Melatonin production: Proteasomal proteolysis in serotonin N- acetyltransferase regulation

Science

Volumn 279, Issue 5355, 1998, Pages 1358-1360

  Gastel, Jonathan A ^a   Roseboom, Patrick H ^a   Rinaldi, Peter A ^a   Weller, Joan L ^a   Klein, David C ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; CYCLIC AMP; MELATONIN; PROPRANOLOL DERIVATIVE; PROTEASOME;

ARTICLE; CENTRAL NERVOUS SYSTEM; ENZYME REGULATION; NERVE STIMULATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; VERTEBRATE;

ADRENERGIC BETA-AGONISTS; ADRENERGIC BETA-ANTAGONISTS; ANIMALS; ARYLAMINE N-ACETYLTRANSFERASE; BUCLADESINE; CYCLIC AMP; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; ISOPROTERENOL; LIGHT; MELATONIN; MULTIENZYME COMPLEXES; PINEAL GLAND; PROPRANOLOL; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RECEPTORS, ADRENERGIC, BETA;

VERTEBRATA;

EID: 0032570593     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.279.5355.1358     Document Type: Article

References (48)

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2. A. B. Lerner, J. D. Case, Y. Takahashi, J. Biol. Chem. 235, 1992 (1960); J. Axelrod, Science 184, 1341 (1974); J. Arendt, Melatonin and the Mammalian Pineal Gland (Chapman & Hall, London, 1995), pp. 1-273; F. J. Karsch, C. J. I. Woodfill, B. Malpaux, J. E. Robinson, N. L. Wayne, in The Suprachiasmatic Nucleus: The Mind's Clock, D. C. Klein, R. Y. Moore, S. M. Reppert, Eds. (Oxford Univ. Press, New York, 1991), pp. 217-230.
3. A. B. Lerner, J. D. Case, Y. Takahashi, J. Biol. Chem. 235, 1992 (1960); J. Axelrod, Science 184, 1341 (1974); J. Arendt, Melatonin and the Mammalian Pineal Gland (Chapman & Hall, London, 1995), pp. 1-273; F. J. Karsch, C. J. I. Woodfill, B. Malpaux, J. E. Robinson, N. L. Wayne, in The Suprachiasmatic Nucleus: The Mind's Clock, D. C. Klein, R. Y. Moore, S. M. Reppert, Eds. (Oxford Univ. Press, New York, 1991), pp. 217-230.
4. A. B. Lerner, J. D. Case, Y. Takahashi, J. Biol. Chem. 235, 1992 (1960); J. Axelrod, Science 184, 1341 (1974); J. Arendt, Melatonin and the Mammalian Pineal Gland (Chapman & Hall, London, 1995), pp. 1-273; F. J. Karsch, C. J. I. Woodfill, B. Malpaux, J. E. Robinson, N. L. Wayne, in The Suprachiasmatic Nucleus: The Mind's Clock, D. C. Klein, R. Y. Moore, S. M. Reppert, Eds. (Oxford Univ. Press, New York, 1991), pp. 217-230.
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9. D. C. Klein and J. L. Weller, Science 169, 1093 (1970); ibid. 177, 532 (1972); H. Illnerova, Life Sci. 10, 955 (1971); S. Binkley, S. E. Macbride, D. C. Klein, C. L. Ralph, Endocrinology 96, 848 (1975); M. D. Rollag and G. D. Niswender, ibid. 98, 482 (1976).
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11. D. C. Klein, G. R. Berg, J. L. Weller, W. Glinsmann, Science 167, 1738 (1970); M. Brownstein and J. Axelrod, ibid. 184, 163 (1974); D. C. Klein, N. Schaad, M. A. A. Namboodiri, L. Yu, J. L. Weller, Biochem. Soc. Trans. 20, 299 (1992).
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13. 288-302 (accession number p41356) [C. Partidos, C. Stanley, M. Steward, Mol. Immunol. 29, 651 (1992)]. irAA-NAT on protein immunoblots (19) was quantitated with a Storm Phosphor-Imager (Molecular Dynamics) or from nonsaturated autoradiographs (X-O-MAT film, Kodak), which were digitized (Microtek Scanmaker II; Adobe Photoshop, version 3.05) and analyzed with NIH Image version 1.57 software. A unit of immunoreactive protein is approximately equal to the signal generated by ∼30 pg of bacterially expressed rAANAT, determined with As2559. This is 1% of the signal typically generated by a rat pineal gland obtained in the middle of the night [Zeitgeber time (ZT) 21].
