Purifying selection drives the evolution of surfactant protein C (SP-C) independently of body temperature regulation in mammals

Comparative Biochemistry and Physiology - Part D: Genomics and Proteomics

Volumn 2, Issue 2, 2007, Pages 165-176

  Potter, Sally ^a   Orgeig, Sandra ^a   Donnellan, Stephen ^a,b   Daniels, Christopher B ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b SOUTH AUSTRALIAN MUSEUM   (Australia)

Author keywords

Heterothermy; Mammalian evolution; Phylogenetic analysis by maximum likelihood; Positive selection; Pulmonary surfactant; Surfactant protein C

Indexed keywords

CHOLESTEROL; GENOMIC DNA; LIPID; LUNG SURFACTANT; SURFACTANT PROTEIN C;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BAYES THEOREM; BEAR; BODY TEMPERATURE; CODON USAGE; CONTROLLED STUDY; EVOLUTION; GENETIC CONSERVATION; GENETIC SELECTION; LIPID COMPOSITION; MAMMAL; MAXIMUM LIKELIHOOD METHOD; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PURIFICATION; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; TEMPERATURE ACCLIMATIZATION; THERMOREGULATION;

MAMMALIA; URSUS AMERICANUS;

EID: 34247495251     PISSN: 1744117X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbd.2007.02.003     Document Type: Article

References (88)

