Molecular basis of a novel adaptation to hypoxic-hypercapnia in a strictly fossorial mole

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Campbell, Kevin L ^a   Storz, Jay F ^b   Signore, Anthony V ^a   Moriyama, Hideaki ^b   Catania, Kenneth C ^c   Payson, Alexander P ^d   Bonaventura, Joseph ^d   Stetefeld, Jörg ^a   Weber, Roy E ^e  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF NEBRASKA   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d DUKE UNIVERSITY   (United States)

^e AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BLOOD; FOSSIL RECORD; HYPOXIA; MOLECULAR ANALYSIS; OXYGEN; PALEOECOLOGY; PHYSIOLOGICAL RESPONSE; SURVIVAL;

INSECTIVORA; MAMMALIA; SCALOPUS; SCALOPUS AQUATICUS; VERTEBRATA;

CARBON DIOXIDE; HEMOGLOBIN; ISOPROTEIN; OXYGEN;

ADAPTATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL; ANOXIA; ARTICLE; BLOOD; CHEMICAL STRUCTURE; DNA SEQUENCE; GENE LIBRARY; GENETICS; HYPERCAPNIA; METABOLISM; MOLE (INSECTIVORA); MOLECULAR GENETICS; PHENOTYPE; PHYLOGENY;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANOXIA; CARBON DIOXIDE; GENE LIBRARY; HEMOGLOBINS; HYPERCAPNIA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLES; OXYGEN; PHENOTYPE; PHYLOGENY; PROTEIN ISOFORMS; SEQUENCE ANALYSIS, DNA;

EID: 77954550402     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-214     Document Type: Article

References (62)

