plasma insulin levels are rather similar in chicken and rat

2
Viewpoint Plasma insulin levels are rather similar in chicken and rat A brief overview of literature permitted to conclude that fasting plasma insulin levels are in the same range in chicken and 6 mam- malian species (including rat, [35]). In a subsequent study from our group, much higher plasma insulin levels were found in fasted rats than in fasted chickens (Dupont et al., [8]; quoted in a review by Braun and Sweazea [5]). This result could lead to hypothesize that low plasma insulin levels are contributing to the high constitutive plasma glucose levels found in chickens. To clarify this point, we more extensively reviewed the literature. As summarized in Table 1, the high value found for plasma insulin of fasted rats in one as- say by our group is, for an unknown reason, totally out of range. Chicken plasma insulin levels (as determined by an homologous assay, McMurtry’s group at Beltsville, USA or an heterologous as- say, Simon’s group at Nouzilly, France) are in fact rather similar to those found in rat, both in the fasted or the fed status. Therefore, as previously hypothesized, the high glycemia found in chickens despite the presence of an hyperactive insulin circulating at ‘‘nor- mal’’ levels is certainly due to multiple mechanisms; several of them are most likely related to the control of insulin release and/ or the action of insulin in target tissues (see references quoted in [9,26]). References [1] C.M. Ashwell, J.P. McMurtry, Hypoglycemia and reduced feed intake in broiler chickens treated with metformin, Poult. Sci. 82 (2003) 106–110. [2] C. Beccavin, B. Chevalier, L.A. Cogburn, J. Simon, M.J. Duclos, Insulin-like growth factors and body growth in chickens divergently selected for high or low growth rate, J. Endocrinol. 168 (2001) 297–306. [3] S. Bisbis, M. Derouet, J. Simon, Characterization of insulin receptors in chicken kidneys: effect of nutritional status, Gen. Comp. Endocrinol. 96 (1994) 37–49. [4] N. Brandt, K. De Bock, E.A. Richter, P. Hespel, Cafeteria diet-induced insulin resistance is not associated with decreased insulin signaling or AMPK activity and is alleviated by physical training in rats, Am. J. Physiol. Endocrinol. Metab. 299 (2010) E215–E224. [5] E.J. Braun, K.L. Sweazea, Glucose regulation in birds, Comp. Biochem. Physiol. B Biochem. Mol. Biol. 151 (2008) 1–9. [6] S.E. Chen, J.P. McMurtry, R.L. Walzem, Overfeeding-induced ovarian dysfunction in broiler breeder hens is associated with lipotoxicity, Poult. Sci. 85 (2006) 70–81. [7] A. Cryer, S.E. Riley, E.R. Williams, D.S. Robinson, Effects of fructose, sucrose and glucose feeding on plasma insulin concentrations and on adipose-tissue clearing-factor lipase activity in the rat, Biochem. J. 140 (1974) 561–563. [8] J. Dupont, C. Dagou, M. Derouet, J. Simon, M. Taouis, Early steps of insulin receptor signaling in chicken and rat: apparent refractoriness in chicken muscle, Domest. Anim. Endocrinol. 26 (2004) 127–142. [9] J. Dupont, S. Tesseraud, J. Simon, Insulin signaling in chicken liver and muscle, Gen. Comp. Endocrinol. 163 (2009) 52–57. [10] M.R. Edwards, J.P. McMurtry, R. Vasilatos-Younken, Relative insensitivity of avian skeletal muscle glycogen to nutritive status, Domest. Anim. Endocrinol. 16 (1999) 239–247. [11] C.M. Evock-Clover, S.M. Poch, M.P. Richards, C.M. Ashwell, J.P. McMurtry, Expression of an uncoupling protein gene homolog in chickens, Comp. Biochem. Physiol. A Mol. Integr. Physiol. 133 (2002) 345–358. [12] C. Gàcs, The mechanism of hypoglycemia due to semistarvation in the rat, J. Nutr. 106 (1976) 1557–1561. [13] J.R. Girard, G.S. Cuendet, E.B. Marliss, A. Kervran, M. Rieutort, R. Assan, Fuels, hormones, and liver metabolism at term and during the early postnatal period in the rat, J. Clin. Invest. 52 (1973) 3190–3200. Table 1 Plasma glucose and insulin levels in fasted or fed rats and chickens. a Species Rat Chicken Nutritional status Fasted Fed Fasted Fed Research group Nouzilly Beltsville Nouzilly Beltsville Glucose (mg/100 ml) 88 ± 8 n = 10 137 ± 8 n = 11 215 ± 4 b n =8 237 ± 5 n =5 241 ± 7 b n =7 233 ± 15 n =8 Insulin (ng/ml) 0.59 ± 0.13 n = 10 (3.44) c 2.06 ± 0.27 n = 11 0.60 ± 0.10 n =8 0.70 ± 0.33 n =5 1.87 ± 0.42 n =7 2.17 ± 0.43 n = 10 a Data (mean ± SE) are issued from experiments using regular diets or a moderately high fat diet in one rat experiment. In each experiment, only data from control groups were used for both species (i.e., lean or high growth breeds). Chickens were all of broiler type (i.e., heavy breeds or crosses). Rat experiments were chosen at random. In some experiments, rat glucose levels were blood levels, which, in this species, are similar to plasma levels (for this, chickens differ). Also in rats, some plasma insulin levels were reported in lU/ml; these data have been converted in ng/ml (1 lU = 40 pg). In both species, young and adult individuals, mostly males, were involved. References according to species were as follows: fasted rats [4,7,12,14–16,19,21,29,37], fed rats [7,13,14,18,22,23,25,29,30,39,41], fasted chickens at Nouzilly [2,3,8,17,28,31–33], fed chickens at Nouzilly [2,3,17,28,31–33] (in [33], values were from re-fed chickens, at 90 min refeeding following an overnight fast), fasted chickens at Beltsville: [11,24,27,34,36] and fed chickens at Beltsville: [1,6,10,11,20,27,34,38,40]. b These glucose levels were obtained using a glucose oxidase method not coupled to a colorimetric reaction, avoiding interferences and leading to the minimal values. c This plasma insulin value (from [8]) was excluded from the mean. 0016-6480/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ygcen.2011.02.025 General and Comparative Endocrinology 171 (2011) 267–268 Contents lists available at ScienceDirect General and Comparative Endocrinology journal homepage: www.elsevier.com/locate/ygcen

