Australian Journal of Chemistry Australian Journal of Chemistry Society
An international journal for chemical science
RESEARCH FRONT

Developments in Electrospray Ionization Mass Spectrometry of Non-Covalent DNA–Ligand Complexes

Jennifer L. Beck

School of Chemistry, University of Wollongong, NSW 2522, Australia. Email: jbeck@uow.edu.au




Jennifer's undergraduate and Ph.D. studies were carried out at the University of Queensland. Her Ph.D. was titled ‘Metal Ion Binding Sites of Purple Phosphatases’. The theme of biological chemistry was continued through her postdoctoral appointments: first at the University of Illinois at Urbana-Champaign (electron transfer pathways between cytochrome P-450cam and putidaredoxin) and later at the ANU (protein subunits of DNA polymerase III of E. coli). After a substantial career interruption, she re-entered science in the new field of biomolecular mass spectrometry at the University of Wollongong. Her current work involves applications of ESI-MS and other biophysical techniques to investigate non-covalent complexes of the E. coli replisome, DNA–ligand complexes, and new work involves qDNA-associated proteins.

Australian Journal of Chemistry 64(6) 705-717 http://dx.doi.org/10.1071/CH11046
Submitted: 26 January 2011  Accepted: 13 April 2011   Published: 27 June 2011

Abstract

Many anti-cancer drugs function by binding non-covalently to double-stranded (ds) DNA. Electrospray ionization mass spectrometry (ESI-MS) has emerged over the past decade as a sensitive technique for the determination of stoichiometries and relative binding affinities of DNA–ligand interactions. The chromosome contains nucleotide sequences, for example, guanosine-rich regions, that predispose them to the formation of higher order structures such as quadruplex DNA (qDNA). Sequences that form qDNA are found in the telomeres. The proposal that ligands that stabilize qDNA might interfere with the activity of telomerase in cancer cells has stimulated the search for ligands that are selective for qDNA over dsDNA. The insights gained from the development of ESI-MS methods for analysis of non-covalent dsDNA–ligand complexes are now being applied in the search for qDNA-selective ligands. ESI-MS is a useful first-pass screening technique for qDNA-binding ligands. This short review describes some experimental considerations for ESI-MS analysis of DNA–ligand complexes, briefly addresses the question of whether non-covalent DNA–ligand complexes are faithfully transferred from solution to the gas phase, discusses ion mobility mass spectrometry as a technique for probing this issue, and highlights some recent ESI-MS studies of qDNA-selective ligands.


References

[1]  C. M. Whitehouse, R. N. Dreyer, M. Yamashita, J. B. Fenn, Anal. Chem. 1985, 57, 675.
         | CrossRef | 1:CAS:528:DyaL2MXovFeksw%3D%3D&md5=80f8cf6c67cf4ef1e14355f84addc7ceCAS | 2581476PubMed | open url image1

[2]  F. Sanger, Science 1959, 129, 1340.
         | CrossRef | 1:CAS:528:DyaG1MXnsl2lsg%3D%3D&md5=6d59fed613149c398eaff183afd4ab1fCAS | 13658959PubMed | open url image1

[3]  F. Sanger, Science 1981, 214, 1205.
         | CrossRef | 1:CAS:528:DyaL38XjtV2nsw%3D%3D&md5=4e5c8d1a797f836c761b0529c1db5832CAS | 7302589PubMed | open url image1

[4]  V. C. Wasinger, S. J. Cordwell, A. Cerpapoljak, J. X. Yan, A. A. Gooley, M. R. Wilkins, M. W. Duncan, R. Harris, K. L. Williams, I. Humpherysmith, Electrophoresis 1995, 16, 1090.
         | CrossRef | 1:CAS:528:DyaK2MXntF2lsLg%3D&md5=cb3cb2b3012deb082da8b468507675e7CAS | 7498152PubMed | open url image1

[5]  R. D. Smith, Trends Biotechnol. 2002, 20, S3.
         | CrossRef | 1:CAS:528:DC%2BD38XpsFSns7o%3D&md5=cdc2aef5d417cafeba0fd7a5eb3393efCAS | 12570152PubMed | open url image1

[6]  J. L. Beck, M. L. Colgrave, S. F. Ralph, M. M. Sheil, Mass Spectrom. Rev. 2001, 20, 61.
         | CrossRef | 1:CAS:528:DC%2BD3MXls1OhsLY%3D&md5=128cc76c374b3cba148f189f1bebe7a8CAS | 11455562PubMed | open url image1

[7]  J. L. P. Benesch, B. T. Ruotolo, D. A. Simmons, C. V. Robinson, Chem. Rev. 2007, 107, 3544.
         | CrossRef | 1:CAS:528:DC%2BD2sXotVKhu7Y%3D&md5=31df4573a418479000bc4e5c31940c7fCAS | 17649985PubMed | open url image1

