SPC4, SPC6, and the novel protease SPC7 are coexpressed with bone morphogenetic proteins at distinct sites during embryogenesis

Journal of Cell Biology

Volumn 134, Issue 1, 1996, Pages 181-191

  Constam, Daniel B ^a   Calfon, Marcella ^a   Robertson, Elizabeth J ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GROWTH FACTOR; PROTEINASE; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CATALYSIS; DNA CLEAVAGE; DNA SEQUENCE; DROSOPHILA; EMBRYO; EMBRYO CELL; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME ANALYSIS; GENE EXPRESSION; GRANULOSA CELL; IN SITU HYBRIDIZATION; MOLECULAR CLONING; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BONE MORPHOGENETIC PROTEINS; DNA PRIMERS; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; IN SITU HYBRIDIZATION; MALE; MICE; MOLECULAR SEQUENCE DATA; PROTEINS; RNA, MESSENGER; SUBTILISINS;

ANIMALIA;

EID: 0029946619     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.134.1.181     Document Type: Article

References (65)

1. Barr, P.J. 1991. Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell. 66:1-3.
2. Beaubien, G., M.K. Schafer, E. Weihe, W. Dong, M. Chretien, N.G. Seidah, and R. Day. 1995. The distinct gene expression of the pro-hormone convertases in the rat heart suggests potential substrates. Cell Tissue Res. 279:539-549.
3. Benjannet, S., N. Rondeau, R. Day, M. Chretien, and N.G. Seidah. 1991. PC1 and PC2 are proprotein convertases capable of cleaving proopiomelanocortin at distinct pairs of basic residues. Proc. Natl. Acad. Sci. USA. 88:3564-3568.
4. Bitgood, M.J., and A.P. McMahon. 1995. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172:126-138.
5. Brennan, S.O., and K. Nakayama. 1994. Cleavage of proalbumin peptides by furin reveals unexpected restrictions at the P2 and P′1 sites. FEBS Lett. 347: 80-84.
6. Breslin, M.B., I. Lindberg, S. Benjannet, J.P. Mathis, C. Lazure, and N.G. Seidah. 1993. Differential processing of proenkephalin by prohormone convertases 1(3) and 2 and furin. J. Biol. Chem. 268:27084-27093.
7. Celeste, A.J., J.A. Iannazzi, R.C. Taylor, R.M. Hewick, V. Rosen, E.A. Wang, and J.M. Wozney. 1990. Identification of transforming growth factor β family members present in bone-inductive protein purified from bovine bone. Proc. Natl. Acad. Sci. USA. 87:9843-9847.
8. Chomczinsky, P., and N. Sacchi. 1987. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction procedure. Anal. Biochem. 162:156-159.
9. Conlon, F.L., K.M. Lyons, N. Takaesu, K.S. Barth, A. Kispert, B. Herrmann, and E.J. Robertson. 1994. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development. 120: 1919-1928.
10. Creemers, J.W., P.J. Kormelink, A.J. Roebroek, K. Nakayama, and W.J. Van de Ven. 1993. Proprotein processing activity and cleavage site selectivity of the Kex2-like endoprotease PACE4. FEBS Lett. 336:65-69.
11. Dong, W., M. Marcinkiewicz, D. Vieau, M. Chretien, N.G. Seidah, and R. Day. 1995. Distinct mRNA expression of the highly homologous convertases PC5 and PACE4 in the rat brain and pituitary. J. Neurosci. 15:1778-1796.
12. Dubois, C.M., M.H. Laprise, F. Blanchette, L.E. Gentry, and R. Leduc. 1995. Processing of transforming growth factor β 1 precursor by human furin convertase. J. Biol. Chem. 270:10618-10624.
13. Dudley, A.T., K.M. Lyons, and E.J. Robertson. 1995. A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 9:2795-2807.
