Stromal heparan sulfate differentiates neuroblasts to suppress neuroblastoma growth

Journal of Clinical Investigation

Volumn 124, Issue 7, 2014, Pages 3016-3031

  Knelson, Erik H ^a   Gaviglio, Angela L ^a   Nee, Jasmine C ^a   Starr, Mark D ^a   Nixon, Andrew B ^a   Marcus, Stephen G ^b   Blobe, Gerard C ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b Cantex Pharmaceuticals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; PROTEOHEPARAN SULFATE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3;

ARTICLE; CANCER INHIBITION; CANCER PROGNOSIS; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN TISSUE; NEUROBLAST; NEUROBLASTOMA; NEUROBLASTOMA CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL; SULFATION;

ANIMALS; ANTINEOPLASTIC AGENTS; BINDING SITES; CELL DIFFERENTIATION; CELL LINE, TUMOR; FEMALE; FIBROBLAST GROWTH FACTOR 2; HEPARAN SULFATE PROTEOGLYCANS; HEPARIN; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; MICE; MICE, SCID; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEOPLASTIC STEM CELLS; NEUROBLASTOMA; PROGNOSIS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SIGNAL TRANSDUCTION; STROMAL CELLS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901206089     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI74270     Document Type: Article

References (80)

1. National Cancer Institute. Surveillance, Epidemiology and End Results Program. NIH Web site. http://seer.cancer.gov/. Accessed May 13, 2014.
2. Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet. 2007;369(9579):2106-2120.
3. Matthay KK, Atkinson JB, Stram DO, Selch M, Reynolds CP, Seeger RC. Patterns of relapse after autologous purged bone marrow transplantation for neuroblastoma: a Childrens Cancer Group pilot study. J Clin Oncol. 1993;11(11):2226-2233.
4. Shimada H, Ambros IM, Dehner LP, Hata J, Joshi VV, Roald B. Terminology and morphologic criteria of neuroblastic tumors: recommendations by the International Neuroblastoma Pathology Committee. Cancer. 1999;86(2):349-363.
5. Kwiatkowski JL, Rutkowski JL, Yamashiro DJ, Tennekoon GI, Brodeur GM. Schwann cell-conditioned medium promotes neuroblastoma survival and differentiation. Cancer research. 1998;58(20):4602-4606.
6. Liu S, Tian Y, Chlenski A, Yang Q, Salwen HR, Cohn SL. ?Cross-talk? between Schwannian stroma and neuroblasts promotes neuroblastoma tumor differentiation and inhibits angiogenesis. Cancer Lett. 2005;228(1-2):125-131.
7. Matthay KK, et al. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children?s Cancer Group. N Engl J Med. 1999;341(16):1165-1173.
8. Matthay KK, et al. Long-term results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13-cis-retinoic acid: a children?s oncology group study. J Clin Oncol. 2009;27(7):1007-1013.
9. Brodeur GM. Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer. 2003;3(3):203-216.
10. Edsjo A, Holmquist L, Pahlman S. Neuroblastoma as an experimental model for neuronal differentiation and hypoxia-induced tumor cell dedifferentiation. Semin Cancer Biol. 2007;17(3):248-256.
11. Maris JM. Recent advances in neuroblastoma. N Engl J Med. 2010;362(23):2202-2211.
12. Knelson EH, Gaviglio AL, Tewari AK, Armstrong MB, Mythreye K, Blobe GC. Type III TGF-βreceptor promotes FGF2-mediated neuronal differentiation in neuroblastoma. J Clin Invest. 2013; 123(11):4786-4798.
13. Chernousov MA, Carey DJ. N-syndecan (syndecan 3) from neonatal rat brain binds basic fibroblast growth factor. J Biol Chem. 1993;268(22):16810-16814.
14. Carey DJ. N-syndecan: structure and function of a transmembrane heparan sulfate proteoglycan. Perspect Dev Neurobiol. 1996;3(4):331-346.
