Induction of Protection in Mice against a Chlamydia muridarum Respiratory Challenge by a Vaccine Formulated with the Major Outer Membrane Protein in Nanolipoprotein Particles

Tifrea, Delia F.; He, Wei; Pal, Sukumar; Evans, Angela C.; Gilmore, Sean F.; Fischer, Nicholas O.; Rasley, Amy; Coleman, Matthew A.; de la Maza, Luis M.

doi:10.3390/vaccines9070755

Title: Induction of Protection in Mice against a Chlamydia muridarum Respiratory Challenge by a Vaccine Formulated with the Major Outer Membrane Protein in Nanolipoprotein Particles

Journal Article · Wed Jul 07 00:00:00 EDT 2021 · Vaccines

DOI:https://doi.org/10.3390/vaccines9070755· OSTI ID:1806351

Tifrea, Delia F.;

; Pal, Sukumar;

; Gilmore, Sean F.; Fischer, Nicholas O.; Rasley, Amy;

; de la Maza, Luis M.

Chlamydia trachomatis is a sexually transmitted bacterium that infects over 130 million individuals worldwide annually. To implement a vaccine, we developed a cell-free co-translational system to express the Chlamydia muridarum major outer membrane protein (MOMP). This approach uses a nanolipoprotein particles (tNLP) made from ApoA1 protein, amphiphilic telodendrimer and lipids that self-assemble to form 10–25 nm discs. These tNLP provide a protein-encapsulated lipid support to solubilize and fold membrane proteins. The cell-free system co-translated MOMP and ApoA1 in the presence of telodendrimer mixed with lipids. The MOMP-tNLP complex was amenable to CpG and FSL-1 adjuvant addition. To investigate the ability of MOMP-tNLP+CpG+FSL-1 to induce protection against an intranasal (i.n.) C. muridarum challenge, female mice were vaccinated intramuscularly (i.m.) or i.n. and i.m. simultaneously 4 weeks apart. Following vaccination with MOMP-tNLP+CpG+FSL-1, mice mounted significant humoral and cell-mediated immune responses. Following the i.n. challenge, mice vaccinated with MOMP-tNLP+CpG+FSL-1 i.n. + i.m. group were protected as determined by the percentage change in body weight and by the number of C. muridarum inclusion forming units (IFU) recovered from the lungs. To our knowledge, this is the first time a MOMP-based vaccine formulated in tNLP has been shown to protect against C. muridarum.

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Research Organization:: Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Institute of Allergy and Infectious Diseases (NIAID)

Grant/Contract Number:: AC52-07NA27344; R21 AI20925; U19 AI144184

OSTI ID:: 1806351

Alternate ID(s):: OSTI ID: 1815653; OSTI ID: 1836939

Report Number(s):: LLNL-JRNL-829100; VBSABP; PII: vaccines9070755

Journal Information:: Vaccines, Journal Name: Vaccines Vol. 9 Journal Issue: 7; ISSN 2076-393X

Publisher:: MDPI AGCopyright Statement

Country of Publication:: Switzerland

Language:: English

References (58)

