Research Publications

Le et al Cover

Stem cell publications by UCSC researchers

Leung G, Cool T, Valencia C, Worthington A, Beaudin A and Forsberg EC. The lymphoid-associated interleukin 7 receptor (IL-7R) regulates tissue resident macrophage development. 2019. Preprint: bioRxiv 534859

Boyer S, Rajendiran S, Beaudin A, Smith-Berdan S, Muthuswamy P, and Forsberg EC. Clonal and quantitative in vivo assessment of hematopoietic stem and progenitor cell differentiation reveals strong erythoid potential of multipotent cells. (2019) In press.

Cool T and Forsberg EC. Chasing Mavericks: The quest for defining developmental waves of hematopoiesis. Current Topics in Developmental Biology 2019 Invited Review. In press.

Field AR, Jacobs FMJ, Fiddes IT, Phillips APR, Reyes-Ortiz AM, LaMontagne E, Whitehead L, Meng V, Rosenkrantz JL, Olsen M, Hauessler M, Katzman S, Salama SR, Haussler D. Structurally Conserved Primate LncRNAs Are Transiently Expressed during Human Cortical Differentiation and Influence Cell-Type-Specific Genes. Stem Cell Reports. 2019 Vol. 12: 1–13

Fiddes IT, Lodewijk GA, Mooring M, Bosworth CM, Ewing AD, Mantalas GL, Novak AM, van den Bout A, Bishara A, Rosenkrantz JL, Lorig-Roach R, Field AR, Haeussler M, Russo L, Bhaduri A, Nowakowski TJ, Pollen AA, Dougherty ML, Nuttle X, Addor MC, Zwolinski S, Katzman S, Kriegstein A, Eichler EE, Salama SR, Jacobs FMJ, Haussler D. Human-Specific NOTCH2NL Genes Affect Notch Signaling and Cortical NeurogenesisCell. 2018 May 31;173(6):1356-1369

Cole C, Byrne A, Beaudin AE, Forsberg EC, and Vollmers C. Tn5Prime, a Tn5 based 5' capture method for single cell RNA-seq. Nucleic Acids Res. 2018 1;46(10):e62. 

Byrne A, Beaudin AE, Olsen HE, Jain M, Cole C, Palmer T, DuBois RM, Forsberg EC, Akeson M, and Vollmers C Nanopore Long-Read RNAseq Reveals Widespread Transcriptional Variation Among Single B cells. Nat Commun. 2018 8:16027  

Smith P., Azzam M. and Hinck L.  Extracellular regulation of the mitotic spindle and fate determinants driving asymmetric cell division. Results and Problems in Cell Differentiation.  Ed. Kubiak and Tassan, Springer Press. 61:351-373. 2017

Xie, Q., and Wang, Z. A. Transcriptional regulation of the Nkx3.1 gene in prostate luminal stem cell specification and cancer initiation via its 3′ genomic region. Journal of Biological Chemistry 2017 292: 13521-13530. 

Fagg WS*,  Ares M Jr., de Bruin, R.G. et al. Quaking Promotes Monocyte Differentiation into Pro-Atherogenic Macrophages by Controlling Pre-mRNA Splicing and Gene Expression. Nat. Commun. 7:10846 doi: 10.1038/ncomms10846 (2016)                                                                  *former UCSC CIRM fellow

Fagg WS*, Liu N, Yang MJ, Cheng K, Chung E, Kim JS, Wu G, and Fair J. Magnetic Targeting of Stem Cell Derivatives Enhances Hepatic Engraftment into Structurally Normal Liver. Cell Transplantation 2017, 26(12): 1868–1877
*former UCSC CIRM fellow

Fagg WS*, Ares M Jr. Autogenous cross-regulation of Quaking mRNA processing and translation balances Quaking functions in splicing and translation. Genes & Dev. 2017 Oct 11. doi: 10.1101/gad.302059.117.
*former UCSC CIRM fellow

Kessenbrock K, Smith P, Steenbeek SC, Pervolarakis N, Kumar R, Minami Y, Goga A, Hinck L, Werb Z. Diverse regulation of mammary epithelial growth and branching morphogenesis through noncanonical Wnt signaling. Proc Natl Acad Sci USA. 2017 Mar 21;114(12): 3121–3126

Xie Q, Liu Y, Cai T, Horton C, Stefanson J, Wang ZA. Dissecting cell-type-specific roles of androgen receptor in prostate homeostasis and regeneration through lineage tracing. Nat Commun. 2017 Jan 23;(8):14284. doi: 10.1038/ncomms14284.

