Insights into the role of progranulin in immunity, infection, and inflammation

Journal of Leukocyte Biology

Volumn 93, Issue 2, 2013, Pages 199-208

  Jian, Jinlong ^a   Konopka, Jessica ^b   Liu, Chuanju ^c  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Microbial pathogen; Tnf autoimmune diseases

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; GLUCOSE REGULATED PROTEIN 94; INTERLEUKIN 1BETA; INTERLEUKIN 6; PERLECAN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROGRANULIN; TOLL LIKE RECEPTOR 9; TRANSACTIVATOR PROTEIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR INHIBITOR;

ANTIGEN PRESENTATION; ANTIINFLAMMATORY ACTIVITY; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CHRONIC INFLAMMATION; ENZYME DEGRADATION; EXTRACELLULAR MATRIX; GENE MUTATION; HUMAN; IMMUNITY; IMMUNOMODULATION; INFECTION; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; REVIEW; WOUND HEALING;

ANIMALS; HUMANS; IMMUNITY, INNATE; INFECTION; INFLAMMATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84873291182     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0812429     Document Type: Review

References (110)

1. Gillitzer, R., Goebeler, M. (2001) Chemokines in cutaneous wound healing. J. Leukoc. Biol. 69, 513-521.
2. Segal, B. H. (2007) Role of macrophages in host defense against aspergillosis and strategies for immune augmentation. Oncologist 12 (Suppl. 2), 7-13.
3. Warrington, R., Watson, W., Kim, H. L., Antonetti, F. R. (2011) An introduction to immunology and immunopathology. Allergy Asthma Clin. Immunol. 7 (Suppl. 1), S1.
4. Elenkov, I. J., Iezzoni, D. G., Daly, A., Harris, A. G., Chrousos, G. P. (2005) Cytokine dysregulation, inflammation and well-being. Neuroimmunomodulation 12, 255-269.
5. Forsgren, S., Renstrom, L., Purdam, C., Gaida, J. E. (2012) TNF- in the locomotor system beyond joints: high degree of involvement in myositis in a rabbit model. Int. J. Rheumatol. 2012, 637452.
6. Aaltonen, K. J., Virkki, L. M., Malmivaara, A., Konttinen, Y. T., Nordstrom, D. C., Blom, M. (2012) Systematic review and meta-analysis of the efficacy and safety of existing TNF blocking agents in treatment of rheumatoid arthritis. PloS One 7, e30275.
7. Tanaka, Y. (2012) Intensive treatment and treatment holiday of TNFinhibitors in rheumatoid arthritis. Curr. Opin. Rheumatol. 24, 319-326.
8. Blam, M. E., Stein, R. B., Lichtenstein, G. R. (2001) Integrating antitumor necrosis factor therapy in inflammatory bowel disease: current and future perspectives. Am. J. Gastroenterol. 96, 1977-1997.
9. De Chambrun, G. P., Sandborn, W. J. (2012) IBD in 2011: advances in IBD management-towards a tailored approach. Nat. Rev. Gastroenterol Hepatol. 9, 70-72.
10. Zanocco-Marani, T., Bateman, A., Romano, G., Valentinis, B., He, Z. H., Baserga, R. (1999) Biological activities and signaling pathways of the granulin/epithelin precursor. Cancer Res. 59, 5331-5340.
11. Shoyab, M., McDonald, V. L., Byles, C., Todaro, G. J., Plowman, G. D. (1990) Epithelins 1 and 2: isolation and characterization of two cysteine- rich growth-modulating proteins. Proc. Natl. Acad. Sci. USA 87, 7912-7916.
12. Plowman, G. D., Green, J. M., Neubauer, M. G., Buckley, S. D., McDonald, V. L., Todaro, G. J., Shoyab, M. (1992) The epithelin precursor encodes two proteins with opposing activities on epithelial cell growth. J. Biol. Chem. 267, 13073-13078.
13. Anakwe, O. O., Gerton, G. L. (1990) Acrosome biogenesis begins during meiosis: evidence from the synthesis and distribution of an acrosomal glycoprotein, acrogranin, during guinea pig spermatogenesis. Biol. Reproduct. 42, 317-328.
