Substitutions in woolly mammoth hemoglobin confer biochemical properties adaptive for cold tolerance

Nature Genetics

Volumn 42, Issue 6, 2010, Pages 536-540

  Campbell, Kevin L ^a   Roberts, Jason E E ^a   Watson, Laura N ^b   Stetefeld, Jörg ^a   Sloan, Angela M ^a   Signore, Anthony V ^a   Howatt, Jesse W ^a   Tame, Jeremy R H ^c   Rohland, Nadin ^d,g   Shen, Tong Jian ^e   Austin, Jeremy J ^b   Hofreiter, Michael ^d,h   Ho, Chien ^e   Weber, Roy E ^f   Cooper, Alan ^b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^e CARNEGIE MELLON UNIVERSITY   (United States)

^f AARHUS UNIVERSITY   (Denmark)

^g HARVARD MEDICAL SCHOOL   (United States)

^h UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; HEME; HEMOGLOBIN;

ALTITUDE; AMINO ACID SUBSTITUTION; ARTICLE; CELL RESPIRATION; COLD TOLERANCE; DEOXYGENATION; EXTINCT SPECIES; HEAT LOSS; LOW TEMPERATURE; MAMMOTH; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; OXYGEN AFFINITY; PLEISTOCENE; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SUBSTITUTION; ANIMALS; COLD TEMPERATURE; DIPHOSPHOGLYCERIC ACIDS; ELEPHANTS; EVOLUTION, MOLECULAR; FOSSILS; HEMOGLOBINS; MAMMOTHS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXYGEN; PARTIAL PRESSURE;

ELEPHANTIDAE; MAMMUTHUS PRIMIGENIUS;

EID: 77952884376     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.574     Document Type: Article

References (30)

