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Review

Progranulin as a Potential Therapeutic Target in Immune-Mediated Diseases

, , , &
Pages 6543-6556 | Published online: 04 Dec 2021

References

  • Tao JH, Cheng M, Tang JP, Liu Q, Pan F, Li XP. Foxp3, regulatory T cell, and autoimmune diseases. Inflammation. 2017;40(1):328–339. doi:10.1007/s10753-016-0470-8
  • Abdolmaleki F, Kovanen PT, Mardani R, Gheibi-Hayat SM, Bo S, Sahebkar A. Resolvins: emerging players in autoimmune and inflammatory diseases. Clin Rev Allergy Immunol. 2020;58(1):82–91. doi:10.1007/s12016-019-08754-9
  • Jian J, Konopka J, Liu C. Insights into the role of progranulin in immunity, infection, and inflammation. J Leukoc Biol. 2013;93(2):199–208. doi:10.1189/jlb.0812429
  • Wei F, Zhang Y, Zhao W, Yu X, Liu CJ. Progranulin facilitates conversion and function of regulatory T cells under inflammatory conditions. PLoS One. 2014;9(11):e112110. doi:10.1371/journal.pone.0112110
  • Tang W, Lu Y, Tian QY, et al. The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science. 2011;332(6028):478–484. doi:10.1126/science.1199214
  • Wei F, Zhang Y, Jian J, et al. PGRN protects against colitis progression in mice in an IL-10 and TNFR2 dependent manner. Sci Rep. 2014;4:7023. doi:10.1038/srep07023
  • 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. doi:10.1016/j.yexcr.2018.04.001
  • Park B, Buti L, Lee S, et al. Granulin is a soluble cofactor for toll-like receptor 9 signaling. Immunity. 2011;34(4):505–513. doi:10.1016/j.immuni.2011.01.018
  • Shen HH, Yang YX, Meng X, et al. NLRP3: a promising therapeutic target for autoimmune diseases. Autoimmun Rev. 2018;17(7):694–702. doi:10.1016/j.autrev.2018.01.020
  • Moresco EM, Beutler B. Special delivery: granulin brings CpG DNA to Toll-like receptor 9. Immunity. 2011;34(4):453–455. doi:10.1016/j.immuni.2011.04.001
  • Cui Y, Hettinghouse A, Liu CJ. Progranulin: a conductor of receptors orchestra, a chaperone of lysosomal enzymes and a therapeutic target for multiple diseases. Cytokine Growth Factor Rev. 2019;45:53–64. doi:10.1016/j.cytogfr.2019.01.002
  • Jing C, Zhang X, Song Z, Zheng Y, Yin Y. Progranulin Mediates Proinflammatory Responses in Systemic Lupus Erythematosus: implications for the Pathogenesis of Systemic Lupus Erythematosus. J Interferon Cytokine Res. 2020;40(1):33–42. doi:10.1089/jir.2019.0047
  • Bateman A, Cheung ST, Bennett HPJ, Brief A. Overview of Progranulin in Health and Disease. Methods Mol Biol. 2018;1806:3–15.
