Regulation of the dual function tissue transglutaminase/Gα(h) during murine neuromuscular development: Gene and enzyme isoform expression

Neurochemistry International

Volumn 37, Issue 4, 2000, Pages 337-349

  Citron, B A ^a,b   Gregory, E J ^a   Steigerwalt, D S ^a   Qin, F ^a   Festoff, B W ^a,b  

^a Neurobiology Research Lab   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Cross linking; Factor XIII; Neuromuscular junction; Neurons; Plasticity; Synapse elimination

Indexed keywords

BLOOD CLOTTING FACTOR 8; ISOENZYME; MESSENGER RNA; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTHROMBIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL FRACTIONATION; CONTROLLED STUDY; CROSS LINKING; CYTOSOL; DNA SEQUENCE; EMBRYO; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOCHEMISTRY; MOLECULAR WEIGHT; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NERVE CELL PLASTICITY; NERVE GROWTH; NEUROMUSCULAR SYNAPSE; NEUROMUSCULAR SYSTEM; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE;

AGING; ANIMALS; CULTURE TECHNIQUES; CYTOSOL; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MICE; MICE, INBRED BALB C; MOLECULAR WEIGHT; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; PREGNANCY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; TRANSGLUTAMINASES;

MURINAE;

EID: 0034309870     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0197-0186(00)00044-9     Document Type: Article

References (66)

