Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Sports Medicine
Published in: Sports Medicine 8/2011

01-08-2011 | Review Article

Neuroendocrine-Immune Interactions and Responses to Exercise

Authors: Maren S. Fragala, William J. Kraemer, PhD, Craig R. Denegar, Carl M. Maresh, Andrea M. Mastro, Jeff S. Volek

Published in: Sports Medicine | Issue 8/2011

Login to get access

Abstract

This article reviews the interaction between the neuroendocrine and immune systems in response to exercise stress, considering gender differences. The body’s response to exercise stress is a system-wide effort coordinated by the integration between the immune and the neuroendocrine systems. Although considered distinct systems, increasing evidence supports the close communication between them. Like any stressor, the body’s response to exercise triggers a systematic series of neuroendocrine and immune events directed at bringing the system back to a state of homeostasis. Physical exercise presents a unique physiological stress where the neuroendocrine and immune systems contribute to accommodating the increase in physiological demands. These systems of the body also adapt to chronic overload, or exercise training. Such adaptations alleviate the magnitude of subsequent stress or minimize the exercise challenge to within homeostatic limits. This adaptive capacity of collaborating systems resembles the acquired, or adaptive, branch of the immune system, characterized by the memory capacity of the cells involved. Specific to the adaptive immune response, once a specific antigen is encountered, memory cells, or lymphocytes, mount a response that reduces the magnitude of the immune response to subsequent encounters of the same stress. In each case, the endocrine response to physical exercise and the adaptive branch of the immune system share the ability to adapt to a stressful encounter. Moreover, each of these systemic responses to stress is influenced by gender. In both the neuroendocrine responses to exercise and the adaptive (B lymphocyte) immune response, gender differences have been attributed to the ‘protective’ effects of estrogens. Thus, this review will create a paradigm to explain the neuroendocrine communication with leukocytes during exercise by reviewing (i) endocrine and immune interactions; (ii) endocrine and immune systems response to physiological stress; and (iii) gender differences (and the role of estrogen) in both endocrine response to physiological stress and adaptive immune response.
Literature
1.
Chrousos GP. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N Engl J Med 1995 May 18; 332 (20): 1351–62PubMedCrossRef
2.
Blalock JE, Harbour-McMenamin D, Smith EM. Peptide hormones shared by the neuroendocrine and immunologicsystems. J Immunol 1985 Aug; 135 (2 Suppl.): 858s–61sPubMed
3.
Blalock JE, Smith EM. A complete regulatory loop between the immune and neuroendocrine systems. Fed Proc 1985 Jan; 44(1 Pt 1): 108–11PubMed
4.
Addison T. On the constitutional and local effects of the suprarenal capsules. London: Highley; 1855
5.
Jaffe HL. The influence of the suprarenal gland on the thymus. III: stimulation of the growth of the thymusgland following double suprarenalectomy in young rats. J Exp Med 1924; 40: 753–60PubMedCrossRef
6.
Berczi I, Nagy E, Kovacs K, et al. Regulation of humoral immunity in rats by pituitary hormones. Acta Endocrinol(Copenh) 1981 Dec; 98 (4): 506–13
7.
Nagy E, Berczi I. Immunodeficiency in hypophysectomized rats. Acta Endocrinol (Copenh) 1978 Nov; 89 (3): 530–7
8.
Nagy E, Berczi I, Friesen HG. Regulation of immunity in rats by lactogenic and growth hormones. Acta Endocrinol(Copenh) 1983 Mar; 102 (3): 351–7
9.
Bonnyns M, McKenzie JM. Interactions of stress and endocrine status on rat peripheral lymphocyte responsivenessto phytomitogens. Psychoneuroendocrinology 1979 Jan; 4 (1): 67–73PubMedCrossRef
10.
Smith EM, Blalock JE. Human lymphocyte production of corticotropin and endorphin-like substances: associationwith leukocyte interferon. Proc Natl Acad Sci U S A 1981 Dec; 78 (12): 7530–4PubMedCrossRef
11.
Weigent DA, Blalock JE. Interactions between the neuroendocrine and immune systems: common hormones andreceptors. Immunol Rev 1987 Dec; 100: 79–108PubMedCrossRef
12.
Smith EM, Blalock JE. The hormonal nature of the interferon system. Tex Rep Biol Med 1981; 41: 350–8PubMed
13.
Smith EM, Blalock JE. A molecular basis for interactions between the immune and neuroendocrine systems. IntJ Neurosci 1988 Feb; 38 (3-4): 455–64CrossRef
14.
Blalock JE, Smith EM. Human leukocyte interferon: structural and biological relatedness to adrenocorticotropichormone and endorphins. Proc Natl Acad SciU S A 1980 Oct; 77 (10): 5972–4CrossRef
15.
Meyer 3rd WJ, Smith EM, Richards GE, et al. In vivo immunoreactive adrenocorticotropin (ACTH) productionby human mononuclear leukocytes from normal andACTH-deficient individuals. J Clin Endocrinol Metab 1987 Jan; 64 (1): 98–105PubMedCrossRef
16.
Weigent DA, Baxter JB, Wear WE, et al. Production of immunoreactive growth hormone by mononuclear leukocytes. Faseb J 1988 Sep; 2 (12): 2812–8PubMed
17.
Smith EM, Phan M, Kruger TE, et al. Human lymphocyte production of immunoreactive thyrotropin. Proc Natl Acad Sci U S A 1983 Oct; 80 (19): 6010–3PubMedCrossRef
18.
Johnson HM, Smith EM, Torres BA, et al. Regulation of the in vitro antibody response by neuroendocrine hormones. Proc Natl Acad Sci U S A 1982 Jul; 79 (13): 4171–4PubMedCrossRef
19.
Besedovsky H, Sorkin E. Network of immune-neuroendocrine interactions. Clin Exp Immunol 1977 Jan; 27 (1): 1–12PubMed
20.
Cupps TR, Edgar LC, Fauci AS. Corticosteroid-induced modulation of immunoglobulin secretion by humanB lymphocytes: potentiation of background mitogenicsignals. J Immunopharmacol 1982; 4 (4): 255–63PubMed
21.
Hazum E, Chang KJ, Cuatrecasas P. Opiate (Enkephalin) receptors of neuroblastoma cells: occurrence in clusters onthe cell surface. Science 1979 Nov 30; 206 (4422): 1077–9PubMedCrossRef
22.