  • Bhandari V, Palfree RG, Bateman A. Isolation and sequence of the granulin precursor cDNA from human bone marrow reveals tandem cysteine-rich granulin domains. Proc Natl Acad Sci U S A. 1992;89(5):1715–1719. doi:10.1073/pnas.89.5.1715
  • Hrabal R, Chen Z, James S, Bennett HP, 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. doi:10.1038/nsb0996-747
  • Palfree RG, Bennett HP, Bateman A. The Evolution of the Secreted Regulatory Protein Progranulin. PLoS One. 2015;10(8):e0133749. doi:10.1371/journal.pone.0133749
  • Plowman GD, Green JM, Neubauer MG, et al. The epithelin precursor encodes two proteins with opposing activities on epithelial cell growth. J Biol Chem. 1992;267(18):13073–13078. doi:10.1016/S0021-9258(18)42382-4
  • Jian J, Li G, Hettinghouse A, Liu C. Progranulin: a key player in autoimmune diseases. Cytokine. 2018;101:48–55. doi:10.1016/j.cyto.2016.08.007
  • Daniel R, He Z, Carmichael KP, Halper J, Bateman A. Cellular localization of gene expression for progranulin. J Histochem Cytochem. 2000;48(7):999–1009. doi:10.1177/002215540004800713
  • Petkau TL, Leavitt BR. Progranulin in neurodegenerative disease. Trends Neurosci. 2014;37(7):388–398. doi:10.1016/j.tins.2014.04.003
  • Matsubara T, Mita A, Minami K, et al. PGRN is a key adipokine mediating high fat diet-induced insulin resistance and obesity through IL-6 in adipose tissue. Cell Metab. 2012;15(1):38–50. doi:10.1016/j.cmet.2011.12.002
  • Abella V, Scotece M, Conde J, et al. The novel adipokine progranulin counteracts IL-1 and TLR4-driven inflammatory response in human and murine chondrocytes via TNFR1. Sci Rep. 2016;6:20356. doi:10.1038/srep20356
  • Pan CX, Kinch MS, Kiener PA, et al. PC cell-derived growth factor expression in prostatic intraepithelial neoplasia and prostatic adenocarcinoma. Clin Cancer Res. 2004;10(4):1333–1337. doi:10.1158/1078-0432.CCR-1123-03
  • Cheung PF, Cheng CK, Wong NC, et al. Granulin-epithelin precursor is an oncofetal protein defining hepatic cancer stem cells. PLoS One. 2011;6(12):e28246. doi:10.1371/journal.pone.0028246
  • Farag AGA, Shoaib MA, Samaka RM, Abdou AG, Mandour MM, Ibrahim RAL. Progranulin and beta-catenin in psoriasis: an immunohistochemical study. J Cosmet Dermatol. 2019;18(6):2019–2026. doi:10.1111/jocd.12966
  • Xu D, Suenaga N, Edelmann MJ, Fridman R, Muschel RJ, Kessler BM. Novel MMP-9 substrates in cancer cells revealed by a label-free quantitative proteomics approach. Mol Cell Proteomics. 2008;7(11):2215–2228. doi:10.1074/mcp.M800095-MCP200
  • Suh HS, Choi N, Tarassishin L, Lee SC. Regulation of progranulin expression in human microglia and proteolysis of progranulin by matrix metalloproteinase-12 (MMP-12). PLoS One. 2012;7(4):e35115. doi:10.1371/journal.pone.0035115
  • Butler GS, Dean RA, Tam EM, Overall CM. 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. doi:10.1128/MCB.01775-07
  • Ungurs MJ, Sinden NJ, Stockley RA. Progranulin is a substrate for neutrophil-elastase and proteinase-3 in the airway and its concentration correlates with mediators of airway inflammation in COPD. Am J Physiol Lung Cell Mol Physiol. 2014;306(1):L80–87. doi:10.1152/ajplung.00221.2013
  • Kessenbrock K, Frohlich L, Sixt M, et al. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J Clin Invest. 2008;118(7):2438–2447. doi:10.1172/JCI34694
  • Zhu J, Nathan C, Jin W, et al. Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell. 2002;111(6):867–878. doi:10.1016/S0092-8674(02)01141-8
  • Vercellino M, Grifoni S, Romagnolo A, et al. Progranulin expression in brain tissue and cerebrospinal fluid levels in multiple sclerosis. Mult Scler. 2011;17(10):1194–1201. doi:10.1177/1352458511406164
  • Samejima T, Nagamatsu T, Akiba N, et al. Secretory leukocyte protease inhibitor and progranulin as possible regulators of cervical remodeling in pregnancy. J Reprod Immunol. 2021;143:103241. doi:10.1016/j.jri.2020.103241
  • Okura H, Yamashita S, Ohama T, et al. HDL/apolipoprotein A-I binds to macrophage-derived progranulin and suppresses its conversion into proinflammatory granulins. J Atheroscler Thromb. 2010;17(6):568–577. doi:10.5551/jat.3921
  • Liu CJ. Progranulin: a promising therapeutic target for rheumatoid arthritis. FEBS Lett. 2011;585(23):3675–3680. doi:10.1016/j.febslet.2011.04.065
  • Tian Q, Zhao Y, Mundra JJ, et al. Three TNFR-binding domains of PGRN act independently in inhibition of TNF-alpha binding and activity. Front Biosci. 2014;19:1176–1185. doi:10.2741/4274
  • Tian Q, Zhao S, Liu C. A solid-phase assay for studying direct binding of progranulin to TNFR and progranulin antagonism of TNF/TNFR interactions. Methods Mol Biol. 2014;1155:163–172.
