Heide Ford, PhD

Publications

• Patrick AN, Cabrera JH, Smith AL, Chen XS, Ford HL, Zhao R. Structure-function analyses of the human SIX1-EYA2 complex reveal insights into metastasis and BOR syndrome. Nat Struct Mol Biol. 2013 Apr;20(4):447-53. PubMed PMID: 23435380
• Auvergne RM, Sim FJ, Wang S, Chandler-Militello D, Burch J, Al Fanek Y, Davis D, Benraiss A, Walter K, Achanta P, Johnson M, Quinones-Hinojosa A, Natesan S, Ford HL, Goldman SA. Transcriptional differences between normal and glioma-derived glial progenitor cells identify a core set of dysregulated genes. Cell Rep. 2013 Jun 27;3(6):2127-41. PubMed PMID: 23727239
• Cieply B, Farris J, Denvir J, Ford HL, Frisch SM. Epithelial-mesenchymal transition and tumor suppression are controlled by a reciprocal feedback loop between ZEB1 and Grainyhead-like-2. Cancer Res. 2013 Oct 15;73(20):6299-309. PubMed PMID: 23943797
• Kohrt D, Crary J, Zimmer M, Patrick AN, Ford HL, Hinds PW, Grossel MJ. CDK6 binds and promotes the degradation of the EYA2 protein. Cell Cycle. 2014 Jan 1;13(1):62-71. PubMed PMID: 24196439
• O'Brien JH, Hernandez-Lagunas L, Artinger KB, Ford HL. MicroRNA-30a regulates zebrafish myogenesis via targeting the transcription factor Six1. J Cell Sci. 2014 Mar 14. [Epub ahead of print] PubMed PMID: 24634509
• Chapter 17: Neural crest cells and cancer: insights into tumor progression, in Neural Crest, P. Trainor, (Ed.), San Diego: Elsevier.
• Blevins MA, Towers CG, Patrick AN, Zhao R, Ford HL. The SIX1-EYA transcriptional complex as a therapeutic target in cancer. Expert Opin Ther Targets. 2015 Feb;19(2):213-25. PubMed PMID: 25555392
• Neelakantan D, Drasin DJ, Ford HL. Intratumoral heterogeneity: Clonal cooperation in epithelial-to-mesenchymal transition and metastasis. Cell Adh Migr. 2014 Oct 16;:0. [Epub ahead of print] PubMed PMID: 25482627
• Wang CA, Harrell JC, Iwanaga R, Jedlicka P, Ford HL. Vascular endothelial growth factor C promotes breast cancer progression via a novel antioxidant mechanism that involves regulation of superoxide dismutase 3. Breast Cancer Res. 2014 Oct 30;16(5):462. PubMed PMID: 25358638
• Towers CG, Guarnieri AL, Micalizzi DS, Harrell JC, Gillen AE, Kim J, Wang CA, Oliphant MU, Drasin DJ, Guney MA, Kabos P, Sartorius CA, Tan AC, Perou CM, Espinosa JM, Ford HL. The Six1 oncoprotein downregulates p53 via concomitant regulation of RPL26 and microRNA-27a-3p. Nat Commun. 2015 Dec 21;6:10077. PubMed PMID: 26687066
• Drasin DJ, Guarnieri AL, Neelakantan D, Kim J, Cabrera JH, Wang CA, Zaberezhnyy V, Gasparini P, Cascione L, Huebner K, Tan AC, Ford HL. TWIST1-Induced miR-424 Reversibly Drives Mesenchymal Programming while Inhibiting Tumor Initiation. Cancer Res. 2015 May 1;75(9):1908-21. PubMed PMID: 25716682
• Blevins MA, Towers CG, Patrick AN, Zhao R, Ford HL. The SIX1-EYA transcriptional complex as a therapeutic target in cancer. Expert Opin Ther Targets. 2015 Feb;19(2):213-25. PubMed PMID: 25555392
• Neelakantan D, Drasin DJ, Ford HL. Intratumoral heterogeneity: Clonal cooperation in epithelial-to-mesenchymal transition and metastasis. Cell Adh Migr. 2015;9(4):265-76. PubMed PMID: 25482627
• Wang CA, Drasin D, Pham C, Jedlicka P, Zaberezhnyy V, Guney M, Li H, Nemenoff R, Costello JC, Tan AC, Ford HL. Homeoprotein Six2 promotes breast cancer metastasis via transcriptional and epigenetic control of E-cadherin expression. Cancer Res. 2014 Dec 15;74(24):7357-70. PubMed PMID: 25348955
