Detection and Sequence Identification of Dinucleotides Produced from N-Phosphoryl Alanine and Four Nucleosides by HPLC-ESI-MS/MS
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1 Chinese Journal of Chemistry, 2008, 26, Full Paper Detection and Sequence Identification of Dinucleotides Produced from N-Phosphoryl Alanine and Four Nucleosides by HPLC-ESI-MS/MS GUO, Yan-Chun a ( 郭艳春 ) CAO, Shu-Xia*,a ( 曹书霞 ) LIAO, Xin-Cheng a ( 廖新成 ) ZHAO, Yu-Fen*,a,b ( 赵玉芬 ) a Key Laboratory of Chemical Biology and Organic Chemistry of Henan Province, Department of Chemistry, Zhengzhou University, Zhengzhou , China b Key Laboratory for Bioorganic Phosphorus Chemistry of Ministry of Education, Department of Chemistry, School of Life Sciences and Engineering, Tsinghua University, Beijing , China The products of the model reaction between N-(O,O-diisopropyl phosphoryl) alanine (DIPP-Ala) and four nucleosides (adenosine, uridine, cytidine and guanosine) were studied by HPLC-ESI-MS/MS. The results showed that different mononucleotides and dinucleotides were produced. The sequences of dinucleotides formed from the DIPP-Ala and four nucleosides were identified. The results revealed that the c-ions from backbone fragmentation of the dinucleotides could be considered as the sequence-diagnostic ions. It was firstly testified that the diagnostic c-ions in positive and negative modes could be applied to identify the sequence of dinucleotide products formed in the reaction system. Keywords N-(O,O-diisopropyl phosphoryl) alanine (DIPP-Ala), HPLC-ESI-MS/MS, sequence of dinucleotide, fragmentation mechanism Introduction Which came first, nucleic acid or protein? This has long been a major question in studies on origin of life. 1,2 Former research has found that N-(O,O-diisopropyl phosphoryl) amino acids (DIPP-AA) can not only selfassemble into oligopeptides but also act as the phosphoryl donor to phosphorylate nucleosides, nucleotides or oligonucleotides. Therefore, the hypothesis was proposed that N-phosphoryl amino acids might be regarded as the common original seed for nucleic acids and prebiotic proteins. 3 In the previous work, it was found that nucleotides and oligonucleotides could simultaneously be formed by the reaction of DIPP-Thr and uridine. 4 The reactions between nucleosides and different DIPP-AA in aqueous solution were also investigated, and the results showed that DIPP-Asp reacted with adenosine and guanosine at a much higher rate than other kinds of N-phosphoryl amino acids, while phosphorylation of cytidine and uridine was relatively easy by using DIPP-Thr. 5 In addition, the reactions between six different DIPP-AA and adenosine in aqueous solution have been studied in detail, and the result indicated that the different DIPP-AA produced different nucleotides at various concentrations. 6 Furthermore, using poly(beta-(n7-adeninyl)ethyl methacrylate) as a template, an increased yield of the oligouridylates formed with N-(O,O-diisopropyl phosphoryl) alanine (DIPP- Ala) was confirmed. 7 As a consequence, it was not hard to deduce that there was some selectivity between different amino acids and nucleosides. However, the origin of life is so complicated that it seems to be particularly important to study the reaction between special DIPP- AA and nucleoside mixtures under various conditions. From the type of products observed, the selectivity and competition of the reactants can be deduced and the role of phosphorus in the reaction process can be further investigated. The results will also undoubtedly provide some additional experimental evidence for the study of origin of life. On the other hand, how to identify the sequence of oligonucleotide in this reaction system has not been investigated before. It is well known that a tandem mass spectrometry technique is one of the most attractive techniques for providing the high degree of structural information. In terms of identifying sequence of oligonucleotides with a mass spectrometry technique, the basis was set up in the early 1990s by McLuckey and co-workers 8,9 who presented a general nomenclature. The four possible cleavages along the phosphodiester chain were denoted by the lower case letters a, b, c and d for fragments containing the 5'-terminus and w, x, y * csx@zzu.edu.cn; Tel.: ; Fax: Received October 24, 2007; revised December 19, 2007; accepted March 3, Project supported by the National Natural Science Foundation of China (No ) and the Education Department of Henan Province (No ).