1. Augee M.L., and Gooden B.A. Monotreme hibernation-Some afterthoughts. In: Augee M.L. (Ed). Platypus and Echidnas (1992), Royal Zoological Society of New South Wales, Sydney 174-176
2. Baatz J.E., Smyth K.L., Whitsett J.A., Baxter C.F., and Absolom D.R. Structure and functions of a dimeric form of surfactant protein SP-C: a Fourier transform infrared and surfactometry study. Chem. Phys. Lipids 63 (1992) 91-104
3. Beers M.F., and Mulugeta S. Surfactant protein C biosynthesis and its emerging role in conformational lung disease. Annu. Rev. Physiol. 67 (2005) 663-696
4. Bininda-Emonds O.R., Gittleman J.L., and Purvis A. Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol. Rev. Camb. Philos. Soc. 74 (1999) 143-175
5. Cardillo M., Bininda-Emonds O.R., Boakes E., and Purvis A. A species-level phylogenetic supertree of marsupials. J. Zool. (Lond.) 264 (2004)
6. Codd J.R., Slocombe N.C., Daniels C.B., Wood P.G., and Orgeig S. Periodic fluctuations in the pulmonary surfactant system in Gould's wattled bat (Chalinolobus gouldii). Physiol. Biochem. Zool. 73 (2000) 605-612
7. Codd J.R., Schürch S., Daniels C.B., and Orgeig S. Torpor-associated fluctuations in surfactant activity in Gould's wattled bat. Biochim. Biophys. Acta 1580 (2002) 57-66
8. Codd J.R., Orgeig S., Daniels C.B., and Schurch S. Alterations in surface activity of pulmonary surfactant in Gould's wattled bat during rapid arousal from torpor. Biochem. Biophys. Res. Commun. 308 (2003) 463-468
9. Conkright J.J., Na C.L., and Weaver T.E. Overexpression of surfactant protein-C mature peptide causes neonatal lethality in transgenic mice. Am. J. Respir. Cell Mol. Biol. 26 (2002) 85-90
10. Creuwels L.A., Demel R.A., van Golde L.M., and Haagsman H.P. Characterization of a dimeric canine form of surfactant protein C (SP-C). Biochim. Biophys. Acta 1254 (1995) 326-332
11. Creuwels L.A.J.M., Van Golde L.M.G., and Haagsman H.P. The pulmonary surfactant system: biochemical and clinical aspects. Lung 175 (1997) 1-39
12. Curstedt T., Johansson J., Persson P., Eklund A., Robertson B., Löwenadler B., and Jörnvall H. Hydrophobic surfactant-associated polypeptides: SP-C is a lipopeptide with two palmitoylated cysteine residues, whereas SP-B lacks covalently linked fatty acyl groups. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 2985-2989
13. Daniels C.B., and Orgeig S. Pulmonary surfactant: the key to the evolution of air breathing. News Physiol. Sci. 18 (2003) 151-157
14. Daniels C.B., Lopatko O.V., and Orgeig S. Evolution of surface activity related functions of vertebrate pulmonary surfactant. Clin. Exp. Pharmacol. Physiol. 25 (1998) 716-721
15. Dausmann K.H., Ganzhorn J.U., and Heldmaier G. Body temperature and metabolic rate of a hibernating primate in Madagascar: preliminary results from the field study. In: Heldmaier G., and Klingenspor M. (Eds). Life in the cold: eleventh international hibernation symposium (2000), Springer, Berlin 41-47
16. Fons R., Sender S., Peters T., and Jurgens K.D. Rates of rewarming, heart and respiratory rates and their significance for oxygen transport during arousal from torpor in the smallest mammal, the Etruscan shrew Suncus etruscus. J. Exp. Biol. 200 (1997) 1451-1458
17. Foot, N.J., Orgeig, S., Donnellan, S.C., Bertozzi, T., Daniels, C.B., in press. Positive selection in the N-terminal extramembrane domain of lung surfactant protein C (SP-C) in marine mammals. J. Mol. Evol.
18. Geiser F. Temperature regulation in heterothermic marsupials. In: Heller H.C., Musacchia X.J., and Wang L.C.H. (Eds). Living in the Cold: Physiological and Biochemical Adaptations (1986), Elsevier Science Publishing Company, New York 207-212
19. Geiser F. Evolution of daily torpor and hibernation in birds and mammals: importance of body size. Clin. Exp. Pharmacol. Physiol. 25 (1998) 736-739
20. Geiser, F., 2001. Hibernation: Endotherms. Encyclopedia of Life Sciences. Macmillan Publishers Ltd, Nature Publishing Group.
21. Geiser F. Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66 (2004) 239-274
22. Geiser F., and Baudinette R.V. The influence of temperature and photophase on daily torpor in Sminthopsis macroura (Dasyuridae: Marsupialia). J. Comp. Physiol., B 156 (1985) 129-134
23. Geiser F., and Kortner G. Thermal biology, energetics, and torpor in the possums and gliders. In: Goldingay R.L., and Jackson S.M. (Eds). The Biology of Australian Possums and Gliders (2004), Surrey Beatty and Sons, Chipping Norton 186-198
24. Geiser F., and Ruf T. Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol. Zool. 68 (1995) 935-966
25. Geiser F., Coburn D.K., Kortner G., and Law B.S. Thermoregulation, energy metabolism, and torpor in blossom-bats, Syconycteris australis (Megachiroptera). J. Zool. (Lond.) 239 (1996) 583-590
26. Gemmell R.T., Turner S.J., and Krause W.J. The circadian rhythm of body temperature of four marsupials. J. Therm. Biol. 22 (1997) 301-307