• Dimberg L, Towers CG, Behbakht K, Hotz T, Kim J, Fosmire SP, Porter CC, Tan AC, Thorburn A, Ford HL. A genome-wide loss-of-function screen identifies SLC26A2 as a novel mediator of TRAIL resistance. Mol Cancer Res. 2017 Jan 20. [Epub ahead of print] PubMed PMID: 28108622
• Kendrick AA, Schafer J, Dzieciatkowska M, Nemkov T, Alessandro AD, Neelakantan D, Ford HL, Pearson CG, Weekes CD, Hansen KC, Eisenmesser EZ. CD147: a small molecule transporter ancillary protein at the crossroad of multiple hallmarks of cancer and metabolic reprogramming. Oncotarget. 2016 Dec 27. [Epub ahead of print] PubMed PMID: 28039486
• Thorburn J, Staskiewicz L, Goodall ML, Dimberg L, Frankel AE, Ford HL, Thorburn A. Non-cell-autonomous Effects of Autophagy Inhibition in Tumor Cells Promote Growth of Drug-resistant Cells. Mol Pharmacol. 2017 Jan;91(1):58-64. PubMed PMID: 27974637
• Zhou H, Neelakantan D, Ford HL. Clonal cooperativity in heterogenous cancers. Semin Cell Dev Biol. 2016 Aug 28. [Epub ahead of print] PubMed PMID: 27582427
• Towers CG, Ford HL. A tale of two ends. Cell Cycle. 2016 Jun 17;15(12):1523-4. PubMed PMID: 27101085
• Krueger AB, Drasin DJ, Lea WA, Patrick AN, Patnaik S, Backos DS, Matheson CJ, Hu X, Barnaeva E, Holliday MJ, Blevins MA, Robin TP, Eisenmesser EZ, Ferrer M, Simeonov A, Southall N, Reigan P, Marugan J, Ford HL, Zhao R. Allosteric inhibitors of the Eya2 phosphatase are selective and inhibit Eya2-mediated cell migration. J Biol Chem. 2014 Jun 6;289(23):16349-61. PubMed PMID: 24755226
• Zhou H, Zhang L, Vartuli RL, Ford HL, Zhao R. The Eya phosphatase: Its unique role in cancer. Int J Biochem Cell Biol. 2018 Mar;96:165-170. PubMed PMID: 28887153
• O'Brien JH, Hernandez-Lagunas L, Artinger KB, Ford HL. MicroRNA-30a regulates zebrafish myogenesis through targeting the transcription factor Six1. J Cell Sci. 2014 May 15;127(Pt 10):2291-301. PubMed PMID: 24634509
• Neelakantan D, Zhou H, Oliphant MUJ, Zhang X, Simon LM, Henke DM, Shaw CA, Wu MF, Hilsenbeck SG, White LD, Lewis MT, Ford HL. EMT cells increase breast cancer metastasis via paracrine GLI activation in neighbouring tumour cells. Nat Commun. 2017 Jun 12;8:15773. PubMed PMID: 28604738
• Kohrt D, Crary J, Zimmer M, Patrick AN, Ford HL, Hinds PW, Grossel MJ. CDK6 binds and promotes the degradation of the EYA2 protein. Cell Cycle. 2014;13(1):62-71. PubMed PMID: 24196439
• Tavares ALP, Cox TC, Maxson RM, Ford HL, Clouthier DE. Negative regulation of endothelin signaling by SIX1 is required for proper maxillary development. Development. 2017 Jun 1;144(11):2021-2031. PubMed PMID: 28455376
• Dimberg LY, Towers CG, Behbakht K, Hotz TJ, Kim J, Fosmire S, Porter CC, Tan AC, Thorburn A, Ford HL. A Genome-Wide Loss-of-Function Screen Identifies SLC26A2 as a Novel Mediator of TRAIL Resistance. Mol Cancer Res. 2017 Apr;15(4):382-394. PubMed PMID: 28108622
• Kendrick AA, Schafer J, Dzieciatkowska M, Nemkov T, D'Alessandro A, Neelakantan D, Ford HL, Pearson CG, Weekes CD, Hansen KC, Eisenmesser EZ. CD147: a small molecule transporter ancillary protein at the crossroad of multiple hallmarks of cancer and metabolic reprogramming. Oncotarget. 2017 Jan 24;8(4):6742-6762. PubMed PMID: 28039486
