Molecules and Cells

  • 제46권4호
  • /
  • Pages.191-199
  • /
  • 2023
  • /
  • 1016-8478(pISSN)
  • /
  • 0219-1032(eISSN)
한국분자세포생물학회 (Korean Society for Molecular and Cellular Biology)
권호 표지
DOI QR코드

DOI QR Code

Golgi Stress Response: New Insights into the Pathogenesis and Therapeutic Targets of Human Diseases

  • Won Kyu Kim (Natural Product Research Center, Korea Institute of Science and Technology (KIST)) ;
  • Wooseon Choi (Department of Pharmacology, Department of Biomedicine & Health Sciences, College of Medicine, The Catholic University of Korea) ;
  • Barsha Deshar (Department of Pharmacology, Department of Biomedicine & Health Sciences, College of Medicine, The Catholic University of Korea) ;
  • Shinwon Kang (Department of Physiology, University of Toronto) ;
  • Jiyoon Kim (Department of Pharmacology, Department of Biomedicine & Health Sciences, College of Medicine, The Catholic University of Korea)
  • 투고 : 2022.09.27
  • 심사 : 2022.10.30
  • 발행 : 2023.04.30
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

The Golgi apparatus modifies and transports secretory and membrane proteins. In some instances, the production of secretory and membrane proteins exceeds the capacity of the Golgi apparatus, including vesicle trafficking and the post-translational modification of macromolecules. These proteins are not modified or delivered appropriately due to the insufficiency in the Golgi function. These conditions disturb Golgi homeostasis and induce a cellular condition known as Golgi stress, causing cells to activate the 'Golgi stress response,' which is a homeostatic process to increase the capacity of the Golgi based on cellular requirements. Since the Golgi functions are diverse, several response pathways involving TFE3, HSP47, CREB3, proteoglycan, mucin, MAPK/ETS, and PERK regulate the capacity of each Golgi function separately. Understanding the Golgi stress response is crucial for revealing the mechanisms underlying Golgi dynamics and its effect on human health because many signaling molecules are related to diseases, ranging from viral infections to fatal neurodegenerative diseases. Therefore, it is valuable to summarize and investigate the mechanisms underlying Golgi stress response in disease pathogenesis, as they may contribute to developing novel therapeutic strategies. In this review, we investigate the perturbations and stress signaling of the Golgi, as well as the therapeutic potentials of new strategies for treating Golgi stress-associated diseases.

키워드

과제정보

This work was supported by the National Research Foundation (NRF), funded by the Ministry of Science and ICT, Republic of Korea (No. 2021R1C1C1008587), the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), and Korea Dementia Research Center (KDRC) funded by the Ministry of Health & Welfare and Ministry of Science and ICT, Republic of Korea (No. HU22C0069), and the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health & Welfare, the Republic of Korea (No. HI22C1236).

참고문헌

  1. Alborzinia, H., Ignashkova, T.I., Dejure, F.R., Gendarme, M., Theobald, J., Wolfl, S., Lindemann, R.K., and Reiling, J.H. (2018). Golgi stress mediates redox imbalance and ferroptosis in human cells. Commun. Biol. 1, 210.
  2. Alvarez-Erviti, L., Rodriguez-Oroz, M.C., Cooper, J.M., Caballero, C., Ferrer, I., Obeso, J.A., and Schapira, A.H. (2010). Chaperone-mediated autophagy markers in Parkinson disease brains. Arch. Neurol. 67, 1464-1472. https://doi.org/10.1001/archneurol.2010.198
  3. Bae, E.J., Lee, H.J., Rockenstein, E., Ho, D.H., Park, E.B., Yang, N.Y., Desplats, P., Masliah, E., and Lee, S.J. (2012). Antibody-aided clearance of extracellular alpha-synuclein prevents cell-to-cell aggregate transmission. J. Neurosci. 32, 13454-13469. https://doi.org/10.1523/JNEUROSCI.1292-12.2012
  4. Baghban, R., Roshangar, L., Jahanban-Esfahlan, R., Seidi, K., Ebrahimi-Kalan, A., Jaymand, M., Kolahian, S., Javaheri, T., and Zare, P. (2020). Tumor microenvironment complexity and therapeutic implications at a glance. Cell Commun. Signal. 18, 59.
