Establishment and Targeting of the Viral Reservoir in Rhesus Monkeys

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1 Establishment and Targeting of the Viral Reservoir in Rhesus Monkeys Dan H. Barouch, M.D., Ph.D. Center for Virology and Vaccine Research Beth Israel Deaconess Medical Center Ragon Institute of MGH, MIT, and Harvard August 8, 2014

2 Early Treatment of Acute SIVmac251 Infection in Rhesus Monkeys The latent viral reservoir that persists despite ART represents the most critical challenge facing HIV-1 eradication strategies Early ART has been shown to reduce the size of the reservoir in certain HIV-1-infected humans However, it remains unclear precisely when and where the reservoir is established, although it is believed to be seeded in acute HIV-1 infection during peak viremia We therefore investigated the impact of early ART on viral reservoirs in acute SIV infection in rhesus monkeys

3 Study Design IR SIVmac251 infection in 20 rhesus monkeys ART initiated on day 3, 7, 10, 14, or no ART (N=4/group) Gilead ART cocktail (tenofovir, emtricitabine, dolutegravir) Daily ART x 24 weeks followed by treatment discontinuation BIDMC, Ragon Institute, Harvard, MHRP, Gilead, Bioqual

4 SIVmac251 Infection No ART Log SIV RNA Copies / ml Days Following SIV Infection

5 SIVmac251 Infection ART Started Day 14 Log SIV RNA Copies / ml Days Following SIV Infection

6 SIVmac251 Infection ART Started Day 10 Log SIV RNA Copies / ml Days Following SIV Infection

7 SIVmac251 Infection ART Started Day 7 Log SIV RNA Copies / ml Days Following SIV Infection

8 SIVmac251 Infection ART Started Day 3 Log SIV RNA Copies / ml Days Following SIV Infection

9 No SIV Env ELISA Responses with Day 3 ART Reduced SIV Env ELISA Responses with Day 7-14 ART week

10 No SIV ELISPOT Responses with Day 3 ART Reduced SIV ELISPOT Responses with Day 7-14 ART week

11 Proviral DNA Detected in Lymph Nodes and Gut Mucosa but not in PBMC with Day 3 ART Log DNA Copies / 10 6 Cells PBMC LNMC GMMC Days Following SIV Infection

12 Proviral DNA Detected in PBMC, Lymph Nodes, and Gut Mucosa with Day 7 ART Log DNA Copies / 10 6 Cells PBMC LNMC GMMC Days Following SIV Infection

13 Proviral DNA Detected in PBMC, Lymph Nodes, and Gut Mucosa with Day 10 ART Log DNA Copies / 10 6 Cells PBMC LNMC GMMC Days Following SIV Infection

14 Proviral DNA Detected in PBMC, Lymph Nodes, and Gut Mucosa with Day 14 ART Log DNA Copies / 10 6 Cells PBMC LNMC GMMC Days Following SIV Infection

15 Early ART Reduces the Size of Viral Reservoirs PBMC LNMC GMMC P< P< P< P=0.004 P=NS Day of ART Initiation Day of ART Initiation Day of ART Initiation

16 SIV DNA / 10 6 CD4 T C e lls Proviral DNA is First Detected in Transitional and Central Memory CD4+ T Cells in Lymph Nodes Day 3 Day N T M C M 0 0 G e n ita l Ilia c Mesenteric PBMC G e n ita l Ilia c A x illa ry Mesenteric PBMC 1000 Lym ph Node Lym ph Node SIV DNA / 10 6 CD4 T C e lls G e n ita l Inguinal Ilia c P ara PBMC G e n ita l Inguinal Ilia c P ara A x illa ry Mesenteric PBMC Lym ph Node Lym ph Node

17 SIVmac251 Infection ART Started Day 3 No Plasma Virus (<50 Copies/ml) for 24 Weeks Log SIV RNA Copies / ml ART Days Following SIV Infection

