Publications

Clark Lab in News

  • von Meyenn, F and Reik, W (2015). Forget the parents: Epigenetic reprogramming in human germ cells. Cell (link).
  • Cyranoski D. (2014). Rudimentary egg and sperm cells made from stem cells. Nature (link).
  • Laird DJ. (2013) Humans put their eggs in more than one basket. Nature Cell Biology (link).
  • Summers B. (2012). First road map of human sex-cell development: Study marks a step towards stem-cell treatment of infertility. Nature News (link).

2017

  • Chen, D., Liu, W., Lukianchikov, A., Hancock, G., Zimmerman, J., Lowe, M., Kim, R., Galic, Z., Irie, N., Surani, MA., Jacobsen, SE., Clark, AT (2017) Germline competency of human embryonic stem cells depends on  eomesodermin.  Biology of Reproduction (Epub ahead of print.
  • Clark, AT., Gkountela, G., Chen, D., Liu, W., Sosa, E., Sukhwani, M., Hennebold, JD, Oriwg, KE (2017).  Primordial germ cells acquire transplantation potential by Carnegie Stage 23.  Stem Cell Reports, 11: 329-341 (link)
  • Sosa E, Kim R, Rojas EJ, Hosohama L, Hennebold JD, Orwig KE, Clark AT (2017). An integration-free visus-free rhesus macaque induced pluripotent stem cell line (iPSC90) from embryonic fibroblasts Stem Cell Research. 21, 5-8
  • Chen D, Gell J, Tao Y, Sosa E, Clark AT (2017) Modeling human infertility with pluripotent stem cells. Stem Cell Research on line (link)
  • Nagaraj R, Sharpley MS, Chi F, Braas D, Zhou Y, Kim R, Clark AT, Banerjee U. (2017). Nuclear localization of mitochondrial TCA cycle enzymes as a critical step in mammalian zygotic genome activation. Cell 168:210-223. (link)
  • Patel S, Bonora G, Sahakyan A, Kim R, Chronis C, Langerman J, Fitz-Gibbon S, Rubbi L Skelton RJP, Ardehali R, Pellegrini M, Lowry WE, Clark AT, Plath K (2017) Human embryonic stem cells do not change their X inactivation status during differentiation. Cell Reports. 18:54-67 (link)
  • Sahakyan A, Kim R, Chronis C, Sabri S, Bonora G, Theunissen TW, Kuoy E, Langerman J, Clark AT, Jaenisch R, Plath K (2017) Naive Human pluripotent stem cells model X chromosome Dampening and X inactivation Cell Stem Cell. 20: 87-101 (link)
  • O’Brien CM, Chy HS, Zhou Q, Blumenfeld S, Lambshead JW, Liu X, Kie J, Capaldo BD, Chung TL, Adams TE, Phan T, Bentley JD, Mckinstry WJ, Oliva K, Mcmurrick PJ, Wang YC, Rossello FJ, Lindeman GJ, Chen D, Jarde T, Clark AT, Abud HE, Visvader JE, Nefzger CM, Polo JM, Loring JF, Laslett AL. (2017) New monoclonal antibodies to defined cell surface proteins on human pluripotent stem cells  Stem Cells, 35: 626-640 (link)

2016

  • Masaeli M, Gupta D, O’Byrne S, Tse HT, Gossett DR, Tseng P, Utada AS, Jung HJ, Young S, Clark AT, Di Carlo D. (2016) Multiparameter mechanical and morphometric screening of cells. Sci Reports. Dec 2;6:37863 (link)
  • Hargan-Calvopina J, Taylor S, Cook H, Hu Z, Lee SA, Yen M-R, Chiang, Y-S, Chen P-Y and Clark, AT (2016). Stage-specific demethylation in primordial germ cells safeguards against precocious differentiation.  Developmental Cell. 0;39(1):75-86 (link)
  • Pastor W, Chen D, Liu W, Kim R, Sahakyan A, Lukianchikov A, Plath K, Jacobsen SE, Clark AT (2016). Naive human pluripotent stem cells feature a methylation landscape devoid of blastocyst or germline memory. Cell Stem Cell. 18: 1-7 (link)
  • Li S, Yen L, Pastor W, Johnston JB, Du J, Shew CJ, Liu W, Ho J, Stender B, Clark AT, Burlingame AL, Daxinger L, Patel DJ,  Jacobsen SE  (2016). Mouse MORC3 is a GHKL ATPase that localizes to H3K4me3 marked chromatin PNAS Aug 30;113(35):E5108-16 (link)
  • Sosa E, Kim R, Rojas EJ, Hosohama L, Hennebold JD, Orwig KE, Clark AT (2016). An integration-free visus-free rhesus macaque induced pluripotent stem cell line (iPSC89) from embryonic fibroblasts Stem Cell Research.  Sep;17(2):444-447 (link)

