MAPKs and signal transduction in the control of gastrointestinal epithelial cell proliferation and differentiation

International Journal of Molecular Sciences

Volumn 14, Issue 5, 2013, Pages 10143-10161

  Osaki, Luciana H ^a   Gama, Patrícia ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Cell cycle; Differentiation; MAPK

Indexed keywords

BETA CATENIN; JANUS KINASE 1; JANUS KINASE 2; JANUS KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMAD PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL RENEWAL; CELL TRANSFORMATION; GASTROINTESTINAL TRACT; HUMAN; INTESTINE CELL; INTESTINE EPITHELIUM CELL; INTRACELLULAR SIGNALING; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; STOMACH EPITHELIUM; ANIMAL; CYTOLOGY; EPITHELIUM CELL; INTESTINE MUCOSA; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; EPITHELIAL CELLS; GASTROINTESTINAL TRACT; HUMANS; INTESTINAL MUCOSA; MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 84877991564     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140510143     Document Type: Review

References (146)

1. Avruch, J. Map kinase pathways: The first twenty years. Biochim. Biophys. Acta 2007, 1773, 1150-1160.
2. Wagner, E.F.; Nebreda, A.R. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat. Rev. Cancer 2009, 9, 537-549.
3. Asrih, M.; Mach, F.; Nencioni, A.; Dallegri, F.; Quercioli, A.; Montecucco, F. Role of mitogen-activated protein kinase pathways in multifactorial adverse cardiac remodeling associated with metabolic syndrome. Mediators Inflamm. 2013, 2013, e367245.
4. Schlessinger, J. Common and distinct elements in cellular signaling via EGF and FGF receptors. Science 2004, 306, 1506-1507.
5. Kyriakis, J.M.; Avruch, J. Mammalian MAPK signal transduction pathways activated by stress and inflammation: A 10-year update. Physiol. Rev. 2012, 92, 689-737.
6. Payne, D.M.; Rossomando, A.J.; Martino, P.; Erickson, A.K.; Her, J.H.; Shabanowitz, J.; Hunt, D.F.; Weber, M.J.; Sturgill, T.W. Identification of the regulatory phosphorylation sites in pp42/mitogen-activated protein kinase (MAP kinase). EMBO J. 1991, 10, 885-892.
7. Biondi, R.M.; Nebreda, A.R. Signalling specificity of Ser/Thr protein kinases through docking-site-mediated interactions. Biochem. J. 2003, 372, 1-13.
8. Tanoue, T.; Adachi, M.; Moriguchi, T.; Nishida, E. A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat. Cell Biol. 2000, 2, 110-116.
9. Pan, C.Q.; Sudol, M.; Sheetz, M.; Low, B.C. Modularity and functional plasticity of scaffold proteins as p(l)acemakers in cell signaling. Cell. Signal. 2012, 24, 2143-2165.
10. Brown, M.D.; Sacks, D.B. Protein scaffolds in map kinase signalling. Cell. Signal. 2009, 21, 462-469.
11. Owens, D.M.; Keyse, S.M. Differential regulation of map kinase signalling by dual-specificity protein phosphatases. Oncogene 2007, 26, 3203-3213.
12. Andreadi, C.; Noble, C.; Patel, B.; Jin, H.; Aguilar Hernandez, M.M.; Balmanno, K.; Cook, S.J.; Pritchard, C. Regulation of MEK/ERK pathway output by subcellular localization of B-Raf. Biochem. Soc. Trans. 2012, 40, 67-72.
13. Marshall, C.J. Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation. Cell 1995, 80, 179-185.
14. Yang, S.H.; Sharrocks, A.D.; Whitmarsh, A.J. Map kinase signalling cascades and transcriptional regulation. Gene 2013, 513, 1-13.
15. Xiao, Z.Q.; Li, J.; Majumdar, A.P. Regulation of TGF-alpha-induced activation of AP-1 in the aging gastric mucosa. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285, G396-G403.
16. Lv, Z.M.; Wang, Q.; Wan, Q.; Lin, J.G.; Hu, M.S.; Liu, Y.X.; Wang, R. The role of the p38 MAPK signaling pathway in high glucose-induced epithelial-mesenchymal transition of cultured human renal tubular epithelial cells. PLoS One 2011, 6, e22806.
17. Yoon, S.; Seger, R. The extracellular signal-regulated kinase: Multiple substrates regulate diverse cellular functions. Growth Factors 2006, 24, 21-44.
18. Ramos, J.W. The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells. Int. J. Biochem. Cell Biol. 2008, 40, 2707-2719.
19. Seki, E.; Brenner, D.A.; Karin, M. A liver full of JNK: Signaling in regulation of cell function and disease pathogenesis, and clinical approaches. Gastroenterology 2012, 143, 307-320.
