Identification of neural crest and glial enhancers at the mouse Sox10 locus through transgenesis in zebrafish

PLoS Genetics

Volumn 4, Issue 9, 2008, Pages

  Antonellis, Anthony ^a   Huynh, Jimmy L ^b   Lee Lin, Shih Queen ^a   Vinton, Ryan M ^b   Renaud, Gabriel ^a   Loftus, Stacie K ^a   Elliot, Gene ^a   Wolfsberg, Tyra G ^a   Green, Eric D ^a   McCallion, Andrew S ^b   Pavan, William J ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CIS REGULATORY ELEMENT; ENHANCER REGION; GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE LOCUS; GENE SEQUENCE; GENOME; GLIA CELL; MELANOCYTE; MOUSE; NEURAL CREST CELL; NONHUMAN; REGULATORY SEQUENCE; REPORTER GENE; SCHWANN CELL; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SOX10 GENE; TRANSGENIC ANIMAL; TRANSGENICS; TRANSPOSON; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; CELL STRAIN 3T3; CYTOLOGY; GENE TRANSFER; GENETICS; GLIA; METABOLISM; NEURAL CREST; NUCLEOTIDE SEQUENCE; TRANSGENIC MOUSE;

DANIO RERIO; MAMMALIA; MUS; MUS MUSCULUS;

DNA BINDING PROTEIN; HIGH MOBILITY GROUP PROTEIN; SOX-10 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX10;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BINDING SITES; CONSERVED SEQUENCE; DNA-BINDING PROTEINS; EMBRYO, NONMAMMALIAN; ENHANCER ELEMENTS (GENETICS); GENE TRANSFER TECHNIQUES; GENOME; HIGH MOBILITY GROUP PROTEINS; MELANOCYTES; MICE; MICE, TRANSGENIC; NEURAL CREST; NEUROGLIA; NIH 3T3 CELLS; SCHWANN CELLS; TRANSCRIPTION FACTORS; ZEBRAFISH;

EID: 52949123269     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000174     Document Type: Article

References (41)

