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Role of Intracellular Distribution of Feline and Bovine SAMHD1 Proteins in Lentiviral Restriction

  • Research Article
  • Published:
Virologica Sinica

Abstract

Human SAMHD1 (hSAM) restricts lentiviruses at the reverse transcription step through its dNTP triphosphohydrolase (dNTPase) activity. Besides humans, several mammalian species such as cats and cows that carry their own lentiviruses also express SAMHD1. However, the intracellular distribution of feline and bovine SAMHD1 (fSAM and bSAM) and its significance in their lentiviral restriction function is not known. Here, we demonstrated that fSAM and bSAM were both predominantly localized to the nucleus and nuclear localization signal (11KRPR14)-deleted fSAM and bSAM relocalized to the cytoplasm. Both cytoplasmic fSAM and bSAM retained the antiviral function against different lentiviruses and cytoplasmic fSAM could restrict Vpx-encoding SIV and HIV-2 more efficiently than its wild-type (WT) protein as cytoplasmic hSAM. Further investigation revealed that cytoplasmic fSAM was resistant to Vpx-induced degradation like cytoplasmic hSAM, while cytoplasmic bSAM was not, but they all demonstrated the same in vitro dNTPase activity and all could interact with Vpx as their WT proteins, indicating that cytoplasmic hSAM and fSAM can suppress more SIV and HIV-2 by being less sensitive to Vpx-mediated degradation. Our results suggested that fSAM- and bSAM-mediated lentiviral restriction does not require their nuclear localization and that fSAM shares more common features with hSAM. These findings may provide insights for the establishment of alternative animal models to study SAMHD1 in vivo.

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References

  • Ahn J, Hao C, Yan J, DeLucia M, Mehrens J, Wang C, Gronenborn AM, Skowronski J (2012) HIV/simian immunodeficiency virus (SIV) accessory virulence factor Vpx loads the host cell restriction factor SAMHD1 onto the E3 ubiquitin ligase complex CRL4DCAF1. J Biol Chem 287:12550–12558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amie SM, Bambara RA, Kim B (2013) GTP is the primary activator of the anti-HIV restriction factor SAMHD1. J Biol Chem 288:25001–25006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asadian P, Bienzle D (2019) Interferon gamma and alpha have differential effects on SAMHD1, a potent antiviral protein, in feline lymphocytes. Viruses 11:921

    Article  CAS  PubMed Central  Google Scholar 

  • Asadian P, Finnie G, Bienzle D (2018) The expression profile of sterile alpha motif and histidine-aspartate domain-containing protein 1 (SAMHD1) in feline tissues. Vet Immunol Immunopathol 195:7–18

    Article  CAS  PubMed  Google Scholar 

  • Baldauf HM, Pan X, Erikson E, Schmidt S, Daddacha W, Burggraf M, Schenkova K, Ambiel I, Wabnitz G, Gramberg T, Panitz S, Flory E, Landau NR, Sertel S, Rutsch F, Lasitschka F, Kim B, Konig R, Fackler OT, Keppler OT (2012) SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat Med 18:1682–1687

    Article  CAS  PubMed  Google Scholar 

  • Behrendt R, Schumann T, Gerbaulet A, Nguyen LA, 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, Roers A (2013) Mouse SAMHD1 has antiretroviral activity and suppresses a spontaneous cell-intrinsic antiviral response. Cell Rep 4:689–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belshan M, Ratner L (2003) Identification of the nuclear localization signal of human immunodeficiency virus type 2 Vpx. Virology 311:7–15

    Article  CAS  PubMed  Google Scholar 

  • Bergamaschi A, Ayinde D, David A, Le Rouzic E, Morel M, Collin G, Descamps D, Damond F, Brun-Vezinet F, Nisole S, Margottin-Goguet F, Pancino G, Transy C (2009) The human immunodeficiency virus type 2 Vpx protein usurps the CUL4A-DDB1 DCAF1 ubiquitin ligase to overcome a postentry block in macrophage infection. J Virol 83:4854–4860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berger G, Turpin J, Cordeil S, Tartour K, Nguyen XN, Mahieux R, Cimarelli A (2012) Functional analysis of the relationship between Vpx and the restriction factor SAMHD1. J Biol Chem 287:41210–41217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattacharya A, Wang Z, White T, Buffone C, Nguyen LA, Shepard CN, Kim B, Demeler B, Diaz-Griffero F, Ivanov DN (2016) Effects of T592 phosphomimetic mutations on tetramer stability and dNTPase activity of SAMHD1 can not explain the retroviral restriction defect. Sci Rep 6:31353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloch N, Glasker S, Sitaram P, Hofmann H, Shepard CN, Schultz ML, Kim B, Landau NR (2017) A highly active isoform of lentivirus restriction factor SAMHD1 in mouse. J Biol Chem 292:1068–1080

