The conserved transmembrane protein TMEM-39 coordinates with COPII to promote collagen secretion and regulate ER stress response

English version

Autoři: Zhe Zhang ^aff001; Shuo Luo ^aff002; Guilherme Oliveira Barbosa ^aff002; Meirong Bai ^aff002; Thomas B. Kornberg ^aff002; Dengke K. Ma ^aff002
Působiště autorů: School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong University, Jinan, China ^aff001; Cardiovascular Research Institute, University of California San Francisco, San Francisco, California, United States of America ^aff002; Department of Biochemistry and Biophysics, University of California San Francisco, San Francisco, California, United States of America ^aff003; Department of Physiology, University of California San Francisco, San Francisco, California, United States of America ^aff004; Innovative Genomics Institute, Berkeley, California, United States of America ^aff005
Vyšlo v časopise: The conserved transmembrane protein TMEM-39 coordinates with COPII to promote collagen secretion and regulate ER stress response. PLoS Genet 17(2): e1009317. doi:10.1371/journal.pgen.1009317
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009317

Souhrn

Dysregulation of collagen production and secretion contributes to aging and tissue fibrosis of major organs. How procollagen proteins in the endoplasmic reticulum (ER) route as specialized cargos for secretion remains to be fully elucidated. Here, we report that TMEM39, an ER-localized transmembrane protein, regulates production and secretory cargo trafficking of procollagen. We identify the C. elegans ortholog TMEM-39 from an unbiased RNAi screen and show that deficiency of tmem-39 leads to striking defects in cuticle collagen production and constitutively high ER stress response. RNAi knockdown of the tmem-39 ortholog in Drosophila causes similar defects in collagen secretion from fat body cells. The cytosolic domain of human TMEM39A binds to Sec23A, a vesicle coat protein that drives collagen secretion and vesicular trafficking. TMEM-39 regulation of collagen secretion is independent of ER stress response and autophagy. We propose that the roles of TMEM-39 in collagen secretion and ER homeostasis are likely evolutionarily conserved.

Klíčová slova:

Caenorhabditis elegans – Collagens – Endoplasmic reticulum stress response – Fluorescence imaging – Monomers – Protein secretion – RNA interference – Secretion

Zdroje

1. Shoulders MD, Raines RT. Collagen structure and stability. Annu Rev Biochem. 2009;78:929–58. doi: 10.1146/annurev.biochem.77.032207.120833 19344236

2. Humphreys BD. Mechanisms of Renal Fibrosis. Annu Rev Physiol. 2018;80:309–26. doi: 10.1146/annurev-physiol-022516-034227 29068765

3. McKleroy W, Lee TH, Atabai K. Always cleave up your mess: targeting collagen degradation to treat tissue fibrosis. Am J Physiol Lung Cell Mol Physiol. 2013;304(11):L709–21. doi: 10.1152/ajplung.00418.2012 23564511

4. Murtha LA, Schuliga MJ, Mabotuwana NS, Hardy SA, Waters DW, Burgess JK, et al. The Processes and Mechanisms of Cardiac and Pulmonary Fibrosis. Front Physiol. 2017;8:777. doi: 10.3389/fphys.2017.00777 29075197

5. Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med. 2012;18(7):1028–40. doi: 10.1038/nm.2807 22772564

6. Timpane S, Brandling-Bennett H, Kristjansson AK. Autoimmune collagen vascular diseases: Kids are not just little people. Clin Dermatol. 2016;34(6):678–89. doi: 10.1016/j.clindermatol.2016.07.002 27968927

7. Ewald CY, Landis JN, Porter Abate J, Murphy CT, Blackwell TK. Dauer-independent insulin/IGF-1-signalling implicates collagen remodelling in longevity. Nature. 2015;519(7541):97–101. doi: 10.1038/nature14021 25517099

