A subset of bone marrow stromal cells regulate ATP-binding cassette gene expression via insulin-like growth factor-I in a leukemia cell line

Benabbou,Nadia; Mirshahi,Pezhman; Bordu,Camille; Faussat,Anne-Marie; Tang,Ruoping; Therwath,Amu; Soria,Jeannette; Marie,Jean-Pierre; Mirshahi,Massoud

doi:10.3892/ijo.2014.2569

A subset of bone marrow stromal cells regulate ATP-binding cassette gene expression via insulin-like growth factor-I in a leukemia cell line

Authors:
- Nadia Benabbou
- Pezhman Mirshahi
- Camille Bordu
- Anne-Marie Faussat
- Ruoping Tang
- Amu Therwath
- Jeannette Soria
- Jean-Pierre Marie
- Massoud Mirshahi
View Affiliations

Affiliations: UMR, Paris Diderot, Paris 7 University, Lariboisiere Hospital, INSERM U965, Paris, France, Department of Hematology, Saint-Antoine Hospital, Paris, France, Tumor Bank ʻLeukemiaʼ, Saint-Antoine Hospital, Paris, France
Published online on: July 29, 2014 https://doi.org/10.3892/ijo.2014.2569
Pages: 1372-1380
Copyright: © Benabbou et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The importance of the insulin-like growth factor, IGF, as a signaling axis in cancer development, progression and metastasis is highlighted by its effects on cancer cells, notably proliferation and acquired resistance. The role of the microenvironment within which cancer cells evolve and which mediates this effect is far from clear. Here, the involvement of IGF-I in inducing multidrug resistance in a myeloid leukemia cell line, grown in the presence of bone marrow-derived stromal cells called ‘Hospicells’ (BMH), is demonstrated. We found that i) drug sensitive as well as resistant leukemia cells express IGF-I and its receptor IGF-IR. However, the resistant cells were found to secrete high levels of IGF-I. ii) Presence of exogenous IGF-I promoted cell proliferation, which decreased when an inhibitor of IGF-IR (picropodophyllin, PPP) was added. iii) BMH and IGF-I are both involved in the regulation of genes of the ATP binding cassette (ABC) related to resistance development (MDR1, MRP1, MRP2, MRP3 and BCRP). iv) The levels of ABC gene expression by leukemia cells were found to increase in the presence of increasing numbers of BMH. However, these levels decreased when IGF-IR was inhibited by addition of PPP. v) Co-culture of the drug-sensitive leukemia cells with BMH induced protection against the action of daunorubicin. This chemoresistance was amplified by the presence of IGF-I whereas it decreased when IGF-IR was inhibited. Our results underline the role of microenvironment in concert with the IGF-1 pathway in conferring drug resistance to leukemia cells.

