Schwann cell myelination requires Dynein function

Neural Development

Volumn 7, Issue 1, 2012, Pages

  Langworthy, Melissa M ^a   Appel, Bruce ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Dync1h1; Glia; Myelin; Peripheral nerve; Zebrafish

Indexed keywords

CYCLIC AMP; CYTOPLASMIC DYNEIN; DYNC1H1 PROTEIN, ZEBRAFISH; FORSKOLIN; GREEN FLUORESCENT PROTEIN; MORPHOLINO OLIGONUCLEOTIDE; MYELIN BASIC PROTEIN; RNA; ZEBRAFISH PROTEIN;

ANIMAL; ANIMAL EMBRYO; ARTICLE; CELL DIFFERENTIATION; CELL MOTION; CENTRAL NERVOUS SYSTEM; CYTOLOGY; DEMYELINATING DISEASE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; LARVA; METABOLISM; MUTATION; MYELIN SHEATH; PATHOLOGY; PERIPHERAL NERVE; SCHWANN CELL; TRANSGENIC ANIMAL; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM; CYCLIC AMP; CYTOPLASMIC DYNEINS; DEMYELINATING DISEASES; EMBRYO, NONMAMMALIAN; FORSKOLIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; LARVA; MICROSCOPY, ELECTRON, TRANSMISSION; MORPHOLINOS; MUTATION; MYELIN BASIC PROTEIN; MYELIN SHEATH; PERIPHERAL NERVES; RNA; SCHWANN CELLS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84869185737     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-7-37     Document Type: Article

References (58)

