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Article ; Online: Large Rab GTPases: Novel Membrane Trafficking Regulators with a Calcium Sensor and Functional Domains.

Tsukuba, Takayuki / Yamaguchi, Yu / Kadowaki, Tomoko

International journal of molecular sciences

2021 Volume 22, Issue 14

Abstract: Rab GTPases are major coordinators of intracellular membrane trafficking, including vesicle transport, membrane fission, tethering, docking, and fusion events. Rab GTPases are roughly divided into two groups: conventional "small" Rab GTPases and atypical ...

Abstract	Rab GTPases are major coordinators of intracellular membrane trafficking, including vesicle transport, membrane fission, tethering, docking, and fusion events. Rab GTPases are roughly divided into two groups: conventional "small" Rab GTPases and atypical "large" Rab GTPases that have been recently reported. Some members of large Rab GTPases in mammals include Rab44, Rab45/RASEF, and Rab46. The genes of these large Rab GTPases commonly encode an amino-terminal EF-hand domain, coiled-coil domain, and the carboxyl-terminal Rab GTPase domain. A common feature of large Rab GTPases is that they express several isoforms in cells. For instance, Rab44's two isoforms have similar functions, but exhibit differential localization. The long form of Rab45 (Rab45-L) is abundantly distributed in epithelial cells. The short form of Rab45 (Rab45-S) is predominantly present in the testes. Both Rab46 (CRACR2A-L) and the short isoform lacking the Rab domain (CRACR2A-S) are expressed in T cells, whereas Rab46 is only distributed in endothelial cells. Although evidence regarding the function of large Rab GTPases has been accumulating recently, there are only a limited number of studies. Here, we report the recent findings on the large Rab GTPase family concerning their function in membrane trafficking, cell differentiation, related diseases, and knockout mouse phenotypes.
MeSH term(s)	Amino Acid Sequence ; Animals ; Calcium/metabolism ; Female ; Gene Knockout Techniques ; Humans ; Intracellular Membranes/metabolism ; Male ; Mast Cells/metabolism ; Membrane Transport Proteins/chemistry ; Membrane Transport Proteins/genetics ; Membrane Transport Proteins/metabolism ; Mice ; Osteoclasts/cytology ; Osteoclasts/metabolism ; Phenotype ; Protein Domains ; T-Lymphocytes/metabolism ; rab GTP-Binding Proteins/chemistry ; rab GTP-Binding Proteins/genetics ; rab GTP-Binding Proteins/metabolism
Chemical Substances	Membrane Transport Proteins ; rab GTP-Binding Proteins (EC 3.6.5.2) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2021-07-19
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms22147691
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Article ; Online: Liquid-phase ASEM imaging of cellular and structural details in cartilage and bone formed during endochondral ossification: Keap1-deficient osteomalacia.

Sakai, Eiko / Sato, Mari / Memtily, Nassirhadjy / Tsukuba, Takayuki / Sato, Chikara

Scientific reports

2021 Volume 11, Issue 1, Page(s) 5722

Abstract: Chondrogenesis and angiogenesis drive endochondral ossification. Using the atmospheric scanning electron microscopy (ASEM) without decalcification and dehydration, we directly imaged angiogenesis-driven ossification at different developmental stages ... ...

