Publications

Modeling Human Development and Disease

Allison T, Langerman J, Sabri S, Otero-Garcia M, Lund A, Huang J, Wei X, Samarasinghe RA, Polioudakis D, Mody I, Cobos I, Novitch BG, Geschwind DH, Plath K, Lowry WE. Defining the nature of human pluripotent stem cell-derived interneurons via single-cell analysis. Stem Cell Reports. 2021 Sep 6:S2213-6711(21)00424-0. doi: 10.1016/j.stemcr.2021.08.006. Online ahead of print. PMID: 34506726
 
Samarasinghe RA, Miranda OA, Buth JE, Mitchell S, Ferando I, Watanabe M, Allison TF, Kurdian A, Fotion NN, Gandal MJ, Golshani P, Plath K, Lowry WE, Parent JM, Mody I, Novitch BG. Identification of neural oscillations and epileptiform changes in human brain organoids. Nat Neurosci. 2021 Aug 23. doi: 10.1038/s41593-021-00906-5. Online ahead of print. PMID: 34426698
 

Llorente IL, Xie Y, Mazzitelli JA, Hatanaka EA, Cinkornpumin J, Miller DR, Lin Y, Lowry WE, Carmichael ST. Patient-derived glial enriched progenitors repair functional deficits due to white matter stroke and vascular dementia in rodents.  Sci Transl Med. 2021 Apr 21;13(590):eaaz6747. doi: 10.1126/scitranslmed.aaz6747. PMID: 33883275

Polioudakis D, de la Torre-Ubieta L, Langerman J, Elkins AG, Shi X, Stein JL, Vuong CK, Nichterwitz S, Gevorgian M, Opland CK, Lu D, Connell W, Ruzzo EK, Lowe JK, Hadzic T, Hinz FI, Sabri S, Lowry WE, Gerstein MB, Plath K, Geschwind DH. A Single-Cell Transcriptomic Atlas of Human Neocortical Development during Mid-gestation. Neuron. 2019 Jul 3. pii: S0896-6273(19)30561-6. doi: 10.1016/j.neuron.2019.06.011. [Epub ahead of print] PMID: 31303374

Raman AT, Pohodich AE, Wan YW, Yalamanchili HK, Lowry WE, Zoghbi HY, Liu Z. Apparent bias toward long gene misregulation in MeCP2 syndromes disappears after controlling for baseline variations. Nat Commun. 2018 Aug 13;9(1):3225. doi: 10.1038/s41467-018-05627-1.

Ohashi M, Korsakova E, Allen D, Lee P, Fu K, Vargas BS, Cinkornpumin J, Salas C, Park JC, Germanguz I, Langerman J, Chronis C, Kuoy E, Tran S, Xiao X, Pellegrini M, Plath K, Lowry WE. Loss of MECP2 Leads to Activation of P53 and Neuronal Senescence. Stem Cell Reports. 2018 May 8;10(5):1453-1463. doi: 10.1016/j.stemcr.2018.04.001.

Manipulation of neural progenitor fate through the oxygen sensing pathway. Xie Y, Lowry WE. Methods. 2017 Aug 31. pii: S1046-2023(17)30138-X. doi: 10.1016/j.ymeth.2017.08.018. [Epub ahead of print] Review.

Patel S, Bonora G, Sahakyan A, Kim R, Chronis C, Langerman J, Fitz-Gibbon S, Rubbi L, Skelton RJ, Ardehali R, Pellegrini M, Lowry WE, Clark AT, Plath K. Human Embryonic Stem Cells Do Not Change Their X Inactivation Status during Differentiation. Cell Reports 2017

Gaeta X, Le L, Lin Y, Xie Y, Lowry WE. Defining Transcriptional Regulatory Mechanisms for Primary let-7 miRNAs. PLoS One. 2017 Jan 4;12(1):e0169237. doi: 10.1371/journal.pone.0169237.

