Gene Duplication and Evolutionary Innovations in Hemoglobin-Oxygen Transport

Overview

Journal Physiology (Bethesda)

Specialty Physiology

Date 2016 Apr 8

PMID 27053736

Citations 35

Authors

Jay F Storz

Affiliations

Soon will be listed here.

Abstract

During vertebrate evolution, duplicated hemoglobin (Hb) genes diverged with respect to functional properties as well as the developmental timing of expression. For example, the subfamilies of genes that encode the different subunit chains of Hb are ontogenetically regulated such that functionally distinct Hb isoforms are expressed during different developmental stages. In some vertebrate taxa, functional differentiation between co-expressed Hb isoforms may also contribute to physiologically important divisions of labor.

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References

Hoffmann F, Opazo J, Storz J . Differential loss and retention of cytoglobin, myoglobin, and globin-E during the radiation of vertebrates. Genome Biol Evol. 2011; 3:588-600. PMC: 3156568. DOI: 10.1093/gbe/evr055. View

Johnson R, Buck S, Chiu C, Gage D, Shen T, Hendrickx A . Humans and old world monkeys have similar patterns of fetal globin expression. J Exp Zool. 2001; 288(4):318-26. DOI: 10.1002/1097-010X(20001215)288:4<318::AID-JEZ4>3.0.CO;2-0. View

Fago A, Carratore V, Di Prisco G, Feuerlein R, Sottrup-Jensen L, Weber R . The cathodic hemoglobin of Anguilla anguilla. Amino acid sequence and oxygen equilibria of a reverse Bohr effect hemoglobin with high oxygen affinity and high phosphate sensitivity. J Biol Chem. 1995; 270(32):18897-902. DOI: 10.1074/jbc.270.32.18897. View

Perutz M, FERMI G, Luisi B, Shaanan B, Liddington R . Stereochemistry of cooperative mechanisms in hemoglobin. Cold Spring Harb Symp Quant Biol. 1987; 52:555-65. DOI: 10.1101/sqb.1987.052.01.063. View

Johnson R, Buck S, Chiu C, Schneider H, Sampaio I, Gage D . Fetal globin expression in New World monkeys. J Biol Chem. 1996; 271(25):14684-91. DOI: 10.1074/jbc.271.25.14684. View

Opazo J, Hoffmann F, Storz J . Differential loss of embryonic globin genes during the radiation of placental mammals. Proc Natl Acad Sci U S A. 2008; 105(35):12950-5. PMC: 2529089. DOI: 10.1073/pnas.0804392105. View

Kleinschmidt T, Rucknagel K, Weber R, Koop B, Braunitzer G . Primary structure and functional properties of the hemoglobin from the free-tailed bat Tadarida brasiliensis (Chiroptera). Small effect of carbon dioxide on oxygen affinity. Biol Chem Hoppe Seyler. 1987; 368(6):681-90. DOI: 10.1515/bchm3.1987.368.1.681. View

Storz J, Opazo J, Hoffmann F . Gene duplication, genome duplication, and the functional diversification of vertebrate globins. Mol Phylogenet Evol. 2012; 66(2):469-78. PMC: 4306229. DOI: 10.1016/j.ympev.2012.07.013. View

Townes T, Fitzgerald M, Lingrel J . Triplication of a four-gene set during evolution of the goat beta-globin locus produced three genes now expressed differentially during development. Proc Natl Acad Sci U S A. 1984; 81(21):6589-93. PMC: 391975. DOI: 10.1073/pnas.81.21.6589. View

10.

Opazo J, Butts G, Nery M, Storz J, Hoffmann F . Whole-genome duplication and the functional diversification of teleost fish hemoglobins. Mol Biol Evol. 2012; 30(1):140-53. PMC: 3525417. DOI: 10.1093/molbev/mss212. View

11.

Lynch M, Katju V . The altered evolutionary trajectories of gene duplicates. Trends Genet. 2004; 20(11):544-9. DOI: 10.1016/j.tig.2004.09.001. View

12.

Natarajan C, Hoffmann F, Lanier H, Wolf C, Cheviron Z, Spangler M . Intraspecific polymorphism, interspecific divergence, and the origins of function-altering mutations in deer mouse hemoglobin. Mol Biol Evol. 2015; 32(4):978-97. PMC: 4379404. DOI: 10.1093/molbev/msu403. View

13.

Tomita S . Modulation of the oxygen equilibria of human fetal and adult hemoglobins by 2,3-diphosphoglyceric acid. J Biol Chem. 1981; 256(18):9495-500. View

14.

Cheviron Z, Natarajan C, Projecto-Garcia J, Eddy D, Jones J, Carling M . Integrating evolutionary and functional tests of adaptive hypotheses: a case study of altitudinal differentiation in hemoglobin function in an Andean Sparrow, Zonotrichia capensis. Mol Biol Evol. 2014; 31(11):2948-62. PMC: 4209134. DOI: 10.1093/molbev/msu234. View

15.

Damsgaard C, Storz J, Hoffmann F, Fago A . Hemoglobin isoform differentiation and allosteric regulation of oxygen binding in the turtle, Trachemys scripta. Am J Physiol Regul Integr Comp Physiol. 2013; 305(8):R961-7. PMC: 3798770. DOI: 10.1152/ajpregu.00284.2013. View

16.

Wood W . Haemoglobin synthesis during human fetal development. Br Med Bull. 1976; 32(3):282-7. DOI: 10.1093/oxfordjournals.bmb.a071376. View

17.

Weber R, Lalthantluanga R, Braunitzer G . Functional characterization of fetal and adult yak hemoglobins: an oxygen binding cascade and its molecular basis. Arch Biochem Biophys. 1988; 263(1):199-203. DOI: 10.1016/0003-9861(88)90628-5. View

18.

Storz J, Opazo J, Hoffmann F . Phylogenetic diversification of the globin gene superfamily in chordates. IUBMB Life. 2011; 63(5):313-22. PMC: 4399706. DOI: 10.1002/iub.482. View

19.

Berenbrink M, Koldkjaer P, Kepp O, Cossins A . Evolution of oxygen secretion in fishes and the emergence of a complex physiological system. Science. 2005; 307(5716):1752-7. DOI: 10.1126/science.1107793. View

20.

Opazo J, Lee A, Hoffmann F, Toloza-Villalobos J, Burmester T, Venkatesh B . Ancient Duplications and Expression Divergence in the Globin Gene Superfamily of Vertebrates: Insights from the Elephant Shark Genome and Transcriptome. Mol Biol Evol. 2015; 32(7):1684-94. PMC: 4476154. DOI: 10.1093/molbev/msv054. View