Unlocking the Immunomodulatory Potential of Rosmarinic Acid Isolated from Punica granatum L. using Bioactivity-Guided Approach: In Silico, In Vitro, and In Vivo Approaches

  • Авторлар: Gautam R.1, Tripathi S.2, Akash S.3, Sharma S.4, Sharma K.5, Goyal S.6, Behzad S.7, Gundamaraju R.8, Mishra D.9, Zhang Y.1, Shen B.1, Sundriyal S.10, Singla R.1
  • Мекемелер:
    1. Department of Critical Care Medicine and Institutes for Systems Genetics, Frontiers Science Center for Disease-related Molecular Network, West China Hospital, Sichuan University
    2. Department of Pharmacy, Birla Institute of Technology and Science Pilani
    3. Department of Pharmacy, Daffodil International University
    4. Department of Quality Assurance, Shobhaben Pratapbhai Patel School of Pharmacy & Technology Management, SVKMs NMIMS
    5. Bhupal Nobles' College of Pharmacy,, Bhopal Noble's University
    6. Faculty of Pharmacy, Mandsaur University
    7. Evidence-based Phytotherapy and Complementary Medicine Research Center, Alborz University of Medical Sciences
    8. ER stress and mucosal immunology lab, School of Health Sciences, University of CaliforniUniversity of Tasmaniaa, San Francisco
    9. Department of Pharmacy, Guru Ghasidas Vishwavidyalaya (A Central University) Koni
    10. Department of Pharmacy, Birla Institute of Technology and Science Pilani, Pilani Campus
  • Шығарылым: Том 31, № 36 (2024)
  • Беттер: 5969-5988
  • Бөлім: Anti-Infectives and Infectious Diseases
  • URL: https://rjpbr.com/0929-8673/article/view/645252
  • DOI: https://doi.org/10.2174/0109298673291064240227094654
  • ID: 645252

Дәйексөз келтіру

Толық мәтін

Аннотация

Background:Punica granatum L. is well-known for its multifaceted therapeutic potential, including anti-inflammatory and immunomodulatory activities.

Aim:This study aimed to characterize an immunomodulatory compound isolated from Punica granatum L. using a bioactivity-guided approach.

Methods:Chromatographic techniques were adopted for isolation and purification of secondary metabolites. In silico, in vitro, and in vivo methods were performed to characterize the therapeutic potential of the isolated compound.

Results:Using preparative thin-layer chromatography, rosmarinic acid was isolated from F4 (column chromatography product obtained from a butanolic fraction of the extract). The impact of rosmarinic acid was assessed in rats using the neutrophil adhesion test, DTH response, and phagocytic index. In immunized rats, rosmarinic acid demonstrated significant immunomodulatory potential. Computational experiments, like molecular docking and molecular dynamics, were also conducted against two targeted receptors, Cereblon (PDB ID: 8AOQ) and human CD22 (PDB ID: 5VKM). Computational studies suggested that an increase in phagocytic index by rosmarinic acid could be attributed to inhibiting Cereblon and CD22. Pharmacokinetics and toxicity prediction also suggested the drug-likeness of rosmarinic acid.

Conclusion:Rosmarinic acid is a potential candidate, but extensive research needs to be done to translate this molecule from bench to bedside.

Авторлар туралы

Rupesh Gautam

Department of Critical Care Medicine and Institutes for Systems Genetics, Frontiers Science Center for Disease-related Molecular Network, West China Hospital, Sichuan University

Email: info@benthamscience.net

Shailesh Tripathi

Department of Pharmacy, Birla Institute of Technology and Science Pilani

Email: info@benthamscience.net

Shopnil Akash

Department of Pharmacy, Daffodil International University

Email: info@benthamscience.net

Sanjay Sharma

Department of Quality Assurance, Shobhaben Pratapbhai Patel School of Pharmacy & Technology Management, SVKMs NMIMS

Email: info@benthamscience.net

Komal Sharma

Bhupal Nobles' College of Pharmacy,, Bhopal Noble's University

Email: info@benthamscience.net

Swapnil Goyal

Faculty of Pharmacy, Mandsaur University

Email: info@benthamscience.net

Sahar Behzad

Evidence-based Phytotherapy and Complementary Medicine Research Center, Alborz University of Medical Sciences

Email: info@benthamscience.net

Rohit Gundamaraju

ER stress and mucosal immunology lab, School of Health Sciences, University of CaliforniUniversity of Tasmaniaa, San Francisco

Email: info@benthamscience.net

Dinesh Mishra

Department of Pharmacy, Guru Ghasidas Vishwavidyalaya (A Central University) Koni

Email: info@benthamscience.net

Yingbo Zhang

Department of Critical Care Medicine and Institutes for Systems Genetics, Frontiers Science Center for Disease-related Molecular Network, West China Hospital, Sichuan University

Email: info@benthamscience.net

Bairong Shen

Department of Critical Care Medicine and Institutes for Systems Genetics, Frontiers Science Center for Disease-related Molecular Network, West China Hospital, Sichuan University

