Reversal of muscle atrophy by Zhimu-Huangbai herb-pair via Akt/mTOR/FoxO3 signal pathway in streptozotocin-induced diabetic mice

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Zhang, Jinbao ^a   Zhuang, Pengwei ^a,b   Wang, Yan ^a   Song, Lili ^a   Zhang, Mixia ^a   Lu, Zhiqiang ^a   Zhang, Lu ^a   Wang, Jing ^a   Alemu, Paulos N ^a   Zhang, Yanjun ^a   Wei, Hongjun ^b   Li, Hongyan ^b  

^a TIANJIN UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^b Tianjin Economic Technological Development Area   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HERBACEOUS AGENT; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; ZHIMU HUANGBAI HERB PAIR; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, MOUSE; GLUCOSE BLOOD LEVEL; INSULIN; LIPID; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; CONTROLLED STUDY; DIABETES MELLITUS; DRUG ACTIVITY; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; LIPID DIET; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE FUNCTION; MUSCLE MASS; MUSCLE STRENGTH; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; ANIMAL; BLOOD; BODY WEIGHT; CHINESE MEDICINE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DISEASE MODEL; DRUG EFFECTS; GLUCOSE TOLERANCE TEST; METABOLISM; PATHOLOGY;

ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; DRUGS, CHINESE HERBAL; FORKHEAD TRANSCRIPTION FACTORS; GLUCOSE TOLERANCE TEST; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LIPIDS; MALE; MEDICINE, CHINESE TRADITIONAL; MICE; MUSCLE STRENGTH; MUSCULAR ATROPHY; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84903376087     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100918     Document Type: Review

References (58)

