ISG15 in cancer: Beyond ubiquitin-like protein

Cancer Letters

Volumn 438, Issue , 2018, Pages 52-62

  Han, Hye Gyeong ^a   Moon, Hye Won ^a   Jeon, Young Joo ^a  

^a Chungnam National University College of Medicine   (South Korea)

Author keywords

Autophagy; Cancer; Cancer therapies; Exosomes; ISG15; Ubiquitin

Indexed keywords

ADENOSINE TRIPHOSPHATE; BECLIN 1; BETA INTERFERON; CAMPTOTHECIN; DECITABINE; DEUBIQUITINASE; DOXORUBICIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INITIATION FACTOR 2ALPHA; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON STIMULATED GENE 15; LEUCINE RICH REPEAT CONTAINING PROTEIN 25; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; PEPTIDYL PROLYL CIS TRANS ISOMERASE NIMA INTERACTING 1; PROTEIN KINASE R; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; STAT1 PROTEIN; STAT2 PROTEIN; TOLL LIKE RECEPTOR 3; UBIQUITIN PROTEIN LIGASE NEDD4; UBIQUITIN SPECIFIC PROTEASE 18; UNCLASSIFIED DRUG; CYTOKINE; ISG15 PROTEIN, HUMAN; UBIQUITIN;

AUTOPHAGY; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER RESISTANCE; CARCINOGENESIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLORECTAL CANCER; CONJUGATION; CYTOKINE RELEASE; CYTOTOXICITY; DECONJUGATION; DNA REPAIR; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; EXOSOME; HIGH GRADE SEROUS OVARIAN CANCER; HUMAN; IMMUNOGENICITY; IMMUNOMODULATION; LIVER CELL CARCINOMA; MALIGNANT NEOPLASM; MUSCLE INVASIVE BLADDER CANCER; NASOPHARYNX CARCINOMA; NONHUMAN; OVARY CANCER; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSLATION; SHORT SURVEY; SIGNAL TRANSDUCTION; STOMACH CANCER; TRIPLE NEGATIVE BREAST CANCER; TUMOR MICROENVIRONMENT; UPREGULATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; METABOLISM; NEOPLASM;

AUTOPHAGY; CYTOKINES; EXOSOMES; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEOSTASIS; HUMANS; INTERFERONS; NEOPLASMS; SIGNAL TRANSDUCTION; UBIQUITINS;

EID: 85053467871     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2018.09.007     Document Type: Review

References (171)

1. Johnson, L.N., The regulation of protein phosphorylation. Biochem. Soc. Trans. 37 (2009), 627–641.
2. Moremen, K.W., Tiemeyer, M., Nairn, A.V., Vertebrate protein glycosylation: diversity, synthesis and function. Nat. Rev. Mol. Cell Biol., 13, 2012, 448.
3. Choudhary, C., Weinert, B.T., Nishida, Y., Verdin, E., Mann, M., The growing landscape of lysine acetylation links metabolism and cell signalling. Nat. Rev. Mol. Cell Biol., 15, 2014, 536.
4. Goldstein, G., Scheid, M., Hammerling, U., Schlesinger, D., Niall, H., Boyse, E., Isolation of a polypeptide that has lymphocyte-differentiating properties and is probably represented universally in living cells. Proc. Natl. Acad. Sci. Unit. States Am. 72 (1975), 11–15.
5. Soucy, T.A., Dick, L.R., Smith, P.G., Milhollen, M.A., Brownell, J.E., The NEDD8 conjugation pathway and its relevance in cancer biology and therapy. Genes & cancer 1 (2010), 708–716.
6. Mahbubul Bashar, M., Khan, M.A., An overview on surface modification of cotton fiber for apparel use. J. Polym. Environ. 21 (2013), 181–190.
7. Hipp, M.S., Kalveram, B., Raasi, S., Groettrup, M., Schmidtke, G., FAT10, a ubiquitin-independent signal for proteasomal degradation. Mol. Cell Biol. 25 (2005), 3483–3491.
8. Hochstrasser, M., Origin and function of ubiquitin-like proteins. Nature, 458, 2009, 422.
9. van der Veen, A.G., Ploegh, H.L., Ubiquitin-like proteins. Annu. Rev. Biochem. 81 (2012), 323–357.
10. Cappadocia, L., Lima, C.D., Ubiquitin-like protein conjugation: structures, chemistry, and mechanism. Chem. Rev. 118 (2017), 889–918.
11. Hochstrasser, M., Evolution and function of ubiquitin-like protein-conjugation systems. Nat. Cell Biol., 2, 2000, E153.
12. Kim, K.I., Zhang, D.-E., ISG15, not just another ubiquitin-like protein. Biochem. Biophys. Res. Commun. 307 (2003), 431–434.
13. Hershko, A., Ciechanover, A., The Ubiquitin System, Annual Reviews 4139 El Camino Way, PO Box 10139, Palo Alto, CA 94303-0139, USA. 1998.
14. Marks, P.A., Rifkind, R.A., Richon, V.M., Breslow, R., Miller, T., Kelly, W.K., Histone deacetylases and cancer: causes and therapies. Nat. Rev. Canc., 1, 2001, 194.
15. Jentsch, S., Pyrowolakis, G., Ubiquitin and its kin: how close are the family ties?. Trends Cell Biol. 10 (2000), 335–342.
16. Jeon, Y.J., Jo, M.G., Yoo, H.M., Hong, S.-H., Park, J.-M., Ka, S.H., Oh, K.H., Seol, J.H., Jung, Y.K., Chung, C.H., Chemosensitivity is controlled by p63 modification with ubiquitin-like protein ISG15. JCI (J. Clin. Investig.) 122 (2012), 2622–2636.
17. Jeon, Y.J., Yoo, H.M., Chung, C.H., ISG15 and immune diseases. Biochim. Biophys. Acta (BBA) - Mol. Basis Dis. 1802 (2010), 485–496.
