An alternative processing pathway of APP reveals two distinct cleavage modes for rhomboid protease RHBDL4

References

Adrain, C., Zettl, M., Christova, Y., Taylor, N., and Freeman, M. (2012). Tumor necrosis factor signaling requires iRhom2 to promote trafficking and activation of TACE. Science 335, 225–228.10.1126/science.1214400Suche in Google Scholar PubMed PubMed Central

Arutyunova, E., Panwar, P., Skiba, P., Gale, N., Mak, M., and Lemieux, M. (2014). Allosteric regulation of rhomboid intramembrane proteolysis. EMBO J. 33, 1869–1881.10.15252/embj.201488149Suche in Google Scholar PubMed PubMed Central

Bhattacharyya, R., Barren, C., and Kovacs, D.M. (2013). Palmitoylation of amyloid precursor protein regulates amyloidogenic processing in lipid rafts. J. Neurosci. 33, 11169–11183.10.1523/JNEUROSCI.4704-12.2013Suche in Google Scholar PubMed PubMed Central

Bonifacino, J.S., Suzuki, C.K., and Klausner, R.D. (1990). A peptide sequence confers retention and rapid degradation in the endoplasmic reticulum. Science 247, 79–82.10.1126/science.2294595Suche in Google Scholar PubMed

Cheng, T.L., Lai, C.H., Jiang, S.J., Hung, J.H., Liu, S.K., Chang, B.I., Shi, G.Y., and Wu, H.L. (2014). RHBDL2 is a critical membrane protease for anoikis resistance in human malignant epithelial cells. Sci. World J. 2014, 902987.10.1155/2014/902987Suche in Google Scholar PubMed PubMed Central

Christova, Y., Adrain, C., Bambrough, P., Ibrahim, A., and Freeman, M. (2013). Mammalian iRhoms have distinct physiological functions including an essential role in TACE regulation. EMBO Rep. 14, 884–890.10.1038/embor.2013.128Suche in Google Scholar PubMed PubMed Central

De Strooper, B. and Annaert, W. (2000). Proteolytic processing and cell biological functions of the amyloid precursor protein. J. Cell Sci. 113, 1857–1870.10.1242/jcs.113.11.1857Suche in Google Scholar PubMed

El Ayadi, A., Stieren, E., Barral, J., and Boehning, D. (2012). Ubiquilin-1 regulates amyloid precursor protein maturation and degradation by stimulating K63-linked polyubiquitination of lysine 688. Proc. Natl. Acad. Sci. USA 109, 13416–13421.10.1073/pnas.1206786109Suche in Google Scholar PubMed PubMed Central

Fleig, L., Bergbold, N., Sahasrabudhe, P., Geiger, B., Kaltak, L., and Lemberg, M.K. (2012). Ubiquitin-dependent intramembrane rhomboid protease promotes ERAD of membrane proteins. Mol. Cell 47, 558–569.10.1016/j.molcel.2012.06.008Suche in Google Scholar PubMed

Johnson, N., Brezinova, J., Stephens, E., Burbridge, E., Freeman, M., Adrain, C., and Strisovsky, K. (2017). Quantitative proteomics screen identifies a substrate repertoire of rhomboid protease RHBDL2 in human cells and implicates it in epithelial homeostasis. Sci. Rep. 7, 7283.10.1038/s41598-017-07556-3Suche in Google Scholar PubMed PubMed Central

Kaden, D., Munter, L., Reif, B., and Multhaup, G. (2012). The amyloid precursor protein and its homologues: structural and functional aspects of native and pathogenic oligomerization. Eur. J. Cell Biol. 91, 234–239.10.1016/j.ejcb.2011.01.017Suche in Google Scholar PubMed

Kinch, L.N. and Grishin, N.V. (2013). Bioinformatics perspective on rhomboid intramembrane protease evolution and function. Biochim. Biophys. Acta 1828, 2937–2943.10.1016/j.bbamem.2013.06.031Suche in Google Scholar PubMed PubMed Central

Lemberg, M.K. and Adrain, C. (2016). Inactive rhomboid proteins: new mechanisms with implications in health and disease. Semin. Cell Dev. Biol. 60, 29–37.10.1016/j.semcdb.2016.06.022Suche in Google Scholar PubMed

