Modular Mimicry and Engagement of the Hippo Pathway by Marburg Virus VP40: Implications for Filovirus Biology and Budding


Autoři: Ziying Han aff001;  Shantoshini Dash aff001;  Cari A. Sagum aff002;  Gordon Ruthel aff001;  Chaitanya K. Jaladanki aff003;  Corbett T. Berry aff001;  Michael Patrick Schwoerer aff001;  Nina M. Harty aff001;  Bruce D. Freedman aff001;  Mark T. Bedford aff002;  Hao Fan aff003;  Sachdev S. Sidhu aff004;  Marius Sudol aff003;  Olena Shtanko aff005;  Ronald N. Harty aff001
Působiště autorů: Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America aff001;  Department of Epigenetics & Molecular Carcinogenesis, M.D. Anderson Cancer Center, University of Texas, Smithville, Texas, United States of America aff002;  Department of Physiology and Mechanobiology Institute at National University of Singapore, Institute for Molecular and Cell Biology, IMCB, and Bioinformatics Institute, Agency for Science, Technology and Research (A*STAR), Singapore aff003;  Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada aff004;  Texas Biomedical Research Institute, San Antonio, Texas, United States of America aff005
Vyšlo v časopise: Modular Mimicry and Engagement of the Hippo Pathway by Marburg Virus VP40: Implications for Filovirus Biology and Budding. PLoS Pathog 16(1): e32767. doi:10.1371/journal.ppat.1008231
Kategorie: Research Article
doi: 10.1371/journal.ppat.1008231

Souhrn

Ebola (EBOV) and Marburg (MARV) are members of the Filoviridae family, which continue to emerge and cause sporadic outbreaks of hemorrhagic fever with high mortality rates. Filoviruses utilize their VP40 matrix protein to drive virion assembly and budding, in part, by recruitment of specific WW-domain-bearing host proteins via its conserved PPxY Late (L) domain motif. Here, we screened an array of 115 mammalian, bacterially expressed and purified WW-domains using a PPxY-containing peptide from MARV VP40 (mVP40) to identify novel host interactors. Using this unbiased approach, we identified Yes Associated Protein (YAP) and Transcriptional co-Activator with PDZ-binding motif (TAZ) as novel mVP40 PPxY interactors. YAP and TAZ function as downstream transcriptional effectors of the Hippo signaling pathway that regulates cell proliferation, migration and apoptosis. We demonstrate that ectopic expression of YAP or TAZ along with mVP40 leads to significant inhibition of budding of mVP40 VLPs in a WW-domain/PPxY dependent manner. Moreover, YAP colocalized with mVP40 in the cytoplasm, and inhibition of mVP40 VLP budding was more pronounced when YAP was localized predominantly in the cytoplasm rather than in the nucleus. A key regulator of YAP nuclear/cytoplasmic localization and function is angiomotin (Amot); a multi-PPxY containing protein that strongly interacts with YAP WW-domains. Interestingly, we found that expression of PPxY-containing Amot rescued mVP40 VLP egress from either YAP- or TAZ-mediated inhibition in a PPxY-dependent manner. Importantly, using a stable Amot-knockdown cell line, we found that expression of Amot was critical for efficient egress of mVP40 VLPs as well as egress and spread of authentic MARV in infected cell cultures. In sum, we identified novel negative (YAP/TAZ) and positive (Amot) regulators of MARV VP40-mediated egress, that likely function in part, via competition between host and viral PPxY motifs binding to modular host WW-domains. These findings not only impact our mechanistic understanding of virus budding and spread, but also may impact the development of new antiviral strategies.

Klíčová slova:

Cell membranes – Cytoplasm – Graphs – Host-pathogen interactions – Membrane proteins – Phosphorylation – Protein domains – Filoviruses


Zdroje

1. Coffin KM, Liu J, Warren TK, Blancett CD, Kuehl KA, et al. (2018) Persistent Marburg Virus Infection in the Testes of Nonhuman Primate Survivors. Cell host & microbe 24: 405–416 e403.

2. Schindell BG, Webb AL, Kindrachuk J (2018) Persistence and Sexual Transmission of Filoviruses. Viruses 10.

3. Yeh S, Varkey JB, Crozier I (2015) Persistent Ebola Virus in the Eye. The New England journal of medicine 373: 1982–1983.

