Cross-talk between endocytic clearance and secretion in macrophages

Immunobiology

Volumn 214, Issue 7, 2009, Pages 576-593

  Kzhyshkowska, Julia ^a,b   Krusell, Liis ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b INSTITUTE OF GENERAL PATHOLOGY AND PATHOPHYSIOLOGY   (Russian Federation)

Author keywords

Chitinase; Endocytosis; Macrophages; Mannose 6 phosphate receptor; Scavenger receptor; Secretion; Stabilin 1

Indexed keywords

ADAPTOR PROTEIN; CELL ENZYME; CHITINASE; CLATHRIN; CYTOKINE; HYDROLASE; LOW DENSITY LIPOPROTEIN; MANNOSE 6 PHOSPHATE; OSTEONECTIN; PLACENTA LACTOGEN; SCAVENGER RECEPTOR; STABILIN 1; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CATALYSIS; CELL ADHESION; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL SECRETION; CELL SELECTION; CELL STRUCTURE; CELL SUBPOPULATION; CELL TRANSPORT; CELL VACUOLE; ENDOCYTOSIS; ENDOSOME; EXOCYTOSIS; EXTRACELLULAR MATRIX; GOLGI COMPLEX; HUMAN; IMMUNOMODULATION; INFLAMMATION; INTERNALIZATION; LYSOSOME; MACROPHAGE; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TELOMERE; TRANSCRIPTION INITIATION; TRANSCYTOSIS; UBIQUITINATION;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; HUMANS; IMMUNITY, INNATE; MACROPHAGES; PROTEIN TRANSPORT; RECEPTOR CROSS-TALK; RECEPTORS, LYMPHOCYTE HOMING; SECRETORY PATHWAY; SIGNAL TRANSDUCTION; VESICULAR TRANSPORT PROTEINS;

EID: 68649119986     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2009.03.007     Document Type: Article

References (125)

1. Adachi H., and Tsujimoto M. FEEL-1, a novel scavenger receptor with in vitro bacteria-binding and angiogenesis-modulating activities. J. Biol. Chem. 277 (2002) 34264-34270
2. Andrews N.W. Regulated secretion of conventional lysosomes. Trends Cell Biol. 10 (2000) 316-321
3. Anthony R.V., Fanning M.D., Limesand S.W., and Liang R. Placental lactogen and growth hormone: regulation and action. In: Bazer F.W. (Ed). Endocrinology of Pregnancy (1998), Humana Press Inc., Totawa, NJ 461-490
4. Arighi C.N., Hartnell L.M., Aguilar R.C., Haft C.R., and Bonifacino J.S. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165 (2004) 123-133
5. Arunachalam B., Phan U.T., Geuze H.J., and Cresswell P. Enzymatic reduction of disulfide bonds in lysosomes: characterization of a gamma-interferon-inducible lysosomal thiol reductase (GILT). Proc. Natl. Acad. Sci. USA 97 (2000) 745-750
6. Astarie-Dequeker C., Carreno S., Cougoule C., and Maridonneau-Parini I. The protein tyrosine kinase Hck is located on lysosomal vesicles that are physically and functionally distinct from CD63-positive lysosomes in human macrophages. J. Cell Sci. 115 (2002) 81-89
7. Badariotti F., Kypriotou M., Lelong C., Dubos M.P., Renard E., Galera P., and Favrel P. The phylogenetically conserved molluscan chitinase-like protein 1 (Cg-Clp1), homologue of human HC-gp39, stimulates proliferation and regulates synthesis of extracellular matrix components of mammalian chondrocytes. J. Biol. Chem. 281 (2006) 29583-29596
8. Bai H., Doray B., and Kornfeld S. GGA1 interacts with the adaptor protein AP-1 through a WNSF sequence in its hinge region. J. Biol. Chem. 279 (2004) 17411-17417
9. Bigg H.F., Wait R., Rowan A.D., and Cawston T.E. The mammalian chitinase-like lectin, YKL-40, binds specifically to type I collagen and modulates the rate of type I collagen fibril formation. J. Biol. Chem. 281 (2006) 21082-21095
10. Bonifacino J.S. The GGA proteins: adaptors on the move. Nat. Rev. Mol. Cell Biol. 5 (2004) 23-32
11. Bornstein P., and Sage E.H. Matricellular proteins: extracellular modulators of cell function. Curr. Opin. Cell Biol. 14 (2002) 608-616
12. Bradshaw A.D., Reed M.J., and Sage E.H. SPARC-null mice exhibit accelerated cutaneous wound closure. J. Histochem. Cytochem. 50 (2002) 1-10
