Complement membrane attack and tumorigenesis a systems biology approach

Journal of Biological Chemistry

Volumn 291, Issue 29, 2016, Pages 14927-14938

  Towner, Laurence D ^a,b   Wheat, Richard A ^a   Hughes, Timothy R ^a   PaulMorgan, B ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b THOMSON REUTERS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; CELL DEATH; CHEMICAL ACTIVATION; COMPLEX NETWORKS; GENES; TUMORS;

CO-REGULATED GENES; EXTRACELLULAR SPACE; GENE EXPRESSION SIGNATURES; GENE EXPRESSION STUDIES; INFLAMMATORY CYTOKINES; MEMBRANE ATTACK COMPLEXES; RECEPTOR ACTIVATION; THERAPEUTIC STRATEGY;

GENE EXPRESSION;

COMPLEMENT MEMBRANE ATTACK COMPLEX; EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; EXTRACELLULAR SPACE; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATOR GENE; STROMA; SYSTEMS BIOLOGY; TRANSCRIPTION REGULATION; TUMOR CELL; TUMOR GROWTH; TUMOR PROMOTION; ALGORITHM; ANIMAL; BIOLOGICAL MODEL; CELL TRANSFORMATION; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GENETICS; IMMUNOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ALGORITHMS; ANIMALS; CARCINOGENESIS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; COMPLEMENT MEMBRANE ATTACK COMPLEX; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HUMANS; MODELS, IMMUNOLOGICAL; REAL-TIME POLYMERASE CHAIN REACTION; SYSTEMS BIOLOGY;

EID: 84978371314     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.708446     Document Type: Article

References (77)

1. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
2. Walport, M. J. (2001) Complement: first of two parts. N. Engl. J. Med. 344, 1058-1066
3. Monk, P. N., Scola, A. M., Madala, P., and Fairlie, D. P. (2007) Function, structure and therapeutic potential of complement C5a receptors. Br. J. Pharmacol. 152, 429- 448
4. Müller-Eberhard, H. J. (1986) The membrane attack complex of complement. Annu. Rev. Immunol. 4, 503-528
5. Morgan, B. P. (1989) Complement membrane attack on nucleated cells: resistance, recovery, and non-lethal effects. Biochem. J. 264, 1-14
6. Cole, D. S., and Morgan, B. P. (2003) Beyond lysis: how complement influences cell fate. Clin. Sci. 104, 455-466
7. Taylor, R. P., and Lindorfer, M. A. (2014) The role of complement in mAb-based therapies of cancer. Methods 65, 18-27
8. Pio, R., Ajona, D., and Lambris, J. D. (2013) Complement inhibition in cancer therapy. Semin. Immunol. 25, 54-64
9. Niculescu, F., Rus, H. G., Retegan, M., and Vlaicu, R. (1992) Persistent complement activation on tumor cells in breast cancer. Am. J. Pathol. 140, 1039-1043
10. Lucas, S. D., Karlsson-Parra, A., Nilsson, B., Grimelius, L., Akerström, G., Rastad, J., and Juhlin, C. (1996) Tumor-specific deposition of immunoglobulin g and complement in papillary thyroid carcinoma. Hum. Pathol. 27, 1329-1335
11. Yamakawa, M., Yamada, K., Tsuge, T., Ohrui, H., Ogata, T., Dobashi, M., and Imai, Y. (1994) Protection of thyroid-cancer cells by complementregulatory factors. Cancer 73, 2808-2817
12. Ytting, H., Jensenius, J. C., Christensen, I. J., Thiel, S., and Nielsen, H. J. (2004) Increased activity of the mannan-binding lectin complement activation pathway in patients with colorectal cancer. Scand. J. Gastroenterol. 39, 674-679
13. Bjørge, L., Hakulinen, J., Vintermyr, O. K., Jarva, H., Jensen, T. S., Iversen, O. E., and Meri, S. (2005) Ascitic complement system in ovarian cancer. Br. J. Cancer 92, 895-905
14. Markiewski, M. M., DeAngelis, R. A., Benencia, F., Ricklin-Lichtsteiner, S. K., Koutoulaki, A., Gerard, C., Coukos, G., and Lambris, J. D. (2008) Modulation of the antitumor immune response by complement. Nat. Immunol. 9, 1225-1235
15. Corrales, L., Ajona, D., Rafail, S., Lasarte, J. J., Riezu-Boj, J. I., Lambris, J. D., Rouzaut, A., Pajares, M. J., Montuenga, L. M., and Pio, R. (2012) Anaphylatoxin C5a creates a favorable microenvironment for lung cancer progression. J. Immunol. 189, 4674-4683
16. Gunn, L., Ding, C., Liu, M., Ma, Y., Qi, C., Cai, Y., Hu, X., Aggarwal, D., Zhang, H. G., and Yan, J. (2012) Opposing roles for complement component C5A in tumor progression and the tumor microenvironment. J. Immunol. 189, 2985-2994
17. O'Barr, S. A., Caguioa, J., Gruol, D., Perkins, G., Ember, J. A., Hugli, T., and Cooper, N. R. (2001) Neuronal expression of a functional receptor for the C5a complement activation fragment. J. Immunol. 166, 4154-4162
18. Rutkowski, M. J., Sughrue, M. E., Kane, A. J., Mills, S. A., and Parsa, A. T. (2010) Cancer and the complement cascade. Mol. Cancer Res. 8, 1453-1465
19. Pio, R., Corrales, L., and Lambris, J. D. (2014) The role of complement in tumor growth. in Tumor Microenvironment and Cellular Stress: Signaling, Metabolism, Imaging, and Therapeutic Targets (Koumenis, C., Hammond, E., and Giaccia, A. eds.), pp 229-262, Springer-Verlag New York Inc., New York
20. Markiewski, M. M., and Lambris, J. D. (2009) Unwelcome Complement. Cancer Res. 69, 6367-6370
21. Markiewski, M. M., and Lambris, J. D. (2009) Is complement good or bad for cancer patients? A new perspective on an old dilemma. Trends Immunol. 30, 286-292
22. Fishelson, Z., Donin, N., Zell, S., Schultz, S., and Kirschfink, M. (2003) Obstacles to cancer immunotherapy: expression of membrane complement regulatory proteins (mCRPs) in tumors. Mol. Immunol. 40, 109-123
23. Campbell, A. K., Daw, R. A., and Luzio, J. P. (1979) Rapid increase in intracellular free Ca2+ induced by antibody plus complement. FEBS Lett. 107, 55-60
