Clathrin mediates endocytosis of progastrin and activates MAPKs: Role of cell surface annexin A2

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 302, Issue 7, 2012, Pages

  Sarkar, Shubhashish ^a   Kantara, Carla ^a   Singh, Pomila ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Caveolin; Chlorpromazine; Clathrin coated pits; IEC 18 intestinal cells

Indexed keywords

CAVEOLIN; CLATHRIN; LIPOCORTIN 2; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROGASTRIN;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; INTERNALIZATION; INTESTINE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT;

ANIMALS; ANNEXIN A2; CELL LINE; CHLORPROMAZINE; CLATHRIN; DOPAMINE ANTAGONISTS; ENDOCYTOSIS; ENZYME ACTIVATION; GASTRINS; GENE EXPRESSION REGULATION; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PROTEIN PRECURSORS; PROTEIN TRANSPORT; RATS; TRANSCRIPTION FACTOR RELA;

EID: 84859473727     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00406.2011     Document Type: Article

References (75)

1. Aly A, Shulkes A, Baldwin GS. Short term infusion of glycine-extended gastrin(17) stimulates both proliferation and formation of aberrant crypt foci in rat colonic mucosa. Int J Cancer 94: 307-313, 2001.
2. Baldwin GS, Hollande F, Yang Z, Karelina Y, Paterson A, Strang R, Fourmy D, Neumann G, Shulkes A. Biologically active recombinant human progastrin(6-80) contains a tightly bound calcium ion. J Biol Chem 276: 7791-7796, 2001.
3. Bellagamba C, Hubaishy I, Bjorge JD, Fitzpatrick SL, Fujita DJ, Waisman DM. Tyrosine phosphorylation of annexin II tetramer is stimulated by membrane binding. J Biol Chem 272: 3195-3199, 1997.
4. Brown D, Yallampalli U, Owlia A, Singh P. pp60c-Src Kinase mediates growth effects of the full-length precursor progastrin1-80 peptide on rat intestinal epithelial cells, in vitro. Endocrinology 144: 201-211, 2003.
5. Choi DS, Park JO, Jang SC, Yoon YJ, Jung JW, Choi DY, Kim JW, Kang JS, Park J, Hwang D, Lee KH, Park SH, Kim YK, Desiderio DM, Kim KP, Gho YS. Proteomic analysis of microvesicles derived from human colorectal cancer ascites. Proteomics 11: 2745-2751, 2011.
6. Chung CY, Erickson HP. Cell surface annexin II is a high affinity receptor for the alternatively spliced segment of tenascin-C. J Cell Biol 126: 539-548, 1994.
7. Ciccotosto GD, McLeish A, Hardy KJ, Shulkes A. Expression, processing, and secretion of gastrin in patients with colorectal carcinoma. Gastroenterology 109: 1142-1153, 1995.
8. Cobb S, Wood T, Ceci J, Varro A, Velasco M, Singh P. Intestinal expression of mutant and wild-type progastrin significantly increases colon carcinogenesis in response to azoxymethane in transgenic mice. Cancer 100: 1311-1323, 2004.
9. Creutz CE, Snyder SL. Interactions of annexins with the mu subunits of the clathrin assembly proteins. Biochemistry 44: 13795-13806, 2005.
10. Deora AB, Kreitzer G, Jacovina AT, Hajjar KA. An annexin 2 phosphorylation switch mediates p11-dependent translocation of annexin 2 to the cell surface. J Biol Chem 279: 43411-43418, 2004.
11. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5: 410-421, 2003.
12. Díaz VM, Hurtado M, Thomson TM, Reventós J, Paciucci R. Specific interaction of tissue-type plasminogen activator (t-PA) with annexin II on the membrane of pancreatic cancer cells activates plasminogen and promotes invasion in vitro. Gut 53: 993-1000, 2004.
13. Esposito I, Penzel R, Chaib-Harrireche M, Barcena U, Bergmann F, Riedl S, Kayed H, Giese N, Kleeff J, Friess H, Schirmacher P. Tenascin C and annexin II expression in the process of pancreatic carcinogenesis. J Pathol 208: 673-685, 2006.
14. Ferrand A, Bertrand C, Portolan G, Cui G, Carlson J, Pradayrol L, Fourmy D, Dufresne M, Wang TC, Seva C. Signaling pathways associated with colonic mucosa hyperproliferation in mice overexpressing gastrin precursors. Cancer Res 65: 2770-2777, 2005.
