The evolutionary origins of chordate hematopoiesis and vertebrate endothelia

Developmental Biology

Volumn 375, Issue 2, 2013, Pages 182-192

  Pascual Anaya, Juan ^a,b   Albuixech Crespo, Beatriz ^a   Somorjai, Ildikó Maureen Lara ^a,f   Carmona, Rita ^c   Oisi, Yasuhiro ^b,d   Álvarez, Susana ^e   Kuratani, Shigeru ^b   Muñoz Chápuli, Ramón ^c   Garcia Fernàndez, Jordi ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c UNIVERSITY OF MÁLAGA   (Spain)

^d KOBE UNIVERSITY   (Japan)

^e UNIVERSITY OF VIGO   (Spain)

^f UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

Amphioxus; Endothelium; Evo devo; Hematopoiesis; Scl Tal 1; VEGFR 2 Flk 1

Indexed keywords

RETINOIC ACID; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR TBX5; VASCULOTROPIN RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRANCHIOSTOMA; BRANCHIOSTOMA FLORIDAE; BRANCHIOSTOMA ISLET; CHORDATA; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; ENDOTHELIUM; GATA1 GENE; GATA3 GENE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; HAND1 GENE; HAND2 GENE; HEART DEVELOPMENT; HEMATOPOIESIS; LARVAL STAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PDVEGFR GENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCL GENE; TBX5 GENE;

BRANCHIOSTOMA LANCEOLATUM; INVERTEBRATA; METAZOA; VERTEBRATA;

EID: 84874243144     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.11.015     Document Type: Article

References (76)

