Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis

Imad J. Matouk; Ibrahim Abbasi; Abraham Hochberg; Eithan Galun; Hassan Dweik; Mutaz Akkawi

doi:10.1097/MEG.0b013e328306a3a2

Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis

Imad J. Matouk, Ibrahim Abbasi, Abraham Hochberg, Eithan Galun, Hassan Dweik, Mutaz Akkawi

Research output: Contribution to journal › Article › peer-review

181 Scopus citations

Abstract

Background The highly upregulated in liver cancer (HULC) gene transcribes to an mRNA-like noncoding RNA (ncRNA) by the RNA polymerase II and processed by capping, splicing and polyadenylation. It is specifically expressed in the hepatocytes with striking upregulation in hepatocellular carcinoma (HCC). Objectives To study the expression levels of HULC in normal colorectal samples, primary colorectal carcinomas and in secondary tumors formed from colorectal carcinomas that metastasize to either the liver or the lymph nodes, taken from the same patients. Also a panel of carcinoma cell lines is tested for HULC expression. Basic methods Semiquantitative reverse transcriptase- PCR technique is used to detect for HULC expression in study specimens and cell lines. Results Consistent with the previous report, HULC is neither expressed in primary colorectal carcinomas samples nor in their normal counterparts. We show for the first time those colorectal carcinomas that metastasize to the livers but not to lymph nodes experience an upregulation of HULC ncRNA in all the samples tested (n=8), with a strong-to-moderate expression in six out of eight Moreover HULC is not expressed in the majority of carcinoma cell lines tested and also in samples of normal bladder and bladder cancers of various grades. We also show that HULC ncRNA is upregulated in two hepatocellular carcinoma cell lines producing HBV relevant to their parental lines that do not produce HBV. Conclusion Our results presented here indicate that HULC expression is not confined to HCC, but also to those colorectal carcinomas that metastasize to the liver.

Original language	American English
Pages (from-to)	688-692
Number of pages	5
Journal	European Journal of Gastroenterology and Hepatology
Volume	21
Issue number	6
DOIs	https://doi.org/10.1097/MEG.0b013e328306a3a2
State	Published - Jun 2009

Bibliographical note

Cited By :176

Export Date: 30 January 2023

CODEN: EJGHE

Correspondence Address: Matouk, I. J.; Alquds And Hebrew Universities, , Jerusalem, Israel; email: imatook@cc.huji.ac.il

Chemicals/CAS: RNA, Neoplasm; RNA, Untranslated

References: Bartel, D.P., MicroRNAs: Genomics, biogenesis, mechanism and function (2004) Cell, 116, pp. 281-297; Zamore, P.D., Haley, B., Ribo-genome: The big world of small RNAs (2005) Science, 309, pp. 1519-1524; Volinia, S., Calin, G.A., Liu, C.G., Ambs, S., Cimmino, A., Petrocca, F., A microRNA expression signature of human solid tumors defines cancer gene targets (2006) Proc Natl Acad Sci USA, 103, pp. 2257-2261; He, L., Thomson, J.M., Hemann, M.T., Hernando-Monge, E., Mu, D., Goodson, S., A microRNA polycistron as a potential human oncogene (2005) Nature, 435, pp. 828-833; Matouk, U., DeGroot, N., Mezan, S., Ayesh, S., Abu-Lail, R., Hochberg, A., The H19 non-coding RNA is essential for human tumor growth (2007) PloS ONE, 2, pp. e845; Matouk, I., Ohana, P., Ayesh, S., Sidi, A., Czerniak, A., De Groot, N., The oncofetal H19 RNA in human cancer from the bench to the patient (2005) Cancer Ther, 3, pp. 249-266; Panzitt, K., Tschernatsch, M.M., Guelly, C., Moustafa, T., Stradner, M., Strohmaier, H.M., Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA (2007) Gastroenterology, 132, pp. 330-342; Kavolius, J., Fong, Y., Blumgart, L.H., Surgical resection of metastatic liver tumors (1996) Surg Oncol Clin, 5, pp. 337-352; Laurent-Puig, P., Zucman-Rossi, J., Genetics of hepatocellular tumors (2006) Oncogene, 25, pp. 3778-3786; Fellig, Y., Almogy, G., Galun, E., Ketzinel-Gilad, M., A hepatocellular carcinoma cell line producing mature hepatitis B viral particles (2004) Biochem Biophys Res Commun, 321, pp. 269-274; Odom, D.T., Dowell, R.D., Jacobsen, E.S., Gordon, W., Danford, T.W., Maclsaac, K.D., Tissue-specific transcriptional regulation has diverged significantly between human and mouse (2007) Wat Genet, 39, pp. 730-732

