Publications

2021

Han G, Yang G, Hao D, Lu Y, Thein K, Simpson BS, Chen J, Sun R, Alhalabi O, Wang R, Dang M, Dai E, Zhang S, Nie F, Zhao S, Guo C, Hamza A, Czerniak B, Cheng C, Siefker-Radtke A, Bhat K, Futreal A, Peng G, Wargo J, Peng W, Kadara H, Ajani J, Swanton C, Litchfield K, Ahnert JR, Gao J, Wang L. 9p21 loss confers a cold tumor immune microenvironment and primary resistance to immune checkpoint therapy. Nat Commun. 2021 Sep 23;12(1):5606.

Valdebenito S, Malik S, Luu R, Loudig O, Mitchell M, Okafo G, Bhat K, Prideaux B, Eugenin EA. Tunneling nanotubes, TNT, communicate glioblastoma with surrounding non-tumor astrocytes to adapt them to hypoxic and metabolic tumor conditions. Sci Rep. 2021 Jul 15;11(1):14556. doi: 10.1038/s41598-021-93775-8. PMID: 34267246; PMCID: PMC8282675.

Banday S, Pandita RK, Mushtaq A, Bacolla A, Mir US, Singh DK, Jan S, Bhat KP, Hunt CR, Rao G, Charaka VK, Tainer JA, Pandita TK, Altaf M. Autism-Associated Vigilin Depletion Impairs DNA Damage Repair. Mol Cell Biol. 2021 Jun 23;41(7):e0008221. doi: 10.1128/MCB.00082-21. Epub 2021 Jun 23. PMID: 33941620; PMCID: PMC8224237.

2020

Bastola S, Pavlyukov MS, Yamashita D, Ghosh S, Cho H, Kagaya N, Zhang Z, Minata M, Lee Y, Sadahiro H, Yamaguchi S, Komarova S, Yang E, Markert J, Nabors LB, Bhat K, Lee J, Chen Q, Crossman DK, Shin-Ya K, Nam DH, Nakano I. Glioma- initiating cells at tumor edge gain signals from tumor core cells to promote their malignancy. Nat Commun. 2020 Sep 16;11(1):4660. doi: 10.1038/s41467-020-18189-y. PMID: 32938908; PMCID: PMC7494913.

Valdebenito S, Audia A, Bhat KPL, Okafo G, Eugenin EA. Tunneling Nanotubes Mediate Adaptation of Glioblastoma Cells to Temozolomide and Ionizing Radiation Treatment. iScience. 2020 Aug 13;23(9):101450. doi: 10.1016/j.isci.2020.101450. Epub ahead of print. PMID: 32882515; PMCID: PMC7476317.

Yamashita D, Bernstock JD, Elsayed G, Sadahiro H, Mohyeldin A, Chagoya G, Ilyas A, Mooney J, Estevez-Ordonez D, Yamaguchi S, Flanary VL, Hackney JR, Bhat KP, Kornblum HI, Zamboni N, Kim SH, Chiocca EA, Nakano I. Targeting glioma- initiating cells via the tyrosine metabolic pathway. J Neurosurg. 2020 Feb 14;134(3):721-732. doi: 10.3171/2019.11.JNS192028. PMID: 32059178; PMCID: PMC8447888.

Balasubramaniyan V, Bhat K. Targeting pyrimidine metabolism for glioblastoma therapy. Neuro Oncol. 2020 Feb 20;22(2):169-170. doi: 10.1093/neuonc/noz239. PMID: 31863119; PMCID: PMC7032621.

Wei J, Chen P, Gupta P, Ott M, Zamler D, Kassab C, Bhat KP, Curran MA, de Groot JF, Heimberger AB. Immune biology of glioma-associated macrophages and microglia: functional and therapeutic implications. Neuro Oncol. 2020 Feb 20;22(2):180-194. doi: 10.1093/neuonc/noz212. PMID: 31679017; PMCID: PMC7442334.

