Generic placeholder image

Anti-Inflammatory & Anti-Allergy Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5230
ISSN (Online): 1875-614X

Review Article

Progranulin Regulates Inflammation and Tumor

Author(s): Chunxiao Liu, Jiayi Li, Wenjing Shi, Liujia Zhang, Shuang Liu, Yingcong Lian, Shujuan Liang and Hongyan Wang*

Volume 19, Issue 2, 2020

Page: [88 - 102] Pages: 15

DOI: 10.2174/1871523018666190724124214

Abstract

Progranulin (PGRN) mediates cell cycle progression and cell motility as a pleiotropic growth factor and acts as a universal regulator of cell growth, migration and transformation, cell cycle, wound healing, tumorigenesis, and cytotoxic drug resistance as a secreted glycoprotein. PGRN overexpression can induce the secretion of many inflammatory cytokines, such as IL-8, -6,-10, TNF-α. At the same time, this protein can promote tumor proliferation and the occurrence and development of many related diseases such as gastric cancer, breast cancer, cervical cancer, colorectal cancer, renal injury, neurodegeneration, neuroinflammatory, human atherosclerotic plaque, hepatocarcinoma, acute kidney injury, amyotrophic lateral sclerosis, Alzheimer’s disease and Parkinson’s disease. In short, PGRN plays a very critical role in injury repair and tumorigenesis, it provides a new direction for succeeding research and serves as a target for clinical diagnosis and treatment, thus warranting further investigation. Here, we discuss the potential therapeutic utility and the effect of PGRN on the relationship between inflammation and cancer.

Keywords: Cell cycle, cell motility, inflammation, pleiotropic growth factor, progranulin, tumor.

Graphical Abstract

[1]
Anakwe, O.O.; Gerton, G.L. Acrosome biogenesis begins during meiosis: evidence from the synthesis and distribution of an acrosomal glycoprotein, acrogranin, during guinea pig spermatogenesis. Biol. Reprod., 1990, 42(2), 317-328.
[http://dx.doi.org/10.1095/biolreprod42.2.317] [PMID: 1692485]
[2]
Wisit, T.; Ginette, S. GP88 (Progranulin) confers Fulvestrant (Faslodex, ICI 182,780) resistance to human breast cancer cells. Sci Res., 2014, 3, 68-78.
[3]
Zhou, J.; Gao, G.; Crabb, J.W.; Serrero, G. Purification of an autocrine growth factor homologous with mouse epithelin precursor from a highly tumorigenic cell line. J. Biol. Chem., 1993, 268(15), 10863-10869.
[PMID: 8496151]
[4]
De Muynck, L.; Van Damme, P. Cellular effects of progranulin in health and disease. J. Mol. Neurosci., 2011, 45(3), 549-560.
[http://dx.doi.org/10.1007/s12031-011-9553-z] [PMID: 21611805]
[5]
He, Z.; Bateman, A. Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis. J. Mol. Med. (Berl.), 2003, 81(10), 600-612.
[http://dx.doi.org/10.1007/s00109-003-0474-3] [PMID: 12928786]
[6]
Bateman, A.; Bennett, H.P. Granulins: the structure and function of an emerging family of growth factors. J. Endocrinol., 1998, 158(2), 145-151.
[http://dx.doi.org/10.1677/joe.0.1580145] [PMID: 9771457]
[7]
Ong, C.H.; Bateman, A. Progranulin (granulin-epithelin precursor, PC-cell derived growth factor, acrogranin) in proliferation and tumorigenesis. Histol. Histopathol., 2003, 18(4), 1275-1288.
[PMID: 12973694]
[8]
Bateman, A.; Belcourt, D.; Bennett, H.; Lazure, C.; Solomon, S. Granulins, a novel class of peptide from leukocytes. Biochem. Biophys. Res. Commun., 1990, 173(3), 1161-1168.
[http://dx.doi.org/10.1016/S0006-291X(05)80908-8] [PMID: 2268320]
[9]
Bhandari, V.; Palfree, R.G.; Bateman, A. Isolation and sequence of the granulin precursor cDNA from human bone marrow reveals tandem cysteine-rich granulin domains. Proc. Natl. Acad. Sci. USA, 1992, 89(5), 1715-1719.
[http://dx.doi.org/10.1073/pnas.89.5.1715] [PMID: 1542665]
[10]
He, Z.; Ong, C.H.; Halper, J.; Bateman, A. Progranulin is a mediator of the wound response. Nat. Med., 2003, 9(2), 225-229.
[http://dx.doi.org/10.1038/nm816] [PMID: 12524533]
[11]
Shoyab, M.; McDonald, V.L.; Byles, C.; Todaro, G.J.; Plowman, G.D. Epithelins 1 and 2: isolation and characterization of two cysteine-rich growth-modulating proteins. Proc. Natl. Acad. Sci. USA, 1990, 87(20), 7912-7916.
