Immunoregulatory role of endogenous catecholamines synthesized by immune cells

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Author:
JIANG Jian-Lan()
QIU Yi-Hua()
PENG Yu-Ping()
WANG Jian-Jun()
Journal Title:
ACTA PHYSIOLOGICA SINICA
Issue:
Volume 58, Issue 04, 2006
DOI:
Key Word:
catecholamines;lymphocytes;tyrosine hydroxylase;adrenergic receptor;cyclic AMP

Abstract: It has been well known that catecholamines (CAs) in the body, including norepinephrine (NE), epinephrine (E) and dopamine (DA), are synthesized and secreted by neurons and endocrine cells and mainly modulate visceral activities such as cardiovascular,respiratory and digestive functions. The studies over the past nearly 30 years have shown that CAs can also regulate immune function.The immunomodulation of CAs is generally considered as a role mediating the regulation of nervous and endocrine systems. However,recent studies reveal that immune cells can also synthesize CAs, which is an update of traditional concept. A classical metabolic pathway of CAs shared by the nervous and endocrine systems is present in the immune cells, i.e., the immunocytes have the enzymes for synthesis of CAs [e.g. tyrosine hydroxylase (TH)] and the enzymes for degradation of CAs [e.g. monoamine oxidase (MAO) and catechol-O-methyl transferase (COMT)]. The endogenous CAs synthesized by immune cells can regulate many immune functions,including cellular proliferation, differentiation, apoptosis and cytokine production. These roles of the endogenous CAs may be mediated by an autocrine/paracrine pathway via relevant receptors on the immunocytes and intracellular cAMP. Intracellular oxidative mechanism may also be involved in immunoregulation of endogenous CAs in immune cells. In addition, some metabolic abnormalities of CAs in the immune cells probably induce some autoimmune diseases, such as multiple sclerosis (MS) and rheumatoid arthritis.These findings not only provide evidence for the new concept that the immune system is possible to become the third CA system other than the nervous and endocrine systems, but also extend our comprehension on functional significance of the endogenous CAs synthesized by immune cells.

  • [1]Blalock JE.The syntax of immune-neuroendocrine communication.Immunol Today 1994; 15(11):504-511.
  • [2]Dahlstroem AB,Zetterstroem BE.Noradrenaline stores in nerve terminals of the spleen:changes during hemorrhagic shock.Science 1965; 147:1583-1585.
  • [3]Meltzer JC,Grimm PC,Greenberg AH,Nance DM.Enhanced immunohistochemical detection of autonomic nerve fibers,cytokines and inducible nitric oxide synthase by light and fluorescent microscopy in rat spleen.J Histochem Cytochem 1997;45(4):599-610.
  • [4]Panuncio AL,De La Pena S,Gualco G,Reissenweber N.Adrenergic innervation in reactive human lymph nodes.J Anat 1999;194:143-146.
  • [5]Swanson MA,Lee WT,Sanders VM.IFN-gamma production by Th1 cells generated from naive CD4+ T cells exposed to norepinephrine.J Immunol 2001; 166(1):232-240.
  • [6]Sanders VM,Baker RA,Ramer-Quinn DS,Kasprowicz DJ,Fuchs BA,Street NE.Differential expression of the beta2-adrenergic receptor by Th1 and Th2 clones:implications for cytokine production and B cell help.J Immunol 1997; 158(9):4200-4210.
  • [7]Kohm AP,Mozaffarian A,Sanders VM.B cell receptor-and beta 2-adrenergic receptor-induced regulation of B7-2 (CD86)expression in B cells.J Immunol 2002; 168(12):6314-6322.
  • [8]Ghosh MC,Mondal AC,Basu S,Banerjee S,Majumderc J,Bhattacharya D,Dasgupta PS.Dopamine inhibits cytokine release and expression of tyrosine kinases,Lck and Fyn in activated T cells.Int Immunopharmacol 2003; 3(7):1019-1026.
  • [9]Dong J,Mrabet O,Moze E,Li K,Neveu PJ.Lateralization and catecholaminergic neuroimmunomodulation:prazosin,an alpha 1/alpha 2-adrenergic receptor antagonist,suppresses interleukin-1 and increases interleukin-10 production induced by lipopolysaccharides.Neuroimmunomodulation 2003; 10(3):163-168.
  • [10]Torres KC,Antonelli LR,Souza AL,Teixeira MM,Dutra WO,Gollob KJ.Norepinephrine,dopamine and dexamethasone modulate discrete leukocyte subpopulations and cytokine profiles from human PBMC.J Neuroimmunol 2005; 166(1-2):144-157.
