primitive gut cell



Overview

Four large phagocytic cells associated with the temporary embryonic pharynx.

 

primitive gut cell

 

"PRIMITIVE GUT CELL" TERM REFERENCES

PMID:28072387

 

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Tissue Description

 

Four yolk-laden primitive gut cells associate with the temporary embryonic pharynx (Figure 1 – figure supplement 13 B-D, black arrows), and can frequently be detected in unstained specimens. Yolk ingested through the temporary embryonic pharynx collects in the central gut cavity.

Definitive gut development may begin as early as S4, with the production of isolated phagocytic cells that gradually form a continuous, honeycomb-like lattice beneath the embryonic wall (Figure 1 – figure supplement 13 B-D). Embryonic gut markers, identified amongst the S4-S5 enriched transcripts, were expressed in gut tissue through S6 and were subsequently downregulated as branching morphogenesis proceeded in elongated S7 embryos (Figure 1 – figure supplement 13 A-D). The progenitor population(s) for embryonic gut cell type(s) are not known.  These early intestinal cells may represent a transient population, turning over during S6-S7, or they may persist, changing their expression signature as morphogenesis proceeds.

Expression of gamma (g) class neoblast transcripts, including gata456a and hnf4, was detected in the temporary embryonic pharynx during S2, and in scattered cells in the embryonic wall during S5 (Figure 1 – figure supplement 13 E-G, Figure 6 B); a similar expression pattern was reported for Spol gata456a (Martín-Durán and Romero, 2011). The anarchic distribution of putative gut progenitors during embryogenesis is reminiscent of the systemic distribution of gut progenitors in the adult parenchyma, as well as the uniform incorporation of neoblast progeny into the adult gut during growth and homeostasis (Forsthoefel et al., 2011). In the adult gut, neoblast progeny incorporated into both new and preexisting gut tissue during regeneration, and morphallaxis of the gut required stem cell activity (Forsthoefel et al., 2011). Branching morphogenesis begins during S6-S7, as gut cells ingress from the anterior dorsoventral margins of the embryo, forming the secondary branches (Figure 1 – figure supplement 13 F-G, I). As in the adult, branching morphogenesis may proceed locally and may be reliant upon the incorporation of differentiating progeny, and/or remodeling of differentiated gut tissue.  Separation of the two posterior gut branches also occurs during S6-S7, concomitant with the development of the definitive pharynx and a medial, muscular septum running from the pharynx pouch to the posterior pole (Figure 1 – figure supplement 13 F-G, I). Many molecular markers of adult gut tissue are expressed during S5 or later (Forsthoefel et al., 2012; Wurtzel et al., 2015), suggesting that gut maturation is a gradual process (Figure 1 – figure supplement 13 H). Newborn hatchlings are born with yolk-filled intestines, and it may take up to one week to completely digest and clear the yolk from the gut. 

 

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Figures

Figure 1 – figure supplement 13: Molecular markers for the developing gut

A, E, H: Average RPKM values per embryo for A) embryonic gut transcripts cathepsin L1-like (CTSL-like: SMED30023322), lysosomal alpha glucosidase-like (LYAG-like: SMED30028442, SMED30008977), macrophage-expressed gene 1 like-3 (MPEG1-like-3: SMED30015696), E) gamma (g) class neoblast transcripts (gata456a, hnf4, prox-1, nkx2.2), and H) transcripts with enriched expression in the adult gut (Forsthoefel et al., 2012; Vu, 2015; Wurtzel et al., 2015) Yolk (Y), S2-S8. Early embryonic gut transcript expression was validated by WISH on staged embryo collections. H: Adult gut-enriched transcripts with enriched expression during S5 and/or S6 (top, n=146), or S7 and/or S8 (bottom, n=292).  Adult gut enriched transcripts are flagged in lists of S5-S8 enriched transcripts (Figure 1 – source data 5, Figure 1 – source data 6, Figure 1 – source data 7, Figure 1 – source data 8).  74% (n=1112) of the intestinal phagocyte enriched transcripts reported in (Forsthoefel et al., 2012) were identified in the smed20140614 transcriptome; 129 (11%) of the cross-referenced transcripts were enriched during S5, S6, S7 and/or S8. 90% (n=425) of the gut-enriched transcripts reported in (Wurtzel et al., 2015) were identified in the smed20140614 transcriptome; 44% (n=186) of the cross-referenced transcripts were enriched during S5, S6, S7 and/or S8. 

