The RIM/NIM Family of Neuronal C2 Domain Proteins
Open accessAbstract
RIM1 is a putative effector protein for Rab3s, synaptic GTP-binding proteins. RIM1 is localized close to the active zone at the synapse, where it interacts in a GTP-dependent manner with Rab3 located on synaptic vesicles. We now describe a second RIM protein, called RIM2, that is highly homologous to RIM1 and also expressed primarily in brain. Like RIM1, RIM2 contains an N-terminal zinc finger domain that binds to Rab3 as a function of GTP, a central PDZ domain, and two C-terminal C(2) domains that are separated by long alternatively spliced sequences. Unexpectedly, the 3'-end of the RIM2 gene produces an independent mRNA that encodes a smaller protein referred as NIM2. NIM2 is composed of a unique N-terminal sequence followed by the C-terminal part of RIM2. Data bank searches identified a third RIM/NIM-related gene, which encodes a NIM isoform referred to as NIM3; no RIM transcript from this gene was detected. To test if NIMs, like RIMs, may function in secretion, we investigated the effect of NIM3 on calcium-triggered exocytosis in PC12 cells. NIM3 induced a dramatic increase in calcium-evoked exocytosis (50%), with no significant effect on base-line release, suggesting that NIMs, like RIMs, regulate exocytosis The combination of conserved and variable sequences in RIMs and NIMs indicates that the individual domains of these proteins provide binding sites for interacting molecules during exocytosis, as shown for the zinc finger domain of RIM, which binds to GTP-bound Rab3s.…
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RIM-BPs bind to RIMs and to N-, P/Q-, and L-type Ca2+ channels.
“However, the latter identification may be erroneous since subsequent studies showed that RIM-BPs are highly expressed only in brain and not peripherally and tightly bind to RIM (Wang et al., 2000) and to N-, P/Q-, and L-type Ca2+ channels (Hibino et al., 2002; Kaeser et al., 2011).”
From The Presynaptic Active Zone (2012) · cites this paper as Wang et al., 2000
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“…the localization of RIM1 in cultured neurons, but many proteins, including Rab3A (Wang et al., 1997), cAMP-GEFII (Ozaki et al., 2000), RIM-BPs (Wang et al., 2000), Munc13-1 (Betz et al., 2001), synaptotagmin (Coppola et al., 2001), Ca 2 channel (Coppola et al., 2001), and -liprin (Schoch et…”
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Self-citationRIM genes differentially contribute to organizing presynaptic release sites
Kaeser, P. S., Deng, L., Fan, M., & Südhof, T. C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209318109 · Cited by 115 · see citing works
Self-citationWang, Y., & Südhof, T. C. (2003) · Genomics · doi:10.1016/s0888-7543(02)00024-1 · Cited by 112 · see citing works
Self-citationRegus-Leidig, H., Dieck, S. T., Specht, D., Meyer, L., & Brandstätter, J. (2009) · The Journal of comparative neurology · doi:10.1002/cne.21915 · Cited by 108 · see citing works
“The mature CAZ of conventional chemical synapses is defined by a set of multidomain proteins that includes Munc13 (Brose et al., 1995), RIM (Wang et al., 1997, 2000), ERC/CAST (Ohtsuka et al., 2002; Wang et al., 2002), Piccolo/Aczonin (Cases-Langhoff et al., 1996; Wang et al., 1999), Bassoon (tom…”
BackgroundAssembly of Active Zone Precursor Vesicles
Dresbach, T., Torres, V. I., Wittenmayer, N., Altrock, W. D., Zamorano, P. L., Zuschratter, W., Nawrotzki, R., Ziv, N. E., Garner, C. C., & Gundelfinger, E. D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508784200 · Cited by 106 · see citing works
Johnson, S., Halford, S., Morris, A., Patel, R. J., Wilkie, S., Hardcastle, A., Moore, A., Zhang, K., & Hunt, D. (2003) · Genomics · doi:10.1016/s0888-7543(03)00010-7 · Cited by 107 · see citing works
Fenster, S. D., Kessels, M. M., Qualmann, B., Chung, W. J., Nash, J. E., Gundelfinger, E. D., & Garner, C. C. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210792200 · Cited by 103 · see citing works
Liprin-α proteins: scaffold molecules for synapse maturation
Spangler, S. A., & Hoogenraad, C. C. (2007) · Biochemical Society Transactions · doi:10.1042/bst0351278 · Cited by 104 · see citing works
Andrews-Zwilling, Y. S., Kawabe, H., Reim, K., Varoqueaux, F., & Brose, N. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m601421200 · Cited by 103 · see citing works
Liquid-Liquid Phase Separation in Neuronal Development and Synaptic Signaling
Wu, X., Cai, Q., Feng, Z., & Zhang, M. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.06.012 · Cited by 110 · see citing works
Kaeser, P. S., Kwon, H.-B., Chiu, C.-Y. Q., Deng, L., Castillo, P., & Südhof, T. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3235-08.2008 · Cited by 97 · see citing works
“Finally, a PxxP sequence between the two C2-domains of RIM1 binds to RIMBPs (Wang et al., 2000), and the N-terminal region of RIM1 binds to 14-3-3 proteins (Sun et al., 2003; Simsek-Duran et al., 2004; Kaeser et al., 2008).”