20. Cuenda, A.; Rousseau, S. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta 2007, 1773, 1358-1375.
21. Cuadrado, A.; Nebreda, A.R. Mechanisms and functions of p38 MAPK signalling. Biochem. J. 2010, 429, 403-417.
22. Lee, J.D.; Ulevitch, R.J.; Han, J. Primary structure of BMK1: A new mammalian map kinase. Biochem. Biophys. Res. Commun. 1995, 213, 715-724.
23. Zhou, G.; Bao, Z.Q.; Dixon, J.E. Components of a new human protein kinase signal transduction pathway. J. Biol. Chem. 1995, 270, 12665-12669.
24. Nithianandarajah-Jones, G.N.; Wilm, B.; Goldring, C.E.; Müller, J.; Cross, M.J. ERK5: Structure, regulation and function. Cell. Signal. 2012, 24, 2187-2196.
25. Kato, Y.; Kravchenko, V.V.; Tapping, R.I.; Han, J.; Ulevitch, R.J.; Lee, J.D. BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 1997, 16, 7054-7066.
26. Junttila, M.R.; Li, S.P.; Westermarck, J. Phosphatase-mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. FASEB J. 2008, 22, 954-965.
27. Fey, D.; Croucher, D.R.; Kolch, W.; Kholodenko, B.N. Crosstalk and signaling switches in mitogen-activated protein kinase cascades. Front. Physiol. 2012, 3, doi: 10.3389/fphys.2012.00355.
28. Liu, Q.; Hofmann, P.A. Protein phosphatase 2A-mediated cross-talk between p38 MAPK and ERK in apoptosis of cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 2004, 286, H2204-H2212.
29. Grethe, S.; Coltella, N.; di Renzo, M.F.; Pörn-Ares, M.I. p38 MAPK downregulates phosphorylation of Bad in doxorubicin-induced endothelial apoptosis. Biochem. Biophys. Res. Commun. 2006, 347, 781-790.
30. Lee, J.; Hong, F.; Kwon, S.; Kim, S.S.; Kim, D.O.; Kang, H.S.; Lee, S.J.; Ha, J. Activation of p38 MAPK induces cell cycle arrest via inhibition of Raf/ERK pathway during muscle differentiation. Biochem. Biophys. Res. Commun. 2002, 298, 765-771.
31. Li, S.P.; Junttila, M.R.; Han, J.; Kähäri, V.M.; Westermarck, J. p38 mitogen-activated protein kinase pathway suppresses cell survival by inducing dephosphorylation of mitogen-activated protein/extracellular signal-regulated kinase kinase1,2. Cancer Res. 2003, 63, 3473-3477.
32. Monick, M.M.; Powers, L.S.; Gross, T.J.; Flaherty, D.M.; Barrett, C.W.; Hunninghake, G.W. Active ERK contributes to protein translation by preventing JNK-dependent inhibition of protein phosphatase 1. J. Immunol. 2006, 177, 1636-1645.
33. Zhang, Q.G.; Wang, R.M.; Han, D.; Yang, L.C.; Li, J.; Brann, D.W. Preconditioning neuroprotection in global cerebral ischemia involves NMDA receptor-mediated ERK-JNK3 crosstalk. Neurosci. Res. 2009, 63, 205-212.
34. Peng, T.; Zhang, T.; Lu, X.; Feng, Q. JNK1/c-fos inhibits cardiomyocyte TNF-α expression via a negative crosstalk with ERK and p38 MAPK in endotoxaemia. Cardiovasc. Res. 2009, 81, 733-741.
35. Aksamitiene, E.; Kiyatkin, A.; Kholodenko, B.N. Cross-talk between mitogenic Ras/MAPK and survival PI3K/Akt pathways: A fine balance. Biochem. Soc. Trans. 2012, 40, 139-146.
36. Barthwal, M.K.; Sathyanarayana, P.; Kundu, C.N.; Rana, B.; Pradeep, A.; Sharma, C.; Woodgett, J.R.; Rana, A. Negative regulation of mixed lineage kinase 3 by protein kinase B/Akt leads to cell survival. J. Biol. Chem. 2003, 278, 3897-3902.
37. Kim, A.H.; Khursigara, G.; Sun, X.; Franke, T.F.; Chao, M.V. Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol. Cell Biol. 2001, 21, 893-901.
38. Vazquez de la Torre, A.; Junyent, F.; Folch, J.; Pelegri, C.; Vilaplana, J.; Auladell, C.; Beas-Zarate, C.; Pallas, M.; Verdaguer, E.; Camins, A. PI3 K/Akt inhibition induces apoptosis through p38 activation in neurons. Pharmacol. Res. 2013, 70, 116-125.
