STAT3: An important regulator of multiple cytokine functions

Transplantation

Volumn 85, Issue 10, 2008, Pages 1372-1377

  Stepkowski, Stanislaw M ^a   Chen, Wenhao ^a   Ross, Jeremy A ^b   Nagy, Zsuzsanna S ^b   Kirken, Robert A ^b  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

Dendritic cell; STAT3; Th17

Indexed keywords

CYTOKINE; CYTOKINE RECEPTOR; INTERLEUKIN 6; JANUS KINASE; STAT3 PROTEIN; STAT3 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DENDRITIC CELL; GENE MUTATION; HUMAN; HYPER IGE SYNDROME; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH17 CELL; GENETICS; HISTOCOMPATIBILITY; HOMEOSTASIS; IMMUNOLOGICAL TOLERANCE; MUTATION; NEOPLASM; PATHOPHYSIOLOGY; PHYSIOLOGY;

CYTOKINES; HOMEOSTASIS; HUMANS; IMMUNE TOLERANCE; JOB'S SYNDROME; MUTATION; NEOPLASMS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSPLANTATION IMMUNOLOGY;

EID: 48649091348     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/TP.0b013e3181739d25     Document Type: Review

References (77)

1. Battle TE, Frank DA. The role of STATs in apoptosis. Curr Mol Med 2002; 2: 381.
2. Darnell JE Jr. STATs and gene regulation. Science 1997; 277: 1630.
3. Leonard WJ, O'Shea JJ. Jaks and STATs: Biological implications. Annu Rev Immunol 1998; 16: 293.
4. Stepkowski SM, Kirken RA. Janus tyrosine kinases and signal transducers and activators of transcription regulate critical functions of T cells in allograft rejection and transplantation tolerance. Transplantation 2006; 82: 295.
5. Ihle JN, Witthuhn BA, Quelle FW, et al. Signaling through the hematopoietic cytokine receptors. Annu Rev Immunol 1995; 13: 369.
6. Zhang Y, Turkson J, Carter-Su C, et al. Activation of Stat3 in v-Srctransformed fibroblasts requires cooperation of Jak1 kinase activity. J Biol Chem 2000; 275: 24935.
7. Turkson J, Bowman T, Adnane J, et al. Requirement for Ras/Rac1- mediated p38 and c-Jun N-terminal kinase signaling in Stat3 transcriptional activity induced by the Src oncoprotein. Mol Cell Biol 1999; 19: 7519.
8. Zhang X, Blenis J, Li HC, et al. Requirement of serine phosphorylation for formation of STAT-promoter complexes. Science 1995; 267: 1990.
9. Yang J, Chatterjee-Kishore M, Staugaitis SM, et al. Novel roles of unphosphorylated STAT3 in oncogenesis and transcriptional regulation. Cancer Res 2005; 65: 939.
10. Takeda K, Noguchi K, Shi W, et al. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci USA 1997; 94: 3801.
11. Takeda K, Kaisho T, Yoshida N, et al. Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: Generation and characterization of T cell-specific Stat3-deficient mice. J Immunol 1998; 161: 4652.
12. Boutin Y, Leitenberg D, Tao X, et al. Distinct biochemical signals characterize agonist- and altered peptide ligand-induced differentiation of naive CD4- T cells into Th1 and Th2 subsets. J Immunol 1997; 159: 5802.
13. Kuo CT, Leiden JM. Transcriptional regulation of T lymphocyte development and function. Annu Rev Immunol 1999; 17: 149.
14. Pflanz S, Timans JC, Cheung J, et al. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(-) T cells. Immunity 2002; 16: 779.
15. Appleman LJ, Boussiotis VA. T cell anergy and costimulation. Immunol Rev 2003; 192: 161.
16. Leonard WJ. STA. Ts and cytokine specificity. Nat Med 1996; 2: 968.
17. Nelson BH, Willerford DM. Biology of the interleukin-2 receptor. Adv Immunol 1998; 70: 1.
18. Stahl N, Boulton TG, Farruggella T, et al. Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 beta receptor components. Science 1994; 263: 92.
19. Van SJ. Interleukin-6: An overview. Annu Rev Immunol 1990; 8: 253.
20. Murakami M, Hibi M, Nakagawa N, et al. IL-6-induced homodimerization of gp130 and associated activation of a tyrosine kinase. Science 1993; 260: 1808.
21. Stahl N, Farruggella TJ, Boulton TG, et al. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 1995; 267: 1349.
22. Schindler C, Darnell JE Jr. Transcriptional responses to polypeptide ligands: The JAK-STAT pathway. Annu Rev Biochem 1995; 64: 621.
23. Becker S, Groner B, Muller CW. Three-dimensional structure of the Stat3beta homodimer bound to DNA. Nature 1998; 394: 145.
