Energy regulation and neuroendocrine-immune control in chronic inflammatory diseases

Journal of Internal Medicine

Volumn 267, Issue 6, 2010, Pages 543-560

  Straub, R H ^a   Cutolo, M ^b   Buttgereit, F ^c   Pongratz, G ^a  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^b UNIVERSITY OF GENOA   (Italy)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Bioenergetics; Chronic inflammatory diseases; Disease sequelae

Indexed keywords

ANDROGEN; ESTROGEN; GLUCAGON; GROWTH HORMONE; HYDROCORTISONE; INSULIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPID; OSTEOCALCIN; SOMATOMEDIN C; THYROID HORMONE; TUMOR NECROSIS FACTOR;

ADRENERGIC SYSTEM; ANEMIA; ANOREXIA; CACHEXIA; CELL ACTIVATION; CHOLINERGIC SYSTEM; CHRONIC INFLAMMATION; CIRCADIAN RHYTHM; DYSLIPIDEMIA; ENERGY BALANCE; ENERGY CONSUMPTION; HUMAN; HYPERCORTISOLISM; HYPERINSULINEMIA; HYPERTENSION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; ILLNESS BEHAVIOR; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; INSULIN RESISTANCE; LIPID STORAGE; METABOLIC SYNDROME X; NEUROENDOCRINOLOGY; OBESITY; OSTEOPENIA; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SENSORY NERVE; VITAMIN D DEFICIENCY;

ADIPOSE TISSUE; ANEMIA; ANOREXIA; BONE DISEASES, METABOLIC; CACHEXIA; CHRONIC DISEASE; CIRCADIAN RHYTHM; DYSLIPIDEMIAS; ENERGY METABOLISM; HUMANS; INFLAMMATION; INSULIN RESISTANCE; NEUROSECRETORY SYSTEMS; OBESITY;

EID: 77951935429     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/j.1365-2796.2010.02218.x     Document Type: Review

References (142)

1. Wilder RL. Neuroimmunoendocrinology of the rheumatic diseases: past, present, and future. Ann N Y Acad Sci 2002 966 : 13 9.
2. Masi AT, Aldag JC, Jacobs JW. Rheumatoid arthritis: neuroendocrine immune integrated physiopathogenetic perspectives and therapy. Rheum Dis Clin North Am 2005 31 : 131 160. (Pubitemid 40082059)
3. Cutolo M, Straub RH, Bijlsma JW. Neuroendocrine-immune interactions in synovitis. Nat Clin Pract Rheumatol 2007 3 : 627 634.
4. Holmdahl R, Carlsten H, Jansson L, Larsson P. Oestrogen is a potent immunomodulator of murine experimental rheumatoid disease. Br J Rheumatol 1989 28 (Suppl. 1 54 8. (Pubitemid 19285696)
5. Straub RH. The complex role of estrogens in inflammation. Endocr Rev 2007 28 : 521 574.
6. Levine JD, Collier DH, Basbaum AI, Moskowitz MA, Helms CA. Hypothesis: the nervous system may contribute to the pathophysiology of rheumatoid arthritis. J Rheumatol 1985 12 : 406 411.
7. Schaffler A, Muller-Ladner U, Scholmerich J, Buchler C. Role of adipose tissue as an inflammatory organ in human diseases. Endocr Rev 2006 27 : 449 467. (Pubitemid 44213227)
8. Straub RH, Besedovsky HO. Integrated evolutionary, immunological, and neuroendocrine framework for the pathogenesis of chronic disabling inflammatory diseases. FASEB J 2003 17 : 2176 2183.
9. Straub RH, Del Rey A, Besedovsky HO. Emerging concepts for the pathogenesis of chronic disabling inflammatory diseases: neuroendocrine-immune interactions and evolutionary biology. In : Ader R, ed. Psychoneuroimmunology.
10. Rassow J, Hauser K, Netzker R, Deutzmann R. Biochemistry.
11. Rolfe DF, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 1997 77 : 731 758.
12. Blaxter K. Energy Metabolism in Animals and Man.
13. Lippert H. Lehrbuch Anatomie.
14. Princiotta MF, Finzi D, Qian SB et al. Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 2003 18 : 343 354. (Pubitemid 36351514)
15. Buttgereit F, Brand MD. A hierarchy of ATP-consuming processes in mammalian cells. Biochem J 1995 312 : 163 167.
16. Schmid D, Burmester GR, Tripmacher R, Kuhnke A, Buttgereit F. Bioenergetics of human peripheral blood mononuclear cell metabolism in quiescent, activated, and glucocorticoid-treated states. Biosci Rep 2000 20 : 289 302.
