Differential gene expression in pancreatic tissues of streptozocin-induced diabetic rats and genetically-diabetic mice in response to hypoglycemic dipeptide cyclo (His-Pro) treatment

Springer Science and Business Media LLC - Tập 39 - Trang 8821-8835 - 2012
Song Ah Choi1, Hyung Joo Suh2, Jong Won Yun3, Jang Won Choi1
1Department of Bioindustry, Daegu University, Kyungsan, Kyungbuk, Republic of Korea
2Department of Food and Nutrition, Korea University, Seoul, Republic of Korea
3Department of Biotechnology, Daegu University, Kyungsan, Kyungbuk, Republic of Korea

Tóm tắt

Diabetic studies are mostly interested in gene expression in the pancreas, the site of insulin secretion that regulates blood glucose levels. However, a single gene approach has been ruled out for many years in discovering new genes or the molecular networks involved in the induction process of diabetes. To understand the molecular mechanisms by which cyclo (His-Pro) (CHP) affects amelioration of diabetes mellitus, we performed gene expression profiling in the pancreatic tissues of two diabetic animal models, streptozocin (STZ)-induced diabetic rats (T1DM) and genetically-diabetic (C57BL/6J ob/ob) mice (T2DM). To understand the healing process of these diabetic rodents, we examined the effects of CHP on various gene expression in pancreatic tissues of both animal models. Our microarray analysis revealed that a total of 1,175 genes were down-regulated and 629 genes were up-regulated in response to STZ treatment, and the altered expression levels of numerous genes were restored to normal state upon CHP treatment. In particular, 476 genes showed significantly altered gene expression upon CHP treatment. In a functional classification, 7,198 genes were counted as differentially expressed in pancreatic tissues of STZ- and CHP-treated rats compared with control, whereas 1,534 genes were restored to normal states by CHP treatment. Microarray data demonstrated for the first time that overexpression of the genes encoding IL-1 receptor, lipid metabolic enzymes (e.g. Mte1, Ptdss1, and Sult2a1), myo-inositol oxygenase, glucagon, and somatostatin as well as down-regulation of olfactory receptor 984 and mitochondrial ribosomal protein, which are highly linked to T1DM etiology. In genetically-diabetic mice, 4,384 genes were altered in gene expression by more than 2-fold compared to the control mice, when counted differentially expressed. In genetically-diabetic mice, 4,384 genes altered in expression by higher than 2-fold were counted as differentially expressed genes in pancreatic tissues of CHP-treated mice. On the other hand, 2,140 genes were up-regulated and 2,244 genes were down-regulated by CHP treatment. The results of the microarray analysis revealed that up-regulation of IL-2, IL12a, and leptin receptor and down-regulation of PIK3 played important physiological roles in the onset of T2DM. In conclusion, we hypothesize that CHP accelerates alterations of gene expression in ameliorating diabetes and antagonizes those that induces the disease.

