An immunoprotective privilege of corneal epithelial stem cells against Th17 inflammatory stress by producing glial cell-derived neurotrophic factor

Stem Cells

Volumn 28, Issue 12, 2010, Pages 2172-2181

  Bian, Fang ^a,b   Qi, Hong ^a,c   Ma, Ping ^a,d   Zhang, Lili ^a   Yoon, Kyung Chul ^a,e   Pflugfelder, Stephen C ^a   Li, De Quan ^a  

^a CULLEN EYE INSTITUTE   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c PEKING UNIVERSITY THIRD HOSPITAL   (China)

^d SHANDONG UNIVERSITY   (China)

^e Chonnam National University Medical School   (South Korea)

Author keywords

Adult stem cell; Corneal epithelium; Glial cell derived neurotrophic factor; Immunoprotection; Th17

Indexed keywords

CYTOKINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; I KAPPA B; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; MESSENGER RNA; NEUROTROPHIC FACTOR; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CORNEA EPITHELIUM; CORNEA LIMBUS; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; GLIA CELL; HUMAN; HUMAN TISSUE; IMMUNITY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; NONHUMAN; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL; TH17 CELL; WESTERN BLOTTING;

ADOLESCENT; ADULT; ANIMALS; CYTOPROTECTION; EPITHELIAL CELLS; EPITHELIUM, CORNEAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HUMANS; INFLAMMATION; INTERLEUKIN-17; MICE; MIDDLE AGED; NF-KAPPA B; OSMOTIC PRESSURE; PROTEIN TRANSPORT; RECEPTORS, INTERLEUKIN-17; SIGNAL TRANSDUCTION; STEM CELLS; STRESS, PHYSIOLOGICAL; TH17 CELLS; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 78651068317     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.539     Document Type: Article

References (52)

