ISG15: Leading a double life as a secreted molecule

Experimental and Molecular Medicine

Volumn 45, Issue 4, 2013, Pages

  Bogunovic, Dusan ^a   Boisson Dupuis, Stephanie ^a,b   Casanova, Jean Laurent ^a,b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b IMAGINE INSTITUTE   (France)

Author keywords

ISG15; MSMD; Mycobacteria; Secreted Molecule

Indexed keywords

GAMMA INTERFERON; ISG15 PROTEIN; SECRETORY PROTEIN; UNCLASSIFIED DRUG; CYTOKINE;

GENE EXPRESSION REGULATION; GENE FUNCTION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; INNATE IMMUNITY; INTERFERON PRODUCTION; ISG15 GENE; MYCOBACTERIOSIS; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN TERTIARY STRUCTURE; REVIEW; SEQUENCE ALIGNMENT; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; INBORN ERROR OF METABOLISM; METABOLISM; MOLECULAR GENETICS; SECRETION (PROCESS);

CORYNEBACTERINEAE; MUS;

AMINO ACID SEQUENCE; ANIMALS; CYTOKINES; HUMANS; INTERFERON-GAMMA; METABOLISM, INBORN ERRORS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA;

EID: 84878306289     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.1038/emm.2013.36     Document Type: Review

References (76)

