Growth hormone modulates hypothalamic inflammation in long-lived pituitary dwarf mice

Aging Cell

Volumn 14, Issue 6, 2015, Pages 1045-1054

  Sadagurski, Marianna ^a   Landeryou, Taylor ^b   Cady, Gillian ^b   Kopchick, John J ^c   List, Edward O ^c   Berryman, Darlene E ^c   Bartke, Andrzej ^d   Miller, Richard A ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c OHIO UNIVERSITY   (United States)

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

Author keywords

Aging; Dwarf mice; Growth hormone; Hypothalamus; Inflammation; Longevity

Indexed keywords

AGOUTI RELATED PEPTIDE; AGOUTI RELATED PROTEIN; ANOREXIGENIC PROOPIOMELANOCORTIN; GROWTH HORMONE; LEPTIN; PEPTIDE; PROOPIOMELANOCORTIN; UNCLASSIFIED DRUG; AGRP PROTEIN, MOUSE; CARRIER PROTEIN; INSULIN; INSULIN-LIKE GROWTH FACTOR-1, MOUSE; SOMATOMEDIN C; SOMATOTROPIN-BINDING PROTEIN; STAT3 PROTEIN; STAT3 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARCUATE NUCLEUS; ARTICLE; CONTROLLED STUDY; FEMALE; HYPOTHALAMIC INFLAMMATION; HYPOTHALAMUS; INFLAMMATION; LIFE EXTENSION; LONGEVITY; MALE; MOUSE; MUTATION; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PITUITARY DWARFISM; PRIORITY JOURNAL; THALAMUS DORSOMEDIAL NUCLEUS; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; GENETICS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; KNOCKOUT MOUSE; LIVER; METABOLISM; PATHOLOGY;

AGOUTI-RELATED PROTEIN; ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; CARRIER PROTEINS; DWARFISM, PITUITARY; GROWTH HORMONE; INFLAMMATION; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LEPTIN; LIVER; LONGEVITY; MALE; MEDIODORSAL THALAMIC NUCLEUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PRO-OPIOMELANOCORTIN; STAT3 TRANSCRIPTION FACTOR;

EID: 84954392616     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12382     Document Type: Article

References (47)