Wybran J, Appelboom T, Famaey JP, et al. Suggestive evidence for receptors for morphine and methionineenkephalinon normal human blood T lymphocytes. J Immunol 1979 Sep; 123 (3): 1068–70PubMed
23.
Kincade PW, Medina KL, Payne KJ, et al. Early B-lymphocyte precursors and their regulation by sexsteroids. Immunol Rev 2000 Jun; 175: 128–37PubMedCrossRef
24.
Blalock JE. Production of peptide hormones and neurotransmitters by the immune system. Chem Immunol 1992; 52: 1–24PubMedCrossRef
25.
Blalock JE, Costa O. Immune neuroendocrine interactions: implications for reproductive physiology. Ann N Y Acad Sci 1989; 564: 261–6PubMedCrossRef
26.
Bost KL, Smith EM, Wear LB, et al. Presence of ACTH and its receptor on a B lymphocytic cell line: a possibleautocrine function for a neuroendocrine hormone. J Biol Regul Homeost Agents 1987 Jan-Mar; 1 (1): 23–7PubMed
27.
Malm C, Sjodin TL, Sjoberg B, et al. Leukocytes, cytokines, growth factors and hormones in human skeletalmuscle and blood after uphill or downhill running. J Physiol 2004 May 1; 556 (Pt3): 983–1000PubMedCrossRef
28.
Pedersen BK, Bruunsgaard H, Klokker M, et al. Exerciseinduced immunomodulation: possible roles of neuroendocrineand metabolic factors. Int J Sports Med 1997 Mar; 18 Suppl.1: S2–7CrossRef
29.
Pedersen BK, Rohde T, Ostrowski K. Recovery of the immune system after exercise. Acta Physiol Scand 1998 Mar; 162 (3): 325–32PubMedCrossRef
30.
McCarthy DA, Dale MM. The leucocytosis of exercise: a review and model. Sports Med 1988 Dec; 6 (6): 333–63PubMedCrossRef
31.
Grossman CJ. Regulation of the immune system by sex steroids. Endocr Rev 1984 Summer; 5 (3): 435–55PubMedCrossRef
32.
Gulshan S, McCruden AB, Stimson WH. Oestrogen receptors in macrophages. Scand J Immunol 1990 Jun; 31 (6): 691–7PubMedCrossRef
33.
Schuurs AH, Verheul HA. Effects of gender and sex steroids on the immune response. J Steroid Biochem 1990 Feb; 35 (2): 157–72PubMedCrossRef
34.
Stupka N, Lowther S, Chorneyko K, et al. Gender differences in muscle inflammation after eccentric exercise. J Appl Physiol 2000 Dec; 89 (6): 2325–32PubMed
35.
Tarnopolsky MA. Sex differences in exercise metabolism and the role of 17-beta estradiol. Med Sci Sports Exerc 2008 Apr; 40 (4): 648–54PubMedCrossRef
36.
Selye H. General Adaptation syndrome and disease adaptation. J Clin Endocrinol Metab 1946 Feb; 6: 117–230PubMedCrossRef
37.
Kraemer WJ. Endocrine responses to resistance exercise. Med Sci Sports Exerc 1988 Oct; 20 (5 Suppl.): S152–7PubMed
38.
Kraemer WJ, Ratamess NA. Hormonal responses and adaptations to resistance exercise and training. Sports Med 2005; 35 (4): 339–61PubMedCrossRef
39.
Inoue K, Yamasaki S, Fushiki T, et al. Androgen receptor antagonist suppresses exercise-induced hypertrophy ofskeletal muscle. Eur J Appl Physiol Occup Physiol 1994; 69 (1): 88–91PubMedCrossRef
40.
Ratamess NA, Kraemer WJ, Volek JS, et al. Androgen receptor content following heavy resistance exercise inmen. J Steroid Biochem Mol Biol 2005 Jan; 93 (1): 35–42PubMedCrossRef
41.
Spiering BA, Kraemer WJ, Vingren JL, et al. Elevated endogenous testosterone concentrations potentiate muscleandrogen receptor responses to resistance exercise. J Steroid Biochem Mol Biol 2009 Apr; 114 (3-5): 195–9PubMedCrossRef
42.
Vingren JL, Kraemer WJ, Hatfield DL, et al. Effect of resistance exercise on muscle steroid receptor protein contentin strength-trained men and women. Steroids 2009 Nov-Dec; 74 (13-14): 1033–9PubMedCrossRef
43.
Hornberger TA, Esser KA. Mechanotransduction and the regulation of protein synthesis in skeletal muscle. Proc Nutr Soc 2004 May; 63 (2): 331–5PubMedCrossRef
44.
Spangenburg EE, Le Roith D, Ward CW, et al. A functional insulin-like growth factor receptor is not necessaryfor load-induced skeletal muscle hypertrophy. J Physiol 2008 Jan; 586 (1): 283–91PubMedCrossRef
45.
Dohi K, Mastro AM, Miles MP, et al. Lymphocyte proliferation in response to acute heavy resistance exercise inwomen: influence of muscle strength and total work. EurJ Appl Physiol 2001 Aug; 85 (3-4): 367–73CrossRef
46.
Kraemer WJ, Ratamess NA. Endocrine responses and adaptations to strength and power training. In: Komi PV, editor. Strength and power in sport. 2nd ed. Malden(MA): Blackwell Scientific Publications; 2003: 361–86CrossRef
47.
Kraemer WJ, Fleck SJ, Maresh CM, et al. Acute hormonal responses to a single bout of heavy resistance exercise intrained power lifters and untrained men. Can J Appl Physiol 1999 Dec; 24 (6): 524–37PubMedCrossRef
48.
Kraemer WJ, Noble BJ, Clark MJ, et al. Physiologic responses to heavy-resistance exercise with very short restperiods. Int J Sports Med 1987 Aug; 8 (4): 247–52PubMedCrossRef
49.
Bush JA, Kraemer WJ, Mastro AM, et al. Exercise and recovery responses of adrenal medullary neurohormonesto heavy resistance exercise. Med Sci Sports Exerc 1999 Apr; 31 (4): 554–9PubMedCrossRef
50.