39. Hartsough, M.T.; Mulder, K.M. Transforming growth factor beta activation of p44MAPK in proliferating cultures of epithelial cells. J. Biol. Chem. 1995, 270, 7117-7124.
40. Hough, C.; Radu, M.; Doré, J.J. TGF-beta induced Erk phosphorylation of smad linker region regulates smad signaling. PLoS One 2012, 7, e42513.
41. Tian, Y.C.; Chen, Y.C.; Chang, C.T.; Hung, C.C.; Wu, M.S.; Phillips, A.; Yang, C.W. Epidermal growth factor and transforming growth factor-β1 enhance HK-2 cell migration through a synergistic increase of matrix metalloproteinase and sustained activation of ERK signaling pathway. Exp. Cell Res. 2007, 313, 2367-2377.
42. Browne, J.A.; Pearson, A.L.; Zahr, R.A.; Niculescu-Duvaz, I.; Baines, D.L.; Dockrell, M.E. TGF-β activates ERK5 in human renal epithelial cells. Biochem. Biophys. Res. Commun. 2008, 373, 440-444.
43. Marchetti, A.; Colletti, M.; Cozzolino, A.M.; Steindler, C.; Lunadei, M.; Mancone, C.; Tripodi, M. ERK5/MAPK is activated by TGFbeta in hepatocytes and required for the GSK-3beta-mediated Snail protein stabilization. Cell. Signal. 2008, 20, 2113-2118.
44. Joko, T.; Shiraishi, A.; Akune, Y.; Tokumaru, S.; Kobayashi, T.; Miyata, K.; Ohashi, Y. Involvement of P38MAPK in human corneal endothelial cell migration induced by TGF-β(2). Exp. Eye Res. 2012, 108C, 23-32.
45. Kretzschmar, M.; Liu, F.; Hata, A.; Doody, J.; Massague, J. The TGF-beta family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 1997, 11, 984-995.
46. Kretzschmar, M.; Doody, J.; Timokhina, I.; Massague, J. A mechanism of repression of TGFβ/Smad signaling by oncogenic Ras. Genes Dev. 1999, 13, 804-816.
47. Kretzschmar, M.; Doody, J.; Massague, J. Opposing BMP and EGF signalling pathways converge on the TGF-β family mediator Smad1. Nature 1997, 389, 618-622.
48. Červenka, I.; Wolf, J.; Mašek, J.; Krejci, P.; Wilcox, W.R.; Kozubík, A.; Schulte, G.; Gutkind, J.S.; Bryja, V. Mitogen-activated protein kinases promote WNT/β-catenin signaling via phosphorylation of LRP6. Mol. Cell Biol. 2011, 31, 179-189.
49. Krejci, P.; Aklian, A.; Kaucka, M.; Sevcikova, E.; Prochazkova, J.; Masek, J.K.; Mikolka, P.; Pospisilova, T.; Spoustova, T.; Weis, M.; et al. Receptor tyrosine kinases activate canonical WNT/β-catenin signaling via MAP kinase/LRP6 pathway and direct β-catenin phosphorylation. PLoS One 2012, 7, e35826.
50. Biechele, T.L.; Kulikauskas, R.M.; Toroni, R.A.; Lucero, O.M.; Swift, R.D.; James, R.G.; Robin, N.C.; Dawson, D.W.; Moon, R.T.; Chien, A.J. Wnt/β-catenin signaling and AXIN1 regulate apoptosis triggered by inhibition of the mutant kinase BRAFV600E in human melanoma. Sci. Signal. 2012, 5, doi: 10.1126/scisignal.2002274.
51. Bikkavilli, R.K.; Feigin, M.E.; Malbon, C.C. p38 mitogen-activated protein kinase regulates canonical Wnt-beta-catenin signaling by inactivation of GSK3β. J. Cell Sci. 2008, 121, 3598-3607.
52. Bikkavilli, R.K.; Feigin, M.E.; Malbon, C.C. Gαo mediates WNT-JNK signaling through dishevelled 1 and 3, RhoA family members, and MEKK 1 and 4 in mammalian cells. J. Cell Sci. 2008, 121, 234-245.
53. Singh, A.M.; Reynolds, D.; Cliff, T.; Ohtsuka, S.; Mattheyses, A.L.; Sun, Y.; Menendez, L.; Kulik, M.; Dalton, S. Signaling network crosstalk in human pluripotent cells: A Smad2/3-regulated switch that controls the balance between self-renewal and differentiation. Cell Stem Cell 2012, 10, 312-326.
54. Rivard, N.; Boucher, M.J.; Asselin, C.; L'Allemain, G. MAP kinase cascade is required for p27 downregulation and S phase entry in fibroblasts and epithelial cells. Am. J. Physiol. 1999, 277, C652-C664.
55. Coleman, M.L.; Marshall, C.J.; Olson, M.F. RAS and RHO GTPases in G1-phase cell-cycle regulation. Nat. Rev. Mol. Cell Biol. 2004, 5, 355-366.
