Skip to main content

Part of the book series: Subcellular Biochemistry ((SCBI,volume 75))

Abstract

The catalytically inactive isoforms of α-carbonic anhydrases are known as carbonic anhydrase related proteins (CARPs). The CARPs occur independently or as domains of other proteins in animals (both vertebrates and invertebrates) and viruses. The catalytic inactivity of CARPs is due to the lack of histidine residues required for the coordination of the zinc atom. The phylogenetic analysis shows that these proteins are highly conserved across the species. The three CARPs in vertebrates are known as CARP VIII, X and XI. CARPs orthologous to CARP VIII are found in deuterostome invertebrates, whereas protostomes only possess orthologs of CARP X. The CA-like domains of receptor-type protein tyrosine phosphatases (PTPR) are found only in PTPRG and PTPRZ. Most of these CARPs are predominantly expressed in central nervous system. Among the three vertebrate CA isoforms, CARP VIII is functionally associated with motor coordination in human, mouse and zebrafish and certain types of cancers in humans. Vertebrate expression studies show that CARP X is exclusively expressed in the brain. CARP XI is only found in tetrapods and is highly expressed in the central nervous system (CNS) of humans and mice and is also associated with several cancers. CARP VIII, PTPRZ and PTPRG have been shown to coordinate the function of other proteins by protein-protein interaction, and viral CARPs participate in attachment to host cells, but the precise biological function of CARPs X and XI is still unknown. The findings so far suggest many novel functions for the CARP subfamily, most likely related to binding to other proteins.

Susan C. Frost and Robert McKenna (eds.). Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Tashian RE (1989) The carbonic anhydrases: widening perspectives on their evolution, expression and function. Bioessays 10:186–192

    Article  PubMed  CAS  Google Scholar 

  2. Sly WS, Hu PY (1995) Human carbonic anhydrases and carbonic anhydrase deficiencies. Annu Rev Biochem 64:375–401

    Article  PubMed  CAS  Google Scholar 

  3. Supuran CT (2008) Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 7:168–181

    Article  PubMed  CAS  Google Scholar 

  4. Tashian RE (1992) Genetics of the mammalian carbonic anhydrases. Adv Genet 30:321–356

    Article  PubMed  CAS  Google Scholar 

  5. Tolvanen ME, Ortutay C, Barker HR, Aspatwar A, Patrikainen M, Parkkila S (2012) Analysis of evolution of carbonic anhydrases IV and XV reveals a rich history of gene duplications and a new group of isozymes. Bioorg Med Chem 21:1503–1510

    Article  PubMed  Google Scholar 

  6. Nishimori I, Vullo D, Minakuchi T, Scozzafava A, Clemente Capasso C, Supuran CT (2012) Restoring catalytic activity to the human carbonic anhydrase (CA) related proteins VIII, X and XI affords isoforms with high catalytic efficiency and susceptibility to anion inhibition. Bioorg Med Chem Lett 23:256–260

    Article  PubMed  Google Scholar 

  7. Sjoblom B, Elleby B, Wallgren K, Jonsson BH, Lindskog S (1996) Two point mutations convert a catalytically inactive carbonic anhydrase-related protein (CARP) to an active enzyme. FEBS Lett 398:322–325

    Article  PubMed  CAS  Google Scholar 

  8. Barnea G, Silvennoinen O, Shaanan B, Honegger AM, Canoll PD, D’Eustachio P, Morse B, Levy JB, Laforgia S, Huebner K (1993) Identification of a carbonic anhydrase-like domain in the extracellular region of RPTP gamma defines a new subfamily of receptor tyrosine phosphatases. Mol Cell Biol 13:1497–1506

    PubMed  CAS  Google Scholar 

  9. Levy JB, Canoll PD, Silvennoinen O, Barnea G, Morse B, Honegger AM, Huang JT, Cannizzaro LA, Park SH, Druck T, Huebner K, Sap J, Ehrlich M, Musacchio JM, Schlessinger J (1993) The cloning of a receptor-type protein tyrosine phosphatase expressed in the central nervous system. J Biol Chem 268:10573–10581

