Impaired growth and force production in skeletal muscles of young partially pancreatectomized rats: A model of adolescent type 1 diabetic myopathy?

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Gordon, Carly S ^a,b   Serino, Antonio S ^a,b   Krause, Matthew P ^b,c   Campbell, Jonathan E ^a,b   Cafarelli, Enzo ^a,b   Adegoke, Olasunkanmi A J ^a,b   Hawke, Thomas J ^b,c   Riddell, Michael C ^a,b  

^a YORK UNIVERSITY   (Canada)

^b YORK UNIVERSITY   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E BINDING PROTEIN 1; S6 KINASE; ANALGESIC AGENT; KETAMINE; MTOR PROTEIN, RAT; SUCCINATE DEHYDROGENASE; TARGET OF RAPAMYCIN KINASE; XYLAZINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CONTROLLED STUDY; DIABETIC MYOPATHY; GASTROCNEMIUS MUSCLE; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE FORCE; MUSCLE GROWTH; MUSCLE MASS; MYOPATHY; NONHUMAN; PANCREAS RESECTION; PLANTARIS MUSCLE; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; SOLEUS MUSCLE; ADOLESCENT; ANIMAL; DISEASE MODEL; DRUG EFFECT; HUMAN; METABOLISM; METHODOLOGY; MUSCLE DISEASE; MUSCLE FATIGUE; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT; UBIQUITINATION;

RATTUS;

ADOLESCENT; ANALGESICS; ANIMALS; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; HUMANS; KETAMINE; MALE; MUSCLE FATIGUE; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MUSCULAR DISEASES; PANCREATECTOMY; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SUCCINATE DEHYDROGENASE; TOR SERINE-THREONINE KINASES; UBIQUITINATION; XYLAZINE;

EID: 78649514712     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014032     Document Type: Article

References (68)

