A stimulation-dependent alternate core promoter links lymphotoxin α expression with TGF-β1 and fibroblast growth factor-7 signaling in primary human T cells

Journal of Immunology

Volumn 190, Issue 9, 2013, Pages 4573-4584

  Yokley, Brian H ^a   Selby, Sandra T ^a   Posch, Phillip E ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KERATINOCYTE GROWTH FACTOR; LYMPHOTOXIN; MESSENGER RNA; RNA POLYMERASE II; TRANSCRIPTION FACTOR II; TRANSCRIPTION FACTOR II I; TRANSCRIPTION FACTOR SP1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; BINDING SITE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VIVO STUDY; LYMPHOTOXIN ALPHA GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION;

B-LYMPHOCYTES; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; DNA-BINDING PROTEINS; EPITHELIAL CELLS; FIBROBLAST GROWTH FACTOR 7; GENE EXPRESSION REGULATION; HUMANS; JURKAT CELLS; LYMPHOTOXIN-ALPHA; MOLECULAR SEQUENCE DATA; POLYPYRIMIDINE TRACT-BINDING PROTEIN; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; RNA, MESSENGER; SIGNAL TRANSDUCTION; SP1 TRANSCRIPTION FACTOR; STROMAL CELLS; T-LYMPHOCYTES; TRANSCRIPTION FACTORS, TFII; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84876790754     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201068     Document Type: Article

References (93)

1. Ware, C. F. 2005. Network communications: lymphotoxins, LIGHT, and TNF. Annu. Rev. Immunol. 23: 787-819. (Pubitemid 40563185)
2. Schneider, K., K. G. Potter, and C. F. Ware. 2004. Lymphotoxin and LIGHT signaling pathways and target genes. Immunol. Rev. 202: 49-66. (Pubitemid 39576904)
3. Kang, H. S., R. K. Chin, Y. Wang, P. Yu, J. Wang, K. A. Newell, and Y. X. Fu. 2002. Signaling via LTbR on the lamina propria stromal cells of the gut is required for IgA production. Nat. Immunol. 3: 576-582. (Pubitemid 34662311)
4. Newberry, R. D., J. S. McDonough, K. G. McDonald, and R. G. Lorenz. 2002. Postgestational lymphotoxin/lymphotoxin b receptor interactions are essential for the presence of intestinal B lymphocytes. J. Immunol. 168: 4988-4997. (Pubitemid 34495961)
5. Fütterer, A., K. Mink, A. Luz, M. H. Kosco-Vilbois, and K. Pfeffer. 1998. The lymphotoxin b receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity 9: 59-70. (Pubitemid 28361295)
6. Chin, R. K., J. C. Lo, O. Kim, S. E. Blink, P. A. Christiansen, P. Peterson, Y. Wang, C. F. Ware, and Y.-X. Fu. 2003. Lymphotoxin pathway directs thymic Aire expression. Nat. Immunol. 4: 1121-1127. (Pubitemid 37428040)
7. Chin, R. K., M. Zhu, P. A. Christiansen, W. Liu, C. F. Ware, L. Peltonen, X. Zhang, L. Guo, S. Han, B. Zheng, and Y.-X. Fu. 2006. Lymphotoxin pathway-directed, autoimmune regulator-independent central tolerance to arthritogenic collagen. J. Immunol. 177: 290-297. (Pubitemid 43939140)
8. Seach, N., T. Ueno, A. L. Fletcher, T. Lowen, M. Mattesich, C. R. Engwerda, H. S. Scott, C. F. Ware, A. P. Chidgey, D. H. D. Gray, and R. L. Boyd. 2008. The lymphotoxin pathway regulates Aire-independent expression of ectopic genes and chemokines in thymic stromal cells. J. Immunol. 180: 5384-5392.
