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Review

Vacuolar ATPase as a possible therapeutic target in human acute myeloid leukemia

, , &
Pages 13-24 | Received 31 Aug 2017, Accepted 16 Nov 2017, Published online: 23 Nov 2017

References

  • Arber DA, Orazi A, Hasserjian R, et al. The 2016 revision to the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia. Blood. 2016;127(20);2391–2405.
  • Döhner H, Estey E, Grimwade D, et al. Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood. 2017;129(4):424–447.
  • Stein EM, DiNardo CD, Pollyea DA, et al. Enasidenib in mutant IDH2 relapsed or refractory acute myeloid leukemia. Blood. 2017;130(6):722–731.
  • Pemmaraju N, Kantarjian H, Garcia-Manero G, et al. Improving outcomes for patients with acute myeloid leukemia in first relapse: a single center experience. Am J Hematol. 2015;90(1):27–30.
  • Stransky L, Cotter K, Forgac M. The function of V-ATPases in cancer. Physiol Rev. 2016;96(3):1071–1091.
  • Spugnini EP, Sonveaux P, Stock C, et al. Proton channels and exchangers in cancer. Biochim Biophys Acta. 2015;1848(10 Pt B):2715–2726.
  • Lee YY, Jeon HK, Hong JE, et al. Proton pump inhibitors enhance the effects of cytotoxic agents in chemoresistant epithelial ovarian carcinoma. Oncotarget. 2015;6(33):35040–35050.
  • Fan S, Niu Y, Tan N, et al. LASS2 enhances chemosensitivity of breast cancer by counteracting acidic tumor microenvironment through inhibiting activity of V-ATPase proton pump. Oncogene. 2013;32(13):1682–1690.
  • Graham RM, Thompson JW, Webster KA. Inhibition of the vacuolar ATPase induces Bnip3-dependent death of cancer cells and a reduction in tumor burden and metastasis. Oncotarget. 2014;5(5):1162–1173.
  • Hamm R, Zeino M, Frewert S, et al. Up-regulation of cholesterol associated genes as novel resistance mechanism in glioblastoma cells in response to archazolid B. Toxicol Appl Pharmacol. 2014;281(1):78–86.
  • Zhao J, Benlekbir S, Rubinstein JL. Electron cryomicroscopy observation of rotational states in a eukaryotic V-ATPase. Nature. 2015;521(7551):241–245.
  • Couoh-Cardel S, Milgrom E, Wilkens S. Affinity purification and structural features of the yeast vacuolar ATPase vo membrane sector. J Biol Chem. 2015;290(46):27959–27971.
  • Mazhab-Jafari MT, Rohou A, Schmidt C, et al. Atomic model for the membrane-embedded VO motor of a eukaryotic V-ATPase. Nature. 2016;539(7627):118–122.
  • Merkulova M, Paunescu TG, Azroyan A, et al. Mapping the H(+) (V)-ATPase interactome: identification of proteins involved in trafficking, folding, assembly and phosphorylation. Sci Rep. 2015;5:14827.
  • Brenner AK, Tvedt TH, Nepstad I, et al. Patients with acute myeloid leukemia can be subclassified based on the constitutive cytokine release of the leukemic cells; the possible clinical relevance and the importance of cellular iron metabolism. Expert Opin Ther Targets. 2017;21(4):357–369.
  • Honnemyr M, Bruserud Ø, Brenner AK. The constitutive protease release by primary human acute myeloid leukemia cells. J Cancer Res Clin Oncol. 2017;143(10):1985–1998.
  • Hartl FU, Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science. 2002;295(5561):1852–1858.
  • Roh SH, Kasembeli M, Bakthavatsalam D, et al. Contribution of the Type II Chaperonin, TRiC/CCT, to Oncogenesis. Int J Mol Sci. 2015;16(11):26706–26720.
  • Lopez T, Dalton K, Frydman J. The mechanism and function of Group II chaperonins. J Mol Biol. 2015;427(18):2919–2930.
  • Roh SH, Kasembeli M, Galaz-Montoya JG, et al. Chaperonin TRiC/CCT modulates the folding and activity of leukemogenic fusion oncoprotein AML1-ETO. J Biol Chem. 2016;291(9):4732–4741.
  • Bruserud Ø, Nepstad I, Hauge M, et al. STAT3 as a possible therapeutic target in human malignancies: lessons from acute myeloid leukemia. Expert Rev Hematol. 2015;8(1):29–41.
