168
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Potential of Onchocerca ochengi inosine-5′-monophosphate dehydrogenase (IMPDH) and guanosine-5′-monophosphate oxidoreductase (GMPR) as druggable and vaccine candidates: immunoinformatics screening

ORCID Icon, ORCID Icon, ORCID Icon, , ORCID Icon, , ORCID Icon & show all
Pages 14832-14848 | Received 29 Aug 2022, Accepted 18 Feb 2023, Published online: 03 Mar 2023

References

  • Achukwi, M. D., Harnett, W., Enyong, P., & Renz, A. (2007). Successful vaccination against Onchocerca ochengi infestation in cattle using live Onchocerca volvulus infective larvae. Parasite Immunology, 29(3), 113–116. https://doi.org/10.1111/j.1365-3024.2006.00917.x
  • Allen, J. E., Adjei, O., Bain, O., Hoerauf, A., Hoffmann, W. H., Makepeace, B. L., Schulz-Key, H., Tanya, V. N., Trees, A. J., Wanji, S., & Taylor, D. W. (2008). Of mice, cattle, and humans: The immunology and treatment of river blindness. PLoS Neglected Tropical Diseases, 2(4), e217. https://doi.org/10.1371/journal.pntd.0000217
  • Arndts, K., Specht, S., Debrah, A. Y., Tamarozzi, F., Klarmann Schulz, U., Mand, S., Batsa, L., Kwarteng, A., Taylor, M., Adjei, O., Martin, C., Layland, L. E., & Hoerauf, A. (2014). Immunoepidemiological profiling of onchocerciasis patients reveals associations with microfilaria loads and Ivermectin intake on both individual and community levels. PLoS Neglected Tropical Diseases, 8(2), e2679. https://doi.org/10.1371/journal.pntd.0002679
  • Bertoni, M., Kiefer, F., Biasini, M., Bordoli, L., & Schwede, T. (2017). Modeling protein quaternary structure of homo- and hetero-oligomers beyond binary interactions by homology. Scientific Reports, 7(1), 1-15. https://doi.org/10.1038/s41598-017-09654-8
  • Bessho, T., Okada, T., Kimura, C., Shinohara, T., Tomiyama, A., Imamura, A., Kuwamura, M., Nishimura, K., Fujimori, K., Shuto, S., Ishibashi, O., Kubata, B. K., & Inui, T. (2016). Novel characteristics of trypanosoma brucei guanosine 5'-monophosphate reductase distinct from host animals. PLOS Neglected Tropical Diseases, 10(1), e0004339. https://doi.org/10.1371/journal.pntd.0004339
  • Boitz, J. M., Jardim, A., & Ullman, B. (2016). GMP reductase and genetic uncoupling of adenylate and guanylate metabolism in leishmania donovani parasites. Molecular and Biochemical Parasitology, 208(2), 74–83. https://doi.org/10.1016/j.molbiopara.2016.06.008
  • Boussinesq, M., Gardon, J., Gardon-Wendel, N., & Chippaux, J. P. (2003). Clinical picture, epidemiology and outcome of Loa-associated serious adverse events related to mass ivermectin treatment of onchocerciasis in Cameroon. Filaria Journal, 2(Suppl 1), S4. https://doi.org/10.1186/1475-2883-2-S1-S4
  • Castiglione, F., Deb, D., Srivastava, A. P., Liò, P., & Liso, A. (2021). From infection to immunity: Understanding the response to SARS-CoV2 through in-silico modeling. Frontiers in Immunology, 12, 646972. https://doi.org/10.3389/fimmu.2021.646972
  • Chesnais, C. B., Pion, S. D., Boullé, C., Gardon, J., Gardon-Wendel, N., Fokom-Domgue, J., Kamgno, J., & Boussinesq, M. (2020). Individual risk of post-ivermectin serious adverse events in subjects infected with Loa loa. EClinicalMedicine, 28, 100582. https://doi.org/10.1016/j.eclinm.2020.100582
  • Choudhury, A., Sen Gupta, P. S., Panda, S. K., Rana, M. K., & Mukherjee, S. (2022). Designing AbhiSCoVac - A single potential vaccine for all “corona culprits”: Immunoinformatics and immune simulation approaches. Journal of Molecular Liquids, 351, 118633. https://doi.org/10.1016/j.molliq.2022.118633
