Deletion of 12/15-Lipoxygenase Alters Macrophage and Islet Function in NOD-Alox15null Mice, Leading to Protection against Type 1 Diabetes Development

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Green Mitchell, Shamina M ^a   Tersey, Sarah A ^b   Cole, Banumathi K ^a   Ma, Kaiwen ^a   Kuhn, Norine S ^a   Cunningham, Tina Duong ^a   Maybee, Nelly A ^d   Chakrabarti, Swarup K ^a   McDuffie, Marcia ^c,d   Taylor Fishwick, David A ^a   Mirmira, Raghavendra G ^b   Nadler, Jerry L ^a,d   Morris, Margaret A ^a  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 15 LIPOXYGENASE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; STAT4 PROTEIN; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARACHIDONATE 12 LIPOXYGENASE GENE; ARACHIDONATE 15 LIPOXYGENASE GENE; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; FEMALE; GAMMA INTERFERON GENE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; IMMUNOCOMPETENT CELL; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; INTERLEUKIN 12 GENE; INTERLEUKIN 12P70 GENE; INTERLEUKIN 1BETA GENE; MACROPHAGE; MOLECULAR PATHOLOGY; MONOCYTE CHEMOTACTIC PROTEIN 1 GENE; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; SPLEEN CELL; STAT4 GENE; TUMOR NECROSIS FACTOR ALPHA GENE;

ANIMALS; ARACHIDONATE 12-LIPOXYGENASE; ARACHIDONATE 15-LIPOXYGENASE; DIABETES MELLITUS, TYPE 1; HUMANS; INSULIN; INSULIN-SECRETING CELLS; INTERLEUKIN-12; ISLETS OF LANGERHANS; MACROPHAGES; MICE; MICE, INBRED NOD; OXYGENASES;

EID: 84874339055     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056763     Document Type: Article

References (41)

