Aplysia mollusk-derived growth factor is a mitogen with adenosine deaminase activity and is expressed in the developing central nervous system

Molecular Brain Research

Volumn 117, Issue 2, 2003, Pages 228-236

  Akalal, David Benjamin G ^a,b   Bottenstein, Jane E ^a,b   Lee, Seung Hee ^c   Han, Jin Hee ^c   Chang, Deog Jin ^c   Kaang, Bong Kiun ^c   Nagle, Gregg T ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c Seoul National University   (South Korea)

Author keywords

ADA; Adenosine deaminase related growth factor; Aplysia; CECR1; Developing central nervous system; Insect derived growth factor; MDGF; Neurotransmitters, modulators, transporters, and receptors; Transmitters in invertebrates

Indexed keywords

ADENOSINE DEAMINASE; GROWTH FACTOR; MITOGENIC AGENT;

APLYSIA; ARTICLE; BRAIN LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; ENZYME ACTIVITY; MITOGENESIS; MOLLUSC; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION;

ADENOSINE DEAMINASE; ANIMALS; APLYSIA; BLOTTING, WESTERN; CELL COUNT; CELL DIVISION; CELL LINE; CENTRAL NERVOUS SYSTEM; DROSOPHILA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH SUBSTANCES; INDOLES; INOSINE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOGENS; MOLECULAR SEQUENCE DATA; OVUM; TIME FACTORS;

APLYSIA; INSECTA; INVERTEBRATA;

EID: 1642361602     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(03)00287-0     Document Type: Article

References (59)

