Granulocyte-macrophage colony-stimulating factor (GM-CSF), also known as CSF2, is a glycoproteincytokine that promotes the proliferation, differentiation, and functional activation of myeloid cells, including granulocytes (such as neutrophils and eosinophils) and macrophages, from bone marrowprogenitor cells.[1] Originally identified for its ability to induce colony formation in vitro from hematopoietic precursors, GM-CSF plays a central role in innate immunity by enhancing phagocytosis, antimicrobial activity, and survival of these immune cells during infection and inflammation.[2]GM-CSF is produced by a variety of cells, including activated T lymphocytes, macrophages, endothelial cells, and fibroblasts, in response to inflammatory stimuli such as cytokines or microbial products.[3] Structurally, it consists of 144 amino acids with a 17-amino acid leader sequence, resulting in a molecular weight of 14 to 35 kDa due to heterogeneous glycosylation, which modulates its biological activity.[1] It exerts its effects by binding to a heterodimeric receptor composed of an α subunit (GM-CSFRα) specific to GM-CSF and a shared β subunit (βc) common to interleukin-3 (IL-3) and IL-5 receptors, activating downstream signaling pathways including JAK2/STAT5, PI3K/AKT, and MAPK/ERK to regulate gene expression in target cells.[4]Beyond hematopoiesis, GM-CSF functions as a proinflammatory mediator, bridging innate and adaptive immunity by promoting dendritic cell maturation, enhancing antigen presentation, and supporting T helper 17 (Th17) cell responses, which contribute to host defense but can also drive pathological inflammation in autoimmune diseases like rheumatoid arthritis and multiple sclerosis.[4] In clinical practice, recombinant human GM-CSF (sargramostim) is approved for accelerating myeloid recovery after chemotherapy-induced neutropenia, bone marrow transplantation, and stem cell mobilization, reducing infection risk and hospitalization duration.[1] Emerging research explores its dual role in cancer, where it enhances antitumor immunity as a vaccine adjuvant but may promote tumor progression through myeloid-derived suppressor cells, alongside therapeutic targeting of the GM-CSF pathway with antibodies such as mavrilimumab (anti-GM-CSFRα) for inflammatory conditions including severe COVID-19.[5]
Molecular Structure and Genetics
Gene and Chromosomal Location
The CSF2 gene, which encodes granulocyte-macrophage colony-stimulating factor (GM-CSF), is located on the long arm of human chromosome 5 at the cytogenetic band 5q31.1, with precise genomic coordinates spanning 132,073,789 to 132,076,170 on the forward strand according to the GRCh38 reference assembly.[6][7] This locus forms part of a well-defined cytokinegene cluster at 5q31 that also encompasses the genes for interleukin-3 (IL3), interleukin-4 (IL4), interleukin-5 (IL5), and interleukin-13 (IL13), reflecting a regional organization of genes involved in immune and inflammatory responses.[8][9]The CSF2 gene consists of four exons and three introns, with the full genomic span measuring approximately 2.5 kb.[6][10] Its promoter region contains regulatory elements that respond to inflammatory stimuli, such as lipopolysaccharide (LPS) via Toll/IL-1 receptor pathways, enabling inducible expression during immune activation.[11]Interstitial deletions encompassing the 5q31.1 region, including CSF2, are associated with myelodysplastic syndromes like the 5q- syndrome, characterized by refractory macrocytic anemia and megakaryocytic dysplasia, as well as progression to acute myeloid leukemia (AML) in some cases.[12] These deletions lead to haploinsufficiency of genes in the cluster, contributing to disrupted hematopoiesis.[13]The CSF2 gene exhibits strong evolutionary conservation across mammals, with the encoded protein sharing approximately 54% amino acid sequence identity between human and mouse orthologs, alongside highly homologous gene organization featuring four exons.[14][15] This conservation underscores its fundamental role in hematopoietic regulation.
