TNFα-induced apoptosis enabled by CCN1/CYR61: Pathways of reactive oxygen species generation and cytochrome C release

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Juric, Vladislava ^a,b   Chen, Chih Chiun ^a   Lau, Lester F ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE RICH PROTEIN 61; CYTOCHROME C; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUTRAL SPHINGOMYELINASE 1; PHOSPHODIESTERASE; PROTEIN P53; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYCLOHEXIMIDE; LRP1 PROTEIN, HUMAN; SPHINGOMYELIN PHOSPHODIESTERASE;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; NEWBORN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS REGULATION; BIOLOGICAL MODEL; DRUG EFFECT; METABOLISM; SECRETION; SIGNAL TRANSDUCTION;

APOPTOSIS; CYCLOHEXIMIDE; CYSTEINE-RICH PROTEIN 61; CYTOCHROMES C; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MODELS, BIOLOGICAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SPHINGOMYELIN PHOSPHODIESTERASE; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84857154364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031303     Document Type: Article

References (58)

1. Aggarwal BB, (2003) Signalling pathways of the TNF superfamily: a double-edged sword. Nat Rev Immunol 3: 745-756.
2. Yin M, Wheeler MD, Kono H, Bradford BU, Gallucci RM, et al. (1999) Essential role of tumor necrosis factor alpha in alcohol-induced liver injury in mice. Gastroenterology 117: 942-952.
3. Maeda S, Chang L, Li ZW, Luo JL, Leffert H, et al. (2003) IKKbeta is required for prevention of apoptosis mediated by cell-bound but not by circulating TNFalpha. Immunity 19: 725-737.
4. Rudiger HA, Clavien PA, (2002) Tumor necrosis factor alpha, but not Fas, mediates hepatocellular apoptosis in the murine ischemic liver. Gastroenterology 122: 202-210.
5. Tokushige K, Yamaguchi N, Ikeda I, Hashimoto E, Yamauchi K, et al. (2000) Significance of soluble TNF receptor-I in acute-type fulminant hepatitis. Am J Gastroenterol 95: 2040-2046.
6. Micheau O, Tschopp J, (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114: 181-190.
7. Gaur U, Aggarwal BB, (2003) Regulation of proliferation, survival and apoptosis by members of the TNF superfamily. Biochem Pharmacol 66: 1403-1408.
8. Chang L, Kamata H, Solinas G, Luo JL, Maeda S, et al. (2006) The E3 ubiquitin ligase itch couples JNK activation to TNFα-induced cell death by inducing c-FLIP(L) turnover. Cell 124: 601-613.
9. Wang J, Ford HR, Grishin AV, (2010) NF-kappaB-mediated expression of MAPK phosphatase-1 is an early step in desensitization to TLR ligands in enterocytes. Mucosal Immunol 3: 523-534.
10. Pham CG, Bubici C, Zazzeroni F, Papa S, Jones J, et al. (2004) Ferritin heavy chain upregulation by NF-kappaB inhibits TNFalpha-induced apoptosis by suppressing reactive oxygen species. Cell 119: 529-542.
11. Werner AB, de VE, Tait SW, Bontjer I, Borst J, (2002) Bcl-2 family member Bfl-1/A1 sequesters truncated bid to inhibit is collaboration with pro-apoptotic Bak or Bax. J Biol Chem 277: 22781-22788.
12. Jun JI, Lau LF, (2011) Taking aim at the extracellular matrix: CCN proteins as emerging therapeutic targets. Nat Rev Drug Discov 10: 945-963.
13. Chen CC, Juric V, Lau LF, (2011) The Extracellular Matrix Protein CCN1 Dictates TNFα and FasL Cytotoxicity In Vivo. Adv Exp Med Biol 691: 595-603.
14. Chen C-C, Young JL, Monzon RI, Chen N, Todorovic V, et al. (2007) Cytotoxicity of TNFα is regulated by Integrin-Mediated Matrix Signaling. EMBO J 26: 1257-1267.
15. Chen C-C, Lau LF, (2009) Functions and Mechanisms of Action of CCN Matricellular Proteins. Int J Biochem Cell Biol 41: 771-783.
