A critical role for GRP78/BiP in the tumor microenvironment for neovascularization during tumor growth and metastasis

Cancer Research

Volumn 71, Issue 8, 2011, Pages 2848-2857

  Dong, Dezheng ^a   Stapleton, Christopher ^b,e   Luo, Biquan ^a   Xiong, Shigang ^c   Ye, Wei ^d   Zhang, Yi ^a   Jhaveri, Niyati ^b   Zhu, Genyuan ^a   Ye, Risheng ^a   Liu, Zhi ^b   Bruhn, Kevin W ^f   Craft, Noah ^f   Groshen, Susan ^d   Hofman, Florence M ^b   Lee, Amy S ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c University School of Medicine   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f HARBOR UCLA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE REGULATED PROTEIN 78;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIUM CELL; GROWTH INHIBITION; HETEROZYGOSITY; HUMAN; HUMAN CELL; MELANOMA CELL; METASTASIS; METASTASIS INHIBITION; MIGRATION INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

ANIMALS; APOPTOSIS; CELL GROWTH PROCESSES; CELL MOVEMENT; ENDOTHELIAL CELLS; FEMALE; HEAT-SHOCK PROTEINS; HETEROZYGOTE; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; TUMOR MICROENVIRONMENT;

EID: 79954569520     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3151     Document Type: Article

References (38)