  • Thurner L, Fadle N, Regitz E, et al. The molecular basis for development of proinflammatory autoantibodies to progranulin. J Autoimmun. 2015;61:17–28. doi:10.1016/j.jaut.2015.05.002
  • Liu C, Li XX, Gao W, Liu W, Liu DS. Progranulin-derived Atsttrin directly binds to TNFRSF25 (DR3) and inhibits TNF-like ligand 1A (TL1A) activity. PLoS One. 2014;9(3):e92743. doi:10.1371/journal.pone.0092743
  • Chen J, Li S, Shi J, et al. Serum progranulin irrelated with Breg cell levels, but elevated in RA patients, reflecting high disease activity. Rheumatol Int. 2016;36(3):359–364. doi:10.1007/s00296-015-3372-4
  • Tian G, Jin X, Wang Q, Ye T, Li G, Liu J. Recent advances in the study of progranulin and its role in sepsis. Int Immunopharmacol. 2020;79:106090. doi:10.1016/j.intimp.2019.106090
  • Fu W, Hu W, Shi L, et al. Foxo4- and Stat3-dependent IL-10 production by progranulin in regulatory T cells restrains inflammatory arthritis. FASEB J. 2017;31(4):1354–1367. doi:10.1096/fj.201601134R
  • Johnson Z, Power CA, Weiss C, et al. Chemokine inhibition–why, when, where, which and how? Biochem Soc Trans. 2004;32(Pt 2):366–377. doi:10.1042/bst0320366
  • Kuan WP, Tam LS, Wong CK, et al. CXCL 9 and CXCL 10 as Sensitive markers of disease activity in patients with rheumatoid arthritis. J Rheumatol. 2010;37(2):257–264. doi:10.3899/jrheum.090769
  • Lee EY, Lee ZH, Song YW. The interaction between CXCL10 and cytokines in chronic inflammatory arthritis. Autoimmun Rev. 2013;12(5):554–557. doi:10.1016/j.autrev.2012.10.001
  • Ruschpler P, Lorenz P, Eichler W, et al. High CXCR3 expression in synovial mast cells associated with CXCL9 and CXCL10 expression in inflammatory synovial tissues of patients with rheumatoid arthritis. Arthritis Res Ther. 2003;5(5):R241–252. doi:10.1186/ar783
  • Mundra JJ, Jian J, Bhagat P, Liu CJ. Progranulin inhibits expression and release of chemokines CXCL9 and CXCL10 in a TNFR1 dependent manner. Sci Rep. 2016;6:21115. doi:10.1038/srep21115
  • Xu K, Zhang Y, Ilalov K, et al. Cartilage oligomeric matrix protein associates with granulin-epithelin precursor (GEP) and potentiates GEP-stimulated chondrocyte proliferation. J Biol Chem. 2007;282(15):11347–11355. doi:10.1074/jbc.M608744200
  • Feng JQ, Guo FJ, Jiang BC, et al. Granulin epithelin precursor: a bone morphogenic protein 2-inducible growth factor that activates Erk1/2 signaling and JunB transcription factor in chondrogenesis. FASEB J. 2010;24(6):1879–1892. doi:10.1096/fj.09-144659
  • Zhao YP, Tian QY, Frenkel S, Liu CJ. The promotion of bone healing by progranulin, a downstream molecule of BMP-2, through interacting with TNF/TNFR signaling. Biomaterials. 2013;34(27):6412–6421. doi:10.1016/j.biomaterials.2013.05.030
  • Wei J, Zhang L, Ding Y, et al. Progranulin promotes diabetic fracture healing in mice with type 1 diabetes. Ann N Y Acad Sci. 2020;1460(1):43–56. doi:10.1111/nyas.14208
  • Turesson C, Bergstrom U, Jacobsson LT, Truedsson L, Berglund G, Saxne T. Increased cartilage turnover and circulating autoantibodies in different subsets before the clinical onset of rheumatoid arthritis. Ann Rheum Dis. 2011;70(3):520–522. doi:10.1136/ard.2010.131896
  • Posey KL, Coustry F, Hecht JT. Cartilage oligomeric matrix protein: cOMPopathies and beyond. Matrix Biol. 2018;71–72:161–173. doi:10.1016/j.matbio.2018.02.023
  • Wang N, Zhang J, Yang JX. Growth factor progranulin blocks tumor necrosis factor-alpha-mediated inhibition of osteoblast differentiation. Genet Mol Res. 2016;15(3):215.
