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Gut fat signaling and appetite control with special emphasis on the effect of thylakoids from spinach on eating behavior

International Journal of Obesity volume 39, pages 1679–1688 (2015)Cite this article

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Abstract

The metabolic controls of eating are embedded in a neural system that permits an interaction with the environment. The result is an integrated adaptive response that coordinates the internal milieu with the prevailing environment. Securing adequate amounts of fat and optimizing its storage and use has an evolutionary basis. By generating neuronal and endocrine feedback signals, behavior and metabolism could then adapt to fluctuations in food availability. However, in modern society, foods that appeal to the palate are neither in shortage nor are they difficult to procure. These foods can activate brain reward circuitry beyond their evolved ‘survival advantage’ limits. Many foods high in fat invoke an undeniably pleasurable sensation and could excessively stimulate the brain’s reward pathways leading to overeating. However, the high appeal and potential for being eaten in excess notwithstanding, fat has the added distinction of inducing powerful signals in the gut that are transduced to the brain and result in the regulation of appetite. Fatty acids are sensed by G-protein-coupled receptors on enteroendocrine cells which trigger the release of peptides involved in appetite regulation. Lipid sensing may also occur through the fatty acid translocase, CD-36, on enterocytes. Additionally, fat can activate dopaminergic systems affecting reward, to promote an inhibition over eating. Prolonging the presence of fats in the gastrointestinal lumen permits the activation of signaling mechanisms. Thylakoids, found within the chloroplasts of plants, are flattened disc-like membranous vesicles in which the light-dependent reactions of photosynthesis occur. By interacting with lipids and delaying fat digestion, thylakoid membranes promote the release of peptides involved in appetite regulation and may influence the reward system. This review explores gut lipid sensing and signaling in the context of appetite regulation. The effects of thylakoid membranes on eating behavior are also reviewed.

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References

  1. Blundell JE, Lawton CL, Cotton JR, Macdiarmid JI . Control of human appetite: implications for the intake of dietary fat. Annu Rev Nutr 1996; 16: 285–319.

    CAS  PubMed  Google Scholar 

  2. Berthoud HR . Metabolic and hedonic drives in the neural control of appetite: who is the boss? Curr Opin Neurobiol 2011; 21: 888–896.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Zheng H, Lenard NR, Shin AC, Berthoud HR . Appetite control and energy balance regulation in the modern world: reward-driven brain overrides repletion signals. Int J Obes (Lond) 2009; 33: S8–S13.

    CAS  Google Scholar 

  4. Berthoud HR, Morrison C . The brain, appetite, and obesity. Annu Rev Psychol 2008; 59: 55–92.

    PubMed  Google Scholar 

  5. Verhagen JV, Engelen L . The neurocognitive bases of human multimodal food perception: sensory integration. Neurosci Biobehav Rev 2006; 30: 613–650.

    PubMed  Google Scholar 

  6. Rolls ET . Taste, olfactory and food texture reward processing in the brain and the control of appetite. Proc Nutr Soc 2012; 71: 488–501.

    PubMed  Google Scholar 

  7. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014; 384: 766–781.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Aarts H, Custers R, Marien H . Preparing and motivating behavior outside of awareness. Science 2008; 319: 1639.

    CAS  PubMed  Google Scholar 

  9. Drewnowski A, Almiron-Roig E . Human perceptions and preferences for fat-rich foods. In: Montmayeur JP, le Coutre J (eds). Fat Detection: Taste, Texture, and Post Ingestive Effects. CRC Press: Boca Raton, Florida, 2010.

    Google Scholar 

  10. Little TJ, Feinle-Bisset C . Effects of dietary fat on appetite and energy intake in health and obesity - Oral and gastrointestinal sensory contributions. Physiol Behav 2011; 104: 613–620.