56. Chambard, J.C.; Lefloch, R.; Pouysségur, J.; Lenormand, P. ERK implication in cell cycle regulation. Biochim. Biophys. Acta 2007, 1773, 1299-1310.
57. Huang, K.T.; Pavlides, S.C.; Lecanda, J.; Blank, S.V.; Mittal, K.R.; Gold, L.I. Estrogen and progesterone regulate p27kip1 levels via the ubiquitin-proteasome system: Pathogenic and therapeutic implications for endometrial cancer. PLoS One 2012, 7, e46072.
58. Ullrich, A.; Schlessinger, J. Signal transduction by receptors with tyrosine kinase activity. Cell 1990, 61, 203-212.
59. Kholodenko, B.N. Map kinase cascade signaling and endocytic trafficking: A marriage of convenience? Trends Cell Biol. 2002, 12, 173-177.
60. Ceresa, B.P. Spatial regulation of epidermal growth factor receptor signaling by endocytosis. Int. J. Mol. Sci. 2012, 14, 72-87.
61. Mills, J.C.; Shivdasani, R.A. Gastric epithelial stem cells. Gastroenterology 2011, 140, 412-424.
62. Karam, S.M.; Leblond, C.P. Dynamics of epithelial cells in the corpus of the mouse stomach. I. Identification of proliferative cell types and pinpointing of the stem cell. Anat. Rec. 1993, 236, 259-279.
63. Pan, Q.; Nicholson, A.M.; Barr, H.; Harrison, L.A.; Wilson, G.D.; Burkert, J.; Jeffery, R.; Alison, M.R.; Looijenga, L.; Lin, W.R.; et al. Identification of lineage-uncommitted, long-lived, label-retaining cells in healthy human esophagus and stomach, and in metaplastic esophagus. Gastroenterology 2013, 144, 761-770.
64. Bredemeyer, A.J.; Geahlen, J.H.; Weis, V.G.; Huh, W.J.; Zinselmeyer, B.H.; Srivatsan, S.; Miller, M.J.; Shaw, A.S.; Mills, J.C. The gastric epithelial progenitor cell niche and differentiation of the zymogenic (chief) cell lineage. Dev. Biol. 2009, 325, 211-224.
65. Barker, N.; Huch, M.; Kujala, P.; van de Wetering, M.; Snippert, H.J.; van Es, J.H.; Sato, T.; Stange, D.E.; Begthel, H.; van den Born, M.; et al. Lgr5+ve stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 2010, 6, 25-36.
66. Alvares, E.P. Extensive networks of tmpase positive basal lysosomes are present in fetal rat gastric epithelium before overt differentiation. J. Submicrosc. Cytol. Pathol. 1994, 26, 515-523.
67. Kim, B.M.; Buchner, G.; Miletich, I.; Sharpe, P.T.; Shivdasani, R.A. The stomach mesenchymal transcription factor Barx1 specifies gastric epithelial identity through inhibition of transient Wnt signaling. Dev. Cell 2005, 8, 611-622.
68. Kiefer, S.M.; Robbins, L.; Rauchman, M. Conditional expression of Wnt9b in Six2-positive cells disrupts stomach and kidney function. PLoS One 2012, 7, e43098.
69. Beauchamp, R.D.; Barnard, J.A.; McCutchen, C.M.; Cherner, J.A.; Coffey, R.J. Localization of transforming growth factor alpha and its receptor in gastric mucosal cells. Implications for a regulatory role in acid secretion and mucosal renewal. J. Clin. Invest. 1989, 84, 1017-1023.
70. Slomiany, B.L.; Liu, J.; Yao, P.; Wu-Wang, C.Y.; Keogh, J.P.; Wang, S.L.; Slomiany, A. Characterization of the epidermal growth factor receptor in the gastric mucosa. Digestion 1990, 47, 181-190.
71. Osaki, L.H.; Curi, M.A.; Alvares, E.P.; Gama, P. Early weaning accelerates the differentiation of mucous neck cells in rat gastric mucosa: Possible role of TGFalpha/EGFR. Differentiation 2010, 79, 48-56.
72. Osaki, L.H.; Figueiredo, P.M.; Alvares, E.P.; Gama, P. EGFR is involved in control of gastric cell proliferation through activation of MAPK and Src signalling pathways in early-weaned rats. Cell Prolif. 2011, 44, 174-182.
73. Alison, M.R.; Sarraf, C.E. The role of growth factors in gastrointestinal cell proliferation. Cell Biol. Int. 1994, 18, 1-10.
74. Hormi, K.; Lehy, T. Developmental expression of transforming growth factor-α and epidermal growth factor receptor proteins in the human pancreas and digestive tract. Cell Tissue Res. 1994, 278, 439-450.