BackgroundSelf-citationRIM Promotes Calcium Channel Accumulation at Active Zones of the Drosophila Neuromuscular Junction
Graf, E., Valakh, V., Wright, C. M., Wu, C.-L., Liu, Z., Zhang, Y. Q., & Diantonio, A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0965-12.2012 · Cited by 96 · see citing works
“, 2011) but also interacting with each other and several other components to form the active zone cytomatrix (Wang et al., 2000; Betz et al., 2001; Coppola et al., 2001; Ohtsuka et al., 2002; Schoch et al., 2002; Wang et al., 2002; Deken et al., 2005; Dulubova et al., 2005).”
BackgroundInfluentialRIM function in short- and long-term synaptic plasticity
Kaeser, P. S., & Südhof, T. C. (2005) · Biochemical Society Transactions · doi:10.1042/bst20051345 · Cited by 83 · see citing works
Self-citationVoltage-Gated Calcium Channels: Key Players in Sensory Coding in the Retina and the Inner Ear
Pangršič, T., Singer, J. H., & Koschak, A. (2018) · Physiological Reviews · doi:10.1152/physrev.00030.2017 · Cited by 113 · see citing works
RIM-BP3 is a manchette-associated protein essential for spermiogenesis
Zhou, J., Du, Y.-R., Qin, W., Hu, Y.-G., Huang, Y.-N., Bao, L., Han, D., Mansouri, A., & Xu, G.-L. (2009) · Development · doi:10.1242/dev.030858 · Cited by 83 · see citing works
“These genes are involved in the regulation of acrosome biogenesis (Hrb, Gopc and Csnk2a2) (Escalier et al., 2003; Kang-Decker et al., 2001; Yao et al., 2002), tail formation (Tektin-t, Vdac3, Sepp1, Akap4 and Spag6) (Olson et al., 2005; Sampson et al., 2001; Sapiro et al., 2002; Shirohzu et al., 2002; Tanaka et al., 2…”
Comprehensive genomics linking between neural development and cancer: neuroblastoma as a model.
Nakagawara, A., & Ohira, M. (2004) · Cancer Letters · doi:10.1016/s0304-3835(03)00457-9 · Cited by 81 · see citing works
“Nbla00697) [65], RAB3 efffector protein RIM1 (Nbla00761) [ 66 ], cell recognition molecule”
Synaptotagmin-like protein 5: a novel Rab27A effector with C-terminal tandem C2 domains
Kuroda, T. S., Fukuda, M., Ariga, H., & Mikoshiba, K. (2002) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)00320-0 · Cited by 82 · see citing works
Specific Regulation of IRS-2 Expression by Glucose in Rat Primary Pancreatic Islet β-Cells*
Lingohr, M. K., Briaud, I., Dickson, L. M., McCuaig, J., Alárcon, C., Wicksteed, B., & Rhodes, C. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m600356200 · Cited by 79 · see citing works
Molecular Machines Regulating the Release Probability of Synaptic Vesicles at the Active Zone
Körber, C., & Kuner, T. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00005 · Cited by 72 · see citing works
“It has been shown that the increase in presynaptic calcium concentration during high frequency synaptic activity speeds-up the refilling of the RRP at the calyx of Held (Wang and Kaczmarek, 1998).”
