A critical role for STAT3 transcription factor signaling in the development and maintenance of human T cell memory

Immunity

Volumn 35, Issue 5, 2011, Pages 806-818

  Siegel, Andrea M ^a   Heimall, Jennifer ^a,c   Freeman, Alexandra F ^a   Hsu, Amy P ^a   Brittain, Erica ^a   Brenchley, Jason M ^a   Douek, Daniel C ^a   Fahle, Gary H ^b   Cohen, Jeffrey I ^a   Holland, Steven M ^a   Milner, Joshua D ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BCL 6; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ADOLESCENT; ADULT; ARTICLE; AUTOSOMAL DOMINANT DISORDER; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; EPSTEIN BARR VIRUS; FEMALE; HUMAN; HUMAN CELL; HYPER IGE SYNDROME; IMMUNOPHENOTYPING; IN VITRO STUDY; MALE; MEMORY T LYMPHOCYTE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHOOL CHILD; SIGNAL TRANSDUCTION; VARICELLA ZOSTER VIRUS; VIRUS LATENCY;

ADOLESCENT; ADULT; APOPTOSIS; BASE SEQUENCE; CHILD; CHILD, PRESCHOOL; EPSTEIN-BARR VIRUS INFECTIONS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HERPESVIRUS 3, HUMAN; HUMANS; IMMUNOLOGIC MEMORY; JOB'S SYNDROME; MALE; MIDDLE AGED; MUTATION; PHENOTYPE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES; YOUNG ADULT;

EID: 82055163110     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.09.016     Document Type: Article

References (63)

