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Laurel Lagenaur Guest Researcher NIH HIV Infection in Women Around the Globe

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Laurel Lagenaur Guest Researcher NIH HIV Infection in Women Around the Globe Modifying the vaginal microbiome to protect against HIV Laurel Lagenaur Guest Researcher NIH HIV Infection in Women Around the Globe • Need for HIV prevention strategies for women • In 2013, almost 60% of all new HIV infections occurred among women, particularly young women and adolescent girls aged 15–24. Women Age 24 – 50% HIV+ Men Age 24 – 6% HIV+ HIV is Transmitted Across Mucosal Surfaces • HIV infection in women occurs in the epithelium of the vagina and cervix • Infection of underlying target cells (mostly CD4+ T cells) From Tom Hope Mucosal Surfaces are a Living Community • All mucosal surfaces are continuously exposed to a community of microorganisms Lactobacilli • Vagina and Cervix Vaginal Lactobacillus sp. are Epithelial Cell found in 51-90 % women H2O2-Colonization • L. crispatus, L. jensenii, D-lactic acid producers L. gasseri (and L. iners) L-lactic acid Vaginal Microbiota is Relevant to Human Health Healthy Vagina Dysbiosis Bacterial Diversity H2O2-producing Lactobacillus Low Diversity High Diversity Lactobacillus = Defense against Increased risk of infections (BV, rUTI) urogenital pathogens Increased risk of preterm birth, other Contribute to low vaginal pH OB/GYN complications Produce antibacterial substances Increased inflammation and risk of HIV Block pathogen binding, i.e. competitive exclusion Cervicovaginal Bacteria are a Major Modulator of the Host Inflammatory Responses • A recent paper by Anahtar et al. (senior authors Walker, Fichorova, Kwon, Immunity 2015 studied a cohort of South African women • A majority of these women had low abundance of Lactobacillus • Low Lactobacillus abundance together with high ecological diversity strongly correlated with genital pro- inflammatory cytokine concentration Four community types • Community types – Group 1, L. crispatus, very low alpha diversity – Group 2 L. iners low diversity – Group 3 Gardnerella moderate diversity – Group 4 Prevotella high diversity Anahtar et al. Immunity 2015 Women with CT4 had high inflammatory cytokines – Increases in IL-1α, IL-1β, TNF-α, IFN-γ, IL-10 and IL-8 IL-1α IL-1β TNF-α IFN-γ IL-10 IL-8 Immunity 2015 Osel’s Technology Modulating the Vaginal Microbiome to Prevent HIV Modulating the Vaginal Microbiome to Prevent HIV • Engineer vaginal Lactobacilli to produce an HIV entry inhibitor (recombinant live biotherapeutic) HIV • Colonize the mucosa modified Lactobacillus jensenii 1153 HIV inhibitor (H2O2) producer Lactobacillus - Natural defense, lactic acid, “anti- inflammatory” HIV - Genetically modified to produce HIV inhibitor an HIV entry inhibitor - Protection at the site of HIV Lactobacillus infection Strain selection process • Screened >20 isolates of L. crispatus, L. jensenii and L. gasseri from healthy women • Selected L. jensenii 1153 - Although variations of the microbiota exist within individuals over time and in different geographical settings, L. jensenii is found in 17%-41% of women across many regions of the world Strain selection • Selected L. jensenii 1153 L. jensenii 1153 - Growth rate-doubling time - D-Lactic acid production - Adherence to tissue - Activity against Gardnerella and Staphylococcus - Transform (no endogenous plasmids) • Broad Institute/J. Craig Venter Institute - sequenced and annotated genome 1153 Selecting an inhibitor; HIV is a diverse virus B A B C C G AE AG B D A C A C B HG C Global distribution of HIV-1 subtypes and recombinants. Trends in Molecular Medicine, Volume 18, Issue 3, 2012, 182 - 192 HIV Inhibitor Selection • Tested expression multiple HIV entry inhibitors in Lactobacillus • Selected HIV inhibitor protein Cyanovirin-N Inhibitor Selection Cyanovirin-N (NCI) - Identified by National Cancer Institute drug screen (Cyanobacterium) - Activity against all subtypes - Concentration of CV-N produced by Lactobacillus [272 nm] - Inhibited >85% HIV viruses in a representative panel of major subtypes - CV-N active pH 4-8 (vaginal(vaginal pHpH range)range) HIV Inhibitor Selection •Cyanovirin-N Binding Courtesy of Carole Bewley Ultrastructural: Cell+ HIVBaL + Lactobacillus HIV HIV cell Identified optimal Lactobacillus strain, strong HIV inhibitor that worked against multiple subtypes and at an appropriate pH range Next we constructed a recombinant Lactobacillus and tested it for fitness Constructing a recombinant • Stably integrated mCV-N Integration plasmid gene into the Lactobacillus chromosome by orfA` mCVN orfA` homologous recombination orfA L. jensenii 1153 chromosome • Biologically active level of inhibitor expression using a Integrate into chromosome constitutive ribosomal promoter Secretion of mCVN Liu et al. 2006, AAC Fitness and Phenotypic Characteristics of