B-D: CTSL-like (B), LYAG-like (C) and MPEG1-like-3 (D) expression (blue) in the temporary embryonic pharynx (S2-S4), four primitive gut cells abutting the temporary embryonic pharynx (S4), and yolk-laden gut cells forming an irregular lattice beneath the embryonic wall (S5-S6). Expression of these markers was downregulated as branching morphogenesis proceeded during S7. 

F-G: gata456a (F) and hnf4 (G) expression (blue) during embryogenesis, S2-S8.  Staining was detected in the presumptive temporary embryonic pharynx (S2), and was later detected in scattered parenchymal cells from S5 onwards. Expression of both markers became more prominent in the developing gut over time, especially after branching morphogenesis was underway during S7-S8.

I: porcn-A expression (blue) during embryogenesis, S2-S8. Hazy, faint expression was detected in the gut during S5-S6, with increasing signal following the initiation of branching morphogenesis during S7-S8.

B-D, F-G, I: Anterior: top (S6-S8). O: oral hemisphere. A: aboral hemisphere. D: dorsal. V: ventral. Black arrowheads: temporary embryonic pharynx.  Black arrows: primitive gut cells. Red arrowheads: definitive pharynx. Scale bars: 100 µm.

 

 

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In Situ Hybridization Data

Smed IDAccessionNameAliasEnriched during stage(s)Tissue/PatternImages
SMED30015696SMED30015696MPEG1-like-3Stage 5embryonic gut cell, primitive gut cell, temporary embryonic pharynx
SMED30023322SMED30023322CTSL-likeStage 5embryonic gut cell, primitive gut cell, temporary embryonic pharynx
SMED30028442SMED30028442Stage 2, Stage 3, Stage 5embryonic gut cell, primitive gut cell, temporary embryonic pharynx

 

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Sequences

smed_20140614 transcript sequences for genes validated by in situ hybridization (above).

