Genetic differences in hemoglobin function between highland and lowland deer mice

Journal of Experimental Biology

Volumn 213, Issue 15, 2010, Pages 2565-2574

  Storz, Jay F ^a   Runck, Amy M ^a   Moriyama, Hideaki ^a   Weber, Roy E ^b   Fago, Angela ^b  

^a UNIVERSITY OF NEBRASKA   (United States)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

High altitude adaptation; Hypoxia; Oxygen transport; Peromyscus; Physiological genetics

Indexed keywords

CHLORIDE; HEMOGLOBIN; OXYGEN;

ALTITUDE; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; ECOSYSTEM; GENETIC POLYMORPHISM; GENETICS; GENOME; ISOELECTRIC FOCUSING; METABOLISM; MULTIGENE FAMILY; PEROMYSCUS; PH; PROTEOMICS;

ALTITUDE; AMINO ACID SEQUENCE; ANIMALS; CHLORIDES; ECOSYSTEM; GENOME; HEMOGLOBINS; HYDROGEN-ION CONCENTRATION; ISOELECTRIC FOCUSING; MULTIGENE FAMILY; OXYGEN; PEROMYSCUS; POLYMORPHISM, GENETIC; PROTEOMICS;

MAMMALIA; MUS; PEROMYSCUS; PEROMYSCUS MANICULATUS; VERTEBRATA;

EID: 77954843627     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.042598     Document Type: Article

References (62)

