The granulin gene family: From cancer to dementia

BioEssays

Volumn 31, Issue 11, 2009, Pages 1245-1254

  Bateman, Andrew ^a   Bennett, Hugh P J ^a  

^a ROYAL VICTORIA HOSPITAL   (Canada)

Author keywords

Carcinogenesis; Evolution; Frontotemporal lobar dementia; Inflammation; Wounds

Indexed keywords

EPIDERMAL GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR; PROGRANULIN; SOMATOMEDIN;

CARCINOGENESIS; EMBRYO DEVELOPMENT; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; HUMAN; KNOCKOUT GENE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; TISSUE REGENERATION;

ANIMALS; DEMENTIA; FRONTAL LOBE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INFLAMMATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MULTIGENE FAMILY; NEOPLASMS; NEURODEGENERATIVE DISEASES; WOUND HEALING;

ANIMALIA; MUS;

EID: 70549109118     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.200900086     Document Type: Review

References (99)

1. Bateman A, Belcourt D, Bennett H, et al. 1990. Granulins, a novel class of peptide from leukocytes. Biochem Biophys Res Commun 173: 1161-1168.
2. Belcourt DR, Lazure C, Bennett HPJ. 1993. Isolation and primary structure of the three major forms of granulin-like peptides from hematopoietic tissues of a teleost fish (Cyprinus carpio). J Biol Chem 268: 9230-9237. (Pubitemid 23145965)
3. Hrabal R, Chen Z, James S, et al. 1996. The hairpin stack fold, a novel protein architecture for a new family of protein growth factors. Nat Struct Biol 3: 747-752. (Pubitemid 26303399)
4. Tolkatchev D, Malik S, Vinogradova A, et al. 2008. Structure dissection of human progranulin identifies well-folded granulin/epithelin modules with unique functional activities. Protein Sci 17: 711-724.
5. Bateman A, Bennett HPJ. 1998. Granulins: the structure and function of an emerging family of growth factors. J Endocrinol 158: 145-151. (Pubitemid 28342057)
6. Baker M, Mackenzie IR, Pickering-Brown SM, et al. 2006. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442: 916-919. (Pubitemid 44285946)
7. Cruts M, Gijselinck I, van der Zee J, et al. 2006. Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442: 920-924. (Pubitemid 44285947)
8. He Z, Bateman A. 1999. Progranulin gene expression regulates epithelial cell growth and promotes tumor growth in vivo. Cancer Res 59: 3222-3229. (Pubitemid 29316026)
9. He Z, Ismail A, Kriazhev L, et al. 2002. Progranulin (PC-cell-derived growth factor/acrogranin) regulates invasion and cell survival. Cancer Res 62: 5590-5596.
10. Zhou J, Gao G, Crabb JW, et al. 1993. Purification of an autocrine growth factor homologous with mouse epithelin precursor from a highly tumorigenic cell line. J Biol Chem 268: 10863-10869. (Pubitemid 23162265)
11. Serrero G, Ioffe OB. 2003. Expression of PC-cell-derived growth factor in benign and malignant human breast epithelium. Hum Pathol 34: 1148-1154. (Pubitemid 37467000)
12. Matsumura N, Mandai M, Miyanishi M, et al. 2006. Oncogenic property of acrogranin in human uterine leiomyosarcoma: direct evidence of genetic contribution in in vivo tumorigenesis. Clin Cancer Res 12: 1402-1411.
13. Wang W, Hayashi J, Kim WE, et al. 2003. PC cell-derived growth factor (granulin precursor) expression and action in human multiple myeloma. Clin Cancer Res 9: 2221-2228. (Pubitemid 36687646)
14. Zhang H, Serrero G. 1998. Inhibition of tumorigenicity of the teratoma PC cell line by transfection with antisense cDNA for PC cell-derived growth factor (PCDGF, epithelin/granulin precursor). Proc Natl Acad Sci USA 95: 14202-14207. (Pubitemid 28549345)
15. Lu R, Serrero G. 2001. Mediation of estrogen mitogenic effect in human breast cancer MCF-7 cells by PC-cell-derived growth factor (PCDGF/ granulin precursor). Proc Natl Acad Sci USA 98: 142-147. (Pubitemid 32095877)
