Norepinephrine and adenosine-5'-triphosphate synergize in inducing IL-6 production by human dermal microvascular endothelial cells

Cytokine

Volumn 64, Issue 2, 2013, Pages 605-612

  Stohl, Lori L ^a   Zang, Julie B ^a   Ding, Wanhong ^a   Manni, Michela ^a   Zhou, Xi K ^a   Granstein, Richard D ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Adenosine 5' triphosphate; Endothelial cells; IL 6; Norepinephrine

Indexed keywords

ADENOSINE TRIPHOSPHATE; BETA 2 ADRENERGIC RECEPTOR; INTERLEUKIN 6; MESSENGER RNA; NORADRENALIN;

ADRENERGIC SYSTEM; ARTICLE; CELL STIMULATION; CELL STRESS; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE EXACERBATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLAMMATION; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PSORIASIS; REAL TIME POLYMERASE CHAIN REACTION; SKIN BLOOD VESSEL; SKIN DISEASE; SYMPATHETIC NERVE CELL; TH17 CELL;

ADENOSINE-5′-TRIPHOSPHATE; ADRENERGIC RECEPTOR; AR; ATP; DEPLETED MEDIUM; DM; EC; ENDOTHELIAL CELL; ENDOTHELIAL CELLS; ICAM-1; IL-6; INTERCELLULAR ADHESION MOLECULE 1; NE; NOREPINEPHRINE; PHDMEC; PRIMARY HUMAN DERMAL ENDOTHELIAL CELLS; PROP; PROPRANOLOL; SAL; SALBUTAMOL; SNS; SYMPATHETIC NERVOUS SYSTEM;

ADENOSINE TRIPHOSPHATE; ADRENERGIC BETA-2 RECEPTOR AGONISTS; ADRENERGIC BETA-2 RECEPTOR ANTAGONISTS; CELL COUNT; CELL LINE; CELL SURVIVAL; DERMIS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-6; MICROVESSELS; NOREPINEPHRINE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ADRENERGIC, BETA-2; RNA, MESSENGER;

EID: 84885188870     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2013.08.005     Document Type: Article

References (100)

