Regulation of progranulin expression in human microglia and proteolysis of progranulin by matrix metalloproteinase-12 (mmp-12)

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Suh, Hyeon Sook ^a   Choi, Namjong ^a   Tarassishin, Leonid ^a   Lee, Sunhee C ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 13; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; MACROPHAGE ELASTASE; POLYINOSINIC POLYCYTIDYLIC ACID; PROGRANULIN; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; GRN PROTEIN, HUMAN; SIGNAL PEPTIDE;

ARTICLE; ASTROCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROGLIA; NERVE CELL STIMULATION; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REGULATORY MECHANISM; CELL CULTURE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; INNATE IMMUNITY; METABOLISM; SIGNAL TRANSDUCTION;

ASTROCYTES; CELLS, CULTURED; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MATRIX METALLOPROTEINASE 12; MICROGLIA; PROTEOLYSIS; RNA, SMALL INTERFERING; SECRETORY LEUKOCYTE PEPTIDASE INHIBITOR; SIGNAL TRANSDUCTION;

EID: 84859590507     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035115     Document Type: Article

References (59)

1. 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.
2. Ahmed Z, Mackenzie IR, Hutton ML, Dickson DW, (2007) Progranulin in frontotemporal lobar degeneration and neuroinflammation. J Neuroinflammation 4: 7.
3. Daniel R, Daniels E, He Z, Bateman A, (2003) Progranulin (acrogranin/PC cell-derived growth factor/granulin-epithelin precursor) is expressed in the placenta, epidermis, microvasculature, and brain during murine development. Dev Dyn 227: 593-599.
4. He Z, Ong CH, Halper J, Bateman A, (2003) Progranulin is a mediator of the wound response. Nat Med 9: 225-229.
5. De ML, Van DP, (2011) Cellular Effects of Progranulin in Health and Disease. J Mol Neurosci.
6. Wang J, Van DP, Cruchaga C, Gitcho MA, Vidal JM, et al. (2010) Pathogenic cysteine mutations affect progranulin function and production of mature granulins. J Neurochem 112: 1305-1315.
7. Kessenbrock K, Frohlich L, Sixt M, Lammermann T, Pfister H, et al. (2008) Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J Clin Invest 118: 2438-2447.
8. Zhu J, Nathan C, Jin W, Sim D, Ashcroft GS, et al. (2002) Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 111: 867-878.
9. Kojima Y, Ono K, Inoue K, Takagi Y, Kikuta K, et al. (2009) Progranulin expression in advanced human atherosclerotic plaque. Atherosclerosis 206: 102-108.
10. Baker M, Mackenzie IR, Pickering-Brown SM, Gass J, Rademakers R, et al. (2006) Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442: 916-919.
11. Cruts M, Gijselinck I, van der ZJ, Engelborghs S, Wils H, et al. (2006) Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442: 920-924.
12. Sleegers K, Cruts M, Van BC, (2010) Molecular pathways of frontotemporal lobar degeneration. Annu Rev Neurosci 33: 71-88.
13. Pereson S, Wils H, Kleinberger G, McGowan E, Vandewoestyne M, et al. (2009) Progranulin expression correlates with dense-core amyloid plaque burden in Alzheimer disease mouse models. J Pathol 219: 173-181.
14. Vercellino M, Grifoni S, Romagnolo A, Masera S, Mattioda A, et al. (2011) Progranulin expression in brain tissue and cerebrospinal fluid levels in multiple sclerosis. Mult Scler 17: 1194-1201.
15. Chen-Plotkin AS, Xiao J, Geser F, Martinez-Lage M, Grossman M, et al. (2010) Brain progranulin expression in GRN-associated frontotemporal lobar degeneration. Acta Neuropathol 119: 111-122.
16. Eriksen JL, (2010) The enigmatic roles of microglial versus neuronal progranulin in neurological disease. Acta Neuropathol 119: 107-109.
17. Coppola G, Karydas A, Rademakers R, Wang Q, Baker M, et al. (2008) Gene expression study on peripheral blood identifies progranulin mutations. Ann Neurol 64: 92-96.
