Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation.
Embryonic morphogenesis is accomplished by cellular movements, rearrangements, and cell fate inductions. Vertebrate gastrulation entails morphogenetic processes that generate three germ layers, endoderm, mesoderm, and ectoderm, shaped into head, trunk, and tail. To understand how cell migration mechanistically contributes to tissue shaping during gastrulation, we examined migration of lateral mesoderm in the zebrafish. Our results illustrate that cell behaviors, different from mediolaterally oriented cell intercalation, also promote convergence and extension (C&E). During early gastrulation, upon internalization, individually migrating mesendodermal cells contribute to the elongation of the mesoderm by moving animally, without dorsal movement. Convergence toward dorsal starts later, by 70% epiboly (7.7 hpf). Depending on location along the Animal-Vegetal axis, an animal or vegetal bias is added to the dorsalward movement, so that paths fan out and the lateral mesoderm both converges and extends. Onset of convergence is independent of noncanonical Wnt signaling but is delayed when Stat3 signaling is compromised. To understand which aspects of motility are controlled by guidance cues, we measured turning behavior of lateral mesodermal cells. We show that cells exhibit directional preference, directionally-regulated speed, and turn toward dorsal when off-course. We estimate that ectoderm could supply from a fraction to all the dorsalward displacement seen in mesoderm cells. Using mathematical modeling, we demonstrate that directional preference is sufficient to account for mesoderm convergence and extension, and that, at minimum, two sources of guidance cues could orient cell paths realistically if located in the dorsal midline.
Sepich
Diane S
DS
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235-1634, USA. diane.s.sepich@vanderbilt.edu
Calmelet
Colette
C
Kiskowski
Maria
M
Solnica-Krezel
Lila
L
D000818:Animals; D002465:Cell Movement; D002630:Chemotactic Factors / Q000737:chemistry; D002633:Chemotaxis; D004475:Ectoderm / Q000378:metabolism; D004707:Endoderm / Q000378:metabolism; D005775:Gastrula / Q000378:metabolism / Q000473:pathology*; D005786:Gene Expression Regulation; D008648:Mesoderm / Q000378:metabolism / Q000473:pathology*; D008954:Models, Biological; D008957:Models, Genetic; D009068:Movement; D050796:STAT3 Transcription Factor / Q000378:metabolism; D015398:Signal Transduction; D013997:Time Factors; D051153:Wnt Proteins / Q000378:metabolism; D060508:Wnt3 Protein; D015027:Zebrafish
D002630:Chemotactic Factors; D050796:STAT3 Transcription Factor; D051153:Wnt Proteins; D060508:Wnt3 Protein