Publications
2023
Voskoboynik A. Stem cell-mediated development, regeneration, chimerism, and aging in the colonial chordate Botryllus schlosseri. Genesis. 2023. PMID: 37888861
Anselmi C, Caicci F, Bocci T, Guidetti M, Priori A, Giusti V, Levy T, Raveh T, Voskoboynik A, Weissman IL, Manni L. Multiple Forms of Neural Cell Death in the Cyclical Brain Degeneration of A Colonial Chordate. Cells 2023 Mar 29;12(7):1041. doi: 10.3390/cells12071041.
2022
Gordon T, Zaquin T, Kowarsky MA, Voskoboynik Y, Hendin N, Wurtzel O, Caicci F, Manni L†, Voskoboynik A†, Shenkar N†. Stemness activity underlying whole brain regeneration in a basal chordate. Cells 2022 Nov 22;11(23):3727. doi: 10.3390/cells11233727.PMID: 36496987
Anselmi C, Kowarsky M, Gasoarini F, Caicci F, Ishizuka KJ, Palmeri KJ, Raveh T, Sinha R, Neff NF, Quake SR, Weissman IL, Voskoboynik A, Manni L. Two distinct evolutionary conserved neural degeneration pathways characterized in a colonial chordate. Proc Natl Acad Sci U S A. 2022 July 11; 119(29): e2203032119.
Stanford News
Vanni V, Anselmi C, Ballarin L, Drago L, Gasparini F, Gordon T, Peronato A, Rosental B, Rosner A, Rinkevich B, Spagnuolo A, Manni L, Voskoboynik A. Current knowledge on stem cell in ascidian development and regeneration. In: Rinkevich B., and Ballarin L editors. Advances in aquatic invertebrate stem cells research-from basic research to innovative applications. MDPI, Basel, Switzerland, 2022.
Stuart H, Thompson SH, Anselmi C, Ishizuka KJ, Palmeri KJ, Voskoboynik A. Contributions from both the brain and the vascular network guide behavior in the colonial tunicate Botryllus schlosseri. J Exp Biol 2022 PMID:36314197
2021
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Kowarsky M, Anselmi C, Hotta K, Burighel P, Zaniolo G, Caicci F, Rosental B, Neff NF, Ishizuka KJ, Palmeri KJ, Okamoto J, Gordon T, Weissman IL, Quake SR, Manni L, Voskoboynik A. Sexual and asexual development: Two distinct programs producing the same tunicate. Cell Rep. 2021 Jan 26; 34(4): 108681. PMCID: PMC7949349.
Stanford News
https://med.stanford.edu/stemcell/news/iscbrmarticles/botryllusatlas.html
Ballarin L, Karahan A, Salvetti A, Rossi L, Manni L, Rinkevich B, Rosner A, Voskoboynik A, Rosental B, Canesi L, Anselmi C, Pinsino A, Tohumcu BE, Jemec Kokalj A, Dolar A, Novak S, Sugni M, Corsi I, Drobne D. Stem cells and innate immunity in aquatic invertebrates: bridging two seemingly disparate disciplines for new discoveries in biology. Front Immunol. 2021 Jun 30; 12: 688106. PMCID: PMC8278520.
Goldstein O, Mandujano-Tinoco EA, Levy T, Talice S, Raveh T, Gershoni-Yahalom O, Voskoboynik A, Rosental B. Botryllus schlosseri as a unique colonial chordate model for the study and modulation of innate immune activity. Mar Drugs. 2021 Aug 9; 19(8): 10.3390/md19080454. PMCID: PMC8398012.
Gordon T, Zaquin T, Kowarsky MA, Voskoboynik Y, Hendin N, Wurtzel O, Caicci F, Manni L, Voskoboynik A, Shenkar N. Stemness activity underlying whole brain regeneration in a basal chordate BioRxiv 2021 doi: https://doi.org/10.1101/2021.10.24.465595
2020
Rosental B, Raveh T, Voskoboynik A, Weissman IL. Evolutionary perspective on the hematopoietic system through a colonial chordate: Allogeneic immunity and hematopoiesis. Curr Opin Immunol. 2020 Feb; 62: 91-98. PMCID: PMC7136747.