[8]  J. S. Brodbelt, Annu. Rev. Anal. Chem. 2010, 3, 67.
         | CrossRef | 1:CAS:528:DC%2BC3cXhtVOlsr%2FF&md5=7f97ac54cda8e36fa6045fcbe878f4faCAS | open url image1

[9]  D. Fabris, J. Am. Soc. Mass Spectrom. 2010, 21, 1.
         | CrossRef | 1:CAS:528:DC%2BC3cXjslymug%3D%3D&md5=5ccf9ea9e45fa4a3a048884c1b05ea81CAS | 19897384PubMed | open url image1

[10]  P. Belmont, J. F. Constant, M. Demeunynck, Chem. Soc. Rev. 2001, 30, 70.
         | CrossRef | 1:CAS:528:DC%2BD3MXkt1Oisw%3D%3D&md5=b99cd72191dbba2d58f57eed98c66190CAS | open url image1

[11]  A. Rich, S. G. Zhang, Nat. Rev. Genet. 2003, 4, 566.
         | CrossRef | 1:CAS:528:DC%2BD3sXltVWnsr8%3D&md5=b03aa45966d86fc410c1b1506887dcefCAS | 12838348PubMed | open url image1

[12]  G. L. Wang, L. A. Christensen, K. M. Vasquez, Proc. Natl. Acad. Sci. USA 2006, 103, 2677.
         | CrossRef | 1:CAS:528:DC%2BD28XksF2rtr8%3D&md5=111f78cc69935a349cafb0c3e3cc9e24CAS | open url image1

[13]  J. R. Goni, X. de la Cruz, M. Orozco, Nucleic Acids Res. 2004, 32, 354.
         | CrossRef | 1:CAS:528:DC%2BD2cXhtlKgtrc%3D&md5=c9e00830ba210587fab942866a274a62CAS | 14726484PubMed | open url image1

[14]  N. V. Hud, P. Schultze, V. Sklenar, J. Feigon, J. Mol. Biol. 1999, 285, 233.
         | CrossRef | 1:CAS:528:DyaK1MXntFCruw%3D%3D&md5=8945c90abbc859ce41ad932c78c1ae5bCAS | 9878402PubMed | open url image1

[15]  S. Neidle, G. N. Parkinson, Biochimie 2008, 90, 1184.
         | CrossRef | 1:CAS:528:DC%2BD1cXptVWlt7c%3D&md5=d71c499c97c7ba9a09cd45bea600b120CAS | 18395014PubMed | open url image1

[16]  S. Burge, G. N. Parkinson, P. Hazel, A. K. Todd, S. Neidle, Nucleic Acids Res. 2006, 34, 5402.
         | CrossRef | 1:CAS:528:DC%2BD28Xht1Srt7fM&md5=b0b6764486434aeaa1a51d7dc19d488bCAS | 17012276PubMed | open url image1

[17]  A. T. Phan, V. Kuryavyi, H. Y. Gaw, D. J. Patel, Nat. Chem. Biol. 2005, 1, 167.
         | CrossRef | 1:CAS:528:DC%2BD2MXmt1ygsr8%3D&md5=f776f7059635066d98abd41d39ecee6eCAS | 16408022PubMed | open url image1

[18]  N. W. Kim, M. A. Piatyszek, K. R. Prowse, C. B. Harley, M. D. West, P. L. C. Ho, G. M. Coviello, W. E. Wright, S. L. Weinrich, J. W. Shay, Science 1994, 266, 2011.
         | CrossRef | 1:CAS:528:DyaK2MXisl2lu7g%3D&md5=82b8296935088d093c7cc87ce0c75875CAS | 7605428PubMed | open url image1

[19]  S. Neidle, FEBS J. 2010, 277, 1118.
         | CrossRef | 1:CAS:528:DC%2BC3cXivVSmtr4%3D&md5=923796ca1143980b3c0e45ffbaaf73bbCAS | 19951354PubMed | open url image1

[20]  S. V. S. Mariappan, X. Cheng, R. B. van Breemen, L. A. Silks, G. Gupta, Anal. Biochem. 2004, 334, 216.
         | CrossRef | 1:CAS:528:DC%2BD2cXos1Kls78%3D&md5=ffb7cd3e20e0c7e9bc5b4c489e6619eaCAS | 15494127PubMed | open url image1

[21]  F. Rosu, V. Gabelica, C. Houssier, P. Colson, E. De Pauw, Rapid Commun. Mass Spectrom. 2002, 16, 1729.
         | CrossRef | 1:CAS:528:DC%2BD38XntlOnsLo%3D&md5=5245eda81d5a7b1474121b8d18937e4aCAS | 12207360PubMed | open url image1

[22]  S. J. Gaskell, J. Mass Spectrom. 1997, 32, 677.
         | CrossRef | 1:CAS:528:DyaK2sXkvFCnsLc%3D&md5=8f646027a4a2d05d8545bb6a196f57e1CAS | open url image1