13. Bradshaw A.D., and Sage E.H. SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J. Clin. Invest. 107 (2001) 1049-1054
14. Brekken R.A., Puolakkainen P., Graves D.C., Workman G., Lubkin S.R., and Sage E.H. Enhanced growth of tumors in SPARC null mice is associated with changes in the ECM. J. Clin. Invest. 111 (2003) 487-495
15. Brekken R.A., and Sage E.H. SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol. 19 (2001) 816-827
16. Cai H., Reinisch K., and Ferro-Novick S. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev. Cell 12 (2007) 671-682
17. Carroll K.S., Hanna J., Simon I., Krise J., Barbero P., and Pfeffer S.R. Role of Rab9 GTPase in facilitating receptor recruitment by TIP47. Science 292 (2001) 1373-1376
18. Chung E.Y., Liu J., Homma Y., Zhang Y., Brendolan A., Saggese M., Han J., Silverstein R., Selleri L., and Ma X. Interleukin-10 expression in macrophages during phagocytosis of apoptotic cells is mediated by homeodomain proteins Pbx1 and Prep-1. Immunity 27 (2007) 952-964
19. Collot-Teixeira S., Martin J., McDermott-Roe C., Poston R., and McGregor J.L. CD36 and macrophages in atherosclerosis. Cardiovasc. Res. 75 (2007) 468-477
20. Cotena A., Gordon S., and Platt N. The class A macrophage scavenger receptor attenuates CXC chemokine production and the early infiltration of neutrophils in sterile peritonitis. J. Immunol. 173 (2004) 6427-6432
21. Crump C.M., Xiang Y., Thomas L., Gu F., Austin C., Tooze S.A., and Thomas G. PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J. 20 (2001) 2191-2201
22. Czibener C., Sherer N.M., Becker S.M., Pypaert M., Hui E., Chapman E.R., Mothes W., and Andrews N.W. Ca2+ and synaptotagmin VII-dependent delivery of lysosomal membrane to nascent phagosomes. J. Cell Biol. 174 (2006) 997-1007
23. Dahms N.M., Lobel P., and Kornfeld S. Mannose 6-phosphate receptors and lysosomal enzyme targeting. J. Biol. Chem. 264 (1989) 12115-12118
24. Diaz E., and Pfeffer S.R. TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 93 (1998) 433-443
25. Doray B., Bruns K., Ghosh P., and Kornfeld S. Interaction of the cation-dependent mannose 6-phosphate receptor with GGA proteins. J. Biol. Chem. 277 (2002) 18477-18482
26. Doray B., Bruns K., Ghosh P., and Kornfeld S.A. Autoinhibition of the ligand-binding site of GGA1/3 VHS domains by an internal acidic cluster-dileucine motif. Proc. Natl. Acad. Sci. USA 99 (2002) 8072-8077
27. Doray B., Ghosh P., Griffith J., Geuze H.J., and Kornfeld S. Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science 297 (2002) 1700-1703
28. Du H., Masuko-Hongo K., Nakamura H., Xiang Y., Bao C.D., Wang X.D., Chen S.L., Nishioka K., and Kato T. The prevalence of autoantibodies against cartilage intermediate layer protein, YKL-39, osteopontin, and cyclic citrullinated peptide in patients with early-stage knee osteoarthritis: evidence of a variety of autoimmune processes. Rheumatol. Int. 26 (2005) 35-41
29. Elomaa O., Kangas M., Sahlberg C., Tuukkanen J., Sormunen R., Liakka A., Thesleff I., Kraal G., and Tryggvason K. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 80 (1995) 603-609
30. Fitzgerald M.L., and Reed G.L. Rab6 is phosphorylated in thrombin-activated platelets by a protein kinase C-dependent mechanism: effects on GTP/GDP binding and cellular distribution. Biochem. J. 342 Part 2 (1999) 353-360
31. Framson P.E., and Sage E.H. SPARC and tumor growth: where the seed meets the soil?. J. Cell Biochem. 92 (2004) 679-690
32. Garmroudi F., and MacDonald R.G. Localization of the insulin-like growth factor II (IGF-II) binding/cross-linking site of the IGF-II/mannose 6-phosphate receptor to extracellular repeats 10-11. J. Biol. Chem. 269 (1994) 26944-26952
