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PMID: 12415118 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Time-lapse imaging of a dynamic phosphorylation-dependent protein-protein interaction in mammalian cells.

Spotts JM, Dolmetsch RE, Greenberg ME

Abstract

The ability to make sensitive measurements of protein-protein interaction kinetics in single neurons is critical for understanding the molecular and cellular basis of neuronal function. We have developed a reporter technology based on the differential induction of Escherichia coli TEM-1 beta-lactamase (Bla) enzymatic activity that can function as a sensor of the interaction state of two target proteins within single neurons in vivo. To modulate Bla enzymatic activity, we first split the enzyme into two separate, complementary protein fragments that we identified by using a functional screening approach based on circular permutation of the Bla enzyme. The split enzyme was then brought together by the phosphorylation-dependent association of the kinase inducible domain of the cAMP response element binding protein (CREB) and the KIX domain of the CREB binding protein. Using an intracellular substrate whose fluorescence spectrum changes after hydrolysis by Bla, we performed time-lapse ratiometric imaging measurements of Bla enzymatic induction after association of the CREB and CREB binding protein interaction domains. This approach permits direct imaging of protein-protein interactions in single cells with high signal discrimination.

MeSH Terms
Cell Line Cells, Cultured Cerebral Cortex/physiology Enzymes/metabolism Escherichia coli/enzymology Humans Kinetics Microscopy, Video Models, Neurological Neurons/microbiology,physiology Phosphorylation Time Factors Transfection beta-Lactamases/metabolism
Chemicals
Enzymes beta-Lactamases beta-lactamase TEM-1
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Spotts James M
Division of Neuroscience, John F. Enders Pediatric Laboratories, Children's Hospital, 300 Longwood Avenue, Boston, MA 02115, USA.
Dolmetsch Ricardo E
Greenberg Michael E
References (30)
30 references, click to expand
  1. Circularly permuted beta-lactamase from Staphylococcus aureus PC1.
    Biochemistry. 1997 Jul 22;36(29):8767-74 PMID: 9220963
  2. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism.
    J Neurosci. 1996 Sep 1;16(17):5425-36 PMID: 8757255
  3. Quantitation of transcription and clonal selection of single living cells with beta-lactamase as reporter.
    Science. 1998 Jan 2;279(5347):84-8 PMID: 9417030
  4. A bioluminescence resonance energy transfer (BRET) system: application to interacting circadian clock proteins.
    Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):151-6 PMID: 9874787
  5. Random circular permutation of DsbA reveals segments that are essential for protein folding and stability.
    J Mol Biol. 1999 Mar 5;286(4):1197-215 PMID: 10047491
  6. Circularly permuted variants of the green fluorescent protein.
    FEBS Lett. 1999 Aug 27;457(2):283-9 PMID: 10471794
  7. Interaction blues: protein interactions monitored in live mammalian cells by beta-galactosidase complementation.
    Trends Cell Biol. 2000 Mar;10(3):119-22 PMID: 10675906
  8. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals.
    Annu Rev Biochem. 1999;68:821-61 PMID: 10872467
  9. Detection of protein-protein interactions by protein fragment complementation strategies.
    Methods Enzymol. 2000;328:208-30 PMID: 11075347
  10. Imaging FRET between spectrally similar GFP molecules in single cells.
    Nat Biotechnol. 2001 Feb;19(2):167-9 PMID: 11175733
  11. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1.
    Nature. 2001 Jun 28;411(6841):1065-8 PMID: 11429608
  12. Distinct effects of cAMP and mitogenic signals on CREB-binding protein recruitment impart specificity to target gene activation via CREB.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10936-41 PMID: 11535812
  13. Detection of protein-protein interactions in vivo based on protein splicing.
    Curr Opin Chem Biol. 2001 Oct;5(5):578-83 PMID: 11578933
  14. Measurement of molecular interactions in living cells by fluorescence resonance energy transfer between variants of the green fluorescent protein.
    Sci STKE. 2000 Jun 27;2000(38):pl1 PMID: 11752595
  15. Biological and chemical applications of fluorescence correlation spectroscopy: a review.
    Biochemistry. 2002 Jan 22;41(3):697-705 PMID: 11790090
  16. Protein-protein interactions monitored in mammalian cells via complementation of beta -lactamase enzyme fragments.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3469-74 PMID: 11904411
  17. Beta-lactamase protein fragment complementation assays as in vivo and in vitro sensors of protein protein interactions.
    Nat Biotechnol. 2002 Jun;20(6):619-22 PMID: 12042868
  18. Novel method for detection of beta-lactamases by using a chromogenic cephalosporin substrate.
    Antimicrob Agents Chemother. 1972 Apr;1(4):283-8 PMID: 4208895
  19. beta-Lactamase detection by three simple methods: Intralactam, nitrocefin and acidimetric.
    J Antimicrob Chemother. 1980 Sep;6(5):617-21 PMID: 6997258
  20. Both isoforms of the cAMP-dependent protein kinase catalytic subunit can activate transcription of the prolactin gene.
    J Biol Chem. 1989 Apr 25;264(12):6870-3 PMID: 2540166
  21. A standard numbering scheme for the class A beta-lactamases.
    Biochem J. 1991 May 15;276 ( Pt 1):269-70 PMID: 2039479
  22. CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases.
    Science. 1991 Jun 7;252(5011):1427-30 PMID: 1646483
  23. Protein-kinase-A-dependent activator in transcription factor CREB reveals new role for CREM repressors.
    Nature. 1993 Aug 26;364(6440):821-4 PMID: 8102791
  24. Crystal structure of Escherichia coli TEM1 beta-lactamase at 1.8 A resolution.
    Proteins. 1993 Aug;16(4):364-83 PMID: 8356032
  25. Phosphorylated CREB binds specifically to the nuclear protein CBP.
    Nature. 1993 Oct 28;365(6449):855-9 PMID: 8413673
  26. Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB.
    Cell. 1994 Jun 3;77(5):713-25 PMID: 8205620
  27. Nuclear protein CBP is a coactivator for the transcription factor CREB.
    Nature. 1994 Jul 21;370(6486):223-6 PMID: 7913207
  28. Serine 133-phosphorylated CREB induces transcription via a cooperative mechanism that may confer specificity to neurotrophin signals.
    Mol Cell Neurosci. 1995 Apr;6(2):168-83 PMID: 7551568
  29. Phosphorylation of CREB at Ser-133 induces complex formation with CREB-binding protein via a direct mechanism.
    Mol Cell Biol. 1996 Feb;16(2):694-703 PMID: 8552098
  30. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator:coactivator interactions.
    Cell. 1997 Dec 12;91(6):741-52 PMID: 9413984
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-11-12
Epub
2002-00-01
Pages
15142-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC137557
Subset
IM
Grants
NINDS NIH HHS · R37 NS028829 · United States
NINDS NIH HHS · NS28829 · United States
NINDS NIH HHS · R01 NS028829 · United States
NICHD NIH HHS · P30 HD018655 · United States
NICHD NIH HHS · P30-HD18655 · United States
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