Oral Administration of Apple Procyanidins Ameliorates Insulin Resistance via Suppression of Pro-Inflammatory Cytokine Expression in Liver of Diabetic ob/ob Mice

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 46, 2016, Pages 8857-8865

  Ogura, Kasane ^a   Ogura, Masahito ^a   Shoji, Toshihiko ^b   Sato, Yuichi ^a   Tahara, Yumiko ^a   Yamano, Gen ^a   Sato, Hiroki ^a   Sugizaki, Kazu ^a   Fujita, Naotaka ^a   Tatsuoka, Hisato ^a   Usui, Ryota ^a   Mukai, Eri ^c   Fujimoto, Shimpei ^d   Inagaki, Nobuya ^a   Nagashima, Kazuaki ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF FRUIT TREE SCIENCE   (Japan)

^c RITSUMEIKAN UNIVERSITY   (Japan)

^d KOCHI UNIVERSITY   (Japan)

Author keywords

apple procyanidins; inflammation; insulin resistance; ob ob mouse

Indexed keywords

BIOCHEMISTRY; FLAVONOIDS; FRUITS; GLUCOSE; INSULIN; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY;

ANTI-INFLAMMATORY EFFECTS; C-JUN N-TERMINAL KINASE; HEPATIC GLUCONEOGENESIS; INFLAMMATION; INSULIN RESISTANCE; OB/OB MOUSE; PANCREATIC BETA CELLS; PROCYANIDINS;

MAMMALS;

BIFLAVONOID; CATECHIN; CYTOKINE; INSULIN; PLANT EXTRACT; PROANTHOCYANIDIN; PROCYANIDIN;

ANIMAL; C57BL MOUSE; CHEMISTRY; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; GENETICS; HUMAN; INSULIN RESISTANCE; LIVER; MALE; MALUS; METABOLISM; MOUSE;

ANIMALS; BIFLAVONOIDS; CATECHIN; CYTOKINES; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN; INSULIN RESISTANCE; LIVER; MALE; MALUS; MICE; MICE, INBRED C57BL; PLANT EXTRACTS; PROANTHOCYANIDINS;

EID: 84999748059     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b03424     Document Type: Article

References (45)