  • Hatfield KJ, Bedringsaas SL, Ryningen A, et al. Hypoxia increases HIF-1alpha expression and constitutive cytokine release by primary human acute myeloid leukaemia cells. Eur Cytokine Netw. 2010;21(3):154–164.
  • Anensen N, Hjelle SM, Van Belle W, et al. Correlation analysis of p53 protein isoforms with NPM1/FLT3 mutations and therapy response in acute myeloid leukemia. Oncogene. 2012;31(12):1533–1545.
  • Brenner AK, Reikvam H, Lavecchia A, et al. Therapeutic targeting the cell division cycle 25 (CDC25) phosphatases in human acute myeloid leukemia–the possibility to target several kinases through inhibition of the various CDC25 isoforms. Molecules. 2014;19(11):18414–18447.
  • Konopleva M, Milella M, Ruvolo P, et al. MEK inhibition enhances ABT-737-induced leukemia cell apoptosis via prevention of ERK-activated MCL-1 induction and modulation of MCL-1/BIM complex. Leukemia. 2012;26(4):778–787.
  • Wermke M, Camgoz A, Paszkowski-Rogacz M, et al. RNAi profiling of primary human AML cells identifies ROCK1 as a therapeutic target and nominates fasudil as an antileukemic drug. Blood. 2015;125(24):3760–3768.
  • Salem M, Delwel R, Touw I, et al. Human AML colony growth in serum-free culture. Leuk Res. 1988;12(2):157–165.
  • Paolillo R, Spinello I, Mt Q, et al. Human TM9SF4 is a new gene down-regulated by hypoxia and involved in cell adhesion of leukemic cells. PLoS One. 2015;10(5):e0126968.
  • Bernhard SM, Seidel K, Schmitz J, et al. The (pro)renin receptor ((P)RR) can act as a repressor of Wnt signalling. Biochem Pharmacol. 2012;84(12):1643–1650.
  • Pamarthy S, Jaiswal MK, Kulshreshtha A, et al. The Vacuolar ATPase a2-subunit regulates Notch signaling in triple-negative breast cancer cells. Oncotarget. 2015;6(33):34206–34220.
  • Brenner AK, Andersson Tvedt TH, Bruserud Ø. The complexity of targeting PI3K-Akt-mTOR signalling in human acute myeloid leukaemia: the importance of leukemic cell heterogeneity, neighbouring mesenchymal stem cells and immunocompetent cells. Molecules. 2016;21(11):1512.
  • Stransky LA, Forgac M. Amino acid availability modulates vacuolar H+-ATPase assembly. J Biol Chem. 2015;290(45):27360–27369.
  • Sharma M, Astekar M, Soi S, et al. pH gradient reversal: an emerging hallmark of cancers. Recent Pat Anticancer Drug Discov. 2015;10(3):244–258.
  • Webb BA, Chimenti M, Jacobson MP, et al. Dysregulated pH: a perfect storm for cancer progression. Nat Rev Cancer. 2011;11(9):671–677.
  • De Milito A, Canese R, Marino ML, et al. pH-dependent antitumor activity of proton pump inhibitors against human melanoma is mediated by inhibition of tumor acidity. Int J Cancer. 2010;127(1):207–219.
  • Marino ML, Fais S, Djavaheri-Mergny M, et al. Proton pump inhibition induces autophagy as a survival mechanism following oxidative stress in human melanoma cells. Cell Death Dis. 2010;1:e87.
  • Von Schwarzenberg K, Wiedmann RM, Oak P, et al. Mode of cell death induction by pharmacological vacuolar H+-ATPase (V-ATPase) inhibition. J Biol Chem. 2013;288(2):1385–1396.
  • Horova V, Hradilova N, Jelinkova I, et al. Inhibition of vacuolar ATPase attenuates the TRAIL-induced activation of caspase-8 and modulates the trafficking of TRAIL receptosomes. Febs J. 2013;280(14):3436–3450.
  • Reikvam H, Hauge M, Brenner AK, et al. Emerging therapeutic targets for the treatment of human acute myeloid leukemia (part 1) - gene transcription, cell cycle regulation, metabolism and intercellular communication. Expert Rev Hematol. 2015;8(3):299–313.
