Activation of PKA leads to mesenchymal-to-epithelial transition and loss of tumor-initiating ability

Science

Volumn 351, Issue 6277, 2016, Pages

  Pattabiraman, Diwakar R ^a   Bierie, Brian ^a   Kober, Katharina Isabelle ^a   Thiru, Prathapan ^a   Krall, Jordan A ^a   Zill, Christina ^a   Reinhardt, Ferenc ^a   Tam, Wai Leong ^a,b,c   Weinberg, Robert A ^a,d  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b GENOME INSTITUTE OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ADENYLATE CYCLASE ACTIVATOR; ANTIINFECTIVE AGENT; CHOLERA TOXIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; HISTONE H3; LUCIFERASE; LYSINE; UVOMORULIN; ADENOSINE PHOSPHATE; HISTONE DEMETHYLASE; HOMEODOMAIN PROTEIN; PHF2 PROTEIN, HUMAN;

CANCER; CELLS AND CELL COMPONENTS; ENZYME; ENZYME ACTIVITY; INHIBITION; PROTEIN; TUMOR;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST EPITHELIUM CELL; CARCINOGENESIS; CARCINOMA CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; DEMETHYLATION; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME ACTIVITY; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MESENCHYME CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BREAST TUMOR; CANCER STEM CELL; CELL TRANSFORMATION; DRUG EFFECTS; DRUG SCREENING; EPITHELIUM CELL; FEMALE; GENETIC EPIGENESIS; GENETICS; MAMMARY GLAND; MESODERM; METABOLISM; PATHOLOGY; SECOND MESSENGER; TUMOR CELL LINE;

ADENOSINE MONOPHOSPHATE; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CHOLERA TOXIN; COLFORSIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; EPIGENESIS, GENETIC; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HISTONE DEMETHYLASES; HOMEODOMAIN PROTEINS; HUMANS; MAMMARY GLANDS, HUMAN; MESODERM; MICE; NEOPLASTIC STEM CELLS; SECOND MESSENGER SYSTEMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84960441572     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aad3680     Document Type: Article

References (60)

