Abstract
Vertebrate cranial mesoderm is a discrete developmental unit compared to the mesoderm below the developing neck. An extraordinary feature of the cranial mesoderm is that it includes a common progenitor pool contributing to the chambered heart and the craniofacial skeletal muscles. This striking developmental potential and the excitement it generated led to advances in our understanding of cranial mesoderm developmental mechanism. Remarkably, recent findings have begun to unravel the origin of its distinct developmental characteristics. Here, we take a detailed view of the ontogenetic trajectory of cranial mesoderm and its regulatory network. Based on the emerging evidence, we propose that cranial and posterior mesoderm diverge at the earliest step of the process that patterns the mesoderm germ layer along the anterior–posterior body axis. Further, we discuss the latest evidence and their impact on our current understanding of the evolutionary origin of cranial mesoderm. Overall, the review highlights the findings from contemporary research, which lays the foundation to probe the molecular basis of unique developmental potential and evolutionary origin of cranial mesoderm.
Similar content being viewed by others
References
Gans C, Northcutt RG (1983) Neural crest and the origin of vertebrates: a new head. Science (80-) 220:268–273. https://doi.org/10.1126/science.220.4594.268
Stolfi A et al (2010) Early chordate origins of the vertebrate second heart field. Science (80-). https://doi.org/10.1126/science.1190181
Kaplan N, Razy-Krajka F, Christiaen L (2015) Regulation and evolution of cardiopharyngeal cell identity and behavior: insights from simple chordates. Curr Opin Genet Dev 32:119–128. https://doi.org/10.1016/j.gde.2015.02.008
Delsuc F et al (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968. https://doi.org/10.1038/nature04336
Sambasivan R, Kuratani S, Tajbakhsh S (2011) An eye on the head: the development and evolution of craniofacial muscles. Development 138:2401–2415. https://doi.org/10.1242/dev.040972
Gopalakrishnan S, Comai G, Sambasivan R et al (2015) A cranial mesoderm origin for esophagus striated muscles. Dev Cell 34:694–704. https://doi.org/10.1016/j.devcel.2015.07.003
Heude E, Tesarova M, Sefton EM et al (2018) Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues. Elife 7:1–26. https://doi.org/10.7554/eLife.40179
Lescroart F, Hamou W, Francou A et al (2015) Clonal analysis reveals a common origin between nonsomite-derived neck muscles and heart myocardium. Proc Natl Acad Sci 112:1446–1451. https://doi.org/10.1073/pnas.1424538112
Noden DM (1983) The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am J Anat 168:257–276. https://doi.org/10.1002/aja.1001680302
Evans DJR, Noden DM (2006) Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells. Dev Dyn 235:1310–1325. https://doi.org/10.1002/dvdy.20663
Jacob M et al (1984) Ontogeny of avian extrinsic muscles. Cell Tissue Res. https://doi.org/10.1007/bf00228439
Couly GF, Coltey PM, Le Douarin NM (1992) The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114:1–15
Kuratani S (2005) Craniofacial development and the evolution of the vertebrates: the old problems on a new background. Zoolog Sci 19:19. https://doi.org/10.2108/zsj.22.1
Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194–1218. https://doi.org/10.1002/dvdy.20697
Couly GF, Coltey PM, Le Douarin NM (1993) The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429
Bothe I, Ahmed MU, Winterbottom FL et al (2007) Extrinsic versus intrinsic cues in avian paraxial mesoderm patterning and differentiation. Dev Dyn 236:2397–2409. https://doi.org/10.1002/dvdy.21241