• Thorburn J, Staskiewicz L, Goodall ML, Dimberg L, Frankel AE, Ford HL, Thorburn A. Non-cell-autonomous Effects of Autophagy Inhibition in Tumor Cells Promote Growth of Drug-resistant Cells. Mol Pharmacol. 2017 Jan;91(1):58-64. PubMed PMID: 27974637
• Zhou H, Neelakantan D, Ford HL. Clonal cooperativity in heterogenous cancers. Semin Cell Dev Biol. 2017 Apr;64:79-89. PubMed PMID: 27582427
• Zhang, L., Zhou, H., Li, X., Vartuli, R., Rowse, M., Xing, Y., Rudra, P., Ghosh, D., Zhao, R.*, Ford, H.L.* (2018). Eya3 partners with PP2A to induce c-Myc stabilization and tumor progression. In Press Nature Communications. *co-corresponding authors
• Oliphant MUJ, Vincent MY, Galbraith MD, Pandey A, Zaberezhnyy V, Rudra P, Johnson KR, Costello JC, Ghosh D, DeGregori J, Espinosa JM, Ford HL. Six2 mediates late-stage metastasis via direct regulation of Sox2 and induction of a cancer stem cell program. Cancer Res. 2019 Jan 3. [Epub ahead of print] PubMed PMID: 30606720
• Vartuli RL, Zhou H, Zhang L, Powers RK, Klarquist J, Rudra P, Vincent MY, Ghosh D, Costello JC, Kedl RM, Slansky JE, Zhao R, Ford HL. Eya3 promotes breast tumor-associated immune suppression via threonine phosphatase-mediated PD-L1 upregulation. J Clin Invest. 2018 Jun 1;128(6):2535-2550. PubMed PMID: 29757193
• Guarnieri AL, Towers CG, Drasin DJ, Oliphant MUJ, Andrysik Z, Hotz TJ, Vartuli RL, Linklater ES, Pandey A, Khanal S, Espinosa JM, Ford HL. The miR-106b-25 cluster mediates breast tumor initiation through activation of NOTCH1 via direct repression of NEDD4L. Oncogene. 2018 Jul;37(28):3879-3893. PubMed PMID: 29662198
• Zhang L, Zhou H, Li X, Vartuli RL, Rowse M, Xing Y, Rudra P, Ghosh D, Zhao R, Ford HL. Eya3 partners with PP2A to induce c-Myc stabilization and tumor progression. Nat Commun. 2018 Mar 13;9(1):1047. PubMed PMID: 29535359
• Zhou H, Zhang L, Vartuli RL, Ford HL, Zhao R. The Eya phosphatase: Its unique role in cancer. Int J Biochem Cell Biol. 2018 Mar;96:165-170. PubMed PMID: 28887153
• Oliphant MUJ, Vincent MY, Galbraith MD, Pandey A, Zaberezhnyy V, Rudra P, Johnson KR, Costello JC, Ghosh D, DeGregori J, Espinosa JM, Ford HL. SIX2 Mediates Late-Stage Metastasis via Direct Regulation of SOX2 and Induction of a Cancer Stem Cell Program. Cancer Res. 2019 Feb 15;79(4):720-734. PubMed PMID: 30606720
• Anantharajan J, Zhou H, Zhang L, Hotz T, Vincent MY, Blevins MA, Jansson AE, Kuan JWL, Ng EY, Yeo YK, Baburajendran N, Lin G, Hung AW, Joy J, Patnaik S, Marugan J, Rudra P, Ghosh D, Hill J, Keller TH, Zhao R, Ford HL, Kang C. Structural and Functional Analyses of an Allosteric EYA2 Phosphatase Inhibitor That Has On-Target Effects in Human Lung Cancer Cells. Mol Cancer Ther. 2019 Sep;18(9):1484-1496. PubMed PMID: 31285279
• Sheng, G, Antin, P, Berx, G, Blanpain, C, Brabletz, T, Bronner, M, Campbell, K, Cano, A, Christofori, G, Dedhar, S, Derynck, R, Ford, HL, Garcia de Herreros, A, Goodall, G, Hadjantonakis, A-K, Huang, R, Kalcheim, C, Kalluri, R, Kang, Y, Khew-Goodal, Y, Levine, H, Liu, J, Longmore, GD, Mani, SA, Massagué, J, Mayor, R, McClay, D, Newgreen, DF, Nieto, MA, Puisieux, A, Runyan, R, Savagner, P, Stanger, B, Stemmler, M, Takahashi, Y, Thiery, JP, Thompson, EW, Weinberg, RA, Williams, E, Xing, J, Zhou, BP, and Yang, J. (2019). Definitions and Guidelines for Research on Epithelial-Mesenchymal Transition. Nature Reviews Molecular Cell Biology. In Press.
