Computational, biochemical and ex vivo evaluation of xanthine derivatives against phosphodiesterases to enhance the sperm motility

References

• Amer, M., Metawae, B., Hosny, H., & Raef, A. (2013). Beneficial effect of adding pentoxifylline to processed semen samples on ICSI outcome in infertile males with mild and moderate asthenozoospermia: A randomized controlled prospective crossover study. Iranian Journal of Reproductive Medicine, 11(11), 939–944.
   PubMedGoogle Scholar
• Buffone, M. G., Wertheimer, E. V., Visconti, P. E., & Krapf, D. (2014). Central role of soluble adenylyl cyclase and cAMP in sperm physiology. Biochimica et Biophysica Acta, 1842(12), 2610–2620. https://doi.org/10.1016/j.bbadis.2014.07.013
   PubMed Web of Science ®Google Scholar
• Ebner, T., Tews, G., Mayer, R. B., Ziehr, S., Arzt, W., Costamoling, W., & Shebl, O. (2011). Pharmacological stimulation of sperm motility in frozen and thawed testicular sperm using the dimethylxanthine theophylline. Fertility and Sterility, 96(6), 1331–1336. https://doi.org/10.1016/j.fertnstert.2011.08.041
   PubMed Web of Science ®Google Scholar
• Ferretti, C., Coppi, G., Blengio, M., & Genazzani, E. (1992). Inhibitory effect of theophylline, theophylline-7-acetic acid, ambroxol and ambroxol-theophylline-7-acetate on rat lung cAMP phosphodiesterase isoenzymes. International Journal of Tissue Reactions, 14(1), 31–36.
   PubMedGoogle Scholar
• Fisch, J. D., Behr, B., & Conti, M. (1998). Enhancement of motility and acrosome reaction in human spermatozoa: Differential activation by type-specific phosphodiesterase inhibitors. Human Reproduction (Oxford, England), 13(5), 1248–1254. https://doi.org/10.1093/humrep/13.5.1248
   PubMed Web of Science ®Google Scholar
• Ford, W. C., Rees, J. M., McLaughlin, E. A., Ling, L., & Hull, M. G. (1994). Pentoxifylline acts synergistically with A23187 to increase the penetration of zona-free hamster oocytes by cryopreserved human spermatozoa. International Journal of Andrology, 17(4), 199–204. https://doi.org/10.1111/j.1365-2605.1994.tb01243.x
   PubMedGoogle Scholar
• Fort, D. J., Stover, E. L., Propst, T. L., Faulkner, B. C., Vollmuth, T. A., & Murray, F. J. (1998). Evaluation of the developmental toxicity of caffeine and caffeine metabolites using the frog embryo teratogenesis assay—Xenopus (FETAX). Food and Chemical Toxicology, 36(7), 591–600. https://doi.org/10.1016/S0278-6915(98)00021-0
   PubMed Web of Science ®Google Scholar
• Freund, Y. R., Akama, T., Alley, M. R. K., Antunes, J., Dong, C., Jarnagin, K., Kimura, R., Nieman, J. A., Maples, K. R., Plattner, J. J., Rock, F., Sharma, R., Singh, R., Sanders, V., & Zhou, Y. (2012). Boron-based phosphodiesterase inhibitors show novel binding of boron to PDE4 bimetal center. FEBS Letters, 586(19), 3410–3414. https://doi.org/10.1016/j.febslet.2012.07.058
   PubMed Web of Science ®Google Scholar
• Gibbs, C. A., Weber, D. S., & Warren, J. J. (2021). Clustering of aromatic amino acid residues around methionine in proteins. Biomolecules, 12(1), 6. https://doi.org/10.3390/biom12010006
   PubMed Web of Science ®Google Scholar
• Halgren, T. A. (2009). Identifying and characterizing binding sites and assessing druggability. Journal of Chemical Information and Modeling, 49(2), 377–389. https://doi.org/10.1021/ci800324m
   PubMed Web of Science ®Google Scholar
• Hansel, T. T., Tennant, R. C., Tan, A. J., Higgins, L. A., Neighbour, H., Erin, E. M., & Barnes, P. J. (2004). Theophylline: Mechanism of action and use in asthma and chronic obstructive pulmonary disease. Drugs of Today (Barcelona, Spain : 1998), 40(1), 55–69. https://doi.org/10.1358/dot.2004.40.1.799438
   PubMed Web of Science ®Google Scholar
• Hendeles, L., Massanari, M., & Weinberger, M. (1985). Update on the pharmacodynamics and pharmacokinetics of theophylline. Chest, 88(2 Suppl), 103S–111S. https://doi.org/10.1378/chest.88.2_supplement.103s
   PubMed Web of Science ®Google Scholar
• Huai, Q., Colicelli, J., & Ke, H. (2003). The crystal structure of AMP-Bound PDE4 suggests a mechanism for phosphodiesterase catalysis. Biochemistry, 42(45), 13220–13226. https://doi.org/10.1021/bi034653e
   PubMed Web of Science ®Google Scholar
• Hudson, L. D., Tyler, M. L., & Petty, T. L. (1973). Oral aminophylline and dikydroxypropyl theophylline in reversible obstructive airway disease: A single-dose, double-blind, crossover comparison. Current Therapeutic Research, Clinical and Experimental, 15(7), 367–372.
