Skip to main content

Intracellular zinc in insulin secretion and action: a determinant of diabetes risk?

  • Guy A. Rutter (a1), Pauline Chabosseau (a1), Elisa A. Bellomo (a2), Wolfgang Maret (a2), Ryan K. Mitchell (a1), David J. Hodson (a1), Antonia Solomou (a1) and Ming Hu (a1)...

Zinc is an important micronutrient, essential in the diet to avoid a variety of conditions associated with malnutrition such as diarrhoea and alopecia. Lowered circulating levels of zinc are also found in diabetes mellitus, a condition which affects one in twelve of the adult population and whose treatments consume approximately 10 % of healthcare budgets. Zn2+ ions are essential for a huge range of cellular functions and, in the specialised pancreatic β-cell, for the storage of insulin within the secretory granule. Correspondingly, genetic variants in the SLC30A8 gene, which encodes the diabetes-associated granule-resident Zn2+ transporter ZnT8, are associated with an altered risk of type 2 diabetes. Here, we focus on (i) recent advances in measuring free zinc concentrations dynamically in subcellular compartments, and (ii) studies dissecting the role of intracellular zinc in the control of glucose homeostasis in vitro and in vivo. We discuss the effects on insulin secretion and action of deleting or over-expressing Slc30a8 highly selectively in the pancreatic β-cell, and the role of zinc in insulin signalling. While modulated by genetic variability, healthy levels of dietary zinc, and hence normal cellular zinc homeostasis, are likely to play an important role in the proper release and action of insulin to maintain glucose homeostasis and lower diabetes risk.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Intracellular zinc in insulin secretion and action: a determinant of diabetes risk?
      Available formats
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Intracellular zinc in insulin secretion and action: a determinant of diabetes risk?
      Available formats
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Intracellular zinc in insulin secretion and action: a determinant of diabetes risk?
      Available formats
Corresponding author
* Corresponding author: G. A. Rutter, email
Hide All
1. Prasad, AS (2013) Discovery of human zinc deficiency: its impact on human health and disease. Adv Nutr 4, 176190.
2. Magneson, GR, Puvathingal, JM & Ray, WJ Jr (1987) The concentrations of free Mg2+ and free Zn2+ in equine blood plasma. J Biol Chem 262, 1114011148.
3. Andreini, C, Banci, LF, Bertini, IF et al. (2006) Counting the zinc-proteins encoded in the human genome. J Proteome Res 5, 196201.
4. Maret, W (2013) Zinc biochemistry: from a single zinc enzyme to a key element of life. Adv Nutr 4, 8291.
5. Huang, L & Tepaamorndech, S (2013) The SLC30 family of zinc transporters - a review of current understanding of their biological and pathophysiological roles. Mol Aspects Med 34, 548560.
6. Jeong, J & Eide, DJ (2013) The SLC39 family of zinc transporters. Mol Aspects Med 34, 612619.
7. Vinkenborg, JL, Nicolson, TJ, Bellomo, EA et al. (2009) Genetically encoded FRET sensors to monitor intracellular Zn2+ homeostasis. Nat Methods 6, 737740.
8. Chabosseau, P, Tuncay, E, Meur, G et al. (2014) Mitochondrial and ER-targeted eCALWY probes reveal high levels of free Zn2+ . ACS Chem Biol 9, 21112120.
9. Taylor, KM, Hiscox, S, Nicholson, RI et al. (2012) Protein kinase CK2 triggers cytosolic zinc signaling pathways by phosphorylation of zinc channel ZIP7. Sci Signal 5, ra11.
10. Krezel, A, Hao, Q & Maret, W (2007) The zinc/thiolate redox biochemistry of metallothionein and the control of zinc ion fluctuations in cell signaling. Arch Biochem Biophys 463, 188200.
11. Li, Y & Maret, W (2009) Transient fluctuations of intracellular zinc ions in cell proliferation. Exp Cell Res 315, 24632470.
12. Hasan, R, Rink, L & Haase, H (2013) Zinc signals in neutrophil granulocytes are required for the formation of neutrophil extracellular traps. Innate Immun 19, 253264.