Keywords

Bladder carcinomas
Colorectal carcinomas
Highly upregulated in liver cancer
Liver metastasis
Liver microenvironment
Lymph nodes metastasis
Noncoding RNA
Primary and secondary growth
untranslated RNA
animal model
animal tissue
article
bladder
bladder cancer
bladder carcinoma
breast carcinoma
cancer cell culture
cancer staging
carcinoma cell
cell strain MCF 7
colon
colon carcinoma
colorectal cancer
colorectal carcinoma
disease severity
female
gene expression
gene overexpression
HeLa cell
Hepatitis B virus
highly upregulated in liver cancer gene
human
human cell
human tissue
liver cell
liver cell carcinoma
liver metastasis
lymph node metastasis
metastasis
mouse
nonhuman
ovary carcinoma
pancreas cancer
pancreas carcinoma
priority journal
quantitative analysis
rectum
reverse transcription polymerase chain reaction
sample
tumor gene
upregulation
Animals
Colorectal Neoplasms
Gene Expression Regulation, Neoplastic
Humans
Liver Neoplasms
Mice
Mice, Nude
Neoplasm Transplantation
Reverse Transcriptase Polymerase Chain Reaction
RNA, Neoplasm
RNA, Untranslated
Transplantation, Heterologous
Tumor Cells, Cultured
Up-Regulation

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1097/MEG.0b013e328306a3a2

https://www.scopus.com/inward/record.uri?eid=2-s2.0-67649664083&doi=10.1097%2fMEG.0b013e328306a3a2&partnerID=40&md5=69cf2c4eb7de2a13e93fde6b6b2da10a

Cite this

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title = "Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis",

abstract = "Background The highly upregulated in liver cancer (HULC) gene transcribes to an mRNA-like noncoding RNA (ncRNA) by the RNA polymerase II and processed by capping, splicing and polyadenylation. It is specifically expressed in the hepatocytes with striking upregulation in hepatocellular carcinoma (HCC). Objectives To study the expression levels of HULC in normal colorectal samples, primary colorectal carcinomas and in secondary tumors formed from colorectal carcinomas that metastasize to either the liver or the lymph nodes, taken from the same patients. Also a panel of carcinoma cell lines is tested for HULC expression. Basic methods Semiquantitative reverse transcriptase- PCR technique is used to detect for HULC expression in study specimens and cell lines. Results Consistent with the previous report, HULC is neither expressed in primary colorectal carcinomas samples nor in their normal counterparts. We show for the first time those colorectal carcinomas that metastasize to the livers but not to lymph nodes experience an upregulation of HULC ncRNA in all the samples tested (n=8), with a strong-to-moderate expression in six out of eight Moreover HULC is not expressed in the majority of carcinoma cell lines tested and also in samples of normal bladder and bladder cancers of various grades. We also show that HULC ncRNA is upregulated in two hepatocellular carcinoma cell lines producing HBV relevant to their parental lines that do not produce HBV. Conclusion Our results presented here indicate that HULC expression is not confined to HCC, but also to those colorectal carcinomas that metastasize to the liver.",

