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Macrophage Colony-Stimulating Factor in the Pathogenesis of HIV Infection: Potential Target for Therapeutic Intervention

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Abstract

Macrophage colony stimulating factor (M-CSF) appears to play a major role in promoting and maintaining reservoirs of human immunodeficiency virus type 1 (HIV-1) in infected individuals. HIV-1 infection induces production of M-CSF by macrophages, which in turn promotes further infection of macrophages via increases in CD4 and CCR5 receptors, as well as increases in virus gene expression. M-CSF promotes the ontogeny and survival of macrophages, contributing to both the number and longevity of these infected cells. M-CSF dysregulation promotes the differentiation of monocytes toward macrophages and osteoclasts and at the same time may inhibit differentiation toward dendritic cells, resulting in immune impairment. The potential role of M-CSF in HIV-associated end organ diseases including HIV-associated dementia, HIV-associated nephropathy, and osteoporosis is discussed. This review emphasizes the need for developing M-CSF antagonists for treatment of HIV-1-infected patients.

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References

  • Alonso K, Pontiggia P, Medenica R, Rizzo S (1997) Cytokine patterns in adults with AIDS. Immunol Invest 26:341–350

    Article  PubMed  CAS  Google Scholar 

  • Annapoorna N, Rao GV, Reddy NS, Rambabu P, Rao KR (2004) An increased risk of osteoporosis during acquired immunodeficiency syndrome. Int J Med Sci 1:152–164

    CAS  PubMed  Google Scholar 

  • Bartelmez SH, Bradley TR, Bertoncello I, Mochizuki DY, Tushinski RJ, Stanley ER, Hapel AJ, Young IG, Kriegler AB, Hodgson GS (1989) Interleukin 1 plus interleukin 3 plus colony-stimulating factor 1 are essential for clonal proliferation of primitive myeloid bone marrow cells. Exp Hematol 17:240–245

    PubMed  CAS  Google Scholar 

  • Bell JE (2004) An update on the neuropathology of HIV in the HAART era. Histopathology 45:549–559

    Article  PubMed  CAS  Google Scholar 

  • Bergamini A, Perno CF, Dini L, Capozzi M, Pesce CD, Ventura L, Cappannoli L, Falasca L, Milanese G, Calio R (1994) Macrophage colony-stimulating factor enhances the susceptibility of macrophages to infection by human immunodeficiency virus and reduces the activity of compounds that inhibit virus binding. Blood 84:3405–3412

    PubMed  CAS  Google Scholar 

  • Bour S, Geleziunas R, Wainberg MA (1995) The human immunodeficiency virus type 1 (HIV-1) CD4 receptor and its central role in promotion of HIV-1 infection. Microbiol Rev 59:63–93

    PubMed  CAS  Google Scholar 

  • Bucay N, Sarosi I, Dunstan CR, Morony S, Tarpley J, Capparelli C, Scully S, Tan HL, Xu W, Lacey DL, Boyle WJ, Simonet WS (1998) Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev 12:1260–1268

    Article  PubMed  CAS  Google Scholar 

  • Canque B, Rosenzwajg M, Gey A, Tartour E, Fridman WH, Gluckman JC (1996) Macrophage inflammatory protein-1alpha is induced by human immunodeficiency virus infection of monocyte-derived macrophages. Blood 87:2011–2019

    PubMed  CAS  Google Scholar 

  • Chehimi J, Campbell DE, Azzoni L, Bacheller D, Papasavvas E, Jerandi G, Mounzer K, Kostman J, Trinchieri G, Montaner LJ (2002) Persistent decreases in blood plasmacytoid dendritic cell number and function despite effective highly active antiretroviral therapy and increased blood myeloid dendritic cells in HIV-infected individuals. J Immunol 168:4796–4801

    PubMed  CAS  Google Scholar 

  • Cinque P, Vago L, Ceresa D, Mainini F, Terreni MR, Vagani A, Torri W, Bossolasco S, Lazzarin A (1998) Cerebrospinal fluid HIV-1 RNA levels: correlation with HIV encephalitis. AIDS 12:389–394