The mature human granulocyte-macrophage colony-stimulating factor (GM-CSF) is a monomeric glycoprotein composed of 127 amino acids, exhibiting a molecular weight of 14-35 kDa that varies with the degree of glycosylation.[16][17] This glycoprotein structure supports its role as a cytokine, with the unglycosylated form calculated at approximately 14.5 kDa and higher masses arising from post-translational modifications.[18] The protein contains two potential N-glycosylation sites at Asn27 and Asn37, contributing to its heterogeneity.[19]GM-CSF folds into a compact four-α-helix bundle, a hallmark of short-chain helical bundle cytokines, arranged in an up-up-down-down topology where helices A and B point upward and helices C and D point downward relative to a central hydrophobic core.[20] This bundle is flanked by two short antiparallel β-sheets, forming a globular domain approximately 30 Å in diameter.[18] The structure is stabilized by two intramolecular disulfide bonds: one linking Cys54 to Cys96 and the other connecting Cys88 to Cys121, which maintain the integrity of the loop regions and helical packing.[21] These bonds are essential for the protein's thermal stability and resistance to proteolysis.[22]Crystallographic studies, such as the refined structure at 2.4 Å resolution (PDB ID: 2GMF), highlight the spatial organization of functionally critical residues on the helical surfaces.[20] For instance, Arg23 on helix A and Lys72 on helix C are positioned on the exposed face of the bundle, forming part of the primary receptor-binding interface through electrostatic and hydrogen-bonding interactions.[20]Mutagenesis of these residues significantly impairs binding affinity, underscoring their role in ligand recognition without altering the overall fold.[23]
Glycosylation and Modifications
Human granulocyte-macrophage colony-stimulating factor (GM-CSF) undergoes N-linked glycosylation primarily at two asparagine residues, Asn27 and Asn37, which are the only potential consensus sites (Asn-X-Ser/Thr) in its 127-amino-acid polypeptide chain.[19] These modifications involve the attachment of complex oligosaccharide chains, typically tri- or tetraantennary structures with high fucose content (>90% α1-6-linked fucose) and sialylation, contributing to the protein's molecular heterogeneity observed between 18 and 32 kDa in recombinant forms.[19] In some production systems, site occupancy varies, with a portion of molecules glycosylated at only one N-site, leading to isoforms with differing charge and size profiles.[19]O-linked glycosylation occurs in the N-terminal region of GM-CSF, predominantly at Ser7, Ser9, and Thr10, with occasional extension to Ser5 in more heavily modified forms.[24] These O-glycans are typically simple structures, such as NeuNAcα2-3Galβ1-3GalNAc, and are more prominent in recombinant productions, where they influence the protein's overall molecular weight and conformational stability.[19] Unlike N-linked sites, O-glycosylation is not essential for core folding but adds to the glycoprotein's diversity, with up to three or four sites occupied depending on the expression host.[25]Native GM-CSF, derived from human sources, exhibits extensive glycosylation, including both N- and O-linked modifications with complex sialylated chains that enhance circulatory persistence.[26] In contrast, recombinant forms like sargramostim (produced in yeast) feature two N-linked glycans at Asn27 and Asn37 but with simpler, mannose-rich O-glycans, resulting in less overall glycosylation compared to native protein.[26] This reduced modification in recombinants, such as those from CHO cells, often shows variable O-glycan occupancy and fewer sialic acid residues, affecting electrophoretic mobility and isoform distribution.[19]These post-translational modifications significantly impact GM-CSF pharmacokinetics by extending serum half-life; unglycosylated forms clear rapidly with half-lives of 5-20 minutes, while glycosylated variants achieve circulation times of several hours due to sialylation shielding against hepatic clearance.[19] Desialylation accelerates elimination via asialoglycoprotein receptors, underscoring the role of terminal sialic acids in prolonging bioavailability.[19] In recombinant sargramostim, the presence of two N-glycans supports a pharmacokinetic profile closer to native GM-CSF, with improved stability over non-glycosylated analogs.[26]
Receptor and Signaling
Receptor Complex
The granulocyte-macrophage colony-stimulating factor (GM-CSF) receptor is a heterodimeric complex composed of a ligand-specific α subunit, encoded by the CSF2RA gene, and a shared β subunit (βc), encoded by the CSF2RB gene. The α subunit is unique to the GM-CSF receptor, while the βc chain is common to the receptors for interleukin-3 (IL-3) and IL-5, enabling shared signaling components among these cytokines.[27]Expression of the GM-CSF receptor is primarily restricted to cells of the myeloid lineage, including hematopoietic progenitors, monocytes, macrophages, and dendritic cells. The α subunit alone confers low-affinity binding to GM-CSF (with a dissociation constant in the nanomolar range), but association with the βc subunit forms a high-affinity complex (picomolar range), which is essential for effective ligand recognition and cellular activation.[28]Upon ligand binding, the receptor assembles into a 2:2 stoichiometry complex, where two GM-CSF molecules bridge two α-β heterodimers, forming a hexameric structure that stabilizes the interaction. Two such hexamers associate in a head-to-head manner to form the signaling-competent dodecameric complex. This arrangement positions the cytokine between the receptor subunits, with specific interfaces involving the N-terminal and D1-D2 domains of the α chain and the cytokine-binding regions of the βc chain.[29]Crystal structures of the extracellular domains, such as that deposited in the Protein Data Bank (PDB ID 4NKQ), have elucidated the molecular architecture of this hexameric assembly, revealing a distinct activation mechanism compared to other cytokine receptors. These structures highlight key hydrophobic and electrostatic interactions at the cytokine-receptor interfaces, which drive dimerization of the βc chains and ensure specificity in ligand binding.[29]