[http://dx.doi.org/10.1073/pnas.87.20.7912] [PMID: 2236009]
[12]
Plowman, G.D.; Green, J.M.; Neubauer, M.G.; Buckley, S.D.; McDonald, V.L.; Todaro, G.J.; Shoyab, M. The epithelin precursor encodes two proteins with opposing activities on epithelial cell growth. J. Biol. Chem., 1992, 267(18), 13073-13078.
[PMID: 1618805]
[13]
Hrabal, R.; Chen, Z.; James, S.; Bennett, H.P.; Ni, F. The hairpin stack fold, a novel protein architecture for a new family of protein growth factors. Nat. Struct. Biol., 1996, 3(9), 747-752.
[http://dx.doi.org/10.1038/nsb0996-747] [PMID: 8784346]
[14]
Li, S.S.; Zhang, M.X.; Wang, Y.; Wang, W.; Zhao, C.M.; Sun, X.M.; Dong, G.K.; Li, Z.R.; Yin, W.J.; Zhu, B.; Cai, H.X. Reduction of PGRN increased fibrosis during skin wound healing in mice. Histol. Histopathol., 2018, 18, 18076.
[PMID: 30561754]
[15]
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. Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell, 2002, 111(6), 867-878.
[http://dx.doi.org/10.1016/S0092-8674(02)01141-8] [PMID: 12526812]
[16]
Daniel, R.; He, Z.; Carmichael, K.P.; Halper, J.; Bateman, A. Cellular localization of gene expression for progranulin. J. Histochem. Cytochem., 2000, 48(7), 999-1009.
[http://dx.doi.org/10.1177/002215540004800713] [PMID: 10858277]
[17]
Cynthia, L.; Jada, Z.; Dennis, L.; Dickson, W. Progranulin is located in secretory granules and vesicles of neutrophils and macro-phages by immunogold electron microscopy. J. Neuropathol. Exp. Neurol., 2007, 7, 418-459.
[18]
Xu, D.; Suenaga, N.; Edelmann, M.J.; Fridman, R.; Muschel, R.J.; Kessler, B.M. Novel MMP-9 substrates in cancer cells revealed by a label-free quantitative proteomics approach. Mol. Cell. Proteomics, 2008, 7(11), 2215-2228.
[http://dx.doi.org/10.1074/mcp.M800095-MCP200] [PMID: 18596065]
[19]
Butler, G.S.; Dean, R.A.; Tam, E.M.; Overall, C.M. Pharmacoproteomics of a metalloproteinase hydroxamate inhibitor in breast cancer cells: dynamics of membrane type 1 matrix metalloproteinase-mediated membrane protein shedding. Mol. Cell. Biol., 2008, 28(15), 4896-4914.
[http://dx.doi.org/10.1128/MCB.01775-07] [PMID: 18505826]
[20]
Kessenbrock, K.; Fröhlich, L.; Sixt, M.; Lämmermann, T.; Pfister, H.; Bateman, A.; Belaaouaj, A.; Ring, J.; Ollert, M.; Fässler, R.; Jenne, D.E. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J. Clin. Invest., 2008, 118(7), 2438-2447.
[http://dx.doi.org/10.1172/JCI34694] [PMID: 18568075]
[21]
Kakudo, N.; Minakata, T.; Mitsui, T.; Kushida, S.; Notodihardjo, F.Z.; Kusumoto, K. Proliferation-promoting effect of platelet-rich plasma on human adipose-derived stem cells and human dermal fibroblasts. Plast. Reconstr. Surg., 2008, 122(5), 1352-1360.
[http://dx.doi.org/10.1097/PRS.0b013e3181882046] [PMID: 18971718]
[22]
Mundra, J.J.; Jian, J.; Bhagat, P.; Liu, C.J. Progranulin inhibits expression and release of chemokines CXCL9 and CXCL10 in a TNFR1 dependent manner. Sci. Rep., 2016, 6, 21115.
[http://dx.doi.org/10.1038/srep21115] [PMID: 26892362]
[23]
Montoya, A.; Yepes, L.; Bedoya, A.; Henao, R.; Delgado, G.; Vélez, I.D.; Robledo, S.M. Transforming Growth Factor Beta (TGFβ1) and Epidermal Growth Factor (EGF) as biomarkers of infection and early therapeutic response in cutaneous Leishmaniasis: studies in hamsters. Front. Cell. Infect. Microbiol., 2018, 2(8), 350.
[24]
Yu, Y.; Xu, X.; Liu, L.; Mao, S.; Feng, T.; Lu, Y.; Cheng, Y.; Wang, H.; Zhao, W.; Tang, W. Progranulin deficiency leads to severe inflammation, lung injury and cell death in a mouse model of endotoxic shock. J. Cell. Mol. Med., 2016, 20(3), 506-517.
[http://dx.doi.org/10.1111/jcmm.12756] [PMID: 26757107]
[25]
Luo, Q.; Yan, X.; Tu, H.; Yin, Y.; Cao, J. Progranulin aggravates pulmonary immunopathology during influenza virus infection. Thorax, 2019, 74(3), 305-308.
