Geminin overexpression promotes imatinib sensitive breast cancer: A novel treatment approach for aggressive breast cancers, including a subset of triple negative

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Blanchard, Zannel ^a   Mullins, Nicole ^a   Ellipeddi, Pavani ^a   Lage, Janice M ^b   McKinney, Shawn ^b   El Etriby, Rana ^a   Zhang, Xu ^a   Isokpehi, Raphael ^c   Hernandez, Brenda ^d   ElShamy, Wael M ^a  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^c Jackson State University   (United States)

^d UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; DOXORUBICIN; GEMININ; IMATINIB; NILOTINIB; ANTINEOPLASTIC AGENT; BENZAMIDE DERIVATIVE; PIPERAZINE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CANCER MODEL; CANCER PATIENT; CELL NUCLEUS; COHORT ANALYSIS; CONTROLLED STUDY; CYTOPLASM; DISEASE ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; ONCOGENE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRIPLE NEGATIVE BREAST CANCER; TUMOR INVASION; FEMALE; METABOLISM; PHOSPHORYLATION; TRIPLE NEGATIVE BREAST NEOPLASMS;

ANTINEOPLASTIC AGENTS; BENZAMIDES; FEMALE; GEMININ; HUMANS; PHOSPHORYLATION; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-ABL; PYRIMIDINES; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84899715179     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095663     Document Type: Article

References (66)

1. McGarry T, Kirschner M (2011) Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93(6): 1043-5321.
2. Wohlschlegel J, Dwyer B, Dhar S, Cvetic C, Walter J, et al (2000) Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290: 2309-2312. (Pubitemid 32041574)
3. Thépaut M, Maiorano D, Guichou J, Augé M, Dumas C, et al (2004) Crystal structure of the coiled-coil dimerization motif of geminin: structural and functional insights on DNA replication regulation. J Mol Biol 342(1): 275-287. (Pubitemid 39094520)
4. Kroll K, Salic A, Evans L, Kirschner M (1998) Geminin, a neutralizing molecule that demarcates the future neural plate at the onset of gastrulation. Development 125: 3247-3258. (Pubitemid 28434422)
5. Del Bene F, Tessmar-Raible K, Wittbrodt J (2004) Direct interaction of geminin and Six3 in eye development. Nature 427: 745-749. (Pubitemid 38294594)
6. Luo L, Yang X, Takihara Y, Knoetgen H, Kessel M (2004) The cell-cycle regulator geminin inhibits Hox function through direct and polycomb-mediated interactions. Nature 427: 749-753. (Pubitemid 38294595)
7. Kadam S, McAlpine G, Phelan M, Kingston R, Jones K et al (2004) Functional selectivity of recombinant mammalian SWI/SNF subunits. Genes Dev 14: 2441-2451.
8. Nakuci E, Xu M, Pujana M, Valls J, ElShamy WM (2006) Geminin is bound to chromatin in G2/M phase to promote proper cytokinesis. Int J Biochem Cell Biol 38(7): 1207-1220.
9. Gardner L, Malik R, Shimizu Y, Mullins N, ElShamy WM (2011) Geminin overexpression prevents the completion of topoisomerase IIa chromosome decatenation leading to aneuploidy in human mammary epithelial cells. Breast Cancer Res 13(3): R53.
10. Blanchard Z, Malik R, Mullins N, Maric C, Luk H, et al (2011) Geminin overexpression induces mammary tumors via suppressing cytokinesis. Oncotarget 2(12): 1011-1027.
11. Giet R, Glover M (2001) Drosophila Aurora B kinase is required for histone H3 phosphorylation and condensing recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 152: 669-681. (Pubitemid 34280153)
12. Salabat M, Melstrom L, Strouch M, Ding X, Milam B, et al (2008) Geminin is overexpressed in human pancreatic cancer and downregulated by the bioflavanoid apigenin in pancreatic cancer cell lines. Mol Carcinog 47(11): 835-844.
