Maternal taurine supplementation in rats partially prevents the adverse effects of early-life protein deprivation on β-cell function and insulin sensitivity

Reproduction

Volumn 145, Issue 6, 2013, Pages 609-620

  Tang, Christine ^a   Marchand, Kelly ^b   Lam, Loretta ^a   Lux Lantos, Victoria ^c   Thyssen, Sandra M ^b   Guo, June ^a   Giacca, Adria ^a   Arany, Edith ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

C PEPTIDE; GLUCOSE; INSULIN; TAURINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; FEMALE; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; IMPAIRED GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LACTATION; MALE; NONHUMAN; PANCREAS ISLET BETA CELL; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROTEIN INTAKE; RAT; WEANING;

ANIMALS; C-PEPTIDE; DIABETES MELLITUS, TYPE 2; DIET, PROTEIN-RESTRICTED; DIETARY PROTEINS; DIETARY SUPPLEMENTS; FEMALE; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; LACTATION; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PREGNANCY; PREGNANCY COMPLICATIONS; PROTEIN DEFICIENCY; RATS; RATS, WISTAR; SEX CHARACTERISTICS; TAURINE; WEANING;

EID: 84877996148     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-12-0388     Document Type: Article

References (55)

1. Arany E, Strutt B, Romanus P, Remacle C, Reusens B & Hill DJ 2004 Taurine supplement in early life altered islet morphology, decreased insulitis and delayed the onset of diabetes in non-obese diabetic mice. Diabetologia 47 1831-1837. (doi:10.1007/s00125-004-1535-z)
2. Bergman RN, Phillips LS & Cobelli C 1981 Physiologic evaluation of factors controlling glucose tolerance in man: measurement of insulin sensitivity and β-cell glucose sensitivity from the response to intravenous glucose. Journal of Clinical Investigation 68 1456-1467. (doi:10.1172/JCI110398)
3. Bergman RN, Ader M, Huecking K & Van Citters G 2002 Accurate assessment of β-cell function: the hyperbolic correction. Diabetes 51 (Suppl 1) S212-S220. (doi:10.2337/diabetes.51.2007.S212)
4. Bouckenooghe T, Remacle C & Reusens B 2006 Is taurine a functional nutrient? Current Opinion in Clinical Nutrition and Metabolic Care 9 728-733. (doi:10.1097/01.mco.0000247469.26414.55)
5. Boujendar S, Reusens B, Merezak S, Ahn MT, Arany E, Hill D & Remacle C 2002 Taurine supplementation to a low protein diet during foetal and early postnatal life restores a normal proliferation and apoptosis of rat pancreatic islets. Diabetologia 45 856-866. (doi:10.1007/s00125-002-0833-6)
6. Boujendar S, Arany E, Hill D, Remacle C & Reusens B 2003 Taurine supplementation of a low protein diet fed to rat dams normalizes the vascularization of the fetal endocrine pancreas. Journal of Nutrition 133 2820-2825. (Pubitemid 37099765)
7. Chamson-Reig A, Thyssen SM, Hill DJ & Arany E 2009 Exposure of the pregnant rat to low protein diet causes impaired glucose homeostasis in the young adult offspring by different mechanisms in males and females. Experimental Biology and Medicine 234 1425-1436. (doi:10.3181/0902-RM-69)
8. Cherif H, Reusens B, Ahn MT, Hoet JJ & Remacle C 1998 Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. Journal of Endocrinology 159 341-348. (doi:10.1677/joe.0.1590341)
9. Chintoh AF, Mann SW, Lam L, Giacca A, Fletcher P, Nobrega J & Remington G 2009 Insulin resistance and secretion in vivo: effects of different antipsychotics in an animal model. Schizophrenia Research 108 127-133. (doi:10.1016/j.schres.2008.12.012)
