Immune and Antioxidant Enzyme Response of Longfin Yellowtail (Seriola rivoliana) Juveniles to Ultra-diluted Substances Derived from Phosphorus, Silica and Pathogenic Vibrio

Abstract

Background This research aimed to observe the effect of homeopathic treatments prepared from Vibrio parahaemolyticus and V. alginolyticus (H1) and commercial homeopathic medication Phosphoricum acidum and Silicea terra (H2) on the immune and antioxidant response in Seriola rivoliana juveniles under usual culture conditions and challenged with V. parahaemolyticus.

Materials and Methods Quantitative polymerase chain reaction analysis was used to study changes in the expression of key genes related to immune response, cytokines (interleukin-1β [IL-1β]), adapter protein for cytokine release (MyD88) and piscidin and spectrophotometric techniques to analyze the activity of antioxidant superoxide dismutase (SOD) and catalase (CAT) enzymes in Seriola rivoliana juveniles at 30 (weaning stage [WS]) and 60 (early juveniles [EJ]) days post-hatching.

Results The H1 treatment led to over-expression of the IL-1β and MyD88 genes in fish at WS and EJ with respect to control, contrary to the H2 treatment that led to under-expression of the IL-1β, MyD88 and piscidin genes at the EJ stage. In fish challenged with V. parahaemolyticus, both H1 and H2 led to over-expression of IL-1β and MyD88; H2 caused an over-expression of piscidin. The SOD activity was higher in H1 with respect to H2 and the control group. CAT remained relatively stable with both H1 and H2 treatments.

Conclusions The results suggest that the overall effect of H1 was due to the presence of unknown antigens in low concentrations, while the response to H2—specifically during challenge—may have been due to a stimulating effect of nano-structures, prevailing from mother tincture after sequential dilution/succussion, in a pathway similar to that attributed to nano-vaccines.

Keywords

aquacultural homeopathy - cytokines - piscidin - MyD88 - Seriola rivoliana

Highlights

• Effect of two homeopathic treatments on immune and antioxidant response in Seriola rivoliana was evaluated.

• Homeopathy generated from Vibrio pathogenic strains caused stimulation of immune system in Seriola rivoliana.

• The expression of MyD88 and IL-1β by nosode seems to initiate a cascade of intracellular signaling initiated by the recognition of a PAMP by the TLR-like receptor.