9. 3 induces chemokines and adhesion molecules: insight into the role of LTa in inflammation and lymphoid organ development. J. Immunol. 161: 6853-6860. (Pubitemid 28562230)
10. 2 in lymphotoxin-induced inflammation: critical role of TNF receptor 1 signaling. J. Immunol. 160: 485-491. (Pubitemid 28116765)
11. Koni, P. A., R. Sacca, P. Lawton, J. L. Browning, N. H. Ruddle, and R. A. Flavell. 1997. Distinct roles in lymphoid organogenesis for lymphotoxins a and b revealed in lymphotoxin b-deficient mice. Immunity 6: 491-500. (Pubitemid 27208204)
12. De Togni, P., J. Goellner, N. H. Ruddle, P. R. Streeter, A. Fick, S. Mariathasan, S. C. Smith, R. Carlson, L. P. Shornick, J. Strauss-Schoenberger, et al. 1994. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264: 703-707. (Pubitemid 24185880)
13. Lo, J. C., Y. Wang, A. V. Tumanov, M. Bamji, Z. Yao, C. A. Reardon, G. S. Getz, and Y. X. Fu. 2007. Lymphotoxin b receptor-dependent control of lipid ho-meostasis. Science 316: 285-288. (Pubitemid 46633106)
14. Ware, C. F., P. D. Crowe, M. H. Grayson, M. J. Androlewicz, and J. L. Browning. 1992. Expression of surface lymphotoxin and tumor necrosis factor on activated T, B, and natural killer cells. J. Immunol. 149: 3881-3888. (Pubitemid 23068868)
15. + T cells are a major source of lymphotoxin a. J. Immunol. 162: 3790-3794. (Pubitemid 29314755)
16. Worm, M. M., A. Tsytsykova, and R. S. Geha. 1998. CD40 ligation and IL-4 use different mechanisms of transcriptional activation of the human lymphotoxin alpha promoter in B cells. Eur. J. Immunol. 28: 901-906. (Pubitemid 28116203)
17. Luther, S. A., A. Bidgol, D. C. Hargreaves, A. Schmidt, Y. Xu, J. Paniyadi, M. Matloubian, and J. G. Cyster. 2002. Differing activities of homeostatic chemokines CCL19, CCL21, and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis. J. Immunol. 169: 424-433. (Pubitemid 34686164)
18. Nedwin, G. E., S. L. Naylor, A. Y. Sakaguchi, D. Smith, J. Jarrett-Nedwin, D. Pennica, D. V. Goeddel, and P. W. Gray. 1985. Human lymphotoxin and tumor necrosis factor genes: structure, homology and chromosomal localization. Nucleic Acids Res. 13: 6361-6373.
19. Messer, G., E. H. Weiss, and P. A. Baeuerle. 1990. Tumor necrosis factor beta (TNF-b) induces binding of the NF-kB transcription factor to a high-affinity kB element in the TNF-b promoter. Cytokine 2: 389-397.
20. Buonaguro, L., F. M. Buonaguro, G. Giraldo, and B. Ensoli. 1994. The human immunodeficiency virus type 1 Tat protein transactivates tumor necrosis factor b gene expression through a TAR-like structure. J. Virol. 68: 2677-2682. (Pubitemid 24091947)
21. Tschachler, E., E. Böhnlein, S. Felzmann, and M. S. Reitz, Jr. 1993. Human T-lymphotropic virus type I tax regulates the expression of the human lymphotoxin gene. Blood 81: 95-100. (Pubitemid 23013682)
22. Smirnova, A. S., K. C. Ferreira-Silva, K. L. Mine, V. Andrade-Oliveira, N. Shulzhenko, M. Gerbase-DeLima, and A. Morgun. 2008. Differential expression of new LTA splice variants upon lymphocyte activation. Mol. Immunol. 45: 295-300. (Pubitemid 47334749)
23. Taylor, J. M., K. Wicks, C. Vandiedonck, and J. C. Knight. 2008. Chromatin profiling across the human tumour necrosis factor gene locus reveals a complex, cell type-specific landscape with novel regulatory elements. Nucleic Acids Res. 36: 4845-4862.
24. Kobayashi, Y., D. Miyamoto, M. Asada, M. Obinata, and T. Osawa. 1986. Cloning and expression of human lymphotoxin mRNA derived from a human T cell hybridoma. J. Biochem. 100: 727-733.
25. Strausberg, R. L., E. A. Feingold, L. H. Grouse, J. G. Derge, R. D. Klausner, F. S. Collins, L. Wagner, C. M. Shenmen, G. D. Schuler, S. F. Altschul, et al; Mammalian Gene Collection Program Team. 2002. Generation and initial analysis of more than 15, 000 full-length human and mouse cDNA sequences. Proc. Natl. Acad. Sci. USA 99: 16899-16903. (Pubitemid 36034070)
26. Davuluri, R. V., Y. Suzuki, S. Sugano, C. Plass, and T. H.-M. Huang. 2008. The functional consequences of alternative promoter use in mammalian genomes. Trends Genet. 24: 167-177.
