Adjuvant immunotherapy increases β cell regenerative factor Reg2 in the pancreas of diabetic mice

Journal of Immunology

Volumn 185, Issue 9, 2010, Pages 5120-5129

  Huszarik, Katrina ^a,b   Wright, Benjamin ^a,b   Keller, Christina ^a,b   Nikoopour, Enayat ^a,b   Krougly, Olga ^a,b   Lee Chan, Edwin ^a,b   Qin, Hui Yu ^a,b   Cameron, Mark J ^c,d   Gurr, Werner K ^e   Hill, David J ^a   Sherwin, Robert S ^e   Kelvin, David J ^c,d   Singh, Bhagirath ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXENDIN 4; FREUND ADJUVANT; INSULIN; INTERLEUKIN 6; ISLET NEOGENESIS ASSOCIATED PROTEIN; LECTIN; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN; REGENERATION 2 PROTEIN; STREPTOZOCIN; UNCLASSIFIED DRUG; IMMUNOLOGICAL ADJUVANT; PAP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL REGENERATION; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; GENE EXPRESSION; GLUCOSE TOLERANCE TEST; IMMUNOTHERAPY; INSULIN RELEASE; INSULITIS; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STREPTOZOCIN DIABETES; UPREGULATION; ADJUVANT CHEMOTHERAPY; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG EFFECT; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION PROFILING; GENETICS; IMMUNOHISTOCHEMISTRY; INSULIN DEPENDENT DIABETES MELLITUS; METABOLISM; METHODOLOGY; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PANCREAS; PHYSIOLOGY; REGENERATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BLOTTING, WESTERN; CHEMOTHERAPY, ADJUVANT; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; FEMALE; FREUND'S ADJUVANT; GENE EXPRESSION; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; PANCREAS; PROTEINS; REGENERATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 78149485387     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001596     Document Type: Article

References (51)

1. Butler, A. E., J. Janson, S. Bonner-Weir, R. Ritzel, R. A. Rizza, and P. C. Butler. 2003. β-Cell deficit and increased b-cell apoptosis in humans with type 2 diabetes. Diabetes 52:102-110.
2. Bhushan, R., K. E. Elkind-Hirsch, M. Bhushan, W. J. Butler, K. Duncan, and O. Marrioneaux. 2009. Improved glycemic control and reduction of cardiometabolic risk factors in subjects with type 2 diabetes and metabolic syndrome treated with exenatide in a clinical practice setting. Diabetes Technol. Ther. 11:353-359.
3. Perfetti, R., J. Zhou, M. E. Doyle, and J. M. Egan. 2000. Glucagon-like peptide-1 induces cell proliferation and pancreatic-duodenum homeobox-1 expression and increases endocrine cell mass in the pancreas of old, glucose-intolerant rats. Endocrinology 141:4600-4605.
4. Rafaeloff, R., S. W. Barlow, L. Rosenberg, and A. I. Vinik. 1995. Expression of Reg gene in the Syrian golden hamster pancreatic islet regeneration model. Diabetologia 38:906-913.
5. Seaberg, R. M., S. R. Smukler, T. J. Kieffer, G. Enikolopov, Z. Asghar, M. B. Wheeler, G. Korbutt, and D. van der Kooy. 2004. Clonal identification of multipotent precursors from adult mouse pancreas that generate neural and pancreatic lineages. Nat. Biotechnol. 22:1115-1124.
6. Dor, Y., J. Brown, O. I. Martinez, and D. A. Melton. 2004. Adult pancreatic b-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429:41-46.
7. Thorel, F., V. Népote, I. Avril, K. Kohno, R. Desgraz, S. Chera, and P. L. Herrera. 2010. Conversion of adult pancreatic α-cells to β-cells after extreme β-cell loss. Nature 464:1149-1154.
