Oncogenic Kras expression in postmitotic neurons leads to S100A8-S100A9 protein overexpression and gliosis

Journal of Biological Chemistry

Volumn 287, Issue 27, 2012, Pages 22948-22958

  Ryu, Myung Jeom ^a   Liu, Yangang ^a   Zhong, Xiaofen ^b   Du, Juan ^a   Peterson, Nicholas ^c   Kong, Guangyao ^a   Li, Hongda ^b,c   Wang, Jinyong ^a   Salamat, Shahriar ^d   Chang, Qiang ^b,c   Zhang, Jing ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SIGNALING; MAMMALS; MOLECULES;

ADVANCED GLYCATION END PRODUCTS; EXPRESSION PATTERNS; HYPERACTIVATION; MICROARRAY ANALYSIS; OVER-EXPRESSION; SECRETED MOLECULES; SIGNALING PATHWAYS; UP-REGULATION;

NEURONS;

CALGRANULIN A; CALGRANULIN B; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOMA; BIOACCUMULATION; BRAIN CORTEX; CARCINOGENESIS; CONTROLLED STUDY; EXPERIMENTAL MOUSE; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GLIOSIS; IN VITRO STUDY; MICROARRAY ANALYSIS; MICROGLIA; MITOSIS; MOUSE; NONHUMAN; ONCOGENE K RAS; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

MUS;

EID: 84863308353     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.357772     Document Type: Article

References (54)

