Neuroblastoma as an experimental model for neuronal differentiation and hypoxia-induced tumor cell dedifferentiation

Seminars in Cancer Biology

Volumn 17, Issue 3, 2007, Pages 248-256

  Edsjö, Anders ^a   Holmquist, Linda ^a   Påhlman, Sven ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Hypoxia; Neuroblastoma; Neuronal differentiation; Sympathetic nervous system

Indexed keywords

ADRENERGIC SYSTEM; BENIGN TUMOR; CANCER MODEL; CELL DIFFERENTIATION; CHILDHOOD CANCER; EXPERIMENTAL MODEL; HUMAN; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; MALIGNANT NEOPLASTIC DISEASE; NERVE CELL DIFFERENTIATION; NEUROBLASTOMA; NONHUMAN; PHENOTYPE; REVIEW; STEM CELL; TUMOR DIFFERENTIATION;

CELL DIFFERENTIATION; CELL HYPOXIA; HUMANS; NEUROBLASTOMA; NEURONS;

EID: 33947138135     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcancer.2006.04.005     Document Type: Review

References (66)

1. Brodeur G.M., Pritchard J., Berthold F., Carlsen N.L., Castel V., Castelberry R.P., et al. Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment. J Clin Oncol 11 (1993) 1466-1477
2. Hedborg F., Bjelfman C., Sparen P., Sandstedt B., and Påhlman S. Biochemical evidence for a mature phenotype in morphologically poorly differentiated neuroblastomas with a favorable outcome. Eur J Cancer 4 (1995) 435-443
3. Patterson P.H. Control of cell fate in a vertebrate neurogenic lineage. Cell 62 (1990) 1035-1038
4. Hoehner J.C., Gestblom C., Hedborg F., Sandstedt B., Olsen L., and Påhlman S. A developmental model of neuroblastoma: differentiating stroma-poor tumors' progress along an extra-adrenal chromaffin lineage. Lab Invest 75 (1996) 659-675
5. Gestblom C., Hoehner J.C., Hedborg F., Sandstedt B., and Påhlman S. In vivo spontaneous neuronal to neuroendocrine lineage conversion in a subset of neuroblastomas. Am J Pathol 150 (1997) 107-117
6. Påhlman S., Odelstad L., Larsson E., Grotte G., and Nilsson K. Phenotypic changes of human neuroblastoma cells in culture induced by 12-O-tetradecanoyl-phorbol-13-acetate. Int J Cancer 28 (1981) 583-589
7. Reynolds C.P., Matthay K.K., Villablanca J.G., and Maurer B.J. Retinoid therapy of high-risk neuroblastoma. Cancer Lett 197 (2003) 185-192
8. Rastinejad F. Retinoid X receptor and its partners in the nuclear receptor family. Curr Opin Struct Biol 11 (2001) 33-38
9. Sidell N. Retinoic acid-induced growth inhibition and morphologic differentiation of human neuroblastoma cells in vitro. J Natl Cancer Inst 68 (1982) 589-596
10. Påhlman S., Ruusala A.I., Abrahamsson L., Mattsson M.E., and Esscher T. Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation. Cell Differ 14 (1984) 135-144
11. Thiele C.J., Reynolds C.P., and Israel M.A. Decreased expression of N-myc precedes retinoic acid-induced morphological differentiation of human neuroblastoma. Nature 313 (1985) 404-406
12. Thiele C.J., Deutsch L.A., and Israel M.A. The expression of multiple proto-oncogenes is differentially regulated during retinoic acid induced maturation of human neuroblastoma cell lines. Oncogene 3 (1988) 281-288
13. Hill D.P., and Robertson K.A. Characterization of the cholinergic neuronal differentiation of the human neuroblastoma cell line LA-N-5 after treatment with retinoic acid. Brain Res Dev Brain Res 102 (1997) 53-67
14. Handler A., Lobo M.D., Alonso F.J., Paino C.L., and Mena M.A. Functional implications of the noradrenergic-cholinergic switch induced by retinoic acid in NB69 neuroblastoma cells. J Neurosci Res 60 (2000) 311-320
15. Edsjö A., Lavenius E., Nilsson H., Hoehner J.C., Simonsson P., Culp L.A., et al. Expression of trkB in human neuroblastoma in relation to MYCN expression and retinoic acid treatment. Lab Invest 83 (2003) 813-823
16. Huang M.E., Ye Y.C., Chen S.R., Chai J.R., Lu J.X., Zhoa L., et al. Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia. Blood 72 (1988) 567-572
17. Påhlman S., Meyerson G., Lindgren E., Schalling M., and Johansson I. Insulin-like growth factor I shifts from promoting cell division to potentiating maturation during neuronal differentiation. Proc Natl Acad Sci USA 88 (1991) 9994-9998
18. Åkerman K.E.O., Scott I.G., and Andersson L.C. Functional differentiation of human ganglion cell derived neuroblastoma cell line SHSY-5Y induced by a phorbolester (TPA). Neurochem Int 6 (1984) 77-80
