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Curt I. Civin, MD

Philip A. Zaffere Distinguished Professor of Regenerative Medicine

Academic Title:

Professor

Primary Appointment:

Pediatrics

Secondary Appointment(s):

Physiology

Administrative Title:

Director, Center for Stem Cell Biology & Regenerative Medicine

Email:

ccivin@som.umaryland.edu

Location:

HSF II, S103D

Phone (Primary):

(410) 706-1181

Phone (Secondary):

(410) 706-1198

Download CV

Education and Training

  • Amherst College, BA, Biology/Independent Study, 1966-70 (magna cum-laude)
  • Harvard Medical School, MD, 1970-74 (cum-laude)
  • Residency in Pediatrics, Boston Children’s Hospital, 1974-76
  • Fellowships, Pediatric Hematology-Oncology & Tumor-Immunology, National Cancer Institute, National Institutes of Health, 1976-79

Biosketch

Dr. Civin is a pioneer in stem cell research and cancer research known internationally for developing a technology to isolate stem cells from other blood cells. The founding director for the University of Maryland’s Center for Stem Cell Biology & Regenerative Medicine, he has received wide recognition for his groundbreaking 1984 discovery of CD34, which has had a major impact on the field of blood research, as well as his mentoring of scientist and physician trainees who have become world leaders.

Dr. Civin’s breakthrough discovery of the CD34 lympho-hematopoietic stem cell antigen and monoclonal antibody (Civin et al., J. Immunology 1984) accelerated basic research in stem cell and leukemia biology and improved stem cell transplantation for thousands of patients. This led to multiple honors, including the 1999 National Inventor of the Year Award and the 2009 Landsteiner Award (Civin et al., Transfusion 2010). Through his laboratory research, Dr. Civin accomplished the rare feat of making discoveries that not only opened entirely new directions and continue to empower stem cell, leukemia, and transplantation research, but that are also valuable in clinical bone marrow stem cell transplantation and leukemia diagnosis.

His work led to the first successful stem cell therapies emanating from basic research, as he proved in his own patients (Civin et al., J. Clinical Oncology 1996). CD34 was the first and is still the best marker for hematopoietic stem-progenitor cells, as well as endothelial cells (Beschorner et al., Am. J. Pathology 1985). CD34 monoclonal antibodies have provided an efficient, robust technology to immunoaffinity-purify these key cells. Tens of thousands of scientific articles involve CD34 (e.g., Loken et al., Blood 1987), and thousands of patients have received CD34+ cell transplants and/or have had their mobilized peripheral blood stem cell harvests assessed for numbers of CD34+ cells.

Dr. Civin’s laboratory has over 4 decades of expertise with comprehensive cell and molecular biologic studies of normal and malignant hematopoiesis using cell lines, primary human CD34+ hematopoietic stem-progenitor cells, mouse cells, and primary human leukemia cells. His own current research focuses on the roles of key molecules (e.g., Creed et al., Development 2020), including microRNAs (e.g., Georgantas et al. PNAS, 2007) and their targets in normal and leukemic stem-progenitor cells, on targeting leukemias (e.g., Moses et al., Blood Advances 2021), and on applying new bioengineering technologies to problems in hematology and oncology (e.g., Campos-González et al., SLAS Technology 2018).

Dr. Civin and colleagues immunophenotypically identified and characterized most of the major stages and lineages of normal human blood and immune cell development, including the CD34+CD38- subset that is highly enriched in engrafting human hematopoietic stem cells (Civin et al., Blood 1996). The direct clinical impact of CD34 and other monoclonal antibodies made by his lab include many thousands of patients whose leukemias have been sub-classified using immunophenotyping panels. They also developed monoclonal antibody panels that define normal lympho-hematopoietic cell subtypes (e.g., Loken et al., Blood 1987), to determine diagnostic and prognostic subtypes of leukemia cases (e.g., Hurwitz et al., Blood 1988), and to detect minimal residual leukemia (Gore et al., Blood 1991).

Civin’s team discovered several key human stem-progenitor cell molecules, such as the human FLT3 receptor (Small et al., PNAS 1994) and the TNK1 tyrosine kinase. They were among the first to find that certain microRNAs were key normal hematopoietic regulators (e.g., Georgantas et al., PNAS 2007), and they continue to use microRNAs to identify novel target molecules and pathways involved in regulation of normal and leukemic human hematopoiesis, including miR144, miR451, RAB14 (Kim et al., British J. Haematology 2015), EYA and SIX (Creed et al., Development 2020).

Via screens of a repurposing library of 4000 clinical drugs, Dr. Civin and colleagues discovered that artemisinins, which have low/absent clinical toxicity in worldwide use as antimalarials, are active against human leukemia cell lines and primary acute leukemia patient samples in vitro and in mouse xenograft models in vivo. They identified a highly potent analog dimeric analog with prolonged in vivo half-life, artemisinin-derived trioxane diphenylphosphate 838 (ART838) (Mott et al., Bioorg. Med. Chem. 2013). Because multiagent combination regimens are necessary to cure fully evolved leukemias, they sought to identify synergies of artemisinin analogs with established and emerging low toxicity antileukemic drugs. In addition to standard acute myeloid leukemia drugs, tyrosine kinase inhibitors and B-cell lymphoma 2 (BCL2) inhibitors synergized strongly with artemisinins (Fox et al., Oncotarget 2016). Validation assays confirmed that the selective BCL2 inhibitor, venetoclax, and the broad kinase inhibitor, sorafenib, both synergized strongly with artemisinin analogs to inhibit growth and induce apoptotic cell death of multiple acute leukemia cell lines and primary patient samples in vitro. An oral 3-drug “SAV” regimen (sorafenib plus the potent ART838 analog plus venetoclax) efficiently killed leukemia cell lines and primary leukemia cells from patients in vitro but spared normal human hematopoietic progenitor cells. Leukemia cells cultured in ART838 had decreased induced myeloid leukemia cell differentiation protein (MCL1) levels and increased levels of DNA damage-inducible transcript 3 (DDIT3; GADD153) messenger RNA and its encoded CCATT/enhancer-binding protein homologous protein (CHOP), a key component of the integrated stress response. Thus, synergy of the SAV combination may involve combined targeting of MCL1 and BCL2 via discrete, tolerable mechanisms, and cellular levels of MCL1 and DDIT3/CHOP may serve as biomarkers for the mechanism of action of artemisinins and SAV. Finally, SAV treatment was tolerable and resulted in deep responses with extended survival in 2 acute myeloid leukemia cell line xenograft models, both harboring a mixed lineage leukemia gene rearrangement and an FMS-like receptor tyrosine kinase-3 internal tandem duplication, and SAV treatment also inhibited growth in 2 AML primagraft models (Moses et al., Blood Advances 2021). They are currently working to further develop patented novel artemisinin analogs for clinical trials and commercialization, and to elucidate the full molecular mechanism of the unique antileukemic activity of artemisinins (Kagan et al., Frontiers Oncol. 2023; Cancer Chemother. Pharmacol. 2023)

