Dying tumor cells stimulate proliferation of living tumor cells via caspase-dependent protein kinase Cδ activation in pancreatic ductal adenocarcinoma

Molecular Oncology

Volumn 9, Issue 1, 2015, Pages 105-114

  Cheng, Jin ^a   Tian, Ling ^a   Ma, Jingjing ^a   Gong, Yanping ^a   Zhang, Zhengxiang ^a   Chen, Zhiwei ^a   Xu, Bing ^a   Xiong, Hui ^b   Li, Chuanyuan ^c   Huang, Qian ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Akt MAPK; Apoptosis; Caspase; Pancreatic cancer; PKC ; Repopulation

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; CASPASE; CASPASE 3; CASPASE 7; LENTIVIRUS VECTOR; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; PROTEIN KINASE C DELTA; ROTTLERIN; STRESS ACTIVATED PROTEIN KINASE 1; CASP3 PROTEIN, HUMAN; CASP7 PROTEIN, HUMAN; PRKCD PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; CANCER RADIOTHERAPY; CELL GROWTH; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; FEEDER CELL; GROWTH STIMULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PANCREAS ADENOCARCINOMA; PROTEIN PHOSPHORYLATION; TUMOR CELL; TUMOR GROWTH; APOPTOSIS; CARCINOMA, PANCREATIC DUCTAL; ENZYME ACTIVATION; ENZYMOLOGY; METABOLISM; PANCREATIC NEOPLASMS; PATHOLOGY; RADIATION RESPONSE; TUMOR CELL LINE;

APOPTOSIS; CARCINOMA, PANCREATIC DUCTAL; CASPASE 3; CASPASE 7; CELL LINE, TUMOR; CELL PROLIFERATION; ENZYME ACTIVATION; HUMANS; NEOPLASM PROTEINS; PANCREATIC NEOPLASMS; PROTEIN KINASE C-DELTA;

EID: 84920414826     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.07.024     Document Type: Article

References (37)

