Functional Annotation of Human RASA2 (Q15283) OpenAI o3-deep-research-2025-06-26 68 citations 2025-11-04T00:10:36.611892

Functional Annotation of Human RASA2 (Q15283)

Gene and Protein Overview

RASA2 (RAS p21 protein activator 2, UniProt Q15283) is a human gene encoding a Ras GTPase-activating protein (Ras GAP) that turns off Ras signaling by accelerating the hydrolysis of Ras-bound GTP (pmc.ncbi.nlm.nih.gov). The RASA2 protein belongs to the GAP1 family of Ras GAPs and is sometimes referred to by the alias GAP1(m) (www.ncbi.nlm.nih.gov). By enhancing Ras’s weak intrinsic GTPase activity, RASA2 promotes conversion of active Ras–GTP to inactive Ras–GDP, thereby suppressing Ras function (www.ncbi.nlm.nih.gov). This “off-switch” role allows RASA2 to control downstream signaling pathways that drive cell proliferation and differentiation (www.ncbi.nlm.nih.gov). Importantly, RASA2 stimulates GTP hydrolysis on normal Ras (p21) but is ineffective on certain oncogenic Ras mutants (e.g. Ras^G12V), which are resistant to GAPs (www.ncbi.nlm.nih.gov). In essence, RASA2 is a negative regulator of Ras, helping maintain appropriate Ras activity levels in cells.

Protein Structure and Localization

The RASA2 protein is a multi-domain cytosolic protein that can associate with the inner surface of the plasma membrane in response to signaling cues. It has a conserved C-terminal RasGAP domain responsible for its catalytic activity, and N-terminal regulatory domains typical of the GAP1 family (pmc.ncbi.nlm.nih.gov) (pmc.ncbi.nlm.nih.gov). Notably, RASA2 contains two tandem C2 domains (calcium-dependent phospholipid-binding domains) and a pleckstrin homology (PH) domain, also known as a BTK-type PH domain (pmc.ncbi.nlm.nih.gov). These domains mediate lipid binding and subcellular targeting: for example, the PH domains of RASA2 and its close relative RASA3 bind strongly to the membrane lipid phosphatidylinositol (3,4,5)-trisphosphate (PIP₃) (pmc.ncbi.nlm.nih.gov). In fact, high-resolution pull-down experiments identified RASA2 as a PIP₃-binding protein, indicating that RASA2 is recruited to PIP₃-enriched membranes (such as activated receptor signaling sites) (pmc.ncbi.nlm.nih.gov). The C2 domains can bind membranes in a Ca²⁺-dependent manner, suggesting that calcium signals may also promote RASA2 membrane localization (pmc.ncbi.nlm.nih.gov). Together, these domains allow RASA2 to shuttle from the cytosol to the plasma membrane where its substrate Ras resides. RASA2 lacks transmembrane regions and is not secreted; it functions inside the cell, with its activity occurring at the cytosol–inner membrane interface. Consistent with a general signaling role, RASA2 is broadly expressed across tissues, with particularly notable expression in immune and lymphoid organs (www.ncbi.nlm.nih.gov). This widespread distribution reflects its fundamental role in regulating Ras signals in many cell types.

Biochemical Function and Mechanism

As a Ras GTPase-activating protein, RASA2’s primary biochemical function is to catalyze the inactivation of Ras by accelerating Ras’s GTPase activity. Ras proteins are molecular switches that toggle between an active GTP-bound state and an inactive GDP-bound state. RASA2 binds to active Ras–GTP and inserts a “catalytic arginine finger” into Ras’s active site, greatly accelerating GTP hydrolysis (pmc.ncbi.nlm.nih.gov). In the human RASA2 protein, the critical arginine residue is Arg-511, which is contributed into the Ras catalytic site to stimulate GTP cleavage to GDP (pmc.ncbi.nlm.nih.gov). This mechanism is analogous to other Ras GAPs (such as p120^RasGAP/RASA1 and neurofibromin), whereby the GAP protein provides an arginine residue that complements Ras’s active-site chemistry and induces GTP breakdown (pmc.ncbi.nlm.nih.gov). Through this enzymatic action, RASA2 converts Ras-GTP (active) to Ras-GDP (inactive), effectively terminating the Ras signal. The “substrate” of RASA2 is Ras (primarily H-Ras, N-Ras, K-Ras and related small GTPases in the Ras subfamily) in its GTP-bound form. RASA2 shows specificity for normal (wild-type) Ras and does not effectively stimulate hydrolysis on mutant Ras proteins that carry activating oncogenic mutations (www.ncbi.nlm.nih.gov). Some GAP1 family members are known to act on the Ras-related GTPase Rap1 as well as Ras (pmc.ncbi.nlm.nih.gov); however, RASA2 is chiefly a Ras-specific GAP in physiological contexts, whereas the related RASA3 (GAP1^IP4BP) predominantly inactivates Rap1 (pmc.ncbi.nlm.nih.gov). By turning off Ras, RASA2 attenuates downstream signaling cascades initiated by Ras, most prominently the RAF–MEK–ERK (MAP kinase) pathway which controls cell growth and differentiation. In this way, RASA2 acts as a molecular brake in signaling pathways that require timely shutdown of Ras activity.