Tài liệu tham khảo

WHO (2006) Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia. World Health Organization. http://www.who.int/diabetes/publications/diagnosis_diabetes2006/en/index.html Atta-Ur-Rahman, Zaman K (1989) Medicinal plants with hypoglycemic activity. J Ethnopharmacol 26:1–55 Bnouham M, Ziyyat A, Mekhfi H, Tahri A, Legssyer A (2006) Medicinal plants with potential antidiabetic activity—a review of ten years of herbal medicine research (1990–2000). Int J Diabetes Metab 14:1–25 Yamada M, Shibusawa N, Hashida T, Satoh T, Monden T, Prasad C, Mori M (1999) Abundance of cyclo (His-Pro)-like immunoreactivity in the brain of TRH-deficient mice. Endocrinology 140:538–541 Ortiz-Caro J, González C, Jolin T (1984) Diurnal variations of plasma growth hormone, thyrotropin, thyroxine, and triiodothyronine in streptozocin-diabetic and food-restricted rats. Endocrinology 115:2227–2232 Song MK, Rosenthal MJ, Naliboff BD, Phanumas L, Kang KW (1998) Effects of bovine prostate powder on zinc, glucose, and insulin metabolism in old patients with non-insulin-dependent diabetes mellitus. Metabolism 47:39–43 Song MK, Hwang IK, Rosenthal MJ, Harris DM, Yamaguchi DT, Yip I, Go VL (2003) Anti-hyperglycemic activity of zinc plus cyclo (his-pro) in genetically diabetic Goto-Kakizaki and aged rats. Exp Biol Med (Maywood) 228:1338–1345 Friedman M, Brandon DL (2001) Nutritional and health benefits of soy proteins. J Agric Food Chem 49:1069–1086 Song MK, Rosenthal MJ, Song AM, Yang H, Ao Y, Yamaguchi DT (2005) Raw vegetable food containing high cyclo (his-pro) improved insulin sensitivity and body weight control. Metabolism 54:1480–1489 Song MK, Rosenthal MJ, Song AM, Uyemura K, Yang H, Ament ME, Yamaguchi DT, Cornford EM (2009) Body weight reduction in rats by oral treatment with zinc plus cyclo-(His-Pro). Br J Pharmacol 158:442–450 Resjö S, Berger K, Fex M, Hansson O (2008) Proteomic studies in animal models of diabetes. Proteomics Clin Appl 2:654–669 Wu KK, Huan Y (2008) Streptozocin-induced diabetic models in mice and rats. Curr Protoc Pharmacol 40:1–14 Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432 Ohno T, Ishii C, Kato N, Ito Y, Shimizu M, Tomono S, Murata K, Kawazu S (1995) Increased expression of a regenerating (reg) gene protein in neonatal rat pancreas treated with streptozotocin. Endocr J 42:649–653 Takasawa S, Okamoto H (2002) Pancreatic beta-cell death, regeneration and insulin secretion: roles of poly(ADP-ribose) polymerase and cyclic ADP-ribose. Int J Exp Diabetes Res 3:79–96 Kodama S, Toyonaga T, Kondo T, Matsumoto K, Tsuruzoe K, Kawashima J, Goto H, Kume K, Kume S, Sakakida M, Araki E (2005) Enhanced expression of PDX-1 and Ngn3 by exendin-4 during beta cell regeneration in STZ-treated mice. Biochem Biophys Res Commun 327:1170–1178 Qiu L, List EO, Kopchick JJ (2005) Differentially expressed proteins in the pancreas of diet-induced diabetic mice. Mol Cell Proteomics 4:1311–1318 Mathis D, Vence L, Benoist C (2001) beta-Cell death during progression to diabetes. Nature 414:792–798 Marzo N, Mora C, Fabregat ME, Martín J, Usac EF, Franco C, Barbacid M, Gomis R (2004) Pancreatic islets from cyclin-dependent kinase 4/R24C (Cdk4) knockin mice have significantly increased beta cell mass and are physiologically functional, indicating that Cdk4 is a potential target for pancreatic beta cell mass regeneration in Type 1 diabetes. Diabetologia 47:686–694 Wong FS, Wen L, Tang M, Ramanathan M, Visintin I, Daugherty J, Hannum LG, Janeway CA Jr, Shlomchik MJ (2004) Investigation of the role of B-cells in type 1 diabetes in the NOD mouse. Diabetes 53:2581–2587 Buchholz M, Boeck W, Fensterer H, Müller F, Wenger C, Michl P, Adler G, Gress TM (2001) Use of DNA arrays/microarrays in pancreatic research. Pancreatology 1:581–586 Scearce LM, Brestelli JE, McWeeney SK, Lee CS, Mazzarelli J, Pinney DF, Pizarro A, Stoeckert CJ Jr, Clifton SW, Permutt MA, Brown J, Melton DA, Kaestner KH (2002) Functional genomics of the endocrine pancreas: the pancreas clone set and PancChip, new resources for diabetes