Haifan Lin, PhD
Research & Publications
Biography
News
Research Summary
We study molecular mechanisms underlying the self-renewing division of stem cells. Currently, we focus on small RNA-mediated epigenetic programming and post-transcriptional regulation that are required for the self-renewal of germline and embryonic stem cells. Meanwhile, we are studying these mechanisms in cancer and germline development. Stem cells are characterized by their abilities to self-renew and to produce numerous differentiated daughter cells. These special properties enable stem cells to play a central role in generating and maintaining most tissues in higher organisms. Over-proliferation of stem cells can cause cancer, whereas under-proliferation of stem cells leads to tissue dystrophy, anemia, immuno-deficiency, or infertility. Drosophila and the mouse represent two powerful systems for studying stem cells since they allow easy access to combined genetic, cell biological, and molecular analyses. We use Drosophila as a pilot model to explore molecular mechanisms underlying stem cell division, and the mouse as an advanced model to expand what we learn from Drosophila to mammalian systems. Previously, we identified germline stem cells in the Drosophila ovary and revealed their self-renewing asymmetric division. We and others showed that the asymmetric division of these stem cells is controlled by both niche signaling and intracellular mechanisms. Using systematic genetic screens, we have identified key genes involved in both niche signaling and intracellular regulation of stem cell division. Among them, the argonaute/piwi gene family represent the only known gene family required for stem cell self-renewal in both animal and plant kingdoms. Currently, our research is focused on epigenetic programming and post-transcriptional regulation of germline stem cell self-renewal mediated by the Piwi proteins and a novel class of non-coding small RNAs called piwi-Interacting RNAs (piRNAs) that we and others discovered in 2006. Meanwhile, we have been studying post-transcriptional regulation of embryonic stem cells mediated by the Pumilio proteins.
Specialized Terms: Stem cell, small RNA, epigenetic programming, post-transcriptional regulation
Coauthors
Research Interests
Cell Biology; Genetics; Gynecology; RNA Processing, Post-Transcriptional; Stem Cells; Embryonic Stem Cells; Argonaute Proteins
Selected Publications
- Impaired neurogenesis alters brain biomechanics in a neuroprogenitor-based genetic subtype of congenital hydrocephalusDuy PQ, Weise SC, Marini C, Li XJ, Liang D, Dahl PJ, Ma S, Spajic A, Dong W, Juusola J, Kiziltug E, Kundishora AJ, Koundal S, Pedram MZ, Torres-Fernández LA, Händler K, De Domenico E, Becker M, Ulas T, Juranek SA, Cuevas E, Hao LT, Jux B, Sousa AMM, Liu F, Kim SK, Li M, Yang Y, Takeo Y, Duque A, Nelson-Williams C, Ha Y, Selvaganesan K, Robert SM, Singh AK, Allington G, Furey CG, Timberlake AT, Reeves BC, Smith H, Dunbar A, DeSpenza T, Goto J, Marlier A, Moreno-De-Luca A, Yu X, Butler WE, Carter BS, Lake EMR, Constable RT, Rakic P, Lin H, Deniz E, Benveniste H, Malvankar NS, Estrada-Veras JI, Walsh CA, Alper SL, Schultze JL, Paeschke K, Doetzlhofer A, Wulczyn FG, Jin SC, Lifton RP, Sestan N, Kolanus W, Kahle KT. Impaired neurogenesis alters brain biomechanics in a neuroprogenitor-based genetic subtype of congenital hydrocephalus Nature Neuroscience 2022, 25: 458-473. PMID: 35379995, PMCID: PMC9664907, DOI: 10.1038/s41593-022-01043-3.
- PUMILIO proteins promote colorectal cancer growth via suppressing p21Gong Y, Liu Z, Yuan Y, Yang Z, Zhang J, Lu Q, Wang W, Fang C, Lin H, Liu S. PUMILIO proteins promote colorectal cancer growth via suppressing p21 Nature Communications 2022, 13: 1627. PMID: 35338151, PMCID: PMC8956581, DOI: 10.1038/s41467-022-29309-1.
- Precision analysis of mutant U2AF1 activity reveals deployment of stress granules in myeloid malignanciesBiancon G, Joshi P, Zimmer JT, Hunck T, Gao Y, Lessard MD, Courchaine E, Barentine AES, Machyna M, Botti V, Qin A, Gbyli R, Patel A, Song Y, Kiefer L, Viero G, Neuenkirchen N, Lin H, Bewersdorf J, Simon MD, Neugebauer KM, Tebaldi T, Halene S. Precision analysis of mutant U2AF1 activity reveals deployment of stress granules in myeloid malignancies Molecular Cell 2022, 82: 1107-1122.e7. PMID: 35303483, PMCID: PMC8988922, DOI: 10.1016/j.molcel.2022.02.025.
- 20 years of Developmental Cell: Looking back.Chory J, Olson EN, Solnica-Krezel L, Munro S, Fuchs E, St Johnston D, Lefebvre V, Coupland G, Millar SE, Lin H. 20 years of Developmental Cell: Looking back. Developmental Cell 2021, 56: 3181-3184. PMID: 34875223, DOI: 10.1016/j.devcel.2021.11.014.
- Maternal Piwi regulates primordial germ cell development to ensure the fertility of female progeny in Drosophila.Gonzalez LE, Tang X, Lin H. Maternal Piwi regulates primordial germ cell development to ensure the fertility of female progeny in Drosophila. Genetics 2021, 219 PMID: 34142134, PMCID: PMC8757300, DOI: 10.1093/genetics/iyab091.
