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Article: Modulating TRPV4 Channel Activity in Pro-Inflammatory Macrophages within the 3D Tissue Analog.

Babaniamansour, Parto / Jacho, Diego / Niedzielski, Skyler / Rabino, Agustin / Garcia-Mata, Rafael / Yildirim-Ayan, Eda

2024 Volume 12, Issue 1

Abstract: Investigating macrophage plasticity emerges as a promising strategy for promoting tissue regeneration and can be exploited by regulating the transient receptor potential vanilloid 4 (TRPV4) channel. The TRPV4 channel responds to various stimuli including ...

Abstract	Investigating macrophage plasticity emerges as a promising strategy for promoting tissue regeneration and can be exploited by regulating the transient receptor potential vanilloid 4 (TRPV4) channel. The TRPV4 channel responds to various stimuli including mechanical, chemical, and selective pharmacological compounds. It is well documented that treating cells such as epithelial cells and fibroblasts with a TRPV4 agonist enhances the Ca
Language	English
Publishing date	2024-01-19
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2720867-9
ISSN	2227-9059
ISSN	2227-9059
DOI	10.3390/biomedicines12010230
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: The Scribble/SGEF/Dlg1 complex regulates the stability of apical junctions in epithelial cells.

Rabino, Agustin / Awadia, Sahezeel / Ali, Nabaa / Edson, Amber / Garcia-Mata, Rafael

bioRxiv : the preprint server for biology

2024

Abstract: SGEF, a RhoG specific GEF, can form a ternary complex with the Scribble polarity complex proteins Scribble and Dlg1, which regulates the formation and maintenance of adherens junctions and barrier function of epithelial cells. Notably, silencing SGEF ... ...

Abstract	SGEF, a RhoG specific GEF, can form a ternary complex with the Scribble polarity complex proteins Scribble and Dlg1, which regulates the formation and maintenance of adherens junctions and barrier function of epithelial cells. Notably, silencing SGEF results in a dramatic downregulation of the expression of both E-cadherin and ZO-1. However, the molecular mechanisms involved in the regulation of this pathway are not known. Here, we describe a novel signaling pathway governed by the Scribble/SGEF/Dlg1 complex. Our results show that an intact ternary complex is required to maintain the stability of the apical junctions, the expression of ZO-1, and TJ permeability. In contrast, only SGEF is necessary to regulate E-cadherin expression. The absence of SGEF destabilizes the E-cadherin/catenin complex at the membrane, triggering a positive feedback loop that exacerbates the phenotype through the repression of E-cadherin transcription in a process that involves the internalization of E-cadherin by endocytosis, β-catenin signaling and the transcriptional repressor Slug.
Language	English
Publishing date	2024-03-27
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.26.586884
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Article ; Online: Nonredundant Rac-GEF control of actin cytoskeleton reorganization.

Kazanietz, Marcelo G / Cooke, Mariana / Garcia-Mata, Rafael

Trends in cell biology

2022 Volume 32, Issue 10, Page(s) 815–818

Abstract: Rac-GEFs operate in a nonredundant manner as downstream effectors of receptor tyrosine kinases to promote ruffle formation, indicative of unique modes of regulation and targeting. Current research is shedding light on the intricate signaling paradigms ... ...

Abstract	Rac-GEFs operate in a nonredundant manner as downstream effectors of receptor tyrosine kinases to promote ruffle formation, indicative of unique modes of regulation and targeting. Current research is shedding light on the intricate signaling paradigms shaping spatiotemporal activation of the small GTPase Rac during the generation of actin-rich membrane protrusions.
MeSH term(s)	Actin Cytoskeleton/metabolism ; Actins/metabolism ; Humans ; Signal Transduction
Chemical Substances	Actins
Language	English
Publishing date	2022-06-23
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	30122-x
ISSN	1879-3088 ; 0962-8924
ISSN (online)	1879-3088
ISSN	0962-8924
DOI	10.1016/j.tcb.2022.06.003
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Article ; Online: Cell-based optimization and characterization of genetically encoded location-based biosensors for Cdc42 or Rac activity.

