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Publications

François-Moutal L, Scott DD, Ambrose AJ, Zerio CJ, Rodriguez-Sanchez M, Dissanayake K, May DG, Carlson JM, Barbieri E, Moutal A, Roux KJ, Shorter J, Khanna R, Barmada SJ, McGurk L, Khanna M. Heat shock protein Grp78/BiP/HspA5 binds directly to TDP-43 and mitigates toxicity associated with disease pathology. Sci Rep. 2022 May 17;12(1):8140. doi: 10.1038/s41598-022-12191-8

Tello JA, Williams HE, Eppler RM, Steinhilb ML, Khanna M. Animal Models of Neurodegenerative Disease: Recent Advances in Fly Highlight Innovative Approaches to Drug Discovery. Front Mol Neurosci. 2022 Apr 19;15:883358. doi:10.3389/fnmol.2022.883358

Mollasalehi N, Francois-Moutal L, Porciani D, Burke DH, Khanna M. Aptamers Targeting Hallmark Proteins of Neurodegeneration. Nucleic Acid Ther. 2022 Apr 22. doi: 10.1089/nat.2021.0091

Cai S, Moutal A, Yu J, Chew LA, Isensee J, Chawla R, Gomez K, Luo S, Zhou Y, Chefdeville A, Madura C, Perez-Miller S, Bellampalli SS, Dorame A, Scott DD, François-Moutal L, Shan Z, Woodward T, Gokhale V, Hohmann AG, Vanderah TW, Patek M, Khanna M, Hucho T, Khanna R. Selective targeting of NaV1.7 via inhibition of the CRMP2-Ubc9 interaction reduces pain in rodents. Sci Transl Med. 2021 Nov 10;13(619):eabh1314. doi:10.1126/scitranslmed.abh1314

Iwanski J, Kazmouz SG, Li S, Stansfield B, Salem TT, Perez-Miller S, Kazui T, Jena L, Uhrlaub JL, Lick S, Nikolich-Žugich J, Konhilas JP, Gregorio CC, Khanna M, Campos SK, Churko JM. Antihypertensive drug treatment and susceptibility to SARS-CoV-2 infection in human PSC-derived cardiomyocytes and primary endothelial cells. Stem Cell Reports. 2021 Oct 12;16(10):2459-2472. doi:10.1016/j.stemcr.2021.08.018

Francois-Moutal L, Scott DD, Khanna M. Direct targeting of TDP-43, from small molecules to biologics: the therapeutic landscape. RSC Chem Biol. 2021 Jun 21;2(4):1158-1166. doi: 10.1039/d1cb00110h

François-Moutal L, Miranda VG, Mollasalehi N, Gokhale V, Khanna M. In Silico Targeting of the Long Noncoding RNA MALAT1. ACS Med Chem Lett. 2021 Apr 1;12(6):915-921. doi: 10.1021/acsmedchemlett.1c00060

Mollasalehi N, Francois-Moutal L, Scott DD, Tello JA, Williams H, Mahoney B, Carlson JM, Dong J, Li X, Miranda VG, Gokhale V, Wang W, Barmada SJ, Khanna M. An Allosteric Modulator of RNA Binding Targeting the N-Terminal Domain of TDP-43 Yields Neuroprotective Properties. ACS Chemical Biology 2020 15 (11), 2854-2859 doi: 10.1021/acschembio.0c00494 

Kump JK, Miao L, Mady ASA, Ansari NH, Shrestha UK, Yang Y, Pal M, Liao C, Perdih A, Abulwerdi FA, Chinnaswamy K, Meagher JL, Carlson JM, Khanna M, Stuckey JA, Nikolovska-Coleska Z. Discovery and Characterization of 2,5-Substituted Benzoic Acid Dual Inhibitors of the Anti-Apoptotic Mcl-1 and Bfl-1 Proteins. J Medicinal Chem (2020) doi: 10.1021/acs.jmedchem.9b01442

