Skip to main content

Advertisement

SpringerLink
Log in

Role of MAML1 and MEIS1 in Esophageal Squamous Cell Carcinoma Depth of Invasion

  • Original Article
  • Published:
Pathology & Oncology Research

Abstract

Homeobox (HOX) transcription factors and NOTCH signaling pathway are critical regulators of stem cell functions, cell fate in development and homeostasis of gastrointestinal tissues. In the present study, we analyzed cross talk between NOTCH pathway and HOX genes through assessment of probable correlation betweenMAML1 and MEIS1 as the main transcription factor of NOTCH pathway and enhancer of HOX transcriptional machinery, respectively in esophageal squamous cell carcinoma (ESCC) patients. Fifty one ESCC cases were enrolled to assess the levels of Meis1 and Maml1 mRNA expression using real-time polymerase chain reaction (PCR). Only 3 out of 51 (5.9%) cases had MEIS1/MAML1 under expression and 2/51 (3.9%) cases had MEIS1/MAML1over expression. Nine out of 51 samples (17.6%) have shown MEIS1 under expression and MAML1 over expression. There was a significant correlation between MAML1and MEIS1mRNA expressions (p ≤ 0.05). There were significant correlations between MEIS1 under/MAML1 over expressed cases and tumor location (p = 0.05), tumor depth of invasion (p = 0.011), and sex (p = 0.04). Our results showed that MEIS1 may have a negative role in regulation of MAML1expression during the ESCC progression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90. doi:10.3322/caac.20107

    Article  PubMed  Google Scholar 

  2. Moghbeli M, Abbaszadegan MR, Farshchian M, Montazer M, Raeisossadati R, Abdollahi A, Forghanifard MM (2013) Association of PYGO2 and EGFR in esophageal squamous cell carcinoma. Med Oncol 30(2):516

    Article  PubMed  Google Scholar 

  3. Moghbeli M, Abbaszadegan MR, Golmakani E, Forghanifard MM (2016) Correlation of Wnt and NOTCH pathways in esophageal squamous cell carcinoma. J Cell Commun Signal 10(2):129–135

    Article  PubMed  PubMed Central  Google Scholar 

  4. Moghbeli M, Forghanifard MM, Sadrizadeh A, Mozaffari HM, Golmakani E, Abbaszadegan MR (2015) Role of Msi1 and MAML1 in regulation of notch signaling pathway in patients with esophageal squamous cell carcinoma. J Gastrointest Cancer 46(4):365–369

    Article  CAS  PubMed  Google Scholar 

  5. Moghbeli M, Moghbeli F, Forghanifard MM, Garayali A, Abbaszadegan MR (2013) Cancer stem cell markers in esophageal cancer. American Journal of Cancer Science 2(1):37–50

    Google Scholar 

  6. Moghbeli M, Rad A, Farshchian M, Taghehchian N, Gholamin M, Abbaszadegan MR (2016) Correlation between Meis1 and Msi1 in esophageal squamous cell carcinoma. J Gastrointest Cancer 47(3):273–277

    Article  CAS  PubMed  Google Scholar 

  7. Moghbeli M, Sadrizadeh A, Forghanifard MM, Mozaffari HM, Golmakani E, Abbaszadegan MR (2016) Role of Msi1 and PYGO2 in esophageal squamous cell carcinoma depth of invasion. J Cell Commun Signal 10(1):49–53

    Article  PubMed  Google Scholar 

  8. Taleb S, Abbaszadegan MR, Moghbeli M, Roudbari NH, Forghanifard MM (2014) HES1 as an independent prognostic marker in esophageal squamous cell carcinoma. J Gastrointest Cancer 45(4):466–471

    Article  CAS  PubMed  Google Scholar 

  9. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284(5415):770–776

    Article  CAS  PubMed  Google Scholar 

  10. Hsieh JJ, Zhou S, Chen L, Young DB, Hayward SD (1999) CIR, a corepressor linking the DNA binding factor CBF1 to the histone deacetylase complex. Proc Natl Acad Sci U S A 96(1):23–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kao HY, Ordentlich P, Koyano-Nakagawa N, Tang Z, Downes M, Kintner CR, Evans RM, Kadesch T (1998) A histone deacetylase corepressor complex regulates the notch signal transduction pathway. Genes Dev 12(15):2269–2277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Taniguchi Y, Furukawa T, Tun T, Han H, Honjo T (1998) LIM protein KyoT2 negatively regulates transcription by association with the RBP-J DNA-binding protein. Mol Cell Biol 18(1):644–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Oswald F, Tauber B, Dobner T, Bourteele S, Kostezka U, Adler G, Liptay S, Schmid RM (2001) p300 acts as a transcriptional coactivator for mammalian notch-1. Mol Cell Biol 21(22):7761–7774. doi:10.1128/MCB.21.22.7761-7774.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kurooka H, Honjo T (2000) Functional interaction between the mouse notch1 intracellular region and histone acetyltransferases PCAF and GCN5. J Biol Chem 275(22):17211–17220. doi:10.1074/jbc.M000909200