    Article  CAS  PubMed  Google Scholar 

  • Corder EH, Robertson K, Lannfelt L, Bogdanovic N, Eggertsen G, Wilkins J, Hall C (1998) HIV-infected subjects with the E4 allele for APOE have excess dementia and peripheral neuropathy. Nat Med 4:1182–1184

    Article  PubMed  CAS  Google Scholar 

  • Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, Sylvestre V, Stanley ER (2002) Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99:111–1202

    Article  PubMed  CAS  Google Scholar 

  • De Strooper B, Annaert W (2000) Proteolytic processing and cell biological functions of the amyloid precursor protein. J Cell Sci 113(Pt 11):1857–1870

    PubMed  Google Scholar 

  • Dickie P, Felser J, Eckhaus M, Bryant J, Silver J, Marinos N, Notkins AL (1991) HIV-associated nephropathy in transgenic mice expressing HIV-1 genes. Virology 185:109–119

    Article  PubMed  CAS  Google Scholar 

  • Dickie P, Roberts A, Uwiera R, Witmer J, Sharma K, Kopp JB (2004) Focal glomerulosclerosis in proviral and c–fms transgenic mice links Vpr expression to HIV-associated nephropathy. Virology 322:69–81

    Article  PubMed  CAS  Google Scholar 

  • Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, Cayanan C, Maddon PJ, Koup RA, Moore JP, Paxton WA (1996) HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC–CKR–5. Nature 381:667–673

    Article  PubMed  CAS  Google Scholar 

  • Fischer–Smith T, Croul S, Sverstiuk AE, Capini C, L'Heureux D, Regulier EG, Richardson MW, Amini S, Morgello S, Khalili K, Rappaport J (2001) CNS invasion by CD14+/CD16+peripheral blood-derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection. J Neurovirol 7:528–541

    Article  PubMed  CAS  Google Scholar 

  • Fixe P, Praloran V (1998) M-CSF: haematopoietic growth factor or inflammatory cytokine? Cytokine 10:32–37

    Article  PubMed  CAS  Google Scholar 

  • Gadducci A, Ferdeghini M, Castellani C, Annicchiarico C, Prontera C, Facchini V, Bianchi R, Genazzani AR (1998) Serum macrophage colony-stimulating factor (M-CSF) levels in patients with epithelial ovarian cancer. Gynecol Oncol 70:111–114

    Article  PubMed  CAS  Google Scholar 

  • Gallo P, Laverda AM, De Rossi A, Pagni S, Del Mistro A, Cogo P, Piccinno MG, Plebani A, Tavolato B, Chieco–Bianchi L (1991) Immunological markers in the cerebrospinal fluid of HIV-1–infected children. Acta Paediatr Scand 80:659–666

    Article  PubMed  CAS  Google Scholar 

  • Gallo P, De Rossi A, Sivieri S, Chieco–Bianchi L, Tavolato B (1994) M-CSF production by HIV-1–infected monocytes and its intrathecal synthesis. Implications for neurological HIV-1–related disease. J Neuroimmunol 51:193–198

    Article  PubMed  CAS  Google Scholar 

  • Garbuglia AR, Zaccarelli M, Calcaterra S, Cappiello G, Marini R, Benedetto A (2001) Dynamics of viral load in plasma and HIV DNA in lymphocytes during highly active antiretroviral therapy (HAART): high viral burden in macrophages after 1 year of treatment. J Chemother 13:188–194

    PubMed  CAS  Google Scholar 

  • Glass JD, Fedor H, Wesselingh SL, McArthur JC (1995) Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 38:755–762

    Article  PubMed  CAS  Google Scholar 

  • Glesby MJ (2003) Bone disorders in human immunodeficiency virus infection. Clin Infect Dis 37(Suppl 2):S91–S95

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez–Scarano F, Martin–Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5:69–81

    Article  PubMed  CAS  Google Scholar 

  • Gruber MF, Weih KA, Boone EJ, Smith PD, Clouse KA (1995) Endogenous macrophage CSF production is associated with viral replication in HIV-1–infected human monocyte-derived macrophages. J Immunol 154:5528–5535

