Uterine smooth muscle tumors with features suggesting fumarate hydratase aberration: detailed morphologic analysis and correlation with S-(2-succino)-cysteine immunohistochemistry - PubMed
Uterine smooth muscle tumors with features suggesting fumarate hydratase aberration: detailed morphologic analysis and correlation with S-(2-succino)-cysteine immunohistochemistry
Carolina Reyes et al. Mod Pathol. 2014 Jul.
Abstract
Rare, sporadic uterine leiomyomas arise in the setting of severe metabolic aberration due to a somatic fumarate hydratase mutation. Germline mutations account for the hereditary leiomyomatosis and renal cell carcinoma syndrome, which predisposes for cutaneous and uterine leiomyomas and aggressive renal cell carcinomas. Altered fumarate hydratase leads to fumarate accumulation in affected cells with formation of S-(2-succino)-cysteine, which can be detected with the polyclonal antibody. High levels of these modified cysteine residues are found characteristically in fumarate hydratase-deficient cells but not in normal tissues or tumors unassociated with hereditary leiomyomatosis and renal cell carcinoma syndrome. We hypothesized that S-(2-succino)-cysteine-positive leiomyomas, indicating fumarate hydratase aberration, have morphologic features that differ from those without S-(2-succino)-cysteine positivity. Hematoxylin and eosin-stained slides of uterine smooth-muscle tumors were prospectively analyzed for features suggesting hereditary leiomyomatosis and renal cell carcinoma syndrome, such as prominent eosinophilic macronucleoli with perinucleolar halos, yielding nine cases. Germline genetic testing for fumarate hydratase mutations was performed in three cases. A detailed morphological analysis was undertaken, and S-(2-succino)-cysteine immunohistochemical analysis was performed with controls from a tissue microarray (leiomyomas (19), leiomyosarcomas (29), and endometrial stromal tumors (15)). Of the nine study cases, four had multiple uterine smooth muscle tumors. All cases had increased cellularity, staghorn vasculature, and fibrillary cytoplasm with pink globules. All cases had inclusion-like nucleoli with perinuclear halos (7 diffuse, 1 focal). All showed diffuse granular cytoplasmic labeling with the S-(2-succino)-cysteine antibody. Two of three tested patients had germline fumarate hydratase mutations. Only one leiomyoma from the tissue microarray controls was immunohistochemically positive, and it showed features similar to other immunohistochemically positive cases. Smooth-muscle tumors with fumarate hydratase aberration demonstrate morphological reproducibility across cases and S-(2-succino)-cysteine immuno-positivity. Although the features described are not specific for the germline fumarate hydratase mutation or the hereditary leiomyomatosis and renal cell carcinoma syndrome, their presence should suggest fumarate hydratase aberration. Identifying these cases is an important step in the diagnostic workup of patients with possible hereditary leiomyomatosis and renal cell carcinoma.
Figures

S-(2-succino)-cysteine-positive leiomyoma showing staghorn vasculature and increased cellularity.

S-(2-succino)-cysteine-positive
leiomyoma showing prominent eosinophilic nucleoli with perinucleolar halos and eosinophilic globules.
S-(2-succino)-cysteine-positive leiomyoma showing prominent eosinophilic nucleoli with perinucleolar halos and fibrillary cytoplasm.

S-(2-succino)-cysteine-positive leiomyoma showing a neurilemmoma-like growth pattern.

(A) S-(2-succino)-cysteine-positive leiomyoma showing eosinophilic globules indicated by arrowheads. (B) S-(2-succino)-cysteine immunohistochemistry demonstrates granular cytoplasmic labeling that spares the eosinophilic globules, indicated by arrowheads.

(A) S-(2-succino)-cysteine-positive leiomyoma showing eosinophilic globules indicated by arrowheads. (B) S-(2-succino)-cysteine immunohistochemistry demonstrates granular cytoplasmic labeling that spares the eosinophilic globules, indicated by arrowheads.

(A) S-(2-succino)-cysteine-positive leiomyoma from the tissue microarray, showing staghorn vasculature and increased cellularity. (B) Many nuclei show optical clearing (arrow) and small, eosinophilic nucleoli (arrowhead).

(A) S-(2-succino)-cysteine-positive leiomyoma from the tissue microarray, showing staghorn vasculature and increased cellularity. (B) Many nuclei show optical clearing (arrow) and small, eosinophilic nucleoli (arrowhead).
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