Noden DM, Trainor PA (2005) Relations and interactions between cranial mesoderm and neural crest populations. J Anat 207:575–601. https://doi.org/10.1111/j.1469-7580.2005.00473.x
Mootoosamy RC, Dietrich S (2002) Distinct regulatory cascades for head and trunk myogenesis. Development 129:573–583
Tzahor E, Kempf H, Mootoosamy RC et al (2003) Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle. Genes Dev 17:3087–3099. https://doi.org/10.1101/gad.1154103
Bothe I, Dietrich S (2006) The molecular setup of the avian head mesoderm and its implication for craniofacial myogenesis. Dev Dyn 235:2845–2860. https://doi.org/10.1002/dvdy.20903
Harel I, Maezawa Y, Avraham R et al (2012) Pharyngeal mesoderm regulatory network controls cardiac and head muscle morphogenesis. Proc Natl Acad Sci 109:18839–18844. https://doi.org/10.1073/pnas.1208690109
Lu J, Chang P, Valdez R et al (2001) Control of facial muscle development by MyoR and capsulin. Science 298:2378–2381. https://doi.org/10.1126/science.1078273
Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89:127–138. https://doi.org/10.1016/S0092-8674(00)80189-0
Kelly RG, Jerome-Majewska LA, Papaioannou VE (2004) The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum Mol Genet 13:2829–2840. https://doi.org/10.1093/hmg/ddh304
Shih HP, Gross MK, Kioussi C (2007) Cranial muscle defects of Pitx2 mutants result from specification defects in the first branchial arch. Proc Natl Acad Sci 104:5907–5912. https://doi.org/10.1073/pnas.0701122104
Dong F, Sun X, Liu W et al (2006) Pitx2 promotes development of splanchnic mesoderm-derived branchiomeric muscle. Development 133:4891–4899. https://doi.org/10.1242/dev.02693
Sambasivan R et al (2009) Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev Cell 16:810–821. https://doi.org/10.1016/j.devcel.2009.05.008
Cao J, Spielmann M, Qiu X et al (2019) The single-cell transcriptional landscape of mammalian organogenesis. Nature 566:496–502. https://doi.org/10.1038/s41586-019-0969-x
Kelly RG, Brown NA, Buckingham ME, Kingdom U (2001) The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 1:435–440
Lescroart F, Kelly RG, Le Garrec J-F et al (2010) Clonal analysis reveals common lineage relationships between head muscles and second heart field derivatives in the mouse embryo. Development 137:3269–3279. https://doi.org/10.1242/dev.050674
Lescroart F, Chabab S, Lin X et al (2014) Early lineage restriction in temporally distinct populations of Mesp1 progenitors during mammalian heart development. Nat Cell Biol 16:829–840. https://doi.org/10.1038/ncb3024
Zaffran S, Odelin G, Stefanovic S et al (2018) Ectopic expression of Hoxb1 induces cardiac and craniofacial malformations. Genesis 56:1–13. https://doi.org/10.1002/dvg.23221
Kelly RG, Buckingham ME (2002) The anterior heart-forming field: voyage to the arterial pole of the heart. Trends Genet 18:210–216. https://doi.org/10.1016/S0168-9525(02)02642-2
Tirosh-Finkel L (2006) Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract. Development 133:1943–1953. https://doi.org/10.1242/dev.02365
Nathan E, Monovich A, Tirosh-Finkel L et al (2008) The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. Development 135:647–657. https://doi.org/10.1242/dev.007989
Grifone R, Kelly RG (2007) Heartening news for head muscle development. Trends Genet 23:365–369. https://doi.org/10.1016/j.tig.2007.05.002
Diogo R, Kelly RG, Christiaen L et al (2015) A new heart for a new head in vertebrate cardiopharyngeal evolution. Nature 520:466–473. https://doi.org/10.1038/nature14435
