Galectin-3 deficiency protects pancreatic islet cells from cytokine-triggered apoptosis in vitro

Journal of Cellular Physiology

Volumn 228, Issue 7, 2013, Pages 1568-1576

  Saksida, Tamara ^a   Nikolic, Ivana ^a   Vujicic, Milica ^a   Nilsson, Ulf J ^b   Leffler, Hakon ^b   Lukic, Miodrag L ^c   Stojanovic, Ivana ^a   Stosic Grujicic, Stanislava ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b LUND UNIVERSITY   (Sweden)

^c UNIVERSITY OF KRAGUJEVAC   (Serbia)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; FAS ANTIGEN; GALECTIN 3; GAMMA INTERFERON; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL ASSAY; CELL ISOLATION; CELL SURVIVAL; CONTROLLED STUDY; DELETION MUTANT; DIABETES MELLITUS; IN VITRO STUDY; INSULIN RELEASE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET CELL; PANCREAS ISLET CELL FUNCTION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CELL SURVIVAL; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; GALECTIN 3; INFLAMMATION MEDIATORS; INSULIN-SECRETING CELLS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA;

MUS;

EID: 84875509705     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24318     Document Type: Article

References (42)

1. Acharya JD, Ghaskadbi SS. 2010. Islets and their antioxidant defense. Islets 2: 225-235.
2. Chen HY, Liu FT, Yang RY. 2005. Roles of galectin-3 in immune responses. Arch Immunol Ther Exp 53: 497-504.
3. Costes S, Broca C, Bertrand G, Lajoix AD, Bataille D, Bockaert J, Dalle S. 2006. ERK1/2 control phosphorylation and protein level of cAMP-responsive element-binding protein: A key role in glucose-mediated pancreatic beta-cell survival. Diabetes 55: 2220-2230.
4. Cumpstey I, Sundin A, Leffler H, Nilsson UJ. 2005. C2-symmetrical thiodigalactoside bis-benzamido derivatives as high-affinity inhibitors of galectin-3: Efficient lectin inhibition through double arginine-arene interactions. Angew Chem Int Ed 44: 5110-5112.
5. Di Mario U, Dotta F. 1998. Beta-cell autoimmunity Diabete Metab Rev 14: 1-2.
6. Donath MY, Ehses JA, Maedler K, Schumann DM, Ellingsgaard H, Eppler E, Reinecke M. 2005. Mechanisms of beta cell death in type 2 diabetes. Diabetes 54: S108-S113.
7. Donath MY, Storling J, Berchtold LA, Billestrup N, Mandrup-Poulsen T. 2008. Cytokines and beta-cell biology: From concept to clinical translation. Endocr Rev 29: 334-350.
8. Dumic J, Dabelic S, Flögel M. 2006. Galectin-3: An open-ended story. Biochim Biophys Acta 1760: 616-635.
9. Fernandez GC, Ilarregui JM, Rubel CJ, Toscano MA, Gómez SA, Beigier Bompadre M, Isturiz MA, Rabinovich GA, Palermo MS. 2005. Galectin-3 and soluble fibrinogen act in concert to modulate neutrophil activation and survival: Involvement of alternative MAPK pathways. Glycobiology 15: 519-527.
10. Fukumori T, Takenaka Y, Yoshii T, Kim HR, Hogan V, Inohara H, Kagawa S, Raz A. 2003. CD29 and CD7 mediate galectin-3-induced type II T-cell apoptosis. Cancer Res 63: 8302-8311.
11. Fukumori T, Takenaka Y, Oka N, Yoshii T, Hogan V, Inohara H, Kanayama HO, Kim HR, Raz A. 2004. Endogenous galectin-3 determines the routing of CD95 apoptotic signaling pathways. Cancer Res 64: 3376-3379.
