• 1
    Naz RK, Gupta SK, Gupta JC, Vyas HK, Talwar GP: Recent advances in contraceptive vaccine development: a mini-review. Hum Reprod 2005; 20:32713283.
  • 2
    Gupta SK, Bansal P: Vaccines for immunological control of fertility. Reprod Med Biol 2010; 9:6171.
  • 3
    Oonk HB, Turkstra JA, Schaaper WM, Erkens JH, Schuitemaker-de Weerd MH, van Nes A, Verheijden JH, Meloen RH: New GnRH-like peptide construct to optimize efficient immunocastration of male pigs by immunocontraception of GnRH. Vaccine 1998; 16:10741082.
  • 4
    Miller LA, Gionfriddo JP, Fagerstone KA, Ryan JC, Killian GJ: The single-shot GnRH immunocontraceptive vaccine (GonaCon) in white-tailed deer: comparison of several GnRH preparations. Am J Reprod Immunol 2008; 60:214223.
  • 5
    Walker J, Ghosh S, Pagnon J, Colantoni C, Newbold A, Zeng W, Jackson DC: Totally synthetic peptide-based immunocontraceptive vaccines show activity in dogs of different breeds. Vaccine 2007; 25:71117119.
  • 6
    Yoder CA, Miller LA: Effect of GonaConTM vaccine on black-tailed prairie dogs: immune response and health effects. Vaccine 2010; 29:233239.
  • 7
    Jung MJ, Moon YC, Cho IH, Yeh JY, Kin SE, Chang WS, Park SY, Song CS, Kim HY, Park KK, McOrist S, Choi IS, Lee JB: Induction of castration by immunization of male dogs with recombinant gonadotropin-releasing hormone (GnRH)-canine distemper virus (CDV) T helper cell epitope p35. J Vet Sci 2005; 6:2124.
  • 8
    Levy JK, Miller LA, Crawford PC, Ritchey JW, Ross MK, Fagerstone KA: GnRH immunocontraception of male cats. Theriogenology 2004; 62:11161130.
  • 9
    Talwar GP, Singh O, Pal R, Chatterjee N, Sahai P, Dhall K, Kaur J, Das SK, Suri S, Buckshee K, Saraya L, Saxena BN: A vaccine that prevents pregnancy in women. Proc Natl Acad Sci USA 1994; 91:85328536.
  • 10
    Primakoff P, Lathrop W, Wollman L, Cowan A, Myles D: Fully effective contraception in male and female guinea pigs immunized with the sperm protein PH-20. Nature 1988; 335:543546.
  • 11
    Lea IA, Van Lierop MJ, Widgren EE, Grootenhuis A, Wen Y, van Duin M, O’Rand MG: A chimeric sperm peptide induces antibodies and strain-specific reversible infertility in mice. Biol Reprod 1998; 59:527536.
  • 12
    Zhu X, Naz RK: Fertilization antigen-1: cDNA cloning, testis-specific expression and immunocontraceptive effects. Proc Natl Acad Sci USA 1997; 94:47044709.
  • 13
    O’Rand MG, Widgren EE, Sivashanmugam P, Richardson RT, Hall SH, French FS, vandeVoort CA, Ramachandra SG, Ramesh V, Jagannadha Rao A: Reversible immunocontraception in male monkeys immunized with eppin. Science 2004; 306:11891190.
  • 14
    Naz RK, Chauhan SC: Human sperm-specific peptide vaccine that causes long-term reversible contraception. Biol Reprod 2002; 67:674680.
  • 15
    Wang M, Lv Z, Shi J, Hu Y, Xu C: Immunocontraceptive potential of the Ig-like domain of Izumo. Mol Reprod Dev 2009; 76:794801.
  • 16
    Sacco AG, Yurewicz EC, Subramanian MG: Effect of varying dosage and adjuvants on antibody response in squirrel monkeys (Saimiri sciureus) immunized with the porcine zona pellucida Mr = 55,000 glycoprotein (ZP3). Am J Reprod Immunol 1989; 21:18.
