Pharmacological inhibition of Carbonic Anhydrase IX and XII to enhance targeting of acute myeloid leukaemia cells under hypoxic conditions
dc.contributor.author | Chen, Fangli | |
dc.contributor.author | Licarete, Emilia | |
dc.contributor.author | Wu, Xue | |
dc.contributor.author | Petrusca, Daniela | |
dc.contributor.author | Maguire, Callista | |
dc.contributor.author | Jacobsen, Max | |
dc.contributor.author | Colter, Austyn | |
dc.contributor.author | Sandusky, George E. | |
dc.contributor.author | Czader, Magdalena | |
dc.contributor.author | Capitano, Maegan L. | |
dc.contributor.author | Ropa, James P. | |
dc.contributor.author | Boswell, H. Scott | |
dc.contributor.author | Carta, Fabrizio | |
dc.contributor.author | Supuran, Claudiu T. | |
dc.contributor.author | Parkin, Brian | |
dc.contributor.author | Fishel, Melissa L. | |
dc.contributor.author | Konig, Heiko | |
dc.date.accessioned | 2022-01-06T15:51:54Z | |
dc.date.available | 2023-01-06 10:51:51 | en |
dc.date.available | 2022-01-06T15:51:54Z | |
dc.date.issued | 2021-12 | |
dc.identifier.citation | Chen, Fangli; Licarete, Emilia; Wu, Xue; Petrusca, Daniela; Maguire, Callista; Jacobsen, Max; Colter, Austyn; Sandusky, George E.; Czader, Magdalena; Capitano, Maegan L.; Ropa, James P.; Boswell, H. Scott; Carta, Fabrizio; Supuran, Claudiu T.; Parkin, Brian; Fishel, Melissa L.; Konig, Heiko (2021). "Pharmacological inhibition of Carbonic Anhydrase IX and XII to enhance targeting of acute myeloid leukaemia cells under hypoxic conditions." Journal of Cellular and Molecular Medicine (24): 11039-11052. | |
dc.identifier.issn | 1582-1838 | |
dc.identifier.issn | 1582-4934 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/171236 | |
dc.description.abstract | Acute myeloid leukaemia (AML) is an aggressive form of blood cancer that carries a dismal prognosis. Several studies suggest that the poor outcome is due to a small fraction of leukaemic cells that elude treatment and survive in specialised, oxygen (O2)‐deprived niches of the bone marrow. Although several AML drug targets such as FLT3, IDH1/2 and CD33 have been established in recent years, survival rates remain unsatisfactory, which indicates that other, yet unrecognized, mechanisms influence the ability of AML cells to escape cell death and to proliferate in hypoxic environments. Our data illustrates that Carbonic Anhydrases IX and XII (CA IX/XII) are critical for leukaemic cell survival in the O2‐deprived milieu. CA IX and XII function as transmembrane proteins that mediate intracellular pH under low O2 conditions. Because maintaining a neutral pH represents a key survival mechanism for tumour cells in O2‐deprived settings, we sought to elucidate the role of dual CA IX/XII inhibition as a novel strategy to eliminate AML cells under hypoxic conditions. Our findings demonstrate that the dual CA IX/XII inhibitor FC531 may prove to be of value as an adjunct to chemotherapy for the treatment of AML. | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.subject.other | acute myeloid leukemia | |
dc.subject.other | Carbonic Anhydrases | |
dc.subject.other | drug resistance | |
dc.subject.other | hypoxia | |
dc.subject.other | pH regulation | |
dc.title | Pharmacological inhibition of Carbonic Anhydrase IX and XII to enhance targeting of acute myeloid leukaemia cells under hypoxic conditions | |
dc.type | Article | |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Molecular, Cellular and Developmental Biology | |
dc.subject.hlbtoplevel | Health Sciences | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/171236/1/jcmm17027_am.pdf | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/171236/2/jcmm17027-sup-0001-FigS1-S4.pdf | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/171236/3/jcmm17027.pdf | |
dc.identifier.doi | 10.1111/jcmm.17027 | |
dc.identifier.source | Journal of Cellular and Molecular Medicine | |
