Constitutive but not inducible attenuation of transforming growth factor β signaling increases natural killer cell responses without directly affecting dendritic cells early after persistent viral infection

Journal of Virology

Volumn 89, Issue 6, 2015, Pages 3343-3355

  Lewis, Gavin M ^a   Macal, Monica ^a   Hesser, Charles R ^a,b   Zuñiga, Elina I ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Berkeley   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERFERON; INTERLEUKIN 2; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EFFECTOR CELL; IN VIVO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; MURINE CYTOMEGALOVIRUS; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRUS ATTENUATION; VIRUS INFECTION; ANIMAL; C57BL MOUSE; FEMALE; GENETICS; HERPES VIRUS INFECTION; HUMAN; IMMUNOLOGY; LYMPHOCYTIC CHORIOMENINGITIS; MALE; METABOLISM; MUROMEGALOVIRUS; PHYSIOLOGY; RODENT DISEASE; VETERINARY; VIROLOGY;

LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MAIZE CHLOROTIC MOTTLE VIRUS; MURID HERPESVIRUS 1; MUS; RODENTIA;

ANIMALS; CYTOKINES; DENDRITIC CELLS; FEMALE; HERPESVIRIDAE INFECTIONS; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; MICE; MICE, INBRED C57BL; MUROMEGALOVIRUS; RODENT DISEASES; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84923163843     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03076-14     Document Type: Article

References (72)

1. Arase H, Mocarski ES, Campbell AE, Hill AB, Lanier LL. 2002. Direct recognition of cytomegalovirus by activating and inhibitoryNKcell receptors. Science 296:1323-1326. http://dx.doi.org/10.1126/science.1070884.
2. Li Q, Skinner PJ, Ha SJ, Duan L, Mattila TL, Hage A, White C, Barber DL, O'Mara L, Southern PJ, Reilly CS, Carlis JV, Miller CJ, Ahmed R, Haase AT. 2009. Visualizing antigen-specific and infected cells in situ predicts outcomes in early viral infection. Science 323:1726-1729. http://dx.doi.org/10.1126/science.1168676.
3. Kekow J, Wachsman W, McCutchan JA, Gross WL, Zachariah M, Carson DA, Lotz M. 1991. Transforming growth factor-beta and suppression of humoral immune responses in HIV infection. J Clin Invest 87:1010-1016. http://dx.doi.org/10.1172/JCI115059.
4. Hirsch CS, Ellner JJ, Blinkhorn R, Toossi Z. 1997. In vitro restoration of T cell responses in tuberculosis and augmentation of monocyte effector function against Mycobacterium tuberculosis by natural inhibitors of transforming growth factor beta. Proc Natl Acad Sci U S A 94:3926-3931. http://dx.doi.org/10.1073/pnas.94.8.3926.
5. Nelson DR, Gonzalez-Peralta RP, Qian K, Xu Y, Marousis CG, Davis GL, Lau JY. 1997. Transforming growth factor-beta 1 in chronic hepatitis C. J Viral Hepat 4:29-35.
6. Omer FM, Riley EM. 1998. Transforming growth factor beta production is inversely correlated with severity of murine malaria infection. J Exp Med 188:39-48. http://dx.doi.org/10.1084/jem.188.1.39.
7. Tinoco R, Alcalde V, Yang Y, Sauer K, Zuniga EI. 2009. Cell-intrinsic transforming growth factor-beta signaling mediates virus-specific CD8+ T cell deletion and viral persistence in vivo. Immunity 31:145-157. http://dx.doi.org/10.1016/j.immuni.2009.06.015.
8. Asselin-Paturel C, Boonstra A, Dalod M, Durand I, Yessaad N, Dezutter-Dambuyant C, Vicari A, O'Garra A, Biron C, Briere F, Trinchieri G. 2001. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat Immunol 2:1144-1150. http://dx.doi.org/10 .1038/ni736.
