Table 2.
Fluorescent reporters for monitoring Autophagy in C. elegans
| Protein | Function | Tissue Expression¥ | TransgenesΦ | References |
|---|---|---|---|---|
| LGG-1 | Microtubule – associated protein-1/Ubiquitin-like protein | Intestine, Hypodermis, Muscle, Pharynx, Neurons, Vulva, Somatic Gonad, Germline | adIs2122[Plgg-1::GFP::LGG-1; rol-6(su1006)] izEx1[Plgg-1::GFP::LGG-1; rol-6(su1006)] izEx5[Plgg-1::GFP::LGG-1; Podr-1::RFP] vkEx1093[Pnhx-2::mCherry::LGG-1] dkIs399[Ppie-1::GFP::lgg-1, unc-119 (+)] Is(Ppie-1::GFP::mCherry::LGG-1; unc-119(+)) Ex[Plgg-1::DsRED::LGG-1; Pmyo-2::GFP] | (Melendez et al. 2003; Kang et al. 2007; Samara et al. 2008; Gosai et al. 2010; Manil-Segalen et al. 2014) |
| LGG-2 | Ubiquitin-like protein | Hypodermis, Intestine, Vulva, Pharynx, Neurons, Muscle | RD108 Ex[Plgg-2::GFP::LGG-2; rol-6(su1006)] RD217 unc119(ed3)III; Ex[unc-119(+); Ppie-1::gfp::mcherry::lgg-1] VIG9 unc119(ed3)III; Is[unc-119(+); Plgg-2::gfp::lgg-2] | (Alberti et al. 2010; Manil-Segalen et al. 2014) |
| DFCP1 | Double FYVE-Containing Protein | Head, Tail, Vulva, Neurons | bpIs168[Pnfya-1::DFCP1::GFP; unc-76(+)] | (Derubeis et al. 2000; Cheung et al. 2001; Axe et al. 2008; Tian et al. 2010) |
| ATG-16.1 | WD repeat-containing protein | Intestine, Head, Pharynx, Muscle, Neurons | [Patg-16.1::ATG-16.1::GFP; rol-6(su10006)] | (Zhang et al. 2013) |
| ATG-16.2 | WD repeat-containing protein | Intestine, Head, Pharynx, Muscle, Neurons | [Patg-16.2::ATG-16.2::GFP; rol-6(su10006)] | (Zhang et al. 2013) |
| ATG-9 | Integral Membrane Protein | Head, Tail, Vulva, Neurons | bpIs211[Pnfya-1::ATG-9::GFP; unc-76(+)] | (Noda et al. 2000; Lu et al. 2011; Liang et al. 2012; Lin et al. 2013) |
| EPG-1 | Atg13 homolog | Neurons, Pharynx, Muscle | bpIs175[Pepg-1::EPG-1::GFP; rol-6(su1006)] | (Tian et al. 2009) |
| EPG-9 | Atg101 homolog | Intestine, Pharynx, Neurons | bpIs214[Pepg-9::EPG-9::GFP; unc-76(+)] | (Liang et al. 2012) |
| BEC-1 | Coiled-Coil protein | Intestine, Hypodermis, Vulva, Neurons, Somatic Gonad | swEx520 [Pbec-1::BEC-1::GFP; rol-6(su1006)] grEx129[Pbec-1::BEC-1::mRFP; lin-15(+)] Ex[Pced-1::mCherry::BEC-1; rol-6(su1006)] Ex[Pegl1-::mCherry::BEC-1; rol-6(su1006)] | (Takacs-Vellai et al. 2005; Rowland et al. 2006; Ruck et al. 2011; Huang et al. 2012) |
| SQST-1 | p62/Autophagy adaptor protein | Hypodermis, Neurons, Intestine, Vulva, Muscle | bpIs151[Psqst-1::SQST-1::GFP; unc-76(+)] | (Hunt-Newbury et al. 2007; Pankiv et al. 2007; Tian et al. 2010) |
| SEPA-1 | Autophagy adaptor protein | Intestine, Head, Tail | bpIs131[Psepa-1::SEPA-1::GFP; unc-76(+)] | (Zhang et al. 2009; Tian et al. 2010) |
| PGL-1 | RNA-binding protein/P-granule component | P-granules, Intestine | bnIs1[Ppie-1::GFP::PGL-1; unc-119(+)] bnIs26[Pelt-2::PGL-1::GFP; Pmyo-2::mCherry] | (Cheeks et al. 2004; Zhang et al. 2009; Updike et al. 2011) |
Tissue expression may vary depending on the specific promoter used
Transgenes shown are those found in autophagy studies or those which may be beneficial in autophagy studies; Additional transgenes may be available for each gene
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Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT. 2008. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. The Journal of cell biology 182: 685–701.
Cheeks RJ, Canman JC, Gabriel WN, Meyer N, Strome S, Goldstein B. 2004. C. elegans PAR proteins function by mobilizing and stabilizing asymmetrically localized protein complexes. Current biology : CB 14: 851–862.