L. jensenii 1153 with Integrated mCV-N Recombinant strains produced equivalent amounts of D-Lactic acid as the parent (WT) 4.5 4 D-Lactic acid 3.5 3 WT1153 wt 2.5 R1pox1 2 1.5 R2pepO 1 D-LacticAcid (g/L) Lactic Acid (g/L) Acid Lactic - 0.5 D 0 0 1 OD600 2 3 OD600 Fitness and Phenotypic Characteristics of L. jensenii 1153 with Integrated mCV-N Recombinant strains have similar growth rates to the parent (WT) 20 18 ) 8 16 14 12 WT1153 wt ) 8 10 growth rates R2pepO 8 R1pox1 6 4 Cell Numbers (10 2 Cell numbers (10 numbers Cell 0 0 200 400 600 800 TimeTime Minutes (Minutes) Phenotypic Characteristics of L. jensenii 1153 with Integrated mCV-N Recombinant strains secreted biologically active mCV-N 1153 WT Rec 1 Rec 2 OD600 0.5 1.0 3 0.5 1.0 3 0.5 1.0 3 kDa 14 mCV-N 11kDa 6 Recombinant strain produced H2O2 We had constructed a fit recombinant L. jensenii expressing mCV-N Next we wanted to test it in vivo Macaque model Intravaginal Inoculation of L. jensenii producing mCV-N in Macaques In initial studies….. Pellet + 3% hydroxyethyl cellulose Lactobacilli Vaginal Epithelial Cell Freshly prepared Rhesus macaque overnight culture Brown and Hopps Modified Gram stain Recovery of L. jensenii-mCV-N from Rhesus Macaques following 5-day dose Followed 10macaques10 for 6 weeks 9 10 Vaginal colonization 108 107 recovered 106 105 104 103 102 Lactobacillus jensenii 101 Lactobacillus CFU recovered Lactobacillus 100 7 14 21 28 35 42 49 Days PI L. jensenii-mCV-N We showed that our L. jensenii recombinant could colonize the macaque Next we wanted to prove that it was making mCV-N protein in situ Proof of Principle • Colonized rhesus macaques Lj 1153-1666 Lj 1153-2666 • Cervical vaginal lavage M1 M2 M3 M4 M5 M6 taken weekly Week 0 (before inoculation) Day 1 • mCV-N protein (24 hrs after inoculation) detected by immunoblot for at least 6 weeks Week 3 Week 6 Proof of Principle • Colonized rhesus macaques • Immunohistochemistry on vaginal biopsies for mCV-N protein Pre-immune Anti-CV-N • mCV-N protein localized vaginal lumen on mucosal surface at the site of virus entry mucosal surface 1:4000 1:4000 We showed that our L. jensenii recombinant could colonize the macaque and make mCV-N protein in situ Now we wanted to challenge macaques with Simian (S)HIV to test whether infection could be prevented SHIV Repeated Dose Challenge • Two arm study – 12 macaques received L. jensenii expressing mCV-N – 12 control (8 macaques received HEC placebo gel/4 no gel – Macaques were challenged each week for 6 weeks with (S)HIV – Monitored for viral infection each week • Repeated dose challenges measure the rate of infection per exposure • Infection rate about 33% macaques/exposure (100- 1000X higher than amount found in human) • Monitor time to infection Repeated Dose Challenge-Power Analysis Control group: n=12 Experimental group: n = 12 31 challenges 61 challenges 11 infected animals 8 infected animal 35.4% infection rate 13.1% infection rate 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 SHIV Repeated Dose Challenge Results • Controls: 35% infection per exposure • LB-mCV-N: 13% infection per exposure • 63% reduction in acquisition p<0.004 • 6X reduction in viral load (macaques with breakthrough infection) 61 challenge 8 infections=13.1% 31 challenges/11 infected=35.4% Lagenaur et al. 2011 Mucosal Immunology Efficacy in a SHIV challenge model Now we moved forward with formulation of a product that could be used in the “real world” Formulation into a Product-MucoCept • Formulation Prototype tablet -Developed a vaginal ~100 mg disintegrating tablet 10 9 -Tablets are potent 5X1011 8 CFU/gm and stable (1yr) at 7 M 6 4oC or 25oC 5 4 Limit of detection by culture - Colonize macaques 3 L. jensenii 1153-1666 (CFU/swab) L. jensenii 1153-1666 Detection by PCR 2 10 1 Log Tablet administration 0 7 14 21 Days Post Dosing Lagenaur et al. 2015 PLoSOne SHIV challenge Days 0 7 10 14 17 21 24 MucoCept Tablet Placebo Tablet 34715 Survival proportions: Davis Study Part 1 all macaques 35065 100 36230 Active VDT 36262 infected 39332 50 Percent survival VDT placebo 34103 (P) infected 0 37712 (P) infected 0 1 2 3 Challenges 38603 (P) infected Snapshot during SHIV challenge SHIV challenge Days 0 7 10 14 17 21 24 MucoCept Tablet Placebo Tablet Protected Phylum:Firmicutes;Bacilli 34715 MucoCept Placebo Order: Family: Genus Tablet 100%# Tablet Turicibacterales;#Turicibacteraceae;#Turicibacter# 100%# Lactobacillales;#Streptococcaceae;#Streptococcus#Turicibacterales;#Turicibacteraceae;#Turicibacter# Lactobacillales;#Streptococcaceae;#Lactococcus#Lactobacillales;#Streptococcaceae;#Streptococcus# Lactobacillales;#Lactobacillaceae;#Lactobacillus#Lactobacillales;#Streptococcaceae;#Lactococcus# 75%# Lactobacillales;#Enterococcaceae;#Enterococcus#Lactobacillales;#Lactobacillaceae;#Lactobacillus#
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  • Lactobacillus Crispatus
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