Intracellular Signaling Pathways
Upon binding of granulocyte-macrophage colony-stimulating factor (GM-CSF) to its receptor complex, which consists of an alpha chain (CSF2RA) and a shared beta chain (CSF2RB) with interleukin-3 and interleukin-5 receptors, the receptor undergoes dimerization, recruiting and activating Janus kinase 2 (JAK2) molecules associated with the beta chain cytoplasmic domains.[30] This activation leads to autophosphorylation of JAK2 and subsequent tyrosine phosphorylation of specific residues on the receptor beta chain, creating docking sites for downstream signaling effectors.[31]The primary signaling cascade initiated by JAK2 involves the phosphorylation and activation of signal transducer and activator of transcription 5 (STAT5), with STAT5a and STAT5b isoforms serving as key mediators.[5] Phosphorylated STAT5 dimers translocate to the nucleus, where they bind to gamma-activated sites in the promoters of target genes involved in cellular processes such as survival and differentiation.[32] Additionally, GM-CSF induces tyrosinephosphorylation of STAT3, which also undergoes nuclear translocation to regulate transcription, although STAT5 remains the dominant STAT family member in this pathway.[33] Parallel pathways are activated concurrently: the phosphoinositide 3-kinase (PI3K)-Akt axis promotes cell survival by inhibiting pro-apoptotic proteins, while the mitogen-activated protein kinase/extracellular signal-regulated kinase (MAPK/ERK) pathway drives proliferative responses through activation of transcription factors like Elk-1.[30]Protein kinase C (PKC) signaling, particularly via PKC isoforms, contributes to differentiation signals by modulating cytoskeletal rearrangements and gene expression in myeloid cells.[34]To prevent excessive or prolonged signaling, negative regulators such as suppressors of cytokine signaling (SOCS) proteins, particularly SOCS3, are induced in a feedback loop, binding to phosphorylated JAK2 or receptor chains to inhibit further kinase activity.[35] Protein tyrosine phosphatases, including SHP-1 and SHP-2, also dephosphorylate key components like JAK2 and receptor tyrosines, attenuating the signal and maintaining homeostasis in responsive cells.[36]
Biological Functions
Hematopoietic Effects
Granulocyte-macrophage colony-stimulating factor (GM-CSF) plays a central role in hematopoiesis by regulating the proliferation and differentiation of myeloid progenitors in the bone marrow. It acts primarily on early myeloid progenitors, such as common myeloid progenitors (CMPs), and can influence hematopoietic stem cells (HSCs) in certain contexts to drive the expansion of the granulocyte-macrophage lineage, ensuring the production of key immune effector cells primarily during stress or emergency conditions, such as infection or inflammation.[28]GM-CSF stimulates hematopoietic stem cells and common myeloid progenitors (CMPs) to differentiate into granulocyte-macrophage progenitors (GMPs), which serve as bipotent precursors for both granulocytic and monocytic lineages. This process occurs in a concentration-dependent manner, promoting the commitment of progenitors toward myeloid fates while restricting alternative lineages such as erythropoiesis. Through this mechanism, GM-CSF supports the maintenance of myeloid homeostasis in the bone marrow niche.[37][28]Following GMP formation, GM-CSF further promotes the differentiation and maturation of these progenitors into neutrophils, eosinophils, monocytes, and macrophages. It enhances the survival, proliferation, and functional maturation of these cells, enabling rapid responses to infection or inflammation by increasing myeloid output. In vitro studies demonstrate that GM-CSF can increase the number of colony-forming unit-granulocyte-macrophage (CFU-GM) colonies by up to several dozen-fold under optimal conditions, highlighting its potent stimulatory capacity.[38][39][40]GM-CSF exhibits synergy with other colony-stimulating factors, such as granulocyte colony-stimulating factor (G-CSF), in colony formation assays, where their combination yields greater numbers and sizes of granulocytic and macrophage colonies compared to either factor alone. This cooperative effect amplifies hematopoietic recovery, particularly in settings of myelosuppression. Signaling through the GM-CSF receptor activates pathways including STAT5, which mediates progenitorproliferation and differentiation.[41][42][43]
Immune and Inflammatory Roles
