title: Functional genomic characterization of neoblast-like stem cells in larval Schistosoma mansoni
abstract: Schistosomes infect hundreds of millions of people in the developing world. Transmission of these parasites relies on a stem cell-driven, clonal expansion of larvae inside a molluscan intermediate host. How this novel asexual reproductive strategy relates to current models of stem cell maintenance and germline specification is unclear. Here, we demonstrate that this proliferative larval cell population (germinal cells) shares some molecular signatures with stem cells from diverse organisms, in particular neoblasts of planarians (free-living relatives of schistosomes). We identify two distinct germinal cell lineages that differ in their proliferation kinetics and expression of a nanos ortholog. We show that a vasa/PL10 homolog is required for proliferation and maintenance of both populations, whereas argonaute2 and a fibroblast growth factor receptor-encoding gene are required only for nanos-negative cells. Our results suggest that an ancient stem cell-based developmental program may have enabled the evolution of the complex life cycle of parasitic flatworms. DOI:http://dx.doi.org/10.7554/eLife.00768.001.
authors.affiliation: Howard Hughes Medical Institute, University of Illinois at Urbana-Champaign , Urbana , United States ; Institute for Genomic Biology , University of Illinois at Urbana-Champaign , Urbana , United States.
authors.forename: Bo
authors.initials: B
authors.lastname: Wang
authors.forename: James J
authors.initials: JJ
authors.lastname: Collins
authors.forename: Phillip A
authors.initials: PA
authors.lastname: Newmark
mesh_terms: D000818:Animals; D023281:Genomics; D009474:Neurons / Q000166:cytology*; D012550:Schistosoma mansoni / Q000166:cytology* / Q000235:genetics; D013234:Stem Cells / Q000166:cytology*
keywords: Other; Schistosoma mansoni; neoblasts; schistosomiasis; stem cells; trematode development
references.citation: J Invertebr Pathol. 1980 Nov;36(3):307-72
references.pmid: 7452064
references.citation: Nature. 2013 Apr 04;496(7443):57-63
references.pmid: 23485966
references.citation: PLoS Negl Trop Dis. 2012 Jan;6(1):e1455
references.pmid: 22253936
references.citation: J Parasitol. 1963 Jun;49:353-64
references.pmid: 14020610
references.citation: Parasitology. 2010 Mar;137(3):451-62
references.pmid: 19765348
references.citation: Mol Biochem Parasitol. 2003 May;128(2):205-15
references.pmid: 12742587
references.citation: Exp Parasitol. 1980 Dec;50(3):349-57
references.pmid: 7428911
references.citation: Cell Res. 2011 Dec;21(12):1750-4
references.pmid: 21894189
references.citation: J Parasitol. 1984 Jun;70(3):321-31
references.pmid: 6541688
references.citation: Dev Biol. 1999 Feb 1;206(1):73-87
references.pmid: 9918696
references.citation: Proc Natl Acad Sci U S A. 2008 Feb 19;105(7):2415-20
references.pmid: 18272492
references.citation: J Parasitol. 1974 Dec;60(6):935-41
references.pmid: 4436765
references.citation: Development. 2010 Dec;137(24):4113-26
references.pmid: 21098563
references.citation: Dev Growth Differ. 2002 Jun;44(3):191-204
references.pmid: 12060069
references.citation: Parasitol Res. 1989;75(5):368-74
references.pmid: 2542928
references.citation: Development. 2010 Oct;137(20):3351-60
references.pmid: 20876656
references.citation: Int J Parasitol. 2009 Sep;39(11):1223-33
references.pmid: 19394337
references.citation: Int J Parasitol. 1974 Apr;4(2):115-23
references.pmid: 4822479
references.citation: Nat Neurosci. 2011 Aug 30;14(11):1481-8
references.pmid: 21878933
references.citation: Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):4965-70
references.pmid: 10220402
references.citation: Parasitology. 1983 Apr;86 (Pt 4):121-60
references.pmid: 6346231
references.citation: BMC Dev Biol. 2013 Mar 12;13:8
references.pmid: 23497040
references.citation: Nature. 2013 Feb 28;494(7438):476-9
references.pmid: 23426263
references.citation: J Parasitol. 1995 Oct;81(5):714-22
references.pmid: 7472861
references.citation: Acta Trop. 2003 May;86(2-3):125-39
references.pmid: 12745133
references.citation: EMBO J. 2012 Jun 13;31(12):2755-69
references.pmid: 22543868
references.citation: PLoS Pathog. 2012;8(7):e1002820
references.pmid: 22911241
references.citation: Parasitol Int. 2009 Mar;58(1):61-8
references.pmid: 19007911
references.citation: Dev Cell. 2006 Aug;11(2):159-69
references.pmid: 16890156
references.citation: Exp Parasitol. 1954 Mar;3(2):185-225
references.pmid: 13161963
references.citation: J Parasitol. 1988 Feb;74(1):46-59
references.pmid: 3282054
references.citation: Mol Biochem Parasitol. 2010 Mar;170(1):37-40
references.pmid: 19914302
references.citation: Cell Stem Cell. 2012 Mar 2;10(3):299-311
references.pmid: 22385657
references.citation: Dev Biol. 2010 May 15;341(2):429-43
references.pmid: 20230812
references.citation: Int J Parasitol. 2007 Apr;37(5):515-23
references.pmid: 17188275
references.citation: Exp Parasitol. 1988 Jun;66(1):78-85
references.pmid: 3366217
references.citation: Science. 2011 May 13;332(6031):811-6
references.pmid: 21566185
references.citation: J Parasitol. 1949 Jun;35(3):267-75
references.pmid: 18153098
references.citation: PLoS Negl Trop Dis. 2012;6(6):e1686
references.pmid: 22720105
references.citation: Mol Biochem Parasitol. 2009 Mar;164(1):32-44
references.pmid: 19095013
references.citation: J Parasitol. 1981 Apr;67(2):179-85
references.pmid: 7241277
references.citation: PLoS Biol. 2010 Oct 12;8(10):e1000509
references.pmid: 20967238
references.citation: PLoS Negl Trop Dis. 2011 Aug;5(8):e1274
references.pmid: 21912711
references.citation: Mol Biochem Parasitol. 2009 Oct;167(2):118-26
references.pmid: 19463860
references.citation: PLoS Negl Trop Dis. 2011 Mar 08;5(3):e1009
references.pmid: 21408085
references.citation: J Parasitol. 2001 Oct;87(5):1167-8
references.pmid: 11695386
references.citation: Parasitology. 1972 Feb;64(1):129-41
references.pmid: 5010454
references.citation: Nat Rev Genet. 2002 Mar;3(3):210-9
references.pmid: 11972158
references.citation: Nature. 2009 Jul 16;460(7253):352-8
references.pmid: 19606141
references.citation: Development. 2010 Jan;137(2):213-21
references.pmid: 20040488
references.citation: Nat Cell Biol. 2012 Nov;14(11):1114-21
references.pmid: 23131918
references.citation: Cell Stem Cell. 2010 Sep 3;7(3):288-98
references.pmid: 20804966
references.citation: Micron. 2002;33(3):279-323
references.pmid: 11742750
references.citation: PLoS Negl Trop Dis. 2010 Aug 24;4(8):e804
references.pmid: 20808766