4. Zeng X, Blancett CD, Koistinen KA, Schellhase CW, Bearss JJ, et al. (2017) Identification and pathological characterization of persistent asymptomatic Ebola virus infection in rhesus monkeys. Nat Microbiol 2: 17113. doi: 10.1038/nmicrobiol.2017.113 28715405

5. Han Z, Madara JJ, Liu Y, Liu W, Ruthel G, et al. (2015) ALIX Rescues Budding of a Double PTAP/PPEY L-Domain Deletion Mutant of Ebola VP40: A Role for ALIX in Ebola Virus Egress. The Journal of infectious diseases 212 Suppl 2: S138–145.

6. Lu J, Qu Y, Liu Y, Jambusaria R, Han Z, et al. (2013) Host IQGAP1 and Ebola virus VP40 interactions facilitate virus-like particle egress. Journal of virology 87: 7777–7780. doi: 10.1128/JVI.00470-13 23637409

7. Liu Y, Lee MS, Olson MA, Harty RN (2011) Bimolecular Complementation to Visualize Filovirus VP40-Host Complexes in Live Mammalian Cells: Toward the Identification of Budding Inhibitors. Advances in virology 2011.

8. Noda T, Ebihara H, Muramoto Y, Fujii K, Takada A, et al. (2006) Assembly and budding of Ebolavirus. PLoS pathogens 2: e99. doi: 10.1371/journal.ppat.0020099 17009868

9. Hartlieb B, Weissenhorn W (2006) Filovirus assembly and budding. Virology 344: 64–70. doi: 10.1016/j.virol.2005.09.018 16364737

10. Jasenosky LD, Kawaoka Y (2004) Filovirus budding. Virus research 106: 181–188. doi: 10.1016/j.virusres.2004.08.014 15567496

11. Yasuda J, Nakao M, Kawaoka Y, Shida H (2003) Nedd4 regulates egress of Ebola virus-like particles from host cells. Journal of virology 77: 9987–9992. doi: 10.1128/JVI.77.18.9987-9992.2003 12941909

12. Timmins J, Schoehn G, Ricard-Blum S, Scianimanico S, Vernet T, et al. (2003) Ebola virus matrix protein VP40 interaction with human cellular factors Tsg101 and Nedd4. Journal of molecular biology 326: 493–502. doi: 10.1016/s0022-2836(02)01406-7 12559917

13. Harty RN, Brown ME, Wang G, Huibregtse J, Hayes FP (2000) A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Proceedings of the National Academy of Sciences of the United States of America 97: 13871–13876. doi: 10.1073/pnas.250277297 11095724

14. Bieniasz PD (2006) Late budding domains and host proteins in enveloped virus release. Virology 344: 55–63. doi: 10.1016/j.virol.2005.09.044 16364736

15. Calistri A, Salata C, Parolin C, Palu G (2009) Role of multivesicular bodies and their components in the egress of enveloped RNA viruses. Reviews in medical virology 19: 31–45. doi: 10.1002/rmv.588 18618839

16. Chen BJ, Lamb RA (2008) Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 372: 221–232. doi: 10.1016/j.virol.2007.11.008 18063004

17. Harty RN (2009) No exit: targeting the budding process to inhibit filovirus replication. Antiviral research 81: 189–197. doi: 10.1016/j.antiviral.2008.12.003 19114059

18. Irie T, Licata JM, Harty RN (2005) Functional characterization of Ebola virus L-domains using VSV recombinants. Virology 336: 291–298. doi: 10.1016/j.virol.2005.03.027 15892969

19. Liu Y, Harty RN (2010) Viral and host proteins that modulate filovirus budding. Future virology 5: 481–491. doi: 10.2217/FVL.10.33 20730024

20. Urata S, de la Torre JC (2011) Arenavirus budding. Advances in virology 2011: 180326. doi: 10.1155/2011/180326 22312335

21. Han Z, Lu J, Liu Y, Davis B, Lee MS, et al. (2014) Small-molecule probes targeting the viral PPxY-host Nedd4 interface block egress of a broad range of RNA viruses. Journal of virology 88: 7294–7306. doi: 10.1128/JVI.00591-14 24741084

