MiR-196 regulates axial patterning and pectoral appendage initiation

Developmental Biology

Volumn 357, Issue 2, 2011, Pages 463-477

  He, Xinjun ^a   Yan, Yi Lin ^a   Eberhart, Johann K ^a   Herpin, Amaury ^b   Wagner, Toni U ^b   Schartl, Manfred ^b   Postlethwait, John H ^a,b  

^a UNIVERSITY OF OREGON   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Axial skeletal patterning; MicroRNA (miRNA); Mir196 (miR 196); Pectoral fin; Pharyngeal arch; Retinoic acid

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA 196; MICRORNA 196A1; MICRORNA 196A2; MICRORNA 196B; MICRORNA 196C; MICRORNA 196D; RETINOIC ACID; RETINOIC ACID RECEPTOR; RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL ANATOMY; ANIMAL TISSUE; ARTICLE; AXIAL SKELETAL PATTERNING; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; GENE CLUSTER; GENE FUNCTION; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; GENETIC REGULATION; HOMEOBOX; HOX GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PECTORAL FIN; PECTORAL FIN BUD; PHARYNX ARCH; PHENOTYPE; PRIORITY JOURNAL; RARAB GENE; RECEPTOR GENE; REPORTER GENE; RIB; ROSTRAL VERTEBRATE; SIGNAL TRANSDUCTION; SKIN APPENDAGE; SOMITE; TISSUE CULTURE; ZEBRA FISH;

DANIO RERIO; VERTEBRATA;

EID: 80052165277     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.07.014     Document Type: Article

References (89)

