The ATP Transporter VNUT Mediates Induction of Dectin-1-Triggered Candida Nociception
Summary: Candida albicans infection can cause skin, vulvar, or oral pain. Despite the obvious algesic activity of C. albicans, the molecular mechanisms of fungal nociception remain largely unknown. Here we show that the C. albicans-specific signaling pathway led to severe mechanical allodynia. We di...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2018-08-01
|
| Series: | iScience |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004218301196 |
| _version_ | 1818285932055363584 |
|---|---|
| author | Kenta Maruyama Yasunori Takayama Erika Sugisawa Yu Yamanoi Takashi Yokawa Takeshi Kondo Ken-ichi Ishibashi Bikash Ranjan Sahoo Naoki Takemura Yuki Mori Hisashi Kanemaru Yutaro Kumagai Mikaël M. Martino Yoshichika Yoshioka Hisao Nishijo Hiroki Tanaka Atsushi Sasaki Naohito Ohno Yoichiro Iwakura Yoshinori Moriyama Masatoshi Nomura Shizuo Akira Makoto Tominaga |
| author_facet | Kenta Maruyama Yasunori Takayama Erika Sugisawa Yu Yamanoi Takashi Yokawa Takeshi Kondo Ken-ichi Ishibashi Bikash Ranjan Sahoo Naoki Takemura Yuki Mori Hisashi Kanemaru Yutaro Kumagai Mikaël M. Martino Yoshichika Yoshioka Hisao Nishijo Hiroki Tanaka Atsushi Sasaki Naohito Ohno Yoichiro Iwakura Yoshinori Moriyama Masatoshi Nomura Shizuo Akira Makoto Tominaga |
| author_sort | Kenta Maruyama |
| collection | DOAJ |
| description | Summary: Candida albicans infection can cause skin, vulvar, or oral pain. Despite the obvious algesic activity of C. albicans, the molecular mechanisms of fungal nociception remain largely unknown. Here we show that the C. albicans-specific signaling pathway led to severe mechanical allodynia. We discovered that C. albicans-derived β-glucan stimulated nociceptors depending on Dectin-1, and two pathways in inflammatory pain. The major pathway operates via the Dectin-1-mediated ATP-P2X3/P2X2/3 axis through intercellular relationships between keratinocytes and primary sensory neurons, which depends on the ATP transporter vesicular nucleotide transporter (VNUT). The other pathway operates via the Dectin-1-mediated PLC-TRPV1/TRPA1 axis in primary sensory neurons. Intriguingly, C. albicans-derived β-glucan has the ability to enhance histamine-independent pruritus, and VNUT inhibitor clodronate can be used to treat unpleasant feelings induced by β-glucan. Collectively, this is the first report to indicate that Dectin-1 and VNUT mediated innate sensory mechanisms that detect fungal infection. : Molecular Mechanism of Behavior; Molecular Neuroscience; Medical Microbiology Subject Areas: Molecular Mechanism of Behavior, Molecular Neuroscience, Medical Microbiology |
| first_indexed | 2024-12-13T01:16:33Z |
| format | Article |
| id | doaj.art-af790e5323b74bdb88c067532d689b01 |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-12-13T01:16:33Z |
| publishDate | 2018-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-af790e5323b74bdb88c067532d689b012022-12-22T00:04:20ZengElsevieriScience2589-00422018-08-016306318The ATP Transporter VNUT Mediates Induction of Dectin-1-Triggered Candida NociceptionKenta Maruyama0Yasunori Takayama1Erika Sugisawa2Yu Yamanoi3Takashi Yokawa4Takeshi Kondo5Ken-ichi Ishibashi6Bikash Ranjan Sahoo7Naoki Takemura8Yuki Mori9Hisashi Kanemaru10Yutaro Kumagai11Mikaël M. Martino12Yoshichika Yoshioka13Hisao Nishijo14Hiroki Tanaka15Atsushi Sasaki16Naohito Ohno17Yoichiro Iwakura18Yoshinori Moriyama19Masatoshi Nomura20Shizuo Akira21Makoto Tominaga22Laboratory of Host Defense, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, Japan; Corresponding authorThermal Biology group, Exploratory Research Center on Life and Living Systems National Institutes of Natural Sciences, Okazaki Aichi 444-8787, Japan; Division of Cell Signaling, National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan; Department of Physiological Sciences, the Graduate University for Advanced Studies, Aichi 444-8787, JapanLaboratory of Host Defense, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, JapanThermal Biology group, Exploratory Research Center on Life and Living Systems National Institutes of Natural Sciences, Okazaki Aichi 444-8787, Japan; Division of Cell Signaling, National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan; Department of Physiological Sciences, the Graduate University for Advanced Studies, Aichi 444-8787, Japan; Research Laboratory, Ikedamohando Co., Ltd., 2-16-16 Iwamoto-cho, Chiyoda-ku, Tokyo 101-0032, JapanBioView Corporation, 2-16-16 Iwamoto-cho, Chiyoda-ku, Tokyo 101-0032, JapanLaboratory of Host Defense, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, JapanLaboratory for Immunopharmacology of Microbial Products, School of Pharmacy, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, JapanLaboratory of Host Defense, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, JapanDepartment of Mucosal Immunology, School of Medicine, Chiba University, 1-8-1 Inohana, Chuou-ku, Chiba 260-8670, JapanLaboratory of Biofunctional Imaging, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, JapanLaboratory of Host Defense, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, JapanLaboratory of Host Defense, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, Japan; Biotechnology Research Institute for Drug Discovery National Institute of Advanced Industrial Science and Technology Central 5-41, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8565, JapanLaboratory of Host Defense, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, Japan; European Molecular Biology Laboratory Australia, Australian Regenerative Medicine Institute, Innovation Walk, Monash University, Wellington Road, Clayton, VIC 3800, AustraliaLaboratory of Biofunctional Imaging, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, JapanSystem Emotional Science (Physiology), Graduate School of Medicine and Pharmaceutical Sciences for Research, University of Toyama, 2630 Sugitani, Toyama 930-0194, JapanLaboratory of Host Defense, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, JapanResearch Unit/Neuroscience Sohyaku, Innovative Research Division, Mitsubishi Tanabe Pharma Corporation, 1000, Kamoshida-cho, Aoba-ku, Yokohama 227-0033, JapanLaboratory for Immunopharmacology of Microbial Products, School of Pharmacy, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, JapanResearch Institute for Biomedical Sciences, Tokyo University of Science, 2669 Yamazaki, Noda, Chiba 278-0022, JapanDepartment of Membrane Biochemistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama 700-8530, JapanDepartment of