Mahlandt, Eike K / Kreider-Letterman, Gabriel / Chertkova, Anna O / Garcia-Mata, Rafael / Goedhart, Joachim

Journal of cell science

2023 Volume 136, Issue 10

Abstract: Rac (herein referring to the Rac family) and Cdc42 are Rho GTPases that regulate the formation of lamellipoda and filopodia, and are therefore crucial in processes such as cell migration. Relocation-based biosensors for Rac and Cdc42 have not been ... ...

Abstract	Rac (herein referring to the Rac family) and Cdc42 are Rho GTPases that regulate the formation of lamellipoda and filopodia, and are therefore crucial in processes such as cell migration. Relocation-based biosensors for Rac and Cdc42 have not been characterized well in terms of their specificity or affinity. In this study, we identify relocation sensor candidates for both Rac and Cdc42. We compared their (1) ability to bind the constitutively active Rho GTPases, (2) specificity for Rac and Cdc42, and (3) relocation efficiency in cell-based assays. Subsequently, the relocation efficiency was improved by a multi-domain approach. For Rac1, we found a sensor candidate with low relocation efficiency. For Cdc42, we found several sensors with sufficient relocation efficiency and specificity. These optimized sensors enable the wider application of Rho GTPase relocation sensors, which was showcased by the detection of local endogenous Cdc42 activity at assembling invadopodia. Moreover, we tested several fluorescent proteins and HaloTag for their influence on the recruitment efficiency of the Rho location sensor, to find optimal conditions for a multiplexing experiment. This characterization and optimization of relocation sensors will broaden their application and acceptance.
MeSH term(s)	rho GTP-Binding Proteins ; Cell Movement ; Podosomes ; Pseudopodia
Chemical Substances	rho GTP-Binding Proteins (EC 3.6.5.2)
Language	English
Publishing date	2023-05-25
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2993-2
ISSN	1477-9137 ; 0021-9533
ISSN (online)	1477-9137
ISSN	0021-9533
DOI	10.1242/jcs.260802
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Zs.MG 14: Show issues

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Article ; Online: Macrophage Mechano-Responsiveness Within Three-Dimensional Tissue Matrix upon Mechanotherapy-Associated Strains.

Babaniamansour, Parto / Jacho, Diego / Teow, Ashley / Rabino, Agustin / Garcia-Mata, Rafael / Yildirim-Ayan, Eda

Tissue engineering. Part A

2023 Volume 30, Issue 7-8, Page(s) 314–329

Abstract: Mechano-rehabilitation, also known as mechanotherapy, represents the forefront of noninvasive treatment for musculoskeletal (MSK) tissue disorders, encompassing conditions affecting tendons, cartilage, ligaments, and muscles. Recent emphasis has ... ...

Abstract	Mechano-rehabilitation, also known as mechanotherapy, represents the forefront of noninvasive treatment for musculoskeletal (MSK) tissue disorders, encompassing conditions affecting tendons, cartilage, ligaments, and muscles. Recent emphasis has underscored the significance of macrophage presence in the healing of MSK tissues. However, a considerable gap still exists in comprehending how mechanical strains associated with mechanotherapy impact both the naïve and pro-inflammatory macrophage phenotypes within the three-dimensional (3D) tissue matrix, as well as whether the shift in macrophage phenotype is contingent on the mechanical strains inherent to mechanotherapy. In this study, we delineated alterations in mechano-adaptation and polarization of both naive and M1 macrophages within 3D matrices, elucidating their response to varying degrees of mechanical strain exposure (3%, 6%, and 12%). To evaluate macrophage mechano-adaptation and mechano-sensitivity within 3D collagen matrices under mechanical loading, we employed structural techniques (scanning electron microscopy, histology), quantitative morphological measures for phenotypic assessment, and genotypic methods such as quantitative real-time polymerase chain reaction. Our data reveal that the response of macrophages to mechanical loading is not only contingent on their specific sub-phenotype but also varies with the amplitude of mechanical strain. Notably, although supra-mechanical loading (12% strain) was requisite to induce a phenotypic shift in naive (M0) macrophages, as little as 3% mechanical strain proved sufficient to prompt phenotypic alterations in pro-inflammatory (M1) macrophages. These findings pave the way for leveraging the macrophage mechanome in customized and targeted applications of mechanical strain within the mechano-therapeutic framework. Considering the prevalence of MSK tissue injuries and their profound societal and economic implications, the development of well-informed and effective clinical mechanotherapy modalities for MSK tissue healing becomes an imperative endeavor. Impact statement Mechanotherapy is a primary noninvasive treatment for musculoskeletal (MSK) tissue injuries, but the effect of mechanical strain on macrophage phenotypes is not fully understood. A recent study found that macrophage response to mechanical loading is both sub-phenotype specific and amplitude-dependent, with even small strains enough to induce phenotypic changes in pro-inflammatory macrophages. These findings could pave the way for using macrophage mechanome in targeted mechanotherapy applications for better MSK tissue healing.
MeSH term(s)	Macrophages ; Wound Healing ; Collagen/pharmacology ; Phenotype ; Musculoskeletal System
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2023-10-27
Publishing country	United States
Document type	Journal Article
ZDB-ID	2420582-5
ISSN	1937-335X ; 1937-3341
ISSN (online)	1937-335X
ISSN	1937-3341
DOI	10.1089/ten.TEA.2023.0110
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Article ; Online: Mechanoresponsive regulation of fibroblast-to-myofibroblast transition in three-dimensional tissue analogues: mechanical strain amplitude dependency of fibrosis.

