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Article

Comparative Fluorescence In Situ Hybridization (FISH) Mapping of Twenty-Three Endogenous Jaagsiekte Sheep Retrovirus (enJSRVs) in Sheep (Ovis aries) and River Buffalo (Bubalus bubalis) Chromosomes

by
Angela Perucatti
1,
Alessandra Iannuzzi
1,*,
Alessia Armezzani
2,
Massimo Palmarini
2 and
Leopoldo Iannuzzi
1
1
National Research Council (CNR), Institute of Animal Production System on Mediterranean Environment (ISPAAM), Piazzale E. Fermi, 1, 80055 Portici, Italy
2
MRC-University of Glasgow Centre for Virus Research, 464 Bearsden Road, Glasgow G61-1QH, UK
*
Author to whom correspondence should be addressed.
Animals 2022, 12(20), 2834; https://doi.org/10.3390/ani12202834
Submission received: 27 August 2022 / Revised: 14 October 2022 / Accepted: 17 October 2022 / Published: 19 October 2022
(This article belongs to the Special Issue Cytogenetics of Domestic Animals: Clinical, Molecular and Evolutionary Aspects)
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Abstract

:

Simple Summary

The genome of domestic sheep (Ovis aries) harbors at least twenty-seven copies of enJSRVs, endogenous retroviruses (ERVs) highly related to the exogenous and pathogenic Jaagsiekte sheep betaretrovirus (JSRV). Interestingly, some of these loci are insertionally polymorphic, that is they are present only in some individuals or populations of their host species. This differential distribution of enJSRVs has provided important insights into tracing host and viral evolution. In this study, we report the first comparative fluorescent in situ hybridization (FISH) mapping of genetically characterized enJSRVs in domestic sheep (2n = 54) and river buffalo (Bubalus bubalis, 2n = 50), and reveal a high conservation of enJSRVs chromosome localization between these two species.

Abstract

Endogenous retroviruses (ERVs) are the remnants of ancient infections of host germline cells, thus representing key tools to study host and viral evolution. Homologous ERV sequences often map at the same genomic locus of different species, indicating that retroviral integration occurred in the genomes of the common ancestors of those species. The genome of domestic sheep (Ovis aries) harbors at least twenty-seven copies of ERVs related to the exogenous and pathogenic Jaagsiekte sheep retrovirus (JSRVs), thus referred to as enJSRVs. Some of these loci are unequally distributed between breeds and individuals of the host species due to polymorphic insertions, thereby representing invaluable tools to trace the evolutionary dynamics of virus populations within their hosts. In this study, we extend the cytogenetic physical maps of sheep and river buffalo by performing fluorescent in situ hybridization (FISH) mapping of twenty-three genetically characterized enJSRVs. Additionally, we report the first comparative FISH mapping of enJSRVs in domestic sheep (2n = 54) and river buffalo (Bubalus bubalis, 2n = 50). Finally, we demonstrate that enJSRV loci are conserved in the homologous chromosomes and chromosome bands of both species. Altogether, our results support the hypothesis that enJSRVs were present in the genomes of both species before they differentiated within the Bovidae family.

1. Introduction

Retroviruses possess the unique ability to integrate into the genome of infected cells. Occasionally, they can infect germline cells and give rise to endogenous retroviruses (ERVs), retroviral sequences transmitted vertically, in a Mendelian fashion, as part of the host genome. As such, ERVs represent fascinating tools to study both virus and host genome evolution [1]. ERVs have been found in all vertebrates studied to date, including fish, amphibians, birds, reptiles, and mammals [2]. Comparative genomic studies have shown that related species often share ERV families or specific ERV loci, and that, in many cases, homologous ERV sequences map at the same genomic locus in multiple species’ genomes, indicating that retroviral integration events occurred in the genomes of the common ancestors of those species [3,4].
In 2013, Garcia-Etxebarria and Jugo traced the evolutionary history of bovine ERVs (BoERVs) by performing computational analyses on the genomes of several bovid species, including cattle, sheep, goat, and water buffalo [5]. Interestingly, they found twenty-six BoERV families in all the species studied, suggesting that most of these families could be present in all members of the Bovidae family. However, they could not detect four BoERV families (i.e., BoERV24, BoERV26, BoERV28, and BoERV29) in sheep or goat genomes, indicating that these families may be specific to the Bovinae subfamily. The authors hypothesize that the majority of the BoERV families invaded the genome of the common ancestor of the Bovidae family approximately 20 million years ago (MYA) and only later, between 12MYA and 20MYA, the ancestors of the BoERV24, BoERV26, BoERV28, and BoERV29 families might have been inserted into the genome of the Bovinae subfamily ancestor [5].
The domestic sheep (Ovis aries) harbors at least twenty-seven ERV loci related to the exogenous and pathogenic Jaagsiekte sheep retrovirus (JSRV), thus referred to as enJSRVs [6,7]. Interestingly, some enJSRV loci are insertionally polymorphic, that is they are present only in some individuals or populations of their host species. This differential distribution has provided important insights into tracing the evolutionary dynamics of virus populations within their hosts [8].
Along these lines, in previous studies, we used enJSRVs to (i) investigate the history of sheep domestication [9], (ii) explore the molecular mechanisms through which the most recent enJSRV—enJSRV-26—eludes the restriction exerted by enJS56A1 (which entered the sheep genome before and during the speciation within the genus Ovis) [10], or (iii) study the chromosome location of some enJSRV loci by fluorescent in situ hybridization (FISH) analyses of metaphase R-banded sheep chromosomes [9,10].
In the present work, we extend the cytogenetic physical maps of both sheep and river buffalo chromosomes by FISH mapping fifteen and twenty-three additional enJSRVs, respectively. In addition, we perform the first comparative FISH mapping of genetically characterized enJSRVs in domestic sheep and river buffalo (Bubalus bubalis).