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Sandeep Sundriyal

Department of Pharmacy, Birla Institute of Technology and Science Pilani, Pilani Campus

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Rajeev Singla

Department of Critical Care Medicine and Institutes for Systems Genetics, Frontiers Science Center for Disease-related Molecular Network, West China Hospital, Sichuan University

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Әдебиет тізімі

  1. Wagner, H.; Hikino, H.; Farnsworth, N. Economic and Medicinal Plant Research, 3rd ed.; Elsevier, 1989.
  2. Singla, R.K.; Guimarães, A.G.; Zengin, G. Editorial: Application of plant secondary metabolites to pain neuromodulation, volume III. Front. Pharmacol., 2023, 14, 1166272. doi: 10.3389/fphar.2023.1166272 PMID: 36895948
  3. Singla, R.K.; Joon, S.; Sinha, B.; Kamal, M.A.; Simal-Gandara, J.; Xiao, J.; Shen, B. Current trends in natural products for the treatment and management of dementia: Computational to clinical studies. Neurosci. Biobehav. Rev., 2023, 147, 105106. doi: 10.1016/j.neubiorev.2023.105106 PMID: 36828163
  4. Babbar, R.; Kaur, R.; Rana, P.; Arora, S.; Behl, T.; Albratty, M.; Najmi, A.; Meraya, A.M.; Alhazmi, H.A.; Singla, R.K.; Parajuli, N. The current landscape of bioactive molecules against DENV: A systematic review. Evid. Based Complement. Alternat. Med., 2023, 2023, 1-17. doi: 10.1155/2023/2236210 PMID: 36818227
  5. Kumar, D.; Singla, R.K.; Sharma, R.; Sharma, P.; Kumar, L.; Kaur, N.; Dhawan, R.K.; Sharma, S.; Dua, K. Phytochemistry and polypharmacological potential of Colebrookea oppositifolia smith. Curr. Top. Med. Chem., 2023, 23(5), 334-348. doi: 10.2174/1568026623666221202112414 PMID: 36476430
  6. Singla, R.K.; De, R.; Efferth, T.; Mezzetti, B.; Sahab Uddin, M. The International Natural Product Sciences Taskforce (INPST) and the power of Twitter networking exemplified through #INPST hashtag analysis. Phytomedicine, 2023, 108, 154520.
  7. Singla, R.K.; Dubey, A.K. Phytochemical profiling, GC-MS analysis and α-amylase inhibitory potential of ethanolic extract of Cocos nucifera linn. endocarp. Endocr. Metab. Immune Disord. Drug Targets, 2019, 19(4), 419-442. doi: 10.2174/1871530319666181128100206 PMID: 30484412
  8. Marzocco, S.; Singla, R.K.; Capasso, A. Multifaceted effects of lycopene: A boulevard to the multitarget-based treatment for cancer. Molecules, 2021, 26(17), 5333. doi: 10.3390/molecules26175333 PMID: 34500768
  9. Singla, R.K.; Sai, C.S.; Chopra, H.; Behzad, S.; Bansal, H.; Goyal, R.; Gautam, R.K.; Tsagkaris, C.; Joon, S.; Singla, S.; Shen, B. Natural products for the management of castration-resistant prostate cancer: Special focus on nanoparticles based studies. Front. Cell Dev. Biol., 2021, 9, 745177. doi: 10.3389/fcell.2021.745177 PMID: 34805155
  10. Patel, P.; Asdaq, S.M.B. Immunomodulatory activity of methanolic fruit extract of Aegle marmelos in experimental animals. Saudi Pharm. J., 2010, 18(3), 161-165. doi: 10.1016/j.jsps.2010.05.006 PMID: 23964175
  11. Neelam Balekar, S.B.; Mohan, V.; Prasad, A. Modulatory activity of a polyphenolic fraction of Cinnamomum zeylanicum L. bark on multiple arms of immunity in normal and immunocompromised mice. J. Appl. Pharm. Sci., 2014, 4(7), 114-122.
  12. Alhazmi, H.A.; Najmi, A.; Javed, S.A.; Sultana, S.; Al Bratty, M.; Makeen, H.A.; Meraya, A.M.; Ahsan, W.; Mohan, S.; Taha, M.M.E.; Khalid, A. Medicinal plants and isolated molecules demonstrating immunomodulation activity as potential alternative therapies for viral diseases including COVID-19. Front. Immunol., 2021, 12, 637553.