Jacho, Diego / Rabino, Agustin / Garcia-Mata, Rafael / Yildirim-Ayan, Eda

Scientific reports

2022 Volume 12, Issue 1, Page(s) 16832

Abstract: The spatiotemporal interaction and constant iterative feedback between fibroblasts, extracellular matrix, and environmental cues are central for investigating the fibroblast-induced musculoskeletal tissue regeneration and fibroblast-to-myofibroblast ... ...

Abstract	The spatiotemporal interaction and constant iterative feedback between fibroblasts, extracellular matrix, and environmental cues are central for investigating the fibroblast-induced musculoskeletal tissue regeneration and fibroblast-to-myofibroblast transition (FMT). In this study, we created a fibroblast-laden 3D tissue analogue to study (1) how mechanical loading exerted on three-dimensional (3D) tissues affected the residing fibroblast phenotype and (2) to identify the ideal mechanical strain amplitude for promoting tissue regeneration without initiating myofibroblast differentiation. We applied uniaxial tensile strain (0, 4, 8, and 12%) to the cell-laden 3D tissue analogues to understand the interrelation between the degree of applied mechanical loading amplitudes and FMT. Our data demonstrated that 4% mechanical strain created an anabolic effect toward tissue regeneration, but higher strain amplitudes over-stimulated the cells and initiated fibrotic tissue formation. Under increased mechanical strain amplitudes, fibroblasts were activated from a homeostatic state to a proto-myofibroblast state which resulted in increased cellularity accompanied by increased expressions of extracellular matrix (ECM) components, activation stressors (TGF-β1 and TGF-βR1), and profibrotic markers. This further transformed fibroblasts into α-smooth muscle actin expressing myofibroblasts. Understanding the interplay between the applied degree of mechanical loading exerted on 3D tissues and residing fibroblast phenotypic response is important to identify specific mechanomodulatory approaches for tissue regeneration and the informed mechanotherapy-guided tissue healing strategies.
MeSH term(s)	Actins/metabolism ; Anabolic Agents/pharmacology ; Cell Differentiation/physiology ; Cells, Cultured ; Fibroblasts/metabolism ; Fibrosis ; Humans ; Myofibroblasts/metabolism ; Transforming Growth Factor beta1/metabolism
Chemical Substances	Actins ; Anabolic Agents ; Transforming Growth Factor beta1
Language	English
Publishing date	2022-10-07
Publishing country	England
Document type	Journal Article
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-022-20383-5
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Article ; Online: Fixing the GAP: The role of RhoGAPs in cancer.