14. Zhou, J., Gao, G., Crabb, J. W., Serrero, G. (1993) Purification of an autocrine growth factor homologous with mouse epithelin precursor from a highly tumorigenic cell line. J. Biol. Chem. 268, 10863-10869.
15. Hrabal, R., Chen, Z., James, S., Bennett, H. P., Ni, F. (1996) The hairpin stack fold, a novel protein architecture for a new family of protein growth factors. Nat. Struct. Biol. 3, 747-752.
16. Kessenbrock, K., Frohlich, L., Sixt, M., Lammermann, T., Pfister, H., Bateman, A., Belaaouaj, A., Ring, J., Ollert, M., Fassler, R., Jenne, D. E. (2008) Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J. Clin. Investig. 118, 2438-2447.
17. Zhu, J., Nathan, C., Jin, W., Sim, D., Ashcroft, G. S., Wahl, S. M., Lacomis, L., Erdjument-Bromage, H., Tempst, P., Wright, C. D., Ding, A. (2002) Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 111, 867-878.
18. Butler, G. S., Dean, R. A., Tam, E. M., Overall, C. M. (2008) Pharmacoproteomics of a metalloproteinase hydroxamate inhibitor in breast cancer cells: dynamics of membrane type 1 matrix metalloproteinase-mediated membrane protein shedding. Mol. Cell. Biol. 28, 4896-4914.
19. Suh, H. S., Choi, N., Tarassishin, L., Lee, S. C. (2012) Regulation of progranulin expression in human microglia and proteolysis of progranulin by matrix metalloproteinase-12 (MMP-12). PloS One 7, e35115.
20. Xu, D., Suenaga, N., Edelmann, M. J., Fridman, R., Muschel, R. J., Kessler, B. M. (2008) Novel MMP-9 substrates in cancer cells revealed by a label-free quantitative proteomics approach. Mol. Cell. Proteomics 7, 2215-2228.
21. Daniel, R., He, Z., Carmichael, K. P., Halper, J., Bateman, A. (2000) Cellular localization of gene expression for progranulin. J. Histochem. Cytochem. 48, 999-1009.
22. Wang, D., Bai, X., Tian, Q., Lai, Y., Lin, E. A., Shi, Y., Mu, X., Feng, J. Q., Carlson, C. S., Liu, C. J. (2012) GEP constitutes a negative feedback loop with MyoD and acts as a novel mediator in controlling skeletal muscle differentiation. Cell. Mol. Life Sci. 69, 1855-1873.
23. Matsubara, T., Mita, A., Minami, K., Hosooka, T., Kitazawa, S., Takahashi, K., Tamori, Y., Yokoi, N., Watanabe, M., Matsuo, E., Nishimura, O., Seino, S. (2012) PGRN is a key adipokine mediating high fat dietinduced insulin resistance and obesity through IL-6 in adipose tissue. Cell Metab. 15, 38-50.
24. Elkabets, M., Gifford, A. M., Scheel, C., Nilsson, B., Reinhardt, F., Bray, M. A., Carpenter, A. E., Jirstrom, K., Magnusson, K., Ebert, B. L., Ponten, F., Weinberg, R. A., McAllister, S. S. (2011) Human tumors instigate granulin-expressing hematopoietic cells that promote malignancy by activating stromal fibroblasts in mice. J. Clin. Investig. 121, 784-799.
25. He, Z., Bateman, A. (1999) Progranulin gene expression regulates epithelial cell growth and promotes tumor growth in vivo. Cancer Res. 59, 3222-3229.
26. Frampton, G., Invernizzi, P., Bernuzzi, F., Pae, H.Y., Quinn, M., Horvat, D., Galindo, C., Huang, L., McMillin, M., Cooper, B., Rimassa, L., DeMorrow, S. (2012) Interleukin-6-driven progranulin expression increases cholangiocarcinoma growth by an Akt-dependent mechanism. Gut 61, 268-277.
27. Serrero, G., Ioffe, O. B. (2003) Expression of PC-cell-derived growth factor in benign and malignant human breast epithelium. Hum. Pathol. 34, 1148-1154.