- CPA-seq reveals small ncRNAs with methylated nucleosides and diverse terminiWang H, Huang R, Li L, Zhu J, Li Z, Peng C, Zhuang X, Lin H, Shi S, Huang P. CPA-seq reveals small ncRNAs with methylated nucleosides and diverse termini Cell Discovery 2021, 7: 25. PMID: 33867522, PMCID: PMC8053708, DOI: 10.1038/s41421-021-00265-2.
- Mentorship in Science: Response to AlShebli et al., Nature Communications 2020.Mummery C, Little M, Lin H, Clark A, Zaret K, Srivastava D, Fuchs E, Watt F, Temple S. Mentorship in Science: Response to AlShebli et al., Nature Communications 2020. Stem Cell Reports 2021, 16: 1-2. PMID: 33440177, PMCID: PMC7815941, DOI: 10.1016/j.stemcr.2020.12.016.
- Roles of piRNAs in transposon and pseudogene regulation of germline mRNAs and lncRNAsWang C, Lin H. Roles of piRNAs in transposon and pseudogene regulation of germline mRNAs and lncRNAs Genome Biology 2021, 22: 27. PMID: 33419460, PMCID: PMC7792047, DOI: 10.1186/s13059-020-02221-x.
- Genome-wide mapping of Piwi association with specific loci in Drosophila ovariesLiu N, Neuenkirchen N, Zhong M, Lin H. Genome-wide mapping of Piwi association with specific loci in Drosophila ovaries G3: Genes, Genomes, Genetics 2021, 11: jkaa059. PMID: 33609367, PMCID: PMC8022938, DOI: 10.1093/g3journal/jkaa059.
- The Essential Function of SETDB1 in Homologous Chromosome Pairing and Synapsis during MeiosisCheng EC, Hsieh CL, Liu N, Wang J, Zhong M, Chen T, Li E, Lin H. The Essential Function of SETDB1 in Homologous Chromosome Pairing and Synapsis during Meiosis Cell Reports 2021, 34: 108575. PMID: 33406415, PMCID: PMC8513770, DOI: 10.1016/j.celrep.2020.108575.
- Ultradeep sequencing differentiates patterns of skin clonal mutations associated with sun-exposure status and skin cancer burdenWei L, Christensen SR, Fitzgerald ME, Graham J, Hutson ND, Zhang C, Huang Z, Hu Q, Zhan F, Xie J, Zhang J, Liu S, Remenyik E, Gellen E, Colegio OR, Bax M, Xu J, Lin H, Huss WJ, Foster BA, Paragh G. Ultradeep sequencing differentiates patterns of skin clonal mutations associated with sun-exposure status and skin cancer burden Science Advances 2021, 7: eabd7703. PMID: 33523857, PMCID: PMC7775785, DOI: 10.1126/sciadv.abd7703.
- Piwi in the stem cell niche regulates nurse cell number and oocyte specificationZhu G, Gonzalez LE, Lin H. Piwi in the stem cell niche regulates nurse cell number and oocyte specification MicroPublication Biology 2020, 2020: 10.17912/micropub.biology.000327. PMID: 33274324, PMCID: PMC7704254, DOI: 10.17912/micropub.biology.000327.
- Ovarian somatic Piwi regulates nurse cell proliferation and oocyte specification in DrosophilaGonzalez LE, Zhu G, Lin H. Ovarian somatic Piwi regulates nurse cell proliferation and oocyte specification in Drosophila MicroPublication Biology 2020, 2020: 10.17912/micropub.biology.000324. PMID: 33274329, PMCID: PMC7704259, DOI: 10.17912/micropub.biology.000324.
- PIWIL1 promotes gastric cancer via a piRNA-independent mechanismShi S, Yang ZZ, Liu S, Yang F, Lin H. PIWIL1 promotes gastric cancer via a piRNA-independent mechanism Proceedings Of The National Academy Of Sciences Of The United States Of America 2020, 117: 22390-22401. PMID: 32848063, PMCID: PMC7486755, DOI: 10.1073/pnas.2008724117.
- MIWI prevents aneuploidy during meiosis by cleaving excess satellite RNAHsieh C, Xia J, Lin H. MIWI prevents aneuploidy during meiosis by cleaving excess satellite RNA The EMBO Journal 2020, 39: e103614. PMID: 32677148, PMCID: PMC7429737, DOI: 10.15252/embj.2019103614.
- Pumilio proteins utilize distinct regulatory mechanisms to achieve complementary functions required for pluripotency and embryogenesisUyhazi KE, Yang Y, Liu N, Qi H, Huang XA, Mak W, Weatherbee SD, de Prisco N, Gennarino VA, Song X, Lin H. Pumilio proteins utilize distinct regulatory mechanisms to achieve complementary functions required for pluripotency and embryogenesis Proceedings Of The National Academy Of Sciences Of The United States Of America 2020, 117: 7851-7862. PMID: 32198202, PMCID: PMC7148564, DOI: 10.1073/pnas.1916471117.
- Development of a Brigatinib degrader (SIAIS117) as a potential treatment for ALK positive cancer resistanceSun N, Ren C, Kong Y, Zhong H, Chen J, Li Y, Zhang J, Zhou Y, Qiu X, Lin H, Song X, Yang X, Jiang B. Development of a Brigatinib degrader (SIAIS117) as a potential treatment for ALK positive cancer resistance European Journal Of Medicinal Chemistry 2020, 193: 112190. PMID: 32179332, DOI: 10.1016/j.ejmech.2020.112190.
