The heartstrings mutation in zebrafish causes heart/fin Tbx5 deficiency syndrome

Development

Volumn 129, Issue 19, 2002, Pages 4635-4645

  Garrity, Deborah M ^a   Childs, Sarah ^a   Fishman, Mark C ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Heart; Holt Oram syndrome; Limb induction; Pectoral fin; T box; Tbx5; Zebrafish

Indexed keywords

AMINO ACID; MORPHOLINE DERIVATIVE; MUTANT PROTEIN; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARM MALFORMATION; ARTICLE; AUTOSOMAL DOMINANT DISORDER; BRADYCARDIA; CELL SPECIFICITY; CELL TYPE; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; EMBRYO DEVELOPMENT; FISH; GENE MAPPING; GENE MUTATION; GENETIC CODE; GENETIC SCREENING; HEART ATRIUM; HEART DISEASE; HEART FUNCTION; HEART RATE; HEART VENTRICLE; HOLT ORAM SYNDROME; HOMOZYGOSITY; LETHAL GENE; LIMB MALFORMATION; MALFORMATION SYNDROME; MAMMAL; MOLECULAR CLONING; MORPHOGENESIS; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN ISOLATION; RECESSIVE GENE; SIBLING; WILD TYPE; ZEBRA FISH;

ANIMALS; CHROMOSOME MAPPING; GENE EXPRESSION PROFILING; HEART; HEART DEFECTS, CONGENITAL; PROTEIN BIOSYNTHESIS; SYNDROME; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO; MAMMALIA; VERTEBRATA;

EID: 0036800297     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (91)

1. Abdelilah, S. and Driever, W. (1997). Pattern formation in janus-mutant zebrafish embryos. Dev. Biol. 184, 70-84.
2. Ahn, D., Kourakis, M. J., Rohde, L. A., Silver, L. M. and Ho, R. K. (2002). T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature 417, 754-758.
3. Akimenko, M. A., Ekker, M., Wegner, J., Lin, W. and Westerfield, M. (1994). Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 14, 3475-3486.
4. Allende, M. L., Amsterdam, A., Becker, T., Kawakami, K., Gaiano, N. and Hopkins, N. (1996). Insertional mutagenesis in zebrafish identifies two novel genes, pescadillo and dead eye, essential for embryonic development. Genes Dev. 10, 3141-3155.
5. Bamshad, M., Le, T., Watkins, W. S., Dixon, M. E., Kramer, B. E., Roeder, A. D., Carey, J. C., Root, S., Schinzel, A., Van Maldergem, L. et al. (1999). The spectrum of mutations in TBX3: Genotype/Phenotype relationship in ulnar-mammary syndrome. Am. J. Hum. Genet. 64, 1550-1562.
6. Bamshad, M., Lin, R. C., Law, D. J., Watkins, W. C., Krakowiak, P. A., Moore, M. E., Franceschini, P., Lala, R., Holmes, L. B., Gebuhr, T. C. et al. (1997). Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome. Nat. Genet. 10, 311-313.
7. Barresi, M. J., Stickney, H. L. and Devoto, S. H. (2000). The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity. Development 127, 2189-2199.
8. Basson, C. T., Bachinsky, D. R., Lin, R. C., Levi, T., Elkins, J. A., Soults, J., Grayzel, D., Kroumpouzou, E., Traill, T. A., Leblanc-Straceski, J. et al. (1997) Mutation in human TBX5 cause limb and cardiac malformation in Holt-Oram syndrome. Nat. Genet. 15, 30-35.
9. Basson, C. T., Cowley, G. S., Solomon, S. D., Weissman, B., Poznanski, A. K., Traill, T. A., Seidman, J. G. and Seidman, C. E. (1994). The clinical and genetic spectrum of the Holt-Oram syndrome (heart-hand syndrome). New Engl. J. Med. 330, 885-891.
10. Basson, C. T., Huang, T., Lin, R. C., Bachinsky, D. R., Weremowicz, S., Yaglio, A., Bruzzone, R., Quadrelli, R., Lerone, M., Romeo, G. et al. (1999). Different TBX5 interactions in heart and limb defined by Holt-Oram, syndrome mutations. Proc. Natl. Acad. Sci. USA 96, 2919-2924.
11. Begemann, G. and Ingham, P. W. (2000). Developmental regulation of Tbx5 in zebrafish embryogenesis. Mech. Dev. 90, 299-304.