Biological Role in Signaling Pathways

RASA2 plays a critical role in regulating Ras-dependent signaling pathways, thereby influencing various cellular processes. Ras activation is a key step in pathways downstream of many receptors (e.g. growth factor receptors, cytokine receptors, antigen receptors), leading to outcomes such as proliferation, differentiation, and survival. RASA2 provides negative feedback in these pathways by ensuring that Ras activation is transient and appropriately scaled. For example, in growth factor signaling, receptor tyrosine kinases activate Ras (via Ras GEFs like SOS or RasGRP), and RASA2 can bind to the membrane (through its PH domain binding PIP₃ generated by receptor-activated PI3K) to inactivate Ras and terminate the signal (pmc.ncbi.nlm.nih.gov). This feedback loop prevents over-activation of the Ras–MAPK cascade, thereby maintaining normal control of cell proliferation. Consistently, loss of RASA2 leads to prolonged or enhanced Ras signaling, which can drive excessive cell growth and other aberrant behaviors (pmc.ncbi.nlm.nih.gov).

One well-studied context for RASA2 function is in T lymphocyte signaling. Ras activation is essential for T-cell receptor (TCR) signaling, leading to downstream ERK/MAPK activation important for T cell proliferation and activation. Recent genetic screens in primary human T cells identified RASA2 as a crucial “brake” on TCR signaling (pmc.ncbi.nlm.nih.gov) (pmc.ncbi.nlm.nih.gov). RASA2 is expressed in both CD4⁺ and CD8⁺ T cells (pmc.ncbi.nlm.nih.gov), and when T cells are stimulated via the TCR, RASA2 normally acts to limit Ras activity and downstream activation. In experiments using CRISPR/Cas9 knockout, loss of RASA2 resulted in a roughly 2-fold increase in T cell proliferation upon stimulation, along with upregulation of activation markers (such as CD69 and CD154) (pmc.ncbi.nlm.nih.gov). RASA2-deficient T cells also showed enhanced functional outcomes – for instance, T cells lacking RASA2 had heightened sensitivity to antigen and killed target cancer cells more efficiently in co-culture assays (pmc.ncbi.nlm.nih.gov). Notably, RASA2 knockout T cells proliferated more robustly even under typically suppressive conditions (presence of immunosuppressive factors like adenosine, TGF-β, or regulatory T cells) (pmc.ncbi.nlm.nih.gov). These findings demonstrate that RASA2 serves as a gatekeeper in the TCR signaling pathway, restraining Ras/MAPK pathway activation to keep T cell responses in check (pmc.ncbi.nlm.nih.gov). When RASA2 is removed, Ras signaling goes unchecked, resulting in hyperactive T cell responses. This precise role in T cells exemplifies how RASA2 functions in signaling pathways: by dampening Ras activity, it modulates the magnitude of downstream biological responses (in this case, cell proliferation and effector function). Such negative regulation is crucial for maintaining immune homeostasis and preventing over-activation.

Beyond T cells, RASA2 is thought to perform a similar homeostatic role in other cell types. It contributes to controlling Ras-dependent pathways in development and differentiation. Indeed, germline mutations in RASA2 have been identified in Noonan syndrome, a developmental disorder (Rasopathy) caused by hyperactive Ras/MAPK signaling (pmc.ncbi.nlm.nih.gov). Although RASA2 mutations appear to be a rare cause of Noonan syndrome, their occurrence underscores that RASA2’s regulatory function is important in normal human development – loss of RASA2 can elevate Ras signaling enough to produce developmental abnormalities (pmc.ncbi.nlm.nih.gov). In summary, RASA2 operates in multiple signaling contexts as a negative regulator: it ensures that Ras-driven pathways (like the MAPK cascade) are properly shut off, thereby influencing cell proliferation, differentiation, and activation in a tightly controlled manner.