Colleagues at Princeton University and GPB Scientific Inc. had previously developed a deterministic lateral displacement (DLD) microfluidic method to separate cells of various sizes from blood. With NIH STTR grant support, the Civin lab collaborated with them to reduce this technology to practice via a commercially produced, high-precision plastic microfluidic chip-based device designed for automated preparation of human leukocytes for flow cytometry. After a human blood sample was incubated with fluorochrome-conjugated monoclonal antibodies, the mixture was input to a DLD microfluidic chip where it was driven through a micropost array designed to deflect leukocytes purely on the basis of size from the input flow stream into a buffer stream, thus separating leukocytes from smaller cells and particles and washing them simultaneously. They developed a microfluidic cell processing protocol that recovered ~90% of input leukocytes and removed >99.9% of input erythrocytes and >99% of unbound antibody in <20 minutes. Flow cytometric evaluation of the microchip-processed cell product revealed excellent forward and side light scattering and fluorescence characteristics of immunolabeled leukocytes.

These results indicate that cost-effective plastic DLD microchips can speed and automate leukocyte processing for high-quality flow cytometry analysis, and potentially multiple other research and diagnostic applications (Civin et al., Cytometry A 2016). Subsequently, they extended this work toward therapeutic application via a novel DLD device for processing of large-volume apheresis blood products. Supported by a second NIH STTR grant, they demonstrated efficient leukocyte recovery and erythrocyte/platelet depletion, and the recovered T lymphocytes expanded extensively in culture.

Thus, DLD leukocyte processing provides a path to develop a simple closed and automated system, and simultaneously accomplishes multiple steps that involve potential for human error, microbial contamination, and other current technical challenges associated with manufacture of therapeutic cells such as CAR T-cells. As a result of this collaborative research developing bioengineering tools for blood cell separation, Dr. Civin is an inventor on multiple patents with Princeton and GPB colleagues. Recently, the collaborative team has begun to develop DLD processing of mobilized blood apheresis samples for hematopoietic stem cell therapies, and GPB Scientific Inc. has grown and receives substantial venture capital funding (Campos-González et al., SLAS Technology 2018).

Dr. Civin holds dozens of biomedical patents and is currently a principal or collaborating investigator on multiple peer-reviewed research projects funded by the National Institutes of Health, the State of Maryland, and private foundations. Dr. Civin taught and led research and clinical pediatric oncology at Johns Hopkins University School of Medicine for 30 years before becoming founding director for the University of Maryland’s Center for Stem Cell Biology & Regenerative Medicine and Associate Dean for Research in 2009.

He has lectured around the world, published more than 250 scientific articles and many book chapters, received many awards, and served in leadership positions of multiple distinguished committees and editorial boards. Throughout his career, he has mentored a large number of talented scientists and physician-scientists to pursue field-leading academic careers in translational research.

Research/Clinical Keywords

Stem Cell Biology, Hematopoiesis, Regenerative Medicine, Oncology, Pediatric Oncology, Gene Therapy, Hematology, Cancer, Leukemia, Bone Marrow Transplantation, Hematopoietic Stem Cells, CD34

Highlighted Publications

Civin CI. CD34 stem cell stories and lessons from the CD34 wars: the Landsteiner Lecture 2009. Transfusion. 2010 Sep;50(9):2046-56. PubMed ID: 20561292; NIHMSID: NIHMS668003.

Civin CI, Trischmann T, Kadan NS, Davis J, Noga S, Cohen K, Duffy B, Groenewegen I, Wiley J, Law P, Hardwick A, Oldham F, Gee A. Highly purified CD34-positive cells reconstitute hematopoiesis. J Clin Oncol. 1996 Aug;14(8):2224-33. PubMed PMID: 8708711.

Loken MR, Shah VO, Dattilio KL, Civin CI. Flow cytometric analysis of human bone marrow. II. Normal B lymphocyte development. Blood. 1987 Nov;70(5):1316-24. PubMed PMID: 3117132.

Beschorner WE, Civin CI, Strauss LC. Localization of hematopoietic progenitor cells in tissue with the anti-My-10 monoclonal antibody. Am J Pathol. 1985 Apr;119(1):1-4. PubMed Central PMCID: PMC1888077.

Civin CI, Strauss LC, Brovall C, Fackler MJ, Schwartz JF, Shaper JH. Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J Immunol. 1984 Jul;133(1):157-65. PubMed PMID: 6586833.

Additional Publication Citations

Complete List of Published Work:
https://www.ncbi.nlm.nih.gov/myncbi/curt.civin.1/bibliography/40991787/public/

Felschow, D.M., Civin, C.I., Hoehn, G.T. Characterization of the Tyrosine Kinase Tnk1 and its Binding with Phosphalipase C-gamma1. Biochem Biophy Res Commun 273:294-301, 2000. PMID: 10873601

Civin, C.I., Gene Therapy in Clinical Applications: Overview: How Do We Translate Gene Therapy to Clinical Trials? Stem Cells 18:150-156, 2000. PMID: 10742388

Civin, C.I., Human Pluripotent Stem Cells: Science Fiction Poses No Immediate Danger. Stem Cells 18: iv-v, 2000. PMID: 11072037

Civin, C.I., Young Turks Forum – for the Young and Young at Heart. Stem Cells 18:ii, 2000.

