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James Palis

Title	Professor
Institution	School of Medicine and Dentistry
Department	Pediatrics
Address	University of Rochester Medical Center School of Medicine and Dentistry 601 Elmwood Ave, Box 703 Rochester NY 14642

Awards And Honors

1982			Second Choremion Research Award, Athens, Greece
1999			University of Rochester Postdoctoral Academic Mentoring Award
2005			George Washington Goler Associate Professor of Pediatrics
2005			George Washington Goler Professor of Pediatrics

Overview

Dr. Palis' research interests are:
1) Ontogeny of the mammalian hematopoietic system,
2) Differentiation of the erythroid lineage,
3) Erythroid precursor self-renewal, and
4) Response of the hematopoietic system to ionizing radiation

Hematopoietic stem cells responsible for the production of blood cells throughout life arise during embryogenesis. However, the mechanisms that initiate blood cell development are largely unknown. The long-term aim of Dr. Palis' laboratory is to elucidate the cellular and molecular events underlying the initiation of hematopoiesis in the mammalian embryo. The first hematopoietic cells to emerge during mammalian embryogenesis are "primitive" red cells that are necessary for survival of the fetus. Their recent studies indicate that the primitive erythroid lineage in mice as "mammalian", rather than "non-mammalian" in character. Primitive erythropoiesis will thus serve as an important model of mammalian erythroid differentiation. Hematopoiesis originates in the yolk sac of embryos and transitions to the liver of the fetus. Two waves of hematopoietic progenitors have been identified in the yolk sac prior to colonization of the liver and the lineage composition and relationships of these primitive and definitive progenitor waves are under active investigation. Their studies indicate that the onset of hematopoiesis within the yolk sac of mammals is much more complex than previously thought.

The hematopoietic system of the adult is exquisitely sensitive to xenotoxic insults. The Palis laboratory is investigating the response of the erythroid and megakaryocyte lineages to ionizing radiation. These studies will provide for the rational use of cytokines and other agents to mitigate the deleterious effects of external radiation.

An understanding of the ontogeny of mammalian hematopoiesis and its reponse to damage will ultimately produce insights into the regulation and expansion of hematopoietic stem cells. These insights will also lead to a better understanding of genetic disorders, bone marrow failure syndromes and leukemias, ultimately leading to improvements in bone marrow transplantation for the curative treatment of numerous congenital anemias, genetic diseases, and several forms of childhood and adult cancers.

Selected Publications

Greenfest-Allen E, Malik J, Palis J, Stoeckert CJ. Stat and interferon genes identified by network analysis differentially regulate primitive and definitive erythropoiesis. BMC Syst Biol. 2013; 7:38.

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Chen C, Garcia-Santos D, Ishikawa Y, Seguin A, Li L, Fegan KH, Hildick-Smith GJ, Shah DI, Cooney JD, Chen W, King MJ, Yien YY, Schultz IJ, Anderson H, Dalton AJ, Freedman ML, Kingsley PD, Palis J, Hattangadi SM, Lodish HF, Ward DM, Kaplan J, Maeda T, Ponka P, Paw BH. Snx3 regulates recycling of the transferrin receptor and iron assimilation. Cell Metab. 2013 Mar 5; 17(3):343-52.

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Shah RR, Koniski A, Shinde M, Blythe SA, Fass DM, Haggarty SJ, Palis J, Klein PS. Regulation of primitive hematopoiesis by class I histone deacetylases. Dev Dyn. 2013 Feb; 242(2):108-21.

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Kingsley PD, Greenfest-Allen E, Frame JM, Bushnell TP, Malik J, McGrath KE, Stoeckert CJ, Palis J. Ontogeny of erythroid gene expression. Blood. 2013 Feb 7; 121(6):e5-e13.

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Waugh RE, Huang YS, Arif BJ, Bauserman R, Palis J. Development of membrane mechanical function during terminal stages of primitive erythropoiesis in mice. Exp Hematol. 2013 Apr; 41(4):398-408.e2.