16. Lau LF, (2011) CCN1/CYR61: the very model of a modern matricellular protein. Cell Mol Life Sci 68: 3149-3163.
17. Juric V, Chen CC, Lau LF, (2009) Fas-Mediated Apoptosis is Regulated by the Extracellular Matrix Protein CCN1 (CYR61) in vitro and in vivo. Mol Cell Biol 29: 3266-3279.
18. Lillis AP, Van Duyn LB, Murphy-Ullrich JE, Strickland DK, (2008) LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol Rev 88: 887-918.
19. Segarini PR, Nesbitt JE, Li D, Hayes LG, Yates JR III, et al. (2001) The low density lipoprotein receptor-related protein/α2-Macroglobulin receptor is a receptor for connective tissue growth factor (CTGF). J Biol Chem 276: 40659-40667.
20. Gao R, Brigstock DR, (2003) Low density lipoprotein receptor-related protein (LRP) is a heparin-dependent adhesion receptor for connective tissue growth factor (CTGF) in rat activated hepatic stellate cells. Hepatol Res 27: 214-220.
21. Yang M, Huang H, Li J, Li D, Wang H, (2004) Tyrosine phosphorylation of the LDL receptor-related protein (LRP) and activation of the ERK pathway are required for connective tissue growth factor to potentiate myofibroblast differentiation. FASEB J 18: 1920-1921.
22. Herz J, Strickland DK, (2001) LRP: a multifunctional scavenger and signaling receptor. J Clin Invest 108: 779-784.
23. Willnow TE, Rohlmann A, Horton J, Otani H, Braun JR, et al. (1996) RAP, a specialized chaperone, prevents ligand-induced ER retention and degradation of LDL receptor-related endocytic receptors. EMBO J 15: 2632-2639.
24. Gao R, Brigstock DR, (2004) Connective tissue growth factor (CCN2) induces adhesion of rat activated hepatic stellate cells by binding of its C-terminal domain to integrin αvβ3 and heparan sulfate proteoglycan. J Biol Chem 279: 8848-8855.
25. Mercurio S, Latinkic BV, Itasaki N, Krumlauf R, Smith JC, (2004) Connective-tissue growth factor modulates WNT signalling and interacts with the WNT receptor complex. Development 131: 2137-2147.
26. Lillis AP, Mikhailenko I, Strickland DK, (2005) Beyond endocytosis: LRP function in cell migration, proliferation and vascular permeability. J Thromb Haemost 3: 1884-1893.
27. Schutze S, Tchikov V, Schneider-Brachert W, (2008) Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat Rev Mol Cell Biol 9: 655-662.
28. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, et al. (2001) ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2: 222-228.
29. Kamata H, Honda S, Maeda S, Chang L, Hirata H, et al. (2005) Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120: 649-661.
30. Son Y, Cheong YK, Kim NH, Chung HT, Kang DG, et al. (2011) Mitogen-Activated Protein Kinases and Reactive Oxygen Species: How Can ROS Activate MAPK Pathways? J Signal Transduct 2011: 792639.
31. Valladares A, Alvarez AM, Ventura JJ, Roncero C, Benito M, et al. (2000) p38 mitogen-activated protein kinase mediates tumor necrosis factor-alpha-induced apoptosis in rat fetal brown adipocytes. Endocrinology 141: 4383-4395.
32. Roulston A, Reinhard C, Amiri P, Williams LT, (1998) Early activation of c-Jun N-terminal kinase and p38 kinase regulate cell survival in response to tumor necrosis factor alpha. J Biol Chem 273: 10232-10239.
33. Ghatan S, Larner S, Kinoshita Y, Hetman M, Patel L, et al. (2000) p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons. J Cell Biol 150: 335-347.
34. Green DR, Kroemer G, (2009) Cytoplasmic functions of the tumour suppressor p53. Nature 458: 1127-1130.
35. Jun J-I, Lau LF, (2010) The Matricellular Protein CCN1/CYR61 Induces Fibroblast Senescence and Restricts Fibrosis in Cutaneous Wound Healing. Nat Cell Biol 12: 676-685.
