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. 1985 Sep;82(17):5593–5597. doi: 10.1073/pnas.82.17.5593

Differential expression of the mouse cholecystokinin gene during brain and gut development.

J Friedman, B S Schneider, D Powell
PMCID: PMC390597  PMID: 3862083

Abstract

Cholecystokinin (CCK) is a neuropeptide found in brain and intestine. In this report, we have isolated a cDNA clone that encodes CCK from a mouse brain cDNA library. This cDNA clone has extensive homology to CCK precursors that have been sequenced previously. Southern blots of genomic DNA probed with this cDNA clone revealed single bands for each of eight different restriction enzymes, all of which could be accounted for by a single genomic clone, suggesting that the CCK gene is present as a single-copy gene in mice. RNA blots, primer extensions, and S1 nuclease protection assays have suggested that the same RNA start site is utilized in brain and in gut. Finally, we have shown, by using RNA blots and a radioimmunoassay specific for CCK, that CCK is expressed at maximum adult levels in intestine at birth but that adult concentrations of CCK and its mRNA are not reached in brain until much later in development.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amara S. G., Evans R. M., Rosenfeld M. G. Calcitonin/calcitonin gene-related peptide transcription unit: tissue-specific expression involves selective use of alternative polyadenylation sites. Mol Cell Biol. 1984 Oct;4(10):2151–2160. doi: 10.1128/mcb.4.10.2151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amara S. G., Jonas V., Rosenfeld M. G., Ong E. S., Evans R. M. Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature. 1982 Jul 15;298(5871):240–244. doi: 10.1038/298240a0. [DOI] [PubMed] [Google Scholar]
  3. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  5. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  6. Bond J. F., Robinson G. S., Farmer S. R. Differential expression of two neural cell-specific beta-tubulin mRNAs during rat brain development. Mol Cell Biol. 1984 Jul;4(7):1313–1319. doi: 10.1128/mcb.4.7.1313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  8. Darnell J. E., Jr Variety in the level of gene control in eukaryotic cells. Nature. 1982 Jun 3;297(5865):365–371. doi: 10.1038/297365a0. [DOI] [PubMed] [Google Scholar]
  9. Derman E., Krauter K., Walling L., Weinberger C., Ray M., Darnell J. E., Jr Transcriptional control in the production of liver-specific mRNAs. Cell. 1981 Mar;23(3):731–739. doi: 10.1016/0092-8674(81)90436-0. [DOI] [PubMed] [Google Scholar]
  10. Deschenes R. J., Lorenz L. J., Haun R. S., Roos B. A., Collier K. J., Dixon J. E. Cloning and sequence analysis of a cDNA encoding rat preprocholecystokinin. Proc Natl Acad Sci U S A. 1984 Feb;81(3):726–730. doi: 10.1073/pnas.81.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dockray G. J. Immunochemical evidence of cholecystokinin-like peptides in brain. Nature. 1976 Dec 9;264(5586):568–570. doi: 10.1038/264568a0. [DOI] [PubMed] [Google Scholar]
  12. Durnam D. M., Hoffman J. S., Quaife C. J., Benditt E. P., Chen H. Y., Brinster R. L., Palmiter R. D. Induction of mouse metallothionein-I mRNA by bacterial endotoxin is independent of metals and glucocorticoid hormones. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1053–1056. doi: 10.1073/pnas.81.4.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eysselein V. E., Reeve J. R., Jr, Shively J. E., Hawke D., Walsh J. H. Partial structure of a large canine cholecystokinin (CCK58): amino acid sequence. Peptides. 1982 Jul-Aug;3(4):687–691. doi: 10.1016/0196-9781(82)90171-1. [DOI] [PubMed] [Google Scholar]
  14. Eysselein V. E., Reeve J. R., Jr, Shively J. E., Miller C., Walsh J. H. Isolation of a large cholecystokinin precursor from canine brain. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6565–6568. doi: 10.1073/pnas.81.21.6565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gubler U., Chua A. O., Hoffman B. J., Collier K. J., Eng J. Cloned cDNA to cholecystokinin mRNA predicts an identical preprocholecystokinin in pig brain and gut. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4307–4310. doi: 10.1073/pnas.81.14.4307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hanahan D., Meselson M. Plasmid screening at high colony density. Gene. 1980 Jun;10(1):63–67. doi: 10.1016/0378-1119(80)90144-4. [DOI] [PubMed] [Google Scholar]
