Trichosanthin increases Granzyme B penetration into tumor cells by upregulation of CI-MPR on the cell surface

Oncotarget

Volumn 8, Issue 16, 2017, Pages 26460-26470

  Li, Chunman ^a   Zeng, Meiqi ^a   Chi, Huju ^a   Shen, Jing ^b   Ng, Tzi Bun ^c   Jin, Guangyi ^a   Lu, Desheng ^a   Fan, Xinmin ^a   Xiong, Bilian ^a   Xiao, Zhangang ^b   Sha, Ou ^a  

^a Shenzhen University   (China)

^b SOUTHWEST MEDICAL UNIVERSITY   (China)

^c Prince of Wales Hospital   (Hong Kong)

Author keywords

Cation independent mannose 6 phosphate receptor; Granzyme B (GrzB); Immunotherapy; Trichosanthin; Tumor cells

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; BINDING PROTEIN; CATION INDEPENDENT MANNOSE 6 PHOSPHATE RECEPTOR; CISPLATIN; GAMMA ADAPTIN; GRANZYME B; SOMATOMEDIN B RECEPTOR; TRICHOSANTHIN; UNCLASSIFIED DRUG; GRANZYME; GZMB PROTEIN, HUMAN; PROTEIN BINDING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BINDING COMPETITION; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; DRUG MECHANISM; DRUG PENETRATION; DRUG POTENTIATION; DRUG PROTEIN BINDING; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MALE; MONOTHERAPY; MOUSE; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RECEPTOR UPREGULATION; TUMOR CELL; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DISEASE MODEL; DRUG SCREENING; METABOLISM; PROTEIN DOMAIN; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DISEASE MODELS, ANIMAL; GRANZYMES; HUMANS; MALE; MICE; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTOR, IGF TYPE 2; TRICHOSANTHIN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85017499356     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.15518     Document Type: Article

References (37)