Lemberg, M. and Freeman, M. (2007a). Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases. Genome Res. 17, 1634–1646.10.1101/gr.6425307Suche in Google Scholar PubMed PubMed Central

Lemberg, M.K. and Freeman, M. (2007b). Cutting proteins within lipid bilayers: rhomboid structure and mechanism. Mol. Cell 28, 930–940.10.1016/j.molcel.2007.12.003Suche in Google Scholar PubMed

Lemberg, M.K. and Freeman, M. (2007c). Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases. Genome Res. 17, 1634–1646.10.1101/gr.6425307Suche in Google Scholar

Lemieux, M.J., Fischer, S.J., Cherney, M.M., Bateman, K.S., and James, M.N. (2007). The crystal structure of the rhomboid peptidase from Haemophilus influenzae provides insight into intramembrane proteolysis. Proc. Natl. Acad. Sci. USA 104, 750–754.10.1073/pnas.0609981104Suche in Google Scholar PubMed PubMed Central

Marrosu, M.G., Vaccargiu, S., Marrosu, G., Vannelli, A., Cianchetti, C., and Muntoni, F. (1998). Charcot-Marie-Tooth disease type 2 associated with mutation of the myelin protein zero gene. Neurology 50, 1397–1401.10.1212/WNL.50.5.1397Suche in Google Scholar

McIlwain, D.R., Lang, P.A., Maretzky, T., Hamada, K., Ohishi, K., Maney, S.K., Berger, T., Murthy, A., Duncan, G., Xu, H.C., et al. (2012). iRhom2 regulation of TACE controls TNF-mediated protection against Listeria and responses to LPS. Science 335, 229–232.10.1126/science.1214448Suche in Google Scholar PubMed PubMed Central

Miao, F., Zhang, M., Zhao, Y., Li, X., Yao, R., Wu, F., Huang, R., Li, K., Miao, S., Ma, C., et al. (2017). RHBDD1 upregulates EGFR via the AP-1 pathway in colorectal cancer. Oncotarget 8, 25251–25260.10.18632/oncotarget.15694Suche in Google Scholar PubMed PubMed Central

Minopoli, G., de Candia, P., Bonetti, A., Faraonio, R., Zambrano, N., and Russo, T. (2001). The beta-amyloid precursor protein functions as a cytosolic anchoring site that prevents Fe65 nuclear translocation. J. Biol. Chem. 276, 6545–6550.10.1074/jbc.M007340200Suche in Google Scholar PubMed

Muller, U.C., Deller, T., and Korte, M. (2017). Not just amyloid: physiological functions of the amyloid precursor protein family. Nat. Rev. Neurosci. 18, 281–298.10.1038/nrn.2017.29Suche in Google Scholar PubMed

Numakura, C., Lin, C.Q., Ikegami, T., Guldberg, P., and Hayasaka, K. (2002). Molecular analysis in Japanese patients with Charcot-Marie-Tooth disease: DGGE analysis for PMP22, MPZ, and Cx32/GJB1 mutations. Hum. Mutat. 20, 392–398.10.1002/humu.10134Suche in Google Scholar PubMed

Paschkowsky, S., Hamze, M., Oestereich, F., and Munter, L.M. (2016). Alternative processing of the amyloid precursor protein family by rhomboid protease RHBDL4. J. Biol. Chem. 291, 21903–21912.10.1074/jbc.M116.753582Suche in Google Scholar PubMed PubMed Central

Paschkowsky, S., Oestereich, F., and Munter, L.M. (2018a). Embedded in the membrane: how lipids confer activity and specificity to intramembrane proteases. J. Membr. Biol. 251, 369–378.10.1007/s00232-017-0008-5Suche in Google Scholar PubMed

Paschkowsky, S., Recinto, S.J., Young, J.C., Bondar, A.N., and Munter, L.M. (2018b). Membrane cholesterol as regulator of human rhomboid protease RHBDL4. J. Biol. Chem. DOI: 10.1074/jbc.RA118.002640. [Epub ahead of print].10.1074/jbc.RA118.002640Suche in Google Scholar PubMed PubMed Central

Reinhard, C., Hebert, S.S., and De Strooper, B. (2005). The amyloid-beta precursor protein: integrating structure with biological function. EMBO J. 24, 3996–4006.10.1038/sj.emboj.7600860Suche in Google Scholar PubMed PubMed Central