Voskoboynik Y*, Glina A*, Kowarsky MA*, Anselmi C, Neff NF, Ishizuka KJ, Palmeri KJ, Rosental B, Gordon T, Quake SR, Weissman IL, Ben-Shlomo R, Sahoo D†, Voskoboynik A†. Global age-specific patterns of cyclic gene expression revealed by tunicate transcriptome atlas. BioRxiv 2020 doi: https://doi.org/10.1101/2020.12.08.417055
2019
Manni L, Anselmi C, Cima F, Gasparini F, Voskoboynik A, Martini M, Peronato A, Burighel P, Zaniolo G, Ballarin L. Sixty years of experimental studies on the blastogenesis of the colonial tunicate botryllus schlosseri. Dev Biol. 2019 Apr 15; 448(2): 293-308.
2018
Rosental B, Kowarsky M, Seita J, Corey DM, Ishizuka KJ, Palmeri KJ, Chen SY, Sinha R, Okamoto J, Mantalas G, Manni L, Raveh T, Clarke DN, Tsai JM, Newman AM, Neff NF, Nolan GP, Quake SR, Weissman IL, Voskoboynik A. Complex mammalian-like haematopoietic system found in a colonial chordate. Nature. 2018 Dec; 564(7736): 425-429. PMCID: PMC6347970.
Stanford News
Voskoboynik A, Newman AM, Kowarsky M, Weissman IL. Advances in Comparative Immunology. Cooper EL, editor. USA: Springer-Nature; 2018. Urochordate Botryllus: Natural Chimerism and Tolerance Induction in a Colonial Chordate
2016
Corey DM, Rosental B, Kowarsky M, Sinha R, Ishizuka KJ, Palmeri KJ, Quake SR, Voskoboynik A, Weissman IL. Developmental cell death programs license cytotoxic cells to eliminate histocompatible partners. Proc Natl Acad Sci U S A. 2016 Jun 7; 113(23): 6520-6525. PMCID: PMC4988592.
Gasparini F, Skobo T, Benato F, Gioacchini G, Voskoboynik A, Carnevali O, Manni L, Dalla Valle L. Characterization of Ambra1 in asexual cycle of a non-vertebrate chordate, the colonial tunicate botryllus schlosseri, and phylogenetic analysis of the protein group in bilateria. Mol Phylogenet Evol. 2016 Feb; 95: 46-57.
2015
Stolfi A, Sasakura Y, Chalopin D, Satou Y, Christiaen L, Dantec C, Endo T, Naville M, Nishida H, Swalla BJ, Volff JN, Voskoboynik A, Dauga D, Lemaire P. Guidelines for the nomenclature of genetic elements in tunicate genomes. Genesis. 2015 Jan; 53(1): 1-14. PMCID: PMC4308547.
Voskoboynik A, Weissman IL. Botryllus schlosseri, an emerging model for the study of aging, stem cells, and mechanisms of regeneration. Invertebr Reprod Dev. 2015 Jan 30; 59(sup1): 33-38. PMCID: PMC4464096.
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Weissman IL. Stem cells are units of natural selection for tissue formation, for germline development, and in cancer development. Proc Natl Acad Sci U S A. 2015 Jul 21; 112(29): 8922-8928. PMCID: PMC4517284.
2014
Griggio F, Voskoboynik A, Iannelli F, Justy F, Tilak MK, Turon X, Pesole G, Douzery EJ, Mastrototaro F, Gissi C. Ascidian mitogenomics: Comparison of evolutionary rates in closely related taxa provides evidence of ongoing speciation events. Genome Biol Evol. 2014 Mar; 6(3): 591-605. PMCID: PMC3971592.
Manni L, Gasparini F, Hotta K, Ishizuka KJ, Ricci L, Tiozzo S, Voskoboynik A, Dauga D. Ontology for the asexual development and anatomy of the colonial chordate botryllus schlosseri. PLoS One. 2014 May 1; 9(5): e96434. PMCID: PMC4006837.
2013
Rinkevich Y, Voskoboynik A, Rosner A, Rabinowitz C, Paz G, Oren M, Douek J, Alfassi G, Moiseeva E, Ishizuka KJ, Palmeri KJ, Weissman IL, Rinkevich B. Repeated, long-term cycling of putative stem cells between niches in a basal chordate. Dev Cell. 2013 Jan 14; 24(1): 76-88. PMCID: PMC3810298.
