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Structures of C1q-like proteins reveal unique features among the C1q/TNF superfamily.

Ressl S, Vu BK, Vivona S, Martinelli DC, Südhof TC, Brunger AT
Structure 23 688-99 (2015)
Related entries: 4qpy, 4qq2, 4qqh, 4qqo, 4qqp

Cited: 40 times
EuropePMC logo PMID: 25752542

Abstract

C1q-like (C1QL) -1, -2, and -3 proteins are encoded by homologous genes that are highly expressed in brain. C1QLs bind to brain-specific angiogenesis inhibitor 3 (BAI3), an adhesion-type G-protein coupled receptor that may regulate dendritic morphology by organizing actin filaments. To begin to understand the function of C1QLs, we determined high-resolution crystal structures of the globular C1q-domains of C1QL1, C1QL2, and C1QL3. Each structure is a trimer, with each protomer forming a jelly-roll fold consisting of 10 β strands. Moreover, C1QL trimers may assemble into higher-order oligomers similar to adiponectin and contain four Ca(2+)-binding sites along the trimeric symmetry axis, as well as additional surface Ca(2+)-binding sites. Mutation of Ca(2+)-coordinating residues along the trimeric symmetry axis lowered the Ca(2+)-binding affinity and protein stability. Our results reveal unique structural features of C1QLs among C1q/TNF superfamily proteins that may be associated with their specific brain functions.

Reviews - 4qql mentioned but not cited (1)

  1. Neurexins - versatile molecular platforms in the synaptic cleft. Rudenko G. Curr Opin Struct Biol 54 112-121 (2019)

Articles - 4qql mentioned but not cited (1)

  1. Crystallographically correct but confusing presentation of structural models deposited in the Protein Data Bank. Dauter Z, Wlodawer A. Acta Crystallogr D Struct Biol 74 939-945 (2018)


Reviews citing this publication (9)

  1. Synaptic Neurexin Complexes: A Molecular Code for the Logic of Neural Circuits. Südhof TC. Cell 171 745-769 (2017)
  2. Adhesion G protein-coupled receptors in nervous system development and disease. Langenhan T, Piao X, Monk KR. Nat Rev Neurosci 17 550-561 (2016)
  3. Mechanisms of adhesion G protein-coupled receptor activation. Vizurraga A, Adhikari R, Yeung J, Yu M, Tall GG. J Biol Chem 295 14065-14083 (2020)
  4. The C1q complement family of synaptic organizers: not just complementary. Yuzaki M. Curr Opin Neurobiol 45 9-15 (2017)
  5. Regulation of Hepcidin by Erythropoiesis: The Story So Far. Pasricha SR, McHugh K, Drakesmith H. Annu Rev Nutr 36 417-434 (2016)
  6. Structural commonality of C1q TNF-related proteins and their potential to activate relaxin/insulin-like family peptide receptor 1 signalling pathways in cancer cells. Klonisch T, Glogowska A, Thanasupawat T, Burg M, Krcek J, Pitz M, Jaggupilli A, Chelikani P, Wong GW, Hombach-Klonisch S. Br J Pharmacol 174 1025-1033 (2017)
  7. Asparaginase treatment side-effects may be due to genes with homopolymeric Asn codons (Review-Hypothesis). Banerji J. Int J Mol Med 36 607-626 (2015)
  8. Complement 1q/Tumor Necrosis Factor-Related Proteins (CTRPs): Structure, Receptors and Signaling. Schanbacher C, Hermanns HM, Lorenz K, Wajant H, Lang I. Biomedicines 11 559 (2023)
  9. Invertebrate C1q Domain-Containing Proteins: Molecular Structure, Functional Properties and Biomedical Potential. Grinchenko A, Buriak I, Kumeiko V. Mar Drugs 21 570 (2023)

Articles citing this publication (29)

