Developmental regulation of hemoglobin synthesis in the green anole lizard Anolis carolinensis

Journal of Experimental Biology

Volumn 214, Issue 4, 2011, Pages 575-581

  Storz, Jay F ^a   Hoffmann, Federico G ^a,d   Opazo, Juan C ^b   Sanger, Thomas J ^c   Moriyama, Hideaki ^a  

^a UNIVERSITY OF NEBRASKA   (United States)

^b UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^c HARVARD UNIVERSITY   (United States)

^d MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

Anolis; Gene duplication; Globin gene family; Hemoglobin; Reptile genomics

Indexed keywords

HEMOGLOBIN; ISOPROTEIN;

ANIMAL; ARTICLE; BIOSYNTHESIS; COMPARATIVE STUDY; DENSITOMETRY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOELECTRIC FOCUSING; LIZARD; METABOLISM; PHYLOGENY; PHYSIOLOGY; PROTEOMICS; SPECIES DIFFERENCE;

ANIMALS; DENSITOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMOGLOBINS; ISOELECTRIC FOCUSING; LIZARDS; PHYLOGENY; PROTEIN ISOFORMS; PROTEOMICS; SPECIES SPECIFICITY;

AMPHIBIA; ANOLIS; ANOLIS CAROLINENSIS; AVES; MAMMALIA; REPTILIA; SQUAMATA; TETRAPODA; VERTEBRATA;

EID: 79951479847     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.050443     Document Type: Article

References (47)