13. Nishihara K, Shomori K, Tamura T, Fujioka S, Ogawa T, et al (2009) Immunohistochemical expression of geminin in colorectal cancer: Implication of prognostic significance. Oncol Rep 21(5): 1189-1195.
14. Yamazaki M, Fujii S, Murata Y, Hayashi R, Ochiai A (2010) High expression level of geminin predicts a poor clinical outcome in salivary gland carcinomas. Histopathology. 56(7): 883-892.
15. Haruki T, Shomori K, Hamamoto Y, Taniguchi Y, Nakamura H, et al. (2011) Geminin expression in small lung adenocarcinomas: implication of prognostic significance. Lung Cancer. 71(3): 356-362.
16. Kimura F, Okayasu I, Kakinuma H, Satoh Y, Kuwao S, et al (2013) Differential diagnosis of reactive mesothelial cells and malignant mesothelioma cells using the cell proliferation markers minichromosome maintenance protein 7, geminin, topoisomerase II alpha and Ki-67. Acta Cytol 57(4): 384-390.
17. Plattner R, Kadlec L, Demali K, Kazlauskas A, Pendergast A (1999) C-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev 13: 2400-2411. (Pubitemid 29453611)
18. Colicelli J (2010) ABL tyrosine kinases: evolution of function, regulation, and specificity. Sci Signal 3(139): re6.
19. Taagepera S, McDonald D, Loeb J, Whitaker L, McElroy A (1998) Nuclear-cytoplasmic shuttling of c-Abl tyrosine kinase. Proc Natl Acad Sci USA 95: 7457-7462. (Pubitemid 28293274)
20. Van Etten R, Jackson P, Baltimore D, Sanders M, Matsudaira P, et al (1994) The COOH terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains and bundling activity. J Cell Biol 124: 325-340.
21. Melo L (1996) The diversity of BCR-ABL fusion proteins and their relationship to leukemia phenotype. Blood 88: 2375-2384.
22. Baskaran R, Wood L, Whitaker L, Canman C, Morgan S, et al (1997) Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature 387: 516-519. (Pubitemid 27235471)
23. Shaul Y, Ben-Yehoyada M (2005) Role of c-Abl in the DNA damage stress response. Cell Res 15: 33-35. (Pubitemid 41653962)
24. Aoyama K, Fukumoto Y, Ishibashi K, Kubota S, Morinaga T, et al (2011) Nuclear c-Abl-mediated tyrosine phosphorylation induces chromatin structural changes through histone modifications that include H4K16 hypoacetylation. Exp Cell Res 317: 2874-2903.
25. Santos F, Ravandi F (2009) Advances in treatment of chronic myelogenous leukemia - new treatment options with tyrosine kinase inhibitors. Leuk Lymphoma 50(Suppl 2): 16-26.
26. Srinivasan D, Plattner R (2006) Activation of Abl tyrosine kinases promotes invasion of aggressive breast cancer cells. Cancer Res 66: 5648-5655. (Pubitemid 43927117)
27. Srinivasan D, Kaetzel D, Plattner R (2009) Reciprocal regulation of Abl and receptor tyrosine kinases. Cell Signal 21: 1143-1150.
28. Ganguly S, Fiore L, Sims L, Friend J, Srinivasan D, et al (2012) C-Abl and Arg are activated in human primary melanomas, promote melanoma cell invasion via distinct pathways, and drive metastatic progression. Oncogene 31(14): 1804-1816.
29. Lin J, Sun T, Ji L, Deng W, Roth J, et al (2007) Oncogenic activation of c-Abl in non-small cell lung cancer cells lacking FUS1 expression: inhibition of c-Abl by the tumor suppressor gene product Fus1. Oncogene 26: 6989-6996. (Pubitemid 350014606)
30. Peng B, Lloyd P, Schran H (2005) Clinical pharmacokinetics of imatinib. Clin Pharmacokinet 44: 879-894. (Pubitemid 41252840)
31. Dematteo R (2009) Nanoneoadjuvant therapy of gastrointestinal stromal tumor (GIST). Ann Surg Oncol 16: 799-800.
32. Druker B, Talpaz M, Resta D, Peng B, Buchdunger E, et al (2001) Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N. Engl J Med 344: 1031-1037. (Pubitemid 32267972)
33. Reichardt P, Montemurro M (2010) Clinical experience to date with nilotinib in gastrointestinal stromal tumors. Semin Oncol 38(Suppl 1): S20-S27.