24. Krebs A, Kuchumov AR, Sharma PK, et al. Molecular shape, dissociation, and oxygen binding of the dodecamer subunit of Lumbricus terrestris hemoglobin. J Biol Chem 1996; 271: 18695.
25. Taga K, Mostowski H, Tosato G. Human interleukin-10 can directly inhibit T-cell growth. Blood 1993; 81: 2964.
26. Mosmann TR. Regulation of immune responses by T cells with different cytokine secretion phenotypes: Role of a new cytokine, cytokine synthesis inhibitory factor (IL10). Int Arch Allergy Appl Immunol 1991; 94: 110.
27. Wen Z, Zhong Z, Darnell JE Jr. Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 1995; 82: 241.
28. Ng J, Cantrell D. STAT3 is a serine kinase target in T lymphocytes. Interleukin 2 and T cell antigen receptor signals converge upon serine 727. J Biol Chem 1997; 272: 24542.
29. Lafont V, Decker T, Cantrell D. Antigen receptor signal transduction: Activating and inhibitory antigen receptors regulate STAT1 serine phosphorylation. Eur J Immunol 2000; 30: 1851.
30. Winston LA, Hunter T. Intracellular signalling: Putting JAKs on the kinase MAP. Curr Biol 1996; 6: 668.
31. David M, Petricoin E III, Benjamin C, et al. Requirement for MAP kinase (ERK2) activity in interferon alpha- and interferon beta-stimulated gene expression through STAT proteins. Science 1995; 269: 1721.
32. Chung J, Uchida E, Grammer TC, et al. STAT3 serine phosphorylation by ERK-dependent and -independent pathways negatively modulates its tyrosine phosphorylation. Mol Cell Biol 1997; 17: 6508.
33. Kuroki M, O'Flaherty JT. Extracellular signal-regulated protein kinase (ERK)-dependent and ERK-independent pathways target STAT3 on serine-727 in human neutrophils stimulated by chemotactic factors and cytokines. Biochem J 1999; 341(Pt 3): 691.
34. McLoughlin RM, Jenkins BJ, Grail D, et al. IL-6 trans-signaling via STAT3 directs T cell infiltration in acute inflammation. Proc Natl Acad Sci USA 2005; 102: 9589.
35. Grimbacher B, Holland SM, Puck JM. Hyper-IgE syndromes. Immunol Rev 2005; 203: 244.
36. Minegishi Y, Saito M, Tsuchiya S, et al. Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature 2007; 448: 1058.
37. Holland SM, DeLeo FR, Elloumi HZ, et al. STAT3 mutations in the hyper-IgE syndrome. N Engl J Med 2007; 357: 1608.
38. Catlett-Falcone R, Landowski TH, Oshiro MM, et al. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999; 10: 105.
39. Grandis JR, Drenning SD, Chakraborty A, et al. Requirement of Stat3 but not Stat1 activation for epidermal growth factor receptor- mediated cell growth In vitro. J Clin Invest 1998; 102: 1385.
40. Bromberg JF, Wrzeszczynska MH, Devgan G, et al. Stat3 as an oncogene. Cell 1999; 98: 295.
41. Nagy ZS, Rui H, Stepkowski SM, et al. A preferential role for STAT5, not constitutively active STAT3, in promoting survival of a human lymphoid tumor. J Immunol 2006; 177: 5032.
42. Hussain SF, Kong LY, Jordan J, et al. A novel small molecule inhibitor of signal transducers and activators of transcription 3 reverses immune tolerance in malignant glioma patients. Cancer Res 2007; 67: 9630.
43. Laurence A, O'Shea JJ. T(H)-17 differentiation of mice and men. Nat Immunol 2007; 8: 903.
44. Maynard CL, Harrington LE, Janowski KM, et al. Regulatory T cells expressing interleukin 10 develop from Foxp3- and Foxp3- precursor cells in the absence of interleukin 10. Nat Immunol 2007; 8: 931.
45. Mathur AN, Chang HC, Zisoulis DG, et al. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J Immunol 2007; 178: 4901.
46. Yang XO, Pappu BP, Nurieva R, et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 2008; 28: 29.
47. Bettelli E, Korn T, Kuchroo VK. Th17: The third member of the effector T cell trilogy. Curr Opin Immunol 2007; 19: 652.
48. Ross JA, Nagy ZS, Cheng H, et al. Regulation of T cell homeostasis by JAKs and STATs. Arch Immunol Ther Exp (Warsz) 2007; 55: 231.
49. Yao Z, Kanno Y, Kerenyi M, et al. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood 2007; 109: 4368.
50. Murphy KM, Reiner SL. The lineage decisions of helper T cells. Nat Rev Immunol 2002; 2: 933.
