Structural and functional characterization explains loss of dNTPase activity of the cancer-specific R366C/H mutant SAMHD1 proteins

Bowen, Nicole E.; Temple, Joshua; Shepard, Caitlin; Oo, Adrian; Arizaga, Fidel; Kapoor-Vazirani, Priya; Persaud, Mirjana; Yu, Corey H.; Kim, Dong-Hyun; Schinazi, Raymond F.; Ivanov, Dmitri N.; Diaz-Griffero, Felipe; Yu, David S.; Xiong, Yong; Kim, Baek

doi:10.1016/j.jbc.2021.101170

Title: Structural and functional characterization explains loss of dNTPase activity of the cancer-specific R366C/H mutant SAMHD1 proteins

Journal Article · 01 October 2021 · Journal of Biological Chemistry

DOI: https://doi.org/10.1016/j.jbc.2021.101170 · OSTI ID:1818800

;

; Shepard, Caitlin; Oo, Adrian;

; Kapoor-Vazirani, Priya;

; Yu, Corey H.; Kim, Dong-Hyun; Schinazi, Raymond F.; Ivanov, Dmitri N.; Diaz-Griffero, Felipe; Yu, David S.; Xiong, Yong;

Not Available

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1818800

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 4 Vol. 297; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Characterization of human disease phenotypes associated with mutations in TREX1 , RNASEH2A , RNASEH2B , RNASEH2C , SAMHD1 , ADAR , and IFIH1 Crow, Yanick J.; Chase, Diana S.; Lowenstein Schmidt, Johanna American Journal of Medical Genetics Part A, Vol. 167, Issue 2 https://doi.org/10.1002/ajmg.a.36887	journal	January 2015
A SAMHD1 mutation associated with Aicardi-Goutières syndrome uncouples the ability of SAMHD1 to restrict HIV-1 from its ability to downmodulate type I interferon in humans: WHITE et al. White, Tommy E.; Brandariz-Nuñez, Alberto; Martinez-Lopez, Alicia Human Mutation, Vol. 38, Issue 6 https://doi.org/10.1002/humu.23201	journal	May 2017
Physiological concentrations of purines and pyrimidines Traut, Thomas W. Molecular and Cellular Biochemistry, Vol. 140, Issue 1 https://doi.org/10.1007/BF00928361	journal	January 1994
Cell cycle-dependent expression of mammalian ribonucleotide reductase. Differential regulation of the two subunits. Engström, Y.; Eriksson, S.; Jildevik, I. Journal of Biological Chemistry, Vol. 260, Issue 16 https://doi.org/10.1016/S0021-9258(17)39337-7	journal	August 1985
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Inhibition of Hepatitis B virus replication by SAMHD1 Chen, Zhangming; Zhu, Mengying; Pan, Xiang Biochemical and Biophysical Research Communications, Vol. 450, Issue 4 https://doi.org/10.1016/j.bbrc.2014.07.023	journal	August 2014
SAMHD1 is down regulated in lung cancer by methylation and inhibits tumor cell proliferation Wang, Jia-lei; Lu, Fan-zhen; Shen, Xiao-Yong Biochemical and Biophysical Research Communications, Vol. 455, Issue 3-4 https://doi.org/10.1016/j.bbrc.2014.10.153	journal	December 2014
Phosphorylation of SAMHD1 by Cyclin A2/CDK1 Regulates Its Restriction Activity toward HIV-1 Cribier, Alexandra; Descours, Benjamin; Valadão, Ana Luiza Chaves Cell Reports, Vol. 3, Issue 4 https://doi.org/10.1016/j.celrep.2013.03.017	journal	April 2013
Mouse SAMHD1 Has Antiretroviral Activity and Suppresses a Spontaneous Cell-Intrinsic Antiviral Response Behrendt, Rayk; Schumann, Tina; Gerbaulet, Alexander Cell Reports, Vol. 4, Issue 4 https://doi.org/10.1016/j.celrep.2013.07.037	journal	August 2013
Modulation of LINE-1 and Alu/SVA Retrotransposition by Aicardi-Goutières Syndrome-Related SAMHD1 Zhao, Ke; Du, Juan; Han, Xue Cell Reports, Vol. 4, Issue 6 https://doi.org/10.1016/j.celrep.2013.08.019	journal	September 2013
Genomic Correlates of Immune-Cell Infiltrates in Colorectal Carcinoma Giannakis, Marios; Mu, Xinmeng Jasmine; Shukla, Sachet A. Cell Reports, Vol. 15, Issue 4 https://doi.org/10.1016/j.celrep.2016.03.075	journal	April 2016
