Exploration of the extracellular space by a large-scale secretion screen in the early Xenopus embryo

International Journal of Developmental Biology

Volumn 49, Issue 7, 2005, Pages 781-796

  Pera, Edgar M ^a,b,d   Hou, Shirui ^b   Strate, Ina ^b   Wessely, Oliver ^a,c   De Robertis, Edward M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d LUND UNIVERSITY   (Sweden)

Author keywords

Gastrula; Lysosomal; Maternal; Secretion cloning; Spemann Mangold organizer

Indexed keywords

COMPLEMENTARY DNA; CYSTEINE PROTEINASE INHIBITOR; CYTOPLASM PROTEIN; EPIDERMAL GROWTH FACTOR; GROWTH FACTOR; HEME; TRANSFORMING GROWTH FACTOR ALPHA; UNCLASSIFIED DRUG; XYSTATIN;

ARTICLE; BODY FLUID; CYTOPLASM; EMBRYO; EMBRYO DEVELOPMENT; EPIDERMIS; EXTRACELLULAR SPACE; GENE EXPRESSION; GENE IDENTIFICATION; GENE LIBRARY; GENE SEQUENCE; GENETIC TRANSFECTION; LYSOSOME; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN SECRETION; PROTEIN STRUCTURE; SCREENING; SECRETION; SEQUENCE HOMOLOGY; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; EMBRYO, NONMAMMALIAN; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; GROWTH SUBSTANCES; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TIME FACTORS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 27144545798     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.052003ep     Document Type: Article

References (78)

