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Substance P and Human Immunodeficiency Virus Infection: Psychoneuroimmunology

Published online by Cambridge University Press:  07 November 2014

Wen-Zhe Ho ,
Dwight L. Evans  and
Steven D. Douglas
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Abstract

Effects on the immune system caused by changes in behavioral state or brain activity are mediated, at least in part, through neuroendocrine-immune pathways. Life stress and depression may be associated with altered blood levels of central nervous system-released neuropeptides, including substance P (SP). SP acts as a neuroregulator or neurotransmitter in the conduction of nociceptive stimuli, and is a modulator of neuroimmunoregulation. This review summarizes current knowledge regarding the role of the neuropeptide, SP, in psychoneuroimmunology, in particular as it relates to human immunodeficiency virus infection and acquired immunodeficiency disease syndrome. The association between depression, anxiety, and stress in HIV-disease progression suggests that neurobiologic and neurophysiologic factors play a role in modulating HIV infection and responses to antiretroviral therapy. Individuals with HIV or AIDS may experience stressful life circumstances that can result in increased symptoms of anxiety, stress, and/or depression. Furthermore, psychological and psychiatric symptoms, which occur in individuals with HIV and AIDS, may be related to the progression of AIDS disease. This review presents evidence from the literature, as well as findings from basic investigations conducted in the authors' laboratories, demonstrating that SP may play an important role in HIV pathophysiology. SP can impact the susceptibility of immune cells to HIV infection and modulate immune cell functions in ways that may affect the course of HIV in infected individuals. Moreover, modulation of SP activity and SP receptor is being explored for its potential as a novel therapeutic approach to the treatment of some psychological and psychiatric disorders and to the design of new anti-HIV therapy.

Type
Review
Information
CNS Spectrums , Volume 7 , Issue 12: Investigating Neuropsychiatric Disorders , December 2002 , pp. 867 - 874
Copyright
Copyright © Cambridge University Press 2002

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References

REFERENCES

1.Koff, WC, Dunegan, MA. Modulation of macrophage-mediated tumoricidal activity by neuropeptides and neurohormones. J Immunol. 1985;135:350–354.CrossRefGoogle ScholarPubMed
2.Payan, DG, Brewster, DR, Missirian-Bastian, A, Goetzl, EJ. Substance P recognition by a subset of human T lymphocytes. J Clin Invest. 1984;74:1532–1539.CrossRefGoogle ScholarPubMed
3.Malek-Ahmadi, P. Substance P and neuropsychiatric disorders: an overview. Neurosci Biobehav Rev. 1992;16:365–369.CrossRefGoogle ScholarPubMed
4.Harrison, S, Geppetti, P. Substance, P. Int J Biochem Cell Biol. 2001;33:555–576.CrossRefGoogle Scholar
5.Hassan, NF, Douglas, SD. Stress-related neuroimmunomodulation of monocyte-macrophage functions in HIV-1 infection. Clin Immunol Immunopathol. 1990;54:220–227.CrossRefGoogle ScholarPubMed
6.Evans, DL, Leserman, J, Perkins, DO, et al.Stress-associated reductions of cytotoxic T lymphocytes and natural killer cells in asymptomatic HIV infection. Am J Psychiatry. 1995;152:543–550.Google ScholarPubMed