Germanguz I, Listgarten J, Cinkornpumin J, Solomon A, Gaeta X, and Lowry WE. Identifying gene expression modules that define human cell fates. Stem Cell Research. 2016 May;16(3):712-24. PMCID 4903895.

Gu W, Gaeta X, Sahakyan A, Chan AB, Hong CS, Kim R, Braas D, Plath K, Lowry WE, Christofk HR. Glycolytic Metabolism Plays a Functional Role in Regulating Human Pluripotent Stem Cell State. Cell Stem Cell. 2016 Oct 6;19(4):476-490. doi: 10.1016/j.stem.2016.08.008.

Patterson M*, Gaeta X*, Loo K, Edwards M, Smale S, Cinkornpumin J, Xie Y, Listgarten J, Douglass SM, Pellegrini M, & Lowry WE (2014). let-7 miRNAs can act through notch to regulate human gliogenesis. Stem cell reports, 3(5), 758-773. [PubMed Link]

Xie Y, Zhang J, Lin Y, Gaeta X, Meng X, Wisidagama DR, Cinkornpumin J, Koehler CM, Malone CS, Teitell MA@, & Lowry  WE (2014). Defining the role of oxygen tension in human neural progenitor fate. Stem cell reports, 3(5), 743-757. [PubMed Link]

Lowry WE. –OH No! hiPSCs misplace their 5hmCs; Cell Stem Cell, July 3, 2013. [PubMed Link]

Gaeta X, Xie Y and Lowry WE. Sequential Addition of reprogramming factors improves efficiency; Nature Cell Biology, July 1, 2013. [PubMed Link]

Kartikasari AER, Zhou JX, Kanji MS, Chan DN, Sinha A, Grapin-Botton A, Magnuson MA, Lowry WE, and Bhushan A. The histone demethylase Jmjd3 sequentially associates with Tbx3 and Eomes to drive endoderm differentiation; EMBO, May 15 2013. [PubMed Link]

Lee P, Martin N, Nakamura K, Azghadi S, Amiri M, Perlman S, Gatti RA., Hu H. and Lowry WE. SMRT compounds can abrogate phenotypes of Ataxia Telangiectasia in neural derivatives of patient-specific hiPSCs; Nature Communications, 2013. [PubMed Link]

Chan DN, Azghadi SF, Feng J and Lowry WE. Ptk7 marks the first human developmental EMT in vitro; PLOSOne, in press [PubMed Link]

Lowry WE. Does transcription factor induced pluripotency accurately mimic embryo derived pluripotency?; Current Opinion in Genetics and Development, Oct 15 2012. [PubMed Link]

Li J, Patterson M, Mikkola H, Lowry WE and Kurdistani S. Dynamic Distribution of Linker Histone H1.5 in Cellular Differentiation; PLOS Genetics, Aug 8 2012 [PubMed Link]

Patterson M*, D. Chan*, Ha IC, Case D, Khuu K, and Lowry WE. Defining the nature of pluripotent progeny; Cell Research, Jan 2012 [PubMed Link]

Lowry WE.  E-cadherin, a new mixer in the Yamanaka cocktail; EMBO Reports, July 2011 [PubMed Link]

Plath K and Lowry WE. Progress in understanding reprogramming to the induced pluripotent state; Nature Rev Genetics, April 12, 2011 [PubMed Link]

Mayshar Y, Ben-David U, Lavon N, Plath K, Lowry WE and Benvensity N.Chromosomal aneuploidy in induced pluripotent stem cells identified by gene expression profiling, Cell Stem Cell, October, 2010. [PubMed Link]

Tchieu, J, Kuoy E, Chin M, Trinh H, Patterson M, Sherman S, Aimiuwu O, Lingren A, Zack J, Clark A, Pyle A, Lowry WE and Plath K@. Female human iPS cells retain an inactive X-chromosome, Cell Stem Cell, September 5, 2010. [PubMed Link]

Chin MC, Pellegrini M, Plath K and Lowry WE. Molecular analyses of human induced pluripotent stem cells and embryonic stem cells, Cell Stem Cell, Aug 5, 2010. [PubMed Link]