Structural Features and Regulatory Interactions

The multi-domain structure of RASA2 hints at mechanisms by which its activity is regulated within the cell. The pleckstrin homology (PH) domain of RASA2 binds membrane phosphoinositides, especially PIP₃, with high affinity (pmc.ncbi.nlm.nih.gov). This means that when PI3K enzymes produce PIP₃ (for instance, during receptor signaling), RASA2 can be recruited to the plasma membrane via its PH domain. Co-localization at the membrane brings RASA2 into proximity with active Ras, enabling it to inactivate Ras at the site of signal transduction. Thus, PIP₃ acts as a docking signal for RASA2, coupling PI3K activation to Ras signal termination. This is a form of crosstalk between the PI3K pathway and Ras pathway: the generation of PIP₃ not only triggers AKT signaling but also helps initiate negative feedback on Ras through RASA2’s recruitment (pmc.ncbi.nlm.nih.gov).

The tandem C2 domains in RASA2 likely mediate additional regulatory interactions. C2 domains typically bind acidic phospholipids in a calcium-dependent manner. While RASA2’s C2 domains have not been studied as extensively as those of RASA4/CAPRI (a calcium-promoted Ras GAP), their presence suggests that calcium fluxes might enhance RASA2’s membrane association or activity. For example, analogies to RASA4 (which translocates to the membrane upon Ca²⁺ signals) raise the possibility that RASA2 could respond to Ca²⁺ increases by a similar mechanism (pmc.ncbi.nlm.nih.gov). In combination, the PH and C2 domains position RASA2 as a signal-responsive inhibitor: it integrates second messengers (like lipid products and Ca²⁺) to modulate when and where it turns off Ras. Structurally, RASA2 does not contain SH2 or SH3 domains (domains found in some other Ras regulators like RASA1/p120^RasGAP), so it may not directly bind phosphotyrosine sites on receptors. Instead, RASA2 relies on lipid-binding for localization, and potentially partners with other proteins via its PH/C2 regions or other motifs. There is evidence that RASA2 can form signaling complexes at the membrane; for instance, earlier studies showed that the closely related GAP1 family member (RASA3) binds inositol 1,3,4,5-tetrakisphosphate (IP₄) and PIP₂, suggesting complex regulatory ligand interactions (pmc.ncbi.nlm.nih.gov). RASA2’s PH domain, in particular, shows specificity for PIP₃, which may distinguish its recruitment profile from RASA3 or RASAL1 (pmc.ncbi.nlm.nih.gov).

On the enzymatic side, RASA2’s activity can be inferred to be subject to feedback regulation. When Ras is active, one of its downstream effects is to activate PI3K, raising PIP₃ levels; this in turn recruits RASA2 to dampen Ras – a negative feedback loop. Conversely, if Ras signaling is minimal, RASA2 may remain diffuse in the cytosol (less membrane-bound). This dynamic localization has been observed for similar GAP1 family proteins. In addition, post-translational modifications could regulate RASA2 (though specific modifications are not well characterized in literature as of current knowledge). By analogy, other Ras GAPs are known to be phosphorylated or cleaved in certain conditions (pmc.ncbi.nlm.nih.gov). One example in the broader GAP family: caspase-3 can cleave p120^RasGAP (RASA1) during apoptosis, enhancing Ras signaling in dying cells (pmc.ncbi.nlm.nih.gov). It’s reported that a point mutation preventing a RasGAP’s cleavage led to prolonged Ras activity (pmc.ncbi.nlm.nih.gov). Whether RASA2 undergoes similar regulatory phosphorylation or proteolysis remains to be fully explored, but these are potential layers of control. In summary, RASA2’s function is tightly linked to its structural domains: the PH and C2 domains target it to the membrane in response to lipid/Ca²⁺ signals, and the GAP domain then executes Ras inactivation. This design ensures RASA2 is activated at the right place and time to modulate Ras signaling.