Increased Immunoaccessibility of MOMP Epitopes in a Vaccine Formulated with Amphipols May Account for the Very Robust Protection Elicited against a Vaginal Challenge with Chlamydia muridarum Tifrea, Delia F.; Pal, Sukumar; Popot, Jean-Luc The Journal of Immunology, Vol. 192, Issue 11 https://doi.org/10.4049/jimmunol.1303392	journal	April 2014
Protection Against Chlamydia trachomatis Infection and Upper Genital Tract Pathological Changes by Vaccine-Promoted Neutralizing Antibodies Directed to the VD4 of the Major Outer Membrane Protein Olsen, Anja W.; Follmann, Frank; Erneholm, Karin Journal of Infectious Diseases, Vol. 212, Issue 6 https://doi.org/10.1093/infdis/jiv137	journal	March 2015
DNA immunization with pgp3 gene of Chlamydia trachomatis inhibits the spread of chlamydial infection from the lower to the upper genital tract in C3H/HeN mice Donati, Manuela; Sambri, Vittorio; Comanducci, Maurizio Vaccine, Vol. 21, Issue 11-12 https://doi.org/10.1016/S0264-410X(02)00631-X	journal	March 2003
Pelvic Inflammatory Disease and Fertility: A Cohort Study of 1,844 Women with Laparoscopically Verified Disease and 657 Control Women with Normal Laparoscopic Results WestrÖM, Lars; Joesoef, Riduan; Reynolds, Gladys Sexually Transmitted Diseases, Vol. 19, Issue 4 https://doi.org/10.1097/00007435-199207000-00001	journal	January 1992
Safety and immunogenicity of the chlamydia vaccine candidate CTH522 adjuvanted with CAF01 liposomes or aluminium hydroxide: a first-in-human, randomised, double-blind, placebo-controlled, phase 1 trial Abraham, Sonya; Juel, Helene B.; Bang, Peter The Lancet Infectious Diseases, Vol. 19, Issue 10 https://doi.org/10.1016/S1473-3099(19)30279-8	journal	October 2019
A new computer model for estimating the impact of vaccination protocols and its application to the study of Chlamydia trachomatis genital infections de la Maza, Michael A.; de la Maza, Luis M. Vaccine, Vol. 13, Issue 1 https://doi.org/10.1016/0264-410X(95)80022-6	journal	January 1995
A TLR2 agonist is a more effective adjuvant for a Chlamydia major outer membrane protein vaccine than ligands to other TLR and NOD receptors Cheng, Chunmei; Jain, Pooja; Bettahi, Ilham Vaccine, Vol. 29, Issue 38 https://doi.org/10.1016/j.vaccine.2011.06.105	journal	September 2011
Immunization with the Chlamydia trachomatis Mouse Pneumonitis Major Outer Membrane Protein Can Elicit a Protective Immune Response against a Genital Challenge Pal, S.; Theodor, I.; Peterson, E. M. Infection and Immunity, Vol. 69, Issue 10 https://doi.org/10.1128/IAI.69.10.6240-6247.2001	journal	October 2001
Enhancement of the protective efficacy of a Chlamydia trachomatis recombinant vaccine by combining systemic and mucosal routes for immunization Ralli-Jain, Pooja; Tifrea, Delia; Cheng, Chunmei Vaccine, Vol. 28, Issue 48 https://doi.org/10.1016/j.vaccine.2010.09.040	journal	November 2010
Update on Chlamydia trachomatis Vaccinology de la Maza, Luis M.; Zhong, Guangming; Brunham, Robert C. Clinical and Vaccine Immunology, Vol. 24, Issue 4 https://doi.org/10.1128/CVI.00543-16	journal	April 2017
Resolution of Secondary Chlamydia trachomatis Genital Tract Infection in Immune Mice with Depletion of Both CD4 ⁺ and CD8 ⁺ T cells Morrison, Sandra G.; Morrison, Richard P. Infection and Immunity, Vol. 69, Issue 4 https://doi.org/10.1128/IAI.69.4.2643-2649.2001	journal	April 2001
Vaccine adjuvants: scientific challenges and strategic initiatives Harandi, Ali M.; Davies, Gwyn; Olesen, Ole F. Expert Review of Vaccines, Vol. 8, Issue 3 https://doi.org/10.1586/14760584.8.3.293	journal	March 2009
Protection against an intranasal challenge by vaccines formulated with native and recombinant preparations of the Chlamydia trachomatis major outer membrane protein Sun, Guifeng; Pal, Sukumar; Weiland, Joseph Vaccine, Vol. 27, Issue 36 https://doi.org/10.1016/j.vaccine.2009.05.008	journal	August 2009
Mapping antigenic domains expressed by Chlamydia trachomatis major outer membrane protein genes. Baehr, W.; Zhang, Y. X.; Joseph, T. Proceedings of the National Academy of Sciences, Vol. 85, Issue 11 https://doi.org/10.1073/pnas.85.11.4000	journal	June 1988
