Plant and animal calpain functions, association with microtubules and possible medical applications
Main Article Content
Abstract
Calpains are calcium-activated cysteine proteases that activate a vast variety of substrates by cleavage. First reported in 1964, calpains are found in both prokaryotes and eukaryotes and display disparate multidomain architectures. The term calpainopathy was coined in 1995 when calpains were first linked to cell cycle control and cancer, and since then calpains have been implicated in many additional medical conditions including heart disease, multiple sclerosis, diabetes, sickle cell disease, and various neurological disorders. The evolution of calpains is under active investigation, but the core CysPc cysteine protease domain can be traced back to bacteria and the membrane associated MIT domain to Archaea. Here we review calpain evolution and suggest that the MIT-CysPc domain was present in the first eukaryotic common ancestor, and that this diverged into a minimum of four independent last eukaryotic common ancestors making up diverse groups from animals to land and marine plants. How calpains function at the cellular level is likewise not fully resolved. However, they are recognized to play roles in cell division, adhesion, fusion, proliferation, migration and signaling in animals and to act on stem cell functions via microtubules in land plants. Just recently calpains have also been connected to the microtubule organizing center in land plants and brown algae. We present a possible basic function of calpain domains, their connections to membranes and a possible calcium channel, supported by an updated phylogeny. Finally, we provide an overview of human calpains, potential functions and medical conditions to which they are linked and suggest possible development of calpain transcriptomic diagnostics to increase medical precision and treatment. We believe that understanding calpains has promising medical spinoffs and look forward to seeing this field unfold in the years to come.
Keywords:
Calpain, calcium, cell division, microtubule, disease, cancer
Article Details
How to Cite
OPSAHL-SORTEBERG, Hilde Gunn et al.
Plant and animal calpain functions, association with microtubules and possible medical applications.
Medical Research Archives, [S.l.], v. 12, n. 9, sep. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5639>. Date accessed: 22 dec. 2024.
doi: https://doi.org/10.18103/mra.v12i9.5639.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Murachi T, Tanaka K, Hatanaka M, Murakami T. Intracellular Ca2+-dependent protease (calpain) and its high-molecular-weight endogenous inhibitor (calpastatin). Advances in enzyme regulation. 1981;19:407-424.
2. Nian H, Ma B. Calpain–calpastatin system and cancer progression. Biological Reviews. 2021;96(3):961-975.
3. Spinozzi S, Albini S, Best H, Richard I. Calpains for dummies: What you need to know about the calpain family. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics. 2021;1869(5):140616.
4. Sorimachi H, Hata S, Ono Y. Calpain chronicle—an enzyme family under multidisciplinary characterization. Proceedings of the Japan Academy, Series B. 2011;87(6):287-327.
5. Hosfield CM, Elce JS, Davies PL, Jia Z. Crystal structure of calpain reveals the structural basis for Ca2+‐dependent protease activity and a novel mode of enzyme activation. The EMBO journal. 1999;
6. Strobl S, Fernandez-Catalan C, Braun M, et al. The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium. Proceedings of the National Academy of Sciences. 2000;97(2):588-592.
7. Rawlings ND. Bacterial calpains and the evolution of the calpain (C2) family of peptidases. Biology Direct. 2015;10:1-12.
8. Vešelényiová D, Hutárová L, Lukáčová A, Schneiderová M, Vesteg M, Krajčovič J. Calpains in cyanobacteria and the origin of calpains. Scientific Reports. 2022;12(1):13872.
9. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev. Jul 2003;83(3):731-801. doi:10.1152/physrev.00029.2002
10. Zhao S, Liang Z, Demko V, et al. Massive expansion of the calpain gene family in unicellular eukaryotes. BMC Evol Biol. Sep 29 2012;12:193. doi:10.1186/1471-2148-12-193
11. Lid SE, Gruis D, Jung R, et al. The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proceedings of the National Academy of Sciences. 2002;99(8):5460-5465.
12. Denoeud F, Godfroy O, Cruaud C, et al. Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems. bioRxiv. 2024:2024.02. 19.579948.
13. Liang Z, Brown RC, Fletcher JC, Opsahl-Sorteberg H-G. Calpain-Mediated Positional Information Directs Cell Wall Orientation to Sustain Plant Stem Cell Activity, Growth and Development. Plant and Cell Physiology. 2015;56(9):1855-1866. doi:10.1093/pcp/pcv110
14. Liang Z, Demko V, Wilson RC, et al. The catalytic domain CysPc of the DEK 1 calpain is functionally conserved in land plants. The Plant Journal. 2013;75(5):742-754.
15. Araujo H, Julio A, Cardoso M. Translating genetic, biochemical and structural information to the calpain view of development. Mechanisms of Development. 2018;154:240-250.
16. Šafranek M, Shumbusho A, Johansen W, et al. Membrane-anchored calpains–hidden regulators of growth and development beyond plants? Frontiers in Plant Science. 2023;14:1289785.
17. Jékely G, Friedrich P. Characterization of two recombinant Drosophila calpains: CALPA and a novel homolog, CALPB. Journal of Biological Chemistry. 1999;274(34):23893-23900.
