Advertisement

Journal of Applied Phycology

, Volume 31, Issue 2, pp 1415–1424 | Cite as

Diets enriched in red seaweed (Pyropia columbina and Gracilaria chilensis) cryo concentrates modulate the immune-relevant gene encoding the Mx antiviral protein in salmon (Salmo salar) white blood cells

  • Ivonne Lozano MuñozEmail author
  • Jurij Wacyk
  • Claudio Perez
  • Jaime Carrasco
  • Marcelo Cortez-San Martin
Article

Abstract

Pharmacotherapy has long been used to control viral diseases. However, its success is questionable because its use can negatively impact environmental and human health. An alternative solution is the use of functional foods and diets containing natural products, which tend to be more biodegradable than synthetic molecules and are less likely to generate resistance. Seaweed contains biologically active macronutrients and minerals that offer a natural alternative to synthetic molecules. Red seaweeds, in particular, are a rich source of anti-viral compounds. This study aimed to evaluate the effect of two edible red seaweeds, Pyropia columbina and Gracilaria chilensis cryo concentrates (RSCC), on the gene transcription levels in leukocyte proteins involved in antiviral response (INFγ, Mx, interleukin-6, cathelicidin, and lysozyme). The RSCCs were fed to fish (Salmo salar L.) at concentrations of 0.1, 1, or 10 g kg−1 for 56 days, and blood samples were collected at 8 weeks. The transcription levels of key genes associated with the antiviral response were analyzed by qRT-PCR using leukocyte mRNA as template. The Mx transcript level was significantly decreased (p < 0.05) with the RSCC diets, and lysozyme transcript levels were significantly increased (1 g kg−1P. columbina cryo concentrate). Cathelicidin, interleukin-6, and INFɣ had stable transcription levels. Importantly, RSCC modulated the immune-relevant gene that encodes the Mx antiviral protein in white blood cells.

Keywords

Red seaweed concentrates Pyropia columbina Gracilaria chilensis Mx antiviral protein Lysozyme Functional ingredient Salmo salar 

