Intercellular Mitochondrial Transfer in the Tumor Microenvironment
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
Grantová podpora
GA CR 19-25354Y
Grantová Agentura České Republiky
project no. IRP03_2018-2020
Institutional Development Plan of University of Ostrava
No. CZ.02.1.01/0.0/0.0/16_019/0000868
ERDF-Project ENOCH
No. CZ.02.1.01/0.0/0.0/18_069/0010060
ERDF-Project New Directions of Biomedical Research in the Ostrava Region
SGS03/LF/2019-2020 and SGS03/PrF/2019-2020
University of Ostrava
PubMed
32635428
PubMed Central
PMC7407231
DOI
10.3390/cancers12071787
PII: cancers12071787
Knihovny.cz E-zdroje
- Klíčová slova
- cancer, mitochondria, mitochondrial transfer, tumor microenvironment, tunneling nanotubes,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Cell-to-cell communication is a fundamental process in every multicellular organism. In addition to membrane-bound and released factors, the sharing of cytosolic components represents a new, poorly explored signaling route. An extraordinary example of this communication channel is the direct transport of mitochondria between cells. In this review, we discuss how intercellular mitochondrial transfer can be used by cancer cells to sustain their high metabolic requirements and promote drug resistance and describe relevant molecular players in the context of current and future cancer therapy.
Department of Hematooncology University Hospital Ostrava 70200 Ostrava Czech Republic
Faculty of Science University of Ostrava 70800 Ostrava Czech Republic
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Warburg O. On the Origin of Cancer Cells. Am. Assoc. Adv. Sci. 1956;123:309–314. doi: 10.1126/science.123.3191.309. PubMed DOI
Potter M., Newport E., Morten K.J. The Warburg effect: 80 years on. Biochem. Soc. Trans. 2016;44:1499–1505. doi: 10.1042/BST20160094. PubMed DOI PMC
Moreno-Sanchez R., Rodriguez-Enriquez S., Saavedra E., Marin-Hernandez A., Gallardo-Perez J.C. The bioenergetics of cancer: Is glycolysis the main ATP supplier in all tumor cells? Biofactors. 2009;35:209–225. doi: 10.1002/biof.31. PubMed DOI
Michelakis E.D., Webster L., Mackey J.R. Dichloroacetate (DCA) as a potential metabolic-targeting therapy for cancer. Br. J. Cancer. 2008;99:989–994. doi: 10.1038/sj.bjc.6604554. PubMed DOI PMC
Gatenby R.A., Gillies R.J. Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer. 2004;4:891–899. doi: 10.1038/nrc1478. PubMed DOI
Tsvetkov P., Detappe A., Cai K., Keys H.R., Brune Z., Ying W., Thiru P., Reidy M., Kugener G., Rossen J., et al. Mitochondrial metabolism promotes adaptation to proteotoxic stress. Nat. Chem. Biol. 2019;15:681–689. doi: 10.1038/s41589-019-0291-9. PubMed DOI PMC
Kuntz E.M., Baquero P., Michie A.M., Dunn K., Tardito S., Holyoake T.L., Helgason G.V., Gottlieb E. Targeting mitochondrial oxidative phosphorylation eradicates therapy-resistant chronic myeloid leukemia stem cells. Nat. Med. 2017;23:1234–1240. doi: 10.1038/nm.4399. PubMed DOI PMC
Moreno-Sanchez R., Rodriguez-Enriquez S., Marin-Hernandez A., Saavedra E. Energy metabolism in tumor cells. FEBS J. 2007;274:1393–1418. doi: 10.1111/j.1742-4658.2007.05686.x. PubMed DOI
