Neural stem cell targeting of glioma is dependent on phosphoinositide 3-kinase signaling

Stem Cells

Volumn 26, Issue 6, 2008, Pages 1575-1586

  Kendall, Stephen E ^a   Najbauer, Joseph ^a   Johnston, Heather F ^b   Metz, Marianne Z ^a   Li, Shan ^a,b   Bowers, Marisa ^a   Garcia, Elizabeth ^a   Kim, Seung U ^c,d   Barish, Michael E ^b   Aboody, Karen S ^a,b   Glackin, Carlotta A ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b Department of Hematology/Hematopoietic Cell Transplantation City of Hope ^*  (United States)

^c Ajou University School of Medicine   (South Korea)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

c Met; Cell migration; Glioma; Hepatocyte growth factor; Neural stem cells; Ras phosphoinositide 3 kinase signaling; Tumor targeting

Indexed keywords

EPIDERMAL GROWTH FACTOR; GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; RAS PROTEIN; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SHORT HAIRPIN RNA; TRANSFORMING GROWTH FACTOR ALPHA; VASCULOTROPIN; RAC1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; CYTOSKELETON; ENZYME INHIBITION; FEMALE; GLIOMA; HUMAN; HUMAN CELL; MOUSE; NEURAL STEM CELL; NONHUMAN; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR GROWTH; BRAIN TUMOR; CELL LINE; CELL MOTION; ENZYMOLOGY; KIDNEY; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY; STEM CELL; TUMOR CELL LINE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; BRAIN NEOPLASMS; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOTAXIS; GLIOMA; HUMANS; KIDNEY; NEURONS; RAC1 GTP-BINDING PROTEIN; STEM CELLS;

EID: 48649096658     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2007-0887     Document Type: Article

References (62)

