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How Z-DNA/RNA binding proteins shape homeostasis, inflammation, and immunity

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The right-handed double-helical structure of DNA (B-DNA), which follows the Watson-Crick model, is the canonical form of DNA existing in normal physiological settings. Even though an alternative left-handed structure of DNA (Z-DNA) was discovered in the late 1970s, Z-form nucleic acid has not received much attention from biologists, because it is extremely unstable under physiological conditions, has an ill-defined mechanism of its formation, and has obscure biological functions. The debate about the physiological relevance of Z-DNA was settled only after a class of proteins was found to potentially recognize the Z-form architecture of DNA. Interestingly, these Z-DNA binding proteins can bind not only the left-handed form of DNA but also the equivalent structure of RNA (Z-RNA). The Z-DNA/RNA binding proteins present from viruses to humans function as important regulators of biological processes. In particular, the proteins ADAR1 and ZBP1 are currently being extensively re-evaluated in the field to understand potential roles of the noncanonical Z-conformation of nucleic acids in host immune responses and human disease. Despite a growing body of evidence supporting the biological importance of Z-DNA/RNA, there remain many unanswered principal questions, such as when Z-form nucleic acids arise and how they signal to downstream pathways. Understanding Z-DNA/RNA and the sensors in different pathophysiological conditions will widen our view on the regulation of immune responses and open a new door of opportunity to develop novel types of immunomodulatory therapeutic possibilities.

Abstract

The right-handed double-helical structure of DNA (B-DNA), which follows the Watson-Crick model, is the canonical form of DNA existing in normal physiological settings. Even though an alternative left-handed structure of DNA (Z-DNA) was discovered in the late 1970s, Z-form nucleic acid has not received much attention from biologists, because it is extremely unstable under physiological conditions, has an ill-defined mechanism of its formation, and has obscure biological functions. The debate about the physiological relevance of Z-DNA was settled only after a class of proteins was found to potentially recognize the Z-form architecture of DNA. Interestingly, these Z-DNA binding proteins can bind not only the left-handed form of DNA but also the equivalent structure of RNA (Z-RNA). The Z-DNA/RNA binding proteins present from viruses to humans function as important regulators of biological processes. In particular, the proteins ADAR1 and ZBP1 are currently being extensively re-evaluated in the field to understand potential roles of the noncanonical Z-conformation of nucleic acids in host immune responses and human disease. Despite a growing body of evidence supporting the biological importance of Z-DNA/RNA, there remain many unanswered principal questions, such as when Z-form nucleic acids arise and how they signal to downstream pathways. Understanding Z-DNA/RNA and the sensors in different pathophysiological conditions will widen our view on the regulation of immune responses and open a new door of opportunity to develop novel types of immunomodulatory therapeutic possibilities.

참고문헌 (52)