Mikkelsen UR, Gissel H, Fredsted A, et al. Excitation-induced cell damage and beta2-adrenoceptor agonist stimulated forcerecovery in rat skeletal muscle. Am J Physiol Regul Integr Comp Physiol 2006 Feb; 290 (2): R265–72PubMedCrossRef
51.
French DN, Kraemer WJ, Volek JS, et al. Anticipatory responses of catecholamines on muscle force production. J Appl Physiol 2007 Jan; 102 (1): 94–102PubMedCrossRef
52.
Kraemer WJ, Patton JF, Knuttgen HG, et al. Effects of high-intensity cycle exercise on sympathoadrenal-medullaryresponse patterns. J Appl Physiol 1991 Jan; 70 (1): 8–14PubMed
53.
Tod D, Iredale F, Gill N. ‘Psyching-up’ and muscular force production. Sports Med 2003; 33 (1): 47–58PubMedCrossRef
54.
Mazzeo RS. Catecholamine responses to acute and chronic exercise. Med Sci Sports Exerc 1991 Jul; 23 (7): 839–45PubMed
55.
Richter EA, Sonne B, Christensen NJ, et al. Role of epinephrine for muscular glycogenolysis and pancreatichormonal secretion in running rats. Am J Physiol 1981 May; 240 (5): E526–32PubMed
56.
Dienstbier RA. Behavioral correlates of sympathoadrenal reactivity: the toughness model. Med Sci Sports Exerc 1991 Jul; 23 (7): 846–52PubMed
57.
Fry AC, Kraemer WJ, Stone MH, et al. Endocrine responses to overreaching before and after 1 year of weightlifting. CanJ Appl Physiol 1994 Dec; 19 (4): 400–10CrossRef
58.
Dardevet D, Sornet C, Savary I, et al. Glucocorticoid effects on insulin- and IGF-I-regulated muscle protein metabolismduring aging. J Endocrinol 1998 Jan; 156 (1): 83–9PubMedCrossRef
59.
Hickson RC, Czerwinski SM, Falduto MT, et al. Glucocorticoid antagonism by exercise and androgenic-anabolicsteroids. Med Sci Sports Exerc 1990 Jun; 22 (3): 331–40PubMed
60.
Auclair D, Garrel DR, Chaouki Zerouala A, et al. Activation of the ubiquitin pathway in rat skeletal muscle bycatabolic doses of glucocorticoids. Am J Physiol 1997 Mar; 272 (3Pt1): C1007–16
61.
Peeters GM, van Schoor NM, van Rossum EF, et al. The relationship between cortisol, muscle mass and musclestrength in older persons and the role of genetic variationsin the glucocorticoid receptor. Clin Endocrinol (Oxf) 2008 Oct; 69 (4): 673–82CrossRef
62.
Kraemer WJ, Fleck SJ, Dziados JE, et al. Changes in hormonal concentrations after different heavy-resistanceexercise protocols in women. J Appl Physiol 1993 Aug; 75 (2): 594–604PubMed
63.
Kraemer WJ, Fry AC, Warren BJ, et al. Acute hormonal responses in elite junior weightlifters. Int J Sports Med 1992 Feb; 13 (2): 103–9PubMedCrossRef
64.
Kraemer WJ, Hakkinen K, Newton RU, et al. Effects of heavyresistance training on hormonal response patterns in younger vs. older men. J Appl Physiol 1999 Sep; 87 (3): 982–92PubMed
65.
Kraemer WJ, Fleck SJ, Callister R, et al. Training responses of plasma beta-endorphin, adrenocorticotropin, and cortisol. Med Sci Sports Exerc 1989 Apr; 21 (2): 146–53PubMed
66.
Hakkinen K, Pakarinen A. Acute hormonal responses to two different fatiguing heavy-resistance protocols in maleathletes. J Appl Physiol 1993 Feb; 74 (2): 882–7PubMed
67.
Kraemer WJ, Dziados JE, Marchitelli LJ, et al. Effects of different heavy-resistance exercise protocols on plasmabeta-endorphin concentrations. J Appl Physiol 1993 Jan; 74 (1): 450–9PubMed
68.
Simpson ER, Mahendroo MS, Means GD, et al. Aromatase cytochrome P450, the enzyme responsible for estrogenbiosynthesis. Endocr Rev 1994 Jun; 15 (3): 342–55PubMed
69.
Kraemer RR, Heleniak RJ, Tryniecki JL, et al. Follicular and luteal phase hormonal responses to low-Vol. resistiveexercise. Med Sci Sports Exerc 1995 Jun; 27 (6): 809–17PubMed
70.
Walberg-Rankin J, Franke WD, Gwazdauskas FC. Response of beta-endorphin and estradiol to resistanceexercise in females during energy balance and energy restriction. Int J Sports Med 1992 Oct; 13 (7): 542–7PubMedCrossRef
71.
Amelink GJ, Kamp HH, Bar PR. Creatine kinase isoenzyme profiles after exercise in the rat: sex-linked differencesin leakage of CK-MM. Pflugers Arch 1988 Sep; 412 (4): 417–21PubMedCrossRef
72.
Amelink GJ, Koot RW, Erich WB, et al. Sex-linked variation in creatine kinase release, and its dependence onoestradiol, can be demonstrated in an in-vitro rat skeletalmuscle preparation. Acta Physiol Scand 1990 Feb; 138 (2): 115–24PubMedCrossRef
73.
Amelink GJ, van der Wal WA, Wokke JH, et al. Exerciseinduced muscle damage in the rat: the effect of vitamin Edeficiency. Pflugers Arch 1991 Oct; 419 (3-4): 304–9PubMedCrossRef
74.
Bar PR, Amelink GJ, Oldenburg B, et al. Prevention of exercise-induced muscle membrane damage by oestradiol. Life Sci 1988; 42 (26): 2677–81PubMedCrossRef
75.
Subbiah MT, Kessel B, Agrawal M, et al. Antioxidant potential of specific estrogens on lipid peroxidation. J Clin Endocrinol Metab 1993 Oct; 77 (4): 1095–7PubMedCrossRef
76.
Tiidus PM. Can estrogens diminish exercise induced muscle damage? Can J Appl Physiol 1995 Mar; 20 (1): 26–38PubMedCrossRef
77.
