Targeted germ line disruptions reveal general and species-specific roles for paralog group 1 hox genes in zebrafish

BMC Developmental Biology

Volumn 14, Issue 1, 2014, Pages

  Weicksel, Steven E ^a   Gupta, Ankit ^a   Zannino, Denise A ^a   Wolfe, Scot A ^a   Sagerström, Charles G ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Gene expression; Hindbrain; Nucleosome positioning; Retinoic acid signaling; TALEN nuclease; Zinc finger nuclease

Indexed keywords

HOMEOBOX A1 PROTEIN; HOMEODOMAIN PROTEIN; HOXB1 HOMEODOMAIN PROTEIN; RETINOIC ACID; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; ARTICLE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; GERMLINE MUTATION; KNOCKOUT MOUSE; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; MOUSE; NERVE CELL; NUCLEOSOME; PRENATAL DEVELOPMENT; RHOMBENCEPHALON; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; GERM-LINE MUTATION; HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; NEURONS; NUCLEOSOMES; RHOMBENCEPHALON; TRANSCRIPTION FACTORS; TRETINOIN; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84903175492     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-14-25     Document Type: Article

References (69)

1. Homeobox genes and axial patterning. McGinnis W, Krumlauf R, Cell 1992 68 2 283 302 10.1016/0092-8674(92)90471-N 1346368
2. The Caenorhabditis elegans homeobox gene cluster. Burglin TR, Ruvkun G, Curr Opin Genet Dev 1993 3 4 615 620 10.1016/0959-437X(93)90097-9 7902148
3. A gene complex controlling segmentation in Drosophila. Lewis EB, Nature 1978 276 5688 565 570 10.1038/276565a0 103000
4. Zebrafish hox clusters and vertebrate genome evolution. Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH, Science 1998 282 5394 1711 1714 9831563
5. The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. Duboule D, Dolle P, EMBO J 1989 8 5 1497 1505 2569969
6. Organizing axes in time and space; 25 years of colinear tinkering. Kmita M, Duboule D, Science 2003 301 5631 331 333 10.1126/science.1085753 12869751
7. Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Simeone A, Acampora D, Arcioni L, Andrews PW, Boncinelli E, Mavilio F, Nature 1990 346 6286 763 766 10.1038/346763a0 1975088
8. Hindbrain patterning involves graded responses to retinoic acid signalling. Dupe V, Lumsden A, Development 2001 128 12 2199 2208 11493540
9. Enhancement of HL-60 differentiation by a new class of retinoids with selective activity on retinoid X receptor. Apfel CM, Kamber M, Klaus M, Mohr P, Keidel S, LeMotte PK, J Biol Chem 1995 270 51 30765 30772 10.1074/jbc.270.51. 30765 8530518
10. Molecular determinants of nuclear receptor-corepressor interaction. Perissi V, Staszewski LM, McInerney EM, Kurokawa R, Krones A, Rose DW, Lambert MH, Milburn MV, Glass CK, Rosenfeld MG, Genes Dev 1999 13 24 3198 3208 10.1101/gad.13.24.3198 10617569
11. Synergistic activation of retinoic acid (RA)-responsive genes and induction of embryonal carcinoma cell differentiation by an RA receptor alpha (RAR alpha)-, RAR beta-, or RAR gamma-selective ligand in combination with a retinoid X receptor-specific ligand. Roy B, Taneja R, Chambon P, Mol Cell Biol 1995 15 12 6481 6487 8524212
12. Nuclear re-organisation of the Hoxb complex during mouse embryonic development. Chambeyron S, Da Silva NR, Lawson KA, Bickmore WA, Development 2005 132 9 2215 2223 10.1242/dev.01813 15829525
13. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Chambeyron S, Bickmore WA, Genes Dev 2004 18 10 1119 1130 10.1101/gad.292104 15155579