2019

Lowe S, Bhat KP, Olar A. Current clinical management of patients with glioblastoma. Cancer Rep (Hoboken). 2019 Dec;2(6):e1216. doi: 10.1002/cnr2.1216. Epub 2019 Sep 4. PMID: 32721125; PMCID: PMC7941570.

Yang Y, Dodbele S, Park T, Glass R, Bhat K, Sulman EP, Zhang Y, Abounader R. MicroRNA-29a inhibits glioblastoma stem cells and tumor growth by regulating the PDGF pathway. J Neurooncol. 2019 Oct;145(1):23-34. doi: 10.1007/s11060-019-03275-z. Epub 2019 Sep 3. PMID: 31482267.

Day BW, Lathia JD, Bruce ZC, D'Souza RCJ, Baumgartner U, Ensbey KS, Lim YC, Stringer BW, Akgül S, Offenhäuser C, Li Y, Jamieson PR, Smith FM, Jurd CLR, Robertson T, Inglis PL, Lwin Z, Jeffree RL, Johns TG, Bhat KPL, Rich JN, Campbell KP, Boyd AW. The dystroglycan receptor maintains glioma stem cells in the vascular niche. Acta Neuropathol. 2019 Dec;138(6):1033-1052. doi: 10.1007/s00401-019-02069-x. Epub 2019 Aug 28. PMID: 31463571; PMCID: PMC6851226.

Minata M, Audia A, Shi J, Lu S, Bernstock J, Pavlyukov MS, Das A, Kim SH, Shin YJ, Lee Y, Koo H, Snigdha K, Waghmare I, Guo X, Mohyeldin A, Gallego-Perez D, Wang J, Chen D, Cheng P, Mukheef F, Contreras M, Reyes JF, Vaillant B, Sulman EP, Cheng SY, Markert JM, Tannous BA, Lu X, Kango-Singh M, Lee LJ, Nam DH, Nakano I, Bhat KP. Phenotypic Plasticity of Invasive Edge Glioma Stem-like Cells in Response to Ionizing Radiation. Cell Rep. 2019 Feb 12;26(7):1893-1905.e7. doi: 10.1016/j.celrep.2019.01.076. PMID: 30759398; PMCID: PMC6594377.

D'Angelo F, Ceccarelli M, Tala, Garofano L, Zhang J, Frattini V, Caruso FP, Lewis G, Alfaro KD, Bauchet L, Berzero G, Cachia D, Cangiano M, Capelle L, de Groot J, DiMeco F, Ducray F, Farah W, Finocchiaro G, Goutagny S, Kamiya-Matsuoka C, Lavarino C, Loiseau H, Lorgis V, Marras CE, McCutcheon I, Nam DH, Ronchi S, Saletti V, Seizeur R, Slopis J, Suñol M, Vandenbos F, Varlet P, Vidaud D, Watts C, Tabar V, Reuss DE, Kim SK, Meyronet D, Mokhtari K, Salvador H, Bhat KP, Eoli M, Sanson M, Lasorella A, Iavarone A. The molecular landscape of glioma in patients with Neurofibromatosis 1. Nat Med. 2019 Jan;25(1):176-187. doi: 10.1038/s41591-018-0263-8. Epub 2018 Dec 10. PMID: 30531922; PMCID: PMC6857804.

2018

D’Angelo, F., Ceccarelli, M., Garofano, L., Zhang, J., Frattini, V., Caruso, F.P., Alfaro, K.D., Bauchet, L., Berzero, G., Cachia, D., Cangiano, M., Capelle, L., de Groot, J., Di Meco, F., Ducray, F., Farah, W., Finocchiaro, G., Goutagny, S., Kamiya-Matsuoka, C., Loiseau, H., Lorgis, V., Marras, C. E., McCutcheon, I., Mokhtari, K., Nam, D-H., Ronchi, S., Saletti, V.,  Seizeur, R., Slopis, J., Vandenbos, F., Varlet, P., Vidaud, D., Watts, C., Tabar, V., Reuss, D.E., Kim, S-K., Salvador, H., Bhat, K.P., Eoli, M., Sanson, M., Lasorella, A., and Iavarone, A. The Molecular Landscape of Glioma in Patients with Neurofibromatosis-1. Nat. Med., doi: 10.1038/s41591-018-0263-8, 2018.