1. Akaishi H., Takeda K., Kaisho T., Shineha R., Satomi S., Takeda J., Akira S. Defective IL-2-mediated IL-2 receptor alpha chain expression in Stat3-deficient T lymphocytes. Int. Immunol. 1998, 10:1747-1751.
2. Avery D.T., Deenick E.K., Ma C.S., Suryani S., Simpson N., Chew G.Y., Chan T.D., Palendira U., Bustamante J., Boisson-Dupuis S., et al. B cell-intrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans. J. Exp. Med. 2010, 207:155-171.
3. Bromberg J.F., Wrzeszczynska M.H., Devgan G., Zhao Y., Pestell R.G., Albanese C., Darnell J.E. Stat3 as an oncogene. Cell 1999, 98:295-303.
4. Buckley R.H., Schiff S.E., Hayward A.R. Reduced frequency of CD45RO+ T lymphocytes in blood of hyper-IgE syndrome patients. J. Allergy Clin. Immunol. 1991, 87:313.
5. Burke B.L., Steele R.W., Beard O.W., Wood J.S., Cain T.D., Marmer D.J. Immune responses to varicella-zoster in the aged. Arch. Intern. Med. 1982, 142:291-293.
6. Carrio R., Bathe O.F., Malek T.R. Initial antigen encounter programs CD8+ T cells competent to develop into memory cells that are activated in an antigen-free, IL-7- and IL-15-rich environment. J. Immunol. 2004, 172:7315-7323.
7. Cohen J.I., Fahle G., Kemp M.A., Apakupakul K., Margolis T.P. Human herpesvirus 6-A, 6-B, and 7 in vitreous fluid samples. J. Med. Virol. 2010, 82:996-999.
8. Conti H.R., Shen F., Nayyar N., Stocum E., Sun J.N., Lindemann M.J., Ho A.W., Hai J.H., Yu J.J., Jung J.W., et al. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J. Exp. Med. 2009, 206:299-311.
9. Cui W., Kaech S.M. Generation of effector CD8+ T cells and their conversion to memory T cells. Immunol. Rev. 2010, 236:151-166.
10. + T cells. Immunity 2011, 35:792-805. this issue.
11. de Beaucoudrey L., Puel A., Filipe-Santos O., Cobat A., Ghandil P., Chrabieh M., Feinberg J., von Bernuth H., Samarina A., Jannière L., et al. Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing T cells. J. Exp. Med. 2008, 205:1543-1550.
12. Donabedian H., Gallin J.I. The hyperimmunoglobulin E recurrent-infection (Job's) syndrome. A review of the NIH experience and the literature. Medicine (Baltimore) 1983, 62:195-208.
13. Donahue J.G., Choo P.W., Manson J.E., Platt R. The incidence of herpes zoster. Arch. Intern. Med. 1995, 155:1605-1609.
14. Douek D.C., Vescio R.A., Betts M.R., Brenchley J.M., Hill B.J., Zhang L., Berenson J.R., Collins R.H., Koup R.A. Assessment of thymic output in adults after haematopoietic stem-cell transplantation and prediction of T-cell reconstitution. Lancet 2000, 355:1875-1881.
15. Durant L., Watford W.T., Ramos H.L., Laurence A., Vahedi G., Wei L., Takahashi H., Sun H.W., Kanno Y., Powrie F., O'Shea J.J. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 2010, 32:605-615.
16. Eddahri F., Denanglaire S., Bureau F., Spolski R., Leonard W.J., Leo O., Andris F. Interleukin-6/STAT3 signaling regulates the ability of naive T cells to acquire B-cell help capacities. Blood 2009, 113:2426-2433.
17. Elsaesser H., Sauer K., Brooks D.G. IL-21 is required to control chronic viral infection. Science 2009, 324:1569-1572.
18. Faulkner G.C., Burrows S.R., Khanna R., Moss D.J., Bird A.G., Crawford D.H. X-Linked agammaglobulinemia patients are not infected with Epstein-Barr virus: implications for the biology of the virus. J. Virol. 1999, 73:1555-1564.
19. Feng W.H., Cohen J.I., Fischer S., Li L., Sneller M., Goldbach-Mansky R., Raab-Traub N., Delecluse H.J., Kenney S.C. Reactivation of latent Epstein-Barr virus by methotrexate: a potential contributor to methotrexate-associated lymphomas. J. Natl. Cancer Inst. 2004, 96:1691-1702.
20. Ferwerda B., Ferwerda G., Plantinga T.S., Willment J.A., van Spriel A.B., Venselaar H., Elbers C.C., Johnson M.D., Cambi A., Huysamen C., et al. Human dectin-1 deficiency and mucocutaneous fungal infections. N. Engl. J. Med. 2009, 361:1760-1767.
21. Foulds K.E., Rotte M.J., Seder R.A. IL-10 is required for optimal CD8 T cell memory following Listeria monocytogenes infection. J. Immunol. 2006, 177:2565-2574.
22. Freeman A.F., Holland S.M. Clinical manifestations of hyper IgE syndromes. Dis. Markers 2010, 29:123-130.