1. Farrell PJ, Broeze RJ, Lengyel P. Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells. Nature 1979; 279: 523-525. (Pubitemid 9195259)
2. Korant BD, Blomstrom DC, Jonak GJ, Knight E Jr. Interferon-induced proteins. Purification and characterization of a 15000-dalton protein from human and bovine cells induced by interferon. J Biol Chem 1984; 259: 14835-14839. (Pubitemid 15222216)
3. Blomstrom DC, Fahey D, Kutny R, Korant BD, Knight E Jr. Molecular characterization of the interferon-induced 15-kDa protein. Molecular cloning and nucleotide and amino acid sequence. J Biol Chem 1986; 261: 8811-8816. (Pubitemid 17205080)
4. Haas AL, Ahrens P, Bright PM, Ankel H. Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J Biol Chem 1987; 262: 11315-11323. (Pubitemid 17122874)
5. Jeon YJ, Yoo HM, Chung CH. ISG15 and immune diseases. Biochim Biophys Acta 2010; 1802: 485-496.
6. Knight E Jr., Fahey D, Cordova B, Hillman M, Kutny R, Reich N et al. A 15-kDa interferon-induced protein is derived by COOH-terminal processing of a 17-kDa precursor. J Biol Chem 1988; 263: 4520-4522.
7. Skaug B, Chen ZJ. Emerging role of ISG15 in antiviral immunity. Cell 2010; 143: 187-190.
8. Harty RN, Pitha PM, Okumura A. Antiviral activity of innate immune protein ISG15. J Innate Immun 2009; 1: 397-404.
9. Zhang D, Zhang DE. Interferon-stimulated gene 15 and the protein ISGylation system. J Interferon Cytokine Res 2011; 31: 119-130.
10. Durfee LA, Lyon N, Seo K, Huibregtse JM. The ISG15 conjugation system broadly targets newly synthesized proteins: Implications for the antiviral function of ISG15. Mol Cell 2010; 38: 722-732.
11. Durfee LA, Huibregtse JM. Identification and validation of ISG15 target proteins. Subcell Biochem 2010; 54: 228-237.
12. Schlesinger DH, Goldstein G. Molecular conservation of 74 amino acid sequence of ubiquitin between cattle and man. Nature 1975; 255: 42304.
13. Liu C, Li X, Yao X, Kong X, Qiao W, Geng Y. Bovine ISG15: An antiviral and inducible protein in BIV infected fetal bovine lung cells. Virol J 2010; 7: 134.
14. Reich N, Evans B, Levy D, Fahey D, Knight E Jr., Darnell JE Jr. Interferoninduced transcription of a gene encoding a 15-kDa protein depends on an upstream enhancer element. Proc Natl Acad Sci USA 1987; 84: 6394-6398. (Pubitemid 18002807)
15. Kessler DS, Levy DE, Darnell JE Jr. Two interferon-induced nuclear factors bind a single promoter element in interferon-stimulated genes. Proc Natl Acad Sci USA 1988; 85: 8521-8525. (Pubitemid 19024993)
16. Lenschow DJ. Antiviral properties of ISG15. Viruses 2010; 2: 2154-2168.
17. Osiak A, Utermohlen 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: 6338-6345. (Pubitemid 41023211)
18. Lenschow DJ, Lai C, Frias-Staheli N, Giannakopoulos NV, Lutz A, Wolff T et al. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc Natl Acad Sci USA 2007; 104: 1371-1376. (Pubitemid 46184011)
19. Guerra S, Caceres A, Knobeloch KP, Horak I, Esteban M. Vaccinia virus E3 protein prevents the antiviral action of ISG15. PLoS Pathog 2008; 4: E1000096.
20. Dai J, Pan W, Wang P. ISG15 facilitates cellular antiviral response to dengue and West Nile virus infection in vitro. Virol J 2011; 8: 468.
21. Hsiang TY, Zhao C, Krug RM. Interferon-induced ISG15 conjugation inhibits influenza A virus gene expression and replication in human cells. J Virol 2009; 83: 5971-5977.
22. Okumura A, Lu G, Pitha-Rowe I, Pitha PM. Innate antiviral response targets HIV-1 release by the induction of ubiquitin-like protein ISG15. Proc Natl Acad Sci USA 2006; 103: 1440-1445. (Pubitemid 43191184)
23. Hsiao NW, Chen JW, Yang TC, Orloff GM, Wu YY, Lai CH et al. ISG15 over-expression inhibits replication of the Japanese encephalitis virus in human medulloblastoma cells. Antiviral Res 2010; 85: 504-511.
24. Okumura A, Pitha PM, Harty RN. ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc Natl Acad Sci USA 2008; 105: 3974-3979. (Pubitemid 351723509)
25. Broering R, Zhang X, Kottilil S, Trippler M, Jiang M, Lu M et al. The interferon stimulated gene 15 functions as a proviral factor for the hepatitis C virus and as a regulator of the IFN response. Gut 2010; 59: 1111-1119.
26. Werneke SW, Schilte C, Rohatgi A, Monte KJ, Michault A, Arenzana-Seisdedos F et al. ISG15 is critical in the control of Chikungunya virus infection independent of UbE1L mediated conjugation. PLoS Pathog 2011; 7: E1002322.
27. Knight E Jr, Cordova B. IFN-induced 15-kDa protein is released from human lymphocytes and monocytes. J Immunol 1991; 146: 2280-2284.
28. Recht M, Borden EC, Knight E Jr. A human 15-kDa IFN-induced protein induces the secretion of IFN-gamma. J Immunol 1991; 147: 2617-2623.
