Overview of scientific advances toward an HIV cure

Overview of scientific
advances toward an HIV
cure
Sharon R Lewin
Director, Infectious Disease Unit, Alfred Hospital
Professor, Department of Medicine, Monash University
Co-head, Centre for Virology, Burnet Institute,
Melbourne, Australia
13th European AIDS Conference, Belgrade, Oct 2011
Outline
ƒ Why can’t cART cure HIV?
ƒ What are potential strategies to
achieve a cure?
ƒ Current clinical trials aimed at cure
ƒ Current and future challenges
why can’t cART cure
HIV?
Rapid rebound in virus when cART
stopped
HIV RNA
CD4 count
50
0
1
Years on HAART
off cART
HIV DNA
CD4 count
HIV RNA
HIV DNA in infected cells is always
detectable
50
0
1
Years on cART
Chun et al., Nature 1997; 387:183; Finzi et al., Science 1997; 278:1295; Wong et al., Science 1997; 278:1291
HIV DNA
CD4 count
HIV RNA
No such thing as an “undetectable
viral load”
50
1
0
1
Years on cART
Palmer et al., Proc Natl Acad Sci U S A. 2008;105:3879-84 Maldarelli et al., Plos Pathogens 2007; 3:484
Barriers to cure
ƒ Latently infected T-cells
ƒ Residual viral replication
ƒ Anatomical reservoirs
HIV latency and infection of resting
T-cells
cART
Activated CD4+ T-cell
Resting CD4+ T-cell
Tissue
chemokines
Eckstein et al, Immunity 2001; 15: 671; Kreisberg et al., J Exp Med 2006; 203:865; Saleh et al., Blood 2007;
110:416; Marini et al., J Immunol 2008; 181: 7713-20; Bosque and Planelle, Blood 2009; 113:58;
Cameron et al., Proc Natl Acad Sci 2010; 107(39):16934
Latently infected T-cells
cART
Latent infection can be established
in many T cells
Bone marrow
Thymus
Peripheral circulation
Ag
M M
M M
Naive
Multipotent
progenitor cells
Naïve T cells
Effector/
transitional
Transitional memory
Central
memory
Central memory
Latent reservoir
Chun et al., Nature 1997; 387:183; Finzi et al., Science 1997; 278:1295; Brooks et al., Nat Med 2001; 7:459 ;
Chomont et al., Nat Med 2009; 15: 893; Dai et al., J Virol 2009: 83(9):4528-37; Carter et al., Nat Med 2010; 16: 446;
Wightman et al., J Infect Dis 2010; 202(11):1738-48; Carter et al., Cell Host Microbe. 2011;9(3):223-34.
Residual replication
cART
cART
Immune activation associated with viral
persistence in tissue
Hatano et al., 6th IAS Conference, Rome, 2011
Anatomical reservoirs
Anatomical reservoirs
DCs, macrophages, astrocytes
cART
cART
GI tract is a significant viral reservoir on
cART
HIV DNA per million cells
HIV DNA
N=8, time on cART with undetectable HIV RNA 2.8 – 12 years
Chun et al., J Infect Dis 2008; 197:714; Yukl et al., J Infect Dis 2010 202:1553
What are potential
strategies to achieve
a cure?
Cure or remission?
Cure
Remission
Infectious Diseases
model
Elimination of all HIVinfected cells
HIV RNA < 1 copy/ml
Cancer model
Sterilising cure
Long term health in
absence of HAART
HIV RNA < 50
copies/ml
Functional cure
Strategies for cure
ƒ Eliminate residual virus replication
ƒ Eliminate latently infected cells
ƒ Make cells “resistant” to HIV
ƒ Enhance HIV-specific immunity
current clinical
trials aimed at cure
Eliminating viral replication:
treatment intensification
HIV RNA
HIV DNA
CD4 count
T20
LPV/r
ATV/r
Raltegravir (x4)
Maraviroc (x2)
50
1
0
1
Years on HAART
intensification
Dinoso et al., Proc Natl Acad Sci U S A, 2009. 106(23): 9403-8; McMahon et al., Clin Infect Dis, 2010. 50(6):
912-9; Ghandi et al., J Infect Dis. 2010.201(2):293-6 and CROI 2011 ; Buzon et al., Nat Med, 2010 16: 460;
Ghandi et al., Plos Med 2011; Yukl et al., AIDS 2010; Hatano et al., J Infect Dis 2011; Hunt et al., CROI 2010
Cell-to-cell infection not blocked by
cART
Cell free infection
Cell-cell infection
e.g., lymphoid tissue
cART
+
• Reduce immune activation
• Inhibit cellular not viral targets
• Enhance tissue penetration of cART
Sigal et al., Nature, 2011; 477(7362):95-8
Eliminate latently infected T-cells:
activate latent HIV
cART
Activated CD4+ T-cell
Resting CD4+ T-cell
Activating latent HIV
The Economist, July 17, 2011
Licensed drugs that activate
latently infected cells
Phase Phase Phase
I
II
III
Histone
deacetylase
inhibitors
Methylation
inhibitor
Cytokine
Anti-alcoholic
Vorinostat
Romidepsin
Panabinostat
Entinostat
Belinostat
Givinostat
Others (9)
Licensed
Yes
Yes
#
Latency
Trials* trials
176
32
94
20
28
7
2
5-azacytidine
>26
Interleukin-7
52
1
20
1
Disulfiram
Yes
* Total number of trials listed on http://clinicaltrials.gov (July 2011)
Prince et al. Clin Canc Res 2009;15:3958; Contreras et al, J Biol Chem 2009; 284: 6782; Archin et al AIDS Res
Hum Retroviruses 2009;25:207; Xing et al., J Virol; 2011;85(12):6060-4; Friedman et al., J Virol. 2011;85(17):
9078-89; Matalon et al., Mol Med. 2011 May-Jun;17(5-6):466-72 Saleh et al., Retrovirology 2011 (in press)