  5. Bajaj, R., Warner, A.N., Fradette, J.F., and Gibbons, D.L. (2022). Dance of the Golgi: understanding Golgi dynamics in cancer metastasis. Cells 11, 1484.
  6. Bascil Tutuncu, N., Verdi, H., Yalcin, Y., Baysan Cebi, P., Kinik, S., Tutuncu, T., and Atac, F.B. (2022). Beta-cell Golgi stress response to lipotoxicity and glucolipotoxicity: a preliminary study of a potential mechanism of beta-cell failure in posttransplant diabetes and intraportal islet transplant. Exp. Clin. Transplant. 20, 585-594. https://doi.org/10.6002/ect.2022.0027
  7. Baumann, J., Ignashkova, T.I., Chirasani, S.R., Ramirez-Peinado, S., Alborzinia, H., Gendarme, M., Kuhnigk, K., Kramer, V., Lindemann, R.K., and Reiling, J.H. (2018). Golgi stress-induced transcriptional changes mediated by MAPK signaling and three ETS transcription factors regulate MCL1 splicing. Mol. Biol. Cell 29, 42-52. https://doi.org/10.1091/mbc.E17-06-0418
  8. Bayer, T.A. (2015). Proteinopathies, a core concept for understanding and ultimately treating degenerative disorders? Eur. Neuropsychopharmacol. 25, 713-724. https://doi.org/10.1016/j.euroneuro.2013.03.007
  9. Beckmann, H., Su, L.K., and Kadesch, T. (1990). TFE3: a helix-loop-helix protein that activates transcription through the immunoglobulin enhancer muE3 motif. Genes Dev. 4, 167-179. https://doi.org/10.1101/gad.4.2.167
  10. Bone, R.N., Oyebamiji, O., Talware, S., Selvaraj, S., Krishnan, P., Syed, F., Wu, H., and Evans-Molina, C. (2020). A computational approach for defining a signature of beta-cell Golgi stress in diabetes. Diabetes 69, 2364-2376. https://doi.org/10.2337/db20-0636
  11. Boss, W.F., Morre, D.J., and Mollenhauer, H.H. (1984). Monensin-induced swelling of Golgi apparatus cisternae mediated by a proton gradient. Eur. J. Cell Biol. 34, 1-8.
  12. Bui, S., Mejia, I., Diaz, B., and Wang, Y. (2021). Adaptation of the Golgi apparatus in cancer cell invasion and metastasis. Front. Cell Dev. Biol. 9, 806482.
  13. Cancino, J. and Luini, A. (2013). Signaling circuits on the Golgi complex. Traffic 14, 121-134. https://doi.org/10.1111/tra.12022
  14. Chang, K.H., Lee, L., Chen, J., and Li, W.S. (2006). Lithocholic acid analogues, new and potent alpha-2,3-sialyltransferase inhibitors. Chem. Commun. (Camb.) (6), 629-631.
  15. Chen, J. and Chen, Z.J. (2018). PtdIns4P on dispersed trans-Golgi network mediates NLRP3 inflammasome activation. Nature 564, 71-76. https://doi.org/10.1038/s41586-018-0761-3
  16. Chiti, F. and Dobson, C.M. (2017). Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade. Annu. Rev. Biochem. 86, 27-68. https://doi.org/10.1146/annurev-biochem-061516-045115
  17. De Niz, M., Caldelari, R., Kaiser, G., Zuber, B., Heo, W.D., Heussler, V.T., and Agop-Nersesian, C. (2021). Hijacking of the host cell Golgi by Plasmodium berghei liver stage parasites. J. Cell Sci. 134, jcs252213.
  18. Deleidi, M. and Maetzler, W. (2012). Protein clearance mechanisms of alpha-synuclein and amyloid-Beta in lewy body disorders. Int. J. Alzheimers Dis. 2012, 391438.
  19. Deng, S., Hu, Q., Chen, X., Lei, Q., and Lu, W. (2022). GM130 protects against blood-brain barrier disruption and brain injury after intracerebral hemorrhage by regulating autophagy formation. Exp. Gerontol. 163, 111772.
