Combining MK626, a novel DPP-4 inhibitor, and low-dose monoclonal cd3 antibody for stable remission of new-onset diabetes in mice

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Ding, Lei ^a   Gysemans, Conny A ^a   Stangé, Geert ^b   Heremans, Yves ^b   Yuchi, Yixing ^b   Takiishi, Tatiana ^a   Korf, Hannelie ^a   Chintinne, Marie ^b   Carr, Richard D ^c   Heimberg, Harry ^b   Pipeleers, Daniel ^b   Mathieu, Chantal ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DIABETES RESEARCH CENTER   (Belgium)

^c MSD A/S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; DIPEPTIDYL PEPTIDASE IV INHIBITOR; MK 626; MONOCLONAL ANTIBODY CD3; PLACEBO; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; VASCULOTROPIN; ANTIDIABETIC AGENT; CD3 ANTIGEN; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL FUNCTION; CELL REGENERATION; CELL STRUCTURE; CELL VOLUME; CONTROLLED STUDY; DIABETES CONTROL; DIABETES MELLITUS; DRUG EFFECT; EFFECTOR CELL; FOXP3+ REGULATORY T LYMPHOCYTE; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; LOW DRUG DOSE; LYMPHATIC DRAINAGE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PANCREAS ISLET BETA CELL; REGULATORY T LYMPHOCYTE; REMISSION; SHORT COURSE THERAPY; SPLEEN; TISSUE DISTRIBUTION; ANIMAL; CD8+ T LYMPHOCYTE; DIABETES MELLITUS, TYPE 1; DRUG COMBINATION; DRUG EFFECTS; DRUG POTENTIATION; GENETICS; HAMSTER; IMMUNOLOGY; LYMPH NODE; PANCREAS; PATHOLOGY;

MUS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; CD8-POSITIVE T-LYMPHOCYTES; CRICETINAE; DIABETES MELLITUS, TYPE 1; DIPEPTIDYL-PEPTIDASE IV INHIBITORS; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; HYPOGLYCEMIC AGENTS; INSULIN-SECRETING CELLS; LYMPH NODES; MICE; MICE, INBRED NOD; PANCREAS; REMISSION INDUCTION; SPLEEN; T-LYMPHOCYTES, REGULATORY;

EID: 84907493895     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107935     Document Type: Article

References (49)