34. Saglio G, Kim D, Issaragrisil S, le Coutre P, Etienne G, et al (2010) Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. N Engl J Med 362(24): 2251-2219.
35. Kulartz M, Hiller E, Kappes F, Pinna L, Knippers R (2004) Protein kinase CK2 phosphorylates the cell cycle regulatory protein Geminin. Biochem Biophys Res Commun 315(4): 1011-1017. (Pubitemid 38249403)
36. Amoui M, Miller W (2000) The substrate specificity of the catalytic domain of Abl plays an important role in directing phosphorylation of the adaptor protein Crk. Cell Signal 12(9-10): 637-643.
37. Ruchaud S, Carmena M, Earnshaw W (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798-812. (Pubitemid 47462135)
38. Neve R, Chin K, Fridlyand F, Yeh J, Baehner F, et al (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10: 515-527. (Pubitemid 44854747)
39. Greenberg S, Rugo H (2010) Challenging clinical scenarios: treatment of patients with triple-negative or basal-like metastatic breast cancer. Clin Breast Cancer 10(Suppl 2) S20-S29.
40. Ringnér M, Fredlund E, Häkkinen J, Borg Å, Staaf J (2011) GOBO: gene expression-based outcome for breast cancer online. PLoS One 6: e17911.
41. Duesberg P, Rasnick D, Li R, Winters L, Rausch R, et al (1999) How aneuploidy may cause cancer and genetic instability. Anticancer Res 19(6A): 4887-4906.
42. Margolis R (2005) Tetraploidy and tumor development. Cancer Cell 8(5): 353-354.
43. Sistayanarain A, Tsuneyama K, Zheng H, Takahashi H, Nomoto K (2006) Expression of Aurora-B kinase and phosphorylated histone H3 in hepatocellular carcinoma. Anticancer Res 26(5A): 3585-3593. (Pubitemid 44701543)
44. Yoshida K, Yamaguchi Y, Natsume T, Kufe D, Miki Y (2005) JNK phosphorylation of 14-3-3 proteins regulates nuclear targeting of c-Abl in the apoptotic response to DNA damage. Nat Cell Biol 7(3): 278-285. (Pubitemid 40331129)
45. Mancini M, Veljkovic N, Corradi V, Zuffa E, Corrado P, et al (2009) 14-3-3 ligand prevents nuclear import of c-ABL protein in chronic myeloid leukemia. Traffic 10(6): 637-647.
46. Zurita M, Lara P, del Moral R, Torres B, Linares-Fernández J, et al (2010) Hypermethylated 14-3-3-sigma and ESR1 gene promoters in serum as candidate biomarkers for the diagnosis and treatment efficacy of breast cancer metastasis. BMC Cancer 10, 217.
47. Matsubara T, Ikeda M, Kiso Y, Sakuma M, Yoshino K, et al (2012) c-Abl tyrosine kinase regulates serum-induced nuclear export of diacylglycerol kinase α by phosphorylation at Tyr-218. J Biol Chem 287(8): 5507-5517.
48. Zhao H, Chen MS, Lo YH, Waltz SE, Wang J, et al (2014) The Ron receptor tyrosine kinase activates c-Abl to promote cell proliferation through tyrosine phosphorylation of PCNA in breast cancer. Oncogene 13(33): 1429-1437.
49. Oh A, Lahusen J, Chien C, Fereshteh M, Zhang X, et al (2008) Tyrosine phosphorylation of the nuclear receptor coactivator AIB1/SRC-3 is enhanced by Abl kinase and is required for its activity in cancer cells. Mol Cell Biol 28(21): 6580-6593.
