Small molecule antagonist of the bone morphogenetic protein type I receptors suppresses growth and expression of Id1 and Id3 in lung cancer cells expressing Oct4 or nestin

Molecular Cancer

Volumn 12, Issue 1, 2013, Pages

  Langenfeld, Elaine ^a   Deen, Malik ^a   Zachariah, Emmanuel ^b   Langenfeld, John ^a,b  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

Author keywords

Antagonist; BMP; Cell death; Cell growth; Id1; Id3; Nestin; NueN; Oct4

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 1; GREEN FLUORESCENT PROTEIN; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 3; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL DEATH; CELL GROWTH; CELL ISOLATION; CELL POPULATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE SILENCING; GROWTH INHIBITION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG CANCER; LUNG NON SMALL CELL CANCER; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ANTIGENS, NUCLEAR; ANTINEOPLASTIC AGENTS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INHIBITOR OF DIFFERENTIATION PROTEINS; LUNG NEOPLASMS; MICE; MICE, NUDE; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; NERVE TISSUE PROTEINS; NESTIN; OCTAMER TRANSCRIPTION FACTOR-3; SIGNAL TRANSDUCTION; TRANSCRIPTOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84886150771     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-12-129     Document Type: Article

References (64)

1. Wang D, Zhu H, Zhu Y, Liu Y, Shen H, Yin R, Zhang Z, Su Z. CD133(+)/CD44(+)/Oct4(+)/Nestin(+) stem-like cells isolated from Panc-1 cell line may contribute to multi-resistance and metastasis of pancreatic cancer. Acta Histochem 2013, 115:349-356. 310.1016/j.acthis.2012.1009.1007. Epub 2012 Oct 1011, 10.1016/j.acthis.2012.09.007, 23036582.
2. Wen K, Fu Z, Wu X, Feng J, Chen W, Qian J. Oct-4 is required for an antiapoptotic behavior of chemoresistant colorectal cancer cells enriched for cancer stem cells: effects associated with STAT3/Survivin. Cancer Lett 2013, 333:56-65. 10.1016/j.canlet.2013.1001.1009. Epub 2013 Jan 1020, 10.1016/j.canlet.2013.01.009, 23340171.
3. Bourguignon LY, Wong G, Earle C, Chen L. Hyaluronan-CD44v3 interaction with Oct4-Sox2-Nanog promotes miR-302 expression leading to self-renewal, clonal formation, and cisplatin resistance in cancer stem cells from head and neck squamous cell carcinoma. J Biol Chem 2012, 287:32800-32824. Epub 32012 Jul 32830, 10.1074/jbc.M111.308528, 3463333, 22847005.
4. Qin Q, Sun Y, Fei M, Zhang J, Jia Y, Gu M, Xia R, Chen S, Deng A. Expression of putative stem marker nestin and CD133 in advanced serous ovarian cancer. Neoplasma 2012, 59:310-315. 310.4149/neo_2012_4040, 10.4149/neo_2012_040, 22296500.
5. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, Parada LF. A restricted cell population propagates glioblastoma growth after chemotherapy. Nat 2012, 488:522-526. 510.1038/nature11287.
6. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008, 8:755-768. 10.1038/nrc2499, 18784658.
7. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100:3983-3988. Epub 2003 Mar 3910, 10.1073/pnas.0530291100, 153034, 12629218.
8. Toole BP, Slomiany MG. Hyaluronan, CD44 and Emmprin: partners in cancer cell chemoresistance. Drug Resist Updat 2008, 11:110-121. 110.1016/j.drup.2008.1004.1002. Epub 2008 May 1019, 10.1016/j.drup.2008.04.002, 2584579, 18490190.
9. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006, 5:67. 10.1186/1476-4598-5-67, 1697823, 17140455.
10. Izumiya M, Kabashima A, Higuchi H, Igarashi T, Sakai G, Iizuka H, Nakamura S, Adachi M, Hamamoto Y, Funakoshi S, et al. Chemoresistance is associated with cancer stem cell-like properties and epithelial-to-mesenchymal transition in pancreatic cancer cells. Anticancer Res 2012, 32:3847-3853.