Physiological and Clinical Significance

RASA2 is vital for normal cellular homeostasis, and its dysfunction has been implicated in human diseases that center on aberrant Ras signaling. Here are key contexts in which RASA2’s role has been highlighted:

Expert Commentary and Current Research Directions

Experts regard RASA2 as an important regulatory hub in Ras signaling, with roles that bridge fundamental biochemistry and clinical relevance. A 2023 review in Trends in Immunology dubbed RASA2 (and its Rap-GAP counterpart RASA3) “gatekeepers” of T cell activation and adhesion (pmc.ncbi.nlm.nih.gov) (pmc.ncbi.nlm.nih.gov), emphasizing that these GAPs maintain immune cells in a quiescent state until appropriate activation is needed. The authors note that genetic screens have firmly placed RASA2 as a key limiting factor in T cell responses (pmc.ncbi.nlm.nih.gov). They discuss the exciting possibility of manipulating RASA2 for therapy – for example, inhibiting RASA2 to enhance T cell attack on cancers, or conversely activating/augmenting RASA2 to tone down immune activation in autoimmunity (pmc.ncbi.nlm.nih.gov) (pmc.ncbi.nlm.nih.gov). Such ideas are built on solid experimental evidence (e.g. CRISPR studies) and represent a new direction in immunotherapy research. At the same time, cancer biologists have pointed out the significance of RASA2 in tumors lacking direct Ras mutations. Since Ras itself is hard to target with drugs (aside from specific mutants like KRAS^G12C), restoring or mimicking RASA2 function could be a strategy to suppress Ras activity in tumors. However, reactivating a lost tumor suppressor is challenging – thus, current research is more focused on understanding the pathways affected by RASA2 loss and finding synthetic lethal interactions. For instance, if a tumor loses RASA2, it might become particularly dependent on other signaling nodes that could be drugged. One study noted that RASA2 loss in melanoma often co-occurs with certain RAF or MEK pathway alterations, implying these tumors heavily rely on the MAPK cascade for growth (pmc.ncbi.nlm.nih.gov) (pmc.ncbi.nlm.nih.gov). This suggests that such tumors might respond well to MEK or ERK inhibitors, a hypothesis under investigation.

Structurally, ongoing research aims to resolve the three-dimensional structure of RASA2’s domains and their complexes with Ras, to better understand how exactly RASA2 engages Ras at membranes. While Ras–GAP interactions have been visualized for other GAPs (like p120^RasGAP and neurofibromin) (pmc.ncbi.nlm.nih.gov), RASA2 has unique regulatory domains whose conformational changes (perhaps upon binding PIP₃ or Ca²⁺) are of great interest. Bioinformatic analyses show that RASA2 and its GAP1 family homologs are evolutionarily conserved in vertebrates and share significant homology, hinting that insights from one (e.g. RASA3’s interaction with phosphoinositides) can inform understanding of another. There is also interest in evolutionary biology of Ras GAPs: RASA2 might have arisen to provide fine-tuned control of Ras in specialized contexts (potentially relating to the immune system, given its prominent expression there). Comparative studies in mice have indicated that Rasa2 deficiency can enhance immune responses (as seen in T cell studies), and future work may create Rasa2-knockout animal models to observe any spontaneous disease or predisposition (e.g. cancer incidence or autoimmune phenotypes) arising from chronic Ras hyperactivity.

In summary, RASA2 is recognized as a key functional node in the Ras signaling network, coupling membrane second messengers to the termination of Ras activity. Its primary role is enzymatic: stimulating GTP hydrolysis on Ras to shut Ras off at the right time and place. Through this function, it safeguards cells from excessive Ras signaling, thereby influencing processes like proliferation, migration, and immune cell activation. The protein localizes to the cytosol and inner plasma membrane, guided by its PH and C2 domains, ensuring it acts in proximity to Ras. Disruption of RASA2 has tangible biological consequences – from hyperactive T cells to aggressive tumor behavior – underscoring why nature has conserved this Ras regulator. Current research (2023–2024) continues to unravel the nuances of RASA2’s regulation and to exploit its function in clinical applications, whether by targeting it in immunotherapy or considering its status in cancer treatment decisions. All evidence to date solidifies the view of RASA2 as an essential “off-switch” for Ras, crucial for balanced signaling and normal cellular function (pmc.ncbi.nlm.nih.gov) (pmc.ncbi.nlm.nih.gov).