75. Nakajima, N.; Kuwayama, H. Stimulatory effect of transforming growth factor-alpha on gastric epithelial cell migration through proliferation. J. Clin. Gastroenterol. 1995, 21, S45-S49.
76. Turner, J.R.; Liu, L.; Fligiel, S.E.; Jaszewski, R.; Majumdar, A.P. Aging alters gastric mucosal responses to epidermal growth factor and transforming growth factor-α. Am. J. Physiol. Gastrointest. Liver Physiol. 2000, 278, G805-G810.
77. Xiao, Z.Q.; Majumdar, A.P. Increased in vitro activation of EGFR by membrane-bound TGF-alpha from gastric and colonic mucosa of aged rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 281, G111-G116.
78. Pai, R.; Ohta, M.; Itani, R.M.; Sarfeh, I.J.; Tarnawski, A.S. Induction of mitogen-activated protein kinase signal transduction pathway during gastric ulcer healing in rats. Gastroenterology 1998, 114, 706-713.
79. Coffey, R.J.; Washington, M.K.; Corless, C.L.; Heinrich, M.C. Ménétrier disease and gastrointestinal stromal tumors: Hyperproliferative disorders of the stomach. J. Clin. Invest. 2007, 117, 70-80.
80. Tétreault, M.P.; Chailler, P.; Beaulieu, J.F.; Rivard, N.; Ménard, D. Epidermal growth factor receptor-dependent PI3K-activation promotes restitution of wounded human gastric epithelial monolayers. J. Cell. Physiol. 2008, 214, 545-557.
81. Albeck, J.G.; Mills, G.B.; Brugge, J.S. Frequency-modulated pulses of ERK activity transmit quantitative proliferation signals. Mol. Cell 2013, 49, 249-261.
82. Shin, S.H.; Park, S.Y.; Kang, G.H. Down-regulation of dual-specificity phosphatase 5 in gastric cancer by promoter CpG island hypermethylation and its potential role in carcinogenesis. Am. J. Pathol.2013, 182, 1275-1285.
83. Tureaud, J.; Sarkar, F.H.; Fligiel, S.E.; Kulkarni, S.; Jaszewski, R.; Reddy, K.; Yu, Y.; Majumdar, A.P. Increased expression of EGFR in gastric mucosa of aged rats. Am. J. Physiol. 1997, 273, G389-G398.
84. Nakamizo, H.; Suzuki, H.; Miura, S.; Mogami, S.; Kishikawa, H.; Yoshida, H.; Matsui, H.; Hibi, T. Transmural pressure loading enhances gastric mucosal cell proliferation. Dig. Dis. Sci. 2012, 57, 2545-2554.
85. Schneider, R.; Bornstein, S.R.; Chrousos, G.P.; Boxberger, S.; Ehninger, G.; Breidert, M. Leptin mediates a proliferative response in human gastric mucosa cells with functional receptor. Horm. Metab. Res. 2001, 33, 1-6.
86. Sasaki, E.; Tominaga, K.; Watanabe, T.; Fujiwara, Y.; Oshitani, N.; Matsumoto, T.; Higuchi, K.; Tarnawski, A.S.; Arakawa, T. COX-2 is essential for EGF induction of cell proliferation in gastric RGM1 cells. Dig. Dis. Sci. 2003, 48, 2257-2262.
87. Osawa, H.; Ohnishi, H.; Takano, K.; Noguti, T.; Mashima, H.; Hoshino, H.; Kita, H.; Sato, K.; Matsui, H.; Sugano, K. Sonic hedgehog stimulates the proliferation of rat gastric mucosal cells through ERK activation by elevating intracellular calcium concentration. Biochem. Biophys. Res. Commun. 2006, 344, 680-687.
88. Ohsawa, R.; Miyazaki, H.; Niisato, N.; Shiozaki, A.; Iwasaki, Y.; Otsuji, E.; Marunaka, Y. Intracellular chloride regulates cell proliferation through the activation of stress-activated protein kinases in MKN28 human gastric cancer cells. J. Cell. Physiol. 2010, 223, 764-770.
89. Ruggiero, P. Helicobacter pylori infection: What's new. Curr. Opin. Infect. Dis. 2012, 25, 337-344.
90. Ding, S.Z.; Smith, M.F.; Goldberg, J.B. Helicobacter pylori and mitogen-activated protein kinases regulate the cell cycle, proliferation and apoptosis in gastric epithelial cells. J. Gastroenterol. Hepatol. 2008, 23, e67-e78.
91. Burdick, J.S.; Chung, E.; Tanner, G.; Sun, M.; Paciga, J.E.; Cheng, J.Q.; Washington, K.; Goldenring, J.R.; Coffey, R.J. Treatment of ménétrier's disease with a monoclonal antibody against the epidermal growth factor receptor. N. Engl. J. Med. 2000, 343, 1697-1701.
