AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Genes & Diseases Article
PDF (839.8 KB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Review Article | Open Access

Mechanism and effect of stress granule formation in cancer and its potential roles in breast cancer therapy

Taobo Hua, Wei Houb, Enhua Xiaoc( ), Mengping Longb,c( )
Department of Breast Surgery, Peking University People's Hospital, Beijing 100044, PR China
Department of Pathology, Peking University Cancer Hospital, Beijing 100142, PR China
Department of Radiology, The Second Xiangya Hospital, Central South University, Changsha, Hunan 410011, PR China

Peer review under responsibility of Chongqing Medical University.

Show Author Information

Abstract

Stress granules are non-membranous cytoplasmic foci induced by various stress conditions. It is a protective strategy used by cells to suppress overall translation during stress. In cancer cells, it was thought that the formation of stress granules could protect them from apoptosis and induces resistance towards anti-cancer drugs or radiation treatment which makes the stress granules a potential target for cancer treatment. However, most of our understanding of stress granules are still in the stage of molecular and cell biology, and a transitional gap for its actual effect on clinical settings remains. In this review, we summarize the mechanism and effect of stress granules formation in cancer and try to illuminate its potential applications in cancer therapy, using breast cancer as an example.

Keywords

Drug resistanceBreast cancerApoptosisStress granulesTranslation initiation

References

1

Collier NC, Heuser J, Levy MA, Schlesinger MJ. Ultrastructural and biochemical analysis of the stress granule in chicken embryo fibroblasts. J Cell Biol. 1988;106(4): 1131-1139.
Crossref Google Scholar
2

Jevtov I, Zacharogianni M, van Oorschot MM, et al. TORC2 mediates the heat stress response in Drosophila by promoting the formation of stress granules. J Cell Sci. 2015;128(14): 2497-2508.
Crossref Google Scholar
3

Buchan JR, Muhlrad D, Parker R. P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol. 2008;183(3): 441-455.
Crossref Google Scholar
4

Grabocka E, Bar-Sagi D. Mutant KRAS enhances tumor cell fitness by upregulating stress granules. Cell. 2016;167(7): 1803-1813.
Crossref Google Scholar
5

Somasekharan SP, El-Naggar A, Leprivier G, et al. YB-1 regulates stress granule formation and tumor progression by translationally activating G3BP1. J Cell Biol. 2015;208(7): 913-929.
Crossref Google Scholar
6

Valentin-Vega YA, Wang YD, Parker M, et al. Cancer-associated DDX3X mutations drive stress granule assembly and impair global translation. Sci Rep. 2016;6: 25996.
Crossref Google Scholar
7

Kedersha NL, Gupta M, Li W, Miller I, Anderson P. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol. 1999;147(7): 1431-1442.
Crossref Google Scholar
8

Kimball SR, Horetsky RL, Ron D, Jefferson LS, Harding HP. Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes. Am J Physiol Cell Physiol. 2003;284(2): C273-C284.
Crossref Google Scholar
9

Kedersha N, Chen S, Gilks N, et al. Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol Biol Cell. 2002;13(1): 195-210.
Crossref Google Scholar
10

Mokas S, Mills JR, Garreau C, et al. Uncoupling stress granule assembly and translation initiation inhibition. Mol Biol Cell. 2009;20(11): 2673-2683.
Crossref Google Scholar
11

Tourrière H, Chebli K, Zekri L, et al. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol. 2003;160(6): 823-831.
Crossref Google Scholar
12

Protter DSW, Parker R. Principles and properties of stress granules. Trends Cell Biol. 2016;26(9): 668-679.
Crossref Google Scholar
13

Jain S, Wheeler JR, Walters RW, Agrawal A, Barsic A, Parker R. ATPase-modulated stress granules contain a diverse proteome and substructure. Cell. 2016;164(3): 487-498.
Crossref Google Scholar
14

Martin S, Tazi J. Visualization of G3BP stress granules dynamics in live primary cells. J Vis Exp. 2014;87: 51197.
Crossref Google Scholar
15

Wall ML, Lewis SM. Methylarginines within the RGG-motif region of hnRNP A1 affect its IRES trans-acting factor Activity and are required for hnRNP A1 stress granule localization and formation. J Mol Biol. 2017;429(2): 295-307.
Crossref Google Scholar
16