References: (Publication dates and sources are included in citations)

Citations

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  17. AnnotationURLCitation(end_index=6310, start_index=6180, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=Several%20RAS,specific%20GAPs%20%5B%2041%2C54')
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  27. AnnotationURLCitation(end_index=10488, start_index=10361, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=Repeats,these%20GAPs%2C%20how%20they%20are')
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  34. AnnotationURLCitation(end_index=15204, start_index=15070, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=which%20includes%20RASAL1%20,2%7D%20%5B%2050%2C32')
  35. AnnotationURLCitation(end_index=16077, start_index=15910, title='A Systematic Analysis of Expression and Function of RAS GTPase-Activating Proteins (RASGAPs) in Urological Cancers: A Mini-Review - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC12071082/#:~:text=Mutations%20in%20RASGAPs%20also%20play,of%20RASGAPs%20promote%20tumorigenesis%20by')
  36. AnnotationURLCitation(end_index=16383, start_index=16216, title='A Systematic Analysis of Expression and Function of RAS GTPase-Activating Proteins (RASGAPs) in Urological Cancers: A Mini-Review - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC12071082/#:~:text=Mutations%20in%20RASGAPs%20also%20play,of%20RASGAPs%20promote%20tumorigenesis%20by')
  37. AnnotationURLCitation(end_index=16649, start_index=16482, title='A Systematic Analysis of Expression and Function of RAS GTPase-Activating Proteins (RASGAPs) in Urological Cancers: A Mini-Review - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC12071082/#:~:text=Mutations%20in%20RASGAPs%20also%20play,of%20RASGAPs%20promote%20tumorigenesis%20by')
  38. AnnotationURLCitation(end_index=17762, start_index=17609, title='Recurrent inactivating RASA2 mutations in melanoma - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC4954601/#:~:text=Analysis%20of%20501%20melanoma%20exomes,of%20Ras%20GAPs%20in%20cancer')
  39. AnnotationURLCitation(end_index=18027, start_index=17861, title='Recurrent inactivating RASA2 mutations in melanoma - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC4954601/#:~:text=mutations%20encompass%20at%20least%2020,the%20CytoScan%20High%20Definition%20array')
  40. AnnotationURLCitation(end_index=18353, start_index=18200, title='Recurrent inactivating RASA2 mutations in melanoma - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC4954601/#:~:text=Analysis%20of%20501%20melanoma%20exomes,of%20Ras%20GAPs%20in%20cancer')
  41. AnnotationURLCitation(end_index=18658, start_index=18505, title='Recurrent inactivating RASA2 mutations in melanoma - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC4954601/#:~:text=Analysis%20of%20501%20melanoma%20exomes,of%20Ras%20GAPs%20in%20cancer')
  42. AnnotationURLCitation(end_index=19028, start_index=18875, title='Recurrent inactivating RASA2 mutations in melanoma - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC4954601/#:~:text=Analysis%20of%20501%20melanoma%20exomes,of%20Ras%20GAPs%20in%20cancer')
  43. AnnotationURLCitation(end_index=19355, start_index=19198, title='Recurrent inactivating RASA2 mutations in melanoma - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC4954601/#:~:text=Analysis%20of%20501%20melanoma%20exomes,importance%20of%20Ras%20GAPs%20in')
  44. AnnotationURLCitation(end_index=19948, start_index=19781, title='A Systematic Analysis of Expression and Function of RAS GTPase-Activating Proteins (RASGAPs) in Urological Cancers: A Mini-Review - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC12071082/#:~:text=Mutations%20in%20RASGAPs%20also%20play,of%20RASGAPs%20promote%20tumorigenesis%20by')
  45. AnnotationURLCitation(end_index=20118, start_index=19949, title='A Systematic Analysis of Expression and Function of RAS GTPase-Activating Proteins (RASGAPs) in Urological Cancers: A Mini-Review - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC12071082/#:~:text=cell%20lung%20cancer%20,pathological%20implications%20in%20urological%20malignancies')
  46. AnnotationURLCitation(end_index=20992, start_index=20831, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=RASA2%20was%20identified%20as%20an,defects%20and%20elevated%20RAS%20activity')
  47. AnnotationURLCitation(end_index=21245, start_index=21122, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=%2A%2039.Chen%20P,PMC%20free%20article')