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Page 1: Plasma insulin levels are rather similar in chicken and rat

General and Comparative Endocrinology 171 (2011) 267–268

Contents lists available at ScienceDirect

General and Comparative Endocrinology

journal homepage: www.elsevier .com/locate /ygcen

Viewpoint

Plasma insulin levels are rather similar in chicken and rat

A brief overview of literature permitted to conclude that fastingplasma insulin levels are in the same range in chicken and 6 mam-malian species (including rat, [35]). In a subsequent study from ourgroup, much higher plasma insulin levels were found in fasted ratsthan in fasted chickens (Dupont et al., [8]; quoted in a review byBraun and Sweazea [5]). This result could lead to hypothesize thatlow plasma insulin levels are contributing to the high constitutiveplasma glucose levels found in chickens. To clarify this point, wemore extensively reviewed the literature. As summarized in Table1, the high value found for plasma insulin of fasted rats in one as-say by our group is, for an unknown reason, totally out of range.Chicken plasma insulin levels (as determined by an homologousassay, McMurtry’s group at Beltsville, USA or an heterologous as-say, Simon’s group at Nouzilly, France) are in fact rather similarto those found in rat, both in the fasted or the fed status. Therefore,as previously hypothesized, the high glycemia found in chickensdespite the presence of an hyperactive insulin circulating at ‘‘nor-mal’’ levels is certainly due to multiple mechanisms; several ofthem are most likely related to the control of insulin release and/or the action of insulin in target tissues (see references quoted in[9,26]).

References

[1] C.M. Ashwell, J.P. McMurtry, Hypoglycemia and reduced feed intake in broilerchickens treated with metformin, Poult. Sci. 82 (2003) 106–110.