A vaccine formulated with a combination of TLR-2 and TLR-9 adjuvants and the recombinant major outer membrane protein elicits a robust immune response and significant protection against a Chlamydia muridarum challenge Cheng, Chunmei; Pal, Sukumar; Tifrea, Delia Microbes and Infection, Vol. 16, Issue 3 https://doi.org/10.1016/j.micinf.2013.11.009	journal	March 2014
Controlling the diameter, monodispersity, and solubility of ApoA1 nanolipoprotein particles using telodendrimer chemistry: Size and Stability of NLPs He, Wei; Luo, Juntao; Bourguet, Feliza Protein Science, Vol. 22, Issue 8 https://doi.org/10.1002/pro.2292	journal	June 2013
Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis Caldwell, H. D.; Kromhout, J.; Schachter, J. Infection and Immunity, Vol. 31, Issue 3 https://doi.org/10.1128/iai.31.3.1161-1176.1981	journal	March 1981
Chlamydia trachomatisinfection in early neonatal period Numazaki, Kei; Asanuma, Hideomi; Niida, Yuichi BMC Infectious Diseases, Vol. 3, Issue 1 https://doi.org/10.1186/1471-2334-3-2	journal	April 2003
Enhancement of antigen-specific CD4+ and CD8+ T cell responses using a self-assembled biologic nanolipoprotein particle vaccine Weilhammer, Dina; Dunkle, Alexis D.; Blanchette, Craig D. Vaccine, Vol. 35, Issue 11 https://doi.org/10.1016/j.vaccine.2017.02.004	journal	March 2017
Protective Effect of Vaccine Promoted Neutralizing Antibodies against the Intracellular Pathogen Chlamydia trachomatis Olsen, Anja Weinreich; Lorenzen, Emma Kathrine; Rosenkrands, Ida Frontiers in Immunology, Vol. 8 https://doi.org/10.3389/fimmu.2017.01652	journal	December 2017
Is the Increase in Notifications of Chlamydia trachomatis Infections in Sweden the Result of Changes in Prevalence, Sampling Frequency or Diagnostic Methods? Götz, Hannelore; Lindbäck, Johan; Ripa, Torvald Scandinavian Journal of Infectious Diseases, Vol. 34, Issue 1 https://doi.org/10.1080/00365540110077001	journal	January 2002
Intranasal Vaccination with a Secreted Chlamydial Protein Enhances Resolution of Genital Chlamydia muridarum Infection, Protects against Oviduct Pathology, and Is Highly Dependent upon Endogenous Gamma Interferon Production Murthy, Ashlesh K.; Chambers, James P.; Meier, Patricia A. Infection and Immunity, Vol. 75, Issue 2 https://doi.org/10.1128/IAI.01280-06	journal	February 2007
Protective role of magnesium in the neutralization by antibodies of Chlamydia trachomatis infectivity Peterson, E. M.; Zhong, G. M.; Carlson, E. Infection and Immunity, Vol. 56, Issue 4 https://doi.org/10.1128/iai.56.4.885-891.1988	journal	April 1988
Protection of outbred mice against a vaginal challenge by a Chlamydia trachomatis serovar E recombinant major outer membrane protein vaccine is dependent on phosphate substitution in the adjuvant Pal, Sukumar; Ausar, Salvador Fernando; Tifrea, Delia F. Human Vaccines & Immunotherapeutics, Vol. 16, Issue 10 https://doi.org/10.1080/21645515.2020.1717183	journal	March 2020
High-resolution mapping of serovar-specific and common antigenic determinants of the major outer membrane protein of Chlamydia trachomatis. Stephens, R. S.; Wagar, E. A.; Schoolnik, G. K. Journal of Experimental Medicine, Vol. 167, Issue 3 https://doi.org/10.1084/jem.167.3.817	journal	March 1988
National Institute of Allergy and Infectious Diseases workshop report: “Chlamydia vaccines: The way forward” Zhong, Guangming; Brunham, Robert C.; de la Maza, Luis M. Vaccine, Vol. 37, Issue 50 https://doi.org/10.1016/j.vaccine.2017.10.075	journal	November 2019
Protection against influenza virus infection by intranasal administration of hemagglutinin vaccine with chitin microparticles as an adjuvant Hasegawa, Hideki; Ichinohe, Takeshi; Strong, Peter Journal of Medical Virology, Vol. 75, Issue 1 https://doi.org/10.1002/jmv.20247	journal	January 2004
Toll-dependent selection of microbial antigens for presentation by dendritic cells Blander, J. Magarian; Medzhitov, Ruslan Nature, Vol. 440, Issue 7085 https://doi.org/10.1038/nature04596	journal	February 2006
