Acylglycerol kinase promotes cell proliferation and tumorigenicity in breast cancer via suppression of the FOXO1 transcription factor

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Wang, Xi ^a   Lin, Chuyong ^a   Zhao, Xiaohui ^a   Liu, Aibin ^b   Zhu, Jinrong ^a   Li, Xinghua ^a   Song, Libing ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

AGK; Breast cancer; FOXO1; Tumorigenicity

Indexed keywords

ACYLGLYCEROL KINASE; BROXURIDINE; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; LUCIFERASE; PHOSPHOTRANSFERASE; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG; AGK PROTEIN, HUMAN; CDKN1A PROTEIN, HUMAN; CDKN1B PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, HUMAN; PROTEIN KINASE B; SMALL INTERFERING RNA;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRDU ASSAY; BREAST CANCER; BREAST CANCER CELL LINE; CANCER CELL; CANCER CLASSIFICATION; CANCER PATIENT; CANCER STAGING; CANCER TISSUE; CARCINOGENICITY; CELL PROLIFERATION; CLINICAL FEATURE; COLONY FORMATION; CONTROLLED STUDY; FEMALE; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; OVERALL SURVIVAL; PATHOPHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; TUMOR XENOGRAFT; WESTERN BLOTTING; ADENOCARCINOMA; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST TUMOR; CELL CYCLE; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR INVASION;

ADENOCARCINOMA; ANIMALS; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901193863     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-106     Document Type: Article