1. P. B. Gupta et al., Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138, 645-659 (2009). doi: 10.1016/j.cell.2009.06.034; pmid: 19682730
2. J. Chen et al., A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 488, 522-526 (2012). doi: 10.1038/nature11287; pmid: 22854781
3. A. Kreso, J. E. Dick, Evolution of the cancer stem cell model. Cell Stem Cell 14, 275-291 (2014). doi: 10.1016/ j.stem.2014.02.006; pmid: 24607403
4. D. R. Pattabiraman, R. A. Weinberg, Tackling the cancer stem cells-what challenges do they pose? Nat. Rev. Drug Discov. 13, 497-512 (2014). doi: 10.1038/nrd4253; pmid: 24981363
5. B. De Craene, G. Berx, Regulatory networks defining EMT during cancer initiation and progression. Nat. Rev. Cancer 13, 97-110 (2013). doi: 10.1038/nrc3447; pmid: 23344542
6. S. A. Mani et al., The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715 (2008). doi: 10.1016/j.cell.2008.03.027; pmid: 18485877
7. A. P. Morel et al., Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLOS ONE 3, e2888 (2008). doi: 10.1371/journal.pone.0002888; pmid: 18682804
8. C. Chen et al., Evidence for epithelial-mesenchymal transition in cancer stem cells of head and neck squamous cell carcinoma. PLOS ONE 6, e16466 (2011). doi: 10.1371/journal. pone.0016466; pmid: 21304586
9. N. Ahmed, K. Abubaker, J. Findlay, M. Quinn, Epithelial mesenchymal transition and cancer stem cell-like phenotypes facilitate chemoresistance in recurrent ovarian cancer. Curr. Cancer Drug Targets 10, 268-278 (2010). doi: 10.2174/ 156800910791190175; pmid: 20370691
10. J. A. Beavo, L. L. Brunton, Cyclic nucleotide research - still expanding after half a century. Nat. Rev. Mol. Cell Biol. 3, 710-718 (2002). doi: 10.1038/nrm911; pmid: 12209131
11. K. Taskén, E. M. Aandahl, Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol. Rev. 84, 137-167 (2004). doi: 10.1152/physrev.00021.2003; pmid: 14715913
12. S. S. Taylor, R. Ilouz, P. Zhang, A. P. Kornev, Assembly of allosteric macromolecular switches: Lessons from PKA. Nat. Rev. Mol. Cell Biol. 13, 646-658 (2012). doi: 10.1038/nrm3432; pmid: 22992589
13. M. R. MacPherson et al., Phosphorylation of serine 11 and serine 92 as new positive regulators of human Snail1 function: Potential involvement of casein kinase-2 and the cAMPactivated kinase protein kinase A. Mol. Biol. Cell 21, 244-253 (2010). doi: 10.1091/mbc.E09-06-0504; pmid: 19923321
14. D. Shaikh et al., cAMP-dependent protein kinase is essential for hypoxia-mediated epithelial-mesenchymal transition, migration, and invasion in lung cancer cells. Cell. Signal. 24, 2396-2406 (2012). doi: 10.1016/j.cellsig.2012.08.007; pmid: 22954688
15. K. S. Nadella et al., Targeted deletion of Prkar1a reveals a role for protein kinase A in mesenchymal-to-epithelial transition. Cancer Res. 68, 2671-2677 (2008). doi: 10.1158/0008-5472. CAN-07-6002; pmid: 18413734
16. P. S. Amieux et al., Increased basal cAMP-dependent protein kinase activity inhibits the formation of mesoderm-derived structures in the developing mouse embryo. J. Biol. Chem. 277, 27294-27304 (2002). doi: 10.1074/jbc.M200302200; pmid: 12004056
17. R. Iglesias-Bartolome et al., Inactivation of a Ga(s)-PKA tumour suppressor pathway in skin stem cells initiates basal-cell carcinogenesis. Nat. Cell Biol. 17, 793-803 (2015). doi: 10.1038/ncb3164; pmid: 25961504
18. X. Li et al., Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J. Natl. Cancer Inst. 100, 672-679 (2008). doi: 10.1093/jnci/djn123; pmid: 18445819
19. B. Elenbaas et al., Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev. 15, 50-65 (2001). doi: 10.1101/gad.828901; pmid: 11156605
20. M. Al-Hajj, M. S. Wicha, A. Benito-Hernandez, S. J. Morrison, M. F. Clarke, Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. U.S.A. 100, 3983-3988 (2003). doi: 10.1073/pnas.0530291100; pmid: 12629218
21. W. L. Tam et al., Protein kinase C a is a central signaling node and therapeutic target for breast cancer stem cells. Cancer Cell 24, 347-364 (2013). doi: 10.1016/j.ccr.2013.08.005; pmid: 24029232
22. T. T. Onder et al., Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 68, 3645-3654 (2008). doi: 10.1158/0008-5472.CAN-07-2938; pmid: 18483246
23. D. Anastassiou et al., Human cancer cells express Slug-based epithelial-mesenchymal transition gene expression signature obtained in vivo. BMC Cancer 11, 529 (2011). doi: 10.1186/1471- 2407-11-529; pmid: 22208948
24. E. Charafe-Jauffret et al., Gene expression profiling of breast cell lines identifies potential new basal markers. Oncogene 25, 2273-2284 (2006). doi: 10.1038/sj.onc.1209254; pmid: 16288205
25. J. de Rooij et al., Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396, 474-477 (1998). doi: 10.1038/24884; pmid: 9853756
26. M. C. Broillet, S. Firestein, Cyclic nucleotide-gated channels. Molecular mechanisms of activation. Ann. N. Y. Acad. Sci. 868, 730-740 (1999). doi: 10.1111/j.1749-6632.1999.tb11352.x; pmid: 10414360
27. R. B. Meyer Jr., J. P. Miller, Analogs of cyclic AMP and cyclic GMP: General methods of synthesis and the relationship of structure to enzymic activity. Life Sci. 14, 1019-1040 (1974). doi: 10.1016/0024-3205(74)90228-8; pmid: 4362776
28. J. M. Enserink et al., A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat. Cell Biol. 4, 901-906 (2002). doi: 10.1038/ncb874; pmid: 12402047
29. S. A. Orellana, G. S. McKnight, Mutations in the catalytic subunit of cAMP-dependent protein kinase result in unregulated biological activity. Proc. Natl. Acad. Sci. U.S.A. 89, 4726-4730 (1992). doi: 10.1073/pnas.89.10.4726; pmid: 1584809