research. Diabetes 51:1997–2004 Sun G (2007) Application of DNA microarrays in the study of human obesity and type 2 diabetes. OMICS 11:25–40 Dunbar DR (2009) Gene expression mining in type 2 diabetes research. Methods Mol Biol 560:263–271 White P, Kaestner KH (2009) Gene expression analysis in diabetes research. Methods Mol Biol 560:239–261 Cardozo AK, Kruhøffer M, Leeman R, Orntoft T, Eizirik DL (2001) Identification of novel cytokine-induced genes in pancreatic beta-cells by high-density oligonucleotide arrays. Diabetes 50:909–920 Diraison F, Motakis E, Parton LE, Nason GP, Leclerc I, Rutter GA (2004) Impact of adenoviral transduction with SREBP1c or AMPK on pancreatic islet gene expression profile: analysis with oligonucleotide microarrays. Diabetes 53:S84–S91 Devi SS, Mehendale HM (2006) Microarray analysis of thioacetamide-treated type 1 diabetic rats. Toxicol Appl Pharmacol 212:69–78 Kim SW, Hwang HJ, Lee SH, Yun JW (2008) Proteomic and transcriptomic analysis for streptozotocin-induced diabetic rat pancreas in response to fungal polysaccharide treatments. Proteomics 8:2344–2361 Koo KB, Suh HJ, Ra KS, Choi JW (2011) Protective effect of cyclo(his-pro) on streptozotocin-induced cytotoxicity and apoptosis in vitro. J Microbiol Biotechnol 21:218–227 Larsen CM, Faulenbach M, Vaag A, Vølund A, Ehses JA, Seifert B, Mandrup-Poulsen T, Donath MY (2007) Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 356:1517–1526 Kaye WA, Adri MN, Soeldner JS, Rabinowe SL, Kaldany A, Kahn CR, Bistrian B, Srikanta S, Ganda OP, Eisenbarth GS (1986) Acquired defect in interleukin-2 production in patients with type I diabetes mellitus. N Engl J Med 315:920–924 Duarte PM, de Oliveira MC, Tambeli CH, Parada CA, Casati MZ, Nociti FH Jr (2007) Overexpression of interleukin-1beta and interleukin-6 may play an important role in periodontal breakdown in type 2 diabetic patients. J Periodontal Res 42:377–381 Chu SH, Geyer RP (1983) Tissue content and metabolism of myo-inositol in normal and lipodystrophic gerbils. J Nutr 113:293–303 Ostlund RE Jr, McGill JB, Herskowitz I, Kipnis DM, Santiago JV, Sherman WR (1993) D-chiro-inositol metabolism in diabetes mellitus. Proc Natl Acad Sci USA 90:9988–9992 Kawa JM, Przybylski R, Taylor CG (2003) Urinary chiro-inositol and myo-inositol excretion is elevated in the diabetic db/db mouse and streptozotocin diabetic rat. Exp Biol Med 228:907–914 Breer H, Strotmann J (1997) Olfactory receptor gene expression. Semin Cell Dev Biol 8:189–195 Dang H, Franklin G, Darlak K, Spatola AF, Ellis SR (1990) Discoordinate expression of the yeast mitochondrial ribosomal protein MRP1. J Biol Chem 265:7449–7454 Chen YC, Chang MY, Shiau AL, Yo YT, Wu CL (2007) Mitochondrial ribosomal protein S36 delays cell cycle progression in association with p53 modification and p21(WAF1/CIP1) expression. J Cell Biochem 100:981–990 Accardi R, Oxelmark E, Jauniaux N, de Pinto V, Marchini A, Tommasino M (2004) High levels of the mitochondrial large ribosomal subunit protein 40 prevent loss of mitochondrial DNA in null mmf1 Saccharomyces cerevisiae cells. Yeast 21:539–548 Adorini L (2001) Interleukin 12 and autoimmune diabetes. Nat Genet 27:131–132 Dancygier H, Berg J, Classen M (1987) Interleukin-2 production and type I diabetes. N Engl J Med 316:949–950 Andreelli F, Laville M, Ducluzeau PH, Vega N, Vallier P, Khalfallah Y, Riou JP, Vidal H (1999) Defective regulation of phosphatidylinositol-3-kinase gene expression in skeletal muscle and adipose tissue of non-insulin-dependent diabetes mellitus patients. Diabetologia 42:358–364 Nikoulina SE, Ciaraldi TP, Carter L, Mudaliar S, Park KS, Henry RR (2001) Impaired muscle glycogen synthase in type 2 diabetes is associated with diminished phosphatidylinositol 3-kinase activation. J Clin Endocrinol Metab 86:4307–4314 Morioka T, Asilmaz E, Hu J, Dishinger JF, Kurpad AJ, Elias CF, Li H, Elmquist JK, Kennedy RT, Kulkarni RN (2007) Disruption of leptin receptor expression in the pancreas directly affects beta cell growth and function in mice. J Clin Invest 117:2860–2868