7.Leserman, J, Petitto, JM, Perkins, DO, et al.Severe stress, depressive symptoms, and changes in lymphocyte subsets in human immunodeficiency virus-infected men. A 2-year follow-up study. Arch Gen Psychiatry. 1997;54:279–285.CrossRefGoogle Scholar
8.Evans, DL, Ten Have, TR, Douglas, SD, et al.Association of depression with viral load, CD8 T lymphocytes, and natural killer cells in women with HIV infection. Am J Psychiatry. 2002;159:1752–1759.CrossRefGoogle ScholarPubMed
9.Evans, DL, Mason, K, Bauer, R, Leserman, J, Petitto, JM. Neuropsychiatric manifestations of HIV-1 infection and AIDS. In: Charney, D, Coyle, J, Davis, K, Nemeroff, CB, eds. Neuropsychopharmacology: The Fifth Generation of Progress. New York, NY: Raven Press; 2002.Google Scholar
10.Evans, DL, Folds, JD, Petitto, JM, et al.Circulating natural killer cell phenotypes in men and women with major depression. Relation to cytotoxic activity and severity of depression. Arch Gen Psychiatry. 1992;49:388–395.CrossRefGoogle ScholarPubMed
11.Herbert, TB, Cohen, S. Depression and immunity: a meta-analytic review. Psychol Bull. 1993;113:472–486.CrossRefGoogle ScholarPubMed
12.Irwin, M. Psychoneuroimmunology of depression: clinical implications. Brain Behav Immun. 2002;16:1–16.CrossRefGoogle ScholarPubMed
13.Petitto, JM, Lewis, MH, Lysle, DT, et al.Behavioral states and immune responsiveness. In: Goodkin, K, Visser, AP, eds. Psychoneuroimmunology. Washington, DC: American Psychiatric Press, Inc.; 2000.Google Scholar
14.Gumnick, JF, Evans, DL, Miller, AH. Nervous, endocrine and Immune system interactions in psychiatry. In: Yudofsky, SC, Hales, RC, eds. Textbook of Neuropsychiatry and Clinical Neurosciences. Washington, DC: American Psychiatric Press, Inc.; 2002.Google Scholar
15.Fehder, WP, Sachs, J, Uvaydova, M, Douglas, SD. Substance P as an immune modulator of anxiety. Neuroimmunomodulation. 1997;4:42–48.CrossRefGoogle ScholarPubMed
16.Longmore, J, Hill, RG, Hargreaves, RJ. Neurokinin-receptor antagonists: pharmacological tools and therapeutic drugs. Can J Physiol Pharmacol. 1997;75:612–621.CrossRefGoogle ScholarPubMed
17.Payan, DG, McGillis, JP, Goetzl, EJ. Neuroimmunology. Adv Immunol. 1986;39:299–323.CrossRefGoogle ScholarPubMed
18.Takahashi, K, Tanaka, A, Hara, M, Nakanishi, S. The primary structure and gene organization of human substance P and neuromedin K receptors. Eur J Biochem. 1992;204:1025–1033.CrossRefGoogle ScholarPubMed
19.Dunn, AJ. Nervous system-immune system interactions: an overview. J Recept Res. 1988;8:589–607.CrossRefGoogle ScholarPubMed
20.Payan, DG. Neuropeptides and inflammation: the role of substance P. Annu Rev Med. 1989;40:341–352.CrossRefGoogle ScholarPubMed
21.McGillis, JP, Mitsuhashi, M, Payan, DG. Immunomodulation by tachykinin neuropeptides. Ann N YAcad Sci. 1990;594:85–94.CrossRefGoogle ScholarPubMed
22.Lembeck, F, Gamse, R. Substance P in peripheral sensory processes. Ciba Found Symp 1982;91:35–54.Google Scholar
23.Matsuda, H, Kawakita, K, Kiso, Y, Nakano, T, Kitamura, Y. Substance P induces granulocyte infiltration through degranulation of mast cells. J Immunol. 1989;142:927–931.CrossRefGoogle ScholarPubMed
24.Nieber, K, Baumgarten, CR, Rathsack, R, Furkert, J, Oehme, P, Kunkel, G. Substance P and beta-endorphin-like immunoreactivity in lavage fluids of subjects with and without allergic asthma. J Allergy Clin Immunol. 1992;90:646–652.CrossRefGoogle ScholarPubMed