    CAS  PubMed  Google Scholar 

  11. Pironi L, Stanghellini V, Miglioli M, Corinaldesi R, De Giorgio R, Ruggeri E et al. Fat-induced ileal brake in humans: a dose-dependent phenomenon correlated to the plasma levels of peptide YY. Gastroenterology 1993; 105: 733–739.

    CAS  PubMed  Google Scholar 

  12. Maljaars PW, Peters HP, Mela DJ, Masclee AA . Ileal brake: a sensible food target for appetite control. A review. Physiol Behav 2008; 95: 271–281.

    Article  CAS  PubMed  Google Scholar 

  13. Emek SC, Szilagyi A, Akerlund HE, Albertsson PA, Kohnke R, Holm A et al. A large scale method for preparation of plant thylakoids for use in body weight regulation. Prep Biochem Biotech 2010; 40: 13–27.

    CAS  Google Scholar 

  14. Booth DA . Conditioned satiety in the rat. J Comp Physiol Psych 1972; 81: 457–471.

    CAS  Google Scholar 

  15. Montelius C, Erlandsson D, Vitija E, Stenblom EL, Egecioglu E, Erlanson-Albertsson C . Body weight loss, reduced urge for palatable food and increased release of GLP-1 through daily supplementation with green-plant membranes for three months in overweight women. Appetite 2014; 81: 295–304.

    PubMed  Google Scholar 

  16. Kohnke R, Lindbo A, Larsson T, Lindqvist A, Rayner M, Emek SC et al. Thylakoids promote release of the satiety hormone cholecystokinin while reducing insulin in healthy humans. Scand J Gastroenterol 2009; 44: 712–719.

    CAS  PubMed  Google Scholar 

  17. Duca FA, Yue JT . Fatty acid sensing in the gut and the hypothalamus: in vivo and in vitro perspectives. Mol Cell Endocrinol 2014; 397: 23–33.

    CAS  PubMed  Google Scholar 

  18. Piomelli D . A fatty gut feeling. Trends Endocrinol Metab 2013; 24: 332–341.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Stewart JE, Feinle-Bisset C, Golding M, Delahunty C, Clifton PM, Keast RS . Oral sensitivity to fatty acids, food consumption and BMI in human subjects. Br J Nutr 2010; 104: 145–152.

    CAS  PubMed  Google Scholar 

  20. Mattes RD . Is there a fatty acid taste? Annu Rev Nutr 2009; 29: 305–327.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Liou AP, Lu X, Sei Y, Zhao X, Pechhold S, Carrero RJ et al. The G-protein-coupled receptor GPR40 directly mediates long-chain fatty acid-induced secretion of cholecystokinin. Gastroenterology 2011; 140: 903–912.

    CAS  PubMed  Google Scholar 

  22. Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, Yamada M et al. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 2005; 11: 90–94.

    Article  CAS  PubMed  Google Scholar 

  23. Lan H, Vassileva G, Corona A, Liu L, Baker H, Golovko A et al. GPR119 is required for physiological regulation of glucagon-like peptide-1 secretion but not for metabolic homeostasis. J Endocrinol 2009; 201: 219–230.

    CAS  PubMed  Google Scholar 

  24. Schwartz GJ . Gut fat sensing in the negative feedback control of energy balance—recent advances. Physiol Behav 2011; 104: 621–623.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Zittel TT, De Giorgio R, Sternini C, Raybould HE . Fos protein expression in the nucleus of the solitary tract in response to intestinal nutrients in awake rats. Brain Res 1994; 663: 266–270.

    CAS  PubMed  Google Scholar 

  26. Savastano DM, Hayes MR, Covasa M . Serotonin-type 3 receptors mediate intestinal lipid-induced satiation and Fos-like immunoreactivity in the dorsal hindbrain. Am J Physiol Regul Integr Comp Physiol 2007; 292: R1063–R1070.

    CAS  PubMed  Google Scholar 

  27. Burton-Freeman B, Gietzen DW, Schneeman BO . Cholecystokinin and serotonin receptors in the regulation of fat-induced satiety in rats. Am J Physiol 1999; 276: R429–R434.