  13. Zebeaman, M.; Tadesse, M.G.; Bachheti, R.K.; Bachheti, A.; Gebeyhu, R.; Chaubey, K.K.; Li, M.H. Plants and plant-derived molecules as natural immunomodulators. BioMed Res. Int., 2023, 2023, 1-14. doi: 10.1155/2023/7711297 PMID: 37313550
  14. Satyavati, G.V.; Gupta, A.K.; Tandon, N.; Seth, S.D. Medicinal Plants of India; Indian Council of Medical Research, 1987, 2, p. 262.
  15. Morzelle, M.C.; Salgado, J.M.; Telles, M.; Mourelle, D.; Bachiega, P.; Buck, H.S.; Viel, T.A. Neuroprotective effects of pomegranate peel extract after chronic infusion with amyloid-β peptide in mice. PLoS One, 2016, 11(11), e0166123. doi: 10.1371/journal.pone.0166123 PMID: 27829013
  16. Venkatrao, N.; Koroth, S.M.; Satyanarayana, S.; Hemamalini, K.; Kumar, S.M.S. Antidiarrhoeal and anti-inflammatory activity of fruit rind extracts of Punica granatum. Indian Drugs, 2007, 44(12), 909-914.
  17. Das, S.; Singh, S.R.; Ahmed, S.; Kanodia, L. Analgesic and anti-inflammatory activities of ethanolic extract of leaves of Punica granatum L. on experimental animal models. Pharmacologyonline, 2011, 3, 379-385.
  18. Labsi, M.; Khelifi, L.; Mezioug, D.; Soufli, I.; Touil-Boukoffa, C. Antihydatic and immunomodulatory effects of Punica granatum peel aqueous extract in a murine model of echinococcosis. Asian Pac. J. Trop. Med., 2016, 9(3), 211-220. doi: 10.1016/j.apjtm.2016.01.038 PMID: 26972390
  19. Tiwari, P.; Kumar, B.; Kaur, M.; Kaur, G.; Kaur, H. Phytochemical screening and extraction: A review. Int. Pharm. Sci., 2011, 1(1), 98-106.
  20. Wang, J.; Rani, N.; Jakhar, S.; Redhu, R.; Kumar, S.; Kumar, S.; Kumar, S.; Devi, B.; Simal-Gandara, J.; Shen, B.; Singla, R.K. Opuntia ficus-indica (L.) Mill. - anticancer properties and phytochemicals: current trends and future perspectives. Front. Plant Sci., 2023, 14, 1236123. doi: 10.3389/fpls.2023.1236123
  21. Singla, R.K.; Singh, D.; Verma, R.; Kaushik, D.; Echeverría, J.; Garg, V.; Gupta, P.; Rahman, M.A.; Sharma, A.; Mittal, V.; Shen, B. Fermented formulation of silybum marianum seeds: Optimization, heavy metal analysis, and hepatoprotective assessment. Phytomedicine, 2023. PMID: 38241906
  22. Singla, R.K.; Zhang, Y.; Singla, S.; Shen, B. Bibliometric and temporal trend analysis of nipah virus- an emerging zoonotic disease: what do we know so far. bioRxiv, 2023. doi: 10.1101/2023.10.17.562837
  23. Hajiluian, G.; Karegar, S.J.; Shidfar, F.; Aryaeian, N.; Salehi, M.; Lotfi, T.; Farhangnia, P.; Heshmati, J.; Delbandi, A.A. The effects of Ellagic acid supplementation on neurotrophic, inflammation, and oxidative stress factors, and indoleamine 2, 3-dioxygenase gene expression in multiple sclerosis patients with mild to moderate depressive symptoms: A randomized, triple-blind, placebo-controlled trial. Phytomedicine, 2023, 121, 155094. doi: 10.1016/j.phymed.2023.155094 PMID: 37806153
  24. Ghadimi, M.; Foroughi, F.; Hashemipour, S.; Nooshabadi, R.M.; Ahmadi, M.H.; Ahadi Nezhad, B.; Khadem Haghighian, H. Randomized double-blind clinical trial examining the Ellagic acid effects on glycemic status, insulin resistance, antioxidant, and inflammatory factors in patients with type 2 diabetes. Phytother. Res., 2021, 35(2), 1023-1032. doi: 10.1002/ptr.6867 PMID: 32909365
  25. Barghchi, H.; Milkarizi, N.; Belyani, S.; Norouzian Ostad, A.; Askari, V.R.; Rajabzadeh, F.; Goshayeshi, L.; Ghelichi Kheyrabadi, S.Y.; Razavidarmian, M.; Dehnavi, Z.; Sobhani, S.R.; Nematy, M. Pomegranate (Punica granatum L.) peel extract ameliorates metabolic syndrome risk factors in patients with non-alcoholic fatty liver disease: A randomized double-blind clinical trial. Nutr. J., 2023, 22(1), 40. doi: 10.1186/s12937-023-00869-2 PMID: 37605174
