Induction of Bv8 Expression by granulocyte colony-stimulating factor in CD11b+Gr1+ cells: Key role of Stat3 signaling

Journal of Biological Chemistry

Volumn 287, Issue 23, 2012, Pages 19574-19584

  Qu, Xueping ^a   Zhuang, Guanglei ^a   Yu, Lanlan ^a   Meng, Gloria ^a   Ferrara, Napoleone ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN IMMUNOPRECIPITATION; EXTRACELLULAR SIGNAL-REGULATED KINASE; GRANULOCYTE-COLONY STIMULATING FACTOR; HUMAN BONE MARROW CELLS; IN-VITRO; IN-VIVO; KEY REGULATORS; LUCIFERASE ASSAYS; MOUSE BONE MARROW CELLS; MYELOID CELLS; PHARMACOLOGICAL INHIBITORS; PRE-TREATMENT; PRIMARY CELLS; PROKINETICIN 2; SIGNAL TRANSDUCERS; SIGNALING PATHWAYS; TUMOR ANGIOGENESIS; TUMORIGENESIS; UP-REGULATION;

CELL CULTURE; CELL PROLIFERATION; CHEMICAL ACTIVATION; SIGNALING;

CELLS;

BV8 PROTEIN; CD11B ANTIGEN; CELL PROTEIN; GRANULOCYTE COLONY STIMULATING FACTOR; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN INHIBITOR; SMALL INTERFERING RNA; STAT3 PROTEIN; UNCLASSIFIED DRUG; WP 1066;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; BONE MARROW CELL; CELL POPULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENHANCER REGION; ENZYME ACTIVATION; ENZYME ASSAY; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTIGENS, CD11B; BONE MARROW CELLS; CELLS, CULTURED; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GASTROINTESTINAL HORMONES; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GRANULOCYTE COLONY-STIMULATING FACTOR; HUMANS; MICE; MICE, INBRED BALB C; NEUROPEPTIDES; PROMOTER REGIONS, GENETIC; PYRIDINES; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TYRPHOSTINS;

EID: 84861728918     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.326801     Document Type: Article

References (50)