Ashton T.M., McKenna W.G., Kunz-Schughart L.A., Higgins G.S. Oxidative Phosphorylation as an Emerging Target in Cancer Therapy. Clin. Cancer Res. 2018;24:2482–2491. doi: 10.1158/1078-0432.CCR-17-3070. PubMed DOI
Song I.S., Kim H.K., Lee S.R., Jeong S.H., Kim N., Ko K.S., Rhee B.D., Han J. Mitochondrial modulation decreases the bortezomib-resistance in multiple myeloma cells. Int. J. Cancer. 2013;133:1357–1367. doi: 10.1002/ijc.28149. PubMed DOI
Chauncey T.R. Drug resistance mechanisms in acute leukemia. Curr. Opin. Oncol. 2001;13:21–26. doi: 10.1097/00001622-200101000-00005. PubMed DOI
Zhan J., Gu Y., Chen B. Mechanisms of drug resistance in acute myeloid leukemia. OncoTargets Ther. 2019;12:1937–1945. doi: 10.2147/OTT.S191621. PubMed DOI PMC
Roh J.S., Sohn D.H. Damage-associated molecular patterns in inflammatory diseases. Immune Netw. 2018;18:1–14. doi: 10.4110/in.2018.18.e27. PubMed DOI PMC
Rubartelli A., Lotze M.T. Inside, outside, upside down: Damage-associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol. 2007;28:429–436. doi: 10.1016/j.it.2007.08.004. PubMed DOI
Zhang Q., Raoof M., Chen Y., Sumi Y., Sursal T., Junger W., Brohi K., Itagaki K., Hauser C.J. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature. 2010;464:104–107. doi: 10.1038/nature08780. PubMed DOI PMC
Hernandez C., Huebener P., Schwabe R. Damage-associated molecular patterns in cancer: A double edged sword. Oncogene. 2016;35:5931–5941. doi: 10.1038/onc.2016.104. PubMed DOI PMC
Krysko O., Aaes T.L., Bachert C., Vandenabeele P., Krysko D.V. Many faces of DAMPs in cancer therapy. Cell Death Dis. 2013;4:e631. doi: 10.1038/cddis.2013.156. PubMed DOI PMC
Spees J.L., Olson S.D., Whitney M.J., Prockop D.J. Mitochondrial transfer between cells can rescue aerobic respiration. Proc. Natl. Acad. Sci. USA. 2006;103:1283–1288. doi: 10.1073/pnas.0510511103. PubMed DOI PMC
Hayakawa K., Esposito E., Wang X., Terasaki Y., Liu Y., Xing C., Ji X., Lo E.H. Transfer of mitochondria from astrocytes to neurons after stroke. Nature. 2016;535:551–555. doi: 10.1038/nature18928. PubMed DOI PMC
Lu J., Zheng X., Li F., Yu Y., Chen Z., Liu Z., Xu H., Yang W. Tunneling nanotubes promote intercellular mitochondria transfer followed by increased invasiveness in bladder cancer cells. Oncotarget. 2017;8:15539–15552. doi: 10.18632/oncotarget.14695. PubMed DOI PMC
Pasquier J., Guerrouahen B.S., Al Thawadi H., Ghiabi P., Maleki M., Abu-Kaoud N., Jacob A., Mirshahi M., Galas L., Rafii S., et al. Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J. Transl. Med. 2013;11:1–14. doi: 10.1186/1479-5876-11-94. PubMed DOI PMC
Burt R., Dey A., Aref S., Aguiar M., Akarca A., Bailey K., Day W., Hooper S., Kirkwood A., Kirschner K., et al. Activated stromal cells transfer mitochondria to rescue acute lymphoblastic leukemia cells from oxidative stress. Blood. 2019;134:1415–1429. doi: 10.1182/blood.2019001398. PubMed DOI PMC
Marlein C.R., Piddock R.E., Mistry J.J., Zaitseva L., Hellmich C., Horton R.H., Zhou Z., Auger M.J., Bowles K.M., Rushworth S.A. CD38-driven mitochondrial trafficking promotes bioenergetic plasticity in multiple myeloma. Cancer Res. 2019;79:2285–2297. doi: 10.1158/0008-5472.CAN-18-0773. PubMed DOI
