Effects of growth hormone and insulin-like growth factor I on muscle in mouse models of human growth disorders

Hormone Research

Volumn 66, Issue SUPPL. 1, 2007, Pages 26-34

  Clark, Ryan P ^a   Schuenke, Mark D ^a   Keeton, Stephanie M ^a   Staron, Robert S ^a   Kopchick, John J ^a,b  

^a OHIO UNIVERSITY   (United States)

^b OHIO UNIVERSITY   (United States)

Author keywords

Growth hormone; Growth hormone receptor gene disruption; Insulin like growth factor I; Mouse models; Muscle

Indexed keywords

ESTRADIOL; GROWTH HORMONE; LIOTHYRONINE; RECOMBINANT SOMATOMEDIN C; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; THYROXINE;

BONE DEVELOPMENT; CARBOHYDRATE METABOLISM; CELL STRUCTURE; CONFERENCE PAPER; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG INTERMITTENT THERAPY; EXPERIMENTAL MODEL; GROWTH DISORDER; GROWTH HORMONE DEFICIENCY; HORMONAL REGULATION; HORMONE ACTION; HORMONE RESISTANCE; HORMONE SUBSTITUTION; HUMAN; HYPOPLASIA; INSULIN SENSITIVITY; INTRAUTERINE GROWTH RETARDATION; LIPID METABOLISM; MOTONEURON; MUSCLE CELL; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PUBERTY; TRANSGENIC MOUSE;

ANIMALS; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; GROWTH DISORDERS; GROWTH HORMONE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, KNOCKOUT; MUSCLE FIBERS; MUSCLES;

EID: 33846554819     PISSN: 03010163     EISSN: None     Source Type: Journal    
DOI: 10.1159/000096620     Document Type: Conference Paper

References (90)

