Inhibition of type i insulin-like growth factor receptor tyrosine kinase by picropodophyllin induces apoptosis and cell cycle arrest in T lymphoblastic leukemia/lymphoma

Leukemia and Lymphoma

Volumn 55, Issue 8, 2014, Pages 1876-1883

  Huang, Zhiwei ^a   Fang, Zhijia ^a   Zhen, Hong ^b   Zhou, Li ^b   Amin, Hesham M ^c   Shi, Ping ^b  

^a DONGHUA UNIVERSITY   (China)

^b EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

IGF IR; Jurkat cells; Molt 3 cells; Picropodophyllin; Proteomics; T lymphoblastic leukemia lymphoma

Indexed keywords

ANTILEUKEMIC AGENT; PICROPODOPHYLLIN; PROTEIN TYROSINE KINASE INHIBITOR; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; PODOPHYLLOTOXIN; PROTEIN TYROSINE KINASE;

AMINO ACID SEQUENCE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL METABOLISM; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; JURKAT CELL LINE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEOMICS; SIGNAL TRANSDUCTION; T CELL LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; CELL CYCLE CHECKPOINT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; JURKAT CELLS; PHOSPHORYLATION; PODOPHYLLOTOXIN; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN-TYROSINE KINASES; PROTEOMICS; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION;

EID: 84904890812     PISSN: 10428194     EISSN: 10292403     Source Type: Journal    
DOI: 10.3109/10428194.2013.862241     Document Type: Article

References (53)

