Cell membrane gp96 facilitates HER2 dimerization and serves as a novel target in breast cancer

International Journal of Cancer

Volumn 137, Issue 3, 2015, Pages 512-524

  Li, Xin ^a   Sun, Lu ^a   Hou, Junwei ^a   Gui, Mingming ^a   Ying, Jianming ^b   Zhao, Hong ^b   Lv, Ning ^b   Meng, Songdong ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b CANCER HOSPITAL   (China)

Author keywords

breast cancer; cell membrane gp96; grp94; HER2 dimerization; targeted therapy

Indexed keywords

ADENOVIRUS VECTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GLYCOPROTEIN GP 96; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY GP96; SCAFFOLD PROTEIN; TRASTUZUMAB; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; GLUCOSE REGULATED PROTEIN 94; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CELL GROWTH; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; DIMERIZATION; FEMALE; GENE OVEREXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; VIRAL GENE DELIVERY SYSTEM; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CHEMISTRY; DISEASE MODEL; GENE EXPRESSION; GENETICS; ISOGRAFT; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; TRANSFORMED CELL LINE; TRANSGENIC MOUSE; TUMOR CELL LINE; TUMOR VOLUME; XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELL MEMBRANE; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; HETEROGRAFTS; HUMANS; ISOGRAFTS; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; TUMOR BURDEN;

EID: 84929512660     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29405     Document Type: Article

References (49)