29. D'Cunha J, Knight E Jr, Haas AL, Truitt RL, Borden EC. Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc Natl Acad Sci USA 1996; 93: 211-215. (Pubitemid 26038129)
30. D'Cunha J, Ramanujam S, Wagner RJ, Witt PL, Knight E Jr. Borden EC. In vitro and in vivo secretion of human ISG15, an IFN-induced immunomodulatory cytokine. J Immunol 1996; 157: 4100-4108. (Pubitemid 126449322)
31. Liu CS, Sun Y, Zhang M, Sun L. Identification and analysis of a Sciaenops ocellatus ISG15 homologue that is involved in host immune defense against bacterial infection. Fish Shellfish Immunol 2010; 29: 167-174.
32. Casanova JL, Abel L. Inborn errors of immunity to infection: The rule rather than the exception. J Exp Med 2005; 202: 197-201. (Pubitemid 41043814)
33. Casanova JL, Abel L. Genetic dissection of immunity to mycobacteria: The human model. Annu Rev Immunol 2002; 20: 581-620. (Pubitemid 34293435)
34. Quintana-Murci L, Alcais A, Abel L, Casanova JL. Immunology in natura: Clinical, epidemiological and evolutionary genetics of infectious diseases. Nat Immunol 2007; 8: 1165-1171. (Pubitemid 350011752)
35. Casanova JL, Abel L. Primary immunodeficiencies: A field in its infancy. Science 2007; 317: 617-619. (Pubitemid 47229951)
36. Alcais A, Abel L, Casanova JL. Human genetics of infectious diseases: Between proof of principle and paradigm. J Clin Invest 2009; 119: 2506-2514.
37. Boisson-Dupuis S, El Baghdadi J, Parvaneh N, Bousfiha A, Bustamante J, Feinberg J et al. IL-12Rbeta1 deficiency in two of fifty children with severe tuberculosis from Iran, Morocco, and Turkey. PLoS One 2011; 6: E18524.
38. Bustamante J, Boisson-Dupuis S, Jouanguy E, Picard C, Puel A, Abel L et al. Novel primary immunodeficiencies revealed by the investigation of paediatric infectious diseases. Curr Opin Immunol 2008; 20: 39-48.
39. Alcais A, Quintana-Murci L, Thaler DS, Schurr E, Abel L, Casanova JL. Life-threatening infectious diseases of childhood: Single-gene inborn errors of immunity? Ann N Y Acad Sci 2010; 1214: 18-33.
40. Jouanguy E, Altare F, Lamhamedi S, Revy P, Emile JF, Newport M et al. Interferon-gamma-receptor deficiency in an infant with fatal bacille Calmette-Guerin infection. N Engl J Med 1996; 335: 1956-1961.
41. Newport MJ, Huxley CM, Huston S, Hawrylowicz CM, Oostra BA, Williamson R et al. A mutation in the interferon-gamma-receptor gene and susceptibility to mycobacterial infection. N Engl J Med 1996; 335: 1941-1949. (Pubitemid 26428218)
42. Altare F, Durandy A, Lammas D, Emile JF, Lamhamedi S, Le Deist F et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 1998; 280: 1432-1435. (Pubitemid 28264836)
43. Altare F, Lammas D, Revy P, Jouanguy E, Doffinger R, Lamhamedi S et al. Inherited interleukin 12 deficiency in a child with bacille Calmette-Guerin and Salmonella enteritidis disseminated infection. J Clin Invest 1998; 102: 2035-2040. (Pubitemid 29018809)
44. de Jong R, Altare F, Haagen IA, Elferink DG, Boer T, van Breda Vriesman PJ et al. Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 1998; 280: 1435-1438. (Pubitemid 28264837)
45. Dorman SE, Holland SM. Mutation in the signal-transducing chain of the interferon-gamma receptor and susceptibility to mycobacterial infection. J Clin Invest 1998; 101: 2364-2369. (Pubitemid 28270430)
46. Dupuis S, Dargemont C, Fieschi C, Thomassin N, Rosenzweig S, Harris J et al. Impairment of mycobacterial but not viral immunity by a germline human STAT1 mutation. Science 2001; 293: 300-303. (Pubitemid 32694746)
47. Filipe-Santos O, Bustamante J, Haverkamp MH, Vinolo E, Ku CL, Puel A et al. X-linked susceptibility to mycobacteria is caused by mutations in NEMO impairing CD40-dependent IL-12 production. J Exp Med 2006; 203: 1745-1759. (Pubitemid 44036280)
48. Bustamante J, Arias AA, Vogt G, Picard C, Galicia LB, Prando C et al. Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease. Nat Immunol 2011; 12: 213-221.
49. Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S, Azevedo J et al. IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med 2011; 365: 127-138.
50. Bogunovic D, Byun M, Durfee LA, Abhyankar A, Sanal O, Mansouri D et al. Mycobacterial disease and impaired IFN-gamma immunity in humans with inherited ISG15 deficiency. Science 2012; 337: 1684-1688.
51. Borregaard N. Neutrophils, from marrow to microbes. Immunity 2010; 33: 657-670.
52. Theilgaard-Monch K, Jacobsen LC, Borup R, Rasmussen T, Bjerregaard MD, Nielsen FC et al. The transcriptional program of terminal granulocytic differentiation. Blood 2005; 105: 1785-1796. (Pubitemid 40223703)
