Recognition-dependent signaling events in response to apoptotic targets inhibit epithelial cell viability by multiple mechanisms: Implications for non-immune tissue homeostasis

Journal of Biological Chemistry

Volumn 287, Issue 17, 2012, Pages 13761-13777

  Patel, Vimal A ^a,b   Feng, Lanfei ^a,b   Lee, Daniel J ^a,b   Massenburg, Donald ^a,b   Pattabiraman, Goutham ^a   Antoni, Angelika ^c   Schwartz, John H ^d   Lieberthal, Wilfred ^e,f   Rauch, Joyce ^g   Ucker, David S ^a   Levine, Jerrold S ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

^c KUTZTOWN UNIVERSITY   (United States)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

^f Northport Veterans Affairs Hospital   (United States)

^g RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC; CELL LINES; ENVIRONMENTAL CHANGE; EPITHELIAL CELLS; LOCAL STRESS; SIGNALING EVENTS; SIGNALING PATHWAYS; TARGET CELLS; TARGET TYPE; TISSUE HOMEOSTASIS;

CELL CULTURE; TISSUE;

CELL DEATH;

BETA CATENIN; CASPASE 8; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAD; PROTEIN KINASE B;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL INTERACTION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TISSUE METABOLISM;

ANIMALS; APOPTOSIS; BETA CATENIN; CELL PROLIFERATION; CELL SURVIVAL; CHO CELLS; CRICETINAE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HELA CELLS; HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; KIDNEY; NECROSIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHAGOCYTES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84860003662     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.350843     Document Type: Article

References (34)

