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Solution structure of the calponin homology (CH) domain from the smoothelin-like 1 protein: a unique apocalmodulin-binding mode and the possible role of the C-terminal type-2 CH-domain in smooth muscle relaxation.

Ishida H, Borman MA, Ostrander J, Vogel HJ, MacDonald JA
J Biol Chem 283 20569-78 (2008)
Cited: 23 times
EuropePMC logo PMID: 18477568

Abstract

The SMTNL1 protein contains a single type-2 calponin homology (CH) domain at its C terminus that shares sequence identity with the smoothelin family of smooth muscle-specific proteins. In contrast to the smoothelins, SMTNL1 does not associate with F-actin in vitro, and its specific role in smooth muscle remains unclear. In addition, the biological function of the C-terminal CH-domains found in the smoothelin proteins is also poorly understood. In this work, we have therefore determined the solution structure of the CH-domain of mouse SMTNL1 (SMTNL1-CH; residues 346-459). The secondary structure and the overall fold for the C-terminal type-2 CH-domain is very similar to that of other CH-domains. However, two clusters of basic residues form a unique surface structure that is characteristic of SMTNL1-CH. Moreover, the protein has an extended C-terminal alpha-helix, which contains a calmodulin (CaM)-binding IQ-motif, that is also a distinct feature of the smoothelins. We have characterized the binding of apo-CaM to SMTNL1-CH through its IQ-motif by isothermal titration calorimetry and NMR chemical shift perturbation studies. In addition, we have used the HADDOCK protein-protein docking approach to construct a model for the complex of apo-CaM and SMTNL1-CH. The model revealed a close interaction of SMTNL1-CH with the two Ca(2+) binding loop regions of the C-terminal domain of apo-CaM; this mode of apo-CaM binding is distinct from previously reported interactions of apo-CaM with IQ-motifs. Finally, we comment on the putative role of the CH-domain in the biological function of SMTNL1.

Reviews citing this publication (5)

  1. Survey of the year 2008: applications of isothermal titration calorimetry. Falconer RJ, Penkova A, Jelesarov I, Collins BM. J Mol Recognit 23 395-413 (2010)
  2. Novel contributions of the smoothelin-like 1 protein in vascular smooth muscle contraction and its potential involvement in myogenic tone. Turner SR, MacDonald JA. Microcirculation 21 249-258 (2014)
  3. Structural Characteristics, Binding Partners and Related Diseases of the Calponin Homology (CH) Domain. Yin LM, Schnoor M, Jun CD. Front Cell Dev Biol 8 342 (2020)
  4. Structure and Emerging Functions of LRCH Proteins in Leukocyte Biology. Rivière T, Bader A, Pogoda K, Walzog B, Maier-Begandt D. Front Cell Dev Biol 8 584134 (2020)
  5. MICAL-mediated oxidation of actin and its effects on cytoskeletal and cellular dynamics. Rajan S, Terman JR, Reisler E. Front Cell Dev Biol 11 1124202 (2023)

Articles citing this publication (18)

  1. Thermodynamic effects of noncoded and coded methionine substitutions in calmodulin. Yamniuk AP, Ishida H, Lippert D, Vogel HJ. Biophys J 96 1495-1507 (2009)
  2. Smoothelin-like 1 protein regulates myosin phosphatase-targeting subunit 1 expression during sexual development and pregnancy. Lontay B, Bodoor K, Weitzel DH, Loiselle D, Fortner C, Lengyel S, Zheng D, Devente J, Hickner R, Haystead TA. J Biol Chem 285 29357-29366 (2010)
  3. The role of the calponin homology domain of smoothelin-like 1 (SMTNL1) in myosin phosphatase inhibition and smooth muscle contraction. Borman MA, Freed TA, Haystead TA, Macdonald JA. Mol Cell Biochem 327 93-100 (2009)
  4. The Calcium-Dependent Switch Helix of L-Plastin Regulates Actin Bundling. Ishida H, Jensen KV, Woodman AG, Hyndman ME, Vogel HJ. Sci Rep 7 40662 (2017)
  5. Specific 12CβD(2)12CγD(2)S13CεHD(2) isotopomer labeling of methionine to characterize protein dynamics by 1H and 13C NMR relaxation dispersion. Weininger U, Liu Z, McIntyre DD, Vogel HJ, Akke M. J Am Chem Soc 134 18562-18565 (2012)
  6. Smoothelin-like 1 protein is a bifunctional regulator of the progesterone receptor during pregnancy. Bodoor K, Lontay B, Safi R, Weitzel DH, Loiselle D, Wei Z, Lengyel S, McDonnell DP, Haystead TA. J Biol Chem 286 31839-31851 (2011)
  7. A calcium-dependent interaction between calmodulin and the calponin homology domain of human IQGAP1. Andrews WJ, Bradley CA, Hamilton E, Daly C, Mallon T, Timson DJ. Mol Cell Biochem 371 217-223 (2012)
  8. Conformation of the calmodulin-binding domain of metabotropic glutamate receptor subtype 7 and its interaction with calmodulin. Isozumi N, Iida Y, Nakatomi A, Nemoto N, Yazawa M, Ohki S. J Biochem 149 463-474 (2011)
  9. Mapping and functional characterization of the murine smoothelin-like 1 promoter. Ulke-Lemée A, Turner SR, Mughal SH, Borman MA, Winkfein RJ, MacDonald JA. BMC Mol Biol 12 10 (2011)
  10. Binding orientation and specificity of calmodulin to rat olfactory cyclic nucleotide-gated ion channel. Irene D, Huang JW, Chung TY, Li FY, Tzen JT, Lin TH, Chyan CL. J Biomol Struct Dyn 31 414-425 (2013)
  11. Tropomyosin-binding properties of the CHASM protein are dependent upon its calponin homology domain. Ulke-Lemée A, Ishida H, Borman MA, Valderrama A, Vogel HJ, MacDonald JA. FEBS Lett 584 3311-3316 (2010)
  12. In situ analysis of smoothelin-like 1 and calmodulin interactions in smooth muscle cells by proximity ligation. Ulke-Lemée A, Turner SR, MacDonald JA. J Cell Biochem 116 2667-2675 (2015)
  13. Two domains of the smoothelin-like 1 protein bind apo- and calcium-calmodulin independently. Ulke-Lemée A, Ishida H, Chappellaz M, Vogel HJ, MacDonald JA. Biochim Biophys Acta 1844 1580-1590 (2014)
  14. Binding of smoothelin-like 1 to tropomyosin and calmodulin is mutually exclusive and regulated by phosphorylation. Ulke-Lemée A, Sun DH, Ishida H, Vogel HJ, MacDonald JA. BMC Biochem 18 5 (2017)
  15. Bioinformatic analysis of smoothelin family members supports tissue-specific functions of unique C-terminal calponin homology domains. Garg D, Fisher SA. Physiol Rep 11 e15844 (2023)
  16. The Recognition of Calmodulin to the Target Sequence of Calcineurin-A Novel Binding Mode. Chyan CL, Irene D, Lin SM. Molecules 22 (2017)
  17. Assignment of the 1H, 13C and 15N resonances of the calponin homology-2 domain of alpha-actinin-4. Chen HH, Murchland I, Booker GW. Biomol NMR Assign 2 195-197 (2008)
  18. Redox regulation of KV7 channels through EF3 hand of calmodulin. Nuñez E, Jones F, Muguruza-Montero A, Urrutia J, Aguado A, Malo C, Bernardo-Seisdedos G, Domene C, Millet O, Gamper N, Villarroel A. Elife 12 e81961 (2023)


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