2 1286 Chin. J. Chem., 2008, Vol. 26, No. 7 GUO et al. and z for fragments containing the 3'-terminus. Then the sequence of oligonucleotides might be identified by the two series of ions. Although characterization of oligonucleotides by mass spectrometry has been in the focus of researchers for about three decades, it was found that tandem mass spectra of oligonucleotides was far more complex than those of proteins. So far as we know, oligonucleotides still cannot be sequenced by mass spectrometry as easily and efficiently as proteins up to now. The recent research has testified that, in a negative mode, dissociation of oligodeoxyribonucleotides (DNA) is initiated by loss of the nucleobase, followed by cleavage of the 3'-C O bond and formation of a- and w-ions. 13 For oligoribonucleotides (RNA), since the presence of the 2'-hydroxyl substituent, its backbone dissociation is initiated by the formation of an intramolecular cyclic transition state with the 2'-hydroxyl proton bridged to the 5'-phosphate oxygen. Then the 5'-P O bond dissociates to result in the formation of c- and y-ions However, little is known about the dissociation of oligonucleotides in a positive mode of electrospray ionization mass spectrometry (ESI-MS), especially about that of oligoribonucleotides. Furthermore, the fragmentation mechanism proposed for oligonucleotides has not been extensively applied to identify the sequence of reaction products. Therefore, the products generated by the reaction of DIPP-Ala and four nucleosides (adenosine, uridine, cytidine and guanosine) were studied in detail and the sequences of dinucleotides produced were identified by HPLC-ESI- MS/MS in positive and negative modes, respectively. Since the peptide formation from DIPP-AA has been much studied by different methods, the paper is focused on the formation and sequence confirmation of the oligonucleotide in the reaction system. Experimental DIPP-Ala was synthesized according to a literature method. 20 Adenosine, guanosine, cytidine, uridine and two dinucleoside monophosphates CpU and UpG were purchased from Shanghai Sangon Co. (AMRESCO subpackage). Methanol (HPLC grade) was purchased from Tianjin Shield Co. (Tianjin, China). Deionized water was produced by a Milli-Q water purifying system purchased from Millipore (MA, USA). Other common chemicals used were of the highest purity commercially available. Formic acid (HPLC grade, Tianjing BoDi Co.) solution (0.215%) was prepared by dissolving g of formic acid in 1.0 L of deionized water. General procedure DIPP-Ala (0.8 mmol) and the four nucleosides, adenosine, guanosine, cytidine and uridine (each 0.2 mmol) were all dissolved in 1.3 ml of anhydrous pyridine. Imidazole (0.8 mmol) was added to the mixture, which was stirred at a constant temperature (37 ) for two weeks. Solvent was removed by reduced pressure distillation and the yellow thick residue was dissolved in 2.5 ml of deionized water. Then by filtration clarifying filtrate was acquired and extracted with ethyl acetate (300 µl 3). Water phase was diluted to 25 times and used for analysis of HPLC-ESI-MS. The HPLC system used was an Agilent 1100 series (CA, USA) high-performance liquid chromatograph, consisting of a degasser, a binary pump, a manual injector and a UV detector. Chromatographic separations were performed with a Zorbax C18 column (150 mm 2.1 mm i.d., particle size 5 µm) at room temperature. Analyses were performed by UV absorbance at a wavelength of 260 nm and a flow-rate of 0.4 ml min -1. The injection volume was 20 µl. Solvent A was deionized water containing 0.215% HCOOH, and solvent B was methanol. Gradient runs were programmed as follows: linear gradient increase from 2% (V/V) solvent B at 0 min, 2% (V/V) solvent B at 2.5 min, and 7% (V/V) solvent B at 16 min to 7% (V/V) solvent B at 30 min. The effluent from the HPLC system was connected to a mass spectrometer through a split valve (split ratio= 9 1). A Bruker Esquire 3000 (Bruker Dalton, Germany) ion trap mass spectrometer interfaced to an electrospray ionization source was used for detection and mass analysis. Ionization of analytes was carried out using the following setting of the ESI: nebulizer gas flow 7 psi, dry gas 4 L min -1, dry temperature 300, and capillary voltage 4 kv. Calibration of m/z was performed using a standard ESI-tuning-mixer. Scan range was m/z and scan resolution was normal (13000 m/z s -1 ). MS n spectra were obtained by CID experiments with helium after isolation of the appropriate precursor ions. For HPLC-MS analysis, ionization of analytes