14. Echelard, Y., D.J. Epstein, B. St-Jacques, L. Shen, J. Mohler, J.A. McMahon, and A.P. McMahon. 1993. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 75: 1417-1430.
15. Fahrner, K., B.L. Hogan, and R.A. Flavell. 1987. Transcription of H-2 and Qa genes in embryonic and adult mice. EMBO (Eur. Mol. Biol. Organ.) J. 6: 1265-1271.
16. Ferguson, E.L., and K.V. Anderson. 1992. Localized enhancement and repression of the activity of the TGF-β family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development. 114:583-597.
17. Hayflick, J.S., W.J. Wolfgang, M.A. Forte, and G. Thomas. 1992. A unique Kex2-like endoprotease from Drosophila melanogaster is expressed in the central nervous system during early embryogenesis. J. Neurosci. 12:705-717.
18. Hecht, P.M., and K.V. Anderson. 1992. Extracellular proteases and embryonic pattern formation. Trends Cell Biol. 2:197-202.
19. Hosaka, M., K. Murakami, and K. Nakayama. 1994. PACE4 is a ubiquitous endoprotease that has similar but not identical substrate specificity to other KEX2-like processing endoproteases. Biomed. Res. 16:383-390.
20. Hosaka, M., M. Nagahama, W.S. Kim, T. Watanabe, K. Hatsuzawa, J. Ikemizu, K. Murakami, and K. Nakayama. 1991. Arg-X-Lys/Arg-Arg motif as a signal for precursor cleavage catalyzed by furin within the constitutive secretory pathway. J. Biol. Chem. 266:12127-12130.
21. Johnson, R.C., D.N. Darlington, T.A. Hand, B.T. Bloomquist, and R.E. Mains. 1994. PACE4: a subtilisin-like endoprotease prevalent in the anterior pituitary and regulated by thyroid status. Endocrinology. 135:1178-1185.
22. Jones, C.M., K.M. Lyons, and B.L.M. Hogan. 1991. Involvement of bone morphogenetic protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development. 111:531-542.
23. Jones, C.M., D. Simon-Chazottes, J.-L. Guenet, and B.L.M. Hogan. 1992. Isolation of vgr-2, a novel member of the transforming growth factor-β-related gene family. Mol. Endocrinol. 6:1961-1968.
24. Kingsley, D.M. 1994. The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8:133-146.
25. Kingsley, D.M., A.E. Bland, J.M. Grubber, P.C. Marker, L.B. Russell, N.G. Copeland, and N.A. Jenkins. 1992. The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGF β superfamily. Cell. 71:399-410.
26. Laufer, E., C.E. Nelson, R.L. Johnson, B.A. Morgan, and C. Tabin. 1994. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell. 79:993-1003.
27. Leduc, R., S.S. Molloy, B.A. Thorne, and G. Thomas. 1992. Activation of human furin precursor processing endoprotease occurs by an intramolecular autoproteolytic cleavage. J. Biol. Chem. 267:14304-14308.
28. Liem, K.F., Jr., G. Tremml, H. Roelink, and T.M. Jessell. 1995. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell. 82:969-979.
29. Lusson, J., D. Vieau, J. Hamelin, R. Day, M. Chretien, and N.G. Seidah. 1993. cDNA structure of the mouse and rat subtilisin/kexin-like PC5: a candidate proprotein convertase expressed in endocrine and nonendocrine cells. Proc. Natl. Acad. Sci. USA. 90:6691-6695.
30. Lyons, K., R. W. Pelton, and B.L.M. Hogan. 1989. Patterns of expression of murine vgr-1 and BMP-2a RNA suggest that transforming growth factor-β-like genes coordinately regulate aspects of embryonic development. Genes Dev. 3:1657-1668.
31. Lyons, K.M., B.L. Hogan, and E.J. Robertson. 1995. Colocalization of BMP7 and BMP2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50:71-83.
32. Lyons, K.M., R.W. Pelton, and B.L.M. Hogan. 1990. Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for Bone-Morphogenetic-Protein-2A (BMP2A). Development. 109:833-844.
