Skeletal muscle catabolism in trinitrobenzene sulfonic acid-induced murine colitis

Metabolism: Clinical and Experimental

Volumn 59, Issue 11, 2010, Pages 1680-1690

  Puleo, Frances ^a   Meirelles, Katia ^a   Navaratnarajah, Maithili ^a   Fitzpatrick, Leo ^a   Shumate, Margaret L ^a   Cooney, Robert N ^a   Lang, Charles H ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MESSENGER RNA; MUSCLE PROTEIN; MUSCLE RING FINGER 1 PROTEIN; PROTEASOME; SOMATOMEDIN; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 3; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN PROTEIN LIGASE E3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; CATABOLISM; COLITIS; CONTROLLED STUDY; ENTERITIS; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SKELETAL MUSCLE;

ANIMALS; COLITIS; INFLAMMATION MEDIATORS; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED C57BL; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; TRINITROBENZENESULFONIC ACID;

EID: 78049264772     PISSN: 00260495     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.metabol.2010.03.021     Document Type: Article

References (65)

1. Griffiths A.M., Nguyen P., and Smith C. Growth and clinical course of children with Crohn's disease Gut 34 1993 939 943
2. Motil K.J., Grand R.J., and vis-Kraft L. Growth failure in children with inflammatory bowel disease: a prospective study Gastroenterology 105 1993 681 691
3. Ballinger A. Fundamental mechanisms of growth failure in inflammatory bowel disease Horm Res 58 Suppl 1 2002 7 10
4. Ballinger A.B., Azooz O., and El-Haj T. Growth failure occurs through a decrease in insulin-like growth factor 1 which is independent of undernutrition in a rat model of colitis Gut 46 2000 694 700
5. Shamir R., Phillip M., and Levine A. Growth retardation in pediatric Crohn's disease: pathogenesis and interventions Inflamm Bowel Dis 13 2007 620 628
6. Le R.D., Bondy C., and Yakar S. The somatomedin hypothesis: 2001 Endocr Rev 22 2001 53 74
7. Olney R.C. Regulation of bone mass by growth hormone Med Pediatr Oncol 41 2003 228 234
8. Clemmons D.R. Role of IGF-I in skeletal muscle mass maintenance Trends Endocrinol Metab 20 2009 349 356
9. Frost R.A., and Lang C.H. Alteration of somatotropic function by proinflammatory cytokines J Anim Sci 82 E-Suppl 2004 E100 E109
10. Denson L.A., Held M.A., and Menon R.K. Interleukin-6 inhibits hepatic growth hormone signaling via upregulation of Cis and Socs-3 Am J Physiol Gastrointest Liver Physiol 284 2003 G646 G654
11. DiFedele L.M., He J., and Bonkowski E.L. Tumor necrosis factor alpha blockade restores growth hormone signaling in murine colitis Gastroenterology 128 2005 1278 1291
12. Sawczenko A., Azooz O., and Paraszczuk J. Intestinal inflammation-induced growth retardation acts through IL-6 in rats and depends on the -174 IL-6 G/C polymorphism in children Proc Natl Acad Sci U S A 102 2005 13260 13265
13. Lang C.H., Hong-Brown L., and Frost R.A. Cytokine inhibition of JAK-STAT signaling: a new mechanism of growth hormone resistance Pediatr Nephrol 20 2005 306 312
14. Firth S.M., and Baxter R.C. Cellular actions of the insulin-like growth factor binding proteins Endocr Rev 23 2002 824 854
15. Frost R.A., and Lang C.H. Differential effects of insulin-like growth factor I (IGF-I) and IGF- binding protein-1 on protein metabolism in human skeletal muscle cells Endocrinology 140 1999 3962 3970
16. Lang C.H., Vary T.C., and Frost R.A. Acute in vivo elevation of insulin-like growth factor (IGF) binding protein-1 decreases plasma free IGF-I and muscle protein synthesis Endocrinology 144 2003 3922 3933
17. Eivindson M., Gronbaek H., and Flyvbjerg A. The insulin-like growth factor (IGF)-system in active ulcerative colitis and Crohn's disease: relations to disease activity and corticosteroid treatment Growth Horm IGF Res 17 2007 33 40
18. Eivindson M., Gronbaek H., and Skogstrand K. The insulin-like growth factor (IGF) system and its relation to infliximab treatment in adult patients with Crohn's disease Scand J Gastroenterol 42 2007 464 470
19. Mercier S., Breuille D., and Mosoni L. Chronic inflammation alters protein metabolism in several organs of adult rats J Nutr 132 2002 1921 1928