  1. Wang AH, "Molecular structure of a left-handed double helical DNA fragment at atomic resolution", Nature, 282, pp.680~686 (1979)
  2. Drew H, "High-salt d(CpGpCpG), a left-handed Z' DNA double helix", Nature, 286, pp.567~573 (1980)
  3. Herbert A, "Chicken double-stranded RNA adenosine deaminase has apparent specificity for Z-DNA", Proc Natl Acad Sci U S A, 92, pp.7550~7554 (1995)
  4. Berger I, "Spectroscopic characterization of a DNA-binding domain, Z alpha, from the editing enzyme, dsRNA adenosine deaminase : evidence for left-handed Z-DNA in the Z alpha-DNA complex", Biochemistry, 37, pp.13313~13321 (1998)
  5. Schwartz T, "Crystal structure of the Zalpha domain of the human editing enzyme ADAR1 bound to left-handed Z-DNA", Science, 284, pp.1841~1845 (1999)
  6. Placido D, "A left-handed RNA double helix bound by the Z alpha domain of the RNA-editing enzyme ADAR1", Structure, 15, pp.395~404 (2007)
  7. Brown BA 2nd, "The zalpha domain of the editing enzyme dsRNA adenosine deaminase binds left-handed Z-RNA as well as Z-DNA", Proc Natl Acad Sci U S A, 97, pp.13532~13536 (2000)
  8. Schwartz T, "Structure of the DLM-1-Z-DNA complex reveals a conserved family of Z-DNA-binding proteins", Nat Struct Biol, 8, pp.761~765 (2001)
  9. Rothenburg S, "A PKR-like eukaryotic initiation factor 2alpha kinase from zebrafish contains Z-DNA binding domains instead of dsRNA binding domains", Proc Natl Acad Sci U S A, 102, pp.1602~1607 (2005)
  10. Kim YG, "A role for Z-DNA binding in vaccinia virus pathogenesis", Proc Natl Acad Sci U S A, 100, pp.6974~6979 (2003)
  11. Koehler H, "Inhibition of DAI-dependent necroptosis by the Z-DNA binding domain of the vaccinia virus innate immune evasion protein, E3", Proc Natl Acad Sci U S A, 114, pp.11506~11511 (2017)
  12. Kim U, "Purification and characterization of double-stranded RNA adenosine deaminase from bovine nuclear extracts", J Biol Chem, 269, pp.13480~13489 (1994)
  13. O'Connell MA, "Cloning of cDNAs encoding mammalian double-stranded RNA-specific adenosine deaminase", Mol Cell Biol, 15, pp.1389~1397 (1995)
  14. Patterson JB, "Expression and regulation by interferon of a double-stranded-RNA-specific adenosine deaminase from human cells : evidence for two forms of the deaminase", Mol Cell Biol, 15, pp.5376~5388 (1995)
  15. Poulsen H, "CRM1 mediates the export of ADAR1 through a nuclear export signal within the Z-DNA binding domain", Mol Cell Biol, 21, pp.7862~7871 (2001)
  16. Strehblow A, "Nucleocytoplasmic distribution of human RNA-editing enzyme ADAR1 is modulated by double-stranded RNA-binding domains, a leucine-rich export signal, and a putative dimerization domain", Mol Biol Cell, 13, pp.3822~3835 (2002)
  17. Gallo A, "ADAR RNA editing in human disease; more to it than meets the I", Hum Genet, 136, pp.1265~1278 (2017)
  18. Athanasiadis A, "The crystal structure of the Zbeta domain of the RNA-editing enzyme ADAR1reveals distinct conserved surfaces among Z-domains", J Mol Biol, 351, pp.496~507 (2005)
  19. Chung H, "Human ADAR1Prevents Endogenous RNA from Triggering Translational Shutdown", Cell, 172, pp.811~824.e14 (2018)
  20. Rice GI, "Mutations in ADAR1 cause Aicardi-Goutieres syndrome associated with a type I interferon signature", Nat Genet, 44, pp.1243~1248 (2012)
  21. Wang Q, "Requirement of the RNA editing deaminase ADAR1 gene for embryonic erythropoiesis", Science, 290, pp.1765~1768 (2000)
  22. Hartner JC, "Liver disintegration in the mouse embryo caused by deficiency in the RNA-editing enzyme ADAR1", J Biol Chem, 279, pp.4894~4902 (2004)
  23. Wang Q, "Stress-induced apoptosis associated with null mutation of ADAR1RNA editing deaminase gene", J Biol Chem, 279, pp.4952~4961 (2004)
  24. Liddicoat BJ, "RNA editing by ADAR1 prevents MDA5 sensing of endogenous dsRNA as nonself", Science, 349, pp.1115~1120 (2015)