27. Glasser S.W., Burhans M.S., Korfhagen T.R., Na C.L., Sly P.D., Ross G.F., Ikegami M., and Whitsett J.A. Altered stability of pulmonary surfactant in SP-C-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 6366-6371
28. Glasser S.W., Detmer E.A., Ikegami M., Na C.L., Stahlman M.T., and Whitsett J.A. Pneumonitis and emphysema in SP-C gene targeted mice. J. Biol. Chem. 278 (2003) 14291-14298
29. Greyner R., and Purvis A. A composite species-level phylogeny of the 'Insectivora' (Mammalia: Order Lipotyphla Haeckel, 1866). J. Zool. (Lond.) 260 (2003) 245-257
30. Grigg G.C., Beard L.A., Barnes J.A., Perry L.I., Fry G.J., and Hawkins M. Body temperature in captive long-beaked echidnas (Zaglossus bartoni). Comp. Biochem. Physiol., A 136 (2003) 911-916
31. Grigg G.C., Beard L.A., and Augee M.L. The evolution of endothermy and its diversity in mammals and birds. Physiol. Biochem. Zool. 77 (2004) 982-997
32. Haagsman H.P., and Diemel R.V. Surfactant-associated proteins: functions and structural variation. Comp. Biochem. Physiol., A 129 (2001) 91-108
33. Horwitz B.A., and Nelson L. Effect of temperature on mitochondrial respiration in a hibernator (Myotis austroriparius) and a non-hibernator (Rattus rattus). Comp. Biochem. Physiol. 24 (1968) 385-394
34. Hosken D.J., and Withers P.C. Temperature regulation and metabolism of an Australian bat, Chalinolobus gouldii (Chiroptera: Vespertilionidae) when euthermic and torpid. J. Comp. Physiol., B 167 (1997) 71-80
35. Huelsenbeck J.P., and Dyer K.A. Bayesian estimation of positively selected sites. J. Mol. Evol. 58 (2004) 661-672
36. Inoue H., Inoue C., and Hildebrandt J. Temperature and surface forces in excised rabbit lungs. J. Appl. Physiol. 51 (1981) 823-829
37. Inoue H., Inoue C., and Hildebrandt J. Temperature and surface forces in excised rabbit lungs. J. Appl. Physiol. 51 (1982) 823-829
38. Johansson J. Structure and properties of surfactant protein C. Biochim. Biophys. Acta 1408 (1998) 161-172
39. Johansson J., Persson P., Lowenadler B., Robertson B., Jornvall H., and Curstedt T. Canine hydrophobic surfactant polypeptide SP-C. A lipopeptide with one thioester-linked palmitoyl group. FEBS Lett. 281 (1991) 119-122
40. Lang C.J., Daniels C.B., and Orgeig S. New insights into the thermal dynamics of the surfactant system from warm and cold animals. In: Nag K. (Ed). Lung Surfactant Function and Disorder vol. 201 (2005), Taylor and Francis, Boca Raton 17-57
41. Langman C., Orgeig S., and Daniels C.B. Alterations in composition and function of surfactant associated with torpor in Sminthopsis crassicaudata. Am. J. Physiol. 271 (1996) R437-R445
42. Li W.H. Roles of selection and mutation in molecular evolution. In: Li M.A. (Ed). Molecular Evolution (1997), Sinauer Associates, Sunderland 419-432
43. Maddison W.P., and Maddison D.R. Mesquite: A Modular System for Evolutionary Analysis. Vers. 1.05 (2004)
44. McNab B.K. Uniformity in the basal metabolic rate of marsupials: its causes and consequences. Rev. Chil. Hist. Nat. 78 (2005) 183-198
45. McNab B.K., and Armstrong M.I. Sexual dimorphism and scaling of energetics in flying foxes of the genus Pteropus. J. Mammal. 82 (2001) 709-720
46. McNab B.K., and Bonaccorso F.J. The metabolism of New Guinean pteropodid bats. J. Comp. Physiol., B 171 (2001) 201-214
47. Melton K.R., Nesslein L.L., Ikegami M., Tichelaar J.W., Clark J.C., Whitsett J.A., and Weaver T.E. SP-B deficiency causes respiratory failure in adult mice. Am. J. Physiol., Lung Cell. Mol. Physiol. 285 (2003) L543-L549
48. Milsom W.K., and Reid W.D. Pulmonary mechanics of hibernating squirrels (Spermophilus lateralis). Respir. Physiol. 101 (1995) 311-320
49. Montgelard C., Bentz S., Tirard C., Verneau O., and Catzeflis F.M. Molecular systematics of Sciurognathi (Rodentia): the mitochondrial cytochrome b and 12S rRNA genes support the Anomaluroidea (Pedetidae and Anomaluridae). Mol. Phylogenet. Evol. 22 (2002) 220-233
50. Mulugeta S., and Beers M.F. Processing of surfactant protein C requires a type II transmembrane topology directed by juxtamembrane positively charged residues. J. Biol. Chem. 278 (2003) 47979-47986
51. Murphy W.J., Eizirik E., Johnson W.E., Zhang Y.P., Ryder O.A., and O'Brien S.J. Molecular phylogenetics and the origins of placental mammals. Nature 409 (2001) 614-618
52. Na Nakorn P., Meyer M.C., Flach C.R., Mendelsohn R., and Galla H.J. Surfactant protein C and lung function: new insights into the role of alpha-helical length and palmitoylation. Eur. Biophys. J. (2006) 10.1007/s00249-006-0102-6
53. Nagel A. Development of temperature regulation in the common white-toothed shrew, Crocidura russula. Comp. Biochem. Physiol., A 92 (1989) 409-413
54. Nielsen R., and Yang Z. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148 (1998) 929-936
55. Nogee L.M., Dunbar III A.E., Wert S., Askin F., Hamvas A., and Whitsett J.A. Mutations in the surfactant protein C gene associated with interstitial lung disease. Chest 121 (2002) 20S-21S
56. Oosterlaken Dijksterhuis M.A., van Eijk M., van Buel B.L., van Golde L.M., and Haagsman H.P. Surfactant protein composition of lamellar bodies isolated from rat lung. Biochem. J. 274 (1991) 115-119