1. ALATALO S.L., HALLEEN J.M., HENTUNEN T.A., MONKKONEN J. and VAANANEN H.K. (2000). Rapid screening method for osteoclast differentiation in vitro that measures tartrate-resistant acid phosphatase 5b activity secreted into the culture medium. Clin. Chem. 46: 1751-1754.
2. BARTZ R., BENZING C. and ULLRICH O. (2003). Reconstitution of vesicular transport to Rab11-positive recycling endosomes in vitro. Biochem. Biophys. Res. Commun. 312: 663-669.
3. BATEMAN A. and BENNETT H.P. (1998). Granulins: the structure and function of an emerging family of growth factors. J. Endocrinol. 158: 145-151.
4. BENDTSEN J.D., NIELSEN H., von HEIJNE G. and BRUNAK, S. (2004). Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340: 783-795.
5. BHANDARI V., PALFREE R.G.E. and 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.
6. BOMMER U.A. and THIELE B.J. (2004). The translationally controlled tumour protein (TCTP). Int. J. Biochem. Cell Biol. 36: 379-385.
7. BROWN W.M. and DZIEGIELEWSKA K.M. (1997). Friends and relations of the cystatin superfamily-new members and their evolution. Protein Sci. 6: 5-12.
8. BUBLITZ C. and STEAVENSON S. (1988). The pentose phosphate pathway in the endoplasmic reticulum. J. Biol. Chem. 263: 12849-12853.
9. BUKRINSKY M.I. (2002). Cyclophilins: unexpected messengers in intercellular communications. Trends Immunol. 23: 323-325.
10. CHANG B.Y., PEAVY T.R., WARDRIP N.J. and HEDRICK J.L. (2004). The Xenopus laevis cortical granule lectin: cDNA cloning, developmental expression and identification of the eglectin family of lectins. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 137: 115-129.
11. CHENG A.M., THISSE B., THISSE C. and WRIGHT C.V. (2000). The lefty-related factor Xatv acts as a feedback inhibitor of nodal signaling in mesoderm induction and L-R axis development in Xenopus. Development 127: 1049-1061.
12. CLARK H.F., GURNEY A.L., ABAYA E., BAKER K., BALDWIN D., et al. (2003). The secreted protein discovery initiative (SPDI), a large-scale effort to identify novel human secreted and transmembrane proteins: a bioinformatics assessment. Genome Res. 13: 2265-2270.
13. CLAUSEN T., SOUTHAN C. and EHRMANN M. (2002). The HtrA family of proteases: implications for protein composition and cell fate. Mol. Cell 10: 443-455.
14. COLLAVIN L. and KIRSCHNER M.W. (2003). The secreted Frizzled-related protein Sizzled functions as a negative feedback regulator of extreme ventral mesoderm. Development 130: 805-816.
15. DAFFORN T.R., DELLA M. and MILLER A.D. (2001). The molecular interactions of heat shock protein 47 (Hsp47) and their implications for collagen biosynthesis. J. Biol. Chem. 276: 49310-49319.
16. DAHMS N.M., LOBEL P. and KORNFELD S. (1989). Mannose6-phosphate receptors and lysosomal enzyme targeting. J. Biol. Chem. 264: 12115-12118.
17. DEBLANDRE G.A., WETTSTEIN D.A., KOYANO-NAKAGAWA N. and KINTNER C. (1999) A two-step mechanism generates the spacing pattern of the ciliated cells in the skin of Xenopus embryos. Development 126: 4715-4728.
18. DE ROBERTIS E.M., LARRAIN J., OELGESCHLÄGER M. and WESSELY O. (2000). The establishment of Spemann's organizer and patterning of the vertebrate embryo. Nat. Rev. Genet. 1: 171-181.
19. DE ROBERTIS E.M. and KURODA H. (2004). Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20: 285-308.
20. DOSCH R. and NIEHRS C. (2000). Requirement for anti-dorsalizing morphogenetic protein in organizer patterning. Mech. Dev. 90: 195-203.
21. ELLGAARD L. and HELENIUS A. (2003). Quality control in the endoplasmic reticulum. Nature Rev. Mol. Cell Biol. 4: 181-191.
22. GALLI A., ROURE A., ZELLER R. and DONO R. (2003). Glypican 4 modulates FGF signalling and regulates dorsoventral forebrain patterning in Xenopus embryos. Development 130: 4919-4929.
23. GHOSH S., HEVI S. and CHUCK S.L. (2004). Regulated secretion of glycosylated human ferritin from hepatocytes. Blood 103: 2369-2376.
24. HANSEN, C. S., MARION, C. D., STEELE, K., GEORGE, S. and SMITH, W. C. (1997). Direct neural induction and selective inhibition of mesoderm and epidermis inducers by Xnr3. Development 124: 483-492.
25. HASILIK A. (1992). The early and late processing of lysosomal enzymes: proteolysis and compartmentation. Experientia 48: 130-151.
26. HAURI H., APPENZELLER C., KUHN F. and NUFER O. (2000). Lectins and traffic in the secretory pathway. FEBS Letters 476: 32-37.
27. HOWARD T.L., STAUFFER D.R., DEGNIN C.R. and HOLLENBERG S.M. (2001). CHMP1 functions as a member of a newly defined family of vesicle trafficking proteins. J. Cell Sci. 114: 2395-2404.
28. HSU D.R., ECONOMIDES A.N., WANG X., EIMON P.M. and HARLAND R.M. (1998). The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol. Cell 1: 673-683.