Dong L.F., Kovarova J., Bajzikova M., Bezawork-Geleta A., Svec D., Endaya B., Sachaphibulkij K., Coelho A.R., Sebkova N., Ruzickova A., et al. Horizontal transfer of whole mitochondria restores tumorigenic potential in mitochondrial DNA-deficient cancer cells. eLife. 2017;6:e22187. doi: 10.7554/eLife.22187. PubMed DOI PMC
Wang X., Gerdes H.H. Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death Differ. 2015;22:1181–1191. doi: 10.1038/cdd.2014.211. PubMed DOI PMC
Liu K., Ji K., Guo L., Wu W., Lu H., Shan P., Yan C. Mesenchymal stem cells rescue injured endothelial cells in an in vitro ischemia-reperfusion model via tunneling nanotube like structure-mediated mitochondrial transfer. Microvasc. Res. 2014;92:10–18. doi: 10.1016/j.mvr.2014.01.008. PubMed DOI
Li X., Zhang Y., Yeung S.C., Liang Y., Liang X., Ding Y., Ip M.S.M., Tse H.F., Mak J.C.W., Lian Q. Mitochondrial transfer of induced pluripotent stem cell-derived mesenchymal stem cells to airway epithelial cells attenuates cigarette smoke-induced damage. Am. J. Respir. Cell Mol. Biol. 2014;51:455–465. doi: 10.1165/rcmb.2013-0529OC. PubMed DOI
Vallabhaneni K.C., Haller H., Dumler I. Vascular smooth muscle cells initiate proliferation of mesenchymal stem cells by mitochondrial transfer via tunneling nanotubes. Stem Cells Dev. 2012;21:3104–3113. doi: 10.1089/scd.2011.0691. PubMed DOI PMC
Islam M.N., Das S.R., Emin M.T., Wei M., Sun L., Westphalen K., Rowlands D.J., Quadri S.K., Bhattacharya S., Bhattacharya J. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat. Med. 2012;18:759–765. doi: 10.1038/nm.2736. PubMed DOI PMC
Jiang D., Gao F., Zhang Y., Wong D.S.H., Li Q., Tse H.F., Xu G., Yu Z., Lian Q. Mitochondrial transfer of mesenchymal stem cells effectively protects corneal epithelial cells from mitochondrial damage. Cell Death Dis. 2016;7:e2467. doi: 10.1038/cddis.2016.358. PubMed DOI PMC
Jackson M.V., Morrison T.J., Doherty D.F., McAuley D.F., Matthay M.A., Kissenpfennig A., O’Kane C.M., Krasnodembskaya A.D. Mitochondrial Transfer via Tunneling Nanotubes is an Important Mechanism by Which Mesenchymal Stem Cells Enhance Macrophage Phagocytosis in the in vitro and in vivo Models of ARDS. Stem Cells. 2016;34:2210–2223. doi: 10.1002/stem.2372. PubMed DOI PMC
Mistry J.J., Marlein C.R., Moore J.A., Hellmich C., Wojtowicz E.E., Smith J.G.W., Macaulay I., Sun Y., Morfakis A., Patterson A., et al. ROS-mediated PI3K activation drives mitochondrial transfer from stromal cells to hematopoietic stem cells in response to infection. Proc. Natl. Acad. Sci. USA. 2019;116:24610–24619. doi: 10.1073/pnas.1913278116. PubMed DOI PMC
Marlein C.R., Zaitseva L., Piddock R.E., Robinson S.D., Edwards D.R., Shafat M.S., Zhou Z., Lawes M., Bowles K.M., Rushworth S.A. NADPH oxidase-2 derived superoxide drives mitochondrial transfer from bone marrow stromal cells to leukemic blasts. Blood. 2017;130:1649–1660. doi: 10.1182/blood-2017-03-772939. PubMed DOI
