Serglycin: At the crossroad of inflammation and malignancy

Frontiers in Oncology

Volumn 4 JAN, Issue , 2014, Pages

  Korpetinou, Angeliki ^a   Skandalis, Spyros S ^a   Labropoulou, Vassiliki T ^b   Smirlaki, Gianna ^a   Noulas, Argyrios ^c   Karamanos, Nikos K ^a   Theocharis, Achilleas D ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b UNIVERSITY HOSPITAL OF PATRAS   (Greece)

^c Technological Educational Institute   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CHEMOKINE RECEPTOR; CISPLATIN; DOXORUBICIN; FIBRONECTIN; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; MANNOSE BINDING LECTIN; MATRIX METALLOPROTEINASE; METHOTREXATE; PROTEOGLYCAN; SERGLYCIN; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VINCRISTINE;

ANGIOGENESIS; APOPTOSIS; CARCINOGENESIS; CELL DIFFERENTIATION; COMPLEMENT SYSTEM; EPITHELIAL MESENCHYMAL TRANSITION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; HEMATOPOIESIS; HUMAN; IMMUNOREGULATION; INFLAMMATION; MACROPHAGE; NEOPLASM; NEUTROPHIL; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; TUMOR GROWTH; UBIQUITINATION; UPREGULATION;

EID: 84893676049     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00327     Document Type: Review

References (125)

1. Theocharis AD, Skandalis SS, Tzanakakis GN, Karamanos NK. Proteoglycans in health and disease: novel roles for proteoglycans in malignancy and their pharmacological targeting. FEBS J (2010) 277(19):3904-23. doi: 10.1111/j.1742-4658.2010.07800.x
2. Iozzo RV, Sanderson RD. Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J Cell Mol Med (2011) 15(5):1013-31. doi:10.1111/j.1582-4934.2010.01236.x
3. Afratis N, Gialeli C, Nikitovic D, Tsegenidis T, Karousou E, Theocharis AD, et al. Glycosaminoglycans: key players in cancer cell biology and treatment. FEBS J (2012) 279(7):1177-97. doi:10.1111/j.1742-4658.2012.08529.x
4. Kolset SO, Pejler G. Serglycin: a structural and functional chameleon with wide impact on immune cells. J Immunol (2011) 187(10):4927-33. doi:10.4049/jimmunol.1100806
5. Scully OJ, Chua PJ, Harve KS, Bay BH, Yip GW. Serglycin in health and diseases. Anat Rec (Hoboken) (2012) 295(9):1415-20. doi:10.1002/ar.22536
6. Bourdon MA, Oldberg A, Pierschbacher M, Ruoslahti E. Molecular cloning and sequence analysis of a chondroitin sulfate proteoglycan cDNA. Proc Natl Acad Sci U S A (1985) 82(5):1321-5. doi:10.1073/pnas.82.5.1321
7. Schick BP. Serglycin proteoglycan deletion in mouse platelets: physiological effects and their implications for platelet contributions to thrombosis, inflammation, atherosclerosis, and metastasis. Prog Mol Biol Transl Sci (2010) 93:235-87. doi:10.1016/S1877-1173(10)93011-1
8. Kolset SO, Gallagher JT. Proteoglycans in haemopoietic cells. Biochim Biophys Acta (1990) 1032(2-3):191-211.
9. Maillet P, Alliel PM, Mitjavila MT, Perin JP, Jolles P, Bonnet F. Expression of the serglycin gene in human leukemic cell lines. Leukemia (1992) 6(11):1143-7.
10. Niemann CU, Kjeldsen L, Ralfkiaer E, Jensen MK, Borregaard N. Serglycin proteoglycan in hematologic malignancies: a marker of acute myeloid leukemia. Leukemia (2007) 21(12):2406-10. doi:10.1038/sj.leu.2404975
11. Oynebraten I, Hansen B, Smedsrod B, Uhlin-Hansen L. Serglycin secreted by leukocytes is efficiently eliminated from the circulation by sinusoidal scavenger endothelial cells in the liver. J Leukoc Biol (2000) 67(2):183-8.