    Article  CAS  PubMed  Google Scholar 

  15. Wu L, Sun T, Kobayashi K, Gao P, Griffin JD (2002) Identification of a family of mastermind-like transcriptional coactivators for mammalian notch receptors. Mol Cell Biol 22(21):7688–7700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kitagawa M, Oyama T, Kawashima T, Yedvobnick B, Kumar A, Matsuno K, Harigaya K (2001) A human protein with sequence similarity to drosophila mastermind coordinates the nuclear form of notch and a CSL protein to build a transcriptional activator complex on target promoters. Mol Cell Biol 21(13):4337–4346. doi:10.1128/MCB.21.13.4337-4346.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lin SE, Oyama T, Nagase T, Harigaya K, Kitagawa M (2002) Identification of new human mastermind proteins defines a family that consists of positive regulators for notch signaling. J Biol Chem 277(52):50612–50620. doi:10.1074/jbc.M209529200

    Article  CAS  PubMed  Google Scholar 

  18. Wu L, Aster JC, Blacklow SC, Lake R, Artavanis-Tsakonas S, Griffin JD (2000) MAML1, a human homologue of drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nat Genet 26(4):484–489. doi:10.1038/82644

    Article  CAS  PubMed  Google Scholar 

  19. Jeffries S, Robbins DJ, Capobianco AJ (2002) Characterization of a high-molecular-weight notch complex in the nucleus of notch(ic)-transformed RKE cells and in a human T-cell leukemia cell line. Mol Cell Biol 22(11):3927–3941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Saint Just Ribeiro M, Hansson ML, Wallberg AE (2007) A proline repeat domain in the notch co-activator MAML1 is important for the p300-mediated acetylation of MAML1. Biochem J 404(2):289–298. doi:10.1042/BJ20061900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Owens BM, Hawley RG (2002) HOX and non-HOX homeobox genes in leukemic hematopoiesis. Stem Cells 20(5):364–379

    Article  CAS  PubMed  Google Scholar 

  22. Sitwala KV, Dandekar MN, Hess JL (2008) HOX proteins and leukemia. Int J Clin Exp Pathol 1(6):461–474

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Cillo C, Cantile M, Faiella A, Boncinelli E (2001) Homeobox genes in normal and malignant cells. J Cell Physiol 188(2):161–169

    Article  CAS  PubMed  Google Scholar 

  24. Goh SL, Looi Y, Shen H, Fang J, Bodner C, Houle M, Ng AC, Screaton RA, Featherstone M (2009) Transcriptional activation by MEIS1A in response to protein kinase a signaling requires the transducers of regulated CREB family of CREB co-activators. J Biol Chem 284(28):18904–18912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Huang H, Rastegar M, Bodner C, Goh SL, Rambaldi I, Featherstone M (2005) MEIS C termini harbor transcriptional activation domains that respond to cell signaling. J Biol Chem 280(11):10119–10127

    Article  CAS  PubMed  Google Scholar 

  26. Wang Z, Iwasaki M, Ficara F, Lin C, Matheny C, Wong SH, Smith KS, Cleary ML (2010) GSK-3 promotes conditional association of CREB and its coactivators with MEIS1 to facilitate HOX-mediated transcription and oncogenesis. Cancer Cell 17(6):597–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Boucherat O, Chakir J, Jeannotte L (2012) The loss of Hoxa5 function promotes notch-dependent goblet cell metaplasia in lung airways. Biol Open 1(7):677–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chariot A, Gielen J, Merville MP, Bours V (1999) The homeodomain-containing proteins: an update on their interacting partners. Biochem Pharmacol 58(12):1851–1857

    Article  CAS  PubMed  Google Scholar 

  29. Esparza SD, Chang J, Shankar DB, Zhang B, Nelson SF, Sakamoto KM (2008) CREB regulates Meis1 expression in normal and malignant hematopoietic cells. Leukemia 22(3):665–667. doi:10.1038/sj.leu.2404933

    Article  CAS  PubMed  Google Scholar 

  30. Ferretti E, Villaescusa JC, Di Rosa P, Fernandez-Diaz LC, Longobardi E, Mazzieri R, Miccio A, Micali N, Selleri L, Ferrari G, Blasi F (2006) Hypomorphic mutation of the TALE gene Prep1 (pKnox1) causes a major reduction of Pbx and Meis proteins and a pleiotropic embryonic phenotype. Mol Cell Biol 26(15):5650–5662. doi:10.1128/MCB.00313-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Moghbeli M, Maleknejad M, Arabi A, Abbaszadegan MR (2012) Mutational analysis of uroporphyrinogen III cosynthase gene in Iranian families with congenital erythropoietic porphyria. Mol Biol Rep 39(6):6731–6735

