A screen for hoxb1-regulated genes identifies ppp1r14al as a regulator of the rhombomere 4 Fgf-signaling center

Developmental Biology

Volumn 358, Issue 2, 2011, Pages 356-367

  Choe, Seong Kyu ^a   Zhang, Xiaolan ^a   Hirsch, Nicolas ^a   Straubhaar, Juerg ^a   Sagerström, Charles G ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Fgf; Hindbrain; Hox; Microarray; Transcription; Zebrafish

Indexed keywords

CELL PROTEIN; CELLULAR RETINOL BINDING PROTEIN 1; EPHRIN; FIBROBLAST GROWTH FACTOR 3; FIBROBLAST GROWTH FACTOR 8; FORKHEAD TRANSCRIPTION FACTOR; GELATINASE A; GROWTH ARREST SPECIFIC PROTEIN 6; HOMEODOMAIN PROTEIN; HOXB1 PROTEIN; JAGGED1; MYELIN PROTEIN; PARALOG GROUP 1 HOX PROTEIN; PROTEIN PHOSPHATASE 1 REGULATROTY 14 AL SUBUNIT PROTEIN; SULFATASE; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSCRIPTION FACTOR AP 2; UNCLASSIFIED DRUG;

ARTICLE; BRAIN DEVELOPMENT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC SCREENING; GENETIC TRANSCRIPTION; HOX GENE; HOXB1B GENE; NEUROMERE; NONHUMAN; NUCLEOTIDE SEQUENCE; PPP1R14AL GENE; PRIORITY JOURNAL; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; UNINDEXED SEQUENCE; UPREGULATION; ZEBRA FISH;

DANIO RERIO; VERTEBRATA;

EID: 80053094384     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.05.676     Document Type: Article

References (64)