1. Adel-Moallem S., Hales B.F. Transglutaminase and clusterin induction during normal and abnormal limb development in the mouse. Biology of Reproduction. 55:1996;281-290.
2. Aeschlimann D., Koeller M.K., Allen-Hoffmann B.L., Mosher D.F. Isolation of a cDNA encoding a novel member of the transglutaminase gene family from human keratinocytes. Detection and identification of transglutaminase gene products based on reverse transcription-polymerase chain reaction with degenerate primers. Journal of Biological Chemistry. 273:1998;3452-3460.
3. Aeschlimann D., Paulsson M. Cross-linking of laminin-nidogen complexes by tissue transglutaminase. A novel mechanism for basement membrane stabilization. Journal of Biological Chemistry. 266:1991;15308-15317.
4. Aeschlimann D., Paulsson M., Mann K. Identification of Gln726 in nidogen as the amine acceptor in transglutaminase-catalyzed cross-linking of laminin-nidogen complexes. Journal of Biological Chemistry. 267:1992;11316-11321.
5. Akaaboune M., Hantaï D., Smirnova I., Lachkar S., Kapsimali M., Verdiere-Sahuque M., Festoff B.W. Developmental regulation of the serpin, protease nexin I, localization during activity-dependent polyneuronal synapse elimination in mouse skeletal muscle. Journal of Comparative Neurology. 397:1998;572-579.
6. Akaaboune M., Ma J., Festoff B.W., Greenberg B.D., Hantaï D. Neurotrophic regulation of mouse muscle beta-amyloid protein precursor and alpha 1-antichymotrypsin as revealed by axotomy. Journal of Neurobiology. 25:1994;503-514.
7. Ando M., Kunii S., Tatematsu T., Nagata Y. Selective alterations in transglutaminase activity of rat superior cervical ganglia in response to neurotransmitters, high potassium and sialic acid-containing compounds. Brain Res. 604:1993;64-68.
8. Ashley C.T. Jr., Warren S.T. Trinucleotide repeat expansion and human disease. Annual Review of Genetics. 29:1995;703-728.
9. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. Current Protocols in Molecular Biology. 1987;Wiley, New York.
10. Cariello L., de Cristofaro T., Zanetti L., Cuomo T., Di Maio L., Campanella G., Rinaldi S., Zanetti P., Di Lauro R., Varrone S. Transglutaminase activity is related to CAG repeat length in patients with Huntington's disease. Human Genetics. 98:1996;633-635.
11. Chang S.K., Chung S.I. Cellular transglutaminase. The particulate-associated transglutaminase from chondrosarcoma and liver: partial purification and characterization. Journal of Biological Chemistry. 261:1986;8112-8121.
12. Citron B.A., Smirnova I.V., Zoubine M.N., Festoff B.W. Quantitative PCR analysis reveals novel expression of prothrombin mRNA and regulation of its levels in developing mouse muscle. Thrombos. Res. 87:1997;303-313.
13. Cocuzzi E.T., Chung S.I. Cellular transglutaminase: lung matrix-associated transglutaminase characterization and activation with sulfhydryls. Journal of Biological Chemistry. 261:1986;8122.
14. Cooper A.J., Sheu K.F., Burke J.R., Strittmatter W.J., Gentile V., Peluso G., Blass J.P. Pathogenesis of inclusion bodies in (CAG)n/Qn-expansion diseases with special reference to the role of tissue transglutaminase and to selective vulnerability. Journal of Neurochemistry. 72:1999;889-899.
15. Dennis M.J., Harris A.J. Elimination of inappropriate nerve-muscle connections during development of rat embryos. Progress in Brain Res. 49:1979;359-364.
16. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucl. Acids Res. 12:1984;387-395.
17. Fernandez H.L., Duell M.J., Festoff B.W. Neurotrophic control of 16S acetylcholinesterase at the vertebrate neuromuscular junction. Journal of Neurobiology. 10:1979;441-454.
18. Festoff B.W., Rao J.S., Hantaï D. Plasminogen activators and inhibitors in the neuromuscular system: III. The serpin protease nexin I is synthesized by muscle and localized at neuromuscular synapses. J. Cell. Physiol. 147:1991;76-86.
19. Festoff B.W., Rao J.S., Maben C., Hantaï D. Plasminogen activators and their inhibitors in the neuromuscular system: I. Developmental regulation of plasminogen activator isoforms during in vitro myogenesis in two cell lines. Journal of Cellular Physiology. 144:1990;262-271.
20. Festoff B.W., Rao J.S., Reddy B.R., Hantaï D. A cascade approach to synapse formation based on thrombogenic and fibrinolytic models. Festoff B.W. Serine Proteases and Their Serpin Inhibitors in the Nervous System: Regulation in Development and in Degenerative and Malignant Disease. 1990;245-252 Plenum Press, New York.
21. Festoff, B.W., Yong, C., SantaCruz, K., Arnold, P.M., Sebastian, C.T., Davies, P.J.A., Citron, B.A., 2000. Spinal cord injury induces a GTP-independent alternative transcript of retinoic acid-inducible transglutaminase and reverses changes in development. Journal of Neurotrauma, submitted.