Beaudin AE, Boyer SW, Perez-Cunningham J, Hernandez GE, Derderian SC, Jujjavarapu C, Aaserude E, MacKenzie T, Forsberg EC. A Transient Developmental Hematopoietic Stem Cell Gives Rise to Innate-like B and T Cells. Cell Stem Cell. 2016 Sep 15. pii: S1934-5909(16)30260-0.

Perez-Cunningham J, Boyer S.W., Landon M, Forsberg EC. 2016. Hematopoietic stem cell-specific GFP-expressing transgenic mice generated by genetic excision of a pan-hematopoietic reporter gene. Exp Hematol. 2016 Aug;44(8):755-76

Ennajdaoui H, Howard JM, Sterne-Weiler T, Coyne DJ, Uren PJ, Dargyte M, Katzman S, Draper JM, Cazares O, Burns SC, Qiao M, Jahaniani F, Hinck L, Smith AD, Penalva L.O.F., Toloue MM, Blencowe BJ, and Sanford JR. 2016. IGF2BP3 controls cancer cell invasiveness by modulating RISC function. Cell Reports. 2016 May 31; 15(9):1876-83. 

Le T-N, Mouw J.K., Macias H, Cazares O, Moran A, Ramos J, Keely P. J., Weaver V. M., Hinck L. 2016. Loss of miR-203 increases ROBO1 expression to regulate focal adhesion size in response to elevated extracellular stiffness. Journal of Cell Biology. 2016 Mar 14;212(6):707-19.

Ugarte F, Sousae R, Cinquin B, Martin EW, Krietsch J, Sanchez G, Inman M, Tsang H, Warr M, Passegué E, Larabell C, and Forsberg EC. Progressive chromatin condensation and H3K9 methylation regulate the differentiation of embryonic and hematopoietic stem cells. Stem Cell Reports. 2015 Oct 15. doi: 10.1016/j.stemcr.2015.09.009. [Epub ahead of print].

Ballard MS, Zhu A, Iwai N, Stensrud M, Mapps A, Postiglione MP, Knoblich JA, Hinck L. Mammary stem cell self-renewal is regulated by Slit2/Robo1 signaling through Snail and mInscuteable. Cell reports. 2015;13(2):290-301. doi:10.1016/j.celrep.2015.09.006.

Zovein AC, Forsberg EC. Hematopoietic development at high altitude: blood stem cells put to the test. Development. 2015 May 15;142(10):1728-1732.

Hoeffel G, Chen J, Lavin Y, Low D, Almeida FF, See P, Beaudin AE, Lum J, Low I, Fordberg EC, Poidinger M, Zolezzi F, Larbi A, Ng LG, Chan JK, Greter M, Becher B, Samokhvalov IM, Merad M, Ginhoux F. C-myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity. 2015 Apr 21;42(4):665-78.

Poulsen LD, Kielpinski LJ, Salama SR, Krogh A, Vinther J. SHAPE Selection (SHAPES) enrich for RNA structure signal in SHAPE sequencing-based probing data. RNA. 2015 May;21(5):1042-52. doi: 10.1261/rna.047068.114. Epub 2015 Mar 24. PubMed PMID: 25805860; PubMed Central PMCID: PMC4408784.

Smith-Berdan S, Nguyen A, Hong MA, Forsberg EC. ROBO4-Mediated Vascular Integrity Regulates the Directionality of Hematopoietic Stem Cell Trafficking. Stem Cell Reports. 2015 Feb 10;4(2):255-68.

