2,014
Views
10
CrossRef citations to date
0
Altmetric
Research paper

Silencing the intestinal GUCY2C tumor suppressor axis requires APC loss of heterozygosity

, , , , , ORCID Icon & show all
Pages 799-805 | Received 08 Apr 2020, Accepted 31 May 2020, Published online: 28 Jun 2020

References

  • Siegel RL, SaHSRACSA G, Miller KD, SaHSRACSA G, Jemal A, SaHSRACSA G. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7–30. doi:10.3322/caac.21590.
  • Powell SM, Zilz N, Beazer-Barclay Y, Bryan TM, Hamilton SR, Thibodeau SN, Vogelstein B, Kinzler KW. Apc mutations occur early during colorectal tumorigenesis. Nature. 1992;359:235–237. doi:10.1038/359235a0.
  • Fodde R, Smits R, Clevers H. Apc, signal transduction and genetic instability in colorectal cancer. Nat Rev Cancer. 2001;1:55–67. doi:10.1038/35094067.
  • Miyoshi Y, Ando H, Nagase H, Nishisho I, Horii A, Miki Y, Mori T, Utsunomiya J, Baba S, Petersen G, et al. Germ-line mutations of the apc gene in 53 familial adenomatous polyposis patients. Proc Nat Acad Sci. 1992;89:4452. doi:10.1073/pnas.89.10.4452.
  • Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol. 2011;6:479–507. doi:10.1146/annurev-pathol-011110-130235.
  • Yamada Y, Hata K, Hirose Y, Hara A, Sugie S, Kuno T, Yoshimi N, Tanaka T, Mori H. Microadenomatous lesions involving loss of apc heterozygosity in the colon of adult apc(min/+) mice. Cancer Res. 2002;62:6367–6370.
  • Sameer AS. Colorectal cancer: molecular mutations and polymorphisms. Front Oncol. 2013;3:114. doi:10.3389/fonc.2013.00114.
  • Miyoshi Y, Nagase H, Ando H, Horii A, Ichii S, Nakatsuru S, Aoki T, Miki Y, Mori T, Nakamura Y, et al. Somatic mutations of the APC gene in colorectal tumors: mutation cluster region in the APC gene. Hum Mol Genet. 1992;1:229–233. doi:10.1093/hmg/1.4.229.
  • Miyaki M, Iijima T, Kimura J, Yasuno M, Mori T, Hayashi Y, Koike M, Shitara N, Iwama T, Kuroki T. Frequent mutation of beta-catenin and apc genes in primary colorectal tumors from patients with hereditary nonpolyposis colorectal cancer. Cancer Res. 1999;59:4506.
  • Nieuwenhuis MH, Vasen HFA. Correlations between mutation site in apc and phenotype of familial adenomatous polyposis (fap): A review of the literature. Crit Rev Oncol Hematol. 2007;61:153–161. doi:10.1016/j.critrevonc.2006.07.004.
  • Corley DA, Jensen CD, Marks AR, Zhao WK, Lee JK, Doubeni CA, Zauber AG, de Boer J, Fireman BH, Schottinger JE, et al. Adenoma detection rate and risk of colorectal cancer and death. N Engl J Med. 2014;370:1298–1306. doi:10.1056/NEJMoa1309086.
  • Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. Activation of beta-catenin-tcf signaling in colon cancer by mutations in beta-catenin or apc. Science. 1997;275:1787–1790. doi:10.1126/science.275.5307.1787.
  • Sparks AB, Morin PJ, Vogelstein B, Kinzler KW. Mutational analysis of the apc/β-catenin/tcf pathway in colorectal cancer. Cancer Res. 1998;58:1130.
  • Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B, Clevers H. Constitutive transcriptional activation by a beta-catenin-tcf complex in apc-/- colon carcinoma. Science. 1997;275:1784–1787. doi:10.1126/science.275.5307.1784.
  • Clevers H, Nusse R. Wnt/beta-catenin signaling and disease. Cell. 2012;149:1192–1205. doi:10.1016/j.cell.2012.05.012.
  • Arshad N, Visweswariah SS. The multiple and enigmatic roles of guanylyl cyclase c in intestinal homeostasis. FEBS Lett. 2012;586:2835–2840. doi:10.1016/j.febslet.2012.07.028.
  • Lin JE, Li P, Snook AE, Schulz S, Dasgupta A, Hyslop TM, Gibbons AV, Marszlowicz G, Pitari GM, Waldman SA, et al. The hormone receptor gucy2c suppresses intestinal tumor formation by inhibiting akt signaling. Gastroenterology. 2010;138:241–254. doi:10.1053/j.gastro.2009.08.064.
  • Li P, Lin JE, Chervoneva I, Schulz S, Waldman SA, Pitari GM. Homeostatic control of the crypt-villus axis by the bacterial enterotoxin receptor guanylyl cyclase c restricts the proliferating compartment in intestine. Am J Pathol. 2007;171:1847–1858. doi:10.2353/ajpath.2007.070198.
