Mayo Clinic HIV ecurriculum Series Essentials of HIV Medicine Module 2 HIV Virology

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1 Mayo Clinic HIV ecurriculum Series Essentials of HIV Medicine Module 2 HIV Virology Eric M. Poeschla, MD Professor of Medicine College of Medicine Consultant, Division of Infectious Diseases Mayo Clinic

2 2 HIV Virology Learning Objectives Upon conclusion of this HIV virology module, participants should be able to Understand the origins of HIV-1. Be familiar with retroviral classification and know which retroviruses have been demonstrated to cause human disease. Understand the structure of HIV-1 virions. Be familiar with the genetic make-up of the virus and the main steps in the life cycle. Understand how HIV enters a cell and what cell types are infected in the body. Know how basic features of the replication cycle influence transmission risk and drug resistance. Understand the concept of antiviral restriction.

3 3 HIV Virology Retroviruses HIV-1 is a lentivirus. Lentiviruses are one of the seven genera of retroviruses. The seven retroviral genera are: 1. Alpha - such as avian leukosis virus of birds. 2. Beta - such as mouse mammary tumor virus. 3. Gamma (e.g., murine type C) such as murine leukemia virus or gibbon ape leukemia virus, and in humans, xenotropic murine leukemia virus (MLV)-related virus (XMRV). 4. Delta - such as HTLV-I and HTLV-II. 5. Epsilon certain fish retroviruses. 6. Lentivirus - e.g. HIV-1, HIV-2, SIVs (monkeys), FIV (feline), EIAV (equine), etc. These retroviruses have a conical core morphology in the electron microscope, possess complex genomes, all cause slowly progressive pathology (lenti = latin, slow ). 3 main groups (primate, feline, ungulate) with robust blocks to inter-species transmission. 7. Spumavirus - e.g. Human Foamy virus (HFV). Human retroviruses fall into three of these genera. Only for HIV-1/2 and HTLV-I has a causal role in disease been established. For HTLV-II and XMRV, it remains unclear what role, if any, these retroviruses play in disease. Human retroviruses HIV-1 o Ancestrally derived from a chimpanzee lentivirus called SIVcpz o Globally, the vast majority of HIV cases are caused by HIV-1. HIV-2 o Quite different from HIV-1 genetically, 40-60% amino acid sequence homology with HIV-1 o Identical mode of transmission but less transmissible o If disease occurs, identical clinical picture to disease caused by HIV-1 (but much lower rate of disease progression) o Derived from a lentivirus of sooty mangabeys (SIVsm) o Found predominantly in West Africa and Western India

4 4 HIV Virology HTLV-I (Human T cell lymphotropic virus type 1) o Endemic in Japan, the Caribbean, South America, Africa, and the Middle East o Most patients are asymptomatic o Causes T-cell leukemias/lymphomas and HTLV-I-associated myelopathy (HAM), also known as tropical spastic paraparesis HTLV-II o An orphan virus, not clearly linked to any disease XMRV - xenotropic murine retrovirus. o Similar genetically to mouse retroviruses o Recent associations reported with human prostate cancer and chronic fatigue syndrome (viral DNA and protein detection in prostate or WBCs respectively) but causal roles have in no way been established. These are regarded as tentative findings at present. Retroviruses are in turn members of a larger family of retroelements. For example, 8% of the human genome consists of endogenous retroviruses, which are no longer replicating but were inserted long ago into their genomic locations in our ancestors. In fact, approximately half of the human genome is recognizably derived from the products of reverse transcription of various retroelements. Retroviruses thus have two defining features: Reverse transcription into double-stranded cdna Integration of the cdna into a host chromosome Origins of HIV The only viruses very closely related to HIV-1 have been isolated from chimpanzees (SIVcpz in Pan troglodytes) from western equatorial Africa. The only species naturally infected with viruses closely related to HIV-2 is the sooty mangabey (SIVsm) from western Africa. Molecular clock analyses place last common ancestor of the HIV-1 M group prior to Jump from chimpanzees to humans occurred before then.