1. 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.
2. Amores A., Suzuki T., Yan Y.L., Pomeroy J., Singer A., Amemiya C., Postlethwait J.H. Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fish. Genome Res. 2004, 14:1-10.
3. Asli N.S., Kessel M. Spatiotemporally restricted regulation of generic motor neuron programs by miR-196-mediated repression of Hoxb8. Dev. Biol. 2010, 344:857-868.
4. Bagnall K.M., Higgins S.J., Sanders E.J. The contribution made by a single somite to the vertebral column: experimental evidence in support of resegmentation using the chick-quail chimaera model. Development 1988, 103:69-85.
5. Bayha E., Jorgensen M.C., Serup P., Grapin-Botton A. Retinoic acid signaling organizes endodermal organ specification along the entire antero-posterior axis. PLoS One 2009, 4:e5845.
6. Begemann G., Schilling T.F., Rauch G.J., Geisler R., Ingham P.W. The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 2001, 128:3081-3094.
7. Bird N.C., Mabee P.M. Developmental morphology of the axial skeleton of the zebrafish, Danio rerio (Ostariophysi: Cyprinidae). Dev. Dyn. 2003, 228:337-357.
8. Birkholz D.A., Olesnicky Killian E.C., George K.M., Artinger K.B. Prdm1a is necessary for posterior pharyngeal arch development in zebrafish. Dev. Dyn. 2009, 238:2575-2587.
9. Bruce A.E., Oates A.C., Prince V.E., Ho R.K. Additional hox clusters in the zebrafish: divergent expression patterns belie equivalent activities of duplicate hoxB5 genes. Evol. Dev. 2001, 3:127-144.
10. Burke A.C., Nelson C.E., Morgan B.A., Tabin C. Hox genes and the evolution of vertebrate axial morphology. Development 1995, 121:333-346.
11. Chambers K.E., McDaniell R., Raincrow J.D., Deshmukh M., Stadler P.F., Chiu C.H. Hox cluster duplication in the basal teleost Hiodon alosoides (Osteoglossomorpha). Theory Biosci. 2009, 128:109-120.
12. Chen F., Capecchi M.R. Targeted mutations in hoxa-9 and hoxb-9 reveal synergistic interactions. Dev. Biol. 1997, 181:186-196.
13. Chen C., Zhang Y., Zhang L., Weakley S.M., Yao Q. MicroRNA-196: critical roles and clinical applications in development and cancer. J. Cell. Mol. Med. 2011, 15:14-23.
14. Crump J.G., Maves L., Lawson N.D., Weinstein B.M., Kimmel C.B. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 2004, 131:5703-5716.
15. Davis A.P., Witte D.P., Hsieh-Li H.M., Potter S.S., Capecchi M.R. Absence of radius and ulna in mice lacking hoxa-11 and hoxd-11. Nature 1995, 375:791-795.
16. Di-Poi N., Koch U., Radtke F., Duboule D. Additive and global functions of HoxA cluster genes in mesoderm derivatives. Dev. Biol. 2010, 341:488-498.
17. Duboule D., Morata G. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 1994, 10:358-364.
18. Dupe V., Ghyselinck N.B., Wendling O., Chambon P., Mark M. Key roles of retinoic acid receptors alpha and beta in the patterning of the caudal hindbrain, pharyngeal arches and otocyst in the mouse. Development 1999, 126:5051-5059.
19. Emoto Y., Wada H., Okamoto H., Kudo A., Imai Y. Retinoic acid-metabolizing enzyme Cyp26a1 is essential for determining territories of hindbrain and spinal cord in zebrafish. Dev. Biol. 2005, 278:415-427.
20. Ericson J.U., Krauss S., Fjose A. Genomic sequence and embryonic expression of the zebrafish homeobox gene hox-3.4. Int. J. Dev. Biol. 1993, 37:263-272.
21. Finnerty J.R., Pang K., Burton P., Paulson D., Martindale M.Q. Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science 2004, 304:1335-1337.
22. Fischer S., Draper B.W., Neumann C.J. The zebrafish fgf24 mutant identifies an additional level of Fgf signaling involved in vertebrate forelimb initiation. Development 2003, 130:3515-3524.
23. Fjose A., Zhao X.F. Exploring microRNA functions in zebrafish. N. Biotechnol. 2010.
24. Garcia-Gasca A., Spyropoulos D.D. Differential mammary morphogenesis along the anteroposterior axis in Hoxc6 gene targeted mice. Dev. Dyn. 2000, 219:261-276.
25. Garrity D.M., Childs S., Fishman M.C. The heartstrings mutation in zebrafish causes heart/fin Tbx5 deficiency syndrome. Development 2002, 129:4635-4645.
26. Gehring W.J., Kloter U., Suga H. Evolution of the Hox gene complex from an evolutionary ground state. Curr. Top. Dev. Biol. 2009, 88:35-61.
27. Gibert Y., Gajewski A., Meyer A., Begemann G. Induction and prepatterning of the zebrafish pectoral fin bud requires axial retinoic acid signaling. Development 2006, 133:2649-2659.
28. Graham A., Papalopulu N., Krumlauf R. The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 1989, 57:367-378.
29. Grande T., Young B. The ontogeny and homology of the Weberian apparatus in the zebrafish Danio rerio (Ostariophysi: Cypriniformes). Zool. J. Linn. Soc. 2005, 104:241-254.
30. Grandel H., Lun K., Rauch G.J., Rhinn M., Piotrowski T., Houart C., Sordino P., Kuchler A.M., Schulte-Merker S., Geisler R., Holder N., Wilson S.W., Brand M. Retinoic acid signalling in the zebrafish embryo is necessary during pre-segmentation stages to pattern the anterior-posterior axis of the CNS and to induce a pectoral fin bud. Development 2002, 129:2851-2865.
31. Griffiths-Jones S., Saini H.K., van Dongen S., Enright A.J. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008, 36:D154-D158.