Abstract	Chondrogenesis and angiogenesis drive endochondral ossification. Using the atmospheric scanning electron microscopy (ASEM) without decalcification and dehydration, we directly imaged angiogenesis-driven ossification at different developmental stages shortly after aldehyde fixation, using aqueous radical scavenger glucose solution to preserve water-rich structures. An embryonic day 15.5 mouse femur was fixed and stained with phosphotungstic acid (PTA), and blood vessel penetration into the hypertrophic chondrocyte zone was visualised. We observed a novel envelope between the perichondrium and proliferating chondrocytes, which was lined with spindle-shaped cells that could be borderline chondrocytes. At postnatal day (P)1, trabecular and cortical bone mineralisation was imaged without staining. Additional PTA staining visualised surrounding soft tissues; filamentous connections between osteoblast-like cells and osteocytes in cortical bone were interpreted as the osteocytic lacunar-canalicular system. By P10, resorption pits had formed on the tibial trabecular bone surface. The applicability of ASEM for pathological analysis was addressed using knockout mice of Keap1, an oxidative-stress sensor. In Keap1
MeSH term(s)	Animals ; Atmosphere ; Bone and Bones/diagnostic imaging ; Bone and Bones/pathology ; Bone and Bones/ultrastructure ; Calcification, Physiologic ; Cartilage/diagnostic imaging ; Cartilage/pathology ; Cartilage/ultrastructure ; Chondrogenesis ; Cortical Bone/diagnostic imaging ; Cortical Bone/ultrastructure ; Embryo, Mammalian/diagnostic imaging ; Femur/diagnostic imaging ; Femur/ultrastructure ; Imaging, Three-Dimensional ; Kelch-Like ECH-Associated Protein 1/deficiency ; Kelch-Like ECH-Associated Protein 1/metabolism ; Mice, Inbred C57BL ; Microscopy, Electron, Scanning ; Osteocytes/metabolism ; Osteogenesis ; Osteomalacia/pathology ; Phenotype ; Tibia/diagnostic imaging ; Tibia/ultrastructure ; Mice
Chemical Substances	Kelch-Like ECH-Associated Protein 1
Language	English
Publishing date	2021-03-11
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-021-84202-z
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Article ; Online: Coronin1C Is a GDP-Specific Rab44 Effector That Controls Osteoclast Formation by Regulating Cell Motility in Macrophages.

Yamaguchi, Yu / Kadowaki, Tomoko / Aibara, Nozomi / Ohyama, Kaname / Okamoto, Kuniaki / Sakai, Eiko / Tsukuba, Takayuki

International journal of molecular sciences

2022 Volume 23, Issue 12

Abstract: Osteoclasts are multinucleated bone-resorbing cells that are formed by the fusion of macrophages. Recently, we ... ...

Abstract	Osteoclasts are multinucleated bone-resorbing cells that are formed by the fusion of macrophages. Recently, we identified
MeSH term(s)	Animals ; Bone Resorption/metabolism ; Cell Differentiation/genetics ; Cell Movement ; Macrophages/metabolism ; Mice ; Microfilament Proteins/genetics ; Microfilament Proteins/metabolism ; Osteoclasts/metabolism ; Osteogenesis/genetics ; RANK Ligand/metabolism ; rab GTP-Binding Proteins/metabolism
Chemical Substances	Microfilament Proteins ; RANK Ligand ; Rab44 protein, mouse (EC 3.6.5.2) ; rab GTP-Binding Proteins (EC 3.6.5.2)
Language	English
Publishing date	2022-06-14
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms23126619
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Article ; Online: Transposon mutagenesis and genome sequencing identify two novel, tandem genes involved in the colony spreading of

Kondo, Yoshio / Ohara, Kenichi / Fujii, Ryoji / Nakai, Yudai / Sato, Chikara / Naito, Mariko / Tsukuba, Takayuki / Kadowaki, Tomoko / Sato, Keiko

Frontiers in cellular and infection microbiology

2023 Volume 13, Page(s) 1095919

Abstract: Bacteria of the ... ...

Abstract	Bacteria of the family
MeSH term(s)	Animals ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Osmeriformes/genetics ; Osmeriformes/metabolism ; Flavobacterium/genetics ; Mutagenesis ; Bacteroidetes ; Fish Diseases/microbiology
Chemical Substances	Bacterial Proteins
Language	English
Publishing date	2023-02-10
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2619676-1
ISSN	2235-2988 ; 2235-2988
ISSN (online)	2235-2988
ISSN	2235-2988
DOI	10.3389/fcimb.2023.1095919
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Article ; Online: Rab44 Deficiency Induces Impaired Immune Responses to Nickel Allergy.

