Family of prohormone convertases in Lymnaea: Characterization of two alternatively spliced furin-like transcripts and cell-specific regulation of their expression

Journal of Neurobiology

Volumn 41, Issue 3, 1999, Pages 399-413

  Spijker, Sabine ^a   Smit, August B ^a   Sharp Baker, Hilary E ^b   Van Elk, René ^a   Van Kesteren, Ellen R ^a   Van Minnen, Jan ^a   Kurosky, Alexander ^c   Geraerts, Wijnand P M ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b Department of Obstetrics Gynecology   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Central nervous system; Mollusk Lymnaea stagnalis; Neuropeptide biosynthesis; Quantitative in situ hybridization; Subtilisin like prohormone convertases

Indexed keywords

AMINO ACID; COMPLEMENTARY DNA; FURIN; MESSENGER RNA; NEUROPEPTIDE;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; ENZYME REGULATION; GENE; IN SITU HYBRIDIZATION; LYMNAEA; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ALTERNATIVE SPLICING; ANIMALS; BLOTTING, NORTHERN; BRAIN CHEMISTRY; CATALYTIC DOMAIN; FURIN; GANGLIA, INVERTEBRATE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, REGULATOR; IN SITU HYBRIDIZATION; LYMNAEA; MOLECULAR SEQUENCE DATA; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SUBTILISINS;

EID: 0033571593     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(19991115)41:3<399::AID-NEU8>3.0.CO;2-Z     Document Type: Article

References (62)

