Growth hormone secretagogues exert differential effects on skeletal muscle calcium homeostasis in male rats depending on the peptidyl/nonpeptidyl structure

Endocrinology

Volumn 154, Issue 10, 2013, Pages 3764-3775

  Liantonio, Antonella ^a   Gramegna, Gianluca ^a   Carbonara, Giuseppe ^a   Sblendorio, Valeriana Teresa ^a   Pierno, Sabata ^a   Fraysse, Bodvaël ^b   Giannuzzi, Viviana ^a   Rizzi, Laura ^c   Torsello, Antonio ^c   Camerino, Diana Conte ^a  

^a UNIVERSITY OF BARI   (Italy)

^b INRA UMR 703   (France)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CAFFEINE; CALCIUM; CYCLOSPORIN A; GHRELIN; GROWTH HORMONE SECRETAGOGUE; THAPSIGARGIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CHEMICAL STRUCTURE; CONTROLLED STUDY; DRUG EFFECT; MALE; MUSCLE ATROPHY; MUSCLE FUNCTION; NONHUMAN; PRIORITY JOURNAL; RAT; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE;

ANIMALS; APPETITE STIMULANTS; CALCIUM SIGNALING; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CYTOSOL; GHRELIN; GROWTH HORMONE; MALE; MITOCHONDRIA, MUSCLE; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; OLIGOPEPTIDES; PIPERIDINES; PITUITARY GLAND, ANTERIOR; RATS; RATS, WISTAR; RECEPTORS, GHRELIN; SARCOLEMMA; SARCOPLASMIC RETICULUM; SPIRO COMPOUNDS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84884696191     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1334     Document Type: Article

References (68)

1. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature. 1999;402:656-660. (Pubitemid 129516334)
2. van der Lely AJ, Tschöp M, Heiman ML, Ghigo E. Biological, physiological, pathophysiological, and pharmacological aspects of ghrelin. Endocr Rev. 2004;25:426-457. (Pubitemid 38780667)
3. Smith RG, Jiang H, Sun Y. Developments in ghrelin biology and potential clinical relevance. Trends Endocrinol Metab. 2005;16:436-442. (Pubitemid 41506951)
4. Kamiji MM, Inui A. The role of ghrelin and ghrelin analogues in wasting disease. Curr Opin Clin Nutr Metab Care. 2008;11:443-451.
5. Akamizu T, Kangawa K. Ghrelin for cachexia. J Cachexia Sarcopenia Muscle. 2010;1:169-176.
6. Ueno H, Shiiya T, Nakazato M. Translational research of ghrelin. Ann NY Acad Sci. 2010;1200:120-127.
7. Ariyasu H, Iwakura H, Yamada G, Nakao K, Kangawa K, Akamizu T. Efficacy of ghrelin as a therapeutic approach for age-related physiological changes. Endocrinology. 2008;149:3722-3728. (Pubitemid 351919584)
8. Nass R, Pezzoli SS, Oliveri MC, et al. Effects of an oral ghrelin mimetic on body composition and clinical outcomes in healthy older adults: a randomized trial. Ann Intern Med. 2008;149:601-611.
9. White HK, Petrie CD, Landschulz W, et al. Effects of an oral growth hormone secretagogue in older adults. J Clin Endocrinol Metab. 2009;94:1198-1206.
10. Koshinaka K, Toshinai K, Mohammad A, et al. Therapeutic potential of ghrelin treatment for unloading-induced muscle atrophy in mice. Biochem Biophys Res Commun. 2011;412:296-301.
11. Broglio F, Boutignon F, Benso A, et al. EP1572: a novel peptidomimetic GH secretagogue with potent and selective GH-releasing activity in man. J Endocrinol Invest. 2002;25:RC26-RC28.
12. Smith RG. Development of growth hormone secretagogues. Endocr Rev. 2005;26:346-360. (Pubitemid 40686648)
13. Moulin A, Ryan J, Martinez J, Fehrentz JA. Recent developments in ghrelin receptor ligands. ChemMedChem. 2007;2:1242-1259.
14. Cordido F, Isidro ML, Nemiña R, Sangiao-Alvarellos S. Ghrelin and growth hormone secretagogues, physiological and pharmacological aspect. Curr Drug Discov Technol. 2009;6:34-42.
15. Svensson J, Ohlsson C, Jansson JO, et al. Treatment with the oral growth hormone secretagogue MK-677 increases markers of bone formation and bone resorption in obese young males. J Bone Miner Res. 1998;13:1158-1166. (Pubitemid 28311784)
16. Blackman MR. Use of growth hormone secretagogues to prevent or treat the effects of aging: not yet ready for prime time. Ann Intern Med. 2008;149:677-679.
17. Nagaya N, Moriya J, Yasumura Y, et al. Effects of ghrelin administration on left ventricular function, exercise capacity, and muscle wasting in patients with chronic heart failure. Circulation. 2004;110:3674-3679. (Pubitemid 39665256)
18. Cao JM, Ong H, Chen C. Effects of ghrelin and synthetic GH secretagogues on the cardiovascular system. Trends Endocrinol Metab. 2006;17:13-18. (Pubitemid 43031379)
19. Locatelli V, Rossoni G, Schweiger F, et al. Growth hormone-independent cardioprotective effects of hexarelin in the rat. Endocrinology. 1999;140:4024-4031. (Pubitemid 30647097)
20. Benso A, Broglio F, Marafetti L, et al. Ghrelin and synthetic growth hormone secretagogues are cardioactive molecules with identities and differences. Semin Vasc Med. 2004;4:107-114. (Pubitemid 39433660)
21. Xu XB, Cao JM, Pang JJ, et al. The positive inotropic and calcium-mobilizing effects of growth hormone-releasing peptides on rat heart. Endocrinology. 2003;144:5050-5057.
22. 2+ homeostasis of isolated adult rat ventricular myocytes. Endocrinology. 2010;151:4446-4454.
23. Sun Q, Zang WJ, Chen C. Growth hormone secretagogues reduce transient outward K+ current via phospholipase C/protein kinase C signaling pathway in rat ventricular myocytes. Endocrinology. 2010;151:1228-1235.
24. Baldanzi G, Filigheddu N, Cutrupi S, et al. Ghrelin and des-acyl ghrelin inhibit cell death in cardiomyocytes and endothelial cells through ERK1/2 and PI 3-kinase/AKT. J Cell Biol. 2002;159:1029-1037. (Pubitemid 36055757)
25. Pang JJ, Xu RK, Xu XB, et al. Hexarelin protects rat cardiomyocytes from angiotensin II-induced apoptosis in vitro. Am J Physiol Heart Circ Physiol. 2004;286:H1063-H1069.
