Advertisement

Endogenous DAMPs, Category II: Constitutively Expressed, Injury-Modified Molecules (Cat. II DAMPs)

  • Walter Gottlieb Land
Chapter

Abstract

This chapter presents a collection of endogenous DAMPs in terms of constitutively expressed injury-modified molecules. The first class of this category refers to DAMPs released from the extracellular matrix. These molecules are defined to operate as bona fide DAMPs in the form of proteolytically cleaved fragments released as soluble modified proteins into the circulation. They include subclasses such as proteoglycans, glycosaminoglycans, and glycoproteins. The second class of this category refers to molecules, which act as cell-extrinsically expressed modified DAMPs. Subclasses of this class include membrane-bound oxidation-specific epitopes, which act as both antigens to be recognized by host T cells and DAMPs sensed by various pattern recognition molecules to promote innate immune responses, membrane-bound modified structural sugar patterns, and plasma-derived modified soluble molecules such as oxidized low-density lipoprotein. The third class refers to molecules, which operate as cell-intrinsically expressed modified DAMPs. Subclasses include nuclear DNA breaks, cytosolic mislocated/dislocated nuclear and mitochondrial DNA, cytosolic abnormally accumulating RNA, dyshomeostasis-associated perturbed molecular patterns such as reflected by intracellular potassium efflux, and accumulating metabolic molecules such as succinate.

All these DAMPs are of different structure, localization, and function and are sensed by various pattern recognition receptors. It is concluded that evolution, from the very beginning, has apparently taken care to furnish damaged mammalian cells with clear-cut stigmatic markers which enable the sensing molecules to properly recognize them. Such markers act as DAMPs to signal any infectious or sterile intracellular perturbation, cell stress, and tissue injury, wheresoever they are located and whatsoever their distinct nature is.

References

  1. 1.
    Naba A, Clauser KR, Ding H, Whittaker CA, Carr SA, Hynes RO. The extracellular matrix: tools and insights for the “omics” era. Matrix Biol. 2016;49:10–24. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26163349 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Iozzo RV, Schaefer L. Proteoglycan form and function: a comprehensive nomenclature of PGs. Matrix Biol. 2015;42:11–55. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0945053X15000402 PubMedCentralCrossRefPubMedGoogle Scholar
  3. 3.
    Schaefer L, Schaefer RM. PGs: from structural compounds to signaling molecules. Cell Tissue Res. 2010;339:237–46. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19513755 CrossRefGoogle Scholar
  4. 4.
    Frey H, Schroeder N, Manon-Jensen T, Iozzo RV, Schaefer L. Biological interplay between PGs and their innate immune receptors in inflammation. FEBS J. 2013;280:2165–79. Available from: http://doi.wiley.com/10.1111/febs.12145 PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    Schaefer L, Tredup C, Gubbiotti MA, Iozzo RV. Proteoglycan neofunctions: regulation of inflammation and autophagy in cancer biology. FEBS J. 2017;284:10–26. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27860287 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Babelova A, Moreth K, Tsalastra-Greul W, Zeng-Brouwers J, Eickelberg O, Young MF, et al. Biglycan, a danger signal that activates the NLRP3 inflammasome via toll-like and P2X receptors. J Biol Chem. 2009;284:24035–48. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19605353 PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Nandadasa S, Foulcer S, Apte SS. The multiple, complex roles of versican and its proteolytic turnover by ADAMTS proteases during embryogenesis. Matrix Biol. 2014;35:34–41. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0945053X14000067 PubMedCentralCrossRefPubMedGoogle Scholar
  8. 8.
    Andersson-Sjöland A, Hallgren O, Rolandsson S, Weitoft M, Tykesson E, Larsson-Callerfelt A-K, et al. Versican in inflammation and tissue remodeling: the impact on lung disorders. Glycobiology. 2015;25:243–51. Available from: https://academic.oup.com/glycob/article-lookup/doi/10.1093/glycob/cwu120CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Wight TN. Provisional matrix: a role for versican and hyaluronan. Matrix Biol. 2017;60–61:38–56. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0945053X16303092 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Schaefer L. Complexity of danger: the diverse nature of damage-associated molecular patterns. J Biol Chem. 2014;289:35237–45. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25391648 PubMedCentralCrossRefPubMedGoogle Scholar
  11. 11.
    Almond A. Hyaluronan Cell Mol Life Sci. 2007;64:1591–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17502996 CrossRefGoogle Scholar
  12. 12.
    Kogan G, Soltés L, Stern R, Gemeiner P. Hyaluronic acid: a natural biopolymer with a broad range of biomedical and industrial applications. Biotechnol Lett. 2007;29:17–25. Available from: http://link.springer.com/10.1007/s10529-006-9219-z CrossRefGoogle Scholar
  13. 13.
    Jiang D, Liang J, Noble PW. Hyaluronan in tissue injury and repair. Annu Rev Cell Dev Biol. 2007;23:435–61. Available from: http://www.annualreviews.org/doi/10.1146/annurev.cellbio.23.090506.123337 CrossRefGoogle Scholar
  14. 14.
    Goldberg R, Meirovitz A, Hirshoren N, Bulvik R, Binder A, Rubinstein AM, et al. Versatile role of heparanase in inflammation. Matrix Biol. 2013;32:234–40. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0945053X13000279 PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    Brennan TV, Lin L, Huang X, Cardona DM, Li Z, Dredge K, et al. Heparan sulphate, an endogenous TLR4 agonist, promotes acute GVHD after allogeneic stem cell transplantation. Blood. 2012;120:2899–908. Available from: http://www.bloodjournal.org/cgi/doi/10.1182/blood-2011-07-368720 PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    Goodall KJ, Poon IKH, Phipps S, Hulett MD. Soluble heparan sulphate fragments generated by heparanase trigger the release of pro-inflammatory cytokines through TLR-4. PLoS One. 2014;e109596:9. Available from: http://dx.plos.org/10.1371/journal.pone.0109596 Google Scholar
  17. 17.
    Pankov R, Yamada KM. Fibronectin at a glance. J Cell Sci. 2002;115:3861–3. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12244123 CrossRefGoogle Scholar
  18. 18.
