N-terminal cleaved pancreatitis-associated protein-III (PAP-III) serves as a scaffold for neurites and promotes neurite outgrowth

Journal of Biological Chemistry

Volumn 288, Issue 15, 2013, Pages 10205-10213

  Konishi, Hiroyuki ^a,b   Matsumoto, Sakiko ^a,b   Namikawa, Kazuhiko ^b,c   Kiyama, Hiroshi ^a,b  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EXTRACELLULAR; FIBRILLAR STRUCTURES; N-TERMINALS; NERVE REGENERATION; NEURITE EXTENSION; NEURITE OUTGROWTH; NEURITES; NOVEL STRATEGIES;

PROTEINS; SCAFFOLDS (BIOLOGY);

NEURONS;

AMINO TERMINAL TELOPEPTIDE; PANCREATITIS ASSOCIATED PROTEIN; PANCREATITIS ASSOCIATED PROTEIN III; SODIUM ION; TRYPTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; FEMALE; GLIA CELL; IN VITRO STUDY; MALE; NERVE FIBER GROWTH; NERVE INJURY; NEURITE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; RAT;

ANIMALS; ANTIGENS, NEOPLASM; AXONS; CELLS, CULTURED; LECTINS, C-TYPE; MALE; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURITES; PROTEOLYSIS; RATS; RATS, WISTAR; SCIATIC NERVE; SODIUM; TUMOR MARKERS, BIOLOGICAL;

EID: 84876217482     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.395301     Document Type: Article

References (42)

