Skip to main content
SpringerLink
Log in

Ribosomal RNA Genes and Their Regulation in Entamoeba histolytica

  • Chapter
  • First Online:
Amebiasis

  • 1351 Accesses

Abstract

The transcription of ribosomal RNA genes is tightly regulated in response to different environmental and growth stress conditions. This chapter summarizes our current understanding of such regulation in Entamoeba histolytica. The rRNA genes of E. histolytica are located exclusively on extrachromosomal plasmids, which may have one transcription unit (rDNA I) or two units (rDNA I and rDNA II) per circle. These plasmids are localized to the nuclear periphery where the nucleolus has been mapped using antibodies against RNA polymerase I and a known nucleolar marker, fibrillarin. Transcription of rDNA I is driven by two promoters, P1 and P2, which are 1.5 kb apart. Pre-rRNAs are transcribed from both promoters under normal growth conditions, although P1 is a weaker promoter. Upon growth stress (serum starvation and cycloheximide treatment), pre-rRNAs accumulate from promoter P2 but not P1, showing that the two promoters respond differentially to stress. Surprisingly, we found that transcripts of 0.7–0.9 kb also accumulated along with pre-rRNA under stress. These transcripts map to the 5′-external transcribed spacer (ETS) of pre-rRNA from promoter P2. These novel transcripts are heterogeneously sized circular molecules and accumulate as noncoding RNA. They can spontaneously self-circularize in vitro in the absence of cellular proteins. Because the 5′-ETS has binding sites for pre-rRNA processing factors, we speculate that these circular transcripts inhibit processing of pre-rRNA by sequestering the processing factors. Thus, ribosome biogenesis during growth stress in E. histolytica seems to be controlled posttranscriptionally by downregulating the processing of pre-rRNA.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ETS:

External transcribed spacer

IGS:

Intergenic spacer

ITS:

Internal transcribed spacer

NoRC:

Nucleolar remodeling complex

ori:

Origin

rDNA:

Ribosomal DNA

rRNA:

Ribosomal RNA

RNA Pol:

RNA polymerase

tsp:

Transcription start point

References

  1. Grummt I (2003) Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 7:1691–1702

    Article  Google Scholar 

  2. Moss T (2004) At the crossroads of growth control; making ribosomal RNA. Curr Opin Genet Dev 14:210–217

    Article  CAS  PubMed  Google Scholar 

  3. Long EO, Dawid IB (1980) Repeated genes in eukaryotes. Annu Rev Biochem 49:727–764

    Article  CAS  PubMed  Google Scholar 

  4. Grummt I, Langst G (2012) Epigenetic control of RNA polymerase I transcription in mammalian cells. Biochim Biophys Acta 1829:393–404

    Article  PubMed  Google Scholar 

  5. French SL, Osheim YN, Cioci F, Nomura M, Beyer AL (2003) In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes. Mol Cell Biol 23:1558–1568

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Mayer C, Schmitz KM, Li J, Grummt I, Santoro R (2006) Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 22:351–361

    Article  CAS  PubMed  Google Scholar 

  7. Mayer C, Neubert M, Grummt I (2008) The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep 9:774–780

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Santoro R, Schmitz KM, Sandoval J, Grummt I (2010) Intergenic transcripts originating from a subclass of ribosomal DNA repeats silence ribosomal RNA genes in trans. EMBO Rep 11:52–58

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Laferte A, Favry E, Sentenac A, Riva M, Carles C, Chedin S (2006) The transcriptional activity of RNA polymerase I is a key determinant for the level of all ribosome components. Genes Dev 20:2030–2040

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Young RA, Davis RW (1983) Yeast RNA polymerase II genes: isolation with antibody probes. Science 222:778–782

    Article  CAS  PubMed  Google Scholar 

  11. Valenzuela P, Bell GI, Weinberg F, Rutter WJ (1976) Yeast DNA dependent RNA polymerases I, II and III. The existence of subunits common to the three enzymes. Biochem Biophys Res Commun 71:1319–1325

    Article  CAS  PubMed  Google Scholar 

  12. Vanik JM, Detke S, Albach RA (1986) Partial characterization of DNA-dependent RNA polymerases from Entamoeba histolytica. Arch Invest Med (Mex) 17:101–106

    CAS  Google Scholar 

  13. Jhingan GD (2008) Studies on RNA polymerase basal transcription factors in Entamoeba histolytica. PhD thesis. Jawaharlal Nehru University, New Delhi