    Article  CAS  PubMed  Google Scholar 

  • Brandariz-Nunez A, Valle-Casuso JC, White TE, Laguette N, Benkirane M, Brojatsch J, Diaz-Griffero F (2012) Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac. Retrovirology 9:49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan EL, Espinoza DA, McAlexander MA, Myers SL, Moyer A, Witwer KW (2016) SAMHD1 transcript upregulation during SIV infection of the central nervous system does not associate with reduced viral load. Sci Rep 6:22629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buzovetsky O, Tang C, Knecht KM, Antonucci JM, Wu L, Ji X, Xiong Y (2018) The SAM domain of mouse SAMHD1 is critical for its activation and regulation. Nat Commun 9:411

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Zhu M, Pan X, Zhu Y, Yan H, Jiang T, Shen Y, Dong X, Zheng N, Lu J, Ying S, Shen Y (2014) Inhibition of Hepatitis B virus replication by SAMHD1. Biochem Biophys Res Commun 450:1462–1468

    Article  CAS  PubMed  Google Scholar 

  • Cribier A, Descours B, Valadao AL, Laguette N, Benkirane M (2013) Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep 3:1036–1043

    Article  CAS  PubMed  Google Scholar 

  • Descours B, Cribier A, Chable-Bessia C, Ayinde D, Rice G, Crow Y, Yatim A, Schwartz O, Laguette N, Benkirane M (2012) SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells. Retrovirology 9:87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fregoso OI, Ahn J, Wang C, Mehrens J, Skowronski J, Emerman M (2013) Evolutionary toggling of Vpx/Vpr specificity results in divergent recognition of the restriction factor SAMHD1. PLoS Pathog 9:e1003496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstone DC, Ennis-Adeniran V, Hedden JJ, Groom HC, Rice GI, Christodoulou E, Walker PA, Kelly G, Haire LF, Yap MW, de Carvalho LP, Stoye JP, Crow YJ, Taylor IA, Webb M (2011) HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480:379–382

    Article  CAS  PubMed  Google Scholar 

  • Goncalves A, Karayel E, Rice GI, Bennett KL, Crow YJ, Superti-Furga G, Burckstummer T (2012) SAMHD1 is a nucleic-acid binding protein that is mislocalized due to aicardi-goutieres syndrome-associated mutations. Hum Mutat 33:1116–1122

    Article  CAS  PubMed  Google Scholar 

  • Gramberg T, Kahle T, Bloch N, Wittmann S, Mullers E, Daddacha W, Hofmann H, Kim B, Lindemann D, Landau NR (2013) Restriction of diverse retroviruses by SAMHD1. Retrovirology 10:26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Zhang N, Shen S, Yu XF, Wei W (2019) Determinants of lentiviral Vpx-CRL4 E3 ligase-mediated SAMHD1 degradation in the substrate adaptor protein DCAF1. Biochem Biophys Res Commun 513:933–939

    Article  CAS  PubMed  Google Scholar 

  • Hofmann H, Logue EC, Bloch N, Daddacha W, Polsky SB, Schultz ML, Kim B, Landau NR (2012) The Vpx lentiviral accessory protein targets SAMHD1 for degradation in the nucleus. J Virol 86:12552–12560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hollenbaugh JA, Gee P, Baker J, Daly MB, Amie SM, Tate J, Kasai N, Kanemura Y, Kim DH, Ward BM, Koyanagi Y, Kim B (2013) Host factor SAMHD1 restricts DNA viruses in non-dividing myeloid cells. PLoS Pathog 9:e1003481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, Florens L, Washburn MP, Skowronski J (2011) Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474:658–661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji X, Tang C, Zhao Q, Wang W, Xiong Y (2014) Structural basis of cellular dNTP regulation by SAMHD1. Proc Natl Acad Sci USA 111:E4305–E4314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji X, Wu Y, Yan J, Mehrens J, Yang H, DeLucia M, Hao C, Gronenborn AM, Skowronski J, Ahn J, Xiong Y (2013) Mechanism of allosteric activation of SAMHD1 by dGTP. Nat Struct Mol Biol 20:1304–1309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khare PD, Loewen N, Teo W, Barraza RA, Saenz DT, Johnson DH, Poeschla EM (2008) Durable, safe, multi-gene lentiviral vector expression in feline trabecular meshwork. Mol Ther 16:97–106

