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Journal of Clinical Microbiology, February 2007, p. 577-580, Vol. 45, No. 2
0095-1137/07/$08.00+0     doi:10.1128/JCM.02262-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Identification of Group A Porcine Rotavirus Strains Bearing a Novel VP4 (P) Genotype in Italian Swine Herds{triangledown}

V. Martella,1* M. Ciarlet,2 K. Bányai,3 E. Lorusso,1 S. Arista,4 A. Lavazza,5 G. Pezzotti,6 N. Decaro,1 A. Cavalli,1 M. S. Lucente,1 M. Corrente,1 G. Elia,1 M. Camero,1 M. Tempesta,1 and C. Buonavoglia1

Department of Animal Health and Well-Being, University of Bari, Valenzano, Bari, Italy,1 Biologics—Clinical Research, Merck and Co., Inc., Blue Bell, Pennsylvania,2 Regional Laboratory of Virology, Baranya County Institute, State Public Health Service, Pécs, Hungary,3 Department of Hygiene and Microbiology, University of Palermo, Palermo, Italy,4 Istituto Zooprofilattico Sperimentale di Lombardia/Emilia Romagna, Brescia, Italy,5 Istituto Zooprofilattico Sperimentale di Umbria/Marche, Perugia, Italy6

Received 6 November 2006/ Accepted 13 November 2006


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ABSTRACT
 
The VP4 gene of a G5 Italian porcine rotavirus strain, 344/04-1, was nontypeable by PCR genotyping. The amino acid sequence of the full-length VP4 protein had low identity (≤76.6%) with the homologous sequences of representative strains of the remaining P genotypes, providing evidence for a novel P genotype.


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TEXT
 
Group A rotaviruses are classified in the genus Rotavirus, of the family Reoviridae. The double-stranded RNA genome is composed of 11 segments enclosed in a nonenveloped, triple-layered icosahedral capsid protein (14). The two outer capsid proteins, VP4 and VP7, independently elicit neutralizing antibodies, induce protective immunity, and are used to classify rotavirus strains into P (for protease-sensitive) and G (for glycoprotein) serotypes (14).

Fifteen G genotypes (defined by sequence analysis and/or nucleic acid hybridization data) have been identified and shown to belong to distinct G serotypes (defined by serology data) (6). Out of 26 different P genotypes (designated in brackets), only 15 P serotypes (P1A, P1B, and P2 to P14) have been identified with available antisera or anti-VP4 monoclonal antibodies (21, 24, 26, 28, 30, 34, 35, 38, 39). Rotavirus strains within a G serotype have at least 90 to 91% VP7 amino acid sequence identity (6). Rotavirus strains having >89% VP4 amino acid sequence identities belong to the same P genotype (17). The greatest amino acid divergence in VP4 is seen between amino acids (aa) 71 and 204 of the VP4 trypsin cleavage product VP8*, which tends to correlate with VP4 genotype specificity (25, 26).

Among porcine rotaviruses (PoRVs), 10 G types (G1, G2-like, G3 to G6, and G9 to G12) have been described (7, 8, 9, 11, 15, 31, 32). The most common PoRV G serotypes are G3, G4, and G5, which are usually associated with VP4 serotypes P9[7] or P2B[6]. Additional P types (P7[5], P1A[8], P[13], P12[19], P14[23], and P[26]) in PoRV strains isolated from or detected in porcine stool samples have been described (4, 22, 28, 29, 31, 33, 34, 40, 41, 44).

During a large surveillance study to monitor rotavirus diversity and the occurrence of unusual strains in Italy, a total of 751 fecal samples were collected from nursing and weaning pigs involved in outbreaks of diarrhea at 74 farms in five regions of Italy between 2003 and 2004. A total of 124 (16.1%) rotavirus-positive samples were identified by electron microscopy or by a commercial immunoenzyme assay. Upon either PCR genotyping or sequencing, the PoRVs displayed a broad spectrum of VP7 and VP4 types, including G2-like, G3, G4, G5, G6, G9, P[6], P[7], P[13], P[23], and P[26] (32, 33, 34).

