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Article information

Submitting author: Jens Staal[a][i]  
Additional contributors: Wikipedia community

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  1. ↑ Ghent University
  1. ↑ jens.staal@irc.vib-ugent.be

Abstract

The CARD-CC protein family is defined by an evolutionary conserved "caspase activation and recruitment domain" (CARD) and a coiled-coil (CC) domain.[1] Coiled-coils (CC) act as oligomerization domains for many proteins such as structural and motor proteins, and transcription factors. This means that monomers are converted to macromolecular complexes by polymerization.[2] In humans and other jawed vertebrates, the family consists of CARD9 and the three "CARD-containing MAGUK protein" (CARMA)[3] proteins CARD11 (CARMA1), CARD14 (CARMA2) and CARD10 (CARMA3).


Evolution and species distribution

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Graphical overview of the protein domains n the CARD-CC family members
CARD-CC protein family structure

The protein family is ancient and can be found as far back as Cnidaria, but has almost exclusively been studied in humans and mice. Notably, the protein family is absent in insects and nematodes, which makes it impossible to study its function in the most popular invertebrate model organisms (Drosophila and C. elegans). Invertebrates only have a CARD9-like ancestral CARD-CC member, and the earliest occurrence of a CARD-CC member with the CARMA domain composition is in the jawless vertebrate hagfish. All four CARD-CC family members are present in sharks, indicating that the 3 distinct CARMA CARD-CC family members were formed by two duplication events just before or very early in the jawed vertebrate evolution. The four CARD-CC members in mice and humans differ in expression domains, where CARD9 is mostly expressed in myelocytes, CARD11 in lymphocytes, while CARD10 and CARD14 are mostly expressed in non-hemapoetic cells. This gene expression differentiation between the four CARD-CC family members conserved at least as far back as frogs (Xenopus tropicalis) and fish (Danio rerio),[4] indicating that the four CARD-CC family members have had distinct functions since early jawed vertebrate evolution.

Functions

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Graphical overview of signaling pathways dependent on a CARD-CC family member
Graphical overview of signaling pathways dependent on a CARD-CC family member

A common theme for all four CARD-CC family proteins in mice and humans is that they are activated by different protein kinase C isoforms,[5] and recruit BCL10 and the paracaspase MALT1 upon activation, forming a so-called CBM complex. There are four different CBM complexes, defined by which CARD-CC family member that is responsible for its assembly: CBM-9 (CARD9), CBM-1 (CARD11/CARMA1), CBM-2 (CARD14/CARMA2) and CBM-3 (CARD10/CARMA3). [6] CBM complex assembly results in recruitment of TRAF6 to MALT1 and downstream activation of NF-κB transcriptional activity and expression of pro-inflammatory cytokines. The different CARD-CC family members show different expression pattern and gain- or loss of function mutation in the different CARD-CC family proteins cause different phenotypes.