50. Chen C, Shang X, Cui L, Xu T, Luo J, et al (2008) L-selectin ligation-induced CSF-1 gene transcription is regulated by AP-1 in a c-Abl kinase-dependent manner. Hum Immunol 69(8): 501-519.
51. Jing Y, Song Z, Wang M, Tang W, Hao S, et al (2005) c-Abl tyrosine kinase regulates c-fos gene expression via phosphorylating RNA polymerase II. Arch Biochem Biophys 15, 437(2): 199-204.
52. Lin J, Arlinghaus R (2008) Activated c-Abl tyrosine kinase in malignant solid tumors. Oncogene. 27: 4385-4391.
53. Zhoa H, Ou-Yang F, Chen I, Hou M, Yaun S, et al (2010) Enhanced Resistance to Tamoxifen by the c-Abl Proto-oncogene in Breast Cancer. Neoplasia 12(3): 214-223.
54. Rappa G, Anzanello F, Lorico A (2011) Imatinib mesylate enhances the malignant behavior of human breast carcinoma cells. Cancer Chemother Pharmacol 67(4): 919-926.
55. Ngebraateno B, Odstad Ø (1999) Site-specific experimental metastasis patterns of two human breast cancer cell lines in nude Rats. Int J Cancer 82: 219-225.
56. Waterfield W, Tashima C, Hortobagyi G, Blumenschein G, Buzdar A, et al (1978) Adriamycin and 1-(2-chlorethyl)-3-cyclohexyl-1-nitrosourea (CCNU) in the treatment of metastatic breast cancer. Cancer 41: 1235-1239. (Pubitemid 8330402)
57. Pishvaian M, Slack R, Koh E, Beumer J, Hartley M, et al (2012) A Phase I clinical trial of the combination of imatinib and paclitaxel in patients with advanced or metastatic solid tumors refractory to standard therapy. Cancer Chemother Pharmacol 70(6): 843-853.
58. Chew H, Barlow W, Albain K, Lew D, Gown A, et al (2008) A phase II study of imatinib mesylate and capecitabine in metastatic breast cancer: Southwest Oncology Group Study 0338. Clin Breast Cancer 8(6): 511-515.
59. Pantaleo M, Saponara M, Nannini M, Biasco G (2007) Targeted therapies in solid tumours: results and promises. Minerva Med 98(5): 603-623. (Pubitemid 350240287)
60. ElShamy WM, Livingston DM (2004) Identification of BRCA1-IRIS, a BRCA1 locus product. Nat Cell Biol 6(10): 954-967. (Pubitemid 39359848)
61. Cipres A, Abassi Y, Vuori K (2007) Abl functions as a negative regulator of Met-induced cell motility via phosphorylation of the adapter protein CrkII. Cell Signal. 19(8): 1662-1670. (Pubitemid 46935423)
62. Allred D, Harvey J, Berardo M, et al (1998) Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 11: 155-168. (Pubitemid 28144151)
63. Allred D, Clark G, Elledge R, et al (1993) Association of p53 protein expression with tumor cell proliferation rate and clinical outcome in node-negative breast cancer. J Natl Cancer Inst 85: 200-206. (Pubitemid 23046895)
64. Matros E, Wang Z, Lodeiro G, Miron A, Iglehart J, et al (2005) BRCA1 promoter methylation in sporadic breast tumors: relationship to gene expression profiles. Breast Cancer Res Treat 91(2): 179-186. (Pubitemid 40684930)
65. Wang Z, Lin M, Wei L, Li C, Miron A, et al. (2004) Loss of heterozygosity and its correlation with expression profiles in subclasses of invasive breast cancers. Cancer Res 64: 64-71. (Pubitemid 38114083)
66. Signoretti S, Di Marcotullio L, Richardson A, Ramaswamy S, Isaac B, et al (2002) Oncogenic role of the ubiquitin ligase subunit Skp2 in human breast cancer. J Clin Invest 110: 633-641. (Pubitemid 34988787)