  • [11]Offen D,Ziv I,Gorodins S,Barzilai A,Malik Z,Melamed E.Dopamine-induced programmed cell death in mouse thymocytes.Biochim Biophys Acta 1995; 1268(2):171-177.
  • [12]Peng YP (彭聿平),Qiu YH,Zhang QQ,Wang JH.Effect ofnoradrenaline on T lymphocyte proliferation.Chin J Appl Physiol (中国应用生理学杂志) 1995; 11:75-78 (Chinese,English abstract).
  • [13]Peng YP,Qiu YH,Jiang JL,Wang JJ.Effect ofcatecholamines on IL-2 production and NK cytotoxicity of rats in vitro.Acta Pharmacol Sin 2004; 25(10):1354-1360.
  • [14]Bergquist J,Tarkowski A,Ekman R,Ewing A.Discovery of endogenous catecholamines in lymphocyte evidence for catecholamine regulation of lymphocyte function via an autocrine loop.Proc Natl Acad Sci USA 1994; 91(26):12912-12916.
  • [15]Bergquist J,Josefsson E,Tarkowski A,Ekman R,Ewing A.Measurements of catecholamine-mediated apoptosis of immunocompetent cells by capillary electrophoresis.Electrophoresis 1997; 18(10):1760-1766.
  • [16]Bergquist J,Sliberring J.Identification of catecholamines in the immune system by electrosprayionization mass.Rapid Commun Mass Spectrom 1998; 12(11):683-688.
  • [17]Knudsen JH,Christensen NJ,Bratholm P.Lymphocyte norepinephrine and epinephrine,but not plasma catecholamines predict lymphocyte cAMP production.Life Sci 1996; 59(8):639-647.
  • [18]Cosentino M,Bombelli R,Ferrari M,Marino F,Rasini M,Maestroni GJ,Conti A,Boveri M,Lecchini S,Frigo G.HPLC-ED measurement of endogenous catecholamines in human immune cells and hematopoietic cell lines.Life Sci 2000; 68(3):283-295.
  • [19]Cosentino M,Marino F,Bombelli R,Ferrari M,Lecchini S,Frigo G.Endogenous catecholamine synthesis,metabolism,storage and uptake in human neutrophils.Life Sci 1999; 64(11):975-981.
  • [20]Brown SW,Meyers RT,Brennan KM,Rumble JM,Narasimhachari N,Perozzi EF,Ryan JJ,Stewart JK,FischerStenger K.Catecholamines in a macrophage cell line.J Neuroimmunol 2003; 135(1-2):47-55.
  • [21]Josefsson E,Bergquist J,Ekman R,Tarkowski A.Catecholamines are synthesized by mouse lymphocytes and regulate function of these cells by induction of apoptosis.Immunology 1996;88(1):140-146.
  • [22]Freeman JG,Ryan JJ,Shelburne CP,Bailey DP,Bouton,LA,Narasimhachari N,Domen J,Simeon N,Couderc F,Stewart JK.Catecholamines in murine bone marrow derived mast cells.J Neuroimmunol 2001; 119:231-238.
  • [23]Qiu YH,Peng YP,Jiang JM,Wang JJ.Expression of tyrosine hydroxylase in lymphocytes and effect of endogenous catecholamines on lymphocyte function.Neuroimmunomodulation 2004;11(2):75-83.
  • [24]Qiu YH,Cheng C,Dai L,Peng YP.Effect of endogenous catecholamines in lymphocytes on lymphocyte function.J Neuroimmunol 2005; 167(1-2):45-52.
  • [25]Tsao CW,Lin YS,Cheng JT.Inhibition of immune cell proliferation with haloperidol and relationship of tyrosine hydroxylase expression to immune cell growth.Life Sci 1998; 62(21):335-344.
  • [26]Cosentino M,Marino F,Bombelli R,Ferrari M,Rasini E,Lecchini S,Frigo G.Stimulation with phytohaemagglutinin induces the synthesis of catecholamines in human peripheral blood mononuclear cells:role of protein kinase C and contribution of intracellular calcium.J Neuroimmunol 2002; 125(1-2):125-133.
  • [27]Musso NR,Brenci S,Settim M,Indiveri F,Lotti G.Catecholamine content and in vitro catecholamine synthesis in peripheral human lymphocytes.J Clin Endocrinol Metab 1996; 81 (10):3553-3557.
  • [28]Shore PA.The mechanism of norepinephrine depletion by reserpine,metaraminol and related agents.The role of monoamine oxidase.Pharmacol Rev 1966; 18(1):561-568.