BackgroundRIM proteins and their role in synapse function
Mittelstaedt, T., Álvarez‐Barón, E., & Schoch, S. (2010) · Biological Chemistry · doi:10.1515/bc.2010.064 · Cited by 76 · see citing works
“The RIM C2 domains do not contain the consensus calcium binding sites that have been defined in the Synaptotagmin C2 domains, and do not bind to phospholipids (Wang et al., 2000).”
BackgroundAsaba, N., Hanada, T., Takeuchi, A., & Chishti, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210362200 · Cited by 69 · see citing works
Modulation of Cav1.3 Ca2+ channel gating by Rab3 interacting molecule.
Gebhart, M., Juhász-Vedres, G., Zuccotti, A., Brandt, N., Engel, J., Trockenbacher, A., Kaur, G., Obermair, G., Knipper, M., Koschak, A., et al. (2010) · Molecular and cellular neurosciences · doi:10.1016/j.mcn.2010.03.011 · Cited by 67
Sun, L., Bittner, M. A., & Holz, R. W. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212801200 · Cited by 62 · see citing works
Regulation of Arabidopsis COPINE 1 Gene Expression in Response to Pathogens and Abiotic Stimuli1
Jambunathan, N., & McNellis, T. W. (2003) · Plant Physiology · doi:10.1104/pp.103.022970 · Cited by 63
“C2 domain-containing proteins include protein kinase C (Azzi et al., 1992), phospholipase C (Essen et al., 1996), synaptotagmin (Brose et al., 1995), and rabphilin (Wang et al., 2000).”
BackgroundNielsen, D. A., Ji, F., Yuferov, V., Ho, A., He, C.-S., Ott, J., & Kreek, M. (2010) · Psychiatric Genetics · doi:10.1097/ypg.0b013e32833a2106 · Cited by 62 · see citing works
“RIMs are found in the active zone of presynaptic nerve terminals, the sites on the plasma membrane where synaptic vesicle exocytosis occurs (Wang et al., 2000).”
BackgroundWang, X., Hu, B., Zimmermann, B., & Kilimann, M. W. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m103337200 · Cited by 59 · see citing works
Hamanaka, Y., & Meinertzhagen, I. A. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22268 · Cited by 54 · see citing works
“Although knowledge of the complete protein composition of the CAZ remains incomplete, the list includes: Munc13-1 (Brose et al., 1995), RIMs (Wang et al., 1997, 2000), ERC/ CAST (Ohtsuka et al., 2002; Wang et al., 2002), Piccolo/ Aczonin, and Bassoon (Cases-Langhoff et al., 1996; tom Dieck et al.,…”
BackgroundGerber, S. H., Garcia, J. M., Rizo, J., & Südhof, T. (2001) · EMBO Journal · doi:10.1093/emboj/20.7.1605 · Cited by 56 · see citing works
Self-citationSynapse development and maturation at the drosophila neuromuscular junction
Chou, V., Johnson, S. A., & Vactor, D. V. (2020) · Neural Development · doi:10.1186/s13064-020-00147-5 · Cited by 68 · see citing works
Molecular Organization and Assembly of the Presynaptic Active Zone of Neurotransmitter Release
Fejtová, A., & Gundelfinger, E. D. (2006) · Results and problems in cell differentiation · doi:10.1007/400_012 · Cited by 50 · see citing works
“The diversity of RIM family members is even increased by alternative splicing of α and β isoforms ( Wang et al. 2000; Wang and Sudhof 2003).”
BackgroundInfluentialMolecular mechanisms of synaptogenesis
Qi, C., Luo, L.-D., Feng, I., & Ma, S. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.939793 · Cited by 54 · see citing works
“…domains, the active zone protein RIM (Rab3 Interacting Molecules) and its interaction partners such as RIM-BP, ELKS, and CAST were identified (Wang et al., 1997, 2000, 2002) [sub-cellular fractionation of mammals’ synaptic fraction also independently discovered CAST (Ohtsuka et al., 2002)].”
