Allosteric regulation of the human and mouse deoxyribonucleotide triphosphohydrolase sterile α-motif/histidine-aspartate domain-containing protein 1 (SAMHD1)

Journal of Biological Chemistry

Volumn 289, Issue 26, 2014, Pages 18339-18346

  Miazzi, Cristina ^a   Ferraro, Paola ^a   Pontarin, Giovanna ^a   Rampazzo, Chiara ^a   Reichard, Peter ^a   Bianchi, Vera ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; CELL CULTURE; CELLS; LAKES; PROTEINS; SUBSTRATES;

ALLOSTERIC EFFECTORS; ALLOSTERIC PROPERTIES; ALLOSTERIC REGULATION; DNA REPLICATIONS; DOMAIN-CONTAINING PROTEINS; HUMAN FIBROBLAST; SUBSTRATE-BINDING SITES; TETRAMERIC STRUCTURES;

MAMMALS;

ADENOSINE TRIPHOSPHATE; GUANOSINE TRIPHOSPHATE; PHOSPHATASE; RECOMBINANT ENZYME; RECOMBINANT STERILE ALPHA MOTIF HISTIDINE ASPARTATE DOMAIN CONTAINING PROTEIN 1; STERILE ALPHA MOTIF HISTIDINE ASPARTATE DOMAIN CONTAINING PROTEIN 1; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; BINDING COMPETITION; BINDING SITE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME STABILITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS;

ALLOSTERIC REGULATION; DNA ENZYME; DNA REPLICATION; ENZYME KINETICS; ENZYME MECHANISM;

ALLOSTERIC REGULATION; ANIMALS; BINDING SITES; DEOXYADENINE NUCLEOTIDES; DEOXYGUANINE NUCLEOTIDES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; HYDROLYSIS; KINETICS; MICE; MODELS, MOLECULAR; MONOMERIC GTP-BINDING PROTEINS; NUCLEOTIDASES;

EID: 84903534175     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.571091     Document Type: Article

References (28)