1. Flax JD, Aurora S, Yang C et al. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol 1998;16:1033-1039.
2. Fricker RA, Carpenter MK, Winkler C et al. Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J Neurosci 1999;19:5990-6005.
3. Kim SU, Park IH, Kim TH et al. Brain transplantation of human neural stem cells transduced with tyrosine hydroxylase and GTP cyclohydrolase 1 provides functional improvement in animal models of Parkinson disease. Neuropathology 2006;26:129-140.
4. Bachoud-Lévi AC, Remy P, Nguyen JP et al. Motor and cognitive improvements in patients with Huntington's disease after neural transplantation. Lancet 2000;356:1975-1979.
5. Kim SU. Genetically engineered human neural stem cells for brain repair in neurological diseases. Brain Dev 2007;29:193-201.
6. Lee HJ, Kim KS, Park IH et al. Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS ONE 2007;2:e156.
7. Lee JP, Jeyakumar M, Gonzalez R et al. Stem cells act through multiple mechanisms to benefit mice with neurodegenerative metabolic disease. Nat Med 2007;13:439-447.
8. Kim SU. Human neural stem cells genetically modified for brain repair in neurological disorders. Neuropathology 2004;24:159-171.
9. Goldman S. Stem and progenitor cell-based therapy of the human central nervous system. Nat Biotechnol 2005;23:862-871.
10. Aboody KS, Brown A, Rainov NG et al. Neural stem cells display extensive tropism for pathology in adult brain: Evidence from intracranial gliomas. Proc Natl Acad Sci U S A 2000;97:12846-12851.
11. Brown AB, Yang W, Schmidt NO et al. Intravascular delivery of neural stem cell lines to target intracranial and extracranial tumors of neural and non-neural origin. Hum Gene Ther 2003;14:1777-1785.
12. Benedetti S, Pirola B, Pollo B et al. Gene therapy of experimental brain tumors using neural progenitor cells. Nat Med 2000;6:447-450.
13. Najbauer J, Danks MK, Schmidt NO et al. Neural stem cell-mediated therapy of primary and metastatic solid tumors. In: Bertolotti R, Ozawa K, eds. Progress in Gene Therapy, Autologous and Cancer Stem Cell Gene Therapy. Vol 3. Singapore: World Scientific, 2007;335-372.
14. Lin D, Najbauer J, Salvaterra PM et al. Novel method for visualizing and modeling the spatial distribution of neural stem cells within intracranial glioma. Neuroimage 2007;37(suppl 1):S18-S26.
15. Terzis AJ, Niclou SP, Rajcevic U et al. Cell therapies for glioblastoma. Expert Opin Biol Ther 2006;6:739-749.
16. Aboody KS, Bush RA, Garcia E et al. Development of a tumor-selective approach to treat metastatic cancer. PLoS ONE 2006;1:e23.
17. Aboody KS, Najbauer J, Schmidt NO et al. Targeting of melanoma brain metastases using engineered neural stem/progenitor cells. Neuro Oncol 2006;8:119-126.
18. Danks MK, Yoon KJ, Bush RA et al. Tumor-targeted enzyme/prodrug therapy mediates long-term disease-free survival of mice bearing disseminated neuroblastoma. Cancer Res 2007;67:22-25.
19. Shimato S, Natsume A, Takeuchi H et al. Human neural stem cells target and deliver therapeutic gene to experimental leptomeningeal medulloblastoma. Gene Ther 2007;14:1132-1142.
20. Kim SK, Kim SU, Park IH et al. Human neural stem cells target experimental intracranial medulloblastoma and deliver a therapeutic gene leading to tumor regression. Clin Cancer Res 2006;12:5550-5556.
21. Jeong SW, Chu K, Jung KH et al. Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke 2003;34:2258-2263.
22. Kim TE, Park MJ, Choi EJ et al. Cloning and cell type-specific regulation of the human tyrosine hydroxylase gene promoter. Biochem Biophys Res Commun 2003;312:1123-1131.
23. Kim SK, Cargioli TG, Machluf M et al. PEX-producing human neural stem cells inhibit tumor growth in a mouse glioma model. Clin Cancer Res 2005;11:5965-5970.
24. Dao MA, Creer MH, Nolta JA et al. Biology of umbilical cord blood progenitors in bone marrow niches. Blood 2007;110:74-81.
25. Kucia M, Reca R, Miekus K et al. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: Pivotal role of the SDF-1-CXCR4 axis. STEM CELLS 2005;23:879-894.
26. Erlandsson A, Larsson J, Forsberg-Nilsson K. Stem cell factor is a chemoattractant and a survival factor for CNS stem cells. Exp Cell Res 2004;301:201-210.
27. Widera D, Holtkamp W, Entschladen F et al. MCP-1 induces migration of adult neural stem cells. Eur J Cell Biol 2004;83:381-387.
28. Imitola J, Raddassi K, Park KI et al. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A 2004;101:18117-18122.
29. Sun L, Lee J, Fine HA. Neuronally expressed stem cell factor induces neural stem cell migration to areas of brain injury. J Clin Invest 2004;113:1364-1374.
30. Heese O, Disko A, Zirkel D et al. Neural stem cell migration toward gliomas in vitro. Neuro Oncol 2005;7:476-484.
31. Schmidt NO, Przylecki W, Yang W et al. Brain tumor tropism of transplanted human neural stem cells is induced by vascular endothelial growth factor. Neoplasia 2005;7:623-629.