2. Materials and Methods

Cell cultures. Peripheral blood lymphocytes of sheep (Ovis aries, OAR; 2n = 54) (four animals) and river buffalo (Bubalus bubalis, BBU; 2n = 50) (three animals) were cultured for 72 h in Roswell Park Memorial Institute (RPMI)-1640 culture medium enriched with 15% fetal calf serum (FCS), concanavalin A (15 µg/mL), penicillin/streptomycin (0.1 mL), L-glutamine (0.1 mL), and one drop of sterile sodium heparin to prevent coagulation. In order to obtain R-banding patterns and cause metaphase arrest, 7 h prior to harvesting, cells were labeled with BrdU (15 μg/mL) and Hoechst 33258 (30 μg/mL) and, 6 h later, they were treated with colcemid (0.1 μg/mL). After incubation in a hypotonic solution (KCl 0.075 M at 37.5 °C for 20 min), cells were fixed three times with 3:1 methanol–acetic acid (v/v) solution. Cell suspensions were then spread onto a slide, and stored at −20 °C.
Probes and FISH mapping. FISH analysis was performed using standard procedures [11,12]. Briefly, cells were pre-treated overnight at 50 °C, and subsequently stained with Hoechst 33258 (25 μg/mL) for 10 min. Slides were then exposed to UV light for 20 min, washed with distilled water, and air-dried. Hybridization, chromosome staining, signal detection and image processing were carried out as already described [11,12]. Slides were mounted in antifade mounting medium with propidium iodide to visualize both FITC-signals and RBPI-banding using two microscope filter combinations. Two images for each metaphase were acquired with both FITC signals and RBPI-banding. Next, FITC signals were superimposed on RBPI-banding to get a precise position of FITC-signals on chromosome bands. Thirty metaphases for each probe were examined. Chromosome identification and banding numbering system followed the standard nomenclature of both species [13,14]. The bacterial artificial chromosome (BAC) clones used for sheep cytogenetic mapping have been already characterized and described elsewhere [6]. Notably, each BAC clone used to obtain the sequences of the various enJSRV loci was subjected to Southern blot analyses to verify that it contained only one locus. The list of sheep BAC clones of the CHORI-243 library containing the 27 enJSRVs used in this study is reported in Table 1:

3. Results

In the present study, we conducted FISH mapping on sheep and river buffalo chromosomes (or chromosome arms) using twenty-seven sheep BAC clones (Table 1). As reported in Table 2, we obtained good hybridization signals only with twenty-three BAC clones, allowing us to map the corresponding twenty-three enJSRV loci. Interestingly, we localized these loci on twelve different chromosomes (or chromosome arms) of both species. As reported in Table 1, we found that, for all the probes used, hybridization signals and chromosome bands localized in the same homologous chromosome pairs of both sheep and river buffalo (Table 2). For example, we found that the enJSRV-1 and enJSRV-10 loci map onto homologous sheep and river buffalo R-banded chromosomes, as shown in Figure 1. Moreover, the BAC containing the enJSRV-1 map onto two different chromosomes in both sheep (chromosomes 6 and 18) and river buffalo (chromosomes 7 and 20) (Figure 1 and Table 2). In addition, the enJSRV-15, enJSRV-20, enJSRV-21, and enJSRV-27 display the same chromosome localization as the enJSRV-1 in both species (OAR6q13 and BBU7q21, respectively) (Table 2). Finally, the enJSRV-2 and enJSRV-6 map very close in both sheep (OAR1q45 and OARiq43, respectively) and river buffalo homologous chromosomes (BBU1q45 and BBU1q43, respectively). Notably, only the enJSRV-7 maps onto the centromeric regions of all autosomes [10], probably due to the presence of highly repetitive sequences in the BAC clones, the centromeric regions being highly rich in these sequences.