  • Combet, C., Blanchet, C., Geourjon, C., & Deléage, G. (2000). NPS@: Network protein sequence analysis. Trends in Biochemical Sciences, 25(3), 147–150. https://doi.org/10.1016/s0968-0004(99)01540-6
  • Cuny, G. D., Suebsuwong, C., & Ray, S. S. (2017). Inosine-5’-monophosphate dehydrogenase (IMPDH) inhibitors: A patent and scientific literature review (2002-2016). Expert Opinion on Therapeutic Patents, 27(6), 677–690. https://doi.org/10.1080/13543776.2017.1280463
  • Das, N. C., Patra, R., Gupta, P. S. S., Ghosh, P., Bhattacharya, M., Rana, M. K., & Mukherjee, S. (2021). Designing of a novel multi-epitope peptide based vaccine against Brugia malayi: An in silico approach. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 87, 104633. https://doi.org/10.1016/j.meegid.2020.104633
  • Das, N. C., Ray, A. S., Bayry, J., & Mukherjeee, S. (2021). Therapeutic efficacy of anti-bestrophin antibodies against experimental filariasis: Immunological, immune-informatics and immune simulation investigations. Antibodies (Basel, Switzerland), 10(2), 14. https://doi.org/10.3390/antib10020014
  • Dhanda, S. K., Gupta, S., Vir, P., & Raghava, G. P. (2013a). Prediction of IL4 inducing peptides. Clinical & Developmental Immunology, 2013, 263952–263959. https://doi.org/10.1155/2013/263952
  • Dhanda, S. K., Vir, P., & Raghava, G. P. (2013b). Designing of interferon-gamma inducing MHC class-II binders. Biology Direct, 8(1), 1-15. https://doi.org/10.1186/1745-6150-8-30
  • Dimitrov, I., Bangov, I., Flower, D. R., & Doytchinova, I. (2014). AllerTOP v.2–a server for in silico prediction of allergens. Journal of Molecular Modeling, 20(6), 2278. https://doi.org/10.1007/s00894-014-2278-5
  • Doyle, S. R., Armoo, S., Renz, A., Taylor, M. J., Osei-Atweneboana, M. Y., & Grant, W. N. (2016). Discrimination between Onchocerca volvulus and O. ochengi filarial larvae in Simulium damnosum (s.l.) and their distribution throughout central Ghana using a versatile high-resolution speciation assay. Parasites & Vectors, 9(1), 1-8. https://doi.org/10.1186/s13071-016-1832-7
  • Doytchinova, I. A., & Flower, D. R. (2007). VaxiJen: A server for prediction of protective antigens, tumour antigens and subunit vaccines. BMC Bioinformatics, 8(1), 4. https://doi.org/10.1186/1471-2105-8-4
  • Forrer, A., Wanji, S., Obie, E. D., Nji, T. M., Hamill, L., Ozano, K., Piotrowski, H., Dean, L., Njouendou, A. J., Ekanya, R., Ndongmo, W. P. C., Fung, E. G., Nnamdi, D.-B., Abong, R. A., Beng, A. A., Eyong, M. E., Ndzeshang, B. L., Nkimbeng, D. A., Teghen, S., … Taylor, M. J. (2021). Why onchocerciasis transmission persists after 15 annual ivermectin mass drug administrations in South-West Cameroon. BMJ Global Health, 6(1), e003248. https://doi.org/10.1136/bmjgh-2020-003248
  • Frallonardo, L., Di Gennaro, F., Panico, G. G., Novara, R., Pallara, E., Cotugno, S., Guido, G., De Vita, E., Ricciardi, A., Totaro, V., Camporeale, M., De Iaco, G., Bavaro, D. F., Lattanzio, R., Patti, G., Brindicci, G., Papagni, R., Pellegrino, C., Santoro, C. R., … Saracino, A. (2022). Onchocerciasis: Current knowledge and future goals. Frontiers in Tropical Diseases, 3, 986884. https://doi.org/10.3389/fitd.2022.986884
  • Gaiya, D. D., Jonathan, B., Udu, S. K., & Hassan, G. (2021). Possible recrudescence of onchocerciasis within Kaduna metropolis: microfilariae load and transmission potential posed by blackfly. Dysona - Life Science, 2, 33–38. https://doi.org/10.30493/DLS.2021.284623
