Diving into the Evolutionary History of HSC70-Linked Selective Autophagy Pathways: Endosomal Microautophagy and Chaperone-Mediated Autophagy

Overview

Journal Cells

Publisher MDPI

Specialties Biochemistry
Biophysics
Cell Biology
Molecular Biology

Date 2022 Jun 24

PMID 35741074

Authors

Simon Schnebert

Maxime Goguet

Emilio J Velez

Alexandra Depince

Florian Beaumatin

Amaury Herpin

Iban Seiliez

Affiliations

Soon will be listed here.

Abstract

Autophagy is a pleiotropic and evolutionarily conserved process in eukaryotes that encompasses different types of mechanisms by which cells deliver cytoplasmic constituents to the lysosome for degradation. Interestingly, in mammals, two different and specialized autophagic pathways, (i) the chaperone-mediated autophagy (CMA) and (ii) the endosomal microautophagy (eMI), both rely on the use of the same cytosolic chaperone HSPA8 (also known as HSC70) for targeting specific substrates to the lysosome. However, this is not true for all organisms, and differences exist between species with respect to the coexistence of these two autophagic routes. In this paper, we present an in-depth analysis of the evolutionary history of the main components of CMA and eMI and discuss how the observed discrepancies between species may contribute to improving our knowledge of these two functions and their interplays.

Citing Articles

Selective protein degradation through chaperone‑mediated autophagy: Implications for cellular homeostasis and disease (Review).

Huang J, Wang J Mol Med Rep. 2024; 31(1).

PMID: 39513615 PMC: 11542157. DOI: 10.3892/mmr.2024.13378.

The Antipsychotic Drug Aripiprazole Suppresses Colorectal Cancer by Targeting LAMP2a to Induce RNH1/miR-99a/mTOR-Mediated Autophagy and Apoptosis.

Hu H, Fu J, Han L, Gao G, Zhang W, Yu S Adv Sci (Weinh). 2024; 11(48):e2409498.

PMID: 39513392 PMC: 11672294. DOI: 10.1002/advs.202409498.

Mechanism and complex roles of HSC70/HSPA8 in viral entry.

Chen Q, Chen Y, Bao C, Xiang H, Gao Q, Mao L Virus Res. 2024; 347:199433.

PMID: 38992806 PMC: 11305274. DOI: 10.1016/j.virusres.2024.199433.

Autophagy: a necessary evil in cancer and inflammation.

Mathur A, Ritu , Chandra P, Das A 3 Biotech. 2024; 14(3):87.

PMID: 38390576 PMC: 10879063. DOI: 10.1007/s13205-023-03864-w.

Is Autophagy a Prerequisite for Steroidogenesis in Leydig Cells?.

Park J, Kim Y, Kim J Dev Reprod. 2023; 27(3):149-157.

PMID: 38074457 PMC: 10703103. DOI: 10.12717/DR.2023.27.3.149.

References

Leung K, Dacks J, Field M . Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic. 2008; 9(10):1698-716. DOI: 10.1111/j.1600-0854.2008.00797.x. View

Harter C, Mellman I . Transport of the lysosomal membrane glycoprotein lgp120 (lgp-A) to lysosomes does not require appearance on the plasma membrane. J Cell Biol. 1992; 117(2):311-25. PMC: 2289424. DOI: 10.1083/jcb.117.2.311. View

Gough N, Hatem C, Fambrough D . The family of LAMP-2 proteins arises by alternative splicing from a single gene: characterization of the avian LAMP-2 gene and identification of mammalian homologs of LAMP-2b and LAMP-2c. DNA Cell Biol. 1995; 14(10):863-7. DOI: 10.1089/dna.1995.14.863. View

Guarnieri F, Arterburn L, Penno M, Cha Y, August J . The motif Tyr-X-X-hydrophobic residue mediates lysosomal membrane targeting of lysosome-associated membrane protein 1. J Biol Chem. 1993; 268(3):1941-6. View