References

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  1. ↑ Staal J, Driege Y, Haegman M, Borghi A, Hulpiau P, Lievens L, Gul IS, Sundararaman S, Gonçalves A, Dhondt I, Pinzón JH, Braeckman BP, Technau U, Saeys Y, van Roy F, Beyaert R (2018). "Ancient Origin of the CARD-Coiled Coil/Bcl10/MALT1-Like Paracaspase Signaling Complex Indicates Unknown Critical Functions". Frontiers in Immunology 9: 1136. doi:10.3389/fimmu.2018.01136. PMID 29881386. PMC 5978004. //www.ncbi.nlm.nih.gov/pmc/articles/PMC5978004/. 
  2. ↑ "CC Protein Domain | Coiled Coil | Cell Signaling Technology". www.cellsignal.com. Retrieved 2020-02-01.
  3. ↑ Scudiero I, Vito P, Stilo R (August 2014). "The three CARMA sisters: so different, so similar: a portrait of the three CARMA proteins and their involvement in human disorders". Journal of Cellular Physiology 229 (8): 990–7. doi:10.1002/jcp.24543. PMID 24375035. 
  4. ↑ "BioGPS". BioGPS. The Scripps Research Institute. Retrieved 2021-07-27.
  5. ↑ Staal, Jens; Driege, Yasmine; Haegman, Mira; Kreike, Marja; Iliaki, Styliani; Vanneste, Domien; Lork, Marie; Afonina, Inna S. et al. (2020-08-13). "Defining the combinatorial space of PKC::CARD-CC signal transduction nodes". The FEBS Journal 288 (5): 1630–1647. doi:10.1111/febs.15522. ISSN 1742-4658. PMID 32790937. https://febs.onlinelibrary.wiley.com/doi/full/10.1111/febs.15522. 
  6. ↑ Gehring, Torben; Seeholzer, Thomas; Krappmann, Daniel (2018). "BCL10 – Bridging CARDs to Immune Activation". Frontiers in Immunology 9: 1539. doi:10.3389/fimmu.2018.01539. ISSN 1664-3224. PMID 30022982. PMC 6039553. //www.ncbi.nlm.nih.gov/pmc/articles/PMC6039553/. 
  7. ↑ Gross O, Gewies A, Finger K, Schäfer M, Sparwasser T, Peschel C, Förster I, Ruland J (August 2006). "Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity". Nature 442 (7103): 651–6. doi:10.1038/nature04926. PMID 16862125. 
  8. ↑ Online 'Mendelian Inheritance in Man' (OMIM) 607212
  9. ↑ Stepensky P, Keller B, Buchta M, Kienzler AK, Elpeleg O, Somech R, Cohen S, Shachar I, Miosge LA, Schlesier M, Fuchs I, Enders A, Eibel H, Grimbacher B, Warnatz K (February 2013). "Deficiency of caspase recruitment domain family, member 11 (CARD11), causes profound combined immunodeficiency in human subjects". The Journal of Allergy and Clinical Immunology 131 (2): 477–85.e1. doi:10.1016/j.jaci.2012.11.050. PMID 23374270. https://openresearch-repository.anu.edu.au/bitstream/1885/11324/7/Stepensky%20et%20al%20%20Deficiency%20of%20caspase%202013.docx.pdf. 
  10. ↑ Ma CA, Stinson JR, Zhang Y, Abbott JK, Weinreich MA, Hauk PJ, Reynolds PR, Lyons JJ, Nelson CG, Ruffo E, Dorjbal B, Glauzy S, Yamakawa N, Arjunaraja S, Voss K, Stoddard J, Niemela J, Zhang Y, Rosenzweig SD, McElwee JJ, DiMaggio T, Matthews HF, Jones N, Stone KD, Palma A, Oleastro M, Prieto E, Bernasconi AR, Dubra G, Danielian S, Zaiat J, Marti MA, Kim B, Cooper MA, Romberg N, Meffre E, Gelfand EW, Snow AL, Milner JD (August 2017). "Germline hypomorphic CARD11 mutations in severe atopic disease". Nature Genetics 49 (8): 1192–1201. doi:10.1038/ng.3898. PMID 28628108. PMC 5664152. //www.ncbi.nlm.nih.gov/pmc/articles/PMC5664152/. 
  11. ↑ Brohl AS, Stinson JR, Su HC, Badgett T, Jennings CD, Sukumar G, Sindiri S, Wang W, Kardava L, Moir S, Dalgard CL, Moscow JA, Khan J, Snow AL (January 2015). "Germline CARD11 Mutation in a Patient with Severe Congenital B Cell Lymphocytosis". Journal of Clinical Immunology 35 (1): 32–46. doi:10.1007/s10875-014-0106-4. PMID 25352053. PMC 4466218. //www.ncbi.nlm.nih.gov/pmc/articles/PMC4466218/. 
  12. ↑ Lenz G, Davis RE, Ngo VN, Lam L, George TC, Wright GW, Dave SS, Zhao H, Xu W, Rosenwald A, Ott G, Muller-Hermelink HK, Gascoyne RD, Connors JM, Rimsza LM, Campo E, Jaffe ES, Delabie J, Smeland EB, Fisher RI, Chan WC, Staudt LM (March 2008). "Oncogenic CARD11 mutations in human diffuse large B cell lymphoma". Science 319 (5870): 1676–9. doi:10.1126/science.1153629. PMID 18323416. 
  13. ↑ Jordan CT, Cao L, Roberson ED, Pierson KC, Yang CF, Joyce CE, Ryan C, Duan S, Helms CA, Liu Y, Chen Y, McBride AA, Hwu WL, Wu JY, Chen YT, Menter A, Goldbach-Mansky R, Lowes MA, Bowcock AM (May 2012). "PSORS2 is due to mutations in CARD14". American Journal of Human Genetics 90 (5): 784–95. doi:10.1016/j.ajhg.2012.03.012. PMID 22521418. PMC 3376640. //www.ncbi.nlm.nih.gov/pmc/articles/PMC3376640/. 
  14. ↑ Online 'Mendelian Inheritance in Man' (OMIM) 607211
  15. ↑ Peled A, Sarig O, Sun G, Samuelov L, Ma CA, Zhang Y, Dimaggio T, Nelson CG, Stone KD, Freeman AF, Malki L, Vidal LS, Chamarthy LM, Briskin V, Mohamad J, Pavlovsky M, Walter JE, Milner JD, Sprecher E (January 2019). "Loss-of-function mutations in caspase recruitment domain-containing protein 14 (CARD14) are associated with a severe variant of atopic dermatitis". The Journal of Allergy and Clinical Immunology 143 (1): 173–181.e10. doi:10.1016/j.jaci.2018.09.002. PMID 30248356. 
  16. ↑ McAuley JR, Freeman TJ, Ekambaram P, Lucas PC, McAllister-Lucas LM (2018). "CARMA3 Is a Critical Mediator of G Protein-Coupled Receptor and Receptor Tyrosine Kinase-Driven Solid Tumor Pathogenesis". Frontiers in Immunology 9: 1887. doi:10.3389/fimmu.2018.01887. PMID 30158935. PMC 6104486. //www.ncbi.nlm.nih.gov/pmc/articles/PMC6104486/. 
  17. ↑ Zhou T, Souzeau E, Sharma S, Siggs OM, Goldberg I, Healey PR, Graham S, Hewitt AW, Mackey DA, Casson RJ, Landers J, Mills R, Ellis J, Leo P, Brown MA, MacGregor S, Burdon KP, Craig JE (November 2016). "CARD10 enriched in primary open-angle glaucoma". Molecular Genetics & Genomic Medicine 4 (6): 624–633. doi:10.1002/mgg3.248. PMID 27896285. PMC 5118207. //www.ncbi.nlm.nih.gov/pmc/articles/PMC5118207/. 
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