1. Sharma, M. K., Zehnbauer, B. A., Watson, M. A., and Gutmann, D. H. (2005) RAS pathway activation and an oncogenic RAS mutation in sporadic pilocytic astrocytoma. Neurology 65, 1335-1336 (Pubitemid 41508250)
2. Gutmann, D. H. (2008) Using neurofibromatosis-1 to better understand and treat pediatric low grade glioma. J. Child Neurol. 23, 1186-1194
3. Gutmann, D. H., Donahoe, J., Brown, T., James, C. D., and Perry, A. (2000) Loss of neurofibromatosis 1 (NF1) gene expression in NF1-associated pilocytic astrocytomas. Neuropathol. Appl. Neurobiol. 26, 361-367 (Pubitemid 30609432)
4. Xu, G. F., O'Connell, P., Viskochil, D., Cawthon, R., Robertson, M., Culver, M., Dunn, D., Stevens, J., Gesteland, R., White, R., et al. (1990) The neurofibromatosis type 1 gene encodes a protein related to GAP. Cell 62, 599-608
5. Basu, T. N., Gutmann, D. H., Fletcher, J. A., Glover, T. W., Collins, F. S., and Downward, J. (1992) Aberrant regulation of ras proteins in malignant tumorcells from type 1 neurofibromatosis patients. Nature 356, 713-715
6. DeClue, J. E., Papageorge, A. G., Fletcher, J. A., Diehl, S. R., Ratner, N., Vass, W. C., and Lowy, D. R. (1992) Abnormal regulation of mammalian p21ras contributes to malignant tumor growth in von Recklinghausen (type 1) neurofibromatosis. Cell 69, 265-273
7. Sherman, L. S., Atit, R., Rosenbaum, T., Cox, A. D., and Ratner, N. (2000) Single cell Ras-GTP analysis reveals altered Ras activity in a subpopulation of neurofibroma Schwann cells but not fibroblasts. J. Biol. Chem. 275, 30740-30745
8. Lau, N., Feldkamp, M. M., Roncari, L., Loehr, A. H., Shannon, P., Gutmann, D. H., and Guha, A. (2000) Loss of neurofibromin is associated with activation of RAS/MAPK and PI3-K/AKT signaling in a neurofibromatosis 1 astrocytoma. J. Neuropathol. Exp. Neurol. 59, 759-767
9. Bollag, G., Clapp, D. W., Shih, S., Adler, F., Zhang, Y. Y., Thompson, P., Lange, B. J., Freedman, M. H., McCormick, F., Jacks, T., and Shannon, K. (1996) Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in hematopoietic cells. Nat. Genet. 12, 144-148 (Pubitemid 26051293)
10. Largaespada, D. A., Brannan, C. I., Jenkins, N. A., and Copeland, N. G. (1996) Nf1 deficiency causes Ras-mediated granulocyte/macrophage colony-stimulating factor hypersensitivity and chronic myeloid leukemia. Nat. Genet. 12, 137-143 (Pubitemid 26051292)
11. -/- cells. J. Biol. Chem. 276, 7240-7245
12. Dasgupta, B., Li, W., Perry, A., and Gutmann, D. H. (2005) Glioma formation in neurofibromatosis 1 reflects preferential activation of K-RAS in astrocytes. Cancer Res. 65, 236-245 (Pubitemid 40070815)
13. Janzarik, W. G., Kratz, C. P., Loges, N. T., Olbrich, H., Klein, C., Schäfer, T., Scheurlen, W., Roggendorf, W., Weiller, C., Niemeyer, C., Korinthenberg, R., Pfister, S., and Omran, H. (2007) Further evidence for a somatic KRAS mutation in a pilocytic astrocytoma. Neuropediatrics 38, 61-63 (Pubitemid 47434497)
14. Zhu, Y., Romero, M. I., Ghosh, P., Ye, Z., Charnay, P., Rushing, E. J., Marth, J. D., and Parada, L. F. (2001) Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev. 15, 859-876 (Pubitemid 32295067)
15. Riccardi, V. M. (1999) in Neurofibromatosis: Phenotypes, Natural History,and Pathogenesis (Friedman, J. M., Gutmann, D. H., MacCollin, M., and Riccardi, V. M., eds) pp. 1-25, John Hopkins Press, Baltimore, MD
16. Bajenaru, M. L., Zhu, Y., Hedrick, N. M., Donahoe, J., Parada, L. F., and Gutmann, D. H. (2002) Astrocyte-specific inactivation of the neurofibromatosis 1 gene (NF1) is insufficient for astrocytoma formation. Mol. Cell. Biol. 22, 5100-5113 (Pubitemid 34700701)
17. Bajenaru, M. L., Hernandez, M. R., Perry, A., Zhu, Y., Parada, L. F., Garbow, J. R., and Gutmann, D. H. (2003) Optic nerve glioma in mice requires astrocyte Nf1 gene inactivation and Nf1 brain heterozygosity. Cancer Res. 63, 8573-8577 (Pubitemid 38064027)
18. Ghavami, S., Chitayat, S., Hashemi, M., Eshraghi, M., Chazin, W. J., Halayko, A. J., and Kerkhoff, C. (2009) S100A8-S100A9. A Janus-faced molecule in cancer therapy and tumorigenesis. Eur. J. Pharmacol. 625, 73-83
