Ethanol alters the relationship between IGF-1 and bone turnover in male macaques

in Journal of Endocrinology
Authors:
Lara H SattgastSkeletal Biology Laboratory, School of Biological and Population Health Sciences, Oregon State University, Corvallis, Oregon, USA

Search for other papers by Lara H Sattgast in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0001-8724-753X
,
Adam J BranscumBiostatistics Program, School of Biological and Population Health Sciences, Oregon State University, Corvallis, Oregon, USA

Search for other papers by Adam J Branscum in
Current site
Google Scholar
PubMed
Close
,
Natali NewmanDivision of Neuroscience, Oregon National Primate Research Center, Oregon Health and Science University, Beaverton, Oregon, USA

Search for other papers by Natali Newman in
Current site
Google Scholar
PubMed
Close
,
Steven W GonzalesDivision of Neuroscience, Oregon National Primate Research Center, Oregon Health and Science University, Beaverton, Oregon, USA

Search for other papers by Steven W Gonzales in
Current site
Google Scholar
PubMed
Close
,
Mary Lauren BentonDepartment of Computer Science, Baylor University, Waco, Texas, USA

Search for other papers by Mary Lauren Benton in
Current site
Google Scholar
PubMed
Close
,
Erich J BakerDepartment of Computer Science, Baylor University, Waco, Texas, USA

Search for other papers by Erich J Baker in
Current site
Google Scholar
PubMed
Close
,
Kathleen A GrantDivision of Neuroscience, Oregon National Primate Research Center, Oregon Health and Science University, Beaverton, Oregon, USA

Search for other papers by Kathleen A Grant in
Current site
Google Scholar
PubMed
Close
,
Russell T TurnerSkeletal Biology Laboratory, School of Biological and Population Health Sciences, Oregon State University, Corvallis, Oregon, USA

Search for other papers by Russell T Turner in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-3031-0398
, and
Urszula T IwaniecSkeletal Biology Laboratory, School of Biological and Population Health Sciences, Oregon State University, Corvallis, Oregon, USA

Search for other papers by Urszula T Iwaniec in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0001-6203-0932

Correspondence should be addressed to U T Iwaniec: Urszula.Iwaniec@oregonstate.edu
Restricted access

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

USD  $0.01
USD  $0.01

Insulin-like growth factor 1 (IGF-1) influences bone turnover. Transient decreases in IGF-I levels and/or bioavailability may contribute to the detrimental effects of alcohol on bone. The goals of this non-human primate study were to i) evaluate the 20-h response of bone turnover markers to ethanol consumption and ii) assess how ethanol consumption influences the relationship between IGF-1 and these markers. Osteocalcin (bone formation), carboxyterminal cross-linking telopeptide of type 1 collagen (CTX, bone resorption), IGF-1, and IGF binding protein 1 (IGFBP-1) were measured in plasma from male rhesus macaques (N = 10, 8.4 ± 0.3 years) obtained at 12:00, 16:00, and 06:00 h during two phases: pre-ethanol (alcohol-naïve) and ethanol access. During the ethanol access phase, monkeys consumed 1.5 g/kg/day ethanol (4% w/v) beginning at 10:00 h. Osteocalcin and CTX were lower, and the ratio of osteocalcin to CTX was higher at each time point during ethanol access compared to the pre-ethanol phase. Pre-ethanol marker levels did not vary across time points, but markers varied during ethanol access. IGF-1 levels, but not IGFBP-1 levels, varied during the pre-ethanol phase. In contrast, IGF-1 levels were stable during ethanol access but IGFBP-1 levels varied. There were positive relationships between IGF-1 and turnover markers during the pre-ethanol phase, but not during ethanol access. In conclusion, chronic ethanol consumption reduces levels of bone turnover markers and blocks the normal positive relationship between IGF-1 and turnover markers and alters the normal relationship between IGF-1 and IGFBP-1. These findings support the hypothesis that chronic alcohol consumption leads to growth hormone/IGF-1 resistance.