30. H. D. Soule et al., Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50, 6075-6086 (1990). pmid: 1975513
31. C. L. Sommers, A. Papageorge, G. Wilding, E. P. Gelmann, Growth properties and tumorigenesis of MCF-7 cells transfected with isogenic mutants of rasH. Cancer Res. 50, 67-71 (1990). pmid: 2403419
32. V. Ellenrieder et al., Transforming growth factor beta1 treatment leads to an epithelial-mesenchymal transdifferentiation of pancreatic cancer cells requiring extracellular signal-regulated kinase 2 activation. Cancer Res. 61, 4222-4228 (2001). pmid: 11358848
33. C. T. Guy, R. D. Cardiff, W. J. Muller, Induction of mammary tumors by expression of polyomavirus middle T oncogene: A transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12, 954-961 (1992). doi: 10.1128/MCB.12.3.954; pmid: 1312220
34. J. R. Linnemann et al., Quantification of regenerative potential in primary human mammary epithelial cells. Development 142, 3239-3251 (2015). doi: 10.1242/dev.123554; pmid: 26071498
35. A. Hollestelle et al., Distinct gene mutation profiles among luminal-type and basal-type breast cancer cell lines. Breast Cancer Res. Treat. 121, 53-64 (2010). doi: 10.1007/s10549- 009-0460-8; pmid: 19593635
36. J. B. Shabb, Physiological substrates of cAMP-dependent protein kinase. Chem. Rev. 101, 2381-2412 (2001). doi: 10.1021/cr000236l; pmid: 11749379
37. G. A. Gonzalez, M. R. Montminy, Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59, 675-680 (1989). doi: 10.1016/0092-8674 (89)90013-5; pmid: 2573431
38. M. Johannessen, M. P. Delghandi, U. Moens, What turns CREB on? Cell. Signal. 16, 1211-1227 (2004). doi: 10.1016/ j.cellsig.2004.05.001; pmid: 15337521
39. D. Wu et al., cAMP-responsive element-binding protein regulates vascular endothelial growth factor expression: Implication in human prostate cancer bone metastasis. Oncogene 26, 5070-5077 (2007). doi: 10.1038/sj.onc.1210316; pmid: 17310988
40. R. Singh, B. S. Shankar, K. B. Sainis, TGF-b1-ROS-ATM-CREB signaling axis in macrophage mediated migration of human breast cancer MCF7 cells. Cell. Signal. 26, 1604-1615 (2014). doi: 10.1016/j.cellsig.2014.03.028; pmid: 24705025
41. T. Sheng, S. Chi, X. Zhang, J. Xie, Regulation of Gli1 localization by the cAMP/protein kinase A signaling axis through a site near the nuclear localization signal. J. Biol. Chem. 281, 9-12 (2006). doi: 10.1074/jbc.C500300200; pmid: 16293631
42. A. Baba et al., PKA-dependent regulation of the histone lysine demethylase complex PHF2-ARID5B. Nat. Cell Biol. 13, 668-675 (2011). doi: 10.1038/ncb2228; pmid: 21532585
43. P. Hublitz, M. Albert, A. H. F. M. Peters, Mechanisms of transcriptional repression by histone lysine methylation. Int. J. Dev. Biol. 53, 335-354 (2009). doi: 10.1387/ijdb.082717ph; pmid: 19412890
44. M. P. Saunders et al., A novel cyclic adenosine monophosphate analog induces hypercalcemia via production of 1, 25- dihydroxyvitamin D in patients with solid tumors. J. Clin. Endocrinol. Metab. 82, 4044-4048 (1997). doi: 10.1210/ jcem.82.12.4410; pmid: 9398710
45. D. J. Propper et al., Phase I study of the novel cyclic AMP (cAMP) analogue 8-chloro-cAMP in patients with cancer: Toxicity, hormonal, and immunological effects. Clin. Cancer Res. 5, 1682-1689 (1999). pmid: 10430069
46. J. Taylor-Papadimitriou, P. Purkis, I. S. Fentiman, Cholera toxin and analogues of cyclic AMP stimulate the growth of cultured human mammary epithelial cells. J. Cell. Physiol. 102, 317-321 (1980). doi: 10.1002/jcp.1041020306; pmid: 6248570
47. H. Green, Cyclic AMP in relation to proliferation of the epidermal cell: A new view. Cell 15, 801-811 (1978). doi: 10.1016/0092-8674(78)90265-9; pmid: 83196
48. W. Guo et al., Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 148, 1015-1028 (2012). doi: 10.1016/j.cell.2012.02.008; pmid: 22385965
49. S. R. Daigle et al., Selective killing of mixed lineage leukemia cells by a potent small-molecule DOT1L inhibitor. Cancer Cell 20, 53-65 (2011). doi: 10.1016/j.ccr.2011.06.009; pmid: 21741596
50. C. Dong et al., G9a interacts with Snail and is critical for Snailmediated E-cadherin repression in human breast cancer. J. Clin. Invest. 122, 1469-1486 (2012). doi: 10.1172/JCI57349; pmid: 22406531
51. G. Dontu et al., In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17, 1253-1270 (2003). doi: 10.1101/gad.1061803; pmid: 12756227
52. D. Kim et al., TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013). doi: 10.1186/gb-2013-14-4-r36; pmid: 23618408
53. S.Anders, P. T.Pyl, W. Huber, HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015). doi: 10.1093/bioinformatics/btu638; pmid: 25260700
54. S. Anders, W. Huber, Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010). doi: 10.1186/gb-2010-11-10-r106; pmid: 20979621
55. B. Langmead, S. L. Salzberg, Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012). doi: 10.1038/ nmeth.1923; pmid: 22388286
56. Y. Zhang et al., Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008). doi: 10.1186/gb-2008-9-9-r137; pmid: 18798982
57. H. Shin, T. Liu, A. K. Manrai, X. S. Liu, CEAS: Cis-regulatory element annotation system. Bioinformatics 25, 2605-2606 (2009). doi: 10.1093/bioinformatics/btp479; pmid: 19689956
58. L. Shen, N. Shao, X. Liu, E. Nestler, ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics 15, 284 (2014). doi: 10.1186/1471-2164-15-284; pmid: 24735413
59. A. R. Quinlan, I. M. Hall, BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010). doi: 10.1093/bioinformatics/btq033; pmid: 20110278
60. J. T. Robinson et al., Integrative genomics viewer. Nat. Biotechnol. 29, 24-26 (2011). doi: 10.1038/nbt.1754; pmid: 21221095