1. Rudich, A.; Tirosh, A.; Potashnik, R.; Hemi, R.; Kanety, H.; Bashan, N. Prolonged oxidative stress impairs insulin-induced GLUT4 translocation in 3T3-L1 adipocytes Diabetes 1998, 47, 1562-1569 10.2337/diabetes.47.10.1562
2. Tiganis, T. Reactive oxygen species and insulin resistance: the good, the bad and the ugly Trends Pharmacol. Sci. 2011, 32, 82-89 10.1016/j.tips.2010.11.006
3. Hung, H. C.; Joshipura, K. J.; Jiang, R.; Hu, F. B.; Hunter, D.; Smith-Warner, S. A.; Colditz, G. A.; Rosner, B.; Spiegelman, D.; Willett, W. C. Fruit and vegetable intake and risk of major chronic disease J. Natl. Cancer Institute. 2004, 96, 1577-1584 10.1093/jnci/djh296
4. Muraki, I.; Imamura, F.; Manson, J. E.; Hu, F. B.; Willett, W. C.; van Dam, R. M.; Sun, Q. Fruit consumption and risk of type 2 diabetes: results from three prospective longitudinal cohort studies BMJ. 2013, 347, f5001 10.1136/bmj.f5001
5. Leontowicz, H.; Gorinstein, S.; Lojek, A.; Leontowicz, M.; Čĺž, M.; Soliva-Fortuny, R.; Park, Y. S.; Jung, S. T.; Trakhtenberg, S.; Martin-Belloso, O. Comparative content of some bioactive compounds in apples, peaches and pears and their influence on lipids and antioxidant capacity in rats J. Nutr. Biochem. 2002, 13, 603-610 10.1016/S0955-2863(02)00206-1
6. Jung, M.; Triebel, S.; Anke, T.; Richling, E.; Erkel, G. Influence of apple polyphenols on inflammatory gene expression Mol. Nutr. Food Res. 2009, 53, 1263-1280 10.1002/mnfr.200800575
7. Lapidot, T.; Walker, M. D.; Kanner, J. Can apple antioxidants inhibit tumor cell proliferation? Generation of H(2)O(2) during interaction of phenolic compounds with cell culture media J. Agric. Food Chem. 2002, 50, 3156-3160 10.1021/jf011522g
8. Shoji, T.; Mutsuga, M.; Nakamura, T.; Kanda, T.; Akiyama, H.; Goda, Y. Isolation and structural elucidation of some procyanidins from apple by low-temperature nuclear magnetic resonance J. Agric. Food Chem. 2003, 51, 3806-3813 10.1021/jf0300184
9. Vayndorf, E. M.; Lee, S. S.; Liu, R. H. Whole apple extracts increase lifespan, healthspan and resistance to stress in Caenorhabditis elegans J. Funct. Foods 2013, 5, 1236-1243
10. Sugiyama, H.; Akazome, Y.; Shoji, T.; Yamaguchi, A.; Yasue, M.; Kanda, T.; Ohtake, Y. Oligomeric procyanidins in apple polyphenol are main active components for inhibition of pancreatic lipase and triglyceride absorption J. Agric. Food Chem. 2007, 55, 4604-4609 10.1021/jf070569k
11. Yoshioka, Y.; Akiyama, H.; Nakano, M.; Shoji, T.; Kanda, T.; Ohtake, Y.; Takita, T.; Matsuda, R.; Maitani, T. Orally administered apple procyanidins protect against experimental inflammatory bowel disease in mice Int. Immunopharmacol. 2008, 8, 1802-1807 10.1016/j.intimp.2008.08.021
12. Yanagida, A.; Kanda, T.; Takahashi, T.; Kamimura, A.; Hamazono, T.; Honda, S. Fractionation of apple procyanidins according to their degree of polymerization by normal-phase high-performance liquid chromatography J. Chromatogr. A 2000, 890, 251-259 10.1016/S0021-9673(00)00614-2
13. Kahn, B. B.; Shulman, G. I.; DeFronzo, R. A.; Cushman, S. W.; Rossetti, L. Normalization of blood glucose in diabetic rats with phlorizin treatment reverses insulin-resistant glucose transport in adipose cells without restoring glucose transporter gene expression J. Clin. Invest. 1991, 87, 561-570 10.1172/JCI115031
14. Bagdas, D.; Etoz, B. C.; Gul, Z.; Ziyanok, S.; Inan, S.; Turacozen, O.; Gul, N. Y.; Topal, A.; Cinkilic, N.; Tas, S.; Ozyigit, M. O.; Gurun, M. S. In vivo systemic chlorogenic acid therapy under diabetic conditions: Wound healing effects and cytotoxicity/genotoxicity profile Food Chem. Toxicol. 2015, 81, 54-61 10.1016/j.fct.2015.04.001
15. Onakpoya, I. J.; Spencer, E. A.; Thompson, M. J.; Heneghan, C. J. The effect of chlorogenic acid on blood pressure: a systematic review and meta-analysis of randomized clinical trials J. Hum. Hypertens. 2015, 29, 77-81 10.1038/jhh.2014.46
