Reduced nuclear protein 1 expression improves insulin sensitivity and protects against diet-induced glucose intolerance through up-regulation of heat shock protein 70

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 5, 2015, Pages 962-969

  Barbosa Sampaio, H C ^a   Drynda, R ^a   Liu, B ^a   Rodriguez De Ledesma, A M ^a   Malicet, C ^b   Iovanna, J L ^b   Jones, P M ^a   Muller, D S ^a   Persaud, S J ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Glucose homeostasis; Heat shock protein; High fat diet; Insulin resistance; Islets of Langerhans

Indexed keywords

BROXURIDINE; GLUCOSE; HEAT SHOCK PROTEIN 70; INSULIN; MESSENGER RNA; NUCLEAR PROTEIN; NUCLEAR PROTEIN 1; PROTEIN KINASE B; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; NUPR1 PROTEIN, MOUSE; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CLEARANCE; DIET INDUCED GLUCOSE INTOLERANCE; DIET RESTRICTION; GENE DOSAGE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE CLEARANCE; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INSULIN BLOOD LEVEL; INSULIN RELEASE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; INTRAABDOMINAL FAT; INVESTIGATIVE PROCEDURES; LIPID DIET; LIPID STORAGE; MORPHOMETRICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; WILD TYPE; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; GENETICS; INSULIN RESISTANCE; KNOCKOUT MOUSE; METABOLISM; PANCREAS ISLET; PHOSPHORYLATION; SECRETION (PROCESS); TIME; TUMOR CELL LINE;

ANIMALIA; MUS;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL PROLIFERATION; DIET, HIGH-FAT; DNA-BINDING PROTEINS; GENE EXPRESSION; GLUCOSE INTOLERANCE; HSP70 HEAT-SHOCK PROTEINS; IMMUNOHISTOCHEMISTRY; INSULIN; INSULIN RESISTANCE; ISLETS OF LANGERHANS; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASM PROTEINS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS; UP-REGULATION;

EID: 84922738759     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.01.013     Document Type: Article

References (39)