18. Wang C, Barry JK, Min Z, Tordsen G, Rao AG, Olsen O-A. The calpain domain of the maize DEK1 protein contains the conserved catalytic triad and functions as a cysteine proteinase. Journal of Biological Chemistry. 2003;278(36):34467-34474.
19. Gibbons IR, Rowe AJ. Dynein: a protein with adenosine triphosphatase activity from cilia. Science. 1965;149(3682):424-426.
20. Tran D, Galletti R, Neumann ED, et al. A mechanosensitive Ca2+ channel activity is dependent on the developmental regulator DEK1. Nature Communications. 2017;8(1):1009.
21. Kaczmarek JS, Riccio A, Clapham DE. Calpain cleaves and activates the TRPC5 channel to participate in semaphorin 3A-induced neuronal growth cone collapse. Proceedings of the National Academy of Sciences. 2012;109(20):7888-7892.
22. Arias-Darraz L, Cabezas D, Colenso CK, et al. A transient receptor potential ion channel in Chlamydomonas shares key features with sensory transduction-associated TRP channels in mammals. The Plant Cell. 2015;27(1):177-188.
23. Owsianik G, D'hoedt D, Voets T, Nilius B. Structure–function relationship of the TRP channel superfamily. Reviews of physiology, biochemistry and pharmacology. 2006:61-90.
24. Hellwig N, Albrecht N, Harteneck C, Schultz Gn, Schaefer M. Homo-and heteromeric assembly of TRPV channel subunits. Journal of cell science. 2005;118(5):917-928.
25. Himmel NJ, Cox DN. Transient receptor potential channels: current perspectives on evolution, structure, function and nomenclature. Proceedings of the Royal Society B. 2020;287(1933):20201309.
26. Lid SE, Olsen L, Nestestog R, et al. Mutation in the Arabidopisis thaliana DEK1 calpain gene perturbs endosperm and embryo development while over-expression affects organ development globally. Planta. 2005;221:339-351.
27. Tian Q, Olsen L, Sun B, et al. Subcellular localization and functional domain studies of DEFECTIVE KERNEL 1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. The Plant Cell. 2007;19(10):3127-3145. doi:10.1105/tpc.106.048868
28. Perroud PF, Demko V, Johansen W, Wilson RC, Olsen OA, Quatrano RS. Defective Kernel 1 (DEK 1) is required for three‐dimensional growth in P hyscomitrella patens. New Phytologist. 2014;203(3):794-804.
29. Liu Y, Li X, Zhao J, et al. Direct evidence that suspensor cells have embryogenic potential that is suppressed by the embryo proper during normal embryogenesis. Proc Natl Acad Sci U S A. Oct 6 2015;112(40):12432-7. doi:10.1073/pnas.1508651112
30. Friml J, Vieten A, Sauer M, et al. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature. 2003;426(6963):147-153.
31. Perroud PF, Meyberg R, Demko V, Quatrano RS, Olsen OA, Rensing SA. DEK1 displays a strong subcellular polarity during Physcomitrella patens 3D growth. New phytologist. 2020;226(4):1029-1041.
32. Yan Y, Sun Z, Yan P, Wang T, Zhang Y. Mechanical regulation of cortical microtubules in plant cells. New Phytologist. 2023;239(5):1609-1621.
33. Jánossy J, Ubezio P, Apáti Á, Magócsi M, Tompa P, Friedrich P. Calpain as a multi-site regulator of cell cycle. Biochemical pharmacology. 2004;67(8):1513-1521.
34. Franco SJ, Huttenlocher A. Regulating cell migration: calpains make the cut. Journal of cell science. 2005;118(17):3829-3838.
35. Santos DM, Xavier JM, Morgado AL, Sola S, Rodrigues CM. Distinct regulatory functions of calpain 1 and 2 during neural stem cell self-renewal and differentiation. PloS one. 2012;7(3):e33468.
36. Potz BA, Abid MR, Sellke FW. Role of calpain in pathogenesis of human disease processes. Journal of nature and science. 2016;2(9)
37. Shapovalov I, Harper D, Greer PA. Calpain as a therapeutic target in cancer. Expert Opinion on Therapeutic Targets. 2022;26(3):217-231.
38. Ferreira A. Calpain dysregulation in Alzheimer’s disease. International Scholarly Research Notices. 2012;2012
39. Mahaman YAR, Huang F, Wu M, et al. Moringa oleifera alleviates homocysteine-induced Alzheimer’s disease-like pathology and cognitive impairments. Journal of Alzheimer's Disease. 2018;63(3):1141-1159.
40. Shams R, Banik NL, Haque A. Calpain in the cleavage of alpha-synuclein and the pathogenesis of Parkinson's disease. Progress in molecular biology and translational science. 2019;167:107-124.
41. Gafni J, Ellerby LM. Calpain activation in Huntington's disease. Journal of Neuroscience. 2002;22(12):4842-4849.
42. Rao SS, Mu Q, Zeng Y, et al. Calpain‐activated mTORC2/Akt pathway mediates airway smooth muscle remodelling in asthma. Clinical & Experimental Allergy. 2017;47(2):176-189.
