Top

Published in:

01-06-2019 | Amphotericin B | Original Article

Leishmanicidal effects of amphotericin B in combination with selenium loaded on niosome against Leishmania tropica

Authors: Mahshid Mostafavi, Saeedeh Farajzadeh, Iraj Sharifi, Payam Khazaeli, Hamid Sharifi

Published in: Journal of Parasitic Diseases | Issue 2/2019

Abstract

The strategy for improving the treatment of leishmaniasis by the World Health Organization, is the development of new drugs and combination therapy. The aim of this survey was to investigate the effect of amphotericin B (AmB) in combination with selenium, in a simple or niosomal form, on Leishmania tropica (L. tropica) by in vitro advanced assays. In this study, a niosomal formulation of AmB with selenium was prepared and characterized based on size and morphology. Using MTT assay, macrophage model, flow cytometry, and qPCR, the cytotoxicity and efficiency of the niosomal formulation and simple form of combination were evaluated. No toxicity was reported for both the niosomal and simple form of the combination. The niosomal formulation significantly showed higher inhibitory effect on the promastigote and amastigote forms of L. tropica than simple combination form. Interleukin (IL)-10 significantly decreased while the level of IL-12 and metacasoase as Th-1 activator significantly increased (P < 0.001). The findings of this study indicated that niosomes are the stable carriers for this combination, easy to produce and provide promising results as an effective formulation in the inhibition of extracellular and intracellular forms of L. tropica in compared with simple combination form.

Agrawal S, Rai M, Sundar S (2005) Management of visceral leishmaniasis: Indian perspective. J Postgrad Med 51(Suppl 1):S53–S57PubMed

Aguiar MG, Pereira AMM et al (2010) Reductions in skin and systemic parasite burdens as a combined effect of topical paromomycin and oral miltefosine treatment of mice experimentally infected with Leishmania (Leishmania) amazonensis. Antimicrob Agents Chemother 54:4699–4704. https://doi.org/10.1128/AAC.00809-10 CrossRefPubMedPubMedCentral

Alvar J, Vélez ID, Bern C et al (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7:e35671. https://doi.org/10.1371/journal.pone.0035671 CrossRefPubMedPubMedCentral

Ambit A, Fasel N, Coombs GH, Mottram JC (2008) An essential role for the Leishmania major metacaspase in cell cycle progression. Cell Death Differ 15:113–122. https://doi.org/10.1038/sj.cdd.4402232 CrossRefPubMed

Annaloro C, Olivares C, Usardi P et al (2009) Retrospective evaluation of amphotericin B deoxycholate toxicity in a single centre series of haematopoietic stem cell transplantation recipients. J Antimicrob Chemother 63:625–626. https://doi.org/10.1093/jac/dkn549 CrossRefPubMed

Bayindir ZS, Be AB, Yüksel N (2015) Paclitaxel-loaded niosomes for intravenous administration: pharmacokinetics and tissue distribution in rats. Turk J Med Sci 45:1403–1412CrossRefPubMed

Beheshti N, Soflaei S, Shakibaie M et al (2013) Efficacy of biogenic selenium nanoparticles against Leishmania major: in vitro and in vivo studies. J Trace Elem Med Biol 27:203–207. https://doi.org/10.1016/j.jtemb.2012.11.002 CrossRefPubMed

Cassago A, Rodrigues EM, Prieto EL et al (2006) Identification of Leishmania selenoproteins and SECIS element. Mol Biochem Parasitol 149:128–134. https://doi.org/10.1016/j.molbiopara.2006.05.002 CrossRefPubMed

Chandra D, Naik S, Naik S (2008) Leishmania donovani infection down-regulates TLR2-stimulated IL-12p40 and activates IL-10 in cells of macrophage/monocytic lineage by modulating MAPK pathways through a contact-dependent mechanism. Clin Exp Immunol. https://doi.org/10.1111/j.1365-2249.2008.03741.x CrossRefPubMedPubMedCentral

Chattopadhyay A, Jafurulla M (2011) A novel mechanism for an old drug: amphotericin B in the treatment of visceral leishmaniasis. Biochem Biophys Res Commun 416:7–12. https://doi.org/10.1016/j.bbrc.2011.11.023 CrossRefPubMed

Croft SL, Seifert K, Yardley V (2006a) Current scenario of drug development for leishmaniasis. Indian J Med Res 123:399–410PubMed