  17. Imperiale M. J., Feldman L. T., Nevins J. R. Activation of gene expression by adenovirus and herpesvirus regulatory genes acting in trans and by a cis-acting adenovirus enhancer element. Cell. 1983 Nov;35(1):127–136. doi: 10.1016/0092-8674(83)90215-5. [DOI] [PubMed] [Google Scholar]
  18. Land H., Grez M., Hauser H., Lindenmaier W., Schütz G. 5'-Terminal sequences of eucaryotic mRNA can be cloned with high efficiency. Nucleic Acids Res. 1981 May 25;9(10):2251–2266. doi: 10.1093/nar/9.10.2251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  20. Muller J. E., Straus E., Yalow R. S. Cholecystokinin and its COOH-terminal octapeptide in the pig brain. Proc Natl Acad Sci U S A. 1977 Jul;74(7):3035–3037. doi: 10.1073/pnas.74.7.3035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ott M. O., Sperling L., Herbomel P., Yaniv M., Weiss M. C. Tissue-specific expression is conferred by a sequence from the 5' end of the rat albumin gene. EMBO J. 1984 Nov;3(11):2505–2510. doi: 10.1002/j.1460-2075.1984.tb02164.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Powell D. J., Friedman J. M., Oulette A. J., Krauter K. S., Darnell J. E., Jr Transcriptional and post-transcriptional control of specific messenger RNAs in adult and embryonic liver. J Mol Biol. 1984 Oct 15;179(1):21–35. doi: 10.1016/0022-2836(84)90304-8. [DOI] [PubMed] [Google Scholar]
  23. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  24. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schibler U., Hagenbüchle O., Wellauer P. K., Pittet A. C. Two promoters of different strengths control the transcription of the mouse alpha-amylase gene Amy-1a in the parotid gland and the liver. Cell. 1983 Jun;33(2):501–508. doi: 10.1016/0092-8674(83)90431-2. [DOI] [PubMed] [Google Scholar]
  26. Schibler U., Pittet A. C., Young R. A., Hagenbüchle O., Tosi M., Gellman S., Wellauer P. K. The mouse alpha-amylase multigene family. Sequence organization of members expressed in the pancreas, salivary gland and liver. J Mol Biol. 1982 Mar 5;155(3):247–266. doi: 10.1016/0022-2836(82)90004-3. [DOI] [PubMed] [Google Scholar]
  27. Schneider B. S., Monahan J. W., Hirsch J. Brain cholecystokinin and nutritional status in rats and mice. J Clin Invest. 1979 Nov;64(5):1348–1356. doi: 10.1172/JCI109591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shaw P. H., Held W. A., Hastie N. D. The gene family for major urinary proteins: expression in several secretory tissues of the mouse. Cell. 1983 Mar;32(3):755–761. doi: 10.1016/0092-8674(83)90061-2. [DOI] [PubMed] [Google Scholar]
  29. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  30. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tsai H. M., Garber B. B., Larramendi L. M. 3H-thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo: II. Dynamics of neuronal migration, displacement, and aggregation. J Comp Neurol. 1981 May 10;198(2):293–306. doi: 10.1002/cne.901980208. [DOI] [PubMed] [Google Scholar]
  32. Vanderhaeghen J. J., Signeau J. C., Gepts W. New peptide in the vertebrate CNS reacting with antigastrin antibodies. Nature. 1975 Oct 16;257(5527):604–605. doi: 10.1038/257604a0. [DOI] [PubMed] [Google Scholar]
  33. Walker M. D., Edlund T., Boulet A. M., Rutter W. J. Cell-specific expression controlled by the 5'-flanking region of insulin and chymotrypsin genes. Nature. 1983 Dec 8;306(5943):557–561. doi: 10.1038/306557a0. [DOI] [PubMed] [Google Scholar]
  34. Wallace R. B., Johnson M. J., Hirose T., Miyake T., Kawashima E. H., Itakura K. The use of synthetic oligonucleotides as hybridization probes. II. Hybridization of oligonucleotides of mixed sequence to rabbit beta-globin DNA. Nucleic Acids Res. 1981 Feb 25;9(4):879–894. doi: 10.1093/nar/9.4.879. [DOI] [PMC free article] [PubMed] [Google Scholar]

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