Standard operating procedures for describing and performing metabolic tests of glucose homeostasis in mice

DMM Disease Models and Mechanisms

Volumn 3, Issue 9-10, 2010, Pages 525-534

  Ayala, Julio E ^a,b   Samuel, Varman T ^c   Morton, Gregory J ^d   Obici, Silvana ^e   Croniger, Colleen M ^f   Shulman, Gerald I ^c   Wasserman, David H ^a   McGuinness, Owen P ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b BURNHAM INSTITUTE   (United States)

^c Yale NIH Mouse Metabolic Phenotyping Center   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY OF CINCINNATI   (United States)

^f CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C PEPTIDE; CARBOHYDRATE; CATECHOLAMINE; FAT; GLUCOSE; GLYCOGEN; HEMOGLOBIN A1C; INCRETIN; INSULIN; NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; PROTEIN;

ADIPOSE TISSUE; BLOOD SAMPLING; BLOOD VOLUME; BODY COMPOSITION; BODY WEIGHT; CAROTID ARTERY; CIRCADIAN RHYTHM; DIET RESTRICTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMORAL VEIN; FLUOROMETRY; GENOTYPE; GLUCONEOGENESIS; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; HEMATOCRIT; HYPERGLYCEMIA; HYPERINSULINEMIA; HYPOGLYCEMIA; INSULIN RELEASE; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; JUGULAR VEIN; LEAN BODY WEIGHT; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RADIOIMMUNOASSAY; REVIEW; SCREENING TEST; SEX DIFFERENCE; SKELETAL MUSCLE; SPECTROPHOTOMETRY; STOMACH EMPTYING; WILD TYPE;

ANIMALS; BLOOD GLUCOSE; CATHETERIZATION; DIAGNOSTIC TECHNIQUES, ENDOCRINE; FASTING; GLUCOSE; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; HYPERGLYCEMIA; INSULIN; MICE; MODELS, ANIMAL; PHENOTYPE;

MUS;

EID: 77956534963     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.006239     Document Type: Review

References (62)