[http://dx.doi.org/10.1136/thoraxjnl-2018-211916] [PMID: 30228207]
[26]
Li, L.; Li, L.; Xiao, L.; Shangguan, J. Progranulin ameliorates coxsackievirus-B3-induced viral myocarditis by downregulating Th1 and Th17 cells. Exp. Cell Res., 2018, 367(2), 241-250.
[http://dx.doi.org/10.1016/j.yexcr.2018.04.001] [PMID: 29625085]
[27]
Miyagawa, T.; Ichimura, Y.; Nakamura, K.; Hirabayashi, M.; Yamashita, T.; Saigusa, R.; Miura, S.; Takahashi, T.; Toyama, T.; Taniguchi, T.; Akamata, K.; Yoshizaki, A.; Sato, S.; Asano, Y. Progranulin overproduction due to constitutively activated c-Abl/PKC-δ/Fli1 pathway contributes to the resistance of dermal fibroblasts to the anti-fibrotic effect of tumor necrosis factor-α in localized scleroderma. J. Dermatol. Sci., 2018, 92(2), 207-214.
[http://dx.doi.org/10.1016/j.jdermsci.2018.09.005] [PMID: 30268392]
[28]
Yang, T.; Zhang, X.; Chen, A.; Xiao, Y.; Sun, S.; Yan, J.; Cao, Y.; Chen, J.; Li, F.; Huang, K. Progranulin promotes bleomycin-induced skin sclerosis by enhancing TGF-β/Smad3 signaling through up-regulation of TGF-β type I receptor. Am. J. Pathol., 2019, 17, 30947.
[29]
Hyung, S.; Im, S.K.; Lee, B.Y.; Shin, J.; Park, J.C.; Lee, C.; Suh, J.F.; Hur, E.M. Dedifferentiated Schwann cells secrete progranulin that enhances the survival and axon growth of motor neurons. Glia, 2019, 67(2), 360-375.
[http://dx.doi.org/10.1002/glia.23547] [PMID: 30444070]
[30]
Bozyczko-Coyne, D.; McKenna, B.W.; Connors, T.J.; Neff, N.T. A rapid fluorometric assay to measure neuronal survival in vitro. J. Neurosci. Methods, 1993, 50(2), 205-216.
[http://dx.doi.org/10.1016/0165-0270(93)90009-G] [PMID: 8107502]
[31]
Van D, P.; Van H., A.; Lambrechts, D.; Vanacker, P.; Bogaert, E.; Van S., J.; Carmeliet, P.; Van Den B., L.; Robberecht, W. Progranulin functions as a neurotrophic factor to regulate neurite outgrowth and enhance neuronal survival. J. Cell Biol., 2008, 181, 37-41.
[http://dx.doi.org/10.1083/jcb.200712039]
[32]
Ma, Y.; Matsuwaki, T.; Yamanouchi, K.; Nishihara, M. Involvement of progranulin in modulating neuroinflammatory responses but not neurogenesis in the hippocampus of aged mice. Exp. Gerontol., 2017, 95, 1-8.
[http://dx.doi.org/10.1016/j.exger.2017.05.003] [PMID: 28479389]
[33]
Ahmed, Z.; Mackenzie, I.R.; Hutton, M.L.; Dickson, D.W. Progranulin in frontotemporal lobar degeneration and neuroinflammation. J. Neuroinflammation, 2007, 4, 7.
[http://dx.doi.org/10.1186/1742-2094-4-7] [PMID: 17291356]
[34]
Suh, H.S.; Choi, N.; Tarassishin, L.; Lee, S.C. Regulation of progranulin expression in human microglia and proteolysis of progranulin by matrix metalloproteinase-12 (MMP-12). PLoS One, 2012, 7(4)e35115
[http://dx.doi.org/10.1371/journal.pone.0035115] [PMID: 22509390]
[35]
Beel, S.; Herdewyn, S.; Fazal, R.; De Decker, M.; Moisse, M.; Robberecht, W.; Van Den Bosch, L.; Van Damme, P. Progranulin reduces insoluble TDP-43 levels, slows down axonal degeneration and prolongs survival in mutant TDP-43 mice. Mol. Neurodegener., 2018, 13(1), 55.