Granulocyte-macrophage colony-stimulating factor (GM-CSF) plays a critical role in modulating the functions of mature myeloid cells during immune responses and inflammation, enhancing host defense against pathogens while also contributing to inflammatory processes. It activates and primes these cells to improve their antimicrobial and antigen-presenting capabilities, thereby bridging innate and adaptive immunity. In inflammatory contexts, GM-CSF promotes the recruitment and activation of monocytes and granulocytes, sustaining immune responses but potentially exacerbating chronic conditions.[32]GM-CSF activates macrophages, enhancing their phagocytosis of pathogens and debris, which is essential for clearing infections. It stimulates the production of pro-inflammatory cytokines such as TNF-α, IL-6, and IL-23 by macrophages, amplifying the inflammatory cascade and promoting Th17 cell differentiation. Additionally, GM-CSF upregulates MHC class II expression on macrophages, improving their antigen presentation to T cells and facilitating adaptive immune activation.[4][28][32]For neutrophils, GM-CSF enhances migration to sites of infection by increasing adhesion and trafficking capabilities, while also priming them for oxidative burst through elevated reactive oxygen species production. It prolongs neutrophil survival by delaying apoptosis, allowing sustained antimicrobial activity against pathogens like fungi during acute inflammation. These effects collectively bolster neutrophil-mediated defenses without primarily driving their differentiation from precursors.[4][28]GM-CSF is pivotal in dendritic cell (DC) maturation, promoting the differentiation and activation of subsets such as CD103+ CD11b+ DCs, which enhances their ability to present antigens via MHC II. This maturation process enables DCs to prime T cells more effectively, secreting cytokines like IL-6 and IL-23 to support T-cell differentiation and bridging innate and adaptive immunity in inflammatory settings.[4][32][28]In chronic inflammation, particularly in autoimmune diseases, GM-CSF drives sustained monocyte recruitment to tissues, where these cells differentiate into inflammatory macrophages that perpetuate pathology. For instance, it unlocks a pathogenic signature in Ly6C hi monocytes, coordinating tissue inflammation through ongoing myeloid cell activation and cytokine release. This mechanism contributes to the persistence of inflammation in conditions like rheumatoid arthritis and multiple sclerosis by maintaining monocyte-derived antigen-presenting cell activity.[32][4][28]
Non-Hematopoietic Roles
Granulocyte-macrophage colony-stimulating factor (GM-CSF), also known as CSF2, functions as an embryokine during early mammalian development, particularly in supporting trophoblast growth and placental function. In human pregnancy, GM-CSF is produced by uterine epithelial cells and trophoblast cells, where it promotes trophoblastproliferation and invasion, essential for proper implantation and placentation. Studies have shown that GM-CSF enhances the viability and developmental competence of preimplantation embryos, reducing apoptosis and improving blastocyst formation rates in vitro. Deficiency in GM-CSF leads to impaired fetal and placental development, as observed in animal models, underscoring its non-redundant role in embryonic survival and organogenesis.[44]Beyond reproduction, GM-CSF plays a critical role in maintaining lung homeostasis through regulation of alveolar macrophages (AMs). AMs, which are long-lived resident immune cells in the alveoli, rely on GM-CSF signaling for maturation, survival, and phagocytic function, particularly in the clearance of pulmonary surfactant to prevent accumulation that could impair gas exchange. Produced primarily by alveolar type II epithelial cells, GM-CSF ensures surfactant homeostasis by activating pathways that enhance lipidcatabolism in AMs; disruptions in this axis, as seen in GM-CSF knockout mice, result in alveolar proteinosis-like phenotypes with surfactant overload. This function highlights GM-CSF's essentiality in non-inflammatory pulmonary maintenance, independent of its hematopoietic effects.[45]In the central nervous system (CNS), GM-CSF exerts neuroprotective effects by modulating microglial activation following injury. Post-traumatic events, such as traumatic brain injury or ischemia, trigger GM-CSF release from neurons and endothelial cells, which promotes a noninflammatory microglial phenotype that supports neuronal survival and repair. This cytokine enhances microglial proliferation without inducing excessive inflammation, thereby facilitating debris clearance and limiting secondary damage; for instance, exogenous GM-CSF administration in rodent models of Parkinson's disease and brain injury reduces dopaminergicneuron loss and improves motor outcomes. These actions position GM-CSF as a key regulator of CNS resilience, bridging innate immunity with tissue protection.[46]GM-CSF also contributes to wound healing and tissue repair by stimulating epithelial cell proliferation in various tissues. In skin and mucosal wounds, locally produced GM-CSF from keratinocytes and fibroblasts accelerates re-epithelialization through direct mitogenic effects on epithelial cells and indirect enhancement of macrophage-mediated angiogenesis and extracellular matrix remodeling. Experimental evidence from murine wound models demonstrates that topical or systemic GM-CSF application increases keratinocyte migration and proliferation rates, shortening healing time without promoting fibrosis. This reparative role extends to gastrointestinal epithelia, where GM-CSF supports barrier integrity post-injury by fostering controlled proliferation and reducing ulceration severity.[47]
Production and Regulation
Cellular Sources