8. Mienaltowski MJ, Birk DE. Structure, physiology, and biochemistry of collagens. Adv Exp Med Biol. 2014;802:5–29. doi: 10.1007/978-94-007-7893-1_2 24443018

9. Jensen D, Schekman R. COPII-mediated vesicle formation at a glance. Journal of cell science. 2011;124(1):1–4. doi: 10.1242/jcs.069773 21172817

10. Barlowe C, Helenius A. Cargo Capture and Bulk Flow in the Early Secretory Pathway. Annu Rev Cell Dev Biol. 2016;32:197–222. doi: 10.1146/annurev-cellbio-111315-125016 27298089

11. D’Arcangelo JG, Stahmer KR, Miller EA. Vesicle-mediated export from the ER: COPII coat function and regulation. Biochim Biophys Acta. 2013;1833(11):2464–72. doi: 10.1016/j.bbamcr.2013.02.003 23419775

12. Barrowman J, Bhandari D, Reinisch K, Ferro-Novick S. TRAPP complexes in membrane traffic: convergence through a common Rab. Nat Rev Mol Cell Biol. 2010;11(11):759–63. doi: 10.1038/nrm2999 20966969

13. Barlowe C. Twenty-five years after coat protein complex II. Mol Biol Cell. 2020;31(1):3–6. doi: 10.1091/mbc.E19-11-0621 31887067

14. Malhotra V, Erlmann P. The pathway of collagen secretion. Annu Rev Cell Dev Biol. 2015;31:109–24. doi: 10.1146/annurev-cellbio-100913-013002 26422332

15. Malhotra V, Erlmann P, Nogueira C. Procollagen export from the endoplasmic reticulum. Biochem Soc Trans. 2015;43(1):104–7. doi: 10.1042/BST20140286 25619253

16. Santos AJ, Raote I, Scarpa M, Brouwers N, Malhotra V. TANGO1 recruits ERGIC membranes to the endoplasmic reticulum for procollagen export. Elife. 2015;4. doi: 10.7554/eLife.10982 26568311

17. Ito S, Nagata K. Roles of the endoplasmic reticulum-resident, collagen-specific molecular chaperone Hsp47 in vertebrate cells and human disease. J Biol Chem. 2019;294(6):2133–41. doi: 10.1074/jbc.TM118.002812 30541925

18. Wilson DG, Phamluong K, Li L, Sun M, Cao TC, Liu PS, et al. Global defects in collagen secretion in a Mia3/TANGO1 knockout mouse. J Cell Biol. 2011;193(5):935–51. doi: 10.1083/jcb.201007162 21606205

19. Yuan L, Kenny SJ, Hemmati J, Xu K, Schekman R. TANGO1 and SEC12 are copackaged with procollagen I to facilitate the generation of large COPII carriers. Proc Natl Acad Sci U S A. 2018;115(52):E12255–E64. doi: 10.1073/pnas.1814810115 30545919

20. Raote I, Ernst AM, Campelo F, Rothman JE, Pincet F, Malhotra V. TANGO1 membrane helices create a lipid diffusion barrier at curved membranes. Elife. 2020;9. doi: 10.7554/eLife.57822 32452385

21. Page AP, Johnstone IL. The cuticle. WormBook. 2007:1–15.

22. Chioran A, Duncan S, Catalano A, Brown TJ, Ringuette MJ. Collagen IV trafficking: The inside-out and beyond story. Dev Biol. 2017;431(2):124–33. doi: 10.1016/j.ydbio.2017.09.037 28982537

23. Kramer JM. Basement membranes. WormBook. 2005:1–15. doi: 10.1895/wormbook.1.16.1 18050423

24. Teuscher AC, Jongsma E, Davis MN, Statzer C, Gebauer JM, Naba A, et al. The in-silico characterization of the Caenorhabditis elegans matrisome and proposal of a novel collagen classification. Matrix Biology Plus. 2019;1:100001.

