Fabrication and production of conjugated neurotensin–silver nanoparticles and evaluation of its effect on pathophysiology of allergic asthma
Main Article Content
Keywords
allergy, inflammation, lung, nanoparticle
Abstract
Asthma, a respiratory tract disease, is characterized by inflammation and obstruction of airway. Inflammatory cells play a significant role in allergic asthma, and there is no complete cure for asthma. One of the new approaches in medicines is nanoparticle-base treatment. The aim of the current study is to introduce a new therapeutic approach in nano-medicine with neurotensin. Conjugated peptide nanoparticles were prepared and characterized, and then administrated to asthmatic mice. Airway hyperresponsiveness (AHR) test, broncho-alveolar lavage fluid (BALF) cells counting, cytokines level, and histopathology study were conducted. Treatment with peptide nanoparticles could control AHR, percentage of eosinophils in BALF, levels of interleukin 4 (IL-4), IL-5, and IL-33, peri-airways and perivascular eosinophilic inflammation. Producing and using of new peptide nano-drugs could introduce new therapeutic approach in controlling pathological-related mechanisms in allergic asthma.
References
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6 Jiang J, Nasab EM, Athari SM, Athari SS. Effects of vitamin E and selenium on allergic rhinitis and asthma pathophysiology. Resp Physiol Neurobiol. 2021;286:103614. 10.1016/j.resp.2020.103614
7 Haddadzadeh H., Athari SS, Hajimohammadi B. The first record of linguatulaserrata infection of two-humped camel (Camelusbacterinus) in Iran. Iran J Parasitol. 2009;4(1):59–61.
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9 Huang M, Nasab EM, Athari SS. Immunoregulatory effect of mesenchymal stem cell via mitochondria signaling pathways in allergic asthma. Saudi JBiol Sci. 2021;28:6957–6962. 10.1016/j.sjbs.2021.07.071
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11 Nasab DN, Taheri A, Athari SS. Evaluation anti-inflammatory effect of conjugated gold nanoparticles with cortistatin peptide as drug delivery to asthmatic lung tissue. Int J Peptide Res Therap. 2023;29:16. 10.1007/s10989-022-10487-x
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14 Wang D, Nasab EM, Athari SS. Study effect of baicalein encapsulated/loaded chitosan-nanoparticle on allergic asthma pathology in mouse model. Saudi J Biol Sci. 2021;28:4311–7. 10.1016/j.sjbs.2021.04.009
15 Arora P, Athari SS, Nainwal LM. Piperine attenuates production of inflammatory biomarkers, oxidative stress and neutrophils in lungs of cigarette smoke-exposed experimental mice. Food Biosci. 2022;49:101909. 10.1016/j.fbio.2022.101909
16 Nasaba EM, Atharib SM, Ghafarzadec S, Nasabd ARM, Athari SS. Immunomodulatory effects of two silymarin isomers in a Balb/c mouse model of allergic asthma. Allergol Immunopathol. 2020;48(6):646–53. 10.1016/j.aller.2020.01.003
17 Nasr M, Najlah M, D’Emanuele A, Elhissi A. PAMAM dendrimers as aerosol drug nanocarriers for pulmonary delivery via nebulization. Int J Pharm. 2014;461:242–50. 10.1016/j.ijpharm.2013.11.023
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23 Merdan T, Callahan J, Petersen H, Kunath K, Bakowsky U, Kopecková P, et al. Pegylatedpolyethylenimine-Fab′ antibody fragment conjugates for targeted gene delivery to human ovarian carcinoma cells. Bioconjug Chem. 2003;14:989–96. 10.1021/bc0340767