10. Dahri S, Snoeck A, Reusens-Billen B, Remacle C & Hoet JJ 1991 Islet function in offspring of mothers on low-protein diet during gestation. Diabetes 40 (Suppl 2) 115-120.
11. Dahri S, Reusens B, Remacle C & Hoet JJ 1995 Nutritional influences on pancreatic development and potential links with non-insulin-dependent diabetes. Proceedings of the Nutrition Society 54 345-356. (doi:10.1079/ PNS19950003)
12. De Fronzo RA, Tobin JD & Andres R 1979 Glucose clamp technique: a method quantifying insulin secretion and resistance. American Journal of Physiology 237 E214-E223. (Pubitemid 9249478)
13. Desai M, Growther NJ, Lucas A & Hales CN 1996 Organ-selective growth in the offspring of protein-restricted mothers. British Journal of Nutrition 76 591-603. (doi:10.1079/BJN19960065)
14. Desai M, Byrne CD, Zhang J, Petry CJ, Lucas A & Hales CN 1997 Programming of hepatic insulin-sensitive enzymes in offspring of rat dams fed a protein-restricted diet. American Journal of Physiology 272 G1083-G1090.
15. Durst MA, Lux-Lantos VA, Hardy DB, Hill DJ & Arany EJ 2012 Protein restriction during early life in rats alters pancreatic GABAa receptor subunit expression and glucagon secretion in adulthood. Canadian Journal of Diabetes 36 100-107. (doi:10.1016/j.jcjd.2012.06.002)
16. Evans JL, Goldfine ID, Maddux BA & Grodsky GM 2003 Are oxidative stress-activated signaling pathways mediators of insulin resistance and β-cell dysfunction? Diabetes 52 1-8. (doi:10.2337/diabetes.52.1.1)
17. Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin MS, Hales CN & Ozanne SE 2005 Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 288 R368-R373. (doi:10.1152/ajpregu.00206.2004)
18. Finegood DT, Bergman RN & Vranic M 1987 Estimation of endogenous glucose production during hyperinsulinemic-euglycemic glucose clamps. Comparison of unlabeled and labeled exogenous glucose infusates. Diabetes 36 914-924. (doi:10.2337/diabetes.36.8.914)
19. Forsen T, Eriksson J, Tuomilehto J, Reunanen A, Osmond C & Barker D 2000 The fetal and childhood growth of persons who develop type 2 diabetes. Annals of Internal Medicine 133 176-182. (doi:10.7326/0003-4819-133-3-200008010- 00008)
20. Fortman J II, Reichling T & German RZ 2005 The impact of maternal protein malnutrition on pre-weaning skeletal and visceral organ growth in neonatal offspring of Rattus norvegicus. Growth, Development, and Aging 69 39-52. (Pubitemid 41387689)
21. Garcia-Souza EP, da Silva SV, Felix GB, Rodrigues AL, de Freitas MS, Moura AS & Barja-Fidalgo C 2008 Maternal protein restriction during early lactation induces GLUT4 translocation and mTOR/Akt activation in adipocytes of adult rats. American Journal of Physiology. Endocrinology and Metabolism 295 E626-E636. (doi:10.1152/ajpendo.00439.2007)
22. Gluckman PD & Hanson MA 2006 The consequences of being born small - an adaptive perspective. Hormone Research 65 (Suppl 3) 5-14. (doi:10.1159/000091500)
23. Goh TT, Mason TM, Gupta N, So A, Lam TK, Lam L, Lewis GF, Mari A & Giacca A 2007 Lipid-induced β-cell dysfunction in vivo in models of progressive b-cell failure. American Journal of Physiology. Endocrinology and Metabolism 292 E549-E560. (doi:10.1152/ajpendo.00255.2006)
24. Hales CN & Barker DJ 1992 Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35 595-601. (doi:10.1007/BF00400248)
