Plasma IGF-1 is negatively correlated with body mass in a comparison of 36 mammalian species

Mechanisms of Ageing and Development

Volumn 131, Issue 9, 2010, Pages 591-598

  Stuart, Jeffrey A ^a   Page, Melissa M ^a  

^a BROCK UNIVERSITY   (Canada)

Author keywords

Aging; Body mass; IGF 1; Insulin like growth factor 1; Lifespan; Longevity

Indexed keywords

SOMATOMEDIN C;

AGING; ARTICLE; BLOOD ANALYSIS; BODY MASS; CONTROLLED STUDY; CORRELATION ANALYSIS; DATA ANALYSIS; INTERSPECIFIC RELATIONSHIP; LIFESPAN; LONGEVITY; MAMMAL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SPECIES COMPARISON;

ANIMALS; BODY COMPOSITION; BODY MASS INDEX; BODY WEIGHT; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; LONGEVITY; MALE; MICE; PHYLOGENY; REGENERATION; SPECIES SPECIFICITY; TIME FACTORS;

ANIMALIA; MAMMALIA; MUS;

EID: 77957322323     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2010.08.005     Document Type: Article

References (91)

1. Adamczewski J.Z., Fargey P.J., Laarveld B., Gunn A., Flood P.F. The influence of fatness on the likelihood of early-winter pregnancy in muskoxen (Ovibos moschatus). Theriogenology 1998, 50:605-614.
2. Bartoš L., Reyes E., Schams D., Bubenik G., Lobos A. Rank dependent seasonal levels of IGF-1, cortisol and reproductive hormones in male pudu (Pudu puda). Comp. Biochem. Physiol. A 1998, 120:373-378.
3. Bartoš L., Schams D., Bubenik G.A. Testosterone, but not IGF-1, LH, prolactin or cortisol, may serve as antler-stimulating hormone in red deer stags (Cervus elaphus). Bone 2009, 44:691-698.
4. Bernstein R.M., Leigh S.R., Donovan S.M., Monaco M.H. Hormones and body size evolution in papionin primates. Am. J. Phys. Anthropol. 2007, 132:247-260.
5. Bubenik G.A., Schams D., White R.G., Rowell J., Blake J., Bartoš L. Seasonal levels of metabolic hormones and substrates in male and female reindeer (Rangifer tarandus). Comp. Biochem. Physiol. C 1998, 120:307-315.
6. Campbell D.J., Rawlings J.M., Heaton P.R., Blount D.G., Pritchard D.I., Strain J.J., Hannigan B.M. Insulin-like growth factor-I (IGF-I) and its association with lymphocyte homeostasis in the ageing cat. Mech. Ageing Dev. 2004, 125:497-505.
7. Carter E.A., Tompkins R.G., Hsu H.B., Christian B., Alpert N.M., Weise S., Fischman A.J. Metabolic alterations in muscle of thermally injured rabbits, measured by positron emission tomography. Life Sci. 1997, 61:39-44.
8. Castigliego L., Grifoni G., Rosati R., Iannone G., Armani A., Gianfaldoni D., Guidi A. On the alterations in serum concentration of somatotropin and insuline-like growth factor 1 in lactating cows after the treatment with a little studied recombinant bovine somatotropin. Res. Vet. Sci. 2009, 87:29-35.
9. Chatterjee H.J., Ho S.Y.W., Barnes I., Groves C. Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evol. Biol. 2009, 9:259-278.
10. Conlon M.A., Kita K. Porcine growth hormone and LongR3IGF-I can improve recovery from surgery-induced weight loss in Guinea pigs. Gen. Comp. Endocrin. 2001, 123:332-336.
11. Cook R.C., Cook J.G., Murray D.L., Zager P., Johnson B.K., Gratso M.W. Development of predictive models of nutritional condition for rocky mountain elk. J. Wildlife Manage. 2001, 65:973-987.
12. Delisle I., Strobeck C. A phylogeny of the Caniformia (order Carnivora) based on 12 complete protein-coding mitochondrial genes. Mol. Phylogenet. Evol. 2005, 37:192-201.
13. Deichsel K., Hoppen H.-O., Bruckmaier R.M., Kolm G., Aurich C. Acute insulin-induced hypoglycaemia does not alter IGF-1 and LH release in cyclic mares. Reprod. Dom. Anim. 2005, 40:117-122.