Kreider-Letterman, Gabriel / Carr, Nicole M / Garcia-Mata, Rafael

European journal of cell biology

2022 Volume 101, Issue 2, Page(s) 151209

Abstract: Cancer progression and metastasis are processes that involve significant cellular changes. Many of these changes include alterations in the activity of the Rho GTPase family of proteins. Rho GTPases are signaling proteins that function as molecular ... ...

Abstract	Cancer progression and metastasis are processes that involve significant cellular changes. Many of these changes include alterations in the activity of the Rho GTPase family of proteins. Rho GTPases are signaling proteins that function as molecular switches and are involved in the regulation of most major cellular processes. Cancer development is often associated with abnormalities in Rho GTPase signaling. Rho GTPase signaling is regulated by two families of proteins, guanine nucleotide-exchange factors (RhoGEFs) and GTPase activating proteins (RhoGAPs), that function upstream of the Rho proteins to regulate their activation and inactivation, respectively. While initial work has focused on the role of RhoGEFs in cancer, the RhoGAP family members are rapidly being established as key regulators of cancer development and progression. The aim of this review is to summarize our advances in understanding the role of RhoGAPs in cancer and to discuss their significance in the development of therapeutics.
MeSH term(s)	GTPase-Activating Proteins/genetics ; GTPase-Activating Proteins/metabolism ; Guanine Nucleotide Exchange Factors/metabolism ; Humans ; Neoplasms/metabolism ; rho GTP-Binding Proteins/metabolism
Chemical Substances	GTPase-Activating Proteins ; Guanine Nucleotide Exchange Factors ; rho GTPase-activating protein ; rho GTP-Binding Proteins (EC 3.6.5.2)
Language	English
Publishing date	2022-02-10
Publishing country	Germany
Document type	Journal Article ; Review
ZDB-ID	391967-5
ISSN	1618-1298 ; 0070-2463 ; 0171-9335
ISSN (online)	1618-1298
ISSN	0070-2463 ; 0171-9335
DOI	10.1016/j.ejcb.2022.151209
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ab Jg. 2022: Lesesaal (EG)

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Article ; Online: Quantification of ruffle area and dynamics in live or fixed lung adenocarcinoma cells.

Kreider-Letterman, Gabriel / Cooke, Mariana / Goicoechea, Silvia M / Kazanietz, Marcelo G / Garcia-Mata, Rafael

STAR protocols

2022 Volume 3, Issue 2, Page(s) 101437

Abstract: Ruffles are actin-rich membrane protrusions implicated in actin reorganization and initiation of cell motility. Here, we describe methods for measuring and analyzing ruffle dynamics in live cells and average ruffle area per cell in fixed samples. The ... ...

Abstract	Ruffles are actin-rich membrane protrusions implicated in actin reorganization and initiation of cell motility. Here, we describe methods for measuring and analyzing ruffle dynamics in live cells and average ruffle area per cell in fixed samples. The specific steps described are for the analysis of A549 lung adenocarcinoma cells, but the protocol can be applied to other cell types. The protocol has applications for dissecting the signaling events linked to ruffling. For complete details on the use and execution of this protocol, please refer to Cooke et al. (2021).
MeSH term(s)	Actins/metabolism ; Adenocarcinoma of Lung/metabolism ; Cell Membrane Structures/metabolism ; Cell Movement ; Humans
Chemical Substances	Actins
Language	English
Publishing date	2022-06-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	2666-1667
ISSN (online)	2666-1667
DOI	10.1016/j.xpro.2022.101437
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Article: A PACAP-activated network for secretion requires coordination of Ca

Chen, Xiaohuan / Bell, Nicole A / Coffman, Breanna L / Rabino, Agustin A / Garcia-Mata, Rafael / Kammermeier, Paul J / Yule, David I / Axelrod, Daniel / Smrcka, Alan V / Giovannucci, David R / Anantharam, Arun

bioRxiv : the preprint server for biology

2024

Abstract: Chromaffin cells of the adrenal medulla transduce sympathetic nerve activity into stress hormone secretion. The two neurotransmitters principally responsible for coupling cell stimulation to secretion are acetylcholine and pituitary adenylate activating ... ...