8. Sreenan, S., A. J. Pick, M. Levisetti, A. C. Baldwin, W. Pugh, and K. S. Polonsky. 1999. Increased β-cell proliferation and reduced mass before diabetes onset in the nonobese diabetic mouse. Diabetes 48:989-996.
9. Liu, J. L., W. Cui, B. Li, and Y. Lu. 2008. Possible roles of reg family proteins in pancreatic islet cell growth. Endocr. Metab. Immune Disord. Drug Targets 8:1-10.
10. Terazono, K., H. Yamamoto, S. Takasawa, K. Shiga, Y. Yonemura, Y. Tochino, and H. Okamoto. 1988. A novel gene activated in regenerating islets. J. Biol. Chem. 263:2111-2114.
11. Zhang, Y. W., L. S. Ding, and M. D. Lai. 2003. Reg gene family and human diseases. World J. Gastroenterol. 9:2635-2641.
12. Castellarin, M. L., M. Petropavlovskaia, M. A. Lipsett, and L. Rosenberg. 2007. The identification and sequence analysis of a new Reg3g and Reg2 in the Syrian golden hamster. Biochim. Biophys. Acta 1769:579-585.
13. Taylor-Fishwick, D. A., S. Rittman, H. Kendall, L. Roy, W. Shi, Y. Cao, G. L. Pittenger, and A. I. Vinik. 2003. Cloning genomic INGAP: a Reg-related family member with distinct transcriptional regulation sites. Biochim. Biophys. Acta 1638:83-89.
14. Unno, M., K. Nata, N. Noguchi, Y. Narushima, T. Akiyama, T. Ikeda, K. Nakagawa, S. Takasawa, and H. Okamoto. 2002. Production and characterization of Reg knockout mice: reduced proliferation of pancreatic β-cells in Reg knockout mice. Diabetes 51 (Suppl. 3): S478-S483.
15. Watanabe, T., Y. Yonemura, H. Yonekura, Y. Suzuki, H. Miyashita, K. Sugiyama, S. Moriizumi, M. Unno, O. Tanaka, H. Kondo, et al. 1994. Pancreatic β-cell replication and amelioration of surgical diabetes by Reg protein. Proc. Natl. Acad. Sci. USA 91:3589-3592.
16. Baeza, N., D. Sanchez, B. Vialettes, and C. Figarella. 1997. Specific reg II gene overexpression in the non-obese diabetic mouse pancreas during active diabetogenesis. FEBS Lett. 416:364-368.
17. Sanchez, D., N. Baeza, R. Blouin, C. Devaux, G. Grondin, K. Mabrouk, O. Guy-Crotte, and C. Figarella. 2000. Overexpression of the reg gene in non-obese diabetic mouse pancreas during active diabetogenesis is restricted to exocrine tissue. J. Histochem. Cytochem. 48:1401-1410.
18. Qiu, L., E. O. List, and J. J. Kopchick. 2005. Differentially expressed proteins in the pancreas of diet-induced diabetic mice. Mol. Cell. Proteomics 4:1311-1318.
19. Planas, R., A. Alba, J. Carrillo, M. C. Puertas, R. Ampudia, X. Pastor, H. Okamoto, S. Takasawa, W. Gurr, R. Pujol-Borrell, et al. 2006. Reg (regenerating) gene overexpression in islets from non-obese diabetic mice with accelerated diabetes: role of IFNβ. Diabetologia 49:2379-2387.
20. Lu, Y., A. Ponton, H. Okamoto, S. Takasawa, P. L. Herrera, and J. L. Liu. 2006. Activation of the Reg family genes by pancreatic-specific IGF-I gene deficiency and after streptozotocin-induced diabetes in mouse pancreas. Am. J. Physiol. Endocrinol. Metab. 291: E50-E58.
21. Qin, H. Y., M. W. Sadelain, C. Hitchon, J. Lauzon, and B. Singh. 1993. Complete Freund's adjuvant-induced T cells prevent the development and adoptive transfer of diabetes in nonobese diabetic mice. J. Immunol. 150:2072-2080.
