Therapeutic effect of neural stem cells expressing TRAIL and bortezomib in mice with glioma xenografts

Cancer Letters

Volumn 310, Issue 2, 2011, Pages 148-159

  Balyasnikova, Irina V ^a   Ferguson, Sherise D ^a   Han, Yu ^a   Liu, Feifei ^a   Lesniak, Maciej S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Bortezomib; Brain cancer; Glioma; Neural stem cells; TRAIL

Indexed keywords

BORTEZOMIB; DEATH RECEPTOR 5; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER SURVIVAL; CELL SURFACE; COCULTURE; CONTROLLED STUDY; DRUG CYTOTOXICITY; GLIOMA; GLIOMA CELL; IN VIVO STUDY; MALE; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ANIMALS; BORONIC ACIDS; BRAIN NEOPLASMS; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; GLIOMA; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; JURKAT CELLS; MALE; MICE; MICE, NUDE; NEURAL STEM CELLS; PROTEASE INHIBITORS; PYRAZINES; STEM CELL TRANSPLANTATION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; XENOGRAFT MODEL ANTITUMOR ASSAYS;

ANIMALIA; MUS;

EID: 80051678161     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.06.029     Document Type: Article

References (50)

1. Stupp R., Mason W.P., van den Bent M.J., Weller M., Fisher B., Taphoorn M.J., Belanger K., Brandes A.A., Marosi C., Bogdahn U., Curschmann J., Janzer R.C., Ludwin S.K., Gorlia T., Allgeier A., Lacombe D., Cairncross J.G., Eisenhauer E., Mirimanoff R.O. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. New Engl. J. Med. 2005, 352:987-996.
2. Surawicz T.S., Davis F., Freels S., Laws E.R., Menck H.R. Brain tumor survival: results from the National Cancer Data Base. J. Neurooncol. 1998, 40:151-160.
3. Legler J.M., Ries L.A., Smith M.A., Warren J.L., Heineman E.F., Kaplan R.S., Linet M.S. Cancer surveillance series [corrected]: brain and other central nervous system cancers: recent trends in incidence and mortality. J. Natl. Cancer Inst. 1999, 91:1382-1390.
4. Aboody K.S., Brown A., Rainov N.G., Bower K.A., Liu S., Yang W., Small J.E., Herrlinger U., Ourednik V., Black P.M., Breakefield X.O., Snyder E.Y. Neural stem cells display extensive tropism for pathology in adult bra. Proc. Natl. Acad. Sci. USA 2000, 97:12846-12851.
5. Nakamizo A., Marini F., Amano T., Khan A., Studeny M., Gumin J., Chen J., Hentschel S., Vecil G., Dembinski J., Andreeff M., Lang F.F. Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res. 2005, 65:3307-3318.
6. Wu X., Hu J., Zhou L., Mao Y., Yang B., Gao L., Xie R., Xu F., Zhang D., Liu J., Zhu J. In vivo tracking of superparamagnetic iron oxide nanoparticle-labeled mesenchymal stem cell tropism to malignant gliomas using magnetic resonance imaging. Laboratory investigation. J. Neurosurg. 2008, 108:320-329.
7. Yong R.L., Shinojima N., Fueyo J., Gumin J., Vecil G.G., Marini F.C., Bogler O., Andreeff M., Lang F.F. Human bone marrow-derived mesenchymal stem cells for intravascular delivery of oncolytic adenovirus Delta24-RGD to human gliomas. Cancer Res. 2009, 69:8932-8940.
8. Benedetti S., Pirola B., Pollo B., Magrassi L., Bruzzone M.G., Rigamonti D., Galli R., Selleri S., Di Meco F., De Fraja C., Vescovi A., Cattaneo E., Finocchiaro G. Gene therapy of experimental brain tumors using neural progenitor cells. Nat. Med. 2000, 6:447-450.
9. Ehtesham M., Kabos P., Kabosova A., Neuman T., Black K.L., Yu J.S. The use of interleukin 12-secreting neural stem cells for the treatment of intracranial glioma. Cancer Res. 2002, 62:5657-5663.
