Elsevier

Fish & Shellfish Immunology

Volume 100, May 2020, Pages 418-426
Fish & Shellfish Immunology

Full length article
Assessment of chemical, biological and immunological properties of “Damiana de California” Turnera diffusa Willd extracts in Longfin yellowtail (Seriola rivoliana) leukocytes

https://doi.org/10.1016/j.fsi.2020.03.045Get rights and content

Highlights

  • Damiana de California Turnera diffusa Willd compounds in infusion and methanolic extracts were analyzed.

  • Infusion extract present a considerable amount of phenolic and flavonoid compounds.

  • Both T. diffusa extracts had considerable antioxidant capacity.

  • Infusion extract increased immune and antioxidant parameters in splenocytes of Seriola lalandi.

  • Both T. diffusa extracts upregulated the pro-inflammatory cytokine IL-1β in V. parahaemolyticus-infected leukocytes.

Abstract

In Mexican herbal medicines or natural remedies, Turnera diffusa (Turneraceae) known as “Damiana de California”, has ethnopharmacological relevance, including aphrodisiac, diuretic, and antimicrobial activities. To explore the immunological effect of infusion and methanolic extracts from Damiana de California, this study investigated its chemical, biological, antimicrobial and immunological properties in Longfin yellowtail Seriola rivoliana leukocytes. The analysis of chemical compounds revealed a considerable level of total phenolic and flavonoid contents in the infusion compared with methanolic extract. Furthermore, the antioxidant activity showed high hydroxyl radical scavenging activity in infusion extract compared with BHT positive control. Superoxide radical scavenging activity and ion chelation were higher in methanolic extract followed by infusion treatment. Interestingly, notable antimicrobial activity was observed in both extracts of T. diffusa against Vibrio parahaemolyticus. An in vitro study was performed using leukocytes of S. rivoliana treated with infusion or methanolic extracts at 12.5, 25 and 50 μg/mL for 24 h. Remarkably, infusion extract induced proliferation at any concentration but not the methanolic extract, which was diminished in a dose-dependent fashion. The immunostimulation study demonstrated that the phagocytosis activity increased in those leukocytes stimulated with methanolic extract but diminished the respiratory burst activity, in contrast to the activity observed in those leukocytes stimulated with infusion treatment. Finally, leukocytes incubated with the extracts and confronted with V. parahaemolyticus up-regulated the transcription of proinflammatory cytokine IL-1β gene in a dose response relationship. These findings suggest that the infusion treatment has potential therapeutic properties, promoting the antioxidant capacity and enhancing immune parameters in Longfin yellowtail S. rivoliana.

Introduction

In recent years, the interest in herbal or plant extracts have increased as alternative therapies that could effectively protect fish of diseases by stimulating their immune system. Moreover, natural medicinal products relatively non-toxic, environmentally friendly, and cost-effective, are often locally available, and can act against a broad spectrum of pathogens [1]. Herbs or plants are potential sources of phytochemicals (alkaloids, flavonoids, phenols, tannins) that are major bioactive compounds and natural antioxidants [2]. Phytochemicals act as reducing agents, metal ion chelators and scavengers of free radicals with great therapeutic potential such as antioxidant and immunomodulatory activities [3,4].

Turnera diffusa Willd or ‘‘Damiana de California’’ belongs to the Turneraceae family and it is a medicinal plant native of Baja California desert in Mexico [5,6]. Mexican indigenous populations used damiana leaves for the treatment of different illness, including sexual disfunction [7,8]. This small shrub is widely recognized for its medicinal properties among them, estrogenic, antibacterial and prosexual activities [6,9]. Zhao et al. [10] and Alcaraz-Meléndez et al. [11] showed a huge quantity of essential oils and flavonoids in T. diffusa, which could be responsible for its therapeutic properties. Antioxidant and phytochemical properties of T. diffusa have been reported for water-ethanol [9], methanolic [10,12] and essential oil extractions [11,13], but not for infusion preparations, which is the most consumed form. Tea-type infusion or water extracts is the method of obtaining bioactive compounds from plants, by keeping them immersed in cold or hot water [14]. Studies using aqueous extracts like infusion preparation are scarce, which have been traditionally used because of digestive and antispasmodic effects [15]. Actually, therapeutic applications of Damiana de California have gained an increasing interest for medical applications; however, no studies have been conducted to assess antioxidant composition and immunostimulant effects of methanolic and infusion extracts (the most consumed forms) of damiana in fish. Therefore, phytochemical compounds and antiradical capacity of infusion and methanolic extracts were studied. In addition, for the first time, the proliferation and immunostimulant effects of both (infusion and methanolic) extracts were evaluated in Longfin yellowtail Seriola rivoliana leukocytes.

Section snippets

Preparation of infusion and methanolic extracts

Dry plants of “Damiana de California” T. diffusa Willd were collected in La Paz, Baja California Sur, Mexico. Damiana leaves were homogenized and milled to a fine powder (0.5- mm mesh).

For the infusion, 1 g of powder was dispensed to 100 mL of miliQ water, heated for 10 min, and let cool at 25 °C and sieved through Whatman No. 1 filter paper. Finally, infusion was lyophilized for 24 h.

