TNF-related apoptosis-inducing ligand promotes human preadipocyte proliferation via ERK1/2 activation

FASEB Journal

Volumn 29, Issue 7, 2015, Pages 3065-3075

  Funcke, Jan Bernd ^a   Zoller, Verena ^a   El Hay, Muad Abd ^a   Debatin, Klaus Michael ^a   Wabitsch, Martin ^a   Fischer Posovszky, Pamela ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

Adipocyte progenitor; Adipose tissue homeostasis; Death ligand; Noncanonical signaling

Indexed keywords

CASPASE 3; CASPASE 8; CYCLOHEXIMIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LEXATUMUMAB; MAPATUMUMAB; MITOGEN ACTIVATED PROTEIN KINASE 1; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; PROTEIN KINASE B; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; SELUMETINIB; SHORT HAIRPIN RNA; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; BENZAMIDE DERIVATIVE; BENZIMIDAZOLE DERIVATIVE; CASP8 PROTEIN, HUMAN; DIPHENYLAMINE; PROTEIN KINASE INHIBITOR; RNA; RNA, RECOMBINANT; TNFSF10 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ADIPOSE DERIVED STEM CELL; ADULT; APOPTOSIS; ARTICLE; CASE REPORT; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUMAN TISSUE; LENTIVIRINAE; PREADIPOCYTE PROLIFERATION; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SUBCUTANEOUS FAT; WESTERN BLOTTING; ADULT STEM CELL; ANALOGS AND DERIVATIVES; CELL CULTURE; CONGENITAL HEART MALFORMATION; CYTOLOGY; DRUG EFFECTS; GENETICS; GIGANTISM; HEART ARRHYTHMIA; INTELLECTUAL IMPAIRMENT; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; WHITE ADIPOCYTE; X CHROMOSOME LINKED DISORDER;

LENTIVIRUS;

ADIPOCYTES, WHITE; ADULT; ADULT STEM CELLS; ARRHYTHMIAS, CARDIAC; BENZAMIDES; BENZIMIDAZOLES; CASPASE 8; CELL PROLIFERATION; CELLS, CULTURED; DIPHENYLAMINE; FEMALE; GENETIC DISEASES, X-LINKED; GIGANTISM; HEART DEFECTS, CONGENITAL; HUMANS; INTELLECTUAL DISABILITY; MAP KINASE SIGNALING SYSTEM; NF-KAPPA B; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RNA; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84940417333     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-267278     Document Type: Article

References (55)