1. The ecological significance of certain new haematological findings in the mole and hedgehog. TA Quilliam A Clarke AJ Salsbury, Comp Biochem Physiol A 1971 40 89 102 10.1016/0300-9629(71)90150-2 4401112
2. Concentrations of carbon dioxide and oxygen in mole tunnels. VH Schaefer RMFS Sadleir, Acta Theriol 1979 24 267 276
3. Comparative studies of the respiratory function of mammalian blood. V. Insectivora: shrew, mole and nonhibernating and hibernating hedgehog. H Bartels R Schmelzle S Ulrich, Respir Physiol 1969 7 278 286 10.1016/0034-5687(69)90011-5 5823837
4. Adaptation of hemoglobin function to subterranean life in the mole, Talpa europaea. W Jelkmann W Oberthür T Kleinschmidt G Braunitzer, Respir Physiol 1981 46 7 16 10.1016/0034-5687(81)90064-5 7330493 (Pubitemid 11029886)
5. Die primärstruktur des hämoglobins des maulwurfs (Talpa europaea). T Kleinschmidt W Jelkmann G Braunitzer, Hoppe-Seyler's Z Physiol Chem 1981 362 1263 1272 7346384
6. Molecular phylogenetic relationships of moles, shrew moles, and desmans from the new and old worlds. A Shinohara KL Campbell H Suzuki, Mol Phylogenet Evol 2003 27 247 258 10.1016/S1055-7903(02)00416-5 12695089
7. Phylogenetic relationships with the Family Talpidae (Mammalia: Insectivora). M Motokawa, J Zool 2004 263 147 157 10.1017/S0952836904004972 (Pubitemid 38681784)
8. Comparative mycology of moles and the phylogeny of the Talpidae (Mammalia, Lipotyphla). HP Whidden, Am Museum Novitates 2000 3294 1 53 10.1206/0003-0082(2000)3294<0001:CMOMAT>2.0.CO;2
9. From the Arctic to fetal life: physiological importance and structural basis of an 'additional' chloride-binding site in haemoglobin. MC De Rosa M Castagnola C Bertonati A Galtier B Giardina, Biochem J 2004 380 889 896 10.1042/BJ20031421 14979874
10. Blood oxygen affinity and alveolar ventilation in relation in body weight in mammals. S Lahiri, Am J Physiol 1975 229 529 536 240284
11. Mechanism of deamidation in haemoglobin Providence Asn. MF Perutz JH Fogg JA Fox, J Mol Biol 1980 138 669 670 10.1016/S0022-2836(80)80023-4 7411621
12. Posttranslational deamidation of proteins: the case of hemoglobin J Sardegna [50(CD8)HisAsnAsp]. R Paleari E Paglietti A Mosca M Mortarino L Maccioni S Satta A Cao R Galanello, Clin Chem 1999 45 21 28 9895333
13. Differential loss of embryonic globin genes during the radiation of placental mammals. JC Opazo FG Hoffmann JF Storz, Proc Natl Acad Sci USA 2008 105 12950 12955 10.1073/pnas.0804392105 18755893
14. Origin and ascendency of a chimeric fusion gene: the /-globin gene of paenungulate mammals. JC Opazo AM Sloan KL Campbell JF Storz, Mol Biol Evol 2009 26 1469 1478 10.1093/molbev/msp064 19332641
15. Hedgehogs, shrews, moles, and solenodons (Eulipothyphla). CJ Douady EJP Douzery, The Timetree of Life Oxford University Press, Hedges SB, Kumar S, 2009 495 498
16. Differences in the interaction of 2,3-diphosphoglycerate with certain mammalian hemoglobins. HF Bunn, Science 1971 172 1049 1050 10.1126/science.172. 3987.1049 5573955
17. Species adaptation in a protein molecule. MF Perutz, Mol Biol Evol 1983 1 1 28 6400645
18. A novel allosteric mechanism in haemoglobin: structure of bovine deoxyhaemoglobin, absence of specific chloride-binding sites and origin of the chloride-linked Bohr effect. MF Perutz G Fermi C Poyart J Pagnier J Kister, J Mol Biol 1993 232 536 545 10.1006/jmbi.1993.1530 (Pubitemid 23299180)
19. Regulation of oxygen affinity of mammalian haemoglobins. MF Perutz K Imai, J Mol Biol 1980 138 649 670 10.1016/S0022-2836(80)80022-2 7411620
20. 2136(H14)GlyAsp). J Thillet J Caburi B Brun M Cohen-Solal MC Garel M N'Go Minh J Rosa, FEBS Letts 1974 47 47 52 10.1016/0014-5793(74)80423-0
21. Hb Hope, 136(H14)GlyAsp, in a diabetic Japanese female and its functional characterization. Y Enoki Y Ogha K Furukawa A Takaya S Sakata H Kohzuki S Shimizu T Tsujii, Hemoglobin 1989 13 17 32 10.3109/03630268908998050 2703363
22. Molecular pathology of human haemoglobin. MF Perutz H Lehmann, Nature 1968 219 902 909 10.1038/219902a0 5691676
23. The carbon dioxide affinity of various human hemoglobins. C Bauer R Baumann U Engels B Pacyna, J Biol Chem 1975 250 2173 2176 234958
24. Hemoglobin Hope: studies of oxygen equilibrium in heterozygotes, hemoglobin S-Hope disease, and isolated hemoglobin Hope. MH Steinberg WJ Lovell S Wells M Coleman BJ Dreiling JG Adams, J Lab Clin Med 1976 88 125 131 932531
25. Hemoglobin Hope: a beta-chain variant. V Minnich RJ Hill PD Khuri ME Anderson, Blood 1965 25 830 838 14282052
26. Determination of the pK values for the alpha-amino groups of human hemoglobin. MH Garner RA Bogardt Jr FR Gurd, J Biol Chem 1975 250 4398 4404 237898
27. The carbamate equilibrium of - and -amino groups of human hemoglobin at 37°C. G Gros HS Rollema RE Forster, J Biol Chem 1981 256 5471 5480 6165715
28. Hemoglobin Raleigh (1 valineacetylalanine). Structural and functional characterization. WF Moo-Penn KC Bechtel RM Schmidt MH Johnson DL Jue DE Schmidt WM Dunlap SJ Opella J Bonaventura C Bonaventura, Biochemistry 1977 16 4872 4879 10.1021/bi00641a019 20942
29. Hb Fukuoka [2 (NA2) HisTyr]: a new mutation at the 2,3-diphosphoglycerate binding site. T Harano K Harano S Ueda K Imai A Ohkuma Y Koya H Takahashi, Hemoglobin 1990 14 199 205 10.3109/03630269009046961 2272842
30. Hemoglobin Little Rock (143 (H21) HisGln). Effects of an amino acid substitution at the 2,3-diphosphoglycerate binding site. GH Bare JO Alben PA Bromberg RT Jones B Brimhall F Padilla, J Biol Chem 1974 249 773 779 4811903
