Download PDF
Horm Metab Res 2006; 38(4): 260-268
DOI: 10.1055/s-2006-925347
Original
© Georg Thieme Verlag KG Stuttgart · New York

Plasma-binding Globulins and Acute Stress Response

C.  W.  Breuner1 , S.  E.  Lynn2 , G.  E.  Julian1 , J.  M.  Cornelius3 , B.  J.  Heidinger4 , O.  P.  Love5 , R.  S.  Sprague1 , H.  Wada1 , B.  A.  Whitman6
  • 1 Integrative Biology, University of Texas at Austin, Austin, TX
  • 2 Department of Biology, College of Wooster, Wooster, OH
  • 3 Neurobiology, Physiology and Behavior, University of California Davis, Davis, CA
  • 4 Biology, Indiana University, Bloomington, IN
  • 5 Biological Sciences, Simon Fraser University, Burnaby, BC
  • 6 Department of Biology, Boise State University, Boise, ID, USA
Further Information

Publication History

Received 30 September 2005

Accepted after revision 24 January 2006

Publication Date:
15 May 2006 (online)

Also available at
    Permissions and Reprints

Abstract

Within studies of acute stress physiology an increase in glucocorticoid secretion is thought to be the primary mediator of tissue response to stress. Corticosteroid-binding globulin may regulate tissue availability of steroids, but has not been considered a dynamic component of the acute stress response. Here, we examined CBG level over the common 60-minute time frame in an acute capture and handling protocol to investigate whether CBG capacity is dynamic or static over short stressors. Using a comparative approach, we measured CBG response to capture and handling stress in nine species of birds, representing five orders and nine families. CBG capacity significantly declined within 30 - 60 minutes of capture in five of the nine species examined. This decline may serve to significantly increase the level of corticosterone reaching tissues during acute stress.