18. Jeon, Y.J., Choi, J.S., Lee, J.Y., Yu, K.R., Kim, S.M., Ka, S.H., Oh, K.H., Kim, K.I., Zhang, D.E., Bang, O.S., ISG15 modification of filamin B negatively regulates the type I interferon‐induced JNK signalling pathway. EMBO Rep. 10 (2009), 374–380.
19. Perng, Y.-C., Lenschow, D.J., ISG15 in antiviral immunity and beyond. Nat. Rev. Microbiol., 2018, 1.
20. Haas, A.L., Ahrens, P., Bright, P., Ankel, H., Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J. Biol. Chem. 262 (1987), 11315–11323.
21. Der, S.D., Zhou, A., Williams, B.R., Silverman, R.H., Identification of genes differentially regulated by interferon α β or γ using oligonucleotide arrays. Proc. Natl. Acad. Sci. Unit. States Am. 95 (1998), 15623–15628.
22. Loeb, K.R., Haas, A.L., The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J. Biol. Chem. 267 (1992), 7806–7813.
23. Jeon, Y.J., Park, J.H., Chung, C.H., Interferon-stimulated gene 15 in the control of cellular responses to genotoxic stress. Mol. Cell., 40, 2017, 83.
24. Narasimhan, J., Wang, M., Fu, Z., Klein, J.M., Haas, A.A., Kim, J.-J.P., Crystal structure of the interferon-induced ubiquitin-like protein ISG15. J. Biol. Chem. 280 (2005), 27356–27365.
25. Yuan, W., Krug, R.M., Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)‐induced ubiquitin‐like ISG15 protein. EMBO J. 20 (2001), 362–371.
26. Radoshevich, L., Impens, F., Ribet, D., Quereda, J.J., Tham, T.N., Nahori, M.-A., Bierne, H., Dussurget, O., Pizarro-Cerdá J., Knobeloch, K.-P., ISG15 counteracts Listeria monocytogenes infection. Elife, 4, 2015, e06848.
27. Malakhova, O., Malakhov, M., Hetherington, C., Zhang, D.-E., Lipopolysaccharide activates the expression of ISG15-specific protease UBP43 via interferon regulatory factor 3. J. Biol. Chem. 277 (2002), 14703–14711.
28. Pitha-Rowe, I.F., Hassel, B.A., Dmitrovsky, E., Involvement of UBE1L in ISG15 conjugation during retinoid induced differentiation of acute Promyelocytic Leukemia. J. Biol. Chem. 279 (2004), 18178–18187.
29. Ochi, K., Daigo, Y., Katagiri, T., Nagayama, S., Tsunoda, T., Myoui, A., Naka, N., Araki, N., Kudawara, I., Ieguchi, M., Prediction of response to neoadjuvant chemotherapy for osteosarcoma by gene-expression profiles. Int. J. Oncol. 24 (2004), 647–655.
30. Qiu, K., Netravali, A.N., A review of fabrication and applications of bacterial cellulose based nanocomposites. Polym. Rev. 54 (2014), 598–626.
31. Knight, E., Cordova, B., IFN-induced 15-kDa protein is released from human lymphocytes and monocytes. J. Immunol. 146 (1991), 2280–2284.
32. D'Cunha, J., Ramanujam, S., Wagner, R.J., Witt, P.L., Knight, E., Borden, E.C., In vitro and in vivo secretion of human ISG15, an IFN-induced immunomodulatory cytokine. J. Immunol. 157 (1996), 4100–4108.
33. Lai, C., Struckhoff, J.J., Schneider, J., Martinez-Sobrido, L., Wolff, T., García-Sastre, A., Zhang, D.-E., Lenschow, D.J., Mice lacking the ISG15 E1 enzyme UbE1L demonstrate increased susceptibility to both mouse-adapted and non-mouse-adapted influenza B virus infection. J. Virol. 83 (2009), 1147–1151.
34. Guilbaud, G., Guilbaud, G., et al. PLoS Comput. Biol., 7, 2011, e1002322.
35. D'Cunha, J., Knight, E., Haas, A.L., Truitt, R.L., Borden, E.C., Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc. Natl. Acad. Sci. Unit. States Am. 93 (1996), 211–215.
36. Padovan, E., Terracciano, L., Certa, U., Jacobs, B., Reschner, A., Bolli, M., Spagnoli, G.C., Borden, E.C., Heberer, M., Interferon stimulated gene 15 constitutively produced by melanoma cells induces e-cadherin expression on human dendritic cells. Canc. Res. 62 (2002), 3453–3458.
37. Owhashi, M., Taoka, Y., Ishii, K., Nakazawa, S., Uemura, H., Kambara, H., Identification of a ubiquitin family protein as a novel neutrophil chemotactic factor. Biochem. Biophys. Res. Commun. 309 (2003), 533–539.
38. Zhang, X., Bogunovic, D., Payelle-Brogard, B., Francois-Newton, V., Speer, S.D., Yuan, C., Volpi, S., Li, Z., Sanal, O., Mansouri, D., Human intracellular ISG15 prevents interferon-α/β over-amplification and auto-inflammation. Nature, 517, 2015, 89.
39. Okumura, A., Pitha, P.M., Harty, R.N., ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc. Natl. Acad. Sci. Unit. States Am. 105 (2008), 3974–3979.
40. Rask-Andersen, M., Almén, M.S., Lind, L., Schiöth, H.B., Association of the LINGO2-related SNP rs10968576 with body mass in a cohort of elderly Swedes. Mol. Genet. Genom. 290 (2015), 1485–1491.
41. Desai, S.D., Reed, R.E., Burks, J., Wood, L.M., Pullikuth, A.K., Haas, A.L., Liu, L.F., Breslin, J.W., Meiners, S., Sankar, S., ISG15 disrupts cytoskeletal architecture and promotes motility in human breast cancer cells. Exp. Biol. Med. 237 (2012), 38–49.
