Publicado

2026-01-26

The role of calcium ions and the calcineurin route in fungal virulence: a review

El papel de los iones de calcio y de la vía de calcineurina en la virulencia fúngica: una revisión

O papel dos íons de cálcio e da via de calcineurina na virulência fúngica: uma revisão

DOI:

https://doi.org/10.15446/rcciquifa.v55n1.125068

Palabras clave:

Calcium, calcineurin, fungi, virulence (en)
Calcio, calcineurina, hongos, virulencia (es)
Cálcio, calcineurina, fungos, virulência (pt)

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Autores/as

  • Francisco Patricio de Andrade Júnior Faculty of Medical Sciences, State University of Piauí, Teresina, Brazil
  • Gleice Rayanne da Silva Faculty of Medical Sciences, State University of Piauí, Teresina, Brazil
  • Valgrícia Matias de Sousa Faculty of Medical Sciences, State University of Piauí, Teresina, Brazil
  • Bagnólia Araújo Costa Faculty of Medical Sciences, State University of Piauí, Teresina, Brazil

Introduction: Calcium ions (Ca²⁺) play a fundamental role in regulating various cellular processes and are present in all living organisms. In microorganisms such as fungi, the Ca²⁺ signaling pathway supports essential functions for survival, including stress resistance, apoptosis, growth, reproduction, and virulence. Objective: This review aims to explore the importance of Ca²⁺ and the calcineurin pathway in the development and maintenance of fungal virulence. Method: This is a narrative review based on literature available in the PubMed and ScienceDirect databases, focusing on articles published between 2015 and 2024. Results: The findings reveal that the calcineurin pathway is crucial for several processes contributing to fungal virulence. Calcineurin becomes active through calmodulin, a protein that requires calcium ions for its activation. The main processes regulated by calcium and calcineurin include the formation and maintenance of cell walls, hyphae, and biofilms. Moreover, these components are involved in conidia formation and increase thermotolerance in certain pathogenic fungi. It is worth noting that calcineurin inhibitors, such as cyclosporine A and tacrolimus, have shown synergistic effects when combined with antifungal agents like fluconazole and micafungin. Conclusions: These findings highlight the potential of Ca²⁺ and the calcineurin pathway as promising pharmacological targets for the development of new antifungal strategies.

Introducción: Los iones de calcio (Ca²⁺) desempeñan un papel fundamental en la regulación de diversos procesos celulares y están presentes en todos los organismos vivos. En microorganismos como los hongos, la vía de señalización del Ca²⁺ sostiene funciones esenciales para la supervivencia, incluyendo la resistencia al estrés, la apoptosis, el crecimiento, la reproducción y la virulencia. Objetivo: Esta revisión tiene como objetivo explorar la importancia del Ca²⁺ y de la vía de la calcineurina en el desarrollo y mantenimiento de la virulencia fúngica. Metodología: Se trata de una revisión narrativa basada en la literatura disponible en las bases de datos PubMed y ScienceDirect, con énfasis en artículos publicados entre 2015 y 2024. Resultados: Los resultados revelan que la vía de la calcineurina es crucial para diversos procesos que contribuyen a la virulencia fúngica. La calcineurina se activa a través de la calmodulina, una proteína que requiere iones de calcio para su activación. Los principales procesos regulados por el calcio y la calcineurina incluyen la formación y el mantenimiento de las paredes celulares, las hifas y el biofilm. Además, estos componentes participan en la formación de conidios y aumentan la termotolerancia en ciertos hongos patógenos. Cabe destacar que los inhibidores de la calcineurina, como la ciclosporina A y el tacrolimus, han demostrado efectos sinérgicos cuando se combinan con agentes antifúngicos como el fluconazol y la micafungina. Conclusiones: Estos hallazgos destacan el potencial del Ca²⁺ y de la vía de la calcineurina como objetivos farmacológicos prometedores para el desarrollo de nuevas estrategias antifúngicas

Introdução: Os íons de cálcio (Ca²⁺) desempenham um papel fundamental na regulação de diversos processos celulares e estão presentes em todos os organismos vivos. Em microrganismos como os fungos, a via de sinalização do Ca²⁺ apoia funções essenciais para a sobrevivência, incluindo resistência ao estresse, apoptose, crescimento, reprodução e virulência. Objetivo: Esta revisão tem como objetivo explorar a importância do Ca²⁺ e da via de calcineurina no desenvolvimento e manutenção da virulência fúngica. Método: Trata-se de uma revisão narrativa realizada com base na literatura disponível nas bases de dados PubMed e ScienceDirect, com foco em artigos publicados entre 2015 e 2024. Resultados: Os resultados revelam que a via de calcineurina é crucial para diversos processos que contribuem para a virulência fúngica. A calcineurina torna-se ativa por meio da calmodulina, uma proteína que necessita de íons de cálcio para sua ativação. Os principais processos regulados pelo cálcio e pela calcineurina incluem a formação e manutenção das paredes celulares, das hifas e do biofilme. Além disso, esses componentes estão envolvidos na formação de conídios e aumentam a termotolerância em certos fungos patogênicos. Vale destacar que os inibidores de calcineurina, como a ciclosporina A e o tacrolimo, demonstraram efeitos sinérgicos quando combinados com agentes antifúngicos como fluconazol e micafungina. Conclusões: Esses achados destacam o potencial do Ca²⁺ e da via de calcineurina como alvos farmacológicos promissores para o desenvolvimento de novas estratégias antifúngicas.

