Fructose and Fructans: Opposite Effects on Health?

Plant Foods for Human Nutrition

Volumn 70, Issue 3, 2015, Pages 227-237

  Di Bartolomeo, Francesca ^a   Van den Ende, Wim ^b  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b LEUVEN FOOD SCIENCE AND NUTRITION RESEARCH CENTRE LFORCE   (Belgium)

Author keywords

Diabetes; Food; Fructan; Fructose; Health; Oxidative stress; Prebiotics

Indexed keywords

ANTIOXIDANT; CARBOHYDRATE DIET; FRUCTAN; FRUCTOSE; IMMUNOLOGIC FACTOR; PREBIOTIC AGENT; SWEETENING AGENT;

AUTOPHAGY; CARBOHYDRATE DIET; DIET; DRUG EFFECTS; HUMAN; PHARMACOLOGY;

ANTIOXIDANTS; AUTOPHAGY; DIET; DIETARY CARBOHYDRATES; FRUCTANS; FRUCTOSE; HUMANS; IMMUNOLOGIC FACTORS; PREBIOTICS; SWEETENING AGENTS;

EID: 84939472894     PISSN: 09219668     EISSN: 15739104     Source Type: Journal    
DOI: 10.1007/s11130-015-0485-6     Document Type: Review

References (81)