- PIWI–piRNA pathway-mediated transposable element repression in Hydra somatic stem cellsTeefy BB, Siebert S, Cazet JF, Lin H, Juliano CE. PIWI–piRNA pathway-mediated transposable element repression in Hydra somatic stem cells RNA 2020, 26: 550-563. PMID: 32075940, PMCID: PMC7161359, DOI: 10.1261/rna.072835.119.
- Heat shock protein DNAJA1 stabilizes PIWI proteins to support regeneration and homeostasis of planarian Schmidtea mediterraneaWang C, Yang ZZ, Guo FH, Shi S, Han XS, Zeng A, Lin H, Jing Q. Heat shock protein DNAJA1 stabilizes PIWI proteins to support regeneration and homeostasis of planarian Schmidtea mediterranea Journal Of Biological Chemistry 2019, 294: 9873-9887. PMID: 31076507, PMCID: PMC6597837, DOI: 10.1074/jbc.ra118.004445.
- The Role of Maternal HP1a in Early Drosophila Embryogenesis via Regulation of Maternal Transcript ProductionPark AR, Liu N, Neuenkirchen N, Guo Q, Lin H. The Role of Maternal HP1a in Early Drosophila Embryogenesis via Regulation of Maternal Transcript Production Genetics 2018, 211: genetics.301704.2018. PMID: 30442760, PMCID: PMC6325692, DOI: 10.1534/genetics.118.301704.
- A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesisMak W, Xia J, Cheng EC, Lowther K, Lin H. A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis Cell & Bioscience 2018, 8: 54. PMID: 30364263, PMCID: PMC6194604, DOI: 10.1186/s13578-018-0251-1.
- MIWI2 targets RNAs transcribed from piRNA‐dependent regions to drive DNA methylation in mouse prospermatogoniaWatanabe T, Cui X, Yuan Z, Qi H, Lin H. MIWI2 targets RNAs transcribed from piRNA‐dependent regions to drive DNA methylation in mouse prospermatogonia The EMBO Journal 2018, 37 PMID: 30108053, PMCID: PMC6138435, DOI: 10.15252/embj.201695329.
- miR-221/222 activate the Wnt/β-catenin signaling to promote triple-negative breast cancerLiu S, Wang Z, Liu Z, Shi S, Zhang Z, Zhang J, Lin H. miR-221/222 activate the Wnt/β-catenin signaling to promote triple-negative breast cancer Journal Of Molecular Cell Biology 2018, 10: 302-315. PMID: 30053090, DOI: 10.1093/jmcb/mjy041.
- A critical role for nucleoporin 358 (Nup358) in transposon silencing and piRNA biogenesis in DrosophilaParikh RY, Lin H, Gangaraju VK. A critical role for nucleoporin 358 (Nup358) in transposon silencing and piRNA biogenesis in Drosophila Journal Of Biological Chemistry 2018, 293: 9140-9147. PMID: 29735528, PMCID: PMC6005430, DOI: 10.1074/jbc.ac118.003264.
- Novel evidence for a PIWI-interacting RNA (piRNA) as an oncogenic mediator of disease progression, and a potential prognostic biomarker in colorectal cancerWeng W, Liu N, Toiyama Y, Kusunoki M, Nagasaka T, Fujiwara T, Wei Q, Qin H, Lin H, Ma Y, Goel A. Novel evidence for a PIWI-interacting RNA (piRNA) as an oncogenic mediator of disease progression, and a potential prognostic biomarker in colorectal cancer Molecular Cancer 2018, 17: 16. PMID: 29382334, PMCID: PMC5791351, DOI: 10.1186/s12943-018-0767-3.
- Post-transcriptional regulation of mouse neurogenesis by Pumilio proteinsZhang M, Chen D, Xia J, Han W, Cui X, Neuenkirchen N, Hermes G, Sestan N, Lin H. Post-transcriptional regulation of mouse neurogenesis by Pumilio proteins Genes & Development 2017, 31: 1354-1369. PMID: 28794184, PMCID: PMC5580656, DOI: 10.1101/gad.298752.117.
- PIWI-Interacting RNAs in Gliomagenesis: Evidence from Post-GWAS and Functional AnalysesJacobs DI, Qin Q, Lerro MC, Fu A, Dubrow R, Claus EB, DeWan AT, Wang G, Lin H, Zhu Y. PIWI-Interacting RNAs in Gliomagenesis: Evidence from Post-GWAS and Functional Analyses Cancer Epidemiology Biomarkers & Prevention 2016, 25: 1073-1080. PMID: 27197292, DOI: 10.1158/1055-9965.epi-16-0047.
- An Important Role of Pumilio 1 in Regulating the Development of the Mammalian Female Germline1Mak W, Fang C, Holden T, Dratver MB, Lin H. An Important Role of Pumilio 1 in Regulating the Development of the Mammalian Female Germline1 Biology Of Reproduction 2016, 94: 134, 1-11. PMID: 27170441, PMCID: PMC4946805, DOI: 10.1095/biolreprod.115.137497.
- Change point analysis of histone modifications reveals epigenetic blocks linking to physical domainsChen M, Lin H, Zhao H. Change point analysis of histone modifications reveals epigenetic blocks linking to physical domains The Annals Of Applied Statistics 2016, 10: 506-526. PMID: 27231496, PMCID: PMC4876974, DOI: 10.1214/16-aoas905.