1. Akimenko M.A., Ekker M., Wegner J., Lin W., Westerfield M. Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 1994, 14:3475-3486.
2. Alexander T., Nolte C., Krumlauf R. Hox genes and segmentation of the hindbrain and axial skeleton. Annu. Rev. Cell Dev. Biol. 2009, 25:431-456.
3. Alexandre D., Clarke J.D., Oxtoby E., Yan Y.L., Jowett T., Holder N. Ectopic expression of Hoxa-1 in the zebrafish alters the fate of the mandibular arch neural crest and phenocopies a retinoic acid-induced phenotype. Development 1996, 122:735-746.
4. Amores A., Force A., Yan Y.L., Joly L., Amemiya C., Fritz A., Ho R.K., Langeland J., Prince V., Wang Y.L., Westerfield M., Ekker M., Postlethwait J.H. Zebrafish hox clusters and vertebrate genome evolution. Science 1998, 282:1711-1714.
5. Bosley T.M., Salih M.A., Alorainy I.A., Oystreck D.T., Nester M., Abu-Amero K.K., Tischfield M.A., Engle E.C. Clinical characterization of the HOXA1 syndrome BSAS variant. Neurology 2007, 69:1245-1253.
6. Brown L.A., Amores A., Schilling T.F., Jowett T., Baert J.L., de Launoit Y., Sharrocks A.D. Molecular characterization of the zebrafish PEA3 ETS-domain transcription factor. Oncogene 1998, 17:93-104.
7. Carpenter E.M., Goddard J.M., Chisaka O., Manley N.R., Capecchi M.R. Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development 1993, 118:1063-1075.
8. Choe S.-K., Vlachakis N., Sagerström C.G. Meis family proteins are required for hindbrain development in the zebrafish. Development 2002, 129:585-595.
9. Choe S.-K., Sagerstrom C.G. Paralog group 1 hox genes regulate rhombomere 5/6 expression of vnhf1, a repressor of rostral hindbrain fates, in a meis-dependent manner. Dev. Biol. 2004, 271:350-361.
10. Choe S.K., Lu P., Nakamura M., Lee J., Sagerstrom C.G. Meis cofactors control HDAC and CBP accessibility at Hox-regulated promoters during zebrafish embryogenesis. Dev. Cell 2009, 17:561-567.
11. Cohen P.T. Protein phosphatase 1-targeted in many directions. J. Cell Sci. 2002, 115:241-256.
12. Eto M., Ohmori T., Suzuki M., Furuya K., Morita F. A novel protein phosphatase-1 inhibitory protein potentiated by protein kinase C. Isolation from porcine aorta media and characterization. J. Biochem. 1995, 118:1104-1107.
13. Eto M., Senba S., Morita F., Yazawa M. Molecular cloning of a novel phosphorylation-dependent inhibitory protein of protein phosphatase-1 (CPI17) in smooth muscle: its specific localization in smooth muscle. FEBS Lett. 1997, 410:356-360.
14. Gavalas A., Studer M., Lumsden A., Rijli F.M., Krumlauf R., Chambon P. Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 1998, 125:1123-1136.
15. Gavalas A., Trainor P., Ariza-McNaughton L., Krumlauf R. Synergy between Hoxa1 and Hoxb1: the relationship between arch patterning and the generation of cranial neural crest. Development 2001, 128:3017-3027.
16. Georgijevic S., Subramanian Y., Rollins E.L., Starovic-Subota O., Tang A.C., Childs S.J. Spatiotemporal expression of smooth muscle markers in developing zebrafish gut. Dev. Dyn. 2007, 236:1623-1632.
17. Goddard J.M., Rossel M., Manley N.R., Capecchi M.R. Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VII nerve. Development 1996, 122:3217-3226.
18. Hernandez R.E., Rikhof H.A., Bachmann R., Moens C.B. vhnf1 integrates global RA patterning and local FGF signals to direct posterior hindbrain development in zebrafish. Development 2004, 131:4511-4520.
19. Kiefer P., Strahle U., Dickson C. The zebrafish Fgf-3 gene: cDNA sequence, transcript structure and genomic organization. Gene 1996, 168:211-215.
20. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullman B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
21. Kitta K., Day R.M., Kim Y., Torregroza I., Evans T., Suzuki Y.J. Hepatocyte growth factor induces GATA-4 phosphorylation and cell survival in cardiac muscle cells. J. Biol. Chem. 2003, 278:4705-4712.
22. Krauss S., Johansen T., Korzh V., Fjose A. Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Development 1991, 113:1193-1206.
23. Krumlauf R. Hox genes in vertebrate development. Cell 1994, 78:191-201.
24. Kuraku S., Meyer A. The evolution and maintenance of Hox gene clusters in vertebrates and the teleost-specific genome duplication. Int. J. Dev. Biol. 2009, 53:765-773.
25. Kwak S.J., Phillips B.T., Heck R., Riley B.B. An expanded domain of fgf3 expression in the hindbrain of zebrafish valentino mutants results in mis-patterning of the otic vesicle. Development 2002, 129:5279-5287.
26. Kwak S.J., Vemaraju S., Moorman S.J., Zeddies D., Popper A.N., Riley B.B. Zebrafish pax5 regulates development of the utricular macula and vestibular function. Dev. Dyn. 2006, 235:3026-3038.
27. Lewis E.B. Homeosis: the first 100years. Trends Genet. 1994, 10:341-343.
28. Li Y., Allende M.L., Finkelstein R., Weinberg E.S. Expression of two zebrafish orthodenticle-related genes in the embryonic brain. Mech. Dev. 1994, 48:229-244.
29. Liao J., He J., Yan T., Korzh V., Gong Z. A class of neuroD-related basic helix-loop-helix transcription factors expressed in developing central nervous system in zebrafish. DNA Cell Biol. 1999, 18:333-344.
30. Maconochie M.K., Nonchev S., Studer M., Chan S.K., Popperl H., Sham M.H., Mann R.S., Krumlauf R. Cross-regulation in the mouse HoxB complex: the expression of Hoxb2 in rhombomere 4 is regulated by Hoxb1. Genes Dev. 1997, 11:1885-1895.
31. Makki N., Capecchi M.R. Hoxa1 lineage tracing indicates a direct role for Hoxa1 in the development of the inner ear, the heart, and the third rhombomere. Dev. Biol. 2010, 341:499-509.
32. Mark M., Lufkin T., Vonesch J.L., Ruberte E., Olivo J.C., Dolle P., Gorry P., Lumsden A., Chambon P. Two rhombomeres are altered in Hoxa-1 mutant mice. Development 1993, 119:319-338.
33. Maroon H., Walshe J., Mahmood R., Kiefer P., Dickson C., Mason I. Fgf3 and Fgf8 are required together for formation of the otic placode and vesicle. Development 2002, 129:2099-2108.