  • Tvedt TH, Nepstad I, Bruserud Ø. Antileukemic effects of midostaurin in acute myeloid leukemia - the possible importance of multikinase inhibition in leukemic as well as nonleukemic stromal cells. Expert Opin Investig Drugs. 2017;26(3):343–355.
  • Brenner AK, Reikvam H, Bruserud Ø. A subset of patients with acute myeloid leukemia has leukemia cells characterized by chemokine responsiveness and altered expression of transcriptional as well as angiogenic regulators. Front Immunol. 2016;7:205.
  • Reikvam H, Brenner AK, Hagen KM, et al. The cytokine-mediated crosstalk between primary human acute myeloid cells and mesenchymal stem cells alters the local cytokine network and the global gene expression profile of the mesenchymal cells. Stem Cell Res. 2015;15(3):530–541.
  • Lynch JR, Wang JY. G protein-coupled receptor signaling in stem cells and cancer. Int J Mol Sci. 2016;17(5):707.
  • Brenner AK, Nepstad I, Bruserud Ø. Mesenchymal stem cells support survival and proliferation of primary human acute myeloid leukemia cells through heterogeneous molecular mechanisms. Front Immunol. 2017;8:106.
  • Bruserud Ø, Aasebø E, Hernandez-Valladares M, et al. Therapeutic targeting of leukemic stem cells in acute myeloid leukemia - the biological background for possible strategies. Expert Opin Drug Discov. 2017;12(10):1053–1065.
  • Zhou HS, Carter BZ, Andreeff M. Bone marrow niche-mediated survival of leukemia stem cells in acute myeloid leukemia: Yin and Yang. Cancer Biol Med. 2016;13(2):248–259.
  • Sadras T, Perugini M, Kok CH, et al. Interleukin-3-mediated regulation of beta-catenin in myeloid transformation and acute myeloid leukemia. J Leukoc Biol. 2014;96(1):83–91.
  • Despeaux M, Chicanne G, Rouer E, et al. Focal adhesion kinase splice variants maintain primitive acute myeloid leukemia cells through altered Wnt signaling. Stem Cells. 2012;30(8):1597–1610.
  • Kuhn K, Cott C, Bohler S, et al. The interplay of autophagy and beta-Catenin signaling regulates differentiation in acute myeloid leukemia. Cell Death Discov. 2015;1:15031.
  • Griffiths EA, Golding MC, Srivastava P, et al. Pharmacological targeting of beta-catenin in normal karyotype acute myeloid leukemia blasts. Haematologica. 2015;100(2):e49–52.
  • Lobry C, Oh P, Mansour MR, et al. Notch signaling: switching an oncogene to a tumor suppressor. Blood. 2014;123(16):2451–2459.
  • Kannan S, Sutphin RM, Hall MG, et al. Notch activation inhibits AML growth and survival: a potential therapeutic approach. J Exp Med. 2013;210(2):321–337.
  • Lobry C, Ntziachristos P, Ndiaye-Lobry D, et al. Notch pathway activation targets AML-initiating cell homeostasis and differentiation. J Exp Med. 2013;210(2):301–319.
  • Takam Kamga P, Bassi G, Cassaro A, et al. Notch signalling drives bone marrow stromal cell-mediated chemoresistance in acute myeloid leukemia. Oncotarget. 2016;7(16):21713–21727.
  • Zhang J, Ye J, Ma D, et al. Cross-talk between leukemic and endothelial cells promotes angiogenesis by VEGF activation of the Notch/Dll4 pathway. Carcinogenesis. 2013;34(3):667–677.
  • Reikvam H, Tamburini J, Skrede S, et al. Antileukaemic effect of PI3K-mTOR inhibitors in acute myeloid leukaemia-gene expression profiles reveal CDC25B expression as determinate of pharmacological effect. Br J Haematol. 2014;164(2):200–211.
  • Reikvam H, Nepstad I, Bruserud Ø, et al. Pharmacological targeting of the PI3K/mTOR pathway alters the release of angioregulatory mediators both from primary human acute myeloid leukemia cells and their neighboring stromal cells. Oncotarget. 2013;4(6):830–843.
  • Xie C, He Y, Zhen M, et al. Puquitinib, a novel orally available PI3Kdelta inhibitor, exhibits potent antitumor efficacy against acute myeloid leukemia. Cancer Sci. 2017;108(7):1476–1484.