Chin M, Mason M, Xie W, Volinia S, Singer M, Peterson C, Richter L, Aimiuwu O, Zhang J, Khvorostov I, Ott V, Grunstein M, Benvenisty N, Croce C, Clark A, Baxter T, Pyle A, Teitell M, Pelegrini M, Plath K, and Lowry WE. Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures, Cell Stem Cell, July 2, 2009. [PubMed Link]

Karumbayaram S*, Novitch BG*@, Patterson M*, Umbach JA, Richter L, Lindgren A, Conway A, Clark A, Goldman SA, Plath K, Wiedau-Pazos M, Kornblum HI, and Lowry WE. Directed differentiation of human induced-pluripotent stem cells (iPS) generates active motor neurons, Stem Cells, April 27, 2009. [PubMed Link]

Park, T.S., Galic, Z., Conway, A.E., Lindgren, A., Van Handel, B.V., Magnusson, M., Richter. L., Teitell, M.A., Mikkola, H.K.A., Lowry, W.E., Plath, K. and Clark, AT. Derivation of Primordial germ cells from Human Embryonic and Induced Pluripotent Stem Cells is significantly improved by co-culture with human fetal gonadal cells. Stem Cells, April 27, 2009. [PubMed Link]

Lowry WE and Plath K The many ways to make an iPS cell. Nature Biotechnology, Nov 26 2008. [PubMed Link]

Wu H, Kim KJ, Mehta K, Paxia S, Sundstrom A, Anantharaman T, Kuraishy AI, Doan T, Ghosh J, Pyle AD, Clark A, Lowry W, Fan G, Baxter T, Mishra B, Sun Y, Teitell MA. Copy number variant analysis of human embryonic stem cells.Stem Cells. June, 2008. [PubMed Link]

Lowry WE@, Richter L, Yachechko R, Pyle AD, Tchieu J, Sridharan R, Clark AT, and Plath K. Generation of human-induced pluripotent cells from dermal fibroblasts, PNAS, 2008 Feb 26;105(8):2883-8. [PubMed Link]

Epidermal Biology

Miranda M, Avila I, Esparza J, Shwartz Y, Hsu YC, Berdeaux R, Lowry WE.Defining a Role for G-Protein Coupled Receptor/cAMP/CRE-Binding Protein Signaling in Hair Follicle Stem Cell Activation. J Invest Dermatol. 2021 Jul 17:S0022-202X(21)01454-8. doi: 10.1016/j.jid.2021.05.031. Online ahead of print. PMID: 34280464
 
Flores A, Choi S, Hsu YC, Lowry WE. Inhibition of pyruvate oxidation as a versatile stimulator of the hair cycle in models of alopecia. Exp Dermatol. 2021 Apr;30(4):448-456. doi: 10.1111/exd.14307. Epub 2021 Mar 19. PMID: 33739490
 
Lowry WE. Its written all over your face: The molecular and physiological consequences of aging skin. Mech Ageing Dev. 2020 Sep;190:111315. doi: 10.1016/j.mad.2020.111315. Epub 2020 Jul 15. PMID: 32681843 Review.
 
Takahashi R, Grzenda A, Allison TF, Rawnsley J, Balin SJ, Sabri S, Plath K, Lowry WE. Defining Transcriptional Signatures of Human Hair Follicle Cell States. J Invest Dermatol. 2020 Apr;140(4):764-773.e4. doi: 10.1016/j.jid.2019.07.726. Epub 2019 Oct 31. PMID: 31676413 Free PMC article. Review.
 

Flores A, Sandoval-Gonzalez S, Takahashi R, Krall A, Sathe L, Wei L, Radu C, Jolly J, Graham N, Christofk HR, Lowry WE. Increased lactate dehydrogenase activity is dispensable in squamous carcinoma cells of origin. Nat Commun. 2019 Jan 9;10(1):91. doi: 10.1038/s41467-018-07857-9.

