Recent Publications from Ford Laboratory/Collaborators (2012-2022)

https://www.ncbi.nlm.nih.gov/myncbi/heide.ford.1/bibliography/public/

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):e142984. doi: 10.1172/jci.insight.142984

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 Reports.  2022 Feb 1;38(5):110323.
 doi: 10.1016/j.celrep.2022.110323.

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.
 doi: 10.1002/pro.4234. Epub 2021 Nov 18.

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):e20202669. doi: 10.1084/jem.20202669. Epub 2021 Oct 7.

Kong, D*, Zhou H*, Neelakantan D, Hughes CJ, Hsu, JY, Srinivasan, RR, Lewis MT, and Ford, HL.  VEGF-C Enhances Tumor Growth and Metastasis through Mediating Crosstalk Between EMT and Epithelial Breast Cancer cells.  Oncogene. 2021 Feb;40(5):964-979. doi: 10.1038/s41388-020-01539-x. Epub 2020 Dec 9
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Kong D, Hughes CJ, Ford HL. Cellular Plasticity in Breast Cancer Progression and Therapy.  Front Mol Biosci. 2020 Apr 24;7:72. doi: 10.3389/fmolb.2020.00072. PMID: 32391382; PMCID: PMC7194153.

Zhou H, Blevins MA, Hsu JY, Kong D, Galbraith MD, Goodspeed A, Culp-Hill R, Oliphant MU, Ramirez D, Zhang L, Pineiro JT, 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. A SIX1/EYA2 small molecule inhibitor disrupts EMT and metastasis. Cancer Res. 2020;  80:2689-2702. doi: 10.1158/0008-5472.CAN-20-0435. PMID: 32341035.

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 25: 85-102.  doi: 10.1007/s10911-020-09449-0. Epub ahead of print. 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; EMT International Association (TEMTIA). Guidelines and definitions for research on epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2020; 21: 341-352.  doi: 10.1038/s41580-020-0237-9.  PMID: 32300252.

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; 9:1484-1496. doi: 10.1158/1535-7163.MCT-18-1239. Epub 2019 Jul 8. PMID: 31285279; PMCID: PMC6726557.

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. doi: 10.1158/0008-5472.CAN-18-1791. Epub 2019 Jan 3. PMID: 30606720; PMCID: PMC6586234.

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. doi: 10.1172/JCI96784. Epub 2018 May 14. PMID: 29757193; PMCID: PMC5983346.

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. doi: 10.1038/s41388-018-0239-7. Epub 2018 Apr 17. PMID: 29662198; PMCID: PMC6043359.

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. doi: 10.1038/s41467-018-03327-4. Erratum in: Nat Commun. 2018 Sep 17;9(1):3830. PMID: 29535359; PMCID: PMC5849647.

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. doi: 10.1016/j.biocel.2017.09.001. Epub 2017 Sep 5. PMID: 28887153; PMCID: PMC5808901.

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. doi: 10.1038/ncomms15773. PMID: 28604738; PMCID: PMC5472791.

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. doi: 10.1242/dev.145144. Epub 2017 Apr 28. PMID: 28455376; PMCID: PMC5482985.

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. doi: 10.1158/1541-7786.MCR-16-0234. Epub 2017 Jan 20. PMID: 28108622; PMCID: PMC5380511.

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. doi: 10.18632/oncotarget.14272. PMID: 28039486; PMCID: PMC5341751.

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. doi: 10.1124/mol.116.106070. Epub 2016 Nov 9. PMID: 27974637; PMCID: PMC5198514.

Zhou H, Neelakantan D, Ford HL. Clonal cooperativity in heterogenous cancers. Semin Cell Dev Biol. 2017 Apr;64:79-89. doi: 10.1016/j.semcdb.2016.08.028. Epub 2016 Aug 28. PMID: 27582427; PMCID: PMC5330947.

Towers CG, Ford HL. A tale of two ends. Cell Cycle. 2016 Jun 17;15(12):1523-4. doi: 10.1080/15384101.2016.1171652. Epub 2016 Apr 21. PMID: 27101085; PMCID: PMC4934064.

Towers CG, Guarnieri AL, Micalizzi DS, Harrell JC, Gillen AE, Kim J, Wang CA, Oliphant MUJ, 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. doi: 10.1038/ncomms10077. PMID: 26687066; PMCID: PMC4703841.

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. doi: 10.1158/0008-5472.CAN-14-2394. Epub 2015 Feb 25. PMID: 25716682; PMCID: PMC4417413.

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. doi: 10.1517/14728222.2014.978860. Epub 2015 Jan 2. PMID: 25555392; PMCID: PMC4336540.

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. doi: 10.4161/19336918.2014.972761. Epub 2014 Oct 16. PMID: 25482627; PMCID: PMC4594578.

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. doi: 10.1158/0008-5472.CAN-14-0666. Epub 2014 Oct 27. PMID: 25348955; PMCID: PMC4268359.