1. Sha O, Niu J, Ng TB, Cho EY, Fu X, Jiang W. Anti-tumor action of trichosanthin, a type 1 ribosome-inactivating protein, employed in traditional Chinese medicine: a mini review. Cancer Chemother Pharmacol. 2013; 71:1387-93. doi: 10.1007/s00280-013-2096-y.
2. Zhao W, Feng D, Sun S, Han T, Sui S. The anti-viral protein of trichosanthin penetrates into human immunodeficiency virus type 1. Acta Biochim Biophys Sin (Shanghai). 2010; 42:91-7. doi: 10.1093/abbs/gmp111.
3. Yang CH, Ji YY, Yeh M. The kinetics of IL-4 and IFN-gamma gene expression in mice after Trichosansin immunization. Cell Res. 1998; 8:295-302. doi: 10.1038/cr.1998.29.
4. Fang EF, Zhang CZ, Zhang L, Wong JH, Chan YS, Pan WL, Dan XL, Yin CM, Cho CH, Ng TB. Trichosanthin inhibits breast cancer cell proliferation in both cell lines and nude mice by promotion of apoptosis. PLoS One. 2012; 7:e41592. doi: 10.1371/journal.pone.0041592.
5. Liu F, Wang B, Wang Z, Yu S. Trichosanthin down-regulates Notch signaling and inhibits proliferation of the nasopharyngeal carcinoma cell line CNE2 in vitro. Fitoterapia. 2012; 83:838-42. doi: 10.1016/j.fitote.2012.02.011.
6. Zhu Y, Sun Y, Cai Y, Sha O, Jiang W. Trichosanthin reduces the viability of SUDHL2 cells via the activation of the extrinsic and intrinsic apoptotic pathways. Mol Med Rep. 2016; 13:403-11. doi: 10.3892/mmr.2015.4531.
7. Byers VS, Levin AS, Malvino A, Waites L, Robins RA, Baldwin RW. A phase II study of effect of addition of trichosanthin to zidovudine in patients with HIV disease and failing antiretroviral agents. AIDS Res Hum Retroviruses. 1994; 10:413-20. doi: 10.1089/aid.1994.10.413.
8. Chan WL, Shaw PC, Tam SC, Jacobsen C, Gliemann J, Nielsen MS. Trichosanthin interacts with and enters cells via LDL receptor family members. Biochem Biophys Res Commun. 2000; 270:453-7. doi: 10.1006/bbrc.2000.2441.
9. Chan WY, Huang H, Tam SC. Receptor-mediated endocytosis of trichosanthin in choriocarcinoma cells. Toxicology. 2003; 186:191-203. doi: 10.1016/S0300-483X(02)00746-1.
10. Chan SH, Hung FS, Chan DS, Shaw PC. Trichosanthin interacts with acidic ribosomal proteins P0 and P1 and mitotic checkpoint protein MAD2B. Eur J Biochem. 2001; 268:2107-12. doi: 10.1046/j.1432-1327.2001.02091.x.
11. Shaw PC, Lee KM, Wong KB. Recent advances in trichosanthin, a ribosome-inactivating protein with multiple pharmacological properties. Toxicon. 2005; 45:683-9. doi: 10.1016/j.toxicon.2004.12.024.
12. Doray B, Bruns K, Ghosh P, Kornfeld S. Interaction of the cation-dependent mannose 6-phosphate receptor with GGA proteins. J Biol Chem. 2002; 277:18477-82. doi: 10.1074/jbc.M201879200.
13. Ghosh P, Griffith J, Geuze HJ, Kornfeld S. Mammalian GGAs act together to sort mannose 6-phosphate receptors. J Cell Biol. 2003; 163:755-66. doi: 10.1083/jcb.200308038.
14. He X, Li F, Chang WP, Tang J. GGA proteins mediate the recycling pathway of memapsin 2 (BACE). J Biol Chem. 2005; 280:11696-703. doi: 10.1074/jbc.M411296200.
15. Puertollano R, Aguilar RC, Gorshkova I, Crouch RJ, Bonifacino JS. Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science. 2001; 292:1712-6. doi: 10.1126/science.1060750.
16. Ghosh P, Kornfeld S. The GGA proteins: key players in protein sorting at the trans-Golgi network. Eur J Cell Biol. 2004; 83:257-62. doi: 10.1078/0171-9335-00374.
17. Boman AL, Zhang C, Zhu X, Kahn RA. A family of ADP-ribosylation factor effectors that can alter membrane transport through the trans-Golgi. Mol Biol Cell. 2000; 11:1241-55. doi: 10.1091/mbc.11.4.1241.
18. Dell'Angelica EC, Puertollano R, Mullins C, Aguilar RC, Vargas JD, Hartnell LM, Bonifacino JS. GGAs: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J Cell Biol. 2000; 149:81-94. doi: 10.1083/jcb.149.1.81.
19. Hirst J, Lui WW, Bright NA, Totty N, Seaman MN, Robinson MS. A family of proteins with gamma-adaptin and VHS domains that facilitate trafficking between the trans-Golgi network and the vacuole/lysosome. J Cell Biol. 2000; 149:67-80. doi: 10.1083/jcb.149.1.67.
