Melanoma differentiation associated gene-7/interleukin-24 potently induces apoptosis in human myeloid leukemia cells through a process regulated by endoplasmic reticulum stress

Molecular Pharmacology

Volumn 78, Issue 6, 2010, Pages 1096-1104

  Rahmani, Mohamed ^a   Mayo, Mandy ^a   Dash, Rupesh ^b   Sokhi, Upneet Kaur ^b   Dmitriev, Igor P ^d   Sarkar, Devanand ^a,b,c   Dent, Paul ^a,c   Curiel, David T ^d   Fisher, Paul B ^a,b,c   Grant, Steven ^a,b,c  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; CD34 ANTIGEN; GLUCOSE REGULATED PROTEIN 78; INITIATION FACTOR 2ALPHA; INTERLEUKIN 24; MIXED LINEAGE LEUKEMIA PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN IRE1; PROTEIN MCL 1; SHORT HAIRPIN RNA;

APOPTOSIS; ARTICLE; CELL STRAIN HL 60; CELL STRAIN U937; COLONY FORMING UNIT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE SILENCING; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MYELOID LEUKEMIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; UPREGULATION;

APOPTOSIS; CELL DIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; ENDOPLASMIC RETICULUM; HL-60 CELLS; HUMANS; INTERLEUKINS; LEUKEMIA, MYELOID; STEM CELLS; STRESS, PHYSIOLOGICAL; U937 CELLS;

EID: 78649911452     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.110.068007     Document Type: Article

References (40)

