PAR-3 mediates the initial clustering and apical localization of junction and polarity proteins during<i>C. elegans</i>intestinal epithelial cell polarization

Achilleos, Annita; Wehman, Ann M.; Nance, Jeremy

doi:10.1242/dev.047647

Cited by 113 publications

(133 citation statements)

References 56 publications

(74 reference statements)

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“…The arcade cell epithelium forms extremely quickly, in less than ten minutes (Portereiko and Mango, 2001). Therefore, we chose to focus on the well-described initiation of polarity of the intestine and epidermis, which occurs more slowly and allows intermediate stages to be visualized (Achilleos et al, 2010; Leung et al, 1999; Podbilewicz and White, 1994; Totong et al, 2007). …”

Section: Resultsmentioning

confidence: 99%

PAR-6, but not E-cadherin and β-integrin, is necessary for epithelial polarization in C. elegans

Stetina

Mango

2015

Developmental Biology

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Cell polarity is a fundamental characteristic of epithelial cells. Classical cell biological studies have suggested that establishment and orientation of polarized epithelia depend on outside-in cues that derive from interactions with either neighboring cells or the substratum (Akhtar and Streuli, 2013; Chen and Zhang, 2013; Chung and Andrew, 2008; McNeill et al., 1990; Nejsum and Nelson, 2007; Nelson et al., 2013; Ojakian and Schwimmer, 1994; Wang et al., 1990; Yu et al., 2005). This paradigm has been challenged by examples of epithelia generated in the absence of molecules that mediate cell-cell or cell-matrix interactions, notably E-cadherin and integrins (Baas et al., 2004; Choi et al., 2013; Costa et al., 1998; Harris and Peifer, 2004; Raich et al., 1999; Roote and Zusman, 1995; Vestweber et al., 1985; Williams and Waterston, 1994; Wu et al., 2009). Here we explore an alternative hypothesis, that cadherins and integrins function redundantly to substitute for one another during epithelium formation (Martinez-Rico et al., 2010; Ojakian et al., 2001; Rudkouskaya et al., 2014; Weber et al., 2011). We use C. elegans, which possesses a single E-cadherin (Costa et al., 1998; Hardin et al., 2013; Tepass, 1999) and a single β-integrin (Gettner et al., 1995; Lee et al., 2001), and analyze the arcade cells, which generate an epithelium late in embryogenesis (Portereiko and Mango, 2001; Portereiko et al., 2004), after most maternal factors are depleted. Loss of E-cadherinHMR-1 in combination with β-integrinPAT-3 had no impact on the onset or formation of the arcade cell epithelium, nor the epidermis or digestive tract. Moreover, β-integrinPAT-3 was not enriched at the basal surface of arcades, and the candidate PAT-3 binding partner β-lamininLAM-1 was not detected until after arcade cell polarity was established and exhibited no obvious polarity defect when mutated. Instead, the polarity protein par-6 (Chen and Zhang, 2013; Watts et al., 1996) was required to polarize the arcade cells, and par-6 mutants exhibited mislocalized or absent apical and junctional proteins. We conclude that the arcade cell epithelium polarizes by a PAR-6-mediated pathway that is independent of E-cadherin, β-integrin and β-laminin.

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Section: Resultsmentioning

confidence: 99%

PAR-6, but not E-cadherin and β-integrin, is necessary for epithelial polarization in C. elegans

Stetina

Mango

2015

Developmental Biology

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“…Strains used in this study include GE24 [ pha-1(e2123) III ], WY847 [ pha-1(tm3671) III ; fdEx181 (pBX ( pha-1 –wild-type genomic locus); sur-5 :: GFP )], WY848 [ pha-1(tm3671) III ; fdEx182 (pBX; sur-5 :: GFP )], WY849 [ pha-1(tm3671) III ; fdEx183 (pBX; sur-5 :: GFP )], MH1384 [ kuIs46 (AJM-1:: GFP ; unc-119+ X )], MH1385 [ kuIs47 (AJM-1:: GFP ; unc-119+ II )], WY924 [ pha-1(tm3671) III ; kuIs47 II ; fdEx182 ], WY876 [ pha-1(tm3671) III , kuIs46 X ; fdEx182 ], SU159 [ ajm-1(ok160) ; jcEx44( AJM-1:: GFP) ], SM481 [ Is ( P pha-4 :: GFP -mem + pRF4)], WY871 [ pha-1(tm3671) III , Is ( P pha-4 :: GFP -mem + pRF4); fdEx182 ], WY872 [ pha-1(e2123) III , Is ( P pha-4 ::GFP-mem + pRF4); fdEx182 ], SU295 [ jcIs25 ( pPE103 (JAC-1::GFP); pRF4)] (Pettitt et al 2003), WY997 [ pha-1(tm3671) III ; jcIs25 ; fdEx182 ], FT250 [ unc-119(ed3) III ; xnIs96 ( pJN455 (HMR-1::GFP) + unc-119 +] (…”

