FOXD1-ALDH1A3 signaling is a determinant for the self-renewal and tumorigenicity of mesenchymal glioma stem cells

Cancer Research

Volumn 76, Issue 24, 2016, Pages 7219-7230

  Cheng, Peng ^a,b   Wang, Jia ^a,c   Waghmare, Indrayani ^d   Sartini, Stefania ^e   Coviello, Vito ^e   Zhang, Zhuo ^a   Kim, Sung Hak ^a   Mohyeldin, Ahmed ^f   Pavlyukov, Marat S ^a   Minata, Mutsuko ^a   Valentim, Claudia L L ^g   Chhipa, Rishi Raj ^h   Bhat, Krishna P L ⁱ   Dasgupta, Biplab ^h   La Motta, Concettina ^e   Kango Singh, Madhuri ^d   Nakano, Ichiro ^a,j  

^a University of Alabama at Birmingham   (United States)

^b CHINA MEDICAL UNIVERSITY   (China)

^c XI'AN JIAOTONG UNIVERSITY   (China)

^d UNIVERSITY OF DAYTON   (United States)

^e UNIVERSITY OF PISA   (Italy)

^f OHIO STATE UNIVERSITY   (United States)

^g LERNER RESEARCH INSTITUTE   (United States)

^h CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF TEXAS   (United States)

^j UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ALDH1A3; PROTEIN FOXD1; TUMOR PROTEIN; UNCLASSIFIED DRUG; ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE (NAD(P)+); ANTINEOPLASTIC AGENT; FORKHEAD TRANSCRIPTION FACTOR; FOXD1 PROTEIN, HUMAN;

ALDH1A3 GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CARCINOGENICITY; CELL FATE; CELL PROLIFERATION; CELL SELF-RENEWAL; CLINICAL ARTICLE; CLONOGENESIS; CONTROLLED STUDY; FOXD1 GENE; GENE EXPRESSION; GLIOMA; GLIOMA STEM CELL; HUMAN; HUMAN TISSUE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR GENE; ANIMAL; BRAIN TUMOR; CANCER STEM CELL; CELL TRANSFORMATION; CONFOCAL MICROSCOPY; DROSOPHILA; DRUG SCREENING; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STROMA CELL; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; WESTERN BLOTTING;

ALDEHYDE OXIDOREDUCTASES; ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DROSOPHILA; FLUORESCENT ANTIBODY TECHNIQUE; FORKHEAD TRANSCRIPTION FACTORS; GLIOMA; HUMANS; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STROMAL CELLS; MICE; MICE, NUDE; MICROSCOPY, CONFOCAL; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85006893117     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-2860     Document Type: Article

References (44)

1. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008;359:492-507.
2. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96.
3. Venere M, Fine HA, Dirks PB, Rich JN. Cancer stem cells in gliomas: identifying and understanding the apex cell in cancer's hierarchy. Glia 2011;59:1148-54.
4. Bhat KP, Balasubramaniyan V, Vaillant B, Ezhilarasan R, Hummelink K, Hollingsworth F, et al. Mesenchymal differentiation mediated by NF-kappaB promotes radiation resistance in glioblastoma. Cancer Cell 2013;24:331-46.
5. Waghmare I, Roebke A, Minata M, Kango-Singh M, Nakano I. Intercellular cooperation and competition in brain cancers: lessons from Drosophila and human studies. Stem Cells Translational Med 2014;3:1262-8.
6. Mao P, Joshi K, Li J, Kim SH, Li P, Santana-Santos L, et al. Mesenchymal glioma stem cells are maintained by activated glycolytic metabolism involving aldehyde dehydrogenase 1A3. Proc Natl Acad Sci U S A 2013;110:8644-9.
7. Hannenhalli S, Kaestner KH. The evolution of Fox genes and their role in development and disease. Nat Rev Genet 2009;10:233-40.
8. Nakano I. Transcription factors as master regulator for cancer stemness: remove milk from fox? Expert Rev Anticancer Ther 2014;14:873-5.
9. Pierrou S, Hellqvist M, Samuelsson L, Enerback S, Carlsson P. Cloning and characterization of seven human forkhead proteins: binding site specificity and DNA bending. EMBO J 1994;13:5002-12.
10. Hatini V, Huh SO, Herzlinger D, Soares VC, Lai E. Essential role of stromal mesenchyme in kidney morphogenesis revealed by targeted disruption of Winged Helix transcription factor BF-2. Genes Dev 1996;10:1467-78.
11. Thackray VG. Fox tales: regulation of gonadotropin gene expression by forkhead transcription factors. Mol Cell Endocrinol 2014;385:62-70.
12. Carreres MI, Escalante A, Murillo B, Chauvin G, Gaspar P, Vegar C, et al. Transcription factor Foxd1 is required for the specification of the temporal retina in mammals. J Neurosci 2011;31:5673-81.
13. Fetting JL, Guay JA, Karolak MJ, Iozzo RV, Adams DC, Maridas DE, et al. FOXD1 promotes nephron progenitor differentiation by repressing decorin in the embryonic kidney. Development 2014;141:17-27.
14. Hung C, Linn G, Chow YH, Kobayashi A, Mittelsteadt K, Altemeier WA, et al. Role of lung pericytes and resident fibroblasts in the pathogenesis of pulmonary fibrosis. Am J Respir Crit Care Med 2013;188:820-30.
15. Gumbel JH, Patterson EM, Owusu SA, Kabat BE, Jung DO, Simmons J, et al. The forkhead transcription factor, Foxd1, is necessary for pituitary luteinizing hormone expression in mice. PLoS one 2012;7:e52156.
16. Koga M, Matsuda M, Kawamura T, Sogo T, Shigeno A, Nishida E, et al. Foxd1 is a mediator and indicator of the cell reprogramming process. Nat Commun 2014;5:3197.
17. Karlsson J, Holmquist Mengelbier L, Ciornei CD, Naranjo A, O'Sullivan MJ, Gisselsson D. Clear cell sarcoma of the kidney demonstrates an embryonic signature indicative of a primitive nephrogenic origin. Gen Chromosomes Cancer 2014;53:381-91.
18. van der Heul-Nieuwenhuijsen L, Dits NF, Jenster G. Gene expression of forkhead transcription factors in the normal and diseased human prostate. BJU Int 2009;103:1574-80.
19. Zhao YF, Zhao JY, Yue H, Hu KS, Shen H, Guo ZG, et al. FOXD1 promotes breast cancer proliferation and chemotherapeutic drug resistance by targeting p27. Biochem Biophys Res Commun 2015;456:232-7.
20. Kim SH, Ezhilarasan R, Phillips E, Gallego-Perez D, Sparks A, Taylor D, et al. Serine/threonine kinase MLK4 determines mesenchymal identity in glioma stem cells in an NF-kappaB-dependent manner. Cancer Cell 2016; 29:201-13.
21. Cheng P, Phillips E, Kim SH, Taylor D, Hielscher T, Puccio L, et al. Kinome-wide shRNA screen identifies the receptor tyrosine kinase AXL as a key regulator for mesenchymal glioblastoma stem-like cells. Stem Cell Rep 2015;4:899-913.
22. Hu Y, Smyth GK. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 2009;347:70-8.