Sullivan WJ, Mullen PJ, Schmid EW, Flores A, Momcilovic M, Sharpley MS, Jelinek D, Whiteley AE, Maxwell MB, Wilde BR, Banerjee U, Coller HA, Shackelford DB, Braas D, Ayer DE, de Aguiar Vallim TQ, Lowry WE, Christofk HR. Extracellular Matrix Remodeling Regulates Glucose Metabolism through TXNIP Destabilization. Cell. 2018 Sep 20;175(1):117-132.e21. doi: 10.1016/j.cell.2018.08.017. Epub 2018 Sep 6.

Miranda MM, Lowry WE. Hip to the Game: YAP/TAZ is required for nonmelanoma skin cancers. EMBO J. 2018 Sep 3;37(17). pii: e99921. doi: 10.15252/embj.201899921. Epub 2018 Jul 23

Jelinek D, Flores A, Uebelhoer M, Pasque V, Plath K, Iruela-Arispe ML, Christofk HR, Lowry WE, Coller HA. Mapping Metabolism: Monitoring Lactate Dehydrogenase Activity Directly in Tissue. J Vis Exp. 2018 Jun 21;(136). doi: 10.3791/57760.

Topical inhibition of the electron transport chain can stimulate the hair cycle. Miranda M, Christofk H, Jones DL, Lowry WE. J Invest Dermatol. 2017 Oct 26. pii: S0022-202X(17)33093-2. doi: 10.1016/j.jid.2017.10.021. [Epub ahead of print]

Melanocyte Stem Cell Activation and Translocation Initiate Cutaneous Melanoma in Response to UV Exposure. Moon H, Donahue LR, Choi E, Scumpia PO, Lowry WE, Grenier JK, Zhu J, White AC. Cell Stem Cell. 2017 Nov 2;21(5):665-678.e6. doi: 10.1016/j.stem.2017.09.001. Epub 2017 Oct 12.

Lactate dehydrogenase activity drives hair follicle stem cell activation. Flores A, Schell J, Krall AS, Jelinek D, Miranda M, Grigorian M, Braas D, White AC, Zhou JL, Graham NA, Graeber T, Seth P, Evseenko D, Coller HA, Rutter J, Christofk HR, Lowry WE. Nat Cell Biol. 2017 Sep;19(9):1017-1026. doi: 10.1038/ncb3575. Epub 2017 Aug 14.

Exploiting Mouse Models to Study Ras-Induced Cutaneous Squamous Cell Carcinoma. Lowry WE@, Flores A, White AC. J Invest Dermatol. 2016 Aug;136(8):1543-8. doi: 10.1016/j.jid.2016.03.017. Review.PMID:27160068

Control of intestinal stem cell function and proliferation by mitochondrial pyruvate metabolism. Schell JC, Wisidagama DR, Bensard C, Zhao H, Wei P, Tanner J, Flores A, Mohlman J, Sorensen LK, Earl CS, Olson KA, Miao R, Waller TC, Delker D, Kanth P, Jiang L, DeBerardinis RJ, Bronner MP, Li DY, Cox JE, Christofk HR, Lowry WE, Thummel CS, Rutter J. Nat Cell Biol. 2017 Sep;19(9):1027-1036. doi: 10.1038/ncb3593. Epub 2017 Aug 14.

Hmga2 is dispensable for cutaneous squamous cell carcinoma. White A, Flores A, Ong J, Lowry WE@. Exp Dermatol. 2016 May;25(5):409-12. doi: 10.1111/exd.12978. PMID: 26901496

Tumor suppressor identity can contribute to heterogeneity of phenotype in hair follicle stem cell-induced squamous cell carcinoma. Flores A, Grant W, White AC, Scumpia P, Takahashi R, Lowry WE. Exp Dermatol. 2016 Sep;25(9):733-5. doi: 10.1111/exd.13037. PMID:27095696

White  AC, and Lowry WE “Refining the role for adult stem cells as cancer cells of origin.” Trends in cell biology 25.1 (2015): 11-20. [PubMed Link]

White AC, Khuu JK, Dang CY, Hu J, Tran KV, Liu A, Gomez S, Zhang Z, Yi R, Scumpia P, Grigorian M, Lowry WE. Stem cell quiescence acts as a tumor suppressor  in squamous tumors. Nat Cell Biol. 2014 Jan;16(1):99-107.

