Papillomaviruses: a systematic review

Araldi, Rodrigo Pinheiro; Assaf, Suely Muro Reis; Carvalho, Rodrigo Franco de; Carvalho, Márcio Augusto Caldas Rocha de; Souza, Jacqueline Mazzuchelli de; Magnelli, Roberta Fiusa; Módolo, Diego Grando; Roperto, Franco Peppino; Stocco, Rita de Cassia; Beçak, Willy

doi:10.1590/1678-4685-GMB-2016-0128

Rodrigo Pinheiro Araldi

Laboratório de Genética, Instituto Butantan, São Paulo, SP, Brazil

Programa de Pós-graduação Interunidades em Biotecnologia, Instituto de Ciências Biomédicas (ICB), Universidade de São Paulo (USP), São Paulo, SP, Brazil

Suely Muro Reis Assaf

Laboratório de Genética, Instituto Butantan, São Paulo, SP, Brazil

Rodrigo Franco de Carvalho

Laboratório de Genética, Instituto Butantan, São Paulo, SP, Brazil

Márcio Augusto Caldas Rocha de Carvalho

Laboratório de Genética, Instituto Butantan, São Paulo, SP, Brazil

Programa de Aprimoramento Profissional (PAP), Instituto Butantan, São Paulo, SP, Brazil

Jacqueline Mazzuchelli de Souza

Laboratório de Genética, Instituto Butantan, São Paulo, SP, Brazil

Programa de Pós-graduação Interunidades em Biotecnologia, Instituto de Ciências Biomédicas (ICB), Universidade de São Paulo (USP), São Paulo, SP, Brazil

Roberta Fiusa Magnelli

Laboratório de Genética, Instituto Butantan, São Paulo, SP, Brazil

Programa de Pós-graduação Interunidades em Biotecnologia, Instituto de Ciências Biomédicas (ICB), Universidade de São Paulo (USP), São Paulo, SP, Brazil

Diego Grando Módolo

Laboratório de Genética, Instituto Butantan, São Paulo, SP, Brazil

Franco Peppino Roperto

Dipartimento di Medicina Veterinaria e Produzioni Animali, Università degli Studi di Napoli Federico II, Napoli, Campania, Italy

Rita de Cassia Stocco

Laboratório de Genética, Instituto Butantan, São Paulo, SP, Brazil

Willy Beçak Send correspondence to Willy Beçak. Laboratório de Genética, Instituto Butantan, Avenida Vital Brasil 1500, 00553900 São Paulo, SP, Brazil. E-mail: wbecak@yahoo.com.br

Laboratório de Genética, Instituto Butantan, São Paulo, SP, Brazil

Send correspondence to Willy Beçak. Laboratório de Genética, Instituto Butantan, Avenida Vital Brasil 1500, 00553900 São Paulo, SP, Brazil. E-mail: wbecak@yahoo.com.br

Figures (3)
Tables (1)

Thumbnail

Figure 1
BPV genome organization and differential protein expression: double strand DNA circular genome divided in early (E), late (L) and long codon region (LCR). Early region codifies replication proteins (E1, E2, E4, E5, E6 and E7). These proteins are expressed from basal to cornified layer, being involved with virus replication and virion release (E4). Late region codifies L1 and L2 capsid proteins. Once these structural proteins are involved with virus assembly, they are expressed in the most differenciated epithelium layers (granular and cornified).

Thumbnail

Figure 2
Adult bovine (Simmental breed) with bovine papillomatosis (BP): skin papillomas on face (A), dewlap (B) and back (C).

