Skip to main content

Interstrand Cross-Linking of Nucleic Acids: From History to Recent and Future Applications

  • Chapter
  • First Online:
Modified Nucleic Acids in Biology and Medicine

Part of the book series: RNA Technologies ((RNATECHN))

Abstract

This chapter contains an elaborate overview of various methods that have been developed for interstrand cross-linking of nucleic acids. The existing cross-link methodologies can be subcategorized in different groups, each interesting depending on the requirements of the envisaged application. An endogenous or exogenous bifunctional compound can react with two different nucleophilic groups on the nucleobases, resulting in fast and high-yielding cross-linking. However, when site selectivity of the formed cross-link is desired, other approaches are required. Therefore, a series of methodologies are at hand where functionalities are introduced in oligonucleotide probes, which can be intrinsically reactive or can be triggered and activated at a selected time upon target recognition. In a third class, both strands are modified with orthogonal groups. After reaction of the introduced functionalities, a cross-link is formed at a specific and fixed position. The chapter ends with an overview of and outlook to present and future applications. It is thus shown that cross-linking agents can be exploited as useful therapeutic or diagnostic tools and have further proven their utility in the stabilization or structure elucidation of cross-linked systems aimed at studying and understanding the repair systems in a cell.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ali MM, Oishi M, Nagatsugi F et al (2006) Intracellular inducible alkylation system that exhibits antisense effects with greater potency and selectivity than the natural oligonucleotide. Angew Chem Int Ed Engl 45:3136–3140

    Article  CAS  PubMed  Google Scholar 

  • Alzeer J, Schärer OD (2006) A modified thymine for the synthesis of site-specific thymine-guanine DNA interstrand crosslinks. Nucleic Acids Res 34:4458–4466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amoah-Apraku B, Fang MZ, Guzman NJ (2000) A non-nucleotide-bridged DNA decoy inhibits renal epithelial nitric oxide synthase expression. Kidney Int 57:83–91

    Article  CAS  PubMed  Google Scholar 

  • Angelov T, Guainazzi A, Schärer OD (2009) Generation of DNA interstrand cross-links by post-synthetic reductive amination. Org Lett 11:661–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baskin JM, Prescher J a, Laughlin ST et al (2007) Copper-free click chemistry for dynamic in vivo imaging. Proc Natl Acad Sci USA 104:16793–16797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beda NV, Nedospasov AA (2006) Inorganic nitric oxide metabolites participating in no-dependent modifications of biopolymers. Russ J Bioorg Chem 32:1–22

    Article  CAS  Google Scholar 

  • Beda NV, Nedospasov AA (2007) NO-dependent modifications of nucleic acids. Russ J Bioorg Chem 33:181–212

    Article  CAS  Google Scholar 

  • Berka V, Yeh H-C, Gao D et al (2004) Redox function of tetrahydrobiopterin and effect of L-arginine on oxygen binding in endothelial nitric oxide synthase. Biochemistry 43:13137–13148

    Article  CAS  PubMed  Google Scholar 

  • Brookes P, Lawley PD (1961) The alkylation of guanosine and guanylic acid. J Chem Soc 3923–3928

    Google Scholar 

  • Carrette LLG, Gyssels E, Loncke J, Madder A (2014) A mildly inducible and selective cross-link methodology for RNA duplexes. Org Biomol Chem 12:931–935

    Article  CAS  PubMed  Google Scholar 

  • Castro CE, Kilchherr F, Kim D-N et al (2011) A primer to scaffolded DNA origami. Nat Methods 8:221–229

    Article  CAS  PubMed  Google Scholar 

  • Catalano MJ, Liu S, Andersen N et al (2015) Chemical structure and properties of interstrand cross-links formed by reaction of guanine residues with abasic sites in duplex DNA. J Am Chem Soc 137:3933–3945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caulfield JL, Wishnok JS, Tannenbaum SR (2003) Nitric oxide-induced interstrand cross-links in DNA. Chem Res Toxicol 16:571–574

    Article  CAS  PubMed  Google Scholar 

  • Cecchini S, Massen C, La Madeleine C et al (2005) Interstrand cross-link induction by UV radiation in bromodeoxyuridine- substituted DNA: dependence on DNA conformation. Biochemistry 44:16957–16966