Polak R., Rooij B.D., Pieters R., Boer M.L. Den B-cell precursor acute lymphoblastic leukemia cells use tunneling nanotubes to orchestrate their microenvironment. Blood. 2015;126:2404–2414. doi: 10.1182/blood-2015-03-634238. PubMed DOI
Cho Y.M., Kim J.H., Kim M., Park S.J., Koh S.H., Ahn H.S., Kang G.H., Lee J.-B., Park K.S., Lee H.K. Mesenchymal stem cells transfer mitochondria to the cells with virtually no mitochondrial function but not with pathogenic mtDNA mutations. PLoS ONE. 2012;7:e32778. doi: 10.1371/journal.pone.0032778. PubMed DOI PMC
Lin H., Liou C., Chen S., Hsu T., Chuang J., Wang P., Huang S., Tiao M., Chen J., Lin T., et al. Mitochondrial transfer from Wharton’s jelly-derived mesenchymal stem cells to mitochondria-defective cells recaptures impaired mitochondrial function. Mitochondrion. 2015;22:31–34. doi: 10.1016/j.mito.2015.02.006. PubMed DOI
Moschoi R., Imbert V., Nebout M., Chiche J., Mary D., Prebet T., Saland E., Castellano R., Pouyet L., Collette Y., et al. Protective mitochondrial transfer from bone marrow stromal cells to acute myeloid leukemic cells during chemotherapy. Blood. 2016;128:253–264. doi: 10.1182/blood-2015-07-655860. PubMed DOI
Marlein C.R., Zaitseva L., Piddok R., Schafat M., Collins A., Bowles K., Rushworth S. PGC1α Driven Mitochondrial Biogenesis within the Bone Marrow Stromal Cells of the Acute Myeloid Leukemia Micro-Environment Is a Pre-Requisite for Mitochondrial Transfer to Leukemic Blasts. Blood. 2017;130(Suppl. 1):3927.
Torralba D., Baixauli F., Sánchez-Madrid F. Mitochondria know no boundaries: Mechanisms and functions of intercellular mitochondrial transfer. Front. Cell Dev. Biol. 2016;4:107. doi: 10.3389/fcell.2016.00107. PubMed DOI PMC
Rustom A., Saffrich R., Markovic I., Walther P., Gerdes H.H. Nanotubular Highways for Intercellular Organelle Transport. Science. 2004;303:1007–1010. doi: 10.1126/science.1093133. PubMed DOI
Schapman D., Lebon A., Monterroso B., Bellenger M., Foll F.L., Pasquier J., Vaudry H., Vaudry D., Galas L. Structural and functional analysis of tunneling nanotubes (TnTs) using g CW STED and g confocal approaches. Biol. Cell. 2015;107:419–425. doi: 10.1111/boc.201500004. PubMed DOI
Gousset K., Marzo L., Commere P., Zurzolo C. Myo10 is a key regulator of TNT formation in neuronal cells. J. Cell Sci. 2013;126:4424–4435. doi: 10.1242/jcs.129239. PubMed DOI
Tardivel M., Bégard S., Bousset L., Dujardin S., Coens A., Melki R. Tunneling nanotube (TNT)-mediated neuron-to neuron transfer of pathological Tau protein assemblies. Acta Neuropathol. Commun. 2016;4:117. doi: 10.1186/s40478-016-0386-4. PubMed DOI PMC
Zhang Y., Yu Z., Jiang D., Liang X., Liao S., Zhang Z., Yue W., Li X., Chiu S.M., Chai Y.H., et al. iPSC-MSCs with High Intrinsic MIRO1 and Sensitivity to TNF-α Yield Efficacious Mitochondrial Transfer to Rescue Anthracycline-Induced Cardiomyopathy. Stem Cell Rep. 2016;7:749–763. doi: 10.1016/j.stemcr.2016.08.009. PubMed DOI PMC
Ahmad T., Mukherjee S., Pattnaik B., Kumar M., Singh S., Rehman R., Tiwari B.K., Jha K.A., Barhanpurkar A.P., Wani M.R., et al. Miro1 regulates intercellular mitochondrial transport & enhances mesenchymal stem cell rescue efficacy. EMBO J. 2014;33:994–1010. doi: 10.1002/embj.201386030. PubMed DOI PMC