43. Tabata C, Tabata R, Nakano T. The calpain inhibitor calpeptin prevents bleomycin-induced pulmonary fibrosis in mice. Clinical & Experimental Immunology. 2010;162(3):560-567.
44. Ono Y, Saido TC, Sorimachi H. Calpain research for drug discovery: challenges and potential. Nature Reviews Drug Discovery. 2016;15(12):854-876.
45. Carafori E. Calpain: a protease in search of a function? Biochem Biophys Res Commun. 1998;247:193-203.
46. Azam M, Andrabi SS, Sahr KE, Kamath L, Kuliopulos A, Chishti AH. Disruption of the mouse μ-calpain gene reveals an essential role in platelet function. Molecular and cellular biology. 2001;21(6):2213-2220.
47. Gan-Or Z, Bouslam N, Birouk N, et al. Mutations in CAPN1 cause autosomal-recessive hereditary spastic paraplegia. The American Journal of Human Genetics. 2016;98(5):1038-1046.
48. Smith AW, Das A, Guyton MK, Ray SK, Rohrer B, Banik NL. Calpain inhibition attenuates apoptosis of retinal ganglion cells in acute optic neuritis. Investigative Ophthalmology & Visual Science. 2011;52(7):4935-4941.
49. Wang KK. Calpain and caspase: can you tell the difference? Trends in neurosciences. 2000;23(1):20-26.
50. Wang Y, Liu Y, Bi X, Baudry M. Calpain-1 and calpain-2 in the brain: new evidence for a critical role of calpain-2 in neuronal death. Cells. 2020;9(12):2698.
51. Morton JD, Lee HY, McDermott JD, et al. A macrocyclic calpain inhibitor slows the development of inherited cortical cataracts in a sheep model. Investigative ophthalmology & visual science. 2013;54(1):389-395.
52. Huang Y, Wang KK. The calpain family and human disease. Trends in molecular medicine. 2001;7(8):355-362.
53. Conze C, Rierola M, Trushina NI, et al. Caspase-cleaved tau is senescence-associated and induces a toxic gain of function by putting a brake on axonal transport. Molecular psychiatry. 2022;27(7):3010-3023.
54. Azuma M, Fukiage C, David L, Shearer T. Activation of calpain in lens: a review and proposed mechanism. Experimental eye research. 1997;64(4):529-538.
55. Richard I, Broux O, Allamand V, et al. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell. 1995;81(1):27-40.
56. Sorimachi H, Imajoh-Ohmi S, Emori Y, et al. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m-and μ-types: specific expression of the mRNA in skeletal muscle. Journal of Biological Chemistry. 1989;264(33):20106-20111.
57. Moretti D, Del Bello B, Allavena G, Corti A, Signorini C, Maellaro E. Calpain-3 impairs cell proliferation and stimulates oxidative stress-mediated cell death in melanoma cells. PloS one. 2015;10(2):e0117258.
58. Roperto S, De Tullio R, Raso C, et al. Calpain3 is expressed in a proteolitically active form in papillomavirus-associated urothelial tumors of the urinary bladder in cattle. PLoS One. 2010;5(4):e10299.
59. Kramerova I, Kudryashova E, Wu B, Ottenheijm C, Granzier H, Spencer MJ. Novel role of calpain-3 in the triad-associated protein complex regulating calcium release in skeletal muscle. Human molecular genetics. 2008;17(21):3271-3280.
60. Peng P, Wu W, Zhao J, et al. Decreased expression of Calpain-9 predicts unfavorable prognosis in patients with gastric cancer. Scientific reports. 2016;6(1):29604.
61. Matena K, Boehm T, Dear TN. Genomic organization of mouse Capn5 and Capn6 Genes confirms that they are a distinct calpain subfamily. Genomics. 1998;48(1):117-120.
62. Franz T, Vingron M, Boehm T, Dear TN. Capn7: a highly divergent vertebrate calpain with a novel C-terminal domain. Mammalian genome. 1999;10:318-321.
63. Paine EL, Skalicky JJ, Whitby FG, et al. The Calpain-7 protease functions together with the ESCRT-III protein IST1 within the midbody to regulate the timing and completion of abscission. bioRxiv. 2022:2022.10.18.512775. doi:10.1101/2022.10.18.512775
64. Storr SJ, Carragher NO, Frame MC, Parr T, Martin SG. The calpain system and cancer. Nature Reviews Cancer. 2011;11(5):364-374.
65. Tang PH, Chemudupati T, Wert KJ, et al. Phenotypic variance in Calpain-5 retinal degeneration. American journal of ophthalmology case reports. 2020;18:100627.
66. Frances CP, Conde MC, Saez ME, et al. Identification of a protective haplogenotype within CAPN10 gene influencing colorectal cancer susceptibility. Journal of gastroenterology and hepatology. 2007;22(12):2298-2302.
67. Fong P-y, Fesinmeyer MD, White E, et al. Association of diabetes susceptibility gene calpain-10 with pancreatic cancer among smokers. Journal of gastrointestinal cancer. 2010;41:203-208.
