Decreased expression level of apoptosis-related genes and/or proteins in skeletal muscles, but not in hearts, of growth hormone receptor knockout mice

Experimental Biology and Medicine

Volumn 236, Issue 2, 2011, Pages 156-168

  Gesing, Adam ^a,b   Masternak, Michal M ^a,c   Wang, Feiya ^a   Lewinski, Andrzej ^b,d   Karbownik Lewinska, Malgorzata ^b,d   Bartke, Andrzej ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL UNIVERSITY OF LODZ   (Poland)

^c INSTITUTE OF HUMAN GENETICS   (Poland)

^d POLISH MOTHER S MEMORIAL HOSPITAL RESEARCH INSTITUTE   (Poland)

Author keywords

Apoptosis; Calorie restriction; Caspase; GHRKO mice; Heart; Skeletal muscles

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CASPASE 8; CASPASE 9; CYTOCHROME C; GROWTH HORMONE RECEPTOR; HEART MUSCLE EXTRACT; MESSENGER RNA; PHOSPHOPROTEIN; PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE;

AGING; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CALORIC RESTRICTION; CONTROLLED STUDY; GENE EXPRESSION; HEART; KNOCKOUT MOUSE; LONGEVITY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SKELETAL MUSCLE;

ANIMALS; APOPTOSIS; CALORIC RESTRICTION; GENE EXPRESSION PROFILING; HEART; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; RECEPTORS, SOMATOTROPIN;

ANIMALIA; MUS;

EID: 79951657821     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1258/ebm.2010.010202     Document Type: Article

References (63)