López-Doménech G., Covill-Cooke C., Ivankovic D., Halff E.F., Sheehan D.F., Norkett R., Birsa N., Kittler J.T. Miro proteins coordinate microtubule- and actin-dependent mitochondrial transport and distribution. EMBO J. 2018;37:321–336. doi: 10.15252/embj.201696380. PubMed DOI PMC
Zhang Y. Tunneling-nanotube. Commun. Integr. Biol. 2011;4:324–325. doi: 10.4161/cib.4.3.14855. PubMed DOI PMC
Hase K., Kimura S., Takatsu H., Ohmae M., Kawano S., Kitamura H., Ito M., Watarai H., Hazelett C., Yeaman C., et al. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat. Cell Biol. 2009;12:1427–1432. doi: 10.1038/ncb1990. PubMed DOI
Ohno H., Hase K., Kimura S. M-Sec: Emerging secrets of tunneling nanotube formation. Commun. Integr. Biol. 2010;3:231–233. doi: 10.4161/cib.3.3.11242. PubMed DOI PMC
Aarhus R., Graeff R.M., Dickey D.M., Walseth T.F., Lee H.C. ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. J. Biol. Chem. 1995;270:30327–30333. doi: 10.1074/jbc.270.51.30327. PubMed DOI
Lee H.C. Physiologival functions of cyclic ADP-ribose and NAADP as calcium messangers. Annu. Rev. Pharmacol. Toxicol. 2001;41:317–345. doi: 10.1146/annurev.pharmtox.41.1.317. PubMed DOI
Bruzzone S., Moreschi I., Guida L., Usai C., Zocchi E., De Flora A. Extracellular NAD+ regulates intracellular calcium levels and induces activation of human granulocytes. Biochem. J. 2006;393:697–704. doi: 10.1042/BJ20051302. PubMed DOI PMC
Ariazi J., Benowitz A., De Biasi V., Den Boer M.L., Cherqui S., Cui H., Douillet N., Eugenin E.A., Favre D., Goodman S., et al. Tunneling Nanotubes and Gap Junctions—Their Role in Long-Range Intercellular Communication during Development, Health, and Disease Conditions. Front. Mol. Neurosci. 2017;10:333. doi: 10.3389/fnmol.2017.00333. PubMed DOI PMC
Osswald M., Jung E., Sahm F., Solecki G., Venkataramani V., Blaes J., Weil S., Horstmann H., Wiestler B., Syed M., et al. Brain tumour cells interconnect to a functional and resistant network. Nature. 2015;528:93–98. doi: 10.1038/nature16071. PubMed DOI
Wang X., Veruki M.L., Bukoreshtliev N.V., Hartveit E., Gerdes H. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. Proc. Natl. Acad. Sci. USA. 2010;107:17194–17199. doi: 10.1073/pnas.1006785107. PubMed DOI PMC
He K., Shi X., Zhang X., Dang S., Ma X., Liu F., Xu M., Lv Z., Han D., Fang X., et al. Long-distance intercellular connectivity between cardiomyocytes and cardiofibroblasts mediated by membrane nanotubes. Cardiovasc. Res. 2011;92:39–47. doi: 10.1093/cvr/cvr189. PubMed DOI
Eugenin E.A. Role of Connexin/Pannexin containing channels in infectious diseases. FEBS Lett. 2014;588:1389–1395. doi: 10.1016/j.febslet.2014.01.030. PubMed DOI PMC
Aasen T. Connexins: Junctional and non-junctional modulators of proliferation. Cell Tissue Res. 2015;360:685–699. doi: 10.1007/s00441-014-2078-3. PubMed DOI
Gerdes H.H., Carvalho R.N. Intercellular transfer mediated by tunneling nanotubes. Curr. Opin. Cell Biol. 2008;20:470–475. doi: 10.1016/j.ceb.2008.03.005. PubMed DOI