• Kong D, Zhou H, Neelakantan D, Hughes CJ, Hsu JY, Srinivasan RR, Lewis MT, Ford HL. VEGF-C mediates tumor growth and metastasis through promoting EMT-epithelial breast cancer cell crosstalk. Oncogene. 2020 Dec 9. [Epub ahead of print] PubMed PMID: 33299122
• Kong D, Hughes CJ, Ford HL. Cellular Plasticity in Breast Cancer Progression and Therapy. Front Mol Biosci. 2020;7:72. PubMed PMID: 32391382
• Anantharajan J, Baburajendran N, Lin G, Loh YY, Xu W, Ahmad NHB, Liu S, Jasson AE, Kuan JWL, Ng EY, Yeo YK, Hung AW, Joy J, Hill J, Ford HL, Zhao R, Keller TH, Kang C. Structure-activity relationship studies of allosteric inhibitors of EYA2 tyrosine phosphatase. Protein Sci. 2021 Nov 11. [Epub ahead of print] PubMed PMID: 34761455
• Zhang G, Dong Z, Gimple RC, Wolin A, Wu Q, Qiu Z, Wood LM, Shen JZ, Jiang L, Zhao L, Lv D, Prager BC, Kim LJY, Wang X, Zhang L, Anderson RL, Moore JK, Bao S, Keller TH, Lin G, Kang C, Hamerlik P, Zhao R, Ford HL, Rich JN. Targeting EYA2 tyrosine phosphatase activity in glioblastoma stem cells induces mitotic catastrophe. J Exp Med. 2021 Nov 1;218(11). PubMed PMID: 34617969
• Zhou H, Blevins MA, Hsu JY, Kong D, Galbraith MD, Goodspeed A, Culp-Hill R, Oliphant MUJ, Ramirez D, Zhang L, Trinidad-Pineiro J, Mathews Griner L, King R, Barnaeva E, Hu X, Southall NT, Ferrer M, Gustafson DL, Regan DP, D'Alessandro A, Costello JC, Patnaik S, Marugan J, Zhao R, Ford HL. Identification of a Small-Molecule Inhibitor That Disrupts the SIX1/EYA2 Complex, EMT, and Metastasis. Cancer Res. 2020 Jun 15;80(12):2689-2702. PubMed PMID: 32341035
• Kong D, Zhou H, Neelakantan D, Hughes CJ, Hsu JY, Srinivasan RR, Lewis MT, Ford HL. VEGF-C mediates tumor growth and metastasis through promoting EMT-epithelial breast cancer cell crosstalk. Oncogene. 2021 Feb;40(5):964-979. PubMed PMID: 33299122
• Hsu, JY, Danis, EP, Nance ,  O’Brien, J,   Wessells, VM, Goodspeed, AE, Talbot, JC, Amacher, SL, Jedlicka, P, Black, JC, Costello, JC, Durbin, AD, Artinger, KB*, Ford, HL.* (2021).  SIX1 Reprograms Myogenic Transcription Factors to Maintain the Rhabdomyosarcoma undifferentiated state.  BioRxiv 2021, In Press Cell Reports.  *co-corresponding authors
• Wilson, C, Mertens, TCJ, Bi, W, Collum, SD, Wareing, N, Ko, J, Weng, T, Naikawadi, RP, Wolters, PJ,  Maire, P, Jyothula, SSK, Rajagopal, K, Thandavarayan, RA, Bruckner, BA, Ren, D, Huang, HJ, Bailey, JM, Dickey, BF, Ford, HL, and Karmouty-Quintana, H. (2021).  Sine Oculis Homeobox Homolog 1    (Six1) is elevated in Idiopathic Pulmonary Fibrosis and its deletion from alveolar epithelial cells prevents and halts lung Fibrosis.  Revised version under review at JCI Insight. 
