Survival and proliferation of neural progenitor-derived glioblastomas under hypoxic stress is controlled by a CXCL12/CXCR4 Autocrine-Positive Feedback Mechanism

Clinical Cancer Research

Volumn 23, Issue 5, 2017, Pages 1250-1262

  Calinescu, Anda Alexandra ^a   Yadav, Viveka Nand ^a   Carballo, Erica ^a   Kadiyala, Padma ^a   Tran, Dustin ^a   Zamler, Daniel B ^a   Doherty, Robert ^a   Srikanth, Maithreyi ^a   Lowenstein, Pedro Ricardo ^a   Castro, Maria Graciela ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; DNA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PLERIXAFOR; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; SLEEPING BEAUTY TRANSPOSASE, HUMAN; STROMAL CELL DERIVED FACTOR 1; TRANSPOSASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CELL CYCLE PROGRESSION; CELL HYPOXIA; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE COURSE; DISEASE RESISTANCE; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA STEM CELL; HEMATOPOIETIC STEM CELL; HISTOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LATERAL BRAIN VENTRICLE; MOUSE; NEOPLASM; NEURAL STEM CELL; NEWBORN; NONHUMAN; POSITIVE FEEDBACK; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; RECURRENT DISEASE; SLEEPING BEAUTY TRANSPOSASE METHOD; THERAPY EFFECT; TRANSPOSON; TUMOR SUPPRESSOR GENE; ANIMAL; CANCER STEM CELL; GENETICS; MOLECULARLY TARGETED THERAPY; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR RECURRENCE;

ANIMALS; APOPTOSIS; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; CHEMOKINE CXCL12; GLIOBLASTOMA; HUMANS; MICE; MOLECULAR TARGETED THERAPY; NEOPLASM RECURRENCE, LOCAL; NEOPLASTIC STEM CELLS; NEURAL STEM CELLS; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; TRANSPOSASES;

EID: 85014715425     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-2888     Document Type: Article

References (67)

