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Establishment and maintenance of compartmental boundaries: role of contractile actomyosin barriers

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Abstract

During animal development, tissues and organs are partitioned into compartments that do not intermix. This organizing principle is essential for correct tissue morphogenesis. Given that cell sorting defects during compartmentalization in humans are thought to cause malignant invasion and congenital defects such as cranio-fronto-nasal syndrome, identifying the molecular and cellular mechanisms that keep cells apart at boundaries between compartments is important. In both vertebrates and invertebrates, transcription factors and short-range signalling pathways, such as EPH/Ephrin, Hedgehog, or Notch signalling, govern compartmental cell sorting. However, the mechanisms that mediate cell sorting downstream of these factors have remained elusive for decades. Here, we review recent data gathered in Drosophila that suggest that the generation of cortical tensile forces at compartmental boundaries by the actomyosin cytoskeleton could be a general mechanism that inhibits cell mixing between compartments.

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Fig. 1a, b
Fig. 2a–b′
Fig. 3a, b
Fig. 4a–d

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Abbreviations

AEL:

After egg laying

A/P:

Anterior-posterior

Cad99C :

Cadherin 99C

CALI:

Chromophore-assisted laser inactivation

DAH:

Differential adhesion hypothesis

Dpp:

Decapentaplegic

D/V:

Dorsal-ventral

F-actin:

Filamentous actin

Hh:

Hedgehog

LRR:

Leucine rich repeat

L2:

Second instar larva

L3:

Third instar larva

MHC:

Myosin II Heavy Chain

MRLC:

Myosin II Regulatory Light Chain

MyoII:

Nonmuscle Myosin II

Omb:

Optomotor-blind

sqh :

spaghetti-squash

Wg:

Wingless

zip :

zipper

ZLI:

Zona limitans intrathalamica

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Acknowledgments

This work has been supported by ARC (Association pour la Recherche contre le Cancer) and Herchel Smith fellowships to B.M., by an EMBO fellowship to A.P.-M. and by HSFP and Wellcome Trust grants to B.S. A.P.-M. would like to thank Andrea Brand for her support.

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  1. Bruno Monier & Anne Pélissier-Monier

    Present address: Institut de Biologie du Développement de Marseille-Luminy, UMR6216, Campus de Luminy, Case 907, 13288, Marseille cedex 9, France

Authors and Affiliations

  1. Department of Physiology, Development and Neuroscience, Anatomy Building, Downing Street, Cambridge, CB2 3DY, UK

    Bruno Monier, Anne Pélissier-Monier & Bénédicte Sanson

  2. Wellcome Trust, Cancer Research UK Gurdon Institute, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QN, UK

    Anne Pélissier-Monier

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Supplementary Figure S1: Mechanisms that could implement cell sorting at compartmental boundaries

. a Differential adhesion: based on the analogy that liquids such as oil and water are immiscible due to distinct surface tension, it has been suggested that dissociated cells of distinct identities could sort according to their surface tension [1, 2]. It has been proposed that differential surface tension could be conferred by distinct adhesion molecules or by different levels of the same adhesion molecule. This hypothesis was validated in vitro by varying the levels or the nature of cadherins transfected in cultured cells [3]. This theory has been extrapolated to compartmental cell sorting [4–7]: here, the two cell populations express two distinct adhesion molecules: red and blue, respectively. However, one might note that additional parameters might come in the interplay to produce surface tension. In particular, surface tension probably relies on a balance between adhesion at the plasma membrane and contractibility at the cell cortex [8]. In other words, differential expression of adhesion molecules might not be the only strategy to produce differential surface tension between two groups of cells. b Extracellular matrix fence: in a tissue, two compartments could be kept separated by a groove filled with extracellular matrix that would act as a physical fence. c Nonproliferative zone: in a mitotically active epithelium, division of boundary cells could lead to an irregular boundary between two compartments. Inhibition of cell division a few rows of cells on each side of the compartmental boundary could prevent the boundary from being challenged, and thus maintain stable compartmentalization. In the Drosophila wing disc, Notch and Wingless signalling inhibits cell division close to the D/V boundary [9, 10]. d Local orientation of cell division axis: alternatively to c, the mitotic spindle of dividing boundary cells could be oriented so that boundary cells would divide parallel to the boundary. In this case, the progeny of dividing boundary cells would never be found in the opposite compartment, thereby preventing cell mixing. (TIFF 5778 kb)

Supplementary Figure S2: Cell behavior at morphogen-dependent boundaries.

a Compartmentalization can be maintained by morphogen-dependent boundaries. Cell identity (blue) relies on reception of a given morphogen (green), and it changes when cells move too far away from the morphogen source. Stable compartmentalization maintained by morphogen-dependent boundaries does not involve physical segregation of cells. An example of morphogen-dependent boundary can be found in the Drosophila wing disc where the wing/notum boundary relies on reception of EGF signalling [11]. b In the Drosophila embryo at stages 8–11, anterior and posterior compartments are separated by parasegmental boundaries and by posterior-anterior (P-A) boundaries. P-A boundaries, at the level of which the segmental grooves will develop after stage 12, are morphogen-dependent boundaries: engrailed expression in posterior cells relies on reception of the Wingless morphogen secreted by cells of the anterior compartment that face the parasegmental boundary [12–15]. (TIFF 1752 kb)

Supplementary Figure S3: A narrow nonproliferative zone at the

Drosophilawing disc A/P boundary? Schematization of the pattern of cell proliferation at boundaries in the Drosophila wing pouch showing the broad nonproliferative zone at the D/V boundary. A nonproliferative zone, although narrow, could also form at the A/P boundary in late third instar wing discs. The color-code is similar to the one used in figure 1, green indicates BrdU-positive cells of unknown identity. Schematization is based on the pattern of BrdU incorporation reported in Figure 1b of Johnston and Edgar (1998) [10]. A similar pattern was also reported in Figure 2A of Herranz and coworkers (2008) [9]. In the initial analysis by O’Brochta and Bryant (1985) [16], a nonproliferative zone was not identified at the A/P boundary. High resolution images of the pattern of BrdU incorporation in the more recent reports suggest that such a nonproliferative zone might exist at the A/P boundary after all, although its presence is not discussed by the authors [9, 10]. Additional experiments are required to clarify this situation. (TIFF 721 kb)

Supplementary Figure S4: Influence of the pattern of Myosin II activation upon groove formation.

Top views (top) and cross-section (bottom) of the eye disc epithelium (left) and of the embryonic epithelium (right) showing the pattern of Myosin II activation (green) and the shape of the associated groove. (TIFF 2427 kb)

Supplementary material 5 (DOC 29 kb)

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Monier, B., Pélissier-Monier, A. & Sanson, B. Establishment and maintenance of compartmental boundaries: role of contractile actomyosin barriers. Cell. Mol. Life Sci. 68, 1897–1910 (2011). https://doi.org/10.1007/s00018-011-0668-8

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