USP18-mediated protein deISGylation and its role in tuberculosis and other infectious diseases
Received date: 2023-07-07
Revised date: 2023-10-17
Online published: 2023-11-01
Supported by
National Natural Science Foundation of China(82211530059);National Natural Science Foundation of China(82072246)
The transcription of interferon-stimulated gene 15 (isg15) is induced by type I interferons. ISG15 can covalently modify target proteins through the sequential action of enzymesE1, E2, and E3, a process known as ISGylation. The ISGylation of host proteins is widely involved in immune responses, such as host antiviral defence. Ubiquitin-specific protease 18 (USP18), as a deubiquitinase (DUB), can remove ISG15 conjugated to target proteins and inhibit host immune responses by suppressing the type I interferon signaling. The dynamic balance between ISGylation and deISGylation mediated by ISG15 or USP18 respectively plays a significant role in the tuberculosis. Furthermore, similar to ISG15, USP18 is extensively involved in virus-host interaction. In this review, we summarize the roles of ISGylation and deISGylation in tuberculosis and other important diseases mediated by ISG15 and USP18 respectively, underlying regulator network. Further studies in this aspect will inspire new host-targeted strategies to control important diseases such as tuberculosis.
Key words： USP18; ISG15; tuberculosis
Qi’ao Zhang, Zilu Wang, Peibo Li, Jianping Xie . USP18-mediated protein deISGylation and its role in tuberculosis and other infectious diseases[J]. Hereditas(Beijing), 2023 , 45(11) : 998 -1006 . DOI: 10.16288/j.yczz.23-185
| [1] | Reyes-Turcu FE, Ventii KH, Wilkinson KD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem, 2009, 78: 363-397. |
| [2] | Li ZB, Wang DK, Messing EM, Wu G. VHL protein- interacting deubiquitinating enzyme 2 deubiquitinates and stabilizes HIF-1alpha. EMBO Rep, 2005, 6(4): 373-378. |
| [3] | Berthouze M, Venkataramanan V, Li Y, Shenoy SK. The deubiquitinases USP33 and USP20 coordinate beta2 adrenergic receptor recycling and resensitization. EMBO J, 2009, 28(12): 1684-1696. |
| [4] | Yasunaga J, Lin FC, Lu XB, Jeang KT. Ubiquitin-specific peptidase 20 targets TRAF6 and human T cell leukemia virus type 1 tax to negatively regulate NF-kappaB signaling. J Virol, 2011, 85(13): 6212-6219. |
| [5] | Yuan J, Luo KT, Deng M, Li YH, Yin P, Gao BW, Fang Y, Wu PQ, Liu TZ, Lou ZK. HERC2-USP20 axis regulates DNA damage checkpoint through Claspin. Nucleic Acids Res, 2014, 42(21): 13110-13121. |
| [6] | Zhu M, Zhao HC, Liao J, Xu XZ. HERC2/USP20 coordinates CHK1 activation by modulating CLASPIN stability. Nucleic Acids Res, 2014, 42(21): 13074-13081. |
| [7] | Malakhov MP, Malakhova OA, Kim KI, Ritchie KJ, Zhang DE. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J Biol Chem, 2002, 277(12): 9976-9981. |
| [8] | Schwer H, Liu LQ, Zhou L, Little MT, Pan Z, Hetherington CJ, Zhang DE. Cloning and characterization of a novel human ubiquitin-specific protease, a homologue of murine UBP43 (Usp18). Genomics, 2000, 65(1): 44-52. |
| [9] | Ritchie KJ, Malakhov MP, Hetherington CJ, Zhou LM, Little MT, Malakhova OA, Sipe JC, Orkin SH, Zhang DE. Dysregulation of protein modification by ISG15 results in brain cell injury. Genes Dev, 2002, 16(17): 2207-2212. |