Arnold SJ, Robertson EJ (2009) Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 10:91–103. https://doi.org/10.1038/nrm2618
Ramkumar and Anderson (2011) SnapShot: mouse primitive streak. Cell 146:488. https://doi.org/10.1016/j.cell.2011.07.028
Kinder SJ, Tsang TE, Quinlan GA et al (1999) The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo. Development 126:4691–4701
Tam PP, Beddington RS (1987) The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis. Development 99:109–126
Lawson KA, Pedersen RA (1992) Clonal analysis of cell fate during gastrulation and early neurulation in the mouse. In: Ciba foundation symposium, pp 3–26
Tam PP, Parameswaran M, Kinder SJ, Weinberger RP (1997) The allocation of epiblast cells to the embryonic heart and other mesodermal lineages: the role of ingression and tissue movement during gastrulation. Development 124:1631–1642
Yang L, Soonpaa MH, Adler ED et al (2008) Human cardiovascular progenitor cells develop from a KDR + embryonic-stem-cell-derived population. Nature 453:524–528. https://doi.org/10.1038/nature06894
Rao J, Pfeiffer MJ, Frank S et al (2016) Stepwise clearance of repressive roadblocks drives cardiac induction in human ESCs. Cell Stem Cell 18:341–353. https://doi.org/10.1016/j.stem.2015.11.019
Mendjan S, Mascetti VL, Ortmann D et al (2014) NANOG and CDX2 pattern distinct subtypes of human mesoderm during exit from pluripotency. Cell Stem Cell 15:310–325. https://doi.org/10.1016/j.stem.2014.06.006
Peng G, Suo S, Chen J et al (2016) Spatial transcriptome for the molecular annotation of lineage fates and cell identity in mid-gastrula mouse embryo. Dev Cell 36:681–697. https://doi.org/10.1016/j.devcel.2016.02.020
Vermillion KL, Bacher R, Tannenbaum AP et al (2018) Spatial patterns of gene expression are unveiled in the chick primitive streak by ordering single-cell transcriptomes. Dev Biol 439:30–41. https://doi.org/10.1016/j.ydbio.2018.04.007
Pijuan-Sala B, Griffiths JA, Guibentif C et al (2019) A single-cell molecular map of mouse gastrulation and early organogenesis. Nature 566:490–495. https://doi.org/10.1038/s41586-019-0933-9
Saykali B, Mathiah N, Nahaboo W et al (2019) Distinct mesoderm migration phenotypes in extra-embryonic and embryonic regions of the early mouse embryo. Elife 8:1–27. https://doi.org/10.7554/eLife.42434
Trainor PA, Tan SS, Tam PP (1994) Cranial paraxial mesoderm: regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development 120:2397–2408
Parameswaran M, Tam PPL (1995) Regionalisation of cell fate and morphogenetic movement of the mesoderm during mouse gastrulation. Dev Genet 17:16–28. https://doi.org/10.1002/dvg.1020170104
Nandkishore N, Vyas B, Javali A et al (2018) Divergent early mesoderm specification underlies distinct head and trunk muscle programmes in vertebrates. Development 4529:4522–4529. https://doi.org/10.1242/dev.173187
Takaoka K, Yamamoto M, Hamada H (2011) Origin and role of distal visceral endoderm, a group of cells that determines anterior-posterior polarity of the mouse embryo. Nat Cell Biol 13:743–752. https://doi.org/10.1038/ncb2251
Meno C, Gritsman K, Ohishi S et al (1999) Mouse lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation. Mol Cell 4:287–298. https://doi.org/10.1016/S1097-2765(00)80331-7
Yamamoto M, Saijoh Y, Perea-Gomez A et al (2004) Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428:387–392. https://doi.org/10.1038/nature02418
Finley KR, Tennessen J, Shawlot W (2003) The mouse Secreted frizzled-related protein 5 gene is expressed in the anterior visceral endoderm and foregut endoderm during early post-implantation development. Gene Expr Patterns 3:681–684. https://doi.org/10.1016/S1567-133X(03)00091-7