51. Wilson NJ, Boniface K, Chan JR, et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 2007; 8: 950.
52. Xu J, Drew PD. Peroxisome proliferator-activated receptor-gamma agonists suppress the production of IL-12 family cytokines by activated glia. J Immunol 2007; 178: 1904.
53. Madi-Obi A, Yu CR, Liu X, et al. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat Med 2007; 13: 711.
54. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity 2004; 21: 467.
55. Ye P, Rodriguez FH, Kanaly S, et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colonystimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001; 194: 519.
56. Huang W, Na L, Fidel PL, et al. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 2004; 190: 624.
57. Cua DJ, Sherlock J, Chen Y, et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003; 421: 744.
58. Murphy CA, Langrish CL, Chen Y, et al. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003; 198: 1951.
59. Cheng F, Wang HW, Cuenca A, et al. A critical role for Stat3 signaling in immune tolerance. Immunity 2003; 19: 425.
60. Gabrilovich D. Mechanisms and functional significance of tumourinduced dendritic-cell defects. Nat Rev Immunol 2004; 4: 941.
61. Stepkowski SM, Phan T, Zhang H, et al. Immature syngeneic dendritic cells potentiate tolerance to pancreatic islet allografts depleted of donor dendritic cells in microgravity culture condition. Transplantation 2006; 82: 1756.
62. Chaput N, Rrasse-Jeze G, Bergot AS, et al. Regulatory T cells prevent CD8 T cell maturation by inhibiting CD4 Th cells at tumor sites. J Immunol 2007; 179: 4969.
63. Barton BE. STAT3: A potential therapeutic target in dendritic cells for the induction of transplant tolerance. Expert Opin Ther Targets 2006; 10: 459.
64. Park SJ, Nakagawa T, Kitamura H, et al. IL-6 regulates in vivo dendritic cell differentiation through STAT3 activation. J Immunol 2004; 173: 3844.
65. Orabona C, Belladonna ML, Vacca C, et al. Cutting edge: Silencing suppressor of cytokine signaling 3 expression in dendritic cells turns CD28-Ig from immune adjuvant to suppressant. J Immunol 2005; 174: 6582.
66. Munn DH, Sharma MD, Lee JR, et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 2002; 297: 1867.
67. Kortylewski M, Kujawski M, Wang T, et al. Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat Med 2005; 11: 1314.
68. Bettelli E, Carrier Y, Gao W, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441: 235.
69. Carrier Y, Yuan J, Kuchroo VK, et al. Th3 cells in peripheral tolerance. I. Induction of Foxp3-positive regulatory T cells by Th3 cells derived from TGF-beta T cell-transgenic mice. J Immunol 2007; 178: 179.
70. Chen X, Vodanovic-Jankovic S, Johnson B, et al. Absence of regulatory T-cell control of TH1 and TH17 cells is responsible for the autoimmunemediated pathology in chronic graft-versus-host disease. Blood 2007; 110: 3804.
71. Xu L, Kitani A, Fuss I, et al. Cutting edge: Regulatory T cells induce CD4-CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol 2007; 178: 6725.
72. Lutticken C, Wegenka UM, Yuan J, et al. Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science 1994; 263: 89.
73. Alonzi T, Maritano D, Gorgoni B, et al. Essential role of STAT3 in the control of the acute-phase response as revealed by inducible gene inactivation [correction of activation] in the liver. Mol Cell Biol 2001; 21: 1621.
74. Debonera F, Aldeguer X, Shen X, et al. Activation of interleukin-6/ STAT3 and liver regeneration following transplantation. J Surg Res 2001; 96: 289.
75. Selzner N, Selzner M, Tian Y, et al. Cold ischemia decreases liver regeneration after partial liver transplantation in the rat: A TNF-alpha/IL-6- dependent mechanism. Hepatology 2002; 36: 812.
76. Guo L, Haga S, Enosawa S, et al. Improved hepatic regeneration with reduced injury by redox factor-1 in a rat small-sized liver transplant model. Am J Transplant 2004; 4: 879.
77. Bobadilla JL, Love RB, Jankowska-Gan E, et al. TH-17, monokines, collagen type V, and primary graft dysfunction in lung transplantation. Am J Respir Crit Care Med 2008; Epub ahead of print.