20. El Y.M., Breuille D., and Papet I. Increased tissue protein synthesis during spontaneous inflammatory bowel disease in HLA-B27 rats Clin Sci (Lond) 105 2003 437 446
21. Lecker S.H., Solomon V., and Mitch W.E. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states J Nutr 129 1999 227S 237S
22. Roos-Mattjus P., and Sistonen L. The ubiquitin-proteasome pathway Ann Med 36 2004 285 295
23. Bodine S.C., Latres E., and Baumhueter S. Identification of ubiquitin ligases required for skeletal muscle atrophy Science 294 2001 1704 1708
24. Frost R.A., Nystrom G.J., and Jefferson L.S. Hormone, cytokine, and nutritional regulation of sepsis-induced increases in atrogin-1 and MuRF1 in skeletal muscle Am J Physiol Endocrinol Metab 292 2007 E501 E512
25. Krawiec B.J., Nystrom G.J., and Frost R.A. AMP-activated protein kinase agonists increase mRNA content of the muscle-specific ubiquitin ligases MAFbx and MuRF1 in C2C12 cells Am J Physiol Endocrinol Metab 292 2007 E1555 E1567
26. Li H.H., Kedar V., and Zhang C. Atrogin-1/muscle atrophy F-box inhibits calcineurin- dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex J Clin Invest 114 2004 1058 1071
27. Nystrom G., Pruznak A., and Huber D. Local insulin-like growth factor I prevents sepsis- induced muscle atrophy Metabolism 58 2009 787 797
28. Sacheck J.M., Ohtsuka A., and McLary S.C. IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 Am J Physiol Endocrinol Metab 287 2004 E591 E601
29. Morris G.P., Beck P.L., and Herridge M.S. Hapten-induced model of chronic inflammation and ulceration in the rat colon Gastroenterology 96 1989 795 803
30. Zhang X.J., Cortiella J., and Doyle D. Ketamine anesthesia causes greater muscle catabolism in rabbits than does propofol J Nutr Biochem 8 1997 133 139
31. Garlick P.J., McNurlan M.A., and Preedy V.R. A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of [3H]phenylalanine Biochem J 192 1980 719 723
32. Lang C.H., and Frost R.A. Differential effect of sepsis on ability of leucine and IGF-I to stimulate muscle translation initiation Am J Physiol Endocrinol Metab 287 2004 E721 E730
33. Lang C.H., and Frost R.A. Endotoxin disrupts the leucine-signaling pathway involving phosphorylation of mTOR, 4E-BP1, and S6K1 in skeletal muscle J Cell Physiol 203 2005 144 155
34. Vary T.C., Frost R.A., and Lang C.H. Acute alcohol intoxication increases atrogin-1 and MuRF1 mRNA without increasing proteolysis in skeletal muscle Am J Physiol Regul Integr Comp Physiol 294 2008 R1777 R1789
35. Waalkes T.P., and Udenfriend S. A fluorometric method for the estimation of tyrosine in plasma and tissues J Lab Clin Med 50 1957 733 736
36. Solomon V., and Goldberg A.L. Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts J Biol Chem 271 1996 26690 26697
37. Wang X., Hu Z., and Hu J. Insulin resistance accelerates muscle protein degradation: activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling Endocrinology 147 2006 4160 4168
38. Frost R.A., Nystrom G.J., and Lang C.H. Lipopolysaccharide regulates proinflammatory cytokine expression in mouse myoblasts and skeletal muscle Am J Physiol Regul Integr Comp Physiol 283 2002 R698 R709
39. Frost R.A., Nystrom G.J., and Lang C.H. Lipopolysaccharide stimulates nitric oxide synthase-2 expression in murine skeletal muscle and C(2)C(12) myoblasts via Toll-like receptor-4 and c- Jun NH(2)-terminal kinase pathways Am J Physiol Cell Physiol 287 2004 C1605 C1615
40. Lang C.H., Pruznak A.M., and Nystrom G.J. Alcohol-induced decrease in muscle protein synthesis associated with increased binding of mTOR and raptor: comparable effects in young and mature rats Nutr Metab (Lond) 6 2009 4
41. Lang C.H., Frost R.A., and Nairn A.C. TNF-alpha impairs heart and skeletal muscle protein synthesis by altering translation initiation Am J Physiol Endocrinol Metab 282 2002 E336 E347
42. Lang C.H., and Frost R.A. Glucocorticoids and TNFalpha interact cooperatively to mediate sepsis-induced leucine resistance in skeletal muscle Mol Med 12 2006 291 299
43. Lang C.H., and Frost R.A. Sepsis-induced suppression of skeletal muscle translation initiation mediated by tumor necrosis factor alpha Metabolism 56 2007 49 57