Conroy, S., Kruyt, F.A.E., Wagemakers, M., Bhat, K.P.L*., den Dunnen, W.F.A*. IL-8 associates with a pro-angiogenic and mesenchymal subtype in glioblastoma. Oncotarget. 9(21):15721-15731, 2018.

2017

Boyd, N.H., Walker, K., Fried, J., Hackney, J.R., McDonald, P.C., Benavides, G.A., Spina, R., Audia, A., Scott, S.E., Libby, C.J., Tran, A.N., Bevensee, M.O., Griguer, C., Nozell, S., Gillespie, G.Y., Nabors, B., Bhat, K.P., Bar, E.E., Darley-Usmar, V., Xu, B., Gordon, E., Cooper, S.J., Dedhar, S., and Hjelmeland AB. Addition of carbonic anhydrase 9 inhibitor SLC-0111 to temozolomide treatment delays glioblastoma growth in vivo. JCI Insight., 2(24): 92928, 2017.

Moreno, M., Pedrosa, L., Paré, L., Pineda, E., Bejarano, L., Martínez, J., Balasubramaniyan, V., Ezhilarasan, R., Kallarackal, N., Kim, S.H., Wang, J., Audia, A., Conroy, S., Marin, M., Ribalta, T., Pujol, T., Herreros, A., Tortosa, A., Mira, H., Alonso, M.M., Gómez-Manzano, C., Graus, F., Sulman, E.P., Piao, X., Nakano, I., Prat, A., Bhat, K.P., and de la Iglesia, N. GPR56/ADGRG1 Inhibits Mesenchymal Differentiation and Radioresistance in Glioblastoma. Cell Rep., 21(8): 2183-2197 2017.

Boonyawan, K., Hess, K.R., Yang, J., Long, L., Wang, Q., Ezhilarasan, R., Auia, A., Alfaro-Munoz, K.D., de Groot, J.F., Bhat, K.P., and Sulman, E.P. A relative increase in circulating platelets following chemoradiation predicts for poor survival of patients with glioblastoma. Oncotarget, 8(52):90488-90495, 2017.

Li, M., Xiao, A., Floydm, D., Olmez, I., Lee, J., Godlewski, J., Bronisz, A., Bhat, K.P.L., Sulman, E.P., Nakano, I., and Purow, B. CDK4/6 inhibition is more active against the glioblastoma proneural subtype. Oncotarget, 8(33):55319-55331, 2017.

2016

Cheng, P., Wang, J., Waghmare, I., Sartini, S., Coviello, V., Zhang, Z., Kim, S.H., Mohyeldin, A., Pavlyukov, M.S., Minata, M., Valentim, C.L., Chhipa, R.R., Bhat, K.P., Dasgupta, B., La Motta, C., Kango-Singh, M., Nakano, I. FOXD1-ALDH1A3 Signaling Is a Determinant for the Self-Renewal and Tumorigenicity of Mesenchymal Glioma Stem Cells. Cancer Res., 76(24):7219-7230, 2016.

Gabrusiewicz, K., Rodriguez, B., Wei, J., Hashimoto, Y., Healy, L.M., Maiti, S.N., Thomas, G., Zhou, S., Wang, Q., Elakkad, A., Liebelt, B.D., Yaghi, N.K., Ezhilarasan, R., Huang, N., Weinberg, J.S., Prabhu, S.S., Rao, G., Sawaya, R., Langford, L., Bruner, J.M., Fuller, G.N., Bar-Or, A., Li, W., Colen, R.R., Curran, M.A., Bhat, K.P., Antel, J.P., Cooper L.J., Sulman, E.P., Heimberger, A.B. Glioblastoma-infiltrated innate immune cells resemble M0 macrophage phenotype. JCI Insight, 1(2). pii: e85841, 2016.