Section: Methodsmentioning

confidence: 99%

Analysis of PHA-1 Reveals a Limited Role in Pharyngeal Development and Novel Functions in Other Tissues

2014

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PHA-1 encodes a cytoplasmic protein that is required for embryonic morphogenesis and attachment of the foregut (pharynx) to the mouth (buccal capsule). Previous reports have in some cases suggested that PHA-1 is essential for the differentiation of most or all pharyngeal cell types. By performing mosaic analysis with a recently acquired pha-1 null mutation (tm3671), we found that PHA-1 is not required within most or all pharyngeal cells for their proper specification, differentiation, or function. Rather, our evidence suggests that PHA-1 acts in the arcade or anterior epithelial cells of the pharynx to promote attachment of the pharynx to the future buccal capsule. In addition, PHA-1 appears to be required in the epidermis for embryonic morphogenesis, in the excretory system for osmoregulation, and in the somatic gonad for normal ovulation and fertility. PHA-1 activity is also required within at least a subset of intestinal cells for viability. To better understand the role of PHA-1 in the epidermis, we analyzed several apical junction markers in pha-1(tm3671) homozygous embryos. PHA-1 regulates the expression of several components of two apical junction complexes including AJM-1–DLG-1/discs large complex and the classical cadherin–catenin complex, which may account for the role of PHA-1 in embryonic morphogenesis.

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“…In the absence of PAR-3, intestinal HMR-1 is initially dispersed and mislocalized, whereas HMP-1 is still recruited into foci. Basolateral (as opposed to apical) foci of HMP-1 and DLG-1 accumulate, despite unperturbed localization of LET-413/Scribble, 54 which normally excludes AJ components from basolateral surfaces. 55,56 Similar localization defects are seen in the pharynx in par-3 mutants.…”

Section: Regulating the Classical CCC In C Elegansmentioning

confidence: 99%

“…55,56 Similar localization defects are seen in the pharynx in par-3 mutants. 54 Loss of PAR-6 prior to gastrulation results in elongation failure despite successful ventral enclosure. 57 The distribution of DLG-1, AJM-1, HMP-1, and HMR-1 is fragmentary, with the CCC being affected less severely.…”

Section: Regulating the Classical CCC In C Elegansmentioning

confidence: 99%

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Cadherins and Their Partners in the Nematode Worm Caenorhabditis elegans

Hardin

Lynch

Loveless

et al. 2013

Progress in Molecular Biology and Translational Science

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The extreme simplicity of Caenorhabditis elegans makes it an ideal system to study the basic principles of cadherin function at the level of single cells within the physiologically relevant context of a developing animal. The genetic tractability of C. elegans also means that components of cadherin complexes can be identified through genetic modifier screens, allowing a comprehensive in vivo characterization of the macromolecular assemblies involved in cadherin function during tissue formation and maintenance in C. elegans. This work shows that a single cadherin system, the classical cadherin–catenin complex, is essential for diverse morphogenetic events during embryogenesis through its interactions with a range of mostly conserved proteins that act to modulate its function. The role of other members of the cadherin family in C. elegans, including members of the Fat-like, Flamingo/CELSR and calsyntenin families is less well characterized, but they have clear roles in neuronal development and function.

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PAR-3 mediates the initial clustering and apical localization of junction and polarity proteins duringC. elegansintestinal epithelial cell polarization

Cited by 113 publications

References 56 publications

PAR-6, but not E-cadherin and β-integrin, is necessary for epithelial polarization in C. elegans

PAR-6, but not E-cadherin and β-integrin, is necessary for epithelial polarization in C. elegans

Analysis of PHA-1 Reveals a Limited Role in Pharyngeal Development and Novel Functions in Other Tissues

Cadherins and Their Partners in the Nematode Worm Caenorhabditis elegans

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