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26 Bivas-Benita M, Lin MY, Bal SM, Meijgaarden KEV, Franken KLMC, Friggen AH, et al. Pulmonary delivery of DNA encoding mycobacterium tuberculosis latency antigen Rv1733c associated to PLGA-PEI nanoparticles enhances T cell responses in a DNA prime/protein boost vaccination regimen in mice. Vaccine. 2009;27:4010–7. 10.1016/j.vaccine.2009.04.033
27 Pohlit H, Bellinghausen I, Frey H, Saloga J. Recent advances in the use of nanoparticles for allergen-specific immunotherapy. Allergy. 2017;72:1461–74. 10.1111/all.13199
28 Johnson L, Aglas L, Punz B, Dang H-H, Christ C, Pointner L, et al. Mechanistic insights into silica nanoparticle–allergen interactions on antigen presenting cell function in the context of allergic reactions. Nanoscale. 2023;15:2262. 10.1039/D2NR05181H
29 Jin H, Li J, Zhang M, Luo R, Lu P, Zhang W, et al. Berberine-loaded biomimetic nanoparticles attenuate inflammation of experimental allergic asthma via enhancing IL-12 Expression. Front Pharmacol. 2021;12:724525. 10.3389/fphar.2021.724525
30 da Silva AL, de Oliveira GP, Kim N, Cruz FF, Kitoko JZ, Blanco NG, et al. Nanoparticle-based thymulin gene therapy therapeutically reverses key pathology of experimental allergic asthma. Sci Adv. 2020;6:eaay7973. 10.1126/sciadv.aay7973
31 Lunin SM, Khrenov MO, Novoselova TV, Parfenyuk SB, Novoselova EG. Thymulin, a thymic peptide, prevents the overproduction of pro-inflammatory cytokines and heat shock protein Hsp70 in inflammation-bearing mice. Immunol Invest. 2008;37:858–70. 10.1080/08820130802447629
32 Lunin SM, Glushkova OV, Khrenov MO, Parfenyuk SB, Novoselova TV, Fesenko EE, et al. Thymus peptides regulate activity of RAW 264.7 macrophage cells: Inhibitory analysis and a role of signal cascades. Expert Opin Ther Targets. 2011;15:1337–46. 10.1517/14728222.2011.641952
33 Piliponsky AM, Chen CC, Nishimura T, Metz M, Rios EJ, Dobner PR, et al. Neurotensin increases mortality and mast cells reduce neurotensin levels in a mouse model of sepsis. Nat Med. 2008;14:392–8. 10.1038/nm1738
34 Law IK, Bakirtzi K, Polytarchou C, Oikonomopoulos A, Hommes D, Iliopoulos D, et al. Neurotensin-regulated miR-13 is involved in pro-inflammatory signalling in human colonic epithelial cells and in experimental colitis. Gut. 2015;64:1095–1104. 10.1136/gutjnl-2014-307329
35 Akcan A, Muhtaroglu S, Akgun H, Akyildiz H, Kucuk C, Sozuer E, et al. Ameliorative effects of bombesin and neurotensin on trinitrobenzene sulphonic acid-induced colitis, oxidative damage and apoptosis in rats. World J Gastroenterol. 2008;14:1222–30. 10.3748/wjg.14.1222
36 Robbins RA, Nelson KJ, Gossman GL, Rubinstein I. Neurotensin stimulates neutrophil adherence to bronchial epithelial cells in vitro. Life Sci. 1995;56:1353–9. 10.1016/0024-3205(95)00088-7
37 Agache I, Ciobanu C, Agache C, Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med. 2010;104:1131–7. 10.1016/j.rmed.2010.02.018
38 Dragon S, Rahman MS, Yang J, Unruh H, Halayko AJ, Gounni AS. IL-17 enhances IL-1beta-mediated CXCL-8 release from human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2007;292:L1023–9. 10.1152/ajplung.00306.2006
39 Hou C, Sun F, Liang Y, Nasab EM, Athari SS. Effect of transduced mesenchymal stem cells with IL-10 gene on control of allergic asthma. Allergol Immunopathol (Madr). 2023;51(2):45–51. 10.15586/aei.v51i2.789
40 Moghaddasi K, Hesaraki S, Arfaee F, Athari SS. Investigating the effect of mesenchymal stem cells on the rate of clinical and pathological improvement of asthmatic lung in mouse model. Regen Ther. 2024;25:157–61. 10.1016/j.reth.2023.12.013
41 Vacca P, Carbone R, Monselise A, Grosso M, Bottino G. Neurotensin pulmonary metabolism in normal and asthmatic subjects. Eur Rev Med Pharmacol Sci. 2003;7:75–80.