26. DeBoer MD. Ghrelin and cachexia: will treatment with GHSR-1a agonists make a difference for patients suffering from chronic wasting syndromes? Mol Cell Endocrinol. 2011;340:97-105.
27. Pierno S, De Luca A, Desaphy JF, et al. Growth hormone secretagogues modulate the electrical and contractile properties of rat skeletal muscle through a ghrelin-specific receptor. Br J Pharmacol. 2003;139:575-584. (Pubitemid 36819627)
28. Pedersen TH, de Paoli F, Nielsen OB. Increased excitability of acidified skeletal muscle: role of chloride conductance. J Gen Physiol. 2005;125:237-246. (Pubitemid 40224120)
29. Burge, JA, Hanna MG. Novel insights into the pathomechanisms of skeletal muscle channelopathies. Curr Neurol Neurosci Rep. 2012; 12:62-69.
30. Demange L, Boeglin D, Moulin A, et al. Synthesis and pharmacological in vitro and in vivo evaluations of novel triazole derivatives as ligands of the ghrelin receptor. 1. J Med Chem. 2007;50:1939-1957. (Pubitemid 46626603)
31. Moulin A, Demange L, Bergé G, et al. Toward potent ghrelin receptor ligands based on trisubstituted 1,2,4-triazole structure. 2. Synthesis and pharmacological in vitro and in vivo evaluations. J Med Chem. 2007;50:5790-5806. (Pubitemid 350106034)
32. Bresciani E, Tamiazzo L, Torsello A, et al. Ghrelin control of GH secretion and feeding behaviour: the role of the GHS-R1a receptor studied in vivo and in vitro using novel non-peptide ligands. Eat Weight Disord. 2008;13:e67-e74.
33. Fraysse B, Desaphy JF, Pierno S, et al. Decrease in resting calcium and calcium entry associated with slow-to-fast transition in unloaded rat soleus muscle. FASEB J. 2003;17:1916-1918.
34. Liantonio A, Giannuzzi V, Cippone V, Camerino GM, Pierno S, Camerino DC. Fluvastatin and atorvastatin affect calcium homeostasis of rat skeletal muscle fibers in vivo and in vitro by impairing the sarcoplasmic reticulum/mitochondria Ca2+-release system. J Pharmacol Exp Ther. 2007;321:626-634. (Pubitemid 46624499)
35. 2+indicators with greatly improved fluorescence properties. J Biol Chem. 1985;260:3440-3450.
36. Parekh AB, Penner R. Store depletion and calcium influx. Physiol Rev. 1997;77:901-930. (Pubitemid 27459576)
37. Filigheddu N, Gnocchi VF, Coscia M, et al. Ghrelin and des-acyl ghrelin promote differentiation and fusion of C2C12 skeletal muscle cells. Mol Biol Cell. 2007;18:986-994. (Pubitemid 46399502)
38. Yamamoto D, Ikeshita N, Matsubara T, et al. GHRP-2, a GHS-R agonist, directly acts on myocytes to attenuate the dexamethasone-induced expressions of muscle-specific ubiquitin ligases, Atrogin-1 and MuRF1. Life Sci. 2008;82:460-466.
39. Berridge MV, Herst PM, Tan AS. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev. 2005;11:127-152. (Pubitemid 41510276)
40. Ogura T, Tanaka Y, Nakata T, Namikawa T, Kataoka H, Ohtsubo Y. Simvastatin reduces insulin-like growth factor-1 signaling in differentiating C2C12 mouse myoblast cells in an HMG-CoA reductase inhibition-independent manner. J Toxicol Sci. 2007;32:57-67. (Pubitemid 46334070)
41. Shao Y, Molnar LF, Jung Y, et al. Advances in methods and algorithms in a modern quantum chemistry program package. Phys Chem Chem Phys. 2006;8:3172-3191.
42. Hehre WJA. Guide to Molecular Mechanics and Quantum Chemical Calculations, 2nd ed. Irvine, CA: Wavefunction Inc; 2006
43. Bhal SK, Kassam K, Peirson IG, Pearl GM. The Rule of Five revisited: applying log D in place of log P in drug-likeness filters. Mol Pharm. 2007;4:556-560. (Pubitemid 47310166)
44. Ghè C, Cassoni P, Catapano F, et al. The antiproliferative effect of synthetic peptidyl GH secretagogues in human CALU-1 lung carcinoma cells. Endocrinology. 2002;143:484-491. (Pubitemid 34107201)
45. Cassoni P, Ghé C, Marrocco T, et al. Expression of ghrelin and biological activity of specific receptors for ghrelin and des-acyl ghrelin in human prostate neoplasms and related cell lines. Eur J Endocrinol. 2004;150:173-184. (Pubitemid 38312810)
46. Jeffery PL, Herington AC, Chopin LK. Expression and action of the growth hormone releasing peptide ghrelin and its receptor in prostate cancer cell lines. J Endocrinol. 2002;172:R7-R11. (Pubitemid 34232710)
