Nucleotide binding triggers a conformational change of the CBS module of the magnesium transporter CNNM2 from a twisted towards a flat structure

Biochemical Journal

Volumn 464, Issue , 2014, Pages 23-34

  Corral Rodríguez, María Ángeles ^a   Stuiver, Marchel ^b   Abascal Palacios, Guillermo ^a   Diercks, Tammo ^a   Oyenarte, Iker ^a   Ereño Orbea, June ^a   De Opakua, Alain Ibáñez ^a   Blanco, Francisco J ^a,c   Encinar, José Antonio ^d   Spiwok, Vojtêch ^e   Terashima, Hiroyuki ^f   Accardi, Alessio ^f   Müller, Dominik ^b   Martínez Cruz, Luis Alfonso ^a  

^a CIC BIOGUNE   (Spain)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c BASQUE FOUNDATION FOR SCIENCE   (Spain)

^d MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^e INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^f WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Ancient conserved domain protein 2 (ACDP2); Cyclin M2; Cystathionine synthase (CBS) domain; Hypomagnesaemia; Magnesium homoeostasis

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; CYCLIN M2; CYCLINE; CYSTATHIONINE BETA SYNTHASE; MAGNESIUM; POLYPHOSPHATE; UNCLASSIFIED DRUG; CNNM2 PROTEIN, HUMAN; NUCLEOTIDE;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; GENE MUTATION; HYPOMAGNESEMIA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE BINDING SITE; PROTEIN DOMAIN; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; CRYSTALLIZATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; BINDING SITES; CRYSTALLIZATION; CYCLINS; CYSTATHIONINE BETA-SYNTHASE; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOTIDES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84908383508     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140409     Document Type: Article

References (57)