[http://dx.doi.org/10.1186/s13024-018-0288-y] [PMID: 30326935]
[36]
Suárez-Calvet, M.; Capell, A.; Araque Caballero, MA.; Morenas-Rodríguez, E.; Fellerer, K.; Franzmeier, N.; Kleinberger, G.; Eren, E.; Deming, Y.; Piccio, L.; Karch, C.M.; Cruchaga, C.; Paumier, K.; Bateman, R.J.; Fagan, A.M.; Morris, J.C.; Levin, J.; Danek, A.; Jucker, M.; Masters, C.L.; Rossor, M.N.; Ringman, J.M.; Shaw, L.M.; Trojanowski, J.Q.; Weiner, M.; Ewers, M.; Haass, C. Dominantly Inherited alzheimer network; alzheimer’s disease neuroimaging initiative. CSF progranulin increases in the course of Alzheimer’s disease and is associated with sTREM2, neurodegeneration and cognitive decline. EMBO Mol. Med., 2018, 10(12)pii e9712
[http://dx.doi.org/10.15252/emmm.201809712]
[37]
Van Kampen, J.M. methods to investigate the protection against neurodegenerative disorders provided by progranulin gene transfer in the brain. Methods Mol. Biol., 2018, 1806, 255-267.
[http://dx.doi.org/10.1007/978-1-4939-8559-3_17] [PMID: 29956281]
[38]
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. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature, 2006, 442(7105), 916-919.
[http://dx.doi.org/10.1038/nature05016] [PMID: 16862116]
[39]
Ratnavalli, E.; Brayne, C.; Dawson, K.; Hodges, J.R. The prevalence of frontotemporal dementia. Neurology, 2002, 58(11), 1615-1621.
[http://dx.doi.org/10.1212/WNL.58.11.1615]
[40]
Neary, D.; Snowden, J.; Mann, D. Frontotemporal dementia. Lancet Neurol., 2005, 4(11), 771-780.
[http://dx.doi.org/10.1016/S1474-4422(05)70223-4] [PMID: 16239184]
[41]
Alquézar, C.; de la Encarnación, A.; Moreno, F.; López de Munain, A.; Martín-Requero, Á. Progranulin deficiency induces overactivation of WNT5A expression via TNF-α/NF-κB pathway in peripheral cells from frontotemporal dementia-linked granulin mutation carriers. J. Psychiatry Neurosci., 2016, 41(4), 225-239.
[http://dx.doi.org/10.1503/jpn.150131] [PMID: 26624524]
[42]
Wang, H.; Sun, Y.; Liu, S.; Yu, H.; Li, W.; Zeng, J.; Chen, C.; Jia, J. 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., 2011, 63(1), 82-92.
[http://dx.doi.org/10.1111/j.1574-695X.2011.00833.x] [PMID: 21707777]
[43]
Yang, D.; Li, R.; Wang, H.; Wang, J.; Han, L.; Pan, L.; Li, X.; Kong, Q.; Wang, G.; Su, X. Clinical implications of progranulin in gastric cancer and its regulation via a positive feedback loop involving AKT and ERK signaling pathways. Mol. Med. Rep., 2017, 16(6), 9685-9691.
[http://dx.doi.org/10.3892/mmr.2017.7796] [PMID: 29039535]
[44]
Farzi, N.; Yadegar, A.; Aghdaei, H.A.; Yamaoka, Y.; Zali, M.R. Genetic diversity and functional analysis of oipA gene in association with other virulence factors among Helicobacter pylori isolates from Iranian patients with different gastric diseases. Infect. Genet. Evol., 2018, 60, 26-34.
[http://dx.doi.org/10.1016/j.meegid.2018.02.017] [PMID: 29452293]
[45]
Pormohammad, A.; Mohtavinejad, N.; Gholizadeh, P.; Dabiri, H.; Salimi Chirani, A.; Hashemi, A.; Nasiri, M.J. Global estimate of gastric cancer in Helicobacter pylori-infected population: A systematic review and meta-analysis. J. Cell. Physiol., 2019, 234(2), 1208-1218.
[http://dx.doi.org/10.1002/jcp.27114] [PMID: 30132888]
[46]
Liu, F.; Zhang, W.; Yang, F.; Feng, T.; Zhou, M.; Yu, Y.; Yu, X.; Zhao, W.; Yi, F.; Tang, W.; Lu, Y. Interleukin-6-stimulated progranulin expression contributes to the malignancy of hepatocellular carcinoma cells by activating mTOR signaling. Sci. Rep., 2016, 6, 21260.
[http://dx.doi.org/10.1038/srep21260] [PMID: 26879559]
[47]
Wang, B.C.; Liu, H.; Talwar, A.; Jian, J. New discovery rarely runs smooth: an update on progranulin/TNFR interactions. Protein Cell, 2015, 6(11), 792-803.
[http://dx.doi.org/10.1007/s13238-015-0213-x] [PMID: 26408020]
[48]
Lu, Y.; Zheng, L.; Zhang, W.; Feng, T.; Liu, J.; Wang, X.; Yu, Y.; Qi, M.; Zhao, W.; Yu, X.; Tang, W. Growth factor progranulin contributes to cervical cancer cell proliferation and transformation in vivo and in vitro. Gynecol. Oncol., 2014, 134(2), 364-371.