Referencias

1. M.A. Ruggiero, D.P. Gordon, T.M. Orrell, N. Bailly, T. Bourgoin, R.C. Brusca, T. Cavalier-Smith, M.D. Guiry & P.M. Kirk. Correction: A higher level classification of all living organisms. PLoS One, 10(4), e0130114 (2015). https://doi.org/10.1371/journal.pone.0130114

2. C.J.A. Silva & D.J.N. Malta. A importância dos fungos na biotecnologia. Cadernos de Graduação, 2(3) 49-66 (2016). URL: https://periodicos.grupotiradentes.com/unitsaude/article/view/3210/2080

3. L. Vuyst, H. Harth, S. Van Kerrebroeck & F. Leroy. Yeast diversity of sourdoughs and associated metabolic properties and functionalities. International Journal of Food Microbiology, 239, 26–34 (2016). https://doi.org/10.1016/j.ijfoodmicro.2016.07.018

4. M. Lange & E. Peiter. Cytosolic free calcium dynamics as related to hyphal and colony growth in the filamentous fungal pathogen Colletotrichum graminicola. Fungal Genetics and Biology, 91, 55–65 (2016). https://doi.org/10.1016/j.fgb.2016.04.001

5. E. Carafoli & J. Krebs. Why calcium? How calcium became the best communicator. The Journal of Biological Chemistry, 291(40), 20849–20857 (2016). https://doi.org/10.1074/jbc.R116.735894

6. A, Roy, A. Kumar, D. Baruah & R. Tamuli. Calcium signaling is involved in diverse cellular processes in fungi. Mycology, 12(1), 10–24 (2020). https://doi.org/10.1080/21501203.2020.1785962

7. S. Wang, X. Liu, H. Qian, S. Zhang & L. Lu. Calcineurin and calcium channel CchA coordinate the salt stress response by regulating cytoplasmic Ca2+ homeostasis in Aspergillus nidulans. Applied and Environmental Microbiology, 82(11), 3420–3430 (2016). https://doi.org/10.1128/AEM.00330-16

8. H. Tian, S. Qu, Y. Wang, Z. Lu, M. Zhang, Y. Gan, P. Zhang & J. Tian. Calcium and oxidative stress mediate perillaldehyde-induced apoptosis in Candida albicans. Applied Microbiology and Biotechnology. 101, 3335–3345 (2017). https://doi.org/10.1007/s00253-017-8146-3

9. J. Wang, X.-G. Zhu, S.-H. Ying & M.-G. Feng. Differential roles for six P-type calcium ATPases in sustaining intracellular Ca2+ homeostasis, asexual cycle and environmental fitness of Beauveria bassiana. Scientific Reports. 7, 1420 (2017). https://doi.org/10.1038/s41598-017-01570-1

10. M. Lange & E. Peiter. Calcium transport proteins in fungi: The phylogenetic diversity of their relevance for growth, virulence, and stress resistance. Frontiers in Microbiology, 10, 3100 (2020). https://doi.org/10.3389/fmicb.2019.03100

11. S.K. Shishodia, S. Tiwari, S. Hoda, P. Vijayaraghavan & J. Shankar. SEM and qRT-PCR revealed quercetin inhibits morphogenesis of Aspergillus flavus conidia via modulating calcineurin-Crz1 signalling pathway. Mycology, 11(2), 118–125 (2020). https://doi.org/10.1080/21501203.2020.1711826

12. D. Chinnapun. Virulence factors involved in pathogenicity of dermatophytes. Walailak Journal of Science and Technology (WJST), 12(7), 573–580 (2015). URL: https://wjst.wu.ac.th/index.php/wjst/article/view/1473/501

13. R.A. Cordeiro, J.S. Oliveira, D.S. Castelo-Branco, C.E. Teixeira, F.J. Marques, P.V. Bittencourt, et al. Candida tropicalis isolates obtained from veterinary sources show resistance to azoles and produce virulence factors. Medical Mycology, 53(2), 145–152 (2015). https://doi.org/10.1093/mmy/myu081