15. Hienola A, Tumova S, Kulesskiy E, Rauvala H. N-syndecan deficiency impairs neural migration in brain. J Cell Biol. 2006;174(4):569-580.
16. Kinnunen T, Kaksonen M, Saarinen J, Kalkkinen N, Peng HB, Rauvala H. Cortactin-Src kinase signaling pathway is involved in N-syndecandependent neurite outgrowth. J Biol Chem. 1998; 273(17):10702-10708.
17. Akita K, et al. Heparan sulphate proteoglycans interact with neurocan and promote neurite outgrowth from cerebellar granule cells. Biochem J. 2004;383(Pt 1):129-138.
18. Rapraeger AC, Krufka A, Olwin BB. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science. 1991; 252(5013):1705-1708.
19. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 1991;64(4):841-848.
20. Lundin L, et al. Selectively desulfated heparin inhibits fibroblast growth factor-induced mitogenicity and angiogenesis. J Biol Chem. 2000;275(32):24653-24660.
21. Takeuchi A, et al. Low molecular weight heparin suppresses receptor for advanced glycation end products-mediated expression of malignant phenotype in human fibrosarcoma cells. Cancer Sci. 2013;104(6):740-749.
22. Bendas G, Borsig L. Cancer cell adhesion and metastasis: selectins, integrins, and the inhibitory potential of heparins. Int J Cell Biol. 2012;2012:676731.
23. Battinelli EM, et al. Anticoagulation inhibits tumor cell mediated release of platelet angiogenic proteins and diminishes platelet angiogenic response. Blood. 2014;123(1):101-112.
24. Ostrovsky O, et al. Differential effects of heparin saccharides on the formation of specific fibroblast growth factor (FGF) and FGF receptor complexes. J Biol Chem. 2002;277(4):2444-2453.
25. Whitelock JM, Iozzo RV. Heparan sulfate: a complex polymer charged with biological activity. Chem Rev. 2005;105(7):2745-2764.
26. Spivak-Kroizman T, et al. Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell. 1994;79(6):1015-1024.
27. Ornitz DM, Yayon A, Flanagan JG, Svahn CM, Levi E, Leder P. Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol Cell Biol. 1992;12(1):240-247.
28. Iolascon A, et al. Reduced expression of transforming growth factor-&receptor type III in high stage neuroblastomas.?beta; Br J Cancer. 2000;82(6):1171-1176.
29. Takita J, et al. Gene expression profiling and identification of novel prognostic marker genes in neuroblastoma. Genes Chromosomes Cancer. 2004;40(2):120-132.
30. De Preter K, et al. Human fetal neuroblast and neuroblastoma transcriptome analysis confirms neuroblast origin and highlights neuroblastoma candidate genes. Genome Biol. 2006;7(9):R84.
31. Albino D, et al. Identification of low intratumoral gene expression heterogeneity in neuroblastic tumors by genome-wide expression analysis and game theory. Cancer. 2008;113(6):1412-1422.
32. Acosta S, et al. Identification of tumoral glial precursor cells in neuroblastoma. Cancer Lett. 2011; 312(1):73-81.
33. Ross RA, Biedler JL, Spengler BA. A role for distinct cell types in determining malignancy in human neuroblastoma cell lines and tumors. Cancer Lett. 2003;197(1-2):35-39.
34. Oberthuer A, et al. Customized oligonucleotide microarray gene expression-based classification of neuroblastoma patients outperforms current clinical risk stratification. J Clin Oncol. 2006; 24(31):5070-5078.
35. Wei JS, et al. Prediction of clinical outcome using gene expression profiling and artificial neural networks for patients with neuroblastoma. Cancer Res. 2004;64(19):6883-6891.
36. Pahlman S, Ruusala AI, Abrahamsson L, Mattsson ME, Esscher T. Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation. Cell Differ. 1984;14(2):135-144.
37. Kaneko M, Yang W, Matsumoto Y, Watt F, Funa K. Activity of a novel PDGF beta-receptor enhancer during the cell cycle and upon differentiation of neuroblastoma. Exp Cell Res. 2006;312(11):2028-2039.