22. Lewis B, Whitney S, Hudacik L, Galmin L, Huaman MC, et al. (2014) Nedd4-mediated increase in HIV-1 Gag and Env proteins and immunity following DNA-vaccination of BALB/c mice. PloS one 9: e91267. doi: 10.1371/journal.pone.0091267 24614057

23. Sette P, Nagashima K, Piper RC, Bouamr F (2013) Ubiquitin conjugation to Gag is essential for ESCRT-mediated HIV-1 budding. Retrovirology 10: 79. doi: 10.1186/1742-4690-10-79 23895345

24. Zhadina M, Bieniasz PD (2010) Functional interchangeability of late domains, late domain cofactors and ubiquitin in viral budding. PLoS pathogens 6: e1001153. doi: 10.1371/journal.ppat.1001153 20975941

25. Weiss ER, Popova E, Yamanaka H, Kim HC, Huibregtse JM, et al. (2010) Rescue of HIV-1 release by targeting widely divergent NEDD4-type ubiquitin ligases and isolated catalytic HECT domains to Gag. PLoS pathogens 6: e1001107. doi: 10.1371/journal.ppat.1001107 20862313

26. Sette P, Jadwin JA, Dussupt V, Bello NF, Bouamr F (2010) The ESCRT-associated protein Alix recruits the ubiquitin ligase Nedd4-1 to facilitate HIV-1 release through the LYPXnL L domain motif. Journal of virology 84: 8181–8192. doi: 10.1128/JVI.00634-10 20519395

27. Urata S, Yasuda J (2010) Regulation of Marburg virus (MARV) budding by Nedd4.1: a different WW domain of Nedd4.1 is critical for binding to MARV and Ebola virus VP40. The Journal of general virology 91: 228–234. doi: 10.1099/vir.0.015495-0 19812267

28. Usami Y, Popov S, Popova E, Inoue M, Weissenhorn W, et al. (2009) The ESCRT pathway and HIV-1 budding. Biochemical Society transactions 37: 181–184. doi: 10.1042/BST0370181 19143627

29. Calistri A, Del Vecchio C, Salata C, Celestino M, Celegato M, et al. (2009) Role of the feline immunodeficiency virus L-domain in the presence or absence of Gag processing: involvement of ubiquitin and Nedd4-2s ligase in viral egress. Journal of cellular physiology 218: 175–182. doi: 10.1002/jcp.21587 18792916

30. Pincetic A, Medina G, Carter C, Leis J (2008) Avian sarcoma virus and human immunodeficiency virus, type 1 use different subsets of ESCRT proteins to facilitate the budding process. The Journal of biological chemistry 283: 29822–29830. doi: 10.1074/jbc.M804157200 18723511

31. Chung HY, Morita E, von Schwedler U, Muller B, Krausslich HG, et al. (2008) NEDD4L overexpression rescues the release and infectivity of human immunodeficiency virus type 1 constructs lacking PTAP and YPXL late domains. Journal of virology 82: 4884–4897. doi: 10.1128/JVI.02667-07 18321968

32. Zhadina M, McClure MO, Johnson MC, Bieniasz PD (2007) Ubiquitin-dependent virus particle budding without viral protein ubiquitination. Proceedings of the National Academy of Sciences of the United States of America 104: 20031–20036. doi: 10.1073/pnas.0708002104 18056634

33. Urata S, Noda T, Kawaoka Y, Yokosawa H, Yasuda J (2006) Cellular factors required for Lassa virus budding. Journal of virology 80: 4191–4195. doi: 10.1128/JVI.80.8.4191-4195.2006 16571837

34. Klinger PP, Schubert U (2005) The ubiquitin-proteasome system in HIV replication: potential targets for antiretroviral therapy. Expert review of anti-infective therapy 3: 61–79. doi: 10.1586/14787210.3.1.61 15757458

35. Vana ML, Tang Y, Chen A, Medina G, Carter C, et al. (2004) Role of Nedd4 and ubiquitination of Rous sarcoma virus Gag in budding of virus-like particles from cells. Journal of virology 78: 13943–13953. doi: 10.1128/JVI.78.24.13943-13953.2004 15564502

36. Sakurai A, Yasuda J, Takano H, Tanaka Y, Hatakeyama M, et al. (2004) Regulation of human T-cell leukemia virus type 1 (HTLV-1) budding by ubiquitin ligase Nedd4. Microbes and infection / Institut Pasteur 6: 150–156.