François-Moutal L, Perez-Miller S, Scott DD, Miranda VG, Mollasalehi N, Khanna M. Structural Insights Into TDP-43 and Effects of Post-translational Modifications. Front Mol Neurosci (2019) doi: 10.3389/fnmol.2019.00301

François-Moutal L, Felemban R, Scott DD, Sayegh MR, Miranda VG, Perez-Miller S, Khanna R, Gokhale V, Zarnescu DC, Khanna M. Small Molecule Targeting TDP-43’s RNA Recognition Motifs Reduces Locomotor Defects in a Drosophila Model of Amyotrophic Lateral Sclerosis (ALS). ACS Chem Biol (2019) 14(9):2006-2013. doi: 10.1021/acschembio.9b00481

Khanna R, Yu J, Yang X, Moutal A, Chefdeville A, Gokhale V, Shuja Z, Chew LA, Bellampalli SS, Luo S, François-Moutal L, Serafini MJ, Ha T, Perez-Miller S, Park KD, Patwardhan AM, Streicher JM, Colecraft HM, Khanna M. Targeting the CaVα-CaVβ interaction yields an antagonist of the N-type CaV2.2 channel with broad antinociceptive efficacy. Pain (2019) 160(7):1644-1661. doi: 10.1097/j.pain.0000000000001524

Scott DD, Francois-Moutal L, Kumirov VK, Khanna M.  1H, 15N and 13C backbone assignment of apo TDP-43 RNA recognition motifs. Biomol NMR Assign (2019) 13(1):163-167. doi: 10.1007/s12104-018-09870-x

Katz DS, Allen G, Barba LA, Berg DR, Bik H, Boettiger C, Borgman CL, Brown CT, Buck S, Burd R, de Waard A, Eve MP, Granger BE, Greenberg J, Howe A, Howe B, Khanna M, Killeen TL, Mayernik M, McKiernan E, Mentzel C, Merchant N, Niemeyer KE, Noren L, Nusser SM, Reed DA, Seidel E, Smith M, Spies JR, Turk M, Van Horn JD, Walsh J. The principles of tomorrow's university. F1000Res. (2018) 7:1926. doi: 10.12688/f1000research.17425.1. eCollection 2018

Cai S, Bellampalli SS, Yu J, Li W, Ji Y, Wijeratne EMK, Dorame A, Luo S, Shan Z, Khanna M, Moutal A, Streicher JM, Gunatilaka AAL, Khanna R. (-)-Hardwickiic Acid and Hautriwaic Acid Induce Antinociception via Blockade of Tetrodotoxin-Sensitive Voltage-Dependent Sodium Channels. ACS Chem Neurosci (2019) 10(3):1716-1728. doi: 10.1021/acschemneuro.8b00617.

Bellampalli SS, Ji Y, Moutal A, Cai S, Wijeratne EMK, Gandini MA, Yu J, Chefdeville A, Dorame A, Chew LA, Madura CL, Luo S, Molnar G, Khanna M, Streicher JM, Zamponi GW, Gunatilaka AAL, Khanna R. Betulinic acid, derived from the desert lavender Hyptis emoryi, attenuates paclitaxel-, HIV-, and nerve injury-associated peripheral sensory neuropathy via block of N- and T-type calcium channels. Pain (2019) 160(1):117-135. doi: 10.1097/j.pain.0000000000001385

François-Moutal L, Jahanbakhsh S, Nelson A, Ray D, Scott DD, Hennefarth MR, Moutal A, Perez-Miller S, Al-Shamari A, Coursodon P, Meechoovet B, Reiman R, Lyons E, Beilstein M, Morris QD, Van Keuren-Jensen K, Hughes TR, Khanna R, Koehler C, Jen Joanna, Gokhale V, Khanna M. A Chemical Biology Approach to Model Pontocerebellar Hypoplasia Type 1B (PCH1B). ACS Chem Biol. (2018) 13(10):3000-3010. doi: 10.1021/acschembio.8b00745

