Investigation of TMPYP4 porphyrin interaction with AS1411 aptamer using spectroscopic methods

Document Type : Original Research

Authors

1 student

2 Professor

3 full Profesor

Abstract
Spectral properties and thermal stability of AS1411 G-quadruplex AS1411 is an anticancer four-stranded deoxyoligonucleotide with high affinity and specificity to a putative surface biomarker, nucleolin, which is an overexpressed protein on numerous cancer cells. AS1411 has valuable functional potential for the targeted delivery of nanoparticles, oligonucleotides, peptides and small drug molecules to cancer cells. Considering that understanding interaction of drug with target molecule is important and necessary for pharmaceutical studies, in the present study, the interaction of a porphyrin photosensitizer called TMPYP4 was evaluated with aptamer AS1411. Absorption and fluorescence spectroscopy and circular dichroism technique were used to identify how and where TMPYP4 binds to AS1411 and the resulting structural changes. The results showed that binding of the porphyrin to AS1411 caused 13 nm red shift and 56% hypochromicity in the absorption spectrum; in addition, due to this binding, the emission spectrum of porphyrin is changed and its emission intensity is reduced. The results of structural studies showed that the binding of TMPYP4 does not significantly change the shape of the AS1411 circular dichroism spectrum, but at high concentrations leads to an intense decrease in the intensity of the spectrum. These changes in the spectra indicate that TMPYP4 binds to the aptamer through intercalation between tetrad planes and end-staking and causes to opening of the aptamer structure. As a conclusion, it can be proposed that AS1411 aptamer has appropriate potential for delivery of porphyrin compounds and their photosensitizer types and can be used in photodynamic therapy of cancer cells.