4. Discussion

FISH represents a very powerful cytogenetic technique for mapping a particular genomic sequence on a chromosome [15,16], and better anchoring of radiation hybrid (RH) and genomic maps to specific chromosome regions [17,18,19,20]. In more recent years, FISH has also been recognized as a reliable diagnostic and discovery tool to evaluate genetic anomalies, by studying chromosomal aberrations in both metaphase and interphase nuclei [reviewed in [21,22,23,24,25], and defects in chromosome segregation during meiosis [26,27]. In addition, implementations of FISH with whole-chromosome painting have led to the generation of detailed comparative maps to study chromosomal homologies and divergences between related and unrelated species [28,29,30,31,32]. Finally, FISH has also become instrumental in generating detailed comparative maps to study gene order, conserved chromosomal regions, and chromosomal rearrangements between related and unrelated species [33,34,35,36].
Along these lines, FISH analyses unveiled the phylogenetic relationships between the Caprinae subfamily and the earliest-diverging Bovinae subfamily, by showing two main chromosome events occurring at the autosomes 9 and 14, and the sex chromosomes (mainly the X-chromosome). More specifically, in previous studies carried out in our group, we demonstrated that a chromosome transposition has occurred from the proximal region of Bovinae chromosome 9 to the proximal region of Caprinae chromosome 14, and that at least four chromosome rearrangements (i.e., three transpositions and one inversion) differentiated the Caprinae from the Bovinae X-chromosomes reviewed in [37].
A comparative FISH mapping of enJSRVs has been reported previously in sheep and goat cell lines [38]. In this study, the authors only partially found enJSRVs localized on the same homologous chromosome band of the two species. In addition, they found enJSRV loci in seven and eight chromosomes of sheep and goats, respectively.
In the present work, we report the first comparative FISH mapping between two species belonging to the Caprinae (Ovis aries) and Bovinae (Bubalus bubalis) subfamilies of the Bovidae family by using well-identified and genetically characterized enJSRVs [5,6]. We show that hybridization signals of enJSRVs are found in at least twelve different chromosomes (or chromosome arms) of both species, and that all mapped loci are conserved in homologous chromosome regions and chromosome bands of these two species (Table 1). However, since BACs contain large genomic inserts, it is entirely possible that, besides enJSRVs, we also simultaneously mapped other genes and sequences present on such clones that share homology with some river buffalo chromosomal regions. Indeed, since some BoERV families (i.e., BoERV24, BoERV26, BoERV28, and BoERV29) are specific to the Bovinae family [5], the same could have occurred for some enJSRV which are present in the Caprinae subfamily (i.e., Ovis aries) but not in the Bovinae subfamily (i.e., Bubabus bubalis).
We observed that, in both species, the BAC clones containing enJSRV-1 map onto two different chromosomal locations (Table 2). Interestingly, we found that enJSRV-7 is the only locus mapping at the centromeric regions of both sheep [10] and buffalo chromosomes.
The same results were achieved by FISH mapping several ERV in sheep chromosomes which exhibited abundant centromeric to the dispersed distribution of various endoviruses, probably due to the abundance of genomic organization ERV-related repetitive elements which are particularly present at the centromeric regions of the chromosomes [39].
Our comparative FISH mapping in two different bovid species further confirms the high degree of chromosome (and chromosome arm) conservation among bovids reviewed in [37]. In addition, our study supports the hypothesis that enJSRVs were present in the genomes of their bovine ancestor before the differentiation of the Caprinae subfamily (including Ovis aries) from the most ancient Bovinae subfamily (including Bubalus bubalis) [37,40]. These results are in agreement with those published in a previous study [5] tracing BoERVs evolution in several species of the Bovidae family, including cattle, sheep, goats, and water buffalo [5]. Interestingly, these authors found that most of the BoERV families are present in all the species studied, supporting the hypothesis that BoERVs entered the genome of the common ancestor of the Bovidae family about 20 MYA or less. In addition, they detected higher BoERV copy numbers in cattle compared to other bovid species, suggesting that an additional expansion of retroviral copies might have occurred in the cattle genome [5].
Interestingly, we found five enJSRV loci (enJSRV-1, enJSRV-15, enJSRV-20, enJSRV-21, and enJSRV-27) on the same chromosome band (OAR6q13/BBU7q21) (Table 2). Previous FISH mapping conducted in our group revealed two type-one loci on this very same chromosome band: the pyroglutamylated RFamide peptide receptor (QRFPR) and the translocation-associated membrane protein 1-like 1 (TRAM1L1) [41]. The RFamide peptide family consists of several groups, including the neuropeptide FF group, the prolactin-releasing peptide group, the gonadotropin inhibitory hormone group, the kisspeptin group, and the pyroglutamylated RFamide peptide (26RFa/QRFP) group [42]. Interestingly, pyroglutamylated RFamide peptide 43 has been proven to be a putative modulator of testicular steroidogenesis, playing an important role in reproduction [43]. Notably, ERVs are key in placental morphogenesis and mammalian reproduction [44]. TRAM1L1 seems to be closely related to chronic widespread musculoskeletal pain (CWP), a common disorder affecting about 5–15% of the population, and one of the main symptoms of fibromyalgia, which has been shown to be associated with an altered gut microbiome [45]. By using the sheep genome reference sequence (https://www.ncbi.nlm.nih.gov/genome/gdv/browser/genome/?id=GCF_016772045.1, accessed on 12 May 2018), we identified sixteen genes included between QRFPR and TRAM1L (Supplementary Table S1). In this table we reported some of the functions of those genes (including QRFPR and TRAM1L), mostly involved in anti-tumor immune response probably to counteract the presence of several enJSRVs in these chromosomic regions. Indeed, genomic amplification within the 6q13 region was detected, and it was found that the number of enJSRV-6q13 is correlated to the number of protective mutations [46].

