Novel Applications of Elastin-like Polypeptides (ELPs) in the Treatment of Pathogenic Free-Living Amoeba
DOI:
https://doi.org/10.58445/rars.1277Keywords:
ELPs, Pathogenic Free-Living Amoeba, Primary amoebic meningoencephalitisAbstract
Primary amoebic meningoencephalitis (PAM) is a rare and acute yet fulminant infection caused by the amoeba Naegleria fowleri. PAM is characterized by headaches, fever, nausea, and stiff neck. Although rare, PAM is fatal, with a mortality rate of 98% and causes death within two weeks of exposure. There are several key factors involved in the high mortality rate including the ineffectiveness of common treatments such as amphotericin B, fluconazole, azithromycin, and Rifampin alongside poor penetration of the blood-brain barrier (BBB). Elastin-like polypeptides (ELPs) are biopolymeric nanoparticles that mimic the properties of natural elastin, a key component of the extracellular matrix found in connective tissue. ELPs are specifically characterized by their biocompatibility, targeted and controlled release, phase change behavior, and the ability to encapsulate multiple drugs. While ELPs have been extensively researched in the context of various diseases, their potential in treating PAM remains an unexplored area of interest. This papers therefore focuses on possible approaches in which ELPs might be leveraged to increase the efficacy of existing treatments for PAM. By imagining how ELP nanomedicines could be applied for novel therapeutic strategies against PAM, we hope to inspire future translational avenues for this rare disease to improve patient outcomes.
References
Grace, E., Asbill, S., & Virga, K. (2015). Naegleria fowleri: Pathogenesis, Diagnosis, and Treatment Options. Antimicrobial Agents and Chemotherapy, 59(11), 6677–6681. https://doi.org/10.1128/aac.01293-15
Güémez, A., & García, E. (2021). Primary Amoebic Meningoencephalitis by Naegleria fowleri: Pathogenesis and Treatments. Biomolecules, 11(9), 1320. https://doi.org/10.3390/biom11091320
Tillery, L., Barrett, K., Goldstein, J., Lassner, J. W., Osterhout, B., Tran, N. L., Xu, L., Young, R. M., Craig, J., Chun, I., Dranow, D. M., Abendroth, J., Delker, S. L., Davies, D. R., Mayclin, S. J., Calhoun, B., Bolejack, M. J., Staker, B., Subramanian, S., . . . Van Voorhis, W. C. (2021). Naegleria fowleri: Protein structures to facilitate drug discovery for the deadly, pathogenic free-living amoeba. PloS One, 16(3), e0241738. https://doi.org/10.1371/journal.pone.0241738
Herman, E. K., Greninger, A., Van Der Giezen, M., Ginger, M. L., Ramirez-Macias, I., Miller, H. C., Morgan, M. J., Tsaousis, A. D., Velle, K., Vargová, R., Záhonová, K., Najle, S. R., MacIntyre, G., Muller, N., Wittwer, M., Zysset-Burri, D. C., Eliáš, M., Slamovits, C. H., Weirauch, M. T., . . . Dacks, J. B. (2021). Genomics and transcriptomics yields a system-level view of the biology of the pathogen Naegleria fowleri. BMC Biology, 19(1). https://doi.org/10.1186/s12915-021-01078-1
Visvesvara, G. S., Moura, H., & Schuster, F. L. (2007). Pathogenic and opportunistic free-living amoebae:Acanthamoebaspp.,Balamuthia mandrillaris,Naegleria fowleri, andSappinia diploidea. FEMS Immunology and Medical Microbiology, 50(1), 1–26. https://doi.org/10.1111/j.1574-695x.2007.00232.x
Naegleria. (2023, January 1). PubMed. https://pubmed.ncbi.nlm.nih.gov/30571068/