1. Baquedano E, Ruiz-Lopez AM, Sustarsic EG, Herpy J, List EO, Chowen JA, Frago LM, Kopchick JJ, Argente J (2014) The absence of GH signaling affects the susceptibility to high-fat diet-induced hypothalamic inflammation in male mice. Endocrinology 155, 4856-4867.
2. Bartke A (2008) New findings in gene knockout, mutant and transgenic mice. Exp. Gerontol. 43, 11-14.
3. Bartke A (2011) Single-gene mutations and healthy ageing in mammals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 28-34.
4. Bartke A, Brown-Borg H (2004) Life extension in the dwarf mouse. Curr. Top. Dev. Biol. 63, 189-225.
5. Bartke A, Sun LY, Longo V (2013) Somatotropic signaling: trade-offs between growth, reproductive development, and longevity. Physiol. Rev. 93, 571-598.
6. Blissett J, Harris G, Kirk J (2000) Effect of growth hormone therapy on feeding problems and food intake in children with growth disorders. Acta Paediatr. 89, 644-649.
7. Bohlooly YM, Olsson B, Bruder CE, Linden D, Sjogren K, Bjursell M, Egecioglu E, Svensson L, Brodin P, Waterton JC, Isaksson OG, Sundler F, Ahren B, Ohlsson C, Oscarsson J, Tornell J (2005) Growth hormone overexpression in the central nervous system results in hyperphagia-induced obesity associated with insulin resistance and dyslipidemia. Diabetes 54, 51-62.
8. Bonkowski MS, Pamenter RW, Rocha JS, Masternak MM, Panici JA, Bartke A (2006) Long-lived growth hormone receptor knockout mice show a delay in age-related changes of body composition and bone characteristics. J. Gerontol. A Biol. Sci. Med. Sci. 61, 562-567.
9. Bouret SG, Simerly RB (2006) Developmental programming of hypothalamic feeding circuits. Clin. Genet. 70, 295-301.
10. Bouret SG, Simerly RB (2007) Development of leptin-sensitive circuits. J. Neuroendocrinol. 19, 575-582.
11. Bouret SG, Gorski JN, Patterson CM, Chen S, Levin BE, Simerly RB (2008) Hypothalamic neural projections are permanently disrupted in diet-induced obese rats. Cell Metab. 7, 179-185.
12. Bouret SG, Bates SH, Chen S, Myers MG Jr, Simerly RB (2012) Distinct roles for specific leptin receptor signals in the development of hypothalamic feeding circuits. J. Neurosci. 32, 1244-1252.
13. Chan YY, Steiner RA, Clifton DK (1996) Regulation of hypothalamic neuropeptide-Y neurons by growth hormone in the rat. Endocrinology 137, 1319-1325.
14. Chandrashekar V, Bartke A, Coschigano KT, Kopchick JJ (1999) Pituitary and testicular function in growth hormone receptor gene knockout mice. Endocrinology 140, 1082-1088.
15. Conover CA, Bale LK (2007) Loss of pregnancy-associated plasma protein A extends lifespan in mice. Aging Cell 6, 727-729.
16. Dominick G, Berryman DE, List EO, Kopchick JJ, Li X, Miller RA, Garcia GG (2015) Regulation of mTOR activity in snell dwarf and GH receptor gene-disrupted mice. Endocrinology 156, 565-575.
17. 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.
18. Harrison DE, Strong R, Allison DB, Ames BN, Astle CM, Atamna H, Fernandez E, Flurkey K, Javors MA, Nadon NL, Nelson JF, Pletcher S, Simpkins JW, Smith D, Wilkinson JE, Miller RA (2014) Acarbose, 17-alpha-estradiol, and nordihydroguaiaretic acid extend mouse lifespan preferentially in males. Aging Cell 2, 273-282.
19. Hurley DL, Birch DV, Almond MC, Estrada IJ, Phelps CJ (2003) Reduced hypothalamic neuropeptide Y expression in growth hormone- and prolactin-deficient Ames and Snell dwarf mice. Endocrinology 144, 4783-4789.
20. 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.
21. Ikeno Y, Hubbard GB, Lee S, Cortez LA, Lew CM, Webb CR, Berryman DE, List EO, Kopchick JJ, Bartke A (2009) Reduced incidence and delayed occurrence of fatal neoplastic diseases in growth hormone receptor/binding protein knockout mice. J. Gerontol. A Biol. Sci. Med. Sci. 64, 522-529.
22. Junnila RK, List EO, Berryman DE, Murrey JW, Kopchick JJ (2013) The GH/IGF-1 axis in ageing and longevity. Nat. Rev. Endocrinol. 9, 366-376.
23. Kamegai J, Minami S, Sugihara H, Higuchi H, Wakabayashi I (1994) Growth hormone induces expression of the c-fos gene on hypothalamic neuropeptide-Y and somatostatin neurons in hypophysectomized rats. Endocrinology 135, 2765-2771.
24. Kamegai J, Hasegawa O, Minami S, Sugihara H, Wakabayashi I (1996) The growth hormone-releasing peptide KP-102 induces c-fos expression in the arcuate nucleus. Brain Res. Mol. Brain Res. 39, 153-159.
25. Leinninger GM, Myers MG Jr (2008) LRb signals act within a distributed network of leptin-responsive neurones to mediate leptin action. Acta Physiol. (Oxf). 192, 49-59.