Kemp C, Willems E, Abdo S et al (2005) Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development. Dev Dyn 233:1064–1075. https://doi.org/10.1002/dvdy.20408
Perea-Gomez A, Camus A, Moreau A et al (2004) Initiation of gastrulation in the mouse embryo is preceded by an apparent shift in the orientation of the anterior-posterior axis. Curr Biol 14:197–207. https://doi.org/10.1016/S0960-9822(04)00044-2
Kimura C, Yoshinaga K, Tian E et al (2000) Visceral endoderm mediates forebrain development by suppressing posteriorizing signals. Dev Biol 225:304–321. https://doi.org/10.1006/dbio.2000.9835
Perea-Gomez A, Vella FDJ, Shawlot W et al (2002) Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev Cell 3:745–756. https://doi.org/10.1016/S1534-5807(02)00321-0
Thomas P, Beddington R (1996) Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr Biol 6:1487–1496. https://doi.org/10.1016/S0960-9822(96)00753-1
Perea-Gomez Rhinn M, Ang SL (2001) Role of the anterior visceral endoderm in restricting posterior signals in the mouse embryo. Int J Dev Biol 45:311–320
Perea-Gomez Lawson KA, Rhinn M et al (2001) Otx2 is required for visceral endoderm movement and for the restriction of posterior signals in the epiblast of the mouse embryo. Development 128:753–765
Brennan J, Lu CC, Norris DP et al (2001) Nodal signalling in the epiblast patterns the early mouse embryo Nature. 8716:965–969
Tortelote GG, Hernández-Hernández JM, Quaresma AJC et al (2013) Wnt3 function in the epiblast is required for the maintenance but not the initiation of gastrulation in mice. Dev Biol 374:164–173. https://doi.org/10.1016/j.ydbio.2012.10.013
Barrow JR, Howell WD, Rule M et al (2007) Wnt3 signaling in the epiblast is required for proper orientation of the anteroposterior axis. Dev Biol 312:312–320. https://doi.org/10.1016/j.ydbio.2007.09.030
Tam PP, Loebel DA, Tanaka SS (2006) Building the mouse gastrula: signals, asymmetry and lineages. Curr Opin Genet Dev 16:419–425. https://doi.org/10.1016/j.gde.2006.06.008
Rivera-Pérez JA, Magnuson T (2005) Primitive streak formation in mice is preceded by localized activation of Brachyury and Wnt3. Dev Biol 288:363–371. https://doi.org/10.1016/j.ydbio.2005.09.012
Mohamed OA, Clarke HJ, Dufort D (2004) β-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Dev Dyn 231:416–424. https://doi.org/10.1002/dvdy.20135
Kelly OG (2004) The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 131:2803–2815. https://doi.org/10.1242/dev.01137
Andre P, Song H, Kim W et al (2015) Wnt5a and Wnt11 regulate mammalian anterior-posterior axis elongation. Development 142:1516–1527. https://doi.org/10.1242/dev.119065
Hoshino H, Shioi G, Aizawa S (2015) AVE protein expression and visceral endoderm cell behavior during anterior-posterior axis formation in mouse embryos: asymmetry in OTX2 and DKK1 expression. Dev Biol 402:175–191. https://doi.org/10.1016/j.ydbio.2015.03.023
Schneider VA, Mercola M (1999) Spatially distinct head and heart inducers within the Xenopus organizer region. Curr Biol 9:800–809. https://doi.org/10.1016/S0960-9822(99)80363-7
Schneider and Mercola (2001) Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev 15:304–315. https://doi.org/10.1101/gad.855601
Mazzotta S, Neves C, Bonner RJ et al (2016) Distinctive roles of canonical and noncanonical Wnt signaling in human embryonic cardiomyocyte development. Stem Cell Rep 7:764–776. https://doi.org/10.1016/j.stemcr.2016.08.008