17. Kuhnke A, Burmester GR, Krauss S, Buttgereit F. Bioenergetics of immune cells to assess rheumatic disease activity and efficacy of glucocorticoid treatment. Ann Rheum Dis 2003 62 : 133 139. (Pubitemid 36135388)
18. Calder PC. Fuel utilization by cells of the immune system. Proc Nutr Soc 1995 54 : 65 82.
19. Maciver NJ, Jacobs SR, Wieman HL, Wofford JA, Coloff JL, Rathmell JC. Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival. J Leukoc Biol 2008 84 : 949 957.
20. Iemitsu M, Itoh M, Fujimoto T et al. Whole-body energy mapping under physical exercise using positron emission tomography. Med Sci Sports Exerc 2000 32 : 2067 2070.
21. Schedlowski M, Hosch W, Oberbeck R et al. Catecholamines modulate human NK cell circulation and function via spleen-independent beta 2-adrenergic mechanisms. J Immunol 1996 156 : 93 9. (Pubitemid 26006952)
22. Dhabhar FS, McEwen BS. Bidirectional effects of stress and glucocorticoid hormones on immune function: possible explanations for paradoxical observations. In : Ader R, Felten DL, Cohen N, eds. Psychoneuroimmunology.
23. Born J, Lange T, Hansen K, Molle M, Fehm HL. Effects of sleep and circadian rhythm on human circulating immune cells. J Immunol 1997 158 : 4454 4464. (Pubitemid 127483950)
24. Lange T, Dimitrov S, Fehm HL, Westermann J, Born J. Shift of monocyte function toward cellular immunity during sleep. Arch Intern Med 2006 166 : 1695 1700. (Pubitemid 44414455)
25. Merl V, Peters A, Oltmanns KM et al. Preserved circadian rhythm of serum insulin concentration at low plasma glucose during fasting in lean and overweight humans. Metabolism 2004 53 : 1449 1453. (Pubitemid 39410385)
26. Wildenhoff KE, Johansen JP, Karstoft H, Yde H, Sorensen NS. Diurnal variations in the concentrations of blood acetoacetate and 3-hydroxybutyrate. The ketone body peak around midnight and its relationship to free fatty acids, glycerol, insulin, growth hormone and glucose in serum and plasma. Acta Med Scand 1974 195 : 25 8.
27. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008 9 : 46 56. (Pubitemid 350295688)
28. Hart BL. Biological basis of the behavior of sick animals. Neurosci Biobehav Rev 1988 12 : 123 137.
29. Preston BT, Capellini I, McNamara P, Barton RA, Nunn CL. Parasite resistance and the adaptive significance of sleep. BMC Evol Biol 2009 doi:.
30. Buttgereit F, Burmester GR, Brand MD. Bioenergetics of immune functions: fundamental and therapeutic aspects. Immunol Today 2000 21 : 192 199. (Pubitemid 30184792)
31. Higami Y, Barger JL, Page GP et al. Energy restriction lowers the expression of genes linked to inflammation, the cytoskeleton, the extracellular matrix, and angiogenesis in mouse adipose tissue. J Nutr 2006 136 : 343 352. (Pubitemid 43228285)
32. Okano K, Tsukazaki T, Ohtsuru A et al. Parathyroid hormone-related peptide in synovial fluid and disease activity of rheumatoid arthritis. Br J Rheumatol 1996 35 : 1056 1062. (Pubitemid 126719638)
33. Feske S. Calcium signalling in lymphocyte activation and disease. Nat Rev Immunol 2007 7 : 690 702. (Pubitemid 47327393)
34. Del Rey A, Roggero E, Randolf A et al. IL-1 resets glucose homeostasis at central levels. Proc Natl Acad Sci U S A 2006 103 : 16039 16044. (Pubitemid 44657588)
35. Takeda S, Elefteriou F, Levasseur R et al. Leptin regulates bone formation via the sympathetic nervous system. Cell 2002 111 : 305 317. (Pubitemid 35345151)
36. Rennie KL, Hughes J, Lang R, Jebb SA. Nutritional management of rheumatoid arthritis: a review of the evidence. J Hum Nutr Diet 2003 16 : 97 109. (Pubitemid 36527084)
37. van de Laar MA, Nieuwenhuis JM, Former-Boon M, Hulsing J, van der Korst JK. Nutritional habits of patients suffering from seropositive rheumatoid arthritis: a screening of 93 Dutch patients. Clin Rheumatol 1990 9 : 483 488.