- The Role of PIWIL4, an Argonaute Family Protein, in Breast Cancer*Wang Z, Liu N, Shi S, Liu S, Lin H. The Role of PIWIL4, an Argonaute Family Protein, in Breast Cancer* Journal Of Biological Chemistry 2016, 291: 10646-10658. PMID: 26957540, PMCID: PMC4865913, DOI: 10.1074/jbc.m116.723239.
- Tudor-SN Interacts with Piwi Antagonistically in Regulating Spermatogenesis but Synergistically in Silencing Transposons in DrosophilaKu HY, Gangaraju VK, Qi H, Liu N, Lin H. Tudor-SN Interacts with Piwi Antagonistically in Regulating Spermatogenesis but Synergistically in Silencing Transposons in Drosophila PLOS Genetics 2016, 12: e1005813. PMID: 26808625, PMCID: PMC4726654, DOI: 10.1371/journal.pgen.1005813.
- Piwi maintains germline stem cells and oogenesis in Drosophila through negative regulation of Polycomb group proteinsPeng JC, Valouev A, Liu N, Lin H. Piwi maintains germline stem cells and oogenesis in Drosophila through negative regulation of Polycomb group proteins Nature Genetics 2016, 48: 283-291. PMID: 26780607, PMCID: PMC4767590, DOI: 10.1038/ng.3486.
- Poreless eggshellsLin H, Matzuk MM. Poreless eggshells Journal Of Clinical Investigation 2015, 125: 4005-4007. PMID: 26485282, PMCID: PMC4639988, DOI: 10.1172/jci84692.
- Embryonic Stem Cells License a High Level of Dormant Origins to Protect the Genome against Replication StressGe XQ, Han J, Cheng EC, Yamaguchi S, Shima N, Thomas JL, Lin H. Embryonic Stem Cells License a High Level of Dormant Origins to Protect the Genome against Replication Stress Stem Cell Reports 2015, 5: 185-194. PMID: 26190528, PMCID: PMC4618655, DOI: 10.1016/j.stemcr.2015.06.002.
- Piwi Is a Key Regulator of Both Somatic and Germline Stem Cells in the Drosophila TestisGonzalez J, Qi H, Liu N, Lin H. Piwi Is a Key Regulator of Both Somatic and Germline Stem Cells in the Drosophila Testis Cell Reports 2015, 12: 150-161. PMID: 26119740, PMCID: PMC4497877, DOI: 10.1016/j.celrep.2015.06.004.
- Reassessment of Piwi Binding to the Genome and Piwi Impact on RNA Polymerase II DistributionLin H, Chen M, Kundaje A, Valouev A, Yin H, Liu N, Neuenkirchen N, Zhong M, Snyder M. Reassessment of Piwi Binding to the Genome and Piwi Impact on RNA Polymerase II Distribution Developmental Cell 2015, 32: 772-774. PMID: 25805139, PMCID: PMC4472434, DOI: 10.1016/j.devcel.2015.03.004.
- Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germlineWatanabe T, Cheng EC, Zhong M, Lin H. Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germline Genome Research 2014, 25: 368-380. PMID: 25480952, PMCID: PMC4352877, DOI: 10.1101/gr.180802.114.
- Posttranscriptional Regulation of Gene Expression by Piwi Proteins and piRNAsWatanabe T, Lin H. Posttranscriptional Regulation of Gene Expression by Piwi Proteins and piRNAs Molecular Cell 2014, 56: 18-27. PMID: 25280102, PMCID: PMC4185416, DOI: 10.1016/j.molcel.2014.09.012.
- PIWI Proteins Are Dispensable for Mouse Somatic Development and Reprogramming of Fibroblasts into Pluripotent Stem CellsCheng EC, Kang D, Wang Z, Lin H. PIWI Proteins Are Dispensable for Mouse Somatic Development and Reprogramming of Fibroblasts into Pluripotent Stem Cells PLOS ONE 2014, 9: e97821. PMID: 25238487, PMCID: PMC4169525, DOI: 10.1371/journal.pone.0097821.
- Generation of transgenic Hydra by embryo microinjection.Juliano CE, Lin H, Steele RE. Generation of transgenic Hydra by embryo microinjection. Journal Of Visualized Experiments 2014, 51888. PMID: 25285460, PMCID: PMC4828061, DOI: 10.3791/51888.
- Noncoding RNAs in the regulation of DNA replicationGe XQ, Lin H. Noncoding RNAs in the regulation of DNA replication Trends In Biochemical Sciences 2014, 39: 341-343. PMID: 25027733, PMCID: PMC4265214, DOI: 10.1016/j.tibs.2014.06.003.
- PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expressionKu HY, Lin H. PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression National Science Review 2014, 1: 205-218. PMID: 25512877, PMCID: PMC4265212, DOI: 10.1093/nsr/nwu014.
- The ever-expanding RNA worldLin H. The ever-expanding RNA world National Science Review 2014, 1: 182-182. PMID: 25520852, PMCID: PMC4266142, DOI: 10.1093/nsr/nwu010.
- Piwi Is Required in Multiple Cell Types to Control Germline Stem Cell Lineage Development in the Drosophila OvaryMa X, Wang S, Do T, Song X, Inaba M, Nishimoto Y, Liu LP, Gao Y, Mao Y, Li H, McDowell W, Park J, Malanowski K, Peak A, Perera A, Li H, Gaudenz K, Haug J, Yamashita Y, Lin H, Ni JQ, Xie T. Piwi Is Required in Multiple Cell Types to Control Germline Stem Cell Lineage Development in the Drosophila Ovary PLOS ONE 2014, 9: e90267. PMID: 24658126, PMCID: PMC3962343, DOI: 10.1371/journal.pone.0090267.