12. Schick BP, Jacoby JA. Serglycin and betaglycan proteoglycans are expressed in the megakaryocytic cell line CHRF 288-11 and normal human megakaryocytes. J Cell Physiol (1995) 165(1):96-106. doi:10.1002/jcp.1041650113
13. Schick BP, Senkowski-Richardson S. Proteoglycan synthesis in human erythroleukaemia (HEL) cells. Biochem J (1992) 282(Pt 3):651-8.
14. Stellrecht CM, Fraizer G, Selvanayagam C, Chao LY, Lee A, Saunders GF. Transcriptional regulation of a hematopoietic proteoglycan core protein gene during hematopoiesis. J Biol Chem (1993) 268(6):4078-84.
15. Stellrecht CM, Mars WM, Miwa H, Beran M, Saunders GF. Expression pattern of a hematopoietic proteoglycan core protein gene during human hematopoiesis. Differentiation (1991) 48(2):127-35. doi:10.1111/j.1432-0436.1991.tb00251.x
16. Theocharis AD, Seidel C, Borset M, Dobra K, Baykov V, Labropoulou V, et al. Serglycin constitutively secreted by myeloma plasma cells is a potent inhibitor of bone mineralization in vitro. J Biol Chem (2006) 281(46):35116-28. doi:10.1074/jbc. M601061200
17. Toyama-Sorimachi N, Kitamura F, Habuchi H, Tobita Y, Kimata K, Miyasaka M. Widespread expression of chondroitin sulfate-type serglycins with CD44 binding ability in hematopoietic cells. J Biol Chem (1997) 272(42):26714-9. doi:10.1074/jbc.272.42.26714
18. Biederbick A, Licht A, Kleene R. Serglycin proteoglycan is sorted into zymogen granules of rat pancreatic acinar cells. Eur J Cell Biol (2003) 82(1):19-29. doi:10.1078/0171-9335-00287
19. Zhang L, Yang M, Yang D, Cavey G, Davidson P, Gibson G. Molecular interactions of MMP-13 C-terminal domain with chondrocyte proteins. Connect Tissue Res (2010) 51(3):230-9. doi:10.3109/03008200903288902
20. Kulseth MA, Kolset SO, Ranheim T. Stimulation of serglycin and CD44 mRNA expression in endothelial cells exposed to TNF-alpha and IL-1alpha. Biochim Biophys Acta (1999) 1428(2-3):225-32. doi:10.1016/S0304-4165(99)00096-3
21. Lemire JM, Chan CK, Bressler S, Miller J, LeBaron RG, Wight TN. Interleukin-1beta selectively decreases the synthesis of versican by arterial smooth muscle cells. J Cell Biochem (2007) 101(3):753-66. doi:10.1002/jcb.21235
22. Meen AJ, Oynebraten I, Reine TM, Duelli A, Svennevig K, Pejler G, et al. Serglycin is a major proteoglycan in polarized human endothelial cells and is implicated in the secretion of the chemokine GROalpha/CXCL1. J Biol Chem (2011) 286(4):2636-47. doi:10.1074/jbc. M110.151944
23. Schick BP, Gradowski JF, San Antonio JD. Synthesis, secretion, and subcellular localization of serglycin proteoglycan in human endothelial cells. Blood (2001) 97(2):449-58. doi:10.1182/blood. V97.2.449
24. Tyan SW, Hsu CH, Peng KL, Chen CC, Kuo WH, Lee EY, et al. Breast cancer cells induce stromal fibroblasts to secrete ADAMTS1 for cancer invasion through an epigenetic change. PLoS One (2012) 7(4):e35128. doi:10.1371/journal.pone.0035128
25. Werth BB, Bashir M, Chang L, Werth VP. Ultraviolet irradiation induces the accumulation of chondroitin sulfate, but not other glycosaminoglycans, in human skin. PLoS One (2011) 6(8):e14830. doi:10.1371/journal.pone.0014830
26. Grover A, Edwards SA, Bourdon M, Adamson ED. Proteoglycan-19, laminin and collagen type IV production is correlated with the levels of mRNA in F9 cell aggregates differentiating in the presence or absence of cyclic AMP. Differentiation (1987) 36(2):138-44. doi:10.1111/j.1432-0436.1987.tb00188.x
27. Gasimli L, Stansfield HE, Nairn AV, Liu H, Paluh JL, Yang B, et al. Structural remodeling of proteoglycans upon retinoic acid-induced differentiation of NCCIT cells. Glycoconj J (2013) 30(5):497-510. doi:10.1007/s10719-012-9450-x