5. Conclusions

To our knowledge, this is the first comparative FISH mapping of sheep and river buffalo chromosomes using genetically characterized enJSRVs. Interestingly, our results reveal a high degree of conservation of enJSRVs localization in the homologous chromosomes and chromosome bands of both species. These findings support the hypothesis that enJSRVs entered the host genome before the differentiation of the Caprinae subfamily from the earliest-diverging Bovinae subfamily of the Bovidae family. Finally, the present study extends the current genetic physical maps of sheep and river buffalo by mapping, respectively, fifteen and twenty-three additional enJSRV loci on the chromosomes and chromosome arms of these two species.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ani12202834/s1, Table S1: List of genes present in the ORA6q13 and included between QRFPR and TRAM1L1 (from: https://www.ncbi.nlm.nih.gov/genome/gdv/browser/genome/?id=GCF_016772045.1), accessed on 2 October 2022) their main functions and references;

Author Contributions

Conceptualization L.I. and M.P.; investigation, A.P. and A.A.; data curation, A.P. and A.I.; writing—original draft preparation L.I., A.A. and A.I.; writing—review and editing, A.I., L.I., A.P., A.A. and M.P.; supervision, L.I. and M.P.; funding acquisition L.I. and M.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the project PON1_486 GENOBU.

Institutional Review Board Statement

The study was approved by the CNR-ISPAAM Ethics Committee, protocol number 0000606 of 03/27/2015.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author, [AI], upon reasonable request.