14. J.S. Curcio, J.D. Paccez, E. Novaes, M. Brock & C.M.A. Soares. Cell wall synthesis, development of hyphae and metabolic pathways are processes potentially regulated by microRNAs produced between the morphological stages of Paracoccidioides brasiliensis. Frontiers in Microbiology. 9, 3057 (2018). https://doi.org/10.3389/fmicb.2018.03057

15. S.C. Lee, A. Li, S. Calo, M. Inoue, N.K. Tonthat, J.M. Bain, et al. Calcineurin orchestrates dimorphic transitions, antifungal drug responses and host-pathogen interactions of the pathogenic mucoralean fungus Mucor circinelloides. Molecular Microbiology, 97(5), 844–865 (2015). https://doi.org/10.1111/mmi.13071

16. C. Fu, N. Donadio, M.E. Cardenas & J. Heitman. Dissecting the roles of the calcineurin pathway in unisexual reproduction, stress responses, and virulence in Cryptococcus deneoformans. Genetics, 208(2), 639–653 (2018). https://doi.org/10.1534/genetics.117.300422

17. A. Shah, S. Kannambath, S. Herbst, A. Rogers, S. Soresi, M. Carby, A. Reed, S. Mostowy, M.C. Fisher, S. Shaunak & D.P. Armstrong-James. Calcineurin orchestrates lateral transfer of Aspergillus fumigatus during macrophage cell death. American Journal of Respiratory and Critical Care Medicine, 194(9), 1127–1139 (2016). https://doi.org/10.1164/rccm.201601-0070OC

18. H.S. Park, S.C. Lee, M.E. Cardenas & J. Heitman. Calcium-calmodulin-calcineurin signaling: A globally conserved virulence cascade in eukaryotic microbial pathogens. Cell Host & Microbe, 26(4), 453–462 (2019). https://doi.org/10.1016/j.chom.2019.08.004

19. W. Huang, X. Liu, X. Zhou, X. Wang, X. Liu & H. Liu. Calcium signaling is suppressed in Magnaporthe oryzae conidia by Bacillus cereus HS24. Phytopathology, 110(2), 309–316 (2020). https://doi.org/10.1094/phyto-08-18-0311-r

20. R. Tisi, M. Rigamonti, S. Groppi & F. Belotti. Calcium homeostasis and signaling in fungi and their relevance for pathogenicity of yeasts and filamentous fungi. AIMS Molecular Science, 3(4), 505-549 (2016). https://doi.org/10.3934/molsci.2016.4.505

21. M. Lange, F. Weihmann, I. Schliebner, R. Horbach, H.B. Deising, S.G. Wirsel & E. Peiter. The transient receptor potential (TRP) channel family in Colletotrichum graminicola: A molecular and physiological analysis. PLoS One, 11(6), e0158561 (2016). https://doi.org/10.1371/journal.pone.0158561

22. Y. Gao, W. Li, X. Liu, F. Gao & X. Zhao. Reversing effect and mechanism of soluble resistancerelated calcium-binding protein on multidrug resistance in human lung cancer A549/DDP cells. Molecular Medicine Reports, 11(3), 2118–2124 (2015). https://doi.org/10.3892/mmr.2014.2936

23. S. Hamamoto, Y. Mori, I. Yabe & N. Uozumi. In vitro and in vivo characterization of modulation of the vacuolar cation channel TRPY1 from Saccharomyces cerevisiae. The FEBS Journal, 285(6), 1146–1161 (2018). https://doi.org/10.1111/febs.14399

24. P. Thapak, B. Vaidya, H.C. Joshi, J.N. Singh & S.S. Sharma. Therapeutic potential of pharmacological agents targeting TRP channels in CNS disorders. Pharmacological Research, 159, 105026 (2020). https://doi.org/10.1016/j.phrs.2020.105026

25. E.D. Squizani, N.K. Oliveira, J.C.V. Reuwsaat, B.M. Marques, W. Lopes, A.L. Gerber, et al. Cryptococcal dissemination to the central nervous system requires the vacuolar calcium transporter Pmc1. Cellular Microbiology, 20, e12803 (2018). https://doi.org/10.1111/cmi.12803

26. F.P. Andrade Júnior, J.M.M. Sousa, H.I.F. Magalhães & E.O. Lima. Sobrevivendo na ciência em tempos de pandemia: como lidar?. HOLOS, 37(4), e11599 (2021). URL: https://www2.ifrn.edu.br/ojs/index.php/HOLOS/article/view/11599/pdf

27. R.A. Hall. Dressed to impress: impact of environmental adaptation on the Candida albicans cell wall. Molecular Microbiology, 97(1), 7–17 (2015). https://doi.org/10.1111/mmi.13020