28. Diaz-Cueto, L., Arechavaleta-Velasco, F., Diaz-Arizaga, A., Dominguez-Lopez, P., Robles-Flores, M. (2012) PKC signaling is involved in the regulation of progranulin (acrogranin/PC-cell-derived growth factor/ granulin-epithelin precursor) protein expression in human ovarian cancer cell lines. Int. J. Gynecol. Cancer 22, 945-950.
29. Yin, F., Banerjee, R., Thomas, B., Zhou, P., Qian, L., Jia, T., Ma, X., Ma, Y., Iadecola, C., Beal, M. F., Nathan, C., Ding, A. (2010) Exaggerated inflammation, impaired host defense, and neuropathology in progranulin- deficient mice. J. Exp. Med. 207, 117-128.
30. He, Z., Ong, C. H., Halper, J., Bateman, A. (2003) Progranulin is a mediator of the wound response. Nat. Med. 9, 225-229.
31. Baker, M., Mackenzie, I. R., Pickering-Brown, S. M., Gass, J., Rademakers, R., Lindholm, C., Snowden, J., Adamson, J., Sadovnick, A. D., Rollinson, S., Cannon, A., Dwosh, E., Neary, D., Melquist, S., Richardson, A., Dickson, D., Berger, Z., Eriksen, J., Robinson, T., Zehr, C., Dickey, C. A., Crook, R., McGowan, E., Mann, D., Boeve, B., Feldman, H., Hutton, M. (2006) Mutations in progranulin cause -negative frontotemporal dementia linked to chromosome 17. Nature 442, 916-919.
32. Cruts, M., Gijselinck, I., van der Zee, J., Engelborghs, S., Wils, H., Pirici, D., Rademakers, R., Vandenberghe, R., Dermaut, B., Martin, J. J., van Duijn, C., Peeters, K., Sciot, R., Santens, P., De Pooter, T., Mattheijssens, M., Van den Broeck, M., Cuijt, I., Vennekens, K., De Deyn, P. P., Kumar-Singh, S., Van Broeckhoven, C. (2006) Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442, 920-924.
33. Ghidoni, R., Benussi, L., Glionna, M., Franzoni, M., Binetti, G. (2008) Low plasma progranulin levels predict progranulin mutations in frontotemporal lobar degeneration. Neurology 71, 1235-1239.
34. Sleegers, K., Brouwers, N., Van Damme, P., Engelborghs, S., Gijselinck, I., van der Zee, J., Peeters, K., Mattheijssens, M., Cruts, M., Vandenberghe, R., De Deyn, P. P., Robberecht, W., Van Broeckhoven, C. (2009) Serum biomarker for progranulin-associated frontotemporal lobar degeneration. Ann. Neurol. 65, 603-609.
35. Finch, N., Baker, M., Crook, R., Swanson, K., Kuntz, K., Surtees, R., Bisceglio, G., Rovelet-Lecrux, A., Boeve, B., Petersen, R. C., Dickson, D. W., Younkin, S. G., Deramecourt, V., Crook, J., Graff-Radford, N. R., Rademakers, R. (2009) Plasma progranulin levels predict progranulin mutation status in frontotemporal dementia patients and asymptomatic family members. Brain 132, 583-591.
36. Baker, C. A., Manuelidis, L. (2003) Unique inflammatory RNA profiles of microglia in Creutzfeldt-Jakob disease. Proc. Natl. Acad. Sci. USA 100, 675-679.
37. Vercellino, M., Grifoni, S., Romagnolo, A., Masera, S., Mattioda, A., Trebini, C., Chiavazza, C., Caligiana, L., Capello, E., Mancardi, G. L., Giobbe, D., Mutani, R., Giordana, M. T., Cavalla, P. (2011) Progranulin expression in brain tissue and cerebrospinal fluid levels in multiple sclerosis. Mult. Scler. 17, 1194-1201.
38. Malaspina, A., Kaushik, N., de Belleroche, J. (2001) Differential expression of 14 genes in amyotrophic lateral sclerosis spinal cord detected using gridded cDNA arrays. J. Neurochem. 77, 132-145.