1. Abascal F., Zardoya R., Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
2. Belgacem M.R., Escande M.L., Escriva H., Bertrand S. Amphioxus Tbx6/16 and Tbx20 embryonic expression patterns reveal ancestral functions in chordates. Gene Expr. Patterns 2011, 11:239-243.
3. Bertrand S., Escriva H. Evolutionary crossroads in developmental biology: amphioxus. Development 2011, 138:4819-4830.
4. Candiani S., Pestarino M., Cattaneo E., Tartari M. Characterization, developmental expression and evolutionary features of the huntingtin gene in the amphioxus Branchiostoma floridae. BMC Dev. Biol. 2007, 7:127.
5. Cumano A., Godin I. Ontogeny of the hematopoietic system. Annu. Rev. Immunol. 2007, 25:745-785.
6. D'Aniello S., Irimia M., Maeso I., Pascual-Anaya J., Jiménez-Delgado S., Bertrand S., Garcia-Fernàndez J. Gene expansion and retention leads to a diverse tyrosine kinase superfamily in amphioxus. Mol. Biol. Evol. 2008, 25:1841-1854.
7. Davidson E.H., Erwin D.H. Gene regulatory networks and the evolution of animal body plans. Science 2006, 311:796-800.
8. de Jong J.L., Davidson A.J., Wang Y., Palis J., Opara P., Pugach E., Daley G.Q., Zon L.I. Interaction of retinoic acid and scl controls primitive blood development. Blood 2010, 116:201-209.
9. Delsuc F., Brinkmann H., Chourrout D., Philippe H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 2006, 439:965-968.
10. Drummond A., Strimmer K. PAL: an object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 2001, 17:662-663.
11. Ema M., Faloon P., Zhang W.J., Hirashima M., Reid T., Stanford W.L., Orkin S., Choi K., Rossant J. Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev. 2003, 17:380-393.
12. Escriva H., Holland N.D., Gronemeyer H., Laudet V., Holland L.Z. The retinoic acid signaling pathway regulates anterior/posterior patterning in the nerve cord and pharynx of amphioxus, a chordate lacking neural crest. Development 2002, 129:2905-2916.
13. Ferran J.L., de Oliveira E.D., Merchán P., Sandoval J.E., Sánchez-Arrones L., Martínez-De-La-Torre M., Puelles L. Genoarchitectonic profile of developing nuclear groups in the chicken pretectum. J. Comp. Neurol. 2009, 517:405-451.
14. Franz V. Morphologie der Akranier. Ergebnisse der Anatomie und Entwicklungsgeschichte 1927, 27:464-692.
15. Fuentes M., Benito E., Bertrand S., Paris M., Mignardot A., Godoy L., Jiménez-Delgado S., Oliveri D., Candiani S., Hirsinger E., D'Aniello S., Pascual-Anaya J., Maeso I., Pestarino M., Vernier P., Nicolas J.F., Schubert M., Laudet V., Geneviere A.M., Albalat R., Garcia-Fernàndez J., Holland N.D., Escriva H. Insights into spawning behavior and development of the European amphioxus (Branchiostoma lanceolatum). J. Exp. Zool. B: Mol. Dev. Evol. 2007, 308:484-493.
16. Galloway J.L., Zon L.I. Ontogeny of hematopoiesis: examining the emergence of hematopoietic cells in the vertebrate embryo. Curr. Top. Dev. Biol. 2003, 53:139-158.
17. Gering M., Rodaway A.R., Göttgens B., Patient R.K., Green A.R. The SCL gene specifies haemangioblast development from early mesoderm. EMBO J. 1998, 17:4029-4045.
18. Gillis W.Q., Bowerman B.A., Schneider S.Q. The evolution of protostome GATA factors: molecular phylogenetics, synteny, and intron/exon structure reveal orthologous relationships. BMC Evol. Biol. 2008, 8:112.
19. Gillis W.Q., John J., Bowerman B., Schneider S.Q. Whole genome duplications and expansion of the vertebrate GATA transcription factor gene family. BMC Evol. Biol. 2009, 9:207.
20. Giroux S., Kaushik A.L., Capron C., Jalil A., Kelaidi C., Sablitzky F., Dumenil D., Albagli O., Godin I. lyl-1 and tal-1/scl, two genes encoding closely related bHLH transcription factors, display highly overlapping expression patterns during cardiovascular and hematopoietic ontogeny. Gene Expr. Patterns 2007, 7:215-226.
21. Godin I., Cumano A. The hare and the tortoise: an embryonic haematopoietic race. Nat. Rev. Immunol. 2002, 2:593-604.
22. Goodrich E.S. The early development of the nephridia in amphioxus: introduction and part I, Hatschek's nephridium. Q. J. Microsc. Sci. 1934, 75:723-734.
23. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
24. Hartenstein V. Blood cells and blood cell development in the animal kingdom. Annu. Rev. Cell Dev. Biol. 2006, 22:677-712.
25. Holland N.D., Venkatesh T.V., Holland L.Z., Jacobs D.K., Bodmer R. AmphiNk2-tin, an amphioxus homeobox gene expressed in myocardial progenitors: insights into evolution of the vertebrate heart. Dev. Biol. 2003, 255:128-137.
26. Holland P.W., Booth H.A., Bruford E.A. Classification and nomenclature of all human homeobox genes. BMC Biol. 2007, 5:47.