Rodríguez-Mera, I. B., Carrasco-Yépez, M. M., Vásquez-Moctezuma, I., Correa‐Basurto, J., Salinas, G. R., Castillo-Ramírez, D. A., Rosales-Cruz, É., & Rojas‐Hernández, S. (2022). Role of cathepsin B of Naegleria fowleri during primary amebic meningoencephalitis. Parasitology Research, 121(11), 3287–3303. https://doi.org/10.1007/s00436-022-07660-y
JOHN, D. T., Jr., COLE, T. B., Jr., & MARCIANO-CABRAL, F. M. (n.d.). Sucker-Like Structures on the Pathogenic Amoeba Naegleria fowleri. APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 47(1), 12–14. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC239603/pdf/aem00158-0030.pdf
Chen, C., & Moseman, E. A. (2023). Pro-inflammatory cytokine responses to Naegleria fowleri infection. Frontiers in Tropical Diseases, 3. https://doi.org/10.3389/fitd.2022.1082334
Marciano‐Cabral, F., & Cabral, G. A. (2007). The immune response to Naegleria fowler amebae and pathogenesis of infection. Fems Immunology and Medical Microbiology, 51(2), 243–259. https://doi.org/10.1111/j.1574-695x.2007.00332.x
Jamerson, M., Da Rocha-Azevedo, B., Cabral, G. A., & Marciano‐Cabral, F. (2012). Pathogenic Naegleria fowleri and non-pathogenic Naegleria lovaniensis exhibit differential adhesion to, and invasion of, extracellular matrix proteins. Microbiology, 158(3), 791–803. https://doi.org/10.1099/mic.0.055020-0
Oh, Y., Jeong, S., Kim, J., Song, K., Kim, K., Park, S., Sohn, S., & Shin, H. (2005). Cytopathic changes and pro‐inflammatory cytokines induced by Naegleria fowleri trophozoites in rat microglial cells and protective effects of an anti‐Nfa1 antibody. Parasite Immunology, 27(12), 453–459. https://doi.org/10.1111/j.1365-3024.2005.00799.x
Moseman, E. A. (2020). Battling brain-eating amoeba: Enigmas surrounding immunity to Naegleria fowleri. PLOS Pathogens, 16(4), e1008406. https://doi.org/10.1371/journal.ppat.1008406
Lindén, S. K., Sutton, P., Karlsson, N. G., Korolik, V., & McGuckin, M. A. (2008). Mucins in the mucosal barrier to infection. Mucosal Immunology, 1(3), 183–197. https://doi.org/10.1038/mi.2008.5
Cervantes-Sandoval, I., De Jesús Serrano-Luna, J., Meza-Cervantez, P., Arroyo, R., Tsutsumi, V., & Shibayama, M. (2009). Naegleria fowleri induces MUC5AC and pro-inflammatory cytokines in human epithelial cells via ROS production and EGFR activation. Microbiology, 155(11), 3739–3747. https://doi.org/10.1099/mic.0.030635-0
Vugia, D. J., Richardson, J. A., Tarro, T. M., Vareechon, C., Pannaraj, P. S., Traub, E., Cope, J. R., & Balter, S. (2019). Notes from the Field: Fatal Naegleria fowleri Meningoencephalitis After Swimming in Hot Spring Water — California, 2018. Morbidity and Mortality Weekly Report, 68(36), 793–794. https://doi.org/10.15585/mmwr.mm6836a3
Pana, A. (2023, January 21). Amebic meningoencephalitis. StatPearls - NCBI Bookshelf. https://www.ncbi.nlm.nih.gov/books/NBK430754/
Pugh, J. J., & Levy, R. (2016). Naegleria fowleri: Diagnosis, Pathophysiology of Brain Inflammation, and Antimicrobial Treatments. ACS Chemical Neuroscience, 7(9), 1178–1179. https://doi.org/10.1021/acschemneuro.6b00232
Noor, A. (2023, March 24). Amphotericin B. StatPearls - NCBI Bookshelf. https://www.ncbi.nlm.nih.gov/books/NBK482327/
Andrews, J. M. (2001). Determination of minimum inhibitory concentrations. Journal of Antimicrobial Chemotherapy, 48(suppl_1), 5–16. https://doi.org/10.1093/jac/48.suppl_1.5