- Preview: Zhou Y, Lewallen M and Xie T, Stem Cells’ Exodus: A Journey to Immortality. Dev Cell. 2013 24 (1): 113-114
Voskoboynik A, Neff NF, Sahoo D, Newman AM, Pushkarev D, Koh W, Passarelli B, Fan HC, Mantalas GL, Palmeri KJ, Ishizuka KJ, Gissi C, Griggio F, Ben-Shlomo R, Corey DM, Penland L, White RA,3rd, Weissman IL, Quake SR. The genome sequence of the colonial chordate, botryllus schlosseri. Elife. 2013 Jul 2; 2: e00569. PMCID: PMC3699833.
- Research highlight: Goodwin S, McPherson JD, McCombie Rw. Coming of age: ten years of next-generation sequencing technologies. Nature Reviews 2016 17: 333-351
Stanford news
news.stanford.edu/pr/2013/pr-tunicate-genome-sequence-081413.html
Voskoboynik A, Newman AM, Corey DM, Sahoo D, Pushkarev D, Neff NF, Passarelli B, Koh W, Ishizuka KJ, Palmeri KJ, Dimov IK, Keasar C, Fan HC, Mantalas GL, Sinha R, Penland L, Quake SR, Weissman IL. Identification of a colonial chordate histocompatibility gene. Science. Jul 26; 341(6144): 384-387. PMCID: PMC3810301.
- Editors’ choice: KL Mueller, A gene for early acceptance 2013 Sci Signal, 6:ec179
Stanford News
2009
Voskoboynik A, Rinkevich B, Weissman IL. Stem cells, Chimerism and Tolerance: Lessons from Mammals and Ascidians (review; 30 pages). In: Rinkevich B., and Matranga V. editors. Stem Cells in Marine Organisms. Springer. 2009.
2008
Tiozzo S, Voskoboynik A, Brown FD, De Tomaso AW. A conserved role of the VEGF pathway in angiogenesis of an ectodermally-derived vasculature. Dev Biol. 2008 Mar 1; 315(1): 243-255. PMCID: PMC2292797
Voskoboynik A, Soen Y, Rinkevich Y, Rosner A, Ueno H, Reshef R, Ishizuka KJ, Palmeri KJ, Moiseeva E, Rinkevich B, Weissman IL. Identification of the endostyle as a stem cell niche in a colonial chordate. Cell Stem Cell. 2008 Oct 9; 3(4): 456-464. PMCID: PMC4126901.
- Editors’ notes: Challenging homeostasis with age, stress, and regeneration Cell Stem Cell, 2008 Oct 9; 3
Stanford news
https://news.stanford.edu/news/2008/october15/med-squirt-101508.html
2007
Rosner A, Rabinowitz C, Moiseeva E, Voskoboynik A, Rinkevich B. BS-cadherin in the colonial urochordate botryllus schlosseri: One protein, many functions. Dev Biol. 2007 Apr 15; 304(2): 687-700.
Voskoboynik A, Simon-Blecher N, Soen Y, Rinkevich B, De Tomaso AW, Ishizuka KJ, Weissman IL. Striving for normality: Whole body regeneration through a series of abnormal generations. FASEB J. 2007 May; 21(7): 1335-1344.
2006
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Nyholm SV, Passegue E, Ludington WB, Voskoboynik A, Mitchel K, Weissman IL, De Tomaso AW. Fester, A candidate allorecognition receptor from a primitive chordate. Immunity. 2006 Jul; 25(1): 163-173.
2005
De Tomaso AW, Nyholm SV, Palmeri KJ, Ishizuka KJ, Ludington WB, Mitchel K, Weissman IL. Isolation and characterization of a protochordate histocompatibility locus. Nature. 2005 Nov 24; 438(7067): 454-459. PMCID: PMC1401502.
Laird DJ, Chang WT, Weissman IL, Lauzon RJ. Identification of a novel gene involved in asexual organogenesis in the budding ascidian botryllus schlosseri. Dev Dyn. 2005 Dec; 234(4): 997-1005. PMCID: PMC2821222.
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Laird DJ, De Tomaso AW, Weissman IL. Stem cells are units of natural selection in a colonial ascidian. Cell. 2005 Dec 29; 123(7): 1351-1360.