  26. Gautam, R.K.; Gupta, G.; Sharma, S.; Hatware, K.; Patil, K.; Sharma, K.; Goyal, S.; Chellappan, D.K.; Dua, K. Rosmarinic acid attenuates inflammation in experimentally induced arthritis in Wistar rats, using Freund’s complete adjuvant. Int. J. Rheum. Dis., 2019, 22(7), 1247-1254. doi: 10.1111/1756-185X.13602 PMID: 31155849
  27. Kokate, C.K.; Purohit, A.P.; Gohkale, S.B. Pharmacognosy, 21 ed.; Nirali Prakashan: Pune, India, Med. J., 2002, 43(2), pp. 007-085.
  28. Yadav, R.; Agarwala, M. Phytochemical analysis of some medicinal plants. J. Phytol., 2011, 3(12), 10-14.
  29. Gautam, R.K.; Sharma, S.; Sharma, K. Comparative evaluation of anti-arthritic activity of Salvadora persica linn. and Asparagus racemosus willd: an in-vitro study. IAJPR, 2013, 3(10), 8222-8227.
  30. Wilkinson, P. Neutrophil adhesion test. In: In Handbook of experimental pharmacology, I, 1st ed.; Springer: Berlin, 1978; p. 109.
  31. Choudhary, M.; Kumar, V.; Malhotra, H.; Singh, S. Medicinal plants with potential anti-arthritic activity. J. Intercult. Ethnopharmacol., 2015, 4(2), 147-179. doi: 10.5455/jice.20150313021918 PMID: 26401403
  32. Rajput, K.; Dubey, R.C.; Kumar, A. Probiotic potential and immunomodulatory properties in Enterococcus faecium GMB24 and Enterococcus hirae SMB16 isolated from goat and sheep milk. Arch. Microbiol., 2022, 204(10), 619. doi: 10.1007/s00203-022-03217-w PMID: 36098848
  33. Kumar, H.; Vasudeva, N. Immunomodulatory potential of Nyctanthes abrortristis stem bark. J. Ayurveda Integr. Med., 2022, 13(2), 100556. doi: 10.1016/j.jaim.2022.100556 PMID: 35653920
  34. Shen, X.; Zeng, Y.; Li, J.; Tang, C.; Zhang, Y.; Meng, X. The anti-arthritic activity of total glycosides from Pterocephalus hookeri, a traditional Tibetan herbal medicine. Pharm. Biol., 2017, 55(1), 560-570. doi: 10.1080/13880209.2016.1263869 PMID: 27937009
  35. Upadhyay, R.K. Anti-arthritic potential of plant natural products; its use in joint pain medications and anti-inflammatory drug formulations. Int. J. Green. Pharm., 2016, 10(3), S120-S130.
  36. Muthuraman, A.; Sood, S.; Singla, S.K. The antiinflammatory potential of phenolic compounds from Emblica officinalis L. in rat. Inflammopharmacology, 2011, 19(6), 327-334. doi: 10.1007/s10787-010-0041-9 PMID: 20596897
  37. Cheng, W.; Li, J.; You, T.; Hu, C. Anti-inflammatory and immunomodulatory activities of the extracts from the inflorescence of Chrysanthemum indicum Linné. J. Ethnopharmacol., 2005, 101(1-3), 334-337. doi: 10.1016/j.jep.2005.04.035 PMID: 16029939
  38. Shukla, S.; Mehta, A.; John, J.; Mehta, P.; Vyas, S.P.; Shukla, S. Immunomodulatory activities of the ethanolic extract of Caesalpinia bonducella seeds. J. Ethnopharmacol., 2009, 125(2), 252-256. doi: 10.1016/j.jep.2009.07.002 PMID: 19607900
  39. Anonymous Schrödinger Release. 2023. Available from: https://www.schrodinger.com/citations#LigPrep
  40. Jorgensen, W.L.; Tirado-Rives, J. The OPLS optimized potentials for liquid simulations potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin. J. Am. Chem. Soc., 1988, 110(6), 1657-1666. doi: 10.1021/ja00214a001 PMID: 27557051
  41. Anonymous Schrödinger Release. Available from: https://www.schrodinger.com/citations#Epik
  42. Lopez-Girona, A.; Mendy, D.; Ito, T.; Miller, K.; Gandhi, A.K.; Kang, J.; Karasawa, S.; Carmel, G.; Jackson, P.; Abbasian, M.; Mahmoudi, A.; Cathers, B.; Rychak, E.; Gaidarova, S.; Chen, R.; Schafer, P.H.; Handa, H.; Daniel, T.O.; Evans, J.F.; Chopra, R. Cereblon is a direct protein target for immunomodulatory and antiproliferative activities of lenalidomide and pomalidomide. Leukemia, 2012, 26(11), 2326-2335. doi: 10.1038/leu.2012.119 PMID: 22552008
