Analysis of energy expenditure in diet-induced obese rats

Frontiers in Bioscience - Landmark

Volumn 19, Issue 6, 2014, Pages 967-985

  Assaad, Houssein ^a   Yao, Kang ^a   Tekwe, Carmen D ^a   Feng, Shuo ^a   Bazer, Fuller W ^a   Zhou, Lan ^a   Carroll, Raymond J ^a   Meininger, Cynthia J ^a   Wu, Guoyao ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Energy expenditure; Indirect calorimetry; Obesity; Review; Statistical analysis

Indexed keywords

ADVERSE EFFECTS; ANIMAL; BODY WEIGHT; ENERGY METABOLISM; FEMALE; LIPID DIET; MALE; OBESITY; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; WISTAR RAT;

ANIMALS; BODY WEIGHT; DIET, HIGH-FAT; ENERGY METABOLISM; FEMALE; MALE; OBESITY; OXYGEN CONSUMPTION; RATS, SPRAGUE-DAWLEY; RATS, WISTAR;

EID: 84904346780     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4261     Document Type: Article

References (107)

1. Speakman JR: Evolutionary perspectives on the obesity epidemic: adaptive, maladaptive, and neutral viewpoints. Annu Rev Nutr, 33, 289-317 (2013)
2. Hill JO and Peters JC: Environmental contributions to the obesity epidemic. Science, 280, 1371-1374 (1998)
3. McKnight JR, Satterfield MC, Li XL, Gao HJ, Wang JJ, Li DF and Wu G: Obesity in pregnancy: problems and potential solutions. Front Biosci, E3, 442-452 (2011)
4. Aballay LR, Eynard AR, Díaz Mdel P, Navarro A and Muñoz SE: Overweight and obesity: a review of their relationship to metabolic syndrome, cardiovascular disease, and cancer in South America. Nutr Rev, 71, 168-79 (2013)
5. Vucenik I and Stains JP: Obesity and cancer risk: evidence, mechanisms, and recommendations. Ann N Y Acad Sci, 1271, 37-43 (2012)
6. Jobgen W, Meininger CJ, Jobgen SC, Li P, Lee MJ, Smith SB, Spencer TE, Fried SK and Wu G: Dietary L-arginine supplementation reduces white fat gain and enhances skeletal muscle and brown fat masses in diet-induced obese rats. J Nutr, 139, 230-237 (2009)
7. Clemmensen C, Madsen AN, Smajilovic S, Holst B and Brauner-Osborne H: L-Arginine improves multiple physiological parameters in mice exposed to diet-induced metabolic disturbances. Amino Acids, 43, 1265-1275 (2012)
8. Bujnowski D, Xun P, Daviglus ML, Van Horn L, He K and Stamler J: Longitudinal association between animal and vegetable protein intake and obesity among men in the United States: the Chicago Western Electric Study. J Am Diet Assoc, 111, 1150-1155 (2011)
9. Murtaugh MA, Herrick JS, Sweeney C, Baumgartner KB, Guiliano AR, Byers T and Slattery ML: Diet composition and risk of overweight and obesity in women living in the southwestern United States. J Am Diet Assoc, 107, 1311-1321 (2007)
10. Lin Y, Bolca S, Vandevijvere S, De Vriese S, Mouratidou T, De Neve M, Polet A, Van Oyen H, Van Camp J, De Backer G, De Henauw S and Huybrechts I: Plant and animal protein intake and its association with overweight and obesity among the Belgian population. Br J Nutr, 105:1106-1116 (2011)
11. Nall JL, Wu G, Kim KH, Choi CW and Smith SB: Dietary supplementation of L-arginine and conjugated linoleic acid reduces retroperitoneal fat mass and increases lean body mass in rats. J Nutr, 139, 1279-1285 (2009)
12. Jobgen WJ, Meininger CJ, Jobgen SC, Li P, Lee MJ, Smith SB, Spencer TE, Fried SK and Wu G: Dietary L-arginine supplementation reduces white-fat gain and enhances skeletal muscle and brown fat masses in diet-induced obese rats. J Nutr, 139, 230-237 (2009)