1. Pette D, Staron RS: Mammalian skeletal muscle fiber type transitions. Int Rev Cytol 1997;170:143-223.
2. Pette D, Staron RS: The molecular diversity of mammalian muscle fibers. News Physiol Sci 1993;8:153-157.
3. Grossman EJ, Roy RR, Talmadge RJ, Zhong H, Edgerton VR: Effects of inactivity on myosin heavy chain composition and size of rat soleus fibers. Muscle Nerve 1998;21:375-389.
4. Gundersen K, Leberer E, Lomo T, Pette D, Staron RS: Fibre types, calcium-sequestering proteins and metabolic enzymes in denervated and chronically stimulated muscles of the rat. J Physiol 1988;398:177-189.
5. Hamalainen N, Pette D: Slow-to-fast transitions in myosin expression of rat soleus muscle by phasic high-frequency stimulation. FEBS Lett 1996;399:220-222.
6. Huey KA, Haddad F, Qin AX, Baldwin KM: Transcriptional regulation of the type I myosin heavy chain gene in denervated rat soleus. Am J Physiol Cell Physiol 2003;284: C738-C748.
7. Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, Wu H, Zhu W, Bassel-Duby R, Williams RS: A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 1998;12:2499-2509.
8. Chen L, Lund PK, Burgess SB, Rudisch BE, McIlwain DL: Growth hormone, insulin-like growth factor I, and motoneuron size. J Neurobiol 1997;32:202-212.
9. Parsons SA, Banks GB, Rowland JA, Coschigano KT, Kopchick JJ, Waters MJ, Noakes PG: Genetic disruption of the growth hormone receptor does not influence motoneuron survival in the developing mouse. Int J Dev Biol 2003;47:41-49.
10. Messi ML, Delbono O: Target-derived trophic effect on skeletal muscle innervation in senescent mice. J Neurosci 2003;23:1351-1359.
11. Dobrowolny G, Giacinti C, Pelosi L, Nicoletti C, Winn N, Barberi L, Molinaro M, Rosenthal N, Musaro A: Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model. J Cell Biol 2005;168:193-199.
12. Everitt AV, Terry V, Phillips MJ, Kerry HM, Shorey CD: Morphometric analysis of gastrocnemius muscle fiber size and fiber proportions in the hypophysectomized rat after prolonged administration of growth hormone or thyroxine. Growth Dev Aging 1996;60:85-93.
13. Roy RR, Tri C, Grossman EJ, Talmadge RJ, Grindeland RE, Mukku VR, Edgerton VR: IGF-I, growth hormone, and/or exercise effects on non-weight-bearing soleus of hypophysectomized rats. J Appl Physiol 1996;81:302-311.
14. Yamaguchi A, Sakuma K, Morita I, Soya H, Takeda H, Katsuta S: Changes in fibre types in rat soleus and plantaris muscles following hypophysectomy and compensatory overload. Acta Physiol Scand 1996;158:89-95.
15. Loughna PT, Bates PC: Interactions between growth hormone and nutrition in hypophysectomised rats: skeletal muscle myosin heavy chain mRNA levels. Biochem Biophys Res Commun 1994;198:97-102.
16. Ayling CM, Moreland BH, Zanelli JM, Schulster D: Human growth hormone treatment of hypophysectomized rats increases the proportion of type-1 fibres in skeletal muscle. J Endocrinol 1989;123:429-435.
17. Fitts RH, Winder WW, Brooke MH, Kaiser KK, Holloszy JO: Contractile, biochemical, and histochemical properties of thyrotoxic rat soleus muscle. Am J Physiol 1980;238: C14-C20.
18. Larsson L, Yu F: Gender-related differences in the regulatory influence of thyroid hormone on the expression of myosin isoforms in young and old rats. Acta Physiol Scand 1997;159:81-89.
19. Aroniadou-Anderjaska V, Lemon PW, Gilloteaux J: Effects of exogenous growth hormone on skeletal muscle of young female rats. Tissue Cell 1996;28:719-724.
20. Florini JR, Ewton DZ: Skeletal muscle fiber types and myosin ATPase activity do not change with age or growth hormone administration. J Gerontol 1989;44:B110-B117.
21. Dalla Libera L, Ravara B, Volterrani M, Gobbo V, Della Barbera M, Angelini A, Danieli Betto D, Germinario E, Vescovo G: Beneficial effects of GH/IGF-1 on skeletal muscle atrophy and function in experimental heart failure. Am J Physiol Cell Physiol 2004;286: C138-C144.
22. Daugaard JR, Laustsen JL, Hansen BS, Richter EA: Growth hormone induces muscle fibre type transformation in growth hormone-deficient rats. Acta Physiol Scand 1998;164:119-126.
23. Daugaard JR, Bramnert M, Manhem P, Endre T, Groop LC, Lofman M, Richter EA: Effect of 6 months of GH treatment on myosin heavy chain composition in GH-deficient patients. Eur J Endocrinol 1999;141:342-349.
24. Jaffe CA, Turgeon DK, Lown K, Demott-Friberg R, Watkins PB: Growth hormone secretion pattern is an independent regulator of growth hormone actions in humans. Am J Physiol Endocrinol Metab 2002;283:E1008-E1015.