14. M. A. A. Namboodiri, R. Dubbels, D. C. Klein, Methods Enzymol. 142, 583 (1986).
15. T. Deguchi and J. Axelrod, Proc. Natl. Acad. Sci. U.S.A. 69, 2547 (1972).
16. J. A. Romero, M. Zatz, J. Axelrod, ibid. 72, 2107 (1975); H. Illnerova, J. Vanecek, J. Krecek, L. Wetterberg, J. Sääf, J. Neurochem. 32, 673 (1979).
17. J. A. Romero, M. Zatz, J. Axelrod, ibid. 72, 2107 (1975); H. Illnerova, J. Vanecek, J. Krecek, L. Wetterberg, J. Sääf, J. Neurochem. 32, 673 (1979).
18. P. H. Roseboom et al., Endocrinology 137, 3033 (1996); M. Bernard et al., J. Neurochem. 68, 213 (1997); D. C. Klein et al., Recent Prog. Hormone Res. 52, 307 (1997).
19. P. H. Roseboom et al., Endocrinology 137, 3033 (1996); M. Bernard et al., J. Neurochem. 68, 213 (1997); D. C. Klein et al., Recent Prog. Hormone Res. 52, 307 (1997).
20. P. H. Roseboom et al., Endocrinology 137, 3033 (1996); M. Bernard et al., J. Neurochem. 68, 213 (1997); D. C. Klein et al., Recent Prog. Hormone Res. 52, 307 (1997).
21. Norepinepherine, isoproteronol, dibutyryl cAMP, and 8-bromocyclic AMP reproducibly increased AA-NAT activity (2) and irAA-NAT (4) in parallel in pineal organ culture (2) and in isolated pinealocytes (20).
22. D. C. Klein, M. J. Buda, C. L. Kapoor, G. Krishna, Science 199, 309 (1978).
23. 32γ]ATP (adenosine triphosphate). 100mM NaCl, 50mM tris-HCI (pH 7.5), 1 mM DTT, 10 mM MgCl, and 33 U of protein kinase A (PKA, Promega); radioactive bands were analyzed and quantitated as described (4). This technique is quantitative within the range of AA-NAT values used in these experiments.
24. Rat pinealocytes or pineal glands were treated in experiments similar to those in Fig. 3. Unless otherwise indicated, the concentration of all protease inhibitors was 100 μM. The following protease inhibitors (targeted class) were ineffective: (serine) PMSF (Sigma), leupeptin (ICN), aprotinin (ICN), N-p-tosyl-L-phenylalanine chloromethyl ketone (Calbiochem); (lysosomal) chloroquine (0.2 mM, Sigma); (aspartic) pepstatin (ICN); (metallo) ethylenediamine tetraacetic acid (Sigma); (cysteine) trans-epoxysuccinyl-L-leucylamido (4-guanidino)butane (Sigma), calpeptin-(Calbiochem), and α-N-acetyl-leucine-leucine-methioninal (Calbiochem). The following protease or proteasome inhibitors preserved more than 50% of the activity or AA-NAT protein compared with drug alone: calpain inhibitor I and Mg115 [K. L. Rock et al., Cell 78, 761 (1994)], Mg132 (V. J. Palombella, O. J. Rando, A. L. Goldberg, T. Maniatis, ibid., p. 773), Z-leucine-leucine-leucine-vinyl sulfone [M. Bogyo et al., Proc. Natl. Acad. Sci. U.S.A. 94, 6629 (1997)], lactacystin [G. Fenteany et al., Science 268, 726 (1995)], and β-clastolactacystin [L. R. Dick, L. Cruikshank, F. D. Grenier, S. L. Melandri, R. L. Stein, J. Biol. Chem. 271, 7273 (1997)].