32. Dunn IF, Heese O, Black PM. Growth factors in glioma angiogenesis: FGFs, PDGF, EGF, and Tgfs. J Neurooncol 2000;50:121-137.
33. Chicoine MR, Silbergeld DL. Mitogens as motogens. J Neurooncol 1997;35:249-257.
34. Boockvar JA, Kapitonov D, Kapoor G et al. Constitutive EGFR signaling confers a motile phenotype to neural stem cells. Mol Cell Neurosci 2003;24:1116-1130.
35. Ziu M, Schmidt NO, Cargioli TG et al. Glioma-produced extracellular matrix influences brain tumor tropism of human neural stem cells. J Neurooncol 2006;79:125-133.
36. Leslie NR, Yang X, Downes CP et al. The regulation of cell migration by PTEN. Biochem Soc Trans 2005;33:1507-1508.
37. Forte G, Minieri M, Cossa P et al. Hepatocyte growth factor effects on mesenchymal stem cells: Proliferation, migration, and differentiation. STEM CELLS 2006;24:23-33.
38. Glaser T, Brose C, Franceschini I et al. Neural cell adhesion molecule polysialylation enhances the sensitivity of embryonic stem cell-derived neural precursors to migration guidance cues. STEM CELLS 2007;25:3016-3025.
39. Zheng H, Fu G, Dai T et al. Migration of endothelial progenitor cells mediated by stromal cell-derived factor-1alpha/CXCR4 via PI3K/Akt/eNOS signal transduction pathway. J Cardiovasc Pharmacol 2007;50:274-280.
40. Kendall SE, Battelli C, Irwin S et al. NRAGE mediates p38 activation and neural progenitor apoptosis via the bone morphogenetic protein signaling cascade. Mol Cell Biol 2005;25:7711-7724.
41. Boccaccio C, Comoglio PM. Invasive growth: A MET-driven genetic programme for cancer and stem cells. Nat Rev Cancer 2006;6:637-645.
42. Chan TO, Rodeck U, Chan AM et al. Small GTPases and tyrosine kinases coregulate a molecular switch in the phosphoinositide 3-kinase regulatory subunit. Cancer Cell 2002;1:181-191.
43. Sun W, Funakoshi H, Nakamura T. Localization and functional role of hepatocyte growth factor (HGF) and its receptor c-met in the rat developing cerebral cortex. Brain Res Mol Brain Res 2002;103:36-48.
44. Moumen A, Patane S, Porras A et al. Met acts on Mdm2 via mTOR to signal cell survival during development. Development 2007;134:1443-1451.
45. Martins GJ, Plachez C, Powell EM. Loss of embryonic MET signaling alters profiles of hippocampal interneurons. Dev Neurosci 2007;29:143-158.
46. Birchmeier C, Birchmeier W, Gherardi E et al. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003;4:915-925.
47. Lesko E, Majka M. The biological role of HGF-MET axis in tumor growth and development of metastasis. Front Biosci 2008;13:1271-1280.
48. Lengyel E, Sawada K, Salgia R. Tyrosine kinase mutations in human cancer. Curr Mol Med 2007;7:77-84.
49. Eckerich C, Zapf S, Fillbrandt R et al. Hypoxia can induce c-Met expression in glioma cells and enhance SF/HGF-induced cell migration. Int J Cancer 2007;121:276-283.
50. Desiderio MA. Hepatocyte growth factor in invasive growth of carcinomas. Cell Mol Life Sci 2007;64:1341-1354.
51. Abounader R, Laterra J. Scatter factor/hepatocyte growth factor in brain tumor growth and angiogenesis. Neuro-oncol 2005;7:436-451.
52. Lengyel E, Prechtel D, Resau JH et al. C-Met overexpression in node-positive breast cancer identifies patients with poor clinical outcome independent of Her2/neu. Int J Cancer 2005;113:678-682.
53. Cacci E, Salani M, Anastasi S et al. Hepatocyte growth factor stimulates cell motility in cultures of the striatal progenitor cells ST14A. J Neurosci Res 2003;74:760-768.
54. Bolanos-Garcia VM. MET meet adaptors: Functional and structural implications in downstream signalling mediated by the Met receptor. Mol Cell Biochem 2005;276:149-157.
55. Potempa S, Ridley AJ. Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/scatter factor-induced adherens junction disassembly. Mol Biol Cell 1998;9:2185-2200.
56. Cully M, You H, Levine AJ et al. Beyond PTEN mutations: The PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat Rev Cancer 2006;6:184-192.
57. Royal I, Lamarche-Vane N, Lamorte L et al. Activation of cdc42, rac, PAK, and rho-kinase in response to hepatocyte growth factor differentially regulates epithelial cell colony spreading and dissociation. Mol Biol Cell 2000;11:1709-1725.
58. Merlot S, Firtel RA. Leading the way: Directional sensing through phosphatidylinositol 3-kinase and other signaling pathways. J Cell Sci 2003;116:3471-3478.
59. Ward SG. Do phosphoinositide 3-kinases direct lymphocyte navigation? Trends Immunol 2004;25:67-74.
60. Tunici P, Bissola L, Lualdi E et al. Genetic alterations and in vivo tumorigenicity of neurospheres derived from an adult glioblastoma. Mol Cancer 2004;3:25.
61. Furukawa K, Kumon Y, Harada H et al. PTEN gene transfer suppresses the invasive potential of human malignant gliomas by regulating cell invasion-related molecules. Int J Oncol 2006;29:73-81.
62. Furnari FB, Fenton T, Bachoo RM et al. Malignant astrocytic glioma: Genetics, biology, and paths to treatment. Genes Dev 2007;21:2683-2710.