Kraemer WJ, Gordon SE, Fleck SJ, et al. Endogenous anabolic hormonal and growth factor responses to heavyresistance exercise in males and females. Int J Sports Med 1991 Apr; 12 (2): 228–35PubMedCrossRef
78.
Kraemer WJ, Marchitelli L, Gordon SE, et al. Hormonal and growth factor responses to heavy resistance exerciseprotocols. J Appl Physiol 1990 Oct; 69 (4): 1442–50PubMed
79.
Volek JS, Kraemer WJ, Bush JA, et al. Testosterone and cortisol in relationship to dietary nutrients and resistanceexercise. J Appl Physiol 1997 Jan; 82 (1): 49–54PubMedCrossRef
80.
Hakkinen K, Pakarinen A. Acute hormonal responses to heavy resistance exercise in men and women at differentages. Int J Sports Med 1995 Nov; 16 (8): 507–13PubMedCrossRef
81.
Hickson RC, Hidaka K, Foster C, et al. Successive time courses of strength development and steroid hormoneresponses to heavy-resistance training. J Appl Physiol 1994 Feb; 76 (2): 663–70PubMed
82.
Weiss LW, Cureton KJ, Thompson FN. Comparison of serum testosterone and androstenedione responses toweight lifting in men and women. Eur J Appl Physiol Occup Physiol 1983; 50 (3): 413–9PubMedCrossRef
83.
Jensen J, Oftebro H, Breigan B, et al. Comparison of changes in testosterone concentrations after strength andendurance exercise in well trained men. Eur J Appl Physiol Occup Physiol 1991; 63 (6): 467–71PubMedCrossRef
84.
Kraemer WJ, Staron RS, Hagerman FC, et al. The effects of short-term resistance training on endocrine function inmen and women. Eur J Appl Physiol Occup Physiol 1998 JUn; 78 (1): 69–76PubMedCrossRef
85.
Cumming DC, Wall SR, Galbraith MA, et al. Reproductive hormone responses to resistance exercise. Med Sci Sports Exerc 1987 Jun; 19 (3): 234–8PubMed
86.
Nindl BC, Kraemer WJ, Gotshalk LA, et al. Testosterone responses after resistance exercise in women: influence ofregional fat distribution. Int J Sport Nutr Exerc Metab 2001 Dec; 11 (4): 451–65PubMed
87.
Consitt LA, Copeland JL, Copeland JL. Hormone responses to resistance vs. endurance exercise in premenopausal females. Can J Appl Physiol 2001 Dec; 26 (6): 574–87PubMedCrossRef
88.
Enea C, Boisseau N, Ottavy M, et al. Effects of menstrual cycle, oral contraception, and training on exerciseinducedchanges in circulating DHEA-sulphate and testosteronein young women. Eur J Appl Physiol 2009 Jun; 106 (3): 365–73PubMedCrossRef
89.
Kent-Braun JA, Ng AV. Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol 1999 Jul; 87 (1): 22–9PubMed
90.
Fulco CS, Rock PB, Muza SR, et al. Slower fatigue and faster recovery of the adductor pollicis muscle in womenmatched for strength with men. Acta Physiol Scand 1999 Nov; 167 (3): 233–9PubMedCrossRef
91.
Hunter SK, Enoka RM. Changes in muscle activation can prolong the endurance time of a submaximal isometriccontraction in humans. J Appl Physiol 2003 Jan; 94 (1): 108–18PubMed
92.
Kent-Braun JA, Ng AV, Doyle JW, et al. Human skeletal muscle responses vary with age and gender during fatiguedue to incremental isometric exercise. J Appl Physiol 2002 Nov; 93 (5): 1813–23PubMed
93.
Russ DW, Kent-Braun JA. Sex differences in human skeletal muscle fatigue are eliminated under ischemic conditions. J Appl Physiol 2003 Jun; 94 (6): 2414–22PubMed
94.
Carter S, McKenzie S, Mourtzakis M, et al. Short-term 17beta-estradiol decreases glucose R(a) but not wholebody metabolism during endurance exercise. J Appl Physiol 2001 Jan; 90 (1): 139–46PubMed
95.
Komulainen J, Koskinen SO, Kalliokoski R, et al. Gender differences in skeletal muscle fibre damage after eccentricallybiased downhill running in rats. Acta Physiol Scand 1999 Jan; 165 (1): 57–63PubMedCrossRef
96.
Tarnopolsky M, editor. Gender differences in metabolism: practical and nutritional implications. Boca Raton (FL): CRC Press; 1999
97.
Mair J, Koller A, Artner-Dworzak E, et al. Effects of exercise on plasma myosin heavy chain fragments and MRI of skeletal muscle. J Appl Physiol 1992 Feb; 72 (2): 656–63PubMed
98.
Nosaka K, Clarkson PM, Apple FS. Time course of serum protein changes after strenuous exercise of the forearmflexors. J Lab Clin Med 1992 Feb; 119 (2): 183–8PubMed
99.
Harris EK, Wong ET, Shaw Jr ST. Statistical criteria for separate reference intervals: race and gender groups increatine kinase. Clin Chem 1991 Sep; 37 (9): 1580–2PubMed
100.
Norton JP, Clarkson PM, Graves JE, et al. Serum creatine kinase activity and body composition in males and females. Hum Biol 1985 Dec; 57 (4): 591–8PubMed
101.
Apple FS, Rogers MA, Casal DC, et al. Skeletal muscle creatine kinase MB alterations in women marathon runners. Eur J Appl Physiol Occup Physiol 1987; 56 (1): 49–52PubMedCrossRef
102.
Shumate JB, Brooke MH, Carroll JE, et al. Increased serum creatine kinase after exercise: a sex-linked phenomenon. Neurology 1979 Jun; 29 (6): 902–4PubMedCrossRef
103.
Nuttall FQ, Jones B. Creatine kinase and glutamic oxalacetic transaminase activity in serum: kinetics of changewith exercise and effect of physical conditioning. J Lab Clin Med 1968 May; 71 (5): 847–54PubMed
104.
Herbert TB, Cohen S. Stress and immunity in humans: a meta-analytic review. Psychosom Med 1993 Jul-Aug; 55 (4): 364–79PubMed
105.
Kiecolt-Glaser JK, Cacioppo JT, Malarkey WB, et al. Acute psychological stressors and short-term immunechanges: what, why, for whom, and to what extent? Psychosom Med 1992 Nov-Dec; 54 (6): 680–5PubMed
106.