  • 17
    Bagavant H, Thillai-Koothan P, Sharma MG, Talwar GP, Gupta SK: Antifertility effects of porcine zona pellucida-3 immunization using permissible adjuvants in female bonnet monkeys (Macaca radiata): reversibility, effect on follicular development and hormonal profiles. J Reprod Fertil 1994; 102:1725.
  • 18
    Paterson M, Wilson MR, Morris KD, van Duin M, Aitken RJ: Evaluation of the contraceptive potential of recombinant human ZP3 and human ZP3 peptides in a primate model: their safety and efficacy. Am J Reprod Immunol 1998; 40:198209.
  • 19
    Govind CK, Srivastava N, Gupta SK: Evaluation of the immunocontraceptive potential of Escherichia coli-expressed recombinant non-human primate zona pellucida glycoproteins in homologous animal model. Vaccine 2002; 21:7888.
  • 20
    Lou Y, Ang J, Thai H, McElveen F, Tung KS: A zona pellucida-3 peptide vaccine induces antibodies and reversible infertility without ovarian pathology. J Immunol 1995; 155:27152720.
  • 21
    Meslin FX, Fishbein DB, Matter HC: Rationale and prospects for rabies elimination in developing countries. Curr Top Microbiol Immunol 1994; 187:126.
  • 22
    Knobel DL, Cleaveland S, Coleman PG, Fevre EM, Meltzer MI, Miranda ME, Shaw A, Zinsstag J, Meslon FX: Re-evaluating the burden of rabies in Africa and Asia. Bull World Health Org 2005; 83:360368.
  • 23
    Reece JF: Rabies in India: an ABC approach to combating the disease in street dogs. Vet Rec 2007; 161:292293.
  • 24
    Sudarshan MK, Madhusudana SN, Mahendra BJ, Rao NS, Ashwath Narayana DH, Abdul Rahman S, Meslin FX, Lobo D, Ravikumar K, Gangaboraiah B: Assessing the burden of human rabies in India: result of a national multi-center epidemiological survey. Int J Infect Dis 2007; 11:2935.
  • 25
    McDougall K, Hay MA, Goodrowe KL, Gartley CJ, King WA: Changes in the number of follicles and of oocytes in ovaries of prepubertal, peripubertal and mature bitches. J Reprod Fertil Suppl 1997; 51:2531.
  • 26
    Tsutsui T: Gamete physiology and timing of ovulation and fertilization in dogs. J Reprod Fertil Suppl 1989; 39:269275.
  • 27
    Gupta SK, Bansal P, Ganguly A, Bhandari B, Chakrabarty K: Human zona pellucida glycoproteins: functional relevance during fertilization. J Reprod Immunol 2009; 83:5055.
  • 28
    Harris JD, Hibler DW, Fontenot GK, Hsu KT, Yurewicz EC, Sacco AG: Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: the ZPA, ZPB and ZPC gene families. DNA Seq 1994; 4:361393.
  • 29
    Goudet G, Mugnier S, Callebaut I, Monget P: Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol Reprod 2008; 78:796806.
  • 30
    Bleil JD, Wassarman PM: Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocytes zona pellucida. Dev Biol 1980; 76:185202.
  • 31
    Lefievre L, Conner SJ, Salpakar A, Olufowobi O, Ashton P, Pavlovic B, Lenton W, Afnan M, Brewis IA, Monk M, Hughes DC, Barratt CL: Four zona pellucida glucoproteins are expressed in the human. Hum Reprod 2004; 19:15801586.
  • 32
    Sacco AG, Yurewicz EC, Subramanian MG, DeMayo FJ: Zona pellucida composition: species cross reactivity and contraceptive potential of the antiserum to a purified pig zona antigen (PPZA). Biol Reprod 1981; 25:9971008.