    CAS  PubMed  Google Scholar 

  28. Le Foll C, Irani BG, Magnan C, Dunn-Meynell AA, Levin BE . Characteristics and mechanisms of hypothalamic neuronal fatty acid sensing. Am J Physiol Regul Integr Comp Physiol 2009; 297: R655–R664.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Schwartz GJ, Fu J, Astarita G, Li X, Gaetani S, Campolongo P et al. The lipid messenger OEA links dietary fat intake to satiety. Cell Metab 2008; 8: 281–288.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Rodriguez de Fonseca F, Navarro M, Gomez R, Escuredo L, Nava F, Fu J et al. An anorexic lipid mediator regulated by feeding. Nature 2001; 414: 209–212.

    CAS  PubMed  Google Scholar 

  31. Fu J, Gaetani S, Oveisi F, Lo Verme J, Serrano A, Rodriguez De Fonseca F et al. Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-alpha. Nature 2003; 425: 90–93.

    CAS  PubMed  Google Scholar 

  32. Tellez LA, Medina S, Han W, Ferreira JG, Licona-Limon P, Ren X et al. A gut lipid messenger links excess dietary fat to dopamine deficiency. Science 2013; 341: 800–802.

    CAS  PubMed  Google Scholar 

  33. Glatzle J, Darcel N, Rechs AJ, Kalogeris TJ, Tso P, Raybould HE . Apolipoprotein A-IV stimulates duodenal vagal afferent activity to inhibit gastric motility via a CCK1 pathway. Am J Physiol Regul Integr Comp Physiol 2004; 287: R354–R359.

    CAS  PubMed  Google Scholar 

  34. Berridge KC, Robinson TE . What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 1998; 28: 309–369.

    CAS  PubMed  Google Scholar 

  35. Schultz W . Updating dopamine reward signals. Curr Opin Neurobiol 2013; 23: 229–238.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Kenny PJ, Voren G, Johnson PM . Dopamine D2 receptors and striatopallidal transmission in addiction and obesity. Curr Opin Neurobiol 2013; 23: 535–538.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Stice E, Spoor S, Bohon C, Small DM . Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 2008; 322: 449–452.

    CAS  PubMed  Google Scholar 

  38. Kleberg K, Jacobsen AK, Ferreira JG, Windelov JA, Rehfeld JF, Holst JJ et al. Sensing of triacylglycerol in the gut: different mechanisms for fatty acids and 2-monoacylglycerol. J Physiol 2015; 593: 2097–2109.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Blundell JE, Levin F, King NA, Barkeling B, Gustafsson T, Hellstrom PM et al. Overconsumption and obesity: peptides and susceptibility to weight gain. Regul Pept 2008; 149: 32–38.

    CAS  PubMed  Google Scholar 

  40. Kojima M, Kangawa K . Ghrelin: structure and function. Physiol Rev 2005; 85: 495–522.

    CAS  PubMed  Google Scholar 

  41. Briggs DI, Enriori PJ, Lemus MB, Cowley MA, Andrews ZB . Diet-induced obesity causes ghrelin resistance in arcuate NPY/AgRP neurons. Endocrinology 2010; 151: 4745–4755.

    CAS  PubMed  Google Scholar 

  42. Kirchner H, Gutierrez JA, Solenberg PJ, Pfluger PT, Czyzyk TA, Willency JA et al. GOAT links dietary lipids with the endocrine control of energy balance. Nat Med 2009; 15: 741–745.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Dickson SL, Egecioglu E, Landgren S, Skibicka KP, Engel JA, Jerlhag E . The role of the central ghrelin system in reward from food and chemical drugs. Mol Cell Endocrinol 2011; 340: 80–87.

    CAS  PubMed  Google Scholar 

  44. Perello M, Sakata I, Birnbaum S, Chuang JC, Osborne-Lawrence S, Rovinsky SA et al. Ghrelin increases the rewarding value of high-fat diet in an orexin-dependent manner. Biol Psychiatry 2010; 67: 880–886.

