Cyclin D3 promotes pancreatic β-cell fitness and viability in a cell cycle-independent manner and is targeted in autoimmune diabetes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 33, 2014, Pages

  Saavedra Ávila, Noemí Alejandra ^a,b   Sengupta, Upasana ^a,b   Sánchez, Begoña ^a,b   Sala, Ester ^a,b   Haba, Laura ^c   Stratmann, Thomas ^d   Verdaguer, Joan ^a,b   Mauricio, Dídac ^a,b,e   Mezquita, Belén ^d   Ropero, Ana Belén ^f   Nadal, Ángel ^f   Mora, Conchi ^a,b  

^a UNIVERSITY OF LLEIDA   (Spain)

^b UNIVERSITY OF LLEIDA   (Spain)

^c INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

^e HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^f MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D3; GLUCOSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; CELL INFILTRATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HOMEOSTASIS; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; INSULINOMA CELL LINE; LEUKOCYTE; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENE;

ANIMALS; APOPTOSIS; CELL CYCLE; CYCLIN D3; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD;

EID: 84906311291     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1323236111     Document Type: Article

References (40)

1. Itoh N, et al. (1997) Requirement of Fas for the development of autoimmune diabetes in nonobese diabetic mice. J Exp Med 186(4):613-618. (Pubitemid 27360805)
2. Eizirik DL, Mandrup-Poulsen T (2001) A choice of death - the signal-transduction of immune-mediated beta-cell apoptosis. Diabetologia 44(12):2115-2133. (Pubitemid 34015464)
3. Mauricio D, Mandrup-Poulsen T (1998) Apoptosis and the pathogenesis of IDDM: A question of life and death. Diabetes 47(10):1537-1543. (Pubitemid 28445339)
4. Watanabe A, et al. (2012) Quantitative determination of apoptosis of pancreatic β-cells in a murine model of type 1 diabetes mellitus. J Nucl Med 53(10):1585-1591.
5. Moriwaki M, et al. (1999) Fas and Fas ligand expression in inflamed islets in pancreas sections of patients with recent-onset Type I diabetes mellitus. Diabetologia 42(11):1332-1340. (Pubitemid 29500970)
6. Mandrup-Poulsen T (2003) Beta cell death and protection. Ann N Y Acad Sci 1005:32-42.
7. Pakala SV, Kurrer MO, Katz JD (1997) T helper 2 (Th2) T cells induce acute pancreatitis and diabetes in immune-compromised nonobese diabetic (NOD) mice. J Exp Med 186(2):299-306. (Pubitemid 27328030)
8. O'Brien BA, Harmon BV, Cameron DP, Allan DJ (1997) Apoptosis is the mode of beta-cell death responsible for the development of IDDM in the nonobese diabetic (NOD) mouse. Diabetes 46(5):750-757. (Pubitemid 27188250)
9. Stassi G, et al. (1997) Nitric oxide primes pancreatic beta cells for Fas-mediated destruction in insulin-dependent diabetes mellitus. J Exp Med 186(8):1193-1200. (Pubitemid 27469014)
10. Cardozo AK, Kruhøffer M, Leeman R, Orntoft T, Eizirik DL (2001) Identification of novel cytokine-induced genes in pancreatic beta-cells by high-density oligonucleotide arrays. Diabetes 50(5):909-920. (Pubitemid 32374519)
11. Wägner AM, et al. (2007) Post-translational protein modifications in type 1 diabetes: a role for the repair enzyme protein-L-isoaspartate (D-aspartate) O-methyltransferase? Diabetologia 50(3):676-681. (Pubitemid 46215512)
12. Kacheva S, Lenzen S, Gurgul-Convey E (2011) Differential effects of proinflammatory cytokines on cell death and ER stress in insulin-secreting INS1E cells and the involvement of nitric oxide. Cytokine 55(2):195-201.
13. Chen MC, Schuit F, Eizirik DL (1999) Identification of IL-1beta-induced messenger RNAs in rat pancreatic beta cells by differential display of messenger RNA. Diabetologia 42(10):1199-1203.
14. Wang Z, Sicinski P, Weinberg RA, Zhang Y, Ravid K (1996) Characterization of the mouse cyclin D3 gene: Exon/intron organization and promoter activity. Genomics 35(1):156-163. (Pubitemid 26236163)
15. Sherr CJ (1993) Mammalian G1 cyclins. Cell 73(6):1059-1065.
16. Ma Y, Yuan J, Huang M, Jove R, Cress WD (2003) Regulation of the cyclin D3 promoter by E2F1. J Biol Chem 278(19):16770-16776. (Pubitemid 36799544)