Civin, C.I., A Challenge to Solve “Lichtman’s Riddles”. Stem Cells 18:iii, 2000. PMID: 11007927

Loeb, D.M., Bowers, D.C., Civin, C.I., Friedman, A.D. Intensive Time Sequential Remission Induction Chemotherapy with High-Dose Cytarabine for Childhood Acute Myeloid Leukemia. Med Pediatr Oncol 37:365-371, 2001. PMID: 11568900

Felschow, D.M., McVeigh, M.L., Hoehn, G.T., Civin, C.I., Fackler, M.J. The Adapter Protein CrkL Associates with CD34. Blood 97:3768-3775, 2001. PMID: 11389015

Gao, Z., Golob, J., Tanavde, V.M., Civin, C.I., Hawley, R.G., Cheng, L. High Levels of Transgene Expression Following Transduction of Long-Term NOD/SCID-Repopulating Cells with a Modified Lentiviral Vector. Stem Cells 19:247-259, 2001. PMID: 11389015

Gao, Z., Fackler, M.J., Leung, W., Lumkul, R., Ramirez, M., Theobald, N., Malech, H.L., Civin, C.I. Human CD34+ Cell Preparations Contain Over 100-fold Greater NOD/SCID Mouse Engrafting Capacity than do CD34- Cell Preparations. Exp Hematol 29:910-921, 2001. PMID: 11438214

 Tse, K.F., Novelli, E., Civin, C.I., Bohmer, F.D., Small, D. Inhibition of FLT3-Mediated Transformation by use of a Tyrosine Kinase Inhibitor. Leukemia 15:1001-1010, 2001. PMID: 11455967

 Civin, C.I. Stem Cell Research: Back to the Future. Stem Cells 19:356-357, 2001. PMID: 11553844

 Mason, D.Y., Andre, P., Bensussan, A., Buckley, Civin, C.I., C., Clark, E., De Haas, M., Goyert, S., Hadam, M., Hart, D., Horeist, V., Meuer, S., Morrissey, J., Schwartz-Albiez, R., Shaw, S., Simmons, D., Uguccioni, M., Van Der Schoot, E., Vivier, E., Zola, H. CD antigens 2001. Immunology 103:1-10, 2001. PMID: 11929596

Gorin, N.C., Piantadosi, S., Stull, M., Wingard, J.R., Civin, C.I. Increased Risk of Lethal Graft Versus Host Disease-Like Syndrome After Transplantation Into Nod/Scid Mice of Human Mobilized Peripheral Blood Stem Cells, as Compared to Bone Marrow or Cord Blood. J Hematother Stem Cell Res 11:277-292, 2002. PMID: 11983099

Kim, H.J., Whartenby, K.A., Georgantas, R.W., Wingard, J., Civin, C.I. Human CD34+ Hematopoietic Stem/Progenitor Cells Express High Levels of FLIP and are Resistant to Fas-Mediated Apoptosis. Stem Cells 20:174-182, 2002. PMID: 11897874

Yang, Y., Wang, W., Cleaves, R., Zahurak, M., Cheng, L., Civin, C.I., Friedman, A.D. Acceleration of G1 Cooperates with CBF-SMMHC to Induce Acute Leukemia in Mice. Cancer Res 62:2232-2235, 2002. PMID: 11956074

Tanavde, V.M., Malehorn, M.T., Lumkul, R., Gao, Z., Wingard, J., Garrett, E.S. Civin, C.I. Human Stem-Progenitor Cells from Neonatal Cord Blood Have Greater Hematopoietic Expansion Capacity than those from Mobilized Adult Blood. Exp Hematol 30:816-823, 2002. PMID: 12135681

Lumkul, R., Gorin, N.C., Malehorn, M.T., Hoehn, G.T., Zheng, R., Baldwin, B., Small, D., Gore, S., Smith, B.D., Meltzer, P.S., Civin, C.I. Human AML Cells in NOD/SCID Mice: Engraftment Potential and Gene Expression. Leukemia 16:1818-1826, 2002. PMID: 12200698

Bernardin, F., Yang, Y., Cleaves, R., Zahurak, M., Cheng, L., Civin, C.I., Friedman, A.D. TEL-AML1, Expressed From t(12;21) in Human Acute Lymphocytic Leukemia, Induces Acute Leukemia in Mice. Cancer Res 62:3904-3908, 2002. PMID: 12124316

Mason, D., Andre, P., Bensussan, A., Buckley, C., Civin, C.I., Clark, E., de Hass, M., Goyert, S., Hadam, M., Hart, D., Horeist, V., Meuer, S., Morrissey, J., Schwartz-Albiez, R., Shaw, S., Simmons, D., Uguccioni, M., Van Der Schoot, E., Vivier, E., Zola, H. CD Antigens 2002. Blood 99:3877-3880, 2002. PMID: 12014373

Civin, C.I., Gewirtz, A.M. Stem Cells 20th Anniversary. Stem Cells 20:1-2, 2002.

Civin, C.I. Commitment to Biomedical Research: Clearing Unnecessary Impediments to Progress. Stem Cells 20:482-484, 2002. PMID: 12456955

Whartenby, K.A., Straley, E.E., Kim, H.J., Racke, F., Tanavde, V., Gorski, K.S., Cheng, L., Pardoll, D.M., Civin, C.I. Transduction of Donor Hematopoietic Stem-Progenitor Cells with Fas Ligand Enhanced Short-Term Engraftment in a Murine Model of Allogeneic Bone Marrow Transplantation. Blood 100:3147-3154, 2002. PMID: 12384412

Roesler, J., Brenner, S., Bukovsky, A.A., Whiting-Theobald, N., Dull, T., Kelly, M., Civin, C.I., Malech, H.L. Third-generation, Self-Inactivating gp91(phox) Lentivector Corrects the Oxidase Defect in NOD/SCID Mouse-Repopulating Peripheral Blood-Mobilized CD34+ Cells from Patients with X-Linked Chronic Granulomatous Disease. Blood 100:4381-4390, 2002. PMID: 12393624

