Paternal Resistance Training Modulates Calcaneal Tendon Proteome in the Offspring Exposed to High-Fat Diet

Abstract

The increase in high-energy dietary intakes is a well-known risk factor for many diseases, and can also negatively impact the tendon. Ancestral lifestyle can mitigate the metabolic harmful effects of offspring exposed to high-fat diet (HF). However, the influence of paternal exercise on molecular pathways associated to offspring tendon remodeling remains to be determined. We investigated the effects of 8 weeks of paternal resistance training (RT) on offspring tendon proteome exposed to standard diet or HF diet. Wistar rats were randomly divided into two groups: sedentary fathers and trained fathers (8 weeks, three times per week, with 8-12 dynamic movements per climb in a stair climbing apparatus). The offspring were obtained by mating with sedentary females. Upon weaning, male offspring were divided into four groups (five animals per group): offspring from sedentary fathers were exposed either to control diet (SFO-C), or to high-fat diet (SFO-HF); offspring from trained fathers were exposed to control diet (TFO-C) or to a high-fat diet (TFO-HF). The Nano-LC-MS/MS analysis revealed 383 regulated proteins among offspring groups. HF diet induced a decrease of abundance in tendon proteins related to extracellular matrix organization, transport, immune response and translation. On the other hand, the changes in the offspring tendon proteome in response to paternal RT were more pronounced when the offspring were exposed to HF diet, resulting in positive regulation of proteins essential for the maintenance of tendon integrity. Most of the modulated proteins are associated to biological pathways related to tendon protection and damage recovery, such as extracellular matrix organization and

Impact of paternal exercise on physiological systems in the offspring

“…More recently, two studies on paternal resistance exercise showed overlapping proteins in the left ventricle and tendon, which change in the same direction (up-regulation), and were present in trained fathers and offspring. 20,24 Other studies revealed that paternal exercise induced modifications in global DNA methylation status, 50 ncRNAs profile, 22,25,51 and protein expression in the hippocampus, 52 skeletal muscle, 21 tendon, 24 heart 20 and liver 53 in the F1 generation (Figure 2).…”

“…Exercise sessions consisted of 8 ladder climbs with two sets of each load of 50, 75, 90 and 100% of their maximal carrying capacity interspersed by 120 s intervals between each set. 20,24 An additional 30-g load was added to maximal carrying capacity every week according to the overload principle. This protocol induced protective effects on the left ventricle and tendon proteome of offspring exposed to a high-fat diet due to the increase in proteins involved in pathways essential for tissue integrity maintenance.…”

“…The collected articles were categorized into six systems: Nervous system (six articles), 23,50,52,65,73,74 Endocrine and urinary system (four articles) 22,31,51,53 Musculoskeletal system (six articles), 21,24,25,51,64,75 Cardiovascular system and blood circulation (four articles), 20,22,25,51 and Fat tissue and body composition (six articles). 20-22,24,25,51 1.5.1 | Nervous system It is well established that the inheritance of exercise-induced cognition enhancement through the male lineage is a direct factor driving the hippocampus physiology and cognitive behaviour of the offspring.…”

“…The collected articles were categorized into six systems: Nervous system (six articles), 23,50,52,65,73,74 Endocrine and urinary system (four articles) 22,31,51,53 Musculoskeletal system (six articles), 21,24,25,51,64,75 Cardiovascular system and blood circulation (four articles), 20,22,25,51 and Fat tissue and body composition (six articles) 20‐22,24,25,51 …”

“…[19][20][21][22][23] We demonstrated that resistance paternal exercise (RT) modulates left ventricle and tendon proteome of offspring exposed to a high-fat diet, which could be essential for maintenance of tissue integrity. 20,24 Some reports showed that voluntary wheel running in the fathers suppresses the detrimental effects of a paternal high fat (HF) diet on offspring, reducing the negative effects on fat mass and glucose uptake in different skeletal muscles, which could be an important intervention to prevent type 2 diabetes. 21,25 Current advances have introduced new opportunities to map the complex epigenetic mechanisms regarding paternal exercise.…”