1. The Diabetes Control and Complications Trial Research Group. (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329: 977-986.
2. Donaghue KC, Chiarelli F, Trotta D, Allgrove J, Dahl-Jorgensen K (2009) Microvascular and macrovascular complications associated with diabetes in children and adolescents. Pediatr Diabetes 10 Suppl 12: 195-203.
3. Hamilton J, Daneman D (2002) Deteriorating diabetes control during adolescence: Physiological or psychosocial? J Pediatr Endocrinol Metab 15(2): 115-126.
4. Mozdziak PE, Pulvermacher PM, Schultz E (2000) Unloading of juvenile muscle results in a reduced muscle size 9 wk after reloading. J Appl Physiol 88(1): 158-164.
5. Darr KC, Schultz E (1989) Hindlimb suspension suppresses muscle growth and satellite cell proliferation. J Appl Physiol 67(5): 1827-1834.
6. Reske-Nielsen E, Harmsen A, Vorre P (1977) Ultrastructure of muscle biopsies in recent, short-term and long-term juvenile diabetes. Acta Neurol Scand 55(5): 345-362.
7. Jakobsen J, Reske-Nielsen E (1986) Diffuse muscle fiber atrophy in newly diagnosed diabetes. Clin Neuropathol 5(2): 73-77.
8. Reske-Nielsen E, Gregersen G, Harmsen A, Lundbaek K (1970) Morphological abnormalities of the terminal neuromuscular apparatus in recent juvenile diabetes. Diabetologia 6(2): 104-109.
9. Reske-Nielsen E, Lundbaek K, Gregersen G, Harmsen A (1970) Pathological changes in the central and peripheral nervous system of young long-term diabetics. the terminal neuro-muscular apparatus. Diabetologia 6(2): 98-103.
10. Bonner-Weir S, Trent DF, Weir GC (1983) Partial pancreatectomy in the rat and subsequent defect in glucose-induced insulin release. J Clin Invest 71(6): 1544-1553.
11. Burke RE, Levine DN, Tsairis P, Zajac FE, 3rd (1973) Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol (Lond) 234(3): 723-748.
12. Gordon JW, Rungi AA, Inagaki H, Hood DA (2001) Effects of contractile activity on mitochondrial transcription factor A expression in skeletal muscle. J Appl Physiol 90(1): 389-396.
13. Ogilvie RW, Feeback DL (1990) A metachromatic dye-ATPase method for the simultaneous identification of skeletal muscle fiber types I, IIA, IIB and IIC. Stain Technol 65(5): 231-241.
14. Krause MP, Riddell MC, Gordon CS, Imam SA, Cafarelli E, et al. (2009) Diabetic myopathy differs between Ins2Akita+/2 and streptozotocin-induced type 1 diabetic models. J Appl Physiol 106(5): 1650-1659.
15. Crozier SJ, Kimball SR, Emmert SW, Anthony JC, Jefferson LS (2005) Oral leucine administration stimulates protein synthesis in rat skeletal muscle. J Nutr 135(3): 376-382.
16. Adegoke OA, Chevalier S, Morais JA, Gougeon R, Kimball SR, et al. (2009) Fed-state clamp stimulates cellular mechanisms of muscle protein anabolism and modulates glucose disposal in normal men. Am J Physiol Endocrinol Metab 296(1): E105-13.
17. Garlick PJ, McNurlan MA, Preedy VR (1980) A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of [3H]phenylalanine. Biochem J 192(2): 719-723.
18. Suzuki O, Yagi K (1976) A fluorometric assay for beta-phenylethylamine in rat brain. Anal Biochem 75(1): 192-200.
19. Attaix D, Ventadour S, Codran A, Bechet D, Taillandier D, et al. (2005) The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem 41: 173-186.
20. Krause MP, Riddell MC, Hawke TJ (2010) Effects of type 1 diabetes mellitus on skeletal muscle: Clinical observations and physiological mechanisms. Pediatr Diabetes. 2010 Sep 22. doi: 10.1111/j.1399-5448.2010.00699.x. [Epub ahead of print].
21. Andersen H, Poulsen PL, Mogensen CE, Jakobsen J (1996) Isokinetic muscle strength in long-term IDDM patients in relation to diabetic complications. Diabetes 45(4): 440-445.
22. Andersen H, Gadeberg PC, Brock B, Jakobsen J (1997) Muscular atrophy in diabetic neuropathy: A stereological magnetic resonance imaging study. Diabetologia 40(9): 1062-1069.
23. Andersen H (1998) Muscular endurance in long-term IDDM patients. Diabetes Care 21(4): 604-609.