keywords = "Bladder carcinomas, Colorectal carcinomas, Highly upregulated in liver cancer, Liver metastasis, Liver microenvironment, Lymph nodes metastasis, Noncoding RNA, Primary and secondary growth, untranslated RNA, animal model, animal tissue, article, bladder, bladder cancer, bladder carcinoma, breast carcinoma, cancer cell culture, cancer staging, carcinoma cell, cell strain MCF 7, colon, colon carcinoma, colorectal cancer, colorectal carcinoma, disease severity, female, gene expression, gene overexpression, HeLa cell, Hepatitis B virus, highly upregulated in liver cancer gene, human, human cell, human tissue, liver cell, liver cell carcinoma, liver metastasis, lymph node metastasis, metastasis, mouse, nonhuman, ovary carcinoma, pancreas cancer, pancreas carcinoma, priority journal, quantitative analysis, rectum, reverse transcription polymerase chain reaction, sample, tumor gene, upregulation, Animals, Colorectal Neoplasms, Gene Expression Regulation, Neoplastic, Humans, Liver Neoplasms, Mice, Mice, Nude, Neoplasm Transplantation, Reverse Transcriptase Polymerase Chain Reaction, RNA, Neoplasm, RNA, Untranslated, Transplantation, Heterologous, Tumor Cells, Cultured, Up-Regulation",

author = "Matouk, {Imad J.} and Ibrahim Abbasi and Abraham Hochberg and Eithan Galun and Hassan Dweik and Mutaz Akkawi",

note = "Cited By :176 Export Date: 30 January 2023 CODEN: EJGHE Correspondence Address: Matouk, I. J.; Alquds And Hebrew Universities, , Jerusalem, Israel; email: imatook@cc.huji.ac.il Chemicals/CAS: RNA, Neoplasm; RNA, Untranslated References: Bartel, D.P., MicroRNAs: Genomics, biogenesis, mechanism and function (2004) Cell, 116, pp. 281-297; Zamore, P.D., Haley, B., Ribo-genome: The big world of small RNAs (2005) Science, 309, pp. 1519-1524; Volinia, S., Calin, G.A., Liu, C.G., Ambs, S., Cimmino, A., Petrocca, F., A microRNA expression signature of human solid tumors defines cancer gene targets (2006) Proc Natl Acad Sci USA, 103, pp. 2257-2261; He, L., Thomson, J.M., Hemann, M.T., Hernando-Monge, E., Mu, D., Goodson, S., A microRNA polycistron as a potential human oncogene (2005) Nature, 435, pp. 828-833; Matouk, U., DeGroot, N., Mezan, S., Ayesh, S., Abu-Lail, R., Hochberg, A., The H19 non-coding RNA is essential for human tumor growth (2007) PloS ONE, 2, pp. e845; Matouk, I., Ohana, P., Ayesh, S., Sidi, A., Czerniak, A., De Groot, N., The oncofetal H19 RNA in human cancer from the bench to the patient (2005) Cancer Ther, 3, pp. 249-266; Panzitt, K., Tschernatsch, M.M., Guelly, C., Moustafa, T., Stradner, M., Strohmaier, H.M., Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA (2007) Gastroenterology, 132, pp. 330-342; Kavolius, J., Fong, Y., Blumgart, L.H., Surgical resection of metastatic liver tumors (1996) Surg Oncol Clin, 5, pp. 337-352; Laurent-Puig, P., Zucman-Rossi, J., Genetics of hepatocellular tumors (2006) Oncogene, 25, pp. 3778-3786; Fellig, Y., Almogy, G., Galun, E., Ketzinel-Gilad, M., A hepatocellular carcinoma cell line producing mature hepatitis B viral particles (2004) Biochem Biophys Res Commun, 321, pp. 269-274; Odom, D.T., Dowell, R.D., Jacobsen, E.S., Gordon, W., Danford, T.W., Maclsaac, K.D., Tissue-specific transcriptional regulation has diverged significantly between human and mouse (2007) Wat Genet, 39, pp. 730-732",

year = "2009",

month = jun,

doi = "10.1097/MEG.0b013e328306a3a2",

language = "American English",

volume = "21",

pages = "688--692",

journal = "European Journal of Gastroenterology and Hepatology",

issn = "0954-691X",

publisher = "Lippincott Williams and Wilkins Ltd.",

number = "6",

}

TY - JOUR

T1 - Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis

AU - Matouk, Imad J.

