Could T cells be involved in lung deterioration and hyperglycemia in cystic fibrosis?

Diabetes Research and Clinical Practice

Volumn 105, Issue 1, 2014, Pages 22-29

  Ziai, S ^a,b   Coriati, A ^a,b   Gauthier, M S ^b   Rabasa Lhoret, R ^a,b,c,d   Richter, M V ^e  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^c Montreal Diabetes Research Centre (MDRC)   (Canada)

^d CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^e UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Cystic fibrosis related diabetes; Hyperglycemia; IL 17 therapy; Lung function; Regulatory T cells; Th17 cells

Indexed keywords

INTERLEUKIN 17; VITAMIN D;

CONTROLLED STUDY; CYSTIC FIBROSIS; CYSTIC FIBROSIS RELATED DIABETES; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DETERIORATION; DIABETES MELLITUS; DIET SUPPLEMENTATION; DISEASE ASSOCIATION; HUMAN; HYPERGLYCEMIA; LUNG DISEASE; LUNG FUNCTION; PSORIASIS; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TH17 CELL; THERAPY EFFECT;

CYSTIC FIBROSIS-RELATED DIABETES; HYPERGLYCEMIA; IL-17 THERAPY; LUNG FUNCTION; REGULATORY T-CELLS; TH17 CELLS;

ANIMALS; CYSTIC FIBROSIS; HUMANS; HYPERGLYCEMIA; INTERLEUKIN-17; LUNG DISEASES; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84902551614     PISSN: 01688227     EISSN: 18728227     Source Type: Journal    
DOI: 10.1016/j.diabres.2014.03.002     Document Type: Review

References (89)