23. Fröhlich A., Kisielow J., Schmitz I., Freigang S., Shamshiev A.T., Weber J., Marsland B.J., Oxenius A., Kopf M. IL-21R on T cells is critical for sustained functionality and control of chronic viral infection. Science 2009, 324:1576-1580.
24. Glocker E.O., Hennigs A., Nabavi M., Schäffer A.A., Woellner C., Salzer U., Pfeifer D., Veelken H., Warnatz K., Tahami F., et al. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N. Engl. J. Med. 2009, 361:1727-1735.
25. Grimbacher B., Schäffer A.A., Holland S.M., Davis J., Gallin J.I., Malech H.L., Atkinson T.P., Belohradsky B.H., Buckley R.H., Cossu F., et al. Genetic linkage of hyper-IgE syndrome to chromosome 4. Am. J. Hum. Genet. 1999, 65:735-744.
26. Heimall J., Davis J., Shaw P.A., Hsu A.P., Gu W., Welch P., Holland S.M., Freeman A.F. Paucity of genotype-phenotype correlations in STAT3 mutation positive Hyper IgE Syndrome (HIES). Clin. Immunol. 2011, 139:75-84.
27. Holland S.M., DeLeo F.R., Elloumi H.Z., Hsu A.P., Uzel G., Brodsky N., Freeman A.F., Demidowich A., Davis J., Turner M.L., et al. STAT3 mutations in the hyper-IgE syndrome. N. Engl. J. Med. 2007, 357:1608-1619.
28. Hope-Simpson R.E. Postherpetic neuralgia. J. R. Coll. Gen. Pract. 1975, 25:571-575.
29. Ichii H., Sakamoto A., Hatano M., Okada S., Toyama H., Taki S., Arima M., Kuroda Y., Tokuhisa T. Role for Bcl-6 in the generation and maintenance of memory CD8+ T cells. Nat. Immunol. 2002, 3:558-563.
30. Ichii H., Sakamoto A., Kuroda Y., Tokuhisa T. Bcl6 acts as an amplifier for the generation and proliferative capacity of central memory CD8+ T cells. J. Immunol. 2004, 173:883-891.
31. Kaech S.M., Tan J.T., Wherry E.J., Konieczny B.T., Surh C.D., Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 2003, 4:1191-1198.
32. Kallies A., Xin A., Belz G.T., Nutt S.L. Blimp-1 transcription factor is required for the differentiation of effector CD8(+) T cells and memory responses. Immunity 2009, 31:283-295.
33. Kimmig S., Przybylski G.K., Schmidt C.A., Laurisch K., Möwes B., Radbruch A., Thiel A. Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J. Exp. Med. 2002, 195:789-794.
34. Klebanoff C.A., Gattinoni L., Torabi-Parizi P., Kerstann K., Cardones A.R., Finkelstein S.E., Palmer D.C., Antony P.A., Hwang S.T., Rosenberg S.A., et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc. Natl. Acad. Sci. USA 2005, 102:9571-9576.
35. Kost R.G., Straus S.E. Postherpetic neuralgia-pathogenesis, treatment, and prevention. N. Engl. J. Med. 1996, 335:32-42.
36. Ku C.C., Murakami M., Sakamoto A., Kappler J., Marrack P. Control of homeostasis of CD8+ memory T cells by opposing cytokines. Science 2000, 288:675-678.
37. Kumánovics A., Perkins S.L., Gilbert H., Cessna M.H., Augustine N.H., Hill H.R. Diffuse large B cell lymphoma in hyper-IgE syndrome due to STAT3 mutation. J. Clin. Immunol. 2010, 30:886-893.
38. Levy D.E., Lee C.K. What does Stat3 do?. J. Clin. Invest. 2002, 109:1143-1148.
39. Liu H., Rohowsky-Kochan C. Interleukin-27-mediated suppression of human Th17 cells is associated with activation of STAT1 and suppressor of cytokine signaling protein 1. J. Interferon Cytokine Res. 2011, 31:459-469.
40. Ma C.S., Chew G.Y., Simpson N., Priyadarshi A., Wong M., Grimbacher B., Fulcher D.A., Tangye S.G., Cook M.C. Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J. Exp. Med. 2008, 205:1551-1557.
41. Manjunath N., Shankar P., Wan J., Weninger W., Crowley M.A., Hieshima K., Springer T.A., Fan X., Shen H., Lieberman J., von Andrian U.H. Effector differentiation is not prerequisite for generation of memory cytotoxic T lymphocytes. J. Clin. Invest. 2001, 108:871-878.
42. Migone T.S., Lin J.X., Cereseto A., Mulloy J.C., O'Shea J.J., Franchini G., Leonard W.J. Constitutively activated Jak-STAT pathway in T cells transformed with HTLV-I. Science 1995, 269:79-81.
43. Milner J.D., Brenchley J.M., Laurence A., Freeman A.F., Hill B.J., Elias K.M., Kanno Y., Spalding C., Elloumi H.Z., Paulson M.L., et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 2008, 452:773-776.