Granulocyte-macrophage colony-stimulating factor (GM-CSF) is primarily produced by activated T cells, particularly Th1 and Th17 subsets, which serve as a major source during inflammatory responses.[48] Macrophages and monocytes also contribute significantly as producers, releasing GM-CSF in response to immune activation.[49] Additionally, non-hematopoietic cells such as fibroblasts and endothelial cells synthesize GM-CSF, often in the context of tissue injury or infection.[50]Expression of GM-CSF is predominantly inducible, triggered by infections, inflammatory cytokines, or microbial stimuli, leading to rapid production from the aforementioned cellular sources.[51] In contrast, low constitutive levels are maintained in the lungs, primarily by type II alveolar epithelial cells and other pulmonary cells, supporting baseline alveolar macrophage homeostasis.[52]Tissue-specific production includes endothelial cells in inflamed vascular beds, which upregulate GM-CSF to amplify local immune responses.[38] In the bone marrow, osteoblasts constitutively produce GM-CSF and increase secretion upon bacterial exposure or hormonal signals, thereby influencing hematopoietic progenitor support.[53][54]Under normal physiological conditions, circulating plasma levels of GM-CSF are low, typically ranging from undetectable to approximately 1-5 pg/mL in healthy individuals.[55] In severe inflammatory states such as sepsis, these levels can rise markedly, often exceeding 30 pg/mL and reaching up to several hundred pg/mL in critical cases, reflecting heightened production from multiple cellular sources.[56]
Expression Regulation
The expression of granulocyte-macrophage colony-stimulating factor (GM-CSF), encoded by the CSF2 gene, is tightly controlled at multiple levels to ensure rapid induction during inflammation while maintaining basal repression. The proximal promoter region of the CSF2 gene, spanning approximately 100 base pairs upstream of the transcription start site, contains critical binding sites for transcription factors such as NF-κB, AP-1 (composed of Jun/Fos family members), and STAT5. These elements enable responsiveness to proinflammatory stimuli, including lipopolysaccharide (LPS) from bacterial sources, tumor necrosis factor-α (TNF-α), and interleukin-1 (IL-1). For instance, LPS and TNF-α activate NF-κB and AP-1 through Toll-like receptor and cytokine receptor signaling pathways, respectively, leading to enhanced recruitment of RNA polymerase II and initiation of GM-CSF transcription in immune cells like macrophages and T lymphocytes.[57][50][58]Transcriptional regulation of GM-CSF is further modulated by lineage-specific factors such as PU.1 (encoded by SPI1) and IRF4 in myeloid and immune cells. PU.1 binds to ETS motifs in the promoter and cooperates with other factors to drive basal and inducible expression, particularly in macrophages where it integrates signals from hematopoietic development. Similarly, IRF4 interacts with composite elements in the promoter to fine-tune GM-CSF production during dendritic cell maturation and inflammatory responses. Epigenetic modifications, including histone H3 and H4 acetylation at the promoter, create a transcriptionally permissive chromatin environment; for example, stimulation with TNF-α or IL-1 increases histone acetyltransferase activity, such as that of CBP/p300, promoting nucleosome remodeling and gene accessibility.[59][60][61]Post-transcriptional mechanisms provide additional layers of control, with microRNAs (miRNAs) influencing mRNA stability and translation. miR-21, upregulated in activated T cells, enhances GM-CSF expression by targeting repressors like FOXO1, thereby stabilizing CSF2 mRNA and promoting Th17 cell differentiation and cytokine output during autoimmune inflammation. Other miRNAs, such as those in the miR-133 family, modulate mRNA decay under oxidative stress conditions in airway epithelial cells. Feedback loops further refine expression: an autocrine circuit involving STAT5 binding to the CSF2 promoter amplifies GM-CSF production in response to inflammatory cues, sustaining myeloid cell activation. Conversely, glucocorticoids like dexamethasone suppress GM-CSF via transrepression of NF-κB and AP-1, reducing promoter activity and mRNA levels in epithelial and immune cells.[62][63][64][65]
History and Development
Discovery and Initial Characterization
The discovery of granulocyte-macrophage colony-stimulating factor (GM-CSF) began in the mid-1960s through studies on the in vitro growth of hematopoietic cells. In 1966, T.R. Bradley and Donald Metcalf at the Walter and Eliza Hall Institute observed that mouse bone marrow cells formed discrete colonies in semisolid agar cultures when stimulated by feeder layers or conditioned medium, revealing the existence of soluble factors regulating myeloid cell proliferation.[66] Subsequent work by Metcalf and colleagues in the late 1960s and early 1970s identified these activities in various sources, including mouse lung-conditioned medium, which potently stimulated the formation of granulocyte-macrophage colonies from colony-forming unit-granulocyte-macrophage (CFU-GM) progenitors.[67]During the 1970s, Metcalf's team further characterized GM-CSF using colony assays, distinguishing it from other colony-stimulating factors (CSFs) based on the morphology and composition of induced colonies: GM-CSF promoted mixed granulocyte-macrophage colonies, unlike macrophage-CSF (M-CSF), which yielded only macrophage colonies, or granulocyte-CSF (G-CSF), which produced primarily granulocyte colonies.[39] In 1977, Anthony Burgess, Helen Camakaris, and Metcalf achieved the first purification of mouse GM-CSF from lung-conditioned medium, isolating four glycoprotein forms with molecular weights of approximately 22-28 kDa that specifically stimulated CFU-GM proliferation and differentiation.[68]Initial studies on human GM-CSF activity emerged in the late 1970s, with conditioned medium from human placenta demonstrating stimulation of both mouse and human CFU-GM in colony assays.[69] Full purification of human GM-CSF was accomplished in 1984 by John C. Gasson and colleagues from serum-free medium of the Mo T-lymphoblast cell line, yielding a 22 kDa glycoprotein with high potency in stimulating human bone marrow CFU-GM, comparable to its murine counterpart but species-specific in activity. These biochemical characterizations laid the groundwork for later molecular cloning efforts.