33. Ghosh P., Dahms N.M., and Kornfeld S. Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell Biol. 4 (2003) 202-212
34. Ghosh P., Griffith J., Geuze H.J., and Kornfeld S. Mammalian GGAs act together to sort mannose 6-phosphate receptors. J. Cell Biol. 163 (2003) 755-766
35. Ghosh P., and Kornfeld S. AP-1 binding to sorting signals and release from clathrin-coated vesicles is regulated by phosphorylation. J. Cell Biol. 160 (2003) 699-708
36. Ghosh P., and Kornfeld S. The GGA proteins: key players in protein sorting at the trans-Golgi network. Eur. J. Cell Biol. 83 (2004) 257-262
37. Godar S., Horejsi V., Weidle U.H., Binder B.R., Hansmann C., and Stockinger H. M6P/IGFII-receptor complexes urokinase receptor and plasminogen for activation of transforming growth factor-beta1. Eur. J. Immunol. 29 (1999) 1004-1013
38. Goerdt S., and Orfanos C.E. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10 (1999) 137-142
39. Gordon S. Pattern recognition receptors: doubling up for the innate immune response. Cell 111 (2002) 927-930
40. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 3 (2003) 23-35
41. Gratchev A., Kzhyshkowska J., Duperrier K., Utikal J., Velten F.W., and Goerdt S. The receptor for interleukin-17E is induced by Th2 cytokines in antigen-presenting cells. Scand. J. Immunol. 60 (2004) 233-237
42. Gratchev A., Kzhyshkowska J., Kothe K., Muller-Molinet I., Kannookadan S., Utikal J., and Goerdt S. Mphi1 and Mphi2 can be re-polarized by Th2 or Th1 cytokines, respectively, and respond to exogenous danger signals. Immunobiology 211 (2006) 473-486
43. Gratchev A., Kzhyshkowska J., Utikal J., and Goerdt S. Interleukin-4 and dexamethasone counterregulate extracellular matrix remodelling and phagocytosis in type-2 macrophages. Scand. J. Immunol. 61 (2005) 10-17
44. Gratchev A., Schmuttermaier C., Mamidi S., Gooi L., Goerdt S., and Kzhyshkowska J. Expression of osteoarthritis marker YKL-39 is stimulated by transforming growth factor beta (TGF-beta) and IL-4 in differentiating macrophages. Biomarker Insights (2008) 39-44
45. Greaves D.R., and Gordon S. Thematic review series: the immune system and atherogenesis. Recent insights into the biology of macrophage scavenger receptors. J. Lipid Res. 46 (2005) 11-20
46. Hakala J.K., Lindstedt K.A., Kovanen P.T., and Pentikainen M.O. Low-density lipoprotein modified by macrophage-derived lysosomal hydrolases induces expression and secretion of IL-8 via p38 MAPK and NF-kappaB by human monocyte-derived macrophages. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 2504-2509
47. Hakala J.K., Oksjoki R., Laine P., Du H., Grabowski G.A., Kovanen P.T., and Pentikainen M.O. Lysosomal enzymes are released from cultured human macrophages, hydrolyze LDL in vitro, and are present extracellularly in human atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 1430-1436
48. Hattula K., Furuhjelm J., Arffman A., and Peranen J. A Rab8-specific GDP/GTP exchange factor is involved in actin remodeling and polarized membrane transport. Mol. Biol. Cell 13 (2002) 3268-3280
49. Jozefowski S., and Kobzik L. Scavenger receptor A mediates H2O2 production and suppression of IL-12 release in murine macrophages. J. Leukoc. Biol. 76 (2004) 1066-1074
50. Jozefowski S., Sulahian T.H., Arredouani M., and Kobzik L. Role of scavenger receptor MARCO in macrophage responses to CpG oligodeoxynucleotides. J. Leukoc. Biol. 80 (2006) 870-879
51. Kornfeld S. Trafficking of lysosomal enzymes in normal and disease states. J. Clin. Invest. 77 (1986) 1-6
52. Kornfeld S., and Mellman I. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5 (1989) 483-525
