K562 chronic myeloid leukemia cells modify osteogenic differentiation and gene expression of bone marrow stromal cells

Arnulf B, Lecourt S, Soulier J, Ternaux B, Lacassagne MN, Crinquette A, Dessoly J, Sciaini AK, Benbunan M, Chomienne C, Fermand JP, Marolleau JP, Larghero J (2007) Phenotypic and functional characterization of bone marrow mesenchymal stem cells derived from patients with multiple myeloma. Leukemia 21(1):158–163. https://doi.org/10.1038/sj.leu.2404466

Blau O, Baldus CD, Hofmann WK, Thiel G, Nolte F, Burmeister T, Turkmen S, Benlasfer O, Schumann E, Sindram A, Molkentin M, Mundlos S, Keilholz U, Thiel E, Blau IW (2011) Mesenchymal stromal cells of myelodysplastic syndrome and acute myeloid leukemia patients have distinct genetic abnormalities compared with leukemic blasts. Blood 118(20):5583–5592. https://doi.org/10.1182/blood-2011-03-343467

Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425(6960):841–846. https://doi.org/10.1038/nature02040

Campioni D, Rizzo R, Stignani M, Melchiorri L, Ferrari L, Moretti S, Russo A, Bagnara GP, Bonsi L, Alviano F, Lanzoni G, Cuneo A, Baricordi OR, Lanza F (2009) A decreased positivity for CD90 on human mesenchymal stromal cells (MSCs) is associated with a loss of immunosuppressive activity by MSCs. Cytometry B Clin Cytom 76B(3):225–230. https://doi.org/10.1002/cyto.b.20461

Chang J, Liu F, Lee M, Wu BJM, Ting K, Zara JN, Soo C, Al Hezaimi K, Zou WP, Chen XH, Mooney DJ, Wang CY (2013) NF-kappa B inhibits osteogenic differentiation of mesenchymal stem cells by promoting beta-catenin degradation. Proc Natl Acad Sci U S A 110(23):9469–9474. https://doi.org/10.1073/pnas.1300532110

Civini S, Jin P, Ren JQ, Sabatino M, Castiello L, Jin JJ, Wang H, Zhao YL, Marincola F, Stroncek D (2013) Leukemia cells induce changes in human bone marrow stromal cells. J Transl Med 11. https://doi.org/10.1186/1479-5876-11-298

Geyh S, Rodriguez-Paredes M, Jager P, Khandanpour C, Cadeddu RP, Gutekunst J, Wilk CM, Fenk R, Zilkens C, Hermsen D, Germing U, Kobbe G, Lyko F, Haas R, Schroeder T (2016) Functional inhibition of mesenchymal stromal cells in acute myeloid leukemia. Leukemia 30(3):683–691. https://doi.org/10.1038/leu.2015.325

Giallongo C, Romano A, Parrinello NL, La Cava P, Brundo MV, Bramanti V, Stagno F, Vigneri P, Chiarenza A, Palumbo GA, Tibullo D, Di Raimondo F (2016) Mesenchymal stem cells (MSC) regulate activation of granulocyte-like myeloid derived suppressor cells (G-MDSC) in chronic myeloid leukemia patients. PLoS One 11(7). https://doi.org/10.1371/journal.pone.0158392

Huang JC, Basu SK, Zhao X, Chien S, Fang M, Oehler VG, Appelbaum FR, Becker PS (2015) Mesenchymal stromal cells derived from acute myeloid leukemia bone marrow exhibit aberrant cytogenetics and cytokine elaboration. Blood Cancer J 5. https://doi.org/10.1038/bcj.2015.17

Jaganathan BG, Tisato V, Vulliamy T, Dokal I, Marsh J, Dazzi F, Bonnet D (2010) Effects of MSC co-injection on the reconstitution of aplastic anemia patient following hematopoietic stem cell transplantation. Leukemia 24(10):1791–1795. https://doi.org/10.1038/leu.2010.164

Kang K, Ma RL, Cai WF, Huang W, Paul C, Liang JL, Wang YH, Zhao TJ, Kim HW, Xu MF, Millard RW, Wen ZL, Wang YG (2015) Exosomes secreted from CXCR4 overexpressing mesenchymal stem cells promote cardioprotection via Akt signaling pathway following myocardial infarction. Stem Cells Int. https://doi.org/10.1155/2015/659890

