Androglobin: A chimeric globin in metazoans that is preferentially expressed in mammalian testes

Molecular Biology and Evolution

Volumn 29, Issue 4, 2012, Pages 1105-1114

  Hoogewijs, David ^a   Ebner, Bettina ^b   Germani, Francesca ^c   Hoffmann, Federico G ^d   Fabrizius, Andrej ^b   Moens, Luc ^c   Burmester, Thorsten ^e   Dewilde, Sylvia ^c   Storz, Jay F ^f   Vinogradov, Serge N ^g   Hankeln, Thomas ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d MISSISSIPPI STATE UNIVERSITY   (United States)

^e UNIVERSITY OF HAMBURG   (Germany)

^f UNIVERSITY OF NEBRASKA   (United States)

^g WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

gene family; hexacoordination; hypoxia; protein domain; spermatogenesis

Indexed keywords

ANDROGLOBIN; CALMODULIN BINDING PROTEIN; CALPAIN; CHIMERIC PROTEIN; GLOBIN; HEME; MYOGLOBIN; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CHOANOFLAGELLATE; ENZYME ACTIVE SITE; GENE EXPRESSION; GENOME; HUMAN; HUMAN TISSUE; HYPOXIA; METAZOON; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PHYLOGENETIC TREE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN STRUCTURE; SPERMATOGENESIS; TESTIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CALMODULIN-BINDING PROTEINS; CALPAIN; EVOLUTION, MOLECULAR; GLOBINS; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; TESTIS;

ANIMALIA; CHOANOFLAGELLIDA; MAMMALIA; METAZOA; MUS; VERTEBRATA;

EID: 84857613938     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr246     Document Type: Article

