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Distribution of Protease-Resistant Prion Protein and Spongiform Encephalopathy in Free-Ranging Mule Deer (Odocoileus Hemionus) with Chronic Wasting Disease

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Distribution of Protease-Resistant Prion Protein and Spongiform Encephalopathy in Free-Ranging Mule Deer (Odocoileus Hemionus) with Chronic Wasting Disease Vet Pathol 39:546–556 (2002) Distribution of Protease-resistant Prion Protein and Spongiform Encephalopathy in Free-ranging Mule Deer (Odocoileus hemionus) with Chronic Wasting Disease T. R . S PRAKER,R.R.ZINK,B.A.CUMMINGS,C.J.SIGURDSON,M.W.MILLER, AND K. I. O’ROURKE Department of Pathology, College of Veterinary Medicine, Colorado State University, Fort Collins, CO (TRS, RRZ, BAC, CJS); Colorado Division of Wildlife, 317 West Prospect, Fort Collins, CO (MWM); and Animal Disease Research Unit, ARS/USDA, 3003 ADBF, Pullman, WA (KIO) Abstract. Serial sections of brain and palatine tonsil were examined by immunohistochemical staining (IHC) using monoclonal antibody F89/160.1.5 for detecting protease-resistant prion protein (PrPres) in 35 hunter- killed mule deer (Odocoileus hemionus) with chronic wasting disease. Serial sections of brain were stained with hematoxylin and eosin and examined for spongiform encephalopathy (SE). Clinical signs of disease were not observed in any of these deer. On the basis of the location and abundance of IHC and the location and severity of SE, deer were placed into four categories. Category 1 (n ϭ 8) was characterized by IHC in the palatine tonsil with no evidence of IHC or SE in the brain. Category 2 (n ϭ 13) was characterized by IHC in the palatine tonsil and IHC with or without SE in the dorsal motor nucleus of the vagus nerve (DMNV). Category 3(n ϭ 2) was characterized by IHC in the palatine tonsil, IHC with SE in the myelencephalon, and IHC without SE in the hypothalamus. Category 4 (n ϭ 12) was characterized by IHC in the palatine tonsil and IHC with SE throughout the brain. Category 1 may represent early lymphoid tissue localization of PrPres. The DMNV appears to be the most consistent single neuroanatomic site of detectable PrPres. Categories 2–4 may represent a progression of spread of PrPres and SE throughout the brain. IHC in tonsil and brain and SE in brain were not detected in 208 control deer. Key words: Brain; chronic wasting disease; immunohistochemistry; monoclonal antibody F89/160.1.5; mule deer (Odocoileus hemionus); palatine tonsil; PrPres; spongiform encephalopathy. Introduction tions: 1) Does PrPres accumulate in the palatine tonsil without detection in the brain? 2) Can PrPres be de- Chronic wasting disease (CWD), a transmissible tected in a single neuroanatomic region or throughout spongiform encephalopathy (SE), has been described the brain without the detection of SE and vice versa? 20–22 in captive cervids. A similar SE has been described 3) Are there different patterns of IHC and SE in the in free-ranging mule deer (Odocoileus hemionus), brain of free-ranging mule deer that are positive for white-tailed deer (Odocoileus virginianus), and Rocky CWD. Mountain elk (Cervus elaphus nelsoni) from north- central Colorado.18 The neuroanatomic distribution of Materials and Methods histologic lesions and the immunohistochemical stain- For the last 5 years, surveys of harvested deer and ing (IHC) pattern of a protease-resistant prion protein elk have been conducted in Colorado to determine the (PrPres) in brain and lymphoid tissue of free-ranging prevalence and geographic distribution of CWD.13 A mule deer in terminal stages of disease have been com- total of 956 deer heads were collected during hunting pared with those of captive mule deer with CWD. That seasons in Larimer County, Colorado, from August report indicated that naturally occurring SE in free- through December 1997. Brain and palatine tonsil ranging deer is morphologically indistinguishable from were removed from heads and preserved in 10% neu- CWD in captive deer, at least in the terminal stages.19 tral buffered formalin. Sections of tonsil and brain, in- Therefore, the free-ranging deer used in this study cluding the obex, hypothalamus, and cerebellum, from were considered to have CWD and not another SE. each animal were embedded in a single paraffin block. The primary objective of this investigation was to Serial sections were cut at 5 ␮m and mounted on pos- delineate the extent and distribution of PrPres in pala- itively charged glass slides. One slide was stained with tine tonsil and brain and the severity and distribution hematoxylin and eosin (HE)9 and the other with mono- of SE in free-ranging mule deer (O. hemionus) with clonal antibody F89/160.1.5 (MAb).14 This monoclo- CWD. This study would give insight into several ques- nal antibody reacts with a conserved epitope in the 546 Vet Pathol 39:5, 2002 PrPres and Encephalopathy in Mule Deer with Chronic Wasting Disease 547 PrPres, an abnormal isoform of a native cellular sialo- cephalon, and 4 in the cervical spinal cord (Fig. 1, cat- glycoprotein of