1. Fischer-Posovszky, P., Wabitsch, M., and Hochberg, Z. (2007) Endocrinology of adipose tissue-An update. Horm. Metab. Res. 39, 314-321
2. Sun, K., Kusminski, C. M., and Scherer, P. E. (2011) Adipose tissue remodeling and obesity. J. Clin. Invest. 121, 2094-2101
3. Rosen, E. D., and Spiegelman,B.M. (2014)Whatwe talk aboutwhen we talk about fat. Cell 156, 20-44
4. Samocha-Bonet, D., Dixit, V. D., Kahn, C. R., Leibel, R. L., Lin, X., Nieuwdorp, M., Pietilainen, K. H., Rabasa-Lhoret, R., Roden, M., Scherer,P.E.,Klein, S., and Ravussin,E. (2014)Metabolicallyhealthy and unhealthy obese-the 2013 Stock Conference report. Obes. Rev. 15, 697-708
5. Ashkenazi, A., and Salvesen, G. (2014) Regulated cell death: signaling and mechanisms. Annu. Rev. Cell Dev. Biol. 30, 337-356
6. Dickens, L. S., Boyd, R. S., Jukes-Jones, R., Hughes,M. A., Robinson, G.L., Fairall,L., Schwabe, J.W.,Cain, K., and Macfarlane,M. (2012) A death effector domain chain DISCmodel reveals a crucial role for caspase-8 chain assembly in mediating apoptotic cell death. Mol. Cell 47, 291-305
7. Schleich, K., Warnken, U., Fricker, N., Ozturk, S., Richter, P., Kammerer, K., Schnolzer, M., Krammer, P. H., and Lavrik, I. N. (2012) Stoichiometry of the CD95 death-inducing signaling complex: experimental and modeling evidence for a death effector domain chain model. Mol. Cell 47, 306-319
8. Varfolomeev, E., Maecker, H., Sharp, D., Lawrence, D., Renz, M., Vucic, D., and Ashkenazi, A. (2005) Molecular determinants of kinase pathway activation by Apo2 ligand/tumor necrosis factorrelated apoptosis-inducing ligand. J. Biol. Chem. 280, 40599-40608
9. Jin, Z., and El-Deiry, W. S. (2006) Distinct signaling pathways in TRAIL-versus tumor necrosis factor-induced apoptosis. Mol. Cell. Biol. 26, 8136-8148
10. Azijli, K.,Weyhenmeyer, B., Peters, G. J., de Jong, S., and Kruyt, F. A. (2013) Non-canonical kinase signaling by the death ligand TRAIL in cancer cells: discord in the death receptor family. Cell Death Differ. 20, 858-868
11. Lemke, J., von Karstedt, S., Zinngrebe, J., and Walczak, H. (2014) Getting TRAIL back on track for cancer therapy. Cell Death Differ. 21, 1350-1364
12. Spierings, D. C., de Vries, E. G., Vellenga, E., van den Heuvel, F. A., Koornstra, J. J., Wesseling, J., Hollema, H., and de Jong, S. (2004) Tissue distribution of the death ligand TRAIL and its receptors. J. Histochem. Cytochem. 52, 821-831
13. Choi, J. W., Song, J. S., and Pai, S. H. (2004) Associations of serum TRAIL concentrations, anthropometric variables, and serum lipid parameters in healthy adults. Ann. Clin. Lab. Sci. 34, 400-404
14. Keuper,M.,Wernstedt Asterholm, I., Scherer, P. E., Westhoff,M. A., Moller, P., Debatin, K. M., Strauss, G., Wabitsch, M., and Fischer-Posovszky, P. (2013) TRAIL (TNF-related apoptosisinducing ligand) regulates adipocyte metabolism by caspasemediated cleavage of PPARgamma. Cell Death Dis. 4, e474
15. Hotamisligil, G. S., Shargill, N. S., and Spiegelman, B. M. (1993) Adipose expression of tumor necrosis factor-Alpha: direct role in obesity-linked insulin resistance. Science 259, 87-91
16. Wueest, S., Rapold, R. A., Schumann, D. M., Rytka, J. M., Schildknecht, A., Nov, O., Chervonsky, A. V., Rudich, A., Schoenle, E. J., Donath, M. Y., and Konrad, D. (2010) Deletion of Fas in adipocytes relieves adipose tissue inflammation and hepatic manifestations of obesity in mice. J. Clin. Invest. 120, 191-202
17. Hauner, H., Skurk, T., and Wabitsch, M. (2001) Cultures of human adipose precursor cells. Methods Mol. Biol. 155, 239-247
18. Wabitsch, M., Brenner, R. E., Melzner, I., Braun, M., Moller, P., Heinze, E.,Debatin,K.M., and Hauner, H. (2001)Characterization of a human preadipocyte cell strain with high capacity for adipose differentiation. Int. J. Obes. Relat. Metab. Disord. 25, 8-15
19. Nicoletti, I.,Migliorati,G.,Pagliacci,M.C.,Grignani, F., and Riccardi, C. (1991) A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139, 271-279