AU - Abbasi, Ibrahim

AU - Hochberg, Abraham

AU - Galun, Eithan

AU - Dweik, Hassan

AU - Akkawi, Mutaz

N1 - Cited By :176 Export Date: 30 January 2023 CODEN: EJGHE Correspondence Address: Matouk, I. J.; Alquds And Hebrew Universities, , Jerusalem, Israel; email: imatook@cc.huji.ac.il Chemicals/CAS: RNA, Neoplasm; RNA, Untranslated References: Bartel, D.P., MicroRNAs: Genomics, biogenesis, mechanism and function (2004) Cell, 116, pp. 281-297; Zamore, P.D., Haley, B., Ribo-genome: The big world of small RNAs (2005) Science, 309, pp. 1519-1524; Volinia, S., Calin, G.A., Liu, C.G., Ambs, S., Cimmino, A., Petrocca, F., A microRNA expression signature of human solid tumors defines cancer gene targets (2006) Proc Natl Acad Sci USA, 103, pp. 2257-2261; He, L., Thomson, J.M., Hemann, M.T., Hernando-Monge, E., Mu, D., Goodson, S., A microRNA polycistron as a potential human oncogene (2005) Nature, 435, pp. 828-833; Matouk, U., DeGroot, N., Mezan, S., Ayesh, S., Abu-Lail, R., Hochberg, A., The H19 non-coding RNA is essential for human tumor growth (2007) PloS ONE, 2, pp. e845; Matouk, I., Ohana, P., Ayesh, S., Sidi, A., Czerniak, A., De Groot, N., The oncofetal H19 RNA in human cancer from the bench to the patient (2005) Cancer Ther, 3, pp. 249-266; Panzitt, K., Tschernatsch, M.M., Guelly, C., Moustafa, T., Stradner, M., Strohmaier, H.M., Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA (2007) Gastroenterology, 132, pp. 330-342; Kavolius, J., Fong, Y., Blumgart, L.H., Surgical resection of metastatic liver tumors (1996) Surg Oncol Clin, 5, pp. 337-352; Laurent-Puig, P., Zucman-Rossi, J., Genetics of hepatocellular tumors (2006) Oncogene, 25, pp. 3778-3786; Fellig, Y., Almogy, G., Galun, E., Ketzinel-Gilad, M., A hepatocellular carcinoma cell line producing mature hepatitis B viral particles (2004) Biochem Biophys Res Commun, 321, pp. 269-274; Odom, D.T., Dowell, R.D., Jacobsen, E.S., Gordon, W., Danford, T.W., Maclsaac, K.D., Tissue-specific transcriptional regulation has diverged significantly between human and mouse (2007) Wat Genet, 39, pp. 730-732

PY - 2009/6

Y1 - 2009/6

N2 - Background The highly upregulated in liver cancer (HULC) gene transcribes to an mRNA-like noncoding RNA (ncRNA) by the RNA polymerase II and processed by capping, splicing and polyadenylation. It is specifically expressed in the hepatocytes with striking upregulation in hepatocellular carcinoma (HCC). Objectives To study the expression levels of HULC in normal colorectal samples, primary colorectal carcinomas and in secondary tumors formed from colorectal carcinomas that metastasize to either the liver or the lymph nodes, taken from the same patients. Also a panel of carcinoma cell lines is tested for HULC expression. Basic methods Semiquantitative reverse transcriptase- PCR technique is used to detect for HULC expression in study specimens and cell lines. Results Consistent with the previous report, HULC is neither expressed in primary colorectal carcinomas samples nor in their normal counterparts. We show for the first time those colorectal carcinomas that metastasize to the livers but not to lymph nodes experience an upregulation of HULC ncRNA in all the samples tested (n=8), with a strong-to-moderate expression in six out of eight Moreover HULC is not expressed in the majority of carcinoma cell lines tested and also in samples of normal bladder and bladder cancers of various grades. We also show that HULC ncRNA is upregulated in two hepatocellular carcinoma cell lines producing HBV relevant to their parental lines that do not produce HBV. Conclusion Our results presented here indicate that HULC expression is not confined to HCC, but also to those colorectal carcinomas that metastasize to the liver.