1. Ahmed AU, Auffinger B, Lesniak MS. Understanding glioma stem cells: rationale, clinical relevance and therapeutic strategies. Expert Rev Neurother 2013; 13:545-55.
2. Zong H, Parada LF, Baker SJ. Cell of origin for malignant gliomas and its implication in therapeutic development. Cold Spring Harb Perspect Biol 2015; 7:1-12.
3. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444:756-60.
4. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 2006; 66:7843-8.
5. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010; 468:829-33.
6. Stiles CD, Rowitch DH. Glioma stem cells: a midterm exam. Neuron 2008; 58:832-46.
7. Sanai N, Alvarez-Buylla A, Berger MS. Neural stem cells and the origin of gliomas. N Engl J Med 2005; 353:811-22.
8. Caporaso GL, Lim DA, Alvarez-Buylla A, Chao MV. Telomerase activity in the subventricular zone of adult mice. Mol Cell Neurosci 2003; 23:693-702.
9. Marian CO, Cho SK, McEllin BM, Maher EA, Hatanpaa KJ, Madden CJ, et al. The telomerase antagonist, imetelstat, efficiently targets glioblastoma tumor-initiating cells leading to decreased proliferation and tumor growth. Clin Cancer Res 2010; 16:154-63.
10. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63:5821-8.
11. Ligon KL, Huillard E, Mehta S, Kesari S, Liu H, Alberta JA, et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 2007; 53:503-17.
12. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Sub-ventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999; 97:703-16.
13. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008; 3:265-78.
14. Fuentealba LC, Obernier K, Alvarez-Buylla A. Adult neural stem cells bridge their niche. Cell Stem Cell 2012; 10:698-708.
15. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007; 11:69-82.
16. Goffart N, Kroonen J, Di Valentin E, Dedobbeleer M, Denne A, Martinive P, et al. Adult mouse subventricular zones stimulate glioblastoma stem cells specific invasion through CXCL12/CXCR4 signaling. Neuro Oncol 2015; 17:81-94.
17. Tabatabai G, Frank B, Mohle R, Weller M, Wick W. Irradiation and hypoxia promote homing of haematopoietic progenitor cells towards gliomas by TGF-beta-dependent HIF-1alpha-mediated induction of CXCL12. Brain 2006; 129:2426-35.
18. Komatani H, Sugita Y, Arakawa F, Ohshima K, Shigemori M. Expression of CXCL12 on pseudopalisading cells and proliferating microvessels in glioblastomas: an accelerated growth factor in glioblastomas. Int J Oncol 2009; 34:665-72.
19. Soeda A, Park M, Lee D, Mintz A, Androutsellis-Theotokis A, McKay RD, et al. Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 2009; 28:3949-59.
20. Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S, et al. Hypoxiainducible factors regulate tumorigenic capacity ofglioma stem cells. Cancer Cell 2009; 15:501-13.
21. Aiuti A, Webb IJ, Bleul C, Springer T, Gutierrez-Ramos JC. The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J Exp Med 1997; 185:111-20.
22. Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, et al. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci U S A 1998; 95:9448-53.
23. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998; 393:595-9.
24. Teicher BA, Fricker SP. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res 2010; 16:2927-31.
25. Rubin JB, Kung AL, Klein RS, Chan JA, Sun Y, Schmidt K, et al. A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc Natl Acad Sci U S A 2003; 100:13513-8.
26. Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, Brown JM. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J Clin Invest 2010; 120:694-705.
27. Stevenson CB, Ehtesham M, McMillan KM, Valadez JG, Edgeworth ML, Price RR, et al. CXCR4 expression is elevated in glioblastoma multiforme and correlates with an increase in intensity and extent of peritumoral T2-weighted magnetic resonance imaging signal abnormalities. Neurosurgery 2008; 63:560-9.
28. Bian XW, Yang SX, Chen JH, Ping YF, Zhou XD, Wang QL, et al. Preferential expression of chemokine receptor CXCR4 by highly malignant human gliomas and its association with poor patient survival. Neurosurgery 2007; 61:570-8.
29. Ping YF, Yao XH, Jiang JY, Zhao LT, Yu SC, Jiang T, et al. The chemokine CXCL12 and its receptor CXCR4 promote glioma stem cell-mediated VEGF production and tumour angiogenesis via PI3K/AKT signalling. J Pathol 2011; 224:344-54.
30. Bar EE Glioblastoma, cancer stem cells and hypoxia. Brain Pathol 2011; 21:119-29.
31. Calinescu AA, Nunez FJ, Koschmann C, Kolb BL, Lowenstein PR, Castro MG. Transposon mediated integration of plasmid DNA into the subventricular zone of neonatal mice to generate novel models of glioblastoma. J Vis Exp 2015; 96.
32. Lin R, Iacovitti L. Classic and novel stem cell niches in brain homeostasis and repair. Brain Res 2015; 1628:327-42.
33. Ligon KL, Alberta JA, Kho AT, Weiss J, Kwaan MR, Nutt CL, et al. The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J Neuropathol Exp Neurol 2004; 63:499-509.
34. Wiesner SM, Decker SA, Larson JD, Ericson K, Forster C, Gallardo JL, et al. De novo induction of genetically engineered brain tumors in mice using plasmid DNA. Cancer Res 2009; 69:431-9.
35. Ding L, Morrison SJ. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 2013; 495:231-5.