  20. Duden, R. (2003). ER-to-Golgi transport: COP I and COP II function (Review). Mol. Membr. Biol. 20, 197-207. https://doi.org/10.1080/0968768031000122548
  21. Eisenberg-Lerner, A., Benyair, R., Hizkiahou, N., Nudel, N., Maor, R., Kramer, M.P., Shmueli, M.D., Zigdon, I., Cherniavsky Lev, M., Ulman, A., et al. (2020). Golgi organization is regulated by proteasomal degradation. Nat. Commun. 11, 409.
  22. Ellinger, A. and Pavelka, M. (1984). Effect of monensin on the Golgi apparatus of absorptive cells in the small intestine of the rat. Morphological and cytochemical studies. Cell Tissue Res. 235, 187-194. https://doi.org/10.1007/BF00213739
  23. Farber-Katz, S.E., Dippold, H.C., Buschman, M.D., Peterman, M.C., Xing, M., Noakes, C.J., Tat, J., Ng, M.M., Rahajeng, J., Cowan, D.M., et al. (2014). DNA damage triggers Golgi dispersal via DNA-PK and GOLPH3. Cell 156, 413-427. https://doi.org/10.1016/j.cell.2013.12.023
  24. Feng, Y., Jadhav, A.P., Rodighiero, C., Fujinaga, Y., Kirchhausen, T., and Lencer, W.I. (2004). Retrograde transport of cholera toxin from the plasma membrane to the endoplasmic reticulum requires the trans-Golgi network but not the Golgi apparatus in Exo2-treated cells. EMBO Rep. 5, 596-601. https://doi.org/10.1038/sj.embor.7400152
  25. Hannun, Y.A. and Obeid, L.M. (2018). Sphingolipids and their metabolism in physiology and disease. Nat. Rev. Mol. Cell Biol. 19, 175-191. https://doi.org/10.1038/nrm.2017.107
  26. Hartl, F.U. (2017). Protein misfolding diseases. Annu. Rev. Biochem. 86, 21-26. https://doi.org/10.1146/annurev-biochem-061516-044518
  27. He, Q., Liu, H., Huang, C., Wang, R., Luo, M., and Lu, W. (2020). Herpes simplex virus 1-induced blood-brain barrier damage involves apoptosis associated with GM130-mediated Golgi stress. Front. Mol. Neurosci. 13, 2.
  28. He, Z., Liu, D., Liu, Y., Li, X., Shi, W., and Ma, H. (2022). Golgi-targeted fluorescent probe for imaging NO in Alzheimer's disease. Anal. Chem. 94, 10256-10262. https://doi.org/10.1021/acs.analchem.2c01885
  29. Howley, B.V. and Howe, P.H. (2018). Metastasis-associated upregulation of ER-Golgi trafficking kinetics: regulation of cancer progression via the Golgi apparatus. Oncoscience 5, 142-143. https://doi.org/10.18632/oncoscience.426
  30. Howley, B.V., Link, L.A., Grelet, S., El-Sabban, M., and Howe, P.H. (2018). A CREB3-regulated ER-Golgi trafficking signature promotes metastatic progression in breast cancer. Oncogene 37, 1308-1325. https://doi.org/10.1038/s41388-017-0023-0
  31. Jamaludin, M.I., Wakabayashi, S., Taniguchi, M., Sasaki, K., Komori, R., Kawamura, H., Takase, H., Sakamoto, M., and Yoshida, H. (2019). MGSE regulates crosstalk from the mucin pathway to the TFE3 pathway of the Golgi stress response. Cell Struct. Funct. 44, 137-151. https://doi.org/10.1247/csf.19009
  32. Kellokumpu, S., Sormunen, R., and Kellokumpu, I. (2002). Abnormal glycosylation and altered Golgi structure in colorectal cancer: dependence on intra-Golgi pH. FEBS Lett. 516, 217-224. https://doi.org/10.1016/S0014-5793(02)02535-8
