Long-term low carbohydrate diet leads to deleterious metabolic manifestations in diabetic mice

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Handa, Keiko ^a   Inukai, Kouichi ^a   Onuma, Hirohisa ^a   Kudo, Akihiko ^a   Nakagawa, Fumiyuki ^b   Tsugawa, Kazue ^c   Kitahara, Atsuko ^a   Moriya, Rie ^a   Takahashi, Kazuto ^a   Sumitani, Yoshikazu ^a   Hosaka, Toshio ^a   Kawakami, Hayato ^a   Oyadomari, Seiichi ^c   Ishida, Hitoshi ^a  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE 1; FIBROBLAST GROWTH FACTOR 21; ACYL COENZYME A DESATURASE; FATTY ACID; FIBROBLAST GROWTH FACTOR; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIABETES MELLITUS; FATTY ACID BLOOD LEVEL; GLUCOSE INTOLERANCE; INSULIN SENSITIVITY; LIPID BLOOD LEVEL; LIPID COMPOSITION; LOW CARBOHYDRATE DIET; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; OBESITY; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ADVERSE EFFECTS; ANIMAL; BLOOD; C57BL MOUSE; DIET THERAPY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETICS; INSULIN RESISTANCE; LIVER; METABOLISM; MOUSE MUTANT; ORGAN SIZE; PATHOLOGY;

ANIMALS; BODY WEIGHT; DIABETES MELLITUS, EXPERIMENTAL; DIET, CARBOHYDRATE-RESTRICTED; FATTY ACIDS; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION; INSULIN RESISTANCE; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; ORGAN SIZE; RNA, MESSENGER; STEAROYL-COA DESATURASE;

EID: 84929517145     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104948     Document Type: Article

References (39)