22. Sadelain, M. W., H. Y. Qin, J. Lauzon, and B. Singh. 1990. Prevention of type I diabetes in NOD mice by adjuvant immunotherapy. Diabetes 39:583-589.
23. Faustman, D. L., S. D. Tran, S. Kodama, B. M. Lodde, I. Szalayova, S. Key, Z. E. Toth, and E. Mezey. 2006. Comment on papers by Chong et al., Nishio et al., and Suri et al. on diabetes reversal in NOD mice. Science 314:1243, author reply 1243.
24. Kodama, S., W. Kühtreiber, S. Fujimura, E. A. Dale, and D. L. Faustman. 2003. Islet regeneration during the reversal of autoimmune diabetes in NOD mice. Science 302:1223-1227.
25. Chong, A. S., J. Shen, J. Tao, D. Yin, A. Kuznetsov, M. Hara, and L. H. Philipson. 2006. Reversal of diabetes in non-obese diabetic mice without spleen cell-derived β cell regeneration. Science 311:1774-1775.
26. Nishio, J., J. L. Gaglia, S. E. Turvey, C. Campbell, C. Benoist, and D. Mathis. 2006. Islet recovery and reversal of murine type 1 diabetes in the absence of any infused spleen cell contribution. Science 311:1775-1778.
27. Suri, A., B. Calderon, T. J. Esparza, K. Frederick, P. Bittner, and E. R. Unanue. 2006. Immunological reversal of autoimmune diabetes without hematopoietic replacement of b cells. Science 311:1778-1780.
28. Phillips, J. M., L. O'Reilly, C. Bland, A. K. Foulis, and A. Cooke. 2007. Patients with chronic pancreatitis have islet progenitor cells in their ducts, but reversal of overt diabetes in NOD mice by anti-CD3 shows no evidence for islet regeneration. Diabetes 56:634-640.
29. Ablamunits, V., N. A. Sherry, J. A. Kushner, and K. C. Herold. 2007. Autoimmunity and β cell regeneration in mouse and human type 1 diabetes: the peace is not enough. Ann. N. Y. Acad. Sci. 1103:19-32.
30. Okamoto, H., and S. Takasawa. 2002. Recent advances in the Okamoto model: the CD38-cyclic ADP-ribose signal system and the regenerating gene protein (Reg)-Reg receptor system in b-cells. Diabetes 51 (Suppl. 3): S462-S473.
31. Young, H. Y., P. Zucker, R. A. Flavell, A. M. Jevnikar, and B. Singh. 2004. Characterization of the role of major histocompatibility complex in type 1 diabetes recurrence after islet transplantation. Transplantation 78:509-515.
32. Stephens, T. A., E. Nikoopour, B. J. Rider, M. Leon-Ponte, T. A. Chau, S. Mikolajczak, P. Chaturvedi, E. Lee-Chan, R. A. Flavell, S. M. Haeryfar, et al. 2008. Dendritic cell differentiation induced by a self-peptide derived from apolipoprotein E. J. Immunol. 181:6859-6871.
33. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res. 29: e45.
34. Gurr, W., M. Shaw, Y. Li, and R. Sherwin. 2007. RegII is a β-cell protein and autoantigen in diabetes of NOD mice. Diabetes 56:34-40.
35. + regulatory T cells in pancreatic lymph nodes in diabetic NOD mice by adjuvant immunotherapy. Transplantation 87:198-206.
36. Lenzen, S. 2008. The mechanisms of alloxan-and streptozotocin-induced diabetes. Diabetologia 51:216-226.
37. Like, A. A., and A. A. Rossini. 1976. Streptozotocin-induced pancreatic insulitis: new model of diabetes mellitus. Science 193:415-417.
38. Werling, D., and T. W. Jungi. 2003. TOLL-like receptors linking innate and adaptive immune response. Vet. Immunol. Immunopathol. 91:1-12.