28. Schick BP, Ho HC, Brodbeck KC, Wrigley CW, Klimas J. Serglycin proteoglycan expression and synthesis in embryonic stem cells. Biochim Biophys Acta (2003) 1593(2-3):259-67. doi:10.1016/S0167-4889(02)00396-8
29. Keith Ho HC, McGrath KE, Brodbeck KC, Palis J, Schick BP. Serglycin proteoglycan synthesis in the murine uterine decidua and early embryo. Biol Reprod (2001) 64(6):1667-76. doi:10.1095/biolreprod64.6.1667
30. Li XJ, Ong CK, Cao Y, Xiang YQ, Shao JY, Ooi A, et al. Serglycin is a theranostic target in nasopharyngeal carcinoma that promotes metastasis. Cancer Res (2011) 71(8):3162-72. doi:10.1158/0008-5472.CAN-10-3557
31. Stevens RL, Fox CC, Lichtenstein LM, Austen KF. Identification of chondroitin sulfate E proteoglycans and heparin proteoglycans in the secretory granules of human lung mast cells. Proc Natl Acad Sci U S A (1988) 85(7):2284-7. doi:10.1073/pnas.85.7.2284
32. Kjellen L, Pettersson I, Lillhager P, Steen ML, Pettersson U, Lehtonen P, et al. Primary structure of a mouse mastocytoma proteoglycan core protein. Biochem J (1989) 263(1):105-13.
33. Lidholt K, Eriksson I, Kjellen L. Heparin proteoglycans synthesized by mouse mastocytoma contain chondroitin sulphate. Biochem J (1995) 311(Pt 1):233-8.
34. Abrink M, Grujic M, Pejler G. Serglycin is essential for maturation of mast cell secretory granule. J Biol Chem (2004) 279(39):40897-905. doi:10.1074/jbc. M405856200
35. Yurt RW, Leid RW Jr, Austen KF. Native heparin from rat peritoneal mast cells. J Biol Chem (1977) 252(2):518-21.
36. Gilead L, Livni N, Eliakim R, Ligumsky M, Fich A, Okon E, et al. Human gastric mucosal mast cells are chondroitin sulphate E-containing mast cells. Immunology (1987) 62(1):23-8.
37. Enerback L, Kolset SO, Kusche M, Hjerpe A, Lindahl U. Glycosaminoglycans in rat mucosal mast cells. Biochem J (1985) 227(2):661-8.
38. Stevens RL, Lee TD, Seldin DC, Austen KF, Befus AD, Bienenstock J. Intestinal mucosal mast cells from rats infected with Nippostrongylus brasiliensis contain protease-resistant chondroitin sulfate di-B proteoglycans. J Immunol (1986) 137(1):291-5.
39. Murata K. Acidic glycosaminoglycans in human platelets and leukocytes: the isolation and enzymatic characterization of chondroitin 4-sulfate. Clin Chim Acta (1974) 57(2):115-24. doi:10.1016/0009-8981(74)90418-5
40. Olsson I, Gardell S. Isolation and characterization of glycosaminoglycans from human leukocytes and platelets. Biochim Biophys Acta (1967) 141(2):348-57. doi:10.1016/0304-4165(67)90109-2
41. Metcalfe DD, Wasserman SI, Austen KF. Isolation and characterization of sulphated mucopolysaccharides from rat leukaemic (RBL-1) basophils. Biochem J (1980) 185(2):367-72.
42. Orenstein NS, Galli SJ, Dvorak AM, Silbert JE, Dvorak HF. Sulfated glycosaminoglycans of guinea pig basophilic leukocytes. J Immunol (1978) 121(2):586-92.
43. Schick BP, Walsh CJ, Jenkins-West T. Sulfated proteoglycans and sulfated proteins in guinea pig megakaryocytes and platelets in vivo. Relevance to megakaryocyte maturation and platelet activation. J Biol Chem (1988) 263(2):1052-62.
44. Kolset SO. Oversulfated chondroitin sulfate proteoglycan in cultured human peritoneal macrophages. Biochem Biophys Res Commun (1986) 139(2):377-82. doi:10.1016/S0006-291X(86)80001-8
45. Kolset SO, Kjellen L, Seljelid R, Lindahl U. Changes in glycosaminoglycan biosynthesis during differentiation in vitro of human monocytes. Biochem J (1983) 210(3):661-7.
