Cancer Letters
Volume 228, Issue 1 , Pages 97-104 , 18 October 2005

Molecular mechanism of HMGA1 deregulation in human neuroblastoma

  • Giuseppe Giannini

      Affiliations

    • Department of Experimental Medicine and Pathology, Department of Pediatrics, University ‘La Sapienza’, Policlinico Umberto 1, Viale Regina Elena, 324, 00161 Rome, Italy
    • Corresponding Author InformationCorresponding author. Tel.: +39 6 495 86 37; fax: +39 6 446 19 74.
  • ,
  • Fabio Cerignoli

      Affiliations

    • Department of Experimental Medicine and Pathology, Department of Pediatrics, University ‘La Sapienza’, Policlinico Umberto 1, Viale Regina Elena, 324, 00161 Rome, Italy
  • ,
  • Massimiliano Mellone

      Affiliations

    • Department of Experimental Medicine and Pathology, Department of Pediatrics, University ‘La Sapienza’, Policlinico Umberto 1, Viale Regina Elena, 324, 00161 Rome, Italy
  • ,
  • Isabella Massimi

      Affiliations

    • Department of Experimental Medicine and Pathology, Department of Pediatrics, University ‘La Sapienza’, Policlinico Umberto 1, Viale Regina Elena, 324, 00161 Rome, Italy
  • ,
  • Cinzia Ambrosi

      Affiliations

    • Department of Experimental Medicine and Pathology, Department of Pediatrics, University ‘La Sapienza’, Policlinico Umberto 1, Viale Regina Elena, 324, 00161 Rome, Italy
  • ,
  • Christian Rinaldi

      Affiliations

    • Neuromed Institute, Pozzilli, Italy
  • ,
  • Alberto Gulino

      Affiliations

    • Department of Experimental Medicine and Pathology, Department of Pediatrics, University ‘La Sapienza’, Policlinico Umberto 1, Viale Regina Elena, 324, 00161 Rome, Italy
    • Neuromed Institute, Pozzilli, Italy

Received 26 November 2004 ,Accepted 12 January 2005.