1. Swaminathan, R. (2003) Magnesium metabolism and its disorders. Clin. Biochem. Rev. 24, 47-66
2. Jahnen-Dechent, W. and Ketteler, M. (2012) Magnesium basics. Clin. Kidney J. 5 (Suppl. 1), i3-i14
3. Quamme, G. A. (2010) Molecular identification of ancient and modern mammalian magnesium transporters. Am. J. Physiol. Cell Physiol. 298, C407-C429
4. 2+ influx. J. Miner. Electrolyte Metab. 19, 259-265
5. 2+ transporters in apical and basolateral sides of rat liver plasma membrane. J. Biol. Chem. 275, 3772-3780
6. Romani, A. M. and Scarpa, A. (2000) Regulation of cellular magnesium. Front. Biosci. 5, D720-D374
7. 2+ exchanger expressed in CCL39 fibroblasts. Pflugers Arch. 440, 819-827
8. Watanabe, M., Konishi, M., Ohkido, I. and Matsufuji, S. (2005) Enhanced sodium-dependent extrusion of magnesium in mutant cells established from a mouse renal tubular cell line. Am. J. Physiol. Renal Physiol. 289, F742-F748
9. Schweigel, M., Kolisek, M., Nikolic, Z. and Kuzinski, J. (2008) Expression and functional activity of the Na/Mg exchanger, TRPM7 and MagT1 are changed to regulate Mg homeostasis and transport in rumen epithelial cells. Magnes. Res. 21, 118-123
10. Eshaghi, S., Niegowski, D., Kohl, A., Martinez Molina, D., Lesley, S. A. and Nordlund, P. (2006) Crystal structure of a divalent metal ion transporter CorA at 2.9 angstrom resolution. Science 313, 354-357
11. Sponder, G., Svidova, S., Schweigel, M., Vormann, J. and Kolisek, M. (2010) Splice-variant 1 of the ancient domain protein 2 (ACDP2) complements the magnesium-deficient growth phenotype of Salmonella enterica sv. typhimurium strain MM281. Magnes. Res. 23, 105-114
12. 2+ revealed by human T-cell immunodeficiency. Nature 475, 471-476
13. Rude, R. K. and Gruber, H. E. (2004) Magnesium deficiency and osteoporosis: animal and human observations. J. Nutr. Biochem. 15, 710-716
14. 2+ transporters. Curr. Opin. Nephrol. Hypertens. 20, 169-176
15. McKusick, V. A. (1998) Mendelian Inheritance in Man. A Catalog of Human Genes and Genetic Disorders, 12th edn, Johns Hopkins University Press, Baltimore
16. 2+ handling, is mutated in dominant hypomagnesemia. Am. J. Hum. Genet. 88, 333-343
17. De Baaij, J. H., Stuiver, M., Meij, I. C., Lainez, S., Kopplin, K., Venselaar, H., Müller, D., Bindels, R. J. and Hoenderop, J. G. (2012) Membrane topology and intracellular processing of cyclin M2 (CNNM2). J. Biol. Chem. 287, 13644-13655
18. Polok, B., Escher, P., Ambresin, A., Chouery, E, Bolay, S., Meunier, I., Nan, F., Hamel, C., Munier, F. L., Thilo, B. et al. (2009) Mutations in CNNM4 cause recessive cone-rod dystrophy with amelogenesis imperfecta. Am. J. Hum. Genet. 84, 259-265
19. Parry, D. A., Mighell, A. J., El-Sayed, W., Shore, R. C., Jalili, I. K., Dollfus, H., Bloch-Zupan, A., Carlos, R., Carr, I. M., Downey, L. M. et al. (2009) Mutations in CNNM4 cause Jalili syndrome, consisting of autosomal-recessive cone-rod dystrophy and amelogenesis imperfecta. Am. J. Hum. Genet. 84, 266-273
20. 2+ transport across epithelia: a mouse model. PLoS Genet. 9, e1003983
21. Goytain, A. and Quamme, G. A. (2005) Functional characterization of ACDP2 (ancient conserved domain protein), a divalent metal transporter. Physiol. Genomics 22, 382-389
22. Wang, C. Y., Shi, J. D., Yang, P., Kumar, P. G., Li, Q. Z., Run, Q. G., Su, Y. C., Scott, H. S., Kao, K. J. and She, J. X. (2003) Molecular cloning and characterization of a novel gene family of four ancient conserved domain proteins (ACDP). Gene 306, 37-44
23. Wang, C. Y., Yang, P., Shi, J. D., Purohit, S., Guo, D., An, H., Gu, J. G., Ling, J., Dong, Z. and She, J. X. (2004) Molecular cloning and characterization of the mouse Acdp gene family. BMC Genomics 5, 1-9
24. 2+ transport system. Mol. Microbiol. 5, 2753-2762
25. Yang, M., Jensen, L. T., Gardner, A. J. and Culotta, V. C. (2005) Manganese toxicity and Saccharomyces cerevisiae Mam3p, a member of the ACDP (ancient conserved domain protein) family. Biochem. J. 386, 479-487
26. Bateman, A. (1997) The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem. Sci. 22, 12-13
27. Scott, J. W., Hawley, S. A., Green, K. A., Anis, M., Stewart, G., Scullion, G. A., Norman, D. G. and Hardie, D. G. (2004) CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J. Clin. Invest. 113, 274-284
28. Kemp, B. E. (2004) Bateman modules and adenosine derivatives form a binding contract. J. Clin. Invest. 113, 182-184
29. Shabb, J. B. and Corbin, J. D. (1992) Cyclic nucleotide-binding domains in proteins having diverse functions. J. Biol. Chem. 267, 5723-5726