• References

• 1 Teles A, Salas-Leiva J, Alvarez-González CA. , et al. Histological study of the gastrointestinal tract in longfin yellowtail (Seriola rivoliana) larvae. Fish Physiol Biochem 2017; 43: 1613-1628
• 2 Kissinger KR, García-Ortega A, Trushenski JT. Partial fish meal replacement by soy protein concentrate, squid and algal meals in low fish-oil diets containing Schizochytrium limacinum for longfin yellowtail Seriola rivoliana . Aquaculture 2016; 452: 37-44
• 3 Benitez-Hernández A, Jiménez-Bárcenas SPL, Sánchez-Gutiérrez EY. , et al. Use of marine by-product meals in diets for juvenile longfin yellowtail Seriola rivoliana . Aquacult Nutr 2018; 24: 562-570
• 4 Le Du J, Tovar-Ramírez D, Núñez-Vázquez EJ. Embryotoxic effects of dissolved okadaic acid on the development of Longfin yellowtail Seriola rivoliana . Aquat Toxicol 2017; 190: 210-216
• 5 Mesa-Rodríguez A, Hernández-Cruz CM, Betancor MB, Fernández-Palacios H, Izquierdo MS, Roo J. Bone development of the skull, pectoral and pelvic fins in Seriola rivoliana (Valenciennes, 1833) larvae. Fish Physiol Biochem 2016; 42: 1777-1789
• 6 Roo J, Fernández-Palacios H, Hernández-Cruz CM, Mesa-Rodriguez A, Schuchardt D, Izquierdo M. First results of spawning and larval rearing of longfin yellowtail Seriola rivoliana as a fast-growing candidate for European marine finfish aquaculture diversification. Aquacult Res 2014; 45: 689-700
• 7 Roo J, Fernández-Palacios H, Schuchardt D, Hernández-Cruz CM, Izquierdo MS. Influence of hormonal induction and broodstock feeding on longfin yellowtail Seriola rivoliana maturation, spawning quality and egg biochemical composition. Aquacult Nutr 2015; 21: 614-624
• 8 Muncaster S, Kraakman K, Gibbons O. , et al. Antimicrobial peptides within the Yellowtail Kingfish (Seriola lalandi). Dev Comp Immunol 2018; 80: 67-80
• 9 Reyes-Becerril M, Ascencio-Valle F, Hirono I. , et al. TLR21's agonists in combination with Aeromonas antigens synergistically up-regulate functional TLR21 and cytokine gene expression in yellowtail leucocytes. Dev Comp Immunol 2016; 61: 107-115
• 10 Harikrishnan R, Balasundaram C, Heo MS. Impact of plant products on innate and adaptive immune system of cultured finfish and shellfish. Aquaculture 2011; 317: 1-15
• 11 Randelli E, Buonocore F, Scapigliati G. Cell markers and determinants in fish immunology. Fish Shellfish Immunol 2008; 25: 326-340
• 12 Hossain MS, Koshio S, Ishikawa M. , et al. Effects of dietary administration of inosine on growth, immune response, oxidative stress and gut morphology of juvenile amberjack, Seriola dumerili . Aquaculture 2017; 468: 534-544
• 13 Cabello FC. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 2006; 8: 1137-1144
• 14 Mazón-Suástegui JM, García-Bernal M, Saucedo PE, Campa-Córdova Á, Abasolo-Pacheco F. Homeopathy outperforms antibiotics treatment in juvenile scallop Argopecten ventricosus: effects on growth, survival, and immune response. Homeopathy 2017; 106: 18-26
• 15 Ortiz-Cornejo NL, Tovar-Ramírez D, Abasolo-Pacheco F, Mazón-Suástegui JM. Homeopatía, una alternativa para la acuicultura. Rev Médica Homeopat 2017; 10: 18-24
• 16 de Oliveira CC, de Oliveira SM, Godoy LMF, Gabardo J, Buchi Dde F. Canova, a Brazilian medical formulation, alters oxidative metabolism of mice macrophages. J Infect 2006; 52: 420-432
• 17 de Oliveira CC, de Oliveira SM, Goes VM, Probst CM, Krieger MA, Buchi DdeF. Gene expression profiling of macrophages following mice treatment with an immunomodulator medication. J Cell Biochem 2008; 104: 1364-1377
• 18 Feio DC, Muniz JA, Montenegro RC, Burbano RR, De Brito Junior LC, De Lima PD. Evaluation of the immunological cellular response of Cebus apella exposed to the carcinogen N-methyl-N-nitrosourea and treated with CANOVA®. In Vivo 2014; 28: 837-841
• 19 Leal MF, Antunes LM, Lamarão MF. , et al. The protective effect of Canova homeopathic medicine in cyclophosphamide-treated non-human primates. Food Chem Toxicol 2012; 50: 4412-4420