Kim, S-H., Ezhilarasan, R., Phillips, E., Gallego-Perez, D., Sparks, A., Taylor, D., Ladner, K., Furuta, T., Sabit, H., Chhipa, R., Cho, J-H., Mohyeldin, A., Beck, S., Kurozumi, K., Kuroiwa, T., Iwata, R., Asai, A., Kim, J., Sulman, E.P., Cheng, S-Y., Lee, L.J., Nakada, M., Guttridge, D., DasGupta, B., Goidts, V., Bhat, K.P., and Nakano, I. Serine/Threonine Kinase MLK4 Determines Mesenchymal Identity in Glioma Stem Cells in a NF-κB-dependent Manner. Cancer Cell*, 29 (2): 201–213, 2016.

*Highlights from the Literature, Neuro Oncol., 18(8):1040-2, 2016.

2015

Sathyan, P., Zinn, P.O., Marisetty, A.L., Liu, B., Kamal, M.M., Singh, S.K., Bady, P., Lu, L., Wani, K.M., Veo, B.L., Gumin, J., Kassem, D.H., Robinson, F., Weng, C., Baladandayuthapani, V., Suki, D., Colman, H., Bhat, K.P., Sulman, E.P., Aldape, K., Colen, R.R., Verhaak, R.G., Lu, Z., Fuller, G.N., Huang, S., Lang, F.F., Sawaya, R., Hegi, M., Majumder, S. Mir-21-Sox2 Axis Delineates Glioblastoma Subtypes with Prognostic Impact. J Neurosci., 35(45): 15097-112,2015.

Balasubramaniyan, V., Vaillant, B., Wang, S., Gumin, J., Butalid, M.E., Sai, K., Mukheef, F., Kim, S.H., Boddeke, H.W., Lang, F., Aldape, K., Sulman, E.P., Bhat, K.P*., and Colman, H*. Aberrant mesenchymal differentiation of glioma stem-like cells: Implication for therapeutic targeting. Oncotarget., 6(31): 31007-17, 2015

Kim, S-H., Joshi, K., Ezhilarasan, R., Myers, T.R., Siu, J., Gu, J., Nakano-Okuno, M., Taylor, D., Minata, M., Sulman, E.P., Lee, J., Bhat, K.P., Salcini, A.E., and Nakano, I.EZH2 Protects Glioma Stem Cells from Radiation-Induced Cell Death in a MELK/FOXM1-Dependent Manner. Stem Cell Rep., 4(2): 226-38, 2015.

2014

Conroy, S., Kruyt, F.A., Joseph, J.V., Balasubramaniyan, V., Bhat, K.P., Wagemakers, M., Enting, R.H., Walenkamp, A.M., and Dunnen, W.F. Subclassification of Newly Diagnosed Glioblastomas through an Immunohistochemical Approach. PLoS One, 9(12): 2014.

Joseph, J.V., Conroy, S., Tomar, T., Eggens-Meijer, E., Bhat, K., Copray, S., Walenkamp, A.M., Boddeke, E., Balasubramanyian, V., Wagemakers, M., den Dunnen, W.F., and Kruyt, F.A. TGF-β is an inducer of ZEB1-dependent mesenchymal transdifferentiation in glioblastoma that is associated with tumor invasion. Cell Death Dis., 2 (5): e1443, 2014.

2013 and prior

Bhat, K.P*., Balasubramaniyan, V., Vaillant, V., Ezhilarasan, R., Hollingsworth, F., James, J.D., Goodman, L.D., Conroy, S., Wani, S., Wang, S., Gumin, J., Raj, D., Raghunathan, A., Joshi, K., Pelloski, C.E., Heimberger, A., Lang, F.F., denDunnen, W.F.A., Boddeke, H.W.D.G.M.,  Phillips, H.S., Nakano, I., Colman, H., Sulman, E.P*., and Aldape, K*. Mesenchymal differentiation induced by NFkB promotes radiation resistance in glioblastoma. Cancer Cell**, 24 (3): 331-46, 2013. *corresponding authors.