>SMED30015696 ID=SMED30015696|Name=SMED30015696|organism=Schmidtea mediterranea sexual|type=transcript|length=2665bp
AGTCGCGATAGCACGCAACGTCGACATTGCGATGACGTAATCATTGTGAATCTCTACTACAATCGGATCATTCTAATCAC
GTGCATCCTAAAACAATATAAATCTTACAAACGGGAATCCAATTGAACATTTATTTACTCAAGCGTGAAACCAATGATAC
CGTGTAGACTTAATAGTATAATATTGTTTATATTTGTTTATGGAGTTCTATCGGTTTCATGTGAAATTGAACCTAACCGA
GATCAACCATCTTCAAGACGAGTTCATGAGTGTAAACTCACCAGCAACCAATATCCAGTGAATGTTCTTCCCGGATCTGG
GTGGGATAATCTTGAAAACAAAGAACTCGGTCAAGTTTTAGAAATTTCATATAAAGGATGTTTTGGATCGAATGATGGAA
GCTTTCTCATTCCAGACAATGTGGTGATCACCCCAATAAAGAAATCTATTGTCGAGTTAACTTCAGATATATTTGACCAT
TTCTCAAATGTCACCTCTACAACGGCGATGTCTATCAACGCCGATGCCAGTTACTCAACACCAAGCTACAAAATCAGTGG
ATCATTTTCATTTGAAAAAATAAGAATAAAAAACGATCAAATCAAAGAAAAGTCGTCGATTTCGAGATCCCAGTTAAGAC
ATGAATTATATGAAGTAGCGTTCCAACCACACTCAAAACTAGACGCAAAATTCAGAAACAGAATTCTAGATATTGGAGCG
TTATTGAAAGAAGGAAAAGACACAATTTATCCACAATATTTAGCGGATTTAATTGTCCGTGACTTCGGCACTCACGTCAT
TCGGTCGGTGGATGCGGGAGCGACACTAATAAAGACTGATGTTTTAAAATCGAATTATGTCAAAGGTTTTAAAGGGGATA
CAACTAAGATTGCAGCTGCGGCATCATTCAGTATGACAACAATGCTTTCAGTCAACCTCAAAGGAACCTATGTTGGTGAT
ACCACGAGTCTCAATGAATTCAATAGTAATAGTGCAAGTACAAAAGTCGAAACTTTTGGTGGTATACCGTTTGGTTCGAA
TTTTAAGTTGGAAGATTGGGAGAAAACCCTTGAAACGAATTTGGTAGCAATTGATCGCAAAGGTGAACCGTTGTCCTATG
CTATCACACCAAAAAATCTTCCAGAATTCGATGAACAAGCAGTTTTCAAAATAGCTACGCTCATCAAAGAAGCAGTCAAT
AGATATTATGCAGCCAACACGAGAGTGGGATGTATGAATATGGAGTCAGAAAATTTCAATGACGACGCAAATGTTGACGG
TGGAAACTGCGAACCTCCTAATACATTTTACAGTTTTGGAGGAACTTTTCAAACCTGCTCAGGCCCTGATTATCAGTGTA
TGGATGTCGCGGCAAAAAACCCAGTGACCAATAGTTATGCTTGTCCTGATAACTATGATACCATTGAATTACAAAGTGGA
TTGAATAAATGCATAAATTATTGCACCAAATACTTATTTTCCACTCAATGTCATTACGAGTGTTCCCAATATGCATTGTA
TTGGTGTTCTTCTACAAACAAAACGAAAATATCAGAAGGCGCACTTTTCGGGGGATTCTACACTAATACATTTCCGAATC
CACTTACAAATTCCTATAGTTGTCCACAATACTATGTAGCGACAAGATTCGGCGTAAACGCCAAGGTTTGCACTGCACTC
AATAAGGCAGAGGCTATGGAACACCATTTGCCGTTTGGAGGATTTTATAGTTGCAAAGTTGGAAATCCTCTACTAGATGA
TCCTCTCTACAACATTACACAGGATCCCAAATATTGGCCTCAAGGTTGTTCAACCGGATATTCATCACATGTAGCTATTG
TCGACAGAGCTTGTCAAATTTCCTATTGCGTTAAAAATAACGCCCTTAGCATGAGAGAGCAACCGCCTCTCTACCGACCA
CCTTTTATTGATTTGGGATTTGGACCCAATATGACAGTAATTACCTCTCTGGACACTCCAATGGGGGTCCGATTATCTGT
TGATGAAAACGGGAAATGGAGTCATAATCACCAATACAAATTATCCAATTACAATATTATAATAATATCAGTCATTATGG
CGGCAGGAGCCAGCATTGCAATTATTATTATAATTCTTGGAGTTCAAAGATTCAGCAGAAACCGAAAAGGTCAAGTCTCA
CCGGAATCTCATGAATTTGATAGCAGATATGATTCTACTAAAGATGTTGCCAATCTTGCGTTACCCGGCGAGGTTCCACC
GTTTCGTGTTATAATTGACGGAGCGAAATGATGCTTGGAACCTTTTATTATTTCTGTTGAATCTGATCTGTAAATGTTTT
CAGAATATTTTTCTAATAAAATCGTTCTGAAATTTTAAAGTGATCCTTGATGCTATTAAATGATGGACTTTATTGTACCC