1. Anderson ED, VanSlyke JK, Thulin CD, Jean F, Thomas G. 1997. Activation of the furin endoprotease is a multiple-step process: requirements for acidification and internal propeptide cleavage. EMBO J 16:1508-1518.
2. Bogerd J, Van Kesteren RE, Van Heerikhuizen H, Geraerts WPM, Veenstra J, Smit AB, Joosse J. 1993. Alternative splicing generates diversity of VD1/RPD2 alpha peptides in the central nervous system of Lymnaea stagnalis. Cell Mol Neurobiol 13:123-136.
3. Branden C, Tooze J. 1991. Introduction to protein structure. New York: Garland Publishing, p 231-246.
4. Chun JY, Korner J, Kreiner T, Scheller RH, Axel R. 1994. The function and differential sorting of a family of Aplysia prohormone processing enzymes. Neuron 12:831-844.
5. Chomzynski P, Sacchi N. 1987. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
6. Creemers JWM, Siezen RJ, Roebroek AJM, Ayoubi TAY, Huylebroeck D, Van de Ven WJM. 1993. Modulation of furin-mediated proprotein processing activity by site-directed mutagenesis. J Biol Chem 268:21826-21834.
7. Creemers JWM, Vey M, Schäfer W, Ayoubi TA, Roebroek AJM, Klenk HD, Garten W, Van de Ven WJM. 1995. Endoproteolytic cleavage of its propeptide is a prerequisite for efficient transport of furin out of the endoplasmic reticulum. J Biol Chem 270:2695-2702.
8. Creemers JWM, Usac EF, Bright NA, Van de Loo JW, Jansens E, Van de Ven WJM, Hutton JC. 1996. Identification of a transferable sorting domain for the regulated pathway in the prohormone convertase PC2. J Biol Chem 271:25284-25291.
9. De Bie I, Marcinkiewicz M, Malide D, Lazure C, Nakayama K, Bendayan M, Seidah NG. 1996. The isoforms of proprotein convertase PC5 are sorted to different subcellular compartments. J Cell Biol 135:1261-1275.
10. De Bie I, Savaria D, Roebroek AJM, Day R, Lazure C, Van de Ven WJM, Seidah NG. 1995. Processing specificity and biosynthesis of the Drosophila melanogaster convertases dfurin1, dfurin1-CRR, dfurin1-X, and dfurin2. J Biol Chem 270:1020-1028.
11. De Lange RPJ, Van Golen FA, Van Minnen J. 1997. Diversity in cell specific co-expression of four neuropeptide genes involved in control of male copulation behaviour in Lymnaea stagnalis. Neuroscience 78:289-299.
12. Dittié AS, Thomas L, Thomas G, Tooze SA. 1997. Interaction of furin in immature secretory granules from neuroendocrine cells with the AP-1 adaptor complex is modulated by casein kinase II. EMBO J 16:4859-4870.
13. Dong W, Marcinkiewicz M, Vieua D, Chrétien M, Seidah NG, Day R. 1995. Distinct mRNA expression of the highly homologous convertases PC5 and PACE4 in the rat brain and pituitary. J Neurosci 15:1778-1796.
14. Eipper BA, Stoffers DA, Mains RE. 1992. The biosynthesis of neuropeptides: peptide α-amidation. Annu Rev Neurosci 15:57-85.
15. Eng FJ, Novikova EG, Kuroki K, Ganem D, Fricker LD. 1998. gp180, a protein that binds duck hepatitis B virus particles, has metallocarboxypeptidase D-like enzymatic activity. J Biol Chem 273:8382-8388.
16. Felsenstein J. 1995. PHYLYP (Phylogeny Inference Package) version 3.57c. University of Washington, Seattle.
17. 2+-dependent serine protease. Proc Natl Acad Sci USA 86: 1434-1438.
18. Goodman LJ, Gorman CM. 1994. Autoproteolytic activation of the mouse prohormone convertase MPC1. Biochem Biophys Res Commun 201:795-804.
19. Gorham EL, Nagle GT, Smith JS, Shen H, Kurosky A. 1996. Molecular cloning of prohormone convertase 1 from the atrial gland of Aplysia. DNA Cell Biol 15:339-345.
20. Hatsuzawa K, Murakami K, Nakayama K. 1992a. Molecular and enzymatic properties of furin, a Kex2-like endoprotease involved in precursor cleavage at Arg-X-Lys/ Arg-Arg sites. J Biochem 111:296-301.
21. Hatsuzawa K, Nagahama M, Takahashi S, Takada K, Murakami K, Nakayama K. 1992b. Purification and characterization of furin, a Kex2-like processing endoprotease, produced in Chinese hamster ovary cells. J Biol Chem 267:16094-16099.
22. Hayflick JS, Wolfgang W, Forte MA, Thomas G. 1992. A unique Kex2-like endoprotease from Drosophila melanogaster is expressed in the central nervous system during early embryogenesis. J Neurosci 12:705-717.