1. Zhou Y, Xu BC, Maheshwari HG, He L, Reed M, Lozykowski M, Okada S, Cataldo L, Coschigano 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;94:13215-20 (Pubitemid 27518502)
2. Coschigano KT, Clemmons D, Bellush LL, Kopchick JJ. Assessment of growth parameters and life span of GHR/BP gene disrupted mice. Endocrinology 2000;141:2608-13 (Pubitemid 32269083)
3. 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 lifespan. Endocrinology 2003;144:3799-810 (Pubitemid 37088732)
4. Bartke A, Brown-Borg H. Life extension in the dwarf mouse. Curr Top Dev Biol 2004;63:189-225 (Pubitemid 39752388)
5. Coschigano KT. Aging-related characteristics of growth hormone receptor/binding protein gene-disrupted mice. AGE 2006;28:191-200 (Pubitemid 44197729)
6. Kopchick JJ, Laron Z. Is the Laron mouse an accurate model of Laron syndrome? Mol Genet Metab 1999;68:232-6
7. Bartke A, Chandrashekar V, Bailey B, Zaczek D, Turyn D. Consequences of growth hormone (GH) overexpression and GH resistance. Neuropeptides 2002;36:201-8
8. 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:E405-13
9. Salmon AB, Murakami S, Bartke A, Kopchick J, Yasumura K, Miller RA. Fibroblast cell lines from young adult mice of long-lived mutant strains are resistant to multiple forms of stress. Am J Physiol Endocrinol Metab 2005;289:E23-9
10. Sun LY, Steinbaugh MJ, Masternak MM, Bartke A, Miller RA. Fibroblasts from long-lived mutant mice show diminished ERK1/2 phosphorylation but exaggerated induction of immediate early genes. Free Radic Biol Med 2009;47:1753-61
11. Ikeno Y, Hubbard GB, Lee S, Cortez LA, Lew CM, Webb CR, Berryman DE, List EO, Kopchick JJ, Bartke A. Reduced incidence and delayed occurrence of fatal neoplastic diseases in growth hormone receptor/binding protein knockout mice. J Gerontol A Biol Sci Med Sci 2009;64:522-9
12. Batistatou A, Greene LA. Internucleosomal DNA cleavage and neuronal cell survival/death. J Cell Biol 1993;122:523-32 (Pubitemid 23226670)
13. Johnson EM Jr, Deckwerth TL. Molecular mechanisms of developmental neuronal death. Annu Rev Neurosci 1993;16:31-46 (Pubitemid 23073999)
14. Clarke PG. Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 1990;181:195-213 (Pubitemid 20153523)
15. Carson DA, Ribeiro JM. Apoptosis and disease. Lancet 1993;341:1251-4 (Pubitemid 23146938)
16. Budihardjo I, Oliver H, Lutter M, Luo X, Wang X. Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 1999;15:269-90 (Pubitemid 32250377)
17. Boatright KM, Salvesen GS. Mechanisms of caspase activation. Curr Opin Cell Biol 2003;15:725-31 (Pubitemid 37492933)
18. Jin Z, El-Deiry WS. Overview of cell death signaling pathways. Cancer Biol Ther 2005;4:139-63 (Pubitemid 41351311)
19. Masternak MM, Al-Regaiey KA, Del Rosario Lim MM, Jimenez-Ortega V, Panici JA, Bonkowski MS, Bartke A. Effects of caloric restriction on insulin pathway gene expression in the skeletal muscle and liver of normal and long-lived GHR-KO mice. Exp Gerontol 2005;40:679-84 (Pubitemid 41265818)
20. Masternak MM, Al-Regaiey KA, Del Rosario Lim MM, Jimenez-Ortega V, Panici JA, Bonkowski MS, Kopchick JJ, Wang Z, Bartke A. Caloric restriction and growth hormone receptor knockout: effects on expression of genes involved in insulin action in the heart. Exp Gerontol 2006;41:417-29
21. Coultas L, Strasser A. The role of the Bcl-2 protein family in cancer. Semin Cancer Biol 2003;13:115-23 (Pubitemid 36315930)
22. Srinivasula SM, Datta P, Fan XJ, Fernandes-Alnemri T, Huang Z, Alnemri ES. Molecular determinants of the caspase-promoting activity of Smac/DIABLO and its role in the death receptor pathway. J Biol Chem 2000;275:36152-7
23. Henry-Mowatt J, Dive C, Martinou JC, James D. Role of mitochondrial membrane permeabilization in apoptosis and cancer. Oncogene 2004;23:2850-60 (Pubitemid 38638847)
24. Kruidering M, Evan GI. Caspase-8 in apoptosis: the beginning of "the end"? IUBMB Life 2000;50:85-90
25. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov 2008;7:1001-12
26. Zou H, Li Y, Liu X, Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 1999;274:11549-56
27. Adrain C, Martin SJ. The mitochondrial apoptosome: a killer unleashed by the cytochrome seas. Trends Biochem Sci 2001;26:390-7 (Pubitemid 32530658)
28. Weindruch R, Sohal RS. Seminars in medicine of the Beth Israel Deaconess medical center. Caloric intake and aging. N Engl J Med 1997;337:986-94
29. Bonkowski MS, Rocha JS, Masternak MM, Al Regaiey KA, Bartke A. Targeted disruption of growth hormone receptor interferes with the beneficial actions of calorie restriction. Proc Natl Acad Sci USA 2006;103:7901-5
30. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987;162:156-9 (Pubitemid 17064313)
31. Harper JM, Salmon AB, Chang Y, Bonkowski M, Bartke A, Miller RA. Stress resistance and aging: influence of genes and nutrition. Mech Ageing Dev 2006;127:687-94
32. Plant PJ, Bain JR, Correa JE, Woo M, Batt J. Absence of caspase-3 protects against denervation-induced skeletal muscle atrophy. J Appl Physiol 2009;107:224-34
33. Russell ST, Rajani S, Dhadda RS, Tisdale MJ. Mechanism of induction of muscle protein loss by hyperglycaemia. Exp Cell Res 2009;315:16-25
34. Madden SD, Donovan M, Cotter TG. Key apoptosis regulating proteins are down-regulated during postnatal tissue development. Int J Dev Biol 2007;51:415-23
35. Barouch LA, Gao D, Chen L, Miller KL, Xu W, Phan AC, Kittleson MM, Minhas KM, Berkowitz DE, Wei C, Hare JM. Cardiac myocyte apoptosis is associated with increased DNA damage and decreased survival in murine models of obesity. Circ Res 2006;98:119-24 (Pubitemid 43970211)
36. 2+ homeostasis, protein damage and apoptotic protein expression. Aging Cell 2007;6:799-806
37. Hochhauser E, Cheporko Y, Yasovich N, Pinchas L, Offen D, Barhum Y, Pannet H, Tobar A, Vidne BA, Birk E. Bax deficiency reduces infarct size and improves long-term function after myocardial infarction. Cell Biochem Biophys 2007;47:11-20
38. Hochhauser E, Kivity S, Offen D, Maulik N, Otani H, Barhum Y, Pannet H, Shneyvays V, Shainberg A, Goldshtaub V, Tobar A, Vidne B. Bax ablation protects against myocardial ischemia-reperfusion injury in transgenic mice. Am J Physiol Heart Circ Physiol 2003;284:H2351-9
39. Wencker D, Chandra M, Nguyen K, Miao W, Garantziotis S, Factor SM, Shirani J, Armstrong RC, Kitsis RN. A mechanistic role for cardiac myocyte apoptosis in heart failure. J Clin Invest 2003;111:1497-504 (Pubitemid 38063282)
40. Sakamaki K, Inoue T, Asano M, Sudo K, Kazama H, Sakagami J, Sakata S, Ozaki M, Nakamura S, Toyokuni S, Osumi N, Iwakura Y, Yonehara S. Ex vivo whole-embryo culture of caspase-8-deficient embryos normalize their aberrant phenotypes in the developing neural tube and heart. Cell Death Differ 2002;9:1196-206 (Pubitemid 35331766)
41. Varfolomeev EE, Schuchmann M, Luria V, Chiannilkulchai N, Beckmann JS, Mett IL, Rebrikov D, Brodianski VM, Kemper OC, Kollet O, Lapidot T, Soffer D, Sobe T, Avraham KB, Goncharov T, Holtman H, Lonai P, Wallach D. Targeted disruption of the mouse Caspase-8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 1998;9:267-76 (Pubitemid 28400040)
42. Tyner SD, Venkatachalam S, Choi J, Jones S, Ghebranious N, Igelmann H, Lu X, Soron G, Cooper B, Brayton C, Hee S, Thompson T, Karsenty G, Bradley A, Donehower LA. p53 mutant mice that display early ageing-associated phenotypes. Nature 2002;415:45-53 (Pubitemid 34062443)
43. Campisi J. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 2005;120:513-22 (Pubitemid 40269765)
44. Nithipongvanitch R, Ittarat W, Velez JM, Zhao R, Clair DKS, Oberley TD. Evidence for p53 as guardian of the cardiomyocyte mitochondrial genome following acute adriamycin treatment. J Histochem Cytochem 2007;55:629-39 (Pubitemid 46791945)
