Cited by 191Fungal and yeast genetics researchIon channel regulation and functionIon Channels and Receptors

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A Homolog of Mammalian, Voltage-Gated Calcium Channels Mediates Yeast Pheromone-Stimulated Ca 2+ Uptake and Exacerbates the cdc1 (Ts) Growth Defect

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Paidhungat, Madan, Garrett, Stephen·1997·Molecular and Cellular Biology

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Abstract

Previous studies attributed the yeast (Saccharomyces cerevisiae) cdc1(Ts) growth defect to loss of an Mn2+-dependent function. In this report we show that cdc1(Ts) temperature-sensitive growth is also associated with an increase in cytosolic Ca2+. We identified two recessive suppressors of the cdc1(Ts) temperature-sensitive growth which block Ca2+ uptake and accumulation, suggesting that cytosolic Ca2+ exacerbates or is responsible for the cdc1(Ts) growth defect. One of the cdc1(Ts) suppressors is identical to a gene, MID1, recently implicated in mating pheromone-stimulated Ca2+ uptake. The gene (CCH1) corresponding to the second suppressor encodes a protein that bears significant sequence similarity to the pore-forming subunit (alpha1) of plasma membrane, voltage-gated Ca2+ channels from higher eukaryotes. Strains lacking Mid1 or Cch1 protein exhibit a defect in pheromone-induced Ca2+ uptake and consequently lose viability upon mating arrest. The mid1delta and cch1delta mutants also display reduced tolerance to monovalent cations such as Li+, suggesting a role for Ca2+ uptake in the calcineurin-dependent ion stress response. Finally, mid1delta cch1delta double mutants are, by both physiological and genetic criteria, identical to single mutants. These and other results suggest Mid1 and Cch1 are components of a yeast Ca2+ channel that may mediate Ca2+ uptake in response to mating pheromone, salt stress, and Mn2+ depletion.