38. Hansen GV, Nielsen L, Kluger E et al. Nutritional status of Danish rheumatoid arthritis patients and effects of a diet adjusted in energy intake, fish-meal, and antioxidants. Scand J Rheumatol 1996 25 : 325 330. (Pubitemid 26363309)
39. Lundberg AC, Akesson A, Akesson B. Dietary intake and nutritional status in patients with systemic sclerosis. Ann Rheum Dis 1992 51 : 1143 1148.
40. Payne A. Nutrition and diet in the clinical management of multiple sclerosis. J Hum Nutr Diet 2001 14 : 349 357. (Pubitemid 33014888)
41. Bacon MC, White PH, Raiten DJ et al. Nutritional status and growth in juvenile rheumatoid arthritis. Semin Arthritis Rheum 1990 20 : 97 106. (Pubitemid 20364841)
42. Roubenoff R, Roubenoff RA, Cannon JG et al. Rheumatoid cachexia: cytokine-driven hypermetabolism accompanying reduced body cell mass in chronic inflammation. J Clin Invest 1994 93 : 2379 2386. (Pubitemid 24177149)
43. Owen OE, Reichard Jr. GA, Patel MS, Boden G. Energy metabolism in feasting and fasting. Adv Exp Med Biol 1979 111 : 169 188.
44. Liefmann R. Endocrine imbalance in rheumatoid arthritis and rheumatoid spondylitis; hyperglycemia unresponsiveness, insulin resistance, increased gluconeogenesis and mesenchymal tissue degeneration; preliminary report. Acta Med Scand 1949 136 : 226 232.
45. Roubenoff R, Roubenoff RA, Ward LM, Stevens MB. Catabolic effects of high-dose corticosteroids persist despite therapeutic benefit in rheumatoid arthritis. Am J Clin Nutr 1990 52 : 1113 1117. (Pubitemid 120008221)
46. Walsmith J, Roubenoff R. Cachexia in rheumatoid arthritis. Int J Cardiol 2002 85 : 89 99.
47. Marcora SM, Chester KR, Mittal G, Lemmey AB, Maddison PJ. Randomized phase 2 trial of anti-tumor necrosis factor therapy for cachexia in patients with early rheumatoid arthritis. Am J Clin Nutr 2006 84 : 1463 1472. (Pubitemid 44912832)
48. Fong Y, Moldawer LL, Marano M et al. Cachectin/TNF or IL-1 alpha induces cachexia with redistribution of body proteins. Am J Physiol 1989 256 : R659 65. (Pubitemid 19086515)
49. Sarzi-Puttini P, Atzeni F, Scholmerich J, Cutolo M, Straub RH. Anti-TNF antibody therapy improves glucocorticoid- induced insulin-like growth factor-1 (IGF-1) resistance without influencing myoglobin and IGF-1 binding proteins 1 and 3. Ann Rheum Dis 2005 65 : 301 305. (Pubitemid 43268216)
50. Masi AT, Josipovic DB, Jefferson WE. Low adrenal androgenic-anabolic steroids in women with rheumatoid arthritis (RA): gas-liquid chromatographic studies of RA patients and matched normal control women indicating decreased 11-deoxy-17-ketosteroid excretion. Semin Arthritis Rheum 1984 14 : 1 23.
51. Cutolo M, Balleari E, Giusti M, Monachesi M, Accardo S. Sex hormone status of male patients with rheumatoid arthritis: evidence of low serum concentrations of testosterone at baseline and after human chorionic gonadotropin stimulation. Arthritis Rheum 1988 31 : 1314 1317.