Medicine and Bioregulatory Science, Kyushu University, Fukuoka 812-8582, JapanLaboratory of Host Defense, Osaka University, Osaka 565-0871, Japan; WPI Immunology Frontier Research Center (IFReC), Osaka University, Osaka 565-0871, JapanThermal Biology group, Exploratory Research Center on Life and Living Systems National Institutes of Natural Sciences, Okazaki Aichi 444-8787, Japan; Division of Cell Signaling, National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan; Department of Physiological Sciences, the Graduate University for Advanced Studies, Aichi 444-8787, Japan; Institute for Environmental and Gender Specific Medicine, Juntendo University, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan; Corresponding authorSummary: Candida albicans infection can cause skin, vulvar, or oral pain. Despite the obvious algesic activity of C. albicans, the molecular mechanisms of fungal nociception remain largely unknown. Here we show that the C. albicans-specific signaling pathway led to severe mechanical allodynia. We discovered that C. albicans-derived β-glucan stimulated nociceptors depending on Dectin-1, and two pathways in inflammatory pain. The major pathway operates via the Dectin-1-mediated ATP-P2X3/P2X2/3 axis through intercellular relationships between keratinocytes and primary sensory neurons, which depends on the ATP transporter vesicular nucleotide transporter (VNUT). The other pathway operates via the Dectin-1-mediated PLC-TRPV1/TRPA1 axis in primary sensory neurons. Intriguingly, C. albicans-derived β-glucan has the ability to enhance histamine-independent pruritus, and VNUT inhibitor clodronate can be used to treat unpleasant feelings induced by β-glucan. Collectively, this is the first report to indicate that Dectin-1 and VNUT mediated innate sensory mechanisms that detect fungal infection. : Molecular Mechanism of Behavior; Molecular Neuroscience; Medical Microbiology Subject Areas: Molecular Mechanism of Behavior, Molecular Neuroscience, Medical Microbiologyhttp://www.sciencedirect.com/science/article/pii/S2589004218301196 |
| spellingShingle | Kenta Maruyama Yasunori Takayama Erika Sugisawa Yu Yamanoi Takashi Yokawa Takeshi Kondo Ken-ichi Ishibashi Bikash Ranjan Sahoo Naoki Takemura Yuki Mori Hisashi Kanemaru Yutaro Kumagai Mikaël M. Martino Yoshichika Yoshioka Hisao Nishijo Hiroki Tanaka Atsushi Sasaki Naohito Ohno Yoichiro Iwakura Yoshinori Moriyama Masatoshi Nomura Shizuo Akira Makoto Tominaga The ATP Transporter VNUT Mediates Induction of Dectin-1-Triggered Candida Nociception iScience |
| title | The ATP Transporter VNUT Mediates Induction of Dectin-1-Triggered Candida Nociception |
| title_full | The ATP Transporter VNUT Mediates Induction of Dectin-1-Triggered Candida Nociception |
| title_fullStr | The ATP Transporter VNUT Mediates Induction of Dectin-1-Triggered Candida Nociception |
| title_full_unstemmed | The ATP Transporter VNUT Mediates Induction of Dectin-1-Triggered Candida Nociception |
| title_short | The ATP Transporter VNUT Mediates Induction of Dectin-1-Triggered Candida Nociception |
| title_sort | atp transporter vnut mediates induction of dectin 1 triggered candida nociception |
| url | http://www.sciencedirect.com/science/article/pii/S2589004218301196 |
| work_keys_str_mv | AT kentamaruyama theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yasunoritakayama theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT erikasugisawa theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yuyamanoi theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT takashiyokawa theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT takeshikondo theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT kenichiishibashi theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT bikashranjansahoo theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT naokitakemura theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yukimori theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT hisashikanemaru theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yutarokumagai theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT mikaelmmartino theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yoshichikayoshioka theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT hisaonishijo theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT hirokitanaka theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT atsushisasaki theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT naohitoohno theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yoichiroiwakura theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yoshinorimoriyama theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT masatoshinomura theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT shizuoakira theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT makototominaga theatptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT kentamaruyama atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yasunoritakayama atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT erikasugisawa atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yuyamanoi atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT takashiyokawa atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT takeshikondo atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT kenichiishibashi atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT bikashranjansahoo atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT naokitakemura atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yukimori atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT hisashikanemaru atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yutarokumagai atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT mikaelmmartino atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yoshichikayoshioka atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT hisaonishijo atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT hirokitanaka atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT atsushisasaki atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT naohitoohno atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yoichiroiwakura atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT yoshinorimoriyama atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT masatoshinomura atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT shizuoakira atptransportervnutmediatesinductionofdectin1triggeredcandidanociception AT makototominaga atptransportervnutmediatesinductionofdectin1triggeredcandidanociception |