18. Al-Ayadhi LY, Mostafa GA, (2011) Low plasma progranulin levels in children with autism. J Neuroinflammation 8: 111.
19. Ahmed Z, Sheng H, Xu YF, Lin WL, Innes AE, et al. (2010) Accelerated lipofuscinosis and ubiquitination in granulin knockout mice suggest a role for progranulin in successful aging. Am J Pathol 177: 311-324.
20. Yin F, Banerjee R, Thomas B, Zhou P, Qian L, et al. (2010) Exaggerated inflammation, impaired host defense, and neuropathology in progranulin-deficient mice. J Exp Med 207: 117-128.
21. Yin F, Dumont M, Banerjee R, Ma Y, Li H, et al. (2010) Behavioral deficits and progressive neuropathology in progranulin-deficient mice: a mouse model of frontotemporal dementia. FASEB J 24: 4639-4647.
22. Park B, Buti L, Lee S, Matsuwaki T, Spooner E, et al. (2011) Granulin is a soluble cofactor for toll-like receptor 9 signaling. Immunity 34: 505-513.
23. Okura H, Yamashita S, Ohama T, Saga A, Yamamoto-Kakuta A, et al. (2010) HDL/apolipoprotein A-I binds to macrophage-derived progranulin and suppresses its conversion into proinflammatory granulins. J Atheroscler Thromb 17: 568-577.
24. Bateman A, Bennett HP, (2009) The granulin gene family: from cancer to dementia. Bioessays 31: 1245-1254.
25. Eriksen JL, Mackenzie IR, (2008) Progranulin: normal function and role in neurodegeneration. J Neurochem 104: 287-297.
26. Tang W, Lu Y, Tian QY, Zhang Y, Guo FJ, et al. (2011) The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science 332: 478-484.
27. Kao AW, Eisenhut RJ, Martens LH, Nakamura A, Huang A, et al. (2011) A neurodegenerative disease mutation that accelerates the clearance of apoptotic cells. Proc Natl Acad Sci U S A 108: 4441-4446.
28. Dasilva AG, Yong VW, (2008) Expression and regulation of matrix metalloproteinase-12 in experimental autoimmune encephalomyelitis and by bone marrow derived macrophages in vitro. J Neuroimmunol 199: 24-34.
29. Nar H, Werle K, Bauer MM, Dollinger H, Jung B, (2001) Crystal structure of human macrophage elastase (MMP-12) in complex with a hydroxamic acid inhibitor. J Mol Biol 312: 743-751.
30. Arikan MC, Shapiro SD, Mariani TJ, (2005) Induction of macrophage elastase (MMP-12) gene expression by statins. J Cell Physiol 204: 139-145.
31. Jin FY, Nathan C, Radzioch D, Ding A, (1997) Secretory leukocyte protease inhibitor: a macrophage product induced by and antagonistic to bacterial lipopolysaccharide. Cell 88: 417-426.
32. Ong CH, He Z, Kriazhev L, Shan X, Palfree RG, et al. (2006) Regulation of progranulin expression in myeloid cells. Am J Physiol Regul Integr Comp Physiol 291: R1602-R1612.
33. Bhandari V, Daniel R, Lim PS, Bateman A, (1996) Structural and functional analysis of a promoter of the human granulin/epithelin gene. Biochem J 319 (Pt 2): 441-447.
34. Frampton G, Invernizzi P, Bernuzzi F, Pae HY, Quinn M, et al. (2011) Interleukin-6-driven progranulin expression increases cholangiocarcinoma growth by an Akt-dependent mechanism. Gut.
35. Li X, Massa PE, Hanidu A, Peet GW, Aro P, et al. (2002) IKKalpha, IKKbeta, and NEMO/IKKgamma are each required for the NF-kappa B-mediated inflammatory response program. J Biol Chem 277: 45129-45140.
36. Butovsky O, Landa G, Kunis G, Ziv Y, Avidan H, et al. (2006) Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis. J Clin Invest 116: 905-915.
37. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D, (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci U S A 104: 1604-1609.
38. Mohan N, Edwards ET, Cupps TR, Oliverio PJ, Sandberg G, et al. (2001) Demyelination occurring during anti-tumor necrosis factor alpha therapy for inflammatory arthritides. Arthritis Rheum 44: 2862-2869.
39. Sicotte NL, Voskuhl RR, (2001) Onset of multiple sclerosis associated with anti-TNF therapy. Neurology 57: 1885-1888.
