WISP genes are members of the connective tissue growth factor family that are up-regulated in Wnt-1-transformed cells and aberrantly expressed in human colon tumors

Diane Pennica, Todd Swanson, James W. Welsh, Margaret A. Roy, David A. Lawrence, James Lee, Jennifer Brush, Lisa A. Taneyhill, Bethanne Deuel, Michael Lew, Colin Watanabe, Robert L. Cohen, Mona F. Melhem, Gene G. Finley, Phil Quirke, Audrey D. Goddard, Kenneth J. Hillan, Austin L. Gurney, David Botstein, Arnold J. Levine

Research output: Contribution to journalArticle

422 Citations (Scopus)

Abstract

Wnt family members are critical to many developmental processes, and components of the Wnt signaling pathway have been linked to tumorigenesis in familial and sporadic colon carcinomas. Here we report the identification of two genes, WISP-1 and WISP-2, that are up-regulated in the mouse mammary epithelial cell line C57MG transformed by Wnt-1, but not by Wnt-4. Together with a third related gene, WISP-3, these proteins define a subfamily of the connective tissue growth factor family. Two distinct systems demonstrated WISP induction to be associated with the expression of Wnt-1. These included (i) C57MG cells infected with a Wnt-1 retroviral vector or expressing Wnt-1 under the control of a tetracyline repressible promoter, and (ii) Wnt-1 transgenic mice. The WISP-1 gene was localized to human chromosome 8q24.1- 8q24.3. WISP-1 genomic DNA was amplified in colon cancer cell lines and in human colon tumors and its RNA overexpressed (2- to >30-fold) in 84% of the tumors examined compared with patient-matched normal mucosa. WISP-3 mapped to chromosome 6q22-6q23 and also was overexpressed (4- to >40-fold) in 63% of the colon tumors analyzed. In contrast, WISP-2 mapped to human chromosome 20q1220q13 and its DNA was amplified, but RNA expression was reduced (2- to >30-fold) in 79% of the tumors. These results suggest that the WISP genes may be downstream of Wnt-1 signaling and that aberrant levels of WISP expression in colon cancer may play a role in colon tumorigenesis.

Original languageEnglish (US)
Pages (from-to)14717-14722
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume95
Issue number25
DOIs
StatePublished - Dec 8 1998
Externally publishedYes

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Connective Tissue Growth Factor
Colon
Human Chromosomes
Colonic Neoplasms
Genes
Neoplasms
Carcinogenesis
RNA
Cell Line
Wnt Signaling Pathway
DNA
Transgenic Mice
Mucous Membrane
Breast
Chromosomes
Epithelial Cells
Carcinoma
Proteins

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

WISP genes are members of the connective tissue growth factor family that are up-regulated in Wnt-1-transformed cells and aberrantly expressed in human colon tumors. / Pennica, Diane; Swanson, Todd; Welsh, James W.; Roy, Margaret A.; Lawrence, David A.; Lee, James; Brush, Jennifer; Taneyhill, Lisa A.; Deuel, Bethanne; Lew, Michael; Watanabe, Colin; Cohen, Robert L.; Melhem, Mona F.; Finley, Gene G.; Quirke, Phil; Goddard, Audrey D.; Hillan, Kenneth J.; Gurney, Austin L.; Botstein, David; Levine, Arnold J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 95, No. 25, 08.12.1998, p. 14717-14722.

Research output: Contribution to journalArticle

Pennica, D, Swanson, T, Welsh, JW, Roy, MA, Lawrence, DA, Lee, J, Brush, J, Taneyhill, LA, Deuel, B, Lew, M, Watanabe, C, Cohen, RL, Melhem, MF, Finley, GG, Quirke, P, Goddard, AD, Hillan, KJ, Gurney, AL, Botstein, D & Levine, AJ 1998, 'WISP genes are members of the connective tissue growth factor family that are up-regulated in Wnt-1-transformed cells and aberrantly expressed in human colon tumors', Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 25, pp. 14717-14722. https://doi.org/10.1073/pnas.95.25.14717
Pennica, Diane ; Swanson, Todd ; Welsh, James W. ; Roy, Margaret A. ; Lawrence, David A. ; Lee, James ; Brush, Jennifer ; Taneyhill, Lisa A. ; Deuel, Bethanne ; Lew, Michael ; Watanabe, Colin ; Cohen, Robert L. ; Melhem, Mona F. ; Finley, Gene G. ; Quirke, Phil ; Goddard, Audrey D. ; Hillan, Kenneth J. ; Gurney, Austin L. ; Botstein, David ; Levine, Arnold J. / WISP genes are members of the connective tissue growth factor family that are up-regulated in Wnt-1-transformed cells and aberrantly expressed in human colon tumors. In: Proceedings of the National Academy of Sciences of the United States of America. 1998 ; Vol. 95, No. 25. pp. 14717-14722.
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title = "WISP genes are members of the connective tissue growth factor family that are up-regulated in Wnt-1-transformed cells and aberrantly expressed in human colon tumors",
abstract = "Wnt family members are critical to many developmental processes, and components of the Wnt signaling pathway have been linked to tumorigenesis in familial and sporadic colon carcinomas. Here we report the identification of two genes, WISP-1 and WISP-2, that are up-regulated in the mouse mammary epithelial cell line C57MG transformed by Wnt-1, but not by Wnt-4. Together with a third related gene, WISP-3, these proteins define a subfamily of the connective tissue growth factor family. Two distinct systems demonstrated WISP induction to be associated with the expression of Wnt-1. These included (i) C57MG cells infected with a Wnt-1 retroviral vector or expressing Wnt-1 under the control of a tetracyline repressible promoter, and (ii) Wnt-1 transgenic mice. The WISP-1 gene was localized to human chromosome 8q24.1- 8q24.3. WISP-1 genomic DNA was amplified in colon cancer cell lines and in human colon tumors and its RNA overexpressed (2- to >30-fold) in 84{\%} of the tumors examined compared with patient-matched normal mucosa. WISP-3 mapped to chromosome 6q22-6q23 and also was overexpressed (4- to >40-fold) in 63{\%} of the colon tumors analyzed. In contrast, WISP-2 mapped to human chromosome 20q1220q13 and its DNA was amplified, but RNA expression was reduced (2- to >30-fold) in 79{\%} of the tumors. These results suggest that the WISP genes may be downstream of Wnt-1 signaling and that aberrant levels of WISP expression in colon cancer may play a role in colon tumorigenesis.",
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AU - Pennica, Diane