1. De Vos KJ, Grierson AJ, Ackerley S, Miller CC. Role of axonal transport in neurodegenerative diseases. Annu Rev Neurosci 2008, 31:151-173. 10.1146/annurev.neuro.31.061307.090711, 18558852.
2. Weedon MN, Hastings R, Caswell R, Xie W, Paszkiewicz K, Antoniadi T, Williams M, King C, Greenhalgh L, Newbury-Ecob R, Ellard S. Exome sequencing identifies a DYNC1H1 mutation in a large pedigree with dominant axonal Charcot-Marie-Tooth disease. Am J Hum Genet 2011, 89:308-312. 10.1016/j.ajhg.2011.07.002, 3155164, 21820100.
3. Puls I, Jonnakuty C, LaMonte BH, Holzbaur EL, Tokito M, Mann E, Floeter MK, Bidus K, Drayna D, Oh SJ, Brown RH, Ludlow CL, Fischbeck KH. Mutant dynactin in motor neuron disease. Nat Genet 2003, 33:455-456. 10.1038/ng1123, 12627231.
4. Munch C, Sedlmeier R, Meyer T, Homberg V, Sperfeld AD, Kurt A, Prudlo J, Peraus G, Hanemann CO, Stumm G, Ludolph AC. Point mutations of the p150 subunit of dynactin (DCTN1) gene in ALS. Neurology 2004, 63:724-726. 10.1212/01.WNL.0000134608.83927.B1, 15326253.
5. Chen X-J, Levedakou EN, Millen KJ, Wollmann RL, Soliven B, Popko B. Proprioceptive sensory neuropathy in mice with a mutation in the cytoplasmic Dynein heavy chain 1 gene. J Neurosci 2007, 27:14515-14524. 10.1523/JNEUROSCI.4338-07.2007, 18160659.
6. Ilieva HS, Yamanaka K, Malkmus S, Kakinohana O, Yaksh T, Marsala M, Cleveland DW. Mutant dynein (Loa) triggers proprioceptive axon loss that extends survival only in the SOD1 ALS model with highest motor neuron death. Proc Natl Acad Sci USA 2008, 105:12599-12604. 10.1073/pnas.0805422105, 2527957, 18719118.
7. Dupuis L, Fergani A, Braunstein KE, Eschbach J, Holl N, Rene F, Gonzalez De Aguilar J-L, Zoerner B, Schwalenstocker B, Ludolph AC, Loeffler J-P. Mice with a mutation in the dynein heavy chain 1 gene display sensory neuropathy but lack motor neuron disease. Exp Neurol 2009, 215:146-152. 10.1016/j.expneurol.2008.09.019, 18952079.
8. Amsterdam A, Nissen RM, Sun Z, Swindell E, Farrington S, Hopkins N. Submission and curation of data from an insertional mutagenesis screen. ZFIN Direct Data Submission 2005,
9. Insinna C, Baye LM, Amsterdam A, Besharse JC, Link BA. Analysis of a zebrafish dync1h1 mutant reveals multiple functions for cytoplasmic dynein 1 during retinal photoreceptor development. Neural Dev 2010, 5:12. 10.1186/1749-8104-5-12, 2880287, 20412557.
10. Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, Rauch J, Geisler R, Haffter P, Kelsh RN. Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 2001, 128:4113-4125.
11. Kuhlbrodt K, Herbarth B, Sock E, Hermans-Borgmeyer I, Wegner M. Sox10, a novel transcriptional modulator in glial cells. J Neurosci 1998, 18:237-250.
12. Kucenas S, Wang WD, Knapik EW, Appel B. A selective glial barrier at motor axon exit points prevents oligodendrocyte migration from the spinal cord. J Neurosci 2009, 29:15187-15194. 10.1523/JNEUROSCI.4193-09.2009, 2837368, 19955371.
13. Flanagan-Steet H, Fox MA, Meyer D, Sanes JR. Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 2005, 132:4471-4481. 10.1242/dev.02044, 16162647.
14. Jessen KR, Mirsky R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 2005, 6:671-682.
15. Lyons DA, Pogoda HM, Voas MG, Woods IG, Diamond B, Nix R, Arana N, Jacobs J, Talbot WS. erbb3 and erbb2 are essential for schwann cell migration and myelination in zebrafish. Curr Biol 2005, 15:513-524. 10.1016/j.cub.2005.02.030, 15797019.
16. Barrallo-Gimeno A, Holzschuh J, Driever W, Knapik EW. Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development 2004, 131:1463-1477. 10.1242/dev.01033, 14985255.
17. Lister JA, Cooper C, Nguyen K, Modrell M, Grant K, Raible DW. Zebrafish Foxd3 is required for development of a subset of neural crest derivatives. Dev Biol 2006, 290:92-104. 10.1016/j.ydbio.2005.11.014, 16364284.
18. Arroyo EJ, Bermingham JR, Rosenfeld MG, Scherer SS. Promyelinating Schwann cells express Tst-1/SCIP/Oct-6. J Neurosci 1998, 18:7891-7902.