    PubMed  CAS  Google Scholar 

  10. Ortutay C, Olatubosun A, Parkkila S, Vihinen M, Tolvanen ME (2010) An evolutionary analysis of insect carbonic anydrases. In: Berhardt LV (ed) Advances in medicine and biology, vol 7. Nova Science Publishers, Hauppauge, pp 145–168

    Google Scholar 

  11. Maa JS, Rodriguez JF, Esteban M (1990) Structural and functional characterization of a cell surface binding protein of vaccinia virus. J Biol Chem 265:1569–1577

    PubMed  CAS  Google Scholar 

  12. Niles EG, Condit RC, Caro P, Davidson K, Matusick L, Seto J (1986) Nucleotide sequence and genetic map of the 16-kb vaccinia virus HindIII D fragment. Virology 153:96–112

    Article  PubMed  CAS  Google Scholar 

  13. Aspatwar A, Tolvanen ME, Ortutay C, Parkkila S (2010) Carbonic anhydrase related protein VIII and its role in neurodegeneration and cancer. Curr Pharm Des 16:3264–3276

    Article  PubMed  CAS  Google Scholar 

  14. Miyamoto H (2012) Sequence of the pearl oyster carbonic anhydrase-related protein and its evolutionary implications. Biochem Genet 50:269–276

    Article  PubMed  CAS  Google Scholar 

  15. Kato K (1990) Sequence of a novel carbonic anhydrase-related polypeptide and its exclusive presence in Purkinje cells. FEBS Lett 271:137–140

    Article  PubMed  CAS  Google Scholar 

  16. Taniuchi K, Nishimori I, Takeuchi T, Ohtsuki Y, Onishi S (2002) cDNA cloning and developmental expression of murine carbonic anhydrase-related proteins VIII, X, and XI. Brain Res Mol Brain Res 109:207–215

    Article  PubMed  CAS  Google Scholar 

  17. Lakkis MM, Bergenhem NC, O’Shea KS, Tashian RE (1997) Expression of the acatalytic carbonic anhydrase VIII gene, Car8, during mouse embryonic development. Histochem J 29:135–141

    Article  PubMed  CAS  Google Scholar 

  18. 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

    Article  PubMed  CAS  Google Scholar 

  19. Miyaji E, Nishimori I, Taniuchi K, Takeuchi T, Ohtsuki Y, Onishi S (2003) Overexpression of carbonic anhydrase-related protein VIII in human colorectal cancer. J Pathol 201:37–45

    Article  PubMed  CAS  Google Scholar 

  20. Nishikata M, Nishimori I, Taniuchi K, Takeuchi T, Minakuchi T, Kohsaki T, Adachi Y, Ohtsuki Y, Onishi S (2007) Carbonic anhydrase-related protein VIII promotes colon cancer cell growth. Mol Carcinog 46:208–214

    Article  PubMed  CAS  Google Scholar 

  21. Picaud SS, Muniz JR, Kramm A, Pilka ES, Kochan G, Oppermann U, Yue WW (2009) Crystal structure of human carbonic anhydrase-related protein VIII reveals the basis for catalytic silencing. Proteins 76:507–511

    Article  PubMed  CAS  Google Scholar 

  22. Turkmen S, Guo G, Garshasbi M, Hoffmann K, Alshalah AJ, Mischung C, Kuss A, Humphrey N, Mundlos S, Robinson PN (2009) CA8 mutations cause a novel syndrome characterized by ataxia and mild mental retardation with predisposition to quadrupedal gait. PLoS Genet 5:e1000487

    Article  PubMed  Google Scholar 

  23. Kaya N, Aldhalaan H, Al-Younes B, Colak D, Shuaib T, Al-Mohaileb F, Al-Sugair A, Nester M, Al-Yamani S, Al-Bakheet A, Al-Hashmi N, Al-Sayed M, Meyer B, Jungbluth H, Al-Owain M (2011) Phenotypical spectrum of cerebellar ataxia associated with a novel mutation in the CA8 gene, encoding carbonic anhydrase (CA) VIII. Am J Med Genet B Neuropsychiatr Genet 156:826–834

    Article  CAS  Google Scholar 

  24. Jiao Y, Yan J, Zhao Y, Donahue LR, Beamer WG, Li X, Roe BA, Ledoux MS, Gu W (2005) Carbonic anhydrase-related protein VIII deficiency is associated with a distinctive lifelong gait disorder in waddles mice. Genetics 171:1239–1246