5 5 HIV Virology o Bushmeat hypothesis it is likely that HIV-1 spread to humans by parenteral inoculation of SIVcpz, perhaps during hunting/butchering, in West Africa, in southeastern Cameroon, about 100 years ago or so. o HIV-1 and HIV-2 have each arisen several times. In the case of HIV-1, the four groups (M, N, O and most recently, P) are the result of independent cross-species transmission events from chimpanzees. The M or Main group is the lentivirus that has spread world-wide. There are multiple M group subtypes (also known as clades). o These clades are unevenly distributed globally. The principal clade in North America, Europe, and Australia is clade B. HIV-1 clade C is the most prevalent clade in Southern and Eastern Africa HIV-1 Pathogenesis Initial Transmission and Spread Initially infects Langerhans cells (or CD4+ T cells) Fuses with local CD4 + T cells Infiltrates deeper tissues Within 48 to 72 hours after inoculation, HIV can spread to adjacent inguinal lymph nodes; Systemic dissemination and viremia typically develop after about 7 days after initial infection (range, 4 to 11 days): sore throat, fever, rash, malaise. Once viremia develops, HIV-1 extensively seeds lymphoid organs and the central nervous system The gut-associated lymphoid tissue (GALT) is particularly targeted by HIV-1. Recent evidence indicates that mucosal CD4 depletion there leads to increased microbial translocation (bacteria, LPS, other) from the gut. This is now thought to lead to continuous deleterious systemic immune activation and HIV-1 disease progression.

6 6 HIV Virology Target cells for HIV-1 in the body CD4 + T cell (major target) Monocyte-macrophage (major target) Langerhans cells of the skin Follicular dendritic cells Astrocytes Oligodendrocytes M cells of the enteric mucosa Epithelial cells of intestine and vagina HIV-1 Dynamics Approximately 10 billion (10 10 ) particles of HIV-1 are produced and cleared daily in an infected individual Generation time approx 2 days 2 billion CD4+ lymphocytes destroyed each day The entire supply of CD4 cells turns over approximately every 15 days Basic pathophysiology points to consider about transmission in regard to sexual PEP Virus can be found within antigen presenting cells trans-locating across the mucosa within 24 hours of exposure and in regional lymph nodes within hours, and in blood (viremia) within 5 days. Blood injection much more effective than sexual in transmitting the virus. Individuals with acute HIV-1 infection generally have the highest viral loads and are most likely to transmit the virus. Therefore, sexual networks are an important factor in sustaining the epidemic: individuals with multiple simultaneous partners are more likely to transmit HIV-1 during the highly infectious acute infection stage than those who engage in serial monogamy. Viral loads are also high during late disease (end-stage AIDS). HIV-1 Virus Structure Like other retroviruses, HIV-1 is an enveloped virus.

7 7 HIV Virology The HIV envelope is a lipid bilayer that was acquired from the host cell plasma membrane as the virus budded through the cell membrane There are two major glycoproteins associated with the HIV envelope, gp120 and gp 41 o gp120 forms knob of the envelope structure o gp41, a transmembrane protein anchored in the viral lipid bilayer, forms the stalk of the envelope structure, The nucleocapsid core contains the HIV genome and viral enzymes including reverse transcriptase, integrase, and protease enzymes as well as other proteins with structural and regulatory functions. The HIV genome consists of 2 copies of plus-sense, single stranded RNA molecules, each of approximately 9 kilobases in length. To be co-packaged into a virion, there is no requirement that each of the two RNAs come from the same integrated proviral DNA, only that they inhabit the same cell. Since reverse transcriptase can easily jump from one RNA strand to the other during reverse transcription, this has the consequence of allowing prolific recombination. o The clinical significance of this recombination is the emergence of circulating recombinant forms, which arise when two different viruses recombine. o In addition, two viruses each carrying a single drug-resistance mutation can recombine to make a virus that is more resistant. There are 3 major HIV-1 genes, gag, pol, and env: Gag encodes the main structural proteins including matrix, capsid, and nucleocapsid. Pol encodes enzymes such as reverse transcriptase, protease, and integrase Env encodes the envelope glycoproteins gp41 and gp120. There are six auxiliary or accessory HIV-1 genes as well: Tat, rev, nef, vif, vpr, and vpu. These genes have a variety of functions including regulatory, infectivity, virulence, replication, and virus release. Figure 2.