1. Li, M., Bullock, C. M., Knauer, D. J., Ehlert, F. J., and Zhou, Q. Y. (2001) Identification of two prokineticin cDNAs: recombinant proteins potently contract gastrointestinal smooth muscle. Mol. Pharmacol. 59, 692-698 (Pubitemid 32273997)
2. LeCouter, J., Kowalski, J., Foster, J., Hass, P., Zhang, Z., Dillard-Telm, L., Frantz, G., Rangell, L., DeGuzman, L., Keller, G. A., Peale, F., Gurney, A., Hillan, K. J., and Ferrara, N. (2001) Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 412, 877-884 (Pubitemid 32821726)
3. Mollay, C., Wechselberger, C., Mignogna, G., Negri, L., Melchiorri, P., Barra, D., and Kreil, G. (1999) Bv8, a small protein from frog skin and its homologue from snake venom induce hyperalgesia in rats. Eur. J. Pharmacol. 374, 189-196 (Pubitemid 29287133)
4. Masuda, Y., Takatsu, Y., Terao, Y., Kumano, S., Ishibashi, Y., Suenaga, M., Abe, M., Fukusumi, S., Watanabe, T., Shintani, Y., Yamada, T., Hinuma, S., Inatomi, N., Ohtaki, T., Onda, H., and Fujino, M. (2002) Isolation and identification of EG-VEGF/prokineticins as cognate ligands for two orphan G-protein-coupled receptors. Biochem. Biophys. Res. Commun. 293, 396-402 (Pubitemid 34694220)
5. Lin, D. C., Bullock, C. M., Ehlert, F. J., Chen, J. L., Tian, H., and Zhou, Q. Y. (2002) Identification and molecular characterization of two closely related G-protein-coupled receptors activated by prokineticins/endocrine gland vascular endothelial growth factor. J. Biol. Chem. 277, 19276-19280 (Pubitemid 34967431)
6. Melchiorri, D., Bruno, V., Besong, G., Ngomba, R. T., Cuomo, L., De Blasi, A., Copani, A., Moschella, C., Storto, M., Nicoletti, F., Lepperdinger, G., and Passarelli, F. (2001) The mammalian homologue of the novel peptide Bv8 is expressed in the central nervous system and supports neuronal survival by activating the MAP kinase/PI 3-kinase pathways. Eur. J. Neurosci. 13, 1694-1702 (Pubitemid 32488059)
7. Cheng, M. Y., Bullock, C. M., Li, C., Lee, A. G., Bermak, J. C., Belluzzi, J., Weaver, D. R., Leslie, F. M., and Zhou, Q. Y. (2002) Prokineticin 2 transmits the behavioral circadian rhythm of the suprachiasmatic nucleus. Nature 417, 405-410 (Pubitemid 34563527)
8. LeCouter, J., Lin, R., Tejada, M., Frantz, G., Peale, F., Hillan, K. J., and Ferrara, N. (2003) The endocrine-gland-derived VEGF homologue Bv8 promotes angiogenesis in the testis: localization of Bv8 receptors to endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 100, 2685-2690 (Pubitemid 36297559)
9. LeCouter, J., Zlot, C., Tejada, M., Peale, F., and Ferrara, N. (2004) Bv8 and endocrine gland-derived vascular endothelial growth factor stimulate hematopoiesis and hematopoietic cell mobilization. Proc. Natl. Acad. Sci. U.S.A. 101, 16813-16818 (Pubitemid 39601321)
10. Giannini, E., Lattanzi, R., Nicotra, A., Campese, A. F., Grazioli, P., Screpanti, I., Balboni, G., Salvadori, S., Sacerdote, P., and Negri, L. (2009) The chemokine Bv8/prokineticin 2 is up-regulated in inflammatory granulocytes and modulates inflammatory pain. Proc. Natl. Acad. Sci. U.S.A. 106, 14646-14651
11. Shojaei, F., Wu, X., Zhong, C., Yu, L., Liang, X. H., Yao, J., Blanchard, D., Bais, C., Peale, F. V., van Bruggen, N., Ho, C., Ross, J., Tan, M., Carano, R. A., Meng, Y. G., and Ferrara, N. (2007) Bv8 regulates myeloid cell-dependent tumor angiogenesis. Nature 450, 825-831 (Pubitemid 350231321)
12. Shojaei, F., Singh, M., Thompson, J. D., and Ferrara, N. (2008) Role of Bv8 in neutrophil-dependent angiogenesis in a transgenic model of cancer progression. Proc. Natl. Acad. Sci. U.S.A. 105, 2640-2645 (Pubitemid 351520566)
13. Christopher, M. J., and Link, D. C. (2007) Regulation of neutrophil homeostasis. Curr. Opin. Hematol. 14, 3-8 (Pubitemid 44885605)