25.Cappugi, P, Tsampau, D, Lotti, T. Substance P provokes cutaneous erythema and edema through a histamine-independent pathway. Int J Dermatol. 1992;31:206–209.CrossRefGoogle ScholarPubMed
26.Befus, AD, Lee, T, Bienenstock, J. Immunologic and physiologic features of mast cell function at mucosal surfaces. In: Mucosal Immunity and Infections at Mucosal Surfaces. New York, NY: Oxford University Press; 1988;209.Google Scholar
27.Michaels, LA, Ohene-Frempong, K, Zhao, H, Douglas, SD. Serum levels of substance P are elevated in patients with sickle cell disease and increase further during vaso-occlusive crisis. Blood. 1998;92:3148–3151.CrossRefGoogle ScholarPubMed
28.Tripp, RA, Moore, D, Winter, J, Anderson, LJ. Respiratory syncytial virus infection and G and/or SH protein expression contribute to substance P, which mediates inflammation and enhanced pulmonary disease in BALB/c mice. J Virol. 2000;74:1614–1622.CrossRefGoogle ScholarPubMed
29.Bozic, CR, Lu, B, Hopken, UE, Gerard, C, Gerard, NP. Neurogenic amplification of immune complex inflammation. Science. 1996;273:1722–1725.CrossRefGoogle ScholarPubMed
30.Lambrecht, BN, Germonpre, PR, Everaert, EG, et al.Endogenously produced substance P contributes to lymphocyte proliferation induced by dendritic cells and direct TCR ligation. Eur J Immunol. 1999;29:3815–3825.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
31.Marriott, I, Bost, KL. Expression of authentic substance P receptors in murine and human dendritic cells. J Neuroimmunol. 2001;114:131–141.CrossRefGoogle ScholarPubMed
32.Lai, JP, Zhan, GX, Campbell, DE, Douglas, SD, Ho, WZ. Detection of substance P and its receptor in human fetal microglia. Neuroscience. 2000;101:1137–1144.CrossRefGoogle ScholarPubMed
33.Ho, WZ, Lai, JP, Zhu, XH, Uvaydova, M, Douglas, SD. Human monocytes and macrophages express substance P and neurokinin-1 receptor. J Immunol. 1997;159:5654–5660.CrossRefGoogle ScholarPubMed
34.Lai, JP, Douglas, SD, Ho, WZ. Human lymphocytes express substance P and its receptor. J Neuroimmunol. 1998;86:80–86.CrossRefGoogle ScholarPubMed
35.Lai, JP, Douglas, SD, Rappaport, E, Wu, JM, Ho, WZ. Identification of a delta isoform of preprotachykinin mRNA in human mononuclear phagocytes and lymphocytes. J Neuroimmunol. 1998;91:121–128.CrossRefGoogle ScholarPubMed
36.De Giorgio, R, Tazzari, PL, Barbara, G, Stanghellini, V, Corinaldesi, R. Detection of substance P immunoreactivity in human peripheral leukocytes. J Neuroimmunol. 1998;82:175–181.CrossRefGoogle ScholarPubMed
37.Lai, JP, Douglas, SD, Shaheen, F, Pleasure, DE, Ho, WZ. Quantification of substance p mRNA in human immune cells by real-time reverse transcriptase PCR assay. Clin Diagn Lab Immunol. 2002;9:138–143.Google ScholarPubMed
38.Bost, KL, Pascual, DW. Substance P: a late-acting B lymphocyte differentiation cofactor. Am J Physiol. 1992;262:C537–C545.CrossRefGoogle ScholarPubMed
39.Stanisz, AM, Scicchitano, R, Dazin, P, Bienenstock, J, Payan, DG. Distribution of substance P receptors on murine spleen and Peyer's patch T and B cells. J Immunol. 1987;139:749–754.CrossRefGoogle ScholarPubMed
40.Lucey, DR, Novak, JM, Polonis, VR, Liu, Y, Gartner, S. Characterization of substance P binding to human monocytes/macrophages. Clin Diagn Lab Immunol. 1994;1:330–335.CrossRefGoogle ScholarPubMed