Marvin MJ, Di Rocco G, Gardiner A et al (2001) Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev 15:316–327. https://doi.org/10.1101/gad.855501
Palpant NJ, Pabon L, Roberts M et al (2015) Inhibition of β-catenin signaling respecifies anterior-like endothelium into beating human cardiomyocytes. Development 128:e1.2. https://doi.org/10.1242/jcs.180588
Minami I, Yamada K, Otsuji TG et al (2012) A small molecule that promotes cardiac differentiation of human pluripotent stem cells under defined, cytokine- and xeno-free conditions. Cell Rep 2:1448–1460. https://doi.org/10.1016/j.celrep.2012.09.015
Münsterberg AE, Kitajewski J, Bumcrot DA et al (1995) Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev 9:2911–2922. https://doi.org/10.1101/gad.9.23.2911
Capdevila J, Tabin C, Johnson RL (1998) Control of dorsoventral somite patterning by Wnt-1 and β-catenin. Dev Biol 193:182–194. https://doi.org/10.1006/dbio.1997.8806
Ikeya M, Takada S (1998) Wnt signaling from the dorsal neural tube is required for the formation of the medial dermomyotome. Development 125:4969–4976
Tajbakhsh S, Borello U, Vivarelli E et al (1998) Differential activation of Myf5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5. Development 125:4155–4162
Cossu G, Borello U (1999) Wnt signaling and the activation of myogenesis in mammals. EMBO J 18:6867–6872
Takada S, Stark KL, Shea MJ et al (1994) Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 8:174–189
Dunty WC, Biris KK, Chalamalasetty RB et al (2007) Wnt3a/β-catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development 135:85–94. https://doi.org/10.1242/dev.009266
Yamaguchi TP, Takada S, Yoshikawa Y et al (1999) T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev 13:3185–3190. https://doi.org/10.1101/gad.13.24.3185
Herrmann BG (1991) Expression pattern of the Brachyury gene in whole-mount TWis/TWis mutant embryos. Development 113:913–917
Chapman DL, Agulnik I, Hancock S et al (1996) Tbx6, a mouse T-box gene implicated in paraxial mesoderm formation at gastrulation. Dev Biol 180:534–542. https://doi.org/10.1006/dbio.1996.0326
Javali A, Misra A, Leonavicius K et al (2017) Co-expression of Tbx6 and Sox2 identifies a novel transient neuromesoderm progenitor cell state. Development 144:4522–4529. https://doi.org/10.1242/dev.153262
Boulet AM, Capecchi MR (2012) Signaling by FGF4 and FGF8 is required for axial elongation of the mouse embryo. Dev Biol 371:235–245. https://doi.org/10.1016/j.ydbio.2012.08.017
Ciruna B, Rossant J (2001) FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev Cell 1:37–49. https://doi.org/10.1016/S1534-5807(01)00017-X
Martin BL, Kimelman D (2012) Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. Dev Cell 22:223–232. https://doi.org/10.1016/j.devcel.2011.11.001
Turner DA, Hayward PC, Baillie-Johnson P et al (2014) Wnt/β-catenin and FGF signalling direct the specification and maintenance of a neuromesodermal axial progenitor in ensembles of mouse embryonic stem cells. Development 141:4243–4253. https://doi.org/10.1242/dev.112979
Garriock RJ, Chalamalasetty RB, Kennedy MW et al (2015) Lineage tracing of neuromesodermal progenitors reveals novel Wnt-dependent roles in trunk progenitor cell maintenance and differentiation. Development 142:1628–1638. https://doi.org/10.1242/dev.111922
Gouti M, Tsakiridis A, Wymeersch FJ et al (2014) In vitro generation of neuromesodermal progenitors reveals distinct roles for Wnt signalling in the specification of spinal cord and paraxial mesoderm identity. PLoS Biol. https://doi.org/10.1371/journal.pbio.1001937