[23]  E. Nordhoff, F. Kirpekar, P. Roepstorff, Mass Spectrom. Rev. 1996, 15, 67.
         | CrossRef | open url image1

[24]  K. J. Light-Wahl, D. L. Springer, B. E. Winger, C. G. Edmonds, D. G. Camp, B. D. Thrall, R. D. Smith, J. Am. Chem. Soc. 1993, 115, 803.
         | CrossRef | 1:CAS:528:DyaK3sXitFens7c%3D&md5=fa2a93b6414efc6e8deaa0456e193a99CAS | open url image1

[25]  E. Bayer, T. Bauer, K. Schmeer, K. Bleicher, M. Maler, H. J. Gaus, Anal. Chem. 1994, 66, 3858.
         | CrossRef | 1:CAS:528:DyaK2cXmslekurc%3D&md5=6129aa6585e91a586336f24c549044faCAS | 7810895PubMed | open url image1

[26]  D. C. Gale, D. R. Goodlett, K. J. Lightwahl, R. D. Smith, J. Am. Chem. Soc. 1994, 116, 6027.
         | CrossRef | 1:CAS:528:DyaK2cXkslaqs78%3D&md5=cde71d69e4d88db7a8ab5c1acdc228adCAS | open url image1

[27]  A. Kapur, J. L. Beck, M. M. Sheil, Rapid Commun. Mass Spectrom. 1999, 13, 2489.
         | CrossRef | 1:CAS:528:DC%2BD3cXhtFWjsg%3D%3D&md5=c16c38f94a828e719108d51b8da53decCAS | 10589098PubMed | open url image1

[28]  V. Gabelica, E. De Pauw, F. Rosu, J. Mass Spectrom. 1999, 34, 1328.
         | CrossRef | 1:CAS:528:DC%2BD3cXht1aluw%3D%3D&md5=1d562ee4680c801d10ed29c475e67debCAS | 10587629PubMed | open url image1

[29]  K. X. Wan, T. Shibue, M. L. Gross, J. Am. Chem. Soc. 2000, 122, 300.
         | CrossRef | 1:CAS:528:DC%2BD3cXovVY%3D&md5=b2298d1d33bfdea8607e817c8e85b1ddCAS | open url image1

[30]  R. Gupta, J. L. Beck, S. F. Ralph, M. M. Sheil, J. R. Aldrich-Wright, J. Am. Soc. Mass Spectrom. 2004, 15, 1382.
         | CrossRef | 1:CAS:528:DC%2BD2cXotFGls7k%3D&md5=c85143bfefddecabb4d32b4b54d3c3feCAS | 15465350PubMed | open url image1

[31]  R. Gupta, A. Kapur, J. L. Beck, M. M. Sheil, Rapid Commun. Mass Spectrom. 2001, 15, 2472.
         | CrossRef | 1:CAS:528:DC%2BD38XjtVKgtg%3D%3D&md5=82ab1a2a89058695f6263474f5ede072CAS | 11746919PubMed | open url image1

[32]  T. Urathamakul, D. J. Waller, J. L. Beck, J. R. Aldrich-Wright, S. F. Ralph, Inorg. Chem. 2008, 47, 6621.
         | CrossRef | 1:CAS:528:DC%2BD1cXot1ahur8%3D&md5=54bc6909b5a793e69dda2166e6033e52CAS | 18611003PubMed | open url image1

[33]  V. Gabelica, F. Rosu, C. Houssier, E. De Pauw, Rapid Commun. Mass Spectrom. 2000, 14, 464.
         | CrossRef | 1:CAS:528:DC%2BD3cXitFWhtbc%3D&md5=6f5debdd8b7e964c494b7e30de0489fcCAS | 10717657PubMed | open url image1

[34]  D. R. Goodlett, D. G. Camp, C. C. Hardin, M. Corregan, R. D. Smith, Biol. Mass Spectrom. 1993, 22, 181.
         | CrossRef | 1:CAS:528:DyaK3sXltlCksLo%3D&md5=a5c3817def5d6a26be359a7d748bdd18CAS | 8461341PubMed | open url image1

[35]  J. Garcia de la Torre, S. Navarro, M. C. L. Martinez, Biophys. J. 1994, 66, 1573.
         | CrossRef | 1:STN:280:DyaK2czjvFemtA%3D%3D&md5=a827d2d926cfb904690c0a76595a8642CAS | 8061206PubMed | open url image1

[36]  H. R. Drew, R. M. Wing, T. Takano, C. Broka, S. Tanaka, K. Itakura, R. E. Dickerson, Proc. Natl. Acad. Sci. USA 1981, 78, 2179.
         | CrossRef | 1:CAS:528:DyaL3MXktVajt74%3D&md5=03975d5a98c74ddb2bf8785c88939a52CAS | open url image1

[37]  V. Gabelica, E. De Pauw, Int. J. Mass Spectrom. 2002, 219, 151.
         | CrossRef | 1:CAS:528:DC%2BD38XmtVWksrY%3D&md5=30d6a71297ae0155e4e35b8864e025c9CAS | open url image1