24. Lo, T. N., and Boyle, M. D. (1979) Relationship between the intracellular cyclic adenosine 3′:5′-monophosphate level of tumor cells and their sensitivity to killing by antibody and complement. Cancer Res. 39, 3156-3162
25. Hänsch, G. M., Seitz, M., and Betz, M. (1987) Effect of the late complement components-C5b-9 on human monocytes: release of prostanoids, oxygen radicals, and of a factor inducing cell-proliferation. Int. Arch. Allergy Appl. Immunol. 82, 317-320
26. Kilgore, K. S., Shen, J. P., Miller, B. F., Ward, P. A., and Warren, J. S. (1995) Enhancement by the complement membrane attack complex of tumor necrosis factor-α-induced endothelial-cell expression of E-selectin and ICAM-1. J. Immunol. 155, 1434-1441
27. Benzaquen, L. R., Nicholson-Weller, A., and Halperin, J. A. (1994) Terminal complement proteins C5b-9 release basic fibroblast growth-factor and platelet-derived growth-factor from endothelial-cells. J. Exp. Med. 179, 985-992
28. Fosbrink, M., Niculescu, F., Rus, V., Shin, M. L., and Rus, H. (2006) C5b-9-induced endothelial cell proliferation and migration are dependent on Akt inactivation of forkhead transcription factor FOXO1. J. Biol. Chem. 281, 19009-19018
29. Wagner, C., Braunger, M., Beer, M., Rother, K., and Hänsch, G. M. (1994) Induction of matrix protein-synthesis in human glomerular mesangial cells by the terminal complement complex. Exp. Nephrol. 2, 51-56
30. Lueck, K., Wasmuth, S., Williams, J., Hughes, T. R., Morgan, B. P., Lommatzsch, A., Greenwood, J., Moss, S. E., and Pauleikhoff, D. (2011) Sublytic C5b-9 induces functional changes in retinal pigment epithelial cells consistent with age-related macular degeneration. Eye 25, 1074-1082
31. Halperin, J. A., Taratuska, A., and Nicholson-Weller, A. (1993) Terminal complement complex C5b-9 stimulates mitogenesis in 3T3 cells. J. Clin. Invest. 91, 1974-1978
32. Rus, H. G., Niculescu, F., and Shin, M. L. (1996) Sublytic complement attack induces cell cycle oligodendrocytes: S phase induction is dependent on c-jun activation. J. Immunol. 156, 4892-4900
33. Hila, S., Soane, L., and Koski, C. L. (2001) Sublytic C5b-9-stimulated Schwann cell survival through PI 3-kinase-mediated phosphorylation of BAD. Glia 36, 58-67
34. Liu, L., Qiu, W., Wang, H., Li, Y., Zhou, J., Xia, M., Shan, K., Pang, R., Zhou, Y., Zhao, D., and Wang, Y. (2012) Sublytic C5b-9 Complexes induce apoptosis of glomerular mesangial cells in rats with Thy-1 nephritis through role of interferon regulatory factor-1-dependent caspase 8 activation. J. Biol. Chem. 287, 16410-16423
35. Triantafilou, K., Hughes, T. R., Triantafilou, M., and Morgan, B. P. (2013) The complement membrane attack complex triggers intracellular Ca2+ fluxes leading to NLRP3 inflammasome activation. J. Cell Sci. 126, 2903-2913
36. Nunn, M. A., Sharma, A., Paesen, G. C., Adamson, S., Lissina, O., Willis, A. C., and Nuttall, P. A. (2005) Complement inhibitor of C5 activation from the soft tick Ornithodoros moubata. J. Immunol. 174, 2084-2091
37. Hepburn, N. J., Williams, A. S., Nunn, M. A., Chamberlain-Banoub, J. C., Hamer, J., Morgan, B. P., and Harris, C. L. (2007) In vivo characterization and therapeutic efficacy of a C5-specific inhibitor from the soft tick Ornithodoros moubata. J. Biol. Chem. 282, 8292- 8299
38. Wai, P. Y., Mi, Z., Guo, H., Sarraf-Yazdi, S., Gao, C., Wei, J., Marroquin, C. E., Clary, B., and Kuo, P. C. (2005) Osteopontin silencing by small interfering RNA suppresses in vitro and in vivo CT26 murine colon adenocarcinoma metastasis. Carcinogenesis 26, 741-751
39. Eisenhart, C. (1947) The assumptions underlying the analysis of variance. Biometrics 3, 1-21
40. Bessarabova, M., Ishkin, A., JeBailey, L., Nikolskaya, T., and Nikolsky, Y. (2012) Knowledge-based analysis of proteomics data. BMC Bioinformatics 13, S13
41. Johnson, G. R., Kannan, B., Shoyab, M., and Stromberg, K. (1993) Amphiregulin induces tyrosine phosphorylation of the epidermal growth-factor receptor and p185(ERBB2): evidence that amphiregulin acts exclusively through the epidermal growth-factor receptor at the surface of human epithelial cells. J. Biol. Chem. 268, 2924-2931