dc.identifier.citedreference | Chen F, Wu X, Niculite C, et al. Classic and targeted anti‐leukaemic agents interfere with the cholesterol biogenesis metagene in acute myeloid leukaemia: therapeutic implications. J Cell Mol Med. 2020; 24 ( 13 ): 7378 ‐ 7392. | |
dc.identifier.citedreference | Paietta E. Minimal residual disease in acute myeloid leukemia: coming of age. Hematology. 2012; 2012: 35 ‐ 42. | |
dc.identifier.citedreference | Pacchiano F, Carta F, McDonald PC, et al. Ureido‐substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis. J Med Chem. 2011; 54 ( 6 ): 1896 ‐ 1902. | |
dc.identifier.citedreference | Mboge MY, Mahon BP, McKenna R, Frost SC. Carbonic anhydrases: role in pH control and cancer. Metabolites. 2018; 8 ( 1 ): 19. | |
dc.identifier.citedreference | Swietach P, Vaughan‐Jones RD, Harris AL. Regulation of tumor pH and the role of carbonic anhydrase 9. Cancer Metastasis Rev. 2007; 26 ( 2 ): 299 ‐ 310. | |
dc.identifier.citedreference | Supuran CT. Inhibition of carbonic anhydrase IX as a novel anticancer mechanism. World J Clin Oncol. 2012; 3 ( 7 ): 98 ‐ 103. | |
dc.identifier.citedreference | Supuran CT, Winum JY. Carbonic anhydrase IX inhibitors in cancer therapy: an update. Future Med Chem. 2015; 7 ( 11 ): 1407 ‐ 1414. | |
dc.identifier.citedreference | Dubois L, Peeters SGJA, van Kuijk SJA, et al. Targeting carbonic anhydrase IX by nitroimidazole based sulfamides enhances the therapeutic effect of tumor irradiation: a new concept of dual targeting drugs. Radiother Oncol. 2013; 108 ( 3 ): 523 ‐ 528. | |
dc.identifier.citedreference | Duivenvoorden WC, Hopmans SN, Gallino D, et al. Inhibition of carbonic anhydrase IX (CA9) sensitizes renal cell carcinoma to ionizing radiation. Oncol Rep. 2015; 34 ( 4 ): 1968 ‐ 1976. | |
dc.identifier.citedreference | Konopleva M, Thall PF, Yi CA, et al. Phase I/II study of the hypoxia‐activated prodrug PR104 in refractory/relapsed acute myeloid leukemia and acute lymphoblastic leukemia. Haematologica. 2015; 100 ( 7 ): 927 ‐ 934. | |
dc.identifier.citedreference | Viikilä P, Kivelä AJ, Mustonen H, et al. Carbonic anhydrase enzymes II, VII, IX and XII in colorectal carcinomas. World J Gastroenterol. 2016; 22 ( 36 ): 8168 ‐ 8177. | |
dc.identifier.citedreference | Chien M‐H, Ying T‐H, Hsieh Y‐H, et al. Tumor‐associated carbonic anhydrase XII is linked to the growth of primary oral squamous cell carcinoma and its poor prognosis. Oral Oncol. 2012; 48 ( 5 ): 417 ‐ 423. | |
dc.identifier.citedreference | Ilie MI, Hofman V, Ortholan C, et al. Overexpression of carbonic anhydrase XII in tissues from resectable non‐small cell lung cancers is a biomarker of good prognosis. Int J Cancer. 2011; 128 ( 7 ): 1614 ‐ 1623. | |
dc.identifier.citedreference | Chen Z, Ai L, Mboge MY, et al. Differential expression and function of CAIX and CAXII in breast cancer: a comparison between tumorgraft models and cells. PLoS One. 2018; 13 ( 7 ): e0199476. | |
dc.identifier.citedreference | Lounnas N, Rosilio C, Nebout M, et al. Pharmacological inhibition of carbonic anhydrase XII interferes with cell proliferation and induces cell apoptosis in T‐cell lymphomas. Cancer Lett. 2013; 333 ( 1 ): 76 ‐ 88. | |
dc.identifier.citedreference | Li G, Chen T‐W, Nickel A‐C, et al. Carbonic anhydrase XII is a clinically significant, molecular tumor‐subtype specific therapeutic target in glioma with the potential to combat invasion of brain tumor cells. Onco Targets Ther. 2021; 14: 1707 ‐ 1718. | |
dc.identifier.citedreference | Hsieh MJ, Chen KS, Chiou HL, Hsieh YS. Carbonic anhydrase XII promotes invasion and migration ability of MDA‐MB‐231 breast cancer cells through the p38 MAPK signaling pathway. Eur J Cell Biol. 2010; 89 ( 8 ): 598 ‐ 606. | |
dc.identifier.citedreference | Ma J, Li X, Su Y, et al. Mechanisms responsible for the synergistic antileukemic interactions between ATR inhibition and cytarabine in acute myeloid leukemia cells. Sci Rep. 2017; 7: 41950. | |
