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Chlorella Viruses Evoke a Rapid Release of K+ from Host Cells During the Early Phase of Infection

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Chlorella Viruses Evoke a Rapid Release of K+ from Host Cells During the Early Phase of Infection University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Virology Papers Virology, Nebraska Center for 3-15-2008 Chlorella Viruses Evoke a Rapid Release of K+ from Host Cells During the Early Phase of Infection Monika Neupartl Institute of Botany, Technische Universität Darmstadt, Schnittspahnstrasse 3, D-64287 Darmstadt, Germany Christine Meyer Institute of Botany, Technische Universität Darmstadt, Schnittspahnstrasse 3, D-64287 Darmstadt, Germany Isabell Woll Institute of Botany, Technische Universität Darmstadt, Schnittspahnstrasse 3, D-64287 Darmstadt, Germany Florian Frohns Institute of Botany, Technische Universität Darmstadt, Schnittspahnstrasse 3, D-64287 Darmstadt, Germany Ming Kang University of Nebraska-Lincoln, [email protected] See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/virologypub Part of the Virology Commons Neupartl, Monika; Meyer, Christine; Woll, Isabell; Frohns, Florian; Kang, Ming; Van Etten, James L.; Kramer, Detlef; Hertel, Brigitte; Moroni, Anna; and Thiel, Gerhard, "Chlorella Viruses Evoke a Rapid Release of K+ from Host Cells During the Early Phase of Infection" (2008). Virology Papers. 165. https://digitalcommons.unl.edu/virologypub/165 This Article is brought to you for free and open access by the Virology, Nebraska Center for at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Virology Papers by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Monika Neupartl, Christine Meyer, Isabell Woll, Florian Frohns, Ming Kang, James L. Van Etten, Detlef Kramer, Brigitte Hertel, Anna Moroni, and Gerhard Thiel This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ virologypub/165 Published in Virology 372:2 (March 15, 2008), pp. 340-348; doi 10.1016/j.virol.2007.10.024 Copyright © 2007 Elsevier Inc. Used by permission. http://www.elsevier.com/locate/yviro Submitted August 9, 2007; revised September 30, 2007; accepted October 24, 2007; published online November 28, 2007. Chlorella viruses evoke a rapid release of K+ from host cells during the early phase of infection Monika Neupärtl,1 Christine Meyer,1 Isabell Woll,1 Florian Frohns,1 Ming Kang,2 James L. Van Etten,2 Detlef Kramer,1 Brigitte Hertel,1 Anna Moroni,3 and Gerhard Thiel 1 1 Institute of Botany, Technische Universität Darmstadt, Schnittspahnstrasse 3, D-64287 Darmstadt, Germany 2 Department of Plant Pathology and Nebraska Center for Virology, 406 Plant Sciences Hall, University of Nebraska–Lincoln, Lincoln, NE 8583-0722, USA 3 Department of Biology and CNR IBF-Mi, and Istituto Nazionale di Fisica della Materia, Università degli Studi di Milano, Via Celoria 26, 20133 I-Milano, Italy Correspondence — G. Thiel, fax 49 06151163202, email [email protected] Abstract Infection of Chlorella NC64A cells by PBCV-1 produces a rapid depolarization of the host probably by incorporation of a viral-en- coded K+ channel (Kcv) into the host membrane. To examine the effect of an elevated conductance, we monitored the virus-stim- ulated efflux of K+ from the Chlorella cells. The results indicate that all 8 Chlorella viruses tested evoked a host specific K+ efflux with a concomitant decrease in the intracellular K+. This K+ efflux is partially reduced by blockers of the Kcv channel. Qualita- tively these results support the hypothesis that depolarization and K+ efflux are at least partially mediated by Kcv. The virus-trig- gered K+ efflux occurs in the same time frame as host cell wall degradation and ejection of viral DNA. Therefore, it is reasonable to postulate that loss of K+ and associated water fluxes from the host lower the pressure barrier to aid ejection of DNA from the vi- rus particles into the host. Keywords: Chlorella viruses, Viral K+ channel Kcv, K+ efflux, Phycodnaviridae, PBCV-1 Introduction Paramecium bursaria Chlorella virus (PBCV-1) was the first virus discovered to encode a functional K+ channel protein. The M2 protein from influenza virus A was the first pro- The 94-amino acid protein (called Kcv) produces a K+-se- tein encoded by a virus gene reported to form a functional lective and slightly voltage-sensitive conductance in Xeno- ion channel in heterologous systems (Pinto et al., 1992). pus oocytes (Plugge et al., 2000) and mammalian HEK293 Since these initial studies, gene products from several other (Moroni et al., 2002) and CHO cells (Gazzarrini et al., 2003). viruses have been described that either form functional ion Kcv is the smallest protein known to form a functional tet- channels (Schubert et al., 1996, Plugge et al., 2000, Wilson et rameric K+ selective channel and its predicted transmem- al., 2004, Melton et al., 2002 and Lu et al., 2006) or alter the brane (TM1)-pore-TM2 structure