Elsevier

Nutrition

Volume 24, Issues 7–8, July–August 2008, Pages 717-726
Nutrition

Basic nutritional investigation
Dietary lipids modify redox homeostasis and steroidogenic status in rat testis

https://doi.org/10.1016/j.nut.2008.03.008Get rights and content

Abstract

Objective

The present study explored the effect of dietary oils on lipid composition, antioxidant status, and the activity of the main steroidogenic enzymes in the testis.

Methods

Forty Wistar rats were randomly assigned to one of four groups (n = 10) fed for 60 d on the same basal diet plus different lipid sources as commercial oils: soybean, olive, coconut, or grapeseed. After sacrifice, testicular lipids and fatty acid composition, free radical biomarkers, antioxidant levels, hormones, and steroidogenic enzymes were determined.

Results

The lipid composition of diets produced significant changes in neutral/phospholipids, free/esterified cholesterol, and plasmalogen proportion. Fatty acid patterns of these lipids were also strongly modified, influencing the double bond index. We also found a close correlation between the type of diet and the generation of free radicals. The oxidative stress in testes was higher with the grapeseed oil–supplemented diet and decreased with the other diets in this order: soybean oil > olive oil > coconut oil. Animals fed with the olive oil and coconut oil diets showed the highest testicular levels of antioxidants in addition to significantly high levels of testosterone and 3β- or 17β-hydroxysteroid dehydrogenase enzymes.

Conclusion

Different oils in the diets strongly modified the homeostasis of the testicular antioxidant defense system and, in consequence, affected steroidogenic function, showing a clear correlation with the damage induced. According to our results, an appropriate mixture of olive and soybean oils could be a healthy recommendation.

Introduction

During previous decades great interest was focused on the relation between lipid metabolism and the atherogenic condition as a cause of different vascular-related diseases [1]. However, much less attention was given to the role played by lipid metabolism in other human pathologies, especially those involved in reproductive function. Disorders associated with male infertility have exhibited an increased incidence during the past few years, due to many concomitant factors not fully understood or even recognized [2].

It is well known that testicular lipids strongly influence the histology and physiology of this tissue [3], [4], [5]. Essential fatty acid deficiency [6], [7] or alterations in fatty acid metabolism in diabetic patients [7] have been associated with testicular malfunction. Moreover, it was previously demonstrated that polyunsaturated fatty acid (PUFA) supplementation to diets produced significant changes in testicular lipid composition, modifying the metabolism of C20–22 fatty acids with a strong impact on the physiology of germinal and steroidogenic cells [3], [5]. In addition, lipids have been closely associated with intracellular generation of reactive oxygen species [8] as substrates for oxidative attack and a source for free radical generation and/or chain propagator reactions. This “two-face” characteristic of lipids depends on multiple factors; one of them is the quantity and quality of the fatty acyl chains acylated to complex cellular lipids [8], [9], [10]. Several reports demonstrated that under oxidative stress conditions testes are especially susceptible to develop damage derived from the redox imbalance [11], [12], [13], [14], [15], [16], [17]. This fact is considered one of the most important features in the etiology of human reproductive illnesses of high incidence such as varicocele [2], [18].

However, strong differences in the lipid composition of diets across the world have been poorly studied from the point of view of their influence on the relation between free radical generation and testicular steroidogenesis. Thus, the lipid composition of testes (modifiable by the diet), the regulation of reactive oxygen species (and other reactive species), and the testicular integrity and function are closely related factors.

In this study we investigated the effect of diet-induced modification of testicular lipids on the generation of reactive oxygen species and the activity of the main steroidogenic enzymes (3β- and 17β-hydroxysteroid dehydrogenases [3β-HSD and 17β-HSD]). Results obtained may contribute to the understanding of the role played by dietary lipid sources on testicular function and its relation to redox homeostasis.

Section snippets

Chemicals

Solvents (high-performance liquid chromatographic grade) were provided by Carlo Erba (Milano, Italy). Other chemicals were from Sigma Chemical Co. and Fluka Chemie AG (Buenos Aires, Argentina).

Lipids used as standards were from Serdary Research Laboratory (London, ON, Canada) or Nu-Check-Prep (Elysian, MN, USA). Commercial oils added to diets were from Molinos Río de La Plata SAIC and Platafarm SA (La Plata, Argentina).