  • [29]Musso NR,Brenci S,Indiveri F,Lotti G.Acetylcholine-induced,calcium-dependent norepinephrine outflow from peripheral human lymphocytes.J Neuroimmunol 1998; 87(1-2):82-87.
  • [30]Kilpatrick DL,Slepetis RJ,Corcoran JJ,Kirshner N.Calcium uptake and catecholamine secretion by cultured bovine adrenal medulla cells.J Neurochem 1982; 38(2):427-435.
  • [31]Faraj BA,Olkowski ZL and Jackson RT.Binding of[3H]-dopamine to human lymphocytes:possible relationship to neurotransmitter uptake sites.Pharmacology 1991; 42(3):135-141.
  • [32]Faraj BA,Olkowski ZL,Jackson RT.A cocaine-sensitive active dopamine transport in human lymphocytes.Biochem Pharmacol 1995; 50(7):1007-1014.
  • [33]Basu S,Dasgupta PS,Lahiri T,Roychowdhury J.Uptake and biodistribution of dopamine in bone marrow,spleen and lymph nodes of normal and tumor bearing mice.Life Sci 1993; 53(5):415-424.
  • [34]Krieger K,Klimke A,Henning U.Active[3H]-dopamine uptake displayed by native lymphocyte suspensions is mainly due to contaminating platelets.Pharmacopsychiatry 1998; 31 (5):193-198.
  • [35]Amenta F,Bronzetti E,Cantalamessa F,El-Assouad D,Felici L,Ricci A,Tayebati SK.Identification of dopamine plasma membrane and vesicular transporters in human peripheral blood lymphocyte.J Neuroimmunol2001; 117(1-2):133-142.
  • [36]Mill J,Asherson P,Browes C,D' Souza U,Craig I.Expression of the dopamine transporter gene is regulated by the 3' UTR VNTR:Evidence from brain and lymphocytes using quantitative RT-PCR.Am J Med Genet 2002; 114(8):975-979.
  • [37]Marino F,Cosentino M,Bombelli R,Ferrari M,Lecchini S,Frigo GM.Endogenous catecholamine synthesis,metabolism,storage,and uptake in human peripheral blood mononuclear cells.Exp Hematol 1999; 27(3):489-495.
  • [38]Cosentino M,Marino F,Bombelli R,Ferrari M,Lecchini S,Frigo G.Unravelling dopamine (and catecholamine)physiopharmacology in lymphocytes:open questions.Trends Immunol 2003; 24(11):581-582.
  • [39]Gordon J,Barnes NM.Lymphocytes transport serotonin and dopamine:agony or ecstasy? Trends Immunol 2003; 24(8):438-443.
  • [40]Bidart JM,Motte PH,Assicot M,Bohuon C,Bellet D.Catechol-O-methyltransferase activity and aminergic binding sites distribution in human peripheral blood lymphocyte subpopulations.Clin Immunol Immunopathol 1983; 26(1):1-9.
  • [41]Balsa MD,Gomez N,Unzeta M.Characterization of monoamine oxidase activity present in human granulocytes and lymphocytes.Biochim Biophys Acta 1989; 992(2):140-144.
  • [42]Rouppe van der Voort C,Kavelaars A,van de Pol M,Heijnen CJ.Noradrenaline induces the phosphorylation of ERK-2 in human peripheral blood mononuclear cells after induction of α1-adrenergic receptors.J Neuroimmunol2000; 108(1-2):82-91.
  • [43]Zoukos Y,Kidd D,Woodroofe MN,Kendall BE,Thompson AJ,Cuzner ML.Increased expression of high affinity IL-2receptors and β-adrenoceptors on peripheral blood mononuclear cells is associated with clinical and MRI activity in multiple sclerosis.Brain 1994; 117:307-315.
  • [44]Cosentino M,Zaffaronid M,Marino F,Bombelli R,Ferrari M,Rasini E,Lecchini S,Ghezzi A,Frigo G.Catecholamine production and tyrosine hydroxylase expression in peripheral blood mononuclear cells from multiple sclerosis patients:effect of cell stimulation and possible relevance for activation-induced apoptosis.J Neuroimmunol 2002; 133(1-2):233-240.
  • [45]Pochet R,Delespesse G,Gausset PW,Collet H.Distribution of β-adrenergic receptors on human lymphocyte subpopulations.Clin Exp Immunol 1979; 38(3):578-584.
  • [46]Brodde OE,Engel G,Hoyer D,Bock KD,Weber F.The betaadrenergic receptor in human lymphocytes:subclassification by the use of a new radio-ligand,(±)-125 iodocyanopindolol.Life Sci1981; 29(21):2189-2198.