| [10] | Ketscher L, Hann? R, Morales DJ, Basters A, Guerra S, Goldmann T, Hausmann A, Prinz M, Naumann R, Pekosz A, Uterm?hlen O, Lenschow DJ, Knobeloch KP. Selective inactivation of USP18 isopeptidase activity in vivo enhances ISG15 conjugation and viral resistance. Proc Natl Acad Sci USA, 2015, 112(5): 1577-1582. |
| [11] | Ritchie KJ, Hahn CS, Kim KI, Yan M, Rosario D, Li L, de la Torre JC, Zhang DE. Role of ISG 15 protease UBP43 (USP18) in innate immunity to viral infection. Nat Med, 2004, 10(12): 1374-1378. |
| [12] | Potter JL, Narasimhan J, Mende-Mueller L, Haas AL. Precursor processing of pro-ISG15/UCRP, an interferon- beta-induced ubiquitin-like protein. J Biol Chem, 1999, 274(35): 25061-25068. |
| [13] | Li XL, Blackford JA, Judge CS, Liu M, Xiao W, Kalvakolanu DV, Hassel BA.RNase-L-dependent destabilization of interferon-induced mRNAs. A role for the 2-5 A system in attenuation of the interferon response. J Biol Chem, 2000, 275(12): 8880-8888. |
| [14] | Malakhova OA, Yan M, Malakhov MP, Yuan YZ, Ritchie KJ, Kim KI, Peterson LF, Shuai K, Zhang DE. Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev, 2003, 17(4): 455-460. |
| [15] | Malakhova O, Malakhov M, Hetherington C, Zhang DE.Lipopolysaccharide activates the expression of ISG15-specific protease UBP 43 via interferon regulatory factor 3. J Biol Chem, 2002, 277(17): 14703-14711. |
| [16] | Tokarz S, Berset C, La Rue J, Friedman K, Nakayama KI, Nakayama K, Zhang DE, Lanker S. The ISG 15 isopeptidase UBP43 is regulated by proteolysis via the SCFSkp2 ubiquitin ligase. J Biol Chem, 2004, 279(45): 46424-46430. |
| [17] | Li L, Lei QS, Zhang SJ, Kong LN, Qin B. Suppression of USP 18 potentiates the anti-HBV activity of interferon alpha in HepG2.2.15 cells via JAK/STAT signaling. Plos One, 2016, 11(5): e0156496. |
| [18] | Malakhova OA, Kim KI, Luo JK, Zou WG, Kumar KGS, Fuchs SY, Shuai K, Zhang DE. UBP 43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J, 2006, 25(11): 2358-2367. |
| [19] | Knobeloch KP, Uterm?hlen O, Kisser A, Prinz M, Horak I. Reexamination of the role of ubiquitin-like modifier ISG15 in the phenotype of UBP43-deficient mice. Mol Cell Biol, 2005, 25(24): 11030-11034. |
| [20] | Osiak A, Uterm?hlen O, Niendorf S, Horak I, Knobeloch KP. ISG15, an interferon-stimulated ubiquitin-like protein, is not essential for STAT1 signaling and responses against vesicular stomatitis and lymphocytic choriomeningitis virus. Mol Cell Biol, 2005, 25(15): 6338-6345. |
| [21] | Kim KI, Yan M, Malakhova O, Luo JK, Shen MF, Zou WG, de la Torre JC, Zhang DE. Ube1L and protein ISGylation are not essential for alpha/beta interferon signaling. Mol Cell Biol, 2006, 26(2): 472-479. |
| [22] | Arimoto KI, L?chte S, Stoner SA, Burkart C, Zhang Y, Miyauchi S, Wilmes S, Fan JB, Heinisch JJ, Li Z, Yan M, Pellegrini S, Colland F, Piehler J, Zhang DE. STAT2 is an essential adaptor in USP18-mediated suppression of type I interferon signaling. Nat Struct Mol Biol, 2017, 24(3): 279-289. |
| [23] | Liu NX, Pang XX, Zhang H, Ji P. The cGAS-STING pathway in bacterial infection and bacterial immunity. Front Immunol, 2021, 12: 814709. |
| [24] | Bomfim CCB, Fisher L, Amaral EP, Mittereder L, McCann K, Correa AAS, Namasivayam S, Swamydas M, Moayeri M, Weiss JM, Chari R, McVicar DW, Costa DL, D'Império Lima MR, Sher A. Mycobacterium tuberculosis induces Irg1 in murine macrophages by a pathway involving both TLR-2 and STING/IFNAR signaling and requiring bacterial phagocytosis. Front Cell Infect Microbiol, 2022, 12: 862582. |