1. Ahn G.O., Brown J.M. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell 2008, 13:193-205.
2. Basu A., Lu D., Sun B., Moor A.N., Akkaraju G.R., Huang J. Proteolytic activation of protein kinase C-epsilon by caspase-mediated processing and transduction of antiapoptotic signals. J.Biol. Chem. 2002, 277:41850-41856.
3. Bluwstein A., Kumar N., Leger K., Traenkle J., Oostrum J., Rehrauer H., Baudis M., Hottiger M.O. PKC signaling prevents irradiation-induced apoptosis of primary human fibroblasts. Cell Death Dis. 2013, 4:e498.
4. Brodie C., Blumberg P.M. Regulation of cell apoptosis by protein kinase c delta. Apoptosis 2003, 8:19-27.
5. Cataldi A., Di Giacomo V., Rapino M., Zara S., Rana R.A. Ionizing radiation induces apoptotic signal through protein kinase Cdelta (delta) and survival signal through Akt and cyclic-nucleotide response element-binding protein (CREB) in Jurkat T cells. Biol. Bull. 2009, 217:202-212.
6. Datta R., Kojima H., Yoshida K., Kufe D. Caspase-3-mediated cleavage of protein kinase C theta in induction of apoptosis. J.Biol. Chem. 1997, 272:20317-20320.
7. D'Costa A.M., Denning M.F. A caspase-resistant mutant of PKC-delta protects keratinocytes from UV-induced apoptosis. Cell Death Differ. 2005, 12:224-232.
8. Dugourd C., Gervais M., Corvol P., Monnot C. Akt is a major downstream target of PI3-kinase involved in angiotensin II-induced proliferation. Hypertension 2003, 41:882-890.
9. Emoto Y., Manome Y., Meinhardt G., Kisaki H., Kharbanda S., Robertson M., Ghayur T., Wong W.W., Kamen R., Weichselbaum R., et al. Proteolytic activation of protein kinase C delta by an ICE-like protease in apoptotic cells. EMBO J. 1995, 14:6148-6156.
10. Galluzzi L., Kepp O., Kroemer G. Caspase-3 and prostaglandins signal for tumor regrowth in cancer therapy. Oncogene 2012, 31:2805-2808.
11. Gliki G., Wheeler-Jones C., Zachary I. Vascular endothelial growth factor induces protein kinase C (PKC)-dependent Akt/PKB activation and phosphatidylinositol 3'-kinase-mediates PKC delta phosphorylation: role of PKC in angiogenesis. Cell Biol. Int. 2002, 26:751-759.
12. Hallahan D.E., Virudachalam S., Schwartz J.L., Panje N., Mustafi R., Weichselbaum R.R. Inhibition of protein kinases sensitizes human tumor cells to ionizing radiation. Radiat. Res. 1992, 129:345-350.
13. Hallahan D.E., Virudachalam S., Sherman M.L., Huberman E., Kufe D.W., Weichselbaum R.R. Tumor necrosis factor gene expression is mediated by protein kinase C following activation by ionizing radiation. Cancer Res. 1991, 51:4565-4569.
14. Hermens A.F., Barendsen G.W. Changes of cell proliferation characteristics in a rat rhabdomyosarcoma before and after x-irradiation. Eur. J. Cancer 1969, 5:173-189.
15. Huang Q., Li F., Liu X., Li W., Shi W., Liu F.F., O'Sullivan B., He Z., Peng Y., Tan A.C., Zhou L., Shen J., Han G., Wang X.J., Thorburn J., Thorburn A., Jimeno A., Raben D., Bedford J.S., Li C.Y. Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nat. Med. 2011, 17:860-866.
16. Kim M.J., Kim R.K., Yoon C.H., An S., Hwang S.G., Suh Y., Park M.J., Chung H.Y., Kim I.G., Lee S.J. Importance of PKCdelta signaling in fractionated-radiation-induced expansion of glioma-initiating cells and resistance to cancer treatment. J.Cell Sci. 2011, 124:3084-3094.
17. Koriyama H., Kouchi Z., Umeda T., Saido T.C., Momoi T., Ishiura S., Suzuki K. Proteolytic activation of protein kinase C delta and epsilon by caspase-3 in U937 cells during chemotherapeutic agent-induced apoptosis. Cell Signal 1999, 11:831-838.
18. Kurokawa M., Kornbluth S. Caspases and kinases in a death grip. Cell 2009, 138:838-854.
19. Li F., Huang Q., Chen J., Peng Y., Roop D.R., Bedford J.S., Li C.Y. Apoptotic cells activate the "phoenix rising" pathway to promote wound healing and tissue regeneration. Sci. Signal 2010, 3:ra13.
20. Li F., Sonveaux P., Rabbani Z.N., Liu S., Yan B., Huang Q., Vujaskovic Z., Dewhirst M.W., Li C.Y. Regulation of HIF-1alpha stability through S-nitrosylation. Mol. Cell 2007, 26:63-74.
21. Lieber M., Mazzetta J., Nelson-Rees W., Kaplan M., Todaro G. Establishment of a continuous tumor-cell line (panc-1) from a human carcinoma of the exocrine pancreas. Int. J. Cancer 1975, 15:741-747.
22. Ma J., Tian L., Cheng J., Chen Z., Xu B., Wang L., Li C., Huang Q. Sonic hedgehog signaling pathway supports cancer cell growth during cancer radiotherapy. PLoS One 2013, 8:e65032.
23. Moeller B.J., Cao Y., Li C.Y., Dewhirst M.W. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 2004, 5:429-441.
24. Munshi A., Hobbs M., Meyn R.E. Clonogenic cell survival assay. Methods Mol. Med. 2005, 110:21-28.
25. Nakajima T. Signaling cascades in radiation-induced apoptosis: roles of protein kinase C in the apoptosis regulation. Med. Sci. Monit. 2006, 12:RA220-224.
26. Nakajima T. Positive and negative regulation of radiation-induced apoptosis by protein kinase C. J.Rad. Res. 2008, 49:1-8.
27. Park J.S., Qiao L., Su Z.Z., Hinman D., Willoughby K., McKinstry R., Yacoub A., Duigou G.J., Young C.S., Grant S., Hagan M.P., Ellis E., Fisher P.B., Dent P. Ionizing radiation modulates vascular endothelial growth factor (VEGF) expression through multiple mitogen activated protein kinase dependent pathways. Oncogene 2001, 20:3266-3280.
28. Ravi D., Muniyappa H., Das K.C. Caffeine inhibits UV-mediated NF-kappaB activation in A2058 melanoma cells: an ATM-PKCdelta-p38 MAPK-dependent mechanism. Mol. Cell Biochem 2008, 308:193-200.
29. Reyland M.E. Protein kinase C isoforms: multi-functional regulators of cell life and death. Front. Biosc. 2009, 14:2386-2399.
30. Rodriguez-Wallberg K.A. Principles of cancer treatment: impact on reproduction. Adv. Exp. Med. Biol. 2012, 732:1-8.
31. Schmidt-Ullrich R.K., Mikkelsen R.B., Dent P., Todd D.G., Valerie K., Kavanagh B.D., Contessa J.N., Rorrer W.K., Chen P.B. Radiation-induced proliferation of the human A431 squamous carcinoma cells is dependent on EGFR tyrosine phosphorylation. Oncogene 1997, 15:1191-1197.
32. Schuurbiers O.C., Kaanders J.H., van der Heijden H.F., Dekhuijzen R.P., Oyen W.J., Bussink J. The PI3-K/AKT-pathway and radiation resistance mechanisms in non-small cell lung cancer. J.Thorac. Oncol. 2009, 4:761-767.
33. Stabile E., Zhou Y.F., Saji M., Castagna M., Shou M., Kinnaird T.D., Baffour R., Ringel M.D., Epstein S.E., Fuchs S. Akt controls vascular smooth muscle cell proliferation invitro and invivo by delaying G1/S exit. Circ. Res. 2003, 93:1059-1065.
34. Stephens T.C., Currie G.A., Peacock J.H. Repopulation of gamma-irradiated Lewis lung carcinoma by malignant cells and host macrophage progenitors. Br. J. Cancer 1978, 38:573-582.
35. Vassileva V., Allen C.J., Piquette-Miller M. Effects of sustained and intermittent paclitaxel therapy on tumor repopulation in ovarian cancer. Mol. Cancer Ther. 2008, 7:630-637.
36. Xia S., Chen Z., Forman L.W., Faller D.V. PKCdelta survival signaling in cells containing an activated p21Ras protein requires PDK1. Cell Signal 2009, 21:502-508.
37. Zhang W., Liu H.T. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 2002, 12:9-18.