40. Breedveld FC, Weisman MH, Kavanaugh AF, Cohen SB, Pavelka K, et al. (2006) The PREMIER study: A multicenter, randomized, double-blind clinical trial of combination therapy with adalimumab plus methotrexate versus methotrexate alone or adalimumab alone in patients with early, aggressive rheumatoid arthritis who had not had previous methotrexate treatment. Arthritis Rheum 54: 26-37.
41. (1999) TNF neutralization in MS: results of a randomized, placebo-controlled multicenter study. The Lenercept Multiple Sclerosis Study Group and The University of British Columbia MS/MRI Analysis Group. Neurology 53: 457-465.
42. Neurath MF, Finotto S, (2011) IL-6 signaling in autoimmunity, chronic inflammation and inflammation-associated cancer. Cytokine Growth Factor Rev 22: 83-89.
43. Sui Y, Potula R, Dhillon N, Pinson D, Li S, et al. (2004) Neuronal apoptosis is mediated by CXCL10 overexpression in simian human immunodeficiency virus encephalitis. Am J Pathol 164: 1557-1566.
44. Butler GS, Dean RA, Tam EM, Overall CM, (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.
45. Xu D, Suenaga N, Edelmann MJ, Fridman R, Muschel RJ, et al. (2008) Novel MMP-9 substrates in cancer cells revealed by a label-free quantitative proteomics approach. Mol Cell Proteomics 7: 2215-2228.
46. Bai XH, Wang DW, Kong L, Zhang Y, Luan Y, et al. (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.
47. Gossas T, Danielson UH, (2006) Characterization of Ca2+ interactions with matrix metallopeptidase-12: implications for matrix metallopeptidase regulation. Biochem J 398: 393-398.
48. Brown EM, MacLeod RJ, (2001) Extracellular calcium sensing and extracellular calcium signaling. Physiol Rev 81: 239-297.
49. Ramadas RA, Wu L, LeVine AM, (2009) Surfactant protein A enhances production of secretory leukoprotease inhibitor and protects it from cleavage by matrix metalloproteinases. J Immunol 182: 1560-1567.
50. Song X, Zeng L, Jin W, Thompson J, Mizel DE, et al. (1999) Secretory leukocyte protease inhibitor suppresses the inflammation and joint damage of bacterial cell wall-induced arthritis. J Exp Med 190: 535-542.
51. Mueller AM, Pedre X, Stempfl T, Kleiter I, Couillard-Despres S, et al. (2008) Novel role for SLPI in MOG-induced EAE revealed by spinal cord expression analysis. J Neuroinflammation 5: 20.
52. Taggart CC, Cryan SA, Weldon S, Gibbons A, Greene CM, et al. (2005) Secretory leucoprotease inhibitor binds to NF-kappaB binding sites in monocytes and inhibits p65 binding. J Exp Med 202: 1659-1668.
53. Denis M, (1994) Human monocytes/macrophages: NO or no NO? J Leukoc Biol 55: 682-684.
54. McNeely TB, Dealy M, Dripps DJ, Orenstein JM, Eisenberg SP, et al. (1995) Secretory leukocyte protease inhibitor: a human saliva protein exhibiting anti-human immunodeficiency virus 1 activity in vitro. J Clin Invest 96: 456-464.
55. Lee SC, Liu W, Brosnan CF, Dickson DW, (1992) Characterization of human fetal dissociated CNS cultures with an emphasis on microglia. Lab Invest 67: 465-475.
56. Liu J, Zhao ML, Brosnan CF, Lee SC, (1996) Expression of type II nitric oxide synthase in primary human astrocytes and microglia: role of IL-1beta and IL-1 receptor antagonist. J Immunol 157: 3569-3576.
57. Suh HS, Zhao ML, Rivieccio M, Choi S, Connolly E, et al. (2007) Astrocyte indoleamine 2, 3 dioxygenase (IDO) is induced by the TLR3 ligand poly IC: mechanism of induction and role in anti-viral response. J Virol.
58. Krause D, Suh HS, Tarassishin L, Cui QL, Durafourt BA, et al. (2011) The tryptophan metabolite 3-hydroxyanthranilic acid plays anti-inflammatory and neuroprotective roles during inflammation: role of hemeoxygenase-1. Am J Pathol 179: 1360-1372.
59. Rivieccio MA, Suh HS, Zhao Y, Zhao ML, Chin KC, et al. (2006) TLR3 ligation activates an antiviral response in human fetal astrocytes: a role for viperin/cig5. J Immunol 177: 4735-4741.