29. ISAKSSON A. and HULTBERG B. (1995). Serum beta-hexosaminidase isoenzymes are precursor forms. Scand. J. Clin. Lab. Invest. 55: 433-440.
30. JESSOP C.E., CHAKRAVARTHI S., WATKINS R.H. and BULLEID N.J. (2004). Oxidative protein folding in the mammalian endoplasmic reticulum. Biochem. Soc. Trans. 32: 655-658.
31. KATZ A.B. and TAICHMAN L.B. (1999). A partial catalog of proteins secreted by epidermal keratinocytes in culture. J. Invest. Dermatol. 112: 818-821.
32. KLEIN R.D., GU Q., GODDARD A. and ROSENTHAL A. (1996). Selection for genes encoding secreted proteins and receptors. Proc. Natl. Acad. Sci. USA. 93: 7108-7113.
33. KUBO H., KAWANO T., TSUBUKI S., KOTANI M., KAWASAKI H. and KAWASHIMA S. (2000). Egg envelope glycoprotein gp37 as a Xenopus homolog of mammalian ZP1, based on cDNA cloning. Dev. Growth Differ. 42: 419-427.
34. KURY P., SCHAEREN-WIEMERS N. and MONARD D. (1997). Protease nexin-1 is expressed at the mouse met-/mesencephalic junction and FGF signaling regulates its promoter activity in primary met-/mesencephalic cells. Development 124: 1251-1262.
35. LARRAÍN J., BACHILLER D., LU B., AGIUS E., PICCOLO S. and DE ROBERTIS E.M. (2000). BMP-binding modules in chordin: a model for signalling regulation in the extracellular space. Development 127: 821-830.
36. LAVOIE C., MEERLOO T., LIN P. and FARQUHAR M.G. (2002). Calnuc, an EF-hand Ca(2+)-binding protein, is stored and processed in the Golgi and secreted by the constitutive-like pathway in AtT20 cells. Mol. Endocrinol. 16: 2462-2474.
37. LEYNS L., BOUWMEESTER T., KIM S.H., PICCOLO S. and DE ROBERTIS E.M. (1997). Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88: 747-756.
38. LIN X. (2004). Functions of heparan sulfate proteoglycans in cell signaling during development. Development 131: 6009-6021.
39. MAIER T., STRATER N., SCHUETTE C.G., KLINGENSTEIN R., SANDHOFF K. and SAENGER W. (2003). The X-ray crystal structure of human beta-hexosaminidase B provides new insights into Sandhoff disease. J. Mol. Biol. 328: 669-681.
40. MCNAUGHT K.S., KAPUSTIN A., JACKSON T., JENGELLEY T.A., JNOBAPTISTE R., SHASHIDHARAN P., PERL D.P., PASIK P. and OLANOW C.W. (2004). Brainstem pathology in DYT1 primary torsion dystonia. Ann. Neurol. 56: 540-547.
41. MOLONEY D.J., PANIN V.M., JOHNSTON S.H., CHEN J., SHAO L., WILSON R., WANG Y., STANLEY P., IRVINE K.D., HALTIWANGER R.S. and VOGT T.F. (2000). Fringe is a glycosyltransferase that modifies Notch. Nature 406: 369-375.
42. MOOS M. J.R., WANG S. and KRINKS M. (1995). Anti-dorsalizing morphogenetic protein is a novel TGF-beta homolog expressed in the Spemann organizer. Development 121: 4293-4301.
43. MURATA J., LEE H.Y., CLAIR T., KRUTZSCH H.C., ARESTAD A.A., SOBEL M.E., LIOTTA L.A. and STRACKE M.L. (1994). cDNA cloning of the human tumor motility-stimulating protein, autotaxin, reveals a homology with phosphodiesterases. J. Biol. Chem. 269: 30479-30484.
44. NEUFELD E.F. (1991). Lysosomal storage diseases. Ann. Rev. Biochem. 60: 257-280.
45. NIEHRS C. and MEINHARDT H. (2002). Modular feedback. Nature 417: 35-36.
46. O'BRIEN J.S., CARSON G.S., SEO H.C., HIRAIWA M. and KISHIMOTO Y. (1994). Identification of prosaposin as a neurotrophic factor. Proc. Natl. Acad. Sci. USA. 91: 9593-9596.
47. OHKAWARA B., YAMAMOTO T.S., TADA M. and UENO N. (2003). Role of glypican 4 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 130: 2129-2138.
48. OTTE S., BARNIKOL-WATANABE S., VORBRUGGEN G. and HILSCHMANN N. (1999). NUCB1, the Drosophila melanogaster homolog of the mammalian EF-hand proteins NEFA and nucleobindin. Mech. Dev. 86: 155-158.
49. PARK, H.S., KIM, M., SHIM, S. and HAN, J.K. (1998). Identification and expression study of a Xenopus homologue of prenylated SNARE gene. Biochem. Biophys. Res. Commun. 248: 235-239.
50. PATSTON P.A., CHURCH F.C. and OLSON S.T. (2004). Serpin-ligand interactions. Methods 32: 93-109.
51. PERA E.M. and DE ROBERTIS E.M. (2000). A direct screen for secreted proteins in Xenopus embryos identifies distinct activities for the Wnt antagonists Crescent and Frzb-1. Mech. Dev. 96: 183-195.
52. PERA E.M., WESSELY O., LI S.-Y. and DE ROBERTIS E.M. (2001). Neural and head induction by insulin-like growth factor signals. Dev. Cell 1: 655-665.
53. PERA E.M., KIM J.I., MARTINEZ S.L., BRECHNER M., LI S.-Y., WESSELY O. and DE ROBERTIS E.M. (2002). Isthmin is a novel secreted protein expressed as part of the Fgf-8 synexpression group in the Xenopus midbrain-hindbrain organizer. Mech. Dev. 116: 169-172.