42. Kiessling, A., Hogrefe, C., Erb, S., Bobach, C., Fuessel, S., Wessjohann, L., Seliger, B., Expression, regulation and function of the ISGylation system in prostate cancer. Oncogene, 28, 2009, 2606.
43. Li, C., Wang, J., Zhang, H., Zhu, M., Chen, F., Hu, Y., Liu, H., Zhu, H., Interferon-stimulated gene 15 (ISG15) is a trigger for tumorigenesis and metastasis of hepatocellular carcinoma. Oncotarget, 5, 2014, 8429.
44. Wood, L.M., Pan, Z.-K., Seavey, M.M., Muthukumaran, G., Paterson, Y., The ubiquitin-like protein, ISG15, is a novel tumor-associated antigen for cancer immunotherapy, Cancer immunology. Immunotherapy 61 (2012), 689–700.
45. Park, J.M., Yang, S.W., Yu, K.R., Ka, S.H., Lee, S.W., Seol, J.H., Jeon, Y.J., Chung, C.H., Modification of PCNA by ISG15 plays a crucial role in termination of error-prone translesion DNA synthesis. Mol. Cell 54 (2014), 626–638.
46. Potter, J.L., Narasimhan, J., Mende-Mueller, L., Haas, A.L., Precursor processing of pro-ISG15/UCRP, an interferon-β-induced ubiquitin-like protein. J. Biol. Chem. 274 (1999), 25061–25068.
47. Zhao, C., Beaudenon, S.L., Kelley, M.L., Waddell, M.B., Yuan, W., Schulman, B.A., Huibregtse, J.M., Krug, R.M., The UbcH8 ubiquitin E2 enzyme is also the E2 enzyme for ISG15, an IFN-α/β-induced ubiquitin-like protein. Proc. Natl. Acad. Sci. Unit. States Am. 101 (2004), 7578–7582.
48. Kim, K.I., Giannakopoulos, N.V., Virgin, H.W., Zhang, D.-E., Interferon-inducible ubiquitin E2, Ubc8, is a conjugating enzyme for protein ISGylation. Mol. Cell Biol. 24 (2004), 9592–9600.
49. Okumura, F., Zou, W., Zhang, D.-E., ISG15 modification of the eIF4E cognate 4EHP enhances cap structure-binding activity of 4EHP. Gene Dev. 21 (2007), 255–260.
50. Tan, N.G., Ardley, H.C., Scott, G.B., Rose, S.A., Markham, A.F., Robinson, P.A., Human homologue of ariadne promotes the ubiquitylation of translation initiation factor 4E homologous protein, 4EHP. FEBS Lett. 554 (2003), 501–504.
51. Zou, W., Zhang, D.-E., The interferon-inducible ubiquitin-protein isopeptide ligase (E3) EFP also functions as an ISG15 E3 ligase. J. Biol. Chem. 281 (2006), 3989–3994.
52. Zou, W., Wang, J., Zhang, D.-E., Negative regulation of ISG15 E3 ligase EFP through its autoISGylation. Biochem. Biophys. Res. Commun. 354 (2007), 321–327.
53. Dastur, A., Beaudenon, S., Kelley, M., Krug, R.M., Huibregtse, J.M., Herc5, an interferon-induced HECT E3 enzyme, is required for conjugation of ISG15 in human cells. J. Biol. Chem. 281 (2006), 4334–4338.
54. Wong, J.J.Y., Pung, Y.F., Sze, N.S.-K., Chin, K.-C., HERC5 is an IFN-induced HECT-type E3 protein ligase that mediates type I IFN-induced ISGylation of protein targets. Proc. Natl. Acad. Sci. Unit. States Am. 103 (2006), 10735–10740.
55. Malakhov, M.P., Malakhova, O.A., Kim, K.I., Ritchie, K.J., Zhang, D.-E., UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J. Biol. Chem. 277 (2002), 9976–9981.
56. Basters, A., Geurink, P.P., Röcker, A., Witting, K.F., Tadayon, R., Hess, S., Semrau, M.S., Storici, P., Ovaa, H., Knobeloch, K.-P., Structural basis of the specificity of USP18 toward ISG15. Nat. Struct. Mol. Biol., 24, 2017, 270.
57. François-Newton, V., de Freitas Almeida, G.M., Payelle-Brogard, B., Monneron, D., Pichard-Garcia, L., Piehler, J., Pellegrini, S., Uzé G., USP18-based negative feedback control is induced by type I and type III interferons and specifically inactivates interferon α response. PLoS One, 6, 2011, e22200.
58. Kang, D.-c., Jiang, H., Wu, Q., Pestka, S., Fisher, P.B., Cloning and characterization of human ubiquitin-processing protease-43 from terminally differentiated human melanoma cells using a rapid subtraction hybridization protocol RaSH. Gene 267 (2001), 233–242.
59. Li, L., Lei, Q.-s., Zhang, S.-J., Kong, L.-n., Qin, B., Suppression of USP18 potentiates the anti-HBV activity of interferon alpha in HepG2. 2.15 cells via JAK/STAT signaling. PLoS One, 11, 2016, e0156496.
60. Li, X.-L., Blackford, J.A., Judge, C.S., Liu, M., Xiao, W., Kalvakolanu, D.V., Hassel, B.A., Rnase-l-dependent destabilization of interferon-induced mRNAs a role for the 2–5A system IN attenuation OF the interferon response. J. Biol. Chem. 275 (2000), 8880–8888.
61. Kim, K.I., Malakhova, O.A., Hoebe, K., Yan, M., Beutler, B., Zhang, D.-E., Enhanced antibacterial potential in UBP43-deficient mice against Salmonella typhimurium infection by up-regulating type I IFN signaling. J. Immunol. 175 (2005), 847–854.
62. MacParland, S.A., Ma, X.-Z., Chen, L., Khattar, R., Cherepanov, V., Selzner, M., Feld, J.J., Selzner, N., McGilvray, I.D., LPS and TNF-α inhibit interferon-signaling in hepatocytes by increasing USP18 expression. J. Virol. 90 (2016), 5549–5560.