   PubMed Web of Science ®Google Scholar
• Inhorn, M. C., & Patrizio, P. (2015). Infertility around the globe: New thinking on gender, reproductive technologies and global movements in the 21st century. Human Reproduction Update, 21(4), 411–426. https://doi.org/10.1093/humupd/dmv016
   PubMed Web of Science ®Google Scholar
• Irvine, D. S. (1998). Epidemiology and aetiology of male infertility. Human Reproduction (Oxford, England), 13(Suppl 1), 33–44. https://doi.org/10.1093/humrep/13.suppl_1.33
   PubMedGoogle Scholar
• Jansen, C., Kooistra, A. J., Kanev, G. K., Leurs, R., de Esch, I. J. P., & de Graaf, C. (2016). PDEStrIAn: A phosphodiesterase structure and ligand interaction annotated database as a tool for structure-based drug design. Journal of Medicinal Chemistry, 59(15), 7029–7065. https://doi.org/10.1021/acs.jmedchem.5b01813
   PubMed Web of Science ®Google Scholar
• Javed, M., Abdulrazzak, O., Matrafi, H., Najashi, S., & Sufyan, H. (2017). Outcome of ICSI using pentoxifylline or theophylline to identify viable spermatozoa in patients with all immotile spermatozoa. Fertility and Sterility, 108(3), e131. https://doi.org/10.1016/j.fertnstert.2017.07.396
   Google Scholar
• Jayaprakash, D., Kumar, K. S., Shivaji, S., & Seshagiri, P. B. (1997). Pentoxifylline induces hyperactivation and acrosome reaction in spermatozoa of golden hamsters: Changes in motility kinematics. Human Reproduction (Oxford, England), 12(10), 2192–2199. https://doi.org/10.1093/humrep/12.10.2192
   PubMed Web of Science ®Google Scholar
• Jilani, T. N., Preuss, C. V., & Sharma, S. (2021). Theophylline. In StatPearls. StatPearls Publishing. http://www.ncbi.nlm.nih.gov/books/NBK519024/
   Google Scholar
• Journey, J. D., & Bentley, T. P. (2021). Theophylline toxicity. In StatPearls. StatPearls Publishing. http://www.ncbi.nlm.nih.gov/books/NBK532962/
   Google Scholar
• Khan, S., Farooq, U., & Kurnikova, M. (2017). Protein stability and dynamics influenced by ligands in extremophilic complexes - a molecular dynamics investigation. Molecular bioSystems, 13(9), 1874–1887. https://doi.org/10.1039/c7mb00210f
   PubMedGoogle Scholar
• Kovacic, B., Vlaisavljevic, V., & Reljic, M. (2006). Clinical use of pentoxifylline for activation of immotile testicular sperm before ICSI in patients with azoospermia. Journal of Andrology, 27(1), 45–52. https://doi.org/10.2164/jandrol.05079
   PubMedGoogle Scholar
• Kumar, N., & Singh, A. K. (2015). Trends of male factor infertility, an important cause of infertility: A review of literature. Journal of Human Reproductive Sciences, 8(4), 191–196. https://doi.org/10.4103/0974-1208.170370
   PubMedGoogle Scholar
• Lacham-Kaplan, O., & Trounson, A. O. (1994). Embryo development capacity of oocytes fertilized by immature sperm and sperm treated with motility stimulants. Reproduction, Fertility, and Development, 6(1), 113–116. https://doi.org/10.1071/rd9940113
   PubMed Web of Science ®Google Scholar
• Levine, E. R. (1965). An effective oral medication for long term bronchodilation. Annals of Allergy, 23(9), 403–413.