52. Lahita RG, Bradlow HL, Ginzler E, Pang S, New M. Low plasma androgens in women with systemic lupus erythematosus. Arthritis Rheum 1987 30 : 241 248. (Pubitemid 17098574)
53. Härle P, Pongratz G, Weidler C, Büttner R, Schölmerich J, Straub RH. Possible role of leptin in hypoandrogenicity in patients with systemic lupus erythematosus and rheumatoid arthritis. Ann Rheum Dis 2004 63 : 809 816. (Pubitemid 38850452)
54. Kaufmann J, Kielstein V, Kilian S, Stein G, Hein G. Relation between body mass index and radiological progression in patients with rheumatoid arthritis. J Rheumatol 2003 30 : 2350 2355. (Pubitemid 37413892)
55. Escalante A, Haas RW, del RI. Paradoxical effect of body mass index on survival in rheumatoid arthritis: role of comorbidity and systemic inflammation. Arch Intern Med 2005 165 : 1624 1629. (Pubitemid 41124157)
56. van der Helm-van Mil AH, van der Kooij SM, Allaart CF, Toes RE, Huizinga TW. A high body mass index has a protective effect on the amount of joint destruction in small joints in early rheumatoid arthritis. Ann Rheum Dis 2008 67 : 769 774.
57. Westhoff G, Rau R, Zink A. Radiographic joint damage in early rheumatoid arthritis is highly dependent on body mass index. Arthritis Rheum 2007 56 : 3575 3582. (Pubitemid 350100690)
58. Svenson KL, Lundqvist G, Wide L, Hallgren R. Impaired glucose handling in active rheumatoid arthritis: relationship to the secretion of insulin and counter-regulatory hormones. Metabolism 1987 36 : 940 943. (Pubitemid 17160510)
59. Paolisso G, Valentini G, Giugliano D et al. Evidence for peripheral impaired glucose handling in patients with connective tissue diseases. Metabolism 1991 40 : 902 907.
60. Dessein PH, Stanwix AE, Joffe BI. Cardiovascular risk in rheumatoid arthritis versus osteoarthritis: acute phase response related decreased insulin sensitivity and high-density lipoprotein cholesterol as well as clustering of metabolic syndrome features in rheumatoid arthritis. Arthritis Res 2002 4 : R5.
61. Dessein PH, Joffe BI. Insulin resistance and impaired beta cell function in rheumatoid arthritis. Arthritis Rheum 2006 54 : 2765 2775. (Pubitemid 44497755)
62. Erdem H, Dinc A, Pay S, Simsek I, Turan M. Peripheral insulin resistance in patients with Behcet's disease. J Eur Acad Dermatol Venereol 2006 20 : 391 395.
63. Chung CP, Avalos I, Oeser A et al. High prevalence of the metabolic syndrome in patients with systemic lupus erythematosus: association with disease characteristics and cardiovascular risk factors. Ann Rheum Dis 2007 66 : 208 214. (Pubitemid 46226056)
64. Bregenzer N, Hartmann A, Strauch U, Scholmerich J, Andus T, Bollheimer LC. Increased insulin resistance and beta cell activity in patients with Crohn's disease. Inflamm Bowel Dis 2006 12 : 53 6. (Pubitemid 43032452)
65. La MG, Cacciapuoti F, Buono R et al. Insulin resistance is an independent risk factor for atherosclerosis in rheumatoid arthritis. Diab Vasc Dis Res 2007 4 : 130 135. (Pubitemid 47167497)
66. Babu NP, Bobby Z, Selvaraj N, Harish BN. Increased fructosamine in non-diabetic rheumatoid arthritis patients: role of lipid peroxides and glutathione. Clin Chem Lab Med 2006 44 : 848 852. (Pubitemid 43911559)
67. Rodriguez-Garcia J, Requena JR, Rodriguez-Segade S. Increased concentrations of serum pentosidine in rheumatoid arthritis. Clin Chem 1998 44 : 250 255. (Pubitemid 28087720)
68. Lakatos J, Harsagyi A. Serum total, HDL, LDL cholesterol, and triglyceride levels in patients with rheumatoid arthritis. Clin Biochem 1988 21 : 93 6.
69. Bruderlein H, Daniel R, Boismenu D, Julien N, Couture F. Fatty acid profiles of serum phospholipids in patients suffering rheumatoid arthritis. Prog Lipid Res 1981 20 : 625 631.
