Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Retinoic acid receptors and tissue-transglutaminase mediate short-term effect of retinoic acid on migration and invasion of neuroblastoma SH-SY5Y cells

Oncogene volume 25, pages 240–247 (2006)Cite this article

Abstract

Long-term treatment with all trans-retinoic acid (RA) induces neuronal differentiation and apoptosis. However, the effect of short-term RA treatment on cell proliferation, migration and invasion of neuroblastoma cell lines (SH-SY5Y and IMR-32) remains unclear. RA induces expression of tissue-transglutaminase (TGase) and promotes migration and invasion after 24 h of treatment in SH-SY5Y cells, but not in IMR-32 cells. RA receptor (RAR) agonist (4-(E-2-[5,6,7,8-tetrahydro-5,5,8,8-tetramethyl-2-naphthalenyl]-1-propenyl) benzoic acid) and RAR/retinoid X receptor (RXR) agonist (9-cis-RA) promote expression of TGase, migration and invasion of SH-SY5Y cells, while RXR agonist has no significant effect. RAR antagonist blocks RA effect on migration and invasion, indicating that RAR receptors are required. Retinoid receptors are expressed and activated by RA in both cell lines. However, only transient activation of RAR is observed in IMR-32 cells. These findings suggest that different responses observed in SH-SY5Y and IMR-32 cells could be due to differential activation of retinoid receptors. Overexpression of TGase has no effect on migration or invasion, while overexpression of antisense TGase blocks RA-induced migration and invasion, indicating that other molecules along with TGase mediate RA effects. In addition to the long-term effects of RA that are coupled with cell differentiation, short-term effects involve migration and invasion of neuroblastoma SH-SY5Y cells.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  • Abel EL . (2001). J Pediatr 138: 295–296.

  • Akimov SS, Belkin AM . (2001). Blood 98: 1567–1576.

  • Akimov SS, Krylov D, Fleischman LF, Belkin AM . (2000). J Cell Biol 148: 825–838.

  • Antonyak MA, Singh US, Lee DA, Boehm JE, Combs C, Zgola MM et al. (2001). J Biol Chem 276: 33582–33587.

  • Arvidsson Y, Hamazaki TS, Ichijo H, Funa K . (2001). Cell Death Differ 8: 1029–1037.

  • Biedler JL, Spengler BA, Chang TD, Ross RA . (1988). Prog Clin Biol Res 271: 265–276.

  • Carpentier A, Balitrand N, Rochette-Egly C, Shroot B, Degos L, Chomienne C . (1997). Oncogene 15: 1805–1813.

  • Castleberry RP . (1997). Pediatr Clin North Am 44: 919–937.

  • Chambaut-Guerin AM, Herigault S, Rouet-Benzineb P, Rouher C, Lafuma C . (2000). J Neurochem 74: 508–517.

  • Chambon P . (1996). FASEB J 10: 940–954.

  • Cianfarani S, Rossi P . (1997). Eur J Pediatr 156: 256–261.

  • Ciccarone V, Spengler BA, Meyers MB, Biedler JL, Ross RA . (1989). Cancer Res 49: 219–225.

  • Davies PJA, Stein JP, Chiocca EA, Basilion JP, Gentile V, Thomazy V et al. (1992). Retinoids in Normal Development and Teratogenesis. New York: Oxford University Press.

    Google Scholar 

  • Denning MF, Verma AK . (1991). Biochem Biophys Res Commun 175: 344–350.

  • Eggert A, Grotzer MA, Ikegaki N, Liu XG, Evans AE, Brodeur GM . (2002). Cancer Res 62: 1802–1808.

  • Emionite L, Galmozzi F, Raffo P, Vergani L, Toma S . (2003). Anticancer Res 23 (1A): 13–19.

  • Farina A, Tacconelli A, Vacca A, Maroder M, Gulino A, Mackay A . (1999). Cell Growth Differ 10: 353–367.

  • Farina AR, Masciulli MP, Tacconelli A, Cappabianca L, De Santis G, Gulino A et al. (2002). Cell Growth Differ 13: 343–354.

