Nucleic acid sensing and beyond: Virtues and vices of high-mobility group box 1

Journal of Internal Medicine

Volumn 276, Issue 5, 2014, Pages 444-453

  Yanai, H ^a,b   Taniguchi, T ^a,b  

^a INSTITUTE OF INDUSTRIAL SCIENCE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Autophagy; High mobility group box 1; Infection; Inflammation; Nucleic acids; Sepsis

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; NUCLEIC ACID; PROTEIN BINDING;

ANIMAL; HUMAN; IMMUNOLOGY; INFECTION; INFLAMMATION; INNATE IMMUNITY; METABOLISM;

ANIMALS; HMGB1 PROTEIN; HUMANS; IMMUNITY, INNATE; INFECTION; INFLAMMATION; NUCLEIC ACIDS; PROTEIN BINDING;

EID: 84911165280     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/joim.12285     Document Type: Review

References (88)

1. Read CM, Cary PD, Crane-Robinson C, Driscoll PC, Norman DG. Solution structure of a DNA-binding domain from HMG1. Nucleic Acids Res 1993; 21: 3427-36.
2. Thomas JO, Travers AA. HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem Sci 2001; 26: 167-74.
3. Merenmies J, Pihlaskari R, Laitinen J, Wartiovaara J, Rauvala H. 30-kDa heparin-binding protein of brain (amphoterin) involved in neurite outgrowth. Amino acid sequence and localization in the filopodia of the advancing plasma membrane. J Biol Chem 1991; 266: 16722-9.
4. Wang H, Bloom O, Zhang M et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999; 285: 248-51.
5. Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 2011; 29: 139-62.
6. Bianchi ME. HMGB1 loves company. J Leukoc Biol 2009; 86: 573-6.
7. Ellerman JE, Brown CK, de Vera M et al. Masquerader: high mobility group box-1 and cancer. Clin Cancer Res 2007; 13: 2836-48.
8. Harris HE, Andersson U, Pisetsky DS. HMGB1: a multifunctional alarmin driving autoimmune and inflammatory disease. Nat Rev Rheumatol 2012; 8: 195-202.
9. Li G, Liang X, Lotze MT. HMGB1: the central cytokine for all lymphoid cells. Front Immunol 2013; 4: 68.
10. Sims GP, Rowe DC, Rietdijk ST, Herbst R, Coyle AJ. HMGB1 and RAGE in inflammation and cancer. Annu Rev Immunol 2010; 28: 367-88.
11. Dumitriu IE, Bianchi ME, Bacci M, Manfredi AA, Rovere-Querini P. The secretion of HMGB1 is required for the migration of maturing dendritic cells. J Leukoc Biol 2007; 81: 84-91.
12. Schiraldi M, Raucci A, Munoz LM et al. HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4. J Exp Med 2012; 209: 551-63.
13. Kang R, Livesey KM, Zeh HJ, Loze MT, Tang D. HMGB1: a novel Beclin 1-binding protein active in autophagy. Autophagy 2010; 6: 1209-11.
14. Tang D, Kang R, Livesey KM et al. Endogenous HMGB1 regulates autophagy. J Cell Biol 2010; 190: 881-92.
15. Lu B, Antoine DJ, Kwan K et al. JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation. Proc Natl Acad Sci USA 2014; 111: 3068-73.
16. Antoine DJ, Harris HE, Andersson U, Tracey KJ, Bianchi ME. A systematic nomenclature for the redox states of high mobility group box (HMGB) proteins. Mol Med 2014; 20: 135-7.
17. Lee MN, Roy M, Ong SE et al. Identification of regulators of the innate immune response to cytosolic DNA and retroviral infection by an integrative approach. Nat Immunol 2013; 14: 179-85.
18. Yanai H, Ban T, Taniguchi T. High-mobility group box family of proteins: ligand and sensor for innate immunity. Trends Immunol 2012; 33: 633-40.
19. Yanai H, Ban T, Wang Z et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 2009; 462: 99-103.
20. Yanai H, Chiba S, Ban T et al. Suppression of immune responses by nonimmunogenic oligodeoxynucleotides with high affinity for high-mobility group box proteins (HMGBs). Proc Natl Acad Sci USA 2011; 108: 11542-7.
21. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010; 11: 373-84.
22. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007; 449: 819-26.
23. Yoneyama M, Fujita T. RNA recognition and signal transduction by RIG-I-like receptors. Immunol Rev 2009; 227: 54-65.
24. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461: 788-92.
25. Schroder K, Muruve DA, Tschopp J. Innate immunity: cytoplasmic DNA sensing by the AIM2 inflammasome. Curr Biol 2009; 19: R262-5.
26. Sun L, Wu J, Du F, Chen X, Chen ZJ. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013; 339: 786-91.
27. Takaoka A, Wang Z, Choi MK et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007; 448: 501-5.