47. Traebert M, Riediger T, Whitebread S, Scharrer E, Schmid HA. Ghrelin acts on leptin-responsive neurones in the rat arcuate nucleus. J Neuroendocrinol. 2002;14:580-586. (Pubitemid 34679222)
48. Crompton M, Virji S, Doyle V, Johnson N, Ward JM. The mitochondrial permeability transition pore. Biochem Soc Symp. 1999;66:167-179. (Pubitemid 129639031)
49. Saris NE, Carafoli E. A historical review of cellular calcium handling, with emphasis on mitochondria. Biochemistry (Mosc). 2005;70:187-194. (Pubitemid 40512327)
50. Moulin A, Brunel L, Boeglin D, et al. The 1,2,4-triazole as a scaffold for the design of ghrelin receptor ligands: development of JMV 2959, a potent antagonist. Amino Acids. 2013;44:301-314.
51. Rimessi A, Giorgi C, Pinton P, Rizzuto R. The versatility of mitochondrial calcium signals: from stimulation of cell metabolism to induction of cell death. Biochim Biophys Acta. 2008;1777:808-816.
52. Papotti M, Ghè C, Cassoni P, et al. Growth hormone secretagogue binding sites in peripheral human tissues. J Clin Endocrinol Metab. 2000;85:3803-3807.
53. Gnanapavan S, Kola B, Bustin SA, et al. The tissue distribution of the mRNA of ghrelin and subtypes of its receptor, GHS-R, in humans. J Clin Endocrinol Metab. 2002;87:2988-2991. (Pubitemid 34655375)
54. Muccioli G, Baragli A, Granata R, Papotti M, Ghigo E. Heterogeneity of ghrelin/growth hormone secretagogue receptors. Toward the understanding of the molecular identity of novel ghrelin/GHS receptors. Neuroendocrinology. 2007;86:147-164. (Pubitemid 350073603)
55. Kulstad R, Schoeller DA. The energetics of wasting diseases. Curr Opin Clin Nutr Metab Care. 2007;10:488-493. (Pubitemid 46934119)
56. Menconi MJ, Wei W, Yang H, Wray CJ, Hasselgren PO. Treatment of cultured myotubes with the calcium ionophore A23187 increases proteasome activity via a CaMK II-caspase-calpain-dependent mechanism. Surgery. 2004;136:135-142. (Pubitemid 39037646)
57. Costelli P, Reffo P, Penna F, Autelli R, Bonelli G, Baccino FM. Ca(2+)-dependent proteolysis in muscle wasting. Int J Biochem Cell Biol. 2005;37:2134-2146.
58. Fareed MU, Evenson AR, Wei W, et al. Treatment of rats with calpain inhibitors prevents sepsis-induced muscle proteolysis independent of atrogin-1/MAFbx and MuRF1 expression. AmJ Physiol Regul Integr Comp Physiol. 2006;290:R1589-R1597. (Pubitemid 43830824)
59. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4:517-529. (Pubitemid 36773404)
60. Fraysse B, Desaphy JF, Rolland JF, et al. Fiber type-related changes in rat skeletal muscle calcium homeostasis during aging and restoration by growth hormone. Neurobiol Dis. 2006;21:372-380. (Pubitemid 43099860)
61. Hasselgren PO, Fischer JE. Muscle cachexia: current concepts of intracellular mechanisms and molecular regulation. Ann Surg. 2001;233:9-17. (Pubitemid 32042769)
62. Gissel H. The role of Ca2+ in muscle cell damage. Ann NY Acad Sci. 2005;1066:166-180.
63. Bach MA, Rockwood K, Zetterberg C, et al. The effects of MK-0677, an oral growth hormone secretagogue, in patients with hip fracture. J Am Geriatr Soc. 2004;52:516-523. (Pubitemid 38480627)
64. Balasubramaniam A, Joshi R, Su C, et al. Ghrelin inhibits skeletal muscle protein breakdown in rats with thermal injury through normalizing elevated expression of E3 ubiquitin ligases MuRF1 and MAFbx. AmJ Physiol Regul IntegrCompPhysiol. 2009;296:R893-R901.
65. Sheriff S, Joshi R, Friend LA, James JH, Balasubramaniam A. Ghrelin receptor agonist, GHRP-2, attenuates burn injury-induced MuRF-1 and MAFbx expression and muscle proteolysis in rats. Peptides. 2009;30:1909-1913.
66. Miki K, Maekura R, Nagaya N, et al. Ghrelin treatment of cachectic patients with chronic obstructive pulmonary disease: a multicenter, randomized, double-blind, placebo-controlled trial. PLoS One. 2012;7:e35708.
67. Matsumoto N, Nakazato M. Clinical application of ghrelin for chronic respiratory diseases. Methods Enzymol. 2012;514:399-407.
68. Porporato PE, Filigheddu N, Reano S, et al. Acylated and unacylated ghrelin impair skeletal muscle atrophy in mice. J Clin Invest. 2013; 123:611-622.