26. List EO, Berryman DE, Funk K, Jara A, Kelder B, Wang F, Stout MB, Zhi X, Sun L, White TA, LeBrasseur NK, Pirtskhalava T, Tchkonia T, Jensen EA, Zhang W, Masternak MM, Kirkland JL, Miller RA, Bartke A, Kopchick JJ (2014) Liver-specific GH receptor gene-disrupted (LiGHRKO) mice have decreased endocrine IGF-I, increased local IGF-I, and altered body size, body composition, and adipokine profiles. Endocrinology 155, 1793-1805.
27. Masternak MM, Bartke A (2012) Growth hormone, inflammation and aging. Pathobiol. Aging Age Relat. Dis. 2, 17293-DOI.
28. Meyer CW, Klingenspor M, Rozman J, Heldmaier G (2004) Gene or size: metabolic rate and body temperature in obese growth hormone-deficient dwarf mice. Obes. Res. 12, 1509-1518.
29. Miller RA, Harrison DE, Astle CM, Baur JA, Boyd AR, de CR, Fernandez E, Flurkey K, Javors MA, Nelson JF, Orihuela CJ, Pletcher S, Sharp ZD, Sinclair D, Starnes JW, Wilkinson JE, Nadon NL, Strong R (2011) Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J. Gerontol. A Biol. Sci. Med. Sci. 66, 191-201.
30. Muller EE, Locatelli V, Cocchi D (1999) Neuroendocrine control of growth hormone secretion. Physiol. Rev. 79, 511-607.
31. Munzberg H, Flier JS, Bjorbaek C (2004) Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology 145, 4880-4889.
32. Myers MG Jr (2004) Leptin receptor signaling and the regulation of mammalian physiology. Recent Prog. Horm. Res. 59, 287-304.
33. Nyberg F (2000) Growth hormone in the brain: characteristics of specific brain targets for the hormone and their functional significance. Front. Neuroendocrinol. 21, 330-348.
34. Panici JA, Harper JM, Miller RA, Bartke A, Spong A, Masternak MM (2010) Early life growth hormone treatment shortens longevity and decreases cellular stress resistance in long-lived mutant mice. FASEB J. 24, 5073-5079.
35. Patterson CM, Bouret SG, Park S, Irani BG, Dunn-Meynell AA, Levin BE (2010) Large litter rearing enhances leptin sensitivity and protects selectively bred diet-induced obese rats from becoming obese. Endocrinology 151, 4270-4279.
36. Peng XD, Park S, Gadelha MR, Coschigano KT, Kopchick JJ, Frohman LA, Kineman RD (2001) The growth hormone (GH)-axis of GH receptor/binding protein gene-disrupted and metallothionein-human GH-releasing hormone transgenic mice: hypothalamic neuropeptide and pituitary receptor expression in the absence and presence of GH feedback. Endocrinology 142, 1117-1123.
37. Sadagurski M, Norquay L, Farhang J, D'Aquino K, Copps K, White MF (2010) Human IL6 enhances leptin action in mice. Diabetologia 53, 525-535.
38. Sadagurski M, Leshan RL, Patterson C, Rozzo A, Kuznetsova A, Skorupski J, Jones JC, DePinho RA, Myers MG Jr, White MF (2012) IRS2 signaling in LepR-b neurons suppresses FoxO1 to control energy balance independently of leptin action. Cell Metab. 15, 703-712.
39. Sadagurski M, Landeryou T, Cady G, Bartke A, Bernal-Mizrachi E, Miller RA (2015) Transient early food restriction leads to hypothalamic changes in the long-lived crowded litter female mice. Physiol. Rep. 3, pii: e12379.
40. Sonntag WE, Ramsey M, Carter CS (2005) Growth hormone and insulin-like growth factor-1 (IGF-1) and their influence on cognitive aging. Ageing Res. Rev. 4, 195-212.
41. Strong R, Miller RA, Astle CM, Floyd RA, Flurkey K, Hensley KL, Javors MA, Leeuwenburgh C, Nelson JF, Ongini E, Nadon NL, Warner HR, Harrison DE (2008) Nordihydroguaiaretic acid and aspirin increase lifespan of genetically heterogeneous male mice. Aging Cell 7, 641-650.
42. Sun L, Sadighi Akha AA, Miller RA, Harper JM (2009) Life-span extension in mice by preweaning food restriction and by methionine restriction in middle age. J. Gerontol. A Biol. Sci. Med. Sci. 64, 711-722.
43. Sun LY, Spong A, Swindell WR, Fang Y, Hill C, Huber JA, Boehm JD, Westbrook R, Salvatori R, Bartke A (2013) Growth hormone-releasing hormone disruption extends lifespan and regulates response to caloric restriction in mice. eLife 2, e01098.
44. Vergara M, Smith-Wheelock M, Harper JM, Sigler R, Miller RA (2004) Hormone-treated snell dwarf mice regain fertility but remain long lived and disease resistant. J. Gerontol. A Biol. Sci. Med. Sci. 59, 1244-1250.
45. Vogt MC, Paeger L, Hess S, Steculorum SM, Awazawa M, Hampel B, Neupert S, Nicholls HT, Mauer J, Hausen AC, Predel R, Kloppenburg P, Horvath TL, Bruning JC (2014) Neonatal insulin action impairs hypothalamic neurocircuit formation in response to maternal high-fat feeding. Cell 156, 495-509.
46. Woods KA, Camacho-Hubner C, Savage MO, Clark AJ (1996) Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N. Engl. J. Med. 335, 1363-1367.
47. Zhang G, Li J, Purkayastha S, Tang Y, Zhang H, Yin Y, Li B, Liu G, Cai D (2013) Hypothalamic programming of systemic ageing involving IKK-beta, NF-kappaB and GnRH. Nature 497, 211-216.