Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis

Journal of Molecular Medicine

Volumn 81, Issue 10, 2003, Pages 600-612

  He, Zhiheng ^a   Bateman, Andrew ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b ROYAL VICTORIA HOSPITAL   (Canada)

Author keywords

Growth factor; Inflammation; Neovascularization; Tumorigenesis; Wound repair

Indexed keywords

CYCLIN B; CYCLIN D; CYTOKINE; ELASTASE; GROWTH FACTOR; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROGRANULIN; PROTEINASE INHIBITOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

BRAIN DEVELOPMENT; BREAST CARCINOMA; CARCINOGENESIS; CELL CYCLE; CELL DIFFERENTIATION; CELL MOTILITY; EPITHELIUM CELL; INFLAMMATION; KIDNEY CARCINOMA; OVARY CARCINOMA; PREIMPLANTATION EMBRYO; PROGNOSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; TISSUE REPAIR; TUMOR GROWTH; WOUND HEALING;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NEOPLASMS; SIGNAL TRANSDUCTION; WOUNDS AND INJURIES;

EID: 0242320195     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-003-0474-3     Document Type: Review

References (106)

1. Bateman A, Bennett HP (1998) Granulins: the structure and function of an emerging family of growth factors. J Endocrinol 158:145-151
2. Zanocco-Marani T, Bateman A, Romano G, Valentinis B, He ZH, Baserga R (1999) Biological activities and signaling pathways of the granulin/epithelin precursor. Cancer Res 59:5331-5340
3. Plowman GD, Green JM, Neubauer MG, Buckley SD, McDonald VL, Todaro GJ, Shoyab M (1992) The epithelin precursor encodes two proteins with opposing activities on epithelial cell growth. J Biol Chem 267:13073-13078
4. Zhou J, Gao G, Crabb JW, 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
5. Baba T, Hoff HB, 3rd, Nemoto H, Lee H, Orth J, Arai Y, Gerton GL (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
6. 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
7. Hrabal R, Chen Z, James S, Bennett HP, 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
8. Tolkatchev D, Ng A, Vranken W, Ni F (2000) Design and solution structure of a well-folded stack of two beta-hairpins based on the amino-terminal fragment of human granulin A. Biochemistry 39:2878-2886
9. Avrova AO, Stewart HE, De Jong WD, Heilbronn J, Lyon GD, Birch PR (1999) A cysteine protease gene is expressed early in resistant potato interactions with Phytophthora infestans. Mol Plant Microbe Interact 12:1114-1119
10. Bateman A, Belcourt D, Bennett H, Lazure C, Solomon S (1990) Granulins, a novel class of peptide from leukocytes. Biochem Biophys Res Commun 173:1161-1168
11. Sparro G, Galdenzi G, Eleuteri AM, Angeletti M, Schroeder W, Fioretti E (1997) Isolation and N-terminal sequence of multiple forms of granulins in human urine. Protein Expr Purif 10:169-174
12. Shoyab M, McDonald VL, Byles C, Todaro GJ, Plowman GD (1990) Epithelins 1 and 2: isolation and characterization of two cysteine-rich growth-modulating proteins. Proc Natl Acad Sci USA 87:7912-7916
13. Couto MA, Harwig SS, Cullor JS, Hughes JP, Lehrer RI (1992) Identification of eNAP-1, an antimicrobial peptide from equine neutrophils. Infect Immun 60:3065-3071
14. Belcourt DR, Lazure C, Bennett HP (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
15. Belcourt DR, Okawara Y, Fryer JN, Bennett HP (1995) Immunocytochemical localization of granulin-1 to mononuclear phagocytic cells of the teleost fish Cyprinus carpio and Carassius auratus. J Leukoc Biol 57:94-100
16. Uesaka T, Yano K, Yamasaki M, Ando M (1995) Somatostatin-, vasoactive intestinal peptide-, and granulin-like peptides isolated from intestinal extracts of goldfish, Carassius auratus. Gen Comp Endocrinol 99:298-306