    PubMed  CAS  Google Scholar 

  • Henderson AJ, Calame KL (1997) CCAAT/enhancer binding protein (C/EBP) sites are required for HIV-1 replication in primary macrophages but not CD4(+) T cells. Proc Natl Acad Sci U S A 94:8714–8719

    Article  CAS  PubMed  Google Scholar 

  • Henderson AJ, Connor RI, Calame KL (1996) C/EBP activators are required for HIV-1 replication and proviral induction in monocytic cell lines. Immunity 5:91–101

    Article  PubMed  CAS  Google Scholar 

  • Hofmann B, Odum N, Jakobsen BK, Platz P, Ryder LP, Nielsen JO, Gerstoft J, Svejgaard A (1986) Immunological studies in the acquired immunodeficiency syndrome. II. Active suppression or intrinsic defect-investigated by mixing AIDS cells with HLA–DR identical normal cells. Scand J Immunol 23:669–678

    Article  PubMed  CAS  Google Scholar 

  • Hollak CE, Evers L, Aerts JM, van Oers MH (1997) Elevated levels of M-CSF, sCD14 and IL8 in type 1 Gaucher disease. Blood Cells Mol Dis 23:201–212

    Article  PubMed  CAS  Google Scholar 

  • Honda Y, Rogers L, Nakata K, Zhao BY, Pine R, Nakai Y, Kurosu K, Rom WN, Weiden M (1998) Type I interferon induces inhibitory 16–kD CCAAT/enhancer binding protein (C/EBP)beta, repressing the HIV-1 long terminal repeat in macrophages: pulmonary tuberculosis alters C/EBP expression, enhancing HIV-1 replication. J Exp Med 188:1255–1265

    Article  CAS  PubMed  Google Scholar 

  • Igarashi T, Brown CR, Endo Y, Buckler–White A, Plishka R, Bischofberger N, Hirsch V, Martin MA (2001) Macrophage are the principal reservoir and sustain high virus loads in rhesus macaques after the depletion of CD4+ T cells by a highly pathogenic simian immunodeficiency virus/HIV type 1 chimera (SHIV): implications for HIV-1 infections of humans. Proc Natl Acad Sci U S A 98:658–663

    Article  CAS  PubMed  Google Scholar 

  • Ji XH, Sun LH, Qin JC, Yao K, Ding RN, Li HD, Zhu DX (2000) Effects of rhM-CSF expressed in silkworm on cytokine productions and membrane molecule expressions of human monocytes. Acta Pharmacol Sin 21:797–801

    PubMed  CAS  Google Scholar 

  • Jin Y, Dons L, Kristensson K, Rottenberg ME (2002) Colony-stimulating factor 1–dependent cells protect against systemic infection with Listeria monocytogenes but facilitate neuroinvasion. Infect Immun 70:4682–4686

    Article  PubMed  CAS  Google Scholar 

  • Kajiyama W, Kopp JB, Marinos NJ, Klotman PE, Dickie P (2000) Glomerulosclerosis and viral gene expression in HIV-transgenic mice: role of nef. Kidney Int 58:1148–1159

    Article  PubMed  CAS  Google Scholar 

  • Kalter DC, Nakamura M, Turpin JA, Baca LM, Hoover DL, Dieffenbach C, Ralph P, Gendelman HE, Meltzer MS (1991) Enhanced HIV replication in macrophage colony-stimulating factor-treated monocytes. J Immunol 146:298–306

    PubMed  CAS  Google Scholar 

  • Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988–994

    Article  PubMed  CAS  Google Scholar 

  • Khosla S (2001) Minireview: the OPG/RANKL/RANK system. Endocrinology 142:5050–5055

    Article  PubMed  CAS  Google Scholar 

  • Komuro I, Yokota Y, Yasuda S, Iwamoto A, Kagawa KS (2003) CSF-induced and HIV-1–mediated distinct regulation of Hck and C/EBPbeta represent a heterogeneous susceptibility of monocyte-derived macrophages to M-tropic HIV-1 infection. J Exp Med 198:443–453