19. Blanchard AD, Sinanan A, Parmantier E, Zwart R, Broos L, Meijer D, Meier C, Jessen KR, Mirsky R. Oct-6 (SCIP/Tst-1) is expressed in Schwann cell precursors, embryonic Schwann cells, and postnatal myelinating Schwann cells: comparison with Oct-1, Krox-20, and Pax-3. J Neurosci Res 1996, 46:630-640. 10.1002/(SICI)1097-4547(19961201)46:5<630::AID-JNR11>3.0.CO;2-0, 8951674.
20. Scherer SS, Wang DY, Kuhn R, Lemke G, Wrabetz L, Kamholz J. Axons regulate Schwann cell expression of the POU transcription factor SCIP. J Neurosci 1994, 14:1930-1942.
21. Zorick TS, Syroid DE, Arroyo E, Scherer SS, Lemke G. The transcription factors SCIP and Krox-20 mark distinct stages and cell fates in Schwann cell differentiation. Mol Cell Neurosci 1996, 8:129-145. 10.1006/mcne.1996.0052, 8954628.
22. Topilko P, Schneider-Maunoury S, Levi G, Baron-Van Evercooren A, Chennoufi AB, Seitanidou T, Babinet C, Charnay P. Krox-20 controls myelination in the peripheral nervous system. Nature 1994, 371:796-799. 10.1038/371796a0, 7935840.
23. Norenberg MD, Rao KVR. The mitochondrial permeability transition in neurologic disease. Neurochem Int 2007, 50:983-997. 10.1016/j.neuint.2007.02.008, 17397969.
24. Morgan L, Jessen KR, Mirsky R. The effects of cAMP on differentiation of cultured Schwann cells: progression from an early phenotype (04+) to a myelin phenotype (P0+, GFAP-, N-CAM-, NGF-receptor-) depends on growth inhibition. J Cell Biol 1991, 112:457-467. 10.1083/jcb.112.3.457, 2288828, 1704008.
25. Cosker KE, Courchesne SL, Segal RA. Action in the axon: generation and transport of signaling endosomes. Curr Opin Neurobiol 2008, 18:270-275. 10.1016/j.conb.2008.08.005, 2693191, 18778772.
26. Allan VJ. Cytoplasmic dynein. Biochem Soc Trans 2011, 39:1169-1178. 10.1042/BST0391169, 21936784.
27. Hunt SD, Stephens DJ. The role of motor proteins in endosomal sorting. Biochem Soc Trans 2011, 39:1179-1184. 10.1042/BST0391179, 21936785.
28. Zweifel LS, Kuruvilla R, Ginty DD. Functions and mechanisms of retrograde neurotrophin signalling. Nat Rev Neurosci 2005, 6:615-625. 10.1038/nrn1727, 16062170.
29. Wu C, Cui B, He L, Chen L, Mobley WC. The coming of age of axonal neurotrophin signaling endosomes. J Proteomics 2009, 72:46-55. 10.1016/j.jprot.2008.10.007, 2677075, 19028611.
30. Howe DG, McCarthy KD. Retroviral inhibition of cAMP-dependent protein kinase inhibits myelination but not Schwann cell mitosis stimulated by interaction with neurons. J Neurosci 2000, 20:3513-3521.
31. Monuki ES, Weinmaster G, Kuhn R, Lemke G. SCIP: a glial POU domain gene regulated by cyclic AMP. Neuron 1989, 3:783-793. 10.1016/0896-6273(89)90247-X, 2561978.
32. Mandemakers W, Zwart R, Jaegle M, Walbeehm E, Visser P, Grosveld F, Meijer D. A distal Schwann cell-specific enhancer mediates axonal regulation of the Oct-6 transcription factor during peripheral nerve development and regeneration. EMBO J 2000, 19:2992-3003. 10.1093/emboj/19.12.2992, 203354, 10856243.
33. Nickols JC, Valentine W, Kanwal S, Carter BD. Activation of the transcription factor NF-kappaB in Schwann cells is required for peripheral myelin formation. Nat Neurosci 2003, 6:161-167. 10.1038/nn995, 12514737.
34. Ghislain J, Charnay P. Control of myelination in Schwann cells: a Krox20 cis-regulatory element integrates Oct6, Brn2 and Sox10 activities. EMBO Rep 2006, 7:52-58. 10.1038/sj.embor.7400573, 1369227, 16311519.
35. Denarier E, Forghani R, Farhadi HF, Dib S, Dionne N, Friedman HC, Lepage P, Hudson TJ, Drouin R, Peterson A. Functional organization of a Schwann cell enhancer. J Neurosci 2005, 25:11210-11217. 10.1523/JNEUROSCI.2596-05.2005, 16319321.
36. Farhadi HF, Lepage P, Forghani R, Friedman HC, Orfali W, Jasmin L, Miller W, Hudson TJ, Peterson AC. A combinatorial network of evolutionarily conserved myelin basic protein regulatory sequences confers distinct glial-specific phenotypes. J Neurosci 2003, 23:10214-10223.