1. Kerr, J. F., Wyllie, A. H., and Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257
2. Majno, G., and Joris, I. (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am. J. Pathol. 146, 3-15
3. Patel, V. A., Longacre, A., Hsiao, K., Fan, H., Meng, F., Mitchell, J. E., Rauch, J., Ucker, D. S., and Levine, J. S. (2006) Apoptotic cells, at all stages of the death process, trigger characteristic signaling events that are divergent from and dominant over those triggered by necrotic cells: implications for the delayed clearance model of autoimmunity. J. Biol. Chem. 281, 4663-4670 (Pubitemid 43847725)
4. Cvetanovic, M., and Ucker, D. S. (2004) Innate immune discrimination of apoptotic cells: repression of proinflammatory macrophage transcription is coupled directly to specific recognition. J. Immunol. 172, 880-889 (Pubitemid 38113745)
5. Reddy, S. M., Hsiao, K. H., Abernethy, V. E., Fan, H., Longacre, A., Lieberthal, W., Rauch, J., Koh, J. S., and Levine, J. S. (2002) Phagocytosis of apoptotic cells by macrophages induces novel signaling events leading to cytokine-independent survival and inhibition of proliferation: activation of Akt and inhibition of extracellular signal-regulated kinases 1 and 2. J. Immunol. 169, 702-713 (Pubitemid 34753425)
6. Cvetanovic, M., Mitchell, J. E., Patel, V., Avner, B. S., Su, Y., van der Saag, P. T., Witte, P. L., Fiore, S., Levine, J. S., and Ucker, D. S. (2006) Specific recognition of apoptotic cells reveals a ubiquitous and unconventional innate immunity. J. Biol. Chem. 281, 20055-20067 (Pubitemid 44065780)
7. Voll, R. E., Herrmann, M., Roth, E. A., Stach, C., Kalden, J. R., and Girkontaite, I. (1997) Immunosuppressive effects of apoptotic cells. Nature 390, 350-351
8. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., and Henson, P. M. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Investig. 101, 890-898 (Pubitemid 28096086)
9. McDonald, P. P., Fadok, V. A., Bratton, D., and Henson, P. M. (1999) Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-β in macrophages that have ingested apoptotic cells. J. Immunol. 163, 6164-6172
10. Huynh, M. L., Fadok, V. A., and Henson, P. M. (2002) Phosphatidylserinedependent ingestion of apoptotic cells promotes TGF-β1 secretion and the resolution of inflammation. J. Clin. Investig. 109, 41-50 (Pubitemid 34052540)
11. Freire-de-Lima, C. G., Xiao, Y. Q., Gardai, S. J., Bratton, D. L., Schiemann, W. P., and Henson, P. M. (2006) Apoptotic cells, through transforming growth factor-β, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. J. Biol. Chem. 281, 38376-38384 (Pubitemid 46041961)
12. Cocco, R. E., and Ucker, D. S. (2001) Distinct modes of macrophage recognition for apoptotic and necrotic cells are not specified exclusively by phosphatidylserine exposure. Mol. Biol. Cell 12, 919-930 (Pubitemid 33051988)
13. Albert, M. L., Pearce, S. F., Francisco, L. M., Sauter, B., Roy, P., Silverstein, R. L., and Bhardwaj, N. (1998) Immature dendritic cells phagocytose apoptotic cells via αvβ5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med. 188, 1359-1368 (Pubitemid 28478024)
14. Bellone, M., Iezzi, G., Rovere, P., Galati, G., Ronchetti, A., Protti, M. P., Davoust, J., Rugarli, C., and Manfredi, A. A. (1997) Processing of engulfed apoptotic bodies yields T cell epitopes. J. Immunol. 159, 5391-5399 (Pubitemid 127470066)
15. Skoberne, M., Beignon, A. S., Larsson, M., and Bhardwaj, N. (2005) Apoptotic cells at the crossroads of tolerance and immunity. Curr. Top. Microbiol. Immunol. 289, 259-292 (Pubitemid 40283467)
16. Muñoz, L. E., Peter, C., Herrmann, M., Wesselborg, S., and Lauber, K. (2010) Scent of dying cells: the role of attraction signals in the clearance of apoptotic cells and its immunological consequences. Autoimmun. Rev. 9, 425-430
17. Patel, V. A., Lee, D. J., Feng, L., Antoni, A., Lieberthal, W., Schwartz, J. H., Rauch, J., Ucker, D. S., and Levine, J. S. (2010) Recognition of apoptotic cells by epithelial cells: conserved versus tissue-specific signaling responses. J. Biol. Chem. 285, 1829-1840
18. Patel, V. A., Longacre-Antoni, A., Cvetanovic, M., Lee, D. J., Feng, L., Fan, H., Rauch, J., Ucker, D. S., and Levine, J. S. (2007) The affirmative response of the innate immune system to apoptotic cells. Autoimmunity 40, 274-280 (Pubitemid 46845520)
19. Patel, V. A., Lee, D. J., Longacre-Antoni, A., Feng, L., Lieberthal, W., Rauch, J., Ucker, D. S., and Levine, J. S. (2009) Apoptotic and necrotic cells as sentinels of local tissue stress and inflammation: response pathways initiated in nearby viable cells. Autoimmunity 42, 317-321
20. Sinha, D., Wang, Z., Price, V. R., Schwartz, J. H., and Lieberthal, W. (2003) Chemical anoxia of tubular cells induces activation of c-Src and its translocation to the zonula adherens. Am. J. Physiol. Renal Physiol. 284, F488-F497 (Pubitemid 36227909)
21. Sinha, D., Wang, Z., Ruchalski, K. L., Levine, J. S., Krishnan, S., Lieberthal, W., Schwartz, J. H., and Borkan, S. C. (2005) Lithium activates the Wnt and phosphatidylinositol 3-kinase Akt signaling pathways to promote cell survival in the absence of soluble survival factors. Am. J. Physiol. Renal Physiol. 288, F703-F713 (Pubitemid 40381737)
22. Jat, P. S., Noble, M. D., Ataliotis, P., Tanaka, Y., Yannoutsos, N., Larsen, L., and Kioussis, D. (1991) Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc. Natl. Acad. Sci. U.S.A. 88, 5096-5100 (Pubitemid 21914690)
23. Kennedy, S. G., Wagner, A. J., Conzen, S. D., Jordán, J., Bellacosa, A., Tsichlis, P. N., and Hay, N. (1997) The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 11, 701-713 (Pubitemid 27157159)
24. Eves, E. M., Xiong, W., Bellacosa, A., Kennedy, S. G., Tsichlis, P. N., Rosner, M. R., and Hay, N. (1998) Akt, a target of phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neuronal cell line. Mol. Cell. Biol. 18, 2143-2152 (Pubitemid 28152663)
25. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63
26. Lieberthal, W., Menza, S. A., and Levine, J. S. (1998) Graded ATP depletion can cause necrosis or apoptosis of cultured mouse proximal tubular cells. Am. J. Physiol. Renal Physiol. 274, F315-F327
27. Lieberthal, W., Zhang, L., Patel, V. A., and Levine, J. S. (2011) AMPK protects proximal tubular cells from stress-induced apoptosis by an ATP-independent mechanism: potential role of Akt activation. Am. J. Physiol. Renal Physiol. 301, F1177-F1192
28. Doble, B. W., and Woodgett, J. R. (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116, 1175-1186 (Pubitemid 36410657)
29. Thornton, T. M., Pedraza-Alva, G., Deng, B., Wood, C. D., Aronshtam, A., Clements, J. L., Sabio, G., Davis, R. J., Matthews, D. E., Doble, B., and Rincon, M. (2008) Phosphorylation by p38 MAPK as an alternative pathway for GSK3β inactivation. Science 320, 667-670 (Pubitemid 351928349)
30. Wang, Z., Havasi, A., Gall, J. M., Mao, H., Schwartz, J. H., and Borkan, S. C. (2009) β-Catenin promotes survival of renal epithelial cells by inhibiting Bax. J. Am. Soc. Nephrol. 20, 1919-1928
31. Safirstein, R. L. (2011) Am I my brother's keeper?: fratricide in the kidney. Kidney Int. 79, 149-150
32. Tan, K. H., and Hunziker, W. (2003) Compartmentalization of Fas and Fas ligand may prevent auto- or paracrine apoptosis in epithelial cells. Exp. Cell Res. 284, 283-290
33. Liu, M., Chien, C. C., Burne-Taney, M., Molls, R. R., Racusen, L. C., Colvin, R. B., and Rabb, H. (2006) A pathophysiologic role for T lymphocytes in murine acute cisplatin nephrotoxicity. J. Am. Soc. Nephrol. 17, 765-774
34. Linkermann, A., Himmerkus, N., Rölver, L., Keyser, K. A., Steen, P., Bräsen, J. H., Bleich, M., Kunzendorf, U., and Krautwald, S. (2011) Renal tubular Fas ligand mediates fratricide in cisplatin-induced acute kidney failure. Kidney Int. 79, 169-178