   PubMedGoogle Scholar
• Loughlin, K. R., & Agarwal, A. (1992). Use of theophylline to enhance sperm function. Archives of Andrology, 28(2), 99–103. https://doi.org/10.3109/01485019208987686
   PubMed Web of Science ®Google Scholar
• Mangoli, V., Mangoli, R., Dandekar, S., Suri, K., & Desai, S. (2011). Selection of viable spermatozoa from testicular biopsies: A comparative study between pentoxifylline and hypoosmotic swelling test. Fertility and Sterility, 95(2), 631–634. https://doi.org/10.1016/j.fertnstert.2010.10.007
   PubMed Web of Science ®Google Scholar
• Maréchal, L., Guillemette, C., Goupil, S., Blondin, P., Leclerc, P., & Richard, F. J. (2017). Cyclic nucleotide phosphodiesterases in human spermatozoa and seminal fluid: Presence of an active PDE10A in human spermatozoa. Biochimica et Biophysica Acta. General Subjects, 1861(2), 147–156. https://doi.org/10.1016/j.bbagen.2016.11.006
   PubMed Web of Science ®Google Scholar
• Masood, S., Rehman, W., Khan, Z., Arshad, H., Begum, S., & Perveen, A. (2018). Structure breaking/making property of acefylline piperazine in aqueous, aqueous methanol, and aqueous ethylene glycol systems. Journal of Structural Chemistry, 59(5), 1148–1157. https://doi.org/10.1134/S0022476618050189
   Web of Science ®Google Scholar
• McCOLL, J. D., Parker, J. M., & Ferguson, J. K. W. (1956). A comparison of the relative toxic, emetic and convulsive actions of a series of methylated xanthine derivatives. The Journal of Pharmacology and Experimental Therapeutics, 116(3), 343–350.
   PubMed Web of Science ®Google Scholar
• National Toxicology Program. (1998). NTP toxicology and carcinogenesis studies of theophylline (CAS No. 58-55-9) in F344/N rats and B6C3F1 mice (feed and gavage studies). National Toxicology Program Technical Report Series (Vol. 473, pp. 1–326).
   Google Scholar
• Negri, P., Grechi, E., Tomasi, A., Fabbri, E., & Capuzzo, A. (1996). Effectiveness of pentoxifylline in semen preparation for intrauterine insemination. Human Reproduction (Oxford, England), 11(6), 1236–1239. https://doi.org/10.1093/oxfordjournals.humrep.a019363
   PubMed Web of Science ®Google Scholar
• Oraibi, H. H., Mossa, H. A. L., Al-Kawaz, U. M., & Madeed, N. S. (2017). Study of theophylline role in sperm selection for intracytoplasmic sperm injection (ICSI) in men with non-obstructive azoospermia. Journal of Pharmaceutical Sciences and Research, 9, 5.
   Google Scholar
• Phear, D. N. (1957). An objective comparison of two recent neutral theophylline compounds with aminophylline. British Medical Journal, 2(5036), 74–75.
   PubMedGoogle Scholar
• Recht, M. I., Sridhar, V., Badger, J., Hernandez, L., Chie-Leon, B., Nienaber, V., & Torres, F. E. (2012). Fragment-based screening for inhibitors of PDE4A using enthalpy arrays and X-ray crystallography. SLAS Discovery, 17(4), 469–480. https://doi.org/10.1177/1087057111430987
   Google Scholar
• Richter, W., Dettmer, D., & Glander, H. (1999). Detection of mRNA transcripts of cyclic nucleotide phosphodiesterase subtypes in ejaculated human spermatozoa. Molecular Human Reproduction, 5(8), 732–736. https://doi.org/10.1093/molehr/5.8.732
   PubMed Web of Science ®Google Scholar
• Rzasa, R. M., Hu, E., Rumfelt, S., Chen, N., Andrews, K. L., Chmait, S., falsey, J. R., Zhong, W., Jones, A. D., Porter, A., Louie, S. W., Zhao, X., Treanor, J. J., & Allen, J. R. (2012). Discovery of selective biaryl ethers as PDE10A inhibitors: Improvement in potency and mitigation of Pgp-mediated efflux. Bioorganic & Medicinal Chemistry Letters, 22(24), 7371–7375. https://doi.org/10.1016/j.bmcl.2012.10.078
   PubMed Web of Science ®Google Scholar