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Peslak SA, Wenger J, Bemis JC, Kingsley PD, Koniski AD, McGrath KE, Palis J. EPO-mediated expansion of late-stage erythroid progenitors in the bone marrow initiates recovery from sublethal radiation stress. Blood. 2012 Sep 20; 120(12):2501-11.

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Sturgeon CM, Chicha L, Ditadi A, Zhou Q, McGrath KE, Palis J, Hammond SM, Wang S, Olson EN, Keller G. Primitive Erythropoiesis Is Regulated by miR-126 via Nonhematopoietic Vcam-1(+) Cells. Dev Cell. 2012 Jul 17; 23(1):45-57.

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Palis J. Losing a "nucleus" to gain a cytoplasm. Blood. 2012 Jun 21; 119(25):5948-9.

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McGrath KE, Frame JM, Fromm GJ, Koniski AD, Kingsley PD, Little J, Bulger M, Palis J. A transient definitive erythroid lineage with unique regulation of the ß-globin locus in the mammalian embryo. Blood. 2011 Apr 28; 117(17):4600-8.

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Peslak SA, Wenger J, Bemis JC, Kingsley PD, Frame JM, Koniski AD, Chen Y, Williams JP, McGrath KE, Dertinger SD, Palis J. Sublethal radiation injury uncovers a functional transition during erythroid maturation. Exp Hematol. 2011 Apr; 39(4):434-45.

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England SJ, McGrath KE, Frame JM, Palis J. Immature erythroblasts with extensive ex vivo self-renewal capacity emerge from the early mammalian fetus. Blood. 2011 Mar 3; 117(9):2708-17.

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de Jong JL, Davidson AJ, Wang Y, Palis J, Opara P, Pugach E, Daley GQ, Zon LI. Interaction of retinoic acid and scl controls primitive blood development. Blood. 2010 Jul 15; 116(2):201-9.

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Dertinger SD, Phonethepswath S, Franklin D, Weller P, Torous DK, Bryce SM, Avlasevich S, Bemis JC, Hyrien O, Palis J, MacGregor JT. Integration of mutation and chromosomal damage endpoints into 28-day repeat dose toxicology studies. Toxicol Sci. 2010 Jun; 115(2):401-11.

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Palis J, Malik J, McGrath KE, Kingsley PD. Primitive erythropoiesis in the mammalian embryo. Int J Dev Biol. 2010; 54(6-7):1011-8.

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Krance SM, Keng PC, Palis J, Ballatori N. Transient glutathione depletion determines terminal differentiation in HL-60 cells. Oxid Med Cell Longev. 2010 Jan-Feb; 3(1):53-60.

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Phonethepswath S, Franklin D, Torous DK, Bryce SM, Bemis JC, Raja S, Avlasevich S, Weller P, Hyrien O, Palis J, Macgregor JT, Dertinger SD. Pig-a mutation: kinetics in rat erythrocytes following exposure to five prototypical mutagens. Toxicol Sci. 2010 Mar; 114(1):59-70.

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Fromm G, de Vries C, Byron R, Fields J, Fiering S, Groudine M, Bender MA, Palis J, Bulger M. Histone hyperacetylation within the beta-globin locus is context-dependent and precedes high-level gene expression. Blood. 2009 Oct 15; 114(16):3479-88.

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Bernard JJ, Seweryniak KE, Koniski AD, Spinelli SL, Blumberg N, Francis CW, Taubman MB, Palis J, Phipps RP. Foxp3 regulates megakaryopoiesis and platelet function. Arterioscler Thromb Vasc Biol. 2009 Nov; 29(11):1874-82.

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Nilsson R, Schultz IJ, Pierce EL, Soltis KA, Naranuntarat A, Ward DM, Baughman JM, Paradkar PN, Kingsley PD, Culotta VC, Kaplan J, Palis J, Paw BH, Mootha VK. Discovery of genes essential for heme biosynthesis through large-scale gene expression analysis. Cell Metab. 2009 Aug; 10(2):119-30.

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Dertinger SD, Bemis JC, Phonethepswath S, Tsai Y, Nowak I, Hyrien O, Palis J, Chen Y. Reticulocyte and micronucleated reticulocyte responses to gamma irradiation: effect of age. Mutat Res. 2009 Apr 30; 675(1-2):77-80.

