All trans retinoic acid nanodisks enhance retinoic acid receptor mediated apoptosis and cell cycle arrest in mantle cell lymphoma

British Journal of Haematology

Volumn 150, Issue 2, 2010, Pages 158-169

  Singh, Amareshwar T K ^a   Evens, Andrew M ^a   Anderson, Reilly J ^a   Beckstead, Jennifer A ^b   Sankar, Natesan ^a   Sassano, Antonella ^a   Bhalla, Savita ^a   Yang, Shuo ^a   Platanias, Leonidas C ^a   Forte, Trudy M ^b   Ryan, Robert O ^b   Gordon, Leo I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

all trans retinoic acid (ATRA); apoptosis; mantle cell lymphoma; nanodisks; reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; ANTINEOPLASTIC AGENT; CYCLIN D1; DIMETHYL SULFOXIDE; PROTEIN P21; PROTEIN P27; REACTIVE OXYGEN METABOLITE; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOIC ACID RECEPTOR ALPHA; RETINOID X RECEPTOR GAMMA; RO 41 5253; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BIOLOGICAL ACTIVITY; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL DEATH; CELL GROWTH; CELL KILLING; CONTROLLED STUDY; DOWN REGULATION; DRUG INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MANTLE CELL LYMPHOMA; NANOANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZOATES; CELL CYCLE; CELL CYCLE PROTEINS; CHROMANS; DRUG DELIVERY SYSTEMS; DRUG EVALUATION, PRECLINICAL; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; LYMPHOMA, MANTLE-CELL; NANOPARTICLES; NEOPLASM PROTEINS; NUCLEAR PROTEINS; REACTIVE OXYGEN SPECIES; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; TRANSCRIPTION, GENETIC; TRETINOIN; TUMOR CELLS, CULTURED;

EID: 77954347482     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2010.08209.x     Document Type: Article

References (46)