  25. Mannion NM, "The RNA-editing enzyme ADAR1 controls innate immune responses to RNA", Cell Rep, 9, pp.1482~1494 (2014)
  26. Suzuki N, "Mutation analysis of the ADAR1 gene in dyschromatosis symmetrica hereditaria and genetic differentiation from both dyschromatosis universalis hereditaria and acropigmentatio reticularis", J Invest Dermatol, 124, pp.1186~1192 (2005)
  27. Koeris M, "Modulation of ADAR1 editing activity by Z-RNA in vitro", Nucleic Acids Res, 33, pp.5362~5370 (2005)
  28. Ng SK, "Proteins that contain a functional Z-DNA-binding domain localize to cytoplasmic stress granules", Nucleic Acids Res, 41, pp.9786~9799 (2013)
  29. Protter DS, "Principles and Properties of Stress Granules", Trends Cell Biol, 26, pp.668~679 (2016)
  30. Herbert A, "Z-DNA and Z-RNA in human disease", Commun Biol, 2, pp.7~ (2019)
  31. Fu Y, "Cloning of DLM-1, a novel gene that is up-regulated in activated macrophages, using RNA differential display", Gene, 240, pp.157~163 (1999)
  32. Takaoka A, "DAI(DLM-1", ZBP1)is a cytosolic DNA sensor and an activator of innate immune response, 2007, pp.448, 501~505
  33. Ishii KJ, "TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines", Nature, 451, pp.725~729 (2008)
  34. Lippmann J, "IFNbeta responses induced by intracellular bacteria or cytosolic DNA in different human cells do not require ZBP1(DLM-1", DAI), 2008, pp.10, 2579~2588
  35. Kuriakose T, "ZBP1 : Innate Sensor Regulating Cell Death and Inflammation", Trends Immunol, 39, pp.123~134 (2018)
  36. Pasparakis M, "Necroptosis and its role in inflammation", Nature, 517, pp.311~320 (2015)
  37. Kaiser WJ, "Receptor interacting protein homotypic interaction motif-dependent control of NF-kappa B activation via the DNA-dependent activator of IFN regulatory factors", J Immunol, 181, pp.6427~6434 (2008)
  38. Rebsamen M, "DAI", ZBP1recruits RIP1 and RIP3 through RIP homotypic interaction motifs to activate NF-kappaB, 2009, pp.10, 916~922
  39. Upton JW, "DAI", ZBP1, Cell Host Microbe, pp.2012, 11[DOI]
  40. Pham TH, "DNA sensing-independent inhibition of herpes simplex virus 1 replication by DAI", ZBP1, 2013, pp.87, 3076~3086
  41. Kuriakose T, "ZBP1", DAI is an innate sensor of influenza virus triggering the NLRP3inflammasome and programmed cell death pathways, 2016, pp.1, aag2045~
  42. Thapa RJ, "DAI Senses Influenza A Virus Genomic RNA and Activates RIPK3-Dependent Cell Death", Cell Host Microbe, 20, pp.674~681 (2016)
  43. Maelfait J, "Sensing of viral and endogenous RNA by ZBP1", DAI induces necroptosis, 2017, pp.36, 2529~2543
  44. Lin J, "RIPK1 counteracts ZBP1-mediated necroptosis to inhibit inflammation", Nature, 540, pp.124~128 (2016)
  45. Newton K, "RIPK1inhibits ZBP1-driven necroptosis during development", Nature, 540, pp.129~133 (2016)
  46. Schoggins JW, "Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity", Nature, 505, pp.691~695 (2014)
  47. Daniels BP, "The Nucleotide Sensor ZBP1 and Kinase RIPK3 Induce the Enzyme IRG1 to Promote an Antiviral Metabolic State in Neurons", Immunity, 50, pp.64~76 (2019)
  48. Lladser A, "DAI(DLM-1", ZBP1)as a genetic adjuvant for DNA vaccines that promotes effective antitumor CTL immunity, 2011, pp.19, 594~601
  49. Hirvinen M, "Expression of DAI by an oncolytic vaccinia virus boosts the immunogenicity of the virus and enhances antitumor immunity", Mol Ther Oncolytics, 3, pp.16002~ (2016)
  50. Jiao H, "Z-nucleic-acid sensing triggers ZBP1-dependent necroptosis and inflammation", Nature, 580, pp.391~395 (2020)
  51. Wang R, "Gut stem cell necroptosis by genome instability triggers bowel inflammation", Nature, 580, pp.386~390 (2020)
  52. Marshall PR, "Dynamic regulation of Z-DNA in the mouse prefrontal cortex by the RNAediting enzyme Adar1 is required for fear extinction", Nat Neurosci, 23, pp.718~729 (2020)

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