Cloning and Recombinant Production
The molecular cloning of human granulocyte-macrophage colony-stimulating factor (GM-CSF) was accomplished in 1985 by several independentresearch groups, utilizing complementary DNA (cDNA) libraries derived from activated human T-lymphocytes. A pivotal study by Wong et al. isolated full-length cDNA clones from mRNA of phytohemagglutinin-stimulated peripheral blood T cells, encoding a 207-amino acid precursor protein that matures to a 144-amino acid polypeptide with two potential N-linked glycosylation sites, sharing approximately 60% sequence homology with the previously cloned murine GM-CSF.[70] Concurrently, Lee et al. cloned the human GM-CSF cDNA from a similar T-cell library, confirming the codingsequence and identifying a single-copy gene structure with introns, which facilitated initial functional validation through transient expression assays. These efforts built on prior biochemical assays that had partially sequenced native GM-CSF to design oligonucleotide probes for library screening.[70]Following cloning, recombinant human GM-CSF (rhGM-CSF) production was established in prokaryotic and eukaryotic expression systems to enable large-scale manufacturing for research and therapeutic applications. Early expression in Escherichia coli yielded non-glycosylated rhGM-CSF with a molecular weight of approximately 14.5 kDa, demonstrating comparable in vitro bioactivity to the native protein in stimulating colony formation but with reduced circulatory half-life due to the absence of glycosylation.[70] To address this, glycosylated variants were developed in yeast (Saccharomyces cerevisiae) and mammalian cells, such as Chinese hamster ovary (CHO) cells, which introduce O- and N-linked glycans more akin to the native human form, enhancing protein stability, solubility, and pharmacokinetics.[25]Key therapeutic analogs emerged from these systems, including sargramostim (Leukine), a yeast-derived glycosylated rhGM-CSF approved by the FDA in 1991, featuring a leucine substitution at position 23 relative to the native sequence for optimized expression and with a specific activity of approximately 5.6 × 10^6 IU/mg.[71][72] In contrast, molgramostim, produced in E. coli as a non-glycosylated 127-amino acid protein, offers a simpler production process but requires formulation adjustments to mitigate rapid clearance.[73] Production challenges centered on glycosylation optimization, as yeast-derived forms exhibit hypermannosylated O-glycans that can provoke immunogenicity or alter receptor binding, while mammalian systems provide more human-like sialylated structures at the cost of higher complexity and yield variability; strategies like site-directed mutagenesis and glycoengineering have been employed to balance bioactivity and manufacturing efficiency.[25][74]
Clinical Applications
Approved Uses and Therapeutics
Granulocyte-macrophage colony-stimulating factor (GM-CSF) is utilized in approved therapeutics primarily through its recombinant form, sargramostim (Leukine), which stimulates hematopoiesis to accelerate myeloid cell recovery. The U.S. Food and Drug Administration (FDA) approved sargramostim on March 5, 1991, for acceleration of myeloid reconstitution following autologous peripheral blood progenitor cell (PBPC) or bone marrow transplantation in adult and pediatric patients ≥2 years with non-Hodgkin's lymphoma (NHL), acute lymphoblastic leukemia (ALL), and Hodgkin's lymphoma (HL).[75] It is also indicated for acceleration of myeloid reconstitution following allogeneic bone marrow transplantation from HLA-matched related donors in adult and pediatric patients ≥2 years.[76] Additional indications include shortening the time to neutrophil recovery and reducing the incidence of severe infections following induction chemotherapy in adults aged 55 years and older with acute myelogenous leukemia (AML),[72] mobilization of hematopoietic progenitor cells into peripheral blood for collection by leukapheresis for autologous transplantation in adults,[76] and to increase survival in patients from birth to <18 years old acutely exposed to myelosuppressive doses of radiation (hematopoietic syndrome of acute radiation syndrome [H-ARS]).[76]For delayed engraftment or graft failure post-BMT, sargramostim supports neutrophil recovery by promoting the proliferation and differentiation of hematopoietic progenitor cells.[72] The standard dosing regimen varies by indication but generally involves 250 μg/m²/day administered subcutaneously or intravenously, with infusion times of 2 to 24 hours depending on the setting, typically starting 2 to 4 hours after BMT or around day 11 post-chemotherapy, and continued until the absolute neutrophil count exceeds the target (500 or 1,500 cells/mm³ for three consecutive days, depending on indication), for up to 42 days.[72][76] Pharmacokinetically, sargramostim exhibits a half-life of approximately 1.4 hours following subcutaneous injection, with peak serum levels occurring 1 to 3 hours post-dose and facilitating targeted stimulation of bone marrow function.[76]Another approved application involves talimogene laherparepvec (Imlygic), an oncolytic immunotherapy approved by the FDA on October 27, 2015, for the local treatment of unresectable cutaneous, subcutaneous, and nodal lesions in patients with melanoma recurrent after initial surgery.[77] This genetically modified herpes simplex virus type 1 replicates selectively in tumor cells, leading to cell lysis and the production of GM-CSF, which enhances antitumor immune responses by recruiting and activating dendritic cells and T cells.[77] Imlygic is administered via intralesional injection, with an initial dose of up to 4 mL at 10⁶ plaque-forming units (PFU)/mL followed by 10⁸ PFU/mL every 2 weeks, continuing for at least 6 months or until injectable lesions are absent.[77]