was carried out using the following settings of the ESI: nebulizer gas flow 30 psi, dry gas 12 L min -1, dry temperature 350, and capillary voltage 4 kv. Results and discussion DIPP-Ala and the four nucleosides, adenosine, guanosine, cytidine and uridine, were mixed and stirred in anhydrous pyridine at 37 for two weeks, and then the reaction products were subjected to reversed phase HPLC separation. In terms of analyzing mononucleotides and dinucleotides by HPLC, an ODS [C(18)] column and acetonitrile with phosphate buffer have been most widely used. 21,22 The ph value of the mobile phase was varied from 3 to 7. Although literature demonstrated good resolution and high sensitivity in the conditions, phosphate buffer would suppress mass signal and decrease mass sensitivity in the HPLC-ESI-MS analysis. Consequently, the elution of methanol-water system adjusted with formic acid (0.215%) was selected to analyze the reaction products with better resolution and higher mass sensitivity. Typical HPLC spectra of DIPP-Ala reaction products are shown in Figure 1. It could be seen that although there were only a few dinucleotides produced, the analysis method by HPLC-ESI-
3 N-(O,O-Diisopropyl phosphoryl) alanine(dipp-ala) Chin. J. Chem., 2008 Vol. 26 No MS was sensitive enough to detect the products. Figure 1 HPLC spectra of reaction products of DIPP-Ala with four nucleosides (C, U, A, G are corresponding to cytidine, uridine, adenosine and guanosine, separately). Furthermore, altering modes between positive and negative ones was selected to detect the reaction products for acquiring more information. Our target products, the mononucleotides and dinucleotides, include a phosphate group which is more sensitive in the negative mode, so the extracted ion chromatogram (EIC) of negative ion was more suitable for detection and identification of the reaction products. By HPLC-ESI-MS, not only monophosphoryl nucleotide (XMP), 2',3'-cyclomonophosphoryl nucleotide (XMP-cyclo), phosphoryl nucleotide isopropyl ester (XMP(i-PrO)) and diphosphoryl nucleotide isopropyl ester (XDP(i-PrO)), but also dinucleotides (XpY, X and Y represent the different nucleoside) were observed. The products formed in the reaction of DIPP-Ala with the four nucleosides are listed in Table 1. It is well known that HPLC-ESI-MS/MS could be used to identify the structures of reaction products even in the absence of standard compounds with better sensitivity. The structures of XMP, XMPcyclo, XMP(i-PrO) and XDP(i-PrO) were easily identified by their MS/MS spectra, but it was not easy to de- Table 1 Identification of reaction products by HPLC-ESI-MS in a negative mode Product Ion Retention time a /min AMP ; 9.1; ',3'-cyclo-AMP ',3'-cyclo-CMP ',3'-cyclo-UMP AMP(i-PrO) UMP(i-PrO) ADP(i-PrO) CDP(i-PrO) UpC UpU UpA a Retention time in total ion current of ESI-MS is delayed about min compared to that in HPLC spectrum. XMP(i-PrO): monophosphoryl nucleotide isopropyl ester; XDP(i-PrO): diphosphoryl nucleotide isopropyl ester. XpY: dinucleotides (X and Y represent the different nucleosides). duce the sequence of the dinucleotides produced in the reaction system. For example, in Figure 2 the peak eluted at 25.2 min, whose mass peak was at m/z 549.4, could be presumed to be protonated ion of UpU by main peaks in its tandem mass spectra. However, the peaks eluted at 23.4 and 24.7 min, whose mass peaks were at m/z and 572.5, could only be known as the constituent nucleosides, but could not be confirmed as either dinulceotide being UpC or CpU, UpA or ApU, respectively. In addition, the sodium adducts of the dinucleotide products were also observed in Figure 2. For instance, the peak at m/z corresponded to the sodium adduct of dinucleotide UpC or CpU. However, the sequence of the dinucleotide could not be identified by their molecular weight acquired by HPLC-ESI-MS and their main peaks in the tandem mass spectra. Figure 2 HPLC-MS of reaction products of DIPP-Ala with four nucleosides. Since the sequence of dinucleotides XpY or YpX, formed by DIPP-Ala and the four nucleosides, could not be identified only by HPLC-ESI-MS, their fragmentation patterns were investigated to identify it. The characteristic fragmentation patterns of protonated dinucleotide and deprotonated dinucleotide were compared. It was firstly found that not only deprotonated ions but also protonated ions could show characteristic information. For example, MS 2 diagrams of protonated ions at m/z 550 and 574 are shown in Figure 3. It was apparent Figure 3 The positive MS 2 diagrams of UpA and UpC.