[38]  C. Kelso, V. Tillott, J. D. Rojas, R. L. A. Furlan, G. Padilla, J. L. Beck, Arch. Biochem. Biophys. 2008, 477, 348.
         | CrossRef | 1:CAS:528:DC%2BD1cXhtVOit7bM&md5=f19adaf7d70b9cd333ff34b978890392CAS | 18541138PubMed | open url image1

[39]  W. M. David, J. Brodbelt, S. M. Kerwin, P. W. Thomas, Anal. Chem. 2002, 74, 2029.
         | CrossRef | 1:CAS:528:DC%2BD38XisVart7g%3D&md5=bb8c12b98057c0e4958474e2098f14b5CAS | 12033303PubMed | open url image1

[40]  K. C. Gornall, S. Samosorn, J. Talib, J. B. Bremner, J. L. Beck, Rapid Commun. Mass Spectrom. 2007, 21, 1759.
         | CrossRef | 1:CAS:528:DC%2BD2sXmt1Omsr8%3D&md5=a34c8b0e41bc248d20e3d3abdfa59291CAS | 17486674PubMed | open url image1

[41]  S. E. Pierce, J. M. Wang, J. Jayawickramarajah, A. D. Hamilton, J. S. Brodbelt, Chemistry 2009, 15, 11244.
         | CrossRef | 1:CAS:528:DC%2BD1MXhtlWlsLbN&md5=7756839e40c6b78b75406567fe8ad903CAS | 19746468PubMed | open url image1

[42]  D. J. Douglas, A. J. Frank, D. M. Mao, Mass Spectrom. Rev. 2005, 24, 1.
         | CrossRef | 1:CAS:528:DC%2BD2MXmsFWlsA%3D%3D&md5=7d3e1d4dadb605e4b3aed6ca36592a7eCAS | 15389865PubMed | open url image1

[43]  A. El-Aneed, A. Cohen, J. Banoub, Appl. Spectrosc. Rev. 2009, 44, 210.
         | CrossRef | 1:CAS:528:DC%2BD1MXivFyntbo%3D&md5=aa0ca7b547089e3232a00df2e56063f3CAS | open url image1

[44]  W. J. Griffiths, A. P. Jonsson, S. Y. Liu, D. K. Rai, Y. Q. Wang, Biochem. J. 2001, 355, 545.
         | 1:CAS:528:DC%2BD3MXjslCntb8%3D&md5=8ba18f28fce9fc6b5d6c3c947cfd55fcCAS | 11311115PubMed | open url image1

[45]  M. Guilhaus, D. Selby, V. Mlynski, Mass Spectrom. Rev. 2000, 19, 65.
         | CrossRef | 1:CAS:528:DC%2BD3cXjt1Sksb8%3D&md5=c4d9ac62242bcfbd6dcf8a3f6b6a2da8CAS | 10795088PubMed | open url image1

[46]  J. A. Loo, Mass Spectrom. Rev. 1997, 16, 1.
         | CrossRef | 1:CAS:528:DyaK2sXlsVKhtr0%3D&md5=2c5dec2cdb9c7d50a464474b945ed799CAS | 9414489PubMed | open url image1

[47]  R. Franski, B. Gierczyk, T. Kozik, Rapid Commun. Mass Spectrom. 2008, 22, 2747.
         | CrossRef | 1:CAS:528:DC%2BD1cXhtVClur7I&md5=d10f091da163aafa4220e5949aa2b6c1CAS | 18668632PubMed | open url image1

[48]  J. M. Ding, R. J. Anderegg, J. Am. Soc. Mass Spectrom. 1995, 6, 159.
         | CrossRef | 1:CAS:528:DyaK2MXkvVyrsL4%3D&md5=c4301b63048a83b9cf581669b481fa8eCAS | open url image1

[49]  L. Drahos, R. M. A. Heeren, C. Collette, E. De Pauw, K. Vekey, J. Mass Spectrom. 1999, 34, 1373.
         | CrossRef | 1:CAS:528:DC%2BD3cXht1aktw%3D%3D&md5=aa8cceef97a69402c7818b6921a54e07CAS | 10587635PubMed | open url image1

[50]  V. Gabelica, E. De Pauw, J. Mass Spectrom. 2001, 36, 397.
         | CrossRef | 1:CAS:528:DC%2BD3MXjs1Wlur8%3D&md5=f5059e65275e7bf0741c43982b426566CAS | 11333443PubMed | open url image1

[51]  J. B. Chaires, J. L. Mergny, Biochimie 2008, 90, 973.
         | CrossRef | 1:CAS:528:DC%2BD1cXnvVKgtbo%3D&md5=4bd2361a7ead552b755a98814cfcda3cCAS | 18515096PubMed | open url image1