Cambray N, Wilson V (2007) Two distinct sources for a population of maturing axial progenitors. Development 134:2829–2840. https://doi.org/10.1242/dev.02877
Tzouanacou E, Wegener A, Wymeersch FJ et al (2009) Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev Cell 17:365–376. https://doi.org/10.1016/j.devcel.2009.08.002
McGrew MJ, Sherman A, Lillico SG et al (2008) Localised axial progenitor cell populations in the avian tail bud are not committed to a posterior Hox identity. Development 135:2289–2299. https://doi.org/10.1242/dev.022020
Henrique D, Abranches E, Verrier L, Storey KG (2015) Neuromesodermal progenitors and the making of the spinal cord. Development 142:2864–2875. https://doi.org/10.1242/dev.119768
Steventon B, Martinez Arias A (2017) Evo-engineering and the cellular and molecular origins of the vertebrate spinal cord. Dev Biol 432:3–13. https://doi.org/10.1016/j.ydbio.2017.01.021
Chapman DL et al (1998) Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature 391:695–697. https://doi.org/10.1038/35624
King T, Beddington RSP, Brown NA (1998) The role of the brachyury gene in heart development and left-right specification in the mouse. Mech Dev 79:29–37. https://doi.org/10.1016/S0925-4773(98)00166-X
Kitaguchi T, Mizugishi K, Hatayama M et al (2002) Xenopus Brachyury regulates mesodermal expression of Zic3, a gene controlling left-right asymmetry. Dev Growth Differ 44:55–61. https://doi.org/10.1046/j.1440-169x.2002.00624.x
Hadjantonakis AK, Pisano E, Papaioannou VE (2008) Tbx6 regulates left/right patterning in mouse embryos through effects on nodal cilia and perinodal signaling. PLoS One. https://doi.org/10.1371/journal.pone.0002511
Liu P, Wakamiya M, Shea MJ et al (1999) Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22:361–365. https://doi.org/10.1038/11932
Galceran J, Fariñas I, Depew MJ et al (1999) Wnt3a−/−-like phenotype and limb deficiency in Lef−/−Tcf1−/− mice. Genes Dev 13:709–717
De Robertis EM (2008) Evo-Devo: variations on ancestral themes. Cell 132:185–195. https://doi.org/10.1016/j.cell.2008.01.003
Niehrs C (2010) On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137:845–857. https://doi.org/10.1242/dev.039651
Petersen CP, Reddien PW (2009) wnt signaling and the polarity of the primary body axis. Cell 139:1056–1068. https://doi.org/10.1016/j.cell.2009.11.035
Ikeya M, Takada S (2001) Wnt-3a is required for somite specification along the anteroposterior axis of mouse embryo and for regulation of Cdx-1 expression. Mech Dev 103:27–33
Nordström U, Maier E, Jessell TM, Edlund T (2006) An early role for Wnt signaling in specifying neural patterns of Cdx and Hox gene expression and motor neuron subtype identity. PLoS Biol 4:1438–1452. https://doi.org/10.1371/journal.pbio.0040252
Pilon N, Oh K, Sylvestre JR et al (2006) Cdx4 is a direct target of the canonical Wnt pathway. Dev Biol 289:55–63. https://doi.org/10.1016/j.ydbio.2005.10.005
Shimizu T, Bae YK, Muraoka O, Hibi M (2005) Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. Dev Biol 279:125–141. https://doi.org/10.1016/j.ydbio.2004.12.007
van de Ven C, Bialecka M, Neijts R et al (2011) Concerted involvement of Cdx/Hox genes and Wnt signaling in morphogenesis of the caudal neural tube and cloacal derivatives from the posterior growth zone. Development 138:3859. https://doi.org/10.1242/dev.072462
van den Akker E, Forlani S, Chawengsaksophak K et al (2002) Cdx1 and Cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development 129:2181–2193
Neijts R, Amin S, van Rooijen C, Deschamps J (2017) Cdx is crucial for the timing mechanism driving colinear Hox activation and defines a trunk segment in the Hox cluster topology. Dev Biol 422:146–154. https://doi.org/10.1016/j.ydbio.2016.12.024