Jacobs FM, Greenberg D, Nguyen N, Haeussler M, Ewing AD, Katzman S, Paten B, Salama SR, Haussler D. An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons. Nature. 2014 Dec 11;516(7530):242-5. doi: 10.1038/nature13760. Epub 2014 Sep 28. PubMed PMID: 25274305; PubMed Central PMCID: PMC4268317.

Gaydos LJ, Wang W, Strome S. H3K27me and PRC2 transmit a memory of repression across generations and during development. Science. 2014 Sept 19;345(6203):1515-8.

Harburg G, Compton J, Liu W, Iwai N, Zada S, Marlow R, Strickland P, Zeng YA, Hinck L. SLIT/ROBO2 Signaling Promotes Mammary Stem Cell Senescence by Inhibiting Wnt Signaling. Stem Cell Reports. 2014 Sep 9; 3(3): 385–393.

Flach J, Bakker ST, Mohrin M, Conroy PC, Pietras EM, Reynaud D, Alvarez S, Diolaiti ME, Ugarte F, Forsberg EC, Le Beau MM, Stohr BA, Méndez J, Morrison CG, Passegué E. Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells.. Nature. 2014 July 30;512(7513):198-202.

Triplett JW, Wei W, Gonzalez C, Sweeney NT, Huberman AD, Feller MB, Feldheim DA. Dendritic and axonal targeting patterns of a genetically-specified class of retinal ganglion cells that participate in image-forming circuits. Neural Dev. 2014 Feb 5;9(1):2.

Halbisen MA, Ralston A. Shaking up the salt and pepper: origins of cellular heterogeneity in the inner cell mass of the blastocyst. EMBO J. 2014 Jan 27.

Epelman S, Lavine KJ, Beaudin AE, Sojka DK, Carrero JA, Calderon B, Brija T, Gautier EL, Ivanov S, Satpathy AT, Schilling JD, Schwendener R, Sergin I, Razani B, Forsberg EC, Yokoyama WM, Unanue ER, Colonna M, Randolph GJ, Mann DL. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity. 2014 Jan 16;40(1):91-104.

Guo C, Eckler MJ, McKenna WL, McKinsey GL, Rubenstein JL, Chen BFezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron. 2013 Dec 4;80(5):1167-74.

Beaudin AE, Boyer SW, Forsberg EC. Flk2/Flt3 promotes both myeloid and lymphoid development by expanding non-self-renewing multipotent hematopoietic progenitor cells. Exp Hematol. 2013 Dec 10. pii: S0301-472X(13)00922-3.

Ugarte F, Forsberg EC. Haematopoietic stem cell niches: new insights inspire new questions. EMBO J. 2013 Oct 2;32(19):2535-47.

Dorighi KM, Tamkun JW. The trithorax group proteins Kismet and ASH1 promote H3K36 dimethylation to counteract Polycomb group repression in Drosophila. Development. 2013 Oct;140(20):4182-92.

Roberts JM, Ennajdaoui H, Edmondson C, Wirth B, Sanford J, Chen B. Splicing factor TRA2B is required for neural progenitor survival. J Comp Neurol. 2013 Jul 1.

Kmet M, Guo C, Edmondson C, Chen B. Directed differentiation of human embryonic stem cells into corticofugal neurons uncovers heterogeneous fezf2-expressing subpopulations. PLoS One. 2013 Jun 24;8(6):e67292.

Frum T, Halbisen MA, Wang C, Amiri H, Robson P, Ralston A. Oct4 cell-autonomously promotes primitive endoderm development in the mouse blastocyst. Dev Cell. 2013 Jun 24;25(6):610-22.

Betancourt J, Katzman S, Chen B. Nuclear factor one b regulates neural stem cell differentiation and axonal projection of corticofugal neurons. J Comp Neurol. 2013 Jun 8. 

Hall MP, Nagel RJ, Fagg WS, Shiue L, Cline MS, Perriman RJ, Donohue JP, Ares M Jr. Quaking and PTB control overlapping splicing regulatory networks during muscle cell differentiation. RNA. 2013 May;19(5):627-38.

Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB, Leboeuf M, Becker CD, See P, Price J, Lucas D, Greter M, Mortha A, Boyer SW, Forsberg EC, Tanaka M, van Rooijen N, García-Sastre A, Stanley ER, Ginhoux F, Frenette PS, Merad M. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity. 2013 Apr 18;38(4):792-804.

Ballard MS, Hinck L. A roundabout way to cancer. Adv Cancer Res. 2012;114:187-235.

Kotadia S, Montembault E, Sullivan W, Royou A. Cell elongation is an adaptive response for clearing long chromatid arms from the cleavage plane. J Cell Biol. 2012 Nov 26;199(5):745-53.

Blij S, Frum T, Akyol A, Fearon E, Ralston A. Maternal Cdx2 is dispensable for mouse development. Development. 2012 Sep 19;139(21):3969-72. 

Boyer SW, Beaudin AE, Forsberg EC. Mapping differentiation pathways from hematopoietic stem cells using Flk2/Flt3 lineage tracing. Cell Cycle. 2012 Sep 1;11(17):3180-8.

Fasulo B, Deuring R, Murawska M, Gause M, Dorighi KM, Schaaf CA, Dorsett D, Brehm A, Tamkun JW. The Drosophila MI-2 chromatin-remodeling factor regulates higher-order chromatin structure and cohesin dynamics in vivo. PLoS Genet. 2012;8(8):e1002878.

Onodera CS, Underwood JG, Katzman S, Jacobs F, Greenberg D, Salama SR, Haussler D. Gene isoform specificity through enhancer-associated antisense transcription. PLoS One. 2012;7(8):e43511.

Tao X, Crest J, Kotadia S, Azucena O, Chen DC, Sullivan W, Kubby J. Live imaging using adaptive optics with fluorescent protein guide-stars. Optics Express. 2012 July 2:20(14):15969-82.

Smith-Berdan S, Schepers K, Ly A, Passegué E, Forsberg EC. Dynamic expression of the Robo ligand Slit2 in bone marrow cell populations. Cell Cycle. 2012 Feb 15;11(4):675-82.

Landmann F, Foster JM, Slatko BE, Sullivan W. Efficient in vitro RNA interference and immunofluorescence-based phenotype analysis in a human parasitic nematode, Brugia malayi. Parasit Vectors. 2012 Jan 13;5:16.

Harburg GC, Hinck L. Navigating breast cancer: axon guidance molecules as breast cancer tumor suppressors and oncogenes. J Mammary Gland Biol Neoplasia. 2011 Sep;16(3):257-70.

Boyer SW, Schroeder AV, Smith-Berdan S, Forsberg EC. All hematopoietic cells develop from hematopoietic stem cells through Flk2/Flt3-positive progenitor cells. Cell Stem Cell. 2011 Jul 8;9(1):64-73.

Koeva M, Forsberg EC, Stuart JM. Computational integration of homolog and pathway gene module expression reveals general stemness signatures. PLoS One. 2011 Apr 29;6(4):e18968.

Azucena O, Crest J, Kotadia S, Sullivan W, Tao X, Reinig M, Gavel D, Olivier S, Kubby J. Adaptive optics wide-field microscopy using direct wavefront sensing. Opt Lett. 2011 Mar 15;36(6):825-7.

Azucena O, Tao X, Crest J, Kotadia S, Sullivan W, Gavel D, Reinig M, Kubby JAdaptive optics wide-field microscope corrections using a MEMS DM and Shack-Hartmann wavefront sensor. SPIE Conf Proc. 2011 Feb 14;7931.

McKenna WL, Betancourt J, Larkin KA, Abrams B, Guo C, Rubenstein JL, Chen B. Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J Neurosci. 2011 Jan 12;31(2):549-64.