17. Nakakura N, Hietter H, Van Dorsselaer A, Luu B (1992) Isolation and structural determination of three peptides from the insect Locusta migratoria. Identification of a deoxyhexose-linked peptide. Eur J Biochem 204:147-153
18. Deloffre L, Sautiere P, Cocquerelle C, Andries JC (1999) Identification of granulin-related peptides in a marine invertebrate, Hediste diversicolor. Bull Soc Zool France 124: 337-346
19. Hong SJ, and Kang KW (1999) Purification of granulin-like polypeptide from the blood-sucking leech, Hirudo nipponia. Protein Expr Purif 16:340-346
20. Zhu J, Nathan C, Jin W, Sim D, Ashcroft GS, Wahl SM, Lacomis L, Erdjument-Bromage H, Tempst P, Wright CD, Ding A (2002) Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 111:867-878
21. Parnell PG, Wunderlich J, Carter B, Halper J (1992) Transforming growth factor e: amino acid analysis and partial amino acid sequence. Growth Factors 7:65-72
22. Bhandari V, Bateman A (1992) Structure and chromosomal location of the human granulin gene. Biochem Biophys Res Commun 188:57-63
23. Bucan M, Gatalica B, Baba T, Gerton GL (1996) Mapping of Grn, the gene encoding the granulin/epithelin precursor (acrogranin), to mouse chromosome 11. Mamm Genome 7:704-705
24. 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
25. Daniel R, He Z, Carmichael KP, Halper J, Bateman A (2000) Cellular localization of gene expression for progranulin. J Histochem Cytochem 48:999-1009
26. He Z, Bateman A (1999) Progranulin gene expression regulates epithelial cell growth and promotes tumor growth in vivo. Cancer Res 59:3222-3229
27. He Z, Ong CH, Halper J, Bateman A (2003) Progranulin is a mediator of the wound response. Nat Med 9:225-229
28. Xu SQ, Sell C, DuBois GC, Baserga R (1997) A novel growth stimulating activity from BRL-3A cell conditioned medium. Cell Prolif 30:295-307
29. Xu SQ, Tang D, Chamberlain S, Pronk G, Masiarz FR, Kaur S, Prisco M, Zanocco-Marani T, Baserga R (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
30. 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
31. Sell C, Dumenil G, Deveaud C, Miura M, Coppola D, DeAngelis T, Rubin R, Efstratiadis A, Baserga R (1994) Effect of a null mutation of the insulin-like growth factor I receptor gene on growth and transformation of mouse embryo fibroblasts. Mol Cell Biol 14:3604-3612
32. Anakwe OO, Gerton GL (1990) Acrosome biogenesis begins during meiosis: evidence from the synthesis and distribution of an acrosomal glycoprotein, acrogranin, during guinea pig spermatogenesis. Biol Reprod 42:317-328
33. Diaz-Cueto L, Stein P, Jacobs A, Schultz RM, Gerton GL (2000) Modulation of mouse preimplantation embryo development by acrogranin (epithelin/granulin precursor). Dev Biol 217:406-418
34. Suzuki M, Matsumuro M, Hirabayashi K, Ogawara M, Nishiahara M, Takahashi M (2000) Oocyte-specific expression of granulin precursor (acrogranin) in rat ovary. J Reprod Dev 46:271
35. Daniel R, Daniels E, He Z, Bateman A (2003) Progranulin (Acrogranin/PC cell-derived growth factor/epithelin precursor) is expressed in the placenta, epidermis, microvasculature and brain during murine development. Dev Dyn 227:593-599
36. Suzuki M, Nishiahara M (2002) Granulin precursor gene: a sex steroid-inducible gene involved in sexual differentiation of the rat brain. Mol Genet Metab 75:31-37
37. Arnold AP, Gorski RA (1984) Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci 7:413-442
38. Suzuki M, Yoshida S, Nishihara M, Takahashi M (1998) Identification of a sex steroid-inducible gene in the neonatal rat hypothalamus. Neurosci Lett 242:127-130
39. Suzuki M, Yonezawa T, Fujioka H, Matuamuro M, Nishihara M (2001) Induction of granulin precursor gene expression by estrogen treatment in neonatal rat hypothalamus. Neurosci Lett 297:199-202