1. Costa M., Potvin S., Hammana I., Malet A., Berthiaume Y., Jeanneret A., et al. Increased glucose excursion in cystic fibrosis and its association with a worse clinical status. J Cyst Fibros 2007, 6:376-383.
2. Andersen D.H., Hodges R.G. Celiac syndrome; genetics of cystic fibrosis of the pancreas, with a consideration of etiology. Am J Dis Child 1946, 72:62-80.
3. Cystic Fibrosis Canada Canadian Cystic Fibrosis Registry 2011 Annual Report 2013, CF Statistics. http://www.cysticfibrosis.ca/en/aboutCysticFibrosis/CfStatistics [accessed 24.08.13]. http://www.cysticfibrosis.ca/en/publications/CanadianCysticFibrosisRegistry.
4. Riordan J.R., Rommens J.M., Kerem B., Alon N., Rozmahel R., Grzelczak Z., et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989, 245:1066-1073.
5. The Hospital for Sick Children Cystic Fibrosis Mutation Database 2011, http://www.genet.sickkids.on.ca/cftr/ [accessed 24.08.13].
6. Berdiev B.K., Qadri Y.J., Benos D.J. Assessment of the CFTR and ENaC association. Mol Biosyst 2009, 5:123-127.
7. Quinton P.M. Cystic fibrosis: lessons from the sweat gland. Physiology (Bethesda) 2007, 22:212-225.
8. Moyer K., Balistreri W. Hepatobiliary disease in patients with cystic fibrosis. Curr Opin Gastroenterol 2009, 25:272-278.
9. Dodge J.A., Morrison G. Diabetes mellitus in cystic fibrosis: a review. J R Soc Med 1992, 85(Suppl. 19):25-28.
10. Costa M., Potvin S., Berthiaume Y., Gauthier L., Jeanneret A., Lavoie A., et al. Diabetes: a major co-morbidity of cystic fibrosis. Diabetes Metab 2005, 31:221-232.
11. Nathan D.M. Long-term complications of diabetes mellitus. N Engl J Med 1993, 328:1676-1685.
12. Bismuth E., Laborde K., Taupin P., Velho G., Ribault V., Jennane F., et al. Glucose tolerance and insulin secretion, morbidity, and death in patients with cystic fibrosis. J Pediatr 2008, 152:540-545.
13. Soejima K., Landing B.H. Pancreatic islets in older patients with cystic fibrosis with and without diabetes mellitus: morphometric and immunocytologic studies. Pediatr Pathol 1986, 6:25-46.
14. Iannucci A., Mukai M., Johnson D., Burke B. Endocrine pancreas in cystic fibrosis: an immunohistochemical study. Hum Pathol 1984, 15:278-284.
15. Couce M., O'Brien T.D., Moran A., Roche P.C., Butler P.C. Diabetes mellitus in cystic fibrosis is characterized by islet amyloidosis. J Clin Endocrinol Metab 1996, 81:1267-1272.
16. Lanng S., Thorsteinsson B., Nerup J., Koch C. Influence of the development of diabetes mellitus on clinical status in patients with cystic fibrosis. Eur J Pediatr 1992, 151:684-687.
17. Stalvey M.S., Brusko T.M., Mueller C., Wasserfall C.H., Schatz D.A., Atkinson M.A., et al. CFTR mutations impart elevated immune reactivity in a murine model of cystic fibrosis related diabetes. Cytokine 2008, 44:154-159.
18. Hayes E., Pohl K., McElvaney N.G., Reeves E.P. The cystic fibrosis neutrophil: a specialized yet potentially defective cell. Arch Immunol Ther Exp (Warsz) 2011, 59:97-112.
19. Romeo G.R., Lee J., Shoelson S.E. Metabolic syndrome, insulin resistance, and roles of inflammation - mechanisms and therapeutic targets. Arterioscler Thromb Vasc Biol 2012, 32:1771-1776.
20. Rogers G.B., Hoffman L.R., Doring G. Novel concepts in evaluating antimicrobial therapy for bacterial lung infections in patients with cystic fibrosis. J Cyst Fibros 2011, 10:387-400.
21. Anton P., O'Connell J., O'Connell D., Whitaker L., O'Sullivan G.C., Collins J.K., et al. Mucosal subepithelial binding sites for the bacterial chemotactic peptide, formyl-methionyl-leucyl-phenylalanine (FMLP). Gut 1998, 42:374-379.
22. Hubeau C., Le Naour R., Abely M., Hinnrasky J., Guenounou M., Gaillard D., et al. Dysregulation of IL-2 and IL-8 production in circulating T lymphocytes from young cystic fibrosis patients. Clin Exp Immunol 2004, 135:528-533.
23. Moss R.B. Lymphocytes in cystic fibrosis lung disease: a tale of two immunities. Clin Exp Immunol 2004, 135:358-360.
24. Widmaier E.P., Raff H., Strang K.T. Defense mechanisms of the body. Vander's Human Physiology 2006, 712. McGraw-Hill, New York.
