An acylic polyisoprenoid derivative, geranylgeranylacetone protects against visceral adiposity and insulin resistance in high-fat-fed mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 299, Issue 5, 2010, Pages

  Adachi, Hironori ^a   Kondo, Tatsuya ^a   Ogawa, Rei ^b   Sasaki, Kazunari ^a   Morino Koga, Saori ^a   Sakakida, Michiharu ^b   Kawashima, Junji ^a   Motoshima, Hiroyuki ^a   Furukawa, Noboru ^a   Tsuruzoe, Kaku ^a   Miyamura, Nobuhiro ^a   Kai, Hirofumi ^a   Araki, Eiichi ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b PREFECTURAL UNIVERSITY OF KUMAMOTO   (Japan)

Author keywords

Diabetes; Heat shock protein 72; Obesity

Indexed keywords

ADIPONECTIN; CYTOKINE; HEAT SHOCK PROTEIN 72; LEPTIN; STRESS ACTIVATED PROTEIN KINASE; TEPRENONE; DITERPENE; INSULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; GENE EXPRESSION; GLUCOSE HOMEOSTASIS; INSULIN RESISTANCE; INTRAABDOMINAL FAT; LIPID DIET; MALE; METABOLIC PARAMETERS; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; AREA UNDER THE CURVE; BLOOD; BODY WEIGHT; C57BL MOUSE; EATING; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; LIVER; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADIPONECTIN; ANIMALS; AREA UNDER CURVE; BLOOD GLUCOSE; BODY WEIGHT; DITERPENES; EATING; GLUCOSE TOLERANCE TEST; HSP72 HEAT-SHOCK PROTEINS; INSULIN; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; LEPTIN; LIVER; MALE; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION;

EID: 78349237445     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00075.2010     Document Type: Article

References (56)