42 Alysandratos K-D, Asadi S, Angelidou A, Zhang B, Sismanopoulos N, Yang H, et al. Neurotensin and CRH interactions augment human mast cell activation. PLoS One. 2012;7(11):e48934. 10.1371/journal.pone.0048934
43 Lauritano D, Mastrangelo F, D’Ovidio C, Ronconi G, Caraffa A, Gallenga CE, et al. Activation of mast cells by neuropeptides: The role of pro-inflammatory and anti-inflammatory cytokines. Int J Mol Sci. 2023;24(5):4811. 10.3390/ijms24054811
2 Esmaeilzadeh A, Tahmasebi S, Athari SS. Chimeric antigen receptor-T cell therapy: Applications and challenges in treatment of allergy and asthma. Biomed Pharmacother. 2020;123:109685. 10.1016/j.biopha.2019.109685
3 Athari SM, Mehrabi Nasab E, Athari SS. Study effect of ocimumbasilicum seeds on mucus production and cytokine gene expression in allergic asthma mice model. Rev Fr Allergol. 2018;58(7):489–93. 10.1016/j.reval.2018.08.003
4 Athari SS, Athari SM. The importance of eosinophil, platelet and dendritic cell in asthma. Asian Pac J Trop Dis. 2014;4(1): 41–7. 10.1016/S2222-1808(14)60413-8
5 Lankarani KB, Honarvar B, Athari SS. The mechanisms underlying helicobacter pylori-mediated protection against allergic asthma. Tanaffos. 2017;16(4):251–9.
6 Jiang J, Nasab EM, Athari SM, Athari SS. Effects of vitamin E and selenium on allergic rhinitis and asthma pathophysiology. Resp Physiol Neurobiol. 2021;286:103614. 10.1016/j.resp.2020.103614
7 Haddadzadeh H., Athari SS, Hajimohammadi B. The first record of linguatulaserrata infection of two-humped camel (Camelusbacterinus) in Iran. Iran J Parasitol. 2009;4(1):59–61.
8 Nasab EM, Athari SM, Motlagh B, Athari SS. Effects of oral administration of ocimumbasilicum on goblet cell hyperplasia and upstream cytokine gene expression in allergic asthma. Rev Fr Allergol. 2020;60:64–68. 10.1016/j.reval.2019.02.226
9 Huang M, Nasab EM, Athari SS. Immunoregulatory effect of mesenchymal stem cell via mitochondria signaling pathways in allergic asthma. Saudi JBiol Sci. 2021;28:6957–6962. 10.1016/j.sjbs.2021.07.071
10 Wang L, Feng M, Li Q, Qiu C, Chen R. Advances in nanotechnology and asthma. Ann Transl Med. 2019;7(8):180. 10.21037/atm.2019.04.62
11 Nasab DN, Taheri A, Athari SS. Evaluation anti-inflammatory effect of conjugated gold nanoparticles with cortistatin peptide as drug delivery to asthmatic lung tissue. Int J Peptide Res Therap. 2023;29:16. 10.1007/s10989-022-10487-x
12 Athari SS, Pourpak Z, Folkerts G, Garssen J, Moin M, Adcock IM, et al. Conjugated alpha-alumina nanoparticle with vasoactive intestinal peptide as a nano-drug in treatment of allergic asthma in mice. Eur J Pharmacol. 2016;791:811–20. 10.1016/j.ejphar.2016.10.014
13 Russjan E, Kaczynska K. Beneficial effects of neurotensin in murine model of hapten-induced asthma. Int J Mol Sci. 2019;20:5025. 10.3390/ijms20205025
14 Wang D, Nasab EM, Athari SS. Study effect of baicalein encapsulated/loaded chitosan-nanoparticle on allergic asthma pathology in mouse model. Saudi J Biol Sci. 2021;28:4311–7. 10.1016/j.sjbs.2021.04.009
15 Arora P, Athari SS, Nainwal LM. Piperine attenuates production of inflammatory biomarkers, oxidative stress and neutrophils in lungs of cigarette smoke-exposed experimental mice. Food Biosci. 2022;49:101909. 10.1016/j.fbio.2022.101909