27. Ozaki, K., Y. Ohnishi, A. Iida, A. Sekine, R. Yamada, T. Tsunoda, H. Sato, H. Sato, M. Hori, Y. Nakamura, and T. Tanaka. 2002. Functional SNPs in the lymphotoxin-a gene that are associated with susceptibility to myocardial infarction. Nat. Genet. 32: 650-654. (Pubitemid 35435179)
28. Knight, J. C., B. J. Keating, and D. P. Kwiatkowski. 2004. Allele-specific repression of lymphotoxin-a by activated B cell factor-1. Nat. Genet. 36: 394-399. (Pubitemid 38437263)
29. Posch, P. E., I. Cruz, D. Bradshaw, and B. A. Medhekar. 2003. Novel polymorphisms and the definition of promoter "alleles" of the tumor necrosis factor and lymphotoxin a loci: inclusion in HLA haplotypes. Genes Immun. 4: 547-558. (Pubitemid 38961150)
30. Hehlgans, T., and K. Pfeffer. 2005. The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: players, rules and the games. Immunology 115: 1-20. (Pubitemid 40598088)
31. Dejardin, E., N. M. Droin, M. Delhase, E. Haas, Y. Cao, C. Makris, Z.-W. Li, M. Karin, C. F. Ware, and D. R. Green. 2002. The lymphotoxin-b receptor induces different patterns of gene expression via two NF-kB pathways. Immunity 17: 525-535. (Pubitemid 35223540)
32. Ross, S., and C. S. Hill. 2008. How the Smads regulate transcription. Int. J. Biochem. Cell Biol. 40: 383-408. (Pubitemid 351241229)
33. Moustakas, A., and C.-H. Heldin. 2009. The regulation of TGFb signal trans-duction. Development 136: 3699-3714.
34. Feng, X.-H., and R. Derynck. 2005. Specificity and versatility in TGF-b signaling through Smads. Annu. Rev. Cell Dev. Biol. 21: 659-693. (Pubitemid 41740650)
35. Eberlé, D., B. Hegarty, P. Bossard, P. Ferré, and F. Foufelle. 2004. SREBP transcription factors: master regulators of lipid homeostasis. Biochimie 86: 839-848. (Pubitemid 39602764)
36. Shimano, H. 2001. Sterol regulatory element-binding proteins (SREBPs): tran-scriptional regulators of lipid synthetic genes. Prog. Lipid Res. 40: 439-452. (Pubitemid 32929966)
37. Espenshade, P. J., and A. L. Hughes. 2007. Regulation of sterol synthesis in eukaryotes. Annu. Rev. Genet. 41: 401-427.
38. Chang, Y., J. Wang, X. Lu, D. P. Thewke, and R. J. Mason. 2005. KGF induces lipogenic genes through a PI3K and JNK/SREBP-1 pathway in H292 cells. J. Lipid Res. 46: 2624-2635. (Pubitemid 43107474)
39. Mason, R. J., T. Pan, K. E. Edeen, L. D. Nielsen, F. Zhang, M. Longphre, M. R. Eckart, and S. Neben. 2003. Keratinocyte growth factor and the transcription factors C/EBP a, C/EBP d, and SREBP-1c regulate fatty acid synthesis in alveolar type II cells. J. Clin. Invest. 112: 244-255. (Pubitemid 38056360)
40. Mason, I. 2007. Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat. Rev. Neurosci. 8: 583-596. (Pubitemid 47093932)
41. Beenken, A., and M. Mohammadi. 2009. The FGF family: biology, patho-physiology and therapy. Nat. Rev. Drug Discov. 8: 235-253.
42. Baumann, M., J. Pontiller, and W. Ernst. 2010. Structure and basal transcription complex of RNA polymerase II core promoters in the mammalian genome: an overview. Mol. Biotechnol. 45: 241-247.
43. Butler, J. E. F., and J. T. Kadonaga. 2002. The RNA polymerase II core promoter: a key component in the regulation of gene expression. Genes Dev. 16: 2583-2592.