Blalock JE. The immune system as a sensory organ. J Immunol 1984 Mar; 132 (3): 1067–70PubMed
107.
Shek PN, Sabiston BH, Buguet A, et al. Strenuous exercise and immunological changes: a multiple-time-point analysisof leukocyte subsets, CD4/CD8 ratio, immunoglobulinproduction and NK cell response. Int J Sports Med 1995 Oct; 16 (7): 466–74PubMedCrossRef
108.
Simpson RJ, Florida-James GD, Whyte GP, et al. The effects of intensive, moderate and downhill treadmillrunning on human blood lymphocytes expressing theadhesion/activation molecules CD54 (ICAM-1), CD18(beta2 integrin) and CD53. Eur J Appl Physiol 2006 May; 97 (1): 109–21PubMedCrossRef
109.
Gannon GA, Rhind SG, Shek PN, et al. Differential cell adhesion molecule expression and lymphocyte mobilisationduring prolonged aerobic exercise. Eur J Appl Physiol 2001 Apr; 84 (4): 272–82PubMedCrossRef
110.
Simpson RJ, Cosgrove C, Ingram LA, et al. Senescent T-lymphocytes are mobilised into the peripheral bloodcompartment in young and older humans after exhaustiveexercise. Brain Behav Immun 2008 May; 22 (4): 544–51PubMedCrossRef
111.
112.
Kraemer WJ, Clemson A, Triplett NT, et al. The effects of plasma cortisol elevation on total and differential leukocytecounts in response to heavy-resistance exercise. EurJ Appl Physiol Occup Physiol 1996; 73 (1-2): 93–7CrossRef
113.
Miles MP, Leach SK, Kraemer WJ, et al. Leukocyte adhesion molecule expression during intense resistance exercise. J Appl Physiol 1998 May; 84 (5): 1604–9PubMed
114.
Calle MC, Fernandez ML. Effects of resistance training on the inflammatory response. Nutr Res Pract 2010 Aug; 4 (4): 259–69PubMedCrossRef
115.
Mathur N, Pedersen BK. Exercise as a mean to control low-grade systemic inflammation. Mediators Inflamm. Epub 2009 Jan 11
116.
Mastro AM, Schlosser DA, Grove DS, et al. Lymphocyte subpopulations in lymphoid organs of rats after acuteresistance exercise. Med Sci Sports Exerc 1999 Jan; 31 (1): 74–81PubMedCrossRef
117.
Purtilo DT, Sullivan JL. Immunological bases for superior survival of females. Am J Dis Child 1979 Dec; 133 (12): 1251–3PubMed
118.
Verthelyi D. Sex hormones as immunomodulators in health and disease. Int Immunopharmacol 2001 Jun; 1 (6): 983–93PubMedCrossRef
119.
Cannon JG, St Pierre BA. Gender differences in host defense mechanisms. J Psychiatr Res 1997 Jan-Feb; 31 (1): 99–113PubMedCrossRef
120.
Diodato MD, Knoferl MW, Schwacha MG, et al. Gender differences in the inflammatory response and survivalfollowing haemorrhage and subsequent sepsis. Cytokine 2001 May; 14 (3): 162–9PubMedCrossRef
121.
122.
Yancey AL, Watson HL, Cartner SC, et al. Gender is a major factor in determining the severity of mycoplasmarespiratory disease in mice. Infect Immun 2001 May; 69 (5): 2865–71PubMedCrossRef
123.
124.
Aljubeh J, Miller A, Meyer 3rd W, et al. Glucocorticoid receptor characteristics in healthy childrens’ leukocytes:correlation with gender, weight, age and plasma cortisol. J Pediatr Endocrinol Metab 2001 Nov-Dec; 14 (9): 1641–7PubMedCrossRef
125.
Giron-Gonzalez JA, Moral FJ, Elvira J, et al. Consistent production of a higher TH1:TH2 cytokine ratio by stimulatedT cells in men compared with women. Eur J Endocrinol 2000 Jul; 143 (1): 31–6PubMedCrossRef
126.
Posma E, Moes H, Heineman MJ, et al. The effect of testosterone on cytokine production in the specific and nonspecificimmune response. Am J Reprod Immunol 2004 Oct; 52 (4): 237–43PubMedCrossRef
127.
Blondeau JM, Embil JA, McFarlane ES. Herpes simplex virus infections in male and female mice following pinnainoculation: responses to primary infection and artificiallyinduced recurrent disease. J Med Virol 1989 Dec; 29 (4): 320–6PubMedCrossRef
128.
Travi BL, Osorio Y, Melby PC, et al. Gender is a major determinant of the clinical evolution and immune responsein hamsters infected with Leishmania spp. Infect Immun 2002 May; 70 (5): 2288–96PubMedCrossRef
129.
Choudhry MA, Bland KI, Chaudry IH. Trauma and immune response: effect of gender differences. Injury 2007 Dec; 38 (12): 1382–91PubMedCrossRef
130.
Gabrilovac J, Marotti T. Gender-related differences in murine T- and B-lymphocyte proliferative ability in responseto in vivo [Met(5)]enkephalin administration. EurJ Pharmacol 2000 Mar 24; 392 (1-2): 101–8CrossRef
131.
De Lanne R, Barnes JR, Brouha L. Hematological changes during muscular activity and recovery. J Appl Physiol 1960 Jan; 15: 31–6
132.
Timmons BW, Hamadeh MJ, Devries MC, et al. Influence of gender, menstrual phase, and oral contraceptive use onimmunological changes in response to prolonged cycling. J Appl Physiol 2005 Sep; 99 (3): 979–85PubMedCrossRef
133.
Bouillon LE, Flynn MG, Lambert CP, et al. Exercise during late-follicular menstrual phase: influence on immuneparameters. J Sports Med Phys Fitness 2006 Mar; 46 (1): 143–51PubMed
134.
de la Fuente M, Martin MI, Ortega E. Changes in the phagocytic function of peritoneal macrophages from oldmice after strenuous physical exercise. Comp Immunol Microbiol Infect Dis 1990; 13 (4): 189–98PubMedCrossRef
135.