63. Yang, Z., Xian, H., Hu, J., Tian, S., Qin, Y., Wang, R.-F., Cui, J., USP18 negatively regulates NF-κB signaling by targeting TAK1 and NEMO for deubiquitination through distinct mechanisms. Sci. Rep., 5, 2015, 12738.
64. Tokarz, S., Berset, C., La Rue, J., Friedman, K., Nakayama, K.-I., Nakayama, K., Zhang, D.-E., Lanker, S., The ISG15 isopeptidase UBP43 is regulated by proteolysis via the SCFSkp2 ubiquitin ligase. J. Biol. Chem. 279 (2004), 46424–46430.
65. Frescas, D., Pagano, M., Deregulated proteolysis by the F-box proteins SKP2 and β-TrCP: tipping the scales of cancer. Nat. Rev. Canc., 8, 2008, 438.
66. Malakhova, O.A., Kim, K.I., Luo, J.K., Zou, W., Kumar, K.S., Fuchs, S.Y., Shuai, K., Zhang, D.E., UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J. 25 (2006), 2358–2367.
67. Arimoto, K.-i., Löchte, S., Stoner, S.A., Burkart, C., Zhang, Y., Miyauchi, S., Wilmes, S., Fan, J.-B., Heinisch, J.J., Li, Z., STAT2 is an essential adaptor in USP18-mediated suppression of type I interferon signaling. Nat. Struct. Mol. Biol., 24, 2017, 279.
68. Giannakopoulos, N.V., Luo, J.-K., Papov, V., Zou, W., Lenschow, D.J., Jacobs, B.S., Borden, E.C., Li, J., Virgin, H.W., Zhang, D.-E., Proteomic identification of proteins conjugated to ISG15 in mouse and human cells. Biochem. Biophys. Res. Commun. 336 (2005), 496–506.
69. Zhao, C., Denison, C., Huibregtse, J.M., Gygi, S., Krug, R.M., Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc. Natl. Acad. Sci. Unit. States Am. 102 (2005), 10200–10205.
70. Bogunovic, D., Byun, M., Durfee, L.A., Abhyankar, A., Sanal, O., Mansouri, D., Salem, S., Radovanovic, I., Grant, A.V., Adimi, P., Mycobacterial disease and impaired IFN-γ immunity in humans with inherited ISG15 deficiency. Science 337 (2012), 1684–1688.
71. Care, M.A., Stephenson, S.J., Barnes, N.A., Fan, I., Zougman, A., El-Sherbiny, Y.M., Vital, E.M., Westhead, D.R., Tooze, R.M., Doody, G.M., Network analysis identifies proinflammatory plasma cell polarization for secretion of ISG15 in human autoimmunity. J. Immunol., 2016, 1600624.
72. Hoan, N.X., Van Tong, H., Giang, D.P., Toan, N.L., Meyer, C.G., Bock, C.-T., Kremsner, P.G., Song, L.H., Velavan, T.P., Interferon-stimulated gene 15 in hepatitis B-related liver diseases. Oncotarget, 7, 2016, 67777.
73. Recht, M., Borden, E.C., Knight, E., A human 15-kDa IFN-induced protein induces the secretion of IFN-gamma. J. Immunol. 147 (1991), 2617–2623.
74. Knight, E., Fahey, D., Cordova, B., Hillman, M., Kutny, R., Reich, N., Blomstrom, D., A 15-kDa interferon-induced protein is derived by COOH-terminal processing of a 17-kDa precursor. J. Biol. Chem. 263 (1988), 4520–4522.
75. Sun, L., Wang, X., Zhou, Y., Zhou, R.-H., Ho, W.-Z., Li, J.-L., Exosomes contribute to the transmission of anti-HIV activity from TLR3-activated brain microvascular endothelial cells to macrophages. Antivir. Res. 134 (2016), 167–171.
76. dos Santos, P.F., Mansur, D.S., Beyond ISGlylation: functions of free intracellular and extracellular ISG15. J. Interferon Cytokine Res. 37 (2017), 246–253.
77. Swaim, C.D., Scott, A.F., Canadeo, L.A., Huibregtse, J.M., Extracellular ISG15 signals cytokine secretion through the LFA-1 integrin receptor. Mol. Cell, 68, 2017, e585 581-590.
78. Yoo, Y.S., Han, H.G., Jeon, Y.J., Unfolded protein response of the endoplasmic reticulum in tumor progression and immunogenicity. Oxidative medicine and cellular longevity, 2017, 2017.
79. Balchin, D., Hayer-Hartl, M., Hartl, F.U., Vivo Aspects of Protein Folding and Quality Control, Science, vol. 353, 2016 aac4354.
80. Nillegoda, N.B., Wentink, A.S., Bukau, B., Protein disaggregation in multicellular organisms. Trends Biochem. Sci. 43 (2018), 285–300.
81. Okumura, F., Okumura, A.J., Uematsu, K., Hatakeyama, S., Zhang, D.-E., Kamura, T., Activation of double-stranded RNA-activated protein kinase (PKR) by interferon stimulated gene 15 (ISG15) modification down-regulates protein translation. J. Biol. Chem. 288 (2012), 2839–2847.
82. Durfee, L.A., Lyon, N., Seo, K., Huibregtse, J.M., The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol. Cell 38 (2010), 722–732.
83. Zhao, C., Sridharan, H., Chen, R., Baker, D.P., Wang, S., Krug, R.M., Influenza B virus non-structural protein 1 counteracts ISG15 antiviral activity by sequestering ISGylated viral proteins. Nat. Commun., 7, 2016, 12754.
84. Rahnefeld, A., Klingel, K., Schuermann, A., Diny, N.L., Althof, N., Lindner, A., Bleienheuft, P., Savvatis, K., Respondek, D., Opitz, E., Ubiquitin-like protein ISG15 in host defense against heart failure in a mouse model of virus-induced cardiomyopathy. Circulation 130 (2014), 1589–1600.
