Skip to main content

Advertisement

SpringerLink
Log in

Tissue inhibitor of metalloproteinase-1 promotes hematopoietic differentiation via caspase-3 upstream the MEKK1/MEK6/p38α pathway

  • Leading Article
  • Published:
Leukemia Submit manuscript

Abstract

Besides its matrix metalloproteinases inhibitory activity, TIMP-1 exhibits other biological activities such as cell survival and proliferation. The intracellular signalling pathway elicited by TIMP-1 begins to be elucidated. We have shown previously that the caspase-3 and the p38α MAP kinase were activated during TIMP-1-induced UT-7 cells erythroid differentiation. In this study, we demonstrated that TIMP-1 differentiating effect can be extended to the IL-3-dependent myeloid murine 32D cell line and human erythroid progenitors derived from cord blood CD34+ cells. By performing small interfering RNA transfection and using chemical inhibitors, we evidenced that caspase-3 was involved in TIMP-1 differentiating effect. We then identified the MEKK1 kinase as a caspase-3 substrate and demonstrated that the MEKK1/MEK6/p38α pathway was activated downstream the caspase-3 in TIMP-1-induced hematopoietic differentiation.

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

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

References

  1. Gomez DE, Alonso DF, Yoshiji H, Thorgeirsson UP . Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol 1997; 389: 77–81.

    Google Scholar 

  2. Fassina G, Ferrari N, Brigati C, Benelli R, Santi L, Noonan DM et al. Tissue inhibitors of metalloproteases: regulation and biological activities. Clin Exp Metastasis 2000; 18: 111–120.

    Article  CAS  Google Scholar 

  3. Lambert E, Dasse E, Haye B, Petitfrere E . TIMPs as multifacial proteins. Crit Rev Onc Hematol 2004; 49: 187–198.

    Article  Google Scholar 

  4. Hayakawa T, Yamashita K, Kishi J, Harigaya K . Tissue inhibitor of metalloproteinases from human bone marrow stromal cell line KM 102 has erythroid-potentiating activity, suggesting its possibly bifunctional role in the hematopoietic microenvironment. FEBS Lett 1990; 268: 125–128.

    Article  CAS  Google Scholar 

  5. Avalos BR, Kaufman SE, Tomonaga M, Williams RE, Golde DW, Gasson JC . K562 produce and respond to human erythroid-potentiating activity. Blood 1988; 71: 1720–1725.

    CAS  Google Scholar 

  6. Westbrook CA, Gasson JC, Gerber SE, Selsted ME, Golde DW . Purification and characterization of human T-lymphocyte derived erythroid-potentiating activity. J Biol Chem 1984; 259: 9992–9996.

    CAS  Google Scholar 

  7. Hayakawa T, Yamashita K, Tanzawa K, Uchijima E, Iwata K . Growth promoting activity of tissue inhibitor of metalloproteinases-1 (TIMP-1) for a wide range of cells. A possible new growth factor in serum. FEBS Lett 1992; 298: 29–32.

    Article  CAS  Google Scholar 

  8. Obinata M, Yanai N . Cellular and molecular regulation of an erythropoietic inductive microenvironment (EIM). Cell Str Funct 1999; 24: 171–179.

    Article  CAS  Google Scholar 

  9. Zermati Y, Garrido C, Amsellem S, Fishelson S, Bouscary D, Valensi F et al. Caspase activation is required for terminal erythroid differentiation. J Exp Med 2001; 193: 247–254.

    Article  CAS  Google Scholar 

  10. Carlile GW, Smith DH, Wiedmann M . Caspase-3 has a nonapoptotic function in erythroid maturation. Blood 2004; 103: 4310–4316.

    Article  CAS  Google Scholar 

  11. Guedez L, Martinez A, Zhao S, Vivero A, Pittaluga S, Stetler-Stevenson M et al. Tissue inhibitor of metalloproteinase 1 (TIMP-1) promotes plasmablastic differentiation of a Burkitt lymphoma cell line: implications in the pathogenesis of plasmacytic/plasmablastic tumors. Blood 2005; 105: 1660–1668.

    Article  CAS  Google Scholar 

  12. Petitfrere E, Kadri Z, Boudot C, Sowa ML, Mayeux P, Haye B et al. Involvement of the p38 mitogen-activated protein kinase pathway in tissue inhibitor of metalloproteinases-1-induced erythroid differentiation. FEBS Lett 2000; 485: 117–121.

    Article  CAS  Google Scholar 

  13. Uddin S, Ah-Kang J, Ulaszek J, Lahlud D, Wickrema A . Differentiation stage-specific activation of p38 mitogen-activated protein kinase isoforms in primary human erythroid cells. PNAS 2004; 101: 147–152.

    Article  CAS  Google Scholar 

  14. Ono K, Han J . The p38 signal transduction pathway. Activation and function. Cell Signal 2000; 12: 1–13.

    Article  CAS  Google Scholar 

  15. Han J, Lee JD, Jiang Y, Li Z, Feng L, Ulevitch RJ . Characterization of the structure and function of a novel MAP kinase kinase (MKK6). J Biol Chem 1996; 271: 2886–2891.