1. Goldstone, D. C., Ennis-Adeniran, V., Hedden, J. J., Groom, H. C., Rice, G. I., Christodoulou, E., Walker, P. A., Kelly, G., Haire, L. F., Yap, M. W., de Carvalho, L. P., Stoye, J. P., Crow, Y. J., Taylor, I. A., and Webb, M. (2011) HIV-1 restriction factor SAMHD1 is a deoxyribonucleoside triphosphate triphosphohydrolase. Nature. 480, 379-382
2. Powell, R. D., Holland, P. J., Hollis, T., and Perrino, F. W. (2011) Aicardi-Goutieres syndrome gene and HIV-1 restriction factor SAMHD1 is a dGTP-regulated deoxynucleotide triphosphohydrolase. J. Biol. Chem. 286, 43596-43600
3. Laguette, N., Sobhian, B., Casartelli, N., Ringeard, M., Chable-Bessia, C., Ségéral, E., Yatim, A., Emiliani, S., Schwartz, O., and Benkirane, M. (2011) SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature. 474, 654-657
4. Hrecka, K., Hao, C., Gierszewska, M., Swanson, S. K., Kesik-Brodacka, M., Srivastava, S., Florens, L., Washburn, M. P., and Skowronski, J. (2011) Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature. 474, 658-661
5. Rice, G. I., Bond, J., Asipu, A., Brunette, R. L., Manfield, I. W., Carr, I. M., Fuller, J. C., Jackson, R. M., Lamb, T., Briggs, T. A., Ali, M., Gornall, H., Couthard, L. R., Aeby, A., Attard-Montalto, S. P., Bertini, E., Bodemer, C., Brockmann, K., Brueton, L. A., Corry, P. C., Desguerre, I., Fazzi, E., Cázorla, A. G., Gener, B., Hamel, B. C., Heiberg, A., Hunter, M., van der Knaap, M. S., Kumar, R., Lagae, L., Landrieu, P. G., Lourenco, C. M., Marom, D., McDermott, M. F., van der Merwe, W., Orcesi, S., Prendiville, J. S., Rasmussen, M., Shalev, S. A., Soler, D. M., Shinawi, M., Spiegel, R., Tan, T. Y., Vanderver, A., Wakeling, E. L., Wassmer, E., Whittaker, E., Lebon, P., Stetson, D. B., Bonthron, D. T., and Crow, Y. J. (2009) Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat. Genet. 41, 829-832
6. Lahouassa, H., Daddacha, W., Hofmann, H., Ayinde, D., Logue, E. C., Dragin, L., Bloch, N., Maudet, C., Bertrand, M., Gramberg, T., Pancino, G., Priet, S., Canard, B., Laguette, N., Benkirane, M., Transy, C., Landau, N. R., Kim, B., and Margottin-Goguet, F. (2012) SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxyribonucleoside triphosphates. Nat. Immunol. 13, 223-228
7. Amie, S. M., Bambara, R. A., and Kim, B. (2013) GTP is the primary activator of the anti-HIV restriction factor SAMHD1. J. Biol. Chem. 288, 25001-25006
8. Kim, C. A., and Bowie, J. U. (2003) SAM domains: uniform structure, diversity of function. Trends Biochem. Sci. 28, 625-628
9. Vorontsov, I. I., Minasov, G., Kiryukhina, O., Brunzelle, J. S., Shuvalova, L., and Anderson, W. F. (2011) Characterization of the deoxynucleotide triphosphate triphosphohydrolase (dNTPase) activity of the EF1143 protein from Enterococcus faecalis and crystal structure of the activator-substrate complex. J. Biol. Chem. 286, 33158-33166
10. Vorontsov, I. I., Wu, Y., DeLucia, M., Minasov, G., Mehrens, J., Shuvalova, L., Anderson, W. F., and Ahn, J. (2014) Mechanismsofallosteric activation and inhibition ofthe deoxyribonucleoside triphosphate triphosphohydrolase from Enterococcus faecalis. J. Biol. Chem. 289, 2815-2824
11. Mega, R., Kondo, N., Nakagawa, N., Kuramitsu, S., and Masui, R. (2009) Two dNTP triphosphohydrolases from Pseudomonas aeruginosa possess diverse substrate specificities. FEBS J. 276, 3211-3221
12. Kondo, N., Nakagawa, N., Ebihara, A., Chen, L., Liu, Z. J., Wang, B. C., Yokoyama, S., Kuramitsu, S., and Masui, R. (2007) Structure of dNTP-inducible dNTP triphosphohydrolase: insight into broad specificity for dNTPs and triphosphohydrolase-type hydrolysis. Acta Crystallogr. D. Biol. Crystallogr. 63, 230-239
13. Ji, X., Wu, Y., Yan, J., Mehrens, J., Yang, H., DeLucia, M., Hao, C., Gronenborn, A. M., Skowronski, J., Ahn, J., and Xiong, Y. (2013) Mechanism of allosteric activation of SAMHD1 by dGTP. Nat. Struct. Mol. Biol. 20, 1304-1309