BackgroundSaw, N. M. N., Kang, S.-Y. A., Parsaud, L., Han, G. A., Jiang, T., Grzegorczyk, K., Surkont, M., Sun-Wada, G., Wada, Y., Li, L., et al. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-02-0155 · Cited by 53 · see citing works
“…315– Volume 22 September 15, 2011 Voa1/Voa2 in vesicular acidification | 3407 in K-glutamate buffer (20 mM HEPES, pH 7.1, 140 mM potassium glutamate, 2 mM EGTA, 1 mM MgCl2), and mechanically permeabilized with a ball homogenizer (Wang et al., 2000, 2004a; Fujita et al., 2007; Li et al., 2007).”
MethodInfluentialSelf-citationWater channels and zymogen granules in salivary glands.
Ishikawa, Y., Cho, G., Yuan, Z.-F., Skowroński, M., Pan, Y., & Ishida, H. (2006) · Journal of Pharmacological Sciences · doi:10.1254/jphs.crj06007x · Cited by 53
Structure and evolution of RIM-BP genes: Identification of a novel family member
Mittelstaedt, T., & Schoch, S. (2007) · Gene · doi:10.1016/j.gene.2007.08.004 · Cited by 55 · see citing works
“RIM-BPs display structures typical of adaptor proteins and have been shown to interact with the active zone proteins RIM1 and RIM2 as well as with different α-subunits of voltage-gated calcium channels (Wang et al., 2000; Hibino et al., 2002).”
BackgroundInfluentialRab3D: a regulator of exocytosis in non-neuronal cells.
Millar, A., Pavios, N. J., Xu, J., & Zheng, M.-H. (2002) · Histology and Histopathology · doi:10.14670/hh-17.929 · Cited by 50
Variants in several genomic regions associated with asperger disorder
Salyakina, D., Ma, D. Q., Jaworski, J. M., Konidari, I., Whitehead, P. L., Henson, R., Martinez, D. M., Robinson, J. L., Sacharow, S. J., Wright, H. H., et al. (2010) · Autism Research · doi:10.1002/aur.158 · Cited by 44 · see citing works
Uriu, Y., Kiyonaka, S., Miki, T., Yagi, M., Akiyama, S., Mori, E., Nakao, A., Beedle, A. M., Campbell, K. P., Wakamori, M., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.101311 · Cited by 46 · see citing works
RIM1: an edge for presynaptic plasticity.
Lonart, G. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02193-8 · Cited by 49 · see citing works
Ellencrona, K., Syed, A., & Johansson, M. (2009) · Biological chemistry · doi:10.1515/bc.2009.041 · Cited by 43 · see citing works
Dembla, E., Dembla, M., Maxeiner, S., & Schmitz, F. (2020) · Scientific Reports · doi:10.1038/s41598-020-62734-0 · Cited by 47 · see citing works
Kushibiki, Y., Suzuki, T., Jin, Y.-S., & Taru, H. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0506-19.2019 · Cited by 41 · see citing works
“3 (Y. Wang et al., 2000; Hibino et al., 2002; Kaeser et al., 2011; Davydova et al., 2014).”
Differential signaling in presynaptic neurotransmitter release
Ghijsen, W., & Leenders, A. G. M. (2005) · Cellular and Molecular Life Sciences (CMLS) · doi:10.1007/s00018-004-4525-0 · Cited by 41 · see citing works
Serano, J., & Rubin, G. (2003) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1835727100 · Cited by 41
Solution Structure of the RIM1α PDZ Domain in Complex with an ELKS1b C-terminal Peptide
Lu, J., Li, H., Wang, Y., Südhof, T. C., & Rizo, J. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.07.047 · Cited by 38 · see citing works
Self-citationRetinitis Pigmentosa and Allied Disorders
Gregory-Evans, K., Pennesi, M. E., & Weleber, R. G. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4557-0737-9.00040-0 · Cited by 112 · see citing works
Khanna, R., Li, Q., Sun, L., Collins, T., & Stanley, E. F. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.053 · Cited by 40 · see citing works
Ortega, J. M., Genç, Ö., & Davis, G. W. (2018) · eLife · doi:10.7554/elife.40385 · Cited by 38 · see citing works
Coupling the Structural and Functional Assembly of Synaptic Release Sites
Ghelani, T., & Sigrist, S. J. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00081 · Cited by 38 · see citing works
Maturation of Synaptic Contacts in Differentiating Neural Stem Cells
Liebau, S., Vaida, B., Storch, A., & Boeckers, T. M. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0823 · Cited by 34 · see citing works
Enrichment of integral membrane proteins from small amounts of brain tissue
Schindler, J., Jung, S., Niedner-Schatteburg, G., Friauf, E., & Nothwang, H. (2006) · Journal of neural transmission · doi:10.1007/s00702-006-0508-4 · Cited by 37
“Another identified protein was the Rab3-interacting protein 2 (RIMS2) which is involved in synaptic release (Wang et al., 2000; Graham et al., 2004; Sudhof, 2004).”