42. Chintakuntlawar, A. V., and Chodosh, J. (2009) Chemokine CXCL1/KC and its receptor CXCR2 are responsible for neutrophil chemotaxis in adenoviral keratitis. J. Interferon Cytokine Res. 29, 657- 666
43. Nagase, H., Visse, R., and Murphy, G. (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 69, 562-573
44. Kumbrink, J., Kirsch, K. H., and Johnson, J. P. (2010) EGR1, EGR2, and EGR3 activate the expression of their coregulator NAB2 establishing a negative feedback loop in cells of neuroectodermal and epithelial origin. J. Cell. Biochem. 111, 207-217
45. Fang, F. (2011) The early growth response gene Egr2 (alias Krox20) is a novel transcriptional target of transforming growth factor-β that is upregulated in systemic sclerosis and mediates profibrotic responses. Am. J. Pathol. 178, 2077-2090; Correction (2011) Am. J. Pathol. 179, 537
46. James, A. B., Conway, A. M., and Morris, B. J. (2005) Genomic profiling of the neuronal target genes of the plasticity-related transcription factor-Zif268. J. Neurochem. 95, 796-810
47. Ahmad, R., Sylvester, J., and Zafarullah, M. (2007) MyD88, IRAK1 and TRAF6 knockdown in human chondrocytes inhibits interleukin-1-induced matrix metalloproteinase-13 gene expression and promoter activity by impairing MAP kinase activation. Cell. Signal. 19, 2549-2557
48. Fleischmann, A., Hafezi, F., Elliott, C., Remé, C. E., Rüther, U., and Wagner, E. F. (2000) Fra-1 replaces c-Fos-dependent functions in mice. Genes Dev. 14, 2695-2700
49. Shen, F., Hu, Z., Goswami, J., and Gaffen, S. L. (2006) Identification of common transcriptional regulatory elements in interleukin-17 target genes. J. Biol. Chem. 281, 24138-24148
50. Yee, J., Kuncio, G. S., Bhandari, B., Shihab, F. S., and Neilson, E. G. (1997) Identification of promoter activity and differential expression of transcripts encoding the murine stromelysin-1 gene in renal cells. Kidney Int. 52, 120-129
51. Zenz, R., Eferl, R., Scheinecker, C., Redlich, K., Smolen, J., Schonthaler, H. B., Kenner, L., Tschachler, E., and Wagner, E. F. (2008) Activator protein 1 (Fos/Jun) functions in inflammatory bone and skin disease. Arthritis Res. Ther. 10, 201
52. Liacini, A., Sylvester, J., Li, W. Q., and Zafarullah, M. (2002) Inhibition of interleukin-1-stimulated MAP kinases, activating protein-1 (AP-1), and nuclear factor κB (NF-κB) transcription factors down-regulates matrix metalloproteinase gene expression in articular chondrocytes. Matrix Biol. 21, 251-262
53. Viedt, C., Hänsch, G. M., Brandes, R. P., Kübler, W., and Kreuzer, J. (2000) The terminal complement complex C5b-9 stimulates interleukin-6 production in human smooth muscle cells through activation of transcription factors NF-κB and AP-1. FASEB J. 14, 2370-2372
54. Badea, T. D., Park, J. H., Soane, L., Niculescu, T., Niculescu, F., Rus, H., and Shin, M. L. (2003) Sublytic terminal complement attack induces c-fos transcriptional activation in myotubes. J. Neuroimmunol. 142, 58-66
55. Wang, Q., Rozelle, A. L., Lepus, C. M., Scanzello, C. R., Song, J. J., Larsen, D. M., Crish, J. F., Bebek, G., Ritter, S. Y., Lindstrom, T. M., Hwang, I., Wong, H. H., Punzi, L., Encarnacion, A., Shamloo, M., et al. (2011) Identification of a central role for complement in osteoarthritis. Nat. Med. 17, 1674-1679
56. Olayioye, M. A., Neve, R. M., Lane, H. A., and Hynes, N. E. (2000) The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 19, 3159-3167
57. Carpenter, G. (1999) Employment of the epidermal growth factor receptor in growth factor-independent signaling pathways. J. Cell Biol. 146, 697-702
58. Cybulsky, A. V., Takano, T., Papillon, J., and McTavish, A. J. (1999) Complement C5b-9 induces receptor-tyrosine kinase transactivation in glomerular epithelial cells. Am. J. Pathol. 155, 1701-1711
59. Niculescu, F., Rus, H., and Shin, M. L. (1994) Receptor-independent activation of guanine-nucleotide-binding regulatory proteins by terminal complement complexes. J. Biol. Chem. 269, 4417-4423