 

  • Collapse
  • Expand

Society for Endocrinology logo

  • Alvisa-Negrín J, González-Reimers E, Santolaria-Fernández F, García-Valdecasas-Campelo E, Valls MRA, Pelazas-González R, Durán-Castellón MC & de Los Angeles Gómez-Rodríguez M 2009 Osteopenia in alcoholics: effect of alcohol abstinence. Alcohol and Alcoholism 44 468475. (https://doi.org/10.1093/alcalc/agp038)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Benton ML, Jimenez VA, Newman N, Gonzales SW, Grant KA, Turner RT, Iwaniec UT & Baker EJ 2022 Dose-response effects of alcohol on biochemical markers of bone turnover in non-human primates: effects of species, sex and age of onset of drinking. Bone Reports 16 101159. (https://doi.org/10.1016/j.bonr.2021.101159)

    • Search Google Scholar
    • Export Citation
  • Birketvedt GS, Geliebter A, Kristiansen I, Firgenschau Y, Goll R & Florholmen JR 2012 Diurnal secretion of ghrelin, growth hormone, insulin binding proteins, and prolactin in normal weight and overweight subjects with and without the night eating syndrome. Appetite 59 688692. (https://doi.org/10.1016/j.appet.2012.07.015)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Chen JR, Lazarenko OP, Shankar K, Blackburn ML, Badger TM & Ronis MJ 2010 A role for ethanol-induced oxidative stress in controlling lineage commitment of mesenchymal stromal cells through inhibition of Wnt/beta-catenin signaling. Journal of Bone and Mineral Research 25 11171127. (https://doi.org/10.1002/jbmr.7)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Daunais JB, Davenport AT, Helms CM, Gonzales SW, Hemby SE, Friedman DP, Farro JP, Baker EJ & Grant KA 2014 Monkey alcohol tissue research resource: banking tissues for alcohol research. Alcoholism, Clinical and Experimental Research 38 19731981. (https://doi.org/10.1111/acer.12467)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Dees WL, Dissen GA, Hiney JK, Lara F & Ojeda SR 2000 Alcohol ingestion inhibits the increased secretion of puberty-related hormones in the developing female rhesus monkey. Endocrinology 141 13251331. (https://doi.org/10.1210/endo.141.4.7413)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Faje AT & Barkan AL 2010 Basal, but not pulsatile, growth hormone secretion determines the ambient circulating levels of insulin-like growth factor-I. Journal of Clinical Endocrinology and Metabolism 95 24862491. (https://doi.org/10.1210/jc.2009-2634)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gaddini GW, Grant KA, Woodall A, Stull C, Maddalozzo GF, Zhang B, Turner RT & Iwaniec UT 2015 Twelve months of voluntary heavy alcohol consumption in male rhesus macaques suppresses intracortical bone remodeling. Bone 71 227236. (https://doi.org/10.1016/j.bone.2014.10.025)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gaddini GW, Turner RT, Grant KA & Iwaniec UT 2016 Alcohol: a simple nutrient with complex actions on bone in the adult skeleton. Alcoholism, Clinical and Experimental Research 40 657671. (https://doi.org/10.1111/acer.13000)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Giustina A, Mazziotti G & Canalis E 2008 Growth hormone, insulin-like growth factors, and the skeleton. Endocrine Reviews 29 535559. (https://doi.org/10.1210/er.2007-0036)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Grant KA, Leng X, Green HL, Szeliga KT, Rogers LSM & Gonzales SW 2008 Drinking typography established by scheduled induction predicts chronic heavy drinking in a monkey model of ethanol self-administration. Alcoholism, Clinical and Experimental Research 32 18241838. (https://doi.org/10.1111/j.1530-0277.2008.00765.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gundberg CM, Markowitz ME, Mizruchi M & Rosen JF 1985 Osteocalcin in human serum: a circadian rhythm. Journal of Clinical Endocrinology and Metabolism 60 736739. (https://doi.org/10.1210/jcem-60-4-736)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kahler-Quesada AM, Grant KA, Walter NAR, Newman N, Allen MR, Burr DB, Branscum AJ, Maddalozzo GF, Turner RT & Iwaniec UT 2019 Voluntary chronic heavy alcohol consumption in male rhesus macaques suppresses cancellous bone formation and increases bone marrow adiposity. Alcoholism, Clinical and Experimental Research 43 24942503. (https://doi.org/10.1111/acer.14202)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kawai M & Rosen CJ 2012 The insulin-like growth factor system in bone: basic and clinical implications. Endocrinology and Metabolism Clinics of North America 41 323333, vi. (https://doi.org/10.1016/j.ecl.2012.04.013)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Klerman EB, Adler GK, Jin M, Maliszewski AM & Brown EN 2003 A statistical model of diurnal variation in human growth hormone. American Journal of Physiology: Endocrinology and Metabolism 285 E1118E1126. (https://doi.org/10.1152/ajpendo.00562.2002)