• Oliphant MUJ, Kong D, Zhou H, Lewis MT, Ford HL. Two Sides of the Same Coin: The Role of Developmental pathways and pluripotency factors in normal mammary stem cells and breast cancer metastasis. J Mammary Gland Biol Neoplasia. 2020 Jun;25(2):85-102. PubMed PMID: 32323111
• Yang J, Antin P, Berx G, Blanpain C, Brabletz T, Bronner M, Campbell K, Cano A, Casanova J, Christofori G, Dedhar S, Derynck R, Ford HL, Fuxe J, García de Herreros A, Goodall GJ, Hadjantonakis AK, Huang RJY, Kalcheim C, Kalluri R, Kang Y, Khew-Goodall Y, Levine H, Liu J, Longmore GD, Mani SA, Massagué J, Mayor R, McClay D, Mostov KE, Newgreen DF, Nieto MA, Puisieux A, Runyan R, Savagner P, Stanger B, Stemmler MP, Takahashi Y, Takeichi M, Theveneau E, Thiery JP, Thompson EW, Weinberg RA, Williams ED, Xing J, Zhou BP, Sheng G. Guidelines and definitions for research on epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2020 Jun;21(6):341-352. PubMed PMID: 32300252
• Hsu JY, Danis EP, Nance S, O'Brien JH, Gustafson AL, Wessells VM, Goodspeed AE, Talbot JC, Amacher SL, Jedlicka P, Black JC, Costello JC, Durbin AD, Artinger KB, Ford HL. SIX1 reprograms myogenic transcription factors to maintain the rhabdomyosarcoma undifferentiated state. Cell Rep. 2022 Feb 1;38(5):110323. PubMed PMID: 35108532
• Anantharajan J, Baburajendran N, Lin G, Loh YY, Xu W, Ahmad NHB, Liu S, Jansson AE, Kuan JWL, Ng EY, Yeo YK, Hung AW, Joy J, Hill J, Ford HL, Zhao R, Keller TH, Kang C. Structure-activity relationship studies of allosteric inhibitors of EYA2 tyrosine phosphatase. Protein Sci. 2022 Feb;31(2):422-431. PubMed PMID: 34761455
• Wilson C, Mertens TC, Shivshankar P, Bi W, Collum SD, Wareing N, Ko J, Weng T, Naikawadi RP, Wolters PJ, Maire P, Jyothula SS, Thandavarayan RA, Ren D, Elrod ND, Wagner EJ, Huang HJ, Dickey BF, Ford HL, Karmouty-Quintana H. Sine oculis homeobox homolog 1 plays a critical role in pulmonary fibrosis. JCI Insight. 2022 May 23;7(10). PubMed PMID: 35420997
• Hughes, CJ, Fields, KM, Danis, E, Hsu, JY, Neelakantan, D, Vincent, MY, Gustafson, A, Oliphant, MUJ, Sreekanth, V, Zaberezhnyym V, Costello, JC, Jedlicka, P, and Ford, HL (2023). SIX1 and EWS/FLI1 co-regulate an anti-metastatic gene network in Ewing Sarcoma. Nature Communications 14: 4357.
• Wolin AR, Vincent MY, Hotz T, Purdy SC, Rosenbaum SR, Hughes CJ, Hsu JY, Oliphant MUJ, Armstrong B, Wessells V, Varella-Garcia M, Galbraith MD, Pierce A, Wang D, Venkataraman S, Danis E, Veo B, Serkova N, Espinosa JM, Gustafson DL, Vibhakar R, Ford HL. EYA2 tyrosine phosphatase inhibition reduces MYC and prevents medulloblastoma progression. Neuro Oncol. 2023 Dec 8;25(12):2287-2301. PubMed PMID: 37486991
• Alderman C, Krueger A, Rossi J, Ford HL, Zhao R. In Vitro Phosphatase Assays for the Eya2 Tyrosine Phosphatase. Methods Mol Biol. 2024;2743:285-300. PubMed PMID: 38147222