25. Zhang Z, Bai M, Barbosa GO, Chen A, Wei Y, Luo S, et al. Broadly conserved roles of TMEM131 family proteins in intracellular collagen assembly and secretory cargo trafficking. Sci Adv. 2020;6(7):eaay7667. doi: 10.1126/sciadv.aay7667 32095531

26. Thein MC, McCormack G, Winter AD, Johnstone IL, Shoemaker CB, Page AP. Caenorhabditis elegans exoskeleton collagen COL-19: an adult-specific marker for collagen modification and assembly, and the analysis of organismal morphology. Dev Dyn. 2003;226(3):523–39. doi: 10.1002/dvdy.10259 12619137

27. Miao G, Zhang Y, Chen D, Zhang H. The ER-Localized Transmembrane Protein TMEM39A/SUSR2 Regulates Autophagy by Controlling the Trafficking of the PtdIns(4)P Phosphatase SAC1. Mol Cell. 2020;77(3):618–32 e5. doi: 10.1016/j.molcel.2019.10.035 31806350

28. Lee K, Sung JY, Lee S, Lim G, Jung KJ, Chung JM, et al. SURO-2/TMEM39 Facilitates Collagen Secretion through the Formation of Large COPII Vesicles. 2020.

29. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell. 2003;11(3):619–33. doi: 10.1016/s1097-2765(03)00105-9 12667446

30. Ihara S, Hagedorn EJ, Morrissey MA, Chi Q, Motegi F, Kramer JM, et al. Basement membrane sliding and targeted adhesion remodels tissue boundaries during uterine-vulval attachment in Caenorhabditis elegans. Nat Cell Biol. 2011;13(6):641–51. doi: 10.1038/ncb2233 21572423

31. Keeley DP, Hastie E, Jayadev R, Kelley LC, Chi Q, Payne SG, et al. Comprehensive Endogenous Tagging of Basement Membrane Components Reveals Dynamic Movement within the Matrix Scaffolding. Dev Cell. 2020;54(1):60–74 e7. doi: 10.1016/j.devcel.2020.05.022 32585132

32. Dang H, Klokk TI, Schaheen B, McLaughlin BM, Thomas AJ, Durns TA, et al. Derlin-dependent retrograde transport from endosomes to the Golgi apparatus. Traffic. 2011;12(10):1417–31. doi: 10.1111/j.1600-0854.2011.01243.x 21722281

33. Munoz-Lobato F, Rodriguez-Palero MJ, Naranjo-Galindo FJ, Shephard F, Gaffney CJ, Szewczyk NJ, et al. Protective role of DNJ-27/ERdj5 in Caenorhabditis elegans models of human neurodegenerative diseases. Antioxid Redox Signal. 2014;20(2):217–35. doi: 10.1089/ars.2012.5051 23641861

34. Pastor-Pareja JC, Xu T. Shaping cells and organs in Drosophila by opposing roles of fat body-secreted Collagen IV and perlecan. Dev Cell. 2011;21(2):245–56. doi: 10.1016/j.devcel.2011.06.026 21839919

35. Liu M, Feng Z, Ke H, Liu Y, Sun T, Dai J, et al. Tango1 spatially organizes ER exit sites to control ER export. J Cell Biol. 2017;216(4):1035–49. doi: 10.1083/jcb.201611088 28280122

36. Park J, Lee H, Tran Q, Mun K, Kim D, Hong Y, et al. Recognition of Transmembrane Protein 39A as a Tumor-Specific Marker in Brain Tumor. Toxicol Res. 2017;33(1):63–9. doi: 10.5487/TR.2017.33.1.063 28133515

37. Kumar S, Stecher G, Suleski M, Hedges SB. TimeTree: A Resource for Timelines, Timetrees, and Divergence Times. Mol Biol Evol. 2017;34(7):1812–9. doi: 10.1093/molbev/msx116 28387841

