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Research Article | Clinical Science and Epidemiology

Metagenomic Discovery of 83 New Human Papillomavirus Types in Patients with Immunodeficiency

Diana V. Pastrana, Alberto Peretti, Nicole L. Welch, Cinzia Borgogna, Carlotta Olivero, Raffaele Badolato, Lucia D. Notarangelo, Marisa Gariglio, Peter C. FitzGerald, Carl E. McIntosh, Jesse Reeves, Gabriel J. Starrett, Valery Bliskovsky, Daniel Velez, Isaac Brownell, Robert Yarchoan, Kathleen M. Wyvill, Thomas S. Uldrick, Frank Maldarelli, Andrea Lisco, Irini Sereti, Christopher M. Gonzalez, Elliot J. Androphy, Alison A. McBride, Koenraad Van Doorslaer, Francisco Garcia, Israel Dvoretzky, Joceline S. Liu, Justin Han, Philip M. Murphy, David H. McDermott, Christopher B. Buck
Michael J. Imperiale, Editor
Diana V. Pastrana
Laboratory of Cellular Oncology, National Cancer Institute, Bethesda, Maryland, USA
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Alberto Peretti
Laboratory of Cellular Oncology, National Cancer Institute, Bethesda, Maryland, USA
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Nicole L. Welch
Laboratory of Cellular Oncology, National Cancer Institute, Bethesda, Maryland, USA
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Cinzia Borgogna
Novara Medical School, Novara, Italy
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Carlotta Olivero
Novara Medical School, Novara, Italy
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Raffaele Badolato
University of Brescia, Brescia, Italy
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Lucia D. Notarangelo
University of Brescia, Brescia, Italy
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Marisa Gariglio
Novara Medical School, Novara, Italy
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Peter C. FitzGerald
NCI Genome Analysis Unit, NCI, Bethesda, Maryland, USA
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Carl E. McIntosh
NCI Genome Analysis Unit, NCI, Bethesda, Maryland, USA
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Jesse Reeves
Laboratory of Cellular Oncology, National Cancer Institute, Bethesda, Maryland, USA
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Gabriel J. Starrett
Laboratory of Cellular Oncology, National Cancer Institute, Bethesda, Maryland, USA
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Valery Bliskovsky
Cancer Genetics Branch, NCI, Bethesda, Maryland, USA
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Daniel Velez
Molecular Signaling Section, Laboratory of Molecular Immunology, NIAID, Bethesda, Maryland, USA
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Isaac Brownell
National Institute of Arthritis and Musculoskeletal and Skin Diseases, Bethesda, Maryland, USA
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Robert Yarchoan
HIV and AIDS Malignancy Branch, NCI, Bethesda, Maryland, USA
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  • ORCID record for Robert Yarchoan
Kathleen M. Wyvill
HIV and AIDS Malignancy Branch, NCI, Bethesda, Maryland, USA
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Thomas S. Uldrick
HIV and AIDS Malignancy Branch, NCI, Bethesda, Maryland, USA
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Frank Maldarelli
Host Virus Interaction Branch, NCI, Bethesda, Maryland, USA
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Andrea Lisco
Laboratory of Immunoregulation, NIAID, Bethesda, Maryland, USA
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Irini Sereti
Laboratory of Immunoregulation, NIAID, Bethesda, Maryland, USA
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Christopher M. Gonzalez
Department of Urology, Case Western Reserve University, Cleveland, Ohio, USADepartment of Pathology, Case Western Reserve University, Cleveland, Ohio, USA
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Elliot J. Androphy
Stark Neurosciences Research Institute, Indiana University, Indianapolis, Indiana, USA
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Alison A. McBride
DNA Tumor Virus Section, NIAID, Bethesda, Maryland, USA
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Koenraad Van Doorslaer
School of Animal and Comparative Biomedical Sciences, Department of Immunobiology, Cancer Biology Graduate Interdisciplinary Program, University of Arizona, Tucson, Arizona, USASchool of Animal and Comparative Biomedical Sciences, Department of Immunobiology, Genetics Graduate Interdisciplinary Program, University of Arizona, Tucson, Arizona, USABio5 Institute, University of Arizona, Tucson, Arizona, USAUniversity of Arizona Cancer Center, University of Arizona, Tucson, Arizona, USA
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Francisco Garcia
Mel and Enid Zuckerman College of Public Health, University of Arizona, Tucson, Arizona, USA
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Israel Dvoretzky
Yale University, New Haven, Connecticut, USA
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Joceline S. Liu
Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA
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Justin Han
Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA
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Philip M. Murphy
Molecular Signaling Section, Laboratory of Molecular Immunology, NIAID, Bethesda, Maryland, USA
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David H. McDermott
Molecular Signaling Section, Laboratory of Molecular Immunology, NIAID, Bethesda, Maryland, USA
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Christopher B. Buck
Laboratory of Cellular Oncology, National Cancer Institute, Bethesda, Maryland, USA
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Michael J. Imperiale
University of Michigan—Ann Arbor
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Ulrike Wieland
University of Cologne
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Elizabeth Grice
Perelman School of Medicine, University of Pennsylvania
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DOI: 10.1128/mSphereDirect.00645-18
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  • FIG 1
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    FIG 1

