Adult-onset growth hormone and insulin-like growth factor I deficiency reduces neoplastic disease, modifies age-related pathology, and increases life span

Endocrinology

Volumn 146, Issue 7, 2005, Pages 2920-2932

  Sonntag, William E ^a   Carter, Christy S ^a,d   Ikeno, Yuji ^b   Ekenstedt, Kari ^d   Carlson, Cathy S ^a,d   Loeser, Richard F ^e   Chakrabarty, Shilla ^f   Lee, Shuko ^b,c   Bennett, Colleen ^a   Ingram, Rhonda ^a   Moore, Tracy ^a   Ramsey, Melinda ^a  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^b SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e RUSH MEDICAL COLLEGE   (United States)

^f University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH HORMONE; SOMATOMEDIN C;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HEMORRHAGE; CANCER INCIDENCE; CARTILAGE DEGENERATION; COGNITION; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE EXACERBATION; FEMALE; FUNCTIONAL DISEASE; GROWTH; GROWTH HORMONE DEFICIENCY; HETEROZYGOTE; HORMONE DEFICIENCY; HUMAN; INSULIN LIKE GROWTH FACTOR 1 DEFICIENCY; LIFESPAN; MALE; NEOPLASM; NEPHROTOXICITY; NONHUMAN; ONSET AGE; PATHOLOGY; PLEIOTROPY; PRIORITY JOURNAL; PROGENY; RAT; REPRODUCTIVE HEALTH; TIME SERIES ANALYSIS; ANIMAL; BODY COMPOSITION; BODY TEMPERATURE; CIRCADIAN RHYTHM; DRUG EFFECT; DWARFISM; GENETICS; HAND GRIP; HOMOZYGOTE; INBORN ERROR OF STEROID METABOLISM; LEWIS RAT; LONGEVITY; MAZE TEST; MOTOR ACTIVITY; PATHOPHYSIOLOGY; REPRODUCTION;

AGING; ANIMALS; BODY COMPOSITION; BODY TEMPERATURE; CIRCADIAN RHYTHM; DWARFISM; GROWTH HORMONE; HAND STRENGTH; HETEROZYGOTE; HOMOZYGOTE; INSULIN-LIKE GROWTH FACTOR I; LONGEVITY; MALE; MAZE LEARNING; MOTOR ACTIVITY; NEOPLASMS; RATS; RATS, INBRED LEW; REPRODUCTION; STEROID METABOLISM, INBORN ERRORS;

EID: 22144444220     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2005-0058     Document Type: Article

References (68)

1. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R 1993 AC. elegans mutant that lives twice as long as wild type. Nature 366:461-464
2. Johnson TE 1990 Increased life-span of age-1 mutants in Caenorhabditis elegans and lower Gompertz rate of aging. Science 249:908-912
3. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS 2001 A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107-110
4. Fabrizio P, Pozza F, Pletcher SD, Gendron CM, Longo VD 2001 Regulation of longevity and stress resistance by Sch9 in yeast. Science 292:288-290
5. Kenyon C 2001 A conserved regulatory system for aging. Cell 105:165-168
6. Flurkey K, Papaconstantinou J, Miller RA, Harrison DE 2001 Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proc Natl Acad Sci USA 98:6736-6741
7. Brown-Borg HM, Borg KE, Meliska CJ, Bartke A 1996 Dwarf mice and the ageing process. Nature 384:33
8. Coschigano KT, Clemmons D, Bellush LL, Kopchick JJ 2000 Assessment of growth parameters and life span of GHR/BP gene-disrupted mice. Endocrinology 141:2608-2613
9. Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P, Le Bouc Y 2003 IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421:182-187
10. Carter CS, Ramsey MM, Ingram RL, Cashion AB, Cefalu WT, Wang ZQ, Sonntag WE 2002 Models of growth hormone and IGF-1 deficiency: applications to studies of aging processes and life-span determination. J Gerontol A Biol Sci Med Sci 57:B177-B188
11. Coschigano KT, Holland AN, Riders ME, List EO, Flyvbjerg A, Kopchick JJ 2003 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 144:3799-3810
12. Rudman D, Feller AG, Nagraj HS, Gergans GA, Lalitha PY, Goldberg AF, Schlenker RA, Cohn L, Rudman IW, Mattson DE 1990 Effects of human growth hormone in men over 60 years old. N Engl J Med 323:1-6
13. Khan AS, Lynch CD, Sane DC, Willingham MC, Sonntag WE 2001 Growth hormone increases regional coronary blood flow and capillary density in aged rats. J Gerontol A Biol Sci Med Sci 56:B364-B371
14. Sonntag WE, Lynch CD, Cefalu WT, Ingram RL, Bennett SA, Thornton PL, Khan AS 1999 Pleiotropic effects of growth hormone and insulin-like growth factor (IGF)-1 on biological aging: inferences from moderate caloric-restricted animals. J Gerontol A Biol Sci Med Sci 54:B521-B538
15. Khansari DN, Gustad T 1991 Effects of long-term, low-dose growth hormone therapy on immune function and life expectancy of mice. Mech Ageing Dev 57:87-100
16. Markowska AL, Mooney M, Sonntag WE 1998 Insulin-like growth factor-1 ameliorates age-related behavioral deficits. Neuroscience 87:559-569
17. Liu JL, Coschigano KT, Robertson K, Lipsett M, Guo Y, Kopchick JJ, Kumar U, Liu YL 2004 Disruption of growth hormone receptor gene causes diminished pancreatic islet size and increased insulin sensitivity in mice. Am J Physiol Endocrinol Metab 287:E405-E413
18. Carter CS, Ramsey MM, Sonntag WE 2002 A critical analysis of the role of growth hormone and IGF-1 in aging and lifespan. Trends Genet 18:295-301
19. Charlton HM, Clark RG, Robinson IC, Goff AE, Cox BS, Bugnon C, Bloch BA 1988 Growth hormone-deficient dwarfism in the rat: a new mutation. J Endocrinol 119:51-58
20. Nogami H, Takeuchi T 1993 Increased population of nonhormone-producing cells suggests the presence of dysfunctional growth hormone cells in the anterior pituitary gland of the spontaneous dwarf rat. Neuroendocrinology 57:374-380
21. Tierney T, Robinson IC 2002 Increased lactotrophs despite decreased somatotrophs in the dwarf (dw/dw) rat: a defect in the regulation of lactotroph/ somatotroph cell fate? J Endocrinol 175:435-446
22. Maeda H, Gleiser CA, Masoro EJ, Murata I, McMahan CA, Yu BP 1985 Nutritional influences on aging of Fischer 344 rats: II. Pathology. J Gerontol 40:671-688
23. Ikeno Y, Hubbard GB, Lee S, Yu BP, Herlihy JT 2002 The influence of long-term aloe vera ingestion on age-related disease in male Fischer 344 rats. Phytother Res 16:712-718