- PIWI proteins and PIWI-interacting RNAs in the somaRoss RJ, Weiner MM, Lin H. PIWI proteins and PIWI-interacting RNAs in the soma Nature 2014, 505: 353-359. PMID: 24429634, PMCID: PMC4265809, DOI: 10.1038/nature12987.
- PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cellsJuliano CE, Reich A, Liu N, Götzfried J, Zhong M, Uman S, Reenan RA, Wessel GM, Steele RE, Lin H. PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells Proceedings Of The National Academy Of Sciences Of The United States Of America 2013, 111: 337-342. PMID: 24367095, PMCID: PMC3890812, DOI: 10.1073/pnas.1320965111.
- PIWI proteins are essential for early Drosophila embryogenesisMani SR, Megosh H, Lin H. PIWI proteins are essential for early Drosophila embryogenesis Developmental Biology 2013, 385: 340-349. PMID: 24184635, PMCID: PMC3915879, DOI: 10.1016/j.ydbio.2013.10.017.
- Chromatin Immunoprecipitation Assay of Piwi in DrosophilaYin H, Lin H. Chromatin Immunoprecipitation Assay of Piwi in Drosophila 2013, 1093: 1-11. PMID: 24178552, DOI: 10.1007/978-1-62703-694-8_1.
- Piwi Genes Are Dispensable for Normal Hematopoiesis in MiceNolde MJ, Cheng EC, Guo S, Lin H. Piwi Genes Are Dispensable for Normal Hematopoiesis in Mice PLOS ONE 2013, 8: e71950. PMID: 24058407, PMCID: PMC3751959, DOI: 10.1371/journal.pone.0071950.
- Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germlineSaxe JP, Chen M, Zhao H, Lin H. Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline The EMBO Journal 2013, 32: 1869-1885. PMID: 23714778, PMCID: PMC3981179, DOI: 10.1038/emboj.2013.121.
- Repressing the Repressor: A lincRNA as a MicroRNA Sponge in Embryonic Stem Cell Self-RenewalCheng EC, Lin H. Repressing the Repressor: A lincRNA as a MicroRNA Sponge in Embryonic Stem Cell Self-Renewal Developmental Cell 2013, 25: 1-2. PMID: 23597480, PMCID: PMC3906851, DOI: 10.1016/j.devcel.2013.03.020.
- Beyond transposons: the epigenetic and somatic functions of the Piwi-piRNA mechanismPeng JC, Lin H. Beyond transposons: the epigenetic and somatic functions of the Piwi-piRNA mechanism Current Opinion In Cell Biology 2013, 25: 190-194. PMID: 23465540, PMCID: PMC3651849, DOI: 10.1016/j.ceb.2013.01.010.
- A Major Epigenetic Programming Mechanism Guided by piRNAsHuang XA, Yin H, Sweeney S, Raha D, Snyder M, Lin H. A Major Epigenetic Programming Mechanism Guided by piRNAs Developmental Cell 2013, 24: 502-516. PMID: 23434410, PMCID: PMC3600162, DOI: 10.1016/j.devcel.2013.01.023.
- Function of Piwi, a nuclear Piwi/Argonaute protein, is independent of its slicer activityDarricarrère N, Liu N, Watanabe T, Lin H. Function of Piwi, a nuclear Piwi/Argonaute protein, is independent of its slicer activity Proceedings Of The National Academy Of Sciences Of The United States Of America 2013, 110: 1297-1302. PMID: 23297219, PMCID: PMC3557079, DOI: 10.1073/pnas.1213283110.
- Capturing the Cloud: UAP56 in Nuage Assembly and FunctionLin H. Capturing the Cloud: UAP56 in Nuage Assembly and Function Cell 2012, 151: 699-701. PMID: 23141532, PMCID: PMC4234066, DOI: 10.1016/j.cell.2012.10.026.
- piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanismBeyret E, Liu N, Lin H. piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism Cell Research 2012, 22: 1429-1439. PMID: 22907665, PMCID: PMC3463270, DOI: 10.1038/cr.2012.120.
- Essential Roles of the Chromatin Remodeling Factor Brg1 in Spermatogenesis in Mice1Wang J, Gu H, Lin H, Chi T. Essential Roles of the Chromatin Remodeling Factor Brg1 in Spermatogenesis in Mice1 Biology Of Reproduction 2012, 86: article 186, 1-10. PMID: 22495890, PMCID: PMC3386149, DOI: 10.1095/biolreprod.111.097097.
- High‐Efficiency Transfection and siRNA‐Mediated Gene Knockdown in Human Pluripotent Stem CellsMa Y, Lin H, Qiu C. High‐Efficiency Transfection and siRNA‐Mediated Gene Knockdown in Human Pluripotent Stem Cells Current Protocols In Stem Cell Biology 2012, 21: 5c.2.1-5c.2.9. PMID: 22605647, DOI: 10.1002/9780470151808.sc05c02s21.
- Pumilio 1 Suppresses Multiple Activators of p53 to Safeguard SpermatogenesisChen D, Zheng W, Lin A, Uyhazi K, Zhao H, Lin H. Pumilio 1 Suppresses Multiple Activators of p53 to Safeguard Spermatogenesis Current Biology 2012, 22: 420-425. PMID: 22342750, PMCID: PMC3449084, DOI: 10.1016/j.cub.2012.01.039.
