Oxygen restriction as challenge test reveals early high-fat-diet-induced changes in glucose and lipid metabolism

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 6, 2015, Pages 1179-1193

  Duivenvoorde, Loes P M ^a   van Schothorst, Evert M ^a   Derous, Davina ^a   van der Stelt, Inge ^a   Masania, Jinit ^b   Rabbani, Naila ^b   Thornalley, Paul J ^b   Keijer, Jaap ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

High fat diet; Hypoxia; Indirect calorimetry; Metabolism; Obesity; Oxidative stress

Indexed keywords

GLUCOSE; OXYGEN; PROTEIN DEGRADATION END PRODUCT;

ADIPOSE TISSUE; ADVERSE EFFECTS; ANIMAL; ANOXIA; C57BL MOUSE; LIPID DIET; LIPID METABOLISM; LIVER; MALE; METABOLISM; MOUSE; OBESITY; OXYGEN CONSUMPTION;

ADIPOSE TISSUE; ANIMALS; ANOXIA; DIET, HIGH-FAT; GLUCOSE; LIPID METABOLISM; LIVER; MALE; MICE; MICE, INBRED C57BL; OBESITY; OXYGEN; OXYGEN CONSUMPTION; PROTEIN DEGRADATION END PRODUCTS;

EID: 84939884646     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1553-8     Document Type: Article

References (60)

