Regulation of chamber-specific gene expression in the developing heart by Irx4

Science

Volumn 283, Issue 5405, 1999, Pages 1161-1164

  Bao, Zheng Zheng ^a   Bruneau, Benoit G ^a   Seidman, J G ^a   Seidman, Christine E ^b   Cepko, Constance L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN HEAVY CHAIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ELECTROPHYSIOLOGY; EMBRYO; EMBRYO DEVELOPMENT; FUNCTIONAL ANATOMY; GENE EXPRESSION REGULATION; HEART DEVELOPMENT; HOMEOBOX; IN SITU HYBRIDIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; ATRIAL MYOSINS; AVIAN PROTEINS; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART ATRIA; HEART VENTRICLES; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; MYOSIN HEAVY CHAINS; MYOSINS; PHENOTYPE; RECOMBINANT FUSION PROTEINS; RETROVIRIDAE;

ANIMALIA; GALLUS GALLUS; VERTEBRATA;

EID: 0033582685     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.283.5405.1161     Document Type: Article

References (38)

1. R. L. DeHaan, in Organogenesis, R. L. DeHaan and H. Ursprung, Eds. (Holt, Rinehart and Winston, New York, 1965), pp. 377-419.
2. M. C. Fishman and E. N. Olson, Cell 91, 153 (1997); M. C. Fishman and K. R. Chien, Development 124, 2099 (1997).
3. M. C. Fishman and E. N. Olson, Cell 91, 153 (1997); M. C. Fishman and K. R. Chien, Development 124, 2099 (1997).
4. R. Zeller, K. D. Bloch, B. S. Williams, R. J. Arceci, C. E. Seidman, Genes Dev. 1, 693 (1987).
5. K. R. Chien et al., Annu. Rev. Physiol. 55, 77 (1993); G. E. Lyons, Trends Cardiovasc. Med. 3, 184 (1994).
6. K. R. Chien et al., Annu. Rev. Physiol. 55, 77 (1993); G. E. Lyons, Trends Cardiovasc. Med. 3, 184 (1994).
7. J. Chen et al., J. Biol. Chem. 273, 1252 (1998); C. M. Pawloski-Dahm et al., Circulation 97, 1508 (1998).
8. J. Chen et al., J. Biol. Chem. 273, 1252 (1998); C. M. Pawloski-Dahm et al., Circulation 97, 1508 (1998).
9. Chick Irx4 cDNA was isolated by low-stringency hybridization of an E6-E8 random-primed retinal cDNA library with probes derived from a mouse expressed sequence tag (EST) clone (GenBank accession number W41873) and a human EST clone (GenBank accession number R46202). A full-length cDNA was obtained by screening an oligo(dT)-primed whole-embryo cDNA library (stages 12 to 15), with the original Irx4 done as a probe. Mouse Irx4 cONA was isolated similarly by low-stringency screening with chick Irx4 as a probe from an E10 mouse heart library (Stratagene). The DNA sequence was determined on both strands by an automated DNA sequencer (Applied Biosystems).
10. J. L. Gomez-Skarmeta, R. D. del Corral, E. de la Calle-Mustienes, D. Ferre-Marco, J. Modolell, Cell 85, 95 (1996).
11. H. McNeill, C. H. Yang, M. Brodsky, J. Ungos, M. A. Simon, Genes Dev. 11, 1073 (1997).
12. B. G. Bruneau et al., unpublished data.
13. Probe synthesis and in situ hybridization procedures were performed as in (25, 26). Proteinase K was used at 1 μg/ml, 2.5 μg/ml, and 10 μg/ml for embryos of stages 5 to 9, stages 10 to 14, or stage 15 and older, respectively. To avoid cross-hybridization to other Iroquois family members, we generated a template by Bbs I digestion of the Irx4 cDNA cloned in pBluescript SK(-) for synthesis of an antisense riboprobe (1.2 kb) without the homeobox sequence. In the misexpression experiments, a probe specific for the 5′ untranslated region (UTR) of chick Irx4 was used. Probes specific for VMHC1 and AMHC1 were created on the basis of their least conserved 3′ sequence including the 3′ UTR (12, 13). To prepare templates for making VMHC1 and AMHC1 probes, we performed reverse transcription-polymerase chain reaction (RT-PCR) using total RNA from stage-17 chick embryos (primers for VMHC1: 5′-CTACAAACACCAAGCAGAGGAAGC, 3′-GGTTTGCACTTGATATTTATTTTTGTA; and for AMHC1: 5′-GCGGGTCCAGCTTCTCCACTCC, 3′-GCACCTTGACACGCCGCTCTGACTT).