14. Zhu, C, Gao, W., Zhao, K., Qin, X., Zhang, Y., Peng, X., Zhang, L., Dong, Y., Zhang, W., Li, P., Wei, W., Gong, Y., and Yu, X. F. (2013) Structural insight into dGTP-dependent activation of tetrameric SAMHD1 deoxynucleoside triphosphate triphosphohydrolase. Nat. Commun. 4, 2722
15. Beloglazova, N., Flick, R., Tchigvintsev, A., Brown, G., Popovic, A., Nocek, B., and Yakunin, A. F. (2013) Nuclease activity of the human SAMHD1 protein implicated in the Aicardi-Goutieres syndrome and HIV-1 restriction. J. Biol. Chem. 288, 8101-8110
16. Rampazzo, C., Miazzi, C., Franzolin, E., Pontarin, G., Ferraro, P., Frangini, M., Reichard, P., and Bianchi, V. (2010) Regulation by degradation, a cellular defense against deoxyribonucleotide pool imbalances. Mutat. Res. 703, 2-10
17. Franzolin, E., Pontarin, G., Rampazzo, C., Miazzi, C., Ferraro, P., Palumbo, E., Reichard, P., and Bianchi, V. (2013) The deoxynucleotide triphosphohydrolase SAMHD1 is a major regulator of DNA precursor pools in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 110, 14272-14277
18. Chabes, A., and Stillman, B. (2007) Constitutively high dNTP concentration inhibits cell cycle progression and the DNA damage checkpoint in yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 104, 1183-1188
19. Li, N, Zhang, W., and Cao, X. (2000) Identification of human homologue of mouse IFN-7-induced protein from human dendritic cells. Immunol. Lett. 74, 221-224
20. Rehwinkel, J., Maelfait, J., Bridgeman, A., Rigby, R., Hayward, B., Liberatore, R. A., Bieniasz, P. D., Towers, G. J., Moita, L. F., Crow, Y. J., Bonthron, D. T., and Reis e Sousa, C. (2013) SAMHD1-dependent retroviral control and escape in mice. EMBOJ. 32, 2454-2462
21. Behrendt, R., Schumann, T., Gerbaulet, A., Nguyen, L. A., Schubert, N, Alexopoulou, D., Berka, U., Lienenklaus, S., Peschke, K., Gibbert, K., Wittmann, S., Lindemann, D., Weiss, S., Dahl, A., Naumann, R., Dittmer, U., Kim, B., Mueller, W., Gramberg, T., and Roers, A. (2013) Mouse SAMHD1 has antiretroviral activity and suppresses a spontaneous cellintrinsic antiviral response. Cell. Rep. 4, 689-696
22. Yan, J., Kaur, S., DeLucia, M., Hao, C., Mehrens, J., Wang, C., Golczak, M., Palczewski, K., Gronenborn, A. M., Ahn, J., and Skowronski, J. (2013) Tetramerization of SAMHD1 is required for biological activity and inhibition of HIV infection. J. Biol. Chem. 288, 10406-10417
23. Gandhi, V. V., and Samuels, D. C. (2011) A review comparing deoxyribonucleoside triphosphate (dNTP) concentrations in the mitochondrial and cytoplasmic compartments of normal and transformed cells. Nucleosides Nucleotides Nucleic Acids. 30, 317-339
24. Reichard, P. (1988) Interactions between deoxyribonucleotide and DNA synthesis. Annu. Rev. Biochem. 57, 349-374
25. Ferraro, P., Pontarin, G., Crocco, L., Fabris, S., Reichard, P., and Bianchi, V. (2005) Mitochondrial deoxynucleotide pools in quiescent fibroblasts: a possible model for mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). J. Biol. Chem. 280, 24472-24480
26. Pontarin, G., Ferraro, P., Bee, L., Reichard, P., and Bianchi, V. (2012) Mammalian ribonucleotide reductase subunit p53R2 is required for mitochondrial DNA replication and DNA repair in quiescent cells. Proc. Natl. Acad. Sci. U. S. A. 109, 13302-13307
27. Hollenbaugh, J. A., Gee, P., Baker, J., Daly, M. B., Amie, S. M., Tate, J., Kasai, N., Kanemura, Y., Kim, D. H., Ward, B. M., Koyanagi, Y., and Kim, B. (2013) Host factor SAMHD1 restricts DNA viruses in non-dividing myeloid cells. PLoS Pathog. 9, e1003481
28. Kim, E. T., White, T. E., Brandariz-Núñez, A., Diaz-Griffero, F., and Weitzman, M. D. (2013) SAMHD1 restricts herpes simplex virus 1 in macrophages by limiting DNA replication. J. Virol. 87, 12949-12956