53. Koukourakis M.I., Giatromanolaki A., Brekken R.A., Sivridis E., Gatter K.C., Harris A.L., and Sage E.H. Enhanced expression of SPARC/osteonectin in the tumor-associated stroma of non-small cell lung cancer is correlated with markers of hypoxia/acidity and with poor prognosis of patients. Cancer Res. 63 (2003) 5376-5380
54. Krieger M., and Stern D.M. Series introduction: multiligand receptors and human disease. J. Clin. Invest. 108 (2001) 645-647
55. Kzhyshkowska J., Gratchev A., Brundiers H., Mamidi S., Krusell L., and Goerdt S. Phosphatidylinositide 3-kinase activity is required for stabilin-1-mediated endosomal transport of acLDL. Immunobiology 210 (2005) 161-173
56. Kzhyshkowska J., Gratchev A., and Goerdt S. Stabilin-1, a homeostatic scavenger receptor with multiple functions. J. Cell Mol. Med. 10 (2006) 635-649
57. Kzhyshkowska J., Gratchev A., and Goerdt S. Human chitinases and chitinase-like proteins as indicators for inflammation and cancer. Biomarker Insights (2007) 128-146
58. Kzhyshkowska J., Gratchev A., Martens J.H., Pervushina O., Mamidi S., Johansson S., Schledzewski K., Hansen B., He X., Tang J., Nakayama K., and Goerdt S. Stabilin-1 localizes to endosomes and the trans-Golgi network in human macrophages and interacts with GGA adaptors. J. Leukoc. Biol. 76 (2004) 1151-1161
59. Kzhyshkowska J., Gratchev A., Schmuttermaier C., Brundiers H., Krusell L., Mamidi S., Zhang J., Workman G., Sage E.H., Anderle C., Sedlmayr P., and Goerdt S. Alternatively activated macrophages regulate extracellular levels of the hormone placental lactogen via receptor-mediated uptake and transcytosis. J. Immunol. 180 (2008) 3028-3037
60. Kzhyshkowska J., Mamidi S., Gratchev A., Kremmer E., Schmuttermaier C., Krusell L., Haus G., Utikal J., Schledzewski K., Scholtze J., and Goerdt S. Novel stabilin-1 interacting chitinase-like protein (SI-CLP) is up-regulated in alternatively activated macrophages and secreted via lysosomal pathway. Blood 107 (2006) 3221-3228
61. Kzhyshkowska J., Marciniak-Czochra A., and Gratchev A. Perspectives of mathematical modelling for understanding of intracellular signalling and vesicular trafficking in macrophages. Immunobiology 212 (2007) 813-825
62. Kzhyshkowska J., Workman G., Cardo-Vila M., Arap W., Pasqualini R., Gratchev A., Krusell L., Goerdt S., and Sage E.H. Novel function of alternatively activated macrophages: stabilin-1-mediated clearance of SPARC. J. Immunol. 176 (2006) 5825-5832
63. Lackman R.L., Jamieson A.M., Griffith J.M., Geuze H., and Cresswell P. Innate immune recognition triggers secretion of lysosomal enzymes by macrophages. Traffic 8 (2007) 1179-1189
64. Le Borgne R., Schmidt A., Mauxion F., Griffiths G., and Hoflack B. Binding of AP-1 Golgi adaptors to membranes requires phosphorylated cytoplasmic domains of the mannose 6-phosphate/insulin-like growth factor II receptor. J. Biol. Chem. 268 (1993) 22552-22556
65. Lemansky P., Fester I., Smolenova E., Uhlander C., and Hasilik A. The cation-independent mannose 6-phosphate receptor is involved in lysosomal delivery of serglycin. J. Leukoc. Biol. 81 (2007) 1149-1158
66. Lettau M., Schmidt H., Kabelitz D., and Janssen O. Secretory lysosomes and their cargo in T and NK cells. Immunol. Lett. 108 (2007) 10-19
67. Li A.C., and Glass C.K. The macrophage foam cell as a target for therapeutic intervention. Nat. Med. 8 (2002) 1235-1242
68. Limmon G.V., Arredouani M., McCann K.L., Corn Minor R.A., Kobzik L., and Imani F. Scavenger receptor class-A is a novel cell surface receptor for double-stranded RNA. FASEB J. 22 (2008) 159-167
69. Ling H., and Recklies A.D. The chitinase 3-like protein human cartilage glycoprotein 39 inhibits cellular responses to the inflammatory cytokines interleukin-1 and tumour necrosis factor-alpha. Biochem. J. 380 (2004) 651-659