39. Billiau, A., and P. Matthys. 2001. Modes of action of Freund's adjuvants in experimental models of autoimmune diseases. J. Leukoc. Biol. 70:849-860.
40. Barbosa, H., S. Bordin, L. Stoppiglia, K. Silva, M. Borelli, H. Del Zotto, J. Gagliardino, and A. Boschero. 2006. Islet neogenesis associated protein (INGAP) modulates gene expression in cultured neonatal rat islets. Regul. Pept. 136:78-84.
41. Rosenberg, L., M. Lipsett, J. W. Yoon, M. Prentki, R. Wang, H. S. Jun, G. L. Pittenger, D. Taylor-Fishwick, and A. I. Vinik. 2004. A pentadecapeptide fragment of islet neogenesis-associated protein increases b-cell mass and reverses diabetes in C57BL/6J mice. Ann. Surg. 240:875-884.
42. Dungan, K. M., J. B. Buse, and R. E. Ratner. 2009. Effects of therapy in type 1 and type 2 diabetes mellitus with a peptide derived from islet neogenesis associated protein (INGAP). Diabetes Metab. Res. Rev. 25:558-565.
43. Ogawa, N., J. F. List, J. F. Habener, and T. Maki. 2004. Cure of overt diabetes in NOD mice by transient treatment with anti-lymphocyte serum and exendin-4. Diabetes 53:1700-1705.
44. Sherry, N. A., W. Chen, J. A. Kushner, M. Glandt, Q. Tang, S. Tsai, P. Santamaria, J. A. Bluestone, A. M. Brillantes, and K. C. Herold. 2007. Exendin-4 improves reversal of diabetes in NOD mice treated with anti-CD3 monoclonal antibody by enhancing recovery of β-cells. Endocrinology 148:5136-5144.
45. Xu, G., D. A. Stoffers, J. F. Habener, and S. Bonner-Weir. 1999. Exendin-4 stimulates both β-cell replication and neogenesis, resulting in increased β-cell mass and improved glucose tolerance in diabetic rats. Diabetes 48:2270-2276.
46. Baeza, N. J., C. I. Moriscot, W. P. Renaud, H. Okamoto, C. G. Figarella, and B. H. Vialettes. 1996. Pancreatic regenerating gene overexpression in the nonobese diabetic mouse during active diabetogenesis. Diabetes 45:67-70.
47. Dusetti, N. J., G. V. Mallo, E. M. Ortiz, V. Keim, J. C. Dagorn, and J. L. Iovanna. 1996. Induction of lithostathine/reg mRNA expression by serum from rats with acute pancreatitis and cytokines in pancreatic acinar AR-42J cells. Arch. Biochem. Biophys. 330:129-132.
48. Watanabe, T., H. Yonekura, K. Terazono, H. Yamamoto, and H. Okamoto. 1990. Complete nucleotide sequence of human reg gene and its expression in normal and tumoral tissues: the reg protein, pancreatic stone protein, and pancreatic thread protein are one and the same product of the gene. J. Biol. Chem. 265:7432-7439.
49. Carrère, J., O. Guy-Crotte, E. Gaia, and C. Figarella. 1999. Immunoreactive pancreatic Reg protein in sera from cystic fibrosis patients with and without pancreatic insufficiency. Gut 44:545-551.
50. De León, D. D., C. Farzad, M. F. Crutchlow, J. Brestelli, J. Tobias, K. H. Kaestner, and D. A. Stoffers. 2006. Identification of transcriptional targets during pancreatic growth after partial pancreatectomy and exendin-4 treatment. Physiol. Genomics 24:133-143.
51. Gross, D. J., L. Weiss, I. Reibstein, J. van den Brand, H. Okamoto, A. Clark, and S. Slavin. 1998. Amelioration of diabetes in nonobese diabetic mice with advanced disease by linomide-induced immunoregulation combined with Reg protein treatment. Endocrinology 139:2369-2374.