Acknowledgments

We are grateful to Domenico Incarnato, CNR-ISPAAM, Portici, Italy for his excellent technical assistance.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Stoye, J.P. Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat. Rev. Microbiol. 2012, 10, 395–406. [Google Scholar] [CrossRef] [PubMed]
  2. Johnson, W.E. Origins and evolutionary consequences of ancient endogenous retroviruses. Nat. Rev. Microbiol. 2019, 17, 355–370. [Google Scholar] [CrossRef] [PubMed]
  3. Johnson, W.E. Endogenous Retroviruses. In Encyclopedia of Virology; Mahy, B.W.J., Van Regenmortel, M.H.V., Eds.; Elsevier: Oxford, UK, 2008; pp. 105–109. [Google Scholar]
  4. Gifford, R.J.; Blomberg, J.; Coffin, J.M.; Fan, H.; Heidmann, T.; Mayer, J.; Stoye, J.; Tristem, M.; Johnson, W.E. Nomenclature for endogenous retrovirus (ERV) loci. Retrovirology 2018, 15, 59. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Garcia-Etxebarria, K.; Jugo, B.M. Evolutionary history of bovine endogenous retroviruses in the Bovidae family. BMC Evol. Biol. 2013, 13, 256. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Arnaud, F.; Caporale, M.; Varela, M.; Biek, R.; Chessa, B.; Alberti, A.; Golder, M.; Mura, M.; Zhang, Y.-P.; Yu, L.; et al. A paradigm for virus-host coevolution: Sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog. 2007, 3, e170. [Google Scholar] [CrossRef] [PubMed]
  7. Arnaud, F.; Varela, M.; Spencer, T.E.; Palmarini, M. Coevolution of endogenous betaretroviruses of sheep and their host. Cell Mol. Life Sci. 2008, 65, 3422–3432. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. Armezzani, A.; Varela, M.; Spencer, T.E.; Palmarini, M.; Arnaud, F. "Ménage à Trois": The evolutionary interplay between JSRV, enJSRVs and domestic sheep. Viruses 2014, 6, 4926–4945. [Google Scholar] [CrossRef]
  9. Chessa, B.; Pereira, F.; Arnaud, F.; Amorim, A.; Goyache, F.; Mainland, I.; Kao, R.R.; Pemberton, J.M.; Beraldi, D.; Stear, M.J.; et al. Revealing the history of sheep domestication using retrovirus integrations. Science 2009, 324, 532–536. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  10. Armezzani, A.; Arnaud, F.; Caporale, M.; Di Meo, G.P.; Iannuzzi, L.; Murgia, C.; Palmarini, M. The signal peptide of a recently integrated endogenous sheep betaretrovirus envelope plays a major role in eluding gag-mediated late restriction. J. Virol. 2011, 85, 7118–7128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  11. Iannuzzi, L.; Di Berardino, D. Tools of the trade: Diagnostics and research in domestic animal cytogenetics. J. Appl. Genet. 2008, 49, 357–366. [Google Scholar] [CrossRef]
  12. Di Meo, G.P.; Perucatti, A.; Floriot, S.; Hayes, H.; Schibler, L.; Incarnato, D.; Di Berardino, D.; Williams, J.; Cribiu, E.; Eggen, A.; et al. An extended river buffalo (Bubalus bubalus, 2n = 50) cytogenetic map: Assignment of 68 autosomal loci by FISH-mapping and R-banding and comparison with human chromosomes. Chromos. Res. 2008, 16, 827–837. [Google Scholar] [CrossRef] [Green Version]
  13. Cribiu, E.; Di Berardino, D.; Di Meo, G.; Eggen, A.; Gallagher, D.; Gustavsson, I.; Hayes, H.; Iannuzzi, L.; Popescu, C.; Rubes, J.; et al. International System for Chromosome Nomenclature of Domestic Bovids (ISCNDB 2000). Cytogenet. Genome Res. 2001, 95, 283–299. [Google Scholar] [CrossRef] [PubMed]
  14. Iannuzzi, L. Report of the committee for standard karyotype of the river buffalo (Bubalus bubalis L., 2n = 50). Cytogenet. Cell Genet. 1994, 67, 102–113. [Google Scholar] [CrossRef] [PubMed]
  15. Hayes, H.; Elduque, C.; Gautier, M.; Schibler, L.; Cribiu, E.; Eggen, A. Mapping of 195 genes in cattle and updated comparative map with man, mouse, rat and pig. Cytogenet. Genome Res. 2003, 102, 16–24. [Google Scholar] [CrossRef] [PubMed]