References 

  1. Johnson KR, Lehn DA, Reeves R. Alternative processing of mRNAs encoding mammalian chromosomal high-mobility-group proteins HMG-I and HMG-Y. Mol. Cell. Biol. 1989;9:2114–2123
  2. Friedmann M, Holth LT, Zoghbi HY, Reeves R. Organization, inducible-expression and chromosome localization of the human HMG-I(Y) nonhistone protein gene. Nucleic Acids Res. 1993;21:4259–4267
  3. Kottickal LV, Sarada B, Ashar H, Chada K, Nagarajan L. Preferential expression of HMGI-C isoforms lacking the acidic carboxy terminal in human leukemia. Biochem. Biophys. Res. Commun. 1998;242:452–456
  4. Reeves R. Molecular biology of HMGA proteins: hubs of nuclear function. Gene. 2001;277:63–81
  5. Disney JE, Johnson KR, Magnuson NS, Sylvester SR, Reeves R. High-mobility group protein HMG-I localizes to G/Q- and C-bands of human and mouse chromosomes. J. Cell Biol. 1989;109:1975–1982
  6. Hill DA, Pedulla ML, Reeves R. Directional binding of HMG-I(Y) on four-way junction DNA and the molecular basis for competitive binding with HMG-1 and histone H1. Nucleic Acids Res. 1999;27:2135–2144
  7. Takaha N, Hawkins AL, Griffin CA, Isaacs WB, Coffey DS. High mobility group protein I(Y): a candidate architectural protein for chromosomal rearrangements in prostate cancer cells. Cancer Res. 2002;62:647–651
  8. Farnet CM, Bushman FD. HIV-1 cDNA integration: requirement of HMG I(Y) protein for function of preintegration complexes in vitro. Cell. 1997;88:483–492
  9. Manabe T, Katayama T, Sato N, Gomi F, Hitomi J, Yanagita T, et al. Induced HMGA1a expression causes aberrant splicing of Presenilin-2 pre-mRNA in sporadic Alzheimer's disease. Cell Death Differ. 2003;10:698–708
  10. Zhao K, Kas E, Gonzalez E, Laemmli UK. SAR-dependent mobilization of histone H1 by HMG-I/Y in vitro: HMG-I/Y is enriched in H1-depleted chromatin. Eur. Mol. Biol. Org. J. 1993;12:3237–3247
  11. Yie J, Merika M, Munshi N, Chen G, Thanos D. The role of HMG I(Y) in the assembly and function of the IFN-beta enhanceosome. Eur. Mol. Biol. Org. J. 1999;18:3074–3089
  12. Munshi N, Agalioti T, Lomvardas S, Merika M, Chen G, Thanos D. Coordination of a transcriptional switch by HMGI(Y) acetylation. Science. 2001;293:1133–1136
  13. Sgarra R, Rustighi A, Tessari MA, Di Bernardo J, Altamura S, Fusco A, et al. Nuclear phosphoproteins HMGA and their relationship with chromatin structure and cancer. Fed. Eur. Biochem. Soc. Lett. 2004;574:1–8
  14. Chin MT, Pellacani A, Wang H, Lin SS, Jain MK, Perrella MA, et al. Enhancement of serum-response factor-dependent transcription and DNA binding by the architectural transcription factor HMG-I(Y). J. Biol. Chem. 1998;273:9755–9760
  15. Reeves R, Edberg DD, Li Y. Architectural transcription factor HMGI(Y) promotes tumor progression and mesenchymal transition of human epithelial cells. Mol. Cell. Biol. 2001;21:575–594
  16. Martinez Hoyos J, Fedele M, Battista S, Pentimalli F, Kruhoffer M, Arra C, et al. Identification of the genes up- and down-regulated by the high mobility group A1 (HMGA1) proteins: tissue specificity of the HMGA1-dependent gene regulation. Cancer Res. 2004;64:5728–5735
  17. Zhou X, Benson KF, Ashar HR, Chada K. Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature. 1995;376:771–774
  18. Battista S, Fidanza V, Fedele M, Klein-Szanto AJ, Outwater E, Brunner H, et al. The expression of a truncated HMGI-C gene induces gigantism associated with lipomatosis. Cancer Res. 1999;59:4793–4797
  19. Arlotta P, Tai AK, Manfioletti G, Clifford C, Jay G, Ono SJ. Transgenic mice expressing a truncated form of the high mobility group I-C protein develop adiposity and an abnormally high prevalence of lipomas. J. Biol. Chem. 2000;275:14394–14400
  20. Liu J, Schiltz JF, Ashar HR, Chada KK. Hmga1 is required for normal sperm development. Mol. Reprod. Dev. 2003;66:81–89
  21. Melillo RM, Pierantoni GM, Scala S, Battista S, Fedele M, Stella A, et al. Critical role of the HMGI(Y) proteins in adipocytic cell growth and differentiation. Mol. Cell. Biol. 2001;21:2485–2495
  22. Battista S, Pentimalli F, Baldassarre G, Fedele M, Fidanza V, Croce CM, et al. Loss of Hmga1 gene function affects embryonic stem cell lympho-hematopoietic differentiation. Fed. Am. Soc. Exp. Biol. J. 2003;17:1496–1498
  23. Goodwin GH, Cockerill PN, Kellam S, Wright CA. Fractionation by high-performance liquid chromatography of the low-molecular-mass high-mobility-group (HMG) chromosomal proteins present in proliferating rat cells and an investigation of the HMG proteins present in virus transformed cells. Eur. J. Biochem. 1985;149:47–51
  24. Giancotti V, Berlingieri MT, Di Fiore PP, Fusco A, Vecchio G, Crane-Robinson C. Changes in nuclear proteins on transformation of rat epithelial thyroid cells by a murine sarcoma retrovirus. Cancer Res. 1985;45:6051–6057
  25. Tallini G, Dal Cin P. HMGI(Y) and HMGI-C dysregulation: a common occurrence in human tumors. Adv. Anat. Pathol. 1999;6:237–246
  26. Chiappetta G, Tallini G, De Biasio MC, Manfioletti G, Martinez-Tello FJ, Pentimalli F, et al. Detection of high mobility group I HMGI(Y) protein in the diagnosis of thyroid tumors: HMGI(Y) expression represents a potential diagnostic indicator of carcinoma. Cancer Res. 1998;58:4193–4198