14. Donahue S.W., Galley S.A., Vaughan M.R., Patterson-Buckendahl P., Demers L.M., Vance J.L., McGee M.E. Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis. J. Exp. Biol. 2006, 209:1630-1638.
15. du Dot, T.J., 2007. Diet quality and season affect physiology and energetic priorities of captive steller sea lions during and after periods of nutritional stress. M.Sc. Thesis, University of British Columbia, Canada.
16. Dubreuil P., Abribat T., Broxup B., Brazeau P. Long-term growth hormone-releasing factor administration on growth hormone, insulin-like growth factor-I concentrations, and bone healing in the beagle. Can. J. Vet. Res. 1996, 60:7-13.
17. Dunn S.E., Kari F.W., French J., Leininger J.R., Travlos G., Wilson R., Barrett J.C. Dietary restriction reduces insulin-like growth factor I levels, which modulates apoptosis, cell proliferation, and tumor progression in p53-deficient mice. Cancer Res. 1997, 57:4667-4672.
18. Endres M., Piriz J., Gertz K., Harms C., Meisel A., Kronenberg G., Torres-Aleman I. Serum insulin-like growth factor I and ischemic brain injury. Brain Res. 2007, 1185:328-335.
19. Felsenstein J. Phylogenies and the comparative method. Am. Nat. 1985, 125:1-15.
20. Fontana L., Weiss E.P., Villareal D.T., Klein S., Holloszy J.O. Long-term effects of calorie or protein restriction on serum IGF-1 and IGFBP-3 concentration in humans. Aging Cell 2008, 7:681-687.
21. Garcia J.M., Cata J.P., Dougherty P.M., Smith R.G. Ghrelin prevents cisplatin-induced mechanical hyperalgesia and cachexia. Endocrinology 2008, 149:455-460.
22. Garland T., Bennett A.F., Rezende E.L. Phylogenetic approaches in comparative physiology. J. Exp. Biol. 2005, 208:3015-3035.
23. 15N signatures and insulin-like growth factor. Ursus 2002, 13:285-291.
24. Harper J.M., Durkee S.J., Dysko R.C., Austad S.N., Miller R.A. Genetic modulation of hormone levels and life span in hybrids between laboratory and wild-derived mice. J. Gerontol. A: Biol. Sci. Med. Sci. 2006, 61:1019-1029.
25. Heidler B., Parvizi N., Sauerwein H., Bruckmaier R.M., Heintges U., Aurich J.E., Aurich C. Effects of lactation on metabolic and reproductive hormones in Lipizzaner mares. Dom. Anim. Endocrinol. 2003, 25:47-59.
26. Hempenstall S., Picchio L., Mitchell S.E., Speakman J.R., Selman C. The impact of acute caloric restriction on the metabolic phenotype in male C57BL/6 and DBA/2 mice. Mech. Ageing Dev. 2010, 131:111-118.
27. Hilleson-Gayne C.K., Clapper J.A. Effects of decreased estradiol-17β on the serum and anterior pituitary IGF-I system in pigs. J. Endocrinol. 2005, 187:369-378.
28. Holzenberger M., Dupont J., Ducos B., Leneuve P., Géloën A., Even P.C., Cervera P., Le Bouc Y. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 2003, 421:182-187.
29. Hulbert A.J., Else P.L. Basal metabolic rate: history, composition, regulation, and usefulness. Physiol. Biochem. Zool. 2004, 77:869-876.
30. Kapahi P., Boulton M.E., Kirkwood T.B. Positive correlation between mammalian life span and cellular resistance to stress. Free Radic. Biol. Med. 1999, 26:495-500.
31. Khandwala H.M., McCutcheon I.E., Flyvbjerg A., Friend K.E. The effects of insulin-like growth factors on tumorigenesis and neoplastic growth. Endocr. Rev. 2000, 21:215-244.
32. Kenyon C.J. The genetics of aging. Nature 2010, 464:504-512.
33. Kooijman R., Sarre S., Michotte Y., De Keyser J. Insulin-like growth factor I: a potential neuroprotective compound for the treatment of acute ischemic stroke?. Stroke 2009, 40:e83-e88.
34. Lee E.K., Gorospe M. Minireview: posttranscriptional regulation of the insulin and insulin-like growth factor systems. Endocrinology 2010, 151:1403-1408.