1. Andrikopoulos, S., Blair, A. R., Deluca, N., Fam, B. C. and Proietto, J. (2008). Evaluating the glucose tolerance test in mice. Am. J. Physiol. Endocrinol. Metab. 295, E1323-E1332.
2. Ayala, J. E., Bracy, D. P., McGuinness, O. P. and Wasserman, D. H. (2006). Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 55, 390-397.
3. Ayala, J. E., Bracy, D. P., Hansotia, T., Flock, G., Seino, Y., Wasserman, D. H. and Drucker, D. J. (2008). Insulin action in the double incretin receptor knockout mouse. Diabetes 57, 288-297.
4. Bailey, C. J. and Flatt, P. R. (1980). Insulin and glucagon during pentobarbitone anaesthesia. Diabetes Metab. 6, 91-95.
5. Bailey, C. J. and Flatt, P. R. (1982). Hormonal control of glucose homeostasis during development and ageing in mice. Metabolism. 31, 238-246.
6. Balcombe, J. P., Barnard, N. D. and Sandusky, C. (2004). Laboratory routines cause animal stress. Contemp. Top. Lab. Anim. Sci. 43, 42-51.
7. Berglund, E. D., Li, C. Y., Poffenberger, G., Ayala, J. E., Fueger, P. T., Willis, S. E., Jewell, M. M., Powers, A. C. and Wasserman, D. H. (2008). Glucose metabolism in vivo in four commonly used inbred mouse strains. Diabetes 57, 1790-1799.
8. Biddinger, S. B., Almind, K., Miyazaki, M., Kokkotou, E., Ntambi, J. M. and Kahn, C. R. (2005). Effects of diet and genetic background on sterol regulatory element-binding protein-1c, stearoyl-CoA desaturase 1, and the development of the metabolic syndrome. Diabetes 54, 1314-1323.
9. Brown, E. T., Umino, Y., Solessio, E., Loi, T., Quinn, R. and Barlow, R. (2004). Anesthesia affects mouse ERG and blood glucose. Invest. Ophthalmol. Vis. Sci. 45, B742-B745.
10. Brown, E. T., Umino, Y., Loi, T., Solessio, E. and Barlow, R. (2005). Anesthesia can cause sustained hyperglycemia in C57/BL6J mice. Vis. Neurosci. 22, 615-618. (Pubitemid 43237756)
11. Burcelin, R., Crivelli, V., Dacosta, A., Roy-Tirelli, A. and Thorens, B. (2002). Heterogeneous metabolic adaptation of C57BL/6J mice to high-fat diet. Am. J. Physiol. Endocrinol. Metab. 282, E834-E842.
12. Burgess, S. C., Jeffrey, F. M., Storey, C., Milde, A., Hausler, N., Merritt, M. E., Mulder, H., Holm, C., Sherry, A. D. and Malloy, C. R. (2005). Effect of murine strain on metabolic pathways of glucose production after brief or prolonged fasting. Am. J. Physiol. Endocrinol. Metab. 289, E53-E61.
13. Carvalho, C. R., Brenelli, S. L., Silva, A. C., Nunes, A. L., Velloso, L. A. and Saad, M. J. (1996). Effect of aging on insulin receptor, insulin receptor substrate-1, and phosphatidylinositol 3-kinase in liver and muscle of rats. Endocrinology 137, 151-159.
14. Coleman, D. L. (1992). The influence of genetic background on the expression of mutations at the diabetes (db) locus in the mouse. VI: Hepatic malic enzyme activity is associated with diabetes severity. Metabolism 41, 1134-1136.
15. Collins, S., Martin, T. L., Surwit, R. S. and Robidoux, J. (2004). Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics. Physiol. Behav. 81, 243-248. (Pubitemid 38670090)
16. Colombo, C., Haluzik, M., Cutson, J. J., Dietz, K. R., Marcus-Samuels, B., Vinson, C., Gavrilova, O. and Reitman, M. L. (2003). Opposite effects of background genotype on muscle and liver insulin sensitivity of lipoatrophic mice. Role of triglyceride clearance. J. Biol. Chem. 278, 3992-3999.
17. Cresto, J. C., Lavine, R. L., Buchly, M. L., Penhos, J. C., Bhathena, S. J. and Recant, L. (1977). Half life of injected 125I-insulin in control and ob/ob mice. Acta Physiol. Lat. Am. 27, 7-15.
18. Del Prato, S., Marchetti, P. and Bonadonna, R. C. (2002). Phasic insulin release and metabolic regulation in type 2 diabetes. Diabetes. 51, S109-S116.
19. Fernandez, A. M., Kim, J. K., Yakar, S., Dupont, J., Hernandez-Sanchez, C., Castle, A. L., Filmore, J., Shulman, G. I. and Le Roith, D. (2001). Functional inactivation of the IGF-I and insulin receptors in skeletal muscle causes type 2 diabetes. Genes. Dev. 15, 1926-1934. (Pubitemid 32738622)
20. Ferrannini, E. and Cobelli, C. (1987a). The kinetics of insulin in man. I. General aspects. Diabetes Metab. Rev. 3, 335-363. (Pubitemid 17050762)
21. Ferrannini, E. and Cobelli, C. (1987b). The kinetics of insulin in man. II. Role of the liver. Diabetes Metab. Rev. 3, 365-397. (Pubitemid 17050763)
22. Finegood, D. T., Bergman, R. N. and 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.
23. Finegood, D. T., Bergman, R. N. and Vranic, M. (1988). Modeling error and apparent isotope discrimination confound estimation of endogenous glucose production during euglycemic glucose clamps. Diabetes 37, 1025-1034.