15. Fotin A, Cheng Y, Sliz P, Grigorieff N, Harrison SC, Kirchhausen T, Walz T. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432: 573-579, 2004.
16. Goh LK, Huang F, Kim W, Gygi S, Sorkin A. Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J Cell Biol 189: 871-883, 2010.
17. Hajjar KA, Jacovina AT, Chacko J. An endothelial cell receptor for plasminogen/tissue plasminogen activator. I. Identity with annexin II. J Biol Chem 269: 21191-21197, 1994.
18. Henriques CM, Rino J, Nibbs RJ, Graham GJ, Barata JT. IL-7 induces rapid clathrin-mediated internalization and JAK3-dependent degradation of IL-7Ralpha in T cells. Blood 115: 3269-3277, 2010.
19. Hoeller D, Volarevic S, Dikic I. Compartmentalization of growth factor receptor signalling. Curr Opin Cell Biol 17: 107-111, 2005.
20. Ikari A, Takiguchi A, Atomi K, Sugatani J. Epidermal growth factor increases clathrin-dependent endocytosis and degradation of claudin-2 protein in MDCK II cells. J Cell Physiol 226: 2448-2456, 2011.
21. Jacovina AT, Deora AB, Ling Q, Broekman MJ, Almeida D, Greenberg CB, Marcus AJ, Smith JD, Hajjar KA. Homocysteine inhibits neoangiogenesis in mice through blockade of annexin A2-dependent fibrinolysis. J Clin Invest 119: 3384-3394, 2009.
22. Jean-Alphonse F, Hanyaloglu AC. Regulation of GPCR signal networks via membrane trafficking. Mol Cell Endocrinol 331: 205-214, 2011.
23. Jin G, Ramanathan V, Quante M, Baik GH, Yang X, Wang SS, Tu S, Gordon SA, Pritchard DM, Varro A, Shulkes A, Wang TC. Inactivating cholecystokinin-2 receptor inhibits progastrin-dependent colonic crypt fission, proliferation, and colorectal cancer in mice. J Clin Invest 119: 2691-2701, 2009.
24. Ji NY, Park MY, Kang YH, Lee CI, Kim DG, Yeom YI, Jang YJ, Myung PK, Kim JW, Lee HG, Kim J, Lee K, Song EY. Evaluation of annexin II as a potential serum marker for hepatocellular carcinoma using a developed sandwich ELISA method. Int J Mol Med 24: 765-771, 2009.
25. Kantara C, Sarkar S, Swiercz R, Ortiz I, Singh P. Over-expression of progastrin imparts tumorigenic/metastatic potential to immortalized embryonic cells and cancer cells: role of stem/progenitor cell markers and annexin A2. In: Proceedings of the Digestive Disease Week, Chicago, IL, May 2011, abstract no. 208, A-52.
26. Kesavan K, Ratliff J, Johnson EW, Dahlberg W, Asara JM, Misra P, Frangioni JV, Jacoby DB. Annexin A2 is a molecular target for TM601, a peptide with tumor-targeting and anti-angiogenic effects. J Biol Chem 285: 4366-4374, 2010.
27. Kim DM, Noh HB, Park DS, Ryu SH, Koo JS, Shim YB. Immunosensors for detection of annexin II and MUC5AC for early diagnosis of lung cancer. Biosens Bioelectron 25: 456-462, 2009.
28. Kozik P, Francis RW, Seaman MN, Robinson MS. A screen for endocytic motifs. Traffic 11: 843-855, 2010.
29. Lakadamyali M, Rust MJ, Zhuang X. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124: 997-1009, 2006.
30. Lambert O, Cavusoglu N, Gallay J, Vincent M, Rigaud JL, Henry JP, Ayala-Sanmartin J. Novel organization and properties of annexin 2-membrane complexes. J Biol Chem 279: 10872-10882, 2004.
31. Lei JT, Martinez-Moczygemba M. Separate endocytic pathways regulate IL-5 receptor internalization and signaling. J Leukoc Biol 84: 499-509, 2008.
32. Liu AP, Aguet F, Danuser G, Schmid SL. Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J Cell Biol 191: 1381-1393, 2010.
33. Longerich T, Haller MT, Mogler C, Aulmann S, Lohmann V, Schirmacher P, Brand K. Annexin A2 as a differential diagnostic marker of hepatocellular tumors. Pathol Res Pract 207: 8-14, 2011.
34. Lu G, Maeda H, Reddy SV, Kurihara N, Leach R, Anderson JL, Roodman GD. Cloning and characterization of the annexin II receptor on human marrow stromal cells. J Biol Chem 81: 30542-30550, 2006.
35. Ma AS, Bel DJ, Mittal AA, Harrison HH. Immunocytochemical detection of extracellular annexin II in cultured human skin keratinocytes and isolation of annexin II isoforms enriched in the extracellular pool. J Cell Sci 107: 1973-1984, 1994.