dc.identifier.citedreference | Green SD, Konig H. Treatment of acute myeloid leukemia in the era of genomics‐achievements and persisting challenges. Front Genet. 2020; 11: 480. | |
dc.identifier.citedreference | Parkin B, Londono‐Joshi A, Kang Q, Tewari M, Rhim AD, Malek SN. Ultrasensitive mutation detection identifies rare residual cells causing acute myelogenous leukemia relapse. J Clin Invest. 2017; 127 ( 9 ): 3484 ‐ 3495. | |
dc.identifier.citedreference | Leppilampi M, Koistinen P, Savolainen ER, et al. The expression of carbonic anhydrase II in hematological malignancies. Clin Cancer Res. 2002; 8 ( 7 ): 2240 ‐ 2245. | |
dc.identifier.citedreference | Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov. 2008; 7 ( 2 ): 168 ‐ 181. | |
dc.identifier.citedreference | Konig H, Levis M. Targeting FLT3 to treat leukemia. Expert Opin Ther Targets. 2015; 19 ( 1 ): 37 ‐ 54. | |
dc.identifier.citedreference | Sironi S, Wagner M, Kuett A, et al. Microenvironmental hypoxia regulates FLT3 expression and biology in AML. Sci Rep. 2015; 5: 17550. | |
dc.identifier.citedreference | Andreucci E, Ruzzolini J, Peppicelli S, et al. The carbonic anhydrase IX inhibitor SLC‐0111 sensitises cancer cells to conventional chemotherapy. J Enzyme Inhib Med Chem. 2019; 34 ( 1 ): 117 ‐ 123. | |
dc.identifier.citedreference | Hidalgo M, Amant F, Biankin AV, et al. Patient‐derived xenograft models: an emerging platform for translational cancer research. Cancer Discov. 2014; 4 ( 9 ): 998 ‐ 1013. | |
dc.identifier.citedreference | Muz B, de la Puente P, Azab F, Azab AK. The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia. 2015; 3: 83 ‐ 92. | |
dc.identifier.citedreference | Carreau A, El Hafny‐Rahbi B, Matejuk A, Grillon C, Kieda C. Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia. J Cell Mol Med. 2011; 15 ( 6 ): 1239 ‐ 1253. | |
dc.identifier.citedreference | Estey E. Why is progress in acute myeloid leukemia so slow? Semin Hematol. 2015; 52 ( 3 ): 243 ‐ 248. | |
dc.identifier.citedreference | Griessinger E, Anjos‐Afonso F, Pizzitola I, et al. A niche‐like culture system allowing the maintenance of primary human acute myeloid leukemia‐initiating cells: a new tool to decipher their chemoresistance and self‐renewal mechanisms. Stem Cells Transl Med. 2014; 3 ( 4 ): 520 ‐ 529. | |
dc.identifier.citedreference | Pastorekova S, Gillies RJ. The role of carbonic anhydrase IX in cancer development: links to hypoxia, acidosis, and beyond. Cancer Metastasis Rev. 2019; 38 ( 1–2 ): 65 ‐ 77. | |
dc.identifier.citedreference | Mujumdar P, Kopecka J, Bua S, Supuran CT, Riganti C, Poulsen SA. Carbonic anhydrase XII inhibitors overcome temozolomide resistance in glioblastoma. J Med Chem. 2019; 62 ( 8 ): 4174 ‐ 4192. | |
dc.identifier.citedreference | Haapasalo J, Hilvo M, Nordfors K, et al. Identification of an alternatively spliced isoform of carbonic anhydrase XII in diffusely infiltrating astrocytic gliomas. Neuro Oncol. 2008; 10 ( 2 ): 131 ‐ 138. | |
dc.identifier.citedreference | Sowa T, Menju T, Chen‐Yoshikawa TF, et al. Hypoxia‐inducible factor 1 promotes chemoresistance of lung cancer by inducing carbonic anhydrase IX expression. Cancer Med. 2017; 6 ( 1 ): 288 ‐ 297. | |
dc.identifier.citedreference | McDonald PC, Chia S, Bedard PL, et al. A phase 1 study of SLC‐0111, a novel inhibitor of carbonic anhydrase IX, in patients with advanced solid tumors. Am J Clin Oncol. 2020; 43 ( 7 ): 484 ‐ 490. | |
dc.identifier.citedreference | Švastová E, Hulı́ková A, Rafajová M, et al. Hypoxia activates the capacity of tumor‐associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett. 2004; 577 ( 3 ): 439 ‐ 445. | |
dc.identifier.citedreference | Cecchi A, Hulikova A, Pastorek J, et al. Carbonic anhydrase inhibitors. Design of fluorescent sulfonamides as probes of tumor‐associated carbonic anhydrase IX that inhibit isozyme IX‐mediated acidification of hypoxic tumors. J Med Chem. 2005; 48 ( 15 ): 4834 ‐ 4841. | |