Abstract	Chromaffin cells of the adrenal medulla transduce sympathetic nerve activity into stress hormone secretion. The two neurotransmitters principally responsible for coupling cell stimulation to secretion are acetylcholine and pituitary adenylate activating polypeptide (PACAP). In contrast to acetylcholine, PACAP evokes a persistent secretory response from chromaffin cells. However, the mechanisms by which PACAP acts are poorly understood. Here, it is shown that PACAP induces sustained increases in cytosolic Ca
Language	English
Publishing date	2024-01-03
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.01.03.574069
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Article ; Online: Deciphering the Cell-Specific Effect of Osteoblast-Macrophage Crosstalk in Periodontitis.

Jacho, Diego / Babaniamansour, Parto / Osorio, Raquel / Toledano, Manuel / Rabino, Agustín / Garcia-Mata, Rafael / Yildirim-Ayan, Eda

Tissue engineering. Part A

2023 Volume 29, Issue 21-22, Page(s) 579–593

Abstract: In periodontitis, the bone remodeling process is disrupted by the prevalent involvement of bacteria-induced proinflammatory macrophage cells and their interaction with osteoblast cells residing within the infected bone tissue. The complex interaction ... ...

Abstract	In periodontitis, the bone remodeling process is disrupted by the prevalent involvement of bacteria-induced proinflammatory macrophage cells and their interaction with osteoblast cells residing within the infected bone tissue. The complex interaction between the cells needs to be deciphered to understand the dominant player in tipping the balance from osteogenesis to osteoclastogenesis. Yet, only a few studies have examined the crosstalk interaction between osteoblasts and macrophages using biomimetic three-dimensional (3D) tissue-like matrices. In this study, we created a cell-laden 3D tissue analog to study indirect crosstalk between these two cell types and their direct synergistic effect when cultured on a 3D scaffold. The cell-specific role of osteoclast differentiation was investigated through osteoblast- and proinflammatory macrophage-specific feedback studies. The results suggested that when macrophages were exposed to osteoblasts-derived conditioned media from the mineralized matrix, the M1 macrophages tended to maintain their proinflammatory phenotype. Further, when osteoblasts were exposed to secretions from proinflammatory macrophages, they demonstrated elevated receptor activator of nuclear factor-κB ligand (RANKL) expression and decreased alkaline phosphate (ALP) activities compared to osteoblasts exposed to only osteogenic media. In addition, the upregulation of tumor necrosis factor-alpha (TNF-α) and c-Fos in proinflammatory macrophages within the 3D matrix indirectly increased the RANKL expression and reduced the ALP activity of osteoblasts, promoting osteoclastogenesis. The contact coculturing with osteoblast and proinflammatory macrophages within the 3D matrix demonstrated that the proinflammatory markers (TNF-α and interleukin-1β) expressions were upregulated. In contrast, anti-inflammatory markers (c-c motif chemokine ligand 18 [CCL18]) were downregulated, and osteoclastogenic markers (TNF receptor associated factor 6 [TRAF6] and acid phosphatase 5, tartrate resistant [ACP5]) were unchanged. The data suggested that the osteoblasts curbed the osteoclastogenic differentiation of macrophages while macrophages still preserved their proinflammatory lineages. The osteoblast within the 3D coculture demonstrated increased ALP activity and did not express RANKL significantly different than the osteoblast cultured within a 3D collagen matrix without macrophages. Contact coculturing has an anabolic effect on bone tissue in a bacteria-derived inflammatory environment.
MeSH term(s)	Humans ; Osteoclasts ; Tumor Necrosis Factor-alpha/pharmacology ; Osteoblasts/metabolism ; Macrophages/metabolism ; Osteogenesis ; Cell Differentiation ; Periodontitis/metabolism ; RANK Ligand/metabolism ; RANK Ligand/pharmacology
Chemical Substances	Tumor Necrosis Factor-alpha ; RANK Ligand
Language	English
Publishing date	2023-10-06
Publishing country	United States
Document type	Journal Article
ZDB-ID	2420582-5
ISSN	1937-335X ; 1937-3341
ISSN (online)	1937-335X
ISSN	1937-3341
DOI	10.1089/ten.TEA.2023.0104
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ab Jg. 2022: Lesesaal (EG)

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