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The plant cell wall integrity maintenance mechanism – A case study of a cell wall plasma membrane signaling network
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“CCH1 exhibits limited similarity to the a1 subunit of animal voltage gated calcium channels suggesting it may respond to other stimuli as well (Paidhungat and Garrett, 1997).”
Background
NSC1: a novel high‐current inward rectifier for cations in the plasma membrane of Saccharomyces cerevisiae
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Phylogeny Unites Animal Sodium Leak Channels with Fungal Calcium Channels in an Ancient, Voltage-Insensitive Clade
Liebeskind, B. J., Hillis, D. M., & Zakon, H. H. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss182 · Cited by 64
“Fungal calcium channels have been implicated in mating in yeast (Paidhungat and Garrett 1997), calcium-store restoration in the meningitis-causing fungus Cryptococcus neoformans (Liu et al.”
BackgroundResult
The Involvement of the Mid1/Cch1/Yvc1 Calcium Channels in Aspergillus fumigatus Virulence
de Castro, P. A., Chiaratto, J., Winkelströter, L. K., Bom, V. L. P., Ramalho, L. N. Z., Goldman, M. H. S., Brown, N. A., & Goldman, G. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103957 · Cited by 60
The fungal opsin gene nop-1 is negatively-regulated by a component of the blue light sensing pathway and influences conidiation-specific gene expression in Neurospora crassa
Bieszke, J. A., Li, L., & Borkovich, K. A. (2007) · Current Genetics · doi:10.1007/s00294-007-0148-8 · Cited by 60
Vacuolar H+-ATPase (V-ATPase) Promotes Vacuolar Membrane Permeabilization and Nonapoptotic Death in Stressed Yeast
Kim, H., Kim, A., & Cunningham, K. W. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.363390 · Cited by 60
Fuel Ethanol Production from Sugarcane
Basso, T. P., & Basso, L. C. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.74271 · Cited by 57
Cch1 Restores Intracellular Ca2+ in Fungal Cells during Endoplasmic Reticulum Stress
Hong, M.-P., Vu, K., Bautos, J., & Gelli, A. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.056218 · Cited by 54
Ion-channel blocker sensitivity of voltage-gated calcium-channel homologue Cch1 in Saccharomyces cerevisiae
Teng, J., Goto, R., Iida, K., Kojima, I., & Iida, H. (2008) · Microbiology · doi:10.1099/mic.0.2008/021089-0 · Cited by 53
“3776 Microbiology 154 Downloaded from www.microbiologyresearch.org by IP: 54.70.40.11 On: Sun, 06 Jan 2019 12:35:16 the S. cerevisiae genome (Paidhungat & Garrett, 1997), but we have recently succeeded in cloning it, using a plasmid whose copy number is kept low in Escherichia coli (Iida et al.,…”
BackgroundMethodInfluential
Mid1, a Mechanosensitive Calcium Ion Channel, Affects Growth, Development, and Ascospore Discharge in the Filamentous Fungus Gibberella zeae
Cavinder, B., Hamam, A. M., Lew, R. R., & Trail, F. (2011) · Eukaryotic Cell · doi:10.1128/ec.00235-10 · Cited by 53
“Initially characterized in Saccharomyces cerevisiae, the HACS is composed minimally of Cch1, an L-type voltage gated calcium channel, and Mid1, a stretchactivated nonselective channel capable of being permeated by calcium and acting as the major calcium entry route when calcium availability is low (22, 27, 38), wherea…”
Background
Functional Analysis of a Rice Putative Voltage-Dependent Ca2+ Channel, OsTPC1, Expressed in Yeast Cells Lacking its Homologous Gene CCH1
Hashimoto, K., Saito, M., Matsuoka, H., Iida, K., & Iida, H. (2004) · Plant and Cell Physiology · doi:10.1093/pcp/pch053 · Cited by 49
Role of Fig1, a Component of the Low-Affinity Calcium Uptake System, in Growth and Sexual Development of Filamentous Fungi
Cavinder, B., & Trail, F. (2012) · Eukaryotic Cell · doi:10.1128/ec.00007-12 · Cited by 48
“All strains lacking functional Fig1 failed to develop perithecia, including the double and triple mutants with the HACS components Mid1 and Cch1, although they produced the characteristic black pigment seen in the top 2 to 4 mm of the medium after induction (Fig.”
BackgroundInfluential
Phenotype of a Mechanosensitive Channel Mutant, mid - 1 , in a Filamentous Fungus, Neurospora crassa
Lew, R. R., Abbas, Z., Anderca, M. I., & Free, S. J. (2008) · Eukaryotic Cell · doi:10.1128/ec.00411-07 · Cited by 47
Subcellular localization and oligomeric structure of the yeast putative stretch-activated Ca2+ channel component Mid1
Yoshimura, H., Tada, T., & Iida, H. (2004) · Experimental Cell Research · doi:10.1016/j.yexcr.2003.09.020 · Cited by 45
Calcium Release and Influx in Yeast: TRPC and VGCC Rule Another Kingdom
Bonilla, M., & Cunningham, K. W. (2002) · Science s STKE · doi:10.1126/stke.2002.127.pe17 · Cited by 45
The cell wall sensor Wsc1p is involved in reorganization of actin cytoskeleton in response to hypo‐osmotic shock in Saccharomyces cerevisiae
Gualtieri, T., Ragni, E., Mizzi, L., Fascio, U., & Popolo, L. (2004) · Yeast · doi:10.1002/yea.1155 · Cited by 45
“The existence of mechanosensors has been reported in yeast (Kanzaki et al., 1999; Paidhungat and Garrett, 1997).”
Background
Evidence for the Role of Calcineurin in Morphogenesis and Calcium Homeostasis during Mycelium-to-Yeast Dimorphism of Paracoccidioides brasiliensis
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Calcium homeostasis and signaling in fungi and their relevance forpathogenicity of yeasts and filamentous fungi
Tisi, R., Rigamonti, M. M., Groppi, S., & Belotti, F. (2016) · AIMS molecular science · doi:10.3934/molsci.2016.4.505 · Cited by 41
“pheromones [4], salt and environmental stresses [72,83,111,162,182,252], hypotonic shock [71,75], nutrient sensing [77,79,89,253-255], cell cycle progression [85,256], vacuole fusion [257], and cell integrity response [258].”