38. Scarpa S, et al. Transforming growth factor beta regulates differentiation and proliferation of human neuroblastoma. Exp Cell Res. 1996;229(1):147-154.
39. Encinas M, et al. Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuronlike cells. J Neurochem. 2000;75(3):991-1003.
40. Hahn CK, et al. Expression-based screening identifies the combination of histone deacetylase inhibitors and retinoids for neuroblastoma differentiation. Proc Natl Acad Sci U S A. 2008;105(28):9751-9756.
41. Leli U, Cataldo A, Shea TB, Nixon RA, Hauser G. Distinct mechanisms of differentiation of SH-SY5Y neuroblastoma cells by protein kinase C activators and inhibitors. J Neurochem. 1992;58(4):1191-1198.
42. Voigt A, Hartmann P, Zintl F. Differentiation, proliferation and adhesion of human neuroblastoma cells after treatment with retinoic acid. Cell Adhes Commun. 2000;7(5):423-440.
43. Kelsh RN. Sorting out Sox10 functions in neural crest development. Bioessays. 2006;28(8):788-798.
44. Gershon TR, Oppenheimer O, Chin SS, Gerald WL. Temporally regulated neural crest transcription factors distinguish neuroectodermal tumors of varying malignancy and differentiation. Neoplasia. 2005; 7(6):575-584.
45. Mythreye K, Blobe GC. Proteoglycan signaling co-receptors: roles in cell adhesion, migration and invasion. Cell Signal. 2009;21(11):1548-1558.
46. Blair CR, Stone JB, Wells RG. The type III TGFbeta receptor betaglycan transmembrane-cytoplasmic domain fragment is stable after ectodomain cleavage and is a substrate of the intramembrane protease gamma-secretase. Biochim Biophys Acta. 2011;1813(2):332-339.
47. Kirkbride KC, Townsend TA, Bruinsma MW, Barnett JV, Blobe GC. Bone morphogenetic proteins signal through the transforming growth factor-&type III receptor.?beta; J Biol Chem. 2008;283(12):7628-7637.
48. Guillemot F, Zimmer C. From cradle to grave: the multiple roles of fibroblast growth factors in neural development. Neuron. 2011;71(4):574-588.
49. Lavenius E, Parrow V, Nanberg E, Pahlman S. Basic FGF and IGF-I promote differentiation of human SH-SY5Y neuroblastoma cells in culture. Growth Factors. 1994;10(1):29-39.
50. Singh A, et al. Retinoic acid induces REST degradation and neuronal differentiation by modulating the expression of SCF(β-TRCP) in neuroblastoma cells. Cancer. 2011;117(22):5189-5202.
51. Thiele C. Neuroblastoma cell lines. In: Masters J, ed. Human Cell Culture. Lancaster, United Kingdom: Kluwer Academic Publishers; 1998:21-53.
52. Rao NV, et al. Low anticoagulant heparin targets multiple sites of inflammation, suppresses heparin-induced thrombocytopenia, and inhibits interaction of RAGE with its ligands. Am J Physiol Cell Physiol. 2010;299(1):C97-C110.
53. Villablanca JG, et al. Phase II study of oral capsular 4-hydroxyphenylretinamide (4-HPR/fenretinide) in pediatric patients with refractory or recurrent neuroblastoma: a report from the Children?s Oncology Group. Clin Cancer Res. 2011;17(21):6858-6866.
54. Karmakar S, Choudhury SR, Banik NL, Ray SK. Combination of N-(4-hydroxyphenyl) retinamide and genistein increased apoptosis in neuroblastoma SK-N-BE2 and SH-SY5Y xenografts. Neuroscience. 2009;163(1):286-295.
55. Sidell N. Retinoic acid-induced growth inhibition and morphologic differentiation of human neuroblastoma cells in vitro. J Natl Cancer Inst. 1982; 68(4):589-596.
56. Gilbert SF. The neural crest. In: Developmental Biology. Sunderland, Massachusetts, USA: Sinauer Associates; 2000.
57. Huang D, et al. Schwann cell-conditioned medium inhibits angiogenesis. Cancer Res. 2000; 60(21):5966-5971.
58. Huang D, et al. Schwann cell-conditioned medium inhibits angiogenesis in vitro and in vivo. Med Pediatr Oncol. 2000;35(6):590-592.