Baron DM, Kaushansky LJ, Ward CL, et al. Amyotrophic lateral sclerosis-linked FUS/TLS alters stress granule assembly and dynamics. Mol Neurodegener. 2013;8: 30.
Crossref Google Scholar
17

Gilks N, Kedersha N, Ayodele M, et al. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell. 2004;15(12): 5383-5398.
Crossref Google Scholar
18

Aguzzi A, Altmeyer M. Phase separation: linking cellular compartmentalization to disease. Trends Cell Biol. 2016;26(7): 547-558.
Crossref Google Scholar
19

Lin Y, Protter DSW, Rosen MK, Parker R. Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol Cell. 2015;60(2): 208-219.
Crossref Google Scholar
20

Panas MD, Ivanov P, Anderson P. Mechanistic insights into mammalian stress granule dynamics. J Cell Biol. 2016;215(3): 313-323.
Crossref Google Scholar
21

Buchan JR, Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell. 2009;36(6): 932-941.
Crossref Google Scholar
22

Reineke LC, Cheema SA, Dubrulle J, Neilson JR. Chronic starvation induces noncanonical pro-death stress granules. J Cell Sci. 2018;131(19): jcs220244.
Crossref Google Scholar
23

Fujimura K, Sasaki AT, Anderson P. Selenite targets eIF4E-binding protein-1 to inhibit translation initiation and induce the assembly of non-canonical stress granules. Nucleic Acids Res. 2012;40(16): 8099-8110.
Crossref Google Scholar
24

Visser LJ, Medina GN, Rabouw HH, et al. Foot-and-Mouth disease virus leader protease cleaves G3BP1 and G3BP2 and inhibits stress granule formation. J Virol. 2019;93(2): e00922-18.
Crossref Google Scholar
25

Gordon D, Dafinca R, Scaber J, et al. Single-copy expression of an amyotrophic lateral sclerosis-linked TDP-43 mutation (M337V) in BAC transgenic mice leads to altered stress granule dynamics and progressive motor dysfunction. Neurobiol Dis. 2019;121: 148-162.
Crossref Google Scholar
26

Anderson P, Kedersha N, Ivanov P. Stress granules, P-bodies and cancer. Biochim Biophys Acta. 2015;1849(7): 861-870.
Crossref Google Scholar
27

Pelicano H, Carney D, Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist Updat. 2004;7(2): 97-110.
Crossref Google Scholar
28

Conklin KA. Chemotherapy-associated oxidative stress: impact on chemotherapeutic effectiveness. Integr Canc Ther. 2004;3(4): 294-300.
Crossref Google Scholar
29

Moeller BJ, Richardson RA, Dewhirst MW. Hypoxia and radiotherapy: opportunities for improved outcomes in cancer treatment. Cancer Metastasis Rev. 2007;26(2): 241-248.
Crossref Google Scholar
30

Longley DB, Harkin DP, Johnston PG. 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer. 2003;3(5): 330-338.
Crossref Google Scholar
31

Kaehler C, Isensee J, Hucho T, Lehrach H, Krobitsch S. 5-Fluorouracil affects assembly of stress granules based on RNA incorporation. Nucleic Acids Res. 2014;42(10): 6436-6447.
Crossref Google Scholar
32

Wilhelm S, Carter C, Lynch M, et al. Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat Rev Drug Discov. 2006;5(10): 835-844.
Crossref Google Scholar
33

Escudier B, Eisen T, Stadler WM, et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med. 2007;356(2): 125-134.
Crossref Google Scholar
34

Spinzi G, Paggi S. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008;359(23): 2497-2498.
Crossref Google Scholar
35

Zafrakas M, Papasozomenou P, Emmanouilides C. Sorafenib in breast cancer treatment: a systematic review and overview of clinical trials. World J Clin Oncol. 2016;7(4): 331-336.
Crossref Google Scholar
36

Adjibade P, St-Sauveur VG, Quevillon Huberdeau M, et al. Sorafenib, a multikinase inhibitor, induces formation of stress granules in hepatocarcinoma cells. Oncotarget. 2015;6(41): 43927-43943.
Crossref Google Scholar
37