17. Stamatakos M, et al. (2010) Cell cyclins: Triggering elements of cancer or not? World J Surg Oncol 8:111.
18. Sarruf DA, et al. (2005) Cyclin D3 promotes adipogenesis through activation of peroxisome proliferator-activated receptor gamma. Mol Cell Biol 25(22):9985-9995. (Pubitemid 41572745)
19. Wei Y, et al. (2006) ATF5 increases cisplatin-induced apoptosis through up-regulation of cyclin D3 transcription in HeLa cells. Biochem Biophys Res Commun 339(2):591-596. (Pubitemid 41739708)
20. Aguilar V, Fajas L (2010) Cycling through metabolism. EMBO Mol Med 2(9):338-348.
21. Coqueret O (2002) Linking cyclins to transcriptional control. Gene 299(1-2):35-55.
22. Sicinska E, et al. (2003) Requirement for cyclin D3 in lymphocyte development and T cell leukemias. Cancer Cell 4(6):451-461. (Pubitemid 38050042)
23. Kushner JA, et al. (2005) Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 25(9):3752-3762. (Pubitemid 40559580)
24. Georgia S, et al. (2010) Cyclin D2 is essential for the compensatory β-cell hyperplastic response to insulin resistance in rodents. Diabetes 59(4):987-996.
25. Blunt T, et al. (1996) Identification of a nonsense mutation in the carboxyl-terminal region of DNA-dependent protein kinase catalytic subunit in the scid mouse. Proc Natl Acad Sci USA 93(19):10285-10290. (Pubitemid 26314614)
26. Guerder S, Picarella DE, Linsley PS, Flavell RA (1994) Costimulator B7-1 confers antigen-presenting-cell function to parenchymal tissue and in conjunction with tumor necrosis factor alpha leads to autoimmunity in transgenic mice. Proc Natl Acad Sci USA 91(11):5138-5142. (Pubitemid 24177808)
27. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103(2):239-252.
28. Andersen NA, Larsen CM, Mandrup-Poulsen T (2000) TNFalpha and IFNgamma potentiate IL-1beta induced mitogen activated protein kinase activity in rat pancreatic islets of Langerhans. Diabetologia 43(11):1389-1396.
29. Liu W, et al. (2004) Cyclin D3 interacts with human activating transcription factor 5 and potentiates its transcription activity. Biochem Biophys Res Commun 321(4):954-960. (Pubitemid 39044401)
30. Knudsen KE, Cavenee WK, Arden KC (1999) D-type cyclins complex with the androgen receptor and inhibit its transcriptional transactivation ability. Cancer Res 59(10):2297-2301. (Pubitemid 29242271)
31. Yamada K, et al. (1996) Mouse islet cell lysis mediated by interleukin-1-induced Fas. Diabetologia 39(11):1306-1312. (Pubitemid 26356058)
32. Mandrup-Poulsen T (1996) The role of interleukin-1 in the pathogenesis of IDDM. Diabetologia 39(9):1005-1029.
33. Fiaschi-Taesch NM, et al. (2013) Cytoplasmic-nuclear trafficking of G1/S cell cycle molecules and adult human β-cell replication: A revised model of human β-cell G1/S control. Diabetes 62(7):2460-2470.
34. O'Brien BA, Huang Y, Geng X, Dutz JP, Finegood DT (2002) Phagocytosis of apoptotic cells by macrophages from NOD mice is reduced. Diabetes 51(8):2481-2488. (Pubitemid 34827397)
35. Marée AF, et al. (2005) Quantifying macrophage defects in type 1 diabetes. J Theor Biol 233(4):533-551. (Pubitemid 40320599)
36. Mendelsohn AR, Hamer JD, Wang ZB, Brent R (2002) Cyclin D3 activates Caspase 2, connecting cell proliferation with cell death. Proc Natl Acad Sci USA 99(10):6871-6876. (Pubitemid 34526225)
37. Kikutani H, Makino S (1992) The murine autoimmune diabetes model: NOD and related strains. Adv Immunol 51:285-322.
38. Marzo N, et al. (2008) Cyclin-dependent kinase 4 hyperactivity promotes autoreactivity in the immune system but protects pancreatic cell mass from autoimmune destruction in the nonobese diabetic mouse model. J Immunol 180(2):1189-1198.
39. Inaba T, et al. (1992) Genomic organization, chromosomal localization, and independent expression of human cyclin D genes. Genomics 13(3):565-574.
40. Soriano S, et al. (2009) Rapid regulation of K(ATP) channel activity by 17beta-estradiol in pancreatic beta-cells involves the estrogen receptor beta and the atrial natriuretic peptide receptor. Mol Endocrinol 23(12):1973-1982.