1. (accessed 180914). http://www.idf.org/diabetesatlas/introduction.
2. DeFronzo R.A., Abdul-Ghani M.A. Preservation of β-cell function: the key to diabetes prevention. J. Clin. Endocrinol. Metab. 2011, 96:2354-2366.
3. Kahn S.E. The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of type 2 diabetes. Diabetologia 2003, 46:3-19.
4. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444:860-867.
5. Saad M.J., Araki E., Miralpeix M., Rothenberg P.L., White M.F., Kahn C.R. Regulation of insulin receptor substrate-1 in liver and muscle of animal models of insulin resistance. J. Clin. Invest. 1992, 90:1839-1849.
6. Ducluzeau P.H., Fletcher L.M., Welsh G.I., Tavare J.M. Functional consequence of targeting protein kinase B/Akt to GLUT4 vesicles. J. Cell Sci. 2002, 115:2857-2866.
7. Wu C. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 1995, 11:441-469.
8. Sharp F.R., Massa S.M., Swanson R.A. Heat shock protein protection. Trends Neurosci. 1999, 22:97-99.
9. Chung J., Nguyen A.K., Henstridge D.C., et al. HSP72 protects against obesity-induced insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1739-1744.
10. Kurucz I., Morva A., Vaag A., et al. Decreased expression of heat shock protein 72 in skeletal muscle of patients with type 2 diabetes correlates with insulin resistance. Diabetes 2002, 51:1102-1109.
11. Bruce C.R., Carey A.L., Hawley J.A., Febbraio M.A. 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 2003, 52:2338-2345.
12. Morino S., Kondo T., Sasaki K., Adachi H., Suico M.A., 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 2008, 3:e4068.
13. Welch W.J. The role of heat-shock proteins as molecular chaperones. Curr. Opin. Cell Biol. 1991, 3:1033-1038.
14. McHaourab H.S., Godar J.A., Stewart P.L. Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins. Biochemistry 2009, 48:3828-3837.
15. Mymrikov E.V., Seit-Nebi A.S., Gusev N.B. Large potentials of small heat shock proteins. Physiol. Rev. 2011, 91:1123-1159.
16. Shamovsky I., Nudler E. New insights into the mechanism of heat shock response activation. Cell. Mol. Life Sci. 2008, 65:855-861.
17. Lindquist S., Craig E.A. The heat-shock proteins. Annu. Rev. Genet. 1988, 22:631-677.
18. Barbosa-Sampaio H.C., Liu B., Drynda R., Rodriguez de Ledesma A.M., King A.J., Bowe J.E., Malicet C., Iovanna J.L., Jones P.M., Persaud S.J., Muller D.S. Nupr1 deletion protects against glucose intolerance by increasing beta cell mass. Diabetologia 2013, 56:2477-2486.
19. Vasseur S., Hoffmeister A., Garcia-Montero A., Mallo G.V., Feil R., Kühbandner S., et al. p8-Deficient fibroblasts grow more rapidly and are more resistant to adriamycin-induced apoptosis. Oncogene 2002, 21:1685-1694.
20. Papadimitriou A., King A.J., Jones P.M., Persaud S.J. Anti-apoptotic effects of arachidonic acid and prostaglandin E2 in pancreatic beta-cells. Cell. Physiol. Biochem. 2007, 20:607-616.
21. Persaud S.J., Muller D., Belin V.D., Kitsou-Mylona I., Asare-Anane H., Papadimitriou A., Burns C.J., Huang G.C., Amiel S.A., Jones P.M. The role of arachidonic acid and its metabolites in insulin secretion from human islets of Langerhans. Diabetes 2007, 56:197-203.
22. 2+, cyclic AMP, a phorbol ester and noradrenaline. Biochem. J. 1988, 254:397-403.
23. Persaud S.J., Liu B., Sampaio H.B., Jones P.M., Muller D.S. Calcium/calmodulin-dependent kinase IV controls glucose-induced Irs2 expression in mouse beta cells via activation of cAMP response element-binding protein. Diabetologia 2011, 54:1109-1120.
24. Vasseur S., Vidal Mallo G., Fiedler F., Bödeker H., Cánepa E., Moreno S., et al. Cloning and expression of the human p8, a nuclear protein with mitogenic activity. Eur. J. Biochem. 1999, 259:670-675.
25. Wronska A., Kmiec Z. Structural and biochemical characteristics of various white adipose tissue depots. Acta Physiol. (Oxf.) 2012, 205:194-208.
26. Kondo T., Motoshima H., Igata M., Kawashima J., Matsumura T., Kai H., Araki E. The role of heat shock response in insulin resistance and diabetes. Diabetes Metab. J. 2014, 38:100-106.
27. Chang L., Chiang S.H., Saltiel A.R. Insulin signaling and the regulation of glucose transport. Mol. Med. 2004, 10:65-71.
28. Fargnoli J., Kunisada T., Fornace A.J., Scheider E.L., Holbrook N.J. Decreased expression of heat shock protein 70 mRNA and protein after heat treatment in cells of aged rats. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:846-850.
29. Gabriel J.E., Ferro J.A., Stefani R.M., Ferro M.I., Gomes S.L., Macari M. Effect of acute heat stress on heat shock protein 70 mRNA expression and on heat shock protein expression in the liver of broilers. Br. Poult. Sci. 1996, 37:443-449.
30. Qian S.B., McDonough H., Boellmann F., Cyr D.M., Patterson C. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 2006, 440:551-555.
31. Mao R.-F., Rubio V., Chen H., Bai L., Mansour O.C., Shi Z.-Z. OLA1 protects cells in heat shock by stabilizing HSP70. Cell Death Dis. 2013, 4:e491.
32. Kavanagh K., Flynn D.M., Jenkins K.A., Zhang L., Wagner J.D. Restoring HSP70 deficiencies improves glucose tolerance in diabetic monkeys. Am. J. Physiol. Endocrinol. Metab. 2011, 300:E894-E901.
33. Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., Görgün C.Z., Hotamisligil G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313:1137-1140.
34. Hooper P.L. Hot-tub therapy for type 2 diabetes mellitus. N. Engl. J. Med. 1999, 341:924-925.
35. Literáti-Nagy B., Kulcsár E., Literáti-Nagy Z., et al. 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. 2009, 41:374-380.
36. Gupte A.A., Bomhoff G.L., Swerdlow R.H., Geiger P.C. Heat treatment improves glucose tolerance and prevents skeletal muscle insulin resistance in rats fed a high-fat diet. Diabetes 2009, 58:567-578.
37. Hoffmeister A., Ropolo A., Vasseur S., Mallo G.V., Bodeker H., Ritz-Laser B., et al. The HMG-I/Y-related protein p8 binds to p300 and Pax2 trans-activation domain-interacting protein to regulate the trans-activation activity of the Pax2A and Pax2B transcription factors on the glucagon gene promoter. J. Biol. Chem. 2002, 277:22314-22319.
38. Li Q., Heerler M., Landsberger N., Kaludov N., Ogrryzko V.V., Nakatani Y., Wolffe A.P. Xenopus NF-Y pre-sets chromatin to potentiate p300 and acetylation-responsive transcription from the Xenopus hsp70 promoter in vivo. EMBO J. 1998, 17:6300-6315.
39. Xu D., Zalmas L.P., La Thangue N.B. A transcription cofactor required for the heat-shock response. EMBO Rep. 2008, 9:662-669.