Table 1Plasma glucose and insulin levels in fasted or fed rats and chickens.a

Species Rat C

Nutritional status Fasted Fed Fa

Research group N

Glucose (mg/100 ml) 88 ± 8n = 10

137 ± 8n = 11

2n

Insulin (ng/ml) 0.59 ± 0.13n = 10 (3.44)c

2.06 ± 0.27n = 11

0n

a Data (mean ± SE) are issued from experiments using regular diets or a moderately hiwere used for both species (i.e., lean or high growth breeds). Chickens were all of broiler texperiments, rat glucose levels were blood levels, which, in this species, are similar to preported in lU/ml; these data have been converted in ng/ml (1 lU = 40 pg). In both specto species were as follows: fasted rats [4,7,12,14–16,19,21,29,37], fed rats [7,13,14,18,22Nouzilly [2,3,17,28,31–33] (in [33], values were from re-fed chickens, at 90 min refeedinchickens at Beltsville: [1,6,10,11,20,27,34,38,40].

b These glucose levels were obtained using a glucose oxidase method not coupled toc This plasma insulin value (from [8]) was excluded from the mean.

0016-6480/$ - see front matter � 2011 Elsevier Inc. All rights reserved.doi:10.1016/j.ygcen.2011.02.025

[2] C. Beccavin, B. Chevalier, L.A. Cogburn, J. Simon, M.J. Duclos, Insulin-likegrowth factors and body growth in chickens divergently selected for high orlow growth rate, J. Endocrinol. 168 (2001) 297–306.

[3] S. Bisbis, M. Derouet, J. Simon, Characterization of insulin receptors in chickenkidneys: effect of nutritional status, Gen. Comp. Endocrinol. 96 (1994) 37–49.

[4] N. Brandt, K. De Bock, E.A. Richter, P. Hespel, Cafeteria diet-induced insulinresistance is not associated with decreased insulin signaling or AMPK activityand is alleviated by physical training in rats, Am. J. Physiol. Endocrinol. Metab.299 (2010) E215–E224.

[5] E.J. Braun, K.L. Sweazea, Glucose regulation in birds, Comp. Biochem. Physiol. BBiochem. Mol. Biol. 151 (2008) 1–9.

[6] S.E. Chen, J.P. McMurtry, R.L. Walzem, Overfeeding-induced ovariandysfunction in broiler breeder hens is associated with lipotoxicity, Poult. Sci.85 (2006) 70–81.

[7] A. Cryer, S.E. Riley, E.R. Williams, D.S. Robinson, Effects of fructose, sucrose andglucose feeding on plasma insulin concentrations and on adipose-tissueclearing-factor lipase activity in the rat, Biochem. J. 140 (1974) 561–563.

[8] J. Dupont, C. Dagou, M. Derouet, J. Simon, M. Taouis, Early steps of insulinreceptor signaling in chicken and rat: apparent refractoriness in chickenmuscle, Domest. Anim. Endocrinol. 26 (2004) 127–142.

[9] J. Dupont, S. Tesseraud, J. Simon, Insulin signaling in chicken liver and muscle,Gen. Comp. Endocrinol. 163 (2009) 52–57.

[10] M.R. Edwards, J.P. McMurtry, R. Vasilatos-Younken, Relative insensitivity ofavian skeletal muscle glycogen to nutritive status, Domest. Anim. Endocrinol.16 (1999) 239–247.

[11] C.M. Evock-Clover, S.M. Poch, M.P. Richards, C.M. Ashwell, J.P. McMurtry,Expression of an uncoupling protein gene homolog in chickens, Comp.Biochem. Physiol. A Mol. Integr. Physiol. 133 (2002) 345–358.

[12] C. Gàcs, The mechanism of hypoglycemia due to semistarvation in the rat, J.Nutr. 106 (1976) 1557–1561.