31. Anionic control of function in vertebrate hemoglobins. C Bonaventura J Bonaventura, Am Zool 1980 20 131 138
32. Hemoglobin Rahere, a human hemoglobin variant with amino acid substitution at the 2,3-diphosphoglycerate binding site. Functional consequences of the alteration and effects of bezafibrate on the oxygen bindings. J Sugihara T Imamura S Nagafuchi J Bonaventura C Bonaventura R Cashon, J Clin Invest 1985 76 1169 1173 10.1172/JCI112072 3930571
33. Hemoglobin Providence. Functional consequences of two alterations of the 2,3-diphosphoglycerate binding site at position beta 82. J Bonaventura C Bonaventura B Sullivan G Ferruzzi PR McCurdy J Fox WF Moo-Penn, J Biol Chem 1976 251 7563 7571 12172
34. Structure of human foetal deoxyhaemoglobin. JA Frier MF Perutz, J Mol Biol 1977 112 97 112 10.1016/S0022-2836(77)80158-7 881729
35. Hemoglobin: Structure, function, evolution, and pathology. RE Dickerson I Geis, Menlo Park: Benjamin/Cummings Publishing Company 1983
36. The reaction between diphosphoglycerate and hemoglobin. RE Benesch R Benesch, Fed Proc 1970 29 1101 1104 5443776
37. Oxygen transport in the blood of arctic mammals: adaptation to local heterothermia. O Brix A Bårdgard S Matheisen N Tyler M Nuutinen SG Condo B Giardina, J Comp Physiol B 1990 159 665 660 10.1007/BF00691710
38. Hemoglobin structure and function. RE Weber RMG Wells, Lung Biology in Health and Disease. Comparative Pulmonary Physiology, Current Concepts New York: Marcel Dekker, Inc, Wood SC, 1989 279 310
39. Hemoglobin: Molecular, Genetic and Clinical Aspects. HF Bunn BG Forget, Philadelphia: W.B. Saunders Company 1986
40. Mammals in the highlands of southern Peru. OP Pearson, Bull Mus Comp Zool 1951 106 1 174
41. Seasonal changes in haematological and respiratory properties of muskrat (Ondatra zibethicus) blood. RA MacArthur, Can J Zool 1984 62 537 545 10.1139/z84-080
42. The specific influence of carbon dioxide and carbamate compounds on the buffer power and Bohr effects of human haemoglobin solutions. L Rossi-Bernardi FJW Roughton, J Physiol 1967 189 1 29 16992238
43. Specifically carboxymethylated hemoglobin as an analogue of carbamino hemoglobin. Solution and X-ray studies of carboxymethylated hemoglobin and X-ray studies of carbamino hemoglobin. WJ Fantl A Di Donato JM Manning PH Rogers A Arnone, J Biol Chem 1987 262 12700 12713 3114261
44. Carbon dioxide transport in alligator blood and its erythrocyte permeability to anions and water. FB Jensen T Wang DR Jones J Brahm, Am J Physiol 1998 274 661 R671 9530231
45. Body oxygen stores, aerobic dive limits and diving behaviour of the star-nosed mole (Condylura cristata) and comparisons with non-aquatic talpids. IW McIntyre KL Campbell RA MacArthur, J Exp Biol 2002 205 45 54 11818411
46. The life history and ecology of Townsend's mole Scapanus townsendii (Bachman) in Tillamook County Oregon. RJ Pedersen, MSc thesis. Oregon State University, Biology Department 1963
47. Simplified method for the determination of myoglobin. B Reynafarje, J Lab Clin Med 1963 61 138 145
48. Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. MA Castellini GN Somero, J Comp Physiol B 1981 143 191 198
49. Preferential hemolysis of postnatal calf red cells induced by internal alkanlinization. R Zeidler HD Kim, J Gen Physiol 1977 70 385 401 10.1085/jgp.70.3.385 19557
50. Veterinary hematology. OW Schalm NC Jain EJ Carroll, Philadelphia: Lea and Febiger 3 1975
51. Use of ionic and zwitterionic (Tris/BisTris and HEPES) buffers in studies on hemoglobin function. RE Weber, J Appl Physiol 1992 72 1611 1615 1592755
52. Thin-layer methods for determination of oxygen binding curves of hemoglobin solutions and blood. GN Lapennas JM Colacino J Bonaventura, Methods Enzymol 1981 76 449 470 full-text 7329270
53. Fasting metabolism and thermoregulatory competence of the star-nosed mole, Condylura cristata (Talpidae: Condylurinae). KL Campbell IW McIntyre RA MacArthur, Comp Biochem Physiol A 1999 123 293 298 10.1016/S1095-6433(99)00065-3 (Pubitemid 29395576)
54. 2dissociation computations. JW Severinghaus, J Appl Physiol 1979 46 599 602 35496
55. Magnetic bead capture of cDNAs from double-stranded plasmid cDNA libraries. AR Shepard JL Rae, Nucl Acids Res 1997 25 3183 3185 10.1093/nar/25.15.3183 9224622
56. A chain having two substitutions, one being that of Hb F-Sardinia. M Pirastru L Manca M Palici di Suni SM Speziga B Masala, Hemoglobin 2004 28 297 303 10.1081/HEM-200038868 15666429
57. Protein-protein interactions of tandem affinity purification-tagged protein kinases in rice. JS Rohila M Chen J Chen R Cerny C Dardick P Canlas X Xu M Gribskov S Kanrar J-K Zhu P Ronald ME Fromm, Plant J 2006 46 1 13 10.1111/j.1365-313X.2006.02671.x 16553892
58. Conserved sequences of sperm-activating peptide and its receptor throughout evolution, despite speciation in the sea star Asterias amurensis and closely related species. M Nakachi M Hoshi M Matsumoto H Moriyama, Zygote 2008 16 229 237 10.1017/S0967199408004759 18578950
59. MUSCLE: multiple sequence alignment with high accuracy and high throughput. RC Edgar, Nucl Acids Res 2004 32 1792 1797 10.1093/nar/gkh340 15034147
60. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. G Jobb A von Haeselern K Strimmer, BMC Evol Biol 2004 4 18 10.1186/1471-2148-4-18 15222900
61. A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6. C Oostenbrink A Villa AE Mark WF van Gunsteren, J Comput Chem 2004 25 1656 1676 10.1002/jcc.20090 15264259
62. DINO: Visualizing Structural Biology. A Philippsen, University of Basal 2002 http://www.dino3d.org