37. Forghani R, Garofalo L, Foran DR, Farhadi HF, Lepage P, Hudson TJ, Tretjakoff I, Valera P, Peterson A. A distal upstream enhancer from the myelin basic protein gene regulates expression in myelin-forming schwann cells. J Neurosci 2001, 21:3780-3787.
38. Jones EA, Jang SW, Mager GM, Chang LW, Srinivasan R, Gokey NG, Ward RM, Nagarajan R, Svaren J. Interactions of Sox10 and Egr2 in myelin gene regulation. Neuron Glia Biol 2007, 3:377-387. 2605513, 18634568.
39. Delcroix JD, Valletta JS, Wu C, Hunt SJ, Kowal AS, Mobley WC. NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron 2003, 39:69-84. 10.1016/S0896-6273(03)00397-0, 12848933.
40. Howe CL, Valletta JS, Rusnak AS, Mobley WC. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 2001, 32:801-814. 10.1016/S0896-6273(01)00526-8, 11738027.
41. Ye H, Kuruvilla R, Zweifel LS, Ginty DD. Evidence in support of signaling endosome-based retrograde survival of sympathetic neurons. Neuron 2003, 39:57-68. 10.1016/S0896-6273(03)00266-6, 12848932.
42. Heerssen HM, Pazyra MF, Segal RA. Dynein motors transport activated Trks to promote survival of target-dependent neurons. Nat Neurosci 2004, 7:596-604. 10.1038/nn1242, 15122257.
43. Cox LJ, Hengst U, Gurskaya NG, Lukyanov KA, Jaffrey SR. Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival. Nat Cell Biol 2008, 10:149-159. 10.1038/ncb1677, 3153364, 18193038.
44. Shrum CK, Defrancisco D, Meffert MK. Stimulated nuclear translocation of NF-kappaB and shuttling differentially depend on dynein and the dynactin complex. Proc Natl Acad Sci USA 2009, 106:2647-2652. 10.1073/pnas.0806677106, 2650318, 19196984.
45. Monk KR, Naylor SG, Glenn TD, Mercurio S, Perlin JR, Dominguez C, Moens CB, Talbot WS. A G protein-coupled receptor is essential for Schwann cells to initiate myelination. Science 2009, 325:1402-1405. 10.1126/science.1173474, 2856697, 19745155.
46. Monk KR, Oshima K, Jörs S, Heller S, Talbot WS. Gpr126 is essential for peripheral nerve development and myelination in mammals. Development 2011, 138:2673-2680. 10.1242/dev.062224, 3109596, 21613327.
47. Calebiro D, Nikolaev VO, Persani L, Lohse MJ. Signaling by internalized G-protein-coupled receptors. Trends Pharmacol Sci 2010, 31:221-228. 10.1016/j.tips.2010.02.002, 20303186.
48. Jalink K, Moolenaar WH. G protein-coupled receptors: the inside story. Bioessays 2010, 32:13-16. 10.1002/bies.200900153, 20020476.
49. Driskell OJ, Mironov A, Allan VJ, Woodman PG. Dynein is required for receptor sorting and the morphogenesis of early endosomes. Nat Cell Biol 2007, 9:11-120.
50. Sorkin A, Goh LK. Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 2009, 315:683-696. 10.1016/j.yexcr.2008.07.029, 19278030.
51. Giri DK, Ali-Seyed M, Li L-Y, Lee D-F, Ling P, Bartholomeusz G, Wang S-C, Hung M-C. Endosomal transport of ErbB-2: mechanism for nuclear entry of the cell surface receptor. Mol Cell Biol 2005, 25:11005-11018. 10.1128/MCB.25.24.11005-11018.2005, 1316946, 16314522.
52. Sato T, Takahoko M, Okamoto H. HuC:Kaede, a useful tool to label neural morphologies in networks in vivo. Genesis 2006, 44:136-142. 10.1002/gene.20196, 16496337.
53. Hauptmann G, Gerster T. Multicolor whole-mount in situ hybridization. Methods Mol Biol 2000, 137:139-148.
54. Brosamle C, Halpern ME. Characterization of myelination in the developing zebrafish. Glia 2002, 39:47-57. 10.1002/glia.10088, 12112375.
55. Oxtoby E, Jowett T. Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res 1993, 21:1087-1095. 10.1093/nar/21.5.1087, 309267, 8464695.
56. Hauptmann G, Soll I, Gerster T. The early embryonic zebrafish forebrain is subdivided into molecularly distinct transverse and longitudinal domains. Brain Res Bull 2002, 57:371-375. 10.1016/S0361-9230(01)00691-8, 11922991.
57. Park HC, Boyce J, Shin J, Appel B. Oligodendrocyte specification in zebrafish requires notch-regulated cyclin-dependent kinase inhibitor function. J Neurosci 2005, 25:6836-6844. 10.1523/JNEUROSCI.0981-05.2005, 16033893.
58. Carmany-Rampey A, Moens CB. Modern mosaic analysis in the zebrafish. Methods 2006, 39:228-238. 10.1016/j.ymeth.2006.02.002, 16829130.