  • Ragon BK, Kantarjian H, Jabbour E, et al. Buparlisib, a PI3K inhibitor, demonstrates acceptable tolerability and preliminary activity in a phase I trial of patients with advanced leukemias. Am J Hematol. 2017;92(1):7–11.
  • Tan P, Tiong IS, Fleming S, et al. The mTOR inhibitor everolimus in combination with azacitidine in patients with relapsed/refractory acute myeloid leukemia: a phase Ib/II study. Oncotarget. 2017;8(32):52269–52280.
  • Zeng Z, Liu W, Tsao T, et al. High-throughput profiling of signaling networks identifies mechanism-based combination therapy to eliminate microenvironmental resistance in acute myeloid leukemia. Haematologica. 2017;102(9):1537–1548.
  • Aasebo E, Vaudel M, Mjaavatten O, et al. Performance of super-SILAC based quantitative proteomics for comparison of different acute myeloid leukemia (AML) cell lines. Proteomics. 2014;14(17–18):1971–1976.
  • Kaufmann SH, Steensma DP. On the TRAIL of a new therapy for leukemia. Leukemia. 2005;19(12):2195–2202.
  • Zhe N, Chen S, Zhou Z, et al. HIF-1alpha inhibition by 2-methoxyestradiol induces cell death via activation of the mitochondrial apoptotic pathway in acute myeloid leukemia. Cancer Biol Ther. 2016;17(6):625–634.
  • Vukovic M, Guitart AV, Sepulveda C, et al. Hif-1alpha and Hif-2alpha synergize to suppress AML development but are dispensable for disease maintenance. J Exp Med. 2015;212(13):2223–2234.
  • Folkerts H, Hilgendorf S, Wierenga ATJ, et al. Inhibition of autophagy as a treatment strategy for p53 wild-type acute myeloid leukemia. Cell Death Dis. 2017;8(7):e2927.
  • Chen L, Guo P, Zhang Y, et al. Autophagy is an important event for low-dose cytarabine treatment in acute myeloid leukemia cells. Leuk Res. 2017;60:44–52.
  • Piya S, Kornblau SM, Ruvolo VR, et al. Atg7 suppression enhances chemotherapeutic agent sensitivity and overcomes stroma-mediated chemoresistance in acute myeloid leukemia. Blood. 2016;128(9):1260–1269.
  • Zhang S, Schneider LS, Vick B, et al. Anti-leukemic effects of the V-ATPase inhibitor Archazolid A. Oncotarget. 2015;6(41):43508–43528.
  • Greijer AE, van der Wall E. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J Clin Pathol. 2004;57(10):1009–1014.
  • Koshiji M, Huang LE. Dynamic balancing of the dual nature of HIF-1alpha for cell survival. Cell Cycle. 2004;3(7):853–854.
  • Sermeus A, Michiels C. Reciprocal influence of the p53 and the hypoxic pathways. Cell Death Dis. 2011;2:e164.
  • Fridman JS, Lowe SW. Control of apoptosis by p53. Oncogene. 2003;22(56):9030–9040.
  • Schneider LS, von Schwarzenberg K, Lehr T, et al. Vacuolar-ATPase inhibition blocks iron metabolism to mediate therapeutic effects in breast cancer. Cancer Res. 2015;75(14):2863–2874.
  • Zhang L, McGraw KL, Sallman DA, et al. The role of p53 in myelodysplastic syndromes and acute myeloid leukemia: molecular aspects and clinical implications. Leuk Lymphoma. 2017;58(8):1777–1790.
  • Bruserud Ø, Frostad S, Foss B. In vitro culture of acute myelogenous leukemia blasts: a comparison of four different culture media. J Hematother. 1999;8(1):63–73.
  • Frostad S, Bjerknes R, Abrahamsen JF, et al. Insulin-like growth factor-1 (IGF-1) has a costimulatory effect on proliferation of committed progenitors derived from human umbilical cord CD34+ cells. Stem Cells (Dayton, Ohio). 1998;16(5):334–342.
  • Andrews NC. Molecular control of iron metabolism. Best practice & research. Clin Haematol. 2005;18(2):159–169.
  • Roth M, Will B, Simkin G, et al. Eltrombopag inhibits the proliferation of leukemia cells via reduction of intracellular iron and induction of differentiation. Blood. 2012;120(2):386–394.
  • Wang SJ, Gao C, Chen BA. Advancement of the study on iron metabolism and regulation in tumor cells. Chin J Cancer. 2010;29(4):451–455.