  • 33
    Mahi-Brown CA, Huang TT Jr, Yanagimachi R: Infertility in bitches induced by active immunization with porcine zonae pellucidae. J Exp Zool 1982; 222:8995.
  • 34
    Yurewicz EC, Sacco AG, Subramanian MG: Structural characterization of the Mr = 55,00 antigen (ZP3) of porcine oocyte zona pellucida. Purification and characterization of alpha–and beta–glycoproteins following digestion of lactosaminoglycan with endo–beta–galactosidase. J Biol Chem 1987; 262:564571.
  • 35
    Mahi-Brown CA, Yanagimachi R, Hoffman JC, Huang TT Jr: Fertility control in the bitch by active immunization with porcine zonae pellucidae: use of different adjuvants and patterns of estradiol and progesterone levels in estrous cycles. Biol Reprod 1985; 32:761772.
  • 36
    Mahi-Brown CA, Yanagimachi R, Nelson ML, Yanagimachi H, Palumbo N: Ovarian histopathology of bitches immunized with porcine zonae pellucidae. Am J Reprod Immunol Microbiol 1988; 18:94103.
  • 37
    Santhanam R, Panda AK, Kumar VS, Gupta SK: Dog zona pellucida glycoprotein-3 (ZP3): expression in Escherichia coli and immunological characterization. Protein Expr Purif 1998; 12:331339.
  • 38
    Srivastava N, Santhanam R, Sheela P, Mukund S, Thakral SS, Malik BS, Gupta SK: Evaluation of the immunocontraceptive potential of Escherichia coli-expressed recombinant dog ZP2 and ZP3 in a homologous animal model. Reproduction 2002; 123:847857.
  • 39
    Elin RJ, Wolff SM, McAdam KP, Chedid L, Audibert F, Bernard C, Oberling F: Properties of reference Escherichia coli endotoxin and its phthalylated derivative in humans. J Infect Dis 1981; 144:329336.
  • 40
    Sad S, Gupta HM, Talwar GP, Raghupathy R: Carrier-induced suppression of the antibody response to a ‘self’ hapten. Immunology 1991; 74:223227.
  • 41
    Ho PC, Mutch DA, Winkel KD, Saul AJ, Jones GL, Doran TJ, Rzepcyk CM: Identification of two promiscuous T-cell epitopes from tetanus toxin. Eur J Immunol 1990; 20:477483.
  • 42
    Lairmore MD, DiGeorge AM, Conrad SF, Trevino AV, Lal RB, Kaumaya PT: Human T-lymphotropic virus type 1 peptides in chimeric and multivalent constructs with ‘promiscuous’ T-cell epitopes enhance immunogenicity and overcome genetic restriction. J Virol 1995; 69:60776089.
  • 43
    O’Hern PA, Liang ZG, Bambra CS, Goldberg E: Colinear synthesis of an antigen-specific B-cell epitope with a ‘promiscuous’ tetanus toxin T-cell epitope: a synthetic peptide immunocontraceptive. Vaccine 1997; 16:17611766.
  • 44
    Kirkpatrick JF, Liu IKM, Turner JW Jr: Remotely-delivered immunocontraception in feral horses. Wildl Soc Bull 1990; 18:326330.
  • 45
    McShea WJ, Monfort SL, Hakim S, Kirkpatrick JF, Liu IKM, Turner JW, Chassy L, Munson L: Immunocontraceptive efficacy and the impact of contraception on the reproductive behaviors of white-tailed deer. J Wildl Manage 1997; 61:560569.
  • 46
    Fayrer-Hosken RA, Grobler D, Van Altena JJ, Bertschinger HJ, Kirkpatrick JF: Immunocontraception of African elephants. Nature 2000; 407:149.
  • 47
    Kitchener AL, Kay DJ, Walters B, Menkhorst P, McCartney CA, Buist JA, Mate KE, Rodger JC: The immune response and fertility of koalas (Phascolarctos cinereus) immunized with porcine zonae pellucidae or recombinant brushtail possum ZP3 protein. J Reprod Immunol 2009; 82:4047.