2004
De Tomaso AW, Weissman IL. Evolution of a protochordate allorecognition locus. Science. 2004 Feb 13; 303(5660): 977.
Laird DJ, Weissman IL. Telomerase maintained in self-renewing tissues during serial regeneration of the urochordate botryllus schlosseri. Dev Biol. 2004 Sep 15; 273(2): 185-194.
Laird DJ, Weissman IL. Continuous development precludes radioprotection in a colonial ascidian. Dev Comp Immunol. 2004 Mar; 28(3): 201-209.
Voskoboynik A, Rinkevich B, Weiss A, Moiseeva E, Reznick AZ. Macrophage involvement for successful degeneration of apoptotic organs in the colonial urochordate botryllus schlosseri. J Exp Biol. 2004 Jun; 207(Pt 14): 2409-2416.
2003
Bartl S, Baish M, Weissman IL, Diaz M. Did the molecules of adaptive immunity evolve from the innate immune system? Integr Comp Biol. 2003 Apr; 43(2): 338-346.
Chadwick-Furman NE, Weissman IL. Effects of allogeneic contact on life-history traits of the colonial ascidian botryllus schlosseri in Monterey Bay. Biol Bull. 2003 Oct; 205(2): 133-143.
De Tomaso AW, Weissman IL. Initial characterization of a protochordate histocompatibility locus. Immunogenetics. 2003 Oct; 55(7): 480-490.
De Tomaso AW, Weissman IL. Construction and characterization of large-insert genomic libraries (BAC and fosmid) from the ascidian botryllus schlosseri and initial physical mapping of a histocompatibility locus. Mar Biotechnol (NY). 2003 Mar-Apr; 5(2): 103-115.
2002
Lauzon RJ, Ishizuka KJ, Weissman IL. Cyclical generation and degeneration of organs in a colonial urochordate involves crosstalk between old and new: A model for development and regeneration. Dev Biol. 2002 Sep 15; 249(2): 333-348.
Stoner DS, Ben-Shlomo R, Rinkevich B, Weissman IL. Genetic variability of Botryllus schlosseri invasions to the east and west coasts of the USA. Marine Ecology Progress Series, 2002: p. 93-100.
Voskoboynik A, Reznick AZ, Rinkevich B. Rejuvenescence and extension of an urochordate life span following a single, acute administration of an anti-oxidant, butylated hydroxytoluene. Mech Ageing Dev. 2002 May; 123(9): 1203-1210.
Weissman IL. The road ended up at stem cells. Immunol Rev. 2002 Jul; 185: 159-174.
2000
Laird DJ, De Tomaso AW, Cooper MD, Weissman IL. 50 million years of chordate evolution: Seeking the origins of adaptive immunity. Proc Natl Acad Sci U S A. 2000 Jun 20; 97(13): 6924-6926. PMCID: PMC34360.
Lauzon RJ, Rinkevich B, Patton CW, Weissman IL. A morphological study of nonrandom senescence in a colonial urochordate. Biol Bull. 2000 Jun; 198(3): 367-378.
Weissman IL. Stem cells: Units of development, units of regeneration, and units in evolution. Cell. 2000 Jan 7; 100(1): 157-168.
1999
Magor BG, De Tomaso A, Rinkevich B, Weissman IL. Allorecognition in colonial tunicates: Protection against predatory cell lineages? Immunol Rev. 1999 Feb; 167: 69-79.
Stoner DS, Rinkevich B, Weissman IL. Heritable germ and somatic cell lineage competitions in chimeric colonial protochordates. Proc Natl Acad Sci U S A. 1999 Aug 3; 96(16): 9148-9153. PMCID: PMC17747.
1998
Cohen CS, Saito Y, Weissman IL. Evolution of allorecognition in botryllid ascidians inferred from a molecular phylogeny. Evolution. 1998 Jun; 52(3): 746-756.
De Tomaso AW, Saito Y, Ishizuka KJ, Palmeri KJ, Weissman IL. Mapping the genome of a model protochordate. I. A low resolution genetic map encompassing the fusion/histocompatibility (Fu/HC) locus of botryllus schlosseri. Genetics. 1998 May; 149(1): 277-287. PMCID: PMC1460123.
Fagan MB, Weissman IL. Characterization of a polymorphic protein localized to vascular epithelium in botryllus schlosseri: Role in tunic synthesis? Mol Mar Biol Biotechnol. 1998 Sep; 7(3): 204-213.