1. Antonini, E. and Brunori, M. (1971). Hemoglobin and Myoglobin in their Reactions ith Ligands. Amsterdam: North-Holland.
2. Bonaventura, C., Arumugam, M., Cashon, R., Bonaventura, J. and Moo-Penn, W. F. (1994). Chloride masks effects of opposing positive charges in HbA and Hb Hinsdale (β139Asn-Lys) that can modulate cooperativity as well as oxygen affinity. J. Mol. Biol. 239, 561-568. (Pubitemid 124001991)
3. Bouverot, P. (1985). Adaptation to Altitude-Hypoxia in Vertebrates. Berlin: Springer-Verlag.
4. Bunn, H. F. (1971). Differences in the interaction of 2,3-diphosphoglycerate with certain mammalian haemoglobins. Science 172, 1049-1052.
5. Bunn, H. F. (1980). Regulation of hemoglobin function in mammals. Am. Zool. 20, 199-211.
6. Bunn, H. F., Seal, U. S. and Scott, A. F. (1974). Role of 2,3-diphosphoglycerate in mediating hemoglobin function of mammalian red cells. Ann. NY Acad. Sci. 241, 498-512.
7. Chappell, M. A. and Snyder, L. R. G. (1984). Biochemical and physiological correlates of deer mouse a-chain hemoglobin polymorphisms. Proc. Natl. Acad. Sci. USA 81, 5484-5488.
8. Chappell, M. A., Hayes, J. P. and Snyder, L. R. G. (1988). Hemoglobin polymorphisms in deer mice (Peromyscus manicuiatus): physiology of β-globin variants and α-globin recombinants. Evolution 42, 681-688.
9. De Rosa, M. C., Castagnola, M., Bertonati, C., Galtieri, A. and Giardina, B. (2004). From the Arctic to fetal life: physiological importance and structural basis of an 'additional' chloride-binding site in haemoglobin. Biochem. J. 380, 889-896.
10. Eaton, W. A., Skelton, T. D. and Berger, E. (1974). Survival at extreme altitude: protective effect of increased hemoglobin affinity. Science 183, 743-744.
11. Fronticelli, C. (1990). A possible new mechanism of oxygen affinity modulation in mammalian hemoglobins. Biophys. Chem. 37, 141-146.
12. Hayashi, A., Suzuki, T. and Shin, M. (1973). An enzymatic reduction system for metmyoglobin and methemoglobin, and its application to functional studies of oxygen carriers. Biochim. Biophys. Acta 10, 309-316.
13. Hock, R. J. (1964). Physiological responses of deer mice to various native altitudes. In The Physiological Effects of High Altitude (ed. W. H. Weihe). New York: Macmillan.
14. Hoffmann, F. G., Opazo, J. C. and Storz, J. F. (2008a). Rapid rates of lineagespecific gene duplication and deletion in the α-globin gene family. Mol. Biol. Evol. 25, 591-602.
15. Hofmann, O., Carrucan, G., Robson, N. and Brittain, T. (1995). The chloride effect in the human embryonic haemoglobins. Biochem. J. 309, 959-962.
16. Jelkmann, W., Oberthur, W., Kleinschmidt, T. and Braunitzer, G. (1981). Adaptation of hemoglobin function to subterranean life in the mole, Talpa europaea. Respir. Physiol. 46, 7-16. (Pubitemid 11029886)
17. Monge, C. and León-Velarde, F. (1991). Physiological adaptation to high altitude: oxygen transport in mammals and birds. Physiol. Rev. 71, 1135-1172.
18. Nikinmaa, M. (2001). Haemoglobin function in vertebrates: evolutionary changes in cellular regulation in hypoxia. Respir. Physiol. 128, 317-329.
19. Penny, D. G. and Thomas, M. (1975). Hematological alterations and response to acute hypobaric stress. J. Appl. Physiol. 39, 1034-1037.
20. Perutz, M. F. (1983). Species adaptation in a protein molecule. Mol. Biol. Evol. 1, 1-28.
21. Perutz, M. F. (2001). Molecular anatomy and physiology of hemoglobin. In Disorders of Hemoglobin: Genetics, Pathophysiology, and Clinical Management (ed. M. H. Steinberg, B. G. Forget, D. R. Higgs and R. L. Nagel), pp. 174-196. Cambridge: Cambridge University Press.
22. Perutz, M. F., Fermi, G., Poyart, C., Pagnier, J. and Kister, J. (1993). A novel allosteric mechanism in haemoglobin: structure of bovine deoxyhaemoglobin, absence of specific chloride binding sites and origin of chloride linked Bohr effect in bovine and human haemoglobin. J. Mol. Biol. 233, 536-545. (Pubitemid 23299180)
23. Perutz, M. F., Shih, D. T. B. and Williamson, D. (1994). The chloride effect in human haemoglobin, a new kind of allosteric mechanism. J. Mol. Biol. 239, 555-560. (Pubitemid 124001990)
24. 2 affinity of animals living at high altitude. J. Appl. Physiol. 42, 139-143.
25. Piccinini, M., Kleinschmidt, T., Gorr, T., Weber, R. E., Kunzel, H. and Braunitzer, G. (1991). Primary structure and oxygen-binding properties of the hemoglobin from the lesser hedgehog tenrec (Echinops telfairi, Zalambdonta). Evidence for phylogenetic isolation. Biol. Chem. Hoppe-Seyler 372, 975-989.
26. Rasmussen, D. T., Jensen, J. N. and Koehn, R. K. (1968). Hemoglobin polymorphism in the deer mouse, Peromyscus manicuiatus. Biochem. Genet. 2, 87-92.
27. Reynafarje, C., Faura, J., Villavicencio, D., Curaca, A., Reynafarje, B., Oyola, L., Contreras, L., Vallenas, E. and Faura, A. (1975). Oxygen transport of hemoglobin in high-altitude animals (Camelidae). J. Appl. Physiol. 38, 806-810.
28. Riggs, A. F. (1988). The Bohr effect. Annu. Rev. Physiol. 50, 181-204.
29. Runck, A. M., Weber, R. E., Fago, A. and Storz, J. F. (2010). Evolutionary and functional properties of a two-locus β-globin polymorphism in Indian house mice. Genetics 184, 1121-1131.
30. Samaja, M., di Prampero, P. E. and Cerretelli, P. (1986). The role of 2,3-DPG in the oxygen transport at altitude. Respir. Physiol. 64, 191-202. (Pubitemid 16109723)
31. Samaja, M., Crespi, T., Guazzi, M. and Vandegriff, K. D. (2003). Oxygen transport in blood at high altitude: role of the hemoglobin-oxygen affinity and impact of the phenomena related to hemoglobin allosterism and red cell function. Eur. J. Biochem. 90, 351-359. (Pubitemid 37460965)