    Google Scholar 

  14. Allison LA, Moyle M, Shales M, Ingles CJ (1985) Extensive homology among the largest subunits of eukaryotic and prokaryotic RNA polymerases. Cell 42:599–610

    Article  CAS  PubMed  Google Scholar 

  15. Knackmuss S, Bautz EF, Petersen G (1997) Identification of the gene coding for the largest subunit of RNA polymerase I (A) of Drosophila melanogaster. Mol Gen Genet 253:529–534

    Article  CAS  PubMed  Google Scholar 

  16. Lalo D, Carles C, Sentenac A, Thuriaux P (1993) Interactions between three common subunits of yeast RNA polymerases I and III. Proc Natl Acad Sci USA 90:5524–5528

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Jhingan GD, Panigrahi SK, Bhattacharya A, Bhattacharya S (2009) The nucleolus in Entamoeba histolytica and Entamoeba invadens is located at the nuclear periphery. Mol Biochem Parasitol 167:72–80

    Article  CAS  PubMed  Google Scholar 

  18. Quon DV, Delgadillo MG, Johnson PJ (1996) Transcription in the early diverging eukaryote Trichomonas vaginalis: an unusual RNA polymerase II and alpha-amanitin-resistant transcription of protein-coding genes. J Mol Evol 43:253–262

    Article  CAS  PubMed  Google Scholar 

  19. Cramer P, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: RNA polymerase II at 2.8 Ǻ resolution. Science 292:1863–1876

    Article  CAS  PubMed  Google Scholar 

  20. Lioutas C, Tannich E (1995) Transcription of protein-coding genes in Entamoeba histolytica is insensitive to high concentrations of alpha-amanitin. Mol Biochem Parasitol 73:259–261

    Article  CAS  PubMed  Google Scholar 

  21. Pearson RJ, Singh U (2010) Approaches to characterizing Entamoeba histolytica transcriptional regulation. Cell Microbiol 12:1681–1690

    Article  CAS  PubMed  Google Scholar 

  22. Sucganag R et al (2003) Sequence and structure of the extrachromosomal palindrome encoding the ribosomal RNA genes in Dictyostelium. Nucleic Acids Res 31:2361–2368

    Article  Google Scholar 

  23. Clark CG, Cross GA (1987) rRNA genes of Naegleria gruberi are carried exclusively on a 14-kilobase-pair plasmid. Mol Cell Biol 7:3027–3031

    CAS  PubMed Central  PubMed  Google Scholar 

  24. Ravel-Chapuis P, Nicolas P, Nigon V, Neyret O, Freyssinet G (1985) Extrachromosomal circular nuclear rDNA in Euglena gracilis. Nucleic Acids Res 13:7529–7537

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Bhattacharya S, Bhattacharya A, Diamond LS (1988) Comparison of repeated DNA from strains of Entamoeba histolytica and other Entamoeba. Mol Biochem Parasitol 27:257–262

    Article  CAS  PubMed  Google Scholar 

  26. Bhattacharya S, Bhattacharya A, Diamond LS, Soldo AT (1989) Circular DNA of Entamoeba histolytica encodes ribosomal RNA. J Protozool 36:455–458

    Article  CAS  PubMed  Google Scholar 

  27. Huber M, Koller B, Gitler C, Mirelman D, Revel M, Rozenblatt S, Garfinkel L (1989) Entamoeba histolytica ribosomal RNA genes are carried on palindromic circular DNA molecules. Mol Biochem Parasitol 32:285–296

    Article  CAS  PubMed  Google Scholar 

  28. Sehgal D, Mittal V, Ramachandran S, Dhar SK, Bhattacharya A, Bhattacharya S (1994) Nucleotide sequence organisation and analysis of the nuclear ribosomal DNA circle of the protozoan parasite Entamoeba histolytica. Mol Biochem Parasitol 67:205–214

    Article  CAS  PubMed  Google Scholar 

  29. Bhattacharya S, Som I, Bhattacharya A (1998) The ribosomal DNA plasmids of Entamoeba. Parasitol Today 14:181–185

    Article  CAS  PubMed  Google Scholar 

  30. Ghosh S, Zaki M, Clark CG, Bhattacharya S (2001) Recombinational loss of a ribosomal DNA unit from the circular episome of Entamoeba histolytica HM-1:IMSS. Mol Biochem Parasitol 116:105–108

    Article  CAS  PubMed  Google Scholar 

  31. Paul J, Bhattacharya A, Bhattacharya S (2002) Close sequence identity between ribosomal DNA episomes of the nonpathogenic Entamoeba dispar and pathogenic Entamoeba histolytica. J Biosci 27:619–627

