Platelet-derived growth factor protects neurons against gp120-mediated toxicity

Journal of NeuroVirology

Volumn 14, Issue 1, 2008, Pages 62-72

  Peng, Fuwang ^a   Dhillon, Navneet ^a   Callen, Shannon ^a   Yao, Honghong ^a   Bokhari, Sirosh ^b   Zhu, Xuhui ^a   Baydoun, Hicham H ^b   Buch, Shilpa J ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Gp120; HIV dementia; Neurons; PDGF

Indexed keywords

CASPASE 3; GLYCOPROTEIN GP 120; LACTATE DEHYDROGENASE; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN BAX; PROTEIN BCL XL; PROTEIN KINASE B;

APOPTOSIS; ARTICLE; CELL SHAPE; CONTROLLED STUDY; DEMENTIA; ENZYME ACTIVATION; ENZYME ASSAY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYPOTHESIS; INHIBITION KINETICS; NERVE CELL NECROSIS; NERVE FIBER GROWTH; NEURITE; NEUROPROTECTION; NEUROTOXICITY; NICK END LABELING; PRIORITY JOURNAL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; CASPASE 3; CELL LINE, TUMOR; CELL SHAPE; CEREBRAL CORTEX; CYTOPATHOGENIC EFFECT, VIRAL; ENZYME ACTIVATION; HIV ENVELOPE PROTEIN GP120; HUMANS; NEURITES; NEUROBLASTOMA; NEURONS; PLATELET-DERIVED GROWTH FACTOR; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 39849097691     PISSN: 13550284     EISSN: None     Source Type: Journal    
DOI: 10.1080/13550280701809084     Document Type: Article

References (70)

1. Adamson, D. C., Dawson, T. M., Zink, M. C., Clements, J. E. and Dawson, V. L. (1996) Neurovirulent simian immunodeficiency virus infection induces neuronal, endothelial, and glial apoptosis. Mol Med, 2, pp. 417-428.
2. Bachis, A. and Mocchetti, I. (2005) Brain-derived neurotrophic factor is neuroprotective against human immunodeficiency virus-1 envelope proteins. Ann N Y Acad Sci, 1053, pp. 247-257.
3. Bachis, A. and Mocchetti, I. (2006) Semisynthetic sphingoglycolipid LIGA20 is neuroprotective against human immunodeficiency virus-gp120-mediated apoptosis. J Neurosci Res, 83, pp. 890-896.
4. Bansal, A. K., Mactutus, C. F., Nath, A., Maragos, W., Hauser, K. F. and Booze, R. M. (2000) Neurotoxicity of HIV-1 proteins gp120 and Tat in the rat striatum. Brain Res, 879, pp. 42-49.
5. Bell, J. E. (1998) The neuropathology of adult HIV infection. Rev Neurol (Paris), 154, pp. 816-829.
6. Bergsten, E., Uutela, M., Li, X., Pietras, K., Ostman, A., Heldin, C. H., Alitalo, K. and Eriksson, U. (2001) PDGF-D is a specific, protease-activated ligand for the PDGF beta-receptor. Nat Cell Biol, 3, pp. 512-516.
7. Biard-Piechaczyk, M., Robert-Hebmann, V., Richard, V., Roland, J., Hipskind, R. A. and Devaux, C. (2000) Caspase-dependent apoptosis of cells expressing the chemokine receptor CXCR4 is induced by cell membrane-associated human immunodeficiency virus type 1 envelope glycoprotein (gp120). Virology, 268, pp. 329-344.
8. Brenneman, D. E., Westbrook, G. L., Fitzgerald, S. P., Ennist, D. L., Elkins, K. L., Ruff, M. R. and Pert, C. B. (1988) Neuronal cell killing by the envelope protein of HIV and its prevention by vasoactive intestinal peptide. Nature, 335, pp. 639-642.
9. Brewer, G. J., Torricelli, J. R., Evege, E. K. and Price, P. J. (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res, 35, pp. 567-576.