40. Frankfurt M (1994) Gonadal steroids and neuronal plasticity. Studies in the adult rat hypothalamus. Ann N Y Acad Sci 743:45-59
41. Suzuki M, Bannai M, Matsumuro M, Furuhata Y, Ikemura R, Kuranaga E, Kaneda Y, Nishihara M, Takahashi M (2000) Suppression of copulatory behavior by intracerebroventricular infusion of antisense oligodeoxynucleotide of granulin in neonatal male rats. Physiol Behav 68:707-713
42. Wertz K, Herrmann BG (2000) Large-scale screen for genes involved in gonad development. Mech Dev 98:51-70
43. Martin P (1997) Wound healing-aiming for perfect skin regeneration. Science 276:75-81
44. Singer AJ, Clark RA (1999) Cutaneous wound healing. N Engl J Med 341:738-746
45. Kasama T, Kobayashi K, Yajima N, Shiozawa F, Yoda Y, Takeuchi HT, Mori Y, Negishi M, Ide H, Adachi M (2000) Expression of vascular endothelial growth factor by synovial fluid neutrophils in rheumatoid arthritis (RA). Clin Exp Immunol 121:533-538
46. McCourt M, Wang JH, Sookhai S, Redmond HP (2001) Activated human neutrophils release hepatocyte growth factor/scatter factor. Eur J Surg Oncol 27:396-403
47. Grotendorst GR, Smale G, Pencev D (1989) Production of transforming growth factor beta by human peripheral blood monocytes and neutrophils. J Cell Physiol 140:396-402
48. Sunderkotter C, Steinbrink K, Goebeler M, Bhardwaj R, Sorg C (1994) Macrophages and angiogenesis. J Leukoc Biol 55: 410-422
49. Werner S, Peters KG, Longaker MT, Fuller-Pace F, Banda MJ, Williams LT (1992) Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc Natl Acad Sci USA 89:6896-6900
50. Ihn H (2002) Pathogenesis of fibrosis: role of TGF-beta and CTGF. Curr Opin Rheumatol 14:681-685
51. Nicosia RF, Ottinetti A (1990) Modulation of microvascular growth and morphogenesis by reconstituted basement membrane gel in three-dimensional cultures of rat aorta: a comparative study of angiogenesis in matrigel, collagen, fibrin, and plasma clot. In Vitro Cell Dev Biol 26:119-128
52. Bussolati B, Dunk C, Grohman M, Kontos CD, Mason J, Ahmed A (2001) Vascular endothelial growth factor receptor-1 modulates vascular endothelial growth factor-mediated angiogenesis via nitric oxide. Am J Pathol 159:993-1008
53. Kitajima I, Unoki K, Maruyama I (1999) Phosphorothioate oligodeoxynucleotides inhibit basic fibroblast growth factor-induced angiogenesis in vitro and in vivo. Antisense Nucleic Acid Drug Dev 9:233-239
54. Jones MB, Michener CM, Blanchette JO, Kuznetsov VA, Raffeld M, Serrero G, Emmert-Buck MR, Petricoin EF, Krizman DB, Liotta LA, Kohn EC (2003) The granulin-epithelin precursor/PC-cell-derived growth factor is a growth factor for epithelial ovarian cancer. Clin Cancer Res 9:44-51
55. Garcia-Cardena G, Comander J, Anderson KR, Blackman BR, Gimbrone MA Jr (2001) Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc Natl Acad Sci USA 98:4478-4485
56. Passerini AG, Milsted A, Rittgers SE (2003) Shear stress magnitude and directionality modulate growth factor gene expression in preconditioned vascular endothelial cells. J Vasc Surg 37:182-190
57. 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
58. Bhandari V, Daniel R, Lim PS, Bateman A (1996) Structural and functional analysis of a promoter of the human granulin/epithelin gene. Biochem J 319:441-447
59. Baba T, Nemoto H, Watanabe K, Arai Y, Gerton GL (1993) Exon/intron organization of the gene encoding the mouse epithelin/granulin precursor (acrogranin). FEBS Lett 322:89-94
60. Subrahmanyam YV, Yamaga S, Prashar Y, Lee HH, Hoe NP, Kluger Y, Gerstein M, Goguen JD, Newburger PE, Weissman SM (2001) RNA expression patterns change dramatically in human neutrophils exposed to bacteria. Blood 97:2457-2468
