Serine/threonine/tyrosine phosphorylation of the LHX3 LIM-homeodomain transcription factor

Journal of Cellular Biochemistry

Volumn 94, Issue 1, 2005, Pages 67-80

  Parker, Gretchen E ^a   West, Brooke E ^a   Witzmann, Frank A ^b   Rhodes, Simon J ^a  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Casein kinase; Hormone; Pituitary; PKC

Indexed keywords

AMINO ACID; CASEIN KINASE II; HOMEODOMAIN PROTEIN; HYPOPHYSIS HORMONE; ISOPROTEIN; PROTEIN; PROTEIN KINASE C; PROTEIN LHX3 LIM HOMEODOMAIN; PROTEIN MRG1; PROTEIN NL1; PROTEIN PIT1; SERINE; THREONINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LHX3; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; ENZYME SUBSTRATE; GENE ACTIVATION; GENE FUNCTION; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPOPHYSIS; LHX3 GENE; MASS SPECTROMETRY; MOTONEURON; NERVOUS SYSTEM DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REPORTER GENE; CELL LINE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; SEQUENCE HOMOLOGY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

MAMMALIA;

AMINO ACID SEQUENCE; CELL LINE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HOMEODOMAIN PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; SEQUENCE HOMOLOGY, AMINO ACID; SERINE; THREONINE; TYROSINE;

EID: 21044459803     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.20287     Document Type: Article

References (47)

