The role of basic fibroblast growth factor in glioblastoma multiforme and glioblastoma stem cells and in their in vitro culture

Cancer Letters

Volumn 346, Issue 1, 2014, Pages 1-5

  Haley, Elizabeth M ^a   Kim, Yonghyun ^a  

^a University of Alabama   (United States)

Author keywords

Basic fibroblast growth factor (FGF 2); Cancer stem cells; Cell culture; Glioblastoma multiforme (GBM); Glioblastoma stem cells; Synthetic analogs

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; ISOPROTEIN;

CANCER CELL CULTURE; CANCER GROWTH; CANCER STEM CELL; CANCER SURVIVAL; CELL PROLIFERATION; CODON; COMPARATIVE STUDY; CULTURE MEDIUM; GLIOBLASTOMA; HUMAN; IN VITRO STUDY; INTRACELLULAR SIGNALING; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SHORT SURVEY; TUMOR VASCULARIZATION;

BASIC FIBROBLAST GROWTH FACTOR (FGF-2); CANCER STEM CELLS; CELL CULTURE; GLIOBLASTOMA MULTIFORME (GBM); GLIOBLASTOMA STEM CELLS; SYNTHETIC ANALOGS;

BRAIN NEOPLASMS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CULTURE MEDIA; FIBROBLAST GROWTH FACTOR 2; GLIOBLASTOMA; HUMANS; NEOPLASTIC STEM CELLS;

EID: 84896702422     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.12.003     Document Type: Review

References (74)