16. Zanocco-Marani T, Bateman A, Romano G, et al. 1999. Biological activities and signaling pathways of the granulin/epithelin precursor. Cancer Res 59: 5331-5340. (Pubitemid 29504002)
17. Lu R, Serrero G. 2000. Inhibition of PC cell-derived growth factor (PCDGF, epithelin/granulin precursor) expression by antisense PCDGF cDNA transfection inhibits tumorigenicity of the human breast carcinoma cell line MDA-MB-468. Proc Natl Acad Sci USA 97: 3993-3998. (Pubitemid 30226075)
18. Chen XY, Li JS, Liang QP, et al. 2008. Expression of PC cell-derived growth factor and vascular endothelial growth factor in esophageal squamous cell carcinoma and their clinicopathologic significance. Chin Med J (Engl) 121: 881-886.
19. Tangkeangsirisin W, Serrero G. 2004. PC cell-derived growth factor (PCDGF/GP88, progranulin) stimulates migration, invasiveness and VEGF expression in breast cancer cells. Carcinogenesis 25: 1587-1592. (Pubitemid 39214300)
20. Miyanishi M, Mandai M, Matsumura N, et al. 2007. Immortalized ovarian surface epithelial cells acquire tumorigenicity by acrogranin gene overexpression. Oncol Rep 17: 329-333.
21. Kamrava M, Simpkins F, Alejandro E, et al. 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. (Pubitemid 41573637)
22. Davidson B, Alejandro E, Florenes VA, et al. 2004. Granulin-epithelin precursor is a novel prognostic marker in epithelial ovarian carcinoma. Cancer 100: 2139-2147. (Pubitemid 38580332)
23. Jones MB, Michener CM, Blanchette JO, et al. 2003. The granulinepithelin precursor/PC-cell-derived growth factor is a growth factor for epithelial ovarian cancer. Clin Cancer Res 9: 44-51. (Pubitemid 36109714)
24. Monami G, Gonzalez EM, Hellman M, et al. 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. (Pubitemid 44197687)
25. Ho JC, Ip YC, Cheung ST, et al. 2008. Granulin-epithelin precursor as a therapeutic target for hepatocellular carcinoma. Hepatology 47: 1524-1532. (Pubitemid 351702736)
26. Liau LM, Lallone RL, Seitz RS, et al. 2000. Identification of a human glioma-associated growth factor gene, granulin, using differential immuno-absorption. Cancer Res 60: 1353-1360.
27. Diaz-Cueto L, Stein P, Jacobs A, et al. 2000. Modulation of mouse preimplantation embryo development by acrogranin (epithelin/granulin precursor). Dev Biol 217: 406-418. (Pubitemid 30060887)
28. He Z, Ong CH, Halper J, et al. 2003. Progranulin is a mediator of the wound response. Nat Med 9: 225-229.
29. Zhu J, Nathan C, Jin W, et al. 2002. Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 111: 867-878. (Pubitemid 36106407)
30. Kessenbrock K, Frohlich L, Sixt M, et al. 2008. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiin- flammatory progranulin. J Clin Invest 118: 2438-2447. (Pubitemid 351949772)
31. Chen HJ, Huang DJ, Hou WC, et al. 2006. Molecular cloning and characterization of a granulin-containing cysteine protease SPCP3 from sweet potato (Ipomoea batatas) senescent leaves. J Plant Physiol 163: 863-876.
32. Eichinger L, Pachebat JA, Glockner G, et al. 2005. The genome of the social amoeba Dictyostelium discoideum. Nature 435: 43-57. (Pubitemid 40655903)
33. Cadieux B, Chitramuthu BP, Baranowski D, et al. 2005. The zebrafish progranulin gene family and antisense transcripts. BMC Genomics 6: 156. (Pubitemid 41662739)
34. Nichols SA, DirksW, Pearse JS, et al. 2006. Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 103: 12451-12456.
35. King N, Westbrook MJ, Young SL, et al. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451: 783-788. (Pubitemid 351253174)
36. Shoyab M, McDonald VL, Byles C, et al. 1990. Plowman GD. Epithelins 1 and 2: isolation and characterization of two cysteine-rich growth-modulating proteins. Proc Natl Acad Sci USA 87: 7912-7916.
37. Bhandari V, Palfree RG, Bateman A. 1992. Isolation and sequence of the granulin precursor cDNA from human bone marrow reveals tandem cysteine-rich granulin domains. Proc Natl Acad Sci USA 89: 1715-1719.
