Critical appraisal of the piRNA-PIWI axis in cancer and cancer stem cells

Garcia-Borja, Elena; Siegl, Frantisek; Mateu, Rosana; Slaby, Ondrej; Sedo, Aleksi; Busek, Petr; Sana, Jiri

doi:10.1186/s40364-024-00563-3

Biomarker Research

Table 2 Expression of piRNAs in cancer tissue compared to non-tumorous tissue and their association with clinicopathological data

From: Critical appraisal of the piRNA-PIWI axis in cancer and cancer stem cells

piRNA	Cancer type	piRNA expression	Detection method	Association of higher piRNA expression with		Notes, references
piRNA	Cancer type	piRNA expression	Detection method	Survival	Metastasis	Notes, references
piR-Hep1	Hepatocellular carcinoma	Increased	NGS, RT-qPCR			[96]
piR-001773	Prostate cancer	Increased	NGS, RT-qPCR		↑	[97]
piR-017184	Prostate cancer	Increased	NGS, RT-qPCR		↑	[97]
piR-017724	Hepatocellular carcinoma	Decreased	RT-qPCR	↑		Lower expression associated with stage III-IV tumors and poor survival [98].
piR-021285	Breast cancer	Not evaluated				Single nucleotide polymorphism (SNP)- rs1326306G > T in piR-021285 is associated with increased risk of breast cancer [99].
piR-18	Colorectal cancer	Decreased	RT-qPCR			[100]
piR-651	Breast cancer	Increased	RT-qPCR			[101]
	Lung cancer (NSCLC)	Increased	RT-qPCR, Northern Blot, in situ hybridization			[102]
	Hodgkin lymphoma		RT-qPCR			Higher expression in affected lymph nodes associated with limited response to first line therapy, shorter disease-free survival and overall survival (OS) [103].
piR-823	Multiple myeloma	Increased	RT-qPCR			Higher expression correlates with advanced stages [55].
	Colorectal cancer	Increased	RT-qPCR			Higher expression correlates with advanced stages [104, 105].
	Gastric cancer	Decreased	RT-qPCR			[106]
	Esophageal cancer	Increased	RT-qPCR		↑	Higher expression associated with lymph node metastasis [107].
	Renal cell carcinoma	Decreased	RT-qPCR	↓		Lower expression compared to healthy tissue. However, higher expression correlates with shorter disease-free survival [108].
piR-1245	Colorectal cancer	Increased	NGS	↓	↑	Expression correlates with metastasis, stage of the disease and lower OS [109].
piR-1742	Renal cell carcinoma	Increased	Microarray	↓	↑	Increased expression is associated with high tumor grade, advanced stage of the disease and lower survival. Downregulation led to lower proliferation, migration, enhanced apoptosis and tumor growth in vivo. piR-1742 affects cancer cell behavior via the USP8/MUC12 axis [110].
piR-2158	Breast cancer	Decreased	NGS, RT-qPCR			PiR-2158 is decreased in ALDH⁺ cancer stem cells (CSC) compared to ALDH- cancer cells. Upregulation led to lower cell proliferation, migration and suppression of EMT and stemness markers [81].
piR-4987	Breast cancer	Increased	NGS, RT-qPCR		↑	Higher expression associated with lymph node metastasis [111].
piR-8041	Glioblastoma	Decreased	Microarray, RT-qPCR			[112]
piR-9491	Glioblastoma	Decreased	NGS, RT-qPCR			[113]
piR-12488	Glioblastoma	Decreased	NGS, RT-qPCR			[113]
piR-13643	Papillary thyroid carcinoma	Increased	NGS, RT-qPCR			[114]
piR-14633	Cervical cancer	Increased	NGS, RT-qPCR			piR-14633 involved in the regulation of METTL14/CYP1B1 [115].
piR-18849	Colorectal cancer	Increased	NGS, RT-qPCR		↑	Associated with low degree of differentiation and lymph node metastases [116].
piR-19521	Colorectal cancer	Increased	NGS, RT-qPCR		none	Associated with low degree of differentiation [116].
piR-20365	Breast cancer	Increased	NGS, RT-qPCR			[111]