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[1] P.J. Bates, D.A. Laber, D.M. Miller, S.D. Thomas, J.O. Trent. (2009) Discovery and development of the G-rich oligonucleotide AS1411 as a novel treatment for cancer. Exp Mol Pathol. 86, 151-164.
[2] P.J. Bates, J.B. Kahlon, S.D. Thomas, J.O. Trent, D.M. Miller. (1999) Antiproliferative activity ofG-rich oligonucleotides correlates with protein binding. The Journal of biological chemistry. 274, 26369-26377.
[3] V. Dapic, V. Abdomerovic, R. Marrington, J. Peberdy, A. Rodger, J.O. Trent, P.J. Bates. (2003)
Biophysical and biological properties of quadruplex oligodeoxyribonucleotides. Nucleic Acids
Res. 31, 2097-2107.
[4] Dapić V, Bates PJ, Trent JO, Rodger A, Thomas SD, M. DM. (2002) Antiproliferative activity of Gquartet-forming oligonucleotides with backbone and sugar modifications. Biochemistry. 41,
3676-3685.
[5] Sannohe, Yuta, and Hiroshi Sugiyama. (2010) "Overview of formation of G‐quadruplex structures." Current protocols in nucleic acid chemistry. 40.1, 17-2.‌
[6] W. Jia, Z. Yao, J. Zhao, Q. Guan, L. Gao. (2017) New perspectives of physiological and pathological functions of nucleolin (NCL). Life sciences. 186, 1-10.
[7] T. Le Trinh, G. Zhu, X. Xiao, W. Puszyk, K. Sefah, Q. Wu, W. Tan, C. Liu. (2015) A synthetic
aptamer-drug adduct for targeted liver cancer therapy. PLoS One. 10(11), e0136673.
[8] S.H. Rajabnejad, A. Mokhtarzadeh, K. Abnous, S.M. Taghdisi, M. Ramezani, B.M. Razavi,
(2018) Targeted delivery of melittin to cancer cells by AS1411 anti-nucleolin aptamer. Drug
development and industrial pharmacy. 44(6), 982-987.
[9] F.S.M. Tekie, M. Soleimani, A. Zakerian, M. Dinarvand, M. Amini, R. Dinarvand, E.
Arefian, F. Atyabi. (2018) Glutathione responsive chitosan-thiolated dextran conjugated miR-145
nanoparticles targeted with AS1411 aptamer for cancer treatment. Carbohydrate polymers. 201,
131-140.
[10] R. Zhang, S.-B. Wang, W.-G. Wu, R.K. Kankala, A.-Z. Chen, Y.-G. Liu, J.-Q. (2017) Fan, Codelivery of doxorubicin and AS1411 aptamer by poly (ethylene glycol)-poly (β-amino esters)
polymeric micelles for targeted cancer therapy. Journal of Nanoparticle Research. 19,
224.
[11] Liao, Zi-Xian, et al. (2015) "An AS1411 aptamer-conjugated liposomal system containing a bubble-generating agent for tumor-specific chemotherapy that overcomes multidrug resistance." Journal of controlled release. 208, 42-51.‌
[12] Li, Xin, et al. (2015) "Targeted delivery of anticancer drugs by aptamer AS1411 mediated Pluronic F127/cyclodextrin-linked polymer composite micelles." Nanomedicine: Nanotechnology, Biology and Medicine. 11.1, 175-184.‌
[13] Peng, Li-Hua, et al. (2015) "Cell membrane capsules for encapsulation of chemotherapeutic and cancer cell targeting in vivo." ACS applied materials & interfaces. 7.33, 18628-18637.‌
[14] Gao, Huile, et al. (2012) "Precise glioma targeting of and penetration by aptamer and peptide dual-functioned nanoparticles." Biomaterials. 33.20, 5115-5123.‌
[15] Dolmans, D.E., Fukumura, D. and Jain, R.K. (2003) Photodynamic therapy for cancer. Nature reviews cancer. 3, 380-387.
[16] Cao, Z., Tong, R., Mishra, A., Xu, W., Wong, G.C., Cheng, J. and Lu, Y. (2009) Reversible Cell‐Specific Drug Delivery with Aptamer‐Functionalized Liposomes. Angewandte Chemie International Edition. 48(35), 6494-6498.
[17] Carvalho, Josué, et al. (2019) "Aptamer-based targeted Delivery of a G-quadruplex Ligand in Cervical Cancer Cells." Scientific reports. 9.1, 1-12.‌
[18] Y.A. Shieh, S.J. Yang, M.F. Wei, M.J. Shieh. (2010) Aptamer-based tumor-targeted drug delivery
for photodynamic therapy. ACS nano. 4, 1433-1442.
[19] Wei, Chunying, et al. (2006) "A spectroscopic study on the interactions of porphyrin with G-quadruplex DNAs." Biochemistry. 45.21, 6681-6691.‌
[20] Zhang, HuiJuan, et al. (2008) "Interactions between meso-tetrakis (4-(N-methylpyridiumyl)) porphyrin TMPyP4 and DNA G-quadruplex of telomeric repeated sequence TTAGGG." Science in China Series B: Chemistry. 51.5, 452-456.‌
[21] Cogoi, Susanna, and Luigi E. Xodo. (2006) "G-quadruplex formation within the promoter of the KRAS proto-oncogene and its effect on transcription." Nucleic acids research. 34.9, 2536-2549.

[22] Waller, Zoë AE, et al. (2016) "Control of bacterial nitrate assimilation by stabilization of G-quadruplex DNA." Chemical Communications. 52.92, 13511-13514.‌
[23] Zidanloo, Saeedeh Ghazaey, et al. (2016) "Downregulation of the WT 1 gene expression via TMPyP4 stabilization of promoter G-quadruplexes in leukemia cells." Tumor Biology. 37.7, 9967-9977.‌
[24] Ofer, Noa, et al. (2009) "The quadruplex r (CGG) n destabilizing cationic porphyrin TMPyP4 cooperates with hnRNPs to increase the translation efficiency of fragile X premutation mRNA." Nucleic acids research. 37.8, 2712-2722.‌
[25] Singh, Anju, Savita Joshi, and Shrikant Kukreti. (2020) "Cationic porphyrins as destabilizer of a G-quadruplex located at the promoter of human MYH7 β gene." Journal of Biomolecular Structure and Dynamics. 38.16, 4801-4816.‌
[26] Andrew, Elizabeth J., et al. (2013) "Pentose phosphate pathway function affects tolerance to the G-quadruplex binder TMPyP4." PloS one. 8.6, e66242.