10. Ashkenazi A., Pai R.C., Fong S., Leung S., Lawrence D.A., Marsters S.A., Blackie C., Chang L., McMurtrey A.E., Hebert A., DeForge L., Koumenis I.L., Lewis D., Harris L., Bussiere J., Koeppen H., Shahrokh Z., Schwall R.H. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 1999, 104:155-162.
11. Walczak H., Miller R.E., Ariail K., Gliniak B., Griffith T.S., Kubin M., Chin W., Jones J., Woodward A., Le T., Smith C., Smolak P., Goodwin R.G., Rauch C.T., Schuh J.C., Lynch D.H. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 1999, 5:157-163.
12. Hao C., Beguinot F., Condorelli G., Trencia A., Van Meir E.G., Yong V.W., Parney I.F., Roa W.H., Petruk K.C. Induction and intracellular regulation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) mediated apoptosis in human malignant glioma cells. Cancer Res. 2001, 61:1162-1170.
13. Wang S., El-Deiry W.S. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 2003, 22:8628-8633.
14. Bouralexis S., Findlay D.M., Evdokiou A. Death to the bad guys: targeting cancer via Apo2L/TRAIL. Apoptosis 2005, 10:35-51.
15. Hetschko H., Voss V., Seifert V., Prehn J.H., Kogel D. Upregulation of DR5 by proteasome inhibitors potently sensitizes glioma cells to TRAIL-induced apoptosis. FEBS J. 2008, 275:1925-1936.
16. Muhlenbeck F., Schneider P., Bodmer J.L., Schwenzer R., Hauser A., Schubert G., Scheurich P., Moosmayer D., Tschopp J., Wajant H. The tumor necrosis factor-related apoptosis-inducing ligand receptors TRAIL-R1 and TRAIL-R2 have distinct cross-linking requirements for initiation of apoptosis and are non-redundant in JNK activation. J. Biol. Chem. 2000, 275:32208-32213.
17. Wajant H., Moosmayer D., Wuest T., Bartke T., Gerlach E., Schonherr U., Peters N., Scheurich P., Pfizenmaier K. Differential activation of TRAIL-R1 and -2 by soluble and membrane TRAIL allows selective surface antigen-directed activation of TRAIL-R2 by a soluble TRAIL derivative. Oncogene 2001, 20:4101-4106.
18. Kim K., Fisher M.J., Xu S.Q., el-Deiry W.S. Molecular determinants of response to TRAIL in killing of normal and cancer cells. Clin. Cancer Res. 2000, 6:335-346.
19. Marsters S.A., Sheridan J.P., Pitti R.M., Huang A., Skubatch M., Baldwin D., Yuan J., Gurney A., Goddard A.D., Godowski P., Ashkenazi A. A novel receptor for Apo2L/TRAIL contains a truncated death domain. Curr. Biol. 1997, 7:1003-1006.
20. Pan G., Ni J., Yu G., Wei Y.F., Dixit V.M. TRUNDD, a new member of the TRAIL receptor family that antagonizes TRAIL signalling. FEBS Lett. 1998, 424:41-45.
21. Song J.H., Song D.K., Pyrzynska B., Petruk K.C., Van Meir E.G., Hao C. TRAIL triggers apoptosis in human malignant glioma cells through extrinsic and intrinsic pathways. Brain Pathol. 2003, 13:539-553.
22. Nencioni A., Wille L., Dal Bello G., Boy D., Cirmena G., Wesselborg S., Belka C., Brossart P., Patrone F., Ballestrero A. Cooperative cytotoxicity of proteasome inhibitors and tumor necrosis factor-related apoptosis-inducing ligand in chemoresistant Bcl-2-overexpressing cells. Clin. Cancer Res. 2005, 11:4259-4265.
23. Conticello C., Adamo L., Vicari L., Giuffrida R., Iannolo G., Anastasi G., Caruso L., Moschetti G., Cupri A., Palumbo G.A., Gulisano M., De Maria R., Giustolisi R., Di Raimondo F. Antitumor activity of bortezomib alone and in combination with TRAIL in human acute myeloid leukemia. Acta Haematol. 2008, 120:19-30.