Spontaneous Resolution of Genital Chlamydia trachomatis Infection in Women and Protection from Reinfection Geisler, William M.; Lensing, Shelly Y.; Press, Christen G. The Journal of Infectious Diseases, Vol. 207, Issue 12 https://doi.org/10.1093/infdis/jit094	journal	March 2013
Cell-free production of a functional oligomeric form of a Chlamydia major outer-membrane protein (MOMP) for vaccine development He, Wei; Felderman, Martina; Evans, Angela C. Journal of Biological Chemistry, Vol. 292, Issue 36 https://doi.org/10.1074/jbc.M117.784561	journal	July 2017
Global Estimates of the Prevalence and Incidence of Four Curable Sexually Transmitted Infections in 2012 Based on Systematic Review and Global Reporting Newman, Lori; Rowley, Jane; Vander Hoorn, Stephen PLOS ONE, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pone.0143304	journal	December 2015
Quantifying size distributions of nanolipoprotein particles with single-particle analysis and molecular dynamic simulations Blanchette, Craig D.; Law, Richard; Benner, W. Henry Journal of Lipid Research, Vol. 49, Issue 7 https://doi.org/10.1194/jlr.M700586-JLR200	journal	April 2008
A Recombinant Chlamydia trachomatis MOMP Vaccine Elicits Cross-serogroup Protection in Mice Against Vaginal Shedding and Infertility Tifrea, Delia F.; Pal, Sukumar; de la Maza, Luis M. The Journal of Infectious Diseases, Vol. 221, Issue 2 https://doi.org/10.1093/infdis/jiz438	journal	August 2019
Reproductive system infections in women: upper genital tract, fetal, neonatal and infant syndromes Brunham, Robert C.; Paavonen, Jorma Pathogens and Disease, Vol. 78, Issue 5 https://doi.org/10.1093/femspd/ftaa023	journal	May 2020
Reproductive system infections in women: lower genital tract syndromes Brunham, Robert C.; Paavonen, Jorma Pathogens and Disease, Vol. 78, Issue 5 https://doi.org/10.1093/femspd/ftaa022	journal	May 2020
Evaluation of a multisubunit recombinant polymorphic membrane protein and major outer membrane protein T cell vaccine against Chlamydia muridarum genital infection in three strains of mice Yu, Hong; Karunakaran, Karuna P.; Jiang, Xiaozhou Vaccine, Vol. 32, Issue 36 https://doi.org/10.1016/j.vaccine.2014.06.002	journal	August 2014
Colocalized Delivery of Adjuvant and Antigen Using Nanolipoprotein Particles Enhances the Immune Response to Recombinant Antigens Fischer, Nicholas O.; Rasley, Amy; Corzett, Michele Journal of the American Chemical Society, Vol. 135, Issue 6 https://doi.org/10.1021/ja3063293	journal	January 2013
The use of nanolipoprotein particles to enhance the immunostimulatory properties of innate immune agonists against lethal influenza challenge Weilhammer, Dina R.; Blanchette, Craig D.; Fischer, Nicholas O. Biomaterials, Vol. 34, Issue 38 https://doi.org/10.1016/j.biomaterials.2013.09.038	journal	December 2013
Differential Regulation of CD4 Lymphocyte Recruitment between the Upper and Lower Regions of the Genital Tract during Chlamydia trachomatis Infection Kelly, Kathleen A.; Walker, Jennifer C.; Jameel, Shimul H. Infection and Immunity, Vol. 68, Issue 3 https://doi.org/10.1128/IAI.68.3.1519-1528.2000	journal	March 2000
Seventy Years of Chlamydia Vaccine Research – Limitations of the Past and Directions for the Future Phillips, Samuel; Quigley, Bonnie L.; Timms, Peter Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00070	journal	January 2019
Vaccination with the recombinant major outer membrane protein elicits long-term protection in mice against vaginal shedding and infertility following a Chlamydia muridarum genital challenge Pal, Sukumar; Cruz-Fisher, Maria I.; Cheng, Chunmei npj Vaccines, Vol. 5, Issue 1 https://doi.org/10.1038/s41541-020-00239-7	journal	October 2020
Vaccination against Chlamydia Genital Infection Utilizing the Murine C. muridarum Model Farris, Christina M.; Morrison, Richard P. Infection and Immunity, Vol. 79, Issue 3 https://doi.org/10.1128/IAI.00881-10	journal	March 2011
The global roadmap for advancing development of vaccines against sexually transmitted infections: Update and next steps Gottlieb, Sami L.; Deal, Carolyn D.; Giersing, Birgitte Vaccine, Vol. 34, Issue 26 https://doi.org/10.1016/j.vaccine.2016.03.111	journal	June 2016