Gerdes H.H., Rustom A., Wang X. Tunneling nanotubes, an emerging intercellular communication route in development. Mech. Dev. 2013;130:381–387. doi: 10.1016/j.mod.2012.11.006. PubMed DOI
Whiteside T. The tumor microenvironment and its role in promoting tumor growth. Oncogene. 2008;27:5904–5912. doi: 10.1038/onc.2008.271. PubMed DOI PMC
Saha T., Dash C., Khiste S., Sengupta S. A novel mechanism of immunosuppression via nanotube mediated mitochondrial trafficking between cancer cell and immune cell. Cancer Res. 2019 doi: 10.1038/nmat769. DOI
Ippolito L., Morandi A., Taddei M.L., Parri M., Comito G., Iscaro A., Raspollini M.R., Magherini F., Rapizzi E., Masquelier J., et al. Cancer-associated fibroblasts promote prostate cancer malignancy via metabolic rewiring and mitochondrial transfer. Oncogene. 2019;38:5339–5355. doi: 10.1038/s41388-019-0805-7. PubMed DOI
Wang J., Liu X., Qiu Y., Shi Y., Cai J., Wang B., Wei X., Ke Q., Sui X., Wang Y., et al. Cell adhesion-mediated mitochondria transfer contributes to mesenchymal stem cell-induced chemoresistance on T cell acute lymphoblastic leukemia cells. J. Hematol. Oncol. 2018;11:11. doi: 10.1186/s13045-018-0554-z. PubMed DOI PMC
Poburko D., Santo-Domingo J., Demaurex N. Dynamic regulation of the mitochondrial proton gradient during cytosolic calcium elevations. J. Biol. Chem. 2011;286:11672–11684. doi: 10.1074/jbc.M110.159962. PubMed DOI PMC
Basak N.P., Banerjee S. Mitochondrial dependency in progression of acute myeloid leukemia. Mitochondrion. 2015;21:41–48. doi: 10.1016/j.mito.2015.01.006. PubMed DOI
Putten W.V., Sc M., Schouten H.C., Graux C., Ferrant A., Sonneveld P., Biemond B.J., Gratwohl A., Greef G.E.D., Verdonck L.F., et al. Cytarabine Dose for Acute Myeloid Leukemia. N. Engl. J. Med. 2011:1027–1036. PubMed
Greenberg P.L., Lee S.J., Advani R., Tallman M.S., Sikic B.I., Letendre L., Dugan K., Lum B., Chin D.L., Dewald G., et al. Mitoxantrone, Etoposide, and Cytarabine with or without Valspodar in Patients with Relapsed or Refractory Acute Myeloid Leukemia and High-Risk Myelodysplastic Syndrome: A Phase III Trial (E2995) J. Clin. Oncol. 2004;22:1078. doi: 10.1200/JCO.2004.07.048. PubMed DOI PMC
Teuffel O., Leibundgut K., Lehrnbecher T., Alonzo T.A., Beyene J., Sung L. Anthracyclines during induction therapy in acute myeloid leukaemia: A systematic review and meta-analysis. Br. J. Haematol. 2013;161:192–203. doi: 10.1111/bjh.12233. PubMed DOI
Hole P.S., Zabkiewicz J., Munje C., Newton Z., Pearn L., White P., Marquez N., Hills R.K., Burnett A.K., Tonks A., et al. Overproduction of NOX-derived ROS in AML promotes proliferation and is associated with defective oxidative stress signaling. Blood. 2013;122:3322–3330. doi: 10.1182/blood-2013-04-491944. PubMed DOI
Naik J., Themeli M., de Jong-Korlaar R., Ruiter R.W.J., Poddighe P.J., Yuan H., de Bruijin J.D., Ossenkoppele G.J., Zweegman S., Smit L., et al. CD38 as a therapeutic target for adult acute myeloid leukemia and T-cell acute lymphoblastic leukemia Acute. Haematologica. 2019;14:100–103. doi: 10.3324/haematol.2018.192757. PubMed DOI PMC
Abdallah N., Kumar S.K. Daratumumab in untreated newly diagnosed multiple myeloma. Ther. Adv. Hematol. 2019;10 doi: 10.1177/2040620719894871. PubMed DOI PMC