1. Aguirre V, Uchida T, Yenush L, Davis R, White MF. The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J Biol Chem 275: 9047-9054, 2000. (Pubitemid 30180265)
2. Ahn SG, Liu PC, Klyachko K, Morimoto RI, Thiele DJ. The loop domain of heat shock transcription factor 1 dictates DNA-binding specificity and responses to heat stress. Genes Dev 15: 2134-2145, 2001. (Pubitemid 32762056)
3. Bendriss-Vermare N, Barthelemy C, Durand I, Bruand C, Dezutter- Dambuyant C, Moulian N, Berrih-Aknin S, Caux C, Trinchieri G, Briere F. Human thymus contains IFN-alpha-producing CD11c(-), myeloid CD11c(+), and mature interdigitating dendritic cells. J Clin Invest 107: 835-844, 2001. (Pubitemid 32274036)
4. Broderick TL. Whole-body heat shock protects the ischemic rat heart by stimulating mitochondria respiration. Can J Physiol Pharmacol 84: 929-933, 2006.
5. Bruce CR, Carey AL, Hawley JA, Febbraio MA. Intramuscular heat shock protein 72 and heme oxygenase-1 mRNA are reduced in patients with type 2 diabetes: evidence that insulin resistance is associated with a disturbed antioxidant defense mechanism. Diabetes 52: 2338-2345, 2003.
6. Chung J, Nguyen AK, Henstridge DC, Holmes AG, Chan MH, Mesa JL, Lancaster GI, Southgate RJ, Bruce CR, Duffy SJ, Horvath I, Mestril R, Watt MJ, Hooper PL, Kingwell BA, Vigh L, Hevener A, Febbraio MA. HSP72 protects against obesity-induced insulin resistance. Proc Natl Acad Sci USA 105: 1739-1744, 2008.
7. Cuezva JM, Flores AI, Liras A, Santaren JF, Alconada A. Molecular chaperones and the biogenesis of mitochondria and peroxisomes. Biol Cell 77: 47-62, 1993.
8. Flier JS. Obesity wars: molecular progress confronts an expanding epidemic. Cell 116: 337-350, 2004.
9. Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA 287: 356-359, 2002.
10. Fudaba Y, Ohdan H, Tashiro H, Ito H, Fukuda Y, Dohi K, Asahara T. Geranylgeranylacetone, a heat shock protein inducer, prevents primary graft nonfunction in rat liver transplantation. Transplantation 72: 184-189, 2001.
11. Fujiki M, Kobayashi H, Abe T, Ishii K. Astroglial activation accompanies heat shock protein upregulation in rat brain following single oral dose of geranylgeranylacetone. Brain Res 991: 254-257, 2003.
12. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114: 1752-1761, 2004.
13. Gabai VL, Meriin AB, Yaglom JA, Volloch VZ, Sherman MY. Role of HSP70 in regulation of stress-kinase JNK: implications in apoptosis and aging. FEBS Lett 438: 1-4, 1998.
14. Gupte AA, Bomhoff GL, Swerdlow RH, Geiger PC. Heat treatment improves glucose tolerance and prevents skeletal muscle insulin resistance in rats fed a high-fat diet. Diabetes 58: 567-578, 2009.
15. Hayashi Y, Sawa Y, Fukuyama N, Nakazawa H, Matsuda H. Preoperative glutamine administration induces heat-shock protein 70 expression and attenuates cardiopulmonary bypass-induced inflammatory response by regulating nitric oxide synthase activity. Circulation 106: 2601-2607, 2002.
16. Hirakawa T, Rokutan K, Nikawa T, Kishi K. Geranylgeranylacetone induces heat shock proteins in cultured guinea pig gastric mucosal cells and rat gastric mucosa. Gastroenterology 111: 345-357, 1996. (Pubitemid 26256722)
17. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature 420: 333-336, 2002.
18. Hoffman RP. Indices of insulin action calculated from fasting glucose and insulin reflect hepatic, not peripheral, insulin sensitivity in African-American and Caucasian adolescents. Pediatr Diabetes 9: 57-61, 2008.
19. Hotamisligil GS. Inflammation and endoplasmic reticulum stress in obesity and diabetes. Int J Obes (Lond) 32, Suppl 7: S52-S54, 2008.
20. Hotamisligil GS. Inflammation and metabolic disorders. Nature 444: 860-867, 2006.
21. Ikeyama S, Kusumoto K, Miyake H, Rokutan K, Tashiro S. A non-toxic heat shock protein 70 inducer, geranylgeranylacetone, suppresses apoptosis of cultured rat hepatocytes caused by hydrogen peroxide and ethanol. J Hepatol 35: 53-61, 2001.