Croft SL, Sundar S, Fairlamb AH (2006b) Drug resistance in Leishmaniasis. Clin Microbiol Rev 19:111–126. https://doi.org/10.1128/CMR.19.1.111-126.2006 CrossRefPubMedPubMedCentral

Cunha MA, de Cassia Soler R, Leão ACQ, Lindoso JAL (2015) Efficacy and safety of liposomal amphotericin B for the treatment of mucosal leishmaniasis from the new world: a retrospective study. Am J Trop Med Hyg 93:1214–1218. https://doi.org/10.4269/ajtmh.15-0033 CrossRefPubMedPubMedCentral

Debrabant A, Lee N, Bertholet S et al (2003) Programmed cell death in trypanosomatids and other unicellular organisms. Int J Parasitol 33:257–267CrossRefPubMed

Donowitz GR (1994) Tissue-directed antibiotics and intracellular parasites: complex interaction of phagocytes, pathogens, and drugs. Clin Infect Dis 19:926–930. https://doi.org/10.1093/clinids/19.5.926 CrossRefPubMed

Duarte MC, Tavares GSV, Valadares DG et al (2016) Antileishmanial activity and mechanism of action from a purified fraction of Zingiber officinalis Roscoe against Leishmania amazonensis. Exp Parasitol 166:21–28. https://doi.org/10.1016/j.exppara.2016.03.026 CrossRefPubMed

Escudero-Martínez JM, Pérez-Pertejo Y, Reguera RM et al (2017) Antileishmanial activity and tubulin polymerization inhibition of podophyllotoxin derivatives on Leishmania infantum. Int J Parasitol Drugs Drug Resist 7:272–285. https://doi.org/10.1016/J.IJPDDR.2017.06.003 CrossRefPubMedPubMedCentral

Farajzadeh S, Esfandiarpour I, Haghdoost AA et al (2015a) Comparison between combination therapy of oral terbinafine and cryotherapy versus systemic meglumine antimoniate and cryotherapy in cutaneous leishmaniasis: a randomized clinical trial. Iran J Parasitol 10:1–8PubMedPubMedCentral

Farajzadeh S, Heshmatkhah A, Vares B et al (2015b) Topical terbinafine in the treatment of cutaneous leishmaniasis: triple blind randomized clinical trial. J Parasit Dis. 1:1. https://doi.org/10.1007/s12639-014-0641-1 CrossRef

Farajzadeh S, Heshmatkhah A, Vares B et al (2016) Topical terbinafine in the treatment of cutaneous leishmaniasis: triple blind randomized clinical trial. J Parasit Dis 40:1159–1164. https://doi.org/10.1007/s12639-014-0641-1 CrossRefPubMed

Frankenburg S, Glick D, Klaus S, Barenholz Y (1998) Efficacious topical treatment for murine cutaneous leishmaniasis with ethanolic formulations of amphotericin B. Antimicrob Agents Chemother 42:3092–3096CrossRefPubMedPubMedCentral

Freitas-Junior LH, Chatelain E, Kim HA, Siqueira-Neto JL (2012) Visceral leishmaniasis treatment: What do we have, what do we need and how to deliver it? Int J Parasitol Drugs Drug Resist 2:11–19. https://doi.org/10.1016/J.IJPDDR.2012.01.003 CrossRefPubMedPubMedCentral

Frézard F, Demicheli C, Ribeiro RR (2009) Pentavalent antimonials: new perspectives for old drugs. Molecules 14:2317–2336. https://doi.org/10.3390/molecules14072317 CrossRefPubMedPubMedCentral

Ganguly S, Bandyopadhyay S, Sarkar A, Chatterjee M (2006) Development of a semi-automated colorimetric assay for screening anti-leishmanial agents. J Microbiol Methods 66:79–86. https://doi.org/10.1016/J.MIMET.2005.10.011 CrossRefPubMed

Gannavaram S, Bhattacharya P, Ismail N et al (2016) Modulation of innate immune mechanisms to enhance Leishmania vaccine-induced immunity: role of coinhibitory molecules. Front Immunol 7:187. https://doi.org/10.3389/fimmu.2016.00187 CrossRefPubMedPubMedCentral

Kaye P, Scott P (2011) Leishmaniasis: complexity at the host–pathogen interface. Nat Rev Microbiol 9:604–615. https://doi.org/10.1038/nrmicro2608 CrossRefPubMed

