May Michael S, Park Heekuk, Moallem Dalia H, Seeram Dwayne, Dajiang Sun, Hibshoosh Hanina, Jamison Jacob K, Uhlemann Anne-Catrin, Manji Gulam A
Department of Medicine, Vagelos College of Physicians & Surgeons, Columbia University, 630 West 168th Street, New York, NY 10032, USA.
Department of Pathology, Vagelos College of Physicians & Surgeons, Columbia University, 630 West 168th Street, New York, NY 10032, USA.
Int J Mol Sci. 2024 Dec 27;26(1):140. doi: 10.3390/ijms26010140.
The gut microbiome plays an important role in the carcinogenesis of luminal gastrointestinal malignancies and response to antineoplastic therapy. Preclinical studies have suggested a role of intratumoral gammaproteobacteria in mediating response to gemcitabine-based chemotherapy in pancreatic ductal adenocarcinoma (PDAC). To our knowledge, this is the first study to evaluate the impact of the PDAC microbiome on chemotherapy response using samples from human pancreatic tumor resections. We performed 16S rRNA gene amplification and sequencing on both formalin-fixed paraffin-embedded (FFPE) and fresh frozen human PDAC resection samples. We analyzed frozen samples from 26 patients with resected PDAC and examined tumor and tumor-adjacent normal tissue. These patients represented nine long-term survivors (LTS) and nine short-term survivors (STS) after neoadjuvant gemcitabine therapy and eight control patients who did not receive any neoadjuvant therapy prior to resection. We also included FFPE samples from five patients, including tumor samples (3 samples per patient), tumor-adjacent normal tissue (2 per patient) and tumor-adjacent paraffin (1 per patient). Within frozen tissue, total DNA yields were high, but bacterial DNA was generally low, comparable to those seen in negative controls. In FFPE tissue, DNA yields were low and bacterial abundances were comparable in paraffin, tumor and normal PDAC samples. Gammaproteobacteria concentrations did not correlate with outcomes in patients treated with neoadjuvant gemcitabine-based chemotherapy. Our study found low microbial biomass in pancreatic tumor tissue, with no detectable association between bacterial taxa and chemotherapy outcomes. These results suggest a limited role of the microbiome in gemcitabine-based chemotherapy response in PDAC. Preclinical studies have implicated the pancreatic tumor microbiome in driving response to therapy. Cytidine deaminase, an enzyme produced by gammaproteobacteria, can metabolize gemcitabine and has been hypothesized to inhibit pancreatic tumor response to chemotherapy. Several clinical trials have evaluated the role of the tumor microbiome in pancreatic cancer treatment. We evaluated the impact of the pancreatic tumor microbiome on chemotherapy response using samples from human pancreatic tumor resections. We found a low microbial load that is partially attributable to contaminants and that gammaproteobacteria levels did not correlate with outcomes in patients with pancreatic cancer treated with gemcitabine-based chemotherapy.
肠道微生物群在管腔胃肠道恶性肿瘤的致癌作用及抗肿瘤治疗反应中发挥着重要作用。临床前研究表明,肿瘤内γ-变形菌在介导胰腺导管腺癌(PDAC)对吉西他滨为基础的化疗反应中发挥作用。据我们所知,这是第一项利用人类胰腺肿瘤切除样本评估PDAC微生物群对化疗反应影响的研究。我们对福尔马林固定石蜡包埋(FFPE)和新鲜冷冻的人类PDAC切除样本进行了16S rRNA基因扩增和测序。我们分析了26例接受PDAC切除患者的冷冻样本,并检查了肿瘤及肿瘤旁正常组织。这些患者包括新辅助吉西他滨治疗后的9例长期存活者(LTS)和9例短期存活者(STS),以及8例在切除前未接受任何新辅助治疗的对照患者。我们还纳入了5例患者的FFPE样本,包括肿瘤样本(每位患者3份样本)、肿瘤旁正常组织(每位患者2份)和肿瘤旁石蜡(每位患者1份)。在冷冻组织中,总DNA产量较高,但细菌DNA通常较低,与阴性对照中的情况相当。在FFPE组织中,DNA产量较低,石蜡、肿瘤和正常PDAC样本中的细菌丰度相当。γ-变形菌浓度与接受新辅助吉西他滨为基础化疗的患者的预后无关。我们的研究发现胰腺肿瘤组织中的微生物生物量较低,细菌分类群与化疗结果之间未发现可检测到的关联。这些结果表明微生物群在PDAC以吉西他滨为基础的化疗反应中作用有限。临床前研究表明胰腺肿瘤微生物群在驱动治疗反应中发挥作用。胞苷脱氨酶是一种由γ-变形菌产生的酶,可代谢吉西他滨,并被推测可抑制胰腺肿瘤对化疗的反应。几项临床试验评估了肿瘤微生物群在胰腺癌治疗中的作用。我们利用人类胰腺肿瘤切除样本评估了胰腺肿瘤微生物群对化疗反应的影响。我们发现微生物负荷较低,部分归因于污染物,并且γ-变形菌水平与接受吉西他滨为基础化疗的胰腺癌患者的预后无关。