Brown AS, Davis JM, Murphy EA, et al. Gender differences in viral infection after repeated exercise stress. Med Sci Sports Exerc 2004 Aug; 36 (8): 1290–5PubMedCrossRef
136.
Navalta JW, Sedlock DA, Park KS, et al. Neither gender nor menstrual cycle phase influences exercise-inducedlymphocyte apoptosis in untrained subjects. Appl Physiol Nutr Metab 2007 Jun; 32 (3): 481–6PubMedCrossRef
137.
Miles MP, Kraemer WJ, Grove DS, et al. Effects of resistance training on resting immune parameters in women. Eur J Appl Physiol 2002 Oct; 87 (6): 506–8PubMedCrossRef
138.
Webster Marketon JI, Glaser R. Stress hormones and immune function. Cell Immunol 2008 Mar-Apr; 252 (1-2): 16–26PubMedCrossRef
139.
Brenner I, Shek PN, Zamecnik J, et al. Stress hormones and the immunological responses to heat and exercise. IntJ Sports Med 1998 Feb; 19 (2): 130–43CrossRef
140.
Pyne DB. Exercise-induced muscle damage and inflammation: a review. Aust J Sci Med Sport 1994 Sep-Dec; 26 (3-4): 49–58PubMed
141.
142.
Nieman DC. Exercise, upper respiratory tract infection, and the immune system. Med Sci Sports Exerc 1994 Feb; 26 (2): 128–39PubMedCrossRef
143.
Cupps TR, Fauci AS. Corticosteroid-mediated immunoregulation in man. Immunol Rev 1982; 65: 133–55PubMedCrossRef
144.
Nieman DC. Immune response to heavy exertion. J Appl Physiol 1997 May; 82 (5): 1385–94PubMed
145.
Tanaka H, Akama H, Ichikawa Y, et al. Glucocorticoid receptors in normal leukocytes: effects of age, gender,season, and plasma cortisol concentrations. Clin Chem 1991 Oct; 37 (10 Pt 1): 1715–9PubMed
146.
Maki T. Density and functioning of human lymphocytic beta-adrenergic receptors during prolonged physical exercise. Acta Physiol Scand 1989 Aug; 136 (4): 569–74PubMedCrossRef
147.
Blalock JE. Shared ligands and receptors as a molecular mechanism for communication between the immune andneuroendocrine systems. Ann N Y Acad Sci 1994 Nov 25; 741: 292–8PubMedCrossRef
148.
Garza Jr HH, Carr DJ. Neuroendocrine peptide receptors on cells of the immune system. Chem Immunol 1997; 69: 132–54PubMedCrossRef
149.
Weigent DA, Carr DJ, Blalock JE. Bidirectional communication between the neuroendocrine and immune systems:common hormones and hormone receptors. AnnN Y Acad Sci 1990; 579: 17–27CrossRef
150.
Dohi K, Kraemer WJ, Mastro AM. Exercise increases prolactin-receptor expression on human lymphocytes. J Appl Physiol 2003 Feb; 94 (2): 518–24PubMed
151.
Yamamoto KR. Steroid receptor regulated transcription of specific genes and gene networks. Annu Rev Genet 1985; 19: 209–52PubMedCrossRef
152.
Gustafsson JA, Carlstedt-Duke J, Poellinger L, et al. Biochemistry, molecular biology, and physiology of the glucocorticoid receptor. Endocr Rev 1987 May; 8 (2): 185–234PubMedCrossRef
153.
154.
Yehuda R, Boisoneau D, Lowy MT, et al. Dose-response changes in plasma cortisol and lymphocyte glucocorticoidreceptors following dexamethasone administration incombat veterans with and without posttraumatic stressdisorder. Arch Gen Psychiatry 1995 Jul; 52 (7): 583–93PubMedCrossRef
155.
Sanchez ER, Faber LE, Henzel WJ, et al. The 56-59-kilodalton protein identified in untransformed steroid receptorcomplexes is a unique protein that exists in cytosolin a complex with both the 70- and 90-kilodalton heat shockproteins. Biochemistry 1990 May; 29 (21): 5145–52PubMedCrossRef
156.
de Waal RM. The anti-inflammatory activity of glucocorticoids. Mol Biol Rep 1994 Mar; 19 (2): 81–8PubMedCrossRef
157.
Funder JW. Mineralocorticoid receptors and glucocorticoid receptors. Clin Endocrinol (Oxf) 1996 Dec; 45 (6): 651–6CrossRef
158.
Soontjens CD, Rafter JJ, Gustafsson JA. Ligands for orphan receptors? J Endocrinol 1996 Sep; 150 Suppl.: S241–57
159.
Besedovsky HO, Del Rey A, Sorkin E. Antigenic competition between horse and sheep red blood cells as a hormone-dependent phenomenon. Clin Exp Immunol 1979 Jul; 37 (1): 106–13PubMed
160.
del Rey A, Besedovsky H, Sorkin E. Endogenous blood levels of corticosterone control the immunologic cell massand B cell activity in mice. J Immunol 1984 Aug; 133 (2): 572–5PubMed
161.
Hench PS, Kendall EC, Slocumb CH, et al. The effect of a hormone of the adrenal cortex (17-hydroxycorticosterone:compound E) and of pituitary adrenocorticotropic hormoneon rheumatoid arthritis. Mayo Clinic Proc 1949; 24: 181–97
162.
Newton R. Molecular mechanisms of glucocorticoid action: what is important? Thorax 2000 Jul; 55 (7): 603–13PubMedCrossRef
163.
Wiegers GJ, Knoflach M, Bock G, et al. CD4(+)CD8(+)- TCR(low) thymocytes express low levels of glucocorticoidreceptors while being sensitive to glucocorticoid-inducedapoptosis. Eur J Immunol 2001 Aug; 31 (8): 2293–301PubMedCrossRef
164.
Fragala MS, Kraemer WJ, Mastro AM, et al. Glucocorticoid receptor expression on human b-cells in response toacute heavy resistance exercise. Neuroimmunomodulation 2011; 18 (3): 156–64PubMedCrossRef
165.
Collins S. Recent perspectives on the molecular structure and regulation of the beta 2-adrenoceptor. Life Sci 1993; 52 (26): 2083–91PubMedCrossRef
166.