92. Fiske, W.H.; Threadgill, D.; Coffey, R.J. Erbbs in the gastrointestinal tract: Recent progress and new perspectives. Exp. Cell Res. 2009, 315, 583-601.
93. Van den Brink, G.R.; Hardwick, J.C.; Tytgat, G.N.; Brink, M.A.; Ten Kate, F.J.; van Deventer, S.J.; Peppelenbosch, M.P. Sonic hedgehog regulates gastric gland morphogenesis in man and mouse. Gastroenterology 2001, 121, 317-328.
94. Itoh, K.; Kataoka, H.; Sasaki, M.; Tanida, S.; Oshima, T.; Ogasawara, N.; Ohara, H.; Nakao, H.; Joh, T. Bone morphogenetic protein 2 induced differentiation toward superficial epithelial cells in the gastric mucosa. J. Gastroenterol. 2006, 41, 1064-1075.
95. Nyeng, P.; Norgaard, G.A.; Kobberup, S.; Jensen, J. FGF10 signaling controls stomach morphogenesis. Dev. Biol. 2007, 303, 295-310.
96. Keeley, T.M.; Samuelson, L.C. Cytodifferentiation of the postnatal mouse stomach in normal and Huntingtin-interacting protein 1-related-deficient mice. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G1241-G1251.
97. Bockman, D.E.; Sharp, R.; Merlino, G. Regulation of terminal differentiation of zymogenic cells by transforming growth factor α in transgenic mice. Gastroenterology 1995, 108, 447-454.
98. Fiorucci, S.; Lanfrancone, L.; Santucci, L.; Calabro, A.; Orsini, B.; Federici, B.; Morelli, A. Epidermal growth factor modulates pepsinogen secretion in guinea pig gastric chief cells. Gastroenterology 1996, 111, 945-958.
99. Stepan, V.; Pausawasdi, N.; Ramamoorthy, S.; Todisco, A. The Akt and MAPK signal-transduction pathways regulate growth factor actions in isolated gastric parietal cells. Gastroenterology 2004, 127, 1150-1161.
100. Chew, C.S.; Parente, J.A.; Zhou, C.; Baranco, E.; Chen, X. Lasp-1 is a regulated phosphoprotein within the cAMP signaling pathway in the gastric parietal cell. Am. J. Physiol. 1998, 275, C56-C67.
101. Chew, C.S.; Parente, J.A.; Chen, X.; Chaponnier, C.; Cameron, R.S. The LIM and SH3 domain-containing protein, lasp-1, may link the cAMP signaling pathway with dynamic membrane restructuring activities in ion transporting epithelia. J. Cell. Sci. 2000, 113, 2035-2045.
102. Kopic, S.; Murek, M.; Geibel, J.P. Revisiting the parietal cell. Am. J. Physiol. Cell Physiol. 2010, 298, C1-C10.
103. Todisco, A.; Pausawasdi, N.; Ramamoorthy, S.; del Valle, J.; van Dyke, R.W.; Askari, F.K. Functional role of protein kinase B/Akt in gastric acid secretion. J. Biol. Chem. 2001, 276, 46436-46444.
104. Barker, N.; van Es, J.H.; Kuipers, J.; Kujala, P.; van den Born, M.; Cozijnsen, M.; Haegebarth, A.; Korving, J.; Begthel, H.; Peters, P.J.; et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449, 1003-1007.
105. Barker, N.; van de Wetering, M.; Clevers, H. The intestinal stem cell. Genes Dev. 2008, 22, 1856-1864.
106. Sato, T.; van Es, J.H.; Snippert, H.J.; Stange, D.E.; Vries, R.G.; van den Born, M.; Barker, N.; Shroyer, N.F.; van de Wetering, M.; Clevers, H. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011, 469, 415-418.
107. Van der Flier, L.G.; van Gijn, M.E.; Hatzis, P.; Kujala, P.; Haegebarth, A.; Stange, D.E.; Begthel, H.; van den Born, M.; Guryev, V.; Oving, I.; et al. Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 2009, 136, 903-912.
108. Simons, B.D.; Clevers, H. Stem cell self-renewal in intestinal crypt. Exp. Cell Res. 2011, 317, 2719-2724.
109. Ireland, H.; Kemp, R.; Houghton, C.; Howard, L.; Clarke, A.R.; Sansom, O.J.; Winton, D.J. Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: Effect of loss of β-catenin. Gastroenterology 2004, 126, 1236-1246.
110. Fevr, T.; Robine, S.; Louvard, D.; Huelsken, J. Wnt/β-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol. Cell Biol. 2007, 27, 7551-7559.