1. Abramoff, M. D., Magelhaes, P. J. and Ram, S. J. (2004). Image processing with Image J. Biophotonics Int. 11, 36-42.
2. Alev, C., McIntyre, B. A. S., Nagai, H., Shin, M., Shinmyozu, K., Jakt, L. M. and Sheng, G. (2008). BetaA, the major beta globin in definitive red blood cells, is present from the onset of primitive erythropoiesis in chicken. Dev. Dyn. 237, 1193-1197. (Pubitemid 351542315)
3. Alev, C., Shinmyozu, K., McIntyre, B. A. S. and Sheng, G. (2009). Genomic organization of zebra finch alpha and beta globin genes and their expression in primitive and definitive blood in comparison with globins in chicken. Dev. Genes Evol. 219, 353-360.
4. Banville, D. and Williams, J. G. (1985a). Developmental changes in the pattern of larval beta-globin gene expression in Xenopus laevis. Identification of two early larval beta-globin mRNA sequences. J. Mol. Biol. 184, 611-620. (Pubitemid 15024768)
5. Banville, D. and Williams, J. G. (1985b). The pattern of expression of the Xenopus laevis tadpole α-globin genes and the amino acid sequence of the three major tadpole α-globin polypeptides. Nucleic Acids Res. 13, 5407-5421.
6. Baumann, R., Padeken, S. and Haller, E. A. (1982). Functional properties of embryonic chicken hemoglobins. J. Appl. Physiol. 53, 1439-1448. (Pubitemid 13217035)
7. Birchard, G. F., Black, C. P., Schuett, G. W. and Black, V. (1984). Foetal-maternal blood respiratory properties of an ovoviparous snake, the cottonmouth, Agkistrodon piscivorus. J. Exp. Biol. 108, 247-255.
8. Borgese, T. A. and Bertles, J. F. (1965). Hemoglobin heterogeneity: embryonic hemoglobin in the duckling and its disappearance in the adult. Science 148, 509-511.
9. Borgese, T. A. and Nagel, R. L. (1977). Differential effects of 2, 3-DPG, ATP and inositol pentaphosphate (IP5) on the oxygen equilibrium of duck embryonic, fetal and adult hemoglobins. Comp. Biochem. Physiol. 56A, 539-543. (Pubitemid 8052160)
10. Brittain, T. (2002). Molecular aspects of embryonic hemoglobin function. Mol. Aspects Med. 23, 293-342. (Pubitemid 34722606)
11. Brown, J. L. and Ingram, V. M. (1974). Structural studies on chick embryonic hemoglobins. J. Biol. Chem. 249, 3960-3972.
12. Campbell, K. L., Storz, J. F., Signore, A. V., Moriyama, H., Catania, K. C., Payson, A. P., Bonaventura, J., Stetefeld, J. and Weber, R. E. (2010). Molecular basis of a novel adaptation to hypoxic-hypercapnia in a strictly fossorial mole. BMC Evol. Biol. 10, 214.
13. Collins, F. S. and Weissman, S. M. (1984). The molecular genetics of human hemoglobin. Prog. Nucleic Acid Res. Mol. Biol. 31, 315-462.
14. Cooper, S. J. B., Wheeler, D., De Leo, A., Cheng, J., Holland, R. A. B., Marshall Graves, J. A. and Hope, R. M. (2006). The mammalian alphaD-globin gene lineage and a new model for the molecular evolution of alpha-globin gene clusters at the stem of the mammalian radiation. Mol. Phylogenet. Evol. 38, 439-448. (Pubitemid 43069388)
15. Fuchs, C., Burmester, T. and Hankeln, T. (2006). The amphibian globin gene repertoire as revealed by the Xenopus genome. Cytogenet. Genome Res. 112, 296-306. (Pubitemid 43260758)
16. Gorr, T. A., Mable, B. K. and Kleinschmidt, T. (1998). Phylogenetic analysis of reptilian hemoglobins: trees rates and divergences. J. Mol. Evol. 47, 471-485. (Pubitemid 28457764)
17. Grigg, G. C. and Harlow, P. (1981). A fetal-maternal shift of blood oxygen affinity in an Australian viviparous lizard, Sphenomorphus quoyii (Reptilia: Scincidae). J. Comp. Physiol. 142, 495-499.
18. Grigg, G. C., Wells, R. M. G. and Beard, L. A. (1993). Allosteric control of oxygen binding by haemoglobin during development in the crocodile Crocodylus porosus: the role of red cell organic phosphates and carbon dioxide. J. Exp. Biol. 175, 15-32.
19. Hardison, R. (1998). Hemoglobins from bacteria to man: evolution of different patterns of gene expression. J. Exp. Biol. 201, 1099-1117. (Pubitemid 28278316)
20. Hardison, R. (2001). Organization, evolution, and regulation of the globin genes. In Disorders of Hemoglobin: Genetics, Pathophysiology, and Clinical Management (eds M. H. Steinberg, B. G. Forget, D. R. Higgs and R. L. Nagel), pp. 95-115. Cambridge: Cambridge University Press.
21. Hiebl, I., Braunitzer, G. and Schneeganss, D. (1987). The primary structures of the major and minor hemoglobin-components of adult Andean goose (Chloephaga melanoptera Anatidae): the mutation Leu→Ser in position 55 of the β-chains. Biol. Chem. Hoppe-Seyler 368, 1559-1569.
22. Higgs, D. R., Vickers, M. A., Wilkie, A. O., Pretorius, I. M., Jarman, A. P. and Weatherall, D. J. (1989). A review of the molecular genetics of the human α-globin gene cluster. Blood 73, 1081-1104. (Pubitemid 19107407)
23. D-globin gene originated via duplication of an embryonic α-like globin gene in the ancestor of tetrapod vertebrates. Mol. Biol. Evol. 24, 1982-1990. (Pubitemid 47357613)
