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Control of Leukocyte Migration by Chemokines

Leukocyte Trafficking

White blood cells are the first line of host defense against invaders from without (e.g., microbial pathogens) or within (e.g., tumors). To be effective, leukocytes must engage in complex trafficking patterns. Some travel to the site of the initial breach to fight the invasion nonspecifically. Others sample the invasion site and carry bits of information back to lymph nodes where they initiate an immune response that directs the migration of effector cells back to the invasion site. We now know that these movements are controlled by a family of small secreted proteins called chemokines.

One approach our laboratory takes to understanding chemokines is to study one in detail, namely monocyte chemoattractant protein-1 (MCP-1). We have dissected the molecular determinants of its function by structure-activity analyses and have attempted to understand its physiology using genetically modified mice. For example, studies in MCP-1-deficient mice show that this chemokine is essential for monocyte recruitment in inflammation, including diseases with inflammatory components such as atherosclerosis. We have also discovered that MCP-1 is required for the development of type 2 T helper cell-polarized immune responses, that is, those that fight parasites and are involved in allergies. Current efforts are directed toward understanding the molecular basis for this effect. We are also interested in the interface between chemokines and cancer. Chemokines can stimulate leukocytes to engage in host antitumor activity, but some chemokines can affect tumor cells directly. Recently, we demonstrated that ambient chemokines stimulate anti-apoptotic responses in tumor cells. In fact, some tumors secrete chemokines that act in an autocrine manner to inhibit apoptosis - a powerful and direct mechanism whereby inflammation can promote cancer.

Finally, a new area of research involves the Langerhans cell histiocytoses, a family of diseases in which chemokine abnormalities may play a role in determining patterns of organ involvement. We have demonstrated that pathologic Langerhans cells aberrantly express chemokine receptors in a manner that could explain patterns of tissue involvement in the histiocytoses.

Cell Cycle Control

In addition to leukocyte trafficking, our laboratory studies cell cycle control. In particular, we have demonstrated that cyclin C, an understudied regulator of the cell cycle, combines with cdk3 to promote exit from the G0 state by phosphorylation of pRb, the product of the retinoblastoma susceptibility gene. These new insights into the G0 resting state may have important implications for cancer treatment.

