Exogenous essential amino acids stimulate an adaptive unfolded protein response in the mammary glands of lactating cows

Journal of Dairy Science

Volumn 100, Issue 7, 2017, Pages 5909-5921

  Nichols, K ^a,c   Doelman, J ^b,d   Kim, J J M ^a   Carson, M ^b   Metcalf, J A ^b   Cant, J P ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b Trouw Nutrition Agresearch Canada   (Canada)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d Trouw Nutrition Research and Development   (Netherlands)

Author keywords

mammalian target of rapamycin complex 1 (mTORC1); mammary; milk synthesis; unfolded protein response

Indexed keywords

AMINO ACID; ESSENTIAL AMINO ACID; MILK PROTEIN; TARGET OF RAPAMYCIN KINASE;

ANIMAL; BOVINE; DRUG EFFECTS; FEMALE; LACTATION; METABOLISM; MILK; SIGNAL TRANSDUCTION; UDDER; UNFOLDED PROTEIN RESPONSE;

AMINO ACIDS; AMINO ACIDS, ESSENTIAL; ANIMALS; CATTLE; FEMALE; LACTATION; MAMMARY GLANDS, ANIMAL; MILK; MILK PROTEINS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UNFOLDED PROTEIN RESPONSE;

EID: 85018975423     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2016-12387     Document Type: Article

References (38)