1. Shai I, Schwarzfuchs D, Henkin Y, Shahar DR, Witkow S, et al. (2008) Weight loss with a low-carbohydrate, Mediterranean, or low-fat diet. N Engl J Med 359: 229-241. (Pubitemid 352008438)
2. Foster GD, Wyatt HR, Hill JO, McGuckin BG, Brill C, et al. (2003) A randomized trial of a low-carbohydrate diet for obesity. N Engl J Med 348: 2082-2090. (Pubitemid 36583303)
3. Samaha FF, Iqbal N, Seshadri P, Chicano KL, Daily DA, et al. (2003) A low-carbohydrate as compared with a low-fat diet in severe obesity. N Engl J Med 348: 2074-2081. (Pubitemid 36583302)
4. Lagiou P, Sandin S, Lof M, Trichopoulos D, Adami HO, et al. (2012) Low carbohydrate-high protein diet and incidence of cardiovascular diseases in Swedish women: prospective cohort study. BMJ 344: +e4026.
5. Sjögren P, Becker W, Warensjö E, Olsson E, Byberg L, et al. (2012) Mediterranean and carbohydrate-restricted diets and mortality among elderly men: a cohort study in Sweden. Am J Clin Nutr 92: 967-974.
6. Westman EC, Feinman RD, Mavropoulos JC, Vernon MC, Volek JS, et al. (2007) Low-carbohydrate nutrition and metabolism. Am J Clin Nutr 86: 276-284. (Pubitemid 47256909)
7. Dyson PA (2008) A review of low and reduced carbohydrate diets and weight loss in type 2 diabetes. Hum Nutr Diet 21: 530-538.
8. Jornayvaz FR, Jurczak MJ, Lee HY, Birkenfeld AL, Frederick DW, et al. (2010) A high-fat, ketogenic diet causes hepatic insulin resistance in mice, despite increasing energy expenditure and preventing weight gain. Am J Physiol Endocrinol Metab 299: E808-815.
9. Garbow JR, Doherty JM, Schugar RC, Travers S, Weber ML, et al. (2011) Hepatic steatosis, inflammation, and ER stress in mice maintained long term on a very low-carbohydrate ketogenic diet. Am J Physiol Gastrointest Liver Physiol 300: G956-967.
10. Badman MK, Pissios P, Kennedy AR, Koukos G, Flier JS, et al. (2007) Hepatic fibroblast growth factor 21 is regulated by PPARa and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab 5: 426-437. (Pubitemid 46825495)
11. Xu J, Lloyd DJ, Hale C, Stanislaus S, Chen M, et al. (2009) Fibroblast growth factor 21 reverses hepatic steatosis, increases energy expenditure, and improves insulin sensitivity in diet-induced obese mice. Diabetes 58: 250-259.
12. Taketomi S, Tsuda M, Matsuo T, Iwatsuka H, Suzuoki Z (1973) Alteration of hepatic enzyme activities in KK and yellow KK mice with various diabetic states. Horm Metab Res 5: 333-339.
13. Nakashima Y, Inukai K, Imai K, Ikegami Y, Awata T, et al. (2008) Involvement of low adiponectin levels in impaired glucose tolerance. Metabolism 57: 1350-1354.
14. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
15. Bowen CL, Kehler J, Evans CA (2010) Development and validation of a sensitive and selective UHPLC-MS/MS method for simultaneous determination of both free and total eicosapentaeonic acid and docosahexenoic acid in human plasma. J Chromatogr B Analyt Technol Biomed Life Sci 878: 3125-3133.
16. Ikegami Y, Inukai K, Imai K, Sakamoto Y, Katagiri H, et al. (2009) Adiponectin upregulates ferritin heavy chain in skeletal muscle cells. Diabetes 58: 61-70.
17. Yamashita S, Kudo A, Kawakami H, Okada Y (2013) Mechanisms of angiogenic suppression in uteri exposed to diethylstilbestrol neonatally in the mouse. Biology of Reproduction 88: 1-13.
18. Ruifrok AC, Johnston DA (2001) Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 23: 291-299. (Pubitemid 32762920)
19. Kim S, Sohn I, Ahn JI, Lee KH, Lee YS, et al. (2004) Hepatic gene expression profiles in a long-term high-fat diet-induced obesity mouse model. Gene 340: 99-109. (Pubitemid 39360236)
20. Camporez JP, Jornayvaz FR, Petersen MC, Pesta D, Guigni BA, et al. (2013) Cellular mechanisms by which FGF21 improves insulin sensitivity in male mice. Endocrinology 154: 3099-3109.
21. Al-Shudiefat AA, Sharma AK, Bagchi AK, Dhingra S, Singal PK (2013) Oleic acid mitigates TNF-α-induced oxidative stress in rat cardiomyocytes. Mol Cell Biochem 372: 75-82.
22. Anderson JW, Randles KM, Kendall CW, Jenkins DJ (2004) Carbohydrate and fiber recommendations for individuals with diabetes: a quantitative assessment and meta-analysis of the evidence. J Am Coll Nutr 23: 5-17. (Pubitemid 38200830)
23. Wheeler ML, Dunbar SA, Jaacks LM, Karmally W, Mayer-Davis EJ, et al. (2012) Macronutrients, food groups, and eating patterns in the management of diabetes: a systematic review of the literature. Diabetes Care 35: 434-445.
24. Yong R, Chen XM, Shen S, Vijayaraj S, Ma Q, et al. (2013) Plumbagin ameliorates diabetic nephropathy via interruption of pathways that include NOX4 signalling. PLoS One 8: e73428.
25. Fisher FM, Kleiner S, Douris N, Fox EC, Mepani RJ, et al. (2012) FGF21 regulates PGC1α and browning of white adipose tissues in adaptive thermogenesis. Genes Dev 26: 271-281.
26. Holland WL, Adams AC, Brozinick JT, Bui HH, Miyauchi Y, et al. (2013) An FGF21-adiponectin-ceramide axis controls energy expenditure and insulin action in mice. Cell Metab 17: 790-797.
27. Murata Y, Nishio K, Mochiyama T, Konishi M, Shimada M, et al. (2013) Fgf21 impairs adipocyte insulin sensitivity in mice fed a low-carbohydrate, high-fat ketogenic diet. PLoS One 8: e69330.
28. Kim KH, Kim SH, Min YK, Yang HM, Lee JB, et al. (2013) Acute exercise induces FGF21 expression in mice and in healthy humans. PLoS One 9: e63517.
29. Schaap FG, Kremer AE, Lamers WH, Jansen PL, Gaemers IC (2012) Fibloblast growth factor 21 is induced by endoplasmic reticulum stress. Biochimie 95: 692-699.
30. Ding X, Boney-Montoya J, Owen BM, Bookout AL, Coate KC, et al. (2012) bKlotho is required for fibroblast growth factor 21 effects on growth and metabolism. Cell Metab 16: 387-393.
31. Zhang Y, Xie Y, Berglund ED, Coate KC, He TT, et al. (2012) The starvation hormone, fibroblast growth factor-21, extends lifespan in mice. Elife 1: e00065.
32. Geng T, Hu W, Broadwater MH, Snider JM, Bielawski J, et al. (2013) Fatty acids differentially regulate insulin resistance through endoplasm reticulum stress-mediated induction of tribbles homologue 3: a potential link between dietary fat composition and the pathophysiological outcomes of obesity. Diabetologia 56: 2078-2087.
33. Stefan N, Peter A, Cegan A, Staiger H, Machann J, et al. (2008) Low hepatic stearoyl-CoA desaturase 1 activity is associated with fatty liver and insulin resistance in obese humans. Diabetologia 51: 648-656.
34. Fernández Gianotti T, Burgueño A, Gonzales Mansilla N, Pirola CJ, Sookoian S (2013) Fatty liver is associated with transcriptional downregulation of stearoyl-CoA desaturase and impaired protein dimerization. PLoS One 8: e76912.
35. Ntambi JM (1992) Dietary regulation of stearoyl-CoA desaturase 1 gene expression in mouse liver. J Biol Chem 267: 10925-10930.
36. Gillingham LG, Harris-Janz S, Jones PJ (2011) Dietary monounsaturated fatty acids are protective against metabolic syndrome and cardiovascular disease risk factors. Lipids 46: 209-228.
37. Robert AE, Alexandra KL, Noguchi Y, Shiota M (2014) Palmitate-induced activation of mitochondrial metabolism promote oxidative stress and apoptosis in H4IIEC3 rat hepatocytes. Metabolism 63: 283-295.
38. Hoevenaar-Blom MP, Nooyens AC, Kromhout D, Spijkerman AM, Beulens JW, et al. (2012) Mediterranean style diet and 12-year incidence of cardiovascular diseases. PLoS One 7: e45458.
39. Solon-Biet SM, McMahon AC, Ballard JW, Ruohonen K, Wu LE, et al. (2014) The ratio of macronutrients, not calorie intake, dictates cardiometabolic health, aging and longevity in ad libitum-fed mice. Cell Metab 19:418-430.