  1. Single cell transcriptomic analysis of human pluripotent stem cell chondrogenesis. Wu CL, Dicks A, Steward N, Tang R, Katz DB, Choi YR, Guilak F. Nat Commun 12 362 (2021)
  2. Expression of C1ql3 in Discrete Neuronal Populations Controls Efferent Synapse Numbers and Diverse Behaviors. Martinelli DC, Chew KS, Rohlmann A, Lum MY, Ressl S, Hattar S, Brunger AT, Missler M, Südhof TC. Neuron 91 1034-1051 (2016)
  3. Conformational Plasticity in the Transsynaptic Neurexin-Cerebellin-Glutamate Receptor Adhesion Complex. Cheng S, Seven AB, Wang J, Skiniotis G, Özkan E. Structure 24 2163-2173 (2016)
  4. A Synaptic Circuit Required for Acquisition but Not Recall of Social Transmission of Food Preference. Wang CY, Liu Z, Ng YH, Südhof TC. Neuron 107 144-157.e4 (2020)
  5. Distinct Subunit Domains Govern Synaptic Stability and Specificity of the Kainate Receptor. Straub C, Noam Y, Nomura T, Yamasaki M, Yan D, Fernandes HB, Zhang P, Howe JR, Watanabe M, Contractor A, Tomita S. Cell Rep 16 531-544 (2016)
  6. Complement 1q-like-3 protein inhibits insulin secretion from pancreatic β-cells via the cell adhesion G protein-coupled receptor BAI3. Gupta R, Nguyen DC, Schaid MD, Lei X, Balamurugan AN, Wong GW, Kim JA, Koltes JE, Kimple ME, Bhatnagar S. J Biol Chem 293 18086-18098 (2018)
  7. Adiponectin and related C1q/TNF-related proteins bind selectively to anionic phospholipids and sphingolipids. Ye JJ, Bian X, Lim J, Medzhitov R. Proc Natl Acad Sci U S A 117 17381-17388 (2020)
  8. Effect of calcium ions on structure and stability of the C1q-like domain of otolin-1 from human and zebrafish. Hołubowicz R, Wojtas M, Taube M, Kozak M, Ożyhar A, Dobryszycki P. FEBS J 284 4278-4297 (2017)
  9. Anatomical and Behavioral Investigation of C1ql3 in the Mouse Suprachiasmatic Nucleus. Chew KS, Fernandez DC, Hattar S, Südhof TC, Martinelli DC. J Biol Rhythms 32 222-236 (2017)
  10. RNA-Seq reveals a central role for lectin, C1q and von Willebrand factor A domains in the defensive glue of a terrestrial slug. Smith AM, Papaleo C, Reid CW, Bliss JM. Biofouling 33 741-754 (2017)
  11. Extracellular matrix and synapse formation. Yang L, Wei M, Xing B, Zhang C. Biosci Rep 43 BSR20212411 (2023)
  12. Functional Characterization of OXYL, A SghC1qDC LacNAc-specific Lectin from The Crinoid Feather Star Anneissia Japonica. Hasan I, Gerdol M, Fujii Y, Ozeki Y. Mar Drugs 17 E136 (2019)
  13. Protein Modifications Critical for Myonectin/Erythroferrone Secretion and Oligomer Assembly. Stewart AN, Little HC, Clark DJ, Zhang H, Wong GW. Biochemistry 59 2684-2697 (2020)
  14. C1ql1 is expressed in adult outer hair cells of the cochlea in a tonotopic gradient. Biswas J, Pijewski RS, Makol R, Miramontes TG, Thompson BL, Kresic LC, Burghard AL, Oliver DL, Martinelli DC. PLoS One 16 e0251412 (2021)
  15. CTRP11 contributes modestly to systemic metabolism and energy balance. Sarver DC, Xu C, Carreno D, Arking A, Terrillion CE, Aja S, Wong GW. FASEB J 36 e22347 (2022)
  16. CTRP14 inactivation alters physical activity and food intake response to fasting and refeeding. Sarver DC, Xu C, Aja S, Wong GW. Am J Physiol Endocrinol Metab 322 E480-E493 (2022)
  17. A tick C1q protein alters infectivity of the Lyme disease agent by modulating interferon γ. Tang X, Arora G, Matias J, Hart T, Cui Y, Fikrig E. Cell Rep 41 111673 (2022)
  18. C1QL1/CTRP14 Is Largely Dispensable for Atherosclerosis Formation in Apolipoprotein-E-Deficient Mice. Guan H, Shi T, Liu M, Wang X, Guo F. J Cardiovasc Dev Dis 9 341 (2022)
  19. Molecular mechanism of calcium induced trimerization of C1q-like domain of otolin-1 from human and zebrafish. Hołubowicz R, Ożyhar A, Dobryszycki P. Sci Rep 11 12778 (2021)
  20. Bdellovibrio bacteriovorus uses chimeric fibre proteins to recognize and invade a broad range of bacterial hosts. Caulton SG, Lambert C, Tyson J, Radford P, Al-Bayati A, Greenwood S, Banks EJ, Clark C, Till R, Pires E, Sockett RE, Lovering AL. Nat Microbiol 9 214-227 (2024)
  21. CTRP13 ablation improves systemic glucose and lipid metabolism. Chen F, Sarver DC, Saqib M, Zhou M, Aja S, Seldin MM, Wong GW. Mol Metab 78 101824 (2023)
  22. Crystallographic characterization of a tri-Asp metal-binding site at the three-fold symmetry axis of LarE. Fellner M, Huizenga KG, Hausinger RP, Hu J. Sci Rep 10 5830 (2020)
  23. Epigenetically distinct synaptic architecture in clonal compartments in the teleostean dorsal pallium. Isoe Y, Nakamura R, Nonaka S, Kamei Y, Okuyama T, Yamamoto N, Takeuchi H, Takeda H. Elife 12 e85093 (2023)
  24. N-Linked Glycosylation-Dependent and -Independent Mechanisms Regulating CTRP12 Cleavage, Secretion, and Stability. Stewart AN, Tan SY, Clark DJ, Zhang H, Wong GW. Biochemistry 58 727-741 (2019)
  25. Structural Arrangement Produced by Concanavalin A Binding to Homomeric GluK2 Receptors. Gonzalez CU, Carrillo E, Berka V, Jayaraman V. Membranes (Basel) 11 613 (2021)
  26. A C1qTNF3 collagen domain fusion chaperones diverse secreted proteins and anti-Aβ scFvs: Applications for gene therapies. Moore BD, Ran Y, Goodwin MS, Komatineni K, McFarland KN, Dillon K, Charles C, Ryu D, Liu X, Prokop S, Giasson BI, Golde TE, Levites Y. Mol Ther Methods Clin Dev 31 101146 (2023)
  27. Characterization of erythroferrone oligomerization and its impact on BMP antagonism. Mast JF, Leach EAE, Thompson TB. J Biol Chem 300 105452 (2024)
  28. Deletion of large-conductance calcium-activated potassium channels promotes vascular remodelling through the CTRP7-mediated PI3K/Akt signaling pathway. Bi J, Duan Y, Wang M, He C, Li X, Zhang X, Tao Y, Du Y, Liu H. Acta Biochim Biophys Sin (Shanghai) 54 1-11 (2022)
  29. Glycosylation of Cblns attenuates their receptor binding. Rong Y, Bansal PK, Wei P, Guo H, Correia K, Parris J, Morgan JI. Brain Res 1694 129-139 (2018)


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