Liao Y, Tang L . The critical roles of HSC70 in physiological and pathological processes. Curr Pharm Des. 2013; 20(1):101-7. DOI: 10.2174/13816128113199990585. View

Tekirdag K, Cuervo A . Chaperone-mediated autophagy and endosomal microautophagy: Joint by a chaperone. J Biol Chem. 2017; 293(15):5414-5424. PMC: 5900761. DOI: 10.1074/jbc.R117.818237. View

Ikami Y, Terasawa K, Sakamoto K, Ohtake K, Harada H, Watabe T . The two-domain architecture of LAMP2A regulates its interaction with Hsc70. Exp Cell Res. 2021; 411(1):112986. DOI: 10.1016/j.yexcr.2021.112986. View

Mukherjee A, Patel B, Koga H, Cuervo A, Jenny A . Selective endosomal microautophagy is starvation-inducible in Drosophila. Autophagy. 2016; 12(11):1984-1999. PMC: 5103356. DOI: 10.1080/15548627.2016.1208887. View

Krenek S, Schlegel M, Berendonk T . Convergent evolution of heat-inducibility during subfunctionalization of the Hsp70 gene family. BMC Evol Biol. 2013; 13:49. PMC: 3606833. DOI: 10.1186/1471-2148-13-49. View

10.

Bonhoure A, Vallentin A, Martin M, Senff-Ribeiro A, Amson R, Telerman A . Acetylation of translationally controlled tumor protein promotes its degradation through chaperone-mediated autophagy. Eur J Cell Biol. 2017; 96(2):83-98. DOI: 10.1016/j.ejcb.2016.12.002. View

11.

Ravi V, Venkatesh B . The Divergent Genomes of Teleosts. Annu Rev Anim Biosci. 2018; 6:47-68. DOI: 10.1146/annurev-animal-030117-014821. View

12.

Tuttle D, Lewin A, Dunn Jr W . Selective autophagy of peroxisomes in methylotrophic yeasts. Eur J Cell Biol. 1993; 60(2):283-90. View

13.

Marzella L, Ahlberg J, Glaumann H . Autophagy, heterophagy, microautophagy and crinophagy as the means for intracellular degradation. Virchows Arch B Cell Pathol Incl Mol Pathol. 1981; 36(2-3):219-34. DOI: 10.1007/BF02912068. View

14.

Pan Z, Zhang Z, Zhuo L, Wan T, Li Y . Bioinformatic and Functional Characterization of Hsp70s in Myxococcus xanthus. mSphere. 2021; 6(3). PMC: 8265645. DOI: 10.1128/mSphere.00305-21. View

15.

Fujiwara Y, Furuta A, Kikuchi H, Aizawa S, Hatanaka Y, Konya C . Discovery of a novel type of autophagy targeting RNA. Autophagy. 2013; 9(3):403-9. PMC: 3590259. DOI: 10.4161/auto.23002. View

16.

Schuck S, Gallagher C, Walter P . ER-phagy mediates selective degradation of endoplasmic reticulum independently of the core autophagy machinery. J Cell Sci. 2014; 127(Pt 18):4078-88. PMC: 4163648. DOI: 10.1242/jcs.154716. View

17.

Pasquier J, Cabau C, Nguyen T, Jouanno E, Severac D, Braasch I . Gene evolution and gene expression after whole genome duplication in fish: the PhyloFish database. BMC Genomics. 2016; 17:368. PMC: 4870732. DOI: 10.1186/s12864-016-2709-z. View

18.

Lescat L, Herpin A, Mourot B, Veron V, Guiguen Y, Bobe J . CMA restricted to mammals and birds: myth or reality?. Autophagy. 2018; 14(7):1267-1270. PMC: 6103740. DOI: 10.1080/15548627.2018.1460021. View

19.

Nikolaidis N, Nei M . Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. Mol Biol Evol. 2003; 21(3):498-505. DOI: 10.1093/molbev/msh041. View

20.

Lindquist S, Craig E . The heat-shock proteins. Annu Rev Genet. 1988; 22:631-77. DOI: 10.1146/annurev.ge.22.120188.003215. View