• 20 Rodrigues de Santana F, Coelho CP, Cardoso TN, Laurenti MD, Perez Hurtado EC, Bonamin LV. Modulation of inflammation response to murine cutaneous Leishmaniosis by homeopathic medicines: thymulin 5cH. Homeopathy 2014; 103: 275-284
• 21 Smit E, Oberholzer HM, Pretorius E. A review of immunomodulators with reference to Canova. Homeopathy 2009; 98: 169-176
• 22 Mazón-Suástegui J, Tovar-Ramírez D, Salas-Leiva J. , et al. Aquacultural homeopathy: a focus on marine species. In: Diarte-Plata G. , ed. Aquaculture - Plants and Invertebrates. London: IntechOpen; 2018. . In Press
• 23 Jokinen EI, Vielma J, Aaltonen TM, Koskela J. The effect of dietary phosphorus deficiency on the immune responses of European whitefish (Coregonus lavaretus L.). Fish Shellfish Immunol 2003; 15: 159-168
• 24 Nielsen FH. A novel silicon complex is as effective as sodium metasilicate in enhancing the collagen-induced inflammatory response of silicon-deprived rats. J Trace Elem Med Biol 2008; 22: 39-49
• 25 Cheesman SE, Neal JT, Mittge E, Seredick BM, Guillemin K. Epithelial cell proliferation in the developing zebrafish intestine is regulated by the Wnt pathway and microbial signaling via Myd88. Proc Natl Acad Sci U S A 2011; 108 (Suppl. 01) 4570-4577
• 26 Yan B, Han P, Pan L. , et al. IL-1β and reactive oxygen species differentially regulate neutrophil directional migration and Basal random motility in a zebrafish injury-induced inflammation model. J Immunol 2014; 192: 5998-6008
• 27 Kono T, Fujiki K, Nakao M, Yano T, Endo M, Sakai M. The immune responses of common carp, Cyprinus carpio L., injected with carp interleukin-1β gene. J Interferon Cytokine Res 2002; 22: 413-419
• 28 Zou J, Secombes CJ. The function of fish cytokines. Biology (Basel) 2016; 5: 1-35
• 29 Masso-Silva JA, Diamond G. Antimicrobial peptides from fish. Pharmaceuticals (Basel) 2014; 7: 265-310
• 30 Du Y, Yi M, Xiao P. , et al. The impact of Aeromonas salmonicida infection on innate immune parameters of Atlantic salmon (Salmo salar L). Fish Shellfish Immunol 2015; 44: 307-315
• 31 Martínez-Álvarez RM, Morales AE, Sanz A. Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish 2005; 15: 75-88
• 32 Elia V, Baiano S, Duro I, Napoli E, Niccoli M, Nonatelli L. Permanent physico-chemical properties of extremely diluted aqueous solutions of homeopathic medicines. Homeopathy 2004; 93: 144-150
• 33 Bellavite P, Signorini A. The Emerging Science of Homeopathy. Complexity, Biodynamics, and Nanopharmacology. 2nd ed. Berkeley, CA: North Atlantic Books; 2002
• 34 Upadhyay RP. The possible mechanism of memory through nanoparticles and exclusion zones. Water 2017; 7: 158-176
• 35 Basu A, Suresh AK, Kane SG, Bellare JR. A review of machines and devices to potentize homeopathic medicines. Homeopathy 2017; 106 (04) 240-249
• 36 Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254
• 37 Eyckmans M, Celis N, Horemans N, Blust R, De Boeck G. Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species. Aquat Toxicol 2011; 103: 112-120
• 38 Clairborne A. Catalase activity. Greenwald, RA CRC Handb methods oxyg radic. Res CRC Press; 1985: 283-284
• 39 Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−ΔΔC(T)) method. Methods 2001; 25: 402-408
• 40 Augimeri RV, Strap JL. The phytohormone ethylene enhances cellulose production, regulates CRP/FNRKx transcription and causes differential gene expression within the bacterial cellulose synthesis operon of Komagataeibacter (Gluconacetobacter) xylinus ATCC 53582. Front Microbiol 2015; 6: 1459
• 41 Leung TLF, Bates AE. More rapid and severe disease outbreaks for aquaculture at the tropics: implications for food security. J Appl Ecol 2013; 50: 215-222
• 42 Zhang Q, Dong X, Chen B, Zhang Y, Zu Y, Li W. Zebrafish as a useful model for zoonotic Vibrio parahaemolyticus pathogenicity in fish and human. Dev Comp Immunol 2016; 55: 159-168