Adjibade P, Simoneau B, Ledoux N, et al. Treatment of cancer cells with Lapatinib negatively regulates general translation and induces stress granules formation. PLoS One. 2020;15(5): e0231894.
Crossref Google Scholar
38

Cruickshanks N, Tang Y, Booth L, Hamed H, Grant S, Dent P. Lapatinib and obatoclax kill breast cancer cells through reactive oxygen species-dependent endoplasmic reticulum stress. Mol Pharmacol. 2012;82(6): 1217-1229.
Crossref Google Scholar
39

Rahmani M, Davis EM, Crabtree TR, et al. The kinase inhibitor sorafenib induces cell death through a process involving induction of endoplasmic reticulum stress. Mol Cell Biol. 2007;27(15): 5499-5513.
Crossref Google Scholar
40

Doan NTQ, Paulsen ES, Sehgal P, et al. Targeting thapsigargin towards tumors. Steroids. 2015;97: 2-7.
Crossref Google Scholar
41
Macor JE. Annual Reports in Medicinal Chemistry. vol. 46. SanDiego, California: Academic Press; 2011. Annual reports inmedicinal chemistry.
42

Hood KA, West LM, Northcote PT, Berridge MV, Miller JH. Induction of apoptosis by the marine sponge (Mycale) metabolites, mycalamide A and pateamine. Apoptosis. 2001;6(3): 207-219.
Crossref Google Scholar
43

Cencic R, Carrier M, Galicia-Vázquez G, et al. Antitumor activity and mechanism of action of the cyclopentabbenzofuran, silvestrol. PLoS One. 2009;4(4): e5223.
Crossref Google Scholar
44

Tsumuraya T, Ishikawa C, Machijima Y, et al. Effects of hippuristanol, an inhibitor of eIF4A, on adult T-cell leukemia. Biochem Pharmacol. 2011;81(6): 713-722.
Crossref Google Scholar
45

Martins I, Kepp O, Schlemmer F, et al. Restoration of the immunogenicity of cisplatin-induced cancer cell death by endoplasmic reticulum stress. Oncogene. 2011;30(10): 1147-1158.
Crossref Google Scholar
46

Raymond E, Chaney SG, Taamma A, Cvitkovic E. Oxaliplatin: a review of preclinical and clinical studies. Ann Oncol. 1998;9(10): 1053-1071.
Crossref Google Scholar
47

Noordhuis P, Laan AC, van de Born K, Losekoot N, Kathmann I, Peters GJ. Oxaliplatin activity in selected and unselected human ovarian and colorectal cancer cell lines. Biochem Pharmacol. 2008;76(1): 53-61.
Crossref Google Scholar
48

Demtröder C, Solass W, Zieren J, Strumberg D, Giger-Pabst U, Reymond MA. Pressurized intraperitoneal aerosol chemotherapy with oxaliplatin in colorectal peritoneal metastasis. Colorectal Dis. 2016;18(4): 364-371.
Crossref Google Scholar
49

Dasari S, Tchounwou PB. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol. 2014;740: 364-378.
Crossref Google Scholar
50

Tesniere A, Schlemmer F, Boige V, et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene. 2010;29(4): 482-491.
Crossref Google Scholar
51
Fournier MJ, Gareau C, Mazroui R. The ChemotherapeuticAgent Bortezomib Induces the Formation of Stress Granules.BioMed Central Ltd; 2010.
Crossref
52

Kashiwagi K, Ito T, Yokoyama S. Crystal structure of eIF2B and insights into eIF2-eIF2B interactions. FEBS J. 2017;284(6): 868-874.
Crossref Google Scholar
53

Emara MM, Fujimura K, Sciaranghella D, Ivanova V, Ivanov P, Anderson P. Hydrogen peroxide induces stress granule formation independent of eIF2α phosphorylation. Biochem Biophys Res Commun. 2012;423(4): 763-769.
Crossref Google Scholar
54

Timalsina S, Arimoto-Matsuzaki K, Kitamura M, et al. Chemical compounds that suppress hypoxia-induced stress granule formation enhance cancer drug sensitivity of human cervical cancer HeLa cells. J Biochem. 2018;164(5): 381-391.
Crossref Google Scholar
55

Bordeleau ME, Mori A, Oberer M, et al. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat Chem Biol. 2006;2(4): 213-220.
Crossref Google Scholar
56