39. Lopez de Munain, A., Alzualde, A., Gorostidi, A., Otaegui, D., Ruiz-Martinez, J., Indakoetxea, B., Ferrer, I., Perez-Tur, J., Saenz, A., Bergareche, A., Barandiaran, M., Poza, J. J., Zabalza, R., Ruiz, I., Urtasun, M., Fernandez-Manchola, I., Olasagasti, B., Espinal, J. B., Olaskoaga, J., Ruibal, M., Moreno, F., Carrera, N., Marti Masso, J. F. (2008) Mutations in progranulin gene: clinical, pathological, and ribonucleic acid expression findings. Biol. Psychiatry 63, 946-952.
40. Xu, K., Zhang, Y., Ilalov, K., Carlson, C. S., Feng, J. Q., Di Cesare, P. E., Liu, C. J. (2007) Cartilage oligomeric matrix protein associates with granulin-epithelin precursor (GEP) and potentiates GEP-stimulated chondrocyte proliferation. J. Biol. Chem. 282, 11347-11355.
41. Feng, J. Q., Guo, F. J., Jiang, B. C., Zhang, Y., Frenkel, S., Wang, D. W., Tang, W., Xie, Y., Liu, C. J. (2010) Granulin epithelin precursor: a bone morphogenic protein 2-inducible growth factor that activates Erk1/2 signaling and JunB transcription factor in chondrogenesis. FASEB J. 24, 1879-1892.
42. Tang, W., Lu, Y., Tian, Q. Y., Zhang, Y., Guo, F. J., Liu, G. Y., Syed, N. M., Lai, Y., Lin, E. A., Kong, L., Su, J., Yin, F., Ding, A. H., Zanin-Zhorov, A., Dustin, M. L., Tao, J., Craft, J., Yin, Z., Feng, J. Q., Abramson, S. B., Yu, X. P., Liu, C. J. (2011) The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science 332, 478-484.
43. Puga, I., Cols, M., Barra, C. M., He, B., Cassis, L., Gentile, M., Comerma, L., Chorny, A., Shan, M., Xu, W., Magri, G., Knowles, D. M., Tam, W., Chiu, A., Bussel, J. B., Serrano, S., Lorente, J. A., Bellosillo, B., Lloreta, J., Juanpere, N., Alameda, F., Baro, T., de Heredia, C. D., Toran, N., Catala, A., Torrebadell, M., Fortuny, C., Cusi, V., Carreras, C., Diaz, G. A., Blander, J. M., Farber, C. M., Silvestri, G., Cunningham- Rundles, C., Calvillo, M., Dufour, C., Notarangelo, L. D., Lougaris, V., Plebani, A., Casanova, J. L., Ganal, S. C., Diefenbach, A., Arostegui, J. I., Juan, M., Yague, J., Mahlaoui, N., Donadieu, J., Chen, K., Cerutti, A. (2012) B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat. Immunol. 13, 170-180.
44. Park, B., Buti, L., Lee, S., Matsuwaki, T., Spooner, E., Brinkmann, M. M., Nishihara, M., Ploegh, H. L. (2011) Granulin is a soluble cofactor for Toll-like receptor 9 signaling. Immunity 34, 505-513.
45. Guo, F., Lai, Y., Tian, Q., Lin, E. A., Kong, L., Liu, C. (2010) Granulinepithelin precursor binds directly to ADAMTS-7 and ADAMTS-12 and inhibits their degradation of cartilage oligomeric matrix protein. Arthritis Rheum. 62, 2023-2036.
46. Gonzalez, E. M., Mongiat, M., Slater, S. J., Baffa, R., Iozzo, R. V. (2003) A novel interaction between Perlecan protein core and progranulin: potential effects on tumor growth. J. Biol. Chem. 278, 38113-38116.
47. Okura, H., Yamashita, S., Ohama, T., Saga, A., Yamamoto-Kakuta, A., Hamada, Y., Sougawa, N., Ohyama, R., Sawa, Y., Matsuyama, A. (2010) HDL/apolipoprotein A-I binds to macrophage-derived progranulin and suppresses its conversion into proinflammatory granulins. J. Atheroscl. Thromb. 17, 568-577.
48. Trinh, D. P., Brown, K. M., Jeang, K. T. (1999) Epithelin/granulin growth factors: extracellular cofactors for HIV-1 and HIV-2 Tat proteins. Biochem. Biophys. Res. Commun. 256, 299-306.
49. Shoham, N., Cohen, L., Gazit, A., Yaniv, A. (2003) The Tat protein of the caprine arthritis encephalitis virus interacts with the Notch2 EGFlike repeats and the epithelin/granulin precursor. Intervirology 46, 239-244.