1. Aon MA, Stanley BA, Sivakumaran V, Kembro JM, O’Rourke B, Paolocci N, Cortassa S (2012) Glutathione/thioredoxin systems modulate mitochondrial H2O2 emission: an experimental-computational study. J Gen Physiol 139:479–491. doi:10.1085/jgp.201210772
2. Asterholm IW, Scherer PE (2010) Enhanced metabolic flexibility associated with elevated adiponectin levels. Am J Pathol 176:1364–1376. doi:10.2353/ajpath.2010.090647
3. Bartelt A, Heeren J (2012) The holy grail of metabolic disease: brown adipose tissue. Curr Opin Lipidol 23:190–195. doi:10.1097/MOL.0b013e328352dcef
4. Baze MM, Schlauch K, Hayes JP (2010) Gene expression of the liver in response to chronic hypoxia. Physiol Genomics. doi:10.1152/physiolgenomics.00075.2009
5. Butler AA, Kozak LP (2010) A recurring problem with the analysis of energy expenditure in genetic models expressing lean and obese phenotypes. Diabetes 59:323–329. doi:10.2337/db09-1471
6. Cannon B, Nedergaard J (2011) Nonshivering thermogenesis and its adequate measurement in metabolic studies. J Exp Biol 214:242–253. doi:10.1242/jeb.050989
7. Cao H, Gerhold K, Mayers JR, Wiest MM, Watkins SM, Hotamisligil GS (2008) Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 134:933–944. doi:10.1016/j.cell.2008.07.048
8. Carstens MT, Goedecke JH, Dugas L, Evans J, Kroff J, Levitt NS, Lambert EV (2013) Fasting substrate oxidation in relation to habitual dietary fat intake and insulin resistance in non-diabetic women: a case for metabolic flexibility? Nutr Metab (Lond) 10:8. doi:10.1186/1743-7075-10-8
9. Charlot K, Pichon A, Richalet JP, Chapelot D (2013) Effects of a high-carbohydrate versus high-protein meal on acute responses to hypoxia at rest and exercise. Eur J Appl Physiol 113:691–702. doi:10.1007/s00421-012-2472-z
10. Choi JH, Park MJ, Kim KW, Choi YH, Park SH, An WG, Yang US, Cheong J (2005) Molecular mechanism of hypoxia-mediated hepatic gluconeogenesis by transcriptional regulation. FEBS Lett 579:2795–2801. doi:10.1016/j.febslet.2005.03.097
11. David JM, Chatziioannou AF, Taschereau R, Wang H, Stout DB (2013) The hidden cost of housing practices: using noninvasive imaging to quantify the metabolic demands of chronic cold stress of laboratory mice. Comp Med 63:386–391
12. Drager LF, Li J, Reinke C, Bevans-Fonti S, Jun JC, Polotsky VY (2011) Intermittent hypoxia exacerbates metabolic effects of diet-induced obesity. Obesity (Silver Spring) 19:2167–2174. doi:10.1038/oby.2011.240
13. Duivenvoorde LP, van Schothorst EM, Bunschoten A, Keijer J (2011) Dietary restriction of mice on a high-fat diet induces substrate efficiency and improves metabolic health. J Mol Endocrinol 47:81–97. doi:10.1530/JME-11-0001
14. Duivenvoorde LPM, van Schothorst EM, Swarts HJ, Keijer J (2014) Assessment of metabolic flexibility of old and adult mice using three non-invasive, indirect calorimetry-based treatments. J Gerontol A Biol Sci Med Sci. doi:10.1093/gerona/glu027
15. Eccleston HB, Andringa KK, Betancourt AM, King AL, Mantena SK, Swain TM, Tinsley HN, Nolte RN, Nagy TR, Abrams GA, Bailey SM (2011) Chronic exposure to a high-fat diet induces hepatic steatosis, impairs nitric oxide bioavailability, and modifies the mitochondrial proteome in mice. Antioxid Redox Signal 15:447–459. doi:10.1089/ars.2010.3395
16. Eissing L, Scherer T, Todter K, Knippschild U, Greve JW, Buurman WA, Pinnschmidt HO, Rensen SS, Wolf AM, Bartelt A, Heeren J, Buettner C, Scheja L (2013) De novo lipogenesis in human fat and liver is linked to ChREBP-beta and metabolic health. Nat Commun 4:1528. doi:10.1038/ncomms2537
17. Feldmann HM, Golozoubova V, Cannon B, Nedergaard J (2009) UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9:203–209. doi:10.1016/j.cmet.2008.12.014
18. Gamboa JL, Andrade FH (2010) Mitochondrial content and distribution changes specific to mouse diaphragm after chronic normobaric hypoxia. Am J Physiol Regul Integr Comp Physiol 298:R575–R583. doi:10.1152/ajpregu.00320.2009
19. Golja P, Flander P, Klemenc M, Maver J, Princi T (2008) Carbohydrate ingestion improves oxygen delivery in acute hypoxia. High Alt Med Biol 9:53–62. doi:10.1089/ham.2008.1021
20. Hoevenaars FP, Keijer J, Swarts HJ, Snaas-Alders S, Bekkenkamp-Grovenstein M, van Schothorst EM (2013) Effects of dietary history on energy metabolism and physiological parameters in C57BL/6J mice. Exp Physiol 98:1053–1062. doi:10.1113/expphysiol.2012.069518