68. Horikawa Y, Oda N, Cox NJ, et al. Genetic variation in the gene encoding calpain-10 is associated with type 2 diabetes mellitus. Nature genetics. 2000;26(2):163-175.
69. Liu X, Schnellmann RG. Calpain mediates progressive plasma membrane permeability and proteolysis of cytoskeleton-associated paxillin, talin, and vinculin during renal cell death. Journal of Pharmacology and Experimental Therapeutics. 2003;304(1):63-70.
70. Frangié C, Zhang W, Perez J, Dubois Y-CX, Haymann J-P, Baud L. Extracellular calpains increase tubular epithelial cell mobility: implications for kidney repair after ischemia. Journal of biological chemistry. 2006;281(36):26624-26632.
71. Liu K, Li L, Cohen SN. Antisense RNA-mediated deficiency of the calpain protease, nCL-4, in NIH3T3 cells is associated with neoplastic transformation and tumorigenesis. Journal of Biological Chemistry. 2000;275(40):31093-31098.
72. Shiba E, Kambayashi J-I, Sakon M, et al. Ca 2+-dependent neutral protease (Calpain) activity in breast cancer tissue and estrogen receptor status. Breast Cancer. 1996;3:13-17.
73. Kulkarni S, Reddy K, Esteva F, Moore H, Budd G, Tubbs R. Calpain regulates sensitivity to trastuzumab and survival in HER2-positive breast cancer. Oncogene. 2010;29(9):1339-1350.
74. Hong JY, Park SY, Kim Y, Lee CY, Lee MG. Calpain and spectrin breakdown products as potential biomarkers in tuberculous pleural effusion. Journal of Thoracic Disease. 2018;10(5):2558.
75. Kunišek L, Ilijaš KM, Medved I, et al. Cardiomyocytes calpain 2 expression: Diagnostic forensic marker for sudden cardiac death caused by early myocardial ischemia and an indicator of the duration of myocardial agonal period? Medical hypotheses. 2022;158:110738.
76. Farmer LK, Rollason R, Whitcomb DJ, et al. TRPC6 binds to and activates calpain, independent of its channel activity, and regulates podocyte cytoskeleton, cell adhesion, and motility. Journal of the American Society of Nephrology. 2019;30(10):1910-1924.
77. Lasserre R, Alcover A. Cytoskeletal cross-talk in the control of T cell antigen receptor signaling. FEBS letters. 2010;584(24):4845-4850.
78. Conacci-Sorrell M, Ngouenet C, Eisenman RN. Myc-nick: a cytoplasmic cleavage product of Myc that promotes α-tubulin acetylation and cell differentiation. Cell. 2010;142(3):480-493.
79. Leloup L, Wells A. Calpains as potential anti-cancer targets. Expert opinion on therapeutic targets. 2011;15(3):309-323.
80. García-Trevijano ER, Ortiz-Zapater E, Gimeno A, Viña JR, Zaragozá R. Calpains, the proteases of two faces controlling the epithelial homeostasis in mammary gland. Frontiers in Cell and Developmental Biology. 2023;11:1249317.
81. Pardo-Pastor C, Rubio-Moscardo F, Vogel-González M, et al. Piezo2 channel regulates RhoA and actin cytoskeleton to promote cell mechanobiological responses. Proceedings of the National Academy of Sciences. 2018;115(8):1925-1930.
82. Fernández LR. Subcellular Distribution of Calpain-1 and Calpain-2 as a Key Event for Calpain-mediated Functions in Physiological and Neoplastic Mammary Models. Universitat de València. Facultat de Ciències Biològiques.; 2019.
83. Demarchi F, Bertoli C, Greer P, Schneider C. Ceramide triggers an NF-κB-dependent survival pathway through calpain. Cell Death & Differentiation. 2005;12(5):512-522.
84. Li C, Chen S, Yue P, et al. Proteasome inhibitor PS-341 (bortezomib) induces calpain-dependent IκBα degradation. Journal of Biological Chemistry. 2010;285(21):16096-16104.
85. Carragher NO. Calpain inhibition: a therapeutic strategy targeting multiple disease states. Current pharmaceutical design. 2006;12(5):615-638.
86. Dong B, Liu R. Characterization of endogenous and recombinant human calpain-10. Biochimie. 2008;90(9):1362-1371.
87. Pánico P, Salazar AM, Burns AL, Ostrosky-Wegman P. Role of calpain-10 in the development of diabetes mellitus and its complications. Archives of medical research. 2014;45(2):103-115.
88. Ben‐Aharon I, Brown PR, Shalgi R, Eddy EM. Calpain 11 is unique to mouse spermatogenic cells. Molecular Reproduction and Development: Incorporating Gamete Research. 2006;73(6):767-773.
89. Charlton R, Henderson M, Richards J, et al. Immunohistochemical analysis of calpain 3: advantages and limitations in diagnosing LGMD2A. Neuromuscular Disorders. 2009;19(7):449-457.