[13] J.R. Girard, G.S. Cuendet, E.B. Marliss, A. Kervran, M. Rieutort, R. Assan, Fuels,hormones, and liver metabolism at term and during the early postnatal periodin the rat, J. Clin. Invest. 52 (1973) 3190–3200.

hicken

sted Fed

ouzilly Beltsville Nouzilly Beltsville

15 ± 4b

= 8237 ± 5n = 5

241 ± 7b

n = 7233 ± 15n = 8

.60 ± 0.10= 8

0.70 ± 0.33n = 5

1.87 ± 0.42n = 7

2.17 ± 0.43n = 10

gh fat diet in one rat experiment. In each experiment, only data from control groupsype (i.e., heavy breeds or crosses). Rat experiments were chosen at random. In somelasma levels (for this, chickens differ). Also in rats, some plasma insulin levels wereies, young and adult individuals, mostly males, were involved. References according,23,25,29,30,39,41], fasted chickens at Nouzilly [2,3,8,17,28,31–33], fed chickens at

g following an overnight fast), fasted chickens at Beltsville: [11,24,27,34,36] and fed

a colorimetric reaction, avoiding interferences and leading to the minimal values.

Page 2: Plasma insulin levels are rather similar in chicken and rat

268 Viewpoint / General and Comparative Endocrinology 171 (2011) 267–268

[14] C. Karakash, B.E. Hustvedt, A. Lovo, Y. Le Marchand, B. Jeanrenaud,Consequences of ventromedial hypothalamic lesions on metabolism ofperfused rat liver, Am. J. Physiol. 232 (1977) E286–E293.

[15] A.I. Katz, A.H. Rubenstein, Metabolism of proinsulin, insulin, and C-peptide inthe rat, J. Clin. Invest. 52 (1973) 1113–1121.

[16] S.F. Kuku, J.B. Jaspan, D.S. Emmanouel, A.I. Katz, A.H. Rubenstein, Plasmaglucagon, insulin and glucose responses to intravenous arginine infusion in therat, Horm. Metab. Res. 10 (1978) 99–100.

[17] B. Leclercq, J. Simon, H. Karmann, Glucagon-insulin balance in genetically leanor fat chickens, Diabetes Metab. 14 (1988) 641–645.

[18] H.A. Mahmood, P.J. Wood, V. Marks, The effect of induced hyperglucagonaemiaon the Zucker fatty rat, Diabetologia 14 (1978) 405–412.

[19] T.R. Nardelli, R.A. Ribeiro, S.L. Balbo, E.C. Vanzela, E.M. Carneiro, A.C. Boschero,M.L. Bonfleur, Taurine prevents fat deposition and ameliorates plasma lipidprofile in monosodium glutamate-obese rats, Amino Acids, 2010 [Epub aheadof print].

[20] M. Newcombe, A.L. Cartwright, J.M. Harter-Dennis, J.P. McMurtry, The effect ofincreasing photoperiod and food restriction in sexed, broiler-type birds. II.Plasma thyroxine, triiodothyronine, insulin-like growth factor-I and insulin,Br. Poult. Sci. 33 (1992) 427–435.

[21] K. O’Dea, S. Koletsky, Effect of caloric restriction on basal insulin levels and thein vivo lipogenesis and glycogen synthesis from glucose in the Koletsky obeserat, Metabolism 26 (1977) 763–772.

[22] B. Portha, L. Picon, G. Rosselin, Chemical diabetes in the adult rat as thespontaneous evolution of neonatal diabetes, Diabetologia 17 (1979) 371–377.

[23] D.E. Potter, S. Ellis, Isoproterenol- and epinephrine-induced changes in bloodglucose and tissue glycogen levels in normal and diabetic rats: the influence ofalteration in endogenous insulin levels and state of nourishment, J. Pharmacol.Exp. Ther. 193 (1975) 576–584.

[24] M. Proszkowiec-Weglarz, M.P. Richards, B.D. Humphrey, R.W. Rosebrough, J.P.McMurtry, AMP-activated protein kinase and carbohydrate response elementbinding protein: a study of two potential regulatory factors in the hepaticlipogenic program of broiler chickens, Comp. Biochem. Physiol. B Biochem.Mol. Biol. 154 (2009) 68–79.

[25] G.M. Reaven, T.R. Risser, Y.D. Chen, E.P. Reaven, Characterization of a model ofdietary-induced hypertriglyceridemia in young, nonobese rats, J. Lipid Res. 20(1979) 371–378.

[26] N. Rideau, M. Derouet, J. Grimsby, J. Simon, Glucokinase activation inducespotent hypoglycemia without recruiting insulin and inhibits food intake inchicken, Gen. Comp. Endocrinol. 169 (2010) 276–283.