Collins S, Caron MG, Lefkowitz RJ. From ligand binding to gene expression: new insights into the regulation ofG-protein-coupled receptors. Trends Biochem Sci 1992 Jan; 17 (1): 37–9PubMedCrossRef
167.
Collins S, Caron MG, Lefkowitz RJ. Regulation of adrenergic receptor responsiveness through modulation of receptorgene expression. Annu Rev Physiol 1991; 53: 497–508PubMedCrossRef
168.
Dohlman HG, Thorner J, Thorner J, et al. Model systems for the study of seven-transmembrane-segment receptors. Annu Rev Biochem 1991; 60: 653–88PubMedCrossRef
169.
Haen E, Hauck R, Emslander HP, et al. Nocturnal asthma. Beta 2-adrenoceptors on peripheral mononuclear leukocytes,cAMP- and cortisol-plasma concentrations. Chest 1991 Nov; 100 (5): 1239–45PubMedCrossRef
170.
Inglese J, Luttrell LM, Iniguez-Lluhi JA, et al. Functionally active targeting domain of the beta-adrenergic receptorkinase: an inhibitor of G beta gamma-mediatedstimulation of type II adenylyl cyclase. Proc Natl Acad SciU S A 1994 Apr 26; 91 (9): 3637–41CrossRef
171.
Pei G, Tiberi M, Caron MG, et al. An approach to the study of G-protein-coupled receptor kinases: an in vitropurifiedmembrane assay reveals differential receptorspecificity and regulation by G beta gamma subunits. Proc Natl Acad Sci U S A 1994 Apr 26; 91 (9): 3633–6PubMedCrossRef
172.
Clausen T, Flatman JA. Beta 2-adrenoceptors mediate the stimulating effect of adrenaline on active electrogenic Na-K-transport in rat soleus muscle. Br J Pharmacol 1980 Apr; 68 (4): 749–55PubMedCrossRef
173.
Holmberg E, Waldeck B. On the possible role of potassium ions in the action of terbutaline on skeletal muscle contractions. Acta Pharmacol Toxicol (Copenh) 1980 Feb; 46 (2): 141–9CrossRef
174.
Elenkov IJ, Wilder RL, Chrousos GP, et al. The sympathetic nerve. An integrative interface between two supersystems:the brain and the immune system. Pharmacol Rev 2000 Dec; 52 (4): 595–638PubMed
175.
Van Tits LJ, Michel MC, Grosse-Wilde H, et al. Catecholamines increase lymphocyte beta 2-adrenergic receptorsvia a beta 2-adrenergic, spleen-dependent process. Am JPhysiol 1990 Jan; 258 (1Pt1): E191–202
176.
Boxer LA, Allen JM, Baehner RL. Diminished polymorphonuclear leukocyte adherence: function dependent onrelease of cyclic AMP by endothelial cells after stimulationof beta-receptors by epinephrine. J Clin Invest 1980 Aug; 66 (2): 268–74PubMedCrossRef
177.
Schedlowski M, Falk A, Rohne A, et al. Catecholamines induce alterations of distribution and activity of humannatural killer (NK) cells. J Clin Immunol 1993 Sep; 13 (5): 344–51PubMedCrossRef
178.
Fragala MS, Kraemer WJ, Mastro AM, et al. Leukocyte b2-adrenergic receptor expression in response to resistanceexercise. Med Sci Sports Exerc. In press
179.
Bunt JC, Boileau RA, Bahr JM, et al. Sex and training differences in human growth hormone levels during prolongedexercise. J Appl Physiol 1986 Nov; 61 (5): 1796–801PubMed
180.
Eskes T, Haanen C. Why do women live longer than men? Eur J Obstet Gynecol Reprod Biol 2007 Aug; 133 (2): 126–33PubMedCrossRef
181.
182.
Carlsten H, Holmdahl R, Tarkowski A, et al. Oestradioland testosterone-mediated effects on the immune systemin normal and autoimmune mice are genetically linkedand inherited as dominant traits. Immunology 1989 Oct; 68 (2): 209–14PubMed
183.
Carlsten H, Holmdahl R, Tarkowski A, et al. Oestradiol suppression of delayed-type hypersensitivity in autoimmune(NZB/NZW)F1 mice is a trait inherited from thehealthy NZW parental strain. Immunology 1989 Jun; 67 (2): 205–9PubMed
184.
Josefsson E, Tarkowski A, Carlsten H. Anti-inflammatory properties of estrogen. I: in vivo suppression of leukocyte production in bone marrow and redistribution of peripheral blood neutrophils. Cell Immunol 1992 Jun; 142 (1): 67–78PubMedCrossRef
185.
Hanna N, Schneider M. Enhancement of tumor metastasis and suppression of natural killer cell activity by betaestradioltreatment. J Immunol 1983 Feb; 130 (2): 974–80PubMed
186.
Nilsson N, Carlsten H. Estrogen induces suppression of natural killer cell cytotoxicity and augmentation of polyclonalB cell activation. Cell Immunol 1994 Oct 1; 158 (1): 131–9PubMedCrossRef
187.
Masuzawa T, Miyaura C, Onoe Y, et al. Estrogen deficiency stimulates B lymphopoiesis in mouse bone marrow. J Clin Invest 1994 Sep; 94 (3): 1090–7PubMedCrossRef
188.
Smithson G, Beamer WG, Shultz KL, et al. Increased B lymphopoiesis in genetically sex steroid-deficient hypogonadal(hpg) mice. J Exp Med 1994 Aug 1; 180 (2): 717–20PubMedCrossRef
189.
Wilson CA, Mrose SA, Thomas DW. Enhanced production of B lymphocytes after castration. Blood 1995 Mar 15; 85 (6): 1535–9PubMed
190.
Medina KL, Kincade PW. Pregnancy-related steroids are potential negative regulators of B lymphopoiesis. Proc Natl Acad Sci U S A 1994 Jun 7; 91 (12): 5382–6PubMedCrossRef
191.
Rijhsinghani AG, Thompson K, Bhatia SK, et al. Estrogen blocks early T cell development in the thymus. Am J Reprod Immunol 1996 Nov; 36 (5): 269–77PubMedCrossRef
192.
Medina KL, Smithson G, Kincade PW. Suppression of B lymphopoiesis during normal pregnancy. J Exp Med 1993 Nov; 178 (5): 1507–15PubMedCrossRef
193.