Young T, Rowland JE, van de Ven C et al (2009) Cdx and hox genes differentially regulate posterior axial growth in mammalian embryos. Dev Cell 17:516–526. https://doi.org/10.1016/j.devcel.2009.08.010
van Rooijen C, Simmini S, Bialecka M et al (2012) Evolutionarily conserved requirement of Cdx for post-occipital tissue emergence. Development 139:2576–2583. https://doi.org/10.1242/dev.079848
Ciruna BG, Rossant J (1999) Expression of the T-box gene eomesodermin during early mouse development. Mech Dev 81:199–203. https://doi.org/10.1016/S0925-4773(98)00243-3
Saga Y, Hata N, Taketo MM et al (1996) MesP1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development 122:2769–2778
Saga Y, Miyagawa-Tomita S, Takagi A et al (1999) MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 126:3437–3447
Harel I, Nathan E, Tirosh-Finkel L et al (2009) Distinct origins and genetic programs of head muscle satellite cells. Dev Cell 16:822–832. https://doi.org/10.1016/j.devcel.2009.05.007
Kitajima S, Takagi A, Inoue T, Saga Y (2000) MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development 127:3215–3226
Chan SSK, Shi X, Toyama A et al (2013) Mesp1 patterns mesoderm into cardiac, hematopoietic, or skeletal myogenic progenitors in a context-dependent manner. Cell Stem Cell 12:587–601. https://doi.org/10.1016/j.stem.2013.03.004
Satou Y et al (2004) The ascidian Mesp gene specifies heart precursor cells. Development 131:2533–2541. https://doi.org/10.1242/dev.01145
Costello I, Pimeisl IM, Dräger S et al (2011) The T-box transcription factor eomesodermin acts upstream of Mesp1 to specify cardiac mesoderm during mouse gastrulation. Nat Cell Biol 13:1084–1092. https://doi.org/10.1038/ncb2304
Arnold SJ, Hofmann UK, Bikoff EK, Robertson EJ (2008) Pivotal roles for eomesodermin during axis formation, epithelium-to-mesenchyme transition and endoderm specification in the mouse. Development 135:501–511. https://doi.org/10.1242/dev.014357
Bondue A, Blanpain C (2010) Mesp1: a key regulator of cardiovascular lineage commitment. Circ Res 107:1414–1427. https://doi.org/10.1161/CIRCRESAHA.110.227058
Hacker A, Guthrie S (1998) A distinct developmental programme for the cranial paraxial mesoderm in the chick embryo. Development 125:3461–3472
Rios AC, Serralbo O, Salgado D, Marcelle C (2011) Neural crest regulates myogenesis through the transient activation of NOTCH. Nature 473:532–535. https://doi.org/10.1038/nature09970
Köntges G, Lumsden A (1996) Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 122:3229–3242
Grenier J, Teillet MA, Grifone R et al (2009) Relationship between neural crest cells and cranial mesoderm during head muscle development. PLoS One. https://doi.org/10.1371/journal.pone.0004381
Rinon A, Lazar S, Marshall H et al (2007) Cranial neural crest cells regulate head muscle patterning and differentiation during vertebrate embryogenesis. Development 134:3065–3075. https://doi.org/10.1242/dev.002501
Rios AC, Marcelle C (2009) Head muscles: aliens who came in from the cold? Dev Cell 16:779–780. https://doi.org/10.1016/j.devcel.2009.06.004
Kuratani S, Schilling T (2008) Head segmentation in vertebrates. Integr Comp Biol 48:604–610. https://doi.org/10.1093/icb/icn036
Onai T, Adachi N, Kuratani S (2017) Metamerism in cephalochordates and the problem of the vertebrate head. Int J Dev Biol 61:621–632. https://doi.org/10.1387/ijdb.170121to
Holland LZ, Holland ND, Gilland E (2008) Amphioxus and the evolution of head segmentation. Integr Comp Biol 48:630–646. https://doi.org/10.1093/icb/icn060