1. Agarwal R.P., Sagar S., Parks R.E. Jr. Adenosine deaminase from human erythrocytes. Biochem. Pharmacol. 24:1974;693701.
2. Agarwal R.P., Crabtree G.W., Parks R.E. Jr., Nelson J.A., Keightley R., Parkman R., Rosen F.S., Stern R.C., Polmar S.H. Purine nucleoside metabolism in the erythrocytes of patients with adenosine deaminase deficiency and severe combined immunodeficiency. J. Clin. Invest. 57:1976;1025-1035.
3. Agarwal R.P., Parks R.E. Jr. Adenosine deaminase from human erythrocytes. Methods Enzymol. 51:1978;502-507.
4. Ahmed S.A., Gogal R.M. Jr., Walsh J.E. A new rapid and simple non-radioactive assay to monitor and determine the proliferation of lymphocytes: an alternative to [3H]thymidine incorporation assay. J. Immunol. Methods. 170:1994;211-224.
5. Aikawa T., Umemori-Aikawa Y., Fisher J.R. Purification and properties of the adenosine deaminase from the midgut gland of a marine bivalved mollusc, Atrina spp. Comp. Biochem. Physiol. B. 58:1977;357-364.
6. Akalal D.-B.G., Nagle G.T. Mollusk-derived growth factor: cloning and developmental expression in the central nervous system and reproductive tract of Aplysia. Mol. Brain Res. 91:2001;163-168.
7. Bateman A., Birney E., Durbin R., Eddy S.R., Howe K.L., Sonnhammer E.L. The Pfam protein families database. Nucleic Acids Res. 28:2000;263-266.
8. Benowitz L.I., Goldberg D.E., Madsen J.R., Soni D., Irwin N. Inosine stimulates extensive axon collateral growth in the rat corticospinal tract after injury. Proc. Natl. Acad. Sci. USA. 96:1999;13486-13490.
9. Benowitz L.I., Jing Y., Tabibiazar R., Jo S.A., Petrausch B., Stuermer C.A.O., Rosenberg P.A., Irwin N. Axon outgrowth is regulated by an intracellular purine-sensitive mechanism in retinal ganglion cells. J. Biol. Chem. 273:1998;29626-29634.
10. Brady T.G., O'Donovan C.I. A study of the tissue distribution of adenosine deaminase in six mammal species. Comp. Biochem. Physiol. 14:1965;101-119.
11. Burnstock G., Wood J.N. Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr. Opin. Neurobiol. 6:1996;526-532.
12. Carter C.S., Ramsey M.M., Sonntag W.E. A critical analysis of the role of growth hormone and IGF-1 in aging and lifespan. Trends Genet. 18:2002;295-301.
13. Cash D., Carew T.J. A quantitative analysis of the development of the central nervous system in juvenile Aplysia californica. J. Neurobiol. 20:1988;25-47.
14. Chang Z., Nygaard P., Chinault A.C., Kallems R.E. Deduced amino acid sequence of Escherichia coli adenosine deaminase reveals evolutionarily conserved amino acid residue: implications for catalytic function. Biochemistry. 30:1991;2273-2280.
15. Charlab R., Rowton E.D., Ribeiro J.M.C. The salivary adenosine deaminase from the sand fly Lutzomyia longipalpis. Exp. Parasitol. 95:2000;45-53.
16. Charlab R., Valenzuela J.G., Andersen J., Ribeiro J.M. The invertebrate growth factor/CECR1 subfamily of adenosine deaminase proteins. Gene. 267:2001;13-22.
17. Chen P., Goldberg D.E., Kolb B., Lanser M., Benowitz L.I. Inosine induces axonal rewiring and improves behavioral outcome after stroke. Proc. Natl. Acad. Sci. USA. 99:2002;9031-9036.
18. Chomcyznski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
19. Coleman M.S., Donofrio J., Hutton J.J., Hahn L., Daoud A., Lampkin B., Dyminski J. Identification and quantitation of adenine deoxynucleotides in erythrocytes of a patient with adenosine deaminase deficiency and severe combined immunodeficiency. J. Biol. Chem. 253:1978;1619-1626.
20. Cristalli G., Costanzi S., Lambertucci C., Lupidi G., Vittori S., Volpini R., Camaioni E. Adenosine deaminase: functional implications and different classes of inhibitors. Med. Res. Rev. 21:2001;105-128.
21. Edgar B.A., Lehner C.F. Developmental control of cell cycle regulators: a fly's perspective. Science. 274:1996;1646-1652.
22. Fainzilber M., Smit A.B., Syed N.I., Wildering W.C., Hermann P.M., van der Schors R.C., Jimenez C., Li K.W., van Minnen J., Bulloch A.G.M., Ibanez C.F., Geraerts W.P.M. CRNF, a molluscan neurotrophic factor that interacts with the p75 neurotrophin receptor. Science. 274:1996;1540-1543.
23. Franco R., Casado V., Ciruela F., Saura C., Mallol J., Canela E.I., Lluis C. Cell surface adenosine deaminase: much more than an ectoenzyme. Prog. Neurobiol. 52:1997;283-294.
24. Graff J.M., Bansal A., Melton D.A. Xenopus Mad proteins transduce distinct subsets of signals for the TGF beta superfamily. Cell. 85:1996;479-487.
25. Hamakawa T., Woodin M.A., Bjorgum M.C., Painter S.D., Takasaki M., Lukowiak K., Nagle G.T., Syed N.I. Excitatory synaptogenesis between identified Lymnaea neurons requires extrinsic trophic factors and is mediated by receptor tyrosine kinases. J. Neurosci. 19:1999;9306-9312.
26. Hermann P.M., van Kesteren R.E., Wildering W.C., Painter S.D., Reno J.M., Smith J.S., Kumar S.B., Geraerts W.P.M., Ericsson L.H., Smit A.B., Bulloch A.G.M., Nagle G.T. Neurotrophic actions of a novel molluscan epidermal growth factor. J. Neurosci. 20:2000;6355-6364.
27. Hershfield M.S. Adenosine deaminase deficiency: clinical expression, molecular basis, and therapy. Semin. Hematol. 35:1998;291-298.
28. Hickmott P.W., Carew T.J. An autoradiographic analysis of neurogenesis in juvenile Aplysia californica. J. Neurobiol. 22:1991;313-326.
29. Homma K., Matsushita T., Natori S. Purification, characterization, and cDNA cloning of a novel growth factor from the conditioned medium of NIH-Sape-4, an embryonic cell line of Sarcophaga peregrina (flesh fly). J. Biol. Chem. 271:1996;13770-13775.
30. Homma K.J., Tanaka Y., Matsushita T., Yokoyama K., Matsui H., Natori S. Adenosine deaminase activity of insect-derived growth factor is essential for its growth factor activity. J. Biol. Chem. 276:2001;43761-43766.