23. Remmele W, Schicketanz KH. Immunohistochemical determination of estrogen and progesterone receptor content in human breast cancer. Computer-assisted image analysis (QIC score) vs. subjective grading (IRS). Pathol Res Pract 1993;189:862-6.
24. Hutterer M, Knyazev P, Abate A, Reschke M, Maier H, Stefanova N, et al. Axl and growth arrest-specific gene 6 are frequently overexpressed in human gliomas and predict poor prognosis in patients with glioblastoma multiforme. Clin Cancer Res 2008;14:130-8.
25. Verghese S, Bedi S, Kango-Singh M. Hippo signalling controls Dronc activity to regulate organ size in Drosophila. Cell Death Differ 2012;19:1664-76.
26. Ravasi T, Suzuki H, Cannistraci CV, Katayama S, Bajic VB, Tan K, et al. An atlas of combinatorial transcriptional regulation in mouse and man. Cell 2010;140:744-52.
27. Nakano I, Joshi K, Visnyei K, Hu B, Watanabe M, Lam D, et al. Siomycin A targets brain tumor stem cells partially through a MELK-mediated pathway. Neuro-oncol 2011;13:622-34.
28. Joshi K, Banasavadi-Siddegowda Y, Mo X, Kim SH, Mao P, Kig C, et al. MELK-dependent FOXM1 phosphorylation is essential for proliferation of glioma stem cells. Stem Cells 2013;31:1051-63.
29. Minata M, Gu C, Joshi K, Nakano-Okuno M, Hong C, Nguyen CH, et al. Multi-kinase inhibitor C1 triggers mitotic catastrophe of glioma stem cells mainly through MELK kinase inhibition. PLoS One 2014;9:e92546.
30. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006;9:391-403.
31. Bredel M, Bredel C, Juric D, Harsh GR, Vogel H, Recht LD, et al. Functional network analysis reveals extended gliomagenesis pathway maps and three novel MYC-interacting genes in human gliomas. Cancer Res 2005;65:8679-89.
32. Sun L, Hui AM, Su Q, Vortmeyer A, Kotliarov Y, Pastorino S, et al. Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell 2006;9:287-300.
33. Nakano I, Kornblum HI. Methods for analysis of brain tumor stem cell and neural stem cell self-renewal. Methods Mol Biol 2009;568:37-56.
34. Cheng P, Phillips E, Kim SH, Taylor D, Hielscher T, Puccio L, et al. Kinome-wide shRNA screen identifies the receptor tyrosine kinase AXL as a key regulator for mesenchymal glioblastoma stem-like cells. Stem Cell Rep 2015;4:899-913.
35. Lee HH, Frasch M. Survey of forkhead domain encoding genes in the Drosophila genome: Classification and embryonic expression patterns. Dev Dyn 2004;229:357-66.
36. Chakravorty S, Wajda MP, Vigoreaux JO. Courtship song analysis of Drosophila muscle mutants. Methods 2012;56:87-94.
37. Read RD, Cavenee WK, Furnari FB, Thomas JB. A drosophila model for EGFR-Ras and PI3K-dependent human glioma. PLoS Genet 2009;5:e1000374.
38. Gao GY, Li DJ, Keung WM. Synthesis of potential antidipsotropic isoflavones: inhibitors of the mitochondrial monoamine oxidase-aldehyde dehydrogenase pathway. J Med Chem 2001;44:3320-8.
39. Del Turco S, Sartini S, Sentieri C, Saponaro C, Navarra T, Dario B, et al. A novel 2,3-diphenyl-4H-pyrido[1,2-a]pyrimidin-4-one derivative inhibits endothelial cell dysfunction and smooth muscle cell proliferation/activation. Eur J Med Chem 2014;72:102-9.
40. Pajouhesh H, Lenz GR. Medicinal chemical properties of successful central nervous system drugs. NeuroRx 2005;2:541-53.
41. Saigal D, Cunningham SJ, Farres J, Weiner H. Molecular cloning of the mitochondrial aldehyde dehydrogenase gene of Saccharomycesce revisiae by genetic complementation. J Bacteriol 1991;173:3199-208.
42. Pan Q, Li Q, Liu S, Ning N, Zhang X, Xu Y, et al. Concise review: targeting cancer stem cells using immunologic approaches. Stem Cells 2015;33:2085-92.
43. Lathia JD, Mack SC, Mulkearns-Hubert EE, Valentim CL, Rich JN. Cancer stem cells in glioblastoma. Genes Dev 2015;29:1203-17.
44. Tian NM, Pratt T, Price DJ. Foxg1 regulates retinal axon pathfinding by repressing an ipsilateral program in nasal retina and by causing optic chiasm cells to exert a net axonal growth-promoting activity. Development 2008;135:4081-9.