38. Eckley DM, Gill SR, Melkonian KA, Bingham JB, Goodson HV, Heuser JE, et al. Analysis of dynactin subcomplexes reveals a novel actin-related protein associated with the arp1 minifilament pointed end. J Cell Biol. 1999;147(2):307–20. doi: 10.1083/jcb.147.2.307 10525537

39. Urnavicius L, Zhang K, Diamant AG, Motz C, Schlager MA, Yu M, et al. The structure of the dynactin complex and its interaction with dynein. Science. 2015;347(6229):1441–6. doi: 10.1126/science.aaa4080 25814576

40. Reck-Peterson SL, Redwine WB, Vale RD, Carter AP. The cytoplasmic dynein transport machinery and its many cargoes. Nat Rev Mol Cell Biol. 2018;19(6):382–98. doi: 10.1038/s41580-018-0004-3 29662141

41. Khoriaty R, Hesketh GG, Bernard A, Weyand AC, Mellacheruvu D, Zhu G, et al. Functions of the COPII gene paralogs SEC23A and SEC23B are interchangeable in vivo. Proc Natl Acad Sci U S A. 2018;115(33):E7748–E57. doi: 10.1073/pnas.1805784115 30065114

42. Bi X, Corpina RA, Goldberg J. Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature. 2002;419(6904):271–7. doi: 10.1038/nature01040 12239560

43. Boyadjiev SA, Kim SD, Hata A, Haldeman-Englert C, Zackai EH, Naydenov C, et al. Cranio-lenticulo-sutural dysplasia associated with defects in collagen secretion. Clin Genet. 2011;80(2):169–76. doi: 10.1111/j.1399-0004.2010.01550.x 21039434

44. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature. 2002;415(6867):92–6. doi: 10.1038/415092a 11780124

45. Sasagawa Y, Yamanaka K, Ogura T. ER E3 ubiquitin ligase HRD-1 and its specific partner chaperone BiP play important roles in ERAD and developmental growth in Caenorhabditis elegans. Genes Cells. 2007;12(9):1063–73. doi: 10.1111/j.1365-2443.2007.01108.x 17825049

46. Bai M, Vozdek R, Hnizda A, Jiang C, Wang B, Kuchar L, et al. Conserved roles of C. elegans and human MANFs in sulfatide binding and cytoprotection. Nat Commun. 2018;9(1):897. doi: 10.1038/s41467-018-03355-0 29497057

47. Glover-Cutter KM, Lin S, Blackwell TK. Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet. 2013;9(9):e1003701. doi: 10.1371/journal.pgen.1003701 24068940

48. Essers PB, Nonnekens J, Goos YJ, Betist MC, Viester MD, Mossink B, et al. A Long Noncoding RNA on the Ribosome Is Required for Lifespan Extension. Cell Rep. 2015;10(3):339–45. doi: 10.1016/j.celrep.2014.12.029 25600869

49. Nakamura S, Karalay O, Jager PS, Horikawa M, Klein C, Nakamura K, et al. Mondo complexes regulate TFEB via TOR inhibition to promote longevity in response to gonadal signals. Nat Commun. 2016;7:10944. doi: 10.1038/ncomms10944 27001890

50. Melendez A, Levine B. Autophagy in C. elegans. WormBook. 2009:1–26. doi: 10.1895/wormbook.1.147.1 19705512

51. Jung CH, Ro SH, Cao J, Otto NM, Kim DH. mTOR regulation of autophagy. FEBS Lett. 2010;584(7):1287–95. doi: 10.1016/j.febslet.2010.01.017 20083114

52. Zhang H, Chang JT, Guo B, Hansen M, Jia K, Kovacs AL, et al. Guidelines for monitoring autophagy in Caenorhabditis elegans. Autophagy. 2015;11(1):9–27. doi: 10.1080/15548627.2014.1003478 25569839

