Calmodulin Kinase 2 Genetically Interacts with Rch1p to Negatively Regulate Calcium Import into Saccharomyces Cerevisiae After Extracellular Calcium Pulse

Overview

Journal Arch Microbiol

Specialty Microbiology

Date 2022 Jul 24

PMID 35871646

Authors

Christian E Coleman

Chelsea Landin

Abigail Neuer

Fadi M Sayegh

Pamela A Marshall

Affiliations

Soon will be listed here.

Abstract

After a single extracellular 100 mM calcium pulse (final concentration), wild type S. cerevisiae exhibits a sharp peak in cytosolic calcium. The concentration drops rapidly in these cells as the calcium is sequestered away in the endoplasmic reticulum, Golgi, and vacuoles leaving resting cytosolic levels higher than their original state, followed by changes in gene expression. In cells lacking calmodulin kinase 2 (Cmk2p), a secondary rise in cytosolic calcium concentration is seen after extracellular calcium increases and the cytosolic calcium is subsequently sequestered. Utilizing double deletions, we demonstrate that Cmk2p is modulating the activity of Rch1p, a known inhibitor of Channel X which is a yeast plasma membrane channel through which calcium ions are transported after an extracellular calcium pulse. We hypothesize that Cmk2p is acting as a regulator of Channel X by activating Rch1p and without CMK2, Channel X inactivation does not occur fully.

Citing Articles

The calcineurin-responsive transcription factor Crz1 regulates the expression of CMK2 via a sole CDRE site in its promoter in budding yeast.

Jiang L, Gu Y, Jiang Y, Wei L, Meng L, Guan N Sci Rep. 2025; 15(1):7046.

PMID: 40016385 PMC: 11868491. DOI: 10.1038/s41598-025-91599-4.

Shedding Light on Calcium Dynamics in the Budding Yeast: A Review on Calcium Monitoring with Recombinant Aequorin.

Gogianu L, Ruta L, Farcasanu I Molecules. 2024; 29(23).

PMID: 39683786 PMC: 11643140. DOI: 10.3390/molecules29235627.

Identification of the Beta Subunit Fas1p of Fatty Acid Synthetase as an Interacting Partner of Yeast Calcium/Calmodulin-Dependent Protein Kinase Cmk2p Through Mass Spectrometry Analysis.

Jiang L, Li Y, Gu Y, Zheng J, Wei L, Wei M Appl Biochem Biotechnol. 2024; 196(10):6836-6848.

PMID: 38411936 DOI: 10.1007/s12010-024-04891-w.

References

Adamikova L, Straube A, Schulz I, Steinberg G . Calcium signaling is involved in dynein-dependent microtubule organization. Mol Biol Cell. 2004; 15(4):1969-80. PMC: 379291. DOI: 10.1091/mbc.e03-09-0675. View

Ahmed T, Nisler C, Fluck 3rd E, Walujkar S, Sotomayor M, Moiseenkova-Bell V . Structure of the ancient TRPY1 channel from Saccharomyces cerevisiae reveals mechanisms of modulation by lipids and calcium. Structure. 2021; 30(1):139-155.e5. PMC: 8741645. DOI: 10.1016/j.str.2021.08.003. View

Amini M, Wang H, Belkacemi A, Jung M, Bertl A, Schlenstedt G . Identification of Inhibitory Ca Binding Sites in the Upper Vestibule of the Yeast Vacuolar TRP Channel. iScience. 2018; 11:1-12. PMC: 6299153. DOI: 10.1016/j.isci.2018.11.037. View

Amini M, Chang Y, Wissenbach U, Flockerzi V, Schlenstedt G, Beck A . Activity of the yeast vacuolar TRP channel TRPY1 is inhibited by Ca-calmodulin binding. J Biol Chem. 2021; 297(4):101126. PMC: 8449268. DOI: 10.1016/j.jbc.2021.101126. View

Bagur R, Hajnoczky G . Intracellular Ca Sensing: Its Role in Calcium Homeostasis and Signaling. Mol Cell. 2017; 66(6):780-788. PMC: 5657234. DOI: 10.1016/j.molcel.2017.05.028. View

