Conservation of cis-Regulatory Syntax Underlying Deuterostome Gastrulation
Abstract
:1. Introduction
2. Materials and Methods
2.1. Raw ATAC-Seq Data Retrieval
2.2. ATAC-Seq Analysis
2.3. Human Reactome Pathway Enrichment Analysis
3. Results
3.1. Identification of Accessible Putative Regulatory Regions (APREs)
3.2. Characterization of the APRE Distribution
3.3. Transcription Factor Binding Motifs Analyses
3.4. Identification of a Conserved Core of Transcription Factor-Binding Motifs during Gastrulation
Binding Motif Sequence | TF Family | TF | Germ Layer Pathway | Known Role in Gastrulation | Role in Organogenesis | Refs. |
---|---|---|---|---|---|---|
WAAGTAAACA | Forkhead | FoxA1 | Endoderm Mesoderm | Specification of anterior ectodermal program and repressor of posterior fates | Specification and differentiation of endodermal structures: gut, lungs, liver, kidneys, pancreas, prostate, notochord, nodes | [30,31,34,35,39,46,48,49,50,51,52,53] |
CYTGTTTACWYW | FoxA2 | Ectoderm | ||||
BSNTGTTTACWYWGN | FoxA3 | Endoderm Mesoderm | ||||
NVWTGTTTAC | FoxK1 | Mesoderm | Myogenesis | |||
SCHTGTTTACAT | FoxK2 | |||||
WWTRTAAACAVG | FoxL2 | Mesoderm Ectoderm | Specification of ovaries and eyes | |||
DGTAAACA | FoxO3 | Mesoderm | Vasculogenesis (blood vessels) | |||
TRTTTACTTW | FoxM1 | Ectoderm | Activation of G2-M cell-cycle regulators | Neuronal differentiation | ||
WWATRTAAACAN | FoxF1 | Mesoderm | Lung, liver, and gut development | |||
KTGTTTGC | FoxJ2 | Angiogenesis, spermatogenesis, ciliogenesis | ||||
CTGTTTAC | FoxO1 | Mesoderm | Vasculogenesis (blood vessels) | |||
NYYTGTTTACHN | FoxP1 | Ectoderm | Specification of nervous system and heart | |||
TTRAGTGSYK | Homeobox | Nkx3-2 | Endoderm Mesoderm | Neuroendoderm specification | Development of embryonic skeletal system and intestinal epithelium | [36,37,38,39,40,41,42,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68] |
VNNGGATTADNN | Gcs | Endoderm Mesoderm | Head organizer, notochord formation, cell migration | Anterior brain induction, craniofacial development, head patterning | ||
WACACGTAACTT | Irx3 | Ectoderm Mesoderm | Organizer, specification of neuronal progenitor cells of the spinal cord, anteroposterior patterning of neural axis | SHH-dependent neural patterning, development of inner ear, limbs, heart, kidneys, and facial/gill cartilage (regulated by the Wnt pathway) | ||
NGTGTTCAVTSAAGCGKAAA | Pax6 | Ectoderm Mesoderm | Specification of neuronal progenitor cells of the spinal cord | Development of eyes, pancreas, nose, nervous system, and pituitary gland | ||
RTGATTKATRGN | Pbx2 | Mesoderm | Development of hindbrain, tectum, retina, axial skeleton, and thyme | |||
SCTGTCAVTCAV | Pknox1 | Mesoderm | Apoptosis, chick primitive streak formation, (novel) regulator of EMT | Adipogenesis, differentiation of hematopoietic precursor cells, hindbrain segmentation, head cartilage development | ||
NYTAATCCYB | Otx2 | Ectoderm Endoderm | Specification of neuroectoderm and endoderm | Development of eyes, nose, ears, nervous system, first pharyngeal arch formation, and midbrain–hindbrain border (MHB) induction (regulated by retinoic acid signaling) | ||
KACACGTCTCTY | bHLH | Hey2 | Mesoderm | Cardiovascular development (Notch signaling) | [44,45,69,70,71] | |
VVCCACGTGG | c-Myc | Mesoderm Extraembryonic tissues | Cellular plasticity maintenance | |||
VRCCACGTGG | n-Myc | |||||
BAACAGCTGT | Myf5 | Mesoderm | Myogenesis | |||
AACAGCTG | MyoG | |||||
DGCACACGTG | Mnt | |||||
WNBCACGTGA | Arntl1 | Chick primitive streak, mediates hypoxia-induced IGFBP-1 expression | Development of nervous system, optic vesicles, notochord, foregut, and somites | |||
GHCACGTG | Clock | Chick primitive streak | Development of nervous system, optic vesicles, notochord, foregut, somites, and heart | |||
KCCACGTGAC | Npas2 | |||||
KCACGTGMCN | Dec2 | Prechordal plate | Neural crest cells | |||
VTTACGTAAYNNNNN | bZip | Nfil3 | Immune system | [72,73] | ||
RTTATGYAAB | Hlf | Clock-controlled gene, never associated with gastrulation | ||||
VTGACTCATC | AP-1 | |||||
GATGASTCATCN RATGASTCAT | JunB | Innate and adaptive immune responses, tumorigenesis | ||||
NNATGASTCATH | Fra1 | Differentiation of adipocytes, chondrocytes, and osteoblasts; placental vascularization | ||||
GGATGACTCATC NATGASTCABNN | FosL2 | Cell proliferation and differentiation | ||||