  16. Iannuzzi, L.; Di Meo, G.P.; Gallagher, D.S.; Ryan, A.M.; Ferrara, L.; Womack, J.E. Chromosomal localization of omega and trophoblast interferon genes in goat and sheep by fluorescent in situ hybridization. J. Hered. 1993, 84, 301–304. [Google Scholar] [CrossRef]
  17. Amaral, M.E.; Grant, J.R.; Riggs, P.K.; Stafuzza, N.B.; Filho, E.A.; Goldammer, T.; Weikard, R.; Brunner, R.M.; Kochan, K.J.; Greco, A.J.; et al. A first generation whole genome RH map of the river buffalo with comparison to domestic cattle. BMC Genom. 2008, 9, 631. [Google Scholar] [CrossRef] [Green Version]
  18. Ianella, P.; Venancio, L.P.; Stafuzza, N.B.; Miziara, M.N.; Agarwala, R.; Schäffer, A.A.; Riggs, P.K.; Womack, J.E.; Amaral, M.E.J. First radiation hybrid map of the river buffalo X chromosome (BBUX) and comparison with BTAX. Anim. Genet. 2008, 39, 196–200. [Google Scholar] [CrossRef] [PubMed]
  19. Goldammer, T.; Brunner, R.M.; Rebl, A.; Wu, C.H.; Nomura, K.; Hadfield, T.; Maddox, J.F.; Cockett, N.E. Cytogenetic anchoring of radiation hybrid and virtual maps of sheep chromosome X and comparison of X chromosomes in sheep, cattle, and human. Chromos. Res. 2009, 17, 497–506. [Google Scholar] [CrossRef] [PubMed]
  20. De Lorenzi, L.; Parma, P. Identification of Some Errors in the Genome Assembly of Bovidae by FISH. Cytogenet Genome Res. 2020, 160, 85–93. [Google Scholar] [CrossRef] [PubMed]
  21. Ducos, A.; Revay, T.; Kovacs, A.; Hidas, A.; Pinton, A.; Bonnet-Garnier, A.; Molteni, L.; Slota, E.; Switonski, M.; Arruga, M.; et al. Cytogenetic screening of livestock populations in Europe: An overview. Cytogenet. Genome Res. 2008, 120, 26–41. [Google Scholar] [CrossRef] [PubMed]
  22. Iannuzzi, A.; Parma, P.; Iannuzzi, L. Chromosome Abnormalities and Fertility in Domestic Bovids: A Review. Animals 2021, 11, 802. [Google Scholar] [CrossRef] [PubMed]
  23. Szczerbal, I.; Switonski, M. Clinical Cytogenetics of the Dog: A Review. Animals 2021, 11, 947. [Google Scholar] [CrossRef] [PubMed]
  24. Iannuzzi, A.; Braun, M.; Genualdo, V.; Perucatti, A.; Reinartz, S.; Proios, I.; Heppelmann, M.; Rehage, J.; Hülskötter, K.; Beineke, A.; et al. Clinical, cytogenetic and molecular genetic characterization of a tandem fusion translocation in a male Holstein cattle with congenital hypospadias and a ventricular septal defect. PLoS ONE 2020, 15, e0227117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Donaldson, B.; Villagomez, D.; King, W.A. Classical, Molecular, and Genomic Cytogenetics of the Pig, a Clinical Perspective. Animals 2021, 11, 1257. [Google Scholar] [CrossRef] [PubMed]
  26. Di Dio, C.; Longobardi, V.; Zullo, G.; Parma, P.; Pauciullo, A.; Perucatti, A.; Higgins, J.; Iannuzzi, A. Analysis of meiotic segregation by triple-color fish on both total and motile sperm fractions in a t(1p;18) river buffalo bull. PLos ONE 2020, 15, e0232592. [Google Scholar] [CrossRef] [PubMed]
  27. Genualdo, V.; Turri, F.; Pizzi, F.; Castiglioni, B.; Marletta, D.; Iannuzzi, A. Sperm Nuclei Analysis and Nuclear Organization of a Fertile Boar-Pig Hybrid by 2D FISH on Both Total and Motile Sperm Fractions. Animals 2021, 11, 738. [Google Scholar] [CrossRef] [PubMed]
  28. Hayes, H. Chromosome painting with human chromosome-specific DNA libraries reveals the extent and distribution of conserved segments in bovine chromosomes. Cytogenet. Cell Genet. 1995, 71, 168–174. [Google Scholar] [CrossRef]
  29. Chowdhary, B.P.; Frönicke, L.; Gustavsson, I.; Scherthan, H. Comparative analysis of the cattle and human genomes: Detection of ZOO-FISH and gene mapping-based chromosomal homologies. Mamm. Genome 1996, 7, 297–302. [Google Scholar] [CrossRef] [PubMed]
  30. Iannuzzi, L.; Di Meo, G.P.; Perucatti, A.; Bardaro, T. ZOO-FISH and R-banding reveal extensive conservation of human chromosome regions in euchromatic regions of river buffalo chromosomes. Cytogenet. Cell Genet. 1998, 82, 210–214. [Google Scholar] [CrossRef] [PubMed]