Fagan MB, Weissman IL. Linkage analysis of HSP70 genes and historecognition locus in botryllus schlosseri. Immunogenetics. 1998 May; 47(6): 468-476.
Rinkevich B, Weissman IL, De Tomaso AW. Transplantation of Fu/HC-incompatible zooids in botryllus schlosseri results in chimerism. Biol Bull. 1998 Oct; 195(2): 98-106.
1997
Fagan MB, Weissman IL. HSP70 genes and historecognition in botryllus schlosseri: Implications for MHC evolution. Hereditas. 1997; 127(1-2): 25-35.
Stoner DS, Quattro JM, Weissman IL. Highly polymorphic microsatellite loci in the colonial ascidian botryllus schlosseri. Mol Mar Biol Biotechnol. 1997 Sep; 6(3): 163-171.
1996
Fagan MB, Weissman IL. Sequence and characterization of two HSP70 genes in the colonial protochordate botryllus schlosseri. Immunogenetics. 1996; 44(2): 134-142.
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Stoner DS, Weissman IL. Somatic and germ cell parasitism in a colonial ascidian: Possible role for a highly polymorphic allorecognition system. Proc Natl Acad Sci U S A. 1996 Dec 24; 93(26): 15254-15259. PMCID: PMC26390.
1995
Chadwick-Furman NE, Weissman IL. Life history plasticity in chimaeras of the colonial ascidian botryllus schlosseri. Proc Biol Sci. 1995 Nov 22; 262(1364): 157-162.
Chadwick-Furman NE, Weissman IL. Life histories and senescence of botryllus schlosseri (chordata, ascidiacea) in monterey bay. Biol Bull. 1995 Aug; 189(1): 36-41.
1994
Bartl S, Baltimore D, Weissman IL. Molecular evolution of the vertebrate immune system. Proc Natl Acad Sci U S A. 1994 Nov 8; 91(23): 10769-10770. PMCID: PMC45107.
Bartl S, Weissman IL. The isolation of putative major histocompatibility complex gene fragments from dogfish and nurse shark. Ann N Y Acad Sci. 1994 Apr 15; 712: 346-349.
Bartl S, Weissman IL. PCR primers containing an inosine triplet to complement a variable codon within a conserved protein-coding region. BioTechniques. 1994 Feb; 16(2): 246-8, 250.
Bartl S, Weissman IL. Isolation and characterization of major histocompatibility complex class IIB genes from the nurse shark. Proc Natl Acad Sci U S A. 1994 Jan 4; 91(1): 262-266. PMCID: PMC42927.
Rinkevich B, Weissman IL, Shapira M. Alloimmune hierarchies and stress–induced reversals in the resorption of chimeric protochordate colonies. Proc R Soc Lond. B 1994; 258: 215–220.
1993
Lauzon RJ, Patton CW, Weissman IL. A morphological and immunohistochemical study of programmed cell death in botryllus schlosseri (tunicata, ascidiacea). Cell Tissue Res. 1993 Apr; 272(1): 115-127.
Rinkevich B, Saito Y, Weissman IL. A colonial invertebrate species that displays a hierarchy of allorecognition responses. Biol Bull. 1993 Feb; 184(1): 79-86.
1992
Lauzon RJ, Ishizuka KJ, Weissman IL. A cyclical, developmentally-regulated death phenomenon in a colonial urochordate. Dev Dyn. 1992 May; 194(1): 71-83.
Rinkevich B, Lauzon RJ, Brown BW, Weissman IL. Evidence for a programmed life span in a colonial protochordate. Proc Natl Acad Sci U S A. 1992 Apr 15; 89(8): 3546-3550. PMCID: PMC48905.
Rinkevich B, Weissman IL. Incidents of rejection and indifference in Fu/HC incompatible protochordate colonies. J Exp Zool. 1992 Aug 1; 263(1): 105-111.
Rinkevich B, Weissman IL. Allogeneic resorption in colonial protochordates: Consequences of nonself recognition. Dev Comp Immunol. 1992 Jul-Aug; 16(4): 275-286.
Rinkevich B, Shapira M, Weissman IL, Saito Y. Allogeneic responses between three remote populations of the cosmopolitan ascidian Botryllus schlosseri. Zool Sci. 1992; 9: 989–994.