20. Fischer-Posovszky,P.,Tornqvist,H.,Debatin,K.M., and Wabitsch,M. (2004) Inhibition of death-receptor mediated apoptosis in human adipocytes by the insulin-like growth factor I (IGF-I)/IGF-I receptor autocrine circuit. Endocrinology 145, 1849-1859
21. Andrews, N. C., and Faller, D. V. (1991) A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19, 2499
22. Kasperczyk, H., La Ferla-Bruhl, K., Westhoff, M. A., Behrend, L., Zwacka, R.M., Debatin, K.M., and Fulda, S. (2005) Betulinic acid as new activator of NF-kappaB: molecular mechanisms and implications for cancer therapy. Oncogene 24, 6945-6956
23. Fischer-Posovszky,P.,Newell, F. S.,Wabitsch,M., and Tornqvist,H.E. (2008) Human SGBS cells-A unique tool for studies of human fat cell biology. Obes. Facts 1, 184-189
24. Mader, I., Wabitsch, M., Debatin, K. M., Fischer-Posovszky, P., and and Fulda, S. (2010) Identification of a novel proapoptotic function of resveratrol in fat cells: SIRT1-independent sensitization to TRAILinduced apoptosis. FASEB J. 24, 1997-2009
25. Jones, J. I., and Clemmons, D. R. (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16, 3-34
26. Gallagher, E. J., and LeRoith, D. (2010) The proliferating role of insulin and insulin-like growth factors in cancer. Trends in endocrinology and metabolism. Trends Endocrinol. Metab. 21, 610-618
27. Isakson, P., Hammarstedt, A., Gustafson, B., and Smith, U. (2009) Impaired preadipocyte differentiation in human abdominal obesity: role ofWnt, tumor necrosis factor-Alpha, and inflammation. Diabetes 58, 1550-1557
28. Rippo, M. R., Babini, L., Prattichizzo, F., Graciotti, L., Fulgenzi, G., Tomassoni Ardori, F., Olivieri, F., Borghetti, G., Cinti, S., Poloni, A., Fazioli, F., and Procopio, A. D. (2013) Low FasL levels promote proliferation of human bone marrow-derived mesenchymal stem cells, higher levels inhibit their differentiation into adipocytes. Cell Death Dis. 4, e594
29. Kras,K.M.,Hausman,D.B., and Martin,R. J. (2000)Tumor necrosis factor-Alpha stimulates cell proliferation in adipose tissue-derived stromal-vascular cell culture: promotion of adipose tissue expansion by paracrine growth factors. Obes. Res. 8, 186-193
30. Hausman,D.B., DiGirolamo,M., Bartness, T. J.,Hausman, G. J., and Martin, R. J. (2001) The biology of white adipocyte proliferation. Obes. Rev. 2, 239-254
31. Wiley, S. R., Schooley, K., Smolak, P. J., Din, W. S., Huang, C. P., Nicholl, J.K., Sutherland, G.R., Smith, T.D., Rauch, C., Smith, C. A., et al. (1995) Identification and characterization of a newmember of the TNF family that induces apoptosis. Immunity 3, 673-682
32. Pitti, R. M., Marsters, S. A., Ruppert, S., Donahue, C. J., Moore, A., and Ashkenazi, A. (1996) Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271, 12687-12690
33. Falschlehner, C., Schaefer, U., and Walczak, H. (2009) Following TRAIL's path in the immune system. Immunology 127, 145-154
34. Zauli, G., and Secchiero, P. (2006) The role of the TRAIL/TRAIL receptors system in hematopoiesis and endothelial cell biology. Cytokine Growth Factor Rev. 17, 245-257
35. Kavurma, M. M., and Bennett, M. R. (2008) Expression, regulation and function of trail in atherosclerosis. Biochem. Pharmacol. 75, 1441-1450
36. Secchiero, P., Gonelli, A., Carnevale, E., Milani, D., Pandolfi, A., Zella, D., and Zauli, G. (2003) TRAIL promotes the survival and proliferation of primary human vascular endothelial cells by activating the Akt and ERK pathways. Circulation 107, 2250-2256
37. Secchiero, P., Zerbinati, C., Rimondi, E., Corallini, F.,Milani, D., Grill, V., Forti, G., Capitani, S., and Zauli, G. (2004) TRAIL promotes the survival, migration and proliferation of vascular smooth muscle cells. Cell. Mol. Life Sci. 61, 1965-1974
38. Kavurma, M. M., Schoppet, M., Bobryshev, Y. V., Khachigian, L. M., and Bennett, M. R. (2008) TRAIL stimulates proliferation of vascular smooth muscle cells via activation of NF-kappaB and induction of insulin-like growth factor-1 receptor. J. Biol. Chem. 283, 7754-7762