16 Nasaba EM, Atharib SM, Ghafarzadec S, Nasabd ARM, Athari SS. Immunomodulatory effects of two silymarin isomers in a Balb/c mouse model of allergic asthma. Allergol Immunopathol. 2020;48(6):646–53. 10.1016/j.aller.2020.01.003
17 Nasr M, Najlah M, D’Emanuele A, Elhissi A. PAMAM dendrimers as aerosol drug nanocarriers for pulmonary delivery via nebulization. Int J Pharm. 2014;461:242–50. 10.1016/j.ijpharm.2013.11.023
18 Nasab EM, Makoei RHZ, Aghajani H, Athari SS. IL-33/ST2 pathway as upper-hand of inflammation in allergic asthma contributes as predictive biomarker in heart failure. ESC Heart Fail. 2022;9(6):3785–90. 10.1002/ehf2.14111
19 Kenyon NJ, Bratt JM, Lee J, Luo J, Franzi LM, Zeki AA, et al. Self-assembling nanoparticles containing dexamethasone as a novel therapy in allergic airways inflammation. PLoS One. 2013;8:e77730. 10.1371/journal.pone.0077730
20 Jackson JK, Zhang X, Llewellen S, Hunter WL, Burt HM. The characterization of novel polymeric paste formulations for intratumoral delivery. Int J Pharm. 2004;270:185–98. 10.1016/j.ijpharm.2003.10.010
21 Bao X-H, Gao F, Athari SS, Wang H. Immunomodulatory effect of IL-35 gene-transfected mesenchymal stem cells on allergic asthma. Fundam Clin Pharmacol. 2023;37(1):116–24. 10.1111/fcp.12823
22 Di Gioia S, Trapani A, Castellani S, Carbone A, Belgiovine G, Craparo EF, et al. Nanocomplexes for gene therapy of respiratory diseases: Targeting and overcoming the mucus barrier. Pulm Pharmacol Ther. 2015;34:8–24. 10.1016/j.pupt.2015.07.003
23 Merdan T, Callahan J, Petersen H, Kunath K, Bakowsky U, Kopecková P, et al. Pegylatedpolyethylenimine-Fab′ antibody fragment conjugates for targeted gene delivery to human ovarian carcinoma cells. Bioconjug Chem. 2003;14:989–96. 10.1021/bc0340767
24 Köping-Höggård M, Tubulekas I, Guan H, Edwards K, Nilsson M, Vårum KM, et al. Chitosan as a nonviral gene delivery system. Structure-property relationships and characteristics compared with polyethylenimine in vitro and after lung administration in vivo. Gene Ther. 2001;8:1108–21. 10.1038/sj.gt.3301492
25 Rudolph C, Lausier J, Naundorf S, Müller RH, Rosenecker J. In vivo gene delivery to the lung using polyethylenimine and fractured polyamidoamine dendrimers. J Gene Med. 2000;2:269–78. 10.1002/1521-2254(200007/08)2:4<269::AID-JGM112>3.0.CO;2-F
26 Bivas-Benita M, Lin MY, Bal SM, Meijgaarden KEV, Franken KLMC, Friggen AH, et al. Pulmonary delivery of DNA encoding mycobacterium tuberculosis latency antigen Rv1733c associated to PLGA-PEI nanoparticles enhances T cell responses in a DNA prime/protein boost vaccination regimen in mice. Vaccine. 2009;27:4010–7. 10.1016/j.vaccine.2009.04.033
27 Pohlit H, Bellinghausen I, Frey H, Saloga J. Recent advances in the use of nanoparticles for allergen-specific immunotherapy. Allergy. 2017;72:1461–74. 10.1111/all.13199
28 Johnson L, Aglas L, Punz B, Dang H-H, Christ C, Pointner L, et al. Mechanistic insights into silica nanoparticle–allergen interactions on antigen presenting cell function in the context of allergic reactions. Nanoscale. 2023;15:2262. 10.1039/D2NR05181H
29 Jin H, Li J, Zhang M, Luo R, Lu P, Zhang W, et al. Berberine-loaded biomimetic nanoparticles attenuate inflammation of experimental allergic asthma via enhancing IL-12 Expression. Front Pharmacol. 2021;12:724525. 10.3389/fphar.2021.724525