4 1288 Chin. J. Chem., 2008, Vol. 26, No. 7 GUO et al. that there were some common fragmentation ions, such as those at m/z 439, 421 and 307. The observations suggested that the two dinucleotides might bear one common nucleoside. As shown in Scheme 1, just like the patterns in a negative mode, backbone dissociation formed an intramolecular cyclic ion with the 2'-hydroxyl proton bridged to the 5'-phosphate oxygen firstly. Then with the abstraction of 2'-hydroxyl proton, the 5'-P O bond dissociated to produce the c-ions. Simultaneously, the y-fragment was released as a neutral molecule, which could not give signals in the mass spectra. In succession bond rearrangement resulted in the formation of a 3'-metaphosphoric-acid ester group, which stabilized the c-fragment ions. Therefore, XpY could differ significantly from YpX by the formation of the diagnostic c-fragment ion, which includes X nucleoside, whereas c-fragment ion with Y nucleoside was produced from a YpX molecular ion. Consequently, for the existence of ion at m/z 307 in Figures 3a and 3b, the sequence of dinucleotides should be identified to be UpA and UpC, rather than ApU and CpU by HPLC-ESI-MS/MS. The potential mechanism for their dissociation is depicted in Scheme 2. It can be seen that only from UpA and UpC, the fragmentation ion at m/z 307 can be generated. However, if those were from ApU and CpU, the corresponding c-ions would be at m/z 330 and 306. Therefore, the sequence of dinucleotides could be identified by the diagnostic c-fragment ion as shown in Scheme 1. Furthermore, the common fragmentation ions, such as those at m/z 439 and 421 in Figure 3 (a and b), were generated by water loss following loss of the neutral nucleobase as shown in Scheme 2. The fragmentation ions at m/z in Figure 3a and m/z in Figure 3b were all formed by water loss from the molecular ions of UpC and UpA. In the negative mode, the fragmentation mechanism of two deprotonated ions, at m/z and 549.3, has also been studied. By the similar dissociation pathway, sequence ions in the negative mode arising from cleavage of the phosphate-sugar bonds were also observed, so the sequences of products could be identified to be UpC and UpU by the diagnostic ion at m/z 305. Data are listed in Table 2. As reported, 1,2-elimination of nucleobase from the 5'-terminus is always preferred over nucleobase loss from the 3'-terminus for the dinucleotides in the negative mode. Therefore, for UpU and UpC, loss Scheme 1 Proposed fragmentation mechanism of protonated dinucleotides Scheme 2 Proposed fragmentation mechanism of protonated UpA and UpC
5 N-(O,O-Diisopropyl phosphoryl) alanine(dipp-ala) Chin. J. Chem., 2008 Vol. 26 No Table 2 ESI-MS 2 data of dinucleotides m/z (IR/%) Mode Compound Precursor ion Fragment ion (relative intensity/%) Product MS+ UpA 574.4(18) 556 (35), 531 (22), (42), (100), 391 (17), (16), (13), (14), (21), (14) MS+ UpC 550.3(10) 532 (12), (41), (100), (17), (17), (25) MS- UpC 548.0(33) (100), 463 (51), (16), (13) MS- UpU 549.3(49) (100), (55), (58), (37), (35), (22) Standard MS+ CpU 550.0(2) (100), (58), (16), (78) MS- CpU 548.0(18) (65), (91), (100), (52), (18) MS- UpG 588.0(2) (100), (59), (6), (88) Boldfaced number: diagnostic c-ions. of neutral uracil was preferred to form the ions at m/z 437 and 436. The proposed fragmentation mechanisms are shown in Scheme 3. In addition, a significant loss of 43 u to form base ion at m/z 505 was also observed for UpC. This product ion has also been observed for 2'-deoxycytidine 5'-monophosphate, 23 and attributed to loss of CONH via a retro Diels-Alder mechanism. To confirm the mechanisms proposed above, the fragmentation mechanism of standard samples, CpU and UpG, was studied and their MS 2 data are also listed in Table 2. In the same way, the