25. Schepers K., Arens R., Schumacher T.N. Dissection of cytotoxic and helper T cell responses. Cell Mol Life Sci 2005, 62:2695-2710.
26. Jager A., Kuchroo V.K. Effector and regulatory T-cell subsets in autoimmunity and tissue inflammation. Scand J Immunol 2012, 72:173-184.
27. Aujla S.J., Dubin P.J., Kolls J.K. Th17 cells and mucosal host defense. Semin Immunol 2007, 19:377-382.
28. Dubin P.J., Kolls J.K. Th17 cytokines and mucosal immunity. Immunol Rev 2008, 226:160-171.
29. Roep B.O., Peakman M., Diabetogenic T lymphocytes in human Type 1 diabetes. Curr Opin Immunol 2011, 23:746-753.
30. Louten J., Boniface K., de Waal Malefyt R. Development and function of TH17 cells in health and disease. J Allergy Clin Immunol 2009, 123:1004-1011.
31. Emamaullee J.A., Davis J., Merani S., Toso C., Elliott J.F., Thiesen A., et al. Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes 2009, 58:1302-1311.
32. Zhang X., Angkasekwinai P., Dong C., Tang H. Structure and function of interleukin-17 family cytokines. Protein Cell 2011, 2:26-40.
33. McAllister F., Henry A., Kreindler J.L., Dubin P.J., Ulrich L., Steele C., 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.
34. Tan H.L., Regamey N., Brown S., Bush A., Lloyd C.M., Davies J.C. The Th17 pathway in cystic fibrosis lung disease. Am J Respir Crit Care Med 2011, 184:252-258.
35. Nembrini C., Marsland B.J., Kopf M., IL-17-producing T cells in lung immunity and inflammation. J Allergy Clin Immunol 2009, 123:986-994. quiz 95-6.
36. Chen Y., Thai P., Zhao Y.H., Ho Y.S., DeSouza M.M., Wu R. Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop. J Biol Chem 2003, 278:17036-17043.
37. Quinton P.M. Cystic fibrosis: impaired bicarbonate secretion and mucoviscidosis. Lancet 2008, 372:415-417.
38. Decraene A., Willems-Widyastuti A., Kasran A., De Boeck K., Bullens D.M., Dupont L.J. Elevated expression of both mRNA and protein levels of IL-17A in sputum of stable Cystic Fibrosis patients. Respir Res 2010, 11:177.
39. Roussel L., Rousseau S. IL-17 primes airway epithelial cells lacking functional Cystic Fibrosis Transmembrane conductance Regulator (CFTR) to increase NOD1 responses. Biochem Biophys Res Commun 2009, 391:505-509.
40. Mizunoe S., Shuto T., Suzuki S., Matsumoto C., Watanabe K., Ueno-Shuto K., et al. Synergism between interleukin (IL)-17 and toll-like receptor 2 and 4 signals to induce IL-8 expression in cystic fibrosis airway epithelial cells. J Pharmacol Sci 2012, 118:512-520.
41. Brodlie M., McKean M.C., Johnson G.E., Anderson A.E., Hilkens C.M., Fisher A.J., et al. Raised interleukin-17 is immunolocalised to neutrophils in cystic fibrosis lung disease. Eur Respir J 2011, 37:1378-1385.
42. Gwyer Findlay E., Hussell T. Macrophage-mediated inflammation and disease: A focus on the lungs. Mediators Inflamm 2012, 2012:140937.
43. Dubin P.J., McAllister F., Kolls J.K. Is cystic fibrosis a Th17 disease?. Inflamm Res 2007, 56:221-227.
44. Tiringer K., Treis A., Fucik P., Gona M., Gruber S., Renner S., et al. A Th17- and Th2-skewed cytokine profile in cystic fibrosis lungs represents a potential risk factor for Pseudomonas aeruginosa infection. Am J Respir Crit Care Med 2013, 187:621-629.
45. Wang M., Yang L., Sheng X., Chen W., Tang H., Sheng H., et al. T-cell vaccination leads to suppression of intrapancreatic Th17 cells through Stat3-mediated RORgammat inhibition in autoimmune diabetes. Cell Res 2011, 21:1358-1369.
46. Yaochite J.N., Caliari-Oliveira C., Davanso M.R., Carlos D., Ribeiro Malmegrim K.C., Ribeiro de Barros Cardoso C., et al. Dynamic changes of the Th17/Tc17 and regulatory T cell populations interfere in the experimental autoimmune diabetes pathogenesis. Immunobiology 2012.
47. Joseph J., Bittner S., Kaiser F.M., Wiendl H., Kissler S. IL-17 silencing does not protect nonobese diabetic mice from autoimmune diabetes. J Immunol 2012, 188:216-221.