19. Gebhardt, C., Németh, J., Angel, P., and Hess, J. (2006) S100A8 and S100A9 in inflammation and cancer. Biochem. Pharmacol. 72, 1622-1631 (Pubitemid 44666730)
20. Tuveson, D. A., Shaw, A. T., Willis, N. A., Silver, D. P., Jackson, E. L., Chang, S., Mercer, K. L., Grochow, R., Hock, H., Crowley, D., Hingorani, S. R., Zaks, T., King, C., Jacobetz, M. A., Wang, L., Bronson, R. T., Orkin, S. H., DePinho, R. A., and Jacks, T. (2004) Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 5, 375-387 (Pubitemid 38482073)
21. Fan, G., Beard, C., Chen, R. Z., Csankovszki, G., Sun, Y., Siniaia, M., Biniszkiewicz, D., Bates, B., Lee, P. P., Kuhn, R., Trumpp, A., Poon, C., Wilson, C. B., and Jaenisch, R. (2001) DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci. 21, 788-797 (Pubitemid 32163120)
22. Rios, M., Fan, G., Fekete, C., Kelly, J., Bates, B., Kuehn, R., Lechan, R. M., and Jaenisch, R. (2001) Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol. Endocrinol. 15, 1748-1757 (Pubitemid 32939305)
23. Vollrath, A. L., Smith, A. A., Craven, M., and Bradfield, C. A. (2009) EDGE(3). A web-based solution for management and analysis of Agilent two-color microarray experiments. BMC Bioinformatics 10, 280
24. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
25. Dennis, G., Jr., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., and Lempicki, R. A. (2003) DAVID. Database for annotation, visualization, and integrated discovery. Genome Biol. 4, P3
26. Ryu, M. J., Kim, D., Kang, U. B., Kim, J., Shin, H. S., Lee, C., and Yu, M. H. (2007) Proteomic analysis of γ-butyrolactone-treated mouse thalamus reveals dysregulated proteins upon absence seizure. J. Neurochem. 102, 646-656 (Pubitemid 47057274)
27. Cardona, A. E., Huang, D., Sasse, M. E., and Ransohoff, R. M. (2006) Isolation of murine microglial cells for RNA analysis or flow cytometry. Nat. Protoc. 1, 1947-1951 (Pubitemid 46773316)
28. Pino, P. A., and Cardona, A. E. (2011) Isolation of brain and spinal cord mononuclear cells using percoll gradients. J. Vis. Exp. 48, 2348
29. McCarthy, K. D., and de Vellis, J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902 (Pubitemid 10007455)
30. + T cells regulates TCR activation and experimental colitis in mice. J. Clin. Invest. 120, 570-581
31. Ghavami, S., Rashedi, I., Dattilo, B. M., Eshraghi, M., Chazin, W. J., Hashemi, M., Wesselborg, S., Kerkhoff, C., and Los, M. (2008) S100A8-S100A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J. Leukocyte Biol. 83, 1484-1492 (Pubitemid 351960330)
32. Kraig, R. P., Dong, L. M., Thisted, R., and Jaeger, C. B. (1991) Spreading depression increases immunohistochemical staining of glial fibrillary acidic protein. J. Neurosci. 11, 2187-2198
33. Steward, O., Torre, E. R., Tomasulo, R., and Lothman, E. (1991) Neuronal activity up-regulates astroglial gene expression. Proc. Natl. Acad. Sci. U.S.A. 88, 6819-6823 (Pubitemid 21915041)
34. Finco, T. S., Westwick, J. K., Norris, J. L., Beg, A. A., Der, C. J., and Baldwin, A. S., Jr. (1997) Oncogenic Ha-Ras-induced signaling activates NF-κB transcriptional activity, which is required for cellular transformation. J. Biol. Chem. 272, 24113-24116 (Pubitemid 27418602)
35. Mayo, M. W., Wang, C. Y., Cogswell, P. C., Rogers-Graham, K. S., Lowe, S. W., Der, C. J., and Baldwin, A. S., Jr. (1997) Requirement of NF-κB activation to suppress p53-independent apoptosis induced by oncogenic Ras. Science 278, 1812-1815 (Pubitemid 27527651)
36. Bassères, D. S., Ebbs, A., Levantini, E., and Baldwin, A. S. (2010) Requirement of the NF-κB subunit p65/RelA for K-Ras-induced lung tumorigenesis. Cancer Res. 70, 3537-3546
37. Mathias, R. A., Chen, Y. S., Wang, B., Ji, H., Kapp, E. A., Moritz, R. L., Zhu, H. J., and Simpson, R. J. (2010) Extracellular remodeling during oncogenic Ras-induced epithelial-mesenchymal transition facilitates MDCK cell migration. J. Proteome Res. 9, 1007-1019