The chlamydial pneumonias Cunha, B. A. Drugs of Today, Vol. 34, Issue 12 https://doi.org/10.1358/dot.1998.34.12.487485	journal	January 1998
The Unexpected Impact of a Chlamydia trachomatis Infection Control Program on Susceptibility to Reinfection Brunham, Robert C.; Pourbohloul, Babak; Mak, Sunny The Journal of Infectious Diseases, Vol. 192, Issue 10 https://doi.org/10.1086/497341	journal	November 2005
Antigenic Analysis of the Major Outer Membrane Protein of Chlamydia spp Caldwell, Harlan D.; Schachter, Julius Infection and Immunity, Vol. 35, Issue 3 https://doi.org/10.1128/iai.35.3.1024-1031.1982	journal	March 1982
T-Cell Epitopes in Variable Segments of Chlamydia trachomatis Major Outer Membrane Protein Elicit Serovar-Specific Immune Responses in Infected Humans Ortiz, Linette; Angevine, Mark; Kim, Seon-Kyeong Infection and Immunity, Vol. 68, Issue 3 https://doi.org/10.1128/IAI.68.3.1719-1723.2000	journal	March 2000
Correlation of host immune response with quantitative recovery of Chlamydia trachomatis from the human endocervix Brunham, R. C.; Kuo, C. C.; Cles, L. Infection and Immunity, Vol. 39, Issue 3 https://doi.org/10.1128/iai.39.3.1491-1494.1983	journal	March 1983
A Predominant Role for Antibody in Acquired Immunity to Chlamydial Genital Tract Reinfection Morrison, Sandra G.; Morrison, Richard P. The Journal of Immunology, Vol. 175, Issue 11 https://doi.org/10.4049/jimmunol.175.11.7536	journal	November 2005
An Unidentified Virus Which Produces Pneumonia and Systemic Infection in mice Nigg, C. Science, Vol. 95, Issue 2454 https://doi.org/10.1126/science.95.2454.49-a	journal	January 1942
Risk of Sequelae after Chlamydia trachomatis Genital Infection in Women Haggerty, Catherine L.; Gottlieb, Sami L.; Taylor, Brandie D. The Journal of Infectious Diseases, Vol. 201, Issue S2 https://doi.org/10.1086/652395	journal	June 2010
Protection against infertility in a BALB/c mouse salpingitis model by intranasal immunization with the mouse pneumonitis biovar of Chlamydia trachomatis Pal, S.; Fielder, T. J.; Peterson, E. M. Infection and Immunity, Vol. 62, Issue 8 https://doi.org/10.1128/iai.62.8.3354-3362.1994	journal	August 1994
The purification of eukaryotic polypeptides synthesized in Escherichia coli Marston, F. A. Biochemical Journal, Vol. 240, Issue 1 https://doi.org/10.1042/bj2400001	journal	November 1986
CD4+ T Cells and Antibody Are Required for Optimal Major Outer Membrane Protein Vaccine-Induced Immunity to Chlamydia muridarum Genital Infection Farris, C. M.; Morrison, S. G.; Morrison, R. P. Infection and Immunity, Vol. 78, Issue 10 https://doi.org/10.1128/IAI.00622-10	journal	July 2010
Amphipols stabilize the Chlamydia major outer membrane protein and enhance its protective ability as a vaccine Tifrea, Delia F.; Sun, Guifeng; Pal, Sukumar Vaccine, Vol. 29, Issue 28 https://doi.org/10.1016/j.vaccine.2011.04.065	journal	June 2011
Vaccination with the Chlamydia trachomatis Major Outer Membrane Protein Can Elicit an Immune Response as Protective as That Resulting from Inoculation with Live Bacteria Pal, S.; Peterson, E. M.; de la Maza, L. M. Infection and Immunity, Vol. 73, Issue 12 https://doi.org/10.1128/IAI.73.12.8153-8160.2005	journal	November 2005
Induction of protection against vaginal shedding and infertility by a recombinant Chlamydia vaccine Carmichael, Jennifer R.; Pal, Sukumar; Tifrea, Delia Vaccine, Vol. 29, Issue 32 https://doi.org/10.1016/j.vaccine.2011.05.013	journal	July 2011
Subunit vaccines for the prevention of mucosal infection with Chlamydia trachomatis Yu, Hong; Karunakaran, Karuna P.; Jiang, Xiaozhou Expert Review of Vaccines, Vol. 15, Issue 8 https://doi.org/10.1586/14760584.2016.1161510	journal	March 2016

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60 APPLIED LIFE SCIENCES
Chlamydia
vaccine
immunization
mice
nanolipoprotein particles
major outer membrane protein
intranasal challenge
telodisks
amphipols

Title: Induction of Protection in Mice against a Chlamydia muridarum Respiratory Challenge by a Vaccine Formulated with the Major Outer Membrane Protein in Nanolipoprotein Particles

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