[52]  N. C. Garbett, P. A. Ragazzon, J. B. Chaires, Nat. Protoc. 2007, 2, 3166.
         | CrossRef | 1:CAS:528:DC%2BD2sXhsVejtrbE&md5=9e1d4d0ca72a960a8d0b3656fb6f3427CAS | 18079716PubMed | open url image1

[53]  G. Minotti, P. Menna, E. Salvatorelli, G. Cairo, L. Gianni, Pharmacol. Rev. 2004, 56, 185.
         | CrossRef | 1:CAS:528:DC%2BD2cXltlKgtb0%3D&md5=193caf3620622dfb09b690c802efc313CAS | 15169927PubMed | open url image1

[54]  K. Wiederholt, S. B. Rajur, J. Giuliano, M. J. Odonnell, L. W. McLaughlin, J. Am. Chem. Soc. 1996, 118, 7055.
         | CrossRef | 1:CAS:528:DyaK28XktFyitrc%3D&md5=6a87df1ede9d44fd5328eecd7242cbf0CAS | open url image1

[55]  F. M. Chen, F. Sha, Biochemistry 1998, 37, 11143.
         | CrossRef | 1:CAS:528:DyaK1cXks1ynurk%3D&md5=2cb344851aad42638ab103a3062fff45CAS | 9698360PubMed | open url image1

[56]  P. H. von Hippel, Annu. Rev. Biophys. Biomol. Struct. 2007, 36, 79.
         | CrossRef | 1:CAS:528:DC%2BD2sXnsVahur0%3D&md5=917d8c080592bf1e464b429b99fdaabfCAS | 17477836PubMed | open url image1

[57]  R. Rohs, X. S. Jin, S. M. West, R. Joshi, B. Honig, R. S. Mann, Annu. Rev. Biochem. 2010, 79, 233.
         | CrossRef | 1:CAS:528:DC%2BC3cXpslShtr4%3D&md5=fa0b506fef444036c81f1f7cdf3b6f48CAS | 20334529PubMed | open url image1

[58]  J. L. Beck, T. Urathamakul, S. J. Watt, M. M. Sheil, P. M. Schaeffer, N. E. Dixon, Expert Rev. Proteomics 2006, 3, 197.
         | CrossRef | 1:CAS:528:DC%2BD28XkvVagur8%3D&md5=a95f7879d2541118255871eae4ad69eeCAS | 16608433PubMed | open url image1

[59]  X. H. Cheng, A. C. Harms, P. N. Goudreau, T. C. Terwilliger, R. D. Smith, Proc. Natl. Acad. Sci. USA 1996, 93, 7022.
         | CrossRef | 1:CAS:528:DyaK28Xkt1Whsbo%3D&md5=30722dd44e98caf95b3466bcea9b1e5fCAS | open url image1

[60]  N. Potter, I. Chernushevich, W. Ens, K. G. Standing, L. J. Donald, A. Ayed, H. W. Duckworth, C. H. Arrowsmith, Protein Sci. 1998, 7, 1388.
         | CrossRef | 9655343PubMed | open url image1

[61]  A. Kapur, J. L. Beck, S. E. Brown, N. E. Dixon, M. M. Sheil, Protein Sci. 2002, 11, 147.
         | CrossRef | 1:CAS:528:DC%2BD38Xltlyj&md5=d20cae9dfc737afd37949ed69219aa35CAS | 11742131PubMed | open url image1

[62]  K. Kamada, T. Horiuchi, K. Ohsumi, N. Shimamoto, K. Morikawa, Nature 1996, 383, 598.
         | CrossRef | 1:CAS:528:DyaK28XmtlSqsLo%3D&md5=76d2b7f1771440a7755a4af631d576baCAS | 8857533PubMed | open url image1

[63]  C. Atmanene, D. Chaix, Y. Bessin, N. Declerck, A. van Dorsselaer, S. Sanglier-Cianferani, Anal. Chem. 2010, 82, 3597.
         | CrossRef | 1:CAS:528:DC%2BC3cXktFOisLo%3D&md5=0cd1752eea0975d07f14b921f48acb06CAS | 20361740PubMed | open url image1

[64]  A. B. Kanu, P. Dwivedi, M. Tam, L. Matz, H. H. Hill, J. Mass Spectrom. 2008, 43, 1.
         | CrossRef | 1:CAS:528:DC%2BD1cXisFKntbk%3D&md5=d0731448f7ad361e013eb2f7ac53d24aCAS | 18200615PubMed | open url image1

[65]  E. S. Baker, S. L. Bernstein, V. Gabelica, E. De Pauw, M. T. Bowers, Int. J. Mass Spectrom. 2006, 253, 225.
         | CrossRef | 1:CAS:528:DC%2BD28Xmt1amtr8%3D&md5=b72504522530df6f8c8c2f740c744cb1CAS | open url image1