1. Darefsky A.S., King J.T., Dubrow R. Adult glioblastoma multiforme survival in the temozolomide era: a population-based analysis of Surveillance, Epidemiology, and End Results registries. Cancer 2012, 118:2163-2172.
2. Juratli T.A., Schackert G., Krex D. Current status of local therapy in malignant gliomas - a clinical review of three selected approaches. Pharmacol. Therapeut. 2013, 139:341-358.
3. Schoenhals M., Kassambara A., De Vos J., Hose D., Moreaux J., Klein B. Embryonic stem cell markers expression in cancers. Biochem. Biophys. Res. Commun. 2009, 383:157-162.
4. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
5. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3:730-737.
6. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100:3983-3988.
7. Hermann P.C., Huber S.L., Herrler T., Aicher A., Ellwart J.W., Guba M., Bruns C.J., Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1:313-323.
8. Li C., Heidt D.G., Dalerba P., Burant C.F., Zhang L., Adsay V., Wicha M., Clarke M.F., Simeone D.M. Identification of pancreatic cancer stem cells. Cancer Res. 2007, 67:1030-1037.
9. O'Brien C.A., Pollett A., Gallinger S., Dick J.E. A human colon cancer cell capable of initiating tumour growth in immuno deficient mice. Nature 2007, 445:106-110.
10. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., Biffoni M., Todaro M., Peschle C., De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445:111-115.
11. Singh S.K., Clarke I.D., Terasaki M., Bonn V.E., Hawkins C., Squire J., Dirks P.B. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003, 63:5821-5828.
12. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
13. Galli R., Binda E., Orfanelli U., Cipelletti B., Gritti A., De Vitis S., Fiocco R., Foroni C., Dimeco F., Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004, 64:7011-7021.
14. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
15. Joo K.M., Jin J., Kim E., Ho Kim K., Kim Y., Gu Kang B., Kang Y.J., Lathia J.D., Cheong K.H., Song P.H., Kim H., Seol H.J., Kong D.S., Lee J.I., Rich J.N., Lee J., Nam D.H. MET signaling regulates glioblastoma stem cells. Cancer Res. 2012, 72:3828-3838.
16. Hardee M.E., Marciscano A.E., Medina-Ramirez C.M., Zagzag D., Narayana A., Lonning S.M., Barcellos-Hoff M.H. Resistance of glioblastoma-initiating cells to radiation mediated by the tumor microenvironment can be abolished by inhibiting transforming growth factor-beta. Cancer Res. 2012, 72:4119-4129.
17. Kim Y., Joo K.M., Jin J., Nam D.H. Cancer stem cells and their mechanism of chemo-radiation resistance. Int. J. Stem Cells 2009, 2:109-114.
18. Wang J., Wang C., Meng Q., Li S., Sun X., Bo Y., Yao W. SiRNA targeting Notch-1 decreases glioma stem cell proliferation and tumor growth. Mol. Biol. Rep. 2012, 39:2497-2503.
19. Sauvageot C.M., Weatherbee J.L., Kesari S., Winters S.E., Barnes J., Dellagatta J., Ramakrishna N.R., Stiles C.D., Kung A.L., Kieran M.W., Wen P.Y. Efficacy of the HSP90 inhibitor 17-AAG in human glioma cell lines and tumorigenic glioma stem cells. Neuro-oncol. 2009, 11:109-121.
20. Kim Y., Kim K.H., Lee J., Lee Y.A., Kim M., Lee S.J., Park K., Yang H., Jin J., Joo K.M., Nam D.H. Wnt activation is implicated in glioblastoma radioresistance. Laboratory Invest.; A J. Techn. Meth. Pathol. 2012, 92:466-473.
21. Heimberger A.B., Suki D., Yang D., Shi W., Aldape K. The natural history of EGFR and EGFRvIII in glioblastoma patients. J. Transl. Med. 2005, 3:38.
22. Hatanpaa K.J., Burma S., Zhao D., Habib A.A. Epidermal growth factor receptor in glioma: signal transduction, neuropathology, imaging, and radioresistance. Neoplasia 2010, 12:675-684.
23. The Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways, Nature, vol. 455, 2008, pp. 1061-1068.
