Agonist-induced Ca2+ sensitization in smooth muscle: Redundancy of Rho guanine nucleotide exchange factors (RhoGEFs) and response kinetics, a caged compound study

Journal of Biological Chemistry

Volumn 288, Issue 47, 2013, Pages 34030-34040

  Artamonov, Mykhaylo V ^a   Momotani, Ko ^a   Stevenson, Andra ^c   Trentham, David R ^d   Derewenda, Urszula ^a   Derewenda, Zygmunt S ^a   Read, Paul W ^b   Silvio Gutkind, J ^e   Somlyo, Avril V ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CHEMICAL ACTIVATION; MUSCLE; NUCLEOTIDES; PHOTOLYSIS; POSITIVE IONS; PROTEINS;

C-TERMINAL DOMAINS; CAGED COMPOUNDS; CONTRACTILE FORCE; G PROTEIN COUPLED RECEPTORS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HETERODIMERIZATION; HETEROTRIMERIC G PROTEINS; RESPONSE KINETICS;

BLOOD VESSELS;

CALCIUM ION; ENDOTHELIN 1; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); LEUKEMIA ASSOCIATED RHOGEF; MESSENGER RNA; PHENYLEPHRINE; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SHORT HAIRPIN RNA; THROMBOXANE A2; UNCLASSIFIED DRUG; 1-(2-NITRO)PHENYLETHYL-P(3)-GUANOSINE 5'-O-(3-THIO)TRIPHOSPHATE; ARHGEF11 PROTEIN, HUMAN; ARHGEF11 PROTEIN, MOUSE; ARHGEF12 PROTEIN, HUMAN; ARHGEF12 PROTEIN, MOUSE; ARHGEF12 PROTEIN, RAT; CALCIUM; ENDOTHELIN A RECEPTOR; N-2-NITROBENZYLPHENYLEPHRINE; PDZ-RHOGEF, RAT; RECOMBINANT PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; RHOA PROTEIN, HUMAN; RHOA PROTEIN, MOUSE; THROMBOXANE A2 RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SENSITIZATION; DIMERIZATION; ENZYME ACTIVATION; LIGHT CHAIN; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SENSITIZATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; CELL LINE; DRUG EFFECTS; GENE SILENCING; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; ORGAN CULTURE TECHNIQUE; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; RABBIT; RAT;

MUS;

ANIMALS; CALCIUM; CELL LINE; GENE SILENCING; GUANINE NUCLEOTIDE EXCHANGE FACTORS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; MICE; MICE, KNOCKOUT; ORGAN CULTURE TECHNIQUES; PHENYLEPHRINE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RABBITS; RATS; RECEPTOR, ENDOTHELIN A; RECEPTORS, THROMBOXANE A2, PROSTAGLANDIN H2; RECOMBINANT PROTEINS; RHO GTP-BINDING PROTEINS; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; RHO-SPECIFIC GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; RHOA GTP-BINDING PROTEIN;

EID: 85047688254     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.514596     Document Type: Article

References (49)