[66]  F. Rosu, V. Gabelica, H. Poncelet, E. De Pauw, Nucleic Acids Res. 2010, 38, 5217.
         | CrossRef | 1:CAS:528:DC%2BC3cXhtV2qsLjF&md5=a0c4fce150c9ef17bb6f3acbe9e892baCAS | 20400500PubMed | open url image1

[67]  K. C. Porter, J. L. Beck, Int. J. Mass Spectrom. 2011,
         | CrossRef | open url image1

[68]  J. L. Mergny, A. De Cian, A. Ghelab, B. Sacca, L. Lacroix, Nucleic Acids Res. 2005, 33, 81.
         | CrossRef | 1:CAS:528:DC%2BD2MXmsVyiug%3D%3D&md5=ee3707278c0cf310d920b63eb6596e5eCAS | 15642696PubMed | open url image1

[69]  J. Zhou, G. Yuan, J. J. Liu, C. G. Zhan, Chemistry 2007, 13, 945.
         | CrossRef | 1:CAS:528:DC%2BD2sXhtVGms7g%3D&md5=c1091fea282c1aff2613c164a4bf42faCAS | 17036297PubMed | open url image1

[70]  M. Rueda, S. G. Kalko, F. J. Luque, M. Orozco, J. Am. Chem. Soc. 2003, 125, 8007.
         | CrossRef | 1:CAS:528:DC%2BD3sXltV2jsbs%3D&md5=096fcd290531a872c71907c5a72488f4CAS | 12823023PubMed | open url image1

[71]  M. Rueda, F. J. Luque, M. Orozco, J. Am. Chem. Soc. 2006, 128, 3608.
         | CrossRef | 1:CAS:528:DC%2BD28XhvVequ7w%3D&md5=149c562ee3ad46bb9096e35144762bdcCAS | 16536534PubMed | open url image1

[72]  J. Gidden, A. Ferzoco, E. S. Baker, M. T. Bowers, J. Am. Chem. Soc. 2004, 126, 15132.
         | CrossRef | 1:CAS:528:DC%2BD2cXptVartr4%3D&md5=6042d0b1f7e770b4fdd334ce2c2c8886CAS | 15548010PubMed | open url image1

[73]  E. S. Baker, M. T. Bowers, J. Am. Soc. Mass Spectrom. 2007, 18, 1188.
         | CrossRef | 1:CAS:528:DC%2BD2sXntF2ls74%3D&md5=4707eb3e29c4d00c9f1d40df09e33f13CAS | 17434745PubMed | open url image1

[74]  E. S. Baker, N. F. Dupuis, M. T. Bowers, J. Phys. Chem. B 2009, 113, 1722.
         | CrossRef | 1:CAS:528:DC%2BD1MXns1OlsA%3D%3D&md5=1db2c14df5f1552ed5b48deef20612ecCAS | 19193169PubMed | open url image1

[75]  T. Wyttenbach, P. R. Kemper, M. T. Bowers, Int. J. Mass Spectrom. 2001, 212, 13.
         | CrossRef | 1:CAS:528:DC%2BD38XisVOl&md5=763e42ec8df589bb67dfe88beac8d036CAS | open url image1

[76]  S. D. Pringle, K. Giles, J. L. Wildgoose, J. P. Williams, S. E. Slade, K. Thalassinos, R. H. Bateman, M. T. Bowers, J. H. Scrivens, Int. J. Mass Spectrom. 2007, 261, 1.
         | CrossRef | 1:CAS:528:DC%2BD2sXhsFCru7c%3D&md5=d8663101f13c15d030209240905b544fCAS | open url image1

[77]  D. P. Smith, T. W. Knapman, I. Campuzano, R. W. Malham, J. T. Berryman, S. E. Radford, A. E. Ashcroft, Eur. J. Mass Spectrom. 2009, 15, 113.
         | CrossRef | 1:CAS:528:DC%2BD1MXksVKlsbg%3D&md5=34053dc3a63c428b7579a99c8f16dffcCAS | open url image1

[78]  S. B. Cohen, M. E. Graham, G. O. Lovrecz, N. Bache, P. J. Robinson, R. R. Reddel, Science 2007, 315, 1850.
         | CrossRef | 1:CAS:528:DC%2BD2sXjsFSitr0%3D&md5=553912f758dca9dadf63a491369961d2CAS | 17395830PubMed | open url image1

[79]  M. J. Giraud-Panis, S. Pisano, A. Poulet, M. H. Le Du, E. Gilson, FEBS Lett. 2010, 584, 3785.
         | CrossRef | 1:CAS:528:DC%2BC3cXhtVKgtr3P&md5=ef5df430b48324c869457b059c229c09CAS | 20696167PubMed | open url image1

[80]  S. Y. Zhou, D. Liu, Crit. Rev. Eukaryot. Gene Expr. 2006, 16, 103.
         | 1:CAS:528:DC%2BD28Xls1Cqt74%3D&md5=3e3b415f95647f359b7047297ec76d6bCAS | 16749892PubMed | open url image1