AB - Background The highly upregulated in liver cancer (HULC) gene transcribes to an mRNA-like noncoding RNA (ncRNA) by the RNA polymerase II and processed by capping, splicing and polyadenylation. It is specifically expressed in the hepatocytes with striking upregulation in hepatocellular carcinoma (HCC). Objectives To study the expression levels of HULC in normal colorectal samples, primary colorectal carcinomas and in secondary tumors formed from colorectal carcinomas that metastasize to either the liver or the lymph nodes, taken from the same patients. Also a panel of carcinoma cell lines is tested for HULC expression. Basic methods Semiquantitative reverse transcriptase- PCR technique is used to detect for HULC expression in study specimens and cell lines. Results Consistent with the previous report, HULC is neither expressed in primary colorectal carcinomas samples nor in their normal counterparts. We show for the first time those colorectal carcinomas that metastasize to the livers but not to lymph nodes experience an upregulation of HULC ncRNA in all the samples tested (n=8), with a strong-to-moderate expression in six out of eight Moreover HULC is not expressed in the majority of carcinoma cell lines tested and also in samples of normal bladder and bladder cancers of various grades. We also show that HULC ncRNA is upregulated in two hepatocellular carcinoma cell lines producing HBV relevant to their parental lines that do not produce HBV. Conclusion Our results presented here indicate that HULC expression is not confined to HCC, but also to those colorectal carcinomas that metastasize to the liver.

KW - Bladder carcinomas

KW - Colorectal carcinomas

KW - Highly upregulated in liver cancer

KW - Liver metastasis

KW - Liver microenvironment

KW - Lymph nodes metastasis

KW - Noncoding RNA

KW - Primary and secondary growth

KW - untranslated RNA

KW - animal model

KW - animal tissue

KW - article

KW - bladder

KW - bladder cancer

KW - bladder carcinoma

KW - breast carcinoma

KW - cancer cell culture

KW - cancer staging

KW - carcinoma cell

KW - cell strain MCF 7

KW - colon

KW - colon carcinoma

KW - colorectal cancer

KW - colorectal carcinoma

KW - disease severity

KW - female

KW - gene expression

KW - gene overexpression

KW - HeLa cell

KW - Hepatitis B virus

KW - highly upregulated in liver cancer gene

KW - human

KW - human cell

KW - human tissue

KW - liver cell

KW - liver cell carcinoma

KW - liver metastasis

KW - lymph node metastasis

KW - metastasis

KW - mouse

KW - nonhuman

KW - ovary carcinoma

KW - pancreas cancer

KW - pancreas carcinoma

KW - priority journal

KW - quantitative analysis

KW - rectum

KW - reverse transcription polymerase chain reaction

KW - sample

KW - tumor gene

KW - upregulation

KW - Animals

KW - Colorectal Neoplasms

KW - Gene Expression Regulation, Neoplastic

KW - Humans

KW - Liver Neoplasms

KW - Mice

KW - Mice, Nude

KW - Neoplasm Transplantation

KW - Reverse Transcriptase Polymerase Chain Reaction

KW - RNA, Neoplasm

KW - RNA, Untranslated

KW - Transplantation, Heterologous

KW - Tumor Cells, Cultured

KW - Up-Regulation

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U2 - 10.1097/MEG.0b013e328306a3a2

DO - 10.1097/MEG.0b013e328306a3a2

M3 - Article

C2 - 19445043

AN - SCOPUS:67649664083

SN - 0954-691X

VL - 21

SP - 688

EP - 692

JO - European Journal of Gastroenterology and Hepatology

JF - European Journal of Gastroenterology and Hepatology

IS - 6

ER -

Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis

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Bibliographical note

Keywords

UN SDGs

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