1. Kalcheim C, Le Douarin NM (1986) Requirement of a neural tube signal for the differentiation of neural crest cells into dorsal root ganglia. Dev Biol 116: 451-466.
2. Bondurand N, Kobetz A, Pingault V, Lemort N, Encha-Razavi F, et al. (1998) Expression of the SOX10 gene during human development. FEBS Lett 432: 168-172.
3. Pusch C, Hustert E, Pfeifer D, Sudbeck P, Kist R, et al. (1998) The SOX10/Sox10 gene from human and mouse: sequence, expression, and transactivation by the encoded HMG domain transcription factor. Hum Genet 103: 115-123.
4. Herbarth B, Pingault V, Bondurand N, Kuhlbrodt K, Hermans-Borgmeyer I, et al. (1998) Mutation of the Sry-related Sox10 gene in Dominant megacolon, a mouse model for human Hirschsprung disease. Proc Natl Acad Sci U S A 95: 5161-5165.
5. Kapur RP (1999) Early death of neural crest cells is responsible for total enteric aganglionosis in Sox10(Dom)/Sox10(Dom) mouse embryos. Pediatr Dev Pathol 2: 559-569.
6. Kuhlbrodt K, Herbarth B, Sock E, Hermans-Borgmeyer I, Wegner M (1998) Sox10, a novel transcriptional modulator in glial cells. J Neurosci 18: 237-250.
7. Paratore C, Goerich DE, Suter U, Wegner M, Sommer L (2001) Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128: 3949-3961.
8. Southard-Smith EM, Kos L, Pavan WJ (1998) Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model. Nat Genet 18: 60-64.
9. Mollaaghababa R, Pavan WJ (2003) The importance of having your SOX on: role of SOX10 in the development of neural crest-derived melanocytes and glia. Oncogene 22: 3024-3034.
10. Stolt CC, Rehberg S, Ader M, Lommes P, Riethmacher D, et al. (2002) Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev 16: 165-170.
11. Inoue K, Khajavi M, Ohyama T, Hirabayashi S, Wilson J, et al. (2004) Molecular mechanism for distinct neurological phenotypes conveyed by allelic truncating mutations. Nat Genet 36: 361-369.
12. Kuhlbrodt K, Schmidt C, Sock E, Pingault V, Bondurand N, et al. (1998) Functional analysis of Sox10 mutations found in human Waardenburg-Hirschsprung patients. J Biol Chem 273: 23033-23038.
13. Pingault V, Bondurand N, Kuhlbrodt K, Goerich DE, Prehu MO, et al. (1998) SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat Genet 18: 171-173.
14. Shah KN, Dalal SJ, Desai MP, Sheth PN, Joshi NC, et al. (1981) White forelock, pigmentary disorder of irides, and long segment Hirschsprung disease: possible variant of Waardenburg syndrome. J Pediatr 99: 432-435.
15. Inoue K, Tanabe Y, Lupski JR (1999) Myelin deficiencies in both the central and the peripheral nervous systems associated with a SOX10 mutation. Ann Neurol 46: 313-318.
16. Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, et al. (2001) Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128: 4113-4125.
17. Kelsh RN, Eisen JS (2000) The zebrafish colourless gene regulates development of non-ectomesenchymal neural crest derivatives. Development 127: 515-525.
18. Britsch S, Goerich DE, Riethmacher D, Peirano RI, Rossner M, et al. (2001) The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 15: 66-78.
19. Antonellis A, Bennett WR, Menheniott TR, Prasad AB, Lee-Lin SQ, et al. (2006) Deletion of long-range sequences at Sox10 compromises developmental expression in a mouse model of Waardenburg-Shah (WS4) syndrome. Hum Mol Genet 15: 259-271.
20. Frazer KA, Elnitski L, Church DM, Dubchak I, Hardison RC (2003) Cross-species sequence comparisons: a review of methods and available resources. Genome Res 13: 1-12.
21. Nardone J, Lee DU, Ansel KM, Rao A (2004) Bioinformatics for the 'bench biologist': how to find regulatory regions in genomic DNA. Nat Immunol 5: 768-774.
22. Wasserman WW, Palumbo M, Thompson W, Fickett JW, Lawrence CE (2000) Human-mouse genome comparisons to locate regulatory sites. Nat Genet 26: 225-228.
23. Carney TJ, Dutton KA, Greenhill E, Delfino-Machin M, Dufourcq P, et al. (2006) A direct role for Sox10 in specification of neural crest-derived sensory neurons. Development 133: 4619-4630.
24. Sonnenberg-Riethmacher E, Miehe M, Stolt CC, Goerich DE, Wegner M, et al. (2001) Development and degeneration of dorsal root ganglia in the absence of the HMG-domain transcription factor Sox10. Mech Dev 109: 253-265.
25. Peirano RI, Wegner M (2000) The glial transcription factor Sox10 binds to DNA both as monomer and dimer with different functional consequences. Nucleic Acids Res 28: 3047-3055.
26. Cheung M, Briscoe J (2003) Neural crest development is regulated by the transcription factor Sox9. Development 130: 5681-5693.
27. Fisher S, Grice EA, Vinton RM, Bessling SL, McCallion AS (2006) Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science 312: 276-279.
28. LeBlanc SE, Jang SW, Ward RM, Wrabetz L, Svaren J (2006) Direct regulation of myelin protein zero expression by the Egr2 transactivator. J Biol Chem 281: 5453-5460.
29. Deal KK, Cantrell VA, Chandler RL, Saunders TL, Mortlock DP, et al. (2006) Distant regulatory elements in a Sox10-beta GEO BAC transgene are required for expression of Sox10 in the enteric nervous system and other neural crestderived tissues. Dev Dyn 235: 1413-1432.
30. Werner T, Hammer A, Wahlbuhl M, Bosl MR, Wegner M (2007) Multiple conserved regulatory elements with overlapping functions determine Sox10 expression in mouse embryogenesis. Nucleic Acids Res 35: 6526-6538.
31. Abbasi AA, Paparidis Z, Malik S, Goode DK, Callaway H, et al. (2007) Human GLI3 intragenic conserved non-coding sequences are tissue-specific enhancers. PLoS ONE 2: e366.
32. Ahituv N, Zhu Y, Visel A, Holt A, Afzal V, et al. (2007) Deletion of ultraconserved elements yields viable mice. PLoS Biol 5: e234.
33. de la Calle-Mustienes E, Feijoo CG, Manzanares M, Tena JJ, Rodriguez-Seguel E, et al. (2005) A functional survey of the enhancer activity of conserved non-coding sequences from vertebrate Iroquois cluster gene deserts. Genome Res 15: 1061-1072.
34. McGaughey DM, Vinton RM, Huynh J, Al-Saif A, Beer MA, et al. (2008) Metrics of sequence constraint overlook regulatory sequences in an exhaustive analysis at phox2b. Genome Res 18: 252-260.
35. Nobrega MA, Ovcharenko I, Afzal V, Rubin EM (2003) Scanning human gene deserts for long-range enhancers. Science 302: 413.
36. Sviderskaya EV, Hill SP, Evans-Whipp TJ, Chin L, Orlow SJ, et al. (2002) p16(Ink4a) in melanocyte senescence and differentiation. J Natl Cancer Inst 94: 446-454.
37. Toda K, Small JA, Goda S, Quarles RH (1994) Biochemical and cellular properties of three immortalized Schwann cell lines expressing different levels of the myelin-associated glycoprotein. J Neurochem 63: 1646-1657.
38. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
39. Westerfield M (2000) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). Eugene: University of Oregon Press.
40. Fisher S, Grice EA, Vinton RM, Bessling SL, Urasaki A, et al. (2006) Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat Protoc 1: 1297-1305.
41. Hogan B, Constantini F, Lacy E (1986) Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Press.