Homologous and heterologous carboxyl terminal peptide (CTP) linker sequences enhance the secretion of bioactive single-chain bovine LH analogs

Experimental and Clinical Endocrinology and Diabetes

Volumn 114, Issue 3, 2006, Pages 95-104

  Nakav, S ^a   Dantes, A ^b   Pen, S ^c   Chadna Mohanty, P ^d   Braw Tal, R ^c   Amsterdam, A ^b   Grotjan, H E ^d   Ben Menahem, David ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c VOLCANI CENTER   (Israel)

^d UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Bovine LH; Cryptic CTP; Linker; Recombinant; Single chain gonadotropins

Indexed keywords

CHORIONIC GONADOTROPIN BETA SUBUNIT; GLYCAN DERIVATIVE; GLYCOSYLATED PROTEIN; LUTEINIZING HORMONE; MUCIN; PEPTIDE; PROGESTERONE; RECOMBINANT HORMONE; STEROID;

ALPHA CHAIN; ANIMAL CELL; ARTICLE; BETA CHAIN; CARBOXY TERMINAL SEQUENCE; CHIMERA; CHO CELL; CONTROLLED STUDY; COW; DRUG ACTIVITY; GENE MUTATION; GENETIC ENGINEERING; GENETIC TRANSFECTION; GRANULOSA CELL; HORMONE RELEASE; HORSE; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CATTLE; CHO CELLS; CHORIONIC GONADOTROPIN; CRICETINAE; FEMALE; GLYCOSYLATION; GRANULOSA CELLS; HUMANS; LUTEINIZING HORMONE; MOLECULAR SEQUENCE DATA; PROTEIN ENGINEERING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; TRANSFECTION; VARIATION (GENETICS);

EID: 33646444733     PISSN: 09477349     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2005-865926     Document Type: Article

References (50)