46. Uhlin-Hansen L, Eskeland T, Kolset SO. Modulation of the expression of chondroitin sulfate proteoglycan in stimulated human monocytes. J Biol Chem (1989) 264(25):14916-22.
47. Mattei MG, Perin JP, Alliel PM, Bonnet F, Maillet P, Passage E, et al. Localization of human platelet proteoglycan gene to chromosome 10, band q22.1, by in situ hybridization. Hum Genet (1989) 82(1):87-8. doi:10.1007/BF00288281
48. Stevens RL, Avraham S, Gartner MC, Bruns GA, Austen KF, Weis JH. Isolation and characterization of a cDNA that encodes the peptide core of the secretory granule proteoglycan of human promyelocytic leukemia HL-60 cells. J Biol Chem (1988) 263(15):7287-91.
49. Humphries DE, Nicodemus CF, Schiller V, Stevens RL. The human serglycin gene. Nucleotide sequence and methylation pattern in human promyelocytic leukemia HL-60 cells and T-lymphoblast Molt-4 cells. J Biol Chem (1992) 267(19):13558-63.
50. Nicodemus CF, Avraham S, Austen KF, Purdy S, Jablonski J, Stevens RL. Characterization of the human gene that encodes the peptide core of secretory granule proteoglycans in promyelocytic leukemia HL-60 cells and analysis of the translated product. J Biol Chem (1990) 265(10):5889-96.
51. Schick BP, Petrushina I, Brodbeck KC, Castronuevo P. Promoter regulatory elements and DNase I-hypersensitive sites involved in serglycin proteoglycan gene expression in human erythroleukemia, CHRF 288-11, and HL-60 cells. J Biol Chem (2001) 276(27):24726-35. doi:10.1074/jbc. M102958200
52. Papas TS, Watson DK, Sacchi N, Fujiwara S, Seth AK, Fisher RJ, et al. ETS family of genes in leukemia and Down syndrome. Am J Med Genet Suppl (1990) 7:251-61.
53. Deininger P. Alu elements: know the SINEs. Genome Biol (2011) 12(12):236. doi:10.1186/gb-2011-12-12-236
54. Castronuevo P, Thornton MA, McCarthy LE, Klimas J, Schick BP. DNase I hypersensitivity patterns of the serglycin proteoglycan gene in resting and phorbol 12-myristate 13-acetate-stimulated human erythroleukemia (HEL), CHRF 288-11, and HL-60 cells compared with neutrophils and human umbilical vein endothelial cells. J Biol Chem (2003) 278(49):48704-12. doi:10.1074/jbc. M310220200
55. Toyama-Sorimachi N, Sorimachi H, Tobita Y, Kitamura F, Yagita H, Suzuki K, et al. A novel ligand for CD44 is serglycin, a hematopoietic cell lineage-specific proteoglycan. Possible involvement in lymphoid cell adherence and activation. J Biol Chem (1995) 270(13):7437-44. doi:10.1074/jbc.270.13.7437
56. Skliris A, Happonen KE, Terpos E, Labropoulou V, Borset M, Heinegard D, et al. Serglycin inhibits the classical and lectin pathways of complement via its glycosaminoglycan chains: implications for multiple myeloma. Eur J Immunol (2011) 41(2):437-49. doi:10.1002/eji.201040429
57. Skliris A, Labropoulou VT, Papachristou DJ, Aletras A, Karamanos NK, Theocharis AD. Cell-surface serglycin promotes adhesion of myeloma cells to collagen type I and affects the expression of matrix metalloproteinases. FEBS J (2013) 280(10):2342-52. doi:10.1111/febs.12179
58. Brennan MJ, Oldberg A, Hayman EG, Ruoslahti E. Effect of a proteoglycan produced by rat tumor cells on their adhesion to fibronectin-collagen substrata. Cancer Res (1983) 43(9):4302-7.
59. Schick BP, Pestina TI, San Antonio JD, Stenberg PE, Jackson CW. Decreased serglycin proteoglycan size is associated with the plateletalpha granule storage defect in Wistar Furth hereditary macrothrombocytopenic rats. Serglycin binding affinity to type I collagen is unaltered. J Cell Physiol (1997) 172(1):87-93. doi:10.1002/(SICI)1097-4652(199707)172:1>87::AID-JCP10>3.0.CO;2-L
60. Kolset SO, Mann DM, Uhlin-Hansen L, Winberg JO, Ruoslahti E. Serglycin-binding proteins in activated macrophages and platelets. J Leukoc Biol (1996) 59(4):545-54.