    Article  CAS  PubMed  Google Scholar 

  • Kim B, Nguyen LA, Daddacha W, Hollenbaugh JA (2012) Tight interplay among SAMHD1 protein level, cellular dNTP levels, and HIV-1 proviral DNA synthesis kinetics in human primary monocyte-derived macrophages. J Biol Chem 287:21570–21574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim ET, White TE, Brandariz-Nunez A, Diaz-Griffero F, Weitzman MD (2013) SAMHD1 restricts herpes simplex virus 1 in macrophages by limiting DNA replication. J Virol 87:12949–12956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koharudin LM, Wu Y, DeLucia M, Mehrens J, Gronenborn AM, Ahn J (2014) Structural basis of allosteric activation of sterile alpha motif and histidine-aspartate domain-containing protein 1 (SAMHD1) by nucleoside triphosphates. J Biol Chem 289:32617–32627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral E, Yatim A, Emiliani S, Schwartz O, Benkirane M (2011) SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474:654–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, Dragin L, Bloch N, Maudet C, Bertrand M, Gramberg T, Pancino G, Priet S, Canard B, Laguette N, Benkirane M, Transy C, Landau NR, Kim B, Margottin-Goguet F (2012) SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol 13:223–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Zhou P (2007) DCAFs, the missing link of the CUL4-DDB1 ubiquitin ligase. Mol Cell 26:775–780

    Article  CAS  PubMed  Google Scholar 

  • Li J, Xu F, Hu S, Zhou J, Mei S, Zhao X, Cen S, Jin Q, Liang C, Guo F (2015) Characterization of the interactions between SIVrcm Vpx and red-capped mangabey SAMHD1. Biochem J 468:303–313

    Article  CAS  PubMed  Google Scholar 

  • Li W, You L, Cooper J, Schiavon G, Pepe-Caprio A, Zhou L, Ishii R, Giovannini M, Hanemann CO, Long SB, Erdjument-Bromage H, Zhou P, Tempst P, Giancotti FG (2010) Merlin/NF2 suppresses tumorigenesis by inhibiting the E3 ubiquitin ligase CRL4(DCAF1) in the nucleus. Cell 140:477–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Huan C, Wang H, Liu Y, Liu X, Su X, Yu J, Zhao Z, Yu XF, Zheng B, Zhang W (2020) TRIM21-mediated proteasomal degradation of SAMHD1 regulates its antiviral activity. EMBO Rep 21:e47528

    Article  CAS  PubMed  Google Scholar 

  • Lim ES, Fregoso OI, McCoy CO, Matsen FA, Malik HS, Emerman M (2012) The ability of primate lentiviruses to degrade the monocyte restriction factor SAMHD1 preceded the birth of the viral accessory protein Vpx. Cell Host Microbe 11:194–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mereby SA, Maehigashi T, Holler JM, Kim DH, Schinazi RF, Kim B (2018) Interplay of ancestral non-primate lentiviruses with the virus-restricting SAMHD1 proteins of their hosts. J Biol Chem 293:16402–16412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pancio HA, Vander Heyden N, Ratner L (2000) The C-terminal proline-rich tail of human immunodeficiency virus type 2 Vpx is necessary for nuclear localization of the viral preintegration complex in nondividing cells. J Virol 74:6162–6167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pauls E, Ruiz A, Badia R, Permanyer M, Gubern A, Riveira-Munoz E, Torres-Torronteras J, Alvarez M, Mothe B, Brander C, Crespo M, Menendez-Arias L, Clotet B, Keppler OT, Marti R, Posas F, Ballana E, Este JA (2014) Cell cycle control and HIV-1 susceptibility are linked by CDK6-dependent CDK2 phosphorylation of SAMHD1 in myeloid and lymphoid cells. J Immunol 193:1988–1997