Chute, J.P., Saini, A.A., Chute, D.J., Wells, M.R., Clark, W.B., Harlan, D.M., Park, J., Stull, M.K., Civin, C.I., Davis, T.A. Ex vivo Culture with Human Brain Endothelial Cells Increases the SCID-Repopulating Capacity of Adult Human Bone Marrow. Blood 100:4433-4439, 2002. PMID: 12393435

Bernardin, F., Yang, Y., Civin, C.I., Friedman, A.D. c-Myc Overcomes Cell Cycle Inhibition by CBFbeta-SMMHC, a Myeloid Leukemia Oncoprotein. Cancer Biol. Ther. 1:492-494, 2002. PMID: 12496475

Angelopoulou, M., Novelli, E., Grove, J.E., Rinder, H.M., Civin, C.I., Cheng, L., Krause, D. Cotransplantation of Human Mesenchymal Stem Cells Enhances Human Myelopoiesis and Megakaryocytopoiesis in NOD/SCID Mice. Exp Hematol 31:413-420, 2003. PMID: 12763140

Yu X., Zhan X., D’Costa J., Tanavde V.M., Ye Z., Peng T., Malehorn M.T., Yang X., Civin C.I., Cheng L. Lentiviral Vectors with Two Independent Internal Promoters Transfer High-Level Expression of Multiple Transgenes to Human Hematopoietic Stem-Progenitor Cells. Mol Ther 7:827-838, 2003. PMID: 12788657

Civin, C.I., Gewirtz, A.M., Hawley, R.G. Stem Cells: 21 Years Old, with the Best Yet to Come. Stem Cells 21:513, 2003.

Cui Y., Kelleher E., Straley E., Fuchs E., Gorski K., Levitsky H., Borrello I., Civin C.I., Schoenberger S., Cheng L., Pardoll D.M., Whartenby K.A. Immunotherapy of Established Tumors Using Bone Marrow Transplantation With Antigen Gene--Modified Hematopoietic Stem Cells. Nat Med 9:952-958, 2003.PMID: 12778137

Dunlap S., Yu X., Cheng L., Civin C.I., Alani RM. High-Efficiency Stable Gene Transduction in Primary Human Melanocytes Using a Lentiviral Expression System. J Invest Dermatol 122:549-551, 2004. PMID: 15009744

Civin, C.I., Gewirtz, A.M., Hawley, R.G. Editors’ note for 2004. Stem Cells 22:1, 2004.

Palaganas, J., Civin, C.I. Two Steps Forward: Keeping the Momentum in Stem Cell Research. Stem Cells 22:240-241, 2004. PMID: 15153598

Civin, C.I., STEM CELLS: Some Good News. Stem Cells 22:648, 2004.

Bohana-Kashtan, O., Civin, C.I. Fas Ligand as a Tool for Immunosuppression and Generation of Immune Tolerance. Stem Cells 22:908-924, 2004. PMID: 15536183

Civin, C.I. Whither STEM CELLS? Stem Cells 22:1127, 2004.

Civin, C.I. CD34: Conception to Birth. ISCT Telegraft 11:1-2, 2004.

Matsui W, Huff C.A., Wang Q., Malehorn M.T., Barber J., Tanhehco Y., Smith B.D., Civin C.I., Jones R.J. Characterization of Clonogenic Multiple Myeloma Cells. Blood 103:2332-2336, 2004. PMID: 14630803

Georgantas R.W., Tanavde V., Malehorn M, Heimfeld S., Chen C., Carr L, Murillo F, Riggins G, Civin C.I. Microarray and Serial Analysis of Gene Expression Analyses Identify Known and Novel Transcripts Overexpressed in Hematopoietic Stem Cells. Cancer Res 64:4434-4441, 2004. PMID: 15231652

Lewis L.D., Amin S., Civin C.I., Leitman P.S. Ex Vivo Zidovudine (AZT) Treatment of CD34+ Bone Marrow Progenitors Causes Decreased Steady State Mitochondrial DNA (mtDNA) and INcreased Lactate Production. Hum Exp Toxicol 23:173-185, 2004. PMID: 15171568

Topaloglu O., Civin C.I., Bunz F. Digital HLA Allelotyping. Cancer Biol 3:899-902, 2004. PMID: 15326386

Esni F., Ghosh B., Biankin A.V., Lin J.W., Albert M.A., Yu X, MacDonald R.J., Civin C.I., Real F.X., Pack M.S., Ball D.W., Leach S.D. Notch inhibits Ptf1 function and acinar cell differentiation in developing mouse and zebrafish pancreas. Develop 131:4213-4224, 2004. PMID: 15280211

D'Costa J., Chaudhuri S., Civin C.I., Friedman A.D. CBFbeta-SMMHC slows proliferation of primary murine and human myeloid progenitors. Leukemia 19:921-929, 2005. PMID: 15815715

Zambidis, E.T., Peault B., Park T.S., Bunz F., Civin C.I. Hematopoietic Differentiation of Human Embryonic Stem Cells Progresses Through Sequential Hematoendothelial, Primitive, and Definitive Stages Resembling Human Yolk Sac Development. Blood 106:860-870, 2005. PMID: 15831705

Civin, C.I., Gewirtz, A.M., Hawley, R.G., Goodell, M.A Advancing the Fast-Paced Field of Stem Cell Research: Stem Cells Increases from 6 to 10 Issues in its 23rd Year of Publication. Stem Cells 23:1-2, 2005. PMID: 15625117

Bohana-Kashtan O., Civin C.I. Profiling Tumor Counterattack: Do Fas Ligand-Containing Microvesicles Reduce Anticancer Immunity? Clin Cancer Res 11:968-970, 2005. PMID: 15709161

Rao M.S., Civin C.I. Translational Research: Toward Better Characterization of Human Embryonic Stem Cells Lines. Stem Cells 23:1453, 2005. PMID: 16293580

Topaloglu O., Hurley P.J., Yildirim O., Civin C.I., Bunz F. Improved Methods for the Generation of Human Gene Knockout and Knockin Cell Lines. Nucleic Acids Res. 33:158, 2005. PMID: 16214806