35. Leifke E., Gorenoi V., Wichers C., von zur Muhlen A., von Buren E., Brabant G. Age-related changes of serum sex hormones, insulin-like growth factor-1 and sex-hormone binding globulin levels in men: cross-sectional data from a healthy male cohort. Clin. Endocrinol. 2000, 53:689-695.
36. Lennox A.R., Goodship A.E. Polar bears (Ursus maritimus), the most evolutionary advanced hibernators, avoid significant bone loss during hibernation. Comp. Biochem. Physiol. A 2008, 149:203-208.
37. Leray V., Siliart B., Dumon H., Martin L., Sergheraert R., Biourge V., Nguyen P. Protein intake does not affect insulin sensitivity in normal weight cats. J. Nutr. 2006, 136:2028S-2030S.
38. Lian F., Chung J., Russell R.M., Wang X.-D. Alcohol-reduced plasma IGF-I levels and hepatic IGF-I expression can be partially restored by retinoic acid supplementation in rats. J. Nutr. 2004, 134:2953-2956.
39. Lincoln G.A., Rhind S.M., Pompolo S., Clarke I.J. Hypothalamic control of photoperiod-induced cycles in food intake, body weight, and metabolic hormones in rams. Am. J. Physiol. 2001, 281:R76-R90.
40. Lindqvist C., Schuster S.C., Sun Y., Talbot S.L., Qi J., Ratan A., Tomsho L.P., Kasson L., Zeyl E., Aars J., Miller W., Ingólfsson O., Bachmann L., Wiig Ø. Complete mitochondrial genome of a Pleistocene jawbone unveils the origin of polar bear. Proc. Natl. Acad. Sci. U. S. A. 2009, 107:5053-5057.
41. Longo V.D., Fontana L. Calorie restriction and cancer prevention: metabolic and molecular mechanisms. Trends Pharmacol. Sci. 2010, 31:89-98.
42. de Magalhães J.P., Costa J., Toussaint O. HAGR: the human ageing genomic resources. Nucleic Acids Res. 2005, 33:D537-D543.
43. Matthee C.A., Davies S.K. Molecular insights into the evolution of the family bovidae: a nuclear DNA perspective. Mol. Biol. Evol. 2001, 18:220-1230.
44. Martins E.P., Garland T. Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution 1991, 45:534-557.
45. Miller R.A., Harper J.M., Dysko R.C., Durkee S.J., Austad S.N. Longer life spans and delayed maturation in wild-derived mice. Exp. Biol. Med. 2002, 227:500-508.
46. Movérare-Skrtic S., Svensson J., Karlsson M.K., Orwoll E., Ljunggren O., Mellström D., Ohlsson C. Serum insulin-like growth factor-I concentration is associated with leukocyte telomere length in a population-based cohort of elderly men. J. Clin. Endocrinol. Metab. 2009, 94:5078-5084.
47. Nielsen M.O., Skakkebaek N.E., Giwercman A. Insulin-like growth factor-I (somatomedin-C) in goats during normal lactation and in response to somatotropin treatment. Comp. Biochem. Physiol. A 1990, 95:303-306.
48. Noble G.K., Houghton E., Roberts C.J., Faustino-Kemp J., de Kock S.S., Swanepoel B.C., Sillence M.N. Effect of exercise, training, circadian rhythm, age, and sex on insulin-like growth factor-1 in the horse. J. Anim. Sci. 2007, 85:163-171.
49. Osorio A., Ruiz E., Ortega E. Possible role of GH/IGF-1 in the ovarian function of adult hypothyroid rats. Mol. Cell. Biochem. 1998, 179:7-11.
50. Page M.M., Richardson J., Wiens B.E., Tiedtke E., Peters C.W., Faure P.A., Burness G., Stuart J.A. Antioxidant enzyme activities are not broadly correlated with longevity in 14 endotherm species. Age 2010, 32:255-270.
51. Philippou A., Halapas A., Maridaki M., Koutsilieris M. Type I insulin-like growth factor receptor signaling in skeletal muscle regeneration and hypertrophy. J. Musculoskelet. Neuronal Interact. 2007, 7:208-218.
52. Pitra C., Fickela J., Meijaard E., Groves P.C. Evolution and phylogeny of old world deer. Mol. Phylogenet. Evol. 2004, 33:880-895.
53. Porter R.K. Allometry of mammalian cellular oxygen consumption. Cell. Mol. Life Sci. 2001, 58:815-822.
54. Price T. Correlated evolution and independent contrasts. Philos. Trans. R. Soc. Lond. B 1997, 352:519-529.