28. A. Rella, A.M. Farnoud & M. Del Poeta. Plasma membrane lipids and their role in fungal virulence. Progress in Lipid Research, 61, 63–72 (2016). https://doi.org/10.1016/j.plipres.2015.11.003

29. Y. Wang, J. Wang, J. Cheng, D. Xu & L. Jiang. Genetic interactions between the Golgi Ca2+/H+ exchanger Gdt1 and the plasma membrane calcium channel Cch1/Mid1 in the regulation of calcium homeostasis, stress response and virulence in Candida albicans. FEMS Yeast Research, 15(7), fov069 (2015). https://doi.org/10.1093/femsyr/fov069

30. H. Akiyama & Y. Hirabayashi. A novel function for glucocerebrosidase as a regulator of sterylglucoside metabolism. Biochimica et Biophysica Acta (BBA) - General Subjects, 1861(10), 2507–2514 (2017). https://doi.org/10.1016/j.bbagen.2017.06.003

31. V. Yadav & J. Heitman. Calcineurin: The Achilles’ heel of fungal pathogens. PLoS Pathogens, 19(7), e1011445 (2023). https://doi.org/10.1371/journal.ppat.1011445

32. C.V. Giuraniuc, C. Parkin, M.C. Almeida, M. Fricker, P. Shadmani, S. Nye, et al. Dynamic calciummediated stress response and recovery signatures in the fungal pathogen, Candida albicans. mBio, 14(5), e0115723 (2023). https://doi.org/10.1128/mbio.01157-23

33. T. Kato, A. Kubo, T. Nagayama, S. Kume, C. Tanaka, Y. Nakayama, K. Iida & H. Iida. Genetic analysis of the regulation of the voltage-gated calcium channel homolog Cch1 by the γ subunit homolog Ecm7 and cortical ER protein Scs2 in yeast. PLoS One, 12(7), e0181436 (2017). https://doi.org/10.1371/journal.pone.0181436

34. M. Xie, X. Zhou, Y. Xia & Y. Cao. Mid1 affects ion transport, cell wall integrity, and host penetration of the entomopathogenic fungus Metarhizium acridum. Applied Microbiology and Biotechnology, 103, 1801–1810 (2019). https://doi.org/10.1007/s00253-018-09589-8

35. H.S. Kim, J.-E. Kim, H. Son, D. Frailey, R. Cirino, Y.W. Lee, R. Duncan, K.J. Czymmek & S. Kang. Roles of three Fusarium graminearum membrane Ca2+ channels in the formation of Ca2+ signatures, growth, development, pathogenicity and mycotoxin production. Fungal Genetics and Biology, 111, 30–46 (2018). https://doi.org/10.1016/j.fgb.2017.11.005

36. W. Zhang, C. Hu, M. Hussain, J. Chen, M. Xiang & X. Liu. Role of low-affinity calcium system member Fig1 homologous proteins in conidiation and trap-formation of nematode-trapping fungus Arthrobotrys oligospora. Scientific Reports, 9, 4440 (2019). https://doi.org/10.1038/s41598-019-40493-x

37. A. Cacciotti, M. Beccaccioli & M. Reverberi. The CRZ1 transcription factor in plant fungi: regulation mechanism and impact on pathogenesis. Molecular Biology Reports, 51, 647 (2024). https://doi.org/10.1007/s11033-024-09593-4

38. L. Jiang, H. Xu, M. Wei, Y. Gu, H. Yan, L. Pan & C. Wei. Transcriptional expression of PHR2 is positively controlled by the calcium signaling transcription factor Crz1 through its binding motif in the promoter. Microbiology Spectrum, 12(1), e0168923 (2024). https://doi.org/10.1128/spectrum.01689-23

39. A. Takeuchi, B. Kim & S. Matsuoka. The destiny of Ca2+ released by mitochondria. The Journal of Physiological Sciences, 65(1), 11–24 (2015). https://doi.org/10.1007/s12576-014-0326-7

40. Z. Gong & A.J. Karlsson. Translocation of cell-penetrating peptides into Candida fungal pathogens. Protein Science, 26(9), 1714–1725 (2017). https://doi.org/10.1002/pro.3203

41. Y. Zhang, H. Jiang & L. Lu. Calcium cation cycling and signaling pathways in fungi. In: D. Hoffmeister & M. Gressler (editors) Biology of the Fungal Cell. (The Mycota, vol 8). Springer, Cham, 2019; pp. 111–123. https://doi.org/10.1007/978-3-030-05448-9_7

42. M. Amini, H. Wang, A. Belkacemi, M. Jung, A. Bertl, G. Schlenstedt, V. Flockerzi & A. Beck. Identification of inhibitory Ca2+ binding sites in the upper vestibule of the yeast vacuolar TRP channel. iScience, 11, 1–12 (2019). https://doi.org/10.1016/j.isci.2018.11.037