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O'Brien JJ, Spinelli SL, Tober J, Blumberg N, Francis CW, Taubman MB, Palis J, Seweryniak KE, Gertz JM, Phipps RP. 15-deoxy-delta12,14-PGJ2 enhances platelet production from megakaryocytes. Blood. 2008 Nov 15; 112(10):4051-60.

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McGrath KE, Bushnell TP, Palis J. Multispectral imaging of hematopoietic cells: where flow meets morphology. J Immunol Methods. 2008 Jul 31; 336(2):91-7.

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Palis J. Ontogeny of erythropoiesis. Curr Opin Hematol. 2008 May; 15(3):155-61.

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Keel SB, Doty RT, Yang Z, Quigley JG, Chen J, Knoblaugh S, Kingsley PD, De Domenico I, Vaughn MB, Kaplan J, Palis J, Abkowitz JL. A heme export protein is required for red blood cell differentiation and iron homeostasis. Science. 2008 Feb 8; 319(5864):825-8.

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Tober J, McGrath KE, Palis J. Primitive erythropoiesis and megakaryopoiesis in the yolk sac are independent of c-myb. Blood. 2008 Mar 1; 111(5):2636-9.

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McGrath K, Palis J. Ontogeny of erythropoiesis in the mammalian embryo. Curr Top Dev Biol. 2008; 82:1-22.

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McGrath KE, Kingsley PD, Koniski AD, Porter RL, Bushnell TP, Palis J. Enucleation of primitive erythroid cells generates a transient population of "pyrenocytes" in the mammalian fetus. Blood. 2008 Feb 15; 111(4):2409-17.

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Lux CT, Yoshimoto M, McGrath K, Conway SJ, Palis J, Yoder MC. All primitive and definitive hematopoietic progenitor cells emerging before E10 in the mouse embryo are products of the yolk sac. Blood. 2008 Apr 1; 111(7):3435-8.

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Dertinger SD, Tsai Y, Nowak I, Hyrien O, Sun H, Bemis JC, Torous DK, Keng P, Palis J, Chen Y. Reticulocyte and micronucleated reticulocyte responses to gamma irradiation: dose-response and time-course profiles measured by flow cytometry. Mutat Res. 2007 Dec 1; 634(1-2):119-25.

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Tober J, Koniski A, McGrath KE, Vemishetti R, Emerson R, de Mesy-Bentley KK, Waugh R, Palis J. The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis. Blood. 2007 Feb 15; 109(4):1433-41.

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Yi Z, Cohen-Barak O, Hagiwara N, Kingsley PD, Fuchs DA, Erickson DT, Epner EM, Palis J, Brilliant MH. Sox6 directly silences epsilon globin expression in definitive erythropoiesis. PLoS Genet. 2006 Feb; 2(2):e14.

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Kingsley PD, Malik J, Emerson RL, Bushnell TP, McGrath KE, Bloedorn LA, Bulger M, Palis J. "Maturational" globin switching in primary primitive erythroid cells. Blood. 2006 Feb 15; 107(4):1665-72.

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McGrath KE, Palis J. Hematopoiesis in the yolk sac: more than meets the eye. Exp Hematol. 2005 Sep; 33(9):1021-8.

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Wingert RA, Galloway JL, Barut B, Foott H, Fraenkel P, Axe JL, Weber GJ, Dooley K, Davidson AJ, Schmid B, Schmidt B, Paw BH, Shaw GC, Kingsley P, Palis J, Schubert H, Chen O, Kaplan J, Zon LI. Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis. Nature. 2005 Aug 18; 436(7053):1035-39.

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Palis J, Koniski A. Analysis of hematopoietic progenitors in the mouse embryo. Methods Mol Med. 2005; 105:289-302.

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Palis J. Developmental biology: no red cell is an island. Nature. 2004 Dec 23; 432(7020):964-5.

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Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature. 2004 Dec 2; 432(7017):625-30.