  • Gorai, S., Das, N. C., Gupta, P. S. S., Panda, S. K., Rana, M. K., & Mukherjee, S. (2022). Designing efficient multi-epitope peptide-based vaccine by targeting the antioxidant thioredoxin of bancroftian filarial parasite. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 98, 105237. https://doi.org/10.1016/j.meegid.2022.105237
  • Guedes, R. L., Rodrigues, C. M., Coatnoan, N., Cosson, A., Cadioli, F. A., Garcia, H. A., Gerber, A. L., Machado, R. Z., Minoprio, P. M., Teixeira, M. M., & De Vasconcelos, A. T. (2019). A comparative in silico linear B-cell epitope prediction and characterization for south American and African trypanosoma vivax strains. Genomics, 111(3), 407–417. https://doi.org/10.1016/j.ygeno.2018.02.017
  • Hedstrom, L. (2012). The dynamic determinants of reaction specificity in the IMPDH/GMPR family of (β/α)8barrel enzymes. Critical Reviews in Biochemistry and Molecular Biology, 47(3), 250–263. https://doi.org/10.3109/10409238.2012.656843
  • Heo, L., Park, H., & Seok, C. (2013). GalaxyRefine: Protein structure refinement driven by side-chain repacking. Nucleic Acids Research, 41(Web Server issue), W384–8. https://doi.org/10.1093/nar/gkt458
  • Hess, J. A., Zhan, B., Bonne-Année, S., Deckman, J. M., Bottazzi, M. E., Hotez, P. J., Klei, T. R., Lustigman, S., & Abraham, D. (2014). Vaccines to combat river blindness: Expression, selection and formulation of vaccines against infection with Onchocerca volvulus in a mouse model. International Journal for Parasitology, 44(9), 637–646. https://doi.org/10.1016/j.ijpara.2014.04.006
  • Hildebrandt, J. C., Eisenbarth, A., Renz, A., & Streit, A. (2014). Reproductive biology of Onchocerca ochengi, a nodule forming filarial nematode in zebu cattle. Veterinary Parasitology, 205(1-2), 318–329. https://doi.org/10.1016/j.vetpar.2014.06.006
  • Jaleta, T. G., Rödelsperger, C., Abanda, B., Eisenbarth, A., Achukwi, M. D., Renz, A., & Streit, A. (2018). Full mitochondrial and nuclear genome comparison confirms that Onchocerca sp. “Siisa” is Onchocerca ochengi. Parasitology Research, 117(4), 1069–1077. https://doi.org/10.1007/s00436-018-5783-0
  • Jensen, K. K., Andreatta, M., Marcatili, P., Buus, S., Greenbaum, J. A., Yan, Z., Sette, A., Peters, B., & Nielsen, M. (2018). Improved methods for predicting peptide binding affinity to MHC class II molecules. Immunology, 154(3), 394–406. https://doi.org/10.1111/imm.12889
  • Lagatie, O., Verheyen, A., van Dorst, B., Batsa Debrah, L., Debrah, A., & Stuyver, L. J. (2018). Linear epitopes in Onchocerca volvulus vaccine candidate proteins and excretory-secretory proteins. Parasite Immunology, 40(11), e12587. https://doi.org/10.1111/pim.12587
  • Lee, G. R., Heo, L., & Seok, C. (2016). Effective protein model structure refinement by loop modeling and overall relaxation: Refinement with Loop Modeling and MD Relaxation. Proteins: Structure, Function, and Bioinformatics, 84, 293–301. https://doi.org/10.1002/prot.24858
  • Lustigman, S., Makepeace, B. L., Klei, T. R., Babayan, S. A., Hotez, P., Abraham, D., & Bottazzi, M. E. (2018). Onchocerca volvulus: The road from basic biology to a vaccine. Trends in Parasitology, 34(1), 64–79. https://doi.org/10.1016/j.pt.2017.08.011