41.Wozniak, A, McLennan, G, Betts, WH, Murphy, GA, Scicchitano, R. Activation of human neutrophils by substance P: effect on FMLP-stimulated oxidative and arachidonic acid metabolism and on antibody-dependent cell-mediated cytotoxicity. Immunology. 1989;68:359–364.Google ScholarPubMed
42.Shanahan, F, Denburg, JA, Fox, J, Bienenstock, J, Befus, D. Mast cell heterogeneity: effects of neuroenteric peptides on histamine release. J Immunol. 1985;135:1331–1337.CrossRefGoogle ScholarPubMed
43.Bost, KL. Quantification of macrophage-derived substance P receptor mRNA using competitive polymerase chain reaction. Adv Exp Med Biol. 1995;373:219–223.CrossRefGoogle ScholarPubMed
44.Bost, KL, Breeding, SA, Pascual, DW. Modulation of the mRNAs encoding substance P and its receptor in rat macrophages by LPS. Reg Immunol. 1992;4:105–112.Google ScholarPubMed
45.Lai, JP, Douglas, SD, Zhao, M, Ho, WZ. Quantification of substance P mRNA in human mononuclear phagocytes and lymphocytes using a mimic-based RT-PCR. J Immunol Methods. 1999;230:149–157.CrossRefGoogle ScholarPubMed
46.Li, Y, Douglas, SD, Ho, W. Human stem cells express substance P gene and its receptor. J Hematother Stem Cell Res. 2000;9:445–452.CrossRefGoogle ScholarPubMed
47.Jeurissen, F, Kavelaars, A, Korstjens, M, et al.Monocytes express a non-neurokinin substance P receptor that is functionally coupled to MAP kinase. J Immunol. 1994;152:2987–2994.CrossRefGoogle ScholarPubMed
48.Kavelaars, A, Broeke, D, Jeurissen, F, Kardux, J, Meijer, A, Franklin, R, Gelfand, EW, Heijnen, CJ. Activation of human monocytes via a non-neurokinin substance P receptor that is coupled to Gi protein, calcium, phospholipase D, MAP kinase, and IL-6 production. J Immunol. 1994;153:3691–3699.CrossRefGoogle Scholar
49.Schumann, MA, Gardner, P. Modulation of membrane K+ conductance in T-lymphocytes by substance P via a GTP-binding protein. J Membr Biol. 1989;111:133–139.CrossRefGoogle ScholarPubMed
50.Kavelaars, A, Jeurissen, F, Heijnen, CJ. Substance P receptors and signal transduction in leukocytes. Immunomethods. 1994;5:41–48.CrossRefGoogle ScholarPubMed
51.Rameshwar, P, Gascon, P. Substance P (SP) mediates production of stem cell factor and interleukin-1 in bone marrow stroma: potential autoregulatory role for these cytokines in SP receptor expression and induction. Blood. 1995;86:482–490.CrossRefGoogle ScholarPubMed
52.Black, PH. Psychoneuroimmunology: Brain and Immunity. Sci Am Sci Med 1995;272:16–24.Google Scholar
53.Matis, WL, Lavker, RM, Murphy, GF. Substance P induces the expression of an endothelial-leukocyte adhesion molecule by microvascular endothelium. J Invest Dermatol. 1990;94:492–495.CrossRefGoogle ScholarPubMed
54.Catalan, RE, Martinez, AM, Aragones, MD, Fernandez, I. Substance P stimulates translocation of protein kinase C in brain microvessels. Biochem Biophys Res Commun. 1989;164:595–600.CrossRefGoogle ScholarPubMed
55.Annunziata, P, Cioni, C, Toneatto, S, Paccagnini, E. HIV-1 gp120 increases the permeability of rat brain endothelium cultures by a mechanism involving substance P. AIDS. 1998;12:2377–2385.CrossRefGoogle ScholarPubMed
56.Toneatto, S, Finco, O, van der Putten, H, Abrignani, S, Annunziata, P. Evidence of blood-brain barrier alteration and activation in HIV-1 gp120 transgenic mice. AIDS. 1999;13:2343–2348.CrossRefGoogle ScholarPubMed