    Article  CAS  PubMed  Google Scholar 

  32. Forghanifard MM, Moghbeli M, Raeisossadati R, Tavassoli A, Mallak AJ, Boroumand-Noughabi S, Abbaszadegan MR (2013) Role of SALL4 in the progression and metastasis of colorectal cancer. J Biomed Sci 20:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Forghanifard MM, Moaven O, Farshchian M, Montazer M, Raeisossadati R, Abdollahi A, Moghbeli M, Nejadsattari T, Parivar K, Abbaszadegan MR (2012) Expression analysis elucidates the roles of MAML1 and Twist1 in esophageal squamous cell carcinoma aggressiveness and metastasis. Ann Surg Oncol 19(3):743–749

    Article  PubMed  Google Scholar 

  34. Grier DG, Thompson A, Kwasniewska A, McGonigle GJ, Halliday HL, Lappin TR (2005) The pathophysiology of HOX genes and their role in cancer. J Pathol 205(2):154–171. doi:10.1002/path.1710

    Article  CAS  PubMed  Google Scholar 

  35. Wermuth PJ, Buchberg AM (2005) Meis1-mediated apoptosis is caspase dependent and can be suppressed by coexpression of HoxA9 in murine and human cell lines. Blood 105(3):1222–1230. doi:10.1182/blood-2004-03-0802

    Article  CAS  PubMed  Google Scholar 

  36. Yamashita T, Tazawa S, Yawei Z, Katayama H, Kato Y, Nishiwaki K, Yokohama Y, Ishikawa M (2006) Suppression of invasive characteristics by antisense introduction of overexpressed HOX genes in ovarian cancer cells. Int J Oncol 28(4):931–938

    CAS  PubMed  Google Scholar 

  37. Argiropoulos B, Yung E, Humphries RK (2007) Unraveling the crucial roles of Meis1 in leukemogenesis and normal hematopoiesis. Genes Dev 21(22):2845–2849. doi:10.1101/gad.1619407

    Article  CAS  PubMed  Google Scholar 

  38. Calvo KR, Knoepfler PS, Sykes DB, Pasillas MP, Kamps MP (2001) Meis1a suppresses differentiation by G-CSF and promotes proliferation by SCF: potential mechanisms of cooperativity with Hoxa9 in myeloid leukemia. Proc Natl Acad Sci U S A 98(23):13120–13125. doi:10.1073/pnas.231115398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kumar AR, Li Q, Hudson WA, Chen W, Sam T, Yao Q, Lund EA, Wu B, Kowal BJ, Kersey JH (2009) A role for MEIS1 in MLL-fusion gene leukemia. Blood 113(8):1756–1758. doi:10.1182/blood-2008-06-163287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS, Reed JC (1998) IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 17(8):2215–2223. doi:10.1093/emboj/17.8.2215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lindahl T, Satoh MS, Poirier GG, Klungland A (1995) Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem Sci 20(10):405–411

    Article  CAS  PubMed  Google Scholar 

  42. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91(4):479–489

    Article  CAS  PubMed  Google Scholar 

  43. Brinkmann U, Brinkmann E, Gallo M, Pastan I (1995) Cloning and characterization of a cellular apoptosis susceptibility gene, the human homologue to the yeast chromosome segregation gene CSE1. Proc Natl Acad Sci U S A 92(22):10427–10431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Vice Chancellor for Research at Mashhad University of Medical Sciences, No. 921202.

Author information

Authors and Affiliations

  1. Division of Human Genetics, Immunology Research Center, Avicenna Research Institute, Mashhad University of Medical Sciences, Mashhad, Iran

    Mohammad Reza Abbaszadegan

  2. Medical Genetics Research Center, Medical School, Mashhad University of Medical Sciences, Mashhad, Iran

    Mohammad Reza Abbaszadegan

  3. North Khorasan University of Medical Sciences, Bojnurd, Iran

    Meysam Moghbeli

Authors
  1. Mohammad Reza Abbaszadegan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Meysam Moghbeli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Meysam Moghbeli.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Funding

This work was supported by a grant from the Vice Chancellor for Research at Mashhad University of Medical Sciences, No. 921202.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abbaszadegan, M.R., Moghbeli, M. Role of MAML1 and MEIS1 in Esophageal Squamous Cell Carcinoma Depth of Invasion. Pathol. Oncol. Res. 24, 245–250 (2018). https://doi.org/10.1007/s12253-017-0243-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12253-017-0243-1

Keywords

Search

Navigation