    CAS  PubMed  Google Scholar 

  45. Moran-Ramos S, Tovar AR, Torres N . Diet: friend or foe of enteroendocrine cells—how it interacts with enteroendocrine cells. Adv Nutr 2012; 3: 8–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Blackshaw LA, Grundy D . Effects of cholecystokinin (CCK-8) on two classes of gastroduodenal vagal afferent fibre. J Auton Nerv Syst 1990; 31: 191–201.

    CAS  PubMed  Google Scholar 

  47. Figlewicz DP, Nadzan AM, Sipols AJ, Green PK, Liddle RA, Porte D Jr et al. Intraventricular CCK-8 reduces single meal size in the baboon by interaction with type-A CCK receptors. Am J Physiol 1992; 263: R863–R867.

    CAS  PubMed  Google Scholar 

  48. Pi-Sunyer X, Kissileff HR, Thornton J, Smith GP . C-terminal octapeptide of cholecystokinin decreases food intake in obese men. Physiol Behav 1982; 29: 627–630.

    CAS  PubMed  Google Scholar 

  49. Muurahainen N, Kissileff HR, Derogatis AJ, Pi-Sunyer FX . Effects of cholecystokinin-octapeptide (CCK-8) on food intake and gastric emptying in man. Physiol Behav 1988; 44: 645–649.

    CAS  PubMed  Google Scholar 

  50. Blevins JE, Stanley BG, Reidelberger RD . Brain regions where cholecystokinin suppresses feeding in rats. Brain Res 2000; 860: 1–10.

    CAS  PubMed  Google Scholar 

  51. Zhang J, Ritter RC . Circulating GLP-1 and CCK-8 reduce food intake by capsaicin-insensitive, nonvagal mechanisms. Am J Physiol Regul Integr Comp Physiol 2012; 302: R264–R273.

    CAS  PubMed  Google Scholar 

  52. Lee J, Martin E, Paulino G, de Lartigue G, Raybould HE . Effect of ghrelin receptor antagonist on meal patterns in cholecystokinin type 1 receptor null mice. Physiol Behav 2011; 103: 181–187.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Beglinger S, Drewe J, Schirra J, Goke B, D'Amato M, Beglinger C . Role of fat hydrolysis in regulating glucagon-like Peptide-1 secretion. J Clin Endocrinol Metab 2010; 95: 879–886.

    CAS  PubMed  Google Scholar 

  54. Dockray GJ . Gastrointestinal hormones and the dialogue between gut and brain. J Physiol 2014; 592: 2927–2941.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Chelikani PK, Haver AC, Reidelberger RD . Intravenous infusion of peptide YY(3-36) potently inhibits food intake in rats. Endocrinology 2005; 146: 879–888.

    CAS  PubMed  Google Scholar 

  56. Degen L, Oesch S, Casanova M, Graf S, Ketterer S, Drewe J et al. Effect of peptide YY3-36 on food intake in humans. Gastroenterology 2005; 129: 1430–1436.

    CAS  PubMed  Google Scholar 

  57. Tschop M, Castaneda TR, Joost HG, Thone-Reineke C, Ortmann S, Klaus S et al. Physiology: does gut hormone PYY3-36 decrease food intake in rodents? Nature 2004; 430: 1 p following 165; discussion 2 p following 65.

    PubMed  Google Scholar 

  58. Karhunen LJ, Juvonen KR, Huotari A, Purhonen AK, Herzig KH . Effect of protein, fat, carbohydrate and fibre on gastrointestinal peptide release in humans. Regul Pept 2008; 149: 70–78.

    CAS  PubMed  Google Scholar 

  59. Essah PA, Levy JR, Sistrun SN, Kelly SM, Nestler JE . Effect of macronutrient composition on postprandial peptide YY levels. J Clin Endocrinol Metab 2007; 92: 4052–4055.