25. Rat pinealocytes or pineal glands were treated in experiments similar to those in Fig. 3. Unless otherwise indicated, the concentration of all protease inhibitors was 100 μM. The following protease inhibitors (targeted class) were ineffective: (serine) PMSF (Sigma), leupeptin (ICN), aprotinin (ICN), N-p-tosyl-L-phenylalanine chloromethyl ketone (Calbiochem); (lysosomal) chloroquine (0.2 mM, Sigma); (aspartic) pepstatin (ICN); (metallo) ethylenediamine tetraacetic acid (Sigma); (cysteine) trans-epoxysuccinyl-L-leucylamido (4-guanidino)butane (Sigma), calpeptin-(Calbiochem), and α-N-acetyl-leucine-leucine-methioninal (Calbiochem). The following protease or proteasome inhibitors preserved more than 50% of the activity or AA-NAT protein compared with drug alone: calpain inhibitor I and Mg115 [K. L. Rock et al., Cell 78, 761 (1994)], Mg132 (V. J. Palombella, O. J. Rando, A. L. Goldberg, T. Maniatis, ibid., p. 773), Z-leucine-leucine-leucine-vinyl sulfone [M. Bogyo et al., Proc. Natl. Acad. Sci. U.S.A. 94, 6629 (1997)], lactacystin [G. Fenteany et al., Science 268, 726 (1995)], and β-clastolactacystin [L. R. Dick, L. Cruikshank, F. D. Grenier, S. L. Melandri, R. L. Stein, J. Biol. Chem. 271, 7273 (1997)].
26. Rat pinealocytes or pineal glands were treated in experiments similar to those in Fig. 3. Unless otherwise indicated, the concentration of all protease inhibitors was 100 μM. The following protease inhibitors (targeted class) were ineffective: (serine) PMSF (Sigma), leupeptin (ICN), aprotinin (ICN), N-p-tosyl-L-phenylalanine chloromethyl ketone (Calbiochem); (lysosomal) chloroquine (0.2 mM, Sigma); (aspartic) pepstatin (ICN); (metallo) ethylenediamine tetraacetic acid (Sigma); (cysteine) trans-epoxysuccinyl-L-leucylamido (4-guanidino)butane (Sigma), calpeptin-(Calbiochem), and α-N-acetyl-leucine-leucine-methioninal (Calbiochem). The following protease or proteasome inhibitors preserved more than 50% of the activity or AA-NAT protein compared with drug alone: calpain inhibitor I and Mg115 [K. L. Rock et al., Cell 78, 761 (1994)], Mg132 (V. J. Palombella, O. J. Rando, A. L. Goldberg, T. Maniatis, ibid., p. 773), Z-leucine-leucine-leucine-vinyl sulfone [M. Bogyo et al., Proc. Natl. Acad. Sci. U.S.A. 94, 6629 (1997)], lactacystin [G. Fenteany et al., Science 268, 726 (1995)], and β-clastolactacystin [L. R. Dick, L. Cruikshank, F. D. Grenier, S. L. Melandri, R. L. Stein, J. Biol. Chem. 271, 7273 (1997)].
27. Rat pinealocytes or pineal glands were treated in experiments similar to those in Fig. 3. Unless otherwise indicated, the concentration of all protease inhibitors was 100 μM. The following protease inhibitors (targeted class) were ineffective: (serine) PMSF (Sigma), leupeptin (ICN), aprotinin (ICN), N-p-tosyl-L-phenylalanine chloromethyl ketone (Calbiochem); (lysosomal) chloroquine (0.2 mM, Sigma); (aspartic) pepstatin (ICN); (metallo) ethylenediamine tetraacetic acid (Sigma); (cysteine) trans-epoxysuccinyl-L-leucylamido (4-guanidino)butane (Sigma), calpeptin-(Calbiochem), and α-N-acetyl-leucine-leucine-methioninal (Calbiochem). The following protease or proteasome inhibitors preserved more than 50% of the activity or AA-NAT protein compared with drug alone: calpain inhibitor I and Mg115 [K. L. Rock et al., Cell 78, 761 (1994)], Mg132 (V. J. Palombella, O. J. Rando, A. L. Goldberg, T. Maniatis, ibid., p. 773), Z-leucine-leucine-leucine-vinyl sulfone [M. Bogyo et al., Proc. Natl. Acad. Sci. U.S.A. 94, 6629 (1997)], lactacystin [G. Fenteany et al., Science 268, 726 (1995)], and β-clastolactacystin [L. R. Dick, L. Cruikshank, F. D. Grenier, S. L. Melandri, R. L. Stein, J. Biol. Chem. 271, 7273 (1997)].
