Abstract
Carbonic anhydrase-related protein XI (CA-RP XI) is a member of the α-carbonic anhydrase family (encoded by the gene CA-11), which has lost features of the active site required for enzymatic activity. Using PCR, we amplified CA-11 from genomic DNA of the bat Megaderma lyra. To elucidate the gene structure, we sequenced PCR products and compared their sequences with genomic and mRNA sequences known from human and domestic pig. We identified and sequenced eight introns in the bat CA-11. Five introns (introns 3–7) are located in identical or similar positions in other members of the vertebrate α-carbonic anhydrase gene family. Two 5′ introns and one 3′ intron are located in the regions of little or no sequence similarity with other members of the gene family. The low sequence similarity and additional introns suggest a separate evolutionary origin for the 5′ and 3′ portions of the CA-RP XI gene.
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References
Aspatwar A, Tolvanen MEE, Parkkila S (2010) Phylogeny and expression of carbonic anhydrase-related proteins. BMC Mol Biol 11:25
Aspatwar A, Tolvanen MEE, Parkkila S (2013) An update on carbonic anhydrase-related proteins VIII, X and XI. J Enzym Inhib Med Chem (in press)
Bellingham J, Gregory-Evans K, Gregory-Evans CY (1998) Sequence and tissue expression of a novel human carbonic anhydrase-related protein, CARP-2, mapping to chromosome 19q13.3. Biochem Biophys Res Commun 253:364–367
Chegwidden WR, Carter ND (2000) Introduction to the carbonic anhydrases. In: Chegwidden WR, Carter ND, Edwards YH (eds) The carbonic anhydrases: new horizons. Birkhäuser, Basel, pp 13–28
Fujikawa-Adachi K, Nishimori I, Taguchi T, Yuri K, Onshi S (1999) cDNA sequence, mRNA expression, and chromosomal localization of human carbonic anhydrase-related protein, CA-RP XI. Biochim Biophys Acta 1431:518–524
Hewett-Emmett D (2000) Evolution and distribution of the carbonic anhydrase gene families. In: Chegwidden WR, Carter ND, Edwards YH (eds) The carbonic anhydrases: new horizons. Birkhäuser, Basel, pp 29–76
Hewett-Emmett D, Tashian RE (1991) Structure and evolutionary origins of the carbonic anhydrase multigene family. In: Dodgson SJ, Tashian RE, Gros G, Carter ND (eds) The carbonic anhydrases: cellular physiology and molecular genetics. Plenum Press, New York, pp 13–32
Hewett-Emmett D, Tashian RE (1996) Functional diversity, conservation, and convergence in the evolution of the α-, β-, and γ-carbonic anhydrase gene families. Mol Phylogenet Evol 5:50–77
Hood CS, Schlitter DA, Georgudaki JI, Yenbutra SY, Baker RJ (1988) Chromosomal studies of bats (Mammalia: Chiroptera) from Thailand. Ann Carnegie Mus 57:99–109
Lindskog S (1983) Carbonic anhydrase. In: Spiro TG (ed) Zinc enzymes. Wiley, New York, pp 78–121
Longmire JL, Maltbie M, Baker RJ (1997) Use of “lysis buffer” in DNA isolation and its implications for museum collections. Occasional Papers, Museum of Texas Tech University, 163:1–3
Lovejoy DA, Hewett-Emmett D, Porter CA, Cepoi D, Sheffield A, Vale WW, Tashian RE (1998) Evolutionarily-conserved “acatalytic” carbonic anhydrase-related protein XI contains a sequence motif present in the neuropeptide sauvagine: the human CA-RP XI gene (CA-11) is imbedded between the Secretor gene cluster and the DBP gene at 19q13.3. Genomics 54:484–493
Montgomery JC, Venta PJ, Eddy RL, Fukushima Y-S, Shows TB, Tashian RE (1991) Characterization of the human gene for a newly discovered carbonic anhydrase, CA VII, and its localization to chromosome 16. Genomics 11:835–848
Morimoto K, Nishimori I, Takeuchi T, Kohasaki T, Okamoto N, Taguchi T, Yunoki S, Watanabe R, Ohtsuki Y, Onishi S (2005) Overexpression of carbonic anhydrase-related protein XI promotes proliferation and invasion of gastrointestinal stromal tumors. Virchows Arch 447:66–73
Nagao Y, Batanian JR, Clemente MF, Sly WS (1995) Genomic organization of the human gene (CA5) and pseudogene for mitochondrial carbonic anhydrase V and their localization to chromosomes 16q and 16p. Genomics 28:477–484
Okamoto N, Fujikawa-Adachi K, Nishimori I, Taniuchi K, Onishi S (2001) cDNA sequence of human carbonic anhydrase-related protein, CA-RP X: mRNA expressions of CA-RP X and XI in human brain. Biochim Biophys Acta 1518:311–316
Okuyama T, Badanian JR, Sly WS (1993) Genomic organization and localization of gene for human carbonic anhydrase IV to chromosome 17q. Genomics 16:678–684
Opavský R, Pastoreková S, Zelník V, Gibadulinová A, Stanbridge EG, Závada J, Ketterman R, Pastorek J (1996) Human MN/CA9 gene, a novel member of the carbonic anhydrase family: structure and exon to protein domain relationships. Genomics 33:480–487
Taniuchi K, Nishimori I, Takeuchi T, Fujikawa-Adachi K, Ohtsuki Y, Onishi S (2002) Developmental expression of carbonic anhydrase-related proteins VIII, X, and XI in the human brain. Neuroscience 112:93–99
Tashian RE (1992) Genetics of the mammalian carbonic anhydrases. Adv Genet 30:321–356
Tashian RE, Hewett-Emmett D, Carter N, Bergenhem NCH (2000) Carbonic anhydrase (CA)-related proteins (CA-RPs), and transmembrane proteins with CA or CA-RP domains. In: Chegwidden WR, Carter ND, Edwards YH (eds) The carbonic anhydrases: new horizons. Birkhäuser, Basel, pp 105–120
Acknowledgments
The tissue samples of M. lyra were provided by the Genetic Resources Collection of the Natural Science Research Laboratory of the Museum of Texas Tech University. We thank the field workers (listed in Hood et al. 1988) who collected the specimens used in the study. Electrophoresis of cycle sequencing reactions was performed by the DNA Sequence Core of the University of Michigan Medical School, by the Keck Laboratory at the University of New Orleans, and in the laboratory of Robert J. Baker at Texas Tech University. Karin Wiebauer provided helpful discussions and input. Robin Rowe of the University of New Orleans assisted with sequencing and provided valuable laboratory advice. The Biomedical Research Core Facilities at the University of Michigan Medical School synthesized primers used in the preliminary study. Funding was provided by a grant from the National Institutes of Health (GM-24681) to RET. The study also benefited from funding to CAP from the United Negro College Fund, the Research Initiative for Scientific Enhancement funded by the National Institutes of Health, and the Center for Undergraduate Research at Xavier University of Louisiana. The completion of this study was stimulated by the Morris Goodman Memorial Molecular Phylogenetics and Evolution Symposium held at Wayne State University in October 2011. The authors recognize Morris’s work as a colleague and collaborator on a variety of studies over many years.
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Porter, C.A., Hewett-Emmett, D. & Tashian, R.E. Carbonic Anhydrase-Related Protein XI: Structure of the Gene in the Greater False Vampire Bat (Megaderma lyra) Compared with Human and Domestic Pig. Biochem Genet 51, 474–481 (2013). https://doi.org/10.1007/s10528-013-9578-9
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DOI: https://doi.org/10.1007/s10528-013-9578-9