23. Hosaka M, Nagahama M, Kim W, Watanabe T, Hatsuzawa K, Ikemizu J, Murakami K, Nakayami K. 1991. Arg-X-Lys/Arg-Arg motif as a signal for precursor cleavage catalyzed by furin within the consitutive secretory pathway. J Biol Chern 266:12127-12130.
24. Jiménez CR, Li KW, Dreisewerd K, Spijker S, Kingston R, Bateman RH, Burlingame AL, Smit AB, Van Minnen J, Geraerts WPM. 1998. Direct mass spectrometric peptide profiling and sequencing of single neurons reveals differential peptide patterns in a small neuronal network. Biochemistry 37:2070-2076.
25. Jones BG, Thomas L, Molloy SS, Thulin CD, Fry MD, Walsh KA, Thomas G. 1995. Intracellular trafficking of furin is modulated by the phosphorylation state of a casein kinase II site in its cytoplasmic tail. EMBO J 14:5869-5883.
26. Leduc R, Molloy SS, Thorne BA, Thomas G. 1992. Activation of human furin precursor processing endoprotease occurs by an intramolecular autoproteolytic cleavage. J Biol Chem 267:14304-14308.
27. Li KW, Hoek RM, Smith F, Jiménez CR, Van der Schors RC, Van Veelen PA, Chen S, Van der Greef J, Parish DC, Benjamin PR, Geraerts WPM. 1994a. Direct peptide profiling by mass spectrometry of single identified neurons reveals complex neuropeptide-processing pattern. J Biol Chem 269:30288-30292.
28. Li KW, Jiménez CR, Van Veelen PA, Geraerts WPM. 1994b. Processing and targeting of a molluscan egg-laying peptide prohormone as revealed by mass spectrometric peptide fingerprinting and peptide sequencing. Endocrinology 34:1812-1819.
29. Lipkind GM, Zhou A, Steiner DF. 1998. A model for the structure of the P domains in the subtilisin-like prohormone convertases. Proc Natl Acad Sci USA 95:7310-7315.
30. Lusson J, Vieau D, Hamelin J, Day R, Chrétien M, Seidah NG. 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.
31. Mania-Farnell BL, Botros I, Day R, Davis TP. 1996. Differential modulation of prohormone convertase mRNA by second messenger activators in two cholecystokinin-producing cell lines. Peptides 17:47-54.
32. Matthews G, Shennan KIJ, Seal AJ, Taylor NA, Colman A, Docherty K. 1994. Autocatalytic maturation of the prohormone convertase PC2. J Biol Chem 269:588-592.
33. Mbikay M, Raffin-Sanson M-L, Tadros H, Sirois F, Seidah NG, Chrétien M. 1994. Structure of the gene for the testis-specific proprotein convertase 4 and of its alternate messenger RNA isoform. Genomics 20:231-237.
34. Mizuno K, Nakamura T, Ohshima T, Tanaka S, Matsuo H. 1988. Yeast KEX2 gene encodes an endopeptidase homologous to subtilisin-like serine proteases. Biochem Biophys Res Commun 156:246-254.
35. Molloy SS, Thomas L, VanSlyke JK, Stenberg PE, Thomas G. 1994. Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J 13:18-33.
36. Nakagawa T, Hosaka M, Torii S, Watanabe T, Murakami K, Nakayama K. 1993a. Identification and functional expression of a new member of the mammalian Kex2-like processing endoprotease family: its striking structural similarity to PACE4. J Biochem 113:132-135.
37. Nakagawa T, Murakami K. Nakayama K. 1993b. Identification of an isoform with an extreme large Cys-rich region of PC6, a Kex2-like processing endoprotease. FEBS Lett 327:165-171.
38. Ohagi S, LaMendola J, Lebeau MM, Espinosa R, Takeda J, Smeekens SP, Chan SJ, Steiner DF. 1992. Identification and analysis of the gene encoding human PC2, a prohormone con vertase expressed in neuroendocrine tissues. Proc Natl Acad Sci USA 89:4977-4981.
39. Ortego J, Coca-Prados M. 1997. Molecular characterization and differential gene induction of the neuroendocrine-specific genes neurotensin, neurotensin receptor, PC1, PC2, and 7B2 in the human ocular ciliary epithelium. J Neurochem 69:1829-1339.
40. Ouimet T, Castelucci VF. 1997. Gene expression and regulation of Aplysia californica prohormone convertases aPC1B and aPC2. J Neurochem 68:1031-1040.
41. Roebroek AJM, Creemers JWM, Pauli IGL, Bogaert T, Van de Ven WJM. 1993. Generation of structural and functional diversity in furin-like proteins in Drosophila melanogaster by alternative splicing of the Dfur1 gene. EMBO J 12:1853-1870.