10. Budka, H. (1991) Neuropathology of human immunodeficiency virus infection. Brain Pathol, 1, pp. 163-175.
11. Cameron, A. A., Cliffer, K. D., Dougherty, P. M., Willis, W. D. and Carlton, S. M. (1991) Changes in lectin, GAP-43 and neuropeptide staining in the rat superficial dorsal horn following experimental peripheral neuropathy. Neurosci Lett, 131, pp. 249-252.
12. Cameron, R. S. and Rakic, P. (1991) Glial cell lineage in the cerebral cortex: A review and synthesis. Glia, 4, pp. 124-137.
13. Campus, G., Lumbau, A. and Bachisio, S. L. (2000) Caries experience and streptococci and lactobacilli salivary levels in 6-8-year-old Sardinians. Int J Paediatr Dent, 10, pp. 306-312.
14. Chen, Z., Huang, Y., Zhao, X., Skulsky, E., Lin, D., Ip, J., Gettie, A. and Ho, D. D. (2000) Enhanced infectivity of an R5-tropic simian/human immunodeficiency virus carrying human immunodeficiency virus type 1 subtype C envelope after serial passages in pig-tailed macaques (Macaca nemestrina). J Virol, 74, pp. 6501-6510.
15. Davis, C. B., Dikic, I., Unutmaz, D., Hill, C. M., Arthos, J., Siani, M. A., Thompson, D. A., Schlessinger, J. and Littman, D. R. (1997) Signal transduction due to HIV-1 envelope interactions with chemokine receptors CXCR4 or CCR5. J Exp Med, 186, pp. 1793-1798.
16. Dreyer, E. B., Kaiser, P. K., Offermann, J. T. and Lipton, S. A. (1990) HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists. Science, 248, pp. 364-367.
17. Everall, I. P., Bell, C., Mallory, M., Langford, D., Adame, A., Rockestein, E. and Masliah, E. (2002) Lithium ameliorates HIV-gp120-mediated neurotoxicity. Mol Cell Neurosci, 21, pp. 493-501.
18. Everall, I. P., Luthert, P. J. and Lantos, P. L. (1991) Neuronal loss in the frontal cortex in HIV infection. Lancet, 337, pp. 1119-1121.
19. Gendelman, H. E., Lipton, S. A., Tardieu, M., Bukrinsky, M. I. and Nottet, H. S. (1994) The neuropathogenesis of HIV-1 infection. J Leukoc Biol, 56, pp. 389-398.
20. Giacobini, M. M., Almstrom, S., Funa, K. and Olson, L. (1993) Differential effects of platelet-derived growth factor isoforms on dopamine neurons in vivo: -BB supports cell survival, -AA enhances fiber formation. Neuroscience, 57, pp. 923-929.
21. Hanai, Y., Tokuda, H., Ohta, T., Matsushima-Nishiwaki, R., Takai, S. and Kozawa, O. (2006) Phosphatidylinositol 3-kinase/Akt auto-regulates PDGF-BB-stimulated interleukin-6 synthesis in osteoblasts. J Cell Biochem, 99, pp. 1564-1571.
22. Hashimoto, M., Sagara, Y., Langford, D., Everall, I. P., Mallory, M., Everson, A., Digicaylioglu, M. and Masliah, E. (2002) Fibroblast growth factor 1 regulates signaling via the glycogen synthase kinase-3beta pathway. Implications for neuroprotection. J Biol Chem, 277, pp. 32985-32991.
23. Heldin, C. H., Eriksson, U. and Ostman, A. (2002) New members of the platelet-derived growth factor family of mitogens. Arch Biochem Biophys, 398, pp. 284-290.
24. Herbein, G., Mahlknecht, U., Batliwalla, F., Gregersen, P., Pappas, T., Butler, J., O'Brien, W. A. and Verdin, E. (1998) Apoptosis of CD8+ T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature, 395, pp. 189-194.