- A High-Resolution Whole-Genome Map of Key Chromatin Modifications in the Adult Drosophila melanogasterYin H, Sweeney S, Raha D, Snyder M, Lin H. A High-Resolution Whole-Genome Map of Key Chromatin Modifications in the Adult Drosophila melanogaster PLOS Genetics 2011, 7: e1002380. PMID: 22194694, PMCID: PMC3240582, DOI: 10.1371/journal.pgen.1002380.
- The microRNA regulation of stem cellsHuang XA, Lin H. The microRNA regulation of stem cells Wiley Interdisciplinary Reviews Membrane Transport And Signalling 2011, 1: 83-95. PMID: 23024929, PMCID: PMC3459065, DOI: 10.1002/wdev.5.
- The microRNA regulation of stem cells.Huang XA, Lin H. The microRNA regulation of stem cells. WIREs Mechanisms Of Disease 2011, 1: 83-95. PMID: 23801669, DOI: 10.1002/wdev.5.
- Uniting Germline and Stem Cells: The Function of Piwi Proteins and the piRNA Pathway in Diverse OrganismsJuliano C, Wang J, Lin H. Uniting Germline and Stem Cells: The Function of Piwi Proteins and the piRNA Pathway in Diverse Organisms Annual Review Of Genetics 2011, 45: 447-469. PMID: 21942366, PMCID: PMC3832951, DOI: 10.1146/annurev-genet-110410-132541.
- Small Noncoding RNAs in the GermlineSaxe JP, Lin H. Small Noncoding RNAs in the Germline Cold Spring Harbor Perspectives In Biology 2011, 3: a002717. PMID: 21669983, PMCID: PMC3181032, DOI: 10.1101/cshperspect.a002717.
- Role for piRNAs and Noncoding RNA in de Novo DNA Methylation of the Imprinted Mouse Rasgrf1 LocusWatanabe T, Tomizawa S, Mitsuya K, Totoki Y, Yamamoto Y, Kuramochi-Miyagawa S, Iida N, Hoki Y, Murphy PJ, Toyoda A, Gotoh K, Hiura H, Arima T, Fujiyama A, Sado T, Shibata T, Nakano T, Lin H, Ichiyanagi K, Soloway PD, Sasaki H. Role for piRNAs and Noncoding RNA in de Novo DNA Methylation of the Imprinted Mouse Rasgrf1 Locus Science 2011, 332: 848-852. PMID: 21566194, PMCID: PMC3368507, DOI: 10.1126/science.1203919.
- Pinpointing the expression of piRNAs and function of the PIWI protein subfamily during spermatogenesis in the mouseBeyret E, Lin H. Pinpointing the expression of piRNAs and function of the PIWI protein subfamily during spermatogenesis in the mouse Developmental Biology 2011, 355: 215-226. PMID: 21539824, PMCID: PMC3443393, DOI: 10.1016/j.ydbio.2011.04.021.
- PAPI, a novel TUDOR-domain protein, complexes with AGO3, ME31B and TRAL in the nuage to silence transpositionLiu L, Qi H, Wang J, Lin H. PAPI, a novel TUDOR-domain protein, complexes with AGO3, ME31B and TRAL in the nuage to silence transposition Development 2011, 138: 1863-1873. PMID: 21447556, PMCID: PMC3074456, DOI: 10.1242/dev.059287.
- Genome‐Wide Studies Reveal That Lin28 Enhances the Translation of Genes Important for Growth and Survival of Human Embryonic Stem CellsPeng S, Chen L, Lei X, Yang L, Lin H, Carmichael GG, Huang Y. Genome‐Wide Studies Reveal That Lin28 Enhances the Translation of Genes Important for Growth and Survival of Human Embryonic Stem Cells Stem Cells 2011, 29: 496-504. PMID: 21425412, DOI: 10.1002/stem.591.
- MITOPLD Is a Mitochondrial Protein Essential for Nuage Formation and piRNA Biogenesis in the Mouse GermlineWatanabe T, Chuma S, Yamamoto Y, Kuramochi-Miyagawa S, Totoki Y, Toyoda A, Hoki Y, Fujiyama A, Shibata T, Sado T, Noce T, Nakano T, Nakatsuji N, Lin H, Sasaki H. MITOPLD Is a Mitochondrial Protein Essential for Nuage Formation and piRNA Biogenesis in the Mouse Germline Developmental Cell 2011, 20: 364-375. PMID: 21397847, PMCID: PMC3062204, DOI: 10.1016/j.devcel.2011.01.005.
- Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variationGangaraju VK, Yin H, Weiner MM, Wang J, Huang XA, Lin H. Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation Nature Genetics 2010, 43: 153-158. PMID: 21186352, PMCID: PMC3443399, DOI: 10.1038/ng.743.
- The Yb Body, a Major Site for Piwi-associated RNA Biogenesis and a Gateway for Piwi Expression and Transport to the Nucleus in Somatic Cells*Qi H, Watanabe T, Ku HY, Liu N, Zhong M, Lin H. The Yb Body, a Major Site for Piwi-associated RNA Biogenesis and a Gateway for Piwi Expression and Transport to the Nucleus in Somatic Cells* Journal Of Biological Chemistry 2010, 286: 3789-3797. PMID: 21106531, PMCID: PMC3030380, DOI: 10.1074/jbc.m110.193888.