[http://dx.doi.org/10.1016/j.ygyno.2014.05.025] [PMID: 24905774]
[49]
Feng, T.; Zheng, L.; Liu, F.; Xu, X.; Mao, S.; Wang, X.; Liu, J.; Lu, Y.; Zhao, W.; Yu, X.; Tang, W. Growth factor progranulin promotes tumorigenesis of cervical cancer via PI3K/Akt/mTOR signaling pathway. Oncotarget, 2016, 7(36), 58381-58395.
[http://dx.doi.org/10.18632/oncotarget.11126] [PMID: 27517315]
[50]
Zhang, X.Y.; Pan, Z.X.; Liu, H.; Yu, J.L.; Li, G.X.; Wang, H.Y.; Liu, M.M. Effect of progranulin (PGRN) on the proliferation and senescence of cervical cancer cells. Genet. Mol. Res., 2015, 14(4), 14331-14338.
[PMID: 26600492]
[51]
Wei, Z.; Huang, Y.; Xie, N.; Ma, Q. Elevated expression of secreted autocrine growth factor progranulin increases cervical cancer growth. Cell Biochem. Biophys., 2015, 71(1), 189-193.
[http://dx.doi.org/10.1007/s12013-014-0183-2] [PMID: 25417056]
[52]
Saslow, D.; Solomon, D.; Lawson, H.W.; Killackey, M.; Kulasingam, S.L.; Cain, J.; Garcia, F.A.; Moriarty, A.T.; Waxman, A.G.; Wilbur, D.C.; Wentzensen, N.; Downs, L.S., Jr; Spitzer, M.; Moscicki, A.B.; Franco, E.L.; Stoler, M.H.; Schiffman, M.; Castle, P.E.; Myers, E.R. American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. Am. J. Clin. Pathol., 2012, 137(4), 516-542.
[http://dx.doi.org/10.1309/AJCPTGD94EVRSJCG] [PMID: 22431528]
[53]
Dong, T.; Yang, D.; Li, R.; Zhang, L.; Zhao, H.; Shen, Y.; Zhang, X.; Kong, B.; Wang, L. PGRN promotes migration and invasion of epithelial ovarian cancer cells through an epithelial mesenchymal transition program and the activation of cancer associated fibroblasts. Exp. Mol. Pathol., 2016, 100(1), 17-25.
[http://dx.doi.org/10.1016/j.yexmp.2015.11.021] [PMID: 26607602]
[54]
Ding, D.; Li, C.; Zhao, T.; Li, D.; Yang, L.; Zhang, B. LncRNA H19/miR-29b-3p/PGRN axis promoted epithelial-mesenchymal transition of colorectal cancer cells by acting on Wnt signaling. Mol. Cells, 2018, 41(5), 423-435.
[PMID: 29754471]
[55]
Koo, D.H.; Do, I.G.; Oh, S.; Lee, Y.G.; Kim, K.; Sohn, J.H.; Park, S.K.; Yang, H.J.; Jung, Y.S.; Park, D.I.; Jeong, K.U.; Kim, H.O.; Kim, H.; Serrero, G.; Chun, H.K. KBSMC Colorectal Cancer Team. Prognostic value of progranulin in patients with colorectal cancer treated with curative resection. Pathol. Oncol. Res., 2018, 10, 397-404.
[http://dx.doi.org/10.1007/s12253-018-0520-7] [PMID: 30378010]
[56]
Abrhale, T.; Brodie, A.; Sabnis, G.; Macedo, L.; Tian, C.; Yue, B.; Serrero, G. GP88 (PC-Cell Derived Growth Factor, progranulin) stimulates proliferation and confers letrozole resistance to aromatase overexpressing breast cancer cells. BMC Cancer, 2011, 11, 231.
[http://dx.doi.org/10.1186/1471-2407-11-231] [PMID: 21658239]
[57]
Zanocco-Marani, T.; Bateman, A.; Romano, G.; Valentinis, B.; He, Z.H.; Baserga, R. Biological activities and signaling pathways of the granulin/epithelin precursor. Cancer Res., 1999, 59(20), 5331-5340.
[PMID: 10537317]
[58]
Liu, C.J. Progranulin: a promising therapeutic target for rheumatoid arthritis. FEBS Lett., 2011, 585(23), 3675-3680.
[http://dx.doi.org/10.1016/j.febslet.2011.04.065] [PMID: 21550343]
[59]
Wang, Q.; Xia, Q.; Wu, Y.; Zhang, X.; Wen, F.; Chen, X.; Zhang, S.; Heng, B.C.; He, Y.; Ouyang, H.W. 3D-Printed atsttrin-incorporated alginate/hydroxyapatite scaffold promotes bone defect regeneration with TNF/TNFR signaling involvement. Adv. Healthc. Mater., 2015, 4(11), 1701-1708.
[http://dx.doi.org/10.1002/adhm.201500211] [PMID: 26085382]
[60]
Liu, C.J.; Bosch, X. Progranulin: a growth factor, a novel TNFR ligand and a drug target. Pharmacol. Ther., 2012, 133(1), 124-132.