1. Ben-Menahem D. Single chain variants of the glycoprotein hormones and their receptors as tools to study receptor activation and for analogue design. J Neuroendocrinol 2004; 16: 171-177
2. Ben-Menahem D, Boime I. Converting heterodimeric gonadotropins to genetically linked single chains: New approaches to structure activity relationships and analogue design. Trends Endocrinol Metab 1996; 7: 100-105
3. Ben-Menahem D, Kudo M, Pixley MR, Sato A, Suganuma M, Perlas E, Hsueh AJW, Boime I. The biological action of single chain choriogonadotropin is not dependent on the individual disulfide bonds of the β subunit. J Biol Chem 1997; 272: 6827-6830
4. Birken S, Maydelman Y, Gawinowicz MA, Pound A, Liu Y, Hartee AS. Isolation and characterization of human pituitary chorionic gonadotropin. Endocrinology 1996; 147: 1402-1411
5. Birken S, Yershova O, Myers RV, Bernard MP, Moyle W. Analysis of human choriogonadotropin core 2 o-glycan isoforms. Mol Cell Endocrinol 2003; 204: 21-30
6. Boime I, Ben-Menahem D, Olijve W. Studies of recombinant gonadotropins: interaction of basic sciences and therapeutics. In: Fauser BCJM, Rutherford AJ, Strauss JF, Van Streiteghem A (eds). Molecular Biology in Reproductive Medicine. New York, London: Parthenon Publishing, 1999: 147-164
7. Bousfield GR, Liu WK, Sugino H, Ward DN. Structural studies on equine glycoprotein hormones. Amino acid sequence of equine lutropin beta-subunit. J Biol Chem 1987; 262: 8610-8620
8. Boussif O, Lezouale'h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, Behr JP. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci USA 1995; 92: 7297-7301
9. Chopineau M, Stewart F, Allen WR. Cloning and analysis of the cDNA encoding the horse and donkey luteinizing hormone beta-subunits Gene 1995; 28: 253-256
10. Dirnberger D, Steinkellner H, Abdennebi L, Remy JJ, van de Wiel D. Secretion of biologically active glycoforms of bovine follicle stimulating hormone in plants. Eur J Biochem 2001; 268: 4570-4579
11. Fares FA, Suganuma N, Nishimori K, LaPolt PS, Hsueh AJ, Boime I. Design of a long-acting follitropin agonist by fusing the C-terminal sequence of the chorionic gonadotropin β subunit to the follitropin β subunit. Proc Natl Acad Sci USA 1992; 89: 4304-4308
12. Fares FA, Yamabe S, Ben-Menahem D, Pixley M, Hsueh AJ, Boime I. Conversion of thyrotropin heterodimer to a biologically active single-chain. Endocrinology 1998; 139: 2459-2464
13. Fiddes JC, Goodman HM. The cDNA for the beta-subunit of human chorionic gonadotropin suggest evolution of a gene by readthrough into the 3′-untranslated region. Nature 1980; 286: 684-687
14. Fidler AE, Lin JS, Lun S, Ng Chie W, Western A, Stent V, McNatty KP. Production of biologically active tethered ovine FSHβα by the methylotrophic yeast Pichia pastoris. J Mol Endocrinol 2003; 30: 213-225
15. Fritz TA, Hurley JH, Trinh LB, Shiloach J, Tabak LA. The beginnings of mucin biosynthesis: the crystal structure of UDP-GalNAc:polypeptide alpha-N-acetylgalactosaminyltransferase-T1. Proc Natl Acad Sci USA 2004; 101: 15,307-15,312
16. Furuhashi M, Shikone T, Fares FA, Sugahara T, Hsueh AJ, Boime I. Fusing the carboxy-terminal peptide of the chorionic gonadotropin (CG) beta-subunit to the common alpha-subunit: retention of O-linked glycosylation and enhanced in vivo bioactivity of chimeric human CG. Mol Endocrinol 1995; 9: 54-63
17. Galet C, Le Bourhis CM, Chopineau M, Le Griec G, Perrin A, Magallon T, Attal J, Viglietta C, Houdebine LM, Guillou F. Expression of a single βα chain protein of equine LH/CG in milk of transgenic rabbits and its biological activity. Mol Cell Endocrinol 2001; 174: 31-40
18. Garcia-Campayo V, Sato A, Hirsch B, Sugahara T, Muyan M, Hsueh AJ, Boime I. Design of stable biologically active recombinant lutropin analogs. Nat Biotechnol 1997; 15: 663-667
19. Garcia-Campayo V, Boime I. Novel recombinant gonadotropins. Trends Endocrinol Metab 2001; 12: 72-77
20. Garcia-Campayo V, Kumar TR, Boime I. Thyrotropin, follitropin and chorionic gonadotropin expressed as a single multifunctional unit reveal remarkable permissiveness in receptor-ligand interactions. Endocrinology 2002; 143: 3773-3778
21. Grossmann M, Wong R, Szkudlinski MW, Weintraub BD. Human thyroid stimulating hormone (hTSH) subunit gene fusion produces hTSH with increased stability and serum half-life and compensates for mutagenesis-induced defects in subunit association. J Biol Chem 1997; 272: 21312-21316
22. Heikoop JC, van Beuningen-de Vaan NMM, van den Boogart P, Grootenhuis PD. Evaluation of subunit truncation and the nature of the spacer for single chain human gonadotropins. Eur J Biochem 1997; 245: 656-662
23. Hill HD Jr, Schwyzer M, Steinman, HM, Hill RL. Ovine submaxillary mucin. Primary structure and peptide substrates of UDP-N-acetylgalactosamine:mucin transferase. J Biol Chem 1977; 252: 3799-3804
24. Jackson AM, Berger P, Pixley M, Klein C, Hsueh AJ, Boime I. The biological action of choriogonadotropin is not dependent on the complete native quaternary interactions between the subunits. Mol Endocrinol 1999; 13: 2175-2188
25. Kaetzel DM, Virgin JB, Clay CM, Nilson JH. Disruption of N-linked glycosylation of bovine luteinizing hormone β-subunit by site-directed mutagenesis dramatically increases its intracellular stability but does not affect biological activity of the secreted heterodimer. Mol Endocrinol 1989; 3: 1765-1774