**Editor’s Choice: Cutting EMT at the Pass, Sci. Signal., 293 (6), 223, 2013.

Doucette, T.A., Kong, L.Y., Yang, Y., Ferguson, S.D., Yang, J., Wei, J., Qiao, W., Fuller, G.N., Bhat, K.P., Aldape, K., Priebe, W., Bögler, O., Heimberger, A.B., and Rao, G. Signal transducer and activator of transcription 3 promotes angiogenesis and drives malignant progression in glioma. Neuro Oncol., 14(9):1136-45, 2012.

Bhat, K.P*., Salazar, K.L., Balasubramaniyan, V., Wani, K., Heathcock, L., Hollingsworth, F., Gumin, J., Diefes, K.L., Kim, S.H., Turski, A., Azodi, Y., Yang, Y., Doucette, T., Colman, H., Sulman, E.P., Lang, F.F., Rao, G., Copray, S., Vaillant, B.D., Aldape, K.D*. The transcriptional coactivator TAZ regulates mesenchymal differentiation in malignant glioma. Genes Dev**., 25(24):2594-609, 2011. *corresponding authors.

**Breaking Advances in Cancer Research. Proneural-to-mesenchymal transitions in brain tumors. Cancer Res., 72:377-378, 2012.

**Cancer stem cells: TAZ takes centre stage. Nat. Rev. Cancer, 12 (2): 82, 2012.

**Faculty of 1000 prime.

Singh, M.M., Manton, C.A., Bhat, K.P., Tsai, W.W., Aldape, K., Barton, M.C., Chandra, J. Inhibition of LSD1 sensitizes glioblastoma cells to histone deacetylase inhibitors. Neuro Oncol., 13(8):894-903, 2011.

Gu, D., Tonthat, N.K., Lee, M., Ji, H., Bhat, K.P., Hollingsworth, F., Aldape, K.D., Schumacher, M.A., Zwaka, T.P., McCrea, P.D. Caspase-3 cleavage links delta-catenin to the novel nuclear protein ZIFCAT. J Biol Chem., 286(26):23178-88, 2011.

Colman, H., Zhang, L., Sulman, E.P., McDonald, J.M., Shooshtari, N.L., Rivera, A., Popoff, S., Nutt, C.L., Louis, D.N., Cairncross, J.G., Gilbert, M.R., Phillips, H.S., Mehta, M.P., Chakravarti, A., Pelloski, C.E., Bhat, K., Feuerstein, B.G., Jenkins, R.B., Aldape, K. A multigene predictor of outcome in glioblastoma. Neuro Oncol., 12(1):49-57, 2010.

Macias, E., Jin, A., Deisenroth, C., Bhat, K.P., Mao, H., Lindström, M.S., Zhang, Y. Mdm2 zinc finger is essential for ribosomal protein mediated stabilization of p53 and suppression of Myc-induced lymphomagenesis. Cancer Cell, 18(3):231-43, 2010.

Noushmehr, H., Weisenberger, D.J., Diefes, K., Phillips, H.S., Pujara, K., Berman, B.P., Pan, F., Pelloski, C.E., Sulman, E.P., Bhat, K.P., Verhaak, R.G., Hoadley, K.A., Hayes, D.N., Perou, C.M., Schmidt, H.K., Ding, L., Wilson, R.K., Van Den Berg, D., Shen, H., Bengtsson, H., Neuvial, P., Cope, L.M., Buckley, J., Herman, J.G., Baylin, S.B., Laird, P.W., Aldape, K; The Cancer Genome Atlas Research Network.  Identification of a CpG Island Methylator Phenotype that Defines a Distinct Subgroup of Glioma. Cancer Cell, 17(5):510-22, 2010.

Martin, V., Xu, J., Pabbisetty, S.K., Alonso, M.M., Liu, D., Lee, O.H., Gumin, J., Bhat, K.P., Colman, H., Lang, F.F., Fueyo, J., Gomez-Manzano, C. Tie2-mediated multidrug resistance in malignant gliomas is associated with upregulation of ABC transporters. Oncogene, 28(24):2358-63, 2009.