Eckler MJ, McKenna WL, Taghvaei S, McConnell SK, Chen BFezf1 and Fezf2 are required for olfactory development and sensory neuron identity. J Comp Neurol. 2011 Jan 12. doi: 10.1002/cne.22596. [Epub ahead of print]

Smith-Berdan S, Nguyen A, Hassanein D, Zimmer M, Ugarte F, Ciriza J, Li D, García-Ojeda ME, Hinck L, Forsberg EC. Robo4 cooperates with CXCR4 to specify hematopoietic stem cell localization to bone marrow niches. Cell Stem Cell. 2011 Jan 7;8(1):72-83.

Underwood JG, Uzilov AV, Katzman S, Onodera CS, Mainzer JE, Mathews DH, Lowe TM, Salama SR, Haussler D. FragSeq: transcriptome-wide RNA structure probing using high-throughput sequencing. Nat Methods. 2010 Dec;7(12):995-1001. Epub 2010 Nov 7.

Chang E, Forsberg EC, Wu J, Bingyin Wang, Prohaska SS, Allsopp R, Weissman IL, Cooke JP. Cholinergic activation of hematopoietic stem cells: role in tobacco-related disease? Vasc Med. 2010 Oct;15(5):375-85.

Azucena O, Crest J, Cao J, Sullivan W, Kner P, Gavel D, Dillon D, Olivier S, Kubby J. Wavefront aberration measurements and corrections through thick tissue using fluorescent microsphere reference beacons. Opt Express. 2010 Aug 2;18(16):17521-32.

Marlow R, Binnewies M, Sorensen LK, Monica SD, Strickland P, Forsberg EC, Li DY, Hinck L. Vascular Robo4 restricts proangiogenic VEGF signaling in breast. Proc Natl Acad Sci USA. 2010 Jun 8;107(23):10520-5. Epub 2010 May 24.

Azucena O, Crest J, Cao J, Sullivan W, Kner P, Gavel D, Dillon D, Olivier S, Kubby J. Implementation of adaptive optics in fluorescent microscopy using wavefront sensing and correction. SPIE Conf Proc. 2010 Feb;7595.

Ralston A, Cox BJ, Nishioka N, Sasaki H, Chea E, Rugg-Gunn P, Guo G, Robson P, Draper JS, Rossant J. Gata3 regulates trophoblast fate downstream of Tead4 and in parallel to Cdx2. Development. 2010 Feb;137(3):395-403.

Du H, Cline MS, Osborne RJ, Tuttle DL, Clark TA, Donohue JP, Hall MP, Shiue L, Swanson MS, Thornton CA, Ares M Jr. Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat Struct Mol Biol. 2010 Feb;17(2):187-93. Epub 2010 Jan 24.

Royou A, Gagou ME, Karess R, Sullivan W. BubR1- and Polo-coated DNA tethers facilitate poleward segregation of acentric chromatids. Cell 2010 Jan 22;140(2):235-45.

Forsberg EC, Passegué E, Prohaska SS, Wagers AJ, Koeva M, Stuart JM, Weissman IL. Molecular signatures of quiescent, mobilized and leukemia-initiating hematopoietic stem cells. PLoS One. 2010 Jan 20;5(1):e8785.

Ralston A, Rossant J. The genetics of induced pluripotency. Reproduction. 2010 Jan;139(1):35-44.

Albertson R, Casper-Lindley C, Cao J, Tram U, Sullivan W. Symmetric and asymmetric mitotic segregation patterns influence Wolbachia distribution in host somatic tissue. J Cell Sci. 2009 Dec 15;122(Pt 24):4570-83.

Forsberg EC, Smith-Berdan S. Parsing the niche code: the molecular mechanisms governing hematopoietic stem cell adhesion and differentiation. Haematologica. 2009 Nov;94(11):1477-81.

Santaguida M, Schepers K, King B, Sabnis AJ, Forsberg EC, Attema JL, Braun BS, Passegué E. JunB protects against myeloid malignancies by limiting hematopoietic stem cell proliferation and differentiation without affecting self-renewal. Cancer Cell. 2009 Apr 7;15(4):341-52.