25. Isgaard J, Carlsson L, Isaksson OG, Jansson JO: Pulsatile intravenous growth hormone (GH) infusion to hypophysectomized rats increases insulin-like growth factor I messenger ribonucleic acid in skeletal tissues more effectively than continuous GH infusion. Endocrinology 1988;123:2605-2610.
26. Polla B, Bottinelli R, Sandoli D, Sardi C, Reggiani C: Cortisone-induced changes in myosin heavy chain distribution in respiratory and hindlimb muscles. Acta Physiol Scand 1994;151:353-361.
27. Dudley GA, Portanova R: Histochemical characteristics of soleus muscle in hGH transgenic mice. Proc Soc Exp Biol Med 1987;185:403-408.
28. Hikida RS, Knapp JR, Chen WY, Gozdanovic JA, Kopchick JJ: Effects of bovine growth hormone analogs on mouse skeletal muscle structure. Growth Dev Aging 1995;59:121-128.
29. Casse AH, Desplanches D, Mayet-Sornay MH, Raccurt M, Jegou S, Morel G: Growth hormone receptor expression in atrophying muscle fibers of rats. Endocrinology 2003;144:3692-3697.
30. Fournier M, Lewis MI: Influences of IGF-I gene disruption on the cellular profile of the diaphragm. Am J Physiol Endocrinol Metab 2000;278:E707-E715.
31. Musaro A, McCullagh K, Paul A, Houghton L, Dobrowolny G, Molinaro M, Barton ER, Sweeney HL, Rosenthal N: Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 2001;27:195-200.
32. Hameed M, Lange KH, Andersen JL, Schjerling P, Kjaer M, Harridge SD, Goldspink G: The effect of recombinant human growth hormone and resistance training on IGF-I mRNA expression in the muscles of elderly men. J Physiol 2004;555:231-240.
33. Iida K, Itoh E, Kim DS, del Rincon JP, Coschigano KT, Kopchick JJ, Thorner MO: Muscle mechano growth factor is preferentially induced by growth hormone in growth hormone-deficient lit/lit mice. J Physiol 2004;560:341-349.
34. Jacquemin V, Furling D, Bigot A, Butler-Browne GS, Mouly V: IGF-1 induces human myotube hypertrophy by increasing cell recruitment. Exp Cell Res 2004;299:148-158.
35. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ: Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 2001;3:1009-1013.
36. Semsarian C, Sutrave P, Richmond DR, Graham RM: Insulin-like growth factor (IGF-I) induces myotube hypertrophy associated with an increase in anaerobic glycolysis in a clonal skeletal-muscle cell model. Biochem J 1999;339(Pt 2):443-451.
37. Paul AC, Rosenthal N: Different modes of hypertrophy in skeletal muscle fibers. J Cell Biol 2002;156:751-760.
38. Barton-Davis ER, Shoturma DI, Musaro A, Rosenthal N, Sweeney HL: Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function. Proc Natl Acad Sci USA 1998;95:15603-15607.
39. Coleman ME, DeMayo F, Yin KC, Lee HM, Geske R, Montgomery C, Schwartz RJ: Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J Biol Chem 1995;270:12109-12116.
40. Fernandez AM, Dupont J, Farrar RP, Lee S, Stannard B, Le Roith D: Muscle-specific inactivation of the IGF-I receptor induces compensatory hyperplasia in skeletal muscle. J Clin Invest 2002;109:347-355.
41. Adams GR, Haddad F: The relationships among IGF-1, DNA content, and protein accumulation during skeletal muscle hypertrophy. J Appl Physiol 1996;81:2509-2516.
42. Fiorotto ML, Schwartz RJ, Delaughter MC: Persistent IGF-I overexpression in skeletal muscle transiently enhances DNA accretion and growth. FASEB J 2003;17:59-60.
43. Rosenblatt JD, Parry DJ: Gamma irradiation prevents compensatory hypertrophy of overloaded mouse extensor digitorum longus muscle. J Appl Physiol 1992;73:2538-2543.
44. Roy RR, Monke SR, Allen DL, Edgerton VR: Modulation of myonuclear number in functionally overloaded and exercised rat plantaris fibers. J Appl Physiol 1999;87:634-642.
45. Chakravarthy MV, Abraha TW, Schwartz RJ, Fiorotto ML, Booth FW: Insulin-like growth factor-I extends in vitro replicative life span of skeletal muscle satellite cells by enhancing G1/S cell cycle progression via the activation of phosphatidylinositol 3′-kinase/Akt signaling pathway. J Biol Chem 2000;275:35942-35952.
46. Machida S, Spangenburg EE, Booth FW: Forkhead transcription factor FoxO1 transduces insulin-like growth factor's signal to p27Kip1 in primary skeletal muscle satellite cells. J Cell Physiol 2003;196:523-531.
47. Adams GR, McCue SA: Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J Appl Physiol 1998;84:1716-1722.
48. Kopchick JJ, Laron Z: Is the Laron mouse an accurate model of Laron syndrome? Mol Genet Metab 1999;68:232-236.