    Article  CAS  PubMed  Google Scholar 

  • Powell RD, Holland PJ, Hollis T, Perrino FW (2011) Aicardi-Goutieres syndrome gene and HIV-1 restriction factor SAMHD1 is a dGTP-regulated deoxynucleotide triphosphohydrolase. J Biol Chem 286:43596–43600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rice GI, Bond J, Asipu A, Brunette RL, Manfield IW, Carr IM, Fuller JC, Jackson RM, Lamb T, Briggs TA, Ali M, Gornall H, Couthard LR, Aeby A, Attard-Montalto SP, Bertini E, Bodemer C, Brockmann K, Brueton LA, Corry PC, Desguerre I, Fazzi E, Cazorla AG, Gener B, Hamel BC, Heiberg A, Hunter M, van der Knaap MS, Kumar R, Lagae L, Landrieu PG, Lourenco CM, Marom D, McDermott MF, van der Merwe W, Orcesi S, Prendiville JS, Rasmussen M, Shalev SA, Soler DM, Shinawi M, Spiegel R, Tan TY, Vanderver A, Wakeling EL, Wassmer E, Whittaker E, Lebon P, Stetson DB, Bonthron DT, Crow YJ (2009) Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat Genet 41:829–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaller T, Pollpeter D, Apolonia L, Goujon C, Malim MH (2014) Nuclear import of SAMHD1 is mediated by a classical karyopherin alpha/beta1 dependent pathway and confers sensitivity to VpxMAC induced ubiquitination and proteasomal degradation. Retrovirology 11:29

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwefel D, Boucherit VC, Christodoulou E, Walker PA, Stoye JP, Bishop KN, Taylor IA (2015) Molecular determinants for recognition of divergent SAMHD1 proteins by the lentiviral accessory protein Vpx. Cell Host Microbe 17:489–499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shingai M, Welbourn S, Brenchley JM, Acharya P, Miyagi E, Plishka RJ, Buckler-White A, Kwong PD, Nishimura Y, Strebel K, Martin MA (2015) The expression of functional Vpx during pathogenic SIVmac Infections of rhesus macaques suppresses SAMHD1 in CD4+ memory T Cells. PLoS Pathog 11:e1004928

    Article  PubMed  PubMed Central  Google Scholar 

  • Spragg CJ, Emerman M (2013) Antagonism of SAMHD1 is actively maintained in natural infections of simian immunodeficiency virus. Proc Natl Acad Sci USA 110:21136–21141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava S, Swanson SK, Manel N, Florens L, Washburn MP, Skowronski J (2008) Lentiviral Vpx accessory factor targets VprBP/DCAF1 substrate adaptor for cullin 4 E3 ubiquitin ligase to enable macrophage infection. PLoS Pathog 4:e1000059

    Article  PubMed  PubMed Central  Google Scholar 

  • St Gelais C, de Silva S, Amie SM, Coleman CM, Hoy H, Hollenbaugh JA, Kim B, Wu L (2012) SAMHD1 restricts HIV-1 infection in dendritic cells (DCs) by dNTP depletion, but its expression in DCs and primary CD4+ T-lymphocytes cannot be upregulated by interferons. Retrovirology 9:105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang C, Ji X, Wu L, Xiong Y (2015) Impaired dNTPase activity of SAMHD1 by phosphomimetic mutation of Thr-592. J Biol Chem 290:26352–26359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Zhang K, Meng L, Zhang X, Song Y, Zhang Y, Gai Y, Zhang Y, Yu B, Wu J, Wang S, Yu X (2020) The C-terminal domain of feline and bovine SAMHD1 proteins has a crucial role in lentiviral restriction. J Biol Chem 295:4252–4264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, St Gelais C, de Silva S, Zhang H, Geng Y, Shepard C, Kim B, Yount JS, Wu L (2016) Phosphorylation of mouse SAMHD1 regulates its restriction of human immunodeficiency virus type 1 infection, but not murine leukemia virus infection. Virology 487:273–284

    Article  CAS  PubMed  Google Scholar 

  • Wei W, Guo H, Gao Q, Markham R, Yu XF (2014) Variation of two primate lineage-specific residues in human SAMHD1 confers resistance to N terminus-targeted SIV Vpx proteins. J Virol 88:583–591