DATGASTCATHN | Atf3 | Mesoderm | ||||
DATGASTCAT | Batf | Differentiation of immune system cells | ||||
NKGMCACGTGDCMNN | Creb3L2 | Chondrogenesis, regulation of the secretory pathway | ||||
RRTSACGTSD | Usf2 | |||||
BCCATTGTTC | HMG | Sox2 | Ectoderm Endoderm | Development of nervous system, progenitor state maintenance | Embryonic stem cell pluripotency; specification of nervous system and eyes | [43,47,74,75,76,77,78,79,80,81,82,83] |
CCWTTGTY | Sox3 | Ectoderm Endoderm | Nervous system development, progenitor state maintenance | Formation of hypothalamic–pituitary axis, suppression of neuronal differentiation, craniofacial morphogenesis, sex determination | ||
YCTTTGTTCC | Sox4 | Regulator of epithelial–mesenchymal transition (EMT) | Development of eyes, pancreas, and skeletal system; differentiation of noradrenergic neurons | |||
CCATTGTTNY | Sox6 | Ectoderm Endoderm Mesoderm | Development of nervous system, chondrogenesis, maintenance of cardiac and skeletal muscle cells | |||
CCWTTGTYYB | Sox10 | Specification of neural crest | Development of neural crest and peripheral nervous system; glia and melanocyte development | |||
RAACAATGGN | Sox15 | Inhibition of myoblast differentiation, skeletal muscle regeneration, regulation of stem cell pluripotency, germline development | ||||
AGGVNCCTTTGT | Sox9 | Endoderm | Specification of neural crest | Chondrocyte, otic placode and glial differentiation, development of skeletal system, inner ear, craniofacial, male sex determination | ||
ASWTCAAAGG | Tcf3 | Endoderm | Axis specification, regulator of pluripotency | Neuronal differentiation, mesenchymal–epithelial transition (MET), eye development | ||
ASATCAAAGGVA | Tcf4 | Mesoderm | Neuronal differentiation | |||
CCTTTGATST | Lef1 | Ectoderm | ||||
CTTTGATGTGSB | Tcf7 | Mesoderm | T-cell lymphocyte differentiation | |||
CTGTCTGG | MAD | Smad2 | Endoderm | Specification of the anterior primitive streak, dorsoventral axis specification | [84,85,86,87] | |
VBSYGTCTGG | Smad4 | Endoderm | Specification of the anterior primitive streak | Heart and skeletal muscle development | ||
BGTTGACTWH | NR | Nr2E1 | Anterior brain differentiation, eye (retinal) development | [23] | ||
CGTTGACTWW NCGTTGACTT | Nr2F1 | Neurogenesis (regulated by retinoic acid signaling) | ||||
NNNTTGACYWNNNNN | Nr4A1 | Endoderm Mesoderm | Regeneration, immune response | |||
YACGTMAY | Zinc Finger | Atf1 | Role in correct gastrulation | (regulated by Notch signaling) | [88,89,90] | |
CCTGCTGAGH | Zic | Ectoderm | Left–right axis formation | Early neurogenesis (BMP signaling) | ||
MAATCACTGC | Gfi1b | Mesoderm | Hematopoiesis | |||
GGCGGCTG | Znf460 | |||||
Several BMs | Yy1 Yy2 | Embryonic and extraembryonic tissues | Morphogenetic movements | Cardiac morphogenesis (regulated by nodal signaling) | ||
HNACGCTCCT | Klf13 | Heart development |
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Species | Genome Assembly | Genome Size |
---|---|---|
Strongylocentrotus purpuratus | GCF_000002235.5 | 9.21 × 108 |
Branchiostoma lanceolatum | GCA_927797965.1 | 4.74 × 108 |
Ciona intestinalis | GCA_000224145.1 | 1.12 × 108 |
Danio rerio | GCF_000002035.5 | 1.46 × 109 |
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Buono, L.; Annona, G.; Magri, M.S.; Negueruela, S.; Sepe, R.M.; Caccavale, F.; Maeso, I.; Arnone, M.I.; D’Aniello, S. Conservation of cis-Regulatory Syntax Underlying Deuterostome Gastrulation. Cells 2024, 13, 1121. https://doi.org/10.3390/cells13131121
Buono L, Annona G, Magri MS, Negueruela S, Sepe RM, Caccavale F, Maeso I, Arnone MI, D’Aniello S. Conservation of cis-Regulatory Syntax Underlying Deuterostome Gastrulation. Cells. 2024; 13(13):1121. https://doi.org/10.3390/cells13131121
Chicago/Turabian StyleBuono, Lorena, Giovanni Annona, Marta Silvia Magri, Santiago Negueruela, Rosa Maria Sepe, Filomena Caccavale, Ignacio Maeso, Maria Ina Arnone, and Salvatore D’Aniello. 2024. "Conservation of cis-Regulatory Syntax Underlying Deuterostome Gastrulation" Cells 13, no. 13: 1121. https://doi.org/10.3390/cells13131121
APA StyleBuono, L., Annona, G., Magri, M. S., Negueruela, S., Sepe, R. M., Caccavale, F., Maeso, I., Arnone, M. I., & D’Aniello, S. (2024). Conservation of cis-Regulatory Syntax Underlying Deuterostome Gastrulation. Cells, 13(13), 1121. https://doi.org/10.3390/cells13131121