43. D. Kundu & R. Pasrija. The ERMES (Endoplasmic Reticulum and Mitochondria Encounter Structures) mediated functions in fungi. Mitochondrion, 52, 89–99 (2020). https://doi.org/10.1016/j.mito.2020.02.010

44. H. Wang, R. Gao, Y. Zhang & L. Lu. The versatility of the putative transient receptor potential ion channels in regulating the calcium signaling in Aspergillus nidulans. mSphere, 8(6), e0054923 (2023). https://doi.org/10.1128/msphere.00549-23

45. X. Zhang, J. Shao, A. Chen, C. Shang, X. Hu, S. Luo, M. Lei, L. Peng & Q. Zeng. Effects of cadmium on calcium homeostasis in the white-rot fungus Phanerochaete chrysosporium. Ecotoxicology and Environmental Safety, 157, 95–101 (2018). https://doi.org/10.1016/j.ecoenv.2018.03.071

46. C.V. Giuraniuc, C. Parkin, M.C. Almeida, M. Fricker, P. Shadmani, S. Nye, et al. Dynamic calciummediated stress response and recovery signatures in the fungal pathogen, Candida albicans. mBio, 14(5), e01157-23 (2023). https://doi.org/10.1128/mbio.01157-23

47. I. Kyrmizi, H. Ferreira, A. Carvalho, J.A.L. Figueroa, P. Zarmpas, C. Cunha, et al. Calcium sequestration by fungal melanin inhibits calcium-calmodulin signalling to prevent LC3-associated phagocytosis. Nature Microbiology, 3, 791–803 (2018). https://doi.org/10.1038/s41564-018-0167-x

48. A. González-Montoro, K. Auffarth, C. Hönscher, M. Bohnert, T. Becker, B. Warscheid, F. Reggiori, M. van der Laan, F. Fröhlich & C. Ungermann. Vps39 interacts with Tom40 to establish one of two functionally distinct vacuole-mitochondria contact sites. Developmental Cell, 45(5), 621–636.e7 (2018). https://doi.org/10.1016/j.devcel.2018.05.011

49. Y. Tamura, S. Kawano & T. Endo. Organelle contact zones as sites for lipid transfer. The Journal of Biochemistry, 165(2), 115–123 (2019). https://doi.org/10.1093/jb/mvy088

50. S. Cohen, A.M. Valm & J. Lippincott-Schwartz. Interacting organelles. Current Opinion in Cell Biology, 53, 84–91 (2018). https://doi.org/10.1016/j.ceb.2018.06.003

51. A.P. Gonçalves, J. Heller, A. Daskalov, A. Videira & N.L. Glass. Regulated forms of cell death in fungi. Frontiers in Microbiology, 8, 1837 (2017). https://doi.org/10.3389/fmicb.2017.01837

52. N.A.R. Gow & M.D. Lenardon. Architecture of the dynamic fungal cell wall. Nature Reviews: Microbiology, 21(4), 248–259 (2023). https://doi.org/10.1038/s41579-022-00796-9

53. H. Martín & M. Molina. Special issue "The fungal cell wall integrity pathway". Journal of Fungi (Basel, Switzerland), 9(3), 293 (2023). https://doi.org/10.3390/jof9030293

54. I. Geoghegan, G. Steinberg & S. Gurr. The role of the fungal cell wall in the infection of plants. Trends in microbiology. 25(12), 957-967 (2017). https://doi.org/10.1016/j.tim.2017.05.015

55. N.A.R. Gow, J. Latge & C.A. Munro. The fungal cell wall: Structure, biosynthesis, and function. Microbiology Spectrum, 5(3), FUNK-0035-2016 (2017). https://doi.org/10.1128/microbiolspec.funk0035-2016

56. L. Liu, B. Yu, W. Sun, C. Liang, H. Ying, S. Zhou, H. Niu, Y. Wang, D. Liu & Y. Chen. Calcineurin signaling pathway influences Aspergillus niger biofilm formation by affecting hydrophobicity and cell wall integrity. Biotechnology for Biofuels and Bioproducts, 13, 54 (2020). https://doi.org/10.1186/s13068-020-01692-1

57. P. Wang, B. Li, Y.T. Pan, Y.Z. Zhang, D. W. Li & L. Huang. Calcineurin-responsive transcription factor CgCrzA is required for cell wall integrity and infection-related morphogenesis in Colletotrichum gloeosporioides. The Plant Pathology Journal, 36(5), 385–397 (2020). https://doi.org/10.5423/ppj.oa.04.2020.0071