27. Horton A.C., Mahadevan N.R., Minguillon C., Osoegawa K., Rokhsar D.S., Ruvinsky I., de Jong P.J., Logan M.P., Gibson-Brown J.J. Conservation of linkage and evolution of developmental function within the Tbx2/3/4/5 subfamily of T-box genes: implications for the origin of vertebrate limbs. Dev. Genes Evol. 2008, 218:613-628.
28. Irimia M., Piñeiro C., Maeso I., Gómez-Skarmeta J.L., Casares F., Garcia-Fernàndez J. Conserved developmental expression of Fezf in chordates and Drosophila and the origin of the Zona Limitans Intrathalamica (ZLI) brain organizer. Evodevo 2010, 1:7.
29. Ishitobi H., Wakamatsu A., Liu F., Azami T., Hamada M., Matsumoto K., Kataoka H., Kobayashi M., Choi K., Nishikawa S., Takahashi S., Ema M. Molecular basis for Flk1 expression in hemato-cardiovascular progenitors in the mouse. Development 2011, 138:5357-5368.
30. Jackman W.R., Langeland J.A., Kimmel C.B. islet reveals segmentation in the amphioxus hindbrain homolog. Dev. Biol. 2000, 220:16-26.
31. Jiménez-Delgado S., Pascual-Anaya J., Garcia-Fernàndez J. Implications of duplicated cis-regulatory elements in the evolution of metazoans: the DDI model or how simplicity begets novelty. Brief. Funct. Genomic Proteomic 2009, 8:266-275.
32. Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002, 30:3059-3066.
33. Kattman S.J., Huber T.L., Keller G.M. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev. Cell 2006, 11:723-732.
34. Kozmik Z., Holland N.D., Kalousova A., Paces J., Schubert M., Holland L.Z. Characterization of an amphioxus paired box gene, AmphiPax2/5/8: developmental expression patterns in optic support cells, nephridium, thyroid-like structures and pharyngeal gill slits, but not in the midbrain-hindbrain boundary region. Development 1999, 126:1295-1304.
35. Kučera T., Strilić B., Regener K., Schubert M., Laudet V., Lammert E. Ancestral vascular lumen formation via basal cell surfaces. PLoS One 2009, 4:e4132.
36. Ma D., Zhang J., Lin H.F., Italiano J., Handin R.I. The identification and characterization of zebrafish hematopoietic stem cells. Blood 2011, 118:289-297.
37. Mandal L., Banerjee U., Hartenstein V. Evidence for a fruit fly hemangioblast and similarities between lymph-gland hematopoiesis in fruit fly and mammal aorta-gonadal-mesonephros mesoderm. Nat. Genet. 2004, 36:1019-1023.
38. McFadden D.G., Barbosa A.C., Richardson J.A., Schneider M.D., Srivastava D., Olson E.N. The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner. Development 2005, 132:189-201.
39. Mead P.E., Deconinck A.E., Huber T.L., Orkin S.H., Zon L.I. Primitive erythropoiesis in the Xenopus embryo: the synergistic role of LMO-2, SCL and GATA-binding proteins. Development 2001, 128:2301-2308.
40. Medioni C., Sénatore S., Salmand P.A., Lalevée N., Perrin L., Sémériva M. The fabulous destiny of the Drosophila heart. Curr. Opin. Genet. Dev. 2009, 19:518-525.
41. Minguillon C., Gibson-Brown J.J., Logan M.P. Tbx4/5 gene duplication and the origin of vertebrate paired appendages. Proc. Nat. Acad. Sci. U.S.A. 2009, 106:21726-21730.
42. Moller P.C., Philpott C.W. The circulatory system of Amphioxus (Branchiostoma floridae). I. Morphology of the major vessels of the pharyngeal area. J. Morphol. 1973, 139:389-406.
43. Muñoz-Chápuli R. Evolution of angiogenesis. Int. J. Dev. Biol. 2011, 55:345-351.
44. Muñoz-Chápuli R., Carmona R., Guadix J.A., Macías D., Pérez-Pomares J.M. The origin of the endothelial cells: an evo-devo approach for the invertebrate/vertebrate transition of the circulatory system. Evol. Dev. 2005, 7:351-358.
45. Muñoz-Chápuli R., Pérez-Pomares J.M. Cardiogenesis: an embryological perspective. J. Cardiovasc. Transl. Res. 2010, 3:37-48.
46. Naiche L.A., Harrelson Z., Kelly R.G., Papaioannou V.E. T-box genes in vertebrate development. Annu. Rev. Genet. 2005, 39:219-239.
47. Olson E.N. Gene regulatory networks in the evolution and development of the heart. Science 2006, 313:1922-1927.
48. Onimaru K., Shoguchi E., Kuratani S., Tanaka M. Development and evolution of the lateral plate mesoderm: comparative analysis of amphioxus and lamprey with implications for the acquisition of paired fins. Dev. Biol. 2011, 359:124-136.
49. Orkin S.H., Zon L.I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
50. Otrock Z.K., Makarem J.A., Shamseddine A.I. Vascular endothelial growth factor family of ligands and receptors: review. Blood Cells Mol. Dis. 2007, 38:258-268.
51. Panopoulou G.D., Clark M.D., Holland L.Z., Lehrach H., Holland N.D. AmphiBMP2/4, an amphioxus bone morphogenetic protein closely related to Drosophila decapentaplegic and vertebrate BMP2 and BMP4: insights into evolution of dorsoventral axis specification. Dev. Dyn. 1998, 213:130-139.