9. Dalod M, Chelbi R, Malissen B, Lawrence T. 2014. Dendritic cell maturation: functional specialization through signaling specificity and transcriptional programming. EMBO J 33:1104-1116. http://dx.doi.org/10 .1002/embj.201488027.
10. Dalod M, Salazar-Mather TP, Malmgaard L, Lewis C, Asselin-Paturel C, Briere F, Trinchieri G, Biron CA. 2002. Interferon alpha/beta and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J Exp Med 195:517-528. http://dx.doi.org/10 .1084/jem.20011672.
11. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. 2011. Innate or adaptive immunity? The example of natural killer cells. Science 331:44-49. http://dx.doi.org/10 .1126/science.1198687.
12. Kallies A, Carotta S, Huntington ND, Bernard NJ, Tarlinton DM, Smyth MJ, Nutt SL. 2011. A role for Blimp1 in the transcriptional network controlling natural killer cell maturation. Blood 117:1869-1879. http://dx.doi.org/10.1182/blood-2010-08-303123.
13. Waggoner SN, Cornberg M, Selin LK, Welsh RM. 2010. Natural killer cells act as rheostats modulating antiviral T cells. Nature 481:394-398. http://dx.doi.org/10.1038/nature10624.
14. Andrews DM, Andoniou CE, Scalzo AA, van Dommelen SL, Wallace ME, Smyth MJ, Degli-Esposti MA. 2005. Cross-talk between dendritic cells and natural killer cells in viral infection. Mol Immunol 42:547-555. http://dx.doi.org/10.1016/j.molimm.2004.07.040.
15. Lang PA, Lang KS, Xu HC, Grusdat M, Parish IA, Recher M, Elford AR, Dhanji S, Shaabani N, Tran CW, Dissanayake D, Rahbar R, Ghazarian M, Brustle A, Fine J, Chen P, Weaver CT, Klose C, Diefenbach A, Haussinger D, Carlyle JR, Kaech SM, Mak TW, Ohashi PS. 2012. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc Natl Acad Sci U S A 109:1210-1215. http://dx.doi.org/10.1073/pnas.1118834109.
16. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, Annunziata N, Doetschman T. 1992. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359:693-699. http://dx.doi.org/10.1038/359693a0.
17. Marie JC, Liggitt D, Rudensky AY. 2006. Cellular mechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factor-beta receptor. Immunity 25:441-454. http://dx.doi.org/10.1016/j.immuni.2006.07.012.
18. Siddiqui KR, Laffont S, Powrie F. 2010. E-cadherin marks a subset of inflammatory dendritic cells that promote T cell-mediated colitis. Immunity 32:557-567. http://dx.doi.org/10.1016/j.immuni.2010.03.017.
19. Belladonna ML, Volpi C, Bianchi R, Vacca C, Orabona C, Pallotta MT, Boon L, Gizzi S, Fioretti MC, Grohmann U, Puccetti P. 2008. Cutting edge: autocrine TGF-beta sustains default tolerogenesis by IDOcompetent dendritic cells. J Immunol 181:5194-5198. http://dx.doi.org/10.4049/jimmunol.181.8.5194.
20. Borkowski TA, Letterio JJ, Mackall CL, Saitoh A, Farr AG, Wang XJ, Roop DR, Gress RE, Udey MC. 1997. Langerhans cells in the TGF beta 1 null mouse. Adv Exp Med Biol 417:307-310. http://dx.doi.org/10.1007/978-1-4757-9966-8_50.
21. Contractor N, Louten J, Kim L, Biron CA, Kelsall BL. 2007. Cutting edge: Peyer's patch plasmacytoid dendritic cells (pDCs) produce low levels of type I interferons: possible role for IL-10, TGFbeta, and prostaglandin E2 in conditioning a unique mucosal pDC phenotype. J Immunol 179: 2690-2694. http://dx.doi.org/10.4049/jimmunol.179.5.2690.