Notes

Acknowledgments

This study was supported by Laboratorio de Genética y Biotecnología, Facultad de Ciencias Agronómicas, Universidad de Chile and BioMar Chile S.A.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Ahmadi PY, Farahmand H, Miandare HK, Mirvaghefi A, Hoseinifar SH (2014) The effects of dietary Immunogen® on innate immune response, immune related genes expression and disease resistance of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 37:209–214Google Scholar
  2. Alés E, Tabares L, Poyato JM, Valero V, Lindau M, Alvarez de Toledo G (1999) High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat Cell Biol 1:40–44CrossRefGoogle Scholar
  3. Asif MB, Hai FI, Price WE, Nghiem LD (2018) Impact of pharmaceutically active compounds in marine environment on aquaculture. In: HAI FI, Visavanathan C, Boopathy R (eds) Sustainable Aquaculture. Springer, Cham, pp 265–299CrossRefGoogle Scholar
  4. Bi GQ, Alderton JM, Steinhardt RA (1995) Calcium-regulated exocytosis is required for cell membrane resealing. J Cell Biol 131:1747–1758CrossRefGoogle Scholar
  5. Boulho R, Marty C, Freile-Pelegrín Y, Robledo D, Bourgougnon N, Bedoux G (2017) Antiherpetic (HSV-1) activity of carrageenans from the red seaweed Solieria chordalis (Rhodophyta, Gigartinales) extracted by microwave-assisted extraction (MAE). J Appl Phycol 29:2219–2228CrossRefGoogle Scholar
  6. Broekman DC, Guḥmundsson GH, Maier VH (2013) Differential regulation of cathelicidin in salmon and cod. Fish Shellfish Immunol 35:532–538CrossRefGoogle Scholar
  7. Cantley LC, Cantley LG, Josephson L (1978) A characterization of vanadate interactions with the (Na,K)-ATPase. Mechanistic and regulatory implications J Biol Chem 253:7361–7368Google Scholar
  8. Castilla V, Sepúlveda CS, García CC, Damonte EB (2017) Progress for antiviral development in Latin America. In: Ludert JE, Pujol FH, Arbiza J (eds) Human virology in Latin America. Springer, Cham, pp 439–460CrossRefGoogle Scholar
  9. Chang CI, Zhang YA, Zou J, Nie P, Secombes CJ (2006) Two cathelicidin genes are present in both rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Antimicrob Agents Chemother 50:185–195CrossRefGoogle Scholar
  10. Chen C, Sun B, Guan W, Bi Y, Li P, Ma J, Chen F, Pan Q, Xie Q (2016) N-3 essential fatty acids in Nile tilapia, Oreochromis niloticus: effects of linolenic acid on non-specific immunity and anti-inflammatory responses in juvenile fish. Aquaculture 450:250–257CrossRefGoogle Scholar
  11. Das BK, Ellis AE, Collet B (2009) Induction and persistence of mx protein in tissues, blood and plasma of Atlantic salmon parr, Salmo salar, injected with poly I:C. Fish Shellfish Immunol 26:40–48CrossRefGoogle Scholar
  12. Dienz O, Rud JG, Eaton SM, Lanthier PA, Burg E, Drew A, Bunn J, Suratt BT, Haynes L, Rincon M (2012) Essential role of IL-6 in protection against H1N1 influenza virus by promoting neutrophil survival in the lung. Mucosal Immunol 5:258–266CrossRefGoogle Scholar
  13. El Gamal AA (2010) Biological importance of marine algae. Saudi Pharm J 18:1–25CrossRefGoogle Scholar
  14. Ellis AE (2001) Innate host defense mechanisms of fish against viruses and bacteria. Dev Comp Immunol 25:827–839CrossRefGoogle Scholar
  15. Fletcher TC, White A (1976) The lysozyme of the plaice Pleuronectes platessa L. Comp Biochem Physiol B 55:207–210CrossRefGoogle Scholar
  16. Fujiwara A, Nishida-Umehara C, Sakamoto T, Okamoto N, Nakayama I, Abe S (2001) Improved fish lymphocyte culture for chromosome preparation. Genetica 111:77–89CrossRefGoogle Scholar
  17. Garcia-Vaquero M, Hayes M (2016) Red and green macroalgae for fish and animal feed and human functional food development. Food Rev Int 32:15–45CrossRefGoogle Scholar
  18. Goldstein I, Lerer E, Laiba E, Mallet J, Mujaheed M, Laurent C, Rosen H, Ebstein RP, Lichtstein D (2009) Association between sodium- and potassium-activated adenosine triphosphatase α isoforms and bipolar disorders. Biol Psychiatry 65:985–991CrossRefGoogle Scholar
  19. Grimm H, Mayer K, Mayser P, Eigenbrodt E (2002) Regulatory potential of n-3 fatty acids in immunological and inflammatory processes. Br J Nutr 87:S59–S67CrossRefGoogle Scholar
  20. Haller O, Staeheli P, Kochs G (2007) Interferon-induced Mx proteins in antiviral host defense. Biochimie 89:812–818CrossRefGoogle Scholar
  21. Halperin ML, Kamel KS (1998) Potassium. Lancet 352:135–140CrossRefGoogle Scholar
  22. Johnson ML, Navanukraw C, Grazul-Bilska AT, Reynolds LP, Redmer DA (2003) Heparinase treatment of RNA before quantitative real-time RT-PCR. Biotechniques 35:1140–1143CrossRefGoogle Scholar
  23. Kiron V (2012) Fish immune system and its nutritional modulation for preventive health care. Anim Feed Sci Technol 173:111–133CrossRefGoogle Scholar
  24. Lester K, Hall M, Urquhart K, Gahlawat S, Collet B (2012) Development of an in vitro system to measure the sensitivity to the antiviral Mx protein of fish viruses. J Virol Methods 182:1–8CrossRefGoogle Scholar
  25. Lingrel JB, Kuntzweiler T (1994) Na+,K(+)-ATPase. J Biol Chem 269:19659–19662Google Scholar
  26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408CrossRefGoogle Scholar
  27. Lortat-Jacob H, Baltzer F, Grimaud J-A (1996) Heparin decreases the blood clearance of interferon-γ and increases its activity by limiting the processing of its carboxyl-terminal sequence. J Biol Chem 271:16139–16143CrossRefGoogle Scholar
  28. Lozano I, Wacyk JM, Carrasco J, Cortez-San Martín MA (2016) Red macroalgae Pyropia columbina and Gracilaria chilensis: sustainable feed additive in the Salmo salar diet and the evaluation of potential antiviral activity against infectious salmon anemia virus. J Appl Phycol 28:1343–1351CrossRefGoogle Scholar