Kedzierski L, Zhu Y, Handman E (2006) Leishmania vaccines: progress and problems. Parasitology 133:S87. https://doi.org/10.1017/S0031182006001831 CrossRefPubMed

Koutsoni O, Barhoumi M, Guizani I, Dotsika E (2014) Leishmania eukaryotic initiation factor (LeIF) inhibits parasite growth in murine macrophages. PLoS ONE 9:1–10. https://doi.org/10.1371/journal.pone.0097319 CrossRef

Kremsner PG, Krishna S (2004) Combinations of anti malaria drugs—Malaria site. Lancet (London, England). https://www.malariasite.com/antimalarial-combinations/. Accessed 11 Jun 2018

Kumar R, Engwerda C (2014) Vaccines to prevent leishmaniasis. Clin Transl Immunol 3:e13. https://doi.org/10.1038/cti.2014.4 CrossRef

Lee N, Bertholet S, Debrabant A et al (2002) Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death Differ 9:53–64. https://doi.org/10.1038/sj.cdd.4400952 CrossRefPubMed

Lira R, Sundar S, Makharia A et al (1999) Evidence that the high incidence of treatment failures in Indian Kala-Azar is due to the emergence of antimony-resistant strains of Leishmania donovani. J Infect Dis 180:564–567. https://doi.org/10.1086/314896 CrossRefPubMed

Lobanov AV, Gromer S, Salinas G, Gladyshev VN (2016) Selenium metabolism in Trypanosoma: characterization of selenoproteomes and identification of a Kinetoplastida-specific selenoprotein. Nucl Acids Res 1:1. https://doi.org/10.1093/nar/gkl541 CrossRef

Mahale NB, Thakkar PD, Mali RG et al (2012) Niosomes: novel sustained release nonionic stable vesicular systems—an overview. Adv Colloid Interface Sci 183–184:46–54. https://doi.org/10.1016/j.cis.2012.08.002 CrossRefPubMed

Mahmoudvand H, Shakibaie M, Tavakoli R et al (2014) In vitro study of leishmanicidal activity of biogenic selenium nanoparticles against Iranian isolate of sensitive and glucantime-resistant Leishmania tropica. Iran J Parasitol 9:452–460PubMedPubMedCentral

Martín-Montes Á, Plano D, Martín-Escolano R et al (2017) Library of seleno-compounds as novel agents against Leishmania species. Antimicrob Agents Chemother 61:1–13. https://doi.org/10.1128/AAC.02546-16 CrossRef

Mitchison D, Davies G (2012) The chemotherapy of tuberculosis: past, present and future [State of the art]. Int J Tuberc Lung Dis 16:724–732. https://doi.org/10.5588/ijtld.12.0083 CrossRefPubMed

Momeni AZ, Aminjavaheri M, Omidghaemi MR (2003) Treatment of cutaneous leishmaniasis with ketoconazole cream. J Dermatolog Treat 14:26–29CrossRefPubMed

Moosavian Kalat SA, Khamesipour A, Bavarsad N et al (2014) Use of topical liposomes containing meglumine antimoniate (Glucantime) for the treatment of L. major lesion in BALB/c mice. Exp Parasitol 143:5–10. https://doi.org/10.1016/j.exppara.2014.04.013 CrossRef

Murray HW, Flanders KC, Debra D et al (2005) Antagonizing deactivating cytokines to enhance host defense and chemotherapy in experimental visceral leishmaniasis antagonizing deactivating cytokines to enhance host defense and chemotherapy in experimental visceral leishmaniasis. Infect Immun 73:3903–3911. https://doi.org/10.1128/IAI.73.7.3903 CrossRefPubMedPubMedCentral

Olliaro PL, Taylor WRJ (2003) Antimalarial compounds: from bench to bedside. J Exp Biol 206:3753–3759CrossRefPubMed

Omollo R, Alexander N, Edwards T et al (2011) Safety and efficacy of miltefosine alone and in combination with sodium stibogluconate and liposomal amphotericin B for the treatment of primary visceral leishmaniasis in East Africa: study protocol for a randomized controlled trial. Trials 12:166. https://doi.org/10.1186/1745-6215-12-166 CrossRefPubMedPubMedCentral

Osorio LE, Palacios R, Chica ME, Ochoa MT (1998) Treatment of cutaneous leishmaniasis in Colombia with dapsone. Lancet 351:498–499. https://doi.org/10.1016/S0140-6736(05)78687-6 CrossRefPubMed