36. Schafer T, Scheuer C, Roemer K, Menger MD, Vollmar B, (2003) Inhibition of p53 protects liver tissue against endotoxin-induced apoptotic and necrotic cell death. FASEB J 17: 660-667.
37. Piguet PF, Vesin C, Guo J, Donati Y, Barazzone C, (1998) TNF-induced enterocyte apoptosis in mice is mediated by the TNF receptor 1 and does not require p53. Eur J Immunol 28: 3499-3505.
38. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, et al. (2003) p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11: 577-590.
39. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, et al. (2004) Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303: 1010-1014.
40. Todorovic V, Chen C-C, Hay N, Lau LF, (2005) The matrix protein CCN1 (CYR61) induces apoptosis in fibroblasts. J Cell Biol 171: 559-568.
41. Juric V, Chen CC, Lau LF, (2009) Fas-mediated apoptosis is regulated by the extracellular matrix protein CCN1 (CYR61) in vitro and in vivo. Mol Cell Biol 29: 3266-3279.
42. Zumbansen M, Stoffel W, (2002) Neutral sphingomyelinase 1 deficiency in the mouse causes no lipid storage disease. Mol Cell Biol 22: 3633-3638.
43. Esposito E, Cuzzocrea S, (2009) TNF-alpha as a therapeutic target in inflammatory diseases, ischemia-reperfusion injury and trauma. Curr Med Chem 16: 3152-3167.
44. Wang L, Du F, Wang X, (2008) TNF-alpha induces two distinct caspase-8 activation pathways. Cell 133: 693-703.
45. Chen CC, Lau LF, (2010) Deadly liaisons: fatal attraction between CCN matricellular proteins and the tumor necrosis factor family of cytokines. J Cell Commun Signal 4: 63-69.
46. Gomez-Reino JJ, Carmona L, Valverde VR, Mola EM, Montero MD, (2003) Treatment of rheumatoid arthritis with tumor necrosis factor inhibitors may predispose to significant increase in tuberculosis risk: a multicenter active-surveillance report. Arthritis Rheum 48: 2122-2127.
47. Lubel JS, Testro AG, Angus PW, (2007) Hepatitis B virus reactivation following immunosuppressive therapy: guidelines for prevention and management. Intern Med J 37: 705-712.
48. Brown SL, Greene MH, Gershon SK, Edwards ET, Braun MM, (2002) Tumor necrosis factor antagonist therapy and lymphoma development: twenty-six cases reported to the Food and Drug Administration. Arthritis Rheum 46: 3151-3158.
49. Levine AJ, Oren M, (2009) The first 30 years of p53: growing ever more complex. Nat Rev Cancer 9: 749-758.
50. Wagner EF, Nebreda AR, (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9: 537-549.
51. Chen C-C, Mo F-E, Lau LF, (2001) The angiogenic inducer Cyr61 induces a genetic program for wound healing in human skin fibroblasts. J Biol Chem 276: 47329-47337.
52. Jensen JK, Dolmer K, Schar C, Gettins PG, (2009) Receptor-associated protein (RAP) has two high-affinity binding sites for the low-density lipoprotein receptor-related protein (LRP): consequences for the chaperone functions of RAP. Biochem J 421: 273-282.
53. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, et al. (2004) Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 16: 819-830.
54. Ubezio P, Civoli F, (1994) Flow cytometric detection of hydrogen peroxide production induced by doxorubicin in cancer cells. Free Radic Biol Med 16: 509-516.
55. Uggeri J, Gatti R, Belletti S, Scandroglio R, Corradini R, et al. (2004) Calcein-AM is a detector of intracellular oxidative activity. Histochem Cell Biol 122: 499-505.
56. Li Y, Lu W, Bu G, (2003) Essential role of the low density lipoprotein receptor-related protein in vascular smooth muscle cell migration. FEBS Lett 555: 346-350.
57. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, et al. (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 21: 635-637.
58. Hublitz P, Kunowska N, Mayer UP, Muller JM, Heyne K, et al. (2005) NIR is a novel INHAT repressor that modulates the transcriptional activity of p53. Genes Dev 19: 2912-2924.