Mills PJ, Ziegler MG, Dimsdale JE, et al. Enumerative immune changes following acute stress: effect of the menstrualcycle. Brain Behav Immun 1995 Sep; 9 (3): 190–5PubMedCrossRef
194.
Grimaldi CM, Hill L, Xu X, et al. Hormonal modulation of B cell development and repertoire selection. Mol Immunol 2005 May; 42 (7): 811–20PubMedCrossRef
195.
McMurray RW, Ndebele K, Hardy KJ, et al. 17-betaestradiol suppresses IL-2 and IL-2 receptor. Cytokine 2001 Jun; 14 (6): 324–33PubMedCrossRef
196.
Smithson G, Couse JF, Lubahn DB, et al. The role of estrogen receptors and androgen receptors in sex steroid regulation ofB lymphopoiesis. J Immunol 1998 Jul 1; 161 (1): 27–34PubMed
197.
Hewitt SC, Harrell JC, Korach KS. Lessons in estrogen biology from knockout and transgenic animals. Annu Rev Physiol 2005; 67: 285–308PubMedCrossRef
198.
Matthews J, Gustafsson JA. Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol Interv 2003 Aug; 3 (5): 281–92PubMedCrossRef
199.
Phiel KL, Henderson RA, Adelman SJ, et al. Differential estrogen receptor gene expression in human peripheralblood mononuclear cell populations. Immunol Lett 2005 Feb 15; 97 (1): 107–13PubMedCrossRef
200.
Bakir S, Mori T, Durand J, et al. Estrogen-induced vasoprotection is estrogen receptor dependent: evidence fromthe balloon-injured rat carotid artery model. Circulation 2000 May; 101 (20): 2342–4PubMedCrossRef
201.
Miller AP, Feng W, Xing D, et al. Estrogen modulates inflammatory mediator expression and neutrophil chemotaxisin injured arteries. Circulation 2004 Sep 21; 110 (12): 1664–9PubMedCrossRef
202.
Xing D, Miller A, Novak L, et al. Estradiol and progestins differentially modulate leukocyte infiltration after vascularinjury. Circulation 2004 Jan 20; 109 (2): 234–41PubMedCrossRef
203.
Luster AD. Chemokines: chemotactic cytokines that mediate inflammation. N Engl J Med 1998 Feb 12; 338 (7): 436–45PubMedCrossRef
204.
Meyers MJ, Sun J, Sun J, et al. Estrogen receptor-beta potency-selective ligands: structure-activity relationshipstudies of diarylpropionitriles and their acetylene and polaranalogues. J Med Chem 2001 Nov 22; 44 (24): 4230–51PubMedCrossRef
205.
Xing D, Feng W, Miller AP, et al. Estrogen modulates TNF-alpha-induced inflammatory responses in rat aorticsmooth muscle cells through estrogen receptor-beta activation. Am J Physiol Heart Circ Physiol 2007 Jun; 292 (6): H2607–12PubMedCrossRef
206.
Lew KH, Ludwig EA, Milad MA, et al. Gender-based effects on methylprednisolone pharmacokinetics andpharmacodynamics. Clin Pharmacol Ther 1993 Oct; 54 (4): 402–14PubMedCrossRef
207.
Nelson DH, Tanney H, Mestman G, et al. Potentiation of the biologic effect of administered cortisol by estrogentreatment. J Clin Endocrinol Metab 1963 Mar; 23: 261–5PubMedCrossRef
208.
Bulbrook RD, Herian M, Tong D, et al. Effect of steroidal contraceptives on levels of plasma androgen sulphatesand cortisol. Lancet 1973 Mar 24; 1 (7804): 628–31PubMedCrossRef
209.
Plager JE, Schmidt KG, Staubitz WJ. Increased unbound cortisol in the plasma of estrogen-treated subjects. J Clin Invest 1964 Jun; 43: 1066–72PubMedCrossRef
210.
Janele D, Lang T, Capellino S, et al. Effects of testosterone, 17beta-estradiol, and downstream estrogens on cytokinesecretion from human leukocytes in the presence andabsence of cortisol. Ann N Y Acad Sci 2006 Jun; 1069: 168–82PubMedCrossRef
211.
Fujimoto R, Morimoto I, Morita E, et al. Androgen receptors, 5 alpha-reductase activity and androgen-dependentproliferation of vascular smooth muscle cells. J Steroid Biochem Mol Biol 1994 Aug; 50 (3-4): 169–74PubMedCrossRef
212.
Benten WP, Lieberherr M, Giese G, et al. Functional testosterone receptors in plasmamembranes of T cells. FasebJ 1999 Jan; 13 (1): 123–33
213.
Benten WP, Lieberherr M, Stamm O, et al. Testosterone signaling through internalizable surface receptors in androgenreceptor-free macrophages. Mol Biol Cell 1999 Oct; 10 (10): 3113–23PubMed
214.
Mealy K, Robinson B, Millette CF, et al. The testicular effects of tumor necrosis factor. Ann Surg 1990 Apr; 211 (4): 470–5PubMedCrossRef
215.
Mosmann TR, Sad S. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 1996 Mar; 17 (3): 138–46PubMedCrossRef
216.
Butts CL, Jones YL, Lim JK, et al. Tissue expression of steroid hormone receptors is associated with differentialimmune responsiveness. Brain Behav Immun 2011 Jul; 25 (5): 1000–7PubMedCrossRef
217.
MacLean HE, Chiu WS, Notini AJ, et al. Impaired skeletal muscle development and function in male, but not female,genomic androgen receptor knockout mice. Faseb J 2008 Aug; 22 (8): 2676–89PubMedCrossRef
218.
Ophoff J, Van Proeyen K, Callewaert F, et al. Androgen signaling in myocytes contributes to the maintenance ofmuscle mass and fiber type regulation but not to musclestrength or fatigue. Endocrinology 2009 Aug; 150 (8): 3558–66PubMedCrossRef
Metadata
Title
Neuroendocrine-Immune Interactions and Responses to Exercise
Authors
Maren S. Fragala
William J. Kraemer, PhD
Craig R. Denegar
Carl M. Maresh
Andrea M. Mastro
Jeff S. Volek
Publication date
01-08-2011
Publisher
Springer International Publishing
Published in
Sports Medicine / Issue 8/2011
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.2165/11590430-000000000-00000