1. Adamson, P.C. (1996) All trans retinoic acid pharmacology and its impact on the treatment of acute promyelocytic leukemia. Oncologist, 1, 305 314.
2. Alkan, S., Schnitzer, B., Thompson, J.L., Moscinski, L.C. Ross, C.W. (1995) Cyclin D1 protein expression in mantle cell lymphoma. Annals of Oncology, 6, 567 570.
3. Altucci, L. Gronemeyer, H. (2001) The promise of retinoids to fight against cancer. Nature Reviews Cancer, 1, 181 193.
4. Altucci, L., Leibovitz, M.D., Ogilvie, K.M., de Lera, A.R. Gronemeyer, H. (2007) RAR and RXR modulation in cancer and metabolic disease. Nature Reviews, 6, 793 810.
5. Amin, H.M., McDonnell, T.J., Medeiros, J., Rassidakis, G.Z., Leventaki, V., O'Connor, S.L., Keating, M.J. Lai, R. (2003) Characterization of 4 mantle cell lymphoma cell lines. Archives of Pathology and Laboratory Medicine, 127, 424 431.
6. Baldassarre, G., Boccia, A., Bruni, P., Sandomenico, C., Barone, M.V., Pepe, S., Angrisano, T., Belletti, B., Motti, M.L., Fusco, A. Viglietto, G. (2000) Retinoic acid induces neuronal differentiation of embryonal carcinoma cells by reducing proteasome-dependent proteolysis of the cyclin-dependent inhibitor p27. Cell Growth & Differentiation, 11, 517 526.
7. Bao-Lei, T., Zhu-Zhong, M., Yi, S., Jun-Jie, Q., Yan, D., Hua, L., Bin, L., Guo-Wei, Z. Zhi-Xian, S. (2006) Knocking down PML impairs p53 signaling transduction pathway and suppresses irradiation induced apoptosis in breast carcinoma cell MCF-7. Journal of Cellular Biochemistry, 97, 561 571.
8. Bertoni, F. Ponzoni, M. (2007) The cellular origin of mantle cell lymphoma. International Journal of Biochemistry and Cell Biology, 39, 1747 1753.
9. Bogner, C., Peschel, C. Decker, T. (2006) Targeting the proteasome in mantle cell lymphoma: a promising therapeutic approach. Leukemia and Lymphoma, 47, 195 205.
10. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248 254.
11. Cariati, R., Zancai, P., Quaia, M., Cutrona, G., Giannini, F., Rizzo, S., Boiocchi, M. Dolcetti, R. (2000) Retinoic acid induces persistent, RARα-mediated anti-proliferative responses in Epstein Barr virus immortalized B lymphoblasts carrying an activated c-myc oncogene but not in Burkitt's lymphoma cell lines. International Journal of Cancer, 86, 375 384.
12. Chiarle, R., Budel, L.M., Skolnik, J., Frizzera, G., Chilosi, M., Corato, A., Pizzolo, G., Magidson, J., Montagnoli, A., Pagano, M., Maes, B., De Wolf-Peeters, C. Inghirami, G. (2000) Increased proteasome degradation of cyclin-dependent kinase inhibitor p27 is associated with a decreased overall survival in mantle cell lymphoma. Blood, 95, 619 626.
13. Chiarle, R., Pagano, M. Inghirami, G. (2001) The cyclin dependent kinase inhibitor p27 and its prognostic role in breast cancer. Breast Cancer Research, 3, 91 94.
14. Clarke, P.R. Allan, L.A. (2009) Cell-cycle control in the face of damage-a matter of life or death. Trends in Cell Biology, 19, 89 98.
15. Delia, D., Aiello, A., Meroni, L., Nicolini, M., Reed, J.C. Pierotti, M.A. (1997) Role of antioxidants and intracellular free radicals in retinamide induced cell death. Carcinogenesis, 18, 943 948.
16. Dierov, J., Sawaya, B.E., Prosniak, M. Gartenhaus, R.B. (1999) Retinoic acid modulates a bimodal effect on cell cycle progression in human adult T-cell leukemia cells. Clinical Cancer Research, 5, 2540 2547.
17. Evens, A.M., Lecane, P., Magda, D., Prachand, S., Singhal, S., Nelson, J., Miller, R.A., Gartenhaus, R.B. Gordon, L.I. (2005) Motexafin gadolinium generates reactive oxygen species and induces apoptosis in sensitive and highly resistant multiple myeloma cells. Blood, 105, 1265 1273.
18. Faderl, S., Lotan, R., Kantarjian, H.M., Harris, D., Van, Q. Estrov, Z. (2003) N-(4-Hydroxylphenyl)retinamide (fenretinide, 4-HPR), a retinoid compound with antileukemic and proapoptotic activity in acute lymphoblastic leukemia (ALL). Leukemia Research, 27, 259 266.
19. Fu, K., Weisenburger, D.D., Greiner, T.C., Dave, S., Wright, G., Rosenwald, A., Chiorazzi, M., Iqbal, J., Gesk, S., Siebert, R., De Jong, D., Jaffe, E.S., Wilson, W.H., Delabie, J., Ott, G., Dave, B.J., Sanger, W.G., Smith, L.M., Rimsza, L., Braziel, R.M., Müller-Hermelink, H.K., Campo, E., Gascoyne, R.D., Staudt, L.M. Chan, W.C. (2005) Cyclin D1-negative mantle cell lymphoma: A clinicopathologic study based on gene expression profiling. Blood, 106, 4315 4321.
20. Green, D.R. Reed, J.C. (1998) Mitochondria and apoptosis. Science, 281, 1309 1312.
21. Guidoboni, M., Zancai, P., Cariati, R., Rizzo, S., Dal Col, J., Pavan, A., Gloghini, A., Spina, M., Cuneo, A., Pomponi, F., Bononi, A., Doglioni, C., Maestro, R., Carbone, A., Boiocchi, M. Dolcetti, R. (2005) Retinoic acid inhibits the proliferative response induced by CD40 activation and interleukin-4 in mantle cell lymphoma. Cancer Research, 65, 587 595.
22. Iovannisci, D.M., Beckstead, J.A. Ryan, R.O. (2009) Targeting nanodisks via an apolipoprotein - single chain variable antibody chimera. Biochemical and Biophysical Research Communications, 379, 466 469.
23. Izban, K.F., Alkan, S., Singleton, T.P. His, E.D. (2000) Multiparameter immunohistochemical analysis of the cell cycle proteins cyclin D1, Ki-67, p21, p27, and p53 in mantle cell lymphoma. Archives of Pathology and Laboratory Medicine, 124, 1457 1462.