References (41)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61:69-90. 10.3322/caac.20107, 21296855.
2. Guo L, Cui ZM, Zhang J, Huang Y. Chemokine axes CXCL12/CXCR4 and CXCL16/CXCR6 correlate with lymph node metastasis in epithelial ovarian carcinoma. Chin J Cancer 2011, 30:336-343. 10.5732/cjc.010.10490, 4013398, 21527066.
3. Zeng Z, Lin H, Zhao X, Liu G, Wang X, Xu R, Chen K, Li J, Song L. Overexpression of GOLPH3 promotes proliferation and tumorigenicity in breast cancer via suppression of the FOXO1 transcription factor. Clin Cancer Res 2012, 18:4059-4069. 10.1158/1078-0432.CCR-11-3156, 22675169.
4. Lu Z. Nonmetabolic functions of pyruvate kinase isoform M2 in controlling cell cycle progression and tumorigenesis. Chin J Cancer 2012, 31:5-7. 3777463, 22200182.
5. Arden KC. FoxOs in tumor suppression and stem cell maintenance. Cell 2007, 128:235-237. 10.1016/j.cell.2007.01.009, 17254960.
6. Paik JH, Kollipara R, Chu G, Ji H, Xiao Y, Ding Z, Miao L, Tothova Z, Horner JW, Carrasco DR, Jiang S, Gilliland DG, Chin L, Wong WH, Castrillon DH, DePinho RA. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 2007, 128:309-323. 10.1016/j.cell.2006.12.029, 1855089, 17254969.
7. Medema RH, Kops GJ, Bos JL, Burgering BM. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 2000, 404:782-787. 10.1038/35008115, 10783894.
8. Kops GJ, Medema RH, Glassford J, Essers MA, Dijkers PF, Coffer PJ, Lam EW, Burgering BM. Control of cell cycle exit and entry by protein kinase B-regulated forkhead transcription factors. Mol Cell Biol 2002, 22:2025-2036. 10.1128/MCB.22.7.2025-2036.2002, 133681, 11884591.
9. Schmidt M, Fernandez de Mattos S, van der Horst A, Klompmaker R, Kops GJ, Lam EW, Burgering BM, Medema RH. Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D. Mol Cell Biol 2002, 22:7842-7852. 10.1128/MCB.22.22.7842-7852.2002, 134724, 12391153.
10. You H, Pellegrini M, Tsuchihara K, Yamamoto K, Hacker G, Erlacher M, Villunger A, Mak TW. FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J Exp Med 2006, 203:1657-1663. 10.1084/jem.20060353, 2118330, 16801400.
11. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol 2000, 10:1201-1204. 10.1016/S0960-9822(00)00728-4, 11050388.
12. Yang JY, Xia W, Hu MC. Ionizing radiation activates expression of FOXO3a, Fas ligand, and Bim, and induces cell apoptosis. Int J Oncol 2006, 29:643-648. 2632978, 16865280.
13. Modur V, Nagarajan R, Evers BM, Milbrandt J. FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer. J Biol Chem 2002, 277:47928-47937. 10.1074/jbc.M207509200, 12351634.
14. Furukawa-Hibi Y, Yoshida-Araki K, Ohta T, Ikeda K, Motoyama N. FOXO forkhead transcription factors induce G (2)-M checkpoint in response to oxidative stress. J Biol Chem 2002, 277:26729-26732. 10.1074/jbc.C200256200, 12048180.
15. Dong XY, Chen C, Sun X, Guo P, Vessella RL, Wang RX, Chung LW, Zhou W, Dong JT. FOXO1A is a candidate for the 13q14 tumor suppressor gene inhibiting androgen receptor signaling in prostate cancer. Cancer Res 2006, 66:6998-7006. 10.1158/0008-5472.CAN-06-0411, 16849544.
16. Ward EC, Hoekstra AV, Blok LJ, Hanifi-Moghaddam P, Lurain JR, Singh DK, Buttin BM, Schink JC, Kim JJ. The regulation and function of the forkhead transcription factor, Forkhead box O1, is dependent on the progesterone receptor in endometrial carcinoma. Endocrinology 2008, 149:1942-1950. 10.1210/en.2007-0756, 2276720, 18096667.
17. Seoane J, Le HV, Shen L, Anderson SA, Massagué J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 2004, 117:211-223. 10.1016/S0092-8674(04)00298-3, 15084259.
18. Guttilla IK, White BA. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J Biol Chem 2009, 284:23204-23216. 10.1074/jbc.M109.031427, 2749094, 19574223.
19. Bektas M, Payne SG, Liu H, Goparaju S, Milstien S, Spiegel S. A novel acylglycerol kinase that produces lysophosphatidic acid modulates cross talk with EGFR in prostate cancer cells. J Cell Biol 2005, 169:801-811. 10.1083/jcb.200407123, 2171605, 15939762.
20. Epand RM, Shulga YV, Timmons HC, Perri AL, Belani JD, Perinpanathan K, Johnson-McIntire LB, Bajjalieh S, Dicu AO, Elias C, Rychnovsky SD, Topham MK. Substrate chirality and specificity of diacylglycerol kinases and the multisubstrate lipid kinase. Biochemistry 2007, 46:14225-14231. 10.1021/bi701584v, 18004883.
21. Zhao Y, Natarajan V. Lysophosphatidic acid signaling in airway epithelium: role in airway inflammation and remodeling. Cell Signal 2009, 21:367-377. 10.1016/j.cellsig.2008.10.010, 2660380, 18996473.