    CAS  PubMed  Google Scholar 

  60. Batterham RL, ffytche DH, Rosenthal JM, Zelaya FO, Barker GJ, Withers DJ et al. PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans. Nature 2007; 450: 106–109.

    CAS  PubMed  Google Scholar 

  61. Hayes MR, De Jonghe BC, Kanoski SE . Role of the glucagon-like-peptide-1 receptor in the control of energy balance. Physiol Behav 2010; 100: 503–510.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Dickson SL, Shirazi RH, Hansson C, Bergquist F, Nissbrandt H, Skibicka KP . The glucagon-like peptide 1 (GLP-1) analogue, exendin-4, decreases the rewarding value of food: a new role for mesolimbic GLP-1 receptors. J Neurosci 2012; 32: 4812–4820.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Dossat AM, Lilly N, Kay K, Williams DL . Glucagon-like peptide 1 receptors in nucleus accumbens affect food intake. J Neurosci 2011; 31: 14453–14457.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Holst JJ . Incretin hormones and the satiation signal. Int J Obes (Lond) 2013; 37: 1161–1168.

    CAS  Google Scholar 

  65. Tovar J, Melito C, Herrera E, Rascon A, Perez E . Resistant starch formation does not parallel syneresis tendency in different starch gels. Food Chemistry 2002; 76: 455–459.

    CAS  Google Scholar 

  66. Dakin CL, Small CJ, Batterham RL, Neary NM, Cohen MA, Patterson M et al. Peripheral oxyntomodulin reduces food intake and body weight gain in rats. Endocrinology 2004; 145: 2687–2695.

    CAS  PubMed  Google Scholar 

  67. Dakin CL, Small CJ, Park AJ, Seth A, Ghatei MA, Bloom SR . Repeated ICV administration of oxyntomodulin causes a greater reduction in body weight gain than in pair-fed rats. Am J Physiol Endocrinol Metab 2002; 283: E1173–E1177.

    CAS  PubMed  Google Scholar 

  68. Cohen MA, Ellis SM, Le Roux CW, Batterham RL, Park A, Patterson M et al. Oxyntomodulin suppresses appetite and reduces food intake in humans. J Clin Endocrinol Metab 2003; 88: 4696–4701.

    CAS  PubMed  Google Scholar 

  69. McGavigan AK, Murphy KG . Gut hormones: the future of obesity treatment? Br J Clin Pharmacol 2012; 74: 911–919.

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Sainsbury A, Shi YC, Zhang L, Aljanova A, Lin Z, Nguyen AD et al. Y4 receptors and pancreatic polypeptide regulate food intake via hypothalamic orexin and brain-derived neurotropic factor dependent pathways. Neuropeptides 2010; 44: 261–268.

    CAS  PubMed  Google Scholar 

  71. Jesudason DR, Monteiro MP, McGowan BM, Neary NM, Park AJ, Philippou E et al. Low-dose pancreatic polypeptide inhibits food intake in man. Br J Nutr 2007; 97: 426–429.

    CAS  PubMed  Google Scholar 

  72. Rayner M, Ljusberg H, Emek SC, Sellman E, Erlanson-Albertsson C, Albertsson PA . Chloroplast thylakoid membrane-stabilised emulsions. J Sci Food Agric 2011; 91: 315–321.

    CAS  PubMed  Google Scholar 

  73. Okada S, York DA, Bray GA, Erlanson-Albertsson C . Enterostatin (Val-Pro-Asp-Pro-Arg), the activation peptide of procolipase, selectively reduces fat intake. Physiol Behav 1991; 49: 1185–1189.

    CAS  PubMed  Google Scholar 

  74. Mei J, Bowyer RC, Jehanli AM, Patel G, Erlanson-Albertsson C . Identification of enterostatin, the pancreatic procolipase activation peptide in the intestine of rat: effect of CCK-8 and high-fat feeding. Pancreas 1993; 8: 488–493.