44. Smale, S. T. 1997. Transcription initiation from TATA-less promoters within eukaryotic protein-coding genes. Biochim. Biophys. Acta 1351: 73-88. (Pubitemid 27117470)
45. Roy, A. L. 2001. Biochemistry and biology of the inducible multifunctional transcription factor TFII-I. Gene 274: 1-13. (Pubitemid 32817118)
46. Roy, A. L., S. Malik, M. Meisterernst, and R. G. Roeder. 1993. An alternative pathway for transcription initiation involving TFII-I. Nature 365: 355-359. (Pubitemid 23288979)
47. II110 component of the Drosophila TFIID complex and mediates transcriptional activation. Proc. Natl. Acad. Sci. USA 91: 192-196.
48. Weis, L., and D. Reinberg. 1992. Transcription by RNA polymerase II: initiator-directed formation of transcription-competent complexes. FASEB J. 6: 3300-3309.
49. Manzano-Winkler, B., C. D. Novina, and A. L. Roy. 1996. TFII is required for transcription of the naturally TATA-less but initiator-containing Vb promoter. J. Biol. Chem. 271: 12076-12081. (Pubitemid 26157287)
50. Javahery, R., A. Khachi, K. Lo, B. Zenzie-Gregory, and S. T. Smale. 1994. DNA sequence requirements for transcriptional initiator activity in mammalian cells. Mol. Cell. Biol. 14: 116-127.
51. Novina, C. D., V. Cheriyath, M. C. Denis, and A. L. Roy. 1997. Methods for studying the biochemical properties of an Inr element binding protein: TFII-I. Methods 12: 254-263. (Pubitemid 27356921)
52. Johansson, E., E. Skogman, and L. Thelander. 1995. The TATA-less promoter of mouse ribonucleotide reductase R1 gene contains a TFII-I binding initiator element essential for cell cycle-regulated transcription. J. Biol. Chem. 270: 30162-30167. (Pubitemid 26001691)
53. Wu, Y., and C. Patterson. 1999. The human KDR/flk-1 gene contains a functional initiator element that is bound and transactivated by TFII-I. J. Biol. Chem. 274: 3207-3214. (Pubitemid 29075410)
54. Cheriyath, V., C. D. Novina, and A. L. Roy. 1998. TFII-I regulates Vb promoter activity through an initiator element. Mol. Cell. Biol. 18: 4444-4454. (Pubitemid 28343029)
55. Kim, H. J., M. S. Ko, H. K. Kim, W. J. Cho, S. H. Lee, B. J. Lee, and J. W. Park. 2011. Transcription factor Sp1 regulates basal transcription of the human DRG2 gene. Biochim. Biophys. Acta 1809: 184-190.
56. Tian, H., G.-W. Qian, W. Li, F.-F. Chen, J.-H. Di, B.-F. Zhang, D.-S. Pei, P. Ma, and J.-N. Zheng. 2011. A critical role of Sp1 transcription factor in regulating the human Ki-67 gene expression. Tumour Biol. 32: 273-283.
57. Kim, H., S. Lee, B. Park, L. Che, and S. Lee. 2010. Sp1 and Sp3 mediate basal and serum-induced expression of human CENP-W. Mol. Biol. Rep. 37: 3593-3600.
58. Dishart, D., N. Schnur, N. Klan, O. Werz, D. Steinhilber, B. Samuelsson, and O. Rådmark. 2005. GC-rich sequences in the 5-lipoxygenase gene promoter are required for expression in Mono Mac 6 cells, characterization of a novel Sp1 binding site. Biochim. Biophys. Acta 1738: 37-47. (Pubitemid 43124108)
59. Muse, G. W., D. A. Gilchrist, S. Nechaev, R. Shah, J. S. Parker, S. F. Grissom, J. Zeitlinger, and K. Adelman. 2007. RNA polymerase is poised for activation across the genome. Nat. Genet. 39: 1507-1511. (Pubitemid 350191341)
60. Guenther, M. G., S. S. Levine, L. A. Boyer, R. Jaenisch, and R. A. Young. 2007. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77-88. (Pubitemid 47031323)
61. Moore, M. J., and N. J. Proudfoot. 2009. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136: 688-700.
62. Williams, B. R. G. 1999. PKR; a sentinel kinase for cellular stress. Oncogene 18: 6112-6120.
63. Kozak, M. 2005. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361: 13-37. (Pubitemid 41506931)
64. Svoboda, P., and A. Di Cara. 2006. Hairpin RNA: a secondary structure of primary importance. Cell. Mol. Life Sci. 63: 901-908.