32. Sarkar, M., Pal, R. N., Das, D. N., Mondal, D. B., Mohanty, T. K. and Pattanaik, S. (1999). Postnatal persistence of foetal haemoglobin in yaks. Aust. Vet. J. 77, 190.
33. Scott, G. R. and Milsom, W. K. (2006). Flying high: a theoretical analysis of the factors limiting exercise performance in birds at altitude. Respir. Physiol. Neurobiol. 154, 284-301.
34. Shih, D. T. B., Luisi, B. F., Miyazaki, G., Perutz, M. F. and Nagai, K. (1993). A mutagenic study of the allosteric linkage of His(HC3)146B in haemoglobin. J. Mol. Biol. 230, 1291-1296.
35. Snyder, L. R. G. (1978). Genetics of hemoglobin in the deer mouse, Peromyscus manicuiatus. I. Multiple α- and β-globin structural loci. Genetics 89, 511-530. (Pubitemid 8396069)
36. Snyder, L. R. G. (1981). Deer mouse hemoglobins: Is there genetic adaptation to high altitude? Bioscience 31, 299-304.
37. Snyder, L. R. G. (1982). 2,3-diphosphoglycerate in high- and low-altitude populations of the deer mouse. Respir. Physiol. 48, 107-123. (Pubitemid 12074782)
38. 50 in deer mice native to high altitude. J. Appl. Physiol. 58, 193-199.
39. Snyder, L. R. G., Born, S. and Lechner, A. J. (1982). Blood oxygen affinity in high-and low-altitude populations of the deer mouse. Respir. Physiol. 48, 89-105. (Pubitemid 12074781)
40. Snyder, L. R. G., Chappell, M. A. and Hayes, J. P. (1988). α-chain hemoglobin polymorphisms are correlated with altitude in the deer mouse, Peromyscus manicuiatus. Evolution 42, 689-697.
41. Storz, J. F. (2007). Hemoglobin function and physiological adaptation to hypoxia in high-altitude mammals. J. Mammal. 88, 24-31.
42. Storz, J. F. and Dubach, J. M. (2004). Natural selection drives altitudinal divergence at the albumin locus in deer mice, Peromyscus manicuiatus. Evolution 58, 1342-1352.
43. Storz, J. F. and Kelly, J. K. (2008). Effects of spatially varying selection on nucleotide diversity and linkage disequilibrium: insights from deer mouse globin genes. Genetics 180, 367-379.
44. Storz, J. F. and Moriyama, H. (2008). Mechanisms of hemoglobin adaptation to high-altitude hypoxia. High Alt. Med. Biol. 9, 148-157.
45. Storz, J. F. and Nachman, M. W. (2003). Natural selection on protein polymorphism in the rodent genus Peromyscus: evidence from interlocus contrasts. Evolution 57, 2628-2635.
46. Storz, J. F., Sabatino, S. J., Hoffmann, F. G., Gering, E. J., Moriyama, H., Ferrand, N., Monteiro, B. and Nachman, M. W. (2007). The molecular basis of high-altitude adaptation in deer mice. PLoS Genet. 3, 448-459.
47. 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.
48. Storz, J. F., Runck, A. M., Sabatino, S. J., Kelly, J. K., Ferrand, N., Moriyama, H., Weber, R. E. and Fago, A. (2009). Evolutionary and functional insights into the mechanism underlying high-altitude adaptation of deer mouse hemoglobin. Proc. Natl. Acad. Sci. USA 106, 14450-14455.
49. Turek, Z., Kreuzer, F. and Hoofd, L. (1973). Advantage or disadvantage of a decrease of blood oxygen affinity for tissue oxygen supply at hypoxia. A theoretical study comparing man and rat. Pflügers Arch. 342, 185-187.
50. Turek, Z., Kreuzer, F. and Ringnalda, B. E. M. (1978a). Blood gases at several levels of oxygenation in rats with a left-shifted blood oxygen dissociation curve. flügers Arch. 376, 7-13. (Pubitemid 8390063)
51. 2 content, cardiac output, and flow to organs at several levels of oxygenation in rats with a left-shifted blood oxygen dissociation curve. Pflügers Arch. 376, 201-207.
52. 2 affinity in lugworm erythrocruorin. Nature 292, 386-387.
53. Weber, R. E. (1992). Use of ionic and zwitterionic (Tris/BisTris and Hepes) buffers in studies on hemoglobin function. J. Appl. Physiol. 72, 1611-1615.
54. Weber, R. E. (2007). High-altitude adaptations in vertebrate hemoglobins. Respir. Physiol. Neurobiol. 158, 132-142.
55. Weber, R. E. and Fago, A. (2004). Functional adaptation and its molecular basis in vertebrate hemoglobins, neuroglobins and cytoglobins. Respir. Physiol. Neurobiol. 144, 141-159.
56. Weber, R. E. and White, F. N. (1994). Chloride-dependent organic phosphate sensitivity of the oxygenation reaction in crocodilian hemoglobins. J. Exp. Biol. 192, 1-11.
57. Weber, R. E., Lalthantluanga, R. and Braunitzer, G. (1988). Functional characterization of fetal and adult yak hemoglobins: an oxygen binding cascade and its molecular basis. Arch. Biochem. Biophys. 263, 199-203.
58. 55-Ser)-functions related to high-altitude respiration in geese. J. Appl. Physiol. 75, 2646-2655.
59. 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 Hoplostemum littorale. J. Biol. Chem. 275, 17297-17305.
60. Weber, R. E., Ostojic, H., Fago, A., Dewilde, S., Van Hauwaert, M. L., Moens, L. and Monge, C. (2002). Novel mechanism for high-altitude adaptation in hemoglobin of the Andean frog Telmatobius peruvianus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283, R1052-R1060.
61. Weber, R. E., Fago, A., Bang, A., Voelter, W. and Low, S. P. (2004). Modulation of red cell glycolysis: Interaction between vertebrate hemoglobins and cytoplasmic domains of band 3 red cell membrane proteins. Am. J. Physiol. 287, R454-R464.
62. Zheng, T., Brittain, T., Watmough, N. J. and Weber, R. E. (1999). The role of amino acid α38 in the control of oxygen binding to human adult and embryonic haemoglobin Portland. Biochem. J. 343, 681-685. (Pubitemid 29537382)