Wang, C., Harrell, J.C, Iwanaga, R., Jedlicka, P. and Ford, H.L.  (2014).  VEGF-C promotes breast cancer         progression via a novel anti-oxidant mechanism that involves regulation of Superoxide dismutase 3.  Breast Cancer Research 16: 462.

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. doi: 10.1074/jbc.M114.566729. Epub 2014 Apr 22. PMID: 24755226; PMCID: PMC4047403.

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. doi: 10.1242/jcs.143677. Epub 2014 Mar 14. PMID: 24634509; PMCID: PMC4021474.

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. doi: 10.4161/cc.26755. Epub 2013 Oct 12. PMID: 24196439; PMCID: PMC3925736.

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. doi: 10.1158/0008-5472.CAN-12-4082. Epub 2013 Aug 13. PMID: 23943797; PMCID: PMC3806457.

Auvergne, R.M., Sim, F.R., 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, H.L., and Goldman, S.A. (2013).  Transcriptional Differences between normal and glioma-derived glial   progenitor cells identify a core set of dysregulated genes. Cell Reports 3: 2127-2141. ​

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. doi: 10.1038/nsmb.2505. Epub 2013 Feb 24. PMID: 23435380; PMCID: PMC3618615.

Krueger AB, Dehdashti SJ, Southall N, Marugan JJ, Ferrer M, Li X, Ford HL, Zheng W, Zhao R. Identification of a selective small-molecule inhibitor series targeting the eyes absent 2 (Eya2) phosphatase activity. J Biomol Screen. 2013 Jan;18(1):85-96. doi: 10.1177/1087057112453936. Epub 2012 Jul 20. PMID: 22820394; PMCID: PMC3893891.

 Dimberg LY, Anderson CK, Camidge R, Behbakht K, Thorburn A, Ford HL. On the TRAIL to successful cancer therapy? Predicting and counteracting resistance against TRAIL-based therapeutics. Oncogene. 2013 Mar 14;32(11):1341-50. doi: 10.1038/onc.2012.164. Epub 2012 May 14. PMID: 22580613; PMCID: PMC4502956.

Robin TP, Smith A, McKinsey E, Reaves L, Jedlicka P, Ford HL. EWS/FLI1 regulates EYA3 in Ewing sarcoma via modulation of miRNA-708, resulting in increased cell survival and chemoresistance. Mol Cancer Res. 2012 Aug;10(8):1098-108. doi: 10.1158/1541-7786.MCR-12-0086. Epub 2012 Jun 20. PMID: 22723308; PMCID: PMC3432289.

Smith AL, Robin TP, Ford HL. Molecular pathways: targeting the TGF-β pathway for cancer therapy. Clin Cancer Res. 2012 Sep 1;18(17):4514-21. doi: 10.1158/1078-0432.CCR-11-3224. Epub 2012 Jun 18. PMID: 22711703.

Iwanaga, R., Wang, C., Micalizzi, D.S., J.C. Harrell, Jedlicka, P., Sartorius, C., Kabos, P., Farabaugh, S., Bradford, A., Ford, H.L. (2012). The Six1 Expression of Six1 in luminal breast cancers predicts poor  prognosis and promotes increases in tumor initiating cells by activation of ERK and TGF-b pathways.  Breast Cancer Res 14: R100 

Wang CA, Jedlicka P, Patrick AN, Micalizzi DS, Lemmer KC, Deitsch E, Casás- Selves M, Harrell JC, Ford HL. SIX1 induces lymphangiogenesis and metastasis via upregulation of VEGF-C in mouse models of breast cancer. J Clin Invest. 2012 May;122(5):1895-906. doi: 10.1172/JCI59858. Epub 2012 Apr 2. PMID: 22466647; PMCID: PMC3336979.

Qamar L, Deitsch E, Patrick AN, Post MD, Spillman MA, Iwanaga R, Thorburn A, Ford HL, Behbakht K. Specificity and prognostic validation of a polyclonal antibody to detect Six1 homeoprotein in ovarian cancer. Gynecol Oncol. 2012 May;125(2):451-7. doi: 10.1016/j.ygyno.2012.02.007. Epub 2012 Feb 12. PMID: 22333994; PMCID: PMC3607428.

Smith AL, Iwanaga R, Drasin DJ, Micalizzi DS, Vartuli RL, Tan AC, Ford HL. The miR-106b-25 cluster targets Smad7, activates TGF-β signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene. 2012 Dec 13;31(50):5162-71. doi: 10.1038/onc.2012.11. Epub 2012 Jan 30. PMID: 22286770; PMCID: PMC3342483.

Farabaugh SM, Micalizzi DS, Jedlicka P, Zhao R, Ford HL. Eya2 is required to mediate the pro-metastatic functions of Six1 via the induction of TGF-β signaling, epithelial-mesenchymal transition, and cancer stem cell properties. Oncogene. 2012 Feb 2;31(5):552-62. doi: 10.1038/onc.2011.259. Epub 2011 Jun 27. PMID: 21706047; PMCID: PMC3183358.