44. Minegishi Y., Saito M., Tsuchiya S., Tsuge I., Takada H., Hara T., Kawamura N., Ariga T., Pasic S., Stojkovic O., et al. Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature 2007, 448:1058-1062.
45. Nurieva R.I., Chung Y., Hwang D., Yang X.O., Kang H.S., Ma L., Wang Y.H., Watowich S.S., Jetten A.M., Tian Q., Dong C. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 2008, 29:138-149.
46. Pellegrini M., Calzascia T., Toe J.G., Preston S.P., Lin A.E., Elford A.R., Shahinian A., Lang P.A., Lang K.S., Morre M., et al. IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 2011, 144:601-613.
47. Peschon J.J., Morrissey P.J., Grabstein K.H., Ramsdell F.J., Maraskovsky E., Gliniak B.C., Park L.S., Ziegler S.F., Williams D.E., Ware C.B., et al. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J. Exp. Med. 1994, 180:1955-1960.
48. Puel A., Cypowyj S., Bustamante J., Wright J.F., Liu L., Lim H.K., Migaud M., Israel L., Chrabieh M., Audry M., et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011, 332:65-68.
49. Renner E.D., Rylaarsdam S., Anover-Sombke S., Rack A.L., Reichenbach J., Carey J.C., Zhu Q., Jansson A.F., Barboza J., Schimke L.F., et al. Novel signal transducer and activator of transcription 3 (STAT3) mutations, reduced T(H)17 cell numbers, and variably defective STAT3 phosphorylation in hyper-IgE syndrome. J. Allergy Clin. Immunol. 2008, 122:181-187.
50. Rutishauser R.L., Martins G.A., Kalachikov S., Chandele A., Parish I.A., Meffre E., Jacob J., Calame K., Kaech S.M. Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 2009, 31:296-308.
51. Rystedt I., Strannegard I.L., Strannegard O. Recurrent viral infections in patients with past or present atopic dermatitis. Br. J. Dermatol. 1986, 114:575-582.
52. Sallusto F., Lanzavecchia A., Araki K., Ahmed R. From vaccines to memory and back. Immunity 2010, 33:451-463.
53. Scheinberg P., Melenhorst J.J., Brenchley J.M., Hill B.J., Hensel N.F., Chattopadhyay P.K., Roederer M., Picker L.J., Price D.A., Barrett A.J., Douek D.C. The transfer of adaptive immunity to CMV during hematopoietic stem cell transplantation is dependent on the specificity and phenotype of CMV-specific T cells in the donor. Blood 2009, 114:5071-5080.
54. Shin H., Blackburn S.D., Intlekofer A.M., Kao C., Angelosanto J.M., Reiner S.L., Wherry E.J. A role for the transcriptional repressor Blimp-1 in CD8(+) T cell exhaustion during chronic viral infection. Immunity 2009, 31:309-320.
55. Speckmann C., Enders A., Woellner C., Thiel D., Rensing-Ehl A., Schlesier M., Rohr J., Jakob T., Oswald E., Kopp M.V., et al. Reduced memory B cells in patients with hyper IgE syndrome. Clin. Immunol. 2008, 129:448-454.
56. Steininger C. Clinical relevance of cytomegalovirus infection in patients with disorders of the immune system. Clin. Microbiol. Infect. 2007, 13:953-963.
57. Vogelzang A., McGuire H.M., Yu D., Sprent J., Mackay C.R., King C. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 2008, 29:127-137.
58. Winkelstein J.A., Marino M.C., Lederman H.M., Jones S.M., Sullivan K., Burks A.W., Conley M.E., Cunningham-Rundles C., Ochs H.D. X-linked agammaglobulinemia: report on a United States registry of 201 patients. Medicine (Baltimore) 2006, 85:193-202.
59. Yang X.O., Panopoulos A.D., Nurieva R., Chang S.H., Wang D., Watowich S.S., Dong C. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 2007, 282:9358-9363.
60. Yawn B.P., Saddier P., Wollan P.C., St Sauver J.L., Kurland M.J., Sy L.S. A population-based study of the incidence and complication rates of herpes zoster before zoster vaccine introduction. Mayo Clin. Proc. 2007, 82:1341-1349.
61. Yi J.S., Du M., Zajac A.J. A vital role for interleukin-21 in the control of a chronic viral infection. Science 2009, 324:1572-1576.
62. Young T.Y., Jerome D., Gupta S. Hyperimmunoglobulinemia E syndrome associated with coronary artery aneurysms: deficiency of central memory CD4+ T cells and expansion of effector memory CD4+ T cells. Ann. Allergy Asthma Immunol. 2007, 98:389-392.
63. Yu C.L., Meyer D.J., Campbell G.S., Larner A.C., Carter-Su C., Schwartz J., Jove R. Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 1995, 269:81-83.