Abstract
Phylogenetic analyses of the families of mammalian lung surfactant proteins (SP-A, SP-B, SP-C, and SP-D) supported the hypothesis that these proteins have diverged between birds and mammals as a result of lineage-specific gene duplications and deletions. Homologs of mammalian genes encoding SP-B, SP-C, and SP-D appear to have been deleted in chickens, whereas there was evidence of avian-specific duplications of the genes encoding SP-A and presaposin. Analysis of the genes closely linked to human SP-B, SP-C, and SP-D genes revealed that all three of these genes are closely linked to genes having orthologs on chicken chromosome 6 and also to genes lacking chicken orthologs. These relationships suggest that all of the lung surfactant protein genes, as well as certain related genes, may have been linked in the ancestor of humans and chickens. Further, they imply that the loss of surfactant protein genes in the avian lineages formed part of major genomic rearrangement events that involved the loss of other genes as well.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Bernhard W, Gebert A, Vieten A, Rau GA, Hohlfeld JM, Postle AD, Freihorst J (2001) Pulmonary surfactant in birds: coping with surface tension in a tubular lung. Am J Physiol Regul Integr Comp Physiol 281:R327–R337
Bernhard W, Haslam PL, Floros J (2004) From birds to humans: new concepts on airways relative to alveolar surfactant. Am J Respir Cell Mol Biol 30:6–11
Bruhn H (2005) A short guided tour through functional and structural features of saposin-like proteins. Biochem J 389:249–257
Daniels CB, Orgeig S (2003) Pulmonary surfactant: the key to the evolution of air breathing. News Physiol Sci 18:151–157
Daniels CB, Orgeig S, Sullivan LC, Ling N, Bennett MB, Schürch S, Val AL, Brauner CJ (2004) The origin and evolution of the surfactant system in fish: insights into the evolution of lungs and swim bladders. Physiol Biochem Zool 77:732–749
Feduccia A (1996) The origin and evolution of birds. New Haven, Yale University Press
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Hansen S, Holmskov U (2002) Lung surfactant protein D (SP-D) and the molecular diverted descendants: conglutinin, CL-43, and CL-46. Immunobiology 205:498–517
Hickling TP, Clark H, Malhotra R, Sim RB (2004) Collectins and their role in lung immunity. J Leuk Biol 75:27–33
Hiraki Y, Shukunami C (2000) Chondromodulin-I as a novel catilage-specific growth-modulating factor. Pediatr Nephrol 14:602–605
Hogenkamp A, van Eijk M, van Dik A, van Aston AJ, Veldhuisen EJ, Haagsman HP (2006) Characterization and expression sites of newly identified chicken collectins. Mol Immunol 43:1604–1616
Jones DT, Taylor WR, Thornton M (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282
Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920
Kumar S, Tamura K, Nei M (2004) MEGA3:integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Mindell DP, Sorenson MD, Dimcheff DE, Hasegawa M, Asy JC, Yuri T (1999) Interordinal relationships of birds and other reptiles based on whole mitochondrial genomes. Syst Biol 48:138–152
Possmayer F, Naga K, Rodriguez K, Quanbar R, Schurch S (2001) Surface activity in vitro: role of surfactant proteins. Comp Biochem Physiol A 129:209–220
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sano H, Kuroki Y (2005) The lung collectins, SP-A and SP-D, modulate pulmonary innate immunity. Mol Immunol 42:279–287
Scheid P, Piiper J (1971) Mechanisms of gas exchange in bird lungs. Rev Physiol Biochem Pharmacol 86:138–186
Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504
Shukunami C, Oshima Y, Hiraki Y (2001) Molecular cloning of tenomodulin, a novel Chondromodulin-I related gene. Biochem Biophys Res Commun 280:1323–1327
Strimmer K, von Haeseler A (1996) Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969
Sullivan LC, Daniels CB, Phillips AD, Orgeig S, Whitsett JA (1998) Conservation of surfactant protein A: evidence for a single origin for vertebrate pulmonary surfactant. J Mol Evol 46:131–138
Thompson JD, Higgins DG, Gibson T (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Turner MW (2003) The role of mannose-binding lectin in health and disease. Mol Immunol 40:423–429
Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Edgar R, Federhen S, Geer LY, Helmberg W, Kapustin Y, Kenton DL, Khovayko O, Lipman DJ, Madden TL, Maglott DR, Ostell J, Pruitt KD, Schuler GD, Schriml LM, Sequeira E, Sherrt ST, Sirotkin K, Souvorov A, Starchenko G, Suzek TO, Tatusov R, Tatusova TA, Wagner L, Yaschenko F (2006) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 34:D173–D180
Wright JR (2003) Immunoregulatory functions of surfactant proteins. Nature Rev Immunol 5:58–68
Acknowledgment
This research was supported by grant GM43940 from the National Institutes of Health.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Figure S1
Amino acid sequence alignments of surfactant proteins and related proteins: a surfactants A and D; b surfactant B; and c surfactant C (PDF 56 kb).
Rights and permissions
About this article
Cite this article
Hughes, A.L. Evolution of the lung surfactant proteins in birds and mammals. Immunogenetics 59, 565–572 (2007). https://doi.org/10.1007/s00251-007-0218-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00251-007-0218-6