65. Montano, M. A., K. Kripke, C. D. Norina, P. Achacoso, L. A. Herzenberg, A. L. Roy, and G. P. Nolan. 1996. NF-kB homodimer binding within the HIV-1 initiator region and interactions with TFII-I. Proc. Natl. Acad. Sci. USA 93: 12376-12381. (Pubitemid 26367151)
66. Ainbinder, E., M. Revach, O. Wolstein, S. Moshonov, N. Diamant, and R. Dikstein. 2002. Mechanism of rapid transcriptional induction of tumor necrosis factor a-responsive genes by NF-kB. Mol. Cell. Biol. 22: 6354-6362.
67. Perkins, N. D., A. B. Agranoff, E. Pascal, and G. J. Nabel. 1994. An interaction between the DNA-binding domains of RelA(p65) and Sp1 mediates human immunodeficiency virus gene activation. Mol. Cell. Biol. 14: 6570-6583. (Pubitemid 24299726)
68. Messer, G., U. Spengler, M. C. Jung, G. Honold, K. Blömer, G. R. Pape, G. Riethmüller, and E. H. Weiss. 1991. Polymorphic structure of the tumor necrosis factor (TNF) locus: an NcoI polymorphism in the first intron of the human TNF-b gene correlates with a variant amino acid in position 26 and a reduced level of TNF-b production. J. Exp. Med. 173: 209-219.
69. Massagué, J., J. Seoane, and D. Wotton. 2005. Smad transcription factors. Genes Dev. 19: 2783-2810. (Pubitemid 41739965)
70. Zhang, Y., X.-H. Feng, and R. Derynck. 1998. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-b-induced transcription. Nature 394: 909-913. (Pubitemid 28410915)
71. Liberati, N. T., M. B. Datto, J. P. Frederick, X. Shen, C. Wong, E. M. Rougier-Chapman, and X.-F. Wang. 1999. Smads bind directly to the Jun family of AP-1 transcription factors. Proc. Natl. Acad. Sci. USA 96: 4844-4849. (Pubitemid 29214499)
72. Datta, P. K., M. C. Blake, and H. L. Moses. 2000. Regulation of plasminogen activator inhibitor-1 expression by transforming growth factor-b-induced physical and functional interactions between Smads and Sp1. J. Biol. Chem. 275: 40014-40019. (Pubitemid 32064624)
73. Schwappacher, R., J. Weiske, E. Heining, V. Ezerski, B. Marom, Y. I. Henis, O. Huber, and P. Knaus. 2009. Novel crosstalk to BMP signalling: cGMP-dependent kinase I modulates BMP receptor and Smad activity. EMBO J. 28: 1537-1550.
74. Chin, R., J. Wang, and Y.-X. Fu. 2003. Lymphoid microenvironment in the gut for immunoglobulin A and inflammation. Immunol. Rev. 195: 190-201. (Pubitemid 37153462)
75. Cerutti, A. 2008. The regulation of IgA class switching. Nat. Rev. Immunol. 8: 421-434. (Pubitemid 351733417)
76. Pardali, E., X.-Q. Xie, P. Tsapogas, S. Itoh, K. Arvanitidis, C.-H. Heldin, P. ten Dijke, T. Grundström, and P. Sideras. 2000. Smad and AML proteins synergis-tically confer transforming growth factor b1 responsiveness to human germ-line IgA genes. J. Biol. Chem. 275: 3552-3560. (Pubitemid 30083064)
77. Sonoda, E., R. Matsumoto, Y. Hitoshi, T. Ishii, M. Sugimoto, S. Araki, A. Tominaga, N. Yamaguchi, and K. Takatsu. 1989. Transforming growth factor b induces IgA production and acts additively with interleukin 5 for IgA pro duction. J. Exp. Med. 170: 1415-1420. (Pubitemid 19250703)
78. Lebman, D. A., F. D. Lee, and R. L. Coffman. 1990. Mechanism for transforming growth factor b and IL-2 enhancement of IgA expression in lipopolysaccharide-stimulated B cell cultures. J. Immunol. 144: 952-959. (Pubitemid 20065037)
79. Dunkley, M. L., and A. J. Husband. 1990-1991/1991. The role of non-B cells in localizing an IgA plasma cell response in the intestine. Reg. Immunol. 3: 336-340.