19. Parrow V., Nånberg E., Heikkila J., Hammerling U., and Påhlman S. Protein kinase C remains functionally active during TPA induced neuronal differentiation of SH-SY5Y human neuroblastoma cells. J Cell Physiol 152 (1992) 536-544
20. Zeidman R., Löfgren B., Påhlman S., and Larsson C. PKCepsilon, via its regulatory domain and independently of its catalytic domain, induces neurite-like processes in neuroblastoma cells. J Cell Biol 145 (1999) 713-726
21. Anderson D.J. Cellular and molecular biology of neural crest cell lineage determination. Trends Genet 13 (1997) 276-280
22. Lavenius E., Parrow V., Nånberg E., and Påhlman S. Basic FGF and IGF-I promote differentiation of human SH-SY5Y neuroblastoma cells in culture. Growth Factors 10 (1994) 29-39
23. Airaksinen M.S., and Saarma M. The GDNF family: signaling, biological functions and therapeutic value. Nat Rev Neurosci 3 (2002) 383-394
24. Hishiki T., Nimura Y., Isogai E., Kondo K., Ichimiya S., Nakamura Y., et al. Glial cell line-derived neurotrophic factor/neurturin-induced differentiation and its enhancement by retinoic acid in primary human neuroblastomas expressing c-Ret, GFR alpha-1, and GFR alpha-2. Cancer Res 58 (1998) 2158-2165
25. Bibel M., and Barde Y.A. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 14 (2000) 2919-2937
26. Barbacid M. The Trk family of neurotrophin receptors. J Neurobiol 25 (1994) 1386-1403
27. Chao M.V. Neurotrophins and their receptors: a convergence point for many signaling pathways. Nat Rev Neurosci 4 (2003) 299-309
28. Clary D.O., and Reichardt L.F. An alternatively spliced form of the nerve growth factor receptor TrkA confers an enhanced response to neurotrophin 3. Proc Natl Acad Sci USA 91 (1994) 11133-11137
29. Strohmaier C., Carter B.D., Urfer R., Barde Y.A., and Dechant G. A splice variant of the neurotrophin receptor trkB with increased specificity for brain-derived neurotrophic factor. Embo J 15 (1996) 3332-3337
30. Lamballe F., Tapley P., and Barbacid M. trkC encodes multiple neurotrophin-3 receptors with distinct biological properties and substrate specificities. Embo J 12 (1993) 3083-3094
31. Tacconelli A., Farina A.R., Cappabianca L., Desantis G., Tessitore A., Vetuschi A., et al. TrkA alternative splicing: a regulated tumor-promoting switch in human neuroblastoma. Cancer Cell 6 (2004) 347-360
32. Hapner S.J., Boeshore K.L., Large T.H., and Lefcort F. Neural differentiation promoted by truncated trkC receptors in collaboration with p75(NTR). Dev Biol 201 (1998) 90-100
33. Biffo S., Offenhauser N., Carter B.D., and Barde Y.A. Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. Development 121 (1995) 2461-2470
34. Hoehner J.C., Olsen L., Sandstedt B., Kaplan D.R., and Påhlman S. Association of neurotrophin receptor expression and differentiation in human neuroblastoma. Am J Pathol 147 (1995) 102-113
35. Azar C.G., Scavarda N.J., Reynolds C.P., and Brodeur G.M. Multiple defects of the nerve growth factor receptor in human neuroblastomas. Cell Growth Differ 1 (1990) 421-428
36. Nakagawara A., Arima-Nakagawara M., Scavarda N.J., Azar C.G., Cantor A.B., and Brodeur G.M. Association between high levels of expression of the TRK gene and favorable outcome in human neuroblastoma. New Engl J Med 328 (1993) 847-854
37. Ryden M., Sehgal R., Dominici C., Schilling F.H., Ibanez C.F., and Kogner P. Expression of mRNA for the neurotrophin receptor trkC in neuroblastomas with favorable tumor stage and good prognosis. Br J Cancer 74 (1996) 773-779
38. Yamashiro D.J., Nakagawara A., Ikegaki N., Liu X.G., and Brodeur G.M. Expression of TrkC in favorable human neuroblastomas. Oncogene 12 (1996) 37-41
39. Nakagawara A., Azar C.G., Scavarda N.J., and Brodeur G.M. Expression and function of TRK-B and BDNF in human neuroblastomas. Mol Cell Biol 14 (1994) 759-767
40. Nakagawara A., Arima M., Azar C.G., Scavarda N.J., and Brodeur G.M. Inverse relationship between trk expression and N-myc amplification in human neuroblastomas. Cancer Res 52 (1992) 1364-1368
41. Kogner P., Barbany G., Dominici C., Castello M.A., Raschella G., and Persson H. Coexpression of messenger RNA for TRK proto-oncogene and low affinity nerve growth factor receptor in neuroblastoma with favorable prognosis. Cancer Res 53 (1993) 2044-2050
42. Kwiatkowski J.L., Rutkowski J.L., Yamashiro D.J., Tennekoon G.I., and Brodeur G.M. Schwann cell-conditioned medium promotes neuroblastoma survival and differentiation. Cancer Res 58 (1998) 4602-4606