2015

  • Clark AT, Zwaka, TP (2015). Editorial overview: cell reprogramming regeneration and repair: Reprogramming: the eternal circle. Current Opinion in Genetics and Development. 34 v-vi (link)
  • Clark AT (2015). DNA methylation remodeling in vitro and in vivoCurrent Opinion in Genetics and Development. 34: 82-87 (link)
  • Oliveros-Etter M, Li Z, Nee K, Hosohama L, Hargan-Calvopina J, Lee SA, Joti P, Yu J, Clark AT (2015) PGC Reversion to pluripotency involves erasure of DNA methylation from imprinting control centers followed by locus-specific remethylation Stem Cell Reports. 5: 337-339 (link)
  • Gkountela S, Zhang KX, Shafiq T, Liao W-W, Hargan-Calvopina J, P-Y Chen, Clark, AT (2015). DNA methylation dynamics in the human prenatal germline Cell. 161;1425-1436 (link)
  • Morselli M, Pastor W, Montanini B, Nee K, Ferrari R, Fu K, Bonora G, Rubbi L, Clark AT, Ottonello S, Jacobsen SE, Pellegrini M (2015). In vivo targeting of de novo DNA methylation by histone modifications in yeast and mouse. eLIFE. 10.7554/eLife.06205 (link)   
  • Chen, D Clark AT (2015). Human germline differentiation charts a new courseEMBO J. 34;974-977 (link)
  • Hargan-Calvopina J, Cook H, Vincent J, Nee K, Clark AT (2015). The aorta gonad mesonephros organ culture recapitulates 5hmC reorganization and replication-dependent and independent loss of DNA methylation in the germline. Stem Cells Dev. 24:1536-1545 (link)
  • Li Z, Hosohama L, Nee K, Gkountela S, Chaudhari S, Cass AA, Xiao X, Clark AT (2015). The Sm protein methyltransferase PRMT5 is not required for primordial germ cell specification in mice. EMBO J. 34;748-758 (link).

2014

  • Pastor WA, Stroud H, Nee K, Liu W, Pezic D, Manakov S, Lee SA, Moissiard G, Zamudio N, Bourchis D, Aravin AA, Clark AT*, Jacobsen SE* (* co-corresponding) (2014). MORC1 represses transposable elements in the mouse male germline. Nature Communications. 5: 5795 (link).
  • Gkountela S, Clark AT (2014). A Big Surprise in the Little Zygote: The Curious Business of Losing Methylated Cytosines. Cell Stem Cell. 15:4 (393-4) (link).
  • Ben-David U, Arad G, Weissbein U, Mandefro B, Maimon A, Golan-Lev T, Narwani K, Clark AT, Andrews PW, Benvenisty N, Biancotti JC. (2014) Aneuploidy induces profound changes in gene expression, proliferation and tumorigenicity of human pluripotent stem cells. Nature Communications. 5:4825 (link).
  • Gkountela S, Li Z, Chin CJ, Lee SA, Clark AT. (2014) PRMT5 is required for human embryonic stem cell proliferation but not pluripotency. Stem Cell Rev. 10(2):230-9 (link).
  • Valli H, Phillips BT, Shetty G, Byrne JA, Clark AT, Meistrich ML, Orwig KE (2013). Germline stem cells: toward the regeneration of spermatogenesis. Fertility and Sterility. 101: 1 (3-13) (link).

2013

  • Vincent, JJ., Huang, Y., Chen, PY., Feng, S., Calvopina, JH., Noom K., Lee, SA., Le, T., Yoon, AJ., Faull, K., Fan, G., Rao, A., Jacobsen, SE., Pellegrini, M., Clark, AT (2013) Stage-specific roles for Tet1/Tet2 in DNA demethylation in primordial germ cells Cell Stem Cell 12 (4):470-478 (link)
  • Gkountela, S., Li, Z., Vincent, JJ, Zhang, KX, Chen, A., Pellegrini, M., Clark, AT (2013) The ontogeny of cKIT+ human primordial germ cells proves to be a resource for human germ line reprograming, imprint erasure and in vitro differentiation. Nature Cell Biology 15:113-122 (link).
  • Awe JP, Lee PC, Ramatha C, Crespo A, Durruthy J, Cooper A, Karumbayaram S, Lowry WE, Clark AT, Zack JA, Sebastiano V, Kohn DB, Pyle AD, Martin MG, Lipshutz GS, Phelps PE, Pera R, Byrne JA (2013) Generation and characterization of transgene-free human induced pluripotent stem cells and conversion to putative clinical-grade status. Stem Cell Research and Therapy. Jul 4:87, 1-15 (link).
  • Feng Y, Maity R, Whitelegge JP, Hadjikyriacou A, Li Z, Lopez C, Hadid Q, Clark AT, Bedford MT, Masson J, Clarke SG (2013) Mammalian protein Arginine Methyltransferase 7 (PRMT7) specifically targets RXR sites in Lysine- and Arginine-rich regions. The Journal of Biological Chemistry. Vol. 288, No. 52, pp. 37010 –37025 (link).