Rajendran, K., Anwar, A., Khan, N. A., & Siddiqui, R. (2017). Brain-Eating Amoebae: Silver Nanoparticle Conjugation Enhanced Efficacy of Anti-Amoebic Drugs against Naegleria fowleri. ACS Chemical Neuroscience, 8(12), 2626–2630. https://doi.org/10.1021/acschemneuro.7b00430
Goswick, S. M., & Brenner, G. M. (2003). Activities of Azithromycin and Amphotericin B against Naegleria fowleri In Vitro and in a Mouse Model of Primary Amebic Meningoencephalitis. Antimicrobial Agents and Chemotherapy, 47(2), 524–528. https://doi.org/10.1128/aac.47.2.524-528.2003
Zervos, E. E., Bass, S. S., Robson, M. C., & Rosemurgy, A. S. (1996). Fluconazole increases bactericidal activity of neutrophils. Journal of Trauma-injury Infection and Critical Care, 41(1), 10–14. https://doi.org/10.1097/00005373-199607000-00003
Ayudhya, D. P. N., Thanompuangseree, N., & Tansuphaswadikul, S. (2004). Effect of Rifampicin on the Pharmacokinetics of Fluconazole in Patients with AIDS. Clinical Pharmacokinectics, 43(11), 725–732. https://doi.org/10.2165/00003088-200443110-00003
Alli, A., Ortíz, J. F., Cox, Á. M., De Armas, M. G. G., & Orellana, V. A. (2021). Miltefosine: a miracle drug for meningoencephalitis caused by Free-Living Amoebas. Cureus. https://doi.org/10.7759/cureus.13698
Roy, S. L., Atkins, J. T., Gennuso, R., Kofos, D., Sriram, R., Dorlo, T. P. C., Hayes, T., Qvarnström, Y., Kučerová, Z., Guglielmo, B. J., & Visvesvara, G. S. (2015). Assessment of blood–brain barrier penetration of miltefosine used to treat a fatal case of granulomatous amebic encephalitis possibly caused by an unusual Balamuthia mandrillaris strain. Parasitology Research, 114(12), 4431–4439. https://doi.org/10.1007/s00436-015-4684-8
Siripurapu, G., Samad, S. A., Fatima, S., Wig, N., & Srivastava, M. V. P. (2021). Successful management of post-COVID-19 acanthamoebic encephalitis. International Journal of Infectious Diseases, 110, 226–228. https://doi.org/10.1016/j.ijid.2021.07.046
Parija, S. C., Kp, D., & Venugopal, H. (2015). Management of granulomatous amebic encephalitis: Laboratory diagnosis and treatment. Tropical Parasitology, 5(1), 23. https://doi.org/10.4103/2229-5070.149889
Keane, N., Lane, L. M., Canniff, E., Hare, D., Doran, S., Wallace, E., Hutchinson, S., Healy, M., Hennessy, B., Meaney, J., Chiodini, P. L., O’Connell, B., Beausang, A., & Vandenberghe, E. (2020). A surviving case of acanthamoeba granulomatous amebic encephalitis in a hematopoietic stem cell transplant recipient. American Journal of Case Reports, 21. https://doi.org/10.12659/ajcr.923219
Da Rocha-Azevedo, B., Tanowitz, H. B., & Marciano‐Cabral, F. (2009). Diagnosis of infections caused by pathogenic Free-Living AmoeBAe. Interdisciplinary Perspectives on Infectious Diseases, 2009, 1–14. https://doi.org/10.1155/2009/251406
Kalra, S. K., Sharma, P., Shyam, K., Tejan, N., & Ghoshal, U. (2020). Acanthamoeba and its pathogenic role in granulomatous amebic encephalitis. Experimental Parasitology, 208, 107788. https://doi.org/10.1016/j.exppara.2019.107788
Wang, Y., Jiang, L., Zhao, Y., Ju, X., Wang, L., Liang, J., Fine, R. D., & Li, M. (2023). Biological characteristics and pathogenicity of Acanthamoeba. Frontiers in Microbiology, 14. https://doi.org/10.3389/fmicb.2023.1147077
Siddiqui, R., & Khan, N. A. (2012). Biology and pathogenesis of Acanthamoeba. Parasites & Vectors, 5(1). https://doi.org/10.1186/1756-3305-5-6