1. Keim, V., Iovanna, J. L., Rohr, G., Usadel, K. H., and Dagorn, J. C. (1991) Characterization of a rat pancreatic secretory protein associated with pancreatitis. Gastroenterology 100, 775-782
2. Frigerio, J. M., Dusetti, N. J., Garrido, P., Dagorn, J. C., and Iovanna, J. L. (1993) The pancreatitis-associated protein III (PAP III), a new member of the PAP gene family. Biochim. Biophys. Acta 1216, 329-331
3. Frigerio, J. M., Dusetti, N. J., Keim, V., Dagorn, J. C., and Iovanna, J. L. (1993) Identification of a second rat pancreatitis-associated protein: messenger RNA cloning, gene structure, and expression during acute pancreatitis. Biochemistry 32, 9236-9241
4. Namikawa, K., Fukushima, M., Murakami, K., Suzuki, A., Takasawa, S., Okamoto, H., and Kiyama, H. (2005) Expression of Reg/PAP family members during motor nerve regeneration in rat. Biochem. Biophys. Res. Commun. 332, 126-134
5. Hunt, S. P., Kiyama, H., Smith, A. J. H., and C., L. (2007) Which gene Reg2 or Reg3, was targeted that affected liver regeneration? Reply. Hepatology 45, 1585-1586
6. Gironella, M., Iovanna, J. L., Sans, M., Gil, F., Peñalva, M., Closa, D., Miquel, R., Piqué, J. M., and Panés, J. (2005) Anti-inflammatory effects of pancreatitis-associated protein in inflammatory bowel disease. Gut 54, 1244-1253
7. Algül, H., Treiber, M., Lesina, M., Nakhai, H., Saur, D., Geisler, F., Pfeifer, A., Paxian, S., and Schmid, R. M. (2007) Pancreas-specific RelA/p65 truncation increases susceptibility of acini to inflammation-associated cell death following cerulein pancreatitis. J. Clin. Invest. 117, 1490-1501
8. Gironella, M., Folch-Puy, E., LeGoffic, A., Garcia, S., Christa, L., Smith, A., Tebar, L., Hunt, S. P., Bayne, R., Smith, A. J., Dagorn, J. C., Closa, D., and Iovanna, J. L. (2007) Experimental acute pancreatitis in PAP/HIP knockout mice. Gut 56, 1091-1097
9. Cash, H. L., Whitham, C. V., Behrendt, C. L., and Hooper, L. V. (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313, 1126-1130
10. Brandl, K., Plitas, G., Schnabl, B., DeMatteo, R. P., and Pamer, E. G. (2007) MyD88-mediated signals induce the bactericidal lectin Reg-III, and protect mice against intestinal Listeria monocytogenes infection. J. Exp. Med. 204, 1891-1900
11. Brandl, K., Plitas, G., Mihu, C. N., Ubeda, C., Jia, T., Fleisher, M., Schnabl, B., DeMatteo, R. P., and Pamer, E. G. (2008) Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455, 804-807
12. Vaishnava, S., Yamamoto, M., Severson, K. M., Ruhn, K. A., Yu, X., Koren, O., Ley, R., Wakeland, E. K., and Hooper, L. V. (2011) The antibacterial lectin Reg-III, promotes the spatial segregation of microbiota and host in the intestine. Science 334, 255-258
13. Livesey, F. J., O'Brien, J. A., Li, M., Smith, A. G., Murphy, L. J., and Hunt, S. P. (1997) A Schwann cell mitogen accompanying regeneration of motor neurons. Nature 390, 614-618
14. Averill, S., Davis, D. R., Shortland, P. J., Priestley, J. V., and Hunt, S. P. (2002) Dynamic pattern of reg-2 expression in rat sensory neurons after peripheral nerve injury. J. Neurosci. 22, 7493-7501
15. Tebar, L. A., Géranton, S. M., Parsons-Perez, C., Fisher, A. S., Bayne, R., Smith, A. J., Turmaine, M., Perez-Luz, S., Sheasby, A., De Felipe, C., Ruff, C., Raivich, G., and Hunt, S. P. (2008) Deletion of the mouse Reg-III< (Reg2) gene disrupts ciliary neurotrophic factor signaling and delays myelination of mouse cranial motor neurons. Proc. Natl. Acad. Sci. U.S.A. 105, 11400-11405
16. Ampo, K., Suzuki, A., Konishi, H., and Kiyama, H. (2009) Induction of pancreatitis-associated protein (PAP) family members in neurons after traumatic brain injury. J Neurotrauma 26, 1683-1693
17. Kawahara, S., Konishi, H., Morino, M., Ohata, K., and Kiyama, H. (2011) Pancreatitis-associated protein-I and pancreatitis-associated protein-III expression in a rat model of kainic acid-induced seizure. Neuroscience 175, 273-280
18. März-Weiss, P., Kunz, D., Bimmler, D., Berkemeier, C., Özbek, S., Dimitriades-Schmutz, B., Haybaeck, J., Otten, U., and Graf, R. (2011) Expression of pancreatitis-associated protein after traumatic brain injury: a mechanism potentially contributing to neuroprotection in human brain. Cell. Mol. Neurobiol. 31, 1141-1149
19. Nishimune, H., Vasseur, S., Wiese, S., Birling, M. C., Holtmann, B., Sendtner, M., Iovanna, J. L., and Henderson, C. E. (2000) Reg-2 is a motoneuron neurotrophic factor and a signalling intermediate in the CNTF survival pathway. Nat. Cell Biol. 2, 906-914
20. Fang, M., Huang, J. Y., Ling, S. C., Rudd, J. A., Yew, D. T., and Han, S. (2010) Effects of Reg-2 on survival of spinal cord neurons in vitro. Anat. Rec. 293, 464-476
21. Beuche, W., and Friede, R. L. (1984) The role of nonresident cells in Wallerian degeneration. J. Neurocytol. 13, 767-796