  • Weiss G. Modification of iron regulation by the inflammatory response. Best practice & research. Clin Haematol. 2005;18(2):183–201.
  • Torti SV, Torti FM. Iron and cancer: more ore to be mined. Nat Rev Cancer. 2013;13(5):342–355.
  • Bruserud Ø, Ryningen A, Olsnes AM, et al. Subclassification of patients with acute myelogenous leukemia based on chemokine responsiveness and constitutive chemokine release by their leukemic cells. Haematologica. 2007;92(3):332–341.
  • Miller LD, Coffman LG, Chou JW, et al. An iron regulatory gene signature predicts outcome in breast cancer. Cancer Res. 2011;71(21):6728–6737.
  • Chirasani SR, Markovic DS, Synowitz M, et al. Transferrin-receptor-mediated iron accumulation controls proliferation and glutamate release in glioma cells. J Mol Med (Berl). 2009;87(2):153–167.
  • Peréz MJ, Fernandez N, Pasquini JM. Oligodendrocyte differentiation and signaling after transferrin internalization: a mechanism of action. Exp Neurol. 2013;248:262–274.
  • Bruserud Ø, Ryningen A, Wergeland L, et al. Osteoblasts increase proliferation and release of pro-angiogenic interleukin 8 by native human acute myelogenous leukemia blasts. Haematologica. 2004;89(4):391–402.
  • Hatfield K, Ryningen A, Corbascio M, et al. Microvascular endothelial cells increase proliferation and inhibit apoptosis of native human acute myelogenous leukemia blasts. Int J Cancer. 2006;119(10):2313–2321.
  • Hindenburg AA, Gervasoni JE Jr, Krishna S, et al. Intracellular distribution and pharmacokinetics of daunorubicin in anthracycline-sensitive and -resistant HL-60 cells. Cancer Res. 1989;49(16):4607–4614.
  • Liao C, Hu B, Arno MJ, et al. Genomic screening in vivo reveals the role played by vacuolar H+ ATPase and cytosolic acidification in sensitivity to DNA-damaging agents such as cisplatin. Mol Pharmacol. 2007;71(2):416–425.
  • Marquardt D, Center MS. Involvement of vacuolar H(+)-adenosine triphosphatase activity in multidrug resistance in HL60 cells. J Natl Cancer Inst. 1991;83(15):1098–1102.
  • Torigoe T, Izumi H, Ishiguchi H, et al. Enhanced expression of the human vacuolar H+-ATPase c subunit gene (ATP6L) in response to anticancer agents. J Biol Chem. 2002;277(39):36534–36543.
  • Saito T, Schlegel R, Andresson T, et al. Induction of cell transformation by mutated 16K vacuolar H+-atpase (ductin) is accompanied by down-regulation of gap junctional intercellular communication and translocation of connexin 43 in NIH3T3 cells. Oncogene. 1998;17(13):1673–1680.
  • Krysiak K, Gomez F, White BS, et al. Recurrent somatic mutations affecting B-cell receptor signaling pathway genes in follicular lymphoma. Blood. 2017;129(4):473–483.
  • Okosun J, Wolfson RL, Wang J, et al. Recurrent mTORC1-activating RRAGC mutations in follicular lymphoma. Nat Genet. 2016;48(2):183–188.
  • Gottlieb RA, Giesing HA, Zhu JY, et al. Cell acidification in apoptosis: granulocyte colony-stimulating factor delays programmed cell death in neutrophils by up-regulating the vacuolar H(+)-ATPase. Proc Natl Acad Sci U S A. 1995;92(13):5965–5968.
  • Ishisaki A, Hashimoto S, Amagasa T, et al. Caspase-3 activation during the process of apoptosis induced by a vacuolar type H(+)-ATPase inhibitor. Biol Cell. 1999;91(7):507–513.
  • Karwatowska-Prokopczuk E, Nordberg JA, Li HL, et al. Effect of vacuolar proton ATPase on pHi, Ca2+, and apoptosis in neonatal cardiomyocytes during metabolic inhibition/recovery. Circ Res. 1998;82(11):1139–1144.
  • Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov. 2011;10(10):767–777.
  • Hagland H, Nikolaisen J, Hodneland LI, et al. Targeting mitochondria in the treatment of human cancer: a coordinated attack against cancer cell energy metabolism and signalling. Expert Opin Ther Targets. 2007;11(8):1055–1069.
