Environmental reprogramming of the expression of protein kinase CK2β subunit in fish

  • Marco Alvarez
  • Gudrun Kausel
  • Jaime Figueroa
  • María Inés Vera
Part of the Molecular and Cellular Biochemistry book series (DMCB, volume 35)


The dramatic segregation of the nucleolar components in winter-acclimatized carp is the most striking cellular-phenotypical feature observed during the seasonal adaptation of this fish toward the circannual changes in its habitat. Our studies also show that the carp habitat temperature and photoperiod winter conditions provoke a remarkable reduction of both rRNA transcription and the processing of their precursors. To gain knowledge on the mechanisms involved in the regulation of nucleolar activity during the seasonal adaptation process, we studied the behavior of some genes, specifically snoRNA U3 and protein kinase CK2.

Consistent with the reduction in the synthesis and processing of pre-rRNA observed during the cold season, the level of CK2β expression decreases in winter when compared to that attained in summer. Similarly, in winter, liver and kidney cells contain lower levels of CK213 subunit protein compared to summer. CK2 is associated with or modifies different factors and enzymes involved in the nucleolar activity; therefore, its higher or lower content could be part of the molecular mechanisms underlying the nucleolar seasonal changes that occur during the compensatory acclimatization process. (Mol Cell Biochem 227: 107-112, 2001)