58. G.U. Braga, D.E. Rangel, É.K. Fernandes, S.D. Flint & D.W. Roberts. Molecular and physiological effects of environmental UV radiation on fungal conidia. Current Genetics, 61(3), 405–425 (2015). https://doi.org/10.1007/s00294-015-0483-0

59. T.J.H. Baltussen, J. Zoll, P.E. Verweij & W.J.G. Melchers. Molecular mechanisms of conidial germination in Aspergillus spp. Microbiology and Molecular Biology Reviews, 84(1), e00049-19 (2019). https://doi.org/10.1128/mmbr.00049-19

60. A. Yoshimi, K. Miyazawa, M. Kawauchi & K. Abe. Cell wall integrity and its industrial applications in filamentous fungi. Journal of Fungi (Basel, Switzerland), 8(5), 435 (2022). https://doi.org/10.3390/jof8050435

61. J.G. Vasselli & B.D. Shaw. Fungal spore attachment to substrata. Fungal Biology Reviews, 41, 2-9 (2022). https://doi.org/10.1016/j.fbr.2022.03.002

62. K. Chittem, M.F.R. Khan & R.S. Goswami. Efficacy of precipitated calcium carbonate in managing fusarium root rot of field pea. Phytoparasitica, 44, 295–303 (2016). https://doi.org/10.1007/s12600-016-0528-z

63. X. Li, C. Zhang & L. Lu. Fungal calcineurin complex as an antifungal target: From past to present to future. Fungal Biology Reviews, 43, 100290 (2023). https://doi.org/10.1016/j.fbr.2022.10.003

64. R. Ancuceanu, M.V. Hovaneț, M. Cojocaru-Toma, A.I. Anghel & M. Dinu. Potential antifungal targets for Aspergillus sp. from the calcineurin and heat shock protein pathways. International Journal of Molecular Sciences, 23(20), 12543 (2022). https://doi.org/10.3390/ijms232012543

65. L. Chevalier, M. Pinar, R. Le Borgne, C. Durieu, M. A. Peñalva, A. Boudaoud & N. Minc. Cell wall dynamics stabilize tip growth in a filamentous fungus. PLoS Biology, 21(1), e3001981 (2023). https://doi.org/10.1371/journal.pbio.3001981

66. H. Chen, X. Zhou, B. Ren & L. Cheng. The regulation of hyphae growth in Candida albicans. Virulence, 11(1), 337–348 (2020). https://doi.org/10.1080/21505594.2020.1748930

67. R.W. Roberson. Subcellular structure and behaviour in fungal hyphae. Journal of Microscopy, 280(2), 75–85 (2020). https://doi.org/10.1111/jmi.12945

68. T. Gao, L. Shi, T. Zhang, A. Ren, A. Jiang, H. Yu & M. Zhao. Cross talk between calcium and reactive oxygen species regulates hyphal branching and ganoderic acid biosynthesis in Ganoderma lucidum under copper stress. Applied and Environmental Microbiology, 84(13), e00438-18 (2018). https://doi.org/10.1128/aem.00438-18

69. N. Takeshita, M. Evangelinos, L. Zhou, T. Serizawa, R.A. Somera-Fajardo, L. Lu, N. Takaya, G.U. Nienhaus & R. Fischer. Pulses of Ca2+ coordinate actin assembly and exocytosis for stepwise cell extension. Proceedings of the National Academy of Sciences of the United States of America. 114(22), 5701– 5706 (2017). https://doi.org/10.1073/pnas.1700204114

70. H.S. Park, E.W. Chow, C. Fu, E.J. Soderblom, M.A. Moseley, J. Heitman & M.E. Cardenas. Calcineurin targets involved in stress survival and fungal virulence. PLoS Pathogens, 12(9), e1005873 (2016). https://doi.org/10.1371/journal.ppat.1005873

71. P.R. Juvvadi & W.J. Steinbach. Calcineurin orchestrates hyphal growth, septation, drug resistance and pathogenesis of Aspergillus fumigatus: Where do we go from here? Pathogens (Basel, Switzerland), 4(4), 883–893 (2015). https://doi.org/10.3390/pathogens4040883

72. Y. Ishitsuka, N. Savage, Y. Li, A. Bergs, N. Grün, D. Kohler, R. Donnelly, G.U. Nienhaus, R. Fischer & N. Takeshita. Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth. Science Advances, 1(10), e1500947 (2015). https://doi.org/10.1126/sciadv.1500947

73. N. Takeshita. Coordinated process of polarized growth in filamentous fungi. Bioscience, Biotechnology & Biochemistry, 80(9), 1693–1699 (2016). https://doi.org/10.1080/09168451.2016.1179092