    Article  PubMed  CAS  Google Scholar 

  25. Yan J, Jiao Y, Jiao F, Stuart J, Donahue LR, Beamer WG, Li X, Roe BA, LeDoux MS, Gu W (2007) Effects of carbonic anhydrase VIII deficiency on cerebellar gene expression profiles in the wdl mouse. Neurosci Lett 413:196–201

    Article  PubMed  CAS  Google Scholar 

  26. Hirota J, Ando H, Hamada K, Mikoshiba K (2003) Carbonic anhydrase-related protein is a novel binding protein for inositol 1,4,5-trisphosphate receptor type 1. Biochem J 372:435–441

    Article  PubMed  CAS  Google Scholar 

  27. Ishihara T, Takeuchi T, Nishimori I, Adachi Y, Minakuchi T, Fujita J, Sonobe H, Ohtsuki Y, Onishi S (2006) Carbonic anhydrase-related protein VIII increases invasiveness of non-small cell lung adenocarcinoma. Virchows Arch 448:830–837

    Article  PubMed  CAS  Google Scholar 

  28. Lu SH, Takeuchi T, Fujita J, Ishida T, Akisawa Y, Nishimori I, Kohsaki T, Onishi S, Sonobe H, Ohtsuki Y (2004) Effect of carbonic anhydrase-related protein VIII expression on lung adenocarcinoma cell growth. Lung Cancer 44:273–280

    Article  PubMed  Google Scholar 

  29. Kilpinen S, Autio R, Ojala K, Iljin K, Bucher E, Sara H, Pisto T, Saarela M, Skotheim RI, Bjorkman M, Mpindi J-P, Haapa-Paananen S, Vainio P, Edgren H, Wolf M, Astola J, Nees M, Hautaniemi S, Kallioniem O (2008) Systematic bioinformatic analysis of expression levels of 17,330 human genes across 9,783 samples from 175 types of healthy and pathological tissues. Genome Biol 9:R139

    Article  PubMed  Google Scholar 

  30. Aspatwar A, Tolvanen ME, Jokitalo E, Parikka M, Ortutay C, Harjula SK, Ramet M, Vihinen M, Parkkila S (2013) Abnormal cerebellar development and ataxia in CARP VIII morphant zebrafish. Hum Mol Genet 22:417–432

    Article  PubMed  CAS  Google Scholar 

  31. Skaggs LA, Bergenhem NC, Venta PJ, Tashian RE (1993) The deduced amino acid sequence of human carbonic anhydrase-related protein (CARP) is 98% identical to the mouse homologue. Gene 126:291–292

    Article  PubMed  CAS  Google Scholar 

  32. Aspatwar A, Tolvanen ME, Parkkila S (2013) An update on carbonic anhydrase-related proteins VIII, X and XI. J Enzyme Inhib Med Chem 2013:1–14

    Article  Google Scholar 

  33. Aspatwar A, Tolvanen ME, Parkkila S (2010) Phylogeny and expression of carbonic anhydrase-related proteins. BMC Mol Biol 11:25

    Article  PubMed  Google Scholar 

  34. Mikoshiba K (2007) IP3 receptor/Ca2+ channel: from discovery to new signaling concepts. J Neurochem 102:1426–1446

    Article  PubMed  CAS  Google Scholar 

  35. Kiefer LL, Paterno SA, Fierke CA (1995) Hydrogen bond network in the metal binding site of carbonic anhydrase enhances zinc affinity and catalytic efficiency. J Am Chem Soc 117:6831–45837

    Article  CAS  Google Scholar 

  36. Elleby B, Sjoblom B, Tu C, Silverman DN, Lindskog S (2000) Enhancement of catalytic efficiency by the combination of site-specific mutations in a carbonic anhydrase-related protein. Eur J Biochem 267:5908–5915

    Article  PubMed  CAS  Google Scholar 

  37. 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

    Article  PubMed  CAS  Google Scholar 

  38. Wen FC, Li YH, Tsai HF, Lin CH, Li C, Liu CS, Lii CK, Nukina N, Hsieh M (2003) Down-regulation of heat shock protein 27 in neuronal cells and non-neuronal cells expressing mutant ataxin-3. FEBS Lett 546:307–314