    Known taxa in skin swabs from healthy subjects, WHIM patients, and patients with other diseases. Donut graphs show the total numbers of reads of known taxa of interest detected in swab samples from individuals from various categories: healthy lab volunteers (TVMBS), lichen sclerosus (LS) patients, Merkel cell carcinoma (M) patients, EV patients, GATA2 (GA2), DOCK8, and WHIM patients (W or WG). For the WHIM patients, each graph shows the first collected sample of affected nongenital or genital (-Gen) skin for each patient.

  • FIG 2
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    FIG 2

    HPVs and HPyVs in wart biopsy samples/scrapings. (A and B) Warts from immunologically normal subjects (A) or immunodeficient patients (WILD, idiopathic CD4 lymphopenia [ICL], and WHIM [W] patients) (B) were assessed for the presence of distinct HPV types. Genera are depicted in different colors, with slices of the same color representing different types in the same genus. Blue numbers inside the donut represent the total number of viral types for the sample. In some cases, such as W03, some of the types represented a very small fraction of the whole, and wedges are not discernible. Black numbers on the donut correspond to the HPV type or isolate designation (letters are used to denote not-yet-assigned new HPV types), or human polyomavirus (HPyV) species number. For example, Wart I contained a single type, HPV1 from the Mupapillomavirus genus (Mu). For clarity, only the larger predominant graph segments are annotated with HPV type designations. Some patients had biopsy specimens of multiple warts, and each is shown individually.

  • FIG 3
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    FIG 3

    Phylogenetic analysis of reported HPV types. (A and B) Protein sequences from L1 (A) or E1 (B) were used to construct phylogenetic trees. At least one HPV type from each previously known species (black font) was analyzed along with each of the 83 complete HPV genomes catalogued in the current study. Asterisks were used to show known representative species that did not fit due to the figure’s space restrictions (counterclockwise, Beta 3-HPV49, Gamma 20-HPV163, Gamma 21-HPV167, and Gamma 2-HPV48). HPV genera are depicted by different colors as follows: orange, Alpha; red, Beta; blue, Gamma; pink, Mu; green, Nu. Dotted lines are not significant; they were used to indicate HPV type names. Arrows indicate potential new species.

  • FIG 4
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    FIG 4

    Comparison of viral diversity among skin swabs of patients. (A to D) Analysis of pooled swab samples from affected (warts, rashes, etc.) and healthy skin from the earliest single time point for MCC patients (A), EV patients (B), a GATA2, a DOCK8 and an ICL patient (originally classified as EV-like) (C), and WHIM patients (D). Blue numbers inside the donut represent the numbers of viral types. Black numbers on the donut represent predominant HPV types (letters are used to denote not-yet-assigned new HPV types).

