Lenalidomide targets clonogenic side population in multiple myeloma: Pathophysiologic and clinical implications

Blood

Volumn 117, Issue 17, 2011, Pages 4409-4419

  Jakubikova, Jana ^a,b   Adamia, Sophia ^a,c   Kost Alimova, Maria ^d   Klippel, Steffen ^a   Cervi, David ^a   Daley, John F ^a,c   Cholujova, Dana ^b   Kong, Sun Young ^a   Leiba, Merav ^a   Blotta, Simona ^a   Ooi, Melissa ^a   Delmore, Jake ^a   Laubach, Jacob ^a   Richardson, Paul G ^a   Sedlak, Jan ^b   Anderson, Kenneth C ^a   Mitsiades, Constantine S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CANCER RESEARCH INSTITUTE   (Slovakia)

^c Department of Medical Oncology ^*  (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; LENALIDOMIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PROTEIN C JUN; PROTEIN KINASE B; PROTEIN P53; SYNDECAN 1;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CARCINOGENICITY; CELL PROLIFERATION; CELL VIABILITY; CLONOGENESIS; CONTROLLED STUDY; DRUG TARGETING; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MULTIPLE MYELOMA; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECURRENT DISEASE; SIDE POPULATION CELL;

EID: 79955974540     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-02-267344     Document Type: Article

References (50)