61. Galvin JP, Spaeny-Dekking LH, Wang B, Seth P, Hack CE, Froelich CJ. Apoptosis induced by granzyme B-glycosaminoglycan complexes: implications for granule-mediated apoptosis in vivo. J Immunol (1999) 162(9): 5345-50.
62. Metkar SS, Wang B, Aguilar-Santelises M, Raja SM, Uhlin-Hansen L, Podack E, et al. Cytotoxic cell granule-mediated apoptosis: perforin delivers granzyme B-serglycin complexes into target cells without plasma membrane pore formation. Immunity (2002) 16(3):417-28. doi:10.1016/S1074-7613(02)00286-8
63. Raja SM, Wang B, Dantuluri M, Desai UR, Demeler B, Spiegel K, et al. Cytotoxic cell granule-mediated apoptosis. Characterization of the macromolecular complex of granzyme B with serglycin. J Biol Chem (2002) 277(51):49523-30. doi:10.1074/jbc. M209607200
64. Pejler G, Maccarana M. Interaction of heparin with rat mast cell protease 1. J Biol Chem (1994) 269(20):14451-6.
65. Kolset SO, Prydz K, Pejler G. Intracellular proteoglycans. Biochem J (2004) 379(Pt 2):217-27. doi:10.1042/BJ20031230
66. Lindstedt KA, Kokkonen JO, Kovanen PT. Regulation of the activity of secreted human lung mast cell tryptase by mast cell proteoglycans. Biochim Biophys Acta (1998) 1425(3):617-27. doi:10.1016/S0304-4165(98)00115-9
67. Stevens RL, Adachi R. Protease-proteoglycan complexes of mouse and human mast cells and importance of their beta-tryptase-heparin complexes in inflammation and innate immunity. Immunol Rev (2007) 217:155-67. doi:10.1111/j.1600-065X.2007.00525.x
68. Braga T, Grujic M, Lukinius A, Hellman L, Abrink M, Pejler G. Serglycin proteoglycan is required for secretory granule integrity in mucosal mast cells. Biochem J (2007) 403(1):49-57. doi:10.1042/BJ20061257
69. Ringvall M, Ronnberg E, Wernersson S, Duelli A, Henningsson F, Abrink M, et al. Serotonin and histamine storage in mast cell secretory granules is dependent on serglycin proteoglycan. J Allergy Clin Immunol (2008) 121(4):1020-6. doi:10.1016/j.jaci.2007.11.031
70. Ronnberg E, Calounova G, Pejler G. Mast cells express tyrosine hydroxylase and store dopamine in a serglycin-dependent manner. Biol Chem (2012) 393(1-2):107-12. doi:10.1515/BC-2011-220
71. Niemann CU, Abrink M, Pejler G, Fischer RL, Christensen EI, Knight SD, et al. Neutrophil elastase depends on serglycin proteoglycan for localization in granules. Blood (2007) 109(10):4478-86. doi:10.1182/blood-2006-02-001719
72. Lemansky P, Smolenova E, Wrocklage C, Hasilik A. Neutrophil elastase is associated with serglycin on its way to lysosomes in U937 cells. Cell Immunol (2007) 246(1):1-7. doi:10.1016/j.cellimm.2007.06.001
73. Malla N, Berg E, Theocharis AD, Svineng G, Uhlin-Hansen L, Winberg JO. In vitro reconstitution of complexes between pro-matrix metalloproteinase-9 and the proteoglycans serglycin and versican. FEBS J (2013) 280(12):2870-87. doi:10.1111/febs.12291
74. Winberg JO, Kolset SO, Berg E, Uhlin-Hansen L. Macrophages secrete matrix metalloproteinase 9 covalently linked to the core protein of chondroitin sulphate proteoglycans. J Mol Biol (2000) 304(4):669-80. doi:10.1006/jmbi.2000.4235
75. Vinayagam A, Stelzl U, Foulle R, Plassmann S, Zenkner M, Timm J, et al. A directed protein interaction network for investigating intracellular signal transduction. Sci Signal (2011) 4(189):rs8. doi:10.1126/scisignal.2001699
76. Lim J, Hao T, Shaw C, Patel AJ, Szabo G, Rual JF, et al. A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration. Cell (2006) 125(4):801-14. doi:10.1016/j.cell.2006.03.032
77. Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, et al. Towards a proteome-scale map of the human protein-protein interaction network. Nature (2005) 437(7062):1173-8. doi:10.1038/nature04209
78. Jang CY, Wong J, Coppinger JA, Seki A, Yates JR III, Fang G. DDA3 recruits microtubule depolymerase Kif2a to spindle poles and controls spindle dynamics and mitotic chromosome movement. J Cell Biol (2008) 181(2):255-67. doi:10.1083/jcb.200711032
79. Kumar A, Rajendran V, Sethumadhavan R, Purohit R. CEP proteins: the knights of centrosome dynasty. Protoplasma (2013) 250(5):965-83. doi:10.1007/s00709-013-0488-9
80. Leznicki P, High S. SGTA antagonizes BAG6-mediated protein triage. Proc Natl Acad Sci U S A (2012) 109(47):19214-9. doi:10.1073/pnas.1209997109
81. Akahane T, Sahara K, Yashiroda H, Tanaka K, Murata S. Involvement of Bag6 and the TRC pathway in proteasome assembly. Nat Commun (2013) 4:2234. doi:10.1038/ncomms3234
82. Kim ST, Tasaki T, Zakrzewska A, Yoo YD, Sa Sung K, Kim BY, et al. The N-end rule proteolytic system in autophagy. Autophagy (2013) 9(7): doi:10.4161/auto.24643
83. Tasaki T, Kim ST, Zakrzewska A, Lee BE, Kang MJ, Yoo YD, et al. UBR box N-recognin-4 (UBR4), an N-recognin of the N-end rule pathway, and its role in yolk sac vascular development and autophagy. Proc Natl Acad Sci U S A (2013) 110(10):3800-5. doi:10.1073/pnas.1217358110
84. Su V, Nakagawa R, Koval M, Lau AF. Ubiquitin-independent proteasomal degradation of endoplasmic reticulum-localized connexin43 mediated by CIP75. J Biol Chem (2010) 285(52):40979-90. doi:10.1074/jbc. M110.170753
85. Yun Lee D, Arnott D, Brown EJ. Ubiquilin4 is an adaptor protein that recruits Ubiquilin1 to the autophagy machinery. EMBO Rep (2013) 14(4):373-81. doi:10.1038/embor.2013.22
86. Wu G, Feng X, Stein L. A human functional protein interaction network and its application to cancer data analysis. Genome Biol (2010) 11(5):R53. doi:10.1186/gb-2010-11-5-r53
87. Zernichow L, Abrink M, Hallgren J, Grujic M, Pejler G, Kolset SO. Serglycin is the major secreted proteoglycan in macrophages and has a role in the regulation of macrophage tumor necrosis factor-alpha secretion in response to lipopolysaccharide. J Biol Chem (2006) 281(37):26792-801. doi:10.1074/jbc. M512889200
88. Imoto-Tsubakimoto H, Takahashi T, Ueyama T, Ogata T, Adachi A, Nakanishi N, et al. Serglycin is a novel adipocytokine highly expressed in epicardial adipose tissue. Biochem Biophys Res Commun (2013) 432(1):105-10. doi:10.1016/j.bbrc.2013.01.078
89. Pejler G, Sadler JE. Mechanism by which heparin proteoglycan modulates mast cell chymase activity. Biochemistry (1999) 38(37):12187-95. doi:10.1021/bi991046b
90. Pejler G, Berg L. Regulation of rat mast cell protease 1 activity. Protease inhibition is prevented by heparin proteoglycan. Eur J Biochem (1995) 233(1):192-9. doi:10.1111/j.1432-1033.1995.192_1.x
91. Lindstedt L, Lee M, Kovanen PT. Chymase bound to heparin is resistant to its natural inhibitors and capable of proteolyzing high density lipoproteins in aortic intimal fluid. Atherosclerosis (2001) 155(1):87-97. doi:10.1016/S0021-9150(00)00544-X
92. Hallgren J, Spillmann D, Pejler G. Structural requirements and mechanism for heparin-induced activation of a recombinant mouse mast cell tryptase, mouse mast cell protease-6: formation of active tryptase monomers in the presence of low molecular weight heparin. J Biol Chem (2001) 276(46):42774-81. doi:10.1074/jbc. M105531200