    Okamura Y, Watari M, Jerud ES, Young DW, Ishizaka ST, Rose J, et al. The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem. 2001;276:10229–33. Available from: http://www.jbc.org/lookup/doi/10.1074/jbc.M100099200 CrossRefGoogle Scholar
  19. 19.
    Kelsh-Lasher RM, Ambesi A, Bertram C, McKeown-Longo PJ. Integrin α4β1 and TLR4 cooperate to induce fibrotic gene expression in response to fibronectin’s EDA domain. J Invest Dermatol. 2017;137:2505–12. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28842322 CrossRefGoogle Scholar
  20. 20.
    Midwood K, Sacre S, Piccinini AM, Inglis J, Trebaul A, Chan E, et al. Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med. 2009;15:774–80. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19561617 CrossRefGoogle Scholar
  21. 21.
    Midwood KS, Orend G. The role of tenascin-C in tissue injury and tumorigenesis. J Cell Commun Signal. 2009;3:287–310. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19838819 PubMedCentralCrossRefPubMedGoogle Scholar
  22. 22.
    Midwood KS, Hussenet T, Langlois B, Orend G. Advances in tenascin-C biology. Cell Mol Life Sci. 2011;68:3175–99. Available from: http://link.springer.com/10.1007/s00018-011-0783-6 PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Smiley ST, King JA, Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol. 2001;167:2887–94. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11509636 CrossRefGoogle Scholar
  24. 24.
    Wang H, Zheng C, Xu X, Zhao Y, Lu Y, Liu Z. Fibrinogen links podocyte injury with Toll-like receptor 4 and is associated with disease activity in FSGS patients. Nephrology. 2017;PMID:28407405. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28407405 Google Scholar
  25. 25.
    Daley WP, Peters SB, Larsen M. Extracellular matrix dynamics in development and regenerative medicine. J Cell Sci. 2008;121:255–64. Available from: http://jcs.biologists.org/cgi/doi/10.1242/jcs.006064 CrossRefGoogle Scholar
  26. 26.
    Mecham RP. Overview of extracellular matrix. Curr Protoc Cell Biol. 2012;10:1. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23208544 PubMedGoogle Scholar
  27. 27.
    Hynes RO, Naba A. Overview of the matrisome—an inventory of extracellular matrix constituents and functions. Cold Spring Harb Perspect Biol. 2012;4:a004903. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21937732 PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Schaefer L. Personal communication.Google Scholar
  29. 29.
    Nastase MV, Young MF, Schaefer L. Biglycan. J Histochem Cytochem. 2012;60:963–75. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22821552 PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    Merline R, Moreth K, Beckmann J, Nastase MV, Zeng-Brouwers J, Tralhão JG, et al. Signaling by the matrix proteoglycan decorin controls inflammation and cancer through PDCD4 and MicroRNA-21. Sci Signal. 2011;4:ra75. Available from: http://stke.sciencemag.org/cgi/doi/10.1126/scisignal.2001868 PubMedCentralCrossRefPubMedGoogle Scholar
  31. 31.
    Nastase MV, Iozzo RV, Schaefer L. Key roles for the small leucine-rich PGs in renal and pulmonary pathophysiology. Biochim Biophys Acta. 2014;1840:2460–70. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0304416514000464 PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Wang W, Xu G-L, Jia W-D, Ma J-L, Li J-S, Ge Y-S, et al. Ligation of TLR2 by versican: a link between inflammation and metastasis. Arch Med Res. 2009;40:321–3. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0188440909000605 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Kim S, Takahashi H, Lin W-W, Descargues P, Grivennikov S, Kim Y, et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 2009;457:102–6. Available from: http://www.nature.com/doifinder/10.1038/nature07623 PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Tang M, Diao J, Gu H, Khatri I, Zhao J, Cattral MS. Toll-like receptor 2 activation promotes tumor dendritic cell dysfunction by regulating IL-6 and IL-10 receptor signaling. Cell Rep. 2015;13:2851–64. Available from: http://linkinghub.elsevier.com/retrieve/pii/S2211124715013844 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Mitsui Y, Shiina H, Kato T, Maekawa S, Hashimoto Y, Shiina M, et al. Versican promotes tumor progression, metastasis and predicts poor prognosis in renal carcinoma. Mol Cancer Res. 2017;15:884–95. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28242813 PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    Maishi N, Hida K. Tumor endothelial cells accelerate tumor metastasis. Cancer Sci. 2017;108:1921–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28763139 PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Afratis N, Gialeli C, Nikitovic D, Tsegenidis T, Karousou E, Theocharis AD, et al. Glycosaminoglycans: key players in cancer cell biology and treatment. FEBS J. 2012;279:1177–97. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22333131 CrossRefGoogle Scholar
  38. 38.
    Tesar BM, Jiang D, Liang J, Palmer SM, Noble PW, Goldstein DR. The role of hyaluronan degradation products as innate alloimmune agonists. Am J Transplant. 2006;6:2622–35. Available from: http://doi.wiley.com/10.1111/j.1600-6143.2006.01537.x CrossRefGoogle Scholar
  39. 39.
    Jiang D, Liang J, Noble PW. Hyaluronan as an immune regulator in human diseases. Physiol Rev. 2011;91:221–64. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21248167 PubMedCentralCrossRefPubMedGoogle Scholar
  40. 40.
    Termeer C, Benedix F, Sleeman J, Fieber C, Voith U, Ahrens T, et al. Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med. 2002;195:99–111. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11781369 PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Liang J, Jiang D, Noble PW. Hyaluronan as a therapeutic target in human diseases. Adv Drug Deliv Rev. 2016;97:186–203. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26541745 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Bishop JR, Schuksz M, Esko JD. Heparan sulphate PGs fine-tune mammalian physiology. Nature. 2007;446:1030–7. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17460664 CrossRefGoogle Scholar
  43. 43.
    Linhardt RJ. 2003 Claude S. Hudson Award address in carbohydrate chemistry. heparin: structure and activity. J Med Chem. 2003;46:2551–64. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12801218 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Kahn SR, Lim W, Dunn AS, Cushman M, Dentali F, Akl EA, et al. Prevention of VTE in Nonsurgical Patients. Chest. 2012;141:e195S–226S. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22315261 PubMedCentralCrossRefPubMedGoogle Scholar
  45. 45.
    Liu J, Linhardt RJ. Chemoenzymatic synthesis of heparan sulphate and heparin. Nat Prod Rep. 2014;31:1676–85. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25197032 PubMedCentralCrossRefPubMedGoogle Scholar
  46. 46.