57.Helme, RD, Eglezos, A, Hosking, CS. Substance P induces chemotaxis of neutrophils in normal and capsaicin-treated rats. Immunol Cell Biol. 1987;65:267–269.CrossRefGoogle ScholarPubMed
58.Sacerdote, P, Panerai, AE. Effect of tenoxicam and indomethacin on the chemotaxis induced by substance P and interleukin-8 on human monocytes and polymorphonuclear cells. Int J Tissue React. 1993;15:175–180.Google ScholarPubMed
59.Serra, MC, Calzetti, F, Ceska, M, Cassatella, MA. Effect of substance P on superoxide anion and IL-8 production by human PMNL. Immunology. 1994;82:63–69.Google ScholarPubMed
60.Stanisz, AM, Befus, D, Bienenstock, J. Differential effects of vasoactive intestinal peptide, substance P, and somatostatin on immunoglobulin synthesis and proliferations by lymphocytes from Peyer's patches, mesenteric lymph nodes, and spleen. J Immunol. 1986;136:152–156.CrossRefGoogle ScholarPubMed
61.Moore, TC, Lami, JL, Spruck, CH. Substance P increases lymphocyte traffic and lymph flow through peripheral lymph nodes of sheep. Immunology. 1989;67:109–114.Google ScholarPubMed
62.Moore, TC. Modification of lymphocyte traffic by vasoactive neurotransmitter substances. Immunology. 1984;52:511–518.Google ScholarPubMed
63.Eglezos, A, Helme, RD, Dandie, GW, Andrews, PV, Boyd, RL. Substance P-mediated modulation of the primary antibody response. Adv Exp Med Biol. 1988;237:499–503.CrossRefGoogle ScholarPubMed
64.Pascual, DW, Bost, KL, Xu-Amano, J, Kiyono, H, McGhee, JR. The cytokine-like action of substance P upon B cell differentiation. Reg Immunol. 1992;4:100–104.Google ScholarPubMed
65.Hartung, HP, Toyka, KV. Activation of macrophages by substance P: induction of oxidative burst and thromboxane release. Eur J Pharmacol. 1983;89:301–305.CrossRefGoogle ScholarPubMed
66.Hartung, HP. Activation of macrophages by neuropeptides. Brain Behav Immun. 1988;2:275–281.CrossRefGoogle ScholarPubMed
67.Hartung, HP, Wolters, K, Toyka, KV. Substance P: binding properties and studies on cellular responses in guinea pig macrophages. J Immunol. 1986;136:3856–3863.CrossRefGoogle ScholarPubMed
68.Lotz, M, Vaughan, JH, Carson, DA. Effect of neuropeptides on production of inflammatory cytokines by human monocytes. Science. 1988;241:1218–1221.CrossRefGoogle ScholarPubMed
69.Laurenzi, MA, Persson, MA, Dalsgaard, CJ, Haegerstrand, A. The neuropeptide substance P stimulates production of interleukin 1 in human blood monocytes: activated cells are preferentially influenced by the neuropeptide. Scand J Immunol. 1990;31:529–533.CrossRefGoogle ScholarPubMed
70.Calvo, CF, Chavanel, G, Senik, A. Substance P enhances IL-2 expression in activated human T cells. J Immunol. 1992;148:3498–3504.CrossRefGoogle ScholarPubMed
71.Rameshwar, P, Ganea, D, Gascon, P. In vitro stimulatory effect of substance P on hematopoiesis. Blood. 1993;81:391–398.CrossRefGoogle ScholarPubMed
72.Manske, JM, Sullivan, EL, Andersen, SM. Substance P mediated stimulation of cytokine levels in cultured murine bone marrow stromal cells. Adv Exp Med Biol. 1995;383:53–64.CrossRefGoogle ScholarPubMed
73.Lieb, K, Fiebich, BL, Berger, M, Bauer, J, Schulze-Osthoff, K. The neuropeptide substance P activates transcription factor NF-kappa B and kappa B-dependent gene expression in human astrocytoma cells. J Immunol. 1997;159:4952–4958.CrossRefGoogle ScholarPubMed
74.Tran, MT, Lausch, RN, Oakes, JE. Substance P differentially stimulates IL-8 synthesis in human corneal epithelial cells. Invest Ophthalmol Vis Sci. 2000;41:3871–3877.Google ScholarPubMed