70. Iannello S, Cavaleri A, Milazzo P, Cantarella S, Belfiore F. Low fasting serum triglyceride level as a precocious marker of autoimmune disorders. MedGenMed 2003 5 : 20. (Pubitemid 41348961)
71. Rossner S, Lofmark C. Dyslipoproteinaemia in patients with active, chronic polyarthritis. A study on serum lipoproteins and triglyceride clearance (intravenous fat tolerance test). Atherosclerosis 1977 28 : 41 52. (Pubitemid 8171632)
72. Cauza E, Cauza K, Hanusch-Enserer U, Etemad M, Dunky A, Kostner K. Intravenous anti TNF-alpha antibody therapy leads to elevated triglyceride and reduced HDL-cholesterol levels in patients with rheumatoid and psoriatic arthritis. Wien Klin Wochenschr 2002 114 : 1004 1007. (Pubitemid 36105546)
73. Schenk S, Saberi M, Olefsky JM. Insulin sensitivity: modulation by nutrients and inflammation. J Clin Invest 2008 118 : 2992 3002.
74. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 1996 271 : 665 668. (Pubitemid 26052915)
75. Kiortsis DN, Mavridis AK, Vasakos S, Nikas SN, Drosos AA. Effects of infliximab treatment on insulin resistance in patients with rheumatoid arthritis and ankylosing spondylitis. Ann Rheum Dis 2005 64 : 765 766. (Pubitemid 40559306)
76. Gonzalez-Gay MA, De Matias JM, Gonzalez-Juanatey C et al. Anti-tumor necrosis factor-alpha blockade improves insulin resistance in patients with rheumatoid arthritis. Clin Exp Rheumatol 2006 24 : 83 6.
77. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 2006 6 : 772 783. (Pubitemid 44453463)
78. Frauwirth KA, Thompson CB. Regulation of T lymphocyte metabolism. J Immunol 2004 172 : 4661 4665.
79. Calder PC, Dimitriadis G, Newsholme P. Glucose metabolism in lymphoid and inflammatory cells and tissues. Curr Opin Clin Nutr Metab Care 2007 10 : 531 540. (Pubitemid 46934126)
80. Adiels M, Olofsson SO, Taskinen MR, Boren J. Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler Thromb Vasc Biol 2008 28 : 1225 1236.
81. Ilowite NT, Samuel P, Ginzler E, Jacobson MS. Dyslipoproteinemia in pediatric systemic lupus erythematosus. Arthritis Rheum 1988 31 : 859 863.
82. Ettinger Jr. WH, Hazzard WR. Elevated apolipoprotein-B levels in corticosteroid-treated patients with systemic lupus erythematosus. J Clin Endocrinol Metab 1988 67 : 425 428.
83. Borba EF, Bonfa E. Dyslipoproteinemias in systemic lupus erythematosus: influence of disease, activity, and anticardiolipin antibodies. Lupus 1997 6 : 533 539. (Pubitemid 27371222)
84. Jones SM, Harris CP, Lloyd J, Stirling CA, Reckless JP, McHugh NJ. Lipoproteins and their subfractions in psoriatic arthritis: identification of an atherogenic profile with active joint disease. Ann Rheum Dis 2000 59 : 904 909.
85. Hahn BH, Grossman J, Chen W, McMahon M. The pathogenesis of atherosclerosis in autoimmune rheumatic diseases: roles of inflammation and dyslipidemia. J Autoimmun 2007 28 : 69 75. (Pubitemid 46670686)
86. Grunfeld C, Feingold KR. Tumor necrosis factor, cytokines, and the hyperlipidemia of infection. Trends Endocrinol Metab 1991 2 : 213 219.
87. Sherman ML, Spriggs DR, Arthur KA, Imamura K, Frei III. E, Kufe DW. Recombinant human tumor necrosis factor administered as a five-day continuous infusion in cancer patients: phase I toxicity and effects on lipid metabolism. J Clin Oncol 1988 6 : 344 350. (Pubitemid 18065941)
88. Khovidhunkit W, Kim MS, Memon RA et al. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res 2004 45 : 1169 1196. (Pubitemid 38802622)
89. Pond CM, Mattacks CA. Interactions between adipose tissue around lymph nodes and lymphoid cells in vitro. J Lipid Res 1995 36 : 2219 2231.