36. Marina-García N, Franchi L, Kim YG, Hu Y, Smith DE, Boons GJ, Núñez G. Clathrin-and dynamin-dependent endocytic pathway regulates muramyl dipeptide internalization and NOD2 activation. J Immunol 182: 4321-4327, 2009.
37. Mathivanan S, Lim JW, Tauro BJ, Ji H, Moritz RL, Simpson RJ. Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol Cell Proteomics 9: 197-208, 2010.
38. Mayran N, Parton RG, Gruenberg J. Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J 22: 3242-353, 2003.
39. McLean S, Di Guglielmo GM. TGF beta (transforming growth factor beta) receptor type III directs clathrin-mediated endocytosis of TGF beta receptor types I and II. Biochem J 429: 137-145, 2010.
40. Mettlen M, Loerke D, Yarar D, Danuser G, Schmid SL. Cargo-and adaptor-specific mechanisms regulate clathrin-mediated endocytosis. J Cell Biol 188: 919-933, 2010.
41. Morel E, Gruenberg J. Annexin A2 binding to endosomes and functions in endosomal transport are regulated by tyrosine 23 phosphorylation. J Biol Chem 284: 1604-1611, 2009.
42. Nabi IR, Le PU. Caveolae/raft-dependent endocytosis. J Cell Biol 161: 673-677, 2003.
43. Ottewell PD, Varro A, Dockray GJ, Kirton CM, Watson AJ, Wang TC, Dimaline R, Pritchard DM. COOH-terminal 26-amino acid residues of progastrin are sufficient for stimulation of mitosis in murine colonic epithelium in vivo. Am J Physiol Gastrointest Liver Physiol 288: G541-G549, 2005.
44. Ortiz-Zapater E, Peiró S, Roda O, Corominas JM, Aguilar S, Ampurdanés C, Real FX, Navarro P. Tissue plasminogen activator induces pancreatic cancer cell proliferation by a non-catalytic mechanism that requires extracellular signal-regulated kinase 1/2 activation through epidermal growth factor receptor and annexin A2. Am J Pathol 170: 1573-1784, 2007.
45. Pannequin J, Bonnans C, Delaunay N, Ryan J, Bourgaux JF, Joubert D, Hollande F. The wnt target jagged-1 mediates the activation of notch signaling by progastrin in human colorectal cancer cells. Cancer Res 69: 6065-6073, 2009.
46. Patchell BJ, Wojcik KR, Yang TL, White SR, Dorscheid DR. Glycosylation and annexin II cell surface translocation mediate airway epithelial wound repair. Am J Physiol Lung Cell Mol Physiol 293: L354-L363, 2007.
47. Rengifo-Cam W, Singh P. Role of progastrins and gastrins and their receptors in GI and pancreatic cancers: targets for treatment. Curr Pharm Des 10: 2345-2358, 2004.
48. Rengifo-Cam W, Umar S, Sarkar S, Singh P. Antiapoptotic effects of progastrin on pancreatic cancer cells are mediated by sustained activation of nuclear factor-κB. Cancer Res 67: 7266-7274, 2007.
49. Sarkar S, Swiercz R, Kantara C, Hajjar KA, Singh P. Annexin A2 mediates up-regulation of NF-κB, β-catenin, and stem cell in response to progastrin in mice and HEK-293 cells. Gastroenterology 140: 583-595, 2011.
50. Sarkar S, Maxwell CA, Luthra G, Singal A, Qiu S, Bauer VP, Okorodudu AO, Singh P. Annexina2 is increasingly expressed and released into the serum of patients positive for colonic growths/tumors in relation to disease progression: diagnostic implications. Gastroenterology 140, Suppl 1: S-341, 2011.
51. Schmid SL. Clathrin-mediated endocytosis: a universe of new questions. Mol Biol Cell 21: 3818-3819, 2010.
52. Sharma M, Ownbey RT, Sharma MC. Breast cancer cell surface annexin II induces cell migration and neoangiogenesis via tPA dependent plasmin generation. Exp Mol Pathol 88: 278-286, 2010.
53. Sharma MC, Sharma M. The role of annexin II in angiogenesis and tumor progression: a potential therapeutic target. Curr Pharm Des 13: 3568-3575, 2007.
54. Shiozawa Y, Havens AM, Jung Y, Ziegler AM, Pedersen EA, Wang J, Wang J, Lu G, Roodman GD, Loberg RD, Pienta KJ, Taichman RS. Annexin II/annexin II receptor axis regulates adhesion, migration, homing, and growth of prostate cancer. J Cell Biochem 105: 370-380, 2008.