    Johnson GB, Brunn GJ, Kodaira Y, Platt JL. Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulphate by Toll-like receptor 4. J Immunol. 2002;168:5233–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11994480 CrossRefGoogle Scholar
  47. 47.
    Land W. Allograft injury mediated by reactive oxygen species: from conserved proteins of drosophila to acute and chronic rejection of human transplants. Part III: interaction of (oxidative) stress-induced heat shock proteins with toll-like receptor-bearing cells. Transplant Rev. 2003;17:67–86. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0955470X0380006X CrossRefGoogle Scholar
  48. 48.
    Goodall KJ, Poon IKH, Phipps S, Hulett MD. Soluble heparan sulphate fragments generated by heparanase trigger the release of pro-inflammatory cytokines through TLR-4. Srinivasula SM, editor. PLoS One. 2014;e109596:9. Available from: http://dx.plos.org/10.1371/journal.pone.0109596 Google Scholar
  49. 49.
    Platt JL, Wrenshall LE, Johnson GB, Cascalho M. Heparan sulphate proteoglycan metabolism and the fate of grafted tissues. Adv Exp Med Biol. 2015;865:123–40. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26306447 PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    Thakkar N, Yadavalli T, Jaishankar D, Shukla D. Emerging roles of heparanase in viral pathogenesis. Pathogens. 2017;6:43. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28927006 PubMedCentralCrossRefGoogle Scholar
  51. 51.
    Gamblin DP, Scanlan EM, Davis BG. Glycoprotein synthesis: an update. Chem Rev. 2009;109:131–63. Available from: http://pubs.acs.org/doi/abs/10.1021/cr078291i CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    George J, Wang SS, Sevcsik AM, Sanicola M, Cate RL, Koteliansky VE, et al. Transforming growth factor-beta initiates wound repair in rat liver through induction of the EIIIA-fibronectin splice isoform. Am J Pathol. 2000;156:115–24. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10623659 PubMedCentralCrossRefPubMedGoogle Scholar
  53. 53.
    Liao Y-F, Gotwals PJ, Koteliansky VE, Sheppard D, Van De Water L. The EIIIA segment of fibronectin is a ligand for integrins alpha 9beta 1 and alpha 4beta 1 providing a novel mechanism for regulating cell adhesion by alternative splicing. J Biol Chem. 2002;277:14467–74. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11839764 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Rybak J-N, Roesli C, Kaspar M, Villa A, Neri D. The extra-domain A of fibronectin is a vascular marker of solid tumors and metastases. Cancer Res. 2007;67:10948–57. Available from: http://cancerres.aacrjournals.org/cgi/doi/10.1158/0008-5472.CAN-07-1436 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Turner NA. Inflammatory and fibrotic responses of cardiac fibroblasts to myocardial damage associated molecular patterns (DAMPs). J Mol Cell Cardiol. 2016;94:189–200. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26542796 CrossRefGoogle Scholar
  56. 56.
    Julier Z, de Titta A, Grimm AJ, Simeoni E, Swartz MA, Hubbell JA. Fibronectin EDA and CpG synergize to enhance antigen-specific Th1 and cytotoxic responses. Vaccine. 2016;34:2453–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27016652 PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Lemańska-Perek A, Krzyżanowska-Gołąb D, Pupek M, Klimeczek P, Witkiewicz W, Kątnik-Prastowska I. Analysis of soluble molecular fibronectin-fibrin complexes and EDA-fibronectin concentration in plasma of patients with atherosclerosis. Inflammation. 2016;39:1059–68. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27022744 PubMedCentralPubMedGoogle Scholar
  58. 58.
    Bhattacharyya S, Midwood KS, Yin H, Varga J. Toll-like receptor-4 signaling drives persistent fibroblast activation and prevents fibrosis resolution in scleroderma. Adv Wound Care. 2017;6:356–69. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29062592 CrossRefGoogle Scholar
  59. 59.
    Gubán B, Vas K, Balog Z, Manczinger M, Bebes A, Groma G, et al. Abnormal regulation of fibronectin production by fibroblasts in psoriasis. Br J Dermatol. 2016;174:533–41. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26471375 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Bhattacharyya S, Varga J. Endogenous ligands of TLR4 promote unresolving tissue fibrosis: implications for systemic sclerosis and its targeted therapy. Immunol Lett. 2018;195:9–17. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28964818 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Midwood KS, Chiquet M, Tucker RP, Orend G. Tenascin-C at a glance. J Cell Sci. 2016;129:4321–7. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27875272 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Piccinini AM, Zuliani-Alvarez L, Lim JMP, Midwood KS. Distinct microenvironmental cues stimulate divergent TLR4-mediated signaling pathways in macrophages. Sci Signal. 2016;9:ra86. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27577261 PubMedCentralCrossRefPubMedGoogle Scholar
  63. 63.
    Bergler T, Hoffmann U, Bergler E, Jung B, Banas MC, Reinhold SW, et al. Toll-like receptor 4 in experimental kidney transplantation: early mediator of endogenous danger signals. Nephron Exp Nephrol. 2012;121:e59–70. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23171961 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Wang H, Zheng C, Xu X, Zhao Y, Lu Y, Liu Z. Fibrinogen links podocyte injury with Toll-like receptor 4 and is associated with disease activity in FSGS patients. Nephrology. 2017;2017:PMID: 28407405. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28407405 Google Scholar
  65. 65.
    Mercer PF, Chambers RC. Coagulation and coagulation signalling in fibrosis. Biochim Biophys Acta Mol basis Dis. 2013;1832:1018–27. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23298546 CrossRefGoogle Scholar
  66. 66.
    Papac-Milicevic N, Busch CJ-L, Binder CJ. Malondialdehyde epitopes as targets of immunity and the implications for atherosclerosis. Adv Immunol. 2016;131:1–59. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27235680 PubMedCentralCrossRefPubMedGoogle Scholar
  67. 67.
    Weismann D, Binder CJ. The innate immune response to products of phospholipid peroxidation. Biochim Biophys Acta. 2012;1818:2465–75. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22305963 PubMedCentralCrossRefPubMedGoogle Scholar
  68. 68.