• 43 Reyes-Becerril M, Maldonado-García M, Guluarte C. , et al. Evaluation of ToxA and Vibrio parahaemolyticus lysate on humoral immune response and immune-related genes in Pacific red snapper. Fish Shellfish Immunol 2016; 56: 310-321
• 44 Reyes-Becerril M, Alamillo E, Rosales-Mendoza S, Ascencio F, Esteban MA, Angulo C. Molecular characterization and expression analyses of toll like receptor-5 induced by Vibrio parahaemolyticus antigens in Pacific red snapper. Fish Shellfish Immunol 2017; 68: 180-189
• 45 Parra D, Reyes-Lopez FE, Tort L. Mucosal immunity and B cells in teleosts: effect of vaccination and stress. Front Immunol 2015; 6: 354
• 46 Joshi S, Mukerjee S, Vaidya S, Talele G, Chowdhary A, Shah R. Preparation, standardization and in vitro safety testing of Mycobacterium nosodes (Emtact- polyvalent nosode). Homeopathy 2016; 105: 225-232
• 47 Passeti TA, Bissoli LR, Macedo AP, Libame RB, Diniz S, Waisse S. Action of antibiotic oxacillin on in vitro growth of methicillin-resistant Staphylococcus aureus (MRSA) previously treated with homeopathic medicines. Homeopathy 2017; 106: 27-31
• 48 Bell IR, Sarter B, Koithan M. , et al. Integrative nanomedicine: treating cancer with nanoscale natural products. Glob Adv Health Med 2014; 3: 36-53
• 49 Mondal J, Das J, Shah R, Khuda-Bukhsh AR. A homeopathic nosode, Hepatitis C 30 demonstrates anticancer effect against liver cancer cells in vitro by modulating telomerase and topoisomerase II activities as also by promoting apoptosis via intrinsic mitochondrial pathway. J Integr Med 2016; 14: 209-218
• 50 Aleixo DL, Ferraz FN, Ferreira ÉC. , et al. Highly diluted medication reduces parasitemia and improves experimental infection evolution by Trypanosoma cruzi . BMC Res Notes 2012; 5: 352
• 51 Doehring C, Sundrum A. Efficacy of homeopathy in livestock according to peer-reviewed publications from 1981 to 2014. Vet Rec 2016; 179: 628
• 52 Sandri P, Aleixo DL, Sanchez Falkowski GJ. , et al. Trypanosoma cruzi: biotherapy made from trypomastigote modulates the inflammatory response. Homeopathy 2015; 104: 48-56
• 53 Saha SK, Roy S, Khuda-Bukhsh AR. Ultra-highly diluted plant extracts of Hydrastis canadensis and Marsdenia condurango induce epigenetic modifications and alter gene expression profiles in HeLa cells in vitro. J Integr Med 2015; 13: 400-411
• 54 Heine H, Schmolz M. Immunoregulation via ‘bystander suppression’ needs minute amounts of substances--a basis for homeopathic therapy?. Med Hypotheses 2000; 54: 392-393
• 55 Khuda-Bukhsh AR. Current trends in high dilution research with particular reference to gene regulatory hypothesis. Nucl 2014; 57: 3-17
• 56 Montalban-Arques A, De Schryver P, Bossier P. , et al. Selective manipulation of the gut microbiota improves immune status in vertebrates. Front Immunol 2015; 6: 512
• 57 Katzenback BA. Antimicrobial peptides as mediators of innate immunity in teleosts. Biology (Basel) 2015; 4: 607-639
• 58 Noga EJ, Silphaduang U. Piscidins: a novel family of peptide antibiotics from fish. Drug News Perspect 2003; 16: 87-92
• 59 Corrales J, Mulero I, Mulero V, Noga EJ. Detection of antimicrobial peptides related to piscidin 4 in important aquacultured fish. Dev Comp Immunol 2010; 34: 331-343
• 60 Mulero I, Noga EJ, Meseguer J, García-Ayala A, Mulero V. The antimicrobial peptides piscidins are stored in the granules of professional phagocytic granulocytes of fish and are delivered to the bacteria-containing phagosome upon phagocytosis. Dev Comp Immunol 2008; 32: 1531-1538
• 61 Campagna S, Saint N, Molle G, Aumelas A. Structure and mechanism of action of the antimicrobial peptide piscidin. Biochemistry 2007; 46: 1771-1778
• 62 Bigagli E, Luceri C, Bernardini S, Dei A, Filippini A, Dolara P. Exploring the effects of homeopathic Apis mellifica preparations on human gene expression profiles. Homeopathy 2014; 103: 127-132
• 63 Bellavite P, Marzotto M, Olioso D. , et al. Cellular and transcriptional responses of SH-SY5Y human neurocytes following in vitro exposure to Gelsemium sempervirens . Int J High Dilution Res 2012; 11: 144-146