32. Hale L.A., Tallafuss A., Yan Y.L., Dudley L., Eisen J.S., Postlethwait J.H. Characterization of the retinoic acid receptor genes raraa, rarab and rarg during zebrafish development. Gene Expr. Patterns 2006, 6:546-555.
33. He L., Hannon G.J. MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 2004, 5:522-531.
34. He X., Eberhart J.K., Postlethwait J.H. MicroRNAs and micromanaging the skeleton in disease, development, and evolution. J. Cell. Mol. Med. 2009, 13:606-618.
35. Hoffman L., Miles J., Avaron F., Laforest L., Akimenko M.A. Exogenous retinoic acid induces a stage-specific, transient and progressive extension of Sonic hedgehog expression across the pectoral fin bud of zebrafish. Int. J. Dev. Biol. 2002, 46:949-956.
36. Horan G.S., Kovacs E.N., Behringer R.R., Featherstone M.S. Mutations in paralogous Hox genes result in overlapping homeotic transformations of the axial skeleton: evidence for unique and redundant function. Dev. Biol. 1995, 169:359-372.
37. Hornstein E., Mansfield J.H., Yekta S., Hu J.K., Harfe B.D., McManus M.T., Baskerville S., Bartel D.P., Tabin C.J. The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 2005, 438:671-674.
38. Hou W., Tian Q., Zheng J., Bonkovsky H.L. Zinc mesoporphyrin induces rapid proteasomal degradation of hepatitis C nonstructural 5A protein in human hepatoma cells. Gastroenterology 2010, 138:1909-1919.
39. Huang R., Zhi Q., Patel K., Wilting J., Christ B. Contribution of single somites to the skeleton and muscles of the occipital and cervical regions in avian embryos. Anat. Embryol. (Berl) 2000, 202:375-383.
40. Jarinova O., Hatch G., Poitras L., Prudhomme C., Grzyb M., Aubin J., Berube-Simard F.A., Jeannotte L., Ekker M. Functional resolution of duplicated hoxb5 genes in teleosts. Development 2008, 135:3543-3553.
41. Jeannotte L., Lemieux M., Charron J., Poirier F., Robertson E.J. Specification of axial identity in the mouse: role of the Hoxa-5 (Hox1.3) gene. Genes Dev. 1993, 7:2085-2096.
42. Kawasaki H., Taira K. MicroRNA-196 inhibits HOXB8 expression in myeloid differentiation of HL60 cells. Nucleic Acids Symp. Ser. (Oxf) 2004, 211-212.
43. Kopinke D., Sasine J., Swift J., Stephens W.Z., Piotrowski T. Retinoic acid is required for endodermal pouch morphogenesis and not for pharyngeal endoderm specification. Dev. Dyn. 2006, 235:2695-2709.
44. Kostic D., Capecchi M.R. Targeted disruptions of the murine Hoxa-4 and Hoxa-6 genes result in homeotic transformations of components of the vertebral column. Mech. Dev. 1994, 46:231-247.
45. Koudijs M.J., den Broeder M.J., Groot E., van Eeden F.J. Genetic analysis of the two zebrafish patched homologues identifies novel roles for the hedgehog signaling pathway. BMC Dev. Biol. 2008, 8:15.
46. Krumlauf R. Hox genes in vertebrate development. Cell 1994, 78:191-201.
47. Lawson N.D., Weinstein B.M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 2002, 248:307-318.
48. Lewis J., Hanisch A., Holder M. Notch signaling, the segmentation clock, and the patterning of vertebrate somites. J. Biol. 2009, 8:44.
49. Li Y., Zhang M., Chen H., Dong Z., Ganapathy V., Thangaraju M., Huang S. Ratio of miR-196s to HOXC8 messenger RNA correlates with breast cancer cell migration and metastasis. Cancer Res. 2010, 70:7894-7904.
50. Linville A., Radtke K., Waxman J.S., Yelon D., Schilling T.F. Combinatorial roles for zebrafish retinoic acid receptors in the hindbrain, limbs and pharyngeal arches. Dev. Biol. 2009, 325:60-70.
51. Lund A.H. miR-10 in development and cancer. Cell Death Differ. 2009.
52. Ma L., Teruya-Feldstein J., Weinberg R.A. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007, 449:682-688.
53. 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.
54. McGlinn E., Yekta S., Mansfield J.H., Soutschek J., Bartel D.P., Tabin C.J. In ovo application of antagomiRs indicates a role for miR-196 in patterning the chick axial skeleton through Hox gene regulation. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18610-18615.
55. McIntyre D.C., Rakshit S., Yallowitz A.R., Loken L., Jeannotte L., Capecchi M.R., Wellik D.M. Hox patterning of the vertebrate rib cage. Development 2007, 134:2981-2989.
56. Mercader N. Early steps of paired fin development in zebrafish compared with tetrapod limb development. Dev. Growth Differ. 2007, 49:421-437.
57. Mercader N., Fischer S., Neumann C.J. Prdm1 acts downstream of a sequential RA, Wnt and Fgf signaling cascade during zebrafish forelimb induction. Development 2006, 133:2805-2815.
58. Minoux M., Antonarakis G.S., Kmita M., Duboule D., Rijli F.M. Rostral and caudal pharyngeal arches share a common neural crest ground pattern. Development 2009, 136:637-645.
59. Morin-Kensicki E.M., Melancon E., Eisen J.S. Segmental relationship between somites and vertebral column in zebrafish. Development 2002, 129:3851-3860.
60. Niederreither K., Subbarayan V., Dolle P., Chambon P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 1999, 21:444-448.
61. Nolte C., Amores A., Nagy Kovacs E., Postlethwait J., Featherstone M. The role of a retinoic acid response element in establishing the anterior neural expression border of Hoxd4 transgenes. Mech. Dev. 2003, 120:325-335.