    Article  CAS  PubMed  Google Scholar 

  • Chabot S, Teissié J, Golzio M (2015) Targeted electro-delivery of oligonucleotides for RNA interference: siRNA and antimiR. Adv Drug Deliv Rev 81:161–168

    Article  CAS  PubMed  Google Scholar 

  • Chaney SG, Sancar A (1996) DNA repair: enzymatic mechanisms and relevance to drug response. J Natl Cancer Inst 88:1346–1360

    Article  CAS  PubMed  Google Scholar 

  • Chapman EG, DeRose VJ (2012) Site-specific platinum(II) cross-linking in a ribozyme active site. J Am Chem Soc 134:256–262

    Article  CAS  PubMed  Google Scholar 

  • Cohen SM, Garland EM, St John M et al (1992) Acrolein initiates rat urinary bladder carcinogenesis. Cancer Res 52:3577–3581

    CAS  PubMed  Google Scholar 

  • Coleman RS, Kesicki EA (1995) Template-directed cross-linking of oligonucleotides: site-specific covalent modification of dG-N7 within duplex DNA. J Org Chem 60:6252–6253

    Article  CAS  Google Scholar 

  • Coleman RS, Pires RM (1997) Covalent cross-linking of duplex DNA using 4-thio-2′-deoxyuridine as a readily modifiable platform for introduction of reactive functionality into oligonucleotides. Nucleic Acids Res 25:4771–4777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Czerny C, Eder E, Rünger TM (1998) Genotoxicity and mutagenicity of the α, β-unsaturated carbonyl compound crotonaldehyde (butenal) on a plasmid shuttle vector. Mutat Res 407:125–134

    Article  CAS  PubMed  Google Scholar 

  • Decout J-L, Lhomme J (1992) Reversible photocycloaddition of a 4′,5′-dihydropsoralen derivative with thymine. Photochem Photobiol 56:431–440

    Article  CAS  PubMed  Google Scholar 

  • Dextraze ME, Cecchini S, Bergeron F et al (2009) Reaching for the other side: generating sequence-dependent interstrand cross-links with 5-bromodeoxyuridine and γ-rays. Biochemistry 48:2005–2011

    Article  CAS  PubMed  Google Scholar 

  • Dias N, Stein C (2002) Antisense oligonucleotides: basic concepts and mechanisms minireview antisense oligonucleotides: basic concepts and mechanisms. Mol Cancer Ther 1:347–355

    Article  CAS  PubMed  Google Scholar 

  • Doi T, Kashida H, Asanuma H (2015) Efficiency of [2 + 2] photodimerization of various stilbene derivatives within DNA duplex scaffold. Org Biomol Chem 13:4430–4437

    Article  CAS  PubMed  Google Scholar 

  • Dronkert ML, Kanaar R (2001) Repair of DNA interstrand cross-links. Mutat Res 486:217–247

    Article  CAS  PubMed  Google Scholar 

  • Dutta S, Chowdhury G, Gates KS (2007) Interstrand cross-links generated by abasic sites in duplex DNA. J Am Chem Soc 129:1852–1853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Efimov VA, Fedyunin SV (2010) Cross-linked nucleic acids: isolation, structure, and biological role. Biochemistry 75:1606–1627

    CAS  PubMed  Google Scholar 

  • El-Sagheer AH, Brown T (2008) Synthesis, serum stability and cell uptake of cyclic and hairpin decoy oligonucleotides for TCF/LEF and GLI transcription factors. Int J Pept Res Ther 14:367–372

    Article  CAS  Google Scholar 

  • El-Sagheer AH, Brown T (2012) Click nucleic acid ligation: applications in biology and nanotechnology. Acc Chem Res 45:1258–1267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Sagheer AH, Kumar R, Findlow S et al (2008) A very stable cyclic DNA miniduplex with just two base pairs. Chembiochem 9:50–52

    Article  CAS  PubMed  Google Scholar 

  • El-Yazbi AF, Loppnow GR (2014) Detecting UV-induced nucleic-acid damage. TrAC Trends Anal Chem 61:83–91

    Article  CAS  Google Scholar 

  • Facchinetti F, Amadei F, Geppetti P et al (2007) Alpha, beta-unsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. Am J Respir Cell Mol Biol 37:617–623