  • [47]Miles K,Atweh S,Otten G,Amason BG,Chelmicka-Schorr E.Beta-adrenergic receptors on splenic lymphocytes from axotomized mice.Int J Immunopharmacol 1984; 6(3):171-177.
  • [48]Jetschmann JU,Benschop RJ,Jacobs R,Kemper A,Oberbeck R,Schmidt RE,Schedlowski M.Expression and in-vivo modulation of alpha-and beta-adrenoceptors on human natural killer (CD16+) cells.J Neuroimmunol 1997; 74(1-2):159-164.
  • [49]Kavelaars A.Regulated expression of alpha-1 adrenergic receptors in the immune system.Brain Behav Immun 2002; 16(6):799-807.
  • [50]McKenna F,McLaughlin PJ,Lewis BJ,Sibbring GC,Cummerson JA,Bowen-Jones D.Dopamine receptor expression on human T-and B-lymphocytes,monocytes,neutrophils,eosinophils and NK cells:a flow cytometric study.J Neuroimmunol 2002; 132(1-2):34-40.
  • [51]Ricci A,Veglio F,Amenta F.Radioligand binding characterization of putative dopamine D3 receptor in human peripheral blood lymphocytes with[3H]7-OH-DPAT.J Neuroimmunol 1995; 58(2):139-144.
  • [52]Kwak YT,Koo MS,Choi CH,Sunwoo I.Change of dopamine receptor mRNA expression in lymphocyte of schizophrenic patients.BMC Med Genet 2001; 2:3-11.
  • [53]Spengler RN,Chensue SW,Giacherio DA,Blenk N,Kunkel SL.Endogenous norepinephrine regulates tumor necrosis factor-αproduction from macrophages in vitro.J Immunol 1994; 152(6):3024-3031.
  • [54]Engler KL,Rudd ML,Ryan JJ,Stewarta JK,Fischer-Stenger K.Autocrine actions of macrophage-derived catecholamines on interleukin-1β.J Neuroimmunol 2005; 160(1-2):87-91.
  • [55]Velez-Pardo C,Del Rio MJ,Ebinger G,Vauquelin G.Monoamine and iron-related toxicity:from "erotonin-bindingproteins"to lipid peroxidation and apoptosis in PC 12 cells.Gen Pharmacol 1998; 31(1):19-24.
  • [56]Offen D,Ziv I,Gorodin S,Barzilai A,Malik Z,Melamed E.Dopamine-induced programmed cell death in mouse thymocytes.Biochim Biophys Acta 1995; 1268(2):171-177.
  • [57]Del Rio MJ,Velez-Pardo C.Monoamine neurotoxins-induced apoptosis in lymphocytes by a common oxidative stress mechanism:involvement of hydrogen peroxide (H2O2),caspase-3,and nuclear factor kappa-B (NF-κB),p53,c-Jun transcription factors.Biochem Pharmacol 2002; 63(4):677-688.
  • [58]Jones DC,Gunasekar PG,Borowitz JL,Isom GE.Dopamine induced apoptosis is mediated by oxidative stress and is enhanced by cyanide in differentiated PC12 cells.J Neurochem 2000; 74(6):2296-2304.
  • [59]Cosentino M,Rasini E,Colombo C,Marino F,Blandini F,Ferrari M,Samuele A,Lecchini S,Nappi G,Frigo G.Dopaminergic modulation of oxidative stress and apoptosis in human peripheral blood lymphocytes:evidence for a D1-like receptor-dependent protective effect.Free Radic Biol Med 2004; 36(10):1233-1240.
  • [60]Graham DG,Tiffany SM,Bell WR,Gutknecht WF.Autoxidation versus covalent binding of quinones as the mechanism of toxicity of dopamine,6-hydroxydopamine,and related compounds toward C 1300 neuroblastoma cells in vitro.Mol Pharmacol1978; 14(4):644-653.
  • [61]Burke WJ,Kristal BS,Yu BP,Li SW,Lin TS.Norepinephrine transmitter metabolite generates free radicals and activates mitochondrial permeability transition:a mechanism for DOPEGAL-induced apoptosis.Brain Res 1998; 787(2):328-332.
  • [62]Buu NT.Uptake of 1-methyl-4-phenylpyridinium and dopamine in the mouse brain cell nuclei.J Neurochem 1993; 61(4):1557-1560.
  • [63]Bergquist J,Ohlsson B,Tarkowski A.Nuclear factor-kappa B is involved in the catecholaminergic suppression of immunocompetent cells.Ann NY Acad Sci 2000; 917:281-289.