36. Lathia JD, Mack SC, Mulkearns-Hubert EE, Valentim CL, Rich JN. Cancer stem cells in glioblastoma. Genes Dev 2015; 29:1203-17.
37. Koschmann C, Calinescu AA, Nunez FJ, Mackay A, Fazal-Salom J, Thomas D, et al. ATRX loss promotes tumor growth and impairs nonhomologous end joining DNA repair in glioma. Sci Transl Med 2016; 8:328ra28.
38. Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci U S A 2000; 97:14720-5.
39. Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 2005; 25:10-8.
40. Gilbertson RJ, Rich JN. Makingatumour's bed: glioblastoma stemcells and the vascular niche. Nat Rev Cancer 2007; 7:733-6.
41. Ausman JI, Shapiro WR, Rall DP. Studies on the chemotherapy of experimental brain tumors: development of an experimental model. Cancer Res 1970; 30:2394-400.
42. McGrath KE, Koniski AD, Maltby KM, McGann JK, Palis J. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol 1999; 213:442-56.
43. Balabanian K, Lagane B, Infantino S, Chow KY, Harriague J, Moepps B, et al. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem 2005; 280:35760-6.
44. Hattermann K, Mentlein R. An infernal trio: the chemokine CXCL12 and its receptors CXCR4 and CXCR7 in tumor biology. Ann Anat 2013; 195:103-10.
45. Li M, Ransohoff RM. Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog Neurobiol 2008; 84:116-31.
46. Cancer Genome Atlas Research N. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455:1061-8.
47. Ali SH, DeCaprio JA. Cellular transformation by SV40 large T antigen: interaction with host proteins. Semin Cancer Biol 2001; 11:15-23.
48. Sidle A, Palaty C, Dirks P, Wiggan O, Kiess M, Gill RM, et al. Activity of the retinoblastoma family proteins, pRB, p107, and p130, during cellular proliferation and differentiation. Crit Rev Biochem Mol Biol 1996; 31:237-71.
49. McDowell KA, Riggins GJ, Gallia GL. Targeting the AKT pathway in glioblastoma. Curr Pharm Des 2011; 17:2411-20.
50. Chiariello E, Roz L, Albarosa R, Magnani I, Finocchiaro G. PTEN/MMAC1 mutations in primary glioblastomas and short-term cultures of malignant gliomas. Oncogene 1998; 16:541-5.
51. Haas-Kogan D, Shalev N, Wong M, Mills G, Yount G, Stokoe D. Protein kinase B (PKB/Akt) activity is elevated in glioblastoma cells due to mutation of the tumor suppressor PTEN/MMAC. Curr Biol 1998; 8: 1195-8.
52. Mao W, Yi X, Qin J, Tian M, Jin G. CXCL12 inhibits cortical neuron apoptosis by increasing the ratio of Bcl-2/Bax after traumatic brain injury. Int J Neurosci 2014; 124:281-90.
53. Hetschko H, Voss V, Horn S, Seifert V, Prehn JH, Kogel D. Pharmacological inhibition of Bcl-2 family members reactivates TRAIL-induced apoptosis in malignant glioma. J Neurooncol 2008; 86:265-72.
54. Tabatabai G, Bahr O, Mohle R, Eyupoglu IY, Boehmler AM, Wischhusen J, et al. Lessons from the bone marrow: how malignant glioma cells attract adult haematopoietic progenitor cells. Brain 2005; 128:2200-11.
55. Martini F, Iaccheri L, Lazzarin L, Carinci P, Corallini A, Gerosa M, et al. SV40 early region and large T antigen in human brain tumors, peripheral blood cells, and sperm fluids from healthy individuals. Cancer Res 1996; 56: 4820-5.
56. Suzuki SO, Mizoguchi M, Iwaki T. Detection of SV40 T antigen genome in human gliomas. Brain Tumor Pathol 1997; 14:125-9.
57. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet 2000; 25:55-7.
58. Marumoto T, Tashiro A, Friedmann-Morvinski D, Scadeng M, Soda Y, Gage FH, et al. Development of a novel mouse glioma model using lentiviral vectors. Nat Med 2009; 15:110-6.
59. de Vries NA, Bruggeman SW, Hulsman D, de Vries HI, Zevenhoven J, Buckle T, et al. Rapid and robust transgenic high-grade glioma mouse models for therapy intervention studies. Clin Cancer Res 2010; 16: 3431-41.
60. de Carvalho AC, Nelson K, Lemke N, Lehman NL, Arbab AS, Kalkanis S, et al. Gliosarcoma stem cells undergo glial and mesenchymal differentiation in vivo. Stem Cells 2010; 28:181-90.
61. Mo W, Chen J, Patel A, Zhang L, Chau V, Li Y, et al. CXCR4/CXCL12 mediate autocrine cell-cycle progression in NF1-associated malignant peripheral nerve sheath tumors. Cell 2013; 152:1077-90.
62. Bhardwaj A, Srivastava SK, Singh S, Arora S, Tyagi N, Andrews J, et al. CXCL12/CXCR4 signaling counteracts docetaxel-induced microtubule stabilization via p21-activated kinase 4-dependent activation of LIM domain kinase 1. Oncotarget 2014; 5:11490-500.
63. Nance E, Zhang C, Shih TY, Xu Q, Schuster BS, Hanes J. Brain-penetrating nanoparticles improve paclitaxel efficacy in malignant glioma following local administration. ACS Nano 2014; 8:10655-64.
64. Burkhart DL, Sage J. Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat Rev Cancer 2008; 8:671-82.
65. Khan MZ, Brandimarti R, Shimizu S, Nicolai J, Crowe E, Meucci O. The chemokine CXCL12 promotes survival of postmitotic neurons by regulating Rb protein. Cell Death Differ 2008; 15:1663-72.
66. Wiedemeyer WR, Dunn IF, Quayle SN, Zhang J, Chheda MG, Dunn GP, et al. Pattern of retinoblastoma pathway inactivation dictates response to CDK4/6 inhibition in GBM. Proc Natl Acad Sci U S A 2010; 107: 11501-6.
67. Heddleston JM, Li Z, McLendon RE, Hjelmeland AB, Rich JN. The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009; 8:3274-84.