13. Jobgen W, Fu WJ, Gao H, Li P, Meininger CJ, Smith SB, Spencer TE and Wu G: High fat feeding and dietary L-arginine supplementation differentially regulate gene expression in rat white adipose tissue. Amino Acids, 37, 187-198 (2009)
14. Fu WJ, Haynes TE, Kohli R, Hu J, Shi W, Spencer TE, Carroll RJ, Meininger CJ and Wu G: Dietary L-arginine supplementation reduces fat mass in Zucker diabetic fatty rats. J Nutr, 135, 714-721 (2005)
15. Wu G, Collins JK, Perkins-Veazie P, Siddiq M, Dolan KD, Kelly KA, Heaps CL and Meininger CJ: Dietary supplementation with watermelon pomace juice enhances arginine availability and ameliorates the metabolic syndrome in Zucker diabetic fatty rats. J Nutr, 137, 2680-2685 (2007)
16. Bazer FW, Kim J, Song G, Ka H, Tekwe CD and Wu G: Select nutrients, progesterone, and interferon tau affect conceptus metabolism and development. Ann N Y Acad Sci, 1271, 88-96 (2012)
17. Tan BE, Li XG, Kong XF, Huang RL, Ruan Z, Yao K, Deng ZY, Xie MY, Shinzato I, Yin YL and Wu G: Dietary L-arginine supplementation enhances the immune status in early-weaned piglets. Amino Acids, 37, 323-331 (2009)
18. Tan BE, Yin YL, Liu ZQ, Tang WJ, Xu HJ, Kong XF, Li XG, Yao K, Gu WT, Smith SB and Wu G: Dietary L-arginine supplementation differentially regulates expression of lipid-metabolic genes in porcine adipose tissue and skeletal muscle. J Nutr Biochem, 22, 441-445 (2011)
19. Lucotti P, Setola E, Monti LD, Galluccio E, Costa S, Sandoli EP, Fermo I, Rabaiotti G, Gatti R and Piatti P: Beneficial effects of a long-term oral L-arginine treatment added to a hypocaloric diet and exercise training program in obese, insulin-resistant type 2 diabetic patients. Am J Physiol Endocrinol Metab, 291:E906-912 (2006)
20. McKnight JR, Satterfield MC, Jobgen WS, Smith SB, Spencer TE, Meininger CJ, McNeal CJ and Wu G: Beneficial effects of L-arginine on reducing obesity: Potential mechanisms and important implications for human health. Amino Acids 39:349-357 (2010)
21. Tan BE, Li XG, Yin YL, Wu ZL, Liu C, Tekwe CD and Wu G: Regulatory roles for L-arginine in reducing white adipose tissue. Front Biosci, 17, 2237-2246 (2012)
22. Wu ZL, Satterfield MC, Bazer FW and Wu G: Regulation of brown adipose tissue development and white fat reduction by L-arginine. Curr Opin Clin Nutr Metab Care 15, 529-538 (2012)
23. Dai ZL, Wu ZL, Yang Y, Wang JJ, Satterfield MC, Meininger CJ, Bazer FW and Wu G: Nitric oxide and energy metabolism in mammals. Biofactors, 39, 383-391 (2013)
24. Li XL, Rezaei R, Li P and Wu G: Composition of amino acids in feed ingredients for animal diets. Amino Acids, 40, 1159-1168 (2011)
25. San Gabriel A and Uneyama H: Amino acid sensing in the gastrointestinal tract. Amino Acids, 45, 451-461 (2013)
26. San Gabriel A, Nakamura E, Uneyama H and Torii K (2009) Taste, visceral information and exocrine reflexes with glutamate through umami receptors. J Med Invest 56 (Suppl), 209-217 (2009)
27. Smriga M, Murakami H, Mori M and Torii K: Use of thermal photography to explore the age-dependent effect of monosodium glutamate, NaCl and glucose on brown adipose tissue thermogenesis. Physiol Behav, 71, 403-407 (2000)
28. Kondoh T and Torii K: MSG intake suppresses weight gain, fat deposition, and plasma leptin levels in male Sprague-Dawley rats. Physiol Behav, 95, 135-144 (2008)
29. Rezaei R, Knabe DA, Tekwe CD, Dahanayaka S, Ficken MD, Fielder SE, Eide SJ, Lovering SL and Wu G: Dietary supplementation with monosodium glutamate is safe and improves growth performance in postweaning pigs. Amino Acids, 44, 911-923 (2013)