14. Nuclear reorganisation and chromatin decondensation are conserved, but distinct, mechanisms linked to Hox gene activation. Morey C, Da Silva NR, Perry P, Bickmore WA, Development 2007 134 5 909 919 10.1242/dev.02779 17251268
15. Hox genes in vertebrate development. Krumlauf R, Cell 1994 78 191 201 10.1016/0092-8674(94)90290-9 7913880
16. Hox genes and segmentation of the vertebrate hindbrain. Tumpel S, Wiedemann LM, Krumlauf R, Curr Top Dev Biol 2009 88 103 137 19651303
17. Equivalence in the genetic control of hindbrain segmentation in fish and mouse. Moens CB, Cordes SP, Giorgianni MW, Barsh GS, Kimmel CB, Development 1998 125 3 381 391 9425134
18. Expression of the mouse labial-like homeobox-containing genes, Hox 2.9 and Hox 1.6, during segmentation of the hindbrain. Murphy P, Hill RE, Development 1991 111 1 61 74 1673098
19. Segment-specific expression of a homoeobox-containing gene in the mouse hindbrain. Murphy P, Davidson DR, Hill RE, Nature 1989 341 6238 156 159 10.1038/341156a0 2571087
20. Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression. Lufkin T, Dierich A, LeMeur M, Mark M, Chambon P, Cell 1991 66 6 1105 1119 10.1016/0092-8674(91)90034-V 1680563
21. Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Carpenter EM, Goddard JM, Chisaka O, Manley NR, Capecchi MR, Development 1993 118 4 1063 1075 7903632
22. Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Chisaka O, Musci TS, Capecchi MR, Nature 1992 355 6360 516 520 10.1038/355516a0 1346922
23. Mice mutant for both Hoxa1 and Hoxb1 show extensive remodeling of the hindbrain and defects in craniofacial development. Rossel M, Capecchi MR, Development 1999 126 22 5027 5040 10529420
24. Two rhombomeres are altered in Hoxa-1 mutant mice. Mark M, Lufkin T, Vonesch JL, Ruberte E, Olivo JC, Dolle P, Gorry P, Lumsden A, Chambon P, Development 1993 119 2 319 338 8287791
25. In vivo functional analysis of the Hoxa-1 3' retinoic acid response element (3'RARE). Dupe V, Davenne M, Brocard J, Dolle P, Mark M, Dierich A, Chambon P, Rijli FM, Development 1997 124 2 399 410 9053316
26. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Studer M, Lumsden A, Ariza-McNaughton L, Bradley A, Krumlauf R, Nature 1996 384 6610 630 634 10.1038/384630a0 8967950
27. Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. Goddard JM, Rossel M, Manley NR, Capecchi MR, Development 1996 122 10 3217 3228 8898234
28. Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Gavalas A, Studer M, Lumsden A, Rijli FM, Krumlauf R, Chambon P, Development 1998 125 6 1123 1136 9463359
29. Knockdown of duplicated zebrafish hoxb1 genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention. McClintock JM, Kheirbek MA, Prince VE, Development 2002 129 10 2339 2354 11973267
30. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Meng X, Noyes MB, Zhu LJ, Lawson ND, Wolfe SA, Nat Biotechnol 2008 26 6 695 701 10.1038/nbt1398 18500337
31. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF, Nucleic Acids Res 2011 39 12 82 10.1093/nar/gkr218 21493687
32. Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Szczepek M, Brondani V, Buchel J, Serrano L, Segal DJ, Cathomen T, Nat Biotechnol 2007 25 7 786 793 10.1038/nbt1317 17603476
33. An improved zinc-finger nuclease architecture for highly specific genome editing. Miller JC, Holmes MC, Wang J, Guschin DY, Lee YL, Rupniewski I, Beausejour CM, Waite AJ, Wang NS, Kim KA, Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH, Nat Biotechnol 2007 25 7 778 785 10.1038/nbt1319 17603475