Noguromi, Mayuko / Yamaguchi, Yu / Sato, Keiko / Oyakawa, Shun / Okamoto, Kuniaki / Murata, Hiroshi / Tsukuba, Takayuki / Kadowaki, Tomoko

International journal of molecular sciences

2023 Volume 24, Issue 2

Abstract: Rab44 was recently identified as an atypical Rab GTPase that possesses EF-hand and coiled-coil domains at the N-terminus, and a Rab-GTPase domain at the C-terminus. Rab44 is highly expressed in immune-related cells such as mast cells, macrophages, ... ...

Abstract	Rab44 was recently identified as an atypical Rab GTPase that possesses EF-hand and coiled-coil domains at the N-terminus, and a Rab-GTPase domain at the C-terminus. Rab44 is highly expressed in immune-related cells such as mast cells, macrophages, osteoclasts, and granulocyte-lineage cells in the bone marrow. Therefore, it is speculated that Rab44 is involved in the inflammation and differentiation of immune cells. However, little is known about the role of Rab44 in inflammation. In this study, we showed that Rab44 was upregulated during the early phase of differentiation of M1- and M2-type macrophages. Rab44-deficient mice exhibited impaired tumor necrosis factor alpha and interleukin-10 production after lipopolysaccharide (LPS) stimulation. The number of granulocytes in Rab44-deficient mice was lower, but the lymphocyte count in Rab44-deficient mice was significantly higher than that in wild-type mice after LPS stimulation. Moreover, Rab44-deficient macrophages showed impaired nickel-induced toxicity, and Rab44-deficient mice showed impaired nickel-induced hypersensitivity. Upon nickel hypersensitivity induction, Rab44-deficient mice showed different frequencies of immune cells in the blood and ears. Thus, it is likely that Rab44 is implicated in immune cell differentiation and inflammation, and Rab44 deficiency induces impaired immune responses to nickel allergies.
MeSH term(s)	Mice ; Animals ; Nickel/toxicity ; Lipopolysaccharides/toxicity ; Hypersensitivity/genetics ; rab GTP-Binding Proteins/genetics ; rab GTP-Binding Proteins/metabolism ; Inflammation ; Immunity
Chemical Substances	Nickel (7OV03QG267) ; Lipopolysaccharides ; rab GTP-Binding Proteins (EC 3.6.5.2)
Language	English
Publishing date	2023-01-04
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms24020994
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Article ; Online: Rab44 deficiency accelerates recovery from muscle damage by regulating mTORC1 signaling and transport of fusogenic regulators.

Oyakawa, Shun / Yamaguchi, Yu / Kadowaki, Tomoko / Sakai, Eiko / Noguromi, Mayuko / Tanimoto, Ayuko / Ono, Yusuke / Murata, Hiroshi / Tsukuba, Takayuki

Journal of cellular physiology

2023 Volume 238, Issue 10, Page(s) 2253–2266

Abstract: The skeletal muscle is a tissue that shows remarkable plasticity to adapt to various stimuli. The development and regeneration of skeletal muscles are regulated by numerous molecules. Among these, we focused on Rab44, a large Rab GTPase, that has been ... ...