    Article  CAS  PubMed  Google Scholar 

  • Fire A, Xu S, Montgomery MK et al (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    Article  CAS  PubMed  Google Scholar 

  • Fischhaber P, Gall A, Duncan J et al (1999) Direct demonstration in synthetic oligonucleotides that N, N′-bis(2-chloroethyl)-nitrosourea cross-links N-1 of deoxyguanosine to N-3 of deoxycytidine on opposite strands of duplex DNA. Cancer Res 59:4363–4368

    CAS  PubMed  Google Scholar 

  • Fujimoto K, Konishi-Hiratsuka K, Sakamoto T et al (2010) Site-specific photochemical RNA editing. Chem Commun (Camb) 46:7545–7547

    Article  CAS  Google Scholar 

  • Galliani G, Pantarotto C (1983) The reaction of guanosine and 2′-deoxyguanosine with acrolein. Tetrahedron Lett 24:4491–4492

    Article  CAS  Google Scholar 

  • Gamboa Varela J, Gates KS (2015) A simple, high-yield synthesis of DNA duplexes containing a covalent, thermally cleavable interstrand cross-link at a defined location. Angew Chem Int Ed 54:7666–7669

    Article  CAS  Google Scholar 

  • Gao H, Chidambaram N, Chen BC et al (1994) Double-stranded cyclic oligonucleotides with non-nucleotide bridges. Bioconjug Chem 5:445–453

    Article  CAS  PubMed  Google Scholar 

  • Gerrard SR, Hardiman C, Shelbourne M et al (2012) A new modular approach to nanoassembly: stable and addressable DNA nanoconstructs via orthogonal click chemistries. ACS Nano 6:9221–9228

    Article  CAS  PubMed  Google Scholar 

  • Gilman A, Philips FS (1946) The biological actions and therapeutic applications of the b-chloroethyl amines and sulfides. Science 103:409–436

    Article  CAS  Google Scholar 

  • Glick GD (1998) Design, synthesis, and analysis of conformationally constrained nucleic acids. Biopolymers 48:83–96

    Article  CAS  PubMed  Google Scholar 

  • Goodsell DS (2001) The molecular perspective: ultraviolet light and pyrimidine dimers. Oncologist 6:298–299

    Article  CAS  PubMed  Google Scholar 

  • Greenberg MM (2014) Abasic and oxidized abasic site reactivity in DNA: enzyme inhibition, cross-linking, and nucleosome catalyzed reactions. Acc Chem Res 47:646–55

    Article  CAS  PubMed  Google Scholar 

  • Guainazzi A, Scharer O (2010) Using synthetic DNA interstrand crosslinks to elucidate repair pathways and identify new therapeutic targets for cancer chemotherapy. Cell Mol Life Sci 67:3683–3697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haque MM, Sun H, Liu S et al (2014) Photoswitchable formation of a DNA interstrand cross-link by a coumarin-modified nucleotide. Angew Chem Int Ed 53:7001–7005

    Article  CAS  Google Scholar 

  • Harris ME, Christian EL (2009) RNA crosslinking methods. Methods Enzymol 468:127–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harwood E a, Sigurdsson ST, Edfeldt NBF et al (1999a) Chemical synthesis and preliminary structural characterization of a nitrous acid interstrand cross-linked duplex DNA. J Am Chem Soc 121:5081–5082

    Article  CAS  Google Scholar 

  • Harwood EA, Sigurdsson ST, Edfeldt NBF et al (1999b) Chemical synthesis and preliminary structural characterization of a nitrous acid interstrand cross-linked duplex DNA. J Am Chem Soc 121:5081–5082

    Article  CAS  Google Scholar 

  • Hata T, Hoshi T, Kanamori K et al (1956) Mitomycin, a new antibiotic from streptomyces. I J Antibiot (Tokyo) 9:141–146

    CAS  Google Scholar 

  • Hatano A, Makita S, Kirihara M (2004) Synthesis and characterization of a DNA analogue stabilized by mercapto C-nucleoside induced disulfide bonding. Bioorganic Med Chem Lett 14:2459–2462