Hurst SE, Liktor-Busa E, Moutal A, Parker S, Rice S, Szelinger S, Senner G, Hammer M, Johnstone L, Ramsey K, Narayanan V, Perez-Miller S, Khanna M, Dahlin H, Lewis K, Craig D, Wang EH, Khanna R, Nelson MA.  A novel TAF1 variant affects gene expression and is associated with x-linked TAF1 intellectual disability syndrome.  Neuronal Signaling (2018) 2(3):NS20180141. doi: 10.1042/NS20180141

François-Moutal L, Scott DD, Perez-Miller S, Gokhale V, Khanna M, Khanna R.  Chemical shift perturbation mapping of the Ubc9-CRMP2 interface identifies a pocket in CRMP2 amenable for allosteric modulation of Nav1.7 channels.   

Channels (2018) 12(1):219-227. doi: 10.1080/19336950.2018.1491244

François-Moutal L, Dustrude ET, Wang Y, Brustovetsky T, Dorame A, Ju W, Moutal A, Perez-Miller S, Brustovetsky N, Gokhale V, Khanna M, Khanna R.  Inhibition of the Ubc9 E2 SUMO conjugating enzyme-CRMP2 interaction decreases NaV1.7 currents and reverses experimental neuropathic pain. Pain. 2018 159(10):2115-2127. doi: 10.1097/j.pain.0000000000001294

Moutal A, Yang X, Li W, Gilbraith KB, Luo S, Cai S, François-Moutal L, Chew LA, Yeon SK, Bellampalli SS, Qu C, Xie JY, Ibrahim MM, Khanna M, Park KD, Porreca F, Khanna R.  CRISPR/Cas9 editing of Nf1 gene identifies CRMP2 as a therapeutic target in neurofibromatosis type 1-related pain that is reversed by (S)-Lacosamide. Pain. 2017; 158(12):2301-2319. doi: 10.1097/j.pain.0000000000001002

Moutal A, Li W, Wang Y, Ju W, Luo S, Cai S, François-Moutal L, Perez-Miller S, Hu J, Dustrude ET, Vanderah TW, Gokhale V, Khanna M, Khanna R. Homology-guided mutational analysis reveals the functional requirements for antinociceptive specificity of CRMP2-derived peptides. Br J Pharmacol. 2018; 175(12):2244-2260. doi: 10.1111/bph.13737.

Dustrude ET, Moutal A, Yang X, Wang Y, Khanna M, Khanna R. Hierarchical CRMP2 posttranslational modifications control NaV1.7 function.  Proc Natl Acad Sci U S A. 2016; 113(52):E8443-E8452. doi: 10.1073/pnas.1610531113

Dustrude ET, Perez-Miller S, François-Moutal, Moutal A, Khanna M, Khanna R.  A single structurally conserved SUMOylation site in CRMP2 controls NaV1.7 function.  Channels. 2017; 11(4):316-328. doi: 10.1080/19336950.2017.1299838

Xie JY, Chew LA, Yang X, Wang Y, Qu C, Wang Y, Federici LM, Fitz SD, Ripsch MS, Due MR, Moutal A, Khanna M, White FA, Vanderah TW, Johnson PL, Porreca F, Khanna R. Sustained relief of ongoing experimental neuropathic pain by a CRMP2 peptide aptamer with low abuse potential. Pain. 2016; 157(9):2124-40. doi: 10.1097/j.pain.0000000000000628

Moutal A, Chew LA, Yang X, Wang Y, Yeon SK, Telemi E, Meroueh S, Park KD, Shrinivasan R, Gilbraith KB, Qu C, Xie JY, Patwardhan A, Vanderah TW, Khanna M, Porreca F, Khanna R. (S)-lacosamide inhibition of CRMP2 phosphorylation reduces postoperative and neuropathic pain behaviors through distinct classes of sensory  neurons identified by constellation pharmacology. Pain. 2016; 157(7):1448-63. doi: 10.1097/j.pain.0000000000000555