38. Plowman GD, Green JM, Neubauer MG, et al. 1992. The epithelin precursor encodes two proteins with opposing activities on epithelial cell growth. J Biol Chem 267: 13073-13078.
39. Baba T, Hoff HB, III, Nemoto H, et al. 1993. Acrogranin, an acrosomal cysteine-rich glycoprotein, is the precursor of the growth-modulating peptides, granulins, and epithelins, and is expressed in somatic as well as male germ cells. Mol Reprod Dev 34: 233-243. (Pubitemid 23082890)
40. Xu SQ, Tang D, Chamberlain S, et al. 1998. The granulin/epithelin precursor abrogates the requirement for the insulin-like growth factor 1 receptor for growth in vitro. J Biol Chem 273: 20078-20083. (Pubitemid 28377561)
41. Parnell PG, Wunderlich J, Carter B, et al. 1992. Transforming growth factor e: amino acid analysis and partial amino acid sequence. Growth Factors 7: 65-72.
42. Daniel R, He Z, Carmichael KP, et al. 2000. Cellular localization of gene expression for progranulin. J Histochem Cytochem 48: 999-1009. (Pubitemid 30421564)
43. Bhandari V, Giaid A, Bateman A. 1993. The complementary deoxyribonucleic acid sequence, tissue distribution, and cellular localization of the rat granulin precursor. Endocrinology 133: 2682-2689. (Pubitemid 24000720)
44. Donald CD, Laddu A, Chandham P, et al. 2001. Expression of progranulin and the epithelin/granulin precursor acrogranin correlates with neoplastic state in renal epithelium. Anticancer Res 21: 3739-3742. (Pubitemid 34229235)
45. Pan CX, Kinch MS, Kiener PA, et al. 2004. PC cell-derived growth factor expression in prostatic intraepithelial neoplasia and prostatic adenocarcinoma. Clin Cancer Res 10: 1333-1337. (Pubitemid 38365225)
46. Cheung ST, Wong SY, Leung KL, et al. 2004. Granulin-epithelin precursor overexpression promotes growth and invasion of hepatocellular carcinoma. Clin Cancer Res 10: 7629-7636. (Pubitemid 39557526)
47. Jones MB, Houwink AP, Freeman BK, et al. 2006. The granulin-epithelin precursor is a steroid-regulated growth factor in endometrial cancer. J Soc Gynecol Investig 13: 304-311. (Pubitemid 43668398)
48. Qin J, Diaz-Cueto L, Schwarze JE, et al. 2005. Effects of progranulin on blastocyst hatching and subsequent adhesion and outgrowth in the mouse. Biol Reprod 73: 434-442. (Pubitemid 41170198)
49. Diaz-Cueto L, Gerton GL. 2001. The influence of growth factors on the development of preimplantation mammalian embryos. Arch Med Res 32: 619-626. (Pubitemid 34031755)
50. Desmarais JA, Cao M, Bateman A, et al. 2008. Spatiotemporal expression pattern of progranulin in embryo implantation and placenta formation suggests a role in cell proliferation, remodeling, and angiogenesis. Reproduction 136: 247-257.
51. Daniel R, Daniels E, He Z, et al. 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. (Pubitemid 36951084)
52. Josephs KA. 2007. Frontotemporal lobar degeneration. Neurol Clin 25: 683-696, vi.
53. Wittenberg D, Possin KL, Rascovsky K, et al. 2008. The early neuropsychological and behavioral characteristics of frontotemporal dementia. Neuropsychol Rev 18: 91-102.
54. Snowden JS, Pickering-Brown SM, Mackenzie IR, et al. 2006. Progranulin gene mutations associated with frontotemporal dementia and progressive non-fluent aphasia. Brain 129: 3091-3102.
55. Rizzu P, Van Swieten JC, Joosse M, et al. 1999. High prevalence of mutations in the microtubule-associated protein tau in a population study of frontotemporal dementia in the Netherlands. Am J Hum Genet 64: 414-421. (Pubitemid 129500524)
56. Skibinski G, Parkinson NJ, Brown JM, et al. 2005. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat Genet 37: 806-808. (Pubitemid 41077105)
57. Forman MS, Mackenzie IR, Cairns NJ, et al. 2006. Novel ubiquitin neuropathology in frontotemporal dementia with valosin-containing protein gene mutations. J Neuropathol Exp Neurol 65: 571-581.