SAMHD1 Promotes DNA End Resection to Facilitate DNA Repair by Homologous Recombination Daddacha, Waaqo; Koyen, Allyson E.; Bastien, Amanda J. Cell Reports, Vol. 20, Issue 8 https://doi.org/10.1016/j.celrep.2017.08.008	journal	August 2017
The Ability of Primate Lentiviruses to Degrade the Monocyte Restriction Factor SAMHD1 Preceded the Birth of the Viral Accessory Protein Vpx Lim, Efrem S.; Fregoso, Oliver I.; McCoy, Connor O. Cell Host & Microbe, Vol. 11, Issue 2 https://doi.org/10.1016/j.chom.2012.01.004	journal	February 2012
The Retroviral Restriction Ability of SAMHD1, but Not Its Deoxynucleotide Triphosphohydrolase Activity, Is Regulated by Phosphorylation White, Tommy E.; Brandariz-Nuñez, Alberto; Valle-Casuso, Jose Carlos Cell Host & Microbe, Vol. 13, Issue 4 https://doi.org/10.1016/j.chom.2013.03.005	journal	April 2013
Aggressive CD8+ epidermotropic cutaneous T-cell lymphoma associated with homozygous mutation in SAMHD1 Merati, Miesha; Buethe, Douglas J.; Cooper, Kevin D. JAAD Case Reports, Vol. 1, Issue 4 https://doi.org/10.1016/j.jdcr.2015.05.003	journal	July 2015
SAMHD1 deficient human monocytes autonomously trigger type I interferon Martinez-Lopez, Alicia; Martin-Fernandez, Marta; Buta, Sofija Molecular Immunology, Vol. 101 https://doi.org/10.1016/j.molimm.2018.08.005	journal	September 2018
Contribution of SAM and HD domains to retroviral restriction mediated by human SAMHD1 White, Tommy E.; Brandariz-Nuñez, Alberto; Valle-Casuso, Jose Carlos Virology, Vol. 436, Issue 1 https://doi.org/10.1016/j.virol.2012.10.029	journal	February 2013
SAMHD1 controls cell cycle status, apoptosis and HIV-1 infection in monocytic THP-1 cells Bonifati, Serena; Daly, Michele B.; St. Gelais, Corine Virology, Vol. 495 https://doi.org/10.1016/j.virol.2016.05.002	journal	August 2016
An inducible transcription factor activates expression of human immunodeficiency virus in T cells Nabel, Gary; Baltimore, David Nature, Vol. 326, Issue 6114 https://doi.org/10.1038/326711a0	journal	April 1987
SAMHD1-dependent retroviral control and escape in mice Rehwinkel, Jan; Maelfait, Jonathan; Bridgeman, Anne The EMBO Journal, Vol. 32, Issue 18 https://doi.org/10.1038/emboj.2013.163	journal	July 2013
Downregulation of SAMHD1 Expression Correlates with Promoter DNA Methylation in Sézary Syndrome Patients de Silva, Suresh; Wang, Feifei; Hake, Timothy S. Journal of Investigative Dermatology, Vol. 134, Issue 2 https://doi.org/10.1038/jid.2013.311	journal	February 2014
SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx Laguette, Nadine; Sobhian, Bijan; Casartelli, Nicoletta Nature, Vol. 474, Issue 7353 https://doi.org/10.1038/nature10117	journal	May 2011
Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein Hrecka, Kasia; Hao, Caili; Gierszewska, Magda Nature, Vol. 474, Issue 7353 https://doi.org/10.1038/nature10195	journal	June 2011
HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase Goldstone, David C.; Ennis-Adeniran, Valerie; Hedden, Joseph J. Nature, Vol. 480, Issue 7377 https://doi.org/10.1038/nature10623	journal	November 2011
Structural basis of lentiviral subversion of a cellular protein degradation pathway Schwefel, David; Groom, Harriet C. T.; Boucherit, Virginie C. Nature, Vol. 505, Issue 7482 https://doi.org/10.1038/nature12815	journal	December 2013
Mutations in ADAR1 cause Aicardi-Goutières syndrome associated with a type I interferon signature Rice, Gillian I.; Kasher, Paul R.; Forte, Gabriella M. A. Nature Genetics, Vol. 44, Issue 11 https://doi.org/10.1038/ng.2414	journal	September 2012