  31. Iannuzzi, L.; Di Meo, G.P.; Perucatti, A.; Incarnato, D. Comparison of the human with the sheep genomes by use of human chromosome-specific painting probes. Mamm. Genome 1999, 10, 719–723. [Google Scholar] [CrossRef] [PubMed]
  32. Iannuzzi, A.; Pereira, J.; Iannuzzi, C.; Fu, B.; Ferguson-Smith, M. Pooling strategy and chromosome painting characterize a living zebroid for the first time. PLoS ONE 2017, 12, e0180158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Iannuzzi, L.; Di Meo, G.P.; Perucatti, A.; Incarnato, D.; Schibler, L.; Cribiu, E.P. Comparative FISH-mapping of bovid X chromosomes reveals homologies and divergences between the subfamilies Bovinae and Caprinae. Cytogen. Cell Genet. 2000, 89, 171–176. [Google Scholar] [CrossRef] [PubMed]
  34. Di Meo, G.P.; Perucatti, A.; Floriot, S.; Incarnato, D.; Rullo, R.; Jambrenghi, A.C.; Ferretti, L.; Vonghia, G.; Cribiu, E.; Eggen, A.; et al. Chromosome evolution and improved cytogenetic maps of the Y chromosome in cattle, zebu, river buffalo, sheep and goat. Chromos. Res. 2005, 13, 349–355. [Google Scholar] [CrossRef] [PubMed]
  35. Di Meo, G.P.; Goldammer, T.; Perucatti, A.; Genualdo, V.; Iannuzzi, A.; Incarnato, D.; Rebl, A.; Di Berardino, D.; Iannuzzi, L. Extended cytogenetic maps of sheep chromosome 1 and their cattle and river buffalo homoeologues: Comparison with the OAR1 RH map and human chromosomes 2, 3, 21 and 1q. Cytogenet. Genome Res. 2011, 133, 16–24. [Google Scholar] [CrossRef]
  36. Perucatti, A.; Genualdo, V.; Iannuzzi, A.; Rebl, A.; Di Berardino, D.; Goldammer, T.; Iannuzzi, L. Advanced comparative cytogenetic analysis of X chromosomes in river buffalo, cattle, sheep, and human. Chromos. Res. 2012, 20, 413–425. [Google Scholar] [CrossRef]
  37. Iannuzzi, L.; King, A.W.; Di Berardino, D. Chromosome evolution in domestic bovids as revealed by chromosome banding and FISH-mapping techniques. Cytogenet. Genome Res. 2009, 126, 49–62. [Google Scholar] [CrossRef] [PubMed]
  38. Carlson, J.; Lyon, M.; Bishop, J.; Vaiman, A.; Cribiu, E.; Mornex, J.-F.; Brown, S.; Knudson, D.; De Martini, J.; Leroux, C. Chromosomal Distribution of Endogenous Jaagsiekte Sheep Retrovirus Proviral Sequences in the Sheep Genome. J. Virol. 2003, 77, 9662–9668. [Google Scholar] [CrossRef] [Green Version]
  39. Mustafa, S.I.; Schwarzacher, T.; Heslop-Harrison, J.S. The Nature and Chromosomal Landscape of Endogenous Retroviruses (ERVs) Integrated in the Sheep Nuclear Genome. DNA 2022, 2, 86–103. [Google Scholar] [CrossRef]
  40. Balmus, G.; Trifonov, V.A.; Biltueva, L.S.; O’Brien, P.C.M.; Alkalaeva, E.S.; Fu, B.; Skidmore, J.A.; Allen, T.; Graphodatsky, A.S.; Yang, F.; et al. Cross-species chromosome painting among camel, cattle, pig and human: Further insights into the putative Cetartiodactyla ancestral karyotype. Chromos. Res. 2007, 15, 499–514. [Google Scholar] [CrossRef]
  41. Goldammer, T.; Di Meo, G.P.; Lühken, G.; Drögemüller, C.; Wu, C.H.; Kijas, J.; Dalrymple, B.; Nicholas, F.; Maddox, J.; Iannuzzi, L.; et al. Molecular Cytogenetics and Gene Mapping in Sheep (Ovis aries, 2n = 54). Cytogenet. Genome Res. 2009, 126, 63–76. [Google Scholar] [CrossRef]
  42. Ukena, K.; Osugi, T.; Leprince, J.; Vaudry, H.; Tsutsui, K. Molecular evolution and function of 26RFa/QRFP and its cognate receptor. J. Mol. Endocrinol. 2014, 52, T119–T131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Patel, S.K.; Singh, S.K. Pyroglutamylated RFamide peptide 43: A putative modulator of testicular steroidogenesis. Andrology 2020, 8, 1815–1823. [Google Scholar] [CrossRef]
