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J. Biol. Chem., Vol. 279, Issue 19, 20519-20528, May 7, 2004

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The Involvement of Two cdc2-related Kinases (CRKs) in Trypanosoma brucei Cell Cycle Regulation and the Distinctive Stage-specific Phenotypes Caused by CRK3 Depletion^*

Xiaoming Tu and Ching C. Wang

From the Department of Pharmaceutical Chemistry, University of California, San Francisco, California 94143-2280

Cyclin-dependent protein kinases are among the key regulators of eukaryotic cell cycle progression. Potential functions of the five cdc2-related kinases (CRK) in Trypanosoma brucei were analyzed using the RNA interference (RNA_i) technique. In both the procyclic and bloodstream forms of T. brucei, CRK1 is apparently involved in controlling the G₁/S transition, whereas CRK3 plays an important role in catalyzing cells across the G₂/M junction. A knockdown of CRK1 caused accumulation of cells in the G₁ phase without apparent phenotypic change, whereas depletion of CRK3 enriched cells of both forms in the G₂/M phase. However, two distinctive phenotypes were observed between the CRK3-deficient procyclic and bloodstream forms. The procyclic form has a majority of the cells containing a single enlarged nucleus plus one kinetoplast. There is also an enhanced population of anucleated cells, each containing a single kinetoplast known as the zoids (0N1K). The CRK3-depleted bloodstream form has an increased number of one nucleus-two kinetoplast cells (1N2K) and a small population containing aggregated multiple nuclei and multiple kinetoplasts. Apparently, these two forms have different mechanisms in cell cycle regulation. Although the procyclic form can be driven into cytokinesis and cell division by kinetoplast segregation without a completed mitosis, the bloodstream form cannot enter cytokinesis under the same condition. Instead, it keeps going through another G₁ phase and enters a new S phase resulting in an aggregate of multiple nuclei and multiple kinetoplasts in an undivided cell. The different leakiness in cell cycle regulation between two stage-specific forms of an organism provides an interesting and useful model for further understanding the evolution of cell cycle control among the eukaryotes.

Received for publication, November 25, 2003 , and in revised form, February 12, 2004.

^* This work was supported by National Institutes of Health Grant RO1 AI-2178. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed. Tel.: 415-476-1321; Fax: 415-476-3382; E-mail: ccwang{at}cgl.ucsf.edu.

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