A novel dominant B-cell epitope of FSHR identified by molecular docking induced specific immune response and suppressed fertility

References

• Silber SJ, Grotjan HE. Microscopic vasectomy reversal 30 years later: a summary of 4010 cases by the same surgeon. J Androl 2004;25:845–859.
   PubMedGoogle Scholar
• Patel SR, Sigman M. Comparison of outcomes of vasovasostomy performed in the convoluted and straight vas deferens. J Urol 2008;179:256–259.
   PubMed Web of Science ®Google Scholar
• Foulkes NS, Schlotter F, Pevet P, Sassone-Corsi P. Pituitary hormone FSH directs the CREM functional switch during spermatogenesis. Nature 1993;362:264–267.
   PubMed Web of Science ®Google Scholar
• Gromoll J, Simoni M, Nieschlag E. An activating mutation of the follicle-stimulating hormone receptor autonomously sustains spermatogenesis in a hypophysectomized man. J Clin Endocrinol Metab 1996;81:1367–1370.
   PubMed Web of Science ®Google Scholar
• Fritz IB, Griswold MD, Louis BG, Dorrington JH. Metabolic responses of Sertoli cells in culture to various concentrations of follicle stimulating hormone and cholera toxin. Can J Biochem 1978;56:875–879.
   PubMedGoogle Scholar
• Simoni M, Gromoll J, Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocrinol Rev 1997;18:739–773.
   PubMed Web of Science ®Google Scholar
• Dias JA, Van Roey P. Structural biology of human follitropin and its receptor. Arch Med Res 2001;32:510–519.
   PubMed Web of Science ®Google Scholar
• Kene PS, Nalavadi VC, Dighe RR, Iyer KS, Mahale SD. Identification of the structural and functional determinants of the extracellular domain of the human follicle stimulating hormone receptor. J Endocrinol 2004;182:501–508.
   PubMed Web of Science ®Google Scholar
• Kene PS, Dighe RR, Mahale SD. Delineation of regions in the extracellular domain of follicle-stimulating hormone receptor involved in hormone binding and signal transduction. Am J Reprod Immunol 2005;54:38–48.
   PubMed Web of Science ®Google Scholar
• Abdennebi L, Chun EY, Jammes H, Wei D, Remy JJ. Maintenance of sexual immaturity in male mice and bucks by immunization against N-terminal peptides of the follicle-stimulating hormone receptor. Biol Reprod 2003;68:323–327.
   PubMed Web of Science ®Google Scholar
• Mahale SD, Cavanagh J, Schmidt A, MacColl R, Dias JA. Autologous biological response modification of the gonadotropin receptor. J Biol Chem 2001;276:12410–12419.
   PubMed Web of Science ®Google Scholar
• Dattatreyamurty B, Reichert LE Jr. Functional properties of polyclonal antibodies raised against the N-terminus region (residues 9-30) of the follicle-stimulating hormone (FSH) receptor: significance of this receptor region in FSH recognition and signal transduction. Endocrinology 1993;133:1593–1601.
   PubMed Web of Science ®Google Scholar
• Lindau-Shepard B, Brumberg HA, Peterson AJ, Dias JA. Reversible immunoneutralization of human follitropin receptor. J Reprod Immunol 2001;49:1–19.
   PubMed Web of Science ®Google Scholar
• Hilbert A, Hudecz F, Mezo G, Mucsi I, Kajtar J, Kurucz I, Gergely J, Rajnavolgyi E. The influence of branched polypeptide carriers on the immunogenicity of predicted epitopes of HSV-1 glycoprotein D. Scand J Immunol 1994;40:609–617.
   PubMed Web of Science ®Google Scholar
• Fan QR, Hendrickson WA. Assembly and structural characterization of an authentic complex between human follicle stimulating hormone and a hormone-binding ectodomain of its receptor. Mol Cell Endocrinol 2007;260–262:73–82.
   PubMed Web of Science ®Google Scholar
• Panina-Bordignon P, Tan A, Termijtelen A, Demotz S, Corradin G, Lanzavecchia A. Universally immunogenic T cell epitopes: promiscuous binding to human MHC class II and promiscuous recognition by T cells. Eur J Immunol 1989;19:2237–2242.
   PubMed Web of Science ®Google Scholar
• Alexander J, Sidney J, Southwood S, Ruppert J, Oseroff C, Maewal A, Snoke K, Serra HM, Kubo RT, Sette A, et al Development of high potency universal DR-restricted helper epitopes by modification of high affinity DR-blocking peptides. Immunity 1994;1:751–761.
   PubMed Web of Science ®Google Scholar
• Moudgal NR, Sairam MR, Krishnamurthy HN, Sridhar S, Krishnamurthy H, Khan H. Immunization of male bonnet monkeys (M. radiata) with a recombinant FSH receptor preparation affects testicular function and fertility. Endocrinology 1997;138:3065–3068.
   PubMedGoogle Scholar
• Tayama K, Fujita H, Takahashi H, Nagasawa A, Yano N, Yuzawa K, Ogata A. Measuring mouse sperm parameters using a particle counter and sperm quality analyzer: a simple and inexpensive method. Reprod Toxicol 2006;22:92–101.
   Google Scholar
• Makler A. The improved ten-micrometer chamber for rapid sperm count and motility evaluation. Fertil Steril 1980;33:337–338.
   PubMed Web of Science ®Google Scholar
• Reddy PS, Pushpalatha T. Reduction of spermatogenesis and steroidogenesis in mice after fentin and fenbutatin administration. Toxicol Lett 2006;166:53–59.
   PubMed Web of Science ®Google Scholar
• Talbot P, Chacon RS. A triple-stain technique for evaluating normal acrosome reactions of human sperm. J Exp Zool 1981;215:201–208.