Diets and animal treatment

Female Wistar rats weighing 180 ± 10 g were bred and maintained on a control

Influence of diet on growth parameters

Feeding parameters associated to diets are listed in Table 3. Animals fed the different diets showed almost identical water consumption (approximately 15 mL/d) and food intake (approximately 15 g/d). Initial body weight was similar in all groups. However, final body weight, rate of body weight gain, and food efficiency ratio were significantly elevated in the C group compared with the others. Absolute and relative testicular weights were significantly increased in the O group compared with the

Discussion

In this study we examined the relation among testicular antioxidant status, steroidogenic function, and lipid composition of the diet. The oils selected are widely used all over the world. The S and G oils were characterized by a high content of linoleic acid. However, in both diets the ω-6/ω-3 fatty acid ratio was markedly different. Soybean and fish oils showed similar high levels of ω-3 acids, but the former is more advantageous due to the lack of cholesterol. Therefore the S and G groups

Conclusion

The present results indicate that there is a close relation among the source of dietary oil, the antioxidant defense system status, and the steroidogenic function of the testis. According to our results the consumption of an appropriate mixture of olive and soybean oils could be a healthy eating recommendation.

Acknowledgments

The authors are grateful to Eva Illara de Bozzolo for excellent technical assistance and Norma Tedesco for language revision.

References (63)

  • H. Chen et al.

    Vitamin E, aging and Leydig cell steroidogenesis

    Exp Gerontol

    (2005)
  • P.G. Reeves et al.

    AIN-93 Purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet

    J Nutr

    (1993)
  • C.A. Marra et al.

    Modulation of Δ6 and Δ5 rat liver microsomal desaturase activities by dexamethasone-induced factor

    Biochim Biophys Acta

    (1986)
  • P. Murugesan et al.

    The inhibitory effects of polychlorinated biphenyl Aroclor 1254 on Leydig cell LH receptors, steroidogenic enzymes and antioxidant enzymes in adult rats

    Reprod Toxicol

    (2005)
  • J. Folch et al.

    A simple method for the isolation and purification of total lipides from animal tissues

    J Biol Chem

    (1957)
  • D.J. Hanahan et al.

    A columm chromatographic separation of classes of phospholipides

    J Biol Chem

    (1957)
  • K. Nakamura et al.

    Coomassie brilliant blue staining of lipids on thin-layer plates

    Anal Biochem

    (1984)
  • C.A. Marra et al.

    Neutral and polar lipid metabolism in liver microsomes of growing rats fed a calcium deficient diet

    Biochem Biophys Acta

    (2005)
  • W.J. Gelsema et al.

    Quantitation of the diacyl, alkylacyl, and alk-1-enylacyl subclasses of choline glycerophospholipids by chemical dephosphorylation and benzoylation

    Anal Biochem

    (1994)
  • W.R. Morrison et al.

    Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol

    J Lipid Res

    (1964)
  • K. Yagi

    A simple fluorometric assay for lipoperoxide in blood plasma

    Biochem Med

    (1976)
  • R.O. Recknagel et al.

    Spectrophotometric detection of lipid conjugated dienes

    Methods Enzymol

    (1984)
  • I.F. Benzie et al.

    The ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: the FRAP assay

    Anal Biochem

    (1996)
  • R. Brigelius et al.

    Identification and quantitation of glutathione in hepatic protein mixed disulfides and its relationship to glutathione disulfide

    Biochem Pharmacol

    (1983)
  • M. Asensi et al.

    A high-performance liquid chromatography method for measurement of oxidized glutathion in biological samples

    Anal Biochem

    (1994)
  • M. Bagnati et al.

    Cu(I) Availability paradoxically antagonizes antioxidant consumption and lipid peroxidation during the initiation phase of copper-induced LDL oxidation

    Biochem Biophys Res Commun

    (1998)
  • K. Burton

    Determination of DNA concentration with diphenylamine

    Methods Enzymol

    (1968)
  • A.Z. Reznick et al.

    Oxidative damage to proteins: spectrophotometric method for carbonyl assay

    Methods Enzymol

    (1994)
  • A.F. Boyne et al.

    A methodology for analysis of tissue sulfhydryl components

    Anal Biochem

    (1972)
  • I.F. Benzie

    An automated, specific spectrophotometric method for measuring ascorbic acid in plasma (EFTSA)

    Clin Biochem

    (1996)
  • M.M. Bradford

    A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding

    Anal Biochem

    (1976)
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    This study was supported in part by grants from CIC and CONICET, Argentina.

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