53. Zhang H, Wu F, Wang X, Du H, Wang X, Zhang H. The two C. elegans ATG-16 homologs have partially redundant functions in the basal autophagy pathway. Autophagy. 2013;9(12):1965–74. doi: 10.4161/auto.26095 24185444

54. Watson P, Forster R, Palmer KJ, Pepperkok R, Stephens DJ. Coupling of ER exit to microtubules through direct interaction of COPII with dynactin. Nature cell biology. 2005;7(1):48–55. doi: 10.1038/ncb1206 15580264

55. Tran Q, Park J, Lee H, Hong Y, Hong S, Park S, et al. TMEM39A and Human Diseases: A Brief Review. Toxicol Res. 2017;33(3):205–9. doi: 10.5487/TR.2017.33.3.205 28744351

56. Baruah C, Devi P, Sharma DK. Sequence Analysis and Structure Prediction of SARS-CoV-2 Accessory Proteins 9b and ORF14: Evolutionary Analysis Indicates Close Relatedness to Bat Coronavirus. Biomed Res Int. 2020;2020:7234961. doi: 10.1155/2020/7234961 33102591

57. Gordon DE, Jang GM, Bouhaddou M, Xu J, Obernier K, White KM, et al. A SARS-CoV-2 protein interaction map reveals targets for drug repurposing. Nature. 2020;583(7816):459–68. doi: 10.1038/s41586-020-2286-9 32353859

58. Mello CC, Kramer JM, Stinchcomb D, Ambros V. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991;10(12):3959–70. 1935914

59. Zhao P, Zhang Z, Ke H, Yue Y, Xue D. Oligonucleotide-based targeted gene editing in C. elegans via the CRISPR/Cas9 system. Cell Res. 2014;24(2):247–50. doi: 10.1038/cr.2014.9 24418757

60. Zhao P, Zhang Z, Lv X, Zhao X, Suehiro Y, Jiang Y, et al. One-step homozygosity in precise gene editing by an improved CRISPR/Cas9 system. Cell Res. 2016;26(5):633–6. doi: 10.1038/cr.2016.46 27055372

61. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77(1):71–94. 4366476

62. Kamath RS, Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods. 2003;30(4):313–21. doi: 10.1016/s1046-2023(03)00050-1 12828945

63. Byrne AB, Weirauch MT, Wong V, Koeva M, Dixon SJ, Stuart JM, et al. A global analysis of genetic interactions in Caenorhabditis elegans. J Biol. 2007;6(3):8. doi: 10.1186/jbiol58 17897480

Článek Glucocerebrosidase reduces the spread of protein aggregation in a Drosophila melanogaster model of neurodegeneration by regulating proteins trafficked by extracellular vesicles

Článek Calcium ions trigger the exposure of phosphatidylserine on the surface of necrotic cells

Článek The developmental genetic architecture of vocabulary skills during the first three years of life: Capturing emerging associations with later-life reading and cognition

Článek ATF3 downmodulates its new targets IFI6 and IFI27 to suppress the growth and migration of tongue squamous cell carcinoma cells

Článek Genomic analyses of glycine decarboxylase neurogenic mutations yield a large-scale prediction model for prenatal disease

Článek Transcriptome-wide transmission disequilibrium analysis identifies novel risk genes for autism spectrum disorder

Článek Ush regulates hemocyte-specific gene expression, fatty acid metabolism and cell cycle progression and cooperates with dNuRD to orchestrate hematopoiesis

Článek Genetic loci associated with skin pigmentation in African Americans and their effects on vitamin D deficiency

Článek Actionable pharmacogenetic variants in Hong Kong Chinese exome sequencing data and projected prescription impact in the Hong Kong population

Článek Four families of folate-independent methionine synthases

Článek Increased dopaminergic neurotransmission results in ethanol dependent sedative behaviors in Caenorhabditis elegans

Článek Acetyltransferase Enok regulates transposon silencing and piRNA cluster transcription