  • Li P, Schulz S, Bombonati A, Palazzo JP, Hyslop TM, Xu Y, Baran AA, Siracusa LD, Pitari GM, Waldman SA, et al. Guanylyl cyclase c suppresses intestinal tumorigenesis by restricting proliferation and maintaining genomic integrity. Gastroenterology. 2007;133(2):599–607. doi:10.1053/j.gastro.2007.05.052.
  • Lin JE, Snook AE, Li P, Stoecker BA, Kim GW, Magee MS, Garcia AVM, Valentino MA, Hyslop T, Schulz S, et al. Gucy2c opposes systemic genotoxic tumorigenesis by regulating akt-dependent intestinal barrier integrity. PLoS One. 2012;7(2):e31686. doi:10.1371/journal.pone.0031686.
  • Gibbons AV, Lin JE, Kim GW, Marszalowicz GP, Li P, Stoecker BA, Blomain ES, Rattan S, Snook AE, Schulz S, et al. Intestinal GUCY2C prevents TGF-β secretion coordinating desmoplasia and hyperproliferation in colorectal cancer. Cancer Res. 2013;73(22):6654–6666. doi:10.1158/0008-5472.CAN-13-0887.
  • Brenna O, Furnes MW, Munkvold B, Kidd M, Sandvik AK, Gustafsson BI. Cellular localization of guanylin and uroguanylin mrnas in human and rat duodenal and colonic mucosa. Cell Tissue Res. 2016;365(2):331–341. doi:10.1007/s00441-016-2393-y.
  • Ikpa PT, Sleddens HF, Steinbrecher KA, Peppelenbosch MP, de Jonge HR, Smits R, Bijvelds MJC. Guanylin and uroguanylin are produced by mouse intestinal epithelial cells of columnar and secretory lineage. Histochem Cell Biol. 2016;146(4):445–455. doi:10.1007/s00418-016-1453-4.
  • Whitaker TL, Witte DP, Scott MC, Cohen MB. Uroguanylin and guanylin: distinct but overlapping patterns of messenger rna expression in mouse intestine. Gastroenterology. 1997;113:1000–1006. doi:10.1016/S0016-5085(97)70197-5.
  • Vaandrager AB. Structure and function of the heat-stable enterotoxin receptor/guanylyl cyclase c. Mol Cell Biochem. 2002;230:73–83. doi:10.1023/A:1014231722696.
  • Kuhn M. Molecular physiology of membrane guanylyl cyclase receptors. Physiol Rev. 2016;96:751–804. doi:10.1152/physrev.00022.2015.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–674. doi:10.1016/j.cell.2011.02.013.
  • Li P, Lin JE, Snook AE, Waldman SA. St-producing e. Coli oppose carcinogen-induced colorectal tumorigenesis in mice. Toxins (Basel). 2017;9:279. doi:10.3390/toxins9090279.
  • Shailubhai K, Yu HH, Karunanandaa K, Wang JY, Eber SL, Wang Y, Joo NS, Kim HD, Miedema BW, Abbas SZ, et al. Uroguanylin treatment suppresses polyp formation in the apc(min/+) mouse and induces apoptosis in human colon adenocarcinoma cells via cyclic gmp. Cancer Res. 2000;60:5151–5157.
  • Sharman SK, Islam BN, Hou Y, Singh N, Berger FG, Sridhar S, Yoo W, Browning DD. Cyclic-GMP–Elevating agents suppress polyposis in Apc min mice by targeting the preneoplastic epithelium. Cancer Prev Res (Phila). 2018;11:81–92. doi:10.1158/1940-6207.CAPR-17-0267.
  • Steinbrecher KA, Tuohy TM, Heppner Goss K, Scott MC, Witte DP, Groden J, Cohen MB. Expression of guanylin is downregulated in mouse and human intestinal adenomas. Biochem Biophys Res Commun. 2000;273(1):225–230. doi:10.1006/bbrc.2000.2917.
  • Wilson C, Lin JE, Li P, Snook AE, Gong J, Sato T, Liu C, Girondo MA, Rui H, Hyslop T, et al. The paracrine hormone for the gucy2c tumor suppressor, guanylin, is universally lost in colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2014;23(11):2328–2337. doi:10.1158/1055-9965.EPI-14-0440.
  • Bashir B, Merlino DJ, Rappaport JA, Gnass E, Palazzo JP, Feng Y, Fearon ER, Snook AE, Waldman SA. Silencing the guca2a-gucy2c tumor suppressor axis in cin, serrated, and msi colorectal neoplasia. Hum Pathol. 2019;87:103–114. doi:10.1016/j.humpath.2018.11.032.