  33. Klumperman, J. (2000). Transport between ER and Golgi. Curr. Opin. Cell Biol. 12, 445-449. https://doi.org/10.1016/S0955-0674(00)00115-0
  34. Kumar, V., Sami, N., Kashav, T., Islam, A., Ahmad, F., and Hassan, M.I. (2016). Protein aggregation and neurodegenerative diseases: from theory to therapy. Eur. J. Med. Chem. 124, 1105-1120. https://doi.org/10.1016/j.ejmech.2016.07.054
  35. Lawrence, R.E., Fromm, S.A., Fu, Y., Yokom, A.L., Kim, D.J., Thelen, A.M., Young, L.N., Lim, C.Y., Samelson, A.J., Hurley, J.H., et al. (2019). Structural mechanism of a Rag GTPase activation checkpoint by the lysosomal folliculin complex. Science 366, 971-977. https://doi.org/10.1126/science.aax0364
  36. Lee, M.C., Miller, E.A., Goldberg, J., Orci, L., and Schekman, R. (2004). Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20, 87-123. https://doi.org/10.1146/annurev.cellbio.20.010403.105307
  37. Li, H., Deng, C., Tan, Y., Dong, J., Zhao, Y., Wang, X., Yang, X., Luo, J., Gao, H., Huang, Y., et al. (2022a). Chondroitin sulfate-based prodrug nanoparticles enhance photodynamic immunotherapy via Golgi apparatus targeting. Acta Biomater. 146, 357-369. https://doi.org/10.1016/j.actbio.2022.05.014
  38. Li, J., Ahat, E., and Wang, Y. (2019). Golgi structure and function in health, stress, and diseases. Results Probl. Cell Differ. 67, 441-485. https://doi.org/10.1007/978-3-030-23173-6_19
  39. Li, S., Yang, K., Zeng, J., Ding, Y., Cheng, D., and He, L. (2022b). Golgi-targeting fluorescent probe for monitoring CO-releasing molecule-3 in vitro and in vivo. ACS Omega 7, 9929-9935. https://doi.org/10.1021/acsomega.2c00422
  40. Li, T., You, H., Mo, X., He, W., Tang, X., Jiang, Z., Chen, S., Chen, Y., Zhang, J., and Hu, Z. (2016). GOLPH3 mediated Golgi stress response in modulating N2A cell death upon oxygen-glucose deprivation and reoxygenation injury. Mol. Neurobiol. 53, 1377-1385. https://doi.org/10.1007/s12035-014-9083-0
  41. Li, X., Yu, J., Gong, L., Zhang, Y., Dong, S., Shi, J., Li, C., Li, Y., Zhang, Y., and Li, H. (2021). Heme oxygenase-1(HO-1) regulates Golgi stress and attenuates endotoxin-induced acute lung injury through hypoxia inducible factor-1α (HIF-1α)/HO-1 signaling pathway. Free Radic. Biol. Med. 165, 243-253. https://doi.org/10.1016/j.freeradbiomed.2021.01.028
  42. Liu, J., Huang, Y., Li, T., Jiang, Z., Zeng, L., and Hu, Z. (2021). The role of the Golgi apparatus in disease (Review). Int. J. Mol. Med. 47, 38.
  43. Luo, Q., Liu, Q., Cheng, H., Wang, J., Zhao, T., Zhang, J., Mu, C., Meng, Y., Chen, L., Zhou, C., et al. (2022). Nondegradable ubiquitinated ATG9A organizes Golgi integrity and dynamics upon stresses. Cell Rep. 40, 111195.
  44. Makhoul, C., Gosavi, P., and Gleeson, P.A. (2019). Golgi dynamics: the morphology of the mammalian Golgi apparatus in health and disease. Front. Cell Dev. Biol. 7, 112.
  45. Mathieu, J., Detraux, D., Kuppers, D., Wang, Y., Cavanaugh, C., Sidhu, S., Levy, S., Robitaille, A.M., Ferreccio, A., Bottorff, T., et al. (2019). Folliculin regulates mTORC1/2 and WNT pathways in early human pluripotency. Nat. Commun. 10, 632.