24. Freeman, H. C., Hugill, A., Dear, N. T., Ashcroft, F. M. and Cox, R. D. (2006). Deletion of nicotinamide nucleotide transhydrogenase: a new quantitive trait locus accounting for glucose intolerance in C57BL/6J mice. Diabetes 55, 2153-2156.
25. Geiser, F. (2004). Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66, 239-274.
26. Goren, H. J., Kulkarni, R. N. and Kahn, C. R. (2004). Glucose homeostasis and tissue transcript content of insulin signaling intermediates in four inbred strains of mice: C57BL/6, C57BLKS/6, DBA/2, and 129X1. Endocrinology 145, 3307-3323.
27. Grundleger, M. L., Godbole, V. Y. and Thenen, S. W. (1980). Age-dependent development of insulin resistance of soleus muscle in genetically obese (ob/ob) mice. Am. J. Physiol. 239, E363-E371.
28. Halseth, A. E., Bracy, D. P. and Wasserman, D. H. (1999). Overexpression of hexokinase II increases insulinand exercise-stimulated muscle glucose uptake in vivo. Am. J. Physiol. 276, E70-E77.
29. Haluzik, M., Dietz, K. R., Kim, J. K., Marcus-Samuels, B., Shulman, G. I., Gavrilova, O. and Reitman, M. L. (2002). Adrenalectomy improves diabetes in A-ZIP/F-1 lipoatrophic mice by increasing both liver and muscle insulin sensitivity. Diabetes 51, 2113-2118.
30. Haluzik, M., Colombo, C., Gavrilova, O., Chua, S., Wolf, N., Chen, M., Stannard, B., Dietz, K. R., Le Roith, D. and Reitman, M. L. (2004a). Genetic background (C57BL/6J versus FVB/N) strongly influences the severity of diabetes and insulin resistance in ob/ob mice. Endocrinology 145, 3258-3264.
31. Haluzik, M., Gavrilova, O. and LeRoith, D. (2004b). Peroxisome proliferator-activated receptor-alpha deficiency does not alter insulin sensitivity in mice maintained on regular or high-fat diet: hyperinsulinemic- euglycemic clamp studies. Endocrinology 145, 1662-1667. (Pubitemid 38402373)
32. Han, B. G., Hao, C. M., Tchekneva, E. E., Wang, Y. Y., Lee, C. A., Ebrahim, B., Harris, R. C., Kern, T. S., Wasserman, D. H., Breyer, M. D. et al. (2008). Markers of glycemic control in the mouse: comparisons of 6-hand overnight-fasted blood glucoses to Hb A1c. Am. J. Physiol. Endocrinol. Metab. 295, E981-E986.
33. Heijboer, A. C., Donga, E., Voshol, P. J., Dang, Z. C., Havekes, L. M., Romijn, J. A. and Corssmit, E. P. (2005). Sixteen hours of fasting differentially affects hepatic and muscle insulin sensitivity in mice. J. Lipid Res. 46, 582-588. (Pubitemid 43109794)
34. Heikkinen, S., Argmann, C. A., Champy, M. F. and Auwerx, J. (2007). Evaluation of glucose homeostasis. Curr. Protoc. Mol. Biol. Chapter 29, Unit 29B 23.
35. Jacobson, L., Ansari, T. and McGuinness, O. P. (2006a). Counterregulatory deficits occur within 24 h of a single hypoglycemic episode in conscious, unrestrained, chronically cannulated mice. Am. J. Physiol. Endocrinol. Metab. 290, E678-E684.
36. Jacobson, L., Ansari, T., Potts, J. and McGuinness, O. P. (2006b). Glucocorticoid-deficient corticotropin-releasing hormone knockout mice maintain glucose requirements but not autonomic responses during repeated hypoglycemia. Am. J. Physiol. Endocrinol. Metab. 291, E15-E22. (Pubitemid 44043074)
37. Kim, H., Haluzik, M., Asghar, Z., Yau, D., Joseph, J. W., Fernandez, A. M., Reitman, M. L., Yakar, S., Stannard, B., Heron-Milhavet, L. et al. (2003). Peroxisome proliferator-activated receptor-alpha agonist treatment in a transgenic model of type 2 diabetes reverses the lipotoxic state and improves glucose homeostasis. Diabetes 52, 1770-1778.
38. Kim, H. J., Higashimori, T., Park, S. Y., Choi, H., Dong, J., Kim, Y. J., Noh, H. L., Cho, Y. R., Cline, G., Kim, Y. B. et al. (2004). Differential effects of interleukin-6 and -10 on skeletal muscle and liver insulin action in vivo. Diabetes 53, 1060-1067. (Pubitemid 38436619)
39. Kim, J. K., Zisman, A., Fillmore, J. J., Peroni, O. D., Kotani, K., Perret, P., Zong, H., Dong, J., Kahn, C. R., Kahn, B. B. et al. (2001). Glucose toxicity and the development of diabetes in mice with muscle-specific inactivation of GLUT4. J. Clin. Invest. 108, 153-160. (Pubitemid 32634932)
40. Kim, J. K., Fillmore, J. J., Gavrilova, O., Chao, L., Higashimori, T., Choi, H., Kim, H. J., Yu, C., Chen, Y., Qu, X. et al. (2003). Differential effects of rosiglitazone on skeletal muscle and liver insulin resistance in AZIP/ F-1 fatless mice. Diabetes 52, 1311-1318. (Pubitemid 36666182)
41. Kim, J. K., Fillmore, J. J., Sunshine, M. J., Albrecht, B., Higashimori, T., Kim, D. W., Liu, Z. X., Soos, T. J., Cline, G. W., O'Brien, W. R. et al. (2004). PKC-theta knockout mice are protected from fat-induced insulin resistance. J. Clin. Invest. 114, 823-827. (Pubitemid 39578741)