AU - Swanson, Todd

AU - Welsh, James W.

AU - Roy, Margaret A.

AU - Lawrence, David A.

AU - Lee, James

AU - Brush, Jennifer

AU - Taneyhill, Lisa A.

AU - Deuel, Bethanne

AU - Lew, Michael

AU - Watanabe, Colin

AU - Cohen, Robert L.

AU - Melhem, Mona F.

AU - Finley, Gene G.

AU - Quirke, Phil

AU - Goddard, Audrey D.

AU - Hillan, Kenneth J.

AU - Gurney, Austin L.

AU - Botstein, David

AU - Levine, Arnold J.

PY - 1998/12/8

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N2 - Wnt family members are critical to many developmental processes, and components of the Wnt signaling pathway have been linked to tumorigenesis in familial and sporadic colon carcinomas. Here we report the identification of two genes, WISP-1 and WISP-2, that are up-regulated in the mouse mammary epithelial cell line C57MG transformed by Wnt-1, but not by Wnt-4. Together with a third related gene, WISP-3, these proteins define a subfamily of the connective tissue growth factor family. Two distinct systems demonstrated WISP induction to be associated with the expression of Wnt-1. These included (i) C57MG cells infected with a Wnt-1 retroviral vector or expressing Wnt-1 under the control of a tetracyline repressible promoter, and (ii) Wnt-1 transgenic mice. The WISP-1 gene was localized to human chromosome 8q24.1- 8q24.3. WISP-1 genomic DNA was amplified in colon cancer cell lines and in human colon tumors and its RNA overexpressed (2- to >30-fold) in 84% of the tumors examined compared with patient-matched normal mucosa. WISP-3 mapped to chromosome 6q22-6q23 and also was overexpressed (4- to >40-fold) in 63% of the colon tumors analyzed. In contrast, WISP-2 mapped to human chromosome 20q1220q13 and its DNA was amplified, but RNA expression was reduced (2- to >30-fold) in 79% of the tumors. These results suggest that the WISP genes may be downstream of Wnt-1 signaling and that aberrant levels of WISP expression in colon cancer may play a role in colon tumorigenesis.

AB - Wnt family members are critical to many developmental processes, and components of the Wnt signaling pathway have been linked to tumorigenesis in familial and sporadic colon carcinomas. Here we report the identification of two genes, WISP-1 and WISP-2, that are up-regulated in the mouse mammary epithelial cell line C57MG transformed by Wnt-1, but not by Wnt-4. Together with a third related gene, WISP-3, these proteins define a subfamily of the connective tissue growth factor family. Two distinct systems demonstrated WISP induction to be associated with the expression of Wnt-1. These included (i) C57MG cells infected with a Wnt-1 retroviral vector or expressing Wnt-1 under the control of a tetracyline repressible promoter, and (ii) Wnt-1 transgenic mice. The WISP-1 gene was localized to human chromosome 8q24.1- 8q24.3. WISP-1 genomic DNA was amplified in colon cancer cell lines and in human colon tumors and its RNA overexpressed (2- to >30-fold) in 84% of the tumors examined compared with patient-matched normal mucosa. WISP-3 mapped to chromosome 6q22-6q23 and also was overexpressed (4- to >40-fold) in 63% of the colon tumors analyzed. In contrast, WISP-2 mapped to human chromosome 20q1220q13 and its DNA was amplified, but RNA expression was reduced (2- to >30-fold) in 79% of the tumors. These results suggest that the WISP genes may be downstream of Wnt-1 signaling and that aberrant levels of WISP expression in colon cancer may play a role in colon tumorigenesis.

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