1. Ziegler A-G, Nepom GT, (2010) Prediction and pathogenesis in type 1 diabetes. Immunity 32: 468-478.
2. Todd JA, (2010) Etiology of type 1 diabetes. Immunity 32: 457-467.
3. Anderson MS, Bluestone JA, (2005) The NOD mouse: a model of immune dysregulation. Ann Rev Immunol 23: 447-485.
4. McDuffie M, Maybee NA, Keller SR, Stevens BK, Garmey JC, et al. (2008) Nonobese diabetic (NOD) mice congenic for a targeted deletion of 12/15-lipoxygenase are protected from autoimmune diabetes. Diabetes 57: 199-208.
5. Kuhn H, O'Donnell VB, (2006) Inflammation and immune regulation by 12/15-lipoxygenases. Prog in Lipids Res 45: 334-356.
6. Dobrian AD, Lieb DC, Cole BK, Taylor-Fishwick DA, Chakrabarti SK, et al. (2011) Functional and pathological roles of the 12- and 15-lipoxygenases. Prog Lipid Res 50: 115-131.
7. Soberman RJ, Harper TW, Betteridge D, Lewis RA, Austen KF, (1985) Characterization and separation of the arachidonic acid 5-lipoxygenase and linoleic acid w-6 lipoxygenase (arachidonic acid 15-lipoxygenase) of human polymorphonuclear leukocytes. J Biol Chem 260: 4508-4515.
8. Chen M, Yang ZD, Smith KM, Carter JD, Nadler JL, (2005) Activation of 12-lipoxygenase in proinflammatory cytokine-mediated beta cell toxicity. Diabetologia 48: 486-495.
9. Middleton MK, Rubinstein T, Pure E, (2006) Cellular and molecular mechanisms of the selective regulation of IL-12 production by 12/15-lipoxygenase. J Immunol 176: 265-274.
10. Chakrabarti SK, Wen Y, Dobrian AD, Cole BK, Ma Q, et al. (2011) Evidence for activation of inflammtory lipoxygenase pathways in visceral adipose tissue of obese Zucker rats. Am J Physiol Endocrinol Metab 300: E175-E187.
11. Yang Z, Chen M, Ellett JD, Fialkow LB, Carter JD, et al. (2004) Autoimmune diabetes is blocked in Stat4-deficient mice. J Autoimm 22: 191-200.
12. Zhao L, Cuff CA, Moss E, Wille U, Cyrus T, et al. (2002) Selective interleukin-12 synthesis defect in 12/15-lipoxygenase-deficient macrophages associated with reduced atherosclerosis in a mouse model of familial hypercholesterolemia. J Biol Chem 277: 35350-35356.
13. Dioszeghy V, Rosas M, Maskre BH, Colmont C, Topley N, et al. (2008) 12/15-lipoxygenase regulates the inflammatory response to bacterial products in vivo. J Immunol 181: 6514-6524.
14. Bleich D, Chen S, Gu J-L, Nadler JL, (1998) The role of 12-lipoxygenase in pancreatic beta-cells. Int J Mol Med 1: 265-272.
15. Ma K, Nunemaker CS, Wu R, Chakrabarti SK, Taylor-Fishwick DA, et al. (2010) 12-lipoxygenase products reduce insulin secretion and b-cell viability in human islets. J Clin Endocrinol Metab 95: 887-893.
16. Tersey SA, Nishiki Y, Templin AT, Cabrera SM, Stull ND,et al. (in press) Islet b-cell endoplasmic reticulum stress precedes the onset of type 1 diabees in the non-obese diabetic mouse model. Diabetes.
17. Tersey SA, Cole BK, Nadler JL, Mirmira RG (2011) Pancreas-specific deletion of 12-lipoxygenase protects against islet dysfunction in mouse models of cytokine-mediated diabetes. Diabetes 71st Scientific Sessions: 117-LB.
18. Guest PC, Rhodes CJ, Hutton JC, (1989) Regulation of the biosynthesis of insulin-secretory-granule proteins. Coordinate translational control is exerted on some, but not all, granule matrix constituents. Biochem J 257: 431-437.
19. Chakrabarti SK, Cole BK, Wen Y, Keller SR, Nadler JL, (2009) 12/15-lipoxygenase products induce inflammation and impair insulin signaling in 3T3-L1 adipocytes. Obesity 17: 1657-1663.
20. Kulkarni RN, Jhala US, Winnay JN, Krajewski S, Montminy M, et al. (2004) PDX-1 haploinsufficiency limits the conpensatory islet hyperplasia that occurs in response to insulin resistance. J Clin Invest 114: 828-836.
21. Francis J, Chakrabarti SK, Garmey JC, Mirmira RG, (2005) Pdx-1 links hisotne H3-Lys-4 methylation to RNA polymerase II elongation during activation of insulin transcription. J Biol Chem 280: 36244-36253.
22. Maier B, Ogihara T, Trace AP, Tersey SA, Robbins RD, et al. (2010) The unique hypusine modification of eIF5A promotes islet beta cell inflammation and dysfunction in mice. J Clin Invest 120: 2156-2170.