70. Ludwig T., Munier-Lehmann H., Bauer U., Hollinshead M., Ovitt C., Lobel P., and Hoflack B. Differential sorting of lysosomal enzymes in mannose 6-phosphate receptor-deficient fibroblasts. EMBO J. 13 (1994) 3430-3437
71. Ludwig T., Ovitt C.E., Bauer U., Hollinshead M., Remmler J., Lobel P., Ruther U., and Hoflack B. Targeted disruption of the mouse cation-dependent mannose 6-phosphate receptor results in partial missorting of multiple lysosomal enzymes. EMBO J. 12 (1993) 5225-5235
72. Martens S., and McMahon H.T. Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9 (2008) 543-556
73. Mauxion F., Le Borgne R., Munier-Lehmann H., and Hoflack B. A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J. Biol. Chem. 271 (1996) 2171-2178
74. Moore K.J., El Khoury J., Medeiros L.A., Terada K., Geula C., Luster A.D., and Freeman M.W. A CD36-initiated signaling cascade mediates inflammatory effects of beta-amyloid. J. Biol. Chem. 277 (2002) 47373-47379
75. Mosig, S., Rennert, K., Krause, S., Kzhyshkowska, J., Neunubel, K., Heller, R., Funke, H., 2008. Different functions of monocyte subsets in familial hypercholesterolemia: potential function of CD14+CD16+ monocytes in detoxification of oxidized LDL. FASEB J.
76. Munier-Lehmann H., Mauxion F., Bauer U., Lobel P., and Hoflack B. Re-expression of the mannose 6-phosphate receptors in receptor-deficient fibroblasts. Complementary function of the two mannose 6-phosphate receptors in lysosomal enzyme targeting. J. Biol. Chem. 271 (1996) 15166-15174
77. Murphy J.E., Vohra R.S., Dunn S., Holloway Z.G., Monaco A.P., Homer-Vanniasinkam S., Walker J.H., and Ponnambalam S. Oxidised LDL internalisation by the LOX-1 scavenger receptor is dependent on a novel cytoplasmic motif and is regulated by dynamin-2. J. Cell Sci. 121 (2008) 2136-2147
78. Nakanishi H. Microglial functions and proteases. Mol. Neurobiol. 27 (2003) 163-176
79. Nakanishi H. Neuronal and microglial cathepsins in aging and age-related diseases. Ageing Res. Rev. 2 (2003) 367-381
80. Nickel W. The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur. J. Biochem. 270 (2003) 2109-2119
81. Nolan C.M., Kyle J.W., Watanabe H., and Sly W.S. Binding of insulin-like growth factor II (IGF-II) by human cation-independent mannose 6-phosphate receptor/IGF-II receptor expressed in receptor-deficient mouse L cells. Cell Regul. 1 (1990) 197-213
82. Nunes I., Shapiro R.L., and Rifkin D.B. Characterization of latent TGF-beta activation by murine peritoneal macrophages. J. Immunol. 155 (1995) 1450-1459
83. Orsel J.G., Sincock P.M., Krise J.P., and Pfeffer S.R. Recognition of the 300-kDa mannose 6-phosphate receptor cytoplasmic domain by 47-kDa tail-interacting protein. Proc. Natl. Acad. Sci. USA 97 (2000) 9047-9051
84. Philippidis P., Mason J.C., Evans B.J., Nadra I., Taylor K.M., Haskard D.O., and Landis R.C. Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ. Res. 94 (2004) 119-126
85. Platt N., and Gordon S. Is the class A macrophage scavenger receptor (SR-A) multifunctional? - The mouse's tale. J. Clin. Invest. 108 (2001) 649-654
86. Pluddemann A., Mukhopadhyay S., and Gordon S. The interaction of macrophage receptors with bacterial ligands. Expert. Rev. Mol. Med. 8 (2006) 1-25
87. Pluddemann A., Neyen C., and Gordon S. Macrophage scavenger receptors and host-derived ligands. Methods 43 (2007) 207-217
88. Pohlmann R., Boeker M.W., and von Figura K. The two mannose 6-phosphate receptors transport distinct complements of lysosomal proteins. J. Biol. Chem. 270 (1995) 27311-27318
89. Politz O., Gratchev A., McCourt P.A., Schledzewski K., Guillot P., Johansson S., Svineng G., Franke P., Kannicht C., Kzhyshkowska J., Longati P., Velten F.W., Johansson S., and Goerdt S. Stabilin-1 and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues. Biochem. J. 362 (2002) 155-164