    Tsiantoulas D, Perkmann T, Afonyushkin T, Mangold A, Prohaska TA, Papac-Milicevic N, et al. Circulating microparticles carry oxidation-specific epitopes and are recognized by natural IgM antibodies. J Lipid Res. 2015;56:440–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25525116 PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    Binder CJ, Papac-Milicevic N, Witztum JL. Innate sensing of oxidation-specific epitopes in health and disease. Nat Rev Immunol. 2016;16:485–97. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27346802 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Bae YS, Oh H, Rhee SG, Do YY. Regulation of reactive oxygen species generation in cell signaling. Mol Cells. 2011;32:491–509. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22207195 PubMedCentralCrossRefPubMedGoogle Scholar
  71. 71.
    Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol. 2014;24:R453–62. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24845678 PubMedCentralCrossRefPubMedGoogle Scholar
  72. 72.
    Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med. 1991;11:81–128. Available from: http://www.ncbi.nlm.nih.gov/pubmed/1937131 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Niki E, Yoshida Y, Saito Y, Noguchi N. Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochem Biophys Res Commun. 2005;338:668–76. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0006291X05017766 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Bochkov VN, Oskolkova OV, Birukov KG, Levonen A-L, Binder CJ, Stöckl J. Generation and biological activities of oxidized phospholipids. Antioxid Redox Signal. 2010;12:1009–59. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19686040 PubMedCentralCrossRefPubMedGoogle Scholar
  75. 75.
    Lee S, Birukov KG, Romanoski CE, Springstead JR, Lusis AJ, Berliner JA. Role of phospholipid oxidation products in atherosclerosis. Circ Res. 2012;111:778–99. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22935534 PubMedCentralCrossRefPubMedGoogle Scholar
  76. 76.
    Yin H, Xu L, Porter NA. Free radical lipid peroxidation: mechanisms and analysis. Chem Rev. 2011;111:5944–72. Available from: http://pubs.acs.org/doi/abs/10.1021/cr200084z CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Ayala A, Muñoz MF, Argüelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Med Cell Longev. 2014;2014:360438. Available from: http://www.hindawi.com/journals/omcl/2014/360438/ CrossRefGoogle Scholar
  78. 78.
    Salomon RG. Structural identification and cardiovascular activities of oxidized phospholipids. Circ Res. 2012;111:930–46. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22982874 PubMedCentralCrossRefPubMedGoogle Scholar
  79. 79.
    Bochkov V, Gesslbauer B, Mauerhofer C, Philippova M, Erne P, Oskolkova OV. Pleiotropic effects of oxidized phospholipids. Free Radic Biol Med. 2017;111:6–24. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28027924 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Thomas CP, O’Donnell VB. Oxidized phospholipid signaling in immune cells. Curr Opin Pharmacol. 2012;12:471–7. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1471489212000367 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    O’Donnell VB, Murphy RC. New families of bioactive oxidized phospholipids generated by immune cells: identification and signaling actions. Blood. 2012;120:1985–92. Available from: http://www.bloodjournal.org/cgi/doi/10.1182/blood-2012-04-402826 PubMedCentralCrossRefPubMedGoogle Scholar
  82. 82.
    Miller YI, Choi S-H, Wiesner P, Fang L, Harkewicz R, Hartvigsen K, et al. Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res. 2011;108:235–48. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21252151 PubMedCentralCrossRefPubMedGoogle Scholar
  83. 83.
    Chou M-Y, Fogelstrand L, Hartvigsen K, Hansen LF, Woelkers D, Shaw PX, et al. Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J Clin Invest. 2009;119:1335–49. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19363291 PubMedCentralCrossRefPubMedGoogle Scholar
  84. 84.
    Gallucci S, Matzinger P. Danger signals: SOS to the immune system. Curr Opin Immunol. 2001;13:114–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11154927 CrossRefGoogle Scholar
  85. 85.
    Shi T, Moulton VR, Lapchak PH, Deng G-M, Dalle Lucca JJ, Tsokos GC. Ischemia-mediated aggregation of the actin cytoskeleton is one of the major initial events resulting in ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol. 2009;296:G339–47. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19095765 CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Chang M-K, Binder CJ, Miller YI, Subbanagounder G, Silverman GJ, Berliner JA, et al. Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J Exp Med. 2004;200:1359–70. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15583011 PubMedCentralCrossRefPubMedGoogle Scholar
  87. 87.
    Zhang M, Alicot EM, Chiu I, Li J, Verna N, Vorup-Jensen T, et al. Identification of the target self-antigens in reperfusion injury. J Exp Med. 2006;203:141–52. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16390934 PubMedCentralCrossRefPubMedGoogle Scholar
  88. 88.
    Zhang M, Carroll MC. Natural IgM-mediated innate autoimmunity: a new target for early intervention of ischemia-reperfusion injury. Expert Opin Biol Ther. 2007;7:1575–82. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17916049 CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Chen GY, Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol. 2010;10:826–37. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21088683 PubMedCentralCrossRefPubMedGoogle Scholar
  90. 90.
    Kunjathoor VV, Febbraio M, Podrez EA, Moore KJ, Andersson L, Koehn S, et al. Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J Biol Chem. 2002;277:49982–8. Available from: http://www.jbc.org/lookup/doi/10.1074/jbc.M209649200 CrossRefGoogle Scholar
  91. 91.
    Boullier A, Gillotte KL, Hörkkö S, Green SR, Friedman P, Dennis EA, et al. The binding of oxidized low density lipoprotein to mouse CD36 is mediated in part by oxidized phospholipids that are associated with both the lipid and protein moieties of the lipoprotein. J Biol Chem. 2000;275:9163–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10734051 CrossRefGoogle Scholar
  92. 92.
    Boullier A, Friedman P, Harkewicz R, Hartvigsen K, Green SR, Almazan F, et al. Phosphocholine as a pattern recognition ligand for CD36. J Lipid Res. 2005;46:969–76. Available from: http://www.jlr.org/lookup/doi/10.1194/jlr.M400496-JLR200 CrossRefGoogle Scholar
  93. 93.
    Kim Y-W, Yakubenko VP, West XZ, Gugiu GB, Renganathan K, Biswas S, et al. Receptor-mediated mechanism controlling tissue levels of bioactive lipid oxidation products. Circ Res. 2015;117:321–32. Available from: http://circres.ahajournals.org/lookup/doi/10.1161/CIRCRESAHA.117.305925 PubMedCentralCrossRefPubMedGoogle Scholar
  94. 94.