Aldea D, Subirana L, Keime C et al (2019) Genetic regulation of amphioxus somitogenesis informs the evolution of the vertebrate head mesoderm. Nat Ecol Evol. https://doi.org/10.1038/s41559-019-0933-z
Bertrand S, Camasses A, Somorjai I et al (2011) Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits. Proc Natl Acad Sci 108:9160–9165. https://doi.org/10.1073/pnas.1014235108
Holland ND, Venkatesh TV, Holland LZ et al (2003) AmphiNk2-tin, an amphioxus homeobox gene expressed in myocardial progenitors: insights into evolution of the vertebrate heart. Dev Biol 255:128–137. https://doi.org/10.1016/S0012-1606(02)00050-7
Pascual-Anaya J, Albuixech-Crespo B, Somorjai IML et al (2013) The evolutionary origins of chordate hematopoiesis and vertebrate endothelia. Dev Biol 375:182–192. https://doi.org/10.1016/j.ydbio.2012.11.015
Achim K, Arendt D (2014) Structural evolution of cell types by step-wise assembly of cellular modules. Curr Opin Genet Dev 27:102–108. https://doi.org/10.1016/j.gde.2014.05.001
Brunet T, Fischer AHL, Steinmetz PRH et al (2016) The evolutionary origin of bilaterian smooth and striated myocytes. Elife 5:1–24. https://doi.org/10.7554/eLife.19607
Amacher SL, Draper BW, Summers BR, Kimmel CB (2002) The zebrafish T-box genes no tail and spadetail are required for development of trunk and tail mesoderm and medial floor plate. Development 3323:3311–3323
Baillie-johnson P, Hayward P (2018) The chick caudolateral epiblast acts as a permissive niche for generating neuromesodermal progenitor behaviours. Cell Tissue Organs. https://doi.org/10.1159/000494769
Attardi A, Fulton T, Florescu M et al (2019) Correction: neuromesodermal progenitors are a conserved source of spinal cord with divergent growth dynamics. Development 146:dev175620. https://doi.org/10.1242/dev.175620
Ansari S, Troelenberg N, Dao VA et al (2018) Double abdomen in a short-germ insect: zygotic control of axis formation revealed in the beetle Tribolium castaneum. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1716512115
Fritzenwanker JH, Uhlinger KR, Gerhart J et al (2019) Untangling posterior growth and segmentation by analyzing mechanisms of axis elongation in hemichordates. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1817496116
Niehrs C (2004) Regionally specific induction by the Spemann-Mangold organizer. Nat Rev Genet 5:425–434. https://doi.org/10.1038/nrg1347
De Robertis E (2010) Wnt signaling in axial patterning and regeneration: lessons from planaria. Sci Signal 3:2008–2011. https://doi.org/10.1126/scisignal.3127pe21
Loh KM, van Amerongen R, Nusse R (2016) Generating cellular diversity and spatial form: Wnt signaling and the evolution of multicellular animals. Dev Cell 38:643–655. https://doi.org/10.1016/j.devcel.2016.08.011
Yoshida T, Vivatbutsiri P, Morriss-Kay G et al (2008) Cell lineage in mammalian craniofacial mesenchyme. Mech Dev 125:797–808. https://doi.org/10.1016/j.mod.2008.06.007
Graham A, Shimeld SM (2013) The origin and evolution of the ectodermal placodes. J Anat 222:32–40. https://doi.org/10.1111/j.1469-7580.2012.01506.x
Abitua PB, Wagner E, Navarrete IA, Levine M (2012) Identification of a rudimentary neural crest in a non-vertebrate chordate. Nature 492:104–107. https://doi.org/10.1038/nature11589
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Vyas, B., Nandkishore, N. & Sambasivan, R. Vertebrate cranial mesoderm: developmental trajectory and evolutionary origin. Cell. Mol. Life Sci. 77, 1933–1945 (2020). https://doi.org/10.1007/s00018-019-03373-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00018-019-03373-1