- High-efficiency siRNA-based gene knockdown in human embryonic stem cellsMa Y, Jin J, Dong C, Cheng EC, Lin H, Huang Y, Qiu C. High-efficiency siRNA-based gene knockdown in human embryonic stem cells RNA 2010, 16: 2564-2569. PMID: 20978109, PMCID: PMC2995416, DOI: 10.1261/rna.2350710.
- Identification of Piwil2-Like (PL2L) Proteins that Promote TumorigenesisYe Y, Yin DT, Chen L, Zhou Q, Shen R, He G, Yan Q, Tong Z, Issekutz AC, Shapiro CL, Barsky SH, Lin H, Li JJ, Gao JX. Identification of Piwil2-Like (PL2L) Proteins that Promote Tumorigenesis PLOS ONE 2010, 5: e13406. PMID: 20975993, PMCID: PMC2958115, DOI: 10.1371/journal.pone.0013406.
- A Drosophila Chromatin Factor Interacts With the Piwi-Interacting RNA Mechanism in Niche Cells to Regulate Germline Stem Cell Self-RenewalSmulders-Srinivasan TK, Szakmary A, Lin H. A Drosophila Chromatin Factor Interacts With the Piwi-Interacting RNA Mechanism in Niche Cells to Regulate Germline Stem Cell Self-Renewal Genetics 2010, 186: 573-583. PMID: 20647505, PMCID: PMC2954472, DOI: 10.1534/genetics.110.119081.
- Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencingWu JQ, Habegger L, Noisa P, Szekely A, Qiu C, Hutchison S, Raha D, Egholm M, Lin H, Weissman S, Cui W, Gerstein M, Snyder M. Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing Proceedings Of The National Academy Of Sciences Of The United States Of America 2010, 107: 5254-5259. PMID: 20194744, PMCID: PMC2841935, DOI: 10.1073/pnas.0914114107.
- The Biogenesis and Function of PIWI Proteins and piRNAs: Progress and ProspectThomson T, Lin H. The Biogenesis and Function of PIWI Proteins and piRNAs: Progress and Prospect Annual Review Of Cell And Developmental Biology 2009, 25: 355-376. PMID: 19575643, PMCID: PMC2780330, DOI: 10.1146/annurev.cellbio.24.110707.175327.
- Stem Cells in 2009McKay RD, van der Kooy D, Zwaka TP, Lin H. Stem Cells in 2009 Cell Stem Cell 2009, 5: 483-489. PMID: 19896440, DOI: 10.1016/j.stem.2009.10.012.
- The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogasterSzakmary A, Reedy M, Qi H, Lin H. The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster Journal Of Cell Biology 2009, 185: 613-627. PMID: 19433453, PMCID: PMC2711570, DOI: 10.1083/jcb.200903034.
- Mili Interacts with Tudor Domain-Containing Protein 1 in Regulating SpermatogenesisWang J, Saxe JP, Tanaka T, Chuma S, Lin H. Mili Interacts with Tudor Domain-Containing Protein 1 in Regulating Spermatogenesis Current Biology 2009, 19: 640-644. PMID: 19345100, PMCID: PMC2704239, DOI: 10.1016/j.cub.2009.02.061.
- MicroRNAs: key regulators of stem cellsGangaraju VK, Lin H. MicroRNAs: key regulators of stem cells Nature Reviews Molecular Cell Biology 2009, 10: 116-125. PMID: 19165214, PMCID: PMC4118578, DOI: 10.1038/nrm2621.
- MILI, a PIWI-interacting RNA-binding Protein, Is Required for Germ Line Stem Cell Self-renewal and Appears to Positively Regulate Translation*Unhavaithaya Y, Hao Y, Beyret E, Yin H, Kuramochi-Miyagawa S, Nakano T, Lin H. MILI, a PIWI-interacting RNA-binding Protein, Is Required for Germ Line Stem Cell Self-renewal and Appears to Positively Regulate Translation* Journal Of Biological Chemistry 2008, 284: 6507-6519. PMID: 19114715, PMCID: PMC2649106, DOI: 10.1074/jbc.m809104200.
- Piecing Together the Mosaic of Early Mammalian Development through MicroRNAs*Blakaj A, Lin H. Piecing Together the Mosaic of Early Mammalian Development through MicroRNAs* Journal Of Biological Chemistry 2008, 283: 9505-9508. PMID: 18272516, PMCID: PMC2442291, DOI: 10.1074/jbc.r800002200.
- Cell biology of stem cells: an enigma of asymmetry and self-renewalLin H. Cell biology of stem cells: an enigma of asymmetry and self-renewal Journal Of Cell Biology 2008, 180: 257-260. PMID: 18227277, PMCID: PMC2213586, DOI: 10.1083/jcb.200712159.
- An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogasterYin H, Lin H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster Nature 2007, 450: 304-308. PMID: 17952056, DOI: 10.1038/nature06263.
- Drosophila PIWI associates with chromatin and interacts directly with HP1aBrower-Toland B, Findley SD, Jiang L, Liu L, Yin H, Dus M, Zhou P, Elgin SC, Lin H. Drosophila PIWI associates with chromatin and interacts directly with HP1a Genes & Development 2007, 21: 2300-2311. PMID: 17875665, PMCID: PMC1973144, DOI: 10.1101/gad.1564307.
- piRNAs in the Germ LineLin H. piRNAs in the Germ Line Science 2007, 316: 397-397. PMID: 17446387, DOI: 10.1126/science.1137543.