30. Heinritz SN, Mosenthin R and Weiss E: Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutr Res Rev, 26, 191-209 (2013)
31. Freudenberg A, Petzke KJ and Klaus S: Dietary L-leucine and L-alanine supplementation have similar acute effects in the prevention of high-fat diet-induced obesity. Amino Acids, 44, 519-528 (2013)
32. Segal-Lieberman G and Rosenthal T: Animal models in obesity and hypertension. Curr Hypertens Rep, 15, 190-195 (2013)
33. Satterfield MC, Dunlap KA, Keisler DH, Bazer FW and Wu G: Arginine nutrition and fetal brown adipose tissue development in diet-induced obese sheep. Amino Acids, 43, 1593-1603 (2012)
34. Tekwe CD, Lei J, Yao K, Rezaei R, Li XL, Dahanayaka S, Carroll RJ, Meininger CJ, Bazer FW and Wu G: Oral administration of interferon tau enhances oxidation of energy substrates and reduces adiposity in Zucker diabetic fatty rats. Biofactors, 39, 552-563 (2013)
35. Pinheiro J, Bates D, DebRoy S, Sarkar D and the R Development Core Team: nlme Linear and Nonlinear Mixed Effects Models. R package version 3.1-108 (2013)
36. Pinheiro J and Bates D: Mixed effect models in S and S-Plus. New York: Springer-Verlag (2000)
37. Ramsay JO, Wickham H, Graves S and Hooker G: fda Functional Data Analysis. R package version 2.3.2. http://CRAN.R-project.org/package=fda (2012)
38. R Core Team: R A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/ (2012)
39. Blundell JE, Lawton CL, Cotton JR and Macdiarmid JI: Control of human appetite: implications for the intake of dietary fat. Annu Rev Nutr, 16, 285-319 (1996)
40. Duca FA, Sakar Y and Covasa M: The modulatory role of high fat feeding on gastrointestinal signals in obesity. J Nutr Biochem, 24:1663-1677 (2013)
41. Gallo RV, Babu GN, Bona-Gallo A, Devorshak-Harvey E, Leipheimer RE and Marco J: Regulation of pulsatile luteinizing hormone release during the estrous cycle and pregnancy in the rat. Adv Exp Med Biol, 219, 109-130 (1987)
42. Guberman C, Jellyman JK, Han G, Ross MG and Desai M: Maternal high-fat diet programs rat offspring hypertension and activates the adipose renin-angiotensin system. Am J Obstet Gynecol, 209, 262.e1-8 (2013)
43. Solomon S: Developmental changes in nephron number, proximal tubular length and superficial nephron glomerular filtration rate of rats. J Physiol, 272, 573-589 (1977)
44. Fuzik J, Gellért L, Oláh G, Herédi J, Kocsis K, Knapp L, Nagy D, Kincses ZT, Kis Z, Farkas T and Toldi J: Fundamental interstrain differences in cortical activity between Wistar and Sprague-Dawley rats during global ischemia. Neuroscience, 228, 371-381 (2013)
45. Kobayashi K, Ogasawara R, Tsutaki A, Lee K, Ochi E and Nakazato K: Genetic strain-dependent protein metabolism and muscle hypertrophy under chronic isometric training in rat gastrocnemius muscle. Physiol Res, 61, 527-535 (2012)
46. Sakai N, Saito K, Sakamoto KQ, Ishizuka M and Fujita S: Genetic basis of inter- and intrastrain differences in diazepam p-hydroxylation in rats. Drug Metab Dispos, 37, 268-271 (2009)
47. Berdanier CD and Thomson AR: Comparative studies on mitochondrial respiration in four strains of rats (Rattus norvegicus). Comp Biochem Physiol B, 85, 531-535 (1986)
48. Pérez de Heredia F, Garaulet M, Portillo MP and Zamora S: Resistance to dietary obesity in rats given different high-energy diets. Int J Vitam Nutr Res, 76, 271-279 (2006)