    Duryee MJ, Freeman TL, Willis MS, Hunter CD, Hamilton BC, Suzuki H, et al. Scavenger receptors on sinusoidal liver endothelial cells are involved in the uptake of aldehyde-modified proteins. Mol Pharmacol. 2005;68:1423–30. Available from: http://molpharm.aspetjournals.org/cgi/doi/10.1124/mol.105.016121 CrossRefGoogle Scholar
  95. 95.
    Shechter I, Fogelman AM, Haberland ME, Seager J, Hokom M, Edwards PA. The metabolism of native and malondialdehyde-altered low density lipoproteins by human monocyte-macrophages. J Lipid Res. 1981;22:63–71. Available from: http://www.ncbi.nlm.nih.gov/pubmed/6260883 PubMedGoogle Scholar
  96. 96.
    Kadl A, Sharma PR, Chen W, Agrawal R, Meher AK, Rudraiah S, et al. Oxidized phospholipid-induced inflammation is mediated by Toll-like receptor 2. Free Radic Biol Med. 2011;51:1903–9. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0891584911005399 PubMedCentralCrossRefPubMedGoogle Scholar
  97. 97.
    Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol. 2010;11:155–61. Available from: http://www.nature.com/doifinder/10.1038/ni.1836 CrossRefGoogle Scholar
  98. 98.
    Seimon TA, Nadolski MJ, Liao X, Magallon J, Nguyen M, Feric NT, et al. Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress. Cell Metab. 2010;12:467–82. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1550413110003463 PubMedCentralCrossRefPubMedGoogle Scholar
  99. 99.
    Litvack ML, Palaniyar N. Review: soluble innate immune pattern-recognition proteins for clearing dying cells and cellular components: implications on exacerbating or resolving inflammation. Innate Immun. 2010;16:191–200. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20529971 CrossRefGoogle Scholar
  100. 100.
    Chang M-K, Binder CJ, Torzewski M, Witztum JL. C-reactive protein binds to both oxidized LDL and apoptotic cells through recognition of a common ligand: phosphorylcholine of oxidized phospholipids. Proc Natl Acad Sci U S A. 2002;99:13043–8. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.192399699 PubMedCentralCrossRefPubMedGoogle Scholar
  101. 101.
    Weismann D, Hartvigsen K, Lauer N, Bennett KL, Scholl HPN, Charbel Issa P, et al. Complement factor H binds malondialdehyde epitopes and protects from oxidative stress. Nature. 2011;478:76–81. Available from: http://www.nature.com/doifinder/10.1038/nature10449 PubMedCentralCrossRefPubMedGoogle Scholar
  102. 102.
    Veneskoski M, Turunen SP, Kummu O, Nissinen A, Rannikko S, Levonen A-L, et al. Specific recognition of malondialdehyde and malondialdehyde acetaldehyde adducts on oxidized LDL and apoptotic cells by complement anaphylatoxin C3a. Free Radic Biol Med. 2011;51:834–43. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0891584911003455 CrossRefGoogle Scholar
  103. 103.
    Chou M-Y, Hartvigsen K, Hansen LF, Fogelstrand L, Shaw PX, Boullier A, et al. Oxidation-specific epitopes are important targets of innate immunity. J Intern Med. 2008;263:479–88. Available from: http://doi.wiley.com/10.1111/j.1365-2796.2008.01968.x CrossRefGoogle Scholar
  104. 104.
    Lee H, Ko EH, Lai M, Wei N, Balroop J, Kashem Z, et al. Delineating the relationships among the formation of reactive oxygen species, cell membrane instability and innate autoimmunity in intestinal reperfusion injury. Mol Immunol. 2014;58:151–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24365749 CrossRefGoogle Scholar
  105. 105.
    Elvington A, Atkinson C, Kulik L, Zhu H, Yu J, Kindy MS, et al. Pathogenic natural antibodies propagate cerebral injury following ischemic stroke in mice. J Immunol. 2012;188:1460–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22198950 CrossRefGoogle Scholar
  106. 106.
    Atkinson C, Qiao F, Yang X, Zhu P, Reaves N, Kulik L, et al. Targeting pathogenic postischemic self-recognition by natural IgM to protect against posttransplantation cardiac reperfusion injury. Circulation. 2015;131:1171–80. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25825397 PubMedCentralCrossRefPubMedGoogle Scholar
  107. 107.
    Sihag S, Haas MS, Kim KM, Guerrero JL, Beaudoin J, Alicot EM, et al. Natural IgM blockade limits infarct expansion and left ventricular dysfunction in a swine myocardial infarct model. Circ Cardiovasc Interv. 2016;9:e002547. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26671971 PubMedCentralCrossRefPubMedGoogle Scholar
  108. 108.
    Marshall K, Jin J, Atkinson C, Alawieh A, Qiao F. Lei B, et al. Hepatology: Natural IgM initiates an inflammatory response important for both hepatic ischemia reperfusion injury and regeneration; 2017. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28880403 Google Scholar
  109. 109.
    Farrar CA, Asgari E, Schwaeble WJ, Sacks SH. Which pathways trigger the role of complement in ischaemia/reperfusion injury? Front Immunol. 2012;3:341. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23181062 PubMedCentralCrossRefPubMedGoogle Scholar
  110. 110.
    Sheen JH, Heeger PS. Effects of complement activation on allograft injury. Curr Opin Organ Transplant. 2015;20:468–75. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26132735 PubMedCentralCrossRefPubMedGoogle Scholar
  111. 111.
    Ryan BJ, Nissim A, Winyard PG. Oxidative post-translational modifications and their involvement in the pathogenesis of autoimmune diseases. Redox Biol. 2014;2:715–24. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24955328 PubMedCentralCrossRefPubMedGoogle Scholar
  112. 112.