  46. Meng, J.F. and Luo, M.J. (2021). CRABP2 involvement in a mechanism of Golgi stress and tumor dry matter in non-small cell lung cancer cells via ER dependent Hippo pathway. Acta Biochim. Pol. 69, 31-36. https://doi.org/10.18388/abp.2020_5543
  47. Miyata, S., Mizuno, T., Koyama, Y., Katayama, T., and Tohyama, M. (2013). The endoplasmic reticulum-resident chaperone heat shock protein 47 protects the Golgi apparatus from the effects of O-glycosylation inhibition. PLoS One 8, e69732.
  48. Mytych, J., Solek, P., Bedzinska, A., Rusinek, K., Warzybok, A., Tabecka-Lonczynska, A., and Koziorowski, M. (2020). Towards age-related anti-inflammatory therapy: klotho suppresses activation of ER and Golgi stress response in senescent monocytes. Cells 9, 261.
  49. Nishida, Y., Arakawa, S., Fujitani, K., Yamaguchi, H., Mizuta, T., Kanaseki, T., Komatsu, M., Otsu, K., Tsujimoto, Y., and Shimizu, S. (2009). Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461, 654-658. https://doi.org/10.1038/nature08455
  50. Noguchi, S. and Shimizu, S. (2022). Molecular mechanisms and biological roles of GOMED. FEBS J. 289, 7213-7220. https://doi.org/10.1111/febs.16281
  51. Nolfi, D., Capone, A., Rosati, F., and Della Giovampaola, C. (2020). The alpha-1,2 fucosylated tubule system of DU145 prostate cancer cells is derived from a partially fragmented Golgi complex and its formation is actin-dependent. Exp. Cell Res. 396, 112324.
  52. Ochiai, A., Sawaguchi, S., Memezawa, S., Seki, Y., Morimoto, T., Oizumi, H., Ohbuchi, K., Yamamoto, M., Mizoguchi, K., Miyamoto, Y., et al. (2022). Knockdown of Golgi stress-responsive caspase-2 ameliorates HLD17-associated AIMP2 mutant-mediated inhibition of oligodendroglial cell morphological differentiation. Neurochem. Res. 47, 2617-2631. https://doi.org/10.1007/s11064-021-03451-6
  53. Oku, M., Tanakura, S., Uemura, A., Sohda, M., Misumi, Y., Taniguchi, M., Wakabayashi, S., and Yoshida, H. (2011). Novel cis-acting element GASE regulates transcriptional induction by the Golgi stress response. Cell Struct. Funct. 36, 1-12. https://doi.org/10.1247/csf.10014
  54. Pandey, K.P. and Zhou, Y. (2022). Influenza A virus infection activates NLRP3 inflammasome through trans-Golgi network dispersion. Viruses 14, 88.
  55. Park, J.H., Chung, C.G., Seo, J., Lee, B.H., Lee, Y.S., Kweon, J.H., and Lee, S.B. (2020). C9orf72-associated arginine-rich dipeptide repeat proteins reduce the number of Golgi outposts and dendritic branches in Drosophila neurons. Mol. Cells 43, 821-830.
  56. Petrosyan, A. (2015). Onco-Golgi: is fragmentation a gate to cancer progression? Biochem. Mol. Biol. J. 1, 16.
  57. Reiling, J.H., Olive, A.J., Sanyal, S., Carette, J.E., Brummelkamp, T.R., Ploegh, H.L., Starnbach, M.N., and Sabatini, D.M. (2013). A CREB3-ARF4 signalling pathway mediates the response to Golgi stress and susceptibility to pathogens. Nat. Cell Biol. 15, 1473-1485. https://doi.org/10.1038/ncb2865
  58. Robineau, S., Chabre, M., and Antonny, B. (2000). Binding site of brefeldin A at the interface between the small G protein ADP-ribosylation factor 1 (ARF1) and the nucleotide-exchange factor Sec7 domain. Proc. Natl. Acad. Sci. U. S. A. 97, 9913-9918. https://doi.org/10.1073/pnas.170290597
  59. Rohn, W.M., Rouille, Y., Waguri, S., and Hoflack, B. (2000). Bi-directional trafficking between the trans-Golgi network and the endosomal/lysosomal system. J. Cell Sci. 113 (Pt 12), 2093-2101. https://doi.org/10.1242/jcs.113.12.2093
  60. Romano, J.D., Sonda, S., Bergbower, E., Smith, M.E., and Coppens, I. (2013). Toxoplasma gondii salvages sphingolipids from the host Golgi through the rerouting of selected Rab vesicles to the parasitophorous vacuole. Mol. Biol. Cell 24, 1974-1995. https://doi.org/10.1091/mbc.e12-11-0827
  61. Saenz, J.B., Sun, W.J., Chang, J.W., Li, J., Bursulaya, B., Gray, N.S., and Haslam, D.B. (2009). Golgicide A reveals essential roles for GBF1 in Golgi assembly and function. Nat. Chem. Biol. 5, 157-165. https://doi.org/10.1038/nchembio.144
  62. Sakhrani, N.M. and Padh, H. (2013). Organelle targeting: third level of drug targeting. Drug Des. Devel. Ther. 7, 585-599.