80. Rubin, J. S., D. P. Bottaro, M. Chedid, T. Miki, D. Ron, G. Cheon, W. G. Taylor, E. Fortney, H. Sakata, P. W. Finch, and W. J. LaRochelle. 1995. Keratinocyte growth factor. Cell Biol. Int. 19: 399-411.
81. Tumanov, A. V., P. A. Christiansen, and Y.-X. Fu. 2007. The role of lymphotoxin receptor signaling in diseases. Curr. Mol. Med. 7: 567-578. (Pubitemid 47618053)
82. Rosenau, W., G. C. Burke, and R. Anderson. 1981. Effects of lymphotoxin on target-cell plasma-membrane lipids. Cell. Immunol. 60: 144-154. (Pubitemid 11102723)
83. Boehm, T., S. Scheu, K. Pfeffer, and C. C. Bleul. 2003. Thymic medullary epithelial cell differentiation, thymocyte emigration, and the control of autoim-munity require lympho-epithelial cross talk via LTbR. J. Exp. Med. 198: 757-769. (Pubitemid 37087775)
84. Revest, J.-M., R. K. Suniara, K. Kerr, J. J. T. Owen, and C. Dickson. 2001. Development of the thymus requires signaling through the fibroblast growth factor receptor R2-IIIb. J. Immunol. 167: 1954-1961. (Pubitemid 32747500)
85. Milićević, N. M., K. Nohroudi, Z. Milićević, and J. Westermann. 2008. Activation of cortical and inhibited differentiation of medullary epithelial cells in the thymus of lymphotoxin-b receptor-deficient mice: an ultrastructural study. J. Anat. 212: 114-124. (Pubitemid 351193965)
86. White, A. J., K. Nakamura, W. E. Jenkinson, M. Saini, C. Sinclair, B. Seddon, P. Narendran, K. Pfeffer, T. Nitta, Y. Takahama, et al. 2010. Lymphotoxin signals from positively selected thymocytes regulate the terminal differentiation of medullary thymic epithelial cells. J. Immunol. 185: 4769-4776.
87. Finch, P. W., and J. S. Rubin. 2004. Keratinocyte growth factor/fibroblast growth factor 7, a homeostatic factor with therapeutic potential for epithelial protection and repair. Adv. Cancer Res. 91: 69-136. (Pubitemid 39140957)
88. Werner, S. 1998. Keratinocyte growth factor: a unique player in epithelial repair processes. Cytokine Growth Factor Rev. 9: 153-165. (Pubitemid 28376451)
89. Havran, W. L., and J. M. Jameson. 2010. Epidermal T cells and wound healing. J. Immunol. 184: 5423-5428.
90. Schäffer, M., and A. Barbul. 1998. Lymphocyte function in wound healing and following injury. Br. J. Surg. 85: 444-460. (Pubitemid 28175434)
91. Toulon, A., L. Breton, K. R. Taylor, M. Tenenhaus, D. Bhavsar, C. Lanigan, R. Rudolph, J. Jameson, and W. L. Havran. 2009. A role for human skin-resident T cells in wound healing. J. Exp. Med. 206: 743-750.
92. Ruddell, R. G., B. Knight, J. E. E. Tirnitz-Parker, B. Akhurst, L. Summerville, V. N. Subramaniam, J. K. Olynyk, and G. A. Ramm. 2009. Lymphotoxin-b receptor signaling regulates hepatic stellate cell function and wound healing in a murine model of chronic liver injury. Hepatology 49: 227-239.
93. Tumanov, A. V., E. P. Koroleva, P. A. Christiansen, M. A. Khan, M. J. Ruddy, B. Burnette, S. Papa, G. Franzoso, S. A. Nedospasov, Y.-X. Fu, and R. A. Anders. 2009. T cell-derived lymphotoxin regulates liver regeneration. Gastroenterology 136: 694-704, e4.