21. Hoevenaars FP, van Schothorst EM, Horakova O, Voigt A, Rossmeisl M, Pico C, Caimari A, Kopecky J, Klaus S, Keijer J (2012) BIOCLAIMS standard diet (BIOsd): a reference diet for nutritional physiology. Genes Nutr 7:399–404. doi:10.1007/s12263-011-0262-6
22. Horakova O, Medrikova D, van Schothorst EM, Bunschoten A, Flachs P, Kus V, Kuda O, Bardova K, Janovska P, Hensler M, Rossmeisl M, Wang-Sattler R, Prehn C, Adamski J, Illig T, Keijer J, Kopecky J (2012) Preservation of metabolic flexibility in skeletal muscle by a combined use of n-3 PUFA and rosiglitazone in dietary obese mice. PLoS One 7:e43764. doi:10.1371/journal.pone.0043764
23. Hutter JF, Schweickhardt C, Piper HM, Spieckermann PG (1984) Inhibition of fatty acid oxidation and decrease of oxygen consumption of working rat heart by 4-bromocrotonic acid. J Mol Cell Cardiol 16:105–108
24. Jequier E, Acheson K, Schutz Y (1987) Assessment of energy expenditure and fuel utilization in man. Annu Rev Nutr 7:187–208. doi:10.1146/annurev.nu.07.070187.001155
25. Kelly KR, Williamson DL, Fealy CE, Kriz DA, Krishnan RK, Huang H, Ahn J, Loomis JL, Kirwan JP (2010) Acute altitude-induced hypoxia suppresses plasma glucose and leptin in healthy humans. Metabolism 59:200–205. doi:10.1016/j.metabol.2009.07.014
26. Kim DH, Gutierrez-Aguilar R, Kim HJ, Woods SC, Seeley RJ (2013) Increased adipose tissue hypoxia and capacity for angiogenesis and inflammation in young diet-sensitive C57 mice compared with diet-resistant FVB mice. Int J Obes (Lond) 37:853–860. doi:10.1038/ijo.2012.141
27. Larsen JJ, Hansen JM, Olsen NV, Galbo H, Dela F (1997) The effect of altitude hypoxia on glucose homeostasis in men. J Physiol 504(Pt 1):241–249
28. Li J, Grigoryev DN, Ye SQ, Thorne L, Schwartz AR, Smith PL, O’Donnell CP (1985) Polotsky VY (2005) Chronic intermittent hypoxia upregulates genes of lipid biosynthesis in obese mice. J Appl Physiol 99:1643–1648. doi:10.1152/japplphysiol.00522.2005
29. Livesey G, Elia M (1988) Estimation of energy expenditure, net carbohydrate utilization, and net fat oxidation and synthesis by indirect calorimetry: evaluation of errors with special reference to the detailed composition of fuels. Am J Clin Nutr 47:608–628
30. Louis M, Punjabi NM (2009) Effects of acute intermittent hypoxia on glucose metabolism in awake healthy volunteers. J Appl Physiol 106:1538–1544. doi:10.1152/japplphysiol.91523.2008
31. Masschelein E, Van Thienen R, D’Hulst G, Hespel P, Thomis M, Deldicque L (2014) Acute environmental hypoxia induces LC3 lipidation in a genotype-dependent manner. FASEB J 28:1022–1034. doi:10.1096/fj.13-239863
32. Mazzatti D, Lim FL, O’Hara A, Wood IS, Trayhurn P (2012) A microarray analysis of the hypoxia-induced modulation of gene expression in human adipocytes. Arch Physiol Biochem 118:112–120. doi:10.3109/13813455.2012.654611
33. Mimura Y, Furuya K (1995) Mechanisms of adaptation to hypoxia in energy metabolism in rats. J Am Coll Surg 181:437–443
34. Montgomery MK, Hallahan NL, Brown SH, Liu M, Mitchell TW, Cooney GJ, Turner N (2013) Mouse strain-dependent variation in obesity and glucose homeostasis in response to high-fat feeding. Diabetologia 56:1129–1139. doi:10.1007/s00125-013-2846-8
35. Mortola JP, Rezzonico R, Lanthier C (1989) Ventilation and oxygen consumption during acute hypoxia in newborn mammals: a comparative analysis. Respir Physiol 78:31–43
36. Nieto FJ, Young TB, Lind BK, Shahar E, Samet JM, Redline S, D’Agostino RB, Newman AB, Lebowitz MD, Pickering TG (2000) Association of sleep-disordered breathing, sleep apnea, and hypertension in a large community-based study. Sleep Heart Health Study JAMA 283:1829–1836
37. Oltmanns KM, Gehring H, Rudolf S, Schultes B, Rook S, Schweiger U, Born J, Fehm HL, Peters A (2004) Hypoxia causes glucose intolerance in humans. Am J Respir Crit Care Med 169:1231–1237. doi:10.1164/rccm.200308-1200OC
38. Ostreicher I, Meissner U, Plank C, Allabauer I, Castrop H, Rascher W, Dotsch J (2009) Altered leptin secretion in hyperinsulinemic mice under hypoxic conditions. Regul Pept 153:25–29. doi:10.1016/j.regpep.2008.11.011
39. Peronnet F, Massicotte D (1991) Table of nonprotein respiratory quotient: an update. Can J Sport Sci 16:23–29
40. Pison CM, Chauvin C, Perrault H, Schwebel C, Lafond JL, Boujet C, Leverve XM (1998) In vivo hypoxic exposure impairs metabolic adaptations to a 48 hour fast in rats. Eur Respir J 12:658–665