    Article  CAS  PubMed  Google Scholar 

  • Kure K, Llena JF, Lyman WD, Soeiro R, Weidenheim KM, Hirano A, Dickson DW (1991) Human immunodeficiency virus–1 infection of the nervous system: an autopsy study of 268 adult, pediatric, and fetal brains. Hum Pathol 22:700–710

    Article  PubMed  CAS  Google Scholar 

  • Kutza J, Crim L, Feldman S, Hayes MP, Gruber M, Beeler J, Clouse KA (2000) Macrophage colony-stimulating factor antagonists inhibit replication of HIV-1 in human macrophages. J Immunol 164:4955–4960

    PubMed  CAS  Google Scholar 

  • Lafrenie RM, Lee SF, Hewlett IK, Yamada KM, Dhawan S (2002) Involvement of integrin alphavbeta3 in the pathogenesis of human immunodeficiency virus type 1 infection in monocytes. Virology 297:31–38

    Article  PubMed  CAS  Google Scholar 

  • Lambotte O, Taoufik Y, de Goer MG, Wallon C, Goujard C, Delfraissy JF (2000) Detection of infectious HIV in circulating monocytes from patients on prolonged highly active antiretroviral therapy. J Acquir Immune Defic Syndr 23:114–119

    PubMed  CAS  Google Scholar 

  • Lee ES, Sarma D, Zhou H, Henderson AJ (2002) CCAAT/enhancer binding proteins are not required for HIV-1 entry but regulate proviral transcription by recruiting coactivators to the long-terminal repeat in monocytic cells. Virology 299:20–31

    Article  PubMed  CAS  Google Scholar 

  • Lenda DM, Stanley ER, Kelley VR (2004) Negative role of colony-stimulating factor–1 in macrophage, T cell, and B cell mediated autoimmune disease in MRL–Fas(lpr) mice. J Immunol 173:4744–4754

    PubMed  CAS  Google Scholar 

  • Little SJ, Holte S, Routy JP, Daar ES, Markowitz M, Collier AC, Koup RA, Mellors JW, Connick E, Conway B, Kilby M, Wang L, Whitcomb JM, Hellmann NS, Richman DD (2002) Antiretroviral-drug resistance among patients recently infected with HIV. N Engl J Med 347:385–394

    Article  PubMed  CAS  Google Scholar 

  • Lu TC, Ross M (2005) HIV-associated nephropathy: a brief review. Mt Sinai J Med 72:193–199

    PubMed  Google Scholar 

  • Macatonia SE, Gompels M, Pinching AJ, Patterson S, Knight SC (1992) Antigen-presentation by macrophages but not by dendritic cells in human immunodeficiency virus (HIV) infection. Immunology 75:576–581

    PubMed  CAS  Google Scholar 

  • Manolagas SC (2000) Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 21:115–137

    Article  PubMed  CAS  Google Scholar 

  • McArthur JC, McClernon DR, Cronin MF, Nance–Sproson TE, Saah AJ, St Clair M, Lanier ER (1997) Relationship between human immunodeficiency virus-associated dementia and viral load in cerebrospinal fluid and brain. Ann Neurol 42:689–698

    Article  PubMed  CAS  Google Scholar 

  • Meltzer MS, Skillman DR, Gomatos PJ, Kalter DC, Gendelman HE (1990) Role of mononuclear phagocytes in the pathogenesis of human immunodeficiency virus infection. Annu Rev Immunol 8:169–194

    PubMed  CAS  Google Scholar 

  • Miyamoto T, Ohneda O, Arai F, Iwamoto K, Okada S, Takagi K, Anderson DM, Suda T (2001) Bifurcation of osteoclasts and dendritic cells from common progenitors. Blood 98:2544–2554

    Article  PubMed  CAS  Google Scholar 

  • Nagamura–Inoue T, Tamura T, Ozato K (2001) Transcription factors that regulate growth and differentiation of myeloid cells. Int Rev Immunol 20:83–105