- Precancerous Stem Cells Have the Potential for both Benign and Malignant DifferentiationChen L, Shen R, Ye Y, Pu XA, Liu X, Duan W, Wen J, Zimmerer J, Wang Y, Liu Y, Lasky LC, Heerema NA, Perrotti D, Ozato K, Kuramochi-Miyagawa S, Nakano T, Yates AJ, Carson WE, Lin H, Barsky SH, Gao JX. Precancerous Stem Cells Have the Potential for both Benign and Malignant Differentiation PLOS ONE 2007, 2: e293. PMID: 17356702, PMCID: PMC1808425, DOI: 10.1371/journal.pone.0000293.
- Dr. Haifan Lin. Interviewed by Han Lee and Rachel Rosenstein.Lin H. Dr. Haifan Lin. Interviewed by Han Lee and Rachel Rosenstein. The Yale Journal Of Biology And Medicine 2006, 79: 187-91. PMID: 17940631, PMCID: PMC1994806.
- Sex-lethal is a target of Bruno-mediated translational repression in promoting the differentiation of stem cell progeny during Drosophila oogenesisWang Z, Lin H. Sex-lethal is a target of Bruno-mediated translational repression in promoting the differentiation of stem cell progeny during Drosophila oogenesis Developmental Biology 2006, 302: 160-168. PMID: 17067567, PMCID: PMC1904479, DOI: 10.1016/j.ydbio.2006.09.016.
- MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesisGrivna ST, Pyhtila B, Lin H. MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis Proceedings Of The National Academy Of Sciences Of The United States Of America 2006, 103: 13415-13420. PMID: 16938833, PMCID: PMC1569178, DOI: 10.1073/pnas.0605506103.
- The Role of PIWI and the miRNA Machinery in Drosophila Germline DeterminationMegosh HB, Cox DN, Campbell C, Lin H. The Role of PIWI and the miRNA Machinery in Drosophila Germline Determination Current Biology 2006, 16: 1884-1894. PMID: 16949822, DOI: 10.1016/j.cub.2006.08.051.
- A novel class of small RNAs in mouse spermatogenic cellsGrivna ST, Beyret E, Wang Z, Lin H. A novel class of small RNAs in mouse spermatogenic cells Genes & Development 2006, 20: 1709-1714. PMID: 16766680, PMCID: PMC1522066, DOI: 10.1101/gad.1434406.
- Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cellsKotaja N, Lin H, Parvinen M, Sassone-Corsi P. Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cells Journal Of Cell Science 2006, 119: 2819-2825. PMID: 16787948, DOI: 10.1242/jcs.03022.
- The Division of Drosophila Germline Stem Cells and Their Precursors Requires a Specific CyclinWang Z, Lin H. The Division of Drosophila Germline Stem Cells and Their Precursors Requires a Specific Cyclin Current Biology 2005, 15: 328-333. PMID: 15723793, DOI: 10.1016/j.cub.2005.02.016.
- Regulatory Relationship among piwi, pumilio, and bag-of-marbles in Drosophila Germline Stem Cell Self-Renewal and DifferentiationSzakmary A, Cox DN, Wang Z, Lin H. Regulatory Relationship among piwi, pumilio, and bag-of-marbles in Drosophila Germline Stem Cell Self-Renewal and Differentiation Current Biology 2005, 15: 171-178. PMID: 15668175, DOI: 10.1016/j.cub.2005.01.005.
- Germline stem cells in the Drosophila ovary descend from pole cells in the anterior region of the embryonic gonadAsaoka M, Lin H. Germline stem cells in the Drosophila ovary descend from pole cells in the anterior region of the embryonic gonad Development 2004, 131: 5079-5089. PMID: 15459101, DOI: 10.1242/dev.01391.
- Nanos Maintains Germline Stem Cell Self-Renewal by Preventing DifferentiationWang Z, Lin H. Nanos Maintains Germline Stem Cell Self-Renewal by Preventing Differentiation Science 2004, 303: 2016-2019. PMID: 14976263, DOI: 10.1126/science.1093983.
- Mili, a mammalian member of piwi family gene, is essential for spermatogenesisKuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, Nakano T. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis Development 2004, 131: 839-849. PMID: 14736746, DOI: 10.1242/dev.00973.
- Screens for piwi suppressors in Drosophila identify dosage-dependent regulators of germline stem cell division.Smulders-Srinivasan TK, Lin H. Screens for piwi suppressors in Drosophila identify dosage-dependent regulators of germline stem cell division. Genetics 2003, 165: 1971-91. PMID: 14704180, PMCID: PMC1462913, DOI: 10.1093/genetics/165.4.1971.
- To be and not to beLin H. To be and not to be Nature 2003, 425: 353-355. PMID: 14508468, DOI: 10.1038/425353a.
- The stem-cell niche theory: lessons from fliesLin H. The stem-cell niche theory: lessons from flies Nature Reviews Genetics 2002, 3: 931-940. PMID: 12459723, DOI: 10.1038/nrg952.
- Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomasQiao D, Zeeman AM, Deng W, Looijenga LH, Lin H. Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas Oncogene 2002, 21: 3988-3999. PMID: 12037681, DOI: 10.1038/sj.onc.1205505.
- miwi, a Murine Homolog of piwi, Encodes a Cytoplasmic Protein Essential for SpermatogenesisDeng W, Lin H. miwi, a Murine Homolog of piwi, Encodes a Cytoplasmic Protein Essential for Spermatogenesis Developmental Cell 2002, 2: 819-830. PMID: 12062093, DOI: 10.1016/s1534-5807(02)00165-x.