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Absence of CC chemokine ligand 2 does not limit obesity-associated infiltration of macrophages into adipose tissue. Diabetes. 2007 Sep; 56(9):2242-50.
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Monocyte chemoattractant protein-1-induced tissue inflammation is critical for the development of renal injury but not type 2 diabetes in obese db/db mice. Diabetologia. 2007 Feb; 50(2):471-80.
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The chemokine decoy receptor M3 blocks CC chemokine ligand 2 and CXC chemokine ligand 13 function in vivo. J Immunol. 2006 Nov 15; 177(10):7296-302.
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Critical role of MCP-1 in the pathogenesis of experimental colitis in the context of immune and enterochromaffin cells. Am J Physiol Gastrointest Liver Physiol. 2006 Nov; 291(5):G803-11.
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Release the hounds! A chemokine elicits monocytes from bone marrow. Nat Immunol. 2006 Mar; 7(3):230-2.
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Inflammatory chemokines in cancer growth and progression. Eur J Cancer. 2006 Apr; 42(6):760-7.
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The chemokine CCL2 is required for control of murine gastric Salmonella enterica infection. Infect Immun. 2005 Oct; 73(10):6514-22.
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CXC chemokine ligand 12 (stromal cell-derived factor 1 alpha) and CXCR4-dependent migration of CTLs toward melanoma cells in organotypic culture. J Immunol. 2005 May 01; 174(9):5856-63.
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Chronic expression of monocyte chemoattractant protein-1 in the central nervous system causes delayed encephalopathy and impaired microglial function in mice. FASEB J. 2005 May; 19(7):761-72.
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The effect of MCP-1 depletion on chemokine and chemokine-related gene expression: evidence for a complex network in acute inflammation. Cytokine. 2005 Apr 21; 30(2):64-71.
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CCL2/Monocyte Chemoattractant Protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ Res. 2005 Apr 29; 96(8):881-9.
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Impairment in postischemic neovascularization in mice lacking the CXC chemokine receptor 3. Circ Res. 2005 Mar 18; 96(5):576-82.
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Constitutive homing of mast cell progenitors to the intestine depends on autologous expression of the chemokine receptor CXCR2. Blood. 2005 Jun 01; 105(11):4308-13.
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The CC chemokine ligand, CCL2/MCP1, participates in macrophage fusion and foreign body giant cell formation. Am J Pathol. 2004 Dec; 165(6):2157-66.
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Differential roles of CCL2 and CCR2 in host defense to coronavirus infection. Virology. 2004 Nov 24; 329(2):251-60.
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Aspergillus antigen induces robust Th2 cytokine production, inflammation, airway hyperreactivity and fibrosis in the absence of MCP-1 or CCR2. Respir Res. 2004 Sep 15; 5:12.
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CCL2 (monocyte chemoattractant protein-1) and cancer. Semin Cancer Biol. 2004 Jun; 14(3):149-54.
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Selective suppression of monocyte chemoattractant protein-1 expression by human papillomavirus E6 and E7 oncoproteins in human cervical epithelial and epidermal cells. Int J Cancer. 2003 Nov 10; 107(3):407-15.
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MCP-1 deficiency is associated with reduced intimal hyperplasia after arterial injury. Biochem Biophys Res Commun. 2003 Oct 24; 310(3):936-42.
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An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med. 2003 Nov; 9(11):1390-7.
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Post-BMT lung injury occurs independently of the expression of CCL2 or its receptor, CCR2, on host cells. Am J Physiol Lung Cell Mol Physiol. 2004 Feb; 286(2):L284-92.
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CC chemokine ligand 2 and its receptor regulate mucosal production of IL-12 and TGF-beta in high dose oral tolerance. J Immunol. 2003 Oct 01; 171(7):3560-7.
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DNA methyltransferase 3b contributes to oncogenic transformation induced by SV40T antigen and activated Ras. Oncogene. 2003 Jul 24; 22(30):4723-33.
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Monocyte chemoattractant protein-1 (CCL2) in inflammatory disease and adaptive immunity: therapeutic opportunities and controversies. Microcirculation. 2003 Jun; 10(3-4):247-57.
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Absence of CC chemokine ligand 2 results in an altered Th1/Th2 cytokine balance and failure to expel Trichuris muris infection. J Immunol. 2003 May 01; 170(9):4693-700.
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Coincident expression of the chemokine receptors CCR6 and CCR7 by pathologic Langerhans cells in Langerhans cell histiocytosis. Blood. 2003 Apr 01; 101(7):2473-5.
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Pertussis toxin-induced reversible encephalopathy dependent on monocyte chemoattractant protein-1 overexpression in mice. J Neurosci. 2002 Dec 15; 22(24):10633-42.
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Regulation of cellular proliferation, cytoskeletal function, and signal transduction through CXCR4 and c-Kit in small cell lung cancer cells. Cancer Res. 2002 Nov 01; 62(21):6304-11.
