Recombinant expression and affinity purification of a novel epididymal human sperm-binding protein, BSPH1

Molecular Human Reproduction

Volumn 15, Issue 2, 2009, Pages 105-114

  Lefebvre, Jasmine ^a   Boileau, Guy ^a   Manjunath, Puttaswamy ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Binder of sperm (BSP) proteins; Epididymal protein; Fibronectin (Fn)2 domains; Recombinant protein expression; Thioredoxin

Indexed keywords

BINDER OF SPERM PROTEIN HOMOLOG 1; BINDING PROTEIN; FIBRONECTIN; GLUTATHIONE TRANSFERASE; LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLCHOLINE; RECOMBINANT PROTEIN; THIOREDOXIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BINDING AFFINITY; CELL INCLUSION; CONTROLLED STUDY; DISULFIDE BOND; ESCHERICHIA COLI; FERTILITY; HUMAN; HUMAN CELL; MALE; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; SPERM;

ANIMALS; BLOTTING, WESTERN; CHICKENS; CHROMATOGRAPHY, AFFINITY; EGG YOLK; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION; HUMANS; LIPOPROTEINS, LDL; LIPOSOMES; MALE; MODELS, BIOLOGICAL; PHOSPHATIDYLCHOLINES; PROTEIN BINDING; RECOMBINANT PROTEINS; SEMINAL VESICLE SECRETORY PROTEINS; SPERMATOZOA;

BOVINAE; ESCHERICHIA COLI; MAMMALIA; MURINAE;

EID: 60149095847     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gan077     Document Type: Article

References (59)