8 8 HIV Virology Figure 1. The structure of an HIV-1 virion. Photo courtesy of NIAID.

9 9 HIV Virology Figure 2. Genetic Structure of HIV-1. The genes are expressed via a complex splicing cascade controlled by the viral Rev protein, which binds to viral RNAs in the nucleus and acts as an adaptor to an mrna export pathway. This allows the virus to bypass the normal cellular checkpoint against exporting unspliced mrnas, e.g., the full-length HIV-1 genome RNA, from the nucleus. The HIV-1 accessory genes Vif, Vpr, Vpu, Nef and the Concept of Restriction Factors ( Intrinsic Immunity ). These four genes appear to defend HIV-1 against restriction factors (though some such as Nef and Vpr have other activities as well). Restriction factors make up a newly recognized branch of immunity termed Intrinsic Immunity. Intrinsic immunity involves antiviral proteins and RNAs which function to neutralize viruses early in replication. In contrast to adaptive immunity (antibodies, CTLs), or

10 10 HIV Virology innate immunity (e.g., interferons), they are cell-autonomous, constitutively expressed, and engage the virus immediately, as it enters the cell. Active within individual virus target cells (cell-autonomous). Limit infection of non-native host species (zoonotic transmission). Vif counteracts APOBEC3G, a cellular cytidine deaminase that otherwise enters the virion particle as it buds and then lethally edits the viral minus strand Cs to Us. Vif is an adaptor protein that steers APOBEC3G to the proteasome (the cellular protein recycling machinery). HIV-1 Vpu and Nef counteract Tetherin, an antiviral protein that restricts budding. Vpr counteracts an as yet unknown restriction factor. Another recently identified restriction factor is TRM5-alpha. This protein binds to the capsid of an incoming virion and disables it. Unfortunately, the HIV-1 capsid protein has evolved to evade human TRIM5alpha. But numerous monkey TRIM5-alpha proteins do block HIV-1. Thus HIV-1 is a zoonosis that can evade human restriction factors by means of an altered capsid that avoids human TRIM5alpha and Vif, Vpu, Vpr and Nef proteins that specifically destroy or inactivate other restriction factors.

11 11 HIV Virology Figure 3. Overview of the HIV-1 Life cycle. The incoming virion binds to CD4 and a coreceptor. Fusion is followed by reverse transcription, yielding the pre-integration complex (PIC), which is imported into the nucleus. There the viral cdna is integrated into a chromosome, becoming a provirus. The provirus is transcribed into the genomic RNA which is spliced to form messages for Tat, Rev and Nef. Tat buildup allows for viral transcription and Rev allows for the unspliced RNA to bypass the normal splicing checkpoint and be exported. Assembly and budding occur at the plasma membrane. Protease acts at this stage as well. Cleavage by protease converts the immature form to the mature conical form. HIV-1 entry HIV cell entry occurs in three stages. The first step of the HIV life cycle is binding to specific receptors on the cell surface, primarily CD4 receptor. This step is known as attachment. The envelope protein gp120 binds to the CD4 receptor. Attachment by itself was found not to be sufficient for HIV entry into murine cells. This led to the concept of a second receptor (co-receptor).