Because the VP4 genotype of one PoRV strain, 344/04-1, identified from a diarrheic piglet on a farm in Perugia (Umbria), was nontypeable with our multiple panels of P-type-specific primers, the sequence of the VP4 full-length gene was determined with a 5' consensus primer (33). In addition, the VP6, VP7, and NSP4 genes were analyzed. The VP7 gene was amplified with primers Beg9 and End9 (18). The VP6 genogroup, predictive of VP6 subgroup specificity, was determined by amplification of a 379-bp fragment spanning aa 241 to 367 of VP6 with primer pair VP6F-VP6R (23). The nearly full-length gene of NSP4 was amplified with primer pair 10Beg16-10End722 (27).

Comparative amino acid sequence analysis of the VP6 fragment of strain 344/04-1 showed that it was closely related to genogroup I PoRV strains characterized as subgroup I. The porcine origin of strain 344/04-1 was also evident when the full-length NSP4 protein was compared with representative strains of NSP4 genogroups A, B, C, D, and E (10, 36). NSP4 of PoRV strain 344/04-1 showed the highest amino acid identity (100%) to PoRV strains within the NSP4 B (Wa-like) genotype. Upon sequencing of the VP7 gene, PoRV strain 344/04-1 was identified as genotype G5, as the highest degree of amino acid identity (93.5 to 97.5%) was found with serotype G5 PoRV strains.

The basic structure of the VP4 gene of strain 344/04-1 was very similar to those of other rotavirus strains in that it consisted of 2,350 bp with one open reading frame, beginning at nucleotide 10, and a single TAA stop codon at nucleotide 2328. The predicted size of the porcine VP4 protein was 772 aa, unlike those of most rotavirus strains, which are 775 or 776 aa in length (14). A deletion of 3 aa within the variable region (aa 578 to 608) of VP5* was observed, a feature present only in VP4 genotypes P[11] and P[17] (14, 20). The deduced amino acid sequence of VP4 of PoRV strain 344/04-1 was compared with those of representative rotavirus strains belonging to known P genotypes. The prolines at residues 68, 71, 225, 226, 334, 390, 395, 435, 451, 455, 475, 524 669, 716, 749, and 761 and the cysteines at positions 216, 318, 380, and 774, which are highly conserved among other P genotypes, were maintained in the VP4 protein of strain 344/04-1, while the proline at residue 395 was replaced by glutamine. The potential trypsin cleavage sites Arg-231, Arg-241, and Arg-247 were conserved (2), and the additional cleavage sites identified in VP5*, Lys-259 and, putatively, Arg-467 (13), were also conserved, while Arg-583 was replaced by Lys.

The amino acid sequence of the full-length VP4 protein of PoRV strain 344/04-1 showed amino acid identity values ranging from 57.9% (bovine strain KK3, P8[11]) to 76.6% (simian strain TUCH, P[24]) compared to those of strains representative of all 26 P genotypes (Table 1). Since it has been established that rotavirus strains that exhibit a VP4 amino acid identity of approximately >89% belong to the same P genotype (17), our results indicate that the Italian PoRV strain 344/04-1 represents a novel P genotype, tentatively called P[27]. In the phylogenetic tree (Fig. 1), the VP4 protein of the Italian PoRV strain 344/04-1 was placed on a clearly distinct branch.


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  		TABLE 1. Comparison of the amino acid sequences of VP8* (aa 1 to 247) and VP4 of porcine strain 344/04-1 with those of well-established P-genotype strains


Figure 1
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  		FIG. 1. Phylogenetic tree of VP4 of group A rotavirus displaying the relationships between porcine strain 344/04-1 and strains representative of the 26 P genotypes recognized to date. The tree is drawn to scale. The GenBank accession numbers of the VP4 sequences are listed in Table 1, footnote b. Abbreviations: Si, simian; Eq, equine; Po, porcine; Ca, canine; Bo, bovine; Mu, murine; Hu, human; Go, goat; Ov, ovine; La, lapine.