74. L. Zhou, M. Evangelinos, V. Wernet, A.F. Eckert, Y. Ishitsuka, R. Fischer, G.U. Nienhaus & N. Takeshita. Superresolution and pulse-chase imaging reveal the role of vesicle transport in polar growth of fungal cells. Science Advances, 4(1), e1701798 (2018). https://doi.org/10.1126/sciadv.1701798

75. Q. Yu, T. Ma, C. Ma, B. Zhang & M. Li. Multifunction of the ER P-type calcium pump Spf1 during hyphal development in Candida albicans. Mycopathologia, 184 ,573–583 (2019). https://doi.org/10.1007/s11046-019-00372-5

76. P. Zheng, T.A. Nguyen, J.Y. Wong, M. Lee, T.A. Nguyen, J.S. Fan, D. Yang & G. Jedd. Spitzenkörper assembly mechanisms reveal conserved features of fungal and metazoan polarity scaffolds. Nature Communications, 11(1), 2830 (2020). https://doi.org/10.1038/s41467-020-16712-9

77. H.-C. Flemming, E.D. van Hullebusch, T.R. Neu, P.H. Nielsen, T. Seviour, P. Stoodley, J. Wingender & S. Wuertz. The biofilm matrix: multitasking in a shared space. Nature Reviews: Microbiology, 21, 70–86 (2023). https://doi.org/10.1038/s41579-022-00791-0

78. C.B. Costa-Orlandi, J.C.O. Sardi, N.S. Pitangui, H.C. Oliveira, L. Scorzoni, M.C. Galeane, et al. Fungal biofilms and polymicrobial diseases. Journal of Fungi (Basel, Switzerland), 3(2), 22 (2017). https://doi.org/10.3390/jof3020022

79. J.F. Kernien, B.D. Snarr, D.C. Sheppard & J.E. Nett. The interface between fungal biofilms and innate immunity. Frontiers in Immunology, 8, 1968 (2018). https://doi.org/10.3389/fimmu.2017.01968

80. C.J. Lin, C. Sasse, J. Gerke, O. Valerius, H. Irmer, H. Frauendorf, et al. Transcription factor SomA is required for adhesion, development and virulence of the human pathogen Aspergillus fumigatus. PLoS Pathogens, 11(11), e1005205 (2015). https://doi.org/10.1371/journal.ppat.1005205

81. V.E. Glazier, J.N. Kaur, N.T. Brown, A.A. Rivera & J.C. Panepinto. Puf4 regulates both splicing and decay of HXL1 mRNA encoding the unfolded protein response transcription factor in Cryptococcus neoformans. Eukaryotic Cell, 14(4), 385–395 (2015). https://doi.org/10.1128/ec.00273-14

82. S. Roque, M. Cerciat, I. Gaugué, L. Mora, A.G. Floch, M. Zamaroczy, V. Heurgué-Hamard & S. Kervestin. Interaction between the poly(A)-binding protein Pab1 and the eukaryotic release factor eRF3 regulates translation termination but not mRNA decay in Saccharomyces cerevisiae. RNA (New York, N.Y.), 21, 124–134 (2015). https://doi.org/10.1261/rna.047282.114

83. F. Martani, F. Marano, S. Bertacchi, D. Porro & P. Branduardi. The Saccharomyces cerevisiae poly(A) binding protein Pab1 as a target for eliciting stress tolerant phenotypes. Scientific Reports, 5, 18318 (2015). https://doi.org/10.1038/srep18318

84. Y.-E. Son, C. Fu, W.-H. Jung, S.-H. Oh, J.-H. Kwak, M.E. Cardenas, J. Heitman & H.-S. Park. Pbp1-interacting protein Mkt1 regulates virulence and sexual reproduction in Cryptococcus neoformans. Frontiers in Cellular and Infection Microbiology, 9, 355 (2019). https://doi.org/10.3389/fcimb.2019.00355

85. P.R. Juvvadi, D. Fox, B.G. Bobay, M.J. Hoy, S.M.C. Gobeil, R.A. Venters, et al. Harnessing calcineurin-FK506-FKBP12 crystal structures from invasive fungal pathogens to develop antifungal agents. Nature Communications, 10(1), 4275 (2019). https://doi.org/10.1038/s41467-019-12199-1

86. W. Jia, H. Zhang, C. Li, G. Li, X. Liu & J. Wei. The calcineurin inhibitor cyclosporine A synergistically enhances the susceptibility of Candida albicans biofilms to fluconazole by multiple mechanisms. BMC Microbiology, 16(1), 113 (2016). https://doi.org/10.1186/s12866-016-0728-1

87. T. Wibawa, Nurrokhman, I. Baly, P.R. Daeli, G. Kartasasmita & N. Wijayanti. Cyclosporine A decreases the fluconazole minimum inhibitory concentration of Candida albicans clinical isolates but not biofilm formation and cell growth. Tropical Biomedicine, 32(1), 176-182 (2015). URL: https://www.cabidigitallibrary.org/doi/pdf/10.5555/20153104132