  63. Sasaki, K., Komori, R., Taniguchi, M., Shimaoka, A., Midori, S., Yamamoto, M., Okuda, C., Tanaka, R., Sakamoto, M., Wakabayashi, S., et al. (2019). PGSE is a novel enhancer regulating the proteoglycan pathway of the mammalian Golgi stress response. Cell Struct. Funct. 44, 1-19. https://doi.org/10.1247/csf.18031
  64. Sbodio, J.I., Snyder, S.H., and Paul, B.D. (2018). Golgi stress response reprograms cysteine metabolism to confer cytoprotection in Huntington's disease. Proc. Natl. Acad. Sci. U. S. A. 115, 780-785. https://doi.org/10.1073/pnas.1717877115
  65. Schmidt, O., Weyer, Y., Baumann, V., Widerin, M.A., Eising, S., Angelova, M., Schleiffer, A., Kremser, L., Lindner, H., Peter, M., et al. (2019). Endosome and Golgi-associated degradation (EGAD) of membrane proteins regulates sphingolipid metabolism. EMBO J. 38, e101433.
  66. Schwabl, S. and Teis, D. (2022). Protein quality control at the Golgi. Curr. Opin. Cell Biol. 75, 102074.
  67. Sewell, R., Backstrom, M., Dalziel, M., Gschmeissner, S., Karlsson, H., Noll, T., Gatgens, J., Clausen, H., Hansson, G.C., Burchell, J., et al. (2006). The ST6GalNAc-I sialyltransferase localizes throughout the Golgi and is responsible for the synthesis of the tumor-associated sialyl-Tn O-glycan in human breast cancer. J. Biol. Chem. 281, 3586-3594. https://doi.org/10.1074/jbc.M511826200
  68. Spano, D. and Colanzi, A. (2022). Golgi Complex: a signaling hub in cancer. Cells 11, 1990.
  69. Suga, K., Saito, A., Mishima, T., and Akagawa, K. (2015). Data for the effects of ER and Golgi stresses on the ER-Golgi SNARE Syntaxin5 expression and on the betaAPP processing in cultured hippocampal neurons. Data Brief 5, 114-123. https://doi.org/10.1016/j.dib.2015.08.023
  70. Suga, K., Yamamoto-Hijikata, S., Terao, Y., Akagawa, K., and Ushimaru, M. (2022). Golgi stress induces upregulation of the ER-Golgi SNARE Syntaxin-5, altered betaAPP processing, and Caspase-3-dependent apoptosis in NG108-15 cells. Mol. Cell. Neurosci. 121, 103754.