Owais M, Gupta C (2005) Targeted drug delivery to macrophages in parasitic infections. Curr Drug Deliv 2:311–318. https://doi.org/10.2174/156720105774370177 CrossRefPubMed

Perez AP, Altube MJ, Schilrreff P et al (2016) Topical amphotericin B in ultradeformable liposomes: formulation, skin penetration study, antifungal and antileishmanial activity in vitro. Colloids Surf B Biointerfaces 139:190–198. https://doi.org/10.1016/j.colsurfb.2015.12.003 CrossRefPubMed

Prajapati VK, Awasthi K, Gautam S et al (2011) Targeted killing of Leishmania donovani in vivo and in vitro with amphotericin B attached to functionalized carbon nanotubes. J Antimicrob Chemother 66:874–879. https://doi.org/10.1093/jac/dkr002 CrossRefPubMedPubMedCentral

Raina P, Kaur S (2012) Knockdown of LdMC1 and Hsp70 by antisense oligonucleotides causes cell-cycle defects and programmed cell death in Leishmania donovani. Mol Cell Biochem 359:135–149. https://doi.org/10.1007/s11010-011-1007-y CrossRefPubMed

Rayman MP (2005) Selenium in cancer prevention: a review of the evidence and mechanism of action. Proc Nutr Soc 64:527–542CrossRefPubMed

Rayman MP (2012) Selenium and human health. Lancet 379:1256–1268. https://doi.org/10.1016/S0140-6736(11)61452-9 CrossRefPubMed

Riabi TR, Sharifi I, Mohammadi AM et al (2013) Evaluation of a possible synergistic effect of meglumine antimoniate with paromomycin, miltefosine or allopurinol on in vitro susceptibility of Leishmania tropica resistant isolate. Iran J Parasitol 8:396–401

Rogerson A, Cummings J, Florence AT (1987) Adriamycin-loaded niosomes: drug entrapment, stability and release. J Microencapsul 4:321–328. https://doi.org/10.3109/02652048709021824 CrossRefPubMed

Santos DO, Coutinho CER, Madeira MF et al (2008) Leishmaniasis treatment—a challenge that remains: a review. Parasitol Res 103:1–10. https://doi.org/10.1007/s00436-008-0943-2 CrossRefPubMed

Seifert K, Croft SL (2006) In vitro and in vivo interactions between miltefosine and other antileishmanial drugs. Antimicrob Agents Chemother 50:73–79. https://doi.org/10.1128/AAC.50.1.73-79.2006 CrossRefPubMedPubMedCentral

Shokri A, Sharifi I, Khamesipour A et al (2012) The effect of verapamil on in vitro susceptibility of promastigote and amastigote stages of Leishmania tropica to meglumine antimoniate. Parasitol Res 110:1113–1117. https://doi.org/10.1007/s00436-011-2599-6 CrossRefPubMed

Soflaei S, Dalimi A, Abdoli A et al (2014) Anti-leishmanial activities of selenium nanoparticles and selenium dioxide on Leishmania infantum. Comp Clin Path 23:15–20. https://doi.org/10.1007/s00580-012-1561-z CrossRef

Sundar S, Chakravarty J (2010) Liposomal amphotericin B and leishmaniasis: dose and response. J Glob Infect Dis 2:159–166. https://doi.org/10.4103/0974-777X.62886 CrossRefPubMedPubMedCentral

Sundar S, Singh A, Singh OP (2014) Strategies to overcome antileishmanial drugs unresponsiveness. J Trop Med 2014:1–7. https://doi.org/10.1155/2014/646932 CrossRef

Thakur CP, Kanyok TP, Pandey AK et al (2000) A prospective randomized, comparative, open-label trial of the safety and efficacy of paromomycin (aminosidine) plus sodium stibogluconate versus sodium stibogluconate alone for the treatment of visceral leishmaniasis. Trans R Soc Trop Med Hyg 94(4):429–431CrossRefPubMed

Tolouei S, Hasheminia S, Narimani M et al (2011) Leishmanicidal activity of films containing paromomycin and gentamicin sulfate both in vitro and in vivo. Iran J Parasitol 6:60–65PubMedPubMedCentral

Torrado JJ, Espada R, Ballesteros MP, Torrado-Santiago S (2008) Amphotericin B formulations and drug targeting. J Pharm Sci 97:2405–2425. https://doi.org/10.1002/jps.21179 CrossRefPubMed