39. Chan, J., Prado-Lourenco, L., Khachigian, L. M., Bennett, M. R., Di Bartolo, B. A., and Kavurma, M. M. (2010) TRAIL promotes VSMC proliferation and neointima formation in a FGF-2-, Sp1 phosphorylation-, and NFkappaB-dependent manner. Circ. Res. 106, 1061-1071
40. Belyanskaya, L. L., Ziogas, A., Hopkins-Donaldson, S., Kurtz, S., Simon, H. U., Stahel, R., and Zangemeister-Wittke, U. (2008) TRAILinduced survival and proliferation of SCLC cells ismediated by ERK and dependent on TRAIL-R2/DR5 expression in the absence of caspase-8. Lung Cancer 60, 355-365
41. Vilimanovich, U., and Bumbasirevic, V. (2008) TRAIL induces proliferation of human glioma cells by c-FLIPL-mediated activation of ERK1/2. Cell. Mol. Life Sci. 65, 814-826
42. Morel, J., Audo, R., Hahne, M., and Combe, B. (2005) Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) induces rheumatoid arthritis synovial fibroblast proliferation through mitogen-Activated protein kinases and phosphatidylinositol 3-kinase/Akt. J. Biol. Chem. 280, 15709-15718
43. Audo,R.,Combe,B.,Coulet,B.,Morel, J., and Hahne,M. (2009)The pleiotropic effect of TRAIL on tumor-like synovial fibroblasts from rheumatoidarthritis patients ismediated by caspases. Cell DeathDiffer. 16, 1227-1237
44. Keuper, M., Asterholm, I., Scherer, P., Wolf, A. M., Knippschild, U., Wabitsch,M., and Fischer-Posovszky, P. (2011) TRAIL (TNF related apoptosis inducing ligand) affects adipogenic differentiation and adipocyte metabolism. Horm. Res. Paediatr. 76, 20-48
45. Baer,P.C. (2014)Adipose-derivedmesenchymal stromal/stemcells: Anupdate ontheir phenotype invivo andinvitro.World J. StemCells 6, 256-265
46. Secchiero, P., and Zauli, G. (2008) The puzzling role of TRAIL in endothelial cell biology. Arterioscler. Thromb. Vasc. Biol. 28, e4; author reply e5-e6
47. O'Brien, L. A., Richardson, M. A., Berg, D. T., Gerlitz, B., Gupta, A., and Grinnell, B. W. (2008) The puzzling role of TRAIL in endothelial cell biology. Arterioscler. Thromb. Vasc. Biol. 28, e5-e6
48. Martinez, F. O., Gordon, S., Locati, M., and Mantovani, A. (2006) Transcriptional profiling of the human monocyte-to-macrophage differentiationand polarization: newmolecules and patterns of gene expression. J. Immunol. 177, 7303-7311
49. Ashley, D. T., O'Sullivan, E. P., Davenport, C., Devlin, N., Crowley, R. K., McCaffrey, N., Moyna, N. M., Smith, D., and O'Gorman, D. J. (2011) Similar to adiponectin, serum levels of osteoprotegerin are associated with obesity in healthy subjects. Metabolism 60, 994-1000
50. Brombo, G., Volpato, S., Secchiero, P., Passaro, A., Bosi, C., Zuliani, G., and Zauli,G. (2013)Associationof solubleTumornecrosis factor-Related Apoptosis-Inducing Ligand (TRAIL) with central adiposity and low-density lipoprotein cholesterol. PLoS ONE 8, e58225
51. DiBartolo,B. A., Chan, J., Bennett,M. R., Cartland, S., Bao, S., Tuch, B. E., and Kavurma, M. M. (2011) TNF-related apoptosis-inducing ligand (TRAIL) protects against diabetes and atherosclerosis in Apoe (-)/(-) mice. Diabetologia 54, 3157-3167
52. Bernardi, S., Zauli, G., Tikellis, C., Candido, R., Fabris, B., Secchiero, P., Cooper,M. E., and Thomas,M. C. (2012) TNF-related apoptosisinducing ligand significantly attenuates metabolic abnormalities in high-fat-fed mice reducing adiposity and systemic inflammation. Clin. Sci. 123, 547-555
53. Lamhamedi-Cherradi, S. E., Zheng, S. J.,Maguschak, K. A., Peschon, J., and Chen, Y. H. (2003) Defective thymocyte apoptosis and accelerated autoimmune diseases in TRAIL2/2 mice. Nat. Immunol. 4, 255-260
54. Mi,Q. S., Ly,D., Lamhamedi-Cherradi, S.E., Salojin, K. V.,Zhou,L., Grattan,M.,Meagher,C., Zucker, P., Chen, Y.H., Nagle, J., Taub,D., and Delovitch, T. L. (2003) Blockade of tumor necrosis factorrelated apoptosis-inducing ligand exacerbates type 1 diabetes in NOD mice. Diabetes 52, 1967-1975
55. Zauli, G., Toffoli, B., di Iasio, M. G., Celeghini, C., Fabris, B., and Secchiero, P. (2010) Treatment with recombinant tumor necrosis factor-related apoptosis-inducing ligand alleviates the severity of streptozotocin-induced diabetes. Diabetes 59, 1261-1265