90. Hauerslev S, Sveen M-L, Duno M, Angelini C, Vissing J, Krag TO. Calpain 3 is important for muscle regeneration: evidence from patients with limb girdle muscular dystrophies. BMC Musculoskeletal Disorders. 2012;13:1-11.
91. Mahajan VB, Skeie JM, Bassuk AG, et al. Calpain-5 mutations cause autoimmune uveitis, retinal neovascularization, and photoreceptor degeneration. PLoS Genetics 2012; 8(10): e1003001.
92. Turner MD, Cassell PG, Hitman GA. Calpain‐10: from genome search to function. Diabetes/metabolism research and reviews. 2005;21(6):505-514.
93. Zha C, Farah CA, Holt RJ, et al. Biallelic variants in the small optic lobe calpain CAPN15 are associated with congenital eye anomalies, deafness and other neurodevelopmental deficits. Human molecular genetics. 2020;29(18):3054-3063.
94. Litosh VA, Rochman M, Rymer JK, Porollo A, Kottyan LC, Rothenberg ME. Calpain-14 and its association with eosinophilic esophagitis. Journal of Allergy and Clinical Immunology. 2017;139(6):1762-1771. e7.
2. Nian H, Ma B. Calpain–calpastatin system and cancer progression. Biological Reviews. 2021;96(3):961-975.
3. Spinozzi S, Albini S, Best H, Richard I. Calpains for dummies: What you need to know about the calpain family. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics. 2021;1869(5):140616.
4. Sorimachi H, Hata S, Ono Y. Calpain chronicle—an enzyme family under multidisciplinary characterization. Proceedings of the Japan Academy, Series B. 2011;87(6):287-327.
5. Hosfield CM, Elce JS, Davies PL, Jia Z. Crystal structure of calpain reveals the structural basis for Ca2+‐dependent protease activity and a novel mode of enzyme activation. The EMBO journal. 1999;
6. Strobl S, Fernandez-Catalan C, Braun M, et al. The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium. Proceedings of the National Academy of Sciences. 2000;97(2):588-592.
7. Rawlings ND. Bacterial calpains and the evolution of the calpain (C2) family of peptidases. Biology Direct. 2015;10:1-12.
8. Vešelényiová D, Hutárová L, Lukáčová A, Schneiderová M, Vesteg M, Krajčovič J. Calpains in cyanobacteria and the origin of calpains. Scientific Reports. 2022;12(1):13872.
9. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev. Jul 2003;83(3):731-801. doi:10.1152/physrev.00029.2002
10. Zhao S, Liang Z, Demko V, et al. Massive expansion of the calpain gene family in unicellular eukaryotes. BMC Evol Biol. Sep 29 2012;12:193. doi:10.1186/1471-2148-12-193
11. Lid SE, Gruis D, Jung R, et al. The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proceedings of the National Academy of Sciences. 2002;99(8):5460-5465.
12. Denoeud F, Godfroy O, Cruaud C, et al. Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems. bioRxiv. 2024:2024.02. 19.579948.
13. Liang Z, Brown RC, Fletcher JC, Opsahl-Sorteberg H-G. Calpain-Mediated Positional Information Directs Cell Wall Orientation to Sustain Plant Stem Cell Activity, Growth and Development. Plant and Cell Physiology. 2015;56(9):1855-1866. doi:10.1093/pcp/pcv110
14. Liang Z, Demko V, Wilson RC, et al. The catalytic domain CysPc of the DEK 1 calpain is functionally conserved in land plants. The Plant Journal. 2013;75(5):742-754.
15. Araujo H, Julio A, Cardoso M. Translating genetic, biochemical and structural information to the calpain view of development. Mechanisms of Development. 2018;154:240-250.
16. Šafranek M, Shumbusho A, Johansen W, et al. Membrane-anchored calpains–hidden regulators of growth and development beyond plants? Frontiers in Plant Science. 2023;14:1289785.
17. Jékely G, Friedrich P. Characterization of two recombinant Drosophila calpains: CALPA and a novel homolog, CALPB. Journal of Biological Chemistry. 1999;274(34):23893-23900.
18. Wang C, Barry JK, Min Z, Tordsen G, Rao AG, Olsen O-A. The calpain domain of the maize DEK1 protein contains the conserved catalytic triad and functions as a cysteine proteinase. Journal of Biological Chemistry. 2003;278(36):34467-34474.
19. Gibbons IR, Rowe AJ. Dynein: a protein with adenosine triphosphatase activity from cilia. Science. 1965;149(3682):424-426.
20. Tran D, Galletti R, Neumann ED, et al. A mechanosensitive Ca2+ channel activity is dependent on the developmental regulator DEK1. Nature Communications. 2017;8(1):1009.
21. Kaczmarek JS, Riccio A, Clapham DE. Calpain cleaves and activates the TRPC5 channel to participate in semaphorin 3A-induced neuronal growth cone collapse. Proceedings of the National Academy of Sciences. 2012;109(20):7888-7892.
22. Arias-Darraz L, Cabezas D, Colenso CK, et al. A transient receptor potential ion channel in Chlamydomonas shares key features with sensory transduction-associated TRP channels in mammals. The Plant Cell. 2015;27(1):177-188.