Investigational Uses and Disease Associations
GM-CSF has been implicated in the pathogenesis of various autoimmune diseases, where elevated levels contribute to sustained inflammation by activating myeloid cells such as macrophages and dendritic cells. In rheumatoid arthritis (RA), GM-CSF promotes the differentiation and activation of proinflammatory macrophages, exacerbating joint inflammation and tissue damage.[78] Similarly, in multiple sclerosis (MS), increased GM-CSF production by autoreactive T cells drives the recruitment and activation of microglia and macrophages in the central nervous system, perpetuating demyelination and neuroinflammation.[79] These findings have spurred investigations into GM-CSF blockade as a therapeutic strategy to mitigate disease progression in these conditions.[80]During the COVID-19 pandemic, studies from 2020-2021 highlighted GM-CSF's role in hyperinflammatory responses, particularly in severe cases characterized by cytokine storms and acute respiratory distress syndrome. Elevated GM-CSF levels were associated with excessive activation of alveolar macrophages, leading to lung tissue damage and systemic inflammation.[81] Blocking GM-CSF signaling has shown promise in preclinical models and early clinical observations for reducing this hyperinflammation, with antibodies targeting the cytokine pathway improving outcomes in hypoxic patients.[82]Investigational applications of GM-CSF include its use to counteract sepsis-induced immunosuppression, where the cytokine restores monocytic function and enhances antimicrobial responses in critically ill patients. In phase II trials, recombinant GM-CSF administration safely reversed immunoparalysis, shortening recovery time from secondary infections.[83] Conversely, antagonists such as lenzilumab, a monoclonal antibody against GM-CSF, are being explored to dampen cytokine storms in hyperinflammatory states, including severe infections, by neutralizing the cytokine and limiting myeloid cell overactivation.[84]GM-CSF is associated with cancer progression, notably in acute myeloid leukemia (AML), where it stimulates the proliferation and survival of leukemic blasts, potentially worsening disease outcomes.[85] In neurodegenerative diseases, GM-CSF influences microglial activation, contributing to neuroinflammation; for instance, in Alzheimer's disease models, it sustains proinflammatory microglial states that may accelerate amyloid plaque formation and neuronal loss, while in Parkinson's disease, it can modulate microglial phenotypes toward either protective or detrimental effects depending on context.[86][87]
Safety and Adverse Effects
Granulocyte-macrophage colony-stimulating factor (GM-CSF), administered as recombinant sargramostim, is generally well-tolerated in clinical settings, but common adverse effects occur in a significant proportion of patients. These include fever, fatigue, bone pain, and injection-site reactions such as erythema, pain, or swelling, with incidences typically ranging from 20% to 50% depending on the dosing regimen and patient population.[76][71] Other frequently reported effects encompass nausea, diarrhea, and musculoskeletal discomfort, often resolving with supportive care or dose adjustment.[76]Serious risks associated with GM-CSF therapy, though less common, require vigilant monitoring. Capillary leak syndrome, characterized by hypotension, edema, and organ dysfunction, has an incidence of less than 1% but can be life-threatening, particularly at higher doses; it is managed through dose reduction or discontinuation.[76] Pericardial effusion occurs in approximately 4% of patients compared to 1% in placebo groups, often linked to fluid retention, and first-dose reactions—manifesting as hypoxia, hypotension, flushing, or respiratory distress—affect a subset of patients shortly after initial administration but rarely recur with subsequent doses.[76][88]Contraindications for GM-CSF include hypersensitivity to the drug, yeast-derived products, or its components, as well as excessive leukemic myeloid blasts (≥10%) in bone marrow or peripheral blood due to the risk of stimulating malignant cell growth.[76] It requires monitoring for splenomegaly, which can develop as a side effect and rarely progress to splenic rupture.[89][90]Long-term concerns with prolonged GM-CSF use center on its potential to promote tumor growth in myeloid malignancies by stimulating proliferation of leukemic cells, necessitating discontinuation if disease progression is observed.[76][37] Additionally, immunogenicity may develop in up to 82.9% of patients on extended therapy, potentially leading to reduced efficacy or hypersensitivity, though clinical impact is variable.[76]
Recent Advances and Research Directions
Key Clinical Trials