111. Schepers, A.; Clevers, H. Wnt signaling, stem cells, and cancer of the gastrointestinal tract. Cold Spring Harb. Perspect. Biol. 2012, 4, a007989.
112. Guardavaccaro, D.; Clevers, H. Wnt/β-catenin and MAPK signaling: Allies and enemies in different battlefields. Sci. Signal. 2012, 5, pe15.
113. Schwitalla, S.; Fingerle, A.A.; Cammareri, P.; Nebelsiek, T.; Göktuna, S.I.; Ziegler, P.K.; Canli, O.; Heijmans, J.; Huels, D.J.; Moreaux, G.; et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 2013, 152, 25-38.
114. Aliaga, J.C.; Deschênes, C.; Beaulieu, J.F.; Calvo, E.L.; Rivard, N. Requirement of the map kinase cascade for cell cycle progression and differentiation of human intestinal cells. Am. J. Physiol. 1999, 277, G631-G641.
115. Singh, R.; Subramanian, S.; Rhodes, J.M.; Campbell, B.J. Peanut lectin stimulates proliferation of colon cancer cells by interaction with glycosylated CD44v6 isoforms and consequential activation of c-Met and MAPK: Functional implications for disease-associated glycosylation changes. Glycobiology 2006, 16, 594-601.
116. Chiu, T.; Wu, S.S.; Santiskulvong, C.; Tangkijvanich, P.; Yee, H.F.; Rozengurt, E. Vasopressin-mediated mitogenic signaling in intestinal epithelial cells. Am. J. Physiol. Cell Physiol. 2002, 282, C434-C450.
117. Jasleen, J.; Shimoda, N.; Shen, E.R.; Tavakkolizadeh, A.; Whang, E.E.; Jacobs, D.O.; Zinner, M.J.; Ashley, S.W. Signaling mechanisms of glucagon-like peptide 2-induced intestinal epithelial cell proliferation. J. Surg. Res. 2000, 90, 13-18.
118. Jiang, R.; Lonnerdal, B. Apo-and holo-lactoferrin stimulate proliferation of mouse crypt cells but through different cellular signaling pathways. Int. J. Biochem. Cell Biol. 2012, 44, 91-100.
119. Wakeman, D.; Schneider, J.E.; Liu, J.; Wandu, W.S.; Erwin, C.R.; Guo, J.; Stappenbeck, T.S.; Warner, B.W. Deletion of p38-alpha mitogen-activated protein kinase within the intestinal epithelium promotes colon tumorigenesis. Surgery 2012, 152, 286-293.
120. Suzuki, A.; Sekiya, S.; Gunshima, E.; Fujii, S.; Taniguchi, H. EGF signaling activates proliferation and blocks apoptosis of mouse and human intestinal stem/progenitor cells in long-term monolayer cell culture. Lab. Invest. 2010, 90, 1425-1436.
121. Malecka-Panas, E.; Relan, N.K.; Majumdar, A.P. Increased activation of EGF-receptor tyrosine kinase by EGF and TGF-alpha in the colonic mucosa of aged rats. J. Gerontol. A Biol. Sci. Med. Sci. 1996, 51, B60-B65.
122. Xiao, Z.Q.; Moragoda, L.; Jaszewski, R.; Hatfield, J.A.; Fligiel, S.E.; Majumdar, A.P. Aging is associated with increased proliferation and decreased apoptosis in the colonic mucosa. Mech. Ageing Dev. 2001, 122, 1849-1864.
123. Majumdar, A.P.; Du, J. Phosphatidylinositol 3-kinase/Akt signaling stimulates colonic mucosal cell survival during aging. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290, G49-G55.
124. Houde, M.; Laprise, P.; Jean, D.; Blais, M.; Asselin, C.; Rivard, N. Intestinal epithelial cell differentiation involves activation of p38 mitogen-activated protein kinase that regulates the homeobox transcription factor CDx2. J. Biol. Chem. 2001, 276, 21885-21894.
125. Lorentz, O.; Duluc, I.; Arcangelis, A.D.; Simon-Assmann, P.; Kedinger, M.; Freund, J.N. Key role of the CDx2 homeobox gene in extracellular matrix-mediated intestinal cell differentiation. J. Cell Biol. 1997, 139, 1553-1565.
126. Lemieux, E.; Boucher, M.J.; Mongrain, S.; Boudreau, F.; Asselin, C.; Rivard, N. Constitutive activation of the MEK/ERK pathway inhibits intestinal epithelial cell differentiation. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 301, G719-G730.
127. Koldovský, O. Search for role of milk-borne biologically active peptides for the suckling. J. Nutr. 1989, 119, 1543-1551.
128. Gama, P.; Alvares, E.P. Early weaning and prolonged nursing induce changes in cell proliferation in the gastric epithelium of developing rats. J. Nutr. 2000, 130, 2594-2598.