28. Rat pinealocytes or pineal glands were treated in experiments similar to those in Fig. 3. Unless otherwise indicated, the concentration of all protease inhibitors was 100 μM. The following protease inhibitors (targeted class) were ineffective: (serine) PMSF (Sigma), leupeptin (ICN), aprotinin (ICN), N-p-tosyl-L-phenylalanine chloromethyl ketone (Calbiochem); (lysosomal) chloroquine (0.2 mM, Sigma); (aspartic) pepstatin (ICN); (metallo) ethylenediamine tetraacetic acid (Sigma); (cysteine) trans-epoxysuccinyl-L-leucylamido (4-guanidino)butane (Sigma), calpeptin-(Calbiochem), and α-N-acetyl-leucine-leucine-methioninal (Calbiochem). The following protease or proteasome inhibitors preserved more than 50% of the activity or AA-NAT protein compared with drug alone: calpain inhibitor I and Mg115 [K. L. Rock et al., Cell 78, 761 (1994)], Mg132 (V. J. Palombella, O. J. Rando, A. L. Goldberg, T. Maniatis, ibid., p. 773), Z-leucine-leucine-leucine-vinyl sulfone [M. Bogyo et al., Proc. Natl. Acad. Sci. U.S.A. 94, 6629 (1997)], lactacystin [G. Fenteany et al., Science 268, 726 (1995)], and β-clastolactacystin [L. R. Dick, L. Cruikshank, F. D. Grenier, S. L. Melandri, R. L. Stein, J. Biol. Chem. 271, 7273 (1997)].
29. 2-terminal lysine residue is present in all known vertebrate AA-NAT sequences; this region is important for regulation of AA-NAT activity and irAA-NAT by cAMP and proteosome inhibitors in C6 glioma cells transiently transfected with AA-NAT (J. A. Gastel and D. C. Klein, unpublished observations).
30. 2-terminal lysine residue is present in all known vertebrate AA-NAT sequences; this region is important for regulation of AA-NAT activity and irAA-NAT by cAMP and proteosome inhibitors in C6 glioma cells transiently transfected with AA-NAT (J. A. Gastel and D. C. Klein, unpublished observations).
31. 2-terminal lysine residue is present in all known vertebrate AA-NAT sequences; this region is important for regulation of AA-NAT activity and irAA-NAT by cAMP and proteosome inhibitors in C6 glioma cells transiently transfected with AA-NAT (J. A. Gastel and D. C. Klein, unpublished observations).
32. 2-terminal lysine residue is present in all known vertebrate AA-NAT sequences; this region is important for regulation of AA-NAT activity and irAA-NAT by cAMP and proteosome inhibitors in C6 glioma cells transiently transfected with AA-NAT (J. A. Gastel and D. C. Klein, unpublished observations).
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35. The rapid suppressive effects of light on melatonin production are evolutionarily conserved: rat (6), human [A. J. Lewy, T. A. Wehr, F. K. Goodwin, D. A. Newsome, S. P. Markey, Science 210, 1267 (1980)], chicken [H. E. Hamm, J. S. Takahashi, M. Menaker, Brain Res. 266, 287 (1983)], and fish [J. Falcon, J. B. Marmillon, B. Claustrat, J. P. Collin, J. Neurosci. 9, 1943 (1989)].
36. The rapid suppressive effects of light on melatonin production are evolutionarily conserved: rat (6), human [A. J. Lewy, T. A. Wehr, F. K. Goodwin, D. A. Newsome, S. P. Markey, Science 210, 1267 (1980)], chicken [H. E. Hamm, J. S. Takahashi, M. Menaker, Brain Res. 266, 287 (1983)], and fish [J. Falcon, J. B. Marmillon, B. Claustrat, J. P. Collin, J. Neurosci. 9, 1943 (1989)].
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48. We thank S. Coon (NICHD) and R. Baler (NICHD) for technical advice; P. Loh (NICHD), M. Bogyo, and H. Ploegh (Massachusetts Institute of Technology) for helpful discussions; and A. Ciechanover, A. Goldberg, and M. Zatz for use of reagents and equipment. Supported by a Pharmacology Research Associate Training (PRAT) fellowship from NIGMS (J.A.G.).