22. Yamaguchi Y, Tsumura H, Miwa M, Inaba K. 1997. Contrasting effects of TGF-beta 1 and TNF-alpha on the development of dendritic cells from progenitors in mouse bone marrow. Stem Cells 15:144-153. http://dx.doi .org/10.1002/stem.150144.
23. Sevilla N, McGavern DB, Teng C, Kunz S, Oldstone MB. 2004. Viral targeting of hematopoietic progenitors and inhibition of DC maturation as a dual strategy for immune subversion. J Clin Invest 113:737-745. http://dx.doi.org/10.1172/JCI20243.
24. Zuniga EI, Liou LY, Mack L, Mendoza M, Oldstone MB. 2008. Persistent virus infection inhibits type I interferon production by plasmacytoid dendritic cells to facilitate opportunistic infections. Cell Host Microbe 4:374-386. http://dx.doi.org/10.1016/j.chom.2008.08.016.
25. Fitzgerald-Bocarsly P, Jacobs ES. 2010. Plasmacytoid dendritic cells in HIV infection: striking a delicate balance. J Leukoc Biol 87:609-620. http://dx.doi.org/10.1189/jlb.0909635.
26. Sun C, Fu B, Gao Y, Liao X, Sun R, Tian Z, Wei H. 2012. TGF-beta1 down-regulation of NKG2D/DAP10 and 2B4/SAP expression on human NK cells contributes to HBV persistence. PLoS Pathog 8:e1002594. http://dx.doi.org/10.1371/journal.ppat.1002594.
27. Alter G, Teigen N, Davis BT, Addo MM, Suscovich TJ, Waring MT, Streeck H, Johnston MN, Staller KD, Zaman MT, Yu XG, Lichterfeld M, Basgoz N, Rosenberg ES, Altfeld M. 2005. Sequential deregulation of NKcell subset distribution and function starting in acute HIV-1 infection. Blood 106:3366-3369. http://dx.doi.org/10.1182/blood-2005-03-1100.
28. Herzer K, Falk CS, Encke J, Eichhorst ST, Ulsenheimer A, Seliger B, Krammer PH. 2003. Upregulation of major histocompatibility complex class I on liver cells by hepatitis C virus core protein via p53 and TAP1 impairs natural killer cell cytotoxicity. J Virol 77:8299-8309. http://dx.doi .org/10.1128/JVI.77.15.8299-8309.2003.
29. Su HC, Ishikawa R, Biron CA. 1993. Transforming growth factor-beta expression and natural killer cell responses during virus infection of normal, nude, and SCID mice. J Immunol 151:4874-4890.
30. Laouar Y, Sutterwala FS, Gorelik L, Flavell RA. 2005. Transforming growth factor-beta controls T helper type 1 cell development through regulation of natural killer cell interferon-gamma. Nat Immunol 6:600-607. http://dx.doi.org/10.1038/ni1197.
31. Marcoe JP, Lim JR, Schaubert KL, Fodil-Cornu N, Matka M, McCubbrey AL, Farr AR, Vidal SM, Laouar Y. 2012. TGF-beta is responsible for NK cell immaturity during ontogeny and increased susceptibility to infection during mouse infancy. Nat Immunol 13:843-850. http://dx.doi.org/10.1038/ni.2388.
32. Feil R, Wagner J, Metzger D, Chambon P. 1997. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun 237:752-757. http://dx.doi.org/10 .1006/bbrc.1997.7124.
33. Ruzankina Y, Pinzon-Guzman C, Asare A, Ong T, Pontano L, Cotsarelis G, Zediak VP, Velez M, Bhandoola A, Brown EJ. 2007. Deletion of the developmentally essential gene ATR in adult mice leads to age-related phenotypes and stem cell loss. Cell Stem Cell 1:113-126. http://dx.doi.org/10.1016/j.stem.2007.03.002.
34. Li MO, Sanjabi S, Flavell RA. 2006. Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and-independent mechanisms. Immunity 25:455-471. http://dx.doi.org/10.1016/j.immuni.2006.07.011.