34. Expanding or restricting the target site repertoire of zinc-finger nucleases: the inter-domain linker as a major determinant of target site selectivity. Handel EM, Alwin S, Cathomen T, Mol Ther 2009 17 1 104 111 10.1038/mt.2008.233 19002164
35. Evaluation and application of modularly assembled zinc-finger nucleases in zebrafish. Zhu C, Smith T, McNulty J, Rayla AL, Lakshmanan A, Siekmann AF, Buffardi M, Meng X, Shin J, Padmanabhan A, Zhu C, Smith T, McNulty J, Rayla AL, Lakshmanan A, Siekmann AF, Buffardi M, Meng X, Shin J, Padmanabhan A, Cifuentes D, Giraldez AJ, Look AT, Epstein JA, Lawson ND, Wolfe SA, Development 2011 138 20 4555 4564 10.1242/dev.066779 21937602
36. Zinc finger protein-dependent and -independent contributions to the in vivo off-target activity of zinc finger nucleases. Gupta A, Meng X, Zhu LJ, Lawson ND, Wolfe SA, Nucleic Acids Res 2011 39 1 381 392 10.1093/nar/gkq787 20843781
37. An online bioinformatics tool predicts zinc finger and TALE nuclease off-target cleavage. Fine EJ, Cradick TJ, Zhao CL, Lin Y, Bao G, Nucleic Acids Res 2014 42 6 42 10.1093/nar/gkt1326 24381193
38. Consequences of Hox gene duplication in the vertebrates: an investigation of the zebrafish Hox paralogue group 1 genes. McClintock JM, Carlson R, Mann DM, Prince VE, Development 2001 128 13 2471 2484 11493564
39. The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Begemann G, Schilling TF, Rauch GJ, Geisler R, Ingham PW, Development 2001 128 16 3081 3094 11688558
40. Key roles of retinoic acid receptors alpha and beta in the patterning of the caudal hindbrain, pharyngeal arches and otocyst in the mouse. Dupe V, Ghyselinck NB, Wendling O, Chambon P, Mark M, Development 1999 126 22 5051 5059 10529422
41. Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Niederreither K, Vermot J, Schuhbaur B, Chambon P, Dolle P, Development 2000 127 1 75 85 10654602
42. Direct crossregulation between retinoic acid receptor {beta} and Hox genes during hindbrain segmentation. Serpente P, Tumpel S, Ghyselinck NB, Niederreither K, Wiedemann LM, Dolle P, Chambon P, Krumlauf R, Gould AP, Development 2005 132 3 503 513 10.1242/dev.01593 15634700
43. Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Studer M, Gavalas A, Marshall H, Ariza-McNaughton L, Rijli FM, Chambon P, Krumlauf R, Development 1998 125 6 1025 1036 9463349
44. Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Kudoh T, Wilson SW, Dawid IB, Development 2002 129 18 4335 4346 12183385
45. An early Fgf signal required for gene expression in the zebrafish hindbrain primordium. Roy NM, Sagerstrom CG, Brain Res Dev Brain Res 2004 148 1 27 42 10.1016/j.devbrainres.2003.10.005 14757516
46. Dynamic nucleosome organization at hox promoters during zebrafish embryogenesis. Weicksel SE, Xu J, Sagerstrom CG, PLoS One 2013 8 5 63175 10.1371/journal.pone.0063175 23671670
47. Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Sekinger EA, Moqtaderi Z, Struhl K, Mol Cell 2005 18 6 735 748 10.1016/j.molcel.2005.05. 003 15949447
48. TALE factors poise promoters for activation by Hox proteins. Choe SK, Ladam F, Sagerstrom C, Dev Cell 2014 28 2 203 211 10.1016/j.devcel.2013.12.011 24480644
49. Hoxb1b controls oriented cell division, cell shape and microtubule dynamics in neural tube morphogenesis. Zigman M, Laumann-Lipp N, Titus T, Postlethwait J, Moens CB, Development 2014 141 3 639 649 10.1242/dev.098731 24449840
50. Meis3 synergizes with Pbx4 and Hoxb1b in promoting hindbrain fates in the zebrafish. Vlachakis N, Choe SK, Sagerstrom CG, Development 2001 128 8 1299 1312 11262231