12. Begemann, G., Schilling, T. F., Rauch, G. J., Geisler, R. and Ingham, P. W. (2001). The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 128, 3081-3094.
13. Braybrook, C., Doudney, K., Marcano, A. C., Arnason, A., Bjornsson, A., Patton, M. A., Goodfellow, P. J., Moore, G. E. and Stanier, P. (2001). The T-box transcription factor gene TBX22 is mutated in X-linked cleft palate and ankyloglossia. Nat. Genet. 29, 179-183.
14. Bruneau, B. G., Logan, M., Davis, N., Levi, T., Tabin, C. J., Seidman, J. G. and Seidman, C. E. (1999). Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome. Dev. Biol. 211, 100-108.
15. Bruneau, B. G., Nemer, G., Schmitt, J. P., Charron, F., Robitaille, L., Caron, S., Conner, D. A., Gessler, M., Nemer, M., Seidman, C. E. et al. (2001). A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106, 709-721.
16. Chapman D. L., Garvey, N., Hancock, S., Alexiou, M., Agulnik, S. I., Gibson-Brown, J. J., Cebra-Thomas. J., Bollag, R. J., Silver, L. M. and Papainannou, V. E. (1996). Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev. Dyn. 206, 379-390.
17. Chen, J. N., van Bebber, F., Goldstein, A. M., Serluca, F. C., Jackson, D, Childs, S., Serbedzija, G. N., Warren, K. S., Mably, J. D., Garrity, D. M. et al. (2001). Genetic steps to organ laterality in zebrafish. Comp. Funct. Genomics 2, 60-68.
18. Chen, J. N., van Eeden, F. J., Warren, K. S., Chin, A., Nusslein-Volhard, C., Haffter, P. and Fishman, M. C. (1997). Left-right pattern of cardiac BMP4 may drive asymmetry of the heart in zebrafish. Development 124, 4373-4382.
19. Childs, S., Weinstein, B. M., Mohideen, M. A., Donobue, S., Bonkovsky, H. and Fishman, M. C. (2000). Zebrafish dracula encodes ferrochelatase and its mutation provides a model for erythropoietic protoporphyria. Curr. Biol. 10, 1001-1004.
20. Christoffels, V. M., Habets, P. E., Franco, D., Campione, M., de Jong, F., Lamers, W. H., Bao, Z. Z., Palmer, S., Biben, C., Harvey, R. P. et al. (2000). Chamber formation and morphogenesis in the developing mammalian heart. Dev. Biol. 223, 266-278.
21. Dixon, J. W., Costa, T. and Teshima, I. E. (1993). Mosaicism for duplication 12q (12q13→q24.2) in a dysmorphic male infant. J. Med. Genet. 30, 70-72.
22. Ekker, S. C. and Larson, J. D. (2001). Morphant technology in model developmental systems. Genesis 30, 89-93.
23. Geisler, R., Rauch, G. J., Baier, H., van Bebber, F., Brobeta, L., Dekens, M. P., Finger, K., Fricke, C., Gates, M. A., Geiger, H. et al. (1999). A radiation hybrid map of the zebrafish genome. Nat. Genet. 23, 86-89.
24. Ghosh, T. K., Packham, E. A., Bonser, A. J., Robinson, T. E., Cross, S. J. and Brook, J. D. (2001). Characterization of the TBX5 binding site and analysis of mutations that cause Holt-Oram syndrome. Hum. Mol. Genet. 10, 1983-1994.
25. Gibson-Brown, J. J., Agulnik, S. I., Silver, L. M., Niswander, L. and Papaioannou, V. E. (1998). Involvement of T-box genes Tbx2-Tbx5 in vertebrate limb specification and development. Development 125, 2499-2509.
26. Grandel, H. and Schulte-Merker, S. (1998) The development of the paired fins in the zebrafish (Danio rerio). Mech. Dev. 79, 99-120.
27. Gurdon, J. B. and Bourillot, P. Y. (2001). Morphogen gradient interpretation. Nature 413, 797-803.
28. Hatcher, C. J. and Basson, C. T. (2001). Getting the T-box dose right. Nat. Med. 7, 1163-1170.
29. Hatcher, C. J., Goldstein, M. M., Mah, C. S., Delia, C. S. and Basson, C. T. (2O00a). Identification and localization of TBX5 transcription factor during human cardiac morphogenesis. Dev. Dyn. 219, 90-95.