11. Leung EL, Fiscus RR, Tung JW, Tin VP, Cheng LC, Sihoe AD, Fink LM, Ma Y, Wong MP. Non-small cell lung cancer cells expressing CD44 are enriched for stem cell-like properties. PLoS One 2010, 5:e14062. 14010.11371/journal.pone.0014062, 10.1371/journal.pone.0014062, 2988826, 21124918.
12. Barrett LE, Granot Z, Coker C, Iavarone A, Hambardzumyan D, Holland EC, Nam HS, Benezra R. Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma. Cancer Cell 2012, 21:11-24. doi:10.1016/j.ccr.2011.1011.1025, 10.1016/j.ccr.2011.11.025, 22264785.
13. Ponz-Sarvise M, Nguewa PA, Pajares MJ, Agorreta J, Lozano MD, Redrado M, Pio R, Behrens C, Wistuba II, Garcia-Franco CE, et al. Inhibitor of Differentiation-1 as a Novel Prognostic Factor in NSCLC Patients with Adenocarcinoma Histology and Its Potential Contribution to Therapy Resistance. Clin Cancer Res 2011, 17:4155-4166. Epub 2011 May 4153, 10.1158/1078-0432.CCR-10-3381, 21540238.
14. O'Brien CA, Kreso A, Ryan P, Hermans KG, Gibson L, Wang Y, Tsatsanis A, Gallinger S, Dick JE. ID1 and ID3 regulate the self-renewal capacity of human colon cancer-initiating cells through p21. Cancer Cell 2012, 21:777-792. 710.1016/j.ccr.2012.1004.1036, 10.1016/j.ccr.2012.04.036, 22698403.
15. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, Weissman IL, Clarke MF, Ailles LE. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007, 104:973-978. Epub 2007 Jan 2008, 10.1073/pnas.0610117104, 1783424, 17210912.
16. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney A, Huang EH, Simeone DM, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 2007, 104:10158-10163. Epub 12007 Jun 10154, 10.1073/pnas.0703478104, 1891215, 17548814.
17. Zheng X, Shen G, Yang X, Liu W. Most C6 cells are cancer stem cells: evidence from clonal and population analyses. Cancer Res 2007, 67:3691-3697. 10.1158/0008-5472.CAN-06-3912, 17440081.
18. Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, Pratesi G, Fabbri A, Andriani F, Tinelli S, et al. Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 2009, 106:16281-16286. Epub 12009 Sep 16210, 10.1073/pnas.0905653106, 2741477, 19805294.
19. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nat 2004, 432:396-401.
20. Chen YC, Hsu HS, Chen YW, Tsai TH, How CK, Wang CY, Hung SC, Chang YL, Tsai ML, Lee YY, et al. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS ONE 2008, 3:e2637. 10.1371/journal.pone.0002637, 2440807, 18612434.
21. Janikova M, Skarda J, Dziechciarkova M, Radova L, Chmelova J, Krejci V, Sedlakova E, Zapletalova J, Langova K, Klein J, et al. Identification of cd133+/nestin + putative cancer stem cells in non-small cell lung cancer. BiomedPap Med Fac Univ Olomouc Czech Repub 2010, 154:321-326.
22. Basak SK, Veena MS, Oh S, Huang G, Srivatsan E, Huang M, Sharma S, Batra RK. The malignant pleural effusion as a model to investigate intratumoral heterogeneity in lung cancer. PLoS One 2009, 4:e5884. 10.1371/journal.pone.0005884, 2697051, 19536353.
23. Liu C, Cao X, Zhang Y, Xu H, Zhang R, Wu Y, Lu P, Jin F. Co-expression of Oct-4 and Nestin in human breast cancers. Mol Biol Rep 2012, 39:5875-5881. 5810.1007/s11033-11011-11398-11036. Epub 12011 Dec 11030, 10.1007/s11033-011-1398-6, 22207173.
24. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998, 95:379-391. 10.1016/S0092-8674(00)81769-9, 9814708.
25. Lendahl U, Zimmerman LB, McKay RD. CNS stem cells express a new class of intermediate filament protein. Cell 1990, 60:585-595. 10.1016/0092-8674(90)90662-X, 1689217.
26. Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, Tarasova Y, Wersto RP, Boheler KR, Wobus AM. Nestin expression-a property of multi-lineage progenitor cells?. Cell Mol Life Sci 2004, 61:2510-2522. 10.1007/s00018-004-4144-6, 15526158.
27. Espinosa-Jeffrey A, Becker-Catania SG, Zhao PM, Cole R, Edmond J, de Vellis J. Selective specification of CNS stem cells into oligodendroglial or neuronal cell lineage: cell culture and transplant studies. J Neurosci Res 2002, 69:810-825. 10.1002/jnr.10344, 12205675.
28. Oh SY, Kang HJ, Kim YS, Kim H, Lim YC. CD44-negative cells in head and neck squamous carcinoma also have stem-cell like traits. Eur J Cancer 2013, 49:272-280. 210.1016/j.ejca.2012.1006.1004. Epub 2012 Jul 1016, 10.1016/j.ejca.2012.06.004, 22770891.
29. Ying QL, Nichols J, Chambers I, Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 2003, 115:281-292. 10.1016/S0092-8674(03)00847-X, 14636556.
30. Hollnagel A, Oehlmann V, Heymer J, Ruther U, Nordheim A. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J Biol Chem 1999, 274:19838-19845. 10.1074/jbc.274.28.19838, 10391928.
31. Kurooka H, Nakahiro T, Mori K, Sano K, Yokota Y. BMP signaling is responsible for serum-induced Id2 expression. Biochem Biophys Res Commun 2012, 420:281-287. 210.1016/j.bbrc.2012.1002.1150. Epub 2012 Mar 1016, 10.1016/j.bbrc.2012.02.150, 22421219.
32. Langenfeld E, Hong CC, Lanke G, Langenfeld J. Bone morphogenetic protein type I receptor antagonists decrease growth and induce cell death of lung cancer cell lines. PLoS One 2013, 8:e61256. 61210.61371/journal.pone.0061256. Print 0062013, 10.1371/journal.pone.0061256, 3625205, 23593444.
33. Langenfeld EM, Kong Y, Langenfeld J. Bone morphogenetic protein-2-induced transformation involves the activation of mammalian target of rapamycin. Mol Cancer Res 2005, 3:679-684. 10.1158/1541-7786.MCR-05-0124, 16380505.
34. Gerrard L, Zhao D, Clark AJ, Cui W. Stably transfected human embryonic stem cell clones express OCT4-specific green fluorescent protein and maintain self-renewal and pluripotency. Stem Cells 2005, 23:124-133. 10.1634/stemcells.2004-0102, 15625129.
35. Solway J, Seltzer J, Samaha FF, Kim S, Alger LE, Niu Q, Morrisey EE, Ip HS, Parmacek MS. Structure and expression of a smooth muscle cell-specific gene, SM22 alpha. J Biol Chem 1995, 270:13460-13469. 10.1074/jbc.270.22.13460, 7768949.
36. Langenfeld EM, Kong Y, Langenfeld J. Bone morphogenetic protein 2 stimulation of tumor growth involves the activation of Smad-1/5. Oncogene 2006, 25:685-692. 10.1038/sj.onc.1209110, 16247476.
37. Langenfeld EM, Calvano SE, Abou-Nukta F, Lowry SF, Amenta P, Langenfeld J. The mature bone morphogenetic protein-2 is aberrantly expressed in non-small cell lung carcinomas and stimulates tumor growth of A549 cells. Carcinog 2003, 24:1445-1454. Epub 2003 Jun 1419.
38. Kellner S, Kikyo N. Transcriptional regulation of the Oct4 gene, a master gene for pluripotency. Histol Histopathol 2010, 25:405-412. 3418322, 20054811.