24. Yu BP, Masoro EJ, Murata I, Bertrand HA, Lynd FT 1982 Life span study of SPF Fischer 344 male rats fed ad libitum or restricted diets: longevity, growth, lean body mass and disease. J Gerontol 37:130-141
25. Shimokawa I, Higami Y, Hubbard GB, McMahan CA, Masoro EJ, Yu BP 1993 Diet and the suitability of the male Fischer 344 rat as a model for aging research. J Gerontol 48:B27-B32
26. Shukitt-Hale B, Mouzakis G, Joseph JA 1998 Psychomotor and spatial memory performance in aging male Fischer 344 rats. Exp Gerontol 33:615-624
27. Morris RG, Garrud P, Rawlins JN, O'Keefe J 1982 Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683
28. Dix SL, Aggleton JP 1999 Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behav Brain Res 99:191-200
29. Sonntag WE, Lenham JE, Ingram RL 1992 Effects of aging and dietary restriction on tissue protein synthesis: relationship to plasma insulin-like growth factor-1. J Gerontol 47:B159-B163
30. Thornton PL, Ingram RL, Sonntag WE 2000 Chronic [D-Ala2]-growth hormone-releasing hormone administration attenuates age-related deficits in spatial memory. J Gerontol A Biol Sci Med Sci 55:B106-B112
31. Ramsey M, Weiner J, Moore T, Carter C, Sonntag W 2004 Growth hormone treatment attenuates age-related deficits in short-term platicity and spatial learning. Neuroscience 129:119-127
32. Barton-Davis ER, Shoturma DI, Musaro A, Rosenthal N, Sweeney HL 1998 Viral mediated expression of insulin-like growth factor I blocks the agingrelated loss of skeletal muscle function. Proc Natl Acad Sci USA 95:15603-15607
33. Borg KE, Brown-Borg HM, Bartke A 1995 Assessment of the primary adrenal cortical and pancreatic hormone basal levels in relation to plasma glucose and age in the unstressed Ames dwarf mouse. Proc Soc Exp Biol Med 210:126-133
34. Sornson MW, Wu W, Dasen JS, Flynn SE, Norman DJ, O'Connell SM, Gukovsky I, Carriere C, Ryan AK, Miller AP, Zuo L, Gleiberman AS, Andersen B, Beamer WG, Rosenfeld MG 1996 Pituitary lineage determination by the Prophet of Pit-1 homeodomain factor defective in Ames dwarfism. Nature 384:327-333
35. Li S, Crenshaw EB, III, Rawson EJ, Simmons DM, Swanson LW, Rosenfeld MG 1990 Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene pit-1. Nature 347:528-533
36. Hauck SJ, Hunter WS, Danilovich N, Kopchick JJ, Bartke A 2001 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) 226:552-558
37. Shimokawa I, Higami Y, Utsuyama M, Tuchiya T, Komatsu T, Chiba T, Yamaza H 2002 Life span extension by reduction in growth hormone-insulinlike growth factor-1 axis in a transgenic rat model. Am J Pathol 160:2259-2265
38. Ikeno Y, Bronson RT, Hubbard GB, Lee S, Bartke A 2003 Delayed occurrence of fatal neoplastic diseases in ames dwarf mice: correlation to extended longevity. J Gerontol A Biol Sci Med Sci 58:291-296
39. Ramsey MM, Ingram RL, Cashion AB, Ng AH, Cline JM, Parlow AF, Sonntag WE 2002 Growth hormone-deficient dwarf animals are resistant to dimethylbenzanthracine (DMBA)-induced mammary carcinogenesis. Endocrinology 143:4139-4142
40. Kinney-Forshee BA, Kinney NE, Steger RW, Bartke A 2004 Could a deficiency in growth hormone signaling be beneficial to the aging brain? Physiol Behav 80:589-594
41. Salmon AB, Murakami S, Bartke A, Kopchick J, Yasumura K, Miller RA 2005 Fibroblast cell lines from young adult mice of long-lived mutant strains are resistant to multiple forms of stress. Am J Physiol Endocrinol Metab
42. de Magalhaes JP, Cabral JA, Magalhaes D 2005 The influence of genes on the aging process of mice: a statistical assessment of the genetics of aging. Genetics 169:265-274
43. Steger RW, Bartke A, Cecim M 1993 Premature ageing in transgenic mice expressing different growth hormone genes. J Reprod Fertil Suppl 46:61-75
44. Groesbeck MD, Parlow AF, DaughadayWH1987 Stimulation of supranormal growth in prepubertal, adult plateaued, and hypophysectomized female rats by large doses of rat growth hormone: physiological effects and adverse consequences. Endocrinology 120:1963-1975