24. Hoffmann, F. G., Opazo, J. C. and Storz, J. F. (2008). Rapid rates of lineage-specific gene duplication and deletion in the α-globin gene family. Mol. Biol. Evol. 25, 591-602. (Pubitemid 351301915)
25. Hoffmann, F. G., Storz, J. F., Gorr, T. A. and Opazo, J. C. (2010). Lineage-specific patterns of functional diversification in the α-and β-globin gene families of tetrapod vertebrates. Mol. Biol. Evol. 27, 1126-1138.
26. Hughes, J. R., Cheng, J., Ventress, N., Prabhakar, S., Clark, K., Anguita, E., De Gobbi, M., de Jong, P., Rubin, E. and Higgs, D. R. (2005). Annotation of cisregulatory elements by identification, subclassification, and functional assessment of multispecies conserved sequences. Proc. Natl. Acad. Sci. USA 102, 9830-9835. (Pubitemid 40993653)
27. Ikehara, T., Eguchi, Y., Kayo, S. and Takei, H. (1997). Isolation and sequencing of two alpha-globin genes alpha (A) and alpha (D) in pigeon and evidence for embryospecific expression of the alpha (D)-globin gene. Biochem. Biophys. Res. Commun. 234, 450-453. (Pubitemid 27243923)
28. Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J. and Mann, M. (2005). Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 4, 1265-1272. (Pubitemid 41448714)
29. McIntyre, B. A. S., Alev, C., Tarui, H., Jakt, L. M. and Sheng, G. (2008). Expression profiling of circulating non-red blood cells in embryonic blood. BMC Dev. Biol. 8, 21.
30. Nagai, H. and Sheng, G. (2008). Definitive erythropoiesis in chicken yolk sac. Dev. Dyn. 237, 3332-3341.
31. Nagel, R. L. and Steinberg, M. H. (2001). Hemoglobins of the embryo and fetus and minor hemoglobins of adults. In Disorders of Hemoglobin: Genetics, Pathophysiology, and Clinical Management (eds M. H. Steinberg, B. G. Forget, D. R. Higgs and R. L. Nagel), pp. 197-230. Cambridge: Cambridge University Press.
32. Nakachi, M., Hoshi, M., Matsumoto, M. and Moriyama, H. (2008). Conserved sequences of sperm-activating peptide and its receptor throughout evolution, despite speciation in the sea star Asterias amurensis and closely related species. Zygote 16, 229-237. (Pubitemid 352039907)
33. Nakazawa, F., Nagai, H., Shin, M. and Sheng, G. (2006). Negative regulation of primitive hematopoeisis by the FGF signaling pathway. Blood 108, 3335-3343.
34. Opazo, J. C., Hoffmann, F. G. and Storz, J. F. (2008a). Genomic evidence for independent origins of β-like globin genes in monotremes and therian mammals. Proc. Natl. Acad. Sci. USA 105, 1590-1595. (Pubitemid 351346559)
35. Opazo, J. C., Hoffmann, F. G. and Storz, J. F. (2008b). Differential loss of embryonic globin genes during the radiation of placental mammals. Proc. Natl. Acad. Sci. USA 105, 12950-12955.
36. Patel, V. S., Cooper, S. J. B., Deakin, J. E., Fulton, B., Graves, T., Warren, W. C., Wilson, R. K. and Graves, J. A. M. (2008). Platypus globin genes and flanking loci suggest a new insertional model for β-globin evolution in birds and mammals. BMC Biol. 6, 34.
37. Pough, F. H. (1977). Ontogenetic change in molecular and functional properties of blood of garter snakes. J. Exp. Zool. 201, 47-56.
38. Proudfoot, N. J., Gil, A. and Maniatis, T. (1982). The structure of the human zetaglobin gene and a closely linked, nearly identical pseudogene. Cell 31, 553-563. (Pubitemid 13223940)
39. Ragsdale, F. R. and Ingermann, R. L. (1991). Influence of pregnancy on the oxygen affinity of red cells from the Northern Pacific rattlesnake Crotalis viridis oreganus. J. Exp. Biol. 159, 501-505.
40. Runck, A. M., Moriyama, H. and Storz, J. F. (2009). Evolution of duplicated (3-globin genes and the structural basis of hemoglobin isoform differentiation in Mus. Mol. Biol. Evol. 26, 2521-2532.
41. Sanger, T. J., Losos, J. B. and Gibson-Brown, J. J. (2008a). A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology. J. Morphol. 269, 129-137. (Pubitemid 351156105)
42. Sanger, T. J., Hime, P. M., Johnson, M. A. and Diani, J. (2008b). Protocols for husbandry and embryo collection of Anolis lizards. Herpetol. Rev. 39, 58-63. (Pubitemid 351499948)
43. Sellers, J. C., Trauth, S. E. and Wit, L. C. (1980). A method of caudal blood collection. J. Herpetol. 14, 185-187.
44. Storz, J. F., Hoffmann, F. G., Opazo, J. C. and Moriyama, H. (2008). Adaptive functional divergence among triplicated α-globin genes in rodents. Genetics 178, 1623-1638.
45. Storz, J. F., Runck, A. M., Moriyama, H., Weber, R. E. and Fago, A. (2010). Genetic differences in hemoglobin function between highland and lowland deer mice. J. Exp. Biol. 213, 2565-2574.
46. Weber, R. E., Fago, A., Val, A. L., Bang, A., Van Hauwaert, M. L., Dewilde, S., Zal, F. and Moens, L. (2000). Isohemoglobin differentiation in the bimodal-breathing amazon catfish Hoplosternum littorale. J. Biol. Chem. 275, 17297-17305. (Pubitemid 30430763)
47. Wells, R. M. G. and Baldwin, J. (1994). Oxygen transport in marine green turtle (Chelonia mydas) hatchlings: blood viscosity and control of hemoglobin-oxygen affinity. J. Exp. Biol. 188, 103-114.