Mateos M., Spencer A., Nooka A.K., Pour L., Weisel K., Cavo M., Laubach J.P., Cook G. Daratumumab-based regimens are highly effective and well tolerated in relapsed or refractory multiple myeloma regardless of patient age: Subgroup analysis of the phase 3 CASTOR and POLLUX studies. Haematologica. 2020;105:468–477. doi: 10.3324/haematol.2019.217448. PubMed DOI PMC
Mistry J., Hellmich C., Moore J.A., Marlein C., Pillinger G., Collings A., Bowles K., Rushworth S. Daratumumab Inhibits AML Metabolic Capacity and Tumor Growth through Inhibition of CD38 Mediated Mitochondrial Transfer from Bone Marrow Stromal Cells to Blasts in the Leukemic Microenvironment. Blood. 2019 doi: 10.1182/blood-2019-128592. DOI
Farber M., Arnold L., Chen Y., Mollmann M., Duehrsen U., Hanoun M. Inhibition of CD38 Shows Anti-Leukemic Activity in Acute Myeloid Leukemia. Blood. 2018;132:1456. doi: 10.1182/blood-2018-99-113287. DOI
Saba F., Soleimani M., Abroun S. New role of hypoxia in pathophysiology of multiple myeloma through miR-210. EXCLI J. 2018;17:647–662. doi: 10.17179/excli2018-1109. PubMed DOI PMC
Lipchick B., Fink E., Nikiforoc M. Oxidative Stress and Proteasome Inhibitors in Multiple Myeloma. Pharmacol. Res. 2016;105:210–215. doi: 10.1016/j.phrs.2016.01.029. PubMed DOI PMC
Krejcik J., Casneuf T., Nijhof I.S., Verbist B., Bald J., Plesner T., Syed K., Liu K., van de Donk N.W.C.J., Weiss B.M., et al. Daratumumab depletes CD38+ immune regulatory cells, promotes T-cell expansion, and skews T-cell repertoire in multiple myeloma. Blood. 2016;128:384–394. doi: 10.1182/blood-2015-12-687749. PubMed DOI PMC
Moreno A.L., Perez C., Zabaleta A., Manrique I., Garate S., Jelinek T., Segura V., Moreno C. The Mechanism of Action of The Anti-CD38 Monoclonal Antibody Isatuximab In Multiple Myeloma. Clin. Cancer Res. 2019;25:3176–3187. doi: 10.1158/1078-0432.CCR-18-1597. PubMed DOI
Martin T., Strickland S., Glenn M., Charpentier E., Guillemin H., Hsu K., Mikhael J. Phase I trial of isatuximab monotherapy in the treatment of refractory multiple myeloma. Blood Cancer J. 2019;9:1–10. doi: 10.1038/s41408-019-0198-4. PubMed DOI PMC
Spencer A., Lentzsch S., Weisel K., Avet-Loiseau H., Mark T.M., Spicka I., Masszi T., Lauri B., Levin M.D., Bosi A., et al. Daratumumab plus bortezomib and dexamethasone versus bortezomib and dexamethasone in relapsed or refractory multiple myeloma: Updated analysis of CASTOR. Haematologica. 2018;103:2079–2087. doi: 10.3324/haematol.2018.194118. PubMed DOI PMC
Read M.A., Neish A.S., Luscinskas F.W., Palombella V.J., Yaniatis T., Collins T. The Proteasome Pathway is Required for Cytokine-Induced Endothelial-Leukocyte Adhesion Molecule Expression. Immunity. 1995;2:493–506. doi: 10.1016/1074-7613(95)90030-6. PubMed DOI
Chauhan D., Uchiyama H., Akbarali Y., Urashima M., Yamamoto K.I., Libermann T.A., Anderson K.C. Multiple myeloma cell adhesion-induced interleukin-6 expression in bone marrow stromal cells involves activation of NF-κB. Blood. 1996;87:1104–1112. doi: 10.1182/blood.V87.3.1104.bloodjournal8731104. PubMed DOI