    CAS  PubMed  Google Scholar 

  • Nebuloni M, Pellegrinelli A, Ferri A, Bonetto S, Boldorini R, Vago L, Grassi MP, Costanzi G (2001) Beta amyloid precursor protein and patterns of HIV p24 immunohistochemistry in different brain areas of AIDS patients. AIDS 15:571–575

    Article  PubMed  CAS  Google Scholar 

  • Oravecz T, Pall M, Roderiquez G, Gorrell MD, Ditto M, Nguyen NY, Boykins R, Unsworth E, Norcross MA (1997) Regulation of the receptor specificity and function of the chemokine RANTES (regulated on activation, normal T cell expressed and secreted) by dipeptidyl peptidase IV (CD26)–mediated cleavage. J Exp Med 186:1865–1872

    Article  CAS  PubMed  Google Scholar 

  • Ossipow V, Descombes P, Schibler U (1993) CCAAT/enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials. Proc Natl Acad Sci U S A 90:8219–8223

    Article  CAS  PubMed  Google Scholar 

  • Palucka KA, Taquet N, Sanchez–Chapuis F, Gluckman JC (1998) Dendritic cells as the terminal stage of monocyte differentiation. J Immunol 160:4587–4595

    PubMed  CAS  Google Scholar 

  • Pixley FJ, Stanley ER (2004) CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol 14:628–638

    Article  PubMed  CAS  Google Scholar 

  • Porwit A, Parravicini C, Petren AL, Barkhem T, Costanzi G, Josephs S, Biberfeld P (1989) Cell association of HIV in AIDS-related encephalopathy and dementia. APMIS 97:79–90

    Article  PubMed  CAS  Google Scholar 

  • Potter SJ, Chew CB, Steain M, Dwyer DE, Saksena NK (2004) Obstacles to successful antiretroviral treatment of HIV-1 infection: problems and perspectives. Indian J Med Res 119:217–237

    PubMed  CAS  Google Scholar 

  • Pulliam L, Gascon R, Stubblebine M, McGuire D, McGrath MS (1997) Unique monocyte subset in patients with AIDS dementia. Lancet 349:692–695

    Article  PubMed  CAS  Google Scholar 

  • Pumarola–Sune T, Navia BA, Cordon–Cardo C, Cho ES, Price RW (1987) HIV antigen in the brains of patients with the AIDS dementia complex. Ann Neurol 21:490–496

    Article  PubMed  CAS  Google Scholar 

  • Regulier EG, Reiss K, Khalili K, Amini S, Zagury JF, Katsikis PD, Rappaport J (2004) T–cell and neuronal apoptosis in HIV infection: implications for therapeutic intervention. Int Rev Immunol 23:25–59

    Article  PubMed  CAS  Google Scholar 

  • Rosati M, Valentin A, Patenaude DJ, Pavlakis GN (2001) CCAAT–enhancer-binding protein beta (C/EBP beta) activates CCR5 promoter: increased C/EBP beta and CCR5 in T lymphocytes from HIV-1–infected individuals. J Immunol 167:1654–1662

    PubMed  CAS  Google Scholar 

  • Saionji K, Ohsaka A (2001) Expansion of CD4+CD16+ blood monocytes in patients with chronic renal failure undergoing dialysis: possible involvement of macrophage colony-stimulating factor. Acta Haematol 105:21–26

    Article  PubMed  CAS  Google Scholar 

  • Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, Saragosti S, Lapoumeroulie C, Cognaux J, Forceille C, Muyldermans G, Verhofstede C, Burtonboy G, Georges M, Imai T, Rana S, Yi Y, Smyth RJ, Collman RG, Doms RW, Vassart G, Parmentier M (1996) Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR–5 chemokine receptor gene. Nature 382:722–725

    Article  PubMed  CAS  Google Scholar 

  • Schifitto G, McDermott MP, McArthur JC, Marder K, Sacktor N, McClernon DR, Conant K, Cohen B, Epstein LG, Kieburtz K (2005) Markers of immune activation and viral load in HIV-associated sensory neuropathy. Neurology 64:842–848