[http://dx.doi.org/10.1016/j.pharmthera.2011.10.003] [PMID: 22008260]
[61]
Wei, J.L.; Liu, C.J. establishment of a modified collagen-induced arthritis mouse model to investigate the anti-inflammatory activity of progranulin in inflammatory arthritis. Methods Mol. Biol., 2018, 1806, 305-313.
[http://dx.doi.org/10.1007/978-1-4939-8559-3_20] [PMID: 29956284]
[62]
Fu, Y.F.; Gui, R.; Liu, J. HER-2-induced PI3K signaling pathway was involved in the pathogenesis of gastric cancer. Cancer Gene Ther., 2015, 22(3), 145-153.
[http://dx.doi.org/10.1038/cgt.2014.80] [PMID: 25613482]
[63]
Jiang, F.; Wang, H.; Bao, S.; Zhou, H.; Zhang, Y.; Yan, Y.; Lai, Y.; Teng, W.; Shan, Z. Thyrotropin regulates eNOS expression in the endothelium by PGRN through Akt pathway. Front. Endocrinol. (Lausanne), 2018, 9, 353.
[http://dx.doi.org/10.3389/fendo.2018.00353] [PMID: 30026730]
[64]
Radewa, J. [Observations on autophagocytosis phenomena in the blood]. Z. Rheumaforsch., 1963, 22, 36-46.
[PMID: 13972975]
[65]
Liu, J.; Li, H.; Zhou, B.; Xu, L.; Kang, X.; Yang, W.; Wu, S.; Sun, H. PGRN induces impaired insulin sensitivity and defective autophagy in hepatic insulin resistance. Mol. Endocrinol., 2015, 29(4), 528-541.
[http://dx.doi.org/10.1210/me.2014-1266] [PMID: 25664864]
[66]
Guo, Q.; Xu, L.; Li, H.; Sun, H.; Liu, J.; Wu, S.; Zhou, B. Progranulin causes adipose insulin resistance via increased autophagy resulting from activated oxidative stress and endoplasmic reticulum stress. Lipids Health Dis., 2017, 16(1), 25.
[http://dx.doi.org/10.1186/s12944-017-0425-6] [PMID: 28143512]
[67]
Li, H.; Zhou, B.; Liu, J.; Li, F.; Li, Y.; Kang, X.; Sun, H.; Wu, S. Administration of progranulin (PGRN) triggers ER stress and impairs insulin sensitivity via PERK-eIF2α-dependent manner. Cell Cycle, 2015, 14(12), 1893-1907.
[http://dx.doi.org/10.1080/15384101.2015.1041686] [PMID: 26039714]
[68]
Bhopatkar, A.A.; Ghag, G.; Wolf, L.M.; Dean, D.N.; Moss, M.A.; Rangachari, V. Cysteine-rich granulin-3 rapidly promotes amyloid-β fibrils in both redox states. Biochem. J., 2019, 476(5), 859-873.
[http://dx.doi.org/10.1042/BCJ20180916] [PMID: 30782973]
[69]
Butler, V.J.; Cortopassi, W.A.; Argouarch, A.R.; Ivry, S.L.; Craik, C.S.; Jacobson, M.P.; Kao, A.W. Progranulin stimulates the in vitro maturation of pro-cathepsin D at acidic pH. J. Mol. Biol., 2019, 431(5), 1038-1047.
[http://dx.doi.org/10.1016/j.jmb.2019.01.027] [PMID: 30690031]
[70]
Butler, V.; Cortopassi, W.A.; Gururaj, S.; Wang, A.L.; Pierce, O.M.; Jacobson, M.P.; Kao, A.W. Multi-granulin domain peptides bind to pro-cathepsin D and stimulate its enzymatic activity in vitro. Biochemistry, 2019, 58(23), 2670-2674.
[http://dx.doi.org/10.1021/acs.biochem.9b00275] [PMID: 31099551]
[71]
Pawlitzki, M.; Sweeney-Reed, C.M.; Bittner, D.; Lux, A.; Vielhaber, S.; Schreiber, S.; Paul, F.; Neumann, J. CSF-progranulin and neurofilament light chain levels in patients with radiologically isolated syndrome-sign of inflammation. Front. Neurol., 2018, 9, 1075.
[http://dx.doi.org/10.3389/fneur.2018.01075] [PMID: 30619038]
[72]
Chang, M.C.; Srinivasan, K.; Friedman, B.A.; Suto, E.; Modrusan, Z.; Lee, W.P.; Kaminker, J.S.; Hansen, D.V.; Sheng, M. Progranulin deficiency causes impairment of autophagy and TDP-43 accumulation. J. Exp. Med., 2017, 214(9), 2611-2628.