| [25] | Huijser E, Bodewes ILA, Lourens MS, van Helden- Meeuwsen CG, van den Bosch TPP, Grashof DGB, van de Werken HJG, Lopes AP, van Roon JAG, van Daele PLA, Brkic Z, Dik WA, Versnel MA. Hyperresponsive cytosolic DNA-sensing pathway in monocytes from primary Sj?gren's syndrome. Rheumatology (Oxford), 2022, 61(8): 3491-3496. |
| [26] | Zhang M, Zhang MX, Zhang Q, Zhu GF, Yuan L, Zhang DE, Zhu QY, Yao J, Shu HB, Zhong B. USP 18 recruits USP20 to promote innate antiviral response through deubiquitinating STING/MITA. Cell Res, 2016, 26(12): 1302-1319. |
| [27] | Yang ZF, Xian HF, Hu JJ, Tian S, Qin YF, Wang RF, Cui J. USP 18 negatively regulates NF-kappaB signaling by targeting TAK1 and NEMO for deubiquitination through distinct mechanisms. Sci Rep, 2015, 5: 12738. |
| [28] | Choi YB, Shembade N, Parvatiyar K, Balachandran S, Harhaj EW. TAX1BP1 restrains virus-induced apoptosis by facilitating itch-mediated degradation of the mitochondrial adaptor MAVS. Mol Cell Biol, 2017, 37(1): e00422-16. |
| [29] | White J, Suklabaidya S, Vo MT, Choi YB, Harhaj EW. Multifaceted roles of TAX1BP1 in autophagy. Autophagy, 2023, 19(1): 44-53. |
| [30] | Hou FJ, Sun LJ, Zheng H, Skaug B, Jiang QX, Chen ZJJ. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell, 2011, 146(3): 448-461. |
| [31] | LIU BY, GAO CJ. Regulation of MAVS activation through post-translational modifications. Curr Opin Immunol, 2018, 50: 75-81. |
| [32] | Ling L, Goeddel DV. T6BP, a TRAF6-interacting protein involved in IL-1 signaling. Proc Natl Acad Sci USA, 2000, 97(17): 9567-9572. |
| [33] | Hou JX, Han LL, Zhao Z, Liu HQ, Zhang L, Ma CH, Yi F, Liu BY, Zheng Y, Gao CJ. USP 18 positively regulates innate antiviral immunity by promoting K63-linked polyubiquitination of MAVS. Nat Commun, 2021, 12(1): 2970. |
| [34] | Zhu GF, Badonyi M, Franklin L, Seabra L, Rice GI, Anne-Boland-Auge, Deleuze JF, El-Chehadeh S, Anheim M, de Saint-Martin A, Pellegrini S, Marsh JA, Crow YJ, El-Daher MT.Type I interferonopathy due to a homozygous loss-of-inhibitory function mutation in STAT2. J Clin Immunol, 2023, 43(4): 808-818. |
| [35] | L?chte S, Waichman S, Beutel O, You CJ, Piehler J. Live cell micropatterning reveals the dynamics of signaling complexes at the plasma membrane. J Cell Biol, 2014, 207(3): 407-418. |
| [36] | Tsft J, Bogunovic D. The goldilocks zone of type I IFNs: lessons from human genetics. J Immunol, 2018, 201(12): 3479-3485. |
| [37] | Zhang XQ, Bogunovic D, Payelle-Brogard B, Francois- Newton V, Speer SD, Yuan C, Volpi S, Li Z, Sanal O, Mansouri D, Tezcan I, Rice GI, Chen CY, Mansouri N, Mahdaviani SA, Itan Y, Boisson B, Okada S, Zeng L, Wang X, Jiang H, Liu WQ, Han TT, Liu DL, Ma T, Wang B, Liu MG, Liu JY, Wang QK, Yalnizoglu D, Radoshevich L, Uzé G, Gros P, Rozenberg F, Zhang SY, Jouanguy E, Bustamante J, García-Sastre A, Abel L, Lebon P, Notarangelo LD, Crow YJ, Boisson-Dupuis S, Casanova JL, Pellegrini S. Human intracellular ISG15 prevents interferon-alpha/beta over-amplification and auto-inflammation. Nature, 2015, 517(7532): 89-93. |
| [38] | Bogunovic D, Byun M, Durfee LA, Abhyankar A, Sanal O, Mansouri D, Salem S, Radovanovic I, Grant AV, Adimi P, Mansouri N, Okada S, Bryant VL, Kong XF, Kreins A, Velez MM, Boisson B, Khalilzadeh S, Ozcelik U, Darazam IA, Schoggins JW, Rice CM, Al-Muhsen S, Behr M, Vogt G, Puel A, Bustamante J, Gros P, Huibregtse JM, Abel L, Boisson-Dupuis S, Casanova JL. Mycobacterial disease and impaired IFN-gamma immunity in humans with inherited ISG15 deficiency. Science, 2012, 337(6102): 1684-1688. |