48. Nikoopour E., Schwartz J.A., Huszarik K., Sandrock C., Krougly O., Lee-Chan E., et al. Th17 polarized cells from nonobese diabetic mice following mycobacterial adjuvant immunotherapy delay type 1 diabetes. J Immunol 2010, 184:4779-4788.
49. Honkanen J., Nieminen J.K., Gao R., Luopajarvi K., Salo H.M., Ilonen J., et al. IL-17 immunity in human type 1 diabetes. J Immunol 2010, 185:1959-1967.
50. Arif S., Moore F., Marks K., Bouckenooghe T., Dayan C.M., Planas R., et al. Peripheral and islet interleukin-17 pathway activation characterizes human autoimmune diabetes and promotes cytokine-mediated beta-cell death. Diabetes 2011, 60:2112-2119.
51. Tahrani A.A., Bailey C.J., Del Prato S., Barnett A.H. Management of type 2 diabetes: new and future developments in treatment. Lancet 2011, 378:182-197.
52. Andriankaja O.M., Barros S.P., Moss K., Panagakos F.S., DeVizio W., Beck J., et al. Levels of serum interleukin (IL)-6 and gingival crevicular fluid of IL-1beta and prostaglandin E(2) among non-smoking subjects with gingivitis and type 2 diabetes. J Periodontol 2009, 80:307-316.
53. Osborn O., Brownell S.E., Sanchez-Alavez M., Salomon D., Gram H., Bartfai T. Treatment with an Interleukin 1 beta antibody improves glycemic control in diet-induced obesity. Cytokine 2008, 44:141-148.
54. Acosta-Rodriguez E.V., Napolitani G., Lanzavecchia A., Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immun 2007, 8:942-949.
55. Jagannathan-Bogdan M., McDonnell M.E., Shin H., Rehman Q., Hasturk H., Apovian C.M., et al. Elevated proinflammatory cytokine production by a skewed T cell compartment requires monocytes and promotes inflammation in type 2 diabetes. J Immunol 2011, 186:1162-1172.
56. Geiger T.L., Tauro S. Nature and nurture in Foxp3(+) regulatory T cell development, stability, and function. Hum Immunol 2012, 73:232-239.
57. Brusko T.M., Putnam A.L., Bluestone J.A. Human regulatory T cells: role in autoimmune disease and therapeutic opportunities. Immunol Rev 2008, 223:371-390.
58. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995, 155:1151-1164.
59. Torgerson T.R. Regulatory T cells in human autoimmune diseases. Springer Semin Immunopathol 2006, 28:63-76.
60. Gao Y., Lin F., Su J., Gao Z., Li Y., Yang J., et al. Molecular mechanisms underlying the regulation and functional plasticity of FOXP3(+) regulatory T cells. Genes Immun 2012, 13:1-13.
61. Yang X.O., Nurieva R., Martinez G.J., Kang H.S., Chung Y., Pappu B.P., et al. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 2008, 29:44-56.
62. Marwaha A.K., Crome S.Q., Panagiotopoulos C., Berg K.B., Qin H., Ouyang Q., et al. Cutting edge: Increased IL-17-secreting T cells in children with new-onset type 1 diabetes. J Immunol 2010, 185:3814-3818.
63. Zhen Y., Sun L., Liu H., Duan K., Zeng C., Zhang L., et al. Alterations of peripheral CD4+ CD25+ Foxp3+ T regulatory cells in mice with STZ-induced diabetes. Cell Mol Immunol 2012, 9:75-85.
64. Lindley S., Dayan C.M., Bishop A., Roep B.O., Peakman M., Tree T.I. Defective suppressor function in CD4(+)CD25(+) T-cells from patients with type 1 diabetes. Diabetes 2005, 54:92-99.
65. Bovenschen H.J., van de Kerkhof P.C., van Erp P.E., Woestenenk R., Joosten I., Koenen H.J. Foxp3+ regulatory T cells of psoriasis patients easily differentiate into IL-17A-producing cells and are found in lesional skin. J Invest Dermatol 2011, 131:1853-1860.
66. Dobson L., Sheldon C.D., Hattersley A.T. Conventional measures underestimate glycaemia in cystic fibrosis patients. Diabet Med 2004, 21:691-696.
67. Anzeneder L., Kircher F., Feghelm N., Fischer R., Seissler J. Kinetics of insulin secretion and glucose intolerance in adult patients with cystic fibrosis. Horm Metab Res 2011, 43:355-360.
68. Maciver N.J., Jacobs S.R., Wieman H.L., Wofford J.A., Coloff J.L., Rathmell J.C. Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival. J Leukoc Biol 2008, 84:949-957.
69. Mueller C., Braag S.A., Keeler A., Hodges C., Drumm M., Flotte T.R. Lack of cystic fibrosis transmembrane conductance regulator in CD3+ lymphocytes leads to aberrant cytokine secretion and hyperinflammatory adaptive immune responses. Am J Respir Cell Mol Biol 2011, 44:922-929.