1. Somlyo, A. P., and Somlyo, A. V. (1994) Signal transduction and regulation in smooth muscle. Nature 372, 231-236
2. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83, 1325-1358
3. Hong, F., Haldeman, B. D., Jackson, D., Carter, M., Baker, J. E., and Cremo, C. R. (2011) Biochemistry of smooth muscle myosin light chain kinase. Arch. Biochem. Biophys. 510, 135-146
4. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248
5. Ichikawa, K., Ito, M., and Hartshorne, D. J. (1996) Phosphorylation of the large subunit of myosin phosphatase and inhibition of phosphatase activity. J. Biol. Chem. 271, 4733-4740
6. Wettschureck, N., and Offermanns, S. (2002) Rho/Rho-kinase mediated signaling in physiology and pathophysiology. J. Mol. Med. 80, 629-638
7. Rossman, K. L., Der, C. J., and Sondek, J. (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167-180
8. Jaiswal, M., Dvorsky, R., and Ahmadian, M. R. (2013) Deciphering the molecular and functional basis of Dbl family proteins: a novel systematic approach toward classification of selective activation of the Rho family proteins. J. Biol. Chem. 288, 4486-4500
9. Wirth, A., Benyo, Z., Lukasova, M., Leutgeb, B., Wettschureck, N., Gorbey, S., Orsy, P., Horvath, B., Maser-Gluth, C., Greiner, E., Lemmer, B., Schütz, G., Gutkind, J. S., and Offermanns, S. (2008) G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat. Med. 14, 64-68
10. Wuertz, C. M., Lorincz, A., Vettel, C., Thomas, M. A., Wieland, T., and Lutz, S. (2010) p63RhoGEF-a key mediator of angiotensin II-dependent signaling and processes in vascular smooth muscle cells. FASEB J. 24, 4865-4876
11. 2+ sensitization of vascular smooth muscle contractility. Circ. Res. 109, 993-1002
12. Momotani, K., and Somlyo, A. V. (2012) p63RhoGEF: a new switch for Gq-mediated activation of smooth muscle. Trends Cardiovasc. Med. 22, 122-127
13. 12 family to Rho. FEBS Lett. 485, 183-188
14. Fukuhara, S., Murga, C., Zohar, M., Igishi, T., and Gutkind, J. S. (1999) A novel PDZ domain containing guanine nucleotide exchange factor links heterotrimeric G proteins to Rho. J. Biol. Chem. 274, 5868-5879
15. 13. Science 280, 2109-2111
16. Longenecker, K. L., Lewis, M. E., Chikumi, H., Gutkind, J. S., and Derewenda, Z. S. (2001) Structure of the RGS-like domain from PDZ-RhoGEF: linking heterotrimeric G protein-coupled signaling to Rho GTPases. Structure 9, 559-569
17. Guilluy, C, Bregeon, J., Toumaniantz, G., Rolli-Derkinderen, M., Retailleau, K., Loufrani, L., Henrion, D., Scalbert, E., Bril, A., Torres, R. M., Offermanns, S., Pacaud, P., and Loirand, G. (2010) The Rho exchange factor Arhgef1 mediates the effects of angiotensin II on vascular tone and blood pressure. Nat Med. 16, 183-190
18. Mikelis, C. M., Palmby, T. R., Simaan, M., Li, W., Szabo, R., Lyons, R., Martin, D., Yagi, H, Fukuhara, S., Chikumi, H., Galisteo, R., Mukouyama, Y., Bugge, T. H., and Gutkind, J. S. (2013) PDZ-RhoGEF and LARG are essential for embryonic development and provide a link between thrombin and LPA receptors and Rho activation. J. Biol. Chem. 288, 12232-12243
19. Yoshida, T., Sinha, S., Dandré, F., Wamhoff, B. R., Hoofnagle, M. H, Kremer, B. E., Wang, D. Z., Olson, E. N., and Owens, G. K. (2003) Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ. Res. 92, 856-864
20. 2+ release and contraction induced by photolysis of caged D-myo-inositol 1, 4, 5-trisphosphate in smooth muscle. The effects of heparin, procaine, and adenine nucleotides. J. Biol. Chem. 267, 22316-22322
21. Somlyo, A. V., Goldman, Y. E., Fujimori, T., Bond, M., Trentham, D. R., and Somlyo, A. P. (1988) Cross-bridge kinetics, cooperativity, and negatively strained cross-bridges in vertebrate smooth muscle. A laser-flash photolysis study. J. Gen. Physiol. 91, 165-192
22. Goldman, Y. E., Hibberd, M. G., and Trentham, D. R. (1984) Initiation of active contraction by photogeneration of adenosine-5'-triphosphate in rabbit psoas muscle fibres. J. Physiol. 354, 605-624
23. McCray, J. A, and Trentham, D. R. (1989) Properties and uses of photoreactive caged compounds. Annu. Rev. Biophys. Biophys. Chem. 18, 239-270
24. Read, P. W., Liu, X., Longenecker, K., Dipierro, C. G., Walker, L. A., Somlyo, A. V., Somlyo, A. P., and Nakamoto, R. K. (2000) Human RhoA/RhoGDI complex expressed in yeast: GTP exchange is sufficient for translocation of RhoA to liposomes. Protein Sci. 9, 376-386
25. Scheidig, A. J., Franken, S. M., Corrie, J. E., Reid, G. P., Wittinghofer, A., Pai, E. F., and Goody, R. S. (1995) X-ray crystal structure analysis of the catalytic domain of the oncogene product p21H-ras complexed with caged GTP and mant dGppNHp. J. Mol. Biol. 253, 132-150
26. 3-1-(2-nitrophenyl) ethyl adenosine triphosphate ('caged ATP'). J. Chem. Soc. Perkin Trans. 1, 1015-1019