    Article  PubMed  CAS  Google Scholar 

  39. Hsieh M, Chang WH, Hsu CF, Nishimori I, Kuo CL, Minakuchi T (2012) Altered expression of carbonic anhydrase-related protein XI in neuronal cells expressing mutant ataxin-3. Cerebellum 12:338–349

    Article  Google Scholar 

  40. Chen X, Tang TS, Tu H, Nelson O, Pook M, Hammer R, Nukina N, Bezprozvanny I (2008) Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 3. J Neurosci 28:12713–12724

    Article  PubMed  CAS  Google Scholar 

  41. De Simone G, Supuran CT (2011) (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem 111:117–129

    Article  PubMed  Google Scholar 

  42. Kawaguchi Y, Okamoto T, Taniwaki M, Aizawa M, Inoue M, Katayama S, Kawakami H, Nakamura S, Nishimura M, Akiguchi I et al (1994) CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat Genet 8:221–228

    Article  PubMed  CAS  Google Scholar 

  43. Spencer WC, Zeller G, Watson JD, Henz SR, Watkins KL, McWhirter RD, Petersen S, Sreedharan VT, Widmer C, Jo J et al (2011) A spatial and temporal map of C. elegans gene expression. Genome Res 21:325–341

    Article  PubMed  CAS  Google Scholar 

  44. Andersen JN, Jansen PG, Echwald SM, Mortensen OH, Fukada T, Del Vecchio R, Tonks NK, Moller NP (2004) A genomic perspective on protein tyrosine phosphatases: gene structure, pseudogenes, and genetic disease linkage. FASEB J 18:8–30

    Article  PubMed  CAS  Google Scholar 

  45. Brady-Kalnay SM, Tonks NK (1995) Protein tyrosine phosphatases as adhesion receptors. Curr Opin Cell Biol 7:650–657

    Article  PubMed  CAS  Google Scholar 

  46. Krueger NX, Saito H (1992) A human transmembrane protein-tyrosine-phosphatase, PTP zeta, is expressed in brain and has an N-terminal receptor domain homologous to carbonic anhydrases. Proc Natl Acad Sci USA 89:7417–7421

    Article  PubMed  CAS  Google Scholar 

  47. Kastury K, Ohta M, Lasota J, Moir D, Dorman T, LaForgia S, Druck T, Huebner K (1996) Structure of the human receptor tyrosine phosphatase gamma gene (PTPRG) and relation to the familial RCC t(3;8) chromosome translocation. Genomics 32:225–235

    Article  PubMed  CAS  Google Scholar 

  48. Peles E, Nativ M, Campbell PL, Sakurai T, Martinez R, Lev S, Clary DO, Schilling J, Barnea G, Plowman GD, Grumet M, Schlessinger J (1995) The carbonic anhydrase domain of receptor tyrosine phosphatase beta is a functional ligand for the axonal cell recognition molecule contactin. Cell 82:251–260

    Article  PubMed  CAS  Google Scholar 

  49. Maeda N, Ichihara-Tanaka K, Kimura T, Kadomatsu K, Muramatsu T, Noda M (1999) A receptor-like protein-tyrosine phosphatase PTPzeta/RPTPbeta binds a heparin-binding growth factor midkine. Involvement of arginine 78 of midkine in the high affinity binding to PTPzeta. J Biol Chem 274:12474–12479

    Article  PubMed  CAS  Google Scholar 

  50. Peles E, Schlessinger J, Grumet M (1998) Multi-ligand interactions with receptor-like protein tyrosine phosphatase beta: implications for intercellular signaling. Trends Biochem Sci 23:121–124

    Article  PubMed  CAS  Google Scholar 

  51. Faissner A, Heck N, Dobbertin A, Garwood J (2006) DSD-1-Proteoglycan/Phosphacan and receptor protein tyrosine phosphatase-beta isoforms during development and regeneration of neural tissues. Adv Exp Med Biol 557:25–53