  • Festuccia C, Bologna M, Vicentini C, Tacconelli A, Miano R, Violini S et al. (1996). Int J Cancer 69: 1–8.

  • Fesus L, Piacentini M . (2002). Trends Biochem Sci 27: 534–539.

  • Floyd EE, Jetten AM . (1989). Mol Cell Biol 9: 4846–4851.

  • Folk JE, Finlayson JS . (1977). Adv Protein Chem 31: 1–133.

  • Frappaz D, Michon J, Coze C, Berger C, Plouvier E, Lasset C et al. (2000). J Clin Oncol 18: 468–476.

  • Giannini G, Dawson M, Zhang X, Thiele C . (1997). J Biol Chem 272: 26693–26701.

  • Heyman RA, Mangelsdorf DJ, Dyck JA, Stein RB, Eichele G, Evans RM et al. (1992). Cell 68: 397–406.

  • Ishaq M, Fan M, Natarajan V . (2000). J Immunol 165: 4217–4225.

  • Isobe T, Takahashi H, Ueki S, Takagi J, Saito Y . (1999). Eur J Cell Biol 78: 876–883.

  • Juliano R . (1994). Cancer Met Rev 13: 25–30.

  • Kang SK, Yi KS, Kwon NS, Park KH, Kim UH, Baek KJ et al. (2004). J Biol Chem 279: 36593–36600.

  • Kim B, Leventhal PS, Saltiel AR, Feldman EL . (1997). J Biol Chem 272: 21268–21273.

  • Klaassen I, Brakenhoff R, Smeets S, Snow G, Braakhuis D . (2001). Int J Cancer 92: 661–665.

  • Leelawat K, Ohuchida K, Mizumoto K, Mahidol C, Tanaka M . (2005). Cancer Lett 224: 303–310.

  • Lotan Y, Xu X, Shalev M, Lotan R, Williams R, Wheeler T et al. (2000). J Clin Oncol 18: 116–121.

  • Mackay A, Ballin M, Pellina M, Farina A, Nason A, Hartzler J et al. (1992). Invas Metastasis 12: 168–184.

  • Maden M . (2002). Nat Rev Neurosci 3: 843–853.

  • Maden M, Holder N . (1992). BioEssays 14: 431–438.

  • Mehta K, Fok J, Miller FR, Koul D, Sahin AA . (2004). Clin Cancer Res 10: 8068–8076.

  • Meyer GE, Shelden E, Kim B, Feldman EL . (2001). Oncogene 20: 7542–7550.

  • Mohan K, Pinto D, Issekutz TB . (2003). J Immunol 171: 3179–3186.

  • Niles RM . (2004). Mutat Res 55: 97–105.

  • Palm-Leis A, Singh US, Herbelin BS, Olsovsky GD, Baker KM, Pan J . (2004). J Biol Chem 279: 54905–54917.

  • Pan J, Kao Y, Joshi S, Jeethendran S, DiPette D, Singh U . (2005). J Neurochemistry 10: 1–13.

  • Phuangsab A, Lorence RM, Reichard KW, Peeples ME, Walter RJ . (2001). Cancer Lett 172: 27–36.

  • Pola S, Cattaneo MG, Vicentini LM . (2003). J Biol Chem 278: 40601–40606.

  • Ponthan F, Borgstrom P, Hassan M, Wassberg E, Redfern C, Kogner P . (2001). Med Pediatr Oncol 36: 127–131.

  • Ponthan F, Johnsen JI, Klevenvall L, Castro J, Kogner P . (2003). Int J Cancer 104: 418–424.

  • Praise L, Lee J, Juliano RL . (2000). Sem Cancer Biol 10: 407–414.

  • Priglinger SG, Alge CS, Neubauer AS, Kristin N, Hirneiss C, Eibl K et al. (2004). Invest Ophthalmol Vis Sci 45: 955–963.

  • Qui H, Zhang Wm, El-Naggar A, Lippman S, Lin P, Lotan R et al. (1999). Am J Pathol 155: 1519–1523.