58. Gijselinck I, Van Broeckhoven C, Cruts M. 2008. Granulin mutations associated with frontotemporal lobar degeneration and related disorders: an update. Hum Mutat 29: 1373-1386. (Pubitemid 352774891)
59. Gass J, Cannon A, Mackenzie IR, et al. 2006. Mutations in progranulin are a major cause of ubiquitin-positive frontotemporal lobar degeneration. Hum Mol Genet 15: 2988-3001. (Pubitemid 44530703)
60. van der Zee J, Le Ber I, Maurer-Stroh S, et al. 2007. Mutations other than null mutations producing a pathogenic loss of progranulin in frontotemporal dementia. Hum Mutat 28: 416.
61. Shankaran SS, Capell A, Hruscha AT, et al. 2008. Missense mutations in the progranulin gene linked to frontotemporal lobar degeneration with ubiquitin-immunoreactive inclusions reduce progranulin production and secretion. J Biol Chem 283: 1744-1753.
62. Gijselinck I, van der Zee J, Engelborghs S, et al. 2008. Progranulin locus deletion in frontotemporal dementia. Hum Mutat 29: 53-58.
63. Arai T, Hasegawa M, Akiyama H, et al. 2006. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 351: 602-611. (Pubitemid 44708852)
64. Neumann M, Sampathu DM, Kwong LK, et al. 2006. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314: 130-133. (Pubitemid 44547757)
65. Dermaut B, Kumar-Singh S, Rademakers R, et al. 2005. Tau is central in the genetic Alzheimer-frontotemporal dementia spectrum. Trends Genet 21: 664-672. (Pubitemid 41608689)
66. Schymick JC, Yang Y, Andersen PM, et al. 2007. Progranulin mutations and amyotrophic lateral sclerosis or amyotrophic lateral sclerosis-fronto-temporal dementia phenotypes. J Neurol Neurosurg Psychiatry 78: 754-756. (Pubitemid 46998853)
67. Mackenzie IR. 2007. The neuropathology and clinical phenotype of FTD with progranulin mutations. Acta Neuropathol 114: 49-54.
68. Zhang YJ, Xu YF, Dickey CA, et al. 2007. Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43. J Neurosci 27: 10530-10534.
69. Igaz LM, Kwong LK, Chen-Plotkin A, et al. 2009. Expression of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. J Biol Chem 284: 8516-8524.
70. Zhang YJ, Xu YF, Cook C, et al. 2009. Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity. Proc Natl Acad Sci USA 106: 7607-7612.
71. Strong MJ, Volkening K, Hammond R, et al. 2007. TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol Cell Neurosci 35: 320-327. (Pubitemid 46843567)
72. Moisse K, Volkening K, Leystra-Lantz C, et al. 2009. Divergent patterns of cytosolic TDP-43 and neuronal progranulin expression following axotomy: implications for TDP-43 in the physiological response to neuronal injury. Brain Res 1249: 202-211.
73. Van Damme P, Van Hoecke A, Lambrechts D, et al. 2008. Progranulin functions as a neurotrophic factor to regulate neurite outgrowth and enhance neuronal survival. J Cell Biol 181: 37-41.
74. Guerra RR, Kriazhev L, Hernandez-Blazquez FJ, et al. 2007. Progranulin is a stress-response factor in fibroblasts subjected to hypoxia and acidosis. Growth Factors 25: 280-285.
75. Ahmed Z, Mackenzie IR, Hutton ML, et al. 2007. Progranulin in frontotemporal lobar degeneration and neuroinflammation. J Neuroinflammation 4: 7. (Pubitemid 46351578)
76. Sleegers K, Brouwers N, Maurer-Stroh S, et al. 2008. Progranulin genetic variability contributes to amyotrophic lateral sclerosis. Neurology 71: 253-259.
77. Suzuki M, Yoshida S, Nishihara M, et al. 1998. Identification of a sex steroid-inducible gene in the neonatal rat hypothalamus. Neurosci Lett 242: 127-130. (Pubitemid 28275512)
78. Suzuki M, Bannai M, Matsumuro M, et al. 2000. Suppression of copulatory behavior by intracerebroventricular infusion of antisense oligodeoxynucleotide of granulin in neonatal male rats. Physiol Behav 68: 707-713. (Pubitemid 30182471)
