GABAergic signaling facilitates breast cancer metastasis by promoting ERK1/2-dependent phosphorylation

Cancer Letters

Volumn 348, Issue 1-2, 2014, Pages 100-108

  Zhang, Depu ^a   Li, Xiaowei ^a   Yao, Ziming ^a   Wei, Chuanfei ^a   Ning, Nannan ^a   Li, Jingxin ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

Breast cancer; ERK; GABA receptor; Metastasis; Aminobutyric acid

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR; BACLOFEN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

4T1 CELL LINE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL LINE; CANCER TISSUE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; GABAERGIC SYSTEM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MCF 7 CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; WESTERN BLOTTING;

BREAST CANCER; ERK; GABA RECEPTOR; METASTASIS; Γ-AMINOBUTYRIC ACID;

ANIMALS; BREAST NEOPLASMS; CELL MOVEMENT; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GABA-B RECEPTOR AGONISTS; GABA-B RECEPTOR ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 2; MCF-7 CELLS; MICE; MICE, INBRED BALB C; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM INVASIVENESS; PHOSPHORYLATION; RECEPTORS, GABA-B; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84900521298     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.03.006     Document Type: Article

References (36)

1. Forouzanfar M.H., Foreman K.J., Delossantos A.M., Lozano R., Lopez A.D., Murray C.J., Naghavi M. Breast and cervical cancer in 187 countries between 1980 and 2010: a systematic analysis. Lancet 2011, 378:1461-1484.
2. Kittler J.T., Moss S.J. Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr. Opin. Neurobiol. 2003, 13:341-347.
3. Akinci M.K., Schofield P.R. Widespread expression of GABA(A) receptor subunits in peripheral tissues. Neurosci. Res. 1999, 35:145-153.
4. Young S.Z., Bordey A. GABA's control of stem and cancer cell proliferation in adult neural and peripheral niches. Physiology (Bethesda) 2009, 24:171-185.
5. Xiang Y.Y., Wang S., Liu M., Hirota J.A., Li J., Ju W., Fan Y., Kelly M.M., Ye B., Orser B., O'Byrne P.M., Inman M.D., Yang X., Lu W.Y. A GABAergic system in airway epithelium is essential for mucus overproduction in asthma. Nat. Med. 2007, 13:862-867.
6. Li Y., Xiang Y.Y., Lu W.Y., Liu C., Li J. A novel role of intestine epithelial GABAergic signaling in regulating intestinal fluid secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 303:G453-460.
7. Zhou Z., Sun H., Li X., Li Y., Zhao S., Zhang D., Yao Z., Li J. A local GABAergic system is functionally expressed in human fallopian tube. Biochem. Biophys. Res. Commun. 2010, 398:237-241.
8. Watanabe M., Maemura K., Oki K., Shiraishi N., Shibayama Y., Katsu K. Gamma-aminobutyric acid (GABA) and cell proliferation: focus on cancer cells. Histol. Histopathol. 2006, 21:1135-1141.
9. Mazurkiewicz M., Opolski A., Wietrzyk J., Radzikowski C., Kleinrok Z. GABA level and GAD activity in human and mouse normal and neoplastic mammary gland. J. Exp. Clin. Cancer Res. 1999, 18:247-253.
10. Maemura K., Yamauchi H., Hayasaki H., Kanbara K., Tamayama T., Hirata I., Watanabe M. Gamma-amino-butyric acid immunoreactivity in intramucosal colonic tumors. J. Gastroenterol. Hepatol. 2003, 18:1089-1094.
11. Matuszek M., Jesipowicz M., Kleinrok Z. GABA content and GAD activity in gastric cancer. Med. Sci. Monit. 2001, 7:377-381.
12. Roberts S.S., Mendonca-Torres M.C., Jensen K., Francis G.L., Vasko V. GABA receptor expression in benign and malignant thyroid tumors. Pathol. Oncol. Res. 2009, 15:645-650.
13. Nicholson-Guthrie C.S., Guthrie G.D., Sutton G.P., Baenziger J.C. Urine GABA levels in ovarian cancer patients: elevated GABA in malignancy. Cancer Lett. 2001, 162:27-30.
14. Im B.H., Rhim H. GABA(B) receptor-mediated ERK1/2 phosphorylation via a direct interaction with Ca(V)1.3 channels. Neurosci. Lett. 2012, 513:89-94.
15. Tu H., Rondard P., Xu C., Bertaso F., Cao F., Zhang X., Pin J.P., Liu J. Dominant role of GABAB2 and Gbetagamma for GABAB receptor-mediated-ERK1/2/CREB pathway in cerebellar neurons. Cell Signal 2007, 19:1996-2002.
16. Roehrborn C.G., Sech S., Montoya J., Rhodes T., Girman C.J. Interexaminer reliability and validity of a three-dimensional model to assess prostate volume by digital rectal examination. Urology 2001, 57:1087-1092.