30 da Silva AL, de Oliveira GP, Kim N, Cruz FF, Kitoko JZ, Blanco NG, et al. Nanoparticle-based thymulin gene therapy therapeutically reverses key pathology of experimental allergic asthma. Sci Adv. 2020;6:eaay7973. 10.1126/sciadv.aay7973
31 Lunin SM, Khrenov MO, Novoselova TV, Parfenyuk SB, Novoselova EG. Thymulin, a thymic peptide, prevents the overproduction of pro-inflammatory cytokines and heat shock protein Hsp70 in inflammation-bearing mice. Immunol Invest. 2008;37:858–70. 10.1080/08820130802447629
32 Lunin SM, Glushkova OV, Khrenov MO, Parfenyuk SB, Novoselova TV, Fesenko EE, et al. Thymus peptides regulate activity of RAW 264.7 macrophage cells: Inhibitory analysis and a role of signal cascades. Expert Opin Ther Targets. 2011;15:1337–46. 10.1517/14728222.2011.641952
33 Piliponsky AM, Chen CC, Nishimura T, Metz M, Rios EJ, Dobner PR, et al. Neurotensin increases mortality and mast cells reduce neurotensin levels in a mouse model of sepsis. Nat Med. 2008;14:392–8. 10.1038/nm1738
34 Law IK, Bakirtzi K, Polytarchou C, Oikonomopoulos A, Hommes D, Iliopoulos D, et al. Neurotensin-regulated miR-13 is involved in pro-inflammatory signalling in human colonic epithelial cells and in experimental colitis. Gut. 2015;64:1095–1104. 10.1136/gutjnl-2014-307329
35 Akcan A, Muhtaroglu S, Akgun H, Akyildiz H, Kucuk C, Sozuer E, et al. Ameliorative effects of bombesin and neurotensin on trinitrobenzene sulphonic acid-induced colitis, oxidative damage and apoptosis in rats. World J Gastroenterol. 2008;14:1222–30. 10.3748/wjg.14.1222
36 Robbins RA, Nelson KJ, Gossman GL, Rubinstein I. Neurotensin stimulates neutrophil adherence to bronchial epithelial cells in vitro. Life Sci. 1995;56:1353–9. 10.1016/0024-3205(95)00088-7
37 Agache I, Ciobanu C, Agache C, Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med. 2010;104:1131–7. 10.1016/j.rmed.2010.02.018
38 Dragon S, Rahman MS, Yang J, Unruh H, Halayko AJ, Gounni AS. IL-17 enhances IL-1beta-mediated CXCL-8 release from human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2007;292:L1023–9. 10.1152/ajplung.00306.2006
39 Hou C, Sun F, Liang Y, Nasab EM, Athari SS. Effect of transduced mesenchymal stem cells with IL-10 gene on control of allergic asthma. Allergol Immunopathol (Madr). 2023;51(2):45–51. 10.15586/aei.v51i2.789
40 Moghaddasi K, Hesaraki S, Arfaee F, Athari SS. Investigating the effect of mesenchymal stem cells on the rate of clinical and pathological improvement of asthmatic lung in mouse model. Regen Ther. 2024;25:157–61. 10.1016/j.reth.2023.12.013
41 Vacca P, Carbone R, Monselise A, Grosso M, Bottino G. Neurotensin pulmonary metabolism in normal and asthmatic subjects. Eur Rev Med Pharmacol Sci. 2003;7:75–80.
42 Alysandratos K-D, Asadi S, Angelidou A, Zhang B, Sismanopoulos N, Yang H, et al. Neurotensin and CRH interactions augment human mast cell activation. PLoS One. 2012;7(11):e48934. 10.1371/journal.pone.0048934
43 Lauritano D, Mastrangelo F, D’Ovidio C, Ronconi G, Caraffa A, Gallenga CE, et al. Activation of mast cells by neuropeptides: The role of pro-inflammatory and anti-inflammatory cytokines. Int J Mol Sci. 2023;24(5):4811. 10.3390/ijms24054811