39. Li YQ. Master stem cell transcription factors and signaling regulation. Cell Reprogram 2010, 12:3-13. 10.1089/cell.2009.0033, 20132009.
40. Lepore AC, Han SS, Tyler-Polsz CJ, Cai J, Rao MS, Fischer I. Differential fate of multipotent and lineage-restricted neural precursors following transplantation into the adult CNS. Neuron Glia Biol 2004, 1:113-126. 10.1017/S1740925X04000213, 1389711, 16520830.
41. Ryuge S, Sato Y, Wang GQ, Matsumoto T, Jiang SX, Katono K, Inoue H, Satoh Y, Masuda N. Prognostic significance of nestin expression in resected non-small cell lung cancer. Chest 2011, 139:862-869. Epub 2010 Sep 2019, 10.1378/chest.10-1121, 20829334.
42. Redshaw Z, Strain AJ. Human haematopoietic stem cells express Oct4 pseudogenes and lack the ability to initiate Oct4 promoter-driven gene expression. J Negat Results Biomed 2011, 9:2.
43. Elkabetz Y, Panagiotakos G, Al Shamy G, Socci ND, Tabar V, Studer L. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 2008, 22:152-165. 110.1101/gad.1616208, 10.1101/gad.1616208, 2192751, 18198334.
44. Biunno I, Cattaneo M, Orlandi R, Canton C, Biagiotti L, Ferrero S, Barberis M, Pupa SM, Scarpa A, Menard S. SEL1L a multifaceted protein playing a role in tumor progression. J Cell Physiol 2006, 208:23-38. 10.1002/jcp.20574, 16331677.
45. Ferrero S, Falleni M, Cattaneo M, Malferrari G, Canton C, Biagiotti L, Maggioni M, Nosotti M, Coggi G, Bosari S, Biunno I. SEL1L expression in non-small cell lung cancer. Hum Pathol 2006, 37:505-512. Epub 2006 Mar 2020, 10.1016/j.humpath.2005.12.012, 16647946.
46. Leonardi R, Zhang YM, Yun MK, Zhou R, Zeng FY, Lin W, Cui J, Chen T, Rock CO, White SW, Jackowski S. Modulation of pantothenate kinase 3 activity by small molecules that interact with the substrate/allosteric regulatory domain. Chem Biol 2010, 17:892-902. 810.1016/j.chembiol.2010.1006.1006, 10.1016/j.chembiol.2010.06.006, 2929395, 20797618.
47. Banerjee S, Brooks WS, Crawford DF. Inactivation of the ubiquitin conjugating enzyme UBE2Q2 causes a prophase arrest and enhanced apoptosis in response to microtubule inhibiting agents. Oncogene 2007, 26:6509-6517. Epub 2007 Apr 6530, 10.1038/sj.onc.1210471, 17471241.
48. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nat 2003, 425:836-841.
49. Mizuseki K, Sakamoto T, Watanabe K, Muguruma K, Ikeya M, Nishiyama A, Arakawa A, Suemori H, Nakatsuji N, Kawasaki H, et al. Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells. Proc Natl Acad Sci USA 2003, 100:5828-5833. Epub 2003 Apr 5830, 10.1073/pnas.1037282100, 156286, 12724518.
50. Zimmerman LB, De Jesus-Escobar JM, Harland RM. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 1996, 86:599-606. 10.1016/S0092-8674(00)80133-6, 8752214.
51. Guo Y, Liu S, Wang P, Zhao S, Wang F, Bing L, Zhang Y, Ling EA, Gao J, Hao A. Expression profile of embryonic stem cell-associated genes Oct4, Sox2 and Nanog in human gliomas. Histopathol 2011, 59:763-775. 710.1111/j.1365-2559.2011.03993.x.
52. Matsuda Y, Naito Z, Kawahara K, Nakazawa N, Korc M, Ishiwata T. Nestin is a novel target for suppressing pancreatic cancer cell migration, invasion and metastasis. Cancer 2011, 11:512-523. Epub 2011.