  • Luciani F, Spada M, De Milito A, et al. Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. J Natl Cancer Inst. 2004;96(22):1702–1713.
  • Hendrix A, Sormunen R, Westbroek W, et al. Vacuolar H+ ATPase expression and activity is required for Rab27B-dependent invasive growth and metastasis of breast cancer. Int J Cancer. 2013;133(4):843–854.
  • Buechling T, Bartscherer K, Ohkawara B, et al. Wnt/Frizzled signaling requires dPRR, the Drosophila homolog of the prorenin receptor. Curr Biol. 2010;20(14):1263–1268.
  • Chen SH, Bubb MR, Yarmola EG, et al. Vacuolar H+-ATPase binding to microfilaments: regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B. J Biol Chem. 2004;279(9):7988–7998.
  • Mauvezin C, Neufeld TP. Bafilomycin A1 disrupts autophagic flux by inhibiting both V-ATPase-dependent acidification and Ca-P60A/SERCA-dependent autophagosome-lysosome fusion. Autophagy. 2015;11(8):1437–1438.
  • Liberman R, Bond S, Shainheit MG, et al. Regulated assembly of vacuolar ATPase is increased during cluster disruption-induced maturation of dendritic cells through a phosphatidylinositol 3-kinase/mTOR-dependent pathway. J Biol Chem. 2014;289(3):1355–1363.
  • Thomas L, Rao Z, Gerstmeier J, et al. Selective upregulation of TNFalpha expression in classically-activated human monocyte-derived macrophages (M1) through pharmacological interference with V-ATPase. Biochem Pharmacol. 2017;130:71–82.
  • Scherer O, Steinmetz H, Kaether C, et al. Targeting V-ATPase in primary human monocytes by archazolid potently represses the classical secretion of cytokines due to accumulation at the endoplasmic reticulum. Biochem Pharmacol. 2014;91(4):490–500.
  • Hatfield KJ, Olsnes AM, Gjertsen BT, et al. Antiangiogenic therapy in acute myelogenous leukemia: targeting of vascular endothelial growth factor and interleukin 8 as possible antileukemic strategies. Curr Cancer Drug Targets. 2005;5(4):229–248.
  • Reikvam H, Hatfield KJ, Fredly H, et al. The angioregulatory cytokine network in human acute myeloid leukemia - from leukemogenesis via remission induction to stem cell transplantation. Eur Cytokine Netw. 2012;23(4):140–153.
  • Rath S, Liebl J, Furst R, et al. Regulation of endothelial signaling and migration by v-ATPase. Angiogenesis. 2014;17(3):587–601.
  • Ehninger A, Trumpp A. The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in. J Exp Med. 2011;208(3):421–428.
  • Sennoune SR, Arutunyan A, Del Rosario C, et al. V-ATPase regulates communication between microvascular endothelial cells and metastatic cells. Cell Mol Biol (Noisy-Le-Grand). 2014;60(1):19–25.
  • Di Pompo G, Lemma S, Canti L, et al. Intratumoral acidosis fosters cancer-induced bone pain through the activation of the mesenchymal tumor-associated stroma in bone metastasis from breast carcinoma. Oncotarget. 2017;8(33):54478–54496.
  • Chen X, Wang Z, Duan N, et al. Osteoblast-osteoclast interactions. Connect Tissue Res. 2017;1–9. doi: 10.1080/03008207.2017.1290085. [Epub ahead of print]
  • Sorensen MG, Henriksen K, Neutzsky-Wulff AV, et al. Diphyllin, a novel and naturally potent V-ATPase inhibitor, abrogates acidification of the osteoclastic resorption lacunae and bone resorption. J Bone Miner Res. 2007;22(10):1640–1648.
  • Bruserud Ø, Foss B, Petersen H. Hematopoietic growth factors in patients receiving intensive chemotherapy for malignant disorders: studies of granulocyte-colony stimulating factor (G-CSF), granulocyte-macrophage colony stimulating factor (GM-CSF), interleukin-3 (IL-3) and Flt-3 ligand (Flt3L). Eur Cytokine Netw. 2001;12(2):231–238.
  • Kaneko K, Ohba K, Hirose T, et al. Expression of (Pro)renin receptor during rapamycin-induced erythropoiesis in K562 erythroleukemia cells and its possible dual actions on erythropoiesis. Tohoku J Exp Med. 2017;241(1):35–43.

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