25. Hesselgesser, J., Liang, M., Hoxie, J., Greenberg, M., Brass, L. F., Orsini, M. J., Taub, D. and Horuk, R. (1998) Identification and characterization of the CXCR4 chemokine receptor in human T cell lines: ligand binding, biological activity, and HIV-1 infectivity. J Immunol, 160, pp. 877-883.
26. Hesselgesser, J., Taub, D., Baskar, P., Greenberg, M., Hoxie, J., Kolson, D. L. and Horuk, R. (1998) Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1 alpha is mediated by the chemokine receptor CXCR4. Curr Biol, 8, pp. 595-598.
27. Hof, P. R., Lee, P. Y., Yeung, G., Wang, R. F., Podos, S. M. and Morrison, J. H. (1998) Glutamate receptor subunit GluR2 and NMDAR1 immunoreactivity in the retina of macaque monkeys with experimental glaucoma does not identify vulnerable neurons. Exp Neurol, 153, pp. 234-241.
28. Hynds, D. L., Burry, R. W. and Yates, A. J. (1997) Gangliosides inhibit growth factor-stimulated neurite outgrowth in SH-SY5Y human neuroblastoma cells. J Neurosci Res, 47, pp. 617-625.
29. Kaul, M., Garden, G. A. and Lipton, S. A. (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature, 410, pp. 988-994.
30. Klein, R. S., Williams, K. C., Alvarez-Hernandez, X., Westmoreland, S., Force, T., Lackner, A. A. and Luster, A. D. (1999) Chemokine receptor expression and signaling in macaque and human fetal neurons and astrocytes: Implications for the neuropathogenesis of AIDS. J Immunol, 163, pp. 1636-1646.
31. Kozak, S. L., Kuhmann, S. E., Platt, E. J. and Kabat, D. (1999) Roles of CD4 and coreceptors in binding, endocytosis, and proteolysis of gp120 envelope glycoproteins derived from human immunodeficiency virus type 1. J Biol Chem, 274, pp. 23499-23507.
32. Kruman, I., Guo, Q. and Mattson, M. P. (1998) Calcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC12 cells. J Neurosci Res, 51, pp. 293-308.
33. Kulik, G., Klippel, A. and Weber, M. J. (1997) Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol Cell Biol, 17, pp. 1595-1606.
34. Li, X., Ponten, A., Aase, K., Karlsson, L., Abramsson, A., Uutela, M., Backstrom, G., Hellstrom, M., Bostrom, H., Li, H., Soriano, P., Betsholtz, C., Heldin, C. H., Alitalo, K., Ostman, A. and Eriksson, U. (2000) PDGF-C is a new protease-activated ligand for the PDGF alpha-receptor. Nat Cell Biol, 2, pp. 302-309.
35. Lipton, S. A. and Gendelman, H. E. (1995) Seminars in medicine of the Beth Israel Hospital, Boston. Dementia associated with the acquired immunodeficiency syndrome. N Engl J Med, 332, pp. 934-940.
36. Lipton, S. A., Sucher, N. J., Kaiser, P. K. and Dreyer, E. B. (1991) Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron, 7, pp. 111-118.
37. McArthur, J. C., Brew, B. J. and Nath, A. (2005) Neurological complications of HIV infection. Lancet Neurol, 4, pp. 543-555.
38. McArthur, J. C., Haughey, N., Gartner, S., Conant, K., Pardo, C., Nath, A. and Sacktor, N. (2003) Human immunodeficiency virus-associated dementia: An evolving disease. J NeuroVirol, 9, pp. 205-221.
39. McArthur, J. C., Hoover, D. R., Bacellar, H., Miller, E. N., Cohen, B. A., Becker, J. T., Graham, N. M., McArthur, J. H., Selnes, O. A. and Jacobson, L. P. (1993) Dementia in AIDS patients: Incidence and risk factors. Multicenter AIDS Cohort Study. Neurology, 43, pp. 2245-2252.