57. Palmer S., Nelson R., Ramsay M., Stirling I., and Bahr J. Annual changes in serum sex steroids in male and female black (Ursus americanus) and polar (Ursus maritimus) bears. Biol. Reprod. 38 (1988) 1044-1050
58. Pereira M.E., Aines J., and Scheckter J.L. Tactics of heterothermy in eastern gray squirrels (Sciurus carolinensis). J. Mammal. 83 (2002) 467-477
59. Perez-Gil J., and Keough K.M. Interfacial properties of surfactant proteins. Biochim. Biophys. Acta 1408 (1998) 203-217
60. Plasencia I., Cruz A., Casals C., and Perez-Gil J. Superficial disposition of the N-terminal region of the surfactant protein SP-C and the absence of specific SP-B-SP-C interactions in phospholipid bilayers. Biochem. J. 359 (2001) 651-659
61. Possmayer F., Nag K., Rodriguez K., Qanbar R., and Schurch S. Surface activity in vitro: role of surfactant proteins. Comp. Biochem. Physiol., A 129 (2001) 209-220
62. Poux C., and Douzery J.P. Primate phylogeny, evolutionary rate variations, and divergence times: a contribution from the nuclear gene IRBP. Am. J. Phys. Anthropol. 124 (2004) 1-16
63. Ramsay M.A., Nelson R.A., and Stirling I. Seasonal-changes in the ratio of serum urea to creatinine in feeding and fasting polar bears. Can. J. Zool. 69 (1991) 298-302
64. Rocha E.P.C. Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res. 14 (2004) 2279-2286
65. Ronquist F., and Huelsenbeck J.P. MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003) 1572-1574
66. Schürch S., and Bachofen H. Biophysical aspects in the design of a therapeutic surfactant. In: Robertson B., and Teausch H.W. (Eds). Surfactant Therapy for Lung Disease (1995), Marcel Dekker 3-32
67. Schürch S., Qanbar R., Bachofen H., and Possmayer F. The surface-associated surfactant reservoir in the alveolar lining. Biol. Neonate 67 (1995) 61-76 (suppl)
68. Serrano A.G., and Perez-Gil J. Protein-lipid interactions and surface activity in the pulmonary surfactant system. Chem. Phys. Lipids 141 (2006) 105-118
69. Silva M., and Downing J.A. CRC Handbook of Mammalian Body Mass (1995), CRC Press, Boca Raton
70. Suzuki Y., and Gojobori T. A method for detecting positive selection at single amino acid site. Mol. Biol. Evol. 16 (1999) 1315-1328
71. Teeling E., Springer M., Madsen O., Bates P., O'Brien S., and Murphy W. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307 (2005) 580-584
72. ten Brinke A., Batenburg J.J., Gadella B.M., Haagsman H.P., Vaandrager A.B., and van Golde L.M.G. The juxtamembrane lysine and arginine residues of surfactant protein C precursor influence palmitoylation via effects on trafficking. Am. J. Respir. Cell Mol. Biol. 25 (2001) 156-163
73. ten Brinke A., Batenburg J.J., Haagsman H.P., van Golde L.M., and Vaandrager A.B. Differential effect of brefeldin A on the palmitoylation of surfactant protein C proprotein mutants. Biochem. Biophys. Res. Commun. 290 (2002) 532-538
74. ten Brinke A., van Golde L.M., and Batenburg J.J. Palmitoylation and processing of the lipopeptide surfactant protein C. Biochim. Biophys. Acta 1583 (2002) 253-265
75. Tourasse N.J., and Li W.H. Selective constraints, amino acid composition, and the rate of protein evolution. Mol. Biol. Evol. 17 (2000) 656-664
76. Turbill C., Law B.S., and Geiser F. Summer torpor in a free-ranging bat from subtropical Australia. J. Therm. Biol. 28 (2003) 223-226
77. Wang L.C.H. Ecological, physiological and biochemical aspects of torpor in mammals and birds. In: Wang L.C.H. (Ed). Advances in Comparative and Environmental Physiology vol. 4 (1989), Springer, Heidelberg 361-401
78. Weaver T.E. Synthesis, processing and secretion of surfactant proteins B and C. Biochim. Biophys. Acta 1408 (1998) 173-179
79. Willis C.K.R., Turbill C., and Geiser F. Torpor and thermal energetics in a tiny Australian vespertillonid, the little forest bat (Vespadelus vulturnus). J. Comp. Physiol., B 175 (2005) 479-486
80. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13 (1997) 555-556
81. Yang Z. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15 (1998) 568-573
82. Yang Z. PAML Manual. Vers. 3.14 (2004)
83. Yang Z., and Bielawski J.P. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15 (2000) 496-503
84. Yang Z., and Nielsen R. Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J. Mol. Evol. 46 (1998) 409-418
85. Yang Z., Nielsen R., Goldman N., and Pedersen A.M. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155 (2000) 431-449
86. Yang Z., Swanson W.J., and Vacquier V.D. Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites. Mol. Biol. Evol. 17 (2000) 1446-1455
87. Young R.A. The eastern horseshoe bat, Rhinolophus megaphyllus, in south-east Queensland, Australia: colony demography and dynamics, activity levels, seasonal weight changes, and capture-recapture analyses. Wildl. Res. 28 (2001) 425-434
88. Zhang J. Rates of conservative and radical nonsynonymous nucleotide substitutions in mammalian nuclear genes. J. Mol. Evol. 50 (2000) 56-68