61. Justen HP, Grunewald E, Totzke G, Gouni-Berthold I, Sachinidis A, Wessinghage D, Vetter H, Schulze-Osthoff K, Ko Y (2000) Differential gene expression in synovium of rheumatoid arthritis and osteoarthritis. Mol Cell Biol Res Commun 3:165-172
62. Choy EH, Panayi GS (2001) Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med 344:907-916
63. Matzilevich DA, Rall JM, Moore AN, Grill RJ, Dash PK (2002) High-density microarray analysis of hippocampal gene expression following experimental brain injury. J Neurosci Res 67:646-663
64. Johnston C, Jiang W, Chu T, Levine B (2001) Identification of genes involved in the host response to neurovirulent alphavirus infection. J Virol 75:10431-10445
65. Baker CA, Manuelidis L (2003) Unique inflammatory RNA profiles of microglia in Creutzfeldt-Jakob disease. Proc Natl Acad Sci USA 100:675-679
66. Ohmi K, Greenberg DS, Rajavel KS, Ryazantsev S, Li HH, Neufeld EF (2003) Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc Natl Acad Sci USA 100:1902-1907
67. 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
68. Hall ED, Oostveen JA, Gurney ME (1998) Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23:249-256
69. Cross M, Dexter TM (1991) Growth factors in development, transformation, and tumorigenesis. Cell 64:271-280
70. Aaronson SA (1991) Growth factors and cancer. Science 254:1146-1153
71. 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
72. 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
73. Leerkes MR, Caballero OL, Mackay A, Torloni H, O'Hare MJ, Simpson AJ, de Souza SJ (2002) In silico comparison of the transcriptome derived from purified normal breast cells and breast tumor cell lines reveals candidate upregulated genes in breast tumor cells. Genomics 79:257-265
74. Egland KA, Vincent JJ, Strausberg R, Lee B, Pastan I (2003) Discovery of the breast cancer gene BASE using a molecular approach to enrich for genes encoding membrane and secreted proteins. Proc Natl Acad Sci USA 100:1099-1104
75. Donald CD, Laddu A, Chandham P, Lim SD, Cohen C, Amin M, Gerton GL, Marshall FF, Petros JA (2001) Expression of progranulin and the epithelin/granulin precursor acrogranin correlates with neoplastic state in renal epithelium. Anticancer Res 21:3739-3742
76. Ali SM, Nambi P, Fredrickson TA, Brooks DP (1999) Epithelin mRNA expression in polycystic kidney disease. Peptides 20:1489-1495
77. Line A, Stengrevics A, Slucka Z, Li G, Jankevics E, Rees RC (2002) Serological identification and expression analysis of gastric cancer-associated genes. Br J Cancer 86:1824-1830
78. Liau LM, Lallone RL, Seitz RS, Buznikov A, Gregg JP, Kornblum HI, Nelson SF, Bronstein JM (2000) Identification of a human glioma-associated growth factor gene, granulin, using differential immuno-absorption. Cancer Res 60:1353-1360
79. Markert JM, Fuller CM, Gillespie GY, Bubien JK, McLean LA, Hong RL, Lee K, Gullans SR, Mapstone TB, Benos DJ (2001) Differential gene expression profiling in human brain tumors. Physiol Genomics 5:21-33
80. Virtaneva K, Wright FA, Tanner SM, Yuan B, Lemon WJ, Caligiuri MA, Bloomfield CD, de La Chapelle A, Krahe R (2001) Expression profiling reveals fundamental biological differences in acute myeloid leukemia with isolated trisomy 8 and normal cytogenetics. Proc Natl Acad Sci USA 98:1124-1129
81. Chow ML, Moler EJ, Mian IS (2001) Identifying marker genes in transcription profiling data using a mixture of feature relevance experts. Physiol Genomics 5:99-111
82. Wang W, Hayashi J, Kim WE, Serrera G (2003) PC cell-derived growth factor (granulin precursor) expression and action in human multiple myeloma. Clin Cancer Res 9:2221-2228