40. Meucci, O. and Miller, R. J. (1996) gp120-induced neurotoxicity in hippocampal pyramidal neuron cultures: Protective action of TGF-beta1. J Neurosci, 16, pp. 4080-4088.
41. Mohapel, P., Frielingsdorf, H., Haggblad, J., Zachrisson, O. and Brundin, P. (2005) Platelet-derived growth factor (PDGF-BB) and brain-derived neurotrophic factor (BDNF) induce striatal neurogenesis in adult rats with 6-hydroxydopamine lesions. Neuroscience, 132, pp. 767-776.
42. Mucke, L., Masliah, E. and Campbell, I. L. (1995) Transgenic models to assess the neuropathogenic potential of HIV-1 proteins and cytokines. Curr Top Microbiol Immunol, 202, pp. 187-205.
43. Nath, A. (1999) Pathobiology of human immunodeficiency virus dementia. Semin Neurol, 19, pp. 113-127.
44. Navia, B. A., Jordan, B. D. and Price, R. W. (1986) The AIDS dementia complex: I. Clinical features. Ann Neurol, 19, pp. 517-524.
45. New, D. R., Ma, M., Epstein, L. G., Nath, A. and Gelbard, H. A. (1997) Human immunodeficiency virus type 1 Tat protein induces death by apoptosis in primary human neuron cultures. J NeuroVirol, 3, pp. 168-173.
46. Nikkhah, G., Odin, P., Smits, A., Tingstrom, A., Othberg, A., Brundin, P., Funa, K. and Lindvall, O. (1993) Platelet-derived growth factor promotes survival of rat and human mesencephalic dopaminergic neurons in culture. Exp Brain Res, 92, pp. 516-523.
47. Othberg, A., Odin, P., Ballagi, A., Ahgren, A., Funa, K. and Lindvall, O. (1995) Specific effects of platelet derived growth factor (PDGF) on fetal rat and human dopaminergic neurons in vitro. Exp Brain Res, 105, pp. 111-122.
48. Patel, C. A., Mukhtar, M. and Pomerantz, R. J. (2000) Human immunodeficiency virus type 1 Vpr induces apoptosis in human neuronal cells. J Virol, 74, pp. 9717-9726.
49. Price, R. W., Brew, B., Sidtis, J., Rosenblum, M., Scheck, A. C. and Cleary, P. (1988) The brain in AIDS: Central nervous system HIV-1 infection and AIDS dementia complex. Science, 239, pp. 586-592.
50. Price, R. W., Sidtis, J. J. and Brew, B. J. (1991) AIDS dementia complex and HIV-1 infection: A view from the clinic. Brain Pathol, 1, pp. 155-162.
51. Romashkova, J. A. and Makarov, S. S. (1999) NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature, 401, pp. 86-90.
52. Rubinfeld, H. and Seger, R. (2005) The ERK cascade: A prototype of MAPK signaling. Mol Biotechnol, 31, pp. 151-174.
53. Sacktor, N., Lyles, R. H., Skolasky, R., Kleeberger, C., Selnes, O. A., Miller, E. N., Becker, J. T., Cohen, B. and McArthur, J. C. (2001) HIV-associated neurologic disease incidence changes: Multicenter AIDS Cohort Study, 1990-1998. Neurology, 56, pp. 257-260.
54. Sanders, V. J., Everall, I. P., Johnson, R. W. and Masliah, E. (2000) Fibroblast growth factor modulates HIV coreceptor CXCR4 expression by neural cells. HNRC Group. J Neurosci Res, 59, pp. 671-679.
55. Simakajornboon, N., Szerlip, N. J., Gozal, E., Anonetapipat, J. W. and Gozal, D. (2001) In vivo PDGF beta receptor activation in the dorsocaudal brainstem of the rat prevents hypoxia-induced apoptosis via activation of Akt and BAD. Brain Res, 895, pp. 111-118.