Ooi AGL, Karsunky H, Majeti R, Butz B, Vestweber D, Ishida T, Quertermous T, Weissman IL, Forsberg EC. The adhesion molecule ESAM1 is a novel hematopoietic stem cell marker. Stem Cells. 2009 Mar;27(3):653-61.

Nishioka N, Inoue K, Adachi K, Kiyonari H, Ota M, Ralston A, Yabuta N, Hirahara S, Stephenson RO, Ogonuki N, Makita R, Kurihara H, Morin-Kensicki EM, Nojima H, Rossant J, Nakao K, Niwa H, Sasaki H. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell. 2009 Mar;16(3):398-410.

Azucena O, Kubby J, Crest J, Cao J, Sullivan W, Kner P, Gavel D, Dillon D, Olivier S. Implementation of a Shack-Hartmann wavefront sensor for the measurement of embryo-induced aberrations using fluorescent microscopy. SPIE Conf Proc. 2009 Feb 23;7209.

Suckiel E. Human embryonic stem cell research: a critical survey of the ethical issues. Adv Pediatr. 2008;55:79-96.

Royou A, McCusker D, Kellogg DR, Sullivan W. Grapes(Chk1) prevents nuclear CDK1 activation by delaying cyclin B nuclear accumulation. J Cell Biol. 2008 Oct 6;183(1):63-75.

Srinivasan S, Dorighi KM, Tamkun JW. Drosophila Kismet regulates histone H3 lysine 27 methylation and early elongation by RNA polymerase II. PLoS Genet. 2008 Oct;4(10):e1000217.

Mangel M, Bonsall MB. Phenotypic evolutionary models in stem cell biology: replacement, quiescence, and variability. PLoS ONE. 2008 Feb 13;3(2):e1591.

Ralston A, Rossant J. Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol. 2008 Jan 15;313(2):614-29.

Byrne AB, Weirauch MT, Wong V, Koeva M, Dixon SJ, Stuart JM, Roy PJ. A global analysis of genetic interactions in Caenorhabditis elegans. J Biol. 2007;6(3):8.

Wang T, Zeng J, Lowe CB, Sellers RG, Salama SR, Yang M, Burgess SM, Brachmann RK, Haussler DSpecies-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci U S A. 2007 Nov 20;104(47):18613-8.

Corona DF, Siriaco G, Armstrong JA, Snarskaya N, McClymont SA, Scott MP, Tamkun JW. ISWI regulates higher-order chromatin structure and histone H1 assembly in vivo. PLoS Biol. 2007 Sep;5(9):e232.

Riggs B, Fasulo B, Royou A, Mische S, Cao J, Hays TS, Sullivan W. The concentration of Nuf, a Rab11 effector, at the microtubule-organizing center is cell cycle regulated, dynein-dependent, and coincides with furrow formation. Mol Biol Cell. 2007 Sep;18(9):3313-22.

Attema JL, Papathanasiou P, Forsberg EC, Xu J, Smale ST, Weissman IL. Epigenetic characterization of hematopoietic stem cell differentiation using miniChIP and bisulfite sequencing analysis. Proc Natl Acad Sci USA. 2007;104:12371-6.

Forsberg EC, Bhattacharya D, Weissman IL. Hematopoietic stem cells: expression profiling and beyond. Stem Cell Reviews. 2006;2:23-30.

Forsberg EC, Serwold T, Kogan S, Weissman IL, Passegue E. New evidence supporting megakaryocyte-erythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors. Cell. 2006;126:415-26.

Pollard KS, Salama SR, Lambert N, Lambot MA, Coppens S, Pedersen JS, Katzman S, King B, Onodera C, Siepel A, Kern AD, Dehay C, Igel H, Ares M Jr, Vanderhaeghen P, Haussler D. An RNA gene expressed during cortical development evolved rapidly in humans. Nature. 2006 Sep 14;443(7108):167-72.

Forsberg EC, Prohaska SS, Katzman S, Heffner GC, Stuart JM, Weissman IL. Differential expression of novel potential regulators in hematopoietic stem cells. PLoS Genetics. 2005;Sep 1(3):e28.