12. Fukumori T, Oka N, Takenaka Y, Nangia-Makker P, Elsamman E, Kasai T, Shono M, Kanayama H, Ellerhorst J, Lotan R, Raz A. 2006. Galectin-3 regulates mitochondrial stability and antiapoptotic function in response to anticancer drug in prostate cancer. Cancer Res 66: 3114-3119.
13. Haudek KC, Spronk KJ, Voss PG, Patterson RJ, Wang JL, Arnoys EJ. 2010. Dynamics of galectin-3 in the nucleus and cytoplasm. Biochim Biophys Acta 1800: 181.
14. Henderson NC, Sethi T. 2009. The regulation of inflammation by galectin-3. Immunol Rev 230: 160-171.
15. Hsu DK, Yang RY, Pan Z, Yu L, Salomon DR, Fung-Leung WP, Liu FT. 2000. Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses. Am J Pathol 156: 1073-1083.
16. Jiang H-R, Al Rasebi Z, Mensah-Brown E, Shahin A, Xu D, Goodyear CS, Fukada SY, Liu F-T, Liew FY, Lukic ML. 2009. Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis. J Immunol 182: 1167-1173.
17. Karlsen AE, Størling ZM, Sparre T, Larsen MR, Mahmood A, Størling J, Roepstorff P, Wrzesinski K, Larsen PM, Fey S, Nielsen K, Heding P, Ricordi C, Johannesen J, Kristiansen OP, Christensen UB, Kockum I, Luthman H, Nerup J, Pociot F. 2006. Immune mediated β-cell destruction in vitro and in vivo-A pivotal role for galectin-3, Biochem Biophys Res Commun 344: 406-415.
18. Lepur A, Salomonsson E, Nilsson UJ. Leffler H. 2012. Ligand induced galectin-3 protein self-association. J Biol Chem 287: 21751-21756.
19. Loweth AC, Wiliams GT, James RFL, Scarpello JHB, Morgan NG. 1998. Human islets of Langerhans express Fas ligand and undergo apoptosis in response to interleukin-1β and Fas ligation. Diabetes 47: 727-732.
20. Maedler K, Spinas GA, Lehmann R, Sergeev P, Weber M, Fontana A, Kaiser N, Donath MY. 2001. Glucose induces beta-cell apoptosis via upregulation of the Fas receptor in human islets. Diabetes 50: 1683-1690.
21. Matarrese P, Tinari N, Semeraro ML, Natoli C, Iacobelli S, Malorni W. 2000. Galectin-3 overexpression protects from cell damage and death by influencing mitochondrial homeostasis. FEBS Lett 473: 311-315.
22. Mensah-Brown EP, Al Rabesi Z, Shahin A, Al Shamsi M, Arsenijevic N, Hsu DK, Liu FT, Lukic ML. 2009. Targeted disruption of the galectin-3 gene results in decreased susceptibility to multiple low dose streptozotocin-induced diabetes in mice. Clin Immunol 130: 83-88.
23. Nakahara S, Raz A. 2006. On the role of galectins in signal transduction. Methods Enzymol 417: 273-289.
24. Nielsen K, Kruhøffer M, Ørntoft T, Sparre T, Wang H, Wollheim C, Jørgensen MC, Nerup J, Karlsen AE. 2004. Gene expression profiles during beta cell maturation and after IL-1β exposure reveal important roles of Pdx-1 and Nkx6.1 for IL-1β sensitivity. Diabetologia 48: 2185-2199.
25. Oka N, Nakahara S, Takenaka Y, Fukumori T, Hogan V, Kanayama H, Yanagawa T, Raz A. 2005. Galectin-3 inhibits tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by activating Akt in human bladder carcinoma cells. Cancer Res 65: 7546-7553.
26. Pugliese G, Pricci F, Iacobini C, Leto G, Amadio L, Barsotti P, Frigeri L, Hsu DK, Vlassara H, Liu FT, Di-Mario D. 2001. Accelerated diabetic glomerulopathy in galectin-3/AGE receptor 3 knockout mice. FASEB J 15: 2471-2479.