  • Reynolds CP . (2000). Curr Oncol Rep 2: 511–518.

  • Reynolds CP, Lemons RS . (2001). Hematol Oncol Clin North Am 15: 867–910.

  • Reynolds CP, Matthay KK, Villablanca JG, Maurer BJ . (2003). Cancer Lett 197: 185–192.

  • Rodolfo C, Mormone E, Matarrese P, Ciccosanti F, Farrace MG, Garofano E et al. (2004). J Biol Chem 279: 54783–54792.

  • Rossino P, Defilippi P, Silengo L, Tarone G . (1991). Cell Regul 2: 1021–1033.

  • Sato H, Kida Y, Mai M, Endo Y, Tanaka J, Seiki M . (1995). Oncogene 7: 77–83.

  • Schmidt ML, Lukens JN, Seeger RC, Brodeur GM, Shimada H, Gerbing RB et al. (2000). J Clin Oncol 18: 1260–1268.

  • Singh US, Pan J, Kao YL, Joshi S, Young KL, Baker KM . (2003). J Biol Chem 278: 391–399.

  • Smethurst PA, Griffin M . (1996). Biochem J 313 (Part 3): 803–808.

  • Soprano KJ, Soprano DR . (2002). J Nutr 132: 3809S–3813S.

  • Sporn MB, Roberts AB, Goodman D . (1994). The Retinoids: Biology and Medicine. New York: Raven Press.

    Google Scholar 

  • Stahle M, Veit C, Bachfischer U, Schierling K, Skripczynski B, Hall A et al. (2003). J Cell Sci 116: 3835–3846.

  • Sugiura Y, Shimada H, Seeger R, Laug W, DeClerck Y . (1998). Cancer Res 58: 2209–2216.

  • Tucholski J, Lesort M, Johnson GV . (2001). Neuroscience 102: 481–491.

  • Voigt A, Zintl F . (2003). Med Pediatr Oncol 40: 205–213.

  • Westermann F, Schwab M . (2002). Cancer Lett 184: 127–147.

  • Xu C, Sneige N, Liu X, Nandagiri R, Lee J, Luckmanji F et al. (1997a). Cancer Res 57: 4992–4996.

  • Xu X, Sozzi G, Lee J, Lee JS, Paroeino U, Pilotti S et al. (1997b). J Natl Cancer Inst 89: 624–629.

  • Xu X, Sozzi J, Lee JS, Lee J, Shin D, Hong W et al. (1994). Cancer Res 54: 3580–3587.

  • Yao M, Bain G, Gottlieb DI . (1995). J Neurosci Res 41: 792–804.

  • Zang C, Liu H, Ries C, Ismair MG, Petrides PE . (2000). J Cancer Res Clin Oncol 126: 33–40.

  • Zhang L, Mills K, Dawson M, Collins S, Jetten A . (1995). J Biol Chem 270: 6022–6029.

Download references

Acknowledgements

Support for this work was in part provided by the Veteran Affairs VISN-17 and Scott and White resident training grant # 8271. We thank Gail V Johnson (University of Alabama at Birmingham, AL, USA) for providing stable cell lines of SH-SY5Y cells.

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Cardiovascular Research Institute, The Texas A&M University System Health Science Center, College of Medicine,

    S Joshi, R Guleria, J Pan, D DiPette & U S Singh

  2. Scott & White, Temple, TX, USA

    S Joshi, R Guleria, J Pan, D DiPette & U S Singh

  3. Central Texas Veterans Health Care System, Temple, TX, USA

    S Joshi, R Guleria, J Pan, D DiPette & U S Singh

Authors
  1. S Joshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R Guleria
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D DiPette
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. U S Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to U S Singh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Joshi, S., Guleria, R., Pan, J. et al. Retinoic acid receptors and tissue-transglutaminase mediate short-term effect of retinoic acid on migration and invasion of neuroblastoma SH-SY5Y cells. Oncogene 25, 240–247 (2006). https://doi.org/10.1038/sj.onc.1209027

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1209027

Keywords

This article is cited by

Search

Advanced search

Quick links