    Article  PubMed  PubMed Central  Google Scholar 

  • Wei W, Guo H, Han X, Liu X, Zhou X, Zhang W, Yu XF (2012) A novel DCAF1-binding motif required for Vpx-mediated degradation of nuclear SAMHD1 and Vpr-induced G2 arrest. Cell Microbiol 14:1745–1756

    Article  CAS  PubMed  Google Scholar 

  • Welbourn S, Strebel K (2016) Low dNTP levels are necessary but may not be sufficient for lentiviral restriction by SAMHD1. Virology 488:271–277

    Article  CAS  PubMed  Google Scholar 

  • White TE, Brandariz-Nunez A, Martinez-Lopez A, Knowlton C, Lenzi G, Kim B, Ivanov D, Diaz-Griffero F (2017) A SAMHD1 mutation associated with Aicardi-Goutieres syndrome uncouples the ability of SAMHD1 to restrict HIV-1 from its ability to downmodulate type I interferon in humans. Hum Mutat 38:658–668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White TE, Brandariz-Nunez A, Valle-Casuso JC, Amie S, Nguyen L, Kim B, Brojatsch J, Diaz-Griffero F (2013a) Contribution of SAM and HD domains to retroviral restriction mediated by human SAMHD1. Virology 436:81–90

    Article  CAS  PubMed  Google Scholar 

  • White TE, Brandariz-Nunez A, Valle-Casuso JC, Amie S, Nguyen LA, Kim B, Tuzova M, Diaz-Griffero F (2013b) The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe 13:441–451

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Hao C, DeLucia M, Swanson S, Florens L, Washburn MP, Ahn J, Skowronski J (2015) CyclinA2-cyclin-dependent kinase regulates SAMHD1 protein phosphohydrolase domain. J Biol Chem 290:13279–13292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang R, Bloch N, Nguyen LA, Kim B, Landau NR (2014) SAMHD1 restricts HIV-1 replication and regulates interferon production in mouse myeloid cells. PLoS ONE 9:e89558

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu CF, Wei W, Peng X, Dong YH, Gong Y, Yu XF (2015) The mechanism of substrate-controlled allosteric regulation of SAMHD1 activated by GTP. Acta Crystallogr D Biol Crystallogr 71:516–524

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was funded by the National Natural Science Foundation of China (31270807), the Key Projects in the National Science & Technology Pillar Program in the Thirteenth Five-year Plan Period (2018ZX10731101-002-003 and 2018ZX10731101-001-020), Program for Jilin University Science and Technology Innovative Research Team (JLUSTIRT) (2017TD-05), National Postdoctoral Program for Innovative Talents (BX20180124), China Postdoctoral Science Foundation (2018M641786), and Science and Technology Development Project of Jilin Province (20200901030SF).

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  1. Chu Wang and Lina Meng have contributed equally to this work.

Authors and Affiliations

  1. National Engineering Laboratory for AIDS Vaccine, School of Life Sciences, Jilin University, Changchun, 130012, China

    Chu Wang, Lina Meng, Jialin Wang, Kaikai Zhang, Sizhu Duan, Pengyu Ren, Yingzhe Wei, Xinyu Fu, Bin Yu, Jiaxin Wu & Xianghui Yu

  2. The First Hospital and Institute of Immunology, Jilin University, Changchun, 130012, China

    Chu Wang

  3. Key Laboratory for Molecular Enzymology and Engineering, the Ministry of Education, School of Life Sciences, Jilin University, Changchun, 130012, China

    Bin Yu, Jiaxin Wu & Xianghui Yu

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  1. Chu Wang
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Contributions

CW, JXW and XHY designed the experiments. CW, LNM, JLW, KKZ, SZD, PYR, YZW and XYF carried out the experiments. CW and LNM analyzed the data and wrote the paper. BY, JXW and XHY checked and finalized the manuscript. CW and XHY acquired the funding. All authors read and approved the final manuscript.

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Correspondence to Jiaxin Wu or Xianghui Yu.

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Wang, C., Meng, L., Wang, J. et al. Role of Intracellular Distribution of Feline and Bovine SAMHD1 Proteins in Lentiviral Restriction. Virol. Sin. 36, 981–996 (2021). https://doi.org/10.1007/s12250-021-00351-5

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