75.Ho, WZ, Kaufman, D, Uvaydova, M, Douglas, SD. Substance P augments interleukin-10 and tumor necrosis factor-alpha release by human cord blood monocytes and macrophages. J Neuroimmunol. 1996;71:73–80.CrossRefGoogle ScholarPubMed
76.Kincy-Cain, T, Bost, KL. Substance P-induced IL-12 production by murine macrophages. J Immunol. 1997;158:2334–2339.CrossRefGoogle ScholarPubMed
77.Wagner, F, Fink, R, Hart, R, Dancygier, H. Substance P enhances interferongamma production by human peripheral blood mononuclear cells. Regul Pept. 1987;19:355–364.CrossRefGoogle ScholarPubMed
78.Kang, H, Byun, DG, Kim, JW. Effects of substance P and vasoactive intestinal peptide on interferon-gamma and interleukin-4 production in severe atopic dermatitis. Ann Allergy Asthma Immunol. 2000;85:227–232.CrossRefGoogle ScholarPubMed
79.Lee, HR, Ho, WZ, Douglas, SD. Substance P augments tumor necrosis factor release in human monocyte-derived macrophages. Clin Diagn Lab Immunol. 1994;1:419–423.CrossRefGoogle ScholarPubMed
80.Ho, WZ, Stavropoulos, G, Lai, JP, et al.Substance P C-terminal octapeptide analogues augment tumor necrosis factor-alpha release by human blood monocytes and macrophages. J Neuroimmunol. 1998;82:126–132.CrossRefGoogle ScholarPubMed
81.Marriott, I, Bost, KL. Substance P diminishes lipopolysaccharide and interferon-gamma-induced TGF-beta 1 production by cultured murine macrophages. Cell Immunol. 1998;183:113–120.CrossRefGoogle ScholarPubMed
82.Marriott, I, Mason, MJ, Elhofy, A, Bost, KL. Substance P activates NF-kappaB independent of elevations in intracellular calcium in murine macrophages and dendritic cells. J Neuroimmunol. 2000;102:163–171.CrossRefGoogle ScholarPubMed
83.Folks, TM, Justement, J, Kinter, A, Dinarello, CA, Fauci, AS. Cytokine-induced expression of HIV-1 in a chronically infected promonocyte cell line. Science. 1987;238:800–802.CrossRefGoogle Scholar
84.Folks, TM, Justement, J, Kinter, A, et al.Characterization of a promonocyte clone chronically infected with HIV and inducible by 13-phorbol-12-myristate acetate. J Immunol. 1988;140:1117–1122.CrossRefGoogle ScholarPubMed
85.Clouse, KA, Powell, D, Washington, I, et al.Monokine regulation of human immunodeficiency virus-1 expression in a chronically infected human T cell clone. J Immunol. 1989;142:431–438.CrossRefGoogle Scholar
86.Dorig, RE, Marcil, A, Chopra, A, Richardson, CD. The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell. 1993;75:295–305.CrossRefGoogle ScholarPubMed
87.Harrowe, G, Sudduth-Klinger, J, Payan, DG. Measles virus-substance P receptor interaction: Jurkat lymphocytes transfected with substance P receptor cDNA enhance measles virus fusion and replication. Cell Mol Neurobiol. 1992;12:397–409.CrossRefGoogle ScholarPubMed
88.Ho, WZ, Cnaan, A, Li, YH, et al.Substance P modulates human immunodeficiency virus replication in human peripheral blood monocyte-derived macrophages. AIDS Res Hum Retroviruses. 1996;12:195–198.CrossRefGoogle ScholarPubMed
89.Li, Y, Douglas, SD, Song, L, Sun, S, Ho, WZ. Substance P enhances HIV-1 replication in latently infected human immune cells. J Neuroimmunol. 2001;121:67–75.CrossRefGoogle ScholarPubMed
90.Lai, JP, Ho, WZ, Zhan, GX, Yi, Y, Collman, RG, Douglas, SD. Substance P antagonist (CP-96,345) inhibits HIV-1 replication in human mononuclear phagocytes. Proc Natl Acad Sci U S A. 2001;98:3970–3975.CrossRefGoogle ScholarPubMed