54. PERA E.M., MARTINEZ S.L., FLANAGAN J.J., BRECHNER M., WESSELY O. and DE ROBERTIS E.M. (2003). Darmin is a novel secreted protein expressed during endoderm development in Xenopus. Gene Expr. Patterns 3: 147-152.
55. PEREZ S.E. and STELLER H. (1996). Molecular and genetic analyses of lama, an evolutionary conserved gene expressed in the precursors of the Drosophila first optic ganglion. Mech. Dev. 59: 11-27.
56. PETERS, J.M., WALSH, M.J. and FRANKE, W.W. (1990). An abundant and ubiquitous homo-oligomeric ring-shaped ATPase particle related to the putative vesicle fusion proteins Sec18p and NSF. EMBO J. 9: 1757-1767.
57. PICCOLO S., AGIUS E., LEYNS L., BHATTACHARYYA S., GRUNZ H., BOUWMEESTER T. and DE ROBERTIS E.M. (1999). The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397: 707-710.
58. RODRIGUEZ-NIEDENFÜHR M., PROLS F. and CHRIST B. (2003). Temporal and spatial protease nexin 1 expression during chick development. Gene Expr. Patterns 3: 611-614.
59. ROSA, F., SARGENT, T.D., REBBERT, M.L., MICHAELS, G.S., JAMRICH, M., GRUNZ, H., JONAS, E., WINKLES, J.A. and DAWID, I.B. (1988). Accumulation and decay of DG42 gene products follow a gradient pattern during Xenopus embryogenesis. Dev. Biol. 129: 114-123.
60. SALIC A.N., KROLL K.L., EVANS L.M. and KIRSCHNER M.W. (1997). Sizzled: a secreted Xwnt8 antagonist expressed in the ventral marginal zone of Xenopus embryos. Development 124: 4739-4748.
61. SHRIDHAR V., RIVARD S., WANG X., SHRIDHAR R., PAISLEY C., MULLINS C., BEIRNAT L., DUGAN M., SARKAR F., MILLER O.J., VAITKEVICIUS V.K. and SMITH D.I. (1997). Mutations in the arginine-rich protein gene (ARP) in pancreatic cancer. Oncogens 14: 2213-2216.
62. SILES-LUCAS M., NUNES C.P., ZAHA A. and BREIJO M. (2000). The 14-3-3 protein is secreted by the adult worm of Echinococcus granulosus. Parasite Immunol. 22: 521-528.
63. SKARNES W.C., MOSS J.E., HURTLEY S.M. and BEDDINGTON R.S. (1995). Capturing genes encoding membrane and secreted proteins important for mouse development. Proc. Natl. Acad. Sci. USA. 92: 6592-6596.
64. SPEMANN H. and MANGOLD H. (1924). Induction of embryonic primordia by implantation of organizers from a different species. Roux's Arch. Entw. Mech. 100, 599-638.
65. Reprinted and Transl. Int. J. Dev. Biol. 45: 13-38.
66. SUN H. and WOLFE J.H. (2001). Recent progress in lysosomal alpha-mannosidase and its deficiency. Exp. Mol. Med. 33: 1-7.
67. TASHIRO K., NAKAMURA T. and HONJO T. (1999). The signal sequence trap method. Methods Enzymol. 303: 479-495.
68. WESSELY O., AGIUS E., OELGESCHLÄGER M., PERA E.M. and DE ROBERTIS E.M. (2001). Neural induction in the absence of mesoderm: beta-catenin-dependent expression of secreted BMP antagonists at the blastula stage in Xenopus. Dev. Biol. 234: 161-173
69. WESSELY O., KIM J.I., GEISSERT D., TRAN U. and DE ROBERTIS E.M. (2004) Analysis of Spemann organizer formation in Xenopus embryos by cDNA macroarrays. Dev. Biol. 269: 552-566.
70. WU J.Y., WEN L., ZHANG W.J. and RAO Y. (1996). The secreted product of Xenopus gene lunatic Fringe, a vertebrate signaling molecule. Science 273: 355-358.
71. WU B.X., CHEN Y., CHEN Y., FAN J., ROHRER B., CROUCH R.K. and MA J.X. (2002). Cloning and characterization of a novel all-trans retinol short-chain dehydrogenase/reductase from the RPE. Invest Ophthalmol. Vis. Sci. 43: 3365-3372.
72. WYLIE C., KOFRON M., PAYNE C. ANDERSON R., HOSOBUCHI M., JOSEPH E. and HEASMAN J. (1996). Maternal beta-catenin establishes a 'dorsal signal' in early Xenopus embryos. Development 122: 2987-2996.
73. YAMAMOTO K., HAMADA H., SHINKAI H., KOHNO Y., KOSEKI H. and AOE T. (2003). The KDEL receptor modulates the endoplasmic reticulum stress response through mitogen-activated protein kinase signaling cascades. J. Biol. Chem. 278: 34525-34532.
74. YASUO H. and LEMAIRE P. (1999). A two-step model for the fate determination of presumptive endodermal blastomeres in Xenopus embryos. Curr. Biol. 9: 869-879.
75. YOKOTA C., KOFRON M., ZUCK M., HOUSTON D.W., ISAACS H., ASASHIMA M., WYLIE C.C. and HEASMAN J. (2003). A novel role for a nodal-related protein; Xnr3 regulates convergent extension movements via the FGF receptor. Development 130: 2199-2212.
76. YU M., HASLAM R.H. and HASLAM D.B. (2000). HEDJ, an Hsp40 co-chaperone localized to the endoplasmic reticulum of human cells. J. Biol. Chem. 275: 24984-24992.
77. ZIMMERMAN L.B., DE JESUS-ESCOBAR J.M. and HARLAND R.M. (1996). The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86: 599-606.
78. ZYLKA M.J. and REPPERT S.M. (1999). Discovery of a putative heme-binding protein family (SOUL/HBP) by two-tissue suppression subtractive hybridization and database searches. Mol. Brain Res. 74: 175-181.