[http://dx.doi.org/10.1084/jem.20160999] [PMID: 28778989]
[73]
Holler, C.J.; Taylor, G.; McEachin, Z.T.; Deng, Q.; Watkins, W.J.; Hudson, K.; Easley, C.A.; Hu, W.T.; Hales, C.M.; Rossoll, W.; Bassell, G.J.; Kukar, T. Trehalose upregulates progranulin expression in human and mouse models of GRN haploinsufficiency: a novel therapeutic lead to treat frontotemporal dementia. Mol. Neurodegener., 2016, 11(1), 46.
[http://dx.doi.org/10.1186/s13024-016-0114-3] [PMID: 27341800]
[74]
Tanaka, Y.; Chambers, J.K.; Matsuwaki, T.; Yamanouchi, K.; Nishihara, M. Possible involvement of lysosomal dysfunction in pathological changes of the brain in aged progranulin-deficient mice. Acta Neuropathol. Commun., 2014, 2, 78.
[http://dx.doi.org/10.1186/s40478-014-0078-x] [PMID: 25022663]
[75]
Li, H.; Zhou, B.; Xu, L.; Liu, J.; Zang, W.; Wu, S.; Sun, H. Circulating PGRN is significantly associated with systemic insulin sensitivity and autophagic activity in metabolic syndrome. Endocrinology, 2014, 155(9), 3493-3507.
[http://dx.doi.org/10.1210/en.2014-1058] [PMID: 24971611]
[76]
Holler, C.J.; Taylor, G.; Deng, Q.; Kukar, T. Intracellular proteolysis of progranulin generates stable, lysosomal granulins that are haploinsufficient in patients with frontotemporal dementia caused by GRN mutations. eNeuro, 2017, 4(4), 4.
[http://dx.doi.org/10.1523/ENEURO.0100-17.2017] [PMID: 28828399]
[77]
Tian, R.; Li, Y.; Yao, X. PGRN suppresses inflammation and promotes autophagy in keratinocytes through the Wnt/β-catenin signaling pathway. Inflammation, 2016, 39(4), 1387-1394.
[http://dx.doi.org/10.1007/s10753-016-0370-y] [PMID: 27239673]
[78]
Farag, A.G.A.; Shoaib, M.A.; Samaka, R.M.; Abdou, A.G.; Mandour, M.M.; Ibrahim, R.A.L. Progranulin and beta-catenin in psoriasis: An immunohistochemical study. J. Cosmet. Dermatol., 2019, 18(6), 2019-2026.
[http://dx.doi.org/10.1111/jocd.12966] [PMID: 31091001]
[79]
Zhang, K.; Li, G.Q.; He, Q.H.; Li, Y.; Tang, M.; Zheng, Q.Y.; Xu, G.L.; Zhang, K.Q. C5a/C5aR pathway accelerates renal ischemia-reperfusion injury by downregulating PGRN expression. Int. Immunopharmacol., 2017, 53, 17-23.
[http://dx.doi.org/10.1016/j.intimp.2017.10.006] [PMID: 29031143]
[80]
Xu, X.; Gou, L.; Zhou, M.; Yang, F.; Zhao, Y.; Feng, T.; Shi, P.; Ghavamian, A.; Zhao, W.; Yu, Y.; Lu, Y.; Yi, F.; Liu, G.; Tang, W. Progranulin protects against endotoxin-induced acute kidney injury by downregulating renal cell death and inflammatory responses in mice. Int. Immunopharmacol., 2016, 38, 409-419.
[http://dx.doi.org/10.1016/j.intimp.2016.06.022] [PMID: 27367257]
[81]
Assmann, G.; Zinke, S.; Gerling, M.; Bittenbring, J.T.; Preuss, K.D.; Thurner, L. Progranulin-autoantibodies in sera of rheumatoid arthritis patients negative for rheumatoid factor and anti-citrullinated peptide antibodies. Clin. Exp. Rheumatol., 2019, •••, 10.
[PMID: 31074725]
[82]
Kamei, N.; Yamashita, M.; Nishizaki, Y.; Yanagisawa, N.; Nojiri, S.; Tanaka, K.; Yamashita, Y.; Shibata, T.; Murakoshi, M.; Suzuki, Y.; Gohda, T. Association between circulating tumor necrosis factor-related biomarkers and estimated glomerular filtration rate in type 2 diabetes. Sci. Rep., 2018, 8(1), 15302.
[http://dx.doi.org/10.1038/s41598-018-33590-w] [PMID: 30333553]
[83]
Zhou, X.; Wang, X.; Pal, R.; Ivanov, I.; Bittner, M.; Dougherty, E.R. A Bayesian connectivity-based approach to constructing probabilistic gene regulatory networks. Bioinformatics, 2004, 20(17), 2918-2927.
[http://dx.doi.org/10.1093/bioinformatics/bth318] [PMID: 15145802]
[84]
Jian, J.; Chen, Y.; Liberti, R.; Fu, W.; Hu, W.; Saunders-Pullman, R.; Pastores, G.M.; Chen, Y.; Sun, Y.; Grabowski, G.A.; Liu, C.J. Chitinase-3-like protein 1: a progranulin downstream molecule and potential biomarker for Gaucher disease. EBioMedicine, 2018, 28, 251-260.