  43. Carrancio, S.; Groocock, L.; Janardhanan, P.; Jankeel, D.; Galasso, R.; Guarinos, C.; Narla, R.K.; Groza, M.; Leisten, J.; Pierce, D.W.; Rolfe, M.; Lopez-Girona, A. CC-99282 is a novel cereblon (CRBN) E3 Ligase Modulator (CELMoD) agent with enhanced tumoricidal activity in preclinical models of lymphoma. Blood, 2021, 138(S1), 1200-1200. doi: 10.1182/blood-2021-148068
  44. Moon, H.; Min, C.; Kim, G.; Kim, D.; Kim, K.; Lee, S.A.; Moon, B.; Yang, S.; Lee, J.; Yang, S.J.; Cho, S.K.; Lee, G.; Lee, C.S.; Park, C.S.; Park, D. Crbn modulates calcium influx by regulating Orai1 during efferocytosis. Nat. Commun., 2020, 11(1), 5489. doi: 10.1038/s41467-020-19272-0 PMID: 33127885
  45. Pluvinage, J.V.; Haney, M.S.; Smith, B.A.H.; Sun, J.; Iram, T.; Bonanno, L.; Li, L.; Lee, D.P.; Morgens, D.W.; Yang, A.C.; Shuken, S.R.; Gate, D.; Scott, M.; Khatri, P.; Luo, J.; Bertozzi, C.R.; Bassik, M.C.; Wyss-Coray, T. CD22 blockade restores homeostatic microglial phagocytosis in ageing brains. Nature, 2019, 568(7751), 187-192. doi: 10.1038/s41586-019-1088-4 PMID: 30944478
  46. Aires, V.; Coulon-Bainier, C.; Pavlovic, A.; Ebeling, M.; Schmucki, R.; Schweitzer, C.; Kueng, E.; Gutbier, S.; Harde, E. CD22 blockage restores age-related impairments of microglia surveillance capacity. Front. Immunol., 2021, 12, 684430. doi: 10.3389/fimmu.2021.684430 PMID: 34140954
  47. Rossi, E.A.; Goldenberg, D.M.; Michel, R.; Rossi, D.L.; Wallace, D.J.; Chang, C.H. Trogocytosis of multiple B- cell surface markers by CD22 targeting with epratuzumab. Blood, 2013, 122(17), 3020-3029. doi: 10.1182/blood-2012-12-473744 PMID: 23821660
  48. Enterina, J.R.; Jung, J.; Macauley, M.S. Coordinated roles for glycans in regulating the inhibitory function of CD22 on B cells. Biomed. J., 2019, 42(4), 218-232. doi: 10.1016/j.bj.2019.07.010 PMID: 31627864
  49. Krasavin, M.; Adamchik, M.; Bubyrev, A.; Heim, C.; Maiwald, S.; Zhukovsky, D.; Zhmurov, P.; Bunev, A.; Hartmann, M.D. Synthesis of novel glutarimide ligands for the E3 ligase substrate receptor Cereblon (CRBN): Investigation of their binding mode and antiproliferative effects against myeloma cell lines. Eur. J. Med. Chem., 2023, 246, 114990. doi: 10.1016/j.ejmech.2022.114990 PMID: 36476642
  50. Ereño-Orbea, J.; Sicard, T.; Cui, H.; Mazhab-Jafari, M.T.; Benlekbir, S.; Guarné, A.; Rubinstein, J.L.; Julien, J.P. Molecular basis of human CD22 function and therapeutic targeting. Nat. Commun., 2017, 8(1), 764. doi: 10.1038/s41467-017-00836-6 PMID: 28970495
  51. Madhavi Sastry, G.; Adzhigirey, M.; Day, T.; Annabhimoju, R.; Sherman, W. Protein and ligand preparation: Parameters, protocols, and influence on virtual screening enrichments. J. Comput. Aided Mol. Des., 2013, 27(3), 221-234. doi: 10.1007/s10822-013-9644-8 PMID: 23579614
  52. Friesner, R.A.; Banks, J.L.; Murphy, R.B.; Halgren, T.A.; Klicic, J.J.; Mainz, D.T.; Repasky, M.P.; Knoll, E.H.; Shelley, M.; Perry, J.K.; Shaw, D.E.; Francis, P.; Shenkin, P.S. Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J. Med. Chem., 2004, 47(7), 1739-1749. doi: 10.1021/jm0306430 PMID: 15027865
  53. Raj, P.; Selvam, K.; Roy, K.; Mani Tripathi, S.; Kesharwani, S.; Gopal, B.; Varshney, U.; Sundriyal, S. Identification of a new and diverse set of Mycobacterium tuberculosis uracil-DNA glycosylase (MtUng) inhibitors using structure-based virtual screening: Experimental validation and molecular dynamics studies. Bioorg. Med. Chem. Lett., 2022, 76, 129008. doi: 10.1016/j.bmcl.2022.129008 PMID: 36174837
  54. Van Der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A.E.; Berendsen, H.J.C. GROMACS: Fast, flexible, and free. J. Comput. Chem., 2005, 26(16), 1701-1718. doi: 10.1002/jcc.20291 PMID: 16211538