    Napoletano C, Rughetti A, Agervig Tarp MP, Coleman J, Bennett EP, Picco G, et al. Tumor-associated Tn-MUC1 glycoform is internalized through the macrophage galactose-type C-type lectin and delivered to the HLA class I and II compartments in dendritic cells. Cancer Res. 2007;67:8358–67. Available from: http://cancerres.aacrjournals.org/cgi/doi/10.1158/0008-5472.CAN-07-1035 CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    van Vliet SJ, Saeland E, van Kooyk Y. Sweet preferences of MGL: carbohydrate specificity and function. Trends Immunol. 2008;29:83–90. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1471490607003146 CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Franz S, Frey B, Sheriff A, Gaipl US, Beer A, Voll RE, et al. Lectins detect changes of the glycosylation status of plasma membrane constituents during late apoptosis. Cytom Part A. 2006;69A:230–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16498674 CrossRefGoogle Scholar
  115. 115.
    Zizzari IG, Napoletano C, Battisti F, Rahimi H, Caponnetto S, Pierelli L, et al. MGL receptor and immunity: when the ligand can make the difference. J Immunol Res. 2015;2015:450695. Available from: http://www.hindawi.com/journals/jir/2015/450695/ PubMedCentralCrossRefPubMedGoogle Scholar
  116. 116.
    Harkewicz R, Hartvigsen K, Almazan F, Dennis EA, Witztum JL, Miller YI. Cholesteryl ester hydroperoxides are biologically active components of minimally oxidized low density lipoprotein. J Biol Chem. 2008;283:10241–51. Available from: http://www.jbc.org/lookup/doi/10.1074/jbc.M709006200 PubMedCentralCrossRefPubMedGoogle Scholar
  117. 117.
    Steinberg D, Witztum JL. Oxidized low-density lipoprotein and atherosclerosis. Arterioscler Thromb Vasc Biol. 2010;30:2311–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21084697 CrossRefGoogle Scholar
  118. 118.
    Blatt AZ, Pathan S, Ferreira VP. Properdin: a tightly regulated critical inflammatory modulator. Immunol Rev. 2016;274:172–90. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27782331 PubMedCentralCrossRefPubMedGoogle Scholar
  119. 119.
    Pirillo A, Norata GD, Catapano AL. LOX-1, OxLDL, and atherosclerosis. Mediat Inflamm. 2013;2013:1–12. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23935243 CrossRefGoogle Scholar
  120. 120.
    Kataoka H, Kume N, Miyamoto S, Minami M, Moriwaki H, Murase T, et al. Expression of lectinlike oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation. 1999;99:3110–7. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10377073 CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Gao S, Liu J. Association between circulating oxidized low-density lipoprotein and atherosclerotic cardiovascular disease. Chron Dis Transl Med. 2017;3:89–94. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29063061 Google Scholar
  122. 122.
    Cortes C, Ohtola JA, Saggu G, Ferreira VP. Local release of properdin in the cellular microenvironment: role in pattern recognition and amplification of the alternative pathway of complement. Front Immunol. 2012;3:412. Available from: http://journal.frontiersin.org/article/10.3389/fimmu.2012.00412/abstract PubMedPubMedCentralGoogle Scholar
  123. 123.
    Ferreira VP, Cortes C, Pangburn MK. Native polymeric forms of properdin selectively bind to targets and promote activation of the alternative pathway of complement. Immunobiology. 2010;215:932–40. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20382442 PubMedCentralCrossRefPubMedGoogle Scholar
  124. 124.
    Xu W, Berger SP, Trouw LA, de Boer HC, Schlagwein N, Mutsaers C, et al. Properdin binds to late apoptotic and necrotic cells independently of C3b and regulates alternative pathway complement activation. J Immunol. 2008;180:7613–21. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18490764 CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Kemper C, Mitchell LM, Zhang L, Hourcade DE. The complement protein properdin binds apoptotic T cells and promotes complement activation and phagocytosis. Proc Natl Acad Sci U S A. 2008;105:9023–8. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.0801015105 PubMedCentralCrossRefPubMedGoogle Scholar
  126. 126.
    Baines AC, Brodsky RA. Complementopathies. Blood Rev. 2017;31(4):213–23. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28215731 PubMedCentralCrossRefPubMedGoogle Scholar
  127. 127.
    Roers A, Hiller B, Hornung V. Recognition of endogenous nucleic acids by the innate immune system. Immunity. 2016;44:739–54. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27096317 CrossRefGoogle Scholar
  128. 128.
    Helleday T, Eshtad S, Nik-Zainal S. Mechanisms underlying mutational signatures in human cancers. Nat Rev Genet. 2014;15:585–98. Available from: http://www.nature.com/doifinder/10.1038/nrg3729 PubMedCentralCrossRefPubMedGoogle Scholar
  129. 129.
    Watts F. Repair of DNA double-strand breaks in heterochromatin. Biomol Ther. 2016;6:47. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27999260 Google Scholar
  130. 130.
    Härtlova A, Erttmann SF, Raffi FA, Schmalz AM, Resch U, Anugula S, et al. DNA damage primes the type I interferon system via the cytosolic DNA sensor STING to promote anti-microbial innate immunity. Immunity. 2015;42:332–43. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25692705 CrossRefPubMedPubMedCentralGoogle Scholar
  131. 131.
    Le Bert N, Lam AR, Ho SS, Shen YJ, Liu MM, Gasser S. STING-dependent cytosolic DNA sensor pathways regulate NKG2D ligand expression. Oncoimmunology. 2014;3:e29259. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25114832 PubMedCentralCrossRefPubMedGoogle Scholar
  132. 132.
    Mackenzie KJ, Carroll P, Martin C-A, Murina O, Fluteau A, Simpson DJ, et al. cGAS surveillance of micronuclei links genome instability to innate immunity. Nature. 2017;548:461–5. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28738408 PubMedCentralCrossRefPubMedGoogle Scholar
  133. 133.
    Rongvaux A, Jackson R, Harman CCD, Li T, West AP, de Zoete MR, et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell. 2014;159:1563–77. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0092867414015141 PubMedCentralCrossRefPubMedGoogle Scholar
  134. 134.
    West AP, Khoury-Hanold W, Staron M, Tal MC, Pineda CM, Lang SM, et al. Mitochondrial DNA stress primes the antiviral innate immune response. Nature. 2015;520:553–7. Available from: http://www.nature.com/doifinder/10.1038/nature14156 PubMedCentralCrossRefPubMedGoogle Scholar
  135. 135.
    Harrington JS, Choi AMK, Nakahira K. Mitochondrial DNA in sepsis. Curr Opin Crit Care. 2017;23:284–90. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28562385 PubMedCentralCrossRefPubMedGoogle Scholar
  136. 136.