129. de Andrade Sa, E.R.; Bitencourt, B.; Alvares, E.P.; Gama, P. In vivo effects of TGFbeta1 on the growth of gastric epithelium in suckling rats. Regul. Pept. 2008, 146, 293-302.
130. Ogias, D.; de Andrade Sa, E.R.; Alvares, E.P.; Gama, P. Opposite effects of fasting on TGF-beta3 and Tbetari distribution in the gastric mucosa of suckling and early weanling rats. Nutrition 2010, 26, 224-229.
131. Dvorak, B. Milk epidermal growth factor and gut protection. J. Pediatr. 2010, 156, S31-S35.
132. Moran, J.R.; Courtney, M.E.; Orth, D.N.; Vaughan, R.; Coy, S.; Mount, C.D.; Sherrell, B.J.; Greene, H.L. Epidermal growth factor in human milk: Daily production and diurnal variation during early lactation in mothers delivering at term and at premature gestation. J. Pediatr. 1983, 103, 402-405.
133. Letterio, J.J.; Geiser, A.G.; Kulkarni, A.B.; Roche, N.S.; Sporn, M.B.; Roberts, A.B. Maternal rescue of transforming growth factor-beta 1 null mice. Science 1994, 264, 1936-1938.
134. Penttila, I.A.; van Spriel, A.B.; Zhang, M.F.; Xian, C.J.; Steeb, C.B.; Cummins, A.G.; Zola, H.; Read, L.C. Transforming growth factor-beta levels in maternal milk and expression in postnatal rat duodenum and ileum. Pediatr. Res. 1998, 44, 524-531.
135. Lin, C.H.; Lyons, H.; Seelbach, M.S.; Tolia, V.; Vijesurier, R. Induction of gastric ornithine decarboxylase in early weaning rats. Digestion 2001, 63, 214-219.
136. Morikawa, Y.; Ueyama, E.; Senba, E. Fasting-induced activation of mitogen-activated protein kinases (ERK/p38) in the mouse hypothalamus. J. Neuroendocrinol. 2004, 16, 105-112.
137. Ueyama, E.; Morikawa, Y.; Yasuda, T.; Senba, E. Attenuation of fasting-induced phosphorylation of mitogen-activated protein kinases (ERK/p38) in the mouse hypothalamus in response to refeeding. Neurosci. Lett. 2004, 371, 40-44.
138. Alvares, E.P.; Gama, P. Fasting enhances cell proliferation of gastric epithelium during the suckling period in rats. Braz. J. Med. Biol. Res. 1993, 26, 869-873.
139. Gama, P.; Alvares, E.P. Corticosterone treatment inhibits cell proliferation in the gastric epithelium of suckling rats. J. Gastroenterol. 1998, 33, 32-38.
140. Ogias, D.; de Andrade Sa, E.R.; Kasai, A.; Moisan, M.P.; Alvares, E.P.; Gama, P. Fasting differentially regulates plasma corticosterone-binding globulin, glucocorticoid receptor, and cell cycle in the gastric mucosa of pups and adult rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298, G117-G125.
141. Angevine, K.R.; Wuescher, L.M.; Andrews, K.; Alexander, L.A.; McInerney, M.F.; Kieffer, T.J.; Mensah-Osman, E.J. Menin and GIP are inversely regulated by food intake and diet via PI3/AKT signaling in the proximal duodenum. Nutr. Diabetes 2012, 2, e55.
142. Sabio, G.; Davis, R.J. cJun NH2-terminal kinase 1 (JNK1): Roles in metabolic regulation of insulin resistance. Trends Biochem. Sci. 2010, 35, 490-496.
143. Schultze, S.M.; Hemmings, B.A.; Niessen, M.; Tschopp, O. PI3K/AKT, MAPK and AMPK signalling: Protein kinases in glucose homeostasis. Expert Rev. Mol. Med. 2012, 14, e1.
144. Nautiyal, J.; Banerjee, S.; Kanwar, S.S.; Yu, Y.; Patel, B.B.; Sarkar, F.H.; Majumdar, A.P. Curcumin enhances dasatinib-induced inhibition of growth and transformation of colon cancer cells. Int. J. Cancer 2011, 128, 951-961.
145. Fenton, J.I.; McCaskey, S.J. Curcumin and docosahexaenoic acid block insulin-induced colon carcinoma cell proliferation. Prostaglandins Leukot. Essent. Fatty Acids 2013, 88, 219-226.
146. Bao, M.J.; Shen, J.; Jia, Y.L.; Li, F.F.; Ma, W.J.; Shen, H.J.; Shen, L.L.; Lin, X.X.; Zhang, L.H.; Dong, X.W.; et al. Apple polyphenol protects against cigarette smoke-induced acute lung injury. Nutrition 2013, 29, 235-243.