13. Yamasaki, S, Sakata-Sogawa, K, Hasegawa, A et al. (2007) Zinc is a novel intracellular second messenger. J Cell Biol 177, 637645.
14. Gilon, P, Chae, HY, Rutter, GA et al. (2014) Calcium signaling in pancreatic beta-cells in health and in Type 2 diabetes. Cell Calcium 56, 340361.
15. Laity, JH & Andrews, GK (2007) Understanding the mechanisms of zinc-sensing by metal-response element binding transcription factor-1 (MTF-1). Arch Biochem Biophys 463, 201210.
16. Dean, KM, Qin, Y & Palmer, AE (2012) Visualizing metal ions in cells: an overview of analytical techniques, approaches, and probes. Biochim Biophys Acta 1823, 14061415.
17. de Silva, AP, Fox, DB, Moody, TS et al. (2001) The development of molecular fluorescent switches. Trends Biotechnol 19, 2934.
18. de Silva, AP, Moody, TS & Wright, GD (2009) Fluorescent PET (photoinduced electron transfer) sensors as potent analytical tools. The Analyst 134, 23852393.
19. Carter, KP, Young, AM & Palmer, AE (2014) Fluorescent sensors for measuring metal ions in living systems. Chem Rev 114, 45644601.
20. Zalewski, PD, Forbes, IJ & Betts, WH (1993) Correlation of apoptosis with change in intracellular labile Zn(II) using zinquin [(2-methyl-8-p-toluenesulphonamido-6-quinolyloxy)acetic acid], a new specific fluorescent probe for Zn(II). The Biochem J 296, 403408.
21. Gee, KR, Zhou, ZL, Qian, WJ et al. (2002) Detection and imaging of zinc secretion from pancreatic beta-cells using a new fluorescent zinc indicator. J Am Chem Soc 124, 776778.
22. Tsien, RY (1981) A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290, 527528.
23. Qin, Y, Miranda, JG, Stoddard, CI et al. (2013) Direct comparison of a genetically encoded sensor and small molecule indicator: implications for quantification of cytosolic Zn(2+). ACS Chem Biol 8, 23662371.
24. Thompson, K, Dockery, P & Horobin, RW (2012) Predicting and avoiding subcellular compartmentalization artifacts arising from acetoxymethyl ester calcium imaging probes. The case of fluo-3 AM and a general account of the phenomenon including a problem avoidance chart. Biotech Histochem: Official Pub Biological Stain Commission 87, 468483.
25. Chyan, W, Zhang, DY, Lippard, SJ et al. (2014) Reaction-based fluorescent sensor for investigating mobile Zn2+ in mitochondria of healthy versus cancerous prostate cells. Proc Natl Acad Sci 111, 143148.
26. Li, D, Chen, S, Bellomo, EA et al. (2011) Imaging dynamic insulin release using a fluorescent zinc indicator for monitoring induced exocytotic release (ZIMIR). Proc Natl Acad Sci USA 108, 2106321068.
27. Pancholi, J, Hodson, DJ, Kobe, K et al. (2014) Biologically targeted probes for zinc: a diversity-oriented modular “Click-SNAR” Approach 5, 35283535.
28. Hessels, AM & Merkx, M (2015) Genetically-encoded FRET-based sensors for monitoring Zn(2+) in living cells. Metallomics: Integr Biometal Sci 7, 258266.
29. Dittmer, PJ, Miranda, JG, Gorski, JA et al. (2009) Genetically encoded sensors to elucidate spatial distribution of cellular zinc. J Biol Chem 284, 1628916297.
30. Qin, Y, Dittmer, PJ, Park, JG et al. (2011) Measuring steady-state and dynamic endoplasmic reticulum and Golgi Zn2+ with genetically encoded sensors. Proc Natl Acad Sci USA 108, 73517356.
31. Park, JG, Qin, Y, Galati, DF et al. (2012) New sensors for quantitative measurement of mitochondrial Zn(2+). ACS Chem Biol 7, 16361640.