One of the earliest pivotal trials for granulocyte-macrophage colony-stimulating factor (GM-CSF) involved sargramostim, a recombinant form of GM-CSF, in acute myeloid leukemia (AML). In a randomized, placebo-controlled phase III trial conducted by the Eastern Cooperative Oncology Group in the 1990s, 124 patients aged 55 to 70 years with AML received induction chemotherapy with or without sargramostim (yeast-derived GM-CSF at 250 μg/m²/day). The trial demonstrated a higher complete remission rate of 60% in the sargramostim arm compared to 44% in the placebo arm (P = 0.08), with faster neutrophil recovery and reduced incidence of severe infections.[91] Longer-term analysis showed a survival benefit, with median overall survival of 10.6 months versus 4.8 months in the placebo group (P = 0.048), primarily due to lower early mortality from infections in elderly patients.[91]During the COVID-19 pandemic, anti-GM-CSF therapies were investigated to mitigate hyperinflammation in severe cases. The OSCAR trial, a phase II randomized, double-blind study (NCT04376684), evaluated otilimab, a monoclonal antibody targeting GM-CSF, in 806 hospitalized patients with severe COVID-19pneumonia requiring oxygen or ventilation. Patients received a single intravenous dose of otilimab (90 mg) or placebo alongside standard care. While the primary endpoint of proportion alive and free of respiratory failure at day 28 was not significantly different (71% vs. 67%; odds ratio 1.23, 95% CI 0.89-1.68), secondary analyses indicated a trend toward benefit, with median ventilator-free days of 25 in the otilimab group versus 23 in placebo (P = 0.07) and faster resolution of inflammation markers like C-reactive protein. No new safety signals emerged, though development was discontinued due to lack of primary endpoint achievement.In oncology, GM-CSF has been combined with immune checkpoint inhibitors to enhance antitumor immunity. A multicenter phase II randomized trial (E1608) assessed sargramostim (250 μg/m² subcutaneously three times weekly) added to ipilimumab (3 mg/kg every 3 weeks for four doses, then maintenance) in 245 patients with advanced melanoma. The combination improved median overall survival to 17.5 months compared to 13.0 months with ipilimumab alone (hazard ratio 0.70, 95% CI 0.51-0.96; P = 0.02), with similar objective response rates (42% vs. 39%) but reduced grade 3/4 adverse events (36% vs. 48%).[92] This benefit was attributed to GM-CSF's role in dendritic cell activation and T-cell priming, supporting further exploration in checkpoint combinations. An ongoing phase II/III trial (NCT02339571; ECOG-ACRIN EA6141) is evaluating nivolumab plus ipilimumab with or without sargramostim in advanced melanoma.[93]Recent efforts have focused on GM-CSF blockade to mitigate toxicities in CAR-T cell therapy. The ZUMA-19 trial (NCT04314843), a phase I/II multicenter study, combined lenzilumab (anti-GM-CSF monoclonal antibody at 600-1800 mg IV) with axicabtagene ciloleucel in patients with relapsed/refractory large B-cell lymphoma. In the initial cohort of six high-risk patients, 83% achieved objective responses, with no grade 3 or higher cytokine release syndrome (CRS) or immune effector cell-associated neurotoxicity (ICANS), compared to 13% and 28% rates in the ZUMA-1 trial without lenzilumab. The trial was terminated in 2023 following the sponsor's bankruptcy, with no further expanded cohort data reported.
Emerging Therapeutic Strategies
Recent research has highlighted the potential of GM-CSF antagonists in treating autoimmune conditions such as rheumatoid arthritis (RA) and giant cell arteritis (GCA). Mavrilimumab, a monoclonal antibody targeting the GM-CSF receptor alpha chain, demonstrated superior efficacy in a phase 2 trial for GCA, where it significantly prolonged time to first flare and increased sustained remission rates compared to placebo when combined with a prednisone taper.[94] In RA, phase 2 studies of mavrilimumab showed dose-dependent improvements in disease activity scores and reductions in inflammatory biomarkers, with long-term extensions confirming sustained responses up to 122 weeks in a subset of patients.[95] Although phase 3 trials for these indications have not yet reported definitive results as of 2025, these findings position GM-CSF blockade as an emerging strategy to mitigate chronic inflammation by disrupting myeloid cell activation in affected tissues.[96]Gene therapy approaches incorporating GM-CSF expression have emerged as innovative vaccine platforms, particularly for HIV and cancer. Viral vectors, such as modified vaccinia Ankara (MVA) or adenovirus-based systems co-expressing GM-CSF with HIV antigens, enhance dendritic cell recruitment and T-cell priming, leading to robust cellular immune responses in preclinical models and early clinical studies.[97] For cancer, oncolytic viruses like talimogene laherparepvec (T-VEC/IMLYGIC), which expresses GM-CSF to amplify antitumor immunity, represent an approved paradigm, while newer DNA vaccines fusing tumor antigens with codon-optimized GM-CSF genes have shown increased protein expression and improved immunogenicity in phase 1 trials for solid tumors.[98] These strategies leverage GM-CSF's role in amplifying antigen presentation, offering localized immune boosting without systemic toxicity.[99]Key challenges in advancing GM-CSF-targeted therapies include developing reliable biomarkers for patient selection and addressing resistance in chronic inflammatory settings. Elevated baseline serum GM-CSF levels have been identified as a pharmacodynamic biomarker correlating with disease activity and response to GM-CSF antagonists like mavrilimumab in RA cohorts, potentially guiding stratification for non-responders to TNF inhibitors.[100] In chronic inflammation, resistance may arise from redundant cytokine pathways (e.g., IL-6 or IL-17 signaling), necessitating combination regimens; preclinical evidence suggests that dual blockade overcomes this by suppressing persistent myeloid activation.[4] These hurdles underscore the need for personalized approaches to optimize therapeutic outcomes.[101]