34. Maves L., Jackman W., Kimmel C.B. FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development 2002, 129:3825-3837.
35. McClintock J.M., Carlson R., Mann D.M., Prince V.E. Consequences of Hox gene duplication in the vertebrates: an investigation of the zebrafish Hox paralogue group 1 genes. Development 2001, 128:2471-2484.
36. McClintock J.M., Kheirbek M.A., Prince V.E. Knockdown of duplicated zebrafish hoxb1 genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention. Development 2002, 129:2339-2354.
37. Mechta-Grigoriou F., Garel S., Charnay P. Nab proteins mediate a negative feedback loop controlling Krox-20 activity in the developing hindbrain. Development 2000, 127:119-128.
38. Moens C.B., Cordes S.P., Giorgianni M.W., Barsh G.S., Kimmel C.B. Equivalence in the genetic control of hindbrain segmentation in fish and mouse. Development 1998, 125:381-391.
39. Moens C.B., Yan Y.-L., Appel B., Force A.G., Kimmel C.B. valentino: a zebrafish gene required for normal hindbrain segmentation. Development 1996, 122:3981-3990.
40. Murakami A., Thurlow J., Dickson C. Retinoic acid-regulated expression of fibroblast growth factor 3 requires the interaction between a novel transcription factor and GATA-4. J. Biol. Chem. 1999, 274:17242-17248.
41. Oxtoby E., Jowett T. Cloning of the zebrafish krox-20 gene (krx20) and its expression during development. Nucleic Acids Res. 1993, 21:1087-1095.
42. Phillips B.T., Bolding K., Riley B.B. Zebrafish fgf3 and fgf8 encode redundant functions required for otic placode induction. Dev. Biol. 2001, 235:351-365.
43. Popperl H., Bienz M., Studer M., Chan S.K., Aparicio S., Brenner S., Mann R.S., Krumlauf R. Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 1995, 81:1031-1042.
44. Prince V.E., Moens C.B., Kimmel C.B., Ho R.K. Zebrafish hox genes: expression in the hindbrain region of wild-type and mutants of the segmentation gene valentino. Development 1998, 125:393-406.
45. Raible F., Brand M. Tight transcriptional control of the ETS domain factors Erm and Pea3 by Fgf signaling during early zebrafish development. Mech. Dev. 2001, 107:105-117.
46. Rohrschneider M.R., Elsen G.E., Prince V.E. Zebrafish Hoxb1a regulates multiple downstream genes including prickle1b. Dev. Biol. 2007, 309:358-372.
47. Rossel M., Capecchi M.R. Mice mutant for both Hoxa1 and Hoxb1 show extensive remodeling of the hindbrain and defects in craniofacial development. Development 1999, 126:5027-5040.
48. Studer M., Gavalas A., Marshall H., Ariza-McNaughton L., Rijli F.M., Chambon P., Krumlauf R. Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 1998, 125:1025-1036.
49. Studer M., Lumsden A., Ariza-McNaughton L., Bradley A., Krumlauf R. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 1996, 384:630-634.
50. Sun Z., Hopkins N. vhnf1, the MODY5 and familial GCKD-associated gene, regulates regional specification of the zebrafish gut, pronephros, and hindbrain. Genes Dev. 2001, 15:3217-3229.
51. Tischfield M.A., Bosley T.M., Salih M.A., Alorainy I.A., Sener E.C., Nester M.J., Oystreck D.T., Chan W.M., Andrews C., Erickson R.P., Engle E.C. Homozygous HOXA1 mutations disrupt human brainstem, inner ear, cardiovascular and cognitive development. Nat. Genet. 2005, 37:1035-1037.
52. Tumpel S., Cambronero F., Ferretti E., Blasi F., Wiedemann L.M., Krumlauf R. Expression of Hoxa2 in rhombomere 4 is regulated by a conserved cross-regulatory mechanism dependent upon Hoxb1. Dev. Biol. 2007, 302:646-660.
53. van den Akker W.M., Durston A.J., Spaink H.P. Identification of hoxb1b downstream genes: hoxb1b as a regulatory factor controlling transcriptional networks and cell movement during zebrafish gastrulation. Int. J. Dev. Biol. 2010, 54:55-62.
54. Vlachakis N., Choe S.-K., Sagerström C.G. Meis3 synergizes with Pbx4 and Hoxb1b in promoting hindbrain fates in the zebrafish. Development 2001, 128:1299-1312.
55. Vlachakis N., Ellstrom D.R., Sagerström C.G. A novel pbx family member expressed during early zebrafish embryogenesis forms trimeric complexes with Meis3 and Hoxb1b. Dev. Dyn. 2000, 217:109-119.
56. Walshe J., Maroon H., McGonnell I.M., Dickson C., Mason I. Establishment of Hindbrain Segmental Identity Requires Signaling by FGF3 and FGF8. Curr. Biol. 2002, 12:1117-1123.
57. Walshe J., Mason I. Unique and combinatorial functions of Fgf3 and Fgf8 during zebrafish forebrain development. Development 2003, 130:4337-4349.
58. Wang X., Emelyanov A., Sleptsova-Friedrich I., Korzh V., Gong Z. Expression of two novel zebrafish iroquois homologues (ziro1 and ziro5) during early development of axial structures and central nervous system. Mech. Dev. 2001, 105:191-195.
59. Waskiewicz A.J., Rikhof H.A., Hernandez R.E., Moens C.B. Zebrafish Meis functions to stabilize Pbx proteins and regulate hindbrain patterning. Development 2001, 128:4139-4151.
60. Waskiewicz A.J., Rikhof H.A., Moens C.B. Eliminating zebrafish pbx proteins reveals a hindbrain ground state. Dev. Cell 2002, 3:723-733.
61. Wassef M.A., Chomette D., Pouilhe M., Stedman A., Havis E., Desmarquet-Trin Dinh C., Schneider-Maunoury S., Gilardi-Hebenstreit P., Charnay P., Ghislain J. Rostral hindbrain patterning involves the direct activation of a Krox20 transcriptional enhancer by Hox/Pbx and Meis factors. Development 2008, 135:3369-3378.
62. Whitehead G.G., Makino S., Lien C.L., Keating M.T. fgf20 is essential for initiating zebrafish fin regeneration. Science 2005, 310:1957-1960.
63. Wiellette E.L., Sive H. vhnf1 and Fgf signals synergize to specify rhombomere identity in the zebrafish hindbrain. Development 2003, 130:3821-3829.
64. Xu Q., Holder N., Patient R., Wilson S.W. Spatially regulated expression of three receptor tyrosine kinase genes during gastrulation in the zebrafish. Development 1994, 120:287-299.