55. Ramsey M.M., Ingram R.L., Cashion A.B., Ng A.H., Cline J.M., Parlow A.F., Sonntag W.E. Growth hormone-deficient dwarf animals are resistant to dimethylbenzanthracine (DMBA)-induced mammary carcinogenesis. Endocrinology 2002, 143:4139-4142.
56. Rhinda S.M., McMillen S.R., Duff E., Kyle C.E., Wright S. Effect of long-term feed restriction on seasonal endocrine changes in Soay sheep. Physiol. Behav. 2000, 71:343-351.
57. Robb E.L., Page M.M., Stuart J.A. Mitochondria, cellular stress resistance, somatic cell depletion and lifespan. Curr. Aging Sci. 2009, 1:12-27.
58. Roberts A.J., Klindt J., Jenkins T.G. Effects of varying energy intake and sire breed on duration of postpartum anestrus, insulin like growth factor-1, and growth hormone in mature crossbred cows. J. Anim. Sci. 2005, 83:1705-1714.
59. Rolfe D.F., Brown G.C. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 1997, 77:731-758.
60. Rollo C.D. Growth negatively impacts the life span of mammals. Evol. Dev. 2002, 4:1-5.
61. Rowe N. The Pictorial Guide to Living Primates 1996, Pogonias Press, East Hampton, NY.
62. Schmidt K.E., Kelley K.M. Down-regulation in the insulin-like growth factor (IGF) axis during hibernation in the golden-mantled ground squirrel, Spermophilus lateralis: IGF-I and the IGF-binding proteins (IGFBPs). J. Exp. Zool. 2001, 289:66-73.
63. Scicchitano B.M., Rizzuto E., Musarò A. Counteracting muscle wasting in aging and neuromuscular diseases: the critical role of IGF-1. Aging 2009, 1:451-457.
64. Seluanov A., Chen Z., Hine C., Sasahara T.H., Ribeiro A.A., Catania K.C., Presgraves D.C., Gorbunova V. Telomerase activity coevolves with body mass not lifespan. Aging Cell 2007, 6:45-52.
65. Sherlock M., Toogood A.A. Aging and the growth hormone/insulin like growth factor-1 axis. Pituitary 2007, 10:189-203.
66. Shively C.A., Register T.C., Friedman D.P., Morgan T.M., Thompson J., Lanier T. Social stress-associated depression in adult female cynomolgus monkeys (Macaca fascicularis). Biol. Psychiat. 2005, 69:67-84.
67. Sirotkin A.V., Rafay J., Kotwica J. Leptin controls rabbit ovarian function in vivo and in vitro: possible interrelationships with ghrelin. Theriogenology 2009, 72:765-772.
68. Sonntag W.E., Carter C.S., Ikeno Y., Ekenstedt K., Carlson C.S., Loeser R.F., Chakrabarty S., Lee S., Bennett C., Ingram R., Moore T., Ramsey M. Adult-onset growth hormone and insulin-like growth factor I deficiency reduces neoplastic disease, modifies age-related pathology, and increases life span. Endocrinology 2005, 146:2920-2932.
69. Sonntag W.E., Bennett C., Ingram R., Donahue A., Ingraham J., Chen H., Moore T., Brunso-Bechtold J.K., Riddle D. Growth hormone and IGF-I modulate local cerebral glucose utilization and ATP levels in a model of adult-onset growth hormone deficiency. Am. J. Physiol. Endocrinol. Metab. 2006, 291:E604-E610.
70. Speakman J.R. Correlations between physiology and lifespan-two widely ignored problems with comparative studies. Aging Cell 2005, 4:167-175.
71. Spicer L.J., Hanrahan J.P., Zavy M.T., Enright W.J. Relationship between ovulation rate and concentrations of insulin-like growth factor-1 in plasma during the oestrous cycle in various genotypes of sheep. J. Reprod. Fertil. 1993, 97:403-409.
72. Spichiger A.C., Allenspach K., Zbinden Y., Doherr M.G., Hiss S., Blum J.W., Sauter S.N. Plasma insulin-like growth factor-1 concentration in dogs with chronic enteropathies. Vet. Med. 2006, 51:35-43.
73. Springer M.S., Murphy W.J. Mammalian evolution and biomedicine: new views from phylogeny. Biol. Rev. 2007, 82:375-392.