22. Ishii Y, Kwong JM, Caprioli J. Retinal ganglion cell protection with geranylgeranylacetone, a heat shock protein inducer, in a rat glaucoma model. Invest Ophthalmol Vis Sci 44: 1982-1992, 2003.
23. Kaneto H, Nakatani Y, Kawamori D, Miyatsuka T, Matsuoka TA, Matsuhisa M, Yamasaki Y. Role of oxidative stress, endoplasmic reticulum stress, and c-Jun N-terminal kinase in pancreatic beta-cell dysfunction and insulin resistance. Int J Biochem Cell Biol 38: 782-793, 2006.
24. Kaneto H, Nakatani Y, Miyatsuka T, Kawamori D, Matsuoka TA, Matsuhisa M, Kajimoto Y, Ichijo H, Yamasaki Y, Hori M. Possible novel therapy for diabetes with cell-permeable JNK-inhibitory peptide. Nat Med 10: 1128-1132, 2004.
25. Katsuno M, Sang C, Adachi H, Minamiyama M, Waza M, Tanaka F, Doyu M, Sobue G. Pharmacological induction of heat-shock proteins alleviates polyglutamine-mediated motor neuron disease. Proc Natl Acad Sci USA 102: 16801-16806, 2005.
26. Kawai T, Teshima S, Kusumoto K, Kawahara T, Kondo K, Kishi K, Rokutan K. A non-toxic heat shock protein 70 inducer, geranyl-geranylacetone, restores the heat shock response in gastric mucosa of protein-malnourished rats. J Lab Clin Med 136: 138-148, 2000.
27. Kieran D, Kalmar B, Dick JR, Riddoch-Contreras J, Burnstock G, Greensmith L. Treatment with arimoclomol, a coinducer of heat shock proteins, delays disease progression in ALS mice. Nat Med 10: 402-405, 2004.
28. Klosterhalfen B, Hauptmann S, Offner FA, Amo-Takyi B, Tons C, Winkeltau G, Affify M, Kupper W, Kirkpatrick CJ, Mittermayer C. Induction of heat shock protein 70 by zinc-bis-(DL-hydrogenaspartate) reduces cytokine liberation, apoptosis, and mortality rate in a rat model of LD100 endotoxemia. Shock 7: 254-262, 1997.
29. Kurucz I, Morva A, Vaag A, Eriksson KF, Huang X, Groop L, Koranyi L. Decreased expression of heat shock protein 72 in skeletal muscle of patients with type 2 diabetes correlates with insulin resistance. Diabetes 51: 1102-1109, 2002.
30. Literati-Nagy B, Kulcsar E, Literati-Nagy Z, Buday B, Peterfai E, Horvath T, Tory K, Kolonics A, Fleming A, Mandl J, Koranyi L. Improvement of insulin sensitivity by a novel drug, BGP-15, in insulin-resistant patients: a proof of concept randomized double-blind clinical trial. Horm Metab Res 41: 374-380, 2009.
31. Liu G, Rondinone CM. JNK: bridging the insulin signaling and inflammatory pathway. Curr Opin Investig Drugs 6: 979-987, 2005.
32. Morimoto RI, Santoro MG. Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat Biotechnol 16: 833-838, 1998.
33. Morino S, Kondo T, Sasaki K, Adachi H, Suico MA, Sekimoto E, Matsuda T, Shuto T, Araki E, Kai H. Mild electrical stimulation with heat shock ameliorates insulin resistance via enhanced insulin signaling. PLoS One 3: e4068, 2008.
34. Morino S, Suico MA, Kondo T, Sekimoto E, Yano S, Matsuda T, Matsuno T, Shuto T, Araki E, Kai H. Mild electrical stimulation increases ubiquitinated proteins and HSP72 in A549 cells via attenuation of proteasomal degradation. J Pharm Sci 108: 222-226, 2008.
35. Nagai Y, Fujiki M, Inoue R, Uchida S, Abe T, Kobayashi H, Cetinalp NE. Neuroprotective effect of geranylgeranylacetone, a noninvasive heat shock protein inducer, on cerebral infarction in rats. Neurosci Lett 374: 183-188, 2005.
36. Nakada J, Matsura T, Okazaki N, Nishida T, Togawa A, Minami Y, Inagaki Y, Ito H, Yamada K, Ishibe Y. Oral administration of geranylgeranylacetone improves survival rate in a rat endotoxin shock model: administration timing and heat shock protein 70 induction. Shock 24: 482-487, 2005.
37. Nishida T, Matsura T, Nakada J, Togawa A, Kai M, Sumioka I, Minami Y, Inagaki Y, Ishibe Y, Ito H, Ohta Y, Yamada K. Geranylgeranylacetone protects against acetaminophen-induced hepatotoxicity by inducing heat shock protein 70. Toxicology 219: 187-196, 2006. (Pubitemid 43120719)
38. Ooie T, Kajimoto M, Takahashi N, Shinohara T, Taniguchi Y, Kouno H, Wakisaka O, Yoshimatsu H, Saikawa T. Effects of insulin resistance on geranylgeranylacetone-induced expression of heat shock protein 72 and cardioprotection in high-fat diet rats. Life Sci 77: 869-881, 2005. (Pubitemid 40827191)