Cheung PC, Trinkle-Mulcahy L, Cohen P, Lucocq JM. 2001. Characterization of a novel phosphatidylinositol 3-phosphate-binding protein containing two FYVE fingers in tandem that is targeted to the Golgi. The Biochemical journal 355: 113–121.
Derubeis AR, Young MF, Jia L, Robey PG, Fisher LW. 2000. Double FYVE-containing protein 1 (DFCP1): isolation, cloning and characterization of a novel FYVE finger protein from a human bone marrow cDNA library. Gene 255: 195–203.
Gosai SJ, Kwak JH, Luke CJ, Long OS, King DE, Kovatch KJ, Johnston PA, Shun TY, Lazo JS, Perlmutter DH et al. 2010. Automated high-content live animal drug screening using C. elegans expressing the aggregation prone serpin alpha1-antitrypsin Z. PloS one 5: e15460.
Huang S, Jia K, Wang Y, Zhou Z, Levine B. 2012. Autophagy genes function in apoptotic cell corpse clearance during C. elegans embryonic development. Autophagy 9.
Hunt-Newbury R, Viveiros R, Johnsen R, Mah A, Anastas D, Fang L, Halfnight E, Lee D, Lin J, Lorch A et al. 2007. High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS biology 5: e237.
Kang C, You YJ, Avery L. 2007. Dual roles of autophagy in the survival of Caenorhabditis elegans during starvation. Genes & development 21: 2161–2171.
Liang Q, Yang P, Tian E, Han J, Zhang H. 2012. The C. elegans ATG101 homolog EPG-9 directly interacts with EPG-1/Atg13 and is essential for autophagy. Autophagy 8: 1426–1433.
Lin L, Yang P, Huang X, Zhang H, Lu Q, Zhang H. 2013. The scaffold protein EPG-7 links cargo-receptor complexes with the autophagic assembly machinery. The Journal of cell biology 201: 113–129.
Lu Q, Yang P, Huang X, Hu W, Guo B, Wu F, Lin L, Kovacs AL, Yu L, Zhang H. 2011. The WD40 repeat PtdIns(3)P-binding protein EPG-6 regulates progression of omegasomes to autophagosomes. Developmental cell 21: 343–357.
Manil-Segalen M, Lefebvre C, Jenzer C, Trichet M, Boulogne C, Satiat-Jeunemaitre B, Legouis R. 2014. The C. elegans LC3 acts downstream of GABARAP to degrade autophagosomes by interacting with the HOPS subunit VPS39. Developmental cell 28: 43–55.
Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B. 2003. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301: 1387–1391.
Noda T, Kim J, Huang WP, Baba M, Tokunaga C, Ohsumi Y, Klionsky DJ. 2000. Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. Journal of Cell Biology 148: 465–480.
Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T. 2007. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. The Journal of biological chemistry 282: 24131–24145.
Rowland AM, Richmond JE, Olsen JG, Hall DH, Bamber BA. 2006. Presynaptic terminals independently regulate synaptic clustering and autophagy of GABAA receptors in Caenorhabditis elegans. The Journal of neuroscience : the official journal of the Society for Neuroscience 26: 1711–1720.
Ruck A, Attonito J, Garces KT, Nunez L, Palmisano NJ, Rubel Z, Bai Z, Nguyen KC, Sun L, Grant BD et al. 2011. The Atg6/Vps30/Beclin1 ortholog BEC-1 mediates endocytic retrograde transport in addition to autophagy in C. elegans. Autophagy 7.
Samara C, Syntichaki P, Tavernarakis N. 2008. Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell death and differentiation 15: 105–112.
Takacs-Vellai K, Vellai T, Puoti A, Passannante M, Wicky C, Streit A, Kovacs AL, Muller F. 2005. Inactivation of the autophagy gene bec-1 triggers apoptotic cell death in C. elegans. Current biology : CB 15: 1513–1517.
Tian E, Wang F, Han Ja, Zhang H. 2009. epg-1 functions in autophagy-regulated processes and may encode a highly divergent Atg13 homolog in C. elegans. Autophagy 5: 608–615.
Tian Y, Li Z, Hu W, Ren H, Tian E, Zhao Y, Lu Q, Huang X, Yang P, Li X et al. 2010. C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell 141: 1042–1055.
Updike DL, Hachey SJ, Kreher J, Strome S. 2011. P granules extend the nuclear pore complex environment in the C. elegans germ line. The Journal of cell biology 192: 939–948.
Zhang H, Wu F, Wang X, Du H, Wang X, Zhang H. 2013. The two C. elegans ATG-16 homologs have partially redundant functions in the basal autophagy pathway. Autophagy 9: 1965–1974.
Zhang Y, Yan L, Zhou Z, Yang P, Tian E, Zhang K, Zhao Y, Li Z, Song B, Han J et al. 2009. SEPA-1 mediates the specific recognition and degradation of P granule components by autophagy in C. elegans. Cell 136: 308–321.