characteristic fragment ions of dinucleotides were formed through loss of one nucleobase or one nucleoside. Although the nucleobase loss could occur from either 3'-terminus or 5'-terminus, it always lost the nucleobase from 5'-terminus. For example, CpU lost a cytosine to form an ion at m/z 437, just like that UpG lost a uracil to form ion at m/z 476. Considering the loss of one nucleoside, since cyclic transition state provided a low-energy route for the 2'-position proton transfer, it tended to lose the nucleoside from 3'-terminus, consequently giving rise to the diagnostic c-ion at m/z 304 and 305 from CpU and UpG, which could be used for us to identify the sequence of dinucleotide. It could be seen that the results from the standard compounds of dinucleotides were in good agreement with the assumptions. The detailed depictions of the fragmentation mechanisms of the standard compounds are shown in Scheme 4. Therefore, the c-ion in the mass spectra could be applied as a diagnostic ion to identify the sequence of dinucleotides produced in the reaction of DIPP-Ala with the four nucleosides. Conclusion The reaction products of DIPP-Ala with the four nucleosides (adenosine, uridine, cytidine and guanosine) in anhydrous pyridine were investigated by HPLC-ESI- MS/MS. Different mononucleotides and dinucleotides were observed and the characteristic fragmentation behavior of dinucleotides was discussed and demonstrated. It was firstly found that not only deprotonated ions but also protonated ions of dinucleotides could show characteristic information. The results showed that c-ions could be looked as the diagnostic ion to identify the sequence of dinucleotides produced in the reaction system. The HPLC-ESI-MS/MS technique could be potentially used to further investigate similar reactions between DIPP-AA and mixed nucleosides. Scheme 3 Proposed fragmentation mechanism of deprotonated UpU and UpC
6 1290 Chin. J. Chem., 2008, Vol. 26, No. 7 GUO et al. Scheme 4 Proposed fragmentation mechanism of deprotonated CpU and UpG References 1 Roblfing, D. L.; Fox, S. W. Adv. Catal. 1969, 20, Orgal, L. E. J. Mol. Biol. 1968, 38, Zhao, Y. F.; Cao, P. S. J. Biol. Phys. 1994, 20, Zhou, W. H.; Ju, Y.; Zhao, Y. F.; Wang, Q. G.; Luo, G. A. Origins Life Evol. Biosphere 1996, 26, Zhao, Y. F.; Hu, J. J.; Ju, Y. Chin. Chem. Lett. 2000, 11, Liu, H. X.; Zhao, C. F.; Lu, J. S.; Liu, M.; Zhang, S. S.; Jiang, Y. Y.; Zhao, Y. F. Anal. Chim. Acta 2006, 566, Xiang, H. Q.; Hu, J. J.; Jiang, Y.; Zhao, Y. F. Chin. Chem. Lett. 2001, 12, McLuckey, S. A.; Van Berkel, G. J.; Glish, G. L. J. Am. Soc. Mass Spectrom. 1992, 3, McLuckey, S. A.; Habibi-Goudarzi, S. J. Am. Chem. Soc. 1993, 115, Schulten, H. R.; Schiebel, H. M. Nucleic Acids Res. 1976, 3, Wu, J.; McLuckey, S. A. Int. J. Mass Spectrom. 2004, 237, Monn, S. T. M.; Schürch, S. J. Am. Soc. Mass Spectrom. 2007, 18, Wang, Z.; Wan, K. X.; Ramanathan, R.; Taylor, J. S.; Gross, M. L. J. Am. Soc. Mass Spectrom. 1998, 9, Schürch, S.; Bernal-Méndez, E.; Leumann, C. J. J. Am. Soc. Mass Spectrom. 2002, 13, Tromp, J. M.; Schürch, S. J. Am. Soc. Mass Spectrom. 2005, 16, Tromp, J. M.; Schürch, S. Rapid Commun. Mass Spectrom. 2006, 20, Zhao, Y. F.; Ju, Y.; Li, Y. M.; Wang, Q.; Yin, Y. W.; Tan, B. Int. J. Peptide Protein Res. 1995, 45, Deng, C. H.; Li, Y. M.; Zhao, Y. F. Phosphorus, Sulfur and Silicon 2000, 163, Hu, J. J.; Ju, Y.; Zhao, Y. F. Chin. J. Chem. 2000, 18, Ji, G. J.; Xue, C. B.; Zeng, J. N.; Li, L. P.; Chai, W. G.; Zhao, Y. F. Synthesis 1988, 6, Mack, D. O.; Reed, V. L.; Smith, L. D. J. Liquid Chromatogr. 1985, 8, Pimenov, A. M.; Tikhonov, Y. V.; Toguzov, P. T. J. Liquid Chromatogr. 1986, 9, Habibi-Goudarzi, S.; McLuckey, S. A. J. Am. Soc. Mass Spectrom. 1995, 6, 102. (E CHEN, J. X.)
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