Bordeleau ME, Robert F, Gerard B, et al. Therapeutic suppression of translation initiation modulates chemosensitivity in a mouse lymphoma model. J Clin Invest. 2008;118(7): 2651-2660.
Crossref Google Scholar
57

Cramer Z, Sadek J, Vazquez GG, et al. eIF4A inhibition prevents the onset of cytokine-induced muscle wasting by blocking the STAT3 and iNOS pathways. Sci Rep. 2018;8(1): 8414.
Crossref Google Scholar
58

Mazroui R, Sukarieh R, Bordeleau ME, et al. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol Biol Cell. 2006;17(10): 4212-4219.
Crossref Google Scholar
59

Kim WJ, Kim JH, Jang SK. Anti-inflammatory lipid mediator 15d-PGJ2 inhibits translation through inactivation of eIF4A. EMBO J. 2007;26(24): 5020-5032.
Crossref Google Scholar
60

Fu X, Gao X, Ge L, et al. Malonate induces the assembly of cytoplasmic stress granules. FEBS Lett. 2016;590(1): 22-33.
Crossref Google Scholar
61

Thomas JD, Johannes GJ. Identification of mRNAs that continue to associate with polysomes during hypoxia. RNA. 2007;13(7): 1116-1131.
Crossref Google Scholar
62

Baglioni C. Inhibition of protein synthesis in reticulocytes by antibiotics. 3. Mechanism of action of sparsomycin. Biochim Biophys Acta. 1966;129(3): 642-645.
Crossref Google Scholar
63

Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science. 2000;290(5497): 1717-1721.
Crossref Google Scholar
64

Seguin SJ, Morelli FF, Vinet J, et al. Inhibition of autophagy, lysosome and VCP function impairs stress granule assembly. Cell Death Differ. 2014;21(12): 1838-1851.
Crossref Google Scholar
65

Buchan JR, Kolaitis RM, Taylor JP, Parker R. Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell. 2013;153(7): 1461-1474.
Crossref Google Scholar
66

Benjamin D, Colombi M, Moroni C, Hall MN. Rapamycin passes the torch: a new generation of mTOR inhibitors. Nat Rev Drug Discov. 2011;10(11): 868-880.
Crossref Google Scholar
67

Kim EH, Sohn S, Kwon HJ, et al. Sodium selenite induces superoxide-mediated mitochondrial damage and subsequent autophagic cell death in malignant glioma cells. Cancer Res. 2007;67(13): 6314-6324.
Crossref Google Scholar
68

Wippich F, Bodenmiller B, Trajkovska MG, Wanka S, Aebersold R, Pelkmans L. Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell. 2013;152(4): 791-805.
Crossref Google Scholar
69

Sfakianos AP, Mellor LE, Pang YF, et al. The mTOR-S6 kinase pathway promotes stress granule assembly. Cell Death Differ. 2018;25(10): 1766-1780.
Crossref Google Scholar
70

Attwood KM, Robichaud A, Westhaver LP, et al. Raloxifene prevents stress granule dissolution, impairs translational control and promotes cell death during hypoxia in glioblastoma cells. Cell Death Dis. 2020;11(11): 989.
Crossref Google Scholar
71

Sidrauski C, McGeachy AM, Ingolia NT, Walter P. The small molecule ISRIB reverses the effects of eIF2α phosphorylation on translation and stress granule assembly. Elife. 2015;4: e05033.
Crossref Google Scholar
72

Moeller BJ, Cao Y, Li CY, Dewhirst MW. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell. 2004;5(5): 429-441.
Crossref Google Scholar
73

Semenza GL. Intratumoral hypoxia, radiation resistance, and HIF-1. Cancer Cell. 2004;5(5): 405-406.
Crossref Google Scholar
74

Zou T, Rao JN, Liu L, et al. Polyamines inhibit the assembly of stress granules in normal intestinal epithelial cells regulating apoptosis. Am J Physiol Cell Physiol. 2012;303(1): C102-C111.
Crossref Google Scholar
75

Shah OJ, Wang Z, Hunter T. Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Curr Biol. 2004;14(18): 1650-1656.
Crossref Google Scholar
76