31. Kalckar H. Differential spectrophotometry of purine compounds by means of specific enzymes. J. Biol. Chem. 167:1946;461475.
32. Keegan L.P., Gallo A., O'Connell M.A. Survival is impossible without an editor. Science. 290:2000;1707-1708.
33. Kriegstein K.R., Castellucci V., Kandel E.R. Metamorphosis of Aplysia californica in laboratory culture. Proc. Natl. Acad. Sci. USA. 71:1974;3654-3658.
34. Kriegstein A.R. Stages in the post-hatching development of Aplysia californica. J. Exp. Zool. 199:1977;275-288.
35. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
36. Lee J., Kim H., Kim K., Han J., Lee Y., Lim C., Chang D., Kubo T., Kaang B. Overexpression of and RNA interference with the CCAAP enhancer-binding protein on long-term facilitation of Aplysia sensory to motor synapses. Learn. Mem. 8:2001;220-226.
37. Li S., Aksoy S. A family of genes with growth factor and adenosine deaminase similarity are preferentially expressed in the salivary glands of Glossina m. morsitans. Gene. 252:2000;89-93.
38. Lim C., Chung D.Y., Kaang B. Partial anatomical and physiological characterization and dissociated cell culture of the nervous system of the marine mollusk Aplysia kurodai. Mol. Cells. 7:1997;399-407.
39. Ma P.F., Fisher J.R. Multiple adenosine deaminases in the amphibia and their possible phylogenetic significance. Comp. Biochem. Physiol. 27:1968;687-694.
40. Maier S.A., Podemski L., Graham S.W., McDermid H.E., Locke J. Characterization of the adenosine deaminase-related growth factor (ADGF) gene family in Drosophila. Gene. 280:2001;27-36.
41. Matsushita T., Fujii-Taira I., Tanaka Y., Homma K.J., Natori S. Male-specific IDGF, a novel gene encoding a membrane-bound extracellular signaling molecule expressed exclusively in testis of Drosophila melanogaster. J. Biol. Chem. 275:2000;36934-36941.
42. McAdoo D.J., Robak G., Xu G.-Y., Hughes M.G. Adenosine release upon spinal cord injury. Brain Res. 854:2000;152-157.
43. Mitsuhashi J., Maramorosch K. Leafhopper tissue culture: embryonic, nymphal, and imaginal tissues from aseptic insects. Contrib. Boyce Thompson Inst. 22:1964;435-460.
44. Mohamedali K.A., Kurz L.C., Rudolph F.B. Site-directed mutagenesis of active site glutamate-217 in mouse adenosine deaminase. Biochemistry. 35:1996;1672-1680.
45. Riazi M.A., Brinkman-Mills P., Nguyen T., Pan H., Phan S., Ying F., Roe B.A., Tochigi J., Shimizu Y., Minoshima S., Shimizu N., Buchwald M., McDermid H.E. The human homolog of insect-derived growth factor, CECR1, is a candidate gene for features of cat eye syndrome. Genomics. 64:2000;277-285.
46. Ribeiro J.M., Charlab R., Valenzuela J.G. The salivary adenosine deaminase activity of the mosquitoes Culex quinquefasciatus and Aedes aegypti. J. Exp. Biol. 204:2001;2001-2010.
47. Richard E., Alam S.M., Arredondo-Vega F.X., Patel D.D., Hershfield M.S. Clustered charged amino acids of human adenosine deaminase comprise a functional epitope for binding the adenosine deaminase complexing protein CD26/dipeptidyl peptidase IV. J. Biol. Chem. 277:2002;19720-19726.
48. Richard E., Arredondo-Vega F.X., Santisteban I., Kelly S.J., Patel D.D., Hershfield M.S. The binding site of human adenosine deaminase for CD26/Dipeptidyl peptidase IV: the Arg142Gln mutation impairs binding to CD26 but does not cause immune deficiency. J. Exp. Med. 192:2000;1223-1236.
49. Rusten T.E., Cantera R., Kafatos F.C., Barrio R. The role of TGF beta signaling in the formation of the dorsal nervous system is conserved between Drosophila and chordates. Development. 129:2002;3575-3584.
50. Schacher S., Proshansky E. Neurite regeneration by Aplysia neurons in dissociated cell culture: modulation by Aplysia hemolymph and the presence of the initial axonal segment. J. Neurosci. 3:1983;2403-2413.
51. Schinzel A., Schmid W., Fraccaro M., Tiepolo L., Zuffardi O., Opitz J.M., Lindsten J., Zetterqvist P., Enell H., Baccichetti C., Tenconi R., Pagon R.A. The 'cat eye syndrome': dicentric small marker chromosome probably derived from a no.22 (tetrasomy 22pter to q11) associated with a characteristic phenotype. Report of 11 patients and delineation of the clinical picture. Hum. Genet. 57:1981;148-158.
52. Sideraki V., Wilson D.K., Kurz L.C., Quiocho F.A., Rudolph F.B. Site-directed mutagenesis of histidine 238 in mouse adenosine deaminase: substitution of histidine 238 does not impede hydroxylate formation. Biochemisty. 35:1996;15019-15028.
53. Soni D., Aoki C., Yang M., Black P.M., Irwin N., Benowitz L.I. Inosine induces the growth of new corticospinal tract synapses in the injured rat spinal cord. Soc. Neurosci. Abstr. 26:2000;863.
54. Sossin W.S., Kreiner T., Barinaga M., Schilling J., Scheller R.H. A dense core vesicle protein is restricted to the cortex of granules in the exocrine atrial gland of Aplysia californica. J. Biol. Chem. 264:1989;16933-16940.
55. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:1994;4673-4680.
56. Wildering W.C., Hermann P.M., Bulloch A.G.M. Lymnaea epidermal growth factor promotes axonal regeneration in CNS organ culture. J. Neurosci. 21:2001;9345-9354.
57. Wilson D.K., Quiocho F.A. A pre-transition-state mimic of an enzyme: X-ray structure of adenosine deaminase with bound 1-deazaadenosine and zinc-activated water. Biochemistry. 32:1993;1689-1694.
58. Wilson D.K., Rudolph F.B., Quiocho F.A. Atomic structure of adenosine deaminase complexed with a transition state analog: understanding catalysis and immunodeficiency mutations. Science. 252:1991;1278-1284.
59. Zurovec M., Dolezal T., Gazi M., Pavlova E., Bryant P.J. Adenosine deaminase-related growth factors stimulate cell proliferation in Drosophila by depleting extracellular adenosine. Proc. Natl. Acad. Sci. USA. 99:2002;4403-4408.