49. Zhou Y, Xu BC, Maheshwari HG, He L, Reed M, Lozykowski M, Okada S, Cataldo L, Coschigamo K, Wagner TE, Baumann G, Kopchick JJ: A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse). Proc Natl Acad Sci USA 1997;94:13215-13220.
50. Coschigano KT, Holland AN, Riders ME, List EO, Flyvbjerg A, Kopchick JJ: Deletion, but not antagonism, of the mouse growth hormone receptor results in severely decreased body weights, insulin, and insulin-like growth factor I levels and increased life span. Endocrinology 2003;144:3799-3810.
51. Li Y, Knapp JR, Kopchick JJ: Enlargement of interscapular brown adipose tissue in growth hormone antagonist transgenic and in growth hormone receptor gene-disrupted dwarf mice. Exp Biol Med (Maywood) 2003;228:207-215.
52. Berryman DE, List EO, Coschigano KT, Behar K, Kim JK, Kopchick JJ: Comparing adiposity profiles in three mouse models with altered GH signaling. Growth Horm IGF Res 2004;14:309-318.
53. Egecioglu E, Bjursell M, Ljungberg A, Dickson SL, Kopchick JJ, Bergstrom G, Svensson L, Oscarsson J, Tornell J, Bohlooly-Y M: Growth hormone receptor deficiency results in blunted ghrelin feeding response, obesity, and hypolipidemia in mice. Am J Physiol Endocrinol Metab 2006;290:E317-E325.
54. Nass R, Liu J, Hellmann P, Coschigano KT, Gaylinn B, Berryman DE, Kopchick JJ, Thorner MO: Chronic changes in peripheral growth hormone levels do not affect ghrelin stomach mRNA expression and serum ghrelin levels in three transgenic mouse models. J Neuroendocrinol 2004;16:669-675.
55. Venken K, Schuit F, Van Lommel L, Tsukamoto K, Kopchick JJ, Coschigano K, Ohlsson C, Moverare S, Boonen S, Bouillon R, Vanderschueren D: Growth without growth hormone receptor: estradiol is a major growth hormone-independent regulator of hepatic IGF-I synthesis. J Bone Miner Res 2005;20:2138-2149.
56. Chandrashekar V, Bartke A, Awoniyi CA, Tsai-Morris CH, Dufau ML, Russell LD, Kopchick JJ: Testicular endocrine function in GH receptor gene disrupted mice. Endocrinology 2001;142:3443-3450.
57. Keene DE, Suescun MO, Bostwick MG, Chandrashekar V, Bartke A, Kopchick JJ: Puberty is delayed in male growth hormone receptor gene-disrupted mice. J Androl 2002;23:661-668.
58. Zaczek D, Hammond J, Suen L, Wandji S, Service D, Bartke A, Chandrashekar V, Coschigano K, Kopchick J: Impact of growth hormone resistance on female reproductive function: new insights from growth hormone receptor knockout mice. Biol Reprod 2002;67:1115-1124.
59. Kinney BA, Coschigano KT, Kopchick JJ, Steger RW, Bartke A: Evidence that age-induced decline in memory retention is delayed in growth hormone resistant GH-RKO (Laron) mice. Physiol Behav 2001;72:653-660.
60. Hauck SJ, Hunter WS, Danilovich N, Kopchick JJ, Bartke A: Reduced levels of thyroid hormones, insulin, and glucose, and lower body core temperature in the growth hormone receptor/binding protein knockout mouse. Exp Biol Med (Maywood) 2001;226:552-558.
61. Al-Regaiey KA, Masternak MM, Bonkowski M, Sun L, Bartke A: Long-lived growth hormone receptor knockout mice: interaction of reduced insulin-like growth factor I/insulin signaling and caloric restriction. Endocrinology 2005;146:851-860.
62. Strobl JS, Thomas MJ: Human growth hormone. Pharmacol Rev 1994;46:1-34.
63. Colao A, Di Somma C, Spiezia S, Filippella M, Pivonello R, Lombardi G: Effect of growth hormone (GH) and/or testosterone replacement on the prostate in GH-deficient adult patients. J Clin Endocrinol Metab 2003;88:88-94.
64. Colao A, Spiezia S, Di Somma C, Marzullo P, Cerbone G, Pivonello R, Faggiano A, Lombardi G: Effect of GH and/or testosterone deficiency on the prostate: an ultrasonographic and endocrine study in GH-deficient adult patients. Eur J Endocrinol 2000;143:61-69.
65. Corpas E, Harman SM, Blackman MR: Human growth hormone and human aging. Endocr Rev 1993;14:20-39.
66. Liu JL, Coschigano KT, Robertson K, Lipsett M, Guo Y, Kopchick JJ, Kumar U, Liu YL: Disruption of growth hormone receptor gene causes diminished pancreatic islet size and increased insulin sensitivity in mice. Am J Physiol Endocrinol Metab 2004;287: E405-E413.
67. Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A: Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 1993;75:59-72.
68. Baker J, Liu JP, Robertson EJ, Efstratiadis A: Role of insulin-like growth factors in embryonic and postnatal growth. Cell 1993;75:73-82.
69. Wang J, Zhou J, Bondy CA: Igf1 promotes longitudinal bone growth by insulin-like actions augmenting chondrocyte hypertrophy. FASEB J 1999;13:1985-1990.