1. Adler HT, Chinery R, Wu DY, Kussick SJ, Payne JM, Fornace AJ Jr, and Tkachuk DC (1999) Leukemic HRX fusion proteins inhibit GADD34-induced apoptosis and associate with the GADD34 and hSNF5/INI1 proteins. Mol Cell Biol 19:7050-7060. (Pubitemid 29441887)
2. Barabé F, Kennedy JA, Hope KJ, and Dick JE (2007) Modeling the initiation and progression of human acute leukemia in mice. Science 316:600-604.
3. Bernales S, Papa FR, and Walter P (2006) Intracellular signaling by the unfolded protein response. Annu Rev Cell Dev Biol 22:487-508.
4. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, and Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2:326-332.
5. Cnop M, Ladriere L, Hekerman P, Ortis F, Cardozo AK, Dogusan Z, Flamez D, Boyce M, Yuan J, and Eizirik DL (2007) Selective inhibition of eukaryotic translation initiation factor 2 alpha dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic beta-cell dysfunction and apoptosis. J Biol Chem 282:3989-3997.
6. Dash R, Bhutia SK, Azab B, Su Z-z, Quinn BA, Kegelmen TP, Das SK, Kim K, Lee S-G, Park MA, et al. (2010a) mda-7/IL-24: a unique member of the IL-10 gene family promoting cancer-specific toxicity. Cytokine Growth Factor Rev doi:10.1016/j.cytogfr.2010.08.004.
7. Dash R, Richards JE, Su ZZ, Bhutia SK, Azab B, Rahmani M, Dasmahapatra G, Yacoub A, Dent P, Dmitriev IP, et al. (2010b) Mechanism by which Mcl-1 regulates cancer-specific apoptosis triggered by mda-7/IL-24, an IL-10-related cytokine. Cancer Res 70:5034-5045.
8. Dent P, Yacoub A, Grant S, Curiel DT, and Fisher PB (2005) MDA-7/IL-24 regulates proliferation, invasion and tumor cell radiosensitivity: a new cancer therapy? J Cell Biochem 95:712-719.
9. Derenne S, Monia B, Dean NM, Taylor JK, Rapp MJ, Harousseau JL, Bataille R, and Amiot M (2002) Antisense strategy shows that Mcl-1 rather than Bcl-2 or Bcl-x(L) is an essential survival protein of human myeloma cells. Blood 100:194-199.
10. Dong CY, Zhang F, Duan YJ, Yang BX, Lin YM, and Ma XT (2008) mda-7/IL-24 inhibits the proliferation of hematopoietic malignancies in vitro and in vivo. Exp Hematol 36:938-946.
11. Fisher PB (2005) Is mda-7/IL-24 a "magic bullet" for cancer? Cancer Res 65:10128-10138.
12. Fritsch RM, Schneider G, Saur D, Scheibel M, and Schmid RM (2007) Translational repression of MCL-1 couples stress-induced eIF2 alpha phosphorylation to mitochondrial apoptosis initiation. J Biol Chem 282:22551-22562. (Pubitemid 47267367)
13. Gupta P, Su ZZ, Lebedeva IV, Sarkar D, Sauane M, Emdad L, Bachelor MA, Grant S, Curiel DT, Dent P, et al. (2006a) mda-7/IL-24: multifunctional cancer-specific apoptosis-inducing cytokine. Pharmacol Ther 111:596-628.
14. Gupta P, Walter MR, Su ZZ, Lebedeva IV, Emdad L, Randolph A, Valerie K, Sarkar D, and Fisher PB (2006b) BiP/GRP78 is an intracellular target for MDA-7/IL-24 induction of cancer-specific apoptosis. Cancer Res 66:8182-8191.
15. Jiang H, Lin JJ, Su ZZ, Goldstein NI, and Fisher PB (1995) Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogene 11:2477-2486.
16. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, Green DR, and Newmeyer DD (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17:525-535.
17. Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, Panning B, Shokat KM, Lavail MM, and Walter P (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318:944-949.
18. Lord KA, Hoffman-Liebermann B, and Liebermann DA (1990) Sequence of MyD116 cDNA: a novel myeloid differentiation primary response gene induced by IL6. Nucleic Acids Res 18:2823.
19. Moulding DA, Giles RV, Spiller DG, White MR, Tidd DM, and Edwards SW (2000) Apoptosis is rapidly triggered by antisense depletion of MCL-1 in differentiating U937 cells. Blood 96:1756-1763.
20. Park MA, Yacoub A, Sarkar D, Emdad L, Rahmani M, Spiegel S, Koumenis C, Graf M, Curiel DT, Grant S, et al. (2008) PERK-dependent regulation of MDA-7/IL-24-induced autophagy in primary human glioma cells. Autophagy 4:513-515.
21. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, Huntington ND, Hughes PD, Michalak EM, McKimm-Breschkin J, Motoyama N, et al. (2007) ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129:1337-1349.
22. Qian W, Liu J, Tong Y, Yan S, Yang C, Yang M, and Liu X (2008) Enhanced antitumor activity by a selective conditionally replicating adenovirus combining with MDA-7/interleukin-24 for B-lymphoblastic leukemia via induction of apoptosis. Leukemia 22:361-369.