    CAS  PubMed  Google Scholar 

  75. Erlanson-Albertsson C, York D . Enterostatin—a peptide regulating fat intake. Obes Res 1997; 5: 360–372.

    CAS  PubMed  Google Scholar 

  76. York DA, Lin L, Thomas SR, Braymer HD, Park M . Procolipase gene expression in the rat brain: source of endogenous enterostatin production in the brain. Brain Res 2006; 1087: 52–59.

    CAS  PubMed  Google Scholar 

  77. Okada S, York DA, Bray GA . Procolipase mRNA: tissue localization and effects of diet and adrenalectomy. Biochem J 1993; 292: 787–789.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Tian Q, Nagase H, York DA, Bray GA . Vagal-central nervous system interactions modulate the feeding response to peripheral enterostatin. Obes Res 1994; 2: 527–534.

    CAS  PubMed  Google Scholar 

  79. Berger K, Winzell MS, Mei J, Erlanson-Albertsson C . Enterostatin and its target mechanisms during regulation of fat intake. Physiol Behav 2004; 83: 623–630.

    CAS  PubMed  Google Scholar 

  80. Koizumi M, Kimura S . Enterostatin increases extracellular serotonin and dopamine in the lateral hypothalamic area in rats measured by in vivo microdialysis. Neurosci lett 2002; 320: 96–98.

    CAS  PubMed  Google Scholar 

  81. York DA, Teng L, Park-York M . Effects of dietary fat and enterostatin on dopamine and 5-hydroxytrytamine release from rat striatal slices. Brain Res 2010; 1349: 48–55.

    CAS  PubMed  Google Scholar 

  82. Rossner S, Barkeling B, Erlanson-Albertsson C, Larsson P, Wahlin-Boll E . Intravenous enterostatin does not affect single meal food intake in man. Appetite 1995; 24: 37–42.

    CAS  PubMed  Google Scholar 

  83. Kovacs EM, Lejeune MP, Westerterp-Plantenga MS . The effects of enterostatin intake on food intake and energy expenditure. Br J Nutr 2003; 90: 207–214.

    CAS  PubMed  Google Scholar 

  84. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG . Central nervous system control of food intake. Nature 2000; 404: 661–671.

    CAS  PubMed  Google Scholar 

  85. de Graaf C, Blom WA, Smeets PA, Stafleu A, Hendriks HF . Biomarkers of satiation and satiety. Am J Clin Nutr 2004; 79: 946–961.

    CAS  PubMed  Google Scholar 

  86. Kanoski SE, Hayes MR, Greenwald HS, Fortin SM, Gianessi CA, Gilbert JR et al. Hippocampal leptin signaling reduces food intake and modulates food-related memory processing. Neuropsychopharmacol 2011; 36: 1859–1870.

    CAS  Google Scholar 

  87. Mustardy L, Buttle K, Steinbach G, Garab G . The three-dimensional network of the thylakoid membranes in plants: quasihelical model of the granum-stroma assembly. Plant cell 2008; 20: 2552–2557.

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Albertsson P . A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 2001; 6: 349–358.

    CAS  PubMed  Google Scholar 

  89. Emek SC, Akerlund HE, Clausen M, Ohlsson L, Westrom B, Erlanson-Albertsson C et al. Pigments protect the light harvesting proteins of chloroplast thylakoid membranes against digestion by gastrointestinal proteases. Food Hydrocolloid 2011; 25: 1618–1626.

    CAS  Google Scholar 

  90. Schmid VH . Light-harvesting complexes of vascular plants. Cell Mol Life Sci 2008; 65: 3619–3639.

    CAS  PubMed  Google Scholar 

  91. Pali T, Garab G, Horvath LI, Kota Z . Functional significance of the lipid-protein interface in photosynthetic membranes. Cell Mol Life Sci 2003; 60: 1591–1606.