Moutal A, François-Moutal L, Perez-Miller S, Cottier K, Chew LA, Yeon SK, Dai J, Park KD, Khanna M, Khanna R. (S)-Lacosamide Binding to Collapsin Response Mediator Protein 2 (CRMP2) Regulates CaV2.2 Activity by Subverting Its Phosphorylation by Cdk5. Mol Neurobiol. 2016; 53(3):1959-76. doi: 10.1007/s12035-015-9141-2

François-Moutal L, Wang Y, Moutal A, Cottier KE, Melemedjian OK, Yang X, Wang Y, Ju W, Largent-Milnes TM, Khanna M, Vanderah TW, Khanna R. A membrane-delimited N-myristoylated CRMP2 peptide aptamer inhibits CaV2.2 trafficking and reverses inflammatory and postoperative pain behaviors. Pain. 2015; 156(7):1247-64. doi: 10.1097/j.pain.0000000000000147

Moutal A, François-Moutal L, Brittain JM, Khanna M, Khanna R. Differential neuroprotective potential of CRMP2 peptide aptamers conjugated to cationic, hydrophobic, and amphipathic cell penetrating peptides. Front Cell Neurosci. 2015; 8:471. doi: 10.3389/fncel.2014.00471

Yan C, Liu D, Li L, Wempe MF, Guin S, Khanna M, Meier J, Hoffman B, Owens C, Wysoczynski CL, Nitz MD, Knabe WE, Ahmed M, Brautigan DL, Paschal BM, Schwartz MA, Jones DN, Ross D, Meroueh SO, Theodorescu D. Discovery and characterization of small molecules that target the GTPase Ral. Nature. 2014; 515(7527):443-7. doi: 10.1038/nature13713

Wilson SM, Moutal A, Melemedjian OK, Wang Y, Ju W, François-Moutal L, Khanna M, Khanna R. The functionalized amino acid (S)-Lacosamide subverts CRMP2-mediated tubulin polymerization to prevent constitutive and activity-dependent increase in neurite outgrowth. Front Cell Neurosci. 2014; 8:196. doi: 10.3389/fncel.2014.00196

Chikwana VM, Khanna M, Baskaran S, Tagliabracci VS, Contreras CJ, DePaoli-Roach A, Roach PJ, Hurley TD. Structural basis for 2'-phosphate incorporation into glycogen by glycogen synthase. Proc Natl Acad Sci U S A. 2013; 110(52):20976-81. doi: 10.1073/pnas.1310106111

 

Quach TT, Wilson SM, Rogemond V, Chounlamountri N, Kolattukudy PE, Martinez S, Khanna M, Belin MF, Khanna R, Honnorat J, Duchemin AM. Mapping CRMP3 domains involved in dendrite morphogenesis and voltage-gated calcium channel regulation.  J Cell Sci. 2013; 126(Pt 18):4262-73. doi: 10.1242/jcs.131409

Khanna M, Imasaki T, Chikwana VM, Perez-Miller S, Hunter GO, Mosley A, Takagi Y, Hurley TD. Expression and purification of functional human glycogen synthase-1 (hGYS1) in insect cells. Protein Expr Purif. 2013; 90(2):78-83. doi: 10.1016/j.pep.2013.05.007

Mani T, Wang F, Knabe WE, Sinn AL, Khanna M, Jo I, Sandusky GE, Sledge GW Jr, Jones DR, Khanna R, Pollok KE, Meroueh SO. Small-molecule inhibition of the uPAR·uPA interaction: synthesis, biochemical, cellular, in vivo pharmacokinetics and efficacy studies in breast cancer metastasis. Bioorg Med Chem. 2013; 21(7):2145-55. doi: 10.1016/j.bmc.2012.12.047

Piekarz AD, Due MR, Khanna M, Wang B, Ripsch MS, Wang R, Meroueh SO, Vasko MR, White FA, Khanna R. CRMP-2 peptide mediated decrease of high and low voltage-activated calcium channels, attenuation of nociceptor excitability, and anti-nociception in a model of AIDS therapy-induced painful peripheral neuropathy. Mol Pain. 2012; 8:54. doi: 10.1186/1744-8069-8-54