90. Pols, M.S., Klumperman, J., 2008. Trafficking and function of the tetraspanin CD63. Exp. Cell Res.
91. Prevo R., Banerji S., Ni J., and Jackson D.G. Rapid plasma membrane-endosomal trafficking of the lymph node sinus and high endothelial venule scavenger receptor/homing receptor stabilin-1 (FEEL-1/CLEVER-1). J. Biol. Chem. 279 (2004) 52580-52592
92. Puertollano R., Aguilar R.C., Gorshkova I., Crouch R.J., and Bonifacino J.S. Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292 (2001) 1712-1716
93. Purchio A.F., Cooper J.A., Brunner A.M., Lioubin M.N., Gentry L.E., Kovacina K.S., Roth R.A., and Marquardt H. Identification of mannose 6-phosphate in two asparagine-linked sugar chains of recombinant transforming growth factor-beta 1 precursor. J. Biol. Chem. 263 (1988) 14211-14215
94. Rahaman S.O., Lennon D.J., Febbraio M., Podrez E.A., Hazen S.L., and Silverstein R.L. A CD36-dependent signaling cascade is necessary for macrophage foam cell formation. Cell Metab. 4 (2006) 211-221
95. Recklies A.D., White C., and Ling H. The chitinase 3-like protein human cartilage glycoprotein 39 (HC-gp39) stimulates proliferation of human connective-tissue cells and activates both extracellular signal-regulated kinase- and protein kinase B-mediated signalling pathways. Biochem. J. 365 (2002) 119-126
96. Renkema G.H., Boot R.G., Au F.L., Donker-Koopman W.E., Strijland A., Muijsers A.O., Hrebicek M., and Aerts J.M. Chitotriosidase, a chitinase, and the 39-kDa human cartilage glycoprotein, a chitin-binding lectin, are homologues of family 18 glycosyl hydrolases secreted by human macrophages. Eur. J. Biochem. 251 (1998) 504-509
97. Renkema G.H., Boot R.G., Strijland A., Donker-Koopman W.E., van den B.M., Muijsers A.O., and Aerts J.M. Synthesis, sorting, and processing into distinct isoforms of human macrophage chitotriosidase. Eur. J. Biochem. 244 (1997) 279-285
98. Rizo J., and Rosenmund C. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15 (2008) 665-674
99. Roggero C.M., Tomes C.N., De Blas G.A., Castillo J., Michaut M.A., Fukuda M., and Mayorga L.S. Protein kinase C-mediated phosphorylation of the two polybasic regions of synaptotagmin VI regulates their function in acrosomal exocytosis. Dev. Biol. 285 (2005) 422-435
100. Rojas R., Kametaka S., Haft C.R., and Bonifacino J.S. Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol. Cell Biol. 27 (2007) 1112-1124
101. Ross J.A., and Auger M.J. The biology of the macrophage. In: Burke B., and Lewis C.E. (Eds). The Macrophage (2002), Oxford University Press, Oxford 1-72
102. Sakamoto M., Miyamoto K., Wu Z., and Nakanishi H. Possible involvement of cathepsin B released by microglia in methylmercury-induced cerebellar pathological changes in the adult rat. Neurosci. Lett. 442 (2008) 292-296
103. Sakata M., Masuko-Hongo K., Tsuruha J., Sekine T., Nakamura H., Takigawa M., Nishioka K., and Kato T. YKL-39, a human cartilage-related protein, induces arthritis in mice. Clin. Exp. Rheumatol. 20 (2002) 343-350
104. Schmitz F., Bresciani R., Hartmann H., and Braulke T. Effect of insulin-like growth factor II on uptake of arylsulfatase A by cultured rat hepatocytes and Kupffer cells. J. Hepatol. 22 (1995) 356-363
105. Scott G.K., Fei H., Thomas L., Medigeshi G.R., and Thomas G. A PACS-1, GGA3 and CK2 complex regulates CI-MPR trafficking. EMBO J. 25 (2006) 4423-4435
106. Seaman M.N. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165 (2004) 111-122
