Paternal and/or Maternal Blackberry (Rubus spp.) Polyphenolic Extract Consumption Improved Paternal Fertility and Differentially Affected Female Offspring Antioxidant Capacity and Metabolic Programming in a Mouse Model

Abstract

Dietary polyphenols' role in early life is not clear. While accumulating studies show both beneficial and deleterious effects of maternal consumption of these bioactive compounds on offspring's adult health, very few studies have focused on the impact of paternal consumption. In addition, the potential interaction of combined parental polyphenol consumption is still not known. Thus, the aim of the present study was to investigate the effects of maternal (gestation/lactation) and/or paternal (preconception) blackberry polyphenol (anthocyanins, ellagitannins, and quercetin) methanolic extract consumption on C57BL/6 female mice offspring. Blackberry polyphenol consumption by fathers improved their sperm production and increased fertility. Blackberry polyphenol consumption by fathers, but not mothers, increased their plasma antioxidant capacity. All parental interventions decreased offspring perinatal mortality, with combined fathers' and mothers' polyphenol consumption exerting the most pronounced effects. Paternal or maternal polyphenol consumption decreased plasma total antioxidant capacity in the female offspring. On the other hand, combined parental consumption had opposing effects on the offspring. Only maternal polyphenol interventions increased glucose tolerance in the female offspring. These data only partially confirm our hypothesis that combined paternal and maternal polyphenol intervention would lead to better outcomes in the offspring. These results further show that blackberry polyphenols' effects on offspring health depend on whether their consumption occurred through the father, mother, or both. This suggests that in order to promote long-term health in descendants, nutritional interventions, including those with polyphenols, should target not only the mother but also the future father.

Keywords: DOHaD; POHaD; blackberry; mice; polyphenols; reproduction.

Figure 1

Experimental design of study.

Figure 2

Reproductive parameters of male mice (fathers) from COF and BF groups. (A): Sperm morphology (n = 10/group); (B): daily sperm production (n = 11/group); (C): serum levels of testosterone (n= 4/group); (D): tubular diameter of seminiferous tubule (n = 6/group); (E): tubular area of seminiferous tubule (n = 6/group); and (F): interstitial area of seminiferous tubule (n = 6/group). * Statistically significant difference (p ≤ 0.05) when compared to COF group, according to Student’s t-test. COFs: control fathers, BFs: blackberry fathers.

Figure 3

Plasma antioxidant capacity and liver antioxidant enzyme activity of 7-week-old animals from DCOFM, DBF, DBM, and DBFM groups. (A): Plasma antioxidant capacity of female offspring (n = 5); (B): liver SOD activity of female offspring (n = 6/group); (C): liver CAT activity of female offspring (n = 6/group); and (D): liver GPx activity of female offspring. Different letters between groups indicate statistically significant differences (p ≤ 0.05), according to analysis of variance with two fixed factors and multiple comparisons method of Tukey. DCOFMs: daughters control fathers and mothers; DBFs: daughters blackberry fathers; DBMs: daughters blackberry mothers; DBFMs: daughters blackberry fathers and mothers.