    Article  CAS  Google Scholar 

  32. Srivastava S, Bhattacharya S, Paul J (2005) Species- and strain-specific probes derived from repetitive DNA for distinguishing Entamoeba histolytica and Entamoeba dispar. Exp Parasitol 110:303–308

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Dhar SK, Choudhury NR, Mittal V, Bhattacharya A, Bhattacharya S (1996) Replication initiates at multiple dispersed sites in the ribosomal DNA plasmid of the protozoan parasite Entamoeba histolytica. Mol Cell Biol 16:2314–2324

    CAS  PubMed Central  PubMed  Google Scholar 

  34. Ghosh S, Satish S, Tyagi S, Bhattacharya A, Bhattacharya S (2003) Differential use of multiple replication origins in the ribosomal DNA episome of the protozoan parasite Entamoeba histolytica. Nucleic Acids Res 31:2035–2044

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Mahbubani HM, Paull T, Elder JK, Blow JJ (1992) DNA replication initiates at multiple sites on plasmid DNA in Xenopus egg extracts. Nucleic Acids Res 20:1457–1462

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Hyrien O, Maric C, Méchali M (1995) Transition in specification of embryonic metazoan DNA replication origins. Science 270:994–997

    Article  CAS  PubMed  Google Scholar 

  37. Venema J, Tollervey D (1999) Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet 33:261–311

    Article  CAS  PubMed  Google Scholar 

  38. Koberna K et al (2002) Ribosomal genes in focus: new transcripts label the dense fibrillar components and form clusters indicative of “Christmas trees” in situ. J Cell Biol 157:743–748

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Pederson T (2011) The nucleolus. Cold Spring Harbor Perspect Biol. doi:10.1101/cshperspect.a000638

    Google Scholar 

  40. Zurita M, Alagon A, Vargas-Villarreal J, Lizardi PM (1991) The Entamoeba histolytica rDNA episome: nuclear localization, DNAase I sensitivity map, and specific DNA-protein interactions. Mol Microbiol 5:1843–1851

    Article  CAS  PubMed  Google Scholar 

  41. Raska I, Shaw PJ, Cmarko D (2006) Structure and function of the nucleolus in the spotlight. Curr Opin Cell Biol 18:325–334

    Article  CAS  PubMed  Google Scholar 

  42. Henras AK, Soudet J, Gérus M, Lebaron S, Caizergues-Ferrer M, Mougin A, Henry Y (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 65:2334–2359

    Article  CAS  PubMed  Google Scholar 

  43. Jacob ST (1995) Regulation of ribosomal gene transcription. Biochem J 306:617–626

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Russell J, Zomerdijk JC (2005) RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem Sci 30:87–96

    Article  CAS  PubMed  Google Scholar 

  45. Michel B, Lizardi PM, Alagón A, Zurita M (1995) Identification and analysis of the start site of ribosomal RNA transcription of Entamoeba histolytica. Mol Biochem Parasitol 73:19–30

    Article  CAS  PubMed  Google Scholar 

  46. Panigrahi SK, Jhingan GD, Som I, Bhattacharya A, Petri WA Jr, Bhattacharya S (2009) Promoter analysis of palindromic transcription units in the ribosomal DNA circle of Entamoeba histolytica. Eukaryot Cell 8:69–76

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Schroth GP, Siino JS, Cooney CA, Th’ng JP, Ho PS, Bradbury EM (1992) Intrinsically bent DNA flanks both sides of an RNA polymerase I transcription start site: both regions display novel electrophoretic mobility. J Biol Chem 267:9958–9964

    CAS  PubMed  Google Scholar 

  48. Kneidl C, Dinkl E, Grummt F (1995) An intrinsically bent region upstream of the transcription start site of the rRNA genes of Arabidopsis thaliana interacts with an HMG-related protein. Plant Mol Biol 27:705–713

    Article  CAS  PubMed  Google Scholar 

  49. Zacharias M, Theissen G, Bradaczek C, Wagner R (1991) Analysis of sequence elements important for the synthesis and control of rRNA in Escherichia coli. Biochimie 73:699–712

    Article  CAS  PubMed  Google Scholar 

  50. Sylvester JE, Petersen R, Schmickel RD (1989) Human ribosomal DNA: novel sequence organization in a 4.5-kb region upstream from the promoter. Gene (Amst) 84:193–196

    Article  CAS  Google Scholar 

  51. Bateman E, Iida CT, Kownin P, Paule MR (1985) Footprinting of rRNA genes by transcription initiation factor and RNA polymerase I. Proc Natl Acad Sci USA 82:8004–8008