  • Luu, L., Bah, G. S., Okah-Nnane, N. H., Hartley, C. S., Glover, A. F., Walsh, T. R., Lian, L.-Y., Zhan, B., Bottazzi, M. E., Abraham, D., Petrovsky, N., Bayang, N., Tangwa, B., Ayiseh, R. B., Mbah, G. E., Ekale, D. D., Tanya, V. N., Lustigman, S., Makepeace, B. L., & Graham-Brown, J. (2022). Co-administration of adjuvanted recombinant Ov-103 and Ov-RAL-2 vaccines confer protection against natural challenge in A bovine Onchocerca ochengi infection model of human onchocerciasis. Vaccines, 10(6), 861. https://doi.org/10.3390/vaccines10060861
  • Mahmud, S. N., Rahman, M., Kar, A., Jahan, N., & Khan, A. (2020). Designing of an epitope- Based universal peptide vaccine against highly conserved regions in RNA dependent RNA polymerase protein of human Marburg virus: A computational assay. Anti-Infective Agents, 18(3), 294–305. https://doi.org/10.2174/2211352517666190717143949
  • Makepeace, B. L., Jensen, S. A., Laney, S. J., Nfon, C. K., Njongmeta, L. M., Tanya, V. N., Williams, S. A., Bianco, A. E., & Trees, A. J. (2009). Immunisation with a multivalent, subunit vaccine reduces patent infection in a natural bovine model of onchocerciasis during intense field exposure. PLoS Neglected Tropical Diseases, 3(11), e544. https://doi.org/10.1371/journal.pntd.0000544
  • Makepeace, B. L., & Tanya, V. N. (2016). 25 years of the Onchocerca ochengi model. Trends in Parasitology, 32(12), 966–978. https://doi.org/10.1016/j.pt.2016.08.013
  • Maurya, S. K., Gollapalli, D. R., Kirubakaran, S., Zhang, M., Johnson, C. R., Benjamin, N. N., Hedstrom, L., & Cuny, G. D. (2009). Triazole inhibitors of Cryptosporidium parvum Inosine 5′-Monophosphate Dehydrogenase. Journal of Medicinal Chemistry, 52(15), 4623–4630. https://doi.org/10.1021/jm900410u
  • Nagpal, G., Usmani, S. S., Dhanda, S. K., Kaur, H., Singh, S., Sharma, M., & Raghava, G. P. (2017). Computer-aided designing of immunosuppressive peptides based on IL-10 inducing potential. Scientific Reports, 7(1), 42851. https://doi.org/10.1038/srep42851
  • Nair, V., & Shu, Q. (2007). Inosine monophosphate dehydrogenase as a probe in antiviral drug discovery. Antiviral Chemistry & Chemotherapy, 18(5), 245–258. https://doi.org/10.1177/095632020701800501
  • Naveed, M., Sheraz, M., Amin, A., Waseem, M., Aziz, T., Khan, A. A., Ghani, M., Shahzad, M., Alruways, M. W., Dablool, A. S., Elazzazy, A. M., Almalki, A. A., Alamri, A. S., & Alhomrani, M. (2022). Designing a novel peptide-based multi-Epitope vaccine to evoke a robust immune response against pathogenic multidrug-resistant Providencia heimbachae. Vaccines, 10(8), 1300. https://doi.org/10.3390/vaccines10081300
  • Ngwasiri, N. N., Brattig, N. W., Ndjonka, D., Liebau, E., Paguem, A., Leusder, D., Kingsley, M. T., Eisenbarth, A., Renz, A., & Achukwi, M. D. (2021). Galectins from Onchocerca ochengi and O. volvulus and their immune recognition by Wistar rats, Gudali zebu cattle and human hosts. BMC Microbiology, 21(1), 5. https://doi.org/10.1186/s12866-020-02064-3
  • Ngwewondo, A., Scandale, I., & Specht, S. (2021). Onchocerciasis drug development: From preclinical models to humans. Parasitology Research, 120(12), 3939–3964. https://doi.org/10.1007/s00436-021-07307-4
  • Noma, M., Zouré, H. G., Tekle, A. H., Enyong, P. A., Nwoke, B. E., & Remme, J. H. (2014). The geographic distribution of onchocerciasis in the 20 participating countries of the African Programme for Onchocerciasis Control: (1) priority areas for ivermectin treatment. Parasites and Vectors, 7(1), 325. https://doi.org/10.1186/1756-3305-7-325
  • Ogbonna, E. C., & Ikani, O. R. (2020). Systematic review on Onchocerciasis infection in Nigeria in the past five decades. International Journal of Medicine and Public Health, 10(1), 1–7.