   PubMedGoogle Scholar
• Jeyendran RS, Van der Ven HH, Perez-Pelaez M, Crabo BG, Zaneveld LJ. Development of an assay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics. J Reprod Fertil 1984;70:219–228.
   PubMedGoogle Scholar
• Robb GW, Amann RP, Killian GJ. Daily sperm production and epididymal sperm reserves of pubertal and adult rats. J Reprod Fertil 1978;54:103–107.
   PubMedGoogle Scholar
• Chen J, Liu H, Yang J, Chou KC. Prediction of linear B-cell epitopes using amino acid pair antigenicity scale. Amino Acids 2007;33:423–428.
   PubMed Web of Science ®Google Scholar
• El-Manzalawy Y, Dobbs D, Honavar V. Predicting linear B-cell epitopes using string kernels. J Mol Recognit 2008;21:243–255.
   PubMed Web of Science ®Google Scholar
• El-Manzalawy Y, Dobbs D, Honavar V. Predicting flexible length linear B-cell epitopes. In: 7th International Conference on Computational Systems Bioinformatics, Stanford, CA; 2007. pp. 121–131.
   Google Scholar
• Miyado K, Yamada G, Yamada S, Hasuwa H, Nakamura Y, Ryu F, Suzuki K, Kosai K, Inoue K, Ogura A, et al Requirement of CD9 on the egg plasma membrane for fertilization. Science 2000;287:321–324.
   PubMed Web of Science ®Google Scholar
• Naz RK, Gupta SK, Gupta JC, Vyas HK, Talwar AG. Recent advances in contraceptive vaccine development: a mini-review. Hum Reprod 2005;20:3271–3283.
   PubMed Web of Science ®Google Scholar
• Naz RK. Contraceptive vaccines. Drugs 2005;65:593–603.
   PubMed Web of Science ®Google Scholar
• Narula A, Gu YQ, O'Donnell L, Stanton PG, Robertson DM, McLachlan RI, Bremner WJ. Variability in sperm suppression during testosterone administration to adult monkeys is related to follicle stimulating hormone suppression and not to intratesticular androgens. J Clin Endocrinol Metab 2002;87:3399–3406.
   PubMed Web of Science ®Google Scholar
• McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, de Kretser DM, Pratis K, Robertson DM. Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog Horm Res 2002;57:149–179.
   PubMedGoogle Scholar
• Dias JA, Cohen BD, Lindau-Shepard B, Nechamen CA, Peterson AJ, Schmidt A. Molecular, structural, and cellular biology of follitropin and follitropin receptor. Vitam Horm 2002;64:249–322.
   PubMed Web of Science ®Google Scholar
• Themmen APN, Huhtaniemi IT. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocrinol Rev 2000;21:551–583.
   PubMed Web of Science ®Google Scholar
• Grover A, Smith CE, Gregory M, Cyr DG, Sairam MR, Hermo L. Effects of FSH receptor deletion on epididymal tubules and sperm morphology, numbers, and motility. Mol Reprod Dev 2005;72:135–144.
   PubMed Web of Science ®Google Scholar
• Saha S, Raghava GP. BcePred: prediction of continuous B-cell epitopes in antigenic sequences using physico-chemical properties. In: Bairoch A, Apweiler R, editors. Lecture notes in computer science, Vol: 3239: Artificial immune systems (Third International Conference (ICARIS)). Berlin: Springer; 2004. 197–204.
   Google Scholar
• Smith GR, Sternberg MJ. Prediction of protein-protein interactions by docking methods. Curr Opin Struct Biol 2002;12:28–35.
   PubMed Web of Science ®Google Scholar
• Alonso H, Bliznyuk AA, Gready JE. Combining docking and molecular dynamic simulations in drug design. Med Res Rev 2006;26:531–568.
   PubMed Web of Science ®Google Scholar
• Subramanian S, Karande AA, Adiga PR. Immunocontraceptive potential of major antigenic determinants of chicken riboflavin carrier protein in the female rat. Vaccine 2000;19:1172–1179.
   PubMed Web of Science ®Google Scholar
• Earl ER, Waterston MM, Aughey E, Harvey MJ, Matschke C, Colston A, Ferro VA. Evaluation of two GnRH-I based vaccine formulations on the testes function of entire Suffolk cross ram lambs. Vaccine 2006;24:3172–3183.
   PubMed Web of Science ®Google Scholar
• Chen Z, He W, Liang Z, Yan P, He H, Tang Y, Zhang J, Shen Z, Ni B, Wu Y, Li J. Protein prime-peptide boost as a new strategy induced an Eppin dominant B-cell epitope specific immune response and suppressed fertility. Vaccine 2009;27:733–740.
   Google Scholar
• Amory JK, Bremner W. Endocrine regulation of testicular function in men: implications for contraceptive development. Mol Cell Endocrinol 2001;182:175–179.
   PubMed Web of Science ®Google Scholar
• Meduri G, Bachelot A, Cocca MP, Vasseur C, Rodien P, Kuttenn F, Touraine P, Misrahi M. Molecular pathology of the FSH receptor: new insights into FSH physiology. Mol Cell Endocrinol 2008;282:130–142.
   PubMed Web of Science ®Google Scholar
• McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, de K, Pratis K, Robertson DM. Hormonal regulation of spermatogenesis in primates and man: insights for development of the malehormonal contraceptive. J Androl 2002;23:149–162.
   PubMed Web of Science ®Google Scholar
• Rao AJ, Ramachandra SG, Ramesh V, Couture L, Abdennebi L, Salesse R, Remy JJ. Induction of infertility in adult male bonnet monkeys by immunization with phage-expressed peptides of the extracellular domain of FSH receptor. Reprod Biomed Online 2004;8:385–391.
   PubMed Web of Science ®Google Scholar