22. Stoll, G., Griffin, J. W., Li, C. Y., and Trapp, B. D. (1989) Wallerian degeneration in the peripheral nervous system: participation of both Schwann cells and macrophages in myelin degradation. J. Neurocytol. 18, 671-683
23. Namikawa, K., Okamoto, T., Suzuki, A., Konishi, H., and Kiyama, H. (2006) Pancreatitis-associated protein-III is a novel macrophage chemoattractant implicated in nerve regeneration. J. Neurosci. 26, 7460-7467
24. Konishi, H., Namikawa, K., and Kiyama, H. (2006) Annexin III implicated in the microglial response to motor nerve injury. Glia 53, 723-732
25. Graf, R., Schiesser, M., Scheele, G. A., Marquardt, K., Frick, T. W., Ammann, R. W., and Bimmler, D. (2001) A family of 16-kDa pancreatic secretory stress proteins form highly organized fibrillar structures upon tryptic activation. J. Biol. Chem. 276, 21028-21038
26. Stahmann, M. A., Tsuyuki, E., and Tsuyuki, H. (1956) The synthesis and enzymatic hydrolysis of poly-D-lysine. J. Biol. Chem. 222, 479-485
27. Kishiro, Y., Kagawa, M., Naito, I., and Sado, Y. (1995) A novel method of preparing rat-monoclonal antibody-producing hybridomas by using rat medial iliac lymph node cells. Cell Struct. Funct. 20, 151-156
28. Ushijima, R., Sakaguchi, N., Kano, A., Maruyama, A., Miyamoto, Y., Sekimoto, T., Yoneda, Y., Ogino, K., and Tachibana, T. (2005) Extracellular signal-dependent nuclear import of STAT3 is mediated by various importin alphas. Biochem. Biophys. Res. Commun. 330, 880-886
29. Maeda, M., Ampo, K., Kiryu-Seo, S., Konishi, H., Ohba, N., Kadono, C., and Kiyama, H. (2005) The p53-independent nuclear translocation of cyclin G1 in degenerating neurons by ischemic and traumatic insults. Exp. Neurol. 193, 350-360
30. Nakanishi, K., Okouchi, Y., Ueki, T., Asai, K., Isobe, I., Eksioglu, Y. Z., Kato, T., Hasegawa, Y., and Kuroda, Y. (1994) Astrocytic contribution to functioning synapse formation estimated by spontaneous neuronal intracellular Ca2, oscillations. Brain Res. 659, 169-178
31. Nakajima, K., Shimojo, M., Hamanoue, M., Ishiura, S., Sugita, H., and Kohsaka, S. (1992) Identification of elastase as a secretory protease from cultured rat microglia. J. Neurochem 58, 1401-1408
32. Matsuoka, I., Meyer, M., and Thoenen, H. (1991) Cell type-specific regulation of nerve growth factor (NGF) synthesis in nonneuronal cells: comparison of Schwann cells with other cell types. J. Neurosci. 11, 3165-3177
33. Schiesser, M., Bimmler, D., Frick, T. W., and Graf, R. (2001) Conformational changes of pancreatitis-associated protein (PAP) activated by trypsin lead to insoluble protein aggregates. Pancreas 22, 186-192
34. Mukherjee, S., Partch, C. L., Lehotzky, R. E., Whitham, C. V., Chu, H., Bevins, C. L., Gardner, K. H., and Hooper, L. V. (2009) Regulation of C-type lectin antimicrobial activity by a flexible N-terminal prosegment. J. Biol. Chem. 284, 4881-4888
35. Medveczky, P., Szmola, R., and Sahin-Tóth, M. (2009) Proteolytic activation of human pancreatitis-associated protein is required for peptidoglycan binding and bacterial aggregation. Biochem. J. 420, 335-343
36. Bödeker, H., Keim, V., Fiedler, F., Dagorn, J. C., and Iovanna, J. L. (1999) PAP I interacts with itself, PAP II, PAP III, and lithostathine/ regI<. Mol. Cell. Biol. Res Commun. 2, 150-154
37. Hassanain, E., Huan, C., Mueller, C. M., Stanek, A., Quan, W., Viterbo, D., Bluth, M. H., and Zenilman, M. E. (2011) Pancreatitis-associated proteins' regulation of inflammation is correlated with their ability to aggregate. Pancreas 40, 1151-1153
38. Ho, M. R., Lou, Y. C., Lin, W. C., Lyu, P. C., Huang, W. N., and Chen, C. (2006) Human pancreatitis-associated protein forms fibrillar aggregates with a native-like conformation. J. Biol. Chem. 281, 33566-33576
39. Acquatella-Tran Van Ba, I., Marchal, S., François, F., Silhol, M., Lleres, C., Michel, B., Benyamin, Y., Verdier, J. M., Trousse, F., and Marcilhac, A. (2012) Regenerating islet-derived 1alpha (Reg-1) protein is new neuronal secreted factor that stimulates neurite outgrowth via exostosin tumor-like 3 (EXTL3) receptor. J. Biol. Chem. 287, 4726-4739
40. Lehotzky, R. E., Partch, C. L., Mukherjee, S., Cash, H. L., Goldman, W. E., Gardner, K. H., and Hooper, L. V. (2010) Molecular basis for peptidoglycan recognition by a bactericidal lectin. Proc. Natl. Acad. Sci. U.S.A. 107, 7722-7727
41. Müller, U., Bossy, B., Venstrom, K., and Reichardt, L. F. (1995) Integrin 8,1 promotes attachment, cell spreading, and neurite outgrowth on fibronectin. Mol. Biol. Cell 6, 433-448
42. Bradshaw, A. D., McNagny, K. M., Gervin, D. B., Cann, G. M., Graf, T., and Clegg, D. O. (1995) Integrin 2,1 mediates interactions between developing embryonic retinal cells and collagen. Development 121, 3593-3602