1. Glass DJ (2003) Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat Cell Biol 5: 87-90.
2. Clavel S, Siffroi-Fernandez S, Coldefy AS, Boulukos K, Pisani DF, et al. (2010) Regulation of the intracellular localization of Foxo3a by stress-activated protein kinase signaling pathways in skeletal muscle cells. Mol Cell Biol 30: 470-480.
3. Ito N, Ruegg UT, Kudo A, Miyagoe-Suzuki Y, Takeda S (2013) Activation of calcium signaling through Trpv1 by nNOS and peroxynitrite as a key trigger of skeletal muscle hypertrophy. Nat Med 19: 101-106.
4. Lambertucci AC, Lambertucci RH, Hirabara SM, Curi R, Moriscot AS, et al. (2012) Glutamine supplementation stimulates protein-synthetic and inhibits protein-degradative signaling pathways in skeletal muscle of diabetic rats. PLoS One 7: e50390.
5. Hulmi JJ, Silvennoinen M, Lehti M, Kivela R, Kainulainen H (2012) Altered REDD1, myostatin, and Akt/mTOR/FoxO/MAPK signaling in streptozotocin-induced diabetic muscle atrophy. Am J Physiol Endocrinol Metab 302: E307-315.
6. Newsholme P, Abdulkader F, Rebelato E, Romanatto T, Pinheiro CH, et al. (2011) Amino acids and diabetes: implications for endocrine, metabolic and immune function. Front Biosci (Landmark Ed) 16: 315-339.
7. Glass DJ (2005) Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37: 1974-1984.
8. Musaro A, McCullagh K, Paul A, Houghton L, Dobrowolny G, et al. (2001) Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 27: 195-200. (Pubitemid 32157448)
9. Miyazaki M, Esser KA (2009) Cellular mechanisms regulating protein synthesis and skeletal muscle hypertrophy in animals. J Appl Physiol 106: 1367-1373.
10. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, et al. (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14: 395-403. (Pubitemid 38591410)
11. Latres E, Amini AR, Amini AA, Griffiths J, Martin FJ, et al. (2005) Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J Biol Chem 280: 2737-2744. (Pubitemid 40189380)
12. Goodman CA, Miu MH, Frey JW, Mabrey DM, Lincoln HC, et al. (2010) A phosphatidylinositol 3-kinase/protein kinase B-independent activation of mammalian target of rapamycin signaling is sufficient to induce skeletal muscle hypertrophy. Mol Biol Cell 21: 3258-3268.
13. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, et al. (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019. (Pubitemid 34428747)
14. Risson V, Mazelin L, Roceri M, Sanchez H, Moncollin V, et al. (2009) Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J Cell Biol 187: 859-874.
15. Drummond MJ, Dreyer HC, Fry CS, Glynn EL, Rasmussen BB (2009) Nutritional and contractile regulation of human skeletal muscle protein synthesis and mTORC1 signaling. J Appl Physiol (1985) 106: 1374-1384.
16. Laplante M, Sabatini DM (2012) mTOR signaling in growth control and disease. Cell 149: 274-293.
17. Guertin DA, Stevens DM, Thoreen CC, Burds AA, Kalaany NY, et al. (2006) Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCalpha, but not S6K1. Dev Cell 11: 859-871. (Pubitemid 44804279)
18. Adegoke OA, Abdullahi A, Tavajohi-Fini P (2012) mTORC1 and the regulation of skeletal muscle anabolism and mass. Appl Physiol Nutr Metab 37: 395-406.
19. Bentzinger CF, Romanino K, Cloetta D, Lin S, Mascarenhas JB, et al. (2008) Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab 8: 411-424.
20. Ohanna M, Sobering AK, Lapointe T, Lorenzo L, Praud C, et al. (2005) Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat Cell Biol 7: 286-294. (Pubitemid 40331130)
21. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, et al. (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6: 472-483. (Pubitemid 350163056)
22. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, et al. (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117: 399-412. (Pubitemid 38534545)
23. Mammucari C, Schiaffino S, Sandri M (2008) Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy 4: 524-526. (Pubitemid 351705153)
24. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, et al. (2006) PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci U S A 103: 16260-16265. (Pubitemid 44715184)
25. Zheng B, Ohkawa S, Li H, Roberts-Wilson TK, Price SR (2010) FOXO3a mediates signaling crosstalk that coordinates ubiquitin and atrogin-1/MAFbx expression during glucocorticoid-induced skeletal muscle atrophy. FASEB J 24: 2660-2669.
26. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, et al. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708. (Pubitemid 33104839)
27. Jia W, Gao W, Tang L (2003) Antidiabetic herbal drugs officially approved in China. Phytother Res 17: 1127-1134. (Pubitemid 38057166)
28. Tong XL, Dong L, Chen L, Zhen Z (2012) Treatment of diabetes using traditional Chinese medicine: past, present and future. Am J Chin Med 40: 877-886.
29. Ma C, Fan M, Tang Y, Li Z, Sun Z, et al. (2008) Identification of major alkaloids and steroidal saponins in rat serum by HPLC-diode array detection-MS/MS following oral administration of Huangbai-Zhimu herb-pair Extract. Biomed Chromatogr 22: 835-850.
30. Xie W, Zhao Y, Zhang Y (2011) Traditional chinese medicines in treatment of patients with type 2 diabetes mellitus. Evid Based Complement Alternat Med 2011: 726723.