Tran PA, Webster TJ (2011) Selenium nanoparticles inhibit Staphylococcus aureus growth. Int J Nanomed 6:1553–1558. https://doi.org/10.2147/IJN.S21729 CrossRef

Varikuti S, Oghumu S, Saljoughian N et al (2017) Topical treatment with nanoliposomal amphotericin B reduces early lesion growth but fails to induce cure in an experimental model of cutaneous leishmaniasis caused by Leishmania mexicana. Acta Trop 173:102–108. https://doi.org/10.1016/J.ACTATROPICA.2017.06.004 CrossRefPubMedPubMedCentral

Wagh VD, Deshmukh OJ (2015) Niosomes as ophthalmic drug delivery systems: a review. J Pharm Res 3:1558–1563

Whanger PD (2004) Selenium and its relationship to cancer: an update. Br J Nutr 91:11–28CrossRefPubMed

White NJ (1999) Delaying antimalarial drug resistance with combination chemotherapy. Parassitologia 41:301–308PubMed

Wijnant G-J, Van Bocxlaer K, Yardley V et al (2018) Relation between skin pharmacokinetics and efficacy in Am Bisome treatment of murine cutaneous leishmaniasis. Antimicrob Agents Chemother 62:e02009-17. https://doi.org/10.1128/aac.02009-17 CrossRefPubMedPubMedCentral

World Health Organization (2012) Research priorities for Chagas disease, human African trypanosomiasis and leishmaniasis. World Health Organ Tech Rep Ser (975):v–xii, 1–100

Yang J, Huang K, Qin S et al (2009) Antibacterial action of selenium-enriched probiotics against pathogenic Escherichia coli. Dig Dis Sci 54:246–254. https://doi.org/10.1007/s10620-008-0361-4 CrossRefPubMed

Yardley V, Croft SL (2000) A comparison of the activities of three amphotericin B lipid formulations against experimental visceral and cutaneous leishmaniasis. Int J Antimicrob Agents 13:243–248. https://doi.org/10.1016/S0924-8579(99)00133-8 CrossRefPubMed

Yazdanpanah Y, Sissoko D, Egger M et al (2004) Clinical efficacy of antiretroviral combination therapy based on protease inhibitors or non-nucleoside analogue reverse transcriptase inhibitors: indirect comparison of controlled trials. BMJ 328:249. https://doi.org/10.1136/bmj.37995.435787.A6 CrossRefPubMedPubMedCentral

Zalila H, González IJ, El-Fadili AK et al (2011) Processing of metacaspase into a cytoplasmic catalytic domain mediating cell death in Leishmania major. Mol Microbiol 79:222–239. https://doi.org/10.1111/j.1365-2958.2010.07443.x CrossRefPubMedPubMedCentral

Zhong M, Wang X, Wen J et al (2013) Selection of reference genes for quantitative gene expression studies in the house fly (Musca domestica L.) using reverse transcription quantitative real-time PCR. Acta Biochim Biophys Sin (Shanghai) 45:1069–1073. https://doi.org/10.1093/abbs/gmt111 CrossRef

Title: Leishmanicidal effects of amphotericin B in combination with selenium loaded on niosome against Leishmania tropica
Authors: Mahshid Mostafavi
Saeedeh Farajzadeh
Iraj Sharifi
Payam Khazaeli
Hamid Sharifi
Publication date: 01-06-2019
Publisher: Springer India
Keywords: Amphotericin B
Leishmania
Leishmania
Published in: Journal of Parasitic Diseases / Issue 2/2019
Print ISSN: 0971-7196
Electronic ISSN: 0975-0703
DOI: https://doi.org/10.1007/s12639-018-1071-2

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2019

Strongyloides stercoralis hyperinfection syndrome: a deeper understanding of a neglected disease

Prevalence of dirofilariasis in shepherd and stray dogs in Iranshahr, southeast of Iran

Isolated primary hydatid disease of the breast masquerading a breast tumor: report of a case and review of the literature

Surface ultrastructure, protein profile and zymography of Blastocystis species isolated from patients with colorectal carcinoma

Meteterakis asansolensis sp. nov. (Nematoda: Heterakidae) in Duttaphrynus melanostictus (Schneider, 1899) (Amphibia: Anura: Bufonidae) from Asansol coalfield area, Paschim Bardhaman, West Bengal, India

Prevalence of haemoprotozoan diseases in cattle of Cauvery delta region of Tamil Nadu

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage