Luteinizing hormone plasmid therapy results in long-lasting high circulating lh and increased sperm production in european sea bass (Dicentrarchus labrax)

Biology of Reproduction

Volumn 88, Issue 2, 2013, Pages

  Mazón, María José ^a   Zanuy, Silvia ^a   Muñoz, Iciar ^a   Carrillo, Manuel ^a   Gómez, Ana ^a  

^a CSIC   (Spain)

Author keywords

Gonadotropin; Somatic gene transfer; Spermiation; Teleosts

Indexed keywords

LUTEINIZING HORMONE; PLASMID DNA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROPORATION; EUROPEAN SEA BASS; GENE TRANSFER; IN VIVO STUDY; LUTEINIZING HORMONE BLOOD LEVEL; LUTEINIZING HORMONE RELEASE; MALE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; SPERMATOGENESIS; SPERMATOZOON DENSITY;

ANIMALS; BASS; DNA; GENETIC THERAPY; INJECTIONS, INTRAMUSCULAR; LUTEINIZING HORMONE; MALE; MODELS, ANIMAL; MUSCLE, SKELETAL; PLASMIDS; REPRODUCTIVE PHYSIOLOGICAL PHENOMENA; SPERMATOGENESIS;

DICENTRARCHUS LABRAX; SERRANIDAE; TELEOSTEI;

EID: 84877073372     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.102640     Document Type: Article

References (62)

1. Adams T, Boime I. The expanding role of recombinant gonadotropins in assisted reproduction. Reprod Dom Anim 2008; 43:186-192.
2. Sethuraman N, Stadheim TA. Challenges in therapeutic glycoprotein production. Curr Opin Biotech 2006; 17:341-346.
3. Tripathy SK, Svensson EC, Black BH, Goldwasser E, Margalith M, Hobart PM, Leiden JM. Long-term expression of erythropoietin in the systemic circulation of mice after intramuscular injection of a plasmid DNA vector. Proc Natl Acad Sci U S A 1996; 93:10876-10880.
4. Ratanamart J, Shaw J. Plasmid-mediated muscle-targeted gene therapy for circulating therapeutic protein replacement: a tale of the tortoise and the hare? Curr Gene Ther 2006; 6:93-110.
5. Tonheim TC, Bøgwald J, Dalmo RA. What happens to the DNA vaccine in fish? A review of current knowledge. Fish Shellfish Immunol 2008; 25:1-18.
6. Wolff JA, Malone RW, Williams P, Chong W, Acsadi G, Jani A, Felgner PL. Direct gene transfer into mouse muscle in vivo. Science 1990; 247:1465-1468.
7. Escoffre J, Teissié J, Rols M. Gene transfer: how can the biological barriers be overcome? J Membr Biol 2010; 236:61-74.
8. Miyazaki S, Miyazaki JI. In vivo DNA electrotransfer into muscle. Develop Growth Differ 2008; 50:479-483.
9. Kay MA. State-of-the-art gene-based therapies: the road ahead. Nat Rev Genet 2011; 12:316-328.
10. Raper SE, Chirmule N, Lee FS, Wivel NA, Bagg A, Gao GP, Wilson JM, Batshaw ML. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol Genet Metab 2003; 80:148-158.
11. Niidome T, Huang L. Gene therapy progress and prospects: nonviral vectors. Gene Ther 2002; 9:1647-1652.
12. Lucas ML, Heller R. Immunomodulation by electrically enhanced delivery of plasmid DNA encoding IL-12 to murine skeletal muscle. Mol Ther 2001; 3:47-53.
13. Vilquin JT, Kennel PF, Paturneau-Jouas M, Chapdelaine P, Biossel N, Delaere P, Tremblay JP, Scherman D, Fiszman MY, Schwartz K. Electrotransfer of naked DNA in the skeletal muscles of animal models of muscular dystrophies. Gene Ther 2001; 8:1097-1107.
14. Lesbordes J-C, Bordet T, Haase G, Castelnau-Ptakhine L, Rouhani S, Gilgenkrantz H, Kahn A. In vivo electrotransfer of the cardiotrophin-1 gene into skeletal muscle slows down progression of motor neuron degeneration in pmn mice. Hum Mol Genet 2002; 11:1615-1625.
15. Terada Y, Tanaka H, Okado T, Inoshita S, Kuwahara M, Akiba T, Sasaki S, Marumo F. Efficient and ligand-dependent regulated erythropoietin production by naked DNA injection and in vivo electroporation. Am J Kidney Dis 2001; 38:S50-S53.
16. Yasui A, Oda K, Usunomiya H, Kakudo K, Suzuki T, Yoshida T, Park HM, Fukazawa K, Muramatsu T. Elevated gastrin secretion by in vivo gene electroporation in skeletal muscle. Int J Mol Med 2001; 8:489-494.
17. Fewell JG, MacLaughlin F, Mehta V, Gondo M, Nicol F, Wilson E, Smith LC. Gene therapy for the treatment of hemophilia B using PINC- formulated plasmid delivered to muscle with electroporation. Mol Ther 2001; 3:574-583.
18. Bettan M, Emmauel F, Darteil R, Caillaud JM, Soubrier F, Delaere P, Branelec D, Mahfoudi A, Duverger N, Scherman D. High level protein secretion into blood circulation after electric pulse-mediated gene transfer into skeletal muscle. Mol Ther 2000; 2:204-210.
19. Rizzuto G, Cappelletti M, Mennuni C, Wiznerowicz M, Demartis A, Maione D, Ciliberto G, Monica NL, Fattori E. Gene electrotransfer results in a high-level transduction of rat skeletal muscle and corrects anemia of renal failure. Hum Gene Ther 2000; 11:1891-1900.
20. Fattori E, Cappelletti M, Zampaglione I, Mennuni C, Calvaruso F, Arcuri M, Rizzuto G, Costa P, Perretta G, Ciliberto G, La Monica N. Gene electro-transfer of an improved erythropoietin plasmid in mice and non-human primates. J Gene Med 2005; 7:228-236.
21. Anwer K, Shi M, French MF, Muller SR, Chen W, Liu Q, Proctor BL, Wang J, Mumper RJ, Singhal A, Rolland AP, Alila HW. Systemic effect of human growth hormone after intramuscular injection of a single dose of a muscle-specific gene medicine. Hum Gene Ther 1998; 9:659-670.
22. Xie QF, Wu CX, Meng QY, Li N. Ghrelin and truncated ghrelin variant plasmid vectors administration into skeletal muscle augments long-term growth in rats. Domest Anim Endocrinol 2004; 27:155-164.
23. Abai AM, Hobart PM, Barnhart KM. Insulin delivery with plasmid DNA. Hum Gene Ther 1999; 10:2637-2649.
24. Shaw J, Delday M, Hart A, Docherty H, Maltin C, Docherty K. Secretion of bioactive human insulin following plasmid-mediated gene transfer to non-neuroendocrine cell lines, primary cultures and rat skeletal muscle in vivo. J Endocrinol 2002; 172:653-672.
25. Kurath G. Biotechnology and DNA vaccines for aquatic animals. Rev Sci Tech 2008; 27:175-196.
26. Lorenzen N, Cupit PM, Einer-Jensen K, Lorenzen E, Ahrens P, Secombes CJ, Cunningham C. Immunoprophylaxis in fish by injection of mouse antibody genes. Nat Biotechnol 2000; 18:1177-1180.
27. Anderson ED, Mourich D, Leong JA. Gene expression in rainbow trout (Oncorhynchus mykiss) following intramuscular injection of DNA. Mol Mar Biol Biotech 1996; 5:105-113.
28. Tan J, Chan WK. Efficient gene transfer into zebrafish skeletal muscle by intramuscular injection of plasmid DNA. Mol Mar Biol Biotechnol 1997; 6:98-109.
29. Gomez-Chiarri M, Chiaverini LA. Evaluation of eukaryotic promoters for the construction of DNA vaccines for aquaculture. Genet Anal 1999; 15:121-124.
30. Dijkstra J, Okamoto H, Ototake M, Nakanishi T. Luciferase expression 2 years after DNA injection in glass catfish (Kryptopterus bicirrhus). Fish Shellfish Immunol 2001; 11:199-202.
31. Verri T, Ingrosso L, Chiloiro R, Danieli A, Zonno V, Alifano P, Romano N, Scapigliati G, Vilella S, Storelli C. Assessment of DNA vaccine potential for gilthead sea bream (Sparus aurata) by intramuscular injection of a reporter gene. Fish Shellfish Immunol 2003; 15:283-295.
32. Andersen D, Krummen L. Recombinant protein expression for therapeutic applications. Curr Opin Biotechnol 2002; 13:117-123.
33. Molés G, Zanuy S, Muñoz I, Crespo B, Martínez I, Mañanós E, Gómez A. Receptor specificity and functional comparison of recombinant sea bass (Dicentrarchus labrax) gonadotropins (Fsh and Lh) produced in different host systems. Biol Reprod 2011; 84:1171-1181.
34. Friedenreich H, Schartl M. Transient expression directed by homologous and heterologous promoter and enhancer sequences in fish cells. Nucleic Acids Res 1990; 18:3299-3305.
35. Schatz S, Kerschbaumer R, Gerstenbauer G, Kral M, Dorner F, Cheiflinger F. Higher expression of Fab antibody fragments in a CHO cell line at reduced temperature. Biotechnol Bioeng 2003; 84:433-438.
36. Carrillo M, Zanuy S, Prat F, Cerdá J, Mañanós E, Bromage N. Sea bass (Dicentrarchus labrax). In: Bromage N, Roberts R (eds.), Broodstock Management and Egg and Larval Quality. London: Blackwell Science; 1995:138-168.
37. Sorbera LA, Mylonas C, Zanyu S, Carrillo M, Zohar J. Sustained administration of GnRHa increases milt volume without altering sperm counts in the sea bass. J Exp Zool 1996; 276:361-368.
38. Rainis S, Mylonas CC, Kyriakou Y, Divanach P. Enhancement of spermiation in European sea bass (Dicentrarchus labrax) at the end of the reproductive season using GnRHa implants. Aquaculture 2003; 219:873-890.
39. Mateos J, Mañanós E, Swanson P, Carrillo M, Zanuy S. Purification of luteinizing hormone (LH) in the sea bass (Dicentrarchus labrax) and development of a specific immunoassay. Ciencias Marinas 2006; 32:271-283.
40. Rodríguez L, Begtashi I, Zanyu S, Carrillo M. Long-term exposure to continuous light inhibits precocity in European male sea bass (Dicentrarchus labrax, L.): hormonal aspects. Gen Comp Endocrinol 2005; 140:116-125.
41. Fauvel C, Savoye O, Dreanno C, Cosson J, Suquet M. Characteristics of sperm of captive seabass in relation to its fertilization potential. J Fish Biol 1999; 54:356-369.
42. Hansen E, Fernandes K, Goldspink G, Butterworth P, Umeda PK, Chang KC. Strong expression of foreign genes following direct injection into fish muscle. FEBS Letters 1991; 290:73-76.
43. Rocha A, Zanuy S, Carrillo M, Gómez A. Seasonal changes in gonadal expression of gonadotropin receptors, steroidogenic acute regulatory protein and steroidogenic enzymes in the European sea bass. Gen Comp Endocrinol 2009; 162:265-275.
44. Mañanós E, Carrillo M, Sorbera LA, Mylonas C, Asturiano JF, Bayarri MJ, Zohar J, Zanyu S. Luteinizing hormone and sexual steroid plasma levels after treatment of European sea bass with sustained-release delivery systems for gonadotropin-releasing hormone analogue. J Fish Biol 2002; 60:328-339.
45. Schulz RW, de França LR, Lareyre JJ, LeGac F, Chiarini-Garcia H, Nobrega RH, Miura T. Spermatogenesis in fish. Gen Comp Endocrinol 2010; 165:390-411.
46. Molés G, Gómez A, Carrillo M, Rocha A, Mylonas CC, Zanuy S. Determination of fsh quantity and bioactivity during sex differentiation and oogenesis in European sea bass. Biol Reprod 2011; 85(4):848-857.
47. Tawk M, Tull D, Torrente Y, Vriz S, Paulin D. High-efficiency gene transfer into adult fish: a new tool to study fin regeneration. Genesis 2002; 32:27-31.
48. Rambabu K, Narayana Rao S, Rao N. Efficient expression of transgenes in adult zebrafish by electroporation. BMC Biotech 2005; 5:29.
49. Lin S-B, Fan T-W, Wu J-L, Hui C-F, Chen J-Y. Immune response and inhibition of bacterial growth by electrotransfer of plasmid DNA containing the antimicrobial peptide, epinecidin-1, into zebrafish muscle. Fish Shellfish Immunol 2009; 26:451-458.
50. Trollet C, Scherman D, Bigey P. Delivery of DNA into mouse for treating systemic diseases: advantages and challenges. In: Li S (ed.), Electroporation Protocols. Preclinical and Clinical Gene Medicine, vol. 423. Totowa, NJ: Humana Press; 2008:199-214.
51. Vicat J, Boisseau S, Jourdes P. Muscle transfection by electroporation with high-voltage and short-pulse currents provides high-level and long-lasting gene expression. Hum Gene Ther 2000; 11:909-916.
52. Levy MY, Barron LG, Meyer KB, Szoka FC Jr. Characterization of plasmid DNA transfer into mouse skeletal muscle: evaluation of uptake mechanism, expression and secretion of gene products into blood. Gene Ther 1995; 3:201-211.
53. Draghia-Akli R, Fiorotto ML. A new plasmid-mediated approach to supplement somatotropin production in pigs. J Anim Sci 2004; 82: E264-E269.
54. Klinman DM, Conover J, Leiden JM, Rosenberg AS, Sechler JMG. Safe and effective regulation of hematocrit by gene gun administration of an erythropoietin-encoding DNA plasmid. Hum Gene Ther 1999; 10:659-665.
55. Gothelf A, Hojman P, Gehl J. Therapeutic levels of erythropoietin (EPO) achieved after gene electrotransfer to skin in mice. Gene Ther 2010; 17:1077-1084.
56. Miao CH, Ohashi K, Patijn GA, Meuse L, Ye X, Thompson AR, Kay MA. Inclusion of the hepatic locus control region, an intron, and untranslated region increases and stabilizes hepatic factor IX gene expression in vivo but not in vitro. Mol Ther 2000; 1:522-532.
57. Chen ZY, Yant SR, He CY, Meuse L, Shen S, Kay MA. Linear DNAs concatemerize in vivo and result in sustained transgene expression in mouse liver. Mol Ther 2001; 3:403-410.
58. Swanson P. Salmon gonadotropins: reconciling old and new ideas. In: Scott A, Sumpter JP, Kime DE, Rolfe M (eds.), Proceedings of the Fourth International Symposium on Reproductive Physiology of Fish, vol. 91. Sheffield, United Kingdom: University of Sheffield Press; 1991:2-7.
59. Nagahama Y. Endocrine regulation of gametogenesis in fish. Int J Dev Biol 1994; 38:217-229.
60. Borg B. Androgens in teleost fishes. Comp Biochem Physiol Part C Pharmacol Toxicol Endocrinol 1994; 109:219-245.
61. Levavi-Sivan B, Bogerd J, Mañanós EL, Gómez A, Lareyre JJ. Perspectives on fish gonadotropins and their receptors. Gen Comp Endocrinol 2010; 165:412-437.
62. Faurez F, Dory D, Le Moigne V, Gravier R, Jestin A. Biosafety of DNA vaccines: new generation of DNA vectors and current knowledge on the fate of plasmid after injection. Vaccine 2010; 28:3888-3895.