White AC and Lowry WE. Exploiting the origins of Ras mediated squamous cell carcinoma to develop novel therapeutic interventions; Small GTPases, Nov 2011[PubMed Link]

White AC, Tran K, Khuu J, Binder S and Lowry WE. Defining the origins of Ras/p53 mediated squamous cell carcinoma, PNAS, April 18, 2011[PubMed Link]

Lee R, Chang S, Trinh H, Tu Y, White AC, Davies B, Bergo M, Fong L, Lowry WE and Young SG@. Genetic studies on the functional relevance of the protein prenyltransferases in skin keratinocytes, Human Molecular Genetics, Jan 2010. [PubMed Link]

Lowry WE and Richter L. Adult stem cells and the signals that direct them,Frontiers in Bioscience, May 2007. [PubMed Link]

Blanpain C*, Lowry WE*, Pasolli HA, and Fuchs E. Canonical notch signaling functions as a commitment switch in the epidermal lineage, Genes and Development, 2006 Nov 1. [PubMed Link]

Lowry WE*, Blanpain C*, Nowak J, Guasch G, Lewis L and Fuchs E@.Defining the Impact of ß-Catenin/Tcf Transactivation on Epithelial Stem Cells,Genes and Development, 2005 July 1;19(13):1596-611. Epub 2005 Jun 16. [PubMed Link]

Blanpain C*, Lowry WE*, Geoghegan A, Polak L, Fuchs E. Self-Renewal, Multipotency, and the Existence of Two Cell Populations within an Epithelial Stem Cell Niche, Cell 2004 Sep3;118(5):635-48 [PubMed Link]

Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E. Defining the epithelial stem cell niche in skin, Science 2004 Jan 16 303(5656):359-63 [PubMed Link]

Translational Stem Cell Biology

Llorente IL, Hatanaka EA, Meadow ME, Xie Y, Lowry WE, Carmichael ST. Reliable generation of glial enriched progenitors from human fibroblast-derived iPSCs.Stem Cell Res. 2021 Aug;55:102458. doi: 10.1016/j.scr.2021.102458. Epub 2021 Jul 7. PMID: 34274773

Liu X, Flores AA, Situ L, Gu W, Ding H, Christofk HR, Lowry WE, Jung ME. Development of Novel Mitochondrial Pyruvate Carrier Inhibitors to Treat Hair Loss. J Med Chem. 2021 Feb 25;64(4):2046-2063. doi: 10.1021/acs.jmedchem.0c01570. Epub 2021 Feb 3. PMID: 33534563

Cinkornpumin J, Roos M, Nguyen L, Liu X, Gaeta X, Lin S, Chan DN, Liu A, Gregory RI, Jung M, Chute J, Zhu H, Lowry WE. A small molecule screen to identify regulators of let-7 targets. Sci Rep. 2017 Nov 21;7(1):15973. doi: 10.1038/s41598-017-16258-9.

Hazim RA, Karumbayaram S, Jiang M, Dimashkie A, Lopes VS, Li D, Burgess BL, Vijayaraj P, Alva-Ornelas JA, Zack JA, Kohn DB, Gomperts BN, Pyle AD, Lowry WE, Williams DS. Differentiation of RPE cells from integration-free iPS cells and their cell biological characterization. Stem Cell Res Ther. 2017 Oct 2;8(1):217. doi: 10.1186/s13287-017-0652-9.

Moshayedi P, Nih LR, Llorente IL, Berg AR, Cinkornpumin J, Lowry WE, Segura T, Carmichael ST. Systematic optimization of an engineered hydrogel allows for selective control of human neural stem cell survival and differentiation after transplantation in the stroke brain. Biomaterials. 2016 Oct;105:145-55. doi: 10.1016/j.biomaterials.2016.07.028.