14. Smith, T. J., Khatcheressian, J., Lyman, G. H., Ozer, H., Armitage, J. O., Balducci, L., Bennett, C. L., Cantor, S. B., Crawford, J., Cross, S. J., Demetri, G., Desch, C. E., Pizzo, P. A., Schiffer, C. A., Schwartzberg, L., Somerfield, M. R., Somlo, G., Wade, J. C., Wade, J. L., Winn, R. J., Wozniak, A. J., and Wolff, A. C. (2006) 2006 update of recommendations for the use of white blood cell growth factors: an evidence-based clinical practice guideline. J. Clin. Oncol. 24, 3187-3205 (Pubitemid 46638957)
15. Okazaki, T., Ebihara, S., Asada, M., Kanda, A., Sasaki, H., and Yamaya, M. (2006) Granulocyte colony-stimulating factor promotes tumor angiogenesis via increasing circulating endothelial progenitor cells and Gr1+CD11b+ cells in cancer animal models. Int. Immunol. 18, 1-9 (Pubitemid 43057031)
16. Voloshin, T., Gingis-Velitski, S., Bril, R., Benayoun, L., Munster, M., Milsom, C., Man, S., Kerbel, R. S., and Shaked, Y. (2011) G-CSF supplementation with chemotherapy can promote revascularization and subsequent tumor regrowth: prevention by a CXCR4 antagonist. Blood 118, 3426-3435
17. Natori, T., Sata, M., Washida, M., Hirata, Y., Nagai, R., and Makuuchi, M. (2002) G-CSF stimulates angiogenesis and promotes tumor growth: potential contribution of bone marrow-derived endothelial progenitor cells. Biochem. Biophys. Res. Commun. 297, 1058-1061 (Pubitemid 35230360)
18. Shojaei, F., Wu, X., Qu, X., Kowanetz, M., Yu, L., Tan, M., Meng, Y. G., and Ferrara, N. (2009) G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc. Natl. Acad. Sci. U.S.A. 106, 6742-6747
19. Yu, H., Pardoll, D., and Jove, R. (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 9, 798-809
20. Kujawski, M., Kortylewski, M., Lee, H., Herrmann, A., Kay, H., and Yu, H. (2008) Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J. Clin. Invest. 118, 3367-3377
21. Bollrath, J., Phesse, T. J., von Burstin, V. A., Putoczki, T., Bennecke, M., Bateman, T., Nebelsiek, T., Lundgren-May, T., Canli, O., Schwitalla, S., Matthews, V., Schmid, R. M., Kirchner, T., Arkan, M. C., Ernst, M., and Greten, F. R. (2009) gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell cycle progression during colitis-associated tumorigenesis. Cancer Cell 15, 91-102
22. Kortylewski, M., Xin, H., Kujawski, M., Lee, H., Liu, Y., Harris, T., Drake, C., Pardoll, D., and Yu, H. (2009) Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment. Cancer Cell 15, 114-123
23. Zhong, C., Qu, X., Tan, M., Meng, Y. G., and Ferrara, N. (2009) Characterization and regulation of Bv8 in human blood cells. Clin. Cancer Res. 15, 2675-2684
24. Avalos, B. R. (1996) Molecular analysis of the granulocyte colony-stimulating factor receptor. Blood 88, 761-777
25. Kamezaki, K., Shimoda, K., Numata, A., Haro, T., Kakumitsu, H., Yoshie, M., Yamamoto, M., Takeda, K., Matsuda, T., Akira, S., Ogawa, K., and Harada, M. (2005) Roles of Stat3 and ERK in G-CSF signaling. Stem Cells 23, 252-263 (Pubitemid 40239520)
26. Frémin, C., and Meloche, S. (2010) From basic research to clinical development of MEK1/2 inhibitors for cancer therapy. J. Hematol. Oncol. 3, 8
27. Johnston, S. (2007) AACR-NCI-EORTC Symposium on Molecular Targets and Cancer Therapeutics, San Francisco, CA, October 22-26, 2007, Abstract No. C209, American Association for Cancer Research, Philadelphia, PA
28. Iwamaru, A., Szymanski, S., Iwado, E., Aoki, H., Yokoyama, T., Fokt, I., Hess, K., Conrad, C., Madden, T., Sawaya, R., Kondo, S., Priebe, W., and Kondo, Y. (2007) A novel inhibitor of the STAT3 pathway induces apoptosis in malignant glioma cells both in vitro and in vivo. Oncogene 26, 2435-2444 (Pubitemid 46597261)