50. Hu, F., Padukkavidana, T., Vaegter, C. B., Brady, O. A., Zheng, Y., Mackenzie, I. R., Feldman, H. H., Nykjaer, A., Strittmatter, S. M. (2010) Sortilin-mediated endocytosis determines levels of the frontotemporal dementia protein, progranulin. Neuron 68, 654-667.
51. Sui, D., Wilson, J. E. (2000) Interaction of insulin-like growth factor binding protein-4, Miz-1, leptin, lipocalin-type prostaglandin D synthase, and granulin precursor with the N-terminal half of type III hexokinase. Arch. Biochem. Biophys. 382, 262-274.
52. Lam, C. Y., Yip, C. W., Poon, T. C., Cheng, C. K., Ng, E. W., Wong, N. C., Cheung, P. F., Lai, P. B., Ng, I. O., Fan, S. T., Cheung, S. T. (2012) Identification and characterization of tropomyosin 3 associated with granulin-epithelin precursor in human hepatocellular carcinoma. PloS One 7, e40324.
53. Almeida, S., Zhou, L., Gao, F. B. (2011) Progranulin, a glycoprotein deficient in frontotemporal dementia, is a novel substrate of several protein disulfide isomerase family proteins. PloS One 6, e26454.
54. Hoque, M., Young, T. M., Lee, C. G., Serrero, G., Mathews, M. B., Pe'ery, T. (2003) The growth factor granulin interacts with cyclin T1 and modulates P-TEFb-dependent transcription. Mol. Cell. Biol. 23, 1688-1702.
55. Hoque, M., Tian, B., Mathews, M. B., Pe'ery, T. (2005) Granulin and granulin repeats interact with the Tat.P-TEFb complex and inhibit Tat transactivation. J. Biol. Chem. 280, 13648-13657.
56. Bai, X. H., Wang, D. W., Kong, L., Zhang, Y., Luan, Y., Kobayashi, T., Kronenberg, H. M., Yu, X. P., Liu, C. J. (2009) ADAMTS-7, a direct target of PTHrP, adversely regulates endochondral bone growth by associating with and inactivating GEP growth factor. Mol. Cell. Biol. 29, 4201-4219.
57. Gass, J., Lee, W. C., Cook, C., Finch, N., Stetler, C., Jansen-West, K., Lewis, J., Link, C. D., Rademakers, R., Nykjaer, A., Petrucelli, L. (2012) Progranulin regulates neuronal outgrowth independent of Sortilin. Mol. Neurodegen. 7, 33.
58. De Muynck, L., Van Damme, P. (2011) Cellular effects of progranulin in health and disease. J. Mol. Neurosci. 45, 549-560.
59. Newcomb, J. R., Cresswell, P. (1993) Characterization of endogenous peptides bound to purified HLA-DR molecules and their absence from invariant chain-associated _ _ dimers. J. Immunol. 150, 499-507.
60. McIsaac, S. M., Stadnyk, A. W., Lin, T. J. (2012) Toll-like receptors in the host defense against Pseudomonas aeruginosa respiratory infection and cystic fibrosis. J. Leukoc. Biol. 94, Epub ahead of print.
61. Lazuardi, L., Herndler-Brandstetter, D., Brunner, S., Laschober, G. T., Lepperdinger, G., Grubeck-Loebenstein, B. (2009) Microarray analysis reveals similarity between CD8_CD28_ T cells from young and elderly persons, but not of CD8 CD28 T cells. Biogerontology 10, 191-202.
62. Najafian, N., Chitnis, T., Salama, A. D., Zhu, B., Benou, C., Yuan, X., Clarkson, M. R., Sayegh, M. H., Khoury, S. J. (2003) Regulatory functions of CD8 CD28 T cells in an autoimmune disease model. J. Clin. Investig. 112, 1037-1048.
63. Pickford, F., Marcus, J., Camargo, L. M., Xiao, Q., Graham, D., Mo, J. R., Burkhardt, M., Kulkarni, V., Crispino, J., Hering, H., Hutton, M. (2011) Progranulin is a chemoattractant for microglia and stimulates their endocytic activity. Am J. Pathol. 178, 284-295.