31. Liu YW, Zhu X, Lu Q, Wang JY, Li W, et al. (2012) Total saponins from Rhizoma Anemarrhenae ameliorate diabetes-associated cognitive decline in rats: involvement of amyloid-beta decrease in brain. J Ethnopharmacol 139: 194-200.
32. Bhutada P, Mundhada Y, Bansod K, Tawari S, Patil S, et al. (2011) Protection of cholinergic and antioxidant system contributes to the effect of berberine ameliorating memory dysfunction in rat model of streptozotocin-induced diabetes. Behav Brain Res 220: 30-41.
33. Zhang X, Zhao Y, Zhang M, Pang X, Xu J, et al. (2012) Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PLoS One 7: e42529.
34. He K, Li X, Chen X, Ye X, Huang J, et al. (2011) Evaluation of antidiabetic potential of selected traditional Chinese medicines in STZ-induced diabetic mice. J Ethnopharmacol 137: 1135-1142.
35. Tang YH, Sun ZL, Fan MS, Li ZX, Huang CG (2012) Anti-diabetic effects of TongGuanWan, a Chinese traditional herbal formula, in C57BL/KsJ-db/db mice. Planta Med 78: 18-23.
36. Mu J, Woods J, Zhou YP, Roy RS, Li Z, et al. (2006) Chronic inhibition of dipeptidyl peptidase-4 with a sitagliptin analog preserves pancreatic beta-cell mass and function in a rodent model of type 2 diabetes. Diabetes 55: 1695-1704. (Pubitemid 44324122)
37. Kusakabe T, Tanioka H, Ebihara K, Hirata M, Miyamoto L, et al. (2009) Beneficial effects of leptin on glycaemic and lipid control in a mouse model of type 2 diabetes with increased adiposity induced by streptozotocin and a high-fat diet. Diabetologia 52: 675-683.
38. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, et al. (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337-342. (Pubitemid 44764104)
39. Pandey SN, Cabotage J, Shi R, Dixit M, Sutherland M, et al. (2012) Conditional over-expression of PITX1 causes skeletal muscle dystrophy in mice. Biology Open 1: 629-639.
40. Wu Y, Lousberg EL, Moldenhauer LM, Hayball JD, Coller JK, et al. (2012) Inhibiting the TLR4-MyD88 signalling cascade by genetic or pharmacological strategies reduces acute alcohol-induced sedation and motor impairment in mice. Br J Pharmacol 165: 1319-1329.
41. Chambon C, Duteil D, Vignaud A, Ferry A, Messaddeq N, et al. (2010) Myocytic androgen receptor controls the strength but not the mass of limb muscles. Proc Natl Acad Sci U S A 107: 14327-14332.
42. Ravenscroft G, Jackaman C, Bringans S, Papadimitriou JM, Griffiths LM, et al. (2011) Mouse models of dominant ACTA1 disease recapitulate human disease and provide insight into therapies. Brain 134: 1101-1115.
43. Hill AJ, Mercier MS, Hill TD, Glyn SE, Jones NA, et al. (2012) Cannabidivarin is anticonvulsant in mouse and rat. Br J Pharmacol 167: 1629-1642.
44. Dogra C, Changotra H, Wedhas N, Qin X, Wergedal JE, et al. (2007) TNF-related weak inducer of apoptosis (TWEAK) is a potent skeletal muscle-wasting cytokine. FASEB J 21: 1857-1869. (Pubitemid 46855631)
45. Paul PK, Gupta SK, Bhatnagar S, Panguluri SK, Darnay BG, et al. (2010) Targeted ablation of TRAF6 inhibits skeletal muscle wasting in mice. J Cell Biol 191: 1395-1411.
46. Zhuang P, Zhang Y, Cui G, Bian Y, Zhang M, et al. (2012) Direct stimulation of adult neural stem/progenitor cells in vitro and neurogenesis in vivo by salvianolic acid B. PLoS One 7: e35636.
47. Zhuang PW, Cui GZ, Zhang YJ, Zhang MX, Guo H, et al. (2013) Baicalin regulates neuronal fate decision in neural stem/progenitor cells and stimulates hippocampal neurogenesis in adult rats. CNS Neurosci Ther 19: 154-162.
48. Wu M, Falasca M, Blough ER (2011) Akt/protein kinase B in skeletal muscle physiology and pathology. J Cell Physiol 226: 29-36.
49. Sugita H, Kaneki M, Sugita M, Yasukawa T, Yasuhara S, et al. (2005) Burn injury impairs insulin-stimulated Akt/PKB activation in skeletal muscle. Am J Physiol Endocrinol Metab 288: E585-591. (Pubitemid 40250554)
50. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, et al. (2001) Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3: 1009-1013. (Pubitemid 34428746)
51. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, et al. (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458-471. (Pubitemid 350163055)
52. Schiaffino S, Mammucari C (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 1: 4.
53. Workeneh B, Bajaj M (2013) The regulation of muscle protein turnover in diabetes. Int J Biochem Cell Biol 45: 2239-2244.
54. Pereira S, Marliss EB, Morais JA, Chevalier S, Gougeon R (2008) Insulin resistance of protein metabolism in type 2 diabetes. Diabetes 57: 56-63.
55. Deblon N, Bourgoin L, Veyrat-Durebex C, Peyrou M, Vinciguerra M, et al. (2012) Chronic mTOR inhibition by rapamycin induces muscle insulin resistance despite weight loss in rats. Br J Pharmacol 165: 2325-2340.
56. Wang X, Hu Z, Hu J, Du J, Mitch WE (2006) Insulin resistance accelerates muscle protein degradation: Activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling. Endocrinology 147: 4160-4168. (Pubitemid 44268367)
57. Bassil MS, Gougeon R (2013) Muscle protein anabolism in type 2 diabetes. Curr Opin Clin Nutr Metab Care 16: 83-88.
58. Sishi B, Loos B, Ellis B, Smith W, du Toit EF, et al. (2011) Diet-induced obesity alters signalling pathways and induces atrophy and apoptosis in skeletal muscle in a prediabetic rat model. Exp Physiol 96: 179-193.