  27. Abe N, Watanabe T, Sugiyama M, Uchimura H, Chiappetta G, Fusco A, et al. Determination of high mobility group I(Y) expression level in colorectal neoplasias: a potential diagnostic marker. Cancer Res. 1999;59:1169–1174
  28. Bussemakers MJ, van de Ven WJ, Debruyne FM, Schalken JA. Identification of high mobility group protein I(Y) as potential progression marker for prostate cancer by differential hybridization analysis. Cancer Res. 1991;51:606–611
  29. Tamimi Y, van der Poel HG, Karthaus HF, Debruyne FM, Schalken JA. A retrospective study of high mobility group protein I(Y) as progression marker for prostate cancer determined by in situ hybridization. Br. J. Cancer. 1996;74:573–578
  30. Giannini G, Di Marcotullio L, Ristori E, Zani M, Crescenzi M, Scarpa S, et al. HMGI(Y) and HMGI-C genes are expressed in neuroblastoma cell lines and tumors and affect retinoic acid responsiveness. Cancer Res. 1999;59:2484–2492
  31. Giannini G, Kim CJ, Marcotullio LD, Manfioletti G, Cardinali B, Cerignoli F, et al. Expression of the HMGI(Y) gene products in human neuroblastic tumours correlates with differentiation status. Br. J. Cancer. 2000;83:1503–1509
  32. Wood LJ, Maher JF, Bunton TE, Resar LM. The oncogenic properties of the HMG-I gene family. Cancer Res. 2000;60:4256–4261
  33. Scala S, Portella G, Fedele M, Chiappetta G, Fusco A. Adenovirus-mediated suppression of HMGI(Y) protein synthesis as potential therapy of human malignant neoplasias. Proc. Natl Acad. Sci. USA. 2000;97:4256–4261
  34. Wood LJ, Mukherjee M, Dolde CE, Xu Y, Maher JF, Bunton TE, et al. HMG-I/Y, a new c-Myc target gene and potential oncogene. Mol. Cell. Biol. 2000;20:5490–5502
  35. Lanahan A, Williams JB, Sanders LK, Nathans D. Growth factor-induced delayed early response genes. Mol. Cell. Biol. 1992;12:3919–3929
  36. Ayoubi TA, Jansen E, Meulemans SM, Van de Ven WJ. Regulation of HMGIC expression: an architectural transcription factor involved in growth control and development. Oncogene. 1999;18:5076–5087
  37. Chau KY, Patel UA, Lee KL, Lam HY, Crane-Robinson C. The gene for the human architectural transcription factor HMGI-C consists of five exons each coding for a distinct functional element. Nucleic Acids Res. 1995;23:4262–4266
  38. Ogram SA, Reeves R. Differential regulation of a multipromoter gene. Selective 12-O- tetradecanoylphorbol-13-acetate induction of a single transcription start site in the HMG-I/Y gene. J. Biol. Chem. 1995;270:14235–14242
  39. Holth LT, Thorlacius AE, Reeves R. Effects of epidermal growth factor and estrogen on the regulation of the HMG-I/Y gene in human mammary epithelial cell lines. DNA Cell Biol. 1997;16:1299–1309
  40. Pedulla ML, Treff NR, Resar LM, Reeves R. Sequence and analysis of the murine Hmgiy (Hmga1) gene locus. Gene. 2001;271:51–58
  41. Schwab M, Alitalo K, Klempnauer KH, Varmus HE, Bishop JM, Gilbert F, et al. Amplified DNA with limited homology to myc cellular oncogene is shared by human neuroblastoma cell lines and a neuroblastoma tumour. Nature. 1983;305:245–248
  42. Seeger RC, Brodeur GM, Sather H, Dalton A, Siegel SE, Wong KY, et al. Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas. N. Engl. J. Med. 1985;313:1111–1116
  43. Schwab M. MYCN in neuronal tumours. Cancer Lett. 2004;204:179–187
  44. Thiele CJ, Reynolds CP, Israel MA. Decreased expression of N-myc precedes retinoic acid-induced morphological differentiation of human neuroblastoma. Nature. 1985;313:404–406
  45. Peverali FA, Orioli D, Tonon L, Ciana P, Bunone G, Negri M, et al. Retinoic acid-induced growth arrest and differentiation of neuroblastoma cells are counteracted by N-myc and enhanced by max overexpressions. Oncogene. 1996;12:457–462
  46. Weiss WA, Aldape K, Mohapatra G, Feuerstein BG, Bishop JM. sTargeted expression of MYCN causes neuroblastoma in transgenic mice. Eur. Mol. Biol. Org. J. 1997;16:2985–2995
  47. Jones TA, Flomen RH, Senger G, Nizetic D, Sheer D. The homeobox gene MEIS1 is amplified in IMR-32 and highly expressed in other neuroblastoma cell lines. Eur. J. Cancer. 2000;36:2368–2374
  48. Spieker N, van Sluis P, Beitsma M, Boon K, van Schaik BD, van Kampen AH, et al. The MEIS1 oncogene is highly expressed in neuroblastoma and amplified in cell line IMR32. Genomics. 2001;71:214–221
  49. Geerts D, Schilderink N, Jorritsma G, Versteeg R. The role of the MEIS homeobox genes in neuroblastoma. Cancer Lett. 2003;197:87–92
  50. Axelson H. The Notch signaling cascade in neuroblastoma: role of the basic helix-loop-helix proteins HASH-1 and HES-1. Cancer Lett. 2004;204:171–178
  51. Pahlman S, Stockhausen MT, Fredlund E, Axelson H. Notch signaling in neuroblastoma. Semin. Cancer Biol. 2004;14:365–373
  52. Ji YS, Xu Q, Schmedtje JF. Hypoxia induces high-mobility-group protein I(Y) and transcription of the cyclooxygenase-2 gene in human vascular endothelium. Circ. Res. 1998;83:295–304

PII: S0304-3835(05)00334-4

doi: 10.1016/j.canlet.2005.01.045

Cancer Letters
Volume 228, Issue 1 , Pages 97-104 , 18 October 2005