88. F.H. Schopf, M.M. Biebl & J. Bichner. The HSP90 chaperone machinery. Nature Reviews: Molecular Cell Biology, 18(6), 345-360 (2017). https://doi.org/10.1038/nrm.2017.39

89. K. Liao & L. Sun. Roles of the Hsp90-calcineurin pathway in the antifungal activity of honokiol. Journal of Microbiology and Biotechnology, 28(7), 1086–1093 (2018). https://doi.org/10.4014/jmb.1801.01024

Cómo citar

APA

de Andrade Júnior, F. P., Rayanne da Silva, G., de Sousa, V. M. & Araújo Costa, B. (2026). The role of calcium ions and the calcineurin route in fungal virulence: a review. Revista Colombiana de Ciencias Químico-Farmacéuticas, 55(1), 109–123. https://doi.org/10.15446/rcciquifa.v55n1.125068

ACM

[1]
de Andrade Júnior, F.P., Rayanne da Silva, G., de Sousa, V.M. y Araújo Costa, B. 2026. The role of calcium ions and the calcineurin route in fungal virulence: a review. Revista Colombiana de Ciencias Químico-Farmacéuticas. 55, 1 (ene. 2026), 109–123. DOI:https://doi.org/10.15446/rcciquifa.v55n1.125068.

ACS

(1)
de Andrade Júnior, F. P.; Rayanne da Silva, G.; de Sousa, V. M.; Araújo Costa, B. The role of calcium ions and the calcineurin route in fungal virulence: a review. Rev. Colomb. Cienc. Quím. Farm. 2026, 55, 109-123.

ABNT

DE ANDRADE JÚNIOR, F. P.; RAYANNE DA SILVA, G.; DE SOUSA, V. M.; ARAÚJO COSTA, B. The role of calcium ions and the calcineurin route in fungal virulence: a review. Revista Colombiana de Ciencias Químico-Farmacéuticas, [S. l.], v. 55, n. 1, p. 109–123, 2026. DOI: 10.15446/rcciquifa.v55n1.125068. Disponível em: https://revistas.unal.edu.co/index.php/rccquifa/article/view/125068. Acesso em: 30 ene. 2026.

Chicago

de Andrade Júnior, Francisco Patricio, Gleice Rayanne da Silva, Valgrícia Matias de Sousa, y Bagnólia Araújo Costa. 2026. «The role of calcium ions and the calcineurin route in fungal virulence: a review». Revista Colombiana De Ciencias Químico-Farmacéuticas 55 (1):109-23. https://doi.org/10.15446/rcciquifa.v55n1.125068.

Harvard

de Andrade Júnior, F. P., Rayanne da Silva, G., de Sousa, V. M. y Araújo Costa, B. (2026) «The role of calcium ions and the calcineurin route in fungal virulence: a review», Revista Colombiana de Ciencias Químico-Farmacéuticas, 55(1), pp. 109–123. doi: 10.15446/rcciquifa.v55n1.125068.

IEEE

[1]
F. P. de Andrade Júnior, G. Rayanne da Silva, V. M. de Sousa, y B. Araújo Costa, «The role of calcium ions and the calcineurin route in fungal virulence: a review», Rev. Colomb. Cienc. Quím. Farm., vol. 55, n.º 1, pp. 109–123, ene. 2026.

MLA

de Andrade Júnior, F. P., G. Rayanne da Silva, V. M. de Sousa, y B. Araújo Costa. «The role of calcium ions and the calcineurin route in fungal virulence: a review». Revista Colombiana de Ciencias Químico-Farmacéuticas, vol. 55, n.º 1, enero de 2026, pp. 109-23, doi:10.15446/rcciquifa.v55n1.125068.

Turabian

de Andrade Júnior, Francisco Patricio, Gleice Rayanne da Silva, Valgrícia Matias de Sousa, y Bagnólia Araújo Costa. «The role of calcium ions and the calcineurin route in fungal virulence: a review». Revista Colombiana de Ciencias Químico-Farmacéuticas 55, no. 1 (enero 26, 2026): 109–123. Accedido enero 30, 2026. https://revistas.unal.edu.co/index.php/rccquifa/article/view/125068.

Vancouver

1.
de Andrade Júnior FP, Rayanne da Silva G, de Sousa VM, Araújo Costa B. The role of calcium ions and the calcineurin route in fungal virulence: a review. Rev. Colomb. Cienc. Quím. Farm. [Internet]. 26 de enero de 2026 [citado 30 de enero de 2026];55(1):109-23. Disponible en: https://revistas.unal.edu.co/index.php/rccquifa/article/view/125068

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