64. Marriott, H. M., Jackson, L. E., Wilkinson, T. S., Simpson, A. J., Mitchell, T. J., Buttle, D. J., Cross, S. S., Ince, P. G., Hellewell, P. G., Whyte, M. K., Dockrell, D. H. (2008) Reactive oxygen species regulate neutrophil recruitment and survival in pneumococcal pneumonia. Am. J. Respir. Crit. Care Med. 177, 887-895.
65. Borregaard, N., Cowland, J. B. (1997) Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89, 3503-3521.
66. Wang, H., Sun, Y., Liu, S., Yu, H., Li, W., Zeng, J., Chen, C., Jia, J. (2011) Upregulation of progranulin by Helicobacter pylori in human gastric epithelial cells via p38MAPK and MEK1/2 signaling pathway: role in epithelial cell proliferation and migration. FEMS Immunol. Med. Microbiol. 63, 82-92.
67. Wex, T., Kuester, D., Schonberg, C., Schindele, D., Treiber, G., Malfertheiner, P. (2011) Mucosal progranulin expression is induced by H. pylori, but independent of secretory leukocyte protease inhibitor (SLPI) expression. BMC Gastroenterol. 11, 63.
68. Vachev, B., Tsvetkov, A., Dobrev, V., Nikolov, A., Bailozov, D. (1982) [Diseases of the locomotor apparatus in pigs on commercial farm complexes]. Veterinarno-meditsinski nauki 19, 19-24.
69. Chang, H. K., Gallo, R. C., Ensoli, B. (1995) Regulation of cellular gene expression and function by the human immunodeficiency virus type 1 tat protein. J. Biomed. Sci. 2, 189-202.
70. Hoque, M., Mathews, M. B., Pe'ery, T. (2010) Progranulin (granulin/ epithelin precursor) and its constituent granulin repeats repress transcription from cellular promoters. J. Cell. Physiol. 223, 224-233.
71. Nabell, L. M., Raja, R. H., Sayeski, P. P., Paterson, A. J., Kudlow, J. E. (1994) Human immunodeficiency virus 1 Tat stimulates transcription of the transforming growth factor _ gene in an epidermal growth factor- dependent manner. Cell Growth Diff. 5, 87-93.
72. Zauli, G., Davis, B. R., Re, M. C., Visani, G., Furlini, G., La Placa, M. (1992) Tat protein stimulates production of transforming growth factor- 1 by marrow macrophages: a potential mechanism for human immunodeficiency virus-1-induced hematopoietic suppression. Blood 80, 3036-3043.
73. Purvis, S. F., Georges, D. L., Williams, T. M., Lederman, M. M. (1992) Suppression of interleukin-2 and interleukin-2 receptor expression in Jurkat cells stably expressing the human immunodeficiency virus Tat protein. Cell. Immunol. 144, 32-42.
74. Puri, R. K., Leland, P., Aggarwal, B. B. (1995) Constitutive expression of human immunodeficiency virus type 1 tat gene inhibits interleukin 2 and interleukin 2 receptor expression in a human CD4_ T lymphoid (H9) cell line. AIDS Res. Hum. Retrovir. 11, 31-40.
75. Pocsik, E., Higuchi, M., Aggarwal, B. B. (1992) Down-modulation of cell surface expression of p80 form of the tumor necrosis factor receptor by human immunodeficiency virus-1 tat gene. Lymphokine Cytokine Res. 11, 317-325.
76. Bouillet, L. E., Dias, M. O., Dorigo, N. A., Moura, A. D., Russell, B., Nosten, F., Renia, L., Braga, E. M., Gazzinelli, R. T., Rodrigues, M. M., Soares, I. S., Bruna-Romero, O. (2011) Long-term humoral and cellular immune responses elicited by a heterologous Plasmodium vivax apical membrane antigen 1 protein prime/adenovirus boost immunization protocol. Infect. Immun. 79, 3642-3652.
77. Ong, C. H., Bateman, A. (2003) Progranulin (granulin-epithelin precursor, PC-cell derived growth factor, acrogranin) in proliferation and tumorigenesis. Histol. Histopathol. 18, 1275-1288.