85. Desai, S., Juncker, M., Kim, C., Regulation of mitophagy by the ubiquitin pathway in neurodegenerative diseases. Exp. Biol. Med. 243 (2018), 554–562.
86. Liu, M., Li, X.-L., Hassel, B.A., Proteasomes modulate conjugation to the ubiquitin-like protein, ISG15. J. Biol. Chem. 278 (2003), 1594–1602.
87. Wood, L.M., Sankar, S., Reed, R.E., Haas, A.L., Liu, L.F., McKinnon, P., Desai, S.D., A novel role for ATM in regulating proteasome-mediated protein degradation through suppression of the ISG15 conjugation pathway. PLoS One, 6, 2011, e16422.
88. Shi, H.-X., Yang, K., Liu, X., Liu, X.-Y., Wei, B., Shan, Y.-F., Zhu, L.-H., Wang, C., Positive regulation of interferon regulatory factor 3 activation by Herc5 via ISG15 modification. Mol. Cell Biol. 30 (2010), 2424–2436.
89. Desai, S.D., Haas, A.L., Wood, L.M., Tsai, Y.-C., Pestka, S., Rubin, E.H., Saleem, A., Nur-E-Kamal, A., Liu, L.F., Elevated expression of ISG15 in tumor cells interferes with the ubiquitin/26S proteasome pathway. Canc. Res. 66 (2006), 921–928.
90. Fan, J.-B., Arimoto, K.-l., Motamedchaboki, K., Yan, M., Wolf, D.A., Zhang, D.-E., Identification and characterization of a novel ISG15-ubiquitin mixed chain and its role in regulating protein homeostasis. Sci. Rep., 5, 2015, 12704.
91. Malakhova, O.A., Zhang, D.-E., ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response. J. Biol. Chem. 283 (2008), 8783–8787.
92. Yoo, L., Yoon, A.-R., Yun, C.-O., Chung, K.C., Covalent ISG15 conjugation to CHIP promotes its ubiquitin E3 ligase activity and inhibits lung cancer cell growth in response to type I interferon. Cell Death Dis., 9, 2018, 97.
93. Tanaka, K., Matsuda, N., Proteostasis and neurodegeneration: the roles of proteasomal degradation and autophagy. Biochim. Biophys. Acta Mol. Cell Res. 1843 (2014), 197–204.
94. Nixon, R.A., The role of autophagy in neurodegenerative disease. Nat. Med., 19, 2013, 983.
95. Wong, E., Cuervo, A.M., Integration of clearance mechanisms: the proteasome and autophagy. Cold Spring Harbor perspectives in biology, 2, 2010, a006734.
96. Khaminets, A., Behl, C., Dikic, I., Ubiquitin-dependent and independent signals in selective autophagy. Trends Cell Biol. 26 (2016), 6–16.
97. Nakashima, H., Nguyen, T., Goins, W.F., Chiocca, E.A., ISG15 and ISG-15 linked proteins can associate with members of the selective autophagic process, HDAC6 and SQSTM1/p62. J. Biol. Chem. 290 (2014), 1485–1495.
98. Kawaguchi, Y., Kovacs, J.J., McLaurin, A., Vance, J.M., Ito, A., Yao, T.-P., The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115 (2003), 727–738.
99. Lee, J.Y., Koga, H., Kawaguchi, Y., Tang, W., Wong, E., Gao, Y.S., Pandey, U.B., Kaushik, S., Tresse, E., Lu, J., HDAC6 controls autophagosome maturation essential for ubiquitin‐selective quality‐control autophagy. EMBO J. 29 (2010), 969–980.
100. Katzenell, S., Leib, D.A., Herpes simplex virus and interferon signaling induce novel autophagic clusters in sensory neurons. J. Virol. 90 (2016), 4706–4719.
101. Baldanta, S., Fernández-Escobar, M., Acín-Perez, R., Albert, M., Camafeita, E., Jorge, I., Vázquez, J., Enríquez, J.A., Guerra, S., ISG15 governs mitochondrial function in macrophages following vaccinia virus infection. PLoS Pathog., 13, 2017, e1006651.
102. Villarroya-Beltri, C., Baixauli, F., Mittelbrunn, M., Fernández-Delgado, I., Torralba, D., Moreno-Gonzalo, O., Baldanta, S., Enrich, C., Guerra, S., Sánchez-Madrid, F., ISGylation controls exosome secretion by promoting lysosomal degradation of MVB proteins. Nat. Commun., 7, 2016, 13588.
103. Blanchard, N., Lankar, D., Faure, F., Regnault, A., Dumont, C., Raposo, G., Hivroz, C., TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/ζ complex. J. Immunol. 168 (2002), 3235–3241.
104. Van der Vlist, E.J., Arkesteijn, G.J., van de Lest, C.H., Stoorvogel, W., Nolte-’t Hoen, E.N., Wauben, M.H., CD4+ T cell activation promotes the differential release of distinct populations of nanosized vesicles. J. Extracell. Vesicles, 1, 2012, 18364.
105. Villarroya-Beltri, C., Baixauli, F., Gutiérrez-Vázquez, C., Sánchez-Madrid, F., Mittelbrunn, M., Sorting it Out: Regulation of Exosome Loading, Seminars in Cancer Biology. 2014, Elsevier, 3–13.
106. Moreno-Gonzalo, O., Villarroya-Beltri, C., Sánchez-Madrid, F., Post-translational modifications of exosomal proteins. Front. Immunol., 5, 2014, 383.
107. Nabhan, J.F., Hu, R., Oh, R.S., Cohen, S.N., Lu, Q., Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc. Natl. Acad. Sci. Unit. States Am. 109 (2012), 4146–4151.
108. Putz, U., Howitt, J., Lackovic, J., Foot, N., Kumar, S., Silke, J., Tan, S.-S., Nedd4 family-interacting protein 1 (Ndfip1) is required for the exosomal secretion of Nedd4 family proteins. J. Biol. Chem. 283 (2008), 32621–32627.