  • Neidhart M, Hauser N, Paulsson M, DiCesare PE, Michel BA, Hauselmann HJ. Small fragments of cartilage oligomeric matrix protein in synovial fluid and serum as markers for cartilage degradation. Br J Rheumatol. 1997;36(11):1151–1160. doi:10.1093/rheumatology/36.11.1151
  • Liu CJ, Kong W, Ilalov K, et al. ADAMTS-7: a metalloproteinase that directly binds to and degrades cartilage oligomeric matrix protein. FASEB J. 2006;20(7):988–990. doi:10.1096/fj.05-3877fje
  • Liu CJ, Kong W, Xu K, et al. ADAMTS-12 associates with and degrades cartilage oligomeric matrix protein. J Biol Chem. 2006;281(23):15800–15808. doi:10.1074/jbc.M513433200
  • Guo F, Lai Y, Tian Q, Lin EA, Kong L, Liu C. Granulin-epithelin precursor binds directly to ADAMTS-7 and ADAMTS-12 and inhibits their degradation of cartilage oligomeric matrix protein. Arthritis Rheum. 2010;62(7):2023–2036. doi:10.1002/art.27491
  • Hemmi H, Takeuchi O, Kawai T, et al. A Toll-like receptor recognizes bacterial DNA. Nature. 2000;408(6813):740–745. doi:10.1038/35047123
  • Krieg AM. CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol. 2002;20:709–760. doi:10.1146/annurev.immunol.20.100301.064842
  • Latz E, Verma A, Visintin A, et al. Ligand-induced conformational changes allosterically activate Toll-like receptor 9. Nat Immunol. 2007;8(7):772–779. doi:10.1038/ni1479
  • Kim YM, Brinkmann MM, Paquet ME, Ploegh HL. UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature. 2008;452(7184):234–238. doi:10.1038/nature06726
  • Ewald SE, Lee BL, Lau L, et al. The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature. 2008;456(7222):658–662. doi:10.1038/nature07405
  • Avalos AM, Kirak O, Oelkers JM, et al. Cell-specific TLR9 trafficking in primary APCs of transgenic TLR9-GFP mice. J Immunol. 2013;190(2):695–702. doi:10.4049/jimmunol.1202342
  • Latz E, Schoenemeyer A, Visintin A, et al. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat Immunol. 2004;5(2):190–198. doi:10.1038/ni1028
  • Wei W, Ren J, Yin W, et al. Inhibition of Ctsk modulates periodontitis with arthritis via downregulation of TLR9 and autophagy. Cell Prolif. 2020;53(1):e12722. doi:10.1111/cpr.12722
  • Tanaka A, Tsukamoto H, Mitoma H, et al. Serum progranulin levels are elevated in patients with systemic lupus erythematosus, reflecting disease activity. Arthritis Res Ther. 2012;14(6):R244. doi:10.1186/ar4087
  • Wu GC, Pan HF, Leng RX, et al. Emerging role of long noncoding RNAs in autoimmune diseases. Autoimmun Rev. 2015;14(9):798–805. doi:10.1016/j.autrev.2015.05.004
  • Pan HF, Li XP, Zheng SG, Ye DQ. Emerging role of interleukin-22 in autoimmune diseases. Cytokine Growth Factor Rev. 2013;24(1):51–57. doi:10.1016/j.cytogfr.2012.07.002
  • Shao L, Hou C. miR-138 activates NF-kappaB signaling and PGRN to promote rheumatoid arthritis via regulating HDAC4. Biochem Biophys Res Commun. 2019;519(1):166–171. doi:10.1016/j.bbrc.2019.08.092
  • Atzeni F, Nucera V, Masala IF, Sarzi-Puttini P, Bonitta G. Il-6 Involvement in pain, fatigue and mood disorders in rheumatoid arthritis and the effects of Il-6 inhibitor sarilumab. Pharmacol Res. 2019;149:104402. doi:10.1016/j.phrs.2019.104402
  • Yamamoto Y, Takemura M, Serrero G, et al. Increased serum GP88 (Progranulin) concentrations in rheumatoid arthritis. Inflammation. 2014;37(5):1806–1813. doi:10.1007/s10753-014-9911-4