1. Ullrich A, Gray A, Tam AW, et al. Insulin-like growth factor I receptor primary structure:comparison with insulin receptor suggests structural determinants that define functional specificity. EMBO J 1986; 5: 2503-2512.
2. De Meyts P, Whittaker J. Structural biology of insulin and IGF1 receptors: implications for drug design. Nat Rev Drug Discov 2002; 1: 769-783.
3. Lopez T, Hanahan D. Elevated levels of the IGF-I receptor convey invasion and metastatic capability in a mouse model of pancreatic islet tumourigenesis. Cancer Cell 2002; 1: 339-353.
4. Mauro L, Bartucci M, Morelli C, et al. IGF-I receptor-induced cellcell adhesion of MCF-7 breast cancer cells requires the expression of junction protein ZO-1. J Biol Chem 2001; 276: 39892-39897.
5. Van Golen CM, Schwab TS, Kim B, et al. Insulin-like growth factor-I receptor expression regulates neuroblastoma metastasis to bone. Cancer Res 2006; 66: 6570-6578.
6. Adachi Y, Lee CT, Coffee K, et al. Effects of genetic blockade of the insulin-like growth factor receptor in human colon cancer cell lines. Gastroenterology 2002; 123: 1191-1204.
7. Burfeind P, Chernicky CL, Rininsland F, et al. Antisense RNA to the type I insulin-like growth factor receptor suppresses tumor growth and prevents invasion by rat prostate cancer cells in vivo. Proc Natl Acad Sci USA 1996; 93: 7263-7268.
8. Dunn S E, Ehrlich M, Sharp N J, et al. A dominant negative mutant of the insulin-like growth factor-I receptor inhibits the adhesion, invasion, and metastasis of breast cancer. Cancer Res 1998; 58: 3353-3361.
9. Hongo A, Kuramoto H, Nakamura Y, et al. Antitumor effects of a soluble insulin-like growth factor I receptor in human ovarian cancer cells: advantage of recombinant protein administration in vivo. Cancer Res 2003; 63: 7834-7839.
10. Lee CT, Park KH, Adachi Y, et al. Recombinant adenoviruses expressing dominant negative insulin-like growth factor-I receptor demonstrate antitumor effects on lung cancer. Cancer Gene Ther 2003; 10: 57-63.
11. Yin S, Girnita A, Stromberg T, et al. Targeting the insulin-like growth factor-1 receptor by picropodophyllin as a treatment option for glioblastoma. Neuro Oncol 2010; 12: 19-27.
12. Bertrand FE, Steelman LS, Chappell WH, et al. Synergy between an IGF-1R antibody and Raf/MEK/ERK and PI3K/Akt/mTOR pathway inhibitors in suppressing IGF-1R mediated growth in hematopoietic cells. Leukemia 2006; 20: 1254-1260.
13. Strömberg T, Ekman S, Girnita L, et al. IGF-1 receptor tyrosine kinase inhibition by the cyclolignan PPP induces G2/M-phase accumulation and apoptosis in multiple myeloma cells. Blood 2006; 107: 669-678.
14. Menu E, Jernberg-Wiklund H, Strömberg T, et al. Inhibiting the IGF-1 receptor tyrosine kinase with the cyclolignan PPP: an in vitro and in vivo study in the 5T33MM mouse model. Blood 2006; 107: 655-660.
15. Shi P, Lai R, Lin Q, et al. IGF-IR tyrosine kinase interacts with NPMALK oncogene to induce survival of T-cell ALK anaplastic large-cell lymphoma cells. Blood 2009; 114: 360-370.
16. Shi P, Chandra J, Sun X, et al. Inhibition of IGF-IR tyrosine kinase induces apoptosis and cell cycle arrest in imatinib-resistant chronic myeloid leukemia cells. J Cell Mol Med 2010; 14: 1777-1792.
17. Tazzari PL, Tabellini G, Bortul R, et al. The insulin like growth factor-I receptor kinase inhibitor NVP-AEW541 induces apoptosis in acute myeloid leukemia cells exhibiting autocrine insulin-like growth factor-I secretion. Leukemia 2007; 21: 886-896.
18. Wahner Hendrickson A E, Haluska P, Schneider P A, et al. Expression of insulin receptor isoform A and insulin-like growth factor-1 receptor in human acute myelogenous leukemia: effect of the dual-receptor inhibitor BMS-536924 in vitro. Cancer Res 2009; 69: 7635-7643.
19. Vishwamitra D, Shi P, Wilson D, et al. Expression and effects of inhibition of IGF-IR tyrosine kinase in mantle cell lymphoma. Haematologica 2011; 96: 871-880.
20. Shi B, Vishwamitra D, Granda JG, et al. Molecular and functional characterizations of the association and interactions between nucleophosmin-anaplastic lymphoma kinase and type I insulin-like growth factor receptor. Neoplasia 2013; 15: 669-683.
21. Girnita A, Girnita L, Del Prete F, et al. Cyclolignans as inhibitors of the insulin-like growth factor-1 receptor and malignant cell growth. Cancer Res 2004; 64: 236-242.
22. Vasilcanu D, Girnita A, Girnita L, et al. The cyclolignan PPP induces activation loop-specific inhibition of tyrosine phosphorylation of the insulin-like growth factor-1 receptor. Link to phosphatidyl inositol-3 kinase/Akt apoptotic pathway. Oncogene 2004; 23: 7854-7862.
23. Ohshima-Hosoyama S, Hosoyama T, Nelon LD, et al. IGF-1 receptor inhibition by picropodophyllin in medulloblastoma, Biochem Bioph Res Commun 2010; 399: 727-732.
24. Ekman S, Frödin J, Harmenberg J, et al. Clinical phase I study with an insulin-like growth factor-1 receptor inhibitor: experiences in patients with squamous non-small cell lung carcinoma. Acta Oncol 2011; 50: 441-447.