CGAATTGGGTCACCCTTGTTCACGCAAATTCGTGCTTAGGATATTTGTACGGGCTTATGCAACTTTTTAAATTTTTATTT
TTCCTTATTTTTATTAGCAATCCGTTTTATTTATAACGACAAATGCTTGATGTTTGAATCAAATTTTTATTATGTTTCTT
AATGAAACATAGTGAACAATGTGCCACTAATTTCATAACCAAGGTCTAATCAAATAGTTTGGGTAGTGAAAGCAATATTA
CAGAGTTTAGGTTTGTCATTCATAT
>SMED30023322 ID=SMED30023322|Name=SMED30023322|organism=Schmidtea mediterranea sexual|type=transcript|length=613bp
ACGCATTCTCTACGACAGGCGCGTTAGAAGGTCAACTATTCAGAAAAACTGGAAATTTGATAAGTTTATCTGAACAACAG
ATTGTTGATTGTGATAGTTTTGATTATGCATGTAACGGTGGATTTGTGACTGATACTTTAACTTATATTAAACAAAATGG
AGGAATTGAATCTGAGCAAGATTATCCATATGTGTCAGGAAGGACGAAGAAACCTAATAAAAAATGTTATTTCAAAAAAG
AAAAAATAGTGGGAACAGATACTGGTTTCGTATCTTTACCTCCAGGAGATGAAGAAGCTCTGAGAGAAGCTCTAGTAACA
ATTGGGCCAATTTCAATAGCTTTTTCCGCGTCGCCTTTGTTATCAGGATATAAGAATGGGATATATCATGATTACATGTG
TGCTGATGTTCGCATCAATCATGCAGTTTTACTAGTAGGATATGGAACGGATGAAGAATCAGGAACACCTTATTGGATAA
TAAAAAACAGTTGGGGTCCCGCATGGGGAGAAAATGGATATTTTCGAATGGAAAGAAATAAAAACATGTGCAACATGGCA
TACAATTCATACTATCCATTGGTTTGATTGAACGACTTCTTATGAGTGTGTGT
>SMED30028442 ID=SMED30028442|Name=SMED30028442|organism=Schmidtea mediterranea sexual|type=transcript|length=2946bp
ATTGTTATGCAAAATTATTTTAGCAAAAATTCCGATAGGTTTTATCTAATTAGTAATTAAGTAGATACTTCATGCTCTTG
AACTTGATTTTATTTTAAAATGGAGGTGTGTCGCTGATCTGGAAAAGTTTAATTTCAAATTATCTTTAATTAGATCATCA
CACCTATTTTAGTTGTTGTAGAGAGTCAAAGTTCAGCTTTTAATTAATATATATTCAATTAAAAATTTGCAAAAAATTAT
TTCCATTTCAAATGAAATTAATAATATTAATAAGTTTTATTAATTTGATTTCGTTATTCAACTTTTCCAACGCGACAGCA
CAATGTCAAATAGCCAATAACAATGAGAGACTTGATTGCTACCCAGAATCCGGAGCCAATCAAGATTCATGTATAGCAAG
GGGGTGTTGCTGGTCCGAACCAATGAGATTGTCCAATAAATTGCAAGGTGTTCCACTATCAATCCCATATTGCTATTATC
CAACTGATTATTCCAACTATATGATTAAATCCTTAAGAAAATCTTCAAGAGGGATCAAAGCAAAATTAGTCAGGGAATCA
CCAAGTTATTTACCCTATGAAGTTGCAATGTTAGATCTTGAGGTAATTTATGAAACAAAATCTAGAACTCGAGTCAGAAT
AACAGATCCTAAACAAAAAAGATATGAAGTTCCAATGAAACTCAGTCCTCCAGATTTGAAGCCACCGACTGATCGAGAAT
ATGAAGTCATAATCCCATCTGATGGTTCATTTTCTATTGAAATTAAACGAAAATCAGATGATCGTTCACTTTTCAAATCA
TTTGGGCCACTTTTATATTCTGATCAATTTTTACAAATATCTTCAATAATGTCAACTGATCAAATCTATGGAATAGGAGA
ACAAAATAGACCCTTTCTTCATCAATTATCCAATGGCTGGGAAAGAATTGGATTGTGGGCAAGAGACAATCCGATTGAAA
CATTTATGAATCTTTATGGAGCTCATCCATTTTATATCGGTATGCCAGACGATGGAAAAGCTTTCGGTGTTTTTCACTTT
AATAGTAATGGTCAAGAATTCGCTTTACAACCGGCACCAGCAGTAACTTATAGAACAATCGGTGGAATTTTAGATTTCTT
TATTTTTACCGGAGGCAGCCCTGAAGAAACAGTAAAACAATACCTAGAATTGGTAGGAAAGCCAATGCTTCCTCCATATT
GGTCTCTTGGATTCCATCTGTCAAAATGGGGTTACAAAAATATTGAGCAATTGTCTGAAATATTTCAAAGAAATATTAAT
GCCGGTTTCCCAATCGGTACTCAGTGGAGTGATATAGATTATATGGAAAATTATAAAGATTTTACTGTCGACAAAGAGAA