Kode A, Manavalan JS, Mosialou I, Bhagat G, Rathinam CV, Luo N, Khiabanian H, Lee A, Murty VV, Friedman R, Brum A, Park D, Galili N, Mukherjee S, Teruya-Feldstein J, Raza A, Rabadan R, Berman E, Kousteni S (2014) Leukaemogenesis induced by an activating beta-catenin mutation in osteoblasts. Nature 506(7487):240–244. https://doi.org/10.1038/nature12883

Kode A, Mosialou I, Manavalan SJ, Rathinam CV, Friedman RA, Teruya-Feldstein J, Bhagat G, Berman E, Kousteni S (2016) FoxO1-dependent induction of acute myeloid leukemia by osteoblasts in mice. Leukemia 30(1):1–13. https://doi.org/10.1038/leu.2015.161

Krause DS, Scadden DT (2015) A hostel for the hostile: the bone marrow niche in hematologic neoplasms. Haematologica 100(11):1376–1387. https://doi.org/10.3324/heamatol.2014.113852

Krevvata M, Silva BC, Manavalan JS, Galan-Diez M, Kode A, Matthews BG, Park D, Zhang CA, Galili N, Nickolas TL, Dempster DW, Dougall W, Teruya-Feldstein J, Economides AN, Kalajzic I, Raza A, Berman E, Mukherjee S, Bhagat G, Kousteni S (2014) Inhibition of leukemia cell engraftment and disease progression in mice by osteoblasts. Blood 124(18):2834–2846. https://doi.org/10.1182/blood-2013-07-517219

Kumar A, Bhanja A, Bhattacharyya J, Jaganathan BG (2016) Multiple roles of CD90 in cancer. Tumour Biol. https://doi.org/10.1007/s13277-016-5112-0

Kumar A, Bhattacharyya J, Jaganathan BG (2017) Adhesion to stromal cells mediates imatinib resistance in chronic myeloid leukemia through ERK and BMP signaling pathways. Sci Rep 7(1):9535. https://doi.org/10.1038/s41598-017-10373-3

Levesque JP, Helwani FM, Winkler IG (2010) The endosteal 'osteoblastic' niche and its role in hematopoietic stem cell homing and mobilization. Leukemia 24(12):1979–1992. https://doi.org/10.1038/leu.2010.214

Lo Celso C, Scadden DT (2011) The haematopoietic stem cell niche at a glance. J Cell Sci 124(21):3529–3535. https://doi.org/10.1242/jcs.074112

Lopez AV, Garcia MNV, Melen GJ, Martinez AE, Moreno IC, Garcia-Castro J, Orellana MR, Gonzalez AGZ (2014) Mesenchymal stromal cells derived from the bone marrow of acute lymphoblastic leukemia patients show altered bmp4 production: correlations with the course of disease. PLoS One 9(1). https://doi.org/10.1371/journal.pone.0084496

Martinaud C, Desterke C, Konopacki J, Pieri L, Torossian F, Golub R, Schmutz S, Anginot A, Guerton B, Rochet N, Albanese P, Henault E, Pierre-Louis O, Souraud JB, de Revel T, Dupriez B, Ianotto JC, Bourgeade MF, Vannucchi AM, Lataillade JJ, Le Bousse-Kerdiles MC (2015) Osteogenic potential of mesenchymal stromal cells contributes to primary myelofibrosis. Cancer Res 75(22):4753–4765. https://doi.org/10.1158/0008-5472.CAN-14-3696

Mawrie D, Kumar A, Magdalene D, Bhattacharyya J, Jaganathan BG (2016) Mesenchymal stem cells from human extra ocular muscle harbor neuroectodermal differentiation potential. PLoS One 11(6). https://doi.org/10.1371/journal.pone.0156697

Morrison SJ, Scadden DT (2014) The bone marrow niche for haematopoietic stem cells. Nature 505(7483):327–334. https://doi.org/10.1038/nature12984

Nievergall E, Reynolds J, Kok CH, Watkins D, Biondo M, Busfield SJ, Vairo G, Yeung DT, Lopez A, Hiwase DK, White DL, Hughes TP (2014) High plasma levels of tgf-alpha and IL-6 at diagnosis predict early molecular response failure and transformation in CML. Blood 124(21):1788

Pricola KL, Kuhn NZ, Haleem-Smith H, Song YJ, Tuan RS (2009) Interleukin-6 maintains bone marrow-derived mesenchymal stem cell stemness by an ERK1/2-dependent mechanism. J Cell Biochem 108(3):577–588. https://doi.org/10.1002/jcb.22289