25. Hales CN & Barker DJ 2001 The thrifty phenotype hypothesis. British Medical Bulletin 60 5-20. (doi:10.1093/bmb/60.1.5)
26. Han J, Bae JH, Kim SY, Lee HY, Jang BC, Lee IK, Cho CH, Lim JG, Suh SI, Kwon TK et al. 2004 Taurine increases glucose sensitivity of UCP2-overexpressing β-cells by ameliorating mitochondrial metabolism. American Journal of Physiology. Endocrinology and Metabolism 287 E1008-E1018. (doi:10.1152/ajpendo. 00008.2004)
27. Hansen SH 2001 The role of taurine in diabetes and the development of diabetic complications. Diabetes/Metabolism Research and Reviews 17 330-346. (doi:10.1002/dmrr.229)
28. Hojlund K, Mogensen M, Sahlin K & Beck-Nielsen H 2008 Mitochondrial dysfunction in type 2 diabetes and obesity. Endocrinology and Metabolism Clinics of North America 37 713-731, x. (doi:10.1016/j.ecl.2008.06.006)
29. Hotamisligil GS 2006 Inflammation and metabolic disorders. Nature 444 860-867. (doi:10.1038/nature05485)
30. Huxtable RJ 1992 Physiological actions of taurine. Physiological Reviews 72 101-163.
31. Kahn SE, Prigeon RL, McCulloch DK, Boyko EJ, Bergman RN, Schwartz MW, Neifing JL, Ward WK, Beard JC & Palmer JP 1993 Quantification of the relationship between insulin sensitivity and β-cell function in human subjects. Evidence for a hyperbolic function. Diabetes 42 1663-1672. (doi:10.2337/diabetes.42.11.1663)
32. Lam TK, Yoshii H, Haber CA, Bogdanovic E, Lam L, Fantus IG & Giacca A 2002 Free fatty acid-induced hepatic insulin resistance: a potential role for protein kinase C-δ. American Journal of Physiology. Endocrinology and Metabolism 283 E682-E691. (doi:10.1154/ajendo.00038.2002)
33. Lee YY, Lee HJ, Lee SS, Koh JS, Jin CJ, Park SH, Yi KH, Park KS & Lee HK 2011 Taurine supplementation restored the changes in pancreatic islet mitochondria in the fetal protein-malnourished rat. British Journal of Nutrition 106 1198-1206. (doi:10.1017/S0007114511001632)
34. Lourenco R & Camilo ME 2002 Taurine: a conditionally essential amino acid in humans? An overview in health and disease Nutrición Hospitalaria 17 262-270. (Pubitemid 44616128)
35. Mason TM, Goh T, Tchipashvili V, Sandhu H, Gupta N, Lewis GF & Giacca A 1999 Prolonged elevation of plasma free fatty acids desensitizes the insulin secretory response to glucose in vivo in rats. Diabetes 48 524-530. (doi:10.2337/diabetes.48.3.524)
36. Merezak S, Hardikar AA, Yajnik CS, Remacle C & Reusens B 2001 Intrauterine low protein diet increases fetal β-cell sensitivity to NO and IL-1β: the protective role of taurine. Journal of Endocrinology 171 299-308. (doi:10.1677/joe.0.1710299)
37. Merezak S, Reusens B, Renard A, Goosse K, Kalbe L, Ahn MT, Tamarit-Rodriguez J & Remacle C 2004 Effect of maternal low-protein diet and taurine on the vulnerability of adult Wistar rat islets to cytokines. Diabetologia 47 669-675. (doi:10.1007/s00125-004-1357-z)
38. Minana-Solis Mdel C & Escobar C 2008 Post-weaning protein malnutrition in the rat produces short and long term metabolic impairment, in contrast to earlier and later periods. International Journal of Biological Sciences 4 422-432. (doi:10.7150/ijbs.4.422)
39. Oprescu AI, Bikopoulos G, Naassan A, Allister EM, Tang C, Park E, Uchino H, Lewis GF, Fantus IG, Rozakis-Adcock M et al. 2007 Free fatty acid-induced reduction in glucose stimulated insulin secretion evidence for a role of oxidative stress in vitro and in vivo. Diabetes 56 2027-2937. (doi:10.2337/db07-0075)
