Gastrokines: Stomach-specific proteins with putative homeostatic and tumor suppressor roles

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 2, 2013, Pages

  Menheniott, Trevelyan R ^a   Kurklu, Bayzar ^a   Giraud, Andrew S ^a  

^a ROYAL CHILDREN'S HOSPITAL   (Australia)

Author keywords

BRICHOS; Gastric cancer; Gastrokine; Helicobacter pylori; Trefoil factor

Indexed keywords

BETA DEFENSIN; GASTROKINE; GASTROKINE 1; GASTROKINE 2; GASTROKINE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; INTESTINAL TREFOIL FACTOR; SURFACTANT PROTEIN C; TUMOR NECROSIS FACTOR ALPHA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANTIPROLIFERATIVE ACTIVITY; BARRETT ESOPHAGUS; CANCER INHIBITION; CANCER INVASION; CARCINOGENESIS; CELL MIGRATION; CROHN DISEASE; CYTOPLASM; DISULFIDE BOND; DOWN REGULATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; EXON; GENE INACTIVATION; GENE LOCUS; GLYCOSYLATION; HELICOBACTER INFECTION; HETEROZYGOSITY LOSS; HOMEOSTASIS; HOMOZYGOSITY; HUMAN; NONHUMAN; OVARY TUMOR; PRECANCER; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TERTIARY STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STOMACH CANCER; TRANSCRIPTION REGULATION; WOUND HEALING;

AMINO ACID SEQUENCE; ANIMALS; GASTROINTESTINAL HORMONES; HOMEOSTASIS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PRECANCEROUS CONDITIONS; SIGNAL TRANSDUCTION; STOMACH; STOMACH NEOPLASMS; TUMOR SUPPRESSOR PROTEINS; WOUND HEALING;

EID: 84872405519     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00374.2012     Document Type: Review

References (77)