18 SIVmac251 Infection ART Started Day 3 Viral Rebound in 100% of Animals After Stopping ART ART Stopped Log SIV RNA Copies / ml ART Days Following SIV Infection

19 Day 3 Delayed Viral Rebound in Monkeys Started on ART on Day 3 vs. Days 7-14 Log SIV RNA Copies / ml Day 7 Day 10 Day 14 Days Following SIV Infection

20 Delayed Viral Rebound in Monkeys Started on ART on Day 3 vs. Days 7-14 Days to Viral Rebound P= Day 3 Day 7 Day 10 Day 14

21 ART Regimen Completely Suppressed Viral Replication at Week 20 (<6 Copies/ml) Log SIV RNA Copies / m l D a y 3 D a y 7 Day 10 Day 14 < 6 copies/ml Day of ART Initiation

22 Pre-ART Viremia During Acute Infection Predicts the Size of the Viral Reservoir Log PBMC DNA y = 0.43x 0.70 R 2 = 0.81 P< Log LNMC DNA y = 0.32x 0.25 R 2 = 0.45 P= Log Pre-ART AUC VL Log Pre-ART AUC VL

23 Pre-ART Viremia and Size of the Viral Reservoir Predict Time to Viral Rebound Days to Viral Rebound y = -2.7 x R 2 = 0.71 P< Days to Viral Rebound y = -7.3 x R 2 = 0.48 P= Log Pre-ART AUC VL Log PBMC DNA

24 Conclusions (I) Viral reservoir in this model was established remarkably early: within 3 days of infection, during the eclipse period of infection, and prior to plasma viremia ( Fiebig 0 ) In the first few days after IR SIV infection, reservoir was rapidly established in lymph nodes and/or gut mucosa before PBMC Early ART on day 3 reduced the size of the viral reservoir and delayed viral rebound, but this did not prevent viral rebound This very early establishment of the viral reservoir poses new challenges for HIV-1 cure strategies and suggests potential limitations of early ART strategies

25 Nature /13594 July 20 (2014)

26 Nature /13647 July 20 (2014)

27 Can Potent Neutralizing HIV-1-Specific Monoclonal Antibodies Contribute to HIV-1 Eradication Efforts?

28 Therapeutic Efficacy of Potent Neutralizing HIV-1- Specific Monoclonal Antibodies Current neutralizing HIV-1-specific mabs are substantially more potent and broad than those available previously The broad and potent glycan-dependent and CD4 binding site-specific mabs have been shown to block SHIV acquisition in passive protection studies in rhesus monkeys We and others have recently demonstrated the therapeutic efficacy of potent neutralizing HIV-1-specific mabs in chronically SHIV-infected rhesus monkeys Collaboration with Michel Nussenzweig and Dennis Burton Barouch et al. Nature 2013; 503: Shingai et al. Nature 2013; 503:277

29 Barouch et al. Nature 2013; 503:

30 Summary of Therapeutic Efficacy of PGT121 or PGT121-Containing mab Cocktails

31 A Single N332 Mutation Does Not Fully Abrogate PGT121 Activity: Intrinsic High Bar to Resistance? PGT121 makes at least 4 glycan contacts at N332, N301, N156/173, N137 (Burton, Wilson)

32 Decline of Proviral DNA in Lymph Nodes, GI Mucosa, and PBMC Following a Single Infusion of PGT121 P = 0.05 P = 0.1 P = 0.05

33 Picker and Deeks Nature 2013; 503: Weiss NEJM 2014; 370:

34 Potential Role of Broadly Neutralizing mabs in HIV-1 Eradication Strategies? Our published studies demonstrated that PGT121 reduced proviral DNA in tissues in viremic monkeys, but did not assess if PGT121 can target the reservoir in ART-suppressed animals Clinical studies are planned to assess whether broadly neutralizing mabs can reduce proviral DNA in ART-suppressed, HIV-1-infected humans A key question is whether reservoir cells express sufficient Env to be targeted by mabs (i.e. homeostatic proliferation, low levels of virus production, immune or pharmacologic activation, etc.) We therefore performed a pilot study to evaluate the impact of PGT121 in ART-suppressed, SHIV-infected rhesus monkeys