49. Langer M, Brandt C and Löscher W: Marked strain and substrain differences in induction of status epilepticus and subsequent development of neurodegeneration, epilepsy, and behavioral alterations in rats. Epilepsy Res, 96, 207-224 (2011)
50. MacKenzie WF and Garner FM: Comparison of neoplasms in six sources of rats. J Natl Cancer Inst, 50, 1243-1257 (1973)
51. Miller FP, Cox RH Jr and Maickel RP: Intrastrain differences in serotonin and norepinephrine in discrete areas of rat brain. Science, 162, 463-464 (1968)
52. Valenti VE, Imaizumi C, de Abreu LC, Colombari E, Sato MA and Ferreira C: Intra-strain variations of baroreflex sensitivity in young Wistar-Kyoto rats. Clin Invest Med, 32, E251 (2009)
53. Portelli J, Aourz N, De Bundel D, Meurs A, Smolders I, Michotte Y and Clinckers R: Intrastrain differences in seizure susceptibility, pharmacological response and basal neurochemistry of Wistar rats. Epilepsy Res, 87, 234-246 (2009)
54. Oliff HS, Coyle P and Weber E: Rat strain and vendor differences in collateral anastomoses. J Cereb Blood Flow Metab, 17, 571-576 (1997)
55. Lauterio TJ, Bond JP and Ulman EA: Development and characterization of a purified diet to identify obesity-susceptible and resistant rat populations. J Nutr, 124, 2172-2178 (1994)
56. Farley C, Cook JA, Spar BD, Austin TM and Kowalski TJ: Meal pattern analysis of diet-induced obesity in susceptible and resistant rats. Obes Res, 11, 845-851 (2003)
57. Chang S, Graham B, Yakubu F, Lin D, Peters JC and Hill JO: Metabolic differences between obesity-prone and obesity-resistant rats. Am J Physiol, 259, R1103-R1110 (1990)
58. Arch JR, Hislop D, Wang SJ and Speakman JR: Some mathematical and technical issues in the measurement and interpretation of open-circuit indirect calorimetry in small animals. Int J Obes (Lond), 30, 1322-1331 (2006)
59. Even PC and Nadkarni NA: Indirect calorimetry in laboratory mice and rats: principles, practical considerations, interpretation and perspectives. Am J Physiol Regul Integr Comp Physiol, 303, R459-476 (2012)
60. Kleiber M: The Fire of Life. R.E. Krieger Publishing Company, New York (1975)
61. Wu G: Amino Acids: Biochemistry and Nutrition, CRC Press, Boca Raton (2013)
62. Brouwer E: Report of sub-committee on constants and factors. Energy metabolism. London, UK. Academic Press, pp. 441-443 (1965)
63. Rolfe DF and Brown GC: Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev, 77, 731-758 (1997)
64. Jungas RL, Halperin ML and Brosnan JT: Quantitative analysis of amino acid oxidation and related gluconeogenesis in humans. Physiol Rev, 72, 419-448 (1992)
65. Tamura M, Hazeki O, Nioka S and Chance B: In vivo study of tissue oxygen metabolism using optical and nuclear magnetic resonance spectroscopies. Annu Rev Physiol, 51, 813-834 (1989)
66. Ba ZF, Wang P, Koo DJ, Cioffi WG, Bland KI and Chaudry IH: Alterations in tissue oxygen consumption and extraction after trauma and hemorrhagic shock. Crit Care Med, 28, 2837-2842 (2000)
67. Takeda S, Sato N and Tomaru T: Haemodynamic and splanchnic organ blood flow responses during sevoflurane-induced hypotension in dogs. Eur J. Anaesthesiology 19, 442-446 (2002)
68. Mongan PD, Moon-Massat PF, Rentko V, Mihok S, Dragovich A, Sharma P: Regional blood flow after serial normovolemic exchange transfusion with HBOC-201 (Hemopure) in anesthetized swine. J Trauma, 67, 51-60
69. Weiss HR: Regional oxygen consumption and supply in heart: effect of methoxamine-induced pressure rise. Am J Physiol, 241, H370-375 (1981)