52. Pérez-Pomares J.M., Gonzalez-Rosa J.M., Muñoz-Chápuli R. Building the vertebrate heart-an evolutionary approach to cardiac development. Int. J. Dev. Biol. 2009, 53:1427-1443.
53. Pimanda J.E., Ottersbach K., Knezevic K., Kinston S., Chan W.Y., Wilson N.K., Landry J.R., Wood A.D., Kolb-Kokocinski A., Green A.R., Tannahill D., Lacaud G., Kouskoff V., Göttgens B. Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc. Nat. Acad. Sci. U.S.A. 2007, 104:17692-17697.
54. Ragkousi K., Beh J., Sweeney S., Starobinska E., Davidson B. A single GATA factor plays discrete, lineage specific roles in ascidian heart development. Dev. Biol. 2011, 352:154-163.
55. Rähr H. The circulatory system of Amphioxus [Branchiostoma lanceolatum (Pallas)]. Acta Zool. 1979, 60:1-18.
56. Rähr H. The ultrastructure of the blood vessels of Branchiostoma lanceolatum (Pallas) (Cephalochordata). I. Relations between blood vessels, epithelia, basal laminae, and "conective tissue". Zoomorphology 1981, 97:53-74.
57. Randall D.J., Davie P.S. The hearts of urochordates and cephalochordates. Hearts and Heart-Like Organs 1980, 41-59. Academic Press, New York. G.H. Bourne (Ed.).
58. Rhodes C.P., Ratcliffe N.A., Rowley A.F. Presence of coelomocytes in the primitive chordate amphioxus (Branchiostoma lanceolatum). Science 1982, 217:263-265.
59. Robin C., Ottersbach K., de Bruijn M., Ma X., van der Horn K., Dzierzak E. Developmental origins of hematopoietic stem cells. Oncol. Res. 2003, 13:315-321.
60. Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012, 61:539-542.
61. Ruppert E.E. Cephalochordata (Acrania). Microscopic Anatomy of Invertebrates 1997, 349-504. Wiley Liss, New York. F.W. Harrison, E.E. Ruppert (Eds.).
62. Ruppert E.E., Carle K.J. Morphology of metazoan circulatory systems. Zoomorphology 1983, 103:193-208.
63. Schubert M., Holland N.D., Laudet V., Holland L.Z. A retinoic acid-Hox hierarchy controls both anterior/posterior patterning and neuronal specification in the developing central nervous system of the cephalochordate amphioxus. Dev. Biol. 2006, 296:190-202.
64. Shalaby F., Rossant J., Yamaguchi T.P., Gertsenstein M., Wu X.-F., Breitman M.L., Schuh A.C. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995, 376:62-66.
65. Shubin N., Tabin C., Carroll S. Deep homology and the origins of evolutionary novelty. Nature 2009, 457:818-823.
66. Simões-Costa M.S., Vasconcelos M., Sampaio A.C., Cravo R.M., Linhares V.L., Hochgreb T., Yan C.Y., Davidson B., Xavier-Neto J. The evolutionary origin of cardiac chambers. Dev. Biol. 2005, 277:1-15.
67. Somorjai I.M.L., Bertrand S., Camasses A., Haguenauer A., Escriva H. Evidence for stasis and not genetic piracy in developmental expression patterns of Branchiostoma lanceolatum and Branchiostoma floridae, two amphioxus species that have evolved independently over the course of 200Myr. Dev. Genes Evol. 2008, 218:703-713.
68. Somorjai I.M.L., Somorjai R.L., Garcia-Fernàndez J., Escriva H. Vertebrate-like regeneration in the invertebrate chordate amphioxus. Proc. Nat. Acad. Sci. U.S.A. 2012, 109:517-522.
69. Stach T. Coelomic cavities may function as a vascular system in amphioxus larvae. Biol. Bull. 1998, 195:260-263.
70. Stolfi A., Gainous T.B., Young J.J., Mori A., Levine M., Christiaen L. Early chordate origins of the vertebrate second heart field. Science 2010, 329:565-568.
71. Szatmari I., Iacovino M., Kyba M. The retinoid signaling pathway inhibits hematopoiesis and uncouples from the Hox genes during hematopoietic development. Stem Cells 2010, 28:1518-1529.
72. van Eekelen J.A., Bradley C.K., Göthert J.R., Robb L., Elefanty A.G., Begley C.G., Harvey A.R. Expression pattern of the stem cell leukaemia gene in the CNS of the embryonic and adult mouse. Neuroscience 2003, 122:421-436.
73. van Wijhe J.W. On the anatomy of the larva of Amphioxus lanceolatus and the explanation of its assymetry. Proc. K. Ned. Akad. Wet. 1919, 21:1013-1023.
74. Xavier-Neto J., Castro R.A., Sampaio A.C., Azambuja A.P., Castillo H.A., Cravo R.M., Simões-Costa M.S. Parallel avenues in the evolution of hearts and pumping organs. Cell. Mol. Life Sci. 2007, 64:719-734.
75. Xavier-Neto J., Davidson B., Simoes-Costa M.S., Castro R.A., Castillo H.A., Sampaio A.C., Azambuja A.P. Chapter 1.1-evolutionary origins of hearts. Heart Development and Regeneration 2010, 3-45. Academic Press, Boston. R. Nadia, P.H. Richard (Eds.).
76. Yamaguchi T.P., Dumont D.J., Conlon R.A., Breitman M.L., Rossant J. flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development 1993, 118:489-498.