mule deer, Rocky Mountain elk, do- egory 1). Neuroanatomic locations and nomenclature mestic sheep, and cattle.14 The MAb is made to a short used in this report were primarily taken from Singer.17 amino acid segment of the normal prion protein. It is Texts by Yoshikawa24 and Jenkins8 were also consulted. not specific for detection of the altered prion protein Positive IHC has been interpreted to be a scrapie- isoform. Specificity for PrPres is conferred by the hy- associated prion protein or an antigenically similar drated autoclaving of the sections in buffer before im- PrPres that has been found in lymphoid tissues and munostaining, which destroys the protease-sensitive brain of captive and free-ranging deer with normal prion protein without affecting the resistant CWD.6,7,14,16,18,19 protein. This monoclonal antibody is specific for a The palatine tonsil was considered positive if any peptide sequence within the prion protein that is con- of the follicles exhibited positive IHC. But palatine served in mule deer, Rocky Mountain elk, domestic tonsils that were positive for this IHC technique were sheep, and cattle, and after removal of the protease- characterized by having 50% or more of the follicles sensitive normal prion protein, detects only PrPres.14 filled with positive-staining material. A negative pal- PrPres has been associated with CWD of captive and atine tonsil had no staining in lymphoid follicles. A free-ranging deer and elk.6,7,14,16,18,19 typical section of tonsil contained approximately 100– Before immunostaining, tissue sections were im- 200 follicles. mersed in 88% formic acid (Mallinckrodt, Paris, KY) The relative abundance of IHC in brain was subjec- for 30 minutes, rinsed in tap water, autoclaved for 20 tively graded on a scale of 0–3 on the basis of ex- minutes at 121 C (liquid setting) in Tris buffer, and then amination with light microscopy at 20ϫ:0,nostain- cooled for 30 minutes. Sections were immunostained ing; 1, mild; 2, moderate; and 3, heavy. The intensity with MAb for 30 minutes at 37 C, and this was fol- of the stain was bright red whether the scoring was 1, lowed by addition of a biotinylated anti-mouse second- 2, or 3. ary antibody, an alkaline phosphatase–streptavidin con- Criteria used for histologic diagnosis of CWD in- jugate, a substrate chromogen (fast red), and a hema- cluded intraneuronal vacuolation, microcavitation of toxylin counterstain with bluing (Ventana Medical Sys- gray matter, neuronal degeneration and loss with mild tems, Tucson, AZ). The technique used for the IHC was Astrocytosis, or the presence of PrPres detected by IHC similar to previously described methods.2,10–12,15,16,18,19 in brain (or all).14,18,19,20–22 The severity of SE was grad- Of these 956 animals, 48 deer were considered pos- ed on a scale of 0–3: 0, no lesions; 1, mild; 2, mod- itive for CWD because they had IHC with or without erate; and 3, severe. The primary histologic lesions SE in the dorsal motor nucleus of the vagus nerve used to judge the severity of SE were neuronal cyto- (DMNV). None of the hunters who had killed these plasmic vacuolation and vacuolation of the neuropil. positive deer suspected that the animals had CWD. Ten Astrocytosis was extremely difficult to evaluate using additional deer were found to have IHC in the ger- HE and was not used in evaluation of the severity of minal centers of the palatine tonsil without IHC or lesions. For each neuroanatomic area examined, the histologic lesions of SE in the brain. Animals from prevalence and severity of the SE were recorded. these two groups were selected for further examination Negative controls for this study included brain and and included the 10 deer with IHC only in the follicles tonsil from 208 deer collected from areas within Col- of the palatine tonsil and 25 deer with IHC in palatine orado where CWD had not been found. In all these tonsil and brain. deer, sections of obex, hypothalamus, thalamus, cere- To further characterize the neural lesions in these 35 bellum, and tonsil were stained with HE and MAb. All deer, 13–16 sections were made from the remaining these deer were examined without knowledge that they brain, embedded in paraffin, and serial sections cut from had originated from areas outside the known CWD each block. One slide was stained with HE and the endemic area. other with MAb as previously described. Typical sec- Results tions of brain included one to three levels of rhinen- Thirty-five of the 58 hunter-killed deer with positive cephalon with adjacent cortex and basal nuclei, hypo- IHC of the palatine tonsil had sufficient tissue available thalamus, thalamus (including epithalamus and subthal- for a detailed study of the distribution and abundance amus), hippocampus, amygdala, mesencephalon, pons, of PrPres and the distribution and severity of SE in the cerebellum, obex, and spinal cord (C-1). The number brain. From the evaluation of serial sections of brain, of specific sites and axonal tracts evaluated for IHC and these animals could be placed into four categories.
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