45. Shizukuda Y, Matoba S, Mian OY, Nguyen T, Hwang PM. Targeted disruption of p53 attenuates doxorubicin-induced cardiac toxicity in mice. Mol Cell Biochem 2005;273:25-32 (Pubitemid 40774760)
46. Matsusaka H, Ide T, Matsushima S, Ikeuchi M, Kubota T, Sunagawa K, Kinugawa S, Tsutsui H. Targeted deletion of p53 prevents cardiac rupture after myocardial infarction in mice. Cardiovasc Res 2006;70:457-65
47. Kown MH, Murata S, Jahncke CL, Mari C, Berry GJ, Lijkwan MA, Blankenberg FG, Strauss HW, Robbins RC. Donor cardiac allografts from p53 knockout mice exhibit apoptosis-independent prolongation of survival. Transplant Proc 2002;34:3274-6 (Pubitemid 35463317)
48. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-XL. Cell 1996;87:619-28 (Pubitemid 26386936)
49. Gross A, McDonnell JM, Korsmeyer SJ. BCL-2 family members and the mitochondria in apoptosis. Genes Dev 1999;13:1899-911 (Pubitemid 29407357)
50. Boland R, Vasconsuelo A, Milanesi L, Ronda AC, de Boland AR. 17β-estradiol signaling in skeletal muscle cells and its relationship to apoptosis. Steroids 2008;73:859-63
51. Vasconsuelo A, Milanesi L, Boland R. 17β-estradiol abrogates apoptosis in murine skeletal muscle cells through estrogen receptors: role of the phosphatidylinositol 3-kinase/Akt pathway. J Endocrinol 2008;196:385-97 (Pubitemid 351298524)
52. Wang M, Crisostomo P, Wairiuko GM, Meldrum DR. Estrogen receptor-α mediates acute myocardial protection in females. Am J Physiol Heart Circ Physiol 2006;290:H2204-9
53. Dhahbi J, Li X, Tran T, Masternak MM, Bartke A. Circulating blood leukocyte gene expression profiles: effects of the Ames dwarf mutation on pathways related to immunity and inflammation. Exp Gerontol 2007;42:772-88 (Pubitemid 47058860)
54. Kennedy MA, Rakoczy SG, Brown-Borg HM. Long-living Ames dwarf mouse hepatocytes readily undergo apoptosis. Exp Gerontol 2003;38:997-1008 (Pubitemid 37040801)
55. Heydari AR, Unnikrishnan A, Lucente LV, Richardson A. Caloric restriction and genomic stability. Nucleic Acids Res 2007;35:7485-96
56. Marzetti E, Lawler JM, Hiona A, Manini T, Seo AY, Leeuwenburgh C. Modulation of age-induced apoptotic signaling and cellular remodeling by exercise and calorie restriction in skeletal muscle. Free Radic Biol Med 2008;44:160-8
57. Dirks AJ, Leeuwenburgh C. Aging and lifelong calorie restriction result in adaptations of skeletal muscle apoptosis repressor, apoptosisinducing factor, X-linked inhibitor of apoptosis, caspase-3, and caspase-12. Free Radic Biol Med 2004;36:27-39 (Pubitemid 38068289)
58. Phillips T, Leeuwenburgh C. Muscle fiber-specific apoptosis and TNF-α signaling in sarcopenia are attenuated by life-long calorie restriction. FASEB J 2005;19:668-70 (Pubitemid 40471280)
59. Lee JH, Jung KJ, Kim JW, Kim HJ, Yu BP, Chung HY. Suppression of apoptosis by calorie restriction in aged kidney. Exp Gerontol 2004;39:1361-8 (Pubitemid 39360377)
60. Patel BP, Safdar A, Raha S, Tarnopolsky MA, Hamadeh MJ. Caloric restriction shortens lifespan through an increase in lipid peroxidation, inflammation and apoptosis in the G93A mouse, an animal model of ALS. PLoS One 2010;5:e9386
61. Bonkowski MS, Dominici FP, Arum O, Rocha JS, Al Regaiey KA, Westbrook R, Spong A, Panici J, Masternak MM, Kopchick JJ, Bartke A. Disruption of growth hormone receptor prevents calorie restriction from improving insulin action and longevity. PLoS ONE 2009;4:e4567
62. Giani JF, Bonkowski MS, Muñoz MC, Masternak MM, Turyn D, Bartke A, Dominici FP. Insulin signaling cascade in the hearts of long-lived growth hormone receptor knockout mice: effects of calorie restriction. J Gerontol A Biol Sci Med Sci 2008;63:788-97
63. Argentino DP, Dominici FP, Al Regaiey K, Bonkowski MS, Bartke A, Turyn D. Effects of long-term caloric restriction on early steps of the insulin-signaling system in mouse skeletal muscle. J Gerontol A Biol Sci Med Sci 2005;60:28-34 (Pubitemid 40321854)