12 12 HIV Virology Expression cloning approach led to the discovery of 2 main co-receptors, the chemokine receptors CXCR4 and CCR5. o Chemokines (short for chemoattractant cytokines) are glycoproteins that play a role in activating the immune system's response to infection. o Their actions are mediated by a receptors called chemokine receptors. Viral isolates from HIV-1-infected persons in early HIV infection are predominantly M-tropic o CCR5 is the major coreceptor for M-tropic HIV-1 R5 isolates (Maraviroc blocks entry of R5 viruses) T-tropic virus is noted more commonly at lower CD4 cell counts and higher viral loads o CXCR4 is the major coreceptor for T-tropic X4 strains o CXCR4 usage tends to correlate with late stage HIV disease. This is not absolute. People can die from AIDS with just M-tropic viruses. The second step of the HIV life cycle is coreceptor binding. When the HIV glycoprotein gp120 binds to the CD4 receptor during attachment, it induces a conformational change in gp120 that exposes the coreceptor binding site This exposure of the coreceptor binding site allows binding of gp120 to the coreceptor Coreceptor binding triggers conformational changes in gp41 The third step of the HIV life cycle is known as fusion. Conformational changes in gp41 leads to the insertion of a fusion peptide into the target cell membrane, resulting in fusion between the cell and viral membranes Fusion allows the nucleocapsid, which contains the viral RNA genome and enzymes to enter the cytoplasm of the cell. HIV-1 Reverse Transcription After entry, the virus uncoats and reverse transcription takes place. The HIV reverse transcriptase is an RNA-dependent DNA polymerase.

13 13 HIV Virology During reverse transcription, a double-stranded DNA copy of the single-stranded genomic RNA is made. Reverse transcriptase does not have proof-reading capability. Thus, replication is error-prone resulting in the introduction of point mutations into each new copy of the viral DNA. Each of the ~10,000 nucleotides in the genome becomes mutated somewhere in the body at least once per day. Potential for selection of resistant mutants is enormous and is a main clinical challenge. All single drug resistance mutations pre-exist in vivo. They allow the unwary to re-demonstrate natural selection, quickly. Mathematics of selection: A single drug will always fail. Two drugs almost always fail. Three drugs work. The work because the chance of three different drug resistance mutations arising in the same viral genome is low enough. RT is key therapeutic target (many drugs now). Integration The integration of HIV-1 proviral DNA into the host cell genome is an obligate replication step of the HIV life cycle. Integration is catalyzed by the viral integrase and occurs in three main steps through a series of DNA cutting and joining reactions: 1. A dinucleotide is removed from each 3'-end of the viral DNA, a process termed 3'-end processing. 2. The resulting three-prime ends are joined to the 5 ends of the chromosome DNA, at a staggered distance about 5 nucleotides apart. This step is called DNA strand transfer 3. Unknown host cell enzymes repair the gap in the DNA chain by removing the two unpaired nucleotides at the 5'-ends of the viral DNA.

14 14 HIV Virology Figure 4. HIV-1 genome, with the viral integrase protein illustrated. Integration results in the permanent covalent recombination with host DNA, which yields the provirus. Integration allows HIV-1 to: Establish a permanent reservoir. Evade immune surveillance. Rebound if HAART is withdrawn (latency in resting memory T cells). ARCHIVE drug resistance mutations - serious clinical problem. Replicate through mitosis. In a patient on long-term HAART, the most stable reservoir of integrated proviruses is in rare resting memory T cells (roughly one million persist in the body of a patient with effective HAART). The half life of this reservoir is decades, meaning that HAART cannot be curative. Assembly and Budding (Protease Cleavage) Following integration, immune activation leads to transcription of the viral genome into viral subunits which are then exported to the cytoplasm for translation into viral proteins.

15 15 HIV Virology These viral proteins included genomic RNA as well as structural, enzymatic, and regulatory proteins. Among the viral proteins produced are Gag and Gag-Pol precursor polypeptides that are cleaved into their smaller functional components by the HIV-1 protease. The genomic RNA and viral proteins are packaged into a virion. The mature virion is released from the cell surface in a process called budding Figure 5. HIV-1 protease is released by auto-cleavage from the a long precursor and then acts to cleave other proteins such as capsid (CA), matrix (MA), reverse transcriptase (RT), and integrase (IN). Suggested Reading 1. Coffin, J., S. Hughes, and H. Varmus, Retroviruses. 1997, Cold Spring Harbor: Cold Spring Harbor Laboratory Press. 2. Freed, E.O., HIV-1 replication. Somat Cell Mol Genet, (1-6): p Bieniasz, P.D., Intrinsic immunity: a front-line defense against viral attack. Nat Immunol, (11): p Sharp, P.M., et al., The origins of acquired immune deficiency syndrome viruses: where and when? Philos Trans R Soc Lond B Biol Sci, (1410): p Blankson, J.N., D. Persaud, and R.F. Siliciano, The challenge of viral reservoirs in HIV-1 infection. Annu Rev Med, : p