    • Search Google Scholar
    • Export Citation
  • Kohama SG, Rosene DL & Sherman LS 2012 Age-related changes in human and non-human primate white matter: from myelination disturbances to cognitive decline. Age 34 10931110. (https://doi.org/10.1007/s11357-011-9357-7)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Labib M, Ranganath L, Southgate J, Gama R, Teale D & Marks V 1989 Acute effect of ethanol intake on plasma osteocalcin concentration. Annals of Clinical Biochemistry 26 563564. (https://doi.org/10.1177/000456328902600621)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Marrone JA, Maddalozzo GF, Branscum AJ, Hardin K, Cialdella-Kam L, Philbrick KA, Breggia AC, Rosen CJ, Turner RT & Iwaniec UT 2012 Moderate alcohol intake lowers biochemical markers of bone turnover in postmenopausal women. Menopause 19 974979. (https://doi.org/10.1097/GME.0b013e31824ac071)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Menagh PJ, Turner RT, Jump DB, Wong CP, Lowry MB, Yakar S, Rosen CJ & Iwaniec UT 2010 Growth hormone regulates the balance between bone formation and bone marrow adiposity. Journal of Bone and Mineral Research 25 757768. (https://doi.org/10.1359/jbmr.091015)

    • Search Google Scholar
    • Export Citation
  • Röjdmark S & Brismar K 2001 Decreased IGF-I bioavailability after ethanol abuse in alcoholics: partial restitution after short-term abstinence. Journal of Endocrinological Investigation 24 476482. (https://doi.org/10.1007/BF03343879)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Röjdmark S, Rydvald Y, Aquilonius A & Brismar K 2000 Insulin-like growth factor (IGF)-1 and IGF-binding protein-1 concentrations in serum of normal subjects after alcohol ingestion: evidence for decreased IGF-1 bioavailability. Clinical Endocrinology 52 313318. (https://doi.org/10.1046/j.1365-2265.2000.00908.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ronis MJJ, Wands JR, Badger TM, de la Monte SM, Lang CH & Calissendorff J 2007 Alcohol-induced disruption of endocrine signaling. Alcoholism, Clinical and Experimental Research 31 12691285. (https://doi.org/10.1111/j.1530-0277.2007.00436.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sripanyakorn S, Jugdaohsingh R, Mander A, Davidson SL, Thompson RPH & Powell JJ 2009 Moderate ingestion of alcohol is associated with acute ethanol-induced suppression of circulating ctx in a pth-independent fashion. Journal of Bone and Mineral Research 24 13801388. (https://doi.org/10.1359/JBMR.090222)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Turner RT & Sibonga JD 2001 Effects of alcohol use and estrogen on bone. Alcohol Research and Health 25 276281.

  • Turner RT, Aloia RC, Segel LD, Hannon KS & Bell NH 1988 Chronic alcohol treatment results in disturbed vitamin D metabolism and skeletal abnormalities in rats. Alcoholism, Clinical and Experimental Research 12 159162. (https://doi.org/10.1111/j.1530-0277.1988.tb00152.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Turner RT, Wronski TJ, Zhang M, Kidder LS, Bloomfield SA & Sibonga JD 1998 Effects of ethanol on gene expression in rat bone: transient dose-dependent changes in mRNA levels for matrix proteins, skeletal growth factors, and cytokines are followed by reductions in bone formation. Alcoholism, Clinical and Experimental Research 22 15911599. (https://doi.org/10.1111/j.1530-0277.1998.tb03953.x)

    • Search Google Scholar
    • Export Citation
  • Turner RT, Rosen CJ & Iwaniec UT 2010 Effects of alcohol on skeletal response to growth hormone in hypophysectomized rats. Bone 46 806812. (https://doi.org/10.1016/j.bone.2009.10.027)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Turner RT, Sattgast LH, Jimenez VA, Grant KA & Iwaniec UT 2021 Making sense of the highly variable effects of alcohol on bone. Clinical Reviews in Bone and Mineral Metabolism 19 113. (https://doi.org/10.1007/s12018-021-09277-8)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Vivian JA, Green HL, Young JE, Majerksy LS, Thomas BW, Shively CA, Tobin JR, Nader MA & Grant KA 2001 Induction and maintenance of ethanol self-administration in cynomolgus monkeys (Macaca fascicularis): long-term characterization of sex and individual differences. Alcoholism, Clinical and Experimental Research 25 10871097. (https://doi.org/10.1111/j.1530-0277.2001.tb02321.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wang Y, Nishida S, Elalieh HZ, Long RK, Halloran BP & Bikle DD 2006 Role of IGF-I signaling in regulating osteoclastogenesis. Journal of Bone and Mineral Research 21 13501358. (https://doi.org/10.1359/jbmr.060610)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wichers M, Schmidt E, Bidlingmaier F & Klingmüller D 1999 Diurnal rhythm of crosslaps in human serum. Clinical Chemistry 45 18581860. (https://doi.org/10.1093/clinchem/45.10.1858)

    • Crossref
    • Search Google Scholar
    • Export Citation