  55. Vanommeslaeghe, K.; MacKerell, A.D., Jr. Automation of the CHARMM General Force Field (CGenFF) I: Bond perception and atom typing. J. Chem. Inf. Model., 2012, 52(12), 3144-3154. doi: 10.1021/ci300363c PMID: 23146088
  56. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph., 1996, 14(1), 33-38, 27-28. doi: 10.1016/0263-7855(96)00018-5 PMID: 8744570
  57. Schiffrin, B.; Radford, S.E.; Brockwell, D.J.; Calabrese, A.N. PYXLINKVIEWER : A flexible tool for visualization of protein chemical crosslinking data within the PYMOL molecular graphics system. Protein Sci., 2020, 29(8), 1851-1857. doi: 10.1002/pro.3902 PMID: 32557917
  58. Tripathi, S.M.; Akash, S.; Rahman, M.A.; Sundriyal, S. Identification of synthetically tractable MERS-CoV main protease inhibitors using structure-based virtual screening and molecular dynamics potential of mean force (PMF) calculations. J. Biomol. Struct. Dyn., 2023, 1-11. doi: 10.1080/07391102.2023.2283780 PMID: 37978909
  59. Kumari, R.; Kumar, R.; Lynn, A. g_mmpbsa--a GROMACS tool for high-throughput MM-PBSA calculations. J. Chem. Inf. Model., 2014, 54(7), 1951-1962. doi: 10.1021/ci500020m PMID: 24850022
  60. Daina, A.; Michielin, O.; Zoete, V. SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci. Rep., 2017, 7(1), 42717. doi: 10.1038/srep42717 PMID: 28256516
  61. Banerjee, P.; Eckert, A.O.; Schrey, A.K.; Preissner, R. ProTox-II: A webserver for the prediction of toxicity of chemicals. Nucleic Acids Res., 2018, 46(W1), W257-W263. doi: 10.1093/nar/gky318 PMID: 29718510
  62. Ambriz-Perez, D.L.; Leyva-Lopez, N.; Gutierrez-Grijalva, E.P.; Heredia, J.B.; Yildiz, F. Phenolic compounds: Natural alternative in inflammation treatment. A Review. Cogent Food Agric., 2016, 2(1), 1131412.
  63. do Nascimento, R.F.; de Oliveira Formiga, R.; Machado, F.D.F.; de Sales, I.R.P.; de Lima, G.M.; Alves Júnior, E.B.; Vieira, G.C.; Pereira, R.F.; de Araújo, A.A.; de Araújo Junior, R.F.; Barbosa Filho, J.M.; Batista, L.M. Rosmarinic acid prevents gastric ulcers via sulfhydryl groups reinforcement, antioxidant and immunomodulatory effects. Naunyn Schmiedebergs Arch. Pharmacol., 2020, 393(12), 2265-2278. doi: 10.1007/s00210-020-01894-2 PMID: 32642876
  64. Wang, E.; Sun, H.; Wang, J.; Wang, Z.; Liu, H.; Zhang, J.Z.H.; Hou, T. End-point binding free energy calculation with MM/PBSA and MM/GBSA: Strategies and applications in drug design. Chem. Rev., 2019, 119(16), 9478-9508. doi: 10.1021/acs.chemrev.9b00055 PMID: 31244000
  65. Genheden, S.; Ryde, U. The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opin. Drug Discov., 2015, 10(5), 449-461. doi: 10.1517/17460441.2015.1032936 PMID: 25835573
  66. Lataliza, A.A.B.; de Assis, P.M.; da Rocha Laurindo, L.; Gonçalves, E.C.D.; Raposo, N.R.B.; Dutra, R.C. Antidepressant-like effect of rosmarinic acid during LPS -induced neuroinflammatory model: The potential role of cannabinoid receptors/ PPAR -γ signaling pathway. Phytother. Res., 2021, 35(12), 6974-6989. doi: 10.1002/ptr.7318 PMID: 34709695
  67. Hitl, M.; Kladar, N.; Gavarić, N.; Božin, B. Rosmarinic acid-human pharmacokinetics and health benefits. Planta Med., 2021, 87(4), 273-282. doi: 10.1055/a-1301-8648 PMID: 33285594
  68. Kim, S.B.; Kim, K.S.; Kim, D.D.; Yoon, I.S. Metabolic interactions of rosmarinic acid with human cytochrome P450 monooxygenases and uridine diphosphate glucuronosyltransferases. Biomed. Pharmacother., 2019, 110, 111-117. doi: 10.1016/j.biopha.2018.11.040 PMID: 30466000
  69. Yao, Y.; Li, R.; Liu, D.; Long, L.; He, N. Rosmarinic acid alleviates acetaminophen-induced hepatotoxicity by targeting Nrf2 and NEK7-NLRP3 signaling pathway. Ecotoxicol. Environ. Saf., 2022, 241, 113773. doi: 10.1016/j.ecoenv.2022.113773 PMID: 35753269