Duggal, S. D. (2018, January 22). Role of acanthamoeba in granulomatous encephalitis: a review. https://www.scitechnol.com/peer-review/role-of-acanthamoeba-in-granulomatous-encephalitis-a-review-JszK.php?article_id=7095
Cursons, R. T., Brown, T., Keys, E. A., Moriarty, K. M., & Till, D. G. (1980). Immunity to pathogenic free-living amoebae: role of humoral antibody. Infection and Immunity, 29(2), 401–407. https://doi.org/10.1128/iai.29.2.401-407.1980
Kot, K., Łanocha-Arendarczyk, N., & Kosik-Bogacka, D. (2021). Immunopathogenicity of Acanthamoeba spp. in the Brain and Lungs. International Journal of Molecular Sciences, 22(3), 1261. https://doi.org/10.3390/ijms22031261
Visvesvara, G. S., Moura, H., & Schuster, F. L. (2007). Pathogenic and opportunistic free-living amoebae:Acanthamoebaspp.,Balamuthia mandrillaris,Naegleria fowleri, andSappinia diploidea. Fems Immunology and Medical Microbiology, 50(1), 1–26. https://doi.org/10.1111/j.1574-695x.2007.00232.x
Chalmers, R. M. (2014). Acanthamoeba. In Elsevier eBooks (pp. 263–276). https://doi.org/10.1016/b978-0-12-415846-7.00014-7
Ellison, D. W., Love, S., Chimelli, L., Harding, B., Lowe, J., Vinters, H. V., Brandner, S., & Yong, W. H. (2013). Parasitic infections. In Elsevier eBooks (pp. 403–424). https://doi.org/10.1016/b978-0-7234-3515-0.00018-0
Bhosale, N. K., & Parija, S. C. (2021). Balamuthia mandrillaris: An opportunistic, free-living ameba - An updated review. PubMed, 11(2), 78–88. https://doi.org/10.4103/tp.tp_36_21
Balamuthia mandrillaris | Acanthamoeba and free-living amoebae. (n.d.). https://u.osu.edu/acanthamoeba/the-history-of-acanthamoeba-at-osu/balamuthia-mandrillaris/#:~:text=Results%20from%20this%20phylogenetic%20analysis,the%20Amoebozoa%20and%20the%20Acanthamoebidae.
Phan, I., Rice, C. A., Craig, J. M., Noorai, R. E., McDonald, J., Subramanian, S., Tillery, L., Barrett, L. K., Shankar, V., Morris, J. C., Van Voorhis, W. C., Kyle, D. E., & Myler, P. J. (2021). The transcriptome of Balamuthia mandrillaris trophozoites for structure-guided drug design. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-99903-8
Cope, J. R., Landa, J. T., Nethercut, H., Collier, S., Glaser, C., Moser, M., Puttagunta, R., Yoder, J. S., Ali, I. K. M., & Roy, S. L. (2018). The Epidemiology and Clinical Features of Balamuthia mandrillaris Disease in the United States, 1974–2016. Clinical Infectious Diseases, 68(11), 1815–1822. https://doi.org/10.1093/cid/ciy813
Lee, D., Fiester, S. E., Madeline, L., Fulcher, J. W., Ward, M. E., Schammel, C. M., & Hakimi, R. (2019). Acanthamoeba spp. and Balamuthia mandrillaris leading to fatal granulomatous amebic encephalitis. Forensic Science, Medicine and Pathology, 16(1), 171–176. https://doi.org/10.1007/s12024-019-00202-6
Da Rocha-Azevedo, B., Tanowitz, H. B., & Marciano‐Cabral, F. (2009). Diagnosis of infections caused by pathogenic Free-Living AmoeBAe. Interdisciplinary Perspectives on Infectious Diseases, 2009, 1–14. https://doi.org/10.1155/2009/251406
Da Rocha-Azevedo, B., Tanowitz, H. B., & Marciano‐Cabral, F. (2009b). Diagnosis of infections caused by pathogenic Free-Living AmoeBAe. Interdisciplinary Perspectives on Infectious Diseases, 2009, 1–14. https://doi.org/10.1155/2009/251406
CDC - DPDX - Free Living Amebic infections. (n.d.). https://www.cdc.gov/dpdx/freelivingamebic/index.html
Qvarnström, Y., Da Silva, A. J., Schuster, F. L., Gelman, B. B., & Visvesvara, G. S. (2009). Molecular Confirmation ofSappinia pedataas a Causative Agent of Amoebic Encephalitis. The Journal of Infectious Diseases, 199(8), 1139–1142. https://doi.org/10.1086/597473
