahoko, M. & Okamoto, H. HuC:Kaede, a useful tool to label neural morphologies in networks in vivo. Genesis 44, 136-142 (2006).
54. Dahlem, T. J. et al. Simple methods for generating and detecting locus- specific mutations induced with TALENs in the zebrafish genome. PLoS Genet. 8, e1002861 (2012).
55. Thisse, C. & Thisse, B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 3, 59-69 (2008).
56. Lyons, D. A. et al. erbb3 and erbb2 are essential for schwann cell migration and myelination in zebrafish. Curr. Biol. 15, 513-524 (2005).
57. Barth, K. A. & Wilson, S. W. Expression of zebrafish nk2.2 is influenced by sonic hedgehog/vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121, 1755-1768 (1995).
58. Shiau, C. E., Monk, K. R., Joo, W. & Talbot, W. S. An anti-inflammatory NOD-like receptor is required for microglia development. Cell Rep. 5, 1342-1352 (2013).
59. Krauss, S., Concordet, J. P. & Ingham, P. W. A functionally conserved homolog of the Drosophila segment polarity gene shh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431-1444 (1993).
60. Concordet, J. P. Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122, 2835-2846 (1996).
61. Lewis, K. E., Concordet, J. P. & Ingham, P. W. Characterisation of a second patched gene in the zebrafish Danio rerio and the differential response of patched genes to hedgehog signalling. Dev. Biol. 208, 14-29 (1999).
62. Czopka, T. & Lyons, D. A. Dissecting mechanisms of myelinated axon formation using zebrafish. Methods Cell Biol. 105, 25-62 (2011).
63. Dasgupta, B. & Gutmann, D. H. Neurofibromin regulates neural stem cell proliferation, survival, and astroglial differentiation in vitro and in vivo. J. Neurosci. 23, 5584-5594 (2005).
64. Jeong, S. J. et al. Characterization of G protein-coupled receptor 56 protein expression in the mouse developing neocortex. J. Comp. Neurol. 520, 2930-2940 (2012).
65. Ng, A. N. Y. et al. Formation of the digestive system in zebrafish: III. Intestinal epithelium morphogenesis. Dev. Biol. 286, 114-135 (2005).