35. Ouyang W, Oh SA, Ma Q, Bivona MR, Zhu J, Li MO. 2013. TGF-beta cytokine signaling promotes CD8+ T cell development and low-affinity CD4+ T cell homeostasis by regulation of interleukin-7 receptor alpha expression. Immunity 39:335-346. http://dx.doi.org/10.1016/j.immuni .2013.07.016.
36. Chalmer JE, Mackenzie JS, Stanley NF. 1977. Resistance to murine cytomegalovirus linked to the major histocompatibility complex of the mouse. J Gen Virol 37:107-114. http://dx.doi.org/10.1099/0022-1317-37-1-107.
37. Ahmed R, Salmi A, Butler LD, Chiller JM, Oldstone MB. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J Exp Med 160:521-540.
38. Zuniga EI, McGavern DB, Pruneda-Paz JL, Teng C, Oldstone MB. 2004. Bone marrow plasmacytoid dendritic cells can differentiate into myeloid dendritic cells upon virus infection. Nat Immunol 5:1227-1234. http://dx .doi.org/10.1038/ni1136.
39. Jiang Z, Georgel P, Du X, Shamel L, Sovath S, Mudd S, Huber M, Kalis C, Keck S, Galanos C, Freudenberg M, Beutler B. 2005. CD14 is required for MyD88-independent LPS signaling. Nat Immunol 6:565-570. http://dx.doi.org/10.1038/ni1207.
40. Lin AH, Luo J, Mondshein LH, ten Dijke P, Vivien D, Contag CH, Wyss-Coray T. 2005. Global analysis of Smad2/3-dependent TGF-beta signaling in living mice reveals prominent tissue-specific responses to injury. J Immunol 175:547-554. http://dx.doi.org/10.4049/jimmunol .175.1.547.
41. Swiecki M, Wang Y, Vermi W, Gilfillan S, Schreiber RD, Colonna M. 2011. Type I interferon negatively controls plasmacytoid dendritic cell numbers in vivo. J Exp Med 208:2367-2374. http://dx.doi.org/10.1084/jem.20110654.
42. Swiecki M, Gilfillan S, Vermi W, Wang Y, Colonna M. 2010. Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8(+) T cell accrual. Immunity 33:955-966. http://dx.doi .org/10.1016/j.immuni.2010.11.020.
43. Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wei XQ, Liew FY, Caligiuri MA, Durbin JE, Biron CA. 2002. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J Immunol 169:4279-4287. http://dx.doi.org/10.4049/jimmunol.169.8.4279.
44. Nguyen KB, Watford WT, Salomon R, Hofmann SR, Pien GC, Morinobu A, Gadina M, O'Shea JJ, Biron CA. 2002. Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 297:2063-2066. http://dx.doi.org/10 .1126/science.1074900.
45. Chaix J, Tessmer MS, Hoebe K, Fuseri N, Ryffel B, Dalod M, Alexopoulou L, Beutler B, Brossay L, Vivier E, Walzer T. 2008. Cutting edge: priming ofNKcells by IL-18. J Immunol 181:1627-1631. http://dx.doi.org/10.4049/jimmunol.181.3.1627.
46. Brown MG, Dokun AO, Heusel JW, Smith HR, Beckman DL, Blattenberger EA, Dubbelde CE, Stone LR, Scalzo AA, Yokoyama WM. 2001. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292:934-937. http://dx.doi.org/10.1126/science .1060042.
47. Daniels KA, Devora G, Lai WC, O'Donnell CL, Bennett M, Welsh RM. 2001. Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J Exp Med 194: 29-44. http://dx.doi.org/10.1084/jem.194.1.29.
48. Dokun AO, Kim S, Smith HR, Kang HS, Chu DT, Yokoyama WM. 2001. Specific and nonspecific NK cell activation during virus infection. Nat Immunol 2:951-956. http://dx.doi.org/10.1038/ni714.