1. Greipp PR, San MJ, Durie BG, et al. International staging system for multiple myeloma. J Clin Oncol. 2005;23(15):3412-3420.
2. Mitsiades CS, Mitsiades NS, Richardson PG, Munshi NC, Anderson KC. Multiple myeloma: a prototypic disease model for the characterization and therapeutic targeting of interactions between tumor cells and their local microenvironment. J Cell Biochem. 2007;101(4):950-968. (Pubitemid 47040875)
3. Donnenberg VS, Donnenberg AD. Multiple drug resistance in cancer revisited: the cancer stem cell hypothesis. J Clin Pharmacol. 2005;45(8): 872-877. (Pubitemid 41060226)
4. Ho MM, Ng AV, Lam S, Hung JY. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res. 2007;67(10):4827-4833. (Pubitemid 46910191)
5. Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007; 67(3):1030-1037.
6. Ricci-Vitiani L, Lombardi DG, Pilozzi E, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445(7123): 111-115. (Pubitemid 46067311)
7. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3(7):730-737. (Pubitemid 27298715)
8. Challen GA, Little MH. A side order of stem cells: the SP phenotype. Stem Cells. 2006;24(1):3-12.
9. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 1996;183(4):1797-1806. (Pubitemid 26134320)
10. Wu C, Wei Q, Utomo V, et al. Side population cells isolated from mesenchymal neoplasms have tumor initiating potential. Cancer Res. 2007; 67(17):8216-8222. (Pubitemid 47395158)
11. Singhal S, Mehta J, Desikan R, et al. Antitumor activity of thalidomide in refractory multiple myeloma. N Engl J Med. 1999;341(21):1565-1571.
12. Richardson PG, Blood E, Mitsiades CS, et al. A randomized phase 2 study of lenalidomide therapy for patients with relapsed or relapsed and refractory multiple myeloma. Blood. 2006; 108(10):3458-3464.
13. List A, Kurtin S, Roe DJ, et al. Efficacy of lenalidomide in myelodysplastic syndromes. N Engl J Med. 2005;352(6):549-557. (Pubitemid 40204668)
14. Mitsiades N, Mitsiades CS, Poulaki V, et al. Apoptotic signaling induced by immunomodulatory thalidomide analogs in human multiple myeloma cells: therapeutic implications. Blood. 2002; 99(12):4525-4530. (Pubitemid 34627223)
15. Dredge K, Marriott JB, Macdonald CD, et al. Novel thalidomide analogues display antiangiogenic activity independently of immunomodulatory effects. Br J Cancer. 2002;87(10): 1166-1172. (Pubitemid 35418112)
16. Gupta D, Treon SP, Shima Y, et al. Adherence of multiple myeloma cells to bone marrow stromal cells up-regulates vascular endothelial growth factor secretion: therapeutic applications. Leukemia. 2001;15(12):1950-1961. (Pubitemid 33115003)
17. Chang DH, Liu N, Klimek V, et al. Enhancement of ligand-dependent activation of human natural killer T cells by lenalidomide: therapeutic implications. Blood. 2006;108(2):618-621. (Pubitemid 44061362)
18. Davies FE, Raje N, Hideshima T, et al. Thalidomide and immunomodulatory derivatives augment natural killer cell cytotoxicity in multiple myeloma. Blood. 2001;98(1):210-216.
19. Matsui W, Huff CA, Wang Q, et al. Characterization of clonogenic multiple myeloma cells. Blood. 2004;103(6):2332-2336. (Pubitemid 38326254)
20. Jonker JW, Freeman J, Bolscher E, et al. Contribution of the ABC transporters Bcrp1 and Mdr1a/1b to the side population phenotype in mammary gland and bone marrow of mice. Stem Cells. 2005;23(8):1059-1065. (Pubitemid 41377721)
21. Jordan CT. Cancer stem cells: controversial or just misunderstood? Cell Stem Cell. 2009;4(3): 203-205.
22. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414(6859):105-111. (Pubitemid 33041634)
23. Fukuda K, Saikawa Y, Ohashi M, et al. Tumor initiating potential of side population cells in human gastric cancer. Int J Oncol. 2009;34(5):1201-1207.
24. Huang D, Gao Q, Guo L, et al. Isolation and identification of cancer stem-like cells in esophageal carcinoma cell lines. Stem Cells Dev. 2009;18(3): 465-473.
25. Loebinger MR, Giangreco A, Groot KR, et al. Squamous cell cancers contain a side population of stem-like cells that are made chemosensitive by ABC transporter blockade. Br J Cancer. 2008; 98(2):380-387. (Pubitemid 351161265)
26. Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, et al. Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci U S A. 2006;103(30):11 154-11159.
27. Tavaluc RT, Hart LS, Dicker DT, El-Deiry WS. Effects of low confluency, serum starvation and hypoxia on the side population of cancer cell lines. Cell Cycle. 2007;6(20):2554-2562. (Pubitemid 350058675)
28. Patrawala L, Calhoun T, Schneider-Broussard R, et al. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res. 2005;65(14):6207-6219. (Pubitemid 40994406)
29. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445(7123):106-110. (Pubitemid 46067310)
30. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100(7):3983-3988. (Pubitemid 36418143)
31. Bergsagel PL, Masellis SA, Belch AR, Pilarski LM. The blood B-cells and bone marrow plasma cells in patients with multiple myeloma share identical IgH rearrangements. Curr Top Microbiol Immunol. 1995;194:17-24. (Pubitemid 24369437)
32. Pilarski LM, Masellis-Smith A, Szczepek A, Mant MJ, Belch AR. Circulating clonotypic B cells in the biology of multiple myeloma: speculations on the origin of myeloma. Leuk Lymphoma. 1996;22 (5-6):375-383. (Pubitemid 26341003)
33. Matsui W, Wang Q, Barber JP, et al. Clonogenic multiple myeloma progenitors, stem cell properties, and drug resistance. Cancer Res. 2008; 68(1):190-197. (Pubitemid 351380120)
34. Peacock CD, Wang Q, Gesell GS, et al. Hedgehog signaling maintains a tumor stem cell compartment in multiple myeloma. Proc Natl Acad Sci U S A. 2007;104(10):4048-4053. (Pubitemid 47181576)
35. Yaccoby S, Epstein J. The proliferative potential of myeloma plasma cells manifest in the SCIDhu host. Blood. 1999;94(10):3576-3582. (Pubitemid 29536154)
36. Burkert J, Otto WR, Wright NA. Side populations of gastrointestinal cancers are not enriched in stem cells. J Pathol. 2008;214(5):564-573. (Pubitemid 351482271)
37. Loh YS, Mo S, Brown RD, et al. Presence of Hoechst low side populations in multiple myeloma. Leuk Lymphoma. 2008;49(9):1813-1816.
38. Khotskaya YB, Dai Y, Ritchie JP, et al. Syndecan-1 is required for robust growth, vascularization, and metastasis of myeloma tumors in vivo. J Biol Chem. 2009;284(38):26085-26095.
39. Hadnagy A, Gaboury L, Beaulieu R, Balicki D. SP analysis may be used to identify cancer stem cell populations. Exp Cell Res. 2006;312(19):3701-3710. (Pubitemid 44633895)
40. Moserle L, Indraccolo S, Ghisi M, et al. The side population of ovarian cancer cells is a primary target of IFN-alpha antitumor effects. Cancer Res. 2008;68(14):5658-5668.
41. Zhou J, Wulfkuhle J, Zhang H, et al. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc Natl Acad Sci U S A. 2007; 104(41):16158-16163. (Pubitemid 350099378)
42. Zhou S, Schuetz JD, Bunting KD, et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med. 2001;7(9):1028-1034. (Pubitemid 32937383)
43. Chiba T, Kita K, Zheng YW, et al. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology. 2006;44(1):240-251. (Pubitemid 44049156)
44. Haraguchi N, Utsunomiya T, Inoue H, et al. Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells. 2006;24(3):506-513. (Pubitemid 44464754)
45. Hideshima T, Chauhan D, Shima Y, et al. Thalidomide and its analogs overcome drug resistance of human multiple myeloma cells to conventional therapy. Blood. 2000;96(9):2943-2950.
46. Hu C, Li H, Li J, et al. Analysis of ABCG2 expression and side population identifies intrinsic drug efflux in the HCC cell line MHCC-97L and its modulation by Akt signaling. Carcinogenesis. 2008;29(12):2289-2297.
47. Mogi M, Yang J, Lambert JF, et al. Akt signaling regulates side population cell phenotype via Bcrp1 translocation. J Biol Chem. 2003;278(40): 39068-39075. (Pubitemid 37221810)
48. Bleau AM, Hambardzumyan D, Ozawa T, et al. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell. 2009;4(3): 226-235.
49. Trussardi-Regnier A, Lavenus S, Gorisse MC, Dufer J. Thalidomide alters nuclear architecture without ABCB1 gene modulation in drug-resistant myeloma cells. Int J Oncol. 2009;35(3):641-647.
50. Chepko G, Dickson RB. Ultrastructure of the putative stem cell niche in rat mammary epithelium. Tissue Cell. 2003;35(2):83-93. (Pubitemid 36625938)