16. Robertson, K.; Lu, Y.; De Jesus, K.; Li, B.; Su, Q.; Lund, P. K.; Liu, J. L. A general and islet cell-enriched overexpression of IGF-I results in normal islet cell growth, hypoglycemia, and significant resistance to experimental diabetes Am. J. Physiol Endocrinol Metab. 2008, 294, E928-38 10.1152/ajpendo.00606.2007
17. Konrad, D.; Rudich, A.; Schoenle, E. J. Improved glucose tolerance in mice receiving intraperitoneal transplantation of normal fat tissue Diabetologia 2007, 50, 833-839 10.1007/s00125-007-0596-1
18. Matthews, D. R.; Hosker, J. P.; Rudenski, A. S.; Naylor, B. A.; Treacher, D. F.; Turner, R. C. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man Diabetologia 1985, 28, 412-419 10.1007/BF00280883
19. Mlinar, B.; Marc, J.; Janez, A.; Pfeifer, M. Molecular mechanisms of insulin resistance and associated diseases Clin. Chim. Acta 2007, 375, 20-35 10.1016/j.cca.2006.07.005
20. Fløyel, T.; Brorsson, C.; Nielsen, L. B.; Miani, M.; Bang-Berthelsen, C. H.; Friedrichsen, M.; Overgaard, A. J.; Berchtold, L. A.; Wiberg, A.; Poulsen, P.; Hansen, L.; Rosinger, S.; Boehm, B. O.; Ram, R.; Nguyen, Q.; Mehta, M.; Morahan, G.; Concannon, P.; Bergholdt, R.; Nielsen, J. H.; Reinheckel, T.; von Herrath, M.; Vaag, A.; Eizirik, D. L.; Mortensen, H. B.; Størling, J.; Pociot, F. CTSH regulates β-cell function and disease progression in newly diagnosed type 1 diabetes patients Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 10305-10310 10.1073/pnas.1402571111
21. Nasteska, D.; Harada, N.; Suzuki, K.; Yamane, S.; Hamasaki, A.; Joo, E.; Iwasaki, K.; Shibue, K.; Harada, T.; Inagaki, N. Chronic reduction of GIP secretion alleviates obesity and insulin resistance under high-fat diet conditions Diabetes 2014, 63, 2332-2343 10.2337/db13-1563
22. Kuroda, N.; Inoue, K.; Ikeda, T.; Hara, Y.; Wake, K.; Sato, T. Apoptotic response through a high mobility box 1 protein-dependent mechanism in LPS/GalN-induced mouse liver failure and glycyrrhizin-mediated inhibition PLoS One 2014, 9, e92884 10.1371/journal.pone.0092884
23. Folch, J.; Lees, M.; Sloane Stanley, G. H. A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 1957, 226, 497-509
24. Mezza, T.; Muscogiuri, G.; Sorice, G. P.; Clemente, G.; Hu, J.; Pontecorvi, A.; Holst, J. J.; Giaccari, A.; Kulkarni, R. N. Insulin resistance alters islet morphology in nondiabetic humans Diabetes 2014, 63, 994-1007 10.2337/db13-1013
25. Wahren, J.; Ekberg, K. Splanchnic regulation of glucose production Annu. Rev. Nutr. 2007, 27, 329-345 10.1146/annurev.nutr.27.061406.093806
26. Standaert, M. L.; Sajan, M. P.; Miura, A.; Kanoh, Y.; Chen, H. C.; Farese, R. V.; Farese, R. V., Jr. Insulin-induced activation of atypical protein kinase C, but not protein kinase B, is maintained in diabetic (ob/ob and Goto-Kakazaki) liver. Contrasting insulin signaling patterns in liver versus muscle define phenotypes of type 2 diabetic and high fat-induced insulin-resistant states J. Biol. Chem. 2004, 279, 24929-24934 10.1074/jbc.M402440200
27. Samuel, V. T.; Liu, Z. X.; Qu, X.; Elder, B. D.; Bilz, S.; Befroy, D.; Romanelli, A. J.; Shulman, G. I. Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease J. Biol. Chem. 2004, 279, 32345-32353 10.1074/jbc.M313478200
28. Baratta, J. L.; Ngo, A.; Lopez, B.; Kasabwalla, N.; Longmuir, K. J.; Robertson, R. T. Cellular organization of normal mouse liver: a histological, quantitative immunocytochemical, and fine structural analysis Histochem. Cell Biol. 2009, 131, 713-726 10.1007/s00418-009-0577-1
29. Schwabe, R. F.; Brenner, D. A. Mechanisms of Liver Injury. I. TNF-alpha-induced liver injury: role of IKK, JNK, and ROS pathways Am. J. Physiol. Gastroint. Liver Physiol. 2006, 290, G583-G589 10.1152/ajpgi.00422.2005