74. Stahl W.R. Organ weights in primates and other mammals. Science 1965, 150:1039-1042.
75. Stratikopoulos E., Szabolcs M., Dragatsis I., Klinakis A., Efstratiadis A. The hormonal action of IGF1 in postnatal mouse growth. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19378-19383.
76. Suzuki A., Ishida T. Age changes in plasma IGF-1 concentration in free-ranging Japanese macaques (Macaca fuscata). J. Med. Primatol. 2001, 30:174-178.
77. Suzuki K., Nakagawa M., Katoh K., Kadowaki H., Shibata T., Uchida H., Obara Y., Nishida A. Genetic correlation between serum insulin-like growth factor-1 concentration and performance and meat quality traits in Duroc pigs. J. Anim. Sci. 2004, 82:994-999.
78. Suzuki J., Kato A., Maeda N., Hashimoto C., Uchikoshi M., Mizutani T., Doke C., Matsuzawa T. Plasma insulin-like growth factor-I, testosterone and morphological changes in the growth of captive agile gibbons (Hylobates agilis) from birth to adolescence. Primates 2003, 44:273-280.
79. Suzuki J., Ohkura S., Hayakawa S., Hamada Y. Time series analysis of plasma insulin-like growth factor-I and gonadal steroids in adolescent japanese macaques (Macaca fuscata). J. Reprod. Dev. 2000, 46:157-166.
80. Tarasiuk A., Segev Y. Chronic resistive airway loading reduces weight due to low serum IGF-1 in rats. Respir. Physiol. Neurobiol. 2005, 145:177-182.
81. Ten Broek R.W., Grefte S., Von den Hoff J.W. Regulatory factors and cell populations involved in skeletal muscle regeneration. J. Cell Physiol. 2010, (Epub. Mar 15).
82. Terrien J., Zizzari P., Bluet-Pajot M.-T., Henry P.-Y., Perret M., Epelbaum J., Aujard F. Effects of age on thermoregulatory responses during cold exposure in a nonhuman primate, Microcebus murinus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R696-R703.
83. Tomas M., Walton P.E., Dunshea F.R., Ballard F.J. IGF-I variants which bind poorly to IGF-binding proteins show more potent and prolonged hypoglycaemic action than native IGF-I in pigs and marmoset monkeys. J. Endocrinol. 1997, 155:377-386.
84. Videan E.N., Heward C.B., Chowdhury K., Plummer J., Su Y., Cutler R.G. Comparison of biomarkers of oxidative stress and cardiovascular disease in humans and chimpanzess (Pan troglodytes). Comp. Med. 2009, 59:287-296.
85. Waggoner J.W., Löest C.A., Mathis C.P., Hallford D.M., Petersen M.K. Effects of rumen-protected methionine supplementation and bacterial lipopolysaccharide infusion on nitrogen metabolism and hormonal responses of growing beef steers. J. Anim. Sci. 2009, 87:681-692.
86. Wetterau L.A., Francis M.J., Ma L., Cohen P. Insulin-like growth factor I stimulates telomerase activity in prostate cancer cells. J. Clin. Endocrinol. Metab. 2003, 88:3354-3359.
87. Wu Y., Yakar S., Zhao L., Hennighausen L., LeRoith D. Circulating insulin-like growth factor-I levels regulate colon cancer growth and metastasis. Cancer Res. 2002, 62:1030-1035.
88. Yakar S., Liu J.L., 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. U. S. A. 1999, 96:7324-7329.
89. Yakar S., Wu Y., Setser J., Rosen C.J. The role of circulating IGF-I: lessons from human and animal models. Endocrine 2002, 19:239-248.
90. Yang Z., Yoder A.D. Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene loci and calibration points, with application to a radiation of cute-looking mouse lemur species. Syst. Biol. 2003, 52:705-716.
91. Yuan R., Tsaih S.W., Petkova S.B., Marin de Evsikova C., Xing S., Marion M.A., Bogue M.A., Mills K.D., Peters L.L., Bult C.J., Rosen C.J., Sundberg J.P., Harrison D.E., Churchill G.A., Paigen B. Aging in inbred strains of mice: study design and interim report on median lifespans and circulating IGF1 levels. Aging Cell 2009, 8:277-287.