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Presence of Human Papillomavirus Type 16 Related Sequences in Verrucous Carcinoma of the Larynx'

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Presence of Human Papillomavirus Type 16 Related Sequences in Verrucous Carcinoma of the Larynx' [CANCER RESEARCH 46, 2185-2188, April 19861 Presence of Human Papillomavirus Type 16 Related Sequences in Verrucous Carcinoma of the Larynx' Janet L. Brandsma,2 Bettie M. Steinberg, Allan L. Abramson, and Barbara Winkler Departments ofOtola,yngology (I. L B., B. M. S., A. L. A.J and Pathology (B. W.J, Long Is!andjewish Medical Center, New Hyde Park, New York 11042 ABSTRACT according to the method of Batsakis et a!. (3). The presence of histo logical features associated with human papillomavirus infection of the Verrucous carcinoma of the larynx clinically resembles laryngeal squamous epithelium including koilocytosis, hyperplasia, hyperkera papilloma in that both are wart-like masses on the vocalcords and may tosis, dyskeratosis, giant cells, and bi- or multinucleate cells (9) was be characterized by multifocalityand recurrence. Human papillomavirus recorded. Tissue sections werestained for papillomavirusgroup-specific (HPV) infectionis an etiologicalfactor in laryngealpapilloma,and recent antigen using an antibody produced in rabbits to HPV particles cx evidenceimplicates HPV in squamousneoplasias.To determinewhether . tracted from plantar warts and purified through two cesium chloride HPV is also associated with verrucous carcinoma of the larynx, we gradients. The avidin:biotinylated horseradish peroxidase complex pro analyzedtissue specimensfrom six patients with verrucouscarcinomaof cedure (10) (Vector Laboratories) was used for detection. Sections of the larynx by Southern and DNA dot blot hybridizationfor HPV DNA. skin warts were used as positive controls in each assay. From three patients, specimensof normal laryngealepitheliumwerealso Molecular HybridizationStudies. Biopsyspecimens or excised tissue studied. All tissues showed evidence of HPV sequences related but not samples were removed during direct laryngoscopy or following laryn identical to HPV-16. They were negative for HPV-I 1. In contrast, four gectomy and stored in liquid nitrogen. Tissues were processed without squamouscellcarcinomasofthe larynxand three normallaryngealtissues thawing to extract and purify total DNA (11). For Southern blots, 10 were negativefor HPV DNA. Histological sections of the six verrucous Mgofcellular DNA or standard reconstructions representing 1, 10, and lesions were found to contain koilocytosis. Immunoperoxidasestaining 100 copies per cell of HPV DNA were digested with PstI using condi for HPV capsid antigens was negative in all these cases. The consistent tions recommended by the supplier (New England Biolabs) (100 mr.@i and specific association of HPV with the verrucous carcinomas in this NaCl:10 mM Tris (pH 7.5):bovine serum albumin (100 zg/ml)J; electro report suggests the possibility of a pathogenic involvement. phoresed through a 1% agarose gel; and transferred to Gene Screen Plus (New England Nuclear Research Products, Boston, MA), accord ing to the procedure of Southern (12). Gene Screen Plus was chosen INTRODUCTION because its high strength and binding properties allow multiple rehy Verrucous carcinoma of the larynx is a distinct variant of bridizations without noticeable loss ofsignal (13). For DNA dot blots, 1 @gofundigested cellular DNA was applied to well-differentiated squamous cell carcinoma characterized by a Gene Screen Plus membrane usinga manifold (Seleicherand Schuell). low incidence (1—2%of all carcinomas of the larynx), male For standards, HPV inserts were separated from appropriately digested preponderance, average age over 60, and local aggressiveness plasmid DNAs (7, 8, 14) by agarose gel electrophoresis and recovered without potential to metastasize. First described by Ackerman by electroelution. Probes were cloned HPV types 18, 16, and 11 (7, 8, (1) in the oropharynx, verrucous carcinomas have been reported 14)nick-translated with all four nucleotide [a-32Pjtriphosphates(15) to in the vulva, vagina, glans penis, esophagus, and tracheobron specificactivitiesof0.2—0.9x10@cpm/@g.Southern and dot blots were cial tree as well as in the larynx (2—4).Verrucous carcinomas hybridized sequentially with the probes of choice in 5x SSC (lx SSC are generally exophytic with a markedly hyperkeratotic, papil = 0.15 M NaC1:0.015 M sodium citrate), 50 mr@i sodium phosphate (pH lary surface. They bear a number of similarities to laryngeal 6.8), 1% sodium dodecyl sulfate, 30% formamide, and 10% dextran sulfate at 42C overnight (Tm —34C).Blots were first washed in 2x papilloma. Macroscopically, both appear as warty masses, with SSC:l% sodium dodecyl sulfate at 50C (Tm —41C,“nonstringent―) notable papillary projections of the epithelial surface. Micro and sometimes