70. 2 consumption along the rat small intestine. Microvasc Res, 35, 278-286 (1988)\
71. Peoples GE and McLennan PL: Dietary fish oil reduces skeletal muscle oxygen consumption, provides fatigue resistance and improves contractile recovery in the rat in vivo hindlimb. Br J Nutr, 104, 1771-1779 (2010)
72. Clemens MG and Forrester T: Appearance of adenosine triphosphate in thee coronary sinus effluent from isolated working heart in response to hypoxia. J Physiol (London), 312, 143-158
73. Carlsson C, Smith DS, Keykhah MM, Englebach I, Harp JR: The effects of high-dose fentanyl on cerebral circulation and metabolism in rats. Anesthesiology, 57, 375-380 (1982)
74. Refinetti R: Partition of heat production in the rat. Biotemas, 2, 47-55 (1989)
75. Ma SW, Foster DO, Nadeau BE, Triandafillou J: Absence of increased oxygen consumption in brown adipose tissue of rats exhibiting "cafeteria" diet-induced thermogenesis. Can J Physiol Pharmacol, 66, 1347-1354 (1988)
76. Sörbris R, Monti M, Nilsson-Ehle P and Wadsö I: Heat production by adipocytes from obese subjects before and after weight reduction. Metabolism 31, 973 (1982)
77. Even PC, Rolland V, Roseau S, Bouthegourd JC, Tomé D: Prediction of basal metabolism from organ size in the rat: relationship to strain, feeding, age, and obesity. Am J Physiol Regul Integr Comp Physiol, 280, R1887-1896 (2001)
78. Leibel RL, Rosenbaum M, Hirsch J: Changes in energy expenditure resulting from altered body weight. N Engl J Med, 332, 621 (1995)
79. Jobgen WS, Fried SK, Fu WJ, Meininger CJ and Wu G: Regulatory role for the arginine-nitric oxide pathway in metabolism of energy substrates. J Nutr Biochem, 17, 571-588 (2006)
80. Ichikawa M, Miyasaka K, Fujita Y, Shimazoe T and Funakoshi A: Disappearance of diurnal rhytm of energy expenditure in genetically diabetic obese rats. Jpn J Physiol, 48, 211-214 (1998)
81. Yoshida Y, Ichikawa M, Ohta M, Kanai S, Kobayash M, Ichimaru Y, Shimazoe T, Watanabe S, Funakoshi A, Miyasak K: A peroxisome proliferator-activated receptor gamma agonist influenced daily profile of energy expenditure in genetically obese diabetic rats. Jpn J Pharmacol, 88, 279-284 (2002)
82. Ichikawa M, Kanai S, Ichimani Y, Funakoshi A and Miyasaka K: The diurnal rhythm of energy expenditure differs between obese and glucose intolerant rats and Streptozotocin-induced diabetic rats. J Nutr, 130, 2562-2567 (2000)
83. Li Y, Wang N, Carroll RJ: Selecting the Number of Principal Components in Functional Data. J Am Stat Assoc, doi: 10.1080/01621459.2013.788980 (2013)
84. Longo KA, Charoenthongtrakul S, Giuliana DJ, Govek EK, McDonagh T, Distefano PS, Geddes BJ: The 24-hour respiratory quotient predicts energy intake and changes in body mass. Am J Physiol Regul Integr Comp Physiol, 298, R747-754 (2010)
85. Ogden CL, Yanovski SZ, Carroll MD, Flegal KM: The epidemiology of obesity. Gastroenterology, 132, 2087-2102 (2007)
86. German AJ: The growing problem of obesity in dogs and cats. J Nutr, 136, 1940S-1946S (2006)
87. Song MK, Rosenthal MJ, Song AM, Uyemura K, Yang H, Ament ME, Yamaguchi DT and Cornford EM: Body weight reduction in rats by oral treatment with zinc plus cyclo- (His-Pro). Br J Pharmacol, 158, 442-450 (2009)
88. Everitt RB and Hothorn T: An Introduction to Applied Multivariate Analysis with R. Heidelberg: Springer (2011)
89. Fu WJ, Stromberg AJ, Viele K, Carroll RJ and Wu G: Statistics and bioinformatics in nutritional sciences: analysis of complex data in the era of systems biology. J Nutr Biochem, 21, 561-572 (2010)