37. Yasuda J, Hunter E, Nakao M, Shida H (2002) Functional involvement of a novel Nedd4-like ubiquitin ligase on retrovirus budding. EMBO reports 3: 636–640. doi: 10.1093/embo-reports/kvf132 12101095

38. Harty RN, Brown ME, McGettigan JP, Wang G, Jayakar HR, et al. (2001) Rhabdoviruses and the cellular ubiquitin-proteasome system: a budding interaction. Journal of virology 75: 10623–10629. doi: 10.1128/JVI.75.22.10623-10629.2001 11602704

39. Kikonyogo A, Bouamr F, Vana ML, Xiang Y, Aiyar A, et al. (2001) Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proceedings of the National Academy of Sciences of the United States of America 98: 11199–11204. doi: 10.1073/pnas.201268998 11562473

40. Licata JM, Simpson-Holley M, Wright NT, Han Z, Paragas J, et al. (2003) Overlapping motifs (PTAP and PPEY) within the Ebola virus VP40 protein function independently as late budding domains: involvement of host proteins TSG101 and VPS-4. Journal of virology 77: 1812–1819. doi: 10.1128/JVI.77.3.1812-1819.2003 12525615

41. Bouamr F, Melillo JA, Wang MQ, Nagashima K, de Los Santos M, et al. (2003) PPPYVEPTAP motif is the late domain of human T-cell leukemia virus type 1 Gag and mediates its functional interaction with cellular proteins Nedd4 and Tsg101 [corrected]. Journal of virology 77: 11882–11895. doi: 10.1128/JVI.77.22.11882-11895.2003 14581525

42. Blot V, Perugi F, Gay B, Prevost MC, Briant L, et al. (2004) Nedd4.1-mediated ubiquitination and subsequent recruitment of Tsg101 ensure HTLV-1 Gag trafficking towards the multivesicular body pathway prior to virus budding. Journal of cell science 117: 2357–2367. doi: 10.1242/jcs.01095 15126635

43. Martin-Serrano J, Perez-Caballero D, Bieniasz PD (2004) Context-dependent effects of L domains and ubiquitination on viral budding. Journal of virology 78: 5554–5563. doi: 10.1128/JVI.78.11.5554-5563.2004 15140952

44. Medina G, Pincetic A, Ehrlich LS, Zhang Y, Tang Y, et al. (2008) Tsg101 can replace Nedd4 function in ASV Gag release but not membrane targeting. Virology 377: 30–38. doi: 10.1016/j.virol.2008.04.024 18555885

45. Usami Y, Popov S, Popova E, Gottlinger HG (2008) Efficient and specific rescue of human immunodeficiency virus type 1 budding defects by a Nedd4-like ubiquitin ligase. Journal of virology 82: 4898–4907. doi: 10.1128/JVI.02675-07 18321969

46. Einbond A, Sudol M (1996) Towards prediction of cognate complexes between the WW domain and proline-rich ligands. FEBS letters 384: 1–8. doi: 10.1016/0014-5793(96)00263-3 8797792

47. Chen HI, Einbond A, Kwak SJ, Linn H, Koepf E, et al. (1997) Characterization of the WW domain of human yes-associated protein and its polyproline-containing ligands. The Journal of biological chemistry 272: 17070–17077. doi: 10.1074/jbc.272.27.17070 9202023

48. Chen HI, Sudol M (1995) The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proceedings of the National Academy of Sciences of the United States of America 92: 7819–7823. doi: 10.1073/pnas.92.17.7819 7644498

49. Linn H, Ermekova KS, Rentschler S, Sparks AB, Kay BK, et al. (1997) Using molecular repertoires to identify high-affinity peptide ligands of the WW domain of human and mouse YAP. Biological chemistry 378: 531–537. doi: 10.1515/bchm.1997.378.6.531 9224934