Based on the VP8* nucleotide sequence alignment of rotavirus strains representative of several P genotypes, a primer (MV27, 5'-TAC TTC TAT TTG CTC TTG TTT C-3') specific for strain 344/04-1 was designed and used to screen rotavirus-positive samples that were nontypeable by PCR genotyping. Four diarrheic stool samples, out of 35 nontypeable samples, were recognized by primer MV27. The four stool samples were collected from a single swine herd in the Brescia province (Lombardia), in northern Italy. Sequence analysis of the VP8* gene of two such samples revealed the highest identity (79% nucleotide identity and 85.6% amino acid identity) to PoRV strain 344/04-1.

Along with cattle, pigs are regarded as important reservoirs for human rotavirus diversification, and there is evidence that heterologous rotaviruses of porcine origin or natural porcine-human reassortants may have occurred and spread successfully throughout human populations on multiple occasions in Latin America, Southeast Asia, and Europe (1, 3, 5, 12, 16, 19, 24, 33, 37, 42, 43). The detection of a new rotavirus VP4 type extends our knowledge of the genetic/antigenic diversity of group A rotaviruses and highlights the need to attempt to type "nontypeable" rotavirus-positive samples. A better understanding of rotavirus epidemiology will contribute to the optimization of current vaccines and prevention programs for rotavirus diarrhea of humans and animals and will aid the understanding of the global ecology of rotaviruses.

Nucleotide sequence accession numbers. GenBank accession numbers DQ242615, DQ813658, and DQ823416 have been assigned to the sequences of the VP4, VP7, and NSP4 genes, respectively.


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ACKNOWLEDGMENTS
 
This work was supported by grants from Ministero della Sanità (Ministry of Health) Progetto Finalizzato 2003; from "Il ruolo del suino quale serbatoio e vettore di zoonosi: valutazione del rischio e proposte per nuove strategie," Ministero dell'Istruzione, dell'Università e della Ricerca (Ministry of Education, University and Research) (Fondi di Ateneo ex 60%); and from the project Molecular and Antigenic Evolution of Rotavirus Strains of Human and Animal Origin (ISS-NIH 2004). K.B. is a recipient of the Bolyai János Fellowship of the Hungarian Academy of Sciences.

We thank Filomena Cariola, Caterina Nanna, Nicoletta Tutino, and Donato Narcisi for expert technical assistance. We are extremely grateful to Leland Eugene Carmichael for continued encouragement throughout our studies.


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FOOTNOTES
 
* Corresponding author. Mailing address: Dipartimento di Sanità e Benessere Animale, Facoltà di Medicina Veterinaria di Bari, S.p. per Casamassima km 3, 70010 Valenzano, Bari, Italia. Phone: 39 080 4679805. Fax: 39 080 4679843. E-mail: v.martella{at}veterinaria.uniba.it. Back

{triangledown} Published ahead of print on 22 November 2006. Back


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Journal of Clinical Microbiology, February 2007, p. 577-580, Vol. 45, No. 2
0095-1137/07/$08.00+0     doi:10.1128/JCM.02262-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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  • Santos, N., Honma, S., Timenetsky, M. d. C. S. T., Linhares, A. C., Ushijima, H., Armah, G. E., Gentsch, J. R., Hoshino, Y. (2008). Development of a Microtiter Plate Hybridization-Based PCR-Enzyme-Linked Immunosorbent Assay for Identification of Clinically Relevant Human Group A Rotavirus G and P Genotypes. J. Clin. Microbiol. 46: 462-469 [Abstract] [Full Text]  
  • Honma, S., Chizhikov, V., Santos, N., Tatsumi, M., do Carmo S. T. Timenetsky, M., Linhares, A. C., Mascarenhas, J. D. P., Ushijima, H., Armah, G. E., Gentsch, J. R., Hoshino, Y. (2007). Development and Validation of DNA Microarray for Genotyping Group A Rotavirus VP4 (P[4], P[6], P[8], P[9], and P[14]) and VP7 (G1 to G6, G8 to G10, and G12) Genes. J. Clin. Microbiol. 45: 2641-2648 [Abstract] [Full Text]  
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