23. Morris MA, McDuffie M, Nadler JL, Ley K, (2011) Prevention, but not cure, of autoimmune diabetes in a NOD.scid transfer model by FTY720 despite effective modulation of blood T cells. Autoimmunity 44: 115-128.
24. Bendelac A, Carnaud C, Boitard C, Bach J-F, (1987) Syngeneic transfer of autoimmune diabetes from diabetic NOD mice to healthy neonates: requirement for both L3T4+ and Lyt-2+ T cells. J Exp Med 166: 823-832.
25. Ishihara H, Asano T, Tsukuda K, Katagiri H, Inukai K, et al. (1993) Pancreatic beta cell line MIN6 exhibits characteristics of glucose metabolism and glucose-stimulated insulin secretion similar to those of normal islets. Diabetologia 36: 1139-1145.
26. Wolk K, Sabat R, (2006) Interleukin-22: a novel T- and NK-cell derived cytokine that regulates the biology of tissue cells. Cytokine & Growth Factor Rev 17: 367-380.
27. Taylor-Fishwick DA, Weaver JR, Grzesik W, Chakrabarti SK, Green-Mitchell SM, et al. (2012) Production and function of IL-12 in islets and beta cells. Diabetologia ePub ahead of print.
28. Wen Y, Gu J, Vandenhoff GE, Liu X, Nadler JL, (2008) Role of 12/15-lipoxygenase in the expression of MCP-1 in mouse macrophages. Am J Physiol Heart Circ Physiol 294: H1933-1938.
29. Boyton RJ, Davies S, Marden C, Fantino C, Reynolds C, et al. (2005) Stat4-null non-obeses diabetic mice: protection from diabetes and experimental allergic encephalomyelitis, but with concomitant epitope spread. Int Immunol 17: 1157-1165.
30. Cetkovic-Cvrlje M, Uckun FM, (2005) Effect of targeted disruption of signal transducer and activator of transcription (Stat)4 and Stat6 genes on the autoimmune diabetes development induced by multiple low doses of streptozotocin. Clin Immunol 114: 299-306.
31. Yang Z, Chen M, Fialkow LB, Ellett JD, Wu R, et al. (2003) Inhibition of STAT4 activation by lisofylline is associated with the protection of autoimmune diabetes. Ann N Y Acad Sci 1005: 409-411.
32. Kim HS, Chung DH, (2012) TLR-4 mediated IL_12 production enhances IFN-gamma and IL-1 beta production, which inhibits TGF-beta production and promotes antibody-induced joint inflammation. Arthritis Research and Therapy 14: R210.
33. Zhu J, Jankovic D, Oler AJ, Wei G, Sharma S, et al. (2012) The transcription factor T-bet is induced by multiple pathways and prevents an endogenous Th2 cell program during Th1 cell responses. Immunity 37: 660-673.
34. Li L, He Q, Garland A, Yi Z, Aybar LT, et al. (2009) Beta cell-specific CD4+ T cell clonotypes in peripheral blood and the pancreatic islets are distinct. J Immunol 183: 7585-7591.
35. Ize-Ludlow D, Lightoot Y, Parker M, Xue S, Wasserfall C, et al. (2011) Progressive erosion of beta-cell function preceds the onset of hyperglycemia in the NOD mouse model of type 1 diabetes. Diabetes 60: 2086-2091.
36. Hagman DK, Latour MG, Chakrabarti SK, Fontes G, Amyot J, et al. (2008) Cyclical and alternating infusions of glucose and intralipid in rats inibit insulin gene expression and Pdx-1 binding in islets. Diabetes 57: 424-431.
37. Berardi MJ, Shih WM, Harrison SC, Chou JJ, (2011) Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature 476: 109-113.
38. Estil Les E, Tellez N, Soler J, Montanya E, (2009) High sensitivity of beta-cell replication to the inhibitory effects of interleukin-1beta: modulation by adenoviral overexpression of IGF2 in rat islets. J Endocrin 203: 55-63.
39. Carrington EM, Kos C, Zhan Y, Krishnamurthy B, Allison J, (2011) Reducing or increasing b-cell apoptosis without inflammation does not affect diabetes initiation in neonatal NOD mice. Eur J Immunol 41: 2238-2247.
40. Weaver JR, Holman TR, Imai Y, Jadhav A, Kenyon V, et al. (2012) Integration of pro-inflammatory cytokine, 12-lipoxygenase and NOX-1 in pancreatic islet beta cell dysfunction. Mol Cell Endo 358: 88-95.
41. Cole BK, Kuhn NS, Green-Mitchell SM, Leone KA, Raab RM, et al. (2012) 12/15-lipoxygenase signaling in the endoplasmic reticulum stress response. Am J Physiol Endocrinol Metab 302: E654-E665.