22. Gentile V., Saydak M., Chiocca E.A., Akande O., Birckbichler P.J., Lee K.N., Stein J.P., Davies P.J. Isolation and characterization of cDNA clones to mouse macrophage and human endothelial cell tissue transglutaminases. Journal of Biological Chemistry. 266:1991;478-483.
23. Greenberg C.S., Birckbichler P.J., Rice R.H. Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues. FASEB Journal. 5:1991;3071-3077.
24. Gregory E.J., Steigerwalt D.L., Zoubine M.N., Citron B.A., Festoff B.W. Protein and gene expression for transglutaminase in developing mouse muscle. Soc. for Neurosci. 22:1996;586.2.
25. Hall Z.W., Sanes J.R. Synaptic structure and development: the neuromuscular junction. Cell. 72:(Suppl.):1993;99-121.
26. Hand D., Campoy F.J., Clark S., Fisher A., Haynes L.W. Activity and distribution of tissue transglutaminase in association with nerve-muscle synapses. Journal of Neurochemistry. 61:1993;1064-1072.
27. Hand D., Dias D., Haynes L. Stabilization of collagen-tailed acetylcholinesterase in muscle cells through extracellular anchorage by transglutaminase-catalyzed cross-linking. Mol. Cell. Biochem. 204:2000;65-76.
28. Hand D., Haynes L.W. Anchorage of asymmetric acetylcholinesterase by isodipeptide cross-linking in muscle cells. Biochemical Society Transactions. 20:1992;158S.
29. Hantaï D., Rao J.S., Festoff B.W. Serine proteases and serpins: their possible roles in the motor system. Revue Neurologique. 144:1988;680-687.
30. Haynes L.W. Association of particulate transglutaminase with the nerve-muscle synapse. Biochemical Society Transactions. 17:1989;1069-1070.
31. Ho G.J., Gregory E.J., Smirnova I.V., Zoubine M.N., Festoff B.W. Cross-linking of beta-amyloid precursor protein catalyzed by tissue transglutaminase. FEBS Letters. 349:1994;151-154.
32. Igarashi S., Koide R., Shimohata T., Yamada M., Hayashi Y., Takano H., Date H., Oyake M., Sato T., Sato A., Egawa S., Ikeuchi T., Tanaka H., Nakano R., Tanaka K., Hozumi I., Inuzuka T., Takahashi H., Tsuji S. Suppression of aggregate formation and apoptosis by transglutaminase inhibitors in cells expressing truncated DRPLA protein with an expanded polyglutamine stretch. Nature Genetics. 18:1998;111-117.
33. Jensen P.H., Lorand L., Ebbesen P., Gliemann J. Type-2 plasminogen-activator inhibitor is a substrate for trophoblast transglutaminase and factor XIIIa. Transglutaminase-catalyzed cross-linking to cellular and extracellular structures. European Journal of Biochemistry. 214:1993;141-146.
34. Jensen P.H., Sorensen E.S., Petersen T.E., Gliemann J., Rasmussen L.K. Residues in the synuclein consensus motif of the alpha-synuclein fragment, NAC, participate in transglutaminase-catalysed cross-linking to Alzheimer-disease amyloid beta A4 peptide. Biochemical Journal. 310:1995;91-94.
35. Kahlem P., Terre C., Green H., Djian P. Peptides containing glutamine repeats as substrates for transglutaminase-catalyzed cross-linking: relevance to diseases of the nervous system. Proc. Natl. Acad. Sci. U.S.A. 93:1996;14580-14585.
36. Kojima S., Inui T., Muramatsu H., Suzuki Y., Kadomatsu K., Yoshizawa M., Hirose S., Kimura T., Sakakibara S., Muramatsu T. Dimerization of midkine by tissue transglutaminase and its functional implication. Journal of Biological Chemistry. 272:1997;9410-9416.
37. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
38. Lorand L. Neurodegenerative diseases and transglutaminase. Proc. Natl. Acad. Sci. U.S.A. 93:1996;14310-14313.
39. Ma J., Yang S.X., Ho G.J., Festoff B.W. Insulin-like growth factor binding protein-1 at mouse neuromuscular synapses. Synapse. 17:1994;225-229.
40. Mahoney S.A., Perry M., Seddon A., Bohlen P., Haynes L. Transglutaminase forms midkine homodimers in cerebellar neurons and modulates the neurite-outgrowth response. Biochemical and Biophysical Research Communications. 224:1996;147-152.
41. Melino G., Annicchiarico-Petruzzelli M., Piredda L., Candi E., Gentile V., Davies P.J., Piacentini M. Tissue transglutaminase and apoptosis: sense and antisense transfection studies with human neuroblastoma cells. Molecular and Cellular Biology. 14:1994;6584-6596.
42. Melino G., Piacentini M. Tissue transglutaminase in cell death: a downstream or a multifunctional upstream effector? FEBS Letters. 430:1998;59-63.
43. Miller R.R., Rao J.S., Burton W.V., Festoff B.W. Proteoglycan synthesis by clonal skeletal muscle cells during in vitro myogenesis: differences detected in the types and patterns from primary cultures. Int. J. Devel. Neurosci. 9:1991;259-267.