Background
Thigmo Responses: The Fungal Sense of Touch
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“To test this hypothesis, we constructed a mutant strain lacking Mid1p, which associates with Cch1p, a homologue of the mammalian high-affinity voltage-gated calcium channel component (Iida et al., 1994; Paidhungat and Garrett, 1997; Locke et al., 2000).”
Method
The Yeast Transcription Factor Crz1 Is Activated by Light in a Ca2+/Calcineurin-Dependent and PKA-Independent Manner
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“the role of the high-affinity calcium channel, Cch1p [44,45].”
BackgroundInfluential
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Identification and Analysis of Cation Channel Homologues in Human Pathogenic Fungi
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Yeast Mn2+ Transporter, Smf1p, Is Regulated by Ubiquitin-Dependent Vacuolar Protein Sorting
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“…the possibility thatviously characterized suppressors alleviated the cdc1(Ts) growth defect by mechanisms that are not obviously endocytosis plays a role in rapid elimination of Smf1p from the plasma membrane during transition fromrelated to intracellular Mn2 (Paidhungat and Garrett 1997, 1998a).”
BackgroundMethodSelf-citation
Deletion of Mid1, a putative stretch-activated calcium channel in Claviceps purpurea, affects vegetative growth, cell wall synthesis and virulence
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“…Ca2+ channel Cch1: it was shown previously that Mid1 either interacts with Cch1 or at least shares functional properties with it, as indicated by knockout of either gene in Ca. albicans (Brand et al., 2007) and Sac. cerevisiae (Fischer et al., 1997; Iida et al., 2004; Paidhungat & Garrett, 1997).”
Molecular cloning in yeast by in vivo homologous recombination of the yeast putative α1 subunit of the voltage‐gated calcium channel
Iida, K., Tada, T., & Iida, H. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.09.021 · Cited by 35
Sexual pheromone modulates the frequency of cytosolic Ca2+bursts inSaccharomyces cerevisiae
Carbó, N., Tarkowski, N., Ipiña, E. P., Dawson, S. P., & Aguilar, P. S. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-07-0481 · Cited by 34
“HACS depends on the simultaneous presence of three plasma membrane proteins: Cch1, a homologue of the catalytic α-subunit of voltage-gated Ca2+ channels (Fischer et al., 1997; Paidhungat and Garrett, 1997; Muller et al., 2001); Mid1, an integral membrane glycoprotein that physically interacts with Cch1 (Iida et al.”
Background
The CRaZy Calcium Cycle
Espeso, E. A. (2016) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-319-25304-6_7 · Cited by 33
Activation of an Essential Calcium Signaling Pathway in Saccharomyces cerevisiae by Kch1 and Kch2, Putative Low-Affinity Potassium Transporters
Stefan, C. P., Zhang, N., Sokabe, T., Rivetta, A., Slayman, C. L., Montell, C., & Cunningham, K. W. (2013) · Eukaryotic Cell · doi:10.1128/ec.00299-12 · Cited by 32
“Given the high sequence similarities between Cch1 and the catalytic subunits of mammalian voltage-gated Ca(2) channels (10, 11), we supposed that activation of HACS during the response to mating pheromones is likely to involve electrical depolarization of the cell membrane.”
Background
Cdc1 removes the ethanolamine phosphate of the first mannose of GPI anchors and thereby facilitates the integration of GPI proteins into the yeast cell wall
Vazquez, H. M., Vionnet, C., Roubaty, C., & Conzelmann, A. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-06-1033 · Cited by 32
“…Cdc1 may be involved in the removal of EtN-P from Man1, we produced a cdc1∆/mcd4∆ haploid strain deletion of DFG5 and DCW1 is lethal, suggesting that the covalent attachment of GPI-CWPs to glucans is essential, and this remains true even if cells receive osmotic support (Kitagaki et al., 2002).”
BackgroundInfluential
Cch1 and Mid1 Are Functionally Required for Vegetative Growth under Low-Calcium Conditions in the Phytopathogenic Ascomycete Botrytis cinerea
Harren, K., & Tudzynski, B. (2013) · Eukaryotic Cell · doi:10.1128/ec.00338-12 · Cited by 31
Ecm7, a regulator of HACS, functions in calcium homeostasis maintenance, oxidative stress response and hyphal development in Candida albicans
Ding, X., Yu, Q., Xu, N., Wang, Y., Cheng, X., Qian, K., Zhao, Q., Zhang, B., Xing, L., & Li, M. (2013) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2013.05.010 · Cited by 30
“Nearly all fungi contain a gene whose protein product is homologous to the catalytic a-subunits of voltage-gated Ca2+ channels (VGCCs) in animals (Fischer et al., 1997; Paidhungat and Garrett, 1997).”
Background
Antihypertensive, Amlodipine Besilate Inhibits Growth and Biofilm of Human Fungal Pathogen Candida
Gupta, P., Chanda, R., Rai, N., Kataria, V., & Kumar, N. (2016) · Assay and Drug Development Technologies · doi:10.1089/adt.2016.714 · Cited by 30
“32 –34 A similar Ca 2 + channel protein has also been verified in C. glabrata, that is, CgCch1.”
Ethanol induces calcium influx via the Cch1-Mid1 transporter in Saccharomyces cerevisiae
Courchesne, W. E., Vlasek, C., Klukovich, R., & Coffee, S. (2011) · Archives of Microbiology · doi:10.1007/s00203-010-0673-6 · Cited by 30
“…to voltage-gated ion channels, is emerging as a major player in stress responses, including osmotic stress and other plasma membrane perturbations (Fischer et al. 1997; Paidhungat and Garrett 1997; Locke et al. 2000; Muller et al. 2001; Bonilla et al. 2002; Matsumoto et al. 2002; Iida et al. 2004).”
Background