    Article  CAS  Google Scholar 

  • Hatano A, Okada M, Kawai G (2012) Solution structure of S-DNA formed by covalent base pairing involving a disulfide bond. Org Biomol Chem 10:7327–7333

    Article  CAS  PubMed  Google Scholar 

  • Hentschel S, Alzeer J, Angelov T et al (2012) Synthesis of DNA interstrand cross-links using a photocaged nucleobase. Angew Chem Int Ed 51:3466–3469

    Article  CAS  Google Scholar 

  • Higuchi M, Kobori A, Yamayoshi A et al (2009) Synthesis of antisense oligonucleotides containing 2′-O-psoralenylmethoxyalkyl adenosine for photodynamic regulation of point mutations in RNA. Bioorg Med Chem 17:475–483

    Article  CAS  PubMed  Google Scholar 

  • Higuchi M, Yamayoshi A, Yamaguchi T et al (2007) Selective photo-cross-linking of 2′-O-psoralen-conjugated oligonucleotide with RNAs having point mutations. Nucleosides Nucleotides Nucleic Acids 26:277–290

    Article  CAS  PubMed  Google Scholar 

  • Hong IS, Ding H, Greenberg MM (2006a) Oxygen independent DNA interstrand cross-link formation by a nucleotide radical. J Am Chem Soc 128:485–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong IS, Ding H, Greenberg MM (2006b) Radiosensitization by a modified nucleotide that produces DNA interstrand cross-links under hypoxic conditions. J Am Chem Soc 128:2230–2231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong IS, Greenberg MM (2005a) Efficient DNA interstrand cross-link formation from a nucleotide radical. J Am Chem Soc 127:3692–3693

    Article  CAS  PubMed  Google Scholar 

  • Hong IS, Greenberg MM (2005b) DNA interstrand cross-link formation initiated by reaction between singlet oxygen and a modified nucleotide. J Am Chem Soc 127(30):10510–10511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou D, Greenberg MM (2014) DNA interstrand cross-linking upon irradiation of aryl halide C-nucleotides. J Org Chem 79:1877–1884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichikawa K, Kojima N, Hirano Y et al (2012) Interstrand cross-link of DNA by covalently linking a pair of abasic sites. Chem Commun 48:2143–2145

    Article  CAS  Google Scholar 

  • Imoto S, Chikuni T, Kansui H et al (2012) Fast DNA interstrand cross-linking reaction by 6-vinylpurine. Nucleosides Nucleotides Nucleic Acids 31:752–762

    Article  CAS  PubMed  Google Scholar 

  • Ingale SA, Seela F (2013) Stepwise click functionalization of DNA through a bifunctional azide with a chelating and a nonchelating azido group. J Org Chem 78:3394–3399

    Article  CAS  PubMed  Google Scholar 

  • Ipsaro JJ, Joshua-Tor L (2015) From guide to target: molecular insights into eukaryotic RNA-interference machinery. Nat Struct Mol Biol 22:20–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jawalekar AM, Op de Beeck M, van Delft FL et al (2011) Synthesis and incorporation of a furan-modified adenosine building block for DNA interstrand crosslinking. Chem Commun (Camb) 47:2796–2798

    Article  CAS  Google Scholar 

  • Johnson KM, Price NE, Wang J et al (2013) On the formation and properties of interstrand DNA-DNA cross-links forged by reaction of an abasic site with the opposing guanine residue of 5′-CAp sequences in duplex DNA. J Am Chem Soc 135:1015–1025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kashida H, Doi T, Sakakibara T et al (2013) p-Stilbazole moieties as artificial base pairs for photo-cross-linking of DNA duplex. J Am Chem Soc 135:7960–7966

    Article  CAS  PubMed  Google Scholar 

  • Kawanishi M, Matsuda T, Nakayama A et al (1998) Molecular analysis of mutations induced by acrolein in human fibroblast cells using supF shuttle vector plasmids. Mutat Res 417:65–73

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki T, Nagatsugi F, Ali MM et al (2005) Hybridization-promoted and cytidine-selective activation for cross-linking with the use of 2-amino-6-vinylpurine derivatives. J Org Chem 70:14–23