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Doelling JH, Pikaard CS (1995) The minimal rRNA gene promoter of Arabidopsis thaliana includes a critical element at the transcription initiation site. Plant J 8:683–692

    Article  CAS  PubMed  Google Scholar 

  53. Gallagher JE, Dunbar DA, Granneman S, Mitchell BM, Osheim Y, Beyer AL, Baserga SJ (2004) RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev 18:2506–2517

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Gupta AK, Panigrahi SK, Bhattacharya A, Bhattacharya S (2012) Self-circularizing 59-ETS RNAs accumulate along with unprocessed pre-ribosomal RNAs in growth-stressed Entamoeba histolytica. Sci Rep 2:303

    Article  PubMed Central  PubMed  Google Scholar 

  55. Zhao J, Yuan X, Frodin M, Grummt I (2003) ERK-dependent phosphorylation of the transcription initiation factor TIF-IA is required for RNA polymerase I transcription and cell growth. Mol Cell 11:405–413

    Article  CAS  PubMed  Google Scholar 

  56. Gokal PK, Cavanaugh AH, Thompson EA Jr (1986) The effects of cycloheximide upon transcription of rRNA, 5 S RNA, and tRNA genes. J Biol Chem 261:2536–2541

    CAS  PubMed  Google Scholar 

  57. Bourbon H, Michot B, Hassouna N, Feliu J, Bachellerie JP (1988) Sequence and secondary structure of the 5′-external transcribed spacer of mouse pre-rRNA. DNA 7:181–191

    Article  CAS  PubMed  Google Scholar 

  58. Hughes JM, Ares M Jr (1991) Depletion of U3 small nucleolar RNA inhibits cleavage in the 5′ external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J 10:4231–4239

    CAS  PubMed Central  PubMed  Google Scholar 

  59. Borovjagin AV, Gerbi SA (2000) The spacing between functional cis-elements of U3 snoRNA is critical for rRNA processing. J Mol Biol 300:57–74

    Article  CAS  PubMed  Google Scholar 

  60. Houseley J, LaCava J, Tollervey D (2006) RNA-quality control by the exosome. Nat Rev Mol Cell Biol 7:529–539

    Article  CAS  PubMed  Google Scholar 

  61. Houseley J, Tollervey D (2009) The many pathways of RNA degradation. Cell 136:763–776

    Article  CAS  PubMed  Google Scholar 

  62. Shiao YH, Lupascu ST, Gu YD, Kasprzak W, Hwang CJ, Fields JR, Leighty RM, Quiñones O, Shapiro BA, Alvord WG, Anderson LM (2009) An intergenic non-coding rRNA correlated with expression of the rRNA and frequency of an rRNA single nucleotide polymorphism in lung cancer cells. PLoS One 4:e7505

    Article  PubMed Central  PubMed  Google Scholar 

  63. Dundr M, Olson MO (1998) Partially processed pre-rRNA is preserved in association with processing components in nucleolus-derived foci during mitosis. Mol Biol Cell 9:2407–2422

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Zaphiropoulos PG (1997) Exon skipping and circular RNA formation in transcripts of the human cytochrome P-4502C18 gene in epidermis and rat androgen binding protein gene in testis. Mol Cell Biol 17:2985–2993

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Burd CE et al (2010) Expression of linear and novel circular forms of an INK4/ARF associated on-coding RNA correlates with atherosclerosis risk. PLoS Genet 6:e1001233

    Article  PubMed Central  PubMed  Google Scholar 

  66. Capel B et al (1993) Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 73:1019–1030

    Article  CAS  PubMed  Google Scholar 

  67. Nielsen H et al (2003) The ability to form full-length intron RNA circles is a general property of nuclear group I introns. RNA 9:1464–1475

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Environmental Sciences, Jawaharlal Nehru University, New Delhi, India

    Abhishek K. Gupta & Sudha Bhattacharya

Authors
  1. Abhishek K. Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sudha Bhattacharya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sudha Bhattacharya .

Editor information

Editors and Affiliations

  1. Department of Parasitology, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo, Japan

    Tomoyoshi Nozaki

  2. Jawaharlal Nehru University, New Delhi, India

    Alok Bhattacharya

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Japan

About this chapter

Cite this chapter

Gupta, A.K., Bhattacharya, S. (2015). Ribosomal RNA Genes and Their Regulation in Entamoeba histolytica . In: Nozaki, T., Bhattacharya, A. (eds) Amebiasis. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55200-0_8

Download citation

Publish with us

Policies and ethics

Search

Navigation