40. Ozanne SE,Wang CL, Coleman N & Smith GD 1996 Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. American Journal of Physiology 271 E1128-E1134.
41. Ozanne SE, Nave BT,Wang CL, Shepherd PR, Prins J & SmithGD 1997 Poor fetal nutrition causes long-term changes in expression of insulin signaling components in adipocytes. American Journal of Physiology 273 E46-E51.
42. Ozanne SE, Olsen GS, Hansen LL, Tingey KJ, Nave BT, Wang CL, Hartil K, Petry CJ, Buckley AJ & Mosthaf-Seedorf L 2003 Early growth restriction leads to down regulation of protein kinase Cζ and insulin resistance in skeletal muscle. Journal of Endocrinology 177 235-241. (doi:10.1677/joe.0.1770235)
43. Petrik J, Reusens B, Arany E, Remacle C, Coelho C, Hoet JJ & Hill DJ 1999 A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II. Endocrinology 140 4861-4873. (doi:10.1210/en.140.10.4861)
44. Rehfeldt C, Lefaucheur L, Block J, Stabenow B, Pfuhl R, Otten W, Metges CC & Kalbe C 2012 Limited and excess protein intake of pregnant gilts differently affects body composition and cellularity of skeletal muscle and subcutaneous adipose tissue of newborn and weanling piglets. European Journal of Nutrition 51 151-165. (doi:10.1007/s00394-011-0201-8)
45. Reusens BDS, Snoek A, Bennis-Taleb N, Remacle C & Hoett JJ 1995 Long-term consequences of diabetes and its complications may have a fetal origin: experimental and epidemiological evidence. In Diabetes. Nestle: Workshop Series, 25, pp 187-188. Ed. RM Edit Cowett. New York: Raven Press.
46. Sandovici I, Smith NH, Nitert MD, Ackers-Johnson M, Uribe-Lewis S, Ito Y, Jones RH, Marquez VE, Cairns W, Tadayyon M et al. 2011 Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. PNAS 108 5449-5454. (doi:10.1073/pnas.1019007108)
47. Shaw JE, Sicree RA & Zimmet PZ 2010 Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Research and Clinical Practice 87 4-14. (doi:10.1016/j.diabres.2009.10.007)
48. Shepherd PR, Crowther NJ, Desai M, Hales CN & Ozanne SE 1997 Altered adipocyte properties in the offspring of protein malnourished rats. British Journal of Nutrition 78 121-129. (doi:10.1079/BJN19970124)
49. Snoeck A, Remacle C, Reusens B & Hoet JJ 1990 Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biology of the Neonate 57 107-118. (doi:10.1159/000243170)
50. Steele R, Wall JS, De Bodo RC & Altszuler N 1956 Measurement of size and turnover rate of body glucose pool by the isotope dilution method. American Journal of Physiology 187 15-24.
51. Sturman JA 1993 Taurine in development. Physiological Reviews 73 119-147.
52. Sugden MC & Holness MJ 2002 Gender-specific programming of insulin secretion and action. Journal of Endocrinology 175 757-767. (doi:10.1677/joe.0. 1750757)
53. Suzuki T, Wada T, Saigo K & Watanabe K 2002 Taurine as a constituent of mitochondrial tRNAs: new insights into the functions of taurine and human mitochondrial diseases. EMBO Journal 21 6581-6589. (doi:10.1093/emboj/cdf656)
54. Tang C, Han P, Oprescu AI, Lee SC, Gyulkhandanyan AV, Chan GN, Wheeler MB & Giacca A 2007 Evidence for a role of superoxide generation in glucose-induced b-cell dysfunction in vivo. Diabetes 56 2722-2731. (doi:10.2337/db07-0279)
55. Zambrano E, Bautista CJ, Deas M, Martinez-Samayoa PM, Gonzalez-Zamorano M, Ledesma H, Morales J, Larrea F & Nathanielsz PW 2006 A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. Journal of Physiology 571 221-230. (doi:10.1113/jphysiol.2005.100313)