[27] Cantor, C. R., Warshaw, M. M., & Shapiro, H. (1970). Oligonucleotide interactions. III. Circular dichroism studies of the conformation of deoxyoligonucleolides. Biopolymers: Original Research on Biomolecules. 9(9), 1059-1077.‌
[28] Zhang, H., Xiao, X., Wang, P., Pang, S., Qu, F., Ai, X., & Zhang, J. (2009). Conformational conversion of DNA G-quadruplex induced by a cationic porphyrin. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 74(1), 243-247.
[29] Dehgani, K.M. (2010) A comprehensive description of Biophysics. 1st ed.
[30] Wei, Chunying, et al. (2006) "A spectroscopic study on the interactions of porphyrin with G-quadruplex DNAs." Biochemistry. 45.21, 6681-6691.‌
[31] Le, Vu H., Narayana Nagesh, and Edwin A. Lewis. (2013) "Bcl-2 promoter sequence G-quadruplex interactions with three planar and non-planar cationic porphyrins: TMPyP4, TMPyP3, and TMPyP2." PloS one. 8.8, e72462.‌
[32] Lakowicz, J. R. (Ed.). (2013) Principles of fluorescence spectroscopy. Springer science & business media. ‌
[33] Zhao, L., Liu, R., Zhao, X., Yang, B., Gao, C., Hao, X., & Wu, Y. (2009) New strategy for the evaluation of CdTe quantum dot toxicity targeted to bovine serum albumin. Science of the total environment. 407.18, 5019-5023.‌
[34] Suryawanshi, V. D., Walekar, L. S., Gore, A. H., Anbhule, P. V., & Kolekar, G. B. (2016) Spectroscopic analysis on the binding interaction of biologically active pyrimidine derivative with bovine serum albumin. Journal of Pharmaceutical Analysis. 6.1, 56-63.‌
[35] Asadi, M., Safaei, E., Ranjbar, B., & Hasani, L. (2004) Thermodynamic and spectroscopic study on the binding of cationic Zn (II) and Co (II) tetrapyridinoporphyrazines to calf thymus DNA: the role of the central metal in binding parameters. New journal of chemistry. 28.10, 1227-1234.‌
[36] Ranjbar, B., & Gill, P. (2009). Circular dichroism techniques: biomolecular and nanostructural analyses‐a review. Chemical biology & drug design, 74(2), 101-120.‌
[37] Carvalho, J., Queiroz, J.A., Cruz, C. (2017) Circular Dichroism of G-Quadruplex: a Laboratory Experiment for the Study of Topology and Ligand Binding. J. Chem. Educ. 94, 1547–1551.
[38] Do, N.Q., Chung, W.J., Hong, T., Truong, A., Heddi, B., Phan, A.T. (2017). G-quadruplex structure of an anti-proliferative DNA sequence. Nucleic Acids Res. 1–7.
[39] Le, Vu H., Narayana Nagesh, and Edwin A. Lewis. (2013) "Bcl-2 promoter sequence G-quadruplex interactions with three planar and non-planar cationic porphyrins: TMPyP4, TMPyP3, and TMPyP2." PloS one. 8.8, e72462.‌
[40] M.M. Dailey, M.C. Miller, P.J. Bates, A.N. Lane, J.O. Trent. Resolution and characterization of the structural polymorphism of a single quadruplex-forming sequence, Nucleic Acids Res. 2010; 38: 4877-4888.
[41] Dai, J.; Carver, M.; Yang, D. (2008) Polymorphism of human telomeric quadruplex structures. Biochimie. 90, 1172.
[42] Pasternack, Robert F., Esther J. Gibbs, and Joseph J. Villafranca. (1983) "Interactions of porphyrins with nucleic acids." Biochemistry. 22.23, 5409-5417.‌
[43] Wei, Chunying, et al. (2009) "Evidence for the binding mode of porphyrins to G-quadruplex DNA." Physical Chemistry Chemical Physics. 11.20, 4025-4032.‌
[44] Arora, Amit, and Souvik Maiti. (2008) "Effect of loop orientation on quadruplex− TMPyP4 interaction." The Journal of Physical Chemistry B. 112.27, 8151-8159.‌
[45] Pasternack, Robert F., and Esther J. Gibbs. (1989) "Interaction of porphyrins and metalloporphyrins with nucleic acids." 59-73.‌
[46] Kalayanasundaram, K. (1984). Photochemistry of water-soluble porphyrins: Comparative study of isomeric tetrapyridyl-and tetrakis (N-methylpyridiniumy1) porphyrins. Inorganic Chemistry, 23, 2453-2459.‌
[47] Sazanovich, I. V., & Chirvonyi, V. S. (2005). Deactivation of the S1 state of a water-soluble porphyrin cation in a complex with DNA studied by the method of picosecond absorption spectroscopy. Quantum Electronics, 35(8), 756.‌
[48] Zhang, HuiJuan, et al. (2008) "Interactions between meso-tetrakis (4-(N-methylpyridiumyl)) porphyrin TMPyP4 and DNA G-quadruplex of telomeric repeated sequence TTAGGG." Science in China Series B: Chemistry. 51.5, 452-456.‌
[49] Makarska-Bialokoz, Magdalena. (2012) "Spectroscopic study of porphyrin-caffeine interactions." Journal of fluorescence. 22.6, 1521-1530.‌
[50] Sazanovich, Igor'V., and Vladimir Sergeevich Chirvonyi. (2005) "Deactivation of the S1 state of a water-soluble porphyrin cation in a complex with DNA studied by the method of picosecond absorption spectroscopy." Quantum Electronics. 35.8, 756.‌
[51] Airoldi, Marta, et al. (2014) "Interaction of doxorubicin with polynucleotides. A spectroscopic study." Biochemistry. 53.13, 2197-2207.‌
[52] Ranjan, M., Diffley, P., Stephen, G., Price, D., Walton, T. J., & Newton, R. P. (2002). Comparative study of human steroid 5α-reductase isoforms in prostate and female breast skin tissues: sensitivity to inhibition by finasteride and epristeride. Life sciences, 71(2), 115-126.‌