[http://dx.doi.org/10.1016/j.ebiom.2018.01.022] [PMID: 29396296]
[85]
Zhang, K.; Li, Y.J.; Guo, Y.; Zheng, K.Y.; Yang, Q.; Yang, L.; Wang, X.S.; Song, Q.; Chen, T.; Zhuo, M.; Zhao, M.G. Elevated progranulin contributes to synaptic and learning deficit due to loss of fragile X mental retardation protein. Brain, 2017, 140(12), 3215-3232.
[http://dx.doi.org/10.1093/brain/awx265] [PMID: 29096020]
[86]
Eguchi, R.; Nakano, T.; Wakabayashi, I. Progranulin and granulin-like protein as novel VEGF-independent angiogenic factors derived from human mesothelioma cells. Oncogene, 2017, 36(5), 714-722.
[http://dx.doi.org/10.1038/onc.2016.226] [PMID: 27345409]
[87]
Choi, G.S.; Trinh, H.K.T.; Yang, E.M.; Ye, Y.M.; Shin, Y.S.; Kim, S.H.; Park, H.S. Role of clusterin/progranulin in toluene diisocyanate-induced occupational asthma. Exp. Mol. Med., 2018, 50(5), 58.
[http://dx.doi.org/10.1038/s12276-018-0085-2] [PMID: 29717106]
[88]
Park, B.; Buti, L.; Lee, S.; Matsuwaki, T.; Spooner, E.; Brinkmann, M.M.; Nishihara, M.; Ploegh, H.L. Granulin is a soluble cofactor for toll-like receptor 9 signaling. Immunity, 2011, 34(4), 505-513.
[http://dx.doi.org/10.1016/j.immuni.2011.01.018] [PMID: 21497117]
[89]
Wang, Z.; He, Q.; Zhang, X.; Ma, Y.; Fan, F.; Dong, Y.; Xu, W.; Yin, Y.; He, Y. Innate Anti-microbial and anti-chemotaxis properties of progranulin in an acute otitis media mouse model. Front. Immunol., 2018, 9, 2952.
[http://dx.doi.org/10.3389/fimmu.2018.02952] [PMID: 30619312]
[90]
Li, Y.; Li, S.; Li, Y.; Xia, H.; Mao, Q. Generation of a novel HEK293 luciferase reporter cell line by CRISPR/Cas9-mediated site-specific integration in the genome to explore the transcriptional regulation of the PGRN gene. Bioengineered, 2019, 10(1), 98-107.
[http://dx.doi.org/10.1080/21655979.2019.1607126] [PMID: 31023186]
[91]
Li, Y.; Wang, D.; Li, Y.; Zhu, J.; Zhao, J.; Deng, Y.; Rogalski, E.J.; Bigio, E.H.; Rademaker, A.W.; Xia, H.; Mao, Q. A highly sensitive sandwich ELISA to Detect CSF progranulin: a potential biomarker for CNS disorders. J. Neuropathol. Exp. Neurol., 2019, 78(5), 406-415.
[http://dx.doi.org/10.1093/jnen/nlz022] [PMID: 30939191]
[92]
Hossein-Nezhad, A.; Mirzaei, K.; Ansar, H.; Emam-Gholipour, S.; Tootee, A.; Keshavarz, S.A. Obesity, inflammation and resting energy expenditure: possible mechanism of progranulin in this pathway. Minerva Endocrinol., 2012, 37(3), 255-266.
[PMID: 22766892]
[93]
Nicoletto, B.B.; Sarmento, R.A.; Pedrollo, E.F.; Krolikowski, T.C.; Canani, L.H. Association between progranulin serum levels and dietary intake. PLoS One, 2018, 13(8)e0202149
[http://dx.doi.org/10.1371/journal.pone.0202149] [PMID: 30118483]
[94]
Kojima, Y.; Ono, K.; Inoue, K.; Takagi, Y.; Kikuta, K.; Nishimura, M.; Yoshida, Y.; Nakashima, Y.; Matsumae, H.; Furukawa, Y.; Mikuni, N.; Nobuyoshi, M.; Kimura, T.; Kita, T.; Tanaka, M. Progranulin expression in advanced human atherosclerotic plaque. Atherosclerosis, 2009, 206(1), 102-108.
[http://dx.doi.org/10.1016/j.atherosclerosis.2009.02.017] [PMID: 19321167]
[95]
Xie, W.; Lu, Q.; Wang, K.; Lu, J.; Gu, X.; Zhu, D.; Liu, F.; Guo, Z. miR-34b-5p inhibition attenuates lung inflammation and apoptosis in an LPS-induced acute lung injury mouse model by targeting progranulin. J. Cell. Physiol., 2018, 233(9), 6615-6631.
[http://dx.doi.org/10.1002/jcp.26274] [PMID: 29150939]

© 2024 Bentham Science Publishers | Privacy Policy