Key words

Corticosterone - free CORT - birds

References

  • 1 Wingfield J C, Maney D L, Breuner C W, Jacobs J D, Lynn S, Ramenofsky M, Richardson R D. Ecological bases of hormone-behavior interactions: The ”emergency life history stage“.  Amer Zool. 1998;  38 191-206
    PubMedSearch in Google Scholar
  • 2 Wingfield J C. The concept of allostasis: coping with a capricious environment.  J Mammol. 2005;  86 248-254
    PubMedSearch in Google Scholar
  • 3 Sapolsky R M, Romero L M, Munck A U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions.  Endocrine Rev. 2000;  21 55-89
    CrossrefPubMedSearch in Google Scholar
  • 4 O’Reilly K M, Wingfield J C. Ecological factors underlying the adrenocortical response to capture stress in arctic-breeding shorebirds.  Gen Comp Endocrinol. 2001;  124 1-11
    CrossrefPubMedSearch in Google Scholar
  • 5 Smith G T, Wingfield J C, Veit R R. Adrenocortical response to stress in the common diving petrel, Pelecanoides urinatrix.  Phys Zool. 1994;  67 526-537
    PubMedSearch in Google Scholar
  • 6 Dunlap K D, Wingfield J C. External and Internal Influences on Indices of Physiological Stress. I. Seasonal and Population Variation in Adrenocortical Secretion of Free-Living Lizards, Sceloporus occidentalis.  J Exp Zool. 1995;  271 36-46
    CrossrefPubMedSearch in Google Scholar
  • 7 Breuner C W, Hahn T P. Integrating stress physiology, environmental change, and behavior in free-living sparrows.  Horm Behav. 2003;  43 115-123
    CrossrefPubMedSearch in Google Scholar
  • 8 Breuner C W, Orchinik M, Hahn T P, Meddle S, Moore I T, Owen-Ashley N, Sperry T S, Wingfield J C. Differential mechanisms for regulation of the stress response across latitudinal gradients.  American Journal of Physiology: Regulatory, Comparative, and Integrative Physiology. 2003;  285 R594-R600
    PubMedSearch in Google Scholar
  • 9 Wada H, Hahn T P, Breuner C W. Binding globulins extend stress hyporesponsive period in altricial white-crowned sparrow nestlings.  Gen Comp Endocrinol. in review; 
    PubMedSearch in Google Scholar
  • 10 Breuner C W, Orchinik M. Seasonal regulation of membrane and intracellular corticosteroid receptors in the house sparrow brain.  J Neuroendocrinol. 2001;  13 412-420
    CrossrefPubMedSearch in Google Scholar
  • 11 Adams N J, Cockrem J F, Taylor G A, Candy E J, Bridges J. Corticosterone responses of grey-faced petrels (Pterodroma macroptera gouldi) are higher during incubation than during other breeding stages.  Physiol Biochem Zool. 2005;  78 69-77
    CrossrefPubMedSearch in Google Scholar
  • 12 Mendel C M. The free hormone hypothesis: a physiologically based mathematical model.  Endorcrine Reviews. 1989;  10 232-274
    PubMedSearch in Google Scholar
  • 13 Breuner C W, Orchinik M. Plasma Binding Proteins As Mediators Of Corticosteroid Action In Vertebrates.  J Endocrinol. 2002;  175 99-112
    CrossrefPubMedSearch in Google Scholar
  • 14 Hammond G L. Potential functions of plasma steroid-binding proteins.  TEM. 1995;  6 298-304
    PubMedSearch in Google Scholar
  • 15 Rosner W. The functions of corticosteroid-binding globulin and sex hormone-binding globulin: recent advances.  Endocrine Rev. 1990;  11 80-91
    CrossrefPubMedSearch in Google Scholar
  • 16 Sivukhina E V, Jirikowski G F, Bernstein H G, Lewis J G, Herbert Z. Expression of corticosteroid-binding protein in the human hypothalamus, co-localization with oxytocin and vasopressin.  Hormone and Metabolic Research. 2006;  38 252-258
    PubMedSearch in Google Scholar
  • 17 Möpert B, Herbert Z, Caldwell J D, Jirikowski G F. Expression of corticosteroid-binding globulin CBG in the rat hypothalamus.  Hormone and Metabolic Research. 2006;  38 245-251
    PubMedSearch in Google Scholar
  • 18 Kiseleva E P, Vashkevich I I, Strelchenok O A. Effect of Steroids on Transcortin Binding to Human Syncytiotrophoblast.  Biochemistry-Moscow. 1993;  58 1322-1327
    PubMedSearch in Google Scholar
  • 19 Grasa M D, Cabot C, Adan C, de Matteis R, Esteve M, Cinti S, Fernandez-Lopez J A, Remesar X, Alemany M. Corticosteroid-binding globulin synthesis and distribution in rat white adipose tissue.  Molecular and Cellular Biochemistry. 2001;  228 25-31
    CrossrefPubMedSearch in Google Scholar
  • 20 Marti O, Martin M, Gavalda A, Giralt M, Hidalgo J, Hsu B RS, Kuhn R W, Armario A. Inhibition of corticosteroid-binding globulin caused by a severe stressor is apparently mediated by the adrenal but not by glucocorticoid receptors.  Endocrine. 1997;  6 159-164
    PubMedSearch in Google Scholar
  • 21 Lynn S E, Breuner C W, Wingfield J C. The effects of short-term fasting on activity, corticosterone, and corticosterone binding globulin in a migratory songbird, Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii).  Horm Behav. 2003;  43 150-157
    CrossrefPubMedSearch in Google Scholar
  • 22 Tinnikov A A. Responses of serum corticosterone and corticosteroid-binding globulin to acute and prolonged stress in the rat.  Endocrine. 1999;  11 145-150
    CrossrefPubMedSearch in Google Scholar
  • 23 Love O P, Breuner C W, Vezina F, Williams T D. Mediation of corticosterone-induced reproductive conflict.  Horm Behav. 2004;  46 59-65
    CrossrefPubMedSearch in Google Scholar
  • 24 Ketterson E D, Nolan J V, Wolf L, Zeigenfus C, Dufty A M, Bass G F, Johnsen T S. Testoserone and avian life histories: the effects of experimentally elevated testosterone on corticosterone and body mass in dark-eyed juncos.  Horm Behav. 1991;  25 489-503