90. Pond CM. Paracrine relationships between adipose and lymphoid tissues: implications for the mechanism of HIV-associated adipose redistribution syndrome. Trends Immunol 2003 24 : 13 8.
91. Jessop DS, Harbuz MS. A defect in cortisol production in rheumatoid arthritis: why are we still looking? Rheumatology (Oxford) 2005 44 : 1097 1100.
92. Straub RH, Paimela L, Peltomaa R, Schölmerich J, Leirisalo-Repo M. Inadequately low serum levels of steroid hormones in relation to IL-6 and TNF in untreated patients with early rheumatoid arthritis and reactive arthritis. Arthritis Rheum 2002 46 : 654 662. (Pubitemid 34214248)
93. Dekkers JC, Geenen R, Godaert GL et al. Experimentally challenged reactivity of the hypothalamic pituitary adrenal axis in patients with recently diagnosed rheumatoid arthritis. J Rheumatol 2001 28 : 1496 1504. (Pubitemid 32660619)
94. Miller AH, Pariante CM, Pearce BD. Effects of cytokines on glucocorticoid receptor expression and function. Glucocorticoid resistance and relevance to depression. Adv Exp Med Biol 1999 461 : 107 116. (Pubitemid 32187422)
95. Webster JC, Oakley RH, Jewell CM, Cidlowski JA. Proinflammatory cytokines regulate human glucocorticoid receptor gene expression and lead to the accumulation of the dominant negative beta isoform: a mechanism for the generation of glucocorticoid resistance. Proc Natl Acad Sci U S A 2001 98 : 6865 6870.
96. Djurhuus CB, Gravholt CH, Nielsen S, Pedersen SB, Moller N, Schmitz O. Additive effects of cortisol and growth hormone on regional and systemic lipolysis in humans. Am J Physiol Endocrinol Metab 2004 286 : E488 94. (Pubitemid 38292701)
97. Castagnetta LA, Carruba G, Granata OM et al. Increased estrogen formation and estrogen to androgen ratio in the synovial fluid of patients with rheumatoid arthritis. J Rheumatol 2003 30 : 2597 2605. (Pubitemid 37549336)
98. Schmidt M, Weidler C, Naumann H, Schölmerich J, Straub RH. Androgen conversion in osteoarthritis and rheumatoid arthritis synoviocytes - androstenedione and testosterone inhibit estrogen formation and favor production of more potent 5alpha-reduced androgens. Arthritis Res Ther 2005 7 : R938 48.
99. Pedersen SB, Kristensen K, Hermann PA, Katzenellenbogen JA, Richelsen B. Estrogen controls lipolysis by up-regulating alpha2A-adrenergic receptors directly in human adipose tissue through the estrogen receptor alpha. Implications for the female fat distribution. J Clin Endocrinol Metab 2004 89 : 1869 1878. (Pubitemid 38507947)
100. Elbers JM, Asscheman H, Seidell JC, Gooren LJ. Effects of sex steroid hormones on regional fat depots as assessed by magnetic resonance imaging in transsexuals. Am J Physiol 1999 276 : E317 25. (Pubitemid 29100588)
101. Perry F, Heller PH, Kamiya J, Levine JD. Altered autonomic function in patients with arthritis or with chronic myofascial pain. Pain 1989 39 : 77 84. (Pubitemid 19258912)
102. Kuis W, Jong-de Vos V, Sinnema G et al. The autonomic nervous system and the immune system in juvenile rheumatoid arthritis. Brain Behav Immun 1996 10 : 387 398. (Pubitemid 27116512)
103. Nakajima A, Sendo W, Tsutsumino M et al. Acute sympathetic hyperfunction in overlapping syndromes of systemic lupus erythematosus and polymyositis. J Rheumatol 1998 25 : 1638 1641. (Pubitemid 28364775)
104. Glück T, Oertel M, Reber T, Zietz B, Schölmerich J, Straub RH. Altered function of the hypothalamic stress axes in patients with moderately active systemic lupus erythematosus. I. The hypothalamus-autonomic nervous system axis. J Rheumatol 2000 27 : 903 910. (Pubitemid 30389745)
105. Härle P, Straub RH, Wiest R et al. Increase of sympathetic outflow measured by NPY and decrease of the hypothalamic-pituitary-adrenal axis tone in patients with SLE and RA - another example of uncoupling of response systems. Ann Rheum Dis 2005 65 : 51 6.