79. Kayasuga Y, Chiba S, Suzuki M, et al. 2007. Alteration of behavioural phenotype in mice by targeted disruption of the progranulin gene. Behav Brain Res 185: 110-118. (Pubitemid 47633696)
80. Deloffre L, Sautiere P-E, Sautiere P, et al. 1999. Identification of a granulin-related peptide in a marine invertebrate, Hediste diversicolor. J Ann Soc Zoologique (France) 124: 337-346. (Pubitemid 129513974)
81. Schlaepfer DD, Hauck CR, Sieg DJ. 1999. Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71: 435-478.
82. Sieg DJ, Hauck CR, Ilic D, et al. 2000. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2: 249-256. (Pubitemid 30781108)
83. Stiles CD, Capone GT, Scher CD, et al. 1979. Dual control of cell growth by somatomedins and platelet-derived growth factor. Proc Natl Acad Sci USA 76: 1279-1283. (Pubitemid 9143723)
84. Swantek JL. Baserga R. 1999. Prolonged activation of ERK2 by epidermal growth factor and other growth factors requires a functional insulin-like growth factor 1 receptor. Endocrinology 140: 3163-3169. (Pubitemid 30650632)
85. Hahn WC, Counter CM, Lundberg AS, et al. 1999. Creation of human tumour cells with defined genetic elements. Nature 400: 464-468.
86. Tangkeangsirisin W, Hayashi J, Serrero G. 2004. PC cell-derived growth factor mediates tamoxifen resistance and promotes tumor growth of human breast cancer cells. Cancer Res 64: 1737-1743. (Pubitemid 38428696)
87. Kim WE. Serrero G. 2006. PC cell-derived growth factor stimulates proliferation and confers Trastuzumab resistance to Her-2-overexpressing breast cancer cells. Clin Cancer Res 12: 4192-4199.
88. Pizarro GO, Zhou XC, Koch A, et al. 2007. Prosurvival function of the granulin-epithelin precursor is important in tumor progression and chemoresponse. Int J Cancer 120: 2339-2343. (Pubitemid 46642119)
89. Simpkins FA, Devoogdt NM, Rasool N, et al. 2008. The alarm anti-protease, secretory leukocyte protease inhibitor, is a proliferation and survival factor for ovarian cancer cells. Carcinogenesis 29: 466-472.
90. Devoogdt N, Rasool N, Hoskins E, et al. 2009. Overexpression of protease inhibitor-dead secretory leukocyte protease inhibitor causes more aggressive ovarian cancer in vitro and in vivo. Cancer Sci 100: 434-440.
91. Butler GS, Dean RA, Tam EM, et al. 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.
92. Bai XH, Wang DW, Kong L, et al. 2009. ADAMTS-7, a direct target of PTHrP, adversely regulates endochondral bone growth via associating with and inactivating GEP growth factor. Mol Cell Biol 29: 4201-4219.
93. Liu CJ. 2009. The role of ADAMTS-7 and ADAMTS-12 in the pathogenesis of arthritis. Nat Clin Pract Rheumatol 5: 38-45.
94. Gonzalez EM, Mongiat M, Slater SJ, et al. 2003. A novel interaction between perlecan protein core and progranulin: potential effects on tumor growth. J Biol Chem 278: 38113-38116. (Pubitemid 37221697)
95. Xu K, Zhang Y, Ilalov K, et al. 2007. Cartilage oligomeric matrix protein associates with granulin-epithelin precursor (GEP) and potentiates GEPstimulated chondrocyte proliferation. J Biol Chem 282: 11347-11355. (Pubitemid 47100806)
96. Baladron V, Ruiz-Hidalgo MJ, Bonvini E, et al. 2002. The EGF-like homeotic protein dlk affects cell growth and interacts with growth-modulating molecules in the yeast two-hybrid system. Biochem Biophys Res Commun 291: 193-204. (Pubitemid 34694389)
97. Hoque M, Young TM, Lee CG, et al. 2003. The growth factor granulin interacts with cyclin T1 and modulates P-TEFb-dependent transcription. Mol Cell Biol 23: 1688-1702. (Pubitemid 36246050)
98. Kato M, Hasunuma N, Nakayama R, et al. 2009. Progranulin, a secreted tumorigenesis and dementia-related factor, regulates mouse hair growth. J Dermatol Sci 53: 234-236.
99. Leverenz JB, Yu CE, Montine TJ, et al. 2007. A novel progranulin mutation associated with variable clinical presentation and tau, TDP43 and alpha-synuclein pathology. Brain 130: 1360-1374.