24. Andersen H, Gjerstad MD, Jakobsen J (2004) Atrophy of foot muscles: A measure of diabetic neuropathy. Diabetes Care 27(10): 2382-2385.
25. Poortmans JR, Saerens P, Edelman R, Vertongen F, Dorchy H (1986) Influence of the degree of metabolic control on physical fitness in type I diabetic adolescents. Int J Sports Med 7(4): 232-235.
26. Huttunen NP, Kaar ML, Knip M, Mustonen A, Puukka R, et al. (1984) Physical fitness of children and adolescents with insulin-dependent diabetes mellitus. Ann Clin Res 16(1): 1-5.
27. Baraldi E, Monciotti C, Filippone M, Santuz P, Magagnin G, et al. (1992) Gas exchange during exercise in diabetic children. Pediatr Pulmonol 13(3): 155-160.
28. Gusso S, Hofman P, Lalande S, Cutfield W, Robinson E, et al. (2008) Impaired stroke volume and aerobic capacity in female adolescents with type 1 and type 2 diabetes mellitus. Diabetologia 51(7): 1317-1320.
29. Larsson Y, Persson B, Sterky G, Thoren C (1964) Functional adaptation to rigorous training and exercise in diabetic and nondiabetic adolescents. J Appl Physiol 19: 629-635.
30. Sterky G (1963) Physical work capacity in diabetic schoolchildren. Acta Paediatr 52: 1-10.
31. Bognetti E, Riva MC, Bonfanti R, Meschi F, Viscardi M, et al. (1998) Growth changes in children and adolescents with short-term diabetes. Diabetes Care 21(8): 1226-1229.
32. Gunczler P, Lanes R (1999) Poor metabolic control decreases the growth velocity of diabetic children. Diabetes Care 22(6): 1012.
33. Rosa JS, Galassetti PR (2009) Altered molecular adaptation to exercise in children with type 1 diabetes: Beyond hypoglycemia. Pediatr Diabetes 10(3): 213-226.
34. Caprio S, Cline G, Boulware S, Permanente C, Shulman GI, et al. (1994) Effects of puberty and diabetes on metabolism of insulin-sensitive fuels. Am J Physiol 266(6 Pt 1): E885-91.
35. Caso G, McNurlan MA (2010) Effect of insulin on whole body protein metabolism in children with type 1 diabetes. Curr Opin Clin Nutr Metab Care 13(1): 93-96.
36. Miyazaki M, Esser KA (2009) Cellular mechanisms regulating protein synthesis and skeletal muscle hypertrophy in animals. J Appl Physiol 106(4): 1367-1373.
37. Chonkar A, Hopkin R, Adeghate E, Singh J (2006) Contraction and cation contents of skeletal soleus and EDL muscles in age-matched control and diabetic rats. Ann N Y Acad Sci 1084: 442-451.
38. Cotter MA, Cameron NE, Robertson S, Ewing I (1993) Polyol pathway-related skeletal muscle contractile and morphological abnormalities in diabetic rats. Exp Physiol 78(2): 139-155.
39. Fahim MA, el-Sabban F, Davidson N (1998) Muscle contractility decrement and correlated morphology during the pathogenesis of streptozotocin-diabetic mice. Anat Rec 251(2): 240-244.
40. Lesniewski LA, Miller TA, Armstrong RB (2003) Mechanisms of force loss in diabetic mouse skeletal muscle. Muscle Nerve 28(4): 493-500.
41. McGuire M, MacDermott M (1999) The influence of streptozotocin diabetes and metformin on erythrocyte volume and on the membrane potential and the contractile characteristics of the extensor digitorum longus and soleus muscles in rats. Exp Physiol 84(6): 1051-1058.
42. Sanchez OA, Snow LM, Lowe DA, Serfass RC, Thompson LV (2005) Effects of endurance exercise-training on single-fiber contractile properties of insulintreated streptozotocin-induced diabetic rats. J Appl Physiol 99(2): 472-478.
43. Stephenson GM, O'Callaghan A, Stephenson DG (1994) Single-fiber study of contractile and biochemical properties of skeletal muscles in streptozotocininduced diabetic rats. Diabetes 43(5): 622-628.
44. Vignaud A, Ramond F, Hourde C, Keller A, Butler-Browne G, et al. (2007) Diabetes provides an unfavorable environment for muscle mass and function after muscle injury in mice. Pathobiology 74(5): 291-300.
45. Goldberg AL (1979) Influence of insulin and contractile activity on muscle size and protein balance. Diabetes 28 Suppl 1: 18.
46. Johnston AP, Campbell JE, Found JG, Riddell MC, Hawke TJ (2007) Streptozotocin induces G2 arrest in skeletal muscle myoblasts and impairs muscle growth in vivo. Am J Physiol, Cell Physiol 292(3): C1033-40.