23. Owsianik G, D'hoedt D, Voets T, Nilius B. Structure–function relationship of the TRP channel superfamily. Reviews of physiology, biochemistry and pharmacology. 2006:61-90.
24. Hellwig N, Albrecht N, Harteneck C, Schultz Gn, Schaefer M. Homo-and heteromeric assembly of TRPV channel subunits. Journal of cell science. 2005;118(5):917-928.
25. Himmel NJ, Cox DN. Transient receptor potential channels: current perspectives on evolution, structure, function and nomenclature. Proceedings of the Royal Society B. 2020;287(1933):20201309.
26. Lid SE, Olsen L, Nestestog R, et al. Mutation in the Arabidopisis thaliana DEK1 calpain gene perturbs endosperm and embryo development while over-expression affects organ development globally. Planta. 2005;221:339-351.
27. Tian Q, Olsen L, Sun B, et al. Subcellular localization and functional domain studies of DEFECTIVE KERNEL 1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. The Plant Cell. 2007;19(10):3127-3145. doi:10.1105/tpc.106.048868
28. Perroud PF, Demko V, Johansen W, Wilson RC, Olsen OA, Quatrano RS. Defective Kernel 1 (DEK 1) is required for three‐dimensional growth in P hyscomitrella patens. New Phytologist. 2014;203(3):794-804.
29. Liu Y, Li X, Zhao J, et al. Direct evidence that suspensor cells have embryogenic potential that is suppressed by the embryo proper during normal embryogenesis. Proc Natl Acad Sci U S A. Oct 6 2015;112(40):12432-7. doi:10.1073/pnas.1508651112
30. Friml J, Vieten A, Sauer M, et al. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature. 2003;426(6963):147-153.
31. Perroud PF, Meyberg R, Demko V, Quatrano RS, Olsen OA, Rensing SA. DEK1 displays a strong subcellular polarity during Physcomitrella patens 3D growth. New phytologist. 2020;226(4):1029-1041.
32. Yan Y, Sun Z, Yan P, Wang T, Zhang Y. Mechanical regulation of cortical microtubules in plant cells. New Phytologist. 2023;239(5):1609-1621.
33. Jánossy J, Ubezio P, Apáti Á, Magócsi M, Tompa P, Friedrich P. Calpain as a multi-site regulator of cell cycle. Biochemical pharmacology. 2004;67(8):1513-1521.
34. Franco SJ, Huttenlocher A. Regulating cell migration: calpains make the cut. Journal of cell science. 2005;118(17):3829-3838.
35. Santos DM, Xavier JM, Morgado AL, Sola S, Rodrigues CM. Distinct regulatory functions of calpain 1 and 2 during neural stem cell self-renewal and differentiation. PloS one. 2012;7(3):e33468.
36. Potz BA, Abid MR, Sellke FW. Role of calpain in pathogenesis of human disease processes. Journal of nature and science. 2016;2(9)
37. Shapovalov I, Harper D, Greer PA. Calpain as a therapeutic target in cancer. Expert Opinion on Therapeutic Targets. 2022;26(3):217-231.
38. Ferreira A. Calpain dysregulation in Alzheimer’s disease. International Scholarly Research Notices. 2012;2012
39. Mahaman YAR, Huang F, Wu M, et al. Moringa oleifera alleviates homocysteine-induced Alzheimer’s disease-like pathology and cognitive impairments. Journal of Alzheimer's Disease. 2018;63(3):1141-1159.
40. Shams R, Banik NL, Haque A. Calpain in the cleavage of alpha-synuclein and the pathogenesis of Parkinson's disease. Progress in molecular biology and translational science. 2019;167:107-124.
41. Gafni J, Ellerby LM. Calpain activation in Huntington's disease. Journal of Neuroscience. 2002;22(12):4842-4849.
42. Rao SS, Mu Q, Zeng Y, et al. Calpain‐activated mTORC2/Akt pathway mediates airway smooth muscle remodelling in asthma. Clinical & Experimental Allergy. 2017;47(2):176-189.
43. Tabata C, Tabata R, Nakano T. The calpain inhibitor calpeptin prevents bleomycin-induced pulmonary fibrosis in mice. Clinical & Experimental Immunology. 2010;162(3):560-567.
44. Ono Y, Saido TC, Sorimachi H. Calpain research for drug discovery: challenges and potential. Nature Reviews Drug Discovery. 2016;15(12):854-876.
45. Carafori E. Calpain: a protease in search of a function? Biochem Biophys Res Commun. 1998;247:193-203.
46. Azam M, Andrabi SS, Sahr KE, Kamath L, Kuliopulos A, Chishti AH. Disruption of the mouse μ-calpain gene reveals an essential role in platelet function. Molecular and cellular biology. 2001;21(6):2213-2220.
47. Gan-Or Z, Bouslam N, Birouk N, et al. Mutations in CAPN1 cause autosomal-recessive hereditary spastic paraplegia. The American Journal of Human Genetics. 2016;98(5):1038-1046.