    CAS  PubMed  Google Scholar 

  92. Chu BS, Rich GT, Ridout MJ, Faulks RM, Wickham MS, Wilde PJ . Modulating pancreatic lipase activity with galactolipids: effects of emulsion interfacial composition. Langmuir 2009; 25: 9352–9360.

    CAS  PubMed  Google Scholar 

  93. Borgstrom B . On the interactions between pancreatic lipase and colipase and the substrate, and the importance of bile salts. J Lipid Res 1975; 16: 411–417.

    CAS  PubMed  Google Scholar 

  94. Chu BS, Gunning AP, Rich GT, Ridout MJ, Faulks RM, Wickham MS et al. Adsorption of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol and dipalmitoylphosphatidylcholine monolayers. Langmuir 2010; 26: 9782–9793.

    CAS  PubMed  Google Scholar 

  95. Albertsson PA, Kohnke R, Emek SC, Mei J, Rehfeld JF, Akerlund HE et al. Chloroplast membranes retard fat digestion and induce satiety: effect of biological membranes on pancreatic lipase/co-lipase. Biochem J 2007; 401: 727–733.

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Emek SC, Akerlund HE, Erlanson-Albertsson C, Albertsson PA . Pancreatic lipase-colipase binds strongly to the thylakoid membrane surface. J Sci Food Agric 2013; 93: 2254–2258.

    CAS  PubMed  Google Scholar 

  97. Position of the American Dietetic association: fat replacers. J Am Diet Assoc 2005; 105: 266–275.

  98. Montelius C, Osman N, Westrom B, Ahrne S, Molin G, Albertsson PA et al. Feeding spinach thylakoids to rats modulates the gut microbiota, decreases food intake and affects the insulin response. J Nutr Sci 2013; 2: e20.

    PubMed  PubMed Central  Google Scholar 

  99. Goedecke JH, Barsdorf M, Beglinger C, Levitt NS, Lambert EV . Effects of a lipase inhibitor (Orlistat) on cholecystokinin and appetite in response to a high-fat meal. Int J Obes Relat Metab Disord 2003; 27: 1479–1485.

    CAS  PubMed  Google Scholar 

  100. Kohnke R, Lindqvist A, Goransson N, Emek SC, Albertsson PA, Rehfeld JF et al. Thylakoids suppress appetite by increasing cholecystokinin resulting in lower food intake and body weight in high-fat fed mice. Phytother Res 2009; 23: 1778–1783.

    PubMed  Google Scholar 

  101. Montelius C, Szwiec K, Kardas M, Lozinska L, Erlanson-Albertsson C, Pierzynowski S et al. Dietary thylakoids suppress blood glucose and modulate appetite-regulating hormones in pigs exposed to oral glucose tolerance test. Clin Nutr 2014; 33: 1122–1126.

    CAS  PubMed  Google Scholar 

  102. Kohnke R, Svensson L, Piedra JLV, Pierzynowski SG, Westrom B, Erlanson-Albertsson C . Feeding appetite suppressing thylakoids to pigs alters pancreatic lipase/colipase secretion. Livest Sci 2010; 134: 68–71.

    Google Scholar 

  103. Stenblom EL, Montelius C, Ostbring K, Hakansson M, Nilsson S, Rehfeld JF et al. Supplementation by thylakoids to a high carbohydrate meal decreases feelings of hunger, elevates CCK levels and prevents postprandial hypoglycaemia in overweight women. Appetite 2013; 68: 118–123.

    PubMed  Google Scholar 

  104. Stenblom EL, Montelius C, Erlandsson D, Skarping L, Fransson M, Egecioglu E et al. Decreased urge for palatable food after a two-month dietary intervention with green-plant membranes in overweight women. Obes Weight Loss Ther 2014; 4: 238.

    Google Scholar 

  105. Van Gaal LF, Mertens IL, De Block CE . Mechanisms linking obesity with cardiovascular disease. Nature 2006; 444: 875–880.