1. Liu B, Li Z,. Endoplasmic reticulum HSP90b1 (gp96, grp94) optimizes B-cell function via chaperoning integrin and TLR but not immunoglobulin. Blood 2008; 112: 1223-30.
2. Yang Y, Liu B, Dai J, et al., Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 2007; 26: 215-26.
3. Ostrovsky O, Ahmed NT, Argon Y,. The chaperone activity of GRP94 toward insulin-like growth factor II is necessary for the stress response to serum deprivation. Mol Biol Cell 2009; 20: 1855-64.
4. Melnick J, Dul JL, Argon Y,. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 1994; 370: 373-5.
5. Weekes MP, Antrobus R, Talbot S, et al., Proteomic plasma membrane profiling reveals an essential role for gp96 in the cell surface expression of LDLR family members, including the LDL receptor and LRP6. J Proteome Res 2012; 11: 1475-84.
6. Martins M, Custódio R, Camejo A, et al., Listeria monocytogenes triggers the cell surface expression of Gp96 protein and interacts with its N terminus to support cellular infection. J Biol Chem 2012; 287: 43083-93.
7. Mittal R, Prasadarao NV,. gp96 expression in neutrophils is critical for the onset of Escherichia coli K1 (RS218) meningitis. Nat Commun 2011; 2: 552.
8. Altmeyer A, Maki RG, Feldweg AM, et al., Tumor-specific cell surface expression of the-KDEL containing, endoplasmic reticular heat shock protein gp96. Int J Cancer 1996; 69: 340-9.
9. Robert J, Ménoret A, Cohen N,. Cell surface expression of the endoplasmic reticular heat shock protein gp96 is phylogenetically conserved. J Immunol 1999; 163: 4133-9.
10. Melendez K, Wallen ES, Edwards BS, et al., Heat shock protein 70 and glycoprotein 96 are differentially expressed on the surface of malignant and nonmalignant breast cells. Cell Stress Chaperones 2006; 11: 334-42.
11. Patel PD, Yan P, Seidler PM, et al., Paralog-selective Hsp90 inhibitors define tumor-specific regulation of HER2. Nat Chem Biol 2013; 9: 677-84.
12. Chavany C, Mimnaugh E, Miller P, et al., p185erbB2 binds to GRP94 in vivo. Dissociation of the p185erbB2/GRP94 heterocomplex by benzoquinone ansamycins precedes depletion of p185erbB2. J Biol Chem 1996; 271: 4974-7.
13. Koo BH, Apte SS,. Cell-surface processing of the metalloprotease pro-ADAMTS9 is influenced by the chaperone GRP94/gp96. J Biol Chem 2012 285: 197-205.
14. Sorkin A, Goh LK,. Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 2009; 315: 683-96.
15. Higa GM, Singh V, Abraham J,. Biological considerations and clinical applications of new HER2-targeted agents. Expert Rev Anticancer Ther 2010; 10: 1497-509.
16. Ghosh R, Narasanna A, Wang SE, et al., Trastuzumab has preferential activity against breast cancers driven by HER2 homodimers. Cancer Res 2011; 71: 1871-82.
17. Johnson BE, Jänne PA,. Rationale for a phase II trial of pertuzumab, a HER-2 dimerization inhibitor, in patients with non-small cell lung cancer. Clin Cancer Res 2006; 12: 4436s-40s.
18. Baselga J, Cortés J, Kim SB, et al., Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med 2012; 366: 109-19.
19. Gianni L, Pienkowski T, Im YH, et al., Efficacy and safety of neoadjuvant pertuzumab and trastuzumab in women with locally advanced, inflammatory, or early HER2-positive breast cancer (NeoSphere): a randomised multicentre, open-label, phase 2 trial. Lancet Oncol 2012; 13: 25-32.
20. Liu B, Dai J, Zheng H, et al., Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases. Proc Natl Acad Sci USA 2003; 100: 15824-9.
21. Way TD, Kao MC, Lin JK,. Apigenin induces apoptosis through proteasomal degradation of HER2/neu in HER2/neu-overexpressing breast cancer cells via the phosphatidylinositol 3-kinase/Akt-dependent pathway. J Biol Chem 2004; 279: 4479-89.
22. Hong RL, Spohn WH, Hung MC,. Curcumin inhibits tyrosine kinase activity of p185neu and also depletes p185neu. Clin Cancer Res 1999; 5: 1884-91.
23. Zhang Y, Cao S, Meng S, Gao GF,. A strategy to produce monoclonal antibodies against gp96 by prime-boost regimen using endogenous protein and E. Coli heterologously-expressed fragment. J Cent South Univ Technol 2011; 18: 1857-64.
24. Dollins DE, Warren JJ, Immormino RM, Gewirth DT,. Structures of GRP94-nucleotide complexes reveal mechanistic differences between the hsp90 chaperones. Mol Cell 2007; 28: 41-56.
25. Chung I, Akita R, Vandlen R, et al., Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 2010; 464: 783-7.