Abstract	The skeletal muscle is a tissue that shows remarkable plasticity to adapt to various stimuli. The development and regeneration of skeletal muscles are regulated by numerous molecules. Among these, we focused on Rab44, a large Rab GTPase, that has been recently identified in immune cells and osteoclasts. Recently, bioinformatics data has revealed that Rab44 is upregulated during the myogenic differentiation of myoblasts into myotubes in C2C12 cells. Thus, Rab44 may be involved in myogenesis. Here, we have investigated the effects of Rab44 deficiency on the development and regeneration of skeletal muscle in Rab44 knockout (KO) mice. Although KO mice exhibited body and muscle weights similar to those of wild-type (WT) mice, the histochemical analysis showed that the myofiber cross-sectional area (CSA) of KO mice was significantly smaller than that of WT mice. Importantly, the results of muscle regeneration experiments using cardiotoxin revealed that the CSA of KO mice was significantly larger than that of WT mice, suggesting that Rab44 deficiency promotes muscle regeneration. Consistent with the in vivo results, in vitro experiments indicated that satellite cells derived from KO mice displayed enhanced proliferation and differentiation. Mechanistically, KO satellite cells exhibited an increased mechanistic target of rapamycin complex 1 (mTORC1) signaling compared to WT cells. Additionally, enhanced cell surface transport of myomaker and myomixer, which are essential membrane proteins for myoblast fusion, was observed in KO satellite cells compared to WT cells. Therefore, Rab44 deficiency enhances muscle regeneration by modulating the mTORC1 signaling pathway and transport of fusogenic regulators.
Language	English
Publishing date	2023-08-10
Publishing country	United States
Document type	Journal Article
ZDB-ID	3116-1
ISSN	1097-4652 ; 0021-9541
ISSN (online)	1097-4652
ISSN	0021-9541
DOI	10.1002/jcp.31082
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Article ; Online: Abr, a Rho-regulating protein, modulates osteoclastogenesis by enhancing lamellipodia formation by interacting with poly(ADP-ribose) glycohydrolase.

Farhana, Fatima / Sakai, Eiko / Koyanagi, Yu / Yamaguchi, Yu / Alam, Mohammad Ibtehaz / Okamoto, Kuniaki / Tsukuba, Takayuki

Molecular biology reports

2023 Volume 50, Issue 9, Page(s) 7557–7569

Abstract: Background: Osteoclasts are multinucleated bone-resorbing cells formed by the fusion of monocyte/macrophage lineage. During osteoclast differentiation, Rho GTPases are involved in various processes, including cell migration, adhesion, and polarity. ... ...

Abstract	Background: Osteoclasts are multinucleated bone-resorbing cells formed by the fusion of monocyte/macrophage lineage. During osteoclast differentiation, Rho GTPases are involved in various processes, including cell migration, adhesion, and polarity. However, the role of Rho-regulatory molecules in the regulation of osteoclast differentiation remains unclear. In this study, among these genes, we focused on active breakpoint cluster region-related (Abr) protein that is a multifunctional regulator of Rho GTPases. Methods and results: We examined using knockdown and overexpression experiments in RANKL-stimulated RAW-D macrophages whether Abr regulates osteoclast differentiation and cell morphology. We observed an increase in Abr expression during osteoclast differentiation and identified expression of a variant of the Abr gene in osteoclasts. Knockdown of Abr suppressed osteoclast differentiation and resorption. Abr knockdown markedly inhibited the expression of osteoclast markers, such as Nfatc1, c-fos, Src, and Ctsk in osteoclasts. Conversely, overexpression of Abr enhanced the formation of multinucleated osteoclasts, bone resorption activity, and osteoclast marker gene expression. Moreover, Abr overexpression accelerated lamellipodia formation and induced the formation of well-developed actin in osteoclasts. Importantly, the Abr protein interacted with poly(ADP-ribose) glycohydrolase (PARG) and Rho GTPases, including RhoA, Rac1/2/3, and Cdc42 in osteoclasts. Conclusions: Taken together, these results indicate that Abr modulates osteoclastogenesis by enhancing lamellipodia formation via its interaction with PARG.
MeSH term(s)	Cell Differentiation/genetics ; NFATC Transcription Factors/metabolism ; Osteoclasts/metabolism ; Osteogenesis/genetics ; Pseudopodia/metabolism ; rho GTP-Binding Proteins/genetics ; rho GTP-Binding Proteins/metabolism
Chemical Substances	NFATC Transcription Factors ; poly ADP-ribose glycohydrolase (EC 3.2.1.143) ; rho GTP-Binding Proteins (EC 3.6.5.2) ; Abr protein, mouse
Language	English
Publishing date	2023-07-28
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	186544-4
ISSN	1573-4978 ; 0301-4851
ISSN (online)	1573-4978
ISSN	0301-4851
DOI	10.1007/s11033-023-08690-0
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Article ; Online: Rab44 negatively regulates myoblast differentiation by controlling fusogenic protein transport and mTORC1 signaling.