42. Kohsaka, A. and Bass, J. (2007). A sense of time: how molecular clocks organize metabolism. Trends Endocrinol. Metab. 18, 4-11. (Pubitemid 44960013)
43. Kraegen, E. W., James, D. E., Jenkins, A. B. and Chisholm, D. J. (1985). Dose-response curves for in vivo insulin sensitivity in individual tissues in rats. Am. J. Physiol. 248, E353-E362.
44. Kulkarni, R. N., Almind, K., Goren, H. J., Winnay, J. N., Ueki, K., Okada, T. and Kahn, C. R. (2003). Impact of genetic background on development of hyperinsulinemia and diabetes in insulin receptor/insulin receptor substrate-1 double heterozygous mice. Diabetes 52, 1528-1534.
45. Lodhi, I. J. and Semenkovich, C. F. (2009). Why we should put clothes on mice. Cell Metab. 9, 111-112.
46. Luzi, L. and DeFronzo, R. A. (1989). Effect of loss of first-phase insulin secretion on hepatic glucose production and tissue glucose disposal in humans. Am. J. Physiol. 257, E241-E246.
47. Macotela, Y., Boucher, J., Tran, T. T. and Kahn, C. R. (2009). Gender and depot differences in adipocyte insulin sensitivity and glucose metabolism. Diabetes 58, 803-812.
48. McGuinness, O. P., Ayala, J. E., Laughlin, M. R. and Wasserman, D. H. (2009). NIH experiment in centralized mouse phenotyping: the Vanderbilt experience and recommendations for evaluating glucose homeostasis in the mouse. Am. J. Physiol. Endocrinol. Metab. 297, E849-E855.
49. Mekada, K., Abe, K., Murakami, A., Nakamura, S., Nakata, H., Moriwaki, K., Obata, Y. and Yoshiki, A. (2009). Genetic differences among C57BL/6 substrains. Exp. Anim. 58, 141-149.
50. Muniyappa, R., Lee, S., Chen, H. and Quon, M. J. (2008). Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage. Am. J. Physiol. Endocrinol. Metab. 294, E15-E26.
51. Pomplun, D., Mohlig, M., Spranger, J., Pfeiffer, A. F. and Ristow, M. (2004). Elevation of blood glucose following anaesthetic treatment in C57BL/6 mice. Horm. Metab. Res. 36, 67-69. (Pubitemid 38283197)
52. Ren, J. M., Marshall, B. A., Mueckler, M. M., McCaleb, M., Amatruda, J. M. and Shulman, G. I. (1995). Overexpression of Glut4 protein in muscle increases basal and insulin-stimulated whole body glucose disposal in conscious mice. J. Clin. Invest. 95, 429-432.
53. Rudic, R. D., McNamara, P., Curtis, A. M., Boston, R. C., Panda, S., Hogenesch, J. B. and Fitzgerald, G. A. (2004). BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol. 2, e377.
54. Shi, H., Strader, A. D., Sorrell, J. E., Chambers, J. B., Woods, S. C. and Seeley, R. J. (2008). Sexually different actions of leptin in proopiomelanocortin neurons to regulate glucose homeostasis. Am. J. Physiol. Endocrinol. Metab. 294, E630-E639. (Pubitemid 351355235)
55. Spurlin, B. A., Thomas, R. M., Nevins, A. K., Kim, H. J., Kim, Y. J., Noh, H. L., Shulman, G. I., Kim, J. K. and Thurmond, D. C. (2003). Insulin resistance in tetracycline-repressible Munc18c transgenic mice. Diabetes 52, 1910-1917.
56. Surwit, R. S., Kuhn, C. M., Cochrane, C., McCubbin, J. A. and Feinglos, M. N. (1988). Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37, 1163-1167.
57. Swoap, S. J., Gutilla, M. J., Liles, L. C., Smith, R. O. and Weinshenker, D. (2006). The full expression of fasting-induced torpor requires beta 3-adrenergic receptor signaling. J. Neurosci. 26, 241-245.
58. Tanaka, K., Kawano, T., Tomino, T., Kawano, H., Okada, T., Oshita, S., Takahashi, A. and Nakaya, Y. (2009). Mechanisms of impaired glucose tolerance and insulin secretion during isoflurane anesthesia. Anesthesiology 111, 1044-1051.
59. Tiraby, C., Tavernier, G., Capel, F., Mairal, A., Crampes, F., Rami, J., Pujol, C., Boutin, J. A. and Langin, D. (2007). Resistance to high-fat-diet-induced obesity and sexual dimorphism in the metabolic responses of transgenic mice with moderate uncoupling protein 3 overexpression in glycolytic skeletal muscles. Diabetologia 50, 2190-2199. (Pubitemid 47373849)
60. Turek, F. W., Joshu, C., Kohsaka, A., Lin, E., Ivanova, G., McDearmon, E., Laposky, A., Losee-Olson, S., Easton, A., Jensen, D. R. et al. (2005). Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308, 1043-1045. (Pubitemid 40664419)
61. Wasserman, D. H., Ayala, J. E. and McGuinness, O. P. (2009). Lost in translation. Diabetes 58, 1947-1950.
62. Zabolotny, J. M., Haj, F. G., Kim, Y. B., Kim, H. J., Shulman, G. I., Kim, J. K., Neel, B. G. and Kahn, B. B. (2004). Transgenic overexpression of protein-tyrosine phosphatase 1B in muscle causes insulin resistance, but overexpression with leukocyte antigen-related phosphatase does not additively impair insulin action. J. Biol. Chem. 279, 24844-24851.