27. Sheffield, P., Garrard, S., and Derewenda, Z. (1999) Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Protein Expr. Purif. 15, 34-39
28. Neppl, R. L., Lubomirov, L. T., Momotani, K., Pfitzer, G., Eto, M., and Somlyo, A. V. (2009) Thromboxane A2-induced bi-directional regulation of cerebral arterial tone. J. Biol. Chem. 284, 6348-6360
29. Walker, J. W., and Trentham, D. R. (1988) Caged phenylephrine synthesis and photochemical properties. Biophys. J. 53, A596
30. Walker, J. W., Martin, H., Schmitt, F. R., and Barsotti, R. J. (1993) Rapid release of an α-adrenergic receptor ligand from photolabile analogs. Biochemistry 32, 1338-1345
31. Walker, J. W., Reid, G. P., and Trentham, D. R. (1989) Synthesis and properties of caged nucleotides. Methods Enzymol. 172, 288-301
32. Grabocka, E., and Wedegaertner, P. B. (2007) Disruption of oligomerization induces nucleocytoplasmic shuttling of leukemia-associated Rho guanine-nucleotide exchange factor. Mol. Pharmacol. 72, 993-1002
33. Chikumi, H, Barac, A., Behbahani, B., Gao, Y., Teramoto, H., Zheng, Y, and Gutkind, J. S. (2004) Homo- and hetero-oligomerization of PDZ-RhoGEF, LARG and p115RhoGEF by their C-terminal region regulates their in vivo Rho GEF activity and transforming potential. Oncogene 23, 233-240
34. Horiuti, K., Somlyo, A. V., Goldman, Y. E., and Somlyo, A. P. (1989) Kinetics of contraction initiated by flash photolysis of caged adenosine triphosphate in tonic and phasic smooth muscles. J. Gen. Physiol. 94, 769-781
35. Chen, Z., Singer, W. D., Sternweis, P. C, and Sprang, S. R. (2005) Structure of the p115RhoGEF rgRGS domain-Gα13/i1 chimera complex suggests convergent evolution of a GTPase activator. Nat. Struct. Mol. Biol. 12, 191-197
36. Cario-Toumaniantz, C, Ferland-McCollough, D., Chadeuf, G., Toumaniantz, G., Rodriguez, M., Galizzi, J. P., Lockhart, B., Bril, A., Scalbert, E., Loirand, G., and Pacaud, P. (2012) RhoA guanine exchange factor expression profile in arteries: evidence for a Rho kinase-dependent negative feedback in angiotensin II-dependent hypertension. Am. J. Physiol. Cell Physiol. 302, C1394-C1404
37. 2+ sensitization pathway in smooth muscle. Structure 12, 1955-1965
38. Pfreimer, M., Vatter, P., Langer, T., Wieland, T., Gierschik, P., and Moepps, B. (2012) LARG links histamine-H1-receptor-activated Gq to Rho-GTPase-dependent signaling pathways. Cell. Signal. 24, 652-663
39. Gohla, A., Schultz, G., and Offermanns, S. (2000) Role for G12/G13 in agonist-induced vascular smooth muscle cell contraction. Circ. Res. 87, 221-227
40. Oleksy, A., Opaliński, Ł., Derewenda, U., Derewenda, Z. S., and Otlewski, J. (2006) The molecular basis of RhoA specificity in the guanine nucleotide exchange factor PDZ-RhoGEF. J. Biol. Chem. 281, 32891-32897
41. Jaiswal, M., Gremer, L., Dvorsky, R., Haeusler, L. C, Cirstea, I. C, Uhlenbrock, K., and Ahmadian, M. R. (2011) Mechanistic insights into specificity, activity and regulatory elements of the RGS-containing Rho-specific guanine nucleotide exchange factors p115, PDZ-RhoGEF (PRG) and leukemia-associated RhoGEF (LARG). J. Biol. Chem. 286, 18202-18212
42. Aittaleb, M., Nishimura, A., Linder, M. E., and Tesmer, J. J. (2011) Plasma membrane association of p63 Rho guanine nucleotide exchange factor (p63RhoGEF) is mediated by palmitoylation and is required for basal activity in cells. J. Biol. Chem. 286, 34448-34456
43. Shankaranarayanan, A., Boguth, C. A., Lutz, S., Vettel, C, Uhlemann, F., Aittaleb, M., Wieland, T., and Tesmer, J. J. (2010) Gαq allosterically activates and relieves autoinhibition of p63RhoGEF. Cell. Signal. 22, 1114-1123
44. Hein, P., Frank, M., Hoffmann, C., Lohse, M. J., and Bünemann, M. (2005) Dynamics of receptor/G protein coupling in living cells. EMBO J. 24, 4106-4114
45. Adjobo-Hermans, M. J., Goedhart, J., Van Weeren, L., Nijmeijer, S., Manders, E. M., Offermanns, S., and Gadella, T. W. (2011) Real-time visualization of heterotrimeric G protein Gq activation in living cells. BMC Biol. 9, 32
46. Bünemann, M., Frank, M., and Lohse, M. J. (2003) Gi protein activation in intact cells involves subunit rearrangement rather than dissociation. Proc. Natl. Acad. Sci. U. S. A. 100, 16077-16082
47. Hein, P., Rochais, F., Hoffmann, C., Dorsch, S., Nikolaev, V. O., Engelhardt, S., Berlot, C. H., Lohse, M. J., and Bünemann, M. (2006) Gs activation is time-limiting in initiating receptor-mediated signaling. J. Biol. Chem. 281, 33345-33351
48. Medina, F., Carter, A. M., Dada, O., Gutowski, S., Hadas, J., Chen, Z., and Sternweis, P. C (2013) Activated RhoA is a positive feedback regulator of the Lbc family of Rho guanine nucleotide exchange factor proteins. J. Biol. Chem. 288, 11325-11333
49. Groves, J. T., and Kuriyan, J. (2010) Molecular mechanisms in signal transduction at the membrane. Nat Struct. Mol. Biol. 17, 659-665