    Thomas CA, Tejwani L, Trujillo CA, Negraes PD, Herai RH, Mesci P, et al. Modeling of TREX1-dependent autoimmune disease using human stem cells highlights L1 accumulation as a source of neuroinflammation. Cell Stem Cell. 2017;21:319–331.e8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28803918 PubMedCentralCrossRefPubMedGoogle Scholar
  137. 137.
    George CX, Ramaswami G, Li JB, Samuel CE. Editing of cellular self-RNAs by adenosine deaminase ADAR1 suppresses innate immune stress responses. J Biol Chem. 2016;291:6158–68. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26817845 PubMedCentralCrossRefPubMedGoogle Scholar
  138. 138.
    Miyake K, Shibata T, Ohto U, Shimizu T. Emerging roles of the processing of nucleic acids and Toll-like receptors in innate immune responses to nucleic acids. J Leukoc Biol. 2017;101:135–42. Available from: http://www.jleukbio.org/lookup/doi/10.1189/jlb.4MR0316-108R CrossRefGoogle Scholar
  139. 139.
    Nishikura K. Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem. 2010;79:321–49. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20192758 PubMedCentralCrossRefPubMedGoogle Scholar
  140. 140.
    Wang Q, Li X, Qi R, Billiar T. RNA editing, ADAR1, and the innate immune response. Genes (Basel). 2017;8:41. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28106799 CrossRefGoogle Scholar
  141. 141.
    Rice GI, Kasher PR, Forte GMA, Mannion NM, Greenwood SM, Szynkiewicz M, et al. Mutations in ADAR1 cause Aicardi-Goutières syndrome associated with a type I interferon signature. Nat Genet. 2012;44:1243–8. Available from: http://www.nature.com/doifinder/10.1038/ng.2414 PubMedCentralCrossRefPubMedGoogle Scholar
  142. 142.
    Busoni VB, Lemale J, Dubern B, Frangi F, Bourgeois P, Orsi M, et al. IBD-like features in syndromic diarrhea/trichohepatoenteric syndrome. J Pediatr Gastroenterol Nutr. 2017;64:37–41. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28027214 CrossRefPubMedPubMedCentralGoogle Scholar
  143. 143.
    Walkley CR, Li JB. Rewriting the transcriptome: adenosine-to-inosine RNA editing by ADARs. Genome Biol. 2017;18:205. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29084589 PubMedCentralCrossRefPubMedGoogle Scholar
  144. 144.
    Gallo PM, Gallucci S. The dendritic cell response to classic, emerging, and homeostatic danger signals. Implications for autoimmunity. Front Immunol. 2013;4:138. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23772226 PubMedCentralCrossRefPubMedGoogle Scholar
  145. 145.
    Land WG. The role of damage-associated molecular patterns in human diseases: part I – promoting inflammation and immunity. Sultan Qaboos Univ Med J. 2015;15:e9–21. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25685392 PubMedCentralPubMedGoogle Scholar
  146. 146.
    Liston A, Masters SL. Homeostasis-altering molecular processes as mechanisms of inflammasome activation. Nat Rev Immunol. 2017;17(3):208–14. Available from: http://www.nature.com/doifinder/10.1038/nri.2016.151 CrossRefGoogle Scholar
  147. 147.
    Muñoz-Planillo R, Kuffa P, Martínez-Colón G, Smith BL, Rajendiran TM, Núñez G. K+ efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity. 2013;38:1142–53. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23809161 PubMedCentralCrossRefPubMedGoogle Scholar
  148. 148.
    Kim JH, Park JH, Eisenhut M, Yu JW, Shin JI. Inflammasome activation by cell volume regulation and inflammation-associated hyponatremia: a vicious cycle. Med Hypotheses. 2016;93:117–21. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27372869 CrossRefPubMedPubMedCentralGoogle Scholar
  149. 149.
    van Vliet AR, Martin S, Garg AD, Agostinis P. The PERKs of damage-associated molecular patterns mediating cancer immunogenicity: from sensor to the plasma membrane and beyond. Semin Cancer Biol. 2015;33:74–85. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1044579X15000255 CrossRefPubMedPubMedCentralGoogle Scholar
  150. 150.
    van Vliet AR, Agostinis P. When under pressure, get closer: PERKing up membrane contact sites during ER stress. Biochem Soc Trans. 2016;44:499–504. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27068961 CrossRefGoogle Scholar
  151. 151.
    Sihvola V, Levonen A-L. Keap1 as the redox sensor of the antioxidant response. Arch Biochem Biophys. 2017;617:94–100. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27769838 CrossRefGoogle Scholar
  152. 152.
    Kelly B, O’Neill LAJ. Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Res. 2015;25:771–84. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26045163 PubMedCentralCrossRefPubMedGoogle Scholar
  153. 153.
    O’Neill LAJ, Pearce EJ. Immunometabolism governs dendritic cell and macrophage function. J Exp Med. 2016;213:15–23. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26694970 PubMedCentralCrossRefPubMedGoogle Scholar
  154. 154.
    Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, et al. Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature. 2013;496:238–42. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23535595 PubMedCentralCrossRefPubMedGoogle Scholar
  155. 155.
    Corcoran SE, O’Neill LAJ. HIF1α and metabolic reprogramming in inflammation. J Clin Invest. 2016;126(10):3699–707. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27571407 PubMedCentralCrossRefPubMedGoogle Scholar
  156. 156.
    Rubic T, Lametschwandtner G, Jost S, Hinteregger S, Kund J, Carballido-Perrig N, et al. Triggering the succinate receptor GPR91 on dendritic cells enhances immunity. Nat Immunol. 2008;9:1261–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18820681 CrossRefPubMedPubMedCentralGoogle Scholar
  157. 157.
    Littlewood-Evans A, Sarret S, Apfel V, Loesle P, Dawson J, Zhang J, et al. GPR91 senses extracellular succinate released from inflammatory macrophages and exacerbates rheumatoid arthritis. J Exp Med. 2016;213:1655–62. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27481132 PubMedCentralCrossRefPubMedGoogle Scholar
  158. 158.