  • Thurner L, Preuss KD, Fadle N, et al. Progranulin antibodies in autoimmune diseases. J Autoimmun. 2013;42:29–38. doi:10.1016/j.jaut.2012.10.003
  • Mills JA. Systemic lupus erythematosus. N Engl J Med. 1994;330(26):1871–1879. doi:10.1056/NEJM199406303302608
  • Choi MY, Flood K, Bernatsky S, Ramsey-Goldman R, Clarke AE. A review on SLE and malignancy. Best Pract Res Clin Rheumatol. 2017;31(3):373–396. doi:10.1016/j.berh.2017.09.013
  • Qiu F, Song L, Ding F, et al. Expression level of the growth factor progranulin is related with development of systemic lupus erythematosus. Diagn Pathol. 2013;8:88. doi:10.1186/1746-1596-8-88
  • Yang T, Zhang X, Chen A, et al. Progranulin Promotes Bleomycin-Induced Skin Sclerosis by Enhancing Transforming Growth Factor-beta/Smad3 Signaling through Up-Regulation of Transforming Growth Factor-beta Type I Receptor. Am J Pathol. 2019;189(8):1582–1593. doi:10.1016/j.ajpath.2019.04.012
  • Abraham DJ, Varga J. Scleroderma: from cell and molecular mechanisms to disease models. Trends Immunol. 2005;26(11):587–595. doi:10.1016/j.it.2005.09.004
  • Bhattacharyya S, Wei J, Varga J. Understanding fibrosis in systemic sclerosis: shifting paradigms, emerging opportunities. Nat Rev Rheumatol. 2011;8(1):42–54. doi:10.1038/nrrheum.2011.149
  • van den Hoogen F, Khanna D, Fransen J, et al. 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis. 2013;72(11):1747–1755. doi:10.1136/annrheumdis-2013-204424
  • Miyagawa T, Ichimura Y, Nakamura K, et al. Progranulin overproduction due to constitutively activated c-Abl/PKC-delta/Fli1 pathway contributes to the resistance of dermal fibroblasts to the anti-fibrotic effect of tumor necrosis factor-alpha in localized scleroderma. J Dermatol Sci. 2018;92(2):207–214. doi:10.1016/j.jdermsci.2018.09.005
  • Hasegawa M, Sato S, Nagaoka T, Fujimoto M, Takehara K. Serum levels of tumor necrosis factor and interleukin-13 are elevated in patients with localized scleroderma. Dermatology. 2003;207(2):141–147. doi:10.1159/000071783
  • Ramirez J, Hernandez MV, Galve J, Canete JD, Sanmarti R. Morphea associated with the use of Adalimumab: a case report and review of the literature. Mod Rheumatol. 2012;22(4):602–604. doi:10.3109/s10165-011-0550-4
  • Mattozzi C, Richetta AG, Cantisani C, et al. Morphea, an unusual side effect of anti-TNF-alpha treatment. Eur J Dermatol. 2010;20(3):400–401. doi:10.1684/ejd.2010.0946
  • Kaser A, Zeissig S, Blumberg RS. Inflammatory bowel disease. Annu Rev Immunol. 2010;28:573–621. doi:10.1146/annurev-immunol-030409-101225
  • Atreya I, Atreya R, Neurath MF. NF-kappaB in inflammatory bowel disease. J Intern Med. 2008;263(6):591–596. doi:10.1111/j.1365-2796.2008.01953.x
  • Thurner L, Stoger E, Fadle N, et al. Proinflammatory progranulin antibodies in inflammatory bowel diseases. Dig Dis Sci. 2014;59(8):1733–1742. doi:10.1007/s10620-014-3089-3
  • Tian R, Li Y, Yao X. PGRN Suppresses Inflammation and Promotes Autophagy in Keratinocytes Through the Wnt/beta-Catenin Signaling Pathway. Inflammation. 2016;39(4):1387–1394. doi:10.1007/s10753-016-0370-y
  • Greb JE, Goldminz AM, Elder JT, et al. Psoriasis. Nat Rev Dis Primers. 2016;2:16082. doi:10.1038/nrdp.2016.82