30. Hatcher, C. J., Kim, M. S. and Basson. C. T. (2000b). Atrial form and function: lessons from human molecular genetics. Trends Cardiovasc. Med. 10, 93-101.
31. Heasman, J. (2002). Morpholino oligos: making sense of antisense? Dev. Biol. 243, 209-214.
32. Herrmann, B. G. (1991). Expression pattern of the Brachyury gene in whole-mount TWis/TWis mutant embryos. Development 113, 913-917.
33. Hiroi, Y., Kudoh, S., Monzen, K., Ikeda, Y., Yazaki, Y., Nagai, R. and Komuro, I. (2001). Tbx5 associates with Nkx2-5 and synergistically promotes cardiomyocyte differentiation. Nat. Genet. 28, 276-280.
34. Horb, M. E. and Thomsen, G. H. (1999). Tbx5 is essential for heart development. Development 126, 1739-1751.
35. Hutson, L. D. and Chien, C. B. (2002). Pathfinding and error correction by retinal axons: the role of astray/robo2. Neuron 33, 205-217.
36. Imai, Y. and Talbot, W. S. (2001). Morpholino phenocopies of the bmp2b/swirl and bmp7/snailhouse mutations. Genesis 30, 160-163.
37. Isaac, A., Rodriguez-Esteban, C., Ryan, A., Altabef, M., Tsukui, T., Patel, K., Tickle, C. and Izpisua-Belmonte, J. C. (1998). Tbx genes and limb identity in chick embryo development. Development 125, 1867-1875.
38. Kawakami, Y., Capdevila, J., Buscher, D., Itoh, T., Rodriguez Esteban, C. and Izpisua Belmonte, J. C. (2001). WNT signals control FG2F-dependent limb initiation and AER induction in the chick embryo. Cell 104, 891-900.
39. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
40. Knapik, E. W., Goodman. A., Ekker, M., Chevrette, M., Delgado, J., Neuhauss, S., Shimoda, N., Driever, W., Fishman, M. C. and Jacob, H. J. (1998). A microsatellite genetic linkage map for zebrafish (Danio rerio). Nat. Genet. 18, 338-343.
41. Krauss, S., Concordet, J. P. and Ingham, P. W. (1993). A functionally conserved homolog, of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431-1444.
42. Kupperman, E., An, S., Osborne, N., Waldron, S. and Stainier, D. Y. (2000). A sphingosine-1-phosphate receptor regulates cell migration during vertebrate heart development. Nature 406, 192-195.
43. Li, Q. Y., Newbury-Ecob, R. A., Terrett, J. A., Wilson, D. I., Curtis, A. R., Yi, C. H., Gebuhr, T., Bullen, P. J., Robson, S. C., Strachan, T. et al. (1997). Holt-Oram syndrome is caused by mutations in TBX5, a member of the Brachyury (T) gene family. Nat. Genet. 15, 21-29.
44. Liao, E. C., Trede, N. S., Ransom, D., Zapata, A., Kieran, M. and Zon, L. I. (2002). Non-cell autonomous requirement for the bloodless gene in primitive hematopoiesis of zebrafish. Development 129, 649-659.
45. Liberatore, C. M., Searcy-Schrick, R. D. and Yutzey, K. E. (2000). Ventricular expression of tbx5 inhibits normal heart chamber development. Dev. Biol. 223, 169-180.
46. Lindsay, E. A., Vitelli, F., Su, H., Morishima, M., Huynh, T., Pramparo, T., Jurecic, V., Ogunrinu, G., Sutherland, H. F., Scambler, P. J. et al. (2001). Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 410, 97-101.
47. Logan, M., Simon, H. G. and Tabin, C. (1998). Differential regulation of T-box and homeobox transcription factors suggests roles in controlling chick limb-type identity. Development 125, 2825-2835.
48. Logan, M. and Tabin, C. J. (1999). Role of Pitx1 upstream of Tbx4 in specification of hindlimb identity. Science 283, 1736-1739.
49. Lyons, S. E., Lawson, N. D., Lei, L., Bennett, P. E., Weinstein, B. M. and Liu, P. P. (2002). A nonsense mutation in zebrafish gata1 causes the bloodless phenotype in vlad tepes. Proc. Natl. Acad. Sci. USA 99, 5454-5459.