1. Austin CR. Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res (B) 1951;4:581-596.
2. Banyai L, Trexler M, Koncz S, Gyenes M, Sipos G, Patthy L. The collagen-binding site of type-II units of bovine seminal fluid protein PDC-109 and fibronectin. Eur J Biochem 1990;193:801-806.
3. Bar M, Bar-Ziv R, Scherf T, Fass D. Efficient production of a folded and functional, highly disulfide-bonded beta-helix antifreeze protein in bacteria. Protein Expr Purif 2006;48:243-252.
4. Bergeron A, Crete MH, Brindle Y, Manjunath P. Low-density lipoprotein fraction from hen's egg yolk decreases the binding of the major proteins of bovine seminal plasma to sperm and prevents lipid efflux from the sperm membrane. Biol Reprod 2004;70:708-717.
5. Bessette PH, Aslund F, Beckwith J, Georgiou G. Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm. Proc Natl Acad Sci USA 1999;96:13703-13708.
6. Chang MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 1951;168:697-698.
7. Cooper TG. Role of the epididymis in mediating changes in the male gamete during maturation. Adv Exp Med Biol 1995;377:87-101.
8. Cui T, Gao Y, Liew OW, Puah CM, Gutte B. Efficient preparation of an acyclic permutant of kalata B1 from a recombinant fusion protein with thioredoxin. J Biotechnol 2007;130:378-384.
9. de Lamirande E, Leclerc P, Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 1997;3:175-194.
10. Desnoyers L, Manjunath P. Major proteins of bovine seminal plasma exhibit novel interactions with phospholipid. J Biol Chem 1992; 267:10149-10155.
11. Dyson MR, Shadbolt SP, Vincent KJ, Perera RL, McCafferty J. Production of soluble mammalian proteins in Escherichia coli: Identification of protein features that correlate with successful expression. BMC Biotechnol 2004;4:32.
12. Fan J, Lefebvre J, Manjunath P. Bovine seminal plasma proteins and their relatives: A new expanding superfamily in mammals. Gene 2006; 375:63-74.
13. Fischer B, Sumner I, Goodenough P. Isolation, renaturation, and formation of disulfide bonds of eukaryotic proteins expressed in Escherichia coli as inclusion bodies. Biotechnol Bioeng 1992;41 3-13.
14. Hammarstrom M, Woestenenk EA, Hellgren N, Hard T, Berglund H. Effect of N-terminal solubility enhancing fusion proteins on yield of purified target protein. J Struct Funct Genomics 2006;7:1-14.
15. Hefti MH, Van Vugt-Van der Toorn CJ, Dixon R, Vervoort J. A novel purification method for histidine-tagged proteins containing a thrombin cleavage site. Anal Biochem 2001;295:180-185.
16. Huang KX, Huang QL, Wildung MR, Croteau R, Scott AI. Overproduction, in Escherichia coli, of soluble taxadiene synthase, a key enzyme in the Taxol biosynthetic pathway. Protein Expr Purif 1998; 13 90-96.
17. Jani M, Tordai H, Trexler M, Banyai L, Patthy L. Hydroxamate-based peptide inhibitors of matrix metalloprotease 2. Biochimie 2005; 87:385-392.
18. Jones R. Plasma membrane structure and remodelling during sperm maturation in the epididymis. J Reprod Fertil Suppl 1998;53 73-84.
19. Kemme M, Scheit KH. Cloning and sequence analysis of a cDNA from seminal vesicle tissue encoding the precursor of the major protein of bull semen. DNA 1988;7:595-599.
20. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.
21. Lauber T, Marx UC, Schulz A, Kreutzmann P, Rosch P, Hoffmann S. Accurate disulfide formation in Escherichia coli: Overexpression and characterization of the first domain (HF6478) of the multiple Kazal-type inhibitor LEKTI. Protein Expr Purif 2001;22:108-112.
22. LaVallie ER, DiBlasio EA, Kovacic S, Grant KL, Schendel PF, McCoy JM. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnology (NY) 1993; 11:187-193.
23. Lefebvre J, Fan J, Chevalier S, Sullivan R, Carmona E, Manjunath P. Genomic structure and tissue-specific expression of human and mouse genes encoding homologs of the major bovine seminal plasma proteins. Mol Hum Reprod 2007;13:45-53.
24. Lehmann K, Hoffmann S, Neudecker P, Suhr M, Becker WM, Rosch P. High-yield expression in Escherichia coli, purification, and characterization of properly folded major peanut allergen Ara h 2. Protein Expr Purif 2003;31:250-259.
25. Leung MY, Ho WK. Substitution of serine for non-disulphide-bond-forming cysteine in grass carp (Ctenopharygodon idellus) growth hormone improves in vitro oxidative renaturation. J Biochem Mol Biol 2006;39 150-157.
26. Liu Q, Lin J, Liu M, Tao X, Wei D, Ma X, Yang S. Large scale preparation of recombinant human parathyroid hormone 1-84 from Escherichia coli. Protein Expr Purif 2007;54:212-219.
27. Lunn CA, Kathju S, Wallace BJ, Kushner SR, Pigiet V. Amplification and purification of plasmid-encoded thioredoxin from Escherichia coli K12. J Biol Chem 1984;259:10469-10474.
28. Lusignan M-F, Bergeron A, Lazure C, Manjunath P. Induction of epididymal boar sperm capacitation by pB1 and BSP-A1/-A2 proteins, members of the BSP protein family. Biol Reprod 2007;76:424-432.
29. Manjunath P, Therien I. Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. J Reprod Immunol 2002;53:109-119.
30. Manjunath P, Sairam MR, Uma J. Purification of four gelatin-binding proteins from bovine seminal plasma by affinity chromatography. Biosci Rep 1987;7:231-238.
31. Manjunath P, Baillargeon L, Marcel YL, Seidah NG, Chrétien M, Chapdelaine A. Diversity of novel proteins in gonadal fluids. In: McKerns KW, Chrétien M (eds). Molecular Biology of Brain and Endocrine Peptidergic Systems. New York: Plenum Press, 1988, 259-273.
32. Manjunath P, Marcel YL, Uma J, Seidah NG, Chretien M, Chapdelaine A. Apolipoprotein A-I binds to a family of bovine seminal plasma proteins. J Biol Chem 1989;264:16853-16857.
33. Manjunath P, Chandonnet L, Leblond E, Desnoyers L. Major proteins of bovine seminal vesicles bind to spermatozoa. Biol Reprod 1994; 50: 27-37. [Published erratum appears in Biol Reprod 1994; 50, 977].
34. Manjunath P, Nauc V, Bergeron A, Menard M. Major proteins of bovine seminal plasma bind to the low-density lipoprotein fraction of hen's egg yolk. Biol Reprod 2002;67:1250-1258.
35. Manjunath P, Bergeron A, Lefebvre J, Fan J. Seminal plasma proteins: Functions and interaction with protective agents during semen preservation. In: Roldan ER, Gomendio M (eds). Society for Reproduction and Fertility Supplement. Nottingham: Nottingham University Press, 2007, 217-228.
36. Manjunath P, Lefebvre J, Jois PS, Wright MW. New nomenclature for mammalian BSP genes. Biol Reprod 2008. In press. Published on October 15, 2008 as DOI:10.1095/biolreprod.108.074088.
37. Markwell MA, Haas SM, Bieber LL, Tolbert NE. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 1978;87:206-210.
38. Moura-da-Silva AM, Linica A, Della-Casa MS, Kamiguti AS, Ho PL, Crampton JM, Theakston RD. Jararhagin ECD-containing disintegrin domain: expression in escherichia coli and inhibition of the platelet-collagen interaction. Arch Biochem Biophys 1999;369: 295-301.
39. Ozhogina OA, Trexler M, Banyai L, Llinas M, Patthy L. Origin of fibronectin type II (FN2) modules: Structural analyses of distantly-related members of the kringle family idey the kringle domain of neurotrypsin as a potential link between FN2 domains and kringles. Protein Sci 2001;10:2114-2122.
40. Peisley AA, Gooley PR. High-level expression of a soluble and functional fibronectin type II domain from MMP-2 in the Escherichia coli cytoplasm for solution NMR studies. Protein Expr Purif 2007; 53 124-131.
41. Porath J, Carlsson J, Olsson I, Belfrage G. Metal chelate affinity chromatography, a new approach to protein fractionation. Nature 1975;258:598-599.
42. Prinz WA, Aslund F, Holmgren A, Beckwith J. The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J Biol Chem 1997;272:15661-15667.
43. Salois D, Menard M, Paquette Y, Manjunath P. Complementary deoxyribonucleic acid cloning and tissue expression of BSP-A3 and BSP-30-kDa: Phosphatidylcholine and heparin-binding proteins of bovine seminal plasma. Biol Reprod 1999;61:288-297.
44. Sambrook J, Russel DW. Molecular Cloning. A Laboratory Manuel. New York: Cold Spring Harbor, 2001.
45. Singh SM, Panda AK. Solubilization and refolding of bacterial inclusion body proteins. J Biosci Bioeng 2005;99:303-310.
46. Smith DB, Johnson KS. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 1988;67:31-40.
47. Stewart EJ, Aslund F, Beckwith J. Disulfide bond formation in the Escherichia coli cytoplasm: An in vivo role reversal for the thioredoxins. Embo J 1998;17:5543-5550.
48. Sun Z, Lu W, Tang Y, Zhang J, Chen J, Deng H, Li X, Liu JN. Expression, purification and characterization of human urodilatin in E. coli. Protein Expr Purif 2007;55:312-318.
49. Terpe K. Overview of tag protein fusions: From molecular and biochemical fundamentals to commercial systems. Appl Microbiol Biotechnol 2003; 60:523-533.
50. Therien I, Bleau G, Manjunath P. Phosphatidylcholine-binding proteins of bovine seminal plasma modulate capacitation of spermatozoa by heparin. Biol Reprod 1995;52:1372-1379.
51. Therien I, Soubeyrand S, Manjunath P. Major proteins of bovine seminal plasma modulate sperm capacitation by high-density lipoprotein. Biol Reprod 1997;57:1080-1088.
52. Therien I, Bergeron A, Bousquet D, Manjunath P. Isolation and characterization of glycosaminoglycans from bovine follicular fluid and their effect on sperm capacitation. Mol Reprod Dev 2005;71: 97-106.
53. Tordai H, Patthy L. The gelatin-binding site of the second type-II domain of gelatinase A/MMP-2. Eur J Biochem 1999;259:513-518.
54. Vallejo LF, Rinas U. Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins. Microb Cell Fact 2004; 3:11.
55. Visconti PE, Kopf GS. Regulation of protein phosphorylation during sperm capacitation. Biol Reprod 1998;59:1-6.
56. Visconti PE, Westbrook VA, Chertihin O, Demarco I, Sleight S, Diekman AB. Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 2002;53:133-150.
57. Xiong C, Hixson PM, Mendoza LH, Smith CW. Cloning and expression of rabbit interleukin-15. Vet Immunol Immunopathol 2005;107 131-141.
58. Yuan LD, Hua ZC. Expression, purification, and characterization of a biologically active bovine enterokinase catalytic subunit in Escherichia coli. Protein Expr Purif 2002;25:300-304.
59. Zhao JH, Xu Z, Hua ZC. Expression of human cardiac-specific homeobox protein in Escherichia coli. Protein Expr Purif 2000;18 316-319.