Bouillet L, Cardoso A, Perovano E, Pereira R, Ribeiro E, Tropia M . The involvement of calcium carriers and of the vacuole in the glucose-induced calcium signaling and activation of the plasma membrane H(+)-ATPase in Saccharomyces cerevisiae cells. Cell Calcium. 2011; 51(1):72-81. DOI: 10.1016/j.ceca.2011.10.008. View

Carraro M, Bernardi P . Calcium and reactive oxygen species in regulation of the mitochondrial permeability transition and of programmed cell death in yeast. Cell Calcium. 2016; 60(2):102-7. PMC: 4996716. DOI: 10.1016/j.ceca.2016.03.005. View

Cascella R, Cecchi C . Calcium Dyshomeostasis in Alzheimer's Disease Pathogenesis. Int J Mol Sci. 2021; 22(9). PMC: 8124842. DOI: 10.3390/ijms22094914. View

Castanheira D, Santana E, Godoy-Santos F, Diniz R, Faria-Oliveira F, Pereira R . Lpx1p links glucose-induced calcium signaling and plasma membrane H+-ATPase activation in Saccharomyces cerevisiae cells. FEMS Yeast Res. 2017; 18(1). DOI: 10.1093/femsyr/fox088. View

10.

Chandel A, Das K, Bachhawat A . Glutathione depletion activates the yeast vacuolar transient receptor potential channel, Yvc1p, by reversible glutathionylation of specific cysteines. Mol Biol Cell. 2016; 27(24):3913-3925. PMC: 5170613. DOI: 10.1091/mbc.E16-05-0281. View

11.

Clapham D . Calcium signaling. Cell. 2007; 131(6):1047-58. DOI: 10.1016/j.cell.2007.11.028. View

12.

Colinet A, Sengottaiyan P, Deschamps A, Colsoul M, Thines L, Demaegd D . Yeast Gdt1 is a Golgi-localized calcium transporter required for stress-induced calcium signaling and protein glycosylation. Sci Rep. 2016; 6:24282. PMC: 4830978. DOI: 10.1038/srep24282. View

13.

Courchesne W, Ozturk S . Amiodarone induces a caffeine-inhibited, MID1-depedent rise in free cytoplasmic calcium in Saccharomyces cerevisiae. Mol Microbiol. 2002; 47(1):223-34. DOI: 10.1046/j.1365-2958.2003.03291.x. View

14.

Cui J, Kaandorp J, Ositelu O, Beaudry V, Knight A, Nanfack Y . Simulating calcium influx and free calcium concentrations in yeast. Cell Calcium. 2008; 45(2):123-32. PMC: 3130064. DOI: 10.1016/j.ceca.2008.07.005. View

15.

Cunningham K . Acidic calcium stores of Saccharomyces cerevisiae. Cell Calcium. 2011; 50(2):129-38. PMC: 3137693. DOI: 10.1016/j.ceca.2011.01.010. View

16.

Cyert M . Genetic analysis of calmodulin and its targets in Saccharomyces cerevisiae. Annu Rev Genet. 2001; 35:647-72. DOI: 10.1146/annurev.genet.35.102401.091302. View

17.

Cyert M . Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. Biochem Biophys Res Commun. 2003; 311(4):1143-50. DOI: 10.1016/s0006-291x(03)01552-3. View

18.

Cyert M, Philpott C . Regulation of cation balance in Saccharomyces cerevisiae. Genetics. 2013; 193(3):677-713. PMC: 3583992. DOI: 10.1534/genetics.112.147207. View

19.

Denis V, Cyert M . Internal Ca(2+) release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol. 2002; 156(1):29-34. PMC: 2173594. DOI: 10.1083/jcb.200111004. View

20.

Dudgeon D, Zhang N, Ositelu O, Kim H, Cunningham K . Nonapoptotic death of Saccharomyces cerevisiae cells that is stimulated by Hsp90 and inhibited by calcineurin and Cmk2 in response to endoplasmic reticulum stresses. Eukaryot Cell. 2008; 7(12):2037-51. PMC: 2593186. DOI: 10.1128/EC.00291-08. View