    Ariza AC, Deen PMT, Robben JH. The succinate receptor as a novel therapeutic target for oxidative and metabolic stress-related conditions. Front Endocrinol. 2012;3:22. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22649411 CrossRefGoogle Scholar
  159. 159.
    de Castro Fonseca M, Aguiar CJ, da Rocha Franco JA, Gingold RN, Leite MF. GPR91: expanding the frontiers of Krebs cycle intermediates. Cell Commun Signal. 2016;14:3. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26759054 PubMedCentralCrossRefPubMedGoogle Scholar
  160. 160.
    Gilissen J, Jouret F, Pirotte B, Hanson J. Insight into SUCNR1 (GPR91) structure and function. Pharmacol Ther. 2016;159:56–65. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26808164 PubMedGoogle Scholar
  161. 161.
    Geubelle P, Gilissen J, Dilly S, Poma L, Dupuis N, Laschet C, et al. Identification and pharmacological characterization of succinate receptor agonists. Br J Pharmacol. 2017;174:796–808. Available from: http://doi.wiley.com/10.1111/bph.13738 PubMedCentralCrossRefPubMedGoogle Scholar
  162. 162.
    Singh V, Sharma RK, Athilingam T, Sinha P, Sinha N, Thakur AK. NMR spectroscopy-based metabolomics of Drosophila model of Huntington’s disease suggests altered cell energetics. J Proteome Res. 2017;16:3863–72. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28871787 CrossRefGoogle Scholar
  163. 163.
    Guo Y, Xie C, Li X, Yang J, Yu T, Zhang R, et al. Succinate and its G-protein-coupled receptor stimulates osteoclastogenesis. Nat Commun. 2017;8:15621. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28561074 PubMedCentralCrossRefPubMedGoogle Scholar
  164. 164.
    Chen J, Saxena G, Mungrue IN, Lusis AJ, Shalev A. Thioredoxin-interacting protein: a critical link between glucose toxicity and beta-cell apoptosis. Diabetes. 2008;57:938–44. Available from: http://diabetes.diabetesjournals.org/cgi/doi/10.2337/db07-0715 PubMedCentralCrossRefPubMedGoogle Scholar
  165. 165.
    Schulze PC, Yoshioka J, Takahashi T, He Z, King GL, Lee RT. Hyperglycemia promotes oxidative stress through inhibition of thioredoxin function by thioredoxin-interacting protein. J Biol Chem. 2004;279:30369–74. Available from: http://www.jbc.org/lookup/doi/10.1074/jbc.M400549200 CrossRefPubMedPubMedCentralGoogle Scholar
  166. 166.
    Monteiro HP, Ogata FT, Stern A. Thioredoxin promotes survival signaling events under nitrosative/oxidative stress associated with cancer development. Biom J. 2017;40:189–99. Available from: http://linkinghub.elsevier.com/retrieve/pii/S231941701730046X Google Scholar
  167. 167.
    Spindel ON, World C, Berk BC. Thioredoxin interacting protein: redox dependent and independent regulatory mechanisms. Antioxid Redox Signal. 2012;16:587–96. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21929372 PubMedCentralCrossRefPubMedGoogle Scholar
  168. 168.
    Nakka VP, Prakash-babu P, Vemuganti R. Crosstalk between endoplasmic reticulum stress, oxidative stress, and autophagy: potential therapeutic targets for acute CNS injuries. Mol Neurobiol. 2016;53:532–44. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25482050 CrossRefPubMedPubMedCentralGoogle Scholar
  169. 169.
    Lerner AG, Upton J-P, Praveen PVK, Ghosh R, Nakagawa Y, Igbaria A, et al. IRE1α induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab. 2012;16:250–64. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22883233 PubMedCentralCrossRefPubMedGoogle Scholar
  170. 170.
    Oslowski CM, Hara T, O’Sullivan-Murphy B, Kanekura K, Lu S, Hara M, et al. Thioredoxin-interacting protein mediates ER stress-induced β cell death through initiation of the inflammasome. Cell Metab. 2012;16:265–73. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1550413112002823 PubMedCentralCrossRefPubMedGoogle Scholar
  171. 171.
    Anthony TG, Wek RC. TXNIP switches tracks toward a terminal UPR. Cell Metab. 2012;16:135–7. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1550413112002896 CrossRefPubMedPubMedCentralGoogle Scholar
  172. 172.
    Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol. 2010;11:136–40. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20023662 CrossRefGoogle Scholar
  173. 173.
    Schroder K, Zhou R, Tschopp J. The NLRP3 inflammasome: a sensor for metabolic danger? Science. 2010;327:296–300. Available from: http://www.sciencemag.org/cgi/doi/10.1126/science.1184003 CrossRefPubMedPubMedCentralGoogle Scholar
  174. 174.
    Masters SL, Dunne A, Subramanian SL, Hull RL, Tannahill GM, Sharp FA, et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes. Nat Immunol. 2010;11:897–904. Available from: http://www.nature.com/doifinder/10.1038/ni.1935 PubMedCentralCrossRefPubMedGoogle Scholar
  175. 175.
    Hou Y, Wang Y, He Q, Li L, Xie H, Zhao Y, et al. Nrf2 inhibits NLRP3 inflammasome activation through regulating Trx1/TXNIP complex in cerebral ischemia reperfusion injury. Behav Brain Res. 2018;336:32–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28851669 CrossRefGoogle Scholar
  176. 176.
    Li X, Kover KL, Heruth DP, Watkins DJ, Guo Y, Moore WV, et al. Thioredoxin-interacting protein promotes high-glucose-induced macrovascular endothelial dysfunction. Biochem Biophys Res Commun. 2017;493:291–7. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28890350 PubMedCentralCrossRefPubMedGoogle Scholar
  177. 177.
    Wang X, Han Y, Zhang S, Cui N, Liu Z, Huang Z, et al. Associations of polymorphisms in TXNIP and gene-environment interactions with the risk of coronary artery disease in a Chinese Han population. J Cell Mol Med. 2016;20:2362–73. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27470124 PubMedCentralCrossRefPubMedGoogle Scholar
  178. 178.
    Wang BF, Yoshioka J. The emerging role of thioredoxin-interacting protein in myocardial ischemia/reperfusion injury. J Cardiovasc Pharmacol Ther. 2017;22:219–29. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27807222 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.University of StrasbourgMolecular ImmunoRheumatology, Laboratory of Excellence TransplantexStrasbourgFrance

Personalised recommendations