24. Jimenez-Lara, A.M., Clarke, N., Altucci, L. Gronemeyer, H. (2004) Retinoic acid induced apoptosis in leukemic cells. Trends in Molecular Medicine, 10, 508 515.
25. Jingo, Y., Wang, I., Xia, I., Chen, G.Q., Chen, Z., Miller, W.H. Waxman, S. (2001) Combined effect of all trans retinoic acid and arsenic trioxide in acute promyelocytic leukemia cells in vitro and in vivo. Blood, 97, 264 269.
26. Kambhampati, S., Li, Y., Verma, A., Sassano, A., Majchrzak, B., Deb, D.K., Parmar, S., Giafis, N., Kalvakolanu, D.V., Rahman, A., Uddin, S., Minucci, S., Tallman, M.S., Fish, E.N. Platanias, L.C. (2003) Activation of protein kinase C delta by all trans retinoic acid. Journal of Biological Chemistry, 278, 32544 32551.
27. Kitareewan, S., Blumen, S., Sekula, D., Bissonnette, R.P., Lamph, W.W., Cui, Q., Gallagher, R. Dmitrovsky, E. (2008) G0S2 is an all-trans retinoic acid target gene. International Journal of Oncology, 33, 397 404.
28. Klier, M., Anastasov, N., Hermann, A., Meindl, T., Angermeier, D., Raffeld, M., Fend, F. Quintanilla-Martinez, L. (2008) Specific lentiviral shRNA-mediated knockdown of cyclin D1 in mantle cell lymphoma has minimal effects on cell survival and reveals a regulatory circuit with cyclin D2. Leukemia, 22, 2097 2105.
29. van der Leede, B.M., van den Brink, C.E., Pijnappel, W.W., Sonneveld, E., van der Saag, P.T. van der Burg, B. (1997) Autoinduction of retinoic acid metabolism to polar derivatives with decreased biological activity in retinoic acid sensitive, but not in retinoic acid resistant human breast cancer cells. Journal of Biological Chemistry, 272, 17921 17928.
30. Lehmann, J.M., Jong, L., Fanjul, A., Cameron, J.F., Lu, X.P., Haefner, P., Dawson, M.I. Pfahl, M. (1992) Retinoids selective for retinoid X receptor response pathways. Science, 258, 1944 1946.
31. Lehmann, S., Paul, C. Torma, H. (2001) Retinoid receptor expression and its correlation to retinoid sensitivity in non-M3 acute myeloid leukemia blast cells. Clinical Cancer Research, 7, 367 373.
32. Minnucci, S., Zand, D.J., Dey, A., Marks, M.S., Nagata, T., Grippo, J.F. Ozato, K. (1994) Dominant negative retinoid X receptor beta inhibits retinoic acid-responsive gene regulation in embryonal carcinoma cells. Molecular and Cellular Biology, 14, 360 372.
33. Mozos, A., Royo, C., Hartmann, E., De Jong, D., Baró, C., Valera, A., Fu, K., Weisenburger, D.D., Delabie, J., Chuang, S.S., Jaffe, E.S., Ruiz-Marcellan, C., Dave, S., Rimsza, L., Braziel, R., Gascoyne, R.D., Solé, F., López-Guillermo, A., Colomer, D., Staudt, L.M., Rosenwald, A., Ott, G., Jares, P. Campo, E. (2009) SOX11 expression is highly specific for mantle cell lymphoma and identifies the cyclin D1-negative subtype. Haematologica, 94, 1555 1562.
34. Oridate, N., Suzuki, S., Higuchi, M., Mitchell, M.F., Hong, W.K. Lotan, R. (1997) Involvement of reactive oxygen species in N-(4-hydroxyphenyl) retinamide induced apoptosis in cervical carcinoma cells. Journal of the National Cancer Institute, 89, 1191 1198.
35. Orlandi, M., Mantovani, B., Ammar, K., Avitabile, E., Dal Monte, P. Bartolini, G. (2003) Retinoids and cancer: antitumoral effects of ATRA, 9-cis RA and the new retinoid IIF on the HL-60 leukemic cell line. Medical Principles and Practice, 12, 164 169.
36. Ott, M.M., Helbing, A., Ott, G., Bartek, J., Fischer, L., Dürr, A., Kreipe, H. Müller-Hermelink, H.K. (1996) Bcl-1 rearrangement and cyclin D1 protein expression in mantle cell lymphoma. Journal of Pathology, 179, 238 242.
37. Redmond, K.A., Nguyen, T.-S. Ryan, R.O. (2007) All-trans-retinoic acid nanodisks. International Journal of Pharmaceutics, 339, 246 250.
38. Ryan, R.O. (2008) Nanodisks: hydrophobic drug delivery vehicles. Expert Opinion on Drug Delivery, 5, 343 351.
39. Ryan, R.O., Forte, T.M. Oda, M.N. (2003) Optimized bacterial expression of human apolipoprotein A-I. Protein Expression and Purification, 27, 98 103.
40. Soprano, D.R., Qin, P. Soprano, K.J. (2004) Retinoic acid receptors and cancers. Annual Review of Nutrition, 24, 201 221.
41. Spinella, M.J., Freemantle, S.J., Sekula, D., Chang, J.H., Christie, A.J. Dmitrovsky, E. (1999) Retinoic acid promotes ubiquitination and proteolysis of cyclin D1 during induced tumor cell differentiation. Journal of Biological Chemistry, 31, 22013 22018.
42. Sundaresan, A., Claypool, K., Mehta, K., Lopez-Berestein, G., Cabanillas, F. Ford, Jr., R.J. (1997) Retinoid mediated inhibition of cell growth with stimulation of apoptosis in aggressive B-cell lymphomas. Cell Growth and Differentiation, 8, 1071 1082.
43. Szabova, L., Macejova, D., Dvorcakova, M., Mostbock, S., Blazickova, S., Zorad, S., Walrand, S., Cardinault, N., Vasson, M.P., Rock, E. Brtko, J. (2003) Expression of nuclear retinoic acid receptor in peripheral blood mononuclear cells (PBMC) of healthy subjects. Life Sciences, 72, 831 836.
44. Tanaka, T., Suh, K.S., lo, A.M. De Luca, L.M. (2007) p21 is a common transcriptional target of retinoid receptors. Journal of Biological Chemistry, 282, 29987 29997.
45. Wang, Z.Y. Chen, Z. (2000) Differentiation and apoptosis induction therapy in acute promyelocytic leukemia. Lancet Oncology, 1, 101 106.
46. Yu, Z., Li, W., Lu, Q., Wang, L., Zhang, X., Han, P., Chen, P. Pei, Y. (2008) p21 is required for ATRA-mediated growth inhibition of MEPM cells, which involves RAR. Journal of Cellular Biochemistry, 104, 2185 2192.