1. Danese S., Dejana E., Fiocchi C. Immune regulation by microvascular endothelial cells: directing innate and adaptive immunity, coagulation, and inflammation. J Immunol 2007, 178:6017-6022.
2. Swerlick R.A., Lawley T.J. Role of microvascular endothelial cells in inflammation. J Invest Dermatol 1993, 100:111S-115S.
3. Krishnaswamy G., Kelley J., Yerra L., Smith J.K., Chi D.S. Human endothelium as a source of multifunctional cytokines: molecular regulation and possible role in human disease. J Interferon Cytokine Res 1999, 19:91-104.
4. Goebeler M., Yoshimura T., Toksoy A., Ritter U., Brocker E.B., Gillitzer R. The chemokine repertoire of human dermal microvascular endothelial cells and its regulation by inflammatory cytokines. J Invest Dermatol 1997, 108:445-451.
5. Xu Y., Swerlick R.A., Sepp N., Bosse D., Ades E.W., Lawley T.J. Characterization of expression and modulation of cell adhesion molecules on an immortalized human dermal microvascular endothelial cell line (HMEC-1). J Invest Dermatol 1994, 102:833-837.
6. Lidington E.A., Moyes D.L., McCormack A.M., Rose M.L. A comparison of primary endothelial cells and endothelial cell lines for studies of immune interactions. Transpl Immunol 1999, 7:239-246.
7. Johnston B., Butcher E.C. Chemokines in rapid leukocyte adhesion triggering and migration. Semin Immunol 2002, 14:83-92.
8. Sternberg E.M. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat Rev Immunol 2006, 6:318-328.
9. Elenkov I.J. Neurohormonal-cytokine interactions: implications for inflammation, common human diseases and well-being. Neurochem Int 2008, 52:40-51.
10. Bellinger D.L., Millar B.A., Perez S., Carter J., Wood C., ThyagaRajan S., et al. Sympathetic modulation of immunity: relevance to disease. Cell Immunol 2008, 252:27-56.
11. Elenkov I.J., Wilder R.L., Chrousos G.P., Vizi E.S. The sympathetic nerve-an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 2000, 52:595-638.
12. Dhabhar F.S. Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection versus immunopathology. Allergy Asthma Clin Immunol 2008, 4:2-11.
13. Dhabhar F.S. Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. Neuroimmunomodulation 2009, 16:300-317.
14. Costa-Pinto F.A., Palermo-Neto J. Neuroimmune interactions in stress. Neuroimmunomodulation 2010, 17:196-199.
15. Nance D.M., Sanders V.M. Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav Immun 2007, 21:736-745.
16. Chrousos G.P. Stress and disorders of the stress system. Nat Rev Endocrinol 2009, 5:374-381.
17. Liezmann C., Klapp B., Peters E.M. Stress, atopy and allergy: a re-evaluation from a psychoneuroimmunologic persepective. Dermatoendocrinol 2011, 3:37-40.
18. Kimyai-Asadi A., Usman A. The role of psychological stress in skin disease. J Cutan Med Surg 2001, 5:140-145.
19. Slominski A., Wortsman J., Paus R., Elias P.M., Tobin D.J., Feingold K.R. Skin as an endocrine organ: implications for its function. Drug Discov Today Dis Mech 2008, 5:137-144.
20. Hall J.M., Cruser D., Podawiltz A., Mummert D.I., Jones H., Mummert M.E. Psychological stress and the cutaneous immune response: roles of the HPA axis and the sympathetic nervous system in atopic dermatitis and psoriasis. Dermatol Res Pract 2012, 2012:403908.
21. Felten D.L., Felten S.Y., Carlson S.L., Olschowka J.A., Livnat S. Noradrenergic and peptidergic innervation of lymphoid tissue. J Immunol 1985, 135:755s-765s.
22. Felten S.Y., Felten D.L., Bellinger D.L., Carlson S.L., Ackerman K.D., Madden K.S., et al. Noradrenergic sympathetic innervation of lymphoid organs. Prog Allergy 1988, 43:14-36.
23. Felten S.Y., Madden K.S., Bellinger D.L., Kruszewska B., Moynihan J.A., Felten D.L. The role of the sympathetic nervous system in the modulation of immune responses. Adv Pharmacol 1998, 42:583-587.
24. Madden K.S., Felten S.Y., Felten D.L., Hardy C.A., Livnat S. Sympathetic nervous system modulation of the immune system. II. Induction of lymphocyte proliferation and migration in vivo by chemical sympathectomy. J Neuroimmunol 1994, 49:67-75.