    Article  PubMed  CAS  Google Scholar 

  52. Czopka T, von Holst A, Ffrench-Constant C, Faissner A (2010) Regulatory mechanisms that mediate tenascin C-dependent inhibition of oligodendrocyte precursor differentiation. J Neurosci 30:12310–12322

    Article  PubMed  CAS  Google Scholar 

  53. Barnea G, Grumet M, Milev P, Silvennoinen O, Levy JB, Sap J, Schlessinger J (1994) Receptor tyrosine phosphatase beta is expressed in the form of proteoglycan and binds to the extracellular matrix protein tenascin. J Biol Chem 269:14349–14352

    PubMed  CAS  Google Scholar 

  54. Shimoda Y, Watanabe K (2009) Contactins: emerging key roles in the development and function of the nervous system. Cell Adh Migr 3:64–70

    Article  PubMed  Google Scholar 

  55. Bouyain S, Watkins DJ (2010) The protein tyrosine phosphatases PTPRZ and PTPRG bind to distinct members of the contactin family of neural recognition molecules. Proc Natl Acad Sci USA 107:2443–2448

    Article  PubMed  CAS  Google Scholar 

  56. Lamprianou S, Chatzopoulou E, Thomas JL, Bouyain S, Harroch S (2011) A complex between contactin-1 and the protein tyrosine phosphatase PTPRZ controls the development of oligodendrocyte precursor cells. Proc Natl Acad Sci USA 108:17498–17503

    Article  PubMed  CAS  Google Scholar 

  57. Lawrence MC, Colman PM (1993) Shape complementarity at protein/protein interfaces. J Mol Biol 234:946–950

    Article  PubMed  CAS  Google Scholar 

  58. Harroch S, Furtado GC, Brueck W, Rosenbluth J, Lafaille J, Chao M, Buxbaum JD, Schlessinger J (2002) A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat Genet 32:411–414

    Article  PubMed  CAS  Google Scholar 

  59. Whittington DA, Grubb JH, Waheed A, Shah GN, Sly WS, Christianson DW (2004) Expression, assay, and structure of the extracellular domain of murine carbonic anhydrase XIV: implications for selective inhibition of membrane-associated isozymes. J Biol Chem 279:7223–7228

    Article  PubMed  Google Scholar 

  60. Tamura H, Fukada M, Fujikawa A, Noda M (2006) Protein tyrosine phosphatase receptor type Z is involved in hippocampus-dependent memory formation through dephosphorylation at Y1105 on p190 RhoGAP. Neurosci Lett 399:33–38

    Article  PubMed  CAS  Google Scholar 

  61. Blondet B, Carpentier G, Lafdil F, Courty J (2005) Pleiotrophin cellular localization in nerve regeneration after peripheral nerve injury. J Histochem Cytochem 53:971–977

    Article  PubMed  CAS  Google Scholar 

  62. Meng K, Rodriguez-Pena A, Dimitrov T, Chen W, Yamin M, Noda M, Deuel TF (2000) Pleiotrophin signals increased tyrosine phosphorylation of beta beta-catenin through inactivation of the intrinsic catalytic activity of the receptor-type protein tyrosine phosphatase beta/zeta. Proc Natl Acad Sci USA 97:2603–2608

    Article  PubMed  CAS  Google Scholar 

  63. Herradon G, Ezquerra L (2009) Blocking receptor protein tyrosine phosphatase beta/zeta: a potential therapeutic strategy for Parkinson’s disease. Curr Med Chem 16:3322–3329

    Article  PubMed  CAS  Google Scholar 

  64. Padilla PI, Wada A, Yahiro K, Kimura M, Niidome T, Aoyagi H, Kumatori A, Anami M, Hayashi T, Fujisawa J, Saito H, Moss J, Hirayama T (2000) Morphologic differentiation of HL-60 cells is associated with appearance of RPTPbeta and induction of Helicobacter pylori VacA sensitivity. J Biol Chem 275:15200–15206

    Article  PubMed  CAS  Google Scholar 

  65. Manabe R, Kovalenko M, Webb DJ, Horwitz AR (2002) GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J Cell Sci 115:1497–1510