32. Miranda, JG, Weaver, AL, Qin, Y et al. (2012) New alternately colored FRET sensors for simultaneous monitoring of Zn(2)(+) in multiple cellular locations. PLoS ONE 7, e49371.
33. Bellomo, EA, Meur, G & Rutter, GA (2011) Glucose regulates free cytosolic Zn2+ concentration, Slc39 (ZiP) and metallothionein gene expression in primary pancreatic islet {beta}-cells. J Biol Chem 286, 2577825789.
34. Lindenburg, LH, Hessels, AM, Ebberink, EH et al. (2013) Robust red FRET sensors using self-associating fluorescent domains. ACS Chem Biol 8, 21332139.
35. Bozym, RA, Thompson, RB, Stoddard, AK et al. (2006) Measuring picomolar intracellular exchangeable zinc in PC-12 cells using a ratiometric fluorescence biosensor. ACS Chem Biol 1, 103111.
36. Hurst, TK, Wang, D, Thompson, RB et al. (2010) Carbonic anhydrase II-based metal ion sensing: advances and new perspectives. Biochimica et Biophysica acta 1804, 393403.
37. Scott, DA & Fisher, AM (1938) The Insulin and the zinc content of normal and diabetic pancreas. J Clin Invest 17, 725728.
38. el-Yazigi, A, Hannan, N & Raines, DA (1993) Effect of diabetic state and related disorders on the urinary excretion of magnesium and zinc in patients. Diabetes Res 22, 6775.
39. Garg, VK, Gupta, R & Goyal, RK (1994) Hypozincemia in diabetes mellitus. J Assoc Physicians India 42, 720721.
40. Basaki, M, Saeb, M, Nazifi, S et al. (2012) Zinc, copper, iron, and chromium concentrations in young patients with type 2 diabetes mellitus. Biol Trace Elem Res 148, 161164.
41. Jansen, J, Rosenkranz, E, Overbeck, S et al. (2012) Disturbed zinc homeostasis in diabetic patients by in vitro and in vivo analysis of insulinomimetic activity of zinc. J Nutr Biochem 23, 14581466.
42. Dunn, MF (2005) Zinc-ligand interactions modulate assembly and stability of the insulin hexamer – a review. Biometals 18, 295303.
43. Cruz, KJ, de Oliveira, AR & Marreiro, DN (2015) Antioxidant role of zinc in diabetes mellitus. World J Diabetes 6, 333337.
44. Begin-Heick, N, Dalpe-Scott, M, Rowe, J et al. (1985) Zinc supplementation attenuates insulin secretory activity in pancreatic islets of the ob/ob mouse. Diabetes 34, 179184.
45. Simon, SF & Taylor, CG (2001) Dietary zinc supplementation attenuates hyperglycemia in db/db mice. Exp Biol Med (Maywood) 226, 4351.
46. Wang, X, Li, H, Fan, Z et al. (2012) Effect of zinc supplementation on type 2 diabetes parameters and liver metallothionein expressions in Wistar rats. J Physiol Biochem 68, 563572.
47. Vardatsikos, G, Pandey, NR & Srivastava, AK (2013) Insulino-mimetic and anti-diabetic effects of zinc. J Inorg Biochem 120, 817. Epub@2012 Dec 3., 8–17.
48. Hutton, JC, Penn, EJ & Peshavaria, M (1983) Low-molecular-weight constituents of isolated insulin-secretory vesicles. Bivalent cations, adenine nucleotides and inorganic phosphate. Biochem J 210, 297305.
49. Sondergaard, LG, Stoltenberg, M, Doering, P et al. (2006) Zinc ions in the endocrine and exocrine pancreas of zinc deficient rats. Histol Histopathol 21, 619625.
