A whole-grain diet increases whole-body protein balance compared to a macronutrient-matched refined-grain diet

Authors: MEY, JACOB - Pennington Biomedical Research Center; GODIN, JEAN-PHILIPPE - Nestle Research & Development; SCELSI, AMANDA - Cleveland Clinic; KULLMAN, EMILY - Cleveland State University; MALIN, STEVEN - Rutgers University; YANG, SHENGPING - Pennington Biomedical Research Center; FLOYD, Z - Pennington Biomedical Research Center; POULEV, ALEXANDER - Rutgers University; FIELDING, ROGER - Jean Mayer Human Nutrition Research Center On Aging At Tufts University; ROSS, ALASTAIR - Agresearch; KIRWAN, JOHN - Pennington Biomedical Research Center

Submitted to: Current Developments in Nutrition
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/16/2021
Publication Date: 9/25/2021
Citation: Mey, J.T., Godin, J., Scelsi, A.R., Kullman, E.L., Malin, S.K., Yang, S., Floyd, Z.E., Poulev, A., Fielding, R.A., Ross, A.B., Kirwan, J.P. 2021. A whole-grain diet increases whole-body protein balance compared to a macronutrient-matched refined-grain diet. Current Developments in Nutrition. 5:nzab121. https://doi.org/10.1093/cdn/nzab121.
DOI: https://doi.org/10.1093/cdn/nzab121

Interpretive Summary: There are limited data from randomized controlled studies to support the contention that diets rich in whole-grains can enhance protein metabolism in humans. This study examined: the clinical effects of a whole-grain diet on whole-body protein turnover; the cellular effects of whole-grains on protein synthesis in skeletal muscle cells; and the effects of whole-grain intake on age-related muscle function in a large epidemiological cohort. We studied adults with overweight/obesity who consumed both a whole-grain enriched diet and a refined-grain enriched diet for two separate 8-wk periods. We found that protein balance was 3-fold higher on the whole-grain diet compared with the refined-grain diet. In cell culture experiments we found that whole-grain wheat extract increased protein synthesis in muscle cells. In a large population sample of older adults, whole-grain intake was associated with greater muscle function measured by walking speed. This study demonstrated that consuming whole-grains promotes greater protein turnover and enhances net protein balance in adults. These data point to a new mechanism whereby whole-grain consumption favorably enhances protein turnover and may improve functional outcomes.

Technical Abstract: Background: There are limited data from randomized control trials to support or refute the contention that whole-grains can enhance protein metabolism in humans. Objectives: To examine: 1) the clinical effects of a whole-grain diet on whole-body protein turnover; 2) the cellular effects of whole-grains on protein synthesis in skeletal muscle cells; and 3) the population effects of whole-grain intake on age-related muscle loss. Methods: Adults with overweight/obesity (n = 14; age = 40 +/- 7 y; BMI = 33 +/- 5 kg/m2) were recruited into a crossover, randomized controlled trial (NCT01411540) in which isocaloric, macronutrient-matched whole-grain and refined-grain diets were fully provisioned for two 8-wk periods. Diets differed only in the presence of whole-grains (50 g/1000 kcal). Whole-body protein kinetics were assessed at baseline and after each diet in the fasted-state (13C-leucine) and integrated over 24 h (15N-glycine). In vitro studies using C2C12 cells assessed global protein synthesis by surface sensing of translation and anabolic signaling by Western blot. Complementary epidemiological assessments using the NHANES database assessed the effect of whole-grain intake on muscle function assessed by gait speed in older adults (n = 2783). Results: Integrated 24-h net protein balance was 3-fold higher on a whole-grain diet compared with a refined-grain diet (P = 0.04). A whole-grain wheat extract increased submaximal rates of global protein synthesis (27%, P < 0.05) in vitro. In a large sample of older adults, whole-grain intake was associated with greater muscle function (OR = 0.92; 95% CI: 0.86, 0.98). Conclusions: Consuming 50 g/1000 kcal whole-grains per day promotes greater protein turnover and enhances net protein balance in adults. Whole-grains impact skeletal muscle at the cellular level, and are associated with greater muscle function in older adults. Collectively, these data point to a new mechanism whereby whole-grain consumption favorably enhances protein turnover and improves health outcomes.