29. Chung, A. S., Lee, J., and Ferrara, N. (2010) Targeting the tumor vasculature: insights from physiological angiogenesis. Nat. Rev. Cancer 10, 505-514
30. Ferrara, N., Mass, R. D., Campa, C., and Kim, R. (2007) Targeting VEGF-A to treat cancer and age-related macular degeneration. Annu. Rev. Med. 58, 491-504 (Pubitemid 46706529)
31. Carmeliet, P. (2003) Angiogenesis in health and disease. Nat. Med. 9, 653-660
32. Kerbel, R. S. (2008) Tumor angiogenesis. N. Engl. J. Med. 358, 2039-2049
33. Ferrara, N. (2004) Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 25, 581-611
34. Lin, W. W., and Karin, M. (2007) A cytokine-mediated link between innate immunity, inflammation, and cancer. J. Clin. Invest. 117, 1175-1183
35. Coussens, L. M., and Werb, Z. (2002) Inflammation and cancer. Nature 420, 860-867 (Pubitemid 36019639)
36. Karnoub, A. E., Dash, A. B., Vo, A. P., Sullivan, A., Brooks, M. W., Bell, G. W., Richardson, A. L., Polyak, K., Tubo, R., and Weinberg, R. A. (2007) Mesenchymal stem cells within tumor stroma promote breast cancer metastasis. Nature 449, 557-563 (Pubitemid 47525152)
37. Orimo, A., and Weinberg, R. A. (2006) Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle 5, 1597-1601 (Pubitemid 44285243)
38. Shaked, Y., and Voest, E. E. (2009) Bone marrow-derived cells in tumor angiogenesis and growth: are they the good, the bad, or the evil? Biochim. Biophys. Acta 1796, 1-4
39. Gabrilovich, D. I., and Nagaraj, S. (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-174
40. Shojaei, F., Zhong, C., Wu, X., Yu, L., and Ferrara, N. (2008) Role of myeloid cells in tumor angiogenesis and growth. Trends Cell Biol. 18, 372-378
41. + myeloid cells. Nat. Biotechnol. 25, 911-920
42. +granulocytes. Proc. Natl. Acad. Sci. U.S.A. 107, 21248-21255
43. Meraz, M. A., White, J. M., Sheehan, K. C., Bach, E. A., Rodig, S. J., Dighe, A. S., Kaplan, D. H., Riley, J. K., Greenlund, A. C., Campbell, D., Carver-Moore, K., DuBois, R. N., Clark, R., Aguet, M., and Schreiber, R. D. (1996) Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84, 431-442 (Pubitemid 26058568)
44. Thierfelder, W. E., van Deursen, J. M., Yamamoto, K., Tripp, R. A., Sarawar, S. R., Carson, R. T., Sangster, M. Y., Vignali, D. A., Doherty, P. C., Grosveld, G. C., and Ihle, J. N. (1996) Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature 382, 171-174 (Pubitemid 26242884)
45. Teglund, S., McKay, C., Schuetz, E., van Deursen, J. M., Stravopodis, D., Wang, D., Brown, M., Bodner, S., Grosveld, G., and Ihle, J. N. (1998) Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 93, 841-850 (Pubitemid 28257589)
46. Takeda, K., Tanaka, T., Shi, W., Matsumoto, M., Minami, M., Kashiwamura, S., Nakanishi, K., Yoshida, N., Kishimoto, T., and Akira, S. (1996) Essential role of Stat6 in IL-4 signaling. Nature 380, 627-630 (Pubitemid 26119015)
47. Nicholson, S. E., Novak, U., Ziegler, S. F., and Layton, J. E. (1995) Distinct regions of the granulocyte colony-stimulating factor receptor are required for tyrosine phosphorylation of the signaling molecules JAK2, Stat3, and p42, p44MAPK. Blood 86, 3698-3704
48. Tian, S. S., Lamb, P., Seidel, H. M., Stein, R. B., and Rosen, J. (1994) Rapid activation of the STAT3 transcription factor by granulocyte colony-stimulating factor. Blood 84, 1760-1764
49. McLemore, M. L., Grewal, S., Liu, F., Archambault, A., Poursine-Laurent, J., Haug, J., and Link, D. C. (2001) STAT-3 activation is required for normal G-CSF-dependent proliferation and granulocytic differentiation. Immunity 14, 193-204 (Pubitemid 32206521)
50. Belvin, M., Chan, I. T., Friedman, L., Hoeflich, K. P., Prescott, J., and Wallin, J. (April 14, 2011) U. S. Patent 20,110,086,837