• 64 Bell IR, Schwartz GE. Enhancement of adaptive biological effects by nanotechnology preparation methods in homeopathic medicines. Homeopathy 2015; 104: 123-138
• 65 Zhou X, Tian Z, Wang Y, Li W. Effect of treatment with probiotics as water additives on tilapia (Oreochromis niloticus) growth performance and immune response. Fish Physiol Biochem 2010; 36: 501-509
• 66 Tovar-Ramírez D, Mazurais D, Gatesoupe JF, Quazuguel P, Cahu CL, Zambonino-Infante JL. Dietary probiotic live yeast modulates antioxidant enzyme activities and gene expression of sea bass (Dicentrarchus labrax) larvae. Aquaculture 2010; 300: 142-147
• 67 Yang D, Elner SG, Bian ZM, Till GO, Petty HR, Elner VM. Pro-inflammatory cytokines increase reactive oxygen species through mitochondria and NADPH oxidase in cultured RPE cells. Exp Eye Res 2007; 85: 462-472
• 68 Stoliar O, Lushchak V. Environmental pollution and oxidative stress in fish, oxidative stress-Environmental Induction and Dietary Antioxidants, Dr. Volodymyr Lushchak, ed. ISBN: 978-953-51-0553-4 InTech 2012; doi:10.5772/38094. Available at: https://www.intechopen.com/books/oxidative-stress-environmental-induction-and-dietary-antioxidants/environmental-pollution-and-oxidative-stress-in-fish
• 69 Wang J, Zhu X, Huang X, Gu L, Chen Y, Yang Z. Combined effects of cadmium and salinity on juvenile Takifugu obscurus: cadmium moderates salinity tolerance; salinity decreases the toxicity of cadmium. Sci Rep 2016; 6: 30968
• 70 Guzmán-Villanueva LT, Ascencio-Valle F, Macías-Rodríguez ME, Tovar-Ramírez D. Effects of dietary β-1,3/1,6-glucan on the antioxidant and digestive enzyme activities of Pacific red snapper (Lutjanus peru) after exposure to lipopolysaccharides. Fish Physiol Biochem 2014; 40: 827-837
• 71 Carvalho SC, Bernusso VA, Espíndola EL, Fernandes MN. Biomarker responses as indication of contaminant effects in Oreochromis niloticus. Chemosphere 2012; 89: 60-69
• 72 Guedes JRP, Bonamin LV, Capelozzi VL. Water-related mechanisms proposed for storing and transmitting homeopathic information: putative links with biological responses. Homeopathy 2018; 107: 172-180
• 73 Chikramane PS, Suresh AK, Bellare JR, Kane SG. Extreme homeopathic dilutions retain starting materials: a nanoparticulate perspective. Homeopathy 2010; 99 (04) 231-242
• 74 Chikramane PS, Kalita D, Suresh AK, Kane SG, Bellare JR. Why extreme dilutions reach non-zero asymptotes: a nanoparticulate hypothesis based on froth flotation. Langmuir 2012; 28: 15864-15875
• 75 Jiao Q, Li L, Mu Q, Zhang Q. Immunomodulation of nanoparticles in nanomedicine applications. BioMed Res Int 2014; 2014: 426028
• 76 Morishige T, Yoshioka Y, Inakura H. , et al. Suppression of nanosilica particle-induced inflammation by surface modification of the particles. Arch Toxicol 2012; 86: 1297-1307
• 77 Morishige T, Yoshioka Y, Inakura H. , et al. The effect of surface modification of amorphous silica particles on NLRP3 inflammasome mediated IL-1β production, ROS production and endosomal rupture. Biomaterials 2010; 31: 6833-6842
• 78 Delaval M, Boland S, Solhonne B. , et al. Acute exposure to silica nanoparticles enhances mortality and increases lung permeability in a mouse model of Pseudomonas aeruginosa pneumonia. Part Fibre Toxicol 2015; 12: 1
• 79 Tsugita M, Morimoto N, Nakayama M. SiO₂ and TiO₂ nanoparticles synergistically trigger macrophage inflammatory responses. Part Fibre Toxicol 2017; 14: 11
• 80 Zhang Y, Lin Y, Li X. , et al. Silica dioxide nanoparticles combined with cold exposure induce stronger systemic inflammatory response. Environ Sci Pollut Res Int 2017; 24: 291-298
• 81 Boraschi D, Italiani P. From Antigen delivery system to adjuvanticy: the board application of nanoparticles in vaccinology. Vaccines (Basel) 2015; 3: 930-939
• 82 Rider P, Carmi Y, Guttman O. , et al. IL-1α and IL-1β recruit different myeloid cells and promote different stages of sterile inflammation. J Immunol 2011; 187: 4835-4843