49. Orr MT, Murphy WJ, Lanier LL. 2010. 'Unlicensed' natural killer cells dominate the response to cytomegalovirus infection. Nat Immunol 11: 321-327. http://dx.doi.org/10.1038/ni.1849.
50. Gerosa F, Scardoni M, Tommasi M, Benati C, Snelli L, Gandini G, Libonati M, Tridente G, Carra G. 1991. Interferon alpha induces expression of the CD69 activation antigen in human resting NK cells, while interferon gamma and tumor necrosis factor alpha are ineffective. Int J Cancer 48:473-475. http://dx.doi.org/10.1002/ijc.2910480328.
51. Bukowski JF, Welsh RM. 1985. Inability of interferon to protect virusinfected cells against lysis by natural killer (NK) cells correlates with NK cell-mediated antiviral effects in vivo. J Immunol 135:3537-3541.
52. Jung A, Kato H, Kumagai Y, Kumar H, Kawai T, Takeuchi O, Akira S. 2008. Lymphocytoid choriomeningitis virus activates plasmacytoid dendritic cells and induces a cytotoxic T-cell response via MyD88. J Virol 82:196-206. http://dx.doi.org/10.1128/JVI.01640-07.
53. Macal M, Lewis GM, Kunz S, Flavell R, Harker JA, Zuniga EI. 2012. Plasmacytoid dendritic cells are productively infected and activated through TLR-7 early after arenavirus infection. Cell Host Microbe 11: 617-630. http://dx.doi.org/10.1016/j.chom.2012.04.017.
54. Cervantes-Barragan L, Lewis KL, Firner S, Thiel V, Hugues S, Reith W, Ludewig B, Reizis B. 2012. Plasmacytoid dendritic cells control T-cell response to chronic viral infection. Proc Natl Acad Sci U S A 109:3012-3017. http://dx.doi.org/10.1073/pnas.1117359109.
55. Blasius AL, Krebs P, Sullivan BM, Oldstone MB, Popkin DL. 2012. Slc15a4, a gene required for pDC sensing of TLR ligands, is required to control persistent viral infection. PLoS Pathog 8:e1002915. http://dx.doi .org/10.1371/journal.ppat.1002915.
56. Montoya M, Edwards MJ, Reid DM, Borrow P. 2005. Rapid activation of spleen dendritic cell subsets following lymphocytic choriomeningitis virus infection of mice: analysis of the involvement of type 1 IFN. J Immunol 174:1851-1861. http://dx.doi.org/10.4049/jimmunol.174.4.1851.
57. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 77:4911-4927. http://dx.doi.org/10.1128/JVI.77.8.4911-4927.2003.
58. Brooks DG, Teyton L, Oldstone MB, McGavern DB. 2005. Intrinsic functional dysregulation of CD4 T cells occurs rapidly following persistent viral infection. J Virol 79:10514-10527. http://dx.doi.org/10.1128/JVI.79 .16.10514-10527.2005.
59. Ishigame H, Mosaheb MM, Sanjabi S, Flavell RA. 2013. Truncated form of TGF-betaRII, but not its absence, induces memory CD8+T cell expansion and lymphoproliferative disorder in mice. J Immunol 190:6340-6350. http://dx.doi.org/10.4049/jimmunol.1300397.
60. Chytil A, Magnuson MA, Wright CV, Moses HL. 2002. Conditional inactivation of the TGF-beta type II receptor using Cre:Lox. Genesis 32: 73-75. http://dx.doi.org/10.1002/gene.10046.
61. Tay CH, Welsh RM. 1997. Distinct organ-dependent mechanisms for the control of murine cytomegalovirus infection by natural killer cells. J Virol 71:267-275.
62. Salazar-Mather TP, Orange JS, Biron CA. 1998. Early murine cytomegalovirus (MCMV) infection induces liver natural killer (NK) cell inflammation and protection through macrophage inflammatory protein 1alpha (MIP-1alpha)-dependent pathways. J Exp Med 187:1-14. http://dx.doi .org/10.1084/jem.187.1.1.