16 16 HIV Virology Questions 1. Retroviruses of humans are known to: a. cause AIDS b.cause human T cel leukemia c. be detectable in some human prostate samples d.form a substantial part of the human genome e. all of the above. 2. HIV-1 shares with all other retroviruses the following genes a. vpr and nef b. tat and rev c. gag, pol and env d. gag and vpu e. vif 3. The origin of HIV-1 is thought be a. Zoonotic transfer of a simian (chimpanzee lentivirus) to humans, likely by percutaneous inoculation. b. Recombination with other human retroviruses such as XMRV and HTLV-I c. Repeated exposure to mosquito bites d. vaccines that got contaminated with monkey cells e. A biological weapon manufactured by the developed world 4. Gag encodes: a. Capsid, Matrix, nucleocapsid (main structural proteins of the viral core) b. Protease and reverse transcriptase c. Envelope glycoproteins d. Vif, Vpr, e. Tat, Rev 5. HIV-1 is: a. negative strand RNA virus

17 17 HIV Virology b. a DNA virus, with two copies of the DNA form of the genome in the particle c. a plus stranded RNA virus with two copies of the RNA form of the genome in the particle d. a plus stranded RNA virus with one sense and one antisense copy of the RNA form of the genome in the particle. e. a segmented virus with part of the genome encoded on each of two segments. 6. Restriction factors TRIM5-alpha and APOBEC3G a. Act immediately as the virus is in the process of infecting a cell b. Are counteracted by Capsid and Vif respectively c. Are produced by neighboring cells to prevent further viral spread. d. Enhance antibody binding f. a and b are correct. 7. If you could sample the virus in an untreated HIV-1 patient two weeks after infection and again ten years after infection, you would most likely find that she had: a. CCR5-using virus early and CXCR4 virus late, and in tissue culture the later virus would be more likely to replicate in T cell lines than macrophages. b. CXCR4-using virus early and CCR5 virus late, and in tissue culture the later virus would be more likely to replicate in T cell lines than macrophages. c. CCR5-using virus early and CXCR4 virus late, and in tissue culture the later virus would be more likely to replicate in macrophages than T cell lines. d. CXCR4-using virus and CCR5 virus late, and in tissue culture this later virus would be more likely to replicate in macrophages than infect T cell lines. e. A virus using both coreceptors but not CD4. 8. You evaluate an HIV-1-infected patient with a viral load of 155,000 copies per ml. You decide to prescribe a combination of AZT, lamivudine and lopinavir/ritonavir. You measure her viral load for the next five years and you never detect any viral RNA in her plasma (i.e, she has less than 50 copies per ml of plasma). You decide to continue therapy, although you switch the lopinavir/ritonavir to atazanvir/ritonavir because of

18 18 HIV Virology cholesterol and triglyceride elevations. She remains without detectable viremia on viral RNA load testing. At this point, viral DNA in her body is most likely to be found in: a. integrated from, in most naïve T cells b. integrated form, in rare naïve T cells. c. unintegrated form, in most resting memory T cells. d. integrated form in rare, resting memory T cells. e. unintegrated form, in rare resting memory T cells 9. An HIV-1 protease inhibitor would be predicted to prevent the following from occurring, EXCEPT: a. Production of infectious virions b. Infection of new cells c. Capsid interaction with TRIM5alpha d. Virions with conical morphology e. Assembly of Gag protein into budding particles and release at the plasma membrane 10. The most risky sexual exposure is generally: a. Receptive anal intercourse with a male who has chronic HIV-1 infection of undetermined duration b. Receptive anal intercourse with a male who has acute HIV-1 infection c. Insertive anal intercourse with a male who has chronic HIV-1 infection of undetermined duration d. Receptive vaginal intercourse with an uncircumcised male.

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