41. Postic C, Girard J (2008) Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J Clin Invest 118:829–838. doi:10.1172/JCI34275
42. Rabbani N, Chittari MV, Bodmer CW, Zehnder D, Ceriello A, Thornalley PJ (2010) Increased glycation and oxidative damage to apolipoprotein B100 of LDL cholesterol in patients with type 2 diabetes and effect of metformin. Diabetes 59:1038–1045. doi:10.2337/db09-1455
43. Rabbani N, Shaheen F, Anwar A, Masania J, Thornalley PJ (2014) Assay of methylglyoxal-derived protein and nucleotide AGEs. Biochemical Society Transactions in press
44. Regazzetti C, Peraldi P, Gremeaux T, Najem-Lendom R, Ben-Sahra I, Cormont M, Bost F, Le Marchand-Brustel Y, Tanti JF, Giorgetti-Peraldi S (2009) Hypoxia decreases insulin signaling pathways in adipocytes. Diabetes 58:95–103. doi:10.2337/db08-0457
45. Reinke C, Bevans-Fonti S, Drager LF, Shin MK, Polotsky VY (2011) Effects of different acute hypoxic regimens on tissue oxygen profiles and metabolic outcomes. J Appl Physiol 111:881–890. doi:10.1152/japplphysiol.00492.2011
46. Rupnick MA, Panigrahy D, Zhang CY, Dallabrida SM, Lowell BB, Langer R, Folkman MJ (2002) Adipose tissue mass can be regulated through the vasculature. Proc Natl Acad Sci U S A 99:10730–10735. doi:10.1073/pnas.162349799
47. Saito K, Ohta Y, Sami M, Kanda T, Kato H (2010) Effect of mild restriction of food intake on gene expression profile in the liver of young rats: reference data for in vivo nutrigenomics study. Br J Nutr 104:941–950. doi:10.1017/S0007114510001625
48. Semenza GL, Roth PH, Fang HM, Wang GL (1994) Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 269:23757–23763
49. Takeuchi M, Kimura S, Kuroda J, Ashihara E, Kawatani M, Osada H, Umezawa K, Yasui E, Imoto M, Tsuruo T, Yokota A, Tanaka R, Nagao R, Nakahata T, Fujiyama Y, Maekawa T (2010) Glyoxalase-I is a novel target against Bcr-Abl+ leukemic cells acquiring stem-like characteristics in a hypoxic environment. Cell Death Differ 17:1211–1220. doi:10.1038/cdd.2010.6
50. Taylor CT (2008) Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem J 409:19–26. doi:10.1042/BJ20071249
51. Thornalley PJ, Battah S, Ahmed N, Karachalias N, Agalou S, Babaei-Jadidi R, Dawnay A (2003) Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem J 375:581–592. doi:10.1042/BJ20030763
52. Thornalley PJ, Rabbani N (2014) Detection of oxidized and glycated proteins in clinical samples using mass spectrometry—a user’s perspective. Biochim Biophys Acta 1840:818–829. doi:10.1016/j.bbagen.2013.03.025
53. Tschop MH, Speakman JR, Arch JR, Auwerx J, Bruning JC, Chan L, Eckel RH, Farese RV Jr, Galgani JE, Hambly C, Herman MA, Horvath TL, Kahn BB, Kozma SC, Maratos-Flier E, Muller TD, Munzberg H, Pfluger PT, Plum L, Reitman ML, Rahmouni K, Shulman GI, Thomas G, Kahn CR, Ravussin E (2012) A guide to analysis of mouse energy metabolism. Nat Methods 9:57–63. doi:10.1038/nmeth.1806
54. Ukropcova B, McNeil M, Sereda O, de Jonge L, Xie H, Bray GA, Smith SR (2005) Dynamic changes in fat oxidation in human primary myocytes mirror metabolic characteristics of the donor. J Clin Invest 115:1934–1941. doi:10.1172/JCI24332
55. van Ommen B, Keijer J, Heil SG, Kaput J (2009) Challenging homeostasis to define biomarkers for nutrition related health. Mol Nutr Food Res 53:795–804. doi:10.1002/mnfr.200800390
56. Van Schothorst EM, Franssen-van Hal N, Schaap MM, Pennings J, Hoebee B, Keijer J (2005) Adipose gene expression patterns of weight gain suggest counteracting steroid hormone synthesis. Obes Res 13:1031–1041. doi:10.1038/oby.2005.121
57. Voigt A, Agnew K, van Schothorst EM, Keijer J, Klaus S (2013) Short-term, high fat feeding-induced changes in white adipose tissue gene expression are highly predictive for long-term changes. Mol Nutr Food Res 57:1423–1434. doi:10.1002/mnfr.201200671
58. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Investig 112:1796–1808. doi:10.1172/Jci2000319246
59. Xu HY, Barnes GT, Yang Q, Tan Q, Yang DS, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Investig 112:1821–1830. doi:10.1172/Jci200319451
60. Yin J, Gao Z, He Q, Zhou D, Guo Z, Ye J (2009) Role of hypoxia in obesity-induced disorders of glucose and lipid metabolism in adipose tissue. Am J Physiol Endocrinol Metab 296:E333–E342. doi:10.1152/ajpendo.90760.2008