Chicken embryos share mammalian patterns of apoptosis in the posterior placodal area

Abstract

In the posterior placodal area (PPA) of C57BL/6N mice and primate‐related Tupaia belangeri (Scandentia), apoptosis helps to establish morphologically separated otic and epibranchial placodes. Here, we demonstrate that basically identical patterns of apoptosis pass rostrocaudally through the Pax2+ PPA of chicken embryos. Interplacodal apoptosis eliminates unneeded cells either between the otic anlage and the epibranchial placodes 1, 2 and/or 3, respectively (type A), or between neighbouring epibranchial placodes (type B). These observations support the idea that in chicken embryos, as in mammals, interplacodal apoptosis serves to remove vestigial lateral line placodes (Washausen & Knabe, 2018, Biol Open 7, bio031815). A special case represents the recently discovered Pax2−/Sox2+ paratympanic organ (PTO) placode that has been postulated to be molecularly distinct from and developmentally independent of the ventrally adjacent first epibranchial (or ‘geniculate’) placode (O'Neill et al. 2012, Nat Commun 3, 1041). We show that Sox2+ (PTO placodal) cells seem to segregate from the Pax2+ geniculate placode, and that absence of Pax2 in the mature PTO placode is due to secondary loss. We further report that, between Hamburger–Hamilton (HH) stages HH14 and HH26, apoptosis in the combined anlage of the first epibranchial and PTO placodes is almost exclusively found within and/or immediately adjacent to the dorsally located PTO placode. Hence, apoptosis appears to support decision‐making processes among precursor cells of the early developing PTO placode and, later, regression of the epibranchial placodes 2 and 3.

Responses of Epibranchial Placodes to Disruptions of the FGF and BMP Signaling Pathways in Embryonic Mice

“…They are excellent objects for basic research in developmental biology. This applies first of all to the question to which extent genetic patterning mechanisms, migratory activities and programmed cell death help to transform the “panplacodal primordium” into individual patch-like thickened placodes ( Washausen et al, 2005 ; Schlosser, 2010 ; Washausen and Knabe, 2013 , 2019 ; Breau and Schneider-Maunoury, 2014 ; Thiery et al, 2020 ). Unanswered questions also concern the developmental potential of the panplacodal primordium in different vertebrate classes.…”

Patterns of senescence and apoptosis during development of branchial arches, epibranchial placodes, and pharyngeal pouches

“…[3][4][5][6][7][8][9][10][11][13][14][15][16][17][18][19][20][21][22] Second, through extensive preliminary work on the patterns and functions of apoptosis relevant to branchial and epibranchial development in mouse, chicken, and the primate-related tree shrew (Tupaia belangeri, Scandentia), we have established a satisfactory basis for follow-up studies of cellular senescence in a well-defined biological context. [23][24][25][26][27][28] Third, and finally, the incompletely understood functions of apoptosis during branchial and epibranchial development may be better elucidated by analyzing concurrent senescence events.…”

“…Here, we refer to the apoptosis that, in mouse embryos, chisels out the facial (geniculate), glossopharyngeal (petrosal), and vagal (nodose) epibranchial placodes from the posterior subdivision of the panplacodal primordium on each side of the body. [23][24][25][26][27] In mice, apoptosis on this occasion eliminates the anlagen of lateral line sensory organs that detect water movement in anamniotes. 26 Third, we investigated to what extent apoptosis and/or senescence might play a role in the remodeling of the three epibranchial placodes.…”

“…To date, transient accumulations of senescent cells during vertebrate development have been found in the placenta, preimplantation embryos, cement gland, nose, eye, branchial arches, oral cavity, dental pulp stem cells, stomach, intestine, fusing neural tube, hindbrain, spinal cord, notochord, heart, lung, pronephros, mesonephros, inner ear, fusing sternum midline, apical ectodermal ridge, interdigital tissue, and distal tip of the mouse tail 3‐11,13‐22 . Second, through extensive preliminary work on the patterns and functions of apoptosis relevant to branchial and epibranchial development in mouse, chicken, and the primate‐related tree shrew ( Tupaia belangeri , Scandentia), we have established a satisfactory basis for follow‐up studies of cellular senescence in a well‐defined biological context 23‐28 . Third, and finally, the incompletely understood functions of apoptosis during branchial and epibranchial development may be better elucidated by analyzing concurrent senescence events.…”

“…Second, we sought to determine the temporal, spatial (and possibly functional) contributions of senescence events in the context of previously published “interplacodal” apoptotic events. Here, we refer to the apoptosis that, in mouse embryos, chisels out the facial (geniculate), glossopharyngeal (petrosal), and vagal (nodose) epibranchial placodes from the posterior subdivision of the panplacodal primordium on each side of the body 23‐27 . In mice, apoptosis on this occasion eliminates the anlagen of lateral line sensory organs that detect water movement in anamniotes 26 …”