78. He, Z., Bateman, A. (2003) Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis. J. Mol. Med. 81, 600-612.
79. Yasui, K., Oketa, Y., Higashida, K., Fukazawa, H., Ono, S. (2011) Increased progranulin in the skin of amyotrophic lateral sclerosis: an immunohistochemical study. J. Neurol. Sci. 309, 110-114.
80. Lim, H. Y., Albuquerque, B., Haussler, A., Myrczek, T., Ding, A., Tegeder, I. (2012) Progranulin contributes to endogenous mechanisms of pain defense after nerve injury in mice. J. Cell. Mol. Med. 16, 708-721.
81. Ryan, C. L., Baranowski, D. C., Chitramuthu, B. P., Malik, S., Li, Z., Cao, M., Minotti, S., Durham, H. D., Kay, D. G., Shaw, C. A., Bennett, H. P., Bateman, A. (2009) Progranulin is expressed within motor neurons and promotes neuronal cell survival. BMC Neurosci. 10, 130.
82. Naphade, S. B., Kigerl, K. A., Jakeman, L. B., Kostyk, S. K., Popovich, P. G., Kuret, J. (2010) Progranulin expression is upregulated after spinal contusion in mice. Acta Neuropathol. 119, 123-133.
83. Monami, G., Gonzalez, E. M., Hellman, M., Gomella, L. G., Baffa, R., Iozzo, R. V., Morrione, A. (2006) Proepithelin promotes migration and invasion of 5637 bladder cancer cells through the activation of ERK1/2 and the formation of a paxillin/FAK/ERK complex. Cancer Res. 66, 7103-7110.
84. Kamrava, M., Simpkins, F., Alejandro, E., Michener, C., Meltzer, E., Kohn, E. C. (2005) Lysophosphatidic acid and endothelin-induced proliferation of ovarian cancer cell lines is mitigated by neutralization of granulin-epithelin precursor (GEP), a prosurvival factor for ovarian cancer. Oncogene 24, 7084-7093.
85. Guo, Z., Li, Q., Han, Y., Liang, Y., Xu, Z., Ren, T. (2012) Prevention of LPS-induced acute lung injury in mice by progranulin. Mediat. Inflamm. 2012, 10.
86. Tao, J., Ji, F., Wang, F., Liu, B., Zhu, Y. (2012) Neuroprotective effects of progranulin in ischemic mice. Brain Res. 1436, 130-136.
87. Guerra, R. R., Kriazhev, L., Hernandez-Blazquez, F. J., Bateman, A. (2007) Progranulin is a stress-response factor in fibroblasts subjected to hypoxia and acidosis. Growth Factors 25, 280-285.
88. Williams, R. O., Feldmann, M., Maini, R. N. (1992) Anti-tumor necrosis factor ameliorates joint disease in murine collagen-induced arthritis. Proc. Natl. Acad. Sci. USA 89, 9784-9788.
89. Thorbecke, G. J., Shah, R., Leu, C. H., Kuruvilla, A. P., Hardison, A. M., Palladino, M. A. (1992) Involvement of endogenous tumor necrosis factor and transforming growth factor during induction of collagen type II arthritis in mice. Proc. Natl. Acad. Sci. USA 89, 7375-7379.
90. Brennan, F. M., Chantry, D., Jackson, A., Maini, R., Feldmann, M. (1989) Inhibitory effect of TNF _ antibodies on synovial cell interleukin- 1 production in rheumatoid arthritis. Lancet 2, 244-247.
91. Santee, S. M., Owen-Schaub, L. B. (1996) Human tumor necrosis factor receptor p75/80 (CD120b) gene structure and promoter characterization. J. Biol. Chem. 271, 21151-21159.
92. Cabal-Hierro, L., Lazo, P. S. (2012) Signal transduction by tumor necrosis factor receptors. Cell. Signal. 24, 1297-1305.
93. Hossein-Nezhad, A., Mirzaei, K., Ansar, H., Khooshechin, G., Ahmadivand, Z., Keshavarz, S. A. (2012) Mutual role of PGRN/TNF- on osteopenia developing in obesity's inflammation state. Minerva Med. 103, 165-175.