50. Kahn, SE (2003) The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of Type 2 diabetes. Diabetologia 46, 319.
51. Rutter, GA & Parton, LE (2008) The beta-cell in type 2 diabetes and in obesity. Front Horm Res 36, 118134.
52. Butler, AE, Janson, J, Bonner-Weir, S et al. (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52, 102110.
53. Rahier, J, Guiot, Y, Goebbels, RM et al. (2008) Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab 10, 3242.
54. Stasiuk, GJ, Minuzzi, F, Sae-Hen, M et al. (2015) Dual-modal MR/fluorescent zinc probes towards pancreatic beta cell mass imaging. Chemistry 21, 50235033.
55. Arvan, P & Halban, PA (2004) Sorting ourselves out: seeking consensus on trafficking in the beta-cell. Traffic 5, 5361.
56. Rutter, GA, Pullen, TJ, Hodson, DJ et al. (2015) Pancreatic beta cell identity, glucose sensing and the control of insulin secretion. Biochem J 466, 202218.
57. Rutter, GA, Pralong, W-F & Wollheim, CB (1992) Regulation of mitochondrial glycerol phosphate dehydrogenase activity by Ca2+ within electropermeabilized insulin-secreting cells (INS1). Biochimica et Biophysica Acta – Bioenergetics 1175, 107113.
58. Tarasov, AI, Ravier, MA, Semplici, F et al. (2012) The mitochondrial Ca2+ uniporter MCU is essential for glucose-induced ATP increases in pancreatic â-cells. PLoS ONE 7, e39722.
59. Rutter, GA, Theler, J-M, Li, G et al. (1994) Ca2+ stores in insulin-secreting cells: lack of effect of cADP ribose. Cell Calcium 16, 7180.
60. Rutter, GA (2004) Visualising insulin secretion. The minkowski lecture 2004. Diabetologia 47, 18611872.
61. Chimienti, F, Devergnas, S, Favier, A et al. (2004) Identification and cloning of a beta-cell-specific zinc transporter, ZnT-8, localized into insulin secretory granules. Diabetes 53, 23302337.
62. Wenzlau, JM, Juhl, K, Yu, L et al. (2007) The cation efflux transporter ZnT8 (Slc30A8) is a major autoantigen in human type 1 diabetes. Proc Natl Acad Sci USA 104, 1704017045.
63. Sladek, R, Rocheleau, G, Rung, J et al. (2007) A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445, 881885.
64. Staiger, H, Machicao, F, Stefan, N et al. (2007) Polymorphisms within novel risk loci for type 2 diabetes determine beta-cell function. PLoS ONE 2, e832.
65. Kirchhoff, K, Machicao, F, Haupt, A et al. (2008) Polymorphisms in the TCF7L2, CDKAL1 and SLC30A8 genes are associated with impaired proinsulin conversion. Diabetologia 51, 597601.
66. Dimas, AS, Lagou, V, Barker, A et al. (2014) Impact of type 2 diabetes susceptibility variants on quantitative glycemic traits reveals mechanistic heterogeneity. Diabetes 63, 21582171.
67. Ruchat, SM, Elks, CE, Loos, RJ et al. (2009) Association between insulin secretion, insulin sensitivity and type 2 diabetes susceptibility variants identified in genome-wide association studies. Acta Diabetol 46, 217226.
68. Cauchi, S, Del, GS, Choquet, H et al. (2010) Meta-analysis and functional effects of the SLC30A8 rs13266634 polymorphism on isolated human pancreatic islets. Mol Genet Metab 100, 7782.
69. Kanoni, S, Nettleton, JA, Hivert, MF et al. (2011) Total zinc intake may modify the glucose-raising effect of a zinc transporter (SLC30A8) variant: a 14-Cohort meta-analysis. Diabetes 60, 24072416.
70. Flannick, J, Thorleifsson, G, Beer, NL et al. (2014) Loss-of-function mutations in SLC30A8 protect against type 2 diabetes. Nat Genet 46, 357363.
71. Chao, Y & Fu, D (2004) Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J Biol Chem 279, 1717317180.
72. Nicolson, TJ, Bellomo, EA, Wijesekara, N et al. (2009) Insulin storage and glucose homeostasis in mice null for the granule zinc transporter ZnT8 and studies of the type 2 diabetes-associated variants. Diabetes 58, 20702083.