62. Oliver G., De Robertis E.M., Wolpert L., Tickle C. Expression of a homeobox gene in the chick wing bud following application of retinoic acid and grafts of polarizing region tissue. EMBO J. 1990, 9:3093-3099.
63. Perz-Edwards A., Hardison N.L., Linney E. Retinoic acid-mediated gene expression in transgenic reporter zebrafish. Dev. Biol. 2001, 229:89-101.
64. Postlethwait J.H., Schneiderman H.A. A clonal analysis of determination in Antennapedia a homeotic mutant of Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 1969, 64:176-183.
65. Postlethwait J.H., Yan Y.L., Gates M.A., Horne S., Amores A., Brownlie A., Donovan A., Egan E.S., Force A., Gong Z., Goutel C., Fritz A., Kelsh R., Knapik E., Liao E., Paw B., Ransom D., Singer A., Thomson M., Abduljabbar T.S., Yelick P., Beier D., Joly J.S., Larhammar D., Rosa F., Westerfield M., Zon L.I., Johnson S.L., Talbot W.S. Vertebrate genome evolution and the zebrafish gene map. Nat. Genet. 1998, 18:345-349.
66. Prince V.E., Joly L., Ekker M., Ho R.K. Zebrafish hox genes: genomic organization and modified colinear expression patterns in the trunk. Development 1998, 125:407-420.
67. Rancourt D.E., Tsuzuki T., Capecchi M.R. Genetic interaction between hoxb-5 and hoxb-6 is revealed by nonallelic noncomplementation. Genes Dev. 1995, 9:108-122.
68. Rijli F.M., Matyas R., Pellegrini M., Dierich A., Gruss P., Dolle P., Chambon P. Cryptorchidism and homeotic transformations of spinal nerves and vertebrae in Hoxa-10 mutant mice. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:8185-8189.
69. Rusinov V., Baev V., Minkov I.N., Tabler M. MicroInspector: a web tool for detection of miRNA binding sites in an RNA sequence. Nucleic Acids Res. 2005, 33:W696-W700.
70. Sakaguchi S., Nakatani Y., Takamatsu N., Hori H., Kawakami A., Inohaya K., Kudo A. Medaka unextended-fin mutants suggest a role for Hoxb8a in cell migration and osteoblast differentiation during appendage formation. Dev. Biol. 2006, 293:426-438.
71. Sehm T., Sachse C., Frenzel C., Echeverri K. miR-196 is an essential early-stage regulator of tail regeneration, upstream of key spinal cord patterning events. Dev. Biol. 2009, 334:468-480.
72. Sparrow D.B., Chapman G., Turnpenny P.D., Dunwoodie S.L. Disruption of the somitic molecular clock causes abnormal vertebral segmentation. Birth Defects Res C Embryo Today. 2007, 81:93-110.
73. Taylor J.S., Braasch I., Frickey T., Meyer A., Van de Peer Y. Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res. 2003, 13:382-390.
74. Thatcher E.J., Paydar I., Anderson K.K., Patton J.G. Regulation of zebrafish fin regeneration by microRNAs. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18384-18389.
75. Thisse C., Thisse B. High Throughput Expression Analysis of ZF-Models Consortium Clones. ZFIN Direct Data Submission 2005, http://zfin.org.
76. Trevarrow B., Marks D.L., Kimmel C.B. Organization of hindbrain segments in the zebrafish embryo. Neuron 1990, 4:669-679.
77. van den Akker E., Fromental-Ramain C., de Graaff W., Le Mouellic H., Brulet P., Chambon P., Deschamps J. Axial skeletal patterning in mice lacking all paralogous group 8 Hox genes. Development 2001, 128:1911-1921.
78. Vella M.C., Choi E.Y., Lin S.Y., Reinert K., Slack F.J. The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 3'UTR. Genes Dev 2004, 18:132-137.
79. Wakahara T., Kusu N., Yamauchi H., Kimura I., Konishi M., Miyake A., Itoh N. Fibin, a novel secreted lateral plate mesoderm signal, is essential for pectoral fin bud initiation in zebrafish. Dev. Biol. 2007, 303:527-535.
80. Walker M.B., Kimmel C.B. A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech. Histochem. 2007, 82:23-28.
81. Waxman J.S., Keegan B.R., Roberts R.W., Poss K.D., Yelon D. Hoxb5b acts downstream of retinoic acid signaling in the forelimb field to restrict heart field potential in zebrafish. Dev Cell. 2008, 15:923-934.
82. Wellik D.M. Hox genes and vertebrate axial pattern. Curr. Top. Dev. Biol. 2009, 88:257-278.
83. Wendling O., Ghyselinck N.B., Chambon P., Mark M. Roles of retinoic acid receptors in early embryonic morphogenesis and hindbrain patterning. Development 2001, 128:2031-2038.
84. Wienholds E., Kloosterman W.P., Miska E., Alvarez-Saavedra E., Berezikov E., de Bruijn E., Horvitz H.R., Kauppinen S., Plasterk R.H. MicroRNA expression in zebrafish embryonic development. Science 2005, 309:310-311.
85. Woltering J.M., Durston A.J. The zebrafish hoxDb cluster has been reduced to a single microRNA. Nat. Genet. 2006, 38:601-602.
86. Woltering J.M., Durston A.J. MiR-10 represses HoxB1a and HoxB3a in zebrafish. PLoS ONE 2008, 3:e1396.
87. Wotton K.R., Weierud F.K., Dietrich S., Lewis K.E. Comparative genomics of Lbx loci reveals conservation of identical Lbx ohnologs in bony vertebrates. BMC Evol. Biol. 2008, 8:171.
88. Yekta S., Shih I.H., Bartel D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596.
89. Yekta S., Tabin C.J., Bartel D.P. MicroRNAs in the Hox network: an apparent link to posterior prevalence. Nat. Rev. Genet. 2008, 9:789-796.