70. Iannitti R.G., Carvalho A., Cunha C., De Luca A., Giovannini G., Casagrande A., et al. Th17/Treg imbalance in murine cystic fibrosis is linked to indoleamine 2,3-dioxygenase deficiency but corrected by kynurenines. Am J Respir Crit Care Med 2013, 187:609-620.
71. Martin T.R., Pistorese B.P., Chi E.Y., Goodman R.B., Matthay M.A. Effects of leukotriene B4 in the human lung. Recruitment of neutrophils into the alveolar spaces without a change in protein permeability. J Clin Invest 1989, 84:1609-1619.
72. Wolfenden L.L., Judd S.E., Shah R., Sanyal R., Ziegler T.R., Tangpricha V. Vitamin D and bone health in adults with cystic fibrosis. Clin Endocrinol (Oxf) 2008, 69:374-381.
73. Stephenson A., Brotherwood M., Robert R., Atenafu E., Corey M., Tullis E. Cholecalciferol significantly increases 25-hydroxyvitamin D concentrations in adults with cystic fibrosis. Am J Clin Nutr 2007, 85:1307-1311.
74. Pincikova T., Nilsson K., Moen I.E., Fluge G., Hollsing A., Knudsen P.K., et al. Vitamin D deficiency as a risk factor for cystic fibrosis-related diabetes in the Scandinavian Cystic Fibrosis Nutritional Study. Diabetologia 2011, 54:3007-3015.
75. Rosen C.J., Adams J.S., Bikle D.D., Black D.M., Demay M.B., Manson J.E., et al. The nonskeletal effects of vitamin D: an Endocrine Society scientific statement. Endocr Rev 2012, 33:456-492.
76. Pittas A.G., Lau J., Hu F.B., Dawson-Hughes B. The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis. J Clin Endocrinol Metab 2007, 92:2017-2029.
77. George P.S., Pearson E.R., Witham M.D. Effect of vitamin D supplementation on glycaemic control and insulin resistance: a systematic review and meta-analysis. Diabet Med 2012, 29:e142-e150.
78. Van Belle T.L., Gysemans C., Mathieu C. Vitamin D in autoimmune, infectious and allergic diseases: a vital player?. Best Pract Res Clin Endocrinol Metab 2011, 25:617-632.
79. Kang S.W., Kim S.H., Lee N., Lee W.W., Hwang K.A., Shin M.S., et al. 1,25-Dihyroxyvitamin D3 promotes FOXP3 expression via binding to vitamin D response elements in its conserved noncoding sequence region. J Immunol 2012, 188:5276-5282.
80. Hewison M. Vitamin D and immune function: an overview. Proc Nutr Soc 2012, 71:50-61.
81. Nkondjock A., Receveur O. Fish-seafood consumption, obesity, and risk of type 2 diabetes: an ecological study. Diabetes Metab 2003, 29:635-642.
82. Monk J.M., Jia Q., Callaway E., Weeks B., Alaniz R.C., McMurray D.N., et al. Th17 cell accumulation is decreased during chronic experimental colitis by (n-3) PUFA in Fat-1 mice. J Nutr 2012, 142:117-124.
83. Kim C.H. Regulation of FoxP3 regulatory T cells and Th17 cells by retinoids. Clin Dev Immunol 2008, 416910.
84. Manolescu D.C., Sima A., Bhat P.V. All-trans retinoic acid lowers serum retinol-binding protein 4 concentrations and increases insulin sensitivity in diabetic mice. J Nutr 2010, 140:311-316.
85. Genovese M.C., Durez P., Richards H., Supronik J., Dokoupilova E., Mazurov V., et al. Efficacy and safety of secukinumab in patients with rheumatoid arthritis: a phase II, dose-finding, double-blind, randomised, placebo controlled study. Ann Rheum Dis 2013, 72:863-869.
86. Kellner H. Targeting interleukin-17 in patients with active rheumatoid arthritis: rationale and clinical potential. Ther Adv Musculoskel Dis 2013, 5:141-152.
87. Papp K.A., Leonardi C., Menter A., Ortonne J.P., Krueger J.G., Kricorian G., et al. Brodalumab as an anti-interleukin-17-receptor antibody for psoriasis. N Engl J Med 2012, 366:1181-1189.
88. Leonardi C., Matheson R., Zachariae C., Cameron G., Li L., Edson-Heredia E., et al. Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N Engl J Med 2012, 366:1190-1199.
89. Mueller C., Keeler A., Bragg S., Menz T., Tang Q., Flotte T.R. Modulation of exaggerated-IgE allergic response by gene transfer-mediated antagonism of IL-13 and IL-17e. Mol Ther 2010, 18:511-518.