View Figures

View References

1	Baudard M, Beauchamp-Nicoud A, Delmer A, Rio B, Blanc C, Zittoun R and Marie JP: Has the prognosis of adult patients with acute myeloid leukemia improved over years? A single institution experience of 784 consecutive patients over a 16-year period. Leukemia. 13:1481–1489. 1999.
2	Rafii A, Mirshahi P, Poupot M, Faussat AM, Simon A, Ducros E, Mery E, Couderc B, Lis R, Capdet J, Bergalet J, Querleu D, Dagonnet F, Fournié JJ, Marie JP, Pujade-Lauraine E, Favre G, Soria J and Mirshahi M: Oncologic trogocytosis of an original stromal cells induces chemoresistance of ovarian tumours. PLoS One. 3:e38942008. View Article : Google Scholar : PubMed/NCBI
3	Lis R, Capdet J, Mirshahi P, Lacroix-Triki M, Dagonnet F, Klein C, Mirshahi M, Fournié JJ, Rafii A and Poupot M: Oncologic trogocytosis with Hospicells induces the expression of N-cadherin by breast cancer cells. Int J Oncol. 37:1453–1461. 2010.PubMed/NCBI
4	Benabbou N, Mirshahi P, Cadillon M, Soria J, Therwath A and Mirshahi M: Hospicells promote upregulation of the ATP binding cassette genes by insulin like growth factor-I via JAK2- STAT3 signaling pathway in ovarian cancer cell line. Int J Oncol. 43:685–694. 2013.PubMed/NCBI
5	Pasquet M, Golzio M, Mery E, Rafii A, Benabbou N, Mirshahi P, Hennebelle I, Bourin P, Allal B, Teissie J, Mirshahi M and Couderc B: Hospicells (ascites-derived stromal cells) promote tumorigenicity and angiogenesis. Int J Cancer. 126:2090–2101. 2010.PubMed/NCBI
6	Martinet L, Poupot R, Mirshahi P, Rafii A, Fournié JJ, Mirshahi M and Poupot M: Hospicells derived from ovarian cancer stroma inhibit T-cell immune responses. Int J Cancer. 126:2143–2152. 2010.PubMed/NCBI
7	Castells M, Thibault B, Mery E, Golzio M, Pasquet M, Hennebelle I, Bourin P, Mirshahi M, Delord JP, Querleu D and Couderc B: Ovarian ascites-derived Hospicells promote angiogenesis via activation of macrophages. Cancer Lett. 326:59–68. 2012. View Article : Google Scholar : PubMed/NCBI
8	Mirshahi P, Rafii A, Vincent L, Berthaut A, Varin R, Kalantar G, Marzac C, Calandini OA, Marie JP, Soria C, Soria J and Mirshahi M: Vasculogenic mimicry of acute leukemic bone marrow stromal cells. Leukemia. 23:1039–1048. 2009. View Article : Google Scholar : PubMed/NCBI
9	Wu X, Tortolero-Luna G, Zhao H, Phatak D, Spitz MR and Follen M: Serum levels of insulin-like growth factor I and risk of squamous intraepithelial lesions of the cervix. Clin Cancer Res. 9:3356–3361. 2003.PubMed/NCBI
10	Yang SY and Winslet M: The IGF system in carcinogenesis and its implication for cancer therapy. Curr Oncol. 18:301–302. 2011.PubMed/NCBI
11	Samani AA, Yakar S, Le Roith D and Brodt P: The role ofhe IGF system in cancer growth and metastasis: overview and recent insights. Endocr Rev. 28:20–47. 2007. View Article : Google Scholar : PubMed/NCBI
12	Héron-Milhavet L and LeRoith D: Insulin-like growth factor I induces MDM2-dependent degradation of p53 via the p38 MAPK pathway in response to DNA damage. J Biol Chem. 277:15600–15606. 2002.PubMed/NCBI
13	He Y, Zhang J, Zheng J, Du W, Xiao H, Liu W, Li X, Chen X, Yang L and Huang S: The insulin-like growth factor-1 receptor kinase inhibitor, NVP-ADW742, suppresses survival and resistance to chemotherapy in acute myeloid leukemia cells. Oncol Res. 19:35–43. 2010. View Article : Google Scholar : PubMed/NCBI
14	Abe S, Funato T, Takahashi S, Yokoyama H, Yamamoto J, Tomiya Y, Yamada-Fujiwara M, Ishizawa K, Kameoka J, Kaku M, Harigae H and Sasaki T: Increased expression of insulin-like growth factor 1 is associated with Ara-C resistance in leukemia. Tohoku J Exp Med. 209:217–228. 2006. View Article : Google Scholar : PubMed/NCBI
15	Kuhn DJ, Berkova Z, Jones RJ, Woessner R, Bjorklund CC, Ma W, Davis RE, Lin P, Wang H, Madden TL, Wei C, Baladandayuthapani V, et al: Targeting the insulin-like growth factor-1 receptor to overcome bortezomib resistance in preclinical models of multiple myeloma. Blood. 120:3260–3270. 2012. View Article : Google Scholar : PubMed/NCBI