    PubMed  CAS  Google Scholar 

  • Si Q, Cosenza M, Zhao ML, Goldstein H, Lee SC (2002) GM-CSF and M-CSF modulate beta–chemokine and HIV-1 expression in microglia. Glia 39:174–183

    Article  PubMed  Google Scholar 

  • Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R, Nguyen HQ, Wooden S, Bennett L, Boone T, Shimamoto G, DeRose M, Elliott R, Colombero A, Tan HL, Trail G, Sullivan J, Davy E, Bucay N, Renshaw–Gegg L, Hughes TM, Hill D, Pattison W, Campbell P, Sander S, Van G, Tarpley J, Derby P, Lee R, Boyle WJ (1997) Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89:309–319

    Article  PubMed  CAS  Google Scholar 

  • Stanley ER, Chen DM, Lin HS (1978) Induction of macrophage production and proliferation by a purified colony stimulating factor. Nature 274:168–170

    Article  PubMed  CAS  Google Scholar 

  • Stohr J, Schindler G, Rothe G, Schmitz G (1998) Enhanced upregulation of the Fc gamma receptor IIIa (CD16a) during in vitro differentiation of ApoE4/4 monocytes. Arterioscler Thromb Vasc Biol 18:1424–1432

    PubMed  CAS  Google Scholar 

  • Suzu S, Yanai N, Sato–Somoto Y, Yamada M, Kawashima T, Hanamura T, Nagata N, Takaku F, Motoyoshi K. Characterization of macrophage colony-stimulating factor in body fluids by immunoblot analysis. Blood 77:2160–2165

    PubMed  CAS  Google Scholar 

  • Suzu S, Harada H, Matsumoto T, Okada S (2005) HIV-1 Nef interferes with M-CSF receptor signaling through Hck activation and inhibits M-CSF bioactivities. Blood 105:3230–3237

    Article  PubMed  CAS  Google Scholar 

  • Tushinski RJ, Oliver IT, Guilbert LJ, Tynan PW, Warner JR, Stanley ER (1982) Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell 28:71–81

    Article  PubMed  CAS  Google Scholar 

  • Vaananen K (2005) Mechanism of osteoclast mediated bone resorption—rationale for the design of new therapeutics. Adv Drug Deliv Rev 57:959–971

    Article  PubMed  CAS  Google Scholar 

  • Valcour V, Shikuma C, Shiramizu B, Watters M, Poff P, Selnes OA, Grove J, Liu Y, Abdul–Majid KB, Gartner S, Sacktor N (2004) Age, apolipoprotein E4, and the risk of HIV dementia: the Hawaii Aging with HIV Cohort. J Neuroimmunol 157:197–202

    Article  PubMed  CAS  Google Scholar 

  • Vehmas A, Lieu J, Pardo CA, McArthur JC, Gartner S (2004) Amyloid precursor protein expression in circulating monocytes and brain macrophages from patients with HIV-associated cognitive impairment. J Neuroimmunol 157:99–110

    Article  PubMed  CAS  Google Scholar 

  • Yamada N, Tsujimura T, Ueda H, Hayashi S, Ohyama H, Okamura H, Terada N (2005) Down-regulation of osteoprotegerin production in bone marrow macrophages by macrophage colony-stimulating factor. Cytokine 31:288–297

    Article  PubMed  CAS  Google Scholar 

  • Yoshida H, Hayashi S, Kunisada T, Ogawa M, Nishikawa S, Okamura H, Sudo T, Shultz LD (1990) The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345:442–444

    Article  PubMed  CAS  Google Scholar 

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Haine, V., Fischer-Smith, T. & Rappaport, J. Macrophage Colony-Stimulating Factor in the Pathogenesis of HIV Infection: Potential Target for Therapeutic Intervention. Jrnl NeuroImmune Pharm 1, 32–40 (2006). https://doi.org/10.1007/s11481-005-9003-1

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