24. Loilome W., Joshi A.D., ap Rhys C.M., Piccirillo S., Vescovi A.L., Gallia G.L., Riggins G.J. Glioblastoma cell growth is suppressed by disruption of Fibroblast Growth Factor pathway signaling. J. Neuro-oncol. 2009, 94:359-366.
25. Feng X., Zhang B., Wang J., Xu X., Lin N., Liu H. Adenovirus-mediated transfer of siRNA against basic fibroblast growth factor mRNA enhances the sensitivity of glioblastoma cells to chemotherapy. Med. Oncol. 2011, 28:24-30.
26. Lee J., Kotliarova S., Kotliarov Y., Li A., Su Q., Donin N.M., Pastorino S., Purow B.W., Christopher N., Zhang W., Park J.K., Fine H.A. 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.
27. Itoh N., Ornitz D.M. Evolution of the Fgf and Fgfr gene families. Trends Gen.: TIG 2004, 20:563-569.
28. Sorensen V., Nilsen T., Wiedlocha A. Functional diversity of FGF-2 isoforms by intracellular sorting. BioEssays: News Rev. Mol., Cell. Develop. Biol. 2006, 28:504-514.
29. Powers C.J., McLeskey S.W., Wellstein A. Fibroblast growth factors, their receptors and signaling. Endocrine-related Cancer 2000, 7:165-197.
30. Joy A., Moffett J., Neary K., Mordechai E., Stachowiak E.K., Coons S., Rankin-Shapiro J., Florkiewicz R.Z., Stachowiak M.K. Nuclear accumulation of FGF-2 is associated with proliferation of human astrocytes and glioma cells. Oncogene 1997, 14:171-183.
31. Bossard C., Laurell H., Van Den Berghe L., Meunier S., Zanibellato C., Prats H. Translokin is an intracellular mediator of FGF-2 trafficking. Nature Cell Biol. 2003, 5:433-439.
32. Dvorak P., Dvorakova D., Hampl A. Fibroblast growth factor signaling in embryonic and cancer stem cells. FEBS Lett. 2006, 580:2869-2874.
33. Schlessinger J. Common and distinct elements in cellular signaling via EGF and FGF receptors. Science 2004, 306:1506-1507.
34. Krufka A., Guimond S., Rapraeger A.C. Two hierarchies of FGF-2 signaling in heparin: mitogenic stimulation and high-affinity binding/receptor transphosphorylation. Biochemistry 1996, 35:11131-11141.
35. Okano J., Shiota G., Matsumoto K., Yasui S., Kurimasa A., Hisatome I., Steinberg P., Murawaki Y. Hepatocyte growth factor exerts a proliferative effect on oval cells through the PI3K/AKT signaling pathway. Biochem. Biophys. Res. Commun. 2003, 309:298-304.
36. Shiojima I., Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circul. Res. 2002, 90:1243-1250.
37. Lamothe B., Yamada M., Schaeper U., Birchmeier W., Lax I., Schlessinger J. The docking protein Gab1 is an essential component of an indirect mechanism for fibroblast growth factor stimulation of the phosphatidylinositol 3-kinase/Akt antiapoptotic pathway. Mol. Cell. Biol. 2004, 24:5657-5666.
38. Fuks Z., Persaud R.S., Alfieri A., McLoughlin M., Ehleiter D., Schwartz J.L., Seddon A.P., Cordon-Cardo C., Haimovitz-Friedman A. Basic fibroblast growth factor protects endothelial cells against radiation-induced programmed cell death in vitro and in vivo. Cancer Res. 1994, 54:2582-2590.
39. Zhang L., Sun W., Wang J., Zhang M., Yang S., Tian Y., Vidyasagar S., Pena L.A., Zhang K., Cao Y., Yin L., Wang W., Schaefer K.L., Saubermann L.J., Swarts S.G., Fenton B.M., Keng P.C., Okunieff P. Mitigation effect of an FGF-2 peptide on acute gastrointestinal syndrome after high-dose ionizing radiation. Int. J. Rad. Oncol., Biol., Phys. 2010, 77:261-268.
40. Marie M., Hafner S., Moratille S., Vaigot P., Mine S., Rigaud O., Martin M.T. FGF2 mediates DNA repair in epidermoid carcinoma cells exposed to ionizing radiation. Int. J. Radiat. Biol. 2012, 88:688-693.