70. Wang J, Zhou J, Powell-Braxton L, Bondy C: Effects of Igf1 gene deletion on postnatal growth patterns. Endocrinology 1999;140:3391-3394.
71. Baker J, Hardy MP, Zhou J, Bondy C, Lupu F, Bellve AR, Efstratiadis A: Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 1996;10:903-918.
72. Kadakia R, Arraztoa JA, Bondy C, Zhou J: Granulosa cell proliferation is impaired in the Igf1 null ovary. Growth Horm IGF Res 2001;11:220-224.
73. Zhou J, Kumar TR, Matzuk MM, Bondy C: Insulin-like growth factor I regulates gonadotropin responsiveness in the murine ovary. Mol Endocrinol 1997;11:1924-1933.
74. McAlarney ME, Rizos M, Rocca EG, Nicolay OF, Efstratiadis S: The quantitative and qualitative analysis of the craniofacial skeleton of mice lacking the IGF-I gene. Clin Orthod Res 2001;4:206-219.
75. Beck KD, Powell-Braxton L, Widmer HR, Valverde J, Hefti F: Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 1995;14:717-730.
76. Camarero G, Villar MA, Contreras J, Fernandez-Moreno C, Pichel JG, Avendano C, Varela-Nieto I: Cochlear abnormalities in insulin-like growth factor-1 mouse mutants. Hear Res 2002;170:2-11.
77. Cediel R, Riquelme R, Contreras J, Diaz A, Varela-Nieto I: Sensorineural hearing loss in insulin-like growth factor I-null mice: a new model of human deafness. Eur J Neurosci 2006;23:587-590.
78. Sjogren K, Liu JL, Blad K, Skrtic S, Vidal O, Wallenius V, LeRoith D, Tornell J, Isaksson OG, Jansson JO, Ohlsson C: Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Proc Natl Acad Sci USA 1999;96:7088-7092.
79. Yakar S, Liu JL, Stannard B, Butler A, Accili D, Sauer B, LeRoith D: Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc Natl Acad Sci USA 1999;96:7324-7329.
80. Sjogren K, Sheng M, Moverare S, Liu JL, Wallenius K, Tornell J, Isaksson O, Jansson JO, Mohan S, Ohlsson C: Effects of liver-derived insulin-like growth factor I on bone metabolism in mice. J Bone Miner Res 2002;17:1977-1987.
81. Sjogren K, Wallenius K, Liu JL, Bohlooly-Y M, Pacini G, Svensson L, Tornell J, Isaksson OG, Ahren B, Jansson JO, Ohlsson C: Liver-derived IGF-I is of importance for normal carbohydrate and lipid metabolism. Diabetes 2001;50:1539-1545.
82. Yu R, Yakar S, Liu YL, Lu Y, LeRoith D, Miao D, Liu JL: Liver-specific IGF-I gene deficient mice exhibit accelerated diabetes in response to streptozotocin, associated with early onset of insulin resistance. Mol Cell Endocrinol 2003;204:31-42.
83. Yakar S, Liu JL, Fernandez AM, Wu Y, Schally AV, Frystyk J, Chernausek SD, Mejia W, Le Roith D: Liver-specific igf-1 gene deletion leads to muscle insulin insensitivity. Diabetes 2001;50:1110-1118.
84. Yakar S, Setser J, Zhao H, Stannard B, Haluzik M, Glatt V, Bouxsein ML, Kopchick JJ, LeRoith D: Inhibition of growth hormone action improves insulin sensitivity in liver IGF-1-deficient mice. J Clin Invest 2004;113:96-105.
85. Wallenius K, Sjogren K, Peng XD, Park S, Wallenius V, Liu JL, Umaerus M, Wennbo H, Isaksson O, Frohman L, Kineman R, Ohlsson C, Jansson JO: Liver-derived IGF-I regulates GH secretion at the pituitary level in mice. Endocrinology 2001;142:4762-4770.
86. Bonapace G, Concolino D, Formicola S, Strisciuglio P: A novel mutation in a patient with insulin-like growth factor 1 (IGF1) deficiency. J Med Genet 2003;40:913-917.
87. Walenkamp MJ, Karperien M, Pereira AM, Hilhorst-Hofstee Y, van Doorn J, Chen JW, Mohan S, Denley A, Forbes B, van Duyvenvoorde HA, van Thiel SW, Sluimers CA, Bax JJ, de Laat JA, Breuning MB, Romijn JA, Wit JM: Homozygous and heterozygous expression of a novel insulin-like growth factor-I mutation. J Clin Endocrinol Metab 2005;90:2855-2864.
88. Woods KA, Camacho-Hubner C, Savage MO, Clark AJ: Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N Engl J Med 1996;335:1363-1367.
89. Abuzzahab MJ, Schneider A, Goddard A, Grigorescu F, Lautier C, Keller E, Kiess W, Klammt J, Kratzsch J, Osgood D, Pfaffle R, Raile K, Seidel B, Smith RJ, Chernausek SD, Intrauterine Growth Retardation (IUGR) Study Group: IGF-I receptor mutations resulting in intrauterine and postnatal growth retardation. N Engl J Med 2003;349:2211-2222.
90. Kawashima Y, Kanzaki S, Yang F, Kinoshita T, Hanaki K, Nagaishi J, Ohtsuka Y, Hisatome I, Ninomoya H, Nanba E, Fukushima T, Takahashi S: Mutation at cleavage site of insulin-like growth factor receptor in a short-stature child born with intrauterine growth retardation. J Clin Endocrinol Metab 2005;90:4679-4687.