Tanimoto, Ayuko / Yamaguchi, Yu / Kadowaki, Tomoko / Sakai, Eiko / Oyakawa, Shun / Ono, Yusuke / Yoshida, Noriaki / Tsukuba, Takayuki

Journal of cellular biochemistry

2023 Volume 124, Issue 10, Page(s) 1486–1502

Abstract: Skeletal muscle is composed of multinucleated myotubes formed by the fusion of mononucleated myoblasts. Skeletal muscle differentiation, termed as myogenesis, have been investigated using the mouse skeletal myoblast cell line C2C12. It has been reported ... ...

Abstract	Skeletal muscle is composed of multinucleated myotubes formed by the fusion of mononucleated myoblasts. Skeletal muscle differentiation, termed as myogenesis, have been investigated using the mouse skeletal myoblast cell line C2C12. It has been reported that several "small" Rab proteins, major membrane-trafficking regulators, possibly regulate membrane protein transport in C2C12 cells; however, the role of Rab proteins in myogenesis remains unexplored. Rab44, a member of "large" Rab GTPases, has recently been identified as a negative regulator of osteoclast differentiation. In this study, using C2C12 cells, we found that Rab44 expression was upregulated during myoblast differentiation into myotubes. Knockdown of Rab44 enhanced myoblast differentiation and myotube formation. Consistent with these results, Rab44 knockdown in myoblasts increased expression levels of several myogenic marker genes. Rab44 knockdown increased the surface accumulation of myomaker and myomixer, two fusogenic proteins required for multinucleation, implying enhanced cell fusion. Conversely, Rab44 overexpression inhibited myoblast differentiation and tube formation, accompanied by decreased expression of some myogenic markers. Furthermore, Rab44 was found to be predominantly localized in lysosomes, and Rab44 overexpression altered the number and size of lysosomes. Considering the underlying molecular mechanism, Rab44 overexpression impaired the signaling pathway of the mechanistic target of rapamycin complex1 (mTORC1) in C2C12 cells. Namely, phosphorylation levels of mTORC1 and downstream mTORC1 substrates, such as S6 and P70-S6K, were notably lower in Rab44 overexpressing cells than those in control cells. These results indicate that Rab44 negatively regulates myoblast differentiation into myotubes by controlling fusogenic protein transport and mTORC1 signaling.
Language	English
Publishing date	2023-08-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	392402-6
ISSN	1097-4644 ; 0730-2312
ISSN (online)	1097-4644
ISSN	0730-2312
DOI	10.1002/jcb.30457
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Article: Rab44 isoforms similarly promote lysosomal exocytosis, but exhibit differential localization in mast cells

Kadowaki, Tomoko / Yamaguchi, Yu / Ogawa, Kohei / Tokuhisa, Mitsuko / Okamoto, Kuniaki / Tsukuba, Takayuki

FEBS Open Bio. 2021 Apr., v. 11, no. 4

2021

Abstract: Rab44 is a large Rab GTPase containing a Rab GTPase domain and some additional N‐terminal domains. We recently used Rab44‐deficient mice to demonstrate that Rab44 regulates granule exocytosis in mast cells and IgE‐mediated anaphylaxis. In mouse mast ... ...