2012

  • Clark, AT (2012) Pluripotency takes off without Blimp1. Cell Stem Cell 11; 1-2 (link).
  • Deshpande, AM., Khalid, O., Kim, JJ., Kim, Y., Lindgren, A., Clark, AT., Wong, DTW (2012). Cdk2ap2 Is a Novel Regulator for Self-Renewal of Murine Embryonic Stem Cells. Stem Cells and Development (link).
  • Gossett DR, Tse HTK, Lee SA, Ying Y, Lindgren AG, Yang OO, Rao J, Clark AT, Di Carlo D. (2012) Hydrodynamic stretching of single cells for large population mechanical phenotyping. Proceedings of the National Academy of Sciences (USA) (link).
  • Karumbayaram, S., Lee, P. Azghadi, S.F. Cooper, AR, Patterson, M., Kohn, D.B., Pyle, A.D. Clark, AT. Byrne, J. Zack, J.A. Plath, K. Lowry, W.E (2012). From Skin Biopsy to Neurons through a Pluripotent Intermediate Under Good Manufacturing Practice Protocols. Stem Cells Translational Medicine 1:36–43 (link).

2011

  • Clark AT, Phillips BT, Orwig KE. Fruitful progress to fertility: male fertility in the test tube. Nature Medicine. 2011 Dec 6;17(12):1564-5 (link).
  • Vincent, JJ., Li, Z., Liu, X., Lee, SA., Etter, M., Gkountela, S., Diaz-Perez, S., Lindgren, AG., Clark, AT (2011) Using Single Cell Analysis to Identify and Stage Primordial Germ Cells Derived from Embryonic Stem Cells. PLoS ONE 6(12) (link).
  • Diaz Perez, S., Kim, R., Li, Z., Marquez, V.E., Patel, S., Plath, K., and Clark, A.T. Clark, AT (2011) Derivation of new human embryonic stem cell lines reveals rapid epigenetic progression in vitro that can be prevented by chemical modification of chromatin. Human Molecular Genetics.19(20):3970-82 (link).
  • Mandal, S., Lindgren, AG., Srivastava, AS., Clark, AT*., Banerjee, U* (2011) Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells 29(3):486-495. * denotes co-corresponding author (link).
  • Lindgren, A., Natshuhara, K., Tian, E., Vincent, JJ., Li, X., Jiao, J., Wu, H., Banerjee, U, Clark, AT (2011) Loss of Pten causes tumor initiation from differentiated pluripotent stem cells due to failed repression of Nanog. PLoS ONE Jan 27;6(1):e16478 (link).