1. Herold KC, Gitelman SE, Ehlers MR, Gottlieb PA, Greenbaum CJ, et al. (2013) Teplizumab (Anti-CD3 mAb) Treatment Preserves C-Peptide Responses in Patients With New-Onset Type 1 Diabetes in a Randomized Controlled Trial: Metabolic and Immunologic Features at Baseline Identify a Subgroup of Responders. Diabetes 62: 3766-3774.
2. Herold KC, Gitelman SE, Masharani U, Hagopian W, Bisikirska B, et al. (2005) A single course of anti-CD3 monoclonal antibody hOKT3gamma1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2 years after onset of type 1 diabetes. Diabetes 54: 1763-1769.
3. Herold KC, Hagopian W, Auger JA, Poumian-Ruiz E, Taylor L, et al. (2002) Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N Engl J Med 346: 1692-1698.
4. Keymeulen B, Vandemeulebroucke E, Ziegler AG, Mathieu C, Kaufman L, et al. (2005) Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N Engl J Med 352: 2598-2608.
5. Keymeulen B, Walter M, Mathieu C, Kaufman L, Gorus F, et al. (2010) Fouryear metabolic outcome of a randomised controlled CD3-antibody trial in recent-onset type 1 diabetic patients depends on their age and baseline residual beta cell mass. Diabetologia 53: 614-623.
6. Wan X, Guloglu FB, Vanmorlan AM, Rowland LM, Zaghouani S, et al. (2013) Recovery from overt type 1 diabetes ensues when immune tolerance and betacell formation are coupled with regeneration of endothelial cells in the pancreatic islets. Diabetes 62: 2879-2889.
7. Sherry NA, Chen W, Kushner JA, Glandt M, Tang Q, et al. (2007) Exendin-4 improves reversal of diabetes in NOD mice treated with anti-CD3 monoclonal antibody by enhancing recovery of beta-cells. Endocrinology 148: 5136-5144.
8. Li Y, Hansotia T, Yusta B, Ris F, Halban PA, et al. (2003) Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis. J Biol Chem 278: 471-478.
9. Pospisilik JA, Martin J, Doty T, Ehses JA, Pamir N, et al. (2003) Dipeptidyl peptidase IV inhibitor treatment stimulates beta-cell survival and islet neogenesis in streptozotocin-induced diabetic rats. Diabetes 52: 741-750.
10. Xu G, Stoffers DA, Habener JF, Bonner-Weir S (1999) Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats. Diabetes 48: 2270-2276.
11. Lambeir AM, Diaz Pereira JF, Chacon P, Vermeulen G, Heremans K, et al. (1997) A prediction of DPP IV/CD26 domain structure from a physico-chemical investigation of dipeptidyl peptidase IV (CD26) from human seminal plasma. Biochim Biophys Acta 1340: 215-226.
12. Ohnuma K, Takahashi N, Yamochi T, Hosono O, Dang NH, et al. (2008) Role of CD26/dipeptidyl peptidase IV in human T cell activation and function. Front Biosci 13: 2299-2310.
13. De Meester IA, Kestens LL, Vanham GL, Vanhoof GC, Vingerhoets JH, et al. (1995) Costimulation of CD4+ and CD8+ T cells through CD26: the ADAbinding epitope is not essential for complete signaling. J Leukoc Biol 58: 325-330.
14. Ohnuma K, Yamochi T, Uchiyama M, Nishibashi K, Yoshikawa N, et al. (2004) CD26 up-regulates expression of CD86 on antigen-presenting cells by means of caveolin-1. Proc Natl Acad Sci U S A 101: 14186-14191.
15. Matteucci E, Ghimenti M, Di Beo S, Giampietro O (2011) Altered proportions of naive, central memory and terminally differentiated central memory subsets among CD4+ and CD8 + T cells expressing CD26 in patients with type 1 diabetes. J Clin Immunol 31: 977-984.
16. Masuyama J, Yoshio T, Suzuki K, Kitagawa S, Iwamoto M, et al. (1999) Characterization of the 4C8 antigen involved in transendothelial migration of CD26(hi) T cells after tight adhesion to human umbilical vein endothelial cell monolayers. J Exp Med 189: 979-990.
17. Deacon CF, Hughes TE, Holst JJ (1998) Dipeptidyl peptidase IV inhibition potentiates the insulinotropic effect of glucagon-like peptide 1 in the anesthetized pig. Diabetes 47: 764-769.
18. Lambeir AM, Durinx C, Proost P, Van Damme J, Scharpe S, et al. (2001) Kinetic study of the processing by dipeptidyl-peptidase IV/CD26 of neuropeptides involved in pancreatic insulin secretion. FEBS Lett 507: 327-330.
19. Busso N, Wagtmann N, Herling C, Chobaz-Peclat V, Bischof-Delaloye A, et al. (2005) Circulating CD26 is negatively associated with inflammation in human and experimental arthritis. Am J Pathol 166: 433-442.
20. Fadini GP, Boscaro E, Albiero M, Menegazzo L, Frison V, et al. (2010) The oral dipeptidyl peptidase-4 inhibitor sitagliptin increases circulating endothelial progenitor cells in patients with type 2 diabetes: possible role of stromal-derived factor-1alpha. Diabetes Care 33: 1607-1609.
21. Tian L, Gao J, Hao J, Zhang Y, Yi H, et al. (2010) Reversal of new-onset diabetes through modulating inflammation and stimulating beta-cell replication in nonobese diabetic mice by a dipeptidyl peptidase IV inhibitor. Endocrinology 151: 3049-3060.
22. Suarez-Pinzon WL, Cembrowski GS, Rabinovitch A (2009) Combination therapy with a dipeptidyl peptidase-4 inhibitor and a proton pump inhibitor restores normoglycaemia in non-obese diabetic mice. Diabetologia 52: 1680-1682.
23. Kim SJ, Nian C, Doudet DJ, McIntosh CH (2009) Dipeptidyl peptidase IV inhibition with MK0431 improves islet graft survival in diabetic NOD mice partially via T-cell modulation. Diabetes 58: 641-651.