    Article  CAS  Google Scholar 

  16. Blank JL, Gerwins P, Elliott EM, Sather S, Johnson GL . Molecular cloning of mitogen-activated protein/ERK kinase kinases (MEKK) 2 and 3. Regulation of sequential phosphorylation pathway involving mitogen-activated protein kinase c-Jun Kinase. J Biol Chem 1996; 271: 5361–5368.

    Article  CAS  Google Scholar 

  17. Widman C, Gerwins P, Lassignal Jonhson N, Jarpe MB, Johnson GL . MEK kinase 1, a substrate for DEVD-directed caspases, is involved in genotoxin-induced apoptosis. Mol Cell Biol 1998; 25: 7412–7422.

    Google Scholar 

  18. Alonso G, Ambrosino C, Jones M, Nebreda AR . Differential activation of p38 mitogen-activated protein kinase isoforms depending on signal strength. J Biol Chem 2000; 275: 40641–40648.

    Article  CAS  Google Scholar 

  19. Kadri Z, Maouche-Chretien L, Rooke HM, Orkin SH, Romeo PH, Mayeux P et al. Phosphatidylinositol 3-kinase /Akt induced by erythropoietin renders the erythroid differentiation factor GATA-1 competent for TIMP-1 gene transactivation. Mol Cell Biol 2005; 25: 7412–7422.

    Article  CAS  Google Scholar 

  20. Lambert E, Boudot C, Kadri Z, Soula-Rothhut M, Sowa ML, Mayeux P et al. Tissue inhibitor of metalloproteinases-1 signalling pathway leading to erythroid cell survival. Biochem J 2003; 372: 767–774.

    Article  CAS  Google Scholar 

  21. Haviernik P, Lahoda C, Bradley HL, Hawley TS, Ramezani A, Hawley RG et al. Tissue inhibitor of matrix metalloproteinase-1 overexpression in M1 myeloblasts impairs IL-6-induced differentiation. Oncogene 2004; 23: 9212–9219.

    Article  CAS  Google Scholar 

  22. Sordet O, Rebe C, Plenchette S, Zermati Y, Hermine O, Vainchenker W et al. Specific involvement of caspases in the differentiation of monocytes into macrophages. Blood 2002; 100: 4446–4453.

    Article  CAS  Google Scholar 

  23. Mogi M, Togari A . Activation of caspases is required for osteoblastic differentiation. J Biol Chem 2003; 278: 47477–47482.

    Article  CAS  Google Scholar 

  24. De Botton S, Sabri S, Daugas E, Zermati Y, Guidotti JE, Hermine O et al. Platelet formation is the consequence of caspase activation within megakaryocytes. Blood 2002; 100: 1310–1317.

    Article  CAS  Google Scholar 

  25. Launay S, Hermine O, Fontenay M, Kroemer G, Solary E, Garrido C . Vital functions for lethal caspases. Oncogene 2004; 24: 5137–5148.

    Article  Google Scholar 

  26. Nagata Y, Todokoro K . Requirement of activation of JNK and p38 for environmental stress-induced erythroid differentiation and apoptosis and of inhibition of ERK for apoptosis. Blood 1999; 3: 853–863.

    Google Scholar 

  27. Murate T, Hayakawa T . Multiple functions of tissue inhibitors of metalloproteinases (TIMPs): new aspects in hematopoiesis. Platelets 1999; 10: 5–16.

    Article  CAS  Google Scholar 

  28. Parker CL, Finch RA, Hooper WC . The effect of cytochalasin B on chondrogenesis in chick limb-bud mesoderm cells grown in vitro. In vitro 1978; 14: 606–615.

    Article  CAS  Google Scholar 

  29. Carpentier Y, Mayer P, Bobichon H, Desoize B . Cofactors in in vitro induction of apoptosis in HL60 cells by all-trans retinoic acid (ATRA). Biochem Pharmacol 1998; 55: 177–184.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Ligue Nationale contre le Cancer (Comité de la Haute-Marne).

Author information

Authors and Affiliations

  1. Laboratoire de Biochimie, CNRS 6198, IFR 53 Biomolécules, UFR Sciences Exactes et Naturelles, BP 1039, Université de Reims Champagne Ardenne, Reims, France

    E Dassé, L Bridoux, E Lambert, M L Sowa, L Martiny & E Petitfrère

  2. IPCM 3796, EA, UFR Pharmacie, Reims, France

    T Baranek

  3. Laboratoire de Biologie Cellulaire et Moléculaire, EA 3796, UFR Sciences, Reims, France

    S Salesse

  4. JE 2428, IFR 53 Biomolecules, UFR Pharmacie, Reims, France

    C Trentesaux

Authors
  1. E Dassé
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L Bridoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T Baranek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E Lambert
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S Salesse
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M L Sowa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. L Martiny
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. C Trentesaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. E Petitfrère
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E Petitfrère.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dassé, E., Bridoux, L., Baranek, T. et al. Tissue inhibitor of metalloproteinase-1 promotes hematopoietic differentiation via caspase-3 upstream the MEKK1/MEK6/p38α pathway. Leukemia 21, 595–603 (2007). https://doi.org/10.1038/sj.leu.2404540

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.leu.2404540

  • Springer Nature Limited

Keywords

This article is cited by

Search

Navigation