16	Guo YS, Jin GF, Houston CW, Thompson JC and Townsend CM Jr: Insulin-like growth factor-I promotes multidrug resistance in MCLM colon cancer cells. J Cell Physiol. 175:141–148. 1998. View Article : Google Scholar : PubMed/NCBI
17	Schwarze CP, Neu S, Beck J, Mavridou K, Ranke MB and Binder G: Influence of IGF-I and cell density on MDR1 expression in the T-lymphoblastoid cell line CCRF-CEM. Horm Res. 52:192–199. 1999. View Article : Google Scholar : PubMed/NCBI
18	Shimon I and Shpilberg O: The insulin-like growth factor system in regulation of normal and malignant hematopoiesis. Leuk Res. 19:233–240. 1995. View Article : Google Scholar : PubMed/NCBI
19	Doepfner KT, Spertini O and Arcaro A: Autocrine insulin-like growth factor-I signaling promotes growth and survival of human acute myeloid leukemia cells via the phosphoinositide 3-kinase/Akt pathway. Leukemia. 21:1921–1930. 2007. View Article : Google Scholar : PubMed/NCBI
20	Baier TG, Jenne EW, Blum W, Schönberg D and Hartmann KK: Influence of antibodies against IGF-I, insulin or their receptors on proliferation of human acute lymphoblastic leukemia cell lines. Leuk Res. 16:807–814. 1992. View Article : Google Scholar : PubMed/NCBI
21	Gilmore MJ, Prentice HG, Blacklock HA, Janossy G and Hoffbrand AV: A technique for rapid isolation of bone marrow mononuclear cells using Ficoll-Metrizoate and the IBM 2991 blood cell processor. Br J Haematol. 50:619–626. 1982. View Article : Google Scholar : PubMed/NCBI
22	Girnita A, Girnita L, del Prete F, Bartolazzi A, Larsson O and Axelson M: Cyclolignans as inhibitors of the insulin-like growth factor-1 receptor and malignant cell growth. Cancer Res. 64:236–242. 2004. View Article : Google Scholar : PubMed/NCBI
23	Qiang YW, Kopantzev E and Rudikoff S: Insulin like growth factor-I signaling in multiple myeloma: downstream elements, functional correlates, and pathway cross-talk. Blood. 99:4138–4146. 2002. View Article : Google Scholar : PubMed/NCBI
24	Rodon J, DeSantos V, Ferry RJ Jr and Kurzrock R: Early drug development of inhibitors of the insulin-like growth factor-I receptor pathway: lessons from the first clinical trials. Mol Cancer Ther. 7:2575–2588. 2008. View Article : Google Scholar : PubMed/NCBI
25	Gregory CW, DeGeorges A and Sikes RA: The IGF axis in the development and progression of prostate cancer. Recent Res Dev Cancer. 3:437–462. 2001.
26	Macaulay VM: Insulin-like growth factors and cancer. Br J Cancer. 65:311–320. 1992. View Article : Google Scholar : PubMed/NCBI
27	Burren CP, Berka JL, Edmondson SR, Werther GA and Batch JA: Localization of mRNAs for insulin-like growth factor-I (IGF-I), IGF-I receptor, and IGF binding proteins in rat eye. Invest Ophthalmol Vis Sci. 37:1459–1468. 1996.PubMed/NCBI
28	Clemmons DR and Maile LA: Integral membrane proteins that function coordinately with the insulin-like growth factor I receptor to regulate intracellular signaling. Endocrinology. 144:1664–1670. 2003. View Article : Google Scholar
29	Turner HE, Harris AL, Melmed S and Wass JA: Angiogenesis in endocrine tumors. Endocr Rev. 24:600–632. 2003. View Article : Google Scholar : PubMed/NCBI
30	Wu KD, Zhou L, Burtrum D, Ludwig DL and Moore MA: Antibody targeting of the insulin like growth factor I receptor enhances the anti-tumor response of multiple myeloma to chemotherapy through inhibition of tumor proliferation and angiogenesis. Cancer Immunol Immunother. 56:343–357. 2007.
31	Karamouzis MV and Papavassiliou AG: Targeting insulin-like growth factor in breast cancer therapeutics. Crit Rev Oncol Hematol. 84:8–17. 2012. View Article : Google Scholar : PubMed/NCBI
32	Hopkins A, Crowe PJ and Yang JL: Effect of type 1 insulin-like growth factor receptor targeted therapy on chemotherapy in human cancer and the mechanisms involved. J Cancer Res Clin Oncol. 136:639–650. 2010. View Article : Google Scholar : PubMed/NCBI