14. Z.-Z. Bao, B. G. Bruneau, J. G. Seidman, C. E. Seidman, C. L. Cepko, unpublished data.
15. J. G. Bisaha and D. Bader, Dev. Biol. 148, 355 (1991).
16. K. E. Yutzey, J. T. Rhee, D. Bader, Development 120, 871 (1994).
17. G. F. Wang, J. Nikovits, W. M. Schleinitz, F. E. Stockdale, Mol. Cell. Biol. 18, 6023 (1998).
18. _, J. Biol. Chem. 271, 19836 (1996).
19. 8 plaque-forming units per milliliter.
20. Fertile White Leghorn chicken eggs (SPAFAS, Norwich, CT) were incubated and staged (27). To visualize the embryo, we introduced 1 to 10 μl of India ink, diluted 1:50 in Ringer's buffer, beneath the blastoderm. Concentrated retroviral stocks were pressure injected into the cardiogenic mesoderm at stage 7-8 with a glass micropipette. The injected embryos were returned to the incubator until further analyses.
21. P. Badiani, P. Corbella, D. Kioussis, J. Marvel, K. Weston, Genes Dev. 8, 770 (1994); F. L. Conlon, S. G. Sedgwick, K. M. Weston, J. C. Smith, Development 122, 2427 (1996); T. Furukawa, E. M. Morrow, C. L. Cepko, Cell 91, 531 (1997).
22. P. Badiani, P. Corbella, D. Kioussis, J. Marvel, K. Weston, Genes Dev. 8, 770 (1994); F. L. Conlon, S. G. Sedgwick, K. M. Weston, J. C. Smith, Development 122, 2427 (1996); T. Furukawa, E. M. Morrow, C. L. Cepko, Cell 91, 531 (1997).
23. P. Badiani, P. Corbella, D. Kioussis, J. Marvel, K. Weston, Genes Dev. 8, 770 (1994); F. L. Conlon, S. G. Sedgwick, K. M. Weston, J. C. Smith, Development 122, 2427 (1996); T. Furukawa, E. M. Morrow, C. L. Cepko, Cell 91, 531 (1997).
24. D. Yelon and D. Stainier, unpublished data.
25. K. Yutzey, M. Gannon, D. Bader, Dev. Biol. 170, 531 (1995); T. Mikawa and D. A. Fischman, Annu. Rev. Physiol. 58, 509 (1996); D. Y. Stainier, R. K. Lee, M. C. Fishman, Development 119, 31 (1993).
26. K. Yutzey, M. Gannon, D. Bader, Dev. Biol. 170, 531 (1995); T. Mikawa and D. A. Fischman, Annu. Rev. Physiol. 58, 509 (1996); D. Y. Stainier, R. K. Lee, M. C. Fishman, Development 119, 31 (1993).
27. K. Yutzey, M. Gannon, D. Bader, Dev. Biol. 170, 531 (1995); T. Mikawa and D. A. Fischman, Annu. Rev. Physiol. 58, 509 (1996); D. Y. Stainier, R. K. Lee, M. C. Fishman, Development 119, 31 (1993).
28. J. Satin, S. Fujii, R. DeHaan, Dev. Biol. 129, 103 (1988).
29. P. J. Gruber, S. W. Kubalak, K. R. Chien, Development 125, 4427 (1998).
30. E. J. Bellefroid et al., EMBO J. 17, 191 (1998); J. L. Gomez-Skarmeta, A. Glavic, E. de la Calle-Mustienes, J. Modolell, R. Mayor, ibid., p. 181.
31. E. J. Bellefroid et al., EMBO J. 17, 191 (1998); J. L. Gomez-Skarmeta, A. Glavic, E. de la Calle-Mustienes, J. Modolell, R. Mayor, ibid., p. 181.
32. J. L. Gomez-Skarmeta and J. Modolell, Genes Dev. 10, 2935 (1996).
33. R. D. Riddle, R. L. Johnson, E. Laufer, C. Tabin, Cell 75, 1401 (1993).
34. Z. Z. Bao and C. L. Cepko, J. Neurosci. 17, 1425 (1997); L. Tessarollo, L. Nagarajan, L. F. Parada, Development 115, 11 (1992).
35. Z. Z. Bao and C. L. Cepko, J. Neurosci. 17, 1425 (1997); L. Tessarollo, L. Nagarajan, L. F. Parada, Development 115, 11 (1992).
36. V. Hamburger and H. L. Hamilton, J. Morphol. 88, 49 (1951).
37. Single-letter abbreviations for the amino acid residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu; F, Phe; G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met; N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; W, Trp; and Y, Tyr.
38. We thank K.-H. Lee for his help with histology; D. Schulte and D. Smith for control viruses; D. Schulte, J. Lin, A. Lassar, K.-H. Lee, M. Marvin, and M. Logan for critical review of the manuscript; and D. Yelon and D. Stainier for sharing unpublished results. Supported by the Howard Hughes Medical Institute, NIH (Z.-Z.B.), the American Heart Association, and the Medical Research Council of Canada (B.G.B.).