[81]  L. E. Donate, M. A. Blasco, Phil. Trans. Royal Soc. B Biol. Sci. 2011, 366, 76.
         | CrossRef | 1:CAS:528:DC%2BC3MXktlensLc%3D&md5=73b17977970b2f59da6931c8fa0cd25eCAS | open url image1

[82]  C. Lobetti-Bodoni, E. Bernocco, E. Genuardi, M. Boccadoro, M. Ladetto, Hematol. Oncol. 2010, 28, 157.
         | CrossRef | 1:CAS:528:DC%2BC3MXhtlagt70%3D&md5=7c19fea07ace64d4f2535fb962decc82CAS | 20213664PubMed | open url image1

[83]  S. A. Savage, A. A. Bertuch, Gend. Med. 2010, 12, 753.
         | CrossRef | open url image1

[84]  T. Minamino, Circ. J. 2010, 74, 2527.
         | CrossRef | 1:CAS:528:DC%2BC3MXpvVSq&md5=cd5f634a0a33e776bef6513b988f0c11CAS | 21084758PubMed | open url image1

[85]  A. De Cian, L. Lacroix, C. Douarre, N. Temime-Smaali, C. Trentesaux, J. F. Riou, J. L. Mergny, Biochimie 2008, 90, 131.
         | CrossRef | 1:CAS:528:DC%2BD2sXhsVSqu7rE&md5=342f019ac6dd1e513324c8635c80264bCAS | 17822826PubMed | open url image1

[86]  M. Franceschin, Eur. J. Org. Chem. 2009, 2225.
         | CrossRef | 1:CAS:528:DC%2BD1MXmt1agurY%3D&md5=c6111d55f762de5fa2b22997fc182658CAS | open url image1

[87]  D. Monchaud, M. P. Teulade-Fichou, Org. Biomol. Chem. 2008, 6, 627.
         | CrossRef | 1:CAS:528:DC%2BD1cXhs1yksLs%3D&md5=6d9b5bf8ac375377278f91041280fc4dCAS | 18264563PubMed | open url image1

[88]  J. W. Shay, W. E. Wright, Nat. Rev. Drug Discov. 2006, 5, 577.
         | CrossRef | 1:CAS:528:DC%2BD28XmsVagsrg%3D&md5=0b38059d733aa2e0050619fe302e6f2fCAS | 16773071PubMed | open url image1

[89]  K. Paeschke, T. Simonsson, J. Postberg, D. Rhodes, H. J. Lipps, Nat. Struct. Mol. Biol. 2005, 12, 847.
         | CrossRef | 1:CAS:528:DC%2BD2MXhtVKnsrvF&md5=861a215cb3420277a32b3edbd4e208edCAS | 16142245PubMed | open url image1

[90]  A. Piazza, J. B. Boule, J. Lopes, K. Mingo, E. Largy, M. P. Teulade-Fichou, A. Nicolas, Nucleic Acids Res. 2010, 38, 4337.
         | CrossRef | 1:CAS:528:DC%2BC3cXpsFyisbo%3D&md5=b90d922136e33fc9c323e8b981b34100CAS | 20223771PubMed | open url image1

[91]  C. Schaffitzel, I. Berger, J. Postberg, J. Hanes, H. J. Lipps, A. Pluckthun, Proc. Natl. Acad. Sci. USA 2001, 98, 8572.
         | CrossRef | 1:CAS:528:DC%2BD3MXls1Witr4%3D&md5=ba38244cb697cf0be915a1b6ebe2d8deCAS | open url image1

[92]  S. D. Creacy, E. D. Routh, F. Iwamoto, Y. Nagamine, S. A. Akman, J. P. Vaughn, J. Biol. Chem. 2008, 283, 34626.
         | CrossRef | 1:CAS:528:DC%2BD1cXhsVGqtrnN&md5=345db4c2fa6124ea85d4c695ac5f9faaCAS | 18842585PubMed | open url image1

[93]  A. De Cian, G. Cristofari, P. Reichenbach, E. De Lemos, D. Monchaud, M. P. Teulade-Fichou, K. Shin-Ya, L. Lacroix, J. Lingner, J. L. Mergny, Proc. Natl. Acad. Sci. USA 2007, 104, 17347.
         | CrossRef | 1:CAS:528:DC%2BD2sXht1ymtrjI&md5=67e000cbd48ba3377f2502cbd443475cCAS | open url image1

[94]  L. Oganesian, M. E. Graham, P. J. Robinson, T. M. Bryan, Biochemistry 2007, 46, 11279.
         | CrossRef | 1:CAS:528:DC%2BD2sXhtVCntbrJ&md5=ac56220061b8cdaaad7f7886143f27ecCAS | 17877374PubMed | open url image1

[95]  J. Talib, C. Green, K. J. Davis, T. Urathamakul, J. L. Beck, J. R. Aldrich-Wright, S. F. Ralph, Dalton Trans. 2008, 1018.
         | CrossRef | 1:CAS:528:DC%2BD1cXhvF2ls70%3D&md5=dc695abca7aca3b799b85c2663cc7c0bCAS | 18274682PubMed | open url image1