47. Chiarelli F, Giannini C, Mohn A (2004) Growth, growth factors and diabetes. Eur J Endocrinol 151(Suppl 3): U109-17.
48. Tattersall RB, Pyke DA (1973) Growth in diabetic children. studies in identical twins. Lancet 2(7838): 1105-1109.
49. Vanelli M, de Fanti A, Adinolfi B, Ghizzoni L (1992) Clinical data regarding the growth of diabetic children. Horm Res 37 Suppl 3: 65-69.
50. Du Caju MV, Rooman RP, op de Beeck L (1995) Longitudinal data on growth and final height in diabetic children. Pediatr Res 38(4): 607-611.
51. Brown M, Ahmed ML, Clayton KL, Dunger DB (1994) Growth during childhood and final height in type 1 diabetes. Diabet Med 11(2): 182-187.
52. Armstrong RB, Gollnick PD, Ianuzzo CD (1975) Histochemical properties of skeletal muscle fibers in streptozotocin-diabetic rats. Cell Tissue Res 162(3): 387-394.
53. Oertel G (1988) Morphometric analysis of normal skeletal muscles in infancy, childhood and adolescence. an autopsy study. J Neurol Sci 88(1-3): 303-313.
54. Spangenburg EE, Le Roith D, Ward CW, Bodine SC (2008) A functional insulin-like growth factor receptor is not necessary for load-induced skeletal muscle hypertrophy. J Physiol 586(1): 283-291.
55. Izumiya Y, Hopkins T, Morris C, Sato K, Zeng L, et al. (2008) Fast/Glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab 7(2): 159-172.
56. Anthony JC, Lang CH, Crozier SJ, Anthony TG, MacLean DA, et al. (2002) Contribution of insulin to the translational control of protein synthesis in skeletal muscle by leucine. Am J Physiol Endocrinol Metab 282(5): E1092-101.
57. Charlton M, Nair KS (1998) Protein metabolism in insulin-dependent diabetes mellitus. J Nutr 128(2 Suppl): 323S-27S.
58. Shah OJ, Anthony JC, Kimball SR, Jefferson LS (2000) 4E-BP1 and S6K1: Translational integration sites for nutritional and hormonal information in muscle. Am J Physiol Endocrinol Metab 279(4): E715-29.
59. Anthony JC, Reiter AK, Anthony TG, Crozier SJ, Lang CH, et al. (2002) Orally administered leucine enhances protein synthesis in skeletal muscle of diabetic rats in the absence of increases in 4E-BP1 or S6K1 phosphorylation. Diabetes 51(4): 928-936.
60. Riddell MC, Iscoe KE (2006) Physical activity, sport, and pediatric diabetes. Pediatr.Diabetes 7(1): 60-70.
61. Fricke O, Seewi O, Semler O, Tutlewski B, Stabrey A, et al. (2008) The influence of auxology and long-term glycemic control on muscle function in children and adolescents with type 1 diabetes mellitus. J Musculoskelet Neuronal Interact 8(2): 188-195.
62. Fritzsche K, Bluher M, Schering S, Buchwalow IB, Kern M, et al. (2008) Metabolic profile and nitric oxide synthase expression of skeletal muscle fibers are altered in patients with type 1 diabetes. Exp Clin Endocrinol Diabetes 116(10): 606-613.
63. Crowther GJ, Milstein JM, Jubrias SA, Kushmerick MJ, Gronka RK, et al. (2003) Altered energetic properties in skeletal muscle of men with well-controlled insulin-dependent (type 1) diabetes. Am J Physiol Endocrinol Metab 284(4): E655-62.
64. Klueber KM, Feczko JD (1994) Ultrastructural, histochemical, and morphometric analysis of skeletal muscle in a murine model of type I diabetes. Anat Rec 239(1): 18-34.
65. Snow LM, Lynner CB, Nielsen EM, Neu HS, Thompson LV (2006) Advanced glycation end product in diabetic rat skeletal muscle in vivo. Pathobiology 73(5): 244-251.
66. Mizumoto R, Kawarada Y, Goshima H, Tamaki H, Sekoguchi T, et al. (1982) Carbohydrate metabolism and endocrine function in the pancreas remnant after major pancreatic resection. Am J Surg 143(2): 237-243.
67. Sommer H (1987) Functional recovery of the exocrine pancreas in rats after partial resection. Eur Surg Res 19(5): 318-322.
68. Yasugi H, Mizumoto R, Sakurai H, Honjo I (1976) Changes in carbohydrate metabolism and endocrine function of remnant pancreas after major pancreatic resection. Am J Surg 132(5): 577-580.