ATTTAATGGATTGGGAAGATTTGTCAGAGAGATTAAACAAAAATATAACTCTAGATTTGTTGCAATTGTTGATCCAGGAA
TAAGCTGCACAAGTGGTAACGAATATCCACCTTATTATGAAGGAGTATTTATGGATATTTTCATCAAAGATTCACAGACC
AATCAACCAATTGTTGGCAAGGTTTGGCCCGGAGAAACAGTTTATCCAGACTTCACTCATCCGAACATTTCTATGTATTG
GTATAAACAAATTCAACGCTTTTATAATGATGTTCCAATTGATGGGCTTTGGATTGATATGAATGAGCCATCTAATTTCT
ACGATGGTTCCAAAAGAGGCTGTCAAGGAAATAGTAAATATGACAATCCATTTTTTGTACCGGATATTCGAGATCAGTCA
TTAATATCTAAAACTATTTGTTCTTCAGCACTCCATTACAATAACGAAAAGCATTATAATTTGCACAATCTCTACGGCTA
TACGGAATCAGTAACAACAAATAAAGCATTATTAAAAACGATACACGGAAAAAGACCTTTTATTTTATCCCGGTCAACTT
TCAGTGGATCTGGTAAATATACCTTCCATTGGACCGGGGATAATCAAGCAAGTTGGGATCAGTTAAGAAATTCCATTAGA
CAAGTGCTTAATTTCAACATGTTTGGTATTCCGATGACTGGTGCTGACATTTGTGGATTTAACGGTAACAGTGATGAAGA
ACTCTGTATTAGATGGATGCAATTGGGCGCTTTTTATCCATTCATGAGGAACCACAATGCAATCAACCAGAGAGATCAAG
ATCCAGCTTCATGGAATACGGAAGCCCAGAAAATAATGAAAACAGCTATTTCTAATCGTTATGCAATGTTGCCTTTATTT
TATACATTATTAGTCAAATCCCATATGAATGGTGGCACCGTAATGAGACCAATGAGCTTTGAATTCTTTTCAGATAAAGT
AACGCATTCTATAGAATTACAGTTTATGATTGGATCCTCGATTATGGCAACTCCAGTTGTTTATCCTGGGGCCAGATCTG
TAGATGCATATTTTCCAGCTGGAGTCTGGTACGATTTTCACAGTGGAAAATTGTTACATTCAGATGCTGAAGGAGCTTGG
TTGACTTTGGATGCTCCTTTGGACAAAATTAATATTGCATTACGCGGCGGTCATATAGTTCCTCTATTGGATTCCAATAG
AAATTCTAAATCAAACATACCAAATAAAATGACATTGTATTGCGGAATGGCACAAGATATGAGTGCTTCTGGAGATTTAT
ATTGGGACGATGGCGAGAGCATTGACTCCTACTCACGCAATAGATATAGCTATGTATCATTCAATGCTAGCCCTGAGCAA
CTGTTAATAACACCGGTTTACTTTGGCTACGACTTGTTGCCGGTCTTAAACAAAATCGTAATCCTTGGGTTTGAGAATAA
GTCAATTACTAAATTTCTATTAAATGACAATGATATTCCTTTCCATTATAATCCGGAGACTTCATCTGTGGTGCTCAGCA
GTTTAAATGCCAATTTAAATTCCGAAATAAAAATTCAATGGATGTGAATAATTTTTTGTATTTTAT

 

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References

Forsthoefel, D.J., James, N.P., Escobar, D.J., Stary, J.M., Vieira, A.P., Waters, F.A., and Newmark, P.A. (2012). An RNAi screen reveals intestinal regulators of branching morphogenesis, differentiation, and stem cell proliferation in planarians. Dev Cell 23, 691-704.

Forsthoefel, D.J., Park, A.E., and Newmark, P.A. (2011). Stem cell-based growth, regeneration, and remodeling of the planarian intestine. Dev Biol 356, 445-459.

Martín-Durán, J.M., and Romero, R. (2011). Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa. Dev Biol 352, 164-176.

Wurtzel, O., Cote, L.E., Poirier, A., Satija, R., Regev, A., and Reddien, P.W. (2015). A Generic and Cell-Type-Specific Wound Response Precedes Regeneration in Planarians. Dev Cell 35, 632-645.

 

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