Trichinella Spiralis-infected Muscle Cells: Abundant RNA Polymerase II in Nuclear Speckle Domains Colocalizes with Nuclear Antigens

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 2001 May 12

PMID 11349077

Citations 2

Authors

C Yao

D P Jasmer

Affiliations

Soon will be listed here.

Abstract

Infection of mammalian skeletal muscle cells by Trichinella spiralis causes host nuclei to become polyploid (ca. 4N) and abnormally enlarged. It has been postulated that this enlargement reflects an infection-induced elevation of host transcription. Anthelmintic treatment of T. spiralis-infected rodents with mebendazole (MBZ) causes a reduction in the size of infected cell nuclei and a significant reduction in the total RNA content of individual infected muscle cells. A monoclonal antibody to the large subunit of RNA polymerase II (Pol II) was used here to assess the effects of infection on Pol II levels in isolated infected cell nuclei. Pol II was localized to speckle domains in isolated infected cell nuclei. Similar domains have been previously localized to sites of RNA synthesis or processing. When compared to the levels in nuclei from other, uninfected host cells, speckle-localized Pol II (SL-Pol II) levels were significantly elevated in infected cell nuclei by a mean of 3.9- to 6.8-fold. Nuclear antigens (NA) recognized by antibodies against T. spiralis localized to infected cell nuclei. By use of confocal microscopy, a subpopulation of NA was found colocalized with most speckle domains defined by Pol II. MBZ treatment of chronically infected mice, which depletes NA from infected cell nuclei, caused a significant depletion of SL-Pol II from infected cell nuclei. Control nuclei had a mean of 70% more SL-Pol II than MBZ-treated nuclei. The mean residual level of Pol II in these polyploid nuclei remained elevated by 120% over the level in 2N control nuclei. These observations may indicate two distinct effects of infection on Pol II levels in host cells.

Citing Articles

Matrix metalloproteinase-9 (MMP-9) and tissue inhibitor of metalloproteinases 1 (TIMP-1) are localized in the nucleus of retinal Müller glial cells and modulated by cytokines and oxidative stress.

Lee E, Zheng M, Craft C, Jeong S PLoS One. 2021; 16(7):e0253915.

PMID: 34270579 PMC: 8284794. DOI: 10.1371/journal.pone.0253915.

Trichinella spiralis: nurse cell formation with emphasis on analogy to muscle cell repair.

Wu Z, Sofronic-Milosavljevic L, Nagano I, Takahashi Y Parasit Vectors. 2008; 1(1):27.

PMID: 18710582 PMC: 2538513. DOI: 10.1186/1756-3305-1-27.

References

Jasmer D, Reduker D, Hines S, Perryman L, McGuire T . Surface epitope localization and gene structure of a Babesia bovis 44-kilodalton variable merozoite surface antigen. Mol Biochem Parasitol. 1992; 55(1-2):75-83. DOI: 10.1016/0166-6851(92)90128-7. View

Olson E, Brennan T, Chakraborty T, Cheng T, Cserjesi P, Edmondson D . Molecular control of myogenesis: antagonism between growth and differentiation. Mol Cell Biochem. 1991; 104(1-2):7-13. DOI: 10.1007/BF00229797. View

Bregman D, Du L, van der Zee S, WARREN S . Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J Cell Biol. 1995; 129(2):287-98. PMC: 2199908. DOI: 10.1083/jcb.129.2.287. View

Jasmer D, Reduker D, Perryman L, McGuire T . A Babesia bovis 225-kilodalton protein located on the cytoplasmic side of the erythrocyte membrane has sequence similarity with a region of glycogen phosphorylase. Mol Biochem Parasitol. 1992; 52(2):263-9. DOI: 10.1016/0166-6851(92)90058-r. View

Dirks R, Hattinger C, Molenaar C, Snaar S . Synthesis, processing, and transport of RNA within the three-dimensional context of the cell nucleus. Crit Rev Eukaryot Gene Expr. 2000; 9(3-4):191-201. DOI: 10.1615/critreveukargeneexpr.v9.i3-4.40. View