resembles canonical K+ conductance properties of their host cell membrane during channels (Gazzarrini et al., 2004, Pagliuca et al., 2007, Shim infection (Piller et al., 1998). Although these viral-encoded et al., 2007 and Tayefeh et al., 2007). membrane proteins are not always absolutely required PBCV-1 is a large, icosahedral (diameter of ~ 1900 Å), for virus replication, all of them enhance viral replication plaque-forming, dsDNA-containing virus that infects cer- (Gonzalez and Carrasco, 2003). With the exception of the tain Chlorella-like green algae (Van Etten, 2003 and Yamada proton conducting M2 channel, not much is known about et al., 2006). It is the prototype of a rapidly expanding group the specific function(s) of these membrane proteins in the of viruses in the family Phycodnaviridae. The 331-kb PBCV-1 viral life cycles although protein VPU from virus HIV1 is genome has ~ 365 protein-encoding genes and 11 tRNA-en- involved in the release of progeny viruses (Carrasco, 1995, coding genes. The PBCV-1 virion is a multi-layered structure Fischer and Sansom, 2002 and Hsu et al., 2004). composed of the genome, a lipid bilayer membrane and an 340 C HLORELLA VIRUSES EVOKE RELEASE OF K + DURING EARLY PHASE INFECTION 341 outer icosahedral capsid shell (Yan et al., 2000). PBCV-1 in- host Chlorella cells. The results indicate that the host cells re- fects its host by attaching to the external surface of the algal lease measurable amounts of K+ during the first few min- cell wall. Attachment occurs at a unique virus vertex (On- utes after infection and that this loss of K+ can be mechanis- imatsu et al., 2006) and is followed by degradation of the tically related to the properties of the Kcv channel. host wall at the attachment point by virion-packaged, wall digesting enzymes (Meints et al., 1984). Following host cell Results wall degradation, the internal membrane of the virus prob- ably fuses with the host membrane leading to entry of the To define the early events associated with PBCV-1 in- viral DNA and virion-associated proteins. An empty cap- fection, the time of virus attachment, cell wall degrada- sid is left on the cell surface. Infection results in rapid de- tion and virus DNA ejection was measured by electron mi- polarization of the host membrane (Frohns et al., 2006 and croscopy. Chlorella NC64A cells were incubated with virus Mehmel et al., 2003), and physiological studies have led to PBCV-1 at an m.o.i. of 100; infection was stopped at var- the hypothesis that this rapid depolarization is caused by ious times post infection (p.i.) by transferring cells into a the Kcv channel that is predicted to be located in the virus mixture of cold glutaraldehyde/formaldehyde. After addi- internal membrane. That is, during infection the Kcv chan- tional fixation steps (Frohns et al., 2006), the samples were nel is inserted into the plasma membrane of the host caus- examined by electron microscopy. Figure 1A shows rep- ing a short circuit of the host membrane potential. Pre- resentative images obtained 6 min p.i.: (i) the virus is at- sumably this depolarization is essential for virus infection tached to the host cell, (ii) the virus has digested a hole in because certain K+ channel blockers partially prevent the vi- the cell wall and (iii) the virus has ejected its DNA into the rus-induced membrane depolarization and the ejection of host. A statistical analysis of more than 1200 electron mi- viral DNA into the host cells; thus subsequent virus repli- crographs (see Frohns et al., 2006) provided the dynamics cation in the host is inhibited (Frohns et al., 2006). We pre- of the three stages of infection (Figure 1B). Attachment oc- dict that the PBCV-1-induced depolarization and the aug- curs in a biphasic manner with a rapid and a slow compo- + + mented K conductance effects K fluxes in the host cells. In nent; the half time (t1/2A) of this process is about 20 s. After this manuscript, we examine the effect of infection by 8 dif- a short time, cell wall degradation (t1/2 L = 2 min) and DNA + ferent Chlorella viruses, including PBCV-1, on K fluxes in ejection (t1/2 D = 4.1 min) occur. Figure 1. Time course of early stages of virus PBCV-1 infection of Chlorella NC64A cells. The electron micrographs on the left (A) were taken 6 min p.i. after infecting Chlorella cells with an m.o.i. of 100. The images present three defined and sequential stages of infection: attachment (■), degrada- tion of the host cell wall (○) and empty virus capsids after ejection of DNA into the host cell (●). Electron micrographs of infections terminated at different times p.i. were analyzed with respect to the relative occurrences of these three stages. The relative frequency of the three stages is shown as a function of time p.i. in (B). From the graph the following half times can be calculated: attachment (t1/2A) = 20 s; wall degradation (t1/2L) = 2 min; DNA ejection (t1/2D) = 4.1 min.
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