Virus released from latency
(% maximal stimulation)
Combination therapy: enhances
potency of activation
HDACi
100
+
80
60
40
20
0
ND
IL
-7
tin
tin
α
a
a
r
F
t
tr
s
s
N
o
o
T
pr
pr
+
-7
IL
Saleh et al., Retrovirology 2011 (in press)
Prostratin
or
Bryostatin
or
methylation inhibitor
Reuse et al., Plos One 2009; 4:e6093;
Burnett et al., J Virol. 2010 Jun;84(12):5958-74
Perez et al., Curr HIV Res. 2010 Sep 1;8(6):418-29;
Van Lint, 6th IAS, Rome 2011
HDACi turn HIV genes “on”
HDACi
OFF
TF
Bolden et al., Nat Rev Drug Disc 2006;5:769; Prince et al. Clin Canc Res 2009;15:3958;
Contreras et al, J Biol Chem 2009; 284: 6782; Archin et al AIDS Res Hum Retroviruses 2009;25:207;
Wightman et al., Immunol Cell Biol 2011(in press)
Vorinostat (SAHA)
ƒ Potent HDAC inhibitor
ƒ Activates HIV from latency in vitro
ƒ Licensed for cutaneous T cell lymphoma
ƒ Multiple phase II trials for other
malignancies including lymphoma,
myeloma, solid tumors
ƒ Oral administration
ƒ Long term toxicities unknown
Contreras et al, J Biol Chem 2009; 284: 6782; Archin et al AIDS Res Hum Retroviruses 2009;25:207; Saleh et al.,
Retrovirology 2011 (in press); Wightman et al Immunol Cell Biology 2011 (in press)
Will HDACi turn HIV genes on in vivo?
n=20
0,2,8 hours
* Rectal biopsy
Suppressive cART > 3 years
Vorinostat 400 mg/day
screen
0
2
7
*
Primary
endpoint
14
*
Cell associated
HIV RNA
21
28 and 84
Latently infected cells are rare
Make cells “resistant” to HIV:
gene therapy
cART
Activated CD4+ T-cell
Silence or
eliminate HIV
Gene therapy
Reduce CCR5
Resting CD4+ T-cell
Amado et al., Hum Gene Ther 2004: 15:251-62; An et al., PNAS 2007: 104:13110-5; Digiusto et al.,
Science Transl Med 2010; 2:36; Holt et al., Nature Biotechnol 2010;28(8):839-47; Lalezari et al., 18th CROI,
Boston, Feb 2011 abstract 46; Tebas et al., 18th CROI, Boston, Feb 2011 abstract 165
Nucleases chop up DNA: eliminate
CCR5 expression or eliminate HIV
CCR5
Naldini et al., Nature Genetics 2011; 12:301; Holt et al., Nature Biotechnol 2010;28(8):839-47; Lalezari et al.,
18th CROI, Boston, Feb 2011; Aubert et al., PLoS One. 2011 Feb 9;6(2):e16825
Gene therapy to eliminate CCR5:
Sangamo Biosciences Inc, SB728-902
SB728-902
SB728-T
n=6
Aviremic patients on cART
CD4>450
Treatment interruption
Lalezari et al., 18th CROI,
Boston, Feb 2011
Ando et al., ICAAC, Chicago, Sept 2011
Gene therapy to eliminate CCR5:
SB728T
% bi-allelic CCR5 modified cells correlated with viral suppression
Ando et al., ICAAC, Chicago, Sept 2011
current and future
challenges for HIV
cure
Scientific challenges
ƒ Multiple barriers to eradication meaning a
combination approach will be likely
ƒ Better in vitro and animal models to evaluate
new strategies, alone and in combination
ƒ Drug development to increase potency and
specificity for activating latently infected cells
and/or enhanced tissue delivery
ƒ Role of immune activation: driver of residual
replication or a consequence of virus
persistence?
Clinical and implementation challenges
ƒ Universal access to cART must remain a top
priority
ƒ PLWHA on cART are doing well so any
intervention must have limited or no toxicity
ƒ Clinical endpoints for successful “eradication”
unclear. When will a treatment interruption be
OK?
ƒ Multiple unknowns with gene therapy: safety
of delivery vectors, DNA nucleases and long
term impact of CCR5 suppression
We need a cure that is scalable,
deliverable and cheap
http://www.afripol.org/africa-newspapers/3-africa/2-newshour-with-jim-lehrer-africa-coverage-pbs.html
Funding for research toward a cure for
HIV
Developing a road map for cure
www.iasociety.org
The Rome Statement
Acknowledgements
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Department of Medicine,
Monash University
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Paul Cameron
Suha Saleh
Miranda Xhilaga
Candida Da Fonseca Pereira
Ajantha Solomon
Georgina Sallman
Fiona Wightman
Vanessa Evans
Sam Ramanayake
Melissa Chow
Paula Ellenberg
Miranda Xhilaga
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The Alfred Hospital
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Julian Elliott
Jennifer Hoy
Janine Roney
Gregor Brown
ACBD, Monash University
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Anthony Dear
Burnet Institute
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Anthony Jaworwski
Melissa Churchill
Peter Macallum Cancer Institute
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Miles Prince
National Association of People
living With AIDS
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Jo Watson
Bill Whittaker
Merck
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Charles Farthing
Daria Hazuda