Medical Chemistry Corporation. (2021, November 30). Sappinia spp. - Medical Chemical Corporation. Medical Chemical Corporation. https://med-chem.com/sappinia-spp/
Qvarnström, Y., Da Silva, A. J., Schuster, F. L., Gelman, B. B., & Visvesvara, G. S. (2009b). Molecular Confirmation ofSappinia pedataas a Causative Agent of Amoebic Encephalitis. The Journal of Infectious Diseases, 199(8), 1139–1142. https://doi.org/10.1086/597473
Taravaud, A., Fechtali-Moute, Z., Loiseau, P. M., & Pomel, S. (2021). Drugs used for the treatment of cerebral and disseminated infections caused by free‐living amoebae. Clinical and Translational Science, 14(3), 791–805. https://doi.org/10.1111/cts.12955
Taravaud, A., Loiseau, P. M., & Pomel, S. (2017). In vitro evaluation of antimicrobial agents on Acanthamoeba sp. and evidence of a natural resilience to amphotericin B. International Journal for Parasitology: Drugs and Drug Resistance, 7(3), 328–336. https://doi.org/10.1016/j.ijpddr.2017.09.002
Elsheikha, H. M., Siddiqui, R., & Khan, N. A. (2020). Drug Discovery against Acanthamoeba Infections: Present Knowledge and Unmet Needs. Pathogens, 9(5), 405. https://doi.org/10.3390/pathogens9050405
Chen, X., Zhang, Q., Wen, S., Chen, F., & Zhou, C. (2023). Pathogenic free-living amoebic encephalitis from 48 cases in China: A systematic review. Frontiers in Neurology, 14. https://doi.org/10.3389/fneur.2023.1100785
Spottiswoode, N., Pet, D., Kim, A., Gruenberg, K., Shah, M. P., Ramachandran, A., Laurie, M. T., Zia, M., Fouassier, C., Boutros, C. L., Lu, R., Zhang, Y., Servellita, V., Bollen, A. W., Chiu, C. Y., Wilson, M. R., Valdivia, L., & DeRisi, J. L. (2023). Successful Treatment of Balamuthia mandrillaris Granulomatous Amebic Encephalitis with Nitroxoline. Emerging Infectious Diseases, 29(1), 197–201. https://doi.org/10.3201/eid2901.221531
Joseph, T. M., Mahapatra, D. K., Esmaeili, A., Piszczyk, Ł., Hasanin, M. S., Kattali, M., Haponiuk, J. T., & Thomas, S. (2023). Nanoparticles: taking a unique position in medicine. Nanomaterials, 13(3), 574. https://doi.org/10.3390/nano13030574
Elumalai, K., Srinivasan, S., & Shanmugam, A. (2024). Review of the efficacy of nanoparticle-based drug delivery systems for cancer treatment. Biomedical Technology, 5, 109–122. https://doi.org/10.1016/j.bmt.2023.09.001
Sultana, A., Zare, M., Thomas, V., Kumar, T., & Ramakrishna, S. (2022). Nano-based drug delivery systems: Conventional drug delivery routes, recent developments and future prospects. Medicine in Drug Discovery, 15, 100134. https://doi.org/10.1016/j.medidd.2022.100134
Elumalai, K., Srinivasan, S., & Shanmugam, A. (2024). Review of the efficacy of nanoparticle-based drug delivery systems for cancer treatment. Biomedical Technology, 5, 109–122. https://doi.org/10.1016/j.bmt.2023.09.001
Zottel, A., Paska, A. V., & Jovčevska, I. (2019). Nanotechnology meets Oncology: Nanomaterials in brain cancer research, diagnosis and therapy. Materials, 12(10), 1588. https://doi.org/10.3390/ma12101588
Tobin, E., & Brenner, S. (2021). Nanotechnology fundamentals applied to clinical infectious diseases and public health. Open Forum Infectious Diseases, 8(12). https://doi.org/10.1093/ofid/ofab583