  • Huang K, Chen A, Zhang X, et al. Progranulin is preferentially expressed in patients with psoriasis vulgaris and protects mice from psoriasis-like skin inflammation. Immunology. 2015;145(2):279–287. doi:10.1111/imm.12446
  • Zheng P, Li Z, Zhou Z. Gut microbiome in type 1 diabetes: a comprehensive review. Diabetes Metab Res Rev. 2018;34(7):e3043. doi:10.1002/dmrr.3043
  • Oh J, Vidal-Jordana A, Montalban X. Multiple sclerosis: clinical aspects. Curr Opin Neurol. 2018;31(6):752–759. doi:10.1097/WCO.0000000000000622
  • Chalah MA, Ayache SS. Is there a link between inflammation and fatigue in multiple sclerosis? J Inflamm Res. 2018;11:253–264. doi:10.2147/JIR.S167199
  • Pawlitzki M, Sweeney-Reed CM, Bittner D, et al. CSF-Progranulin and Neurofilament Light Chain Levels in Patients With Radiologically Isolated Syndrome-Sign of Inflammation. Front Neurol. 2018;9:1075. doi:10.3389/fneur.2018.01075
  • Jiao J, Herl LD, Farese RV, Gao FB. MicroRNA-29b regulates the expression level of human progranulin, a secreted glycoprotein implicated in frontotemporal dementia. PLoS One. 2010;5(5):e10551. doi:10.1371/journal.pone.0010551
  • Chen L, Li Q, Wang J, et al. MiR-29b-3p promotes chondrocyte apoptosis and facilitates the occurrence and development of osteoarthritis by targeting PGRN. J Cell Mol Med. 2017;21(12):3347–3359. doi:10.1111/jcmm.13237
  • Xie W, Lu Q, Wang K, et al. 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. doi:10.1002/jcp.26274
  • Miyakawa S, Sakuma H, Warude D, et al. Anti-sortilin1 Antibody Up-Regulates Progranulin via Sortilin1 Down-Regulation. Front Neurosci. 2020;14:586107. doi:10.3389/fnins.2020.586107
  • Xia Q, Zhu S, Wu Y, et al. Intra-articular transplantation of atsttrin-transduced mesenchymal stem cells ameliorate osteoarthritis development. Stem Cells Transl Med. 2015;4(5):523–531. doi:10.5966/sctm.2014-0200
  • Bateman A, Bennett HP. The granulin gene family: from cancer to dementia. Bioessays. 2009;31(11):1245–1254. doi:10.1002/bies.200900086
  • Matsumura N, Mandai M, Miyanishi M, et al. Oncogenic property of acrogranin in human uterine leiomyosarcoma: direct evidence of genetic contribution in in vivo tumorigenesis. Clin Cancer Res. 2006;12(5):1402–1411. doi:10.1158/1078-0432.CCR-05-2003
  • Altmann C, Vasic V, Hardt S, et al. Progranulin promotes peripheral nerve regeneration and reinnervation: role of notch signaling. Mol Neurodegener. 2016;11(1):69. doi:10.1186/s13024-016-0132-1
  • Neill T, Buraschi S, Goyal A, et al. EphA2 is a functional receptor for the growth factor progranulin. J Cell Biol. 2016;215(5):687–703. doi:10.1083/jcb.201603079
  • Kuksin CA, Minter LM. The Link between Autoimmunity and Lymphoma: does NOTCH Signaling Play a Contributing Role? Front Oncol. 2015;5:51. doi:10.3389/fonc.2015.00051
  • Khanmohammadi S, Shabani M, Tabary M, Rayzan E, Rezaei N. Lymphoma in the setting of autoimmune diseases: a review of association and mechanisms. Crit Rev Oncol Hematol. 2020;150:102945. doi:10.1016/j.critrevonc.2020.102945
  • Huang J, Liang Y, Tian W, et al. Antitumor Activity and Mechanism of Robustic Acid from Dalbergia benthami Prain via Computational Target Fishing. Molecules. 2020;25(17):254. doi:10.3390/molecules25173919