1. Bach I, 2000. The LIM domain: Regulation by association. Mech Dev 91:5-17.
2. Bach I, Rhodes SJ, Pearse RV IInd, Heinzel T, Gloss B, Scully KM, Sawchenko PE, Rosenfeld MG, 1995. P-Lim, a LIM homeodomain factor, is expressed during pituitary organ and cell commitment and synergizes with Pit-1. Proc Natl Acad Sci USA 92:2720-2724.
3. Bach I, Carriere C, Ostendorff HP, Andersen B, Rosenfeld MG, 1997. A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev 11:1370-1380.
4. Barford D, Johnson LN, 1989. The allosteric transition of glycogen phosphorylase. Nature 340:609-616.
5. Ben-Yehoyada M, Ben-Dor I, Shaul Y, 2003. c-Abl tyrosine kinase selectively regulates p73 nuclear matrix association. J Biol Chem 278:34475-34482.
6. Bridwell JA, Price JR, Parker GE, McCutchan Schiller A, Sloop KW, Rhodes SJ, 2001. Role of the LIM domains in DNA recognition by the Lhx3 neuroendocrine transcription factor. Gene 277:239-250.
7. Deng X, Gao F, Flagg T, May WS, Jr. 2004. Mono- and multisite phosphorylation enhances Bcl2's antiapoptotic function and inhibition of cell cycle entry functions. Proc Natl Acad Sci USA 101:153-158.
8. Deppmann CD, Thornton TM, Utama FE, Taparowsky EJ, 2003. Phosphorylation of BATF regulates DNA binding: A novel mechanism for AP-1 (activator protein-1) regulation. Biochem J 374:423-431.
9. Fischberg DJ, Chen XH, Bancroft C, 1994. A Pit-1 phosphorylation mutant can mediate both basal and induced prolactin and growth hormone promoter activity. Mol Endocrinol 8:1566-1573.
10. Fowkes RC, King P, Burrin JM, 2002. Regulation of human glycoprotein hormone alpha-subunit gene transcription in LbetaT2 gonadotropes by protein kinase C and extracellular signal-regulated kinase 1/2. Biol Reprod 67:725-734.
11. Glenn DJ, Maurer RA, 1999. MRG1 binds to the LIM domain of Lhx2 and may function as a coactivator to stimulate glycoprotein hormone alpha-subunit gene expression. J Biol Chem 274:36159-36167.
12. Hammer GD, Krylova I, Zhang Y, Darimont BD, Simpson K, Weigel NL, Ingraham HA, 1999. Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: Integration of hormone signaling in reproduction and stress. Mol Cell 3:521-526.
13. Han B, Liu N, Yang X, Sun HB, Yang YC, 2001. MRG1 expression in fibroblasts is regulated by Sp1/Sp3 and an Ets transcription factor. J Biol Chem 276:7937-7942.
14. Haque MA, Hawes JW, Blum JS, 2001. Cysteinylation of MHC class II ligands: Peptide endocytosis and reduction within APC influences T cell recognition. J Immunol 166:4543-4551.
15. Haring HU, White MF, Kahn CR, Ahmad Z, DePaoli-Roach AA, Roach PJ, 1985. Interaction of the insulin receptor kinase with serine/threonine kinases in vitro. J Cell Biochem 28:171-182.
16. Heller-Harrison RA, Czech MP, 1991. Enhanced casein kinase II activity in COS-1 cells upon overexpression of either its catalytic or noncatalytic subunit. J Biol Chem 266:14435-14439.
17. Hibi M, Lin A, Smeal T, Minden A, Karin M, 1993. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 7:2135-2148.
18. Howard PW, Maurer RA, 2000. Identification of a conserved protein that interacts with specific LIM homeodomain transcription factors. J Biol Chem 275:13336-13342.
19. Howard PW, Maurer RA, 2001. A point mutation in the LIM domain of Lhx3 reduces activation of the glycoprotein hormone alpha-subunit promoter. J Biol Chem 276:19020-19026.
20. Hunter T, Karin M, 1992. The regulation of transcription by phosphorylation. Cell 70:375-387.
21. Hurley JH, Dean AM, Thorsness PE, Koshland DE, Jr., Stroud RM, 1990. Regulation of isocitrate dehydrogenase by phosphorylation involves no long-range conformational change in the free enzyme. J Biol Chem 265:3599-3602.
22. James G, Olson E, 1992. Deletion of the regulatory domain of protein kinase C alpha exposes regions in the hinge and catalytic domains that mediate nuclear targeting. J Cell Biol 116:863-874.
23. Kapiloff MS, Farkash Y, Wegner M, Rosenfeld MG, 1991. Variable effects of phosphorylation of Pit-1 dictated by the DNA response elements. Science 253:786-789.
24. Levy DE, Darnell JE, Jr. 2002. Stats: Transcriptional control and biological impact. Nat Rev Mol Cell Biol 3:651-662.
25. Malagon MM, Luque RM, Ruiz-Guerrero E, Rodriguez-Pacheco F, Garcia-Navarro S, Casanueva FF, Gracia-Navarro F, Castano JP, 2003. Intracellular signaling mechanisms mediating ghrelin-stimulated growth hormone release in somatotropes. Endocrinology 144:5372-5380.
26. Meier BC, Price JR, Parker GE, Bridwell JL, Rhodes SJ, 1999. Characterization of the porcine Lhx3/LIM-3/P-Lim LIM homeodomain transcription factor. Mol Cell Endocrinol 147:65-74.
27. Netchine I, Sobrier ML, Krude H, Schnabel D, Maghnie M, Marcos E, Duriez B, Cacheux V, Moers A, Goossens M, Gruters A, Amselem S, 2000. Mutations in LHX3 result in a new syndrome revealed by combined pituitary hormone deficiency. Nat Genet 25:182-186.
28. Okimura Y, Howard PW, Maurer RA, 1994. Pit-1 binding sites mediate transcriptional responses to cyclic adenosine 3′,5′-monophosphate through a mechanism that does not require inducible phosphorylation of Pit-1. Mol Endocrinol 8:1559-1565.
29. Ostendorff HP, Peirano RI, Peters MA, Schluter A, Bossenz M, Scheffner M, Bach I, 2002. Ubiquitination-dependent cofactor exchange on LIM homeodomain transcription factors. Nature 416:99-103.
30. Parker GE, Sandoval RM, Feister HA, Bidwell JP, Rhodes SJ, 2000. The homeodomain coordinates nuclear entry of the Lhx3 neuroendocrine transcription factor and association with the nuclear matrix. J Biol Chem 275:23891-23898.
31. Pickett CA, Manning N, Akita Y, Gutierrez-Hartmann A, 2002. Role of specific protein kinase C isozymes in mediating epidermal growth factor, thyrotropin-releasing hormone, and phorbol ester regulation of the rat prolactin promoter in GH4/GH4C1 pituitary cells. Mol Endocrinol 16:2840-2852.
32. Purcell AL, Carew TJ, 2003. Tyrosine kinases, synaptic plasticity and memory: Insights from vertebrates and invertebrates. Trends Neurosci 26:625-630.
33. Retaux S, Bachy I, 2002. A short history of LIM domains (1993-2002): From protein interaction to degradation. Mol Neurobiol 26:269-281.
34. Richards JS, 2001. New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol Endocrinol 15:209-218.
35. Savage JJ, Yaden BC, Kiratipranon P, Rhodes SJ, 2003. Transcriptional control during mammalian anterior pituitary development. Gene 319:1-19.
36. Sharma K, Sheng HZ, Lettieri K, Li H, Karavanov A, Potter S, Westphal H, Pfaff SL, 1998. LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 95:817-828.
37. Shaulian E, Karin M, 2001. AP-1 in cell proliferation and survival. Oncogene 20:2390-2400.
38. Sheng HZ, Zhadanov AB, Mosinger B, Jr., Fujii T, Bertuzzi S, Grinberg A, Lee EJ, Huang SP, Mahon KA, Westphal H, 1996. Specification of pituitary cell lineages by the LIM homeobox gene Lhx3. Science 272:1004-1007.
39. Sheng HZ, Moriyama K, Yamashita T, Li H, Potter SS, Mahon KA, Westphal H, 1997. Multistep control of pituitary organogenesis. Science 278:1809-1812.
40. Shi Y, Massague J, 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700.
41. Sloop KW, Meier BC, Bridwell JL, Parker GE, Schiller AM, Rhodes SJ, 1999. Differential activation of pituitary hormone genes by human Lhx3 isoforms with distinct DNA binding properties. Mol Endocrinol 13:2212-2225.
42. Sloop KW, Dwyer CJ, Rhodes SJ, 2001a. An isoform-specific inhibitory domain regulates the LHX3 LIM homeodomain factor holoprotein and the production of a functional alternate translation form. J Biol Chem 276:36311-36319.
43. Sloop KW, Parker GE, Hanna KR, Wright HA, Rhodes SJ, 2001b. LHX3 transcription factor mutations associated with combined pituitary hormone deficiency impair the activation of pituitary target genes. Gene 265:61-69.
44. Southan C, 2004. Has the yo-yo stopped? An assessment of human protein-coding gene number. Proteomics 4:1712-1726.
45. Thaler JP, Lee SK, Jurata LW, Gill GN, Pfaff SL, 2002. LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 110:237-249.
46. Thor S, Andersson SG, Tomlinson A, Thomas JB. 1999. A LIM-homeodomain combinatorial code for motor-neuron pathway selection. Nature 397:76-80.
47. Xu L, Lavinsky RM, Dasen JS, Flynn SE, Mclnerney EM, Mullen TM, Heinzel T, Szeto D, Korzus E, Kurokawa R, Aggarwal AK, Rose DW, Glass CK, Rosenfeld MG, 1998. Signal-specific co-activator domain requirements for Pit-1 activation. Nature 395:301-306.