27. Rabinovich GA, Toscano MA. 2009. Turning 'sweet' on immunity: Galectin-glycan interactions in immune tolerance and inflammation. Nat Rev Immunol 9: 338-352.
28. Rabinovich GA, Liu FT, Hirashima M, Anderson A. 2007. An emerging role for galectins in tuning the immune response: Lessons from experimental models of inflammatory disease, autoimmunity and cancer. Scand J Immunol 66: 143-158.
29. Radosavljevic G, Volarevic V, Jovanovic I, Milovanovic M, Pejnovic N, Arsenijevic N, Hsu DK, Lukic ML. 2012. The roles of Galectin-3 in autoimmunity and tumor progression. Immunol Res 52: 100-110.
30. Riedl SJ, Shi Y. 2004. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 5: 897-907.
31. Rydgren T, Sandler S. 2002. Efficacy of 1400W, a novel inhibitor of inducible nitric oxide synthase, in preventing interleukin-1beta-induced suppression of pancreatic islet function in vitro and multiple low-dose streptozotocin-induced diabetes in vivo . Eur J Endocrinol 147: 543-551.
32. Silva-Monteiro E, Reis Lorenzato L, Kenji Nihei O, Junqueira M, Rabinovich GA, Hsu DK, Liu FT, Savino W, Chammas R, Villa-Verde DM. 2007. Altered expression of galectin-3 induces cortical thymocyte depletion and premature exit of immature thymocytes during Trypanosoma cruzi infection. Am J Pathol 170: 546-556.
33. Sparre T, Christensen UB, Larsen PM, Fey SJ, Wrzesinski K, Roepstorff P, Mandrup-Poulsen T, Pociot F, Karlsen AE, Nerup J. 2002. IL-1β induced protein changes in diabetes prone BB rat islets of Langerhans identified by proteome analysis. Diabetologia 45: 1550-1561.
34. Sparre T, Christensen UB, Gotfredsen CF, Larsen PM, Fey SJ, Hjernø K, Roepstorff P, Pociot F, Karlsen AE, Nerup J. 2004. Changes in expression of IL-1 beta influenced proteins in transplanted islets during development of diabetes in diabetes-prone BB rats. Diabetologia 47: 892-908.
35. Stowell SR, Qian Y, Karmakar S, Koyama NS, Dias-Baruffi M, Leffler H, McEver RP, Cummings RD. 2008. Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J Immunol 180: 3091-3102.
36. Suzuki Y, Inoue T, Yoshimaru T, Ra C. 2008. Galectin-3 but not galectin-1 induces mast cell death by oxidative stress and mitochondrial permeability transition. Biochim Biophys Acta 1783: 924-934.
37. Takenaka Y, Fukumori T, Yoshii T, Oka N, Inohara H, Kim HR, Bresalier RS, Raz A. 2004. Nuclear export of phosphorylated galectin-3 regulates its antiapoptotic activity in response to chemotherapeutic drugs. Mol Cell Biol 24: 4395-4406.
38. Tsujimoto Y. 2003. Cell death regulation by the Bcl-2 protein family in the mitochondria. J Cell Physiol 195: 158-167.
39. van Kooyk Y, Rabinovich GA. 2008. Protein-glycan interactions in the control of innate and adaptive immune responses. Nat Immunol 9: 593-601.
40. Volarevic V, Milovanovic M, Ljujic B, Pejnovic N, Arsenijevic N, Nilsson U, Leffler H, Lukic ML. 2012. Galectin-3 deficiency prevents concanavalin A-induced hepatitis in mice. Hepatology 55: 1954-1964.
41. Ware CF, VanArsdale S, VanArsdale TL. 1996. Apoptosis mediated by the TNF-related cytokine and receptor families. J Cell Biochem 60: 47-55.
42. Yang H, Taylor HS, Lei C, Cheng C, Zhang W. 2011. Hormonal regulation of galectin 3 in trophoblasts and its effects on endometrium. Reprod Sci 18: 1118-1127.