[96]  G. R. Clark, P. D. Pytel, C. J. Squire, S. Neidle, J. Am. Chem. Soc. 2003, 125, 4066.
         | CrossRef | 1:CAS:528:DC%2BD3sXitVOls7w%3D&md5=049f40c8b8524bbc572d86f9c2b09165CAS | 12670225PubMed | open url image1

[97]  J. M. Daniel, S. D. Friess, S. Rajagopalan, S. Wendt, R. Zenobi, Int. J. Mass Spectrom. 2002, 216, 1.
         | CrossRef | 1:CAS:528:DC%2BD38Xis1enur4%3D&md5=1fb7a391e12507c6830b2e0bb43cc958CAS | open url image1

[98]  W. Buchmann, A. Boutorine, L. Halby, J. Tortajada, E. De Pauw, J. Mass Spectrom. 2009, 44, 1171.
         | CrossRef | 1:CAS:528:DC%2BD1MXhtVCgu7nO&md5=fb050700b5b5985354f25db7fc1dc9c2CAS | 19408249PubMed | open url image1

[99]  R. Gupta, S. M. Hamdan, N. E. Dixon, M. M. Sheil, J. L. Beck, Protein Sci. 2004, 13, 2878.
         | CrossRef | 1:CAS:528:DC%2BD2cXpsVWhsbs%3D&md5=d09b33ae4c981e0d0b760d2ab8dd38cbCAS | 15459336PubMed | open url image1

[100]  V. Gabelica, F. Rosu, E. De Pauw, Anal. Chem. 2009, 81, 6708.
         | CrossRef | 1:CAS:528:DC%2BD1MXosVWntLw%3D&md5=41ccc4cdc90c9db82c34e806b2d712c2CAS | 19601639PubMed | open url image1

[101]  C. L. Mazzitelli, J. S. Brodbelt, J. T. Kern, M. Rodriguez, S. M. Kerwin, J. Am. Soc. Mass Spectrom. 2006, 17, 593.
         | CrossRef | 1:CAS:528:DC%2BD28XivVOitLg%3D&md5=704e659d26fb3909e8da4c12a1d5df04CAS | 16503153PubMed | open url image1

[102]  F. Rosu, V. Gabelica, K. Shin-ya, E. De Pauw, Chem. Commun. 2003, 2702.
         | CrossRef | 1:CAS:528:DC%2BD3sXot1ersro%3D&md5=670774e719e1dac357f07cca9b861496CAS | open url image1

[103]  V. Gabelica, E. S. Baker, M. P. Teulade-Fichou, E. De Pauw, M. T. Bowers, J. Am. Chem. Soc. 2007, 129, 895.
         | CrossRef | 1:CAS:528:DC%2BD2sXlt1ChsA%3D%3D&md5=297680934ddafcfd04f0db400d2b19deCAS | 17243826PubMed | open url image1

[104]  W. H. Chen, C. L. Chan, Z. W. Cai, G. A. Luo, Z. H. Jiang, Bioorg. Med. Chem. Lett. 2004, 14, 4955.
         | CrossRef | 1:CAS:528:DC%2BD2cXnt12rt7g%3D&md5=ccdc447954ef30f9ba191a9ac8c7bea3CAS | 15341959PubMed | open url image1

[105]  Z. F. Wang, X. H. Guo, Z. Q. Liu, M. R. Cui, F. R. Song, S. Y. Liu, J. Mass Spectrom. 2008, 43, 327.
         | CrossRef | 1:CAS:528:DC%2BD1cXjvVahs7o%3D&md5=4c3b7b4d9bf1642a59716a0ae14c9378CAS | 17968851PubMed | open url image1

[106]  I. Naasani, H. Seimiya, T. Yamori, T. Tsuruo, Cancer Res. 1999, 59, 4004.
         | 1:CAS:528:DyaK1MXlsVOltb4%3D&md5=9392521a184c582dc15591f96e3dfc80CAS | 10463599PubMed | open url image1

[107]  K. C. Gornall, S. Samosorn, B. Tanwirat, A. Suksamrarn, J. B. Bremner, M. J. Kelso, J. L. Beck, Chem. Commun. 2010, 46, 6602.
         | CrossRef | 1:CAS:528:DC%2BC3cXhtVKltb7F&md5=c8d4816ee972e7086b9adb2a90f8a82cCAS | open url image1

[108]  C. M. Lombardo, I. S. Martinez, S. Haider, V. Gabelica, E. De Pauw, J. E. Moses, S. Neidle, Chem. Commun. 2010, 46, 9116.
         | CrossRef | 1:CAS:528:DC%2BC3cXhsVynurjL&md5=015d6fba80468291340220f1b7020adbCAS | open url image1



Rent Article Export Citation Cited By (4)