    Article  CAS  PubMed  Google Scholar 

  • Kean JM, Murakami A, Blake KR et al (1988) Photochemical cross-linking of psoralen-derivatized oligonucleoside methylphosphonates to rabbit globin messenger RNA. Biochemistry 27:9113–9121

    Article  CAS  PubMed  Google Scholar 

  • Klockenbusch C, O’Hara JE, Kast J (2012) Advancing formaldehyde cross-linking towards quantitative proteomic applications. Anal Bioanal Chem 404:1057–1067

    Article  CAS  PubMed  Google Scholar 

  • Kobertz WR, Essigmann JM (1997) Solid-phase synthesis of oligonucleotides containing a site-specific psoralen derivative. J Am Chem Soc 119:5960–5961

    Article  CAS  Google Scholar 

  • Kocalka P, El-Sagheer AH, Brown T (2008) Rapid and efficient DNA strand cross-linking by click chemistry. Chembiochem 9:1280–1285

    Article  CAS  PubMed  Google Scholar 

  • Kusano S, Haruyama T, Ishiyama S et al (2014) Development of the crosslinking reactions to RNA triggered by oxidation. Chem Commun (Camb) 50:3951–3954

    Article  CAS  Google Scholar 

  • Lee BL, Murakami A, Blake KR et al (1988) Interaction of psoralen-derivatized oligodeoxyribonucleoside methylphosphonates with single-stranded DNA. Biochemistry 27:3197–3203

    Article  CAS  PubMed  Google Scholar 

  • Leonard NJ, Barrio JR (1984) Etheno-substituted nucleotides and coenzymes: fluorescence and biological activity. Crit Rev Biochem Mol Biol 15:125–199

    Article  CAS  Google Scholar 

  • Li HY, Qiu YL, Moyroud E et al (2001) Synthesis of DNA oligomers possessing a covalently cross-linked Watson–Crick base pair model. Angew Chem Int Ed Engl 113:1519–1523

    Article  Google Scholar 

  • Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715

    Article  CAS  PubMed  Google Scholar 

  • Lukhtanov EA, Mills AG, Kutyavin IV et al (1997) Minor groove DNA alkylation directed by major groove triplex forming oligodeoxyribonucleotides. Nucleic Acids Res 25:5077–5084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lukhtanov EA, Podyminogin MA, Kutyavin IV et al (1996) Rapid and efficient hybridization-triggered crosslinking within a DNA duplex by an oligodeoxyribonucleotide bearing a conjugated cyclopropapyrroloindole. Nucleic Acids Res 24:683–687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lundberg EP, El-Sagheer AH, Kocalka P et al (2010) A new fixation strategy for addressable nano-network building blocks. Chem Commun 46:3714–3716

    Article  CAS  Google Scholar 

  • Maruenda H, Tomasz M (1996) Antisense sequence-directed cross-linking of DNA oligonucleotides by mitomycin C. Bioconjug Chem 7:541–544

    Article  CAS  PubMed  Google Scholar 

  • Matsuyama Y, Yamayoshi A, Kobori A et al (2014) Functional regulation of RNA-induced silencing complex by photoreactive oligonucleotides. Bioorg Med Chem 22:1003–1007

    Article  CAS  PubMed  Google Scholar 

  • Millard JT, White MM (1993) Diepoxybutane cross-links DNA at 5′-GNC sequences. Biochemistry 32:2120–2124

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee S, Guainazzi A, Schärer OD (2014) Synthesis of structurally diverse major groove DNA interstrand crosslinks using three different aldehyde precursors. Nucleic Acids Res 42:7429–7435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murakami A, Yamamoto Y, Namba M et al (2001) Photo-cross-linked oligonucleotide duplex as a decoy-DNA for inhibition of restriction endonuclease activity. Bioorg Chem 29:223–233

    Article  CAS  PubMed  Google Scholar 

  • Nagatsugi F, Kawasaki T, Usui D et al (1999) Highly efficient and selective cross-linking to cytidine based on a new strategy for auto-activation within a duplex. J Am Chem Soc 121:6753–6754

    Article  CAS  Google Scholar 

  • Nakamura S, Fujimoto K (2014) Creation of DNA array structure equipped with heat resistance by ultrafast photocrosslinking. J Chem Technol Biotechnol 89:1086–1090