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Ransom DG, Bahary N, Niss K, Traver D, Burns C, Trede NS, Paffett-Lugassy N, Saganic WJ, Lim CA, Hersey C, Zhou Y, Barut BA, Lin S, Kingsley PD, Palis J, Orkin SH, Zon LI. The zebrafish moonshine gene encodes transcriptional intermediary factor 1gamma, an essential regulator of hematopoiesis. PLoS Biol. 2004 Aug; 2(8):E237.

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Kingsley PD, Malik J, Fantauzzo KA, Palis J. Yolk sac-derived primitive erythroblasts enucleate during mammalian embryogenesis. Blood. 2004 Jul 1; 104(1):19-25.

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Davidson AJ, Ernst P, Wang Y, Dekens MP, Kingsley PD, Palis J, Korsmeyer SJ, Daley GQ, Zon LI. cdx4 mutants fail to specify blood progenitors and can be rescued by multiple hox genes. Nature. 2003 Sep 18; 425(6955):300-6.

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Ji RP, Phoon CK, Aristizábal O, McGrath KE, Palis J, Turnbull DH. Onset of cardiac function during early mouse embryogenesis coincides with entry of primitive erythroblasts into the embryo proper. Circ Res. 2003 Feb 7; 92(2):133-5.

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Chung YS, Zhang WJ, Arentson E, Kingsley PD, Palis J, Choi K. Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development. 2002 Dec; 129(23):5511-20.

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McGrath KE, Koniski AD, Malik J, Palis J. Circulation is established in a stepwise pattern in the mammalian embryo. Blood. 2003 Mar 1; 101(5):1669-76.

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Lacaud G, Gore L, Kennedy M, Kouskoff V, Kingsley P, Hogan C, Carlsson L, Speck N, Palis J, Keller G. Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro. Blood. 2002 Jul 15; 100(2):458-66.

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Lewis WB, Patel U, Roberts JK, Palis J, Teot L. Angiocentric T-cell lymphoma of the temporal bone. Otolaryngol Head Neck Surg. 2002 Jan; 126(1):85-6.

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Palis J, Yoder MC. Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol. 2001 Aug; 29(8):927-36.

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Keith Ho HC, McGrath KE, Brodbeck KC, Palis J, Schick BP. Serglycin proteoglycan synthesis in the murine uterine decidua and early embryo. Biol Reprod. 2001 Jun; 64(6):1667-76.

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Lacaud G, Robertson S, Palis J, Kennedy M, Keller G. Regulation of hemangioblast development. Ann N Y Acad Sci. 2001 Jun; 938:96-107; discussion 108.

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Palis J, Chan RJ, Koniski A, Patel R, Starr M, Yoder MC. Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis. Proc Natl Acad Sci U S A. 2001 Apr 10; 98(8):4528-33.

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Kingsley PD, McGrath KE, Maltby KM, Koniski AD, Ramchandran R, Palis J. Subtractive hybridization reveals tissue-specific expression of ahnak during embryonic development. Dev Growth Differ. 2001 Apr; 43(2):133-43.

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Borrello MA, Palis J, Phipps RP. The relationship of CD5+ B lymphocytes to macrophages: insights from normal biphenotypic B/macrophage cells. Int Rev Immunol. 2001 Feb; 20(1):137-55.

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Korones DN, Brown MR, Palis J. "Liver function tests" are not always tests of liver function. Am J Hematol. 2001 Jan; 66(1):46-8.

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Donovan A, Brownlie A, Zhou Y, Shepard J, Pratt SJ, Moynihan J, Paw BH, Drejer A, Barut B, Zapata A, Law TC, Brugnara C, Lux SE, Pinkus GS, Pinkus JL, Kingsley PD, Palis J, Fleming MD, Andrews NC, Zon LI. Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature. 2000 Feb 17; 403(6771):776-81.

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Phipps RP, Pollock SJ, Kaur K, Kaufman J, Borrello MA, Graf BA, Nazarenko D, Roberts LJ, Morrow JD, Palis J, Ryan DJ, Bennett JM. Expression of cyclooxygenase-2 and prostaglandins by B-1 cells and B-CLL cells. Curr Top Microbiol Immunol. 2000; 252:293-300.