24. Cabrera SM, Colvin SC, Tersey SA, Maier B, Nadler JL, et al. (2013) Effects of combination therapy with dipeptidyl peptidase-IV and histone deacetylase inhibitors in the non-obese diabetic mouse model of type 1 diabetes. Clin Exp Immunol 172: 375-382.
25. Bhattacharjee A, Allister EM, Wheeler MB (2012) MK-626, a dipeptidyl peptidase-4 inhibitor, does not improve the hyperglycemia or hyperinsulinemia of nonobese diabetic MKR mice. Can J Physiol Pharmacol 90: 663-668.
26. Vargova L, Zacharovova K, Dovolilova E, Vojtova L, Cimburek Z, et al. (2013) The effects of DPP-IV inhibition in NOD mice with overt diabetes. Folia Biol (Praha) 59: 116-122.
27. Hari Kumar KV, Shaikh A, Prusty P (2013) Addition of exenatide or sitagliptin to insulin in new onset type 1 diabetes: a randomized, open label study. Diabetes Res Clin Pract 100: e55-58.
28. Baeke F, Van Belle TL, Takiishi T, Ding L, Korf H, et al. (2012) Low doses of anti-CD3, ciclosporin A and the vitamin D analogue, TX527, synergise to delay recurrence of autoimmune diabetes in an islet-transplanted NOD mouse model of diabetes. Diabetologia 55: 2723-2732.
29. Takiishi T, Korf H, Van Belle TL, Robert S, Grieco FA, et al. (2012) Reversal of autoimmune diabetes by restoration of antigen-specific tolerance using genetically modified Lactococcus lactis in mice. J Clin Invest 122: 1717-1725.
30. Robert S, Gysemans C, Takiishi T, Korf H, Spagnuolo I, et al. (2014) Oral delivery of Glutamic Acid Decarboxylase (GAD)-65 and IL10 by Lactococcus lactis reverses diabetes in recent-onset NOD mice. Diabetes.
31. Edmondson SD, Mastracchio A, Mathvink RJ, He J, Harper B, et al. (2006) (2S,3S)-3-Amino-4-(3,3-difluoropyrrolidin-1-yl)-N,N-dimethyl-4-oxo-2-(4- [1,2,4]tr iazolo[1,5-a]-pyridin-6-ylphenyl)butanamide: a selective alpha-amino amide dipeptidyl peptidase IV inhibitor for the treatment of type 2 diabetes. J Med Chem 49: 3614-3627.
32. Chintinne M, Stange G, Denys B, Ling Z, In 't Veld P, et al. (2012) Beta cell count instead of beta cell mass to assess and localize growth in beta cell population following pancreatic duct ligation in mice. PLoS One 7: e43959.
33. Van de Casteele M, Cai Y, Leuckx G, Heimberg H (2013) Mouse beta cell proliferation is inhibited by thymidine analogue labelling. Diabetologia 56: 2647-2650.
34. Overbergh L, Valckx D, Waer M, Mathieu C (1999) Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR. Cytokine 11: 305-312.
35. Strojek K, Gorska J, Rokicka D, Szymborska-Kajanek A, Wrobel M, et al. (2014) Is there an impact of treatment with DPP-4 inhibitors on lymphocyte subpopulations in type 2 diabetic patients? Endokrynol Pol 65: 78-82.
36. Shevach EM, Davidson TS, Huter EN, Dipaolo RA, Andersson J (2008) Role of TGF-Beta in the induction of Foxp3 expression and T regulatory cell function. J Clin Immunol 28: 640-646.
37. Salvucci O, Yao L, Villalba S, Sajewicz A, Pittaluga S, et al. (2002) Regulation of endothelial cell branching morphogenesis by endogenous chemokine stromalderived factor-1. Blood 99: 2703-2711.
38. Chatenoud L, Primo J, Bach JF (1997) CD3 antibody-induced dominant self tolerance in overtly diabetic NOD mice. J Immunol 158: 2947-2954.
39. Bresson D, Togher L, Rodrigo E, Chen Y, Bluestone JA, et al. (2006) Anti-CD3 and nasal proinsulin combination therapy enhances remission from recent-onset autoimmune diabetes by inducing Tregs. J Clin Invest 116: 1371-1381.
40. Sherry NA, Kushner JA, Glandt M, Kitamura T, Brillantes AM, et al. (2006) Effects of autoimmunity and immune therapy on beta-cell turnover in type 1 diabetes. Diabetes 55: 3238-3245.
41. Ansarullah, Lu Y, Holstein M, DeRuyter B, Rabinovitch A, et al. (2013) Stimulating beta-cell regeneration by combining a GPR119 agonist with a DPPIV inhibitor. PLoS One 8: e53345.
42. Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, et al. (2004) Stromal cellderived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110: 3300-3305.
43. Chen G, Han G, Wang J, Wang R, Xu R, et al. (2008) Essential roles of TGFbeta in anti-CD3 antibody therapy: reversal of diabetes in nonobese diabetic mice independent of Foxp3+CD4+ regulatory T cells. J Leukoc Biol 83: 280-287.
44. Steinbrecher A, Reinhold D, Quigley L, Gado A, Tresser N, et al. (2001) Targeting dipeptidyl peptidase IV (CD26) suppresses autoimmune encephalomyelitis and up-regulates TGF-beta 1 secretion in vivo. J Immunol 166: 2041-2048.
45. Matteucci E, Giampietro O (2009) Dipeptidyl peptidase-4 (CD26): knowing the function before inhibiting the enzyme. Curr Med Chem 16: 2943-2951.
46. Mandapathil M, Hilldorfer B, Szczepanski MJ, Czystowska M, Szajnik M, et al. (2010) Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T cells. J Biol Chem 285: 7176-7186.
47. Fang S, Pentinmikko N, Ilmonen M, Salven P (2012) Dual action of TGF-beta induces vascular growth in vivo through recruitment of angiogenic VEGFproducing hematopoietic effector cells. Angiogenesis 15: 511-519.
48. Irving-Rodgers HF, Ziolkowski AF, Parish CR, Sado Y, Ninomiya Y, et al. (2008) Molecular composition of the peri-islet basement membrane in NOD mice: a barrier against destructive insulitis. Diabetologia 51: 1680-1688.
49. Nikolova G, Strilic B, Lammert E (2007) The vascular niche and its basement membrane. Trends Cell Biol 17: 19-25.