Rinkevich B, Weissman IL. Chimeras vs genetically homogenous individuals: potential fitness costs and benefits. Oikos. 1992; 63: 119–124.
1991
Rinkevich B, Weissman IL. Inter populational allogeneic reactions in the colonial protochordate botryllus schlosseri. Int Immunol. 1991 Dec; 3(12): 1265-1272.
1990
Boyd HC, Weissman IL, Saito Y. Morphologic and genetic verification that monterey botryllus and woods hole botryllus are the same species. Biol Bull. 1990 Jun; 178(3): 239-250.
Lauzon R, Weissman IL. The paternal centrosome directs the polarity of early pattern formation in the fertilized ascidia ceratodes egg. In: Hoshi M, Yamashita O, eds. Advances in Invertebrate Reproduction 5. Amsterdam: Elsevier/North Holland Biomedical Press; 1990: 131–138.
Rinkevich B, Weissman IL. Failure to find alloimmune memory in the resorption phenomenon of botryllus cytomictical chimera. Eur J Immunol. 1990 Aug; 20(8): 1775-1779.
Rinkevich B, Weissman IL. Botryllus schlosseri (tunicata) whole colony irradiation: Do senescent zooid resorption and immunological resorption involve similar recognition events? J Exp Zool. 1990 Feb; 253(2): 189-201.
Weissman IL, Saito Y, Rinkevich B. Allorecognition histocompatibility in a protochordate species: Is the relationship to MHC somatic or structural? Immunol Rev. 1990 Feb; 113: 227-241.
1989
Rinkevich B, Weissman IL. Variation in the outcomes following chimera formation in the colonial tunicate Botryllus schlosseri. Bull Marine Sci. 1989; 45: 213–227.
1988
Harp JA, Tsuchida CB, Weissman IL, Scofield VL. Autoreactive blood cells and programmed cell death in growth and development of protochordates. J Exp Zool. 1988 Sep; 247(3): 257-262.
Rinkevich B, Weissman IL. Retreat growth in the ascidian Botryllus schlosseri: a consequence of nonself recognition. In: Grosberg R, Hedgecock D, Nelson K, eds. Invertebrate Historecognition. New York: Plenum Publishing Corporation; 1988: 93–109.
Weissman IL, Scofield V, Saito Y, Boyd H, Rinkevich B. Speculations on the relationships of two reactions —colony specificity and resorption —to vertebrate histocompatability. In: Grosberg R, Hedgecock D, Nelson K, eds. Invertebrate Historecognition. New York: Plenum Publishing Corporation; 1988; 67–78.
1987
Rinkevich B, Weissman IL. The fate of botryllus (ascidiacea) larvae cosettled with parental colonies: Beneficial or deleterious consequences? Biol Bull. 1987 Dec; 173(3): 474-488.
Rinkevich B, Weissman IL. A long–term study on fused subclones in the ascidian Botryllus schlosseri: the resorption phenomenon (Protochordata: tunicate). J Zoology. 1987; 213: 717–733.
1984
Schlumpberger JM, Weissman IL, Scofield VL. Separation and labeling of specific subpopulations of botryllus blood cells. J Exp Zool. 1984 Mar; 229(3): 401-411.
1982
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Scofield VL, Schlumpberger JM, West LA, Weissman IL. Protochordate allorecognition is controlled by a MHC-like gene system. Nature. 1982 Feb 11; 295(5849): 499-502.
Scofield VL, Schlumpberger JM, Weissman IL. Colony specificity in the colonial tunicate Botryllus and the origins of vertebrate immunity. Am Zoologist. 1982 22; 783–794.
1981
Scofield VL, Weissman IL. Allorecognition in biological systems. Devel and Comp Immunol. 1981; 5: 23–28.
1980
Weissman IL, Scofield VL, Schlumpberger J, Pillemer E, Hollander N, Rouse RV, Stevens SK, Butcher EC. Functional considerations of normal and neoplastic T lymphocytes. Presented at the Symposium on “The Biological Significance to Immune Regulation”, Seattle, Washington, December 27–31, 1980. In: Ruben LN, Gershwin ME, eds. Immune Regulation, Evolutionary and Biological Significance. New York: Marcel Dekker; 1982: 99–113.