109. Villarroya-Beltri, C., Gutiérrez-Vázquez, C., Sánchez-Cabo, F., Pérez-Hernández, D., Vázquez, J., Martin-Cofreces, N., Martinez-Herrera, D.J., Pascual-Montano, A., Mittelbrunn, M., Sánchez-Madrid, F., Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat. Commun., 4, 2013, 2980.
110. Andreola, G., Rivoltini, L., Castelli, C., Huber, V., Perego, P., Deho, P., Squarcina, P., Accornero, P., Lozupone, F., Lugini, L., Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J. Exp. Med. 195 (2002), 1303–1316.
111. Théry, C., Duban, L., Segura, E., Véron, P., Lantz, O., Amigorena, S., Indirect activation of naïve CD4+ T cells by dendritic cell–derived exosomes. Nat. Immunol., 3, 2002, 1156.
112. Frühbeis, C., Fröhlich, D., Kuo, W.P., Amphornrat, J., Thilemann, S., Saab, A.S., Kirchhoff, F., Möbius, W., Goebbels, S., Nave, K.-A., Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte–neuron communication. PLoS Biol., 11, 2013, e1001604.
113. Chalmin, F., Ladoire, S., Mignot, G., Vincent, J., Bruchard, M., Remy-Martin, J.-P., Boireau, W., Rouleau, A., Simon, B., Lanneau, D., Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. JCI (J. Clin. Investig.) 120 (2010), 457–471.
114. Peinado, H., Alečković M., Lavotshkin, S., Matei, I., Costa-Silva, B., Moreno-Bueno, G., Hergueta-Redondo, M., Williams, C., García-Santos, G., Ghajar, C.M., Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med., 18, 2012, 883.
115. Du, Y., Duan, T., Feng, Y., Liu, Q., Lin, M., Cui, J., Wang, R.F., LRRC25 inhibits type I IFN signaling by targeting ISG15‐associated RIG‐I for autophagic degradation. EMBO J. 37 (2018), 351–366.
116. Xu, D., Zhang, T., Xiao, J., Zhu, K., Wei, R., Wu, Z., Meng, H., Li, Y., Yuan, J., Modification of BECN1 by ISG15 plays a crucial role in autophagy regulation by type I IFN/interferon. Autophagy 11 (2015), 617–628.
117. Abrahamsen, H., Stenmark, H., Platta, H.W., Ubiquitination and phosphorylation of Beclin 1 and its binding partners: tuning class III phosphatidylinositol 3-kinase activity and tumor suppression. FEBS Lett. 586 (2012), 1584–1591.
118. Lai, C.-H., Hahm, H.S., Liang, C.-F., Seeberger, P.H., Automated solid-phase synthesis of oligosaccharides containing sialic acids. Beilstein J. Org. Chem., 11, 2015, 617.
119. Costantini, E., Lazzeri, M., Surgery for stress urinary incontinence: so near and yet so far. Eur. Urol. 59 (2011), 945–946.
120. Ren-Gang, W., Marcus, K., Dong-Xian, Z., Interferon-stimulated gene 15 as a general marker for acute and chronic neuronal injuries. Sheng li xue bao:[Acta physiologica Sinica], 64, 2012, 577.
121. Desai, S.D., Reed, R.E., Babu, S., Lorio, E.A., ISG15 deregulates autophagy in genotoxin-treated ataxia telangiectasia cells. J. Biol. Chem. 288 (2013), 2388–2402.
122. Feng, Q., Sekula, D., Guo, Y., Liu, X., Black, C.C., Galimberti, F., Shah, S.J., Sempere, L.F., Memoli, V., Andersen, J.B., UBE1L causes lung cancer growth suppression by targeting cyclin D1. Mol. Canc. Therapeut. 7 (2008), 3780–3788.
123. Desai, S.D., ISG15: a double edged sword in cancer. OncoImmunology, 4, 2015, e1052935.
124. Cheon, H., Borden, E.C., Stark, G.R., Interferons and Their Stimulated Genes in the Tumor Microenvironment, Seminars in Oncology. 2014, Elsevier, 156–173.
125. Lee, G.-Y., Kim, J.-A., Oh, I.-H., Stem cell niche as a prognostic factor in leukemia. BMB reports, 48, 2015, 427.
126. Honke, N., Shaabani, N., Zhang, D.-E., Hardt, C., Lang, K.S., Multiple functions of USP18. Cell Death Dis., 7, 2016, e2444.
127. Mustachio, L.M., Kawakami, M., Lu, Y., Rodriguez-Canales, J., Mino, B., Behrens, C., Wistuba, I., Bota-Rabassedas, N., Yu, J., Lee, J.J., The ISG15-specific protease USP18 regulates stability of PTEN. Oncotarget, 8, 2017, 3.
128. Guo, Y., Chinyengetere, F., Dolinko, A.V., Lopez-Aguiar, A., Lu, Y., Galimberti, F., Ma, T., Feng, Q., Sekula, D., Freemantle, S.J., Evidence for the ubiquitin protease UBP43 as an antineoplastic target. Mol. Canc. Therapeut. 11 (2012), 1968–1977.
129. Kim, Y.-H., Kim, W.T., Jeong, P., Ha, Y.-S., Kang, H.W., Yun, S.J., Moon, S.-K., Choi, Y.H., Kim, I.Y., Kim, W.-J., Novel combination markers for predicting survival in patients with muscle invasive bladder cancer: USP18 and DGCR2. J. Kor. Med. Sci. 29 (2014), 351–356.
130. Duex, J.E., Comeau, L., Sorkin, A., Purow, B., Kefas, B., Usp18 regulates epidermal growth factor (EGF) receptor expression and cancer cell survival via microRNA-7. J. Biol. Chem. 286 (2011), 25377–25386.
131. GuoY, A. Dolinko, Chinyengetere, F., Blockade of the ubiquitin protease UBP43 destabilizes transcription factor PML/RAR alpha and inhibits the gowth of acute promyelocytic leukemia. Canc. Res., 70, 2010, 9875.