24. Lashinger L.M., Zhu K., Williams S.A., Shrader M., Dinney C.P., McConkey D.J. Bortezomib abolishes tumor necrosis factor-related apoptosis-inducing ligand resistance via a p21-dependent mechanism in human bladder and prostate cancer cells. Cancer Res. 2005, 65:4902-4908.
25. Saulle E., Petronelli A., Pasquini L., Petrucci E., Mariani G., Biffoni M., Ferretti G., Scambia G., Benedetti-Panici P., Cognetti F., Humphreys R., Peschle C., Testa U. Proteasome inhibitors sensitize ovarian cancer cells to TRAIL induced apoptosis. Apoptosis 2007, 12:635-655.
26. Koschny R., Holland H., Sykora J., Haas T.L., Sprick M.R., Ganten T.M., Krupp W., Bauer M., Ahnert P., Meixensberger J., Walczak H. Bortezomib sensitizes primary human astrocytoma cells of WHO grades I to IV for tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis. Clin. Cancer Res. 2007, 13:3403-3412.
27. Voelkel-Johnson C., King D.L., Norris J.S. Resistance of prostate cancer cells to soluble TNF-related apoptosis-inducing ligand (TRAIL/Apo2L) can be overcome by doxorubicin or adenoviral delivery of full-length TRAIL. Cancer Gene Ther. 2002, 9:164-172.
28. Carlo-Stella C., Lavazza C., Di Nicola M., Cleris L., Longoni P., Milanesi M., Magni M., Morelli D., Gloghini A., Carbone A., Gianni A.M. Antitumor activity of human CD34+ cells expressing membrane-bound tumor necrosis factor-related apoptosis-inducing ligand. Hum. Gene Ther. 2006, 17:1225-1240.
29. Ehtesham M., Kabos P., Gutierrez M.A., Chung N.H., Griffith T.S., Black K.L., Yu J.S. Induction of glioblastoma apoptosis using neural stem cell-mediated delivery of tumor necrosis factor-related apoptosis-inducing ligand. Cancer Res. 2002, 62:7170-7174.
30. Lal A., Glazer C.A., Martinson H.M., Friedman H.S., Archer G.E., Sampson J.H., Riggins G.J. Mutant epidermal growth factor receptor up-regulates molecular effectors of tumor invasion. Cancer Res. 2002, 62:3335-3339.
31. Frederick L., Wang X.Y., Eley G., James C.D. Diversity and frequency of epidermal growth factor receptor mutations in human glioblastomas. Cancer Res. 2000, 60:1383-1387.
32. Furnari F.B., Fenton T., Bachoo R.M., Mukasa A., Stommel J.M., Stegh A., Hahn W.C., Ligon K.L., Louis D.N., Brennan C., Chin L., DePinho R.A., Cavenee W.K. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 2007, 27:2683-2710.
33. 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. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995, 3:673-682.
34. Abdollahi T., Robertson N.M., Abdollahi A., Litwack G. Identification of interleukin 8 as an inhibitor of tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in the ovarian carcinoma cell line OVCAR3. Cancer Res. 2003, 63:4521-4526.
35. Balyasnikova I.V., Franco-Gou R., Mathis J.M., Lesniak M.S. Genetic modification of mesenchymal stem cells to express a single-chain antibody against EGFRvIII on the cell surface. J. Tissue Eng. Regen. Med. 2009, 4:247-258.
36. Hetschko H., Voss V., Horn S., Seifert V., Prehn J.H., Kogel D. Pharmacological inhibition of Bcl-2 family members reactivates TRAIL-induced apoptosis in malignant glioma. J. Neurooncol. 2008, 86:265-272.
37. Sasportas L.S., Kasmieh R., Wakimoto H., Hingtgen S., van de Water J.A., Mohapatra G., Figueiredo J.L., Martuza R.L., Weissleder R., Shah K. Assessment of therapeutic efficacy and fate of engineered human mesenchymal stem cells for cancer therapy. Proc. Natl. Acad. Sci. USA 2009, 106:4822-4827.
