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Complementary Base-Pair-Facilitated Electron Tunneling for Electrically Pinpointing Complementary Nucleobases

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Complementary Base-Pair-Facilitated Electron Tunneling for Electrically Pinpointing Complementary Nucleobases Complementary base-pair-facilitated electron tunneling for electrically pinpointing complementary nucleobases Takahito Ohshiro and Yoshio Umezawa* Department of Chemistry, School of Science, University of Tokyo, and Japan Science and Technology Agency, Hongo, Bunkyo-Ku, Tokyo 133-0033, Japan Edited by Jacqueline K. Barton, California Institute of Technology, Pasadena, CA, and approved November 17, 2005 (received for review July 19, 2005) Molecular tips in scanning tunneling microscopy can directly detect Results and Discussion intermolecular electron tunneling between sample and tip mole- The nucleobase molecular tips were prepared by chemical cules and reveal the tunneling facilitation through chemical inter- modification of underlying metal tips with thiol derivatives of actions that provide overlap of respective electronic wave func- adenine, guanine, cytosine, and uracil (see Materials and Meth- tions, that is, hydrogen-bond, metal-coordination-bond, and ods) (for their chemical structures, see Fig. 1b; for their prepa- charge-transfer interactions. Nucleobase molecular tips were pre- rations, see Supporting Text, which is published as supporting pared by chemical modification of underlying metal tips with thiol information on the PNAS web site), and the outmost single derivatives of adenine, guanine, cytosine, and uracil and the nucleobase adsorbate probes intermolecular electron tunneling outmost single nucleobase adsorbate probes intermolecular elec- to or from a sample nucleobase molecule. Importantly, the tron tunneling to or from a sample nucleobase molecule. We found tunneling current increases when sample and tip molecules form that the electron tunneling between a sample nucleobase and its a chemical interaction that provides overlap of electronic wave complementary nucleobase molecular tip was much facilitated functions between them. The current increase is ascribed to the compared with its noncomplementary counterpart. The comple- facilitated electron tunneling through the overlapped electronic mentary nucleobase tip was thereby capable of electrically pin- wave functions. Electron tunneling observed here occurs without pointing each nucleobase. Chemically selective imaging using mo- any net chemical oxidation͞reduction of the involved bases. Fig. lecular tips may be coined ‘‘intermolecular tunneling microscopy’’ 2 a–c shows typical STM images of guanine SAMs observed with as its principle goes and is of general significance for novel complementary cytosine tips, noncomplementary adenine, and molecular imaging of chemical identities at the membrane and unmodified tips, respectively (see Materials and Methods). Cross- solid surfaces. sectional profiles of the images are shown in Fig. 2d, which represents the extent of electron tunneling between the tip and DNA ͉ nanobioscience ͉ scanning tunneling microscopy nucleobase. The complementary cytosine tip exhibited the most facilitated electron tunneling and therefore the brightest gua- lectron transfer through DNA double strands has attracted nine images among the three tips. Similarly, for adenine, cyto- Emuch interest (1–4) since Barton and colleagues (5) reported sine, and uracil, their complementary nucleobase tips gave the it in the 1990s. The processes of DNA-mediated electron transfer brightest images of their counterparts, the results of which are have been explored by spectroscopic methods for detecting shown in Fig. 2e together with those using irrelevant tips for photo-induced electron transfer through the DNA strands that validation. We have differentiated the complementary nucleo- are labeled with redox-active probes through intercalation bases from the noncomplementary ones by the tip heights for the and͞or covalent linkages (6, 7). These experiments have revealed sample nucleobases in absolute terms. The height is a quanti- that a DNA strand is capable of mediating electron transfer tative measure of the current, because the tunneling current I is through the DNA base stacking in the strand (intrastrand related to the tip height h by the relation as I ϰ exp(Ϫ2kh), where pathway) (8–13). On the other hand, the contribution of the k ϭបϪ1(2m␸)1/2 and ␸ is the work function of the sample (24). electron transfer through the complementary base pair (inter- The tip height h is usually recorded rather than the current I for strand pathway) to the overall electron transfer in DNA has been the instrumental convenience, keeping the current I constant. investigated by several researchers (14, 15). Here, we report on For example, with the cytosine tips, the heights of the tip were electron tunneling through the complementary