55. Siddheshwar RK, Gray JC, Kelly SB. Plasma levels of progastrin but not amidated gastrin or glycine extended gastrin are elevated in patients with colorectal carcinoma. Gut 48: 47-52, 2001.
56. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15: 209-219, 2008.
57. Singh P, Xu Z, Dai B, Rajaraman S, Rubin N, Dhruva B. Incomplete processing of progastrin expressed by human colon cancer cells: role of noncarboxyamidated gastrins. Am J Physiol Gastrointest Liver Physiol 266: G459-G468, 1994.
58. Singh P, Velasco M, Given R, Varro A, Wang TC. Progastrin expression predisposes mice to colon carcinomas and adenomas in response to a chemical carcinogen. Gastroenterology 119: 162-171, 2000.
59. Singh P, Lu X, Cobb S, Miller BT, Tarasova N, Varro A, Owlia A. Progastrin1-80 stimulates growth of intestinal epithelial cells in vitro via high-affinity binding sites. Am J Physiol Gastrointest Liver Physiol 284: G328-G339, 2003.
60. Singh P, Wu H, Clark C, Owlia A. Annexin II binds progastrin and gastrin-like peptides, and mediates growth factor effects of autocrine and exogenous gastrins on colon cancer and intestinal epithelial cells. Oncogene 26: 425-440, 2007.
61. Singh P. Role of annexin-II in GI cancers: interaction with gastrins/ progastrins. Cancer Lett 252: 19-35, 2007.
62. Traub LM. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 10: 583-596, 2009.
63. Umar S, Sarkar S, Cowey S, Singh P. Activation of NF-kappaB is required for mediating proliferative and antiapoptotic effects of progastrin on proximal colonic crypts of mice, in vivo. Oncogene 27: 5599-5611, 2008.
64. Umar S, Sarkar S, Wang Y, Singh P. Functional cross-talk between beta-catenin and NFkappaB signaling pathways in colonic crypts of mice in response to progastrin. J Biol Chem 284: 22274-22284, 2009.
65. Van Solinge WW, Nielsen FC, Friis-Hansen L, Falkmer UG, Rehfeld JF. Expression but incomplete maturation of progastrin in colorectal carcinomas. Gastroenterology 104: 1099-1107, 1993.
66. Valapala M, Vishwanatha JK. Lipid raft endocytosis and exosomal transport facilitate extracellular trafficking of annexin A2. J Biol Chem 286: 30911-30925, 2011.
67. von Zastrow M, Sorkin A. Signaling on the endocytic pathway. Curr Opin Cell Biol 19: 436-445, 2007.
68. Walsh JH. Gastrin. In: Gut Peptides: Biochemistry and Physiology, edited by Walsh JH, Dockray GJ. New York; Raven, 1994.
69. Wang LH, Rothberg KG, Anderson RG. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123: 1107-1117, 1993.
70. Wang TC, Koh TJ, Varro A, Cahill RJ, Dangler CA, Fox JG, Dockray GJ. Processing and proliferative effects of human progastrin in transgenic mice. J Clin Invest 98: 1918-1929, 1996.
71. Wu H, Owlia A, Singh P. Precursor peptide progastrin(1-80) reduces apoptosis of intestinal epithelial cells and upregulates cytochrome c oxidase Vb levels and synthesis of ATP. Am J Physiol Gastrointest Liver Physiol 285: G1097-G1110, 2003.
72. Yeatman TJ, Updyke TV, Kaetzel MA, Dedman JR, Nicolson GL. Expression of annexins on the surfaces of non-metastatic and metastatic human and rodent tumor cells. Clin Exp Metastasis 11: 37-44, 1993.
73. Zhao P, Zhang W, Tang J, Ma XK, Dai JY, Li Y, Jiang JL, Zhang SH, Chen ZN. Annexin II promotes invasion and migration of human hepatocellular carcinoma cells in vitro via its interaction with HAb18G/CD147. Cancer Sci 101: 387-395, 2010.
74. Zheng L, Foley K, Huang L, Leubner A, Mo G, Olino K, Edil BH, Mizuma M, Sharma R, Le DT, Anders RA, Illei PB, Van Eyk JE, Maitra A, Laheru D, Jaffee EM. Tyrosine 23 phosphorylation-dependent cell-surface localization of annexin A2 is required for invasion and metastases of pancreatic cancer. PLos One 6: e19390, 2011.
75. Zobiack N, Rescher U, Ludwig C, Zeuschner D, Gerke V. The annexin 2/S100A10 complex controls the distribution of transferrin receptorcontaining recycling endosomes. Mol Biol Cell 14: 4896-4908, 2003.