2010

  • Mayshar, Y., Ben-David, U., Lavon, N., Biancotti, JC., Yakir, B., Clark, AT., Plath, K., Lowry, WE., Benvenisty, N (2010) Identification and Classification of Chromosomal Aberrations in Human Induced Pluripotent Stem Cells. Cell Stem Cell 7: 521-531 (link).
  • Tchieu, J., Kuoy, E., Chin, MH., Trinh, H., Patterson, M., Sherman, SP., Aimiuwu, O., Lindgren, A., Hakimian, S., Zack, JA., Clark, AT., Pyle, AD., Lowry, WE., Plath, K (2010) Female Human iPSCs Retainan Inactive X Chromosome. Cell Stem Cell 3;7(3):329-42 (link).
  • Biancotti, JC., Narwani, K., Buehler, N., Mandefro, B., Golan-Lev, T., Yanuka, O., Clark, AT., Hill, D., Benvenisty, N., Lavon, N (2010) Human Embryonic Stem Cells as Models for Aneuploid Chromosomal Syndromes. Stem Cells 28(9):1530-40 (link).
  • Ambartsumyan. G., Gill, RK., Diaz Perez, S., Conway, D., Vincent, J., Dalal, Y., Clark, AT (2010) Centromere Protein A dynamics in human pluripotent stem cell self renewal, differentiation and DNA damage. Human Molecular Genetics 19(20):3970-82 (link).
  • Chodavarapu RK., Feng, S., Bernatavichute, YV., Chen, PY., Stroud, H.,Yu, Y., Hetzel, JA., Kuo, F., Kim, J., Cokus, SJ., Casero, D., Bernal, M., Huijser, P., Clark, AT., Kra¨mer, U., Merchant, SS., Zhang, X., Jacobsem, SE., Pellegrini, M (2010) Relationship between nucleosome positioning and DNA methylation. Nature 466(7304):388-92 (link).
  • Kamei, K., Ohashi, M., Gschweng, E., Ho, Q., Suh, J., Tang, J., Yu, Z., Clark, AT., Pyle, AD., Teitell, MA., Lee, KB., Witte, ON., Tseng, H-R (2010) Microfluidic image cytometry for quantitative single-cell profiling of human pluripotent stem cells in chemically defined conditions. Lab on a chip 10:113-1119 (link).
  • Gkountela, S., Lindgren, A. and Clark, AT. Pluripotent stem cells in reproductive medicine: Formation of the human germ line in vitro. In ‘Stem Cells and Regenerative Medicine From Molecular Embryology to Tissue Engineering‘ ed. Appasani, K & Appasani, RK Humana Press, 2010 Page 371 (link).

2009

  • Xie, W., Song, C., Young, NL., Sperling, AS., Xu, F., Sridharan, R., Conway, AE., Garcia, BA., Plath, K., Clark, AT*., Grunstein, M*. (2009) Histone H3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Molecular Cell. 33: 417-427 (* co-corresponding author) (link).
  • Chin, MH., Mason, MJ., Xie, W., Volinia, S., Singer, M., Peterson, C., Ambartsumyan, G., Aimiuwu, O., Richter, L., Zhang, J., Khvorostov, I., Ott, V., Grunstein, M., Lavon, N., Benvenisty, N., Croce, CM., Clark, AT., Baxter, T., Pyle, AD., Teitell, MA., Pelegrini, M., Plath, K., Lowry, WE (2009). Induced Pluripotent Stem Cells and Embryonic Stem Cells Are Distinguished by Gene Expression Signatures. Cell Stem Cell 5: 111-123 (link).
  • Park, TS., Galic, Z., Lindgren, A., Conway, AE., Van Handel, BJ., Magnusson, M., Richter, L., Teitell, MA., Mikkola, HKA., Lowry, WE., Plath, K., Clark, AT. (2009). 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 (link).
  • Kim, Y., Deshpande, A., Dai, Y., Kim, JJ., Lindgren, A., Conway, A., Clark, AT., Wong, DT. (2009) Cyclin-dependent kinase 2-associating protein 1 Commits Murine Embryonic Stem Cell Differentiation through Retinoblastoma Protein Regulation. Journal of Biological Chemistry (link).
  • Saravanan, K., Novitch, B., Patterson, M., Umbach, J., Richter, L., Lindgren, A., Conway, AE., Clark, AT., Goldman, S., Plath, KP., Kornblum, H., Lowry, WE (2009) Directed differentiation of human induced-pluripotent stem cells (iPS) generates active motor neurons. Stem Cells (link).
  • Conway, AE., Lindgren, A., Galic, Z., Pyle, D., Wu, H., Zack, J., Pelligrini, M., Teitell, MA., Clark, AT. (2009) A Pluripotency and Self-Renewal Program Controls the Expansion of Genetically Unstable Cancer Stem Cells in Pluripotent Stem Cell-Derived Tumors. Stem Cells (link).

2008

  • Ambartsumyan GA, Clark, AT. (2008) Aneuploidy and early human embryo development Human Molecular Genetics 17: R10-5 (link).
  • Hao, W., Kim, K., Mehta, K., Paxia, S., Sundstrom, A., Anantharamen, T., Ali, K., Doan, T., Ghosh, J., Pyle, A., Clark, AT., Lowry, WE., Fan, G., Baxter, T., Mishra, B., Sun, Y., Teitell, M (2008) Copy number variant analysis of human embryonic stem cells. Stem Cells (link).
  • Lowry, WE., Richter, L,. Yachechko, R., Pyle, AD., Tshieu, J., Sridharan, R., Clark, AT., Plath, K (2008) Generation of human induced pluripotent stem cells from dermal fibroblasts, PNAS Feb 26, 105(8):2883-2888 (link).