73. Weijers, RN (2010) Three-dimensional structure of beta-cell-specific zinc transporter, ZnT-8, predicted from the type 2 diabetes-associated gene variant SLC30A8 R325W. Diabetol Metab Syndr 2, 33.
74. Kim, H, Toyofuku, Y, Lynn, FC et al. (2010) Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 16, 804808.
75. Lemaire, K, Ravier, MA, Schraenen, A et al. (2009) Insulin crystallization depends on zinc transporter ZnT8 expression, but is not required for normal glucose homeostasis in mice. Proc Natl Acad Sci USA 106, 1487214877.
76. Pound, LD, Sarkar, SA, Benninger, RK et al. (2009) Deletion of the mouse Slc30a8 gene encoding zinc transporter-8 results in impaired insulin secretion. Biochem J 421, 371376.
77. Gerber, PA, Bellomo, EA, Hodson, DJ et al. (2014) Hypoxia lowers SLC30A8/ZnT8 expression and free cytosolic Zn2+ in pancreatic beta cells. Diabetologia 57, 16351644.
78. Wijesekara, N, Dai, FF, Hardy, AB et al. (2010) Beta cell specific ZnT8 deletion in mice causes marked defects in insulin processing, crystallisation and secretion. Diabetologia 53, 16561668.
79. Tamaki, M, Fujitani, Y, Hara, A et al. (2013) The diabetes-susceptible gene SLC30A8/ZnT8 regulates hepatic insulin clearance. J Clin Invest 123, 45134524.
80. Wicksteed, B, Brissova, M, Yan, W et al. (2010) Conditional gene targeting in mouse pancreatic {beta}-cells: analysis of ectopic cre transgene expression in the brain. Diabetes 59, 30903098.
81. Rutter, GA (2010) Think zinc: new roles for zinc in the control of insulin secretion. Islets 2, 12.
82. Rutter, GA & Chimienti, F (2015) SLC30A8 mutations in type 2 diabetes. Diabetologia 58, 3136.
83. Hardy, AB, Wijesekara, N, Genkin, I et al. (2012) Effects of high-fat diet feeding on Znt8-null mice: differences between beta-cell and global knockout of Znt8. Am J Physiol Endocrinol Metab 302, E1084E1096.
84. Brouwers, B, de, FG, Osipovich, AB et al. (2014) Impaired islet function in commonly used transgenic mouse lines due to human growth hormone minigene expression. Cell Metab 20, 979990.
85. Thorens, B, Tarussio, D, Maestro, MA et al. (2015) Ins1 knock-in mice for beta cell-specific gene recombination. Diabetologia 58, 558656.
86. Mitchell, RK, Hu, M, Meur, G et al. (2015) Reciprocal changes in glucose tolerance after pancreatic beta cell-selective deletion or over-expression of Slc30a8/ZnT8 in mice Diabetologia (In the Press).
87. Pullen, TJ, Sylow, L, Sun, G et al. (2012) Over-expression of Monocarboxylate transporter-1 (Slc16a1) in the pancreatic â-cell leads to relative hyperinsulinism during exercise. Diabetes 61, 17191725.
88. Slepchenko, KG, James, CB & Li, YV (2013) Inhibitory effect of zinc on glucose-stimulated zinc/insulin secretion in an insulin-secreting beta-cell line. Exp Physiol 98, 13011311.
89. Schweiger, M, Steffl, M & Amselgruber, WM (2013) The zinc transporter ZnT8 (slc30A8) is expressed exclusively in beta cells in porcine islets. Histochem Cell Biol 140, 677684.
90. Souza, SC, Qui, L, Inouye, K et al. (2008) Zinc transporter ZnT-8 regulates insulin and glucagon secretion in Min6 and alphaTC1-9 pancreatic cell lines. Diabetologia 51, S206.
91. Ishihara, H, Maechler, P, Gjinovci, A et al. (2003) Islet beta-cell secretion determines glucagon release from neighbouring alpha-cells. Nat Cell Biol 5, 330335.