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Ccr2 regulates the level of MCP-1/CCL2 in vitro and at inflammatory sites and controls T cell activation in response to alloantigen. Cytokine. 2002 May 21; 18(4):184-90.
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MCP-1 expression in endotoxin-induced uveitis. Invest Ophthalmol Vis Sci. 2002 May; 43(5):1493-8.
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A functional IFN-gamma-inducible protein-10/CXCL10-specific receptor expressed by epithelial and endothelial cells that is neither CXCR3 nor glycosaminoglycan. J Immunol. 2001 Dec 01; 167(11):6576-82.
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Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J Exp Med. 2001 Nov 05; 194(9):1361-73.
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Chemokines and atherosclerosis: what Adam Smith has to say about vascular disease. J Clin Invest. 2001 Nov; 108(9):1269-71.
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Wound healing in MIP-1alpha(-/-) and MCP-1(-/-) mice. Am J Pathol. 2001 Aug; 159(2):457-63.
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A phase II trial of the cyclin-dependent kinase inhibitor flavopiridol in patients with previously untreated stage IV non-small cell lung cancer. Clin Cancer Res. 2001 Jun; 7(6):1590-9.
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If it's Tuesday, this must be a Belgian chemokine. Blood. 2001 Apr 15; 97(8):2193.
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Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med. 2001 Mar 19; 193(6):713-26.
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Chemokines and disease. Nat Immunol. 2001 Feb; 2(2):108-15.
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Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature. 2000 Mar 23; 404(6776):407-11.
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The physiology of p16(INK4A)-mediated G1 proliferative arrest. Cell Biochem Biophys. 2000; 33(2):189-97.
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Targeted expression of chemokines in vivo. Methods Mol Biol. 2000; 138:243-51.
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Monocyte chemoattractant protein 1-dependent leukocytic infiltrates are responsible for autoimmune disease in MRL-Fas(lpr) mice. J Exp Med. 1999 Dec 20; 190(12):1813-24.
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Flavopiridol induces cell cycle arrest and p53-independent apoptosis in non-small cell lung cancer cell lines. Clin Cancer Res. 1999 Oct; 5(10):2925-38.
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Physiological coreceptor use by dual-tropic HIV-1: one plus one equals one. J Clin Invest. 1999 Sep; 104(5):531-2.
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Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med. 1999 Jul; 5(7):828-31.
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Monocyte chemoattractant protein-1 accelerates atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 1999 Jun; 19(6):1518-25.
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MCP-1 deficiency reduces susceptibility to atherosclerosis in mice that overexpress human apolipoprotein B. J Clin Invest. 1999 Mar; 103(6):773-8.
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Expression of the focal adhesion protein paxillin in lung cancer and its relation to cell motility. Oncogene. 1999 Jan 07; 18(1):67-77.
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Monocyte chemoattractant protein-1. Chem Immunol. 1999; 72:7-29.
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Monocyte chemoattractant protein-1 promotes macrophage-mediated tubular injury, but not glomerular injury, in nephrotoxic serum nephritis. J Clin Invest. 1999 Jan; 103(1):73-80.
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Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell. 1998 Aug; 2(2):275-81.
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Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J Exp Med. 1998 Feb 16; 187(4):601-8.
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p16INK4A participates in a G1 arrest checkpoint in response to DNA damage. Mol Cell Biol. 1998 Jan; 18(1):378-87.
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Tissue factor is induced by monocyte chemoattractant protein-1 in human aortic smooth muscle and THP-1 cells. J Biol Chem. 1997 Nov 07; 272(45):28568-73.
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In vivo properties of monocyte chemoattractant protein-1. J Leukoc Biol. 1997 Nov; 62(5):577-80.
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Chemokines. Blood. 1997 Aug 01; 90(3):909-28.
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Transgenic monocyte chemoattractant protein-1 (MCP-1) in pancreatic islets produces monocyte-rich insulitis without diabetes: abrogation by a second transgene expressing systemic MCP-1. J Immunol. 1997 Jul 01; 159(1):401-8.
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Renal expression of monocyte chemoattractant protein-1 in lupus autoimmune mice. J Am Soc Nephrol. 1997 May; 8(5):720-9.
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MCP-1-mediated chemotaxis requires activation of non-overlapping signal transduction pathways. J Leukoc Biol. 1997 Apr; 61(4):529-32.
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Human fibroblasts express functional IL-2 receptors formed by the IL-2R alpha- and beta-chain subunits: association of IL-2 binding with secretion of the monocyte chemoattractant protein-1. J Immunol. 1996 Jul 15; 157(2):851-7.