1. Davanger M, Evensen A. Role of the pericorneal papillary structure in renewal of corneal epithelium. Nature 1971;229:560-561.
2. Cotsarelis G, Cheng SZ, Dong G et al. Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: Implications on epithelial stem cells. Cell 1989;57:201-209. (Pubitemid 19112360)
3. Pellegrini G, Golisano O, Paterna P et al. Location and clonal analysis of stem cells and their differentiated progeny in the human ocular surface. J Cell Biol 1999;145:769-782. (Pubitemid 29240854)
4. Lavker RM, Dong G, Cheng SZ et al. Relative proliferative rates of limbal and corneal epithelia. Implications of corneal epithelial migration, circadian rhythm, and suprabasally located DNA-synthesizing keratinocytes. Invest Ophthalmol Vis Sci 1991;32:1864-1875.
5. Jing S, Wen D, Yu Y et al. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell 1996;85:1113-1124. (Pubitemid 26231176)
6. You L, Ebner S, Kruse FE. Glial cell-derived neurotrophic factor (GDNF)-induced migration and signal transduction in corneal epithelial cells. Invest Ophthalmol Vis Sci 2001;42:2496-2504.
7. Takahashi M. The GDNF/RET signaling pathway and human diseases. Cytokine Growth Factor Rev 2001;12:361-373.
8. Meng X, Lindahl M, Hyvonen ME et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000;287: 1489-1493.
9. Oatley JM, Avarbock MR, Telaranta AI et al. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci USA 2006;103:9524-9529.
10. Qi H, Li DQ, Bian F et al. Expression of glial cell-derived neurotrophic factor and its receptor in the stem-cell-containing human limbal epithelium. Br J Ophthalmol 2008;92:1269-1274.
11. Qi H, Shine HD, Li DQ et al. Glial cell-derived neurotrophic factor gene delivery enhances survival of human corneal epithelium in culture and the overexpression of GDNF in bioengineered constructs. Exp Eye Res 2008;87:580-586.
12. Dong C. Diversification of T-helper-cell lineages: Finding the family root of IL-17-producing cells. Nat Rev Immunol 2006;6:329-333.
13. Paradowska A, Maslinski W, Grzybowska-Kowalczyk A et al. The function of interleukin 17 in the pathogenesis of rheumatoid arthritis. Arch Immunol Ther Exp (Warsz) 2007;55:329-334.
14. Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008;28: 454-467.
15. Oboki K, Ohno T, Saito H et al. Th17 and allergy. Allergol Int 2008; 57:121-134.
16. Stockinger B, Veldhoen M. Differentiation and function of Th17 T cells. Curr Opin Immunol 2007;19:281-286.
17. Manel N, Unutmaz D, Littman DR. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol 2008;9:641-649. (Pubitemid 351714729)
18. Zhou L, Ivanov II, Spolski R 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.
19. Moseley TA, Haudenschild DR, Rose L et al. Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev 2003;14:155-174.
20. Molesworth-Kenyon SJ, Yin R, Oakes JE et al. IL-17 receptor signaling influences virus-induced corneal inflammation. J Leukoc Biol 2008; 83:401-408.
21. Zheng X, Bian F, Ma P et al. Induction of Th17 differentiation by corneal epithelial-derived cytokines. J Cell Physiol 2010;222:95-102.
22. Zheng X, de Paiva CS, Li D-Q et al. Desiccating stress promotes Th17 differentiation by ocular surface tissues through a dendritic cell-mediated pathway. Invest Ophthalmol Vis Sci 2010;51:3083-3091.
23. de Paiva CS, Chotikavanich S, Pangelinan SB et al. IL-17 disrupts corneal barrier following desiccating stress. Mucosal Immunol 2009;2: 243-253.
24. Chen Z, de Paiva CS, Luo L et al. Characterization of putative stem cell phenotype in human limbal epithelia. Stem Cells 2004;22: 355-366.
25. Kim HS, Jun Song X, de Paiva CS et al. Phenotypic characterization of human corneal epithelial cells expanded ex vivo from limbal explant and single cell cultures. Exp Eye Res 2004;79:41-49.
26. Li D-Q, Luo L, Chen Z et al. JNK and ERK MAP kinases mediate induction of IL-1beta, TNF-alpha and IL-8 following hyperosmolar stress in human limbal epithelial cells. Exp Eye Res 2006;82: 588-596.
27. Luo L, Li D-Q, Doshi A et al. Experimental dry eye stimulates production of inflammatory cytokines and MMP-9 and activates MAPK signaling pathways on the ocular surface. Invest Ophthalmol Vis Sci 2004;45:4293-4301. (Pubitemid 39564653)
28. Yoon KC, de Paiva CS, Qi H et al. Expression of Th-1 chemokines and chemokine receptors on the ocular surface of C57BL/6 mice: Effects of desiccating stress. Invest Ophthalmol Vis Sci 2007;48: 2561-2569.
29. de Paiva CS, Corrales RM, Villarreal AL et al. Corticosteroid and doxycycline suppress MMP-9 and inflammatory cytokine expression, Mapk activation in the corneal epithelium in experimental dry eye. Exp Eye Res 2006;83:526-535.
30. McAllister F, Henry A, Kreindler JL et al. Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: Implications for airway inflammation in cystic fibrosis. J Immunol 2005;175:404-412.
31. Chang SH, Dong C. A novel heterodimeric cytokine consisting of IL-17 and IL-17F regulates inflammatory responses. Cell Res 2007;17: 435-440.
32. Liang SC, Long AJ, Bennett F et al. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J Immunol 2007;179:7791-7799.
33. Uccelli A, Pistoia V, Moretta L. Mesenchymal stem cells: A new strategy for immunosuppression? Trends Immunol 2007;28:219-226.
34. Bartholomew A, Polchert D, Szilagyi E et al. Mesenchymal stem cells in the induction of transplantation tolerance. Transplantation 2009;87: S55-S57.
35. Ding Y, Xu D, Feng G et al. Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and -9. Diabetes 2009;58:1797-1806.
36. Schwarting S, Litwak S, Hao W et al. Hematopoietic stem cells reduce postischemic inflammation and ameliorate ischemic brain injury. Stroke 2008;39:2867-2875.
37. Geraci F, Turturici G, Galli D et al. Stress response in mesoangioblast stem cells. Cell Death Differ 2006;13:1057-1063. (Pubitemid 43905587)
38. Meyer KC, Klatte JE, Dinh HV et al. Evidence that the bulge region is a site of relative immune privilege in human hair follicles. Br J Dermatol 2008;159:1077-1085.
39. Perin L, Sedrakyan S, Giuliani S et al. Protective effect of human amniotic fluid stem cells in an immunodeficient mouse model of acute tubular necrosis. Plos One 2010;5:e9357.
40. Petrie Aronin CE, Tuan RS. Therapeutic potential of the immunomodulatory activities of adult mesenchymal stem cells. Birth Defects Res C Embryo Today 2010;90:67-74.
41. Chauhan SK, El AJ, Ecoiffier T et al. Autoimmunity in dry eye is due to resistance of Th17 to Treg suppression. J Immunol 2009;182:1247-1252.
42. Lambiase A, Micera A, Mantelli F et al. T-helper 17 lymphocytes in ocular cicatricial pemphigoid. Mol Vis 2009;15:1449-1455.
43. Gaffen SL, Kramer JM, Yu JJ et al. The IL-17 cytokine family. Vitam Horm 2006;74:255-282.
44. Shinoda M, Hoffer BJ, Olson L. Minor immunoreactivity in GDNF-,BDNF-, or NT-3-treated substantia Nigra allografts. J Neural Transplant Plast 1997;6:83-96.
45. Chen ZY, Chen XQ, Lu CL et al. The human recombinant GDNF and study of its biological activity. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 1999;31:203-206.
46. Sakamoto T, Watabe K, Ohashi T et al. Adenoviral vector-mediated GDNF gene transfer prevents death of adult facial motoneurons. NeuroReport 2000;11:1857-1860.
47. Srinivasan S, Anitha M, Mwangi S et al. Enteric neuroblasts require the phosphatidylinositol 3-kinase/Akt/Forkhead pathway for GDNF-stimulated survival. Mol Cell Neurosci 2005;29:107-119.
48. Okun E, Saida H, Albeck M et al. Upregulation of carp GDNF mRNA by the immunomodulator AS101. Dev Comp Immunol 2006; 30:441-446.
49. Tanaka T, Oh-Hashi K, Ito M et al. Identification of a novel GDNF mRNA induced by LPS in immune cell lines. Neurosci Res 2008;61:11-17.
50. Awane M, Andres PG, Li DJ et al. NF-kappa B-inducing kinase is a common mediator of IL-17-, TNF-alpha-, And IL-1 beta-induced chemokine promoter activation in intestinal epithelial cells. J Immunol 1999; 162:5337-5344.
51. Kao CY, Chen Y, Thai P et al. IL-17 markedly up-regulates beta-defensin-2 expression in human airway epithelium via JAK and NF-kappaB signaling pathways. J Immunol 2004;173: 3482-3491. (Pubitemid 39142059)
52. Huang F, Kao CY, Wachi S et al. Requirement for both JAK-mediated PI3K signaling and ACT1/TRAF6/TAK1-dependent NF-kappaB activation by IL-17A in enhancing cytokine expression in human airway epithelial cells. J Immunol 2007;179: 6504-6513.