35 Therapeutic Efficacy of PGT121 in ART-Suppressed, SHIV-Infected Rhesus Monkeys 9 rhesus monkeys infected with SHIV-SF162P3 for 7 months; baseline viral loads log RNA copies/ml Daily suppressive ART initiated in all animals and continued for 20 weeks (tenofovir, emtricitabine, dolutegravir) Group 1 (N=5): ART (weeks 0-20) + PGT121 (weeks 0, 4, 8, 12) Group 2 (N=4): ART (weeks 0-20) alone ART discontinued at week 20

36 Rapid and Complete Virologic Suppression Following Initiation of Both ART + PGT121 and ART Alone ART + PGT121 ART Alone PGT121 ART ART Log RNA Copies/ml Days Following Study Initiation

37 Reduction in Proviral DNA in PBMC in ART + PGT121 Treated Rhesus Monkeys ART + PGT121 ART Alone Log DNA Copies/10 6 PBMC Days Following Study Initiation

38 Reduction in Proviral DNA in Gastrointestinal Mucosa in ART + PGT121 Treated Rhesus Monkeys ART + PGT121 ART Alone Log DNA Copies/10 6 GMMC Days Following Study Initiation

39 Rapid and Complete Virologic Suppression Following Initiation of Both ART + PGT121 and ART Alone ART + PGT121 ART Alone PGT121 ART ART Log RNA Copies/ml Days Following Study Initiation

40 Partial Virologic Control in ART + PGT121 Treated Monkeys Following ART Discontinuation ART + PGT121 ART Alone PGT121 ART ART Log RNA Copies/ml Days Following Study Initiation 60% (3 of 5) Virologic Control 0% (0 of 4) Virologic Control

41 Conclusions (II) In a pilot study, PGT121 reduced proviral DNA in PBMC and tissues in ART-suppressed, SHIV-infected rhesus monkeys ART + PGT121 resulted in virologic control in 60% (3 of 5) of animals following ART discontinuation Larger, definitive NHP studies will be needed to confirm and extend these results and guide clinical development strategies PGT121, both alone and in combination with other mabs, should be evaluated in humans as part of HIV-1 eradication strategies PGT121 GMP manufacturing in progress; clinical studies in HIV- 1-infected humans scheduled to begin in 2015

42 Acknowledgements (Early ART Studies) Beth Israel Deaconess, Harvard Medical School James Whitney Pablo Penaloza Jennifer Shields Lily Parenteau Jinyan Liu Kaitlin Smith Erica Borducchi Crystal Cabral Jeffrey Smith Stephen Blackmore Srisowmya Sanisetty Harvard University Alison Hill Daniel Rosenbloom Martin Nowak Gilead Romas Geleziunas Bioqual Mark Lewis MHRP Nelson Michael Jerome Kim Merlin Robb Ragon Institute of MGH, MIT, and Harvard DAIDS, NIAID, NIH Michael Pensiero

43 Acknowledgements (Therapeutic mab Studies) Beth Israel Deaconess, Harvard Medical School James Whitney Jinyan Liu Kathryn Stephenson Hui-Wen Chang Joseph Nkolola Michael Seaman Kaitlin Smith Erica Borducchi Crystal Cabral Jeffrey Smith Stephen Blackmore Srisowmya Sanisetty James Perry Rockefeller University Florian Klein Thiago Oliveira Michel Nussenzweig Scripps Brian Moldt Pascal Poignard Dennis Burton Bioqual Mark Lewis Catalent Pharma Theraclone Sciences Kristine Swiderek Gilead Sciences Romas Geleziunas Ragon Institute of MGH, MIT, and Harvard DAIDS, NIAID, NIH Michael Pensiero Gates Foundation Pervin Anklesaria Nina Russell

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