51. Zebrafish Meis functions to stabilize Pbx proteins and regulate hindbrain patterning. Waskiewicz AJ, Rikhof HA, Hernandez RE, Moens CB, Development 2001 128 21 4139 4151 11684652
52. Eliminating zebrafish pbx proteins reveals a hindbrain ground state. Waskiewicz AJ, Rikhof HA, Moens CB, Dev Cell 2002 3 5 723 733 10.1016/S1534-5807(02)00319-2 12431378
53. Lazarus is a novel pbx gene that globally mediates hox gene function in zebrafish. Popperl H, Rikhof H, Chang H, Haffter P, Kimmel CB, Moens CB, Mol Cell 2000 6 2 255 267 10.1016/S1097-2765(00)00027-7 10983974
54. Meis cofactors control HDAC and CBP accessibility at Hox-regulated promoters during zebrafish embryogenesis. Choe SK, Lu P, Nakamura M, Lee J, Sagerstrom CG, Dev Cell 2009 17 4 561 567 10.1016/j.devcel.2009.08.007 19853569
55. Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Popperl H, Bienz M, Studer M, Chan SK, Aparicio S, Brenner S, Mann RS, Krumlauf R, Cell 1995 81 7 1031 1042 10.1016/S0092-8674(05)80008-X 7600572
56. Trimeric association of Hox and TALE homeodomain proteins mediates Hoxb2 hindbrain enhancer activity. Jacobs Y, Schnabel CA, Cleary ML, Mol Cell Biol 1999 19 7 5134 5142 10373562
57. A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Marshall H, Studer M, Popperl H, Aparicio S, Kuroiwa A, Brenner S, Krumlauf R, Nature 1994 370 6490 567 571 10.1038/370567a0 7914354
58. Retinoic acid-dependent establishment of positional information in the hindbrain was conserved during vertebrate evolution. Ishioka A, Jindo T, Kawanabe T, Hatta K, Parvin MS, Nikaido M, Kuroyanagi Y, Takeda H, Yamasu K, Dev Biol 2011 350 1 154 168 10.1016/j.ydbio.2010.10.011 20969843
59. Stages of embryonic development of the zebrafish. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, Dev Dyn 1995 203 3 253 310 10.1002/aja.1002030302 8589427
60. Construction and application of site-specific artificial nucleases for targeted gene editing. Kok FO, Gupta A, Lawson ND, Wolfe SA, Methods Mol Biol 2014 1101 267 303 10.1007/978-1-62703-721-1-13 24233786
61. Westerfield M, The Zebrafish Book Eugene, OR: University of Oregon Press 1993
62. A novel pbx family member expressed during early zebrafish embryogenesis forms trimeric complexes with Meis3 and Hoxb1b. Vlachakis N, Ellstrom DR, Sagerstrom CG, Dev Dyn 2000 217 1 109 119 10.1002/(SICI)1097-0177(200001)217: 1<109::AID-DVDY10>3.0.CO;2-8 10679934
63. Hox gene expression reveals regionalization along the anteroposterior axis of the zebrafish notochord. Prince VE, Price AL, Ho RK, Dev Genes Evol 1998 208 9 517 522 10.1007/s004270050210 9799433
64. Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Oxtoby E, Jowett T, Nucleic Acids Res 1993 21 5 1087 1095 10.1093/nar/21.5.1087 8464695
65. Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Krauss S, Johansen T, Korzh V, Fjose A, Development 1991 113 4 1193 1206 1811936
66. The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio). Piotrowski T, Nusslein-Volhard C, Dev Biol 2000 225 2 339 356 10.1006/dbio.2000.9842 10985854
67. The zebrafish Fgf-3 gene: cDNA sequence, transcript structure and genomic organization. Kiefer P, Strahle U, Dickson C, Gene 1996 168 2 211 215 10.1016/0378-1119(95)00736-9 8654946
68. Dynamic and sequential patterning of the zebrafish posterior hindbrain by retinoic acid. Maves L, Kimmel CB, Dev Biol 2005 285 2 593 605 10.1016/j.ydbio.2005.07.015 16102743
69. olig2-Expressing hindbrain cells are required for migrating facial motor neurons. Zannino DA, Sagerstrom CG, Appel B, Dev Dyn 2012 241 2 315 326 10.1002/dvdy.23718 22275004