1. Oser BL (1985) Highlights in the history of saccharin toxicology. Food Chem Toxicol 23:535–542
2. Gwak MJ, Chung SJ, Kim YJ, Lim CS (2012) Relative sweetness and sensory characteristics of bulk and intense sweeteners. Food Sci Biotechnol 21:889–894
3. Waldrop ME, Ross CF (2014) Sweetener blend optimization by using mixture design methodology and the electronic tongue. J Food Sci 79:S1782–S1794
4. Fuchs A (1991) Current and potential food and non-food applications of fructans. Biochem Soc Trans 19:555–560
5. Davis SN, Mann SL, Cherrington AD (2001) Acute fructose administration improves oral glucose tolerance in adults with type 2 diabetes. Diabetes Care 24:1882–1887
6. American Dietetic Association (2004) Use of nutritive and non-nutritive sweeteners. J Am Diet Assoc 104:255–275
7. Elliott SS, Keim NL, Stern JS, Teff K, Havel PJ (2002) Fructose, weight gain and the insulin resistance syndrome. Am J Clin Nutr 76:911–922
8. Niewoehner CB (1986) Metabolic effects of dietary versus parenteral fructose. J Am Coll Nutr 5:443–450
9. Levine R (1986) Monosaccharides in health and disease. Annu Rev Nutr 6:211–224
10. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C (2004) American Heart Association, National Heart, Lung, and Blood Institute, Definition of Metabolic Syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association Conference on Scientific Issues Related to Definition. Circulation 109:433–438
11. Bremer AA, Stanhope KL, Graham JL, Cummings BP, Wang W, Saville BR, Havel PJ (2011) Fructose-fed rhesus monkeys: a nonhuman primate model of insulin resistance, metabolic syndrome, and type 2. Clin Transl Sci 4:243–252
12. Barone S, Fussell SL, Singh AK, Lucas F, Xu J, Kim C, Wu X, Yu Y, Amlal H, Seidler U, Zuo J, Soleimani M (2009) Slc2a5 (Glut5) is essential for the absorption of fructose in the intestine and generation of fructose-induced hypertension. J Biol Chem 284:5056–5066
13. Dyer J, Wood IS, Palejwala A, Ellis A, Shirazi-Beechey SP (2002) Expression of monosaccharide transporters in intestine of diabetic humans. Am J Physiol Gastrointest Liver Physiol 282:G241–G248
14. Douard V, Ferraris RP (2008) Regulation of the fructose transporter GLUT5 in health and disease. Am J Physiol Endocrinol Metab 295:E227–E237
15. Mayes PA (1993) Intermediary metabolism of fructose. Am J Clin Nutr 58:S754–S765
16. Mor I, Cheung EC, Vousden KH (2011) Control of glycolysis through regulation of PFK1: old friends and recent additions. Cold Spring Harb Symp Quant Biol 76:211–216
17. Bruynseels K, Bergans N, Gillis N, van Dorpen F, Van Hecke P, Stalmans W, Vanstapel F (1999) On the inhibition of hepatic glycogenolysis by fructose. A 31P-NMR study in perfused rat liver using the fructose analogue 2,5-anhydro-D-mannitol. NMR Biomed 12:145–156
18. Lanaspa MA, Sanchez-Lozada LG, Choi YJ, Cicerchi C, Kanbay M, Roncal-Jimenez CA, Ishimoto T, Li N, Marek G, Duranay M, Schreiner G, Rodriguez-Iturbe B, Nakagawa T, Kang DH, Sautin YY, Johnson JR (2012) Uric acid induces hepatic steatosis by generation of mitochondrial oxidative stress: potential role in fructose-dependent and -independent fatty liver. J Biol Chem 287:40732–40744
19. Sluijs I, Beulens JW, Van der A DL, Spijkerman AM, Schulze MB, Van der Schouw YT (2013) Plasma uric acid is associated with increased risk of type 2 diabetes independent of diet and metabolic risk factors. J Nutr 143:80–85
20. Cox CL, Stanhope KL, Schwarz JM, Graham JL, Hatcher B, Griffen SC, Bremer AA, Berglund L, McGahan JP, Keim NL, Havel PJ (2012) Consumption of fructose- but not glucose-sweetened beverages for 10 weeks increases circulating concentrations of uric acid, retinol binding protein-4, and gamma-glutamyl transferase activity in overweight/obese humans. Nutr Metab (Lond) 9:68
21. Terra X, Auguet T, Broch M, Sabench F, Hernández M, Pastor RM, Quesada IM, Luna A, Aguilar C, Del Castillo D, Richart C (2013) Retinol binding protein-4 circulating levels were higher in nonalcoholic fatty liver disease vs. histologically normal liver from morbidly obese women. Obesity (Silver Spring) 21:170–177
22. Baron AD, Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G (1995) Insulin-mediated skeletal muscle vasodilation contributes to both insulin sensitivity and responsiveness in lean humans. J Clin Invest 96:786–792
23. Nakagawa T, Hu H, Zharikov S, Tuttle KR, Short RA, Glushakova O, Ouyang X, Feig DI, Block ER, Herrera-Acosta J, Patel JM, Johnson RJ (2006) A causal role for uric acid in fructose-induced metabolic syndrome. Am J Physiol Renal Physiol 290:F625–F631
24. Truswell AS (1992) Glycaemic index of foods. Eur J Clin Nutr 44(Suppl 2):S91–S101
25. Klok MD, Jakobsdottir S, Drent ML (2007) The role of leptin and ghrelin in the regulation of food intake and body weight in humans: a review. Obes Rev 8:21–34
26. Anderson GH, Woodend D (2003) Effect of glycemic carbohydrates on short-term satiety and food intake. Nutr Rev 61:S17–S26
27. Shapiro A, Mu W, Roncal C, Cheng KY, Johnson RJ, Scarpace PJ (2008) Fructose-induced leptin resistance exacerbates weight gain in response to subsequent high-fat feeding. Am J Physiol Regul Integr Comp Physiol 295:R1370–R1375