  29. MacKenzie S, Bardolet LT, Balasch JC (2004) Fish health challenge after stress. Indicators of immunocompetence. Contrib Sci 2:443–454Google Scholar
  30. Magnadóttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151CrossRefGoogle Scholar
  31. Marsham S, Scott GW, Tobin ML (2007) Comparison of nutritive chemistry of a range of temperate seaweeds. Food Chem 100:1331–1336CrossRefGoogle Scholar
  32. McBeath AJA, Snow M, Secombes CJ et al (2007) Expression kinetics of interferon and interferon-induced genes in Atlantic salmon (Salmo salar) following infection with infectious pancreatic necrosis virus and infectious salmon anaemia virus. Fish Shellfish Immunol 22:230–241CrossRefGoogle Scholar
  33. Mohamed S, Hashim SN, Rahman HA (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Technol 23:83–96CrossRefGoogle Scholar
  34. Montero D, Grasso V, Izquierdo MS, Ganga R, Real F, Tort L, Caballero MJ, Acosta F (2008) Total substitution of fish oil by vegetable oils in gilthead sea bream (Sparus aurata) diets: effects on hepatic Mx expression and some immune parameters. Fish Shellfish Immunol 24:147–155CrossRefGoogle Scholar
  35. Morales B, Macgayver M, Rondón-Barragán IS (2011) Comparative biology of the complement system in fish. CES Med Vet Zootec 6:74–90Google Scholar
  36. Moreda‐Piñeiro A, Peña‐Vázquez E, Bermejo‐Barrera P (2012) Significance of the presence of trace and ultratrace elements in seaweeds. In: Kim, S. (ed.) Handbook of marine macroalgae: biotechnology and applied phycology. Wiley-Blackwell, ChichesterGoogle Scholar
  37. Ngo D-H, Wijesekara I, Vo T-S, Ta QV, Kim S-K (2011) Marine food-derived functional ingredients as potential antioxidants in the food industry: an overview. Food Res Int 44:523–529CrossRefGoogle Scholar
  38. Nygaard R, Husgard S, Sommer A-I, Leong JA, Robertsen B (2000) Induction of Mx protein by interferon and double-stranded RNA in salmonid cells. Fish Shellfish Immunol 10:435–450CrossRefGoogle Scholar
  39. Paulsen SM, Lunde H, Engstad RE, Robertsen B (2003) In vivo effects of β-glucan and LPS on regulation of lysozyme activity and mRNA expression in Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 14:39–54CrossRefGoogle Scholar
  40. Pereira L (2016) Edible seaweeds of the world. CRC Press, Boca RatonCrossRefGoogle Scholar
  41. Purcell MK, Laing KJ, Winton JR (2012) Immunity to fish rhabdoviruses. Viruses 4:140–166CrossRefGoogle Scholar
  42. Reilly P, O’Doherty JV, Pierce KM, Callan JJ, O'Sullivan JT, Sweeney T (2008) The effects of seaweed extract inclusion on gut morphology, selected intestinal microbiota, nutrient digestibility, volatile fatty acid concentrations and the immune status of the weaned pig. Animal 2:1465–1473CrossRefGoogle Scholar
  43. Reverter M, Saulnier D, David R, Bardon-Albaret A, Belliard C, Tapissier-Bontemps N, Lecchini D, Sasal P (2016) Effects of local Polynesian plants and algae on growth and expression of two immune-related genes in orbicular batfish (Platax orbicularis). Fish Shellfish Immunol 58:82–88CrossRefGoogle Scholar
  44. Rhimou B, Hassane R, Nathalie B (2015) Antiviral activity of the extracts of Rhodophyceae from Morocco. Afr J Biotechnol 9:7968–7975Google Scholar
  45. Sánchez-Machado DI, López-Cervantes J, López-Hernández J, Paseiro-Losada P (2004) Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chem 85:439–444CrossRefGoogle Scholar
  46. Saurabh S, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquac Res 39:223–239CrossRefGoogle Scholar
  47. Scocchi M, Pallavicini A, Salgaro R, Bociek K, Gennaro R (2009) The salmonid cathelicidins: a gene family with highly varied C-terminal antimicrobial domains. Comp Biochem Physiol B 152:376–381CrossRefGoogle Scholar
  48. Shirozu T, Sasaki K, Kawahara M, Yanagawa Y, Nagano M, Yamauchi N, Takahashi M (2016) Expression dynamics of bovine Mx genes in the endometrium and placenta during early to mid pregnancy. J Reprod Dev 62:29–35CrossRefGoogle Scholar
  49. Skou JC, Esmann M (1992) The Na, K-ATPase. J Bioenerg Biomembr 24:249–261Google Scholar
  50. Statovci D, Aguilera M, MacSharry J, Melgar S (2017) The impact of western diet and nutrients on the microbiota and immune response at mucosal interfaces. Front Immunol 8:838Google Scholar
  51. Toledo I, Avila M, Manríquez A et al (2009) Algas, insumo alternativo para la alimentación, de especies acuícolas. Pontificia Universidad Católica de Valparaíso. Escuela de Ciencias del Mar, ValparaisoGoogle Scholar
  52. Wei S, Huang Y, Cai J, Huang X, Qin Q (2012) Molecular cloning and characterization of c-type lysozyme gene in orange-spotted grouper, Epinephelus coioides. Fish Shellfish Immunol 33:186–196CrossRefGoogle Scholar
  53. Whitmire JK, Tan JT, Whitton JL (2005) Interferon-γ acts directly on CD8+ T cells to increase their abundance during virus infection. J Exp Med 201:1053–1059CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Ivonne Lozano Muñoz
    • 1
    Email author
  • Jurij Wacyk
    • 1
  • Claudio Perez
    • 1
  • Jaime Carrasco
    • 2
  • Marcelo Cortez-San Martin
    • 3
  1. 1.Facultad de Ciencias Agronómicas, Producción Animal, Laboratorio de Genética y Biotecnología en AcuiculturaUniversidad de ChileSantiagoChile
  2. 2.Salmon DivisionBiomar Chile S.A., R&DPuerto MonttChile
  3. 3.Facultad de Química y Biología, Laboratorio de Virología Molecular y Control de PatógenosUniversidad de Santiago de ChileSantiagoChile

Personalised recommendations