45. Bartke A 2003 Can growth hormone (GH) accelerate aging? Evidence from GH-transgenic mice. Neuroendocrinology 78:210-216
46. Ekenstedt K, Sonntag WE, Loeser RF, Lindgren BR, Carlson CS 2004 Effects of chronic growth hormone/insulin-like growth factor-1 deficiency on osteoarthritis in rat knee joints. Osteoarthritis Cartilage 12(Suppl):S7
47. Carlson CS, Loeser RF, Purser CB, Gardin JF, Jerome CP 1996 Osteoarthritis in cynomolgus macaques. III: Effects of age, gender, and subchondral bone thickness on the severity of disease. J Bone Miner Res 11:1209-1217
48. Silberberg R 1972 Articular aging and osteoarthrosis in dwarf mice. Pathol Microbiol (Basel) 38:417-430
49. Silberberg R 1973 Vertebral aging in hypopituitary dwarf mice. Gerontologia 19:281-294
50. Sun LY, Al Regaiey K, Masternak MM, Wang J, Bartke A 2005 Local expression ofGHand IGF-1 in the hippocampus of GH-deficient long-lived mice. Neurobiol Aging 26:929-937
51. Jeay S, Sonenshein GE, Postel-Vinay MC, Kelly PA, Baixeras E 2002 Growth hormone can act as a cytokine controlling survival and proliferation of immune cells: new insights into signaling pathways. Mol Cell Endocrinol 188:1-7
52. Nyberg F 1997 Aging effects on growth hormone receptor binding in the brain. Exp Gerontol 32:521-528
53. Nyberg F, Burman P 1996 Growth hormone and its receptors in the central nervous system - location and functional significance. Horm Res 45:18-22
54. Markowska AL, Mooney M, Sonntag WE 1998 Insulin-like growth factor-1 ameliorates age-related behavioral deficits. Neuroscience 87:559-569
55. Cartee GD, Bohn EE, Gibson BT, Farrar RP 1996 Growth hormone supplementation increases skeletal muscle mass of old male Fischer 344/brown Norway rats. J Gerontol A Biol Sci Med Sci 51:B214-B219
56. Hull KL, Harvey S 2000 Growth hormone: a reproductive endocrine-paracrine regulator? Rev Reprod 5:175-182
57. Yakar S, Pennisi P, Zhao H, Zhang Y, LeRoith D 2004 Circulating IGF-1 and its role in cancer: lessons from the IGF-1 gene deletion (LID) mouse. Novartis Found Symp 262:3-9
58. Breese CR, Ingram RL, Sonntag WE 1991 Influence of age and long-term dietary restriction on plasma insulin-like growth factor-1 (IGF-1), IGF-1 gene expression, and IGF-1 binding proteins. J Gerontol 46:B180-B187
59. Ingram DK, Weindruch R, Spangler EL, Freeman JR, Walford RL 1987 Dietary restriction benefits learning and motor performance of aged mice. J Gerontol 42:78-81
60. Leveille PJ, Weindruch R, Walford RL, Bok D, Horwitz J 1984 Dietary restriction retards age-related loss of γ crystallins in the mouse lens. Science 224:1247-1249
61. Weindruch R, Walford RL, Fligiel S, Guthrie D 1986 The retardation of aging in mice by dietary restriction: longevity, cancer, immunity and lifetime energy intake. J Nutr 116:641-654
62. Weindruch R, Devens BH, Raff HV, Walford RL 1983 Influence of dietary restriction and aging on natural killer cell activity in mice. J Immunol 130:993-996
63. Weindruch R, Walford RL 1982 Dietary restriction in mice beginning at 1 year of age: effect on life-span and spontaneous cancer incidence. Science 215:1415-1418
64. Weindruch RH, Kristie JA, Cheney KE, Walford RL 1979 Influence of controlled dietary restriction on immunologic function and aging. Fed Proc 38:2007-2016
65. Dunn SE, Kari FW, French J, Leininger JR, Travlos G, Wilson R, Barrett JC 1997 Dietary restriction reduces insulin-like growth factor I levels, which modulates apoptosis, cell proliferation, and tumor progression in p53-deficient mice. Cancer Res 57:4667-4672
66. Wu Y, Yakar S, Zhao L, Hennighausen L, LeRoith D 2002 Circulating insulinlike growth factor-I levels regulate colon cancer growth and metastasis. Cancer Res 62:1030-1035
67. Khandwala HM, McCutcheon IE, Flyvbjerg A, Friend KE 2000 The effects of insulin-like growth factors on tumorigenesis and neoplastic growth. Endocr Rev 21:215-244
68. Rose M, Charlesworth B 1980 A test of evolutionary theories of senescence. Nature 287:141-142