  70. Yu, Y.; Wu, Y.; Yan, H.; Xia, Z.; Wen, W.; Liu, D.; Wan, L. Rosmarinic acid ameliorates acetaminophen-induced acute liver injury in mice via RACK1/TNF-α mediated antioxidant effect. Pharm. Biol., 2021, 59(1), 1284-1291. doi: 10.1080/13880209.2021.1974059 PMID: 34517734
  71. Ahmadvand, H.; Jafaripour, L.; Naserzadeh, R.; Alizamani, E.; Javad Mashhadi, S.M.; Moghadam, E.R.; Nouryazdan, N. Effects of rosmarinic acid on methotrexate-induced nephrotoxicity and hepatotoxicity in wistar rats. Indian J. Nephrol., 2021, 31(3), 218-224. doi: 10.4103/ijn.IJN_14_20 PMID: 34376933
  72. Elufioye, T.O.; Habtemariam, S. Hepatoprotective effects of rosmarinic acid: Insight into its mechanisms of action. Biomed. Pharmacother., 2019, 112, 108600. doi: 10.1016/j.biopha.2019.108600 PMID: 30780110
  73. Renzulli, C.; Galvano, F.; Pierdomenico, L.; Speroni, E.; Guerra, M.C. Effects of rosmarinic acid against aflatoxin B 1 and ochratoxin-A-induced cell damage in a human hepatoma cell line (Hep G2). J. Appl. Toxicol., 2004, 24(4), 289-296. doi: 10.1002/jat.982 PMID: 15300717
  74. Furtado, M.A.; de Almeida, L.C.F.; Furtado, R.A.; Cunha, W.R.; Tavares, D.C. Antimutagenicity of rosmarinic acid in Swiss mice evaluated by the micronucleus assay. Mutat. Res. Genet. Toxicol. Environ. Mutagen., 2008, 657(2), 150-154. doi: 10.1016/j.mrgentox.2008.09.003 PMID: 18926924
  75. Han, J.; Wang, D.; Ye, L.; Li, P.; Hao, W.; Chen, X.; Ma, J.; Wang, B.; Shang, J.; Li, D.; Zheng, Q. Rosmarinic acid protects against inflammation and cardiomyocyte apoptosis during myocardial ischemia/reperfusion injury by activating peroxisome proliferator-activated receptor gamma. Front. Pharmacol., 2017, 8, 456. doi: 10.3389/fphar.2017.00456 PMID: 28744220
  76. Chen, C.; Ma, J.; Xu, Z.; Chen, L.; Sun, B.; Shi, Y.; Miao, Y.; Wu, T.; Qin, M.; Zhang, Y.; Zhang, M.; Cao, X. Rosmarinic acid inhibits platelet aggregation and neointimal hyperplasia in vivo and vascular smooth muscle cell dedifferentiation, proliferation, and migration in vitro via activation of the keap1-Nrf2-ARE antioxidant system. J. Agric. Food Chem., 2022, 70(24), 7420-7440. doi: 10.1021/acs.jafc.2c01176 PMID: 35687823
  77. Fetoni, A.R.; Paciello, F.; Rolesi, R.; Eramo, S.L.M.; Mancuso, C.; Troiani, D.; Paludetti, G. Rosmarinic acid up-regulates the noise-activated Nrf2/HO-1 pathway and protects against noise-induced injury in rat cochlea. Free Radic. Biol. Med., 2015, 85, 269-281. doi: 10.1016/j.freeradbiomed.2015.04.021 PMID: 25936352
  78. Deepti, B.; Suyog, G.; Beautikuma, S.; Ankita, P. Tannin rich fraction of Punica granatum linn. leaves ameliorates freund’s adjuvant induced arthritis in experimental animals. Pharmacologia, 2014, 5(1), 19-31. doi: 10.5567/pharmacologia.2014.19.31
  79. Petersen, M.; Simmonds, M.S.J. Rosmarinic acid. Phytochemistry, 2003, 62(2), 121-125. doi: 10.1016/S0031-9422(02)00513-7 PMID: 12482446
  80. Boonyarikpunchai, W.; Sukrong, S.; Towiwat, P. Antinociceptive and anti-inflammatory effects of rosmarinic acid isolated from Thunbergia laurifolia Lindl. Pharmacol. Biochem. Behav., 2014, 124, 67-73. doi: 10.1016/j.pbb.2014.05.004 PMID: 24836183
  81. Ellis, B.E.; Towers, G.H.N. Biogenesis of rosmarinic acid in Mentha. Biochem. J., 1970, 118(2), 291-297. doi: 10.1042/bj1180291 PMID: 5484678
  82. Weitzel, C.; Petersen, M. Cloning and characterisation of rosmarinic acid synthase from Melissa officinalis L. Phytochemistry, 2011, 72(7), 572-578. doi: 10.1016/j.phytochem.2011.01.039 PMID: 21354582