50. Malicki, J. J., Pujic, Z., Thisse, C., Thisse, B. and Wei, X. (2002). Forward and reverse genetic approaches to the analysis of eye development in zebrafish. Vision Res. 42, 527-533.
51. Martinez-Barbera, J. P., Toresson, H., Da Rocha, S. and Krauss, S. (1997). Cloning and expression of three members of the zebrafish Bmp family: Bmp2a, Bmp2b and Bmp4. Gene 198, 53-59.
52. McCorquodale, M. M., Rolf, J., Ruppert, E. S., Kurczynski, T. W. and Kolacki, P. (1986). Duplication (12q) syndrome in female cousins, resulting from maternal (11;12) (p15.5;q24.2) translocations. Am. J. Med. Genet. 24, 613-622.
53. Melnyk, A. R., Weiss, L., Van Dyke, D. L. and Jarvi, P. (1981). Malformation syndrome of duplication 12q24.1 leads to qter. Am. J. Med. Genet. 10, 357-365.
54. Merscher, S., Funke, B., Epstein, J. A., Heyer, J., Puech, A., Lu, M. M., Xavier, R. J., Demay, M. B., Russell. R. G., Factor, S. et al. (2001). TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104, 619-629.
55. Michelmore, R. W., Paran, I. and Kesseli, R. V. (1991). Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl. Acad. Sci. USA 88, 9828-9832.
56. Min, H., Danilenko, D. M., Scully, S. A., Bolon, B., Ring, B. D., Tarpley, J. E., DeRose, M. and Simonet, W. S. (1999). Fgf-10 is required for both limb and lung development and exhibit striking functional similarity to Drosophila branchless. Genes Dev. 12, 3156-3161.
57. Mowbray, C., Hammerschmidt, M. and Whitfield, T. T. (2001). Expression of BMP signalling pathway members in the developing zebrafish inner ear and lateral line. Mech. Dev. 108, 179-184.
58. Murray, J. C. (2001). Time for T. Nat. Genet. 29, 107-109.
59. Nagy, E. and Maquat, L. E. (1998). A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23, 198-199.
60. Neumann, C. J., Grandel, H., Gaffield, W., Schulte-Merker, S. and Nusslein-Volhard, C. (1999). Transient establishment of anteroposterior polarity in the zebrafish pectoral fin bud in the absence of sonic hedgehog activity. Development 126, 4817-4826.
61. Newbury-Ecob, R. A., Leanage, R., Raeburn, J. A. and Young, I. D. (1996). Holt-Oram syndrome: a clinical genetic study. J. Med. Genet. 33, 300-307.
62. Ohuchi, H., Takeuchi, J., Yoshloka, H., Ishimaru, Y., Ogura, K., Takahashi, N., Ogura, T. and Noji, S. (1998). Correlation of wing-leg identity in ectopic FGF-induced chimeric limbs with the differential expression of chick Tbx5 and Tbx4. Development 125, 51-60.
63. Popperl, H., Rikhof, H., Chang, H., Haffter, P., Kimmel, C. B. and Moens, C. B. (2000). lazarus is a novel pbx gene that globally mediates hox gene function in zebrafish. Mol. Cell 6, 233-267.
64. Rodriguez-Esteban, C., Tsukui, T., Yonei, S., Magallon, J., Tamura, K. and Izpisua Belmonte, J. C. (1999). The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identity. Nature 399, 814-818.
65. Rottbauer, W., Baker, K., Wo, Z. G., Mohideen, M. A., Cantiello, H. F. and Fishman, M. C. (2001) Growth and function of the embryonic heart depend upon the cardiac-specific L-type calcium channel alpha1 subunit. Dev. Cell 1, 265-275.
66. Ruvinsky, I, Oates, A. C., Silver, L. M. and Ho, R. K. (2000). The evolution of paired appendages in vertebrates: T-box genes in the zebrafish. Dev. Genes Evol. 210, 82-91.
67. Schilling, T. F, Walker, C. and Kimmel, C. B. (1996). The chinless mutation and neural crest cell interactions in zebrafish jaw development. Development 122, 1417-1426.
68. Sehnert, A. J., Huq, A., Weinstein, B. M., Walker, C., Fishman. M. and Stainier, D. Y. (2002). Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat. Genet. 31, 106-110.