RNF43 is frequently mutated in colorectal and endometrial cancers Giannakis, Marios; Hodis, Eran; Jasmine Mu, Xinmeng Nature Genetics, Vol. 46, Issue 12 https://doi.org/10.1038/ng.3127	journal	October 2014
Mutations involved in Aicardi-Goutières syndrome implicate SAMHD1 as regulator of the innate immune response Rice, Gillian I.; Bond, Jacquelyn; Asipu, Aruna Nature Genetics, Vol. 41, Issue 7 https://doi.org/10.1038/ng.373	journal	June 2009
Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutières syndrome and mimic congenital viral brain infection Crow, Yanick J.; Leitch, Andrea; Hayward, Bruce E. Nature Genetics, Vol. 38, Issue 8 https://doi.org/10.1038/ng1842	journal	July 2006
Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 cause Aicardi-Goutières syndrome at the AGS1 locus Crow, Yanick J.; Hayward, Bruce E.; Parmar, Rekha Nature Genetics, Vol. 38, Issue 8 https://doi.org/10.1038/ng1845	journal	July 2006
SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates Lahouassa, Hichem; Daddacha, Waaqo; Hofmann, Henning Nature Immunology, Vol. 13, Issue 3 https://doi.org/10.1038/ni.2236	journal	February 2012
The ribonuclease activity of SAMHD1 is required for HIV-1 restriction Ryoo, Jeongmin; Choi, Jongsu; Oh, Changhoon Nature Medicine, Vol. 20, Issue 8 https://doi.org/10.1038/nm.3626	journal	July 2014
SAMHD1 is a biomarker for cytarabine response and a therapeutic target in acute myeloid leukemia Schneider, Constanze; Oellerich, Thomas; Baldauf, Hanna-Mari Nature Medicine, Vol. 23, Issue 2 https://doi.org/10.1038/nm.4255	journal	December 2016
Targeting SAMHD1 with the Vpx protein to improve cytarabine therapy for hematological malignancies Herold, Nikolas; Rudd, Sean G.; Ljungblad, Linda Nature Medicine, Vol. 23, Issue 2 https://doi.org/10.1038/nm.4265	journal	January 2017
Mechanism of allosteric activation of SAMHD1 by dGTP Ji, Xiaoyun; Wu, Ying; Yan, Junpeng Nature Structural & Molecular Biology, Vol. 20, Issue 11 https://doi.org/10.1038/nsmb.2692	journal	October 2013
SAMHD1 is recurrently mutated in T-cell prolymphocytic leukemia Johansson, Patricia; Klein-Hitpass, Ludger; Choidas, Axel Blood Cancer Journal, Vol. 8, Issue 1 https://doi.org/10.1038/s41408-017-0036-5	journal	January 2018
Low-level expression of SAMHD1 in acute myeloid leukemia (AML) blasts correlates with improved outcome upon consolidation chemotherapy with high-dose cytarabine-based regimens Rassidakis, George Z.; Herold, Nikolas; Myrberg, Ida Hed Blood Cancer Journal, Vol. 8, Issue 11 https://doi.org/10.1038/s41408-018-0134-z	journal	October 2018
Dephosphorylation of the HIV-1 restriction factor SAMHD1 is mediated by PP2A-B55α holoenzymes during mitotic exit Schott, Kerstin; Fuchs, Nina V.; Derua, Rita Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04671-1	journal	June 2018
Nucleic acid binding by SAMHD1 contributes to the antiretroviral activity and is enhanced by the GpsN modification Yu, Corey H.; Bhattacharya, Akash; Persaud, Mirjana Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21023-8	journal	February 2021
SAMHD1 acts at stalled replication forks to prevent interferon induction Coquel, Flavie; Silva, Maria-Joao; Técher, Hervé Nature, Vol. 557, Issue 7703 https://doi.org/10.1038/s41586-018-0050-1	journal	April 2018
Effects of T592 phosphomimetic mutations on tetramer stability and dNTPase activity of SAMHD1 can not explain the retroviral restriction defect Bhattacharya, Akash; Wang, Zhonghua; White, Tommy Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep31353	journal	August 2016