Xing Y, Johnson C, Dobner P, Lawrence J . Higher level organization of individual gene transcription and RNA splicing. Science. 1993; 259(5099):1326-30. DOI: 10.1126/science.8446901. View

Thompson N, Steinberg T, Aronson D, Burgess R . Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II. J Biol Chem. 1989; 264(19):11511-20. View

Jasmer D . Trichinella spiralis infected skeletal muscle cells arrest in G2/M and cease muscle gene expression. J Cell Biol. 1993; 121(4):785-93. PMC: 2119794. DOI: 10.1083/jcb.121.4.785. View

MAEIR D, ZAIMAN H . The development of lysosomes in rat skeletal muscle in trichinous myositis. J Histochem Cytochem. 1966; 14(5):396-400. DOI: 10.1177/14.5.396. View

10.

Polvere R, Kabbash C, Capo V, Kadan I, Despommier D . Trichinella spiralis: synthesis of type IV and type VI collagen during nurse cell formation. Exp Parasitol. 1997; 86(3):191-9. DOI: 10.1006/expr.1997.4180. View

11.

Appleton J, Schain L, McGregor D . Rapid expulsion of Trichinella spiralis in suckling rats: mediation by monoclonal antibodies. Immunology. 1988; 65(3):487-92. PMC: 1385491. View

12.

Zhang G, TANEJA K, Singer R, Green M . Localization of pre-mRNA splicing in mammalian nuclei. Nature. 1994; 372(6508):809-12. DOI: 10.1038/372809a0. View

13.

Jasmer D . Trichinella spiralis: altered expression of muscle proteins in trichinosis. Exp Parasitol. 1990; 70(4):452-65. DOI: 10.1016/0014-4894(90)90130-5. View

14.

Gustowska L, Gabryel P, Rauhut W . [The role of the muscle cell nucleus in the mechanism of its transformation after infection by Trichinella spiralis larvae. II. Histochemical features of the functional transformation of the muscle cell nucleus in the course of infection]. Wiad Parazytol. 1989; 35(5):401-11. View

15.

Reason A, Ellis L, Appleton J, Wisnewski N, Grieve R, McNeil M . Novel tyvelose-containing tri- and tetra-antennary N-glycans in the immunodominant antigens of the intracellular parasite Trichinella spiralis. Glycobiology. 1994; 4(5):593-603. DOI: 10.1093/glycob/4.5.593. View

16.

Mortillaro M, Blencowe B, Wei X, Nakayasu H, Du L, WARREN S . A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix. Proc Natl Acad Sci U S A. 1996; 93(16):8253-7. PMC: 38656. DOI: 10.1073/pnas.93.16.8253. View

17.

Yao C, Bohnet S, Jasmer D . Host nuclear abnormalities and depletion of nuclear antigens induced in Trichinella spiralis-infected muscle cells by the anthelmintic mebendazole. Mol Biochem Parasitol. 1998; 96(1-2):1-13. DOI: 10.1016/s0166-6851(98)00082-6. View

18.

Jasmer D, Bohnet S, Prieur D . Trichinella spp.: differential expression of acid phosphatase and myofibrillar proteins in infected muscle cells. Exp Parasitol. 1991; 72(3):321-31. DOI: 10.1016/0014-4894(91)90152-m. View

19.

Capo V, Despommier D, Polvere R . Trichinella spiralis: vascular endothelial growth factor is up-regulated within the nurse cell during the early phase of its formation. J Parasitol. 1998; 84(2):209-14. View

20.

Jasmer D, Yao S, Vassilatis D, Despommier D, Neary S . Failure to detect Trichinella spiralis p43 in isolated host nuclei and in irradiated larvae of infected muscle cells which express the infected cell phenotype. Mol Biochem Parasitol. 1994; 67(2):225-34. DOI: 10.1016/0166-6851(94)00131-6. View