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The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell. 1996 Jun 28; 85(7):1135-48.
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Monocyte chemoattractant protein 1: a potential regulator of monocyte recruitment in inflammatory disease. Mol Med Today. 1996 May; 2(5):198-204.
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p16INK4A as a human tumor suppressor. Biochim Biophys Acta. 1996 Mar 18; 1242(3):165-9.
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High level expression of human MCP-1 using the LCR/MEL expression system. Protein Expr Purif. 1996 Mar; 7(2):173-82.
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Multiple mechanisms of p16INK4A inactivation in non-small cell lung cancer cell lines. Cancer Res. 1995 Dec 15; 55(24):6200-9.
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High level monocyte chemoattractant protein-1 expression in transgenic mice increases their susceptibility to intracellular pathogens. J Immunol. 1995 Nov 15; 155(10):4838-43.
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Monocyte chemoattractant protein-1 (MCP-1) gene transduction: an effective tumor vaccine strategy for non-intracranial tumors. Cancer Immunol Immunother. 1995 Oct; 41(4):227-35.
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A dominant negative inhibitor indicates that monocyte chemoattractant protein 1 functions as a dimer. Mol Cell Biol. 1995 Sep; 15(9):4851-5.
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A novel p16INK4A transcript. Cancer Res. 1995 Jul 15; 55(14):2995-7.
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Reciprocal Rb inactivation and p16INK4 expression in primary lung cancers and cell lines. Cancer Res. 1995 Feb 01; 55(3):505-9.
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Serologic analysis of the mouse beta chemokine JE/monocyte chemoattractant protein-1. J Immunol. 1994 Oct 15; 153(8):3708-16.
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Monocyte chemoattractant protein-1 gene is expressed in activated neutrophils and retinoic acid-induced human myeloid cell lines. Blood. 1994 Oct 15; 84(8):2776-83.
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Structure/activity analysis of human monocyte chemoattractant protein-1 (MCP-1) by mutagenesis. Identification of a mutated protein that inhibits MCP-1-mediated monocyte chemotaxis. J Biol Chem. 1994 Jun 03; 269(22):15918-24.
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Biochemical and biologic characterization of murine monocyte chemoattractant protein-1. Identification of two functional domains. J Immunol. 1994 Apr 01; 152(7):3541-9.
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MCP-1 expression by rat type II alveolar epithelial cells in primary culture. J Immunol. 1993 May 15; 150(10):4561-70.
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"Oh, no. Not another cytokine."--MCP-1 and respiratory disease. Am J Respir Cell Mol Biol. 1992 Aug; 7(2):126-7.
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JE mRNA accumulates rapidly in aortic injury and in platelet-derived growth factor-stimulated vascular smooth muscle cells. Circ Res. 1992 Feb; 70(2):314-25.
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Expression of cytokine-like genes JE and KC is increased during renal ischemia. Am J Physiol. 1991 Dec; 261(6 Pt 2):F1095-101.
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JE/MCP-1: an early-response gene encodes a monocyte-specific cytokine. Cancer Cells. 1991 Dec; 3(12):517-24.
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In vivo and in vitro inhibition of JE gene expression by glucocorticoids. J Biol Chem. 1991 Nov 25; 266(33):22375-9.
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Human keratinocyte growth-promoting activity on the surface of fibroblasts. J Cell Physiol. 1991 Oct; 149(1):110-6.
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Recombinant human MCP-1/JE induces chemotaxis, calcium flux, and the respiratory burst in human monocytes. Blood. 1991 Aug 15; 78(4):1112-6.
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Interleukin-4 induces the synthesis and secretion of MCP-1/JE by human endothelial cells. Am J Pathol. 1991 Jun; 138(6):1315-9.
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Monocyte chemotactic protein gene expression by cytokine-treated human retinal pigment epithelial cells. Lab Invest. 1991 Jun; 64(6):819-25.
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Suppression of tumor formation in vivo by expression of the JE gene in malignant cells. Mol Cell Biol. 1991 Jun; 11(6):3125-31.
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Assignment of the human small inducible cytokine A2 gene, SCYA2 (encoding JE or MCP-1), to 17q11.2-12: evolutionary relatedness of cytokines clustered at the same locus. Genomics. 1991 Jun; 10(2):489-92.
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Alveolar macrophage-derived cytokines induce monocyte chemoattractant protein-1 expression from human pulmonary type II-like epithelial cells. J Biol Chem. 1991 May 25; 266(15):9912-8.
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Cytokine-activated human endothelial cells synthesize and secrete a monocyte chemoattractant, MCP-1/JE. Am J Pathol. 1990 Jun; 136(6):1229-33.
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The human homolog of the JE gene encodes a monocyte secretory protein. Mol Cell Biol. 1989 Nov; 9(11):4687-95.
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