Nih LR, Moshayedi P, Llorente IL, Berg AR, Cinkornpumin J, Lowry WE, Segura T, Carmichael ST.
Engineered HA hydrogel for stem cell transplantation in the brain: Biocompatibility data using a design of experiment approach. Data Brief. 2016 Nov 24;10:202-209.

Lam J, Lowry WE, Carmichael ST, & Segura T (2014). Delivery of iPS‐NPCs to the Stroke Cavity within a Hyaluronic Acid Matrix Promotes the Differentiation of Transplanted Cells. Advanced Functional Materials, 24(44), 7053-7062.  [Link]

Lam J, Carmichael ST, Lowry WE, & Segura T (2014). Hydrogel Design of Experiments Methodology to Optimize Hydrogel for iPSC‐NPC Culture. Advanced healthcare materials. [PubMed Link]

Karumbayaram S, Lee P, Azghadi S, Cooper AR, Patterson M, Kohn DB, Pyle A, Clark AT, Byrne J, Zack JA, Plath K, Lowry WE@. From Skin Biopsy to Neurons Through a Pluripotent Intermediate Under Good Manufacturing Practice Protocols; Stem Cells Translational Medicine, Dec 7 2011. [PubMed Link]

Zhang J, Tokatlian T, Zhong J, Ng QK, Patterson M, Lowry WE, Carmichael ST, Segura T@. Physically associated synthetic hydrogels with long-term covalent stabilization for cell culture and stem cell transplantation.; Adv Materials, Nov 2011 [PubMed Link]

Lowry WE@ and Quan W. Roadblocks on the route to clinical application of induced pluripotent stem cells, Journal of Cell Science, March 1, 2010. [PubMed Link]

Heterotrimeric G-Protein Signaling

Lowry WE., Huang J., Ma Y.C., Ali S., Wang D., Williams D., Okada M., Cole P.,and Huang X.Y@.Csk, a Critical Link of G Protein Signals to Actin Cytoskeletal Reorganization, Developmental Cell 2002 June 2 (6): 733-44 [PubMed Link]

Lowry WE., and Huang X.Y@. G protein betagamma subunits act on the catalytic domain to stimulate Bruton’s amgammaglobulinemia tyrosine kinase.Journal of Biological Chemistry, 2002 Jan 11;277(2):1488-92 [PubMed Link]

Lowry WE., Ma Y.C., Cvejic S., and Huang X.Y@. Direct regulation of Btk tyrosine kinase by G proteins. Methods in Enzymology, 2002;345:464-9 [PubMed Link]

Lowry WE., Huang J., Lei M., Harrison S., Rawlings D., and Huang X.Y@. Role of PHTH module in protein substrate recognition by Bruton’s agammaglobulinemia tyrosine kinase. Journal of Biological Chemistry, 2001 Nov 30;276(48):45276-81 [PubMed Link]

Aghazadeh B., Lowry WE., Huang X.Y., and Rosen M.K@. Structural basis for relief of autoinhibition of the Dbl homology domain of proto-oncogene Vav by tyrosine phosphorylation. Cell, 2000 Sep 1;102(5):625-33 [PubMed Link]

Ma Y.C., Huang J., Ali S., Lowry W., and Huang X.Y@. Src tyrosine kinase is a direct novel effector of G proteins. Cell, 2000 Sep 1;102(5):635-46 [PubMed Link]

Muscle Development

Gogos J.A., Lowry W., and Karayiogou M@. 1997. Selection for retroviral insertions into regulated genes. Journal of Virology, 1997 Feb;71(2):1644-50. [PubMed Link]

Gogos J.A., Thompson R., Lowry W., Sloane B.F., Weintraub H., and Horwitz M@. Gene trapping in differentiating cell lines: regulation of the lysosomal protease cathepsin B in skeletal myoblast growth and fusion. Journal of Cell Biology, 1996 Aug; 134(4):837-47 [PubMed Link]

* denotes equal contribution
@ denotes corresponding author