83. Halper J, Moses HL (1983) Epithelial tissue-derived growth factor-like polypeptides. Cancer Res 43:1972-1979
84. Halper J, Moses HL (1987) Purification and characterization of a novel transforming growth factor. Cancer Res 47:4552-4559
85. He Z, Ismail A, Kriazhev L, Sadvakassova G, Bateman A (2002) Progranulin (PC-cell-derived growth factor/acrogranin) regulates invasion and cell survival. Cancer Res 62:5590-5596
86. Grossmann J (2002) Molecular mechanisms of "detachmentinduced apoptosis-Anoikis." Apoptosis 7:247-260
87. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57-70
88. Kudoh K, Ramanna M, Ravatn R, Elkahloun AG, Bittner ML, Meltzer PS, Trent JM, Dalton WS, Chin KV (2000) Monitoring the expression profiles of doxorubicin-induced and doxorubicin-resistant cancer cells by cDNA microarray. Cancer Res 60:4161-4166
89. Xia X, Serrero G (1998) Identification of cell surface binding sites for PC-cell-derived growth factor, PCDGF (epithelin/granulin precursor) on epithelial cells and fibroblasts. Biochem Biophys Res Commun 245:539-543
90. Culouscou JM, Carlton GW, Shoyab M (1993) Biochemical analysis of the epithelin receptor. J Biol Chem 268:10458-10462
91. Parnell PG, Carter BJ, Halper J (1995) Identification of a membrane-associated receptor for transforming growth factor type E. J Recept Signal Transduct Res 15:747-756
92. Baladron V, Ruiz-Hidalgo MJ, Bonvini E, Gubina E, Notario V, Laborda J (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
93. Laborda J (2000) The role of the epidermal growth factor-like protein dlk in cell differentiation. Histol Histopathol 15:119-129
94. Stiles CD, Capone GT, Scher CD, Antoniades HN, Van Wyk JJ, Pledger WJ (1979) Dual control of cell growth by somatomedins and platelet-derived growth factor. Proc Natl Acad Sci USA 76:1279-1283
95. Scher CD, Shepard RC, Antoniades HN, Stiles CD (1979) Platelet-derived growth factor and the regulation of the mammalian fibroblast cell cycle. Biochim Biophys Acta 560:217-241
96. Cristofalo VJ, Phillips PD, Sorger T, Gerhard G (1989) Alterations in the responsiveness of senescent cells to growth factors. J Gerontol 44:55-62
97. King RW, Jackson PK, Kirschner MW (1994) Mitosis in transition. Cell 79:563-571
98. Marshall CJ (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185
99. Weber JD, Raben DM, Phillips PJ, Baldassare JJ (1997) Sustained activation of extracellular-signal-regulated kinase 1 (ERK1) is required for the continued expression of cyclin D1 in G1 phase. Biochem J 326:61-68
100. Khokhlatchev AV, Canagarajah B, Wilsbacher J, Robinson M, Atkinson M, Goldsmith E, Cobb MH (1998) Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell 93:605-615
101. Balmanno K, Cook SJ (1999) Sustained MAP kinase activation is required for the expression of cyclin D1, p21Cip1 and a subset of AP-1 proteins in CCL39 cells. Oncogene 18: 3085-3097
102. Cary LA, Guan JL (1999) Focal adhesion kinase in integrin-mediated signaling. Front Biosci 4:D102-D113
103. Hauck CR, Hsia DA, Schlaepfer DD (2002) The focal adhesion kinase-a regulator of cell migration and invasion. IUBMB Life 53:115-119
104. Abbi S, Guan JL (2002) Focal adhesion kinase: protein interactions and cellular functions. Histol Histopathol 17:1163-1171
105. Trinh DP, Brown KM, Jeang KT (1999) Epithelin/granulin growth factors: extracellular cofactors for HIV-1 and HIV-2 Tat proteins. Biochem Biophys Res Commun 256:299-306
106. Hoque M, Young TM, Lee CG, Serrero G, Mathews MB, Pe'ery T (2003) The growth factor granulin interacts with cyclin T1 and modulates P-TEFb-dependent transcription. Mol Cell Biol 23:1688-1702