33. Marti, E., D.A. Bumerot, R. Takada, and A.P. McMahon. 1995. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature (Lond.). 375:322-325.
34. Matthews, G., K.I. Shennan, A.J. Seal, N.A. Taylor, A. Colman, and K. Docherty. 1994. Autocatalytic maturation of the prohormone convertase PC2. J. Biol. Chem. 269:588-592.
35. Molloy, S.S., P.A. Bresnahan, S.H. Leppla, K.R. Klimpel, and G. Thomas. 1992. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J. Biol. Chem. 267:16396-16402.
36. Nakayama, K., W.S. Kim, S. Torii, M. Hosaka, T. Nakagawa, J. Ikemizu, T. Baba, and K. Murakami. 1992. Identification of the fourth member of the mammalian endoprotease family homologous to the yeast Kex2 protease. Its testis-specific expression. J. Biol. Chem. 257:5897-5900.
37. Niswander, L., S. Jeffrey, G.R. Martin, and C. Tickle. 1994. A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature (Lond.). 371:609-612.
38. Rehemtulla, A., P.J. Barr, C.J. Rhodes, and R.J. Kaufman. 1993. PACE4 is a member of the mammalian propeptidase family that has overlapping but not identical substrate specificity to PACE. Biochemistry. 32:11586-11590.
39. Rholam, M., N. Brakch, D. Germain, D.Y. Thomas, C. Fahy, H. Boussetta, G. Boileau, and P. Cohen. 1995. Role of amino acid sequences flanking dibasic cleavage sites in precursor proteolytic processing. The importance of the first residue C-terminal of the cleavage site. Eur. J Biochem. 227:707-714.
40. Roebroek, A.J., J.W. Creemers, I.G. Pauli, T. Bogaert, and W.J. Van de Ven. 1993. Generation of structural and functional diversity in furin-like proteins in Drosophila melanogaster by alternative splicing of the Dfur1 gene. EMBO (Eur. Mol. Biol. Organ.) J. 12:1853-1870.
41. Roebroek, A.J., J.A. Schalken, J.A. Leunissen, C. Onnekink, H.P. Bloemers, and W.J. Van de Ven. 1986. Evolutionary conserved close linkage of the c-fes/fps, proto-oncogene and gentic sequences encoding a receptor-like protein. EMBO (Eur. Mol. Biol. Organ.) J. 5:2137-2202.
42. Roebroek, A.J., J.W. Creemers, I.G. Pauli, U. Kurzik-Dumke, M. Rentrop, E.A. Gateff, J.A. Leunissen, and W.J. Van de Ven. 1992. Cloning and functional expression of Dfurin2, a subtilisin-like proprotein processing enzyme of Drosophila melanogaster with multiple repeats of a cysteine motif. J. Biol. Chem. 267:17208-17215.
43. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. 2nd edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Saunders, J.W., Jr. 1948. The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108:363-403.
45. Seidah, N.G., L. Gaspar, P. Mion, M. Marcinkiewicz, M. Mbikay, and M. Chretien. 1990. cDNA sequence of two distinct pituitary proteins homologous to Kex2 and furin gene products: tissue-specific mRNAs encoding candidates for pro-hormone processing proteinases. DNA Cell Biol. 9:415-424.
46. Seidah, N.G., M. Marcinkiewicz, S. Benjannet, L. Gaspar, G. Beaubien, M.G. Mattel, C. Lazure, M. Mbikay, and M. Chretien. 1991. Furin, and Kex2: distinct chromosomal localization and messenger RNA distribution in brain and pituitary compared to PC2. Mol. Endocrinol. 5:111-122.
47. Seidah, N.G., M. Chretien, and R. Day. 1994. The family of subtilisin/kexin like pro-protein and pro-hormone convertases: divergent or shared functions. Biochimie. 76:197-209.