94. Liu, C. J. (2011) Progranulin: a promising therapeutic target for rheumatoid arthritis. FEBS Lett. 585, 3675-3680.
95. Hossein-Nezhad, A., Mirzaei, K., Ansar, H., Emam-Gholipour, S., Tootee, A., Keshavarz, S. A. (2012) Obesity, inflammation and resting energy expenditure: possible mechanism of progranulin in this pathway. Minerva Endocrinol. 37, 255-266.
96. Youn, B. S., Bang, S. I., Kloting, N., Park, J. W., Lee, N., Oh, J. E., Pi, K. B., Lee, T. H., Ruschke, K., Fasshauer, M., Stumvoll, M., Bluher, M. (2009) Serum progranulin concentrations may be associated with macrophage infiltration into omental adipose tissue. Diabetes 58, 627-636.
97. Kloting, N., Fasshauer, M., Dietrich, A., Kovacs, P., Schon, M. R., Kern, M., Stumvoll, M., Bluher, M. (2010) Insulin-sensitive obesity. Am. J. Physiol. Endocrinol. Metab. 299, E506-E515.
98. Kim, H. K., Shin, M. S., Youn, B. S., Namkoong, C., Gil, S. Y., Kang, G. M., Yu, J. H., Kim, M. S. (2011) Involvement of progranulin in hypothalamic glucose sensing and feeding regulation. Endocrinology 152, 4672-4682.
99. Yilmaz, Y., Eren, F., Yonal, O., Polat, Z., Bacha, M., Kurt, R., Ozturk, O., Avsar, E. (2011) Serum progranulin as an independent marker of liver fibrosis in patients with biopsy-proven nonalcoholic fatty liver disease. Dis. Markers 31, 205-210.
100. Liu, C. J., Bosch, X. (2012) Progranulin: a growth factor, a novel TNFR ligand and a drug target. Pharmacol Ther. 133, 124-132.
101. Wu, H., Siegel, R. M. (2011) Medicine. Progranulin resolves inflammation. Science 332, 427-428.
102. Nagar, M., Jacob-Hirsch, J., Vernitsky, H., Berkun, Y., Ben-Horin, S., Amariglio, N., Bank, I., Kloog, Y., Rechavi, G., Goldstein, I. (2010) TNF activates a NF-B-regulated cellular program in human CD45RA regulatory T cells that modulates their suppressive function. J. Immunol. 184, 3570-3581.
103. Valencia, X., Stephens, G., Goldbach-Mansky, R., Wilson, M., Shevach, E. M., Lipsky, P. E. (2006) TNF downmodulates the function of human CD4 CD25hi T-regulatory cells. Blood 108, 253-261.
104. Zanin-Zhorov, A., Ding, Y., Kumari, S., Attur, M., Hippen, K. L., Brown, M., Blazar, B. R., Abramson, S. B., Lafaille, J. J., Dustin, M. L. (2010) Protein kinase C- mediates negative feedback on regulatory T cell function. Science 328, 372-376.
105. Moresco, E. M., Beutler, B. (2011) Special delivery: granulin brings CpG DNA to Toll-like receptor 9. Immunity 34, 453-455.
106. Zheng, Y., Brady, O. A., Meng, P. S., Mao, Y., Hu, F. (2011) C-terminus of progranulin interacts with the _-propeller region of Sortilin to regulate progranulin trafficking. PloS One 6, e21023.
107. Rosen, E. Y., Wexler, E. M., Versano, R., Coppola, G., Gao, F., Winden, K. D., Oldham, M. C., Martens, L. H., Zhou, P., Farese R. V., Jr., Geschwind, D. H. (2011) Functional genomic analyses identify pathways dysregulated by progranulin deficiency, implicating Wnt signaling. Neuron 71, 1030-1042.
108. Korade, Z., Mirnics, K. (2011) Wnt signaling as a potential therapeutic target for frontotemporal dementia. Neuron 71, 955-957.
109. Staal, F. J., Luis, T. C., Tiemessen, M. M. (2008) WNT signalling in the immune system: WNT is spreading its wings. Nat. Rev. Immunol. 8, 581-593.
110. Krieckaert, C. L., Nurmohamed, M. T., Wolbink, G. J. (2012) Methotrexate reduces immunogenicity in adalimumab treated rheumatoid arthritis patients in a dose dependent manner. Ann. Rheum. Dis. 71, 1914-1915.