28. Vila L, Roglans N, Alegret M, Sanchez RM, Vazquez-Carrera M, Laguna JC (2008) Suppressor of cytokine signaling-3 (SOCS-3) and a deficit of serine/threonine (Ser/Thr) phosphoproteins involved in leptin transduction mediate the effect of fructose on rat liver lipid metabolism. Hepatology 48:1506–1516
29. Stanhope KL, Griffen SC, Bremer AA, Vink RG, Schaefer EJ, Nakajima K, Schwarz JM, Beysen C, Berglund L, Keim N, Havel PJ (2011) Metabolic responses to prolonged consumption of glucose- and fructose-sweetened beverages are not associated with postprandial or 24-h glucose and insulin excursions. Am J Clin Nutr 94:112–119
30. Faeh D, Minehira K, Schwarz JM, Periasamy R, Park S, Tappy L (2005) Effect of fructose overfeeding and fish oil administration on hepatic de novo lipogenesis and insulin sensitivity in healthy men. Diabetes 54:1907–1913
31. Wu T, Giovannucci E, Pischon T, Hankinson SE, Ma J, Rifai N, Rimm EB (2004) Fructose, glycemic load, and quantity and quality of carbohydrate in relation to plasma C-peptide concentrations in US women. Am J Clin Nutr 80:1043–1049
32. Corcoran MP, Lamon-Fava S, Fielding RA (2007) Skeletal muscle lipid deposition and insulin resistance: effect of dietary fatty acids and exercise. Am J Clin Nutr 85:662–677
33. Pagliassotti MJ, Kang J, Thresher JS, Sung CK, Bizeau ME (2002) Elevated basal PI 3-kinase activity and reduced insulin signaling in sucrose-induced hepatic insulin resistance. Am J Physiol Endocrinol Metab 282:E170–E176
34. Ueno M, Bezerra RM, Silva MS, Tavares DQ, Carvalho CR, Saad MJ (2000) A high-fructose diet induces changes in pp 185 phosphorylation in muscle and liver of rats. Braz J Med Biol Res 33:1421–1427
35. Samuel VT, Petersen KF, Shulman GI (2010) Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375:2267–2277
36. Kim JK, Fillmore JJ, Sunshine MJ et al (2004) PKC-theta knockout mice are protected from fat-induced insulin resistance. J Clin Invest 114:823–827
37. Wei Y, Wang D, Topczewski F, Pagliassotti MJ (2007) Fructose-mediated stress signalling in the liver: implication for hepatic insulin resistance. J Nutr Biochem 18:1–9
38. Lim JS, Mietus-Snyder M, Valente A, Schwarz JM, Lustig RH (2010) The role of fructose in the pathogenesis of NAFLD and the metabolic syndrome. Nat Rev Gastroenterol Hepatol 7:251–264
39. Chong MF, Fielding BA, Frayn KN (2007) Mechanisms for the acute effect of fructose on postprandial lipemia. Am J Clin Nutr 85:1511–1520
40. Bar-On H, Stein Y (1968) Effect of glucose and fructose administration on lipid metabolism in the rat. J Nutr 94:95–105
41. Schwarz JM, Neese R, Shackleton C, Hellerstein MK (1993) De novo lipogenesis during fasting and oral fructose in lean and obese hyperinsulinemic subjects. Diabetes 42(Suppl):1–39A
42. McGarry JD, Brown NF (1997) The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. Eur J Biochem 244:1–14
43. Matsuzaka T, Shimano H, Yahagi N, Amemiya-Kudo M, Okazaki H, Tamura Y, Iizuka Y, Ohashi K, Tomita S, Sekiya M, Hasty A, Nakagawa Y, Sone H, Toyoshima H, Ishibashi S, Osuga J, Yamada N (2004) Insulin-independent induction of sterol regulatory element-binding protein-1c expression in the livers of streptozotocin-treated mice. Diabetes 53:560–569
44. Stanhope KL, Schwarz JM, Keim NL et al (2009) Consuming fructose-sweetened, not glucose- sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J Clin Invest 119:1322–1334
45. Rippe JM, Angelopoulos TJ (2013) Sucrose, high-fructose corn syrup, and fructose, their metabolism and potential health effects: what do we really know? Adv Nutr 4:236–245
46. White JS (2013) Challenging the fructose hypothesis: new perspectives on fructose consumption and metabolism. Adv Nutr 4:246–256
47. Laughlin MR (2014) Normal roles for dietary fructose in carbohydrate metabolism. Nutrients 6:3117–3129
48. Livesey G, Taylor R (2008) Fructose consumption and consequences for glycation, plasma triacylglycerol, and body weight: meta-analyses and meta-regression models of intervention studies. Am J Clin Nutr 88:1419–1437
49. Aeberli I, Hochuli M, Gerber P (2013) Moderate amounts of fructose consumption impair insulin sensitivity in healthy young men. A randomized controlled trial. Diabetes Care 36:150–156
50. Valluru R, Van den Ende W (2008) Plant fructans in stress environments: emerging concepts and future prospects. J Exp Bot 59:2905–2916
51. Di Bartolomeo F, Startek JB, Van den Ende W (2013) Prebiotics to fight diseases: reality or fiction? Phytother Res 27:1457–1473
52. López MG, Urías-Silvas JE (2007) Agave fructans as prebiotics. Recent Advances in Fructooligosaccharides. Eds Shiomi, N., Benkeblia, N. and Onodera. Pp 297–310
53. Tamura K, Kawakami A, Sanada Y, Tase K, Komatsu T, Yoshida M (2009) Cloning and functional analysis of a fructosyltransferase cDNA for synthesis of highly polymerized levans in timothy (Phleum pratense L.). J Exp Bot 60:893–905