26. Kanda M, Jablonka-Shariff A, Sato A, Pixley MR, Bos E, Hiro'oka T, Ben-Menahem D, Boime I. Genetic fusion of an alpha-subunit gene to the follicle stimulating hormone and chorionic gonatrophin-beta subunit genes: production of a bifunctional protein. Mol Endocrinol 1999; 13: 1873-1881
27. Kasuto H, Levavi-Sivan B. Production of biologically active tethered tilapia LHβα by the methylotrophic yeast Pichia pastoris. Gen Comp Endocrinol 2005; 140: 222-232
28. Keren-Tal I, Dantes A, Sprengel R, Amsterdam A. Establishment of steroidogenic granulosa cell lines expressing follicle stimulating hormone receptors. Mol Cell Endocrinol 1993; 95: R1-R10
29. Klein J, Lobel L, Pollak S, Lustbader B, Ogden RT, Sauer MV, Lustbader JW. Development and characterization of a long-acting recombinant hFSH agonist. Hum Reprod 2003; 18: 50-56
30. Krichevsky A, Birken S, O'Connor J, Acevedo HF, Bikel K, Lustbader J, Hartree A, Canfield RE. Development, characterization and application of monoclonal antibodies to the native and synthetic beta COOH-terminal portion of human chorionic gonadotropin (hCG) that distinguish between the native and desialylated forms of hCG. Endocrinology 1994; 134: 1139-1145
31. Mutayoba BM, Meyer HHD, Schams D, Schallenger E. Development of a sensitive enzyme immunoassay for LH determination in bovine plasma using the streptoavidin-biotin technique. Acta Endocrinol 1990; 122: 227-232
32. Muyan M, Ruddon RW, Norton SE, Boime I, Bedows E. Dissociation of early folding events from assembly of the human lutropin beta-subunit. Mol Endocrinol 1998; 12: 1640-1649
33. Nakav S, Jablonka-Shariff A, Kaner S, Chadna-Mohanty P, Grotjan HE, Ben-Menahem D. The LHbeta gene of several mammals embeds a carboxyl-terminal peptide-like sequence revealing a critical role for mucin oligosaccharides in the evolution of lutropin to chorionic gonadotropin in the animal phyla. J Biol Chem 2005; 280: 16,676-16,684
34. Narayan P, Wu C, Puett D. Functional expression of yoked human chorionic gonadotropin in baculovirus-infected insect cells. Mol Endocrinol 1995; 9: 1720-1726
35. Narayan P, Gray J, Puett D. A biologically active single chain human chorionic gonadotropin analog with altered receptor binding properties. Endocrinology 2000; 141: 67-71
36. Peng KC, Puett D, Brewer JM. Homodimer formation by the individual subunits of bovine lutropin as determined by sedimentation equilibrium. J Mol Endocrinol 1997; 18: 259-265
37. Pierce JG, Parsons TF. Glycoprotein hormones: structure and function. Annu Rev Biochem 1981; 50: 465-495
38. Puett D, Wu C, Narayan P. The tie that binds: design of biologically active single chain human chorionic gonadotropins and a gonadotropin-receptor complex using protein engineering. Biol Reprod 1998; 58: 1337-1342
39. Risma K, Clay CM, Nett TM, Wagner T, Yan J, Nilson JH. Targeted overexpression of luteinizing hormone in transgenic mice leads to infertility, polycystic ovaries, and ovarian tumors. Proc Natl Acad Sci USA 1995; 92: 1322-1326
40. Sairam MR. Role of carbohydrates in glycoprotein hormone signal transduction. FASEB J 1989; 3: 1915-1926
41. Sato A, Perlas E, Ben-Menahem D, Kudo M, Pixley MR, Furuhashi M, Hsueh AJ, Boime I. Cystine knot of the gonadotropin alpha subunit is critical for intracellular behavior but not for in vitro biological activity. J Biol Chem 1997; 272: 18098-18103
42. Sen Gupta C, Dighe RR. Biological activity of single chain gonadotropin, hCGalphabeta, is decreased upon deletion of five carboxyl terminal amino acids of the alpha subunit without affecting its receptor binding. J Mol Endocrinol 2000; 24: 157-164
43. Sherman GB, Wolfe MW, Farmeric TA, Clay CM, Threadgill DS, Sharp DC, Nilson JH. A single gene encodes the β-subunits of equine luteinizing hormone and chorionic gonadotropin. Mol Endocrinol 1992; 6: 951-959
44. Sugahara T, Pixley MR, Minami S, Perlas E, Ben-Menahem D, Hsueh AJ, Boime I. Biosynthesis of a biologically active single peptide chain containing the human common alpha and chorionic gonadotropin beta subunits in tandem. Proc Natl Acad Sci USA 1995; 92: 2041-2045
45. Sugahara T, Sato A, Kudo M, Ben-Menahem D, Pixley MR, Hsueh AJW, Boime I. Expression of biologically active fusion genes encoding the common α subunit and the follicle-stimulating hormone β subunit: Role of a linker sequence. J Biol Chem 1996; 271: 10445-10448
46. Suganuma N, Matzuk MM, Boime I. Elimination of disulfide bonds affects assembly and secretion of the human chorionic gonadotropin β subunit. J Biol Chem 1989; 264: 19 302-19 307
47. Suh BS, Sprengel R, Keren-Tal I, Himmelhoch S, Amsterdam A. Introduction of a gonadotropin receptor expression plasmid into immortalized granulosa cells leads to reconstitution of hormone-dependent steroidogenesis. J Cell Biol 1992; 119: 439-450
48. Talmadge K, Vamvakopoulos NC, Fiddes JC. Evolution of the genes for the beta subunits of human chorionic gonadotropin and luteinizing hormone. Nature 1984; 307: 37-40
49. Ulloa-Aguirre A, Timossi C, Zdamian-Matsumura P, Dias JA. Role of glycosylation in function of follicle-stimulating hormone. Endocrine 1999; 11: 205-215
50. Xing Y, Lin W, Jiang M, Myers RV, Cao D, Bernard MP, Moyle WR. Alternatively folded choriogonadotropin analogs. Implications for hormone folding and biological activity. J Biol Chem 2001; 276: 46953-46960