References (61)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104-2105. (Pubitemid 40668057)
2. Aitken RJ, Roman SD. 2008. Antioxidant systems and oxidative stress in the testes. Adv Exp Med Biol. 636:154-171.
3. Altschul SF, Madden TL, Schaffer 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. (Pubitemid 27359211)
4. Bashford D, Chothia C, Lesk AM. 1987. Determinants of a protein fold. Unique features of the globin amino acid sequences. J Mol Biol. 196:199-216. (Pubitemid 17102240)
5. Ben-Aharon I, Brown PR, Shalgi R, Eddy EM. 2006. Calpain 11 is unique to mouse spermatogenic cells. Mol Reprod Dev. 73:767-773.
6. Burmester T, Ebner B, Weich B, Hankeln T. 2002. Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol Biol Evol. 19:416-421. (Pubitemid 34289416)
7. Burmester T, Haberkamp M, Mitz S, Roesner A, Schmidt M, Ebner B, Gerlach F, Fuchs C, Hankeln T. 2004. Neuroglobin and cytoglobin: genes, proteins and evolution. IUBMB Life. 56:703-707. (Pubitemid 40515816)
8. Burmester T, Weich B, Reinhardt S, Hankeln T. 2000. A vertebrate globin expressed in the brain. Nature 407:520-523.
9. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17:540-552. (Pubitemid 30210700)
10. Celino FT, Yamaguchi S, Miura C, Ohta T, Tozawa Y, Iwai T, Miura T. 2011. Tolerance of spermatogonia to oxidative stress is due to high levels of Zn and Cu/Zn superoxide dismutase. PLoS One 6:e16938.
11. Croall DE, Ersfeld K. 2007. The calpains: modular designs and functional diversity. Genome Biol. 8:218.
12. Dewilde S, Kiger L, Burmester T, Hankeln T, Baudin-Creuza V, Aerts T, Marden MC, Caubergs R, Moens L. 2001. Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family. J Biol Chem. 276:38949-38955.
13. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. (Pubitemid 38832724)
14. Fuchs C, Burmester T, Hankeln T. 2006. The amphibian globin gene repertoire as revealed by the Xenopus genome. Cytogenet Genome Res. 112:296-306. (Pubitemid 43260758)
15. Geuens E, Hoogewijs D, Nardini M, et al. (16 co-authors). 2010. Globinlike proteins in Caenorhabditis elegans: in vivo localization, ligand binding and structural properties. BMC Biochem. 11:17.
16. Goll DE, Thompson VF, Li H, Wei W, Cong J. 2003. The calpain system. Physiol Rev. 83:731-801. (Pubitemid 36828925)
17. Gough J, Karplus K, Hughey R, Chothia C. 2001. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol. 313:903-919. (Pubitemid 33063435)
18. Hankeln T, Ebner B, Fuchs C, et al. (23 co-authors). 2005. Neuroglobin and cytoglobin in search of their role in the vertebrate globin family. J Inorg Biochem. 99:110-119. (Pubitemid 39642974)
19. Hardison RC. 1996. A brief history of hemoglobins: plant, animal, protist, and bacteria. Proc Natl Acad Sci USA. 93:5675-5679. (Pubitemid 26190738)
20. Hoffmann FG, Opazo JC, Storz JF. 2010. Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates. Proc Natl Acad Sci USA. 107: 14274-14279.
21. Hoogewijs D, De Henau S, Dewilde S, Moens L, Couvreur M, Borgonie G, Vinogradov SN, Roy SW, Vanfleteren JR. 2008. The Caenorhabditis globin gene family reveals extensive nematodespecific radiation and diversification. BMC Evol Biol. 8:279.
22. Howes BD, Giordano D, Boechi L, et al. (14 co-authors). 2011. The peculiar heme pocket of the 2/2 hemoglobin of cold-adapted Pseudoalteromonas haloplanktis TAC125. J Biol Inorg Chem. 16:299-311.
23. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 8:275-282.
24. Jung J, Lee B. 2001. Circularly permuted proteins in the protein structure database. Protein Sci. 10:1881-1886. (Pubitemid 32848784)
25. Kakar S, Hoffman FG, Storz JF, Fabian M, Hargrove MS. 2010. Structure and reactivity of hexacoordinate hemoglobins. Biophys Chem. 152:1-14.
26. Katoh K, Kuma K, Toh H, Miyata T. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33:511-518. (Pubitemid 40360980)
27. Kitanishi K, Kobayashi K, Kawamura Y, Ishigami I, Ogura T, Nakajima K, Igarashi J, Tanaka A, Shimizu T. 2010. Important roles of Tyr43 at the putative heme distal side in the oxygen recognition and stability of the Fe(II)-O2 complex of YddV, a globin-coupled heme-based oxygen sensor diguanylate cyclase. Biochemistry 49:10381-10393.
28. Kugelstadt D, Haberkamp M, Hankeln T, Burmester T. 2004. Neuroglobin, cytoglobin, and a novel, eye-specific globin from chicken. Biochem Biophys Res Commun. 325:719-725. (Pubitemid 39487931)
29. Larkin MA, Blackshields G, Brown NP, et al. (13 co-authors). 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. (Pubitemid 350162903)
30. Lesk AM, Chothia C. 1980. How different amino acid sequences determine similar protein structures: the structure and evolutionary dynamics of the globins. J Mol Biol. 136:225-270.
31. Long M, Rosenberg C, Gilbert W. 1995. Intron phase correlations and the evolution of the intron/exon structure of genes. Proc Natl Acad Sci USA. 92:12495-12499. (Pubitemid 26014096)