  • 48
    Brown RG, Bowen WD, Eddington JD, Kimmins WC, Mezei M, Parsons JL, Pohajdak B: Evidence for long-lasting single administration contraceptive vaccine in grey seals. J Reprod Immunol 1997; 35:4351.
  • 49
    Kirkpatrick JF, Turner A: Reversibility of action and safety during pregnancy of immunization against porcine zona pellucida in wild mares (Equus caballus). Reprod Suppl 2002; 60:197202.
  • 50
    Kirkpatrick JF, Turner A: Absence of effects from immunocontraception on seasonal birth patterns and foal survival among barrier island wild horses. J Appl Anim Welf Sci 2003; 6:301308.
  • 51
    Curtis PD, Richmond ME, Miller LA, Quimby FW: Pathophysiology of white-tailed deer vaccinated with porcine zona pellucida immunocontraceptive. Vaccine 2007; 25:46234630.
  • 52
    Kitchener AL, Harman A, Kay DJ, McCartney CA, Mate KE, Rodger JC: Immunocontraception of Eastern Grey kangaroos (Macropus giganteus) with recombinant brushtail possum (Trichosurus vulpecula) ZP3 protein. J Reprod Immunol 2009; 79:156162.
  • 53
    Cui X, Duckworth JA, Molinia FC, Cowan PE: Identification and evaluation of an infertility-associated ZP3 epitope from the marsupial brushtail possum (Trichosurus vulpecula). Vaccine 2010; 28:14991505.
  • 54
    Koyama K: Gamete immunology: infertility and contraception. Reprod Immunol Biol 2009; 24:117.
  • 55
    Afzalpurkar A, Shibahara H, Hasegawa A, Koyama K, Gupta SK: Immunoreactivity and in vitro effect on human sperm-egg binding of antibodies against peptides corresponding to bonnet monkey zona pellucida-3 glycoprotein. Hum Reprod 1997; 12:26642670.
  • 56
    Sivapurapu N, Hasegawa A, Gahlay GK, Koyama K, Gupta SK: Efficacy of antibodies against a chimeric synthetic peptide encompassing epitopes of bonnet monkey (Macaca radiata) zona pellucida-1 and zona pellucida-3 glycoproteins to inhibit in vitro human sperm-egg binding. Mol Reprod Dev 2005; 70:247254.
  • 57
    Sivapurapu N, Upadhyay A, Hasegawa A, Koyama K, Gupta SK: Efficacy of antibodies against Escherichia coli expressed chimeric recombinant protein encompassing multiple epitopes of zona pellucida glycoproteins to inhibit in vitro human sperm-egg binding. Mol Reprod Dev 2003; 65:309317.
  • 58
    Lea IA, Widgren EE, O’Rand MG: Analysis of recombinant mouse zona pellucida protein 2 (ZP2) constructs for immunocontraception. Vaccine 2002; 20:15151523.
  • 59
    Hardy CM, Clydesdale G, Mobbs KJ: Development of mouse-specific contraceptive vaccines: infertility in mice immunized with peptide and polyepitope antigens. Reproduction 2004; 128:395407.
  • 60
    Hardy CM, Beaton S, Hinds LA: Immunocontraception in mice using repeated, multi-antigen peptides: immunization with purified recombinant antigens. Mol Reprod Dev 2008; 75:126135.
  • 61
    Cleland JL: Single-administration vaccines: controlled-release technology to mimic repeated immunizations. Trends Biotechnol 1999; 17:2529.
  • 62
    Kanchan V, Panda AK: Interactions of antigen-loaded polylactide particles with macrophages and their correlation with the immune response. Biomaterials 2007; 28:53445357.