1. Ni M, Lee AS. ER chaperones in mammalian development and human diseases. FEBS Lett 2007;581:3641-51. (Pubitemid 47082516)
2. Pfaffenbach KT, Lee AS. The critical role of GRP78 in physiologic and pathologic stress. CurrOpinCell Biol2010Oct21. [Epubaheadof print].
3. Lee AS. GRP78 induction in cancer: Therapeutic and prognostic implications. Cancer Res 2007;67:3496-9. (Pubitemid 46762126)
4. Zhang Y, Liu R, Ni M, Gill P, Lee AS. Cell surface relocalization of the endoplasmic reticulum chaperone and unfolded protein response regulator GRP78/BiP. J Biol Chem 2010;285:15065-75.
5. Shani G, Fischer WH, Justice NJ, Kelber JA, Vale W, Gray PC. GRP78 and Cripto form a complex at the cell surface and collaborate to inhibit transforming growth factor beta signaling and enhance cell growth. Mol Cell Biol 2008;28:666-77.
6. Gonzalez-Gronow M, Selim MA, Papalas J, Pizzo SV. GRP78: A multifunctional receptor on the cell surface. Antioxid Redox Signal 2009;11:2299-306.
7. Ni M, Zhang Y, Lee AS. Beyond the endoplasmic reticulum: Atypical GRP78 in cell viability, signaling and therapeutic targeting. Biochem J 2011;434:181-8.
8. Wang M, Wey S, Zhang Y, Ye R, Lee AS. Role of the unfolded protein response regulator GRP78/BiP in development, cancer, and neurological disorders. Antioxid Redox Signal 2009;11:2307-16.
9. Li J, Lee AS. Stress induction of GRP78/BiP and its role in cancer. Curr Mol Med 2006;6:45-54.
10. Luo S, Mao C, Lee B, Lee AS. GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol Cell Biol 2006;26:5688-97. (Pubitemid 44134326)
11. Dong D, Ni M, Li J, Xiong S, Ye W, Virrey JJ, et al. Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res 2008;68:498-505. (Pubitemid 351380077)
12. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003;3:401-10. (Pubitemid 37328844)
13. Folkman J. The role of angiogenesis in tumor growth. Semin Cancer Biol 1992;3:65-71.
14. Charalambous C, Chen TC, Hofman FM. Characteristics of tumorassociated endothelial cells derived from glioblastoma multiforme. Neurosurg Focus 2006;20:E22.
15. Virrey JJ, Dong D, Stiles C, Patterson JB, Pen L, Ni M, et al. Stress chaperone GRP78/BiP confers chemoresistance to tumor-associated endothelial cells. Mol Cancer Res 2008;6:1268-75.
16. Ewens A, Luo L, Berleth E, Alderfer J, Wollman R, Hafeez BB, et al. Doxorubicin plus interleukin-2 chemoimmunotherapy against breast cancer in mice. Cancer Res 2006;66:5419-26. (Pubitemid 43844969)
17. Wang M, Ye R, Barron E, Baumeister P, Mao C, Luo S, et al. Essential role of the unfolded protein response regulator GRP78/BiP in protection from neuronal apoptosis. Cell Death Differ 2010;17:488-98.
18. Koni PA, Joshi SK, Temann UA, Olson D, Burkly L, Flavell RA. Conditional vascular cell adhesion molecule 1 deletion in mice: Impaired lymphocyte migration to bone marrow. J Exp Med 2001;193: 741-54.
19. Wu Z, Hofman FM, Zlokovic BV. A simple method for isolation and characterization of mouse brain microvascular endothelial cells. J Neurosci Methods 2003;130:53-63. (Pubitemid 37315929)
20. Perriere N, Demeuse P, Garcia E, Regina A, Debray M, Andreux JP, et al. Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J Neurochem 2005;93:279-89. (Pubitemid 40547485)
21. Fu Y, Wey S, Wang M, Ye R, Liao CP, Roy-Burman P, et al. Pten null prostate tumorigenesis and AKT activation are blocked by targeted knockout of ER chaperone GRP78/BiP in prostate epithelium. Proc Natl Acad Sci U S A 2008;105:19444-9.
22. Kim KJ, Li B, Winer J, Armanini M, Gillett N, Phillips HS, et al. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 1993;362:841-4. (Pubitemid 23132159)
23. Craft N, Bruhn KW, Nguyen BD, Prins R, Liau LM, Collisson EA, et al. Bioluminescent imaging of melanoma in live mice. J Invest Dermatol 2005;125:159-65. (Pubitemid 40981437)
24. Hamada K, Sasaki T, Koni PA, Natsui M, Kishimoto H, Sasaki J, et al. The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis. Genes Dev 2005;19:2054-65. (Pubitemid 41247962)
25. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, Bosse DC, et al. HMEC-1: Establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 1992;99:683-90. (Pubitemid 23002027)
26. Pyrko P, Schonthal AH, Hofman FM, Chen TC, Lee AS. The unfolded protein response regulator GRP78/BiP as a novel target for increasing chemosensitivity in malignant gliomas. Cancer Res 2007;67:9809-16. (Pubitemid 47621228)
27. Baumeister P, Dong D, Fu Y, Lee AS. Transcriptional induction of GRP78/BiP by histone deacetylase inhibitors and resistance to histone deacetylase inhibitor-induced apoptosis. Mol Cancer Ther 2009;8:1086-94.
28. Hendershot LM. The ER function BiP is a master regulator of ER function. Mt Sinai J Med 2004;71:289-97.
29. Davidson DJ, Haskell C, Majest S, Kherzai A, Egan DA, Walter KA, et al. Kringle 5 of human plasminogen induces apoptosis of endothelial and tumor cells through surface-expressed glucose-regulated protein 78. Cancer Res 2005;65:4663-72. (Pubitemid 40740802)
30. Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: Role of ATP binding site in suppression of caspase-7 activation. J Biol Chem 2003;278: 20915-24. (Pubitemid 36806399)
31. Katanasaka Y, Ishii T, Asai T, Naitou H, Maeda N, Koizumi F, et al. Cancer antineovascular therapy with liposome drug delivery systems targeted to BiP/GRP78. Int J Cancer 2010;127:2685-98.
32. McFarland BC, Stewart J Jr, Hamza A, Nordal R, Davidson DJ, Henkin J, et al. Plasminogen Kringle 5 induces apoptosis of brain microvessel endothelial cells: Sensitization by radiation and requirement for GRP78 and LRP1. Cancer Res 2009;69:5537-45.
33. Bruneel A, Labas V, Mailloux A, Sharma S, Royer N, Vinh J, et al. Proteomics of human umbilical vein endothelial cells applied to etoposide- induced apoptosis. Proteomics 2005;5:3876-84. (Pubitemid 41502484)
34. Kern J, Untergasser G, Zenzmaier C, Sarg B, Gastl G, Gunsilius E, et al. GRP-78 secreted by tumor cells blocks the antiangiogenic activity of bortezomib. Blood 2009;114:3960-7.
35. Patenaude A, Parker J, Karsan A. Involvement of endothelial progenitor cells in tumor vascularization. Microvasc Res 2010;79:217-23.
36. Xu L, Duda DG, di Tomaso E, Ancukiewicz M, Chung DC, Lauwers GY, et al. Direct evidence that bevacizumab, an anti-VEGF antibody, upregulates SDF1alpha, CXCR4, CXCL6, and neuropilin 1 in tumors from patients with rectal cancer. Cancer Res 2009;69:7905-10.
37. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009;15:220-31.
38. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-9.