44. Lang C.H., Frost R.A., and Vary T.C. Regulation of muscle protein synthesis during sepsis and inflammation Am J Physiol Endocrinol Metab 293 2007 E453 E459
45. Pruznak A.M., Hong-Brown L., and Lantry R. Skeletal and cardiac myopathy in HIV-1 transgenic rats Am J Physiol Endocrinol Metab 295 2008 E964 E973
46. Theiss A.L., Fruchtman S., and Lund P.K. Growth factors in inflammatory bowel disease: the actions and interactions of growth hormone and insulin-like growth factor-I Inflamm Bowel Dis 10 2004 871 880
47. Mitsuyama K., Sata M., and Rose-John S. Interleukin-6 trans-signaling in inflammatory bowel disease Cytokine Growth Factor Rev 17 2006 451 461
48. Frystyk J. Utility of free IGF-I measurements Pituitary 10 2007 181 187
49. Bereket A., Lang C.H., and Blethen S.L. Growth hormone treatment in growth retarded children with end stage renal failure: effect on free/dissociable IGF-I levels J Pediatr Endocrinol Metab 10 1997 197 202
50. Co Ng L.L., Lang C.H., and Bereket A. Effect of hyperthyroidism on insulin-like growth factor-I (IGF-I) and IGF-binding proteins in adolescent children J Pediatr Endocrinol Metab 13 2000 1073 1080
51. Lang C.H., Liu X., and Nystrom G. Acute effects of growth hormone in alcohol-fed rats Alcohol Alcohol 35 2000 148 158
52. Laursen T., Flyvbjerg A., and Jorgensen J.O. Stimulation of the 150-kilodalton insulin-like growth factor-binding protein-3 ternary complex by continuous and pulsatile patterns of growth hormone (GH) administration in GH-deficient patients J Clin Endocrinol Metab 85 2000 4310 4314
53. Belizon A., Kirman I., and Balik E. Major surgical trauma induces proteolysis of insulin-like growth factor binding protein-3 in transgenic mice and is associated with a rapid increase in circulating levels of matrix metalloproteinase-9 Surg Endosc 21 2007 653 658
54. Barreca A., Ketelslegers J.M., and Arvigo M. Decreased acid-labile subunit (ALS) levels by endotoxin in vivo and by interleukin-1beta in vitro Growth Horm IGF Res 8 1998 217 223
55. Benbassat C.A., Lazarus D.D., and Cichy S.B. Interleukin-1 alpha (IL-1 alpha) and tumor necrosis factor alpha (TNF alpha) regulate insulin-like growth factor binding protein-1 (IGFBP-1) levels and mRNA abundance in vivo and in vitro Horm Metab Res 31 1999 209 215
56. Delhanty P.J. Interleukin-1 beta suppresses growth hormone-induced acid-labile subunit mRNA levels and secretion in primary hepatocytes Biochem Biophys Res Commun 243 1998 269 272
57. Fan J., Char D., and Bagby G.J. Regulation of insulin-like growth factor-I (IGF-I) and IGF- binding proteins by tumor necrosis factor Am J Physiol 269 1995 R1204 R1212
58. Fan J., Wojnar M.M., and Theodorakis M. Regulation of insulin-like growth factor (IGF)-I mRNA and peptide and IGF-binding proteins by interleukin-1 Am J Physiol 270 1996 R621 R629
59. Bayol S., Loughna P.T., and Brownson C. Phenotypic expression of IGF binding protein transcripts in muscle, in vitro and in vivo Biochem Biophys Res Commun 273 2000 282 286
60. Lang C.H., Krawiec B.J., and Huber D. Sepsis and inflammatory insults downregulate IGFBP-5, but not IGFBP-4, in skeletal muscle via a TNF-dependent mechanism Am J Physiol Regul Integr Comp Physiol 290 2006 R963 R972
61. De B.F., Alonzi T., and Moretta A. Interleukin 6 causes growth impairment in transgenic mice through a decrease in insulin-like growth factor-I. A model for stunted growth in children with chronic inflammation J Clin Invest 99 1997 643 650
62. Martensson K., Chrysis D., and Savendahl L. Interleukin-1beta and TNF-alpha act in synergy to inhibit longitudinal growth in fetal rat metatarsal bones J Bone Miner Res 19 2004 1805 1812
63. Wu F., and Chakravarti S. Differential expression of inflammatory and fibrogenic genes and their regulation by NF-kappaB inhibition in a mouse model of chronic colitis J Immunol 179 2007 6988 7000
64. Kubes P., and McCafferty D.M. Nitric oxide and intestinal inflammation Am J Med 109 2000 150 158
65. Janssen S.P., Gayan-Ramirez G., and Van den B.A. Interleukin-6 causes myocardial failure and skeletal muscle atrophy in rats Circulation 111 2005 996 1005