25. Madden K.S. Catecholamines, sympathetic innervation, and immunity. Brain Behav Immun 2003, 17(Suppl 1):S5-S10.
26. Szelenyi J., Vizi E.S. The catecholamine cytokine balance: interaction between the brain and the immune system. Ann NY Acad Sci 2007, 1113:311-324.
27. Pavlovsky L., Friedman A. Pathogenesis of stress-associated skin disorders: exploring the brain-skin axis. Curr Probl Dermatol 2007, 35:136-145.
28. Pavlovic S., Daniltchenko M., Tobin D.J., Hagen E., Hunt S.P., Klapp B.F., et al. Further exploring the brain-skin connection: stress worsens dermatitis via substance P-dependent neurogenic inflammation in mice. J Invest Dermatol 2008, 128:434-446.
29. Fortune D.G., Richards H.L., Griffiths C.E. Psychologic factors in psoriasis: consequences, mechanisms, and interventions. Dermatol Clin 2005, 23:681-694.
30. Arndt J., Smith N., Tausk F. Stress and atopic dermatitis. Curr Allergy Asthma Rep 2008, 8:312-317.
31. Reich A., Wojcik-Maciejewicz A., Slominski A.T. Stress and the skin. G Ital Dermatol Venereol 2010, 145:213-219.
32. Paus R., Theoharides T.C., Arck P.C. Neuroimmunoendocrine circuitry of the 'brain-skin connection'. Trends Immunol 2006, 27:32-39.
33. Arck P.C., Slominski A., Theoharides T.C., Peters E.M., Paus R. Neuroimmunology of stress: skin takes center stage. J Invest Dermatol 2006, 126:1697-1704.
34. Seiffert K., Granstein R.D. Neuroendocrine regulation of skin dendritic cells. Ann NY Acad Sci 2006, 1088:195-206.
35. Tausk F., Christian E., Johansson O., Milgram S. Neurobiology of the skin. Dermatology in General Medicine 1993, 396-406. McGraw-Hill, New York. 4th ed. T.B. Fitzpatrick, K. Wolff, I.M. Freedberg, K.F. Austen (Eds.).
36. Matze D. Neuroanatomy of the skin. Neuroimmunology of the skin 2009, 3-12. Springer-Verlag, Berlin. R.D. Granstein, T.A. Luger (Eds.).
37. Graf K., Grafe M., Dummler U., O'Connor A., Regitz-Zagrosek V., Kunkel G., et al. Regulation of beta-adrenergic receptors on endothelial cells in culture. Eur Heart J 1993, 14(Suppl. I):173-176.
38. Howell R.E., Albelda S.M., Daise M.L., Levine E.M. Characterization of beta-adrenergic receptors in cultured human and bovine endothelial cells. J Appl Physiol 1988, 65:1251-1257.
39. Steinkraus V., Steinfath M., Korner C., Mensing H. Binding of beta-adrenergic receptors in human skin. J Invest Dermatol 1992, 98:475-480.
40. Sivamani R.K., Lam S.T., Isseroff R.R. Beta adrenergic receptors in keratinocytes. Dermatol Clin 2007, 25:643-653.
41. McSwigan J.D., Hanson D.R., Lubiniecki A., Heston L.L., Sheppard J.R. Down syndrome fibroblasts are hyperresponsive to beta-adrenergic stimulation. Proc Natl Acad Sci USA 1981, 78:7670-7673.
42. Gillbro J.M., Marles L.K., Hibberts N.A., Schallreuter K.U. Autocrine catecholamine biosynthesis and the beta-adrenoceptor signal promote pigmentation in human epidermal melanocytes. J Invest Dermatol 2004, 123:346-353.
43. Muskhelishvili L.V., Gedevanishvili M.D. Adrenergic receptors in murine epidermis. Tsitologiia 1976, 18:627-629.
44. Drummond P.D., Skipworth S., Finch P.M. Alpha 1-adrenoceptors in normal and hyperalgesic human skin. Clin Sci (Lond) 1996, 91:73-77.
45. Gornikiewicz A., Sautner T., Brostjan C., Schmierer B., Fugger R., Roth E., et al. Catecholamines up-regulate lipopolysaccharide-induced IL-6 production in human microvascular endothelial cells. Faseb J 2000, 14:1093-1100.
46. Burnstock G., Fredholm B.B., North R.A., Verkhratsky A. The birth and postnatal development of purinergic signalling. Acta Physiol (Oxf) 2010, 199:93-147.
47. Burnstock G., Kennedy C. P2X receptors in health and disease. Adv Pharmacol 2011, 61:333-372.
48. Hasko G., Szabo C. Regulation of cytokine and chemokine production by transmitters and co-transmitters of the autonomic nervous system. Biochem Pharmacol 1998, 56:1079-1087.
49. Burnstock G. Purinergic cotransmission. Exp Physio 2009, 94:20-24.
50. Burnstock G. Purinergic cotransmission. F1000 Biol Rep 2009, 1:46.
51. Ralevic V., Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev 1998, 50:413-492.