Thumbnail

Figure 3
Evidences of BPV presence in peripheral blood and cell culture showing: A) amplicon of BPV identified using specific primers for BPV-1, 2 and 4 (Araldi et al., 2013Araldi R, Melo T, Diniz N, Carvalho R, Beçak W and Stocco R (2013) Bovine papillomavirus clastogenic effect analyzed in comet assay. Biomed Res Int 2013:1-7.); B) BPV genome identification by chromogenic in situ hybridization (Melo et al., 2015Melo T, Araldi R, Pessoa N, De-Sá-Júnior P, Carvalho R, Beçak W and Stocco (2015) Bos taurus papillomavirus activity in peripheral blood mononuclear cells?: Demonstrating a productive infection. Genet Mol Res 14:16712-1627.); C) BPV virions identified in cytoplasmic vesicles of PBMCs (Melo et al., 2015Melo T, Araldi R, Pessoa N, De-Sá-Júnior P, Carvalho R, Beçak W and Stocco (2015) Bos taurus papillomavirus activity in peripheral blood mononuclear cells?: Demonstrating a productive infection. Genet Mol Res 14:16712-1627.); D) Immunodetection of BPV L1 and E2 in lymphocytes (Melo et al., 2015Melo T, Araldi R, Pessoa N, De-Sá-Júnior P, Carvalho R, Beçak W and Stocco (2015) Bos taurus papillomavirus activity in peripheral blood mononuclear cells?: Demonstrating a productive infection. Genet Mol Res 14:16712-1627.); E) cytogenetic aberrations (breaks) observed in BPV-infected lymphocyte (Stocco dos Santos et al., 1998Stocco dos Santos RC, Lindsey CJ, Ferraz OP, Pinto JR, Mirandola RS, Benesi FJ, Birgel EH, Pereira CA and Beçak W (1998) Bovine papillomavirus transmission and chromosomal aberrations: An experimental model. J Gen Virol 79:2127-2135.), F) class 2 nucleoids observed in BPV-infected lymphocytes (Araldi et al., 2013Araldi R, Melo T, Diniz N, Carvalho R, Beçak W and Stocco R (2013) Bovine papillomavirus clastogenic effect analyzed in comet assay. Biomed Res Int 2013:1-7.); G) BPV DNA sequences identified in cell culture, using FAP59/64 degenerate primers; H) Immunodetection of BPV early proteins (E1^E4, E2, E7) in both oesophageal and urinary bladder carcinoma cell line (Melo et al., data not published); I) BPV virion, with 55 nm, in cytoplasmic vesicle of cutaneous papilloma cell line, total magnification of 60000X (Melo et al., data not published); J) bovine epithelial cell line (CRIB) treated with E6 recombinant oncoprotein showing micronucleus presence (Araldi et al., 2015aAraldi R, Mazzuchelli-de-Souza J, Modolo D, Souza E, Melo T, Spadacci-Morena D, Magnelli R, Rocha M, De-Sá-Júnior P, Carvalho R, et al. (2015a) Mutagenic potential of Bos taurus papillomavirus type 1 E6 recombinant protein: First description. Biomed Res Int 2015:1-15.); K) cytogenetic aberration observed in BPV-infected cell line (Campos et al., 2013Campos S, Melo T, Assaf S, Araldi R, Mazzuchelli-de-Souza J, Sircili M, Carvalho R, Roperto F, Beçak W and Stocco R (2013) Chromosome aberrations in cells infected with bovine papillomavirus: Comparing cutaneous papilloma, esophagus papilloma, and urinary bladder lesion cells. ISRN Oncol 2013:910849.); L) class 2 nucleoids observed in cutaneous papilloma cell line (Araldi et al., data not published).

Thumbnail

Table 1
Papillomaviruses identified in different vertebrates

Figure 3 Evidences of BPV presence in peripheral blood and cell culture showing: A) amplicon of BPV identified using specific primers for BPV-1, 2 and 4 (**Araldi et al., 2013Araldi R, Melo T, Diniz N, Carvalho R, Beçak W and Stocco R (2013) Bovine papillomavirus clastogenic effect analyzed in comet assay. Biomed Res Int 2013:1-7.); B) BPV genome identification by chromogenic in situ hybridization (Melo et al., 2015Melo T, Araldi R, Pessoa N, De-Sá-Júnior P, Carvalho R, Beçak W and Stocco (2015) Bos taurus papillomavirus activity in peripheral blood mononuclear cells?: Demonstrating a productive infection. Genet Mol Res 14:16712-1627.); C) BPV virions identified in cytoplasmic vesicles of PBMCs (Melo et al., 2015Melo T, Araldi R, Pessoa N, De-Sá-Júnior P, Carvalho R, Beçak W and Stocco (2015) Bos taurus papillomavirus activity in peripheral blood mononuclear cells?: Demonstrating a productive infection. Genet Mol Res 14:16712-1627.); D) Immunodetection of BPV L1 and E2 in lymphocytes (Melo et al., 2015Melo T, Araldi R, Pessoa N, De-Sá-Júnior P, Carvalho R, Beçak W and Stocco (2015) Bos taurus papillomavirus activity in peripheral blood mononuclear cells?: Demonstrating a productive infection. Genet Mol Res 14:16712-1627.); E) cytogenetic aberrations (breaks) observed in BPV-infected lymphocyte (Stocco dos Santos et al., 1998Stocco dos Santos RC, Lindsey CJ, Ferraz OP, Pinto JR, Mirandola RS, Benesi FJ, Birgel EH, Pereira CA and Beçak W (1998) Bovine papillomavirus transmission and chromosomal aberrations: An experimental model. J Gen Virol 79:2127-2135.), F) class 2 nucleoids observed in BPV-infected lymphocytes (Araldi et al., 2013**Araldi R, Melo T, Diniz N, Carvalho R, Beçak W and Stocco R (2013) Bovine papillomavirus clastogenic effect analyzed in comet assay. Biomed Res Int 2013:1-7.); G) BPV DNA sequences identified in cell culture, using FAP59/64 degenerate primers; H) Immunodetection of BPV early proteins (E1^E4, E2, E7) in both oesophageal and urinary bladder carcinoma cell line (Melo et al., data not published); I) BPV virion, with 55 nm, in cytoplasmic vesicle of cutaneous papilloma cell line, total magnification of 60000X (Melo et al., data not published); J) bovine epithelial cell line (CRIB) treated with E6 recombinant oncoprotein showing micronucleus presence (**Araldi et al., 2015aAraldi R, Mazzuchelli-de-Souza J, Modolo D, Souza E, Melo T, Spadacci-Morena D, Magnelli R, Rocha M, De-Sá-Júnior P, Carvalho R, et al. (2015a) Mutagenic potential of Bos taurus papillomavirus type 1 E6 recombinant protein: First description. Biomed Res Int 2015:1-15.); K) cytogenetic aberration observed in BPV-infected cell line (Campos et al., 2013**Campos S, Melo T, Assaf S, Araldi R, Mazzuchelli-de-Souza J, Sircili M, Carvalho R, Roperto F, Beçak W and Stocco R (2013) Chromosome aberrations in cells infected with bovine papillomavirus: Comparing cutaneous papilloma, esophagus papilloma, and urinary bladder lesion cells. ISRN Oncol 2013:910849.); L) class 2 nucleoids observed in cutaneous papilloma cell line (Araldi et al., data not published).