30. 2+ transporter. Nature 448, 1072-1075
31. 2+ homeostasis. EMBO J. 28, 3602-3612
32. 2+ transporter MgtE probed by molecular dynamics study. Proc. Natl. Acad. Sci. U. S. A. 105, 15393-15398
33. Guo, D., Ling, J., Wang, M. H., She, J. X., Gu, J. and Wang, C. Y. (2005) Physical interaction and functional coupling between ACDP4 and the intracellular ion chaperone COX11, an implication of the role of ACDP4 in essential metal ion transport and homeostasis. Mol. Pain 1, 1-11
34. Gómez-García, I., Oyenarte, I. and Martínez-Cruz, L. A. (2011) Purification, crystallization and preliminary crystallographic analysis of the CBS pair of the human metal transporter CNNM4. Acta Crystallogr. F Struct. Biol. Commun. 67, 349-353
35. Gómez-García, I., Stuiver, M., Ereño, J., Oyenarte, I., Corral-Rodríguez, M. A., Müller, D. and Martínez-Cruz, L. A. (2012) Purification, crystallization and preliminary crystallographic analysis of the CBS-domain pair of cyclin M2 (CNNM2). Acta Crystallogr. F Struct. Biol. Commun. 68, 1198-1203
36. Marley, J., Lu, M. and Bracken, C. (2001) A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR 20, 71-75
37. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
38. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C. and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
39. Lucas, M., Encinar, J. A., Arribas, E. A., Oyenarte, I., García, I. G., Kortazar, D., Fernńdez, J. A., Mato, J. M., Martínez-Chantar, M. L. and Martínez-Cruz, L. A. (2010) Binding of S-methyl-5'-thioadenosine and S-adenosyl-L-methionine to protein MJ0100 triggers an open-to-closed conformational change in its CBS motif pair. J. Mol. Biol. 396, 800-820
40. Zwart, P. H., Afonine, P. V., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., McKee, E., Moriarty, N. W., Read, R. J., Sacchettini, J. C. et al. (2008) Automated structure solution with the PHENIX suite. Methods Mol. Biol. 426, 419-435
41. Vagin, A. A., Steiner, R. S., Lebedev, A. A., Potterton, L., McNicholas, S., Long, F. and Murshudov, G. N. (2004) REFMAC5 dictionary: organisation of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D Biol. Crystallogr. 60, 2284-2295
42. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
43. Chen, V. B., Arendall, 3rd, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S. and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
44. Ignoul, S. and Eggermont, J. (2005) CBS domains: structure, function, and pathology in human proteins. Am. J. Physiol. Cell Physiol. 289, C1369-C1378
45. Baykov, A. A., Tuominen, H. K. and Lahti, R. (2011) The CBS domain: a protein module with an emerging prominent role in regulation. ACS Chem. Biol. 6, 1156-1163
46. Ereño-Orbea, J., Oyenarte, I. and Martínez-Cruz, L. A. (2013) CBS domains: ligand binding sites and conformational variability. Arch. Biochem. Biophys. 540, 70-81
47. Gómez-García, I., Oyenarte, I. and Martínez-Cruz, L. A. (2010) The crystal structure of protein MJ1225 from Methanocaldococcus jannaschii shows strong conservation of key structural features seen in the eukaryal γ-AMPK. J. Mol. Biol. 399, 53-70
48. Beis, I. and Newsholme, E. A. (1975) The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates. Biochem. J. 152, 23-32
49. 2- complexes. Eur. J. Biochem. 165, 65-72
50. Hung, L. W., Wang, I. X., Nikaido, K., Liu, P. Q., Ames, G. F. and Kim, S. H. (1998) Crystal structure of the ATP-binding subunit of ABC transporter. Nature 396, 703-707
51. Wu, S. L., Li, C. C., Chen, J. C., Chen, Y. J., Lin, C. T., Ho, T. Y. and Hsiang, C. Y. (2009) Mutagenesis identifies the critical amino acid residues of human endonuclease G involved in catalysis, magnesium coordination, and substrate specificity. J. Biomed. Sci. 16, 6
52. 2+ transport: a guided tour along the nephron. Curr. Opin. Nephrol. Hypertens. 19, 456-462
53. 2+ absorption. J. Biol. Chem. 279, 19-25
54. Li, M., Jiang, J. and Yue, L. (2006) Functional characterization of homo- and heteromeric channel kinases TRPM6 and TRPM7. J. Gen. Physiol. 127, 525-537
55. 2+ permeability and pH sensitivity in TRPM6 and TRPM7. J. Biol. Chem. 282, 25817-25830
56. 2+-dependent interactions of ATP with the cystathionine-β-synthase (CBS) comains of a magnesium transporter. J. Biol. Chem. 289, 14731-14739
57. Hardy, S., Uetani, N., Wong, N., Kostantin, E., Labbé, D. P., Bégin, L. R., Mes-Masson, A., Miranda-Saavedra, D. and Tremblay, M. L. (2014) The protein tyrosine phosphatase PRL-2 interacts with the magnesium transporter CNNM3 to promote oncogenesis. Oncogene, doi: 10.1038/onc.2014.33