    CrossrefPubMedSearch in Google Scholar
  • 25 Barsano C P, Baumann G. Editorial: simple algebraic and graphic methods for the apportionment of hormone (and receptor) into bound and free fractions in binding equilibria; or how to calculate bound and free hormone?.  Endocrinol. 1989;  124 1101-1106
    PubMedSearch in Google Scholar
  • 26 Seabury Sprague R, Breuner C W. Timing of fledging, body condition, and corticosteroid-binding globulin in Laysan Albatross.  Integr Comp Biol. 2005;  45 1070
    PubMedSearch in Google Scholar
  • 27 Breuner C W, Wingfield J C. Rapid behavioral response to corticosterone varies with photoperiod and dose.  Horm Behav. 2000;  37 23-30
    CrossrefPubMedSearch in Google Scholar
  • 28 Diamond D M, Bennett M C, Fleshner M, Rose G M. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation.  Hippocampus. 1992;  2 421-430
    CrossrefPubMedSearch in Google Scholar
  • 29 Hayden-Hixon D M, Ferris C F. Cortisol exerts site-, context- and dose-dependent effects on agonistic responding in hamsters.  J Neuroendocrinol. 1991;  3 613-622
    PubMedSearch in Google Scholar
  • 30 Sandi C, Venero C, Guaza C. Novelty-related rapid locomotor effects of corticosterone in rats.  Eur J of Neurosci. 1996;  8 794-800
    PubMedSearch in Google Scholar
  • 31 Kovacs G L, Telegdy G, Lissak K. Dose-dependent action of corticosteroids on brain serotonin content and passive avoidance behavior.  Horm Behav. 1977;  8 155-165
    CrossrefPubMedSearch in Google Scholar
  • 32 Roozendaal B. Curt P. Richter Award - Glucocorticoids and the regulation of memory consolidation.  Pshychoneuroendocrinology. 2000;  25 213-238
    PubMedSearch in Google Scholar
  • 33 Kuhn R W, Green A L, Raymoure W J, Siiteri P K. Immunocytochemical localization of corticosteroid-binding globulin in rat tissues. J.  Endocrinol.. 1986;  108 31-36
    PubMedSearch in Google Scholar
  • 34 Scrocchi L A, Orava M, Smith C L, Han V KM, Hammond G L. Spatial and temporal distribution of corticosteroid-binding globulin and its messenger ribonucleic acid in embryonic and fetal mice.  Endocrinol. 1993;  132 903-909
    CrossrefPubMedSearch in Google Scholar
  • 35 Hammond G L, Smith C L, Goping I S, Underhill D A, Harley M J, Reventos J, Musto N A, Gunsalus G L, Bardin C W. Primary structure of human corticosteroid-binding globulin, deduced from hepatic and pulmonary cDNAs, exhibits homology with serine protease inhibitors.  PNAS. 1987;  84 5153-5157
    PubMedSearch in Google Scholar
  • 36 Perrot-Applanat M, Racadot O, Milgrom E. Specific localization of plasma corticosteroid-binding globulin immunoreactivity in pituitary corticotrophs.  Endocrinol. 1984;  115 559-569
    PubMedSearch in Google Scholar
  • 37 Kuhn R W. Corticosteroid-Binding Globulin Interactions with Target-Cells and Plasma-Membranes.  Ann N.Y. Acad Sci. 1988;  538 146-158
    CrossrefPubMedSearch in Google Scholar
  • 38 Hryb D J, Khan M S, Romas N A, Rosner W. Specific binding of human corticosteroid-binding globulin to cell membranes.  PNAS. 1986;  83 3253
    PubMedSearch in Google Scholar
  • 39 Singer C J, Khan M S, Rosner W. Characteristics of the binding of corticosteroid-binding globulin to rat cell membranes.  Endocrinol. 1988;  122 89
    PubMedSearch in Google Scholar
  • 40 Esposito P, Gheorghe D, Kandere K, Pang X, Connolly R, Jacobson S, Theoharides T C. Acute stress increases permeability of the blood-brain-barrier through activation of brain mast cells.  Brain Res. 2001;  888 117-127
    CrossrefPubMedSearch in Google Scholar
  • 41 Bested A C, Saunders P R, Logan A C. Chronic fatigue syndrome: neurological findings may be related to blood-brain barrier permeability.  Medical Hypotheses. 2001;  57 231-237
    CrossrefPubMedSearch in Google Scholar
  • 42 Madrigal J L, Moro M A, Lizasoain I, Lorenzo P, Leza J C. Stress-induced increase in extracellular sucrose space in rats is mediated by nitric oxide.  Brain Res. 2002;  938 87-91
    CrossrefPubMedSearch in Google Scholar
  • 43 Nakhla A M, Khan M S, Rosner W. Induction of adenylate cyclase in a mammary carcinoma cell line by human corticosteroid-binding globulin.  Biochemical and Biophysical Research Communication. 1988;  153 1012
    CrossrefPubMedSearch in Google Scholar
  • 44 Strel’chyonok O A, Avvakumov G V. Interaction of human CBG with cell-membranes.  J Steroid Biochem Mol Biol. 1991;  40 795-803
    CrossrefPubMedSearch in Google Scholar
  • 45 Orchinik M. Glucocorticoids, stress, and behavior: shifting the timeframe.  Horm Behav. 1998;  34 320-327
    CrossrefPubMedSearch in Google Scholar
  • 46 Hammes A, Andreassen T K, Spoelgen R, Raila J, Hubner N, Schulz H, Metzger J, Schweigert F J, Luppa P B, Nykjaer A, Willnow T E. Role of endocytosis in cellular uptake of sex steroids.  Cell. 2005;  122 751-762
    CrossrefPubMedSearch in Google Scholar
  • 47 Caldwell J D, Suleman F, Chou S H-H, Shapiro R, Herbert Z, Jirikowski G F. Binding globulins on the rapid effects of steroids.  Hormone and Metabolic Research. (in press); 
    PubMedSearch in Google Scholar
  • 48 Jennings D H, Moore M C, Knapp R, Matthews L, Orchinik M. Plasma steroid-binding globulin mediation of differences in stress reactivity in alternative male phenotypes in tree lizards, Urosaurus ornatus.  Gen Comp Endocrinol. 2000;  120 289-299
    CrossrefPubMedSearch in Google Scholar

C. W. Breuner

The University of Montana, Division of Biological Sciences

32 Campus Drive · Missoula MT 59812-4824 · USA

Fax: +1 (406) 243-4184

Email: creagh@montana.edu (from june 2006)