Species	Virus	References
Bovines	Bos taurus papillomavirus or Bovine papillomavirus (BPV)	*Araldi et al.* (2015b)**Araldi R, Melo T, Neves A, Spadacci-Morena D, Magnelli R, Módulo D, De-Sá-Júnio P, Mazzuchelli-de-Souza J, Carvalho R, Beçak W, et al. (2015b) Hyperproliferative action of bovine papillomavirus (BPV): Genetics and histopathological aspects. Genet Mol Res 14:12942-12954.
		*Araldi et al.* (2014a)**Araldi R, Carvalho R, Melo T, Diniz N, Sant’Ana T, Mazzuchelli-de-Souza J, Spadacci-Morena D, Beçak W and Stocco R (2014a) Bovine papillomavirus in beef cattle: First description of BPV-12 and putative type BAPV8 in Brazil. Genet Mol Res 13:5644-5653.
		*Carvalho et al.* (2013)**Carvalho R, Sakata S, Giovanni D, Mori E, Brandão P, Richtzenhain L, Pozzi C, Arcaro J, Miranda M, Mazzuchelli-de-Souza J, et al. (2013) Bovine papillomavirus in Brazil: Detection of coinfection of unusual types by a PCR-RFLP method. Biomed Res Int 2013:270898.
		*Stocco dos Santos et al.* (1998)**Stocco dos Santos RC, Lindsey CJ, Ferraz OP, Pinto JR, Mirandola RS, Benesi FJ, Birgel EH, Pereira CA and Beçak W (1998) Bovine papillomavirus transmission and chromosomal aberrations: An experimental model. J Gen Virol 79:2127-2135.
Canines	Canine oral papillomavirus (COPV) or Cannis familiaris papillomavirus (CfPV)	*Nicholls et al.* (2001)**Nicholls PK, Moore PF, Anderson DM, Moore RA, Parry NR, Gough GW and Stanley MA (2001). Regression of canine papillomas is associated with infiltration of CD4+ and CD8+ lymphocytes. Virology 283:31-39.
		*Zaugg et al.* (2005)**Zaugg N, Nespeca G, Hauser B, Ackermann M and Favrot C (2005) Detection of novel papillomaviruses in canine mucosal, cutaneous and in situ squamous cell carcinomas. Vet Dermatol 16:290-298.
Deer	Capreolus capreolus papillomavirus (CcPV) or Cervus elaphus papillomavirus (CePV)	*Kràl et al.* (2015)**Kràl J, Band'ouchová H, Brichta J, Kovácová V, Ondracék K, Osicková J, Hrubá H, Hutarová Z, Komínkova M, Cernei N, et al. (2015) Papillomavirus infection of roe deer in the Czech Republic and fibropapilloma-associated levels of metallothionein, zinc and oxidative stress. Acta Vet Brno 84:105-111.
Felines	Felis catus papillomavirus (FcaPV)	Munday (2014)Munday J (2014) Bovine and human papillomaviruses: A comparative review. Vet Pathol 51:1063-1075.
Rabbit	Cotton rabbit papillomavirus (CRPV)	Shope and Hurst (1933)Shope R and Hurst E (1933) Infectious papillomatosis of rabbits. J Exp Med 58:607-624.
		*Danos et al.* (1985)**Danos O, Georges E, Orth G and Yaniv M (1985) Fine structure of the cottontail rabbit papillomavirus mRNAs expressed in the transplantable VX2 carcinoma. J Virol 53:735-741.
		Rashad and Evans (1967)Rashad AL and Evans CA (1967) Histologic features of virus-rich and virus-poor Shope papillomas of cottontail rabbits. Cancer Res 27:1855-1860.
Raccoon	Procyon loto papillomavirus (PlPV)	*Ng et al.* (2015)**Ng T, Miller M, Kondov N, Dodd E, Batac F, Manzer M, Ives S, Saliki J, Deng X and Delwart E (2015) Oral papillomatosis caused by Enhydra lutris papillomavirus 1 (ElPV-1) in southern sea otters (Enhydra lutris nereis) in California, USA. J Wildl Dis 51:446-453.