69. Sekine, K., Ohuchi, H., Fujiwara, M., Yamasaki, M., Yoshizawa, T., Sato, T., Yagishita, N., Matsui, D., Koga, Y., Itoh, N. et al. (1999). Fgf10 is essential for limb and lung formation. Nat. Genet. 21, 138-141.
70. Serbedzija, G. N., Chen, J. N. and Fishman, M. C. (1998). Regulation in the heart field of zebrafish. Development 125, 1095-1101.
71. Serluca, F. C., Drummond, I. A. and Fishman, M. C. (2002). Endothelial signaling in kidney morphogenesis. A role for hemodynamic forces. Curr. Biol. 12, 492-497.
72. Simon, H. (1999). T-box genes and the formation of vertebrate forelimb- and hindlimb specific pattern. Cell Tissue Res. 296, 57-66.
73. Smith, J. (1999). T-box genes: what they do and how they do it. Trends Genet. 15, 154-158.
74. Sordino, P., van der Hoeven, E. and Duboule, D. (1995). Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375, 678-681.
75. Stainier, D. Y. and Fishman, M. C. (1992). Patterning the zebrafish heart tube: acquisition of anteroposterior polarity. Dev. Biol. 153, 91-101.
76. Sun, Z. and Hopkins, N. (2001). vhnfl, the MODY5 and familial GCKD-associated gene, regulates regional specification of the zebrafish gut, pronephros, and hindbrain. Genes Dev. 15, 3217-3229.
77. Tada, M. and Smith, J. C. (2001). T-targets: clues to understanding the functions of T-box proteins. Dev. Growth Differ. 43, 1-11.
78. Takeuchi, J. K., Koshiba-Takeuchi, K., Matsumoto, K., Vogel-Hopker, A., Naitoh-Matsuo, M., Ogura, K., Takahashi, N., Yasuda, K. and Ogura, T. (1999). Tbx5 and Tbx4 genes determine the wing/leg identity of limb buds Nature, 398, 810-814
79. Tamura, K, Kuraishi, R., Saito, D., Masaki, H., Ide, H. and Yonei-Tamura, S. (2001). Evolutionary aspects of positioning and identification of vertebrate limbs. J. Anat. 199, 195-204.
80. Tamura, K., Yonei-Tamura, S. and Belmonte, J. C. (1999). Differential expression of Tbx4 and Tbx5 in zebrafish fin buds. Mech. Dev. 87, 181-184.
81. Thisse, C., Thisse, B., Schilling, T. F. and Postlethwait, J. H. (1993). Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119, 1203-1215.
82. van Eeden, F. J., Granato, M., Schach, U., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J., Kane, D A. et al. (1996). Genetic analysis of fin formation in the zebrafish, Danio rerio. Development 123, 255-262.
83. Veitia, R. A. (2002). Exploring the etiology of haploinsufficiency. BioEssays 24, 175-184.
84. Vihtelic, T. S. and Hyde, D. R. (2O02). Zebrafish mutagenesis yields eye morphological mutants with retinal and lens defects. Vision Res. 42, 535-540.
85. Walsh, E. C. and Stainier, D. Y. (2001). UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 293, 1670-1673.
86. Warren, K. S., Baker, K. and Fishman, M. C. (2001). The slow mo mutation reduce pacemaker current and heart rate in adult zebrafish. Am. J. Physiol. Heart Circ. Physiol. 281, H1711-1719.
87. Xu, X., Meiler, S. E., Zhong, T. P., Mohideen, M., Crossley, D. A., Burggren, W. W. and Firsman, M. C. (2002). Cardiomyopathy in zebrafish due to mutation in an alternatively spliced exon of titin. Nat. Genet. 30, 205-209.
88. Xu, X., Weinstein, M., Li, C., Naski, M., Cohen, R. I, Ornitz, D. M., Leder, P. and Deng, C. (1998). Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125, 753-765.
89. Yelon, D., Horne, S. A. and Stainier, D. Y. (1999). Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 214, 23-37.
90. Yelon, D. and Stainier, D. Y. (1999). Patterning during organogenesis: genetic analysis of cardiac chamber formation. Semin. Cell Dev. Biol. 10, 93-98.
91. Yelon, D., Ticho, B., Halpern, M. E., Ruvinsky, I., Ho, R. K., Silver, L. M. and Stainier, D. Y. (2000). The bHLH transcription factor Hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development 127, 2573-2582.