1. Appuhamy, J.A.D.R.N., Bell, A.L., Nayananjalie, W.A.D., Escobar, J., Hanigan, M.D., Essential amino acids regulate both initiation and elongation of mRNA translation independent of insulin in MAC-T cells and bovine mammary tissue slices. J. Nutr. 141 (2011), 1209–1215 21525255.
2. Bequette, B.J., Kyle, C.E., Crompton, L.A., Anderson, S.E., Hanigan, M.D., Protein metabolism in lactating goats subjected to the insulin clamp. J. Dairy Sci. 85 (2002), 1546–1555 12146487.
3. Burgos, S.A., Dai, M., Cant, J.P., Nutrient availability and lactogenic hormones regulate mammary protein synthesis through the mammalian target of rapamycin signaling pathway. J. Dairy Sci. 93 (2010), 153–161 20059914.
4. Burgos, S.A., Kim, J.J.M., Dai, M., Cant, J.P., Energy depletion of bovine mammary epithelial cells activates AMPK and suppresses protein synthesis through inhibition of mTORC1 signaling. Horm. Metab. Res. 45 (2013), 183–189 22972179.
5. Canadian Council on Animal Care. Guidelines on the Care and Use of Farm Animals in Research, Teaching and Testing, 2009, Canadian Council on Animal Care, Ottawa, ON, Canada.
6. Curtis, R.V., Kim, J.J.M., Bajramaj, D.L., Doelman, J., Osborne, V.R., Cant, J.P., Decline in mammary translational capacity during intravenous glucose infusion into lactating dairy cows. J. Dairy Sci. 97 (2014), 430–438 24268408.
7. Davis, K.R., Giesy, S.L., Long, Q., Krumm, C.S., Harvatine, K.J., Boisclair, Y.R., XBP1 regulates the biosynthetic capacity of the mammary gland during lactation by controlling epithelial expansion and endoplasmic reticulum formation. Endocrinology 157 (2016), 417–428 26562262.
8. Davis, T.A., Fiorotto, M.L., Burrin, D.G., Reeds, P.J., Nguyen, H.V., Beckett, P.R., Vann, R.C., O'Connor, P.M., Stimulation of protein synthesis by both insulin and amino acids is unique to skeletal muscle in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 282 (2002), E880–E890 11882508.
9. Dhar, R., Persaud, S.D., Mireles, J.R., Basu, A., Proteolytic cleavage of p70 ribosomal S6 kinase by caspase-3 during DNA damage-induced apoptosis. Biochemistry 48 (2009), 1474–1480 19191576.
10. Doelman, J., Curtis, R.V., Carson, M., Kim, J.J.M., Metcalf, J.A., Cant, J.P., Essential amino acid infusions stimulate mammary expression of eukaryotic initiation factor 2Bε but milk protein yield is not increased during an imbalance. J. Dairy Sci. 98 (2015), 4499–4508 25912861.
11. Doelman, J., Kim, J.J.M., Carson, M., Metcalf, J.A., Cant, J.P., Branched-chain amino acid and lysine deficiencies exert different effects on mammary translational regulation. J. Dairy Sci. 98 (2015), 7846–7855 26342977.
12. Doepel, L., Lapierre, H., Changes in production and mammary metabolism of dairy cows in response to essential and nonessential amino acid infusions. J. Dairy Sci. 93 (2010), 3264–3274 20630242.
13. Eisenberg, E., Levanon, E.Y., Human housekeeping genes, revisited. Trends Genet. 29 (2013), 569–574 23810203.
14. Hetz, C., Chevet, E., Oakes, S.A., Proteostasis control by the unfolded protein response. Nat. Cell Biol. 17 (2015), 829–838 26123108.
15. Huh, W.J., Esen, E., Geahlen, J.H., Bredemeyer, A.J., Lee, A.-H., Shi, G., Konieczny, S.F., Glimcher, L.H., Mills, J.C., XBP1 controls maturation of gastric zymogenic cells by induction of MIST1 and expansion of the rough endoplasmic reticulum. Gastroenterology 139 (2010), 2038–2049 20816838.
16. Jeyapalan, A.S., Orellana, R.A., Suryawan, A., O'Connor, P.M.J., Nguyen, H.V., Escobar, J., Frank, J.W., Davis, T.A., Glucose stimulates protein synthesis in skeletal muscle of neonatal pigs through an AMPK- and mTOR-independent process. Am. J. Physiol. Endocrinol. Metab. 293 (2007), E595–E603 17551002.
17. Kilberg, M.S., Shan, J., Su, N., ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol. Metab. 20 (2009), 436–443 19800252.
18. Kimball, S.R., Jefferson, L.S., Nguyen, H.V., Suryawan, A., Bush, J.A., Davis, T.A., Feeding stimulates protein synthesis in muscle and liver of neonatal pigs through an mTOR-dependent process. Am. J. Physiol. Endocrinol. Metab. 279 (2000), E1080–E1087 11052963.
19. -ΔΔCT method. Methods 25 (2001), 402–408 11846609.
20. Lobley, G.E., Nutritional and hormonal control of muscle and peripheral tissue metabolism in farm species. Livest. Prod. Sci. 56 (1998), 91–114.
21. Martinon, F., Chen, X., Lee, A.-H., Glimcher, L.H., TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 11 (2010), 411–418 20351694.
22. Metcalf, J.A., Crompton, L.A., Wray-Cahen, D., Lomax, M.A., Sutton, J.D., Beever, D.E., MacRae, J.C., Bequette, B.J., Backwell, F.R.C., Lobley, G.E., Responses in milk constituents to intravascular administration of two mixtures of amino acids to dairy cows. J. Dairy Sci. 79 (1996), 1425–1429 8880466.
23. Moshel, Y., Rhoads, R.E., Barash, I., Role of amino acids in translational mechanisms governing milk protein synthesis in murine and ruminant mammary epithelial cells. J. Cell. Biochem. 98 (2006), 685–700 16440312.
24. Nichols, K., Carson, M., Kim, J.J.M., Metcalf, J.A., Cant, J.P., Doelman, J., Glucose supplementation stimulates peripheral branched-chain amino acid catabolism in lactating dairy cows during essential amino acid infusions. J. Dairy Sci. 99 (2016), 1145–1160 26627857.
25. O'Connor, P.M., Kimball, S.R., Suryawan, A., Bush, J.A., Hguyen, H.V., Jefferson, L.S., Davis, T.A., Regulation of translation initiation by insulin and amino acids in skeletal muscle of neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 285 (2003), E40–E53 12637260.
26. O'Connor, P.M., Kimball, S.R., Suryawan, A., Bush, J.A., Hguyen, H.V., Jefferson, L.S., Davis, T.A., Regulation of neonatal liver protein synthesis by insulin and amino acids in pigs. Am. J. Physiol. Endocrinol. Metab. 286 (2004), E994–E1003 14761876.
27. Piedfer, M., Bouchet, S., Tang, R., Billard, C., Dauzonne, D., Bauvois, B., P70S6 kinase is a target of the novel proteasome inhibitor 3,3′-diamino-4′-methoxyflavone during apoptosis in human myeloid tumor cells. Biochim. Biophys. Acta 1833 (2013), 1316–1328 23481040.
28. Proud, C.G., EIF2 and the control of cell physiology. Semin. Cell Dev. Biol. 16 (2005), 3–12 15659334.
29. Reimold, A.M., Iwakoshi, N.N., Manis, J., Vallabhajosyula, P., Szomolanyi-Tsuda, E., Gravellese, E.M., Friend, D., Grusby, M.J., Alt, F., Glimcher, L.H., Plasma cell differentiation requires the transcription factor XBP-1. Nature 412 (2001), 300–307 11460154.
30. Rius, A.G., Appuhamy, J.A.D.R.N., Cyriac, J., Kirovski, D., Becvar, O., Escobar, J., McGilliard, M.L., Bequette, B.J., Akers, R.M., Hanigan, M.D., Regulation of protein synthesis in mammary glands of lactating dairy cows by starch and amino acids. J. Dairy Sci. 93 (2010), 3114–3127 20630229.
31. Rutkowski, D.T., Hegde, R.S., Regulation of basal cellular physiology by the homeostatic unfolded protein response. J. Cell Biol. 189 (2010), 783–794 20513765.
32. Sadri, H., Giallongo, F., Hristov, A.N., Werner, J., Lang, C.H., Parys, C., Saremi, B., Sauerwein, H., Effects of slow-release urea and rumen-protected methionine and histidine on mammalian target of rapamycin (mTOR) signaling and ubiquitin proteasome-related gene expression in skeletal muscle of dairy cows. J. Dairy Sci. 99 (2016), 6702–6713 27179859.
33. Toerien, C.A., Trout, D.R., Cant, J.P., Nutritional stimulation of milk protein yield of cows is associated with changes in phosphorylation of mammary eukaryotic initiation factor 2 and ribosomal S6 kinase 1. J. Nutr. 140 (2010), 285–292 20032484.
34. Walter, P., Ron, D., The unfolded protein response: From stress pathway to homeostatic regulation. Science 334 (2011), 1081–1086 22116877.
35. Wilson, F.A., Suryawan, A., Gazzaneo, M.C., Orellana, R.A., Nguyen, H.V., Davis, T.A., Stimulation of muscle protein synthesis by prolonged parenteral infusion of leucine is dependent on amino acid availability in neonatal pigs. J. Nutr. 140 (2010), 264–270 20032489.
36. Woo, C.W., Kutzler, L., Kimball, S.R., Tabas, I., Toll-like receptor activation suppresses ER stress factor CHOP and translation inhibition through activation of eIF2B. Nat. Cell Biol. 14 (2012), 192–200 22231169.
37. Wray-Cahen, D., Beckett, P.R., Nguyen, H.V., Davis, T.A., Insulin-stimulated amino acid utilization during glucose and amino acid clamps decreases with development. Am. J. Physiol. 273 (1997), E305–E314 9277383.
38. Wullschleger, S., Loewith, R., Hall, M.N., TOR signaling in growth and metabolism. Cell 124 (2006), 471–484 16469695.