93. Sakai K, Ren S, Schwartz LB. A novel heparin-dependent processing pathway for human tryptase. Autocatalysis followed by activation with dipeptidyl peptidase I. J Clin Invest (1996) 97(4):988-95. doi:10.1172/JCI118523
94. Kolset SO, Tveit H. Serglycin-structure and biology. Cell Mol Life Sci (2008) 65(7-8):1073-85. doi:10.1007/s00018-007-7455-6
95. Grujic M, Braga T, Lukinius A, Eloranta ML, Knight SD, Pejler G, et al. Serglycin-deficient cytotoxic T lymphocytes display defective secretory granule maturation and granzyme B storage. J Biol Chem (2005) 280(39):33411-8. doi:10.1074/jbc. M501708200
96. Woulfe DS, Lilliendahl JK, August S, Rauova L, Kowalska MA, Abrink M, et al. Serglycin proteoglycan deletion induces defects in platelet aggregation and thrombus formation in mice. Blood (2008) 111(7):3458-67. doi:10.1182/blood-2007-07-104703
97. Melo FR, Waern I, Ronnberg E, Abrink M, Lee DM, Schlenner SM, et al. A role for serglycin proteoglycan in mast cell apoptosis induced by a secretory granule-mediated pathway. J Biol Chem (2011) 286(7):5423-33. doi:10.1074/jbc. M110.176461
98. Melo FR, Grujic M, Spirkoski J, Calounova G, Pejler G. Serglycin proteoglycan promotes apoptotic versus necrotic cell death in mast cells. J Biol Chem (2012) 287(22):18142-52. doi:10.1074/jbc. M112.344796
99. Grujic M, Christensen JP, Sorensen MR, Abrink M, Pejler G, Thomsen AR. Delayed contraction of the CD8+ T cell response toward lymphocytic choriomeningitis virus infection in mice lacking serglycin. J Immunol (2008) 181(2):1043-51.
100. Sawesi O, Spillmann D, Lunden A, Wernersson S, Abrink M. Serglycin-independent release of active mast cell proteases in response to Toxoplasma gondii infection. J Biol Chem (2010) 285(49):38005-13. doi:10.1074/jbc. M110.118471
101. Kim JS, Werth VP. Identification of specific chondroitin sulfate species in cutaneous autoimmune disease. J Histochem Cytochem (2011) 59(8):780-90. doi:10.1369/0022155411411304
102. Korpetinou A, Milia-Argeiti E, Labropoulou V, Theocharis AD. Serglycin: a novel player in the terrain of neoplasia. In: Karamanos NK, editor. Extracellular Matrix: Pathobiology and Signaling. Berlin: Walter de Gruyter GmbH & Co. KG (2012). p. 677-88.
103. He L, Zhou X, Qu C, Tang Y, Zhang Q, Hong J. Serglycin (SRGN) overexpression predicts poor prognosis in hepatocellular carcinoma patients. Med Oncol (2013) 30(4):707. doi:10.1007/s12032-013-0707-4
104. Zoller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer (2011) 11(4):254-67. doi:10.1038/nrc3023
105. Skandalis SS, Kozlova I, Engstrom U, Hellman U, Heldin P. Proteomic identification of CD44 interacting proteins. IUBMB Life (2010) 62(11):833-40. doi:10.1002/iub.392
106. Zernichow L, Dalen KT, Prydz K, Winberg JO, Kolset SO. Secretion of proteases in serglycin transfected Madin-Darby canine kidney cells. FEBS J (2006) 273(3):536-47. doi:10.1111/j.1742-4658.2005.05085.x
107. Gialeli C, Theocharis AD, Karamanos NK. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J (2011) 278(1):16-27. doi:10.1111/j.1742-4658.2010.07919.x
108. Labropoulou VT, Theocharis AD, Symeonidis A, Skandalis SS, Karamanos NK, Kalofonos HP. Pathophysiology and pharmacological targeting of tumor-induced bone disease: current status and emerging therapeutic interventions. Curr Med Chem (2011) 18(11):1584-98. doi:10.2174/092986711795471275