106. Dekkers JC, Geenen R, Godaert GL, Bijlsma JW, Doornen LJP. Sympathetic and parasympathetic nervous system activity at night in patients with recently diagnosed rheumatoid arthritis. In : Dekkers JC, ed. Thesis: Psychophysiological Responsiveness in Recently Diagnosed Patients with Rheumatoid Arthritis.
107. Dekkers JC, Geenen R, Godaert GL, Bijlsma JW, van Doornen LJ. Elevated sympathetic nervous system activity in patients with recently diagnosed rheumatoid arthritis with active disease. Clin Exp Rheumatol 2004 22 : 63 70. (Pubitemid 38236126)
108. Scherrer U, Sartori C. Insulin as a vascular and sympathoexcitatory hormone: implications for blood pressure regulation, insulin sensitivity, and cardiovascular morbidity. Circulation 1997 96 : 4104 4113. (Pubitemid 27506070)
109. Levine JD, Dardick SJ, Roizen MF, Helms C, Basbaum AI. Contribution of sensory afferents and sympathetic efferents to joint injury in experimental arthritis. J Neurosci 1986 6 : 3423 3429.
110. Härle P, Mobius D, Carr DJ, Schölmerich J, Straub RH. An opposing time-dependent immune-modulating effect of the sympathetic nervous system conferred by altering the cytokine profile in the local lymph nodes and spleen of mice with type II collagen-induced arthritis. Arthritis Rheum 2005 52 : 1305 1313. (Pubitemid 40530141)
111. Straub RH, Grum F, Strauch UG et al. Anti-inflammatory role of sympathetic nerves in chronic intestinal inflammation. Gut 2008 57 : 911 921. (Pubitemid 351919525)
112. Capellino S, Falk W, Straub RH. Reserpine as a new therapeutical agent in arthritis. Arthritis Rheum 2009 58 : S730.
113. Miller LE, Jüsten HP, Schölmerich J, Straub RH. The loss of sympathetic nerve fibers in the synovial tissue of patients with rheumatoid arthritis is accompanied by increased norepinephrine release from synovial macrophages. FASEB J 2000 14 : 2097 2107.
114. Del Rey A, Wolff C, Wildmann J et al. Disrupted joint-immune-brain communication during experimental arthritis. Arthritis Rheum 2008 58 : 3090 3099.
115. Straub RH, Rauch L, Fassold A, Lowin T, Pongratz G. Neuronally released sympathetic neurotransmitters stimulate splenic interferon-gamma secretion from T cells in early type II collagen-induced arthritis. Arthritis Rheum 2008 58 : 3450 3460.
116. Lorton D, Lubahn C, Sweeney S et al. Differences in the injury/sprouting response of splenic noradrenergic nerves in Lewis rats with adjuvant-induced arthritis compared with rats treated with 6-hydroxydopamine. Brain Behav Immun 2009 23 : 276 285.
117. Moore MC, Satake S, Baranowski B, Hsieh PS, Neal DW, Cherrington AD. Effect of hepatic denervation on peripheral insulin sensitivity in conscious dogs. Am J Physiol Endocrinol Metab 2002 282 : E286 96. (Pubitemid 34654798)
118. Vatamaniuk MZ, Horyn OV, Vatamaniuk OK, Doliba NM. Acetylcholine affects rat liver metabolism via type 3 muscarinic receptors in hepatocytes. Life Sci 2003 72 : 1871 1882.
119. Xue C, Aspelund G, Sritharan KC, Wang JP, Slezak LA, Andersen DK. Isolated hepatic cholinergic denervation impairs glucose and glycogen metabolism. J Surg Res 2000 90 : 19 25. (Pubitemid 30317172)
120. Bartness TJ, Song CK. Thematic review series: adipocyte biology. Sympathetic and sensory innervation of white adipose tissue. J Lipid Res 2007 48 : 1655 1672.
121. Tracey KJ. Physiology and immunology of the cholinergic antiinflammatory pathway. J Clin Invest 2007 117 : 289 296.
122. Waldburger JM, Boyle DL, Pavlov VA, Tracey KJ, Firestein GS. Acetylcholine regulation of synoviocyte cytokine expression by the alpha7 nicotinic receptor. Arthritis Rheum 2008 58 : 3439 3449.