• Satish, M., Kumari, S., Deeksha, W., Abhishek, S., Nitin, K., Adiga, S. K., Hegde, P., Dasappa, J. P., Kalthur, G., & Rajakumara, E. (2021). Structure-based redesigning of pentoxifylline analogs against selective phosphodiesterases to modulate sperm functional competence for assisted reproductive technologies. Scientific Reports, 11(1), 12293. https://doi.org/10.1038/s41598-021-91636-y
   PubMed Web of Science ®Google Scholar
• Selvig, K. (1981). Pharmacokinetics of proxyphylline in adults after intravenous and oral administration. European Journal of Clinical Pharmacology, 19(2), 149–155. https://doi.org/10.1007/BF00568402
   PubMed Web of Science ®Google Scholar
• Simons, K. J., Simons, F. E., & Bierman, C. W. (1977). Bioavailability of a sustained-release dyphylline formulation. Journal of Clinical Pharmacology, 17(4), 237–241. https://doi.org/10.1177/009127007701700408
   PubMed Web of Science ®Google Scholar
• Tardif, S., Madamidola, O. A., Brown, S. G., Frame, L., Lefièvre, L., Wyatt, P. G., Barratt, C. L. R., & Martins Da Silva, S. J. (2014). Clinically relevant enhancement of human sperm motility using compounds with reported phosphodiesterase inhibitor activity. Human Reproduction (Oxford, England), 29(10), 2123–2135. https://doi.org/10.1093/humrep/deu196
   PubMed Web of Science ®Google Scholar
• Tesarik, J., Mendoza, C., & Carreras, A. (1992). Effects of phosphodiesterase inhibitors caffeine and pentoxifylline on spontaneous and stimulus-induced acrosome reactions in human sperm. Fertility and Sterility, 58(6), 1185–1190. https://doi.org/10.1016/S0015-0282(16)55567-8
   PubMed Web of Science ®Google Scholar
• Tournaye, H., Janssens, R., Verheyen, G., Camus, M., Devroey, P., & Van Steirteghem, A. (1994). An indiscriminate use of pentoxifylline does not improve in-vitro fertilization in poor fertilizers. Human Reproduction (Oxford, England), 9(7), 1289–1292. https://doi.org/10.1093/oxfordjournals.humrep.a138696
   PubMed Web of Science ®Google Scholar
• Unsal, E., Turan, V., Aktuna, S., Hurdag, C., Bereketoglu, G., Canillioglu, Y., Baltacı, A., Ozcan, S., Karayalcin, R., Batırbaygil, H., & Baltacı, V. (2016). Effects of pentoxifylline and platelet activating factor on sperm DNA damage. European Journal of Obstetrics, Gynecology, and Reproductive Biology, 197, 125–129. https://doi.org/10.1016/j.ejogrb.2015.12.016
   PubMed Web of Science ®Google Scholar
• Vangone, A., Schaarschmidt, J., Koukos, P., Geng, C., Citro, N., Trellet, M. E., Xue, L. C., & Bonvin, A. M. J. J. (2019). Large-scale prediction of binding affinity in protein-small ligand complexes: The PRODIGY-LIG web server . Bioinformatics (Oxford, England), 35(9), 1585–1587. https://doi.org/10.1093/bioinformatics/bty816
   PubMed Web of Science ®Google Scholar
• Wang, H., Robinson, H., & Ke, H. (2007). The molecular basis for different recognition of substrates by phosphodiesterase families 4 and 10. Journal of Molecular Biology, 371(2), 302–307. https://doi.org/10.1016/j.jmb.2007.05.060
   PubMed Web of Science ®Google Scholar
• Wyatt, R., Weinberger, M., & Hendeles, L. (1978). Oral theophylline dosage for the management of chronic asthma. The Journal of Pediatrics, 92(1), 125–130. https://doi.org/10.1016/S0022-3476(78)80093-6
   PubMed Web of Science ®Google Scholar
• Yoshioka, K., Suzuki, C., Itoh, S., Kikuchi, K., Iwamura, S., & Rodriguez-Martinez, H. (2003). Production of piglets derived from in vitro-produced blastocysts fertilized and cultured in chemically defined media: Effects of theophylline, adenosine, and cysteine during in vitro fertilization. Biology of Reproduction, 69(6), 2092–2099. https://doi.org/10.1095/biolreprod.103.020081
   PubMed Web of Science ®Google Scholar
• Yovich, J. L. (1993). Pentoxifylline: Actions and applications in assisted reproduction. Human Reproduction (Oxford, England), 8(11), 1786–1791. https://doi.org/10.1093/oxfordjournals.humrep.a137935
   PubMed Web of Science ®Google Scholar