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Palis J, Robertson S, Kennedy M, Wall C, Keller G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development. 1999 Nov; 126(22):5073-84.

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Graf BA, Nazarenko DA, Borrello MA, Roberts LJ, Morrow JD, Palis J, Phipps RP. Biphenotypic B/macrophage cells express COX-1 and up-regulate COX-2 expression and prostaglandin E(2) production in response to pro-inflammatory signals. Eur J Immunol. 1999 Nov; 29(11):3793-803.

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McGrath KE, Koniski AD, Maltby KM, McGann JK, Palis J. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol. 1999 Sep 15; 213(2):442-56.

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Liu LQ, Ilaria R, Kingsley PD, Iwama A, van Etten RA, Palis J, Zhang DE. A novel ubiquitin-specific protease, UBP43, cloned from leukemia fusion protein AML1-ETO-expressing mice, functions in hematopoietic cell differentiation. Mol Cell Biol. 1999 Apr; 19(4):3029-38.

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Hetherington CJ, Kingsley PD, Crocicchio F, Zhang P, Rabin MS, Palis J, Zhang DE. Characterization of human endotoxin lipopolysaccharide receptor CD14 expression in transgenic mice. J Immunol. 1999 Jan 1; 162(1):503-9.

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Palis J, Segel GB. Developmental biology of erythropoiesis. Blood Rev. 1998 Jun; 12(2):106-14.

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Kingsley PD, Whitin JC, Cohen HJ, Palis J. Developmental expression of extracellular glutathione peroxidase suggests antioxidant roles in deciduum, visceral yolk sac, and skin. Mol Reprod Dev. 1998 Apr; 49(4):343-55.

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McGann JK, Silver L, Liesveld J, Palis J. Erythropoietin-receptor expression and function during the initiation of murine yolk sac erythropoiesis. Exp Hematol. 1997 Oct; 25(11):1149-57.

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McGrath KE, Palis J. Expression of homeobox genes, including an insulin promoting factor, in the murine yolk sac at the time of hematopoietic initiation. Mol Reprod Dev. 1997 Oct; 48(2):145-53.

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Silver L, Palis J. Initiation of murine embryonic erythropoiesis: a spatial analysis. Blood. 1997 Feb 15; 89(4):1154-64.

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Palis J, Kingsley PD. Differential gene expression during early murine yolk sac development. Mol Reprod Dev. 1995 Sep; 42(1):19-27.

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Palis J, McGrath KE, Kingsley PD. Initiation of hematopoiesis and vasculogenesis in murine yolk sac explants. Blood. 1995 Jul 1; 86(1):156-63.

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Kingsley PD, Palis J. GRP2 proteins contain both CCHC zinc fingers and a cold shock domain. Plant Cell. 1994 Nov; 6(11):1522-3.

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Kramer K, Hicks DG, Palis J, Rosier RN, Oppenheimer J, Fallon MD, Cohen HJ. Epithelioid osteosarcoma of bone. Immunocytochemical evidence suggesting divergent epithelial and mesenchymal differentiation in a primary osseous neoplasm. Cancer. 1993 May 15; 71(10):2977-82.

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Pendola F, Palis J. MacConkey-II lactose agar for screening recombinant plasmids. Trends Genet. 1993 Jan; 9(1):4.

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Reynolds SD, Angerer LM, Palis J, Nasir A, Angerer RC. Early mRNAs, spatially restricted along the animal-vegetal axis of sea urchin embryos, include one encoding a protein related to tolloid and BMP-1. Development. 1992 Mar; 114(3):769-86.

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Palis J, King B, Keng P. Separation of spontaneously differentiating and cell cycle-specific populations of HL-60 cells. Leuk Res. 1988; 12(4):339-44.

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Dacou-Voutetakis C, Palis J, Haidas S, Zannos-Mariolea L, Georgiopoulou P, Matsaniotis N. Abnormal glucose tolerance in children with acute leukemia. Effect of induction chemotherapy including L-asparaginase. Am J Pediatr Hematol Oncol. 1983; 5(2):139-46.

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