  • [64]Noseworthy JH,Lucchinetti C,Rodriguez M,Weisenhenker BG.Multiple sclerosis.N Engl J Med 2000; 343(13):938-952.
  • [65]Lassmann H,Bruck W,Lucchinetti C.Heterogeneity of multiple sclerosis pathogenesis:implications for diagnosis and therapy.Trends Mol Med 2001; 7(3):115-121.
  • [66]Martin R,McFarland HF.Immunological aspects of experimental allergic encephalomyelitis and multiple sclerosis.Crit Rev Clin Lab Sci 1995; 32(2):121-182.
  • [67]Pender MP.Genetically determined failure of activation-induced apoptosis of autoreactive T cells as a cause of multiple sclerosis.Lancet 1998; 351(9017):978-981.
  • [68]Comi C,Leone M,Bonissoni S,DeFranco S,Bottarel F,Mezzatesta C,Chiocchetti A,Perla F,Monaco F,Dianzani U.Defective T cell Fas function in patients with multiple sclerosis.Neurology 2000; 55(7):921-927.
  • [69]Sharief MK,Douglas M,Noori M,Semra YK.The expression of pro-and anti-apoptosis Bcl-2 family proteins in lymphocytes from patients with multiple sclerosis.J Neuroimmunol 2002; 125(1-2):155-162.
  • [70]Rajda C,Bencsik K,Vecsei LL,Bergquist J.Catecholamine levels in peripheral blood lymphocytes from multiple sclerosis patients.J Neuroimmunol 2002; 124(1-2):93-100.
  • [71]Cosentino M,Marco Z,Zaffaroni M,Marino F,Bombelli R,Rasini E,Frigo G,Ghezzi A,ComiG,Lecchini S.Interferon-γand interferon-β affect endogenous catecholamines in human peripheral blood mononuclear cells:Implications for multiple sclerosis.J Neuroimmuno12005; 162(1-2):112-121.
  • [72]Olsson T,Zhi WW,Hojeberg B,Kostulas V,Jiang YP,Anderson G,Ekre HP,Link H.Autoreactive T lymphocytes in multiple sclerosis determined by antigen-induced secretion of interferon-gamma.J Clin Invest 1990; 86(3):981-985.
  • [73]Rieckrnann P,Albrecht M,Kitze B,Weber T,Tumani H,Broocks A,Luer W,Poser S.Cytokine mRNA levels in mononuclear blood cells from patients with multiple sclerosis.Neurology 1994; 44(8):1523-1526.
  • [74]Hohnoki K,Inoue A,Koh CS.Elevated serum levels of IFN-γIL-4 and TNF-α/unelevated serum levels of IL-10 in patients with demyelinating diseases during the acute stage.J Neuroimmunol 1998; 87(1-2):27-32.
  • [75]Panitch HS,Hirsch RL,Haley AS,Johnson KP.Exacerbations of multiple sclerosis in patients treated with gamma interferon.Lancet 1987; 1(8538):893-895.
  • [76]Revel M.Interferon-beta in the treatment of relapsing-remitting multiple sclerosis.Pharmacol Ther 2003; 100(1):49-62.
  • [77]Caronti B,Tanda G,Colosimo C,Ruggieri S,Calderaro C,Palladini G,Pontieri FE,Di Chiara G.Reduced dopamine in peripheral blood lymphocytes in Parkinson's disease.Neuroreport 1999; 10(14):2907-2910.
  • [78]Rajda C,Dibo G,Vecsei L,Bergquist J.Increased dopamine content in lymphocytes from high-dose L-Dopa-treated Parkinson's disease patients.Neuroimmunomodulation 2005; 12(2):81-84.
  • [79]Roupe van der Voort C,Heijnen CJ,Wulffraat N,Kuis W,Kavelaars A.Stress induces increases in IL-6 production by leucocytes of patients with the chronic inflammatory disease juvenile rheumatoid arthritis:a putative role for α1-adrenergic receptors.J Neuroimmunol 2000; 110(1-2):223-229.
  • [80]Chelmicka-Schorr E,Arnason BG.Nervous system-immune system interactions and their role in multiple sclerosis.Ann Neurol 1994; 36:S29-S32.
  • [81]Baerwald CG,Laufenberg M,Specht T,von Wichert P,Burmester GR,Krause A.Impaired sympathetic influence on the immune response in patients with rheumatoid arthritis due to lymphocyte subsetspecific modulation of beta 2-adrenergic receptors.Br J Rheumatol 1997; 36(12):1262-1269.
  • [82]Miller LE,Justen HP,Scholmerich 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(13):2097-2107.
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