132. Mustachio, L.M., Lu, Y., Tafe, L.J., Memoli, V., Rodriguez-Canales, J., Mino, B., Villalobos, P.A., Wistuba, I., Katayama, H., Hanash, S.M., Deubiquitinase USP18 loss mislocalizes and destabilizes KRAS in lung cancer. Mol. Canc. Res. 15 (2017), 905–914.
133. Yan, M., Luo, J.-K., Ritchie, K.J., Sakai, I., Takeuchi, K., Ren, R., Zhang, D.-E., Ubp43 regulates BCR-ABL leukemogenesis via the type 1 interferon receptor signaling. Blood 110 (2007), 305–312.
134. Sgorbissa, A., Tomasella, A., Potu, H., Manini, I., Brancolini, C., Type I IFNs signaling and apoptosis resistance in glioblastoma cells. Apoptosis, 16, 2011, 1229.
135. Yeh, Y.-H., Yang, Y.-C., Hsieh, M.-Y., Yeh, Y.-C., Li, T.-K., A negative feedback of the HIF-1α pathway via interferon-stimulated gene 15 and ISGylation. Clin. Canc. Res. 19 (2013), 5927–5939.
136. Hadjivasiliou, A., ISG15 implicated in cytoskeleton disruption and promotion of breast cancer. Expet Rev. Proteonomics, 9, 2012, 7.
137. Forys, J.T., Kuzmicki, C.E., Saporita, A.J., Winkeler, C.L., Maggi, L.B., Weber, J.D., ARF and p53 coordinate tumor suppression of an oncogenic IFN-β-STAT1-ISG15 signaling axis. Cell Rep. 7 (2014), 514–526.
138. Bektas, N., Noetzel, E., Veeck, J., Press, M.F., Kristiansen, G., Naami, A., Hartmann, A., Dimmler, A., Beckmann, M.W., Knüchel, R., The ubiquitin-like molecule interferon-stimulated gene 15 (ISG15) is a potential prognostic marker in human breast cancer. Breast Canc. Res., 10, 2008, R58.
139. Lo, P.-K., Yao, Y., Lee, J.S., Zhang, Y., Huang, W., Kane, M.A., Zhou, Q., LIPG signaling promotes tumor initiation and metastasis of human basal-like triple-negative breast cancer. eLife, 7, 2018, e31334.
140. Burks, J., Reed, R., Desai, S., ISGylation governs the oncogenic function of Ki-Ras in breast cancer. Oncogene, 33, 2014, 794.
141. Cerikan, B., Schiebel, E., DOCK6 inactivation highlights ISGylation as RHO-GTPase balancer. Cell Cycle, 16, 2017, 304.
142. Hollingsworth, J., Lau, A., Tone, A., Kollara, A., Allen, L., Colgan, T.J., Dube, V., Rosen, B., Murphy, K.J., Greenblatt, E.M., BRCA1 mutation status and follicular fluid exposure alters NFκB signaling and ISGylation in human fallopian tube epithelial cells. Neoplasia 20 (2018), 697–709.
143. Qiu, X., Hong, Y., Yang, D., Xia, M., Zhu, H., Li, Q., Xie, H., Wu, Q., Liu, C., Zuo, C., ISG15 as a novel prognostic biomarker for hepatitis B virus-related hepatocellular carcinoma. Int. J. Clin. Exp. Med., 8, 2015, 17140.
144. Brown, A.R., Simmen, R.C., Raj, V.R., Van, T.T., MacLeod, S.L., Simmen, F.A., Krüppel-like factor 9 (KLF9) prevents colorectal cancer through inhibition of interferon-related signaling. Carcinogenesis 36 (2015), 946–955.
145. Fan, J.-B., Miyauchi-Ishida, S., Arimoto, K.-i., Liu, D., Yan, M., Liu, C.-W., Győrffy, B., Zhang, D.-E., Type I IFN induces protein ISGylation to enhance cytokine expression and augments colonic inflammation. Proc. Natl. Acad. Sci. Unit. States Am. 112 (2015), 14313–14318.
146. Lee, J.H., Bae, J.A., Lee, J.H., Seo, Y.-W., Kho, D.H., Sun, E.G., Lee, S.E., Cho, S.H., Joo, Y.E., Ahn, K.Y., Glycoprotein 90K, downregulated in advanced colorectal cancer tissues, interacts with CD9/CD82 and suppresses the Wnt/β-catenin signal via ISGylation of β-catenin. Gut 59 (2010), 907–917.
147. Kim, S.T., Sohn, I., Do, I.-G., Jang, J., Kim, S.H., JUNG, S.H., Park, J.O., Park, Y.S., Talasaz, A., Lee, J., Transcriptome analysis of CD133-positive stem cells and prognostic value of survivin in colorectal cancer. CANCER GENOMICS PROTEOMICS 11 (2014), 259–266.
148. O'Brien, C.A., Pollett, A., Gallinger, S., Dick, J.E., A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature, 445, 2007, 106.
149. Ricci-Vitiani, L., Lombardi, D.G., Pilozzi, E., Biffoni, M., Todaro, M., Peschle, C., De Maria, R., Identification and expansion of human colon-cancer-initiating cells. Nature, 445, 2007, 111.
150. Singh, S.K., Hawkins, C., Clarke, I.D., Squire, J.A., Bayani, J., Hide, T., Henkelman, R.M., Cusimano, M.D., Dirks, P.B., Identification of human brain tumour initiating cells. Nature, 432, 2004, 396.
151. Chen, R.-H., Du, Y., Han, P., Wang, H.-B., Liang, F.-Y., Feng, G.-K., Zhou, A.-J., Cai, M.-Y., Zhong, Q., Zeng, M.-S., ISG15 predicts poor prognosis and promotes cancer stem cell phenotype in nasopharyngeal carcinoma. Oncotarget, 7, 2016, 16910.