    PubMed  CAS  Google Scholar 

  66. Fujikawa A, Shirasaka D, Yamamoto S, Ota H, Yahiro K, Fukada M, Shintani T, Wada A, Aoyama N, Hirayama T, Fukamachi H, Noda M (2003) Mice deficient in protein tyrosine phosphatase receptor type Z are resistant to gastric ulcer induction by VacA of Helicobacter pylori. Nat Genet 33:375–381

    Article  PubMed  CAS  Google Scholar 

  67. Buxbaum JD, Georgieva L, Young JJ, Plescia C, Kajiwara Y, Jiang Y, Moskvina V, Norton N, Peirce T, Williams H, Craddock NJ, Carroll L, Corfas G, Davis KL, Owen MJ, Harroch S, Sakurai T, O’Donovan MC (2008) Molecular dissection of NRG1-ERBB4 signaling implicates PTPRZ1 as a potential schizophrenia susceptibility gene. Mol Psychiatry 13:162–172

    Article  PubMed  CAS  Google Scholar 

  68. Takahashi N, Sakurai T, Bozdagi-Gunal O, Dorr NP, Moy J, Krug L, Gama-Sosa M, Elder GA, Koch RJ, Walker RH, Hof PR, Davis KL, Buxbaum JD (2011) Increased expression of receptor phosphotyrosine phosphatase-beta/zeta is associated with molecular, cellular, behavioral and cognitive schizophrenia phenotypes. Transl Psychiatry 1:e8

    Article  PubMed  CAS  Google Scholar 

  69. LaForgia S, Morse B, Levy J, Barnea G, Cannizzaro LA, Li F, Nowell PC, Boghosian-Sell L, Glick J, Weston A (1991) Receptor protein-tyrosine phosphatase gamma is a candidate tumor suppressor gene at human chromosome region 3p21. Proc Natl Acad Sci USA 88:5036–5040

    Article  PubMed  CAS  Google Scholar 

  70. Lamprianou S, Vacaresse N, Suzuki Y, Meziane H, Buxbaum JD, Schlessinger J, Harroch S (2006) Receptor protein tyrosine phosphatase gamma is a marker for pyramidal cells and sensory neurons in the nervous system and is not necessary for normal development. Mol Cell Biol 26:5106–5119

    Article  PubMed  CAS  Google Scholar 

  71. Strayer DS, Jerng HH (1992) Sequence and analysis of the BamHI “D” fragment of Shope fibroma virus: comparison with similar regions of related poxviruses. Virus Res 25:117–132

    Article  PubMed  CAS  Google Scholar 

  72. Hsiao JC, Chung CS, Chang W (1999) Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J Virol 73:8750–8761

    PubMed  CAS  Google Scholar 

  73. Moss B (2012) Poxvirus cell entry: how many proteins does it take? Viruses 4:688–707

    Article  PubMed  CAS  Google Scholar 

  74. Matho MH, Maybeno M, Benhnia MR, Becker D, Meng X, Xiang Y, Crotty S, Peters B, Zajonc DM (2012) Structural and biochemical characterization of the vaccinia virus envelope protein D8 and its recognition by the antibody LA5. J Virol 86:8050–8058

    Article  PubMed  CAS  Google Scholar 

  75. Ohradanova A, Vullo D, Kopacek J, Temperini C, Betakova T, Pastorekova S, Pastorek J, Supuran CT (2007) Reconstitution of carbonic anhydrase activity of the cell-surface-binding protein of vaccinia virus. Biochem J 407:61–67

    Article  PubMed  CAS  Google Scholar 

  76. Babkin IV, Babkina IN (2011) Molecular dating in the evolution of vertebrate poxviruses. Intervirology 54:253–260

    Article  PubMed  Google Scholar 

  77. Keightley PD (2012) Rates and fitness consequences of new mutations in humans. Genetics 190:295–304

    Article  PubMed  Google Scholar 

  78. Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612

    Article  PubMed  CAS  Google Scholar 

  79. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  Google Scholar 

  80. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ashok Aspatwar .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Aspatwar, A., Tolvanen, M.E.E., Ortutay, C., Parkkila, S. (2014). Carbonic Anhydrase Related Proteins: Molecular Biology and Evolution. In: Frost, S., McKenna, R. (eds) Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcellular Biochemistry, vol 75. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7359-2_8

Download citation

Publish with us

Policies and ethics