39. Ooie T, Takahashi N, Saikawa T, Nawata T, Arikawa M, Yamanaka K, Hara M, Shimada T, Sakata T. Single oral dose of geranylgeranylacetone induces heat-shock protein 72 and renders protection against ischemia/reperfusion injury in rat heart. Circulation 104: 1837-1843, 2001.
40. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH, Hotamisligil GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461, 2004. (Pubitemid 39372439)
41. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313: 1137-1140, 2006. (Pubitemid 44300242)
42. Park HS, Lee JS, Huh SH, Seo JS, Choi EJ. HSP72 functions as a natural inhibitory protein of c-Jun N-terminal kinase. EMBO J 20: 446-456, 2001. (Pubitemid 32126980)
43. Polla BS, Kantengwa S, Francois D, Salvioli S, Franceschi C, Marsac C, Cossarizza A. Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc Natl Acad Sci USA 93: 6458-6463, 1996.
44. Sakurai M, Takamura T, Ota T, Ando H, Akahori H, Kaji K, Sasaki M, Nakanuma Y, Miura K, Kaneko S. Liver steatosis, but not fibrosis, is associated with insulin resistance in nonalcoholic fatty liver disease. J Gastroenterol 42: 312-317, 2007.
45. Shapiro LE, Katz CP, DeFesi CR, Surks MI. Heat shock of cultured GC cells enhances the level of triiodothyronine induced growth hormone (GH) and GH messenger ribonucleic acid. Endocrinology 125: 180-185, 1989.
46. Shinohara T, Takahashi N, Kohno H, Yamanaka K, Ooie T, Wakisaka O, Murozono Y, Taniguchi Y, Torigoe Y, Hara M, Shimada T, Saikawa T, Yoshimatsu H. Mitochondria are targets for geranylgeranylacetone- induced cardioprotection against ischemia-reperfusion in the rat heart. Am J Physiol Heart Circ Physiol 293: H1892-H1899, 2007.
47. Shirakami A, Toyonaga T, Tsuruzoe K, Shirotani T, Matsumoto K, Yoshizato K, Kawashima J, Hirashima Y, Miyamura N, Kahn CR, Araki E. Heterozygous knockout of the IRS-1 gene in mice enhances obesity-linked insulin resistance: a possible model for the development of type 2 diabetes. J Endocrinol 174: 309-319, 2002.
48. Tanaka K, Tsutsumi S, Arai Y, Hoshino T, Suzuki K, Takaki E, Ito T, Takeuchi K, Nakai A, Mizushima T. Genetic evidence for a protective role of heat shock factor 1 against irritant-induced gastric lesions. Mol Pharmacol 71: 985-993, 2007. (Pubitemid 46457003)
49. Taniguchi CM, Emanuelli B, Kahn CR. Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7: 85-96, 2006.
50. Torok Z, Tsvetkova NM, Balogh G, Horvath I, Nagy E, Penzes Z, Hargitai J, Bensaude O, Csermely P, Crowe JH, Maresca B, Vigh L. Heat shock protein coinducers with no effect on protein denaturation specifically modulate the membrane lipid phase. Proc Natl Acad Sci USA 100: 3131-3136, 2003.
51. Tuncman G, Hirosumi J, Solinas G, Chang L, Karin M, Hotamisligil GS. Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc Natl Acad Sci USA 103: 10741-10746, 2006.
52. Vigh L, Horvath I, Maresca B, Harwood JL. Can the stress protein response be controlled by "membrane-lipid therapy"? Trends Biochem Sci 32: 357-363, 2007.
53. Volloch V, Gabai VL, Rits S, Force T, Sherman MY. HSP72 can protect cells from heat-induced apoptosis by accelerating the inactivation of stress kinase JNK. Cell Stress Chaperones 5: 139-147, 2000.
54. Williamson CL, Dabkowski ER, Dillmann WH, Hollander JM. Mitochondria protection from hypoxia/reoxygenation injury with mitochondria heat shock protein 70 overexpression. Am J Physiol Heart Circ Physiol 294: H249-H256, 2008.
55. Yamagami K, Yamamoto Y, Ishikawa Y, Yonezawa K, Toyokuni S, Yamaoka Y. Effects of geranyl-geranyl-acetone administration before heat shock preconditioning for conferring tolerance against ischemia-reperfusion injury in rat livers. J Lab Clin Med 135: 465-475, 2000.
56. Yasuda H, Shichinohe H, Kuroda S, Ishikawa T, Iwasaki Y. Neuroprotective effect of a heat shock protein inducer, geranylgeranylacetone in permanent focal cerebral ischemia. Brain Res 1032: 176-182, 2005. (Pubitemid 40170324)