48. Shennan, K.I., N.A. Taylor, J.L. Jermany, G. Matthews, and K. Docherty. 1995. Differences in pH optima and calcium requirements for maturation of the prohormone convertases PC2 and PC3 indicates different intracellular locations for these events. J. Biol. Chem. 270:1402-1407.
49. Shimell, M.J., E.L. Ferguson, S.R. Childs, and M.B. O'Connor. 1991. The Drosophila dorsal-ventral patterning gene tolloid is related to human hone morphogenetic protein 1. Cell. 67:469-481.
50. Steiner, D.F., S.P. Smeekens, S. Ohagi, and S.J. Chan. 1992. The new enzymology of precursor processing endoproteases. J. Biol. Chem. 267:23435-23438.
51. Storm, E.E., T.V. Huynh, N.G. Copeland, N.A. Jenkins, D.M. Kingsley, and S.-J. Lee. 1994. Limb alterations in brachypodism mice due to mutations in a new member of the TGFβ-superfamily. Nature (Lond). 368:639-642.
52. Summerbell, D. 1974. A quantitative analysis of the effect of excision of the AER from the chick limb-bud. J. Embryol. Exp. Morphol. 32:651-660.
53. Tabin, C. 1995. The initiation of the limb bud: growth factors, Hox genes, and retinoids. Cell. 80:671-674.
54. Thacker, C., K. Peters, M. Srayko, and A.M. Rose. 1995. The bli-4 locus of Caenorhabditis elegans encodes structurally distinct kex2/subtilisin-like endoproteases essential for early development and adult morphology. Genes Dev. 9:956-971.
55. Thomsen, G.H., and D.A. Melton. 1993. Processed Vg1 protein is an axial mesoderm inducer in Xenopus. Cell. 74:433-441.
56. Tsuji, A., C. Hine, K. Mori, Y. Tamai, K. Higashine, H. Nagamune, and Y. Matsuda. 1994. A novel member, PC7, of the mammalian kexin-like protease family: homology to PACE4A, its brain-specific expression and identification of isoforms. Biochem. Biophys. Res. Commun. 202:1452-1459.
57. Van de Ven, W.J., A.J. Roebroek, and H.L. Van Duijnhoven. 1993. Structure and function of eukaryotic proprotein processing enzymes of the subtilisin family of serine proteases. Crit. Rev. Oncog. 4:115-136.
58. Wang, E.A., V. Rosen, J.S. D'Alessandro, M. Bauduy, P. Cordes, T. Harada, D.I. Israel, R.M. Hewick, K.M. Kerns, P. LaPan, et al. 1990. Recombinant human bone morphogenetic protein induces bone formation. Proc. Natl. Acad. Sci. USA. 87:2220-2224.
59. Williams, T., A. Admon, B. Lüscher, and R. Tjian. 1988. Cloning and expression of AP-2, a cell type-specific transcription factor that activates inducible enhancer elements. Genes Dev. 2:1557-1569.
60. Winnier, G., M. Blessing, P.A. Labosky, and B.L.M. Hogan. 1995. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9:2105-2116.
61. Wozney, J.M., V. Rosen, A.J. Celeste, L.M. Mitsok, M.J. Whitters, R.W. Kriz, R.M. Hewick, and E.A. Wang. 1988. Novel regulators of bone formation: molecular clones and activities. Science (Wash. DC). 242:1528-1534.
62. Yamada, T., S.L. Pfaff, T. Edlund, and T.M. Jessell. 1993. Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from the notochord and floor plate. Cell. 73:673-686.
63. Yang, Y., and L. Niswander. 1995. Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: dorsal signals regulate anteroposterior patterning. Cell. 80:939-947.
64. Zheng, M., R.D. Streck, R.E. Scott, N.G. Seidah, and J.E. Pintar. 1994. The developmental expression in rat of proteases furin, PC1, PC2, and carboxypeptidase E: implications for early maturation of proteolytic processing capacity. J. Neurosci. 14:4656-4673.
65. Zhou, X., H. Sasaki, L. Lowe, B.L.M. Hogan, and M.R. Kuehn. 1993. Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature (Lond.). 361:543-547.