Wang F, Eric Knabe W, Li L, Jo I, Mani T, Roehm H, Oh K, Li J, Khanna M, Meroueh SO. Design, synthesis, biochemical studies, cellular characterization, and structure-based computational studies of small molecules targeting the urokinase receptor. Bioorg Med Chem. 2012; 20(15):4760-73.  doi: 10.1016/j.bmc.2012.06.002​

Ripsch MS, Ballard CJ, Khanna M, Hurley JH, White FA, Khanna R. A peptide uncoupling CRMP-2 from the presynaptic Ca(2+) channel complex demonstrates efficacy in animal models of migrane and aids therapy-oinduced neuropathy. Transl Neurosci. 2012; 3(1):1-8. doi: 10.2478/s13380-012-0002-4

Theimer CA, Smith NL, Khanna M. NMR studies of protein-RNA interactions. Methods Mol Biol. 2012; 831:197-218. doi: 10.1007/978-1-61779-480-3_12

Brittain JM, Duarte DB, Wilson SM, Zhu W, Ballard C, Johnson PL, Liu N, Xiong W, Ripsch MS, Wang Y, Fehrenbacher JC, Fitz SD, Khanna M, Park CK, Schmutzler BS, Cheon BM, Due MR, Brustovetsky T, Ashpole NM, Hudmon A, Meroueh SO, Hingtgen CM, Brustovetsky N, Ji RR, Hurley JH, Jin X, Shekhar A, Xu XM, Oxford GS, Vasko MR, White FA, Khanna R. Suppression of inflammatory and neuropathic pain by uncoupling CRMP-2 from the presynaptic Ca²⁺ channel complex. Nat Med. 2011; 17(7):822-9. doi: 10.1038/nm.2345

Khanna M, Chelladurai B, Gavini A, Li L, Shao M, Courtney D, Turchi JJ, Matei D, Meroueh S. Targeting ovarian tumor cell adhesion mediated by tissue transglutaminase. Mol Cancer Ther. 2011; 10(4):626-36. doi: 10.1158/1535-7163.MCT-10-0912

Khanna M, Chen CH, Kimble-Hill A, Parajuli B, Perez-Miller S, Baskaran S, Kim J, Dria K, Vasiliou V, Mochly-Rosen D, Hurley TD. Discovery of a novel class of covalent inhibitor for aldehyde dehydrogenases. J Biol Chem. 2011; 286(50):43486-94. doi: 10.1074/jbc.M111.293597

Khanna M, Wang F, Jo I, Knabe WE, Wilson SM, Li L, Bum-Erdene K, Li J, W Sledge G, Khanna R, Meroueh SO. Targeting multiple conformations leads to small molecule inhibitors of the uPAR·uPA protein-protein interaction that block cancer cell invasion. ACS Chem Biol. 2011; 6(11):1232-43. doi: 10.1021/cb200180m

Li L, Khanna M, Jo I, Wang F, Ashpole NM, Hudmon A, Meroueh SO. Target-specific support vector machine scoring in structure-based virtual screening: computational validation, in vitro testing in kinases, and effects on lung cancer cell proliferation. J Chem Inf Model. 2011; 51(4):755-9. doi: 10.1021/ci100490w

Parajuli B, Kimble-Hill AC, Khanna M, Ivanova Y, Meroueh S, Hurley TD. Discovery of novel regulators of aldehyde dehydrogenase isoenzymes. Chem Biol Interact. 2011; 191(1-3):153-8. doi: 10.1016/j.cbi.2011.02.018

Wang F, Li J, Sinn AL, Knabe WE, Khanna M, Jo I, Silver JM, Oh K, Li L, Sandusky GE, Sledge GW, Nakshatri H, Jones DR, Pollok KE, Meroueh SO. Virtual screening targeting the urokinase receptor, biochemical and cell-based studies, synthesis, pharmacokinetic characterization, and effect on breast tumor metastasis. J Med Chem. 2011; 54(20):7193-205. doi: 10.1021/jm200782y