38. Lackmann, M., Rajasekariah, P., Iismaa, S. E., Jones, G., Cornish, C. J., Hu, S., Simpson, R. J., Moritz, R. L., and Geczy, C. L. (1993) Identification of a chemotactic domain of the pro-inflammatory S100 protein CP-10. J. Immunol. 150, 2981-2991 (Pubitemid 23127547)
39. Devery, J. M., King, N. J., and Geczy, C. L. (1994) Acute inflammatory activity of the S100 protein CP-10. Activation of neutrophils in vivo and in vitro. J. Immunol. 152, 1888-1897 (Pubitemid 24075722)
40. Hobbs, J. A., May, R., Tanousis, K., McNeill, E., Mathies, M., Gebhardt, C., Henderson, R., Robinson, M. J., and Hogg, N. (2003) Myeloid cell function in MRP-14 (S100A9) null mice. Mol. Cell. Biol. 23, 2564-2576 (Pubitemid 36351035)
41. Roth, J., Vogl, T., Sunderkötter, C., and Sorg, C. (2003) Chemotactic activity of S100A8 and S100A9. J. Immunol. 171, 5651 (Pubitemid 37467175)
42. Watters, J. J., Schartner, J. M., and Badie, B. (2005) Microglia function in brain tumors. J. Neurosci. Res. 81, 447-455 (Pubitemid 41359299)
43. Ehrchen, J. M., Sunderkötter, C., Foell, D., Vogl, T., and Roth, J. (2009) The endogenous Toll-like receptor 4 agonist S100A8-S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J. Leukocyte Biol. 86, 557-566
44. Hermani, A., De Servi, B., Medunjanin, S., Tessier, P. A., and Mayer, D. (2006) S100A8 and S100A9 activate MAP kinase and NF-κB signaling pathways and trigger translocation of RAGE in human prostate cancer cells. Exp. Cell Res. 312, 184-197 (Pubitemid 41721180)
45. Ridet, J. L., Malhotra, S. K., Privat, A., and Gage, F. H. (1997) Reactive astrocytes. Cellular and molecular cues to biological function. Trends Neurosci. 20, 570-577 (Pubitemid 27508969)
46. Nordlund, M. L., Rizvi, T. A., Brannan, C. I., and Ratner, N. (1995) Neurofibromin expression and astrogliosis in neurofibromatosis (type 1) brains. J. Neuropathol. Exp. Neurol. 54, 588-600
47. Braun, B. S., Tuveson, D. A., Kong, N., Le, D. T., Kogan, S. C., Rozmus, J., Le Beau, M. M., Jacks, T. E., and Shannon, K. M. (2004) Somatic activation of oncogenic Kras in hematopoietic cells initiates a rapidly fatal myeloproliferative disorder. Proc. Natl. Acad. Sci. U.S.A. 101, 597-602 (Pubitemid 38084682)
48. Le, D. T., Kong, N., Zhu, Y., Lauchle, J. O., Aiyigari, A., Braun, B. S., Wang, E., Kogan, S. C., Le Beau, M. M., Parada, L., and Shannon, K. M. (2004) Somatic inactivation of Nf1 in hematopoietic cells results in a progressive myeloproliferative disorder. Blood 103, 4243-4250 (Pubitemid 38685370)
49. Zhang, J., Wang, J., Liu, Y., Sidik, H., Young, K. H., Lodish, H. F., and Fleming, M. D. (2009) Oncogenic Kras-induced leukemogenesis. Hematopoietic stem cells as the initial target and lineage-specific progenitors as the potential targets for final leukemic transformation. Blood 113, 1304-1314
50. Alcantara Llaguno, S., Chen, J., Kwon, C. H., Jackson, E. L., Li, Y., Burns, D. K., Alvarez-Buylla, A., and Parada, L. F. (2009) Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 15, 45-56
51. Abel, T. W., Clark, C., Bierie, B., Chytil, A., Aakre, M., Gorska, A., and Moses, H. L. (2009) GFAP-Cre-mediated activation of oncogenic K-ras results in expansion of the subventricular zone and infiltrating glioma. Mol. Cancer Res. 7, 645-653
52. Németh, J., Stein, I., Haag, D., Riehl, A., Longerich, T., Horwitz, E., Breuhahn, K., Gebhardt, C., Schirmacher, P., Hahn, M., Ben-Neriah, Y., Pikarsky, E., Angel, P., and Hess, J. (2009) S100A8 and S100A9 are novel nuclear factor-κB target genes during malignant progression of murine and human liver carcinogenesis. Hepatology 50, 1251-1262
53. Ichikawa, M., Williams, R., Wang, L., Vogl, T., and Srikrishna, G. (2011) S100A8-S100A9 activate key genes and pathways in colon tumor progression. Mol. Cancer Res. 9, 133-148
54. Hiratsuka, S., Watanabe, A., Aburatani, H., and Maru, Y. (2006) Tumor-mediated up-regulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 8, 1369-1375 (Pubitemid 44835111)