28. Unterholzner L, Keating SE, Baran M et al. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 2010; 11: 997-1004.
29. Wu J, Sun L, Chen X et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 2013; 339: 826-30.
30. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 2011; 12: 959-65.
31. Burdette DL, Monroe KM, Sotelo-Troha K et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011; 478: 515-8.
32. Parvatiyar K, Zhang Z, Teles RM et al. The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat Immunol 2012; 13: 1155-61.
33. Woodward JJ, Iavarone AT, Portnoy DA. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 2010; 328: 1703-5.
34. Tamura T, Yanai H, Savitsky D, Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol 2008; 26: 535-84.
35. Baccala R, Gonzalez-Quintial R, Lawson BR et al. Sensors of the innate immune system: their mode of action. Nat Rev Rheumatol 2009; 5: 448-56.
36. Barbalat R, Ewald SE, Mouchess ML, Barton GM. Nucleic acid recognition by the innate immune system. Annu Rev Immunol 2011; 29: 185-214.
37. Kawane K, Ohtani M, Miwa K et al. Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature 2006; 443: 998-1002.
38. Kawasaki T, Kawai T, Akira S. Recognition of nucleic acids by pattern-recognition receptors and its relevance in autoimmunity. Immunol Rev 2011; 243: 61-73.
39. Lenert P. Nucleic acid sensing receptors in systemic lupus erythematosus: development of novel DNA- and/or RNA-like analogues for treating lupus. Clin Exp Immunol 2010; 161: 208-22.
40. Napirei M, Karsunky H, Zevnik B, Stephan H, Mannherz HG, Moroy T. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat Genet 2000; 25: 177-81.
41. Ishii KJ, Coban C, Kato H et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol 2006; 7: 40-8.
42. Ivanov S, Dragoi AM, Wang X et al. A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 2007; 110: 1970-81.
43. Stetson DB, Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 2006; 24: 93-103.
44. Matsumoto Y, Hayashi Y, Omori H et al. Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection. Cell Host Microbe 2012; 11: 492-503.
45. Moisy D, Avilov SV, Jacob Y et al. HMGB1 protein binds to influenza virus nucleoprotein and promotes viral replication. J Virol 2012; 86: 9122-33.
46. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol 2010; 11: 1005-13.
47. Honda K, Takaoka A, Taniguchi T. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 2006; 25: 349-60.
48. Honda K, Taniguchi T. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 2006; 6: 644-58.
49. Nakano H, Yanagita M, Gunn MD. CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med 2001; 194: 1171-8.
50. Chiba S, Baghdadi M, Akiba H et al. Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nat Immunol 2012; 13: 832-42.
51. Pisitkun P, Deane JA, Difilippantonio MJ, Tarasenko T, Satterthwaite AB, Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 2006; 312: 1669-72.
52. Stetson DB, Ko JS, Heidmann T, Medzhitov R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008; 134: 587-98.
53. Urbonaviciute V, Furnrohr BG, Meister S et al. Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J Exp Med 2008; 205: 3007-18.
54. Prinz M, Garbe F, Schmidt H et al. Innate immunity mediated by TLR9 modulates pathogenicity in an animal model of multiple sclerosis. J Clin Invest 2006; 116: 456-64.
55. Segal BM, Chang JT, Shevach EM. CpG oligonucleotides are potent adjuvants for the activation of autoreactive encephalitogenic T cells in vivo. J Immunol 2000; 164: 5683-8.
56. Li J, Kokkola R, Tabibzadeh S et al. Structural basis for the proinflammatory cytokine activity of high mobility group box 1. Mol Med 2003; 9: 37-45.
57. Hreggvidsdottir HS, Lundberg AM, Aveberger AC, Klevenvall L, Andersson U, Harris HE. High mobility group box protein 1 (HMGB1)-partner molecule complexes enhance cytokine production by signaling through the partner molecule receptor. Mol Med 2012; 18: 224-30.
58. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418: 191-5.
59. Hu X, Chakravarty SD, Ivashkiv LB. Regulation of interferon and Toll-like receptor signaling during macrophage activation by opposing feedforward and feedback inhibition mechanisms. Immunol Rev 2008; 226: 41-56.