44. Monsonego A., Shani Y., Friedmann I., Paas Y., Eizenberg O., Schwartz M. Expression of GTP-dependent and GTP-independent tissue-type transglutaminase in cytokine-treated rat brain astrocytes. Journal of Biological Chemistry. 272:1997;3724-3732.
45. Moya K.L., Benowitz L.I., Schneider G.E., Allinquant B. The amyloid precursor protein is developmentally regulated and correlated with synaptogenesis. Developmental Biology. 161:1994;597-603.
46. Nagy L., Saydak M., Shipley N., Lu S., Basilion J.P., Yan Z.H., Syka P., Chandraratna R.A., Stein J.P., Heyman R.A., Davies P.J. Identification and characterization of a versatile retinoid response element (retinoic acid receptor response element-retinoid X receptor response element) in the mouse tissue transglutaminase gene promoter. Journal of Biological Chemistry. 271:1996;4355-4365.
47. Nagy L., Thomazy V.A., Chandraratna R.A., Heyman R.A., Davies P.J. Retinoid-regulated expression of BCL-2 and tissue transglutaminase during the differentiation and apoptosis of human myeloid leukemia (HL-60) cells. Leukemia Res. 20:1996;499-505.
48. Oppenheim R.W. The absence of significant postnatal motoneuron death in the brachial and lumbar spinal cord of the rat. Journal of Comparative Neurology. 246:1986;281-286.
49. Perry M.J., Haynes L.W. Localization and activity of transglutaminase, a retinoid-inducible protein, in developing rat spinal cord. Int. J. Devel. Neurosci. 11:1993;325-337.
50. Piacentini M. Tissue transglutaminase: a candidate effector element of physiological cell death. Current Topics in Microbiology and Immunology. 200:1995;163-175.
51. Sabath D.E., Broome H.E., Prystowsky M.B. Glyceraldehyde-3-phosphate dehydrogenase mRNA is a major interleukin 2-induced transcript in a cloned T-helper lymphocyte. Gene. 91:1990;185-191.
52. Sadeh M., Stern L.Z., Czyzewski K., Finley P.R., Russell D.H. Alterations in creatine kinase, omithine decarboxylase, and transglutaminase during muscle regeneration. Life Sciences. 34:1984;483-488.
53. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor, New York.
54. Schubert W., Prior R., Weidemann A., Dircksen H., Multhaup G., Masters C.L., Beyreuther K. Localization of Alzheimer beta A4 amyloid precursor protein at central and peripheral synaptic sites. Brain Res. 563:1991;184-194.
55. Shimokawa M., Yanagisawa K., Nishiye H., Miyatake T. Identification of amyloid precursor protein in synaptic plasma membrane. Biochemical and Biophysical Research Communications. 196:1993;234-240.
56. Slife C.W., Dorsett M.D., Bouquett G.T., Register A., Taylor E., Conroy S. Subcellular localization of a membrane-associated transglutaminase activity in rat liver. Archives of Biochemistry and Biophysics. 241:1985;329-336.
57. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., Klenk D.C. Measurement of protein using bicinchoninic acid. Analytical Biochemistry. 150:1985;76-85.
58. Spanakis E. Problems related to the interpretation of autoradiographic data on gene expression using common constitutive transcripts as controls. Nucl. Acids Res. 21:1993;3809-3819.
59. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76:1979;4350-4354.
60. Trojanowski J.Q., Goedert M., Iwatsubo T., Lee V.M. Fatal attractions: abnormal protein aggregation and neuron death in Parkinson's disease and Lewy body dementia. Cell Death Differ. 5:1998;832-837.
61. Upchurch H.F., Conway E., Patterson M.K. Jr., Birckbichler P.J., Maxwell M.D. Cellular transglutaminase has affinity for extracellular matrix. In Vitro Cell. Dev. Biol. 23:1987;795-800.
62. Upchurch H.F., Conway E., Patterson M.K.J., Maxwell M.D. Localization of cellular transglutaminase on the extracellular matrix after wounding: characteristics of the matrix bound enzyme. J. Cell. Physiol. 149:1991;375-382.
63. Yan Z.H., Noonan S., Nagy L., Davies P.J., Stein J.P. Retinoic acid induction of the tissue transglutaminase promoter is mediated by a novel response element. Mol. Cell. Endocrinol. 120:1996;203-212.
64. Zhao J., Araki N., Nishimoto S.K. Quantitation of matrix Gla protein mRNA by competitive polymerase chain reaction using glyceraldehyde-3-phosphate dehydrogenase as an internal control. Gene. 155:1995;159-165.
65. Zhong H., Simons J.W. Direct comparison of GAPDH, beta-actin, cyclophilin, and 28S rRNA as internal standards for quantifying RNA levels under hypoxia. Biochemical and Biophysical Research Communications. 259:1999;523-526.
66. Zoubine M.N., Ma J.Y., Smirnova I.V., Citron B.A., Festoff B.Y.W. A molecular mechanism for synapse elimination: novel inhibition of locally generated thrombin delays synapse loss in neonatal mouse muscle. Developmental Biology. 179:1996;447-457.