1. Amiry N, Kong X, Muniraj N, Kannan N, Grandison PM, Lin J, Yang Y, Vouyovitch CM, Borges S, Perry JK, Mertani HC, Zhu T, Liu D, Lobie PE. Trefoil factor-1 (TFF1) enhances oncogenicity of mammary carcinoma cells. Endocrinology 150: 4473-4483, 2009.
2. Arumugam T, Brandt W, Ramachandran V, Moore TT, Wang H, May FE, Westley BR, Hwang RF, Logsdon CD. Trefoil factor 1 stimulates both pancreatic cancer and stellate cells and increases metastasis. Pancreas 40: 815-822, 2011.
3. Baus-Loncar M, Lubka M, Pusch CM, Otto WR, Poulsom R, Blin N. Cytokine regulation of the trefoil factor family binding protein GKN2 (GDDR/TFIZ1/blottin) in human gastrointestinal epithelial cells. Cell Physiol Biochem 20: 193-204, 2007.
4. Buache E, Etique N, Alpy F, Stoll I, Muckensturm M, Reina-San-Martin B, Chenard MP, Tomasetto C, Rio MC. Deficiency in trefoil factor 1 (TFF1) increases tumorigenicity of human breast cancer cells and mammary tumor development in TFF1-knockout mice. Oncogene 30: 3261-3273, 2011.
5. Carmel L, Koonin EV. A universal nonmonotonic relationship between gene compactness and expression levels in multicellular eukaryotes. Genome Biol Evol 1: 382-390, 2009.
6. Carvalho R, Kayademir T, Soares P, Canedo P, Sousa S, Oliveira C, Leistenschneider P, Seruca R, Gott P, Blin N, Carneiro F, Machado JC. Loss of heterozygosity and promoter methylation, but not mutation, may underlie loss of TFF1 in gastric carcinoma. Lab Invest 82: 1319-1326, 2002.
7. Chetty R, Naidoo R, Tarin M, Sitti C. Chromosome 2p, 3p, 5q and 18q status in sporadic gastric cancer. Pathology 34: 275-281, 2002.
8. Clyne M, Dillon P, Daly S, O'Kennedy R, May FE, Westley BR, Drumm B. Helicobacter pylori interacts with the human single-domain trefoil protein TFF1. Proc Natl Acad Sci USA 101: 7409-7414, 2004.
9. Collins JF. Gene chip analyses reveal differential genetic responses to iron deficiency in rat duodenum and jejunum. Biol Res 39: 25-37, 2006.
10. Correa P. A human model of gastric carcinogenesis. Cancer Res 48: 3554-3560, 1988.
11. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process. First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 52: 6735-6740, 1992.
12. Correa P. Helicobacter pylori and gastric carcinogenesis. Am J Surg Pathol 19 Suppl 1: S37-S43, 1995.
13. Correa P. The biological model of gastric carcinogenesis. IARC Sci Publ: 301-310, 2004.
14. Correa P, Haenszel W, Cuello C, Tannenbaum S, Archer M. A model for gastric cancer epidemiology. Lancet 2: 58-60, 1975.
15. Du JJ, Dou KF, Peng SY, Li JT, Wang WZ, Guan WX, Gao ZQ. [Study on novel gene GDDR related to gastric cancer]. Zhonghua Wai Ke Za Zhi 43: 10-13, 2005.
16. Du JJ, Dou KF, Peng SY, Wang WZ, Wang ZH, Xiao HS, Guan WX, Liu YB, Gao ZQ. Down-regulated full-length novel gene GDDR and its effect on gastric cancer. Zhonghua Yi Xue Za Zhi 83: 1166-1168, 2003.
17. Goldenring JR, Nomura S. Differentiation of the gastric mucosa. III. Animal models of oxyntic atrophy and metaplasia. Am J Physiol Gastrointest Liver Physiol 291: G999-G1004, 2006.
18. Hedlund J, Johansson J, Persson B. BRICHOS-a superfamily of multidomain proteins with diverse functions. BMC Res Notes 2: 180, 2009.
19. Hnia K, Notarnicola C, de Santa Barbara P, Hugon G, Rivier F, Laoudj-Chenivesse D, Mornet D. Biochemical properties of gastrokine-1 purified from chicken gizzard smooth muscle. PLos One 3: e3854, 2008.
20. Holland PW. Gene duplication: past, present and future. Semin Cell Dev Biol 10: 541-547, 1999.
21. Johansson H, Eriksson M, Nordling K, Presto J, Johansson J. The BRICHOS domain of prosurfactant protein C can hold and fold a transmembrane segment. Protein Sci 18: 1175-1182, 2009.
22. Karam SM, Tomasetto C, Rio MC. Trefoil factor 1 is required for the commitment programme of mouse oxyntic epithelial progenitors. Gut 53: 1408-1415, 2004.
23. Katz JP, Perreault N, Goldstein BG, Actman L, McNally SR, Silberg DG, Furth EE, Kaestner KH. Loss of Klf4 in mice causes altered proliferation and differentiation and precancerous changes in the adult stomach. Gastroenterology 128: 935-945, 2005.