52. Burnstock G. Purinergic signalling: past, present and future. Braz J Med Biol Res 2009, 42:3-8.
53. Ohman J., Erlinge D. The touching story of purinergic signaling in epithelial and endothelial cells. Purinergic Signal 2012, 8:599-608.
54. Seiffert K., Ding W., Wagner J.A., Granstein R.D. ATPgammaS enhances the production of inflammatory mediators by a human dermal endothelial cell line via purinergic receptor signaling. J Invest Dermatol 2006, 126:1017-1027.
55. Bender A., Zapolanski T., Watkins S., Khosraviani A., Seiffert K., Ding W., et al. Tetracycline suppresses ATP gamma S-induced CXCL8 and CXCL1 production by the human dermal microvascular endothelial cell-1 (HMEC-1) cell line and primary human dermal microvascular endothelial cells. Exp Dermatol 2008, 17:752-760.
56. von Patay B., Kurz B., Mentlein R. Effect of transmitters and co-transmitters of the sympathetic nervous system on interleukin-6 synthesis in thymic epithelial cells. Neuroimmunomodulation 1999, 6:45-50.
57. Korn T., Mitsdoerffer M., Croxford A.L., Awasthi A., Dardalhon V.A., Galileos G., et al. IL-6 controls Th17 immunity in vivo by inhibiting the conversion of conventional T cells into Foxp3+ regulatory T cells. Proc Natl Acad Sci USA 2008, 105:18460-18465.
58. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 Cells. Annu Rev Immunol 2009, 27:485-517.
59. Zhou L., Ivanov I.I., Spolski R., Min R., Shenderov K., Egawa T., et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007, 8:967-974.
60. Goodman W.A., Levine A.D., Massari J.V., Sugiyama H., McCormick T.S., Cooper K.D. IL-6 signaling in psoriasis prevents immune suppression by regulatory T cells. J Immunol 2009, 183:3170-3176.
61. Kimura A., Kishimoto T. IL-6: regulator of Treg/Th17 balance. Eur J Immunol 2010, 40:1830-1835.
62. Benwell R.K., Lee D.R. Essential and synergistic roles of IL1 and IL6 in human Th17 differentiation directed by TLR ligand-activated dendritic cells. Clin Immunol 2010, 134:178-187.
63. Maddur M.S., Miossec P., Kaveri S.V., Bayry J. Th17 cells: biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies. Am J Pathol 2012, 181:8-18.
64. Di Cesare A., Di Meglio P., Nestle F.O. The IL-23/Th17 axis in the immunopathogenesis of psoriasis. J Invest Dermatol 2009, 129:1339-1350.
65. Coimbra S., Figueiredo A., Castro E., Rocha-Pereira P., Santos-Silva A. The roles of cells and cytokines in the pathogenesis of psoriasis. Int J Dermatol 2012, 51:389-395.
66. Kagami S., Rizzo H.L., Lee J.J., Koguchi Y., Blauvelt A. Circulating Th17, Th22, and Th1 cells are increased in psoriasis. J Invest Dermatol 2010, 130:1373-1383.
67. Nograles K.E., Zaba L.C., Guttman-Yassky E., Fuentes-Duculan J., Suarez-Farinas M., Cardinale I., et al. Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways. Br J Dermatol 2008, 159:1092-1102.
68. Lowes M.A., Kikuchi T., Fuentes-Duculan J., Cardinale I., Zaba L.C., Haider A.S., et al. Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J Invest Dermatol 2008, 128:1207-1211.
69. Guttman-Yassky E., Nograles K.E., Krueger J.G. Contrasting pathogenesis of atopic dermatitis and psoriasis - part I: clinical and pathologic concepts. J Allergy Clin Immunol 2011, 127:1110-1118.
70. Guttman-Yassky E., Nograles K.E., Krueger J.G. Contrasting pathogenesis of atopic dermatitis and psoriasis - part II: immune cell subsets and therapeutic concepts. J Allergy Clin Immunol 2011, 127:1420-1432.
71. Raychaudhuri S.P. Role of IL-17 in psoriasis and psoriatic arthritis. Clin Rev Allergy Immunol 2013, 2:183-193.
72. Martin D.A., Towne J.E., Kricorian G., Klekotka P., Gudjonsson J.E., Krueger J.G., et al. The emerging role of IL-17 in the pathogenesis of psoriasis: preclinical and clinical findings. J Invest Dermatol 2013, 133:17-26.
73. Ades E.W., Candal F.J., Swerlick R.A., George V.G., Summers S., Bosse D.C., et al. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 1992, 99:683-690.
74. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
75. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108.
76. Hothorn T., Bretz F., Westfall P. Simultaneous inference in general parametric models. Biom J 2008, 50:346-363.
77. Tausk F., Elenkov I., Moynihan J. Psychoneuroimmunology. Dermatol Ther 2008, 21:22-31.
78. Schmid-Ott G., Jaeger B., Boehm T., Langer K., Stephan M., Raap U., et al. Immunological effects of stress in psoriasis. Br J Dermatol 2009, 160:782-785.
79. Suarez A.L., Feramisco J.D., Koo J., Steinhoff M. Psychoneuroimmunology of psychological stress and atopic dermatitis: pathophysiologic and therapeutic updates. Acta Derm Venereol 2012, 92:7-15.
80. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-238.
81. Hirano T. Interleukin 6 and its receptor: ten years later. Int Rev Immunol 1998, 16:249-284.
82. Hirano T. Interleukin 6 in autoimmune and inflammatory diseases: a personal memoir. Proc Jpn Acad Ser B Phys Biol Sci 2010, 86:717-730.
83. Kishimoto T. IL-6: from its discovery to clinical applications. Int Immunol 2010, 22:347-352.
84. Paquet P., Pierard G.E. Interleukin-6 and the skin. Int Arch Allergy Immunol 1996, 109:308-317.
85. Tesmer L.A., Lundy S.K., Sarkar S., Fox D.A. Th17 cells in human disease. Immunol Rev 2008, 223:87-113.
86. Oukka M. Th17 cells in immunity and autoimmunity. Ann Rheum Dis 2008, 67(Suppl. 3):iii26-iii29.
87. Annunziato F., Cosmi L., Liotta F., Maggi E., Romagnani S. The phenotype of human Th17 cells and their precursors, the cytokines that mediate their differentiation and the role of Th17 cells in inflammation. Int Immunol 2008, 20:1361-1368.
88. Annunziato F., Cosmi L., Liotta F., Maggi E., Romagnani S. Type 17 T helper cells-origins, features and possible roles in rheumatic disease. Nat Rev Rheumatol 2009, 5:325-331.
89. Zheng Y., Danilenko D.M., Valdez P., Kasman I., Eastham-Anderson J., Wu J., et al. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 2007, 445:648-651.
90. Boniface K., Guignouard E., Pedretti N., Garcia M., Delwail A., Bernard F.X., et al. A role for T cell-derived interleukin 22 in psoriatic skin inflammation. Clin Exp Immunol 2007, 150:407-415.
91. Korn T., Bettelli E., Gao W., Awasthi A., Jager A., Strom T.B., et al. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 2007, 448:484-487.
92. Yang L., Anderson D.E., Baecher-Allan C., Hastings W.D., Bettelli E., Oukka M., et al. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 2008, 454:350-352.
93. Neuner P., Urbanski A., Trautinger F., Moller A., Kirnbauer R., Kapp A., et al. Increased IL-6 production by monocytes and keratinocytes in patients with psoriasis. J Invest Dermatol 1991, 97:27-33.
94. Grossman R.M., Krueger J., Yourish D., Granelli-Piperno A., Murphy D.P., May L.T., et al. Interleukin 6 is expressed in high levels in psoriatic skin and stimulates proliferation of cultured human keratinocytes. Proc Natl Acad Sci USA 1989, 86:6367-6371.
95. Killeen M.E., Ferris L., Kupetsky E.A., Falo L., Mathers A.R. Signaling through purinergic receptors for ATP induces human cutaneous innate and adaptive Th17 responses: implications in the pathogenesis of psoriasis. J Immunol 2013, 190:4324-4336.
96. Ding Y., Gao Z.G., Jacobson K.A., Suffredini A.F. Dexamethasone enhances ATP-induced inflammatory responses in endothelial cells. J Pharmacol Exp Ther 2010, 335:693-702.
97. Basavaraj K.H., Ashok N.M., Rashmi R., Praveen T.K. The role of drugs in the induction and/or exacerbation of psoriasis. Int J Dermatol 2010, 49:1351-1361.
98. Brauchli Y.B., Jick S.S., Curtin F., Meier C.R. Association between beta-blockers, other antihypertensive drugs and psoriasis: population-based case-control study. Br J Dermatol 2008, 158:1299-1307.
99. D'Incan M., Fabricio L., Souteyrand P. Ritodrine-induced pustular eruption in a pregnant woman with psoriasis. J Eur Acad Dermatol Venereol 1998, 11:91-93.
100. Kuwabara Y., Sato A., Abe H., Abe S., Kawai N., Takeshita T. Ritodrine-induced pustular eruptions distinctly resembling impetigo herpetiformis. J Nippon Med Sch 2011, 78:329-333.