2007

  • Bostick, M., Kim, JK., Esteve, PO, Clark, AT, Pradhan, S and Jacobson, SE (2007) UHRF1 plays a role in maintaining DNA methylation in mammalian cells Science (2007) 317:1760-1764 (link).
  • Clark, AT (2007) Testicular Cancer Stem Cells. Stem Cell Reviews (2007); 3: 49-59 (link).
  • Fox, M., Clark, AT, Majdoubi, ME., Vigne, JL., Griswald, MD., Urano, J., Weiner, RI., Reijo Pera, RA (2007) Distinct RNA and Protein Complexes Distinguish Human and Mouse Embryonic Stem Cells and Germ Cells Dev Biol 302:417-431 (link).

2006 and earlier

  • Kee, K., Gonsalves, JM., Clark, AT., Reijo Pera, RA (2006) Bone Morphogenetic Proteins Induce Germ Cell Differentiation from Human Embryonic Stem Cells. Stem Cells and Development 15; 831-837 (link).
  • Clark, AT (2006) Establishment and Differentiation of Human Embryonic Stem Cell Derived Germ Cells. Reproduction suppl (link).
  • Clark, AT* & Pera, RA (2006) Modeling Human Germ Cell Formation with Embryonic Stem Cells. Regenerative Medicine. 1(1); 85-93 *Corresponding author (link).
  • Ezeh, U, Turek, PJ, Reijo Pera, RA, Clark, AT* (2005) Human Embryonic Stem Cell Genes OCT4, NANOG, STELLAR and GDF3 are expressed in both Seminoma and Breast Cancer Cancer 104: 2255-2265. *Corresponding author (link).
  • Clark, A.T. Bodnar, M., Fox, M., Rodriguez, R.T., Abeyta, M.J., Firpo, M.T., Reijo-Pera, R.A. (2004) Differentiation of the Human Germ Cell Lineage from Embryonic Stem Cells. Human Molecular Genetics 13(7):727-739 (link).
  • Abeyta, M.J., Clark, A.T. Rodriguez, R.T. Bodnar, M, Reijo-Pera, R.A. Firpo, M.T. (2004) Global Gene Expression in Human Embryonic Stem Cell Lines. Human Molecular Genetics 13(6):601-8 (link).
  • Clark, A.T. Rodriguez, R.T., Abeyta, M.J., Firpo, M.T., Reijo-Pera, R.A. (2004) Chromosome 12p13.1, a hot-spot for Teratocarcinoma, Encodes Three Genes Expressed in Pluripotent Cells with Remarkable Evolutionary Divergence from Humans to Mice Stem Cells 22(2) 169-179 (link).
  • Clark AT, Goldowitz D, Takahashi JS, Vitaterna MH, Siepka SM, Peters LL, Frankel WN, Carlson GA, Rossant J, Nadeau JH, Justice MJ (2004). Implementing Large-scale ENU Mutagenesis Screens in North America. Genetica. Sep;122(1):51-64 (link).
  • Clark, A.T., Firozi, K., Justice, M.J. (2004) Mutations in a Novel Locus on Mouse Chromosome 11 Resulting in Male Infertility Associated with Defects in Microtubule Assembly and Sperm Tail Function Biology of Reproduction 70:5; 1317-1324 (link).
  • Kile B.T*, Hentges K.E*, Clark A.T*, Nakamura H, Salinger A.P, Liu B, Box N, Stockton D.W, Johnson R.L, Behringer R.R, Bradley A, Justice M.J. (2003) Functional Genetic Analysis of Mouse Chromosome 11. Nature. 4;425(6953):81-6. *denotes equal contribution (link).
  • Clark, A.T., Young, R., Bertram, J.F. (2001). In vitro and Localization Studies on the Role of TGF-b1 in Rat Metanephric Development. Kidney International. 59:1641-1653 (link).
  • Joyce I.M., Clark A.T., Pendola, F.L., Eppig J.J. (2000) Comparison of Recombinant Growth Differentiation Factor-9 and Oocyte Regulation of Kit Ligand Messenger Ribonucleic Acid Expression in Mouse Ovarian Follicles. Biology of Reproduction. 63(6):1669-1675 (link).
  • Elvin J,A. Clark A,T., Wang, P., Wolfman N.M., and Matzuk M.M (1999). Paracrine Actions of Growth Differentiation Factor-9 in the Mammalian Ovary. Molecular Endocrinology, 13: 1035-1048 (link).
  • Fox, M, Reijo Pera, RA, and Clark, A.T. The DAZ gene family and human germ cell development from embryonic stem cells In. ‘The Sperm Cell’ ed. De Jong, C & Barratt, C Cambridge University Press, 2006, Chapter 12 (link).