    CAS  PubMed  Google Scholar 

  106. Frankenfield D, Roth-Yousey L, Compher C . Comparison of predictive equations for resting metabolic rate in healthy nonobese and obese adults: a systematic review. J Am Diet Assoc 2005; 105: 775–789.

    PubMed  Google Scholar 

  107. Siervo M, Bertoli S, Battezzati A, Wells JC, Lara J, Ferraris C et al. Accuracy of predictive equations for the measurement of resting energy expenditure in older subjects. Clin Nutr 2014; 33: 613–619.

    CAS  PubMed  Google Scholar 

  108. Stenblom EL, Egecioglu E, Landin-Olsson M, Erlanson-Albertsson C . Consumption of thylakoid-rich spinach extract reduces hunger, increases satiety and reduces cravings for palatable food in overweight women. Appetite 2015; 91: 209–219.

    PubMed  Google Scholar 

  109. Rebello CJ, Chu J, Beyl R, Edwall D, Erlanson-Albertsson C, Greenway FL . Acute effects of a spinach extract rich in thylakoids on satiety: a randomized controlled crossover trial. J Am Coll Nutr e-pub ahead of print 1 June 2015; 1–8.

  110. Finlayson G, King N, Blundell JE . Is it possible to dissociate 'liking' and 'wanting' for foods in humans? A novel experimental procedure. Physiol Behav 2007; 90: 36–42.

    CAS  PubMed  Google Scholar 

  111. Pelchat ML . Food cravings in young and elderly adults. Appetite 1997; 28: 103–113.

    CAS  PubMed  Google Scholar 

  112. Weingarten HP, Elston D . Food cravings in a college population. Appetite 1991; 17: 167–175.

    CAS  PubMed  Google Scholar 

  113. Berridge KC, Robinson TE, Aldridge JW . Dissecting components of reward: 'liking', 'wanting', and learning. Curr Opin Pharmacol 2009; 9: 65–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Moran TH, Kinzig KP . Gastrointestinal satiety signals II. Cholecystokinin. Am J Physiol Gastrointest Liver Physiol 2004; 286: G183–G188.

    CAS  PubMed  Google Scholar 

  115. Davis C . Evolutionary and neuropsychological perspectives on addictive behaviors and addictive substances: relevance to the "food addiction" construct. Subst Abuse Rehabil 2014; 5: 129–137.

    PubMed  PubMed Central  Google Scholar 

  116. Badman MK, Flier JS . The gut and energy balance: visceral allies in the obesity wars. Science 2005; 307: 1909–1914.

    CAS  PubMed  Google Scholar 

  117. Schneeberger M, Gomis R, Claret M . Hypothalamic and brainstem neuronal circuits controlling homeostatic energy balance. J Endocrinol 2014; 220: T25–T46.

    CAS  PubMed  Google Scholar 

  118. Albertsson P . A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 2001; 6: 349–358.

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work is based in part upon work that was supported by the National Institute of Food and Agriculture, US Department of Agriculture, under award number from the USDA Hatch Project LAB 94209.

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Authors and Affiliations

  1. School of Nutrition and Food Sciences, Louisiana State University, Baton Rouge, LA, USA

    C J Rebello

  2. Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, LA, USA

    C J Rebello & F L Greenway

  3. Louisiana State University Agricultural Center, Baton Rouge, LA, USA

    C E O'Neil

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  1. C J Rebello
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  2. C E O'Neil
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  3. F L Greenway
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Correspondence to F L Greenway.

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Any opinions, findings, conclusions or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the US Department of Agriculture.

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Rebello, C., O'Neil, C. & Greenway, F. Gut fat signaling and appetite control with special emphasis on the effect of thylakoids from spinach on eating behavior. Int J Obes 39, 1679–1688 (2015). https://doi.org/10.1038/ijo.2015.142

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  • DOI: https://doi.org/10.1038/ijo.2015.142

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