Takahara T, Maeda T. Transient sequestration of TORC1 into stress granules during heat stress. Mol Cell. 2012;47(2): 242-252.
Crossref Google Scholar
77

Thedieck K, Holzwarth B, Prentzell MT, et al. Inhibition of mTORC1 by astrin and stress granules prevents apoptosis in cancer cells. Cell. 2013;154(4): 859-874.
Crossref Google Scholar
78

Zanke BW, Boudreau K, Rubie E, et al. The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr Biol. 1996;6(5): 606-613.
Crossref Google Scholar
79

Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell. 2000;103(2): 239-252.
Crossref Google Scholar
80

Sui X, Kong N, Ye L, et al. p38 and JNK MAPK pathways control the balance of apoptosis and autophagy in response to chemotherapeutic agents. Cancer Lett. 2014;344(2): 174-179.
Crossref Google Scholar
81

Arimoto K, Fukuda H, Imajoh-Ohmi S, Saito H, Takekawa M. Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat Cell Biol. 2008;10(11): 1324-1332.
Crossref Google Scholar
82

Tsai NP, Wei LN. RhoA/ROCK1 signaling regulates stress granule formation and apoptosis. Cell Signal. 2010;22(4): 668-675.
Crossref Google Scholar
83

Simon HU, Haj-Yehia A, Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis. 2000;5(5): 415-418.
Crossref Google Scholar
84

Khong A, Matheny T, Jain S, Mitchell SF, Wheeler JR, Parker R. The stress granule transcriptome reveals principles of mRNA accumulation in stress granules. Mol Cell. 2017;68(4): 808-820.
Crossref Google Scholar
85

Takahashi M, Higuchi M, Matsuki H, et al. Stress granules inhibit apoptosis by reducing reactive oxygen species production. Mol Cell Biol. 2013;33(4): 815-829.
Crossref Google Scholar
86

Rohwer N, Cramer T. Hypoxia-mediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways. Drug Resist Updat. 2011;14(3): 191-201.
Crossref Google Scholar
87

Glass L, Wente SR. Gle1 mediates stress granule-dependent survival during chemotoxic stress. Adv Biol Regul. 2019;71: 156-171.
Crossref Google Scholar
88

Aditi, Folkmann AW, Wente SR. Cytoplasmic hGle1A regulates stress granules by modulation of translation. Mol Biol Cell. 2015;26(8): 1476-1490.
Crossref Google Scholar
89

El-Naggar AM, Sorensen PH. Translational control of aberrant stress responses as a hallmark of cancer. J Pathol. 2018;244(5): 650-666.
Crossref Google Scholar
90

Schewe DM, Aguirre-Ghiso JA. Inhibition of eIF2alpha dephosphorylation maximizes bortezomib efficiency and eliminates quiescent multiple myeloma cells surviving proteasome inhibitor therapy. Cancer Res. 2009;69(4): 1545-1552.
Crossref Google Scholar
91

Leung AKL, Calabrese JM, Sharp PA. Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc Natl Acad Sci U S A. 2006;103(48): 18125-18130.
Crossref Google Scholar
92

Pare JM, Tahbaz N, López-Orozco J, LaPointe P, Lasko P, Hobman TC. Hsp90 regulates the function of argonaute 2 and its recruitment to stress granules and P-bodies. Mol Biol Cell. 2009;20(14): 3273-3284.
Crossref Google Scholar
93

Wang R, Jiang X, Bao P, Qin M, Xu J. Circadian control of stress granules by oscillating EIF2α. Cell Death Dis. 2019;10(3): 215.
Crossref Google Scholar
Genes & Diseases
Volume 9 Issue 3,
May 2022
Pages 659-667
DOI: 10.1016/j.gendis.2021.02.005
Cite this article:
Hu T, Hou W, Xiao E, et al. Mechanism and effect of stress granule formation in cancer and its potential roles in breast cancer therapy. Genes & Diseases, 2022, 9(3): 659-667. https://doi.org/10.1016/j.gendis.2021.02.005

327

Views

2

Downloads

15

Crossref

13

Web of Science

13

Scopus

0

CSCD

Altmetrics
Received: 19 December 2020
Revised: 04 February 2021
Accepted: 10 February 2021
Published: 23 February 2021
© 2021, Chongqing Medical University.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Return