    Article  CAS  Google Scholar 

  • Nishikawa H, Hayakawa T, Sakai T (1987) Determination of acrolein and crotonaldehyde in automobile exhaust gas by gas chromatography with electron-capture detection. Analyst 112:859–862

    Article  CAS  PubMed  Google Scholar 

  • Noll DM, Mason TM, Miller PS (2006) Formation and repair of interstrand cross-links in DNA. Chem Rev 106:277–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noll DM, Noronha AM, Miller PS (2001) Synthesis and characterization of DNA duplexes containing an N4C-ethyl-N4C interstrand cross-link. J Am Chem Soc 123:3405–3411

    Article  CAS  PubMed  Google Scholar 

  • Norman D, Live D, Sastry M et al (1990) NMR and computational characterization of mitomycin cross-linked to adjacent deoxyguanosines in the minor groove of the d(T-A-C-G-T-A).cntdot.d(T-A-C-G-T-A) duplex. Biochemistry 29:2861–2875

    Article  CAS  PubMed  Google Scholar 

  • Noronha AM, Noll DM, Wilds CJ et al (2002) N4C-ethyl-N4C cross-linked DNA: synthesis and characterization of duplexes with interstrand cross-links of different orientations. Biochemistry 41:760–771

    Article  CAS  PubMed  Google Scholar 

  • Op de Beeck M, Madder A (2011) Unprecedented C-selective interstrand cross-linking through in situ oxidation of furan-modified oligodeoxynucleotides. J Am Chem Soc 133:796–807

    Article  CAS  PubMed  Google Scholar 

  • Op De Beeck M, Madder A (2012) Sequence specific DNA cross-linking triggered by visible light. J Am Chem Soc 134:10737–10740

    Article  CAS  PubMed  Google Scholar 

  • Orlando V, Strutt H, Paro R (1997) Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11:205–214

    Article  CAS  PubMed  Google Scholar 

  • Osborne SE, Völker J, Stevens SY et al (1996) Design, synthesis, and analysis of disulfide cross-linked DNA duplexes. J Am Chem Soc 118:11993–12003

    Article  CAS  Google Scholar 

  • Paz MM, Kumar GS, Glover M et al (2004) Mitomycin dimers: polyfunctional cross-linkers of DNA. J Med Chem 47:3308–3319

    Article  CAS  PubMed  Google Scholar 

  • Peng X, In SH, Li H et al (2008) Interstrand cross-link formation in duplex and triplex DNA by modified pyrimidines. J Am Chem Soc 130:10299–10306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price NE, Johnson KM, Wang J et al (2014) Interstrand DNA-DNA cross-link formation between adenine residues and abasic sites in duplex DNA. J Am Chem Soc 136:3483–3490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pujari SS, Leonard P, Seela F (2014) Oligonucleotides with “clickable” sugar residues: synthesis, duplex stability, and terminal versus central inter-strand cross-linking of 2′-O-propargylated 2-aminoadenosine with a bifunctional azide. J Org Chem 79:4423–4437

    Article  CAS  PubMed  Google Scholar 

  • Pujari SS, Seela F (2012) Cross-linked DNA: propargylated ribonucleosides as “click” ligation sites for bifunctional azides. J Org Chem 77:4460–4465

    Article  CAS  PubMed  Google Scholar 

  • Pujari SS, Seela F (2013) Parallel stranded DNA stabilized with internal sugar cross-links: synthesis and click ligation of oligonucleotides containing 2′-propargylated isoguanosine. J Org Chem 78:8545–8561

    Article  CAS  PubMed  Google Scholar 

  • Pujari SS, Xiong H, Seela F (2010) Cross-linked DNA generated by “bis-click” reactions with bis-functional azides: site independent ligation of oligonucleotides via nucleobase alkynyl chains. J Org Chem 75:8693–8696

    Article  CAS  PubMed  Google Scholar 

  • Rajendran A, Endo M, Katsuda Y et al (2011) Photo-cross-linking-assisted thermal stability of DNA origami structures and its application for higher-temperature self-assembly. J Am Chem Soc 133:14488–14491

    Article  CAS  PubMed  Google Scholar 

  • Rajski SR, Williams RM (1998) DNA cross-linking agents as antitumor drugs. Chem Rev 98:2723–2796