Siddiqui, R., Boghossian, A., Akbar, N., Jabri, T., Aslam, Z., Shah, M. R., Alharbi, A. M., Alfahemi, H., & Khan, N. A. (2022). Zinc Oxide Nanoconjugates against Brain-Eating Amoebae. Antibiotics, 11(10), 1281. https://doi.org/10.3390/antibiotics11101281
Fan, X., Chen, T., Ye, H., Gao, Y., & Chen, Y. (2023). Encephalomyelomeningitis Caused by Balamuthia mandrillaris: A Case Report and Literature Review. Infection and Drug Resistance, Volume 16, 727–733. https://doi.org/10.2147/idr.s400692
Cheng, X., Xie, Q., & Sun, Y. (2023). Advances in nanomaterial-based targeted drug delivery systems. Frontiers in Bioengineering and Biotechnology, 11. https://doi.org/10.3389/fbioe.2023.1177151
Mitchell, M. J., Billingsley, M. M., Haley, R. M., Wechsler, M. E., Peppas, N. A., & Langer, R. (2020). Engineering precision nanoparticles for drug delivery. Nature Reviews Drug Discovery, 20(2), 101–124. https://doi.org/10.1038/s41573-020-0090-8
Abdelnasir, S., Anwar, A., Kawish, M., Ali, A., Shah, M. R., Siddiqui, R., & Khan, N. A. (2020). Metronidazole conjugated magnetic nanoparticles loaded with amphotericin B exhibited potent effects against pathogenic Acanthamoeba castellanii belonging to the T4 genotype. AMB Express, 10(1). https://doi.org/10.1186/s13568-020-01061-z
Mungroo, M. R., Anwar, A., Khan, N. A., & Siddiqui, R. (2020). Gold-Conjugated Curcumin as a Novel Therapeutic Agent against Brain-Eating Amoebae. ACS Omega, 5(21), 12467–12475. https://doi.org/10.1021/acsomega.0c01305
Anwar, A., Numan, A., Siddiqui, R., Khalid, M., & Khan, N. A. (2019). Cobalt nanoparticles as novel nanotherapeutics against Acanthamoeba Castellani. Parasites & Vectors, 12(1). https://doi.org/10.1186/s13071-019-3528-2
Lima, L. F., Da Costa Sousa, M. G., Rodrigues, G. R., De Oliveira, K. B. S., Pereira, A. M., Da Costa, A., Machado, R., Franco, O. L., & Dias, S. C. (2022). Elastin-like polypeptides in development of nanomaterials for application in the medical field. Frontiers in Nanotechnology, 4. https://doi.org/10.3389/fnano.2022.874790
Despanie, J., Dhandhukia, J., Hamm‐Alvarez, S. F., & MacKay, J. A. (2016). Elastin-like polypeptides: Therapeutic applications for an emerging class of nanomedicines. Journal of Controlled Release, 240, 93–108. https://doi.org/10.1016/j.jconrel.2015.11.010
Van Strien, J., Escalona-Rayo, O., Jiskoot, W., Slütter, B., & Kros, A. (2023). Elastin-like polypeptide-based micelles as a promising platform in nanomedicine. Journal of Controlled Release, 353, 713–726. https://doi.org/10.1016/j.jconrel.2022.12.033
Bidwell, G. L. (2021). Novel protein therapeutics created using the Elastin-Like polypeptide platform. Physiology, 36(6), 367–381. https://doi.org/10.1152/physiol.00026.2021
Guo, Y., Liu, S., Jing, D., Liu, N., & Liu, X. (2023). The construction of elastin-like polypeptides and their applications in drug delivery system and tissue repair. Journal of Nanobiotechnology, 21(1). https://doi.org/10.1186/s12951-023-02184-8
Tillery, L., Barrett, K. F., Goldstein, J., Lassner, J. W., Osterhout, B., Tran, N. L., Xu, L., Young, R. M., Craig, J. M., Chun, I., Dranow, D. M., Abendroth, J., Delker, S., Davies, Mayclin, S. J., Calhoun, B., Bolejack, M., Staker, B. L., Subramanian, S., . . . Van Voorhis, W. C. (2021). Naegleria fowleri: Protein structures to facilitate drug discovery for the deadly, pathogenic free-living amoeba. PLOS ONE, 16(3), e0241738. https://doi.org/10.1371/journal.pone.0241738
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