piR-20485	Breast cancer	Increased	NGS, RT-qPCR			[111]
piR-20582	Breast cancer	Increased	NGS, RT-qPCR			[111]
piR-21238	Papillary thyroid carcinoma	Increased	NGS, RT-qPCR			[114]
piR-25783	Ovarian cancer	Increased	ISH	↓	↑	High expression in cancer tissue associated with high-grade serous ovarian cancer, advanced stage, omentum and appendix metastasis and worse overall survival. Ovarian cancer cells secrete piR-25783 in exosomes contributes to the formation of a premetastatic niche by activating the TGF-β/SMAD2/SMAD3 pathway in omentum fibroblasts [117].
piR-30188	Gliomas	Decreased	Microarray, RT-qPCR			[118]
piR-30473	DLBCL	Increased	Microarray	↓		Higher expression associated with low OS [119].
piR-30924	Clear cell renal cell carcinoma	Increased	Microarray			Upregulation is associated with lymph node metastasis. HIgher expression in primary tumor correlates with recurrence and shorter OS [120].
piR-31115	Clear cell renal cell carcinoma	Increased	NGS, RT-qPCR			[121]
piR-31470	Prostate cancer	Increased	RT-qPCR			piR-31470 and PIWIL4 contribute to the inactivation of GSTP1 expression via epigenetic modifications [122].
piR-34536	Clear cell renal cell carcinoma	Decreased	RT-qPCR	↑		Derived from mitochondrial DNA, lower levels associated with worse cancer specific and OS independent of age, grade and pT and M stage [123].
piR-34871	Lung cancer	Variable expression	RT-qPCR			[124]
piR-35127	Lung cancer	Variable expression	RT-qPCR			[124]
piR-36249	Testicular cancer	Decreased	RT-qPCR			[125]
piR-36712	Breast cancer	Decreased	RT-qPCR	↑	↓	Low levels associated with worse PFS and lymph node metastasis, piR-36712 functions as a tumor suppressor. It targets SEPW1P, a retroprocessed pseudogene of SEPW1 and thus inhibits SEPW1 through competition with its regulators miR-7 and miR-324 leading to increased p53, p21 and E-cadherin expression and downregulation of Slug [126].
piR-38756	Clear cell renal cell carcinoma	Increased	Microarray	↓	↑	Upregulation is associated with lymph node metastasis. Higher expression in primary tumor correlates with recurrence and shorter OS [120].
piR-46545	Lung cancer	Variable expression	RT-qPCR			[124]
piR-51810	Clear cell renal cell carcinoma	Decreased	RT-qPCR	↑		Derived from mitochondrial DNA, lower levels associated with worse PFS, cancer specific and OS independent of age, grade and pT and M stage [123].
piR-52200	Lung cancer	Variable expression	RT-qPCR			[124]
piR-54265	Colorectal cancer	Increased	RT-qPCR	↓		Tissue levels of piRNA-54265 are higher in advanced and metastatic colorectal cancer and are associated with shorter PFS and OS. piRNA-54265 binds PIWIL2 and via activation of STAT3 signaling promotes the proliferation, metastasis and chemoresistance of colorectal cancer cells [73].
piR-55490	Lung cancer	Decreased	RT-qPCR	↓		piR-55490 targets 3'UTR of the mTOR mRNA [65].
piR-57125	Clear cell renal cell carcinoma	Decreased	NGS, RT-qPCR, Microarray	↑	↓	Lower expression associated with lymph node metastasis. Lower expression correlates with recurrence and shorter OS [120, 127].
piR-164586	Lung cancer (NSCLC)	Increased	NGS, RT-qPCR			Low expression associated with stage II and III [128].
piR-211106	Lung adenocarcinoma	Decreased	NGS, RT-qPCR			[129]

NGS Next Generation Sequencing, RT-qPCR Reverse Transcription quantitative PCR, DLBCL Diffuse large B cell lymphoma, NSCLC Non-Small Cell Lung Cancer

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