23. Rahmani M, Anderson A, Habibi JR, Crabtree TR, Mayo M, Harada H, Ferreira-Gonzalez A, Dent P, and Grant S (2009) The BH3-only protein Bim plays a critical role in leukemia cell death triggered by concomitant inhibition of the PI3K/Akt and MEK/ERK1/2 pathways. Blood 114:4507-4516.
24. Rahmani M, Dai Y, and Grant S (2002) The histone deacetylase inhibitor sodium butyrate interacts synergistically with phorbol myristate acetate (PMA) to induce mitochondrial damage and apoptosis in human myeloid leukemia cells through a tumor necrosis factor-alpha-mediated process. Exp Cell Res 277:31-47.
25. Rahmani M, Davis EM, Bauer C, Dent P, and Grant S (2005) Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves down-regulation of Mcl-1 through inhibition of translation. J Biol Chem 280:35217-35227.
26. Rahmani M, Davis EM, Crabtree TR, Habibi JR, Nguyen TK, Dent P, and Grant S (2007a) The kinase inhibitor sorafenib induces cell death through a process involving induction of endoplasmic reticulum stress. Mol Cell Biol 27:5499-5513.
27. Rahmani M, Nguyen TK, Dent P, and Grant S (2007b) The multikinase inhibitor sorafenib induces apoptosis in highly imatinib mesylate-resistant bcr/abl+ human leukemia cells in association with signal transducer and activator of transcription 5 inhibition and myeloid cell leukemia-1 down-regulation. Mol Pharmacol 72:788-795.
28. Rahmani M, Yu C, Reese E, Ahmed W, Hirsch K, Dent P, and Grant S (2003) Inhibition of PI-3 kinase sensitizes human leukemic cells to histone deacetylase inhibitor-mediated apoptosis through p44/42 MAP kinase inactivation and abrogation of p21(CIP1/WAF1) induction rather than AKT inhibition. Oncogene 22:6231-6242.
29. Ron D and Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529. (Pubitemid 46985379)
30. Sainz-Perez A, Gary-Gouy H, Gaudin F, Maarof G, Marfaing-Koka A, de Revel T, and Dalloul A (2008) IL-24 induces apoptosis of chronic lymphocytic leukemia B cells engaged into the cell cycle through dephosphorylation of STAT3 and stabilization of p53 expression. J Immunol 181:6051-6060.
31. Sainz-Perez A, Gary-Gouy H, Portier A, Davi F, Merle-Beral H, Galanaud P, and Dalloul A (2006) High Mda-7 expression promotes malignant cell survival and p38 MAP kinase activation in chronic lymphocytic leukemia. Leukemia 20:498-504.
32. Sarkar D, Su ZZ, Lebedeva IV, Sauane M, Gopalkrishnan RV, Valerie K, Dent P, and Fisher PB (2002) mda-7 (IL-24) Mediates selective apoptosis in human melanoma cells by inducing the coordinated overexpression of the GADD family of genes by means of p38 MAPK. Proc Natl Acad Sci USA 99:10054-10059.
33. Sauane M, Gopalkrishnan RV, Choo HT, Gupta P, Lebedeva IV, Yacoub A, Dent P, and Fisher PB (2004) Mechanistic aspects of mda-7/IL-24 cancer cell selectivity analysed via a bacterial fusion protein. Oncogene 23:7679-7690.
34. Schewe DM and Aguirre-Ghiso JA (2009) Inhibition of eIF2alpha dephosphorylation maximizes bortezomib efficiency and eliminates quiescent multiple myeloma cells surviving proteasome inhibitor therapy. Cancer Res 69:1545-1552.
35. 2+: a control point for apoptosis. Science 300:135-139.
36. Shu CW, Sun FC, Cho JH, Lin CC, Liu PF, Chen PY, Chang MD, Fu HW, and Lai YK (2008) GRP78 and Raf-1 cooperatively confer resistance to endoplasmic reticulum stress-induced apoptosis. J Cell Physiol 215:627-635.
37. Su ZZ, Lebedeva IV, Sarkar D, Gopalkrishnan RV, Sauane M, Sigmon C, Yacoub A, Valerie K, Dent P, and Fisher PB (2003) Melanoma differentiation associated gene-7, mda-7/IL-24, selectively induces growth suppression, apoptosis and radiosensitization in malignant gliomas in a p53-independent manner. Oncogene 22:1164-1180.
38. Wang Q, Mora-Jensen H, Weniger MA, Perez-Galan P, Wolford C, Hai T, Ron D, Chen W, Trenkle W, Wiestner A, et al. (2009) ERAD inhibitors integrate ER stress with an epigenetic mechanism to activate BH3-only protein NOXA in cancer cells. Proc Natl Acad Sci USA 106:2200-2205.
39. Watanabe R, Tambe Y, Inoue H, Isono T, Haneda M, Isobe K, Kobayashi T, Hino O, Okabe H, and Chano T (2007) GADD34 inhibits mammalian target of rapamycin signaling via tuberous sclerosis complex and controls cell survival under bioenergetic stress. Int J Mol Med 19:475-483.
40. Yang C, Tong Y, Ni W, Liu J, Xu W, Li L, Liu X, Meng H, and Qian W (2010) Inhibition of autophagy induced by overexpression of mda-7/interleukin-24 strongly augments the antileukemia activity in vitro and in vivo. Cancer Gene Ther 17:109-119.