Seaotter	Enhydralutris papillomavirus (ElPV)	*Ng et al.* (2015)**Ng T, Miller M, Kondov N, Dodd E, Batac F, Manzer M, Ives S, Saliki J, Deng X and Delwart E (2015) Oral papillomatosis caused by Enhydra lutris papillomavirus 1 (ElPV-1) in southern sea otters (Enhydra lutris nereis) in California, USA. J Wildl Dis 51:446-453.
Sheep	Ovis aries papillomavirus (OaPV)	*Alberti et al.* (2010)**Alberti A, Pirino S, Pintore F, Addis MF, Chessa B, Cacciotto C, Cubeddu T, Anfossi A, Benenati G, Coradduzza E, et al. (2010) Ovis aries Papillomavirus 3: A prototype of a novel genus in the family Papillomaviridae associated with ovine squamous cell carcinoma. Virology 407:352-359.
Mice	Mus musculus papillomavirus (MmPV)	*Handisurya et al.* (2013)**Handisurya A, Day P, Thompson C, Buck C, Pang Y, Lowy D and Schiller J (2013) Characterization of Mus musculus papillomavirus 1 infection in situ reveals an unusual pattern of late gene expression and capsid protein localization. J Virol 87:13214-25.
Birds	Fulmarus glaciallis papillomavirus (FgPV)	*Gaynor et al.* (2015a)**Gaynor A, Fish S, Duerr R, Cruz F and Pesavento P (2015a) Identification of a novel papillomavirus in a Northern Fulmar (Fulmarus glacialis) with viral production in cartilage. Vet Pathol 52:553-561.
	Francolinusleucoscepuspapillomavirus (FlPV)	*Moreno-Lopez et al.* (1984)**Moreno-Lopez J, Ahola H, Stenlund A, Osterhaus A and Pettersson U (1984) Genome of an avian papillomavirus. J Virol 51:872-875.
	Fringillacoelebspapillomavirus (FcPV)	*Van Bressem et al.* (2007)**Van Bressem M, Cassonnet P, Rector A, Desaintes C, Van Waerebeek K, Alfaro-Shigueto J, Van Ranst M and Orth G (2007) Genital warts in Burmeister's porpoises: Characterization of Phocoena spinipinnis papillomavirus type 1 (PsPV-1) and evidence for a second, distantly related PsPV. J Gen Virol 88:1928-1233.
	Psittacuserithacuspapillomavirus (PePV)
Rat	Rattus norvegicus papillomavirus (RnPV)	*Hansen et al.* (2015)**Hansen T, Fridholm H, Frøslev T, Kjartansdóttir K, Willerslev E, Nielsen L and Hansen A (2015) New type of papillomavirus and novel circular single stranded DNA virus discovered in urban Rattus norvegicus using circular DNA enrichment and metagenomics. PLoS One 10:e0141952.
Monkey	Rhesus macaca papillomavirus(RmPV)	Roberts (2015)Roberts S (2015) Papillomaviruses. eLS 2015:1-11.
Human	Human papillomavirus (HPV)	zur Hausen (2009)zur Hausen H (2009) The search for infectious causes of human cancers: Where and why. Virology 392:1-10.
		*Herbster et al.* (2012)**Herbster S, Ferraro C, Koff N, Rossini A, Kruel C, Andreollo N, Rapozo D, Blanco T, Faria P, Santos P, et al. (2012) HPV infection in Brazilian patients with esophageal squamous cell carcinoma: Interpopulational differences, lack of correlation with surrogate markers and clinicopathological parameters. Cancer Lett 326:52-58.

[1] Send correspondence to Willy Beçak. Laboratório de Genética, Instituto Butantan, Avenida Vital Brasil 1500, 00553900 São Paulo, SP, Brazil. E-mail: wbecak@yahoo.com.br

Brasil

Brasil

Papillomaviruses: a systematic review

Abstract