24. Khurana S, Mills JC. The gastric mucosa development and differentiation. Prog Mol Biol Transl Sci 96: 93-115, 2010.
25. Kim YS, Yoo HS, Lee KT, Goh SH, Jung JS, Oh SW, Baba M, Yasuda T, Matsubara K, Nagai H. Detection of genetic alterations in the human gastric cancer cell lines by two-dimensional analysis of genomic DNA. Int J Oncol 17: 297-308, 2000.
26. Kjellev S. The trefoil factor family-small peptides with multiple functionalities. Cell Mol Life Sci 66: 1350-1369, 2009.
27. Koizumi Y, Tanaka S, Mou R, Koganei H, Kokawa A, Kitamura R, Yamauchi H, Ookubo K, Saito T, Tominaga S, Matsumura K, Shimada H, Tsuchida N, Sekihara H. Changes in DNA copy number in primary gastric carcinomas by comparative genomic hybridization. Clin Cancer Res 3: 1067-1076, 1997.
28. Kokubu H, Ohtsuka T, Kageyama R. Mash1 is required for neuroendocrine cell development in the glandular stomach. Genes Cells 13: 41-51, 2008.
29. Kosriwong K, Menheniott TR, Giraud AS, Jearanaikoon P, Sripa B, Limpaiboon T. Trefoil factors: tumor progression markers and mitogens via EGFR/MAPK activation in cholangiocarcinoma. World J Gastroenterol 17: 1631-1641, 2011.
30. Kouznetsova I, Laubinger W, Kalbacher H, Kalinski T, Meyer F, Roessner A, Hoffmann W. Biosynthesis of gastrokine-2 in the human gastric mucosa: restricted spatial expression along the antral gland axis and differential interaction with TFF1, TFF2 and mucins. Cell Physiol Biochem 20: 899-908, 2007.
31. Lee CS, Perreault N, Brestelli JE, Kaestner KH. Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev 16: 1488-1497, 2002.
32. Lefebvre O, Chenard MP, Masson R, Linares J, Dierich A, LeMeur M, Wendling C, Tomasetto C, Chambon P, Rio MC. Gastric mucosa abnormalities and tumorigenesis in mice lacking the pS2 trefoil protein. Science 274: 259-262, 1996.
33. MacArthur DG, Seto JT, Raftery JM, Quinlan KG, Huttley GA, Hook JW, Lemckert FA, Kee AJ, Edwards MR, Berman Y, Hardeman EC, Gunning PW, Easteal S, Yang N, North KN. Loss of ACTN3 gene function alters mouse muscle metabolism and shows evidence of positive selection in humans. Nat Genet 39: 1261-1265, 2007.
34. Maguire JA, Mulugeta S, Beers MF. Endoplasmic reticulum stress induced by surfactant protein C BRICHOS mutants promotes proinflammatory signaling by epithelial cells. Am J Respir Cell Mol Biol 44: 404-414, 2011.
35. Mao W, Chen J, Peng TL, Yin XF, Chen LZ, Chen MH. Downregulation of gastrokine-1 in gastric cancer tissues and restoration of its expression induced gastric cancer cells to apoptosis. J Exp Clin Cancer Res 31: 49, 2012.
36. Mao W, Chen J, Peng TL, Yin XF, Chen LZ, Chen MH. Helicobacter pylori infection and administration of non-steroidal anti-inflammatory drugs down-regulate the expression of gastrokine-1 in gastric mucosa. Turk J Gastroenterol 23: 212-219, 2012.
37. Mao W, Chen J, Peng TL, Yin XF, Chen LZ, Chen MH. Role of trefoil factor 1 in gastric cancer and relationship between trefoil factor 1 and gastrokine 1. Oncol Rep 28: 1257-1262, 2012.
38. Martin G, Wex T, Treiber G, Malfertheiner P, Nardone G. Low-dose aspirin reduces the gene expression of gastrokine-1 in the antral mucosa of healthy subjects. Aliment Pharmacol Ther 28: 782-788, 2008.
39. Martin TE, Powell CT, Wang Z, Bhattacharyya S, Walsh-Reitz MM, Agarwal K, Toback FG. A novel mitogenic protein that is highly expressed in cells of the gastric antrum mucosa. Am J Physiol Gastrointest Liver Physiol 285: G332-G343, 2003.
40. May FE, Griffin SM, Westley BR. The trefoil factor interacting protein TFIZ1 binds the trefoil protein TFF1 preferentially in normal gastric mucosal cells but the co-expression of these proteins is deregulated in gastric cancer. Int J Biochem Cell Biol 41: 632-640, 2009.
41. May FE, Westley BR. Trefoil proteins: their role in normal and malignant cells. J Pathol 183: 4-7, 1997.