32. Lupas A, Van Dyke M, Stock J. 1991. Predicting coiled coils from protein sequences. Science 252:1162-1164. (Pubitemid 21917026)
33. Marchler-Bauer A, Lu S, Anderson JB, et al. (27 co-authors). 2011. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39:D225-D229.
34. Murray JW, Delumeau O, Lewis RJ. 2005. Structure of a nonheme globin in environmental stress signaling. Proc Natl Acad Sci USA. 102:17320-17325. (Pubitemid 41740864)
35. Nielsen R, Bustamante C, Clark AG, et al. (13 co-authors). 2005. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 3:e170.
36. Osako Y, Maemoto Y, Tanaka R, Suzuki H, Shibata H, Maki M. 2010. Autolytic activity of human calpain 7 is enhanced by ESCRT-IIIrelated protein IST1 through MIT-MIM interaction. FEBS J. 277:4412-4426.
37. Papadopoulos JS, Agarwala R. 2007. COBALT: constraint-based alignment tool for multiple protein sequences. Bioinformatics 23:1073-1079. (Pubitemid 47050558)
38. Perutz MF. 1979. Regulation of oxygen affinity of hemoglobin: influence of structure of the globin on the heme iron. Annu Rev Biochem. 48:327-386. (Pubitemid 10191092)
39. Platts AE, Dix DJ, Chemes HE, et al. (11 co-authors). 2007. Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Hum Mol Genet. 16:763-773. (Pubitemid 47061623)
40. Reuss S, Saaler-Reinhardt S, Weich B, Wystub S, Reuss MH, Burmester T, Hankeln T. 2002. Expression analysis of neuroglobin mRNA in rodent tissues. Neuroscience 115:645-656. (Pubitemid 35339456)
41. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, Barrette T, Pandey A, Chinnaiyan AM. 2004. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6:1-6. (Pubitemid 38391943)
42. Ribeiro EA Jr., Ramos CH. 2005. Circular permutation and deletion studies of myoglobin indicate that the correct position of its Nterminus is required for native stability and solubility but not for native-like heme binding and folding. Biochemistry 44:4699-4709. (Pubitemid 40396748)
43. Roesner A, Fuchs C, Hankeln T, Burmester T. 2005. A globin gene of ancient evolutionary origin in lower vertebrates: evidence for two distinct globin families in animals. Mol Biol Evol. 22:12-20. (Pubitemid 39628539)
44. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. (Pubitemid 37038874)
45. Shi J, Blundell TL, Mizuguchi K. 2001. FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol. 310:243-257. (Pubitemid 32619966)
46. Sorimachi H, Hata S, Ono Y. 2010. Expanding members and roles of the calpain superfamily and their genetically modified animals. Exp Anim. 59:549-566.
47. Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol. 57:758-771.
48. Steinway SN, Dannenfelser R, Laucius CD, Hayes JE, Nayak S. 2010. JCoDA: a tool for detecting evolutionary selection. BMC Bioinformatics. 11:284.
49. Strobl S, Fernandez-Catalan C, Braun M, et al. (12 co-authors). 2000. The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium. Proc Natl Acad Sci USA. 97:588-592. (Pubitemid 30070353)
50. Tiso M, Tejero J, Basu S, et al. (13 co-authors). 2011. Human neuroglobin functions as a redox-regulated nitrite reductase. J Biol Chem. 286:18277-18289.
51. Vinogradov SN, Hoogewijs D, Bailly X, Arredondo-Peter R, Gough J, Dewilde S, Moens L, Vanfleteren JR. 2006. A phylogenomic profile of globins. BMC Evol Biol. 6:31.
52. Vinogradov SN, Hoogewijs D, Bailly X, Arredondo-Peter R, Guertin M, Gough J, Dewilde S, Moens L, Vanfleteren JR. 2005. Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life. Proc Natl Acad Sci USA. 102:11385-11389. (Pubitemid 41153829)
53. Vinogradov SN, Hoogewijs D, Vanfleteren JR, Dewilde S, Moens L, Hankeln T. 2011. Evolution of the globin superfamily and its function. In: Nagai M, editor. Hemoglobin: recent developments and topics. Kerala (India): Research Signpost. p. 232-254.
54. Vinogradov SN, Moens L. 2008. Diversity of globin function: enzymatic, transport, storage, and sensing. J Biol Chem. 283:8773-8777.
55. Vogel C, Morea V. 2006. Duplication, divergence and formation of novel protein topologies. Bioessays 28:973-978. (Pubitemid 44570446)
56. Weiner J 3rd, Bornberg-Bauer E. 2006. Evolution of circular permutations in multidomain proteins. Mol Biol Evol. 23:734-743.
57. Wenger RH, Katschinski DM. 2005. The hypoxic testis and postmeiotic expression of PAS domain proteins. Semin Cell Dev Biol. 16:547-553. (Pubitemid 41247878)
58. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 18:691-699. (Pubitemid 32372940)
59. Yu NY, Wagner JR, Laird MR, et al. (11 co-authors). 2010. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26:1608-1615.
60. Zatz M, Starling A. 2005. Calpains and disease. N Engl J Med. 352:2413-2423.
61. Zhang Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 9:40.