59. Chlenski A, et al. SPARC is a key Schwannian-derived inhibitor controlling neuroblastoma tumor angiogenesis. Cancer Res. 2002;62(24):7357-7363.
60. Crawford SE, et al. Pigment epithelium-derived factor (PEDF) in neuroblastoma: a multifunctional mediator of Schwann cell antitumor activity. J Cell Sci. 2001;114(pt 24):4421-4428.
61. Kim MS, et al. Fibroblast growth factor 2 induces differentiation and apoptosis of Askin tumour cells. J Pathol. 2004;202(1):103-112.
62. Higgins S, et al. Fibroblast growth factor 2 reactivates G1 checkpoint in SK-N-MC cells via regulation of p21, inhibitor of differentiation genes (Id1-3), and epithelium-mesenchyme transition-like events. Endocrinology. 2009;150(9):4044-4055.
63. Passiatore G, Gentilella A, Rom S, Pacifici M, Bergonzini V, Peruzzi F. Induction of Id-1 by FGF-2 involves activity of EGR-1 and sensitizes neuroblastoma cells to cell death. J Cell Physiol. 2011; 226(7):1763-1770.
64. Wang X, et al. Essential role of ERK activation in neurite outgrowth induced by alpha-lipoic acid. Biochim Biophys Acta. 2011;1813(5):827-838.
65. Qiao J, et al. PI3K/AKT and ERK regulate retinoic acid-induced neuroblastoma cellular differentiation. Biochem Biophys Res Commun. 2012;424(3):421-426.
66. Wang L, Brown JR, Varki A, Esko JD. Heparin?s anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of Land P-selectins. J Clin Invest. 2002;110(1):127-136.
67. Myint KM, et al. RAGE control of diabetic nephropathy in a mouse model: effects of RAGE gene disruption and administration of low-molecular weight heparin. Diabetes. 2006;55(9):2510-2522.
68. Asgharzadeh S, et al. Prognostic significance of gene expression profiles of metastatic neuroblastomas lacking MYCN gene amplification. J Natl Cancer Inst. 2006;98(17):1193-1203.
69. Dong M, et al. The type III TGF-beta receptor suppresses breast cancer progression. J Clin Invest. 2007; 117(1):206-217.
70. Mythreye K, Knelson EH, Gatza CE, Gatza Ml, Blobe GC. TβRIII/β-arrestin2 regulates integrin α5β1 trafficking, function, and localization in epithelial cells. Oncogene. 2013;32(11):1416-1427.
71. Robertson D, Savage K, Reis-Filho JS, Isacke CM. Multiple immunofluorescence labelling of formalin-fixed paraffin-embedded (FFPE) tissue. BMC Cell Biol. 2008;9:13.
72. Finger EC, Turley RS, Dong M, How T, Fields TA, Blobe GC. TβRIII suppresses non-small cell lung cancer invasiveness and tumorigenicity. Carcinogenesis. 2008;29(3):528-535.
73. Hanks BA, et al. Type III TGF-αreceptorβ downregulation generates an immunotolerant tumor microenvironment. J Clin Invest. 2013;123(9):3925-3940.
74. Zittermann SI, Capurro MI, Shi W, Filmus J. Soluble glypican 3 inhibits the growth of hepatocellular carcinoma in vitro and in vivo. Int J Cancer. 2010; 126(6):1291-1301.
75. Boehm JS, et al. Integrative genomic approaches identify IKBKE as a breast cancer oncogene. Cell. 2007;129(6):1065-1079.
76. Sato A, et al. FGF8 signaling is chemotactic for cardiac neural crest cells. Dev Biol. 2011;354(1):18-30.
77. Qiao D, Yang X, Meyer K, Friedl A. Glypican-1 regulates anaphase promoting complex/cyclosome substrates and cell cycle progression in endothelial cells. Mol Biol Cell. 2008;19(7):2789-2801.
78. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M. Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A. 2004;58(2):167-176.
79. Eyler CE, et al. Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2. Cell. 2011;146(1):53-66.
80. Tuominen VJ, Ruotoistenmaki S, Viitanen A, Jumppanen M, Isola J. ImmunoRatio: a publicly available web application for quantitative image analysis of estrogen receptor (ER), progesterone receptor (PR), and Ki-67. Breast Cancer Res. 2010;12(4):R56.