42. Menheniott TR, Peterson AJ, O'Connor L, Lee KS, Kalantzis A, Kondova I, Bontrop RE, Bell KM, Giraud AS. A novel gastrokine, Gkn3, marks gastric atrophy and shows evidence of adaptive gene loss in humans. Gastroenterology 138: 1823-1835, 2010.
43. Moran AP, Gupta A, Joshi L. Sweet-talk: role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut 60: 1412-1425, 2011.
44. Moss SF, Lee JW, Sabo E, Rubin AK, Rommel J, Westley BR, May FE, Gao J, Meitner PA, Tavares R, Resnick MB. Decreased expression of gastrokine 1 and the trefoil factor interacting protein TFIZ1/GKN2 in gastric cancer: influence of tumor histology and relationship to prognosis. Clin Cancer Res 14: 4161-4167, 2008.
45. Mulugeta S, Nguyen V, Russo SJ, Muniswamy M, Beers MF. A surfactant protein C precursor protein BRICHOS domain mutation causes endoplasmic reticulum stress, proteasome dysfunction, and caspase 3 activation. Am J Respir Cell Mol Biol 32: 521-530, 2005.
46. Nagaraj SH, Harsha HC, Reverter A, Colgrave ML, Sharma R, Andronicos N, Hunt P, Menzies M, Lees MS, Sekhar NR, Pandey A, Ingham A. Proteomic analysis of the abomasal mucosal response following infection by the nematode, Haemonchus contortus, in genetically resistant and susceptible sheep. J Proteomics 75: 2141-2152, 2012.
47. Nardone G, Martin G, Rocco A, Rippa E, La Monica G, Caruso F, Arcari P. Molecular expression of gastrokine 1 in normal mucosa and in Helicobacter pylori-related preneoplastic and neoplastic gastric lesions. Cancer Biol Ther 7: 1890-1895, 2008.
48. Nardone G, Rippa E, Martin G, Rocco A, Siciliano RA, Fiengo A, Cacace G, Malorni A, Budillon G, Arcari P. Gastrokine 1 expression in patients with and without Helicobacter pylori infection. Dig Liver Dis 39: 122-129, 2007.
49. Nerelius C, Fitzen M, Johansson J. Amino acid sequence determinants and molecular chaperones in amyloid fibril formation. Biochem Biophys Res Commun 396: 2-6, 2010.
50. Oien KA, McGregor F, Butler S, Ferrier RK, Downie I, Bryce S, Burns S, Keith WN. Gastrokine 1 is abundantly and specifically expressed in superficial gastric epithelium, down-regulated in gastric carcinoma, and shows high evolutionary conservation. J Pathol 203: 789-797, 2004.
51. Oien KA, Vass JK, Downie I, Fullarton G, Keith WN. Profiling, comparison and validation of gene expression in gastric carcinoma and normal stomach. Oncogene 22: 4287-4300, 2003.
52. Ottini L, Falchetti M, Lupi R, Rizzolo P, Agnese V, Colucci G, Bazan V, Russo A. Patterns of genomic instability in gastric cancer: clinical implications and perspectives. Ann Oncol 17 Suppl 7: vii97-vii102, 2006.
53. Otto WR, Patel K, McKinnell I, Evans MD, Lee CY, Frith D, Hanrahan S, Blight K, Blin N, Kayademir T, Poulsom R, Jeffery R, Hunt T, Wright NA, McGregor F, Oien KA. Identification of blottin: a novel gastric trefoil factor family-2 binding protein. Proteomics 6: 4235-4245, 2006.
54. Panani AD. Cytogenetic and molecular aspects of gastric cancer: clinical implications. Cancer Lett 266: 99-115, 2008.
55. Peng S, Fitzen M, Jornvall H, Johansson J. The extracellular domain of Bri2 (ITM2B) binds the ABri peptide (1-23) and amyloid β-peptide (Aβ1-40): implications for Bri2 effects on processing of amyloid precursor protein and Aβ aggregation. Biochem Biophys Res Commun 393: 356-361, 2010.
56. Peterson AJ, Menheniott TR, O'Connor L, Walduck AK, Fox JG, Kawakami K, Minamoto T, Ong EK, Wang TC, Judd LM, Giraud AS. Helicobacter pylori infection promotes methylation and silencing of trefoil factor 2, leading to gastric tumor development in mice and humans. Gastroenterology 139: 2005-2017, 2010.
57. Prest SJ, May FE, Westley BR. The estrogen-regulated protein, TFF1, stimulates migration of human breast cancer cells. FASEB J 16: 592-594, 2002.
58. Ramsey VG, Doherty JM, Chen CC, Stappenbeck TS, Konieczny SF, Mills JC. The maturation of mucus-secreting gastric epithelial progenitors into digestive-enzyme secreting zymogenic cells requires Mist1. Development 134: 211-222, 2007.