dc.identifier.citedreference | Msaki A, Pastò A, Curtarello M, et al. A hypoxic signature marks tumors formed by disseminated tumor cells in the BALB‐neuT mammary cancer model. Oncotarget. 2016; 7 ( 22 ): 33081 ‐ 33095. | |
dc.identifier.citedreference | Dohner H, Weisdorf DJ, Bloomfield CD. Acute myeloid leukemia. N Engl J Med. 2015; 373 ( 12 ): 1136 ‐ 1152. | |
dc.identifier.citedreference | 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. | |
dc.identifier.citedreference | Nombela‐Arrieta C, Pivarnik G, Winkel B, et al. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol. 2013; 15 ( 5 ): 533 ‐ 543. | |
dc.identifier.citedreference | Nombela‐Arrieta C, Silberstein LE. The science behind the hypoxic niche of hematopoietic stem and progenitors. Hematology. 2014; 2014 ( 1 ): 542 ‐ 547. | |
dc.identifier.citedreference | Mohyeldin A, Garzon‐Muvdi T, Quinones‐Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell. 2010; 7 ( 2 ): 150 ‐ 161. | |
dc.identifier.citedreference | Chow DC, Wenning LA, Miller WM, Papoutsakis ET. Modeling pO(2) distributions in the bone marrow hematopoietic compartment. II. Modified Kroghian models. Biophys J. 2001; 81 ( 2 ): 685 ‐ 696. | |
dc.identifier.citedreference | Spencer JA, Ferraro F, Roussakis E, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature. 2014; 508 ( 7495 ): 269 ‐ 273. | |
dc.identifier.citedreference | Xia Y, Choi HK, Lee K. Recent advances in hypoxia‐inducible factor (HIF)‐1 inhibitors. Eur J Med Chem. 2012; 49: 24 ‐ 40. | |
dc.identifier.citedreference | Ma Z, Xiang X, Li S, et al. Targeting hypoxia‐inducible factor‐1, for cancer treatment: Recent advances in developing small‐molecule inhibitors from natural compounds. Semin Cancer Biol. 2020; S1044‐579X(20)30202‐9. | |
dc.identifier.citedreference | Benito J, Zeng Z, Konopleva M, Wilson WR. Targeting hypoxia in the leukemia microenvironment. Int J Hematol Oncol. 2013; 2 ( 4 ): 279 ‐ 288. | |
dc.identifier.citedreference | Konopleva M, Tabe Y, Zeng Z, Andreeff M. Therapeutic targeting of microenvironmental interactions in leukemia: mechanisms and approaches. Drug Resist Updat. 2009; 12 ( 4–5 ): 103 ‐ 113. | |
dc.identifier.citedreference | Rashidi A, DiPersio JF. Targeting the leukemia‐stroma interaction in acute myeloid leukemia: rationale and latest evidence. Ther Adv Hematol. 2016; 7 ( 1 ): 40 ‐ 51. | |
dc.identifier.citedreference | Kung AL, Wang S, Klco JM, Kaelin WG, Livingston DM. Suppression of tumor growth through disruption of hypoxia‐inducible transcription. Nat Med. 2000; 6 ( 12 ): 1335 ‐ 1340. | |
dc.identifier.citedreference | Carmeliet P, Dor Y, Herbert JM, et al. Role of HIF‐1alpha in hypoxia‐mediated apoptosis, cell proliferation and tumour angiogenesis. Nature. 1998; 394 ( 6692 ): 485 ‐ 490. | |
dc.identifier.citedreference | Blouw B, Song H, Tihan T, et al. The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell. 2003; 4 ( 2 ): 133 ‐ 146. | |
dc.identifier.citedreference | 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. | |
dc.identifier.citedreference | Kopecka J, Campia I, Jacobs A, et al. Carbonic anhydrase XII is a new therapeutic target to overcome chemoresistance in cancer cells. Oncotarget. 2015; 6 ( 9 ): 6776 ‐ 6793. | |
dc.identifier.citedreference | Logsdon DP, Shah F, Carta F, et al. Blocking HIF signaling via novel inhibitors of CA9 and APE1/Ref‐1 dramatically affects pancreatic cancer cell survival. Sci Rep. 2018; 8 ( 1 ): 13759. | |
dc.identifier.citedreference | Lou Y, McDonald PC, Oloumi A, et al. Targeting tumor hypoxia: suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors. Cancer Res. 2011; 71 ( 9 ): 3364 ‐ 3376. | |
dc.working.doi | NO | en |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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