Ravindranath Y., Chang M., Steuber C.P., Becton D., Dahl G., Civin C.I., Camitta B., Carroll A., Raimondi S.C., Weinstein H.J. Pediatric Oncology Group (POG) Studies of Acute Myeloid Leukemia (AML): a Review of Four Consecutive Childhood AML Trials Conducted Between 1981 and 2000. Leukemia 19:2101-2116, 2005. PMID: 16136167

Bala P., Georgantas R.W. 3rd, Sudhir D., Suresh M., Shanker K., Vrushabendra B.M., Civin C.I., Pandey A. TAGmapper: A Web-Based Tool for Mapping SAGE Tags. Gene 364:123-129, 2005. PMID: 16112519

Zhang L., D'Costa J., Kummalue T., Civin C.I., Friedman A.D. Identification of a Region on the Outer Surface of the CBFbeta-SMMHC Myeloid Oncoprotein Assembly Competence Domain Critical for Multimerization. Oncogene 25:7289-7296, 2006. PMID: 16767164

McNiece I., Civin C.I., Harrington J., Kellner J., Malehorn M., Turney J., Barber J., Jones R. Ex vivo expansion of mafosfamide-purged PBPC products. Cytotherapy. 8:459-64, 2006. PMID: 17050250

Civin C.I., Rao M.S. How Many Embryonic Stem Cell Lines Are Sufficient? A U.S. Perspective. Stem Cells 24:800-803, 2006. PMID: 16543487

Civin, C.I. Editorial Retraction. Stem Cells 24:804, 2006. PMID: 16582451

Civin, C.I. Troublesome Questions. Stem Cells 24:1411, 2006. PMID: 16687465

Civin, C.I. Stem Cell’s Impact Continues its Ascent. Stem Cells 24:1993-94, 2006.

Yu X., Alder J.K., Chun J.H., Friedman A.D., Heimfeld S., Cheng L., Civin C.I HES1 Inhibits Cycling of Hematopoietic Progenitor Cells Via DNA Binding. Stem Cells 24:876-888, 2006 PMID: 16513761

Wang D., D’Costa J., Civin C.I., Friedman A.D. C/EBPalpha Directs Monocytic Commitment of Primary Myeloid Progenitors. Blood 108:1223-1229, 2006. PMID: 16645168 PMCID: PMC1895870

Georgantas R.W., 3rd, Bohana-Kashtan O., Civin C.I. Ex Vivo Soluble Fas Ligand Treatment of Donor Cells to Selectively Reduce Murine Acute Graft Versus Host Disease. Transplantation 82:471-478, 2006. PMID: 16926590

Georgantas R.W., 3rd, Hildreth R., Morisot S., Alder J., Liu C.G., Heimfeld S., Calin G.A., Croce CM, Civin C.I. CD34+ Hematopoietic Stem-Progenitor Cell MicroRNA Expression and Function: a Circuit Diagram of Differentiation Control. Proc Natl Acad Sci 104:2750-2755, 2007. PMID: 17293455 PMCID: PMC1796783

Alder J.K., Georgantas R.W., Hildreth R.L., Kaplan I.M., Morisot S., Yu X., McDevitt M., Civin C.I. Kruppel-Like Factor 4 is Essential for Inflammatory Monocyte Differentiation in Vivo. J Immunol 180:5645-5652, 2008. PMID: 18390749 PMCID: PMC3074963

Yu X., Zou J., Ye Z., Hammond H., Chen G., Tokunaga A., Mali P., Li Y.M., Civin C.I., Gaiano N., Cheng L. Notch Signaling Activation in Human Embryonic Stem Cells is Required for Embryonic, but not Trophoblastic, Lineage Commitment. Cell Stem Cell 1:461-471, 2008. PMID: 18462696 PMCID: PMC2442567

Bohana-Kashtan O., Morisot S., Hildreth R., Brayton C., Levitsky H.I, Civin C.I. Selective Reduction of Graft-Versus-Host Disease-Mediating Human T Cells By Ex Vivo Treatment with Soluble Fas Ligand. J Immunol 183:696-705, 2009. PMID: 19535642 PMCID: PMC3072680

Kandavelou K., Ramalingam S., London V, Mani M., Wu J., Alexeev V., Civin C.I., Chandrasegaran S. Targeted Manipulation of Mammalian Genomes Using Designed Zinc Finger Nucleases. Biochem Biophys Res Commun 388:56-61, 2009. PMID: 19635463 PMCID: PMC2744961

Huang C.R., Schneider A.M., Lu Y., Niranjan T., Shen P., Robinson M.A., Steranka J.P., Valle D., Civin C.I., Wang T., Wheelan S.J., Ji H., Boeke J.D., Burns K.H. Mobile Interspersed Repeats are Major Structural Variants in the Human Genome. Cell 141:1171-1182, 2010. PMID: 20602999 PMCID: PMC2943426

Morisot S., Wayne, A.S., Bohana-Kashtan, O., Kaplan, I.M., Gocke, C.D., Hildreth, R., Stetler-Stevenson, M., Walker, R.L., Davis, S., Meltzer, P.S., Wheelan, S.J., Brown, P., Jones, R.J., Shultz, L.D., Civin, C.I. High Frequencies of Leukemia Stem Cells in Poor-Outcome Childhood Precursor-B Acute Lymphoblastic Leukemias. Leukemia 11:1859-1866, 2010. PMID: 20739953 PMCID: PMC3035974

Civin C.I. 2009 Landsteiner Lecture: CD34 Stem Cell Stories and Lessons from the CD34 Wars. Transfusion 50:2040-2056, 2010. PMID: 20561292

Lebson L., Gocke, A, Rosenzweig, J., Alder, J., Civin C.I., Calabresi, P.A., Whartenby, K.A. Cutting edge: The Transcription Factor Kruppel-Like Factor 4 Regulates the Differentiation of Th17 Cells Independently of RORgammat. J Immunol 12:7161-7164, 2010. PMID: 21076063 PMCID: PMC3071015