42. Roebroek AJM, Creemers JWM, Pauli IGL, Kurzik-Dumke U, Rentrop M, Gatef EAF, Leunissen JAM, Van de Ven WJM. 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. Roebroek AJM, Pauli IGL, Zhang Y, Van de Ven WJM. 1991. cDNA sequence of a Drosophila melanogaster gene, Dfur1, encoding a protein structurally related to the subtilisin-like proprotein processing enzyme furin. FEBS Lett 289:133-137.
44. Rouille Y, Duguay SJ, Lund K, Furuta M, Gong O, Lipkind G, Oliva AA, Chan SJ, Steiner DF. 1995. Proteolytic processing mechanisms in the biosynthesis of neuropeptides: the subtilisin-like proprotein convertases. Front Neuroendocrinol 16:322-361.
45. Sanger F, Nicklen S, Coulson AR. 1977. DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463-5467.
46. Schäfer W, Stroh A, Berghöfer S, Seler J, Vey M, Kruse M-L, Kern HF, Klenk H-D, Garten W. 1995. Two independent targeting signals in the cytoplasmic domain determine trans-Golgi network localization and endosomal trafficking of the proprotein convertase furin. EMBO J 14:2424-2435.
47. Seidah NG, Day R, Chrétien M. 1993. The family of prohormone and pro-protein convertases. Biochem Soc Trans 21:685-691.
48. Siezen RJ, Leunissen JA. 1997. Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci 6:501-523.
49. Smit AB, Spijker S, Geraerts WPM. 1992. Molluscan putative prohormone convertases: structural diversity in the central nervous system of Lymnaea stagnalis. FEBS Lett 312:213-218.
50. Smit AB, Spijker S, Nagle GT, Knock SL, Kurosky A, Geraerts WPM. 1994. Structural characterization of a Lymnaea putative endoprotease related to human furin. FEBS Lett 343:27-31.
51. Smit AB, Van Kesteren RE, Li KW, Van Minnen J, Spijker S, Van Heerikhuizen H, Geraerts WPM. 1998. Towards understanding the role of insulin in the brain: lessons from insulin-related signaling systems in the invertebrate brain. Prog Neurobiol 54:35-54.
52. Spijker S, Smit AB, Eipper BA, Malik A, Mains RE, Gerearts WPM. 1999. A molluscan peptide α-amidating enzyme precursor that generates five distinct enzymes. FASEB J 13:735-748.
53. Spijker S, Smit, AB, Martens GJM, Geraerts WPM. 1997. Identification of a molluscan homologue of the neuroendocrine polypeptide 7B2. J Biol Chem 272:4116-4120.
54. Takahashi S, Nakagawa T, Banno T, Watanabe T, Murakami K, Nakayama K. 1995a. Localization of furin to the trans-Golgi network and recycling from the cell surface involves Ser and Tyr residues within the cytoplasmic domain. J Biol Chem 270:28397-28401.
55. Takahashi S, Nakagawa T, Kasai K, Banno T, Duguay SJ, Van de Ven WJM, Murakami K, Nakayama K. 1995b. A second mutant allele of furin in the processing-incompetent cell-line, LoVo: evidence for involvement of the homo B domain in autocatalytic activation. J Biol Chem 270:26565-26569.
56. Van de Ven WJM, Voorberg J, Fontijn R, Pannekoek H, Van den Ouweland AMW, Van Duijnhoven JP, Roebroek AJM, Siezen RJ. 1990. Furin is a subtilisin-like proprotein processing enzyme in higher eukaryotes. Mol Biol Rep 14:265-275.
57. Van der Steen WJ, van der Hoven NP, Jager JC. 1969. A method for breeding and studying freshwater snails under continuous water change, with some remarks on growth and reproduction in Lymnaea stagnalis. Neth J Zool 19:131-139.
58. Von Heijne G. 1983. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14:4683-4690.
59. Voorhees P, Deignan E, Van Donselaar E, Humprey J, Marks MS, Peters PJ, Bonaficino JS. 1995. An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J 14: 4961-4975.
60. Zhou A, Mains RE. 1994. Endoproteolytic processing of proopiomelanocortin and prohormone convertases 1 and 2 in neuroendocrine cells overexpressing prohormone convertases 1 and 2. J Biol Chem 269:17440-17447.
61. Zhou A, Martin S, Lipkind G, LaMendola J, Steiner DF. 1998. Regulatory roles of the P domain of the subtilisin-like prohormone convertases. J Biol Chem 273:11107-11114.
62. Zhu X, Muller L, Mains RE, Lindberg I. 1998. Structural elements of PC2 required for interaction with the helper protein 7B2. J Biol Chem 273:1158-1164.