Reassortment of Human Rotavirus Gene Segments into G11 Rotavirus Strains

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Volume 16, Number 4–April 2010
Research
Reassortment of Human Rotavirus Gene Segments into G11 Rotavirus Strains
Jelle Matthijnssens, Mustafizur Rahman, Max Ciarlet, Mark Zeller, Elisabeth Heylen, Toyoko Nakagomi, Ryuichi Uchida,1 Zahid Hassan, Tasnim Azim, Osamu Nakagomi, and Marc Van Ranst
Author affiliations: Rega Institute for Medical Research, Leuven, Belgium (J. Matthijnssens, M. Zeller, E. Heylen, M. Van Ranst); International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh (M. Rahman, Z. Hassan, T. Azim); Merck and Company, Inc., North Wales, Pennsylvania, USA (M. Ciarlet); and Nagasaki University, Nagasaki, Japan (T. Nakagomi, R. Uchida, O. Nakagomi)

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Abstract
G11 rotaviruses are believed to be of porcine origin. However, a limited number of G11 rotaviruses have been recently isolated from humans in combination with P[25], P[8], P[6], and P[4]. To investigate the evolutionary relationships of these strains, we analyzed the complete genomes of 2 human G11P[25] strains, 2 human G11P[8] strains, and 3 porcine reference strains. Most of the 11 gene segments of these 7 strains belonged to genotype 1 (Wa-like). However, phylogenetic clustering patterns suggested that an unknown G11P[25] strain with a new I12 VP6 genotype was transmitted to the human population, in which it acquired human genotype 1 gene segments through reassortment, resulting in a human G11P[8] rotavirus strain with an entire human Wa-genogroup backbone. This Wa-like backbone is believed to have caused the worldwide spread of human G9 and G12 rotaviruses. G11 human rotavirus strains should be monitored because they may also become major human pathogens.

Group A rotaviruses are the most frequently detected viral cause of diarrhea in children worldwide and cause ≈600,000 deaths in children <5 years of age annually, mainly in developing countries (1). Rotaviruses have a genome composed of 11 segments of double-stranded RNA that encodes 6 structural (VP) and 5 or 6 nonstructural (NSP) proteins (2). The 2 outer capsid proteins VP7 and VP4 are the basis for a widely used dual classification system defining G-types and P-types, respectively. Currently 23 G-genotypes and 31 P-genotypes have been described, of which 12 of each type have been found in human rotavirus isolates (3–9). However, only a limited number of G/P-genotype combinations are found frequently in humans, such as G1P[8], G2P[4], G3P[8], G4P[8], and G9P[8], and, more recently, the G12 genotype in combination with P[8] or P[6] (10). It has been hypothesized that the G9 and G12 genotypes have been able to successfully infect, spread, and persist in humans because of reassortment events with human Wa-like rotavirus strains, which has resulted in the G9 and G12 rotaviruses combining with P[8] and the 9 remaining gene segments belonging to genotype 1 (10).

A nucleotide sequence–based classification and nomenclature system encompassing the 11 rotavirus genome segments has been introduced recently, and it defines genotypes for each of the 11 gene segments (11). This system has been useful in investigating reassortment events and interspecies transmission of rotaviruses and their interhost relationships (5,12–20). In this system, the VP1–VP3, VP6, and NSP1–NSP5 genotypes comprising Wa-like strains have been designated as genotype 1 (R1, C1, M1, I1, A1, N1, T1, E1, and H1, respectively), and DS-1 and AU-1-like strains have been designated as genotypes 2 and 3, respectively (11). A Rotavirus Classification Working Group (RCWG) was formed to maintain and update this system and to assign successive genotype numbers to newly discovered rotavirus genotypes (21).

G11 rotaviruses are believed to be circulating in pigs, albeit in low numbers. Only 2 G11P[7] porcine strains have been isolated, strain YM in Mexico in 1983 and strain A253 in Venezuela in 1989 (22,23). Each of these porcine strains was identified as a single isolate in large strain collections obtained during epidemiologic surveys. In subsequent years, no additional G11 strains were detected in the same or nearby pig farms. However, more than a decade after the detection of these 2 porcine G11 strains, several reports have described the isolation of G11 rotavirus strains from humans. Three G11 rotaviruses, Dhaka6, KTM368, and CRI 10795, have been found in combination with the rare human genotype P[25] in India (24), Bangladesh (25), and Nepal (26). Furthermore, G11 human rotaviruses have been found in combination with P[8] (Matlab36–02 and Matlab22–01), with P[6] in Ecuador (EC2184) (27) and Bangladesh (Dhaka13–06) (28) and with P[4] (CUK-1) in South Korea (29).

It was recently suggested that human rotavirus strains belonging to the Wa-like genogroup and porcine rotaviruses have a common origin (11). This report prompted us to investigate the level of genetic relatedness, and possibly evolutionary origins, between these unusual human G11 rotavirus strains and porcine rotavirus strains by complete genome analyses of 2 human G11P[25] strains (KTM368 and Dhaka6), 2 human G11P[8] strains (Matlab36–02 and Dhaka22–01), and 3 cell culture–adapted porcine strains YM (G11P[7]), Gottfried (G4P[6]), and OSU (G5P[7]).

Suggested Citation for this Article
Matthijnssens J, Rahman M, Ciarlet M, Zeller M, Heylen E, Nakagomi T, et al. Reassortment of G11 rotavirus strains in humans. Emerg Infect Dis [serial on the Internet]. 2010 Apr [date cited]. http://www.cdc.gov/EID/content/16/4/625.htm

DOI: 10.3201/eid1604.091591

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