56. Singh, I. N., Goody, R. J., Dean, C., Ahmad, N. M., Lutz, S. E., Knapp, P. E., Nath, A. and Hauser, K. F. (2004) Apoptotic death of striatal neurons induced by human immunodeficiency virus-1 Tat and gp120: Differential involvement of caspase-3 and endonuclease G. J NeuroVirol, 10, pp. 141-151.
57. Smits, A., Kato, M., Westermark, B., Nister, M., Heldin, C. H. and Funa, K. (1991) Neurotrophic activity of platelet-derived growth factor (PDGF): Rat neuronal cells possess functional PDGF beta-type receptors and respond to PDGF. Proc Natl Acad Sci U S A, 88, pp. 8159-8163.
58. Spencer, D. C. and Price, R. W. (1992) Human immunodeficiency virus and the central nervous system. Annu Rev Microbiol, 46, pp. 655-693.
59. Sui, Y., Potula, R., Dhillon, N., Pinson, D., Li, S., Nath, A., Anderson, C., Turchan, J., Kolson, D., Narayan, O. and Buch, S. (2004) Neuronal apoptosis is mediated by CXCL10 overexpression in simian human immunodeficiency virus encephalitis. Am J Pathol, 164, pp. 1557-1566.
60. Sung, J. Y., Lee, S. Y., Min, D. S., Eom, T. Y., Ahn, Y. S., Choi, M. U., Kwon, Y. K. and Chung, K. C. (2001) Differential activation of phospholipases by mitogenic EGF and neurogenic PDGF in immortalized hippocampal stem cell lines. J Neurochem, 78, pp. 1044-1053.
61. Trotot, P. M. and Gray, F. (1997) Diagnostic imaging contribution in the early stages of HIV Infection of the brain. Neuroimaging Clin N Am, 7, pp. 243-260.
62. Tseng, H. C. and Dichter, M. A. (2005) Platelet-derived growth factor-BB pretreatment attenuates excitotoxic death in cultured hippocampal neurons. Neurobiol Dis, 19, pp. 77-83.
63. Ullrich, A. and Schlessinger, J. (1990) Signal transduction by receptors with tyrosine kinase activity. Cell, 61, pp. 203-212.
64. Ullrich, C. K., Groopman, J. E. and Ganju, R. K. (2000) HIV-1 gp120- and gp160-induced apoptosis in cultured endothelial cells is mediated by caspases. Blood, 96, pp. 1438-1442.
65. Vogelbaum, M. A., Tong, J. X., Higashikubo, R., Gutmann, D. H. and Rich, K. M. (1998) Transfection of C6 glioma cells with the bax gene and increased sensitivity to treatment with cytosine arabinoside. J Neurosurg, 88, pp. 99-105.
66. Vogelbaum, M. A., Tong, J. X. and Rich, K. M. (1998) Developmental regulation of apoptosis in dorsal root ganglion neurons. J Neurosci, 18, pp. 8928-8935.
67. Wang, L., Zhang, Z Gang, Zhang, R Lan and Chopp, M. (2005) Activation of the PI3-K/Akt pathway mediates cGMP enhanced-neurogenesis in the adult progenitor cells derived from the subventricular zone. J Cereb Blood Flow Metab, 25, pp. 1150-1158.
68. Wright, K. M., Vaughn, A. E. and Deshmukh, M. (2007) Apoptosome dependent caspase-3 activation pathway is non-redundant and necessary for apoptosis in sympathetic neurons. Cell Death Differ, 14, pp. 625-633.
69. Zhang, L., Zhou, R. and Xiang, G. (2005) Stepholidine protects against H2O2 neurotoxicity in rat cortical neurons by activation of Akt. Neurosci Lett, 383, pp. 328-332.
70. Zhang, S. X., Gozal, D., Sachleben Jr, L. R., Rane, M., Klein, J. B. and Gozal, E. (2003) Hypoxia induces an autocrine-paracrine survival pathway via platelet-derived growth factor (PDGF)-B/PDGF-beta receptor/ phosphatidylinositol 3-kinase/Akt signaling in RN46A neuronal cells. FASEB J, 17, pp. 1709-1711.