48. Smith AW, Das A, Guyton MK, Ray SK, Rohrer B, Banik NL. Calpain inhibition attenuates apoptosis of retinal ganglion cells in acute optic neuritis. Investigative Ophthalmology & Visual Science. 2011;52(7):4935-4941.
49. Wang KK. Calpain and caspase: can you tell the difference? Trends in neurosciences. 2000;23(1):20-26.
50. Wang Y, Liu Y, Bi X, Baudry M. Calpain-1 and calpain-2 in the brain: new evidence for a critical role of calpain-2 in neuronal death. Cells. 2020;9(12):2698.
51. Morton JD, Lee HY, McDermott JD, et al. A macrocyclic calpain inhibitor slows the development of inherited cortical cataracts in a sheep model. Investigative ophthalmology & visual science. 2013;54(1):389-395.
52. Huang Y, Wang KK. The calpain family and human disease. Trends in molecular medicine. 2001;7(8):355-362.
53. Conze C, Rierola M, Trushina NI, et al. Caspase-cleaved tau is senescence-associated and induces a toxic gain of function by putting a brake on axonal transport. Molecular psychiatry. 2022;27(7):3010-3023.
54. Azuma M, Fukiage C, David L, Shearer T. Activation of calpain in lens: a review and proposed mechanism. Experimental eye research. 1997;64(4):529-538.
55. Richard I, Broux O, Allamand V, et al. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell. 1995;81(1):27-40.
56. Sorimachi H, Imajoh-Ohmi S, Emori Y, et al. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m-and μ-types: specific expression of the mRNA in skeletal muscle. Journal of Biological Chemistry. 1989;264(33):20106-20111.
57. Moretti D, Del Bello B, Allavena G, Corti A, Signorini C, Maellaro E. Calpain-3 impairs cell proliferation and stimulates oxidative stress-mediated cell death in melanoma cells. PloS one. 2015;10(2):e0117258.
58. Roperto S, De Tullio R, Raso C, et al. Calpain3 is expressed in a proteolitically active form in papillomavirus-associated urothelial tumors of the urinary bladder in cattle. PLoS One. 2010;5(4):e10299.
59. Kramerova I, Kudryashova E, Wu B, Ottenheijm C, Granzier H, Spencer MJ. Novel role of calpain-3 in the triad-associated protein complex regulating calcium release in skeletal muscle. Human molecular genetics. 2008;17(21):3271-3280.
60. Peng P, Wu W, Zhao J, et al. Decreased expression of Calpain-9 predicts unfavorable prognosis in patients with gastric cancer. Scientific reports. 2016;6(1):29604.
61. Matena K, Boehm T, Dear TN. Genomic organization of mouse Capn5 and Capn6 Genes confirms that they are a distinct calpain subfamily. Genomics. 1998;48(1):117-120.
62. Franz T, Vingron M, Boehm T, Dear TN. Capn7: a highly divergent vertebrate calpain with a novel C-terminal domain. Mammalian genome. 1999;10:318-321.
63. Paine EL, Skalicky JJ, Whitby FG, et al. The Calpain-7 protease functions together with the ESCRT-III protein IST1 within the midbody to regulate the timing and completion of abscission. bioRxiv. 2022:2022.10.18.512775. doi:10.1101/2022.10.18.512775
64. Storr SJ, Carragher NO, Frame MC, Parr T, Martin SG. The calpain system and cancer. Nature Reviews Cancer. 2011;11(5):364-374.
65. Tang PH, Chemudupati T, Wert KJ, et al. Phenotypic variance in Calpain-5 retinal degeneration. American journal of ophthalmology case reports. 2020;18:100627.
66. Frances CP, Conde MC, Saez ME, et al. Identification of a protective haplogenotype within CAPN10 gene influencing colorectal cancer susceptibility. Journal of gastroenterology and hepatology. 2007;22(12):2298-2302.
67. Fong P-y, Fesinmeyer MD, White E, et al. Association of diabetes susceptibility gene calpain-10 with pancreatic cancer among smokers. Journal of gastrointestinal cancer. 2010;41:203-208.
68. Horikawa Y, Oda N, Cox NJ, et al. Genetic variation in the gene encoding calpain-10 is associated with type 2 diabetes mellitus. Nature genetics. 2000;26(2):163-175.
69. Liu X, Schnellmann RG. Calpain mediates progressive plasma membrane permeability and proteolysis of cytoskeleton-associated paxillin, talin, and vinculin during renal cell death. Journal of Pharmacology and Experimental Therapeutics. 2003;304(1):63-70.
70. Frangié C, Zhang W, Perez J, Dubois Y-CX, Haymann J-P, Baud L. Extracellular calpains increase tubular epithelial cell mobility: implications for kidney repair after ischemia. Journal of biological chemistry. 2006;281(36):26624-26632.
71. Liu K, Li L, Cohen SN. Antisense RNA-mediated deficiency of the calpain protease, nCL-4, in NIH3T3 cells is associated with neoplastic transformation and tumorigenesis. Journal of Biological Chemistry. 2000;275(40):31093-31098.