  • Osei-Atweneboana, M. Y., Eng, J. K., Boakye, D. A., Gyapong, J. O., & Prichard, R. K. (2007). Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: A two-phase epidemiological study. Lancet (London, England), 369(9578), 2021–2029. https://doi.org/10.1016/s0140-6736(07)60942-8
  • Rapin, N., Lund, O., Bernaschi, M., & Castiglione, F. (2010). Computational immunology meets bioinformatics: The use of prediction tools for molecular binding in the simulation of the immune system. PLoS One, 5(4), e9862. https://doi.org/10.1371/journal.pone.0009862
  • Rose, C., Praulins, G., Armstrong, S. D., Casas-Sanchez, A., Davis, J., Molyneux, G., Yunta, C., Stead, Z., Prescott, M., Perally, S., Rutter, A., Makepeace, B. L., La Course, E. J., & Acosta-Serrano, A. (2019). Characterization of a novel glycosylated glutathione transferase of Onchocerca ochengi, closest relative of the human river blindness parasite. Parasitology, 146(14), 1773–1784. https://doi.org/10.1017/s0031182019000763
  • Saha, S., & Raghava, G. P. S. (2006). Prediction of continuous B-cell epitopes in an antigen using recurrent neural network. Proteins: Structure, Function, and Bioinformatics, 65(1), 40–48. https://doi.org/10.1002/prot.21078
  • Sarwono, A. E., Suganuma, K., Mitsuhashi, S., Okada, T., Musinguzi, S. P., Shigetomi, K., Inoue, N., & Ubukata, M. (2017). GMP reductase as a drug target for chemotherapy against T. congolense. Parasitology International, 66(5), 537–544. https://doi.org/10.1016/j.parint.2017.03.006
  • Sarwono, A. E. Y. (2018). Purine nucleotide biosynthesis pathway as a drug target: Identification of novel IMPDH and GMPR from Trypanosoma congolense, and an inhibitor screening study of Cryptosporidium parvum and human type II IMPDH. Doctoral dissertation. http://hdl.handle.net/2115/82798
  • Sauerbrey, M., Rakers, L. J., & Richards, F. O. (2018). Progress toward elimination of onchocerciasis in the Americas. International Health, 10(suppl_1), i71–i78. https://doi.org/10.1093/inthealth/ihx039
  • Shamakhi, A., & Kordbacheh, E. (2021). Immunoinformatic design of an epitope-based immunogen candidate against bacillus anthracis. Informatics in Medicine Unlocked, 24, 100574. https://doi.org/10.1016/j.imu.2021.100574
  • Sharling, L., Liu, X., Gollapalli, D. R., Maurya, S. K., Hedstrom, L., & Striepen, B. (2010). A screening pipeline for antiparasitic agents targeting cryptosporidium inosine monophosphate dehydrogenase. PLoS Neglected Tropical Diseases, 4(8), e794. https://doi.org/10.1371/journal.pntd.0000794
  • Shey, R. A., Ghogomu, S. M., Esoh, K. K., Nebangwa, N. D., Shintouo, C. M., Nongley, N. F., Asa, B. F., Ngale, F. N., Vanhamme, L., & Souopgui, J. (2019). In-silico design of a multi-epitope vaccine candidate against onchocerciasis and related filarial diseases. Scientific Reports, 9(1), 1-18. https://doi.org/10.1038/s41598-019-40833-x
  • Shey, R. A., Ghogomu, S. M., Shintouo, C. M., Nkemngo, F. N., Nebangwa, D. N., Esoh, K., Yaah, N. E., Manka’aFri, M., Nguve, J. E., Ngwese, R. A., Njume, F. N., Bertha, F. A., Ayong, L., Njemini, R., Vanhamme, L., & Souopgui, J. (2021). Computational design and preliminary serological analysis of a novel multi-epitope vaccine candidate against onchocerciasis and related filarial diseases. Pathogens, 10(2), 99. https://doi.org/10.3390/pathogens10020099
  • Sheyin, A., Gbem, T. T., Gaiya, D. D., & Nok, J. A. (2021). Genome and proteome screening of Onchocerca volvulus reveal putative vaccine candidates. Molecular Biomedicine, 2(1), 1–3. https://doi.org/10.1186/s43556-021-00062-z