152. Yan, W., Shih, J.H., Rodriguez-Canales, J., Tangrea, M.A., Ylaya, K., Hipp, J., Player, A., Hu, N., Goldstein, A.M., Taylor, P.R., Identification of unique expression signatures and therapeutic targets in esophageal squamous cell carcinoma. BMC Res. Notes, 5, 2012, 73.
153. Tao, J., Hua, P., Wen, J., Hu, Y., Yang, H., Xie, X., Prognostic value of ISG15 mRNA level in drinkers with esophageal squamous cell cancers. Int. J. Clin. Exp. Pathol., 8, 2015, 10975.
154. Jinawath, N., Furukawa, Y., Hasegawa, S., Li, M., Tsunoda, T., Satoh, S., Yamaguchi, T., Imamura, H., Inoue, M., Shiozaki, H., Comparison of gene-expression profiles between diffuse-and intestinal-type gastric cancers using a genome-wide cDNA microarray. Oncogene, 23, 2004, 6830.
155. Shen, J., Wei, J., Wang, H., Yue, G., Yu, L., Yang, Y., Xie, L., Zou, Z., Qian, X., Ding, Y., A three-gene signature as potential predictive biomarker for irinotecan sensitivity in gastric cancer. J. Transl. Med., 11, 2013, 73.
156. Farrell, P.J., Broeze, R.J., Lengyel, P., Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells. Nature, 279, 1979, 523.
157. Burkart, C., Arimoto, K.i., Tang, T., Cong, X., Xiao, N., Liu, Y.C., Kotenko, S.V., Ellies, L.G., Zhang, D.E., Usp18 deficient mammary epithelial cells create an antitumour environment driven by hypersensitivity to IFN‐λ and elevated secretion of Cxcl10. EMBO Mol. Med. 5 (2013), 1035–1050.
158. Hong, B., Li, H., Lu, Y., Zhang, M., Zheng, Y., Qian, J., Yi, Q., USP18 is crucial for IFN-γ-mediated inhibition of B16 melanoma tumorigenesis and antitumor immunity. Mol. Canc., 13, 2014, 132.
159. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., Sica, A., Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23 (2002), 549–555.
160. Zeng, Z., Xu, X., Zhang, Y., Xing, J., Long, J., Gu, L., Wang, X., Sun, D., Ka, W., Yao, W., Tumor‐derived factors impaired motility and immune functions of dendritic cells through derangement of biophysical characteristics and reorganization of cytoskeleton. Cell Motil Cytoskeleton 64 (2007), 186–198.
161. Sainz, B., Martín, B., Tatari, M., Heeschen, C., Guerra, S., ISG15 is a critical microenvironmental factor for pancreatic cancer stem cells. Canc. Res. 74 (2014), 7309–7320.
162. Villarreal, D.O., Wise, M.C., Siefert, R.J., Yan, J., Wood, L.M., Weiner, D.B., Ubiquitin-like molecule ISG15 acts as an immune adjuvant to enhance antigen-specific CD8 T-cell tumor immunity. Mol. Ther. 23 (2015), 1653–1662.
163. Weichselbaum, R.R., Ishwaran, H., Yoon, T., Nuyten, D.S., Baker, S.W., Khodarev, N., Su, A.W., Shaikh, A.Y., Roach, P., Kreike, B., An interferon-related gene signature for DNA damage resistance is a predictive marker for chemotherapy and radiation for breast cancer. Proc. Natl. Acad. Sci. Unit. States Am. 105 (2008), 18490–18495.
164. Desai, S.D., Wood, L.M., Tsai, Y.-C., Hsieh, T.-S., Marks, J.R., Scott, G.L., Giovanella, B.C., Liu, L.F., ISG15 as a novel tumor biomarker for drug sensitivity. Mol. Canc. Therapeut. 7 (2008), 1430–1439.
165. Chun, J.H., Kim, H.K., Kim, E., Kim, I.-H., Kim, J.H., Chang, H.J., Choi, I.J., Lim, H.-S., Kim, I.-J., Kang, H.C., Increased expression of metallothionein is associated with irinotecan resistance in gastric cancer. Canc. Res. 64 (2004), 4703–4706.
166. Park, J.H., Yang, S.W., Park, J.M., Ka, S.H., Kim, J.-H., Kong, Y.-Y., Jeon, Y.J., Seol, J.H., Chung, C.H., Positive feedback regulation of p53 transactivity by DNA damage-induced ISG15 modification. Nat. Commun., 7, 2016, 12513.
167. Roulois, D., Yau, H.L., Singhania, R., Wang, Y., Danesh, A., Shen, S.Y., Han, H., Liang, G., Jones, P.A., Pugh, T.J., DNA-demethylating agents target colorectal cancer cells by inducing viral mimicry by endogenous transcripts. Cell 162 (2015), 961–973.
168. Ina, S., Hirono, S., Noda, T., Yamaue, H., Identifying molecular markers for chemosensitivity to gemcitabine in pancreatic cancer: increased expression of interferon-stimulated gene 15 kd is associated with intrinsic chemoresistance. Pancreas 39 (2010), 473–485.
169. Khodarev, N.N., Beckett, M., Labay, E., Darga, T., Roizman, B., Weichselbaum, R.R., STAT1 is overexpressed in tumors selected for radioresistance and confers protection from radiation in transduced sensitive cells. Proc. Natl. Acad. Sci. Unit. States Am. 101 (2004), 1714–1719.
170. Boelens, M.C., Wu, T.J., Nabet, B.Y., Xu, B., Qiu, Y., Yoon, T., Azzam, D.J., Twyman-Saint Victor, C., Wiemann, B.Z., Ishwaran, H., Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. Cell 159 (2014), 499–513.
171. Speer, S., Li, Z., Buta, S., Payelle-Brogard, B., Qian, L., Vigant, F., Rubino, E., Gardner, T., Wedeking, T., Hermann, M., ISG15 deficiency and increased viral resistance in humans but not mice. Nat. Commun., 7, 2016, 11496.