60. Taniguchi T, Takaoka A. A weak signal for strong responses: interferon-alpha/beta revisited. Nat Rev Mol Cell Biol 2001; 2: 378-86.
61. Tovey MG, Streuli M, Gresser I et al. Interferon messenger RNA is produced constitutively in the organs of normal individuals. Proc Natl Acad Sci USA 1987; 84: 5038-42.
62. Park HJ, Atkinson JP. Autoimmunity: homeostasis of innate immunity gone awry. J Clin Immunol 2012; 32: 1148-52.
63. Calogero S, Grassi F, Aguzzi A et al. The lack of chromosomal protein Hmg1 does not disrupt cell growth but causes lethal hypoglycaemia in newborn mice. Nat Genet 1999; 22: 276-80.
64. Huang H, Nace GW, McDonald KA et al. Hepatocyte-specific high-mobility group box 1 deletion worsens the injury in liver ischemia/reperfusion: a role for intracellular high-mobility group box 1 in cellular protection. Hepatology 2014; 59: 1984-97.
65. Huebener P, Gwak GY, Pradere JP et al. High-mobility group box 1 is dispensable for autophagy, mitochondrial quality control, and organ function in vivo. Cell Metab 2014; 19: 539-47.
66. Kang R, Zhang Q, Hou W et al. Intracellular Hmgb1 inhibits inflammatory nucleosome release and limits acute pancreatitis in mice. Gastroenterology 2014; 146: 1097-107.
67. Yanai H, Matsuda A, An J et al. Conditional ablation of HMGB1 in mice reveals its protective function against endotoxemia and bacterial infection. Proc Natl Acad Sci USA 2013; 110: 20699-704.
68. Kuma A, Hatano M, Matsui M et al. The role of autophagy during the early neonatal starvation period. Nature 2004; 432: 1032-6.
69. Tang D, Billiar TR, Lotze MT. A Janus tale of two active high mobility group box 1 (HMGB1) redox states. Mol Med 2012; 18: 1360-2.
70. Camargo FD, Green R, Capetanaki Y, Jackson KA, Goodell MA. Single hematopoietic stem cells generate skeletal muscle through myeloid intermediates. Nat Med 2003; 9: 1520-7.
71. Gardella S, Andrei C, Ferrera D et al. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 2002; 3: 995-1001.
72. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-. Mol Cell 2002; 10: 417-26.
73. Martinon F, Mayor A, Tschopp J. The inflammasomes: guardians of the body. Annu Rev Immunol 2009; 27: 229-65.
74. Nakahira K, Haspel JA, Rathinam VA et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12: 222-30.
75. Saitoh T, Fujita N, Jang MH et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008; 456: 264-8.
76. Xu Y, Jagannath C, Liu XD, Sharafkhaneh A, Kolodziejska KE, Eissa NT. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 2007; 27: 135-44.
77. Ogawa M, Mimuro H, Yoshikawa Y, Ashida H, Sasakawa C. Manipulation of autophagy by bacteria for their own benefit. Microbiol Immunol 2011; 55: 459-71.
78. Pandol SJ, Saluja AK, Imrie CW, Banks PA. Acute pancreatitis: bench to the bedside. Gastroenterology 2007; 132: 1127-51.
79. Kocsis AK, Szabolcs A, Hofner P et al. Plasma concentrations of high-mobility group box protein 1, soluble receptor for advanced glycation end-products and circulating DNA in patients with acute pancreatitis. Pancreatology 2009; 9: 383-91.
80. Yasuda T, Ueda T, Takeyama Y et al. Significant increase of serum high-mobility group box chromosomal protein 1 levels in patients with severe acute pancreatitis. Pancreas 2006; 33: 359-63.
81. Tsung A, Klune JR, Zhang X et al. HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling. J Exp Med 2007; 204: 2913-23.
82. Tsung A, Sahai R, Tanaka H et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005; 201: 1135-43.
83. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG. PARP inhibition: PARP1 and beyond. Nat Rev Cancer 2010; 10: 293-301.
84. Schriewer JM, Peek CB, Bass J, Schumacker PT. ROS-mediated PARP activity undermines mitochondrial function after permeability transition pore opening during myocardial ischemia-reperfusion. J Am Heart Assoc 2013; 2: e000159.
85. Tang D, Kang R, Livesey KM et al. High-mobility group box 1 is essential for mitochondrial quality control. Cell Metab 2011; 13: 701-11.
86. Cooke MS, Evans MD, Dizdaroglu M, Lunec J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 2003; 17: 1195-214.
87. Yang H, Ochani M, Li J et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci USA 2004; 101: 296-301.
88. Shi CS, Shenderov K, Huang NN et al. Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol 2012; 13: 255-63.