Kaplan I.M., Morisot, S., Heiser, D., Cheng, W.C., Kim, M.J., Civin C.I. Deletion of Tristetraprolin Caused Spontaneous Reactive Granulopoiesis by a Non-Cell-Autonomous Mechanism Without Disturbing Long-Term Hematopoietic Stem Cell Quiescence. J Immunol 1865:2826-2834, 2011. PMID: 21270394 PMCID: PMC3114656

Zhang H., Cui, Y., Voong, N., Sabatino, M., Stroncek, D.F., Morisot, S., Civin C.I., Wayne, A.S., Levine, B.L., Mackall, C.L. Activating Signals Dominate Inhibitory Signals in CD137L/IL-15 Activated Natural Killer Cells. J Immunother 2:187-195, 2011. PMID: 21304401 PMCID: PMC3128544

Yu D., Zhan X.H., Zhao X.F., Williams M.S., Carey G.B., Smith E., Scott D., Zhu J., Guo Y., Cherukuri S., Civin C.I., Zhan X. Mice Deficient in MIM Expression are Predisposed to Lymphomagenesis. Oncogene 30:3561-8, 2012. PMID: 22081072 PMCID: PMC3350826

Sharkis S.J., Jones R.J., Civin C.I., Jang Y.Y. Pluripotent Stem Cell-Based Cancer Therapy: Promise and Challenges. Sci Transl Med 4:127, 2012.  PMID: 22461639 PMCID: PMC3397797

Prince O.D., Langdon J.M., Layman, A., Prince I.C., Sabogal M., Mak H.H., Berger A.E, Cheadle C., Chrest F.J., Yu Q., Andrews N.C., Civin C.I., Walston J.D., Roy C.N. Late Stage Erythroid Precursor Production is Impaired in Mice with Chronic Inflammation. Haematol 11:1648-58, 2012. PMID: 22581006 PMCID: PMC3487436

Scheibner K.A., Teaboldt B., Hauer M.C., Chen X., Cherukuri S., Guo Y., Kelley S.M., Liu Z., Baer M.R., Heimfeld S., Civin C.I. MiR-27a Functions as a Tumor Suppressor in Acute Leukemia by Regulating 14-3-3theta. PLoS One  7:e50895, 2012. PMID: 23236401 PMCID: PMC3517479 

Godsey B., Heiser D., Civin C.I. Inferring MicroRNA Regulation of mRNA with Partially Ordered Samples of Paired Expression Data and Exogenous Prediction Algorithms. PLoS One 7:e51480, 2012. PMID: 23284698 PMCID: PMC3526609

Chu S.H., Heiser D., Li L., Kaplan I., Collector M., Huso D., Sharkis S.J., Civin C.I., Small D. FLT3-ITD Knockin Impairs Hematopoietic Stem Cell Quiescence/Homeostasis, Leading to Myeloproliferative Neoplasm. Cell Stem Cell 11:346-358, 2012. PMID: 22958930 PMCID: PMC3725984

Ramalingam S., London V., Kandavelou K., Cebotaru L., Guggino W., Civin C.I., Chandrasegaran S. Generation and Genetic Engineering of Human Induced Pluripotent Stem Cells Using Designed Zinc Finger Nucleases. Stem Cells Dev 22:595-610, 2013. PMID: 22931452 PMCID: PMC3565436

Farrance, I.K., Civin, C.I. Biochemistry and Signaling in Stem Cells, and Vice Versa. Biochim Biophys Acta 1830:2267, 2013. PMID: 23331875

Cheng W.C., Kingsbury T.J., Wheelan S.J., Civin C.I. A Simple High-throughput Technology Enables Gain-of-function Screening of Human microRNAs. BioTechniques 54:77-86, 2013. PMID: 23384178 PMCID: PMC3671589

Mott B.T., He R., Chen X., Fox J.M., Civin C.I., Arav-Boger R., Posner G.H. Artemisinin-Derived Dimer Phosphate Esters as Potent Anti-Cytomegalovirus (Anti-CMV) and Anti-Cancer Agents: A Structure-Activity Study. Bioorg Med Chem 21:3701-7, 2013. PMID: 23673218 PMCID: PMC3685872

Cramer-Morales K., Nieborowska-Skorska M., Scheibner K., Padget M., Irvine D., Sliwinski T., Haas K., Lee J., Roy D., Slupianek A., Waski M., Childers W., Copland M., Muschen M., Civin C.I., Skorski T. Personalized Synthetic Lethality Induced by Targeting RAD52 in Leukemias Identified by Gene Mutation and Expression Profile. Blood 122:1293-304, 2013.  PMID: 23836560 PMCID:  PMC3744994

McCranor B.J., Langdon J.M., Prince O.D., Femnou L.K., Berger A.E., Cheadle C., Civin C.I., Kim A., Rivera S., Ganz T., Vaulont S., Xue Q.L., Walston J.D., Roy C.N. Investigation of the role of interleukin-6 and hepcidin antimicrobial peptide in the development of anemia with age. Haematologica 98:1633-40, 2013. PMID: 23996485 PMCID: PMC3789470

McCranor B.J., Kim M.J., Cruz N.M., Xue Q.L., Berger A.E., Walston J.D., Civin C.I., Roy C.N.  Interleukin-6 directly impairs the erythroid development of human TF-1 erythroleukemic cells. Blood Cells Mol Dis 52:126-33, 2014. PMID: 24119518 PMCID: PMC3947197

Langdon J.M., Yates S.C., Laurette K., Femnou L.K., McCranor B.J., Qian-Li X., Vaulont S., Civin C.I., Walston J.D., Roy C.N. Hepcidin-dependent and hepcidin-independent regulation of erythropoiesis in a mouse model of anemia of chronic inflammation. Am J Hematol 89:470-9, 2014. PMID: 24415655 PMCID: PMC4200395

Heiser D., Tan Y.S., Kaplan I., Godsey B., Morisot S., Cheng W.C., Small D., Civin C.I. Correlated miR-mRNA expression signatures of mouse hematopoietic stem and progenitor cell subsets predict “stemness” and “myeloid” interaction networks. PLoS One 9:e94852, 2014. PMID: 24747944 PMCID: PMC3991639