[27] R.W. Rosebrough, J.P. McMurtry, M.P. Richards, N.C. Steele, Effect of starvation-refeeding and an exogenous glucocorticoid on carbohydrate metabolism inchick liver, Poult. Sci. 63 (1984) 2444–2449.

[28] A. Saadoun, J. Simon, J. Williams, B. Leclercq, Levels of insulin, corticosterone,T3, T4 and insulin sensitivity in fat and lean chickens, Diabetes Metab. 14(1988) 97–103.

[29] C.D. Saudek, M. Finkowski, R.H. Knopp, Plasma glucagon and insulin in ratpregnancy. Roles in glucose homeostasis, J. Clin. Invest. 55 (1975) 180–187.

[30] J. Schwartz, Enhanced sensitivity to insulin in rats treated with antibodies torat growth hormone, Endocrinology 107 (1980) 877–883.

[31] J. Simon, The effect of injected vanadate on fasted growing chickens, Arch.Geflügelk 52 (1988) 75–79.

[32] J. Simon, B. Chevalier, M. Derouet, B. Leclercq, Normal number and kinaseactivity of insulin receptors in liver of genetically fat chickens, J. Nutr. 121(1991) 379–385.

[33] J. Simon, B. Leclercq, Longitudinal study of adiposity in chickens selected forhigh or low abdominal fat content: further evidence of a glucose-insulinimbalance in the fat line, J. Nutr. 112 (1982) 1961–1973.

[34] J. Simon, R.W. Rosebrough, J.P. McMurtry, N.C. Steele, J. Roth, M. Adamo, D.LeRoith, Fasting and refeeding alter the insulin receptor tyrosine kinase inchicken liver but fail to affect brain insulin receptors, J. Biol. Chem. 261 (1986)17081–17088.

[35] J. Simon, G. Rosselin, Effect of fasting, glucose, amino acids and food intake onin vivo insulin release in the chicken, Horm. Metab. Res. 10 (1978)93–98.

[36] N.A. Sinsigalli, J.P. McMurtry, J.A. Cherry, P.B. Siegel, Glucose tolerance, plasmainsulin and immunoreactive glucagon in chickens selected for high and lowbody weight, J. Nutr. 117 (1987) 941–947.

[37] J.H. Strubbe, P.R. Bouman, Plasma insulin patterns in the unanesthetized ratduring intracardial infusion and spontaneous ingestion of graded loads ofglucose, Metabolism 27 (1978) 341–351.

[38] F.M. Tomas, R.A. Pym, J.P. McMurtry, G.L. Francis, Insulin-like growth factor(IGF)-I but not IGF-II promotes lean growth and feed efficiency in broilerchickens, Gen. Comp. Endocrinol. 110 (1998) 262–275.

[39] J.L. Trevaskis, C. Lei, J.E. Koda, C. Weyer, D.G. Parkes, J.D. Roth, Interaction ofleptin and amylin in the long-term maintenance of weight loss in diet-inducedobese rats, Obesity (Silver Spring) 18 (2010) 21–26.

[40] R. Vasilatos-Younken, Y. Zhou, X. Wang, J.P. McMurtry, R.W. Rosebrough, E.Decuypere, N. Buys, V.M. Darras, S. Van Der Geyten, F. Tomas, Altered chickenthyroid hormone metabolism with chronic GH enhancement in vivo:consequences for skeletal muscle growth, J. Endocrinol. 166 (2000) 609–620.

[41] C.W. Wilkinson, J. Shinsako, M.F. Dallman, Daily rhythms in adrenalresponsiveness to adrenocorticotropin are determined primarily by the timeof feeding in the rat, Endocrinology 104 (1979) 350–359.

Jean SimonNicole Rideau

INRA-Recherches Avicoles, 37380 Nouzilly, FranceFax: +33 (0)2 47 42 77 78

E-mail address: [email protected] (J. Simon)

Mohammed TaouisUniversité Paris-Sud 11, 91405 Orsay, France

Joëlle DupontINRA-PRC, 37380 Nouzilly, France

Available online 21 March 2011