Raaijmakers MHGP, Mukherjee S, Guo SQ, Zhang SY, Kobayashi T, Schoonmaker JA, Ebert BL, Al-Shahrour F, Hasserjian RP, Scadden EO, Aung Z, Matza M, Merkenschlager M, Lin C, Rommens JM, Scadden DT (2010) Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature 464(7290):852–U858. https://doi.org/10.1038/nature08851

Saini AS, Shenoy GN, Rath S, Bal V, George A (2014) Inducible nitric oxide synthase is a major intermediate in signaling pathways for the survival of plasma cells. Nat Immunol 15(3):275–282. https://doi.org/10.1038/ni.2806

Schmidt T, Kharabi Masouleh B, Loges S, Cauwenberghs S, Fraisl P, Maes C, Jonckx B, De Keersmaecker K, Kleppe M, Tjwa M, Schenk T, Vinckier S, Fragoso R, De Mol M, Beel K, Dias S, Verfaillie C, Clark RE, Brummendorf TH, Vandenberghe P, Rafii S, Holyoake T, Hochhaus A, Cools J, Karin M, Carmeliet G, Dewerchin M, Carmeliet P (2011) Loss or inhibition of stromal-derived PlGF prolongs survival of mice with imatinib-resistant Bcr-Abl1(+) leukemia. Cancer Cell 19(6):740–753. https://doi.org/10.1016/j.ccr.2011.05.007

Schroeder T, Geyh S, Germing U, Haas R (2016) Mesenchymal stromal cells in myeloid malignancies. Blood Res 51(4):225–232

Semesiuk NI, Zhylchuk A, Bezdenezhnykh N, Lykhova A, Vorontsova AL, Zhylchuk VE, Kudryavets YI (2013) Disseminated tumor cells and enhanced level of some cytokines in bone marrow and peripheral blood of breast cancer patients as predictive factors of tumor progression. Exp Oncol 35(4):295–302

Somaiah C, Kumar A, Mawrie D, Sharma A, Patil SD, Bhattacharyya J, Swaminathan R, Jaganathan BG (2015) Collagen promotes higher adhesion, survival and proliferation of mesenchymal stem cells. PLoS One 10(12). https://doi.org/10.1371/journal.pone.0145068

Sonowal H, Kumar A, Bhattacharyya J, Gogoi PK, Jaganathan BG (2013) Inhibition of actin polymerization decreases osteogeneic differentiation of mesenchymal stem cells through p38 MAPK pathway. J Biomed Sci 20. https://doi.org/10.1186/1423-0127-20-71

Traer E, Javidi-Sharifi N, Agarwal A, Dunlap J, English I, Martinez J, Tyner JW, Wong M, Druker BJ (2014) Ponatinib overcomes FGF2-mediated resistance in CML patients without kinase domain mutations. Blood 123(10):1516–1524. https://doi.org/10.1182/blood-2013-07-518381

Wallace SR, Oken MM, Lunetta KL, Panoskaitsis-Mortari A, Masellis AM (2001) Abnormalities of bone marrow mesenchymal cells in multiple myeloma patients. Cancer 91(7):1219–1230. https://doi.org/10.1002/1097-0142(20010401)91:7<1219::Aid-Cncr1122>3.0.Co;2-1

Wohrer S, Rabitsch W, Shehata M, Kondo R, Esterbauer H, Streubel B, Sillaber C, Raderer M, Jaeger U, Zielinski C, Valent P (2007) Mesenchymal stem cells in patients with chronic myelogenous leukaemia or bi-phenotypic ph plus acute leukaemia are not related to the leukaemic clone. Anticancer Res 27(6B):3837–3841

Xu S, Evans H, Buckle C, De Veirman K, Hu J, Xu D, Menu E, De Becker A, Broek IV, Leleu X, Camp BV, Croucher P, Vanderkerken K, Van Riet I (2012) Impaired osteogenic differentiation of mesenchymal stem cells derived from multiple myeloma patients is associated with a blockade in the deactivation of the Notch signaling pathway. Leukemia 26(12):2546–2549. https://doi.org/10.1038/leu.2012.126

Zhang JW, Niu C, Ye L, Huang HY, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li LH (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425(6960):836–841. https://doi.org/10.1038/nature02041

Zhang B, Ho YW, Huang Q, Maeda T, Lin A, Lee SU, Hair A, Holyoake TL, Huettner C, Bhatia R (2012) Altered microenvironmental regulation of leukemic and normal stem cells in chronic myelogenous leukemia. Cancer Cell 21(4):577–592. https://doi.org/10.1016/j.ccr.2012.02.018