123. van Maanen MA, Lebre MC, van der PT et al. Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum 2009 60 : 114 122.
124. Bertero MT, Caligaris-Cappio F. Anemia of chronic disorders in systemic autoimmune diseases. Haematologica 1997 82 : 375 381. (Pubitemid 28023326)
125. Kötter I, Wacker A, Koch S et al. Anakinra in patients with treatment-resistant adult-onset Still's disease: four case reports with serial cytokine measurements and a review of the literature. Semin Arthritis Rheum 2007 37 : 189 197. (Pubitemid 350151506)
126. Nicolas G, Bennoun M, Devaux I et al. Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc Natl Acad Sci U S A 2001 98 : 8780 8785. (Pubitemid 32678104)
127. Beard JL. Iron biology in immune function, muscle metabolism and neuronal functioning. J Nutr 2001 131 : 568S 79S.
128. Marx JJ. Iron and infection: competition between host and microbes for a precious element. Best Pract Res Clin Haematol 2002 15 : 411 426. (Pubitemid 35331275)
129. Theurl I, Fritsche G, Ludwiczek S, Garimorth K, Bellmann-Weiler R, Weiss G. The macrophage: a cellular factory at the interphase between iron and immunity for the control of infections. Biometals 2005 18 : 359 367. (Pubitemid 41298020)
130. Hibbert JM, Creary MS, Gee BE, Buchanan ID, Quarshie A, Hsu LL. Erythropoiesis and myocardial energy requirements contribute to the hypermetabolism of childhood sickle cell anemia. J Pediatr Gastroenterol Nutr 2006 43 : 680 687. (Pubitemid 44863698)
131. Fernandez-Real JM, Lopez-Bermejo A, Ricart W. Cross-talk between iron metabolism and diabetes. Diabetes 2002 51 : 2348 2354. (Pubitemid 34827381)
132. Wasserman DH, Lavina H, Lickley A, Vranic M. Effect of hematocrit reduction on hormonal and metabolic responses to exercise. J Appl Physiol 1985 58 : 1257 1262. (Pubitemid 15033191)
133. Walsh NC, Crotti TN, Goldring SR, Gravallese EM. Rheumatic diseases: the effects of inflammation on bone. Immunol Rev 2005 208 : 228 251. (Pubitemid 41746396)
134. Al-Awadhi A, Olusi S, Al-Zaid N, Prabha K. Serum concentrations of interleukin 6, osteocalcin, intact parathyroid hormone, and markers of bone resorption in patients with rheumatoid arthritis. J Rheumatol 1999 26 : 1250 1256. (Pubitemid 29268073)
135. Lange U, Jung O, Teichmann J, Neeck G. Relationship between disease activity and serum levels of vitamin D metabolites and parathyroid hormone in ankylosing spondylitis. Osteoporos Int 2001 12 : 1031 1035. (Pubitemid 34105974)
136. Thomas T, Burguera B, Melton III. LJ et al. Role of serum leptin, insulin, and estrogen levels as potential mediators of the relationship between fat mass and bone mineral density in men versus women. Bone 2001 29 : 114 120. (Pubitemid 32734491)
137. Lee NK, Karsenty G. Reciprocal regulation of bone and energy metabolism. Trends Endocrinol Metab 2008 19 : 161 166. (Pubitemid 351847838)
138. Li YP, Stashenko P. Proinflammatory cytokines tumor necrosis factor-alpha and IL-6, but not IL-1, down-regulate the osteocalcin gene promoter. J Immunol 1992 148 : 788 794.
139. Duncan H. Osteoporosis in rheumatoid arthritis and corticosteroid induced osteoporosis. Orthop Clin North Am 1972 3 : 571 583.
140. Takeda S, Karsenty G. Molecular bases of the sympathetic regulation of bone mass. Bone 2008 42 : 837 840.
141. Selye H, Fortier C. Adaptive reactions to stress. Res Publ Assoc Res Nerv Ment Dis 1949 29 : 3 18.
142. Kohm AP, Sanders VM. Norepinephrine: a messenger from the brain to the immune system. Immunol Today 2000 21 : 539 542.