Wilson SM, Brittain JM, Piekarz AD, Ballard CJ, Ripsch MS, Cummins TR, Hurley JH, Khanna M, Hammes NM, Samuels BC, White FA, Khanna R. Further insights into the antinociceptive potential of a peptide disrupting the N-type calcium channel-CRMP-2 signaling complex. Channels (Austin). 2011; 5(5):449-56. doi: 10.4161/chan.5.5.17363

Allen EM, Anderson DG, Florang VR, Khanna M, Hurley TD, Doorn JA. Relative inhibitory potency of molinate and metabolites with aldehyde dehydrogenase 2: implications for the mechanism of enzyme inhibition. Chem Res Toxicol. 2010; 23(11):1843-50. doi: 10.1021/tx100317q

Li L, Li J, Khanna M, Jo I, Baird JP, Meroueh SO. Docking Small Molecules to Predicted Off-Targets of the Cancer Drug Erlotinib Leads to Inhibitors of Lung Cancer Cell Proliferation with Suitable In vitro Pharmacokinetic Properties. ACS Med Chem Lett. 2010; 1(5):229-233. doi: 10.1021/ml100031a

Khanna M, Van Bakel H, Tang X, Calarco JA, Babak T, Guo G, Emili A, Greenblatt JF, Hughes TR, Krogan NJ, Blencowe BJ. A systematic characterization of Cwc21, the yeast ortholog of the human spliceosomal protein SRm300. RNA. 2009; 15(12):2174-85. doi: 10.1261/rna.1790509

Zhao R, Kakihara Y, Gribun A, Huen J, Yang G, Khanna M, Costanzo M, Brost RL, Boone C, Hughes TR, Yip CM, Houry WA. Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J Cell Biol. 2008; 180(3):563-78. doi: 10.1083/jcb.200709061

Blencowe BJ, Khanna M. Molecular biology: RNA in control. Nature. 2007;447(7143):391-3. doi: 10.1038/447391a

Khanna M, Wu H, Johansson C, Caizergues-Ferrer M, Feigon J. Structural study of the H/ACA snoRNP components Nop10p and the 3' hairpin of U65 snoRNA. RNA. 2006; 12(1):40-52. doi: 10.1261/rna.2221606

Chow CS, Cunningham PR, Lee K, Meroueh M, SantaLucia Jr. J, Varma S. Photoinduced Cleavage by a Rhodium Complex at G-U Mismatches and Exposed Guanines in Large and Small RNAs. Biochimie, 2002; 84(9):859-68. doi: 10.1016/S0300-9084(02)01403-7

Chui H. M, Meroueh M, Scaringe SA, Chow CS.  Synthesis of a 3-methyluridine phosphoramidite to investigate the role of methylation in a ribosomal RNA hairpin. Bioorg. Med. Chem. 2002; 10: 325-32. doi: 10.1016/S0968-0896(01)00283-8

Meroueh M, Grohar PJ, Qiu J, SantaLucia J Jr, Scaringe SA, Chow CS. Unique Structural and Stabilizing Roles for the Individual Pseudouridine Residues in the 1920 Region of Escherichia coli 23S rRNA. Nucleic Acids Res. 2000; 28: 2075-2083. PMID: 10773075

Meroueh M, Kjellström J, Mårtensson KSM, Elmroth SKC, Chow CS. Reactions of Platinum (II) Complexes with  a DNA hairpin, d(CGCGTTGTTCGCG): Structural Characterization  and Kinetic Studies.  Inorg. Chim. Acta 2000; 29: 145-155. doi: 10.1016/S0020-1693(99)00338-2

Meroueh M, Chow CS. Thermodynamics of RNA Hairpins Containing Single Internal Mismatches.  Nucleic Acids Res. 1999; 40: 2049-2052. PMID: 9927746

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