base pair with found to be 197 Ϯ 23 pm for the complementary guanines (Fig. nucleobase molecular tips for selectively discriminating each of 2e, black columns) and 102 Ϯ 5 pm, 98 Ϯ 9 pm, and 99 Ϯ 7pm the complementary nucleobases from the other nucleobases for the noncomplementary adenines, uracils, and cytosines, (Fig. 1a). The molecular tips are prepared by chemical modifi- respectively (Fig. 2e, yellow columns). These heights quantita- cation of underlying metal tips typically with self-assembled tively represent the tunneling currents flowing within the base monolayers (SAMs) of thiols and the outermost single adsorbate pairs. On the contrary, with unmodified tips, or with gold tips probes electron tunneling to or from a sample molecule. Im- modified with 2-mercaptobenzimidazole (MB) and thiophenol portantly, the tunneling current increases when sample and tip (TP) (chemical structures, Fig. 1b), which have a pyrimidine- and molecules form chemical interactions that provide overlap of pyridine-like structure, respectively, but no particular functional their electron wave functions, that is, hydrogen-bond interac- groups for hydrogen-bond formation with nucleobases, selective tions (16–22), metal-coordination-bond interactions (20), and facilitation of electron tunneling was not detected for any charge-transfer interactions (23). We have thus far demonstrated nucleobases (Fig. 2e, yellow columns), as shown in an STM image that this phenomenon can be used for selective observation of chemical species to overcome poor chemical selectivity in con- ventional scanning tunneling microscopy (STM). We herein Conflict of interest statement: No conflicts declared. found that the electron tunneling between a sample nucleobase This paper was submitted directly (Track II) to the PNAS office. and its complementary nucleobase tip was much facilitated Abbreviations: STM, scanning tunneling microscopy; SAM, self-assembled monolayer; PNA, compared with its noncomplementary counterpart. The com- peptide nucleic acid; MB, 2-mercaptobenzimidazole; TP, thiophenol. plementary nucleobase tip was thereby capable of electrically *To whom correspondence should be addressed. E-mail: [email protected]. pinpointing each nucleobase. © 2005 by The National Academy of Sciences of the USA 10–14 ͉ PNAS ͉ January 3, 2006 ͉ vol. 103 ͉ no. 1 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0506130103 Downloaded by guest on September 28, 2021 not show selective large facilitation of electron tunneling (Fig. 2e, yellow column), confirming that the observed difference is caused solely by the hydrogen bonds of complementary base pairs between bases on a tip and substrate. We have earlier reported on the use of hydrogen bond-based molecular tips for selective STM imaging of hydrogen-bond acceptor or donor molecules and functional groups and on the use of other chemical interaction-based molecular tips, metal coordination bond-based molecular tips for selective STM im- aging of metal species in metalloporphyrins (20), and charge- transfer interaction-based molecular tips for that of electron-rich porphyrin rings (23). Upon tailor-making the molecular tips with differing extents of hydrogen-bond acidity or basicity, we have succeeded in selectively pinpointing particular functional groups in sample molecules, including hydroxy, carboxy, carboxylate, ether oxygens and their orientations, and a free-base porphyrin center (16–22). We herein added another example of hydrogen- bond-facilitated electron tunneling, i.e., complementary base- pair-facilitated electron tunneling (Fig. 1a). For example, before the cytosine tip was placed on a guanine base, the guanine base did not possess any greater electron density compared with other bases, but instead a greater electron density was induced along the hydrogen-bonding plane upon placing the cytosine tip on the guanine base. This induced increase in electron density trans- lates into a greater electronic coupling between the two bases and thus an increase in the tunneling current between them. As Fig. 1. A nucleobase tip pinpoints its complementary nucleobase based on a result, nucleobase tips gave large extents of electron tunneling CHEMISTRY base-pair-facilitated electron tunneling. (a) Formation of the complementary currents only for its complementary bases. The direction of base pairs between the nucleobase tip and the sample nucleobases leads to electron flow between bases on a tip and a substrate did not greatly facilitate electron tunneling in STM. Nucleobase tips can thus pinpoint affect the extent of electron tunneling through the same com- the corresponding complementary nucleobases. (b) The chemical structures bination of the material (Fig. 2e): for instance, cytosine and for thiol derivatives of adenine (1), guanine (2), cytosine (3), uracil (4), MB (5), guanine tips gave the same extent of electron tunneling to their and TP (6) are
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