92. Franklin, I, Gromada, J, Gjinovci, A et al. (2005) Beta-cell secretory products activate alpha-cell ATP-dependent potassium channels to inhibit glucagon release. Diabetes 54, 18081815.
93. Gyulkhandanyan, AV, Lu, H, Lee, SC et al. (2008) Investigation of transport mechanisms and regulation of intracellular Zn2+ in pancreatic alpha-cells. J Biol Chem 283, 1018410197.
94. Hardy, AB, Serino, AS, Wijesekara, N et al. (2011) Regulation of glucagon secretion by zinc: lessons from the beta cell-specific Znt8 knockout mouse model. Diabetes Obes Metab 13 (Suppl. 1), 112117.
95. Solomou, A, Meur, G, Bellomo, EA et al. (2015) The zinc transporter Slc30a8/ZnT8 is required in a subpopulation of pancreatic á cells for hypoglycemia-induced glucagon secretion. J Biol Chem (Epublication ahead of print version).
96. Lee, J & Pilch, PF (1994) The insulin receptor: structure, function, and signaling. Am J Physiol 266, C319C334.
97. Kanzaki, M (2006) Insulin receptor signals regulating GLUT4 translocation and actin dynamics. Endocr J 53, 267293.
98. Coulston, L & Dandona, P (1980) Insulin-like effect of zinc on adipocytes. Diabetes 29, 665667.
99. Miranda, ER & Dey, CS (2004) Effect of chromium and zinc on insulin signaling in skeletal muscle cells. Biol Trace Elem Res 101, 1936.
100. Haase, H & Maret, W (2003) Intracellular zinc fluctuations modulate protein tyrosine phosphatase activity in insulin/insulin-like growth factor-1 signaling. Exp Cell Res 291, 289298.
101. Tang, X & Shay, NF (2001) Zinc has an insulin-like effect on glucose transport mediated by phosphoinositol-3-kinase and Akt in 3T3-L1 fibroblasts and adipocytes. J Nutr 131, 14141420.
102. Wu, W, Wang, X, Zhang, W et al. (2003) Zinc-induced PTEN protein degradation through the proteasome pathway in human airway epithelial cells. J Biol Chem 278, 2825828263.
103. Plum, LM, Brieger, A, Engelhardt, G et al. (2014) PTEN-inhibition by zinc ions augments interleukin-2-mediated Akt phosphorylation. Metallomics 6, 12771287.
104. Bellomo, E, Massarotti, A, Hogstrand, C et al. (2014) Zinc ions modulate protein tyrosine phosphatase 1B activity. Metallomics 6, 12291239.
105. Barthel, A, Ostrakhovitch, EA, Walter, PL et al. (2007) Stimulation of phosphoinositide 3-kinase/Akt signaling by copper and zinc ions: mechanisms and consequences. Arch Biochem Biophys 463, 175182.
106. Myers, SA, Nield, A, Chew, GS et al. (2013) The zinc transporter, Slc39a7 (Zip7) is implicated in glycaemic control in skeletal muscle cells. PLoS ONE 8, e79316.
107. Zhu, K, Nie, S, Li, C et al. (2013) Antidiabetic and pancreas-protective effects of zinc threoninate chelate in diabetic rats may be associated with its antioxidative stress ability. Biol Trace Elem Res 153, 291298.
108. Karatug, A, Kaptan, E, Bolkent, S et al. (2013) Alterations in kidney tissue following zinc supplementation to STZ-induced diabetic rats. J Trace Elem Med Biol 27, 5257.
109. Pound, LD, Sarkar, SA, Ustione, A et al. (2012) The physiological effects of deleting the mouse slc30a8 gene encoding zinc transporter-8 are influenced by gender and genetic background. PLoS ONE 7, e40972.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Proceedings of the Nutrition Society
  • ISSN: 0029-6651
  • EISSN: 1475-2719
  • URL: /core/journals/proceedings-of-the-nutrition-society
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 148
Total number of PDF views: 482 *
Loading metrics...

Abstract views

Total abstract views: 901 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 24th April 2018. This data will be updated every 24 hours.