[53] Wang, Y. Q., Zhang, H. M., & Zhou, Q. H. (2009). Studies on the interaction of caffeine with bovine hemoglobin. European journal of medicinal chemistry, 44(5), 2100-2105.‌
[54] Lakowicz J.R. (2006) Principles of Fluorescence Spectroscopy. Springer, Boston, MA. 331-351.
[55] Ren, J.; Chaires, J. B. (1999) Sequence and structural selectivity of nucleic acid binding ligands. Biochemistry. 38, 16067.
[56] Ross, Philip D., and S. Subramanian. (1981) "Thermodynamics of protein association reactions: forces contributing to stability." Biochemistry 20.11, 3096-3102.‌
[57] Hassani, L., et al. (2018) "Thermodynamic Investigation of Copper Porphyrazines and Phthalocyanine Interaction with Human Telomeric G-Quadruplex DNA." Modares Journal of Biotechnology. 9.3, 395-402.‌
[58] Dezhampanah, Hamid, Abdol-Khalegh Bordbar, and Shahram Tangestaninejad. (2009) "Thermodynamic investigation of manganese (III) 5-(1-(4-carboxybutyl) pyridinium-4-yl) 10, 15, 20-tris-(1-methylpyridinium-4-yl) porphyrin with calf thymus DNA." Journal of Porphyrins and Phthalocyanines 13.08n09, 964-972.‌
[59] Dezhampanah, Hamid, and Soghra Fyzolahjani. (2013) "Study on interaction of cationic porphyrazine with synthetic polynucleotides." Analytical Cellular Pathology 36.5, 6 125-132.‌
[60] Olsen, C. M. (2008) Thermodynamic characterization of the folding and interaction of G-quadruplex. Ph.D. Dissertation, University of Nebraska Medical Center.
[61] Z. Bagheri, B. Ranjbar, H. Latifi, M.I. Zibaii, T.T. Moghadam, A. Azizi. (2015) Spectral properties and thermal stability of AS1411 G-quadruplex. International journal of biological
Macromolecules. 72, 806-811.
[62] Fan, Xinmeng, et al. (2016) "Bioactivity of 2′-deoxyinosine-incorporated aptamer AS1411." Scientific reports. 6.1, 1-12.‌