59. Reeves EP, Ali T, Leonard P, Hearty S, O'Kennedy R, May FE, Westley BR, Josenhans C, Rust M, Suerbaum S, Smith A, Drumm B, Clyne M. Helicobacter pylori lipopolysaccharide interacts with TFF1 in a pH-dependent manner. Gastroenterology 135: 2043-2054, 2008.
60. Resnick MB, Sabo E, Meitner PA, Kim SS, Cho Y, Kim HK, Tavares R, Moss SF. Global analysis of the human gastric epithelial transcriptome altered by Helicobacter pylori eradication in vivo. Gut 55: 1717-1724, 2006.
61. Saleh M, Mathison JC, Wolinski MK, Bensinger SJ, Fitzgerald P, Droin N, Ulevitch RJ, Green DR, Nicholson DW. Enhanced bacterial clearance and sepsis resistance in caspase-12-deficient mice. Nature 440: 1064-1068, 2006.
62. Saleh M, Vaillancourt JP, Graham RK, Huyck M, Srinivasula SM, Alnemri ES, Steinberg MH, Nolan V, Baldwin CT, Hotchkiss RS, Buchman TG, Zehnbauer BA, Hayden MR, Farrer LA, Roy S, Nicholson DW. Differential modulation of endotoxin responsiveness by human caspase-12 polymorphisms. Nature 429: 75-79, 2004.
63. Sanchez-Pulido L, Devos D, Valencia A. BRICHOS: a conserved domain in proteins associated with dementia, respiratory distress and cancer. Trends Biochem Sci 27: 329-332, 2002.
64. Shiozaki K, Nakamori S, Tsujie M, Okami J, Yamamoto H, Nagano H, Dono K, Umeshita K, Sakon M, Furukawa H, Hiratsuka M, Kasugai T, Ishiguro S, Monden M. Human stomach-specific gene, CA11, is down-regulated in gastric cancer. Int J Oncol 19: 701-707, 2001.
65. Toback FG, Walsh-Reitz MM, Musch MW, Chang EB, Del Valle J, Ren H, Huang E, Martin TE. Peptide fragments of AMP-18, a novel secreted gastric antrum mucosal protein, are mitogenic and motogenic. Am J Physiol Gastrointest Liver Physiol 285: G344-G353, 2003.
66. Tomita H, Takaishi S, Menheniott TR, Yang X, Shibata W, Jin G, Betz KS, Kawakami K, Minamoto T, Tomasetto C, Rio MC, Lerkowit N, Varro A, Giraud AS, Wang TC. Inhibition of gastric carcinogenesis by the hormone gastrin is mediated by suppression of TFF1 epigenetic silencing. Gastroenterology 140: 879-891, 2011.
67. Urrutia AO, Hurst LD. The signature of selection mediated by expression on human genes. Genome Res 13: 2260-2264, 2003.
68. Verzi MP, Khan AH, Ito S, Shivdasani RA. Transcription factor foxq1 controls mucin gene expression and granule content in mouse stomach surface mucous cells. Gastroenterology 135: 591-600, 2008.
69. Walsh-Reitz MM, Huang EF, Musch MW, Chang EB, Martin TE, Kartha S, Toback FG. AMP-18 protects barrier function of colonic epithelial cells: role of tight junction proteins. Am J Physiol Gastrointest Liver Physiol 289: G163-G171, 2005.
70. Wang X, Grus WE, Zhang J. Gene losses during human origins. PLoS Biol 4: e52, 2006.
71. Westley BR, Griffin SM, May FE. Interaction between TFF1, a gastric tumor suppressor trefoil protein, and TFIZ1, a BRICHOS domain-containing protein with homology to SP-C. Biochemistry 44: 7967-7975, 2005.
72. Xing R, Li W, Cui J, Zhang J, Kang B, Wang Y, Wang Z, Liu S, Lu Y. Gastrokine 1 induces senescence through p16/Rb pathway activation in gastric cancer cells. Gut 61: 43-52, 2012.
73. Xue Y, Daly A, Yngvadottir B, Liu M, Coop G, Kim Y, Sabeti P, Chen Y, Stalker J, Huckle E, Burton J, Leonard S, Rogers J, Tyler-Smith C. Spread of an inactive form of caspase-12 in humans is due to recent positive selection. Am J Hum Genet 78: 659-670, 2006.
74. Yan GR, Xu SH, Tan ZL, Yin XF, He QY. Proteomics characterization of gastrokine 1-induced growth inhibition of gastric cancer cells. Proteomics 11: 3657-3564, 2011.
75. Yoon JH, Kang YH, Choi YJ, Park IS, Nam SW, Lee JY, Lee YS, Park WS. Gastrokine 1 functions as a tumor suppressor by inhibition of epithelial-mesenchymal transition in gastric cancers. J Cancer Res Clin Oncol 137: 1697-1704, 2011.
76. Yoon JH, Song JH, Zhang C, Jin M, Kang YH, Nam SW, Lee JY, Park WS. Inactivation of the gastrokine 1 gene in gastric adenomas and carcinomas. J Pathol 223: 618-625, 2011.
77. Yoshikawa Y, Mukai H, Hino F, Asada K, Kato I. Isolation of two novel genes, down-regulated in gastric cancer. Jpn J Cancer Res 91: 459-463, 2000.