53. Duitman EH, Orinska Z, Bulfone-Paus S. Mechanisms of cytokine secretion: A portfolio of distinct pathways allows flexibility in cytokine activity. Eur J Cell Biol 2011; 90: 476-483.
54. van der Veen AG, Ploegh HL. Ubiquitin-like proteins. Annu Rev Biochem 2012; 81: 323-357.
55. Majetschak M. Extracellular ubiquitin: Immune modulator and endogenous opponent of damage-associated molecular pattern molecules. J Leukoc Biol 2011; 89: 205-219.
56. Hosono H, Yokosawa H. Small ubiquitin-related modifier is secreted and shows cytokine-like activity. Biol Pharm Bull 2008; 31: 834-837. (Pubitemid 351731972)
57. Kondoh T, Nakamura M, Nabika T, Yoshimura Y, Tanigawa Y. Ubiquitin-like polypeptide inhibits the proliferative response of T cells in vivo. Immunobiology 1999; 200: 140-149. (Pubitemid 29089964)
58. Smahi A, Courtois G, Vabres P, Yamaoka S, Heuertz S, Munnich A et al. Genomic rearrangement in NEMO impairs NF-kappaB activation and is a cause of incontinentia pigmenti. The International Incontinentia Pigmenti (IP) Consortium. Nature 2000; 405: 466-472.
59. Ferrari S, Giliani S, Insalaco A, Al-Ghonaium A, Soresina AR, Loubser M et al. Mutations of CD40 gene cause an autosomal recessive form of immunodeficiency with hyper IgM. Proc Natl Acad Sci USA 2001; 98: 12614-12619. (Pubitemid 33019994)
60. Courtois G, Smahi A, Reichenbach J, Doffinger R, Cancrini C, Bonnet M et al. A hypermorphic IkappaBalpha mutation is associated with autosomal dominant anhidrotic ectodermal dysplasia and T cell immunodeficiency. J Clin Invest 2003; 112: 1108-1115. (Pubitemid 38056325)
61. Kofoed EM, Hwa V, Little B, Woods KA, Buckway CK, Tsubaki J et al. Growth hormone insensitivity associated with a STAT5b mutation. N Engl J Med 2003; 349: 1139-1147. (Pubitemid 37122326)
62. Picard C, Puel A, Bonnet M, Ku CL, Bustamante J, Yang K et al. Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 2003; 299: 2076-2079. (Pubitemid 36383736)
63. Casrouge A, Zhang SY, Eidenschenk C, Jouanguy E, Puel A, Yang K et al. Herpes simplex virus encephalitis in human UNC-93B deficiency. Science 2006; 314: 308-312. (Pubitemid 44571977)
64. Minegishi Y, Saito M, Morio T, Watanabe K, Agematsu K, Tsuchiya S et al. Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity 2006; 25: 745-755. (Pubitemid 46131400)
65. Minegishi Y, Saito M, Tsuchiya S, Tsuge I, Takada H, Hara T et al. Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature 2007; 448: 1058-1062. (Pubitemid 47345590)
66. Zhang SY, Jouanguy E, Ugolini S, Smahi A, Elain G, Romero P et al. TLR3 deficiency in patients with herpes simplex encephalitis. Science 2007; 317: 1522-1527. (Pubitemid 47417427)
67. von Bernuth H, Picard C, Jin Z, Pankla R, Xiao H, Ku CL et al. Pyogenic bacterial infections in humans with MyD88 deficiency. Science 2008; 321: 691-696.
68. Glocker EO, Kotlarz D, Boztug K, Gertz EM, Schaffer AA, Noyan F et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med 2009; 361: 2033-2045.
69. Perez de Diego R, Sancho-Shimizu V, Lorenzo L, Puel A, Plancoulaine S, Picard C et al. Human TRAF3 adaptor molecule deficiency leads to impaired Toll-like receptor 3 response and susceptibility to herpes simplex encephalitis. Immunity 2010; 33: 400-411.
70. Sancho-Shimizu V, Perez de Diego R, Lorenzo L, Halwani R, Alangari A, Israelsson E et al. Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency. J Clin Invest 2011; 121: 4889-4902.
71. Boisson B, Laplantine E, Prando C, Giliani S, Israelsson E, Xu Z et al. Immunodeficiency, autoinflammation and amylopectinosis in humans with inherited HOIL-1 and LUBAC deficiency. Nat Immunol 2012; 13: 1178-1186.
72. Herman M, Ciancanelli M, Ou YH, Lorenzo L, Klaudel-Dreszler M, Pauwels E et al. Heterozygous TBK1 mutations impair TLR3 immunity and underlie herpes simplex encephalitis of childhood. J Exp Med 2012; 209: 1567-1582.
73. Salem ML, Gillanders WE, Kadima AN, El-Naggar S, Rubinstein MP, Demcheva M et al. Review: Novel nonviral delivery approaches for interleukin-12 protein and gene systems: Curbing toxicity and enhancing adjuvant activity. J Interferon Cytokine Res 2006; 26: 593-608. (Pubitemid 44689649)
74. Gao XF, Yang ZW, Li J. Adjunctive therapy with interferon-gamma for the treatment of pulmonary tuberculosis: A systematic review. Int J Infect Dis 2011; 15: E594-e600.
75. Yeilding N, Szapary P, Brodmerkel C, Benson J, Plotnick M, Zhou H et al. Development of the IL-12/23 antagonist ustekinumab in psoriasis: Past, present, and future perspectives. Ann N Y Acad Sci 2011; 1222: 30-39.
76. Laws PM, Young HS. Current and emerging systemic treatment strategies for psoriasis. Drugs 2012; 72: 1867-1880.