43. Lavenius E., Gestblom C., Johansson I., Nånberg E., and Påhlman S. Transfection of TRK-A into human neuroblastoma cells restores their ability to differentiate in response to nerve growth factor. Cell Growth Differ 6 (1995) 727-736
44. Edsjö A., Hallberg B., Fagerström S., Larsson C., Axelson H., and Påhlman S. Differences in early and late responses between neurotrophin-stimulated trkA- and trkC-transfected SH-SY5Y neuroblastoma cells. Cell Growth Differ 12 (2001) 39-50
45. Matsushima H., and Bogenmann E. Expression of trkA cDNA in neuroblastomas mediates differentiation in vitro and in vivo. Mol Cell Biol 13 (1993) 7447-7456
46. Poluha W., Poluha D.K., and Ross A.H. TrkA neurogenic receptor regulates differentiation of neuroblastoma cells. Oncogene 10 (1995) 185-189
47. Kim C.J., Matsuo T., Lee K.H., and Thiele C.J. Up-regulation of insulin-like growth factor-II expression is a feature of TrkA but not TrkB activation in SH-SY5Y neuroblastoma cells. Am J Pathol 155 (1999) 1661-1670
48. Matsumoto K., Wada R.K., Yamashiro J.M., Kaplan D.R., and Thiele C.J. Expression of brain-derived neurotrophic factor and p145TrkB affects survival, differentiation, and invasiveness of human neuroblastoma cells. Cancer Res 55 (1995) 1798-1806
49. Schramm A., Schulte J.H., Astrahantseff K., Apostolov O., Limpt V., Sieverts H., et al. Biological effects of TrkA and TrkB receptor signaling in neuroblastoma. Cancer Lett 228 (2005) 143-153
50. Semenza G.L. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 7 (2001) 345-350
51. Höckel M., and Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 93 (2001) 266-276
52. Jögi A., Øra I., Nilsson H., Lindeheim A., Makino Y., Poellinger L., et al. Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. PNAS 99 (2002) 7021-7026
53. Ghafar M.A., Anastasiadis A.G., Chen M.W., Burchardt M., Olsson L.E., Xie H., et al. Acute hypoxia increases the aggressive characteristics and survival properties of prostate cancer cells. Prostate 54 (2003) 58-67
54. Helczynska K., Kronblad A., Jögi A., Nilsson E., Beckman S., Landberg G., et al. Hypoxia promotes a dedifferentiated phenotype in ductal breast carcinoma in situ. Cancer Res 63 (2003) 1441-1444
55. Brown J.M. Tumor microenvironment and the response to anticancer therapy. Cancer Biol Ther 1 (2002) 453-458
56. Tian H., Hammer R.E., Matsumoto A.M., Russell D.W., and McKnight S.L. The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes Dev 12 (1998) 3320-3324
57. Jögi A., Vallon-Christersson J., Holmquist L., Axelson H., Borg A., and Påhlman S. Human neuroblastoma cells exposed to hypoxia: induction of genes associated with growth, survival, and aggressive behavior. Exp Cell Res 295 (2004) 469-487
58. Löfstedt T., Jögi A., Sigvardsson M., Gradin K., Poellinger L., Påhlman S., et al. Induction of ID2 expression by hypoxia-inducible factor-1: a role in dedifferentiation of hypoxic neuroblastoma cells. J Biol Chem 279 (2004) 39223-39231
59. Påhlman S., Stockhausen M.T., Fredlund E., and Axelson H. Notch signaling in neuroblastoma. Semin Cancer Biol 14 (2004) 365-373
60. Axelson H., Fredlund E., Ovenberger M., Landberg G., and Påhlman S. Hypoxia-induced dedifferentiation of tumor cells-a mechanism behind heterogeneity and aggressiveness of solid tumors. Semin Cell Dev Biol 16 (2005) 554-563
61. Hedborg F., Ulleras E., Grimelius L., Wassberg E., Maxwell P.H., Hero B., et al. Evidence for hypoxia-induced neuronal-to-chromaffin metaplasia in neuroblastoma. Faseb J 17 (2003) 598-609
62. Jögi A., Persson P., Grynfeld A., Påhlman S., and Axelson H. Modulation of basic helix-loop-helix transcription complex formation by Id proteins during neuronal differentiation. J Biol Chem 277 (2002) 9118-9126
63. Holmquist L., Jögi A., and Påhlman S. Phenotypic persistence after reoxygenation of hypoxic neuroblastoma cells. Int J Cancer 116 (2005) 218-225
64. Nilsson H., Jögi A., Beckman S., Harris A.L., Poellinger L., and Påhlman S. HIF-2α expression in human fetal paraganglia and neuroblastoma: relation to sympathetic differentiation, glucose deficiency, and hypoxia. Exp Cell Res 303 (2005) 447-456
65. Ceradini D.J., Kulkarni A.R., Callaghan M.J., Tepper O.M., Bastidas N., Kleinman M.E., et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10 (2004) 858-864
66. Yokota Y. Id and development. Oncogene 20 (2001) 8290-8298