  83. Fasolo, J.M.M.A.; Vizuete, A.F.K.; Rico, E.P.; Rambo, R.B.S.; Toson, N.S.B.; Santos, E.; de Oliveira, D.L.; Gonçalves, C.A.S.; Schapoval, E.E.S.; Heriques, A.T. Anti-inflammatory effect of rosmarinic acid isolated from Blechnum brasiliense in adult zebrafish brain. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2021, 239, 108874. doi: 10.1016/j.cbpc.2020.108874 PMID: 32805443
  84. Lin, L.; Dong, Y.; Zhao, H.; Wen, L.; Yang, B.; Zhao, M. Comparative evaluation of rosmarinic acid, methyl rosmarinate and pedalitin isolated from Rabdosia serra (MAXIM.) HARA as inhibitors of tyrosinase and α-glucosidase. Food Chem., 2011, 129(3), 884-889. doi: 10.1016/j.foodchem.2011.05.039 PMID: 25212314
  85. Ulbrich, B.; Wiesner, W.; Arens, H. Large-scale production of rosmarinic acid from plant cell cultures of Coleus blumei benth. In: Primary and Secondary Metabolism of Plant Cell Cultures; Springer, 1985; pp. 293-303. doi: 10.1007/978-3-642-70717-9_28
  86. Zou, Z.W.; Xu, L.N.; Tian, J.Y. Antithrombotic and antiplatelet effects of rosmarinic acid, a water-soluble component isolated from radix Salviae miltiorrhizae (danshen). Yao Xue Xue Bao, 1993, 28(4), 241-245. PMID: 8213164
  87. Nakamura, Y.; Ohto, Y.; Murakami, A.; Ohigashi, H. Superoxide scavenging activity of rosmarinic acid from Perilla frutescens Britton Var. acuta f. viridis. J. Agric. Food Chem., 1998, 46(11), 4545-4550. doi: 10.1021/jf980557m
  88. Gohari, A.R.; Saeidnia, S.; Malmir, M.; Hadjiakhoondi, A.; Ajani, Y. Flavones and rosmarinic acid from Salvia limbata. Nat. Prod. Res., 2010, 24(20), 1902-1906. doi: 10.1080/14786411003766912 PMID: 21108116
  89. Gamaro, G.D.; Suyenaga, E.; Borsoi, M.; Lermen, J.; Pereira, P.; Ardenghi, P. Effect of rosmarinic and caffeic acids on inflammatory and nociception process in rats. ISRN Pharmacol., 2011, 2011, 1-6. doi: 10.5402/2011/451682 PMID: 22084714
  90. Costa, R.S.; Carneiro, T.C.B.; Cerqueira-Lima, A.T.; Queiroz, N.V.; Alcântara-Neves, N.M.; Pontes-de-Carvalho, L.C.; Velozo, E.S.; Oliveira, E.J.; Figueiredo, C.A. Ocimum gratissimum Linn. and rosmarinic acid, attenuate eosinophilic airway inflammation in an experimental model of respiratory allergy to Blomia tropicalis. Int. Immunopharmacol., 2012, 13(1), 126-134. doi: 10.1016/j.intimp.2012.03.012 PMID: 22465960
  91. Luo, C.; Zou, L.; Sun, H.; Peng, J.; Gao, C.; Bao, L.; Ji, R.; Jin, Y.; Sun, S. A review of the anti-inflammatory effects of rosmarinic acid on inflammatory diseases. Front. Pharmacol., 2020, 11, 153. doi: 10.3389/fphar.2020.00153 PMID: 32184728
  92. Zhao, L.; Zhang, Y.; Liu, G.; Hao, S.; Wang, C.; Wang, Y. Black rice anthocyanin-rich extract and rosmarinic acid, alone and in combination, protect against DSS-induced colitis in mice. Food Funct., 2018, 9(5), 2796-2808. doi: 10.1039/C7FO01490B PMID: 29691532
  93. Shakeri, F.; Eftekhar, N.; Roshan, N.M.; Rezaee, R.; Moghimi, A.; Boskabady, M.H. Rosmarinic acid affects immunological and inflammatory mediator levels and restores lung pathological features in asthmatic rats. Allergol. Immunopathol., 2019, 47(1), 16-23. doi: 10.1016/j.aller.2018.04.004 PMID: 29983238
  94. Kraus, R.F.; Gruber, M.A. Neutrophils-from bone marrow to first-line defense of the innate immune system. Front. Immunol., 2021, 12, 767175. doi: 10.3389/fimmu.2021.767175 PMID: 35003081
  95. Singh, R.; Sharma, P.; Wadhwan, V. Neutrophils defending the defenders. J. Oral Maxillofac. Pathol., 2021, 25(1), 177-182. doi: 10.4103/jomfp.jomfp_495_20 PMID: 34349432
  96. Bhattacharjee, S.; Ghosh, D.; Saha, R.; Sarkar, R.; Kumar, S.; Khokhar, M.; Pandey, R.K. Mechanism of immune evasion in mosquito-borne diseases. Pathogens, 2023, 12(5), 635. doi: 10.3390/pathogens12050635 PMID: 37242305

Қосымша файлдар

Қосымша файлдар
Әрекет
1. JATS XML
Жүктеу

© Bentham Science Publishers, 2024