The Neuropathology of AIDS

The Neuropathology of AIDS

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AIDS (acquired immune deficiency syndrome) is a disease of an individual’s immune system caused by HIV-1 (human immunodeficiency virus 1). HIV-1 is a retrovirus of the lentivirus subfamily. This virus is atypical in that it does not require mitotically active cells to reproduce. Reproduction of the viral nucleic acids occurs in the nucleus of infected cells. Until recently it was believed that AIDS related deaths as a result of HIV infection were caused primarily by opportunistic infections, usually bacterial or fungal, gaining a foothold in an immuno-compromised individual. Many of these secondary infections are the result of T-cell mediated immunodeficiency induced by HIV. The sequels of HIV infection often leads to a neuropathological state as a result of unusual secondary infections such as Toxoplasmosis. Postmortem studies have demonstrated that in addition to secondary infection, neurological manifestations may be due to vascular events, tumors (CNS lymphoma) and direct HIV-1 infection. In humans, HIV is known to infect T-lymphocytes within the body binding to the CD-4 receptors present on the cell surface, but in the brain, recent studies have suggested that microglial cells and macrophages serve as the reservoirs of HIV. Direct central nervous system infection by HIV results in a condition known as AIDS Dementia Complex and as such will serve as the topic of this paper.

AIDS Dementia Complex is defined as a constellation of signs and symptoms characterized by cognitive and motor decline. HIV-1 infection occurs early in the course of the disease and may be the sole symptom of infection. HIV encephalopathy is the most common neurological disorder of HIV positive individuals, even more common than neurological opportunistic infections. HIV encephalopathy is characterized by slowly progressing cognitive impairment, psychomotoric slowing and increased apathy, and is limited exclusively to the late stages of HIV infection. It is estimated that between 40 to 70 percent of full-blown AIDS patients are affected by HIV encephalopathy. The mechanism by which HIV invades the brain and causes the subsequent encephalopathy are yet to be fully understood. It has been hypothesized that indirect effects of HIV infection of the brain are the most pathogenic factors. Certain viral proteins and cytokines produced by infected macrophages or activated microglia induce neuronal dysfunction and loss of nerve cells. An understanding of the role of microglia and its relationship with surrounding neuroglial cells appears to be vital.

Microglial cells are present at all levels of the neuroaxis including the spinal cord.

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Differences in concentration of microglia do exist, with the basal ganglia and cerebellum having more than the cerebral cortex. Variation in the regional distribution of microglia helps to explain the pattern of distribution of HIV-1 antigen of CNS infected patients. The basal ganglia, subthalamic nucleus, substantia nigra and dentate nucleus in addition to the cerebral white matter show increased concentrations of HIV-1 invasion. Involvement of these extrapyramidal nuclei may correlate with some of the motor deficiencies common to AIDS Dementia Complex, but a full explanation cannot be obtained from this information alone. It has been surmised that neurological dysfunction may be related to toxic factors derived from the virus. Studies have shown the viral envelope protein, gpl20, to have toxic effects on neurons located in the cortex by effecting an increase in intracellular calcium levels. Further research correlating the regional distribution of microglia and the toxic factors derived from them may lead to an explanation of the motor decline associated with AIDS Dementia Complex.

Staining methods which differentiate microglial and cholinergic neurons have shown a close physical relationship between the two in the basal forebrain. In vitro studies suggest that microglia may express mRNA for nerve growth factor by which basal forebrain cholinergic neurons are known to be stimulated. It has been hypothesized that alterations in microglia, which have been shown to occur by HIV-1 infection, may have profound functional effects on neurons by disrupting the normal microglial-neuronal interaction. Normal function of cholinergic basal forebrain neurons is essential for normal cognitive function and may therefore be responsible for the cognitive dementia associated with AIDS Dementia Complex.

Another relationship between neuroglial cells which has been suspected in the symptomology of HIV encephalopathy, is that between microglia and astrocytes. Astrocytes provide structural support for nervous tissue, and their extensions form a sealed barrier that protects the CNS and helps regulate the environment necessary for the complex procedures involved in electrical signaling. In vitro studies have demonstrated the existence of a colony stimulating factor (CSF) produced at increased rates by macrophages during systemic infections. Macrophage CSF promotes the survival and differentiation of microglia which subsequently secrete the inflammatory cytokines Interleukin-1 (IL-1) and tumor necrosis factor (TNF). These two cytokines have been shown to stimulate astrocyte proliferation. A feedback circuit exists in which astrocyte secretion of IL-3 stimulates microglia proliferation. Therefore, it has been suspected that alteration in microglial properties by either direct or systemic infection by HIV-1 may disrupt the homeostasis between microglia and astrocytes and result in astrocytic gliosis.