20. Poussu A, Lohi O, Lehto VP. Vear, a novel Golgi-associated protein with VHS and gamma-adaptin 'ear' domains. J Biol Chem. 2000; 275:7176-83. doi: 10.1074/jbc.275.10.7176.
21. Chow TP, Feldman RA, Lovett M, Piatak M. Isolation and DNA sequence of a gene encoding alpha-trichosanthin, a type I ribosome-inactivating protein. J Biol Chem. 1990; 265:8670-4. doi:
22. Braulke T, Bonifacino JS. Sorting of lysosomal proteins. Biochim Biophys Acta. 2009; 1793:605-14. doi: 10.1016/j.bbamcr.2008.10.016.
23. Ghosh P, Dahms NM, Kornfeld S. Mannose 6-phosphate receptors: new twists in the tale. Nat Rev Mol Cell Biol. 2003; 4:202-12. doi: 10.1038/nrm1050.
24. Pohlmann R, Nagel G, Hille A, Wendland M, Waheed A, Braulke T, von Figura K. Mannose 6-phosphate specific receptors: structure and function. Biochem Soc Trans. 1989; 17:15-6. doi: 10.1042/bst0170015.
25. Ramakrishnan R, Assudani D, Nagaraj S, Hunter T, Cho HI, Antonia S, Altiok S, Celis E, Gabrilovich DI. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Invest. 2010; 120:1111-24. doi: 10.1172/JCI40269.
26. Ramakrishnan R, Huang C, Cho HI, Lloyd M, Johnson J, Ren X, Altiok S, Sullivan D, Weber J, Celis E, Gabrilovich DI. Autophagy induced by conventional chemotherapy mediates tumor cell sensitivity to immunotherapy. Cancer Res. 2012; 72:5483-93. doi: 10.1158/0008-5472.CAN-12-2236.
27. Ramakrishnan R, Gabrilovich DI. The role of mannose-6-phosphate receptor and autophagy in influencing the outcome of combination therapy. Autophagy. 2013; 9:615-6. doi: 10.4161/auto.23485.
28. Afonina IS, Cullen SP, Martin SJ. Cytotoxic and non-cytotoxic roles of the CTL/NK protease granzyme B. Immunol Rev. 2010; 235:105-16. doi: 10.1111/j.0105-2896.2010.00908.x.
29. Griffiths GM, Isaaz S. Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose-6-phosphate receptor. J Cell Biol. 1993; 120:885-96. doi: 10.1083/jcb.120.4.885.
30. Motyka B, Korbutt G, Pinkoski MJ, Heibein JA, Caputo A, Hobman M, Barry M, Shostak I, Sawchuk T, Holmes CF, Gauldie J, Bleackley RC. Mannose 6-phosphate/insulin-like growth factor II receptor is a death receptor for granzyme B during cytotoxic T cell-induced apoptosis. Cell. 2000; 103:491-500. doi: 10.1016/S0092-8674(00)00140-9.
31. Gehrmann M, Stangl S, Kirschner A, Foulds GA, Sievert W, Doss BT, Walch A, Pockley AG, Multhoff G. Immunotherapeutic targeting of membrane Hsp70-expressing tumors using recombinant human granzyme B. PLoS One. 2012; 7:e41341. doi: 10.1371/journal.pone.0041341.
32. Gross C, Koelch W, DeMaio A, Arispe N, Multhoff G. Cell surface-bound heat shock protein 70 (Hsp70) mediates perforin-independent apoptosis by specific binding and uptake of granzyme B. J Biol Chem. 2003; 278:41173-81. doi: 10.1074/jbc.M302644200.
33. Zeng M, Zheng M, Lu D, Wang J, Jiang W, Sha O. Anti-tumor activities and apoptotic mechanism of ribosome-inactivating proteins. Chin J Cancer. 2015; 34:325-34. doi: 10.1186/s40880-015-0030-x.
34. Cai X, Yao G, Xu G, Yang C, Xu H, Lin Y, Yu J, Sun B. Identification of the amino acid residues in trichosanthin crucial for IgE response. Biochem Biophys Res Commun. 2002; 297:510-6. doi: 10.1016/S0006-291X(02)02076-4.
35. Doray B, Bruns K, Ghosh P, Kornfeld SA. Autoinhibition of the ligand-binding site of GGA1/3 VHS domains by an internal acidic cluster-dileucine motif. Proc Natl Acad Sci USA. 2002; 99:8072-7. doi: 10.1073/pnas.082235699.
36. Shiba Y, Kametaka S, Waguri S, Presley JF, Randazzo PA. ArfGAP3 regulates the transport of cation-independent mannose 6-phosphate receptor in the post-Golgi compartment. Curr Biol. 2013; 23:1945-51. doi: 10.1016/j.cub.2013.07.087.
37. Hsu FT, Chen TC, Chuang HY, Chang YF, Hwang JJ. Enhancement of adoptive T cell transfer with single low dose pretreatment of doxorubicin or paclitaxel in mice. Oncotarget. 2015; 6:44134-50. doi: 10.18632/oncotarget.6628.