50. Espejo A, Cote J, Bednarek A, Richard S, Bedford MT (2002) A protein-domain microarray identifies novel protein-protein interactions. The Biochemical journal 367: 697–702. doi: 10.1042/BJ20020860 12137563

51. Ardestani A, Lupse B, Maedler K (2018) Hippo Signaling: Key Emerging Pathway in Cellular and Whole-Body Metabolism. Trends Endocrinol Metab 29: 492–509. doi: 10.1016/j.tem.2018.04.006 29739703

52. Chen YA, Lu CY, Cheng TY, Pan SH, Chen HF, et al. (2019) WW Domain-Containing Proteins YAP and TAZ in the Hippo Pathway as Key Regulators in Stemness Maintenance, Tissue Homeostasis, and Tumorigenesis. Front Oncol 9: 60. doi: 10.3389/fonc.2019.00060 30805310

53. Kim Y, Jho EH (2018) Regulation of the Hippo signaling pathway by ubiquitin modification. BMB reports 51: 143–150. doi: 10.5483/BMBRep.2018.51.3.017 29366444

54. Ma S, Meng Z, Chen R, Guan KL (2018) The Hippo Pathway: Biology and Pathophysiology. Annual review of biochemistry doi: 10.1146/annurev-biochem-013118-111829

55. Meng Z, Moroishi T, Guan KL (2016) Mechanisms of Hippo pathway regulation. Genes & development 30: 1–17.

56. Misra JR, Irvine KD (2018) The Hippo Signaling Network and Its Biological Functions. Annu Rev Genet 52: 65–87. doi: 10.1146/annurev-genet-120417-031621 30183404

57. Seo J, Kim J (2018) Regulation of Hippo signaling by actin remodeling. BMB reports 51: 151–156. doi: 10.5483/BMBRep.2018.51.3.012 29353600

58. Sudol M, Harvey KF (2010) Modularity in the Hippo signaling pathway. Trends in biochemical sciences 35: 627–633. doi: 10.1016/j.tibs.2010.05.010 20598891

59. Chan SW, Lim CJ, Guo F, Tan I, Leung T, et al. (2013) Actin-binding and cell proliferation activities of angiomotin family members are regulated by Hippo pathway-mediated phosphorylation. The Journal of biological chemistry 288: 37296–37307. doi: 10.1074/jbc.M113.527598 24225952

60. Cox CM, Mandell EK, Stewart L, Lu R, Johnson DL, et al. (2015) Endosomal regulation of contact inhibition through the AMOT:YAP pathway. Molecular biology of the cell 26: 2673–2684. doi: 10.1091/mbc.E15-04-0224 25995376

61. Hong W (2013) Angiomotin'g YAP into the nucleus for cell proliferation and cancer development. Science signaling 6: pe27.

62. Mana-Capelli S, Paramasivam M, Dutta S, McCollum D (2014) Angiomotins link F-actin architecture to Hippo pathway signaling. Molecular biology of the cell 25: 1676–1685. doi: 10.1091/mbc.E13-11-0701 24648494

63. Moleirinho S, Guerrant W, Kissil JL (2014) The Angiomotins—from discovery to function. FEBS letters 588: 2693–2703. doi: 10.1016/j.febslet.2014.02.006 24548561

64. Moleirinho S, Hoxha S, Mandati V, Curtale G, Troutman S, et al. (2017) Regulation of localization and function of the transcriptional co-activator YAP by angiomotin. eLife 6.

65. Zhao B, Li L, Lu Q, Wang LH, Liu CY, et al. (2011) Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes & development 25: 51–63.

66. Lv M, Li S, Luo C, Zhang X, Shen Y, et al. (2016) Angiomotin promotes renal epithelial and carcinoma cell proliferation by retaining the nuclear YAP. Oncotarget 7: 12393–12403. doi: 10.18632/oncotarget.7161 26848622

67. Kim M, Kim M, Park SJ, Lee C, Lim DS (2016) Role of Angiomotin-like 2 mono-ubiquitination on YAP inhibition. EMBO reports 17: 64–78. doi: 10.15252/embr.201540809 26598551

68. Yi C, Shen Z, Stemmer-Rachamimov A, Dawany N, Troutman S, et al. (2013) The p130 isoform of angiomotin is required for Yap-mediated hepatic epithelial cell proliferation and tumorigenesis. Science signaling 6: ra77.