26. Liu P, Clevel TE, IV, Bouyain S, et al., A single ligand is sufficient to activate EGFR dimers. Proc Natl Acad Sci USA 2012; 109: 10861-6.
27. Alvarado D, Klein DE, Lemmon MA,. ErbB2 resembles an autoinhibited invertebrate epidermal growth factor receptor. Nature 2009; 461: 287-91.
28. Dejeans N, Glorieux C, Guenin S, et al., Overexpression of GRP94 in breast cancer cells resistant to oxidative stress promotes high levels of cancer cell proliferation and migration: implications for tumor recurrence. Free Radic Biol Med 2012; 52: 993-1002.
29. Sanz-Pamplona R, Aragüés R, Driouch K, et al., Expression of endoplasmic reticulum stress proteins is a candidate marker of brain metastasis in both ErbB-2+ and ErbB-2- primary breast tumors. Am J Pathol 2011; 179: 564-79.
30. Hodorova I, Rybarova S, Solar P, et al., Gp96 and its different expression in breast carcinomas. Neoplasma 2008; 55: 31-5.
31. Junutula JR, Flagella KM, Graham RA, et al., Engineered thio-trastuzumab-DM1 conjugate with an improved therapeutic index to target human epidermal growth factor receptor 2-positive breast cancer. Clin Cancer Res 2010; 16: 4769-78.
32. Park S, Jiang Z, Mortenson ED, et al., The therapeutic effect of anti-HER2/neu antibody depends on both innate and adaptive immunity. Cancer Cell 2010; 18: 160-70.
33. Sánchez-Martín M, Pandiella A,. Differential action of small molecule HER kinase inhibitors on receptor heterodimerization: therapeutic implications. Int J Cancer 2012; 131: 244-52.
34. Zheng FF, Kuduk SD, Chiosis G, et al., Identification of a geldanamycin dimer that induces the selective degradation of HER-family tyrosine kinases. Cancer Res 2000; 60: 2090-4.
35. Citri A, Alroy I, Lavi S, et al., Drug-induced ubiquitylation and degradation of ErbB receptor tyrosine kinases: implications for cancer therapy. EMBO J 2002; 21: 2407-17.
36. Neckers L,. Using natural product inhibitors to validate Hsp90 as a molecular target in cancer. Curr Top Med Chem 2006; 6: 1163-71.
37. Meng Q, Chen X, Sun L, et al., Carbamazepine promotes HER-2 protein degradation in breast cancer cells by modulating HDAC6 activity and acetylation of Hsp90. Mol Cell Biochem 2011; 348: 165-71.
38. Chandarlapaty S, Sawai A, Ye Q, et al., SNX2112, a synthetic heat shock protein 90 inhibitor, has potent antitumor activity against HER kinase-dependent cancers. Clin Cancer Res 2008; 14: 240-8.
39. Leow CC, Chesebrough J, Coffman KT, et al., Antitumor efficacy of IPI-504, a selective heat shock protein 90 inhibitor against human epidermal growth factor receptor 2-positive human xenograft models as a single agent and in combination with trastuzumab or lapatinib. Mol Cancer Ther 2009; 8: 2131-41.
40. Caldas-Lopes E, Cerchietti L, Ahn JH, et al., Hsp90 inhibitor PU-H71, a multimodal inhibitor of malignancy, induces complete responses in triple-negative breast cancer models. Proc Natl Acad Sci USA 2009; 106: 8368-73.
41. Han J, Hou W, Lu C, et al., Interaction between Her2 and Beclin-1 proteins underlies a new mechanism of reciprocal regulation. J Biol Chem 2013; 288: 20315-25.
42. Mittendorf EA, Liu Y, Tucker SL, et al., A novel interaction between HER2/neu and cyclin E in breast cancer. Oncogene 2010; 29: 3896-907.
43. Paris L, Cecchetti S, Spadaro F, et al., Inhibition of phosphatidylcholine-specific phospholipase C downregulates HER2 overexpression on plasma membrane of breast cancer cells. Breast Cancer Res 2010; 12: R27
44. Binder RJ, Srivastava PK,. Essential role of CD91 in re-presentation of gp96-chaperoned peptides. Proc Natl Acad Sci USA 2004; 101: 6128-33.
45. Zhao B, Wang Y, Zhang Y, et al., TAT-mediated gp96 transduction to APCs enhances gp96-induced antiviral and antitumor T cell responses. Vaccine 2013; 31: 545-52.
46. Kim G, Han JM, Kim S,. Toll-like receptor 4-mediated c-jun N-terminal kinase activation induces gp96 cell surface expression via AIMP1 phosphorylation. Biochem Biophys Res Commun 2010; 397: 100-5.
47. Han JM, Kwon NH, Lee JY, et al., Identification of gp96 as a novel target for treatment of autoimmune disease in mice. PLoS One 2010; 5: e9792.
48. Huang QQ, Pope RM,. The role of glycoprotein 96 in the persistent inflammation of rheumatoid arthritis. Arch Biochem Biophys 2013; 530: 1-6.
49. Rolhion N, Barnich N, Bringer MA, et al., Abnormally expressed ER stress response chaperone Gp96 in CD favours adherent-invasive Escherichia coli invasion. Gut 2010; 59: 1355-62.