22. Kalari S, Zhao Y, Spannhake EW, Berdyshev EV, Natarajan V. Role of acylglycerol kinase in LPA-induced IL-8 secretion and transactivation of epidermal growth factor-receptor in human bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 2009, 296:328-336.
23. Kim JH, Adelstein RS. LPA (1)-induced migration requires nonmuscle myosin II light chain phosphorylation in breast cancer cells. J Cell Physiol 2011, 226:2881-2893. 10.1002/jcp.22631, 3115449, 21302283.
24. Swamydas M, Nguyen D, Allen LD, Eddy J, Dréau D. Progranulin stimulated by LPA promotes the migration of aggressive breast cancer cells. Cell Commun Adhes 2011, 18:119-130. 10.3109/15419061.2011.641042, 22176685.
25. Du J, Sun C, Hu Z, Yang Y, Zhu Y, Zheng D, Gu L, Lu X. Lysophosphatidic acid induces SKBR3 breast cancer cells migration through activation of PI3K/PAK1/ERK signaling. PLoS One 2010, 5:e15940. 10.1371/journal.pone.0015940, 3012724, 21209852.
26. Chen X, Ying Z, Lin X, Lin H, Wu J, Li M, Song L. Acylglycerol kinase augments JAK2/STAT3 signaling in esophageal squamous cells. J Clin Invest 2013, 123:2576-2589. 10.1172/JCI68143, 3668815, 23676499.
27. Nouh MA, Wu XX, Okazoe H, Tsunemori H, Haba R, Abou-Zeid AM, Saleem MD, Inui M, Sugimoto M, Aoki J, Kakehi Y. Expression of autotaxin and acylglycerol kinase in prostate cancer: association with cancer development and progression. Cancer Sci 2009, 100:1631-1638. 10.1111/j.1349-7006.2009.01234.x, 19549252.
28. Nakamura N, Ramaswamy S, Vazquez F, Signoretti S, Loda M, Sellers WR. Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol Cell Biol 2000, 20:8969-8982. 10.1128/MCB.20.23.8969-8982.2000, 86551, 11073996.
29. Roeb W, Boyer A, Cavenee WK, Arden KC. PAX3-FOXO1 controls expression of the p57Kip2 cell-cycle regulator through degradation of EGR1. Proc Natl Acad Sci U S A 2007, 104:18085-18090. 10.1073/pnas.0708910104, 2084300, 17986608.
30. Cardozo T, Pagano M. The SCF ubiquitin ligase: insights into a molecular mechanism. Nat Rev Mol Cell Biol 2004, 5:739-753. 10.1038/nrm1471, 15340381.
31. Masahiro A, Hao J, Peter KV. Proteasomal degradation of the FOXO1 transcriptional regulator in cells transformed by the PI3K and AKT oncoproteins. Proc Natl Acad Sci U S A 2004, 101:13613-13617. 10.1073/pnas.0405454101, 518802, 15342912.
32. Huang H, Regan KM, Wang F, Wang D, Smith DI, van Deursen JM, Tindall DJ. Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc Natl Acad Sci U S A 2005, 102:1649-1654. 10.1073/pnas.0406789102, 545492, 15668399.
33. Vivanco I, Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2002, 2:489-501. 10.1038/nrc839, 12094235.
34. Tokunaga E, Oki E, Egashira A, Sadanaga N, Morita M, Kakeji Y, Maehara Y. Deregulation of the AKT pathway in human cancer. Curr Cancer Drug Targets 2008, 8:27-36. 10.2174/156800908783497140, 18288941.
35. Armanious H, Deschenes J, Gelebart P, Ghosh S, Mackey J, Lai R. Clinical and biological significance of GSK-3β inactivation in breast cancer-an immunohistochemical study. Hum Pathol 2010, 41:1657-1663. 10.1016/j.humpath.2010.04.015, 20709358.
36. Takahashi RU, Takeshita F, Honma K, Ono M, Kato K, Ochiya T. Ribophorin II regulates breast tumor initiation and metastasis through the functional suppression of GSK3β. Sci Rep 2013, 3:2474. 3747512, 23959174.
37. Li Y, Zhang T, Korkaya H, Liu S, Lee HF, Newman B, Yu Y, Clouthier SG, Schwartz SJ, Wicha MS, Sun D. Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res 2010, 16:2580-2590. 10.1158/1078-0432.CCR-09-2937, 2862133, 20388854.
38. Li J, Zhang N, Song LB, Liao WT, Jiang LL, Gong LY, Wu J, Yuan J, Zhang HZ, Zeng MS, Li M. Astrocyte elevated gene-1 is a novel prognostic marker for breast cancer progression and overall patient survival. Clin Cancer Res 2008, 14:3319-3326. 10.1158/1078-0432.CCR-07-4054, 18519759.
39. Edge S, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. Breast Cancer in AJCC Cancer Staging Handbook. TNM Classification of Malignant Tumors 2010, 255-281. New York: Springer Verlag, 7.
40. Hahn WC, Dessain SK, Brooks MW, King JE, Elenbaas B, Sabatini DM, DeCaprio JA, Weinberg RA. Enumeration of the simian virus 40 early region elements necessary for human cell transformation. Mol Cell Biol 2002, 22:2111-2123. 10.1128/MCB.22.7.2111-2123.2002, 133688, 11884599.
41. Tang ED, Nuñez G, Barr FG, Guan KL. Negative regulation of the forkhead transcription factor FKHR by AKT. J Biol Chem 1999, 274:16741-16746. 10.1074/jbc.274.24.16741, 10358014.