  71. Tamaki, H. and Yamashina, S. (2002). The stack of the golgi apparatus. Arch. Histol. Cytol. 65, 209-218. https://doi.org/10.1679/aohc.65.209
  72. Taniguchi, M., Nadanaka, S., Tanakura, S., Sawaguchi, S., Midori, S., Kawai, Y., Yamaguchi, S., Shimada, Y., Nakamura, Y., Matsumura, Y., et al. (2015). TFE3 is a bHLH-ZIP-type transcription factor that regulates the mammalian Golgi stress response. Cell Struct. Funct. 40, 13-30. https://doi.org/10.1247/csf.14015
  73. Vijayan, K., Arang, N., Wei, L., Morrison, R., Geiger, R., Parks, K.R., Lewis, A.J., Mast, F.D., Douglass, A.N., Kain, H.S., et al. (2022). A genome-wide CRISPR-Cas9 screen identifies CENPJ as a host regulator of altered microtubule organization during Plasmodium liver infection. Cell Chem. Biol. 29, 1419-1433.e5. https://doi.org/10.1016/j.chembiol.2022.06.001
  74. Viotti, C. (2016). ER to Golgi-dependent protein secretion: the conventional pathway. Methods Mol. Biol. 1459, 3-29. https://doi.org/10.1007/978-1-4939-3804-9_1
  75. Wang, H., He, Z., Yang, Y., Zhang, J., Zhang, W., Zhang, W., Li, P., and Tang, B. (2019). Ratiometric fluorescence imaging of Golgi H2O2 reveals a correlation between Golgi oxidative stress and hypertension. Chem. Sci. 10, 10876-10880. https://doi.org/10.1039/C9SC04384E
  76. Wang, M., Zhang, Y., Komaniecki, G.P., Lu, X., Cao, J., Zhang, M., Yu, T., Hou, D., Spiegelman, N.A., Yang, M., et al. (2022). Golgi stress induces SIRT2 to counteract Shigella infection via defatty-acylation. Nat. Commun. 13, 4494.
  77. Watson, P. and Stephens, D.J. (2005). ER-to-Golgi transport: form and formation of vesicular and tubular carriers. Biochim. Biophys. Acta 1744, 304-315. https://doi.org/10.1016/j.bbamcr.2005.03.003
  78. Willett, R., Martina, J.A., Zewe, J.P., Wills, R., Hammond, G.R.V., and Puertollano, R. (2017). TFEB regulates lysosomal positioning by modulating TMEM55B expression and JIP4 recruitment to lysosomes. Nat. Commun. 8, 1580.
  79. Wu, J.I., Lin, Y.P., Tseng, C.W., Chen, H.J., and Wang, L.H. (2019). Crabp2 promotes metastasis of lung cancer cells via HuR and integrin beta1/FAK/ERK signaling. Sci. Rep. 9, 845.
  80. Yamaguchi, H., Arakawa, S., Kanaseki, T., Miyatsuka, T., Fujitani, Y., Watada, H., Tsujimoto, Y., and Shimizu, S. (2016). Golgi membrane-associated degradation pathway in yeast and mammals. EMBO J. 35, 1991-2007. https://doi.org/10.15252/embj.201593191
  81. Yamaguchi, H., Honda, S., Torii, S., Shimizu, K., Katoh, K., Miyake, K., Miyake, N., Fujikake, N., Sakurai, H.T., Arakawa, S., et al. (2020). Wipi3 is essential for alternative autophagy and its loss causes neurodegeneration. Nat. Commun. 11, 5311.
  82. Yuen, C.T., Chai, W., Loveless, R.W., Lawson, A.M., Margolis, R.U., and Feizi, T. (1997). Brain contains HNK-1 immunoreactive O-glycans of the sulfoglucuronyl lactosamine series that terminate in 2-linked or 2,6-linked hexose (mannose). J. Biol. Chem. 272, 8924-8931. https://doi.org/10.1074/jbc.272.14.8924
  83. Zhang, X., Yang, B., Shao, D., Zhao, Y., Sun, J., Li, J., Li, Y., and Cao, F. (2019). Longitudinal association of subjective prospective and retrospective memory and depression among patients with glioma. Eur. J. Oncol. Nurs. 42, 1-6. https://doi.org/10.1016/j.ejon.2019.07.003
  84. Zhu, H., Liu, C., Rong, X., Zhang, Y., Su, M., Wang, X., Liu, M., Zhang, X., Sheng, W., and Zhu, B. (2022). A new isothiocyanate-based Golgi-targeting fluorescent probe for Cys and its bioimaging applications during the Golgi stress response. Bioorg. Chem. 122, 105741.
  85. Zhu, X. and Kaverina, I. (2013). Golgi as an MTOC: making microtubules for its own good. Histochem. Cell Biol. 140, 361-367. https://doi.org/10.1007/s00418-013-1119-4