53. Park D, Xiang AP, Mao FF, Zhang L, Di CG, Liu XM, Shao Y, Ma BF, Lee JH, Ha KS, et al. Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 2010, 28:2162-2171. 10.1002/stem.541, 20963821.
54. Sountoulidis A, Stavropoulos A, Giaglis S, Apostolou E, Monteiro R, de Sousa Lopes SM C, Chen H, Stripp BR, Mummery C, Andreakos E, Sideras P. Activation of the Canonical Bone Morphogenetic Protein (BMP) Pathway during Lung Morphogenesis and Adult Lung Tissue Repair. PLoS One 2012, 7:e41460. Epub 42012 Aug 41420, 10.1371/journal.pone.0041460, 3423416, 22916109.
55. Langenfeld EM, Bojnowski J, Perone J, Langenfeld J. Expression of bone morphogenetic proteins in human lung carcinomas. Ann Thorac Surg 2005, 80:1028-1032. 10.1016/j.athoracsur.2005.03.094, 16122479.
56. Le Page C, Puiffe ML, Meunier L, Zietarska M, de Ladurantaye M, Tonin PN, Provencher D, Mes-Masson AM. BMP-2 signaling in ovarian cancer and its association with poor prognosis. J Ovarian Res 2009, 2:4. 10.1186/1757-2215-2-4, 2674440, 19366455.
57. Park Y, Kang MH, Seo HY, Park JM, Choi CW, Kim YH, Kim IS, Kim JS, Oh SC. Bone morphogenetic protein-2 levels are elevated in the patients with gastric cancer and correlate with disease progression. Med Oncol 2010, 27:1192-1199. 10.1007/s12032-009-9358-x, 19924575.
58. Fong YC, Li TM, Wu CM, Hsu SF, Kao ST, Chen RJ, Lin CC, Liu SC, Wu CL, Tang CH. BMP-2 increases migration of human chondrosarcoma cells via PI3K/Akt pathway. J Cell Physiol 2008, 217:846-855. 10.1002/jcp.21568, 18720410.
59. Rothhammer T, Bataille F, Spruss T, Eissner G, Bosserhoff AK. Functional implication of BMP4 expression on angiogenesis in malignant melanoma. Oncogene 2007, 26:4158-4170. Epub 2006 Dec 4118, 10.1038/sj.onc.1210182, 17173062.
60. Qiu H, Yang B, Pei ZC, Zhang Z, Ding K. WSS25 inhibits growth of xenografted hepatocellular cancer cells in nude mice by disrupting angiogenesis via blocking bone morphogenetic protein (BMP)/Smad/Id1 signaling. J Biol Chem 2010, 285:32638-32646. Epub 32010 Aug 32632, 10.1074/jbc.M110.105544, 2952266, 20679340.
61. Lai TH, Fong YC, Fu WM, Yang RS, Tang CH. Osteoblasts-derived BMP-2 enhances the motility of prostate cancer cells via activation of integrins. Prostate 2008, 68:1341-1353. 10.1002/pros.20799, 18512729.
62. Clement JH, Raida M, Sanger J, Bicknell R, Liu J, Naumann A, Geyer A, Waldau A, Hortschansky P, Schmidt A, et al. Bone morphogenetic protein 2 (BMP-2) induces in vitro invasion and in vivo hormone independent growth of breast carcinoma cells. Int J Oncol 2005, 27:401-407.
63. Raida M, Clement JH, Ameri K, Han C, Leek RD, Harris AL. Expression of bone morphogenetic protein 2 in breast cancer cells inhibits hypoxic cell death. Int J Oncol 2005, 26:1465-1470.
64. Raida M, Clement JH, Leek RD, Ameri K, Bicknell R, Niederwieser D, Harris AL. Bone morphogenetic protein 2 (BMP-2) and induction of tumor angiogenesis. J Cancer Res Clin Oncol 2005, 131:741-750. Epub 2005 Nov 2001, 10.1007/s00432-005-0024-1, 16136355.