25. Thomas DA, Kantarjian HM. Lymphoblastic lymphoma. Hematol Oncol Clin North Am 2001; 15: 51-95.
26. Borowitz MJ, Chan JKC. T lymphoblastic leukemia/lymphoma. In: Swerdlow SH, Campo E, Harris NL, et al., editors. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon: IARC; 2008. pp 176-178.
27. Lee P D, Rosenfeld R G, Hintz R L, et al. Characterization of insulin, insulin-like growth factors I and II, and growth hormone receptors on human leukemic lymphoblasts. J Clin Endocrinol Metab 1986; 62: 28-35.
28. Baier T G, Ludwig W D, Schönberg D, et al. Characterisation of insulin-like growth factor I receptors of human acute lymphoblastic leukaemia (ALL) cell lines and primary ALL cells. Eur J Cancer 1992; 28A: 1105-1110.
29. Medyouf H, Gusscott S, Wang H, et al. High-level IGF1R expression is required for leukemia-initiating cell activity in T-ALL and is supported by Notch signaling. J Exp Med 2011; 208: 1809-1822.
30. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem 1976; 72: 248-254.
31. Bergman AC, Benjamin T, Alaiya A, et al. Identification of gel separated tumor marker proteins by mass spectrometry. Electrophoresis 2000; 21: 679-686.
32. Nauseef WM, McCormick SJ, Clark RA. Calreticulin functions as a molecular chaperone in the biosynthesis of myeloperoxidase. J Biol Chem 1995; 270: 4741-4747.
33. Holaska JM, Black BE, Love DC, et al. Calreticulin is a receptor for nuclear export. J Cell Biol 2001; 152: 127-140.
34. Tarr J M, Young P J, Morse R, et al. A mechanism of release of calreticulin from cells during apoptosis. J Mol Biol 2010; 401: 799-812.
35. Van Wijk E, Krieger E, Kemperman MH, et al. A mutation in the gamma actin 1 (ACTG1) gene causes autosomal dominant hearing loss (DFNA20/26). J Med Genet 2003; 40: 879-884.
36. Sonnemann KJ, Fitzsimons DP, Patel JR, et al. Cytoplasmic actin is not required for skeletal muscle development but its absence leads to a progressive myopathy. Dev Cell 2006; 11: 387-397.
37. Dammeyer P, Damdimopoulos AE, Nordman T, et al. Induction of cell membrane protrusions by the N-terminal glutaredoxin domain of a rare splice variant of human thioredoxin reductase 1. J Biol Chem 2008; 283: 2814-2821.
38. Bischoff FR, Krebber H, Kempf T, et al. Human RanGTPaseactivating protein RanGAP1 is a homologue of yeast Rna1p involved in mRNA processing and transport. Proc Natl Acad Sci USA 1995; 92: 1749-1753.
39. Kalab P, Pu R T, Dasso M. The ran GTPase regulates mitotic spindle assembly. Curr Biol 1999; 9: 481-484.
40. Nishimoto T. A new role of ran GTPase. Biochem Biophys Res Commun 1999; 262: 571-574.
41. Antonucci F, Chilosi M, Parolini C, et al. Two-dimensional molecular profiling of mantle cell lymphoma. Electrophoresis 2003; 24: 2376-2385.
42. Jeha S, Luo XN, Beran M, et al. Antisense RNA inhibition of phosphoprotein p18 expression abrogates the transformed phenotype of leukemic cells. Cancer Res 1996; 56: 1445-1450.
43. Gez S, Crossett B, Christopherson RI. Diff erentially expressed cytosolic proteins in human leukemia and lymphoma cell lines correlate with lineages and functions. Biochim Biophys Acta 2007; 1774: 1173-1183.
44. Scherle P, Behrens T, Staudt LM. Ly-GDI, a GDP-dissociation inhibitor of the RhoA GTP-binding protein, is expressed preferentially in lymphocytes. Proc Natl Acad Sci USA 1993; 90: 7568-7572.
45. Scheffzek K, Stephan I, Jensen O N, et al. The Rac-RhoGDI complex and the structural basis for the regulation of Rho proteins by RhoGDI. Nat Struct Biol 2000; 7: 122-126.
46. Olofsson B. Rho guanine dissociation inhibitors: pivotal molecules in cellular signaling. Cell Signal 1999; 11: 545-554.
47. Bilodeau D, Lamy S, Desrosiers RR, et al. Regulation of Rho protein binding to membranes by rhoGDI: inhibition of releasing activity by physiological ionic conditions. Biochem Cell Biol 1999; 77: 59-69.
48. Zhang B, Zhang Y, Dagher M C, et al. Rho GDP dissociation inhibitor protects cancer cells against drug-induced apoptosis. Cancer Res 2005; 65: 6054-6062.
49. Kovarova H, Hajduch M, Korinkova G, et al. Proteomics approach in classifying the biochemical basis of the anticancer activity of the new olomoucine-derived synthetic cyclin-dependent kinase inhibitor, bohemine. Electrophoresis 2000; 21: 3757-3764.
50. Wan J, Wang J, Cheng H, et al. Proteomic analysis of apoptosis initiation induced by all-trans retinoic acid in human acute promyelocytic leukemia cells. Electrophoresis 2001; 22: 3026-3037.
51. Wu X, Sooman L, Wickström M, et al. Alternative cytotoxic effects of the postulated IGF-IR inhibitor picropodophyllin in Vitro. Mol Cancer Ther 2013; 12: 1526-1536.
52. DantumAn P, Heinen C, Hoogstraten D. The ubiquitin receptor Rad23: at the crossroads of nucleotide excision repair and proteasomal degradation. DNA Repair (Amst) 2009; 8: 449-460.
53. Libri D, Mouly V, Lemonnier M, et al. A nonmuscle tropomyosin is encoded by the smooth/skeletal beta-tropomyosin gene and its RNA is transcribed from an internal promoter. J Biol Chem 1990; 265: 3471-3473.