The deoxynucleotide triphosphohydrolase SAMHD1 is a major regulator of DNA precursor pools in mammalian cells Franzolin, E.; Pontarin, G.; Rampazzo, C. Proceedings of the National Academy of Sciences, Vol. 110, Issue 35 https://doi.org/10.1073/pnas.1312033110	journal	July 2013
Structural basis of cellular dNTP regulation by SAMHD1 Ji, X.; Tang, C.; Zhao, Q. Proceedings of the National Academy of Sciences, Vol. 111, Issue 41 https://doi.org/10.1073/pnas.1412289111	journal	September 2014
Heterozygous colon cancer-associated mutations of SAMHD1 have functional significance Rentoft, Matilda; Lindell, Kristoffer; Tran, Phong Proceedings of the National Academy of Sciences, Vol. 113, Issue 17 https://doi.org/10.1073/pnas.1519128113	journal	April 2016
SAMHD1 suppresses innate immune responses to viral infections and inflammatory stimuli by inhibiting the NF-κB and interferon pathways Chen, Shuliang; Bonifati, Serena; Qin, Zhihua Proceedings of the National Academy of Sciences, Vol. 115, Issue 16 https://doi.org/10.1073/pnas.1801213115	journal	April 2018
Aicardi-Goutières Syndrome Gene and HIV-1 Restriction Factor SAMHD1 Is a dGTP-regulated Deoxynucleotide Triphosphohydrolase Powell, Rebecca D.; Holland, Paul J.; Hollis, Thomas Journal of Biological Chemistry, Vol. 286, Issue 51 https://doi.org/10.1074/jbc.C111.317628	journal	November 2011
Tight Interplay among SAMHD1 Protein Level, Cellular dNTP Levels, and HIV-1 Proviral DNA Synthesis Kinetics in Human Primary Monocyte-derived Macrophages Kim, Baek; Nguyen, Laura A.; Daddacha, Waaqo Journal of Biological Chemistry, Vol. 287, Issue 26 https://doi.org/10.1074/jbc.C112.374843	journal	June 2012
GTP Is the Primary Activator of the Anti-HIV Restriction Factor SAMHD1 Amie, Sarah M.; Bambara, Robert A.; Kim, Baek Journal of Biological Chemistry, Vol. 288, Issue 35 https://doi.org/10.1074/jbc.C113.493619	journal	July 2013
Ribonucleoside Triphosphates as Substrate of Human Immunodeficiency Virus Type 1 Reverse Transcriptase in Human Macrophages Kennedy, Edward M.; Gavegnano, Christina; Nguyen, Laura Journal of Biological Chemistry, Vol. 285, Issue 50 https://doi.org/10.1074/jbc.M110.178582	journal	December 2010
HIV/Simian Immunodeficiency Virus (SIV) Accessory Virulence Factor Vpx Loads the Host Cell Restriction Factor SAMHD1 onto the E3 Ubiquitin Ligase Complex CRL4 ^DCAF1 Ahn, Jinwoo; Hao, Caili; Yan, Junpeng Journal of Biological Chemistry, Vol. 287, Issue 15 https://doi.org/10.1074/jbc.M112.340711	journal	February 2012
Tetramerization of SAMHD1 Is Required for Biological Activity and Inhibition of HIV Infection Yan, Junpeng; Kaur, Sarabpreet; DeLucia, Maria Journal of Biological Chemistry, Vol. 288, Issue 15 https://doi.org/10.1074/jbc.M112.443796	journal	February 2013
Macrophage Tropism of HIV-1 Depends on Efficient Cellular dNTP Utilization by Reverse Transcriptase Diamond, Tracy L.; Roshal, Mikhail; Jamburuthugoda, Varuni K. Journal of Biological Chemistry, Vol. 279, Issue 49 https://doi.org/10.1074/jbc.M408573200	journal	December 2004
Interplay of ancestral non-primate lentiviruses with the virus-restricting SAMHD1 proteins of their hosts Mereby, Sarah A.; Maehigashi, Tatsuya; Holler, Jessica M. Journal of Biological Chemistry, Vol. 293, Issue 42 https://doi.org/10.1074/jbc.RA118.004567	journal	September 2018
The dNTPase activity of SAMHD1 is important for its suppression of innate immune responses in differentiated monocytic cells Qin, Zhihua; Bonifati, Serena; St. Gelais, Corine Journal of Biological Chemistry, Vol. 295, Issue 6 https://doi.org/10.1074/jbc.RA119.010360	journal	February 2020