  • 63
    Kanchan V, Katare YK, Panda AK: Memory antibody response from antigen loaded polymer particles and the effect of antigen release kinetics. Biomaterials 2009; 30:47634776.
  • 64
    Grgacic EV, Anderson DA: Virus-like particles: passport to immune recognition. Methods 2006; 40:6065.
  • 65
    Jagadish MN, Edwards SJ, Hayden MB, Grusovin J, Vandenberg K, Schoofs P, Hamilton RC, Shukla DD, Kalnins H, McNamara M, Haynes J, Nisbet IT, Ward CW, Pye D: Chimeric potyvirus-like particles as vaccine carriers. Intervirology 1996; 39:8592.
  • 66
    Choudhary S, Kakkar V, Suman P, Chakrabarti K, Vrati S, Gupta SK: Immunogenicity of zona pellucida glycoprotein-3 and spermatozoa VLP(12) peptides presented on Johnson grass mosaic virus-like particles. Vaccine 2009; 27:29482953.
  • 67
    Walcher P, Cui X, Arrow JA, Scobie S, Molinia FC, Cowan PE, Lubitz W, Duckworth JA: Bacterial ghosts as a delivery system for zona pellucida-2 fertility control vaccines for brushtail possums (Trichosurus vulpecula). Vaccine 2008; 26:68326838.
  • 68
    Zhang X, Lou YH, Koopman M, Doggett T, Tung KS, Curtiss R 3rd: Antibody responses and infertility in mice following oral immunization with attenuated Salmonella typhimurium expressing recombinant murine ZP3. Biol Reprod 1997; 56:3341.
  • 69
    Jackson RJ, Maguire DJ, Hinds LA, Ramshaw IA: Infertiltiy in mice induced by a recombinant ectromelia virus expressing mouse zona pellucida glycoprotein-3. Biol Reprod 1998; 58:152159.
  • 70
    O’Leary S, Lloyd ML, Shellam GR, Robertson SA: Immunization with recombinant murine cytomegalovirus expressing murine zona pellucida 3 causes permanent infertility in BALB/c mice due to follicle depletion and ovulation failure. Biol Reprod 2008; 79:849860.
  • 71
    Gu W, Holland M, Janssens P, Seamark R, Kerr P: Immune response in rabbit ovaries following infection of a recombinant myxoma virus expressing rabbit zona pellucida protein B. Virology 2004; 318:516523.
  • 72
    Mackenzie SM, McLaughlin EA, Perkins HD, French N, Sutherland T, Jackson RJ, Inglis B, Müller WJ, van Leeuwen BH, Robinson AJ, Kerr PJ: Immunocontraceptive effects on female rabbits infected with recombinant myxoma virus expressing rabbit ZP2 or ZP3. Biol Reprod 2006; 74:511521.
  • 73
    Leitner WW, Ying H, Restifo NP: DNA and RNA-based vaccines: principles, progress and prospects. Vaccine 1999; 18:765777.
  • 74
    Xiang RL, Zhou F, Yang Y, Peng JP: Construction of the plasmid pCMV4-rZPC’ DNA vaccine and analysis of its contraceptive potential. Biol Reprod 2003; 68:15181524.
  • 75
    Li J, Jin H, Zhang A, Li Y, Wang B, Zhang F: Enhanced contraceptive response by co-immunization of DNA and protein vaccines encoding the mouse zona pellucida 3 with minimal oophoritis in mouse ovary. J Gene Med 2007; 9:10951103.
  • 76
    Choudhary S, Ganguly A, Chakrabarti K, Sharma RK, Gupta SK: DNA vaccine encoding chimeric protein encompassing epitopes of human ZP3 and ZP4: immunogenicity and characterization of antibodies. J Reprod Immunol 2009; 79:137147.
  • 77
    Rath A, Batra D, Kaur R, Vrati S, Gupta SK: Characterization of immune response in mice to plasmid DNA encoding dog zona pellucida glycoprotein-3. Vaccine 2003; 21:19131923.