rewashed in 0.lx SSC at 60T (Tm —9C,“stringent―). scopically, both are composed of cytologically bland thickened Between hybridizations, the probe was eluted as described (16). The squamous epithelium. Clinically, both types of lesions may be effectivenessof the elution was verified autoradiographically. For au characterized by multifocality and have the tendency to recur toradiography, wet filters were wrapped in Saran Wrap and exposed to locally following endoscopic surgical removal. Because HPV3 Kodak XAR5 film with DuPont Lightening Plus intensifying screens infection is known to be an important etiological factor in for varying lengths of time (see Legends to Figs. 1—3). laryngeal papilloma (5, 6), and because recent evidence impli cates the involvement of HPV in the pathogenesis of squamous neoplasia in a variety of body sites (7, 8), we have examined RESULTS verrucous carcinoma of the larynx for the presence of HPV. [email protected],malesaged51—59,pre Our findings indicate that HPV-16 related DNA is associated sented with a common history of smoking and persistent with verrucous carcinoma of the larynx. hoarseness. At direct laryngoscopy all the lesions were diag nosed as verrucous carcinoma based on their clinical appear MATERIALS AND METHODS ance. Each was circumscribed, papillary, and leukoplakic and involved one or both vocal cords. Histology and Immunohistochemistry. Histological sections from for Histology and Immunohistochemistry. Table 1 summarizes maIm-fixed, paraffin-embedded tissues were reviewed and classified the major histological findings of the six patients. Four were diagnosed as verrucous carcinoma, having thickened processes Received 8/9/85; revised 12/12/85; accepted I 2/18/85. The costs of publication of this article were defrayed in part by the payment of cytologically bland squamous epithelium extending into the of page charges. This article must therefore be hereby marked advertisement in underlying connective tissue and broad invading pushing mar accordance with 18 U.S.C. Section 1734 solely to indicate this fact. gins (17). Two (Patients 1 and 6) showed no penetration of the I This investigation was supported by Grant 5 F32 A106643-02 from the National Institute of Allergy and Infectious Disease and by Grant P01 NS19214 basement membrane in the sections examined but were other from the National Institute of Neurologic and Communicative Disorders. wise consistent with verrucous carcinOma. Koilocytosis, char 2 To whom requests for reprints should be addressed. 3 The abbreviations used are: HPV. human papillomavirus; SSC, 0.15 M acteristic of HPV infection, was identified in all cases. NaCl:0.0l5 M sodium citrate, pH 7.0; Tm, melting temperature ofduplex DNA. Adjacent tissues in four of the six patients showed focal 2185 Downloaded from cancerres.aacrjournals.org on October 1, 2021. © 1986 American Association for Cancer Research. PAPILLOMAVIRUS IN LARYNGEAL CARCINOMA Table 1 The presence ofkoilocytosis, papillomavirus group-specific antigen, and larynxKoilocytosishuman papillomavirus DNA in verrucous carcinoma ofthe E @i E@1 fl (14) was graded to indicate the relative abundance of koilocytotic 1233 12345 sss 61 cells. The presence of HPV capsid antigen was determined by use of a rabbit antibody to human plantar wart virus (see “Materialsand Methods―). The presence of HPV DNA was assessed underconditions.HPV nonstringent capsid PatientDNA1 Koilocytosis antigen HPV +2 2+ — +3 1-2+ — +4 Focal-l+ — +5 1+ — +6 1+ — 1+ — + @ O 1@ U 1 II 1233 12345 sss 67 @. @. .,@ . ,@. .:‘. L@4. Fig. 2. Detectionof HPV-l I related DNA in verrucousand other tissues by Southern blot hybridizationunder nonstringentconditions.See Fig. 1for details. This autoradiogram was exposed for 3 days. four (Patients 2—5)andprobably all five ofthe verrucous lesions (Fig. 1). Differences in the restriction pattern of the DNAs relative to the cloned HPV-16 are noted. Very faint hybridiza tion to HPV-18 was also detected (data not shown). The hy bridization patterns were similar with both probes, but stronger with HPV-16. In addition, the DNAs from visually normal sites adjacent to the tumors of three patients (Fig. 1) were also positive for HPV DNA. It is especially important to note that the adjacent site from Patient 1 is definitely positive. Despite this patient's lesion being borderline, his larynx does harbor Fig. I. Detection of HPV-l6 related DNA in verrucous and other tissues by HPV-16 related sequences. It is of interest to note that the Southern blot hybridization under nonstringent conditions. Lanes marked “.5―amount of detectable HPV-16 related DNA in the lesion did are standards representing I, 10, and 100 copies per cell of HPV-l6; these are bracketed by two blank lanes. The other lanes are numbered according to patient: not correlate with the extent of koilocytosis (Table 1). Stringent Patients
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