17. Schuller H.M., Al-Wadei H.A., Majidi M. GABA B receptor is a novel drug target for pancreatic cancer. Cancer 2008, 112:767-778.
18. Schuller H.M., Al-Wadei H.A., Majidi M. Gamma-aminobutyric acid, a potential tumor suppressor for small airway-derived lung adenocarcinoma. Carcinogenesis 2008, 29:1979-1985.
19. Joseph J., Niggemann B., Zaenker K.S., Entschladen F. The neurotransmitter gamma-aminobutyric acid is an inhibitory regulator for the migration of SW 480 colon carcinoma cells. Cancer Res. 2002, 62:6467-6469.
20. Szczaurska K., Mazurkiewicz M., Opolski A. The role of GABA-ergic system in carcinogenesis. Postepy Hig. Med. Dosw. 2003, 57:485-500.
21. Azuma H., Inamoto T., Sakamoto T., Kiyama S., Ubai T., Shinohara Y., Maemura K., Tsuji M., Segawa N., Masuda H., Takahara K., Katsuoka Y., Watanabe M. Gamma-aminobutyric acid as a promoting factor of cancer metastasis; induction of matrix metalloproteinase production is potentially its underlying mechanism. Cancer Res. 2003, 63:8090-8096.
22. Inamoto T., Azuma H., Sakamoto T., Kiyama S., Ubai T., Kotake Y., Watanabe M., Katsuoka Y. Invasive ability of human renal cell carcinoma cell line Caki-2 is accelerated by gamma-aminobutyric acid, via sustained activation of ERK1/2 inducible matrix metalloproteinases. Cancer Invest. 2007, 25:574-583.
23. Takehara A., Hosokawa M., Eguchi H., Ohigashi H., Ishikawa O., Nakamura Y., Nakagawa H. Gamma-aminobutyric acid (GABA) stimulates pancreatic cancer growth through overexpressing GABAA receptor pi subunit. Cancer Res. 2007, 67:9704-9712.
24. Kim H.A., Kim K.J., Seo K.H., Lee H.K., Im S.Y. PTEN/MAPK pathways play a key role in platelet-activating factor-induced experimental pulmonary tumor metastasis. FEBS Lett. 2012, 586:4296-4302.
25. Chetram M.A., Hinton C.V. PTEN regulation of ERK1/2 signaling in cancer. J. Recept. Signal Transduct. Res. 2012, 32:190-195.
26. Rubinfeld H., Shimon I. PI3K/Akt/mTOR and Raf/MEK/ERK signaling pathways perturbations in non-functioning pituitary adenomas. Endocrine 2012, 42:285-291.
27. Kohno M., Pouyssegur J. Targeting the ERK signaling pathway in cancer therapy. Ann. Med. 2006, 38:200-211.
28. Vanhoose A.M., Emery M., Jimenez L., Winder D.G. ERK activation by G-protein-coupled receptors in mouse brain is receptor identity-specific. J. Biol. Chem. 2002, 277:9049-9053.
29. Ahn S., Shenoy S.K., Wei H., Lefkowitz R.J. Differential kinetic and spatial patterns of beta-arrestin and G protein-mediated ERK activation by the angiotensin II receptor. J. Biol. Chem. 2004, 279:35518-35525.
30. Fava G., Marucci L., Glaser S., Francis H., De Morrow S., Benedetti A., Alvaro D., Venter J., Meininger C., Patel T., Taffetani S., Marzioni M., Summers R., Reichenbach R., Alpini G. Gamma-aminobutyric acid inhibits cholangiocarcinoma growth by cyclic AMP-dependent regulation of the protein kinase A/extracellular signal-regulated kinase 1/2 pathway. Cancer Res. 2005, 65:11437-11446.
31. Liotta L.A., Tryggvason K., Garbisa S., Hart I., Foltz C.M., Shafie S. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 1980, 284:67-68.
32. Garbisa S., Pozzatti R., Muschel R.J., Saffiotti U., Ballin M., Goldfarb R.H., Khoury G., Liotta L.A. Secretion of type IV collagenolytic protease and metastatic phenotype: induction by transfection with c-Ha-ras but not c-Ha-ras plus Ad2-E1a. Cancer Res. 1987, 47:1523-1528.
33. Nakajima M., Welch D.R., Belloni P.N., Nicolson G.L. Degradation of basement membrane type IV collagen and lung subendothelial matrix by rat mammary adenocarcinoma cell clones of differing metastatic potentials. Cancer Res. 1987, 47:4869-4876.
34. Talvensaari-Mattila A., Paakko P., Hoyhtya M., Blanco-Sequeiros G., Turpeenniemi-Hujanen T. Matrix metalloproteinase-2 immunoreactive protein: a marker of aggressiveness in breast carcinoma. Cancer 1998, 83:1153-1162.
35. Talvensaari-Mattila A., Paakko P., Turpeenniemi-Hujanen T. Matrix metalloproteinase-2 (MMP-2) is associated with survival in breast carcinoma. Br. J. Cancer 2003, 89:1270-1275.
36. Leppa S., Saarto T., Vehmanen L., Blomqvist C., Elomaa I. A high serum matrix metalloproteinase-2 level is associated with an adverse prognosis in node-positive breast carcinoma. Clin. Cancer Res. 2004, 10:1057-1063.