63. Andrews DM, Estcourt MJ, Andoniou CE, Wikstrom ME, Khong A, Voigt V, Fleming P, Tabarias H, Hill GR, van der Most RG, Scalzo AA, Smyth MJ, Degli-Esposti MA. 2010. Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J Exp Med 207:1333-1343. http://dx.doi.org/10.1084/jem.20091193.
64. Kanzler S, Baumann M, Schirmacher P, Dries V, Bayer E, Gerken G, Dienes HP, Lohse AW. 2001. Prediction of progressive liver fibrosis in hepatitis C infection by serum and tissue levels of transforming growth factor-beta. J Viral Hepat 8:430-437. http://dx.doi.org/10.1046/j.1365-2893.2001.00314.x.
65. Kornfeld C, Ploquin MJ, Pandrea I, Faye A, Onanga R, Apetrei C, Poaty-Mavoungou V, Rouquet P, Estaquier J, Mortara L, Desoutter JF, Butor C, Le Grand R, Roques P, Simon F, Barre-Sinoussi F, Diop OM, Muller-Trutwin MC. 2005. Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J Clin Invest 115:1082-1091. http://dx.doi.org/10.1172/JCI23006.
66. Boomershine CS, Chamberlain A, Kendall P, Afshar-Sharif AR, Huang H, Washington MK, Lawson WE, Thomas JW, Blackwell TS, Bhowmick NA. 2009. Autoimmune pancreatitis results from loss of TGFbeta signalling in S100A4-positive dendritic cells. Gut 58:1267-1274. http://dx.doi .org/10.1136/gut.2008.170779.
67. Fainaru O, Woolf E, Lotem J, Yarmus M, Brenner O, Goldenberg D, Negreanu V, Bernstein Y, Levanon D, Jung S, Groner Y. 2004. Runx3 regulates mouse TGF-beta-mediated dendritic cell function and its absence results in airway inflammation. EMBO J 23:969-979. http://dx.doi .org/10.1038/sj.emboj.7600085.
68. Laouar Y, Town T, Jeng D, Tran E, Wan Y, Kuchroo VK, Flavell RA. 2008. TGF-beta signaling in dendritic cells is a prerequisite for the control of autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 105:10865-10870. http://dx.doi.org/10.1073/pnas.0805058105.
69. Lievens D, Habets KL, Robertson AK, Laouar Y, Winkels H, Rademakers T, Beckers L, Wijnands E, Boon L, Mosaheb M, Ait-Oufella H, Mallat Z, Flavell RA, Rudling M, Binder CJ, Gerdes N, Biessen EA, Weber C, Daemen MJ, Kuiper J, Lutgens E. 2013. Abrogated transforming growth factor beta receptor II (TGFbetaRII) signalling in dendritic cells promotes immune reactivity of T cells resulting in enhanced atherosclerosis. Eur Heart J 34:3717-3727. http://dx.doi.org/10.1093/eurheartj/ehs106.
70. Allen SJ, Mott KR, Wechsler SL, Flavell RA, Town T, Ghiasi H. 2011. Adaptive and innate transforming growth factor beta signaling impact herpes simplex virus 1 latency and reactivation. J Virol 85:11448-11456. http://dx.doi.org/10.1128/JVI.00678-11.
71. Ramalingam R, Larmonier CB, Thurston RD, Midura-Kiela MT, Zheng SG, Ghishan FK, Kiela PR. 2012. Dendritic cell-specific disruption of TGF-beta receptor II leads to altered regulatory T cell phenotype and spontaneous multiorgan autoimmunity. J Immunol 189:3878-3893. http://dx.doi.org/10.4049/jimmunol.1201029.
72. Robbins SH, Bessou G, Cornillon A, Zucchini N, Rupp B, Ruzsics Z, Sacher T, Tomasello E, Vivier E, Koszinowski UH, Dalod M. 2007. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Pathog 3:e123. http://dx.doi.org/10.1371/journal .ppat.0030123.