Key words

protein kinase CK23 subunit nucleolus fish acclimatization carp 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Krauskopf M, Amthauer R, Araya A, Concha M, León G, Ríos L, Vera MI, Villanueva J: Temperature acclimatization of the carp. Cellular and molecular aspects of the compensatory response. Arch Biol Med Exp 21: 151–157, 1988PubMedGoogle Scholar
  2. 2.
    Figueroa J, Molina A, Alvarez M, Villanueva J, Reyes A, León G, Krauskopf M: Prolactin gene expression and changes of prolactin pituitary level during the seasonal acclimatization of the carp. Comp Biochem Physiol 108B: 551–560, 1994Google Scholar
  3. 3.
    Goldspink G: Adaptation of fish to different environmental temperature by qualitative and quantitative changes in gene expression. J Therm Biol 20: 167–174, 1995CrossRefGoogle Scholar
  4. 4.
    Tiku PE, Gracey AY, Macartney AI, Beynon RJ, Cossins AR: Cold-induced expression of A9-desaturase in carp by transcriptional and posttranscriptional mechanisms. Science 271: 815–818, 1996PubMedCrossRefGoogle Scholar
  5. 5.
    Kausel G, Vera MI, San Martín R, Figueroa J, Molina A, Muller M, Martial J, Krauskopf M: Transcription factor Pit-1 expression is modulated upon seasonal acclimatization of eurythermal ectotherms: Identification of two Pit-1 genes in the carp. J Cell Biochem 75: 598–609, 1999PubMedCrossRefGoogle Scholar
  6. 6.
    Sarmiento J, Leal S, Quezada C, Kausel G, Figueroa J, Vera MI, Krauskopf M: Environmental acclimatization of the carp modulates the transcription of 3-actin. J Cell Biochem 80: 223–228, 2000PubMedCrossRefGoogle Scholar
  7. 7.
    Sáez L, Zuvic T, Amthauer R, Rodríguez E, Krauskopf M: Fish liver protein synthesis during cold acclimatization. Seasonal changes of the ultrastructure of the carp hepatocyte. J Exp Zool 230: 175–186, 1984PubMedCrossRefGoogle Scholar
  8. 8.
    Vera MI, Norambuena L, Alvarez M, Figueroa J, Molina A, León G, Krauskopf M: Reprogramming of nucleolar gene expression during the acclimatization of the carp. Cell Mol Biol Res 39: 665–674, 1993PubMedGoogle Scholar
  9. 9.
    Vera MI, Ríos HM, de la Fuente E, Figueroa J, Krauskopf M: Seasonal acclimatization of the carp involves differential expression of 5.8S ribosomal RNA in pituitary cells. Comp Biochem Physiol 118B: 777–781, 1997Google Scholar
  10. 10.
    Sáez L, Amthauer R, Rodríguez E, Krauskopf M: Effects of insulin on the fine structure of hepatocytes from winter-acclimatized carp: Studies on protein synthesis. J Exp Zool 230: 187–197, 1984PubMedCrossRefGoogle Scholar
  11. 11.
    Vera MI, Romero F, Figueroa J, Amthauer R, León G, Villanueva J, Krauskopf M: Oral administration of insulin in winter-acclimatized carp (Cyprinus carpio) induces hepatic ultrastructural changes. Comp Biochem Physiol 106A: 677–682, 1993CrossRefGoogle Scholar
  12. 12.
    Hannan R, Taylor L, Cavanaugh A, Hannan K, Rothblum LI: UBF and the regulation of ribosomal DNA transcription. In: M.R. Paule (ed). Transcription of Ribosomal RNA Genes by Eukaryotic RNA Polymer-ase I. Springer-Verlag, Berlin, Heidelberg, 1998, pp 221–228Google Scholar
  13. 13.
    Csermely P, Schnaider T, Chatman B, Olson MOJ, Kahn CR: Insulin induces the phosphorylation of nucleolin. J Biol Chem 268: 9747–9752, 1993Google Scholar
  14. 14.
    Guerra B, Issinger O-G: Protein kinase CK2 and its role in cellular proliferation, development and pathology. Electrophoresis 20: 391408, 1999CrossRefGoogle Scholar
  15. 15.
    Allende JE, Allende CC: Protein kinase CK2: An enzyme with multiple substrates and puzzling regulation. FASEB J 9: 313–323, 1995PubMedGoogle Scholar
  16. 16.
    Vera MI, Kausel G, Barrera R, Leal S, Figueroa J, Quezada C: Seasonal adaptation modulates the expression of the protein kinase CK2(3 subunit gene in the carp. Biochem Biophys Res Com 271: 735–740, 2000PubMedCrossRefGoogle Scholar
  17. 17.
    Leal S, Kausel G, Figueroa J, Escobar J, Pinto R, San Martín R, Vera MI: Quantification of the expression of CK213 subunit during the acclimatization of the fish C. carpio. Biol Res: R-90, 2000Google Scholar
  18. 18.
    Stenberger LA, Hardy PH, Cuculis JJ, Meyer HG: The unlabeled antibody enzyme method of immunochemistry. J Histochem Cytochem 18: 315–333, 1970CrossRefGoogle Scholar
  19. 19.
    Inostroza J, Vera MI, Goicoechea O, Amthauer R, Krauskopf M: Apo-lipoprotein A-I synthesis during the acclimatization of the carp (Cyprinus carpio). J Exp Zool 256: 8–15, 1990CrossRefGoogle Scholar
  20. 20.
    Litchfield DW, Lozeman FJ, Cicirelli MF, Harrylock M, Ericsson LH, Piening CJ, Krebs EG: Phosphorylation of the beta subunit of casein kinase II in human A431 cells. Identification of the autophosphorylation site and a site phosphorylated by p34ctic2. J Biol Chem 266: 20380–20389,1991PubMedGoogle Scholar
  21. 21.
    Litchfield DW, Luscher B, Lozeman FJ, Eisenman RN, Krebs EG: Phosphorylation of casein kinase II by p34cdc2 in vitro and at mitosis. J Biol Chem 267: 13943–13951, 1992PubMedGoogle Scholar
  22. 22.
    Kausel G, Vera M-I, Figueroa J, Hernández J, San Martin R, Molina A, Chavez VM, Muller M, Martial J, Krauskopf M: Effect of seasonal acclimatization on the expression of the carp transcription factor Pit-1. Biochem Mol Biol Int 45: 813–821, 1998PubMedGoogle Scholar
  23. 23.
    Peitsch MC: ProMod and Swiss-Model: Internet-based tools for automated comparative protein modeling. Biochem Soc Trans 24: 274–279, 1996PubMedGoogle Scholar
  24. 24.
    Koradi R, Billeter M, Wüthrich K: MOLMOL: A program for display and analysis of macromolecular structures. J Mol Graphics 14: 51–55, 1996CrossRefGoogle Scholar
  25. 25.
    Chantalat L, Leroy D, Filhol O, Nueda A, Benitez MJ, Chambaz EM, Cochet C, Dideberg O: Crystal structure of the human protein kinase CK2 regulatory subunit reveals its zinc finger-mediated dimerization. EMBO J 18: 2930–2940, 1999PubMedCrossRefGoogle Scholar
  26. 26.
    Krek W, Maridor G, Nigg EA: Casein kinase II is a predominantly nuclear enzyme. J Cell Biol 116: 43–55, 1992PubMedCrossRefGoogle Scholar
  27. 27.
    Gerber D, Souquere-Besse S, Puvio F, Dubois M-F, Bensaude O, Cochet C: Heat-induced relocalization of protein kinase CK2. Implication of CK2 in the context of cellular stress. J Biol Chem 275: 23919–23926, 2000PubMedCrossRefGoogle Scholar
  28. 28.
    Faust M, Monternah M: Subcellular localization of protein kinase CK2. A key to its function? Cell Tissue Res 301: 329–340, 2000PubMedCrossRefGoogle Scholar
  29. 29.
    Faust RA, Gapany M, Tristani P, Davis A, Adams GL, Ahmed K: Elevated protein kinase CK2 activity in chromatin of head and neck tumors: Association with malignant transformation. Cancer Lett 101: 31–35, 1996PubMedCrossRefGoogle Scholar
  30. 30.
    Figueroa J, Reyes A, Ríos M, Vera, MI, Krauskopf M: Effect of temperature and photoperiod on prolactin transcription in Cyprinus Carpio. Zool Sci 14: 353–357, 1997CrossRefGoogle Scholar
  31. 31.
    Ginisty H, Sicard H, Roger B, Bouvet P: Structure and functions of nucleolin. J Cell Sei 112: 761–772, 1999Google Scholar

Copyright information

© Springer Science+Business Media New York 2001

Authors and Affiliations

  • Marco Alvarez
    • 1
  • Gudrun Kausel
    • 2
  • Jaime Figueroa
    • 2
  • María Inés Vera
    • 1
  1. 1.Laboratorio de Biología Celular y Molecular, Facultad de Ciencias de la SaludUniversidad Andrés Bello and MIFABSantiagoChile
  2. 2.Instituto de Bioquímica, Facultad de CienciasUniversidad Austral de ChileValdiviaChile

Personalised recommendations