91.Sharkey, KA, Sutherland, LR, Davison, JS, et al.Peptides in the gastrointestinal tract in human immunodeficiency virus infection. The GI/HIV Study Group of the University of Calgary. Gastroenterology. 1992;103:18–28.CrossRefGoogle Scholar
92.Covas, MJ, Pinto, LA, Victorino, RM. Disturbed immunoregulatory properties of the neuropeptide substance P on lymphocyte proliferation in HIV infection. Clin Exp Immunol. 1994;96:384–388.CrossRefGoogle ScholarPubMed
93.Azzari, C, Rossi, ME, Resti, M, et al.Changed levels of substance P and somatostatin in HIV-positive children. Pediatr Med Chir. 1992;14:577–581.Google ScholarPubMed
94.Douglas, SD, Ho, WZ, Gettes, DR, et al.Elevated substance P levels in HIV-infected men. AIDS. 2001;15:2043–2045.CrossRefGoogle ScholarPubMed
95.Ho, WZ, Lai, JP, Li, Y, Douglas, SD. HIV enhances substance P expression in human immune cells. FASEB J. 2002;16:616–618.CrossRefGoogle ScholarPubMed
96.Leserman, J, Jackson, ED, Petitto, JM, et al.Progression to AIDS: the effects of stress, depressive symptoms, and social support. Psychosom Med. 1999;61:397–406.CrossRefGoogle ScholarPubMed
97.Mayne, TJ, Vittinghoff, E, Chesney, MA, Barrett, DC, Coates, TJ. Depressive affect and survival among gay and bisexual men infected with HIV. Arch Intern Med. 1996;156:2233–2238.CrossRefGoogle ScholarPubMed
98.Ickovics, JR, Hamburger, ME, Vlahov, D, et al.Mortality, CD4 cell count decline, and depressive symptoms among HIV-seropositive women: longitudinal analysis from the HIV Epidemiology Research Study. JAMA. 2001;285:1466–1474.CrossRefGoogle ScholarPubMed
99.Morrison, MF, Petitto, JM, Have, TT, et al.Depressive and anxiety disorders in women with HIV infection. Am J Psychiatry. 2002;159:789–796.CrossRefGoogle ScholarPubMed
100.Cole, SW, Kemeny, ME. Psychobiology of HIV infection. Crit Rev Neurobiol. 1997;11:289–321.Google ScholarPubMed
101.Cole, SW, Naliboff, BD, Kemeny, ME, et al.Impaired response to HAART in HIV-infected individuals with high autonomic nervous system activity. Proc Natl Acad Sci U S A. 2001;98:12695–12700.CrossRefGoogle ScholarPubMed
102.Hood, VC, Cruwys, SC, Urban, L, Kidd, BL. Differential role of neurokinin receptors in human lymphocyte and monocyte chemotaxis. Regul Pept. 2000;96:17–21.CrossRefGoogle ScholarPubMed
103.Kennedy, PG, Rodgers, J, Jennings, FW, et al.A substance P antagonist, RP-67,580, ameliorates a mouse meningoencephalitic response to Trypanosoma brucei brucei. Proc Natl Acad Sci U S A. 1997;94:4167–4170.CrossRefGoogle ScholarPubMed
104.Sonea, IM, Palmer, MV, Akili, D, Harp, JA. Treatment with neurokinin-1 receptor antagonist reduces severity of inflammatory bowel disease induced by Cryptosporidium parvum. Clin Diagn Lab Immunol. 2002;9:333–340.Google ScholarPubMed
105.De Felipe, C, Herrero, JF, O'Brien, JA, et al.Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature. 1998;392:394–397.CrossRefGoogle ScholarPubMed
106.Kramer, MS, Cutler, N, Feighner, J, et al.Distinct mechanism for antidepressant activity by blockade of central substance P receptors. Science. 1998;281:1640–1645.CrossRefGoogle ScholarPubMed
107.Stout, SC, Owens, MJ, Nemeroff, CB. Neurokinin(1) receptor antagonists as potential antidepressants. Annu Rev Pharmacol Toxicol. 2001;41:877–906.CrossRefGoogle ScholarPubMed