Abstract	Rab44 is a large Rab GTPase containing a Rab GTPase domain and some additional N‐terminal domains. We recently used Rab44‐deficient mice to demonstrate that Rab44 regulates granule exocytosis in mast cells and IgE‐mediated anaphylaxis. In mouse mast cells, Rab44 is expressed as two isoforms, namely, the long and short forms; however, the characteristics of these two isoforms remain unknown. Here, we investigated secretion and localization of the human long Rab44 isoform and the two mouse isoforms and their mutants expressed in rat basophilic leukemia (RBL)‐2H3 cells. Expression of the human long isoform and both mouse isoforms caused an increase in β‐hexosaminidase secretion. Confocal and quantitative analyses showed that both human and mouse long isoforms localized mainly to lysosomes while the mouse short isoform localized mainly to the ER. Live imaging with LysoTracker indicated that the size and number of LysoTracker‐positive vesicles were altered by the various mutants. Ionomycin treatment partially altered localization of both long isoforms to the plasma membrane and cytosol, whereas it had little effect on colocalization of the short isoform with lysosomes. Mechanistically, both human and mouse Rab44 proteins interacted with vesicle‐associated membrane protein 8 (VAMP8), a v‐SNARE protein. Therefore, Rab44 isoforms similarly promote lysosomal exocytosis, but exhibit differential localization in mast cells.
Keywords	SNARE proteins ; anaphylaxis ; cytosol ; exocytosis ; guanosinetriphosphatase ; humans ; leukemia ; lysosomes ; mice ; plasma membrane ; rats ; secretion
Language	English
Dates of publication	2021-04
Size	p. 1165-1185.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	2651702-4
ISSN	2211-5463
ISSN	2211-5463
DOI	10.1002/2211-5463.13133
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Article ; Online: Rab44 isoforms similarly promote lysosomal exocytosis, but exhibit differential localization in mast cells.

Kadowaki, Tomoko / Yamaguchi, Yu / Ogawa, Kohei / Tokuhisa, Mitsuko / Okamoto, Kuniaki / Tsukuba, Takayuki

FEBS open bio

2021 Volume 11, Issue 4, Page(s) 1165–1185

Abstract: Rab44 is a large Rab GTPase containing a Rab GTPase domain and some additional N-terminal domains. We recently used Rab44-deficient mice to demonstrate that Rab44 regulates granule exocytosis in mast cells and IgE-mediated anaphylaxis. In mouse mast ... ...

Abstract	Rab44 is a large Rab GTPase containing a Rab GTPase domain and some additional N-terminal domains. We recently used Rab44-deficient mice to demonstrate that Rab44 regulates granule exocytosis in mast cells and IgE-mediated anaphylaxis. In mouse mast cells, Rab44 is expressed as two isoforms, namely, the long and short forms; however, the characteristics of these two isoforms remain unknown. Here, we investigated secretion and localization of the human long Rab44 isoform and the two mouse isoforms and their mutants expressed in rat basophilic leukemia (RBL)-2H3 cells. Expression of the human long isoform and both mouse isoforms caused an increase in β-hexosaminidase secretion. Confocal and quantitative analyses showed that both human and mouse long isoforms localized mainly to lysosomes while the mouse short isoform localized mainly to the ER. Live imaging with LysoTracker indicated that the size and number of LysoTracker-positive vesicles were altered by the various mutants. Ionomycin treatment partially altered localization of both long isoforms to the plasma membrane and cytosol, whereas it had little effect on colocalization of the short isoform with lysosomes. Mechanistically, both human and mouse Rab44 proteins interacted with vesicle-associated membrane protein 8 (VAMP8), a v-SNARE protein. Therefore, Rab44 isoforms similarly promote lysosomal exocytosis, but exhibit differential localization in mast cells.
MeSH term(s)	Animals ; Endoplasmic Reticulum/metabolism ; Exocytosis ; Humans ; Lysosomes/metabolism ; Mast Cells/metabolism ; Mice ; Mice, Knockout ; Protein Transport ; Receptors, IgE/metabolism ; SNARE Proteins/metabolism ; beta-N-Acetylhexosaminidases/biosynthesis ; rab GTP-Binding Proteins/genetics ; rab GTP-Binding Proteins/metabolism
Chemical Substances	Receptors, IgE ; SNARE Proteins ; beta-N-Acetylhexosaminidases (EC 3.2.1.52) ; Rab44 protein, mouse (EC 3.6.5.2) ; rab GTP-Binding Proteins (EC 3.6.5.2)
Language	English
Publishing date	2021-03-19
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2651702-4
ISSN	2211-5463 ; 2211-5463
ISSN (online)	2211-5463
ISSN	2211-5463
DOI	10.1002/2211-5463.13133
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