41. Toyoda K., Tanaka K., Nakagawa S., Thuy D.H., Ujifuku K., Kamada K., Hayashi K., Matsuo T., Nagata I., Niwa M. Initial contact of glioblastoma cells with existing normal brain endothelial cells strengthen the barrier function via fibroblast growth factor 2 secretion: a new in vitro blood-brain barrier model. Cell. Mol. Neurobiol. 2013, 33:489-501.
42. Cuevas P., Carceller F., Angulo J., Gonzalez-Corrochano R., Cuevas-Bourdier A., Gimenez-Gallego G. Antiglioma effects of a new, low molecular mass, inhibitor of fibroblast growth factor. Neurosci. Lett. 2011, 491:1-7.
43. Auguste P., Gursel D.B., Lemiere S., Reimers D., Cuevas P., Carceller F., Di Santo J.P., Bikfalvi A. Inhibition of fibroblast growth factor/fibroblast growth factor receptor activity in glioma cells impedes tumor growth by both angiogenesis-dependent and -independent mechanisms. Cancer Res. 2001, 61:1717-1726.
44. Fischer I., Gagner J.P., Law M., Newcomb E.W., Zagzag D. Angiogenesis in gliomas: biology and molecular pathophysiology. Brain Pathol. 2005, 15:297-310.
45. Presta M., Dell'Era P., Mitola S., Moroni E., Ronca R., Rusnati M. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 2005, 16:159-178.
46. Kargiotis O., Rao J.S., Kyritsis A.P. Mechanisms of angiogenesis in gliomas. J. Neuro-oncol. 2006, 78:281-293.
47. Wang P., Zhen H., Zhang J., Zhang W., Zhang R., Cheng X., Guo G., Mao X., Wang J., Zhang X. Survivin promotes glioma angiogenesis through vascular endothelial growth factor and basic fibroblast growth factor in vitro and in vivo. Molecular Carcinogen. 2012, 51:586-595.
48. Turner N., Grose R. Fibroblast growth factor signalling: from development to cancer. Nature Rev. Cancer 2010, 10:116-129.
49. Pollard S.M., Yoshikawa K., Clarke I.D., Danovi D., Stricker S., Russell R., Bayani J., Head R., Lee M., Bernstein M., Squire J.A., Smith A., Dirks P. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009, 4:568-580.
50. Chang K.W., Huang Y.L., Wong Z.R., Su P.H., Huang B.M., Ju T.K., Yang H.Y. Fibroblast growth factor-2 up-regulates the expression of nestin through the Ras-Raf-ERK-Sp1 signaling axis in C6 glioma cells. Biochem. Biophys. Res. Commun. 2013, 434:854-860.
51. Li G., Chen Z., Hu Y.D., Wei H., Li D., Ji H., Wang D.L. Autocrine factors sustain glioblastoma stem cell self-renewal. Oncol. Rep. 2009, 21:419-424.
52. Kondo T., Setoguchi T., Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc. Natl. Acad. Sci. USA 2004, 101:781-786.
53. Phillips H.S., Kharbanda S., Chen R., Forrest W.F., Soriano R.H., Wu T.D., Misra A., Nigro J.M., Colman H., Soroceanu L., Williams P.M., Modrusan Z., Feuerstein B.G., Aldape K. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006, 9:157-173.
54. Ignatova T.N., Kukekov V.G., Laywell E.D., Suslov O.N., Vrionis F.D., Steindler D.A. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 2002, 39:193-206.
55. Lathia J.D., Hitomi M., Gallagher J., Gadani S.P., Adkins J., Vasanji A., Liu L., Eyler C.E., Heddleston J.M., Wu Q., Minhas S., Soeda A., Hoeppner D.J., Ravin R., McKay R.D., McLendon R.E., Corbeil D., Chenn A., Hjelmeland A.B., Park D.M., Rich J.N. Distribution of CD133 reveals glioma stem cells self-renew through symmetric and asymmetric cell divisions. Cell Death Dis. 2011, 2:e200.
56. Bajetto A., Porcile C., Pattarozzi A., Scotti L., Aceto A., Daga A., Barbieri F., Florio T. Differential role of EGF and BFGF in human GBM-TIC proliferation: relationship to EGFR-tyrosine kinase inhibitor sensibility. J. Biol. Regul. Homeost. Agents 2013, 27:143-154.
57. Ader I., Muller C., Bonnet J., Favre G., Cohen-Jonathan E., Salles B., Toulas C. The radioprotective effect of the 24 kDa FGF-2 isoform in HeLa cells is related to an increased expression and activity of the DNA dependent protein kinase (DNA-PK) catalytic subunit. Oncogene 2002, 21:6471-6479.