Kim M.J., Tan Y.S., Cheng W.C., Kingsbury T.J., Heimfeld S., Civin C.I. MiR-144 and miR-451 regulate human erythropoiesis via RAB14. Br J Haematol 168:583-597, 2015. PMID: 25312678; PMCID: PMC4314389

Tan Y.S., Kim M.J., Kingsbury T.J., Civin C.I., Cheng W.C. Regulation of RAB5C is important for the growth inhibitory effects of miR-509 in human precursor-B acute lymphoblastic leukemia. PLoS One 9:e111777, 2014. PMID: 25368993 PMCID: PMC4219775

Huang T.C., Cutler J., Bharne S., Zhong J., Weinstock D., Tyner J., Gojo I., Civin C.I., Pandey A. Integrated analysis of CRLF2 signaling in acute lymphoblastic leukemia identifies Polo-Like Kinase 1 as a potential therapeutic target. Leuk Lymphoma 56:1524-7, 2015. PMID: 25213184 PMCID: PMCID: PMC4420723

Huang T.C., Renuse S., Pinto S., Kumar P., Yang Y., Cherkady R., Godsey B., Mendell J.T., Halushka M.K., Civin C.I., Marchionni L., Pandey A. Identification of miR-145 targets through an integrated omics analysis. Mol Biosyst 11:197-207, 2015. PMID: 25354783 PMCID: PMC4352311

Muvarak N., Kelley S., Robert C., Baer M.R., Perrotti D., Gambacorti-Passerini C., Civin C., Scheibner K., Rassool, F.V. c-MYC Generates Repair Errors via Increased Transcription of Alternative-NHEJ Factors, LIG3 and PARP1, in Tyrosine Kinase-Activated Leukemias. Mol Cancer Res 13:699-712, 2015. PMID: 25828893 PMCID: PMC4398615

Candia J., Cherukuri S., Guo Y., Doshi K., Banavar J.R., Civin C.I., Losert W. Uncovering low-dimensional, miR-based signatures of acute myeloid and lymphoblastic leukemias with a machine learning-driven network approach. Converg Sci Phys Oncol 1:025002, 2015. doi:10.1088/2057-1739/1/2/025002.

Furusawa A., Sadashivaiah K., Singh Z.N., Civin C.I., Banerjee A. Inefficient megakaryopoiesis in mouse hematopoietic stem-progenitor cells lacking T-bet. Exp Hematol 44:194-206, 2016. PMID: 26607595 PMCID: PMC4789076

Fox J.M., Moynihan J.R., Mott B.T., Mazzone J.R., Anders N.M., Brown P.A., Rudek M.A., Liu J.O., Arav-Boger R., Posner G.H., Civin C. I., Chen X. Artemisinin-derived dimer ART-838 potently inhibited human acute leukemias, persisted in vivo, and synergized with antileukemic drugs. Oncotarget 7:7268-7279, 2016. PMID: 26771236 PMCID: PMC4872784

Zhan T., Cao C., Li L., Gu N., Civin C.I., Zhan X. MIM regulates the trafficking of bone marrow vells via modulating surface expression of CXCR4. Leukemia 30:1327-34, 2016. PMID: 26965284 PMCID: PMC4889520

Civin C.I., Ward T., Skelley A.M., Gandhi K., Lee Z.P., Dosier C.R., D’Silva J.L., Chen Y., Kim M.J., Moynihan J., Chen X., Aurich L., Gulnik S., Brittain G.C., Recktenwald D., Austin R.H., Sturm J.C. Automated Leukocyte Processing by Microfluidic Deterministic Lateral Displacement. Cytometry A 89:1073-83, 2016. PMID: 27875619 PMCID: PMC5488292

Nieborowska-Skorska M., Sullivan K., Dasgupta Y., Podszywalow-Bartnicka P., Hoser G., Maifrede S., Martinez E., Marcantonio D.D., Bolton E., Cramer K., Lee J.W., Li S.M, Slupianek A., Gritsyuk D. Cerny-Reiterer S., Seferynska I., Stoklosa T., Bullinger L. Zhao H., Gorbunova V., Piwocka K., Valent P., Civin C., Muschen M., Dick J.E., Wang J.C.Y., Bhatia S., Bhatia R., Eppert K., Minden M.D., Sykes S., Skorski T.  Personalized Medicine-guided Synthetic Lethality Eradicates Proliferating and Quiescent Leukemia Cells. J Clin Invest 127:2392-2406, 2017. PMID: 28481221 PMCID: PMC5451241

Sasaki T., Rivera-Mulial J.C., Vera D., Zimmerman J., Das S., Padget M., Nakamichi N., Chang B.H., Tyner J., Druker B.J., Weng A.P., Civin C.I., Eaves, C.J., Gilbert, D.M. Stability of patient-specific features of altered DNA replication timing in xenografts of primary human acute lymphoblastic leukemia. Exp Hematol 51:71-82, 2017. PMID: 28433605 PMCID: PMC5491210

Campos-González R., Skelley A.M., Gandhi K., Inglis D.W., Sturm J.C., Civin C.I., Ward T. Deterministic Lateral Displacement: The Next Generation CAR T-Cell Processing? SLAS Technol 23:338-351, 2018. PMID: 29361868

Simpson H.M., Furusawa A., Sadashivaiah K., Civin C.I., Banerjee A. STAT5 inhibition induces TRAIL/DR4 dependent apoptosis in peripheral T-cell lymphoma. Oncotarget 9:16792-806, 2018. PMID: 29682185 PMCID: PMC5908286

Lembong J., Lerman M.J., Kingsbury T.J., Civin C.I., Fisher J.P. A fluidic culture platform for spatially patterned cell growth, differentiation, and cocultures. Tissue Eng Part A 24:1715-32, 2018. PMID: 29845891

Kim M.J., Civin C.I., Kingsbury T.J. MicroRNAs as regulators and effectors of hematopoietic transcription factors. WIREs RNA 10:e1537, 2019. PMID: 31007002