38. Choi S.A., Hwang S.K., Wang K.C., Cho B.K., Phi J.H., Lee J.Y., Jung H.W., Lee D.H., Kim S.K. Therapeutic efficacy and safety of TRAIL-producing human adipose tissue-derived mesenchymal stem cells against experimental brainstem glioma. Neuro Oncol. 2010, 13:61-69.
39. Yang B., Wu X., Mao Y., Bao W., Gao L., Zhou P., Xie R., Zhou L., Zhu J. Dual-targeted antitumor effects against brainstem glioma by intravenous delivery of tumor necrosis factor-related, apoptosis-inducing, ligand-engineered human mesenchymal stem cells. Neurosurgery 2009, 65:610-624. (discussion 624).
40. Bagci-Onder T., Wakimoto H., Anderegg M., Cameron C., Shah K. A dual PI3K/mTOR inhibitor, PI-103, cooperates with stem cell delivered TRAIL in experimental glioma models. Cancer Res. 2010, 71:154-163.
41. Luetzkendorf J., Mueller L.P., Mueller T., Caysa H., Nerger K., Schmoll H.J. Growth inhibition of colorectal carcinoma by lentiviral TRAIL-transgenic human mesenchymal stem cells requires their substantial intratumoral presence. J. Cell Mol. Med. 2010, 14:2292-2304.
42. Kohlhaas S.L., Craxton A., Sun X.M., Pinkoski M.J., Cohen G.M. Receptor-mediated endocytosis is not required for tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis. J. Biol. Chem. 2007, 282:12831-12841.
43. Kuijlen J.M., Mooij J.J., Platteel I., Hoving E.W., van der Graaf W.T., Span M.M., Hollema H., den Dunnen W.F. TRAIL-receptor expression is an independent prognostic factor for survival in patients with a primary glioblastoma multiforme. J. Neurooncol. 2006, 78:161-171.
44. Joazeiro C.A., Anderson K.C., Hunter T. Proteasome inhibitor drugs on the rise. Cancer Res. 2006, 66:7840-7842.
45. Kubicek G.J., Werner-Wasik M., Machtay M., Mallon G., Myers T., Ramirez M., Andrews D., Curran W.J., Dicker A.P. Phase I trial using proteasome inhibitor bortezomib and concurrent temozolomide and radiotherapy for central nervous system malignancies. Int. J. Radiat. Oncol. Biol. Phys. 2009, 74:433-439.
46. Labussiere M., Pinel S., Delfortrie S., Plenat F., Chastagner P. Proteasome inhibition by bortezomib does not translate into efficacy on two malignant glioma xenografts. Oncol. Rep. 2008, 20:1283-1287.
47. Shanker A., Brooks A.D., Tristan C.A., Wine J.W., Elliott P.J., Yagita H., Takeda K., Smyth M.J., Murphy W.J., Sayers T.J. Treating metastatic solid tumors with bortezomib and a tumor necrosis factor-related apoptosis-inducing ligand receptor agonist antibody. J. Natl. Cancer Inst. 2008, 100:649-662.
48. Olson J.J., Bowers G., Zhang Z. Proteasome inhibitor therapy in a brain tumor model. Cancer Drug Discovery and Development: Proteasome Inhibitors in Cancer Therapy 2004, 161-170. Humana Press Inc., Totowa (NJ). J. Adams (Ed.).
49. Tamm I. AEG-35156, an antisense oligonucleotide against X-linked inhibitor of apoptosis for the potential treatment of cancer. Curr. Opin. Invest. Drugs 2008, 9:638-646.
50. Oltersdorf T., Elmore S.W., Shoemaker A., Armstrong R., Augeri D., Belli B., Bruncko M., Deckwerth T., Dinges J., Hajduk P., Joseph M., Kitada S., Korsmeyer S., Kunzer A., Letai A., Li C., Mitten M., Nettesheim D., Ng S., Nimmer P., O'Connor J., Oleksijew A., Petros A., Reed J., Shen W., Tahir S., Thompson C., Tomaselli K., Wang B., Wendt M., Zhang H., Fesik S., Rosenberg S. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005, 435:677-681.