For methanolic extract preparation [16], 1 g leaf powder in 10 mL of 100% methanol was incubated under

FT-IR analysis

In order to compare the lyophilized extracts, Fig. 1 depicts FT-IR curves that were normalized to unity based on the most intense band (as a reference band), which appears at 1036 cm−1 for both spectra. In both extracts (infusion extract, curve a; methanolic extract, curve b), similar characteristic signals are revealed: on the region at 3200 cm−1 the –OH vibrations attributed to phenols appear, a shoulder around of 2900 cm−1 is a characteristic signal observed due to the flexion of methylene

Discussion

Herbal or medicinal plants have shown to possess an abundant quantity of metabolites, such as polyphenols, flavonoids, amino acids and carbohydrates [30]. Principal phytochemical and antioxidant characterization of infusion and methanolic leaf extracts of “Damiana de California” T. diffusa Willd have been reported in this study. The antioxidant activity of phenolic compounds is attributed to their different molecular structures, concisely by the number and possible orientations of the hydroxyl

Conclusion

For the first time, this study provides the effect of Damiana de California T. diffusa infusion and methanolic extracts on chemical, biological, and immunostimulant properties using leukocytes of Longfin yellowtail S. rivoliana. The chemical ATR-FTIR analysis revealed the presence of different bioactive compounds, which could be related with the T. diffusa antioxidant capacity. Clearly, infusion extract is the treatment that had more phytochemical compounds and DPPH activity. Infusion and

CRediT authorship contribution statement

Martha Reyes-Becerril: Conceptualization, Writing - original draft. Perla Ginera: Investigation. Jorge Silva-Jara: Investigation. Adriana Macias: Investigation. Carlos Velazquez-Carriles: Investigation. Lilia Alcaraz-Meléndez: Methodology. Carlos Angulo: Writing - review & editing.

Declaration of competing interest

The authors declare no competing financial interest.

Acknowledgments

Authors thanks Kampachi Farms Mexico at CIBNOR-BioHelis Innovation and Technology Park in La Paz Baja California Sur, Mexico. Thanks to Francisco Encarnación, Kevyn Guerra and Rene Rebollar for their technical assistance and Diana Fischer for English editorial services. CONACYT funded this research by INFR-2014-01/225924 grants.

References (59)

  • X.Q. Zha et al.

    The core structure of a Dendrobium huoshanense polysaccharide required for the inhibition of human lens epithelial cell apoptosis

    Carbohydr. Polym.

    (2017)
  • M.C. Wang et al.

    Characterization, antioxidant activity and immunomodulatory activity of polysaccharides from the swollen culms of Zizania latifolia

    Int. J. Biol. Macromol.

    (2017)
  • M.J. Quade et al.

    A rapid, direct assay to measure degranulation of bovine neutrophil primary granules

    Vet. Immunol. Immunopathol.

    (1997)
  • C. Angulo et al.

    C-type lectin 17A and macrophage-expressed receptor genes are magnified by fungal β-glucan after Vibrio parahaemolyticus infection in Totoaba macdonaldi cells

    Immunobiology

    (2019)
  • K.J. Livak et al.

    Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method

    Methods

    (2001)
  • H.E. Tahir et al.

    Rapid prediction of phenolic compounds and antioxidant activity of Sudanese honey using Raman and Fourier transform infrared (FT-IR) spectroscopy

    Food Chem.

    (2017)
  • K. Szewczyk et al.

    Ethnobotany, phytochemistry, and bioactivity of the genus Turnera (Passifloraceae) with a focus on damiana—Turnera diffusa

    J. Ethnopharmacol.

    (2014)
  • N. Donlao et al.

    Impacts of processing conditions on digestive recovery of polyphenolic compounds and stability of the antioxidant activity of green tea infusion during in vitro gastrointestinal digestion

    LWT - Food Sci. Technol. (Lebensmittel-Wissenschaft -Technol.)

    (2018)
  • N. Martins et al.

    Decoction, infusion and hydroalcoholic extract of Origanum vulgare L.: different performances regarding bioactivity and phenolic compounds

    Food Chem.

    (2014)
  • C. Torres-Fuentes et al.

    Iron-chelating activity of chickpea protein hydrolysate peptides

    Food Chem.

    (2012)
  • M. Reyes-Becerril et al.

    Leukocyte susceptibility and immune response against Vibrio parahaemolyticus in Totoaba macdonaldi

    Dev. Comp. Immunol.

    (2016)
  • Z. Sun et al.

    Effects of dietary Panax notoginseng extract on growth performance, fish composition, immune responses, intestinal histology and immune related genes expression of hybrid grouper Epinephelus lanceolatus ♂ × Epinephelus fuscoguttatus ♀) fed high lipid diets

    Fish Shellfish Immunol.

    (2018)
  • T. Hernández et al.

    Ethnobotany and antibacterial activity of some plants used in traditional medicine of Zapotitlán de las Salinas, Puebla (México)

    J. Ethnopharmacol.

    (2003)
  • K. Ben Othmen et al.

    An in vitro study of the effect of carob (Ceratonia siliqua L.) leaf extracts on gilthead seabream (Sparus aurata L.) leucocyte activities. Antioxidant, cytotoxic and bactericidal properties

    Fish Shellfish Immunol.

    (2020)
  • H.S. Abdillahi et al.

    Mutagenicity, antimutagenicity and cytotoxicity evaluation of South African Podocarpus species

    J. Ethnopharmacol.

    (2012)
  • A. Fazio et al.

    In vitro effects of Italian Lavandula multifida L. leaf extracts on gilthead seabream (Sparus aurata) leucocytes and SAF-1 cells

    Fish Shellfish Immunol.

    (2017)
  • D. Pietretti et al.

    Oxidative burst and nitric oxide responses in carp macrophages induced by zymosan, MacroGard and selective dectin-1 agonists suggest recognition by multiple pattern recognition receptors

    Fish Shellfish Immunol.

    (2013)
  • Y. Celik Altunoglu et al.

    Immune responses to methanolic extract of black cumin (Nigella sativa) in rainbow trout (Oncorhynchus mykiss)

    Fish Shellfish Immunol.

    (2017)
  • M. Reyes-Becerril 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)
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