    Article  CAS  PubMed  Google Scholar 

  • Reishus JW, Martin DS (1961) cis-Dichlorodiammineplatinum(ii): acid hydrolysis and isotopic exchange of the chloride ligands 1. J Am Chem Soc 83:2457–2462

    Article  CAS  Google Scholar 

  • Rothemund PWK (2006) Folding DNA to create nanoscale shapes and patterns. Nature 440:297–302

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T, Ooe M, Fujimoto K (2015a) Critical effect of base pairing of target pyrimidine on the interstrand photo-cross-linking of DNA via 3-cyanovinylcarbazole nucleoside. Bioconjug Chem 26:1475–1478

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T, Shigeno A, Ohtaki Y et al (2014) Photo-regulation of constitutive gene expression in living cells by using ultrafast photo-cross-linking oligonucleotides. Biomater Sci 2:1154–1157

    Article  CAS  Google Scholar 

  • Sakamoto T, Tanaka Y, Fujimoto K (2015b) DNA photo-cross-linking using 3-cyanovinylcarbazole modified oligonucleotide with threoninol linker. Org Lett 17:3–6

    Article  CAS  Google Scholar 

  • Sanada M, Hidaka M, Takagi Y et al (2007) Modes of actions of two types of anti-neoplastic drugs, dacarbazine and ACNU, to induce apoptosis. Carcinogenesis 28:2657–2663

    Article  CAS  PubMed  Google Scholar 

  • Schärer OD (2003) Chemistry and biology of DNA repair. Angew Chem Int Ed Engl 42:2946–2974

    Article  PubMed  CAS  Google Scholar 

  • Seeman NC (1982) Nucleic acid junctions and lattices. J Theor Biol 99:237–247

    Article  CAS  PubMed  Google Scholar 

  • Shapiro R, Cohen BI, Shiuey S-J et al (1969) Reaction of guanine with glyoxal, pyruvaldehyde, and kethoxal, and the structure of the acylguanines. Synthesis of N2-alkylguanines. Biochemistry 8:238–245

    Article  CAS  PubMed  Google Scholar 

  • Shapiro R, Dubelman S, Feinberg AM et al (1977) Isolation and identification of cross-linked nucleosides from nitrous acid treated deoxyribonucleic acid. J Am Chem Soc 99:302–303

    Article  CAS  PubMed  Google Scholar 

  • Shelbourne M, Brown T, El-Sagheer AH et al (2012) Fast and efficient DNA crosslinking and multiple orthogonal labelling by copper-free click chemistry. Chem Commun 48:11184–11186

    Article  CAS  Google Scholar 

  • Singh I, Vyle JS, Heaney F (2009) Fast, copper-free click chemistry: a convenient solid-phase approach to oligonucleotide conjugation. Chem Commun 3276–3278

    Google Scholar 

  • Singh I, Freeman C, Madder A, Vyle JS, Heaney F (2012) Fast RNA conjugations on solid phase by strain-promoted cycloadditions. Org Biomol Chem 10:6633–6639

    Article  CAS  PubMed  Google Scholar 

  • Sloane JL, Greenberg MM (2014) Interstrand cross-link and bioconjugate formation in RNA from a modified nucleotide. J Org Chem 79:9792–9798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith MB, Schmidt BF, Czerwinski G et al (1996) Specificity of DNA alkylation by 1-(2-chloroethyl)-3-alkyl-3-acyltriazenes depends on the structure of the acyl group: kinetic and product studies. Chem Res Toxicol 9:466–475

    Article  CAS  PubMed  Google Scholar 

  • Stevens K, Madder A (2009) Furan-modified oligonucleotides for fast, high-yielding and site-selective DNA inter-strand cross-linking with non-modified complements. Nucleic Acids Res 37:1555–1565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stone MP, Cho Y-J, Huang H et al (2008) Interstrand DNA cross-links induced by alpha, beta-unsaturated aldehydes derived from lipid peroxidation and environmental sources. Acc Chem Res 41:793–804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun H, Fan H, Peng X (2014) Quantitative DNA interstrand cross-link formation by coumarin and thymine: structure determination, sequence effect, and fluorescence detection. J Org Chem 79:11359–11369