Creed M., Baldeosingh R., Eberly C.L., Schlee C.S., Kim M.J., Cutler J.A., Pandey A., Civin C.I., Fossett N.G., Kingsbury T.J. PAX-SIX-EYA-DACH Network modulates GATA-FOG function in fly hematopoiesis and human erythropoiesis. Development 147:dev177022, 2020. doi:10.1242/dev.177022. PMID: 31806659 PMCID: PMC6983716

Emadi A., Kapadia B., Bollino D., Bhandary B., Baer M.R., Niyongere S., Strovel E.T., Kaizer H., Chang E., Choi E.Y., Ma X., Tighe K.M., Carcer-Cooper B., Moses B.S., Civin C.I., Mahurkar A., Shetty A.C., Gartenhaus R.B., Kamangar F., Lapidus R.G. Venetoclax and pegcrisantaspase for complex karyotype acute leukemia. Leukemia 16:Doi: 10.1038/s41375-020-01080-6, 2021. PMID: 33199836 PMCID:

Moses B., McCullough S., Fox J.M., Mott B., Bentzen S., Kim M.J., Tyner J.W., Lapidus R.G., Emadi A., Rudek M., Kingsbury T., Civin C.I. Antileukemic efficacy of a potent artemisinin combined with sorafenib and venetoclax. Blood Adv 5:711-724, 2021. PMID: 33560385 PMCID: PMC7876886  

Saha P., Kim M., Tulshyan A., Guo Y., Mishra R., Li D., Civin C.I., Kaushal S., Sharma S. Hypoxia-inducible factor 1-alpha enhances the secretome to rejuvenate adult cardiosphere-derived cells. J Thorac Cardiovasc Surg, 2021; S0022-5223(21)01046-1. PMID: 34465468

Kagan A.B., Moses B.S., Mott B.T., Rai G., Anders N.M., Rudek M.A., Civin C.I. A Novel 2-Carbon-Linked Dimeric Artemisinin with Potent Antileukemic Activity and Favorable Pharmacology. Front Oncol. 2022;11:790037. Published 2022 Jan 11. DOI: 10.3389/fonc.2021.790037. PMID: 35127495 PMCID: PMC8811960

Gunasekaran M., Mishra R., Progyaparamita S., Morales D., Cheng W.C., Jayaraman A.R., Hoffman J.R., Davidson L., Chen L. Shah A.M., Bittle G., Fu X., Tulshyan A., Abdullah M., Kingsbury T., Civin C., Yang P., Davis M.E., Bolli R., Hare J.M., Sharma S., Kaushal S. Comparative efficacy and mechanism of action of cardiac progenitor cells after cardiac injury. iScience 2022;25(8):104656. Published 2022 Jun 22. DOI: 10.1016/j.isci.2022.104656. PMID: 35847554 PMCID: PMC9283895

Kagan A.B., Moses B.S., Lapidus R., Mott B.T., Rai G., Anders N.M., Hoag S.W., Rudek M.A., Civin C.I. ART714 is a best-in-class antileukemic 2-carbon-linked dimeric artemisinin derivative. Cancer Chemother Pharmacol. 2023 Jul;92(1):39-50. DOI: 10.1007/s00280-023-04539-2. Epub 2023 May 30. PMID: 37249624

Research Interests

Hematopoiesis, leukemia, cancer biology, stem cell biology, stem cell purification, stem cell transduction, stem cell gene editing

Awards and Affiliations

  • 2022: Philip A. Zaffere Distinguished Professor in Regnerative Medicine, UMSOM (Inaugural)
  • 2022: American Associationfor the Advancement of Science (AAAS) Fellow
  • 2018: Small Family Visiting Professor in Pediatric Oncology, JHU (Inaugural)
  • 2016: Hometown Health Heroes, Jewish Museum of Maryland
  • 2015: ASH Mentor Award, American Society of Hematology
  • 2013: Baltimore Jewish Hall of Fame, Gordon Jewish Community Center
  • 2011: John L. Kellerman III Memorial Lecture, Maryland Stem Cell Research Fund
  • 2009: Karl Landsteiner Memorial Award & Lectureship, American Association of Blood Banks
  • 2009: Influential Marylanders, The Daily Record
  • 2008: David G. Marsh Genetics of Asthma and Allergic Diseases Award and Lecture, Johns Hopkins University
  • 2006: Return of the Child Award, Leukemia & Lymphoma Society of America
  • 2003-2017: NFCR Fellow Award, National Foundation for Cancer Research
  • 2001: Innovator of the Year, Leukemia & Lymphoma Society of America
  • 2001: Doctor of Science (honorary), Amherst College
  • 2000 2009: Herman & Walter Samuelson Chair in Cancer Research, Johns Hopkins University
  • 1999: National Inventor of the Year Award, Intellectual Property Owners Association
  • 1999: Hope Award for extraordinary achievement, Leukemia Society of America
  • 1997: Kantor Family Prize for Cancer Research Excellence, Kantor Family
  • 1995-2011: Best Doctors Awards, US News & World Report, Baltimore Magazine, Castle Connolly, Woodward/White
  • 1993 - 2000: King Fahd Chair in Pediatric Oncology, Johns Hopkins University
  • 1992: Member, American Society of Clinical Investigation
  • 1989: Distinguished Service Award for Leukemia Research, Leukemia Society of America
  • 1986: Dr Frederick Stohlman Award, Leukemia Society of America
  • 1984-1989: Scholar Award, Leukemia Society of America
  • 1980-1983: ACS Junior Clinical Faculty Fellow, American Cancer Society
  • 1974: Soma Weiss Award, Harvard Medical School
  • 1974: Cum Laude, Harvard Medical School
  • 1970: Oscar E. Schotte Award and Scholarship in Biology, Amherst College
  • 1970: Magna cum Laude, Amherst College
  • 1970: Phi Beta Kappa, Amherst College
  • 1970: Sigma Xi, Amherst College
  • 1966: National Honor Society Scholarship, Amherst College

Previous Positions

  • Active Staff in Oncology and Pediatrics, The Johns Hopkins Hospital, Baltimore, MD, 1979-2009
  • Assistant Professor, Associate Professor, Professor, Oncology and Pediatrics, The Johns Hopkins University School of Medicine, 1979-2009
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