Analysis of the β‐Tubulin Genes from Enterocytozoon bieneusi Isolates from a Human and Rhesus Macaque

ABSTRACT. Enterocytozoon bieneusi is the most common and clinically significant microsporidium associated with chronic diarrhea and wasting in immunocompromised humans. Albendazole, which is effective against several helminths, protozoa, and microsporidia, is relatively ineffective against infections due to E. bieneusi. A likely explanation for the observed clinical resistance to albendazole was discovered from sequence analysis of the E. bieneusiβ‐tubulin from isolates from an infected human and a naturally infected rhesus macaque. The β‐tubulin of E. bieneusi has a substitution at Glu198, which is one of six amino acids reported to be associated with benzimidazole sensitivity.

[1]  S. Tzipori,et al.  Production and Characterization of Monoclonal Antibodies against Enterocytozoon bieneusi Purified from Rhesus Macaques , 2005, Infection and Immunity.

[2]  A. Mathis,et al.  Zoonotic Potential of the Microsporidia , 2005, Clinical Microbiology Reviews.

[3]  S. Tzipori,et al.  Purification of Enterocytozoon bieneusi from Stools and Production of Specific Antibodies , 2005, Journal of Clinical Microbiology.

[4]  P. Brindley,et al.  Epidemiology of microsporidiosis: sources and modes of transmission. , 2004, Veterinary parasitology.

[5]  E. Didier,et al.  Natural and experimental infection of immunocompromised rhesus macaques (Macaca mulatta) with the microsporidian Enterocytozoon bieneusi genotype D. , 2004, Microbes and infection.

[6]  Thomas L. Madden,et al.  BLAST: at the core of a powerful and diverse set of sequence analysis tools , 2004, Nucleic Acids Res..

[7]  M F Lawrence,et al.  Impedance-based detection of DNA sequences using a silicon transducer with PNA as the probe layer. , 2004, Nucleic acids research.

[8]  R. Fayer,et al.  Molecular characterization of Enterocytozoon bieneusi in cattle indicates that only some isolates have zoonotic potential , 2004, Parasitology Research.

[9]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[10]  Fabienne Thomarat,et al.  Functional and evolutionary analysis of a eukaryotic parasitic genome. , 2002, Current opinion in microbiology.

[11]  Martin Vingron,et al.  TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing , 2002, Bioinform..

[12]  P. Keeling,et al.  Microsporidia: biology and evolution of highly reduced intracellular parasites. , 2002, Annual review of microbiology.

[13]  Fabienne Thomarat,et al.  Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi , 2001, Nature.

[14]  J. Ballet,et al.  Metronidazole and albendazole susceptibility of 11 clinical isolates of Giardia duodenalis from France. , 2000, The Journal of antimicrobial chemotherapy.

[15]  O. Berlin,et al.  Therapy for human gastrointestinal microsporidiosis. , 2000, The American journal of tropical medicine and hygiene.

[16]  M. Rabodonirina,et al.  Intestinal microsporidiosis occurring in two renal transplant recipients treated with mycophenolate mofetil. , 1999, Transplantation.

[17]  L. Weiss,et al.  The Microsporidia and Microsporidiosis , 1999 .

[18]  M. Drancourt,et al.  In Vitro Susceptibilities of the MicrosporidiaEncephalitozoon cuniculi, Encephalitozoon hellem, and Encephalitozoon intestinalis to Albendazole and Its Sulfoxide and Sulfone Metabolites , 1998, Antimicrobial Agents and Chemotherapy.

[19]  S. Fenoy,et al.  Detection of Enterocytozoon bieneusi in two human immunodeficiency virus-negative patients with chronic diarrhea by polymerase chain reaction in duodenal biopsy specimens and review. , 1998, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[20]  C. Chastang,et al.  Albendazole for treatment and prophylaxis of microsporidiosis due to Encephalitozoon intestinalis in patients with AIDS: a randomized double-blind controlled trial. , 1998, The Journal of infectious diseases.