1. Benner, S.A., Caraco, M.D., Thomson, M. & Gaucher, E.A. Planetary biology\paleontological, geological, and molecular histories of life. Science 296, 864-868 (2002).
2. Jermann, T.M., Optiz, J.G., Stackhouse, J. & Benner, S.A. Reconstructing the evolutionary history of the artiodactyl ribonuclease superfamily. Nature 374, 57-59 (1995).
3. Beintema, J.J., Schuller, C., Irie, M. & Carsana, A. Molecular evolution of the ribonuclease superfamily. Prog. Biophys. Mol. Biol. 51, 165-192 (1988).
4. Rohland, N. et al. Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup. PLoS Biol. 5, e207 (2007).
5. Lister, A.M., Sher, A.V., van Essen, H. & Wei, G. The pattern and process of mammoth evolution in Eurasia. Quat. Int. 126-128, 49-64 (2005).
6. Lister, A.M. The impact of Quaternary Ice Ages on mammalian evolution. Phil. Trans. R. Soc. Lond. B 359, 221-241 (2004).
7. Lister, A. & Bahn, P.G. Mammoths: Giants of the Ice Age (University of California Press, Berkeley, California, USA, 2007).
8. Repin, V.E., Taranov, O.S., Ryabchikova, E.I., Tikhonov, A.N. & Pugachev, V.G. Sebaceous glands of the woolly mammoth, Mammuthus primigenius Blum: histological evidence. Dokl. Biol. Sci. 398, 382-384 (2004).
9. Römpler, H. et al. Nuclear gene indicates coat-color polymorphism in mammoths. Science 313, 62 (2006).
10. Miller, W. et al. Sequencing the nuclear genome of the extinct woolly mammoth. Nature 456, 387-390 (2008).
11. Braunitzer, G., Jelkmann, W., Stangl, A., Schrank, B. & Krombach, C. Hemoglobins, XLVIII: the primary structure of hemoglobin of the Indian elephant (Elephas maximus, Proboscidea): beta2=Asn. Hoppe-Seyler's Z. Physiol. Chem. 363, 683-691 (1982).
12. Braunitzer, G., Stangl, A., Schrank, B., Krombach, C. & Wiesner, H. Phosphate-haemoglobin interaction. The primary structure of the haemoglobin of the African elephant (Loxodonta africana, Proboscidea): asparagine in position 2 of the beta-chain. Hoppe-Seyler's Z. Physiol. Chem. 365, 743-749 (1984).
13. Opazo, J.C., Sloan, A.M., Campbell, K.L. & Storz, J.F. Origin and ascendency of a chimeric fusion gene: the beta/delta-globin gene of paenungulate mammals. Mol. Biol. Evol. 26, 1469-1478 (2009).
14. Perutz, M.F. Species adaptation in a protein molecule. Mol. Biol. Evol. 1, 1-28 (1983).
15. 2 equilibrium studies of human mutant hemoglobins. J. Biol. Chem. 260, 5919-5924 (1985).
16. Baudin, V. et al. Functional consequences of mutations at the allosteric interface in hetero-and homo-hemoglobin tetramers. Protein Sci. 2, 1320-1330 (1993).
17. Jones, R.T. & Shih, T.B. Hemoglobin variants with altered oxygen affnity. Hemoglobin 4, 243-261 (1980).
18. 2Y2101(G3)Glu- Lys; 75Ile; 136Gly: A high oxygen affnity fetal haemoglobin variant observed in a causcasian newborn. Biochim. Biophys. Acta 789, 224-228 (2004).
19. Clementi, M.E., Condò, S.G., Castagnola, M. & Giardina, B. Hemoglobin function under extreme life conditions. Eur. J. Biochem. 223, 309-317 (1994).
20. De Rosa, M.C., Castagnola, M., Bertonati, C, Galtier, A. & Giardina, B. From the Arctic to fetal life: physiological importance and structural basis of an 'additional' chloride-binding site in haemoglobin. Biochem. J. 380, 889-896 (2004).
21. Irving, L. & Krog, J. Temperature of skin in the arctic as a regulator of heat. J. Appl. Physiol. 7, 355-364 (1955).
22. Fronticelli, C. et al. Allosteric modulation by tertiary structure in mammalian hemoglobins. Introduction of the functional characteristics of bovine hemoglobin into human hemoglobin by fve amino acid substitutions. J. Biol. Chem. 270, 30588-30592 (1995).
23. Shen, T.J. et al. Production of unmodifed human adult hemoglobin in Escherichia coli. Proc. Natl. Acad. Sci. USA 90, 8108-8112 (1993).
24. Weber, R.E. Use of ionic and zwitterionic (Tris/BisTris and HEPES) buffers in studies on hemoglobin function. J. Appl. Physiol. 72, 1611-1615 (1992).
25. Park, S.-Y., Yokoyama, T., Shibayama, N., Shiro, Y. & Tame, J.R.H. 1.25 Å resolution crystal structures of human haemoglobin in the oxy, deoxy and carbonmonoxy forms. J. Mol. Biol. 360, 690-701 (2006).
26. Abraham, D.J., Peascoe, R.A., Randad, R.S. & Panikker, J. X-ray diffraction study of di and tetra-ligated T-state hemoglobin from high salt crystals. J. Mol. Biol. 227, 480-492 (1992).
27. Turner, G.J. et al. Mutagenic dissection of hemoglobin cooperativity: Effects of amino acid alteration on subunit assembly of oxy and deoxy tetramers. Prot. Str. Funct. Gen. 14, 333-350 (1992).
28. Römpler, H. et al. Multiplex amplifcation of ancient DNA. Nat. Protoc. 1, 720-728 (2006).
29. Barnes, I. et al. Genetic structure and extinction of the woolly mammoth, Mammuthus primigenius. Curr. Biol. 17, 1072-1075 (2007).
30. Oostenbrink, C., Villa, A., Mark, A.E. & van Gunsteren, W.F. A biomolecular force feld based on the free enthalpy of hydration and solvation: the GROMOS force-feld parameter sets 53A5 and 53A6. J. Comput. Chem. 25, 1656-1676 (2004).