60. Beadling, C., Druey, K. M., Richter, G., Kehrl, J. H., and Smith, K. A. (1999) Regulators of G protein signaling exhibit distinct patterns of gene expression and target G protein specificity in human lymphocytes. J. Immunol. 162, 2677-2682
61. Bolitho, C., Hahn, M. A., Baxter, R. C., and Marsh, D. J. (2010) The chemokine CXCL1 induces proliferation in epithelial ovarian cancer cells by transactivation of the epidermal growth factor receptor. Endocr. Relat. Cancer 17, 929-940
62. D'Antonio, A., Losito, S., Pignata, S., Grassi, M., Perrone, F., De Luca, A., Tambaro, R., Bianco, C., Gullick, W. J., Johnson, G. R., Iaffaioli, V. R., Salomon, D. S., and Normanno, N. (2002) Transforming growth factor α, amphiregulin and cripto-1 are frequently expressed in advanced human ovarian carcinomas. Int. J. Oncol. 21, 941-948
63. Johnson, G. R., Saeki, T., Gordon, A. W., Shoyab, M., Salomon, D. S., and Stromberg, K. (1992) Autocrine action of amphiregulin in a colon carci-noma cell line and immunocytochemical localization of amphiregulin in human colon. J. Cell Biol. 118, 741-751
64. LeJeune, S., Leek, R., Horak, E., Plowman, G., Greenall, M., and Harris, A. L. (1993) Amphiregulin, epidermal growth-factor receptor, and estrogen-receptor expression in human primary breast-cancer. Cancer Res. 53, 3597-3602
65. Rubie, C., Frick, V. O., Wagner, M., Schuld, J., Gräber, S., Brittner, B., Bohle, R. M., and Schilling, M. K. (2008) ELR plus CXC chemokine expression in benign and malignant colorectal conditions. BMC Cancer 8, 178
66. Yang, G., Rosen, D. G., Zhang, Z., Bast, R. C., Jr., Mills, G. B., Colacino, J. A., Mercado-Uribe, I., and Liu, J. (2006) The chemokine growth-regulated oncogene 1 (Gro-1) links RAS signaling to the senescence of stromal fibroblasts and ovarian tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 103, 16472-16477
67. Huang, M.-Y., Chang, H.-J., Chung, F.-Y., Yang, M.-J., Yang, Y.-H., Wang, J.-Y., and Lin, S.-R. (2010) MMP13 is a potential prognostic marker for colorectal cancer. Oncol. Rep. 24, 1241-1247
68. Morgia, G., Falsaperla, M., Malaponte, G., Madonia, M., Indelicato, M., Travali, S., and Mazzarino, M. (2005) Matrix metalloproteinases as diagnostic (MMP-13) and prognostic (MMP-2, MMP-9) markers of prostate cancer. Urol. Res. 33, 44-50
69. Sternlicht, M. D., Lochter, A., Sympson, C. J., Huey, B., Rougier, J. P., Gray, J. W., Pinkel, D., Bissell, M. J., and Werb, Z. (1999) The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 98, 137-146
70. Acharyya, S., Oskarsson, T., Vanharanta, S., Malladi, S., Kim, J., Morris, P. G., Manova-Todorova, K., Leversha, M., Hogg, N., Seshan, V. E., Norton, L., Brogi, E., and Massagué, J. (2012) A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 150, 165-178
71. Castillo, J., Erroba, E., Perugorría, M. J., Santamaría, M., Lee, D. C., Prieto, J., Avila, M. A., and Berasain, C. (2006) Amphiregulin contributes to the transformed phenotype of human hepatocellular carcinoma cells. Cancer Res. 66, 6129-6138
72. Deryugina, E. I., and Quigley, J. P. (2006) Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 25, 9-34
73. Egeblad, M., and Werb, Z. (2002) New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174
74. Lukashev, M. E., and Werb, Z. (1998) ECM signalling: orchestrating cell behaviour and misbehaviour. Trends Cell Biol. 8, 437-441
75. Lochter, A., Galosy, S., Muschler, J., Freedman, N., Werb, Z., and Bissell, M. J. (1997) Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J. Cell Biol. 139, 1861-1872
76. Kudo, Y., Iizuka, S., Yoshida, M., Tsunematsu, T., Kondo, T., Subarnbhesaj, A., Deraz, E. M., Siriwardena, S. B., Tahara, H., Ishimaru, N., Ogawa, I., and Takata, T. (2012) Matrix Metalloproteinase-13 (MMP-13) Directly and indirectly promotes tumor angiogenesis. J. Biol. Chem. 287, 38716-38728
77. Bolstad, B. M., Irizarry, R. A., Astrand, M., and Speed, T. P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193