69. Chan SW, Lim CJ, Chong YF, Pobbati AV, Huang C, et al. (2011) Hippo pathway-independent restriction of TAZ and YAP by angiomotin. The Journal of biological chemistry 286: 7018–7026. doi: 10.1074/jbc.C110.212621 21224387

70. Sudol M, Shields DC, Farooq A (2012) Structures of YAP protein domains reveal promising targets for development of new cancer drugs. Seminars in cell & developmental biology 23: 827–833.

71. Oka T, Mazack V, Sudol M (2008) Mst2 and Lats kinases regulate apoptotic function of Yes kinase-associated protein (YAP). The Journal of biological chemistry 283: 27534–27546. doi: 10.1074/jbc.M804380200 18640976

72. Zhao B, Wei X, Li W, Udan RS, Yang Q, et al. (2007) Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes & development 21: 2747–2761.

73. Nardone G, Oliver-De La Cruz J, Vrbsky J, Martini C, Pribyl J, et al. (2017) YAP regulates cell mechanics by controlling focal adhesion assembly. Nature communications 8: 15321. doi: 10.1038/ncomms15321 28504269

74. Fan R, Kim NG, Gumbiner BM (2013) Regulation of Hippo pathway by mitogenic growth factors via phosphoinositide 3-kinase and phosphoinositide-dependent kinase-1. Proceedings of the National Academy of Sciences of the United States of America 110: 2569–2574. doi: 10.1073/pnas.1216462110 23359693

75. Plouffe SW, Lin KC, Moore JL 3rd, Tan FE, Ma S, et al. (2018) The Hippo pathway effector proteins YAP and TAZ have both distinct and overlapping functions in the cell. The Journal of biological chemistry 293: 11230–11240. doi: 10.1074/jbc.RA118.002715 29802201

76. Mana-Capelli S, McCollum D (2018) Angiomotins stimulate LATS kinase autophosphorylation and act as scaffolds that promote Hippo signaling. The Journal of biological chemistry 293: 18230–18241. doi: 10.1074/jbc.RA118.004187 30266805

77. Zaltsman Y, Masuko S, Bensen JJ, Kiessling LL (2019) Angiomotin Regulates YAP Localization during Neural Differentiation of Human Pluripotent Stem Cells. Stem Cell Reports doi: 10.1016/j.stemcr.2019.03.009 31006631

78. Shtanko O, Sakurai Y, Reyes AN, Noel R, Cintrat JC, et al. (2018) Retro-2 and its dihydroquinazolinone derivatives inhibit filovirus infection. Antiviral research 149: 154–163. doi: 10.1016/j.antiviral.2017.11.016 29175127

79. Madara JJ, Han Z, Ruthel G, Freedman BD, Harty RN (2015) The multifunctional Ebola virus VP40 matrix protein is a promising therapeutic target. Future virology 10: 537–546. doi: 10.2217/fvl.15.6 26120351

80. Garnier L, Wills JW, Verderame MF, Sudol M (1996) WW domains and retrovirus budding. Nature 381: 744–745. doi: 10.1038/381744a0 8657277

81. Han Z, Schwoerer MP, Hicks P, Liang J, Ruthel G, et al. (2018) Host Protein BAG3 is a Negative Regulator of Lassa VLP Egress. Diseases 6.

82. Liang J, Sagum CA, Bedford MT, Sidhu SS, Sudol M, et al. (2017) Chaperone-Mediated Autophagy Protein BAG3 Negatively Regulates Ebola and Marburg VP40-Mediated Egress. PLoS pathogens 13: e1006132. doi: 10.1371/journal.ppat.1006132 28076420

83. Ulbricht A, Eppler FJ, Tapia VE, van der Ven PF, Hampe N, et al. (2013) Cellular mechanotransduction relies on tension-induced and chaperone-assisted autophagy. Current biology: CB 23: 430–435. doi: 10.1016/j.cub.2013.01.064 23434281

84. Troyanovsky B, Levchenko T, Mansson G, Matvijenko O, Holmgren L (2001) Angiomotin: an angiostatin binding protein that regulates endothelial cell migration and tube formation. The Journal of cell biology 152: 1247–1254. doi: 10.1083/jcb.152.6.1247 11257124

85. Mercenne G, Alam SL, Arii J, Lalonde MS, Sundquist WI (2015) Angiomotin functions in HIV-1 assembly and budding. eLife 4.