58. Rachidi W., Harfourche G., Lemaitre G., Amiot F., Vaigot P., Martin M.T. Sensing radiosensitivity of human epidermal stem cells. Radiother. Oncol.: J. Eur. Soc. Therapeut. Radiol. Oncol. 2007, 83:267-276.
59. Harfouche G., Vaigot P., Rachidi W., Rigaud O., Moratille S., Marie M., Lemaitre G., Fortunel N.O., Martin M.T. Fibroblast growth factor type 2 signaling is critical for DNA repair in human keratinocyte stem cells. Stem Cells 2010, 28:1639-1648.
60. Cao B., Jia J., Ma L., Di L., Song G., Yuan Y., Ma B., Zhu Y., Yu J., Wang X., Zhou X., Lyerly H.K., Ren J. Recombinant human endostatin could eliminate the pro-angiogenesis priority of SP cells sorted from non-small cell lung cancer cells. Clin. Transl. Oncol.: Off. Publ. Fed. Spanish Oncol. Soc. Natl. Cancer Inst. Mexico 2012, 14:575-585.
61. Kelly J.J., Stechishin O., Chojnacki A., Lun X., Sun B., Senger D.L., Forsyth P., Auer R.N., Dunn J.F., Cairncross J.G., Parney I.F., Weiss S. Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells 2009, 27:1722-1733.
62. Kim J., Jung J., Lee S.J., Lee J.S., Park M.J. Cancer stem-like cells persist in established cell lines through autocrine activation of EGFR signaling. Oncology Lett. 2012, 3:607-612.
63. Ballinger M.D., Shyamala V., Forrest L.D., Deuter-Reinhard M., Doyle L.V., Wang J.X., Panganiban-Lustan L., Stratton J.R., Apell G., Winter J.A., Doyle M.V., Rosenberg S., Kavanaugh W.M. Semirational design of a potent, artificial agonist of fibroblast growth factor receptors. Nat. Biotechnol. 1999, 17:1199-1204.
64. L.A. Pena, P.O. Zamora, X. Lin, J.D. Glass, Synthetic Heparin-binding Factor Analogs, in: Biosurface Engineering Technologies, Inc.; Brookhaven Science Associates, US Patent 7,700,563 B2, 2010.
65. Lin X., Takahashi K., Campion S.L., Liu Y., Gustavsen G.G., Pena L.A., Zamora P.O. Synthetic peptide F2A4-K-NS mimics fibroblast growth factor-2 in vitro and is angiogenic in vivo. Int. J. Mol. Med. 2006, 17:833-839.
66. P. Okunieff, L. Zhang, Fibroblast Growth Factor (FGF) Analogs and Uses Thereof, in, US Patent 2011/0207663 A1, 2011.
67. Caldwell M.A., Garcion E., TerBorg M.G., He X., Svendsen C.N. Heparin stabilizes FGF-2 and modulates striatal precursor cell behavior in response to EGF. Exp. Neurol. 2004, 188:408-420.
68. Fox G.M., Schiffer S.G., Rohde M.F., Tsai L.B., Banks A.R., Arakawa T. Production, biological activity, and structure of recombinant basic fibroblast growth factor and an analog with cysteine replaced by serine. J. Biol. Chem. 1988, 263:18452-18458.
69. J.C. Fiddes, J.A. Abraham, A. Protter, Human basic fibroblast growth factor analog, in, US Patent No. 6,294,359, 2001.
70. Abraham J.A., Whang J.L., Tumolo A., Mergia A., Friedman J., Gospodarowicz D., Fiddes J.C. Human basic fibroblast growth factor: nucleotide sequence and genomic organization. EMBO J. 1986, 5:2523-2528.
71. M. Ballinger, M. Kavanaugh, Synthetic peptides having FGF receptor affinity, in, US Patent No. 6,548,634, 2003.
72. Cheng L., Huang Z., Zhou W., Wu Q., Donnola S., Liu J.K., Fang X., Sloan A.E., Mao Y., Lathia J.D., Min W., McLendon R.E., Rich J.N., Bao S. Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 2013, 153:139-152.
73. Chan X.H., Nama S., Gopal F., Rizk P., Ramasamy S., Sundaram G., Ow G.S., Ivshina A.V., Tanavde V., Haybaeck J., Kuznetsov V., Sampath P. Targeting glioma stem cells by functional inhibition of a prosurvival oncomiR-138 in malignant gliomas. Cell Rep. 2012, 2:591-602.
74. Wakimoto H., Mohapatra G., Kanai R., Curry W.T., Yip S., Nitta M., Patel A.P., Barnard Z.R., Stemmer-Rachamimov A.O., Louis D.N., Martuza R.L., Rabkin S.D. Maintenance of primary tumor phenotype and genotype in glioblastoma stem cells. Neuro-oncol. 2012, 14:132-144.