  • FIG 5
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    FIG 5

    HPV typing for three individuals on plerixafor therapy. Analysis of samples from WHIM patients during long treatment. Each donut represents pooled samples from several anatomical locations. Samples from patient W06 are from the same time point, the first donut contains swabs from the following sites: right (R) 4th finger, R wrist, and an oral lesion; the second donut represents pooled swabs from the R 2nd finger, R forearm, and R palm. Samples from patient W20 are from different time points: (i) R calf, R ankle, left (L) top of foot, L thigh, and R sole of foot; (ii) normal skin of the abdomen; (iii) L palm and right foot, (iv) L eye cantus; (v) R leg follicular lesions; (vi) R leg open wound. Samples from patient W27 are from the following sites: (i) R toes, R dorsum of foot, R middle finger, R ankle, R jaw, L hand; (ii) R middle finger, L ring finger, L hand, R toes, R calf; (iii) R sole; (iv) L hand periungal. The first available time points for W20 and W27 were first shown in Fig. 4, and are also added here for comparison. Blue numbers inside the donut represent the numbers of viral types. Black numbers on the donut represent predominant HPV types (letters are used to denote not-yet-assigned new HPV types).

Tables

  • Figures
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  • TABLE 1

    Characteristics of patients and samples in this study

    TABLE 1
    • ↵a The age (in years) for one individual or age range (in years) for more than one individual is shown if known.

    • ↵b The sex (female [F] or male [M]) of the patient or volunteer is shown if known. The number of individuals is shown in parentheses.

    • ↵c One pool of swabs from 14 volunteers was processed as a single sample. The swabs from seven volunteers were processed individually. Vaginal washes from six individuals were pooled.

    • ↵d Swabs from all 18 patients were pooled into a single sample.

Supplemental Material

  • Figures
  • Tables
  • TABLE S1

    Sample description and sequencing data. Description of the samples used in this article, including anatomical site, date of collection, and number of reads per category. Download Table S1, XLSX file, 0.03 MB.

    This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply.

  • FIG S1

    HPV diversity in genital swabs of ICL or WHIM patients. Swabs shown are from a single time point for individual patients. Blue numbers inside the donuts represent the numbers of viral types. Black numbers on the donuts represent the numbers of predominant HPV types. Download FIG S1, TIF file, 0.2 MB.

    This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply.

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Metagenomic Discovery of 83 New Human Papillomavirus Types in Patients with Immunodeficiency
Diana V. Pastrana, Alberto Peretti, Nicole L. Welch, Cinzia Borgogna, Carlotta Olivero, Raffaele Badolato, Lucia D. Notarangelo, Marisa Gariglio, Peter C. FitzGerald, Carl E. McIntosh, Jesse Reeves, Gabriel J. Starrett, Valery Bliskovsky, Daniel Velez, Isaac Brownell, Robert Yarchoan, Kathleen M. Wyvill, Thomas S. Uldrick, Frank Maldarelli, Andrea Lisco, Irini Sereti, Christopher M. Gonzalez, Elliot J. Androphy, Alison A. McBride, Koenraad Van Doorslaer, Francisco Garcia, Israel Dvoretzky, Joceline S. Liu, Justin Han, Philip M. Murphy, David H. McDermott, Christopher B. Buck
mSphere Dec 2018, 3 (6) e00645-18; DOI: 10.1128/mSphereDirect.00645-18

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Metagenomic Discovery of 83 New Human Papillomavirus Types in Patients with Immunodeficiency
Diana V. Pastrana, Alberto Peretti, Nicole L. Welch, Cinzia Borgogna, Carlotta Olivero, Raffaele Badolato, Lucia D. Notarangelo, Marisa Gariglio, Peter C. FitzGerald, Carl E. McIntosh, Jesse Reeves, Gabriel J. Starrett, Valery Bliskovsky, Daniel Velez, Isaac Brownell, Robert Yarchoan, Kathleen M. Wyvill, Thomas S. Uldrick, Frank Maldarelli, Andrea Lisco, Irini Sereti, Christopher M. Gonzalez, Elliot J. Androphy, Alison A. McBride, Koenraad Van Doorslaer, Francisco Garcia, Israel Dvoretzky, Joceline S. Liu, Justin Han, Philip M. Murphy, David H. McDermott, Christopher B. Buck
mSphere Dec 2018, 3 (6) e00645-18; DOI: 10.1128/mSphereDirect.00645-18
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    • ABSTRACT
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KEYWORDS

epidermodysplasia verruciformis
gammapapillomaviruses
metagenomic
next-generation sequencing
plerixafor
skin swabs
WHIM syndrome

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