109. Winberg JO, Berg E, Kolset SO, Uhlin-Hansen L. Calcium-induced activation and truncation of promatrix metalloproteinase-9 linked to the core protein of chondroitin sulfate proteoglycans. Eur J Biochem (2003) 270(19):3996-4007. doi:10.1046/j.1432-1033.2003.03788.x
110. Korpetinou A, Skandalis SS, Moustakas A, Happonen KE, Tveit H, Prydz K, et al. Serglycin is implicated in the promotion of aggressive phenotype of breast cancer cells. PLoS One (2013) 8(10):e78157. doi:10.1371/journal.pone.0078157
111. Rutkowski MJ, Sughrue ME, Kane AJ, Mills SA, Parsa AT. Cancer and the complement cascade. Mol Cancer Res (2010) 8(11):1453-65. doi:10.1158/1541-7786.MCR-10-0225
112. Beyer-Sehlmeyer G, Hiddemann W, Wormann B, Bertram J. Suppressive subtractive hybridisation reveals differential expression of serglycin, sorcin, bone marrow proteoglycan and prostate-tumour-inducing gene I (PTI-1) in drug-resistant and sensitive tumour cell lines of haematopoetic origin. Eur J Cancer (1999) 35(12):1735-42. doi:10.1016/S0959-8049(99)00202-6
113. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell (2006) 10(6):515-27. doi:10.1016/j.ccr.2006.10.008
114. Blick T, Hugo H, Widodo E, Waltham M, Pinto C, Mani SA, et al. Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the CD44(hi/)CD24 (lo/-) stem cell phenotype in human breast cancer. J Mammary Gland Biol Neoplasia (2010) 15(2):235-52. doi:10.1007/s10911-010-9175-z
115. Theocharis AD, Tsolakis I, Tzanakakis GN, Karamanos NK. Chondroitin sulfate as a key molecule in the development of atherosclerosis and cancer progression. Adv Pharmacol (2006) 53:281-95. doi:10.1016/S1054-3589(05)53013-8
116. Cooney CA, Jousheghany F, Yao-Borengasser A, Phanavanh B, Gomes T, Kieber-Emmons AM, et al. Chondroitin sulfates play a major role in breast cancer metastasis: a role for CSPG4 and CHST11 gene expression in forming surface P-selectin ligands in aggressive breast cancer cells. Breast Cancer Res (2011) 13(3):R58. doi:10.1186/bcr2895
117. Evans A, Costello E. The role of inflammatory cells in fostering pancreatic cancer cell growth and invasion. Front Physiol (2012) 3:270. doi:10.3389/fphys.2012.00270
118. Protti MP, De Monte L. Immune infiltrates as predictive markers of survival in pancreatic cancer patients. Front Physiol (2013) 4:210. doi:10.3389/fphys.2013.00210
119. Dai H, Korthuis RJ. Mast cell proteases and inflammation. Drug Discov Today Dis Models (2011) 8(1):47-55. doi:10.1016/j.ddmod.2011.06.004
120. Tchougounova E, Lundequist A, Fajardo I, Winberg JO, Abrink M, Pejler G. A key role for mast cell chymase in the activation of pro-matrix metalloprotease-9 and pro-matrix metalloprotease-2. J Biol Chem (2005) 280(10):9291-6. doi:10.1074/jbc. M410396200
121. Saarinen J, Kalkkinen N, Welgus HG, Kovanen PT. Activation of human interstitial procollagenase through direct cleavage of the Leu83-Thr84 bond by mast cell chymase. J Biol Chem (1994) 269(27):18134-40.
122. Zhang L. Glycosaminoglycan (GAG) biosynthesis and GAG-binding proteins. Prog Mol Biol Transl Sci (2010) 93:1-17. doi:10.1016/S1877-1173(10)93001-9
123. Gay LJ, Felding-Habermann B. Platelets alter tumor cell attributes to propel metastasis: programming in transit. Cancer Cell (2011) 20(5):553-4. doi:10.1016/j.ccr.2011.11.001
124. Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell (2011) 20(5):576-90. doi:10.1016/j.ccr.2011.09.009
125. Li J, King MR. Adhesion receptors as therapeutic targets for circulating tumor cells. Front Oncol (2012) 2:79. doi:10.3389/fonc.2012.00079