[21]  S. Katiyar,et al.  In vitro susceptibilities of the AIDS-associated microsporidian Encephalitozoon intestinalis to albendazole, its sulfoxide metabolite, and 12 additional benzimidazole derivatives , 1997, Antimicrobial agents and chemotherapy.

[22]  H. Albrecht,et al.  Enterocytozoon bieneusi infection in patients who are not infected with human immunodeficiency virus. , 1997, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[23]  H. Philippe,et al.  Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. , 1997, Molecular and biochemical parasitology.

[24]  S. Tzipori,et al.  Identification of an Enterocytozoon bieneusi-like microsporidian parasite in simian-immunodeficiency-virus-inoculated macaques with hepatobiliary disease. , 1997, The American journal of pathology.

[25]  W. Doolittle,et al.  Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. , 1996, Molecular biology and evolution.

[26]  M. Rabodonirina,et al.  Enterocytozoon bieneusi as a cause of chronic diarrhea in a heart-lung transplant recipient who was seronegative for human immunodeficiency virus. , 1996, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[27]  S. Katiyar,et al.  Tubulin genes from AIDS-associated microsporidia and implications for phylogeny and benzimidazole sensitivity. , 1996, Molecular and biochemical parasitology.

[28]  S. Katiyar,et al.  Phylogenetic Analysis of β-Tubulin Sequences from Amitochondrial Protozoa , 1996 .

[29]  Michael L Wilson,et al.  Polymerase chain reaction and culture confirmation of disseminated Encephalitozoon cuniculi in a patient with AIDS: successful therapy with albendazole. , 1995, The Journal of infectious diseases.

[30]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[31]  B. Ruf,et al.  Enterocytozoon bieneusi infection in an immunocompetent patient who had acute diarrhea and who was not infected with the human immunodeficiency virus. , 1994, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[32]  S. Katiyar,et al.  Antiprotozoal activities of benzimidazoles and correlations with beta-tubulin sequence , 1994, Antimicrobial Agents and Chemotherapy.

[33]  T. Edlind,et al.  In vitro susceptibility of the opportunistic fungus Cryptococcus neoformans to anthelmintic benzimidazoles , 1994, Antimicrobial Agents and Chemotherapy.

[34]  M. Kwa,et al.  Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in β-tubulin isotype 1 , 1994 .

[35]  D. Dieterich,et al.  Treatment with albendazole for intestinal disease due to Enterocytozoon bieneusi in patients with AIDS. , 1994, The Journal of infectious diseases.

[36]  E. Canning,et al.  Human microsporidiosis. , 1993, The Journal of infection.

[37]  B. Gazzard,et al.  Treatment of intestinal microsporidiosis with albendazole in patients with AIDS , 1992, AIDS.

[38]  B. Oakley,et al.  Amino acid alterations in the benA (beta-tubulin) gene of Aspergillus nidulans that confer benomyl resistance. , 1992, Cell motility and the cytoskeleton.

[39]  A. Cali General microsporidian features and recent findings on AIDS isolates. , 1991, The Journal of protozoology.

[40]  A. Cali,et al.  Ultrastructural Study of the Development of Pleistophora schubergi Zwölfer, 1927 (Protozoa, Microsporida) in Larvae of the Spruce Budworm, Choristoneura fumiferana and Its Subsequent Taxonomic Change to the Genus Endoreticulatus , 1991 .

[41]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[42]  I. Muscat Human microsporidiosis. , 1990, The Journal of infection.

[43]  E. Lacey The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug resistance to benzimidazoles. , 1988, International journal for parasitology.

[44]  M. Turner,et al.  Cloning and sequence of β tubulin cDNA from Giardia lamblia , 1988 .

[45]  L. C. Davidse,et al.  Benzimidazole Fungicides: Mechanism of Action and Biological Impact , 1986 .

[46]  C. Yanofsky,et al.  Cloning and characterization of the gene for beta-tubulin from a benomyl-resistant mutant of Neurospora crassa and its use as a dominant selectable marker , 1986, Molecular and cellular biology.

[47]  D. Botstein,et al.  Isolation and Characterization of Mutations in the β-Tubulin Gene of SACCHAROMYCES CEREVISIAE , 1985 .