Wang, J., Lv, X., Wu, Y., Xu, T., Jiao, M., Yang, R., Li, X., Chen, M., Yan, Y.-G., Chen, C., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04672-0 · Cited by 38 · see citing works
Voltage-gated calcium channels function as Ca2+-activated signaling receptors
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“Most of the well-characterized VWA domains are found in celladhesion and extracellular-matrix (ECM) proteins, such as integrin b subunits, hemicentin and matrilins ( Tuckwell 1999; Whittaker and Hynes 2002).”
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Rab3a Binding and Secretion-enhancing Domains in Rim1 Are Separate and Unique
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Development and maintenance of vision’s first synapse
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Cell entry machines: a common theme in nature?
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“1 ); and they involve additional factors, such as the exocyst multi-subunit protein docking complex, microtubules and the recruitment of tethering proteins through Rab GTPases (such as Rab3A”
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Molecular organization of excitatory chemical synapses in the mammalian brain
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“RIM1 and RIM2 as well as shorter RIM isoforms containing only the Cterminal C2 domain (named NIM2 and NIM3) can influence Ca2c-evoked exocytosis from PC12 cells and are therefore likely to be involved in the regulation of neurotransmitter release (Wang et al. 1997, 2000).”
BackgroundInfluentialLai, C., Ho, Y., Hsieh, M., Wang, H.-H., Cheng, J., Chau, Y., & Peng, H. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1732-16.2016 · Cited by 32 · see citing works
“RIM1 , the major isoform of mammalian RIM families, was shown to bind with synaptic proteins to mediate vesicle release (Wang et al., 1997, 2000; Kaeser and Südhof, 2005).”
BackgroundWong, F. K., & Stanley, E. F. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06466.x · Cited by 30
- Authors
- Wang, Y., Sugita, S., & Südhof, T. C.
- Affiliations
- Howard Hughes Medical Institute (US)
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2000-06
- Volume
- 275
- Issue
- 26
- Pages
- 20033-20044
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2000501974
- Cited by
- 243
- References
- 42
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2023: 11 · 2022: 9 · 2021: 5 · 2020: 9 · 2019: 6 · 2018: 8 · 2017: 7 · 2016: 5 · 2015: 9 · 2014: 9 · 2013: 11 · 2012: 11
- FWCI
- 5.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Keywords
- RIM1, C2 domain proteins, Rab3, synaptic vesicle exocytosis, calcium-triggered exocytosis, synaptic active zone, zinc finger, PDZ domain, alternative splicing, Src homology 3 domain, fibronectin type III domain, protein-protein interaction
- MeSH terms
- Rabphilin-3A, Amino Acid Sequence, Animals, Brain, Carrier Proteins, Chromatography, Affinity, Cloning, Molecular, DNA-Binding Proteins, Exocytosis, Fungal Proteins, Glutathione Transferase, Humans, Molecular Sequence Data, Nerve Tissue Proteins, Nuclear Proteins, Polymorphism, Genetic, Recombinant Fusion Proteins, Tissue Distribution, Transfection, PC12 Cells, Sequence Homology, Amino Acid, Alternative Splicing, Sequence Analysis, DNA, Protein Structure, Tertiary, DNA, Complementary, src Homology Domains, COS Cells, rab GTP-Binding Proteins, rab3 GTP-Binding Proteins, Two-Hybrid System Techniques, Membrane Transport Proteins, Vesicular Transport Proteins, Adaptor Proteins, Signal Transducing, Rats
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