To date, the mechanism of entry into the CNS is unresolved. It has been generally excepted that the virus enters the CNS via the blood stream as opposed to retrograde transport via peripheral nerves. Current research has focused on the mode of entry into the CNS as either cell-associated virus (Trojan horse hypothesis) or by cell-free virus (viremia). Two different cell-associated transport mechanisms have been studied based upon the projection of a currently unknown mode of microglial turnover. The first hypothesis is based on the belief that normal microglial turnover occurs by monocytes crossing the blood-brain barrier and differentiating. With differentiation of HIV infected monocytes into microglia, HIV-1 could become activated. In this hypothesis, monocyte entry into the CNS would not require a pre-existing inflammatory lesion, but would occur as part of the normal physiologic turnover of the resident macrophage population. The second hypothesis requires an inflammatory response which recruits resident macrophages and in the process aids in the transport to the CNS via passive deterioration of the blood-brain barrier due to inflammation. Supporters of the cell -free virus hypothesis claim that entry of HIV-1 is attained via infection of the choroid plexus. The mechanism would result in dissemination of HIV-1 via the cerebrospinal fluid pathways. It should be noted that the highest concentration of free virus in any of the body fluids is within the cerebrospinal fluid.

The single most difficult factor to explain in association with HIV infection and the subsequent appearance of AIDS Dementia Complex is how neurological disease can result from relatively few infected cells with a low copy number of virus per infected cell. Some patients have very low levels of active viral infection and yet clinically apparent neuronal dysfunction. For example, children less than 3 years old with HIV encephalopathy have very low levels of active viral infection while children older than three years old have antigen levels comparable to adults. Low or absent active viral infection indicates the existence of an alternative mechanism involved in neuronal dysfunction.

Much research is currently being conducted in an attempt to find a cure for AIDS. As the range of diseases associated with AIDS increases, the difficulty in understanding the mechanism of action as well as pinpointing a site of pharmacological intervention increases dramatically. With the understanding of the pathological functions of HIV-1 still forthcoming, current biochemical studies of various types of ribozymes (catalytic RNA’s) have been conducted in an effort to cleave the retrovirus introduced HIV from the host cell DNA. Research in the field of gene therapy has improved the techniques used to introduce genetically altered information into the cell. Experiments have been performed in humans confirming that defective retrovirus vectors can be safely used to transfer new genetic information to the lympho-hematopoietic system. This research is very beneficial in providing a delivery system for anti-HIV ribozymes to the hematopoietic stem cell population. These cells would presumably have a proliferative advantage once transplanted and thus could reconstitute a HIV-resistant hematopoietic system. Thus, ribozymes in conjunction with gene therapy offer a vast array of potential as therapeutic agents in the fight against the fatal diseases associated with AIDS.

Works Cited:

Cournoyer,D. & Caskey, C. T. Gene Therapy of Immune System. Annual Review of Immunology, 1993, 11: 297-329.

Dickson, D. W., Mattiace, L. A,, Kure, K., Hutchins, K., Lyman, W. D. & Brosnan-, C. F. Biology of Disease: Microglia in Human Disease, With An Emphasis on Acquired Immune Deficiency Syndrome. Laboratory Investigation, 1991, 64: 135-156.

Navia, B. A., Cho, E., Petito, C. K. & Price, R. W. The AIDS Dementia Complex: II. Neuropathology. Annals of Neurology, 1986, 19(6): 525-535.

Navia, B. A,, Jordan, B. D. & Price, R. W. The AIDS Dementia Complex: I. Clinical Features. Annals of Neurology, 1986, 19(6): 517-524.

Schielke, E. HIV encephalopathy—clinical aspects, neuropathology and pathogenesis. Nervenarzt, 1993, 64(2): 83-90 (abstract).

Weidenheim, K. M., Epshteyn, I. & Lyman, W. D. Immunocytochemical identification of T-cells in HIV-1 encephalitis: implication for pathogenesis of CNS disease. Modern Pathology, 1993, 6(2): 167-174.
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