86. Pei Z, Bai Y, Schmitt AP (2010) PIV5 M protein interaction with host protein angiomotin-like 1. Virology 397: 155–166. doi: 10.1016/j.virol.2009.11.002 19932912

87. Ray G, Schmitt PT, Schmitt AP (2019) Angiomotin-Like 1 Links Paramyxovirus M Proteins to NEDD4 Family Ubiquitin Ligases. Viruses 11.

88. Oka T, Schmitt AP, Sudol M (2012) Opposing roles of angiomotin-like-1 and zona occludens-2 on pro-apoptotic function of YAP. Oncogene 31: 128–134. doi: 10.1038/onc.2011.216 21685940

89. Adler JJ, Heller BL, Bringman LR, Ranahan WP, Cocklin RR, et al. (2013) Amot130 adapts atrophin-1 interacting protein 4 to inhibit yes-associated protein signaling and cell growth. The Journal of biological chemistry 288: 15181–15193. doi: 10.1074/jbc.M112.446534 23564455

90. Zhang C, Wang F, Xie Z, Chen L, Sinkemani A, et al. (2018) AMOT130 linking F-actin to YAP is involved in intervertebral disc degeneration. Cell Prolif 51: e12492. doi: 10.1111/cpr.12492 30039887

91. Citi S, Guerrera D, Spadaro D, Shah J (2014) Epithelial junctions and Rho family GTPases: the zonular signalosome. Small GTPases 5: 1–15.

92. Spadaro D, Tapia R, Pulimeno P, Citi S (2012) The control of gene expression and cell proliferation by the epithelial apical junctional complex. Essays in biochemistry 53: 83–93. doi: 10.1042/bse0530083 22928510

93. Yi C, Troutman S, Fera D, Stemmer-Rachamimov A, Avila JL, et al. (2011) A tight junction-associated Merlin-angiomotin complex mediates Merlin's regulation of mitogenic signaling and tumor suppressive functions. Cancer cell 19: 527–540. doi: 10.1016/j.ccr.2011.02.017 21481793

94. Zheng Y, Vertuani S, Nystrom S, Audebert S, Meijer I, et al. (2009) Angiomotin-like protein 1 controls endothelial polarity and junction stability during sprouting angiogenesis. Circulation research 105: 260–270. doi: 10.1161/CIRCRESAHA.109.195156 19590046

95. Han Z, Sagum CA, Bedford MT, Sidhu SS, Sudol M, et al. (2016) ITCH E3 Ubiquitin Ligase Interacts with Ebola Virus VP40 to Regulate Budding. Journal of virology doi: 10.1128/JVI.01078-16 27489272

96. Aragon E, Goerner N, Xi Q, Gomes T, Gao S, et al. (2012) Structural basis for the versatile interactions of Smad7 with regulator WW domains in TGF-beta Pathways. Structure 20: 1726–1736. doi: 10.1016/j.str.2012.07.014 22921829

97. Tubert-Brohman I, Sherman W, Repasky M, Beuming T (2013) Improved docking of polypeptides with Glide. Journal of chemical information and modeling 53: 1689–1699. doi: 10.1021/ci400128m 23800267

Štítky
Hygiena a epidemiologie Infekční lékařství Laboratoř

Článek vyšel v časopise

PLOS Pathogens


2020 Číslo 1

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Farmaceutická péče o pacienta s inhalační terapií
nový kurz
Autoři: Mgr. Ondřej Šimandl

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Léčba akutní pooperační bolesti
Autoři: doc. MUDr. Jiří Málek, CSc.

Nové antipsychotikum kariprazin v léčbě schizofrenie
Autoři: prof. MUDr. Cyril Höschl, DrSc., FRCPsych.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se