107. Sekine T., Masuko-Hongo K., Matsui T., Asahara H., Takigawa M., Nishioka K., and Kato T. Recognition of YKL-39, a human cartilage related protein, as a target antigen in patients with rheumatoid arthritis. Ann. Rheum. Dis. 60 (2001) 49-54
108. Sleat D.E., and Lobel P. Ligand binding specificities of the two mannose 6-phosphate receptors. J. Biol. Chem. 272 (1997) 731-738
109. Sohar I., Sleat D., Gong L.C., Ludwig T., and Lobel P. Mouse mutants lacking the cation-independent mannose 6-phosphate/insulin-like growth factor II receptor are impaired in lysosomal enzyme transport: comparison of cation-independent and cation-dependent mannose 6-phosphate receptor-deficient mice. Biochem. J. 330 Part 2 (1998) 903-908
110. Stein M., Zijderhand-Bleekemolen J.E., Geuze H., Hasilik A., and von Figura K. Mr 46,000 mannose 6-phosphate specific receptor: its role in targeting of lysosomal enzymes. EMBO J. 6 (1987) 2677-2681
111. Stinchcombe J.C., and Griffiths G.M. Regulated secretion from hemopoietic cells. J. Cell Biol. 147 (1999) 1-6
112. Stinchcombe J.C., and Griffiths G.M. Normal and abnormal secretion by haemopoietic cells. Immunology 103 (2001) 10-16
113. Stockli J., Honing S., and Rohrer J. The acidic cluster of the CK2 site of the cation-dependent mannose 6-phosphate receptor (CD-MPR) but not its phosphorylation is required for GGA1 and AP-1 binding. J. Biol. Chem. 279 (2004) 23542-23549
114. Storch S., and Braulke T. Multiple C-terminal motifs of the 46-kDa mannose 6-phosphate receptor tail contribute to efficient binding of medium chains of AP-2 and AP-3. J. Biol. Chem. 276 (2001) 4298-4303
115. Sudhof T.C., and Rizo J. Synaptotagmins: C2-domain proteins that regulate membrane traffic. Neuron 17 (1996) 379-388
116. Sundler R. Lysosomal and cytosolic pH as regulators of exocytosis in mouse macrophages. Acta Physiol. Scand. 161 (1997) 553-556
117. Tong P.Y., Gregory W., and Kornfeld S. Ligand interactions of the cation-independent mannose 6-phosphate receptor. The stoichiometry of mannose 6-phosphate binding. J. Biol. Chem. 264 (1989) 7962-7969
118. Tong P.Y., and Kornfeld S. Ligand interactions of the cation-dependent mannose 6-phosphate receptor. Comparison with the cation-independent mannose 6-phosphate receptor. J. Biol. Chem. 264 (1989) 7970-7975
119. Traub L.M., and Kornfeld S. The trans-Golgi network: a late secretory sorting station. Curr. Opin. Cell Biol. 9 (1997) 527-533
120. Tsuruha J., Masuko-Hongo K., Kato T., Sakata M., Nakamura H., Sekine T., Takigawa M., and Nishioka K. Autoimmunity against YKL-39, a human cartilage derived protein, in patients with osteoarthritis. J. Rheumatol. 29 (2002) 1459-1466
121. Ugocsai P., Barlage S., Dada A., and Schmitz G. Regulation of surface CD163 expression and cellular effects of receptor mediated hemoglobin-haptoglobin uptake on human monocytes and macrophages. Cytometry A 69 (2006) 203-205
122. Waguri S., Dewitte F., Le Borgne R., Rouille Y., Uchiyama Y., Dubremetz J.F., and Hoflack B. Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol. Biol. Cell 14 (2003) 142-155
123. Yan Q., and Sage E.H. SPARC, a matricellular glycoprotein with important biological functions. J. Histochem. Cytochem. 47 (1999) 1495-1506
124. Zhao H., Ito Y., Chappel J., Andrews N.W., Teitelbaum S.L., and Ross F.P. Synaptotagmin VII regulates bone remodeling by modulating osteoclast and osteoblast secretion. Dev. Cell 14 (2008) 914-925
125. Zhu Y., Doray B., Poussu A., Lehto V.P., and Kornfeld S. Binding of GGA2 to the lysosomal enzyme sorting motif of the mannose 6-phosphate receptor. Science 292 (2001) 1716-1718