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Yamada M, Nakamura T et al (2000) Products of the reaction between a diazoate derivative of 2′-deoxycytidine and l -lysine and its implication for DNA—nucleoprotein cross-linking by NO or HNO 2. Chem Res Toxicol 13:1223–1227

    Article  CAS  PubMed  Google Scholar 

  • Swenberg JA, Moeller BC, Lu K et al (2013) Formaldehyde carcinogenicity research: 30 years and counting for mode of action, epidemiology, and cancer risk assessment. Toxicol Pathol 41:181–189

    Article  PubMed  CAS  Google Scholar 

  • Tagawa M, Shohda K, Fujimoto K et al (2011) Stabilization of DNA nanostructures by photo-cross-linking. Soft Matter 7:10931–10934

    Article  CAS  Google Scholar 

  • Tomasz M (1995) Mitomycin C: small, fast and deadly (but very selective). Chem Biol 2:575–579

    Article  CAS  PubMed  Google Scholar 

  • Tong WP, Ludlum DB (1981) Formation of the cross-linked base, diguanylethane, in DNA treated with N, N′-Bis(2-chloroethyl)-N-nitrosourea. Cancer Res 41:380–382

    CAS  PubMed  Google Scholar 

  • Wakaki S, Marumo H, Tomioka K et al (1958) Isolation of new fractions of antitumor mitomycins. Antibiot Chemother 8:228–240

    CAS  Google Scholar 

  • Webb TR, Matteucci MD (1986a) Sequence-specific cross-linking of deoxyoligonucleotides via hybridization-triggered alkylation. J Am Chem Soc 108:2764–2765

    Article  CAS  Google Scholar 

  • Webb TR, Matteucci MD (1986b) Hybridization triggered cross-linking of deoxyoligonucleotides. Nucleic Acids Res 14:7661–7674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilds CJ, Booth JD, Noronha AM (2006) Synthesis of oligonucleotides containing an O6-G-alkyl-O6-G interstrand cross-link. Tetrahedron Lett 47:9125–9128

    Article  CAS  Google Scholar 

  • Wilds CJ, Noronha AM, Robidoux S et al (2004) Mispair-aligned N3T-alkyl-N3T interstrand cross-linked DNA: synthesis and characterization of duplexes with interstrand cross-links of variable lengths. J Am Chem Soc 126:9257–9265

    Article  CAS  PubMed  Google Scholar 

  • Xiaorong H, Gang W, Gaffney BL et al (2009) Synthesis of guanosine and deoxyguanosine phosphoramidites with cross-linkable thioalkyl tethers for direct incorporation into RNA and DNA. Nucleosides Nucleotides Nucleic Acids 28:1076–1094

    Article  CAS  Google Scholar 

  • Xiong H, Seela F (2011) Stepwise “click” chemistry for the template independent construction of a broad variety of cross-linked oligonucleotides: influence of linker length, position, and linking number on DNA duplex stability. J Org Chem 76:5584–5597

    Article  CAS  PubMed  Google Scholar 

  • Xiong H, Seela F (2012) Cross-linked DNA: site-selective “click” ligation in duplexes with bis-azides and stability changes caused by internal cross-links. Bioconjug Chem 23:1230–1243

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Suzuki Y, Komiyama M (2009) Click chemistry for the identification of G-quadruplex structures: discovery of a DNA-RNA G-quadruplex. Angew Chem Int Ed Engl 48:3281–3284

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Fujimoto K (2008) Ultrafast reversible photo-cross-linking reaction: toward in situ DNA manipulation. Org Lett 10:3227–3230

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Ohtake T, Okada H et al (2009) A new approach for reversible RNA photocrosslinking reaction: application to sequence-specific RNA selection. ChemBioChem 10:1473–1476

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Annemieke Madder .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Gyssels, E., De Laet, N., Lumley, E., Madder, A. (2016). Interstrand Cross-Linking of Nucleic Acids: From History to Recent and Future Applications. In: Jurga, S., Erdmann (Deceased), V., Barciszewski, J. (eds) Modified Nucleic Acids in Biology and Medicine. RNA Technologies. Springer, Cham. https://doi.org/10.1007/978-3-319-34175-0_15

Download citation

Publish with us

Policies and ethics