90. Wei JW, Carroll RJ, Harden KK and Wu G: Comparisons of treatment means when factors do not interact in two-factorial studies. Amino Acids, 42, 2031-2035 (2012)
91. Li S and Lin JD: Molecular control of circadian metabolic rhythms. J Appl Physiol, 107, 1959-1964 (2009)
92. Liu C, Li S, Liu T, Borjigin J and Lin JD: Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature, 447, 477-481 (2007)
93. Zhang S, Qiao S, Ren M, Zeng X, Ma X, Wu Z, Thacker P and Wu G: Supplementation with branched-chain amino acids to a low-protein diet regulates intestinal expression of amino acid and peptide transporters in weanling pigs. Amino Acids, 45, 1191-1205 (2013)
94. Ruan Z, Lv Y, Fu X, He Q, Deng Z, Liu W, Yingli Y, Wu X, Wu G, Wu X and Yin Y: Metabolomic analysis of amino acid metabolism in colitic rats supplemented with lactosucrose. Amino Acids, 45, 877-887 (2013)
95. Zhang J, Yin Y, Shu XG, Li T, Li F, Tan B, Wu Z and Wu G: Oral administration of MSG increases expression of glutamate receptors and transporters in the gastrointestinal tract of young piglets. Amino Acids, 45, 1169-1177 (2013)
96. Wang WW, Wu ZL, Dai ZL, Yang Y, Wang JJ and Wu G: Glycine metabolism in animals and humans: implications for nutrition and health. Amino Acids, 45, 463-477 (2013)
97. Wu G: Functional amino acids in nutrition and health. Amino Acids, 45, 407-411 (2013)
98. Wu G, Bazer FW, Satterfield MC, Li XL, Wang XQ, Johnson GA, Burghardt RC, Dai ZL, Wang JJ and Wu ZL: Impacts of arginine nutrition on embryonic and fetal development in mammals. Amino Acids, 45, 241-256 (2013)
99. Bernard JR, Liao YH, Ding Z, Hara D, Kleinert M, Nelson JL and Ivy JL: An amino acid mixture improves glucose tolerance and lowers insulin resistance in the obese Zucker rat. Amino Acids, 45, 191-203 (2013)
100. Torii K, Uneyama H and Nakamura E: Physiological roles of dietary glutamate signaling via gut-brain axis due to efficient digestion and absorption. J Gastroenterol, 48, 442-451 (2013)
101. Nakamura H, Kawamata Y, Kuwahara T, Smriga M and Sakai R: Long-term ingestion of monosodium L-glutamate did not induce obesity, dyslipidemia or insulin resistance: a two-generation study in mice. J Nutr Sci Vitaminol (Tokyo), 59, 129-135 (2013)
102. Adeva MM, Calviño J, Souto G, Donapetry C: Insulin resistance and the metabolism of branched-chain amino acids in humans. Amino Acids, 43, 171-181 (2012)
103. Mels CM, Schutte AE, Schutte R, Huisman HW, Smith W, Fourie CM, Kruger R, van Rooyen JM, Malan NT, Malan L: The link between vascular deterioration and branched chain amino acids in a population with high glycated haemoglobin: the SABPA study. Amino Acids, 45, 1405-1413 (2013)
104. Bassil MS, Gougeon R: Muscle protein anabolism in type 2 diabetes. Curr Opin Clin Nutr Metab Care, 16, 83-88 (2013)
105. Marliss EB, Chevalier S, Gougeon R, Morais JA, Lamarche M, Adegoke OA, Wu G: Elevations of plasma methylarginines in obesity and ageing are related to insulin sensitivity and rates of protein turnover. Diabetologia, 49, 351-359 (2006)
106. Fernandez JR, Klimentidis YC, Dulin-Keita A, Casazza K: Genetic influences in childhood obesity: recent progress and recommendations for experimental designs. Int J Obes (Lond), 36, 479-484 (2012)
107. Ramachandrappa S, Farooqi IS: Genetic approaches to understanding human obesity. J Clin Invest, 121, 2080-2086 (2011)