| [39] | Meuwissen ME, Schot R, Buta S, Oudesluijs G, Tinschert S, Speer SD, Li Z, van Unen L, Heijsman D, Goldmann T, Lequin MH, Kros JM, Stam W, Hermann M, Willemsen R, Brouwer RWW, Van IJcken WFJ, Martin-Fernandez M, de Coo I, Dudink J, de Vries FAT, Bertoli Avella A, Prinz M, Crow YJ, Verheijen FW, Pellegrini S, Bogunovic D, Mancini GMS. Human USP 18 deficiency underlies type 1 interferonopathy leading to severe pseudo-TORCH syndrome. J Exp Med, 2016, 213(7): 1163-1174. |
| [40] | Alsohime F, Martin-Fernandez M, Temsah MH, Alabdulhafid M, Le Voyer T, Alghamdi M, Qiu X, Alotaibi N, Alkahtani A, Buta S, Jouanguy E, Al-Eyadhy A, Gruber C, Hasan GM, Bashiri FA, Halwani R, Hassan HH, Al-Muhsen S, Alkhamis N, Alsum Z, Casanova JL, Bustamante J, Bogunovic D, Alangari AA. JAK inhibitor therapy in a child with inherited USP18 deficiency. N Engl J Med, 2020, 382(3): 256-265. |
| [41] | Muglia Amancio A, Mittereder L, Carletti A, Tosh KW, Green D, Antonelli LR, Gazzinelli RT, Sher A, Jankovic D. IFNs reset the differential capacity of human monocyte subsets to produce IL-12 in response to microbial stimulation. J Immunol, 2021, 206(7): 1642-1652. |
| [42] | Liu XK, Li HX, Zhong B, Blonska M, Gorjestani S, Yan M, Tian Q, Zhang DE, Lin X, Dong C.USP 18 inhibits NF-kappa B and NFAT activation during Th 17 differentiation by deubiquitinating the TAK1-TAB 1 complex. J Exp Med, 2013, 210(8): 1575-1590. |
| [43] | Martin-Fernandez M, Buta S, Le Voyer T, Li Z, Dynesen LT, Vuillier F, Franklin L, Ailal F, Muglia Amancio A, Malle L, Gruber C, Benhsaien I, Altman J, Taft J, Deswarte C, Roynard M, Nieto-Patlan A, Moriya K, Rosain J, Boddaert N, Bousfiha A, Crow YJ, Jankovic D, Sher A, Casanova JL, Pellegrini S, Bustamante J, Bogunovic D. A partial form of inherited human USP18 deficiency underlies infection and inflammation. J Exp Med, 2022, 219(4): e20211273. |
| [44] | Chen LM, Li SL, McGilvray I. The ISG15/USP18 ubiquitin-like pathway (ISGylation system) in hepatitis C virus infection and resistance to interferon therapy. Int J Biochem Cell Biol, 2011, 43(10): 1427-1431. |
| [45] | Yan M, Luo JK, Ritchie KJ, Sakai I, Takeuchi K, Ren R, Zhang DE.Ubp 43 regulates BCR-ABL leukemogenesis via the type 1 interferon receptor signaling. Blood, 2007, 110(1): 305-312. |
| [46] | Pinto-Fernandez A, Salio M, Partridge T, Chen JZ, Vere G, Greenwood H, Olie CS, Damianou A, Scott HC, Pegg HJ, Chiarenza A, Díaz-Saez L, Smith P, Gonzalez-Lopez C, Patel B, Anderton E, Jones N, Hammonds TR, Huber K, Muschel R, Borrow P, Cerundolo V, Kessler BM. Deletion of the deISGylating enzyme USP18 enhances tumour cell antigenicity and radiosensitivity. Br J Cancer, 2021, 124(4): 817-830. |
| [47] | Yim HY, Park C, Lee YD, Arimoto K, Jeon R, Baek SH, Zhang DE, Kim HH, Kim KI. Elevated response to type I IFN enhances RANKL-mediated osteoclastogenesis in usp18-knockout mice. J Immunol, 2016, 196(9): 3887-3895. |
| [48] | Wang YQ, Mei YX, Song YS, Bachus C, Sun CX, Sheshbaradaran H, Glogauer M. AP-002: a novel inhibitor of osteoclast differentiation and function without disruption of osteogenesis. Eur J Pharmacol, 2020, 889: 173613. |
| [49] | Kar P, Millo T, Saha S, Mahtab S, Agarwal S, Goswami R. Osteogenic mechanisms of basal ganglia calcification and its ex vivo model in the hypoparathyroid milieu. Endocrinology, 2021, 162(4): bqab024. |
/
| 〈 |
|
〉 |
www.chinagene.cn
备案号：京ICP备09063187号