54. Incoll, LD, Bonnett GD (1993). The occurrence of fructan in food plants. In: Inulin and Inulin-containing Crops. Ed. A Fuchs. Pp 309–322
55. Lammens W, Le Roy K, Schroeven L, Van Laere A, Rabijns A, Van den Ende W (2009) Structural insights into glycoside hydrolase family 32 and 68 enzymes: functional implications. J Exp Bot 60:727–740
56. Delgado GTC, da Silva Cunha Tamashiro WM, Maróstica MRJ, Pastore GM (2013) Yacon (Smallanthus sonchifolius): a functional food. Plant Foods Hum Nutr 68:222–228
57. Kelly G (2008) Inulin-type prebiotics—a review: part 1. Alter Med Rev 13:315–329
58. Peshev D, Van den Ende W (2014) Fructans: prebiotics and immunomodulators. J Funct Foods 8:384–357
59. Van Loo J, Coussement P, De Leenheer L, Hoebregs H, Smits G (1995) On the presence of inulin and oligofructose as natural ingredients in the Western diet. Crit Rev Food Sci Nutr 35:525–552
60. Allsopp P, Possemiers S, Campbell D, Oyarzábal IS, Gill C, Rowland I (2013) An exploratory study into the putative prebiotic activity of fructans isolated from Agave angustifolia and the associated anticancer activity. Anaerobe 22:38–44
61. Tarini J, Wolever TMS (2010) The fermentable fibre inulin increases postprandial serum short-chain fatty acids and reduces free-fatty acids and ghrelin in healthy subjects. Appl Physiol Nutr Metab 35:9–16
62. Kleessen B, Sykura B, Zunft HJ, Blaut M (1997) Effects of inulin and lactose on faecal microflora, microbial activity and bowel habit in elderly constipated persons. Am J Clin Nutr 65:1397–1402
63. Rumessen JJ, Bode S, Hamberg O, Hoyer EG (1990) Fructans of Jerusalem artichoke: intestinal transport, absorption, fermentation and influence on blood glucose, insulin and C-peptide responses in healthy subjects. Am J Clin Nutr 52:675–680
64. Scholz-Ahrens KE, Schrezenmeir J (2007) Inulin and oligofructose and mineral metabolism: the evidence from animal trials. J Nutr 137:2513S
65. Rendon-Huerta JA, Juarez-Flores B, Pinos-Rodriguez JM, Aguirre-Rivera JR, Delgado-Portales RE (2012) Effect of different sources of fructans on body weight, blood metabolites and fecal bacteria in normal and obese non-diabetic and diabetic rats. Plant Foods Hum Nutr 67:64–70
66. Sauer J, Richter KK, Pool-Zobel BL (2007) Physiological concentrations of butyrate favourably modulates genes of oxidative and metabolic stress in primary human colon cells. J Nutr Biochem 18:736–745
67. Vogt L, Ramasamy U, Meyer D, Pullens G, Venema K, Faas MM, Schols HA, de Vos P (2013) Immune modulation by different types of β2 → 1-fructans is toll-like receptor dependent. Plos ONE 8:7
68. Ortega-Gonzales M, Molina Santiago C, Lopez Posadas R, Pacheco D (2014) Fructooligosacharides reduce Pseudomonas aeruginosa PAO1 pathogenicity through distinct mechanisms. Plos ONE 9:1
69. Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, Katan MB, van der Meer R (2006) Dietary fructooligosaccharides affect intestinal barrier function in healthy men. J Nutr 136:70–74
70. Keunen E, Peshev D, Vangronsveld J, Van den Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress. Extending the traditional concept. Plant Cell Environ 36:1242–1255
71. Van den Ende W, Peshev D, De Gara L (2011) Disease prevention by natural antioxidants and prebiotics acting as ROS scavengers in the gastrointestinal tract. Trends Food Sci Technol 22:689–697
72. Pasqualetti V, Altomare A, Guarino MPL, Locato V, Cocca S, Cimini S, Palma R, Alloni R, De Gara L, Cicala L (2014) Antioxidant activity of inulin and its role in the prevention of human colonic muscle cell impairment induced by lipopolysaccharide mucosal exposure. Plos ONE 9, e9803
73. Arroyo DS, Gaviglio EA, Peralta Ramos JM, Bussi C, Rodriguez-Galan MC, Irribaren P (2014) Autophagy in inflammation, infection, neurodegeneration and cancer. Int Immunopharmacol 18:55–65
74. Van den Ende W (2013) Multifunctional fructans and raffinose family oligosaccharides. Front Plant Sci 4:247
75. Viollet B, Foretz M, Guigas B, Horman S, Dentin R, Bertrand L, Hue L (2006) Activation of AMP-activated protein kinase in the liver: a new strategy for the management of metabolic hepatic disorders. J Physiol 574:41–53
76. Kroemer G, Mariño G, Levine B (2010) Autophagy and the integrated stress response. Mol Cell 40:280–293
77. Peng L, Li Z, Green RS, Holzman IR, Lin J (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 139:1619–1625
78. Eiwegger T, Stahl B, Haidl P, Schmitt J, Boehm G, Dehlink E, Urbanek R, Szepfalusi Z (2010) Prebiotic oligosaccharides: in vitro evidence for gastrointestinal epithelial transfer and immunomodulatory properties. Pediatr Allergy Immunol 21:1179–1188
79. Higuchi T, Nishikawa J, Inoue H (2015) Sucrose induces vesicle accumulation and autophagy. J Cell Biochem 116:609–617
80. Kang Y-L, Saleem MA, Chan KW, Yung BY-M, Law HK-W (2014) Trehalose, an mTOR independent autophagy inducer, alleviates human podocyte injury after puromycin aminonucleoside treatment. PLoS ONE 9, e113520
81. Giordano S, Darley-Ismar V, Zhang J (2014) Autophagy as an essential cellular antioxidant pathway in neurodegenerative disease. Redox Biol 2:82–90