  • Blomain ES, Rappaport JA, Pattison AM, Bashir B, Caparosa E, Stem J, Snook AE, Waldman SA. Apc-β-catenin-tcf signaling silences the intestinal guanylin-gucy2c tumor suppressor axis. Cancer Biol Ther. 2020;21(5):441–451. doi:10.1080/15384047.2020.1721262.
  • Carrithers SL, Barber MT, Biswas S, Parkinson SJ, Park PK, Goldstein SD, Waldman SA. Guanylyl cyclase c is a selective marker for metastatic colorectal tumors in human extraintestinal tissues. Proc Natl Acad Sci U S A. 1996;93(25):14827–14832. doi:10.1073/pnas.93.25.14827.
  • Carrithers SL, Parkinson SJ, Goldstein S, Park P, Robertson DC, Waldman SA. Escherichia coli heat-stable toxin receptors in human colonic tumors. Gastroenterology. 1994;107:1653–1661. doi:10.1016/0016-5085(94)90804-4.
  • Danaee H, Kalebic T, Wyant T, Fassan M, Mescoli C, Gao F, Trepicchio WL, Rugge M. Consistent expression of guanylyl cyclase-c in primary and metastatic gastrointestinal cancers. PLoS One. 2017;12:e0189953. doi:10.1371/journal.pone.0189953.
  • Cancer Genome Atlas N. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487:330–337. doi:10.1038/nature11252.
  • Darwich AS, Aslam U, Ashcroft DM, Rostami-Hodjegan A. Meta-analysis of the turnover of intestinal epithelia in preclinical animal species and humans. Drug Metab Dispos. 2014;42:2016. doi:10.1124/dmd.114.058404.
  • Barker N. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat Rev Mol Cell Biol. 2014;15:19–33. doi:10.1038/nrm3721.
  • Creamer B, Shorter RG, Bamforth J. The turnover and shedding of epithelial cells. I. The turnover in the gastro-intestinal tract. Gut. 1961;2:110–118. doi:10.1136/gut.2.2.110.
  • Li P, Waldman SA. Corruption of homeostatic mechanisms in the guanylyl cyclase c signaling pathway underlying colorectal tumorigenesis. Cancer Biol Ther. 2010;10:211–218. doi:10.4161/cbt.10.3.12539.
  • Vermeulen L, Snippert HJ. Stem cell dynamics in homeostasis and cancer of the intestine. Nat Rev Cancer. 2014;14:468–480. doi:10.1038/nrc3744.
  • Steinbrecher KA, Harmel-Laws E, Garin-Laflam MP, Mann EA, Bezerra LD, Hogan SP, Cohen MB. Murine guanylate cyclase c regulates colonic injury and inflammation. J Immunol. 2011;186:7205–7214. doi:10.4049/jimmunol.1002469.
  • Brierley SM. Guanylate cyclase-c receptor activation: unexpected biology. Curr Opin Pharmacol. 2012;12:632–640. doi:10.1016/j.coph.2012.10.005.
  • Lan D, Niu J, Miao J, Dong X, Wang H, Yang G, Wang K, Miao Y. Expression of guanylate cyclase-c, guanylin, and uroguanylin is downregulated proportionally to the ulcerative colitis disease activity index. Sci Rep. 2016;6:25034. doi:10.1038/srep25034.
  • Lin JE, Colon-Gonzalez F, Blomain E, Kim GW, Aing A, Stoecker B, Rock J, Snook AE, Zhan T, Hyslop TM, et al. Obesity-induced colorectal cancer is driven by caloric silencing of the guanylin-gucy2c paracrine signaling axis. Cancer Res. 2016;76:339–346. doi:10.1158/0008-5472.CAN-15-1467-T.
  • Chang WL, Masih S, Thadi A, Patwa V, Joshi A, Cooper HS, Palejwala VA, Clapper ML, Shailubhai K. Plecanatide-mediated activation of guanylate cyclase-C suppresses inflammation-induced colorectal carcinogenesis in Apc +/Min-FCCC mice. World J Gastrointest Pharmacol Ther. 2017;8:47–59. doi:10.4292/wjgpt.v8.i1.47.
  • El Marjou F, Janssen KP, Chang BH, Li M, Hindie V, Chan L, Louvard D, Chambon P, Metzger D, Robine S, et al. Tissue-specific and inducible cre-mediated recombination in the gut epithelium. Genesis. 2004;39:186–193. doi:10.1002/gene.20042.
  • Schulz S, Lopez MJ, Kuhn M, Garbers DL. Disruption of the guanylyl cyclase-c gene leads to a paradoxical phenotype of viable but heat-stable enterotoxin-resistant mice. J Clin Invest. 1997;100:1590–1595. doi:10.1172/JCI119683.
  • Qian X, Prabhakar S, Nandi A, Visweswariah SS, Goy MF. Expression of gc-c, a receptor-guanylate cyclase, and its endogenous ligands uroguanylin and guanylin along the rostrocaudal axis of the intestine*. Endocrinology. 2000;141:3210–3224. doi:10.1210/endo.141.9.7644.