Shi, G., Lee, J.R., Grimes, D.A., Racacho, L., Ye, D., Yang, H., Ross, O.A., Farrer, M., McQuibban, G.A., and Bulman, D.E. (2011). Functional alteration of PARL contributes to mitochondrial dysregulation in Parkinson’s disease. Hum. Mol. Genet. 20, 1966–1974.10.1093/hmg/ddr077Suche in Google Scholar PubMed

Song, W., Liu, W., Zhao, H., Li, S., Guan, X., Ying, J., Zhang, Y., Miao, F., Zhang, M., Ren, X., et al. (2015). Rhomboid domain containing 1 promotes colorectal cancer growth through activation of the EGFR signalling pathway. Nat. Commun. 6, 8022.10.1038/ncomms9022Suche in Google Scholar PubMed PubMed Central

Stangeland, B., Mughal, A.A., Grieg, Z., Sandberg, C.J., Joel, M., Nygard, S., Meling, T., Murrell, W., Vik Mo, E.O., and Langmoen, I.A. (2015). Combined expressional analysis, bioinformatics and targeted proteomics identify new potential therapeutic targets in glioblastoma stem cells. Oncotarget 6, 26192–26215.10.18632/oncotarget.4613Suche in Google Scholar PubMed PubMed Central

Strisovsky, K. (2016). Why cells need intramembrane proteases – a mechanistic perspective. FEBS J. 283, 1837–1845.10.1111/febs.13638Suche in Google Scholar PubMed

Strisovsky, K. and Freeman, M. (2014). Sharpening rhomboid specificity by dimerisation and allostery. EMBO J. 33, 1847–1848.10.15252/embj.201489373Suche in Google Scholar PubMed PubMed Central

Strisovsky, K., Sharpe, H.J., and Freeman, M. (2009). Sequence-specific intramembrane proteolysis: identification of a recognition motif in rhomboid substrates. Mol. Cell 36, 1048–1059.10.1016/j.molcel.2009.11.006Suche in Google Scholar PubMed PubMed Central

Ulmschneider, M.B., Ulmschneider, J.P., Freites, J.A., von Heijne, G., Tobias, D.J., and White, S.H. (2017). Transmembrane helices containing a charged arginine are thermodynamically stable. Eur. Biophys. J. 46, 627–637.10.1007/s00249-017-1206-xSuche in Google Scholar PubMed PubMed Central

Urban, S. and Baker, R.P. (2008). In vivo analysis reveals substrate-gating mutants of a rhomboid intramembrane protease display increased activity in living cells. Biol. Chem. 389, 1107–1115.10.1515/BC.2008.122Suche in Google Scholar PubMed PubMed Central

Urban, S. and Freeman, M. (2003). Substrate specificity of rhomboid intramembrane proteases is governed by helix-breaking residues in the substrate transmembrane domain. Mol. Cell 11, 1425–1434.10.1016/S1097-2765(03)00181-3Suche in Google Scholar PubMed

Urban, S., Lee, J.R., and Freeman, M. (2001). Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107, 173–182.10.1016/S0092-8674(01)00525-6Suche in Google Scholar

Walder, K., Kerr-Bayles, L., Civitarese, A., Jowett, J., Curran, J., Elliott, K., Trevaskis, J., Bishara, N., Zimmet, P., Mandarino, L., et al. (2005). The mitochondrial rhomboid protease PSARL is a new candidate gene for type 2 diabetes. Diabetologia 48, 459–468.10.1007/s00125-005-1675-9Suche in Google Scholar PubMed

Wang, Y., Zhang, Y., and Ha, Y. (2006). Crystal structure of a rhomboid family intramembrane protease. Nature 444, 179–180.10.1038/nature05255Suche in Google Scholar PubMed

Wolfe, M.S. (2012). Processive proteolysis by gamma-secretase and the mechanism of Alzheimer’s disease. Biol. Chem. 393, 899–905.10.1515/hsz-2012-0140Suche in Google Scholar PubMed

Wunderle, L., Knopf, J.D., Kuhnle, N., Morle, A., Hehn, B., Adrain, C., Strisovsky, K., Freeman, M., and Lemberg, M.K. (2016). Rhomboid intramembrane protease RHBDL4 triggers ER-export and non-canonical secretion of membrane-anchored TGFα. Sci. Rep. 6, 27342.10.1038/srep27342Suche in Google Scholar PubMed PubMed Central