72. Shiba E, Kambayashi J-I, Sakon M, et al. Ca 2+-dependent neutral protease (Calpain) activity in breast cancer tissue and estrogen receptor status. Breast Cancer. 1996;3:13-17.
73. Kulkarni S, Reddy K, Esteva F, Moore H, Budd G, Tubbs R. Calpain regulates sensitivity to trastuzumab and survival in HER2-positive breast cancer. Oncogene. 2010;29(9):1339-1350.
74. Hong JY, Park SY, Kim Y, Lee CY, Lee MG. Calpain and spectrin breakdown products as potential biomarkers in tuberculous pleural effusion. Journal of Thoracic Disease. 2018;10(5):2558.
75. Kunišek L, Ilijaš KM, Medved I, et al. Cardiomyocytes calpain 2 expression: Diagnostic forensic marker for sudden cardiac death caused by early myocardial ischemia and an indicator of the duration of myocardial agonal period? Medical hypotheses. 2022;158:110738.
76. Farmer LK, Rollason R, Whitcomb DJ, et al. TRPC6 binds to and activates calpain, independent of its channel activity, and regulates podocyte cytoskeleton, cell adhesion, and motility. Journal of the American Society of Nephrology. 2019;30(10):1910-1924.
77. Lasserre R, Alcover A. Cytoskeletal cross-talk in the control of T cell antigen receptor signaling. FEBS letters. 2010;584(24):4845-4850.
78. Conacci-Sorrell M, Ngouenet C, Eisenman RN. Myc-nick: a cytoplasmic cleavage product of Myc that promotes α-tubulin acetylation and cell differentiation. Cell. 2010;142(3):480-493.
79. Leloup L, Wells A. Calpains as potential anti-cancer targets. Expert opinion on therapeutic targets. 2011;15(3):309-323.
80. García-Trevijano ER, Ortiz-Zapater E, Gimeno A, Viña JR, Zaragozá R. Calpains, the proteases of two faces controlling the epithelial homeostasis in mammary gland. Frontiers in Cell and Developmental Biology. 2023;11:1249317.
81. Pardo-Pastor C, Rubio-Moscardo F, Vogel-González M, et al. Piezo2 channel regulates RhoA and actin cytoskeleton to promote cell mechanobiological responses. Proceedings of the National Academy of Sciences. 2018;115(8):1925-1930.
82. Fernández LR. Subcellular Distribution of Calpain-1 and Calpain-2 as a Key Event for Calpain-mediated Functions in Physiological and Neoplastic Mammary Models. Universitat de València. Facultat de Ciències Biològiques.; 2019.
83. Demarchi F, Bertoli C, Greer P, Schneider C. Ceramide triggers an NF-κB-dependent survival pathway through calpain. Cell Death & Differentiation. 2005;12(5):512-522.
84. Li C, Chen S, Yue P, et al. Proteasome inhibitor PS-341 (bortezomib) induces calpain-dependent IκBα degradation. Journal of Biological Chemistry. 2010;285(21):16096-16104.
85. Carragher NO. Calpain inhibition: a therapeutic strategy targeting multiple disease states. Current pharmaceutical design. 2006;12(5):615-638.
86. Dong B, Liu R. Characterization of endogenous and recombinant human calpain-10. Biochimie. 2008;90(9):1362-1371.
87. Pánico P, Salazar AM, Burns AL, Ostrosky-Wegman P. Role of calpain-10 in the development of diabetes mellitus and its complications. Archives of medical research. 2014;45(2):103-115.
88. Ben‐Aharon I, Brown PR, Shalgi R, Eddy EM. Calpain 11 is unique to mouse spermatogenic cells. Molecular Reproduction and Development: Incorporating Gamete Research. 2006;73(6):767-773.
89. Charlton R, Henderson M, Richards J, et al. Immunohistochemical analysis of calpain 3: advantages and limitations in diagnosing LGMD2A. Neuromuscular Disorders. 2009;19(7):449-457.
90. Hauerslev S, Sveen M-L, Duno M, Angelini C, Vissing J, Krag TO. Calpain 3 is important for muscle regeneration: evidence from patients with limb girdle muscular dystrophies. BMC Musculoskeletal Disorders. 2012;13:1-11.
91. Mahajan VB, Skeie JM, Bassuk AG, et al. Calpain-5 mutations cause autoimmune uveitis, retinal neovascularization, and photoreceptor degeneration. PLoS Genetics 2012; 8(10): e1003001.
92. Turner MD, Cassell PG, Hitman GA. Calpain‐10: from genome search to function. Diabetes/metabolism research and reviews. 2005;21(6):505-514.
93. Zha C, Farah CA, Holt RJ, et al. Biallelic variants in the small optic lobe calpain CAPN15 are associated with congenital eye anomalies, deafness and other neurodevelopmental deficits. Human molecular genetics. 2020;29(18):3054-3063.
94. Litosh VA, Rochman M, Rymer JK, Porollo A, Kottyan LC, Rothenberg ME. Calpain-14 and its association with eosinophilic esophagitis. Journal of Allergy and Clinical Immunology. 2017;139(6):1762-1771. e7.