Authors: Paidhungat, M., & Garrett, S.
Affiliations: Duke University (US)
ORCID: Garrett, Stephen
Venue: Molecular and Cellular Biology
Publisher: Informa UK Limited
Published: 1997-11
Volume: 17
Issue: 11
Pages: 6339-6347
ISSN: 0270-7306 (ISSN-L)
1098-5549
DOI: 10.1128/mcb.17.11.6339
PMC: PMC232485
OpenAlex: W2162829341
Cited by: 191
References: 40
Citations by year: 2026: 1 · 2025: 4 · 2024: 1 · 2023: 2 · 2022: 4 · 2021: 3 · 2020: 4 · 2019: 5 · 2018: 3 · 2017: 11 · 2016: 9 · 2015: 6 · 2014: 8 · 2013: 8 · 2012: 12
FWCI: 2.02
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Molecular and Cellular Biology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
Keywords: voltage-gated calcium channels, calcium uptake, MID1, mating pheromone signaling, intracellular calcium, lithium tolerance, manganese depletion, salt stress, Saccharomyces cerevisiae
MeSH terms: Amino Acid Sequence, Biological Transport, Calcium, Fungal Proteins, Membrane Glycoproteins, Molecular Sequence Data, Mutation, Pheromones, Saccharomyces cerevisiae, Suppression, Genetic, Calcium Channels, Ion Channel Gating, Gene Expression, Sequence Homology, Amino Acid, Cell Cycle Proteins, Saccharomyces cerevisiae Proteins

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A Homolog of Mammalian, Voltage-Gated Calcium Channels Mediates Yeast Pheromone-Stimulated Ca 2+ Uptake and Exacerbates the cdc1 (Ts) Growth Defect

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