  44. Dunlap, K.A.; Palmarini, M.; Varela, M.; Burghardt, R.C.; Hayashi, K.; Farmer, J.L.; Spencer, T.E. Endogenous retroviruses regulate periimplantation placental growth and differentiation. PNAS 2006, 103, 14390–14395. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Freidin, M.B.; Stalteri, M.A.; Wells, P.M.; Lachance, G.; Baleanu, A.-F.; Bowyer, R.C.E.; Kurilshikov, A.; Zhernakova, A.; Steves, C.J.; Williams, F.M.K. An association between chronic widespread pain and the gut microbiome. Rheumatology 2021, 60, 3727–3737. [Google Scholar] [CrossRef] [PubMed]
  46. Cumer, T.; Pompanon, F.; Boyer, F. Old origin of a protective endogenous retrovirus (enJSRV) in the Ovis genus. Heredity 2019, 122, 187–194. [Google Scholar] [CrossRef] [PubMed]
Animals 12 02834 g001 550
Figure 1. FISH mapping of enJSRV-1 (A,B) and enJSRV-10 (C,D) in sheep (OAR) and river buffalo (BBU) chromosomes. Two different images were taken, with hybridization FITC signal and with RBPI-banding. Subsequently, hybridization FITC signals were superimposed on RBPI-banding to get a precise localization of mapped loci in both species. Note that enJSRV-1 maps onto two different chromosomes in both species (A,B).
Figure 1. FISH mapping of enJSRV-1 (A,B) and enJSRV-10 (C,D) in sheep (OAR) and river buffalo (BBU) chromosomes. Two different images were taken, with hybridization FITC signal and with RBPI-banding. Subsequently, hybridization FITC signals were superimposed on RBPI-banding to get a precise localization of mapped loci in both species. Note that enJSRV-1 maps onto two different chromosomes in both species (A,B).
Animals 12 02834 g001
Table
Table 1. List of sheep BAC clones containing the 27 enJSRVs used in the present study.
Table 1. List of sheep BAC clones containing the 27 enJSRVs used in the present study.
ProvirusBAC Clone
enJSRV-16g20
enJSRV-26j6
enJSRV-37i2
enJSRV-415c2
enJSRV-519l17
enJSRV-633k3
enJSRV-735o24
enJSRV-836d13
enJSRV-936p8
enJSRV-1042k15
enJSRV-1144o16
enJSRV-1245l23
enJSRV-1348b6
enJSRV-1452d13
enJSRV-1557m3
enJSRV-1657m4
enJSRV-1765c8
enJSRV-1867f9
enJSRV-1970l9
enJSRV-2081j8
enJSRV-2184d10
enJSRV-2288g3
enJSRV-2390k11
enJSRV-2494c2
enJSRV-2598k22
enJSRV-26102b15
enJSRV-2714c2
Table
Table 2. Chromosomal localization of 23 enJSRVs in sheep (OAR) and river buffalo (BBU) chromosomes by FISH-mapping.
Table 2. Chromosomal localization of 23 enJSRVs in sheep (OAR) and river buffalo (BBU) chromosomes by FISH-mapping.
enJSRVOARBBU
enJSRV-118q2220q22
6q137q13
enJSRV-21q451q45
enJSRV-314q24dist18q24dist
enJSRV-42p21prox3q21prox
enJSRV-61q411q41
enJSRV-7centromericcentromeric
enJSRV-83q214q21
enJSRV-1014q2418q24
enJSRV-111p136q13
enJSRV-1219q2421q24
enJSRV-1314q24dist18q24
enJSRV-143p2412q34
enJSRV-156q137q21
enJSRV-1610q2413q24
enJSRV-1719q2421q24
enJSRV-1811q173p22
enJSRV-191p236q25
enJSRV-206q137q13
enJSRV-216q137q13
enJSRV-2215q2316q23dist
enJSRV-2418q2420q24
enJSRV-262p25dist3q25
enJSRV-276q137q13
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Perucatti, A.; Iannuzzi, A.; Armezzani, A.; Palmarini, M.; Iannuzzi, L. Comparative Fluorescence In Situ Hybridization (FISH) Mapping of Twenty-Three Endogenous Jaagsiekte Sheep Retrovirus (enJSRVs) in Sheep (Ovis aries) and River Buffalo (Bubalus bubalis) Chromosomes. Animals 2022, 12, 2834. https://doi.org/10.3390/ani12202834

AMA Style

Perucatti A, Iannuzzi A, Armezzani A, Palmarini M, Iannuzzi L. Comparative Fluorescence In Situ Hybridization (FISH) Mapping of Twenty-Three Endogenous Jaagsiekte Sheep Retrovirus (enJSRVs) in Sheep (Ovis aries) and River Buffalo (Bubalus bubalis) Chromosomes. Animals. 2022; 12(20):2834. https://doi.org/10.3390/ani12202834

Chicago/Turabian Style

Perucatti, Angela, Alessandra Iannuzzi, Alessia Armezzani, Massimo Palmarini, and Leopoldo Iannuzzi. 2022. "Comparative Fluorescence In Situ Hybridization (FISH) Mapping of Twenty-Three Endogenous Jaagsiekte Sheep Retrovirus (enJSRVs) in Sheep (Ovis aries) and River Buffalo (Bubalus bubalis) Chromosomes" Animals 12, no. 20: 2834. https://doi.org/10.3390/ani12202834

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