30. Jimenez-Gomez, Y.; Mattison, J. A.; Pearson, K. J.; Martin-Montalvo, A.; Palacios, H. H.; Sossong, A. M.; Ward, T. M.; Younts, C. M.; Lewis, K.; Allard, J. S.; Longo, D. L.; Belman, J. P.; Malagon, M. M.; Navas, P.; Sanghvi, M.; Moaddel, R.; Tilmont, E. M.; Herbert, R. L.; Morrell, C. H.; Egan, J. M.; Baur, J. A.; Ferrucci, L.; Bogan, J. S.; Bernier, M.; de Cabo, R. Resveratrol improves adipose insulin signaling and reduces the inflammatory response in adipose tissue of rhesus monkeys on high-fat, high-sugar diet Cell Metab. 2013, 18, 533-545 10.1016/j.cmet.2013.09.004
31. de Luca, C.; Olefsky, J. M. Inflammation and insulin resistance FEBS Lett. 2008, 582, 97-105 10.1016/j.febslet.2007.11.057
32. Akiyama, H.; Sato, Y.; Watanabe, T.; Nagaoka, M. H.; Yoshioka, Y.; Shoji, T.; Kanda, T.; Yamada, K.; Totsuka, M.; Teshima, R.; Sawada, J.; Goda, Y.; Maitani, T. Dietary unripe apple polyphenol inhibits the development of food allergies in murine models FEBS Lett. 2005, 579, 4485-4491 10.1016/j.febslet.2005.07.019
33. Qin, B.; Panickar, K. S.; Anderson, R. A. Cinnamon: potential role in the prevention of insulin resistance, metabolic syndrome, and type 2 diabetes J. Diabetes Sci. Technol. 2010, 4, 685-693 10.1177/193229681000400324
34. Lee, Y. A.; Kim, Y. J.; Cho, E. J.; Yokozawa, T. Ameliorative effects of proanthocyanidin on oxidative stress and inflammation in streptozotocin-induced diabetic rats J. Agric. Food Chem. 2007, 55, 9395-9400 10.1021/jf071523u
35. Yamashita, Y.; Okabe, M.; Natsume, M.; Ashida, H. Cinnamtannin A2, a tetrameric procyanidin, increases GLP-1 and insulin secretion in mice Biosci., Biotechnol., Biochem. 2013, 77, 888-891 10.1271/bbb.130095
36. Perseghin, G. Viewpoints on the way to a consensus session: where does insulin resistance start? The liver Diabetes Care 2009, 32 (Suppl. 2) S164-S167 10.2337/dc09-S303
37. Dixon, L. J.; Barnes, M.; Tang, H.; Pritchard, M. T.; Nagy, L. E. Kupffer cells in the liver Comprehensive Physiol. 2013, 3, 785-797 10.1002/cphy.c120026
38. Michelotti, G. A.; Machado, M. V.; Diehl, A. M. NAFLD, NASH and liver cancer Nat. Rev. Gastroenterol. Hepatol. 2013, 10, 656-665 10.1038/nrgastro.2013.183
39. Luedde, T.; Schwabe, R. F. NF-kappaB in the liver - linking injury, fibrosis and hepatocellular carcinoma Nat. Rev. Gastroenterol. Hepatol. 2011, 8, 108-118 10.1038/nrgastro.2010.213
40. Ley, R. E.; Backhed, F.; Turnbaugh, P.; Lozupone, C. A.; Knight, R. D.; Gordon, J. I. Obesity alters gut microbial ecology Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 11070-11075 10.1073/pnas.0504978102
41. Brun, P.; Castagliuolo, I.; Di Leo, V.; Buda, A.; Pinzani, M.; Palu, G.; Martines, D. Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis Am. J. Physiol. Gastroint. Liver Physiol. 2006, 292, G518-G525 10.1152/ajpgi.00024.2006
42. Ou, K.; Sarnoski, P.; Schneider, K. R.; Song, K.; Khoo, C.; Gu, L. Microbial catabolism of procyanidins by human gut microbiota Mol. Nutr. Food Res. 2014, 58, 2196-2205 10.1002/mnfr.201400243
43. Espley, R. V.; Butts, C. A.; Laing, W. A.; Martell, S.; Smith, H.; McGhie, T. K.; Zhang, J.; Paturi, G.; Hedderley, D.; Bovy, A.; Schouten, H. J.; Putterill, J.; Allan, A. C.; Hellens, R. P. Dietary flavonoids from modified apple reduce inflammation markers and modulate gut microbiota in mice J. Nutr. 2014, 144, 146-154 10.3945/jn.113.182659
44. Masumoto, S.; Terao, A.; Yamamoto, Y.; Mukai, T.; Miura, T.; Shoji, T. Non-absorbable apple procyanidins prevent obesity associated with gut microbial and metabolomic changes Sci. Rep. 2016, 6, 31208 10.1038/srep31208
45. Corssmit, E. P.; Romijn, J. A.; Sauerwein, H. P. Regulation of glucose production with special attention to nonclassical regulatory mechanisms: a review Metab., Clin. Exp. 2001, 50, 742-55 10.1053/meta.2001.24195