  • Stranzl, T., Larsen, M. V., Lundegaard, C., & Nielsen, M. (2010). NetCTLpan: Pan-specific MHC class I pathway epitope predictions. Immunogenetics, 62(6), 357–368. https://doi.org/10.1007/s00251-010-0441-4
  • Studer, G., Tauriello, G., Bienert, S., Biasini, M., Johner, N., & Schwede, T. (2021). ProMod3—A versatile homology modelling toolbox. PLoS Computational Biology, 17(1), e1008667. https://doi.org/10.1371/journal.pcbi.1008667
  • Suganuma, K., Sarwono, A. E., Mitsuhashi, S., Jąkalski, M., Okada, T., Nthatisi, M., Yamagishi, J., Ubukata, M., & Inoue, N. (2016). Mycophenolic acid and its derivatives as potential Chemotherapeutic agents targeting Inosine Monophosphate Dehydrogenase in trypanosoma congolense. Antimicrobial Agents and Chemotherapy, 60(7), 4391–4393. https://doi.org/10.1128/aac.02816-15
  • The World Health Organization 2030 goals for Onchocerciasis, Gates Open Research. (2019). The World Health Organization 2030 goals for onchocerciasis: Insights and perspectives from mathematical modelling. Gates Open Research, 3, 1545. https://doi.org/10.12688/gatesopenres.13067.1
  • Tomar, N., & De, R. K. (2014). Immunoinformatics: A Brief Review. Methods in Molecular Biology, 1184, 23–55. https://doi.org/10.1007/978-1-4939-1115-8_3
  • Trees, A. J., Graham, S. P., Renz, A., Bianco, A. E., & Tanya, V. (2000). Onchocerca ochengi infections in cattle as a model for human onchocerciasis: Recent developments. Parasitology, 120(7), 133–142. https://doi.org/10.1017/S0031182099005788
  • Vieri, M. K., Logora, M. Y., Rafiq, K., & Colebunders, R. (2021). The World Health Organization road map for neglected tropical diseases 2021–2030: Implications for onchocerciasis elimination programs. Infectious Diseases of Poverty, 10(1), 1-4. https://doi.org/10.1186/s40249-021-00848-x
  • Wu, Q., Peng, Z., Zhang, Y., & Yang, J. (2018). COACH-D: Improved protein–ligand binding sites prediction with refined ligand-binding poses through molecular docking. Nucleic Acids Research, 46(W1), W438–W442. https://doi.org/10.1093/nar/gky439
  • Yang, J., Roy, A., & Zhang, Y. (2013). Protein–ligand binding site recognition using complementary binding-specific substructure comparison and sequence profile alignment. Bioinformatics (Oxford, England), 29(20), 2588–2595. https://doi.org/10.1093/bioinformatics/btt447
  • Zhan, B., Bottazzi, M. E., Hotez, P. J., & Lustigman, S. (2022). Advancing a human onchocerciasis vaccine from antigen discovery to efficacy studies against natural infection of cattle with Onchocerca ochengi. Frontiers in Cellular and Infection Microbiology, 12, 869039. https://doi.org/10.3389/fcimb.2022.869039
  • Zhang, J., Shang, Z., Zhang, X., & Zhang, Y. (2011). Modeling and analysis of schistosoma Argonaute protein molecular spatial conformation. Asian Pacific Journal of Tropical Biomedicine, 1(4), 275–278. https://doi.org/10.1016/s2221-1691(11)60042-7
  • Zhao, X., Zhang, F., Li, Z., Wang, H., An, M., Li, Y., Pang, N., & Ding, J. (2019). Bioinformatics analysis of EgA31 and EgG1Y162 proteins for designing a multi-epitope vaccine against echinococcus granulosus. Infection, Genetics and Evolution : Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 73, 98–108. https://doi.org/10.1016/j.meegid.2019.04.017
  • Zoete, V., Cuendet, M. A., Grosdidier, A., & Michielin, O. (2011). SwissParam: A fast force field generation tool for small organic molecules. Journal of Computational Chemistry, 32(11), 2359–2368. https://doi.org/10.1002/jcc.21816

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.