  48. AnnotationURLCitation(end_index=22771, start_index=22651, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=match%20at%20L356%20Figure%202A,TCR')
  49. AnnotationURLCitation(end_index=22898, start_index=22772, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=match%20at%20L360%20antibodies%20in,2%2C3')
  50. AnnotationURLCitation(end_index=23240, start_index=23116, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=,cells%20during%20exhaustion%20and%20in')
  51. AnnotationURLCitation(end_index=23545, start_index=23421, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=,cells%20during%20exhaustion%20and%20in')
  52. AnnotationURLCitation(end_index=23700, start_index=23546, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=match%20at%20L215%20adoptive%20cell,T%20cell%20responses%20in%20mouse')
  53. AnnotationURLCitation(end_index=24074, start_index=23930, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=match%20at%20L211%20,cells%20during%20exhaustion%20and%20in')
  54. AnnotationURLCitation(end_index=24448, start_index=24304, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=match%20at%20L211%20,cells%20during%20exhaustion%20and%20in')
  55. AnnotationURLCitation(end_index=24856, start_index=24702, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=match%20at%20L215%20adoptive%20cell,T%20cell%20responses%20in%20mouse')
  56. AnnotationURLCitation(end_index=25193, start_index=25069, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=,cells%20during%20exhaustion%20and%20in')
  57. AnnotationURLCitation(end_index=26139, start_index=25961, title='Genome-wide CRISPR/Cas9 screens reveal shared and cell-specific mechanisms of resistance to SHP2 inhibition - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC9998968/#:~:text=To%20identify%20SHP2i%20resistance%20mechanisms%2C,sensitization%20to%20SHP2i%20required%20its')
  58. AnnotationURLCitation(end_index=26464, start_index=26286, title='Genome-wide CRISPR/Cas9 screens reveal shared and cell-specific mechanisms of resistance to SHP2 inhibition - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC9998968/#:~:text=To%20identify%20SHP2i%20resistance%20mechanisms%2C,sensitization%20to%20SHP2i%20required%20its')
  59. AnnotationURLCitation(end_index=27724, start_index=27563, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=RASA2%20and%20RASA3%2C%20which%20are,T%20cell%20activation%20and%20migration')
  60. AnnotationURLCitation(end_index=27852, start_index=27725, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=Repeats,these%20GAPs%2C%20how%20they%20are')
  61. AnnotationURLCitation(end_index=28200, start_index=28073, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=Repeats,these%20GAPs%2C%20how%20they%20are')
  62. AnnotationURLCitation(end_index=28559, start_index=28436, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=,T%20cell%20dysfunction%20in%20disease')
  63. AnnotationURLCitation(end_index=28701, start_index=28560, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=match%20at%20L221%20,expression%20of%20Rasa3%20and%20its')
  64. AnnotationURLCitation(end_index=29832, start_index=29645, title='Recurrent inactivating RASA2 mutations in melanoma - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC4954601/#:~:text=Cutaneous%20melanoma%2C%20for%20which%20incidence,additional%20targetable%20alterations%20in%20melanoma')
  65. AnnotationURLCitation(end_index=29961, start_index=29833, title='Recurrent inactivating RASA2 mutations in melanoma - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC4954601/#:~:text=We%20compiled%20somatic%20mutation%20data,of')
  66. AnnotationURLCitation(end_index=30489, start_index=30371, title='Mind the GAP: RASA2 and RASA3 GTPase Activating Proteins as gatekeepers of T cell activation and adhesion - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC10621891/#:~:text=B%29%20RAS,through%20a%20distinct')
  67. AnnotationURLCitation(end_index=32745, start_index=32574, title='A Systematic Analysis of Expression and Function of RAS GTPase-Activating Proteins (RASGAPs) in Urological Cancers: A Mini-Review - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC12071082/#:~:text=The%20RAS%20signaling%20pathway%2C%20a,overactive%2C%20fueling%20cancer%20growth%20and')
  68. AnnotationURLCitation(end_index=32873, start_index=32746, title='A Systematic Analysis of Expression and Function of RAS GTPase-Activating Proteins (RASGAPs) in Urological Cancers: A Mini-Review - PMC', type='url_citation', url='https://pmc.ncbi.nlm.nih.gov/articles/PMC12071082/#:~:text=,from%20general%20mechanisms%20and%20other')