SAMHD1 is a single-stranded nucleic acid binding protein with no active site-associated nuclease activity Seamon, Kyle J.; Sun, Zhiqiang; Shlyakhtenko, Luda S. Nucleic Acids Research, Vol. 43, Issue 13 https://doi.org/10.1093/nar/gkv633	journal	June 2015
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
SAMHD1 Impairs HIV-1 Gene Expression and Negatively Modulates Reactivation of Viral Latency in CD4 ⁺ T Cells Antonucci, Jenna M.; Kim, Sun Hee; St. Gelais, Corine Journal of Virology, Vol. 92, Issue 15 https://doi.org/10.1128/JVI.00292-18	journal	May 2018
The vpx gene of simian immunodeficiency virus facilitates efficient viral replication in fresh lymphocytes and macrophage Yu, X. F.; Yu, Q. C.; Essex, M. Journal of Virology, Vol. 65, Issue 9 https://doi.org/10.1128/jvi.65.9.5088-5091.1991	journal	September 1991
SAMHD1 Regulates Human Papillomavirus 16-Induced Cell Proliferation and Viral Replication during Differentiation of Keratinocytes James, Claire D.; Prabhakar, Apurva T.; Otoa, Raymonde mSphere, Vol. 4, Issue 4 https://doi.org/10.1128/mSphere.00448-19	journal	August 2019
A Quantitative Analysis of Subclonal and Clonal Gene Mutations before and after Therapy in Chronic Lymphocytic Leukemia Amin, Nisar A.; Seymour, Erlene; Saiya-Cork, Kamlai Clinical Cancer Research, Vol. 22, Issue 17 https://doi.org/10.1158/1078-0432.CCR-15-3103	journal	April 2016
Expression and Relationship of SAMHD1 with Other Apoptotic and Autophagic Genes in Acute Myeloid Leukemia Patients Jiang, Huinan; Li, Chuan; Liu, Zhuogang Acta Haematologica, Vol. 143, Issue 1 https://doi.org/10.1159/000500822	journal	August 2019
SAMHD1 is mutated recurrently in chronic lymphocytic leukemia and is involved in response to DNA damage Clifford, Ruth; Louis, Tania; Robbe, Pauline Blood, Vol. 123, Issue 7 https://doi.org/10.1182/blood-2013-04-490847	journal	February 2014
Presence of multiple recurrent mutations confers poor trial outcome of relapsed/refractory CLL Guièze, Romain; Robbe, Pauline; Clifford, Ruth Blood, Vol. 126, Issue 18 https://doi.org/10.1182/blood-2015-05-647578	journal	October 2015
Regulation of deoxynucleotide metabolism in cancer: novel mechanisms and therapeutic implications Kohnken, Rebecca; Kodigepalli, Karthik M.; Wu, Li Molecular Cancer, Vol. 14, Issue 1 https://doi.org/10.1186/s12943-015-0446-6	journal	September 2015
Substrates and Inhibitors of SAMHD1 Hollenbaugh, Joseph A.; Shelton, Jadd; Tao, Sijia PLOS ONE, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pone.0169052	journal	January 2017
Host Factor SAMHD1 Restricts DNA Viruses in Non-Dividing Myeloid Cells Hollenbaugh, Joseph A.; Gee, Peter; Baker, Jonathon PLoS Pathogens, Vol. 9, Issue 6 https://doi.org/10.1371/journal.ppat.1003481	journal	June 2013

Similar Records

Structural and functional characterization explains loss of dNTPase activity of the cancer-specific

Journal Article · 2021 · J. Biol. Chem. · OSTI ID:1828037

Bowen, Nicole E.; Temple, Joshua; Shepard, Caitlin; +12 more

Impaired dNTPase Activity of SAMHD1 by Phosphomimetic Mutation of Thr-592

Journal Article · 2015 · Journal of Biological Chemistry · OSTI ID:1225758

Tang, Chenxiang; Ji, Xiaoyun; Wu, Li; +1 more

Protein expression, characterization and activity comparisons of wild type and mutant DUSP5 proteins

Journal Article · 2014 · BMC Biochemistry (Online) · OSTI ID:1391835

Nayak, Jaladhi; Gastonguay, Adam J.; Talipov, Marat R.; +9 more

Title: Structural and functional characterization explains loss of dNTPase activity of the cancer-specific R366C/H mutant SAMHD1 proteins

Citation Formats

References (68)

Similar Records

Related Subjects